Poultry on Antibiotics:
Hazards to Human Health

[Executive Summary and selected tables]

WALLINGA, BERMUDEZ, & HOPKINS / IATP & Sierra Club Dec02

David Wallinga, M.D., MPA
Navis Bermudez, MESc
Edward Hopkins

2nd Edition

Sierra Club and IATP wish to thank Kendra Kimbirauskas, Jessica Nelson and Erin Jordahl for their assistance with this project. IATP would like to thank the Quixote Foundation for their support of this work. This report has been funded by a grant from The Sierra Club Foundation. Institute for Agriculture and Trade Policy 2105 First Avenue South, Minneapolis, MN 55404 (612) 870-0453 www.iatp.org  Sierra Club 85 Second St., Second Floor, San Francisco, CA 94105, (415) 977-5500 408 C St. NE, Washington, DC 20002, (202) 547-1141 www.sierraclub.org  Download a copy of the report from www.iatp.org or www.siearraclub.org/antibtiotics

EXECUTIVE SUMMARY

Consumers expect the meat they purchase to be free of health-threatening bacteria. Increasingly, though, we’ve learned that food products, particularly meats, may be contaminated with bacteria that pose serious health risks.

In October 2002, the U.S. experienced the largest recall of meat in its history. It was associated with 13 deaths and 120 illnesses. Overall, the Centers for Disease Control and Prevention (CDC) estimates that bacteria cause nearly 5.2 million foodborne infections each year, resulting in 36,000 hospitalizations and almost 1300 deaths. Most foodborne illness caused by bacteria gives victims a few days of intense discomfort and requires no treatment with antibiotics. But for patients whose infections spread beyond the intestine, antibiotics can be lifesaving.

For decades, antibiotics have dramatically reduced illness and death from bacterial infections. But recently, the effectiveness of these life-saving drugs has begun to wane because antibiotics are being overused.

Certainly antibiotics are overused in human medicine. Yet another major, and often overlooked, source of overuse is that factory farms routinely feed antibiotics to livestock to promote growth and to compensate for crowded, unsanitary conditions conducive to infection.

Scientific consensus now says that this antibiotic use in food animals contributes to antibiotic-resistant bacteria transferred to humans, mainly through contaminated food. The Union of Concerned Scientists estimates that 70 percent of all antibiotics in the U.S. are fed to pigs, poultry and cattle for reasons other than treating disease. The majority of such medicines are “medically important” – that is, identical, or nearly so to antibiotics used for humans.

Medical professionals are speaking out against this unnecessary use of antibiotics in food animals. If they can't rely upon effective antibiotics, it will become more difficult, and in some cases impossible, to treat bacterial illnesses. The American Medical Association (AMA) has gone on record opposing the use of antibiotics in farm animals that aren’t sick.

Given the current interest in foodborne illness and antibiotic resistance, this study focuses on determining the prevalence of antibiotic-resistant bacteria on poultry products routinely purchased at grocery stores. Consumers should know what bacteria may contaminate their food and the potential dangers of eating certain food products.

This is the first study to examine brand-name poultry products at the retail level for the presence of antibiotic-resistant bacteria, including resistance to medicines relied upon to treat human infections. We chose brand-name poultry products that were prominent in the grocery stores we visited. Ours is also the first study to test for drug resistance among multiple bacteria found on poultry products at the same time, arguably a better measure of risk to the people actually eating the poultry.

We bought 200 fresh whole chickens and 200 packages of ground turkey from grocery stores in Des Moines, Iowa and Minneapolis-St. Paul, Minnesota. We contracted with a certified food-testing laboratory to test the products for the presence of three bacterial strains – Salmonella, Enterococci and Campylobacter – and for resistance to a number of antibiotics.

Campylobacter and Salmonella are the top two bacterial causes of foodborne illness in the U.S. Together, they account for an estimated 3.3 million foodborne infections and more than 650 deaths each year. Not everyone is at the same level of risk. Infants are ten times more likely than the general population to contract Salmonella infections, and twice as likely as older people to suffer a Campylobacter infection.

Contaminated meat is the dominant source of human Salmonella infections, while 50 percent or more of Campylobacter infections may come from eating contaminated chicken, according to Food and Drug Administration (FDA) estimates.

