Identification and characterization of atypical enteropathogenic and Shiga toxin-producing Escherichia coli isolated from ground beef and poultry breast purchased in Botucatu, Brazil

Abstract

Atypical enteropathogenic (serotypes O4:H16, O8:H25, O68:H2, O105:H7, and OR:H25) and Shigatoxigenic (ONT:H46) Escherichia coli were isolated from samples of ground beef and poultry breast purchased in Botucatu, Brazil. Phenotypic and molecular characterization indicated the potential of these isolates to adhere to host epithelial cells and cause damage.

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References

  1. 1.

    Nataro JP, Kaper JB (1998) Diarrheagenic Escherichia coli. Clin Microbiol Rev 11:142–201

    CAS  Article  Google Scholar 

  2. 2.

    Trabulsi LR, Keller R, Gomes TA (2002) Typical and atypical enteropathogenic Escherichia coli. Emerg Infect Dis 8:508–513

    Article  Google Scholar 

  3. 3.

    Hernandes RT, Elias WP, Vieira MA, Gomes TA (2009) An overview of atypical enteropathogenic Escherichia coli. FEMS Microbiol Lett 297:137–149

    CAS  Article  Google Scholar 

  4. 4.

    Scaletsky IC, Silva ML, Trabulsi LR (1984) Distinctive patterns of adherence of enteropathogenic Escherichia coli to HeLa cells. Infect Immun 45:534–536

    CAS  Article  Google Scholar 

  5. 5.

    Girón JA, Ho AS, Schoolnik GK (1991) An inducible bundle-forming pilus of enteropathogenic Escherichia coli. Science 254(5032):710–713

    Article  Google Scholar 

  6. 6.

    Donnenberg MS, Girón JA, Nataro JP, Kaper JB (1992) A plasmid-encoded type IV fimbrial gene of enteropathogenic Escherichia coli associated with localized adherence. Mol Microbiol 6:3427–3437

    CAS  Article  Google Scholar 

  7. 7.

    Karch H, Tarr PI, Bielaszewska M (2005) Enterohaemorrhagic Escherichia coli in human medicine. Int J Med Microbiol 295:405–418

    CAS  Article  Google Scholar 

  8. 8.

    Riley LW, Remis RS, Helgerson SD, McGee HB, Wells JG, Davis BR, Hebert RJ, Olcott ES, Johnson LM, Hargrett NT, Blake PA, Cohen ML (1983) Hemorrhagic colitis associated with a rare Escherichia coli serotype. N Engl J Med 308:681–685

    CAS  Article  Google Scholar 

  9. 9.

    Gould LH, Mody RK, Ong KL, Clogher P, Cronquist AB, Garman KN, Lathrop S, Medus C, Spina NL, Webb TH, White PL, Wymore K, Gierke RE, Mahon BE, Griffin PM (2013) Increased recognition of non-O157 Shiga toxin-producing Escherichia coli infections in the United States during 2000-2010: epidemiologic features and comparison with E. coli O157 infections. Foodborne Pathog Dis 10:453–460

    Article  Google Scholar 

  10. 10.

    Frank C, Werber D, Cramer JP, Askar M, Faber M, an der Heiden M, Bernard H, Fruth A, Prager R, Spode A, Wadl M, Zoufaly A, Jordan S, Kemper MJ, Follin P, Müller L, King LA, Rosner B, Buchholz U, Stark K, Krause G (2011) Epidemic profile of Shiga-toxin-producing Escherichia coli O104:H4 outbreak in Germany. N Engl J Med 365(19):1771–1780

    CAS  Article  Google Scholar 

  11. 11.

    Kaper JB, O'Brien AD (2014) Overview and historical perspectives. Microbiol Spectr

  12. 12.

    McDaniel TK, Jarvis KG, Donnenberg MS, Kaper JB (1995) A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. Proc Natl Acad Sci U S A 92:1664–1668

    CAS  Article  Google Scholar 

  13. 13.

    Jerse AE, Yu J, Tall BD, Kaper JB (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 U S A 87:7839–7843

    CAS  Article  Google Scholar 

  14. 14.

    Toledo MRF, Fontes CF, Trabulsi LR (1982) EPM-modificação do meio de Rugai e Araújo para a realização simultânea dos testes de produção de gás a partir da glicose, H2S, urease e triptofanodesaminase. Rev Microbiol 13:309–315

    Google Scholar 

  15. 15.

    Toledo MRF, Fontes CF, Trabulsi LR (1982) MILi-um meio para a realização dos testes de motilidade, indol e lisina descarboxilase. Rev. Microbiol13, pp 230–235

    Google Scholar 

  16. 16.

