Federal Register, Volume 89 Issue 152 (Wednesday, August 7, 2024)

[Federal Register Volume 89, Number 152 (Wednesday, August 7, 2024)]
[Proposed Rules]
[Pages 64678-64748]
From the Federal Register Online via the Government Publishing Office [www.gpo.gov]
[FR Doc No: 2024-16963]

[[Page 64677]]

Vol. 89

Wednesday,

No. 152

August 7, 2024

Part IV

Department of Agriculture

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Food Safety and Inspection Service

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9 CFR Part 381

Salmonella Framework for Raw Poultry Products; Proposed Rule

Federal Register / Vol. 89, No. 152 / Wednesday, August 7, 2024 /
Proposed Rules

[[Page 64678]]

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DEPARTMENT OF AGRICULTURE

Food Safety and Inspection Service

9 CFR Part 381

[Docket No. FSIS-2023-0028]
RIN 0583-AD96

Salmonella Framework for Raw Poultry Products

AGENCY: Food Safety and Inspection Service (FSIS), U.S. Department of
Agriculture (USDA).

ACTION: Proposed rule and Proposed Determination.

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SUMMARY: FSIS is announcing its proposed determination that raw chicken
carcasses, chicken parts, comminuted chicken, and comminuted turkey
products contaminated with certain Salmonella levels and serotypes are
adulterated within the meaning of the Poultry Products Inspection Act
(PPIA). The proposed determination would establish final product
standards based on these Salmonella levels and serotypes and would
prevent raw chicken carcasses, chicken parts, comminuted chicken, and
comminuted turkey products that contain Salmonella at the levels and
serotypes that would render them adulterated from entering commerce.
FSIS is also proposing to revise the regulations that require that all
poultry slaughter establishments develop, implement, and maintain
written procedures to prevent contamination by enteric pathogens
throughout the entire slaughter and dressing operation to clarify that
these procedures must include a microbial monitoring program (MMP) that
incorporates statistical process control (SPC) monitoring methods, to
require sampling at rehang instead of pre-chill, and to require that
all establishments conduct paired sampling at rehang and post-chill.

DATES: Comments on this proposal must be received on or before October
7, 2024.

ADDRESSES: FSIS invites interested persons to submit comments on this
document. Comments may be submitted by one of the following methods:
Federal eRulemaking Portal: This website provides the
ability to type short comments directly into the comment field on this
web page or attach a file for lengthier comments. Go to: https://www.regulations.gov. Follow the on-line instructions at that site for
submitting comments.
Mail: Send to Docket Clerk, U.S. Department of
Agriculture, Food Safety and Inspection Service, 1400 Independence
Avenue SW, Mailstop 3758, Washington, DC 20250-3700.
Hand- or courier-delivered submittals: Deliver to 1400
Independence Avenue SW, Jamie L. Whitten Building, Room 350-E,
Washington, DC 20250-3700.
Instructions: All items submitted by mail or electronic mail must
include the Agency name and docket number FSIS-2023-0028. Comments
received in response to this docket will be made available for public
inspection and posted without change, including any personal
information, to https://www.regulations.gov.
Docket: Go to the Federal eRulemaking Portal at https://www.regulations.gov for access to the rulemaking docket, including any
background documents and the plain-language summary of the proposed
rule of not more than 100 words in length required by the Providing
Accountability Through Transparency Act of 2023. For in-person access
to background documents or comments received, call (202) 720-5046 to
schedule a time to visit the FSIS Docket Room at 1400 Independence
Avenue SW, Washington, DC 20250-3700.

FOR FURTHER INFORMATION CONTACT: Rachel Edelstein, Assistant
Administrator, Office of Policy and Program Development, FSIS, USDA;
Telephone: (202) 205-0495.

SUPPLEMENTARY INFORMATION:

Executive Summary

FSIS is responsible for verifying that the nation's commercial
supply of meat, poultry, and egg products is safe, wholesome, and
properly labeled. In support of this mission, FSIS established a
Salmonella verification testing program in 1996 as part of the
``Pathogen Reduction; Hazard Analysis and Critical Control Point
Systems'' (PR/HACCP) final rule (61 FR 38805). Among other things, the
PR/HACCP final rule established Salmonella pathogen reduction
performance standards for raw product to allow FSIS to verify whether
establishments have effective process controls to address Salmonella.
The current performance standards for young chicken and turkey
carcasses, raw chicken parts, and comminuted chicken and turkey
products are represented as a fraction of the maximum number of
allowable Salmonella-positive results over a targeted number of samples
collected and analyzed in a 52-week moving window. FSIS categorizes
establishments based on the Salmonella verification sampling results
and posts the performance categorization of all establishments subject
to the performance standards on the FSIS website. FSIS uses Salmonella
performance standard categorization as a basis to prioritize in-depth
evaluations of failing establishments' food safety systems, including
their HACCP plan and sanitation Standard Operating Procedures (SOPs).
While the results of FSIS' Salmonella verification sampling show
that the current prevalence-based performance standards approach has
been effective in reducing the proportion of poultry products
contaminated with Salmonella, these measures have yet to have an
observable impact on human illness rates. The estimated rate of human
Salmonella infections from all sources has remained consistent over the
last two decades, with over 1.3 million illnesses estimated in the
United States each year. Additionally, while current Salmonella
performance standards are designed to achieve the Department of Health
and Human Services' Healthy People Initiative \1\ targets for foodborne
illness reduction, the 2010 and 2020 Healthy People targets for a
reduction in Salmonella infections from all sources were not met. The
Healthy People 2030 target is to reduce Salmonella infections from all
sources to a national case rate of no more than 11.5 per 100,000
consumers per year. To reach this 2030 target, Salmonella illnesses
must be reduced by 25 percent.
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\1\ Launched by the U.S. Department of Health and Human Services
(HHS) in 1980, the Healthy People Initiative sets out to create
widely accessible plans to help organizations, communities and
individuals improve public health. Each decade, HHS releases new
goals after evaluating the successes and areas of growth from the
previous ten years. They monitor the progress toward Healthy
People's objectives using high-quality data and feedback., the HHS
benchmark continues to focus on reducing poultry-based Salmonella
infections by 25 percent, a goal that has not been reached over the
last decade. The Healthy People 2030 objectives were released on
August 18, 2020.
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Poultry is among the leading sources of Salmonella foodborne
illness acquired domestically in the United States.\2\ Therefore, on
October 19, 2021, FSIS announced that it was mobilizing a stronger, and
more comprehensive effort to reduce Salmonella illnesses associated
with poultry products. In the

[[Page 64679]]

announcement, FSIS stated that it had initiated several activities
designed to gather data and information to inform and support future
actions related to this new effort. FSIS charged the National Committee
on Microbiological Criteria for Food (NACMCF) to provide guidance on
the types of microbiological criteria the Agency might use to better
prevent Salmonella infections associated with poultry products. The
Agency also conducted a risk profile for pathogenic Salmonella subtypes
in poultry and developed two quantitative risk assessments --one for
Salmonella in chicken and one for Salmonella in turkey. Additionally,
FSIS conducted an exploratory sampling program for young chicken
carcasses to generate microbial data to help inform future policies and
added quantification to its Salmonella testing program.
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\2\ Interagency Food Safety Analytics Collaboration (FSAC).
Foodborne illness source attribution estimates for 2020 for
Salmonella, Escherichia coli O157, and Listeria monocytogenes using
multi-year outbreak surveillance data, United States. GA and DC:
U.S. Department of Health and Human Services, Centers for Disease
Control and Prevention, Food and Drug Administration, U.S.
Department of Agriculture's Food Safety and Inspection Service.
2022. Available at: https://www.cdc.gov/ifsac/php/annual-reports/?CDC_AAref_Val=https://www.cdc.gov/foodsafety/ifsac/annual-reports.html.
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In addition to initiating these activities, on October 17, 2022,
FSIS shared with stakeholders a draft regulatory framework that the
Agency was considering for a new strategy to control Salmonella in
poultry products and announced that FSIS would be hosting a virtual
public meeting on November 3, 2022, to discuss the framework. The three
components under consideration in the draft framework included:
Component One. Requiring that establishments characterize
Salmonella as a hazard reasonably likely to occur at receiving and
requiring that incoming flocks be tested for Salmonella before entering
an establishment.
Component Two. Enhancing establishment process control monitoring
and FSIS verification.
Component Three. Implementing an enforceable final product standard
that would define whether certain raw poultry products contaminated
with certain levels and/or serotypes of Salmonella are adulterated.
The draft framework under consideration also addressed cross-
cutting issues associated with testing for Salmonella, considerations
for small and very small establishments, and data sharing. At the
November 2022 public meeting, stakeholders presented oral comments on
the three separate components of the draft framework and the cross-
cutting issues. Stakeholders also had an opportunity to submit written
comments to FSIS by December 16, 2022.
After carefully evaluating the written comments and other
stakeholder input provided on the October 2022 draft framework, along
with new studies and information that have become available since the
Agency made the October 2022 draft framework available to the public,
FSIS is proposing a new regulatory framework targeted at reducing
Salmonella illnesses associated with poultry products. The proposed
regulatory framework reflects the draft framework with some
modifications.
First, consistent with Component Three of the October 2022 draft
framework, FSIS is proposing final product standards that would define
whether certain raw poultry products contaminated with certain
Salmonella levels and serotypes are adulterated as defined in the
Poultry Products Inspection Act (PPIA) (21 U.S.C. 451 et seq.).
Specifically, FSIS has tentatively determined that raw chicken
carcasses, chicken parts, comminuted chicken, and comminuted turkey are
adulterated if they contain any type of Salmonella at or above 10
colony forming units/per milliliter or gram (10 cfu/mL(g)) in
analytical portion (i.e., mL of rinsate or gram of product) and contain
any detectable level of at least one of the Salmonella serotypes of
public health significance identified for that commodity. The proposed
Salmonella serotypes of public health significance identified for raw
chicken carcasses, chicken parts, and comminuted chicken are
Enteritidis, Typhimurium, and I 4,[5],12:i:-, and for raw comminuted
turkey are Hadar, Typhimurium, and Muenchen. These are the most highly
virulent Salmonella serotypes associated with these products identified
in the FSIS chicken and turkey risk assessments.
The Salmonella serotypes of public health significance will likely
change over time as the serotypes commonly associated with human
illnesses change. FSIS would continue to track annual targets for
reducing the proportion of poultry samples that contain Salmonella
serotypes of public health significance as well as data on rates for
additional serotypes commonly associated with human illness to inform
future revisions to the Salmonella serotypes of public health
significance. Should FSIS finalize the proposed final product
standards, the Agency intends to further evaluate and, if necessary,
refine these standards as advances in science and technology related to
pathogen levels, serotypes, and virulence genes become available. If
FSIS finalizes the proposed final product standards, the Agency intends
to re-evaluate the serotypes of public health concern every 3-5 years
at a minimum and whenever new information on Salmonella serotypes
associated with human illness become available. When evaluating the
serotypes, FSIS would consider, among other things, outbreak illness
data, foodborne illness surveillance data, product testing data, and
animal testing data. FSIS would publicly announce any modifications to
the final products standards in the Federal Register. FSIS requests
comments on this proposed timeline for re-evaluating serotypes of
public health concern.
Should FSIS finalize these proposed standards, the Agency intends
to conduct a routine sampling and verification testing program for
Salmonella in chicken carcasses, chicken parts, comminuted chicken, and
comminuted turkey in which the Agency would collect samples of raw
final products and analyze them for Salmonella levels and serotypes to
determine whether the final product is adulterated. Under the proposed
Salmonella verification testing program, FSIS intends to only collect
and analyze samples of the final raw poultry products produced by an
establishment, i.e., chicken carcasses to be shipped in commerce as
whole chickens, chicken parts to be shipped in commerce as chicken
parts, comminuted chicken to be shipped in commerce as comminuted
chicken products, and comminuted turkey to be shipped in commerce as
comminuted turkey products. Under this proposed determination, chicken
parts subject to the final product standards would include legs,
thighs, breasts, wings, quarters, and halves.
When FSIS tests a product sample for adulterants, establishments
must maintain control of products tested for adulterants to ensure that
the products do not enter commerce while waiting for receipt of the
test results. Thus, if FSIS finalizes its proposed routine Salmonella
verification testing program for chicken carcasses, chicken parts,
comminuted chicken, and comminuted turkey, establishments that produce
these raw products would need to control and maintain the integrity of
the sampled lot pending the availability of test results. If test
results detect Salmonella at a level of 10 cfu/mL(g) or higher and at
least one Salmonella serotype of public health significance, FSIS would
consider products represented by the sampled lots to be adulterated and
would issue a non-compliance record (NR). Therefore, all products in
the lot represented by the sample would be prohibited from entering
commerce. If any product from the lot represented by the product
samples has entered and remains available in commerce, FSIS would
request that the producing establishment recall the implicated
products. Depending on the circumstances, in addition to issuing an NR,
FSIS could take other appropriate

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enforcement action as authorized in 9 CFR part 500 because the
establishment would have produced and shipped adulterated product. Such
actions may include immediately suspending inspection or issuing a
Notice of Intended Enforcement (NOIE).
As FSIS implements the final product standards verification
sampling program, the Agency has tentatively decided to phase out all
current Salmonella performance standards for poultry. Thus, when the
proposed final product verification sampling program is fully
implemented, FSIS has tentatively decided that it would no longer use
Salmonella sampling results to categorize establishments that produce
poultry products and would no longer publish these establishments'
performance standards categories on the FSIS website. The Agency is
requesting comments on this issue.
Consistent with Component Two of the initial proposed framework,
FSIS is proposing to revise the regulations in 9 CFR 381.65(g) and (h)
that require that all poultry slaughter establishments develop,
implement, and maintain written procedures to prevent contamination by
enteric pathogens throughout the entire slaughter and dressing
operation and maintain records documenting those procedures. FSIS is
proposing to amend these regulations to establish new requirements
pertaining to how establishments monitor and document whether their
processes for preventing microbial contamination are in control. The
proposed revisions are intended to clarify existing regulatory
requirements related to process control monitoring in 9 CFR 381.65(g)
and (h).
Under this proposal, establishments would be required to
incorporate statistical process control (SPC) monitoring principles
into their microbial monitoring programs (MMPs). The proposed revisions
would require that establishments use only validated and fit for
purpose microbial sampling and analysis procedures, generate and record
statistically meaningful microbial monitoring data, set benchmarks by
which to evaluate microbial monitoring data, and otherwise define the
statistical methods the establishment will use to evaluate the recorded
data against the predefined limits. To offset the costs associated with
this proposal, eligible very small (VS) and very low volume (VLV)
establishments would have access to laboratory services provided by
FSIS at no charge to analyze the establishments' microbial monitoring
samples for them.
FSIS is further proposing to revise the regulations to ensure that
establishments comply with the corrective action provisions required
under HACCP as they apply to the establishment's MMP. FSIS is proposing
to specifically require establishments to, at a minimum, implement
written corrective actions, including a root cause assessment, when
microbial monitoring results deviate from the predefined criteria in
the MMP, the other process control monitoring results, or the process
control determination made for the entire HACCP system.
FSIS has developed new guidance to help establishments meet the
proposed updated sampling and analysis requirements under 9 CFR
381.65(g). The new guidance includes a SPC sampling plan based on
paired sampling for Aerobic Count (AC) at the rehang and post-chill
locations, with a one-sided process control statistical model that
charts and calculates against minimum monitoring criteria at the
minimum required frequency. Establishments that incorporate the
guidance into their MMPs would not be required to provide FSIS with
additional scientific or technical information to support their chosen
statistical methods. FSIS also is proposing to make available to all
poultry slaughter establishments an electronic spreadsheet file that is
pre-programmed to calculate the monitoring measures for the guidance
sampling plan as results are entered.
In addition, FSIS is proposing to amend the recordkeeping
requirements under 9 CFR 381.65(h) to require that establishments
submit their microbial monitoring sampling results to FSIS
electronically. FSIS is developing a web portal that will allow
external partners to securely upload sampling information and submit it
to FSIS electronically in a machine-readable format.\3\ Should FSIS
finalize this proposal, the Agency would provide a template that
establishments could use to record and submit their monthly results.
Establishments that use the template to record the microbial monitoring
results may upload their completed template into the portal or they may
enter the information manually into the portal. Establishments that do
not use the template provided by FSIS to record their results would
need to manually enter microbial sampling data into the portal to
submit the monthly data.
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\3\ In a format that provides a digital representation of data
or information that can be imported and read into a computer system
for further processing.
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Under Component One of the October 2022 draft framework, FSIS
considered whether it should require poultry slaughter establishments
to characterize Salmonella as a hazard reasonably likely to occur at
receiving and require that incoming flocks be tested for Salmonella
before entering an establishment. This approach would require the flock
to meet a predetermined target level for Salmonella at receiving.
FSIS considered the available scientific research as well as input
from the NACMCF and concluded that, at this time, the research does not
support the use of a threshold for test results at the receiving step
to reduce or eliminate Salmonella from raw poultry products. In
addition, FSIS received several comments from small poultry processors
and producers and trade associations representing the meat and poultry
industries that expressed concerns that the measures under
consideration in Component One would impose an overwhelming burden on
small producers and processors. The comments also stated that requiring
that establishments determine that Salmonella is a hazard reasonably
likely to occur at receiving is inconsistent with HACCP principles.
While FSIS has decided at this time not to establish a regulatory
requirement that establishments characterize Salmonella as a hazard
reasonably likely to occur at receiving or that incoming flocks be
tested for Salmonella before entering an establishment, the Agency is
focusing on a non-regulatory approach for reducing the Salmonella load
on incoming birds. The Agency intends to provide updated guidance on
pre-harvest interventions and practices for preventing or reducing
Salmonella colonization of live birds. The Agency also will continue to
explore and develop strategies for industry to address Salmonella
contamination risk at receiving.

Costs and Benefits of the Proposed Rule and Proposed Determination

FSIS estimates this proposal would have a net benefit of $4.1
million per year, ranging from $1.1 million to $6.7 million, assuming
the proposed implementation schedule and annualizing over 10 years at a
7 percent discount rate, as discussed below (Table 1). This proposal is
estimated to cost industry $16.4 million per year, ranging from $3.3 to
$32.3 million. The main cost component in this proposal is the
requirement that establishments subject to FSIS verification sampling
for adulterants maintain control of sampled product pending test
results. This cost is likely an overestimate as discussed below.
Industry may also incur costs associated with HACCP plan

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reassessments and changes to process control requirements.
FSIS estimates this proposal would result in benefits to society of
$20.5 million per year, ranging from $4.4 million to $39.0 million. The
majority of the benefits are derived from prevented illnesses of $12.9
million per year, ranging from $0.3 to $28.7 million. FSIS also
estimated avoided costs from a reduction in the risk of outbreak-
related recalls for industry. Additional industry actions in response
to this proposal may lead to additional benefits.

Table 1--Summary of Costs and Benefits
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Total (million $)
Description -----------------------------------------------
Low Medium High
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Costs:
Costs associated with the proposed rule:
Statistical Process Control................................. 0.04 0.04 0.04
Electronic data submission.................................. 0.18 0.18 0.18
HACCP plan reassessment..................................... 0.09 0.18 0.26
Costs associated with the proposed determination:
Maintaining control of sampled product...................... 2.11 14.47 29.26
Lost value to the industry.................................. 0.87 1.52 2.43
Microbiological sampling plan reassessment.................. 0.02 0.04 0.08
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Total costs............................................. 3.31 16.43 32.25
Benefits and Avoided Costs:
Prevented illnesses from consumption of chicken products.... 0.09 4.35 15.11
Prevented illnesses from consumption of comminuted turkey... 0.19 8.58 13.55
Prevented outbreak-related recalls.......................... 4.16 7.56 10.34
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Total benefits.......................................... 4.45 20.49 39.00
Net benefits........................................ 1.14 4.06 6.75
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Note: All costs and benefits are annualized over 10 years at a 7 percent discount rate. Numbers in table may not
sum to totals due to rounding.

Table of Contents

I. Background
A. Salmonella in Poultry and Human Illnesses
1. Salmonella Illnesses Attributed to Poultry
2. Salmonella Performance Standards for Poultry
3. Salmonella Performance Standards and Illnesses
B. Consideration of Need for a New Framework To Control
Salmonella in Poultry
1. Petitions and Initial Stakeholder Input
2. FSIS Announces New Salmonella Effort
3. Activities Initiated To Support a New Salmonella Framework
4. Initial Measures Implemented To Address Salmonella Illnesses
Associated With Consumption of Poultry Products
C. Public Meeting on Salmonella Framework Under Consideration
and Public Comments
1. Public Meeting and Proposed Framework
2. Public Comments on the Proposed Framework
3. Additional Stakeholder Input
4. Overview of Modifications to the Proposed Salmonella
Framework
5. Severability
II. Component Three: Proposed Final Product Standards
A. Current Salmonella Performance Standards and Consideration of
an Alternative Approach
B. Pathogens as Adulterants in Raw and Not-Ready-To Eat Meat and
Poultry Products
C. The Adulteration Standard for Raw Poultry Products
1. Pathogen Serogroups or Types Associated With Human Illness
2. Dose Considerations
3. Severity of Illnesses
4. Consumer Cooking Practices
E. Risk per Serving, Salmonella Levels, and Proposed
Determination
1. Final Product Standards Salmonella Levels and Risk per
Serving
2. Proposed Determination
F. Proposed Policy Implementation
1. HACCP Reassessment
2. Proposed Implementation and Status of Laboratory Methods
III. Component Two: Enhanced Establishment Process Control
Monitoring
A. Background and Current Regulatory Requirements
B. Need To Enhance Establishment Process Control Monitoring
1. NACMCF Charge and Recommendations
2. PHIS Inspection Data
3. Exploratory Sampling Program Data
4. FSIS Risk Assessments
C. Proposals To Enhance Establishment Process Control Monitoring
1. SPC Monitoring
2. Microbial Monitoring Organism
3. Sampling Location
4. Sample Collection Monitoring Frequency
5. Corrective Actions
6. Recordkeeping Requirements
IV. Component One: Pre-Harvest Measures
A. Scientific Support and Public Comments
B. Possible Approaches To Control Salmonella at Pre-Harvest
1. National Poultry Improvement Program
2. Vaccination
3. Supply Chain Control Programs
4. Updated Pre-Harvest Guidance
V. State Programs and Foreign Government Programs
VI. Executive Orders 12866, as Amended by 14094, and 13563
VII. Regulatory Flexibility Act Assessment
VIII. Paperwork Reduction Act
IX. E-Government Act
X. Executive Order 12988, Civil Justice Reform
XI. E.O. 13175
XII. USDA Non-Discrimination Statement
XIII. Environmental Impact
XIV. Additional Public Notification

I. Background

A. Salmonella in Poultry and Human Illnesses

1. Salmonella Illnesses Attributed to Poultry
Salmonella in poultry is a significant food safety and public
health concern. The Centers for Disease Control and Prevention (CDC)
estimates that non-typhoidal Salmonella from all sources is responsible
for over 1.3 million illnesses, 26,500 hospitalized, and 420 deaths
each year in the United States.\4\ From this overall number, FSIS
estimates that there are 125,115 chicken-associated and 42,669 turkey-
associated foodborne Salmonella illnesses per year. These values are

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calculated as the product of the total number of CDC FoodNet cases per
year (7,600),\5\ the share of these cases that are foodborne (66
percent) \6\ and of domestic origin (89 percent),\7\ and the under-
diagnosis multiplier for Salmonella (24.3),\8\ then dividing by the
FoodNet catchment area (15 percent).\9\ Finally, this number is
multiplied by the portion the Interagency Food Safety Analytics
Collaboration (IFSAC) estimates is attributable to chicken (17.3
percent) or turkey (5.9 percent).\10\ Uncertainty remains in the FSIS
estimation of chicken- and turkey-associated foodborne Salmonella
illnesses per year. These illness estimates are subject to the same
limitations encountered with other illness estimates.\11\ Nevertheless,
FSIS believes these are the best available estimates.
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\4\ Collier SA, Deng L, Adam EA, et al. Estimate of Burden and
Direct Healthcare Cost of Infectious Waterborne Disease in the
United States. Emerging Infectious Diseases. 2021;27(1):140-149.
https://doi.org/10.3201%2Feid2701.190676.
\5\ Collins JP, Shah HJ, Weller DL, et al. Preliminary Incidence
and Trends of Infections Caused by Pathogens Transmitted Commonly
Through Food--Foodborne Diseases Active Surveillance Network, 10
U.S. Sites, 2016-2021. MMWR Morb Mortal Wkly Rep 2022;71:1260-1264.
DOI: https://doi.org/10.15585/mmwr.mm7140a2. Note: the most recent
annual FoodNet report was used for the total estimated FoodNet cases
annually.
\6\ Beshearse E, Bruce BB, Nane GF, Cooke RM, Aspinall W, Hald
T, et al. Attribution of Illnesses Transmitted by Food and Water to
Comprehensive Transmission Pathways Using Structured Expert
Judgment, United, States. Emerg Infect Dis. 2021;27(1):182-195.
https://doi.org/10.3201/eid2701.200316. Note: This article
represented a recent appraisal of the foodborne share of all
Salmonella illnesses.
\7\ Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA,
Roy SL, Jones JL, Griffin PM. Foodborne illness acquired in the
United States--major pathogens. Emerg Infect Dis. 2011 Jan;17(1):7-
15. doi: 10.3201/eid1701.p11101. PMID: 21192848; PMCID: PMC3375761.
Note: This article outlines the general approach to estimating the
burden of domestic foodborne illnesses. It provides an estimate for
share of foodborne illnesses associated with foreign travel (11%)
that was supported in the more recent Collins et al. (2022) article
referenced above.
\8\ Ebel, E.D., Williams, M.S., & Schlosser, W.D. (2012).
Parametric distributions of underdiagnosis parameters used to
estimate annual burden of illness for five foodborne pathogens. J
Food Prot, 75, 775-778. https://doi.org/10.4315/0362-028X.JFP-11-345. Note: This article estimated parametric distributions for
uncertainty about the under-diagnosis multiplier based on the
Scallan et al. (2011) model assumptions.
\9\ Scallan et al. (2011).
\10\ Interagency Food Safety Analytics Collaboration. Foodborne
illness source attribution estimates for 2020 for Salmonella,
Escherichia coli O157, and Listeria monocytogenes using multi-year
outbreak surveillance data, United States. GA and DC: U.S.
Department of Health and Human Services, Centers for Disease Control
and Prevention, Food and Drug Administration, U.S. Department of
Agriculture's Food Safety and Inspection Service. 2022. Annually,
IFSAC releases a report that estimates foodborne illness source
attribution for major commodity groups, including Salmonella in
poultry products. At the time this proposal was developed, the 2019
IFSAC attribution estimates were the most recent data available.
IFSAC released a new annual report in November 2023, which includes
attribution estimates for 2020. In the 2023 report, IFSAC estimated
that 18.6 percent of Salmonella illnesses are attributed to chicken
products and 5.5 percent to turkey products, for a total 24.1
percent attributed to poultry products. FSIS intends to incorporate
the 2023 report attribution estimates if this rule becomes final.
\11\ Illness estimates from any risk assessment model are
limited by uncertainty, simply because they are models. As explained
by Food and Agriculture Organization of the World Health
Organization (FAO/WHO), ``uncertainty is a property of the
methodology and data used. Assessments with different methodologies
and data will have different levels of uncertainty regarding their
outputs. An understanding of uncertainty is important because it
provides insight into how the lack of knowledge can affect
decisions.'' See FAO/WHO Microbiological Risk Assessment Guidance
for Food (MRA 36) at 206. FAO/WHO goes on to say, ``It is the risk
managers' role to decide if the uncertainty of a risk assessment
output allows for a decision to be made or not.'' Id. FSIS fully
explored uncertainty in its risk assessment models to allow risk
managers to make a fully informed decision. Full details are on
pages 116-128 of the chicken risk assessment and pages 94-99 of the
turkey risk assessment. The code for these analyses has also been
provided.
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Salmonella illnesses associated with poultry also represent a
considerable economic burden, particularly when accounting for not just
the direct medical costs, but also productivity losses, lost life
expectancy, chronic illness, and other associated pain and suffering. A
recent study estimates that the economic costs of Salmonella illnesses
in the United States associated with chicken is $2.8 billion
annually.\12\
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\12\ Scharff R.L. Food Attribution and Economic Cost Estimates
for Meat and Poultry-Related Illnesses. Journal of Food Protection.
2020; 83(6): 959-967.
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2. Salmonella Performance Standards for Poultry
FSIS is responsible for verifying that the nation's commercial
supply of meat, poultry, and egg products is safe, wholesome, and
properly labeled. In support of this mission, FSIS began its Salmonella
verification testing program with the PR/HACCP final rule, published on
July 25, 1996 (61 FR 38806). Among other things, the PR/HACCP final
rule established Salmonella pathogen reduction performance standards
for establishments that slaughter selected classes of food animals and/
or that produce selected classes of raw ground products.\13\ The
purpose of the Salmonella performance standards for raw product is to
allow FSIS to verify whether establishments have effective process
controls to address Salmonella. Since publishing the PR/HACCP final
rule, FSIS has updated the performance standards for poultry products
through a series of Federal Register notices.\14\
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\13\ When FSIS initially implemented the Salmonella performance
standards, the regulations authorized FSIS to suspend inspection if
an establishment failed to take the corrective actions necessary to
comply with the performance standards, or if an establishment failed
to meet the standards on the third consecutive series of FSIS-
conducted tests for that product. However, the Agency's ability to
directly enforce the pathogen reduction performance standards has
been limited since 2001, after a ruling by the U.S. Court of Appeals
for the Fifth Circuit in Supreme Beef Processors, Inc. v. USDA, 275
F.3d 432 (5th Cir. 2001). In that case, the court enjoined FSIS from
suspending inspection services against a meat grinding operation for
failure to meet the Salmonella performance standards. Since that
time, FSIS has used Salmonella failures as a basis to conduct an in-
depth evaluation of the establishment's food safety systems,
including its HACCP plan and sanitation SOPs.
\14\ See Salmonella Verification Sample Result Reporting: Agency
Policy and Use in Public Health Protection (71 FR 9772, Feb 27,
2006); New Performance Standards for Salmonella and Campylobacter in
Young Chicken and Turkey Slaughter Establishments: Response to
Comments and Announcement of Implementation Schedule (76 FR 15282,
Mar 21, 2011); New Performance Standards for Salmonella and
Campylobacter in Not-Ready-to-Eat Comminuted Chicken and Turkey
Products and Raw Chicken Parts and Changes to Related Agency
Verification Procedures: Response to Comments and Announcement of
Implementation Schedule (81 FR 7285, Feb 11, 2016); Changes to the
Salmonella and Campylobacter Verification Testing Program: Revised
Categorization and Follow-Up Sampling Procedures (83 FR 56046, Nov
9, 2018).
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FSIS has established Salmonella performance standards for young
chicken and turkey carcasses, raw chicken parts, and comminuted chicken
and turkey products. The current performance standards are expressed as
a fraction of the maximum number of allowable Salmonella-positive
results over a targeted number of samples collected and analyzed in a
52-week moving window (see Table 2). FSIS categorizes establishments
based on the Salmonella verification sampling results and posts the
categorization of all establishments subject to the performance
standards on the FSIS website.^{15 16} In addition, FSIS
schedules follow-up verification sampling, a Public Health Risk
Evaluation (PHRE),\17\

[[Page 64683]]

and possibly a Food Safety Assessment (FSA) \18\ for establishments
that do not meet the pathogen reduction performance standards. If,
after 90 days, an establishment has not been able to regain process
control, as determined from FSIS' follow-up sampling and from the
results of the PHRE or FSA, and the establishment has not taken
corrective actions, FSIS may take enforcement actions, such as by
issuing a NOIE or by suspending inspection, under the conditions and
according to the procedures described in 9 CFR part 500 (81 FR 7285,
7289). FSIS does not issue an NOIE or suspend inspection based solely
on the fact that an establishment did not meet a performance standard.
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\15\ Salmonella Categorization of Individual Establishments for
Poultry Products at: https://www.fsis.usda.gov/science-data/data-sets-visualizations/microbiology/salmonella-verification-testing-program-monthly.
\16\ The category definitions under verification sampling are as
follows:
Category 1: Establishments that have achieved 50
percent or less of the maximum allowable percent positive during the
most recently completed 52- week moving window;
Category2: Establishments that meet the maximum
allowable percent positive but have results greater than 50 percent
of the maximum allowable percent positive during the most recently
completed 52-week moving window; and
Category 3: Establishments that have exceeded the
maximum allowable percent positive during the most recently
completed 52-week moving window.
\17\ The PHRE is an analysis of establishment performance based
on ``For-cause'' and ``Routine risk-based'' criteria, FSIS Directive
5100.4 Revision 2--Public Health Risk Evaluation Methodology
(usda.gov).
\18\ The purpose of an FSA is to conduct a risk-based, targeted
review of establishment food safety systems to verify that the
establishment is able to produce safe and wholesome meat or poultry
products in accordance with FSIS statutory and regulatory
requirements. FSIS Directive 5100.1--Food Safety Assessment
Methodology (usda.gov).

Table 2--Salmonella Performance Standards for Poultry Products
----------------------------------------------------------------------------------------------------------------
Minimum number of
Performance Maximum samples to
Product standard * acceptable assess process
percent positive control
----------------------------------------------------------------------------------------------------------------
Broiler Carcasses...................................... 5 of 51 9.8 11
Turkey Carcasses....................................... 4 of 56 7.1 14
Comminuted Chicken..................................... 13 of 52 25.0 10
Comminuted Turkey...................................... 7 of 52 13.5 10
Chicken Parts.......................................... 8 of 52 15.4 10
----------------------------------------------------------------------------------------------------------------
* The performance standard is represented as a fraction of the maximum allowable positives over the target
number of samples collected and analyzed in a 52-week window.

3. Salmonella Performance Standards and Illnesses
The current Salmonella performance standards are based on risk
assessments \19\ and are designed to achieve the Healthy People targets
for foodborne illness reduction. When FSIS implemented the performance
standards, the Agency expected that there would be an observed
reduction in Salmonella illnesses rates because a smaller proportion of
certain raw poultry products would likely be contaminated with
Salmonella than had been the case without standards (81 FR 7285). The
results of FSIS' Salmonella verification sampling show that the current
prevalence-based performance standards approach has been effective in
reducing Salmonella contamination in poultry.^{20 21 22}
However, these measures have yet to have an observable impact on
Salmonella illnesses. With respect to foodborne illness reduction
goals, the Healthy People 2020 objectives had aimed to reduce the
annual number of foodborne illnesses caused by Salmonella from 15.0 per
100,000 population in 2006-2008 \23\. However, the CDC estimated that
in 2019, Americans experienced 17.1 per 100,000 population Salmonella
illnesses.\24\ This represents an increase of 14 percent from the 2006-
2008 baseline. As discussed below, there are likely several reasons why
the reduction in Salmonella contamination in poultry products has not
resulted in an observable impact on Salmonella illnesses.
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\19\ Ebel, E.D., Williams, M.S., Golden, N.J., Marks, H.M.,
2012. Simplified framework for predicting changes in public health
from performance standards applied in slaughter establishments. Food
Control 28, 250-257; Williams, M.S., Ebel, E.D., Vose, D., 2011.
Framework for microbial food-safety risk assessments amenable to
Bayesian modeling. Risk Analysis 31, 548-565.
\20\ Ebel E.D., Williams M.S., and Schlosser W.D. (2017).
Estimating the Type II error of detecting changes in foodborne
illness via public health surveillance. Microbial Risk Analysis 7:
1-7. https://doi.org/10.1016/j.mran.2017.10.001.
\21\ Ebel, ED and Williams MS (2020). Assessing the
effectiveness of revised performance standards for Salmonella
contamination of comminuted poultry. Microbial Risk Analysis
14:100076. https://doi.org/10.1016/j.mran.2019.05.002.
\22\ Williams MS, Ebel ED, Golden NJ, Saini G, Nyirabahiizi E,
and Clinch N (2022). Assessing the effectiveness of performance
standards for Salmonella contamination of chicken parts.
International Journal of Food Microbiology 378: 109801. https://doi.org/10.1016/j.ijfoodmicro.2022.109801.
\23\ HHS Office of Disease Prevention and Health Promotion
archive. Healthy People 2020 at: https://wayback.archive-it.org/5774/20220414163116/https://www.healthypeople.gov/2020/topics-objectives/topic/food-safety/objectives.
\24\ Tack DM, Ray L, Griffin PM, et al. Preliminary Incidence
and Trends of Infections with Pathogens Transmitted Commonly Through
Food--Foodborne Disease Active Surveillance Network, 10 U.S. Sites,
2016-2019, MMWR Morb Mortal Wkly Rep 202;69:509-514. Available at:
https://www.cdc.gov/mmwr/volumes/69/wr/mm6917a1.htm#T1_down.
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With respect to Salmonella illnesses associated with chicken and
turkey, one study found that the proportion of outbreaks associated
with these commodities was essentially unchanged from 1998-2017 and
that both the proportion of outbreaks and number of outbreaks
associated with chicken remained essentially constant.\25\ During that
period, the per capita annual consumption for pork, beef, and turkey
all declined between 9 percent and 22 percent, while annual consumption
of chicken increased by 15 percent.
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\25\ Williams, M.S., & Ebel, E.D. (2022). Temporal changes in
the proportion of Salmonella outbreaks associated with 12 food
commodity groups in the United States. Epidemiology and infection,
150, e126. https://doi.org/10.1017/S0950268822001042.
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The overall findings of another study indicated declining trends in
illness due to Salmonella serotypes associated with poultry and
increasing trends in illness due to Salmonella serotypes not associated
with poultry.\26\ However, illness attribution was not an objective of
the analysis. Thus, the observed illness declines may have been caused
by reduced risk in non-poultry sources that have poultry-like serotype
profiles.
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\26\ Powell M.R. (2023). Trends in reported illnesses due to
poultry-and nonpoultry associated Salmonella serotypes; United
States 1996-2019. Risk Analysis. https://doi.org/10.1111/risa.14181.
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The Healthy People 2030 target is to reduce the Salmonella illness
national case rate of 15.3 per 100,000 population in 2016-2018 by 25
percent, or to no more than 11.5 per 100,000 population per year.\27\
Thus, to reach the 2030 target, illnesses must be reduced by 25
percent. Although this target is for Salmonella illnesses from all
sources, FSIS has adopted the same target for foodborne illnesses
linked to FSIS-regulated products and aims to reduce these Salmonella
illnesses by 25 percent. To move closer to achieving this target, FSIS
has determined that it will need to adopt a new approach to more
effectively reduce foodborne illness associated with FSIS-regulated
products, starting with poultry as one of the leading food sources.
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\27\ HHS Office of Disease Prevention and Health Promotion
archive. Healthy People 2030 at: https://health.gov/healthypeople/objectives-and-data/browse-objectives/foodborne-illness/reduce-infections-caused-Salmonella-fs-04/data?group=None&state=United+States&from=2016&to=2018&populations=&tab=data-table#data-table.

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[[Page 64684]]

B. Consideration of Need for a New Framework To Control Salmonella in
Poultry

1. Petitions and Initial Stakeholder Input
Consumer advocacy organizations and other stakeholders have noted
that the Healthy People Salmonella reduction targets have not been met
and have submitted petitions and letters to FSIS requesting that the
Agency revise its current approach for reducing Salmonella illnesses
associated with poultry. For example, in January 2020, Marler Clark LLP
submitted a petition on behalf of several individuals and consumer
advocacy organizations requesting FSIS to issue an interpretive rule to
declare 31 Salmonella serotypes that have been associated with
foodborne illness outbreaks to be adulterants of all meat and poultry
products.\28\ According to the petition, such action is needed to
protect the health and welfare of consumers by encouraging the meat and
poultry industry to engage in more effective oversight measures and
create and implement effective preventative measures.
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\28\ Marler Clark LLP petition # 20-01 ``Petition for an
Interpretive Rule Declaring `Outbreak' Serotypes of Salmonella
enteritica subspecies to be Adulterants'' dated January 19, 2020.
Available at: https://www.fsis.usda.gov/policy/petitions/petition-interpretive-rule-related-certain-Salmonella-serotypes.
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In May 2022, FSIS denied the petition without prejudice, citing a
lack of sufficient data available to support the sweeping actions
requested in the petition. In the response, FSIS agreed that an updated
Salmonella strategy is necessary to reduce Salmonella illnesses
associated with poultry and described how FSIS was working towards
gathering data and information necessary to support a revised
strategy.\29\
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\29\ FSIS Final Response to Petition #20-01, May 31, 2022.
Available at: https://www.fsis.usda.gov/policy/petitions/petition-interpretive-rule-related-certain-Salmonella-serotypes.
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On January 25, 2021, the Center for Science in the Public Interest
(CSPI) and other consumer advocacy organizations petitioned FSIS to
establish enforceable standards targeting Salmonella types of greatest
public health concern and all Campylobacter \30\ in poultry.\31\
Referencing the Healthy People reduction goals, the petition asserted
that FSIS' current performance standards have not been effective in
reducing Salmonella illnesses because they aim to reduce the prevalence
of all Salmonella rather than prioritizing control efforts for the
Salmonella serotypes most likely to make people sick. The petition laid
out several suggestions for standards that FSIS could use to address
Salmonella in poultry. The petition recommended that FSIS work with
stakeholders and other public health agencies to establish enforceable
final product standards to target Salmonella serotypes of greatest
public health concern with an aim to eliminate these strains from
poultry products over time. The petition also suggested that FSIS
consider revising the current prevalence-based Salmonella performance
standard to provide for quantitative testing and add Salmonella levels
to the performance standards criteria to better ensure that when
Salmonella is present on a product, it is present at low levels less
likely to cause human illness. The petition asserted that FSIS is
authorized to deem poultry products that contain virulent Salmonella
strains and that contain pathogen levels above a set threshold to be
adulterated under the PPIA because more virulent serotypes and certain
levels of Salmonella are more likely to render poultry products
injurious to health as defined in 21 U.S.C. 453(g)(1).
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\30\ While the CSPI requested that FSIS take actions related to
both Salmonella and Campylobacter, FSIS is currently focusing on re-
evaluating its approach to prevent Salmonella illnesses associated
with poultry.
\31\ CSPI petition #21-01, ``Petition to Establish Enforceable
Standards Targeting Salmonella Types of Greatest Public Health
Concern while Reducing all Salmonella and Campylobacter in Poultry,
and to Require Supply Chain Controls'' (January 25, 2021) at:
https://www.fsis.usda.gov/policy/petitions/petition-submitted-center-science-public-interest.
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The 2021 CSPI petition also requested that FSIS initiate rulemaking
to require that poultry establishments identify and control foodborne
hazards within their supply chains, including Salmonella. The petition
stated that supply chain interventions may include targeted vaccines
developed for specific Salmonella serotypes and purchasing chicks from
suppliers certified to be free of priority serotypes. The petition
asserted that FSIS is authorized to require supply chain controls
through the current HACCP regulations, which direct establishments to
address, as appropriate, hazards both introduced in the establishment
and introduced outside the establishment, including food safety hazards
that occur before entry into the establishment (9 CFR 417.2). The
petition also asserted that FSIS has authority to verify the
effectiveness of supply chain controls under the PPIA's antemortem
inspection authority, which requires FSIS to conduct an antemortem
inspection in each official establishment processing poultry or poultry
products for commerce or otherwise subject to inspection under the PPIA
``where and to the extent considered . . . necessary,'' ``[f]or the
purpose of preventing the entry into or flow or movement in commerce of
. . . any poultry product which is capable of use as human food and is
adulterated'' (21 U.S.C. 455(a)). FSIS has not yet responded to the
2021 CSPI petition but has considered the issues raised in developing
this proposal.
In September 2021, FSIS received a letter from the Food Safety
Coalition (FSC), a coalition of several food safety leaders, public
health and consumer advocates, scientists, and members of the food
industry. Like the CSPI petition, the FSC letter noted that although
FSIS' current prevalence-based pathogen reduction performance standards
have led to reduced occurrence of Salmonella contamination in poultry
products, the Healthy People 2020 goals set by the Department of Health
and Human Services in 2010 for lowering Salmonella and Campylobacter
illness rates were not being met. The FSC letter stated that the likely
reason is that FSIS' current Salmonella performance standards do not
effectively target the particular types of Salmonella and products
containing Salmonella levels that pose the greatest risks of illness.
The letter stated that a new approach is needed to achieve the new
Healthy People 2030 Salmonella illness rate target and presented
several suggested changes to help reduce the rates of foodborne
illness. The proposed changes recommended by the FSC included
establishing modernized enforceable pathogen standards that ``invite
innovation,'' as well as modernizing the HACCP framework to address
risk reduction across the full production process, including defining
the responsibility of poultry processors to consider pre-harvest
practices and interventions in their HACCP plans.\32\
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\32\ Food Safety Coalition Letter, September 2, 2021. Available
at: https://www.fsis.usda.gov/inspection/inspection-programs/inspection-poultry-products/reducing-salmonella-poultry.
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2. FSIS Announces New Salmonella Effort
After considering the available data on Salmonella illnesses
associated with poultry as well as the initial stakeholder input
discussed above, on October 19, 2021, FSIS announced that it was
mobilizing a stronger, and more comprehensive effort to reduce
Salmonella illnesses associated with poultry products.\33\ In the

[[Page 64685]]

announcement, FSIS explained that the Agency would be initiating
several key activities to gather the data and information necessary to
support future action and move closer to the national target of a 25
percent reduction in Salmonella illnesses. The announcement also stated
that FSIS intended to seek stakeholder feedback on specific Salmonella
control and measurement strategies as well as using data to determine
if there are other approaches to reduce Salmonella. The announcement
noted that the effort would leverage USDA's strong research
capabilities and highlighted that FSIS would ask the National Advisory
Committee for Microbiological Criteria in Foods (NACMCF) to advise the
Agency on how it can build on the latest science to improve its
approach to Salmonella control. The announcement emphasized that FSIS
would work closely with stakeholders on informing and implementing key
activities of this framework.
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\33\ USDA Press Release, ``USDA Launches New Effort to Reduce
Salmonella Illnesses Linked to Poultry'' (October 19, 2021) at:
https://www.usda.gov/media/press-releases/2021/10/19/usda-launches-new-effort-reduce-salmonella-illnesses-linked-poultry.
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Following this announcement, the Coalition for Poultry Safety
Reform, a multistakeholder coalition that includes individuals and
organizations representing consumers, victims of foodborne illness,
food safety scientists, food safety officials, and members of the
poultry industry, submitted a letter to the USDA Deputy Under Secretary
for Food Safety in 2022 expressing support for a new effort to address
Salmonella. The letter requested that FSIS focus its efforts on
developing new regulatory standards related to Salmonella covering both
products and supply chains and that these standards be informed by a
risk assessment based on existing data.\34\ The letter recommended that
FSIS adopt enforceable product standards aimed at reducing risk of
illness and develop and conduct a risk assessment to understand illness
reduction benefits of various product standards.
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\34\ Coalition for Poultry Safety Reform Letter, February 2,
2022. Available at: https://www.fsis.usda.gov/inspection/inspection-programs/inspection-poultry-products/reducing-salmonella-poultry.
---------------------------------------------------------------------------

3. Activities Initiated To Support a New Salmonella Framework
After FSIS announced its new initiative to reduce Salmonella
illnesses associated with poultry products, the Agency initiated
several activities designed to gather data and information to inform
and support future actions related to this new effort.
National Advisory Committee Charge. On October 20, 2021, FSIS
announced a public meeting of NACMCF from November 17, 2021, to
November 19, 2021, to discuss, among other things, a new charge focused
on enhancing Salmonella control in poultry products.\35\ Specifically,
FSIS charged the NACMF Subcommittee on Enhancing Salmonella Control in
Poultry Products to provide guidance on the overarching risk management
question: What types of microbiological criteria (e.g., Salmonella
performance standards) might FSIS use to encourage reductions in
Salmonella in poultry products so that they are more effective in
preventing human Salmonella infections associated with these products?
\36\ FSIS also requested that the Subcommittee provide guidance on nine
additional specific risk management questions. On April 25, 2022,
NACMCF held a Subcommittee meeting for the workgroups addressing each
of the questions in FSIS' charge to provide an update to the entire
Subcommittee on their progress and to look at the overall timeline for
completing the work of the Subcommittee.\37\ On November 15, 2022,
NACMCF held a virtual public meeting to discuss and vote on the
Subcommittee's report on Enhancing Salmonella Control in Poultry
Products, which had been posted to the FSIS website on November 1,
2022.\38\ NACMCF adopted the final report pending finalization with
consideration given to oral comments provided at the virtual public
meeting and written comments submitted as directed in a Federal
Register notice announcing the public meeting.\39\ The comment period
for the NACMCF report was scheduled to close on November 15, 2022, but
was extended to December 30, 2022, to provide 60 days for public
review.\40\ After considering the public comments, NACMCF finalized its
report on March 13, 2023. The final report ``Response to Questions
Posed by the Food Safety and Inspection Service: Enhancing Salmonella
Control in Poultry Products'' (referred to as the 2023 NACMCF report in
this document) is available to the public on the FSIS website at:
https://www.fsis.usda.gov/policy/advisory-committees/national-advisory-committee-microbiological-criteria-foods-nacmcf/2021.
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\35\ National Advisory Committee Meeting on Microbiological
Criteria for Foods (NACMF) Public Meeting --November 2021. Available
at: https://www.fsis.usda.gov/news-events/events-meetings/national-advisory-committee-microbiological-criteria-foods-nacmcf-2.
\36\ 2021-2023 National Advisory Committee Meeting on
Microbiological Criteria for Foods (NACMF); FSIS Charge: Enhancing
Salmonella Control in Poultry Products Available at: https://www.fsis.usda.gov/policy/advisory-committees/national-advisory-committee-microbiological-criteria-foods-nacmcf/2021.
\37\ NACMCF FSIS Charge: Enhancing Salmonella Control in
Poultry, April 25, 2022. Available at: https://www.fsis.usda.gov/news-events/events-meetings/national-advisory-committee-microbiological-criteria-foods-nacmcf-fsis.
\38\ Public Meeting; National Advisory Committee on
Microbiological Criteria for Food, Nov 15, 2022. Available at:
https://www.fsis.usda.gov/news-events/events-meetings/public-meeting-national-advisory-committee-microbiological-criteria.
\39\ Public Meeting National Advisory Committee on
Microbiological Criteria for Food (87 FR 64001). Available at:
https://www.fsis.usda.gov/policy/federal-register-rulemaking/federal-register-notices/public-meeting-national-advisory.
\40\ FSIS Constituent Update--Nov 10, 2022: Deadline Extended to
Comment on NACMCF Document. Available at: https://www.fsis.usda.gov/news-events/news-press-releases/constituent-update-november-10-2022.
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Pilot Projects. In December 2021, FSIS announced in its Constituent
Update that the Agency was inviting poultry slaughter and processing
establishments to submit proposals for pilot projects that will test
different control strategies for Salmonella contamination in poultry
products.\41\ The announcement explained that pilot projects would last
for a defined period, during which establishments would experiment with
new or existing pathogen control and measurement strategies and share
data collected during the pilots with FSIS. The announcement included
instructions on how interested establishments could submit proposals
for pilots to FSIS. FSIS intended to analyze the data generated under
the pilots to determine whether it supports changes to FSIS' existing
Salmonella control strategies.
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\41\ FSIS Constituent Update--Dec 3, 2021: FSIS Seeking
Proposals for Pilot Projects to Control Salmonella in Poultry
Slaughter and Processing Establishments. Available at: https://www.fsis.usda.gov/news-events/news-press-releases/constituent-update-december-3-2021.
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Since March 2023, FSIS has granted pilot projects to 9
establishments to examine the merits and logistics of excluding
Salmonella poultry vaccine strains from the FSIS Salmonella performance
categorization calculations. After evaluating the data collected under
these pilots, on March 1, 2024, FSIS announced that beginning April 1,
2024, it intends to exclude current commercial vaccine subtypes
confirmed in FSIS raw poultry samples from the calculation used to
categorize establishments under the raw poultry Salmonella performance
standards.\42\ This action is intended to remove barriers to the use of
vaccination as an important pre-harvest intervention to

