Antimicrobial Resistance: Implications for the Food System Microorganisms have an inherent ability to evolve—to mutate and adapt to environmental stressors─allowing them to survive otherwise lethal conditions.

IFT convened a panel of internationally renowned experts to address the concern that the use of antimicrobials in food production, manufacturing, and elsewhere may lead to the emergence of foodborne pathogens that are resistant to antimicrobials, thus compromising the ability to subsequently control them, whether in production agriculture, food processing, or human medicine.

August 2, 2006

ABSTRACT

The safety of food worldwide remains challenged by the potential for emergence of new pathogens and re-emergence of known pathogens. Microorganisms have an inherent ability to evolve–to mutate and adapt to environmental stressors–allowing them to survive otherwise lethal conditions. The Institute of Food Technologists (IFT),1 the 22000-member nonprofit scientific and educational society, convened a panel of internationally renowned experts to address the concern that the use of antimicrobials in food production, manufacturing, and elsewhere may lead to the emergence of foodborne pathogens that are resistant to antimicrobials, thus compromising the ability to subsequently control them, whether in production agriculture, food processing, or human medicine. The outcome of the panel's deliberations is presented in this Expert Report. IFT's objective for this Expert Report is to increase the understanding–among IFT members, senior policy officials, and other interested groups–of the state of the science on the public health impact of the use of antimicrobials in the food system, and development and control of antimicrobial resistance. This report is the fourth Expert Report produced by IFT.


DIGITAL OBJECT IDENTIFIER (DOI) 10.1111/j.1541-4337.2006.00004.x

Introduction

The availability of antibiotics to treat infectious diseases has radically improved human and animal well being, and to a minor degree, plant health. Paradoxically, this very success threatens the future utility of antibiotics. The discovery of penicillin in 1940 ushered in the era of "modern medicine." Numerous antimicrobials, including most structural classes of antibiotics were discovered during 1920 to 1970. Chemical modification of many of these compounds led to new entities with superior activities. Because of the great success in antibiotic discovery, by the late 1970s, many proclaimed that the war on infectious diseases had been won, leading ultimately to de-emphasis of antibiotic discovery during the 1980s and a decline in the 1990s. At the same time, however, widespread antibiotic resistance was emerging and resulting in impaired treatment of human diseases (Neu 1992). As the genomes of bacteria, especially pathogens, have become increasingly available, the prospect of using them to identify new targets for antibiotic discovery has renewed interest in such investigations between the public sector and large pharmaceutical and biotechnology companies. Many of the larger companies and much of the public sector, however, have redirected research efforts toward noninfectious disease targets.

All uses of antibiotics in human medicine and animal husbandry create selective pressure that favors emergence of antibiotic resistance among microorganisms, which could undermine the effectiveness of the antibiotics and potentially give rise to a "postantibiotic" era. The selection for antibiotic-resistant bacteria in agricultural production environments and the subsequent impact on animal and human health has become a major concern and is the subject of many reports (Table 1). This document focuses on the use of antimicrobial agents to control bacteria in the food system; other microorganisms are considered as well, however. This document builds upon the IFT Scientific Status Summary "Resistance and Adaptation to Food Antimicrobials, Sanitizers, and Other Process Controls" (IFT 2002a), to inform readers about the various types of antimicrobial agents, including antibiotics, food antimicrobial agents, and sanitizers that are used at various stages of the food system, and the mechanisms that microorganisms, particularly foodborne pathogens, have for surviving the stress of exposure to these substances in their environments. Trends in antimicrobial resistance, and the resultant human health, economic, and clinically relevant environmental impacts are also addressed.

Table 1–Reports of antimicrobial use, resistance, and human health impact

1969. English Parliament, United Kingdom. The Report to Parliament by the Joint Committee on Antibiotic Uses in Animal Husbandry and Veterinary Medicine ("Swann Report").

1980. National Research Council (NRC), United States. The Effects on Human Health of Subtherapeutic Use of Antimicrobials in Animal Feed. http://fermat.nap.edu/ catalog/21.html

1981. Council for Agricultural Science & Technology, United States. Antibiotics in Animal Feeds, Report 88.

1981. Institute of Medicine (IOM), United States. Human Health Risks with the Subtherapeutic Use of Penicillin or Tetracyclines in Animal Feed.

1989. IOM Committee on Human Health Risk Assessment of Using Subtherapeutic Antibiotics in Animals, United States. Human Health Risks with the Subtherapeutic Use of Penicillin or Tetracyclines in Animal Feeds.

1997. World Health Organization (WHO), International. The Medical Impact of the Use of Antimicrobials in Food Animals. http://whqlibdoc.who.int/hq/1997/WHO_EMC_ZOO_97.4.pdf

1998. UK Ministry of Agriculture, Fisheries, and Food, United Kingdom. A Review of Antimicrobial Resistance in the Food Chain.

1998. United States Food and Drug Administration (FDA) Center for Veterinary Medicine (CVM), United States. A proposed framework for evaluating and assuring the human safety of the microbial effects of antimicrobial new drugs intended for use in food-producing animals. http://www.fda.gov/cvm/ VMAC/antimi18.html

1998. WHO, International. Use of Quinolones in Food Animals and Potential Impact on Human Health: Report and Proceedings of a WHO Meeting. http://www.who.int/bookorders/

1999. The European Agency for the Evaluation of Medicinal products, European Union. Antibiotic Resistance in the European Union Associated with Therapeutic Use of Veterinary Medicines.

