Journal of Microbiology

, Volume 50, Issue 3, pp 540–543 | Cite as

Copper resistance and its relationship to erythromycin resistance in Enterococcus isolates from bovine milk samples in Korea

  • JiHoon Kim
  • SangJin Lee
  • SungSook ChoiEmail author


Antibiotic resistance in animal isolates of enterococci is a public health concern, because of the risk of transmission of antibiotic-resistant strains or resistance genes to humans through the food chain. This study investigated copper resistance and its relationship with erythromycin resistance in 245 enterococcal isolates from bovine milk. Phenotypic and genotypic resistance to erythromycin and copper sulfate were investigated. Of the 245 enterococcal isolates, 79.2% (n=194) displayed erythromycin resistance (≥8 μg/ml). Of the erythromycin-resistant isolates, 97.4% (n=189) possessed erm(B), 73.7% (n=143) possessed mef(A), and 71.6% (n=139) possessed both genes. Of the 245 enterococcal isolates, only 4.5% (n=11) displayed copper resistance (≥28 mM) and the copper resistance gene, tcr(B), was detected in seven isolates that all possessed erm(B). This study is the first to report the tcr(B) gene in enterococci isolated from Korean bovine milk and its relationship to erythromycin resistance.


antibiotic resistance enterococci bovine milk erythromycin copper 


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  1. Aarestrup, F.M. and Hasman, H. 2004. Susceptibility of different bacterial species isolated from food animals to copper sulphate, zinc chloride and antimicrobial substance used for disinfection. Vet. Microbiol. 100, 83–89.PubMedCrossRefGoogle Scholar
  2. Amachawadi, R.G., Shelton, N.W., Jacob, M.E., Shi, X.S., Narayanan, K., Zurek, L., Dritz, S.S., Nelssen, J.L., Tokach, M.D., and Nagaraja, T.G. 2010. Occurrence of tcrB, a transferable copper resistance gene, in fecal enterococci of swine. Foodborne Pathog. Dis. 7, 1089–1097.PubMedCrossRefGoogle Scholar
  3. Barbosa, J., Ferreira, P., and Teixeira, P. 2009. Antibiotic susceptibility of enterococci isolated from traditional fermented meat products. Food Microbiol. 26, 527–532.PubMedCrossRefGoogle Scholar
  4. CLSI. 2009. Performance standards for antimicrobial susceptibility testing: nineteenth informational supplement. Clinical and Laboratory Standards Institute, Wayne, Pennsylvania, USA.Google Scholar
  5. Devriese, L.A., Pot, B., Damme, L.V., Kersters, K., and Hasebrouck, F. 1995. Identification of Enterococcus species isolated from foods of animal origin. Int. J. Food Microbiol. 26, 187–197.PubMedCrossRefGoogle Scholar
  6. Fard, R.M., Heuzenroeder, M.W., and Barton, M.D. 2011. Antimicrobial and heavy metal resistance in commensal enterococci isolated from pigs. Vet. Microbiol. 148, 276–282.PubMedCrossRefGoogle Scholar
  7. Hasman, H. and Aarestrup, F.M. 2002. tcrB, a gene conferring transferable copper resistance in Enterococcus faecium: occurrence, transferability, and linkage to macrolide and glycopeptides resistance. Antimicrob. Agents Chemother. 46, 1410–1416.PubMedCrossRefGoogle Scholar
  8. Hasman, H., Kempf, I., Chidaine, B., Cariolet, R., Ersbøll, A.K., Houe, H., Bruun Hansen, H.C., and Aarestrup, F.M. 2006. Copper resistance in Enterococcus faecium, mediated by the tcrB gene, is selected by supplementation of pig feed with copper sulfate. Appl. Environ. Microbiol. 72, 5784–5789.PubMedCrossRefGoogle Scholar
  9. Hershberger, E., Oprea, S.F., Donabedian, S.M., Perri, M., Bozigar, P., Bartlett, P., and Zervos, M.J. 2005. Epidemiology of antimicrobial resistance in enterococci of animal origin. J. Antimicrob. Chemother. 55, 127–130.PubMedCrossRefGoogle Scholar
  10. Jeong, S.H., Lim, S.K., Lee, H.S., Jeong, B.Y., Lee, J.Y., Yang, C.B., and Shin, H.C. 2008. The present situation of antibiotics used in animal and resistant bacteria. Infect. Chemother. 40,Suppl. 2144–2149.Google Scholar
