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U.S. Department of Health and Human Services

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NARMS Retail Meat Survey Finds Campylobacter Common, Some Resistant to Antimicrobials

by David G. White, Ph.D., a research microbiologist in the Division of Food and Animal Microbiology, Office of Research; Robert D. Walker, Ph.D., Division Director, Division of Food and Animal Microbiology, Office of Research; and Joanne M. Kla, Assistant Editor
FDA Veterinarian Newsletter May/June 2004 Volume XIX, No 3

Federal officials earlier this year reported the results from a survey of antibiotic-resistant bacteria taken from retail cuts of meat.
In 2002, the officials expanded a surveillance program—the National Antimicrobial Resistance Monitoring System-Enteric Bacteria (NARMS), which is designed to monitor the development of resistant bacteria—to include surveillance of retail cuts of meat. The program was originally implemented to track the development of resistant bacteria in animals that produce food and relate that to resistant bacteria recovered from people suffering from foodborne illness.

NARMS was created by three branches of the Federal government—the Food and Drug Administration, the Centers for Disease Control and Prevention (CDC) and the U.S. Department of Agriculture (USDA)—to advance the safety of food in the U.S.

NARMS monitors changes in susceptibility of selected enteric bacteria to antimicrobial agents of human and veterinary importance.
The Federal managers of the NARMS program expanded it to include surveillance of retail foods of animal origin after conducting a feasibility study in Iowa. The retail food component of NARMS provides data on the prevalence of antimicrobial resistant foodborne pathogens and commensal bacteria among retail meat and poultry samples. Zoonotic foodborne bacterial pathogens currently under surveillance include Campylobacter and Salmonella, and are typically acquired through exposure to contaminated animal food products. Commensal bacteria of the intestinal tract that are under surveillance include enterococci and E. coli. These bacteria ordinarily colonize humans without causing disease, but on occasion, cause opportunistic infections such as wound or bloodstream infections.

NARMS retail meat surveillance is a collaborative effort among FDA, CDC and the Foodborne Diseases Active Surveillance Network (FoodNet). FoodNet is the principal foodborne disease component of CDC’s Emerging Infections Program (EIP). FoodNet is a collaborative project of the CDC, 10 EIP sites (California, Colorado, Connecticut, Georgia, New York, Maryland, Minnesota, Oregon, Tennessee and New Mexico), USDA and FDA. The project consists of active surveillance for foodborne diseases and related epidemiologic studies designed to help public health officials better understand the epidemiology of foodborne diseases in the United States.

The NARMS/FoodNet retail meat surveillance program started with FoodNet laboratories in six States—Connecticut, Georgia, Maryland, Minnesota, Oregon and Tennessee. By January 2004, the number of sites had increased to 10 with the addition of FoodNet laboratories in New York, California, Colorado and New Mexico.

For the NARMS retail meat surveillance program, participating FoodNet laboratory personnel collect retail meat samples from local grocery stores. All NARMS FoodNet participants follow a similar retail meat sampling scheme. Laboratory personnel from each site purchase approximately 40 food samples per month, including 10 samples each of chicken breasts, ground turkey, ground beef and pork chops.

All 10 FoodNet laboratories culture for Campylobacter and Salmonella using standard methods described by FDA. Four sites also culture for the presence of enterococci and E. coli.

Once the FoodNet staff have isolated and identified bacterial isolates, they ship them to the Center for Veterinary Medicine’s Office of Research to confirm species identification.

A comprehensive antibiogram (which is the antimicrobial susceptibility profile of an organism) is determined for the Salmonella, E. coli and enterococcal isolates using the NARMS antimicrobial panels. Both the E-test and agar dilution method are used to determine antimicrobial susceptibility patterns of Campylobacter species.

Antimicrobial susceptibility results are interpreted, where appropriate, according to internationally recognized standards established by the National Committee for Clinical Laboratory Standards (NCCLS). All Salmonella and Campylobacter isolates are also subjected to Pulsed-field gel electrophoresis (PFGE) to determine genetic relatedness. Resultant PFGE patterns are submitted to the CDC led PulseNet program (which is a national network for DNA fingerprinting of foodborne pathogens).

[Designer note -- the following list is associated with the U.S. Map on page 9 of the publication/PDF.]

Participating FoodNet Emerging Infections Program Laboratories

  • California Department of Health Services
  • Colorado Department of Public Health and Environment
  • Connecticut Department of Public Health
  • Georgia Department of Human Resources
  • Maryland Department of Health and Mental Hygiene
  • Minnesota Department of Health
  • New Mexico Department of Health
  • New York State Department of Health
  • Oregon Department of Human Services
  • Tennessee Department of Health

[Legend next to shading indicator for the 10 highlighted states on map:]

Retail Food Study Sites; FoodNet laboratories

Preliminary data

In 2002, 2,513 retail meats were analyzed for the presence of Campylobacter and Salmonella. These samples included 616 chicken breasts, 613 pork chops, 642 ground beef and 642 ground turkey samples.

