Journal of Biomedicine and Biotechnology
Volume 2010 (2010), Article ID 180682, 12 pages
doi:10.1155/2010/180682
Review Article
Role of Antimicrobial Selective Pressure and Secondary Factors on Antimicrobial Resistance Prevalence in Escherichia coli from Food-Producing Animals in Japan
1National Veterinary Assay Laboratory, Ministry of Agriculture, Forestry and Fisheries, 1-15-1 Tokura, Kokubunji, Tokyo 185-8511, Japan
2Department of Veterinary Microbiology, Nippon Veterinary and Life Science University, 1-7-1 Kyonan, Musashino, Tokyo 180-8602, Japan
Received 8 December 2009; Accepted 16 March 2010
Academic Editor: John E. Degener
Copyright © 2010 Kazuki Harada and Tetsuo Asai. This is an open access article distributed under the
Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Linked References
- F. M. Aarestrup, “Association between the consumption of antimicrobial agents in animal husbandry and the occurrence of resistant bacteria among food animals,” International Journal of Antimicrobial Agents, vol. 12, no. 4, pp. 279–285, 1999. View at Publisher · View at Google Scholar
- S. Schwarz, C. Kehrenberg, and T. R. Walsh, “Use of antimicrobial agents in veterinary medicine and food animal production,” International Journal of Antimicrobial Agents, vol. 17, no. 6, pp. 431–437, 2001. View at Publisher · View at Google Scholar
- Anonymous, Report of the Joint Committee on the Use of Antibiotics in Animal Husbandry and Veterinary Medicine, HMSO, London, UK, 1969.
- T. Asai, “Antimicrobial usage and resistant bacteria in food-producing animals,” Annual report of the National Veterinary Assay Laboratory, vol. 42, pp. 1–8, 2005.
- P. Dehaumont, “OIE international standards on antimicrobial resistance,” Journal of Veterinary Medicine Series B, vol. 51, no. 8-9, pp. 411–414, 2004. View at Publisher · View at Google Scholar · View at PubMed
- S. H. Doyran, “Risk analysis of antibiotic resistance, Berlin, BfR, 10-12 November 2003: activities of the codex alimentarius commission related to antibiotic resistance,” Journal of Veterinary Medicine Series B, vol. 51, no. 8-9, pp. 408–410, 2004. View at Publisher · View at Google Scholar · View at PubMed
- World Organisation for Animal Health (OIE), “OIE guidelines on antimicrobial resistance: reports prepared by the OIE Ad hoc group of experts on antimicrobial resistance,” Revue Scientifique et Technique (International Office of Epizootics), vol. 20, pp. 797–870, 2003.
- FAO/OIE/WHO, “Joint FAO/OIE/WHO expert workshop on non-human antimicrobial usage and antimicrobial resistance: scientific assessment,” 2004, http://www.who.int/foodsafety/publications/micro/en/amr.pdf.
- FAO/OIE/WHO, “Second joint FAO/OIE/WHO expert workshop on non-human antimicrobial usage and antimicrobial resistance: management options,” 2004, http://www.who.int/foodsafety/publications/micro/en/oslo_report.pdf.
- Y. Tamura, “The Japanese veterinary antimicrobial resistance monitoring system (JVARM),” in OIE international standards on Antimicrobial Resistance, V. Bernard, Ed., pp. 206–210, OIE (World organization for animal health), Paris, France, 2003.
- Y. Tamura, “Trends in antimicrobial agents for veterinary use and control measures of antimicrobial resistance,” Journal of the Japan Veterinary Medical Association, vol. 56, pp. 685–691, 2003.
- A. A. Valois, Y. S. Endoh, K. Grein, and L. Tollefson, “Geographical differences in market availability, regulation and use of antimicrobial products,” in Guide to Antimicrobial Use in Animals, L. Guardabassi, L. B. Jensen, and H. Kruse, Eds., pp. 59–76, Willey-Blackwell, Bognor, UK, 2008.
- FAO/WHO/OIE, “Joint FAO/OIE/WHO Expert Meeting on Critically Important Antimicrobials,” Report of a meeting held in FAO, Rome, Italy, November 2007, Geneva, Switzerland, 2008, http://www.who.int/foodborne_disease/resources/Report%20joint%20CIA%20Meeting.pdf.
- T. Asai, A. Kojima, K. Harada, K. Ishihara, T. Takahashi, and Y. Tamura, “Correlation between the usage volume of veterinary therapeutic antimicrobials and resistance in Escherichia coli isolated from the feces of food-producing animals in Japan,” Japanese Journal of Infectious Diseases, vol. 58, no. 6, pp. 369–372, 2005.