Disease-causing bacteria, Salmonella or Campylobacter, contaminated a large proportion of the whole chickens and ground turkey we purchased. The widespread resistance of bacteria in poultry samples to one or multiple antibiotics is perhaps an even greater cause for concern.

• Ninety-five percent of the 100 whole chickens we tested were positive for Campylobacter, the top cause of bacterial foodborne illness, or food poisoning, in the U.S. Nearly 62 percent of the Campylobacter bacteria tested for resistance were resistant to 1 or more antibiotics.
• More than 8 percent of Campylobacter tested for resistance were resistant to Cipro, the antibiotic of choice for presumptively treating severe bacterial food poisoning. The FDA’s best estimate recently was that more than 153,000 people in 1999 alone contracted Cipro-resistant Campylobacter, just from eating contaminated chicken.
• Nearly 18 percent of whole chickens purchased were contaminated with Salmonella. Twenty percent of Country Pride chickens carried Salmonella, as did 15 percent of Gold’N Plump chickens. All 35 Salmonella isolated from whole chickens were analyzed for antibiotic resistance, and 6 percent were resistant to 4 or more antibiotics.
• Ground turkey purchased was more contaminated with Salmonella than was whole chicken, with an overall rate of 45 percent. Fifty-six percent of the Honeysuckle White ground turkey and 34 percent of the Jennie-O ground turkey carried Salmonella. Sixty-two percent of the Salmonella bacteria tested that were found in turkey were resistant to 1 or more antibiotics; a third of these Salmonella were resistant to 4 or more antibiotics.
• Both Salmonella and Campylobacter contaminated 32 percent of the Country Pride chickens and 14 percent of the Gold’N Plump chickens that we tested for both organisms (100 total), as well as 2 percent of the Jennie-O turkey we tested (1 of 51 packages)
• More than 90 percent of the Enterococci from chicken or turkey that was tested (101 total) for resistance was resistant to Synercid. Strains of resistant Enterococci are a growing cause of infections and deaths in hospitals, and Synercid is one of a few antibiotics still effective against them.

There are no good estimates of how many people overall suffer from foodborne infections resistant to antibiotics. As noted, more than 150,000 people may have developed fluoroquinolone-resistant Campylobacter infections just from eating contaminated chicken. Most antibiotic-resistant Salmonella in humans stems from eating contaminated food as well.

More people eating food contaminated with antibiotic-resistant Salmonella or Campylobacter will become ill than will people eating food with non-resistant organisms. One estimate is that the mere presence of Salmonella and Campylobacter strains resistant to at least one antibiotic could result in nearly 47,000 additional people getting foodborne illnesses, when compared to the expected number of sick following exposure to non-resistant strains.

In addition, people with antibiotic-resistant Salmonella and Campylobacter are likely to be sicker, for longer, than are people with non-resistant infections. Recommendations

Consuming meat with antibiotic-resistant bacteria is not inevitable. Consumers, poultry producers and restaurants can all take steps to reduce or eliminate these health threats. Poultry producers should reduce overall antibiotic use to a minimum. In addition, they should stop feeding antibiotics to birds or flocks that are not sick. Poultry producers also should stop using any antibiotic “cousins” of Cipro, which is simply too important to humans to risk its effectiveness by continuing the imprudent use of closely related drugs in poultry.

The good news is that some poultry producers are working hard to provide safer chickens and turkeys, by using better hygiene, by implementing growing or slaughter conditions to lower the levels of disease-causing bacteria on their meats, or by avoiding the use of antibiotics which increase the risk that meat will be contaminated with antibiotic-resistant bacteria.

Four of the top five top chicken producers already have sworn off any use of Cipro-like antibiotics, including ConAgra Poultry, producers of Country Pride chicken. Others, also including ConAgra, have made various claims to having stopped or greatly reduced the use of antibiotics for growth promotion or disease prophylaxis. We generally laud this approach, although there is no existing mechanism for verifying producers’ claims.

Large-volume buyers should only purchase poultry from producers that use no antibiotics for animals that are not sick, such as for growth promotion, and that use no critically important human antibiotics, like Cipro, for any reason. McDonald’s, Popeye’s and Wendy’s all now claim they refuse to buy chicken treated with Cipro-like antibiotics. Several other fast food companies, like Hardee’s, Subway and Domino’s, have similar policies, but also say they won’t buy chickens fed important human antibiotics for nontherapeutic reasons, like growth promotion.

