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. 1992 Nov;60(11):4793–4800. doi: 10.1128/iai.60.11.4793-4800.1992

Pathogen and host differences in bacterial adherence to human buccal epithelial cells in a northeast Brazilian community.

B L Walser 1, R D Newman 1, A A Lima 1, R L Guerrant 1
PMCID: PMC258233  PMID: 1398990

Abstract

The adherence of several strains of Escherichia coli to human buccal epithelial cells was studied, using cells obtained from five groups: healthy adults, healthy children, children with acute diarrhea, children with persistent diarrhea associated with cryptosporidial parasites, and children with noncryptosporidial persistent diarrhea. All groups lived or worked in an urban slum in northeastern Brazil. Samples of buccal epithelial cells from subjects in each of these groups were incubated with wild-type E. coli K-12 (strain C600), the enteroaggregative E. coli strains 17-2 and PDAS 30-5, CFA/II-positive E. coli 1392+ and its plasmid-cured derivative 1392-, and hydrophobic E. coli 132-3. Samples were evaluated microscopically to determine background contamination and the percentage of cells with more than 15% of their surface area obscured by adherent bacteria after incubation and washing. The assay was tested under field conditions and was shown to produce reliable and consistent results. Both enteroaggregative strains of E. coli were shown to adhere to a significantly higher percentage of all groups of human buccal epithelial cells than any of the other tested strains. In addition, buccal epithelial cells from children with nonparasitic persistent diarrhea showed substantially more bacterial adherence in both the native state and with all tested strains of E. coli than did cells from children with persistent cryptosporidial diarrhea or acute diarrhea or from healthy controls. This study provides evidence that enteroaggregative strains of E. coli demonstrate increased adherence to human buccal epithelial cells (as well as to cultured HEp-2 cells) and that buccal epithelial cells from children with noncryptosporidial persistent diarrhea appear to be more susceptible to bacterial adherence and colonization than buccal epithelial cells from control groups. These findings suggest that host differences as well as pathogen differences are important in the pathogenesis of persistent diarrhea and have implications for a potential role for buccal epithelial cell analysis in the diagnosis or risk stratification of children susceptible to noncryptosporidial persistent diarrhea.