[[Page 64686]]

control Salmonella in poultry. A summary report of the data from these
pilots is posted on the Pilot Projects: Salmonella Control Strategies
page of the FSIS website at: https://www.fsis.usda.gov/inspection/inspection-programs/inspection-poultry-products/reducing-salmonella-poultry/pilot.
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\42\ FSIS Constituent Update--March 1, 2024: FSIS Intends to
Exclude Vaccine Strains from the FSIS Salmonella Performance
Categorization at: https://www.fsis.usda.gov/news-events/news-press-releases/constituent-update-march-1-2024.
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On September 23, 2023, FSIS granted a pilot to 2 establishments to
examine the merits of using preharvest results to optimize
establishment interventions.\43\ The data generated under the pilot
will be shared with and analyzed by FSIS to determine whether it
supports changes to FSIS' Salmonella control strategies.
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\43\ Pilot Projects: Salmonella control strategies. Current
Salmonella Pilot Participants available at: https://www.fsis.usda.gov/inspection/inspection-programs/inspection-poultry-products/reducing-salmonella-poultry/pilot.
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Research and Science Roundtable. On February 15, 2022, FSIS held a
research and science roundtable on Salmonella in poultry.\44\ The
intent of the roundtable was to convene research scientists to discuss
the scientific support for various potential components of a revised
strategy for Salmonella control in poultry. Among the topics discussed
at the roundtable were: research on surveillance and risk assessments
to evaluate the public health impact of the presence of Salmonella
serotypes of concern and levels of contamination at production;
research on Salmonella serotype dynamics in poultry production;
research to identify pre-harvest food safety challenges and solutions;
research modeling and correlation analysis work on pre-harvest in
poultry; research on interventions to control Salmonella in preharvest
and postharvest poultry production; and research in the area of
microbial biomapping of indicators and pathogenic loads throughout the
processing chain and using pre-harvest and post-harvest quantification
data to develop SPC programs. The presentations on these topics and
other materials associated with the research roundtable are available
to the public on the FSIS website at: https://www.fsis.usda.gov/news-events/events-meetings/Salmonella-poultry-research-and-science-roundtable.
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\44\ Salmonella in Poultry: Research and Science Roundtable.
Available at: https://www.fsis.usda.gov/news-events/events-meetings/Salmonella-poultry-research-and-science-roundtable.
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Exploratory Sampling Program and New Salmonella Quantification
System. In April 2022, FSIS initiated an exploratory program that
expanded young chicken carcass sampling at establishments subject to
the young chicken carcass performance standard.\45\ The purpose of the
exploratory sampling program was to generate microbial data to inform
the Agency's effort to reduce Salmonella illnesses attributable to
poultry. Under the program, in addition to the FSIS Salmonella
verification sample already collected at post-chill, FSIS inspection
program personnel (IPP) began collecting a second carcass sample at
rehang from the same flock. In addition, FSIS IPP were instructed to
collect the regularly scheduled National Antibiotic Resistance
Monitoring System (NARMS) cecal samples from the same flock as the
rehang and post-chill samples. The samples collected under the
exploratory sampling program were initially analyzed for the presence
of Salmonella and AC. FSIS IPP also completed a questionnaire at the
time they collected exploratory samples to collect data on pre-harvest
and slaughter interventions applied to the same flocks. A report on the
exploratory sampling results is available at: https://www.regulations.gov/docket/FSIS-2023-0028.
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\45\ FSIS Constituent Update--April 22, 2022: FSIS Expands
Salmonella Sampling for Young Chicken Carcasses. Available at:
https://www.fsis.usda.gov/news-events/news-press-releases/constituent-update-april-22-2022.
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In August 2022, FSIS announced that FSIS laboratories would begin
using new technology to quantify Salmonella in raw poultry rinses and
updated the exploratory sampling program for young chickens to quantify
confirmed Salmonella positive rehang and post-chill carcass results
using the new quantification system.\46\ These analyses were in
addition to the whole genome sequencing (WGS) that FSIS had already
been performing on confirmed Salmonella-positive post-chill carcass
samples.
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\46\ FSIS Constituent Update--Aug 5, 2022: FSIS to include
Salmonella Quantification in all Poultry Rinse Samples. Available
at: https://www.fsis.usda.gov/news-events/news-press-releases/constituent-update-august-5-2022-0. FSIS Notice 44-22, Revised Young
Chicken Exploratory Sampling Program, Aug 11, 2022.
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On January 30, 2023, FSIS added Salmonella quantification testing
and AC indicator analyses to chicken part rinsates.\47\ FSIS added
these two analyses to comminuted chicken testing on February 27, 2023,
and to comminuted turkey on April 3, 2023. Salmonella quantification is
a significant step in updating the diagnostic capabilities of FSIS'
food testing laboratories. The data generated from the new
quantification system along with the data collected from the young
chicken carcass exploratory sampling program were used to help inform
the policies discussed in this document, including the quantitative
microbial risk assessments to evaluate Salmonella in raw poultry
discussed below. The data generated from the quantification system have
also been added to FSIS' quarterly dataset release and are available
at: https://www.fsis.usda.gov/science-data/data-sets-visualizations/laboratory-sampling-data.
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\47\ FSIS Constituent Update--Feb 3, 2023: FSIS to Expand
Salmonella Enumeration and Aerobic Count Indicator Testing to Other
Poultry Products. Available at: https://www.fsis.usda.gov/news-events/news-press-releases/constituent-update-february-3-2023.
Notice 83-23, New Sampling Instructions and Testing for Chicken
Parts and NRTE Comminuted Poultry, Feb 3, 2023. Available at:
https://www.fsis.usda.gov/policy/fsis-notice/08-23.
---------------------------------------------------------------------------

Risk Profile. In May 2022, FSIS initiated a risk profile for
Salmonella subtypes in poultry linked to foodborne illness. FSIS
developed the risk profile to provide information on whether certain
serotypes or subtypes of Salmonella should be considered as adulterants
in specific poultry products within the meaning of the PPIA (21 U.S.C.
453(g)). The risk profile involved a comprehensive systematic review of
literature and supporting data designed to provide responses to the
following six risk management questions:
1. What Salmonella serotypes or subtypes are linked to foodborne
illness or outbreaks from consuming specific raw or not-ready-to-eat
chicken or turkey products?
2. Are these Salmonella serotypes or subtypes of concern present in
live chickens, live turkeys, and poultry products?
3. Can exposure to a small number of these Salmonella serotypes or
subtypes of concern result in foodborne illness?
4. Can exposure to these Salmonella serotypes or subtypes of
concern cause severe, debilitating health outcomes?
5. How can these Salmonella serotypes or subtypes of concern be
differentiated from other Salmonella subtypes?
6. Would ordinary consumer handling or preparation practices affect
exposure to Salmonella serotypes or subtypes of concern?
The risk profile was submitted for independent peer-review \48\ and
updated in response to peer review comments. The results of the risk
profile and how they were used to inform specific measures proposed in
this document are discussed below. The final Risk Profile for
Pathogenic Salmonella in Poultry (referred to as the 2023 risk profile
in

[[Page 64687]]

this document) is available at: https://www.regulations.gov/docket/FSIS-2023-0028.
---------------------------------------------------------------------------

\48\ Peer Review Plan: Risk Profile for Salmonella Subtypes in
Poultry Products Linked to Foodborne Illness (usda.gov).
---------------------------------------------------------------------------

Risk Assessments FSIS Developed to Inform Rulemaking. FSIS
conducted two new quantitative microbial risk assessments, one for
Salmonella in chicken and one for Salmonella in turkey, to inform the
Agency's new framework for reducing Salmonella attributed to poultry
consumed in the United States. FSIS expanded on this work through a
Cooperative Agreement (FSIS-02152022) with the University of Maryland's
Joint Institute for Food Safety and Applied Nutrition (UMD-JIFSAN), in
partnership with EpiX Analytics, to differentiate Salmonella serotypes
by virulence using advanced bioinformatics (i.e., machine learning) to
evaluate genomic data.\49\ The risk assessments address the following
risk management questions:
---------------------------------------------------------------------------

\49\ FSIS Constituent Update--July 1, 2022: FSIS Announces
Cooperative Agreement on Salmonella Risk Assessments. Available at:
https://www.fsis.usda.gov/news-events/news-press-releases/constituent-update-july-1-2022. Salmonella Risk Assessments and Risk
Management Questions at: https://www.fsis.usda.gov/inspection/inspection-programs/inspection-poultry-products/reducing-Salmonella-poultry/Salmonella-1.
---------------------------------------------------------------------------

1. What is the public health impact (change in illnesses,
hospitalizations, and deaths) achieved by eliminating at receiving a
proportion of chicken (or turkey) contaminated with specific levels of
Salmonella and/or specific Salmonella subtypes?
2. What is the public health impact (change in illnesses,
hospitalizations, and deaths) achieved by eliminating final product
contaminated with specific levels of Salmonella and/or specific
Salmonella subtypes?
3. What is the public health impact of monitoring/enforcing process
control from rehang to post-chill? Monitoring could include analytes
such as Enterobacteriaceae Count (EB), AC, or other indicator
organisms, analysis could include presence/absence or levels and the
monitoring could also include variability of actual result versus
expected result, log reduction, absolute sample result, or other
individual establishment specific criteria.
4. What is the public health impact of implementing combinations of
the risk management options listed above?
The risk assessments were submitted for independent peer-review
\50\ and updated in response to peer review comments. The risk
assessments, and the manner in which the results were used to inform
specific measures proposed in this document, are discussed below. The
final Quantitative Risk Assessment for Salmonella in Raw Chicken and
Raw Chicken Products and Quantitative Risk Assessment for Salmonella in
Raw Turkey and Raw Turkey Products (referred to as the 2023 risk
assessments in this document) are available at: https://www.regulations.gov/docket/FSIS-2023-0028.
---------------------------------------------------------------------------

\50\ Peer Review Plan: Quantitative Microbial Risk Assessment of
Salmonella in Chicken Products available at: https://www.fsis.usda.gov/sites/default/files/media_file/documents/FSIS_Salmonella_Peer_Review_Plan_Chicken.pdf.Peer Review Plan:
Quantitative Microbial Risk Assessment of Salmonella in Turkey
Products available at: https://www.fsis.usda.gov/sites/default/files/media_file/documents/FSIS_Salmonella_Peer_Review_Plan_Turkey.pdf.
---------------------------------------------------------------------------

4. Initial Measures Implemented To Address Salmonella Illnesses
Associated With Consumption of Poultry Products
After FSIS announced its new Salmonella initiative in October 2021,
in addition to initiating the activities to gather data to inform and
support a new Salmonella Framework discussed above, the Agency
implemented some initial measures to support this effort.
Salmonella Key Performance Indicator. As part of USDA's strategic
and performance planning process for fiscal years (FY) 2022-2026, FSIS
established a new ``key performance indicator'' (KPI) targeted to
reduce the proportion of poultry samples with Salmonella serotypes
commonly associated with human illnesses.\51\ This KPI is a measure
that is used to evaluate FSIS' progress towards reaching its objectives
and goals identified in both Agency and USDA strategic plans and will
serve as a metric for success for the USDA FY 2022-2026 Strategic Plan.
FSIS analyzed historical Agency sampling data, in addition to FoodNet
Fast data from the CDC, to determine the top three Salmonella serotypes
commonly associated with human illness for this measure. The analysis
found that these serotypes are Infantis, Enteritidis, and Typhimurium.
FSIS will use annual targets to track progress toward reducing the
proportion of poultry samples with the KPI serotypes and is seeking a 2
percent reduction each year, with the goal of achieving a 10 percent
reduction by FY 2026. KPI serotypes are useful for strategic and
performance planning purposes, and these may differ from the serotypes
of public health significance (which will likely change over time as
the serotypes commonly associated with human illnesses change).
---------------------------------------------------------------------------

\51\ FY2022-2024 Food Safety Key Performance Indicator.
Available at: https://www.fsis.usda.gov/inspection/inspection-
programs/inspection-poultry-products/reducing-Salmonella-poultry/
Salmonella-0#:~:text=FY2022-
2026FoodSafetyKeyPerformanceIndicatorA,theUSDAFiscalYear28FY292022-
2026StrategicPlan.
---------------------------------------------------------------------------

Final Determination. On August 1, 2022, FSIS announced that it
would be declaring Salmonella as an adulterant in breaded and stuffed
not-ready-to-eat (NRTE) chicken products (also referred to as ``NRTE
breaded stuffed chicken products'').\52\ These products contain raw,
comminuted chicken breast meat, trim, or whole chicken breast meat, but
the finished product is heat-treated only to set the batter or breading
on the exterior of the product, which may impart an RTE appearance.\53\
Although the labeling of NRTE breaded stuffed chicken products has
undergone significant changes over time to better inform consumers that
the products are raw and to provide instructions on how to prepare them
safely, these products continue to be associated with Salmonella
illness outbreaks. Based on information from Salmonella illness
outbreaks associated with NRTE breaded stuffed chicken products and
information from research on consumer handling practices with respect
to these products, FSIS concluded that labeling that informs consumers
that these products are raw and how to prepare them safely fails to
sufficiently protect consumers from illness.
---------------------------------------------------------------------------

\52\ Salmonella as an Adulterant in Breaded Stuffed Raw Chicken
Products (Aug 1, 2022). Available at: https://www.usda.gov/media/press-releases/2022/08/01/usda-announces-action-declare-Salmonella-adulterant-breaded-stuffed.
\53\ FSIS Directive 5300.1, Revision 1. Managing the
Establishment Profile in the Public Health Information System.
(usda.gov). See attachment 2 ``NRTE Stuffed Chicken Products that
appear RTE.''
---------------------------------------------------------------------------

On April 28, 2023, FSIS published a proposed determination to
declare that NRTE breaded stuffed chicken products that contain
Salmonella at levels of 1 cfu per gram or higher are adulterated within
the meaning of the PPIA (88 FR 26249). FSIS also proposed to carry out
verification procedures, including sampling and testing of the chicken
component of NRTE breaded stuffed chicken products prior to stuffing
and breading, to ensure producing establishments control Salmonella in
these products. The comment period for the proposed determination was
scheduled to close on June 27, 2023, but was extended to August 11,
2023, in response to requests from members of the regulated
industry.\54\
---------------------------------------------------------------------------

\54\ FSIS Constituent Update--July 21, 2023: FSIS Extends
Comment Period on Proposed Determination: Salmonella in Not-Ready-
To-Eat Breaded Stuffed Chicken Products. Available at: https://
www.fsis.usda.gov/news-events/news-press-releases/constituent-
update-july-21-
2023#:~:text=FSISisextendingthecommentperiodonthe,FSISextendedthedead
lineuntilJuly272023.

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[[Page 64688]]

FSIS received 3,386 comments on the proposed determination. After
careful consideration of the comments, on May 1, 2024, FSIS finalized
the determination as proposed, with one change (89 FR 35033). Instead
of collecting samples after the establishment has completed all
processes needed to prepare the chicken component to be stuffed and
breaded to produce a final NRTE breaded stuffed chicken product, as was
proposed, FSIS will collect verification samples on the raw incoming
chicken components. This change was intended to provide greater
flexibility and reduce costs to industry.
As noted above, NRTE breaded stuffed chicken products are
adulterated if they contain Salmonella at 1 cfu/g or higher, regardless
of the Salmonella serotype. FSIS adopted this approach for NRTE breaded
stuffed chicken products because these products present a unique public
health risk. Unlike raw chicken carcasses, chicken parts, comminuted
chicken, and comminuted turkey, NRTE breaded stuffed chicken products
may have a cooked appearance, are thicker in diameter than many other
poultry products, contain multiple ingredients, and are typically
cooked from a frozen state. In addition, outbreak data cited in the
NRTE breaded stuffed chicken proposal indicate that these products have
been consistently and disproportionately associated with Salmonella
illness outbreaks over the years. As FSIS acknowledged in the NRTE
breaded stuffed chicken proposed and final determination, although not
all Salmonella serotypes are equally likely to cause illness, all
serotypes have the ability to invade, replicate, and survive in human
host cells, resulting in potentially serious disease. Thus, because of
the unique public health risk associated with NRTE breaded stuffed
chicken products, FSIS determined that these products are adulterated
if they contain any Salmonella stereotypes at or above 1 cfu/g.

C. Public Meeting on Salmonella Framework Under Consideration and
Public Comments

1. Public Meeting and Proposed Framework
On October 17, 2022, FSIS published a Federal Register notice
announcing that it was hosting a virtual public meeting on November 3,
2022, to discuss a regulatory framework that the Agency was considering
for a new strategy to control Salmonella in poultry products and more
effectively reduce foodborne Salmonella infections linked to these
products (87 FR 62784). In the notice, FSIS shared the key elements of
the framework under consideration and stated that the Agency was
soliciting comments from stakeholders on all elements of the draft
framework, both at the public meeting and in written comments submitted
in response to the Federal Register notice, before moving forward with
any proposed changes to regulations or other actions. The Agency also
made a document outlining the regulatory framework under consideration
available to the public before the public meeting by publishing it on
the FSIS website.\55\
---------------------------------------------------------------------------

\55\ Proposed Regulatory Framework to Salmonella Illnesses
Attributable to Poultry. Available at: https://www.fsis.usda.gov/inspection/inspection-programs/inspection-poultry-products/reducing-Salmonella-poultry/proposed.
---------------------------------------------------------------------------

The three components under consideration in the draft framework
included:
1. Requiring that incoming flocks be tested for Salmonella before
entering an establishment;
2. Enhancing establishment process control monitoring and FSIS
verification; and
3. Implementing an enforceable final product standard.
The framework under consideration also addressed cross-cutting
issues associated with testing for Salmonella, considerations for small
and VS establishments, and data sharing. FSIS specifically requested
comments on factors the Agency should consider relative to the
approaches outlined in each of the components, how each component can
be strengthened, and where are there gaps in the framework. FSIS also
requested comments on relevant scientific evidence or examples of how
the components may be implemented or the impacts they may have on human
Salmonella illnesses.
At the November 3, 2022, public meeting, stakeholders presented
oral comments to FSIS panels comprised of FSIS leadership and experts
on the three separate components of the framework and the cross-cutting
issues. The primary purpose of the panels was to listen to stakeholder
input and ask clarifying questions as needed.\56\ In addition to the
oral comments presented at the public meeting, FSIS also provided an
opportunity for the public to submit written comments on the framework.
The comment period for submitted written comments was scheduled to
close on November 16, 2022, but was extended to December 16, 2022, to
allow stakeholders sufficient time to take into consideration the
discussion at the November 3, 2022, public meeting.\57\ A summary of
the general issues raised by the public comments is discussed below.
---------------------------------------------------------------------------

\56\ A transcript of the public meeting and other related
materials are available to the public on the FSIS website at:
https://www.fsis.usda.gov/news-events/events-meetings/public-meeting-reducing-Salmonella-poultry.
\57\ FSIS Constituent Update--Oct 28, 20222: FSIS Extends Public
Meeting and Comment Period on Proposed Salmonella Framework.
Available at: https://www.fsis.usda.gov/news-events/news-press-releases/constituent-update-october-28-2022-1.
---------------------------------------------------------------------------

2. Public Comments on the Proposed Framework
During the comment period for the proposed framework, FSIS received
1,034 comments. Seven hundred seventy-three comments were identical or
similar comment letters from individuals in support of the proposed
framework, and 75 were identical or similar comment letters from
individuals opposed to the proposed framework. One consumer advocacy
organization submitted a comment letter with a spreadsheet containing
4,916 names in support of the framework. Another consumer advocacy
organization submitted a comment letter with a spreadsheet containing
3,487 names in support of the framework. FSIS also received 149 unique
comments from individuals, most in opposition to the proposed
framework. In addition to the individual comments and form letters,
FSIS received approximately 35 separate comment letters from trade
associations representing the meat and poultry industries, consumer
advocacy organizations, animal welfare advocacy organizations, small
poultry growers and processors, organizations that support independent
family farmers, a large meat producer, a trade association representing
the veterinary profession, a State Department of Agriculture, an
organic/sustainable agriculture organization, a biotech company
representative, a meat scientist, and academics. The general issues
raised on each of the components under consideration in the framework
and on the cross-cutting issues are described below.
Comments on Component One. Component One of the draft framework
considered whether FSIS should require slaughter establishments to
characterize Salmonella as a hazard reasonably likely to occur at
receiving and require that incoming flocks be tested for Salmonella
before entering an establishment. Under this approach, the flock would
be required to meet a predetermined target for Salmonella at

[[Page 64689]]

receiving, which may be industry-wide or establishment-specific. The
establishment would be required to demonstrate that its subsequent
process will be effective in reducing Salmonella so that the product
meets the final product standard under consideration in Component
Three.
Comments from individuals, consumer advocacy organizations, and
animal welfare advocacy organizations expressed general support for the
measures under consideration in Component One. A consumer advocacy
organization commented that requiring incoming flocks be tested for
Salmonella would provide incentives for producers to adopt effective
pre-harvest measures and for establishments to take action to further
reduce food safety risks from flocks failing the incoming Salmonella
target, such as slaughtering more contaminated flocks at the end of the
day.
Comments from small poultry processors and producers, organizations
representing small poultry producers and independent family farmers,
and trade associations representing the meat and poultry industries
expressed concerns that the measures under consideration in Component
One would impose an overwhelming burden on small producers. An
organization representing small poultry producers and several
individual comments stated that requiring that flocks be tested for
Salmonella before they enter an establishment would add delays and
costs that small operators cannot afford.
Several comments, including comments from trade associations
representing the meat and poultry industries and organizations that
support independent family farmers, asserted that FSIS lacks legal
authority to require the measures under consideration in Component One,
particularly the requirements that incoming flocks be tested for
Salmonella. The commenters stated that FSIS' authority under the PPIA
begins at the official establishment and does not extend to the farm.
The commenters also asserted that Component One conflicts with HACCP
principles in that under HACCP, establishments, not FSIS, are
responsible for making decisions on how to execute their food safety
system.
Comments from trade associations representing the meat and poultry
industries asserted that FSIS had presented no data to demonstrate that
an incoming Salmonella threshold or limit is necessary for an
establishment to maintain process control and sufficiently reduce
Salmonella during processing. They also stated that FSIS did not
explain how on-farm sampling several weeks before a flock is processed
correlates to actual incoming Salmonella loads or provide data to show
that reducing incoming loads would have any public health impact. The
commenters noted that many producers and processors currently employ
interventions aimed at reducing Salmonella on farms and suggested that
FSIS consider other measures to incentivize pre-harvest controls
without requiring testing, such as encouraging establishments to
consider Salmonella a hazard reasonably likely to occur and providing
guidance for addressing Salmonella pre-harvest. Some of the commenters
that opposed Component One suggested removing this component entirely.
Comments on Component Two. The measures under consideration in
Component Two of the proposed framework would build on HACCP
regulations, which provide a prevention-based approach to food safety.
To ensure pathogen control throughout slaughter and processing
operations, Component Two would modify the existing requirements for
microbial organism testing for process control in 9 CFR 381.65(g) and
establish additional parameters to better define the required analysis
of the data. Establishments would be required to test for indicator
organisms (e.g., AC or EB) at rehang and post-chill and would be
required to use a standardized statistical approach to process control.
FSIS would consider production volume when determining the frequency
that establishments must collect samples.
FSIS received several comments in support of the measures under
consideration in Component Two from consumer advocacy organizations and
academia. These commenters generally agreed with the proposal but
recommended that FSIS consider additional measures, such as requiring
establishments to test more broadly for indicator organisms and/or
requiring testing at more sampling points. These commenters also
recommended that FSIS work with stakeholders to develop the SPC
approach after conducting research to determine the best points
predictive of end product Salmonella levels and tailor the SPC for
differences in processors' equipment and plant layouts.
Trade associations representing the meat and poultry industries, a
State Department of Agriculture, and an organic/sustainable agriculture
organization expressed concerns about some of the measures under
consideration in Component Two. The commenters asserted that there is a
lack of necessary data to support creating a rigid SPC framework for
all establishments. An organic/sustainable agriculture organization
requested that small producers be exempt from this component. A trade
association representing the meat and poultry industry suggested that
FSIS consider conducting verification sampling at specific locations
and allow establishments to develop their own sampling plans. An
association representing small and VS poultry establishments stated
that the Component Two measures under consideration will be costly and
will not reduce Salmonella.
Comments on Component Three. Component Three of the draft framework
under consideration would implement an enforceable final product
standard to prevent raw poultry products with certain levels and/or
types of Salmonella contamination from entering the stream of commerce.
FSIS would establish the standard by classifying certain Salmonella
levels and/or serotypes as adulterants in raw poultry and take action
against poultry products that exceed the final product standard.
Consumer advocacy organizations, coalitions promoting food safety,
and individuals with expertise in food and meat science generally
supported Component Three and recommended that FSIS prioritize
developing and implementing Component Three. According to these
commenters, it is the most critical part of the framework. These
commenters recommended an enforceable approach to combatting
Salmonella. The commenters stated that such an approach would provide
much greater safety to consumers by preventing highly contaminated
product from reaching store shelves and would motivate industry to
adequately control Salmonella because of the direct financial cost of
losing product that does not meet the final standard.
Some of the comments in support of Component Three requested that
FSIS provide increased transparency and data regarding how the product
standards under consideration would look. One consumer advocacy
organization emphasized that FSIS should use scientifically sound risk
assessments in determining final product standards. A consumer advocacy
organization recommended establishing separate standards for different
poultry products and stated that, for chicken, the standard could be
based on FSIS' KPI serotypes Enteritidis, Infantis, and Typhimurium,
and that for turkey, the standard could be based on serotypes Reading,
Infantis, and Typhimurium. A

[[Page 64690]]

consumer advocacy organization stated that FSIS should set stricter
standards for certain products if the risk assessment identifies higher
risk poultry products and that the risk assessments would determine
whether the final product standards should be based on Salmonella
enumeration, serotypes, or a combination of both.
Comments from trade associations representing the meat and poultry
industries, trade associations representing small poultry processors
and family farmers, a state government entity, and both large and small
businesses associated with poultry production did not support the
establishment of enforceable final product standards. These comments
opposed considering Salmonella to be an adulterant in raw poultry. Many
of the commenters stated that FSIS has historically not considered
Salmonella as an adulterant in raw poultry because: (1) Salmonella is
not an ``added substance'' and (2) Salmonella is not present in levels
that render chicken or turkey injurious to health because customary
poultry cooking practices destroy Salmonella. The commenters stated
that FSIS has not provided any new information to support a change in
this interpretation. Comments from these trade associations and a state
government entity also stated that FSIS' comparison of Salmonella in
raw poultry to Escherichia coli (E. coli) in non-intact beef is not
relevant, given that the two are very different in how they occur in
products and how they are destroyed through cooking.
On the other hand, comments from consumer advocacy organizations
stated that Salmonella may be considered as an ``added substance''
because it is not found in the muscle tissue of healthy animals but
rather is deposited through cross-contamination during slaughter and
processing. The commenters asserted that regardless of whether FSIS
considers certain Salmonella levels or serotypes most associated with
human illness to be an ``added substance,'' they are adulterants
because they ``ordinarily render'' contaminated poultry products
injurious to health.
Commenters that opposed Component Three expressed concern about the
delay that would result from a national verification testing program. A
trade association representing the chicken industry argued that the
extra time required for poultry producers to hold their product pending
FSIS' Salmonella testing results will significantly decrease the number
of poultry products that can safely reach store shelves. An
organization representing small poultry producers and processors stated
that waiting for acceptable test results would particularly affect
small producers who may not have the capability to hold poultry for a
long period of time.
Some commenters recommended alternatives to Component Three that
the commenters believed would more effectively reduce Salmonella
infection rates from poultry. For example, a large company that
processes poultry recommended that, instead of developing new final
product standards based on product adulteration, FSIS update the
current performance standards to include a new metric based on a
quantification target that measures beyond the prevalence of
Salmonella, which the commenter said would work well within a current
or an updated HACCP system.
Many comments opposed to Component Three asserted that the proposed
measures under consideration lacked information on the data and methods
that would be used to establish the final product standards. A trade
association representing the chicken industry questioned whether FSIS
had sufficient laboratory space needed to sample different product lots
for Salmonella levels or serotypes. An organization representing
independent family farmers recommended that, instead of establishing
final product standards, FSIS should identify the Salmonella strains
that cause most illnesses and target those strains specifically rather
than providing more general product standards. The 75 similar comment
letters that opposed the framework stated that FSIS should remove
Component Three from the framework until the Agency provides a clear
statement of the levels and/or strains of Salmonella that would define
the final product standards.
Comments on other issues raised. In addition to comments about the
above Components, there were comments raised about the framework in
general. Among these comments were write-in campaigns that expressed
general support for the proposed framework. A trade association
representing the chicken industry argued that the proposed framework
under consideration is not necessary because FSIS' existing framework
for addressing Salmonella control has been working. A trade association
representing the poultry industry commented that there is a need for
consumer research and education regarding safe handling of poultry.
Some comments expressed concern that adopting the framework would lead
to an increase in food waste.
Comments on data sharing. FSIS received five comments regarding the
need to share data. An academic suggested FSIS work with stakeholders
to facilitate sharing of industry data that would provide additional
insights into the sampling points that would be most predictive of
process control. Trade associations representing the poultry industry
urged FSIS to create a pathway for companies to share confidential
proprietary data with the Agency and indicated it would be necessary to
ensure that data is shared only with FSIS. A sustainable agriculture
organization emphasized the need for an enhanced ability to share
information among agencies, the academic community, and industry.
3. Additional Stakeholder Input
In addition to the November 2022 public meeting, FSIS also
participated in technical meetings with representatives from the
poultry industry, consumer advocacy organizations, academia, and other
stakeholders to further discuss aspects of the proposed Salmonella
ramework. These technical meetings were organized and hosted by the
regulated industry. The first technical meeting was held on March 21,
2023. Among the topics discussed were differences in production
practices and Salmonella control strategies between chicken and
turkeys, review of ongoing risk assessments, pre-harvest control risk
management measures, creating, implementing, and reacting to
statistical process control measures, and Salmonella quantification
methods. A second technical meeting was held on April 12, 2023. Among
the topics discussed at that meeting were incentivizing use of pre-
harvest interventions, how statistical process control is used in the
poultry industry and educational needs, and addressing lot size and
microbiological independence, and a review of the key differences
between beef and poultry. FSIS officials also held a virtual meeting
with small and VS establishment owners in February 2023 to seek input
on the Salmonella Framework under consideration.\58\
---------------------------------------------------------------------------

\58\ Officials' Calendar of Meetings (Feb 2023) at: https://www.fsis.usda.gov/news-events/events-meetings/officials-calendar-meetings.
---------------------------------------------------------------------------

4. Overview of Modifications to the Proposed Salmonella Framework
FSIS has carefully evaluated the written comments and other
stakeholder input provided on the proposed Salmonella Framework, along
with new studies and information that have become available since the
Agency made the information about the framework under consideration

[[Page 64691]]

available to the public in November 2022. Based on this evaluation,
FSIS has decided to modify some of the measures it had been considering
as part of the Salmonella Framework and is proposing these modified
measures in this document. FSIS requests comments on all measures
proposed in this document. If, after the close of the comment period,
the Agency determines that some portions of the modified Salmonella
Framework can be finalized sooner than others, FSIS will finalize those
portions separately from the others so as not to delay regulatory
action on this important public health initiative.
The proposed modified framework components are discussed in more
detail under separate headings in this document. The headings for the
proposed modified framework correspond to the component headings used
for the draft framework that FSIS presented to the public, i.e.,
Component One, Component Two, Component Three. The components are
discussed in this proposal in an order that emphasizes the most
significant proposed changes first. Therefore, the discussion begins
with Component Three: Final Product Standards, followed by Component
Two: Enhanced Establishment Process Control Monitoring, and finally
Component One: Pre-Harvest Measures.
Following is a general summary of the modifications.
Component Three Modifications. Consistent with Component Three of
the draft framework that was under consideration, FSIS is proposing
enforceable final product standards to prevent raw poultry products
with certain levels and Salmonella serotypes from entering commerce.
Under this proposal, FSIS has tentatively determined that certain raw
poultry products that contain Salmonella in an amount that exceeds a
specified level and that contain any detectable level of certain
Salmonella serotypes are adulterated as defined in the PPIA. The
proposed final product standards are as follows:
Chicken carcasses and chicken parts: Salmonella at or
above 10 cfu per milliliter of rinsate collected in any sample and any
detectable level of at least one of the Salmonella serotypes of public
health significance (i.e., Enteritidis, Typhimurium, and I 4,[5],12:i:-
);
Comminuted chicken: Salmonella at or above 10 cfu per gram
of product collected in any sample and any detectable level of at least
one of the Salmonella serotypes of public health significance (i.e.,
Enteritidis, Typhimurium, and I 4,[5],12:i:-);
Comminuted turkey: Salmonella at or above 10 cfu per gram
of product collected in any sample and any detectable level of at least
one of the Salmonella serotypes of public health significance (i.e.,
Hadar, Typhimurium, and Muenchen).
FSIS is also proposing that the Agency would routinely collect
samples of raw final products subject to the proposed standards and
analyze them for Salmonella levels and serotypes to determine whether
the product is adulterated.
Component Two Modifications. To ensure that poultry slaughter
establishments are effectively controlling Salmonella throughout their
operations, FSIS is proposing to revise the current regulations in 9
CFR 381.65(g) that require that all poultry slaughter establishments
develop, implement, and maintain written procedures to prevent
contamination by enteric pathogens throughout the entire slaughter and
dressing operation. FSIS is proposing to revise these regulations to
clarify that these procedures must include an MMP that incorporates SPC
monitoring methods. These proposed amendments would also specify that
the pre-chill sampling location is at rehang and specify the use of
appropriate microbial organisms for monitoring process control. In
addition, VS and VLV establishments operating under Traditional
Inspection \59\ would have to test at both rehang and post-chill,
instead of at post-chill only, although some of these establishments
would have the option to use laboratory services provided by FSIS to
analyze their monitoring samples. FSIS has developed proposed guidance
to help establishments meet the proposed sampling and analysis
requirements. Under this proposal, the guidance would be considered as
a ``safe harbor'' in that establishments that follow the guidance will
have met the proposed MMP requirements in 9 CFR 381.65(g). FSIS is also
proposing to amend the recordkeeping requirements in 9 CFR 381.65(h) to
require that establishments submit their microbial monitoring results
to the Agency electronically.
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\59\ Traditional Inspection is typically employed at smaller
lower production volume establishments that eviscerate carcasses by
hand (77 FR 4410).
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Component One Modifications. Based on the need for additional
research and due to implementation challenges, FSIS has decided, at
this time, not to establish a regulatory requirement that
establishments characterize Salmonella as a hazard reasonably likely to
occur at receiving or that incoming flocks be tested for Salmonella
before entering an establishment. FSIS, however, will focus on
achieving the goal of Component One--reduce the amount and type of
Salmonella contamination that enters the establishment--through non-
regulatory strategies. These include actively encouraging the wider use
of modified-live vaccines, which have been demonstrated to have a very
effective role in mitigating the hazard associated with specific
Salmonella serotypes, while reducing the entire load of similar
serogroup Salmonella through cross-protection. FSIS is also working
with the Animal and Plant Health Inspection Service (APHIS) to explore
ways to expand the National Poultry Improvement Program (NPIP), which
has been effective in reducing the prevalence of particular Salmonella
serotypes.
The Agency will continue to explore and develop strategies for
addressing Salmonella contamination risk at receiving. FSIS also
intends to revise its existing compliance guideline on Controlling
Salmonella in Raw Poultry \60\ to provide effective guidance on pre-
harvest interventions and practices for preventing or reducing
Salmonella colonization of live birds.
---------------------------------------------------------------------------

\60\ FSIS Guideline for Controlling Salmonella in Raw Poultry
(July 2021). Available at: https://www.fsis.usda.gov/guidelines/2021-0005.
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5. Severability
While the three components in this proposal support a comprehensive
approach to controlling Salmonella in poultry, they are each separate
actions that could operate independently of each other to address
Salmonella illnesses associated with poultry products. Therefore, the
following portions of this proposal are mutually severable from each
other: The proposed determination that would establish final product
standards for certain raw poultry products proposed under Component
Three; the proposed amendments to 9 CFR 381.65 (g) and (h) that would
enhance process control monitoring in all poultry slaughter
establishments under Component Two; and the proposed non-regulatory
approach to address pre-harvest measures in Component One. Should FSIS
finalize this proposal, if any of the above portions were to be set
aside by a reviewing court, FSIS would intend for the remainder of this
action to remain in effect.
These proposals are discussed in more detail below.

[[Page 64692]]

II. Component Three: Proposed Final Product Standards

A. Current Salmonella Performance Standards and Consideration of an
Alternative Approach

As discussed above, although FSIS sampling data show that the
occurrence of Salmonella in raw poultry products has decreased since
FSIS implemented its prevalence-based Salmonella performance standards,
there has not been a corresponding observed reduction in Salmonella
illnesses in the United States. There are likely multiple reasons for
the disconnect between the reduced Salmonella contamination in poultry
products and continued illnesses. Individuals who become ill may be
exposed to more virulent Salmonella strains or higher concentrations of
Salmonella,\61\ and, as noted above, consumption of poultry has
increased.\62\ Additionally, as discussed below, several consumer
behavior research studies suggest that ordinary consumer cooking and
preparation practices for many raw chicken and turkey products do not
provide adequate assurance that these products will not be contaminated
with Salmonella when consumed. Therefore, FSIS has decided to
reconsider its current approach to Salmonella performance standards for
poultry and has tentatively concluded that the Agency should adopt an
alternative approach to more effectively reduce Salmonella illnesses
associated with poultry products. This proposal addresses the
disconnect between Salmonella contamination on poultry and human
illnesses because it targets specific Salmonella serotypes more
frequently associated with illness and limits the concentration of
Salmonella permitted in certain raw poultry products.
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\61\ FSIS Risk Profile for Pathogenic Salmonella in Poultry
(2023); FAO/WHO (Food and Agriculture Organization/World Health
Organization) ``Microbiological Risk Assessment Series 3: Hazard
Characterization for Pathogens in Food and Water''. Geneva, Rome:
World Health Organization, Food and Agricultural Organization of the
United Nations; 2003; Cheng, RA, Eade CR, and Wiedmann M (2019).
Embracing Diversity: Differences in Virulence Mechanisms, Disease
Severity, and Host Adaptations Contribute to the Success of
Nontyphoidal Salmonella as a Foodborne Pathogen. Frontiers in
Microbiology, Volume 10 at: https://doi.org/10.3389/fmicb.2019.01368; Teunis, Peter FM (2022).Dose response for
Salmonella Typhimurium and Enteritidis and other nontyphoid enteric
salmonellae. Epidemics 41: 100653. https://doi.org/10.1016/j.epidem.2022.100653.
\62\ Williams, M.S., & Ebel, E.D. (2022). Temporal changes in
the proportion of Salmonella outbreaks associated with 12 food
commodity groups in the United States. Epidemiology and infection,
150, e126. https://doi.org/10.1017/S0950268822001042.
---------------------------------------------------------------------------

FSIS' current Salmonella performance standards focus on reducing
the prevalence of all Salmonella without considering differences in
virulence among individual Salmonella serotypes, strains, and
genotypes. Thus, the current standards do not focus on the types of
Salmonella most likely to cause human illnesses. In addition, the
current Salmonella performance standards consider only the presence or
absence of Salmonella in the product, while the quantity of the
pathogen may also have an impact on illness. Thus, the current
performance standards do not distinguish between poultry products that
are heavily contaminated and that contain the most virulent type of
Salmonella from those that contain trace amounts of a Salmonella with
types not typically associated with foodborne illnesses in the United
States.
Additionally, and independently, the Agency's ability to directly
enforce the pathogen reduction performance standards has been limited
since 2001, after a ruling by the U.S. Court of Appeals for the Fifth
Circuit in Supreme Beef Processors, Inc. v. USDA, 275 F.3d 432 (5th
Cir. 2001). In that case, the court enjoined FSIS from suspending
inspection services against a meat grinding operation for failure to
meet the Salmonella performance standards. Since that time, FSIS has
used Salmonella performance standard failures as a basis to conduct an
in-depth evaluation of the establishment's food safety systems,
including its HACCP plan and sanitation SOPs. However, because
Salmonella is not currently considered an adulterant in raw poultry,
the Agency cannot withhold the mark of inspection or otherwise prevent
products produced in an establishment that has failed the performance
standards from entering commerce based solely on the establishment's
performance standard results (75 FR 27288, 27293-4). This proposal, on
the other hand, would set an enforceable final product standard that
prevents raw poultry products with certain levels and types of
Salmonella contamination, which would be classified as adulterants,
from entering the stream of commerce.
When FSIS initially established the pathogen reduction Salmonella
performance standards in 1996, the Agency noted that, except for E.
coli O157:H7, FSIS had not taken the position that some amount of a
pathogen necessarily renders a raw meat or poultry product unsafe and
legally adulterated (61 FR 38806, 38835). At the time, the Agency
believed that it was constrained by the lack of a scientific basis for
determining the levels at which specific pathogens do or do not present
a safety hazard, and it also relied in part on the fact that proper
cooking kills pathogens on raw product (60 FR 6774, 6799). Therefore,
the initial pathogen reduction performance standards were based on a
statistical evaluation of the prevalence of bacteria in each
establishment's products, measured against the nationwide prevalence of
the bacteria in the same products (61 FR 38806, 38836). The Salmonella
performance standards were and still are not used to determine whether
specific product lots are legally adulterated. However, when FSIS
established the initial performance standards, the Agency made clear
that ``as more research is done and more data become available, and as
more sophisticated techniques are developed for quantitative risk
assessment for microbiological agents, it may be possible and
appropriate to develop performance standards that use a different
approach'' (61 FR 38806, 38836).
Since FSIS implemented the Salmonella performance standards, the
Agency has evaluated whether certain types of Salmonella should be
considered as adulterants in raw meat and poultry in response to
petitions submitted to the Agency in 2011, 2014, and 2022. For example,
in response to two petitions submitted by CSPI in 2011 and 2014, FSIS
evaluated whether certain antibiotic-resistant (ABR) Salmonella
serotypes could be considered as adulterants in raw meat and raw
poultry products under the Federal Meat Inspection Act (FMIA) and PPIA.
The 2011 petition asked FSIS to declare four strains of ABR Salmonella
as adulterants when found in ground meats and poultry.\63\ FSIS denied
the 2011 petition without prejudice on July 31, 2014. In its response,
FSIS explained that the data available at that time ``did not support
giving the four strains of ABR Salmonella identified in the petition a
different status as an adulterant in raw ground beef and raw ground
poultry than Salmonella strains that are susceptible to antibiotics.''
\64\ The response stated that additional data on the characteristics of
ABR Salmonella are needed to determine whether certain strains could
qualify as adulterants under the FMIA and PPIA.

[[Page 64693]]

The response also noted that because the Agency's denial was without
prejudice, the petitioner was not precluded from submitting a revised
petition that includes additional information to support the requested
action.
---------------------------------------------------------------------------

\63\ CSPI petition #11-06 (May 25, 2011), ``Petition for an
Interpretive Rule Declaring Specific Strains of Antibiotic Resistant
Salmonella to be Adulterants Withing the Meaning or 21 U.S.C.
601(m)(1) and (2)(a) and 21 U.S.C. 453(g)(1) and (2)(a).'' FSIS
final response (July 31, 2014) at: https://www.fsis.usda.gov/policy/petitions/petition-submitted-center-science-public-interest-0.
\64\ FSIS final response to petition #11-06, p. 1.
---------------------------------------------------------------------------

The CSPI 2014 petition was a refiling of the 2011 petition and
asked that FSIS declare certain strains of ABR Salmonella as
adulterants in all meat and poultry products based on evidence attained
since 2011 that, according to the petition, demonstrates both ground
and intact poultry products are associated with outbreaks from ABR
Salmonella.\65\ Based on the data available at the time, FSIS denied
the 2014 petition without prejudice on February 7, 2018. In its
response to the petition, the Agency concluded that, with respect to
its status as an adulterant, ``Salmonella does not appear to present
the same issues as [E. coli O157:H7], regardless of whether it is
resistant or susceptible to antibiotics.'' \66\ Therefore, the Agency
stated that it ``had no basis to conclude that either ABR-Salmonella or
non-ABR Salmonella would render injurious to health what consumers
consider to be properly cooked meat or poultry.'' \67\
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\65\ CSPI petition #14-01 (October 1, 2014), ``Request for an
Interpretive Rule Declaring Certain Antibiotic-Resistant Strains of
Salmonella to be Adulterants'' and FSIS final response (February 7,
2018) at: https://www.fsis.usda.gov/federal-register/petitions/request-interpretive-rule-declaring-certain-antibiotic-resistant-strains.
\66\ FSIS final response to petition #14-06, p. 6.
\67\ FSIS final response to petition #14-06, p. 7.
---------------------------------------------------------------------------

As discussed above, FSIS also considered whether certain Salmonella
serotypes should be considered as adulterants in all meat and poultry
products in response to the January 2020 petition submitted by Marler
Clark LLP requesting FSIS to declare 31 Salmonella serotypes that have
been associated with foodborne illness outbreaks to be adulterants of
all meat and poultry products.\68\ As noted above, FSIS denied the
petition without prejudice. However, in its response, the Agency
explained that it believes that an updated Salmonella strategy is
necessary to reduce Salmonella illnesses associated with poultry
products and that FSIS had initiated several activities designed to
gather data and information to inform and support future actions
related to Salmonella in poultry. These activities were discussed in
the Background section of this document.
---------------------------------------------------------------------------

\68\ Marler Clark LLP petition # 20-01 ``Petition for an
Interpretive Rule Declaring `Outbreak' Serotypes of Salmonella
enteritica subspecies to be Adulterants'' dated January 19, 2020.
Available at: https://www.fsis.usda.gov/policy/petitions/petition-interpretive-rule-related-certain-Salmonella-serotypes.
---------------------------------------------------------------------------

Since FSIS denied the 2020 Marler petition, many of the activities
that were initiated to inform an updated Salmonella strategy have
generated new studies and information that FSIS has determined support
a revised approach on the use of standards to address Salmonella in
final raw poultry products. For example, after FSIS issued the 2020
Marler petition denial, the Agency completed its chicken carcass
exploratory sampling program, NACMCF issued its final 2023 report, FSIS
completed the peer-reviewed 2023 risk profile as well as the peer-
reviewed 2023 risk assessments for chicken and turkey. The Agency also
held the November 3, 2022, public meeting and received written and oral
stakeholder input on the proposed Salmonella Framework that the Agency
was considering.
As part of Component Three of the draft Salmonella Framework, FSIS
stated that it was assessing whether certain levels and/or types of
Salmonella on raw poultry present an elevated risk of causing human
illness such that they should be considered adulterants. To evaluate
the status of Salmonella in raw poultry under the PPIA, FSIS has
considered stakeholder input received in response to the draft
Salmonella Framework together with the available scientific information
on Salmonella in poultry, including recommendations in the 2023 NACMCF
report, the findings of the 2023 risk profile, and the results of the
2023 quantitative risk assessments for Salmonella in chicken and
turkey. Additionally, because FSIS has relied in part on ordinary
consumer cooking practices to determine the status of pathogens as
adulterants in raw products, the Agency also considered the available
consumer behavior research to evaluate whether ordinary consumer
cooking and handling practices are able to consistently mitigate the
risk associated with certain raw poultry products contaminated with
certain levels and/or types of Salmonella. Based on its evaluation of
scientific evidence, the Agency has tentatively concluded that there
are certain raw poultry products and Salmonella levels and serotype
pairs that have characteristics that distinguish them from other raw
products contaminated with Salmonella. FSIS has also tentatively
determined that, based on its evaluation of available scientific
evidence, Salmonella, when present in these specific products at the
specified levels and serotypes, should be considered as an adulterant.
Accordingly, FSIS is proposing final product standards that would
define whether certain raw poultry products contaminated with certain
Salmonella levels and serotypes are adulterants as defined in the PPIA.
Specifically, FSIS had tentatively determined that chicken carcasses,
chicken parts, comminuted chicken, and comminuted turkey are
adulterated if they contain Salmonella at or above 10 cfu/per
milliliter or gram (10 cfu/mL(g)) in analytical portion (i.e., mL of
rinsate or gram of product) and contain any detectable level of at
least one of the Salmonella serotypes of public health significance
identified for that product. The Salmonella serotypes of public health
significance identified for chicken carcasses, chicken parts, and
comminuted chicken are Enteritidis, Typhimurium, and I 4,[5],12:i:- and
for comminuted turkey are Hadar, Typhimurium, and Muenchen. As
discussed below, these serotypes were the three most highly virulent
serotypes associated with a commodity identified in the 2023 risk
assessments. The Salmonella serotypes of public health significance
will likely change over time as the serotypes commonly associated with
human illnesses change. FSIS will continue to track annual targets for
reducing the proportion of poultry samples that contain Salmonella
serotypes of public health significance, as well as data on rates for
serotypes commonly associated with human illness to inform future
revisions to the Salmonella serotypes of public health significance.
FSIS would publicly announce and request comments on any changes to the
serotypes of public health significance in the Federal Register.
Additionally, should FSIS finalize the proposed final product
standards, the Agency intends to further evaluate and, if necessary,
refine these standards as advances in science and technology related to
pathogen levels, serotypes, and virulence genes become available. As
discussed above, if FSIS finalizes the proposed final product
standards, the Agency intends to re-evaluate the serotypes of public
health concern every 3-5 years at a minimum and whenever new
information on Salmonella serotypes associated with human illness
become available.
Under this proposed determination, chicken parts subject to the
final product standards would include legs, breasts, wings, thighs,
quarters, and halves. FSIS is not proposing final product standards for
turkey carcasses or parts because historically there have been very few
Salmonella-positive detections in turkey carcasses. Additionally, the
Agency does not

[[Page 64694]]

quantify Salmonella on turkey carcass sponge samples and has never had
a Salmonella verification sampling program for turkey parts. Thus, it
was not possible for the 2023 turkey risk assessment to assess the risk
management questions for turkey parts or provide a robust assessment on
final product standards for turkey carcasses that FSIS could use to
inform the development of final product standards for these products.
The basis for the proposed final product standards and FSIS'
proposed determination that products that contain the Salmonella levels
and serotypes identified in the proposed final product standards are
adulterated is discussed below.

B. Pathogens as Adulterants in Raw and Not-Ready-To Eat Meat and
Poultry Products

Under the FMIA (21 U.S.C. 601 et seq.) and the PPIA (21 U.S.C 451
et seq.), a meat or poultry product is adulterated if, among other
circumstances, ``it bears or contains any poisonous or deleterious
substance which may render it injurious to health; but in case the
substance is not an added substance, such article shall not be
considered adulterated . . . if the quantity of such substance in or on
such article does not ordinarily render it injurious to health'' (21
U.S.C. 601(m)(1); 21 U.S.C. 453(g)(1)). Meat and poultry products are
also adulterated if they are ``unsound, unhealthful, unwholesome, or
otherwise unfit for human food'' (21 U.S.C. 601(m)(3)); 21 U.S.C.
453(g)(3)).
Historically, most foodborne pathogens, including Salmonella, have
not been considered as adulterants of raw and other NRTE meat and
poultry products based on the assumption that ordinary cooking is
generally sufficient to destroy the pathogens.\69\ \70\ One exception
to date is E. coli O157:H:7 and certain non-O157 Shiga toxin-producing
Escherichia coli (STEC) in raw, non-intact beef products and intact
cuts that are to be further processed into non-intact products before
being distributed for consumption. These pathogens are considered
adulterants in these specific raw products because they render
``injurious to health'' what many consumers believe to be properly
cooked non-intact beef products.\71\ FSIS had also determined that when
contaminated with these pathogens, raw, non-intact beef products are
``unhealthful, unwholesome, and otherwise unfit for human food.'' \72\
---------------------------------------------------------------------------

\69\ See proposed rule ``Pathogen Reduction; Hazard Analysis and
Critical Control Point (HACCP) Systems,'' February 4, 1993 (60 FR
6774 at 6798-6799) and final rule ``Pathogen Reduction; Hazard
Analysis and Critical Control Point (HACCP) Systems,'' July 25, 1996
(61 FR 38806 at 38835.) See also Amer. Public Health Ass'n v. Butz,
511 F.2d 331 (U.S. App. DC, 1974).
\70\ When raw meat or poultry products are associated with an
illness outbreak and contain pathogens that are not considered
adulterants in those products, FSIS considers the product linked to
the illness outbreak to be adulterated under 21 U.S.C. 601(m)(3) or
453(g)(3) because the product is ``. . . unsound, unhealthful,
unwholesome, or otherwise unfit for human food'' (77 FR 72681, 72689
(Dec. 6, 2012). Products that contain an adulterant are considered
adulterated under 21 U.S.C. 601(m)(1) or 453(g)(1) even if they are
not linked to an illness outbreak.
\71\ See Texas Food Industry Association v. Espy, 870 F. Supp.
143 (1994).
\72\ Shiga-Toxin Producing Escherichia coli in Certain Raw Beef
Products (76 FR 58157, 58159).
---------------------------------------------------------------------------

When FSIS determined that certain STEC are adulterants in non-
intact raw beef products, the Agency identified characteristics
associated with both the pathogen and the product that distinguish them
from other raw products contaminated with other pathogens. Specially,
FSIS considered that these STEC had been associated with illnesses and
outbreaks, have a relatively low infectious dose, cause serious human
illness, and can survive what many consumers consider to be ordinary
preparation and cooking practices of non-intact beef products.
As discussed above, on May 1, 2024, FSIS published a final
determination to declare that NRTE breaded stuffed chicken products
that contain Salmonella at levels of 1 cfu/g or higher are adulterated
within the meaning of the PPIA.\73\ In that determination, FSIS stated
that while certain STEC have been the only pathogens to date that are
considered adulterants in a raw product, certain other pathogens may
also exhibit characteristics that would meet the standard to be
considered as adulterants in a specific raw product. In the proposed
determination, FSIS also stated that if the Agency became aware of
evidence to show that a specific pathogen and product pair presents a
significant public health risk, it would consider the factors it
identified to distinguish certain STEC from other pathogens as
adulterants in certain raw beef products to determine the pathogen's
status as an adulterant, i.e., pathogen serogroups or types associated
with human illnesses; pathogen infectious dose; pathogen and serious
human illnesses; and traditional or ordinary cooking practices. After
applying these factors to Salmonella in NRTE breaded stuffed chicken
products, FSIS decided to declare that NRTE breaded stuffed chicken
products that contain Salmonella at levels of 1 cfu/g or higher are
adulterated within the meaning of the PPIA.
---------------------------------------------------------------------------

\73\ Salmonella in Not-Ready-To-Eat Breaded Stuffed Chicken
Products; May 1, 2024 (89 FR 35033) at: https://www.fsis.usda.gov/sites/default/files/media_file/documents/FSIS-2022-0013F.pdf.
---------------------------------------------------------------------------

Specifically, FSIS determined that NRTE breaded stuffed chicken
products that contain Salmonella at 1 cfu/g or higher are adulterated
under 21 U.S.C. 453 (g)(1) because, in these particular products,
Salmonella is an added substance that may render them injurious to
health (89 FR 35034-35035). FSIS also determined that Salmonella at 1
cfu/g in NRTE breaded stuffed chicken meets the more stringent
``ordinarily injurious to health'' standard for substances that are not
added as provided in 21 U.S.C. 453(g)(1)) (89 FR 35035). Finally, FSIS
determined that NRTE breaded stuffed chicken products contaminated with
Salmonella at levels of 1 cfu/g or higher present a serious risk of
causing Salmonella illnesses and that this elevated risk of illness
makes them ``unhealthful, unwholesome, or otherwise unfit for human
food'' as defined in 21 U.S.C. 453(g)(3) (89 FR 35037).

