[Federal Register Volume 73, Number 129 (Thursday, July 3, 2008)]
[Rules and Regulations]
[Pages 38110-38113]
From the Federal Register Online via the Government Publishing Office [www.gpo.gov]
[FR Doc No: E8-15052]


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DEPARTMENT OF HEALTH AND HUMAN SERVICES

Food and Drug Administration

21 CFR Part 530

[Docket No. FDA-2008-N-0326]


New Animal Drugs; Cephalosporin Drugs; Extralabel Animal Drug 
Use; Order of Prohibition

AGENCY: Food and Drug Administration, HHS.

ACTION: Final rule.

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SUMMARY: The Food and Drug Administration (FDA) is issuing an order 
prohibiting the extralabel use of cephalosporin antimicrobial drugs in 
food-producing animals. We are issuing this order based on evidence 
that extralabel use of these drugs in food-producing animals will 
likely cause an adverse event in humans and, as such, presents a risk 
to the public health.

DATES: This rule becomes effective October 1, 2008. Submit written or 
electronic comments on this document by September 2, 2008.

ADDRESSES: You may submit comments, identified by [Docket No. FDA-2008-
N-0326], by any of the following methods:
Electronic Submissions
    Submit electronic comments in the following way:
     Federal eRulemaking Portal: http://www.regulations.gov. 
Follow the instructions for submitting comments.
Written Submissions
    Submit written submissions in the following ways:
     FAX: 301-827-6870.
     Mail/Hand delivery/Courier [For paper, disk, or CD-ROM 
submissions]: Division of Dockets Management (HFA-305), Food and Drug 
Administration, 5630 Fishers Lane, rm. 1061, Rockville, MD 20852.
    To ensure more timely processing of comments, FDA is no longer 
accepting comments submitted to the agency by e-mail. FDA encourages 
you to continue to submit electronic comments by using the Federal 
eRulemaking Portal, as described previously, in the ADDRESSES portion 
of this document under Electronic Submissions.
    Instructions: All submissions received must include the agency name 
and Docket No(s). and Regulatory Information Number (RIN) (if a RIN 
number has been assigned) for this rulemaking. All comments received 
may be posted without change to http://www.regulations.gov, including 
any personal information provided. For additional information on 
submitting comments, see the ``Comments'' heading of the SUPPLEMENTARY 
INFORMATION section of this document.
    Docket: For access to the docket to read background documents or 
comments received, go to http://www.regulations.gov and insert the 
docket number(s), found in brackets in the heading of this document, 
into the ``Search'' box and follow the prompts and/or go to the 
Division of Dockets Management, 5630 Fishers Lane, rm. 1061, Rockville, 
MD 20852.

FOR FURTHER INFORMATION CONTACT: Neal Bataller, Center for Veterinary 
Medicine (HFV-230), Food and Drug Administration, 7519 Standish Pl., 
Rockville, MD, 20855, 240-276-9200, e-mail: [email protected].

SUPPLEMENTARY INFORMATION:

I. Background

A. AMDUCA

    The Animal Medicinal Drug Use Clarification Act of 1994 (AMDUCA) 
(Public Law 103-396) was signed into law on October 22, 1994. It 
amended the Federal Food, Drug, and Cosmetic Act (the act) to permit 
licensed veterinarians to prescribe extralabel uses of approved animal 
and human drugs in animals. In the Federal Register of November 7, 1996 
(61 FR 57732), we published the implementing regulations (codified at 
part 530 (21 CFR part 530)) for AMDUCA. The sections regarding 
prohibition of extralabel use of drugs in animals are Sec.  Sec.  
530.21, 530.25, and 530.30. These sections describe the basis for 
issuing an order prohibiting an extralabel drug use in animals and the 
procedure to be followed in issuing an order of prohibition.
    We may issue a prohibition order if we find that extralabel use of 
a drug in animals presents a risk to the public health. Under Sec.  
530.3(e), this means that we have evidence demonstrating that the use 
of the drug has caused, or likely will cause an adverse event.
    Section 530.25 provides for a public comment period of not less 
than 60 days. It also provides that the order of prohibition become 
effective 90 days after the date of publication, unless we revoke or 
modify the order, or extend the period of public comment. The list of 
drugs prohibited from extralabel use is found in Sec.  530.41.

