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HUMAN AND ENVIRONMENTAL HEALTH RISKS FROM ANTIMICROBIALLY RESISTANT BACTERIA IN FOOD ANIMAL PRODUCTION SYSTEMS

Published by the American Society of Agricultural and Biological Engineers, St. Joseph, Michigan www.asabe.org

Citation:  Pp. 667-720 in Animal Agriculture and the Environment: National Center for Manure and Animal Waste Management White Papers. J. M. Rice, D. F. Caldwell, F. J. Humenik, eds. 2006. St. Joseph, Michigan: ASABE.  .(doi:10.13031/2013.20269)
Authors:   Lisa Casanova, Mark D. Sobsey

Unquestionably, antibiotics rank among the great achievements of human medicine. Although they provided great success in treating deadly bacterial infections, it did not take long for the miracle of antibiotics to meet the reality of biological mutation and evolution. Resistance to antibiotics appeared soon after use began in the 1930s (Aarestrup et al., 1998a), with the discovery of a penicillin- hydrolyzing enzyme in E. coli (Farrington et al., 1999). Since then, the ability of bacteria to mutate, evolve and adapt has kept pace with the development of new drugs, in part because of our own use and misuse of these drugs. In the fight against antibiotic resistant bacteria, we have met the enemy, and he is us. The selective pressure that drives the development and maintenance of antibiotic resistance traits comes from our own use of antibiotics. Human and animal Salmonella collected from 1940-48 were sensitive to tetracycline, but resistance has been rising ever since (Teuber, 1999). Houndt and Ochman (2000) demonstrated this when they gathered antibiotic susceptibility data on a collection of E. coli amassed from 1885 to 1941, before the widespread use of antibiotics (the pre-antibiotic era), and a collection of human and animal E. coli and Salmonella collected since 1958, after the advent of antibiotic use (the post-antibiotic era). When isolates from the pre- and post-antibiotic era were compared, both background and high-level resistance to ampicillin, chloramphenicol, kanamycin, and tetracycline increased in bacteria from the post-antibiotic era. They concluded that Application of antibiotics over the past 50 years has resulted in an unremitting increase in the numbers of commensal and pathogenic bacteria that are resistant to antimicrobial compounds.

Part of this application of antibiotics is in human medicine. Baquero et al. (1998) stated that Daily clinical experience suggests that there is a certain link between the use of antibiotics and the selection of resistance. Their own studies demonstrate a relationship between the number of days patients receive antibiotics and colonization or infection with methicillin-resistant S. aureus. Cephalosporin use in hospitals can select for enterococci resistant to vancomycin, creating difficultto- treat enterococcal infections (Bonten, 2001; Mundy, 2000), and vancomycin use is a risk factor for colonization with vancomycin-resistant enterococci (VRE) (Cetinkaya et al., 2000). Although the link between antibiotic use in medicine and antibiotic resistance is well recognized, antibiotics produced in the United States and worldwide are not used solely for human disease therapy. They have been used for decades in the production of animals for food, including for therapy, disease prevention, and growth promotion.

As the contribution of human antibiotic use to the development of resistance was realized, the contribution of agriculture use to the problem began to be recognized as well. This recognition led to the hypothesis that antibiotic resistance develops as a result of both human and animal antibiotic use (Aarestrup et al., 1999; Baquero et al., 1998). Lipsitch (2002) described antibiotic resistance as a population-level phenomenon, where Members of a population experience indirect effects of antimicrobial use, defined as the enhancement of risk for acquiring a resistant organism, because of the use of antimicrobials by other persons in the group or population. In this sense, humans and animals can be looked at as members of one population, whose use of antimicrobials is interrelated with respect to acquisition from exposure.

The contribution of agricultural antibiotic use to the problem of bacterial resistance first received serious attention in 1969 with the publication of the report of the Joint Committee on the Use of Antibiotics in Animal Husbandry and Veterinary Medicine (the Swann Report) in Britain. The committee recommended that antibiotic use in animals be restricted to three conditions: the drugs are of economic value in livestock production under U.K. farming conditions, they have little or no application as therapeutic agents in humans or animals, and they will not impair the efficacy of a prescribed therapeutic drug or drugs through the development of resistant strains of organisms (http://www.defra.gov.uk/news/vpc/vpc299.htm). These recommendations were not heeded in the decades that followed, resulting in the continued development of antibiotic resistant bacteria in animals to drugs that are used to treat humans. The continued widespread use of antibiotics in livestock production has sparked an intense debate spanning the nearly 30 years since the Swann report over whether this practice may expose the general population to antibiotic resistant bacteria through the food chain, especially via contamination of meat products with resistant organisms harbored by food animals (Berends et al., 2001).

The nature and magnitude of the human health risk from antibiotic bacteria in agricultural animals, and what, if any, actions should be taken to minimize or prevent this risk remains a controversy in the scientific, public health and agricultural communities. Opinion on the issue ranges from a 2001 editorial in the New England Journal of Medicine, Antimicrobial Use in Animal Feed Its Time to Stop (Gorbach, 2001) to letters such as one in the Veterinary Record asserting that Four antibiotic feed additives are about to be banned throughout the EU for reasons admitted to be political even though there is no evidence, after many years of use, that they have led to the increase in antibiotic resistance (Sainsbury, 1999). Reviews on the subject of human health risks can reach differing conclusions. Angulo et al. (2004) concluded that there is evidence that resistant enteric bacteria have human health consequences, and that the acquisition of these microorganisms places people at risk. Phillips et al. (2004), concluded that ...Whereas resistance is undoubtedly selected in man and animals by the use of antibiotics...little additional harm results from resistance, even when infection supervenes. It should be noted that the conclusions of Phillips and colleagues have been criticized on several grounds (Chiller et al., 2004; Jensen et al., 2004; Karp and Engberg, 2004; Tollefson, 2004). Between these two extremes there are a range of views, supporting positions from continuation of current antibiotic use practices to outright bans on certain antibiotics in agriculture.

The American Medical Association acknowledged that restrictions on agricultural antimicrobial use might be necessary, but with a caveat. The AMA adopted a resolution that non-therapeutic use in animals of antimicrobials (that are also used in humans) should be terminated or phased out based on scientifically sound risk assessments (Kahler, 2001). Tools to carry out assessments of risk are available to us (Alban et al., 2002; Anderson et al., 2001; Cox and Popken 2004a,b; Hurd et al., 2004; Smith, 2003). While the tools continue to be improved and refined, the basic underpinning of any scientifically sound risk assessment intended to inform policy is quality data (Snary et al., 2004). In recent years, a sizeable body of literature has developed on agricultural antibiotic use and bacterial antibiotic resistance that can provide us with this kind of data. The purpose of this review is to provide an overview of current knowledge of agricultural antibiotic use, its contribution to bacterial resistance, and the possible risks to human health.

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