C. The Adulteration Standard for Raw Poultry Products

Consistent with its approach used to determine the status of
certain STEC in certain raw beef products and to determine the status
of Salmonella at certain levels in NRTE breaded stuffed chicken
products, FSIS has evaluated the available information on Salmonella
serotypes associated with human illnesses, the Salmonella infectious
dose, the severity of human illnesses caused by Salmonella, and
ordinary consumer preparation practices associated with these raw
poultry products to assess the status of Salmonella in chicken
carcasses, chicken parts, comminuted chicken, and comminuted turkey.
Based on this evaluation, FSIS is proposing final product standards for
levels and serotypes of Salmonella in chicken carcasses, chicken parts,
comminuted chicken, and comminuted turkey. FSIS has also tentatively
determined that chicken carcasses, chicken parts, comminuted chicken,
and comminuted turkey that contain the Salmonella levels and serotypes
identified in the final product standard are adulterated as defined in
the PPIA because they contain a poisonous or deleterious substance that
renders them ``injurious to health'' as defined in 21 U.S.C. 453(g)(1).
Additionally, FSIS has tentatively determined that chicken carcasses,
chicken parts, comminuted chicken, and comminuted turkey that contain
the Salmonella levels and

[[Page 64695]]

serotypes identified in the final product standards are adulterated as
defined in 21 U.S.C. 453(g)(3) because their elevated risk of illness
makes them ``unhealthful, unwholesome, or otherwise unfit for human
food.'' \74\ The basis for this tentative determination is discussed
below.
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\74\ Under 21 U.S.C. 601(m)(3) of the FMIA and 21 U.S.C.
453(g)(3) of the PPIA, a meat or poultry product is adulterated ``if
it consists in whole or in part of any filthy, putrid, or decomposed
substance or is for any other reason unsound, unhealthful,
unwholesome, or otherwise unfit for human food.'' Historically, FSIS
has interpreted the phrase ``is for any other reason unsound,
unhealthful, or otherwise unfit for human food'' as providing a
separate basis for adulteration than consists of ``any filthy,
putrid, or decomposed substance.'' Thus, meat or poultry products
that FSIS has determined are ``otherwise unfit for human food''
within the meaning of 21 U.S.C. 601(m)(3) and 21 U.S.C. 453(g)(3) do
not also need to consist ``in whole or in part of any filthy,
putrid, or decomposed substance.'' For example, when raw meat or
poultry products are associated with an illness outbreak but contain
pathogens that are not considered adulterants in raw products, FSIS
has found products linked to the illness outbreak to be adulterated
under 21 U.S.C. 601(m)(3) or 21 U.S.C. 453(g)(3) because they are
``unsound, unhealthful, unwholesome or otherwise unfit for human
food'' (77 FR 72689). FSIS has also determined that certain
materials from cattle as well as the carcasses of non-ambulatory
disabled cattle are adulterated because they present a sufficient
risk of exposing humans to the bovine spongiform encephalopathy
agent such as to render them ``unfit for human food'' under 21
U.S.C. 601(m)(3) (69 FR 1862).
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1. Pathogen Serogroups or Types Associated With Human Illness
Approximately 2,500 Salmonella serotypes have been identified,\75\
though not all serotypes have been isolated from poultry. Most human
infections have been epidemiologically linked to fewer than 100
serotypes. Almost all strains of Salmonella are pathogenic as they can
invade, replicate and survive in human host cells, resulting in
potentially fatal disease,\76\ though not all are equally likely to
cause illness. To evaluate which Salmonella serotypes are most likely
to be associated with human illness, FSIS considered information from
the 2023 NACMCF report, the 2023 risk profile, and the 2023 risk
assessments.
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\75\ Brenner FW, Villar RG, Angulo FJ, Tauxe R, Swaminathan B.
Salmonella nomenclature. J Clin Microbiol. 2000 Jul;38(7):2465-7.
doi: 10.1128/JCM.38.7.2465-2467.2000. PMID: 10878026; PMCID:
PMC86943.
\76\ Shu-Kee Eng, Priyia Pusparajah, Nurul-Syakima Ab Mutalib,
Hooi-Leng Ser, Kok-Gan Chan & Learn-Han Lee (2015) Salmonella: A
review on pathogenesis, epidemiology and antibiotic resistance,
Frontiers in Life Science, 8:3, 284-293, DOI: 10.1080/
21553769.2015.1051243.
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NACMCF report. In the 2023 NACMCF report, the committee considered
how foodborne illness surveillance data on human Salmonella illnesses,
data from foodborne outbreaks associated with Salmonella in poultry,
and data on Salmonella serotypes in poultry products can be used to
identify the Salmonella serotypes of greatest public health concern
associated with specific poultry products. The report stated that the
relevant serotypes of greatest public health concern are those that are
common causes of reported human illness, are present in poultry, and
are transmitted through foods. The report noted that CDC surveillance
provides data on the frequency of diagnosed illness caused by each
serotype and that FSIS data from slaughterhouses and retail surveys can
confirm the presence and frequency of serotypes in raw poultry. The
report also concluded that outbreak investigations of foodborne
salmonellosis can provide direct evidence that foodborne transmission
of a particular serotype occurs.
The NACMCF report noted that several approaches have been used to
attribute human salmonellosis to specific foods and sources. These
include case-control studies, analysis of reported foodborne outbreaks,
and most recently, source attribution based on WGS genotyping. The
report concluded that attribution based on outbreak data and on
genotype both give the greatest weight to data from the most recent
years. NACMCF found that poultry is the leading source of human
salmonellosis, based on both reported outbreaks and genotype-based
attribution methods. The committee also stated that these data show
that a small number of serotypes account for most poultry-associated
salmonellosis led by Enteritidis, Typhimurium, I:4,5,12:i:-, Infantis,
and Heidelberg, and even fewer serogroups: groups O:4 (formerly group
B), O:7 (group C1), and O:9 (group D1).
Risk profile. In the 2023 risk profile, FSIS conducted a review of
all information on Salmonella outbreaks reported in the CDC National
Outbreak Reporting System (NORS), PubMed, and the web pages FSIS uses
for maintaining records on outbreak investigations to determine which
Salmonella serotypes or subtypes are linked to foodborne illnesses or
outbreaks from consuming specific raw and NRTE chicken or turkey
products. From these data sources, the risk profile identified 210
foodborne Salmonella outbreaks linked to poultry products between 1998
and 2020. Of these 210 foodborne Salmonella outbreaks, 84.8 percent
(178/210) were linked to chicken products and 15.2 percent (32/210) to
turkey products. Serotype information was available for 93.3 percent
(196/210) of these outbreaks, including 2.4 percent (5/210) associated
with multiple serotypes.
For the purposes of the risk profile, Salmonella subtypes
associated with human illness outbreaks attributed to consuming chicken
or turkey are referred to as ``subtypes of concern.'' The 196 outbreaks
in which serotype information was available involved 32 subtypes of
concern. Seventeen serotypes of concern were only linked to chicken
products. One serotype of concern, Reading, was linked to a turkey
product but not to chicken. There were 10 serotypes linked to both
chicken and turkey products.
According to the data compiled for the risk profile, the 210
outbreaks include 7,018 illnesses, 1,202 hospitalizations, and 10
deaths attributed to poultry products. When considering outbreaks
associated with either chicken or turkey products, nine serotypes
accounted for 85 percent (5,794/7,018) of illnesses. Each of these
subtypes caused 200 or more outbreak associated illnesses in chicken
and/or turkey from 1998-2020. The top seven subtypes associated with
chicken were Enteritidis, Heidelberg, Typhimurium, I 4,[5],12:i:-,
Montevideo, Thompson, and Infantis. The top four subtypes associated
with turkey were Enteritidis, Reading, Muenchen, and Heidelberg. The
most common subtypes of concern associated with poultry products
overall were Enteritidis, Heidelberg, Typhimurium, and I 4,[5],12:i:-.
Risk assessments. The chicken and turkey risk assessments leveraged
FSIS' 2023 risk profile to identify Salmonella serotypes in chicken and
turkey linked to foodborne illness and adopted the guidance on risk
assessment recommendations from the 2023 NACMCF report. FSIS developed
a probabilistic risk assessment model describing current Salmonella
contamination in raw poultry products and the potential human exposure
through consumption of servings derived from these raw products. Data
from FSIS microbiological baseline studies, routine PR/HACCP sampling,
and exploratory sampling programs were used to describe Salmonella in
chicken carcasses, fabricated chicken parts, and comminuted chicken and
turkey products. FSIS partnered with EpiX Analytics through a
Cooperative Agreement with the University of Maryland to incorporate
genomics into the risk assessment models developed by FSIS. FSIS
selected the grouping of serotypes into two ``clusters'' (i.e.,
``higher virulence'' and ``lower virulence'') based on the virulence
profiles, exposure in food, and foodborne epidemiological data and EpiX
Analytics then derived two virulence-adjusted Salmonella dose-

[[Page 64696]]

response models.\77\ FSIS used these dose-response models in its
quantitative risk assessment models for Salmonella in chicken and
turkey. FSIS assessed public health benefits, in terms of annual
illnesses prevented, by modeling the impact of removal of lots with
Salmonella at or above a certain level or with certain serotypes and
simulated the probability of illness per serving.
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\77\ Full details of the EpiX Analytics methodology are provided
in Appendix A of the chicken Risk Assessment in the report entitled
``Using genomics to identify nontyphoidal Salmonella serovars of
concern and estimating dose-response models amenable to risk
assessments in poultry.''
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The analysis in the chicken risk assessment found the probability
of illness from chicken contaminated with ``higher virulence''
serotypes exposures is 5.66 times larger than the probability of
illness from chicken contaminated with ``lower virulence'' serotypes.
In FSIS sampling, the average annual percentage of ``higher virulence''
serotypes is approximately 26 percent for chicken carcasses, 32 percent
for comminuted chicken product, and 35 percent for chicken parts. The
chicken risk assessment identified Enteritidis, Typhimurium, I 4,[5],
12:i:-, Hadar, and Litchfield as the five most frequent ``higher
virulence'' serotypes in chicken. The chicken risk assessment
identified Kentucky, Infantis, Schwarzengrund, Heidelberg, and Thompson
as the five most frequent ``lower virulence'' serotypes in chicken.
The analysis in the turkey risk assessment found there are 49
different serotypes in comminuted turkey products, as compared to only
19 serotypes isolated on turkey carcasses in the Agency's pathogen
reduction Salmonella sampling program. Reading and Hadar ranked as the
top two in both carcasses and comminuted, comprising more than 30
percent of the serotype samples for each commodity. Hadar was also
observed most often in the FSIS microbiological baseline studies for
Salmonella in turkey \78\ and appeared in the top ten CDC FoodNet
annual summary from 2020.\79\
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\78\ National Microbiological Baseline Data Collection Program:
Young Turkey Survey available at: https://www.fsis.usda.gov/node/1972
\79\ CDC FoodNet Reports available at: https://www.cdc.gov/foodnet/reports/index.html.
---------------------------------------------------------------------------

The turkey risk assessment identified Hadar, I 4,[5], 12:i: -,
Muenchen Typhimurium, and Saintpaul as the five most frequent ``higher
virulence'' serotypes in turkey. The turkey risk assessment identified
Reading, Infantis, Schwarzengrund, Uganda, and Agona as the five most
frequent ``lower virulence'' serotypes in turkey.
The list of serotypes of public health significance is highly
important for this framework, as it determines whether products are
adulterated as defined in the PPIA. FSIS recognizes that science
constantly evolves and therefore our understanding of virulence and
other factors will evolve over time.
The FSIS risk assessments utilized bioinformatic tools and methods
for clustering Salmonella serotypes, and an optimized new dose-response
model developed by EpiX Analytics. This model was genomically
validated, and results corresponded with other standard bioinformatic
techniques differentiating serotypes based on lineage features. Genomic
virulence factors were used for the initial grouping of serotypes and
the higher virulence serotypes of public health significance were
validated by CDC illness outcome data and FSIS sampling data. FSIS did
not rely solely on the genomic component of the risk assessment model
to determine the list of serotypes of public health significance. FSIS
developed a cohesive risk model that incorporates virulence factors,
epidemiological outcomes, and frequency of exposure and conducted
sensitivity and uncertainty analyses of the full model and the
virulence component. FSIS requests comments on the full risk model and
the uncertainty and sensitivity analyses, whether they are fit for the
purpose of determining the serotypes of public health significance, and
what model adjustments or other approaches FSIS should consider in the
determination to adapt to evolving data, technology, and analytical
methods.
FSIS recognizes that science consistently evolves, and therefore
the Agency's understanding of virulence and other factors will evolve
over time. Because the scientific understanding of virulence and other
relevant factors evolves, FSIS is requesting comments on whether the
EpiX Analytics serotype clustering and dose-response adjustment (i.e.,
risk multiplier) used the best available data and genetic factors
relevant to Salmonella risk and contamination in the United States
poultry population. Additionally, FSIS is requesting comment on
potential improvements to the serotype clustering robustness analysis
and the risk multiplier sensitivity analysis.
Final product standards serotypes of public health significance. As
noted above, as part of USDA's strategic and performance planning
process for FY2022-2026, FSIS established a new KPI targeted to reduce
the proportion of FSIS poultry samples with Salmonella serotypes
commonly associated with human illnesses.\80\ The KPI serotype list was
determined using summary statistics, namely comparison of historical
Agency sampling data for poultry products and CDC FoodNet data to
determine the Salmonella serotypes commonly associated with human
illness. It is important to note that the KPI is used as an internal
performance measure for FSIS, which is not intended to assess industry
performance, and, as such, was not externally peer reviewed. FSIS'
analysis found that these serotypes are Infantis, Enteritidis, and
Typhimurium. Thus, FSIS selected these serotypes as a KPI target for
all raw poultry.
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\80\ FY2022-2024 Food Safety Key Performance Indicator.
Available at: https://www.fsis.usda.gov/inspection/inspection-
programs/inspection-poultry-products/reducing-salmonella-poultry/
salmonella-0#:~:text=FY%202022-
2026%20Food%20Safety%20Key%20Performance%20Indicator%20A,the%20USDA%2
0Fiscal%20Year%20%28FY%29%202022-2026%20Strategic%20Plan.
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When developing the proposed final product standards, FSIS
considered incorporating the KPI serotypes as the ``serotypes of public
health significance'' as suggested by some of the comments on the
initial draft Salmonella Framework. However, after evaluating the
information on serotypes discussed above, FSIS concluded that, while
the KPI serotypes are useful for strategic and performance planning
purposes, the KPI was not a robust scientific tool by which to identify
serotypes of public health concern as adulterants. Further, the KPI
identified serotypes of public health concern for poultry as a whole,
and not by individual product (chicken v. turkey). The KPI does not
reflect the serotypes most commonly associated with illnesses from
turkey, and the chicken risk assessment determined that Infantis is not
a highly virulent serotype.
Therefore, instead of proposing serotypes of public health
significance based solely on the KPI criteria, FSIS has decided that
the proposed serotypes of public health significance should be based on
a thorough review of multiple FSIS scientific analyses in this area,
including the 2023 NACMCF report, the externally peer-reviewed 2023
risk profile, and the two externally peer-reviewed risk assessments.
Based on consideration of these scientific efforts, these serotypes are
Enteritidis, Typhimurium, and I 4,[5],12:i:- for chicken carcasses,
chicken parts, and comminuted chicken, and Hadar, Typhimurium, and
Muenchen for comminuted turkey. FSIS has determined that these
serotypes more accurately reflect serotypes most likely

[[Page 64697]]

to cause illnesses because they are based on the same epidemiological
evidence used in the risk profile and the 2023 NACMCF report, but
pivotally also include analyses conducted in the risk assessments,
which includes an additional analysis of virulence factors,
epidemiological outcomes, and frequency of exposure.
The 2023 NACMCF report, the 2023 risk profile, and the Agency's KPI
all identify Infantis as among the serotypes commonly associated with
poultry-related illnesses, the scientific evidence does not support
that the rising trend in Infantis illnesses is associated with chicken
consumption. The emergence of Infantis in FSIS chicken sampling in 2016
did not correspond to a proportional increase in human Infantis
illnesses, which have been on the rise in the United States since
2010.\81\ Put another way, given the volume of chicken consumed by the
American public--much of which is contaminated with Infantis--if it
were a high-risk poultry serotype, we would predict more Infantis
illnesses. Furthermore, the 2023 chicken risk assessment, which used
published genomic methods,\82\ also determined that Infantis is less
virulent than many other serotypes with the exception of Kentucky.
Additionally, the risk profile found that Infantis accounted for 2
percent of outbreaks identified in the CDC NORS, while I 4,[5],12:i:-
accounted for 4.1 percent of those outbreaks.
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\81\ NACMCF final report ``Response to Questions Posed by the
Food Safety and Inspection Service: Enhancing Salmonella Control in
Poultry Products'' (March 2023).
\82\ Fenske GJ, Pouzou JG, Pouillot R, Taylor DD, Costard S,
Zagmutt FJ. The genomic and epidemiological virulence patterns of
Salmonella enterica serovars in the United States. PLoS One. 2023
Dec 5;18(12):e0294624. doi: 10.1371/journal.pone.0294624. PMID:
38051743; PMCID: PMC10697515.
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However, FSIS is aware Salmonella Infantis remains of considerable
concern in terms of potential severity of illness \83\ and
antimicrobial resistance, as can be observed in its routine inclusion
in national lists of top serotypes by outbreak numbers and sporadic
case counts.\84\ CDC estimates that the serotypes of public health
significance represent 66 percent of outbreaks and 68 percent of
outbreak-associated illnesses in the past five years of outbreak data;
including Infantis as a fourth serotype increases these figures to 75
percent and 79 percent, respectively.\85\ Given the notable concern of
the Salmonella Infantis REPJFX01 strain raised by the CDC and other
public health experts, FSIS is requesting comment on the possible
inclusion of Infantis as a serotype of public health significance. As
discussed above, FSIS was not able to validate that chicken consumption
is the major direct driver of the increased Infantis rates and is
additionally asking for comment on scientific studies and data sources
on this topic that are in line with regulatory evidence guidelines.
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\83\ FSIS is aware only of results on Infantis severity of
illness that reinforce it is not a high risk serotype: Brown AC,
Chen JC, Watkins LK, et al. CTX-M-65 Extended-Spectrum [beta]-
Lactamase-Producing Salmonella enterica Serotype Infantis, United
States. Emerging Infectious Diseases. 2018;24(12):2284-2291.
doi:10.3201/eid2412.180500.
\84\ Centers for Disease Control and Prevention (CDC). BEAM
(Bacteria, Enterics, Amoeba, and Mycotics) Dashboard. Atlanta,
Georgia: U.S. Department of Health and Human Services. www.cdc.gov/ncezid/dfwed/BEAM-dashboard.html. Accessed 06/07/2024.; Centers for
Disease Control and Prevention (CDC). National Outbreak Reporting
System Dashboard. Atlanta, Georgia: U.S. Department of Health and
Human Services, CDC. Last accessed 06/07/2024. Available from URL:
wwwn.cdc.gov/norsdashboard.; Centers for Disease Control and
Prevention (CDC). FoodNet Fast Dashboard. Atlanta, Georgia: U.S.
Department of Health and Human Services, CDC. Last accessed 06/07/
2024. Available from URL: https://www.cdc.gov/foodnet/foodnet-fast.html.
\85\ These estimates are based a CDC pilot analysis of data (CDC
unpublished data) presented in 2023 to the National Advisory
Committee on Microbiological Criteria for Foods. See: NACMCF final
report ``Response to Questions Posed by the Food Safety and
Inspection Service: Enhancing Salmonella Control in Poultry
Products'' (March 13, 2023), available at: https://www.fsis.usda.gov/policy/advisory-committees/national-advisory-committee-microbiological-criteria-foods-nacmcf/2021.
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As research into Salmonella virulence factors and their gene
functions continues to develop, clustering should be revisited to
ensure reliability and consistency. FSIS took care to align the
virulence modeling in the risk assessments with epidemiological and
clinical patterns in surveillance data: however, current bioinformatics
methods are based on the serotypes that have been the consistently
highest illness causes (Enteriditis and Typhimurium) across time rather
than the full genetic landscape of Salmonella. Furthermore, lower
virulence serotypes can still outcompete higher virulence serotypes and
pose public health risks. As noted above, the list of serotypes of
public health significance is essential to this framework, as it
determines whether products are adulterated as defined in the PPIA.
FSIS requests comments on the initial proposed serotypes of public
health significance and what scientific evidence and genetic Salmonella
data sources beyond the most often studied serotypes should be
considered, in addition to that already considered, in the
identification of the most highly virulent serotypes identified in the
risk assessments, which includes a thorough review of multiple FSIS
efforts in this area, including the 2023 NACMCF report and the
externally peer reviewed 2023 risk profile.
2. Dose Considerations
As summarized in the 2023 risk profile, although Salmonella data
are limited, international and domestic outbreak investigations
associated with a variety of food products have been used to estimate
the relationship between the number of organisms consumed and the
probability of illness. These estimates, and more broadly the emergence
of dose-response modeling and quantitative risk assessment over the
past 25 years, are all based on the concept that a single bacterium is
all that is necessary to cause infection and/or illness, that is to say
the single-hit model.\86\ FSIS' evaluation and summarization of dose-
response models, as well as analysis of outbreak data where estimates
for the number of organisms consumed were available, demonstrate that
the scientific consensus is that exposure to a small number of
Salmonella organisms can result in foodborne illness.
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\86\ Teunis, P.F., & Havelaar, A.H. (2000). The Beta Poisson
dose-response model is not a single-hit model. Risk analysis: an
official publication of the Society for Risk Analysis, 20(4), 513-
520. https://doi.org/10.1111/0272-4332.204048.
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In a study published in 2010 (the Teunis 2010 study), and included
in the 2023 risk profile, using a dose-response model approach
utilizing outbreak data, and accounting for variation among outbreaks
represented by the data, the Salmonella median illness dose was 36 cfus
(with 95 percent prediction interval of 0.69-1.26x10\7\ cfu).\87\ The
median illness dose refers to the dose at which 50 percent of
individuals in an exposed population will experience symptomatic
illness. The median illness dose and its prediction interval reflect
variability among outbreak strains and exposed populations and
uncertainty about the dose-response relationship. Thus, it serves as a
useful metric for comparing the pathogenicity of different serotypes.
Additionally, the World Health Organization Food and Agriculture
Organization of the United Nations developed a dose-response approach
for risk assessments for Salmonella.\88\ Also

[[Page 64698]]

using outbreaks, the model estimated a 13 percent chance of becoming
ill if ingesting an average dose of 100 organisms. Even at the level of
1 organism ingested, there was still a non-zero chance of illness (0.25
percent).
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\87\ Teunis P.F., et al., Dose-response modeling of Salmonella
using outbreak data. Int J Food Microbiol, 2010. 144(2): p. 243-9;
https://doi.org/10.1016/j.ijfoodmicro.2010.09.026.
\88\ World Health Organization, Risk assessment of Salmonella in
eggs and broiler chickens, March 25, 2002. Available at: https://www.who.int/publications/i/item/9291562293.
---------------------------------------------------------------------------

A study published after the 2023 FSIS risk profile was peer-
reviewed revisited the 2010 Teunis study discussed above.\89\ Using
outbreak serotype data, and accounting for variation among outbreaks
within a particular serotype, the median Salmonella dose predicted to
result in 50 percent of exposed individuals becoming ill
(IllD50) was 3,360 cfu (95 percent range: 18-3.2x10\9\),
1,500 cfu (38-8.8x10\7\), and 1 cfu (0.69-1.0x10\6\) for Enteritidis,
Typhimurium and Infantis, respectively. For the same study, the median
Salmonella dose predicted to result in 1 percent of exposed individuals
becoming ill (IllD01) was 0.6 cfu (95 percent range: 0.24-
1.9), 9.9 cfu (0.32-57), and 0.07 cfu (0.01-2.0x10\4\) for Enteritidis,
Typhimurium and Infantis, respectively. These results describe that
individuals exposed to small doses of Salmonella can experience
symptomatic illness. Other Salmonella serotypes were also found to
cause illness at small doses including Heidelberg
(IllD50=323 cfu and IllD01=1 cfu) and
Schwarzengrund (IllD50=0.8 cfu and IllD01=0.04
cfu).
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\89\ Teunis P.F.M. Dose response for Salmonella Typhimurium and
Enteritidis and other nontyphoid enteric salmonellae. Epidemics 41
(2022) 100653; https://doi.org/10.1016/j.epidem.2022.100653.
---------------------------------------------------------------------------

Furthermore, the 2023 FSIS risk assessments developed two
virulence-adjusted dose-response models (one for low virulence
Salmonella serotypes, and another for high virulence Salmonella
serotypes), which utilize the work described in the 2023 FSIS risk
profile to poultry specific serotypes. The high virulence dose-response
model (which includes the serotypes of public health significance) was
estimated using outbreak data and employed a beta-Poisson model of
infection for a given dose as outlined in the 2023 risk profile. Risk
multipliers, derived from epidemiological outbreak data attributed to
poultry sources, with consideration of prevalence in animal sources
from FSIS poultry sampling programs, were then used to scale the
relative risk of illness from exposures to each cluster. The
probability of illness from consuming chicken containing high virulence
Salmonella serotypes exposures is 5.66 times greater than the
probability of illness from exposure to chicken products containing low
virulence Salmonella serotypes. The dose-response findings of the 2023
risk assessment rely on the single-hit model, and the virulence
adjusted dose-response models estimate of a 1 in 100 probability of
illness at 1 cfu of high virulence Salmonella per serving and a 0.2 in
100 probability of illnesses at 1 cfu of low virulence Salmonella per
serving. While the median illness is not attained by the low virulence
Salmonella dose response model, the median illness dose described by
the dose-response model for serotypes of public health significance is
approximately 2000 cfu.
As summarized in the 2023 risk profile, five Salmonella foodborne
outbreaks have shown that Salmonella can cause illness from exposure of
10 or fewer organisms per person.\90\Additionally, several outbreaks
from a range of Salmonella serotypes in various food products have
shown that exposure from 11 to 420 organisms per person can result in
illness.\91\ Thus, in these published studies, illnesses resulted from
doses ranging from 1 to 420 Salmonella organisms per person.
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\90\ Killalea, D., et al., International Epidemiological and
Microbiological Study of Outbreak of Salmonella Agona Infection from
a Ready to Eat Savoury Snack--I: England and Wales and the United
States. 1996, British Medical Journal Publishing Group.; Shohat, T.,
et al., International Epidemiological and Microbiological Study of
Outbreak of Salmonella Agona Infection from a Ready to Eat Savoury
Snack--Ii: Israel. BMJ, 1996. 313(7065): p. 1107-1109.; D'aoust,
J.Y. and J.Y.D. Aoust, Infective Dose of Salmonella Typhimurium in
Cheddar Cheese. American Journal of Epidemiology, 1985. 122(4): p.
717-720.; D'aoust, J.Y., D.W. Warburton, and A.M. Sewell, Salmonella
Typhimurium Phage-Type 10 from Cheddar Cheese Implicated in a Major
Canadian Foodborne Outbreak. Journal of Food Protection, 1985.
48(12): p. 1062-1066.; Kapperud, G., et al., Outbreak of Salmonella
Typhimurium Infection Traced to Contaminated Chocolate and Caused by
a Strain Lacking the 60-Megadalton Virulence Plasmid. J Clin
Microbiol, 1990. 28(12): p. 2597-601.; Hockin, J.C. et al., An
International Outbreak of Salmonella Nima from Imported Chocolate. J
Food Prot. 1989. 52(1): p. 51-54.; Lehmacher, A., Bockemuhl, J., and
Aleksic. S. Nationwide outbreak of human salmonellosis in Germany
due to contaminated paprika and paprika-powdered potato chips. 1995.
Epidemiol Infect. 115: p. 501-11.
\91\ Kasuga F.et al., Archiving of food samples from restaurants
and caterers--Quantitative profiling of outbreaks of foodborne
Salmonella in Japan. Journal of Food Protection, 2004. 67: p. 2024-
2032; Blaser, M.J., and Newman, L.S. A review of human
salmonellosis: I. Infective dose. Rev Infect Dis., 1982.4: p.1096-
106; Abe, K., N. et al., Prolonged incubation period of
Salmonellosis associated with low bacterial doses. Journal of food
protection, 2004. 67: p. 2735-2740; Hara-Kudo, Y. and K. Takatori,
Contamination level and ingestion dose of foodborne pathogens
associated with infections. Epidemiology and Infection, 2011. 139:
p. 1505-1510; Hennessy T.W., et al., A national outbreak of
Salmonella enteritidis infections from ice cream. N Engl J Med,
1996. 334(20): p. 1281-6; Hedberg C.W., et al., A multistate
outbreak of Salmonella javiana and Salmonella oranienburg infections
due to consumption of contaminated cheese. JAMA, 1992. 268(22): p.
3203-7; Todd, E.C., et al., Outbreaks where food workers have been
implicated in the spread of foodborne disease. Part 4. Infective
doses and pathogen carriage. J Food Prot, 2004. 71: p. 2339-73;
Scheil W., et al., A South Australian Mdbandaka outbreak
investigation using a database to select controls. Aust NZ J Public
Health, 1998. 22(5): p. 536-9; Tamber, S., E. Swist, and D. Oudit,
Physicochemical and bacteriological characteristics of organic
sprouted chia and flax seed powders implicated in a foodborne
Salmonellosis outbreak. Journal of Food Protection, 2016. 79(5): p.
703-709.
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The 2023 risk profile identified 32 Salmonella serotypes of concern
linked to foodborne Salmonella outbreaks from chicken and turkey
products. These identified serotypes of concern informed all subsequent
risk management questions, including whether exposure to a small number
of these serotypes result in foodborne illness. Because the Salmonella
serotypes of public health significance identified in the final product
standards are among the 32 Salmonella serotypes of concern identified
in the risk profile and risk assessments, it is reasonable to conclude
that the serotypes of public health significance in the final product
standards all cause illness at a relatively low dose.
3. Severity of Illnesses
The 2023 risk profile found that exposure to the profile's
Salmonella subtypes of concern, which include the final product
standards serotypes of public health significance, can cause severe or
debilitating human health outcomes. Although the symptoms of Salmonella
infections are typically not reported to be as severe as some of those
associated with STEC, Salmonella can cause bloody diarrhea, fever,
abdominal cramps, nausea, and vomiting. In some instances, Salmonella
enters the blood stream and makes its way to other areas of the body
including, but not limited to, the heart, lung, bone, joints and the
central nervous system.\92\ This can result in severe illness requiring
hospitalizations and even death, especially in vulnerable populations,
such as very young, elderly, and immunocompromised individuals. Even
when Salmonella is no longer detectable in the body, prior Salmonella
illness has also been associated with an increased risk in colon
cancer.\93\ Also, the illness can cause debilitating, long-lasting
conditions including inflammatory bowel disease, irritable bowel
syndrome and reactive arthritis.
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\92\ Batz, M.B., et al., Long-Term consequences of foodborne
illness. Infect Dis Clin North Am, Sept 2013. 28(3) p. 599-661;
Hohmann, E.L., Nontyphoidal Salmonellosis, Clin Infect Dis, Sept
2001. 32 p. 263-269; Heymann, D. Salmonellosis. Control of
Communicable Disease Manual, 2021.
\93\ Mughini-Gras, L. et al. Increased colon cancer risk after
severe Salmonella infection. PLoS ONE, 2018. 13(1): p. 1-19, https://doi.org/10.1371/journal.pone.0189721.

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[[Page 64699]]

Furthermore, a study that allows for a comparison of case-fatality
proportions of both Salmonella and STEC O157 demonstrates a higher
frequency of deaths among Salmonella cases than among STEC O157
cases.\94\ The estimated annual domestic foodborne illnesses reported
in the study were 1,027,561 and 63,153 for Salmonella and STEC O157,
respectively. Annual deaths from domestic foodborne illnesses are 378
and 20 for Salmonella and STEC O157, respectively. Therefore,
Salmonella deaths occur at a frequency of 4 per 10,000 illnesses, while
STEC O157 deaths occur at a frequency of 3 per 10,000 illnesses.
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\94\ Scallan, et al., 2011.
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4. Consumer Cooking Practices
As noted above, until recently, with the publication of the
proposed determination on Salmonella in NRTE breaded stuffed chicken
products, FSIS historically has not taken the position that certain
Salmonella levels or serotypes render raw poultry products adulterated
as defined in the PPIA. This position was based in part on the fact
that proper cooking kills pathogens on raw product. However, as
discussed below, several consumer behavior research studies suggest
that ordinary consumer cooking and preparation practices for chicken
carcasses, chicken parts, comminuted chicken, and comminuted turkey do
not provide adequate assurance that these products will not be
contaminated when consumed.
Consumer behavior research. FSIS recommends cooking poultry
products until the center of the thickest part of the meat reaches a
minimum internal temperature of 165 [deg]F measured by using a
thermometer to eliminate the presence of Salmonella and other foodborne
pathogens.\95\ However, although using a thermometer is the only
reliable way to ensure that poultry is properly cooked, studies show
that many consumers do not ordinarily use a thermometer to determine
whether whole chicken, chicken parts, comminuted chicken, and
comminuted turkey have reached an internal temperature sufficient to
destroy Salmonella. Studies also show that many consumers that do use a
thermometer do not always do so correctly.
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\95\ FSIS Safe Minimum Internal Temperature Chart. 2020;
Available at: https://www.fsis.usda.gov/food-safety/safe-food-handling-and-preparation/food-safety-basics/safe-temperature-chart.
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In a study published in 2017, a web-enabled panel survey of U.S.
adult grocery shoppers (n = 1,504) was conducted to describe consumers'
handling and preparation practices for raw poultry.\96\ The purpose of
the study was to characterize consumer food thermometer use and
barriers to use. The study found that of the 62 percent of the survey
respondents who reported owning a food thermometer, thermometer usage
was highest among those cooking whole turkeys (73.2 percent). Fewer
respondents reported using a thermometer when cooking whole chickens
(56.7 percent), chicken breasts or other parts (26.3%), and meatloaf or
a similar dish containing ground chicken or turkey (22.8 percent).
Reported thermometer use was lowest among respondents cooking patties
made with ground chicken or turkey (11.7 percent).
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\96\ KM Kosa, et al. (2017). Barriers to Using a Food
Thermometer When Cooking Poultry at Home: Results from a National
Survey. Food Protection Trends, 37/2, 116-125, available at: https://www.foodprotection.org/files/food-protection-trends/mar-apr-17-kosa.pdf.
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Participants who reported owning a food thermometer identified
various reasons for not using a thermometer the last time they cooked
poultry at home. For all cuts of poultry, the most common reason
reported for not using a thermometer was use of another method to
determine that the product was properly cooked (49.8 to 61.5 percent of
respondents). The next most common reason selected was that the
respondent never thought to use a thermometer (27 to 37.6 percent of
respondents), which the researcher concluded suggests that these
respondents do not consider it very important to use a food
thermometer.
Of the respondents that reported using another method instead of a
food thermometer, most reported that they determined that poultry is
properly cooked by using visual cues, i.e., color, juice clarity, and
cleanliness of probing utensil. Of the 61.5 percent of the respondents
that reported using another method to determine that a whole turkey or
chicken is properly cooked, 42.2 percent cut the food to check that it
was no longer pink, 42.2 percent relied on cooking time, and 41 percent
checked that the juices ran clear. Of the 56.1 percent of the
respondents that reported using another method to determine that
chicken and turkey parts were properly cooked, 67.6 percent cut the
food to check that it was no longer pink, 46.2 percent relied on
cooking time and 40 percent checked that the juices ran clear. And of
the 49 percent of the respondents that reported using another method to
determine whether ground chicken or turkey was properly cooked, 61.5
percent inserted a knife, toothpick, or other utensil to see if it came
out clean, 55.4 percent relied on cooking time, and 21.0 percent cut
the food to check that it was no longer pink.
In an observational study published in 2016, 101 participants were
observed as they prepared poultry and egg items to determine whether
they followed food safety guidelines.\97\ The poultry items prepared
for the study were a baked whole chicken breast and a pan-fried ground
turkey patty. The study found that thermometer use for all products was
low. Only 37 percent of participants used a thermometer to determine
that a chicken breast was properly cooked, and only 22 percent used a
thermometer to determine that a turkey patty was properly cooked. For
the chicken breast, the most common method used to determine doneness
was cutting into the chicken (50 percent), followed by color (33
percent) and thermometer use (33 percent). For the turkey patty, the
most common indicator used was color (39 percent), followed by cutting
into it (30 percent), using a thermometer (22 percent), and looking at
the juices (18 percent). The study also found that the participants who
used a food thermometer often would use other methods, such as cutting
into them or observing the juices, to determine if the poultry items
were properly cooked.
---------------------------------------------------------------------------

\97\ Maughan, et al. (2016). Food Handling Behaviors Observed in
Consumers When Cooking Poultry and Eggs. Journal of Food Protection,
79:6, 970-977, available at: https://www.sciencedirect.com/science/article/pii/S0362028X22080814?via%3Dihub.
---------------------------------------------------------------------------

The study also highlighted the importance of correctly using a
thermometer to determine that poultry is properly cooked. Of the study
participants who used a thermometer, 36 percent did not use it
correctly in the chicken breast, the turkey patty, or both. The study
also found that there was no statistical difference between a
participant who did and did not use a thermometer in achieving an end
point temperature of at least 165 [deg]F in both the chicken breast and
the turkey patty. Seventy-eight percent of participants that used a
thermometer to cook the chicken breast reached a final internal
temperature above 165 [deg]F, compared to 75 percent for those who did
not use a thermometer. Seventy-seven percent of participants who used a
thermometer to cook a turkey patty reached a final internal temperature
of at least 165 [deg]F, compared to 66 percent of participants who did
not use a thermometer.

[[Page 64700]]

In another observational study published in 2014,\98\ 120
volunteers were observed as they prepared chicken and salad in their
homes. The study participants chose the manner of chicken preparation.
Three volunteers prepared whole chicken, and all others prepared
chicken parts. The study found that the most common method of
determining whether the chicken was properly cooked was appearance. In
response to a questionnaire administered after meal preparation, the
study participants stated that to determine whether chicken was
properly cooked, they looked for white colored meat, absence of blood
or pink spots, and firm meat. The study found that 40 percent of the
chicken that the participants considered to be properly cooked
registered a temperature below 165 [deg]F.
---------------------------------------------------------------------------

\98\ Bruhn, C.M. (2014). Chicken preparation in the home: An
observational study. Food Protection Trends, 34(5):318-330.
Available at: https://www.proquest.com/trade-journals/chicken-preparation-home-observational-study/docview/1640787777/se-2.
---------------------------------------------------------------------------

In this study, fewer than 5 percent of the participants voluntarily
used a thermometer to record chicken temperature during meal
preparation. When asked by the researcher if they wanted to check the
cooked chicken's temperature, 34 percent of the participants checked
the internal temperature using either their own thermometer or the
thermometer provided by the researcher. When chicken temperature was
taken, the internal temperature of 60 percent of the cooked chicken
registered 165 [deg]F or above. However, 39 percent of households
stopped cooking even though the internal temperature of the poultry
registered below 165 [deg]F.
A 2020 study used a randomized experimental design and direct
observation of meal preparation to test the effectiveness of a USDA
food safety video intervention for consumer thermometer use.\99\ The
study was conducted in test kitchen facilities in which cameras
recorded participants' meal preparation from beginning to end. A total
of 383 people participated in the study, 201 in the control group (the
group that did not watch the food safety video) and 182 in the
treatment group. Before preparing the meal, the treatment group watched
a 3-minute USDA food safety video on the importance of using a food
thermometer. Participants in the control and treatment groups were
observed while cooking turkey burgers and preparing a salad to
determine whether the participants used a thermometer to determine
whether the turkey patties were properly cooked. Following meal
preparation, all participants responded to a post observation interview
about food handling behaviors.
---------------------------------------------------------------------------

\99\ Duong M, Shumaker ET, Cates SC, Shelley L, Goodson L,
Bernstein C, Lavallee A, Kirchner M, Goulter R, Jaykus LA, Chapman B
(2020). An Observational Study of Thermometer Use by Consumers When
Preparing Ground Turkey Patties. J Food Prot. 83(7):1167-1174.
Available at: https://www.sciencedirect.com/science/article/pii/S0362028X2210339X.
---------------------------------------------------------------------------

Sixty-one percent of the control group participants and 63 percent
of the treatment group participants reported owning a food thermometer,
which is consistent with the percentage of the respondents that
reported owning a food thermometer in the 2017 study discussed above
(62 percent). During the meal preparation session, the control group
used a thermometer to determine whether the turkey patties were
properly cooked 34 percent of the time, while the treatment group used
a thermometer 75 percent of the time. The control participants were
also less likely to insert the thermometer into the side of the patty
(23 percent), the recommended practice, than the treatment participants
(52 percent). Of the participants that used a thermometer and for whom
temperature data were available, the turkey patties were observed to
reach an internal temperature of 165 [deg]F 54 percent of the time for
the control group and 73 percent of the time for the treatment group.
Thus, while both the control and treatment groups were likely to own a
food thermometer, the control group was much less likely to use a food
thermometer, correctly place a thermometer, and cook patties to a safe
internal temperature than the treatment group.
The study also addressed whether the participants used methods
other than a thermometer to determine whether the turkey patty was
properly cooked. The study found that 45 percent of all participants
used a method other than a thermometer to determine that the turkey
patty was done cooking. Among participants who did not use the
thermometer and for whom usable data were available, 46 percent of
control group participants and 29 percent of the treatment group
participants relied on the firmness or texture of the patty to
determine that it was properly cooked, and 4 percent in the control
group and 16 percent in the treatment group relied on patty color.
Twenty-five percent of control group and 42 percent of treatment group
were observed using both firmness and color of the patty.
Thus, consumer research shows that, rather than using a thermometer
to check the internal temperature of whole chicken, chicken parts,
comminuted chicken products, and comminuted turkey products, many
consumers ordinarily rely on visual and textural cues to determine that
these products are properly cooked. However, because these subjective
cues have not been correlated with safe internal cooking temperature,
they are unreliable for gauging whether poultry products have reached
an internal temperature sufficient to destroy Salmonella that may be
present.\100\ As noted above, a 2014 observational study found that 40
percent of the chicken that participants considered to be properly
cooked based on subjective cues registered a temperature below 165
[deg]F. The 2017 survey study discussed above also cited a published
summary of food safety literature that concluded that 70 percent of
chicken pieces visually judged by consumers as ``done'' had not reached
a safe internal temperature.\101\ A European study that assessed the
effect of household cooking methods on the presence and numbers of
Salmonella Typhimurium in different types of raw poultry products found
that improper cooking produced inadequate heat treatments that did not
fully eliminate Salmonella from the products even when the initial
contamination levels were as low as 10 cfu/g.\102\ Thus, based on its
review of the available consumer research, FSIS has concluded that many
consumers do not cook chicken carcasses, chicken parts, comminuted
chicken, and comminuted turkey thoroughly and therefore, ordinary
consumer cooking practices associated with these products fail to
provide adequate assurance that the products will not be contaminated
when consumed.
---------------------------------------------------------------------------

\100\ M. Duong et. al (2020).
\101\ Kosa, et al. (2017) citing CJ Byrd-Bredbenner et al.
(2013.) Food safety in home kitchens: a synthesis of the literature.
Int. J. Environ Res Publ Hlth 10:4060-4085.
\102\ Roccato A, Uyttendaele M, Cibin V, Barrucci F, Cappa V,
Zavagnin P, Longo A, Ricci A (2015). Survival of Salmonella
Typhimurium in poultry-based meat preparations during grilling,
frying and baking. Int J Food Microbiol 197:1-8. Available at:
https://www.sciencedirect.com/science/article/pii/S0168160514006011?via%3Dihub.
---------------------------------------------------------------------------

Cross-Contamination. In addition to consumer behavior research that
found that many consumers ordinarily rely on visual and textural cues
to determine that raw chicken and turkey products are properly cooked,
recent studies also found that there are other ordinary consumer
practices that create conditions for Salmonella exposure from raw
poultry regardless of whether the products are properly cooked.
Consumer hand washing practices are

[[Page 64701]]

one example of this cross-contamination concern.
A 2015 observational study of consumers handling raw poultry as
part of an at-home meal preparation event found that hands were washed
12 percent of the time after handling raw poultry.\103\ Of note, 100
percent of the same study group responded on a pre-observation
questionnaire that they washed their hands before and after handling
raw poultry. Further, a 2016 observational study found that, during the
preparation and cooking process, 40 percent of participants correctly
washed their hands after handling raw whole chicken carcasses, and 46
percent correctly washed their hands after handling the raw ground
turkey product.\104\
---------------------------------------------------------------------------

\103\ E Mazengia, et al. (2015). Direct Observational Study of
the Risk of Cross-Contamination during Raw Poultry Handling:
Practices in Private Homes. Food Protection Trends, 35/1, 8-23.
Available at: https://www.foodprotection.org/files/food-protection-trends/JAN-FEB-15-mazengia.pdf.
\104\ Maughan, et al. (2016). Food Handling Behaviors Observed
in Consumers When Cooking Poultry and Eggs. Journal of Food
Protection, 79/6, 970-977. Available at: https://www.sciencedirect.com/science/article/pii/S0362028X22080814?via%3Dihub. For the purposes of the study, proper
hand washing was defined as washing hands with soap for a minimum of
20 seconds immediately after touching the raw product and without
touching anything else.
---------------------------------------------------------------------------

Research shows that washing poultry can spread bacteria to kitchen
surfaces and other foods.\105\ Studies also show that washing or
rinsing raw poultry is a pervasive consumer preparation practice that
raises cross-contamination concerns. For example, a 2019 survey of food
handling practices indicated that a lack of adherence to the
recommended practice to not wash or rinse raw poultry may have
widespread impact on two age groups more susceptible to contracting
foodborne illness--young children and older adults.\106\ The Web-based
survey found that only 39 percent of parents of young children (aged 5
years or younger) and only 31 percent of older adults (aged 60 years or
older) reported not rinsing or washing raw poultry. Further, in a 2014
study on observed consumer handling behavior, 120 participants were
asked to prepare in their home kitchen a chicken product and a salad.
Before the observation, the participants were asked to select and
purchase the ingredients, including a raw chicken carcass or part. The
study found that 45 percent of the participants washed the raw chicken
at the start of preparation.\107\
---------------------------------------------------------------------------

\105\ Food Safety Consumer Research Project: Meal Preparation
Experiment Related to Poultry Washing Final Report (August 20,
2019). Available at: https://www.fsis.usda.gov/sites/default/files/media_file/2021-02/FSCRP_Year%2B2_Final_Aug2019.pdf.
\106\ Kosa, KM, et al. (2019). Older Adults and Parents of Young
Children Have Different Handling Practices for Raw Poultry. Journal
of Food Protection, 82(2), 200-206, available at: https://pubmed.ncbi.nlm.nih.gov/30673351/.
\107\ Bruhn, C.M. (2014). Chicken Preparation in the Home: An
Observational Study. Food Protection Trends, 34/5, 318-330,
available at: https://www.proquest.com/trade-journals/chicken-preparation-home-observational-study/docview/1640787777/se-2.
---------------------------------------------------------------------------

Additional research indicates that food handling education on the
recommendation to not wash or rinse raw poultry may have limited impact
on consumer behavior. In 2016, a four-week intervention survey study
exposed participants to an educational pilot program developed to raise
awareness and influence consumers to not wash raw poultry.\108\ The
results indicated that, while the program improved both knowledge and
behavior of participants toward not washing raw poultry, the majority
of consumers that viewed and understood the material still reported
washing or rinsing raw poultry after the intervention program
concluded.\109\ These studies indicate that cross-contamination events
are common during poultry handling in home kitchens, and that
consumers' knowledge of proper food handling is often not correlated to
safe handling behaviors.
---------------------------------------------------------------------------

\108\ Henley, S., et al. (2016). Don't Wash Your Chicken!: A
Food Safety Education Campaign to Address a Common Food Mishandling
Practice. Food Protection Trends, 36/1, 43-53, available at: https://www.foodprotection.org/files/food-protection-trends/jan-feb-16-henley.pdf.
\109\ Twenty-five percent of consumers in the intervention group
reported not washing whole raw poultry, compared to 20.1 percent of
consumers in the control group. Sixteen-point-three percent of
consumers in the intervention group reported not washing small cuts
of raw poultry, compared to 9.8 percent of consumers in the control
group.
---------------------------------------------------------------------------

E. Risk per Serving, Salmonella Levels, and Proposed Determination

1. Final Product Standards Salmonella Level and Risk per Serving
Salmonella contamination and levels. The 2023 risk assessments
include analyses of FSIS testing of chicken and turkey products that
show that the proportion of raw chicken carcasses, chicken parts,
comminuted chicken and comminuted turkey products contaminated with
Salmonella is very low and that the levels are very low for
contaminated products (Table 3).

Table 3--Estimated Amount of Test Positive Samples per Salmonella Threshold
----------------------------------------------------------------------------------------------------------------
Chicken Chicken parts Comminuted Comminuted
carcasses (%) (%) chicken (%) turkey (%)
----------------------------------------------------------------------------------------------------------------
Tests Salmonella Negative....................... 96.92 93.31 72.90 84.26
Tests Salmonella Positive....................... 3.08 6.69 27.10 15.74
>=1 cfu/mL or /g............................ 9 2 11 12
>=10 cfu/mL or /g........................... 1 0.07 3 4
>=100 cfu/mL or /g.......................... 0.10 <0.01 1 1
----------------------------------------------------------------------------------------------------------------

Approximately 97 percent of chicken carcasses and 93 percent of
chicken parts test negative for Salmonella (i.e., results are below the
0.03 cfu/mL limit of detection (LOD)). Approximately 73 percent of
comminuted chicken and 84 percent of comminuted turkey test results are
below the 0.003 cfu/g LOD. Of the 3 percent of chicken carcasses that
test positive for Salmonella at the end of production, only 1 percent
have Salmonella levels at or above 10 cfu/mL, and 0.10 percent have
Salmonella levels at or above 100 cfu/mL. Of the chicken parts that
test positive for Salmonella, only 0.07 percent have levels at or above
10 cfu/mL, and less than 0.01 percent were found to have levels at or
above 100 cfu/mL. Of the 27 percent of comminuted chicken products that
test positive for Salmonella, only 3 percent have levels at or above 10
cfu/g, and 1 percent have levels at or above 100 cfu/g. Finally, of the
16 percent of comminuted turkey products that test positive for
Salmonella, only 4 percent have levels at or above 10 cfu/g, and 1
percent have levels at or above 100 cfu/g. Thus, given that the
majority of chicken carcasses, chicken parts, comminuted chicken, and
comminuted turkey have Salmonella at levels below 0.03 cfu/

[[Page 64702]]

mL(g), FSIS testing data shows that Salmonella levels at or above 10
cfu/mL(g) represent comparatively higher levels of contamination that
are infrequently identified in these raw poultry products.
Risk per Serving. The risk assessments also quantify and compare
the probability of illness associated with chicken carcasses, chicken
parts, comminuted chicken, and comminuted turkey contaminated with
Salmonella levels at or above 10 cfu/mL(g) with the average level of
contamination for these raw products. The risk assessments used two
dose-response models to provide a description of risk of illness per
serving for Salmonella from chicken carcasses, chicken parts,
comminuted chicken, and comminuted turkey products, when combined with
an attenuation distribution. This attenuation distribution describes
the variety of activities that occur between FSIS sampling a final
product lot and a consumer ingesting a serving from that lot. These
activities include product mixing, transportation, and cooking--all of
which can result in both Salmonella growth and die off.
A summary of probability of illness per serving for the main
scenarios that were considered in the risk assessments is provided in
Table 4. The average Salmonella level for product lots that test at or
above each threshold level are provided, along with the average dose
consumed, i.e., the level after attenuation, and likelihood that
consumers are exposed to such servings.
The model-derived baseline probability of illness for chicken
carcasses is 0.2 illnesses per 100,000 servings, for chicken parts is
0.3 illnesses per 100,000 servings, and 2.5 illnesses per 100,000
servings for comminuted chicken, and 2.5 illnesses per 100,000 servings
for comminuted turkey. Comparison of the threshold probability of
illness to the baseline quantifies how much higher than average the
risk per serving is for each scenario.
Table 4--Average characteristics (level, dose, and probability of
illness by serocluster) of failing lots for Salmonella threshold level
scenarios in FSIS-sampled products under consideration and the overall
likelihood of consumer exposure. The serotypes of public health
significance (Enteritidis, Typhimurium, and I 4,[5],12:i:- for chicken
products and Hadar, Typhimurium and Muenchen for Comminuted turkey) are
among the higher virulence Serotype Cluster

Salmonella Threshold Level Scenarios Under Consideration
[cfu/mL or g]
----------------------------------------------------------------------------------------------------------------
Measurement Product type 0.003 0.033 1 10 100
----------------------------------------------------------------------------------------------------------------
Average level for failing Chicken 0.48 1.65 16 97 682
lots (cfu/mL(g)). Carcasses.
Chicken Parts... 0.08 0.30 4 33 281
Comminuted 17 37 163 582 2,572
Chicken.
Comminuted 163 348 1,373 4,249 15,479
Turkey.
Average dose consumed for Chicken 0.08 0.26 3 15 108
average failing lot (cfu/ Carcasses.
serving).
Chicken Parts... 0.01 0.05 0.67 5 45
Comminuted 3 6 26 92 408
Chicken.
Comminuted 26 55 218 673 2,453
Turkey.
Probability of illness per Chicken 23 54 224 612 1,598
100,000 servings *, high Carcasses.
virulence.
Chicken Parts... 6 16 100 340 1,050
Comminuted 235 363 800 1,486 2,849
Chicken.
Comminuted 801 1,166 2,184 3,490 5,660
Turkey.
OR
Probability of illness per Chicken 4 9 42 119 329
100,000 servings *, low Carcasses.
virulence.
Chicken Parts... 1 3 18 64 211
Comminuted 44 69 158 305 611
Chicken.
Comminuted 158 235 460 761 1,287
Turkey.
Likelihood of consumer Chicken 11% 3% 0.27% 0.03% <0.01%
exposure to raw product at Carcasses.
or above initial level.
Chicken Parts... 31% 7% 0.17% <0.01% <0.01%
Comminuted 27% 13% 3% 0.79% 0.17%
Chicken.
Comminuted 16% 7% 2% 0.60% 0.16%
Turkey.
----------------------------------------------------------------------------------------------------------------
* Given average initial level multiplied by attenuation distribution.