B. Cephalosporins

    Cephalosporins are members of the [beta]-lactam class of 
antimicrobials. These antimicrobials work by targeting synthesis of the 
bacterial cell wall, resulting in increased permeability and eventual 
hydrolysis of the cell. Members of the cephalosporin class have a 
[beta]-lactam ring fused to a sulfur-containing ring-expanded system 
(Ref. 1).
    Certain cephalosporins are currently approved for use in a number 
of animal species. These approved uses include the treatment of 
respiratory disease in cattle, swine, sheep, and goats, as well as 
acute bovine interdigital necrobacillosis, acute metritis, and clinical 
and sub-clinical mastitis in cattle. They are also approved for the 
control of bovine respiratory disease, and the control of early 
mortality associated with Escherichia coli infections in day-old chicks 
and poults. Furthermore, approved animal uses of cephalosporins include 
the treatment of skin and soft tissue infections in dogs and cats, 
genitourinary tract infections (cystitis) in dogs, and respiratory 
tract infections in horses.
    Cephalosporins are also some of the most widely used antimicrobial 
agents in human medicine. Older agents are widely used as therapy for 
skin and soft tissue infections caused by Staphylococcus aureus and 
Streptococcus pyogenes, as well as treatment of upper respiratory tract 
infections, intra-abdominal infections, pelvic inflammatory disease, 
and diabetic foot infections. Newer cephalosporins, with or without 
aminoglycosides, have been considered drugs of choice for serious 
infections caused by Klebsiella, Enterobacter, Proteus, Providencia, 
Serratia, and Haemophilus spp. These cephalosporins are also used to 
treat systemic salmonellosis, although not specifically approved for 
this purpose. Fourth

[[Page 38111]]

generation cephalosporins are indicated for treatment of urinary tract 
infections, febrile neutropenia, intra-abdominal infections, pneumonia, 
and skin and skin structure infections (Ref. 2).
    FDA is concerned that the extralabel use of cephalosporins in food-
producing animals is likely to lead to the emergence of cephalosporin-
resistant strains of foodborne bacterial pathogens. If these drug-
resistant bacterial strains infect humans, it is likely that 
cephalosporins will no longer be effective for treating disease in 
those people. Therefore, FDA is issuing an order prohibiting the 
extralabel use of cephalosporins because, as discussed in section II of 
this document, the agency has determined that such extralabel use will 
likely cause an adverse event and as such presents a risk to the public 
health.

II. Basis for Prohibiting the Extralabel Use of Cephalosporins

A. Cephalosporin-Resistant Zoonotic Foodborne Bacteria

    A recent review of [beta]-lactam resistance in bacteria of animal 
origin states that an emerging issue of concern is the increase in 
reports of broad-spectrum [beta]-lactamases (CMY-2 and CTX-M) (Ref. 3). 
Acquired resistance to [beta]-lactams in animal isolates has been 
observed in surveillance programs such as the Canadian Integrated 
Program for Antimicrobial Resistance Surveillance (CIPARS), Danish 
Integrated Antimicrobial Resistance Monitoring and Research Programme 
(DANMAP), and the U.S. National Antimicrobial Resistance Monitoring 
System (NARMS).
    The 2005 European Antimicrobial Resistance Surveillance System 
(EARSS) report indicated that most European countries reported less 
than 5 percent resistance to third generation cephalosporins in 
foodborne pathogens including Enterococcus faecalis, E. faecium, and E. 
coli. However, the report noted that resistance was rising in 23 of 28 
countries, with significant trends identified for 15 countries. The 
EARSS report states that third generation cephalosporin resistance 
appears to be increasing rapidly, even in countries with formerly very 
low levels of resistance (Ref. 4).
    Ceftiofur is a third generation cephalosporin approved for certain 
uses in animals. Since 1997, the NARMS program has monitored ceftiofur 
resistance in Salmonella isolated from food-producing animals at 
slaughter. In 1997, no isolates from cattle or swine were resistant to 
ceftiofur, while ceftiofur resistance among isolates from chickens and 
turkeys was 0.5 percent and 3.7 percent, respectively. By 2006, the 
prevalence of ceftiofur resistance among Salmonella slaughter isolates 
increased to 18.8 percent for cattle, 2.0 percent for swine, 12.8 
percent for chickens, and 5.3 percent for turkeys (Ref. 5).
    Food-producing animals have been shown to be a source of resistant 
Salmonella infections in humans (Ref. 6). Data collected as part of 
NARMS have shown an increase in multi-drug resistance among Salmonella 
isolates from humans, including resistance to third generation 
cephalosporins. The prevalence of ceftiofur resistance among non-Typhi 
Salmonella isolates from humans rose from 0.2 percent in 1996 to 3.4 
percent in 2004. A similar trend was observed over this same period 
(i.e., 1996 to 2004) for decreased susceptibility to ceftriaxone, a 
third generation cephalosporin approved for use in humans (Ref. 7).
    Although ceftiofur is not used in human medicine, the observed 
trend of increasing resistance to this drug in human isolates 
highlights concerns about the movement of foodborne bacterial pathogens 
between animals and humans. In particular, as discussed in more detail 
in this document, resistance to certain cephalosporins is of public 
health concern in light of the evidence of cross-resistance among drugs 
in the cephalosporin class. Expanded-spectrum cephalosporins (e.g., 
ceftriaxone and cefotaxime) are the antimicrobial agents of choice for 
invasive Salmonella infections of pediatric patients (Ref. 8). FDA 
believes that the surveillance data cited supports the finding that 
certain cephalosporin use in animals is likely contributing to an 
increase in cephalosporin-resistant human pathogens.

