1887

Abstract

The prevalence of infection caused by different categories of diarrhoeagenic (DEC) strains, including enteroaggregative (EAEC), enteropathogenic (EPEC), enterotoxigenic (ETEC), enteroinvasive (EIEC) and enterohaemorrhagic (EHEC) , in children who suffered from diarrhoea ( = 3943) or did not have diarrhoea ( = 1026) were analysed in two areas in Bolivia over a period of 4 years. We also analysed the seasonality of DEC infections and severity of diarrhoea in children with DEC infection and compared antibiotic resistance in DEC strains isolated from children with and without diarrhoea. Stool samples were analysed for the presence of DEC by culturing followed by PCR. The most prevalent DEC categories in samples from the children were: EAEC (11.2 %); ETEC (6.6 %); EPEC (5.8 %); and EIEC and EHEC (<1 %). DEC strains were isolated significantly more often from diarrhoea cases (21.6 %) than from controls (17.6 %;  = 0.002). The number of children with diarrhoea associated with EAEC, EPEC and ETEC infections peaked in the Bolivian winter (April–September), although the proportion of DEC-positive stool samples was higher during the warm rainy season (October–March). High levels of antibiotic resistance were detected among the DEC strains. In particular, resistance to tetracycline and sulfamethoxazole–trimethoprim was significantly higher in strains isolated from individuals with diarrhoea than in samples from controls. The severity of disease in children infected with EAEC, EPEC and ETEC varied from mild to severe diarrhoea, although disease severity did not differ significantly between the different DEC categories. ETEC, EPEC and EAEC are commonly found in Bolivia and may cause severe disease in children.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.060798-0
2013-11-01
2024-11-06
Loading full text...

Full text loading...

/deliver/fulltext/jmm/62/11/1697.html?itemId=/content/journal/jmm/10.1099/jmm.0.060798-0&mimeType=html&fmt=ahah

References

  1. Al-Gallas N., Bahri O., Bouratbeen A., Ben Haasen A., Ben Aissa R. 2007; Etiology of acute diarrhea in children and adults in Tunis, Tunisia, with emphasis on diarrheagenic Escherichia coli: prevalence, phenotyping, and molecular epidemiology. Am J Trop Med Hyg 77:571–582[PubMed]
    [Google Scholar]
  2. Araujo J. M., Tabarelli G. F., Aranda K. R., Fabbricotti S. H., Fagundes-Neto U., Mendes C. M., Scaletsky I. C. 2007; Typical enteroaggregative and atypical enteropathogenic types of Escherichia coli are the most prevalent diarrhea-associated pathotypes among Brazilian children. J Clin Microbiol 45:3396–3399 [View Article][PubMed]
    [Google Scholar]
  3. Berlutti F., Casalino M., Zagaglia C., Fradiani P. A., Visca P., Nicoletti M. 1998; Expression of the virulence plasmid-carried apyrase gene (apy) of enteroinvasive Escherichia coli and Shigella flexneri is under the control of H-NS and the VirF and VirB regulatory cascade. Infect Immun 66:4957–4964[PubMed]
    [Google Scholar]
  4. Bernstein D. I. 2009; Rotavirus overview. Pediatr Infect Dis J 28:SupplS50–S53 [View Article][PubMed]
    [Google Scholar]
  5. Cebula T. A., Payne W. L., Feng P. 1995; Simultaneous identification of strains of Escherichia coli serotype O157:H7 and their Shiga-like toxin type by mismatch amplification mutation assay-multiplex PCR. J Clin Microbiol 33:248–250[PubMed]
    [Google Scholar]
  6. Elliott E. J., Dalby-Payne J. R. 2004; 2. Acute infectious diarrhoea and dehydration in children. Med J Aust 181:565–570[PubMed]
    [Google Scholar]
  7. Estrada-Garcia T., Lopez-Saucedo C., Thompson-Bonilla R., Abonce M., Lopez-Hernandez D., Santos J. I., Rosado J. L., DuPont H. L., Long K. Z. 2009; Association of diarrheagenic Escherichia coli pathotypes with infection and diarrhea among Mexican children and association of atypical enteropathogenic E. coli with acute diarrhea. J Clin Microbiol 47:93–98 [View Article][PubMed]
    [Google Scholar]
  8. Franzolin M. R., Alves R. C., Keller R., Gomes T. A., Beutin L., Barreto M. L., Milroy C., Strina A., Ribeiro H., Trabulsi L. R. 2005; Prevalence of diarrheagenic Escherichia coli in children with diarrhea in Salvador, Bahia, Brazil. Mem Inst Oswaldo Cruz 100:359–363 [View Article][PubMed]
    [Google Scholar]
  9. Gaastra W., Svennerholm A. M. 1996; Colonization factors of human enterotoxigenic Escherichia coli (ETEC). Trends Microbiol 4:444–452 [View Article][PubMed]
    [Google Scholar]
  10. Gómez-Duarte O. G., Arzuza O., Urbina D., Bai J., Guerra J., Montes O., Puello M., Mendoza K., Castro G. Y. 2010; Detection of Escherichia coli enteropathogens by multiplex polymerase chain reaction from children’s diarrheal stools in two Caribbean-Colombian cities. Foodborne Pathog Dis 7:199–206 [View Article][PubMed]
    [Google Scholar]
  11. Grassly N. C., Fraser C. 2006; Seasonal infectious disease epidemiology. Proc Biol Sci 273:2541–2550 [View Article][PubMed]
    [Google Scholar]
  12. Harrington S. M., Dudley E. G., Nataro J. P. 2006; Pathogenesis of enteroaggregative Escherichia coli infection. FEMS Microbiol Lett 254:12–18 [View Article][PubMed]
    [Google Scholar]
  13. INE (Instituto Nacional de Estadística de Bolivia) 2002; Servicio Nacional de Información de Salud. Datos estadísticos en Salud.