As illustrated in Table 4, the risk assessments found that the
probability of illness for servings of raw chicken carcasses that are
contaminated with Salmonella levels at or above 10 cfu/mL and contain a
serotype of public health significance is 612 illnesses per 100,000
servings of raw chicken carcasses, while the average probability of
illness is 0.3 illnesses per 100,000 servings; the great majority of
which have levels far below 10 cfu/mL. Therefore, servings from
production lots of raw chicken carcasses that test positive for
Salmonella at levels of 10 cfu/mL or greater with a serotype of public
health significance are 2,000-fold (i.e., ~ 612/0.3) more likely to
cause illness than the average across all chicken carcass servings.
Thus, while there is a relatively low probability that individuals will
be exposed to carcasses that contain Salmonella at 10 cfu/mL, if
exposed, there is a much higher probability of illness, i.e., 2,000-
fold, when compared to exposure to the majority of servings from
chicken carcasses.
For raw chicken parts, the risk assessment found that chicken parts
servings that are contaminated with Salmonella levels at or above 10
cfu/mL at the end of production and contain a serotype of public health
significance have a probability of illness of 340 illnesses per 100,000
servings, while the average probability of illness is 0.3 per 100,000
servings for all servings; the great majority of which have levels

[[Page 64703]]

much below 10 cfu/mL. Therefore, servings from production lots of raw
chicken parts that test positive for Salmonella at levels at or above
10 cfu/mL with a serotype of public health significance are 1,100-fold
(i.e., ~340/0.3) more likely to cause illness than the average across
all chicken parts servings. Thus, while there is a relatively low
probability that consumers will be exposed to chicken parts that
contain Salmonella at 10 cfu/mL, if exposed, there is a much higher
probability of illness, i.e., 1,100-fold, when compared to exposure to
the majority of servings from raw chicken parts.
For raw comminuted chicken servings, the risk assessments found
that products that are contaminated with at least 10 cfu/g of
Salmonella at the end of production and contain a serotype of public
health significance have a 1,500 per 100,000 servings probability of
illness, while average probability of illness is 2.5 per 100,000
servings for all servings; the majority of which have levels below 10
cfu/g. Therefore, servings from production lots of comminuted chicken
that test positive for Salmonella at or above 10 cfu/g with a serotype
of public health significance are 590-fold (i.e., ~1,500/2.5) more
likely to cause illness than the average across all comminuted chicken
servings. Thus, while there is a relatively low probably that consumers
will be exposed to comminuted chicken that contains Salmonella at 10
cfu/g, if exposed, there is a much higher probability of illness, i.e.,
590-fold, when compared to the majority of servings of comminuted
chicken.
For raw comminuted turkey servings, the risk assessments found that
products that are contaminated with at least 10 cfu/g of Salmonella at
the end of production and contain a serotype of public health
significance have a 3,500 per 100,000 servings probability of illness,
while the average probability of illness is 2.5 per 100,000 servings
across all servings; the majority of which have levels below 10 cfu/g.
Therefore, servings from production lots of comminuted turkey that test
positive for Salmonella at or above 10 cfu/g with a serotype of public
health significance are 1,400-fold (i.e., ~3,500/2.5) more likely to
cause illness than the average across all comminuted turkey servings.
Thus, while there is a relatively low probability that consumers will
be exposed to comminuted turkey that contains Salmonella at 10 cfu/g,
if exposed, there is a much higher probability of illness, i.e., 1,400-
fold, when compared to the majority of servings of comminuted turkey.
Illnesses prevented. The risk assessments also predicted the total
number of illnesses prevented annually for chicken carcasses, parts,
and comminuted chicken and turkey for different Salmonella threshold
levels--0.03 cfu/ml(g), 1 cfu/mL(g), 10 cfu/mL(g), and 100 cfu/mL(g)
(Table 5). Uncertainty analyses were also run for the main scenarios
under consideration. A threshold set at the Salmonella detection level
for comminuted chicken and turkey (0.003 cfu/g) was not as effective as
the higher threshold levels in Table 5 below. Therefore, an analysis
evaluating the uncertainty around the predicted public health impact
for a threshold of 0.003 cfu/g Salmonella in comminuted poultry was not
evaluated in the risk assessments.
The resulting overlapping 95 percent credible intervals around the
estimated number of illnesses prevented suggest that there is little
meaningful difference in effectiveness between the threshold standards
with respect to annual illnesses prevented. However, as discussed
above, when compared with the majority of servings, chicken carcasses,
chicken parts, comminuted chicken, and comminuted turkey that contain
Salmonella at 10 cfu/mL(g) or higher present a much higher probability
of illness. Thus, based on the elevated probability of illness
associated with raw chicken carcasses, chicken parts, comminuted
chicken, and comminuted turkey associated with Salmonella levels at or
above 10 cfu/mL(g), FSIS is proposing 10 cfu/mL(g) as the Salmonella
level for the proposed final product standards.

Table 5--Annual Illnesses Prevented, Most Likely
[95% Credible Interval]
----------------------------------------------------------------------------------------------------------------
Chicken Comminuted Comminuted
Threshold level carcasses Chicken parts chicken turkey
----------------------------------------------------------------------------------------------------------------
0.03 cfu/mL(g)................... 4600 (2000, 7100) 7900 (3300, 12700) 1500 (800, 2200) 2500 (700, 4900)
1 cfu/mL(g)...................... 2400 (700, 5000) 1400 (400, 3600) 1400 (600, 2100) 2300 (600, 4800)
10 cfu/mL(g)..................... 1000 (200, 3100) 200 (40, 700) 1000 (400, 1900) 2000 (500, 4300)
100 cfu/mL(g).................... 200 (0, 1500) 20 (0, 100) 600 (200, 1500) 1400 (200, 3500)
----------------------------------------------------------------------------------------------------------------

2. Proposed Determination
After careful consideration of the information presented above,
FSIS has concluded that raw chicken carcasses, chicken parts,
comminuted chicken, and comminuted turkey contaminated with Salmonella
at or above 10 cfu/mL(g) and a serotype of public health significance
present an unacceptable risk of illness based on their risk per
serving. As discussed above, the 2023 risk assessments for chicken
found that production lots of raw chicken carcasses and raw chicken
parts contaminated with these Salmonella levels and serotypes are at
least 1,000 times more likely than average to cause illness across all
chicken parts and carcass servings, and that servings from production
lots of comminuted chicken and turkey contaminated with Salmonella at
these levels and serotypes are at least 590 times more likely than
average to cause illness across all comminuted chicken and turkey
servings.
Additionally, Salmonella has been associated with severe and
debilitating human illness and available data suggest that the
Salmonella infectious dose for the serotypes of public health concern
is relatively low. Information from consumer behavior research shows
that, rather than using a food thermometer to check the internal
temperature of whole chicken, chicken parts, comminuted chicken
products, and comminuted turkey products, many consumers ordinarily
rely on visual and textural cues to determine that these products are
properly cooked. Consumer research also shows that chicken that
consumers considered to be properly cooked based on these subjective
cues often had not reached an internal temperature sufficient to
destroy Salmonella that may be present, and one study found that for
certain poultry products, that application of inadequate heat
treatments from improper cooking was unable to assure complete
elimination of Salmonella even with a low initial contamination level
of 10 cfu/g. Information from consumer behavior research also shows

[[Page 64704]]

that ordinary consumer handling associated with chicken carcasses,
chicken parts, comminuted chicken, and comminuted turkey creates
conditions for Salmonella exposure from raw poultry through cross
contamination.
Thus, because Salmonella can survive what many consumers consider
to be ordinary cooking and handling practices for chicken carcasses,
chicken parts, comminuted chicken, and comminuted turkey, and because
the 2023 risk assessments found that servings of these products that
test positive for Salmonella at levels at or above 10 cfu/mL(g) and a
serotype of public health significance are much more likely to cause
illness when compared to the majority of chicken carcasses, chicken
parts, comminuted chicken, and comminuted turkey servings, FSIS has
tentatively determined that, when contaminated with Salmonella at these
levels and serotypes, these products are adulterated as defined in the
PPIA. Specifically, FSIS has tentatively concluded that these products
are adulterated as defined in 21 U.S.C. 453(g)(1) because their
elevated risk of illness renders them ``injurious to health.'' FSIS has
also tentatively concluded that they are adulterated as defined in 21
U.S.C. 453(g)(3) because their elevated risk of illness makes them
``unsound, unhealthful, unwholesome, or otherwise unfit for human
food.''
The adulteration definition in 21 U.S.C. 453(g)(1) includes two
separate standards for determining whether a product is adulterated.
Under 21 U.S.C. 453(g)(1), if a substance is an ``added substance'' the
product is adulterated if the substance ``may render'' the product
injurious to health. If the substance is not added, the product is
adulterated ``if the quantity of such substance in or on'' the product
``ordinarily'' renders it injurious to health.
As noted above, in response to the draft October 2022 Salmonella
Framework, FSIS received comments on whether Salmonella should be
considered as an ``added substance'' in raw poultry. Comments from
consumer advocacy organizations asserted that Salmonella should be
considered as an ``added substance'' because it is not normally present
in the muscle tissue of healthy birds. The comments stated that while
Salmonella is present in the gastrointestinal tract of live birds, it
is an ``added substance'' in poultry products because it only makes its
way onto to poultry muscle tissue through contamination that occurs
during slaughter and processing, specifically during defeathering and
evisceration. To support this position, the commenters referenced case
law that provides that where some portion of toxic substance present in
a food has been introduced by human intervention, the entirety of that
substance present in the food will be treated as an ``added
substance''.\110\
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\110\ See United States v. Anderson Seafoods, Inc., 622 F.2d 157
(5th Cir. 1980); Continental Seafoods, Inc. v. Schweiker, 674 F.2d
38 (D.C. Cir. 1982).
---------------------------------------------------------------------------

Comments from trade associations representing the meat and poultry
industries asserted that Salmonella is not an ``added substance''
because it exists naturally in and on the live birds. The comments
stated that Salmonella can exist in a chicken's skin, muscle tissue,
and gut. A trade association representing the chicken industry cited
references that, according to the comment, show that researchers have
identified Salmonella in chicken neck skin, on the outer layer of skin,
on feather follicles, connective tissue, and in drumstick muscle. The
commenter also stated that literature shows correlations between
Salmonella loads on the farm and in birds and at various processing
steps, reinforcing that Salmonella enters the process via the chickens
themselves. A comment from a trade association representing the meat
and poultry industry stated that Salmonella can exist on the exterior
of the animal, harbor in feather follicles, and travel from the
gastrointestinal tract of poultry to the bloodstream, theoretically
providing a pathway for Salmonella to be distributed throughout the
bird.
In addition, the comments stated that the case law provides that to
be ``added,'' a substance must not otherwise be present in the food and
must be artificially introduced by a person.\111\ According to the
chicken industry trade association, the fact that Salmonella may be
present in greater expected concentrations in some parts of a chicken
than others does not make it an ``added substance'' in poultry muscle
because, as with any microbe, naturally-occurring Salmonella can be
spread through cross-contact during processing.
---------------------------------------------------------------------------

\111\ These commenters cite United States v. Coca Cola, 241 U.S.
265 (1915) and United States v. Anderson Seafoods, Inc. 622 F.2d
157, 160 (5th Cir. 1980).
---------------------------------------------------------------------------

FSIS had traditionally viewed Salmonella as ``naturally occurring''
in food animals.\112\ FSIS has previously rejected broad requests for
it to declare that Salmonella is considered an ``added substance'' in
all products,\113\ however, FSIS has not previously determined whether
certain circumstances, considering what current scientific data
indicates about Salmonella's spread to or within products, may render
Salmonella an ``added substance'' in the raw products covered by this
proposed framework. Before taking a position on whether there are any
circumstances in which Salmonella can be considered an ``added
substance'' in raw chicken carcasses, chicken parts, comminuted
chicken, and comminuted turkey, FSIS has decided to request additional
comments on both the legal and factual aspects of this issue.
---------------------------------------------------------------------------

\112\ See FSIS Final Response to Marler Clark LLP petition # 20-
01 ``Petition for an Interpretive Rule Declaring `Outbreak'
Serotypes of Salmonella enteritica subspecies to be Adulterants''
Available at: https://www.fsis.usda.gov/policy/petitions/petition-interpretive-rule-related-certain-Salmonella-serotypes.
\113\ See FSIS Final Response to Marler Clark petition.
---------------------------------------------------------------------------

As noted above, under 21 U.S.C. 453(g)(1), there are two
definitions for adulteration, depending on whether a substance in a
poultry product is ``added'' or ``not added.'' However, the PPIA does
not define the circumstances in which a substance in a poultry product
is ``added'' within the meaning of the statute. Prior court decisions
that address whether Salmonella is an adulterant in raw meat or poultry
products have never directly considered whether and under what
circumstances Salmonella may be considered an ``added substance'' under
the PPIA.\114\
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\114\ See American Public Health Association (APHA) v. Butz, 511
F. 2d 331 (D.C. Cir. 1974); Continental Seafoods, Inc. v. Schweiker,
674 F.2d 38 (D.C. Cir. 1982); Supreme Beef Processors, Inc. v. USDA,
275 F.3d 432 (5th Cir. 2001).
---------------------------------------------------------------------------

As noted above, some of the comments on the October 2022 draft
Salmonella Framework asserted that Salmonella should be considered as
an ``added substance'' in raw poultry based on the holding in U.S. v.
Anderson Seafoods. The Anderson Seafoods case involved toxic levels of
mercury in swordfish. The issue before the court was whether all
mercury found in the swordfish should be considered as an ``added
substance'' under the adulteration provisions of the FFDCA \115\ when
some mercury in swordfish occurs naturally and some is the result of
man-made pollution. The court held that ``where some portion of a toxin
present in a food has been introduced by man, the entirety of that
substance present in the food will be

[[Page 64705]]

treated as an added substance'' as defined in the statute.\116\ Based
on this holding, some comments asserted that Salmonella should be
considered as an ``added substance'' in raw poultry because poultry
muscle does not normally contain Salmonella, and Salmonella only makes
its way onto to poultry muscle tissue through contamination that occurs
during slaughter and processing.
---------------------------------------------------------------------------

\115\ The adulteration definition in the FFDCA at issue in
Anderson Seafoods is, in relevant parts, identical to the definition
in the PPIA and provides that ``A food shall be deemed to be
adulterated (a)(1) if it bears or contains any poisonous or
deleterious substance which may render it injurious to health; but
in case the substance is not an added substance such food shall not
be considered adulterated under this clause if the quantity of such
substance in such food does not ordinarily render it injurious to
health''(21 U.S.C. s 342(a)(1)).
\116\ Anderson Seafoods, 622 F.2d at 161.
---------------------------------------------------------------------------

As noted by the comments, Salmonella is present in the
gastrointestinal tract of live birds, and there is evidence that
extraintestinal Salmonella exist in poultry skin, livers, bones, and
bone marrow before processing.\117\ Most Salmonella contamination on
carcasses is believed to result from leakage of ingesta during crop
removal and from feces during evisceration, as well as aerosolization
during picking.\118\ \119\ After poultry carcasses are scalded, the
carcasses travel through a series of defeathering machines where their
feathers are removed using mechanical pickers with rubber ``fingers.''
During the picking process, these rubber fingers not only can massage
Salmonella-contaminated water remaining from the scalder into the
carcass but can also inadvertently press on the abdomen of the carcass,
pushing out fecal matter and ingesta, resulting in transfer of
Salmonella to the carcass skin or to the machinery.\120\ The 2023 risk
profile identified studies that show that Salmonella can persist on
processing equipment after cleaning and sanitation,\121\ which
increases the potential for cross-contamination.
---------------------------------------------------------------------------

\117\ Rimet, C.S., et al. (2019). Salmonella Harborage Sites in
Infected Poultry That May Contribute to Contamination of Ground
Meat. Frontiers in Sustainable Food Systems 3(2). see also Jones-
Ibarra, A.M., et al. (2019). Salmonella recovery from chicken bone
marrow and cecal counts differ by pathogen challenge method. Poult
Sci 98(9): 4104-4112. see also Cox, N.A., et al. (2007). Recovery of
Campylobacter and Salmonella Serovars from the Spleen, Liver and
Gallbladder, and Ceca of Six-and Eight-Week-Old Commercial Broilers.
Journal of Applied Poultry Research 16(4): 477-480.
\118\ National Advisory Committee on Microbiological Criteria
for Foods. (2019). Response to Questions Posed by the Food Safety
and Inspection Service Regarding Salmonella Control Strategies in
Poultry. J Food Prot. 82(4):645-668.
\119\ Singh M and Thippareddi H (2020). Managing Microbiological
Food Safety Risks in Poultry Processing. White Paper for 3M Food
Safety at: https://berstlerllc.com/wp-content/uploads/2023/03/3M-Food-Safety-Poultry-Segment-Whitepaper.pdf.
\120\ Singh 2020.
\121\ Obe, T., et al., Prevalence of Salmonella Enterica on
Poultry Processing Equipment after Completion of Sanitization
Procedures. Poultry Science, 2020. 99(9): p. 4539-4548. Veluz, G.A.,
S. Pitchiah, and C.Z. Alvarado, Attachment of Salmonella Serovars
and Listeria Monocytogenes to Stainless Steel and Plastic Conveyor
Belts. Poultry Science, 2012. 91(8): p. 2004-2010. Rothrock, M.J.,
Jr., et al., The Characterization of Salmonella Enterica Serotypes
Isolated from the Scalder Tank Water of a Commercial Poultry
Processing Plant: Recovery of a Multidrug-Resistant Heidelberg
Strain. Poultry Science, 2015. 94(3): p. 467-472. Bailey, J.S., et
al., Sources and Movement of Salmonella through Integrated Poultry
Operations: A Multistate Epidemiological Investigation. Journal of
Food Protection, 2001. 64(11): p. 1690-7.
---------------------------------------------------------------------------

Another step in the process in which Salmonella may be spread to or
increased in poultry carcasses is evisceration. During evisceration,
Salmonella that is present in the gastrointestinal tract may be
transferred to the skin and other carcass surfaces due to rupture of
the viscera when the carcass is opened.\122\ Additionally, the 2023
risk profile found that although used as a control step, immersion
chilling may be an opportunity for cross-contamination of broiler
carcasses. For example, in one study, a lower incidence of Salmonella
in air-chilled broilers compared to immersion-chilled broilers (18.7
percent to 24.7 percent positive carcasses) suggests that cross-
contamination may be more prevalent for immersion-chilled
broilers.\123\
---------------------------------------------------------------------------

\122\ Singh (2020); National Advisory Committee on
Microbiological Criteria for Foods. (2019). Response to Questions
Posed by the Food Safety and Inspection Service Regarding Salmonella
Control Strategies in Poultry. J Food Prot. 82(4):645-668.
\123\ Smith, D.P., J.A. Cason, and M.E. Berrang, Effect of Fecal
Contamination and Cross Contamination on Numbers of Coliform,
Escherichia coli, Campylobacter, and Salmonella on Immersion-Chilled
Broiler Carcasses. Journal of Food Protection, 2005. 68(7): p. 1340-
1345.
---------------------------------------------------------------------------

In addition to processes that can contribute to Salmonella
contamination on poultry carcasses during slaughter and processing,
further processing of carcasses into other commodities may also add
Salmonella to or increase Salmonella in finished poultry parts, such as
wings, breasts, and thighs. FSIS sampling data show that further
processed chicken parts have a higher incidence of Salmonella compared
to carcasses.\124\ This difference is likely because of cross
contamination between positive and negative parts and carcasses during
further processing.\125\ \126\ Further processing presents various
opportunities in which Salmonella that is present in certain parts of
the bird may be added to interior edible muscle where Salmonella is not
ordinarily found. For example, Salmonella can be found in feather
follicles in the skin.\127\ \128\ When the skin is cut, Salmonella can
be exposed and spread during processing to previously uncontaminated
product and/or increased in product with low levels of
contamination.\129\ In addition, Salmonella-negative raw poultry parts
and comminuted poultry may become cross-contaminated by contact with
Salmonella-contaminated equipment or when they are commingled with
Salmonella-positive products, such as when they are collected in combo
bins for further processing.\130\ \131\
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\124\ Sampling Results for FSIS-Regulated Products. Available
at: https://www.fsis.usda.gov/science-data/sampling-program/sampling-results-fsis-regulated-products.
\125\ FSIS Guidance for Controlling Salmonella in Poultry (June
2021) p. 59. Available at: https://www.fsis.usda.gov/sites/default/files/media_file/2021-07/FSIS-GD-2021-0005.pdf.
\126\ Codex Guideline for the Control of Campylobacter and
Salmonella in Chicken Meat at: https://www.fao.org/fao-who-codexalimentarius/sh-proxy/en/?lnk=1&url=https%253A%252F%252Fworkspace.fao.org%252Fsites%252Fcodex%252FStandards%252FCXG%2B78-2011%252FCXG_078e.pdf.
\127\ Kim J-W and Slavik MF. 1996. Cetylpyridinium Chloride
(CPC) treatment on poultry skin to reduce attached Salmonella. J.
Food Prot. 59: 322-326.
\128\ Wu D, Alali WQ, Harrison MA, and Hofacre CL. 2014.
Prevalence of Salmonella in neck skin and bone of chickens. J Food
Prot. 77(7): 1193-1197.
\129\ FSIS Guidance for Controlling Salmonella in Poultry (June
2021) pp. 59-60.
\130\ FSIS Guidance for Controlling Salmonella in Poultry (June
2021) pp. 59.
\131\ Codex Guideline for the Control of Campylobacter and
Salmonella in Chicken Meat.
---------------------------------------------------------------------------

Comminuted products are those that are ground, mechanically
separated, or hand- or mechanically deboned and further chopped,
flaked, minced, or otherwise processed to reduce particle size. Because
of the nature of comminuted processes, Salmonella contamination in
chicken skin and bone can spread throughout an entire batch or lot
through cross-contamination. FSIS sampling data show that ground and
other raw comminuted chicken products that were produced using either
bone-in or skin-on source materials were more likely to be contaminated
with Salmonella than those fabricated from deboned, skinless source
materials.\132\ Salmonella-contaminated equipment used to produce
comminuted poultry may also contribute to Salmonella contamination in
these products.
---------------------------------------------------------------------------

\132\ FSIS Guidance for Controlling Salmonella in Poultry (June
2021) pp. 65-66, Table 4 FSIS exploratory sampling test results, raw
comminuted chicken by source material composition (6/1/13-6/30/15,
2,688 samples.
---------------------------------------------------------------------------

FSIS requests comments on whether the available science supports
that some Salmonella in a raw poultry product is ``naturally
occurring'' and some is ``added.'' FSIS also requests comments on
whether, under the reasoning of Anderson Seafoods or another rationale,
the Agency has authority to regulate Salmonella as an ``added
substance'' if it can demonstrate that some Salmonella can be
artificially

[[Page 64706]]

introduced into raw poultry products through processing procedures and
other actions attributable to man.
As discussed above, consumer behavior research shows that
Salmonella can survive what many consumers consider to be ordinary
cooking and handling practices for chicken carcasses, chicken parts,
comminuted chicken, and comminuted turkey. In addition, the 2023 risk
assessments, which modeled a broad distribution of consumer cooking
behavior, found that servings of these products that test positive for
Salmonella at levels at or above 10 cfu/mL(g) and a serotype of public
health significance are much more likely to cause illness when compared
to the majority of chicken carcasses, chicken parts, comminuted
chicken, and comminuted turkey servings. Thus, regardless of whether
Salmonella is considered as an ``added substance,'' FSIS tentatively
determines through this proposal that raw chicken carcasses, chicken
parts, comminuted chicken, and comminuted turkey that contain
Salmonella levels at or above 10 cfu/mL(g) and a serotype of public
health significance are adulterated under 21 U.S.C. 453(g)(1) because
when contaminated with these levels and serotypes of Salmonella, the
high likelihood that raw chicken carcasses, chicken parts, comminuted
chicken, and comminuted turkey will result in illnesses when compared
to the average serving of these products ``ordinarily'' renders them
injurious to health. Additionally, through this proposal, FSIS
tentatively determines that raw chicken carcasses, chicken parts,
comminuted chicken, and comminuted turkey contaminated with Salmonella
levels and serotypes in the proposed final product standards are
adulterated as defined in 21 U.S.C. 453(g)(3) because their elevated
risk of illness makes them ``unsound, unhealthful, unwholesome, or
otherwise unfit for human food.'' This tentative determination does not
depend on the status of Salmonella as an ``added substance.''
FSIS requests comments on its proposed determination that, when
contaminated with Salmonella at the levels and serotypes provided in
the final products standards, chicken carcasses, chicken parts,
comminuted chicken, and comminuted turkey are adulterated as defined in
21 U.S.C. 453(g)(1) and (3) and whether there are alternative bases for
determining adulteration for these poultry products.

F. Proposed Policy Implementation

1. HACCP Reassessment
The HACCP system regulations require that every establishment
reassess the adequacy of its HACCP plan at least annually and whenever
any changes occur that could affect the underlying hazard analysis or
alter the HACCP plan (9 CFR 417.4(a)(3)). If finalized, FSIS' proposed
determination that chicken carcasses, chicken parts, comminuted chicken
and comminuted turkey that contain Salmonella levels of 10 cfu/mL(g) or
higher and any detectable levels of a serotype of public health
significance are adulterated would be such a change. Thus, if FSIS
finalizes this proposed determination, all establishments that produce
chicken carcasses, chicken parts, comminuted chicken, and comminuted
turkey as final products that will enter commerce would need to
reassess their HACCP plans. Establishments that make changes to their
production process because of their reassessment would also need to re-
validate their HACCP plans. FSIS would issue instructions to IPP in
establishments that produce these final products to verify that these
establishments have completed their reassessment before the effective
date of any final determination resulting from this proposal.
2. Proposed Implementation and Status of Laboratory Methods
Products subject to verification sampling. Should FSIS finalize
these proposed standards, the Agency intends to conduct a routine
sampling and verification testing program for Salmonella in chicken
carcasses, chicken parts, comminuted chicken, and comminuted turkey in
which the Agency would collect samples of raw final products and
analyze them for Salmonella levels and serotypes to determine whether
the final product is adulterated. FSIS would collect the verification
samples after the establishment has completed all validated
antimicrobial interventions. Under the proposed Salmonella verification
testing program, FSIS intends to only collect and analyze samples of
the final poultry products produced by an establishment, i.e., chicken
carcasses to be shipped in commerce as whole chickens, chicken parts to
be shipped in commerce as chicken parts, comminuted chicken to be
shipped in commerce as comminuted chicken products, and comminuted
turkey to be shipped in commerce as comminuted turkey products. Thus,
under this proposal, if a chicken slaughter establishment uses
carcasses processed in the establishment to produce other final
products, such as chicken parts or comminuted chicken, FSIS would not
collect whole carcass samples as part of the proposed verification
sampling program. Likewise, chicken parts produced by an establishment
that are intended for use in another final product produced by the
establishment, such as comminuted chicken, would not be subject to FSIS
verification sampling. FSIS also does not intend to collect samples of
mechanically separated chicken or mechanically separated turkey under
the proposed verification sampling program. However, final comminuted
chicken and turkey products that contain mechanically separated chicken
or turkey would be eligible for verification sampling.
The final product samples collected under the proposed verification
sampling plan would be determined on an establishment basis. Thus, all
raw final products produced by an establishment that are not intended
to be further processed into a RTE product would be subject to
verification sampling regardless of where the product is shipped. For
example, FSIS would consider whole carcasses or parts to be final
products subject to verification sampling if the establishment that
produced the carcasses or parts ships them to another establishment for
further processing into a raw parts or comminuted product. FSIS would
not, however, collect verification samples from raw whole carcasses,
parts, or comminuted products that are shipped to another establishment
for cooking or to be further processed into a ready-to-eat product. If
off-site interventions, such as high-pressure processing or
irradiation, are applied to prevent or control Salmonella, FSIS would
sample the product after the off-site intervention is applied.
Additionally, should FSIS finalize these proposed final product
standards, the Agency intends to conduct testing for Salmonella of
imported raw chicken carcasses, chicken parts, comminuted chicken, and
comminuted turkey products in accordance with FSIS' import reinspection
procedures.\133\ Poultry imports represent a small fraction of the U.S.
domestic poultry supply, accounting for less than 0.5

[[Page 64707]]

percent in 2021. Currently, FSIS samples and tests imported chicken
carcasses, chicken parts, comminuted chicken, and comminuted turkey for
the presence of Salmonella. According to data from PHIS, in 2021, FSIS
collected and analyzed about 850 samples of imported chicken and turkey
products, which represented about 15.8 million pounds of product. These
samples were mainly from chicken parts and carcasses, as imports of
comminuted chicken and turkey are relatively low. While data on the
volume of imported product with results at or above 10 cfu/mL(g) are
not available, FSIS estimates this would be a relatively low volume of
product.
---------------------------------------------------------------------------

\133\ FSIS Directive 9900.2, Import Reinspection of Meat,
Poultry and Egg Products (Rev. 2)(Oct 12 2021). Available at:
https://www.fsis.usda.gov/policy/fsis-directives/9900.2.
FSIS Directive 9900.6, Laboratory Sampling Program for Imported
Meat, Poultry, and Egg Products (Nov 3, 2015). Available at: https://www.fsis.usda.gov/policy/fsis-directives/9900.6.
---------------------------------------------------------------------------

Sample analysis. The detection and isolation methodology for
Salmonella is described in MLG chapter 4.14, of the FSIS Microbiology
Laboratory Guidebook.\134\ Based on current FSIS methodologies, when
sampling the chicken carcasses and parts under this proposed
determination, FSIS would collect a rinsate sample from the
establishment to analyze 30 mL per test for Salmonella. When sampling
comminuted chicken or comminuted turkey, the Agency would collect 1
pound of the product from the establishment to analyze 325 g per test
for Salmonella. Samples would be initially screened, post-enrichment,
for the presence or absence of Salmonella. Samples that screen negative
would be reported as ``negative.'' For samples that screen positive,
FSIS would use selective and differential culture-based media and
proteomics testing to confirm. In parallel, all screen positives will
be analyzed for levels and targeted rapid serotype screening. A sample
is considered confirmed positive for Salmonella after completion of
confirmatory tests. Any chicken carcass, chicken parts, comminuted
chicken, or comminuted turkey final product sample ``confirmed
positive'' with Salmonella levels of 10 cfu/mL(g) or higher and
screened positive for a serotype of public health significance would
not be allowed to enter commerce. Any chicken carcass, chicken parts,
comminuted chicken, or comminuted turkey final product sample that
contains Salmonella levels of 10 cfu/mL(g) or higher and a serotype of
public health significance would be considered adulterated.
---------------------------------------------------------------------------

\134\ FSIS Microbiology Laboratory Guidebook available at:
https://www.fsis.usda.gov/news-events/publications/microbiology-laboratory-guidebook.
---------------------------------------------------------------------------

Based on current testing methodologies, FSIS estimates that
Salmonella screening results and quantification results would routinely
be available 2 days after a sample is taken. For samples above the
quantification threshold, an additional 3 days may be necessary for a
confirmed positive or negative result. Currently, the routine procedure
is to use WGS to determine Salmonella isolate sequence, serotypes, and
antimicrobial resistance (AMR) profile, which require at least 14 days
for result reporting. FSIS could use a non-routine molecular serotyping
methodology to determine the serotype in a more time sensitive manner
such that results would be available by Salmonella confirmation, 5 days
after sample collection, if not sooner.
FSIS is proposing the combined quantification and serotype final
product standards recognizing current efforts underway by ARS and
private sector laboratories to develop rapid, reliable, Salmonella
quantification and serotyping technologies. FSIS is actively working to
explore technologies that may have the capability of WGS in determining
serotype and reduce the current timeframe. All timeframes and methods
are likely to change as FSIS continuously incorporates new laboratory
technologies into its sampling verification program. Any final
verification sampling plan resulting from this proposal would use
testing methods that are validated and fit for purpose.
FSIS requests comments on available technologies and methods for of
quantification and serotyping. If FSIS finalizes this proposed sampling
plan, data gathered from the sampling plan would enable the Agency to
gauge more precisely the hazard posed by certain Salmonella levels and
serotypes in chicken carcasses, chicken parts, comminuted chicken, and
comminuted turkey. FSIS intends to further evaluate and, if necessary,
refine the proposed status of Salmonella as an adulterant in these raw
poultry products as advances in science and technology related to
pathogen levels, serotypes, and virulence genes become available.
Sampled Lot. When FSIS tests a product sample for adulterants, the
Agency withholds its determination as to whether product is not
adulterated, and thus eligible to enter commerce, until all test
results that bear on the determination have been received (77 FR
73401). Under this policy, establishments and importers of record at
official import inspection establishments must maintain control of
products tested for adulterants to ensure that the products do not
enter commerce while waiting for receipt of the test results. Thus, if
FSIS finalizes its proposed routine Salmonella verification testing
program for chicken carcasses, chicken parts, comminuted chicken, and
comminuted turkey, establishments that produce these raw products and
official import inspection establishments where these raw products are
reinspected would need to control and maintain the integrity of the
sampled lot pending the availability of test results.
Under any final verification sampling plan, FSIS IPP would give
establishments and official import inspection establishments advance
notice before IPP collect a product sample for Salmonella to give these
entities enough time to control the sampled lot without altering the
process that the sample represents. The sampled lot is the product
represented by the sample collected and analyzed by FSIS.
Establishments are responsible for providing a supportable basis for
defining the sample lot. For sampling purposes, product lots should be
defined such that they are microbiologically independent.
Microbiological independence is documented by separation, e.g.,
physical, temporal, or by sanitation intervention, that clearly
delineates the end of one production lot and the beginning of the next.
The microbiological results from one test are independent of prior or
later lots. In other words, if a product sample tests positive for
Salmonella at a level of 10 cfu/mL(g) or higher and contains a
detectable level of at least one serotype of public health
significance, products from other production lots should not be
implicated, provided the establishment can support that the lots remain
microbiologically independent.
Generally, FSIS recommends that establishments develop and
implement in-plant sampling plans that define production lots or sub-
lots that are microbiologically independent of other production lots or
sub-lots. Production lots that are so identified may bear distinctive
markings on the shipping cartons. FSIS has issued guidance to help
establishments and official import inspection establishments comply
with the Agency's policy that does not allow product that FSIS has
tested for adulterants to enter commerce until test results become
available.\135\ In addition to providing guidance on adequate control
measures that establishments and official import inspection
establishments can implement for products tested for adulterants, the
document also includes guidance on

[[Page 64708]]

how to define a product lot in order to determine the amount of product
that must be controlled pending test results. If FSIS finalizes the
proposed new standards for chicken carcasses, chicken parts, comminuted
chicken, and comminuted turkey, FSIS would consider updating the
guidance to cover Salmonella sampling of these raw poultry products.
---------------------------------------------------------------------------

\135\ FSIS Compliance Guideline: Controlling Meat and Poultry
Product Pending FSIS Test Results (2013) at: https://www.fsis.usda.gov/guidelines/2013-0003.
---------------------------------------------------------------------------

As discussed above, establishments would be required to control the
raw poultry products sampled by FSIS pending the test results. If test
results detect Salmonella at a level of 10 cfu/mL(g) or higher and at
least one Salmonella serotype of public health significance, FSIS would
consider products represented by the sampled lots to be adulterated and
would issue an NR. Additionally, all products in the lot represented by
the sample would be prohibited from entering commerce. If any product
from the lot represented by the product samples has entered commerce,
FSIS would request that the producing establishment recall the
implicated products. Depending on the circumstances, in addition to
issuing an NR, FSIS could take other appropriate enforcement action as
authorized in 9 CFR part 500 because the establishment would have
produced and shipped adulterated product. Such actions may include
immediately suspending inspection or issuing an NOIE.
For imported products tested at port of entry, if the product tests
positive for Salmonella at 10 cfu/mL(g) or higher and any detectable
level of a Salmonella serotype of public health significance and has
not been held at the official import inspection establishment or at an
off-site premises under adequate controls, FSIS would request that the
importer of record recall the product. If the product has been held,
the product will be refused entry. Product lots subsequently presented
for import inspection from the same foreign country and establishment
would be held at the official import inspection establishment pending
results in accordance with FSIS' import reinspection procedures.\136\
The FSIS Office of International Coordination would notify the program
officials of the affected exporting country when a positive result is
reported, so that they can determine whether the producing
establishment has exported any other product from the same production
lot to the United States. If the foreign establishment has properly
defined the product lot on the basis of specific control factors, and
accurately tracked the containerization of product produced under those
controls, the establishment can reduce the likelihood that adulterated
product will enter commerce and can more easily recover product if a
sample is positive for Salmonella levels and serotypes that would
render the product adulterated.
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\136\ FSIS Directive 9900.8, Meat, Poultry, and Egg Products
Refused Entry into the United States (Dec. 1 2020). Available at:
https://www.fsis.usda.gov/policy/fsis-directives/9900.8.
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Proposed implementation. To mitigate the impact of regulatory
changes on small and VS establishments, FSIS has typically used a
phased approach for implementation to provide additional time for small
and VS establishments to adjust their operations to comply with any new
regulatory requirements. FSIS defines large, small, and VS
establishments based on the number of establishment employees and, for
VS establishments, annual sales.\137\
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\137\ Large establishments are establishments with 500 or more
employees, small establishments are establishments with 10 or more
employees but fewer than 500, and very small establishments are
establishments with fewer than 10 employees or annual sales of less
than $2.5 million.
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Should FSIS finalize the proposed final product standards, the
Agency intends to use a phased approach to initiate verification
sampling in establishments that produce raw chicken carcasses, chicken
parts, comminuted chicken, and comminuted turkey. However, instead of
implementing the Agency's verification sampling program based on the
current large, small, and VS establishment size definitions, FSIS has
tentatively decided to establish implementation dates based on annual
number of birds slaughtered or, for establishments that do not conduct
slaughter operations, production volume. The current small
establishment size definition was established in the HACCP final rule
and corresponded to the Small Business Administration's size standards
for business entities at that time (61 FR 38819). However, because FSIS
has applied these standards to individual establishments rather than
business entities, establishments classified as ``small'' may have up
to 500 employees. Thus, FSIS believes that a phased implementation
based on production volume would be a more effective approach to
mitigate the impact of this proposed determination on low and VLV
establishments than the current establishment size definitions.
As FSIS implements the final product standards verification
sampling program, the Agency has tentatively decided to phase out all
current Salmonella performance standards for poultry. Thus, when the
proposed final product verification sampling program is fully
implemented, FSIS would no long use Salmonella sampling results to
categorize poultry establishments and would no longer publish these
establishments' performance standards categories on the FSIS website.
FSIS evaluates and revises its sampling and testing programs each year.
Any final verification sampling program resulting from this proposal
would be sufficient to verify that establishments are meeting the final
product standards.
The proposed production volume categories and proposed verification
sampling implementation schedule are as follows.

Table 6--Proposed Implementation Dates
------------------------------------------------------------------------
Establishment volume category Implementation date
------------------------------------------------------------------------
High...................................... 1 year after publication.
Medium.................................... 2 years after publication.
Low....................................... 3 years after publication.
Very Low.................................. 3 years after publication.
------------------------------------------------------------------------

Table 7--Proposed Volume Categories Chicken Parts
------------------------------------------------------------------------
Definition (annual
Volume category production pounds)
------------------------------------------------------------------------
High...................................... Over 70,000,000.
Medium.................................... Between 1,000,000 and
70,000,000.
Low....................................... Less than 1,000,000.
------------------------------------------------------------------------

Table 8--Proposed Volume Categories Chicken Carcasses
------------------------------------------------------------------------
Definition (birds
Establishment volume category slaughtered per year)
------------------------------------------------------------------------
High...................................... Over 10 million.
Medium.................................... Between 1.1 and 10 million.
Low....................................... Between 440,001 and < 1.1
million.
Very Low.................................. No more than 440,000.
------------------------------------------------------------------------

Table 9--Proposed Volume Categories Comminuted Chicken and Turkey
------------------------------------------------------------------------
Definition (daily production
Volume category pounds)
------------------------------------------------------------------------
High...................................... Over 250,000.
Medium.................................... Between 6,001 and 250,000.
Low....................................... No more than 6,000.
------------------------------------------------------------------------

FSIS requests comments on this proposed implementation approach and
on the proposed establishment production volume categories. FSIS also
requests comments on whether the Agency should phase out the current
performance standards as the Agency implements the final product
standards or if the Agency should retain the current performance
standards and later determine if these standards are still

[[Page 64709]]

needed when evaluating the effectiveness of the proposed final product
standards.
FSIS also requests comments on whether the Agency should consider
an alternative implementation approach that would focus its final
product verification sampling on establishments that have a
demonstrated lack of process control. Under such an approach, FSIS
would establish a microbial process control standard based on a
threshold or some other parameter and require that establishments
conduct sampling at a frequency sufficient to demonstrate that they are
meeting the process control standard. Establishments whose results
exceed the process control standard would be required to conduct
intensified sampling, including environmental sampling and sampling at
multiple points in the process, to determine if the initial results
were an outlier or if there are problems with the establishment's
production process. If an establishment's intensified sampling results
show that it is meeting the process control standard, the establishment
would return to the standard sampling protocol. If the establishment
continues to exceed the process control standard, it would be required
to take corrective actions and continue to conduct intensified
sampling. If the establishment exceeds the process control standard
again, FSIS would collect and analyze final product samples for
Salmonella levels and serotypes because, at this point, the
establishment would have a record that demonstrates that there are
problems with its production process. The establishment would be
required to control product represented by the sampled lot pending
FSIS' test results. Product that tests positive for Salmonella at or
above 10 cfu/mL(g) and a Salmonella serotype of public health
significance would be considered unfit for human food and would be
prohibited from entering commerce. If the establishment released the
product into commerce, the product would be subject to recall.

III. Component Two: Enhanced Establishment Process Control Monitoring

A. Background and Current Regulatory Requirements

Process control monitoring, in the context of poultry slaughter,
consists of the programs and procedures an establishment implements to
ensure its processes are operating as intended in preventing
contamination (including contamination with enteric pathogens and fecal
material) of poultry carcasses and parts throughout the slaughter and
dressing process and to ensure that the resulting products meet
applicable regulatory standards or definitions (79 FR 49565, 49602).
Establishments must demonstrate that their process is in control by
implementing verification procedures, collecting data, and developing
and maintaining accurate records to demonstrate that their processes
and procedures are performing as intended and as required (9 CFR
381.65(g) and (h) and 9 CFR part 417). An effective process control
system entails an establishment responding effectively to re-establish
control when its ongoing verification activities show that its
processes are not producing the expected results. Effective process
control monitoring procedures should lead to lower rates of pathogen
contamination because establishments will discover deficiencies in
processing sooner and more reliably than would be the case without
effective process control monitoring procedures.
Contamination of poultry carcasses and parts by enteric pathogens
and fecal material (e.g., Salmonella and Campylobacter) are hazards
reasonably likely to occur in poultry slaughter establishments unless
addressed in a sanitation SOP or other prerequisite program (79 FR
49565, 49613). To ensure that establishments that slaughter poultry
implement appropriate measures to prevent carcasses from becoming
contaminated with pathogens, and that both FSIS and establishments have
the documentation to verify the effectiveness of these measures on an
on-going basis, current regulations require, among other things, that
all establishments that slaughter poultry other than ratites develop,
implement, and maintain written procedures to prevent contamination of
poultry carcasses and parts by enteric pathogens and fecal material
throughout the entire slaughter and dressing operation (9 CFR
381.65(g)). Establishments are required to incorporate their process
control procedures into their HACCP plan, sanitation SOPs, or other
prerequisite programs (collectively, ``the HACCP system'') and maintain
daily records sufficient to document the implementation and monitoring
of these procedures (9 CFR 381.65(g) and (h)).
Microbiological test results that represent levels of
microbiological contamination at key steps in the slaughter process are
necessary for establishments to provide comprehensive, objective
evidence that they are effectively maintaining process control to
prevent carcasses from becoming contaminated before and after they
enter the chiller (79 FR 49565, 49602). At present, establishments
conduct pre-chill testing to monitor how well an establishment is
minimizing contamination on live birds coming to slaughter and on
carcasses throughout the slaughter and dressing process, and post-chill
testing to monitor how well an establishment is minimizing
contamination during chilling and the overall effectiveness of any
antimicrobial interventions that were applied (79 FR 49565, 49566).
FSIS also collects a verification sample at the post-chill location and
tests for Salmonella and Campylobacter. In 2012, FSIS considered
requiring a third establishment sampling location at rehang (i.e.,
after picking and prior to evisceration) to monitor the incoming load
of pathogens but concluded that it was unnecessary to impose the
additional costs on industry (77 FR 4407, 4428).
Regulations at 9 CFR 381.65 (h) and 9 CFR 417.5 (a)(1) require
establishments to document their procedures and results in records
subject to Agency verification. At a minimum, these procedures must
include sampling and analysis for microbial organisms at the pre- and
post-chill location to monitor for process control, with an exception
for VS and VLV establishments operating under the Traditional
Inspection System (9 CFR 381.65 (g)(1)).\138\ In 2014, FSIS stated that
because these establishments are typically less automated and run
slower line speeds than larger establishments operating under other
inspection systems, they may require less complicated measures for
maintaining and monitoring process control on an ongoing basis (79 FR
49565, 49603). Therefore, at present, they are required to collect and
analyze samples for microbial organisms only at the post-chill
location.
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\138\ Very small establishments are establishments with fewer
than 10 employees or annual sales of less than $2.5 million dollars
(9 CFR 381.65(g)(1)(i)). Very low volume establishments annually
slaughter no more than 440,000 chickens, 60,000 turkeys, 60,000
ducks, 60,000 geese, 60,000 guineas, or 60,000 squab (9 CFR
381.65(g)(1)(ii)). Traditional Inspection must be used for turkeys
when neither the New Turkey Inspection System (NTI) nor the New
Poultry Inspection System (NPIS) is used. For other classes of
poultry, Traditional Inspection must be used when SIS, NELS, and the
NPIS are not used (9 CFR 381.76(b)(1)(v)).
---------------------------------------------------------------------------

In addition to prescribing the sampling locations for monitoring
process control, the regulations specify a minimum sampling frequency
to ensure establishments can detect changes in processing or
inconsistencies

[[Page 64710]]

that may occur (79 FR 49565, 49604). At a minimum, for chickens,
establishments are required to collect a pair of pre-and post-chill
samples once per 22,000 processed carcasses, but at a minimum of once
each week of operation, and for turkeys, ducks, geese, guineas, and
squab, establishments are required to collect a pair of samples once
per 3,000 processed carcasses but a minimum of once each week of
operation (9 CFR 381.65(g)(2)(i)). To minimize the sampling costs to
the lower volume establishments, VLV establishments must minimally
collect and analyze samples at least once during each week of operation
starting June 1 of every year. If, after consecutively collecting 13
weekly samples, an establishment can demonstrate that it is effectively
maintaining process control, it may modify its sampling plan (9 CFR
381.65(g)(2)(ii)). All establishments are required to conduct testing
at a frequency sufficient to detect a loss of process control soon
after it occurs so that they can take the necessary corrective actions
to prevent further product contamination (79 FR 49565, 49605).
Therefore, regardless of the prescribed minimum sampling frequency, the
establishment must sample at a frequency that is adequate to monitor
their ability to maintain process control for enteric pathogens and
fecal contamination (9 CFR 381.65(g)(2)(iii)).
When FSIS updated its poultry inspection regulations in 2014 (79 FR
49565), it referenced data from FSIS' 2007-2008 Young Chicken Baseline
survey (hereinafter, the ``baseline survey''), which found levels of
detectable generic E. coli (GEC) on post-chill carcasses well below the
performance criteria in the existing regulations.\139\ The baseline
survey found that over 60 percent of samples had non-detectable levels
of GEC. Among 12 establishments from which 10 or more samples were
analyzed, none had detectable levels of GEC. On the other hand, FSIS
analyzed 22 samples from each of 2 of these establishments and found
that all 44 samples had detectable AC measurements. FSIS also concluded
that AC levels at rehang were more highly correlated with Salmonella
than GEC levels which suggested that AC measurements might provide a
better measure of process control.\140\
---------------------------------------------------------------------------

\139\ FSIS (2007). Young Chicken Survey (baseline) June 2007-
June 2008. https://www.fsis.usda.gov/sites/default/files/media_file/2020-07/Baseline_Data_Young_Chicken_2007-2008.pdf.
\140\ Williams, M.S., et al. (2015). ``Industry-level changes in
microbial contamination on market hog and broiler chicken carcasses
between two locations in the slaughter process.'' Food Control 51:
361-370.
---------------------------------------------------------------------------

Despite the baseline survey findings, FSIS did not require that
establishments use a specific microbial organism to monitor process
control when it updated its regulations in 2014. Thus, at present,
establishments decide which microbiological organisms will best help
them to monitor the effectiveness of their process control procedures
and may develop sampling plans to test carcasses for enteric pathogens,
such as Salmonella, or another appropriate indicator organism. Because
establishments must incorporate their microbiological sampling plan
into their HACCP system, they are required to provide scientific or
technical documentation to support the judgements made in designing
their sampling plans, as required by 9 CFR 381.65 (h) and HACCP
regulation 9 CFR 417.4(a).

