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Prevalence and antimicrobial resistance of porcine O157 and non-O157 Shiga toxin-producing Escherichia coli from India

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Abstract

The aims of this study were to determine the prevalence of Shiga toxin-producing Escherichia coli (STEC) strains in pigs as a possible STEC reservoir in India as well as to characterize the STEC strains and to determine the antimicrobial resistance pattern of the strains. A total of 782 E. coli isolates from clinically healthy (n = 473) and diarrhoeic piglets (309) belonging to major pig-producing states of India were screened by the polymerase chain reaction (PCR) assay for the presence of virulence genes characteristic for STEC, that is, Shiga toxin-producing gene(s) (stx1, stx2), intimin (eae), enterohemolysin (hlyA) and STEC autoagglutinating adhesin (Saa). Overall STEC were detected in 113 (14.4 %) piglets, and the prevalence of E. coli O157 and non-O157 STEC were 4 (0.5 %) and 109 (13.9 %), respectively. None of the O157 STEC isolates carried gene encoding for H7 antigen (fliCh7). The various combinations of virulence genes present in the strains studied were stx1 in 4.6 %, stx1 in combination with stx2 gene in 5.1 %, stx1 in combination with stx2 and ehxA in 0.6 %, stx1 in combination with stx2 and eae in 0.2 % and stx2 alone in 3.7 %. All STEC isolates were found negative for STEC autoagglutinating adhesin (Saa). The number of STEC isolates which showed resistance to antimicrobials such as ampicillin, tetracycline, streptomycin, lincomycin, nalidixic acid, sulfadiazine, penicillin, gentamicin, kanamycin and ceftriaxone were 100, 99, 98, 97, 95, 94, 92, 88, 85 and 85, respectively. Ninety-seven isolates showed resistance to more than 2 antimicrobials, and 8 resistance groups (R1 to R8) were observed. This study demonstrates that pigs in India harbour both O157 and non-O157 STEC, and this may pose serious public health problems in future.

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References

  • Ateba, C.N. and Bezuidenhout, C.C., 2008. Characterisation of Escherichia coli O157 strains from humans, cattle and pigs in the North-West Province, South Africa, International Journal of Food Microbiology, 128, 181–188.

    Article  CAS  Google Scholar 

  • Barman, N.N., Deb, R., Ramamurthy, T. R., Sharma, K., Borah, P., Wani, S. A. and Kalita, D., 2008. Molecular characterization of shiga like toxin-producing Escherichia coli (STEC) isolates from pigs oedema, Indian Journal of Medical Research, 127, 602–606

    CAS  PubMed  Google Scholar 

  • Barth, S., Tscholshiew, A., Menge, C., Weiss, R., Baljer, G. and Bauerfeind, R., 2007. Virulence and fitness gene patterns of Shigatoxin-encoding Escherichia coli isolated from pigs with edema disease or diarrhea in Germany, Berl Munch Tierarztl Wochenschr, 120, 307–316.

    CAS  PubMed  Google Scholar 

  • Bouvet, J., Montet, M. P., Rossel, R., Le Roux, A., Bavai, C., Ray-Gueniot, S., Mazuy, C., Atrache, V. and Vernozy-Rozand, C., 2002. Effects of slaughter processes on pig carcass contamination by verotoxin producing Escherichia coli and E. coli O157:H7, International Journal of Food Microbiology, 77, 99–108

    Article  CAS  PubMed  Google Scholar 

  • Chase-Topping, M. E., Rosser, T., Allison, L.J., Courcier, E., Evans, J., McKendrick, I. J. Pearce, M.C., Handel, I., Caprioli, A., Karch, H., Hanson, M.F., Pollock, K.G., Locking, M.E., Woolhouse, M. E., Matthews, L., Low, J. C. and Gally, D. L., 2012. Pathogenic potential to humans of bovine Escherichia coli O26, Scotland, Emerging Infectious Diseases, 18, 439–48.

    Article  CAS  PubMed Central  Google Scholar 

  • Choi, C., Ham, H.J., Kwon, D., Kim, J., Cheon, D.S. and Min, K., 2002. Antimicrobial susceptibility of pathogenic Escherichia coli isolated from pigs in Korea, Journal of Veterinary Medical Science, 64, 71–73.

    Article  CAS  PubMed  Google Scholar 

  • CLSI, 2008. Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals; Approved standard-Third edition Vol 28 (8), CLSI document M31-A3, 1–99. Clinical and Laboratory Standards Institute, 940 West Valley Road, Wayne Pennsylvania, USA.