1999. EU Scientific Steering Committee, European Union. Opinion of the Scientific Steering Committee on Antimicrobial Resistance. http://www.europa.eu.int/comm/dg24/health/sc/ssc/out50_en.html

1999. FDA, United States. Risk Assessment on the Human Health Impact of Fluoroquinolone-resistant Campylobacter Associated with Consumption of Chicken. http://www.fda.gov/cvm/Risk_asses.htm (revised as of Jan 5 2001).

1999. NRC National Academy of Sciences Committee on Drug Use in Food Animals and the Panel on Animal Health, Food Safety, and Public Health, United States. The Use of Drugs in Food Animals: Benefits and Risks. Benefits and Risks http://fermat.nap.edu/catalog/5137.html

1999. U.S. General Accounting Office (GAO), United States. Food Safety: The Agricultural Use of Antibiotics and Its Implications for Human Health. Antibiotics and Its Implications for Human Health http://www.gao.gov/archive/1999/rc99074.pdf

1999. Advisory Committee on the Microbiological Safety of Food, United Kingdom. Report on Microbial Antibiotic Resistance in Relation to Food Safety. http://www.poultry-health.com/library/antimicrobials/acmsf996.htm (a synopsis)

1999. Joint Expert Advisory Committee on Antibiotic Resistance, Australia. The Use of Antibiotics in Food-Producing Animals: Antibiotic Resistant Bacteria in Animals and Humans. http://www.health.gov.au/

1999. European Commission, European Union. Opinion of the Scientific Steering Committee on Antimicrobial Resistance, May 28, 1999.

1999. WHO, International. The Medical Impact of the Use of Antimicrobials in Food Animals.

2000. Centers for Disease Control and Prevention Interagency Task Force on Antimicrobial Resistance, United States. Disease Control and Prevention Interagency Task Force on Antimicrobial Resistance A Public Action Health Plan to Combat Antimicrobial Resistance. http://www.cdc.gov/drugresistance/actionplan/

2000. WHO, International. WHO Global Principles for the Containment of Antimicrobial Resistance in Animals Intended for Food. http://www.who.int/salmsurv/links/en/GSSGlobalPrinciples2000.pdf

2000. Food and Agriculture Organization of the United Nations (FAO)/WHO Codex Committee on Residues of Veterinary Drugs in Foods, International. Antimicrobial Resistance and the Use of Antimicrobials in Animal Production. ftp://ftp.fao.org/codex/ccrvdf12/rv00_04e.pdf

2001. Office International Des Epizooties (OIE), International. Antimicrobial Resistance: Reports prepared by the OIE Ad Hoc Group of Experts on Antimicrobial Resistance. prepared by the OIE Ad Hoc Group of Experts on Antimicrobial Resistance http://www.oie.int/eng/publicat/ouvrages/a_106.htm

2001. WHO, International. WHO Global Strategy for Containment of Antimicrobial Resistance. Antimicrobial Resistance http://www.who.int/drugresistance/WHO_Global_Strategy_English.pdf

2001. WHO, International. Monitoring Antimicrobial Usage in Food Animals for the Protection of Human Health. http://www.who.int/salmsurv/links/en/GSSMontitoring AMRuseOslo.pdf

2002. Alliance for the Prudent Use of Antibiotics, United States. The Need to Improve Antimicrobial Use in Agriculture: Ecological and Human Health Consequences ("FAAIR Report"). http://www.journals.uchicago.edu/CID/journal/contents/v34nS3.html

2002. Veterinary Drugs Directorate, Health Canada Report of the Advisory Committee on Animal Uses of Antimicrobials and Impact on Resistance and Human Health, Canada. Uses of Antimicrobials in Food Animals in Canada: Impact on Resistance and Human Health. http://www.hc-sc.gc.ca/dhp-mps/alt_formats/hpfb-dgpsa/pdf/pubs/amr-ram_final_report-rapport_06-27_e.pdf

2003. WHO Department of Communicable Diseases, Prevention and Eradication and Collaborating Centre for Antimicrobial Resistance in Foodborne Pathogens, International. Impacts of Antimicrobial Growth Promoter Termination in Denmark. http://www.who.int/salmsurv/en/Expertsreportgrowthpromoterdenmark.pdf

2004. FAO, OIE, and WHO, International. Joint FAO/OIE/WHO Workshop on Non-Human Antimicrobial Usage and Antimicrobial Resistance: Scientific Assessment. http://www.who.int/foodsafety/publications/micro/en/amr.pdf

2004. FAO, OIE, and WHO, International. Second Joint FAO/OIE/WHO Expert Workshop on Non-Human Antimicrobial Usage and Antimicrobial Resistance: Management Options. http://www.who.int/foodsafety/publications/micro/en/oslo_report.pdf

2004. GAO, United States. Federal Agencies Need to Better Focus Efforts to Address Risk to Humans from Antibiotic Use in Animals. http://www.gao.gov/highlights/d04490high.pdf