European Journal of Internal Medicine
Volume 19, Issue 3 , Pages 181-186 , May 2008

Microscopic colitis: A common and an easily overlooked cause of chronic diarrhoea

  • Nils Nyhlin

      Affiliations

    • Department of Medicine, Division of Gastroenterology, Örebro University Hospital, Örebro, Sweden
    • ,
  • Johan Bohr

      Affiliations

    • Department of Medicine, Division of Gastroenterology, Örebro University Hospital, Örebro, Sweden
    • School of Health and Medical Sciences, Örebro University, Örebro, Sweden
    • ,
  • Sune Eriksson

      Affiliations

    • Department of Pathology, Örebro University Hospital, Örebro, Sweden
    • ,
  • Curt Tysk

      Affiliations

    • Department of Medicine, Division of Gastroenterology, Örebro University Hospital, Örebro, Sweden
    • School of Health and Medical Sciences, Örebro University, Örebro, Sweden
    • Corresponding Author InformationCorresponding author. Department of Medicine, Division of Gastroenterology, Örebro University Hospital, SE-701 85 Örebro, Sweden. Tel.: +46 19 6021000; fax: +46 19 6021774.

Received 21 January 2008 ,Accepted 22 January 2008.

References 

  1. Thomas PD, Forbes A, Green J, et al. Guidelines for the investigation of chronic diarrhoea, 2nd edition. Gut. 2003;52(Suppl 5):v1–v15
  2. Pardi DS. Microscopic colitis: an update. Inflamm Bowel Dis. 2004;10:860–870
  3. Lindström CG. ‘Collagenous colitis’ with watery diarrhoea—a new entity?. Pathol Eur. 1976;11:87–89
  4. Lazenby AJ, Yardley JH, Giardiello FM, Jessurun J, Bayless TM. Lymphocytic (“microscopic”) colitis: a comparative histopathologic study with particular reference to collagenous colitis. Hum Pathol. 1989;20:18–28
  5. Olesen M, Eriksson S, Bohr J, Jarnerot G, Tysk C. Microscopic colitis: a common diarrhoeal disease. An epidemiological study in Orebro, Sweden, 1993–1998. Gut. 2004;53:346–350
  6. Pardi DS, Loftus EV, Smyrk TC, et al. The epidemiology of microscopic colitis: a population based study in Olmsted County, Minnesota. Gut. 2007;56:504–508
  7. Rubio-Tapia A, Martinez-Salgado J, Garcia-Leiva J, Martinez-Benitez B, Uribe M. Microscopic colitides: a single center experience in Mexico. Int J Colorectal Dis. 2007;22:1031–1036
  8. Fekih M, Ben Hriz F, Sassi A, Matri S, Filali A, Boubaker J. Tunis Med. 2006;84:403–406
  9. Tagkalidis P, Bhathal P, Gibson P. Microscopic colitis. J Gastroenterol Hepatol. 2002;17:236–248
  10. Garg PK, Singh J, Dhali GK, Mathur M, Sharma MP. Microscopic colitis is a cause of large bowel diarrhea in Northern India. J Clin Gastroenterol. 1996;22:11–15
  11. Agnarsdottir M, Gunnlaugsson O, Orvar KB, et al. Collagenous and lymphocytic colitis in Iceland. Dig Dis Sci. 2002;47:1122–1128
  12. Bohr J, Tysk C, Eriksson S, Järnerot G. Collagenous colitis in Orebro, Sweden, an epidemiological study 1984–1993. Gut. 1995;37:394–397
  13. Fernandez-Banares F, Salas A, Forne M, Esteve M, Espinos J, Viver JM. Incidence of collagenous and lymphocytic colitis: a 5-year population-based study. Am J Gastroenterol. 1999;94:418–423
  14. Heron T, Walsh S, Mowat A. Microscopic colitis in Tayside: clinical features, associations, and behaviour. Gut. 2005;54(suppl 2):A84
  15. Raclot G, Queneau PE, Ottignon Y, et al. Incidence of collagenous colitis. A retrospective study in the east of France. Gastroenterology. 1994;106:A23
  16. Rajan J, Noble C, Anderson C, Satsangi J, Lessels A, Arnott I. The epidemiology and clinical features of collagenous colitis in Lothian. Gut. 2005;54(suppl 2):A99
  17. Wickbom A, Nyhlin N, Eriksson S, Bohr J, Tysk C. Collagenous colitis and lymphocytic colitis in Örebro, Sweden 1999–2004; a continuous epidemiological study. Gut. 2006;55(suppl V):A111
  18. Williams JJ, Kaplan GG, Makhija S, et al. Microscopic colitis-defining incidence rates and risk factors: a population-based study. Clin Gastroenterol Hepatol. 2008;6:35–40
  19. Bohr J, Tysk C, Eriksson S, Abrahamsson H, Jarnerot G. Collagenous colitis: a retrospective study of clinical presentation and treatment in 163 patients. Gut. 1996;39:846–851
