1887

Abstract

Enteroaggregative (EAEC) is a subgroup of diarrhoeagenic (DEC) that during the past decade has received increasing attention as a cause of watery diarrhoea, which is often persistent. EAEC have been isolated from children and adults worldwide. As well as sporadic cases, outbreaks of EAEC-caused diarrhoea have been described. The definition of EAEC is the ability of the micro-organism to adhere to epithelial cells such as HEp-2 in a very characteristic ‘stacked-brick’ pattern. Although many studies searching for specific virulence factor(s) unique for this category of DEC have been published it is still unknown why the EAEC cause persistent diarrhoea. In addition, the aggregative property of EAEC causes a lot of problems in serotyping due to the cells auto-agglutinating. The gold standard for identification of EAEC includes isolation of the agent and an adherence assay using tissue culture, viz. HEp-2 cells. This assay is in most cases reliable; however, emergence of ‘atypical’ EAEC has been described in several publications. In addition, the HEp-2 assay is time consuming, demands a tissue culture lab and trained staff. Several molecular biological assays have been described, however, none show 100 % specificity.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.46930-0
2007-01-01
2020-01-24
Loading full text...

Full text loading...

/deliver/fulltext/jmm/56/1/4.html?itemId=/content/journal/jmm/10.1099/jmm.0.46930-0&mimeType=html&fmt=ahah

References

  1. Adachi, J. A., Jiang, Z. D., Mathewson, J. J., Verenkar, M. P., Thompson, S., Martinez-Sandoval, F., Steffen, R., Ericsson, C. D. & DuPont, H. L. ( 2001; ). Enteroaggregative Escherichia coli as a major etiologic agent in traveler's diarrhea in 3 regions of the world. Clin Infect Dis 32, 1706–1709.[CrossRef]
    [Google Scholar]
  2. Baudry, B., Savarino, S. J., Vial, P., Kaper, J. B. & Levine, M. M. ( 1990; ). A sensitive and specific DNA probe to identify enteroaggregative Escherichia coli, a recently discovered diarrheal pathogen. J Infect Dis 161, 1249–1251.[CrossRef]
    [Google Scholar]
  3. 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, 4302–4311.[CrossRef]
    [Google Scholar]
  4. Bhan, M. K., Bhandari, N., Sazawal, S., Clemens, J., Raj, P., Levine, M. M. & Kaper, J. B. ( 1989a; ). Descriptive epidemiology of persistent diarrhoea among young children in rural northern India. Bull World Health Organ 67, 281–288.
    [Google Scholar]
  5. Bhan, M. K., Raj, P., Levine, M. M., Kaper, J. B., Bhandari, N., Srivastava, R., Kumar, R. & Sazawal, S. ( 1989b; ). Enteroaggregative Escherichia coli associated with persistent diarrhea in a cohort of rural children in India. J Infect Dis 159, 1061–1064.[CrossRef]
    [Google Scholar]
  6. Bhan, M. K., Sazawal, S., Raj, P., Bhandari, N., Kumar, R., Bhardwaj, Y., Shrivastava, R. & Bhatnagar, S. ( 1989c; ). Aggregative Escherichia coli, Salmonella, and Shigella are associated with increasing duration of diarrhea. Indian J Pediatr 56, 81–86.[CrossRef]
    [Google Scholar]
  7. Bhatnagar, S., Bhan, M. K., Sommerfelt, H., Sazawal, S., Kumar, R. & Saini, S. ( 1993; ). Enteroaggregative Escherichia coli may be a new pathogen causing acute and persistent diarrhea. Scand J Infect Dis 25, 579–583.[CrossRef]
    [Google Scholar]
  8. Boudailliez, B., Berquin, P., Mariani-Kurkdjian, P., Ilef, D., Cuvelier, B., Capek, I., Tribout, B., Bingen, E. & Piussan, C. ( 1997; ). Possible person-to-person transmission of Escherichia coli O111-associated hemolytic uremic syndrome. Pediatr Nephrol 11, 36–39.[CrossRef]
    [Google Scholar]
