1887

Abstract

Enteropathogenic (EPEC) are important agents of diarrhoea in industrialized as well as developing countries, such as Brazil. The hallmark of EPEC pathogenesis is the establishment of attaching and effacing lesions in enterocytes, in which pedestal-like structures are formed underneath adherent bacteria. EPEC are divided into two subgroups, typical (tEPEC) and atypical (aEPEC), based on the presence of the EPEC adherence factor plasmid in tEPEC and its absence in aEPEC. This study was designed to characterize 82 aEPEC isolates obtained from stool samples of diarrhoeic patients during 2012 and 2013 in Brazil. The majority of the aEPEC were assigned to the phylo-group B1 (48.8 %), and intimin subtypes θ (20.7 %), β1 (9.7 %) and λ (9.7 %) were the most prevalent among the isolates. The and genes were concomitantly detected in 32.9 % of the isolates, demonstrating the occurrence of the pathogenicity island O122 among them. The O157-plasmid genes ( and/or ) were detected in 7.3 % of the isolates, suggesting that some aEPEC could be derived from Shiga-toxin-producing that lost the genes while trafficking in the host. PFGE of 14 aEPEC of serotypes O2 : H16, O33 : H34, O39 : H9, O108 : H and ONT : H19 isolated from five distinct outbreaks showed serotype-specific PFGE clusters, indicating a high degree of similarity among the isolates from the same event, thus highlighting these serotypes as potential aetiologic agents of diarrhoeal outbreaks in Brazil.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.000313
2016-09-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/jmm/65/9/998.html?itemId=/content/journal/jmm/10.1099/jmm.0.000313&mimeType=html&fmt=ahah

References

  1. Abe C. M., Trabulsi L. R., Blanco J., Blanco M., Dahbi G., Blanco J. E., Mora A., Franzolin M. R., Taddei C. R. et al. 2009; Virulence features of atypical enteropathogenic Escherichia coli identified by the eae(+) EAF-negative stx(−) genetic profile. Diagn Microbiol Infect Dis 64:357–365 [View Article][PubMed]
    [Google Scholar]
  2. Afset J. E., Bevanger L., Romundstad P., Bergh K. 2004; Association of atypical enteropathogenic Escherichia coli (EPEC) with prolonged diarrhoea. J Med Microbiol 53:1137–1144 [View Article][PubMed]
    [Google Scholar]
  3. Afset J. E., 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 [View Article][PubMed]
    [Google Scholar]
  4. Afset J. E., Anderssen E., Bruant G., Harel J., Wieler L., Bergh K. 2008; Phylogenetic backgrounds and virulence profiles of atypical enteropathogenic Escherichia coli strains from a case-control study using multilocus sequence typing and DNA microarray analysis. J Clin Microbiol 46:2280–2290 [View Article][PubMed]
    [Google Scholar]
  5. Arbeloa A., Blanco M., Moreira F. C., Bulgin R., López C., Dahbi G., Blanco J. E., Mora A., Alonso M. P. et al. 2009; Distribution of espM and espT among enteropathogenic and enterohaemorrhagic Escherichia coli. J Med Microbiol 58:988–995 [View Article][PubMed]
    [Google Scholar]
  6. Bando S. Y., Andrade F. B., Guth B. E., Elias W. P., Moreira-Filho C. A., Pestana de Castro A. F. 2009; Atypical enteropathogenic Escherichia coli genomic background allows the acquisition of non-EPEC virulence factors. FEMS Microbiol Lett 299:22–30 [View Article][PubMed]
    [Google Scholar]
  7. Batisson I., Guimond M. P., Girard F., An H., Zhu C., Oswald E., Fairbrother J. M., Jacques M., Harel J. 2003; Characterization of the novel factor paa involved in the early steps of the adhesion mechanism of attaching and effacing Escherichia coli. Infect Immun 71:4516–4525 [View Article][PubMed]
    [Google Scholar]
