Evolution of ideas on microscopic colitis


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Abstract

The literature review gives the present-day views of the definition, etiology, pathogenesis, diagnosis, and treatment of microscopic colitis (MC). In the present view, MC is an inflammatory bowel disease of unknown etiology, which is characterized by chronic watery diarrhea, no macroscopic signs of large bowel involvement in the presence of specific pathomorphological changes. There are two major forms of MC, which are similar in its clinical picture, yet, heterogeneous in histological criteria: collagenous colitis (CC) and lymphocytic colitis (LC). As of now, the prevalence of MC is about 100 cases per 100,000 population, which is similar with that in other inflammatory bowel diseases, such as ulcerative colitis and Crohn’s disease. MC generally prevails in women aged over 50 years. The etiology and pathogenesis of MC have not fully investigated. Watery diarrhea is as a predominant pathognomonic symptom in all the patients with MC. The major histological criterion for the diagnosis of CC is subepithelial collagen lining thickening (more than 10 µm) and that for LC is higher intraepithelial lymphocyte counts (more than 20 intraepithelial lymphocytes/100 epitheliocytes). The topical glucocorticosteroid budesonide is currently the only agent, the efficacy of which has been proven in both inducing and maintaining remission in patients with MC in many clinical trials.

References

  1. Lindström C.G. Collagenous colitis’ with watery diarrhoea — a new entity? Pathol Eur 1976; 11: 87—89.
  2. Read N.W., Krejs G.J., Read M.G., Santa Ana C.A., Morawski S.G., Fordtran J.S. Chronic diarrhea of unknown origin. Gastroenterology 1980; 78: 264—271.
  3. Lazenby A.J, Yardley J.H., Giardiello F.M., Jessurun J., Bayless T.M. Lymphocytic («microscopic») colitis: a comparative histopathologic study with particular reference to collagenous colitis. Hum Pathol 1989; 20: 18—28.
  4. Кучерявый Ю.А., Андреев Д.Н. Микроскопический колит: пособие для врачей. М: Форте принт 2014.
  5. Ianiro G., Cammarota G., Valerio L., Annicchiarico B.E., Milani A., Siciliano M., Gasbarrini A. Microscopic colitis. World J Gastroenterol 2012; 18 (43): 6206—6215.
  6. Münch A., Aust D., Bohr J., Bonderup O., Fernández Bañares F., Hjortswang H., Madisch A., Munck L.K., Ström M., Tysk C., Miehlke S.; European Microscopic Colitis Group (EMCG). Microscopic colitis: Current status, present and future challenges: statements of the European Microscopic Colitis Group. J Crohns Colitis 2012; 6 (9): 932—945.
  7. Tromm A. Microscopic colitis. Bremen: UNI-MED 2012.
  8. Goldstein N.S., Bhanot P. Paucicellular and asymptomatic lymphocytic colitis. Am J Clin Pathol 2004; 122: 405—411.
  9. Yuan S., Reyes V., Bronner M.P. Pseudomembranous collagenous colitis. Am I Surg Pathol 2003; 27: 1375—1379.
  10. Libbrecht L., Croes R., Ectors N., Staels F., Geboes K. Microscopic colitis with giant cell. Histopathology 2002; 40: 335—338.
  11. Rubio C.A., Lindholm J. Cryptal lymphocytic coloproctitis: a new phenotype of lymphocytic colitis? J Clin Pathol 2002; 55: 138—140.
  12. Gentile N.M., Khanna S., Loftus E.V. Jr, Smyrk T.C., Tremaine W.J., Harmsen W.S., Zinsmeister A.R., Kammer P.P., Pardi D.S. The epidemiology of microscopic colitis in Olmsted County from 2002 to 2010: a population-based study. Clin Gastroenterol Hepatol 2014; 12 (5): 838—842.
  13. Vigren L., Olesen M., Benoni C., Sjöberg K. An epidemiological study of collagenous colitis in southern Sweden from 2001—2010. World J Gastroenterol 2012; 18 (22): 2821—2826.
  14. Pardi D.S., Loftus E.V. Jr, Smyrk T.C., Kammer P.P., Tremaine W.J., Schleck C.D., Harmsen W.S., Zinsmeister A.R., Melton L.J. 3rd, Sandborn W.J. The epidemiology of microscopic colitis: a population based study in Olmsted County, Minnesota. Gut 2007; 56: 504—508.
  15. Olesen M., Erickson S., Bohr J., Jarnerot G., Tysk C. Microscopic colitis: a common diarrheal disease. An epidemiological study in Orebro, Sweden, 1993—1998. Gut 2004; 53: 364—350.
  16. Wickbom A., Nyhlin N.E.S., Bohr J., Tysk C. Stable incidences of collagenous colitis and lymphocytic colitis in Örebro, Sweden 1999—2008. Gut 2009; 58 (Suppl. II): A58.
