Skip to main content
Log in

Detection and analysis of Shiga toxin producing and enteropathogenic Escherichia coli in cattle from Tierra del Fuego, Argentina

  • Veterinary Microbiology - Research Paper
  • Published:
Brazilian Journal of Microbiology Aims and scope Submit manuscript

Abstract

Shiga toxin producing Escherichia coli (STEC) and enteropathogenic E. coli (EPEC) are pathovars that affect mainly infants’ health. Cattle are the main reservoir of STEC. Uremic hemolytic syndrome and diarrheas can be found at high rates in Tierra del Fuego (TDF). This study aimed to establish the prevalence of STEC and EPEC in cattle at slaughterhouses in TDF and to analyze the isolated strains. Out of 194 samples from two slaughterhouses, STEC prevalence was 15%, and EPEC prevalence was 5%. Twenty-seven STEC strains and one EPEC were isolated. The most prevalent STEC serotypes were O185:H19 (7), O185:H7 (6), and O178:H19 (5). There were no STEC eae + strains (AE-STEC) or serogroup O157 detected in this study. The prevalent genotype was stx2c (10/27) followed by stx1a/stx2hb (4/27). Fourteen percent of the strains presented at least one stx non-typeable subtype (4/27). Shiga toxin production was detected in 25/27 STEC strains. The prevalent module for the Locus of Adhesion and Autoaggregation (LAA) island was module III (7/27). EPEC strain was categorized as atypical and with the ability to cause A/E lesion. The ehxA gene was present in 16/28 strains, 12 of which were capable of producing hemolysis. No hybrid strains were detected in this work. Antimicrobial susceptibility tests showed that all strains were resistant to ampicillin and 20/28 were resistant to aminoglycosides. No statistical differences could be seen in the detection of STEC or EPEC either by slaughterhouse location or by production system (extensive grass or feedlot). The rate of STEC detection was lower than the one reported for the rest of Argentina. STEC/EPEC relation was 3 to 1. This is the first study on cattle from TDF as reservoir for strains that are potentially pathogenic to humans.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References 

  1. Trabulsi LR, Keller R, Gomez TAT (2002) Typical and atypical enteropathogenic Escherichia coli. Emerg Infect Dis 8:508–513. https://doi.org/10.3201/eid0805.010385

    Article  PubMed  PubMed Central  Google Scholar 

  2. Guth BEC, Prado V, Rivas M (2010) Shiga toxin-producing Escherichia coli. En Pathogenic Escherichia coli in Latin America, Torres, A.G. (Ed). Bentham Science Publishers U.S.A, pp 25–47 https://doi.org/10.2174/97816080519221100101

  3. Tyler SD, Johnson WM, Lior H, Wang G, Rozee KR (1991) Identification of verotoxin type 2 variant B subunit genes in Escherichia coli by the polymerase chain reaction and restriction fragment length polymorphism analysis. J Clin Microbiol 29(7):1339–431343. https://doi.org/10.1128/jcm.29.7.1339-1343.1991

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Scheutz F, Teel LD, Beutin L, Pierard D, Buvens G, Karch H, Mellmann A, Caprioli A, Tozzoli R, Morabito S, Strockbine NA, Melton-Celsa AR, Sanchez M, Persson S, O’Brien AD (2012) Multicenter evaluation of a sequence-based protocol for subtyping Shiga toxins and standardizing Stx nomenclature. J Clin Microbiol 50:2951–63. https://doi.org/10.1128/JCM.00860-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Werber D, Scheutz F (2019) The importance of integrating genetic strain information for managing cases of Shiga toxin-producing E. coli infection. Epidemiol Infect 147:e264. https://doi.org/10.1017/S0950268819001602

    Article  PubMed  PubMed Central  Google Scholar 

  6. EFSA BIOHAZ Panel, Koutsoumanis K, Allende A, Alvarez-Ordoñez A, Bover-Cid S, Chemaly M, Davies R, De Cesare A, Herman L, Hilbert F, Lindqvist R, Nauta M, Peixe L, Ru G, Simmons M, Skandamis P, Suffredini E, Jenkins C, Monteiro Pires S, Morabito S, Niskanen T, Scheutz F, da Silva Felício MT, Messens W, Bolton D (2020) Pathogenicity assessment of Shiga toxin-producing Escherichia coli (STEC) and the public health risk posed bycontamination of food with STEC. Efsa J Sci Opin. https://doi.org/10.2903/j.efsa.2020.5967

    Article  Google Scholar 

  7. Gomes TAT, González-Pedrajo B, Enteropathogenic Escherichia coli (EPEC) (2010). En Pathogenic Escherichia coli in Latin America, Torres AG (ed). Bentham Science Publishers U.S.A, pp 25–47. https://doi.org/10.2174/97816080519221100101

