Prevalence of enteroaggregative Escherichia coli and its virulence-related genes in a case-control study among children from north-eastern Brazil

Journal of Medical Microbiology

Volumn 62, Issue PART5, 2013, Pages 683-693

  Lima, Ila Fernanda Nunes ^a   Boisen, Nadia ^b   Da Silva Quetz, Josiane ^a   Havt, Alexandre ^a   De Carvalho, Eunice Bobo ^a   Soares, Alberto Melo ^a   Lima, Noélia Leal ^a   Mota, Rosa Maria Salani ^a   Nataro, James P ^b   Guerrant, Richard Littleton ^a   Lima, Aldo Ângelo Moreira ^a  

^a FEDERAL UNIVERSITY OF CEARÁ   (Brazil)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEMOLYSIN; PILIN;

ARTICLE; BACTERIAL GENE; BACTERIAL VIRULENCE; BRAZIL; CASE CONTROL STUDY; CHILD; COMPARATIVE STUDY; CONTROLLED STUDY; DIARRHEA; ENTEROAGGREGATIVE ESCHERICHIA COLI; FECES ANALYSIS; FEMALE; GENOTYPE; HOUSEHOLD; HUMAN; INFANT; MAJOR CLINICAL STUDY; MALE; MULTIPLEX POLYMERASE CHAIN REACTION; PATHOGENESIS; PRESCHOOL CHILD; PREVALENCE; PRIORITY JOURNAL;

EID: 84876532264     PISSN: 00222615     EISSN: None     Source Type: Journal    
DOI: 10.1099/jmm.0.054262-0     Document Type: Article

References (74)

1. 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.
2. Benjelloun-Touimi, Z., Sansonetti, P. J. & Parsot, C. (1995). SepA, the major extracellular protein of Shigella flexneri: autonomous secretion and involvement in tissue invasion. Mol Microbiol 17, 123-135.
3. Bernier, C., Gounon, P. & Le Bouguénec, 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.
4. Betancourt-Sanchez, M. & Navarro-Garcia, F. (2009). Pet secretion, internalization and induction of cell death during infection of epithelial cells by enteroaggregative Escherichia coli. Microbiology 155, 2895-2906.
5. Boisen, N., Struve, C., Scheutz, F., Krogfelt, K. A. & Nataro, J. P. (2008). New adhesin of enteroaggregative Escherichia coli related to the Afa/Dr/AAF family. Infect Immun 76, 3281-3292.
6. 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.
7. Boisen, N., Scheutz, F., Rasko, D. A., Redman, J. C., Persson, S., Simon, J., Kotloff, K. L., Levine, M. M., Sow, S. & other authors (2012). Genomic characterization of enteroaggregative Escherichia coli from children in Mali. J Infect Dis 205, 431-444.
8. Bouzari, S., Jafari, A. & Zarepour, M. (2005). Distribution of virulence related genes among enteroaggregative Escherichia coli isolates: using multiplex PCR and hybridization. Infect Genet Evol 5, 79-83.
9. Bueris, V., Sircili, M. P., Taddei, C. R., dos Santos, M. F., Franzolin, M. R., Martinez, M. B., Ferrer, S. R., Barreto, M. L. & Trabulsi, L. R. (2007). Detection of diarrheagenic Escherichia coli from children with and without diarrhea in Salvador, Bahia, Brazil. Mem Inst Oswaldo Cruz 102, 839-844.
10. Carvalho, E. B., Maga, E. A., Quetz, J. S., Lima, I. F. N., Magalhães, H. Y. F., Rodrigues, F. A. R., Silva, A. V. A., Prata, M. M. G., Cavalcante, P. A. & other authors (2012). Goat milk with and without increased concentrations of lysozyme improves repair of intestinal cell damage induced by enteroaggregative Escherichia coli. BMC Gastroenterol 12, 106.
11. 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.
12. 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.
13. Chaudhuri, R. R., Sebaihia, M., Hobman, J. L., Webber, M. A., Leyton, D. L., Goldberg, M. D., Cunningham, A. F., Scott-Tucker, A., Ferguson, P. R. & other authors (2010). Complete genome sequence and comparative metabolic profiling of the prototypical enteroaggregative Escherichia coli strain 042. PLoS ONE 5, e8801.