  8. Bielaszewska M., Middendorf B., Köck R., Friedrich A. W., Fruth A., Karch H., Schmidt M. A., Mellmann A. 2008; Shiga toxin-negative attaching and effacing Escherichia coli: distinct clinical associations with bacterial phylogeny and virulence traits and inferred in-host pathogen evolution. Clin Infect Dis 47:208–217 [View Article][PubMed]
    [Google Scholar]
  9. Blanco M., Blanco J. E., Dahbi G., Mora A., Alonso M. P., Varela G., Gadea M. P., Schelotto F., González E. A., 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 55:1165–1174 [View Article][PubMed]
    [Google Scholar]
  10. Boisen N., Ruiz-Perez F., Scheutz F., Krogfelt K. A., Nataro J. P. 2009; Short report: high prevalence of serine protease autotransporter cytotoxins. among strains of enteroaggregative Escherichia coli. Am J Trop Med Hyg 80:294–301
    [Google Scholar]
  11. Buss C., Müller D., Rüter C., Heusipp G., Schmidt M. A. 2009; Identification and characterization of Ibe, a novel type III effector protein of A/E pathogens targeting human IQGAP1. Cell Microbiol 11:661–677 [View Article][PubMed]
    [Google Scholar]
  12. Clermont O., Bonacorsi S., Bingen E. 2000; Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 66:4555–4558 [View Article][PubMed]
    [Google Scholar]
  13. Clermont O., Christenson J. K., Denamur E., Gordon D. M. 2013; The Clermont Escherichia coli phylo-typing method revisited: improvement of specificity and detection of new phylo-groups. Environ Microbiol Rep 5:58–65 [View Article][PubMed]
    [Google Scholar]
  14. Clermont O., Gordon D., Denamur E. 2015; Guide to the various phylogenetic classification schemes for Escherichia coli and the correspondence among schemes. Microbiology 161:980–988 [View Article][PubMed]
    [Google Scholar]
  15. Cohen M. B., Nataro J. P., Bernstein D. I., Hawkins J., Roberts N., Staat M. A. 2005; Prevalence of diarrheagenic Escherichia coli in acute childhood enteritis: a prospective controlled study. J Pediatr 146:54–61 [View Article][PubMed]
    [Google Scholar]
  16. Contreras C. A., Ochoa T. J., Lacher D. W., DebRoy C., Navarro A., Talledo M., Donnenberg M. S., Ecker L., Gil A. I. et al. 2010; Allelic variability of critical virulence genes (eae, bfpA and perA) in typical and atypical enteropathogenic Escherichia coli in Peruvian children. J Med Microbiol 59:25–31 [View Article][PubMed]
    [Google Scholar]
  17. Dias R. C., Dos Santos B. C., Dos Santos L. F., Vieira M. A., Yamatogi R. S., Mondelli A. L., Sadatsune T., Sforcin J. M., Gomes T. A., Hernandes R. T. 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 124:299–308 [View Article][PubMed]
    [Google Scholar]
  18. Donnenberg M. S., Girón J. A., Nataro J. P., Kaper J. B. 1992; A plasmid-encoded type IV fimbrial gene of enteropathogenic Escherichia coli associated with localized adherence. Mol Microbiol 6:3427–3437 [View Article][PubMed]
    [Google Scholar]
  19. Foster M. A., Iqbal J., Zhang C., McHenry R., Cleveland B. E., Romero-Herazo Y., Fonnesbeck C., Payne D. C., Chappell J. D. et al. 2015; Enteropathogenic and enteroaggregative E. coli in stools of children with acute gastroenteritis in Davidson County, Tennessee. Diagn Microbiol Infect Dis 83:319–324 [View Article][PubMed]
    [Google Scholar]
  20. Fratamico P. M., Yan X., Caprioli A., Esposito G., Needleman D. S., Pepe T., Tozzoli R., Cortesi M. L., Morabito S. 2011; The complete DNA sequence and analysis of the virulence plasmid and of five additional plasmids carried by Shiga toxin-producing Escherichia coli O26:H11 strain H30. Int J Med Microbiol 301:192–203 [View Article][PubMed]
    [Google Scholar]