  8. Nataro JP, Kaper JB (1998) Diarrheagenic Escherichia coli. Clin Microbiol Rev 11(1):142–201. https://doi.org/10.1128/CMR.11.1.142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Parma AE, Sanz ME, Blanco JE, Blanco J, Viñas MR, Blanco M, Padola NL, Etcheverría AI (2000) Virulence genotypes and serotypes of verotoxigenic Escherichia coli isolated from cattle and foods in Argentina. Eur J Epidemiol 2000(16):757–762. https://doi.org/10.1023/a:1026746016896

    Article  Google Scholar 

  10. Piérard D, De Greve H, Haesebrouck F, Mainil J (2012) O157:H7 and O104:H4 Vero/Shiga toxin-producing Escherichia coli outbreaks: respective role of cattle and humans. Vet Res 43(1):13. https://doi.org/10.1186/1297-9716-43-13

    Article  PubMed  PubMed Central  Google Scholar 

  11. Hernandes RT, Elias WP, Vieira MAM, Gomes TAT (2009) An overview of atypical enteropathogenic Escherichia coli. FEMS Microbiol Lett 297(2):137–149. https://doi.org/10.1111/j.1574-6968.2009.01664.x

    Article  CAS  PubMed  Google Scholar 

  12. Kolenda R, Burdukiewicz M, Schierack, (2015) A systematic review and meta-analysis of the epidemiology of pathogenic Escherichia coli of calves and the role of calves as reservoirs for human pathogenic E. coli. Front Cell Infect Microbiol. https://doi.org/10.3389/fcimb.2015.002

    Article  PubMed  PubMed Central  Google Scholar 

  13. Acuña P, Rojas N, Florentin M, Rodriguez F (2019) Estandarización de una técnica de PCR múltiple para la detección de los serogrupos O157, O104 y “big six” de Escherichia coli productora de la toxina Shiga (STEC). Memorias del Instituto de Investigaciones en Ciencias de la Salud 17(2):71–76. https://doi.org/10.18004/mem.iics/1812-9528/2019.017.02.71-076

    Article  Google Scholar 

  14. Fakih I, Thiry D, Duprez J-N, Saulmont M, Iguchi A, Piérard D, Jouant L, Daube G, Ogura Y, Hayashi T, Taminiau B, Mainil JG (2017) Identification of Shiga toxin-producing (STEC) and enteropathogenic (EPEC) Escherichia coli in diarrhoeic calves and comparative genomics of O5 bovine and human STEC. Vet Microbiol 202:16–22. https://doi.org/10.1016/j.vetmic.2016.02.017

    Article  CAS  PubMed  Google Scholar 

  15. Kaper JB, Nataro JP, Mobley HL (2004) Pathogenic Escherichia coli. Nat Rev Microbiol 2(2):123–140. https://doi.org/10.1038/nrmicro818

    Article  CAS  PubMed  Google Scholar 

  16. Rivas M, Chinen I, Guth BEC (2016) Enterohemorrhagic (Shiga toxin –producing) Escherichia coli. En Escherichia coli in the Americas, Torres AG (Ed) Springer International Publishing, U.S.A, 2016, 149–72. https://doi.org/10.2174/97816080519221100101

  17. Newton HJ, Sloan J, Bulach DM, Seemann T, Allison CC, Tauschek M, Robins-Browne RM, Paton JC, Whittam TS, Paton AW, Hartland EL (2009) Shiga toxin–producing Escherichia coli strains negative for locus of enterocyte effacement. Emerg Infect Dis 15(3):372–380. https://doi.org/10.3201/eid1502.080631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Montero DA, Velasco J, Del Canto F, Puente JL, Padola NL, Rasko DA, Farfán M, Salazar JC, Vidal R (2017) Locus of Adhesion and Autoaggregation (LAA), a pathogenicity island present in emerging Shiga toxin-producing Escherichia coli strains. Sci Rep 7(1):7011. https://doi.org/10.1038/s41598-017-06999-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Bielaszewska M, Mellmann A, Zhang W, Köck R, Fruth A, Bauwens A, Peters G, Karch H (2011) Characterisation of the Escherichia coli strain associated with an outbreak of haemolytic uraemic syndrome in Germany, 2011: a microbiological study. Lancet Infect Dis 11:671–76. https://doi.org/10.1016/S1473-3099(11)70165-7

    Article  CAS  PubMed  Google Scholar 

  20. Ministerio de Salud de la Nación. Boletín Integrado de Vigilancia N222-SE30 (2014) Informe Especial I: Síndrome urémico hemolítico (SUH) en Argentina, 2010 – 2013, p. 92 – 103. Retrieved from: https://www.argentina.gob.ar/salud/epidemiologia/boletines2014. Accessed June 2022

