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Biopsy interpretation of colonic biopsies when inflammatory bowel disease is excluded

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Abstract

The interpretation of colonic biopsies related to inflammatory conditions can be challenging because the colorectal mucosa has a limited repertoire of morphologic responses to various injurious agents. Only few processes have specific diagnostic features, and many of the various histological patterns reflect severity and duration of the disease. Importantly the correlation with endoscopic and clinical information is often cardinal to arrive at a specific diagnosis in many cases.

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References

  1. Kumar NB, Nostrant TT, Appelman HD. The histopathologic spectrum of acute self-limited colitis (acute infectious-type colitis). Am J Surg Pathol. 1982;6:523–9.

    PubMed  CAS  Google Scholar 

  2. Navaneethan U, Giannella RA. Mechanisms of infectious diarrhea. Nat Clin Pract Gastroenterol Hepatol. 2008;5:637–47.

    PubMed  Google Scholar 

  3. Lamps LW. Infective disorders of the gastrointestinal tract. Histopathology. 2007;50:55–63.

    PubMed  CAS  Google Scholar 

  4. Navaneethan U, Giannella RA. Infectious colitis. Curr Opin Gastroenterol. 2011;27:66–71.

    Google Scholar 

  5. Prescott RJ, Harris M, Banerjee SS. Fungal infections of the small and large intestine. J Clin Pathol. 1992;45:806–11.

    PubMed  CAS  Google Scholar 

  6. Schumacher G, Sandstedt B, Mollby R, Kollberg B. Clinical and histologic features differentiating non-relapsing colitis from first attacks of inflammatory bowel disease. Scand J Gastroenterol. 1991;26:151–61.

    PubMed  CAS  Google Scholar 

  7. Mantzaris GJ. Endoscopic diagnosis of infectious colitis. Ann Gastroenterol. 2007;20:71–4.

    Google Scholar 

  8. Surawicz CM, Haggitt RC, Husseman M, McFarland LV. Mucosal biopsy diagnosis of colitis: acute self-limited colitis and idiopathic inflammatory bowel disease. Gastroenterology. 1994;107:755–63.

    PubMed  CAS  Google Scholar 

  9. Carpenter HA, Talley NJ. The importance of clinicopathological correlation in the diagnosis of inflammatory conditions of the colon: histological patterns with clinical implications. Am J Gastroenterol. 2000;95:878–96.

    PubMed  CAS  Google Scholar 

  10. Sherman PM, Ossa JC, Wine E. Bacterial infections: new and emerging enteric pathogens. Curr Opin Gastroenterol. 2010;26:1–4.

    PubMed  Google Scholar 

  11. Tarr PI. Escherichia coli O157:H7: clinical, diagnostic, and epidemiological aspects of human infection. Clin Infect Dis. 1995;20:1–8 (quiz 9–10).

    Google Scholar 

  12. Griffin PM, Olmstead LC, Petras RE. Escherichia coli O157:H7-associated colitis. A clinical and histological study of 11 cases. Gastroenterology. 1990;99:142–9.

    PubMed  CAS  Google Scholar 

  13. Bielaszewska M, Karch H. Consequences of enterohaemorrhagic Escherichia coli infection for the vascular endothelium. Thromb Haemost. 2005;94:312–8.

    PubMed  CAS  Google Scholar 

  14. Kelly J, Oryshak A, Wenetsek M, Grabiec J, Handy S. The colonic pathology of Escherichia coli O157:H7 infection. Am J Surg Pathol. 1990;14:87–92.

    PubMed  CAS  Google Scholar 

  15. Ananthakrishnan AN. Clostridium difficile infection: epidemiology, risk factors and management. Nat Rev Gastroenterol Hepatol. 2011;8:17–26.

    PubMed  CAS  Google Scholar 

  16. Freeman J, Bauer MP, Baines SD, Corver J, Fawley WN, Goorhuis B, et al. The changing epidemiology of Clostridium difficile infections. Clin Microbiol Rev. 2010;23:529–49.

    PubMed  CAS  Google Scholar 

  17. Drudy D, Harnedy N, Fanning S, O’Mahony R, Kyne L. Isolation and characterisation of toxin A-negative, toxin B-positive Clostridium difficile in Dublin, Ireland. Clin Microbiol Infect. 2007;13:298–304.

    PubMed  CAS  Google Scholar 

  18. Hurley BW, Nguyen CC. The spectrum of pseudomembranous enterocolitis and antibiotic-associated diarrhea. Arch Intern Med. 2002;162:2177–84.

    PubMed  Google Scholar 

  19. Price AB, Davies DR. Pseudomembranous colitis. J Clin Pathol. 1977;30:1–12.

    PubMed  CAS  Google Scholar 

  20. Bartlett JG. Historical perspectives on studies of Clostridium difficile and C. difficile infection. Clin Infect Dis. 2008;46(Suppl 1):S4–11.