For consumers to be certain of buying poultry raised without antibiotics, they can buy certified organic chickens and turkeys.

Some poultry producers use U.S. Department of Agriculture (USDA)-defined terms like “raised without antibiotics” or “no antibiotics administered” on their meat labels. Consumers can derive some assurance from these claims, although no third party certifies them, as is the case with organic products.

Check out the Eat Well Guide, www.iatp.org/EatWell, for a state-by-state listing of meat and poultry producers using no antibiotics, or no routine antibiotics, in addition to restaurants and other places to buy these products. If they are not available, consumers should ask grocery store or restaurant managers to provide this option. Consumers also should always cook meat thoroughly and carefully follow safe meathandling procedures. Consumers can find practical advice and general information on food safety at www.foodsafety.gov.

Antibiotics vs. Antimicrobials

Antibiotics are naturally occurring chemicals that kill or inhibit bacteria. But the term is often used more loosely to also include synthetic antibacterial agents, as well as compounds that affect other microorganisms, like parasites (technically “antimicrobials”).

Table 1: Prevalence of Salmonella and Campylobacter (in % of samples) on Raw Broiler Chickens and Ground Turkey Meat in Large U.S. Slaughterhouses Meeting USDA’s Standards Under HACCP, 1998-2001, and Compared to Baseline.

		 Salmonella                   	Campylobacter  (NT = not tested)
Year of Testing	 Whole Chicken	Ground Turkey	Whole Chicken	Ground Turkey
Baseline 	 20.0 		49.9 		88.2 		25.4
1998 		 10.8 		36.5 		NT 		NT
1999 		 9.3 		33.1 		NT 		NT
2000 		 7.5 		26.5 		NT 		NT
2001 		 9.7 		25.2 		NT 		NT

Source: Food Safety Inspection Service, U.S. Department of Agriculture, Progress Report on 
Salmonella Testing of Raw Meat and Poultry Products, 1998-2001, Accessed 11/23/02 at 
www.fsis.usda.gov/OPS/haccp/salm4year.htm.

Table 6: Antibiotic Resistance Summary for 35 Salmonella Isolates from Chicken, 45 Isolates from Turkey

				Whole Chicken 	Ground Turkey
Antibiotic 			% Resistant 	% Resistant
Amikacin			0.0% 		0.0%
Amoxicillin-clavulanic acid 	2.9% 		2.2%
Ampicillin 			2.9% 		0.0%
Cefoxitin 			0.0% 		2.2%
Ceftiofur 			0.0% 		0.0%
Ceftriaxone 			0.0% 		0.0%
Cephalothin 			0.0% 		2.2%
Chloramphenicol 		2.9% 		0.0%
Ciprofloxacin 			0.0% 		0.0%
Gentamicin 			2.9% 		35.6%
Kanamycin 			0.0% 		15.6%
Nalidixic acid 			0.0% 		0.0%
Streptomycin 			5.7% 		48.9%
Sulfamethoxazole 		5.7% 		42.2%
Tetracycline 			5.7% 		48.9%
Trimethoprim-sulfamethoxazole 	0.0% 		0.0%

Table 7: Antibiotic Resistance Summary for 49 Campylobacter Isolates from Poultry

		 % 		% 
Antibiotic 	 Resistant 	Intermediate
Azithromycin 	 2.0 		12.2
Chloramphenicol	 0.0 		0.0
Ciprofloxacin 	 8.2 		0.0
Clindamycin 	 2.0 		14.3
Erythromycin	 2.0 		22.4
Gentamicin 	 0.0 		2.0
Nalidixic acid   8.2 		0.0
Tetracycline 	 61.2 		0.0

ENDNOTES

1 Associated Press, “Largest Meat Recall in U.S. History Announced," (October 14, 2002).

2 Mead PS, L Slutsker, V Dietz, LF McCaig, JS Bresee, C Shapiro, PM Griffini, and RT Tauxe. Food-related illness and death in the United States. Emerg Infect Dis 5:607-625 (1999). http://www.cdc.gov/ncidod/EID/vol5no5/pdf/mead.pdf

3 Ibid.

4 Ibid.

5 Ibid.

6 Angulo F, K Johnson, R Tauxe, and M Cohen. Significance and sources of antimicrobial-resistant nontyphoidal Salmonella infections in the United States, Microbial Drug Resistance. 6(1): 77-83 (2000).