  20. Benchimol EI, Kirsch R, Viero S, Griffiths AM. Collagenous colitis and eosinophilic gastritis in a 4-year old girl: a case report and review of the literature. Acta Paediatr. 2007;96:1365–1367
  21. Olesen M, Eriksson S, Bohr J, Jarnerot G, Tysk C. Lymphocytic colitis: a retrospective clinical study of 199 Swedish patients. Gut. 2004;53:536–541
  22. Pardi DS, Ramnath VR, Loftus EV, Tremaine WJ, Sandborn WJ. Lymphocytic colitis: clinical features, treatment, and outcomes. Am J Gastroenterol. 2002;97:2829–2833
  23. Hjortswang H, Tysk C, Bohr J, et al. Health-related quality of life is impaired in patients with collagenous colitis. Gut. 2005;54(Suppl VII):A183
  24. Madisch A, Heymer P, Voss C, et al. Oral budesonide therapy improves quality of life in patients with collagenous colitis. Int J Colorectal Dis. 2005;20:312–316
  25. Bohr J, Larsson LG, Eriksson S, Jarnerot G, Tysk C. Colonic perforation in collagenous colitis: an unusual complication. Eur J Gastroenterol Hepatol. 2005;17:121–124
  26. Sherman A, Ackert JJ, Rajapaksa R, West AB, Oweity T. Fractured colon: an endoscopically distinctive lesion associated with colonic perforation following colonoscopy in patients with collagenous colitis. J Clin Gastroenterol. 2004;38:341–345
  27. Chan JL, Tersmette AC, Offerhaus GJ, Gruber SB, Bayless TM, Giardiello FM. Cancer risk in collagenous colitis. Inflamm Bowel Dis. 1999;5:40–43
  28. Limsui D, Pardi DS, Camilleri M, et al. Symptomatic overlap between irritable bowel syndrome and microscopic colitis. Inflamm Bowel Dis. 2007;13:175–181
  29. Barta Z, Mekkel G, Csipo I, et al. Microscopic colitis: a retrospective study of clinical presentation in 53 patients. World J Gastroenterol. 2005;11:1351–1355
  30. Bohr J, Tysk C, Yang P, Danielsson D, Jarnerot G. Autoantibodies and immunoglobulins in collagenous colitis. Gut. 1996;39:73–76
  31. Ung KA, Gillberg R, Kilander A, Abrahamsson H. Role of bile acids and bile acid binding agents in patients with collagenous colitis. Gut. 2000;46:170–175
  32. Warren BF, Edwards CM, Travis SP. ‘Microscopic colitis’: classification and terminology. Histopathology. 2002;40:374–376
  33. Tanaka M, Mazzoleni G, Riddell RH. Distribution of collagenous colitis: utility of flexible sigmoidoscopy. Gut. 1992;33:65–70
  34. Wildt S, Nordgaard-Lassen I, Bendtsen F, Rumessen JJ. Metabolic and inflammatory faecal markers in collagenous colitis. Eur J Gastroenterol Hepatol. 2007;19:567–574
  35. Beaugerie L, Pardi DS. Review article: drug-induced microscopic colitis — proposal for a scoring system and review of the literature. Aliment Pharmacol Ther. 2005;22:277–284
  36. Erim T, Alazmi WM, O'Loughlin CJ, Barkin JS. Collagenous colitis associated with Clostridium difficile: a cause effect?. Dig Dis Sci. 2003;48:1374–1375
  37. Perk G, Ackerman Z, Cohen P, Eliakim R. Lymphocytic colitis: a clue to an infectious trigger. Scand J Gastroenterol. 1999;34:110–112
  38. Bohr J, Nordfelth R, Järnerot G, Tysk C. Yersinia species in collagenous colitis: a serologic study. Scand J Gastroenterol. 2002;37:711–714
  39. Makinen M, Niemela S, Lehtola J, Karttunen TJ. Collagenous colitis and Yersinia enterocolitica infection. Dig Dis Sci. 1998;43:1341–1346
  40. LaSala PR, Chodosh AB, Vecchio JA, Schned LM, Blaszyk H. Seasonal pattern of onset in lymphocytic colitis. J Clin Gastroenterol. 2005;39:891–893
  41. Osterholm MT, MacDonald KL, White KE, et al. An outbreak of a newly recognized chronic diarrhea syndrome associated with raw milk consumption. JAMA. 1986;256:484–490
  42. Bryant DA, Mintz ED, Puhr ND, Griffin PM, Petras RE. Colonic epithelial lymphocytosis associated with an epidemic of chronic diarrhea. Am J Surg Pathol. 1996;20:1102–1109
  43. Burgel N, Bojarski C, Mankertz J, Zeitz M, Fromm M, Schulzke JD. Mechanisms of diarrhea in collagenous colitis. Gastroenterology. 2002;123:433–443
  44. Bohr J, Jarnerot G, Tysk C, Jones I, Eriksson S. Effect of fasting on diarrhoea in collagenous colitis. Digestion. 2002;65:30–34