- DANMAP, “DANMAP 2001 Use of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Bacteria from Food Animals, Foods and Humans in Denmark,” 2002, http://www.danmap.org/pdfFiles/Danmap_2001.pdf.
- K. Harada, T. Asai, A. Kojima, K. Ishihara, and T. Takashi, “Role of coresistance in the development of resistance to chloramphenicol in Escherichia coli isolated from sick cattle and pigs,” American Journal of Veterinary Research, vol. 67, no. 2, pp. 230–235, 2006. View at Publisher · View at Google Scholar · View at PubMed
- M. Kijima-Tanaka, K. Ishihara, A. Morioka, et al., “A national surveillance of antimicrobial resistance in Escherichia coli isolated from food-producing animals in Japan,” Journal of Antimicrobial Chemotherapy, vol. 51, no. 2, pp. 447–451, 2003. View at Publisher · View at Google Scholar
- T. Asai, H. Esaki, A. Kojima, K. Ishihara, Y. Tamura, and T. Takahashi, “Antimicrobial resistance in Salmonella isolates from apparently healthy food-producing animal from 2000 to 2003: the first stage of Japanese Veterinary Antimicrobial Resistance Monitoring (JVARM),” Journal of Veterinary Medical Science, vol. 68, no. 8, pp. 881–884, 2006. View at Publisher · View at Google Scholar
- A. Kojima, A. Morioka, M. Kijima, et al., “Classification and antimicrobial susceptibilities of Enterococcus species isolated from apparently healthy food-producing animals in Japan,” Zoonoses and Public Health, vol. 57, no. 2, pp. 137–141, 2010. View at Publisher · View at Google Scholar · View at PubMed
- T. Asai , R. Koike, A. Kojima, et al., “An epidemiological study of antimicrobial resistance in bacteria isolated from domestic animals in Japan,” Reports from National Veterinary Assay Laboratory, vol. 45, pp. 45–52, 2008.
- R. S. Sayah, J. B. Kaneene, Y. Johnson, and R. Miller, “Patterns of antimicrobial resistance observed in Escherichia coli isolates obtained from domestic- and wild-animal fecal samples, human septage, and surface water,” Applied and Environmental Microbiology, vol. 71, no. 3, pp. 1394–1404, 2005. View at Publisher · View at Google Scholar · View at PubMed
- CIPARS, “CIPARS 2005 Canadian Integrated Program for Antimicrobial Resistance Surveillance,” Public Health Agency of Canada, 2006, http://www.phac-aspc.gc.ca/cipars-picra/pdf/cipars-picra-2005_e.pdf.
- DANMAP, “DANMAP 2006 Use of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Bacteria from Food Animals, Foods and Humans in Denmark,” 2007, http://www.danmap.org/pdfFiles/Danmap_2006.pdf.
- FARM, “FARM 2003-2004 French antimicrobial resistance monitoring in bacteria of animal origin,” French Food Safety Agency, French, 2006, http://www.afssa.fr/Documents/SANT-Ra-FARM.pdf.
- NORM/NORM-VET, “NORM/NORM-VET 2005 Usage of antimicrobial agents and occurrence of antimicrobial resistance in Norway,” National Veterinary Institute, 2006, http://www.vetinst.no/eng/Research/Publications/Norm-Norm-Vet-Report/The-Norm-Norm-Vet-Report-2005.
- SVARM, “SVARM 2006, Swedish Veterinary Antimicrobial Resistance Monitoring,” 2007, http://www.sva.se/upload/pdf/Tj%C3%A4nster%20och%20produkter/Trycksaker/svarm2006.pdf.
- DEFRA (Department for Environment, Food and Rural Affairs), “Report on the trends and sources of zoonoses and zoonotic agents in humans, foodstuffs, animals and feeding stuffs in 2004,” 2005, http://www.defra.gov.uk/animalh/diseases/zoonoses/zoonoses_reports/report2004uk.pdf.
- MARAN, “MARAN 2005 Monitoring of Antimicrobial Resistance and Antibiotic Usage in Animals in the Netherlands in 2005,” The Veterinary Antibiotic Usage and Resistance Surveillance Working Group, 2006, http://www.cvi.wur.nl/NR/rdonlyres/A906A4C0-A458-423E-B932-28F222385988/52533/MARAN2005def.pdf.