7 Smith K, et al. Quinolone-resistant Campylobacter jejuni infections in Minnesota, 1992 –1998. NEJM 340:1525-1532 (1999).

8 U.S. Food and Drug Administration, Center for Veterinary Medicine. The Human Health Impact of Fluoroquinolone Resistant Campylobacter Attributed to the Consumption of Chicken. Washington, DC, January 5, 2001. http://www.fda.gov/cvm/antimicrobial/revisedRA.pdf.

9 US Department of Agriculture, Food Safety Inspection Service, Science and Technology Microbiology Division. Nationwide broiler chicken microbiological baseline data collection program, July 1994-June 1995. Washington, DC: US Department of Agriculture, 1996. http://www.fsis.usda.gov/OPHS/baseline/contents.htm

10 Angulo F, K Johnson, R Tauxe, and M Cohen. Significance and sources of antimicrobial-resistant nontyphoidal Salmonella infections in the United States, Microbial Drug Resistance. 6(1): 77-83 (2000).

11 Swartz MN. Human diseases caused by foodborne pathogens of animal origin. Clin Infect Dis 34 (Suppl 3): S111-22 (2002).

12 Angulo F, K Johnson, R Tauxe, and M Cohen. Significance and sources of antimicrobial-resistant nontyphoidal Salmonella infections in the United States, Microbial Drug Resistance. 6(1): 77-83 (2000).

13 Smith K, et al. Quinolone-resistant Campylobacter jejuni infections in Minnesota, 1992 –1998. NEJM 340:1525-1532 (1999).

14 Travers K and M Barza. Morbidity of infections caused by antimicrobial-resistant bacteria. Clin Infect Dis 34 (Suppl 3): S131-4 (2002).

15 Barza M , SL Gorbach, Eds. The need to improve antimicrobial use in agriculture: ecological and human health consequences. Clin Infect Dis 34 (Suppl 3):S71-144 (2002). http://www.journals.uchicago.edu/CID/journal/contents/v34nS3.html  Accessed November 30, 2002.

16 Gorbach SL (editorial). Antimicrobial use in animal feed – time to stop. NEJM 345(16):1202-03 (2001).

17 Falkow S and D Kennedy (editorial). Antibiotics, animals, and people—again! Science 291:397 (2001).

18 World Health Organization, Department Of Communicable Disease Surveillance And Response, WHO Global Principles For The Containment Of Antimicrobial Resistance In Animals Intended For Food: Report of a WHO Consultation with the participation of the Food and Agriculture Organization of the United Nations and the Office International des Epizooties, Geneva, Switzerland, 5-9 June 2000.

19 Angulo F, K Johnson, R Tauxe, and M Cohen. Significance and sources of antimicrobial-resistant nontyphoidal Salmonella infections in the United States, Microbial Drug Resistance. 6(1): 77-83 (2000).

20 Witte W. Medical consequences of antibiotic use in agriculture. Science 279:996-7 (1998).

21 Tollefson L, SF Altekruse, ME Potter. Therapeutic antibiotics in animal feeds and antibiotic resistance, Rev Sci Tech 16:709-15 (1997).

22 Mellon M and S Fondriest. Union of Concerned Scientists. Hogging it: estimates of animal abuse in livestock. Nucleus 23:1-3 (2001). http://www.ucsusa.org, by choosing ”antibiotic resistance” and choosing report for right-hand menu. Accessed Aug. 28,2002.

23 Carnevale R, Presentation to the US Animal Health Association, November 2001; accessed on the website of the Animal Health Institute, www.ahi.org, November 27, 2002.

24 Chapman HD and ZB Johnson. Use of Antibiotics and Roxarsone in Broiler Chickens in the USA: Analysis for the Years 1995 to 2000, Poultry Science 81:356-364 (2000). 