  45. Olesen M, Middelveld R, Bohr J, et al. Luminal nitric oxide and epithelial expression of inducible and endothelial nitric oxide synthase in collagenous and lymphocytic colitis. Scand J Gastroenterol. 2003;38:66–72
  46. Baert F, Schmit A, D'Haens G, et al. Budesonide in collagenous colitis: a double-blind placebo-controlled trial with histologic follow-up. Gastroenterology. 2002;122:20–25
  47. Miehlke S, Heymer P, Bethke B, et al. Budesonide treatment for collagenous colitis: a randomized, double-blind, placebo-controlled, multicenter trial. Gastroenterology. 2002;123:978–984
  48. Bonderup OK, Hansen JB, Birket-Smith L, Vestergaard V, Teglbjaerg PS, Fallingborg J. Budesonide treatment of collagenous colitis: a randomised, double blind, placebo controlled trial with morphometric analysis. Gut. 2003;52:248–251
  49. Chande N, McDonald JW, MacDonald JK. Interventions for treating collagenous colitis. Cochrane Database Syst Rev. 2006;CD003575
  50. Miehlke S, Madisch A, Karimi D, et al. Budesonide for treatment of lymphocytic colitis — a randomized, double-blind, placebo-controlled trial. Gut. 2007;56(Suppl III):A156
  51. Miehlke S, Madisch A, Bethke B, et al. Budesonide for maintenance treatment of collagenous colitis — a randomized, double-blind, placebo-controlled trial. Gut. 2007;56(Suppl III):A155
  52. Munck LK, Kjeldsen J, Philipsen E, Fischer Hansen B. Incomplete remission with short-term prednisolone treatment in collagenous colitis: a randomized study. Scand J Gastroenterol. 2003;38:606–610
  53. Fine KD, Ogunji F, Lee E, Lafon G, Tanzi M. Randomized, double blind, placebo-controlled trial of bismuth subsalicylate for microscopic colitis. Gastroenterology. 1999;116:A880
  54. Calabrese C, Fabbri A, Areni A, Zahlane D, Scialpi C, Di Febo G. Mesalazine with or without cholestyramine in the treatment of microscopic colitis: randomized controlled trial. J Gastroenterol Hepatol. 2007;22:809–814
  55. Wildt S, Munck LK, Vinter-Jensen L, et al. Probiotic treatment of collagenous colitis: a randomized, double-blind, placebo-controlled trial with Lactobacillus acidophilus and Bifidobacterium animalis subsp. Lactis.. Inflamm Bowel Dis. 2006;12:395–401
  56. Madisch A, Miehlke S, Eichele O, et al. Boswellia serrata extract for the treatment of collagenous colitis. A double-blind, randomized, placebo-controlled, multicenter trial. Int J Colorectal Dis. 2007;22:1445–1451
  57. Pardi DS, Loftus EV, Tremaine WJ, Sandborn WJ. Treatment of refractory microscopic colitis with azathioprine and 6-mercaptopurine. Gastroenterology. 2001;120:1483–1484
  58. Riddell J, Hillman L, Chiragakis L, Clarke A. Collagenous colitis: oral low-dose methotrexate for patients with difficult symptoms: long-term outcomes. J Gastroenterol Hepatol. 2007;22:1589–1593
  59. Jarnerot G, Bohr J, Tysk C, Eriksson S. Faecal stream diversion in patients with collagenous colitis. Gut. 1996;38:154–155
  60. Varghese L, Galandiuk S, Tremaine WJ, Burgart LJ. Lymphocytic colitis treated with proctocolectomy and ileal J-pouch-anal anastomosis: report of a case. Dis Colon Rectum. 2002;45:123–126
  61. Goff JS, Barnett JL, Pelke T, Appelman HD. Collagenous colitis: histopathology and clinical course. Am J Gastroenterol. 1997;92:57–60
  62. Bonner GF, Petras RE, Cheong DM, Grewal ID, Breno S, Ruderman WB. Short- and long-term follow-up of treatment for lymphocytic and collagenous colitis. Inflamm Bowel Dis. 2000;6:85–91
  63. Mullhaupt B, Guller U, Anabitarte M, Guller R, Fried M. Lymphocytic colitis: clinical presentation and long term course. Gut. 1998;43:629–633

☆ Grant support: Örebro County Research Committee, Örebro University Hospital Research Foundation and the Swedish Society of Medicine (Bengt Ihre Foundation, grant 16898-2005) supported our studies of microscopic colitis. This is gratefully acknowledged.

PII: S0953-6205(08)00042-3

doi: 10.1016/j.ejim.2008.01.001

European Journal of Internal Medicine
Volume 19, Issue 3 , Pages 181-186 , May 2008

Article Tools

* Image Usage & Resolution