    PubMed  Google Scholar 

  21. Price AB. Histopathology of clostridial gut disease in man. In: Borriello SP, editor. Clostridia in gastrointestinal disease. Boca Raton: CRC; 1985. p. 177.

    Google Scholar 

  22. Schiffman R. Signet-ring cells associated with pseudomembranous colitis. Am J Surg Pathol. 1996;20:599–602.

    PubMed  CAS  Google Scholar 

  23. Wang K, Weinrach D, Lal A, Musunuri S, Ramirez J, Ozer O, et al. Signet-ring cell change versus signet-ring cell carcinoma: a comparative analysis. Am J Surg Pathol. 2003;27:1429–33.

    PubMed  Google Scholar 

  24. Dignan CR, Greenson JK. Can ischemic colitis be differentiated from C. difficile colitis in biopsy specimens? Am J Surg Pathol. 1997;21:706–10.

    PubMed  CAS  Google Scholar 

  25. Papaconstantinou HT, Thomas JS. Bacterial colitis. Clin Colon Rectal Surg. 2007;20:18–27.

    PubMed  Google Scholar 

  26. El-Maraghi NR, Mair NS. The histopathology of enteric infection with Yersinia pseudotuberculosis. Am J Clin Pathol. 1979;71:631–9.

    PubMed  CAS  Google Scholar 

  27. Ebringer A, Wilson C. HLA molecules, bacteria and autoimmunity. J Med Microbiol. 2000;49:305–11.

    PubMed  CAS  Google Scholar 

  28. Matsumoto T, Iida M, Matsui T, Sakamoto K, Fuchigami T, Haraguchi Y, et al. Endoscopic findings in Yersinia enterocolitica enterocolitis. Gastrointest Endosc. 1990;36:583–7.

    PubMed  CAS  Google Scholar 

  29. Gleason TH, Patterson SD. The pathology of Yersinia enterocolitica ileocolitis. Am J Surg Pathol. 1982;6:347–55.

    PubMed  CAS  Google Scholar 

  30. Lamps LW, Havens JM, Gilbrech LJ, Dube PH, Scott MA. Molecular biogrouping of pathogenic Yersinia enterocolitica: development of a diagnostic PCR assay with histologic correlation. Am J Clin Pathol. 2006;125:658–64.

    PubMed  CAS  Google Scholar 

  31. Misra SP, Misra V, Dwivedi M, Gupta SC. Colonic tuberculosis: clinical features, endoscopic appearance and management. J Gastroenterol Hepatol. 1999;14:723–9.

    PubMed  CAS  Google Scholar 

  32. Tandon HD, Prakash A. Pathology of intestinal tuberculosis and its distinction from Crohn’s disease. Gut. 1972;13:260–9.

    PubMed  CAS  Google Scholar 

  33. Pulimood AB, Amarapurkar DN, Ghoshal U, Phillip M, Pai CG, Reddy DN, et al. Differentiation of Crohn’s disease from intestinal tuberculosis in India in 2010. World J Gastroenterol. 2011;17:433–43.

    PubMed  Google Scholar 

  34. Alvares JF, Devarbhavi H, Makhija P, Rao S, Kottoor R. Clinical, colonoscopic, and histological profile of colonic tuberculosis in a tertiary hospital. Endoscopy. 2005;37:351–6.

    PubMed  CAS  Google Scholar 

  35. Gaffney EF, Condell D, Majmudar B, Nolan N, McDonald GS, Griffin M, et al. Modification of caecal lymphoid tissue and relationship to granuloma formation in sporadic ileocaecal tuberculosis. Histopathology. 1987;11:691–704.

    PubMed  CAS  Google Scholar 

  36. van Mook WN, Koek GH, van der Ven AJ, Ceelen TL, Bos RP. Human intestinal spirochaetosis: any clinical significance? Eur J Gastroenterol Hepatol. 2004;16:83–7.

    PubMed  Google Scholar 

  37. Korner M, Gebbers JO. Clinical significance of human intestinal spirochetosis—a morphologic approach. Infection. 2003;31:341–9.

    PubMed  CAS  Google Scholar 

  38. Carr NJ, Mahajan H, Tan KL, Sharma R. The histological features of intestinal spirochetosis in a series of 113 patients. Int J Surg Pathol. 2010;18:144–8.

