Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2014 (2014), Article ID 236260, 11 pages
http://dx.doi.org/10.1155/2014/236260
Research Article

Phenotypic and Genotypic Characterization of Enterotoxigenic Escherichia coli Clinical Isolates from Northern Colombia, South America

1Division of Pediatric Infectious Diseases, Vanderbilt University School of Medicine, 1161 21st Avenue South, Nashville, TN 37232-2581, USA
2Departamento de Microbiología, Grupo de Microbiología Clínica y Ambiental, Universidad de Cartagena, Cartagena, Colombia

Received 17 January 2014; Revised 7 April 2014; Accepted 8 April 2014; Published 30 April 2014

Academic Editor: Chensong Wan

Copyright © 2014 Julio A. Guerra et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. K. L. Kotloff, J. P. Nataro, W. C. Blackwelder et al., “Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study,” The Lancet, vol. 382, no. 9888, pp. 209–222, 2013. View at Publisher · View at Google Scholar
  2. F. Qadri, A.-M. Svennerholm, A. S. G. Faruque, and R. B. Sack, “Enterotoxigenic Escherichia coli in developing countries: epidemiology, microbiology, clinical features, treatment, and prevention,” Clinical Microbiology Reviews, vol. 18, no. 3, pp. 465–483, 2005. View at Publisher · View at Google Scholar · View at Scopus
  3. R. I. Walker, D. Steele, and T. Aguado, “Analysis of strategies to successfully vaccinate infants in developing countries against enterotoxigenic E. coli (ETEC) disease,” Vaccine, vol. 25, no. 14, pp. 2545–2566, 2007. View at Publisher · View at Google Scholar · View at Scopus
  4. World Health Organization (WHO), “Weekly epidemiological record,” 2006, http://www.who.int/wer/2006/wer8111.pdf.
  5. J. Ouyang-Latimer, N. J. Ajami, Z.-D. Jiang et al., “Biochemical and genetic diversity of enterotoxigenic Escherichia coli associated with diarrhea in United States students in Cuernavaca and Guadalajara, Mexico, 2004–2007,” The Journal of Infectious Diseases, vol. 201, no. 12, pp. 1831–1838, 2010. View at Publisher · View at Google Scholar · View at Scopus
  6. C. Rodas, J. D. Klena, M. Nicklasson, V. Iniguez, and Å. Sjöling, “Clonal relatedness of enterotoxigenic Escherichia coli (ETEC) strains expressing LT and CS17 isolated from children with diarrhoea in La Paz, Bolivia,” PLoS ONE, vol. 6, no. 11, Article ID e18313, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. H. I. Shaheen, S. B. Khalil, M. R. Rao et al., “Phenotypic profiles of enterotoxigenic Escherichia coli associated with early childhood diarrhea in rural Egypt,” Journal of Clinical Microbiology, vol. 42, no. 12, pp. 5588–5595, 2004. View at Publisher · View at Google Scholar · View at Scopus
  8. H. Steinsland, D. W. Lacher, H. Sommerfelt, and T. S. Whittam, “Ancestral lineages of human enterotoxigenic Escherichia coli,” Journal of Clinical Microbiology, vol. 48, no. 8, pp. 2916–2924, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. F. C. Dorsey, J. F. Fischer, and J. M. Fleckenstein, “Directed delivery of heat-labile enterotoxin by enterotoxigenic Escherichia coli,” Cellular Microbiology, vol. 8, no. 9, pp. 1516–1527, 2006. View at Publisher · View at Google Scholar · View at Scopus
  10. J. M. Fleckenstein, P. R. Hardwidge, G. P. Munson, D. A. Rasko, H. Sommerfelt, and H. Steinsland, “Molecular mechanisms of enterotoxigenic Escherichia coli infection,” Microbes and Infection, vol. 12, no. 2, pp. 89–98, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. I. Bölin, G. Wiklund, F. Qadri et al., “Enterotoxigenic Escherichia coli with STh and STp genotypes is associated with diarrhea both in children in areas of endemicity and in travelers,” Journal of Clinical Microbiology, vol. 44, no. 11, pp. 3872–3877, 2006. View at Publisher · View at Google Scholar · View at Scopus
