Occurrence and antimicrobial resistance of E. coli non-O157 isolated from beef in Mato Grosso, Brazil

Abstract

Shiga toxin–producing Escherichia coli (STEC) is an important public health concern pathogen, as it produces two toxins, Stx1 and Stx2, with cytotoxic capacity. In addition, STEC strains are frequently involved in food outbreaks worldwide, leading to public health challenges and economic losses. In this context, the occurrence and antimicrobial resistance profile of the STEC isolated from fresh beef produced in Mato Grosso, Brazil, were estimated. One hundred seven retail beef under vacuum-packaged produced by 13 different slaughterhouses were submitted to microbiological, molecular, and antimicrobial resistance analyses. STEC occurrence in beef was of 4.67%, and five strains presented the stx2 gene. The O111 serogroup, reported in several outbreak cases worldwide, was detected, and other serotypes (O8:H20, O22:H16, and O141:H49) were also isolated. All isolated strains displayed sensitivity to 12 antibiotics, except for two strains, which where streptomycin-resistant. The presence of STEC in retail beef samples indicates public health risks with significant economic impact throughout the retail beef chain.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2

References

  1. Bai, J., Paddock, Z.D., Shi, X., Li, S., An, B. and Nagaraja, T.G., 2012. Applicability of a multiplex PCR to detect the seven major Shiga toxin-producing Escherichia coli based on genes that code for serogroup-specific O-antigens and major virulence factors in cattle feces, Foodborne Pathogens Diseases, 9(6), 541–548. https://doi.org/10.1089/fpd.2011.1082.

    Article  CAS  Google Scholar 

  2. Bergamini, M., Simões, M., Irino, K., Aparecida, T., Gomes, 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, Brazilian Journal of Microbiology, 38, 553–556. https://doi.org/10.1590/S1517-83822007000300032.

    Article  Google Scholar 

  3. Bosilevac, J.M. and Koohmaraie, M., 2011. Prevalence and characterization of non-O157 shiga toxin-producing Escherichia coli isolates from commercial ground beef in the United States, Applied Environmental Microbiology, 77:2103–2112. https://doi.org/10.1128/AEM.02833-10

    Article  CAS  PubMed  Google Scholar 

  4. Bouzari, S., Jafari, A. and Aslani, M.M., 2012. Escherichia coli: A brief review of diarrheagenic pathotypes and their role in diarrheal diseases in Iran, Iranian Journal of Microbiology, 4(3):102–117.

    PubMed  PubMed Central  Google Scholar 

  5. Brasil. 2016. Ministério da Agricultura Quantidade de Abate Estadual por Ano/Espécie. Available:http://sigsif.agricultura.gov.br/sigsif_cons/!ap_abate_estaduais_cons?p_select=SIM&p_ano=2016&p_id_especie=9. Accessed in 27 November 2017.

  6. Brusa, V., Restovich, V., Galli, L., Teitelbaum, D., Signorini, M., Brasesco, H. and Leotta, G.A., 2017. Isolation and characterization of non-O157 Shiga toxin-producing Escherichia coli from beef carcasses, cuts and trimmings of abattoirs in Argentina, PLoS One, 12(8), 1–16. https://doi.org/10.1371/journal.pone.0183248

    Article  CAS  Google Scholar 

  7. Castro, V.S., Carvalho, R.C.T., Conte-Junior, C.A. and Figueiredo, E.E.S., 2017. Shiga-toxin producing Escherichia coli : pathogenicity, supershedding, diagnostic methods, occurrence, and foodborne outbreaks, Comprehensive Reviews in Food Science and Food Safety, https://doi.org/10.1111/1541-4337.12302

  8. Cergole-Novella, M.C., Nishimura, L.S., Irino, K., Vaz, T.M.I., De Castro, A.F.P., Leomil, L. and Guth B.E.C., 2006. Stx genotypes and antimicrobial resistance profiles of Shiga toxin-producing Escherichia coli strains isolated from human infections, cattle and foods in Brazil, FEMS Microbiology Letters, 259(2), 234–239. https://doi.org/10.1111/j.1574-6968.2006.00272.x

    Article  CAS  PubMed  Google Scholar 

  9. Cerqueira, A.M.F., Guth, B.E.C., Joaquim, R.M. and Andrade, J.R.C., 1999. High occurrence of Shiga toxin-producing Escherichia coli (STEC) in healthy cattle in Rio de Janeiro State, Brazil, Veterinary Microbiology, 70:111–121. https://doi.org/10.1016/S0378-1135(99)00123-6

    Article  CAS  PubMed  Google Scholar 

  10. CLSI. Clinical and Laboratory Standards Institute. 2014. Performance standards for antimicrobial susceptibility testing: 24th informational supplement M100-S24. Clinical and Laboratory Standards Institute. Wayne, PA.