    PubMed  Google Scholar 

  39. Lee FD, Kraszewski A, Gordon J, Howie JG, McSeveney D, Harland WA. Intestinal spirochaetosis. Gut. 1971;12:126–33.

    PubMed  CAS  Google Scholar 

  40. Haque R, Huston CD, Hughes M, Houpt E, Petri WA Jr. Amebiasis. N Engl J Med. 2003;348:1565–73.

    PubMed  Google Scholar 

  41. McMillan A, Gilmour HM, McNeillage G, Scott GR. Amoebiasis in homosexual men. Gut. 1984;25:356–60.

    PubMed  CAS  Google Scholar 

  42. Herbinger KH, Fleischmann E, Weber C, Perona P, Loscher T, Bretzel G. Epidemiological, clinical, and diagnostic data on intestinal infections with Entamoeba histolytica and Entamoeba dispar among returning travelers. Infection. 2011;39:527–35.

  43. Leung J, Chin A. Amebic colitis. Gastrointest Endosc. 2002;56:732.

    PubMed  Google Scholar 

  44. Prathap K, Gilman R. The histopathology of acute intestinal amebiasis. A rectal biopsy study. Am J Pathol. 1970;60:229–46.

    PubMed  CAS  Google Scholar 

  45. Mitchell LM, Mora LO. Amebiasis simulating idiopathic inflammatory disease of the colon. J Miss State Med Assoc. 1971;12:469–82.

    PubMed  CAS  Google Scholar 

  46. Yamamoto-Furusho JK, Torijano-Carrera E. Intestinal protozoa infections among patients with ulcerative colitis: prevalence and impact on clinical disease course. Digestion. 2010;82:18–23.

    PubMed  Google Scholar 

  47. Schuster FL, Ramirez-Avila L. Current world status of Balantidium coli. Clin Microbiol Rev. 2008;21:626–38.

    PubMed  Google Scholar 

  48. Hulman G, Taylor LA. Entamoeba histolytica: demonstration by PAS/Martius yellow technique. Med Lab Sci. 1987;44:396–7.

    PubMed  CAS  Google Scholar 

  49. Galiatsatos P, Shrier I, Lamoureux E, Szilagyi A. Meta-analysis of outcome of cytomegalovirus colitis in immunocompetent hosts. Dig Dis Sci. 2005;50:609–16.

    PubMed  Google Scholar 

  50. Baroco AL, Oldfield EC. Gastrointestinal cytomegalovirus disease in the immunocompromised patient. Curr Gastroenterol Rep. 2008;10:409–16.

    PubMed  Google Scholar 

  51. Le ST, Lee SS, Prideaux L, Block AA, Moore GT. Primary cytomegalovirus ileitis complicated by massive gastrointestinal haemorrhage in a patient with steroid refractory Crohn’s disease. Intern Med J. 2010;40:788–91.

    PubMed  CAS  Google Scholar 

  52. Hunt NAC, Jewell D, Mortensen N, Warren B. Cytomegalovirus infection complicating ulcerative colitis. CPD Bull Cell Pathol. 1999;1:72.

    Google Scholar 

  53. Cheung AN, Ng IO. Cytomegalovirus infection of the gastrointestinal tract in non-AIDS patients. Am J Gastroenterol. 1993;88:1882–6.

    PubMed  CAS  Google Scholar 

  54. Francis ND, Boylston AW, Roberts AH, Parkin JM, Pinching AJ. Cytomegalovirus infection in gastrointestinal tracts of patients infected with HIV-1 or AIDS. J Clin Pathol. 1989;42:1055–64.

    PubMed  CAS  Google Scholar 

  55. Warren BF, Edwards CM, Travis SP. ‘Microscopic colitis’: classification and terminology. Histopathology. 2002;40:374–6.

    PubMed  CAS  Google Scholar 

  56. Chande N, Driman DK, Reynolds RP. Collagenous colitis and lymphocytic colitis: patient characteristics and clinical presentation. Scand J Gastroenterol. 2005;40:343–7.

    PubMed  Google Scholar 

  57. Giardiello FM, Lazenby AJ, Bayless TM, Levine EJ, Bias WB, Ladenson PW, et al. Lymphocytic (microscopic) colitis. Clinicopathologic study of 18 patients and comparison to collagenous colitis. Dig Dis Sci. 1989;34:1730–8.

    PubMed  CAS  Google Scholar 

  58. Baert F, Wouters K, D’Haens G, Hoang P, Naegels S, D’Heygere F, et al. Lymphocytic colitis: a distinct clinical entity? A clinicopathological confrontation of lymphocytic and collagenous colitis. Gut. 1999;45:375–81.

    PubMed  CAS  Google Scholar 

  59. Pardi DS, Kelly CP. Microscopic colitis. Gastroenterology. 2011;140:1155–65.

    PubMed  Google Scholar 

  60. El-Matary W, Girgis S, Huynh H, Turner J, Diederichs B. Microscopic colitis in children. Dig Dis Sci. 2010;55:1996–2001.