  12. W. Zhang, D. C. Robertson, C. Zhang, W. Bai, M. Zhao, and D. H. Francis, “Escherichia coli constructs expressing human or porcine enterotoxins induce identical diarrheal diseases in a piglet infection model,” Applied and Environmental Microbiology, vol. 74, no. 18, pp. 5832–5837, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. N. Konishi, H. Obata, C. Monma, A. Nakama, A. Kai, and T. Tsuji, “Bacteriological and epidemiological characteristics of enterotoxigenic Escherichia coli isolated in Tokyo, Japan, between 1966 and 2009,” Journal of Clinical Microbiology, vol. 49, no. 9, pp. 3348–3351, 2011. View at Publisher · View at Google Scholar · View at Scopus
  14. W. Gaastra and A.-M. Svennerholm, “Colonization factors of human enterotoxigenic Escherichia coli (ETEC),” Trends in Microbiology, vol. 4, no. 11, pp. 444–452, 1996. View at Publisher · View at Google Scholar · View at Scopus
  15. S. D. Isidean, M. S. Riddle, S. J. Savarino, and C. K. Porter, “A systematic review of ETEC epidemiology focusing on colonization factor and toxin expression,” Vaccine, vol. 29, no. 37, pp. 6167–6178, 2011. View at Publisher · View at Google Scholar · View at Scopus
  16. M. R. Rao, R. Abu-Elyazeed, S. J. Savarino et al., “High disease burden of diarrhea due to enterotoxigenic Escherichia coli among rural Egyptian infants and young children,” Journal of Clinical Microbiology, vol. 41, no. 10, pp. 4862–4864, 2003. View at Publisher · View at Google Scholar · View at Scopus
  17. G. I. Viboud, M. J. Jouve, N. Binsztein et al., “Prospective cohort study of enterotoxigenic Escherichia coli infections in Argentinean children,” Journal of Clinical Microbiology, vol. 37, no. 9, pp. 2829–2833, 1999. View at Google Scholar · View at Scopus
  18. J. M. Fleckenstein, D. J. Kopecko, R. L. Warren, and E. A. Elsinghorst, “Molecular characterization of the tia invasion locus from enterotoxigenic Escherichia coli,” Infection and Immunity, vol. 64, no. 6, pp. 2256–2265, 1996. View at Google Scholar · View at Scopus
  19. C. Lindenthal and E. A. Elsinghorst, “Identification of a glycoprotein produced by enterotoxigenic Escherichia coli,” Infection and Immunity, vol. 67, no. 8, pp. 4084–4091, 1999. View at Google Scholar · View at Scopus
  20. E. A. Brown and P. R. Hardwidge, “Biochemical characterization of the enterotoxigenic Escherichia coli LeoA protein,” Microbiology, vol. 153, no. 11, pp. 3776–3784, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. J. M. Fleckenstein, L. E. Lindler, E. A. Elsinghorst, and J. B. Dale, “Identification of a gene within a pathogenicity island of enterotoxigenic Escherichia coli H10407 required for maximal secretion of the heat-labile enterotoxin,” Infection and Immunity, vol. 68, no. 5, pp. 2766–2774, 2000. View at Publisher · View at Google Scholar · View at Scopus
  22. J.-P. Côté and M. Mourez, “Structure-function analysis of the TibA self-associating autotransporter reveals a modular organization,” Infection and Immunity, vol. 79, no. 5, pp. 1826–1832, 2011. View at Publisher · View at Google Scholar · View at Scopus
  23. C. Lindenthal and E. A. Elsinghorst, “Enterotoxigenic Escherichia coli TibA glycoprotein adheres to human intestine epithelial cells,” Infection and Immunity, vol. 69, no. 1, pp. 52–57, 2001. View at Publisher · View at Google Scholar · View at Scopus