B. Scope of Order of Prohibition

    The cephalosporins are one of the most diverse classes of 
antimicrobials, and have been subject to several different 
classification schemes, including those using chemical structure, 
microbial activity, pharmacokinetics, or marketing date to divide the 
various molecular entities into distinct groups. While there is 
considerable overlap among proposed schemes, individual cephalosporin 
drugs do not always fall into the same groups in all classifications. 
For example, a commonly used scheme that classifies cephalosporins into 
``generations'' provides some general idea of the first marketing date 
for the various cephalosporins. However, classification by generation 
does not necessarily group together cephalosporins with similar 
microbiological or pharmacokinetic characteristics. Therefore, because 
classification into ``generations'' is not based on specific properties 
of individual cephalosporins, there can be disagreement on which drugs 
belong in which generation.
    FDA considered the possibility of limiting the order of prohibition 
to certain individual cephalosporin drugs or to certain generations of 
cephalosporins. However, given the potential for confusion regarding 
the classification of individual cephalosporin drugs into various 
generations, FDA concluded that it would be problematic to define the 
scope of the prohibition based on cephalosporin ``generation.'' 
Furthermore, as discussed in more detail in this document, data 
regarding mechanisms by which bacteria become resistant to 
cephalosporins have demonstrated cross-resistance among various 
individual cephalosporin drugs and among various generations of 
cephalosporin drugs.
    In general, there are three mechanisms by which bacteria become 
resistant to antimicrobial agents: (1) Alteration of the antimicrobial 
target, (2) efflux of the antimicrobial or changes in permeability of 
the bacterial cell, and (3) inactivation of the antimicrobial agent 
itself. Gram negative bacterial resistance to cephalosporins occurs 
mainly through inactivation of the cephalosporin by [beta]-lactamases. 
These enzymes can be both innate and acquired (Ref. 9).
    Among bacteria of human health concern, the two most important 
classes of [beta]-lactamase enzymes are the AmpC cephalosporinases and 
the extended-spectrum [beta]-lactamases (ESBL). AmpC enzymes are found 
on the chromosome of most Enterobacteriaceae, and are also currently 
found on promiscuous plasmids in Salmonella and E. coli. These enzymes 
provide resistance to first, second, and third generation 
cephalosporins. ``Fourth generation'' cephalosporins are active in 
vitro against AmpC producing bacteria, but there is some disagreement 
as to the clinical significance of that activity. The AmpC enzymes are 
currently the predominant [beta]-lactamases associated with Salmonella 
collected from animals and humans in the United States displaying 
resistance to ceftiofur and decreased susceptibility to ceftriaxone 
(Ref. 3).
    ESBLs present in bacteria of human health concern include members 
of the TEM, SHV, and CTX-M families. These enzymes are plasmid mediated 
and have the potential to provide resistance to all

[[Page 38112]]