14. Clermont, O., Bonacorsi, S. & Bingen, E. (2000). Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 66, 4555-4558.
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.
16. Czeczulin, J. R., Balepur, S., Hicks, S., Phillips, A., Hall, R., Kothary, M. H., Navarro-Garcia, F. & Nataro, J. P. (1997). Aggregative adherence fimbria II, a second fimbrial antigen mediating aggregative adherence in enteroaggregative Escherichia coli. Infect Immun 65, 4135-4145.
17. 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.
18. da Silva Quetz, J., Lima, I. F. N., Havt, A., de Carvalho, E. B., Lima, N. L., Soares, A. M., Mota, R. M. S., Guerrant, R. L. & Lima, A. A. M. (2010). Campylobacter jejuni and Campylobacter coli in children from communities in Northeastern Brazil: molecular detection and relation to nutritional status. Diagn Microbiol Infect Dis 67, 220-227.
19. Dudley, E. G., Thomson, N. R., Parkhill, J., Morin, N. P. & Nataro, J. P. (2006). Proteomic and microarray characterization of the AggR regulon identifies a pheU pathogenicity island in enteroaggregative Escherichia coli. Mol Microbiol 61, 1267-1282.
20. Estrada-Garcia, T. & Navarro-Garcia, F. (2012). Enteroaggregative Escherichia coli pathotype: a genetically heterogeneous emerging foodborne enteropathogen. FEMS Immunol Med Microbiol 66, 281- 298.
21. Façanha, M. C. & Pinheiro, A. C. (2005). Acute diarrhea treated by health care services in Fortaleza, Ceará State, Brazil, from 1996 to 2001. Cad Saude Publica 21, 49-54 (in Portuguese).
22. Frank, C., Werber, D., Cramer, J. P., Askar, M., Faber, M., an der Heiden, M., Bernard, H., Fruth, A., Prager, R. & other authors (2011). Epidemic profile of Shiga-toxin-producing Escherichia coli O104:H4 outbreak in Germany. N Engl J Med 365, 1771-1780.
23. Fujiyama, R., Nishi, J., Imuta, N., Tokuda, K., Manago, K. & Kawano, Y. (2008). The shf gene of a Shigella flexneri homologue on the virulent plasmid pAA2 of enteroaggregative Escherichia coli 042 is required for firm biofilm formation. Curr Microbiol 56, 474-480.
24. Guerrant, R. L., Van Gilder, T., Steiner, T. S., Thielman, N. M., Slutsker, L., Tauxe, R. V., Hennessy, T., Griffin, P. M., DuPont, H. & other authors (2001). Practice guidelines for the management of infectious diarrhea. Clin Infect Dis 32, 331-351.
25. Guyer, D. M., Henderson, I. R., Nataro, J. P. & Mobley, H. L. (2000). Identification of sat, an autotransporter toxin produced by uropathogenic Escherichia coli. Mol Microbiol 38, 53-66.
26. Harrington, S. M., Sheikh, J., Henderson, I. R., Ruiz-Perez, F., Cohen, P. S. & Nataro, J. P. (2009). The Pic protease of enteroaggregative Escherichia coli promotes intestinal colonization and growth in the presence of mucin. Infect Immun 77, 2465-2473.
27. 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.
28. Huang, D. B., Nataro, J. P., DuPont, H. L., Kamat, P. P., Mhatre, A. D., Okhuysen, P. C. & Chiang, T. (2006). Enteroaggregative Escherichia coli is a cause of acute diarrheal illness: a meta-analysis. Clin Infect Dis 43, 556-563.
29. Huang, D. B., Mohamed, J. A., Nataro, J. P., DuPont, H. L., Jiang, Z. D. & Okhuysen, P. C. (2007). Virulence characteristics and the molecular epidemiology of enteroaggregative Escherichia coli isolates from travellers to developing countries. J Med Microbiol 56, 1386-1392.
30. 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.