- FINRES-Vet, “FINRES-Vet 2005-2006 Finnish Veterinary Antimicrobial Resistance Monitoring and Consumption of Antimicrobial Agents,” Finnish Food Safety Authority Evira, Finland, 2007, http://www.crl-ar.dana9.dk/data/images/moni/FINRES-Vet_2005-2006_web.pdf.
- R. Bywater, H. Deluyker, E. Deroover, et al., “A European survey of antimicrobial susceptibility among zoonotic and commensal bacteria isolated from food-producing animals,” Journal of Antimicrobial Chemotherapy, vol. 54, no. 4, pp. 744–754, 2004. View at Publisher · View at Google Scholar · View at PubMed
- DAFF (Department of Agriculture, Fisheries and Forestry), “Pilot Surveillance Program for Antimicrobial Resistance in Bacteria of Animal Origin,” Australian Government Department of Agriculture, Fisheries and Forestry, Canberra, 2007, http://www.daff.gov.au/__data/assets/pdf_file/0004/950431/AMR-pilot-survey-report.pdf.
- S.-K. Lim, H.-S. Lee, H.-M. Nam, et al., “Antimicrobial resistance observed in Escherichia coli strains isolated from fecal samples of cattle and pigs in Korea during 2003-2004,” International Journal of Food Microbiology, vol. 116, no. 2, pp. 283–286, 2007. View at Publisher · View at Google Scholar · View at PubMed
- Clinical and Laboratory Standards Institute, Performance standards for antimicrobial susceptibility testing: Seventeeth informational suspplement. M100-S17, vol. 27, Clinical and Laboratory Standards Institute, Wayne, Pa, USA, 2007.
- Working Party of the British Society for Antimicrobial Chemotherapy, “A guide to sensitivity testing,” Journal of Antimicrobial Chemotherapy, vol. 38, pp. 1103–1105, 1996.
- NORM/NORM-VET, “NORM/NORM-VET 2004 Usage of antimicrobial agents and occurrence of antimicrobial resistance in Norway,” National Veterinary Institute, 2005, http://www.vetinst.no/eng/Research/Publications/Norm-Norm-Vet-Report/The-Norm-Norm-Vet-Report-2004.
- VAV, “VAV 2005 Veterinary monitoring of antimicrobial resistance in Spain,” Centro de Vigilancia Sanitaria Veterinaria, Spain, 2006, http://www.vigilanciasanitaria.es/data/VAV2005.pdf.
- H. Y. Kang, Y. S. Jeong, J. Y. Oh, et al., “Characterization of antimicrobial resistance and class 1 integrons found in Escherichia coli isolates from humans and animals in Korea,” Journal of Antimicrobial Chemotherapy, vol. 55, no. 5, pp. 639–644, 2005. View at Publisher · View at Google Scholar · View at PubMed
- B. S. Martin, L. Campos, V. Bravo, M. Adasne, and C. Borie, “Evaluation of antimicrobial resistance using indicator bacteria isolated from pigs and poultry in Chile,” The International Journal of Applied Research in Veterinary Medicine, vol. 3, pp. 171–178, 2005.
- NORM/NORM-VET, “NORM/NORM-VET 2006 Usage of antimicrobial agents and occurrence of antimicrobial resistance in Norway,” 2007, http://www.vetinst.no/eng/Research/Publications/Norm-Norm-Vet-Report/The-Norm-Norm-Vet-Report-2006.
- F. M. Aarestrup, “Monitoring of antimicrobial resistance among food animals: principles and limitations,” Journal of Veterinary Medicine Series B, vol. 51, no. 8-9, pp. 380–388, 2004. View at Publisher · View at Google Scholar · View at PubMed
- B. Catry, H. Laevens, L. A. Devriese, G. Opsomer, and A. De Kruif, “Antimicrobial resistance in livestock,” Journal of Veterinary Pharmacology and Therapeutics, vol. 26, no. 2, pp. 81–93, 2003. View at Publisher · View at Google Scholar
- K. Harada, T. Asai, M. Ozawa, A. Kojima, and T. Takahashi, “Farm-level impact of therapeutic antimicrobial use on antimicrobial- resistant populations of Escherichia coli isolates from pigs,” Microbial Drug Resistance, vol. 14, no. 3, pp. 239–244, 2008. View at Publisher · View at Google Scholar · View at PubMed
- K. Harada, T. Asai, A. Kojima, T. Sameshima, and T. Takahashi, “Contribution of multi-antimicrobial resistance to the population of antimicrobial resistant Escherichia coli isolated from apparently healthy pigs in Japan,” Microbiology and Immunology, vol. 51, no. 5, pp. 493–499, 2007.
