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Colitis pp 107-140 | Cite as

Inflammatory Bowel Diseases

  • Karel Geboes
  • Olivier Dewit
  • Tom G. Moreels
  • Gavino Faa
  • Anne Jouret-Mourin
Chapter

Abstract

Inflammatory bowel disease (IBD) is a group of chronic idiopathic inflammatory conditions. The two major types are ulcerative colitis (UC) which affects the colon and Crohn’s disease (CD) which can involve the whole gastrointestinal tract but is most common in the terminal ileum and colon. There is a genetic predisposition for IBD, and patients with this condition are more prone to the development of malignancy. Further types to be considered are indeterminate colitis (IC) and inflammatory bowel disease unclassified (IBDU). These are essentially “temporary diagnoses” when the difference between UC and CD cannot be established definitely at the time of presentation. IC should be used when examination of surgical samples is available together with clinical, serological, and imaging data, while IBDU is used for patients from whom only endoscopic biopsies are available. CD and UC must be considered in the differential diagnosis of clinically acute colitis because of differences in treatment strategies between infections and IBD. The differential diagnosis is particularly important when the complaints are persisting. Histology plays a key role in the diagnosis. Major diagnostic features of UC are architectural distortion and basal plasmacytosis. It has been suggested that “microscopic colitis” would also be member of the chronic inflammatory bowel diseases.

Keywords

Inflammatory bowel disease (IBD) Ulcerative colitis Crohn’s disease Crypt architecture Crypt atrophy Bifid crypt Crypt distortion Basal plasmacytosis Active inflammatory parameters Non-active inflammatory parameters Cryptitis Crypt abscess Quiescent disease Inactive disease Disease activity Activity score Histological activity score Cytomegalovirus (CMV) Paneth cell metaplasia Ulceration Erosion Mucin depletion Transmucosal inflammation Segmental inflammation Skip area Transmural inflammation Fistula Granuloma Aphthoid ulcer Epithelioid cell Microgranuloma CARD15/NOD2 Toll-like receptor Skip lesion Focal inflammation Patchy inflammation Pseudopyloric metaplasia Hypercrinia Indeterminate colitis IBD unclassified Effect of treatment Multistep biopsies 

References

  1. 1.
    Pera A, Bellardo P, Caldera A, et al. Colonoscopy in inflammatory bowel disease. Diagnostic accuracy and proposal of endoscopic score. Gastroenterology. 1987;92:181–5.CrossRefPubMedGoogle Scholar
  2. 2.
    Broome U, Bergquist A. Primary sclerosing cholangitis, inflammatory bowel disease, and colon cancer. Semin Liver Dis. 2006;26:31–41.CrossRefPubMedGoogle Scholar
  3. 3.
    Loftus EV Jr, Harewood GC, Loftus CG, et al. PSC-IBD: a unique form of inflammatory bowel disease associated with primary sclerosing cholangitis. Gut. 2005;54:91–6.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Joo M, Abreu-E-Lima P, Farraye F, et al. Pathologic features of ulcerative colitis in patients with primary sclerosing cholangitis: a case-control study. Am J Surg Pathol. 2009;33:854–62.CrossRefPubMedGoogle Scholar
  5. 5.
    Jörgensen KK, Grzyb K, Lundin KEA, et al. Inflammatory bowel disease in patients with primary sclerosing cholangitis: clinical characterization in liver transplanted and nontransplanted patients. Inflamm Bowel Dis. 2012;18:536–45.CrossRefPubMedGoogle Scholar
  6. 6.
    Wright R, Truelove SR. Serial rectal biopsy in ulcerative colitis during the course of a controlled therapeutic trial of various diets. Am J Dig Dis. 1966;11:847–57.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Riley SA, Mani V, Goodman MJ, et al. Microscopic activity in ulcerative colitis: what does it mean? Gut. 1991;32:174–8.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Hefti MM, Chessin DB, Harpaz NH, et al. Severity of inflammation as a predictor of colectomy in patients with chronic ulcerative colitis. Dis Colon Rectum. 2009;52:193–7.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Nostrant TT, Kumar NB, Appelman HD. Histopathology differentiates acute self-limited colitis from ulcerative colitis. Gastroenterology. 1987;92:318–28.CrossRefPubMedGoogle Scholar
  10. 10.