  • Cowan, S.T. and Steel, J. K., 1993. Manual for identification of medical bacteria, 3rd ed. edited and rev.by Barrow, G.I. and Feltham, R.K.A. London, UK: The Syndics of the Cambridge University Press.

    Google Scholar 

  • De Boer, E. and Heuvelink, A.E., 2000. Methods for the detection and isolation of shiga toxin producing Escherichia coli, Journal of Applied Microbiology, 88, S133-143.

    Article  Google Scholar 

  • Díaz-Sánchez, S., Sánchez, S., Herrera-León, S., Porrero, C., Blanco, J., Dahbi, G., Blanco, J.E., Mora, A., Mateo, R., Hanning, I. and Vidal, D., 2013. Prevalence of Shiga toxin-producing Escherichia coli, Salmonella spp. and Campylobacter spp. in large game animals intended for consumption: relationship with management practices and livestock influence, Veterinary Microbiology, 163, 274–281.

    Article  PubMed  Google Scholar 

  • Döpfer, D., Geue, L., Schares, S., Mintel, B., Hoffmann, B. and Fischer, E.A., 2012. Dynamics of shiga-toxin producing Escherichia coli (STEC) and their virulence factors in cattle. Preventive Veterinary Medicine, 103, 22–30.

    Article  PubMed  Google Scholar 

  • Durand, F. C., Faqir, F., Ameilbonne, A., Rozand, C. and Martin, C. 2010. Fates of Acid-Resistant and Non-Acid-Resistant Shiga Toxin-Producing Escherichia coli Strains in Ruminant Digestive Contents in the Absence and Presence of Probiotics, Applied and Environmental Microbiology, 75, 640–647.

    Article  Google Scholar 

  • Eriksson, E., Aspan, A., Gunnarsson, A., Borch, E. and Nerbrink, E., 2003. Verocytotoxin producing Escherichia coli O157:H7 in the Swedish pig population, Veterinary Record, 152, 712–717.

    Article  CAS  PubMed  Google Scholar 

  • European Food Safety Authority, 2010. The community summary report on trends and sources of zoonoses and zoonotic agents in the European Union in 2008, European Food Safety Authority Journal, 10, 1496.

    Google Scholar 

  • Fairbrother, J. M. and Nadeau, E., 2006. Escherichia coli: on farm contamination of animals, Revue scientifique et technique (OIE), 25, 555–569.

    CAS  Google Scholar 

  • Farzan, A., Friendship, R. M., Cook, A. and Pollari, F., 2010. Occurrence of Salmonella, Campylobacter, Yersinia enterocolitica, Escherichia coli O157 and Listeria monocytogenes in Swine, Zoonoses and Public Health, 57, 388–396.

    Article  CAS  PubMed  Google Scholar 

  • Fratamico, P.M., Bagi, L. K., Bush, E. L. and Solow, B. T., 2004. Prevalence and Characterization of Shiga Toxin-Producing Escherichia coli in Swine Feces Recovered in the National Animal Health Monitoring System’s Swine 2000 Study, Applied and Environmental Microbiology, 70, 7173–7178.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • García-Sánchez, A., Sánchez, S., Rubio, R., Pereira, G., Alonso, J.M., Hermoso de Mendoza, J. and Rey, J., 2007. Presence of Shiga toxin-producing E. coli O157:H7 in a survey of wild artiodactyls, Veterinary Microbiology, 121, 373–377.

    Article  PubMed  Google Scholar 

  • Gautam, R., Bani-Yaghoub, M., Neill, W.H., Döpfer, D., Kaspar, C. and Ivanek, R., 2011. Modeling the effect of seasonal variation in ambient temperature on the transmission dynamics of a pathogen with a free-living stage: example of Escherichia coli O157:H7 in a dairy herd, Preventive Veterinary Medicine, 102, 10–21.

    Article  PubMed  Google Scholar 

  • Growther, L., Lullu, P.K., Sukirtha, K. and Niren Andrew, S., 2013. Biotyping, molecular characterization and screening for antibacterial phytochemicals against shiga toxin producing E. coli from cattle, Archives of Applied Science Research, 5, 178–182.

    CAS  Google Scholar 

  • Gyles, C.L., 2007. Shiga toxin-producing Escherichia coli: an overview, Journal of Animal Science, 85, E45–62.

    Article  CAS  PubMed  Google Scholar 

  • Helmy, O.M., Ragab, Y.M. and Hussein, M. M. M., 2013. Multiplex polymerase chain reaction (PCR) for the detection of diarrheagenic Escherichia coli and Shigella directly from stool, African Journal of Microbiology Research, 7, 4368–4372.

    Google Scholar 

  • Hussein, H.S., 2007. Prevalence and pathogenicity of Shiga toxin-producing Escherichia coli in beef cattle and their products, Journal of Animal Science, 85, E63-E72.