- A. Kojima, T. Asai, K. Ishihara, et al., “National monitoring for antimicrobial resistance among indicator bacteria isolated from food-producing animals in Japan,” Journal of Veterinary Medical Science, vol. 71, no. 10, pp. 1301–1308, 2009. View at Publisher · View at Google Scholar
- M. Sunde and M. Norström, “The prevalence of, associations between and conjugal transfer of antibiotic resistance genes in Escherichia coli isolated from Norwegian meat and meat products,” Journal of Antimicrobial Chemotherapy, vol. 58, no. 4, pp. 741–747, 2006. View at Publisher · View at Google Scholar · View at PubMed
- T. Asai, K. Harada, K. Ishihara, et al., “Association of antimicrobial resistance in Campylobacter isolated from food-producing animals with antimicrobial use on farms,” Japanese Journal of Infectious Diseases, vol. 60, no. 5, pp. 290–294, 2007.
- K. M. Bischoff, D. G. White, P. F. McDermott, et al., “Characterization of chloramphenicol resistance in -hemolytic Escherichia coli associated with diarrhea in neonatal swine,” Journal of Clinical Microbiology, vol. 40, no. 2, pp. 389–394, 2002. View at Publisher · View at Google Scholar
- A. Kojima, Y. Ishii, K. Ishihara, et al., “Extended-spectrum--lactamase-producing Escherichia coli strains isolated from farm animals from 1999 to 2002: report from the Japanese veterinary antimicrobial resistance monitoring program,” Antimicrobial Agents and Chemotherapy, vol. 49, no. 8, pp. 3533–3537, 2005. View at Publisher · View at Google Scholar · View at PubMed
- K. Ohmae, S. Yonezawa, and N. Terakado, “R plasmid with carbadox resistance from Escherichia coli of porcine origin,” Antimicrobial Agents and Chemotherapy, vol. 19, no. 1, pp. 86–90, 1981.
- F. Bager, F. M. Aarestrup, M. Madsen, and H. C. Wegener, “Glycopeptide resistance in Enterococcus faecium from broilers and pigs following discontinued use of avoparcin,” Microbial Drug Resistance, vol. 5, no. 1, pp. 53–56, 1999.
- F. M. Aarestrup, “Characterization of glycopeptide-resistant Enterococcus faecium (GRE) from broilers and pigs in Denmark: genetic evidence that persistence of GRE in pig herds is associated with coselection by resistance to macrolides,” Journal of Clinical Microbiology, vol. 38, pp. 2774–2777, 2000.
- K. Harada, T. Asai, A. Kojima, C. Oda, K. Ishihara, and T. Takahashi, “Antimicrobial susceptibility of pathogenic Escherichia coli isolated from sick cattle and pigs in Japan,” Journal of Veterinary Medical Science, vol. 67, no. 10, pp. 999–1003, 2005. View at Publisher · View at Google Scholar
- M. Ozawa, K. Harada, A. Kojima, T. Asai, and T. Sameshima, “Antimicrobial susceptibilities, serogroups, and molecular characterization of avian pathogenic Escherichia coli isolates in Japan,” Avian Diseases, vol. 52, no. 3, pp. 392–397, 2008. View at Publisher · View at Google Scholar
- E. A. González Garcia, “Animal health and foodborne pathogens: enterohaemorrhagic O157:H7 strains and other pathogenic Escherichia coli virotypes (EPEC, ETEC, EIEC, EHEC),” Polish Journal of Veterinary Sciences, vol. 5, pp. 103–115, 2002.
- C. L. Gyles, “Shiga toxin-producing Escherichia coli: an overview,” Journal of Animal Science, vol. 85, pp. E45–E62, 2007.
- P. Boerlin, R. Travis, C. L. Gyles, et al., “Antimicrobial resistance and virulence genes of Escherichia coli isolates from swine in Ontario,” Applied and Environmental Microbiology, vol. 71, no. 11, pp. 6753–6761, 2005. View at Publisher · View at Google Scholar · View at PubMed
- A. J. Mazaitis, R. Maas, and W. K. Maas, “Structure of a naturally occurring plasmid with genes for enterotoxin production and drug resistance,” Journal of Bacteriology, vol. 145, no. 1, pp. 97–105, 1981.
