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Antimicrobial resistance, virulence genes and PFGE-profiling of Escherichia coli isolates from South Korean cattle farms

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Abstract

To estimate the prevalence of Escherichia coli with potential pathogenicity in cattle farm in South Korea, a total of 290 E. coli isolates were isolated from cattle farms over a period of 2 years in South Korea. These were examined for phenotypic and genotypic characteristics including antimicrobial susceptibility, serotype, and gene profiles of virulence and antimicrobial resistance. The most dominant virulence gene was f17 (26.2%), followed by stx2 (15.9%), ehxA (11.0%), stx1 (8.3%), eae (5.2%), and sta (4.1%). Some shiga-toxin producing E. coli isolates possessed eae (15.9%). All isolates except for one showed resistance to one or more antimicrobials, with 152 isolates exhibiting multidrug-resistance. The most prevalent resistance phenotype detected was streptomycin (63.1%), followed by tetracycline (54.5%), neomycin (40.3%), cephalothin (32.8%), amoxicillin (30.0%), ampicillin (29.7%), and sulphamethoxazole/trimethoprim (16.6%). The associated resistance determinants detected were strA-strB (39.0%), tet(E) (80.0%), tet(A) (27.6%), aac(3)-IV (33.1%), aphA1 (21.4%), bla TEM (23.8%), and sul2 (22.1%). When investigated by O serotyping and PFGE molecular subtyping, the high degree of diversity was exhibited in E. coli isolates. These results suggest that E. coli isolates from South Korean cattle farms are significantly diverse in terms of virulence and antimicrobial resistance. In conclusion, the gastroinstestinal flora of cattle could be a significant reservoir of diverse virulence and antimicrobial resistance determinants, which is potentially hazardous to public health.

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References

  • Acres, S.D. 1985. Enterotoxigenic Escherichia coli infection in newborn calves:A review. J. Dairy Sci. 68, 229–256.

    Article  PubMed  CAS  Google Scholar 

  • Aidar-Ugrinovich, L., Blanco, J., Blanco, M., Blanco, J.E., Leomil, L., Dahbi, G., Mora, A., Onuma, D.L., Silveira, W.D., and Pestana de Castro, A.F. 2007. Serotypes, virulence genes, and intimin types of Shiga toxin-producing Escherichia coli (STEC) and enteropathogenic E. coli (EPEC) isolated from calves in São Paulo, Brazil. Int. J. Food Microbiol. 115, 297–306.

    Article  CAS  Google Scholar 

  • Belaaouaj, A., Lapoumeroulie, C., Caniça, M.M., Vedel, G., Névot, P., Krishnamoorthy, R., and Paul, G. 1994. Nucleotide sequences of the genes coding for the TEM-like beta-lactamases IRT-1 and IRT-2 (formerly called TRI-1 and TRI-2). FEMS Microbiol. Lett. 120, 75–80.

    PubMed  CAS  Google Scholar 

  • Bergamini, A.M.M., Simões, M., Irino, K., Gomes, T.A.T., and Guth, B.E.C. 2007. Prevalence and characteristics of Shiga toxin-producing Escherichia coli (STEC) strains in ground beef in São Paulo, Brazil. Braz. J. Microbiol. 38, 553–556.

    Article  Google Scholar 

  • Berge, A.C.D., Moore, D.A., Besser, T.E., and Sischo, W.M. 2009. Targeting therapy to minimize antimicrobial use in preweaned calves: Effects on health, growth, and treatment costs. J. Diary Sci. 92, 4707–4714.

    Article  CAS  Google Scholar 

  • Bergström, S. and Normark, S. 1979. Beta-lactam resistance in clinical isolates of Escherichia coli caused by elevated production of the ampC-mediated chromosomal beta-lactamase. Antimicrob. Agents Chemother. 16, 427–433.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bettelheim, K.A., Kuzevski, A., Gilbert, R.A., Krause, D.O., and McSweeney, C.S. 2005. The diversity of Escherichia coli serotypes and biotypes in cattle faeces. J. Appl. Microbiol. 98, 699–709.