    Therkildsen MH, Jensen BN, Stubbe P, Rasmussen TS. The final outcome of patients presenting with their first episode of acute diarrhea and an inflamed mucosa with preserved crypt architecture. A clinicopathologic study. Scand J Gastroenterol. 1989;24:158–64.CrossRefPubMedGoogle Scholar
  11. 11.
    Odze R, Antonioli D, Peppercorn M, et al. Effect of topical 5-amino-salicylic acid (5-ASA) therapy on rectal mucosal biopsy morphology in chronic ulcerative colitis. Am J Surg Pathol. 1993;17:869–75.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Rubio CA, Johansson C, Uribe A, Kock J. A quantitative method of estimating inflammation in the rectal mucosa. IV. Ulcerative colitis in remission. Scand J Gastroenterol. 1982;17:1077–81.PubMedPubMedCentralGoogle Scholar
  13. 13.
    Geboes K, El-Deeb G, El-Haddad S, Desmet VJ. Challenges in ulcerative colitis; the pathologist’s point of view. Acta Endosc. 1994;24:313–26.CrossRefGoogle Scholar
  14. 14.
    Schumacher G, Kollberg B, Sandstedt B. A prospective study of first attacks of inflammatory bowel disease and infectious colitis. Histologic course during the 1st year after presentation. Scand J Gastroenterol. 1994;29:318–32.CrossRefPubMedGoogle Scholar
  15. 15.
    Surawicz C. What’s the best way to differentiate infectious colitis (acute self-limited colitis) from IBD? Inflamm Bowel Dis. 2008;14:s157–8.CrossRefPubMedGoogle Scholar
  16. 16.
    Sachar DB, Andrews H, Farmer RG, et al. Proposed classification of patient subgroups in Crohn’s disease. Working team report 4. Gastroenterol Int. 1992;3:141–54.Google Scholar
  17. 17.
    Vasiliauskas EA, Plevy SE, Landers CJ, et al. Perinuclear antineutrophil cytoplasmic antibodies in patients with Crohn’s disease define a clinical subgroup. Gastroenterology. 1996;110:1810–9.CrossRefPubMedGoogle Scholar
  18. 18.
    Geboes K, Ectors N. Diagnosis of ulcerative colitis in endoscopic biopsies. Hepato-Gastroenterology. 1989;36:188–92.PubMedPubMedCentralGoogle Scholar
  19. 19.
    Forbes E, et al. Immunopathogenesis of experimental ulcerative colitis is mediated by eosinophil peroxidase. J Immunol. 2004;172:5664–75.CrossRefPubMedGoogle Scholar
  20. 20.
    Mir A, et al. Elevated serum eotaxin levels in patients with inflammatory bowel disease. Am J Gastroenterol. 2002;97:1452–7.CrossRefPubMedGoogle Scholar
  21. 21.
    Heatley RV, James PD. Eosinophils in the rectal mucosa. A simple method of predicting the outcome of ulcerative proctocolitis? Gut. 1979;20:787–91.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Bischoff SC, Mayer J, Nguyen QT, et al. Immunnohistological assessment of intestinal eosinophil activation in patients with eosinophilic gastroenteritis and inflammatory bowel disease. Am J Gastroenterol. 1999;94:3521–9.CrossRefPubMedGoogle Scholar
  23. 23.
    Raab Y, Fredens K, Gerdin B, Hällgren R. Eosinophil activation in ulcerative colitis: studies on mucosal release and localization of eosinophil granule constituents. Dig Dis Sci. 1998;43:1061–70.CrossRefPubMedGoogle Scholar
  24. 24.
    Bitton A, Peppercorn MA, Antonioli DA, et al. Clinical, biological, and histologic parameters as predictors of relapse in ulcerative colitis. Gastroenterology. 2001;120:13–20.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Bessissow T, Lemmens B, Ferrante M, et al. Prognostic value of serologic and histologic markers on clinical relapse in ulcerative colitis patients with mucosal healing. Am J Gastroenterol. 2012;107:1684–92.CrossRefPubMedGoogle Scholar
  26. 26.