  11. Colello, R., Etcheverría, A., Di Conza, I.J.A., Gutkind, G.O. and Padola, N.L., 2015. Antibiotic resistance and integrons in Shiga toxin-producing Escherichia coli (STEC), Brazilian Journal Microbiology, 46(1), 1–5. https://doi.org/10.1590/S1517-838246120130698.

    Article  CAS  Google Scholar 

  12. Conrad, C., Stanford, K., McAllister, T., Thomas, J. and Reuter, T., 2016. Shiga toxin-producing and current trends in diagnostics, Animal Frontiers, 6(2), 37. https://doi.org/10.2527/af.2016-0021.

    Article  Google Scholar 

  13. Feng, N., Zhou, Y., Fan, Y., Bi, Y., Yang, R., Zhou, Y. and Wang, X., 2017. Yersinia pestis detection by loop-mediated isothermal amplification combined with magnetic bead capture of DNA, Brazilian Journal of Microbiology, 1–10. https://doi.org/10.1016/j.bjm.2017.03.014.

  14. Guinée, P.A.M., Jansen, W.H., Wadström, T. and Sellwood, R., 1981. Escherichia coli associated with neonatal diarrhoea in piglets and calves, in Laboratory diagnosis in neonatal calf and pig diarrhoea, Current Topics in Veterinary Animal Science, 13, pp. 126–162.

  15. Guth, B.E.C., Ramos, S.R.T.S., Cerqueira, A.M.F., Andrade, J.R.C. and Gomes, T.A.T., 2002. Phenotypic and genotypic characteristics of Shiga toxin-producing Escherichia coli strains isolated from children in São Paulo, Brazil, Memórias do Instituto Oswaldo Cruz, 97(8), 1085–1089. https://doi.org/10.1590/S1517-83822007000300032.

    Article  Google Scholar 

  16. Hall, R.M. and Collis, C.M., 1995. Mobile gene cassettes and integrons: capture and spread of genes by site-specific recombination, Molecular Microbiology, 15(4), 593–600. https://doi.org/10.1111/j.1365-2958.1995.tb02368.x

    Article  CAS  PubMed  Google Scholar 

  17. Naseer, U., Løbersli, I., Hindrum, M., Bruvik, T. and Brandal, L.T., 2017. Virulence factors of Shiga toxin-producing Escherichia coli and the risk of developing hemolytic uraemic syndrome in Norway, 1992-2013, European Journal of Clinical Microbiology, 1613–1620. https://doi.org/10.1007/s10096-017-2974z.

  18. Ngbede, E.O., Raji, M.A., Kwanashie, C.N., Kwaga, J.K.P., 2017. Antimicrobial resistance and virulence profile of enterococci isolated from poultry and cattle sources in Nigeria, Tropical Animal Health and Production, 49(3), 451–458. https://doi.org/10.1007/s11250-016-1212-5.

    Article  PubMed  Google Scholar 

  19. Pianciola, L., D’Astek, B.A., Mazzeo, M., Chinen, I., Masana, M. and Rivas, M., 2016. Genetic features of human and bovine Escherichia coli O157:H7 strains isolated in Argentina, International Journal Medical Microbiology, 306(2), 123–130. https://doi.org/10.1016/j.ijmm.2016.02.005.

    Article  CAS  Google Scholar 

  20. Ribeiro, L.F., Barbosa, M.M.C., Pinto, F.R., Maluta, R.P., Oliveira, M.C., de Souza, V. and Fairbrother, J. M., 2016. Antimicrobial resistance and virulence factors of Escherichia coli in cheese made from unpasteurized milk in three cities in Brazil, Foodborne Pathogens Diseases, 13(9), 469–476. https://doi.org/10.1089/fpd.2015.2106

    Article  CAS  Google Scholar 

  21. Sandvang, D., Aarestrup, F.M. and Jensen, L.B., 1997. Characterisation of integrons and antibiotic resistance genes in Danish multiresistant Salmonella enterica Typhimurium DT104, FEMS Microbiology Letters, 157(1) 177–181. https://doi.org/10.1111/j.1574-6968.1997.tb12770.x.