31. Kaper, J. B., Nataro, J. P. & Mobley, H. L. T. (2004). Pathogenic Escherichia coli. Nat Rev Microbiol 2, 123-140.
32. Kermani, N. A., Jafari, F., Mojarad, H. N., Hoseinkhan, N. & Zali, R. (2010). Prevalence and associated factors of persistent diarrhoea in Iranian children admitted to a paediatric hospital. East Mediterr Health J 16, 831-836.
33. Keusch, G. T., Fontaine, O., Bhargava, A., Boschi-Pinto, C., Bhutta, Z. A., Gotuzzo, E., Rivera, J., Chow, J., Shahid-Salles, S. A. & Laxminarayan, R. (2006). Diarrheal diseases. In Disease Control Priorities in Developing Countries, 2nd edn, pp. 371-387. Edited by D. T. Jamison, J. G. Breman, A. R. Measham, G. Alleyne, M. Claeson, D. B. Evans, P. Jha, A. Mills & P. Musgrov. New York: Oxford University Press.
34. Levine, M. M., Bergquist, E. J., Nalin, D. R., Waterman, D. H., Hornick, R. B., Young, C. R. & Sotman, S. (1978). Escherichia coli strains that cause diarrhoea but do not produce heat-labile or heat-stable enterotoxins and are non-invasive. Lancet 1, 1119-1122.
35. Lima, A. A. M., Moore, S. R., Barboza, M. S., Jr, Soares, A. M., Schleupner, M. A., Newman, R. D., Sears, C. L., Nataro, J. P., Fedorko, D. P. & other authors (2000). Persistent diarrhea signals a critical period of increased diarrhea burdens and nutritional shortfalls: a prospective cohort study among children in northeastern Brazil. J Infect Dis 181, 1643-1651.
36. 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.
37. Meng, C. Y., Smith, B. L., Bodhidatta, L., Richard, S. A., Vansith, K., Thy, B., Srijan, A., Serichantalergs, O. & Mason, C. J. (2011). Etiology of diarrhea in young children and patterns of antibiotic resistance in Cambodia. Pediatr Infect Dis J 30, 331-335.
38. Mohamed, J. A., Huang, D. B., Jiang, Z. D., DuPont, H. L., Nataro, J. P., Belkind-Gerson, J. & Okhuysen, P. C. (2007). Association of putative enteroaggregative Escherichia coli virulence genes and biofilm production in isolates from travelers to developing countries. J Clin Microbiol 45, 121-126.
39. Morin, N., Tirling, C., Ivison, S. M., Kaur, A. P., Nataro, J. P. & Steiner, T. S. (2010). Autoactivation of the AggR regulator of enteroaggregative Escherichia coli in vitro and in vivo. FEMS Immunol Med Microbiol 58, 344-355.
40. Muniesa, M., Hammerl, J. A., Hertwig, S., Appel, B. & Brüssow, H. (2012). Shiga toxin-producing Escherichia coli O104:H4:a new challenge for microbiology. Appl Environ Microbiol 78, 4065-4073.
41. Nataro, J. P. & Kaper, J. B. (1998). Diarrheagenic Escherichia coli. Clin Microbiol Rev 11, 142-201.
42. Nataro, J. P., Baldini, M. M., Kaper, J. B., Black, R. E., Bravo, N. & Levine, M. M. (1985). Detection of an adherence factor of enteropathogenic Escherichia coli with a DNA probe. J Infect Dis 152, 560-565.
43. 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.
44. 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.
45. Nataro, J. P., Mai, V., Johnson, J., Blackwelder, W. C., Heimer, R., Tirrell, S., Edberg, S. C., Braden, C. R., Glenn Morris, J., Jr & Hirshon, J. M. (2006). Diarrheagenic Escherichia coli infection in Baltimore, Maryland, and New Haven, Connecticut. Clin Infect Dis 43, 402- 407.
46. Navarro-García, F., Eslava, C., Villaseca, J. M., López-Revilla, R., Czeczulin, J. R., Srinivas, S., Nataro, J. P. & Cravioto, A. (1998). In vitro effects of a high-molecular-weight heat-labile enterotoxin from enteroaggregative Escherichia coli. Infect Immun 66, 3149-3154.