Preliminary data indicate that Campylobacter was recovered from 47% of the chicken breasts sampled, which means that Campylobacter was recovered more often from chicken breast that from the other three meat types tested.
C. jejuni was the predominant species identified, followed by C. coli.

Because there are presently no NCCLS-approved interpretive criteria (susceptible, intermediate or resistant breakpoints) for Campylobacter, “resistance” refers to those isolates exhibiting ciprofloxacin minimum inhibitory concentrations (MIC) of more than 4 µg/ml and erythromycin MICs of more than 8 µg/ml.

Fifteen percent of C. jejuni recovered from chicken breast exhibited MIC > 4 µg/ml to ciprofloxacin (meaning the bacteria were resistant), as compared with 9 percent of C. coli. Twenty percent of C. coli exhibited MICs more than or equal to 8 µg/ml to erythromycin (making the bacteria resistant), as compared with 0 percent C. jejuni.

Salmonella was recovered from ground turkey in 13 percent of the samples, which was more often than the other three meat types tested. S. Heidelburg was the predominant serotype recovered (found in 34 of the 153 samples) and was more often associated with ground turkey samples (62 percent).

Overall, antimicrobial resistant phenotypes differed by Salmonella serotype and retail food of animal origin. For example, five multi-drug resistant S. Newport strains of bacteria were recovered from ground beef, ground turkey and pork chops. The majority of S. Newport isolates exhibited resistance to at least nine antimicrobials including cefoxitin, chloramphenicol and trimethoprim/sulfamethoxazole.

Salmonella isolates also showed decreased susceptibility to ceftriaxone (16-32 µg/ml). Nalidixic acid resistant Salmonella were isolated only from ground turkey and were predominantly S. Saintpaul (found in four of the six samples).

Indistinguishable Salmonella genetic DNA finger prints (PFGE patterns) were also recovered from different retail meats collected at different sampling times and from different States.

With regards to Enterococcus and E. coli prevalence, 1,574 meat samples were analyzed (only four of the NARMS/FoodNet sites participate in E. coli/Enterococcus surveillance). Sixty-eight percent of these retail meat samples were contaminated with E. coli. The majority of the 1,070 E. coli isolates recovered were susceptible to the antimicrobials tested. However, 52 percent were resistant to tetracycline, 36 percent to streptomycin, 28 percent to sulfamethoxazole, 19 percent to ampicillin and 14 percent to gentamicin.

Ninety-seven percent of the 1,574 retail meat samples were contaminated with enterococci. Among the 1,527 enterococci speciated, Enterococcus faecalis was the predominant species (recovered 59 percent of the time), followed by E. faecium (33 percent) and E. hirae (7 percent). Resistance to linezolid or vancomycin was not detected in any isolate, but high-level gentamicin resistance was observed in 9 percent of enterococci isolates.


Results from the NARMS retail 2002 survey demonstrate that retail meats, in particular chicken breast, are contaminated with Campylobacter, including antimicrobial-resistant variants.

Salmonella may also be found on retail meats, in particular ground turkey. On several occasions, indistinguishable Salmonella genetic finger prints were recovered from different retail foods of animal origin collected at different sample times and by different participating FoodNet laboratories, suggesting the dissemination of specific bacterial clones throughout the food supply.
These results demonstrate the dissemination of specific bacterial clones throughout the food supply.

Because campylobacteriosis and salmonellosis are transmitted primarily through contaminated food or water, the presence of antimicrobial-resistant variants in raw meat products has important public health implications. Further studies are needed to determine the relationships between antimicrobial use in animal husbandry with antimicrobial resistance development in these organisms as well as exploring mitigation strategies to reduce the presence of these foodborne pathogens on retail foods of animal origin.

Our observations also suggest that Enterococcus spp. and E. coli commonly contaminate retail meat products and that differences observed in antimicrobial susceptibility phenotypes may reflect the extent of use of antimicrobials in specific food animal production environments. Enterococci of foodborne origin have not been conclusively identified as direct causes of clinical infections; however, the consumption of meat carrying antibiotic-resistant bacterial populations is a possible route of transfer and could result in either colonization or transfer of resistance determinants to host-adapted strains.

Also, with the possible exception of E. coli O157:H7 and other shiga-toxin producing strains, the current data are insufficient to accurately assess the hazard and the potential public health risk associated with the presence of E. coli in foods, regardless of their antimicrobial resistance traits. Further study is also warranted to determine the significance and virulence potential of these organisms that contaminate retail food of animal origin.