  21. Amigo N, Mercado E, Bentancor A, Singh P, Vilte D, Gerhardt E, Zotta E, Ibarra C, Manning SD, Larzábal M, Cataldi A (2015) Clade 8 and clade 6 strains of Escherichia coli O157:H7 from cattle in Argentina have hypervirulent-like phenotypes. PLoS One 10(6):e0127710. https://doi.org/10.1371/journal.pone.0127710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Ministerio de Salud de la Nación. Boletín Integrado de Vigilancia N477-SE50 (2019). Retrieved from: https://www.argentina.gob.ar/salud/epidemiologia/. Accessed June 2022

  23. Prack McCormick B, Quiroga MP, Álvarez VE, Centrón D, Tittonell P (2022) Diseminación de la resistencia a antimicrobianos asociada a prácticas de producción animal intensiva en Argentina: Una revisión sistemática y metaanálisis. Rev Argent Microbiol. https://doi.org/10.1016/j.ram.2022.07.001

    Article  PubMed  Google Scholar 

  24. Orden JA, Cid D, Ruiz-Santa-Quiteria JA, García S, Martínez S, de la Fuente R (2002) Verotoxin- producing Escherichia coli (VTEC), enteropathogenic E. coli (EPEC) and necrotoxigenic E. coli (NTEC) isolated from healthy cattle in Spain. J Appl Microbiol 93:29–35. https://doi.org/10.1046/j.1365-2672.2002.01649.x

    Article  CAS  PubMed  Google Scholar 

  25. Bentancor A, Rumi MV, Gentilini MV, Sardoy C, Irino K, Agostini A, Cataldi A (2007) Shiga toxin-producing and attaching and effacing Escherichia coli in cats and dogs in a high hemolytic uremic syndrome incidence region in Argentina. FEMS Microbiol Lett 267:251–256. https://doi.org/10.1111/j.1574-6968.2006.00569.x

    Article  CAS  PubMed  Google Scholar 

  26. Blanco Crivelli X, Bonino MP, Sanin M, Petrina JF, Disalvo V, Massa R, Miliwebsky E, Navarro A, Chinen I, Bentancor A (2021) Potential zoonotic pathovars of diarrheagenic Escherichia coli detected in lambs for human consumption from Tierra del Fuego. Argent Microorganisms 9(8):1710. https://doi.org/10.3390/microorganisms9081710

    Article  CAS  Google Scholar 

  27. Leotta G, Chinen I, Epszteyn S, Miliwebsky E, Melamed IC, Motter M, Ferrer M, Marey E, Rivas M (2005) Validación de una técnica de PCR múltiple para la detección de Escherichia coli productor de toxina Shiga. Revista Argentina de Microbiología 37:1–10. Retrieved from: https://www.redalyc.org/articulo.oa?id=213016778001

  28. Blanco M, Blanco JE, Mora A, Dahbi G, Alonso MP, González EA, Bernárdez MI, Blanco J (2004) Serotypes, virulence genes, and intimin types of Shiga Toxin (Verotoxin)-producing Escherichia coli isolates from cattle in Spain and identification of a new intimin variant gene (eae). J Clin Microbiol 42:645–651. https://doi.org/10.1128/JCM.42.2.645-651.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. MacFaddin JF (2003) Pruebas bioquímicas para la identificación de bacterias de importancia clínica, 3rd edn. Buenos Aires, Argentina, Médica Panamericana Ed, pp 54–421

  30. Gunzburg ST, Tornieporth NG, Riley LW (1995) Identification of enteropathogenic Escherichia coli by PCR-based detection of the bundle-forming pilus gene. J Clin Microbiol 33:1375–1377. https://doi.org/10.1128/jcm.33.5.1375-1377.1995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Paton AW, Paton JC (2002) Direct detection and characterization of Shiga toxigenic Escherichia coli by multiplex PCR for stx1, stx2, eae, ehxA, and saa. J Clin Microbiol 40(1):271–274. https://doi.org/10.1128/JCM.40.1.271-274.2002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Boisen N, Scheutz F, Rasko DA, Redman JC, Persson S, Simon J, Kotloff KL, Levine MM, Sow S, Tamboura B, Toure A, Malle D, Panchalingam S, Krogfelt KA, Nataro JP (2012) Genomic characterization of enteroaggregative Escherichia coli from children in Mali. J Infect Dis 205(3):431–444. https://doi.org/10.1093/infdis/jir757