cephalosporins. Different ESBLs hydrolyze different cephalosporins at 
different efficiencies and rates, thus leading to varying patterns of 
in vitro susceptibility. However, although a particular ESBL may not 
raise the minimum inhibitory concentration (MIC) for a given 
cephalosporin to a level above the breakpoint for resistance, these 
strains commonly prove to be resistant in vivo (Ref. 9). Therefore, 
there are specific guidelines for screening bacterial isolates for the 
presence of ESBLs when MIC's fall in the susceptible range. Any 
bacterial isolate which produces either an AmpC enzyme or an ESBL is 
reported to clinicians as resistant to all cephalosporins even though 
susceptibility testing may show in vitro susceptibility to some of the 
cephalosporins (Ref. 10). Thus, regardless of in vitro susceptibility 
results, the effect of resistance mediated by an AmpC enzyme or ESBL is 
that the organism is treated as if it is cross-resistant to all 
cephalosporins.
    In a review of the CTX-M family of ESBLs, Livermore et al. (Ref. 
11) noted that until the late 1990s, European surveys found the TEM and 
SHV families of ESBLs almost exclusively. CTX-M enzymes were recorded 
rarely, although large outbreaks of Salmonella Typhimurium with CTX-M-4 
and CTX-M-5 were reported in Latvia, Russia, and Belarus in the mid 
1990s. However, CTX-M enzymes are now the predominant ESBLs in many 
European countries, and E. coli has joined Klebsiella pneumoniae as a 
major host. CTX-M enzymes are supplanting TEM and SHV in East Asia as 
well as in Europe. Only in North America do TEM and SHV still 
predominate, although CTX-M enzymes have been occasionally detected. 
Once mobilized, CTX-M enzymes can be hosted by many different genetic 
elements, but are most often found on large multi-drug resistance 
plasmids. Therefore, FDA is concerned that if CTM-X becomes prevalent 
in the United States, as has occurred in other countries, cephalosporin 
resistance may escalate.
    Given that [beta]-lactamases have been identified in zoonotic 
bacteria of human health concern, and given that [beta]-lactamases can 
impart cross-resistance among cephalosporins (Ref. 12), FDA concluded 
that measures to prohibit extralabel use should be directed at the 
entire cephalosporin class of drugs.

C. Extralabel Use of Cephalosporins in Animals

    As summarized previously, certain cephalosporins are currently 
approved for use in a number of animal species for a variety of 
indications. However, under the provisions of AMDUCA, cephalosporins 
that are approved for use in animals or humans may be used in an 
extralabel manner in animals provided certain conditions are met. 
Although few data are available regarding the extent to which such 
extralabel use currently occurs in the various food-producing animal 
species, evidence exists that extralabel use is occurring. FDA 
conducted inspections at U.S. poultry hatcheries in 2001 and examined 
records relating to the hatcheries' antimicrobial use during the 30-day 
period prior to inspection. FDA found that six of the eight hatcheries 
inspected that used ceftiofur during that period were doing so in an 
extralabel manner (Ref. 13). For example, ceftiofur was being 
administered at unapproved dosing levels or by unapproved methods of 
administration. In particular, ceftiofur was being administered by egg 
injection, rather than by the approved method of administering the drug 
to day-old chicks.
    As is recognized for the use of antimicrobial drugs in general, the 
use of cephalosporins provides selection pressure that favors expansion 
of resistant variants. FDA believes the extralabel use of 
cephalosporins likely will contribute to the emergence of resistance 
and compromise human therapy. Given the importance of the cephalosporin 
class of drugs for treating disease in humans, FDA believes that 
preserving the effectiveness of such drugs is critical. Therefore, FDA 
believes it is necessary to take action to limit the extent to which 
extralabel use of cephalosporin in animals may be contributing to the 
emergence of resistant variants.
    FDA is particularly concerned about the extralabel use of 
cephalosporins in food-producing animals given that such animals are 
known reservoirs of foodborne bacterial pathogens such as Salmonella. 
Based on information regarding cephalosporin resistance as discussed 
previously, FDA believes it is likely that the extralabel use of 
cephalosporins in food-producing animals is contributing to the 
emergence of cephalosporin-resistant zoonotic foodborne bacteria. 
Therefore, FDA has determined that such extralabel use likely will 
cause an adverse event and, as such, presents a risk to the public 
health.

III. Comments

    Interested persons may submit to the Division of Dockets Management 
(see ADDRESSES) written or electronic comments regarding this document. 
Submit a single copy of electronic comments or two paper copies of any 
mailed comments, except that individuals may submit one paper copy. 
Comments are to be identified with the docket number found in brackets 
in the heading of this document. Received comments may be seen in the 
Division of Dockets Management between 9 a.m. and 4 p.m., Monday 
through Friday.
    Please note that on January 15, 2008, the FDA Division of Dockets 
Management Web site transitioned to the Federal Dockets Management 
System (FDMS). FDMS is a Government-wide, electronic docket management 
system. Electronic comments or submissions will be accepted by FDA only 
through FDMS at http://www.regulations.gov.

IV. Order of Prohibition

    Therefore, I hereby issue the following order under Sec.  Sec.  
530.21 and 530.25. We find that extralabel use of the cephalosporin 
class of antimicrobial drugs in food-producing animals likely will 
cause an adverse event, which constitutes a finding that extralabel use 
of these drugs presents a risk to the public health. Therefore, we are 
prohibiting the extralabel use of the cephalosporin class of 
antimicrobial drugs in food-producing animals.