- A. Franklin and R. Mollby, “Concurrent transfer and recombination between plasmids encoding for heat-stable enterotoxin and drug resistance in porcine enterotoxigenic. Escherichia coli,” Medical Microbiology and Immunology, vol. 172, no. 3, pp. 137–147, 1983.
- N. M. Harnett and C. L. Gyles, “Linkage of genes for heat-stable enterotoxins, drug resistance, K99 antigen, and colicin in bovine and porcine strains of enterotoxigenic Escherichia coli,” American Journal of Veterinary Research, vol. 46, pp. 428–433, 1985.
- R. M. Travis, C. L. Gyles, R. Reid-Smith, et al., “Chloramphenicol and kanamycin resistance among porcine Escherichia coli in Ontario,” Journal of Antimicrobial Chemotherapy, vol. 58, no. 1, pp. 173–177, 2006. View at Publisher · View at Google Scholar · View at PubMed
- T. J. Johnson, C. W. Giddings, S. M. Horne, et al., “Location of increased serum survival gene and selected virulence traits on a conjugative R plasmid in an avian Escherichia coli isolate,” Avian Diseases, vol. 46, no. 2, pp. 342–352, 2002.
- M. Kijima-Tanaka, K. Ishihara, A. Kojima, et al., “A national surveillance of Shiga toxin-producing Escherichia coli in food-producing animals in Japan,” Journal of Veterinary Medicine Series B, vol. 52, no. 5, pp. 230–237, 2005. View at Publisher · View at Google Scholar · View at PubMed
- H. Maidhof, B. Guerra, S. Abbas, H. M. Elsheikha, T. S. Whittam, and L. Beutin, “A multiresistant clone of Shiga toxin-producing Escherichia coli O118:[H16] is spread in cattle and humans over different European countries,” Applied and Environmental Microbiology, vol. 68, no. 12, pp. 5834–5842, 2002. View at Publisher · View at Google Scholar
- P. A. Gulig, “Mini-review: virulence plasmids of Salmonella typhimurium and other salmonellae,” Microbial Pathogenesis, vol. 8, no. 1, pp. 3–11, 1990. View at Publisher · View at Google Scholar
- H. Yoshimura, Y. S. Endoh, M. Ishimaru, and M. Takagi, “Antimicrobial resistance patterns of Salmonella typhimurium and Salmonella dublin isolated from cattle in Japan,” Veterinary Record, vol. 147, no. 2, pp. 48–50, 2000.
- H. Esaki, A. Morioka, A. Kojima, et al., “Epidemiological characterization of Salmonella typhimurium DT104 prevalent among food-producing animals in the Japanese veterinary antimicrobial resistance monitoring program (1999–2001),” Microbiology and Immunology, vol. 48, no. 7, pp. 553–556, 2004.
- K. Kawagoe, H. Mine, T. Asai, et al., “Changes of multi-drug resistance pattern in Salmonella enterica subspecies enterica serovar typhimurium isolates from food-producing animals in Japan,” Journal of Veterinary Medical Science, vol. 69, no. 11, pp. 1211–1213, 2007. View at Publisher · View at Google Scholar
- T. Asai, T. Namimatsu, T. Osumi, et al., “Molecular typing and antimicrobial resistance of Salmonella enterica subspecies enterica serovar Choleraesuis isolates from diseased pigs in Japan,” Comparative Immunology, Microbiology and Infectious Diseases, vol. 33, no. 2, pp. 109–119, 2010. View at Publisher · View at Google Scholar · View at PubMed
- T. Asai, K. Murakami, M. Ozawa, R. Koike, and H. Ishikawa, “Relationships between multidrug-resistant Salmonella enterica serovar Schwarzengrund and both broiler chickens and retail chicken meats in Japan,” Japanese Journal of Infectious Diseases, vol. 62, no. 3, pp. 198–200, 2009.
- T. Asai, M. Itagaki, Y. Shiroki, et al., “Antimicrobial resistance types and genes in Salmonella enterica Infantis isolates from retail raw chicken meat and broiler chickens on farms,” Journal of Food Protection, vol. 69, no. 1, pp. 214–216, 2006.
- T. Asai, K. Ishihara, K. Harada, et al., “Long-term prevalence of antimicrobial-resistant Salmonella enterica subspecies enterica serovar infantis in the broiler chicken industry in Japan,” Microbiology and Immunology, vol. 51, no. 1, pp. 111–115, 2007.