    Keren DF, Appelman HD, Dobbins WO 3rd, et al. Correlation of histopathologic evidence of disease activity with the presence of immunoglobulin-containing cells in the colons of patients with inflammatory bowel disease. Hum Pathol. 1984;15:757–63.CrossRefPubMedGoogle Scholar
  27. 27.
    Truelove SC, Richards WC. Biopsy studies in ulcerative colitis. Br Med J. 1956;1:1315–8.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Bressenot A, Geboes K, Vignaud JM, et al. Microscopic features for initial diagnosis and disease activity evaluation in inflammatory bowel disease. Inflamm Bowel Dis. 2013;19:1745–52.CrossRefPubMedGoogle Scholar
  29. 29.
    Kandiel A, Lashner B. Cytomegalovirus colitis complicating inflammatory bowel disease. Am J Gastroenterol. 2006;101:2857–65.CrossRefPubMedGoogle Scholar
  30. 30.
    Ayre K, Warren BF, Jeffery K, Travis SP. The role of CMV in steroid-resistant ulcerative colitis: a systematic review. J Crohns Colitis. 2009;3:141–8.CrossRefPubMedGoogle Scholar
  31. 31.
    Kuwabara A, Okamoto H, Suda T, et al. Clinicopathologic characteristics of clinically relevant cytomegalovirus infection in inflammatory bowel disease. J Gastroenterol. 2007;42:823–9.CrossRefPubMedGoogle Scholar
  32. 32.
    Markowitz J, Kahn E, Grancher K, et al. Atypical rectosigmoid histology in children with newly diagnosed ulcerative colitis. Am J Gastroenterol. 1993;88:2034–7.PubMedPubMedCentralGoogle Scholar
  33. 33.
    Robert ME, Tang L, Hao M, Reyes-Mugica M. Patterns of inflammation in mucosal biopsies of ulcerative colitis. Perceived differences in pediatric populations are limited to children younger than 10 years. Am J Surg Pathol. 2004;28:183–9.CrossRefPubMedGoogle Scholar
  34. 34.
    Washington K, Greenson JK, Montgomery E, et al. Histopathology of ulcerative colitis in initial rectal biopsy in children. Am J Surg Pathol. 2002;26:1441–9.CrossRefPubMedGoogle Scholar
  35. 35.
    Geboes K, Van Eyken P. My approach to indeterminate colitis: the role of the pathologist. J Clin Pathol. 2009;62:201–5.CrossRefPubMedGoogle Scholar
  36. 36.
    Villanacci V, Antonelli E, Geboes K, et al. Histological healing in inflammatory bowel disease: a still unfulfilled promise. World J Gastroenterol. 2013;19:968–78.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Mosli MH, Feagan B, Sandborn WJ, et al. Histologic evaluation of disease activity in ulcerative colitis: a systematic review of histological disease activity indices. Inflamm Bowel Dis. 2014;20:564–75.CrossRefPubMedGoogle Scholar
  38. 38.
    Dourmashkin RR, Davies H, Wells C, Shah D, et al. Epithelial patchy necrosis in Crohn’s disease. Hum Pathol. 1983;14:643–8.CrossRefPubMedGoogle Scholar
  39. 39.
    Dvorak A, Connell AB, Dickersin GR. Crohn’s disease: a scanning electron microscopic study. Hum Pathol. 1979;10:165–77.CrossRefPubMedGoogle Scholar
  40. 40.
    Cuvelier CA, Quatacker J, Mielants H, et al. M cells are damaged and increased in number in inflamed human ileal mucosa. Eur J Morphol. 1993;31:87–91.PubMedPubMedCentralGoogle Scholar
  41. 41.
    Fujimura Y, Hosobe M, Kihara T. Ultrastructural study of M cells from colonic lymphoid nodules obtained by colonoscopic biopsy. Dig Dis Sci. 1992;37:1089–98.CrossRefPubMedGoogle Scholar
  42. 42.
    Tanaka M, Riddell RH. The pathological diagnosis and differential diagnosis of Crohn’s disease. Hepato-Gastroenterology. 1990;37:18–31.PubMedPubMedCentralGoogle Scholar
  43. 43.
