Advances in Clinical and Experimental Medicine

Title abbreviation: Adv Clin Exp Med
5-Year IF – 2.0, IF – 1.9, JCI (2024) – 0.43
Scopus CiteScore – 4.3
Q1 in SJR 2024, SJR score – 0.598, H-index: 49 (SJR)
ICV – 161.00; MNiSW – 70 pts
Initial editorial assessment and first decision within 24 h

ISSN 1899–5276 (print), ISSN 2451-2680 (online)
Periodicity – monthly

Download original text (EN)

Advances in Clinical and Experimental Medicine

2019, vol. 28, nr 7, July, p. 899–905

doi: 10.17219/acem/94149

Publication type: original article

Language: English

Download citation:

  • BIBTEX (JabRef, Mendeley)
  • RIS (Papers, Reference Manager, RefWorks, Zotero)

The prevalence of mucosa-associated diffusely adherent Escherichia coli in children with inflammatory bowel disease

Urszula Walczuk1,B,C, Beata Sobieszczańska1,A,C,D, Michał Turniak1,B, Marta Rzeszutko1,2,B, Anna Duda-Madej1,B, Barbara Iwańczak1,3,E

1 Department of Microbiology, Wroclaw Medical University, Poland

2 Department of Pathomorphology, Wroclaw Medical University, Poland

3 Department and Clinic of Pediatrics, Gastroenterology and Nutrition, Wroclaw Medical University, Poland

Abstract

Background. The relationship of diffusely adherent Escherichia coli (DAEC) with pediatric inflammatory bowel disease (IBD) has not been previously studied. Diffusely adherent E. coli are a common cause of long-lasting childhood diarrhea and we postulated that they may induce inflammation of the intestinal mucosa, contributing to the development of IBD in susceptible children.
Objectives. The aim of the study was to investigate the relationship between DAEC and pediatric IBD, including Crohn’s disease (CD) and ulcerative colitis (UC). Diffusely adherent E. coli isolates were also assessed regarding their pathogenicity.
Material and Methods. Diffusely adherent E. coli were screened among 130 E. coli strains isolated from intestinal biopsy specimens from 26 children with IBD using polymerase chain reaction (PCR) with primers specific to the pathotype and adherence assays to HEp-2 cells. Diffusely adherent E. coli were further analyzed for their ability to adhere to and invade polarized Caco-2 cells. The immunomodulatory effect of DAEC on the secretion of tumor necrosis factor α (TNF-α) by human monocyte-derived macrophages (MDM) was assessed using an immunoenzymatic assay.
Results. Diffusely adherent E. coli were recovered from 18 (69.2%) of the 26 intestinal biopsy specimens from both CD and UC patients. Most DAEC isolates carried AfaE3 adhesin, adhered to and were internalized by Caco-2 cells, and induced secretion of elevated levels of TNF-α.
Conclusion. The study demonstrated the internalization of DAEC by intestinal epithelial cells and their ability to induce secretion of increased level of TNF-α in a Caco-2/macrophage compartmentalized culture. This indicated that the pathovar should be considered a pathobiont inducing inflammation of the intestinal mucosa in pediatric patients with IBD.

Key words

childhood inflammatory bowel disease, diffusely adherent E. coli, AfaE3 adhesin

References (28)

