Volume 97, Issue 5
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645



is an important cause of Gram-negative bacteremia. The aim of this study was to characterize at the molecular and phenotypic levels strains belonging to different diarrheagenic pathotypes [diarrheagenic (DEC)] isolated from bacteremia in children younger than 5 years of age. Seventy bacteremia strains were collected in a prospective study in 12 hospitals in Lima, Peru. The presence of virulence genes associated with DEC [enterotoxigenic ( and ), enteropathogenic (), shiga toxin-producing (and ), enteroinvasive (), enteroaggregative (), and diffusely adherent ()] was determined by multiplex real-time polymerase chain reaction (PCR). Those positive strains were further analyzed for 18 additional virulence factors encoding genes and others phenotypic features. Virulence genes associated with DEC were identified in seven bacteremic children (10%), including: one -positive [enteroaggregative (EAEC)], one -positive [enteropathogenic (EPEC)], one -positive [enterotoxigenic (ETEC)], one -positive [diffusely adherent (DAEC)], and three strain positive for and (EAEC/DAEC) at the same time. All strains, except EPEC, had the Ag43 adhesin, and all, except ETEC had the siderophore gene . The phylogenetic profile of these strains was variable, two (B2), two (D), two (A), and one (B1) strain. These isolates were susceptible to all tested antibacterial agents except to ampicillin and gentamicin. The three EAEC/DAEC strains showed biofilm formation and aggregative adhesion and had the same repetitive extragenic palindromic–PCR patterns. These findings suggest that some DEC strains, especially agg-R and daa-D positive, might cause bacteremia in children.


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  1. Russo T, Johnson J, , 2000. Proposal for a new inclusive designation for extraintestinal pathogenic isolates of Escherichia coli: ExPEC. J Infect Dis 181: 17531754.[Crossref] [Google Scholar]
  2. Kaper JB, Nataro JP, Mobley HLT, , 2004. Pathogenic Escherichia coli . Natl Rev 2: 123140. [Google Scholar]
  3. Aurass P, Prager R, Flieger A, , 2011. EHEC/EAEC O104:H4 strain linked with the 2011 German outbreak of haemolytic uremic syndrome enters into the viable but non-culturable state in response to various stresses and resuscitates upon stress relief. Environ Microbiol 13: 31393148.[Crossref] [Google Scholar]
  4. Clermont O, Bonacorsi S, Bingen E, , 2000. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 66: 45554558.[Crossref] [Google Scholar]
  5. García C, 2012. Antimicrobial drug resistance in Peru. Emerg Infect Dis 18: 520521.[Crossref] [Google Scholar]
  6. Abe CM, 2008. Uropathogenic Escherichia coli (UPEC) strains may carry virulence properties of diarrhoeagenic E. coli . FEMS Immunol Med Microbiol 52: 397406.[Crossref] [Google Scholar]
  7. Thaver D, Zaidi AK, , 2009. Burden of neonatal infections in developing countries: a review of evidence from community-based studies. Pediatr Infect Dis J 28 (Suppl): S3S9.[Crossref] [Google Scholar]
  8. Barletta F, Ochoa TJ, Ecker L, Gil AI, Lanata CF, Cleary TG, , 2009. Validation of five-colony pool analysis using multiplex real-time PCR for detection of diarrheagenic Escherichia coli . J Clin Microbiol 47: 19151917.[Crossref] [Google Scholar]
  9. Durand D, Contreras C, Mosquito S, Ruíz J, Cleary TG, Ochoa TJ, , 2016. pic gene of enteroaggregative Escherichia coli (EAEC) and its association with diarrhea in Peruvian children. Pathog Dis 74: ftw054.[Crossref] [Google Scholar]
  10. Scaletsky I, Silva M, Trabulsi L, , 1984. Distinctive patterns of adherence of enteropathogenic Escherichia coli to HeLa cells. Infect Immun 45: 534536. [Google Scholar]
  11. Wakimoto N, Nishi J, Sheikh J, Nataro J, Sarantuya J, Iwashita M, Manago K, Tokuda K, Yoshinaga M, Kawano Y, , 2004. Quantitative biofilm assay using microtiter plate to screen for enteroaggregative Escherichia coli . Am J Trop Med Hyg 71: 687690. [Google Scholar]
  12. Niu C, Gilbert ES, , 2004. Colorimetric method for identifying plant essential oil components that affect biofilm formation and structure. Appl Environ Microbiol 70: 69516956.[Crossref] [Google Scholar]
  13. Clinical and Laboratory Standards Institute, 2008. Performance Standards for Antimicrobial Susceptibility Testing; 18th Informational Supplement. M100-S18. Wayne, PA: Clinical and Laboratory Standards Institute.