B. Need To Enhance Establishment Process Control Monitoring

Based on NACMCF recommendations, an analysis of PHIS inspection
results, sampling data, and the findings of the 2023 risk assessments,
FSIS has determined that there is a need to enhance establishment
process control monitoring. These recommendations and findings are
discussed below and collectively support FSIS' conclusion that
regulatory revision will improve establishments' ability to monitor
microbiological process control; demonstrate the effectiveness of their
measures to prevent carcasses from becoming contaminated; and ensure
that both FSIS and establishments have the documentation necessary to
verify the effectiveness of these measures on an on-going basis. These
recommendations and findings have also prompted FSIS to evaluate the
need for additional resources, services, and guidance to help
establishments develop microbiological process control monitoring
programs and comply with FSIS requirements.
1. NACMCF Charge and Recommendations
According to NACMCF, process control can be defined as maintaining
the output of a process within a desired range based on stability and
capability to meet specifications.\141\ Process control is accomplished
through six steps: (1) The output must be monitored and quantified with
appropriate sampling and testing; (2) There must be predefined limits
and targets traceable to acceptable specifications and the history of
the process; (3) The monitoring results must be compared to the
relevant process control limits; (4) There must be a predetermined plan
of action (such as a corrective action plan) based on the size and
frequency of deviation from relevant limits; (5) The proper action must
be decided upon based on the observed deviation; and (6) the proper
action must be promptly taken to adjust the process.\142\
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\141\ Note that a process can be stable and not capable of
meeting specifications, or an unstable process may produce product
that meets specifications. NACMCF (2015). '' Regarding
Microbiological Criteria as Indicators of Process Control or
Insanitary Conditions, available at https://www.fsis.usda.gov/sites/default/files/media_file/2020-07/NACMCF-Report-Process-Control-061015.pdf.
\142\ NACMCF (2018). ``Response to Questions Posed by the
Department of Defense Regarding Microbiological Criteria as
Indicators of Process Control or Insanitary Conditions.'' J Food
Prot 83(1): 115-141.
---------------------------------------------------------------------------

In 2015, NACMCF provided microbiological limits for food categories
that reflect process control and sanitary manufacturing conditions.
These limits can help FSIS-regulated establishments develop systems for
measuring SPC. SPC is an approach that uses statistical methods to
monitor and control a process. A process is under statistical control
when the output varies as expected within a statistical range. Process
variability is caused by chance or assignable causes. Assignable causes
can be linked to improperly adjusted or controlled machines, operator
errors, or defective raw material. A process that is operating with
assignable causes is out-of-control.\143\ Process capability is defined
as the degree by which SPC limits fall within specifications. If the
process exceeds an upper or a lower specification limit, the product
does not meet the specification even if it is operating without
assignable causes and is in control. Process capability is
traditionally measured using a process capability index (Cp). For
example, USDA's Agricultural Marketing Service uses Cp to monitor
process control of fat content meeting allowable upper and
specification lower limits and a one-side calculated process capability
to monitor process control of microbial detection levels meeting upper
allowable limits in raw beef finished products as part of the National
School Lunch Program.\144\
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\143\ Montgomery, D.C. (2013). Introduction to Statistical
Quality Control 7th edition, chapter 5.
\144\ AMS National School Lunch Program, information available
at: https://www.fns.usda.gov/nslp.
---------------------------------------------------------------------------

Using microbiological testing to monitor SPC presents some
challenges. Some testing may result in a discrete (presence/absence or
binary) result or a continuous measure such as a plate

[[Page 64711]]

count. Binary results and plate counts are typically modeled using a
binomial or Poisson probability distributions, and their log-
transformed values usually follow a lognormal distribution from which
the statistical mean and variance may be calculated and used for SPC
analyses that assume a normal probability distribution. Count data may
include zero results, either due to the absence of the organism, or
presence at levels below or above the test's limits of quantitation
(LOQ). The later result is referred to as a censored value. Data with
censored results exceeding the number of zeros expected by the Poisson
distribution may consist of a heterogeneous mixture in which the
organism is completely absent from some portion of the product and
present in another portion. Such results may follow a zero-inflated
Poisson distribution. A variety of methods have been proposed to fit
censored data to a probability distribution. The choice of method
depends on the number of samples and the proportion with enumerated
samples. A distribution function cannot be reliably fitted to a dataset
where fewer than 20 percent of samples are enumerated,\145\ which is an
important consideration for using count data. Other considerations for
SPC include sampling frequency and lot definition. With respect to
frequency, counts are more robust than binary results, and indicators
of process control are best obtained with higher frequency sampling.
NACMCF recommended sampling frequency be capable of detecting the
presence of expected assignable causes within the first 10 percent of
their persistence time since disruptions occur for a finite period and
not much is learned if the disruption is not detected or detected too
late for corrective action. Product lot definition has implications
both for determining the acceptability of a lot and for monitoring SPC.
In general, the defined product lot should be produced under reasonably
constant conditions so that a lot is a homogeneous volume of
contemporaneous production for calculating the mean level and
variability. For poultry slaughter and dressing, a homogeneous volume
of contemporaneous production means that each lot should represent a
cohort (flock) of birds raised, transported, slaughtered and processed
over the same period and locations. Production lots with equivalent
means may have different variabilities and therefore, SPC methods
should evaluate variance both within and between production lots.
---------------------------------------------------------------------------

\145\ Williams, M.S., et al. (2013). ``Sample size guidelines
for fitting a lognormal probability distribution to censored most
probable number data with a Markov chain Monte Carlo method.''
International Journal of Food Microbiology 165(2): 89-96.
---------------------------------------------------------------------------

When a microbiological sampling program is properly designed and
implemented, it can provide valuable information about an
establishment's process control. A well-designed microbiological
sampling program should clearly define the intended use of the testing
program, organisms of concern that will be the target of testing,
sampling units (flocks, houses at preharvest, carcasses or parts at
post-harvest), sampling scheme, microbiologically independent lotting
practices, sampling locations, procedures for sample collection and for
maintaining sample integrity, testing method, method for evaluating
test results, and actions taken based on test results.\146\ Results
charting is typically used to identify trends and for identifying
exceptions to process control that could be due to assignable causes.
For low frequency binary results, NACMCF recommended a g-chart based on
mean time between events. For higher frequency binary results, a p-
chart based on proportions is recommended, and for counts, mean and
range charts can be used.
---------------------------------------------------------------------------

\146\ NACMCF (2019). ``Response to Questions Posed by the Food
Safety and Inspection Service Regarding Salmonella Control
Strategies in Poultry.'' Journal of Food Protection 82(4): 645-668.
---------------------------------------------------------------------------

In 2019, NACMCF concluded that most carcass contamination results
from leakage of ingesta during crop removal, from feces during
evisceration, as well as aerosolization during picking.\147\ The
committee also advised, to best assess controls, each establishment
should look at the whole food safety system from breeder farm through
processing, so it is not overwhelmed by the incoming load. Evaluating
the prevalence and concentration of Salmonella on carcasses and parts
throughout the production process unique to each facility can help to
identify pathogen reduction at each step in the process.
---------------------------------------------------------------------------

\147\ NACMCF (2019). ``Response to Questions Posed by the Food
Safety and Inspection Service Regarding Salmonella Control
Strategies in Poultry.'' Journal of Food Protection 82(4): 645-668.
---------------------------------------------------------------------------

In its October 2021 charge to the NACMCF Subcommittee on Enhancing
Salmonella Control in Poultry Products, FSIS noted there is a
documented correlation between a reduction in the quantity of AC
between carcasses and finished products and the occurrence of
Salmonella in finished products for beef, pork, and poultry. The Agency
specifically requested that the Subcommittee provide guidance on how
this information might be used to set microbiological criteria to
assess process (pathogen) control in poultry.\148\
---------------------------------------------------------------------------

\148\ 2021-2023 NACMCF report: Question 5.
---------------------------------------------------------------------------

In response to FSIS' request for guidance on setting
microbiological criteria to assess process control in poultry, the 2023
NACMCF report discussed process control as a method of determining
trends over time and how it is useful to determine the sources of
variation within a process. It noted that ``indicator organisms such as
Enterobacteriaceae (EB) or [AC] have been used by the industry as
gauges of process control and to measure the microbial reduction from
carcasses at slaughter to post-chill.'' The report stated that
``studies show conflicting and apparent weak correlation between
indicators and either the presence or level of Salmonella post carcass
wash.'' The report also stated that, in addition to published studies,
``unpublished data provided by the poultry industry and university
researchers suggests that indicator bacteria have very limited
predictive value for the prevalence of Salmonella.''
Although the report found that the available data show that in many
cases there may not be a strong statistical correlation between the
presence or amount of an indicator and the presence or amount of
Salmonella at specific points during processing or in finished poultry
products, the report concluded that, ``. . . a change in [AC] from an
early sampling point on the slaughter line to a final sampling point on
the processing line, as well as absolute levels at the final point, may
provide useful information about the effectiveness of the process in
maintaining hygienic conditions.'' Therefore, the report concluded,
``[AC] may be useful to indicate process control even though it is not
a true indication of the presence, level, or virulence of Salmonella.''
2. PHIS Inspection Data
The purpose of 9 CFR 381.65(g) and (h) is to ensure that
establishments implement appropriate measures to prevent carcasses from
becoming contaminated throughout the slaughter and dressing operation.
Establishments must design and implement a program that uses
microbiological sampling and analysis to monitor their ability to
maintain process control and produces the documentation needed for FSIS
and the establishment to continuously verify the effectiveness of these
measures on an on-going basis, i.e., an MMP. Establishments must
provide scientific and technical support to justify the design of their
MMPs.

[[Page 64712]]

As discussed, SPC monitoring evaluates microbial data against
predefined quantitative and qualitative specifications. SPC monitoring
results that do not fall within the predefined specifications with
assignable causes indicate a process is not capable or in control. An
effective MMP must, therefore, define and support the quantitative and
qualitative microbial monitoring criteria an establishment will use to
gauge whether its process is in control and the corrective actions it
will take when its microbial monitoring results are not within its
predefined parameters. Specifically, the establishment MMP must
incorporate three criteria--target change, quantitative consistency,
and qualitative consistency standards. ``Target change'' refers to the
expected change in quantified levels of microbial contamination
detected between two monitoring points that supports the procedures'
ability to control contamination as required in 9 CFR 381.65(g) and as
expected by the establishment. ``Quantitative consistency'' is measured
by how close individual sampling results are to defined target change
parameters and how much variation is expected amongst the results over
time. ``Qualitative consistency'' is measured by assessing whether MMP
process control findings are consistent with other process control
monitoring results representing the same procedures (e.g., fecal zero
tolerance monitoring). Consistency can also be qualitatively assessed
as whether the MMP process control determination is consistent with the
process control determination for the HACCP system overall, i.e., if
all HACCP monitoring intended to assess process control draws the same
conclusion. An effective MMP also defines how an establishment will
respond when performance is not as expected, such as the corrective
actions it will take.
A recent analysis of PHIS inspection data identified issues with
the design and implementation of establishment MMPs, including how
establishments respond to MMP results.\149\ FSIS analyses of the PHIS
inspection verification data from February 17, 2015, through December
31, 2022, found that MMP noncompliance with 9 CFR 381.65(g) was most
often associated with sampling frequency and the monitoring of results
to ensure frequency compliance (49 percent). Specifically, NRs showed
establishments did not plan or adjust their sampling plan minimum
frequencies in accordance with the actual slaughter volume; failed to
collect samples at the frequency planned, at the minimum frequency
required, or to collect additional samples when collected samples could
not be analyzed. These noncompliance issues indicate that
establishments are not assessing or adjusting the sampling frequency
procedures in their MMPs as necessary due to their failure to identify
and document the absence of expected monitoring results. These
noncompliance issues also show that establishments often fail to
provide adequate justification for not evaluating and updating the
sampling frequency procedures in their MMPs in response to monitoring
results, IPP observations, or other relevant information indicating
that their current sampling frequency is not adequate to monitor
process control.
---------------------------------------------------------------------------

\149\ 7096 noncompliance records (NRs) citing 381.65(g) were
issued between 2/17/2015 and 12/31/2022; 8 had incomplete
descriptions and were not further analyzed. Each of the 7088 NRs
were read by OFO analysts to determine if the microbial monitoring
program was reviewed as part of the verification and if the
establishment microbial monitoring program was documented to be the
cause of observed noncompliance.
---------------------------------------------------------------------------

NRs also indicated establishments failed to identify monitoring
criteria, monitoring deviations, or documented trends or--when
identified--failed to perform any root cause assessment for the
deviation or perform corrective actions (31 percent). Further, NRs show
that establishments failed to implement their sample collection or
laboratory analysis methods as written (12 percent). These findings
indicate establishments are not adequately considering or utilizing the
MMP monitoring of process control in their overall consideration of
whether the procedures incorporated into the HACCP system are
performing as expected and the HACCP system is overall controlling the
hazard to the acceptable level as intended.
3. Exploratory Sampling Program Data
As noted above, from April to November 2022, FSIS implemented an
exploratory sampling program \150\ to generate microbial data to inform
the Agency's effort to reduce Salmonella illnesses attributable to
poultry. Under the program, rehang and post-chill rinsate samples were
tested for Salmonella, AC, and EC, and beginning August 11, 2022, for
Salmonella levels using a quantitative method adopted by FSIS
laboratories.
---------------------------------------------------------------------------

\150\ FSIS Notice 44-22Revised Young Chicken Carcass Exploratory
Sampling Program.
---------------------------------------------------------------------------

Overall, FSIS analyzed 4,654 paired samples collected from 204 of
the 272 establishments that slaughtered young chicken in Calendar Year
2022. Testing results indicated that 2,910 rehang and 232 post-chill
samples were positive for Salmonella. Of these, 1,460 rehang and 121
post-chill samples were analyzed with the Salmonella quantitative
method, and the results indicated that approximately 90 percent of
rehang and 86 percent of post-chill samples were below the lower
LOQ.\151\ Further, out of the 4,654 paired samples, tests detected AC
in 4,592 and EB in 4,580 of both the rehang and post-chill location
samples. Of the pairs that detected the AC or EB at both locations,
69.2 percent of the pairs yielded a quantified value at both rehang and
post-chill for AC; whereas only 15.9 percent yielded a quantified value
for EB.\152\
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\151\ The lower LoQ for the Salmonella, AC, and EC tests
utilized by FSIS laboratories was 10 cfu/mL.
\152\ Comparatively, FSIS's 2007-2008 baseline survey did not
assess results as true pairs or when both rehang and post-chill
yielded quantifiable results. This prior survey reported the 3,275
analyzed pairs had levels significantly lower at post-chill and
quantifiable AC and EC was detected in 97.1 percent and 57.4 percent
of post-chill samples, respectively. The average rehang and post-
chill AC values reported 4.51 log AC and 2.43 Log AC and EC as 3.28
Log EC and 1.57 Log EC, respectively (average change 2.08 Log AC and
1.71 Log EC). https://www.fsis.usda.gov/node/1973.
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Of the 3,177 paired samples with quantified levels of AC, 98.7
percent demonstrated a reduction in AC from rehang to post-chill; while
only 1.29 percent of paired samples demonstrated an increase in
AC.\153\ Among the 180 establishments with 12 or more analyzed paired
samples,\154\ all 180 establishments had greater than 20 percent of
samples with AC detectable above the lower LOQ at post-chill, and 25
percent had greater than 20 percent of samples with EB above the lower
LOQ. Salmonella percent positive was reduced from rehang to post-chill
by an average of 56.6 percent and AC quantified level was reduced an
average of 2.93 log10 cfu/mL (74 percent reduction).
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\153\ Because a distribution function cannot be reliably fitted
to a dataset where fewer than 20 percent of the samples are above
the LOQ, FSIS has only summarized results for quantitative AC, not
Salmonella or EC. See Helsel, D. R. (2005). ``Nondetects and Data
Analysis: Statistics for Censored Environmental Data.''
\154\ FSIS had estimated at least 12 pairs would be necessary
over the study period to evaluate an individual establishment's
indicator organism performance and 180 of the 204-establishment
sampled had at least 12 pairs analyzed.
---------------------------------------------------------------------------

Based on these findings, FSIS concluded that microbial monitoring
of EB or Salmonella is unlikely to yield the reliable quantified
results necessary for an individual establishment to support SPC
monitoring. There has been an observable decline in post-chill levels
of organisms detected since the 2007-2008

[[Page 64713]]

Young Chicken Baseline Survey. The current data shows that AC is more
likely to yield reliably detectable quantified microbial results
compared to either EB or Salmonella for most establishments.
Additionally, given all establishments sampled consistently
demonstrated a qualitative decrease in levels of organisms detected
between rehang and post-chill, FSIS has determined that assessing the
quantified level of decrease achieved is more informative of individual
establishment process control changes and trends than the qualitative
criteria of whether a decrease occurred.
4. FSIS Risk Assessments
The 2023 risk assessments for Salmonella in chicken and turkey
evaluated, among other things, the public health impact of monitoring
and enforcing process control from rehang to post-chill.\155\ For all
young chicken establishments sampled during the 2022 exploratory
sampling program, FSIS measured an average of 4.40 and 1.39 log AC per
mL at rehang and post-chill locations, respectively, i.e., an average
reduction of 3.01 log AC per mL. Comparatively, the 2007-2008 baseline
survey measured an average of 4.50 and 2.46 log AC per mL at rehang and
post-chill locations, respectively, i.e., an average log reduction of
2.04 log AC per mL. These data show that between 2008 and 2022, there
were no decreases in incoming AC loads on chicken carcasses; however,
during that time, establishments achieved an additional 1 log reduction
in AC levels after slaughter and processing. Based on this current
study it is reasonable to expect reductions of 3 logs in Salmonella
between rehang and post-chill. The risk assessment found weak
correlations between post-chill Salmonella prevalence and AC, either
based on the AC reduction between rehang and post-chill, or the
fraction of post-chill samples where AC is not observed. Ultimately,
FSIS' recent chicken risk assessment concluded that a hypothetical AC
reduction standard could achieve a 25 percent reduction in Salmonella
illnesses attributed to chicken only if microbiological criteria based
on 2.5-3.0 log reduction or no AC tests exceed 10 cfu/mL at the post-
chill location. The risk assessment concluded that AC is only
moderately correlated with the occurrence of Salmonella and thus an AC
based standard would perform less well than a Salmonella standard.
---------------------------------------------------------------------------

\155\ The risk assessments analyzed data from the 2022
Exploratory Project, 2007-2008 Young Chicken Baseline Survey, and
the 2008-2009 Turkey Baseline Survey.
---------------------------------------------------------------------------

In addition to identifying a decrease in the average level of log
AC detected at post-chill between the 2007-2008 baseline survey and
2022 exploratory sampling program from 2.46 to 1.39 log AC per mL,
respectively, the 2023 chicken risk assessment identified a decrease in
the proportion of young chicken carcass post-chill AC results above the
limit of detection (LOD), from 97.1 percent at baseline to 70.0 percent
currently. EB followed a similar trend with 57.4 percent during the
prior baseline to just 16.1 percent above the LOD currently.
The 2023 turkey risk assessment reported that the correlation
between AC or EB and Salmonella prevalence is weak, and it was not
possible to fully assess the public health impact of monitoring and
enforcing process control from rehang to post-chill.

C. Proposals To Enhance Establishment Process Control Monitoring

FSIS is proposing to amend 9 CFR 381.65(g) and (h) to establish new
requirements pertaining to how establishments monitor and document
whether their processes for preventing microbial contamination
throughout the slaughter and dressing operation are in control. The
goal of the proposed amendments is to clarify existing regulatory
requirements related to process control monitoring and recordkeeping in
9 CFR 381.65(g) and (h) and to better define requirements with respect
to the type of microbial data that should be collected, how the data
should be analyzed, the level of acceptable process control deviations,
and how establishments should respond to process control deviations.
The clarifications are also intended to promote the collection of more
standardized data by establishments to facilitate data quality. If this
proposed rule is finalized, FSIS intends to update relevant guidance to
help establishments comply with new requirements.
1. SPC Monitoring
This proposed rule revises 9 CFR 381.65(g) to require
establishments to incorporate SPC monitoring principles into their
MMPs. As discussed, SPC monitoring uses statistical methods to compare
quantitative results against predefined benchmarks and, thereby,
determine whether a process is operating within expected
parameters.\156\
---------------------------------------------------------------------------

\156\ NACMCF (2015). '' Regarding Microbiological Criteria as
Indicators of Process Control or Insanitary Conditions, available at
https://www.fsis.usda.gov/sites/default/files/media_file/2020-07/NACMCF-Report-Process-Control-061015.pdf.
---------------------------------------------------------------------------

The proposed revisions to 9 CFR 381.65(g) would therefore require
establishments to use only validated microbial sampling and laboratory
analysis procedures, generate and record statistically meaningful
microbial monitoring data, set benchmarks by which to evaluate
microbial monitoring data, and to otherwise define the statistical
methods the establishment will use to evaluate the recorded data
against the predefined limits. The MMP design should also be consistent
with other process control monitoring procedures and the
establishment's HACCP system. For example, if an establishment assesses
process control independently by evisceration line for visible fecal
contamination, the establishment's MMP for process control of
procedures to prevent fecal contamination should also be separated by
evisceration line.
Statistical Methods. There must be scientific and technical support
to justify the design of a MMP, including the statistical methods an
establishment will use. Specifically, the MMP must include
documentation and data demonstrating the initial scientific basis,
validation, and ongoing verification of the statistical methods,
including whether the quantified monitoring data generated by the
establishment's process is normally or not normally distributed and
whether the statistical method is appropriate. In instances where the
minimum sampling frequency requirements of 9 CFR 381.85(g)(2) do not
generate ``statistically robust'' results, an establishment must either
increase its sampling frequency to generate robust results or provide
support to demonstrate that the minimum frequency of collection is,
nonetheless, adequate to demonstrate whether its particular process is
in control.
FSIS has developed a Lower Capability Process Index (CPL)
Statistical Measurement Model (SMM) which fits parameters for normally
distributed data. The CPL-SMM is available for review and comment on
the FSIS website.\157\ Under this proposal, the CPL-SMM would be
considered a ``safe harbor,'' in that establishments that incorporate
the CPL-SMM into their MMPs would not be required to provide FSIS with

[[Page 64714]]

additional scientific or technical information to support their chosen
statistical methods.\158\ Should FSIS finalize this proposal, the
Agency would make available on its website an electronic file for
download (i.e., a spreadsheet) programmed to calculate the change
achieved, CPL, and chart results as the establishment inputs each
sampling result as it is received from the laboratory. FSIS will
provide relevant instructions for adopting the ``safe harbor'' method
in a future guidance document. An example of the electronic file that
FSIS intends to provide is available for viewing and public comment at:
https://www.regulations.gov/docket/FSIS-2023-0028.
---------------------------------------------------------------------------

\157\ Statistical Process Control Monitoring Method Assessment
and the FSIS Proposed Lower Capability Process Index (CPL)
Statistical Measurement Model (SMM) available at: https://www.regulations.gov/docket/FSIS-2023-0028.
\158\ Establishments are to be aware that the proposed CPL-SMM
reflects the minimum frequency prescribed in 9 CFR 381.65(g)(2), and
the establishment may need to increase the frequency of collection
to meet compliance with the requirement the frequency is adequate to
monitor their ability maintain process control as required under 9
CFR 381.65(g)(2)(iii).
---------------------------------------------------------------------------

FSIS requests comments on its proposed CPL-SMM and the related
electronic file. FSIS also requests input on any other statistical
monitoring methods that FSIS should recognize as satisfying the
requirements of 9 CFR 381.65(g) without further scientific support,
including but not limited to methods for normally and non-normally
distributed results, use with specific indicator organisms, and various
analyzed results sample sizes. FSIS requests that commenters include
the appropriate data necessary to support any proposed alternatives as
these data may not have been available to FSIS at the time of this
rulemaking.
Target Change and Quantitative Consistency Criteria. To effectively
incorporate SPC monitoring into an MMP, establishments must define and
support target change and quantitative consistency microbial monitoring
criteria. ``Target change,'' in the context of microbial process
control monitoring, is the expected change in quantified levels of
microbial contamination detected between two sampling locations that
supports a procedure's ability to control contamination as minimally
required in 9 CFR 381.65(g) and as expected by the establishment. For
an MMP, target change parameters must be appropriate for the microbial
monitoring organism an establishment uses to monitor process control.
At a minimum, establishment MMPs must define the minimum target change
expected (lower specification limit). The minimal level target change
approach sets a benchmark from which establishments can evaluate trends
in microbial contamination during slaughter and dressing with other
trends in slaughter performance data such as pathogen, feces and
ingesta, and sanitary operations monitoring findings. Establishment
MMPs may also define a maximum target change expected (upper
specification limit).
AC and EB are routinely utilized to monitor poultry slaughter
process control and are frequently reported in logarithmic format
(log).\159\ FSIS' review of current scientific support indicates that,
when monitoring indicator organisms reported in log, establishments
should strive for a minimum target change value of 1 log reduction and
that a change between 0 and 1 log is not reliably detected in normally
distributed data, particularly at the statistical power associated with
the single pair minimum sampling frequencies prescribed in 9 CFR
381.65(g)(2).\160\ The 2023 risk assessment also identified a moderate
correlation with the detection of post-chill Salmonella when at least a
3 log AC change was observed.\161\ Moreover, FSIS' exploratory sampling
program observed an average 2.93 log AC reduction in establishments
with at least 12 carcass pairs analyzed.
---------------------------------------------------------------------------

\159\ Microbial organism levels are frequently transformed to
base 10 logarithmic format (log) for statistical assessment unless
the conversion would result in log ``0' censored data result.
\160\ De Villena, J.F., et al. (2022). ``Bio-Mapping Indicators
and Pathogen Loads in a Commercial Broiler Processing Facility
Operating with High and Low Antimicrobial Intervention Levels.''
Foods 11(6): 775. Cano, C., et al. (2021). ``Application of
Peroxyacetic Acid for Decontamination of Raw Poultry Products and
Comparison to Other Commonly Used Chemical Antimicrobial
Interventions: A Review.'' J Food Prot 84(10): 1772-1783. Brashears,
M.M. and B.D. Chaves (2017). ``The diversity of beef safety: A
global reason to strengthen our current systems.'' Meat Sci 132: 59-
71.
\161\ Quantitative Microbial Risk Assessment for Salmonella in
Raw Chicken and Raw Chicken Products at: https://www.regulations.gov/docket/FSIS-2023-0028.
---------------------------------------------------------------------------

Based on these findings, the Agency would consider an
establishment's target change criteria to meet the requirements in 9
CFR 381.65(g) when its MMP sets an expected reduction of at least 1.0
log in detected microbial levels between sampling locations.\162\
Establishments may, of course, set more stringent target change
criteria in their MMP than the minimum 1.0 log reduction without
providing additional support to FSIS. MMPs that define an expected
target change value of less than 1.0 log must include comprehensive
scientific support to demonstrate that its target change criteria
reflect a statistically reliable value for measuring process control
and why its expected target change is less than changes identified in
national baseline data (e.g., 2 log or 3 log as above). Establishments
that conduct microbial sampling and testing in more than two locations
in the slaughter process may define different quantified values to be
achieved between the various points but, minimally, the target change
value for monitoring between each pair of points should meet the
minimum requirement as appropriate for the microbial monitoring
organism being monitored. Similarly, establishments monitoring more
than one shift, evisceration line, or species/subclass of poultry may
elect to define different quantified target change values expected
providing they meet the same minimum requirements. In any event,
establishments must use scientifically validated mathematical methods
to calculate the change in levels detected between sampling locations.
FSIS would consider a simple subtraction method (e.g., Sampling Point-A
log value--Sampling Point-B log value) to be scientifically valid.
---------------------------------------------------------------------------

\162\ FSIS notes that all sample results in the exploratory CPL-
SMM modeling datasets had AC reductions greater than 1 log (97.5
percent) and mean log AC reductions across the exploratory sampling
period were greater than 1 for 98.7 percent of establishments.
---------------------------------------------------------------------------

MMPs must also define quantitative consistency criteria. As
discussed, SPC monitoring includes assessing the variation of results
as each result is reported and over time to identify and detect when
procedures may not be functioning as intended to prevent the enteric
pathogen and fecal contamination from being introduced at one or more
points in the process. In statistical applications, 99 percent of
results fall within 6 standard deviations of the mean, or 3 standard
deviations on either side of the mean. For an MMP monitoring whether
the minimum target change expected is met (lower specification), the
detected change between the two points monitored is within 3 standard
deviations less than the average change detected for all samples in the
monitoring period.
The establishment MMP must define and support the acceptable
quantitative consistency (statistical variation) expected among the
changes detected over time. The quantitative consistency expected must
not exceed 3 standard deviations lower than the mean and for the
establishment to conclude microbial contamination variability was
controlled (one-side for lower specification). That is, FSIS recognizes
the MMP defined quantified value is minimally supported when the sample
result is no more than 3 standard deviations below the mean. As with
target change criteria, establishments are

[[Page 64715]]

encouraged to define quantitative consistency criteria at each point
monitored and may also set quantitative consistency criteria specific
to shift, line, or specific/subclass of poultry slaughtered, provided
the consistency variation target limit meets the minimum requirements
discussed herein. Establishment MMP monitoring criteria decisions for
target change and quantitative consistency expected, and the actual
values observed during monitoring, must also consider and support the
establishment's MMP organism, location, and frequency decision
rationale. Establishments must assess their results as ongoing
validation data to maintain support for all MMP requirements.
Monitoring Period. As discussed, SPC involves an assessment of
trends measured over time. As such, an establishment's MMP must define
the period over which trends will be assessed, i.e., the ``monitoring
period.'' FSIS' assessment of exploratory sampling program and
Salmonella Initiative Program \163\ data found that the sample
collection frequency impacts the monitoring period required to generate
a statistically robust sample size and how quickly the entire sample
size is replaced with new results, i.e., the ``sample size turnover.''
Based on the assessment of these available data, FSIS has identified
the monitoring periods necessary for establishments to adequately
assess trends over time. Establishments that incorporate these
monitoring periods into their MMPs would not be required to provide the
Agency with additional scientific or technical support.
---------------------------------------------------------------------------

\163\ FSIS Salmonella Initiative Program, details available at
https://www.fsis.usda.gov/science-data/data-sets-visualizations/microbiology/microbiological-testing-program-rte-meat-and.
---------------------------------------------------------------------------

As shown in Table 10 below, FSIS recommends that establishment MMPs
define the monitoring periods as follows by the minimum monitoring
frequency (paired carcass collection) prescribed in 9 CFR 381.65(g):
(1) Poultry establishments collecting samples at a frequency of once
per 22,000 (chicken) or 3,000 (other species) head slaughtered,
respectively, or greater, are to designate a monitoring period of 140
samples or 52 weeks, whichever is shortest; (2) any poultry
establishments collecting at a weekly frequency are to designate a
monitoring period of the 52 most current weeks; (3) and VLV poultry
establishments collecting 13 samples annually are to designate their
monitoring period as all of the samples available in the most recent 52
weeks or all the samples in the current period of operations if
slaughter of the predominant species is seasonal and not continuous.
All poultry slaughter establishments are required to assess for trends
during their designated monitoring period, as well as compare the
monitoring periods for the current 52 weeks against the prior 52 weeks.
Further, those establishments that collect less than weekly are to also
compare trends going back an additional 52 weeks (i.e., compare the
current 52 weeks against the prior 104 weeks). All poultry slaughter
establishments must also identify the sample size turnover rate based
on their intended frequency of collection and provide scientific
support for how the establishment will consider the turnover in their
assessment of process control trends over time.

Table 10--Monitoring Period by Minimum Frequency Recognized by FSIS Without Further Support
----------------------------------------------------------------------------------------------------------------
Minimum monitoring Minimum trend over
Poultry species frequency Minimum monitoring period time period
----------------------------------------------------------------------------------------------------------------
Chicken............................ >=1 per 22,000 head... Period necessary to obtain Prior 52 weeks.
140 samples or 52 weeks,
whichever is shorter.
Turkey, Goose, Guinea, Duck, Squab. >=1 per 3,000 head....
Any Poultry Species................ Weekly................ 52 weeks...................
Any Poultry Species................ 13 per year........... All samples in 52 weeks or Prior 104 weeks.
the period of operations
for year if seasonal
operations.
----------------------------------------------------------------------------------------------------------------

2. Microbial Monitoring Organism
FSIS is proposing to amend 9 CFR 381.65(g) to establish new
criteria that an establishment must meet to demonstrate that its
selection of microbial organism is fit for purpose. Specifically, FSIS
is proposing that establishments analyze for microbial organisms that
are quantifiably detectable in the establishment's slaughter process
and that will generate microbial monitoring data that is adequate to
monitor their ability to maintain process control for enteric
pathogens. Under this proposal, the establishment's measured results at
each sample location must yield statistically reliable quantified value
results.
The Agency recognizes that in order to successfully analyze
quantified data, at least 20 percent or more of the sample size results
must be quantified; otherwise, the data will be skewed, i.e., shifted
above or below the true value.\164\ Thus, to comply with the proposed
revisions to 9 CFR 381.65(g), establishments would have to demonstrate
and continuously validate that their chosen microbial monitoring
organism generates a quantified value in at least 20 percent of the
results reported at each monitored location. Results that are reported
``above the limit of quantification'' or ``below the limit of
quantification'' or ``0'' when log transformed would not be considered
as quantified results, nor would samples with results not analyzed by
the establishment. The establishment would also have to demonstrate and
continuously validate that for each sample monitoring location, the
microbial organism can be quantified across the upper and lower levels
that actually occur in the establishment's individual process.
---------------------------------------------------------------------------

\164\ Helsel, D.R. (2005). ``Nondetects and Data Analysis:
Statistics for Censored Environmental Data.''
---------------------------------------------------------------------------

The Agency would consider the use of AC to monitor process control
to meet the proposed criteria discussed above. FSIS has evaluated the
available published studies and data at the time of rulemaking and
concluded that AC are the microbial organisms most likely to result in
quantified results that are reliably detectable at rehang and post-
chill. Available paired microbial data representing pathogens like
Salmonella and indicator organisms other than AC do not meet the 20
percent minimum quantified detection recommended. Establishments that
choose to use other indicator organisms like EB, total coliforms, or
GEC to assess the minimum target level of change, equal to or greater
than 1 log10, must support the estimated change in a statistically
appropriate manner.

[[Page 64716]]

Regardless of the microbial monitoring organism chosen, the
proposed revisions would require establishments to demonstrate that
their chosen sample collection method is appropriate for the product
sampled, the microbial organism monitored, and the laboratory method
used to analyze the samples. Moreover, the proposed revision would
require establishments' microbial sampling results to be generated by
validated laboratory analyses and methods. Current HACCP regulations
also require ongoing verification of the establishment's microbial
monitoring procedures including the methods and equipment used (9 CFR
417.4).
Establishments that adhere to the Agency's carcass rinse and sponge
sample collection method \165\ would not be required to provide
additional support to justify their chosen method of organism
collection. Further, establishments that document sample analyses by
International Standards Organization (ISO) or USDA's Accredited
Laboratory Program (ALP) accredited laboratories would not be required
to provide the Agency with additional support to justify their use of
laboratory analyses and methods. Nonetheless, all establishments would
be required to demonstrate and continuously validate that their MMPs
analysis method can detect the selected microbial monitoring organism
at the levels intended, expected, and occurring at the monitored points
in the process. FSIS requests comments on whether FSIS should require
establishments to use ISO accredited or USDA ALP accredited
laboratories to analyze their microbial monitoring samples.
---------------------------------------------------------------------------

\165\ FSIS Directive 10,250.1, Salmonella and Campylobacter
Verification Program for Raw Poultry Products, https://www.fsis.usda.gov/policy/fsis-directives/10250.1.
---------------------------------------------------------------------------

In lieu of requiring the VS or VLV establishments that slaughter
the predominate species of poultry under Traditional Inspection to
utilize their own resources to meet compliance with the proposed
revisions to 9 CFR 381.65(g), FSIS is proposing that such
establishments have access to laboratory services provided by FSIS at
no monetary cost for sample supplies, analyses, or shipment. Eligible
establishments would be required to agree to terms of participation
that would be publicly announced following the publication of any final
rule resulting from this proposal. These terms would limit the use of
laboratory microbial analyses service to eligible establishments that
sample for AC, given more than 75 percent of the post-chill carcass
samples analyzed as part of the recent FSIS exploratory sampling
assessment were below the FSIS lower limit of detection for EB and
nearly 85 percent of the enumerated post-chill Salmonella were below
the level of quantification.\166\ The terms would also address
laboratory service logistics such as establishment sample collection
and shipment methods, collection and shipment dates to assure
laboratory analysis capacity, reporting of establishment results
through PHIS and LIMS-Direct email, and that the establishment agree to
incorporate the FSIS CPL-SMM into its MMP exactly as described in the
Statistical Process Control Monitoring Method Assessment and the FSIS
Proposed Lower Capability Process Index (CPL) Statistical Measurement
Model (SMM) at: https://www.regulations.gov/docket/FSIS-2023-0028.
---------------------------------------------------------------------------

\166\ Quantitative Microbial Risk Assessment for Salmonella in
Raw Chicken and Raw Chicken Products at: https://www.regulations.gov/docket/FSIS-2023-0028.
---------------------------------------------------------------------------

3. Sampling Location
FSIS is proposing to revise the sampling location regulations at 9
CFR 381.65(g)(1) to require that establishments, at a minimum, collect
and analyze samples for microbial organisms at the rehang and post-
chill points in the process, as opposed to the pre-chill and post-chill
locations. FSIS has determined that sampling at the rehang point in the
process, i.e., after picking and prior to evisceration, is likely to be
more effective for monitoring process control, given the introduction
of carcass contamination tends to occur at slaughter process steps at
or just prior to the rehang location and evisceration \167\ and pre-
chill sampling often takes place after evisceration and some
antimicrobial interventions have already occurred.\168\ The FSIS 2023
chicken risk assessment and FSIS assessment of exploratory sampling
program data reported that there has been an increase in the log AC
reduction achieved between rehang and post-chill influenced mostly
because the levels of indicator organisms detected post-chill have
declined since the prior 2007-2008 baseline study. FSIS has observed
that pre-chill samples collected after evisceration and after most
interventions, and prior to the chiller, typically have lower levels of
organisms detected than rehang samples collected prior to evisceration
and fewer intervention steps.
---------------------------------------------------------------------------

\167\ NACMCF (2019). ``Response to Questions Posed by the Food
Safety and Inspection Service Regarding Salmonella Control
Strategies in Poultry.'' Journal of Food Protection 82(4): 645-668.
\168\ Exploratory Project questionnaire responses indicate that
51 percent of the establishments applied one or more interventions
prior to rehang, whereas all but one establishment applied one or
more interventions after rehang.
---------------------------------------------------------------------------

Under this proposal, establishments would be required to identify
and provide supporting rationale for the exact point where they intend
to collect their rehang sample. Establishments would be permitted to
collect a pre-chill sample at a location other than rehang if they
provide supporting data to demonstrate that the alternative location is
at least as effective as rehang sampling for monitoring their ability
to maintain process control. However, one benefit of rehang sampling is
that it allows establishments to assess the level of microbial
contamination early in the slaughter process and, thereby, better
understand the level of enteric pathogen hazard associated with flocks
at receiving. Also, according to NACMCF, monitoring change in AC ``from
an early sampling point on the slaughter line to the final sampling
point on the processing line . . . may provide useful information about
the effectiveness of the process in maintaining hygiene conditions.''
\169\ Moreover, continuing to monitor at pre-chill, which tends to
occur after establishments apply antimicrobial interventions, would
make it more difficult for establishments to justify how the microbial
monitoring data they generate validates that their established target
change and quantitative consistency parameters are adequate to monitor
process control. Thus, ideally, the exact point of an establishment`s
rehang sampling should be immediately after the early slaughter
processing steps that are mostly likely to introduce microbial
contamination and before the establishment's use of antimicrobial
interventions. Establishments slaughtering poultry predominantly under
religious exemptions that result in feet on, un-eviscerated carcasses,
or otherwise are slaughtered at post-picking but prior to the
evisceration rehang step are to collect samples at the point in the
process that results in the greatest source of introduction of enteric
pathogen and fecal contamination.
---------------------------------------------------------------------------

\169\ 2021-2023 National Advisory Committee Meeting on
Microbiological Criteria for Foods (NACMCF); FSIS Charge: Enhancing
Salmonella Control in Poultry Products Available at: https://www.fsis.usda.gov/policy/advisory-committees/national-advisory-committee-microbiological-criteria-foods-nacmcf/2021.
---------------------------------------------------------------------------

Finally, FSIS' proposed amendments to 9 CFR 381.65(g)(1) would
require VS and VLV establishments operating under Traditional
Inspection to--like all other establishments--collect and analyze
microbial samples at rehang and

[[Page 64717]]

post-chill locations. These establishments are currently required to
collect microbial samples at the post-chill point only. To offset the
economic impact of this amendment, these establishments would be
eligible to have access to laboratory services provided by FSIS at no
cost as described and discussed above. The FSIS 2023 risk assessment
and the Agency's assessment of the exploratory sampling program data
both recognized that greater levels of detected microbial organisms
were more likely to be observed in the smaller size and volume
establishments than the larger establishments, although microbial
levels detected at post-chill were overall lower than previously
observed during the 2007-2008 baseline study. FSIS has concluded that
post-chill samples representing only the end of the slaughter process
does not provide the same level of MMP adequacy to monitor process
control throughout the slaughter and dressing process as minimum two-
point sampling. Microbial monitoring at both rehang and post-chill will
help VS and VLV establishments operating under Traditional Inspection
to assess levels of microbial contamination at a point closer to the
start of the slaughter process and the effect that their anti-microbial
intervention steps have in reducing such contamination.
4. Sample Collection Monitoring Frequency
As discussed, a recent FSIS review of PHIS inspection data found
that MMP noncompliance issues were frequently associated with sampling
frequency and that the noncompliant establishments were most often
those that produced lower volumes of product. FSIS is proposing,
therefore, to amend 9 CFR 381.65(g) to make it easier for
establishments to understand and comply with minimum sampling frequency
requirements. First, FSIS is proposing to update the sampling frequency
regulations for VLV establishments, which currently require that such
establishments collect and analyze 13 weekly samples starting on June 1
of each year. FSIS has concluded that the current requirement would not
generate statistically robust process control monitoring data
regardless of if the results are collected over 13 consecutive weeks or
at other intervals throughout the year. FSIS has also concluded that
the June 1 requirement makes it difficult for VLV establishments to
demonstrate that their MMP is adequate to monitor process control
without collecting additional samples at other times of the year, such
as during the establishment's greatest seasonal production or the
slaughter of poultry from growers associated with greater risks of
increased microbial carcass contamination. As such, FSIS is proposing
to revise 9 CFR 381.65(g)(2)(ii) to remove the June 1 requirement and
otherwise give VLV establishments the flexibility to collect their 13
weekly samples in accordance with their slaughter operations throughout
the year. The MMP decision making rationale for all establishments,
regardless of annual slaughter volume, must support how the
establishment will determine when the monitoring will be performed and
how the specific carcass will be selected for sampling.
Second, to help all establishments better understand their minimum
sampling frequency requirements and develop their sampling frequency
procedures, FSIS is proposing to tie sampling frequency requirements to
annual slaughter volumes, as opposed to weekly slaughter volumes. As
discussed, FSIS review of NRs found that many establishments have
trouble planning or adjusting their sampling frequency regime to comply
with current regulations given actual weekly slaughter volumes tends to
fluctuate irregularly. Moreover, FSIS reviewed current sampling
frequency requirements relative to annual slaughter volumes and
determined that they require many lower volume establishments to
collect samples at a greater rate than larger establishments.\170\ The
proposed revisions, which are outlined in Table 11 and Table 12 below,
would simplify proposed slaughter volume criteria cut points for VLV,
low volume, and medium to high volume establishments and make it easier
for establishments to adapt to fluctuating conditions. Specifically,
FSIS is proposing that medium to large volume establishments
slaughtering as their predominant species more than 1,100,000 chickens
or 156,000 other poultry species annually be required to collect at a
minimum frequency of one paired sample every 22,000 or 3,000 head
slaughtered, respectively.\171\ Further, FSIS is proposing that LV
establishments that slaughter as their predominant species between
440,001 to 1,100,000 chickens or 60,001 to 156,000 other poultry
species annually be required to collect a minimum of one paired sample
a week, regardless of weekly fluctuations in their actual slaughter
volume. Lastly, FSIS is proposing that VLV establishments be required
to collect a minimum of 13 weekly paired samples per year. Those VLV
establishments that plan to operate less than 13 weeks per year may
collect their 13 annual samples on a less than weekly basis, assuming
they can demonstrate that their sample frequency is effectively
monitoring that they are maintaining process control throughout the
year and during any periods of slaughter operations. Regardless of
these minimum required frequencies, FSIS regulations would continue to
mandate that all establishments collect samples at a frequency that is
adequate for the establishment to monitor process control.
---------------------------------------------------------------------------

\170\ E.g., under current regulations, non-VLV establishments
that slaughter less than 22,000 chickens per week (i.e., between
440,001 to 1,144,000 head annually) are required to collect at least
1 sample weekly, resulting in a collection range of 1 sample per
every 8,461 to 22,000 chickens (i.e., a midpoint rate of 1 sample
per every 15,231 head). This is a greater sampling rate than those
larger volume establishments collecting a minimum of only one sample
every 22,000 head.
\171\ Under current regulations, these establishments collect 1
sample for every 22,000 chickens or 3000 other poultry species
slaughtered. This is an annualized slaughter volume of 1,140,000
head of chicken or 156,000 other species. To simplify proposed
slaughter volume criteria cut points, FSIS rounded 1,144,000 to the
1,100,000 identified in Table 11; an annual slaughter of 1,100,000
averages 21,153 head per week.

Table 11--Proposed Revisions to 9 CFR 381.65(g)(2) Minimum Sampling Frequency: Chicken
----------------------------------------------------------------------------------------------------------------
Predominant poultry species Establishment volume Annual slaughter head Minimum frequency of
slaughtered sizes volume paired collection
----------------------------------------------------------------------------------------------------------------
Chicken.............................. Very Low Volume........ 1-440,000.............. 13 Weekly Pairs per
Year.
Chicken.............................. Low Volume............. 440,001-1,100,000...... Weekly.
Chicken.............................. Medium and High Volume. >=1,100,000............ 1 per 22,000.
----------------------------------------------------------------------------------------------------------------

[[Page 64718]]

Table 12--Proposed Revisions to 9 CFR 381.65(g)(2) Minimum Sampling Frequency: Turkey, Geese, Guinea, Duck,
Squab
----------------------------------------------------------------------------------------------------------------
Predominant poultry species Establishment volume Annual slaughter head Minimum frequency of
slaughtered sizes volume paired collection
----------------------------------------------------------------------------------------------------------------
Turkey, geese, guineas, Ducks, Squab. Medium and High Volume. >=156,000.............. 1 per 3,000.
Turkey, Geese, Guinea, Ducks, Squab.. Low Volume............. 60,001-156,000......... Weekly.
Turkey, Geese, Guinea, Ducks, Squab.. Very Low Volume........ 1-60,000............... 13 Weekly Pairs per
Year.
----------------------------------------------------------------------------------------------------------------

5. Corrective Actions
FSIS is proposing to amend 9 CFR 381.65(g) to further clarify that
MMP monitoring results and documented corrective actions must be part
of the pre-shipment review process required under 9 CFR 417.5(c).
Current regulations at 9 CFR 381.65(g) require establishments to
incorporate microbial monitoring procedures into their HACCP systems.
Under 9 CFR 417, HACCP records must be maintained and continuously
evaluated as part of the establishment's validation, ongoing
verification, and reassessment process. Moreover, HACCP regulations at
9 CFR 417.3 and 417.5 specifically require establishments to identify,
in writing, the corrective actions that they will take when a HACCP
system procedure may have failed. This failure may be observed by
either the establishment or FSIS and may include failure to implement
or maintain a procedure, evidence that the outcome of a procedure was
ineffective, or when monitoring identifies the defined allowable limits
have not been met.
FSIS is proposing to revise the regulations to ensure that
establishments comply with these corrective action provisions as they
apply to the establishment's MMP. Specifically, FSIS is proposing to
amend 9 CFR 381.65(g) to require establishments to, at a minimum,
implement written corrective actions, including a root cause
assessment, when microbial monitoring results deviate from predefined
target change, quantitative consistency, or other criteria defined in
the MMP.
FSIS is also proposing that establishments' MMPs define the
corrective actions the establishment intends to take when its MMP
results do not align with other process control monitoring conclusions
or when its MMP results do not support the conclusion that its HACCP
system is controlling hazards as intended. FSIS recognizes a
qualitative analysis of MMP results is necessary, given that a process
can be stable and not capable of meeting quantitative specifications or
unstable yet produce product that meets quantitative
specifications.\172\ Thus, establishments will need to continually
consider their MMP results in conjunction with all other process
control monitoring efforts to qualitatively assess the overall ability
of their procedures to maintain process control and function as
intended. Establishments are to investigate and implement corrective
actions when their MMP monitoring results do not align with the other
process control monitoring conclusions. FSIS expects establishments to
consider their MMP results as part of their total HACCP system
validation and ongoing verification in the assessment of whether the
procedures as required by 9 CFR 381.65(g) are controlling the
biological hazard (enteric pathogens) as intended by the
establishment's HACCP system. A slaughter establishment's HACCP system
should clearly identify what process control procedures are monitored
by the MMP, any other process control monitoring results reflecting the
same procedures, a lot of products represented by this process control
monitoring, and any other procedures intended to control the same
hazard as the procedures required by 9 CFR 381.65(g). Establishment
documented corrective actions to observed MMP deviations must
demonstrate the establishment assessed the root cause of any deviation
in target change, quantitative consistency, and qualitative consistency
as described above.
---------------------------------------------------------------------------

\172\ NACMCF (2015). ``Regarding Microbiological Criteria as
Indicators of Process Control or Insanitary Conditions, available at
https://www.fsis.usda.gov/sites/default/files/media_file/2020-07/NACMCF-Report-Process-Control-061015.pdf.
---------------------------------------------------------------------------

6. Recordkeeping Requirements
FSIS is proposing to add a new paragraph (2) to 381.65(h) that
would require establishments to electronically submit a copy of their
microbial monitoring results to FSIS on a monthly basis. As part of the
publication of any final requirements, FSIS would provide a template to
each establishment for submitting monthly results. While FSIS
inspectors would continue to review process control sampling data in
establishments, the proposed change would allow FSIS headquarters
personnel to evaluate national trends to determine the efficacy of the
revised process control requirements in reducing final product
contamination and to inform FSIS' decision-making concerning agency
verification sampling.
As part of the Salmonella Framework effort, FSIS met with internal
FSIS, industry, and other government official stakeholders to explore
potential improvements to FSIS receipt of third-party data. FSIS,
academic, and industry stakeholders expressed concern around the lack
of options for nationally represented industry microbial data. FSIS has
determined it could update its information technology systems to
provide for both individual result and bulk result data uploads by
third parties. FSIS would publish guidance regarding the electronic
submission of data alongside any final rule resulting from this
proposal. FSIS is developing a web portal that will allow external
partners to securely upload their sampling information and submit the
data to FSIS electronically in a machine-readable format. The proposed
fields that would be uploaded into the portal are: a sample
identification number, the establishment number, date, time, slaughter
line number, location of sample collection (e.g., rehang, post-chill),
poultry species sampled, sample type (e.g., rinsate, sponge), analyte
(e.g., AC, EB), analyte units (e.g., cfu/mL), quantified analyte
result, and text analyte result (e.g., Upper LOD). FSIS is
seeking comments on the proposed data fields requested. Establishments
would have the option of entering the information directly into the
system or utilizing the FSIS provided spreadsheet file discussed above
as a template to bulk upload the information. FSIS anticipates that
most establishments would use the FSIS provided template as the HACCP
MMP monitoring record to avoid duplication of monitoring results.
FSIS is also seeking comment on specific data use opportunities
which could be pursued that would support FSIS investing additional
resources into the technology systems necessary to

[[Page 64719]]

blind the proprietary MMP result record copies for research, industry,
academic, or other pursuits.

IV. Component One: Pre-Harvest Measures

A. Scientific Support and Public Comments

Under Component One of the October 2022 draft framework, FSIS
indicated that it was considering whether it should require poultry
slaughter establishments to characterize Salmonella as a hazard
reasonably likely to occur at receiving and require that incoming
flocks be tested for Salmonella before entering an establishment. This
component is grounded in the strong scientific support for use of pre-
harvest interventions and management practices, in particular that
removing flocks of highly Salmonella-contaminated birds from the
slaughter process would result in less human exposure to Salmonella.
The results of the 2023 risk assessments underscore the potential
public health benefit of requiring pre-harvest interventions and
management practices to reduce Salmonella contamination on poultry.
Within the risk assessments, risk management options for controlling
Salmonella at the receiving step focused on chicken and turkey
slaughter establishments and sample results at the rehang location as a
proxy for sampling live birds at or before the receiving step.\173\ The
2023 risk assessments estimated the impact of eliminating certain
serotypes. Two options were modeled: in the first, rehang results were
considered as a verification of pre-harvest Salmonella control
strategies. More effective strategies mean lower rates of certain
serotypes at rehang. For the second option, rehang testing results
would be used to take actions, such as diverting positive flocks with
higher virulence serotypes to a safe end point (e.g., cook product from
those flocks).
---------------------------------------------------------------------------

\173\ For chicken FSIS used rehang sample data collected during
the FSIS young chicken carcass exploratory sampling program (April
to November 2022). For turkey, FSIS modeled Salmonella at receiving
using rehang sampling data from the 2008-2009 FSIS Young Turkey
Carcass baseline study due to the absence of other data for the
turkey industry.
---------------------------------------------------------------------------

If rehang testing is considered as a verification of pre-harvest
strategies, between 27,000 and 55,000 annual salmonellosis cases could
be avoided if flocks that have higher virulence serotypes were not
being processed for food. Alternatively, if rehang testing is used to
identify and divert contaminated carcasses, about 36,000 cases could be
avoided. However, to achieve these outcomes, flocks with a higher
virulence serotype would be diverted to a safe end point (e.g., for
cooking at an official establishment), resulting in the diversion of
46,000 flocks. Further, the rehang step takes place during processing.
Requiring processors to react to testing--with results not available to
at least two days--is not feasible. co Currently, FSIS analyzes about
10,000 young chicken carcasses from rinsates collected at the post-
chill location annually. By comparison, there are approximately 9.384
billion carcasses that are processed each year at approximately two
hundred slaughter establishments. Therefore, currently, FSIS analyzes
about one out of every million young chicken carcasses processed
annually.
Testing results at or before the receiving step may have a
substantial public health impact. However, the requirements associated
with the first option (verification of pre-harvest Salmonella control
strategies) would require substantial industry resources, and there is
no guarantee that the poultry industry would implement such Salmonella
control strategies, since the first option would not penalize
establishments for having highly virulent serotypes at the rehang step.
The second option (divert flocks that test positive to a safe endpoint)
would require the same resources as the first option. However, FSIS is
not proposing such a diversion requirement at this time.
FSIS does not have a routine sampling program at the rehang
location, but the Agency evaluated such a program as part of the 2022
young chicken exploratory sampling program discussed above. Among 180
establishments sampled twelve or more times at the rehang location,
Salmonella positive rates for young chicken carcasses ranged from 0 to
100 percent, and the 95 percent confidence interval ranged from 54.9 to
69.0 percent. Variability at the rehang location was also observed with
AC and EB. Among 180 establishments with at least twelve analyzed
sample pairs, the ACs average at the rehang location was 4.40 log cfu
per mL (95 percent confidence 4.34 to 4.46 log cfu per mL) and EB
average was 3.00 log cfu per mL (95 percent confidence 2.94 to 3.06 log
CFU per mL).
Two recent NACMCF reports, one published in March 2019 and the
March 2023 NACMF Final Report, support the important role pre-harvest
measures play in controlling Salmonella in poultry.
2019 NACMCF Report. At a March 2017 NACMCF meeting, FSIS asked the
committee to address the issue of how to reduce the prevalence of
Salmonella on poultry throughout the farm-to-table continuum.\174\ In
March 2019, the committee's final report addressing the Agency's
questions was published in the Journal of Food Protection.\175\
Questions two, three, and six related to pre-harvest measures to
control Salmonella in poultry. Question two asked where Salmonella
resides inside and on the surface of poultry and how those populations
of bacteria contribute to food contamination. The committee responded
that most carcass contamination is believed to result from leakage of
ingesta during crop removal and from feces during evisceration, as well
as aerosolization during picking. In addition, Salmonella may be
present in feather follicles and on the surface of broilers when they
enter the slaughter establishment. Several preslaughter strategies to
reduce the burden of Salmonella in flocks entering slaughter
establishments have been shown to be effective, and data demonstrating
a correlation between flock status of Salmonella and pre- and post-
chill contamination have been reported. Control measures for Salmonella
in poultry can be classified as those that target (i) exposure and
colonization within an individual animal, (ii) transmission between
parent flocks and progeny, and (iii) transmission between birds within
a flock. The committee also noted that Salmonella vaccination is one
breeder-level pre-harvest intervention that contributes to an overall
reduction and/or elimination of specific Salmonella serotypes. The
committee stated that the most effective vaccination strategy is to
focus on vaccination of breeder flocks and reduce vertical transmission
of Salmonella.
---------------------------------------------------------------------------

\174\ 2015-2017 NACMCF Charge, Salmonella Control Strategies in
Poultry, available at: https://www.fsis.usda.gov/news-events/publications/2015-2017-national-advisory-committee-microbiological-criteria-foods.
\175\ Response to Questions Posed by the Food Safety and
Inspection Service Regarding Salmonella Control Strategies in
Poultry (March 26, 2019), Journal of Food Safety, available at:
https://www.fsis.usda.gov/news-events/publications/2015-2017-national-advisory-committee-microbiological-criteria-foods.
---------------------------------------------------------------------------

Question three asked whether removing flocks of highly Salmonella-
contaminated birds entering the slaughter establishment can reduce
foodborne illnesses in humans. The committee responded that it is
logical to expect that removing flocks of highly Salmonella-
contaminated birds from the slaughter process would result in less
human exposure to that source of Salmonella, potentially resulting in
reduced foodborne illness in humans.