  9. Bouzari, S., Jafari, A., Farhoudi-Moghaddam, A. A., Shokouhi, F. & Parsi, M. ( 1994; ). Adherence of non-enteropathogenic Escherichia coli to HeLa cells. J Med Microbiol 40, 95–97.[CrossRef]
    [Google Scholar]
  10. Cerna, J. F., Nataro, J. P. & Estrada-Garcia, T. ( 2003; ). Multiplex PCR for detection of three plasmid-borne genes of enteroaggregative Escherichia coli strains. J Clin Microbiol 41, 2138–2140.[CrossRef]
    [Google Scholar]
  11. Chan, K. N., Phillips, A. D., Knutton, S., Smith, H. R. & Walker-Smith, J. A. ( 1994; ). Enteroaggregative Escherichia coli: another cause of acute and chronic diarrhoea in England? J Pediatr Gastroenterol Nutr 18, 87–91.[CrossRef]
    [Google Scholar]
  12. Chart, H., Spencer, J., Smith, H. R. & Rowe, B. ( 1997; ). Magnesium ions are required for HEp-2 cell adhesion by enteroaggregative strains of Escherichia coli O126 : H27 and O44 : H18. FEMS Microbiol Lett 148, 49–52.[CrossRef]
    [Google Scholar]
  13. Cobeljic, M., Miljkovic-Selimovic, B., Paunovic-Todosijevic, D., Velickovic, Z., Lepsanovic, Z., Zec, N., Savic, D., Ilic, R., Konstantinovic, S. & other authors ( 1996; ). Enteroaggregative Escherichia coli associated with an outbreak of diarrhoea in a neonatal nursery ward. Epidemiol Infect 117, 11–16.[CrossRef]
    [Google Scholar]
  14. Cravioto, A., Gross, R. J., Scotland, S. M. & Rowe, B. ( 1979; ). An adhesive factor found in strains of Escherichia coli belonging to the traditional enteropathogenic serotypes. Curr Microbiol 3, 95–99.[CrossRef]
    [Google Scholar]
  15. Cravioto, A., Tello, A., Navarro, A., Ruiz, J., Villafan, H., Uribe, F. & Eslava, C. ( 1991; ). Association of Escherichia coli HEp-2 adherence patterns with type and duration of diarrhoea. Lancet 337, 262–264.[CrossRef]
    [Google Scholar]
  16. Czeczulin, J. R., Whittam, T. S., Henderson, I. R., Navarro-Garcia, F. & Nataro, J. P. ( 1999; ). Phylogenetic analysis of enteroaggregative and diffusely adherent Escherichia coli. Infect Immun 67, 2692–2699.
    [Google Scholar]
  17. Debroy, C., Yealy, J., Wilson, R. A., Bhan, M. K. & Kumar, R. ( 1995; ). Antibodies raised against the outer membrane protein interrupt adherence of enteroaggregative Escherichia coli. Infect Immun 63, 2873–2879.
    [Google Scholar]
  18. Echeverria, P., Serichantalerg, O., Changchawalit, S., Baudry, B., Levine, M. M., Orskov, F. & Orskov, I. ( 1992; ). Tissue culture-adherent Escherichia coli in infantile diarrhea. J Infect Dis 165, 141–143.[CrossRef]
    [Google Scholar]
  19. Elias, W. P., Barros, S. F., Moreira, C. G., Trabulsi, L. R. & Gomes, T. A. ( 2002; ). Enteroaggregative Escherichia coli strains among classical enteropathogenic Escherichia coli O serogroups. J Clin Microbiol 40, 3540–3541.[CrossRef]
    [Google Scholar]
  20. Eslava, C., Navarro-Garcia, F., Czeczulin, J. R., Henderson, I. R., Cravioto, A. & Nataro, J. P. ( 1998; ). Pet, an autotransporter enterotoxin from enteroaggregative Escherichia coli. Infect Immun 66, 3155–3163.
    [Google Scholar]
  21. Ewing, W. H., Davis, B. R. & Montague, T. S. ( 1963; ). Studies on the Occurence of Escherichia Coli Serotypes Associated with Diarrheal Disease, pp. 1–38. Atlanta, GA: US Department of Health, Education and Welfare, Public Health Service, CDC.
  22. Fang, G. D., Lima, A. A., Martins, C. V., Nataro, J. P. & Guerrant, R. L. ( 1995; ). Etiology and epidemiology of persistent diarrhea in northeastern Brazil: a hospital-based, prospective, case-control study. J Pediatr Gastroenterol Nutr 21, 137–144.[CrossRef]
    [Google Scholar]
  23. Food Standards Agency ( 2000; ). A Report of the Study of Infectious Intestinal Disease in England. London: The Stationery Office.