  11. Jung, J.H., Yoon, E.J., Choi, E.C., and Choi, S.S. 2009. Development of Taqman probe based real-time PCR method for erm(A), erm(B), and erm(C), rapid detection of macrolide-lincosamide-streptogramin B resistance genes, from clinical isolates. J. Microbiol. Biotechnol. 19, 1464–1469.PubMedCrossRefGoogle Scholar
  12. Kelly, L., Smith, D.L., Snary, E.L., Johnson, J.A., Harris, A.D., Wooldridge, M., and Morris, J.G.Jr. 2004. Animal growth promoters: to ban or not to ban?: A risk assessment approach. Int. J. Antimicrob. Agents 24, 205–212.PubMedCrossRefGoogle Scholar
  13. Kim, J.M., Cho, S.B., Kim, S.K., Lee, S.S., and Lee, S.K. 2010. Contamination analysis of heavy metals in commercial feed for the production of safe-animal products. J. Life Science 20, 717–722.CrossRefGoogle Scholar
  14. Kühn, I., Iversen, A., Burman, L.G., Olsson-Liljequist, B., Franklin, A., Finn, M., Aarestrup, F.M., Seyfarth, A.M., Blanch, A.R., Taylor, H., and et al. 2000. Epidemiology and ecology of enterococci, with special reference to antibiotic resistant strains, in animals, humans and the environment. Example of an ongoing project within the European research programme. Int. J. Antimicrob. Agents 14, 337–342.PubMedCrossRefGoogle Scholar
  15. Kwon, Y.I., Kim, T.W., Kim, H.Y., Chang, Y.H., Kwak, H.S., Woo, G.J., and Chung, Y.H. 2007. Monitoring of antimicrobial resistant bacteria from animal farm environments in Korea. Kor. J. Microbiol. Biotechnol. 35, 17–25.Google Scholar
  16. Leclercq, R. 1997. Enterococci acquire new kinds of resistance. Clin. Infect. Dis. 24,Suppl. 1, S80–S84.PubMedCrossRefGoogle Scholar
  17. Lee, H.I., Jung, J.H., Lee, S.J., and Choi, S.S. 2010. Analysis of genotype and phenotype of erythromycin resistance in Enterococci spp. isolated from raw milk samples. Kor. J. Microbiol. 46, 148–151.Google Scholar
  18. Lester, C.H., Frimodt-Møller, N., Sørensen, T.L., Monnet, D.L., and Hammerum, A.M. 2006. In vivo transfer of the vanA resistance gene from an Enterococcus faecium isolate of animal origin to an E. faecium isolate of human origin the intestines of human volunteers. Antimicrob. Agents Chemother. 50, 596–599.PubMedCrossRefGoogle Scholar
  19. Moellering, R.C. and Krogstad, D.J. 1979. Antibiotic resistance in Enterococci, pp. 293–298. In Schlessinger, D. (ed.), American Society for Microbiology, Washington, D.C., USA.Google Scholar
  20. Murray, B.E. 1990. The life and times of the Enterococcus. Clin. Microbiol. Rev. 3, 46–65.PubMedGoogle Scholar
  21. Nam, H.M., Lim, S.K., Moon, J.S., Kang, H.M., Kim, J.M., Jang, K.C., Kim, J.M., Kang, M.I., Joo, Y.S., and Jung, S.C. 2010. Antimicrobial resistance of enterococci isolated from mastitic bovine milk samples in Korea. Zoonoses Public Health. 57, e59–64.PubMedCrossRefGoogle Scholar
  22. Phillips, I. 2007. Withdrawal of growth-promoting antibiotics in Europe and its effects in relation to human health. Int. J. Antimicrob. Agents 30, 101–107.PubMedCrossRefGoogle Scholar
  23. Sørensen, T.L., Blom, M., Monnet, D.L., Frimodt-Møller, N., Poulsen, R.L., and Espersen, F. 2001. Transient intestinal carriage after ingestion of antibiotic-resistant Enterococcus faecium from chicken and pork. N. Engl. J. Med. 345, 1161–1166.PubMedCrossRefGoogle Scholar
  24. WHO. 1997. The Medical impact of the use of antimicrobials in food animals. World Helath Organization, Berlin, Germany.Google Scholar
  25. WHO. 2000. WHO Global principles for the containment of antimicrobial resistance in animals intended for food. World Health organization, Geneva, Switzerland.Google Scholar
  26. Witte, W., Klare, I., and Werner, G. 1999. Selective pressure by antibiotics as feed additives. Infection 29, S35–38.CrossRefGoogle Scholar

Copyright information

© The Microbiological Society of Korea and Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Division of Animal ScienceSahmyook UniversitySeoulRepublic of Korea
  2. 2.College of PharmacySahmyook UniversitySeoulRepublic of Korea

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