[[Page 64720]]

However, there was no consensus within the committee regarding the
predictive ability of farm sampling and subsequent Salmonella
contamination on neck skin at the end of processing. Given uncertainty
about the impact of removing flocks of highly Salmonella-contaminated
birds from slaughter, the committee recommended that process controls
be validated to address a worst-case scenario for contamination of
incoming birds and be continually operating at that level to address
the potential risk from highly contaminated birds. The committee
concluded that rather than establishing lot- or flock-specific
thresholds, Salmonella management programs should be based on
historical trend analyses of specific farms and transportation
supplying birds to the slaughter process. Sampling birds immediately
before entering the slaughter process would be ideal, but detection
technology did not currently exist to provide the rapid detection
needed for this scenario. Historical data might be used to build
statistical models to predict the potential for elevated levels of
Salmonella from a particular farm. In addition, monitoring of external
factors, such as weather or seasonality, may help indicate the
possibility of a higher-than-normal contamination level. Historical
knowledge of process controls and facility capability can be used by a
processor to determine whether process controls should be reassessed
and validated to address predicted risks.
Question six asked the committee to identify the top three focus
points, control measures, or best practices that would be compatible
with industry-wide practices and could be addressed or implemented to
achieve the highest rate of reductions of Salmonella product
contamination and foodborne illness. The committee's response included
the statement that prevention or elimination of Salmonella
colonization, should be effective for reducing Salmonella in final
product and contributing to public health improvements.
2023 NACMCF Report. In the 2023 NACMCF report, the committee
addressed issues related to pre-harvest measures to control Salmonella
in poultry.\176\ For question two of the NACMCF charges, FSIS asked the
committee what types of microbiological criteria could be established
to encourage control of Salmonella at pre-harvest, and what industry
data would provide evidence of control. As part of its response, the
committee noted that vaccination programs have been incorporated on
U.S. farms. The committee described such vaccination programs as an
effective management practice for controlling Salmonella at pre-harvest
and noted that vaccines are likely the only serotype-specific
intervention strategies.
---------------------------------------------------------------------------

\176\ NACMCF final report ``Response to Questions Posed by the
Food Safety and Inspection Service: Enhancing Salmonella Control in
Poultry Products'' (March 13, 2023), available at: https://www.fsis.usda.gov/policy/advisory-committees/national-advisory-committee-microbiological-criteria-foods-nacmcf/2021.
---------------------------------------------------------------------------

Together, the 2019 and 2023 NACMCF report responses related to pre-
harvest measures support the use of these measures to control
Salmonella in poultry. In the 2019 report, the committee concluded that
preslaughter strategies to reduce the burden of Salmonella in flocks
entering slaughter establishments are effective, and that data show a
correlation between flock status of Salmonella and pre- and post-chill
contamination. The 2019 report also indicated that it is probable that
removing flocks of highly Salmonella-contaminated birds from the
slaughter process would result in less human exposure to that source of
Salmonella, potentially resulting in reduced foodborne illness in
humans. In the 2023 report, the committee recommended that the Agency
target for consideration conditions in houses, transport crates, and
holding areas that harbor and transmit Salmonella by universal
implementation of known and validated mitigation strategies. Of note,
both final reports indicated uncertainty regarding whether current
testing technology and data are available to design and broadly
implement effective threshold requirements for segregating Salmonella-
contaminated flocks at receiving.
As discussed above, FSIS received comments on Component One of the
October 2022 draft Salmonella Framework that raised concerns related to
costs, testing technology, and implementation challenges. Several
comments from small poultry processors and producers and trade
associations representing the meat and poultry industries that
expressed concerns that the measures under consideration in Component
One would impose an overwhelming burden on small producers and
processors.
In light of these comments, FSIS has decided at this time not to
establish a regulatory requirement that establishments characterize
Salmonella as a hazard reasonably likely to occur at receiving or that
incoming flocks be tested for Salmonella before entering an
establishment. FSIS will actively seek evidence and best practices from
the poultry industry. The Agency will revisit its strategy for using
testing (including quantitation and deep serotyping) to minimize the
risk of cross-contamination at processing when logistical challenges
have been addressed and testing becomes more timely and affordable.
FSIS has decided, instead, for the time being, to focus on non-
regulatory approaches to controlling Salmonella at preharvest and
reducing the Salmonella load on birds at receiving. FSIS not proposing
to enforce measures under Component One at this time. If the Agency
decides to make any of the approaches discussed below mandatory, it
will do so through future rulemaking.

B. Possible Approaches To Control Salmonella at Pre-Harvest

1. National Poultry Improvement Program
FSIS will explore whether existing or new certification programs
under the National Poultry Improvement Program (``NPIP'' or the
``Plan'') could serve to verify and document producers' actions (such
as use of Salmonella vaccines) to control Salmonella, including
serotypes of public health significance.
Administered by APHIS, NPIP is a cooperative industry, state, and
federal program initially established to improve poultry and poultry
products and prevent and control poultry diseases.\177\ The Plan
identifies States, flocks, hatcheries, dealers, and slaughter plants
that meet certain disease control standards specified in the Plan's
various programs. NPIP regulations in 9 CFR parts 145 and 146 contain
requirements that must be observed by participating flocks, including
testing and biosecurity measures. These measures are updated over time
as the science and technology evolve and improve. Affiliated flock-
owners participate in the Plan through an agreement with a
participating hatchery. Participating hatcheries must be maintained in
sanitary condition as outlined in the NPIP Program Standards and the
U.S. Code of Federal Regulations and are subject to third party audit
by an official state agency at least once every two years or a
sufficient frequency to ensure compliance. NPIP programs are available
for multiplier and primary breeding flocks for meat-type chicken and
products (9 CFR part 145 subparts C and H), and turkey breeding flocks
and products (9 CFR part 145 subpart D). These programs include
biosecurity measures and may include testing for Salmonella or
Salmonella serotype Enteritidis. The

[[Page 64721]]

Plan's ``U.S. Salmonella Monitored Program'' is intended for primary
breeders of meat type chickens to reduce the incidence of Salmonella
organisms in hatching eggs and chicks through an effective and
practical sanitation program at the breeder farm and in the hatchery.
The Plan's ``U.S. S. Enteritidis Clean Program'' is intended for
primary or multiplier breeders of meat-type chickens wishing to assure
their customers that the chicks produced are certified free of
Salmonella Enteritidis.
---------------------------------------------------------------------------

\177\ USDA Animal and Plant Health and Inspection Service
(APHIS) National Poultry Improvement Plan information available at:
https://www.poultryimprovement.org/default.cfm.
---------------------------------------------------------------------------

2. Vaccination
FSIS will more actively encourage the development, licensure, and
use of poultry vaccines against Salmonella serotypes of public health
concern, particularly live attenuated vaccines, and will provide
sampling data and technical support, as appropriate, to industry and
regulatory bodies to advance these goals.
Salmonella vaccination is one tool in a multifaceted approach to
overall Salmonella reduction and/or elimination of specific Salmonella
serotypes. Vaccines reduce the susceptibility of individual birds to
Salmonella infection, transmission among breeding flocks, cross-
contamination during meat bird production, contamination of poultry
house environments, and transmission to subsequent flocks. Live
attenuated vaccines are derived from a specific strain of a target
organism (i.e., Salmonella Typhimurium), subunit vaccines containing
protein or nucleic acid from the target organism, and autogenous
inactivated vaccines against a cocktail of strains found in a local
area. Vaccines may provide cross protection across serotypes. For
example, the availability of a commercial live attenuated vaccine
created from Salmonella Typhimurium corresponded to a profound decline
in the incidence of both Typhimurium and a related serotype Heidelberg
illnesses.\178\ Attenuated strains can be designed to expose common
antigens, therefore inducing cross-protective immunity against diverse
Salmonella serotypes.\179\ Although vaccines can be protective and
limit horizontal transmission of infection within broiler flocks, they
must be given multiple times to all birds in each flock and, therefore,
present logistical and cost challenges that must be overcome.
---------------------------------------------------------------------------

\178\ NACMCF Report: ``Response to Questions Posed by the Food
Safety and Inspection Service: Enhancing Salmonella Control in
Poultry Products'' (Mar 2023). Available at: https://www.fsis.usda.gov/policy/advisory-committees/national-advisory-committee-microbiological-criteria-foods-nacmcf/2021.
\179\ Aehle, S. and R. Curtiss (2017). Chapter 14--Current and
Future Perspectives on Development of Salmonella Vaccine
Technologies. Producing Safe Eggs. S. C. Ricke and R. K. Gast. San
Diego, Academic Press: 281-299; Hassan, J. O. and R. Curtiss Iii
(1997). ``Efficacy of a live avirulent Salmonella typhimurium
vaccine in preventing colonization and invasion of laying hens by
Salmonella typhimurium and Salmonella enteritidis.'' Avian Dis
41(4): 783-791.
---------------------------------------------------------------------------

FSIS will continue to collect data on the impact of vaccine use on
FSIS verification testing through pilot projects. As noted above, since
March 2023, FSIS has granted pilot projects to 9 establishments to
examine the merits and logistics of excluding Salmonella poultry
vaccine strains from the FSIS Salmonella performance categorization
calculation. Modified live Salmonella vaccines are used to reduce
Salmonella colonization in poultry. These vaccine strains are not
foodborne pathogens, making them a valuable pre-harvest tool for
controlling wild-type Salmonella. FSIS is able to identify vaccine
strains isolated from raw poultry products through the use of whole
genome sequencing.
FSIS examined Salmonella detection and serotype data from flocks
vaccinated with a modified live Salmonella vaccine at pre- and post-
intervention points in the participating slaughter establishments.
These data show that vaccine strains can occasionally be found in raw
poultry products even when the vaccine is used as directed on the
label. After reviewing the data, FSIS concluded that its policy to
count such strains as a positive result in performance categorization
may discourage use of vaccination as a tool to control Salmonella.
Therefore, on March 1, 2024, FSIS announced that beginning April 1,
2024, it intends to exclude current commercial vaccine subtypes
confirmed in FSIS raw poultry samples from the calculation used to
categorize establishments under the raw poultry Salmonella performance
standards.\180\ This action is intended to remove barriers to the use
of vaccination as an important pre-harvest intervention to control
Salmonella in poultry. A summary report of the data from these pilots
is posted on the Pilot Projects: Salmonella Control Strategies page of
the FSIS website at: https://www.fsis.usda.gov/inspection/inspection-programs/inspection-poultry-products/reducing-salmonella-poultry/pilot.
---------------------------------------------------------------------------

\180\ FSIS Constituent Update--March 1, 2024: FSIS Intends to
Exclude Vaccine Strains from the FSIS Salmonella Performance
Categorization at: https://www.fsis.usda.gov/news-events/news-press-releases/constituent-update-march-1-2024.
---------------------------------------------------------------------------

3. Supply Chain Control Programs
Establishments operating under HACCP regulations (9 CFR part 417)
must perform a hazard analysis to identify food safety hazards that can
occur before, during, and after entry into the establishment and to
identify the preventive measures the establishment can apply to control
those hazards. Establishments that identify hazards that occur before
entry face the challenge of providing assurance that preventive
measures are effectively applied. FSIS-inspected establishments
operating under HACCP must document, validate, and verify the
effectiveness of their hazard control(s). While not required to do so,
establishments slaughtering poultry that have identified Salmonella as
a hazard during the breeder and multiplier and production stages are
encouraged by FSIS to use supply chain programs \181\ to verify the
effectiveness of their supplier's interventions, and the Agency will
ramp up its efforts to assist any establishment that wants to implement
a supply chain program.
---------------------------------------------------------------------------

\181\ One example of a supply chain program is a process
verified program (PVP) administered by USDA's Agricultural Marketing
Service (AMS). A PVP may include one or more agricultural processes
or portions of processes where self-described process points are
supported by a documented management system, and independently
verified by a qualified AMS auditor. One PVP available to the
poultry industry is the Quality System Assessment (QSA). The QSA
provides companies that supply agricultural products and services
the opportunity to assure customers of their ability to provide
consistent quality products or services. It is limited to programs
or portions of programs where specified product requirements are
supported by a documented quality management system. USDA AMS
Process Verified Program information available at: https://www.ams.usda.gov/services/auditing/process-verified-programs.
---------------------------------------------------------------------------

4. Updated Pre-Harvest Guidance
FSIS intends to revise its existing guideline on Controlling
Salmonella in Raw Poultry \182\ to provide updated guidance on pre-
harvest interventions and management practices for preventing and
reducing Salmonella colonization in live birds. FSIS remains committed
to identifying and developing strategies for addressing Salmonella
contamination in the pre-harvest environment. Additionally, the Agency
is working with the USDA's Agricultural Research Service (ARS) on a
literature review of Salmonella presence in poultry at pre-harvest.
---------------------------------------------------------------------------

\182\ FSIS Guideline for Controlling Salmonella in Raw Poultry
(June 2021), available at: https://www.fsis.usda.gov/guidelines/2021-0005.
---------------------------------------------------------------------------

V. State Programs and Foreign Government Programs

States that have their own poultry inspection programs for poultry

[[Page 64722]]

products produced and transported solely within the State are required
to have mandatory ante-mortem and post-mortem inspection, reinspection,
and sanitation requirements that are at least equal to those in the
PPIA (21 U.S.C. 454(a)(1)). Therefore, if FSIS finalizes this proposed
rule and determination, these States would need to develop sampling
procedures and testing methods to detect Salmonella at or above 10 cfu/
mL(g) in an analytical portion and Salmonella serotypes of public
health significance identified for raw chicken carcasses, chicken
parts, comminuted chicken, and comminuted turkey products that are at
least as sensitive as FSIS' procedures and testing methods for
Salmonella. Additionally, these States would need to implement
requirements for poultry slaughter establishments to develop,
implement, and maintain written procedures to prevent contamination by
enteric pathogens throughout the entire slaughter and dressing
operation that are at least equal to FSIS' proposed revisions to the
poultry regulations. FSIS will coordinate closely with States that
maintain federally supported poultry inspection programs to ensure that
this Salmonella Framework for raw poultry products is implemented in
all intrastate establishments.
Foreign countries that are eligible to export poultry products to
the United States must apply inspection, sanitary, and other standards
that are equivalent to those that FSIS applies to those products (21
U.S.C. 466). Thus, in evaluating a foreign country's poultry inspection
system to determine the country's eligibility to export products to the
United States, FSIS will consider whether the sampling procedures and
testing methods that the country implements for detection of Salmonella
at or above 10 cfu/mL(g) in an analytical portion and Salmonella
serotypes of public health significance identified for raw chicken
carcasses, chicken parts, comminuted chicken, and comminuted turkey
products are equivalent to FSIS' sampling procedures and testing
methods. Additionally, FSIS will also evaluate whether the country's
requirements for slaughter establishments to develop, implement, and
maintain written procedures to prevent contamination by enteric
pathogens throughout the entire slaughter and dressing operation are
equivalent to FSIS' proposed revisions to the poultry regulations. FSIS
will continue to use the existing equivalence process to ensure that
foreign countries implement requirements, sampling procedures and
testing methods equivalent to FSIS' proposed revisions to the poultry
regulations and the sampling procedures and testing methods for
Salmonella in raw chicken carcasses, chicken parts, comminuted chicken,
and comminuted turkey products. FSIS intends to provide countries that
export poultry products to the United States 3 years after publication
of the final rule to submit adequate documentation to support that
their poultry inspection system is equivalent to FSIS' inspection
system. Thus, exporting countries would have a 3-year transition period
in which they could continue to export poultry products to the United
States while they implement measures to ensure that their poultry
inspection system is equivalent to the U.S. system. FSIS would likely
begin testing imported raw chicken carcasses, chicken parts, comminuted
chicken, and comminuted turkey products to verify products are not
adulterated one year after the final publication. FSIS will provide
additional details on these issues in any final rule and determination
resulting from this proposal.

VI. Executive Orders 12866, as Amended by 14094, and 13563

Executive Orders (E.O.) 12866, as amended by 14094, and 13563
direct agencies to assess all costs and benefits of available
regulatory alternatives and, if regulation is necessary, to select
regulatory approaches that maximize net benefits (including potential
economic, environmental, public health and safety effects, distributive
impacts, and equity). E.O. 13563 emphasizes the importance of
quantifying both costs and benefits, of reducing costs, of harmonizing
rules, and of promoting flexibility. This proposed rule and proposed
determination have been designated a ``significant'' regulatory action
by the Office of Information and Regulatory Affairs under section 3(f)
of E.O. 12866. Accordingly, the proposed rule and proposed
determination have been reviewed by the Office of Management and Budget
under E.O. 12866.
Regulatory Impact Analysis
FSIS is proposing to clarify certain process control requirements
for poultry slaughter establishments and establish final product
standards for chicken carcasses, chicken parts, comminuted chicken, and
comminuted turkey. This proposal is aimed at reducing Salmonella
illnesses in the U.S. population.
FSIS is proposing to clarify current requirements for monitoring
compliance with 9 CFR 381.65(g) for poultry slaughter establishments
and to require poultry slaughter establishments to submit process
control monitoring data electronically to FSIS. These establishments
are currently required to monitor their processes to ensure they comply
with FSIS regulations. FSIS is clarifying that MMPs need to be
statistically based and is requiring that establishments collect
samples specifically at rehang, or an alternative location if they
submit and maintain supporting documentation. The proposed
clarifications are estimated to have minimal economic impact on most
establishments, while the potential effects on VLV and VS
establishments operating under Traditional Inspection, as described in
this analysis, would be potentially mitigated by the use of laboratory
services provided by FSIS.
FSIS is also proposing to implement new standards for chicken
carcasses, chicken parts, comminuted chicken, and comminuted turkey as
final products that would enter commerce. Product subject to these
standards, as described in the foregoing, would be subject to FSIS
routine sampling and verification testing for Salmonella.
Establishments subject to FSIS verification sampling would be required
to maintain control of sampled product pending test results. Product
lots that do not meet the standards would be considered adulterated and
would be diverted from commerce. Establishments could divert
adulterated product to be fully cooked at a federal establishment and
then sent into commerce.
Finally, FSIS is encouraging establishments to consider including
pre-harvest measures in their HACCP systems to address the hazard of
Salmonella contamination prior to slaughter. The Agency is not
requiring that establishments adopt pre-harvest measures; thus, any
potential costs or benefits associated with those measures are
especially challenging to analyze, and we request comment on relevant
data and analytic methods of analysis.
Need for the Rule
This regulatory action is necessary because while the results of
FSIS' Salmonella verification sampling show that the current
prevalence-based performance standards approach has been effective in
reducing the proportion of poultry products contaminated with
Salmonella, these measures have yet to have an observable impact on
overall human Salmonella illness rates (see the Salmonella Performance
Standards and Illnesses section for more details). An estimated 23
percent of Salmonella illnesses are

[[Page 64723]]

attributed to poultry--17 percent to chicken products and 6 percent to
turkey products--making poultry one of the leading sources of foodborne
Salmonella illnesses in the United States.\183\ Thus, a reduction in
Salmonella illnesses associated with poultry consumption would be
expected to have an impact on overall Salmonella illnesses. A 2015
analysis found that poultry consumption was more likely than any other
animal protein to lead to Salmonella illnesses.\184\ Additionally, a
2021 study observed that Salmonella outbreaks related to consumption of
single ingredient poultry products were disproportionately higher than
the estimated level of consumption of single ingredient poultry
products.\185\
---------------------------------------------------------------------------

\183\ The Interagency Food Safety Analytics Collaboration
(IFSAC), ``Foodborne illness source attribution estimates for 2019
for Salmonella, Escherichia coli O157, Listeria monocytogenes, and
Campylobacter using multi-year outbreak surveillance data, United
States,'' October 2021, https://www.cdc.gov/ifsac/php/annual-reports/index.html. Annually, IFSAC releases a report that estimates
foodborne illness source attribution for major commodity groups,
including Salmonella in poultry products. At the time this proposal
was developed, the 2019 IFSAC attribution estimates were the most
recent data available. IFSAC released a new annual report in
November 2023, which includes attribution estimates for 2020. In the
2023 report, IFSAC estimated that 18.6 percent of Salmonella
illnesses are attributed to chicken products and 5.5 percent to
turkey products, for a total 24.1 percent attributed to poultry
products. FSIS intends to incorporate the 2023 report attribution
estimates if this proposal is finalized. IFSAC, ``Foodborne illness
source attribution estimates for Salmonella, Escherichia coli O157,
and Listeria monocytogenes--United States 2021,'' November 2023,
https://www.cdc.gov/ifsac/php/annual-reports/index.html.
\184\ The analysis estimated that the risk of getting sick from
Salmonella from one serving of poultry products was 94, 97, and 87
percent larger than that for a serving of pork, beef, and lamb
products, respectively. Hsi, D.J., Ebel, E.D., Williams, M.S.,
Golden, N.J. and Schlosser, W.D., 2015. Comparing foodborne illness
risks among meat commodities in the United States, Food Control, 54,
pp.353-359. https://doi.org/10.1016/j.foodcont.2015.02.018.
\185\ The analysis observed that while chicken and turkey
consumption represent roughly 0.6 and 0.2 percent of the U.S. daily
diet, the share of outbreaks linked to these products is
significantly higher: 2.1 and 1.5 percent, respectively. These
estimates are for chicken and turkey consumed as single-ingredient
foods. Richardson, L.C., Cole D., Hoekstra, R.M., Rajasingham, A.,
Johnson, S.D., Bruce, B.B., 2021. Foods Implicated in U.S. Outbreaks
Differ from the Types Most Commonly Consumed. Journal of Food
Protection, 84(5), pp.869-875. https://doi.org/10.4315/JFP-20-293.
---------------------------------------------------------------------------

As part of this proposal for Salmonella in poultry, FSIS is
proposing to clarify existing regulatory requirements related to
process control monitoring and recordkeeping in 9 CFR 381.65(g) and (h)
to better ensure that poultry slaughter establishments are effectively
controlling Salmonella throughout their slaughter and dressing
operations. FSIS is also proposing to declare that raw chicken
carcasses, parts, and comminuted chicken and turkey that contain
Salmonella at or above 10 cfu/mL(g) and a serotype of public health
significance are adulterated because the 2023 risk assessments found
that servings contaminated with these Salmonella levels and serotypes
are much more likely to cause illness than the majority of chicken
carcasses, chicken parts, comminuted chicken, and comminuted turkey
servings (see the Risk per Serving, Salmonella Levels, and Proposed
Determination section for more details). The 2023 risk assessments
estimate that diverting products that contain these Salmonella levels
and serotypes from commerce would prevent annual foodborne illnesses
from Salmonella linked to poultry.\186\ Moreover, the FSIS risk profile
indicates that for certain Salmonella serotypes often linked to poultry
products a small amount of Salmonella bacteria can cause illness.\187\
It also noted that these serotypes caused hospitalization more
frequently and led to invasive disease and death as well as
debilitating human health outcomes.
---------------------------------------------------------------------------

\186\ USDA, FSIS, ``Quantitative Microbiological Risk Assessment
for Salmonella in Raw Chicken and Raw Chicken Products,'' January
2023; USDA, FSIS, ``Quantitative Microbiological Risk Assessment for
Salmonella in Raw Turkey and Raw Turkey Products,'' January 2023 at:
https://www.regulations.gov/docket/FSIS-2023-0028.
\187\ USDA, FSIS, ``Risk Profile for Pathogenic Salmonella
Subtypes in Poultry,'' February 28, 2023 at: https://www.regulations.gov/docket/FSIS-2023-0028.
---------------------------------------------------------------------------

FSIS is taking this regulatory action to protect public health and
reduce the number of Salmonella illnesses linked to poultry products.
If this proposal is finalized, it would protect consumers from
consuming products that have a higher probability of illness and would
incentivize producers implement food safety measures that would
minimize the risk of Salmonella illnesses.
Baseline for Evaluation of Costs and Benefits
Poultry consumption has grown 13 percent over the past 10 years,
with broiler meat accounting for 83 percent of the total consumption,
while turkey accounts for about 16 percent. Poultry--mainly chicken--is
the main source of animal protein across demographic groups and is
consumed both at home and away from home.\188\ Poultry products are
available in multiple formulations, ranging from raw whole birds and
parts to fully cooked, ready-to-eat products. In the United States,
chicken breasts, legs, and wings are the most consumed chicken
products.\189\ Turkey consumption, in contrast, is mainly as whole
turkey, deli meat, ground turkey, or turkey bacon. Ground turkey
consumption has increased substantially in the last decade, mainly as
consumers opt for this product as a substitute for ground beef.\190\
---------------------------------------------------------------------------

\188\ There is variability in poultry consumption among
demographic groups. For example, poultry consumption is higher among
the non-Hispanic Black population, followed by Hispanics and non-
Hispanic Asians. Poultry also represents a substantial source of
protein for children, with chicken being the main source of animal
protein among them. USDA, ERS, ``Racial and Ethnic Diversification
Will Likely Shape U.S. Food Demand and Diet Quality,'' by Diansheng
Dong and Hayden Stewart, April 4, 2022, https://www.ers.usda.gov/amber-waves/2022/april/racial-and-ethnic-diversification-will-likely-shape-u-s-food-demand-and-diet-quality/.
\189\ USDA, Economic Research Service (ERS), ``Chicken leads
U.S. per person availability of meat over last decade,'' March 1,
2023, https://www.ers.usda.gov/data-products/chart-gallery/gallery/chart-detail/?chartId=105929.
\190\ National Turkey Federation, ``Turkey by the Numbers,''
accessed June 20, 2021, https://www.eatturkey.org/turkeystats/;
Agricultural Marketing Resource Center, ``Turkey Profile,'' January
2022, https://www.agmrc.org/commodities-products/livestock-dairy-poultry/poultry/turkey-profile.
---------------------------------------------------------------------------

On average, U.S. poultry establishments slaughtered 9.5 billion
birds annually between 2017 and 2021, which is approximately 49.4
billion pounds of poultry. Broiler and turkey meat accounted for 87 and
12 percent of this production, respectively.\191\ The U.S. poultry
supply is mainly comprised of domestically grown and processed poultry
as imports represent a very small fraction of the total supply.\192\
Federally inspected establishments produce the vast majority of U.S.
commercial poultry supply.\193\ Most federally inspected establishments
that produce a high volume of product solely produce chicken or turkey
products. Some establishments also slaughter other classes of poultry,
such as duck and geese. While there are establishments that slaughter
multiple species, they tend to produce a low volume of product.
---------------------------------------------------------------------------

\191\ Other types of poultry (e.g., duck) account for the
remaining 1 percent.
\192\ Imports of poultry products into the United States
represented less than 0.5 percent of total U.S. poultry consumption
in 2021. The United States is a net exporter of poultry to the world
and is the second largest exporter globally, with exports
representing about 16 percent of the total domestic production in
2021. USDA, Foreign Agricultural Service, ``Production, Supply and
Distribution database,'' accessed May 11, 2023.
\193\ USDA, National Agricultural Statistics Service, Surveys:
Poultry Slaughter, October 19, 2020, https://www.nass.usda.gov/Surveys/Guide_to_NASS_Surveys/Poultry_Slaughter/index.php.

---------------------------------------------------------------------------

[[Page 64724]]

Establishments Subject to the Current Salmonella Performance Standards
and Proposed Final Product Standards
FSIS used 2021 Public Health Information System (PHIS) data to
identify establishments under the current Salmonella performance
standards that produce chicken carcasses, chicken parts, comminuted
chicken, and comminuted turkey, as well as their production
volumes.\194\
---------------------------------------------------------------------------

\194\ USDA, FSIS, Public Health Information System database,
accessed January 2, 2023 and April 5, 2023. Certain establishments
are currently excluded from Salmonella verification testing. 81 FR
7288. FSIS adjusted the estimates for chicken parts, comminuted
chicken, and comminuted turkey to match slaughter totals in the
analysis period.
---------------------------------------------------------------------------

Chicken Carcasses
In 2021, there were a total of 188 establishments under FSIS
verification sampling for chicken carcasses that slaughtered over 8.3
billion chickens. FSIS classified these establishments into one of four
volume categories (Table 13). Of these, 142 establishments were high-
volume establishments, 9 were medium-volume, 4 were low-volume, and 33
were VLV chicken slaughter establishments. The 142 high-volume
establishments accounted for over 99.5 percent of the total head count
slaughtered in 2021.

Table 13--Chicken Carcasses: Establishments Under FSIS Performance Standards
[2021]
----------------------------------------------------------------------------------------------------------------
Number of Annual production Share of
Establishment volume category Definition (birds) establishments (million birds) production (%)
----------------------------------------------------------------------------------------------------------------
High............................. 10 million or more.. 142 8,270 99.52
Medium........................... More than 1.1 9 33 0.40
million and less
than 10 million.
Low.............................. More than 440,001 4 2 0.03
and less than 1.1
million.
Very Low \1\..................... No more than 440,000 33 4 0.05
--------------------------------------------------------
Total........................ .................... 188 8,309 .................
----------------------------------------------------------------------------------------------------------------
\1\ Very low-volume establishments are defined in 9 CFR 381.65g(1)(i).
Note: Numbers in table may not sum to totals due to rounding.

Chicken Parts
In 2021, there were 490 establishments under FSIS verification
sampling that produced chicken legs, breasts, wings, halves, and/or
quarters (Table 14). Of these, 484 establishments were subject to FSIS
performance standards sampling for chicken legs, breasts, and wings.
The proposal would apply to establishments that produce chicken legs,
breasts, wings, thighs, halves, and quarters. In 2021, most of the
establishments producing chicken halves and quarters also produced
legs, breasts, and wings. FSIS sampling at these establishments would
be adjusted to incorporate chicken halves and quarters samples, while
maintaining the current sampling frequency. In 2021, six establishments
produced chicken halves and quarters, but did not produce legs,
breasts, or wings. These six establishments are currently sampled as
part of FSIS' exploratory sampling program for chicken halves and
quarters.
FSIS estimates that these establishments produced over 31.2 billion
pounds of chicken parts in 2021. FSIS classified these establishments
according to the volume categories the Agency used in the 2016 cost-
benefit analysis in support of FSIS ``Chicken Parts and Not Ready-To-
Eat Comminuted Poultry Performance Standards.'' \195\ In 2021, 154 of
these establishments were high-volume, 209 were medium-volume, and 127
were low-volume establishments (Table 14). The 154 high-volume
establishments accounted for roughly 90 percent of the production
volume of chicken parts in 2021.
---------------------------------------------------------------------------

\195\ USDA, FSIS, ``Chicken Parts and Not Ready-To-Eat
Comminuted Poultry Performance Standards,'' Final Cost-Benefit
Analysis, February 11, 2016, https://www.fsis.usda.gov/sites/default/files/media_file/documents/FRN-related-CBA-Salmonella-Campy-2014-0023-022016.pdf.

Table 14--Chicken Parts: Establishments Under FSIS Performance Standards (2021)
----------------------------------------------------------------------------------------------------------------
Definition (annual Number of Annual production Share of
Establishment volume category production pounds) establishments (million pounds) production (%)
----------------------------------------------------------------------------------------------------------------

High............................. 70 million or more.. 154 28,113 90.1
Medium........................... More than 1 million 209 3,055 9.8
and less than 70
million.
Low.............................. 1 million or less... 127 40 0.1
--------------------------------------------------------
Total........................ .................... 490 31,208 .................
----------------------------------------------------------------------------------------------------------------
Note: Numbers in table may not sum to totals due to rounding.

Comminuted Chicken
In 2021, there were 74 establishments under FSIS verification
sampling for comminuted chicken (Table 15). FSIS estimates that these
establishments produced about 2.3 billion pounds of comminuted chicken
in 2021. Using the categories in the 2016 cost-benefit analysis, the
Agency classified 35 establishments as medium-volume and 39
establishments as low-volume. The

[[Page 64725]]

35 medium-volume establishments accounted for 97.2 percent of total
production of comminuted chicken in 2021.

Table 15--Comminuted Chicken: Establishments Under FSIS Performance Standards (2021)
----------------------------------------------------------------------------------------------------------------
Definition (daily Number of Annual production Share of
Establishment volume category production pounds) establishments (million pounds) production (%)
----------------------------------------------------------------------------------------------------------------
High............................. 250,000 or more..... 0 0 0.0
Medium........................... More than 6,000 and 35 2,193 97.2
less than 250,000.
Low.............................. Less than 6,000..... 39 63 2.8
--------------------------------------------------------
Total........................ .................... 74 2,256 .................
----------------------------------------------------------------------------------------------------------------
Note: Numbers in table may not sum to totals due to rounding.

Comminuted Turkey
In 2021, there were 48 establishments under FSIS verification
sampling for comminuted turkey (Table 16). FSIS estimates that these
establishments produced about 1.7 billion pounds of comminuted turkey
in 2021. Using the categories in the 2016 cost-benefit analysis, the
Agency classified 5 establishments as high-volume, 25 establishments as
medium-volume, and 18 as low-volume establishments. The 5 high-volume
establishments accounted for 54.2 percent of the total production in
2021, while medium-volume establishments accounted for 45.3 percent,
and low-volume establishments accounted for less than 1 percent of the
total.

Table 16--Comminuted Turkey: Establishments Under FSIS Performance Standards (2021)
----------------------------------------------------------------------------------------------------------------
Definition (daily Number of Annual production Share of
Establishment volume category production pounds) establishments (million pounds) production (%)
----------------------------------------------------------------------------------------------------------------
High............................. 250,000 or more..... 5 917 54.2
Medium........................... More than 6,001 and 25 766 45.3
less than 250,000.
Low.............................. Less than 6,000..... 18 8 0.5
--------------------------------------------------------
Total........................ .................... 48 1,691 .................
----------------------------------------------------------------------------------------------------------------
Note: Numbers in table may not sum to totals due to rounding.

Salmonella on Poultry Products
Salmonella is a foodborne pathogen commonly attributed to
consumption of contaminated products that can lead to serious illness
and death. In the United States, it is estimated to cause over 1.35
million illnesses annually, including 26,500 hospitalizations and 420
deaths.\196\ Salmonella is estimated to be the leading pathogen in
terms of total cost of illnesses in the United States, with about 24
percent of the total cost.\197\ A 2020 study estimated that the
economic costs of Salmonella illnesses associated with chicken is $2.8
billion annually.\198\ A 2021 Interagency Food Safety Analytics
Collaboration report attributed roughly 23 percent of the total annual
Salmonella illnesses to consumption of poultry products, mainly chicken
(17 percent) and turkey (6 percent).\199\ Salmonella outbreaks linked
to poultry products have continued to occur over the last two decades.
From 1998 to 2020, FSIS identified 210 foodborne Salmonella outbreaks
linked to chicken or turkey (Figure 1).\200\ Generally, chicken
products were implicated in 84.8 percent (178 out of 210) of the
outbreaks and turkey products were implicated in 15.2 percent (32 out
of 210) of the outbreaks.\201\
---------------------------------------------------------------------------

\196\ CDC, ``Salmonella,'' November 10, 2022. https://www.cdc.gov/salmonella/index.html; USDA, FSIS, ``Risk Profile for
Pathogenic Salmonella Subtypes in Poultry,'' February 28, 2023 at:
https://www.regulations.gov/docket/FSIS-2023-0028.
\197\ USDA, ERS, ``Cost Estimates of Foodborne Illnesses,''
Total cost of foodborne illness estimates for 15 leading foodborne
pathogens dataset, March 10, 2021, https://www.ers.usda.gov/data-products/cost-estimates-of-foodborne-illnesses.aspx.
\198\ USDA, FSIS, ``USDA Releases Proposed Regulatory Framework
to Reduce Salmonella Infections Linked to Poultry Products,''
October 14, 2022, https://www.fsis.usda.gov/news-events/news-press-releases/usda-releases-proposed-regulatory-framework-reduce-salmonella. A cost of illness model that replaces the productivity
loss estimates with a pain, suffering, and functional disability
measure based on monetized quality-adjusted life year estimates
indicates that the estimated annual cost of Salmonella illness was
around $11.4 billion (ranging from $2.5 to $29.1 billion) in 2010
dollars. Scharff, R.L., 2012. Economic burden from health losses due
to foodborne illness in the United States. Journal of food
protection, 75(1), pp.123-131, DOI: 10.4315/0362-028X.JFP-11-058.
\199\ The Interagency Food Safety Analytics Collaboration,
``Foodborne illness source attribution estimates for 2019 for
Salmonella, Escherichia coli O157, Listeria monocytogenes, and
Campylobacter using multi-year outbreak surveillance data, United
States,'' October 2021, https://www.cdc.gov/foodsafety/ifsac/pdf/P19-2019-report-TriAgency-508.pdf.
\200\ Chicken was considered the source of contamination on the
outbreak linked to stuffed chicken products.
\201\ CDC, National Outbreak Reporting System (NORS), NORS
Dashboard, accessed April 2023, https://wwwn.cdc.gov/norsdashboard/
;USDA, FSIS, ``Outbreak Investigations: Response May 10, 2023
https://www.fsis.usda.gov/food-safety/foodborne-illness-and-disease/outbreaks/outbreak-investigations-response.

---------------------------------------------------------------------------

[[Page 64726]]

[GRAPHIC] [TIFF OMITTED] TP07AU24.041

In 2023, FSIS developed a risk profile that details current
knowledge on Salmonella to inform Agency efforts. The risk profile
identified 28 Salmonella serotypes (out of around 2,500 serotypes) and
four serogroups which were attributed to human salmonellosis from
consuming chicken and turkey products. The FSIS risk profile indicated
that for at least some subtypes of concern a small amount (i.e., low
dose of Salmonella bacteria), can cause illness. The FSIS risk profile
noted that certain serotypes caused hospitalization more frequently and
also led to invasive disease and death. Some subtypes have also been
found to cause debilitating human health outcomes. Among these outcomes
are cancer, inflammatory bowel disease, irritable bowel syndrome, and
reactive arthritis. The overall hospitalization rate for all Salmonella
is about 2 percent and the fatality rate is about 0.04 percent.
However, the hospitalization rate for these serotypes is nearly 23
percent and the fatality rate is about 0.5 percent.\202\
---------------------------------------------------------------------------

\202\ USDA, FSIS, ``Risk Profile for Pathogenic Salmonella
Subtypes in Poultry,'' February 28, 2023 at: https://www.regulations.gov/docket/FSIS-2023-0028.
---------------------------------------------------------------------------

Salmonella is the main pathogen resulting in foodborne illness-
related deaths and hospitalizations, as well as loss of quality-
adjusted life years (QALYs) and disability-adjusted life years (DALYs).
The CDC estimates that Salmonella accounts for about 11 percent of
total cases of domestically acquired foodborne illness.\203\ However,
it disproportionately accounts for about 44 percent of deaths
associated with domestic bacterial foodborne illness from major
pathogens and 28 percent of the hospitalizations. It has also been
estimated to lead to the highest amount of QALYs lost among 14 domestic
foodborne bacterial, viral, and parasitic pathogens. Salmonella is also
estimated to contribute to 32,900 lost DALYs, or about 30 percent of
lost DALYs from seven leading foodborne pathogens.\204\
---------------------------------------------------------------------------

\203\ CDC, ``Burden of Foodborne Illness: Findings,'' November
5, 2018, https://www.cdc.gov/foodborneburden/2011-foodborne-estimates.html.
\204\ USDA, FSIS, ``Risk Profile for Pathogenic Salmonella
Subtypes in Poultry,'' February 28, 2023 at: https://www.regulations.gov/docket/FSIS-2023-0028.
---------------------------------------------------------------------------

Potential Costs and Benefits of the Proposed Rule and Proposed
Determination
FSIS estimates that this proposal would result in a reduction in
Salmonella illnesses among consumers. Furthermore, for producers, the
reduction in the risk of illness, and hence outbreaks, would result in
a lower risk of having to recall product. Producers would, as a result
avoid the costs associated with that reduction. While producers would
respond to this proposal in a way that makes economic sense to them,
FSIS estimated the quantified cost associated with this proposal as
explained in more detail below.
This proposal would also benefit industry as FSIS would clarify
process control requirements for poultry slaughter establishments,
which would likely contribute to a reduction in Salmonella
contamination. Further, the Agency would incentivize innovation and the
adoption of safer scientific methods in poultry production.
In the following sections, this analysis presents potential costs
and benefits generated over a range of assumptions that could accrue as
a result of FSIS' action, if this rule is finalized. To implement this
proposal, FSIS would adopt an implementation schedule that would allow
medium-, low-, and very low-volume establishments additional
flexibility. Specifically, medium-volume establishments would have two
years after the proposal is finalized to comply with the proposed
requirements, while low- and very low-volume establishments would have
three years. High-volume establishments would be required to comply
with these proposed requirements one year after this rule is finalized.
The Agency incorporated this implementation schedule into the
annualization of costs and benefits estimates in this analysis, which
are presented after the one-time and recurring cost estimates for each
requirement. FSIS annualized costs and benefits using a 7 percent
discount rate over a period of 10 years. FSIS applied the share of
production for each establishment category to derive the lost value and
prevented illness estimates that correspond with the implementation
schedule. FSIS is seeking comment on these assumptions.

[[Page 64727]]

Potential Costs of the Proposed Rule and Proposed Determination
Costs Associated With the Proposed Rule
Statistical Process Control Costs
FSIS currently requires poultry slaughter establishments to
develop, implement, and maintain written procedures to prevent
contamination by enteric pathogens and fecal contamination throughout
the entire slaughter operation and incorporate these procedures into
their HACCP systems (9 CFR 381.65(g)). At a minimum, these procedures
must include sampling and analysis for microbial organisms at pre-and
post-chill to monitor their ability to maintain process control, with
some exceptions for VS and VLV establishments operating under
Traditional Inspection. The proposal specifies that establishments must
collect the pre-chill sample at rehang (post-picking and pre-
evisceration) and clarifies that its microbial organism monitoring
practices must result in data suitable for monitoring process control.
While many establishments already meet the proposed specifications,
some establishments may change where they collect the pre-chill sample
or change the microbial organism they test for. However, establishments
may continue their current sampling location and microbial organism
monitoring practices, or adopt an alternative location and organism, if
they submit and maintain supporting documentation. The Agency is also
providing guidance for establishments to develop their MMPs. FSIS
assumes that most establishments would meet the proposed MMP
requirements without having to make any changes that would result in
costs, while some establishments would have to make minor changes in
response to this proposal at de minimis costs. The Agency is seeking
comments on these assumptions.
FSIS regulations currently require that VLV establishments collect
process control monitoring samples minimally once per week for a
minimum of 13 consecutive weeks per year, beginning the first week of
June.\205\ FSIS is proposing to eliminate the requirement that VLV
establishments begin sample collection the first week in June, which
would allow establishments to begin collecting samples throughout the
year. FSIS estimates there is no cost associated with this revised
requirement, while establishments may benefit from this flexibility.
---------------------------------------------------------------------------

\205\ 9 CFR 381.65(g)(2)(ii).
---------------------------------------------------------------------------

FSIS estimates that 90 VLV and 2 VS poultry slaughter
establishments operating under Traditional Inspection would likely need
to make changes in response to the proposed process control
requirements.\206\ FSIS is proposing to revise 9 CFR 381.65g(1) such
that all poultry slaughter establishments would be required to collect
samples at the rehang and post-chill locations. Very small and VLV
establishments operating under Traditional Inspection are currently
required to collect samples only at post-chill. FSIS currently requires
that VLV establishments minimally collect 13 weekly samples per year to
monitor process control. If this rule is finalized, these
establishments would be required to collect and analyze 13 additional
samples per year. The number of additional samples for VS
establishments operating under Traditional Inspection that are not VLV
establishments depends on their production volume. FSIS assumed that
these VS establishments currently collect 52 samples per year and,
consequently, would collect an additional 52 samples per year. FSIS is
seeking comment on these assumptions.
---------------------------------------------------------------------------

\206\ Very low-volume establishments are those that slaughter
less than 440,000 chickens or 60,000 of any other poultry class
annually. Very small establishments are those with less than 10
employees or under $2.5 million in annual sales. 9 CFR 381.65g(1)(i)
and 9 CFR 381.65g(1)(ii).
---------------------------------------------------------------------------

FSIS would reduce the burden this proposed increase in sampling
places on VLV and VS establishments operating under Traditional
Inspection by making laboratory services available to these
establishments. Use of the laboratories provided by FSIS would enable
these establishments to comply with the proposed minimum requirements
for MMPs. Should these establishments elect not to use the laboratory
services provided by FSIS, the Agency estimated the combined cost for
these establishments to meet the proposed increase in sampling would be
$48,412 annually (Table 17). Assuming the proposed implementation
schedule and annualizing over 10 years at a 7 percent discount rate,
the cost for these establishments to meet the proposed increase in
sampling would be $35,950. This analysis assumed samples collected at
these establishments are analyzed for AC, at a cost of $38 per sample.

Table 17--Statistical Process Control Costs
------------------------------------------------------------------------
Number of
Establishments type establishments Testing cost ($)
(2021)
------------------------------------------------------------------------
Very low-volume under Traditional 90 44,460
Inspection.......................
Very small under Traditional 2 3,952
Inspection.......................
-------------------------------------
Total......................... 92 48,412
Annualized \1\................ ................. 35,950
------------------------------------------------------------------------
\1\ Costs annualized at a discount rate of 7% over 10 years.
* Note: Numbers in table may not sum to totals due to rounding.

Electronic Data Submission
FSIS would require poultry slaughter establishments subject to 9
CFR 381.65(g) and (h) to electronically submit data generated as part
of their process control monitoring. FSIS estimates that high- and
medium-volume establishments already compile process control data
electronically due to the large volume of their operations and the
frequency of their sample collection and analysis. To mitigate the
impact on low- and VLV establishments, should this rule become final,
the Agency would develop and publish a template these establishments
could use to record and submit their monthly results.
In 2021, there were 298 establishments that would have been subject
to this change, of which 175 were high-volume, 15 medium-, 14 low-, and
94 very low-volume.\207\

[[Page 64728]]

Establishments that elect to use laboratory services provided by FSIS
for their process control samples would meet this requirement and not
incur additional costs. This analysis assumed that none of the eligible
establishments would choose to use laboratories provided by FSIS and
the Agency estimated the costs associated with this requirement for all
eligible establishments. Consequently, there is a tendency toward
overstatement in the cost to regulated establishments associated with
this proposal.
---------------------------------------------------------------------------

\207\ The 94 VLV establishments include the 90 establishments
operating under Traditional Inspection, as well as four
establishments not under Traditional Inspection.
---------------------------------------------------------------------------

FSIS assumed it would take a quality control (QC) manager 30
minutes (0.5 hours) once a month to submit these data. FSIS estimates
that the average wage for a QC manager is $113.24, which includes an
average hourly wage of $56.62 multiplied by a benefits and overhead
factor of two.\208\ Under these assumptions, the combined cost to
industry is $202,473 (0.5 hours x 12 months x 298 establishments x
$113.24) per year (Table 18), including $118,902 for high-volume
establishments, $10,192 for medium-volume, $9,512 for low-volume, and
$63,867 for VLV. Assuming the proposed implementation schedule and
annualizing over 10 years at a 7 percent discount rate, the cost for
electronic data submissions is $182,228.
---------------------------------------------------------------------------

\208\ Mean hourly wage estimate of $56.62 obtained from the
Bureau of Labor Statistics, May 2021 National Industry Specific
Occupational Employment and Wage Estimates for 11-3051 Management
Occupations. https://www.bls.gov/oes/2021/may/oes113051.htm.

Table 18--Electronic Data Submission Costs
----------------------------------------------------------------------------------------------------------------
Cost ($)
---------------------------------------------------------------
Establishment volume category All other
Chicken Turkey classes Total
----------------------------------------------------------------------------------------------------------------
High............................................ 97,839 19,024 2,038 118,902
Medium.......................................... 8,153 679 1,359 10,192
Low............................................. 7,474 679 1,359 9,512
Very Low........................................ 55,714 7,474 679 63,867
---------------------------------------------------------------
Total....................................... 169,181 27,857 5,436 202,473
Annualized \1\.............................. .............. .............. .............. 182,228
----------------------------------------------------------------------------------------------------------------
\1\ Costs annualized at a discount rate of 7% over 10 years.
Note: Numbers in table may not sum to totals due to rounding.

HACCP Plan Reassessment Costs ²⁰⁹
---------------------------------------------------------------------------

\209\ Note: For simplicity, this section includes HACCP
reassessment costs associated with the proposed rule and proposed
determination, as some establishments subject to the proposed rule
are also subject to the proposed determination.
---------------------------------------------------------------------------

The Agency assumed that every poultry slaughter establishment would
reassess their HACCP plans and incur associated costs. This likely
overestimates costs because not every establishment would reassess
their HACCP plans. For chicken slaughter establishments that produce
chicken carcasses subject to these proposed final product standards and
are also subject to the proposed process control requirements, FSIS
assumed they would only reassess their slaughter HACCP plan once.
However, for establishments that produce multiple products subject to
these final product standards, FSIS assumed they would reassess their
HACCP plans for each of the products they produce that are affected by
the proposed changes. However, establishments that have to reassess
HACCP plans for multiple products would likely experience some
economies of scope. Furthermore, establishments could coordinate
reassessing their HACCP plans in response to this proposal with
currently required annual reassessments.
FSIS estimates that the total cost to industry from reassessing
HACCP plans as a result of this proposal is $1.39 million, ranging from
$0.70 to $2.09 million (Table 19). Assuming the proposed implementation
schedule and annualizing over 10 years at a 7 percent discount rate,
the cost for HACCP plan reassessment is $0.18 million, ranging from
$0.09 million to $0.26 million. High- and medium-volume establishments
need an average of 60 hours (ranging from 30 to 90), while low and VLV
establishments need an average of 30 hours (ranging from 15 to 45) to
reassess a HACCP plan, according to the 2015 ``Costs of Food Safety
Investments'' report. This report estimated costs for large and small
establishments. FSIS assumed the large category would correspond with
high- and medium-volume establishments, while the small category would
correspond with low- and very low-volume establishments. FSIS used data
from the U.S. Bureau of Labor Statistics to update the hourly wage for
estimating these labor costs. Specifically, FSIS used the 2021 hourly
wage for a production worker of $30.78, which includes an average
hourly wage of $15.39 multiplied by a benefits and overhead factor of
two.

Table 19--HACCP Plan Reassessment Costs
----------------------------------------------------------------------------------------------------------------
Cost (million $)
Establishment volume category Number of --------------------------------------------------------
establishments Low Mid High
----------------------------------------------------------------------------------------------------------------
High................................ 333 0.31 0.61 0.92
Medium.............................. 279 0.26 0.52 0.77
Low................................. 193 0.09 0.18 0.27
Very Low............................ 91 0.04 0.08 0.13
---------------------------------------------------------------------------
Total........................... ................. 0.70 1.39 2.09
Annualized \1\.................. ................. 0.09 0.18 0.26
----------------------------------------------------------------------------------------------------------------
\1\ Costs are annualized at a 7 percent discount rate over 10 years.

[[Page 64729]]

Note: Number of establishments is not additive as some establishments produce multiple products. Numbers in
table may not sum to totals due to rounding.