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Selected References

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  1. Baldwin T. J., Brooks S. F., Knutton S., Manjarrez Hernandez H. A., Aitken A., Williams P. H. Protein phosphorylation by protein kinase C in HEp-2 cells infected with enteropathogenic Escherichia coli. Infect Immun. 1990 Mar;58(3):761–765. doi: 10.1128/iai.58.3.761-765.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bhan M. K., Khoshoo V., Sommerfelt H., Raj P., Sazawal S., Srivastava R. Enteroaggregative Escherichia coli and Salmonella associated with nondysenteric persistent diarrhea. Pediatr Infect Dis J. 1989 Aug;8(8):499–502. doi: 10.1097/00006454-198908000-00005. [DOI] [PubMed] [Google Scholar]
  3. Bhan M. K., Raj P., Levine M. M., Kaper J. B., Bhandari N., Srivastava R., Kumar R., Sazawal S. Enteroaggregative Escherichia coli associated with persistent diarrhea in a cohort of rural children in India. J Infect Dis. 1989 Jun;159(6):1061–1064. doi: 10.1093/infdis/159.6.1061. [DOI] [PubMed] [Google Scholar]
  4. Black R. E., Brown K. H., Becker S. Effects of diarrhea associated with specific enteropathogens on the growth of children in rural Bangladesh. Pediatrics. 1984 Jun;73(6):799–805. [PubMed] [Google Scholar]
  5. Black R. E., Brown K. H., Becker S. Malnutrition is a determining factor in diarrheal duration, but not incidence, among young children in a longitudinal study in rural Bangladesh. Am J Clin Nutr. 1984 Jan;39(1):87–94. doi: 10.1093/ajcn/39.1.87. [DOI] [PubMed] [Google Scholar]
  6. Brown A. T., Sims R. E., Raybould T. P., Lillich T. T., Henslee P. J., Ferretti G. A. Oral gram-negative bacilli in bone marrow transplant patients given chlorhexidine rinses. J Dent Res. 1989 Jul;68(7):1199–1204. doi: 10.1177/00220345890680071101. [DOI] [PubMed] [Google Scholar]
  7. Candy D. C., Leung T. S., Marshall W. C., Harries J. T. Increased adhesion of Escherichia coli to mucosal cells from infants with protracted diarrhoea: a possible factor in the pathogenesis of bacterial overgrowth and diarrhoea. Gut. 1983 Jun;24(6):538–541. doi: 10.1136/gut.24.6.538. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cravioto A., Reyes R. E., Trujillo F., Uribe F., Navarro A., De La Roca J. M., Hernández J. M., Pérez G., Vázquez V. Risk of diarrhea during the first year of life associated with initial and subsequent colonization by specific enteropathogens. Am J Epidemiol. 1990 May;131(5):886–904. doi: 10.1093/oxfordjournals.aje.a115579. [DOI] [PubMed] [Google Scholar]
  9. Cravioto A., Tello A., Navarro A., Ruiz J., Villafán H., Uribe F., Eslava C. Association of Escherichia coli HEp-2 adherence patterns with type and duration of diarrhoea. Lancet. 1991 Feb 2;337(8736):262–264. doi: 10.1016/0140-6736(91)90868-p. [DOI] [PubMed] [Google Scholar]
  10. Ertel A., Eng R., Smith S. M. The differential effect of cigarette smoke on the growth of bacteria found in humans. Chest. 1991 Sep;100(3):628–630. doi: 10.1378/chest.100.3.628. [DOI] [PubMed] [Google Scholar]
  11. Fujita K., Yamamoto T., Kitagawa R. Binding sites for P and/or type 1-piliated Escherichia coli in human ureter. J Urol. 1991 Jul;146(1):217–222. doi: 10.1016/s0022-5347(17)37755-8. [DOI] [PubMed] [Google Scholar]
  12. Guerrant R. L., Kirchhoff L. V., Shields D. S., Nations M. K., Leslie J., de Sousa M. A., Araujo J. G., Correia L. L., Sauer K. T., McClelland K. E. Prospective study of diarrheal illnesses in northeastern Brazil: patterns of disease, nutritional impact, etiologies, and risk factors. J Infect Dis. 1983 Dec;148(6):986–997. doi: 10.1093/infdis/148.6.986. [DOI] [PubMed] [Google Scholar]
  13. Hooton T. M., Fennell C. L., Clark A. M., Stamm W. E. Nonoxynol-9: differential antibacterial activity and enhancement of bacterial adherence to vaginal epithelial cells. J Infect Dis. 1991 Dec;164(6):1216–1219. doi: 10.1093/infdis/164.6.1216. [DOI] [PubMed] [Google Scholar]
  14. McAuliffe J. F., Shields D. S., Auxiliadora de Sousa M., Sakell J., Schorling J., Guerrant R. L. Prolonged and recurring diarrhea in the northeast of Brazil: examination of cases from a community-based study. J Pediatr Gastroenterol Nutr. 1986 Nov-Dec;5(6):902–906. doi: 10.1097/00005176-198611000-00014. [DOI] [PubMed] [Google Scholar]