    Article  CAS  PubMed  Google Scholar 

  • Jeong, K., Tzipori, S. and Sheoran, A. S., 2010. Shiga Toxin 2–Specific but Not Shiga Toxin 1–Specific Human Monoclonal Antibody Protects Piglets Challenged with Enterohemorrhagic Escherichia coli Producing Shiga Toxin 1 and Shiga Toxin 2, The Journal of Infectious Diseases, 201,1081–1083.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Karmali, M.A., Gannon, V. and Sargeant, J. M., 2010. Verocytotoxin-producing Escherichia coli (VTEC), Veterinary Microbiology, 140, 360–370.

    Article  CAS  PubMed  Google Scholar 

  • Kaufmann, M., Zweifel, C., Blanco, M., Blanco, J. E., Blanco, J., Beutin, L. and Stephan, R., 2006. Escherichia coli O157 and non-O157 Shigatoxin-producing Escherichia coli in fecal samples of finished pigs at slaughter in Switzerland, Journal of Food Protection, 69, 260–266.

    CAS  PubMed  Google Scholar 

  • Keen, J.E., Wittum, T.E., Dunn, J. R., Bono, J.L. and Durso, L.M., 2006. Shiga-toxigenic Escherichia coli O157 in agricultural fair livestock, United States, Emerging Infectious Diseases, 12, 780–786.

    Article  Google Scholar 

  • Livestock Census., 2007. 18th Livestock Census. Department of Animal Husbandry and Dairying, Government of India.

  • Lorenz, S.C., Son, I., Maounounen-Laasri, A., Lin, A., Fischer, M. and Kase, J. A., 2013. Prevalence of Hemolysin Genes and Comparison of ehxA Subtype Patterns in Shiga Toxin-Producing Escherichia coli (STEC) and Non- STEC Strains from Clinical, Food, and Animal Sources, Applied and Environmental Microbiology, 79, 6301– 6311.

    CAS  Google Scholar 

  • Meng, Q., Bai, Xiangning., Zhao, A., Lan, R., Du, H., Wang, T., Shi, C., Yuan, X., Bai, Xuemei, Ji, S., Jin, D., Yu, B., Wang, Y., Sun, H., Liu, K., Xu, J. and Xiong, Y., 2014. Characterization of Shiga toxin-producing Escherichia coli isolated from healthy pigs in China, BMC Microbiology,14:5.

    Article  PubMed Central  PubMed  Google Scholar 

  • Mohlatlole, R.P., Madoroba, E., Muchadeyi, F.C., Chimonyo, M., Kanengoni, A.T. and Dzomba, E. F., 2013. Virulence profiles of enterotoxigenic, shiga toxin and enteroaggregative Escherichia coli in South African pigs, Tropical Animal Health and Production, 45, 1399–405

    Article  PubMed  Google Scholar 

  • Moredo, F.A., Cappuccio, J.A., Insarralde, L., Perfumo, C.J., Quiroga, M.A. and Leotta, G.A., 2012. Genotypic characterization of toxigenic Escherichia coli isolated from pigs with postweaning diarrhea (PWD) and edema disease (ED), Revista Argentina de Microbiología, 44, 85–88.

    PubMed  Google Scholar 

  • Nakazawa, M., Akiba, M. and Sameshima, T., 1999. Swine as a Potential Reservoir of Shiga Toxin-Producing Escherichia coli O157:H7 in Japan, Emerging Infectious Diseases, 5, 833.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • OIE, 2008. Manual of Diagnostic Tests and Vaccines for Terrestrial Animals, Sixth Edition, edited by the OIE Biological Standards Commission and adopted by the International Committee of the OIE, pp.1294.

  • Ojo, O.E., Ajuwape, A.T.P., Otesile, E.B., Owoade, A.A., Oyekunle, M.A. and Adetosoye, A.I., 2010. Potentially zoonotic shiga toxin-producing Escherichia coli serogroups in the faeces and meat of food-producing animals in Ibadan, Nigeria, International Journal of Food Microbiology, 142, 214–221.

    Article  CAS  Google Scholar 

  • Rey, J., Blanco, J. E., Blanco, M., Mora, A., Dahbi, G., Alonso, J. M., Hermoso, M., Hermoso, J., Alonso, M. P., Usera, M.A., González, E. A., Bernárdez, M. I. and Blanco, J., 2003. Serotypes, phage types and virulence genes of Shiga-producing Escherichia coli isolated from sheep in Spain, Veterinary Microbiology, 94, 47–56.

