Correspondence
Resistant Bacteria in Retail Meats and Antimicrobial Use in Animals
N Engl J Med 2002; 346:777-779March 7, 2002
- Article
To the Editor:
Changes in policy on the use of antimicrobials must be based on a broad perspective reflecting microbial epidemiology, ecology, and resistance. The three reports on specific areas of the overall problem of antimicrobial resistance in the October 18 issue1-3 are valuable, but the authors reach beyond the scope of their results in the conclusions they draw. Gorbach's editorial4 includes conclusions and assertions that are unsupported by his citations.
A ban on the use of antimicrobials in livestock feed could have unintended consequences and undesirable net effects on the environment, economy, and public health. Such a ban could result in increased morbidity and mortality in livestock, jeopardizing food and byproducts. There could also be a substantial increase in animal manure. The potential negative consequences to public health and the environment go far beyond the potential negative effects on livestock profitability. There are now science-based guidelines and stringent regulations for the judicious use of antimicrobials in food-producing animals.5,6
It is unknown whether banning antimicrobials in livestock feed would reduce the incidence of resistant infections in humans. Premature closure of this important debate now by imposition of a ban would lead us to overlook other approaches that could be more beneficial and less costly to society. It is imperative that we use solid science and examine the expected ramifications when proposing changes in antimicrobial-use policy.
6 ReferencesDavid Barber, D.V.M.
Gay Miller, D.V.M., Ph.D.
Paul McNamara, Ph.D.
University of Illinois at Urbana–Champaign, Urbana, IL 61802
dbarber@cvm.uiuc. edu 1
White DG ,Zhao S ,Sudler R , et al. The isolation of antibiotic-resistant salmonella from retail ground meats. N Engl J Med 2001;345:1147-1154
Full Text | Web of Science | Medline2
McDonald LC ,Rossiter S ,Mackinson C , et al. Quinupristin-dalfopristin-resistant Enterococcus faecium on chicken and in human stool specimens. N Engl J Med 2001;345:1155-1160
Full Text | Web of Science | Medline3
Sorensen TL ,Blom M ,Monnet DL ,Frimodt-Moller N ,Poulsen RL ,Espersen F . Transient intestinal carriage after ingestion of antibiotic-resistant Enterococcus faecium from chicken and pork. N Engl J Med 2001;345:1161-1166
Full Text | Web of Science | Medline4
Gorbach SL . Antimicrobial use in animal feed -- time to stop. N Engl J Med 2001;345:1202-1203
Full Text | Web of Science | Medline5
Center for Veterinary Medicine. Animal Medicinal Drug Use Clarification Act of 1994 (AMDUCA). Rockville, Md.: Food and Drug Administration, 2002. (Accessed February 13, 2002, at http://www.fda.gov/cvm/index/amducca/amducatoc.htm.)
6
Center for Veterinary Medicine. CVM and judicious use of antimicrobials. Rockville, Md.: Food and Drug Administration. (Accessed February 13, 2002, at http://www.fda.gov/cvm/fsi/juduse.htm.)
To the Editor:
In his editorial, Gorbach states that restrictions on the use of antimicrobials in food animals would provide health-related benefits. This proposal overlooks the fact that resistance in the human population is widespread because of human use of antimicrobials and will not be changed by eliminating certain veterinary uses of antimicrobials.1
Consistently, improvements have been made in swine housing, “flow”-through production stages, the quality and nutritional value of feed, sanitation, and preventive-medicine practices. Guidelines for the judicious use of antimicrobials2 are being implemented with the support of the American Association of Swine Veterinarians. All these measures have improved the health of swine and thus are essential for ensuring the safety of pork supplied to consumers.
Abolishing the use of additive antimicrobials in feed would force substantial changes in infrastructure and swine management, causing productivity losses that would cost farmers up to $1 billion over 10 years.3 Such losses would drive family farms out of business, despite substantial gaps in the data that are needed to give confidence that there would be any real effect on antimicrobial resistance, let alone public health.
3 ReferencesPaul Sundberg, D.V.M., Ph.D.
National Pork Board, Des Moines, IA 50306
paul.sundberg@porkboard. org 1
Curtiss R . The benefits of antimicrobial use in agriculture: a contrarian's long view. ASM News 2001;67:199-1992
Judicious therapeutic use of antimicrobials. Schaumburg, Ill.: American Veterinary Medical Association, 2002. (Accessed February 13, 2002, at http://www.avma.org/scienact/jtua/default.asp.)