47. Nishi, J., Sheikh, J., Mizuguchi, K., Luisi, B., Burland, V., Boutin, A., Rose, D. J., Blattner, F. R. & Nataro, J. P. (2003). The export of coat protein from enteroaggregative Escherichia coli by a specific ATPbinding cassette transporter system. J Biol Chem 278, 45680-45689.
48. Ochoa, T. J., Mercado, E. H., Durand, D., Rivera, F. P., Mosquito, S., Contreras, C., Riveros, M., Lluque, A., Barletta, F. & other authors (2011). Frequency and pathotypes of diarrheagenic Escherichia coli in Peruvian children with and without diarrhea. Rev Peru Med Exp Salud Publica 28, 13-20 (in Spanish).
49. Okeke, I. N. & Nataro, J. P. (2001). Enteroaggregative Escherichia coli. Lancet Infect Dis 1, 304-313.
50. Okeke, I. N., Lamikanra, A., Czeczulin, J., Dubovsky, F., Kaper, J. B. & Nataro, J. P. (2000). Heterogeneous virulence of enteroaggregative Escherichia coli strains isolated from children in Southwest Nigeria. J Infect Dis 181, 252-260.
51. Olesen, B., Neimann, J., Böttiger, B., Ethelberg, S., Schiellerup, P., Jensen, C., Helms, M., Scheutz, F., Olsen, K. E. P. & other authors (2005). Etiology of diarrhea in young children in Denmark: a casecontrol study. J Clin Microbiol 43, 3636-3641.
52. Opintan, J. A., Newman, M. J., Ayeh-Kumi, P. F., Affrim, R., Gepi--Attee, R., Sevilleja, J. E. A. D., Roche, J. K., Nataro, J. P., Warren, C. A. & Guerrant, R. L. (2010). Pediatric diarrhea in southern Ghana: etiology and association with intestinal inflammation and malnutrition. Am J Trop Med Hyg 83, 936-943.
53. Paschke, C., Apelt, N., Fleischmann, E., Perona, P., Walentiny, C., Löscher, T. & Herbinger, K.-H. (2011). Controlled study on enteropathogens in travellers returning from the tropics with and without diarrhoea. Clin Microbiol Infect 17, 1194-1200.
54. Pereira, A. L., Ferraz, L. R., Silva, R. S. & Giugliano, L. G. (2007). Enteroaggregative Escherichia coli virulence markers: positive association with distinct clinical characteristics and segregation into 3 enteropathogenic E. coli serogroups. J Infect Dis 195, 366-374.
55. Piva, I. C., Pereira, A. L., Ferraz, L. R., Silva, R. S. N., Vieira, A. C., Blanco, J. E., Blanco, M., Blanco, J. & Giugliano, L. G. (2003). Virulence markers of enteroaggregative Escherichia coli isolated from children and adults with diarrhea in Brasília, Brazil. J Clin Microbiol 41, 1827-1832.
56. Rajakumar, K., Sasakawa, C. & Adler, B. (1997). Use of a novel approach, termed island probing, identifies the Shigella flexneri she pathogenicity island which encodes a homolog of the immunoglobulin A protease-like family of proteins. Infect Immun 65, 4606-4614.
57. Regua-Mangia, A. H., Gomes, T. A. T., Vieira, M. A. M., Irino, K. & Teixeira, L. M. (2009). Molecular typing and virulence of enteroaggregative Escherichia coli strains isolated from children with and without diarrhoea in Rio de Janeiro city, Brazil. J Med Microbiol 58, 414-422.
58. Restieri, C., Garriss, G., Locas, M. C. & Dozois, C. M. (2007). Autotransporter-encoding sequences are phylogenetically distributed among Escherichia coli clinical isolates and reference strains. Appl Environ Microbiol 73, 1553-1562.
59. Roche, J. K., Cabel, A., Sevilleja, J., Nataro, J. P. & Guerrant, R. L. (2010). Enteroaggregative Escherichia coli (EAEC) impairs growth while malnutrition worsens EAEC infection: a novel murine model of the infection malnutrition cycle. J Infect Dis 202, 506-514.