  15. Myers L. L., Shoop D. S., Stackhouse L. L., Newman F. S., Flaherty R. J., Letson G. W., Sack R. B. Isolation of enterotoxigenic Bacteroides fragilis from humans with diarrhea. J Clin Microbiol. 1987 Dec;25(12):2330–2333. doi: 10.1128/jcm.25.12.2330-2333.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Ofek I., Mirelman D., Sharon N. Adherence of Escherichia coli to human mucosal cells mediated by mannose receptors. Nature. 1977 Feb 17;265(5595):623–625. doi: 10.1038/265623a0. [DOI] [PubMed] [Google Scholar]
  17. Penny M. E., Harendra de Silva D. G., McNeish A. S. Bacterial contamination of the small intestine of infants with enteropathogenic Escherichia coli and other enteric infections: a factor in the aetiology of persistent diarrhoea? Br Med J (Clin Res Ed) 1986 May 10;292(6530):1223–1226. doi: 10.1136/bmj.292.6530.1223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Ramsey B. W., Wentz K. R., Smith A. L., Richardson M., Williams-Warren J., Hedges D. L., Gibson R., Redding G. J., Lent K., Harris K. Predictive value of oropharyngeal cultures for identifying lower airway bacteria in cystic fibrosis patients. Am Rev Respir Dis. 1991 Aug;144(2):331–337. doi: 10.1164/ajrccm/144.2.331. [DOI] [PubMed] [Google Scholar]
  19. Rothbaum R., McAdams A. J., Giannella R., Partin J. C. A clinicopathologic study of enterocyte-adherent Escherichia coli: a cause of protracted diarrhea in infants. Gastroenterology. 1982 Aug;83(2):441–454. [PubMed] [Google Scholar]
  20. Schlager T. A., Wanke C. A., Guerrant R. L. Net fluid secretion and impaired villous function induced by colonization of the small intestine by nontoxigenic colonizing Escherichia coli. Infect Immun. 1990 May;58(5):1337–1343. doi: 10.1128/iai.58.5.1337-1343.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Schorling J. B., Guerrant R. L. Diarrhoea and catch-up growth. Lancet. 1990 Mar 10;335(8689):599–600. doi: 10.1016/0140-6736(90)90378-i. [DOI] [PubMed] [Google Scholar]
  22. Schorling J. B., Wanke C. A., Schorling S. K., McAuliffe J. F., de Souza M. A., Guerrant R. L. A prospective study of persistent diarrhea among children in an urban Brazilian slum. Patterns of occurrence and etiologic agents. Am J Epidemiol. 1990 Jul;132(1):144–156. doi: 10.1093/oxfordjournals.aje.a115626. [DOI] [PubMed] [Google Scholar]
  23. Stenfors L. E., Räisänen S. Age-dependent changes in bacterial adherence to epithelial cells of nasopharynx in vivo. Acta Otolaryngol. 1990 Sep-Oct;110(3-4):292–299. doi: 10.3109/00016489009122551. [DOI] [PubMed] [Google Scholar]
  24. Vial P. A., Robins-Browne R., Lior H., Prado V., Kaper J. B., Nataro J. P., Maneval D., Elsayed A., Levine M. M. Characterization of enteroadherent-aggregative Escherichia coli, a putative agent of diarrheal disease. J Infect Dis. 1988 Jul;158(1):70–79. doi: 10.1093/infdis/158.1.70. [DOI] [PubMed] [Google Scholar]
  25. Wanke C. A., Guerrant R. L. Small-bowel colonization alone is a cause of diarrhea. Infect Immun. 1987 Aug;55(8):1924–1926. doi: 10.1128/iai.55.8.1924-1926.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Wanke C. A., Schorling J. B., Barrett L. J., Desouza M. A., Guerrant R. L. Potential role of adherence traits of Escherichia coli in persistent diarrhea in an urban Brazilian slum. Pediatr Infect Dis J. 1991 Oct;10(10):746–751. doi: 10.1097/00006454-199110000-00006. [DOI] [PubMed] [Google Scholar]
  27. Weikel C. S., Johnston L. I., De Sousa M. A., Guerrant R. L. Cryptosporidiosis in northeastern Brazil: association with sporadic diarrhea. J Infect Dis. 1985 May;151(5):963–965. doi: 10.1093/infdis/151.5.963. [DOI] [PubMed] [Google Scholar]
  28. Zobel G., Kuttnig M., Grubbauer H. M., Semmelrock H. J., Thiel W. Reduction of colonization and infection rate during pediatric intensive care by selective decontamination of the digestive tract. Crit Care Med. 1991 Oct;19(10):1242–1246. doi: 10.1097/00003246-199110000-00005. [DOI] [PubMed] [Google Scholar]

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