    Article  CAS  PubMed  Google Scholar 

  33. Wieler LH, Semmler T, Eichhorn I, Antao EM, Kinnemann B, Geue L, Karch H, Guenther S, Bethe A (2011) No evidence of the Shiga toxin-producing E. coli O104:H4 outbreak strain o enteroaggregative E. coli (EAEC) found in cattle faeces in northern Germany, the hostpot of the 2011. HUS outbreak area. Gut Pathogens 3:17. https://doi.org/10.1186/1757-4749-3-17

    Article  CAS  PubMed  Google Scholar 

  34. Itoh F, Ogino T, Itoh F, Watanabe H (1992) Differentiation and detection of pathogenic determinants among diarrheagenic Escherichia coli by polymerase chain reaction using mixed primers. Jpn J Clin Med 50:343–347

    Google Scholar 

  35. Vidal M, Kruger C, Duran R, Lagos R, Levine M, Prado V, Toro C, Vidal R (2005) Single PCR assay to identify simultaneously the six categories of diarrheagenic Escherichia coli associated with enteric infections. J Clin Microbiol 43(10):5362–5365. https://doi.org/10.1128/JCM.43.10.5362-5365.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Miliwebsky E, Deza N, Zolezzi G, Baschkier A, Carbonari CC, Manfredi E, D’Astek BA, Chinen I, Rivas M (2019) Manual de Procedimientos: Escherichia coli Productor de Toxina Shiga en el Marco de la Detección de E.coli diarreigénico. Retrieved from: http://sgc.anlis.gob.ar/handle/123456789/2307

  37. Scaletsky IC, Silva ML, Trabulsi LR (1984) Distinctive patterns of adherence of Enteropathogenic Escherichia coli to HeLa cells. Infect Immun 45(2):534–536. https://doi.org/10.1128/iai.45.2.534-536.1984

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Gomes TAT, Irino K, Girão DM, Girão VBC, Guth BEC, Vaz TMI, Moreira FC, Chinarelli SH, Vieira MAM (2004) Emerging enteropathogenic Escherichia coli strains? Emerg Infect Dis 10(10):1851–1855. https://doi.org/10.3201/eid1010.031093

    Article  PubMed  PubMed Central  Google Scholar 

  39. Nakazato G, Gyles C, Ziebell K, Keller R, Trabulsi LR, Gomes TAT, Irino K, Da Silveira WD, Pestana De Castro AF (2004) Attaching and effacing Escherichia coli isolated from dogs in Brazil: characteristics and serotypic relationship to human enteropathogenic E. coli (EPEC). Vet Microbiol 101(4):269–77. https://doi.org/10.1016/j.vetmic.2004.04.009

    Article  CAS  PubMed  Google Scholar 

  40. Edwards PR, Ewing WH (1986) Edwards and Ewing’s identification of Enterobacteriaceae, 4th edn. Elsevier Science Publishing Inc, New York, USA

  41. Orskov F, Orskov I (1984) Serotyping of Escherichia coli. Methods Microbiol 14:43–112. https://doi.org/10.1016/S0580-9517(08)70447-1

    Article  Google Scholar 

  42. Performance Standards for Antimicrobial Susceptibility Testing (2018) 28th Edition. Weinstein, MP, Patel JB. Clinical and Laboratory Standards Institut. Retrieved from: https://file.qums.ac.ir/repository/mmrc/CLSI-2018-M100-S28.pdf. Accessed Mar 2022

  43. INEI-ANLIS (2017) Administración Nacional de Laboratorios e Institutos de Salud. Dr. Carlos G. Malbrán. Servicio Antimicrobianos, Laboratorio Nacional de Referencia en Antimicrobianos, Método de Screening “COLISTIN AGAR-SPOT” Versión 2. Retrieved from: http://antimicrobianos.com.ar/ATB/wp-content/uploads/2017/09/Protocolo-Agar-spot-COL-2017-version2-Agosto2017.pdf. Accessed Mar 2022

  44. Famiglietti A, Quinteros M, Vázquez M, Marin M, Nicola F, Radice M, Galas MF, Pasterán FG, Bantar C, Casellas JM, Kovensky Pupko J, Couto E, Goldberg M, Lopardo H, Gutkind G, Soloaga R (2005) Consenso sobre las pruebas de sensibilidad a los antimicrobianos en Enterobacteriaceae. Revista Argentina de Microbiología 37: 57–66. ISSN 0325–7541 ARTÍCULO ESPECIAL Revista Argentina de Microbiología 37: 57–66

  45. Padola NL, Sanz ME, Blanco JE, Blanco M, Blanco J, Etcheverría AI, Arroyo GH, Usera MA, Parma AE (2004) Serotypes and virulence genes of bovine Shigatoxigenic Escherichia coli (STEC) isolated from a feedlot in Argentina. Vet Microbiol 100(1–2):3–9. https://doi.org/10.1016/S0378-1135(03)00127-5

