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M. = Mycobacterium; Stent. = Stenotrophomonas ..... K. F. Barker, D. James, and R. C. George. 2000. ... Snary, E. L., L. A. Kelly, H. C. Davison, C. J. Teale, and W.
Identification and Surveillance of Antimicrobial Resistance Dissemination in Animal Production R. J. Bywater1 Bywater Consultancy, Little Common House, Clungunford, Shropshire, SY7 0PL, United Kingdom ABSTRACT Antimicrobial resistance is a growing problem in human medicine, and concern has been expressed that use of antimicrobials in animals may be a contributing factor. Although the majority of human pathogens showing antibiotic resistance have no link with animals, the issue of animal use of antimicrobials remains controversial, particularly with respect to antibiotic growth promoters (AGP). The European Union (EU) has withdrawn as AGP some compounds that remain in use in the United Sates. This difference in availability allows comparisons to be made of antimicrobial resistance outcomes with and without use of an AGP. Such comparisons

so far show little apparent measurable benefit to human health resulting from the EU removal of AGP, and there is evidence of increased use of therapeutic antibiotics in animals to treat an apparent increased incidence of clinical disease. Microbial risk assessments are important in judging quantitatively or qualitatively whether the risk of using a particular AGP is acceptable in terms of potential hazard to human health. Resistance surveillance is an essential part of such microbial risk assessments, but such surveillance should be carefully planned to avoid confounding factors that could invalidate any conclusions.

(Key words: antibiotic resistance, surveillance, risk assessment, growth promoters) 2005 Poultry Science 84:644–468

ANTIMICROBIAL AGENTS IN ANIMAL PRODUCTION

INTRODUCTION Antimicrobial resistance is an increasing problem in human medicine, and although it is recognized that this results mainly from antimicrobial use in human medicine, there has been concern that the use in animals may result in microbial resistance that could transfer to human pathogens. Antimicrobials are used in animals for treatment, disease prevention, and growth promotion, and the last of these has been subject to different approaches in Europe and the United States. Antimicrobial growth promoters (AGP) are contentious, and the World Health Organisation has recommended (1997) that they should be phased out and replaced with alternatives. In the European Union (EU) this has begun to occur with a process of removal to be completed in 2006, but AGP continue to be used in the United States. Evidence that antibiotic use in animals is a major threat to human health remains sparse (Phillips et al., 2004), but there is a need for resistance surveillance in animals to explore the epidemiology of resistance dissemination. Application of microbial risk assessment (Snary et al., 2004) can determine whether or not there is real justification for concern with respect to a particular AGP.

What is the Contribution of Animal Sources to Resistance Among Human Pathogens? One approach has been to direct a questionnaire to informed experts (Bywater and Casewell, 2000). This questionnaire was used to identify and prioritize the organisms most threatening to human health through antibiotic resistance and to estimate the perceived contribution from animal sources for each bacterial species. The experts involved were senior clinical medical microbiologists from the United States and Europe, and the results are shown in Figure 1. This survey suggests that the most important resistant pathogens such as methicillin-resistant Staphylococcus aureus were unrelated to animal sources, whereas those organisms for which there were possible animal sources of resistance were those viewed as less problematic. Organisms with a possible animal link were mainly zoonotic bacteria for which there is an obvious possibility that a resistant animal infection may be contracted by a human recipient. In total the perceived contribution from animals amounted to less than 4% of the overall human resistance problem.

2005 Poultry Science Association, Inc. Received for publication August 2, 2004. Accepted for publication September 16, 2004. 1 To whom correspondence should be addressed: rbywater@ onetel.com.

Abbreviation Key: AGP = antibiotic growth promoter; EU = European Union; VRE = vancomycin-resistant enterococcus.

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SYMPOSIUM: ANTIBIOTICS IN ANIMAL FEEDS: ARE THERE VIABLE ALTERNATIVES?

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Tetracyclines. The use of these compounds as AGP was ended in Europe in the 1970s, but they continue to be available for this purpose in the United States.

Background of the EU Ban

FIGURE 1. Perceived contribution (%) of individual bacterial species of possible animal sources to the overall problem of antimicrobial resistance in humans (Bywater and Casewell, 2000). MRSA = methicillinresistant Staphylococcus aureus; Ps. = Pseudomonas; S. = Streptococcus; M. = Mycobacterium; Stent. = Stenotrophomonas; N. = Neisseria; GI = gastrointestinal; UTI = urinary tract infection; Non-typh.= non-typhoid.

Antibiotic Use in Poultry The poultry industry has been outstandingly successful in transforming an industry based originally on small individual producers into an industry based on largescale, efficient units. Antimicrobials have been a factor in the success of the industry, whether for treatment of disease outbreaks, prevention of disease by group medication in the face of existing disease (metaphylaxis), or potential disease (prophylaxis). The final and most contentious use of antibiotics is for health maintenance or growth promotion, although the proportion used for this purpose (estimated as