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Analysis of Escherichia coli Isolated from Patients Affected by Crohn’s Disease

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Abstract

The etiopathogenesis of Crohn’s disease (CD) is still controversial: several genetic, immunologic, and environmental factors, including some bacteria, have been implicated. This study has been devised to assess the involvement of Escherichia coli in CD. Seven E. coli strains were isolated from 14 biopsies obtained from ileocolic ulcers of patients affected by inflammatory bowel disease (IBD), including six with ulcerative colitis and eight with CD. Five strains, exclusively isolated from CD patients, were found inside mucosal cells. Different PCR techniques (for chuA, yjaA, TspE4.C2, escV, and bfpB genes) were performed and PFGE was carried out to characterize these bacteria in comparison with other E. coli strains isolated from non-IBD specimens. The correlation of these characters with bacterial invasiveness on intestinal (Caco-2) and phagocytic (U937) cells was assessed. Overall our pilot data suggest that five among eight strains isolated from CD patients belonged to the adherent-invasive E. coli (AIEC) group, and were invasive on Caco-2 cells and resistant to phagocytosis. These findings suggest that these bacteria could be considered target organisms whose elimination could reduce the intestinal inflammatory process and CD progression.

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References

  1. Abubakar I, Myhill D, Aliyu SH, Hunter PR (2008) Detection of Mycobacterium avium subsp. paratuberculosis from patients with Crohn’s disease using nucleic acid-based techniques: a systematic review and meta-analysis. Inflam Bowel Dis 14:401–410

    Article  CAS  Google Scholar 

  2. Barnich N, Darfeuille-Michaud A (2007) Role of bacteria in the etiopathogenesis of inflammatory bowel disease. World J Gastroenterol 13:5571–5576

    PubMed  CAS  Google Scholar 

  3. Baumgart DC, Carding SR (2007) Inflammatory bowel disease: cause and immunobiology. Lancet 369:1627–1640

    Article  PubMed  CAS  Google Scholar 

  4. Baumgart M, Dogan B, Rishniw M, Weitzman G, Bosworth B, Yantiss R, Orsi RH, Wiedemann M et al (2007) Culture independent analysis of ileal mucosa reveals a selective increase in invasive Escherichia coli of novel phylogeny relative to depletion of Clostridiales in Crohn’s disease involving the ileum. ISME J 1:403–418

    Article  PubMed  CAS  Google Scholar 

  5. Boudeau J, Glasser A, Masseret E, Joly B, Darfeuille-Michaud A (1999) Invasive ability of an Escherichia coli strain isolated from the ileal mucosa of a patient with Crohn’s disease. Infect Immun 67:4499–4509

    PubMed  CAS  Google Scholar 

  6. Bulois P, Desreumaux P, Neut C, Darfeuille-Michaud A, Cortot A, Colombel JF (1999) Infectious agents and Crohn’s disease. Clin Microbiol Infect 5:601–604

    Article  PubMed  CAS  Google Scholar 

  7. CDCPulseNetUSA (2004) One-day (24–28 h) standardized laboratory protocol for molecular subtyping of Escherichia coli O157:H7, non-typhoidal Salmonella serotypes, and Shigella sonnei by pulsed field gel electrophoresis (PFGE). PulseNet PFGE Manual 5.1–5.3:1–13

    Google Scholar 

  8. Clermont O, Bonacorsi S, Bingen E (2000) Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 66:4555–4558

    Article  PubMed  CAS  Google Scholar 

  9. Darfeuille-Michaud A, Neut C, Barnich N, Lederman E, Di Martino P, Desremaux P, Gambiez L, Joly B, Cortot A, Colombel JF (1998) Presence of adherent Escherichia coli strains in ileal mucosa of patients with Crohn’s disease. Gastroenterology 115:1405–1413

    Article  PubMed  CAS  Google Scholar 

  10. Darfeuille-Michaud A, Boudeau J, Bulois P, Neut C, Glasser A-L, Barnich N, Bringer MA, Swidsinski A, Beaugerie L, Colombel JF (2004) High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn’s disease. Gastroenterology 127:412–421

    Article  PubMed  Google Scholar 

  11. De Hertogh G, Aerssens J, Geboes KP, Geboes K (2008) Evidence for the involvement of infectious agents in the pathogenesis of Crohn’s disease. World J Gastroenterol 14:845–852

    Article  PubMed  Google Scholar 

  12. Dice L (1945) Measures of the amount of ecological association between species. Ecology (New York) 26:297–302

    Google Scholar 

  13. El-Zaatari FA, Naser SA, Hulten K, Burch P, Graham DY (1999) Characterization of Mycobacterium paratuberculosis p36 antigen and its seroreactivities in Crohn’s disease. Curr Microbiol 39:115–119