    Sankey EA, Dhillon AP, Anthony A, et al. Early mucosal changes in Crohn’s disease. Gut. 1993;34:375–81.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Sanders DS. Mucosal integrity and barrier function in the pathogenesis of early lesions in Crohn’s disease. J Clin Pathol. 2005;58:568–72.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Maunoury V, Mordon S, Geboes K, et al. Early vascular changes in Crohn’s disease: an endoscopic fluorescence study. Endoscopy. 2000;32:700–5.CrossRefPubMedGoogle Scholar
  46. 46.
    Heresbach D, Heresbach-Le Berre N, Ramée MP, et al. Fréquence et valeur pronostique du granulome épithélioïde au cours des maladies inflammatoires chroniques de l’intestin. Gastroenterol Clin Biol. 1999;23:1376–87.PubMedPubMedCentralGoogle Scholar
  47. 47.
    Geboes K, Vantrappen G. The value of colonoscopy in the diagnosis of Crohn’s disease. Gastrointest Endosc. 1975;22:18–23.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Jouret A, Mainguet P. Diagnostic value of systematic endoscopic biopsies in ileocolonic Crohn’s disease. Acta Gastroenterol Belg. 1993;56:C71.Google Scholar
  49. 49.
    Chambers TJ, Morson BC. The granuloma in Crohn’s disease. Gut. 1979;20:269–74.CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Baert F, Hart J, Blackstone MO. A case of diclofenac-induced colitis with focal granulomatous change. Am J Gastroenterol. 1995;90:1871–3.PubMedPubMedCentralGoogle Scholar
  51. 51.
    Mathew RC, Weinstock JV. Granuloma formation. In: Targan SR, Shanahan F, editors. Inflammatory bowel disease: from bench to bedside. Baltimore: Williams & Wilkins; 1994. p. 151–9.Google Scholar
  52. 52.
    Sanders DSA. The differential diagnosis of Crohn’s disease and ulcerative colitis. Baillieres Clin Gastroenterol. 1998;12:19–33.CrossRefPubMedGoogle Scholar
  53. 53.
    Chiba M. Crohn’s disease associated with diffuse lymphoid hyperplasia of the large intestine: a possible role of the lymph follicle in HLA-DR expression on epithelium. Intern Med. 1992;31:1271–6.CrossRefPubMedGoogle Scholar
  54. 54.
    Rotterdam H, Korelitz BI, Sommers SC. Microgranulomas in grossly normal rectal mucosa in Crohn’s disease. Am J Clin Pathol. 1977;67:550–4.CrossRefPubMedGoogle Scholar
  55. 55.
    Surawicz CM, Rubin CE. Epithelioid granuloma and related histologic features which may differentiate Crohn’s disease from ulcerative colitis in rectal biopsies. In: Rachmilewitz D, editor. Inflammatory bowel diseases. The Hague: Martinus Nijhoff; 1982. p. 19–26.CrossRefGoogle Scholar
  56. 56.
    Sandmeier D, Bouzourene H. Microscopic colitis with giant cells: a rare new histopathologic subtype? Int J Surg Pathol. 2004;12:45–8.CrossRefPubMedGoogle Scholar
  57. 57.
    Kayser K, Probst F, Gabius HJ, et al. Are there characteristic alterations of lung tissue associated with Crohn’s disease. Pathol Res Pract. 1990;186:485–90.CrossRefPubMedGoogle Scholar
  58. 58.
    Desmet VJ, Geboes K. Liver lesions in inflammatory bowel disorders. J Pathol. 1987;151:247–55.CrossRefPubMedGoogle Scholar
  59. 59.
    Van Patter WN, Bargen JA, Dockerty MB, et al. Regional enteritis. Gastroenterology. 1954;26:347–75.Google Scholar
  60. 60.
    Kelly JK, Sutherland LR. The chronological sequence in the pathology of Crohn’s disease. J Clin Gastroenterol. 1988;10:28–33.CrossRefPubMedGoogle Scholar
  61. 61.
    Roberts PL, Schoetz DJ, Pricolo R, et al. Clinical course of Crohn’s disease in older patients. A retrospective study. Dis Colon Rectum. 1990;33:458–62.CrossRefPubMedGoogle Scholar
  62. 62.
    Markowitz J, Kahn E, Daum F. Prognostic significance of epithelioid granulomas found in rectosigmoid biopsies at the initial presentation of pediatric Crohn’s disease. J Pediatr Gastroenterol Nutr. 1989;9:182–6.CrossRefPubMedGoogle Scholar
  63. 63.