    Article  CAS  PubMed  Google Scholar 

  46. Pizarro MA, Orozco JH, Degarbo SM, Calderón AE, Nardello AL, Laciar A, Rüttler ME (2014) Virulence profiles of Shiga toxin-producing Escherichia coli and other potentially diarrheagenic Ecoli of bovine origin, in Mendoza, Argentina. Braz J Microbiol 44(4):1173–1180. https://doi.org/10.1590/S1517-83822014005000010

    Article  PubMed  PubMed Central  Google Scholar 

  47. Etcheverría AI, Lucchesi PMA, Krüger A, Bentancor AB, Padola N (2016) Escherichia coli in Animals. En Escherichia coli in the Americas, Torres AG (Ed.) Springer International Publishing, U.S.A., pp 149–72. https://doi.org/10.2174/97816080519221100101

  48. Masana MO, Leotta GA, Del Castillo LL, D’Astek BA, Palladino PM, Galli L (2010) Prevalence, characterization and genotypic analysis of Escherichia coli O157:H7/NM from selected beef exporting abattoirs of Argentina. J Food Protect 73(4):649–56. https://doi.org/10.4315/0362-028x-73.4.649

    Article  CAS  Google Scholar 

  49. Tanaro JD, Galli L, Lound LH, Leotta GA, Piaggio MC, Carbonari CC, Irino K, Rivas M (2012) Non-O157:H7 Shiga toxin–producing Escherichia coli in bovine rectums and surface water streams on a beef cattle farm in Argentina. Foodborne Pathog Dis 9(10):878–884. https://doi.org/10.1089/fpd.2012.1182

    Article  CAS  PubMed  Google Scholar 

  50. Masana M, D’Astek BA, Palladino PM, Galli L, del Castillo LL, Carbonari CC, Leotta GA, Vilacoba E, Irino K, Rivas M (2011) Genotypic characterization of non-O157 Shiga toxin–producing Escherichia coli in beef abattoirs of Argentina. J Food Protect 74(12):2008–17. https://doi.org/10.4315/0362-028X.JFP-11-189

    Article  CAS  Google Scholar 

  51. Brusa V, Restovich V, Galli L, Teitelbaum D, Signorini M, Brasesco H, Londero A, García D, Padola NL, Superno V, Sanz M, Petroli S, Costa M, Bruzzone M, Sucari A, Ferreghini M, Linares L, Suberbie G, Rodriguez R, Leotta GA (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):e0183248. https://doi.org/10.1371/journal.pone.0183248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Cundon C, Carbonari CC, Zolezzi G, Rivas M, Bentancor A (2018) Putative virulence factors and clonal relationship of O174 Shiga toxin-producing Escherichia coli isolated from human, food and animal sources. Vet Microbiol 215:29–34. https://doi.org/10.1016/j.vetmic.2017.12.006

    Article  CAS  PubMed  Google Scholar 

  53. Rhades LC, Larzábal M, Bentancor A, Sabio y García J, Babineca FJ, Cataldi A, Amigo N, Baldone VN, Urquiza L, Delicia PJ, Forta MC (2019) A one-year longitudinal study of enterohemorrhagic Escherichia coli O157 fecal shedding in a beef cattle herd. Research in Veterinary Science 127:27–32. https://doi.org/10.1016/j.rvsc.2019.10.001

    Article  CAS  PubMed  Google Scholar 

  54. Beutin L, Geier D, Zimmermann S, Karch H (1995) Virulence markers of Shiga-like toxin-producing Escherichia coli strains originating from healthy domestic animals of different species. J Clin Microbiol 33(3):631–635. https://doi.org/10.1128/jcm.33.3.631-635.1995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Blanco M, Blanco JE, Blanco J, Gonzalez EA, Mora A, Prado C, Fernández L, Rio M, Ramos J, Alonso MP (1996) Prevalence and characteristics of Escherichia coli serotype O157:H7 and other verotoxin-producing E. coli in healthy cattle. Epidemiology & Infection 117(2):251–7. https://doi.org/10.1017/s0950268800001424

    Article  CAS  Google Scholar 

  56. Etcheverría AI, Padola NL (2013) Shiga toxin-producing Escherichia coli Factors involved in virulence and cattle colonization. Virulence 4(5):366–372. https://doi.org/10.4161/viru.24642

    Article  PubMed  PubMed Central  Google Scholar 

  57. Fernández D, Rodriguez EM, Arroyo GH, Padola NL, Parma AE (2009) Seasonal variation of Shiga toxin-encoding genes (stx) and detection of E. coli O157 in dairy cattle from Argentina. J Appl Microbiol 106(4):1260–7. https://doi.org/10.1111/j.1365-2672.2008.04088.x