    Article  PubMed  CAS  Google Scholar 

  • Beutin, L., Montenegro, M.A., ørskov, I., ørskov, F., Prada, J., Zimmermann, S., and Stephan, R. 1989. Close association of verotoxin (Shiga-like toxin) production with enterohemolysin production in strains of Escherichia coli. J. Clin. Microbiol. 27, 2559–2564.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Blanco, M., Blanco, J., Blanco, J.E., and Ramos, J. 1993. Enterotoxigenic, verotoxigenic, and necrotoxigenic Escherichia coli isolated from cattle in Spain. Am. J. Vet. Res. 54, 1446–1451.

    PubMed  CAS  Google Scholar 

  • Blanco, M., Blanco, J.E., Blanco, J., Mora, A., Prado, C., Alonso, M.P., Mouriño, M., Madrid, C., Balsalobre, C., and Juárez, A. 1997. Distribution and characterisation of faecal verotoxin-producing Escherichia coli (VTEC) isolated from healthy cattle. Vet. Microbiol. 54, 309–319.

    Article  PubMed  CAS  Google Scholar 

  • Boerlin, P., Travis, R., Gyles, C.L., Reid-Smith, R., Janecko, N., Lim, H., Nicholson, V., McEwen, S.A., Friendship, R., and Archambault, M. 2005. Antimicrobial resistance and virulence genes of Escherichia coli isolates from swine in Ontario. Appl. Environ. Microbiol. 71, 6753–6761.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bonnet, R., Souweine, B., Gauthier, G., Rich, C., Livrelli, V., Sirot, J., Joly, B., and Forestier, C. 1998. Non-O157:H7 Stx2-producing Escherichia coli strains associated with sporadic cases of hemolytic- uremic syndrome in adults. J. Clin. Microbiol. 36, 1777–1780.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Centers for Disease Control and Prevention (CDC). 2001. Escherichia coli general information http://www.cdc.gov/ecoli/general/index.html.

    Google Scholar 

  • Chiou, C.S. and Jones, A.L. 1995. Expression and identification of the strA-strB gene pair from streptomycin-resistant Erwinia amylovora. Gene 152, 47–51.

    Article  PubMed  CAS  Google Scholar 

  • Davies, J. and Davies, D. 2010. Origin and evolution of antibiotic resistance. Microbiol. Mol. Biol. Rev. 74, 417–433.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Enne, V.I., Livermore, D.M., Stephens, P., and Hall, L.M. 2001. Persistence of sulphonamide resistance in Escherichia coli in the UK despite national prescribing restriction. Lancet 357, 1325–1328.

    Article  PubMed  CAS  Google Scholar 

  • Féria, C., Ferreira, E., Correia, J.D., Gonçalves, J., and Caniça, M. 2002. Patterns and mechanisms of resistance to β-lactams and β-lactamase inhibitors in uropathogenic Escherichia coli isolated from dogs in Portugal. J. Antimicrob. Chemother. 49, 77–85.

    Article  PubMed  Google Scholar 

  • Franck, S.M., Bosworth, B.T., and Moon, H.W. 1998. Multiplex PCR for enterotoxigenic, attaching and effacing, and Shiga toxin-producing Escherichia coli strains from calves. J. Clin. Microbiol. 36, 1795–1797.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Franklin, A., Acar, J., Anthony, F., Gupta, R., Nicholls, T., Tamura, Y., Thompson, S., Threlfall, E.J., Vose, D., van Vuuren, M., and et al. 2001. Antimicrobial resistance: harmonisation of national antimicrobial resistance monitoring and surveillance programmes in animals and in animal-derived food. Rev. Sci. Tech. 20, 859–870.

    PubMed  CAS  Google Scholar 

  • Ghanbarpour, R. and Oswald, E. 2009. Characteristics and virulence genes of Escherichia coli isolated from septicemic calves in southeast of Iran. Trop. Anim. Health Prod. 41, 1091–1099.

    Article  PubMed  Google Scholar 

  • Hussein, H.S. 2007. Prevalence and pathogenicity of Shiga toxinproducing Escherichia coli in beef cattle and their products. J. Anim. Sci. 85, 63–72.