  24. K. Roy, D. Hamilton, K. P. Allen, M. P. Randolph, and J. M. Fleckenstein, “The EtpA exoprotein of enterotoxigenic Escherichia coli promotes intestinal colonization and is a protective antigen in an experimental model of murine infection,” Infection and Immunity, vol. 76, no. 5, pp. 2106–2112, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. K. Roy, R. Kansal, S. R. Bartels, D. J. Hamilton, S. Shaaban, and J. M. Fleckenstein, “Adhesin degradation accelerates delivery of heat-labile toxin by enterotoxigenic Escherichia coli,” The Journal of Biological Chemistry, vol. 286, no. 34, pp. 29771–29779, 2011. View at Publisher · View at Google Scholar · View at Scopus
  26. S. K. Patel, J. Dotson, K. P. Allen, and J. M. Fleckenstein, “Identification and molecular characterization of EatA, an autotransporter protein of enterotoxigenic Escherichia coli,” Infection and Immunity, vol. 72, no. 3, pp. 1786–1794, 2004. View at Publisher · View at Google Scholar · View at Scopus
  27. S. Schubert, A. Rakin, H. Karch, E. Carniel, and J. Heesemann, “Prevalence of the “high-pathogenicity island” of Yersinia species among Escherichia coli strains that are pathogenic to humans,” Infection and Immunity, vol. 66, no. 2, pp. 480–485, 1998. View at Google Scholar · View at Scopus
  28. O. G. Gomez-Duarte, Y. C. Romero-Herazo, C. Z. Paez-Canro, J. H. Eslava-Schmalbach, and O. Arzuza, “Enterotoxigenic Escherichia coli associated with childhood diarrhoea in Colombia, South America,” The Journal of Infection in Developing Countries, vol. 7, no. 5, pp. 372–381, 2013. View at Google Scholar
  29. O. G. Gómez-Duarte, O. Arzuza, D. Urbina et al., “Detection of Escherichia coli enteropathogens by multiplex polymerase chain reaction from children's diarrheal stools in two Caribbean-Colombian cities,” Foodborne Pathogens and Disease, vol. 7, no. 2, pp. 199–206, 2010. View at Publisher · View at Google Scholar · View at Scopus
  30. M. R. Green, Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, USA, 4th edition, 2012.
  31. O. G. Gómez-Duarte, J. Bai, and E. Newell, “Detection of Escherichia coli, Salmonella spp., Shigella spp., Yersinia enterocolitica, Vibrio cholerae, and Campylobacter spp. enteropathogens by 3-reaction multiplex polymerase chain reaction,” Diagnostic Microbiology & Infectious Disease, vol. 63, no. 1, pp. 1–9, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. C. Rodas, V. Iniguez, F. Qadri, G. Wiklund, A.-M. Svennerholm, and Å. Sjoling, “Development of multiplex PCR assays for detection of enterotoxigenic Escherichia coli colonization factors and toxins,” Journal of Clinical Microbiology, vol. 47, no. 4, pp. 1218–1220, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. F. del Canto, P. Valenzuela, L. Cantero et al., “Distribution of classical and nonclassical virulence genes in enterotoxigenic Escherichia coli isolates from Chilean children and tRNA gene screening for putative insertion sites for genomic islands,” Journal of Clinical Microbiology, vol. 49, no. 9, pp. 3198–3203, 2011. View at Publisher · View at Google Scholar · View at Scopus
  34. T. Wirth, D. Falush, R. Lan et al., “Sex and virulence in Escherichia coli: an evolutionary perspective,” Molecular Microbiology, vol. 60, no. 5, pp. 1136–1151, 2006. View at Publisher · View at Google Scholar · View at Scopus
  35. A. Dereeper, V. Guignon, G. Blanc et al., “Phylogeny.fr: robust phylogenetic analysis for the non-specialist,” Nucleic Acids Research, vol. 36, pp. W465–W469, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. A. Dereeper, S. Audic, J.-M. Claverie, and G. Blanc, “BLAST-EXPLORER helps you building datasets for phylogenetic analysis,” BMC Evolutionary Biology, vol. 10, no. 1, article 8, 2010. View at Publisher · View at Google Scholar · View at Scopus
  37. I. Orskov, F. Orskov, B. Jann, and K. Jann, “Serology, chemistry, and genetics of O and K antigens of Escherichia coli,” Bacteriological Reviews, vol. 41, no. 3, pp. 667–710, 1977. View at Google Scholar · View at Scopus