    Dias RC, Dos Santos BC, Dos Santos LF, Vieira MA, Yamatogi RS, Mondelli AL, Sadatsune T, Sforcin JM, Gomes TA, Hernandes RT (2016) Diarrheagenic Escherichia coli pathotypes investigation revealed atypical enteropathogenic E. coli as putative emerging diarrheal agents in children living in Botucatu, São Paulo State, Brazil. APMIS 124(4):299–308

    CAS  Article  Google Scholar 

  17. 17.

    Cerqueira AMF, Tibana A, Guth BE (1997) High occurrence of Shiga-like toxin-producing strains among diarrheagenic Escherichia coli isolated from raw beef products in Rio de Janeiro City, Brazil. J Food Prot 60:177–180

    Article  Google Scholar 

  18. 18.

    Bergamini AMM, Simões M, Irino K, Gomes TA, Guth BE (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 

  19. 19.

    Peresi JTM, De Almeida IAZC, Vaz TMI, Hernandes RT, Teixeira ISC, Silva SIL, Graciano RAS, Pinheiro SR, Dos Santos LF (2016) Search for diarrheagenic Escherichia coli in raw kibbe samples reveals the presence of Shiga toxin-producing strains. Food Control 63:165–170

    CAS  Article  Google Scholar 

  20. 20.

    Ristori CA, Rowlands REG, Martins CG, Barbosa ML, dos Santos LF, Jakabi M, de Melo Franco BDG (2017) Assessment of consumer exposure to Salmonella spp., Campylobacter spp., and Shiga toxin-producing Escherichia coli in meat products at retail in the city of São Paulo, Brazil. Foodborne Pathog Dis 14:447–453

    CAS  Article  Google Scholar 

  21. 21.

    Clermont O, Christenson JK, Denamur E, Gordon DM (2013) The Clermont Escherichia coli phylo-typing method revisited: improvement of specificity and detection of new phylo-groups. Environ Microbiol Rep 5:58–65

    CAS  Article  Google Scholar 

  22. 22.

    Ori EL, Takagi EH, Andrade TS, Miguel BT, Cergole-Novella MC, Guth BEC, Hernandes RT, Dias RCB, Pinheiro SRS, Camargo CH, Romero EC, Dos Santos LF (2019) Diarrhoeagenic Escherichia coli and Escherichia albertii in Brazil: pathotypes and serotypes over a 6-year period of surveillance. Epidemiol Infect 147:1–9

  23. 23.

    Abe CM, Trabulsi LR, Blanco J, Blanco M, Dahbi G, Blanco JE, Mora A, Franzolin MR, Taddei CR, Martinez MB, Piazza RM, Elias WP (2009) Virulence features of atypical enteropathogenic Escherichia coli identified by the eae(+) EAF-negative stx(−) genetic profile. Diagn Microbiol Infect Dis 64:357–365

    CAS  Article  Google Scholar 

  24. 24.

    Gomes TA, Irino K, Girão DM, Girão VB, Guth BE, Vaz TM, Moreira FC, Chinarelli SH, Vieira MA (2004) Emerging enteropathogenic Escherichia coli strains? Emerg Infect Dis 10:1851–1855

    Article  Google Scholar 

  25. 25.

    Oliveira MG, Brito JR, Gomes TA, Guth BE, Vieira MA, Naves ZV, Vaz TM, Irino K (2008) Diversity of virulence profiles of Shiga toxin-producing Escherichia coli serotypes in food-producing animals in Brazil. Int J Food Microbiol 127:139–146

    Article  Google Scholar 

  26. 26.

    Blanco M, Blanco JE, Dahbi G, Mora A, Alonso MP, Varela G, Gadea MP, Schelotto F, González EA, Blanco J (2006) Typing of intimin (eae) genes from enteropathogenic Escherichia coli (EPEC) isolated from children with diarrhoea in Montevideo, Uruguay: identification of two novel intimin variants (muB and xiR/beta2B). J Med Microbiol 55(Pt 9:1165–1174

    CAS  Article  Google Scholar 

  27. 27.

    Vieira MA, Dos Santos LF, Dias RC, Camargo CH, Pinheiro SR, Gomes TA, Hernandes RT (2016) Atypical enteropathogenic Escherichia coli as aetiologic agents of sporadic and outbreak-associated diarrhoea in Brazil. J Med Microbiol 65(9):998–1006

    CAS  Article  Google Scholar 

  28. 28.