  14. Perez-Moreno MO, Pico-Plana E, de Toro M, Grande-Armas J, Quiles-Fortuny V, Pons MJ, Gomes C, Saenz Y, Torres C, Ruiz J, , 2013. β-Lactamases, transferable quinolone resistance determinants, and class 1 integron-mediated antimicrobial resistance in human clinical Salmonella enterica isolates of non-Typhimurium serotypes. Int J Med Microbiol 303: 2531.[Crossref] [Google Scholar]
  15. Gallardo F, Ruiz J, Marco F, Towner KJ, Vila J, , 1999. Increase in incidence of resistance to ampicillin, chloramphenicol and trimethoprim in clinical isolates of Salmonella serotype Typhimurium with investigation of molecular epidemiology and mechanisms of resistance. J Med Microbiol 48: 367374.[Crossref] [Google Scholar]
  16. Herzog K, Engeler Dusel J, Hugentobler M, Beutin L, Sägesser G, Stephan R, Hächler H, Nüesch-Inderbinen M, , 2014. Diarrheagenic enteroaggregative Escherichia coli causing urinary tract infection and bacteremia leading to sepsis. Infection 42: 441444.[Crossref] [Google Scholar]
  17. Brauner A, Katouli M, Östenson CG, , 1995. P-fimbriation and haemolysin production are the most important virulence factors in diabetic patients with Escherichia coli bacteraemia: a multivariate statistical analysis of seven bacterial virulence factors. J Infect 31: 2731.[Crossref] [Google Scholar]
  18. Moreno E, Planells I, Prats G, Planes AM, Moreno G, Andreu A, , 2005. Comparative study of Escherichia coli virulence determinants in strains causing urinary tract bacteremia versus strains causing pyelonephritis and other sources of bacteremia. Diagn Microbiol Infect Dis 53: 9399.[Crossref] [Google Scholar]
  19. Clements A, Young JC, Constantinou N, Frankel G, , 2012. Infection strategies of enteric pathogenic Escherichia coli . Gut Microbes 3: 7187.[Crossref] [Google Scholar]
  20. Tobias J, Vutukuru SR, , 2012. Simple and rapid multiplex PCR for identification of the main human diarrheagenic Escherichia coli . Microbiol Res 167: 564570.[Crossref] [Google Scholar]
  21. Jenkins C, van Ijperen C, Dudley EG, Chart H, Willshaw GA, Cheasty T, Smith HR, Nataro JP, , 2005. Use of a microarray to assess the distribution of plasmid and chromosomal virulence genes in strains of enteroaggregative Escherichia coli . FEMS Microbiol Lett 253: 119124.[Crossref] [Google Scholar]
  22. Hasman H, Chakraborty T, Klemm P, , 1999. Antigen-43-mediated autoaggregation of Escherichia coli is blocked by fimbriation. J Bacteriol 181: 48344841. [Google Scholar]
  23. Bernier C, Gounon P, Le Bouguenec C, , 2002. Identification of an aggregative adhesion fimbria (AAF) type III-encoding operon in enteroaggregative Escherichia coli as a sensitive probe for detecting the AAF-encoding operon family. Infect Immun 70: 43024311.[Crossref] [Google Scholar]
  24. Czeczulin JR, Whittam TS, Henderson IR, Navarro-Garcia F, Nataro JP, , 1999. Phylogenetic analysis of enteroaggregative and diffusely adherent Escherichia coli . Infect Immun 67: 26922699. [Google Scholar]