  38. J. Machado, F. Grimont, and P. A. D. Grimont, “Identification of Escherichia coli flagellar types by restriction of the amplified fliC gene,” Research in Microbiology, vol. 151, no. 7, pp. 535–546, 2000. View at Publisher · View at Google Scholar · View at Scopus
  39. M. M. Levine, P. Ristaino, G. Marley et al., “Coli surface antigens 1 and 3 of colonization factor antigen II-positive enterotoxigenic Escherichia coli: morphology, purification, and immune responses in humans,” Infection and Immunity, vol. 44, no. 2, pp. 409–420, 1984. View at Google Scholar
  40. D. G. Evans, R. P. Silver, D. J. Evans Jr., D. G. Chase, and S. L. Gorbach, “Plasmid-controlled colonization factor associated with virulence in Esherichia coli enterotoxigenic for humans,” Infection and Immunity, vol. 12, no. 3, pp. 656–667, 1975. View at Google Scholar
  41. L. Gonzales, S. Sanchez, S. Zambrana et al., “Molecular characterization of enterotoxigenic Escherichia coli isolates recovered from children with diarrhea during a 4-year period (2007 to 2010) in Bolivia,” Journal of Clinical Microbiology, vol. 51, no. 4, pp. 1219–1225, 2013. View at Publisher · View at Google Scholar
  42. R. E. Black, M. H. Merson, A. S. Rahman et al., “A two-year study of bacterial, viral, and parasitic agents associated with diarrhea in rural Bangladesh,” The Journal of Infectious Diseases, vol. 142, no. 5, pp. 660–664, 1980. View at Google Scholar · View at Scopus
  43. F. P. Rivera, T. J. Ochoa, R. C. Maves et al., “Genotypic and phenotypic characterization of enterotoxigenic Escherichia coli strains isolated from peruvian children,” Journal of Clinical Microbiology, vol. 48, no. 9, pp. 3198–3203, 2010. View at Publisher · View at Google Scholar · View at Scopus
  44. B. A. Oyofo, D. S. Subekti, A.-M. Svennerholm et al., “Toxins and colonization factor antigens of enterotoxigenic Escherichia coli among residents of Jakarta, Indonesia,” The American Journal of Tropical Medicine and Hygiene, vol. 65, no. 2, pp. 120–124, 2001. View at Google Scholar · View at Scopus
  45. H. Steinsland, P. Valentiner-Branth, H. M. S. Grewal, W. Gaastra, K. Mølbak, and H. Sommerfelt, “Development and evaluation of genotypic assays for the detection and characterization of enterotoxigenic Escherichia coli,” Diagnostic Microbiology & Infectious Disease, vol. 45, no. 2, pp. 97–105, 2003. View at Publisher · View at Google Scholar · View at Scopus
  46. C. Rodas, R. Mamani, J. Blanco et al., “Enterotoxins, colonization factors, serotypes and antimicrobial resistance of enterotoxigenic Escherichia coli (ETEC) strains isolated from hospitalized children with diarrhea in Bolivia,” Brazilian Journal of Infectious Diseases, vol. 15, no. 2, pp. 132–137, 2011. View at Publisher · View at Google Scholar · View at Scopus
  47. A. C. P. Vicente, L. F. M. Teixeira, L. Iniguez-Rojas et al., “Outbreaks of cholera-like diarrhoea caused by enterotoxigenic Escherichia coli in the Brazilian Amazon Rainforest,” Transactions of the Royal Society of Tropical Medicine & Hygiene, vol. 99, no. 9, pp. 669–674, 2005. View at Publisher · View at Google Scholar · View at Scopus
  48. J. A. Giron, G. I. Viboud, V. Sperandio et al., “Prevalence and association of the Longus pilus structural gene (lngA) with colonization factor antigens, enterotoxin types, and serotypes of enterotoxigenic Escherichia coli,” Infection and Immunity, vol. 63, no. 10, pp. 4195–4198, 1995. View at Google Scholar · View at Scopus
  49. Z. Gutiérrez-Cázarez, F. Qadri, M. J. Albert, and J. A. Girón, “Identification of enterotoxigenic Escherichia coli harboring Longus type IV pilus gene by DNA amplification,” Journal of Clinical Microbiology, vol. 38, no. 5, pp. 1767–1771, 2000. View at Google Scholar · View at Scopus