3
Hayes DJ, Jensen HH, Backstrom L, Fabiosa J. Economic impact of a ban on the use of over-the-counter antibiotics. Ames, Iowa: Center for Agricultural and Rural Development, Iowa State University, December 1999. (Accessed February 13, 2002, at http://www.card.iastate.edu/publications/texts/99sr90.pdf.)
To the Editor:
White et al. report that 16 percent of 45 isolates from ground meats were resistant to ceftriaxone. This is a much higher proportion than that found by the National Antimicrobial Resistance Monitoring System (NARMS) in 1999 (0.4 percent of 1499 human-origin isolates, 0.1 percent of 1610 beef isolates, 0 percent of 1438 chicken isolates, and 0.4 percent of 470 dairy-cattle isolates, 0 percent of 876 swine isolates, and 0.8 percent of 713 turkey isolates).1,2 This inconsistency, combined with the substantial difference in identified serotypes between the samples studied by White et al. and those of the U.S. Department of Agriculture (USDA),3,4 indicates that the authors' sampling may have been confounded by contamination with salmonella that did not originate in food animals. The authors mention the potential for contamination during handling and processing. Seventeen of the 45 isolates were serotypes not found in the USDA sampling of food animals.3
4 ReferencesLyle P. Vogel, D.V.M., M.P.H.
American Veterinary Medical Association, Schaumburg, IL 60173
lvogel@avma.org 1
NARMS annual reports. Atlanta: Centers for Disease Control and Prevention, 2001. (Accessed February 13, 2002, at http://www.cdc.gov/ncidod/dbmd/narms/annuals.htm.)
2
National Antimicrobial Resistance Monitoring System (NARMS). Washington, D.C.: Food and Drug Administration, 2001. (Accessed February 13, 2002, at http://www.ars-grin.gov/ars/SoAtlantic/Athens/arru/narms.html.)
3
Sarwari AR ,Magder LS ,Levine P , et al. Serotype distribution of salmonella isolates from food animals after slaughter differs from that of isolates found in humans. J Infect Dis 2001;183:1295-1299
CrossRef | Web of Science | Medline4
James W. Salmonella serotypes from carcasses and raw ground products. In: Proceedings of the 104th Annual Meeting of the United States Animal Health Association. Richmond, Va.: Animal Health Association, 2000:504-7.
To the Editor:
Although eliminating the use of antimicrobials given to promote the growth of food animals and fowl would obviously be desirable, this suggestion results in strong opposition from groups that regard any such limitations as financially harmful. A more practical way to achieve the same end would be routine irradiation of meat, poultry, and fish. Although there is much prejudice against irradiation, I believe that such prejudice would be easier to deal with than opposition to the elimination of antimicrobials because the problem is ignorance, rather than financial self-interest. Irradiation would also get rid of pathogenic Escherichia coli. In the present era, when much supermarket meat is prepackaged at the slaughterhouse, this approach would be very effective.
Burton T. Blackman, M.D.
6621 Moore Dr., Los Angeles, CA 90048
eblack6621@aol.com Author/Editor Response
The authors reply:
To the Editor: Barber et al. state that in our study of antimicrobial-resistant salmonella from retail ground meats, we “reach beyond the scope” of our results in drawing a conclusion about banning antimicrobial use in livestock feed. In fact, we did not suggest such a ban. The study demonstrated that antimicrobial-resistant salmonella are common in retail meats. The findings provide support for the adoption of guidelines for the prudent use of antimicrobials in food animals and for a reduction of pathogens in our food supply.
In response to Vogel's statement that our sampling was possibly confounded by contamination with salmonella that did not originate in food animals: we agree that it is reasonable to explore other possible sources of salmonella contamination in retail meats. However, it has been established during many years of epidemiologic investigation of outbreaks of foodborne illness that animal products are the primary source of the salmonella that cause such illness.1 In addition, it has been shown that antimicrobial resistance in salmonella is most likely the result of antimicrobial use in food-producing animals and that most infections with antimicrobial-resistant salmonella are acquired by the consumption of contaminated food-animal products.2,3
Of particular importance in our study was the recovery of five isolates of Salmonella enterica serotype agona that were resistant to nine antimicrobials, including ceftriaxone and ceftiofur. They were recovered from turkey or beef purchased from a single store over a two-week period. These meats had been ground at three facilities, suggesting that the source of this serotype was the meat itself. We acknowledge that some of the serotypes we recovered have not been routinely found in the USDA sampling of food animals. However, there are more than 2000 serotypes of salmonella. Serotypes identified in one study do not necessarily match serotypes identified in other studies, unless the number of salmonella isolates reaches thousands. In fact, 62 percent of our isolates belonged to serotypes routinely recovered from animals. Among the 13 serotypes we detected, 3 were among the 8 salmonella serotypes most frequently identified in animal and human isolates submitted to the NARMS surveillance system in 1998.4
Vogel points out that the proportion of ceftriaxone resistance we observed in isolates from meat (16 percent) is much higher than the proportion of resistant isolates reported by NARMS. However, one would not expect the NARMS data to predict the rate of contamination of retail meats. Ground retail meats are produced by the comminution of tissues from multiple carcasses and would be expected to contain salmonella at a higher rate than the NARMS samples. In addition, antimicrobial resistance in salmonella is closely associated with serotype. S. enterica serotype typhimurium, for example, has been found to be more resistant than other serotypes. What is important about our observations is the finding in retail meats of many serotypes with multidrug-resistant phenotypes, including ceftriaxone resistance. Therefore, we need to focus efforts on reducing the prevalence of pathogens throughout food production and processing.