  14. 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]
  15. Kahali S., Sarkar B., Chakraborty S., Macaden R., Deokule J. S., Ballal M., Nandy R. K., Bhattacharya S. K., Takeda Y., Ramamurthy T. 2004; Molecular epidemiology of diarrhoeagenic Escherichia coli associated with sporadic cases and outbreaks of diarrhoea between 2000 and 2001 in India. Eur J Epidemiol 19:473–479 [View Article][PubMed]
    [Google Scholar]
  16. Kotloff K. L., Nataro J. P., Blackwelder W. C., Nasrin D., Farag T. H., Panchalingam S., Wu Y., Sow S. O., Sur D. other authors 2013; 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. Lancet 382:209–222 [View Article][PubMed]
    [Google Scholar]
  17. López-Vidal Y., Calva J. J., Trujillo A., Ponce de León A., Ramos A., Svennerholm A. M., Ruiz-Palacios G. M. 1990; Enterotoxins and adhesins of enterotoxigenic Escherichia coli: are they risk factors for acute diarrhea in the community?. J Infect Dis 162:442–447 [View Article][PubMed]
    [Google Scholar]
  18. Mandomando I. M., Macete E. V., Ruiz J., Sanz S., Abacassamo F., Vallès X., Sacarlal J., Navia M. M., Vila J. other authors 2007; Etiology of diarrhea in children younger than 5 years of age admitted in a rural hospital of southern Mozambique. Am J Trop Med Hyg 76:522–527[PubMed]
    [Google Scholar]
  19. MSD (Ministerio de Salud y Deportes de Bolivia) 2008; Programa Ampliado de Inmunizaciones. Boletín informativo de la vigilancia de rotavirus en Bolivia. Publicación 4.
  20. Moon J. Y., Park J. H., Kim Y. B. 2005; Molecular epidemiological characteristics of virulence factors on enteroaggregative E. coli.. FEMS Microbiol Lett 253:215–220 [View Article][PubMed]
    [Google Scholar]
  21. Nataro J. P., Kaper J. B. 1998; Diarrheagenic Escherichia coli.. Clin Microbiol Rev 11:142–201[PubMed]
    [Google Scholar]
  22. National Committee for Clinical Laboratory Standards 2002; Performance standards for antimicrobial disk susceptibility testing. 12th Informational Supplement, M100–S12.