[Mindfully.org note: Also see Effects of Dietary Roxarsone Supplementation, Lighting Program, and Season on the Incidence of Leg Abnormalities in Broiler Chickens Poultry Science 78:197-203 v.78, n.2, 1feb99]

25 Copeland C and J Zinn. Animal Waste Management and the Environment: Background for Current Issues, Report for Congress, Washington, D.C.: Congressional Research Service, 1998.

26 Ibid.

27 Chapman HD and ZB Johnson. Use of Antibiotics and Roxarsone in Broiler Chickens in the USA: Analysis for the Years 1995 to 2000, Poultry Science 81:356-364 (2000). Note: the industry database defines a poultry “plant” as a production unit in most cases representing a broiler complex comprising a group of individual farms, in a common geographical area, served by a single feed mill.

28 Ibid.

29 Mellon M and S Fondriest. Union of Concerned Scientists. Hogging it: estimates of animal abuse in livestock. Nucleus

23:1-3 (2001 ). http://www.ucsusa.org, by choosing ”antibiotic resistance” and choosing report for right-hand menu. Accessed Aug. 28,2002.

30 Ibid.

31 Carnevale R, Presentation to the US Animal Health Association, November 2001; accessed on the website of the Animal Health Institute, www.ahi.org, November 27, 2002.

32 US Department of Agriculture, Food Safety Inspection Service, Science and Technology Microbiology Division. Nationwide broiler chicken microbiological baseline data collection program, July 1994-June 1995. Washington, DC: US Department of Agriculture, 1996. Internet: http://www.fsis.usda.gov/OPHS/baseline/contents.htm.

33 US Department of Agriculture, Food Safety Inspection Service, Science and Technology Microbiology Division. Nationwide raw ground turkey microbiological survey. Washington, DC: US Department of Agriculture, May 1996. Internet: http://www.fsis.usda.gov/OPHS/baseline/contents.htm

34 US Department of Agriculture, Food Safety Inspection Service, Progress Report on Salmonella Testing of Raw Meat and Poultry Products, 1998-2001, accessed December 1, 2002 at: http://www.fsis.usda.gov/OPHS/haccp/salm4year.htm

35 Center for Science in the Public Interest, Field Guide to Safer Turkeys, accessed November 22, 2002 at www.cspinet.org/new/200211211.htm

36 White DG, S Zhao, and R Sudler, et al. The isolation of antibiotic-resistant Salmonella from retail ground meats. N Engl J Med 345:1147-54 (2001).

37 Ibid.

38 Smith K, et al. Quinolone-resistant Campylobacter jejuni infections in Minnesota, 1992 –1998. NEJM 340:1525-1532 (1999).

39 Preliminary data from the Centers for Disease Control and Prevention, National Antimicrobial [Antibiotic] Resistance Monitoring System for Human Enteric Bacteria:Summary: Antimicrobial [Antibiotic] Resistance of Campylobacter isolates, 1997-2001, Presented at the National Antimicrobial [Antibiotic] Resistance Monitoring Systems 2002 Annual Scientific Meeting in Hilton Head Island, SC, November 20, 2002.

40 U.S. Department of Health and Human Services, Food and Drug Administration (FDA), “Enrofloxacin for Poultry; Opportunity for Hearing,” 65 FR 64954-64965 (October 31, 2000).

41 McDermott PF, SM Bodels, LL English, et al. Ciprofloxacin resistance in Campylobacter jejuni evolves rapidly in chickens treated with fluoroquinolones. JID 185: 837-40 (2002).

42 Department of Health and Human Services, Food and Drug Administration. Enrofloxacin for Poultry; Opportunity for Hearing; Correction. 66 FR 6623-6624 (January 22, 2001).

43 MMWR Weekly, Outbreak of multidrug-resistant Salmonella newport --- United States, January—April 2002. 51(25):545-548 (June 28, 2002).

44 Chiu C-H, T-L Wu, L-H Su, et al. The emergence in Taiwan of fluoroquinolone resistance in Salmonella enterica serotype choleraesuis. NEJM 346:413-19 (2002).

45 Angulo F, K Johnson, R Tauxe, and M Cohen. Significance and sources of antimicrobial-resistant nontyphoidal Salmonella infections in the United States, Microbial Drug Resistance. 6(1): 77-83 (2000).