4 ReferencesDavid G. White, Ph.D.
Patrick F. McDermott, Ph.D.
Food and Drug Administration, Laurel, MD 20708Jianghong Meng, D.V.M., Ph.D.
University of Maryland, College Park, MD 20742
jm332@umail.umd. edu 1
Holmberg SD ,Wells JG ,Cohen ML . Animal-to-man transmission of antimicrobial-resistant salmonella: investigations of U.S. outbreaks, 1971-1983. Science 1984;225:833-835
CrossRef | Web of Science | Medline2
Seyfarth AM ,Wegener HC ,Frimodt-Moller N . Antimicrobial resistance in Salmonella enterica subsp. enterica serovar typhimurium from humans and production animals. J Antimicrob Chemother 1997;40:67-75
CrossRef | Web of Science | Medline3
Glynn MK ,Bopp C ,Dewitt W ,Dabney P ,Mokhtar M ,Angulo FJ . Emergence of multidrug-resistant Salmonella enterica serotype typhimurium DT104 infections in the United States. N Engl J Med 1998;338:1333-1338
Full Text | Web of Science | Medline4
NARMS annual reports. Atlanta: Centers for Disease Control and Prevention, 2001. (Accessed February 13, 2002, at http://www.cdc.gov/narms/annuals.htm.)
Author/Editor Response
Barber et al. contend that we reach “beyond the scope” of our results in the conclusions we draw. Meanwhile, the argument they make — that a ban on antimicrobials in livestock feed “could have unintended consequences and undesirable net effects on the environment, economy, and public health” — is wholly unsubstantiated. Poultry producers in Denmark, for example, voluntarily discontinued the use of all antimicrobials for growth promotion in food-producing animals, without significant untoward effects.1 We found that nearly 60 percent of retail chickens purchased in four states were contaminated with quinupristin-dalfopristin–resistant Enterococcus faecium and that this resistance was probably the result of antimicrobials used in animal feed. Although we found very little evidence to date of resistance among strains isolated from humans, we stand by our conclusion that antimicrobial use in animals is a matter of concern because of possible resistance in humans in the future.
Gorbach, in his editorial, went a step further and called for closer scrutiny of all antimicrobial use in food-producing animals and an outright ban on subtherapeutic use for growth promotion. The basis for both Gorbach's conclusions and ours is a large number of reports from various settings suggesting that antimicrobials used in food-producing animals frequently result in the transmission of clinically significant resistance to humans. Independent, prestigious scientific committees2,3 have examined these data and have arrived at conclusions similar to Gorbach's. The only question that remains is how long it will take for us to act on the data already available to us.
3 ReferencesL. Clifford McDonald, M.D.
University of Louisville, Louisville, KY 40292
lcliffmc@ulh.org 1
Emborg H ,Ersboll AK ,Heuer OE ,Wegener HC . The effect of discontinuing the use of antimicrobial growth promoters on the productivity in the Danish broiler production. Prev Vet Med 2001;50:53-70
CrossRef | Web of Science | Medline2
The use of antibiotics in food-producing animals: antibiotic-resistant bacteria in animals and humans: report of the Joint Expert Technical Advisory Committee on Antibiotic Resistance (JETACAR). Canberra, Australia: Commonwealth Department of Health and Aged Care, Commonwealth Department of Agriculture, Fisheries and Forestry, 1999. (Accessed February 13, 2002, at http://www.health.gov.au/pubs/jetacar.htm.)
3
WHO global principles for the containment of antimicrobial resistance in animals intended for food. Geneva: World Health Organization, 2000. (Also available at http://www.who.int/emc/diseases/zoo/who_global_principles.html.)