  24. Gascón, J., Vargas, M., Quinto, L., Corachan, M., Jimenez de Anta, M. T. & Vila, J. ( 1998; ). Enteroaggregative Escherichia coli strains as a cause of traveler's diarrhea: a case-control study. J Infect Dis 177, 1409–1412.[CrossRef]
    [Google Scholar]
  25. Gioppo, N. M., Elias, W. P., Jr, Vidotto, M. C., Linhares, R. E., Saridakis, H. O., Gomes, T. A., Trabulsi, L. R. & Pelayo, J. S. ( 2000; ). Prevalence of HEp-2 cell-adherent Escherichia coli and characterisation of enteroaggregative E. coli and chain-like adherent E. coli isolated from children with and without diarrhoea, in Londrina, Brazil. FEMS Microbiol Lett 190, 293–298.[CrossRef]
    [Google Scholar]
  26. Gomes, T. A., Blake, P. A. & Trabulsi, L. R. ( 1989; ). Prevalence of Escherichia coli strains with localized, diffuse, and aggregative adherence to HeLa cells in infants with diarrhea and matched controls. J Clin Microbiol 27, 266–269.
    [Google Scholar]
  27. Gonzalez, R., Diaz, C., Marino, M., Cloralt, R., Pequeneze, M. & Perez-Schael, I. ( 1997; ). Age-specific prevalence of Escherichia coli with localized and aggregative adherence in Venezuelan infants with acute diarrhea. J Clin Microbiol 35, 1103–1107.
    [Google Scholar]
  28. Grover, V., Ghosh, S., Sharma, N., Chakraborti, A., Majumdar, S. & Ganguly, N. K. ( 2001; ). Characterization of a galactose specific adhesin of enteroaggregative Escherichia coli. Arch Biochem Biophys 390, 109–118.[CrossRef]
    [Google Scholar]
  29. Haider, K., Faruque, S. M., Albert, M. J., Nahar, S., Neogi, P. K. & Hossain, A. ( 1992; ). Comparison of a modified adherence assay with existing assay methods for identification of enteroaggregative Escherichia coli. J Clin Microbiol 30, 1614–1616.
    [Google Scholar]
  30. Henderson, I. R., Czeczulin, J., Eslava, C., Noriega, F. & Nataro, J. P. ( 1999; ). Characterization of Pic, a secreted protease of Shigella flexneri and enteroaggregative Escherichia coli. Infect Immun 67, 5587–5596.
    [Google Scholar]
  31. Hicks, S., Candy, D. C. & Phillips, A. D. ( 1996; ). Adhesion of enteroaggregative Escherichia coli to pediatric intestinal mucosa in vitro. Infect Immun 64, 4751–4760.
    [Google Scholar]
  32. Huang, D. B., Mohanty, A., DuPont, H. L., Okhuysen, P. C. & Chiang, T. ( 2006; ). A review of an emerging enteric pathogen: enteroaggregative Escherichia coli. J Med Microbiol 55, 1303–1311.[CrossRef]
    [Google Scholar]
  33. Huppertz, H. I., Rutkowski, S., Aleksic, S. & Karch, H. ( 1997; ). Acute and chronic diarrhoea and abdominal colic associated with enteroaggregative Escherichia coli in young children living in western Europe. Lancet 349, 1660–1662.[CrossRef]
    [Google Scholar]
  34. Itoh, Y., Nagano, I., Kunishima, M. & Ezaki, T. ( 1997; ). Laboratory investigation of enteroaggregative Escherichia coli O untypeable : H10 associated with a massive outbreak of gastrointestinal illness. J Clin Microbiol 35, 2546–2550.
    [Google Scholar]
  35. Jenkins, C., Chart, H., Willshaw, G. A., Cheasty, T. & Smith, H. R. ( 2006a; ). Genotyping of enteroaggregative Escherichia coli and identification of target genes for the detection of both typical and atypical strains. Diagn Microbiol Infect Dis 55, 13–19.[CrossRef]
    [Google Scholar]
  36. Jenkins, C., Tembo, M., Chart, H., Cheasty, T., Willshaw, G. A., Phillips, A. D., Tompkins, D. & Smith, H. ( 2006b; ). Detection of enteroaggregative Escherichia coli in faecal samples from patients in the community with diarrhoea. J Med Microbiol 55, 1493–1497.[CrossRef]
    [Google Scholar]
  37. Kaper, J. B., Nataro, J. P. & Mobley, H. L. ( 2004; ). Pathogenic Escherichia coli. Nat Rev Microbiol 2, 123–140.[CrossRef]
    [Google Scholar]
  38. Knutton, S., Shaw, R., Phillips, A. D., Smith, H. R., Willshaw, G. A., Watson, P. & Price, E. ( 2001; ). Phenotypic and genetic analysis of diarrhea-associated Escherichia coli isolated from children in the United Kingdom. J Pediatr Gastroenterol Nutr 33, 32–40.[CrossRef]
    [Google Scholar]
  39. Law, D. & Chart, H. ( 1998; ). Enteroaggregative Escherichia coli. J Appl Microbiol 84, 685–697.[CrossRef]
    [Google Scholar]
  40. Lima, A. A., Fang, G., Schorling, J. B., de Albuquerque, L., McAuliffe, J. F., Mota, S., Leite, R. & Guerrant, R. L. ( 1992; ). Persistent diarrhea in northeast Brazil: etiologies and interactions with malnutrition. Acta Paediatr Suppl 381, 39–44.