    Article  CAS  PubMed  Google Scholar 

  • Sánchez, S., García-Sánchez, A., Martínez, R., Blanco, J., Blanco, J.E., Blanco, M., Dahbi, G., Mora, A., Hermoso de Mendoza, J., Alonso J.M. and Rey, J., 2009. Detection and characterisation of Shiga toxin-producing Escherichia coli other than Escherichia coli O157:H7 in wild ruminants, Veterinary Journal, 180, 384–388.

    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, Infection and Immunity, 63, 1055–1061.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Schroeder, C. M., Zhao, C., DebRoy, C., Torcolini, J. and Zhao, S., 2002. Antimicrobial resistance of Escherichia coli O157 isolated from humans, cattle, swine and food, Applied and Environmental Microbiology, 68, 576–581.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sehgal, R., Kumar, Y. and Kumar, S., 2008. Prevalence and geographical distribution of Escherichia coli O157 in India: a 10-year survey, Transactions of the Royal Society of Tropical Medicine and Hygiene, 102, 380—383.

    Article  PubMed  Google Scholar 

  • Shaw, D.J., Jenkins, C., Pearce, M.C., Cheasty, T., Gunn, G.J., Dougan, G., Smith, H.R., Woolhouse, M.E. and Frankel, G., 2004. Shedding patterns of verocytotoxin-producing Escherichia coli strains in a cohort of calves and their dams on a Scottish beef farm, Applied and Environmental Microbiology, 70: 7456–7465.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sonntag, A.K., Bielaszewska, M., Mellmann, A., Dierksen, N., Schierack, P., Wieler, L.H., Schmidt, M.A. and Karch, H., 2005. Shiga Toxin 2e-Producing Escherichia coli Isolates from Humans and Pigs Differ in Their Virulence Profiles and Interactions with Intestinal Epithelial Cells, Applied and Environmental Microbiology, 71, 8855–8863.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Suardana, W., Artama, W.T., Asmara, W. and Daryono, B.S., 2011. Adherence pheno-genotypic of Escherichia coli O157:H7 isolated from beef, feces of cattle, chicken and human, Indonesian Journal of Biotechnology, 16, 46–52.

    Google Scholar 

  • Tesh, V. L., 2012. Activation of cell stress response pathways by Shiga toxins, Cellular Microbiology, 14, 1–9.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • von Muffling, T., Smaijlovic, M., Nowak, B., Sammet, K., Bulte, M. and Klein, G., 2007. Preliminary study of certain serotypes, genetic and antimicrobial resistance profiles of verotoxigenic Escherichia coli (VTEC) isolated in Bosnia and Germany from cattle or pigs and their products, International Journal of Food Microbiology, 117, 185–191.

    Article  Google Scholar 

  • Vu Khac, H., Holoda, E., Pilipcinec, E., Blanco, M., Blanco, J. E., Mora, A., Dahbi, G., López, C., González, E. A. and Blanco, J. (2006) Serotypes, virulence genes, and PFGE profiles of Escherichia coli isolated from pigs with postweaning diarrhoea in Slovakia, BMC Veterinary Research 2: 10.

    Article  PubMed Central  PubMed  Google Scholar 

  • Wells, J.E., Shackelford, S.D., Berry, E.D., Kalchayanand, N., Bosilevac, J.M. and Wheeler, T.L., 2011. Impact of Reducing the Level of Wet Distillers Grains Fed to Cattle Prior to Harvest on Prevalence and Levels of Escherichia coli O157:H7 in Feces and on Hides, Journal of Food Protection, 74, 1611–1617.

    Article  CAS  PubMed  Google Scholar 

  • Witold, A.F. and Carolyn, J. H., 2011. Escherichia coli O157:H7: Animal Reservoir and Sources of Human Infection, Foodborne Pathogens and Disease, 8, 465–487.

    Article  Google Scholar 

  • Zhao, S., White, D.G., Ge, B., Ayers, S., Friedman, S., English, L., Wagner, D., Gaines, S. and Meng, J., 2001. Identification and characterization of integron-mediated antibiotic resistance among shiga toxin-producing Escherichia coli isolates. Applied Environmental Microbiology, 67, 1556–1564.

    Google Scholar 

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  1. National Research Centre on Pig, Indian Council of Agricultural Research (ICAR), Rani Guwahati, 781 131, Assam, India

    Swaraj Rajkhowa & Dilip Kumar Sarma

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Rajkhowa, S., Sarma, D.K. Prevalence and antimicrobial resistance of porcine O157 and non-O157 Shiga toxin-producing Escherichia coli from India. Trop Anim Health Prod 46, 931–937 (2014). https://doi.org/10.1007/s11250-014-0587-4

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