  17. Olesen M., Eriksson S., Bohr J., Järnerot G., Tysk C. Lymphocytic colitis: a retrospective clinical study of 199 Swedish patients. Gut 2004; 53: 536—541.
  18. Storr M.A. Microscopic colitis: epidemiology, pathophysiology, diagnosis and current management-an update 2013. ISRN Gastroenterol 2013; 2013: 352718.
  19. Cindoruk M., Tuncer C., Dursun A., Yetkin I., Karakan T., Cakir N., Soykan I. Increased colonic intraepithelial lymphocytes in patients with Hashimoto’s thyroiditis. J Clin Gastroenterol 2002; 34 (3): 237—239.
  20. Freeman H.J. Collagenous colitis as the presenting feature of biopsy-defined celiac disease. J Clin Gastroenterol 2004; 38 (8): 664—668.
  21. Williams J.J., Kaplan G.G., Makhija S., Urbanski S.J., Dupre M., Panaccione R., Beck P.L. Microscopic colitis-defining incidence rates and risk factors: a population-based study. Clin Gastroenterol Hepatol 2008; 6 (1): 35—40.
  22. Koskela R.M., Niemelä S.E., Karttunen T.J., Lehtola J.K. Clinical characteristics of collagenous and lymphocytic colitis. Scand J Gastroenterol 2004; 39 (9): 837—845.
  23. Nyhlin N., Montgomery S.M., Wickbom A., Tysk C., Bohr J. Symptom burden in collagenous and lymphocytic colitis compared to a matched control group. Gut 2009; 58 (Suppl. II): A309.
  24. Vigren L., Sjoberg K., Benoni C., Tysk C., Bohr J., Kilander A., Larsson L., Ström M., Hjortswang H. Is smoking a risk factor for collagenous colitis?. Scand J Gastroenterol 2011; 46: 1334—1339.
  25. Fernández-Bañares F., de Sousa M.R., Salas A., Beltrán B., Piqueras M., Iglesias E., Gisbert J.P., Lobo B., Puig-Diví V., García-Planella E., Ordás I., Andreu M., Calvo M., Montoro M., Esteve M., Viver J.M. Epidemiological risk factors in microscopic colitis: a prospective case-control study. Inflamm Bowel Dis 2013; 19: 411—417.
  26. Beaugerie L., Pardi D.S. Review article: drug-induced microscopic colitis — proposal for a scoring system and review of the literature. Aliment Pharmacol Ther 2005; 22: 277—284.
  27. Thomson R.D., Lestina L.S., Bensen S.P., Toor A., Maheshwari Y., Ratcliffe N.R. Lansoprazole-associated microscopic colitis: a case series. Am J Gastroenterol 2002; 97: 2908—2913.
  28. Mukherjee S. Diarrhea associated with lansoprazole. J Gastroenterol Hepatol 2003; 18: 602—603.
  29. Chagnon J.P., Cerf M. Simvastatin-induced protein-losing enteropathy. Am J Gastroenterol 1992; 87: 257.
  30. Duncan H.D., Talbot 1.С., Silk D.B.A. Collagenous colitis and cimetidine. Eur J Gastroenterol Hepatol 1997; 9: 819—820.
  31. Fernandez-Banares F., Esteve M., Espinos J.C., Rosi-nach M., Forne M., Salas A., Viver J.M. Drug consumption and the risk of microscopic colitis. Am J Gastroenterol 2007; 102: 324—330.
  32. Keszthelyi D., Penders J., Masclee A.A., Pierik M. Is microscopic colitis a drug-induced disease? J Clin Gastroenterol 2012; 46: 811—822.
  33. Pardi D.S. Microscopic colitis: an update. Inflamm Bowel Dis 2004; 10: 860—870.
  34. Bohr I., Tysk C., Eriksson S., Jarnerot G. Collagenous Colitis: Epidemiology, associated diseases and medical therapy. Gut 1994; 35 (Suppl. 4) :A2.
  35. Fausa O., Forester A., Hovig T. Collagenous colitis: a clinical, histological and ultrastructural study. Scand J Gastroenterol 1985; 20 (Suppl. 107): 8—23.
  36. Makinen M., Niemela S., Lehtola J., Karttunen T.J. Collagenous colitis and Yersinia enterocolitica infection. Dig Dis Sci 1998; 43: 1341—1346.
  37. Bohr J., Nordfelth R., Tysk C., Jarnerot G. Yersinia species in collagenous colitis: A serologic study. Scand J Gastroenterol 2002; 37: 711—714.
  38. Miehlke S., Madisch A., Morgner A., Bethke B., Stolte M., Lehn N., Schneider-Brachert W. Relevanz von Yersinia-Outer-Membrane-Proteinen bei kollagener und lym-phozytarer Kolitis. Z Gastroenterol 2011; 49: 1007—1026.