- K. Harada, M. Ozawa, K. Ishihara, R. Koike, T. Asai, and H. Ishikawa, “Prevalence of antimicrobial resistance among serotypes of Campylobacter jejuni isolates from cattle and poultry in Japan,” Microbiology and Immunology, vol. 53, no. 2, pp. 107–111, 2009. View at Publisher · View at Google Scholar · View at PubMed
- K. Ishihara, S. Yano, M. Nishimura, et al., “The dynamics of antimicrobial-resistant Campylobacter jejuni on Japanese broiler farms,” Journal of Veterinary Medical Science, vol. 68, no. 5, pp. 515–518, 2006. View at Publisher · View at Google Scholar
- B. E. Langlois, K. A. Dawson, I. Leak, and D. K. Aaron, “Effect of age and housing location on antibiotic resistance of fecal coliforms from pigs in a non-antibiotic-exposed herd,” Applied and Environmental Microbiology, vol. 54, no. 6, pp. 1341–1344, 1988.
- K. Sato, P. C. Bartlett, and M. A. Saeed, “Antimicrobial susceptibility of Escherichia coli isolates from dairy farms using organic versus conventional production methods,” Journal of the American Veterinary Medical Association, vol. 226, no. 4, pp. 589–594, 2005. View at Publisher · View at Google Scholar
- K. A. Ray, L. D. Warnick, R. M. Mitchell, et al., “Antimicrobial susceptibility of Salmonella from organic and conventional dairy farms,” Journal of Dairy Science, vol. 89, no. 6, pp. 2038–2050, 2006.
- C. E. Siemon, P. B. Bahnson, and W. A. Gebreyes, “Comparative investigation of prevalence and antimicrobial resistance of Salmonella between pasture and conventionally reared poultry,” Avian Diseases, vol. 51, no. 1, pp. 112–117, 2007. View at Publisher · View at Google Scholar
- A. G. Mathew, A. M. Saxton, W. G. Upchurch, and S. E. Chattin, “Multiple antibiotic resistance patterns of Escherichia coli isolates from swine farms,” Applied and Environmental Microbiology, vol. 65, no. 6, pp. 2770–2772, 1999.
- Y. Kumai, Y. Suzuki, Y. Tanaka, et al., “Characterization of multidrug-resistance phenotypes and genotypes of Escherichia coli strains isolated from swine from an abattoir in Osaka, Japan,” Epidemiology and Infection, vol. 133, no. 1, pp. 59–70, 2005. View at Publisher · View at Google Scholar
- N. F. Florea and C. H. Nightingale, “Review of the pharmacodynamics of antibiotic use in animal food production,” Diagnostic Microbiology and Infectious Disease, vol. 49, no. 2, pp. 105–108, 2004. View at Publisher · View at Google Scholar · View at PubMed
- M. H. Moro, G. W. Beran, L. J. Hoffman, and R. W. Griffith, “Effects of cold stress on the antimicrobial drug resistance of Escherichia coli of the intestinal flora of swine,” Letters in Applied Microbiology, vol. 27, pp. 251–254, 1988.
- M. H. Moro, G. W. Beran, R. W. Griffith, and L. J. Hoffman, “Effects of heat stress on the antimicrobial drug resistance of Escherichia coli of the intestinal flora of swine,” Journal of Applied Microbiology, vol. 88, no. 5, pp. 836–844, 2000.
- H. Sørum and M. Sunde, “Resistance to antibiotics in the normal flora of animals,” Veterinary Research, vol. 32, pp. 227–241, 2001.
- B. R. Levin, V. Perrot, and N. Walker, “Compensatory mutations, antibiotic resistance and the population genetics of adaptive evolution in bacteria,” Genetics, vol. 154, no. 3, pp. 985–997, 2000.
- V. I. Enne, A. A. Delsol, G. R. Davis, S. L. Hayward, J. M. Roe, and P. M. Bennett, “Assessment of the fitness impacts on Escherichia coli of acquisition of antibiotic resistance genes encoded by different types of genetic element,” Journal of Antimicrobial Chemotherapy, vol. 56, no. 3, pp. 544–551, 2005. View at Publisher · View at Google Scholar · View at PubMed
- A. R. Khachatryan, D. D. Hancock, T. E. Besser, and D. R. Call, “Antimicrobial drug resistance genes do not convey a secondary fitness advantage to calf-adapted Escherichia coli,” Applied and Environmental Microbiology, vol. 72, no. 1, pp. 443–448, 2006. View at Publisher · View at Google Scholar · View at PubMed