    Article  CAS  PubMed  Google Scholar 

  58. Fan R, Shao K, Yang X, Bai X, Fu S, Sun H, Xu Y, Wang H, Li Q, Hu B, Zhang J, Xiong Y (2019) High prevalence of non-O157 Shiga toxin producing Escherichia coli in beef cattle detected by combining four selective agars. BMC Microbiol 19:213. https://doi.org/10.1186/s12866-019-1582-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Coombes BK, Wickham ME, Mascarenhas M, Gruenheid S, Finlay BB, Karmali MA (2008) Molecular analysis as an aid to assess the public health risk of non-O157 Shiga toxin-producing Escherichia coli strains. Appl Environ Microbiol 74(7):2153–2160. https://doi.org/10.1128/AEM.02566-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Byrne L, Jenkins C, Launders N, Elson R, Adak GK (2015) The epidemiology, microbiology and clinical impact of Shiga toxin-producing Escherichia coli in England, 2009–2012. Epidemiology & Infection 143(16):3475–87. https://doi.org/10.1017/S0950268815000746

    Article  CAS  Google Scholar 

  61. Valilis E, Ramsey A, Sidiq S, DuPont HL (2018) Non-O157 Shiga toxin-producing Escherichia coli - a poorly appreciated enteric pathogen: systematic review. Int J Infect Dis 76:82–87. https://doi.org/10.1016/j.ijid.2018.09.002

    Article  CAS  PubMed  Google Scholar 

  62. Rivero MA, Padola NL, Etcheverria AI, Parma AE (2004) Escherichia coli Enterohemorragica y Sindrome Urémico hemolítico en Argentina. MEDICINA 64: 352–356 ISSN 1669–9106

  63. Fernández D, Krüger A, Polifroni R, Bustamante AV, Sanso AM, Etcheverría AI, Lucchesi PMA, Parma AE, Padola NL (2013) Characterization of Shiga toxin-producing Escherichia coli O130:H11 and O178:H19 isolated from dairy cows. Front Cell Infect Microbiol 2013(3):9. https://doi.org/10.3389/fcimb.2013.00009

    Article  Google Scholar 

  64. Llorente P, Barnech L, Irino K, Rumi MV, Bentancor A (2014) Characterization of Shiga toxin-producing Escherichia coli isolated from ground beef collected in different socioeconomic strata markets in Buenos Aires, Argentina. Biomed Res Int 2014:795104. https://doi.org/10.1155/2014/795104

    Article  PubMed  PubMed Central  Google Scholar 

  65. Bielaszewska M, Friedrich AW, Aldick T, Schurk-Bulgrin R, Karch H (2006) Shiga toxin activatable by intestinal mucus in Escherichia coli isolated from humans: predictor for a severe clinical outcome. Clin Infect Dis 43:1160–1167. https://doi.org/10.1086/508195

    Article  CAS  PubMed  Google Scholar 

  66. Giugno SM, Bibiloni N, Rahman R, Miliwebsky E, Chinen I, Rivas M (2007) Association between uremic hemolytic syndrome and infection by Shiga toxin-producing Escherichia coli. Acta Bioquímica Clínica Latinoamericana 41:27–33. ISSN 0325–2957; ISSN 1851–6114

  67. Werber D, Beutin L, Pichner R, Stark K, Fruth A (2008) Shiga toxin-producing Escherichia coli serogroups in food and patients, Germany. Emerg Infect Dis 14:1803–1806. https://doi.org/10.3201/eid1411.080361

    Article  PubMed  PubMed Central  Google Scholar 

  68. De Toni F, de Souza EM, Pedrosa FO, Klassen G, Irino K, Un Rigo L, Steffens MBR, Fialho OB, Farah SMSS, Fadel-Picheth CMT (2009) A prospective study on Shiga toxin-producing Escherichia coli in children with diarrhea in Parana State, Brazil. Lett Appl Microbiol 48:645–647. https://doi.org/10.1111/j.1472-765X.2009.02569.x

    Article  CAS  PubMed  Google Scholar 

  69. Buvens G, Lauwers S, Pierard D (2010) Prevalence of subtilase cytotoxin in verocytotoxin-producing Escherichia coli isolated from humans and raw meats in Belgium. Eur J Clin Microbiol Infect Dis 29:1395–1399. https://doi.org/10.1007/s10096-010-1014-z

    Article  CAS  PubMed  Google Scholar 

  70. Miko A, Rivas M, Bentancor A, Delannoy S, Fach P, Beutin L (2014) Emerging types of Shiga toxin-producing E. coli (STEC) O178 present in cattle, deer, and humans from Argentina and Germany. Front Cell Infect Microbiol 4:78. https://doi.org/10.3389/fcimb.2014.00078