  22. Souto, M.S.M., Coura, F.M., Dorneles, E.M.S., Stynen, A.P.R., Alves, T.M., Santana, J.A., Lage, A.P, 2017. Antimicrobial susceptibility and phylotyping profile of pathogenic Escherichia coli and Salmonella enterica isolates from calves and pigs in Minas Gerais, Brazil, Tropical Animal Health and Production, 49(1), 13–23. https://doi.org/10.1007/s11250-016-1152-0

    Article  PubMed  Google Scholar 

  23. USDA. United States Department of Agriculture. 2011. Food and Drug Administration - Bacteriological Analytical Manual Chapter 4ª Diarrheagenic Escherichia coli. Available: http://www.fda.gov/Food/FoodScienceResearch/LaboratoryMethods/ucm070080.htm#STECPROT. Acessed: 28 November 2017.

  24. USDA. United States Department of Agriculture. Food and Drug Administration. Enumeration of Escherichia coli and the coliform bacteria. Bacteriological Analytical Manual (BAM) 2002. Available: http://www.fda.gov/Food/FoodScienceResearch/LaboratoryMethods/ucm064948.htm 2002 Accessed: 28 November 2017.

  25. USDA. United States Department of Agriculture. Foreign Agricultural Service. 2017. Available:https://www.fas.usda.gov/data/search?f[0]=field_commodities%3A23&f[1]=field_topics%3A43. Accessed: 28 November 2017.

  26. Vaz, T.M.I., Irino, K., Kato, M.A.M.F., Dias, A.M.G., Gomes, T.A.T., Medeiros, M.I.C. and Guth, B.E.C., 2004. Virulence properties and characteristics of Shiga toxin-producing Escherichia coli in São Paulo, Brazil, from 1976 through 1999, Journal of Clinical Microbiology 42(2), 903–5. https://doi.org/10.1128/JCM.42.2.903-905.2004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Wang, Y. and Salazar, J.K., 2016. Culture-independent rapid detection methods for bacterial pathogens and toxins in food matrices, Comprehensive Reviews in Food Science and Food Safety, 15(1), 183–205. https://doi.org/10.1111/1541-4337.12175.

    Article  CAS  Google Scholar 

  28. Watahiki, M., Isobe, J., Kimata, K., Shima, T., Kanatani, J.I., Shimizu, M. and Sata, T., 2014. Characterization of enterohemorrhagic Escherichia coli O111 and O157 strains isolated from outbreak patients in Japan, Journal of Clinical Microbiology, 52(8), 2757–2763. https://doi.org/10.1128/JCM.00420-14.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. White, P.A., McIver, C.J. and Rawlinson, W.D., 2001. Integrons and gene cassettes in the Enterobacteriaceae, Antimicrobrial Agents and Chemotherapy, 45:2658–2661. https://doi.org/10.1128/AAC.45.9.2658-2661.2001.

Download references

Acknowledgments

The authors would like to thank Dr. Rachel Ann Hauser-Davis (Fiocruz) for manuscript revision. The Fiocruz Enterobacteria Laboratory (LABENT), Fundação de Amparo à Pesquisa do Estado de Mato Grosso—FAPEMAT, and the Coordenação de Aperfeiçoamento de Pessoal do Ensino Superior (CAPES).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Eduardo Eustáquio de Souza Figueiredo.

Ethics declarations

Disclosure statement

The authors declare no conflicts of interest. The manuscript does not contain clinical studies or patient data.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Castro, V.S., Teixeira, L.A.C., Rodrigues, D.d. et al. Occurrence and antimicrobial resistance of E. coli non-O157 isolated from beef in Mato Grosso, Brazil. Trop Anim Health Prod 51, 1117–1123 (2019). https://doi.org/10.1007/s11250-018-01792-z

Download citation

Keywords

  • STEC
  • stx1 and stx2 genes
  • Antimicrobial resistance
  • Vacuum-packaged beef
  • O111