    Article  PubMed  CAS  Google Scholar 

  14. Fellermann K, Wehkamp J, Herrlinger KR, Stange EF (2003) Crohn’s disease: a defensing deficiency syndrome. Eur J Gastroenterol Hepatol 15:627–634

    Article  PubMed  CAS  Google Scholar 

  15. Gaia E, Pais P, Salacone P, Morello C (2008) Preliminary results obtained with cefoperazone plus corticosteroids in the treatment of active Crohn’s disease. Inflamm Bowel Dis 15:1123–1124

    Article  Google Scholar 

  16. Hanauer SB (2006) Inflammatory bowel disease: epidemiology, pathogenesis, and therapeutic opportunities. Inflam Bowel Dis 12(Suppl 1):S3–S9

    Article  Google Scholar 

  17. Kotlowski R, Bernstein CN, Sepehri S, Krause DO (2007) High prevalence of Escherichia coli belonging to the B2 + D phylogenetic group in inflammatory bowel disease. Gut 56:669–675

    Article  PubMed  CAS  Google Scholar 

  18. La Ferla K, Seegert D, Schreiber S (2004) Activation of NF-kappa B in intestinal epithelial cells by E. coli strains isolated from the colonic mucosa of IBD patients. Int J Colorectal Dis 19:334–342

    Article  PubMed  Google Scholar 

  19. Lapaquette P, Glasser AL, Huett A, Xavier RJ, Darfeuille-Michaud A (2010) Crohn’s disease-associated adherent-invasive E. coli are selectively favoured by impaired autophagy to replicate intracellularly. Cell Microbiol 12:99–113

    Article  PubMed  CAS  Google Scholar 

  20. Loftus EV Jr (2004) Clinical epidemiology of inflammatory bowel disease: incidence, prevalence, and environmental influences. Gastroenterology 126:1504–1517

    Article  PubMed  Google Scholar 

  21. Martin HM, Campbell BJ, Hart CA, Mpofu C, Nayar M, Singh R, Englyst H, Williams HF, Rhodes JM (2004) Enhanced Escherichia coli adherence and invasion in Crohn’s disease and colon cancer. Gastroenterology 127:80–93

    Article  PubMed  CAS  Google Scholar 

  22. Martinez-Medina M, Aldeguer X, Lopez-Siles M, Gonzalez-Huix F, Lopez-Oliu C, Dahbi G, Blanco JE, Blanco J, Garcia-Gil LJ, Darfeuille-Michaud A (2009) Molecular diversity of Escherichia coli in the human gut: new ecological evidence supporting the role of adherent-invasive E. coli (AIEC) in Crohn’s disease. Inflam Bowel Dis 15:872–882

    Article  Google Scholar 

  23. Martinez-Medina M, Mora A, Blanco M, Lopez C, Alonso MP, Bonacorsi S, Nicolas-Chanoine MH, Darfeuille-Michaud A, Garcia-Gil J, Blanco J (2009) Similarity and divergence among adherent-invasive E. coli (AIEC) and extraintestinal pathogenic E. coli (ExPEC). J Clin Microbiol 47:3968–3979

    Article  PubMed  CAS  Google Scholar 

  24. Moussata D, Goetz M, Gloeckner A, Kerner M, Campbell B, Hoffman A, Biesterfeld S, Flourie B, Saurin J-C, Galle PR, Neurath MF, Watson AJM, Kiesslich R (2011) Confocal laser endomicroscopy is a new imaging modality for recognition of intramucosal bacteria in onflammatory bowel disease in vivo. Gut 60:26–33

    Article  PubMed  Google Scholar 

  25. Muller D, Hagedorn P, Brast S, Heusipp G, Bielaszewska M, Friedrich A, Karch H, Schmidt MA (2006) Rapid identification and differentiation of clinical isolates of enteropathogenic Escherichia coli (EPEC), and Shiga toxin-producing Escherichia coli by one-step multiplex PCR method. J Clin Microbiol 44:2626–2629

    Article  PubMed  Google Scholar 

  26. Naser SA, Ghobrial G, Romero C, Valentine JF (2004) Culture of Mycobacterium avium subsp. paratuberculosis from the blood of patients with Crohn’s disease. Lancet 364:1039–1044

    Article  PubMed  Google Scholar 

  27. Prantera C, Scribano ML (2009) Antibiotics and probiotics in inflammatory bowel disease: why, when, and how. Curr Opin Gastroenterol 25:329–333