  23. Nguyen T. V., Le P. V., Le C. H., Weintraub A. 2005a; Antibiotic resistance in diarrheagenic Escherichia coli and Shigella strains isolated from children in Hanoi, Vietnam. Antimicrob Agents Chemother 49:816–819 [View Article][PubMed]
    [Google Scholar]
  24. Nguyen T. V., Le Van P., Le Huy C., Gia K. N., Weintraub A. 2005b; Detection and characterization of diarrheagenic Escherichia coli from young children in Hanoi, Vietnam. J Clin Microbiol 43:755–760 [View Article][PubMed]
    [Google Scholar]
  25. Nunes E. B., Saridakis H., 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 Lodrina, Brazil. J Med Microbiol 52:499–504 [View Article][PubMed]
    [Google Scholar]
  26. Ochoa T. J., Ruiz J., Molina M., Del Valle L. J., Vargas M., Gil A. I., Ecker L., Barletta F., Hall E. other authors 2009a; High frequency of antimicrobial drug resistance of diarrheagenic Escherichia coli in infants in Peru. Am J Trop Med Hyg 81:296–301[PubMed]
    [Google Scholar]
  27. Ochoa T. J., Ecker L., Barletta F., Mispireta M. L., Gil A. I., Contreras C., Molina M., Amemiya I., Verastegui H. other authors 2009b; Age-related susceptibility to infection with diarrheagenic Escherichia coli among infants from Periurban areas in Lima, Peru. Clin Infect Dis 49:1694–1702 [View Article][PubMed]
    [Google Scholar]
  28. Okeke I. N., Ojo O., Lamikanra A., Kaper J. B. 2003; Etiology of acute diarrhea in adults in southwestern Nigeria. J Clin Microbiol 41:4525–4530 [View Article][PubMed]
    [Google Scholar]
  29. Okeke I. N., Aboderin O. A., Byarugaba D. K., Ojo K. K., Opintan J. A. 2007; Growing problem of multidrug-resistant enteric pathogens in Africa. Emerg Infect Dis 13:1640–1646 [View Article][PubMed]
    [Google Scholar]
  30. Parashar U. D., Holman R. C., Clarke M. J., Bresee J. S., Glass R. I. 1998; Hospitalizations associated with rotavirus diarrhea in the United States, 1993 through 1995: surveillance based on the new ICD-9-CM rotavirus-specific diagnostic code. J Infect Dis 177:13–17 [View Article][PubMed]
    [Google Scholar]
  31. Pascual M., Dobson A. 2005; Seasonal patterns of infectious diseases. PLoS Med 2:e5 [View Article][PubMed]
    [Google Scholar]
  32. Pathela P., Zahid Hasan K., Roy E., Huq F., Kasem Siddique A., Bradley Sack R. 2006; Diarrheal illness in a cohort of children 0–2 years of age in rural Bangladesh: I. Incidence and risk factors. Acta Paediatr 95:430–437 [View Article][PubMed]
    [Google Scholar]
  33. Petri W. A. Jr, Miller M., Binder H. J., Levine M. M., Dillingham R., Guerrant R. L. 2008; Enteric infections, diarrhea, and their impact on function and development. J Clin Invest 118:1277–1290 [View Article][PubMed]
    [Google Scholar]
  34. Prado J. V., Cavagnaro S. M. F. Grupo de Estudio de Infecciones por STEC 2008; [Hemolytic uremic syndrome associated to shigatoxin producing Escherichia coli in Chilean children: clinical and epidemiological aspects]. Rev Chilena Infectol 25:435–444[PubMed]
    [Google Scholar]
  35. Putnam S. D., Riddle M. S., Wierzba T. F., Pittner B. T., Elyazeed R. A., El-Gendy A., Rao M. R., Clemens J. D., Frenck R. W. 2004; Antimicrobial susceptibility trends among Escherichia coli and Shigella spp. isolated from rural Egyptian paediatric populations with diarrhoea between 1995 and 2000. Clin Microbiol Infect 10:804–810 [View Article][PubMed]
    [Google Scholar]
  36. Qadri F., Das S. K., Faruque A. S., Fuchs G. J., Albert M. J., Sack R. B., Svennerholm A. M. 2000; Prevalence of toxin types and colonization factors in enterotoxigenic Escherichia coli isolated during a 2-year period from diarrheal patients in Bangladesh. J Clin Microbiol 38:27–31[PubMed]
    [Google Scholar]
  37. Qadri F., Khan A. I., Faruque A. S., Begum Y. A., Chowdhury F., Nair G. B., Salam M. A., Sack D. A., Svennerholm A. M. 2005; Enterotoxigenic Escherichia coli and Vibrio cholerae diarrhea, Bangladesh, 2004. Emerg Infect Dis 11:1104–1107 [View Article][PubMed]
    [Google Scholar]
  38. Ratchtrachenchai O. A., Subpasu S., Hayashi H., Ba-Thein W. 2004; Prevalence of childhood diarrhoea-associated Escherichia coli in Thailand. J Med Microbiol 53:237–243 [View Article][PubMed]
    [Google Scholar]