    [Google Scholar]
  41. Mathewson, J. J., Johnson, P. C., DuPont, H. L., Morgan, D. R., Thornton, S. A., Wood, L. V. & Ericsson, C. D. ( 1985; ). A newly recognized cause of travelers' diarrhea: enteroadherent Escherichia coli. J Infect Dis 151, 471–475.[CrossRef]
    [Google Scholar]
  42. Mathewson, J. J., Oberhelman, R. A., Dupont, H. L., Javier de la Cabada, F. & Garibay, E. V. ( 1987; ). Enteroadherent Escherichia coli as a cause of diarrhea among children in Mexico. J Clin Microbiol 25, 1917–1919.
    [Google Scholar]
  43. Mayer, H. B. & Wanke, C. A. ( 1995; ). Enteroaggregative Escherichia coli as a possible cause of diarrhea in an HIV-infected patient. N Engl J Med 332, 273–274.
    [Google Scholar]
  44. Morabito, S., Karch, H., Mariani-Kurkdjian, P., Schmidt, H., Minelli, F., Bingen, E. & Caprioli, A. ( 1998; ). Enteroaggregative, Shiga toxin-producing Escherichia coli O111 : H2 associated with an outbreak of hemolytic-uremic syndrome. J Clin Microbiol 36, 840–842.
    [Google Scholar]
  45. Nataro, J. P. & Kaper, J. B. ( 1998; ). Diarrheagenic Escherichia coli. Clin Microbiol Rev 11, 142–201.
    [Google Scholar]
  46. Nataro, J. P., Kaper, J. B., Robins-Browne, R., Prado, V., Vial, P. & Levine, M. M. ( 1987; ). Patterns of adherence of diarrheagenic Escherichia coli to HEp-2 cells. Pediatr Infect Dis J 6, 829–831.[CrossRef]
    [Google Scholar]
  47. Nataro, J. P., Deng, Y., Maneval, D. R., German, A. L., Martin, W. C. & Levine, M. M. ( 1992; ). Aggregative adherence fimbriae I of enteroaggregative Escherichia coli mediate adherence to HEp-2 cells and hemagglutination of human erythrocytes. Infect Immun 60, 2297–2304.
    [Google Scholar]
  48. Nataro, J. P., Yikang, D., Yingkang, D. & Walker, K. ( 1994; ). AggR, a transcriptional activator of aggregative adherence fimbria I expression in enteroaggregative Escherichia coli. J Bacteriol 176, 4691–4699.
    [Google Scholar]
  49. Nataro, J. P., Deng, Y., Cookson, S., Cravioto, A., Savarino, S. J., Guers, L. D., Levine, M. M. & Tacket, C. O. ( 1995; ). Heterogeneity of enteroaggregative Escherichia coli virulence demonstrated in volunteers. J Infect Dis 171, 465–468.[CrossRef]
    [Google Scholar]
  50. Nataro, J. P., Steiner, T. & Guerrant, R. L. ( 1998; ). Enteroaggregative Escherichia coli. Emerg Infect Dis 4, 251–261.[CrossRef]
    [Google Scholar]
  51. Pai, M., Kang, G., Ramakrishna, B. S., Venkataraman, A. & Muliyil, J. ( 1997; ). An epidemic of diarrhoea in South India caused by enteroaggregative Escherichia coli. Indian J Med Res 106, 7–12.