  39. Tamboli C.P., Good M.R., Reynolds E.M., Sharma P., Mitros F.A. Anti-Yersinia antibodies are not associated with microscopic colitis in an American case-control study. Scand J Gastroenterol 2011; 46: 1442—1448.
  40. Ung K.A., Gillberg L., Kilander A., Abrahamsson H. Role of bile acids and bile acid binding agents in patients with collagenous colitis. Gut 2000; 46: 170—175.
  41. Ung K.A., Kilander A., Willen R., Abrahamsson H. Role of bile acids in lymphocytic colitis. Hepatogastroenterology 2002; 49: 432—437.
  42. Abdo A.A., Zetler P.J., Halparin L.S. Familial microscopic colitis. Can J Gastroenterol 2001; 15: 341—343.
  43. Fine K.D., Do K., Schulte K., Ogunji F., Guerra R., Osowski L., McCormack J. High prevalence of celiac sprue-like HLA-DQ genes and enteropathy in patients with the microscopic colitis syndrome. Am J Gastroenterol 2000; 95: 1974—1982.
  44. Fernandez-Banares F., Esteve M., Farre C., Salas A., Alsina M., Casalots J., Espinós J., Forné M., Viver J.M. Predisposing HLA-DQ2 and HLA-DQ8 haplotypes of coeliac disease and associated enteropathy in microscopic colitis. Eur J Gastroenterol Hepatol 2005; 17: 1333—1338.
  45. Ayata G., Ithamukkala S., Sapp H., Shaz B.H., Brien T.P., Wang H.H., Antonioli D.A., Farraye F.A., Odze R.D. Prevalence and significance of inflammatory bowel diseaselike morphological features in collagenous and lymphocytic colitis. Am I Surg Pathol 2002; 26: 1414—1423.
  46. Маев И.В., Андреев Д.Н. Молекулярно-генетические механизмы развития болезни Крона. Мол мед 2014; 3: 21—27.
  47. Maev I.V., Andreev D.N. Role of mutations in NOD2/CARD15, ATG16L1, and IRGM in the pathogenesis of Crohn’s disease. Int J Biomed 2014; 4 (1): 7—10.
  48. Madisch A., Hellmig S., Schreiber S., Bethke B., Stolte M., Miehlke S. NOD2/CARD15 gene polymorphisms are not associated with collagenous colitis. Int J Colorectal Dis 2007; 22: 425—428.
  49. Hwang W.S., Kelly K., Shaffer E.A., Hershfield N.B. Collagenous colitis: a disease of pericryptal fibroblast sheath? J Pathol 1986; 149: 33—40.
  50. Widgren S., Jlidi R., Cox J.N. Collagenous colitis: histologic, morphmetric, immunohistochemical and ultra-structural studies. Virchows Arch a Pathol Anat Histo-pathol 1988; 413: 287—296.
  51. Aigner T., Neureiter D., Muller S., Kuspert G., Belke J., Kirchner T. Extracellular matrix composition and gene expression in collagenous colitis. Gastroenterology 1997; 113: 136—143.
  52. Gunther U., Schuppan D., Bauer M., Matthes H., Stall-mach A., Schmitt-Graff A., Riecken E.O., Herbst H. Fibro-genesis and fibrolysis in collagenous colitis. Patterns of procollagen types I and IV, matrix-metalloproteinase-1 and -13, and TIMP-1 gene expression. Am J Pathol 1999; 155: 493—503.
  53. Griga T., Tromm A., Schmiegel W., Pfisterer O., Muller K.M., Brasch F. Collagenous colitis: implications for the role of vascular endothelial growth factor in repair mechanisms. Eur J Gastroenterol Hepatol 2004; 16: 397—402.
  54. Taha Y., Raab Y., Larsson A., Carlson M., Loof L., Gerdin B., Thorn M. Vascular endothelial growth factor (VEGF) — a possible mediator of inflammation and mucosal permeability in patients with collagenous colitis. Dig Dis Sci 2004; 49: 109—115.
  55. Madisch A., Hellmig S., Schreiber S., Bethke B., Stolte M., Miehlke S. Allelic variation of the matrix metallo-proteinase-9 gene is associated with collagenous colitis. Inflamm Bowel Dis 2011; 17: 2295—2298.
  56. Bohr I., 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.
  57. Bonderup O.K., Folkersen B.H., Gjersoe P., Teglbjaerg P.S. Collagenous colitis: a long-term follow-up study. Eur J Gastroenterol Hepatol 1999; 11: 493—495.