Author/Editor Response
A total ban on the use of antimicrobials in livestock feed has not been proposed, as argued by Barber et al., but there should be a ban on the use of antimicrobials for growth promotion as well as immediate termination of the widespread overuse of prophylactic antimicrobials in cases in which disease can be prevented by alternative strategies. Consequently, the argument concerning “increased morbidity and mortality in livestock” is not relevant.
A scientific study in Denmark found that terminating the use of antimicrobials for growth promotion in broiler chickens had no negative consequences on the animals' health or producers' profitability.1 Similar experiences have been reported in fattening pigs (weight range, 30 to 100 kg). In weaned piglets, however, problems with diarrhea have been observed in some herds after discontinuation of the use of growth-promoting antimicrobials. Such problems have been managed by veterinary interventions and improved feeding and weaning procedures.
Despite recent increases in the use of therapeutic antimicrobials in swine, the total volume of antimicrobials used in animal husbandry in Denmark has been reduced by more than 60 percent (from 206 to 81 tons) with the voluntary discontinuation of the use of antimicrobials for growth promotion.2 The resulting dramatic reduction in the frequency with which resistant bacteria are isolated from food animals, food, and humans has been well documented.2-5 Hence, there is sufficient scientific evidence to support urgent action. Finally, we do not share the concern expressed by Barber et al. regarding the “premature closure of this important debate.” The stamina of the animal-health industry lobby certainly precludes that.
5 ReferencesThomas Lund Sørensen, M.D.
Henrick Caspar Wegener, Ph.D.
Niels Frimodt-Møller, M.D., D.M.Sc.
Statens Serum Institut, DK-2300 Copenhagen S, Denmark
nfm@ssi.dk 1
Emborg H ,Ersboll AK ,Heuer OE ,Wegener HC . The effect of discontinuing the use of antimicrobial growth promoters on the productivity in the Danish broiler production. Prev Vet Med 2001;50:53-70
CrossRef | Web of Science | Medline2
DANMAP 2000 — consumption of antimicrobial agents and resistance to antimicrobial agents in bacteria from food animals, food and humans in Denmark: report from Statens Serum Institut, Danish Veterinary and Food Administration, Danish Medicines Agency and Danish Veterinary Laboratory, 2001. (Available at http://www.vetinst.dk/file/danmap2000.pdf.)
3
Aarestrup FM ,Seyfarth AM ,Emborg HD ,Pedersen K ,Hendriksen RS ,Bager F . Effect of abolishment of the use of antimicrobial agents for growth promotion on occurrence of antimicrobial resistance in fecal enterococci from food animals in Denmark. Antimicrob Agents Chemother 2001;45:2054-2059
CrossRef | Web of Science | Medline4
van Den Bogaard AE ,Bruinsma N ,Stobberingh EE . The effect of banning avoparcin on VRE carriage in the Netherlands. J Antimicrob Chemother 2000;46:146-147
CrossRef | Web of Science | Medline5
Klare I ,Badstubner D ,Konstabel C ,Bohme G ,Claus H ,Witte W . Decreased incidence of VanA-type vancomycin-resistant enterococci isolated from poultry meat and from fecal samples of humans in the community after discontinuation of avoparcin usage in animal husbandry. Microb Drug Resist 1999;5:45-52
CrossRef | Web of Science | Medline
- Citing Articles (4)
Citing Articles
1
Mohamed O. Ahmed, Nicola J. Williams, Peter D. Clegg, Jennifer C. van Velkinburgh, Keith E. Baptiste, Malcolm Bennett. (2012) Analysis of Risk Factors Associated with Antibiotic-Resistant Escherichia coli. Microbial Drug Resistance120109065551003
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Guillermo Blanco, Jesús A. Lemus, Javier Grande, Laura Gangoso, Juan M. Grande, José A. Donázar, Bernardo Arroyo, Oscar Frías, Fernando Hiraldo. (2007) Geographical variation in cloacal microflora and bacterial antibiotic resistance in a threatened avian scavenger in relation to diet and livestock farming practices. Environmental Microbiology 9:7, 1738-1749
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Elaine Larson. (2007) Community Factors in the Development of Antibiotic Resistance. Annual Review of Public Health 28:1, 435-447
CrossRef4
Alicia D. Anderson, Jennifer M. Nelson, Shannon Rossiter, Frederick J. Angulo. (2003) Public Health Consequences of Use of Antimicrobial Agents in Food Animals in the United States. Microbial Drug Resistance 9:4, 373-379
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