  21. Gomes T. A., Hernandes R. T., Torres A. G., Salvador F. A., Guth B. E., Vaz T. M., Irino K., Silva R. M., Vieira M. A. 2011; Adhesin-encoding genes from Shiga toxin-producing Escherichia coli are more prevalent in atypical than in typical enteropathogenic E. coli. J Clin Microbiol 49:3334–3337 [View Article][PubMed]
    [Google Scholar]
  22. Gomes T. A. T., Irino K., Girão D. M., Girão V. B., Guth B. E., Vaz T. M., Moreira F. C., Chinarelli S. H., Vieira M. A. 2004; Emerging enteropathogenic Escherichia coli strains. Emerg Infect Dis 10:1851–1855 [View Article][PubMed]
    [Google Scholar]
  23. Hao R., Qiu S., Wang Y., Yang G., Su W., Song L., Zhang J., Chen J., Jia L. et al. 2012; Quinolone-resistant Escherichia coli O127a:K63 serotype with an extended-spectrum-beta-lactamase phenotype from a food poisoning outbreak in China. J Clin Microbiol 50:2450–2451 [View Article][PubMed]
    [Google Scholar]
  24. Hazen T. H., Sahl J. W., Fraser C. M., Donnenberg M. S., Scheutz F., Rasko D. A. 2013; Refining the pathovar paradigm via phylogenomics of the attaching and effacing Escherichia coli. Proc Natl Acad Sci U S A 110:12810–12815 [View Article][PubMed]
    [Google Scholar]
  25. Hernandes R. T., Elias W. P., Vieira M. A., Gomes T. A. T. 2009; An overview of atypical enteropathogenic Escherichia coli. FEMS Microbiol Lett 297:137–149 [View Article][PubMed]
    [Google Scholar]
  26. Hernandes R. T., Velsko I., Sampaio S. C., Elias W. P., Robins-Browne R. M., Gomes T. A., Girón J. A. 2011; Fimbrial adhesins produced by atypical enteropathogenic Escherichia coli strains. Appl Environ Microbiol 77:8391–8399 [View Article][PubMed]
    [Google Scholar]
  27. Hunter S. B., Vauterin P., Lambert-Fair M. A., Van Duyne M. S., Kubota K., Graves L., Wrigley D., Barrett T., Ribot E. 2005; Establishment of a universal size standard strain for use with the PulseNet standardized pulsed-field gel electrophoresis protocols: converting the national databases to the new size standard. J Clin Microbiol 43:1045–1050 [View Article][PubMed]
    [Google Scholar]
  28. Ingle D. J., Tauschek M., Edwards D. J., Hocking D. M., Pickard D. J., Azzopardi K., Amarasena T., Bennett-Wood V., Pearson J. S. et al. 2016; Evolution of atypical enteropathogenic E. coli by repeated acquisition of LEE pathogenicity island variants. Nat Microbiol 1:15010 [View Article]
    [Google Scholar]
  29. Jerse A. E., Yu J., Tall B. D., 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 U S A 87:7839–7843 [View Article][PubMed]
    [Google Scholar]
  30. Kaper J. B., Nataro J. P., Mobley H. L. 2004; Pathogenic Escherichia coli. Nat Rev Microbiol 2:123–140 [View Article][PubMed]
    [Google Scholar]
  31. Kenny B., DeVinney R., Stein M., Reinscheid D. J., Frey E. A., Finlay B. B. 1997; Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell 91:511–520 [View Article][PubMed]
    [Google Scholar]
  32. Le Bouguenec C., Archambaud M., Labigne A. 1992; Rapid and specific detection of the pap, afa, and sfa adhesin-encoding operons in uropathogenic Escherichia coli strains by polymerase chain reaction. J Clin Microbiol 30:1189–1193[PubMed]
    [Google Scholar]
  33. Makino K., Ishii K., Yasunaga T., Hattori M., Yokoyama K., Yutsudo C. H., Kubota Y., Yamaichi Y., Iida T. et al. 1998; Complete nucleotide sequences of 93-kb and 3.3-kb plasmids of an enterohemorrhagic Escherichia coli O157:H7 derived from Sakai outbreak. DNA Res 5:1–9 [View Article][PubMed]
    [Google Scholar]
  34. McDaniel T. K., Jarvis K. G., Donnenberg M. S., Kaper J. B. 1995; A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. Proc Natl Acad Sci U S A 92:1664–1668 [View Article][PubMed]
    [Google Scholar]
  35. Mora A., Blanco M., Yamamoto D., Dahbi G., Blanco J. E., López C., Alonso M. P., Vieira M. A., Hernandes R. T. et al. 2009; HeLa-cell adherence patterns and actin aggregation of enteropathogenic Escherichia coli (EPEC) and Shiga-toxin-producing E. coli (STEC) strains carrying different eae and tir alleles. Int Microbiol 12:243–251[PubMed]