  58. Chan J.L., Tersmette A.C., Offerhaus G.J.A., Gruber S.B., Bayless T.M., Giardiello F.M. Cancer risk in collagenous colitis. Inflam Bowel Dis 1999; 5: 40—43.
  59. Madisch A., Miehlke S., Lindner M., Bethke B., Stolte M. Clinical Course of collagenous colitis over a period of 10 years. Z Gastroenterol 2006; 44: 971—974.
  60. Thijs W.J., van Baarlen J., Kleibeuker J.H., Kolkman J.J. Microscopic colitis: prevalence and distribution throughout the colon in patients with chronic diarrhea. Neth J Med 2005; 63: 137—140.
  61. Andrews C.N., Beck P.L., Wilsack L.H., Urbanski S.J., Storr M. Evaluation of endoscopist and pathologist factors affecting the incidence of microscopic colitis. Canadian J Gastroenterol 2012; 26: 515—520.
  62. Маев И.В., Кучерявый Ю.А., Черемушкин С.В. Эволюция представлений о синдроме раздраженного кишечника. М: Форте принт 2013.
  63. Дичева Д.Т., Андреев Д.Н. Алгоритм диагностики и лечения синдрома раздраженного кишечника. Consilium Medicum. Гастроэнтерология 2013; 1: 80.
  64. Ingle S.B., Adgaonkar B.D., Ingle C.R. Microscopic colitis: Common cause of unexplained nonbloody diarrhea. World J Gastrointest Pathophysiol 2014; 5 (1): 48—53.
  65. Ивашкин В.Т., Шептулин А.А., Шифрин О.С., Галимова С.Ф., Юрманова Е.Н. Микроскопический колит: клинические формы, диагностика, лечение. Рус журн гастроэнтерол, гепатол, колопроктол 2006; 6: 56—60.
  66. Guslandi M. Microscopic colitis: a therapeutic challenge. World J Gastroenterol 2013; 19 (23): 3531—3533.
  67. Chande N., MacDonald J.K., McDonald J.W.D. Interventions for treating microscopic colitis: a cochrane inflammatory bowel disease and functional bowel disorders review group systematic review of randomized trials. Am J Gastroenterol 2009; 104 (1): 235—241.
  68. Stewart M.J., Seow C.H., Storr M.A. Prednisolone and budesonide for short- and long-term treatment of microscopic colitis: systematic review and meta-analysis. Clin Gastroenterol Hepatol 2011; 9 (10): 881—890.
  69. Miehlke S., Madisch A., Bethke B., Morgner A., Kuhlisch E., Henker C., Vogel G., Andersen M., Meier E., Baretton G.,Stolte А. Oral budesonide for maintenance treatment of collagenous colitis: a randomized, double-blind, placebo-controlled trial. Gastroenterology 2008; 135: 1510—1516.
  70. Bonderup O.K., Hansen J.B., Teglbjaerg P.S., Christensen L.A., Fallingborg J.F. Long-term budesonide treatment of collagenous colitis — a randomized, double-blind, placebo-controlled trial. Gut 2009; 58: 68—72.
  71. Munck L.K., Kjeldsen J., Philipsen E., Fischer H.B. Incomplete remission with short-term prednisolone treatment in collagenous colitis: a randomized study. Scand I Gastroenterol 2003; 38: 606—610.
  72. 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.
  73. Miehlke S., Madisch A., Kupcinskas L., Petrauskas D., Böhm G., Marks H.J., Neumeyer M., Nathan T., Fernández-Bañares F., Greinwald R., Mohrbacher R., Vieth M., Bonderup O.K.; BUC-60/COC Study Group. Budesonide is more effective than mesalamine or placebo in short-term treatment of collagenous colitis. Gastroenterology 2014; 146: 1222—1230.
  74. Fine К.O.F., Lee E., Lafon G., Tanzi M. Randomized, double-blind, placebo-controlled trial of bismuth subsalicylate for microscopic colitis Gastroenterology 1999; U6: A880.
  75. Wildt S., Munck L.K., Vinter-Jensen L., Hanse B.F., Nordgaard-Lassen I., Christensen S., Avnstroem S., Ras-mussen S.N., Rumessen J.J. 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.
  76. Pardi D.S., Loftus E.V., Jr., Tremaine W.J., Sandborn W.J. Treatment of refractory microscopic colitis with azathioprine and 6-mercaptopurine. Gastroenterology 2001; 120: 1483—1484.
  77. Riddell I., 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.
  78. Esteve M., Mahadevan U., Sainz E., Rodriguez E., Salas A., Fernandez-Banares F. Efficacy of anti-TNF therapies in refractory microscopic colitis. J Crohns Colitis 2011; 5: 612—618.
  79. Münch A., Ignatova S., Ström M. Adalimumab in budesonide and methotrexate refractory collagenous colitis. Scand J Gastroenterol 2012; 47: 59—63.

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