    [Google Scholar]
  52. Paul, M., Tsukamoto, T., Ghosh, A. R., Bhattacharya, S. K., Manna, B., Chakrabarti, S., Nair, G. B., Sack, D. A., Sen, D. & Takeda, Y. ( 1994; ). The significance of enteroaggregative Escherichia coli in the etiology of hospitalized diarrhoea in Calcutta, India and the demonstration of a new honey-combed pattern of aggregative adherence. FEMS Microbiol Lett 117, 319–325.[CrossRef]
    [Google Scholar]
  53. Presterl, E., Nadrchal, R., Wolf, D., Rotter, M. & Hirschl, A. M. ( 1999; ). Enteroaggregative and enterotoxigenic Escherichia coli among isolates from patients with diarrhea in Austria. Eur J Clin Microbiol Infect Dis 18, 209–212.[CrossRef]
    [Google Scholar]
  54. Rich, C., Favre-Bonte, S., Sapena, F., Joly, B. & Forestier, C. ( 1999; ). Characterization of enteroaggregative Escherichia coli isolates. FEMS Microbiol Lett 173, 55–61.[CrossRef]
    [Google Scholar]
  55. Savarino, S. J., Fasano, A., Robertson, D. C. & Levine, M. M. ( 1991; ). Enteroaggregative Escherichia coli elaborate a heat-stable enterotoxin demonstrable in an in vitro rabbit intestinal model. J Clin Invest 87, 1450–1455.[CrossRef]
    [Google Scholar]
  56. Schmidt, H., Knop, C., Franke, S., Aleksic, S., Heesemann, J. & Karch, H. ( 1995; ). Development of PCR for screening of enteroaggregative Escherichia coli. J Clin Microbiol 33, 701–705.
    [Google Scholar]
  57. 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, 480–485.
    [Google Scholar]
  58. Schultsz, C., van den Ende, J., Cobelens, F., Vervoort, T., van Gompel, A., Wetsteyn, J. C. & Dankert, J. ( 2000; ). Diarrheagenic Escherichia coli and acute and persistent diarrhea in returned travelers. J Clin Microbiol 38, 3550–3554.
    [Google Scholar]
  59. Sheikh, J., Czeczulin, J. R., Harrington, S., Hicks, S., Henderson, I. R., Le Bouguenec, C., Gounon, P., Phillips, A. & Nataro, J. P. ( 2002; ). A novel dispersin protein in enteroaggregative Escherichia coli. J Clin Invest 110, 1329–1337.[CrossRef]
    [Google Scholar]
  60. Smith, H. R., Cheasty, T. & Rowe, B. ( 1997; ). Enteroaggregative Escherichia coli and outbreaks of gastroenteritis in UK. Lancet 350, 814–815.[CrossRef]
    [Google Scholar]
  61. Spencer, J., Smith, H. R. & Chart, H. ( 1999; ). Characterization of enteroaggregative Escherichia coli isolated from outbreaks of diarrhoeal disease in England. Epidemiol Infect 123, 413–421.[CrossRef]
    [Google Scholar]
  62. Svenungsson, B., Lagergren, A., Ekwall, E., Evengård, B., Hedlund, K. O., Kärnell, A., Löfdahl, S., Svensson, L. & Weintraub, A. ( 2000; ). Enteropathogens in adult patients with diarrhea and healthy control subjects: a 1-year prospective study in a Swedish clinic for infectious diseases. Clin Infect Dis 30, 770–778.[CrossRef]
    [Google Scholar]
  63. Vial, P. A., Robins-Browne, R., Lior, H., Prado, V., Kaper, J. B., Nataro, J. P., Maneval, D., Elsayed, A. & Levine, M. M. ( 1988; ). Characterization of enteroadherent-aggregative Escherichia coli, a putative agent of diarrheal disease. J Infect Dis 158, 70–79.[CrossRef]
    [Google Scholar]
  64. Vial, P. A., Mathewson, J. J., DuPont, H. L., Guers, L. & Levine, M. M. ( 1990; ). Comparison of two assay methods for patterns of adherence to HEp-2 cells of Escherichia coli from patients with diarrhea. J Clin Microbiol 28, 882–885.
    [Google Scholar]
  65. Vu Nguyen, T., Le Van, P., Le Huy, C., Nguyen Gia, K. & Weintraub, A. ( 2006; ). Etiology and epidemiology of diarrhea in children in Hanoi, Vietnam. Int J Infect Dis 10, 298–308.[CrossRef]
    [Google Scholar]
  66. Wanke, C. A., Cronan, S., Goss, C., Chadee, K. & Guerrant, R. L. ( 1990; ). Characterization of binding of Escherichia coli strains which are enteropathogens to small-bowel mucin. Infect Immun 58, 794–800.
    [Google Scholar]
  67. Wanke, C. A., Schorling, J. B., Barrett, L. J., Desouza, M. A. & Guerrant, R. L. ( 1991; ). Potential role of adherence traits of Escherichia coli in persistent diarrhea in an urban Brazilian slum. Pediatr Infect Dis J 10, 746–751.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.46930-0
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