  1. De Souza H, Fiocchi C. Immunopathogenesis of IBD: Current state of art. Nat Rev Gastroenterol Hepatol. 2016;13(1):13–27.
  2. Zhang Y-Z, Li Y-Y. Inflammatory bowel disease: Pathogenesis. World J Gastroenterol. 2014;20(1):91–99.
  3. Watts DA, Satsangi J. The genetic jigsaw of inflammatory bowel disease. Gut. 2002;50(Suppl 3):31–36.
  4. Darfeuille-Michaud A, Boudeau J, Bulois P, et al. High prevalence of adherent–invasive Escherichia coli associated with ileal mucosa in Crohn’s disease. Gastroenterology. 2004;127(2):412–421.
  5. Kotlowski R, Bernstein CN, Sepehris S, Krause DO. High prevalence of Escherichia coli belonging to the B2+D phylogenetic group in inflammatory bowel disease. Gut. 2007;56(5):669–675.
  6. Conte MP, Schippa S, Zamboni I, et al. Gut-associated bacterial microbiota in pediatric patients with inflammatory bowel disease. Gut. 2000;55(12):1760–1767.
  7. Prorok-Hamon M, Friswell MK, Alswied A, et al. Colonic mucosa-associated diffusely adherent afaC+ Escherichia coli expressing lpfA and pks are increased in inflammatory bowel disease and colon cancer. Gut. 2014;63(5):761–770. doi:10.1136/gutjnl-2013-304739
  8. Servin AL. Pathogenesis of human diffusely adhering Escherichia coli expressing Afa/Dr adhesins (Afa/Dr DAEC): Current insights and future challenges. Clin Microbiol Rev. 2014;27(4):823–869.
  9. Le Bougenec C, Servin AL. Diffusely adherent Escherichia coli strains expressing Afa/Dr adhesins (Afa/Dr DAEC): Hitherto unrecognized pathogens. FEMS Microbiol Lett. 2006;256(2):185–194. doi:10.1111/j.1574-6968.2006.00144
  10. Nowicki B, Selvarangan R, Nowicka S. Family of Escherichia coli Dr adhesins: Decay-accelerating factor receptor recognition and invasiveness. J Infect Dis. 2001;183(Suppl 1):24–27.
  11. Guignot J, Bernet-Camard M-F, Poüs C, Plancon L, Le Bougenec C, Servin AL. Polarized entry of uropathogenic Afa/Dr diffusely adhering Escherichia coli strain IH11128 into human epithelial cells: Evidence for α5b1 integrin recognition and subsequent internalization through a pathway involving caveolae and dynamic unstable microtubules. Infect Immun. 2001;69(3):1856–1868.
  12. Garcia MJ, Jouve M, Nataro JP, Gounon P, Le Bougenec C. Characterization of the Afa-like family of invasions encoded by pathogenic Escherichia coli associated with intestinal and extra-intestinal infections. FEBS Lett. 2000;479:111–117.
  13. Bernet-Camard MF, Coconnier MH, Hudault S, Servin AL. Pathogenicity of the diffusely adhering strain Escherichia coli C1845: F1845 adhesin-decay accelerating factor interaction, brush border microvillus injury, and actin assembly in cultured human intestinal epithelial cells. Infect Immun. 1996;64(6):1918–1928.
  14. Le Bougenec C, Lalioui L, Du Merle L, et al. Characterization of AfaE adhesins produced by extraintestinal and intestinal human Escherichia coli isolates: PCR assays for detection of Afa adhesins that do or do not recognize Dr blood group antigen. J Clin Microbiol. 2001;39(5):1738–1745.
  15. Clermont O, Bonacorsi S, Bingen E. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol. 2000;66(10):4555–4558.
  16. Cravioto A, Tello A, Navarro A, et al. Association of Escherichia coli HEp-2 adherence patterns with type and duration of diarrhea. Lancet. 1991;337(8736):262–264.
  17. Geboes K, Riddell R, Ost A, Jensfelt B, Persson T, Löfberg R. A reproducible grading scale for histological assessment of inflammation in ulcerative colitis. Gut. 2000;47(3):404–409.
  18. Martinez-Medina M, Denizot J, Dreux N, et al. Western diet induces dysbiosis with increased E. coli in CEABAC10 mice, alters host barrier function favoring AIEC colonization. Gut. 2014;63(1):116–124.
  19. Mansan-Almeida R, Pereira AL, Giuglano LG. Diffusely adherent Escherichia coli strains isolated from children and adults constitute two different populations. BMC Microbiol. 2013;13:22. doi:10.1186/1471-2180-13-22
  20. Zhang L, Foxman B, Tallman P, Cladera E, Le Bougenec C, Marrs CF. Distribution of drb genes coding for Dr adhesins among uropathogenic and fecal Escherichia coli isolates and identification of new subtypes. Infect Immun. 1997;65(6):2011–2018.
  21. Jouve M, Garcia MI, Courcoux P, Labigne A, Gounon P, Le Bougenec C. Adhesion to and invasion of HeLa cells by pathogenic Escherichia coli carrying the afa-3 gene cluster are mediated by the AfaE and AfaD proteins, respectively. Infect Immun. 1997;65(10):4082–4089.
  22. Tchoupa AK, Schuhmacher T, Hauck CR. Signaling by epithelial members of the CEACAM family-mucosal docking sites for pathogenic bacteria. Cell Commun Signal. 2014;12:27.doi:10.1186/1478-811X-12-27
  23. Tieng V, Le Bougenec C, Du Merle L, et al. Binding of Escherichia coli adhesin AfaE to CD55 triggers cell-surface expression of the MHC class I-related molecule MICA. Proc Natl Acad Sci U S A. 2002;99(5):2977–2982.
  24. Rhoda G, Dahan S, Mezzanotte L, et al. The defect in CEACAM family member expression in Crohn’s disease IECs is regulated by the transcription factor SOX9. Inflamm Bowel Dis. 2009;15(12):1775–1783.
  25. Nasu J, Mizuno M, Uesu T, et al. Cytokine-stimulated release of decay-accelerating factor (DAF; CD55) from HT-29 human intestinal epithelial cells. Clin Exp Immunol. 1998;113(3):379–385.
  26. Betis F, Brest P, Hofman V, et al. The Afa/Dr adhesins of diffusely adhering Escherichia coli stimulate interleukin-8 secretion, activate mitogen-activated protein kinases, and promote polymorphonuclear transepithelial migration in T84 polarized epithelial cells. Infect Immun. 2003;71(3):1068–1074.
  27. Levin A, Shibolet O. Infliximab in ulcerative colitis. Biologics. 2008;2(3):379–388.
  28. Garrity-Park MM, Loftus FV, Bryant SC, Sandborn WJ, Smyrk TC. Tumor necrosis factor-alpha polymorphisms in ulcerative colitis-associated colorectal cancer. Am J Gastroenterol. 2008;103(2):407– 415.
© Wroclaw Medical University