    Article  Google Scholar 

  • Jerse, A.E., Yu, J., Tall, B.D., and Kaper, J.B. 1990. A genetic locus of enteropathogenic Escherichia coli necessary for the production of attaching and effacing lesions on tissue culture cells. Proc. Natl. Acad. Sci. USA 87, 7839–7843.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kang, H.Y., Jeong, Y.S., Oh, J.Y., Tae, S.H., Choi, C.H., Moon, D.C., Lee, W.K., Lee, Y.C., Seol, S.Y., Cho, D.T., and et al. 2005. Characterization of antimicrobial resistance and class 1 integrons found in Escherichia coli isolates from humans and animals in Korea. J. Antimicrob. Chemother. 55, 639–644.

    Article  PubMed  CAS  Google Scholar 

  • Karczmarczyk, M., Abbott, Y., Walsh, C., Leonard, N., and Fanning, S. 2011a. Characteriazation of multidrug-resistant Escherichia coli isolates from animals preseting at a university veterinary hospital. Appl. Environ. Microbiol. 77, 7104–7112.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Karczmarczyk, M., Walsh, C., Slowey, R., Leonard, N., and Fanning, S. 2011b. Molecular characterization of multidrug-resistant Escherichia coli isolates from Irish cattle farms. Appl. Environ. Microbiol. 77, 7121–7127.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kerrn, M.B., Klemmensen, T., Frimodt-Møller, N., and Espersen, F. 2002. Susceptibility of Danish Escherichia coli strains isolated from urinary tract infections and bacteraemia, and distribution of sul genes conferring sulphonamide resistance. J. Antimicrob. Chemother. 50, 513–516.

    Article  PubMed  CAS  Google Scholar 

  • Keyes, K., Hudson, C., Maurer, J.J., Thayer, S., White, D.G., and Lee, M.D. 2000. Detection of florfenicol resistance genes in Escherichia coli isolated from sick chickens. Antimicrob. Agents Chemother. 44, 421–424.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kobayashi, H., Shimada, J., Nakazawa, M., Morozumi, T., Pohjanvirta, T., Pelkonen, S., and Yamamoto, K. 2001. Prevalence and characteristics of Shiga toxin-producing Escherichia coli from healthy cattle in Japan. Appl. Environ. Microbiol. 67, 484–489.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kozak, G.K., Pearl, D.L., Parkman, J., Reid-Smith, R.J., Deckert, A., and Boerlin, P. 2009. Distribution of sulfonamide resistance genes in Escherichia coli and Salmonella isolates from swine and chickens at abattoirs in Ontario and Québec, Canada. Appl. Environ. Microbiol. 75, 5999–6001.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Lanz, R., Kuhnert, P., and Boerlin, P. 2003. Antimicrobial resistance and resistance gene determinants in clinical Escherichia coli from different animal species in Switzerland. Vet. Microbiol. 91, 73–84.

    Article  PubMed  CAS  Google Scholar 

  • Lim, S.K., Lee, H.S., Nam, H.M., Cho, Y.S., Kim, J.M., Song, S.W., Park, Y.H., and Jung, S.C. 2007. Antimicrobial resistance observed in Escherichia coli strains isolated from fecal samples of cattle and pigs in Korea during 2003–2004. Int. J. Food Microbiol. 116, 283–286.

    Article  PubMed  CAS  Google Scholar 

  • López-Saucedo, C., Cerna, J.F., Villegas-Sepulveda, N., Thompson, R., Velazquez, F.R., Torres, J., Tarr, P.I., and Estrada-García, T. 2003. Single multiplex polymerase chain reaction to detect diverse loci associated with diarrheagenic Escherichia coli. Emerg. Infect. Dis. 9, 127–131.

    Article  PubMed  PubMed Central  Google Scholar 

  • Madsen, L., Aarestrup, F.M., and Olsen, J.E. 2000. Characterisation of streptomycin resistance determinants in Danish isolates of Salmonella Typhimurium. Vet. Microbiol. 75, 73–82.