    Pötzi R, Walgram M, Lochs H, et al. Diagnostic significance of endoscopic biopsy in Crohn’s disease. Endoscopy. 1989;21:60–2.CrossRefPubMedGoogle Scholar
  64. 64.
    Domizio P. Pathology of chronic inflammatory bowel disease in children. Baillieres Clin Gastroenterol. 1994;8:35–63.CrossRefPubMedGoogle Scholar
  65. 65.
    Theodossi A, Spiegelhalter DJ, Jass J, et al. Observer variation and discriminatory value of biopsy features in inflammatory bowel disease. Gut. 1994;35:961–8.CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Surawicz CM. Serial sectioning of a portion of a rectal biopsy detects more focal abnormalities. A prospective study of patients with inflammatory bowel disease. Dig Dis Sci. 1982;27:434–6.CrossRefPubMedGoogle Scholar
  67. 67.
    Smedh K, Olaison G, Franzén L, et al. Endoscopic and external bowel changes and histopathology in patients with Crohn’s disease. Br J Surg. 1995;82:191–4.CrossRefPubMedGoogle Scholar
  68. 68.
    Wolfson DM, Sachar DB, Cohen A, et al. Granulomas do not affect postoperative recurrence rates in Crohn’s disease. Gastroenterology. 1982;83:405–9.PubMedPubMedCentralGoogle Scholar
  69. 69.
    Glass RE, Baker WNW. The role of the granuloma in recurrent Crohn’s disease. Gut. 1976;17:75–7.CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Heresbach D, Alexandre JL, Branger B, et al. Frequency and significance of granulomas in a cohort of incident cases of Crohn’s disease. Gut. 2005;54:215–22.CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Pierik M, De Hertogh G, Vermeire S, et al. Epithelioid granulomas, pattern recognition receptors, and phenotypes of Crohn’s disease. Gut. 2005;54:223–7.CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Shaoul R, Karban A, Weiss B, et al. NOD2/CARD15 mutations and presence of granulomas in pediatric and adult Crohn’s disease. Inflamm Bowel Dis. 2004;10:709–14.CrossRefPubMedGoogle Scholar
  73. 73.
    Heresbach D, Gicquel-Douabin V, Birebent B, et al. NOD2/CARD15 gene polymorphism in Crohn’s disease: a genotype phenotype analysis. Eur J Gastroenterol Hepatol. 2004;16:55–62.CrossRefPubMedGoogle Scholar
  74. 74.
    Lennard-Jones JE. Crohn’s disease: definition, pathogenesis and aetiology. In: Wright R, editor. Recent advances in gastrointestinal pathology. London: WB Saunders; 1980. p. 173–89.Google Scholar
  75. 75.
    Hamilton SR. Diagnosis and comparison of ulcerative colitis and Crohn’s disease involving the colon. In: Norris HT, editor. Pathology of the colon, small intestine and anus. New York: Churchill Livingstone; 1983. p. 1.Google Scholar
  76. 76.
    Jenkins D, Balsitis M, Gallivan S, et al. Guidelines for the initial biopsy diagnosis of suspected chronic idiopathic inflammatory bowel disease. The British Society of Gastroenterology Initiative. J Clin Pathol. 1997;50:93–10511.CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Jenkins D, Goodall A, Drew K, et al. What is colitis? Statistical approach to distinguishing clinically important inflammatory change in rectal biopsy specimens. J Clin Pathol. 1988;41:72–9.CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Surawicz CM, Belic L. Rectal biopsy helps to distinguish acute self-limited colitis from idiopathic inflammatory bowel disease. Gastroenterology. 1984;86:104–13.PubMedPubMedCentralGoogle Scholar
  79. 79.
    Schmitz-Moormann P, Himmelmann GW. Does quantitative histology of rectal biopsy improve the differential diagnosis of Crohn’s disease and ulcerative colitis in adults? Pathol Res Pract. 1988;183:481–8.CrossRefPubMedGoogle Scholar
  80. 80.