46 Molbak K, DL Baggesen, FM Aarestrup, et al. An outbreak of multidrug-resistant, quinolone-resistant Salmonella enterica serotype typhimurium DT104. NEJM 341:1420-5 (1999).

47 Holmberg SD, MT Ostereholm, KA Senger, and ML Cohen. Drug-resistant Salmonella from animals fed antimicrobials. NEJM 311:617-22 (1984).

48 Swartz MN. Human diseases caused by foodborne pathogens of animal origin. Clin Infect Dis 34 (Suppl 3): S111-22 (2002).

49 Angulo F, K Johnson, R Tauxe, and M Cohen. Significance and sources of antimicrobial-resistant nontyphoidal Salmonella infections in the United States, Microbial Drug Resistance. 6(1): 77-83 (2000).

50 Smith K, et al. Quinolone-resistant Campylobacter jejuni infections in Minnesota, 1992 –1998. NEJM 340:1525-1532 (1999).

51 McDermott PF, SM Bodels, LL English, et al. Ciprofloxacin resistance in Campylobacter jejuni evolves rapidly in chickens treated with fluoroquinolones. JID 185: 837-40 (2002).

52 Mattila L, H Peltola, A Siitonen, H Kyronseppa, I Simula, M Kataja. Short-term treatment of traveler’s diarrhea with norfloxacin: a double-blind, placebo-controlled study during two seasons. Clin Infect Dis 17:779-82 (1993).

53 Dunne EF, PD Fey, P Kludt, et al. Emergence of Domestically acquired ceftriaxone-resistant Salmonella infections associated with AmpC ß-lactamase. JAMA 284:3151-56 (2000).

54 Angulo F, K Johnson, R Tauxe, and M Cohen. Significance and sources of antimicrobial-resistant nontyphoidal Salmonella infections in the United States, Microbial Drug Resistance. 6(1): 77-83 (2000).

55 Ibid.

56 Travers K and M Barza. Morbidity of infections caused by antimicrobial-resistant bacteria. Clin Infect Dis 34 (Suppl 3): S131-4 (2002).

57 USDA Report to Congress, “FoodNet: An Active Surveillance System for Bacterial Foodborne Diseases in the United States” (1998) www.fsis.usda.gov/OPHS/rpcong09/rpcong98.htm.

58 T.B. Cleary, “Salmonella,” in Nelson Textbook of Pediatrics, 16th ed., eds. RE Behrman, RM Kliegman, HB Jenson Philadelphia: Saunders, 842-48 (2000).

59 Shea K, K Florini, and T Barlam. When Wonder Drugs Don’t Work: How Antibiotic Resistance Threatens Children, Seniors, and the Medically Vulnerable, Environmental Defense: Washington, D.C. (2001). http://www.environmentaldefense.org/documents/162_ABRreport.pdf.

60 Barza M and K Travers. Excess infections due to antimicrobial resistance: the “attributable fraction”. CID 34(Suppl 3):126-130 (2002).

61 Barza M and K Travers. Excess infections due to antimicrobial resistance: the “attributable fraction”. CID 34(Suppl 3):126-130 (2002).

62 Swartz MN. Human diseases caused by foodborne pathogens of animal origin. Clin Infect Dis 34 (Suppl 3): S111-22 (2002).

63 Sorenson TL, M Blom, DL Monnett, N Frimodt-Moller, RL Poulsen, and F Espersen. Transient intestinal carriage after ingestion of antibiotic-resistant Enterococcus faecium from chicken and pork. NEJM 345:1161-6 (2001).

64 Mcclellan J, K Joyce, S Rossiter, T Barrett, and F Angulo. High-level Gentamicin resistant enterococci and quinupristin/dalfopristin resistant E. faecium from ground pork purchased from grocery stores. The 41rst Interscience Conference on Antimicrobial Agents and Chemotherapy (ICAAC) annual meeting. Chicago, IL 2001. Accessed at: http://www.cdc.gov/narms/pub/presentations/icaac/2001/mcclellan_j.htm.

65 McDonald LC, S Rossiter, C Mackinson, et al. Quinipristin-dalfopristin-resistant Enterococcus faecium on chicken and in human stool specimens. NEJM 345:1155-60 (2001).