60. Rúgeles, L. C., Bai, J., Martínez, A. J., Vanegas, M. C. & Gómez--Duarte, O. G. (2010). Molecular characterization of diarrheagenic Escherichia coli strains from stools samples and food products in Colombia. Int J Food Microbiol 138, 282-286.
61. Samie, A., Obi, C. L., Dillingham, R., Pinkerton, R. C. & Guerrant, R. L. (2007). Enteroaggregative Escherichia coli in Venda, South Africa: distribution of virulence-related genes by multiplex polymerase chain reaction in stool samples of human immunodeficiency virus (HIV)--positive and HIV-negative individuals and primary school children. Am J Trop Med Hyg 77, 142-150.
62. Sarantuya, J., Nishi, J., Wakimoto, N., Erdene, S., Nataro, J. P., Sheikh, J., Iwashita, M., Manago, K., Tokuda, K. & other authors (2004). Typical enteroaggregative Escherichia coli is the most prevalent pathotype among E. coli strains causing diarrhea in Mongolian children. J Clin Microbiol 42, 133-139.
63. Savarino, S. J., Fasano, A., Watson, J., Martin, B. M., Levine, M. M., Guandalini, S. & Guerry, P. (1993). Enteroaggregative Escherichia coli heat-stable enterotoxin 1 represents another subfamily of E. coli heatstable toxin. Proc Natl Acad Sci U S A 90, 3093-3097.
64. Scaletsky, I. C., Fabbricotti, S. H., Silva, S. O., Morais, M. B. & Fagundes-Neto, U. (2002). HEp-2-adherent Escherichia coli strains associated with acute infantile diarrhea, São Paulo, Brazil. Emerg Infect Dis 8, 855-858.
65. Scavia, G., Staffolani, M., Fisichella, S., Striano, G., Colletta, S., Ferri, G., Escher, M., Minelli, F. & Caprioli, A. (2008). Enteroaggregative Escherichia coli associated with a foodborne outbreak of gastroenteritis. J Med Microbiol 57, 1141-1146.
66. Scheutz, F., Nielsen, E. M., Frimodt-Møller, J., Boisen, N., Morabito, S., Tozzoli, R., Nataro, J. P. & Caprioli, A. (2011). Characteristics of the enteroaggregative Shiga toxin/verotoxin-producing Escherichia coli O104:H4 strain causing the outbreak of haemolytic uraemic syndrome in Germany, May to June 2011. Euro Surveill 16, 19889. http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=19889
67. 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.
68. Sheikh, J., Czeczulin, J. R., Harrington, S., Hicks, S., Henderson, I. R., Le Bouguénec, C., Gounon, P., Phillips, A. & Nataro, J. P. (2002). A novel dispersin protein in enteroaggregative Escherichia coli. J Clin Invest 110, 1329-1337.
69. Sheikh, J., Dudley, E. G., Sui, B., Tamboura, B., Suleman, A. & Nataro, J. P. (2006). EilA, a HilA-like regulator in enteroaggregative Escherichia coli. Mol Microbiol 61, 338-350.
70. Steiner, T. S., Lima, A. A. M., Nataro, J. P. & Guerrant, R. L. (1998). Enteroaggregative Escherichia coli produce intestinal inflammation and growth impairment and cause interleukin-8 release from intestinal epithelial cells. J Infect Dis 177, 88-96.
71. Steiner, T. S., Samie, A. & Guerrant, R. L. (2006). Infectious diarrhea: new pathogens and new challenges in developed and developing areas. Clin Infect Dis 43, 408-410.
72. Strauman, M. C., Harper, J. M., Harrington, S. M., Boll, E. J. & Nataro, J. P. (2010). Enteroaggregative Escherichia coli disrupts epithelial cell tight junctions. Infect Immun 78, 4958-4964.
73. Usein, C. R., Tatu-Chitoiu, D., Ciontea, S., Condei, M. & Damian, M. (2009). Escherichia coli pathotypes associated with diarrhea in Romanian children younger than 5 years of age. Jpn J Infect Dis 62, 289-293.
74. Wright, P. A. & Wynford-Thomas, D. (1990). The polymerase chain reaction: miracle or mirage? A critical review of its uses and limitations in diagnosis and research. J Pathol 162, 99-117.