    [Google Scholar]
  36. Moreira F. C., Vieira M. A., Ferreira A. J., Girão D. M., Vaz T. M., Rosa A. C., Knobl T., Irino K., Freymüller E., Gomes T. A. 2008; Escherichia coli strains of serotype O51:H40 comprise typical and atypical enteropathogenic E. coli strains and are potentially diarrheagenic. J Clin Microbiol 46:1462–1465 [View Article][PubMed]
    [Google Scholar]
  37. Müller D., Benz I., Liebchen A., Gallitz I., Karch H., Schmidt M. A. 2009; Comparative analysis of the locus of enterocyte effacement and its flanking regions. Infect Immun 77:3501–3513 [View Article][PubMed]
    [Google Scholar]
  38. Nataro J. P., Kaper J. B. 1998; Diarrheagenic Escherichia coli. Clin Microbiol Rev 11:142–201[PubMed]
    [Google Scholar]
  39. Nguyen R. N., Taylor L. S., Tauschek M., Robins-Browne R. M. 2006; Atypical enteropathogenic Escherichia coli infection and prolonged diarrhea in children. Emerg Infect Dis 12:597–603 [View Article][PubMed]
    [Google Scholar]
  40. Nicholls L., Grant T. H., Robins-Browne R. M. 2000; Identification of a novel genetic locus that is required for in Vitro adhesion of a clinical isolate of enterohaemorrhagic Escherichia coli to epithelial cells. Mol Microbiol 35:275–288 [View Article][PubMed]
    [Google Scholar]
  41. Nunes E. B., Saridakis H. O., Irino K., Pelayo J. S. 2003; Genotypic and phenotypic characterization of attaching and effacing Escherichia coli (AEEC) isolated from children with and without diarrhoea in Londrina, Brazil. J Med Microbiol 52:499–504 [View Article][PubMed]
    [Google Scholar]
  42. Oswald E., Schmidt H., Morabito S., Karch H., Marchès O., Caprioli A. 2000; Typing of intimin genes in human and animal enterohemorrhagic and enteropathogenic Escherichia coli: characterization of a new intimin variant. Infect Immun 68:64–71 [View Article][PubMed]
    [Google Scholar]
  43. Paton A. W., Paton J. C. 1998; Detection and characterization of Shiga toxigenic Escherichia coli by using multiplex PCR assays for stx1, stx2, eaeA, enterohemorrhagic E. coli hlyA, rfbO111, and rfbO157. J Clin Microbiol 36:598–602[PubMed]
    [Google Scholar]
  44. Paton A. W., Paton J. C. 2002; Direct detection and characterization of Shiga toxigenic Escherichia coli by multiplex PCR for stx1, stx2, eae, ehxA, and saa. J Clin Microbiol 40:271–274 [View Article][PubMed]
    [Google Scholar]
  45. Paton A. W., Srimanote P., Talbot U. M., Wang H., Paton J. C. 2004; A new family of potent AB(5) cytotoxins produced by Shiga toxigenic Escherichia coli. J Exp Med 200:35–46 [View Article][PubMed]
    [Google Scholar]
  46. Peresi J. T. M., Almeida I. A. Z. C., Vaz T. M. I., Hernandes R. T., Teixeira I. S. C., Silva S. I. L., Graciano R. A. S., Pinheiro S. R., Dos Santos L. F. 2016; Search for diarrheagenic Escherichia coli in raw kibbe samples reveals the presence of Shiga toxin-producing strains. Food Control 63:165–170 [View Article]
    [Google Scholar]
  47. Robins-Browne R. M. 1987; Traditional enteropathogenic Escherichia coli of infantile diarrhea. Rev Infect Dis 9:28–53 [View Article][PubMed]
    [Google Scholar]
  48. Salvador F. A., Hernandes R. T., Vieira M. A., Rockstroh A. C., Gomes T. A. 2014; Distribution of non-LEE-encoded type 3 secretion system dependent effectors in enteropathogenic Escherichia coli. Braz J Microbiol 45:851–855 [View Article][PubMed]
    [Google Scholar]
  49. Scaletsky I. C., Aranda K. R., Souza T. B., Silva N. P., Morais M. B. 2009; Evidence of pathogenic subgroups among atypical enteropathogenic Escherichia coli strains. J Clin Microbiol 47:3756–3759 [View Article][PubMed]