    Seldenrijk CA, Morson BC, Meuwissen SGM, et al. Histopathological evaluation of colonic mucosal biopsy specimens in chronic inflammatory bowel disease: diagnostic implications. Gut. 1991;32:1514–20.CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Shepherd NA. Granulomas in the diagnosis of intestinal Crohn’s disease: a myth exploded. Histopathology. 2002;41:166–8.CrossRefPubMedGoogle Scholar
  82. 82.
    Tanaka M, Riddell RH, Saito H, et al. Morphologic criteria applicable to biopsy specimens for effective distinction of inflammatory bowel disease from other forms of colitis and of Crohn’s disease from ulcerative colitis. Scand J Gastroenterol. 1999;34:55–67.CrossRefPubMedGoogle Scholar
  83. 83.
    Tanaka M, Saito H, Fukuda S, et al. Simple mucosal biopsy criteria differentiating among Crohn’s disease, ulcerative colitis and other forms of colitis: measurement of validity. Scand J Gastroenterol. 2000;35:281–6.CrossRefPubMedGoogle Scholar
  84. 84.
    Schmitz-Moormann P, Schäg M. Histology of the lower intestinal tract in Crohn’s disease of children and adolescents. Pathol Res Pract. 1990;186:479–84.CrossRefPubMedGoogle Scholar
  85. 85.
    Geboes K, Ectors N, D’Haens G, et al. Is ileoscopy with biopsy worthwhile in patients presenting with symptoms of IBD. Am J Gastroenterol. 1998;93:201–6.CrossRefPubMedGoogle Scholar
  86. 86.
    Cuvelier C, Demetter P, Mielants H, et al. Interpretation of ileal biopsies: morphological features in normal and diseased mucosa. Histopathology. 2001;38:1–12.CrossRefPubMedGoogle Scholar
  87. 87.
    Courville EL, Siegerl CA, Vay T, et al. Isolated asymptomatic ileitis does not progress to overt Crohn disease on long-term follow-up despite features of chronicity in ileal biopsies. Am J Surg Pathol. 2009;33:1341–7.CrossRefPubMedGoogle Scholar
  88. 88.
    Bentley E, Jenkins D, Campbell F, et al. How could pathologists improve the initial diagnosis of colitis? Evidence from an international workshop. J Clin Pathol. 2002;55:955–60.CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Dejaco C, Osterreicher C, Angelberger S, Puspok A, et al. Diagnosing colitis: a prospective study on essential parameters for reaching a diagnosis. Endoscopy. 2003;35:1004–8.CrossRefPubMedGoogle Scholar
  90. 90.
    Escher JC, Ten Kate F, Lichtenbelt SK, et al. Value of rectosigmoidoscopy with biopsies for diagnosis of inflammatory bowel disease in children. Inflamm Bowel Dis. 2002;8:16–22.CrossRefPubMedGoogle Scholar
  91. 91.
    Gomes P, Du Boulay C, Smith CL, et al. Relationship between disease activity and colonoscopic findings in patients with colonic inflammatory bowel disease. Gut. 1986;27:92–5.CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    D’Haens G, Van Deventer S, Van Hogezand R, et al. Endoscopic and histological healing with infliximab anti-tumor necrosis factor antibodies in Crohn’s disease: a European multicenter trial. Gastroenterology. 1999;116:1029–34.CrossRefPubMedGoogle Scholar
  93. 93.
    Schmitz-Moorman P, Brandes JW, Jesdinsky H, et al. Relationships between drug regime and histology of rectal mucosa in CD. Pathol Res Pract. 1988;183:30–4.CrossRefGoogle Scholar
  94. 94.
    Magro F, Langner C, Driessen A, et al. European consensus on the histopathology of inflammatory bowel disease. J Crohns Colitis. 2013;7:827–51.CrossRefPubMedPubMedCentralGoogle Scholar
  95. 95.
    Price AB. Overlap in the spectrum of non-specific inflammatory bowel disease - “colitis indeterminate”. J Clin Pathol. 1978;31:567–77.CrossRefPubMedPubMedCentralGoogle Scholar
  96. 96.
    Kent TH, Ammon RK, DenBesten L. Differentiation of ulcerative colitis and regional enteritis. Arch Pathol. 1970;89:20–9.PubMedPubMedCentralGoogle Scholar
  97. 97.