    Article  PubMed  CAS  Google Scholar 

  28. Rachmilewitz D (1989) Coated mesalazine (5-aminosalicylic acid) versus sulphasalazine in the treatment of active ulcerative colitis: a randomized trial. BMJ 298:82–86

    Article  PubMed  CAS  Google Scholar 

  29. Sartor BR (2004) Therapeutic manipulation of the enteric microflora in inflammatory bowel disease: antibiotics, probiotics, and prebiotics. Gastroenterology 126:1620–1633

    Article  PubMed  Google Scholar 

  30. Sartor RB (2008) Microbial influences in inflammatory bowel disease. Gastroenterology 134:577–594

    Article  PubMed  CAS  Google Scholar 

  31. Sasaki M, Sitaraman SV, Babbin BA (2007) Invasive Escherichia coli are a feature of Crohn’s disease. Lab Investig 87:1042–1154

    Article  PubMed  CAS  Google Scholar 

  32. Sauer A, Moraru CI (2009) Inactivation of Escherichia coli ATCC 25922 and Escherichia coli O157:H7 in apple juice and apple cider, using pulsed light treatment. J Food Prot 72:937–944

    PubMed  Google Scholar 

  33. Sepehri S, Khafipour E, Bernstein CN, Coombes BK, Pilar AV, Karmali M, Ziebell K, Krause DO (2010) Characterization of Escherichia coli isolated from gut biopsies of newly diagnosed patients with inflammatory bowel disease. Inflamm Bowel Dis 11:22–33. doi:10.1002/ibd.21509

    Google Scholar 

  34. Strober W, Fuss I, Mannon P (2008) The fundamental basis of inflammatory bowel disease. J Clin Invest 117:514–521

    Article  Google Scholar 

  35. Tennant S, Tauschek M, Azzopardi K, Bigham A, Bennett-Wood V, Hartland EL, Whittam TS, Robins-Browne RM (2009) Characterization of atypical enteropathogenic E. coli strains of clinical origin. BMC Microbiol 9:117–128

    Article  PubMed  Google Scholar 

  36. Tenover FC, Arbeit RD, Goering RV, Mickelsen P, Murray B, Persing DH, Swaminathan B (1995) Interpreting chromosomal DNA restriction patterns produced by pulse-field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol 33:2233–2239

    PubMed  CAS  Google Scholar 

  37. Willing B, Halfvarson J, Dicksved J, Rosenquist M, Jarnerot G, Engstrand L, Tysk C, Jansson JK (2009) Twin studies reveal specific imbalances in the mucosa-associated microbiota of patients with ileal Crohn’s disease. Inflamm Bowel Dis 15:653–660

    Article  PubMed  Google Scholar 

  38. Wine E, Ossa JC, Gray-Owen SD, Sherman PM (2009) Adherent-invasive Escherichia coli, strain LF82 disrupts apical junctional complexes in polarized epithelia. BMC Microbiol 9:180–191

    Article  PubMed  Google Scholar 

  39. Wine E, Ossa JC, Gray-Owen SD, Sherman PM (2010) Adherent-invasive Escherichia coli target the epithelium barrier. Gut Microbes 1:80–84

    Article  PubMed  Google Scholar 

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Acknowledgment

This study was partly supported by a grant from Piedmont Region (2008 bis).

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Authors and Affiliations

  1. Department of Clinical and Biological Sciences, Faculty of Medicine S. Luigi Gonzaga, University of Torino, S. Luigi Gonzaga Hospital, Regione Gonzole 10, 10043, Orbassano, TO, Italy

    Tiziana Raso, Sabrina Crivellaro & Dianella Savoia

  2. Laboratory, S. Luigi Gonzaga Hospital, Orbassano, TO, Italy

    Maria Gabriella Chirillo

  3. Division of Gastroenterology, S. Luigi Gonzaga Hospital, Orbassano, TO, Italy

    Paolo Pais & Ezio Gaia

Authors
  1. Tiziana Raso
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  2. Sabrina Crivellaro
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  3. Maria Gabriella Chirillo
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  4. Paolo Pais
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  5. Ezio Gaia
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  6. Dianella Savoia
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Correspondence to Dianella Savoia.

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Raso, T., Crivellaro, S., Chirillo, M.G. et al. Analysis of Escherichia coli Isolated from Patients Affected by Crohn’s Disease. Curr Microbiol 63, 131–137 (2011). https://doi.org/10.1007/s00284-011-9947-8

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  • DOI: https://doi.org/10.1007/s00284-011-9947-8

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