Validation of HACCP Plans
If an establishment makes changes to their HACCP plan, they would
also have to validate it, incurring associated costs. However, the
Agency assumed few establishments would make changes to their MMPs and
only those that make changes would need to validate their HACCP plans.
Additionally, the Agency assumed that many establishments have already
implemented Salmonella controls in response to the 2016 FSIS
performance standards and will not need to make changes to their HACCP
plan. The 2015 ``Costs of Food Safety Interventions'' report indicates
that high- and medium-volume establishments would need an average of
320 labor hours, while low- or very low-volume establishments would
need an average of 400 hours to validate a HACCP plan. The estimated
cost for HACCP plan validation is $25,894 for a high or medium-volume
establishment, on average, and for a low- or very low-volume
establishment it is $32,368. FSIS used the 2021 hourly wage for a food
scientist of $80.92, which includes an average hourly wage of $40.46
multiplied by a benefits and overhead factor of two, for this
estimate.\210\ FSIS did not include a total industry HACCP validation
cost because FSIS does not have data on the number of establishments
that will make changes to their plans in response to this proposal.
FSIS is requesting comments to address this data gap.
---------------------------------------------------------------------------

\210\ BLS, May 2021 National Industry-Specific Occupational
Employment and Wage Estimates for 19-1012 Food Scientists and
Technologists, accessed April 13, 2023, https://www.bls.gov/oes/2021/may/oes191012.htm.
---------------------------------------------------------------------------

Costs Associated With the Proposed Determination
Maintaining Control of Sampled Product Costs
FSIS is proposing that chicken carcasses, chicken parts, comminuted
chicken, and comminuted turkey with Salmonella levels at or above 10
cfu/mL(g) and one of the Salmonella serotypes of public health
significance intended for consumption as final products would be
adulterated. As proposed, FSIS inspected establishments would be
required to maintain control of product sampled as part of FSIS
verification sampling for adulterants. Any chicken carcass, parts,
comminuted chicken, or comminuted turkey final products testing
positive for Salmonella levels at 10 cfu/mL(g) or higher would not be
allowed to enter commerce until the Salmonella serotype result is
reported and no serotypes of public health significance are detected.
If this proposal is finalized, establishments would be required to
prevent product sampled as part of FSIS verification sampling from
entering commerce until a negative test result or one above the 10 cfu/
mL(g) level but not containing a serotype of public health significance
is received. FSIS does not require establishments to hold product at
their physical location; thus, product can be stored off-site at an
establishment's storage facility, or another private or public storage
facility, pending test results. Product subject to FSIS verification
sampling can also be diverted and processed into a product that is not
subject to these final product standards (i.e., fully cooked products)
instead of being sent to cold storage.
FSIS anticipates that the Agency would provide establishments with
final adulteration results five days after the sample is
collected.\211\ Results on a product's level of Salmonella would
require industry to hold sampled lots for two days and results on the
presence of a serotype of public health significance would take an
additional three days. The Agency assumed that establishments would
maintain control of product until final adulteration results are
available. Establishments would be able to move product with test
results at levels below 10 cfu/mL(g) into commerce, which would
necessitate product to be under establishment's control for up to two
days. The Agency assumed that establishments would decide to divert
adulterated product after results on its adulteration status are
available. This cost is described in the Lost value to the industry
costs section.
---------------------------------------------------------------------------

\211\ While the Agency currently uses whole genome sequencing to
determine the presence of Salmonella serotypes on product sampled by
FSIS, the Agency would adopt an alternative approach that would lead
to results on the presence of Salmonella serotypes in one to three
days after screening.
---------------------------------------------------------------------------

To estimate the industry cost for holding product pending test
results, FSIS used 2021 data from PHIS. FSIS assumed that
establishments subject to these final product standards would maintain
control of each sampled lot pending FSIS verification sampling results.
Regulated establishments define their production lots according to
their specific conditions and FSIS allows establishments to adjust
their lot sizes if they provide scientific justification for defining
lots.\212\ Thus, FSIS used Agency data to approximate the amount of
product subject to verification sampling. For chicken carcasses, the
estimated lot size is 46,000 birds for high- and medium-volume
establishments and 1,800 birds for low- and very low-volume
establishments.\213\ For establishments producing chicken parts,
comminuted chicken, and comminuted turkey, the estimated lot sizes are
(1) one hour, (2) one shift, and (3) one day of production. These
estimated lot sizes, respectively, represent the low, medium, and high
scenarios used for estimating the cost of maintaining control of
product pending test results for chicken parts, comminuted chicken, and
comminuted turkey in this analysis. FSIS is seeking comment on these
assumptions.
---------------------------------------------------------------------------

\212\ 77 FR 73401.
\213\ Establishments that slaughter less than 1 million birds
per year had flock sizes ranging from 100 to 3,500 birds. FSIS used
the average, or 1,800 birds, to approximate the total sampled
production at these establishments.
---------------------------------------------------------------------------

Since FSIS is proposing to sample these products at the same rate
as the current performance standards, the Agency used the number of
samples collected in 2021 at establishments that would be subject to
this proposal and the estimated lot sizes to approximate the volume of
product that would be subject to the Agency's verification sampling
program.\214\
---------------------------------------------------------------------------

\214\ FSIS collects up to five continuous samples per month at
establishments producing young chicken and turkey carcasses, and raw
chicken parts, comminuted chicken and turkey products. USDA, FSIS,
``Salmonella Verification Testing Program Monthly Posting,'' April
20, 2023, https://www.fsis.usda.gov/science-data/data-sets-
visualizations/microbiology/Salmonella-verification-testing-program-
monthly.
---------------------------------------------------------------------------

FSIS used the per pound cost of cold storage as estimated in the
2015 ``Costs of Food Safety Investments'' report to monetize the cost
to industry from holding product due to this proposal.\215\

[[Page 64730]]

FSIS updated this estimate to 2021 dollars by applying the growth in
the ``Moving, storage, freight expense'' consumer price index.\216\ The
resulting cost of cold storage estimate, on a per pound, per day basis
is $0.0023 in 2021 dollars. Establishments may already store product in
their facilities or in an off-site location for a certain amount of
time. However, the Agency assumed that all costs of storing product for
the sampled lots are due to this proposal. FSIS is seeking comments on
cold storage costs and availability at inspected establishments or off-
site facilities.
---------------------------------------------------------------------------

\215\ For cold storage, the report assumes that the cost of
creating and maintaining onsite storage would be equivalent to
third-party, offsite cold storage. The establishment needs to ensure
that the offsite cold storage facility is certified for food-grade
products by USDA. Incoming product will already be cooled, so the
storage facility would only need to maintain the product
temperature. FSIS assumed product would be refrigerated. RTI Costs
of Food Safety Investments. September 2015. Contract No. AG-3A94-B-
13-0003 Order No. AG-3A94-K-14-0056. Revised Final Report. Prepared
by Catherine L. Viator, Mary K. Muth, Jenna E. Brophy. RTI
International. RTI Project Number 0214016.003.000.001. The full
report is available here: https://www.fsis.usda.gov/sites/default/files/media_file/documents/Costs_of_Food_Safety_Investments_FSIS-2022-0013.pdf.
\216\ Bureau of Labor Statistics (BLS), Consumer Price Index
(CPI), ``Moving, storage, freight expense in U.S. city average, all
urban consumers, not seasonally adjusted,'' (Series ID
CUUR0000SEHP03), accessed February 14, 2023. This CPI grew 37.5
percent from 2015 to 2021.
---------------------------------------------------------------------------

Chicken Carcasses
FSIS estimated that in 2021 establishments subject to the
performance standards produced 33.2 billion pounds of chicken
carcasses. \217\ The Agency estimated that about 11 percent of chicken
carcasses are consumed as whole birds and, thus, final products subject
to the proposal.\218\ To account for uncertainty in this estimate, the
Agency used 6, 11, and 16 percent as the low, medium, and high
estimates of the volume of chicken carcasses subject to the proposal.
FSIS estimated that in 2021 a total of 162.9 million pounds, ranging
from 88.9 to 237.0 million, would have been sampled as part of these
final product standards (Table 20).\219\ There is likely a tendency
toward overstatement in this estimate of the volume of product subject
to FSIS verification sampling as lot sizes vary by establishments and
lot sizes may be smaller than the sizes FSIS assumed for this analysis.
---------------------------------------------------------------------------

\217\ (8.3 billion birds x 4 pounds). Dressed weights for
chickens vary. For broilers, which is the main class of poultry
slaughtered at FSIS inspected establishments, the 2023 chicken Risk
Assessment used an average carcass weight was 4 pounds.
\218\ USDA, FSIS, ``Quantitative Microbiological Risk Assessment
for Salmonella in Raw Chicken and Raw Chicken Products,'' January
2023 at: https://www.regulations.gov/docket/FSIS-2023-0028.
Estimates from the National Chicken Council indicate that about
9 percent of broilers, the main chicken subclass produced in the
United States, were marketed as whole birds in 2021. National
Chicken Council (NCC), ``How Broilers are Marketed,'' accessed May
11, 2023, https://www.nationalchickencouncil.org/statistic/how-broilers-are-marketed/.
\219\ This is the sum of the estimated sampled volume for all
establishment categories. For each category, this volume is
calculated as: number of establishments x average number of samples
x lot size converted to pounds x estimated share of production
intended as final product. For example, the medium estimate for
high-volume establishments is 142 x 55 x (46,000 x 4) x 0.10.
Calculations might not sum to totals due to rounding.

Table 20--Chicken Carcasses: Estimated Sampled Volume by Establishment Volume Category
[2021]
----------------------------------------------------------------------------------------------------------------
Estimated sampled volume (million pounds)
Establishment volume category Number of --------------------------------------------------------
establishments Low Medium High
----------------------------------------------------------------------------------------------------------------
High................................ 142 86.8 159.1 231.4
Medium.............................. 9 1.8 3.4 4.9
Low................................. 4 0.04 0.1 0.1
Very Low............................ 33 0.2 0.4 0.6
---------------------------------------------------------------------------
Total........................... 188 88.9 162.9 237.0
----------------------------------------------------------------------------------------------------------------
Note: Numbers in table may not sum to totals due to rounding.

This analysis assumed establishments would maintain control of
sampled product until results on the level of Salmonella are available,
which is expected to take two days. FSIS assumes establishments would
move into commerce product with test results below 10 cfu/mL(g) and
would hold product at or above that level for an additional three days.
FSIS estimated that 654,123 pounds of chicken carcasses would have test
results at or above 10 cfu/mL, which would be held until results on the
presence of a serotype of public health significance were available.
FSIS estimated the total cost to industry of holding all sampled
chicken carcasses pending test results at $0.75 million annually
[(162.9 million x $0.0023 x 2) + (654,123 x $0.0023 x 3)], ranging from
$0.41 to $1.09 million (Table 21). Assuming the proposed implementation
schedule and annualizing over 10 years at a 7 percent discount rate,
the cost for holding chicken carcasses pending test results is $0.75
million, ranging from $0.41 million to $1.09 million.

Table 21--Chicken Carcasses: Maintaining Control of Sampled Product Costs
----------------------------------------------------------------------------------------------------------------
Estimated cost (million $)
Category --------------------------------------------------------
Low Medium High
----------------------------------------------------------------------------------------------------------------
High................................................... 0.40 0.73 1.07
Medium................................................. 0.01 0.02 0.02
Low.................................................... 0.0002 0.0003 0.0005
Very low............................................... 0.0011 0.0020 0.0029
--------------------------------------------------------
Total.............................................. 0.41 0.75 1.09
Annualized \1\..................................... 0.41 0.75 1.09
----------------------------------------------------------------------------------------------------------------
\1\ Costs are annualized at a 7 percent discount rate over 10 years.
Note: Numbers in table may not sum to totals due to rounding.

[[Page 64731]]

Chicken Parts
FSIS estimated that in 2021 establishments subject to the
performance standards processed 31.2 billion pounds of chicken
parts.\220\ Raw chicken parts processed at FSIS regulated
establishments can be sent into commerce as final products or further
processed into a variety of preparations, including cooked products
(e.g., fully cooked chicken breasts). As such, FSIS assumed that 80,
85, or 90 percent of the estimated production of chicken parts would be
raw final product subject to this proposal. FSIS is seeking comments on
this assumption. FSIS estimated that 2.6 billion pounds of chicken
parts, ranging from 308 million to 5.5 billion, would have been sampled
as part of these final product standards (Table 22).\221\ There is
likely a tendency toward overstatement in this estimate of the volume
of product subject to FSIS verification sampling as lot sizes vary by
establishments and lot sizes may be smaller than the sizes FSIS assumed
for this analysis.
---------------------------------------------------------------------------

\220\ The 2023 chicken risk assessment estimated that, of the
total chicken slaughtered volume, about 83 percent is consumed as
chicken parts. In 2021, total chicken slaughter volume was an
estimated 37 billion pounds, 31.2 billion of which are estimated to
be processed into chicken parts.
\221\ FSIS calculated these estimates using average daily
production volume and total number of samples in 2021 for each of
the establishments producing chicken parts assuming lot sizes of one
hour, one shift, and one day of production. FSIS multiplied this
result by the share production intended as final product to obtain
the low, medium, and high estimates.

Table 22--Chicken Parts: Estimated Sampled Volume by Establishment Volume Category
[2021]
----------------------------------------------------------------------------------------------------------------
Estimated sampled volume (million pounds)
Category Number of --------------------------------------------------------
establishments Low Medium High
----------------------------------------------------------------------------------------------------------------
High................................ 154 286 2,433 5,153
Medium.............................. 209 21 181 325
Low................................. 127 0 3 5
---------------------------------------------------------------------------
Total........................... 490 308 2,617 5,483
----------------------------------------------------------------------------------------------------------------
Note: Numbers in table may not sum to totals due to rounding.

This analysis assumed establishments would maintain control of
sampled product until results on the level of Salmonella are available,
which is expected to take two days. FSIS assumed establishments would
move product with test results below 10 cfu/mL(g) into commerce and
would hold for an additional three days product with results at or
above that level. FSIS estimated that about 246,949 pounds of chicken
parts would have test results at or above 10 cfu/mL(g), which would be
held until results on the presence of a serotype of public health
significance were available. FSIS estimated the cost to industry of
holding all sampled chicken parts pending test results at $12.0 million
annually [(2.6 billion x $0.0023 x 2) + (246,949 x $0.0023 x 3)],
ranging from $1.4 to $25.1 million (Table 22). Assuming the proposed
implementation schedule and annualizing over 10 years at a 7 percent
discount rate, the cost for holding chicken parts pending test results
is $11.88 million, ranging from $1.4 million to $24.9 million.

Table 23--Chicken Parts: Maintaining Control of Sampled Product Costs
----------------------------------------------------------------------------------------------------------------
Cost (million $)
Category --------------------------------------------------------
Low Medium High
----------------------------------------------------------------------------------------------------------------
High................................................... 1.31 11.15 23.62
Medium................................................. 0.10 0.83 1.49
Low.................................................... 0.00 0.02 0.02
--------------------------------------------------------
Total.............................................. 1.41 12.00 25.13
Annualized \1\..................................... 1.40 11.88 24.93
----------------------------------------------------------------------------------------------------------------
\1\ Costs are annualized at a 7 percent discount rate over 10 years.
Note: Numbers in table may not sum to totals due to rounding.

Comminuted Chicken
FSIS estimated that in 2021 establishments subject to the
performance standards processed 2.3 billion pounds of comminuted
chicken. Raw comminuted chicken processed at FSIS regulated
establishments can be sent into commerce as final products or further
processed into a variety of preparations, including cooked products
(e.g., fully cooked chicken nuggets). As such, FSIS assumed that 80,
85, or 90 percent of the estimated production of comminuted chicken
would be raw final product subject to this proposal. FSIS is seeking
comments on this assumption. FSIS estimated that 264.19 million pounds,
ranging from 26.1 to 427.65 million pounds of comminuted chicken, would
have been sampled as part of these final product standards (Table
24).\222\ There is likely a tendency toward overstatement in this
estimate of the volume of product subject to FSIS verification sampling
as lot sizes vary by establishments and lot sizes may be smaller than
the sizes FSIS assumed for this analysis.
---------------------------------------------------------------------------

\222\ FSIS calculated these estimates using average daily
production volume and total production days in 2021 for each of the
establishments producing comminuted chicken and multiplying by the
share production intended as final product.

[[Page 64732]]

Table 24--Comminuted Chicken: Estimated Sampled Volume by Establishment Volume Category
[2021]
----------------------------------------------------------------------------------------------------------------
Estimated sampled volume (million pounds)
Category Number of --------------------------------------------------------
establishments Low Medium High
----------------------------------------------------------------------------------------------------------------
High................................ 0 0 0 0
Medium.............................. 35 25.12 254.59 415.22
Low................................. 39 1.02 9.59 12.43
---------------------------------------------------------------------------
Total........................... 74 26.14 264.19 427.65
----------------------------------------------------------------------------------------------------------------
Note: Numbers in table may not sum to totals due to rounding.

This analysis assumed establishments would maintain control of this
product until results on the level of Salmonella are available, which
is expected to take two days. FSIS assumed establishments would move
product with test results below 10 cfu/mL(g) into commerce and would
hold for an additional three days products with results at or above
that level. FSIS estimated that about 5.0 million pounds of comminuted
chicken would have test results at or above 10 cfu/mL(g), which would
be held until results on the presence of a serotype of public health
significance were available. FSIS estimated the cost to industry of
holding all sampled comminuted chicken pending test results at $1.3
million annually (264.2 million x $0.0023 x 2) + (5.0 million x $0.0023
x 3)], ranging from $0.2 to $2.0 million (Table 25). Assuming the
proposed implementation schedule and annualizing over 10 years at a 7
percent discount rate, the cost for holding comminuted chicken products
pending test results is $1.1 million, ranging from $0.1 million to $1.7
million.

Table 25--Comminuted Chicken: Maintaining Control of Sampled Product Costs
----------------------------------------------------------------------------------------------------------------
Cost (million $)
Category --------------------------------------------------------
Low Medium High
----------------------------------------------------------------------------------------------------------------
High................................................... 0 0 0
Medium................................................. 0.15 1.20 1.94
Low.................................................... 0.006 0.04 0.06
--------------------------------------------------------
Total.............................................. 0.15 1.25 1.99
Annualized \1\..................................... 0.13 1.07 1.72
----------------------------------------------------------------------------------------------------------------
\1\ Costs are annualized at a 7 percent discount rate over 10 years.
Note: Numbers in table may not sum to totals due to rounding.

Comminuted Turkey
FSIS estimated that in 2021 establishments subject to the
performance standards processed 1.7 billion pounds of comminuted
turkey. Raw comminuted turkey processed at FSIS regulated
establishments can be sent into commerce as final products or further
processed into preparations including cooked products (e.g., fully
cooked sausages). As such, FSIS assumed that 80, 85, or 90 percent of
the estimated production of comminuted turkey would be raw final
product subject to this proposal. FSIS is seeking comments on this
assumption. FSIS estimates that 156.7 million pounds, ranging from 18.4
to 330.4 million, would have been sampled as part of these final
product standards (Table 26).\223\ There is likely a tendency toward
overstatement in this estimate of the volume of product subject to FSIS
verification sampling as lot sizes vary by establishments and lot sizes
may be smaller than the sizes FSIS assumed for this analysis.
---------------------------------------------------------------------------

\223\ FSIS calculated these estimates using average daily
production volume and total production days in 2021 for each of the
establishments producing comminuted turkey and multiplying by the
share production intended as final product.

Table 26--Comminuted Turkey: Estimated Sampled Volume by Establishment Volume Category
[2021]
----------------------------------------------------------------------------------------------------------------
Estimated sampled volume (million pounds)
Category Number of --------------------------------------------------------
establishments Low Medium High
----------------------------------------------------------------------------------------------------------------
High................................ 5 11.49 97.71 206.91
Medium.............................. 25 6.90 58.63 122.86
Low................................. 18 0.04 0.36 0.65
---------------------------------------------------------------------------
Total........................... 48 18.43 156.69 330.42
----------------------------------------------------------------------------------------------------------------
Note: Numbers in table may not sum to totals due to rounding.

[[Page 64733]]

This analysis assumed establishments would maintain control of this
product until results on the level of Salmonella are available, which
is expected to take two days. FSIS assumed establishments would move
product with test results below 10 cfu/mL(g) into commerce and would
hold for an additional three days product with results at or above that
level. FSIS estimated that about 2.3 million pounds of comminuted
turkey would have test results at or above 10 cfu/mL, which would be
held until results on the presence of a serotype of public health
significance were available. FSIS estimated the cost to industry of
holding all sampled comminuted turkey pending test results at $0.7
million annually [(156.7 million x $0.0023 x 2) + (2.3 million x
$0.0023 x 3)], ranging from $0.1 to $1.5 million (Table 27). Assuming
the proposed implementation schedule and annualizing over 10 years at a
7 percent discount rate, the cost for holding comminuted turkey
products pending test results is $0.70 million, ranging from $0.09
million to $1.45 million.

Table 27--Comminuted Turkey: Maintaining Control of Sampled Product Costs
----------------------------------------------------------------------------------------------------------------
Cost (million $)
Category --------------------------------------------------------
Low Medium High
----------------------------------------------------------------------------------------------------------------
High................................................... 0.06 0.45 0.96
Medium................................................. 0.04 0.28 0.57
Low.................................................... 0.0003 0.0017 0.0031
--------------------------------------------------------
Total.............................................. 0.10 0.73 1.53
Annualized \1\..................................... 0.09 0.70 1.45
----------------------------------------------------------------------------------------------------------------
\1\ Costs are annualized at a 7 percent discount rate over 10 years.
Note: Numbers in table may not sum to totals due to rounding.

Import Establishments Costs
FSIS conducts sampling activities at official import inspection
establishments to verify that a foreign country's poultry inspection
system is equivalent to the U.S. poultry inspection system. If this
rule is finalized, FSIS would adapt its current Salmonella sampling
program for imported chicken carcasses, chicken parts, comminuted
chicken, and comminuted turkey. Import establishments would be required
to maintain control of sampled product pending test results to verify
that these products are not adulterated. Similar to domestic producers,
FSIS assumed that official import inspection establishments would
maintain control of sampled imported product lots for two days until
results on the level of Salmonella are available. Sampled product with
results below 10 CFU/mL(g) could be moved into commerce. If test
results show Salmonella at or above 10 CFU/mL(g), FSIS assumed
establishments would maintain control of these product lots for an
additional one to three days, until the presence or absence of a
serotype of public health significance is confirmed. Adulterated
product would be diverted from U.S. commerce.
FSIS estimates the cost to import establishments for maintaining
control of imported product subject to FSIS verification sampling for
Salmonella, as described in this proposal, would be minimal. Poultry
imports represent a small fraction of the U.S. domestic poultry supply,
accounting for less than 0.5 percent in 2021.\224\ In that year, only
three countries exported raw chicken and turkey products to the United
States: Canada, Chile, and Mexico.\225\ Canada was the sole exporter of
whole chicken carcasses, accounting for about 14 million pounds of
chicken. Chile, in turn, was the main exporter of chicken parts (132
million pounds).\226\
---------------------------------------------------------------------------

\224\ USDA, Foreign Agricultural Service, ``Production, Supply
and Distribution database,'' accessed May 11, 2023. Although U.S.
import data does not directly correspond with the final product
categories in this proposal, FSIS used available trade data to
identify Harmonized Tariff Schedule (HTS) codes that would
approximate imports of chicken carcasses, chicken parts, comminuted
chicken, and comminuted turkey. FSIS estimates that imports of
chicken carcasses to the United States reached 13.7 million pounds
in 2021 (HTS 0207.11 and 0207.12, Whole young chickens and Whole
frozen chickens, respectively), while imports of chicken parts and
comminuted chicken were 164 million pounds (HTS 0207.13 and 0207.14,
Meat and edible offal of chickens, fresh or chilled and frozen,
respectively). FSIS assumed that imports under HTS 0207.26 and
0207.27 (Meat and edible offal of turkeys, fresh or chilled and
frozen, respectively) approximate imports of comminuted turkey,
although this is likely an overestimate as this HTS code also
includes turkey parts. Imports under HTS 0207.26 and 0207.27,
combined, reached 74.3 million pounds in 2022. Imports under these
HTS codes represent 0.5 percent of U.S. production of chicken
carcasses, 0.04 percent of U.S. production of chicken parts and
comminuted chicken, and 4 percent of imports of comminuted turkey.
U.S. International Trade Commission DataWeb/U.S. Department of
Commerce, accessed June 28, 2023.
\225\ Three countries are eligible to export raw chicken and
turkey products to the United States--Canada, Chile, and Poland,--
while Mexico is eligible to export only processed poultry products
slaughtered under Federal inspection in the United States or in a
country eligible to export slaughtered poultry to the United States.
USDA, FSIS, ``Eligible Foreign Establishments,'' July 14, 2023,
https://www.fsis.usda.gov/inspection/import-export/import-export-library/eligible-foreign-establishments.
\226\ U.S. International Trade Commission DataWeb/U.S.
Department of Commerce accessed June 28, 2023.
---------------------------------------------------------------------------

Currently, FSIS samples and tests imported chicken carcasses,
chicken parts, comminuted chicken, and comminuted turkey for the
presence of Salmonella. According to data from PHIS, in 2021, FSIS
collected and analyzed about 850 samples of imported chicken and turkey
products, which represented about 15.8 million pounds of product. These
samples were mainly from chicken parts and carcasses, as imports of
comminuted chicken and turkey are relatively low.
FSIS estimated the cost for these import establishments assuming
that establishments would maintain control pending test results of all
sampled product identified in 2021 data, which is likely an
overestimate. The estimated cost for import establishments is $0.07
million per year (15.8 million pounds x 2 days x $0.0023). While data
on the volume imported of product with results at or above 10 cfu/mL(g)
are not available, FSIS estimates this would be a relatively low volume
of product. In 2021, about 17 percent of imported poultry samples were
positive for the presence of Salmonella, representing about 2.6 million
pounds of product. This is likely a high estimate as countries would be
required to implement measures to maintain equivalence with the U.S.
poultry inspection system if this rule is finalized.

[[Page 64734]]

Total Costs to Industry From Maintaining Control of Sampled Product
FSIS estimated that the total cost to industry from complying with
FSIS verification sampling requirements in this proposal is $14.47
million annually, ranging from $2.11 to $29.26 million (Table 28),
assuming the proposed implementation schedule and annualizing over 10
years at a 7 percent discount rate. As previously described,
establishments are required to maintain control pending test results
for product subject to FSIS verification sampling for adulterants. FSIS
estimated that an average of 3.2 billion pounds of product per year
would be subject to FSIS verification sampling. FSIS allows
establishments to move product to an alternate location pending test
results for an adulterant as long as they maintain control of the
sampled product. Producers can also elect to divert sampled product
into a product that is not subject to these standards (i.e., fully
cooked products), rather than maintaining control of it pending test
results. Moreover, FSIS allows establishments to produce smaller
representative product lots for FSIS verification sampling if they
demonstrate that the lot presented is microbiologically independent
from other production lots.\227\ Thus, the cost for holding product
pending test results is likely an overestimate. FSIS is seeking
comments on these assumptions.
---------------------------------------------------------------------------

\227\ 77 FR 73402.

Table 28--Summary of Costs to Industry From Maintaining Control of Sampled Product
----------------------------------------------------------------------------------------------------------------
Number of Cost (million $) \2\
Product establishments --------------------------------------------------------
\1\ Low Medium High
----------------------------------------------------------------------------------------------------------------
Chicken carcasses................... 188 0.41 0.75 1.09
Chicken parts....................... 490 1.40 11.88 24.93
Comminuted chicken.................. 74 0.13 1.07 1.72
Subtotal for chicken products... 752 1.94 13.71 27.74
Comminuted turkey................... 48 0.09 0.69 1.45
Import establishments............... 12 0.07 0.07 0.07
---------------------------------------------------------------------------
Total........................... ................. 2.11 14.47 29.26
----------------------------------------------------------------------------------------------------------------
\1\ Establishments may produce more than one of the products subject to these final product standards.
\2\ Costs are annualized at a 7 percent discount rate over 10 years.
Note: Numbers in table may not sum to totals due to rounding.

Lost Value to the Industry Costs
FSIS estimated the cost to industry from lost value resulting from
diverting adulterated product subject to these final product standards.
FSIS assumed that establishments would divert product after receiving
final results showing a level of Salmonella at or above 10 cfu/mL(g)
and the presence of a serotype of public health significance. As
previously mentioned, FSIS laboratories would provide results on the
level of Salmonella to establishments within two days from sample
collection and results on the presence of a serotype of public health
significance three days after initial results.
The 2023 risk assessments estimated that approximately 0.2 million
pounds of chicken carcasses, 0.07 million pounds of chicken parts, 1.6
million pounds of comminuted chicken, and 0.6 million pounds of
comminuted turkey per year would have Salmonella levels at or above 10
cfu/mL(g) and would contain a serotype of public health significance
(Table 29). This represents less than 0.1 percent of estimated
production for each of the product categories.

Table 29--Total Production, Volume Over 10 cfu/mL(g) and Containing a Serotype of Public Health Significance,
and Share of Production by Product
----------------------------------------------------------------------------------------------------------------
Volume over 10
cfu/mL(g) and
containing a
Product Total production serotype of Share of
(million pounds) public health production (%)
significance
(million pounds)
----------------------------------------------------------------------------------------------------------------
Chicken carcasses...................................... 33,238 0.2 0.000005
Chicken parts.......................................... 31,208 0.07 0.000002
Comminuted chicken..................................... 2,256 1.6 0.000691
Comminuted turkey...................................... 1,691 0.6 0.000336
----------------------------------------------------------------------------------------------------------------
Note: Numbers in table may not sum to totals due to rounding.

To estimate the cost to industry of this lost value as a result of
this proposal, FSIS applied the per pound retail price of select
poultry products to the estimated volume of lost product. FSIS used
data from 2017 to 2021 and used a range in these prices to account for
variability and uncertainty: the lowest retail price in the five-year
period as the minimum, the highest as the maximum, and the five-year
average as the medium estimate. For chicken carcasses, FSIS used the
retail price for whole fresh chicken while for chicken parts the Agency
used the retail price for chicken breasts (Table 30). Because data for
the five-year period for comminuted or ground chicken were not readily
available, FSIS used the retail price for chicken legs as a proxy. For
comminuted turkey, FSIS used data for whole frozen turkeys as data for
the five-year period for comminuted or ground turkey were not
available.

[[Page 64735]]

Table 30--Retail Prices for Select Commodities
----------------------------------------------------------------------------------------------------------------
Price per pound ($)
Product Price source --------------------------------------------------------
Low Medium High
----------------------------------------------------------------------------------------------------------------
Chicken carcasses................ Whole fresh chicken 1.36 1.51 1.75
\a\.
Chicken parts.................... Chicken breasts \b\. 2.90 3.19 3.72
Comminuted chicken............... Chicken legs \c\.... 1.32 1.50 1.73
Comminuted turkey................ Whole frozen turkey 0.80 0.99 1.23
\d\.
----------------------------------------------------------------------------------------------------------------
\a\ U.S. Bureau of Labor Statistics (BLS), Chicken, fresh, whole, per lb. (453.6 gm) in U.S. city average,
average price, not seasonally adjusted [APU0000706111], , accessed July 6, 2023, https://data.bls.gov/timeseries/APU0000706111?amp%253bdata_tool=XGtable&output_view=data&include_graphs=true.
\b\ BLS, Chicken breast, boneless, per lb. (453.6 gm) [APU0000FF1101], accessed July 6, 2023; https://data.bls.gov/timeseries/APU0000FF1101?amp%253bdata_tool=XGtable&output_view=data&include_graphs=true.
\c\ BLS, Chicken legs, bone-in, per lb. (453.6 gm) in U.S. city average, average price, not seasonally adjusted
[APU0000706212], accessed July 6, 2023, https://data.bls.gov/timeseries/APU0000706212?amp%253bdata_tool=XGtable&output_view=data&include_graphs=true.
\d\ USDA, Economic Research Service, Turkey Sector: Background & Statistics: Price Statistics, April 18, 2023,
https://www.ers.usda.gov/newsroom/trending-topics/turkey-sector-background-statistics.

Previous FSIS analyses assumed that diverted product would lose 66
percent of its value.\228\ As product under these final product
standards are raw materials that can be diverted to a variety of fully
cooked preparations, the Agency used a range to estimate the cost of
lost value to the industry. Specifically, FSIS used 34, 50, and 66
percent as the low, medium, and high estimates. FSIS estimated that the
cost to industry from diverting product is $1.7 million annually, with
a range of $1.0 to $2.6 million (Table 31). Assuming the proposed
implementation schedule and annualizing over 10 years at a 7 percent
discount rate, the cost for lost value of products subject to this
proposal is $1.5 million, ranging from $0.9 million to $2.4 million.
---------------------------------------------------------------------------

\228\ USDA, FSIS, ``Cost-Benefit Analysis for FSIS's
Implementation of Its Non-O157 STEC Testing on Beef Manufacturing
Trimmings and Expansion of Its Testing to Ground Beef and Ground
Beef Components Other Than Beef Manufacturing Trimmings,'' June
2020, https://www.fsis.usda.gov/sites/default/files/media_file/2020-07/FSIS-Non-0157-STEC-Testing-CBA-June-2020.pdf; USDA, FSIS,
``Salmonella in Certain Not-Ready-To-Eat Breaded Stuffed Chicken
Products,'' Preliminary Cost-Benefit Analysis, April 2023, https://www.fsis.usda.gov/sites/default/files/media_file/documents/NRTE_Stuffed_Chicken_CBA_FSIS-2022-0013.pdf.

Table 31--Lost Value to the Industry Costs, Million $
----------------------------------------------------------------------------------------------------------------
Product Low Medium High
----------------------------------------------------------------------------------------------------------------
Chicken carcasses...................................... 0.1 0.1 0.2
Chicken parts.......................................... 0.1 0.1 0.2
Comminuted chicken..................................... 0.7 1.2 1.8
Comminuted turkey...................................... 0.2 0.3 0.5
--------------------------------------------------------
Total.............................................. 1.0 1.7 2.6
Annualized \1\..................................... 0.9 1.5 2.4
----------------------------------------------------------------------------------------------------------------
\1\ Costs are annualized at a 7 percent discount rate over 10 years.
Note: Numbers in table may not sum to totals due to rounding.

Microbiological Sampling Plan Reassessment Costs
Establishments subject to these proposed final product standards
may incur costs associated with reassessing their sampling plans.
Current performance standards focus on the presence or absence of
Salmonella in certain poultry products. However, the proposed standards
would make product adulterated if it contains Salmonella at or above 10
cfu/mL(g) and has at least one of the serotypes of public health
significance. To estimate a cost associated with this requirement, FSIS
assumed a portion of establishments would reassess their
microbiological sampling plans. Consistent with the estimates in the
previous cost-benefit analysis for the 2016 performance standards, FSIS
estimated the cost of reassessing a sampling plan for 30, 40, and 50
percent of the establishments subject to this proposal.\229\ FSIS
included all volume categories in these estimates. However, as
previously noted in the cost-benefit analysis for the 2016 performance
standards, FSIS does not expect low and VLV establishments to have an
internal sampling plan.\230\ FSIS assumed that these establishments
would opt to not incur the expense of developing a sampling plan as
sampling does not directly contribute to pathogen reduction. The Agency
is seeking comments on this assumption.
---------------------------------------------------------------------------

\229\ USDA, FSIS, Chicken Parts and Not Ready-To-Eat Comminuted
Poultry Performance Standards, Final Cost-Benefit Analysis, February
11, 2016, https://www.fsis.usda.gov/sites/default/files/media_file/documents/FRN-related-CBA-Salmonella-Campy-2014-0023-022016.pdf.
\230\ USDA, FSIS, Chicken Parts and Not Ready-To-Eat Comminuted
Poultry Performance Standards, Final Cost-Benefit Analysis, February
11, 2016, https://www.fsis.usda.gov/sites/default/files/media_file/documents/FRN-related-CBA-Salmonella-Campy-2014-0023-022016.pdf.
---------------------------------------------------------------------------

FSIS estimated that the total cost to industry from reassessing
their sampling plans is $0.3 million, ranging from $0.1 to $0.6 million
(Table 32). Assuming the proposed implementation schedule and
annualizing over 10 years at a 7 percent discount rate, the cost for
microbiological sampling plan reassessment is $0.04 million, ranging
from $0.02 million to $0.08 million. High- and medium-volume
establishments need an average of 40 hours (ranging from 20 to 60),
while low- and very low-volume establishments need an average of 20
hours (ranging from 10 to 30) to reassess a sampling plan, according to
the 2017 Costs of Food Safety Investments in the Meat and Poultry
Slaughter

[[Page 64736]]

Industries.\231\ This publication estimated costs for large and small
establishments. FSIS assumed the large category would correspond with
high- and medium-volume establishments, while the small category would
correspond with low- and very low-volume establishments. FSIS used data
from the U.S. Bureau of Labor Statistics to update the hourly wage for
estimating these labor costs. Specifically, FSIS used the 2021 hourly
wage for a production worker of $30.78, which includes an average
hourly wage of $15.39 multiplied by a benefits and overhead factor of
two.
---------------------------------------------------------------------------

\231\ Viator CL, Muth MK, Brophy JE, Noyes G. Costs of Food
Safety Investments in the Meat and Poultry Slaughter Industries. J
Food Sci. 2017 Feb;82(2):260-269. doi: 10.1111/1750-3841.13597. Epub
2017 Jan 24. PMID: 28117890. FSIS derived the labor hours from the
total costs presented on table 5 and the wage rate for production
occupations on table 2. BLS, May 2021 National Industry-Specific
Occupational Employment and Wage Estimates for 19-1012 Food
Scientists and Technologists, accessed April 13, 2023, https://www.bls.gov/oes/current/oes191012.htm.

Table 32--Microbiological Sampling Plan Reassessment Costs
----------------------------------------------------------------------------------------------------------------
Cost (thousand $)
Establishment volume category Number of --------------------------------------------------------
establishments Low Medium High
----------------------------------------------------------------------------------------------------------------
High................................ 302 0.06 0.15 0.28
Medium.............................. 276 0.05 0.14 0.25
Low................................. 190 0.02 0.05 0.08
Very Low............................ 91 0.003 0.007 0.014
---------------------------------------------------------------------------
Total........................... ................. 0.13 0.34 0.63
Annualized \1\.................. ................. 0.02 0.04 0.08
----------------------------------------------------------------------------------------------------------------
\1\ Costs are annualized at a 7 percent discount rate over 10 years.
Note: Numbers in table may not sum to totals due to rounding.

Validation of Microbiological Sampling Plans
If an establishment makes changes to their microbiological sampling
plans in response to this proposal, they would incur costs associated
with validating these changes. The 2015 ``Costs of Food Safety
Interventions'' report indicates that high- and medium-volume
establishments would need an average of 960 labor hours for validation
of a microbiological sampling plan and 1,200 labor hours for low- and
very low-volume establishments. On a per plan basis, the cost for
validation of a microbiological sampling plan for a high- or medium-
volume establishment is $77,683, on average, while for low- or very
low-volume establishments, the average cost is $97,104. FSIS used the
2021 hourly wage for a food scientist of $80.92, which includes an
average hourly wage of $40.46 multiplied by a benefits and overhead
factor of 2.\232\ FSIS did not include an estimate of total industry
validation costs for microbiological sampling plans because FSIS does
not have data on the number of establishments that would make changes
to their plans in response to this proposal. FSIS is requesting
comments to address this data gap.
---------------------------------------------------------------------------

\232\ Viator CL, Muth MK, Brophy JE, Noyes G. Costs of Food
Safety Investments in the Meat and Poultry Slaughter Industries. J
Food Sci. 2017 Feb;82(2):260-269. doi: 10.1111/1750-3841.13597. Epub
2017 Jan 24. PMID: 28117890. FSIS derived the labor hours from the
total costs presented on table 5 and the wage rate for production
occupations on table 2. BLS, May 2021 National Industry-Specific
Occupational Employment and Wage Estimates for 19-1012 Food
Scientists and Technologists, accessed April 13, 2023, https://www.bls.gov/oes/current/oes191012.htm.
---------------------------------------------------------------------------

Corrective Actions
FSIS would require establishments that do not meet the final
product standards to take corrective actions. These corrective actions
would be aimed at removing adulterated product from market and making
changes to prevent production of adulterated product in the future.
Interventions available to the poultry industry include antimicrobial
agents, new equipment, and employee practices. FSIS does not have
information on the types or frequency of corrective actions
establishments may take in response to not meeting the final products
standards, and the Agency is seeking comments on the potential costs
associated with these.
Summary of Costs to Industry From This Proposed Rule and Proposed
Determination
FSIS estimated the main cost to industry to comply with this
proposal is $16.4 million annually, with a range of $3.3 to $32.3
million (Table 33), assuming the proposed implementation schedule and
annualizing over 10 years at a 7 percent discount rate. The principal
component of this cost is the requirement that establishments must
maintain control of product subject to FSIS verification sampling for
adulterants pending test results. The cost estimate associated with
this requirement is likely an overestimate as it is possible that
establishments' current practices and procedures would allow them to
maintain control of a lower volume of product. Additionally, all
timeframes and methods for Salmonella testing are likely to change as
FSIS continuously incorporates new laboratory technologies into its
sampling verification program. FSIS is seeking comment on these
estimates. FSIS estimated that the total costs to establishments from
reassessing HACCP and microbiological sampling plans, combined, is
$0.22 million ($0.18 + $0.04 million). The estimated cost associated
with the proposed statistical process control requirements is $0.04
million, which is likely an overestimate as certain establishments
would be able to mitigate the cost by using laboratory services
provided by FSIS, as previously described. To varying degrees, industry
may also incur other costs associated with their individual responses
to this proposal. The Agency estimated that this total cost represents
less than 1 percent of the total industry's revenue in 2021. In 2021,
the estimated total sales value for broilers and turkeys, on a live
basis, was $37.4 billion, with a five-year average between 2017 and
2021 of $33.5 billion.\233\ This value increased to $57.5 billion in
2022. For the poultry processing industry, the

[[Page 64737]]

total 2021 revenue was $77 billion, according to U.S. Census data.\234\
---------------------------------------------------------------------------

\233\ USDA, ERS, ``Poultry Sector at a Glance'' June 1, 2023,
https://www.ers.usda.gov/topics/animal-products/poultry-eggs/sector-at-a-glance/; USDA, National Agricultural Statistics Service,
``Poultry--Production and Value: 2022 Summary,'' April 2023, https://downloads.usda.library.cornell.edu/usda-esmis/files/m039k491c/wm119387d/5138kw352/plva0423.pdf.
\234\ Sales, value of shipments, or revenue for the Poultry
processing industry, as defined in the North American Industry
Classification System code 311615. U.S. Census Bureau, Annual Survey
of Manufacturers: Summary Statistics for Industry Groups and
Industries in the U.S.: 2018-2021 (NAICS 311615), accessed on April
11, 2023.

Table 33--Summary of Industry Costs
----------------------------------------------------------------------------------------------------------------
Cost (million $)
Cost descriptions -----------------------------------------------
Low Medium High
----------------------------------------------------------------------------------------------------------------
Costs associated with the proposed rule:
Statistical process control................................. 0.04 0.04 0.04
Electronic data submission.................................. 0.18 0.18 0.18
HACCP plan reassessment..................................... 0.09 0.18 0.26
Costs associated with the proposed determination:
Maintaining control of sampled product...................... 2.11 14.47 29.26
Lost value to the industry.................................. 0.87 1.52 2.43
Microbiological sampling plan reassessment.................. 0.02 0.04 0.08
-----------------------------------------------
Total \1\............................................... 3.31 16.43 32.25
----------------------------------------------------------------------------------------------------------------
\1\ Costs are annualized at a 7 percent discount rate over 10 years.
Note: Numbers in table may not sum to totals due to rounding.

FSIS estimates industry would incur annual costs in response to
this rule. Table 34 includes the expected undiscounted annual costs of
this proposal assuming the implementation schedule over a 10-year
period.

Table 34--Summary of Annual Costs Over 10 Years
----------------------------------------------------------------------------------------------------------------
Year Low Medium High
----------------------------------------------------------------------------------------------------------------
1...................................................... 2,342,792 13,490,291 27,612,367
2...................................................... 3,330,215 16,984,639 33,483,179
3...................................................... 3,250,382 16,788,952 33,160,044
4...................................................... 3,099,498 16,471,425 32,667,872
5...................................................... 3,099,498 16,469,009 32,667,872
6...................................................... 3,099,498 16,466,751 32,667,872
7...................................................... 3,099,498 16,464,641 32,667,872
8...................................................... 3,099,498 16,462,668 32,667,872
9...................................................... 3,099,498 16,460,825 32,667,872
10..................................................... 3,099,498 16,459,102 32,667,872
----------------------------------------------------------------------------------------------------------------

Costs to FSIS
FSIS does not anticipate the proposal, including using laboratory
services provided by FSIS for analyzing process control samples for VS
and VLV establishments under Traditional Inspection, as well as
conducting verification sampling for the final product standards, will
increase Agency costs. The Agency would adapt its current sampling for
Salmonella on poultry products to conduct verification sampling for the
new final product standards and would be able to shift existing
resources as necessary to implement this proposal if finalized. FSIS
currently enumerates samples collected as part of FSIS verification
sampling for Salmonella. Consequently, if this proposal is finalized,
the only additional cost to FSIS would be to incorporate serotype
testing on Salmonella positive samples. The Agency estimates analyzing
these tests would require 520 labor hours, or $0.03 million, per year
to analyze results, with additional hours, including data management,
procurement, result review and authorization, as needed.\235\
---------------------------------------------------------------------------

\235\ FSIS used the 2024 base salary of a GS-12 step 1 full time
employee of $35.67 per hour and included the Civilian Position Full
Fringe Benefit Cost Factor of 36.25 percent. Executive Office of The
President, Office of Management and Budget, Circular No. A-76
(Revised), May 29, 2003, https://www.whitehouse.gov/wp-content/uploads/legacy_drupal_files/omb/circulars/A76/a76_incl_tech_correction.pdf.
---------------------------------------------------------------------------

Costs related to follow-up sampling and conducting FSAs are not
expected to increase. The Agency would conduct follow up sampling and a
PHRE for any establishments that does not meet the final product
standards. FSIS would use the results of the PHRE to determine the need
for an FSA. FSIS currently conducts follow up sampling and PHREs on
establishments that do not meet the current Salmonella performance
standards. For instance, in 2022, FSIS conducted 30 FSAs at category
three establishments. The Agency estimated that the average cost to
conduct a for-cause FSA in 2016 was about $4,800, which, inflated to
2021 dollars, is about $5,400 per FSA.\236\
---------------------------------------------------------------------------

\236\ Based on the FSIS Office of the Chief Financial Officer
(OCFO) preliminary analysis of the average cost per FSA under the
new FSA methodology, FY 2016. The costs were inflated, by using the
2021 BLS Consumer Price Index (CPI) All items in U.S. city average,
all urban consumers, not seasonally adjusted (CUUR0000SA0,
CUUS0000SA0 Not Seasonally Adjusted).
---------------------------------------------------------------------------

Potential Benefits and Avoided Costs From the Proposed Rule and
Proposed Determination
Prevented Salmonella Illnesses
FSIS is proposing to declare Salmonella at or above 10 cfu/mL(g)
and containing a serotype of public health significance an adulterant
on chicken carcasses, chicken parts, comminuted chicken, and comminuted
turkey as final products that would enter commerce. The 2023 risk
assessments provide a range of data on the public health impacts
achieved by reducing

[[Page 64738]]

final product contaminated with Salmonella, as well as the higher risk
per serving associated with product that would be declared adulterated
by the proposal. FSIS used this range of data to estimate the potential
public health benefits of this proposal. FSIS also used findings from
the FSIS risk profile to create these estimates, including information
regarding the higher virulence of certain Salmonella serotypes, as well
as the potential debilitating human health outcomes from Salmonella
infection (e.g., reactive arthritis), which are not included in the
cost of illness estimates.
The 2023 risk assessments estimated the number of illnesses that
could be prevented if product lots with results at or above 10 cfu/
mL(g) of Salmonella are diverted from commerce as part of FSIS
verification sampling programs. For chicken carcasses, the 2023 chicken
risk assessment estimated that 1,000 illnesses could be prevented,
while for chicken parts and comminuted chicken it estimated 200 and
1,000 illnesses, respectively. The 2023 chicken risk assessment
assessed the effect of a carcass final product standard on all chicken
associated illnesses, including those from parts and comminuted product
consumption, but could not assess the effect of carcasses and secondary
products standards sequentially. As such, the 2023 chicken risk
assessment estimates for chicken products are not additive.\237\ For
comminuted turkey, the 2023 turkey risk assessment estimated that 2,100
illnesses could be prevented.\238\ This analysis presents three
illustrative scenarios based on these results.
---------------------------------------------------------------------------

\237\ USDA, FSIS, ``Quantitative Microbiological Risk Assessment
for Salmonella in Raw Chicken and Raw Chicken Products,'' January
2023 at: https://www.regulations.gov/docket/FSIS-2023-0028.
\238\ USDA, FSIS, ``Quantitative Microbiological Risk Assessment
for Salmonella in Raw Turkey and Raw Turkey Products,'' January 2023
at: https://www.regulations.gov/docket/FSIS-2023-0028.
---------------------------------------------------------------------------

FSIS estimated that if this proposal becomes final, the number of
illnesses prevented may range from 765 to 4,300 cases per year (Table
34).\239\ These estimates are based on the best data currently
available.
---------------------------------------------------------------------------

\239\ FSIS used these estimates for calculating the monetary
benefits associated with this proposal given the higher risk per
serving and probability of illness associated with serotypes of
public health significance. Thus, while the amount of product with
results at or above 10 cfu/mL(g) that is diverted is higher, the
number of prevented illnesses is potentially a representative
scenario of the total benefits associated with this rule.
---------------------------------------------------------------------------

For the low estimate, the Agency used sampling data and results
from the 2023 risk assessments to estimate the number of prevented
illnesses from the final products standards. FSIS sampling data show
that the serotypes of public health significance identified in this
proposal are present in 24 percent of the chicken carcass samples and
25 percent of the comminuted turkey samples.\240\ The Agency applied
the share of samples with at least one serotype of public health
significance to the estimated number of prevented illnesses from
diverting chicken carcasses and comminuted turkey with results at or
above 10 cfu/mL(g). Thus, for the low estimate in this analysis, the
Agency estimated that the final product standards would prevent a total
of 765 Salmonella illnesses, 240 from chicken carcasses and 525 from
comminuted turkey. Research indicates that chicken carcass samples
often contain multiple Salmonella serotypes.\241\ For example, it is
likely that a sample from a chicken carcass could test positive for
Salmonella Kentucky and also contain Salmonella Enteritidis, which is a
serotype of public health significance, but Salmonella Enteritidis was
not captured by FSIS testing on that sample. At present there is no
rapid way to screen for multiple Salmonella serotypes at one time.
Moreover, the 2023 chicken risk assessment estimated that diverting
from commerce chicken carcasses containing serotypes in the higher
virulence cluster would result in 1,800 prevented illnesses, which is
higher than the estimated number of illnesses prevented from diverting
carcasses with Salmonella at or above 10 cfu/mL (1,000 illnesses).\242\
Additionally, FSIS data show that serotypes of public health
significance have been detected at higher rates in chicken parts and
comminuted chicken products.\243\ Further, the serotypes of public
health significance have been identified in over 50 percent of the
outbreaks associated with chicken products between 2012 and 2021. FSIS
is seeking comments on these assumptions and estimates. While the
estimates in the 2023 risk assessments refer to Salmonella levels and
serotypes separately, the data indicate that the number of illnesses
prevented by the final product standards in this proposal is higher
than the low estimate included in this analysis.
---------------------------------------------------------------------------

\240\ FSIS used only the prevented illness estimates for chicken
carcasses as the 2023 chicken risk assessment could not assess the
effect of carcasses and secondary products standards sequentially.
USDA, FSIS, ``Quantitative Microbiological Risk Assessment for
Salmonella in Raw Chicken and Raw Chicken Products,'' January 2023
at: https://www.regulations.gov/docket/FSIS-2023-0028.
\241\ USDA, FSIS, ``Quantitative Microbiological Risk Assessment
for Salmonella in Raw Chicken and Raw Chicken Products,'' January
2023 at: https://www.regulations.gov/docket/FSIS-2023-0028; Obe, T.,
Siceloff, A.T., Crowe, M.G., Scott, H.M., & Shariat, N.W. (2023).
Combined Quantification and Deep Serotyping for Salmonella Risk
Profiling in Broiler Flocks. Applied and Environmental Microbiology,
899(4), e02035-02022. https://doi.org/10.1128/aem.02035-22;
Thompson, C.P., Doak, A.N., Amirani, N., Schroeder, E.A., Wright,
J., Kariyawasam, S., Lamendella, R., & Shariat, N.W. (2018). High-
Resolution Identification of Multiple Salmonella Serovars in a
Single Sample by Using CRISPR-SeroSeq. Applied and Environmental
Microbiology, 84(21), e01859-18.
\242\ These estimates are not available for chicken parts,
comminuted chicken, or comminuted turkey products.
\243\ The serotypes of public health significance have been
identified in FSIS sampling programs for poultry products at varying
rates between 2016 and 2021: 24 percent of chicken carcass samples,
33 percent of chicken parts samples, 29 percent of comminuted
chicken samples, and 25 percent of comminuted turkey samples. USDA,
FSIS, ``Quantitative Microbiological Risk Assessment for Salmonella
in Raw Chicken and Raw Chicken Products,'' January 2023 at: https://www.regulations.gov/docket/FSIS-2023-0028; USDA, FSIS,
``Quantitative Microbiological Risk Assessment for Salmonella in Raw
Turkey and Raw Turkey Products,'' January 2023 at: https://www.regulations.gov/docket/FSIS-2023-0028.
---------------------------------------------------------------------------

For the medium estimate, FSIS used the 2023 risk assessments
results of illnesses prevented from diverting chicken carcasses (1,000
illnesses) and comminuted turkey (2,100 illnesses) with Salmonella
levels at or above 10 cfu/mL(g). This estimate accounts for some of the
uncertainty around potential health benefits from this proposal. The
Agency used this because as discussed above, products with Salmonella
at or above 10 cfu/mL(g) have a higher risk per serving than other
products and would be more likely to cause illness. Specifically, the
2023 chicken risk assessment noted that the probability of illness for
a serving that tests at or above 10 cfu/mL(g) and has a serotype of
public health significance is 2,000-fold higher than the average across
all servings for carcass lots, 1,100-fold higher than the average
serving for chicken parts, and 590-fold higher than the average serving
for comminuted chicken products. In contrast, the probability of
illness per serving for lots with Salmonella at 0.03 cfu/mL(g), which
is the current screening limit of detection for carcasses and parts is
at least 14-fold higher than for average lots. The probability of
illness per serving for comminuted chicken lots with Salmonella at 0.03
cfu/mL(g), which is the current screening limit of detection, is at
least 160-fold higher than for average lots. Research shows that it is
likely that the share of product samples with serotypes of public
health significance is higher than current estimates indicate, and this
share varies between product subject to this proposal (24 percent for
chicken

[[Page 64739]]

carcasses, 33 percent for chicken parts, 29 percent for comminuted
chicken, and 25 percent for comminuted turkey). Furthermore, industry
may react to this proposal in a variety of ways. For example, while the
assumptions in the cost estimates reflect the requirement of
maintaining control of product until adulteration results are
available, some establishments may opt to divert chicken carcasses,
chicken parts, comminuted chicken, and comminuted turkey products with
test results at or above 10 cfu/mL(g) instead of waiting until results
on the adulteration status of the product is available. For these
reasons, FSIS estimates that the number of prevented illnesses from
diverting chicken carcasses at or above 10 cfu/mL better approximates a
portion of the illnesses not included in the low estimate as the Agency
estimates that diverting these products from commerce would lead to a
greater reduction in illnesses. Additionally, this proposal clarifies
process control requirements, and encourages establishments to adopt
pre-harvest measures, which may have compounding effects on reducing
cross-contamination and may prevent a higher number of illnesses each
year.
For the high estimate, FSIS used the combined estimated number of
prevented illnesses from diverting chicken carcasses (1,000 illnesses),
chicken parts (200 illnesses), comminuted chicken (1,000 illnesses),
and comminuted turkey (2,100 illnesses) product from the 2023 risk
assessments. As noted above, the prevented illness estimates in the
2023 risk assessments reflect a standard at the 10 cfu/mL(g) level for
these products. While these estimates do not reflect the final products
standards in this proposal, FSIS is including these as a high estimate
for the reasons outlined above. For the low and medium estimates, FSIS
used only the prevented illness estimates for chicken carcasses as the
2023 chicken risk assessment could not assess the effect of carcasses
and secondary products (parts and comminuted chicken) standards
sequentially, as mentioned above. In contrast, for the high estimate,
FSIS used the sum of all three estimates (chicken carcasses, chicken
parts, and comminuted chicken) to illustrate a potential number of
illnesses prevented from implementing this proposed policy, including
the potential compounding benefits across product types and the upper
limit of direct and indirect (i.e., benefits from actions industry
voluntarily takes in response to this proposal) health benefits. The
Agency used the same estimate for comminuted turkey for the medium and
high estimates. FSIS is seeking comments on these estimates.