V. References

    The following references have been placed on display in the 
Division of Dockets Management (see ADDRESSES) and may be seen by 
interested persons between 9 a.m. and 4 p.m., Monday through Friday.
    1. Livermore, D. M. and L. D. Williams, ``[beta]-Lactams: Mode 
of Action and Mechanisms of Resistance,'' pp. 502-578, Victor Lorian 
(ed.), Antibiotics in Laboratory Medicine, Williams & Wilkins, 
Baltimore, 1991.
    2. U.S. Food and Drug Administration, Maxipime (cefepime 
hydrochloride) for injection, NDA 50-679/S-021, http://www.fda.gov/medwatch/SAFETY/2003/03MAR_PI/Maxipime_PI.pdf (accessed March 13, 
2007).
    3. Li, X. Z., M. Mehrotra, S. Ghimire, and L. Adewoye, ``[beta]-
Lactam Resistance and [beta]-Lactamases in Bacteria of Animal 
Origin,'' Veterinary Microbiology, 121:197-214, 2007.
    4. European Antimicrobial Resistance Surveillance System, EARSS 
Annual Report 2005, pp. 1-147, Bilthoven, The Netherlands, 2006.
    5. U.S. Department of Health and Human Services, National 
Antimicrobial Resistance Monitoring System/Enteric Bacteria (NARMS/
EB) Salmonella Annual Veterinary Isolates Data, U.S. Department of 
Agriculture, http://www.ars.usda.gov/Main/docs.htm?docid=6750&page=4, 2006.
    6. Holmberg, S. D., J. G. Wells, and M. L. Cohen, ``Animal-to-
Man Transmission of Antimicrobial-Resistant Salmonella: 
Investigations of U.S. Outbreaks, 1971-1983,'' Science, 225:833-835, 
1984.

[[Page 38113]]

    7. CDC, ``National Antimicrobial Resistance Monitoring System 
for Enteric Bacteria (NARMS): Human Isolates Final Report,'' 2004, 
Atlanta, GA, U.S. Department of Health and Human Services, CDC, 
2007.
    8. Giles, W.P. , A. K. Benson, M. E. Olson, R. W. Hutkins, J. M. 
Whichard, P. L. Winokur, and P. D. Fey, ``DNA Sequence Analysis of 
Regions Surrounding blaCMY-2 From Multiple Salmonella Plasmid 
Backbones,'' Antimicrobial Agents and Chemotherapy, 48:2845-2852, 
2004.
    9. Livermore, D. M., ``Beta-Lactamases in Laboratory and 
Clinical Resistance,'' Clinical Microbiology Review, 8:557-584, 
1995.
    10. Clinical and Laboratory Standards Institute, Performance 
Standards for Antimicrobial Susceptibility Testing: Sixteenth 
Informational Supplement, M100-S16, Wayne, PA, USA: CLSI, 2006.
    11. Livermore, D. M., R. Canton, M. Gniadkowski, P. Nordmann, G. 
M. Rossolini, G. Arlet, J. Ayala, T. M. Coque, I. Kern-Zdanowicz, F. 
Luzzaro, L. Poirel, and N. Woodford, ``CTX-M: Changing the Face of 
ESBLs in Europe,'' Journal of Antimicrobial Chemotherapy, 59:165-
174, 2007.
    12. Jacoby, G. A. and L. S. Munoz-Price, ``The New B-
Lactamases,'' New England Journal of Medicine, 352:380-391, 2005.
    13. U.S. Food and Drug Administration, Center for Veterinary 
Medicine, unpublished report, Summary of Data From Hatchery 
Inspections Conducted September-October 2001, April 15, 2002.

List of Subjects in 21 CFR Part 530

    Administrative practice and procedure, Advertising, Animal drugs, 
Labeling, Reporting and recordkeeping requirements.

0
Therefore, under the Federal Food, Drug, and Cosmetic Act and under 
authority delegated to the Commissioner of Food and Drugs and 
redelegated to the Director of the Center for Veterinary Medicine, 21 
CFR part 530 is amended as follows:

PART 530--EXTRALABEL DRUG USE IN ANIMALS

0
1. The authority citation for 21 CFR part 530 continues to read as 
follows:

    Authority: 15 U.S.C. 1453, 1454, 1455; 21 U.S.C. 321, 331, 351, 
352, 353, 355, 357, 360b, 371, 379e.

0
2. In Sec.  530.41, add paragraph (a)(13) to read as follows:


Sec.  530.41  Drugs prohibited for extralabel use in animals.

    (a) * * *
    (13) Cephalosporins.
* * * * *

    Dated: June 24, 2008.
Bernadette Dunham,
Director, Center for Veterinary Medicine.
[FR Doc. E8-15052 Filed 7-2-08; 8:45 am]
BILLING CODE 4160-01-S