  39. Regua-Mangia A. H., Gomes T. A., Vieira M. A., Andrade J. R., Irino K., Teixeira L. M. 2004; Frequency and characteristics of diarrhoeagenic Escherichia coli strains isolated from children with and without diarrhoea in Rio de Janeiro, Brazil. J Infect 48:161–167 [View Article][PubMed]
    [Google Scholar]
  40. Reid S. D., Betting D. J., Whittam T. S. 1999; Molecular detection and identification of intimin alleles in pathogenic Escherichia coli by multiplex PCR. J Clin Microbiol 37:2719–2722[PubMed]
    [Google Scholar]
  41. Ricci K. A., Girosi F., Tarr P. I., Lim Y. W., Mason C., Miller M., Hughes J., von Seidlein L., Agosti J. M., Guerrant R. L. 2006; Reducing stunting among children: the potential contribution of diagnostics. Nature 444:Suppl 129–38[PubMed] [CrossRef]
    [Google Scholar]
  42. Rivas M., Miliwebsky E., Chinen I., Roldán C. D., Balbi L., García B., Fiorilli G., Sosa-Estani S., Kincaid J. other authors 2006; Characterization and epidemiologic subtyping of Shiga toxin-producing Escherichia coli strains isolated from hemolytic uremic syndrome and diarrhea cases in Argentina. Foodborne Pathog Dis 3:88–96 [View Article][PubMed]
    [Google Scholar]
  43. Rivera R., Forney K., Castro M. R., Rebolledo P. A., Mamani N., Patzi M., Halkyer P., Leon J. S., Iñiguez V. 2013; Rotavirus genotype distribution during the pre-vaccine period in Bolivia: 2007-2008. Int J Infect Dis (in press) [View Article][PubMed]
    [Google Scholar]
  44. Rodas C., Iniguez V., Qadri F., Wiklund G., Svennerholm A. M., Sjöling A. 2009; Development of multiplex PCR assays for detection of enterotoxigenic Escherichia coli colonization factors and toxins. J Clin Microbiol 47:1218–1220 [View Article][PubMed]
    [Google Scholar]
  45. Romero C., Madani N., Halvorsen K., Iñiguez V. 2007; Enfermedades diarreicas agudas asociadas a rotavirus. Arch Pediatr Urug 78:170–178
    [Google Scholar]
  46. Rosa A. C., Mariano A. T., Pereira A. M. S., Tibana A., Gomes T. A., Andrade J. R. 1998; Enteropathogenicity markers in Escherichia coli isolated from infants with acute diarrhoea and healthy controls in Rio de Janeiro, Brazil. J Med Microbiol 47:781–790 [View Article][PubMed]
    [Google Scholar]
  47. Ruuska T., Vesikari T. 1990; Rotavirus disease in Finnish children: use of numerical scores for clinical severity of diarrhoeal episodes. Scand J Infect Dis 22:259–267 [View Article][PubMed]
    [Google Scholar]
  48. Sanchez S. R. P., Guachalla L. M., Iñiguez V. 2006; Caracterizacion geno-fenotipica de aislados de Escherichia coli AEEC de pacientes pediatricos con procesos diarreicos infecciosos en la ciudad de La Paz: implicancias para el diagnostico y epidemiologia de las enfermedades diarreicas agudas. Arch Prediatr Urug 77:14
    [Google Scholar]
  49. Sjöling A., Wiklund G., Savarino S. J., Cohen D. I., Svennerholm A. M. 2007; Comparative analyses of phenotypic and genotypic methods for detection of enterotoxigenic Escherichia coli toxins and colonization factors. J Clin Microbiol 45:3295–3301 [View Article][PubMed]
    [Google Scholar]
  50. Smith E. R., Rowlinson E. E., Iniguez V., Etienne K. A., Rivera R., Mamani N., Rheingans R., Patzi M., Halkyer P., Leon J. S. 2011; Cost-effectiveness of rotavirus vaccination in Bolivia from the state perspective. Vaccine 29:6704–6711 [View Article][PubMed]
    [Google Scholar]
  51. Spano L. C., Sadovsky A. D., Segui P. N., Saick K. W., Kitagawa S. M., Pereira F. E., Fagundes-Neto U., Scaletsky I. C. 2008; Age-specific prevalence of diffusely adherent Escherichia coli in Brazilian children with acute diarrhoea. J Med Microbiol 57:359–363 [View Article][PubMed]
    [Google Scholar]
  52. Torres M. E., Pírez M. C., Schelotto F., Varela G., Parodi V., Allende F., Falconi E., Dell’Acqua L., Gaione P. other authors 2001; Etiology of children’s diarrhea in Montevideo, Uruguay: associated pathogens and unusual isolates. J Clin Microbiol 39:2134–2139 [View Article][PubMed]
    [Google Scholar]
  53. Vilchez S., Reyes D., Paniagua M., Bucardo F., Möllby R., Weintraub A. 2009; Prevalence of diarrhoeagenic Escherichia coli in children from León, Nicaragua. J Med Microbiol 58:630–637 [View Article][PubMed]
    [Google Scholar]
  54. World Health Organization, WHO 2008; Bolivia (Plurinational State of). Health profile.
/content/journal/jmm/10.1099/jmm.0.060798-0
Loading
/content/journal/jmm/10.1099/jmm.0.060798-0
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