66 Sorenson TL, M Blom, DL Monnett, N Frimodt-Moller, RL Poulsen, and F Espersen. Transient intestinal carriage after ingestion of antibiotic-resistant Enterococcus faecium from chicken and pork. NEJM 345:1161-6 (2001).

67 Angulo F, N Marano, S Johnson, C Mackinson, L Gilbert, M Park, E Debess, B Taylor, J Madden, B Hill, K Joyce, F Tenover, and L Archibald. EIP enterococci study: monitoring for the seeds of antimicrobial resistance in the food supply. Presentation to the 2nd International Conference on Emerging Infectious Diseases, Atlanta, GA, July 2000. http://www.cdc.gov/narms.

68 McDonald LC, S Rossiter, C Mackinson, et al. Quinipristin-dalfopristin-resistant Enterococcus faecium on chicken and in human stool specimens. NEJM 345:1155-60 (2001).

69 Angulo F, K Johnson, R Tauxe, and M Cohen. Significance and sources of antimicrobial-resistant nontyphoidal Salmonella infections in the United States, Microbial Drug Resistance. 6(1): 77-83 (2000).

70 U.S. Department of Agriculture, Food Safety and Inspection Service, Progress Report on Salmonella Testing of Raw Meat and Poultry Products, 1998-2001, accessed 11/25/02 at: http://www.fsis.usda.gov/OPHS/haccp/salm4year.htm

71 Angulo F, K Johnson, R Tauxe, and M Cohen. Significance and sources of antimicrobial-resistant nontyphoidal Salmonella infections in the United States, Microbial Drug Resistance. 6(1): 77-83 (2000).

72 Mellon M and S Fondriest. Union of Concerned Scientists. Hogging it: estimates of animal abuse in livestock. Nucleus 23:1-3 (2001). http://www.ucsusa.org, by choosing ”antibiotic resistance” and choosing report for right-hand menu. Accessed Aug. 28,2002.

73 Angulo F, K Johnson, R Tauxe, and M Cohen. Significance and sources of antimicrobial-resistant nontyphoidal Salmonella infections in the United States, Microbial Drug Resistance. 6(1): 77-83 (2000).

74 Dunne, EF, PD Fey, P Kludt, R Reporter, F Mostashari, P Shillam, J Wickland, C Miller, B Holland, K Starney, TJ Barrett, FC Tenover, E Ribot, and FJ Angulo. Emergence of domestically acquired ceftriaxone-resistent Salmonella infections associated with ampc B-lactamase. JAMA 284: 3151-3156 (2000).

75 Federal Register, Enrofloxican for Poultry; Opportunity for Hearing, 64954-64965 (October 31, 2000).

76 Fey, PD, TJ Safranek, ME Rupp, EF Dunne, E Ribot, PC Iwen, PA Bradford, FJ Angulo and SH Hinrichs. Ceftriaxoneresistant salmonella infection acquired by a child from cattle. NEJM 342: 1242-1249 (2000).

77 Levy, SB, GB Fitzgerald, and AB Macone. Changes in intestinal flora of farm personnel after introduction of a tetracycline-supplemented feed on a farm. NEJM 295(11): 583-588 (1976).

78 Institute of Medicine. Human health risks with the subtherapeutic use of penicillin or tetracycline in animal feeds. National Academy Press. 1989.

79 Department of Health and Human Services, Food and Drug Administration. Enrofloxacin for Poultry; Opportunity for Hearing; Correction. 66 FR 6623-6624 (January 22, 2001).

80 For more information on USDA-defined labels, see www.eco-label.org

81 Burros M, “Poultry Industry Quietly Cuts Back on Antibiotic Use,” The New York Times (February 10, 2002).

82 Recent Statements on Antibiotic Use by Major Restaurant Chains, Compiled by Keep Antibiotics Working as of October 1, 2002, accessed November 25, 2002 at: http://www.iatp.org/antibiotics/library/uploadedfiles/Recent_Statements_on_Antibiotic_Use_by_Major_R.htm

source: www.iatp.org/foodandhealth/library/admin/uploadedfiles/showfile.cfm?FileName=Poultry_on_Antibiotics_Hazards_to_Human_Health.pdf 14may03