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Qin X, Klein EJ, Galanakis E, Thomas AA, Stapp JR, Rich S, Buccat AM, Tarr PI (2005) Real-time PCR assay for detection and differentiation of Shiga toxin-producing Escherichia coli from clinical samples. J Clin Microbiol 53(7):2148–2153. https://doi.org/10.1128/JCM.00115-15

    Article  CAS  Google Scholar 

  72. Wang L, Jokinen CC, Laing CR, Johnson RP, Ziebell K, Gannon V (2018) Multi-year persistence of verotoxigenic Escherichia coli (VTEC) in a closed Canadian beef herd: a cohort study. Front Microbiol 9:2040. https://doi.org/10.3389/fmicb.2018.02040

    Article  PubMed  PubMed Central  Google Scholar 

  73. Delannoy S, Beutin L, Mariani-Kurkdjian P, Fleiss A, Bonacorsi S, Fach P (2017) The Escherichia coli serogroup O1 and O2 lipopolysaccharides are encoded by multiple O-antigen gene clusters. Front Cell Infect Microbiol 7:1–30. https://doi.org/10.3389/fcimb.2017.00030

    Article  CAS  Google Scholar 

  74. Bürk C, Dietrich R, Açar G, Moravek M, Bülte M, Märtlbauer E (2003) Identification and characterization of a new variant of Shiga toxin 1 in Escherichia coli ONT:H19 of bovine origin. J Clin Microbiol 41(5):2106–2112. https://doi.org/10.1128/JCM.41.5.2106-2112.2003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Bai X, Zhang J, Ambikan A, Jernberg C, Ehricht R, Scheutz F, Xiong Y, Matussek A (2019) Molecular characterization and comparative genomics of clinical hybrid Shiga toxin-producing and enterotoxigenic Escherichia coli (STEC/ETEC) strains in Sweden. Sci Rep 9(1):5619. https://doi.org/10.1038/s41598-019-42122-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Badouei MA, Morabito S, Najafifar A, Mazandarani E (2016) Molecular characterization of enterohemorrhagic Escherichia coli hemolysin gene (EHEC-hlyA)-harboring isolates from cattle reveals a diverse origin and hybrid diarrheagenic strains. Infect Genet Evol 39:342–348. https://doi.org/10.1016/j.meegid.2016.02.002

    Article  CAS  Google Scholar 

  77. Johura F, Parveen R, Islam A, Sadique A, Rahim N, Monira S, Khan AR, Ahsan S, Ohnishi M, Watanabe H, Chakraborty S, George CM, Cravioto A, Navarro A, Hasan B, Alam M (2016) Occurrence of hybrid Escherichia coli strains carrying Shiga toxin and heat-stable toxin in livestock of Bangladesh. Front Public Health 4:287. https://doi.org/10.3389/fpubh.2016.00287

    Article  PubMed  Google Scholar 

  78. Akiyama Y, Futai H, Saito E, Ogita K, Sakae H, Fukunaga M, Tsuji H, Chikahira M, Iguchi A (2017) Shiga toxin subtypes and virulence genes in Escherichia coli isolated from cattle. J Infect Dis 70(2):181–185. https://doi.org/10.7883/yoken.JJID.2016.100

    Article  CAS  Google Scholar 

  79. Cheasty T, Rowe B (1983) Antigenic relationships between the enteroinvasive Escherichia coli O antigens O28ac, O112ac, O124, O136, O143, O144, O152, and O164 and Shigella O antigens. J Clin Microbiol 17(4):681–684. https://doi.org/10.1128/jcm.17.4.681-684.1983

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Beutin L, Gleier K, Kontny I, Echeverria P, Scheutz F (1997) Origin and characteristics of enteroinvasive strains of Escherichia coli (EIEC) isolated in Germany. Epidemiol Infect 118:199–205. https://doi.org/10.1017/s0950268897007413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. da Silva LC, de Mello Santos AC, Silva RM (2017) Uropathogenic Escherichia coli pathogenicity islands and other ExPEC virulence genes may contribute to the genome variability of enteroinvasive E. coli. BMC Microbiology 17(1):68. https://doi.org/10.1186/s12866-017-0979-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Beutin L, Montenegro MA, Orskov I, Orskov F, Prada J, Zimmermann S, Stephan R (1989) Close association of verotoxin (Shiga-like toxin) production with enterohemolysin production in strains of Escherichia coli. J Clin Microbiol 27(11):2559–2564. https://doi.org/10.1128/jcm.27.11.2559-2564.1989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Vieira MA, Andrade JR, Trabulsi LR, Rosa AC, Dias AM, Ramos SR, Frankel G, Gomes TAT (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(5):762–72. https://doi.org/10.1086/318821