    Xu Y, Bai X, Zhao A, Zhang W, Ba P, Liu K, Jin Y, Wang H, Guo Q, Sun H, Xu J, Xiong Y (2016) Genetic diversity of Intimin gene of atypical enteropathogenic Escherichia coli isolated from human, animals and raw meats in China. PLoS One 11(3):e0152571

    Article  Google Scholar 

  29. 29.

    Cravioto A, Gross RJ, Scotland SM, Rowe B (1979) An adhesive factor found in strains of Escherichia coli belonging to the traditional infantile enteropathogenic serotypes. Curr Microbiol 3:95–99

    Article  Google Scholar 

  30. 30.

    Knutton S, Baldwin T, Williams PH, McNeish AS (1989) Actin accumulation at sites of bacterial adhesion to tissue culture cells: basis of a new diagnostic test for enteropathogenic and enterohemorrhagic Escherichia coli. Infect Immun 57:1290–1298

    CAS  Article  Google Scholar 

  31. 31.

    Rodrigues J, Scaletsky IC, Campos LC, Gomes TA, Whittam TS, Trabulsi LR (1996) Clonal structure and virulence factors in strains of Escherichia coli of the classic serogroup O55. Infect Immun 64:2680–2686

    CAS  Article  Google Scholar 

  32. 32.

    Vieira MA, Andrade JR, Trabulsi LR, Rosa AC, Dias AM, Ramos SR, Frankel G, Gomes TA (2001) Phenotypic and genotypic characteristics of Escherichia coli strains of non-enteropathogenic E. coli (EPEC) serogroups that carry eae and lack the EPEC adherence factor and Shiga toxin DNA probe sequences. J Infect Dis 183:762–772

    CAS  Article  Google Scholar 

  33. 33.

    Scaletsky IC, Aranda KR, Souza TB, Silva NP (2010) Adherence factors in atypical enteropathogenic Escherichia coli strains expressing the localized adherence-like pattern in HEp-2 cells. J Clin Microbiol 48(1):302–306

    CAS  Article  Google Scholar 

  34. 34.

    Donnenberg MS, Tacket CO, James SP, Losonsky G, Nataro JP, Wasserman SS, Kaper JB, Levine MM (1993) Role of the eaeA gene in experimental enteropathogenic Escherichia coli infection. J Clin Invest 92(3):1412–1417

    CAS  Article  Google Scholar 

  35. 35.

    Konowalchuk J, Speirs JI, Stavric S (1977) Vero response to a cytotoxin of Escherichia coli. Infect Immun 18:775–779

    CAS  Article  Google Scholar 

  36. 36.

    Afset JE, Bruant G, Brousseau R, Harel J, Anderssen E, Bevanger L, Bergh K (2006) Identification of virulence genes linked with diarrhea due to atypical enteropathogenic Escherichia coli by DNA microarray analysis and PCR. J Clin Microbiol 44:3703–3711

    CAS  Article  Google Scholar 

  37. 37.

    Vieira MA, Salvador FA, Silva RM, Irino K, Vaz TM, Rockstroh AC, Guth BE, Gomes TA (2010) Prevalence and characteristics of the O122 pathogenicity island in typical and atypical enteropathogenic Escherichia coli strains. JClin Microbiol 48:1452–1455

    Article  Google Scholar 

  38. 38.

    Mercado EH, Piscoche C, Contreras C, Durand D, Riveros M, Ruiz J, Ochoa TJ (2016) Pathogenicity Island O-122 in enteropathogenic Escherichia coli strains is associated with diarrhea severity in children from Lima Peru. Int J Med Microbiol 306:231–236

    CAS  Article  Google Scholar 

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Acknowledgments

This study was supported by a grant from Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, grant no. 2012/19077-0). M.A.V. and N.A.B.M. received a fellowship from FAPESP, grant no. 2013/23414-5 and 2013/03460-2, respectively. We thank Tânia A. T. Gomes for the helpful suggestions. Dr. A. Leyva (USA) helped with English editing of the manuscript.

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Correspondence to Rodrigo T. Hernandes.

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Tanabe, R.H.S., Vieira, M.A., Mariano, N.A.B. et al. Identification and characterization of atypical enteropathogenic and Shiga toxin-producing Escherichia coli isolated from ground beef and poultry breast purchased in Botucatu, Brazil. Braz J Microbiol 50, 1099–1103 (2019). https://doi.org/10.1007/s42770-019-00101-6

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Keywords

  • EPEC
  • STEC
  • Pathogenesis
  • Genotyping
  • Ground beef
  • Poultry breast and diarrhea