    Article  PubMed  CAS  Google Scholar 

  • Mainil, J.G., Jacquemin, E.R., Kaeckenbeeck, A.E., and Pohl, P.H. 1993. Association between the effacing (eae) gene and the Shigalike toxin-encoding genes in Escherichia coli isolates from cattle. Am. J. Vet. Res. 54, 1064–1068.

    PubMed  CAS  Google Scholar 

  • Marshall, B., Morrissey, S., Flynn, P., and Levy, S.B. 1986. A new tetracycline-resistance determinant, class E, isolated from Enterobacteriaceae. Gene 50, 111–117.

    Article  PubMed  CAS  Google Scholar 

  • Maynard, C., Fairbrother, J.M., Bekal, S., Sanschagrin, F., Levesque, R.C., Brousseau, R., Masson, L., Larivière, S., and Harel, J. 2003. Antimicrobial resistance genes in enterotoxigenic Escherichia coli O149:K91 isolates obtained over a 23-year period from pigs. Antimicrob. Agents Chemother. 47, 3214–3221.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Medina, A., Horcajo, P., Jurado, S., De la Fuente, R., Ruiz-Santa-Quiteria, J.A., Domínguez-Bernal, G., and Orden, J.A. 2011. Phenotypic and genotypic characterization of antimicrobial resistance in enterohemorrhagic Escherichia coli and atypical enteropathogenic E. coli strains from ruminants. J. Vet. Diagn. Invest. 23, 91–95.

    Article  PubMed  Google Scholar 

  • Menrath, A., Wieler, L.H., Heidemanns, K., Semmler, T., Fruth, A., and Kemper, N. 2010. Shiga toxin producing Escherichia coli: identification of non-O157:H7-Super-Shedding cows and related risk factors. Gut Pathog. 2, 7.

    Article  PubMed  PubMed Central  Google Scholar 

  • Moon, H.W. and Bunn, T.O. 1993. Vaccines for preventing enterotoxigenic Escherichia coli infections in farm animals. Vaccine 11, 213–220.

    Article  PubMed  CAS  Google Scholar 

  • M’Zali, F.H., Gascoyne-Binzi, D.M., Heritage, J., and Hawkey, P.M. 1996. Detection of mutations conferring extended-spectrum activity on SHV beta-lactamases using polymerase chain reaction single strand conformational polymorphism (PCR-SSCP). J. Antimicrob. Chemother. 37, 797–802.

    Article  PubMed  Google Scholar 

  • Nagy, B. and Fekete, P.Z. 1999. Enterotoxigenic Escherichia coli (ETEC) in farm animals. Vet. Res. 30, 259–284.

    PubMed  CAS  Google Scholar 

  • Nataro, J.P. and Kaper, J.B. 1998. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11, 142–201.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Ng, L.K., Martin, I., Alfa, M., and Mulvey, M. 2001. Multiplex PCR for the detection of tetracycline resistant genes. Mol. Cell Probes 15, 209–215.

    Article  PubMed  CAS  Google Scholar 

  • Nguyen, T.D., Vo, T.T., and Vu-Khac, H. 2011. Virulence factors in Escherichia coli isolated from calves with diarrhea in Vietnam. J. Vet. Sci. 12, 159–164.

    Article  PubMed  PubMed Central  Google Scholar 

  • ørskov, F. and ørskov, I. 1984. Serotyping of Escherichia coli. Methods Microbiol. 14, 43–112.

    Article  Google Scholar 

  • Schmidt, H., Beutin, L., and Karch, H. 1995. Molecular analysis of the plasmid-encoded hemolysin of Escherichia coli O157: H7 strain EDL 933. Infect. Immun. 63, 1055–1061.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Tamang, M.D., Oh, J.Y., Seol, S.Y., Kang, H.Y., Lee, J.C., Lee, Y.C., Cho, D.T., and Kim, J. 2007. Emergence of multidrug-resistant Salmonella enterica serovar Typhi associated with a class 1 integron carrying the dfrA7 gene cassette in Nepal. Int. J. Antimicrob. Agents 30, 330–335.