  25. Froehlich B, Parkhill J, Sanders M, Quail MA, Scott JR, , 2005. The pCoo plasmid of enterotoxigenic Escherichia coli is a mosaic cointegrate. J Bacteriol 187: 65096516.[Crossref] [Google Scholar]
  26. Telli M, Guiral E, Martínez JA, Almela M, Bosch J, Vila J, Soto SM, , 2010. Prevalence of enterotoxins among Escherichia coli isolates causing bacteraemia. FEMS Microbiol Lett 306: 117121.[Crossref] [Google Scholar]
  27. Pelludat C, Hogardt M, Heesemann J, , 2002. Transfer of the core region genes of the Yersinia enterocolitica WA-C serotype O: 8 high-pathogenicity island to Y. enterocolitica MRS40, a strain with low levels of pathogenicity, confers a yersiniabactin biosynthesis phenotype and enhanced mouse virulence. Infect Immun 70: 18321841.[Crossref] [Google Scholar]
  28. Schubert S, Rakin A, Karch H, Carniel E, Heesemann J, , 1998. Prevalence of the “high-pathogenicity island” of Yersinia species among Escherichia coli strains that are pathogenic to humans. Infect Immun 66: 480485. [Google Scholar]
  29. Liévin-Le Moal V, Comenge Y, Ruby V, Amsellem R, Nicolas V, Servin AL, , 2011. Secreted autotransporter toxin (Sat) triggers autophagy in epithelial cells that relies on cell detachment. Cell Microbiol 13: 9921013.[Crossref] [Google Scholar]
  30. Taddei CR, Moreno AC, Fernandes Filho A, Montemor LP, Martinez MB, , 2003. Prevalence of secreted autotransporter toxin gene among diffusely adhering Escherichia coli isolated from stools of children. FEMS Microbiol Lett 227: 249253.[Crossref] [Google Scholar]
  31. Mendez-Arancibia E, Vargas M, Soto S, Ruiz J, Kahigwa E, Schellenberg D, Urassa H, Gascón J, Vila J, , 2008. Prevalence of different virulence factors and biofilm production in enteroaggregative Escherichia coli isolates causing diarrhea in children in Ifakara (Tanzania). Am J Trop Med Hyg 78: 985989. [Google Scholar]
  32. Taddei CR, Fasano A, Ferreira AJ, Trabulsi LR, Martinez MB, , 2005. Secreted autotransporter toxin produced by a diffusely adhering Escherichia coli strain causes intestinal damage in animal model assays. FEMS Microbiol Lett 250: 263269.[Crossref] [Google Scholar]
  33. Hacker J, Blum-Oehler G, Mühldorfer I, Tschäpe H, , 1997. Pathogenicity islands of virulent bacteria: structure, function and impact on microbial evolution. Mol Microbiol 23: 10891097.[Crossref] [Google Scholar]
  34. Karch H, Denamur E, Dobrindt U, Finlay BB, Hengge R, Johannes L, Ron EZ, Tonjum T, Sansonetti PJ, Vicente M, , 2012. The enemy within us: lessons from the 2011 European Escherichia coli O104:H4 outbreak. EMBO Mol Med 4: 841848.[Crossref] [Google Scholar]
  35. Ochoa TJ, 2009. High frequency of antimicrobial drug resistance of diarrheagenic Escherichia coli in infants in Peru. Am J Trop Med Hyg 81: 296301. [Google Scholar]

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  • Received : 26 Jan 2017
  • Accepted : 24 Jul 2017
  • Published online : 09 Oct 2017

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