    [Google Scholar]
  50. Szalo I. M., Goffaux F., Pirson V., Piérard D., Ball H., Mainil J. 2002; Presence in bovine enteropathogenic (EPEC) and enterohaemorrhagic (EHEC) Escherichia coli of genes encoding for putative adhesins of human EHEC strains. Res Microbiol 153:653–658 [View Article][PubMed]
    [Google Scholar]
  51. Tennant S. M., Tauschek M., Azzopardi K., Bigham A., Bennett-Wood V., Hartland E. L., Qi W., Whittam T. S., Robins-Browne R. M. 2009; Characterisation of atypical enteropathogenic E. coli strains of clinical origin. BMC Microbiol 9:117 [View Article][PubMed]
    [Google Scholar]
  52. Trabulsi L. R., Keller R., Gomes T. A. T. 2002; Typical and atypical enteropathogenic Escherichia coli. Emerg Infect Dis 8:508–513 [View Article][PubMed]
    [Google Scholar]
  53. Tóth I., Hérault F., Beutin L., Oswald E. 2003; Production of cytolethal distending toxins by pathogenic Escherichia coli strains isolated from human and animal sources: establishment of the existence of a new cdt variant (Type IV). J Clin Microbiol 41:4285–4291 [View Article][PubMed]
    [Google Scholar]
  54. Vieira M. A., Andrade J. R., Trabulsi L. R., Rosa A. C., Dias A. M., Ramos S. R., Frankel G., Gomes T. A. T. 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 [View Article][PubMed]
    [Google Scholar]
  55. Vieira M. A. M., Salvador F. A., Silva R. M., Irino K., Vaz T. M., Rockstroh A. C., Guth B. E., Gomes T. A. T. 2010; Prevalence and characteristics of the O122 pathogenicity island in typical and atypical enteropathogenic Escherichia coli strains. J Clin Microbiol 48:1452–1455 [View Article][PubMed]
    [Google Scholar]
  56. Viljanen M. K., Peltola T., Junnila S. Y., Olkkonen L., Järvinen H., Kuistila M., Huovinen P. 1990; Outbreak of diarrhoea due to Escherichia coli O111:B4 in schoolchildren and adults: association of Vi antigen-like reactivity. Lancet 336:831–834 [View Article][PubMed]
    [Google Scholar]
  57. Vossenkämper A., Macdonald T. T., Marchès O. 2011; Always one step ahead: how pathogenic bacteria use the type III secretion system to manipulate the intestinal mucosal immune system. J Inflamm (LOND) 3:8–11
    [Google Scholar]
  58. Wong A. R., Pearson J. S., Bright M. D., Munera D., Robinson K. S., Lee S. F., Frankel G., Hartland E. L. 2011; Enteropathogenic and enterohaemorrhagic Escherichia coli: even more subversive elements. Mol Microbiol 80:1420–1438 [View Article][PubMed]
    [Google Scholar]
  59. Xu Y., Bai X., Zhao A., Zhang W., Ba P., Liu K., Jin Y., Wang H., Guo Q. et al. 2016; Genetic diversity of intimin gene of atypical enteropathogenic Escherichia coli isolated from human, animals and raw meats in China. PLoS One 11:e0152571 [View Article][PubMed]
    [Google Scholar]
  60. Yamamoto T., Echeverria P. 1996; Detection of the enteroaggregative Escherichia coli heat-stable enterotoxin 1 gene sequences in enterotoxigenic E. coli strains pathogenic for humans. Infect Immun 64:1441–1445[PubMed]
    [Google Scholar]
  61. Yan X., Fratamico P. M., Needleman D. S., Bayles D. O. 2012; DNA sequence and analysis of a 90.1-kb plasmid in Shiga toxin-producing Escherichia coli (STEC) O145:NM 83-75. Plasmid 68:25–32 [View Article][PubMed]
    [Google Scholar]
  62. Yatsuyanagi J., Saito S., Miyajima Y., Amano K., Enomoto K. 2003; Characterization of atypical enteropathogenic Escherichia coli strains harboring the astA gene that were associated with a waterborne outbreak of diarrhea in Japan. J Clin Microbiol 41:2033–2039 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.000313
Loading
/content/journal/jmm/10.1099/jmm.0.000313
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error