  50. L. S. Nishimura, J. A. Girón, S. L. Nunes, and B. E. C. Guth, “Prevalence of enterotoxigenic Escherichia coli strains harboring the Longus pilus gene in Brazil,” Journal of Clinical Microbiology, vol. 40, no. 7, pp. 2606–2608, 2002. View at Publisher · View at Google Scholar · View at Scopus
  51. M. G. Pichel, N. Binsztein, F. Qadri, and J. A. Girón, “Type IV Longus pilus of enterotoxigenic Escherichia coli: occurrence and association with toxin types and colonization factors among strains isolated in Argentina,” Journal of Clinical Microbiology, vol. 40, no. 2, pp. 694–697, 2002. View at Publisher · View at Google Scholar · View at Scopus
  52. A. P. Clavijo, J. Bai, and O. G. Gómez-Duarte, “The Longus type IV pilus of enterotoxigenic Escherichia coli (ETEC) mediates bacterial self-aggregation and protection from antimicrobial agents,” Microbial Pathogenesis, vol. 48, no. 6, pp. 230–238, 2010. View at Publisher · View at Google Scholar · View at Scopus
  53. C. P. Guevara, W. B. Luiz, A. Sierra et al., “Enterotoxigenic Escherichia coli (ETEC) CS21 pilus contributes to adhesion to intestinal cells and to pathogenesis under in vivo conditions,” Microbiology, vol. 159, no. 8, pp. 1725–1735, 2013. View at Publisher · View at Google Scholar
  54. K. Mazariego-Espinosa, A. Cruz, M. A. Ledesma, S. A. Ochoa, and J. Xicohtencatl-Cortes, “Longus, a type IV pilus of enterotoxigenic Escherichia coli, is involved in adherence to intestinal epithelial cells,” Journal of Bacteriology, vol. 192, no. 11, pp. 2791–2800, 2010. View at Publisher · View at Google Scholar · View at Scopus
  55. H. Sommerfeit, H. Steinsland, H. M. S. Grewal et al., “Colonization factors of enterotoxigenic Escherichia coli isolated from children in North India,” The Journal of Infectious Diseases, vol. 174, no. 4, pp. 768–776, 1996. View at Google Scholar · View at Scopus
  56. S. M. Turner, R. R. Chaudhuri, Z.-D. Jiang et al., “Phylogenetic comparisons reveal multiple acquisitions of the toxin genes by enterotoxigenic Escherichia coli strains of different evolutionary lineages,” Journal of Clinical Microbiology, vol. 44, no. 12, pp. 4528–4536, 2006. View at Publisher · View at Google Scholar · View at Scopus
  57. M. K. Wolf, “Occurrence, distribution, and associations of O and H serogroups, colonization factor antigens, and toxins of enterotoxigenic Escherichia coli,” Clinical Microbiology Reviews, vol. 10, no. 4, pp. 569–584, 1997. View at Google Scholar · View at Scopus
  58. A. B. F. Pacheco, B. E. C. Guth, K. C. C. Soares, L. Nishimura, D. F. de Almeida, and L. C. S. Ferreira, “Random amplification of polymorphic DNA reveals serotype-specific clonal clusters among enterotoxigenic Escherichia coli strains isolated from humans,” Journal of Clinical Microbiology, vol. 35, no. 6, pp. 1521–1525, 1997. View at Google Scholar · View at Scopus
  59. N. Al-Gallas, S. M. Abbassi, A. B. Hassan, and R. B. Aissa, “Genotypic and phenotypic profiles of enterotoxigenic Escherichia coli associated with acute diarrhea in Tunis, Tunisia,” Current Microbiology, vol. 55, no. 1, pp. 47–55, 2007. View at Publisher · View at Google Scholar · View at Scopus
  60. M. Ansaruzzaman, N. A. Bhuiyan, Y. A. Begum et al., “Characterization of enterotoxigenic Escherichia coli from diarrhoeal patients in Bangladesh using phenotyping and genetic profiling,” Journal of Medical Microbiology, vol. 56, no. 2, pp. 217–222, 2007. View at Publisher · View at Google Scholar · View at Scopus
  61. M. Nicklasson, J. Klena, C. Rodas et al., “Enterotoxigenic Escherichia coli multilocus sequence types in Guatemala and Mexico,” Emerging Infectious Diseases, vol. 16, no. 1, pp. 143–146, 2010. View at Publisher · View at Google Scholar · View at Scopus