    Article  CAS  PubMed  Google Scholar 

  84. Cookson AL, Bennett J, Thomson-Carter F, Attwood GT (2007) Molecular subtyping and genetic analysis of the Enterohemolysin Gene (ehxA) from Shiga toxin-producing Escherichia coli and atypical enteropathogenic E. coli. Appl Environ Microbiol 73(20):6360–9. https://doi.org/10.1128/AEM.00316-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Zhang S, Yang G, Huang Y, Zhang J, Cui L, Wu Q (2018) Prevalence and characterization of atypical enteropathogenic Escherichia coli isolated from retail foods in China. J Food Prot 81(11):1761–1767. https://doi.org/10.4315/0362-028X.JFP-18-188

    Article  CAS  PubMed  Google Scholar 

  86. Colello R, Velez MV, Gonzáleza J, Montero DA, Bustamante AV, Del Canto F, Etcheverría AI, Vidal R, Padola NL (2018) First report of the distribution of locus of adhesion and autoaggregation (LAA) pathogenicity island in LEE-negative Shiga toxin-producing Escherichia coli isolates from Argentina. Microb Pathog 123:259–263. https://doi.org/10.1016/j.micpath.2018.07.011

    Article  CAS  PubMed  Google Scholar 

  87. Montero DA, Del Canto F, Velasco J, Colello R, Padola NL, Salazar JC, San Martin C, Oñate A, Blanco J, Rasko DA, Contreras C, Puente JL, Scheutz F, Franz E, Vidal RM (2019) Cumulative acquisition of pathogenicity islands has shaped virulence potential and contributed to the emergence of LEE-negative Shiga toxin-producing Escherichia coli strains. Emerg Microbes Infect 8(1):486–502. https://doi.org/10.1080/22221751.2019.1595985

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Mosquito S, Ruiz J, Pons MJ, Durand D, Barletta F, Ochoa TJ (2012) Molecular mechanisms of antibiotic resistance in diarrhoeagenic Escherichia coli isolated from children. Int J Antimicrob Agents 40:544–554. https://doi.org/10.1016/j.ijantimicag.2012.07.021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Gonzales L, Joffre E, Rivera R, Sjöling Å, Svennerholm AM, Iñiguez V (2013) Prevalence, seasonality and severity of disease caused by pathogenic Escherichia coli in children with diarrhoea in Bolivia. J Med Microbiol 62:1697–1706. https://doi.org/10.1099/jmm.0.060798-0

    Article  CAS  PubMed  Google Scholar 

  90. Pantozzi FL, Moredo FA, Vigo GB, Giacoboni GI (2010) Antimicrobial resistance in indicator and zoonotic bacteria isolated from domestic animals in Argentina. Revista Argentina de Microbiología 42(1):49–52. https://doi.org/10.1590/S0325-75412010000100011

    Article  CAS  PubMed  Google Scholar 

  91. Boletín Informativo Resistencia Antimicrobiana (2019) Retrieved from: folletoRAM2019Final.pdf (conicet.gov.ar)

  92. Ribeiro LF, Barbosa MMC, Pinto FR, Lavezzo LF, Rossi GAM, Almeida HMS, Amaral LA (2019) Diarrheagenic Escherichia coli in raw milk, wáter and cattle feces in non-technified dairy farms. Ciência Animal Brasileira 20:e-47449. https://doi.org/10.1590/1089-6891v20e-47449

    Article  Google Scholar 

  93. Calderon Toledo C, Arvidsson I, Karpman D (2011) Cross-reactive protection against enterohemorrhagic Escherichia coli infection by enteropathogenic E. coli in a mouse model. Infect Immun 79(6):2224–33. https://doi.org/10.1128/IAI.01024-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This study was performed at the Universidad de Buenos Aires, Facultad de Ciencias Veterinarias. The authors would like to thank the University and the Microbiology department for the assistance during the whole period of work.

Funding

This research was funded by a magister fellowship by Universidad de Buenos Aires, UBACyT 20020190100320, and PICT 2017–3360.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Maria Paz Bonino.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's note

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

Responsible Editor: Waldir P. Elias

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 23 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bonino, M.P., Crivelli, X.B., Petrina, J.F. et al. Detection and analysis of Shiga toxin producing and enteropathogenic Escherichia coli in cattle from Tierra del Fuego, Argentina. Braz J Microbiol 54, 1257–1266 (2023). https://doi.org/10.1007/s42770-023-00958-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42770-023-00958-8

Keywords

Navigation