    Branco BC, Harpaz N, Sachar D, et al. Colorectal carcinoma in indeterminate colitis. Inflamm Bowel Dis. 2009;15:1076–81.CrossRefPubMedGoogle Scholar
  98. 98.
    Geboes K, Colombel JF, Greenstein A, et al. Indeterminate colitis: a review of the concept – what’s in a name? Inflamm Bowel Dis. 2008;14:860–7.CrossRefGoogle Scholar
  99. 99.
    Silverberg M, Satsangi J, Ahmad T, et al. Toward an integrated clinical, molecular and serological classification of inflammatory bowel disease: report of a Working Party of the 2005 Montreal World Congress of Gastroenterology. Can J Gastroenterol. 2005;19(Suppl A):1A–32A.CrossRefGoogle Scholar
  100. 100.
    Sonnenberg A, Melton RD, Genta RM. Frequent occurrence of gastritis and duodenitis in patients with inflammatory bowel disease. Inflamm Bowel Dis. 2011;17:39–44.CrossRefPubMedGoogle Scholar
  101. 101.
    Parente F, Cucino C, Bollani S, et al. Focal gastric inflammatory infiltrates in inflammatory bowel diseases. Prevalence, immunohistochemical characteristics and diagnostic role. Am J Gastroenterol. 2000;95:705–11.CrossRefPubMedGoogle Scholar
  102. 102.
    Castellaneta SP, Afzzal NA, Greenberg M, et al. Diagnostic role of upper gastrointestinal endoscopy in pediatric inflammatory bowel disease. J Pediatr Gastroenterol Nutr. 2004;39:257–61.CrossRefPubMedGoogle Scholar
  103. 103.
    Lopes S, Figueiredo P, Portela F, et al. Capsule endoscopy in inflammatory bowel disease type unclassified and indeterminate colitis, serologically negative. Inflamm Bowel Dis. 2010;16:1663–8.CrossRefPubMedGoogle Scholar
  104. 104.
    Auvin S, Molinié F, Gower-Rousseau C, et al. Incidence, clinical presentation and location at diagnosis of pediatric inflammatory bowel disease: a prospective population-based study in northern France (1988-1999). J Pediatr Gastroenterol Nutr. 2005;41:49–55.CrossRefPubMedGoogle Scholar
  105. 105.
    Bentsen BS, Moum B, Ekbom A. Incidence of inflammatory bowel disease in children in southeastern Norway. A prospective population-based study 1990-94. Scand J Gastroenterol. 2002;37:540–5.CrossRefPubMedGoogle Scholar
  106. 106.
    Hildebrand H, Fredrikson B, Holmquist L, et al. Chronic inflammatory bowel disease in children and adolescents in Sweden. J Pediatr Gastroenterol Nutr. 1991;13:293–7.CrossRefPubMedGoogle Scholar
  107. 107.
    IBD Working group of the European Society for Paediatric Gastroenterology, Hepatology and Nutrition. Inflammatory bowel disease in children and adolescents: recommendations for diagnosis-the Porto criteria. J Pediatr Gastroenterol Nutr. 2005;41:1–7.CrossRefGoogle Scholar
  108. 108.
    Yantiss RK, Farraye FA, O’Brien MJ, et al. Prognostic significance or superficial fissuring ulceration in patients with severe “indeterminate” colitis. Am J Surg Pathol. 2006;30:165–70.CrossRefPubMedGoogle Scholar
  109. 109.
    Lee KS, Medline A, Shockey Q. Indeterminate colitis in the spectrum of inflammatory bowel disease. Arch Pathol Lab Med. 1979;103:173–6.PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Karel Geboes
    • 1
    • 2
  • Olivier Dewit
    • 3
  • Tom G. Moreels
    • 3
  • Gavino Faa
    • 4
  • Anne Jouret-Mourin
    • 5
  1. 1.Department of PathologyGhent University HospitalGhentBelgium
  2. 2.Department of PathologyKU LeuvenLeuvenBelgium
  3. 3.Department of GastroenterologyCliniques Universitaires St Luc, UCLBrusselsBelgium
  4. 4.Division of Pathology, Department of Surgical SciencesUniversity Hospital San Giovanni di Dio, University of CagliariCagliariItaly
  5. 5.Department of PathologyCliniques Universitaires St Luc, UCLBrusselsBelgium

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