    Article  PubMed  CAS  Google Scholar 

  • Tracz, D.M., Boyd, D.A., Hizon, R., Bryce, E., Mcgeer, A., Ofner-Agostini, M., Simor, A.E., Paton, S., and Mulvey, M.R. 2007. ampC gene expression in promoter mutants of cefoxitin-resistant Escherichia coli clinical isolates. FEMS Microbiol. Lett. 270, 265–271.

    Article  PubMed  CAS  Google Scholar 

  • Travis, R.M., Gyles, C.L., Reid-Smith, R., Poppe, C., McEwen, S.A., Friendship, R., Janecko, N., and Boerlin, P. 2006. Chloramphenicol and kanamycin resistance among porcine Escherichia coli in Ontario. J. Antimicrob. Chemother. 58, 173–177.

    Article  PubMed  CAS  Google Scholar 

  • Van Bost, S., Bâbe, M.H., Jacquemin, E., and Mainil, J. 2001. Characteristics of necrotoxigenic Escherichia coli isolated from septicemic and diarrheic calves between 1958 and 1970. Vet. Microbiol. 82, 311–320.

    Article  PubMed  Google Scholar 

  • Van, T.T., Chin, J., Chapman, T., Tran, L.T., and Coloe, P.J. 2008. Safety of raw meat and shellfish in Vietnam: an analysis of Escherichia coli isolations for antimicrobial resistance and virulence genes. Int. J. Food Microbiol. 124, 217–223.

    Article  PubMed  CAS  Google Scholar 

  • Vinué, L., Sáenz, Y., Rojo-Bezares, B., Olarte, I., Undabeitia, E., Somalo, S., Zarazaga, M., and Torres, C. 2010. Genetic environment of sul genes and characterisation of integrons in Escherichia coli isolates of blood origin in a Spanish hospital. Int. J. Antimicrob. Agents 35, 492–496.

    Article  PubMed  Google Scholar 

  • Wedley, A.L., Maddox, T.W., Westgarth, C., Coyne, K.P., Pinchbeck, G.L., Williams, N.J., and Dawson, S. 2011. Prevalence of antimicrobial-resistant Escherichia coli in dogs in a cross-sectional, community-based study. Vet. Rec. 168, 3–4.

    Article  Google Scholar 

  • Wieler, L.H., Bauerfeind, R., and Baljer, G. 1992. Characterization of Shiga-like toxin producing Escherichia coli (SLTEC) isolated from calves with and without diarrhoea. Zentralbl Bakteriol. 276, 243–253.

    Article  PubMed  CAS  Google Scholar 

  • Wright, G.D. 2007. The antimicrobial resistome: the nexus of chemical and genetic diversity. Nat. Rev. Microbiol. 5, 175–186.

    Article  PubMed  CAS  Google Scholar 

  • Zschöck, M., Hamann, H.P., Kloppert, B., and Wolter, W. 2000. Shiga-toxin-producing Escherichia coli in faeces of healthy dairy cows, sheep and goats: prevalence and virulence properties. Lett. Appl. Microbiol. 31, 203–208.

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Infectious Diseases, College of Veterinary Medicine, Seoul National University, Seoul, 151-742, Republic of Korea

    Seung Won Shin, Myounghwan Jung, Min-Kyoung Shin & Han Sang Yoo

  2. Animal Disease Diagnostic Division, Animal and Plant Quarantine Agency, Anyang, 430-757, Republic of Korea

    Jae-Won Byun

  3. Institute of Green Bio Science and Technology, Seoul National University, Pyeungchang, 232-916, Republic of Korea

    Han Sang Yoo

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  1. Seung Won Shin
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Correspondence to Han Sang Yoo.

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Shin, S.W., Byun, JW., Jung, M. et al. Antimicrobial resistance, virulence genes and PFGE-profiling of Escherichia coli isolates from South Korean cattle farms. J Microbiol. 52, 785–793 (2014). https://doi.org/10.1007/s12275-014-4166-1

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