Table 34--Estimated Number of Illnesses Prevented by Product
----------------------------------------------------------------------------------------------------------------
Prevented illnesses
Product --------------------------------------------------------
Low Medium High
----------------------------------------------------------------------------------------------------------------
Chicken products:...................................... 240 1,000 2,200
Chicken carcasses.................................. 240 1,000 1,000
Chicken parts...................................... ................. ................. 200
Comminuted chicken................................. ................. ................. 1,000
Comminuted turkey...................................... 525 2,100 2,100
--------------------------------------------------------
Total.............................................. 765 3,100 4,300
----------------------------------------------------------------------------------------------------------------

Public health benefits, including in the form of prevented
illnesses, are difficult to monetize as a market for these does not
exist. Typically, economic analyses use alternative methods for these
non-market measures that approximate the value of these benefits. To
monetize the estimated direct public health impact of this proposal,
and consistent with other Agency regulatory impact analyses,\244\ FSIS
applied the estimated cost of a Salmonella illness to the estimated
number of prevented illnesses. FSIS used the ``Cost Estimates of
Foodborne Illnesses'' developed by the U.S. Department of Agriculture,
Economic Research Service to do so.\245\ These estimates incorporate
associated expenditures on medical care, lost wages due to productivity
loss, and estimates of willingness to pay (WTP) to reduce
mortality.\246\ This WTP measure is estimated in the form of the value
of a statistical life. The average per case cost for Salmonella in 2021
dollars was $4,351, with a lower bound estimate of $387 and a higher
bound estimate of $6,873. The variability in the cost estimate is
driven by variations in the number of fatalities, which are zero at the
low estimate and 378 at the high estimate.
---------------------------------------------------------------------------

\244\ USDA, FSIS, ``Salmonella in Certain Not-Ready-To-Eat
Breaded Stuffed Chicken Products,'' Preliminary Cost-Benefit
Analysis, April 2023, https://www.fsis.usda.gov/sites/default/files/media_file/documents/NRTE_Stuffed_Chicken_CBA_FSIS-2022-0013.pdf.
USDA, FSIS, ``Proposed Performance Standards for Salmonella in Raw
Comminuted Pork and Intact or Non-Intact Pork Cuts,'' Preliminary
Cost-Benefit Analysis, February 16, 2022, https://www.fsis.usda.gov/sites/default/files/media_file/2022-02/Pork-Salmonella-Performance-Standards-Cost-Benefit-Analysis.pdf; USDA, FSIS, Chicken Parts and
Not Ready-To-Eat Comminuted Poultry Performance Standards, Final
Cost-Benefit Analysis, February 11, 2016, https://www.fsis.usda.gov/sites/default/files/media_file/documents/FRN-related-CBA-Salmonella-Campy-2014-0023-022016.pdf.
\245\ USDA, ERS, ``Cost Estimates of Foodborne Illnesses,'' Cost
of foodborne illness estimates for Salmonella (non-typhoidal)
dataset, January 29, 2021 https://www.ers.usda.gov/data-products/cost-estimates-of-foodborne-illnesses.aspx.
\246\ This is incorporated through value of a statistical life
estimates that are applied to mortality associated with each
pathogen for which estimates were developed.
---------------------------------------------------------------------------

FSIS estimated the total benefits from prevented illness for this
proposal at $13.49 million ([1,000 prevented illnesses from chicken
products + 2,100 prevented illnesses from comminuted turkey products] x
$4,351), with a range from $0.3 million to $29.55 million (Table 35).
Assuming the proposed implementation schedule and annualizing over 10
years at a 7 percent discount rate, the benefits associated with the
estimated prevented illnesses are $12.92 million, ranging from $0.28
million to $28.66 million.

[[Page 64740]]

Table 35--Estimated Benefits From Prevented Illnesses for Each Product Group
----------------------------------------------------------------------------------------------------------------
Benefits (million $)
Product group --------------------------------------------------------
Low Medium High
----------------------------------------------------------------------------------------------------------------
Chicken products....................................... 0.09 4.35 15.12
Comminuted turkey...................................... 0.20 9.14 14.43
--------------------------------------------------------
Total.............................................. 0.30 13.49 29.55
Annualized \1\..................................... 0.28 12.92 28.66
----------------------------------------------------------------------------------------------------------------
\1\ Costs are annualized at a 7 percent discount rate over 10 years.
Note: Numbers in table may not sum to totals due to rounding.

The cost estimate of foodborne illness for Salmonella cases is
likely an underestimate of the total economic burden of foodborne
illness. Specifically, cost of illness estimates account for major
costs of medical treatment, time lost to illness, and individuals' WTP
to reduce risk of death but these do not include other components of
individual's WTP (to reduce illness, pain and suffering or costs
associated with potential severe, debilitating human health
outcomes).\247\ According to the FSIS Risk Profile, Salmonella subtypes
of concern can cause severe human health outcomes, including acute
gastroenteritis, bacteremia (bacteria in the blood), and focal
infections. Salmonella infections can also lead to debilitating human
health outcomes in a subset of patients, which includes reactive
arthritis, cancer, inflammatory bowel disease, and irritable bowel
syndrome, which are not included in these estimates. The FSIS Risk
Profile notes that 5.8 percent of Salmonella cases develop reactive
arthritis, and about 66 percent had persistent symptoms five years
after becoming infected with Salmonella. Additionally, about 3.3
percent of cases developed irritable bowel syndrome. Salmonella
infection can also increase the risk of colon cancer.\248\
---------------------------------------------------------------------------

\247\ Hoffmann, Sandra, Bryan Maculloch, and Michael Batz.
Economic Burden of Major Foodborne Illnesses Acquired in the United
States, EIB-140, U.S. Department of Agriculture, Economic Research
Service, May 2015, p.3-5.
\248\ USDA, FSIS, ``Risk Profile for Pathogenic Salmonella
Subtypes in Poultry,'' February 28, 2023 at: https://www.regulations.gov/docket/FSIS-2023-0028.
---------------------------------------------------------------------------

Salmonella infections can result in a variety of outcomes and for
some serotypes a small number of bacteria can cause illness.\249\ The
2023 risk assessments estimated a higher proportion of deaths among the
serotypes identified as higher virulence, including some identified by
FSIS as part of this proposal. For all Salmonella, the domestic
foodborne hospitalization rate is about 2 percent, and the fatality
rate is about 0.04 percent. In contrast, the FSIS risk profile noted
that, for a subset of Salmonella serotypes, the hospitalization rate
was 22.8 percent, and the fatality rate was 0.5 percent.\250\
Salmonella illnesses disproportionately impact children under five
years old and adults over 65, who experience higher rates of illnesses
and death.\251\ The FSIS risk profile notes that children under 1 year
of age are particularly susceptible to invasive disease and infants
have a higher likelihood of bacteremia resulting from Salmonella
illness compared with adults.
---------------------------------------------------------------------------

\249\ USDA, FSIS, ``Risk Profile for Pathogenic Salmonella
Subtypes in Poultry,'' February 28, 2023 at: https://www.regulations.gov/docket/FSIS-2023-0028.
\250\ USDA, FSIS, ``Risk Profile for Pathogenic Salmonella
Subtypes in Poultry,'' February 28, 2023 at: https://www.regulations.gov/docket/FSIS-2023-0028.
\251\ CDC, FoodNet Fast, Pathogen Surveillance, October 8, 2022,
https://wwwn.cdc.gov/foodnetfast/ foodnetfast/.
---------------------------------------------------------------------------

Costs Avoided From Prevented Outbreak-Related Recalls
FSIS estimates that this proposal would result in prevented
outbreak-related recalls. Specifically, by diverting adulterated
products entering commerce, should this rule become final, official
establishments would likely have a reduction in the risk of recalls due
to Salmonella illness outbreaks. FSIS assumed that, if finalized, this
proposal would prevent one to three recalls over a 10-year period, as
described below.
Recalls are companies' actions to remove product that may be
adulterated or misbranded from commerce.\252\ Companies recall products
due to a variety of reasons, including due to illness outbreaks. For
instance, between 2012 and 2021 there were 7 recalls due to Salmonella
outbreaks linked to various poultry products.\253\ In that same period,
there were 100 outbreaks linked to Salmonella in poultry products.\254\
While not all outbreaks lead to product recalls, poultry establishments
face the risk of recalling product that may result in human illnesses.
As previously mentioned, product that would be adulterated under this
proposal (i.e., with Salmonella levels at or above 10 cfu/mL(g) and
containing a serotype of public health significance) have a higher risk
per serving and hence a higher probability of resulting in illnesses.
---------------------------------------------------------------------------

\252\ USDA, FSIS, ``Managing Adulterated or Misbranded Meat,
Poultry, and Egg Products--Revision 8,'' December 19, 2023, https://www.fsis.usda.gov/policy/fsis-directives/8080.1.
\253\ This excludes recalls associated with raw stuffed and
breaded chicken products. USDA, FSIS, ``Recalls and Public Health
Alerts,'' accessed July 10, 2023, https://www.fsis.usda.gov/recalls.
\254\ USDA, FSIS, ``Risk Profile for Pathogenic Salmonella
Subtypes in Poultry,'' February 28, 2023 at: https://www.regulations.gov/docket/FSIS-2023-0028.
---------------------------------------------------------------------------

Poultry establishments have economic incentives to prevent recalls,
which are costly to industry and have spillover effects beyond the
product lot that is subject to it. Recalls have a direct cost for
establishments in the form of lost profits, product retrieval and
disposal costs, business interruptions, and customer reimbursement,
among others. Additional indirect costs are also part of the economic
impact of a food recall, including external costs to distributors,
wholesalers, and retailers, among others, which have been estimated to
be 51, 6, and 5 percent of the total cost of a recall for
manufacturers, wholesalers, and retailers, respectively.\255\ These
include lost sales as consumers purchase alternative brands or
products, potential litigation and liability risk, and brand damage
affecting non-recalled product of the same brand. The exact cost of a
recall varies depending on factors such as company size, product
volume, and geographic distribution of the recalled product, among
others. For publicly traded companies, recalls could reduce the

[[Page 64741]]

stock market prices of the implicated companies and could lead them to
bankruptcy and business closure. Recalls also negatively impact
consumers by creating anxiety and time-consuming inconveniences, which
includes looking for recall information, checking the products
purchased, and returning or disposing of products identified by the
recalls.
---------------------------------------------------------------------------

\255\ U.S. Department of Health and Human Services, Food and
Drug Administration (FDA), ``Requirement for Additional Traceability
Records for Certain Foods Final Regulatory Impact Analysis''
November 21, 2022, https://www.fda.gov/media/163155/download?attachment; FDA, ``Requirements for Tobacco Product
Manufacturing Practice (Proposed Rule) Preliminary Regulatory Impact
Analysis,'' March 10, 2023, https://www.fda.gov/media/166055/download?attachment.
---------------------------------------------------------------------------

Individual establishments may not currently effectively control for
Salmonella to further reduce their risk due to the perceived low risk
of a recall. For instance, the 7 recalls between 2014 and 2021 were
linked to different establishments. Further, an individual
establishment may experience pressure to underinvest in food safety
measures given uncertainty over how much other establishments may
invest in food safety measures and a need to maintain cost
competitiveness. Since consumers are unable to distinguish between
products in the marketplace that have higher probabilities of resulting
in Salmonella illness and those with lower probabilities, both types of
products are sold at the same price point. Under such market
conditions, establishments are disincentivized from investing in food
safety measures and controlling for Salmonella. This results in an
increased risk of Salmonella illnesses, and, in consequence, an
increased risk of outbreaks and outbreak-related recalls for
establishments.
If this proposal is finalized, establishments producing chicken
carcasses, chicken parts, comminuted chicken, and comminuted turkey
products would have the same incentives for controlling for Salmonella.
Consequently, establishments producing these products would have a
lower risk of recalls due to Salmonella illnesses and outbreaks.
Establishments that invest in food safety controls would benefit from
having a clear standard where product that would be adulterated would
be diverted from commerce. Diverting adulterated product from commerce
would equally reduce the probability of recalls for all FSIS regulated
establishments, serving as insurance against this risk. While this
would benefit establishments of all sizes, the benefit may be more
pronounced for low and very low volume establishments, for which the
burden of a recall may be higher. As the proposal would reduce the
probability that all regulated establishments incur costs associated
with product recalls, the Agency is approximating this quantitative
benefit by estimating the avoided cost of outbreak-related recalls.
(See discussion above, about recalls leading to external costs,
including to wholesalers and distributors.)
FSIS estimated that one outbreak-related recall may cost the U.S.
poultry industry about $31.3 million in 2021 dollars.\256\ While the
cost of a recall varies depending on multiple factors, recalls due to
illness outbreaks (class I) are a significant event for producers and
are likely more costly than other types of recalls.\257\ The 2023 risk
assessments estimated that annually roughly 8 lots of chicken carcasses
(0.7), chicken parts (0.2), comminuted chicken (5), and comminuted
turkey (2) would be diverted as a result of this proposal.\258\ This
equals roughly 80 lots of adulterated products diverted in 10 years.
FSIS estimates it is likely that at least a portion of these diverted
lots would have otherwise led to outbreaks and, consequently, recalls.
As mentioned above, data indicate that industry has conducted recalls
for about 7 percent of the outbreaks in the last 10 years (7 recalls in
100 outbreaks). Considering these products have a higher probability of
resulting in illnesses and could have led to Salmonella outbreaks, if 7
percent of them led to recalls, this would have resulted in 5.6 recalls
over 10 years. To illustrate the avoided cost from a reduction in the
risk of outbreak-related recalls, FSIS assumed that this proposal would
prevent two recalls (medium estimate), with a range of one (low
estimate) to three (high estimate) recalls in a 10-year period. This is
roughly 2.5 percent of the diverted lots, ranging from 1.3 percent to
3.8 percent. The estimated benefits from preventing recalls as part of
this proposal is $7.6 million, ranging from $4.2 million to $10.3
million, annualized over 10 years at a 7 percent discount rate.
---------------------------------------------------------------------------

\256\ This estimate is derived from a report by the Consumers
Brands Association that surveyed 36 food, beverage, and consumer
products companies that have faced a recall in the previous five
years to derive these estimates. Based on the report, FSIS estimated
the cost of an outbreak related recall at $25.8 million in 2011
dollars. The Agency adjusted this estimate for inflation using the
consumer price index. Consumers Brands Association, ``Capturing
Recall Costs: Measuring and Recovering the Losses,'' 2011, https://globalfoodsafetyresource.com/wp-content/uploads/2014/08/www.gmaonline.org_file-manager_images_gmapublications_Capturing_Recall_Costs_GMA_Whitepaper_FINAL.pdf; BLS, Consumer Price Index, All items in U.S. city
average, all urban consumers, not seasonally adjusted (CUUR0000SA0,
CUUS0000SA0 Not Seasonally Adjusted).
\257\ FSIS uses a classification system for recalls. Class I
recalls are a health hazard situation where there is a reasonable
probability that the use of the product will cause serious, adverse
health consequences or death. Class II recalls are those with a
remote probability that the product will cause adverse health
consequences, while Class III recalls are situations where the
product will not cause adverse health consequences. USDA, FSIS,
``Managing Adulterated or Misbranded Meat, Poultry, and Egg
Products--Revision 8,'' December 19, 2023, https://www.fsis.usda.gov/policy/fsis-directives/8080.1.
\258\ USDA, FSIS, ``Quantitative Microbiological Risk Assessment
for Salmonella in Raw Chicken and Raw Chicken Products,'' January
2023; USDA, FSIS, ``Quantitative Microbiological Risk Assessment for
Salmonella in Raw Turkey and Raw Turkey Products,'' January 2023 at:
https://www.regulations.gov/docket/FSIS-2023-0028.
---------------------------------------------------------------------------

Summary of Costs and Benefits
FSIS estimated this proposal would have a net benefit of $4.1
million per year, ranging from $1.1 million to $6.7 million, assuming
the proposed implementation schedule and annualizing over 10 years at a
7 percent discount rate (Table 35).
This proposal is estimated to cost industry $16.4 million per year,
ranging from $3.3 to $32.3 million, assuming the proposed
implementation schedule and annualizing over 10 years at a 7 percent
discount rate. The majority of this cost, $14.5 million, ranging from
$2.1 million to $29.3 million, is associated with requiring
establishments to maintain control of sampled product pending test
results, followed by industry cost due to lost product value of $1.5
million, ranging from $0.9 million to $2.4 million. Industry may also
incur costs associated with HACCP and microbiological sampling plan
reassessments and changes to MMPs for process control. To varying
degrees, industry may also incur other costs associated with their
individual responses to this proposal.
In terms of benefits, this proposal is estimated to result in
benefits to society of $20.5 million per year, ranging from $4.4
million to $39.0 million (Table 36), assuming the proposed
implementation schedule and annualizing over 10 years at a 7 percent
discount rate. The majority of the benefits are derived from prevented
illnesses of $12.9 million per year, ranging from $0.3 to $28.7
million. Additional benefits from this proposal include the reduction
in the risk of outbreak-related recalls for products subject to these
final product standards, which represent an estimated $7.6 million in
benefits to industry, ranging from $4.2 million to $10.3 million.
Moreover, industry might take additional actions in response to this
proposal, which may lead to additional benefits. For example, producers
may adopt testing programs, process control measures, or pre-harvest
measures that may result in additional benefits from this proposal.

[[Page 64742]]

Table 36--Summary of Costs and Benefits
----------------------------------------------------------------------------------------------------------------
Total (million $)
Description -----------------------------------------------
Low Medium High
----------------------------------------------------------------------------------------------------------------
Costs
----------------------------------------------------------------------------------------------------------------
Costs associated with the proposed rule:
Statistical Process Control................................. 0.04 0.04 0.04
Electronic data submission.................................. 0.18 0.18 0.18
HACCP plan reassessment..................................... 0.09 0.18 0.26
Costs associated with the proposed determination:
Maintaining control of sampled product...................... 2.11 14.47 29.26
Lost value to the industry.................................. 0.87 1.52 2.43
Microbiological sampling plan reassessment.................. 0.02 0.04 0.08
-----------------------------------------------
Total costs............................................. 3.31 16.43 32.25
----------------------------------------------------------------------------------------------------------------
Benefits
----------------------------------------------------------------------------------------------------------------
Prevented illnesses from adulterated chicken products........... 0.09 4.35 15.11
Prevented illnesses from adulterated comminuted turkey.......... 0.19 8.58 13.55
Avoided cost from prevented outbreak-related recalls............ 4.16 7.56 10.34
-----------------------------------------------
Total benefits.............................................. 4.45 20.49 39.00
Net benefits............................................ 1.14 4.06 6.75
----------------------------------------------------------------------------------------------------------------
Note: All costs and benefits are annualized over 10 years at a 7 percent discount rate. Numbers in table may not
sum to totals due to rounding.

This regulatory impact analysis provides potential cost and
benefits scenarios. As discussed in the Potential benefits and avoided
costs from the proposed rule and proposed determination section,
establishments may elect to divert product before final adulteration
results are available to them. To also illustrate this possibility,
FSIS estimated the potential costs associated with establishments
diverting product with test results at or above 10 cfu/mL(g) before a
serotype of public health significance is detected. This would likely
increase industry cost by $3.6 million, ranging from $2.1 million to
$5.7 million. This range is associated with changes to the cost of
maintaining control of sampled product, which would decrease, while the
lost value to industry from diverting product would likely increase.
While FSIS did not incorporate these into the main scenarios presented
in this regulatory impact analysis, the net benefit from industry
diverting product that tests at or above 10 cfu would be $0.5 million,
ranging from a net cost of $0.9 million to a net benefit of $1.0
million and keeping all other assumptions constant.\259\
---------------------------------------------------------------------------

\259\ In this scenario, the low bound in the net benefits
estimate reflects the adjustment in illnesses made in the Expected
benefits section to account for the share of product that is likely
to be at or above 10 cfu/mL(g) and contain a serotype of public
health significance. Hence, the net cost would be lower than $0.9
million.
---------------------------------------------------------------------------

FSIS compared the respective low, medium, and high costs and
benefits estimates as the Agency's primary estimates to summarize the
potential economic outcomes of this proposal. However, each of the cost
scenarios in this analysis could result in any of the benefit scenarios
also previously discussed. As such, when considering a wider range for
these scenarios, FSIS estimated this proposal would have a net benefit
of $4.1 million per year, ranging from -$31.9 million to $35.7 million,
assuming the proposed implementation schedule and annualizing over 10
years at a 7 percent discount rate.
Alternative Regulatory Approaches
FSIS considered the following five alternatives in the analysis for
this proposal (Table 37). To evaluate potential alternatives, FSIS
first analyzed the costs and benefits associated with taking no
regulatory action, which is discussed under Alternative 1 and
represents the baseline for this analysis. Alternative 2 discusses the
proposal. For Alternative 3, which is a more stringent regulatory
scenario, FSIS estimated the costs and benefits associated with
declaring adulterated chicken carcasses, chicken parts, comminuted
chicken, and comminuted turkey with levels of Salmonella at or above 1
cfu/mL(g) and containing a serotype of public health significance.
Alternative 4 represents a more lenient regulatory scenario by
estimating costs and benefits associated with declaring these products
adulterated with Salmonella levels at or above 100 cfu/mL(g) and
containing a serotype of public health significance. Finally,
Alternative 5 represents the most stringent scenario considered and
estimates the benefits and costs associated with declaring chicken
carcasses, chicken parts, comminuted chicken, and comminuted turkey
with Salmonella at or above 1 cfu/mL(g) adulterated regardless of
serotype. For each alternative, the Agency assumed that all other
costs, specifically those associated with process control requirements
(collecting an additional sample and electronic data submission), as
well as HACCP and microbiological sampling plan reassessments, would
remain equal. Similarly, the Agency assumed that the benefits from
preventing outbreak-related recalls would be the same for each
alternative.

[[Page 64743]]

Table 37--Regulatory Alternatives
----------------------------------------------------------------------------------------------------------------
Benefits (medium estimate) Net (medium
Alternative \1\ Costs (medium estimate) \2\ estimate)
----------------------------------------------------------------------------------------------------------------
1: No regulatory action (Baseline) Continued illnesses and No new costs to industry.. n/a.
deaths associated with
Salmonella from these
products.
2: The proposed rule and proposed $16.43 million compared to $20.49 million from $4.06 million.
determination. the baseline. prevented Salmonella
illnesses and outbreak-
related recalls.
3: The proposed rule and proposed $29.52 million compared to $19.65 million from ($9.88) million.
determination with a lower level the baseline. prevented Salmonella
for adulterated product (1 cfu/ illnesses and outbreak-
mL(g) and serotypes of public related recalls.
health significance).
4: The proposed rule and proposed $15.34 million compared to $8.85 million in the form ($6.59 million).
determination with a higher level the baseline. of prevented Salmonella
for adulterated product (100 cfu/ illnesses and outbreak-
mL(g) and serotypes of public related recalls.
health significance).
5: The proposed rule and proposed $49.96 million compared to $34.50 million from ($15.45 million).
determination with a lower the baseline. prevented Salmonella
contamination level for illnesses and outbreak-
adulterated product of 1 cfu/ related recalls.
mL(g) Salmonella regardless of
serotype.
----------------------------------------------------------------------------------------------------------------
\1\ Costs and benefits are annualized at a 7 percent discount rate over 10 years.
\2\ Alternatives 2-5 have additional potential benefits from reduced risk of outbreak-related recalls and
increased consumer trust.
Note: Numbers in table may not sum to totals due to rounding.

Alternative 1: No regulatory action (Baseline).
FSIS considered keeping the current performance standards for
Salmonella in poultry products and taking no regulatory action. This
alternative would prevent society from realizing benefits in the form
of prevented illnesses due to Salmonella contamination. While this
alternative would not impose costs on industry from maintaining control
of sampled product or lost value due to diverted product, the Agency
would fail to address the increased probability of illness resulting
from chicken carcasses, chicken parts, comminuted chicken, and
comminuted turkey that contain Salmonella at or above 10 cfu/mL(g) and
a serotype of public health significance. FSIS would also fail to
clarify process control requirements for poultry slaughter
establishments. Therefore, the Agency rejects this alternative.
Alternative 2: The proposed rule and proposed determination.
Under this proposal, chicken carcasses and parts and comminuted
chicken and turkey products which are final products that will enter
commerce that test at or above 10 cfu/mL(g) and contain a Salmonella
serotype of public health significance would be adulterated. FSIS would
also clarify process control requirements for poultry slaughter
establishments, require that VLV and VS establishments operating under
Traditional Inspection collect and analyze an additional sample for
process control monitoring, and require all establishments
electronically submit process control data. Society would benefit from
this proposal as FSIS estimated that between 765 and 4,300 Salmonella
illnesses could be prevented each year. This represents between 0.5 and
3 percent of the total number of Salmonella illnesses attributed to
products subject to this proposal.\260\ Additionally, industry would
benefit from a reduced risk of outbreak-related recalls. This is the
Agency's preferred alternative.
---------------------------------------------------------------------------

\260\ According to the 2023 risk assessments, there are 125,000
and 18,000 Salmonella illnesses attributed to products subject to
this proposed rule each year. USDA, FSIS, ``Quantitative
Microbiological Risk Assessment for Salmonella in Raw Chicken and
Raw Chicken Products,'' January 2023 at: https://www.regulations.gov/docket/FSIS-2023-0028; USDA, FSIS,
``Quantitative Microbiological Risk Assessment for Salmonella in Raw
Turkey and Raw Turkey Products,'' January 2023 at: https://www.regulations.gov/docket/FSIS-2023-0028.
---------------------------------------------------------------------------

Alternative 3: The proposed rule and proposed determination with a
lower contamination level for adulterated product of 1 cfu/mL(g) and
serotypes of public health significance.
Alternative 3 would consider product under this proposal to be
adulterated if it contains 1 cfu/mL(g) and a Salmonella serotype of
public health significance. This alternative results in higher costs
for industry to comply with the proposal, resulting from the increased
volume of lost product that is diverted ($14.48 million, ranging from
$8.29 million to $21.08 million). Alternative 3 also presents higher
benefits from prevented Salmonella illnesses, which range from 1,214 to
7,750. This represents between 0.8 and 5.4 percent of the total number
of Salmonella illnesses attributed to products subject to this
proposal.\261\ However, the net benefits from this alternative
(benefits minus costs) are negative for all scenarios. Therefore, the
Agency rejects this alternative.
---------------------------------------------------------------------------

\261\ According to the 2023 risk assessments, there are 125,000
and 18,000 Salmonella illnesses attributed to products subject to
this proposed rule each year. USDA, FSIS, ``Quantitative
Microbiological Risk Assessment for Salmonella in Raw Chicken and
Raw Chicken Products,'' January 2023 at: https://www.regulations.gov/docket/FSIS-2023-0028; USDA, FSIS,
``Quantitative Microbiological Risk Assessment for Salmonella in Raw
Turkey and Raw Turkey Products,'' January 2023 at: https://www.regulations.gov/docket/FSIS-2023-0028.
---------------------------------------------------------------------------

Alternative 4: The proposed rule and proposed determination with a
higher contamination level for adulterated product of 100 cfu/mL(g) and
serotypes of public health significance.
Alternative 4 would consider product under this proposal to be
adulterated if it contains 100 cfu/mL(g) and a Salmonella serotype of
public health significance. This alternative results in lower costs for
industry to comply with the proposal, as a lower volume of product
would have initial results at or above 100 cfu/mL(g) and would result
in a lower lost value for the industry ($0.62 million, ranging from
$0.35 million to $3.16 million). Alternative 4 also presents fewer
prevented Salmonella illnesses, which range from 384 to 2,220. This
represents between 0.3 and 1.5 percent of the total number of
Salmonella illnesses attributed to products subject to this
proposal.\262\ The

[[Page 64744]]

net benefits from this alternative (benefits minus costs) are negative
at the medium, and high estimates. Therefore, the Agency rejects this
alternative.
---------------------------------------------------------------------------

\262\ According to the 2023 risk assessments, there are 125,000
and 18,000 Salmonella illnesses attributed to products subject to
this proposed rule each year. USDA, FSIS, ``Quantitative
Microbiological Risk Assessment for Salmonella in Raw Chicken and
Raw Chicken Products,'' January 2023 at: https://www.regulations.gov/docket/FSIS-2023-0028; USDA, FSIS,
``Quantitative Microbiological Risk Assessment for Salmonella in Raw
Turkey and Raw Turkey Products,'' January 2023 at: https://www.regulations.gov/docket/FSIS-2023-0028.
---------------------------------------------------------------------------

Alternative 5. The proposed rule and proposed determination with a
lower contamination level for adulterated product of 1 cfu/mL(g)
Salmonella regardless of serotype.
Alternative 5 would consider product under this proposal to be
adulterated if it contains 1 cfu/mL(g) Salmonella, regardless of the
presence of Salmonella serotype. This alternative results in higher
costs for industry to comply with the proposal, as a higher volume of
product would be adulterated with results at or above 1 cfu/mL(g). The
lost value to industry would increase to $48.0 million (ranging from
$27.4 million to $72.0 million), which is the highest in comparison to
the other alternatives. Alternative 5 also presents higher benefits
from prevented Salmonella illnesses, which range from 5,000 to 7,750.
This represents between 3.5 and 5.4 percent of the total number of
Salmonella illnesses attributed to products subject to this
proposal.\263\ However, this alternative results in the lowest net
benefits (benefits minus costs) and all scenarios result in net costs.
Therefore, the Agency rejects this alternative.
---------------------------------------------------------------------------

\263\ According to the 2023 risk assessments, there are 125,000
and 18,000 Salmonella illnesses attributed to products subject to
this proposed rule each year. USDA, FSIS, ``Quantitative
Microbiological Risk Assessment for Salmonella in Raw Chicken and
Raw Chicken Products,'' January 2023 at: https://www.regulations.gov/docket/FSIS-2023-0028; USDA, FSIS,
``Quantitative Microbiological Risk Assessment for Salmonella in Raw
Turkey and Raw Turkey Products,'' January 2023 at: https://www.regulations.gov/docket/FSIS-2023-0028.
---------------------------------------------------------------------------

VII. Regulatory Flexibility Act Assessment

The FSIS Administrator has made a preliminary determination that
this proposed rule and proposed determination, if finalized, would not
have a significant economic impact on a substantial number of small
entities in the U.S., as defined by the Regulatory Flexibility Act (5
U.S.C. 601 et seq.). Establishments subject to this proposal are
classified in the 311615 Poultry Processing sector of the North
American Industry Classification System (NAICS). The U.S. Small
Business Administration (SBA) size standard for small businesses in
this section is 1,250 employees.\264\ This NAICS sector includes
establishments ``primarily engaged in (1) slaughtering poultry and
small game and/or (2) preparing processed poultry and small game meat
and meat byproducts.'' As a result, the sector includes establishments
that produce products beyond the scope of this proposal, including
further processing of poultry products. FSIS has typically classified
establishments in three size categories based on employment counts and
annual sales: large establishments have over 500 employees, small
establishments have between 10 and 499 employees, and very small
establishments have less than 10 employees or less than $2.5 million in
annual sales.\265\ These categories, however, do not necessarily
capture the variability in production volumes between regulated
establishments. For this reason, FSIS classified establishments based
on production volumes of the products subject to this proposal.
---------------------------------------------------------------------------

\264\ U.S. Census Bureau, ``North American Industry
Classification System--2022 NAICS Definition: 311615 Poultry
Processing January 3, 2024, https://www.census.gov/naics/?input=311615&year=2022&details=311615; SBA, Table of size
standards, October 25, 2023, https://www.sba.gov/sites/default/files/2023-06/Table%20of%20Size%20Standards_Effective%20March%2017%2C%202023%20%282%29.pdf.
\265\ 61 FR 38806.
---------------------------------------------------------------------------

FSIS established volume categories for this proposal based on
Agency data on establishments' production volumes and the 2016 cost-
benefit analysis in support of the FSIS ``Chicken Parts and Not Ready-
To-Eat Comminuted Poultry Performance Standards,'' as shown in tables
38 and 39.\266\ Furthermore, FSIS uses production volumes for
allocating samples to be collected at regulated establishments,
therefore these volume categories more closely capture the estimated
impact of this proposal. This proposal is estimated to impact a total
of 284 establishments classified as low- and very low-volume
establishments. FSIS considers these volume categories to be small
entities.
---------------------------------------------------------------------------

\266\ USDA, FSIS, Chicken Parts and Not Ready-To-Eat Comminuted
Poultry Performance Standards, Final Cost-Benefit Analysis, February
11, 2016, https://www.fsis.usda.gov/sites/default/files/media_file/documents/FRN-related-CBA-Salmonella-Campy-2014-0023-022016.pdf.
---------------------------------------------------------------------------

Final Product Standards

The volume categories for establishments subject to the proposed
final product standards are summarized in Table 38. Of these, 37
establishments produced chicken carcasses, 127 produced chicken parts,
39 produced comminuted chicken, and 18 produced comminuted turkey
products that would be subject to the final product standards. This
represents roughly 27.6 percent of the establishments impacted by this
proposal.\267\ Low- and very low-volume establishments, combined,
accounted for 0.08 percent of the total chicken carcasses produced in
2021. In that same year, low-volume establishments represented 0.1,
2.8, and 0.5 percent of the total production of chicken parts,
comminuted chicken, and comminuted turkey, respectively.\268\
---------------------------------------------------------------------------

\267\ Some establishments may produce more than one product
subject to these final product standards. For these estimates, FSIS
counted establishments separately for each product subject to the
final product standards, therefore, establishments may be counted
more than once.
\268\ Note that there is no very low-volume category for chicken
parts, comminuted chicken, and comminuted turkey.

Table 38--Volume Categories for Establishments Subject to the Final Products Standards
----------------------------------------------------------------------------------------------------------------
Chicken carcasses Chicken parts Comminuted chicken Comminuted turkey
Establishment volume category (birds slaughtered (annual production (daily production (daily production
annually) pounds) pounds) pounds)
----------------------------------------------------------------------------------------------------------------
High............................ 10 million or more 70 million or more 250,000 or more... 250,000 or more.
Medium.......................... More than 1.1 More than 1 More than 6,000 More than 6,000
million and less million and less and less than and less than
than 10 million. than 70 million. 250,000. 250,000.
Low............................. More than 440,001 1 million or less. Less than 6,000... Less than 6,000.
and less than 1.1
million.
Very Low \1\.................... No more than n/a............... n/a............... n/a.
440,000.
----------------------------------------------------------------------------------------------------------------
\1\ Very low-volume establishments are defined in 9 CFR 381.65g(1)(i).

[[Page 64745]]

As a result of the proposal, based on the assumptions and estimates
described in the Regulatory Impact Analysis section, FSIS estimates
that the medium per establishment cost for low-volume establishments
that produce chicken carcasses is $1,260 per year. For very low-volume
establishments in this product group, the medium per establishment cost
would be $1,067, if the proposal is finalized. For low-volume
establishments that produce chicken parts, comminuted chicken, and
comminuted turkey, the estimated medium per establishment cost is
$1,305, $3,152, and $1,296 per year, respectively.
FSIS used the per pound retail prices described in the Lost value
to the industry costs section to estimate the average revenue for low-
and very low-volume establishments from producing chicken carcasses,
chicken parts, comminuted chicken, and comminuted turkey. FSIS
estimates the cost associated with this proposal represents about 0.04
percent of the chicken carcass revenue for low-volume establishments
and 0.15 percent for very low-volume establishments.\269\ For low-
volume establishments producing chicken parts, the estimated cost of
the proposal represents about 0.1 percent of the estimated
revenue.\270\ This estimated cost represents 0.9 and 0.4 percent of the
estimated revenue for low-volume establishments that produce comminuted
chicken and comminuted turkey, respectively.\271\
---------------------------------------------------------------------------

\269\ FSIS estimated the average chicken carcass revenue for
low-volume establishments at $3.2 million, while for very low-volume
establishments this revenue was $0.7 million in 2021.
\270\ FSIS estimated the average chicken parts revenue for low-
volume establishments at $1.2 million.
\271\ FSIS estimated the average comminuted chicken revenue for
low-volume establishments at $0.35 million, while for low-volume
establishments producing comminuted turkey, this estimate is $0.32
million.
---------------------------------------------------------------------------

FSIS also expects the cost burden of this proposal on low- and very
low-volume establishments to be limited due to several factors:
(1) FSIS estimates that the total cost for low- and very low-volume
establishments for complying with this proposal is small. As proposed,
final product standards account for the largest proportion of estimated
costs, which are estimated to cost these establishments $1,569, on
average, per establishment per year. This cost will vary depending on
an establishment's production level.
(2) The cost estimates presented as part of this analysis are based
on FSIS' estimated lot size. FSIS allows establishments to produce
smaller representative batches of product for sampling.\272\
Consequently, low- and very low-volume establishments can reduce costs
by reducing their lot size when FSIS collects a sample.
---------------------------------------------------------------------------

\272\ 77 FR 73402.
---------------------------------------------------------------------------

(3) FSIS is also adopting an implementation schedule that allows
low- and very low-volume establishments additional flexibility to
adjust to the new regulations. Low- and very low-volume establishments
would have three years to comply with this proposal after it is
finalized.

Process Control Requirements

The volume categories for establishments subject to the statistical
process control requirements are summarized in Table 39. Of the 284
small entities impacted by this proposal, 108 are poultry slaughter
establishments subject to the statistical process control requirements,
or about 36.2 percent of all poultry slaughter establishments. This
proposal requires that very low-volume and very small establishments
operating under Traditional Inspection collect an additional sample for
monitoring process control, as explained in the Statistical Process
Control costs section. This requirement is estimated to impact 92
establishments that are considered to be small entities by FSIS. The
rule also requires all poultry slaughter establishments to
electronically submit to FSIS data generated as part of their process
control monitoring. This requirement is estimated to impact 108
establishments that are considered to be small entities by FSIS. In
2021, there were 93 low and very low-volume chicken slaughter
establishments, 12 turkey slaughter, 1 duck slaughter, 1 goose
slaughter, and 1 squab slaughter establishments.\273\ In that year, low
and very low volume establishments accounted for 0.2 percent of chicken
slaughter, 0.1 percent of turkey slaughter, and 0.01 percent of duck
slaughter. For goose slaughter, one establishment accounted for about
98 percent of total slaughter in 2021, while one low volume
establishment accounted for 16 percent of squab slaughter in that year.
---------------------------------------------------------------------------

\273\ For establishments that slaughter multiple species,
process control requirements apply to the most predominant species
slaughtered annually.

Table 39--Volume Categories for Establishments Subject to the
Statistical Process Control Requirements
------------------------------------------------------------------------
Chicken All other poultry classes
------------------------------------------------------------------------
More than 10 million................... More than 1 million.
Between 1.1 million and 10 million..... Between 156 thousand and 1
million.
Between 440 thousand and 1.1 million... Between 60 thousand and 156
thousand.
Less than 440 thousand................. Less than 60 thousand.
------------------------------------------------------------------------

FSIS estimated process control requirements would cost $2,129 per
establishment per year. As these establishments produce a wide variety
of products, including multiple poultry classes, FSIS is unable to
estimate the share this cost represents of establishments' total
revenue. However, FSIS production data show that 79 establishments (73
percent) slaughter more than one class of poultry. Additionally, 36
establishments (about 33 percent) produce other nonpoultry FSIS
inspected products. Nonpoultry products represent 54 percent, on
average, of these establishments' total production by volume. However,
to mitigate the impact and costs of this requirement, the Agency is
proposing to make laboratory services available to analyze process
control samples instead of the establishment using establishment
resources or commercial laboratories. In addition, FSIS is providing a
template for establishments to use when submitting data to the Agency.
Consequently, these costs could be mitigated is represents potential
cost savings for these establishments.

VIII. Paperwork Reduction Act

In accordance with the Paperwork Reduction Act of 1995 (44 U.S.C.
3501-3520), FSIS has reviewed the proposed rule. All establishments
that slaughter poultry are currently required to

[[Page 64746]]

monitor their ability to maintain process control through microbial
testing and recordkeeping under the currently approved information
collection, 0583-0156, Modernization of Poultry Slaughter Inspection.
FSIS is proposing to revise this collection to require that
establishments submit their microbial sampling results to FSIS
electronically on a monthly basis. FSIS is also proposing to require
that all establishments, including VS and VLV establishments operating
under Traditional Inspection to test at 2 points (rehang and post-
chill) instead of only post-chill. VS and VLV establishments operating
under Traditional Inspection would have the option to use laboratory
resources provided by FSIS to analyze their monitoring samples for
them, but they would still be required to have their results recorded
and submitted to FSIS electronically.
Should FSIS finalize this proposal, the Agency would provide a
template that establishments could use to record and submit their
monthly results. FSIS is developing a web portal that will allow
external partners to securely upload sampling information and submit it
to FSIS in a machine- readable format. The proposed fields that would
be uploaded into the portal are: a sample identification number, the
establishment number, date, time, slaughter line number, location of
sample collection (e.g., rehang, post-chill), poultry species sampled,
sample type (e.g., rinsate, sponge), analyte (e.g., AC, EB), analyte
units (e.g., cfu/mL), quantified analyte result, and text analyte
result (e.g., Upper LOD). Establishments that use the
spreadsheet template to record the microbial monitoring results may
upload their completed spreadsheet into the web portal to submit their
monthly microbial data to FSIS or they may enter the information
manually into the portal. Establishments that do not use the spread
sheet provided by FSIS as a template to record their results would need
to manually enter their microbial sampling data into the portal to
submit their monthly data.
FSIS is revising this information collection to add 1,788 total
burden hours due to the proposed new requirements. The burden estimate
has also been updated to reflect the current number of poultry
slaughter establishment respondents, which has increased from 289 to
298 since the initial information collection approval. FSIS requests
comments on the proposed data fields and on the proposed electronic
data submission process.
FSIS estimates that a total of 298 establishments would conduct
microbial testing and enter 6-12 associated data points into the spread
sheet, or directly into the portal, 12 times annually for a total of
1,788 hours.

Microbial Testing, Recording, and Electronic Submission
[9 CFR 381.65(g) and (h)]
--------------------------------------------------------------------------------------------------------------------------------------------------------
Number of Time for
Number of responses per Total annual response in Total annual
respondents respondent responses mins. time in hours
--------------------------------------------------------------------------------------------------------------------------------------------------------
Total.............................................................. 298 1 12 30 1,788
--------------------------------------------------------------------------------------------------------------------------------------------------------

Copies of this information collection assessment can be obtained
from Gina Kouba, Office of Policy and Program Development, Food Safety
and Inspection Service, USDA, 1400 Independence Avenue SW, Mailstop
3758, South Building, Washington, DC 20250-3700; (202) 937-4272.
Comments are invited on: (a) whether the proposed collection of
information is necessary for the proper performance of FSIS' functions,
including whether the information will have practical utility; (b) the
accuracy of FSIS' estimate of the burden of the proposed collection of
information, including the validity of the method and assumptions used;
(c) ways to enhance the quality, utility, and clarity of the
information to be collected; and (d) ways to minimize the burden of the
collection of information, including through the use of appropriate
automated, electronic, mechanical, or other technological collection
techniques, or other forms of information technology. Comments may be
sent to both FSIS, at the addresses provided above, and the Desk
Officer for Agriculture, Office of Information and Regulatory Affairs,
Office of Management and Budget (OMB), Washington, DC 20253

IX. E-Government Act

FSIS and USDA are committed to achieving the purposes of the E-
Government Act (44 U.S.C. 3601, et seq.) by, among other things,
promoting the use of the internet and other information technologies
and providing increased opportunities for citizen access to Government
information and services, and for other purposes.

X. Executive Order 12988, Civil Justice Reform

This proposed rule has been reviewed under E.O. 12988, Civil
Justice Reform. Under this proposed rule: (1) All State and local laws
and regulations that are inconsistent with this proposed rule will be
preempted; (2) no retroactive effect will be given to this proposed
rule; and (3) no administrative proceedings will be required before
parties may file suit in court challenging this proposed rule.

XI. E.O. 13175

E.O. 13175 requires Federal agencies to consult and coordinate with
tribes on a government to-government basis on policies that have tribal
implications, including regulations, legislative comments or proposed
legislation, and other policy statements or actions that have
substantial direct effects on one or more Indian tribes, on the
relationship between the Federal Government and Indian tribes or on the
distribution of power and responsibilities between the Federal
Government and Indian tribes. FSIS has assessed the impact of this
proposed rule on Indian tribes and determined that this proposed rule
does not, to our knowledge, have tribal implications that require
tribal consultation under E.O. 13175. If a tribe requests consultation,
FSIS will work with the Office of Tribal Relations to ensure meaningful
consultation is provided where changes, additions, and modifications
identified herein are not expressly mandated by Congress.

XII. USDA Non-Discrimination Statement

In accordance with Federal civil rights law and USDA civil rights
regulations and policies, USDA, its Mission Areas, agencies, staff
offices, employees, and institutions participating in or administering
USDA programs are prohibited from discriminating based on race, color,
national origin, religion, sex, gender identity (including gender
expression), sexual orientation, disability, age, marital status,
family/parental status,

[[Page 64747]]

income derived from a public assistance program, political beliefs, or
reprisal or retaliation for prior civil rights activity, in any program
or activity conducted or funded by USDA (not all bases apply to all
programs). Remedies and complaint filing deadlines vary by program or
incident. Program information may be made available in languages other
than English. Persons with disabilities who require alternative means
of communication to obtain program information (e.g., Braille, large
print, audiotape, American Sign Language) should contact the
responsible Mission Area, agency, or staff office; the USDA TARGET
Center at (202) 720-2600 (voice and TTY); or the Federal Relay Service
at (800) 877-8339. To file a program discrimination complaint, a
complainant should complete a Form, AD-3027, USDA Program
Discrimination Complaint Form, which can be obtained online at https://www.usda.gov/forms/electronic-forms, from any USDA office, by calling
(866) 632-9992, or by writing a letter addressed to USDA. The letter
must contain the complainant's name, address, telephone number, and a
written description of the alleged discriminatory action in sufficient
detail to inform the Assistant Secretary for Civil Rights about the
nature and date of an alleged civil rights violation. The completed AD-
3027 form or letter must be submitted to USDA by: (1) Mail: U.S.
Department of Agriculture, Office of the Assistant Secretary for Civil
Rights, 1400 Independence Avenue SW, Washington, DC 20250-9410; (2)
Fax: (833) 256-1665 or (202) 690-7442; or (3) Email:
usda.gov">program.intake@usda.gov.
USDA is an equal opportunity provider, employer, and lender.

XIII. Environmental Impact

Each USDA agency is required to comply with 7 CFR part 1b of the
Departmental regulations, which supplements the National Environmental
Policy Act regulations published by the Council on Environmental
Quality. Under these regulations, actions of certain USDA agencies and
agency units are categorically excluded from the preparation of an
Environmental Assessment (EA) or an Environmental Impact Statement
(EIS) unless the agency head determines that an action may have a
significant environmental effect (7 CFR 1b.4(b)). FSIS is among the
agencies categorically excluded from the preparation of an EA or EIS (7
CFR 1b.4(b)(6)). This proposed rule would establish final product
standards for certain raw poultry products. Under this proposal, raw
chicken carcasses, chicken parts, comminuted chicken, and comminuted
turkey that contain Salmonella levels and serotypes in the proposed
final product standards would be adulterated. This proposed rule would
also revise the regulations that require that all poultry slaughter
establishments develop, implement, and maintain written procedures to
prevent contamination by enteric pathogens throughout the entire
slaughter and dressing operation to clarify that these procedures must
include a MMP that incorporates SPC monitoring methods and to require
all establishments to conduct testing at rehang and post chill. FSIS
has determined that this proposed rule would not create any
extraordinary circumstances that would result in this normally excluded
action having a significant individual or cumulative effect on the
human environment. Therefore, this action is appropriately subject to
the categorical exclusion from the preparation of an environmental
assessment or environmental impact statement provided under 7 CFR
1b.4(b)(6) of the U.S. Department of Agriculture regulations.

XIV. Additional Public Notification

Public awareness of all segments of rulemaking and policy
development is important. Consequently, FSIS will announce this Federal
Register publication on-line through the FSIS web page located at:
https://www.fsis.usda.gov/federal-register. FSIS will also announce and
provide a link through the FSIS Constituent Update, which is used to
provide information regarding FSIS policies, procedures, regulations,
Federal Register notices, FSIS public meetings, and other types of
information that could affect or would be of interest to our
constituents and stakeholders. The Constituent Update is available on
the FSIS web page. Through the web page, FSIS is able to provide
information to a much broader, more diverse audience. In addition, FSIS
offers an email subscription service which provides automatic and
customized access to selected food safety news and information. This
service is available at: https://www.fsis.usda.gov/subscribe. Options
range from recalls to export information, regulations, directives, and
notices. Customers can add or delete subscriptions themselves and have
the option to password protect their accounts.

List of Subjects in 9 CFR Part 381

Meat inspection, Poultry and poultry products.

For the reasons set forth in the preamble, FSIS proposes to amend 9
CFR part 381 as follows:

PART 381--POULTRY PRODUCTS INSPECTION REGULATIONS

0
1. The authority citation for part 381 continues to read as follows:

Authority: 7 U.S.C. 138f, 1633; 21 U.S.C. 451-472; 7 CFR 2.7,
2.18, 2.53.
0
2. Amend Sec. 381.65 by revising paragraphs (g) and (h) to read as
follows:

Sec. 381.65 Operations and procedures, generally.

* * * * *
(g) Procedures for controlling contamination throughout the
slaughter and dressing operation. Official poultry slaughter
establishments must develop, implement, and maintain written procedures
to prevent contamination of carcasses and parts by enteric pathogens
and fecal contamination throughout the entire slaughter and dressing
operation. Establishments must incorporate these procedures into their
HACCP plans, or sanitation SOPs, or other prerequisite programs. At a
minimum, these procedures must establish a microbial monitoring program
that includes sampling and analysis of microbial organisms in
accordance with the requirements in paragraphs(g)(1)-(5) of this
section to monitor an establishment's ability to maintain process
control.
(1) Sampling locations. Establishments must collect and analyze
samples for microbial organisms at the rehang and post-chill points in
the process.
(i) The establishment's microbial monitoring program must identify
and provide supporting rationale for the specific point in the process
where rehang and post-chill samples will be collected.
(ii) An establishment may collect samples at a location other than
rehang if the establishment provides supporting data to demonstrate
that the alternate location is at least as effective as rehang sampling
for monitoring the establishment's ability to maintain process control.
(2) Sampling frequency.
(i) Except as provided in paragraph (g)(2)(ii) of this section, all
official poultry establishments must collect and analyze paired
monitoring samples at the following rates. Establishments that
slaughter multiple species may conduct sampling on the type of poultry
slaughtered in the greatest number.
(A) Chickens

[[Page 64748]]

----------------------------------------------------------------------------------------------------------------
Predominant poultry species Establishment volume Annual slaughter Minimum frequency of
slaughtered sizes head volume paired collection
----------------------------------------------------------------------------------------------------------------
Chicken................................ Very Low Volume.......... 1-440,000 13 Weekly Pairs per Year.
Chicken................................ Low Volume............... 440,001-1,100,000 Weekly.
Chicken................................ Medium and High Volume... >=1,100,000 1 per 22,000.
----------------------------------------------------------------------------------------------------------------

(B) Turkeys, ducks, geese, guineas and squabs

----------------------------------------------------------------------------------------------------------------
Predominant poultry species Establishment volume Annual slaughter Minimum frequency of
slaughtered sizes head volume paired collection
----------------------------------------------------------------------------------------------------------------
Turkey, Geese, Guinea, Ducks, Squab.... Very Low Volume.......... 1-60,000 13 Weekly Pairs per Year.
Turkey, Geese, Guinea, Ducks, Squab.... Low Volume............... 60,001-156,000 Weekly.
Turkey, Geese, Guineas, Ducks Squab.... Medium and High Volume... >=156,000 1 per 3,000.
----------------------------------------------------------------------------------------------------------------

(ii) Very low volume establishments as defined in paragraphs
(g)(2)(i)(A) and (B) of this section that plan to operate less than 13
weeks per year may collect and analyze 13 samples less than weekly if
the establishment can demonstrate that it is effectively maintaining
process control throughout the year and during any periods of slaughter
operations.
(iii) Establishments must sample at a frequency that is adequate to
monitor their ability to maintain process control for enteric
pathogens.
(iv) Establishments must maintain accurate records of all test
results and retain these records as provided in paragraph(h) of this
section.
(3) Microbial Organism and Methods. Establishments must analyze
monitoring samples for microbial organisms that are quantifiably
detectable in their slaughter process and that will generate microbial
monitoring data that is adequate to monitor their ability to maintain
process control for enteric pathogens.
(i) The establishment's measured results at each sample location
must yield statistically reliable quantified value results
(ii) The establishments' sample collection method must be
appropriate for the product sampled, the microbial organism monitored,
and the laboratory method used to analyze the samples.
(iii) The establishment's microbial sampling results must be
generated by validated laboratory analyses and methods.
(4) Microbial Monitoring Criteria. The establishment must use
appropriate statistical methods to compare microbial monitoring data
against predefined quantitative limits adequate to gauge its ability to
maintain process control. At a minimum, the microbial monitoring
program must identify and support limits for:
(i) The minimal expected change in microbial levels measured
between sampling locations; and
(ii) The expected consistency of the levels of change detected over
a specified monitoring period.
(5) Corrective Actions. The establishment must implement written
corrective actions, including a root cause assessment, at a minimum
when:
(i) The microbial monitoring results deviate from predefined
quantitative limits;
(ii) The microbial monitoring results are not consistent with the
other process control monitoring results for the same procedures; or
(iii) The microbial monitoring results are not consistent with the
process control determination made for the entire slaughter HACCP
system.
(h) Recordkeeping requirements. Official poultry slaughter
establishments must maintain daily records sufficient to document the
implementation and monitoring of the procedures required under
paragraph (g) of this section. Records required by this section may be
maintained on computers if the establishment implements appropriate
controls to ensure the integrity of the electronic data. Records
required by this section must be maintained for at least one year and
must be accessible to FSIS.
(1) Official poultry slaughter establishments must submit their
microbial sampling results to FSIS electronically on a monthly basis.
(2) [reserved]

Done in Washington, DC.
Paul Kiecker,
Administrator.
[FR Doc. 2024-16963 Filed 8-6-24; 8:45 am]
BILLING CODE 3410-DM-P