    PubMed  Google Scholar 

  61. Bogomoletz WV. Collagenous, microscopic and lymphocytic colitis. An evolving concept. Virchows Arch. 1994;424:573–9.

    PubMed  CAS  Google Scholar 

  62. Bohr J, Larsson LG, Eriksson S, Jarnerot G, Tysk C. Colonic perforation in collagenous colitis: an unusual complication. Eur J Gastroenterol Hepatol. 2005;17:121–4.

    PubMed  Google Scholar 

  63. Jarnerot G, Tysk C, Bohr J, Eriksson S. Collagenous colitis and fecal stream diversion. Gastroenterology. 1995;109:449–55.

    PubMed  CAS  Google Scholar 

  64. 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;45:123–6.

    PubMed  Google Scholar 

  65. Green PH, Yang J, Cheng J, Lee AR, Harper JW, Bhagat G. An association between microscopic colitis and celiac disease. Clin Gastroenterol Hepatol. 2009;7:1210–6.

    PubMed  Google Scholar 

  66. Matteoni CA, Goldblum JR, Wang N, Brzezinski A, Achkar E, Soffer EE. Celiac disease is highly prevalent in lymphocytic colitis. J Clin Gastroenterol. 2001;32:225–7.

    PubMed  CAS  Google Scholar 

  67. Freeman HJ. Collagenous colitis as the presenting feature of biopsy-defined celiac disease. J Clin Gastroenterol. 2004;38:664–8.

    PubMed  Google Scholar 

  68. Marteau P, Lavergne-Slove A, Lemann M, Bouhnik Y, Bertheau P, Becheur H, et al. Primary ileal villous atrophy is often associated with microscopic colitis. Gut. 1997;41:561–4.

    PubMed  CAS  Google Scholar 

  69. Sapp H, Ithamukkala S, Brien TP, Ayata G, Shaz B, Dorfman DM, et al. The terminal ileum is affected in patients with lymphocytic or collagenous colitis. Am J Surg Pathol. 2002;26:1484–92.

    PubMed  Google Scholar 

  70. Lewis FW, Warren GH, Goff JS. Collagenous colitis with involvement of terminal ileum. Dig Dis Sci. 1991;36:1161–3.

    PubMed  CAS  Google Scholar 

  71. O’Brien BH, McClymont K, Brown I. Collagenous ileitis: a study of 13 cases. Am J Surg Pathol. 2011;35:1151–7.

    PubMed  Google Scholar 

  72. Leung ST, Chandan VS, Murray JA, Wu TT. Collagenous gastritis: histopathologic features and association with other gastrointestinal diseases. Am J Surg Pathol. 2009;33:788–98.

    PubMed  Google Scholar 

  73. Koskela RM, Niemela SE, Lehtola JK, Bloigu RS, Karttunen TJ. Gastroduodenal mucosa in microscopic colitis. Scand J Gastroenterol. 2011;46:567–76.

    PubMed  Google Scholar 

  74. Beaugerie L, Pardi DS. Review article: drug-induced microscopic colitis—proposal for a scoring system and review of the literature. Aliment Pharmacol Ther. 2005;22:277–84.

    PubMed  CAS  Google Scholar 

  75. Beaugerie L, Luboinski J, Brousse N, Cosnes J, Chatelet FP, Gendre JP, et al. Drug induced lymphocytic colitis. Gut. 1994;35:426–8.

    PubMed  CAS  Google Scholar 

  76. Fernandez-Banares F, Esteve M, Espinos JC, Rosinach M, Forne M, Salas A, et al. Drug consumption and the risk of microscopic colitis. Am J Gastroenterol. 2007;102:324–30.

    PubMed  Google Scholar 

  77. Moneret-Vautrin DA, Delvaux M, Labouyrie E, El Gueddari Y, Morisset M, Hochard H. Collagenous colitis: possible link with isotretinoin. Eur Ann Allergy Clin Immunol. 2006;38:124–5.

    PubMed  CAS  Google Scholar 

  78. Geboes K. Lymphocytic, collagenous and other microscopic colitides: pathology and the relationship with idiopathic inflammatory bowel diseases. Gastroenterol Clin Biol. 2008;32:689–94.

    PubMed  CAS  Google Scholar 

  79. Jarnerot G, Hertervig E, Granno C, Thorhallsson E, Eriksson S, Tysk C, et al. Familial occurrence of microscopic colitis: a report on five families. Scand J Gastroenterol. 2001;36:959–62.

    PubMed  CAS  Google Scholar 

  80. Fine KD, Do K, Schulte K, Ogunji F, Guerra R, Osowski L, et al. High prevalence of celiac sprue-like HLA-DQ genes and enteropathy in patients with the microscopic colitis syndrome. Am J Gastroenterol. 2000;95:1974–82.

    PubMed  CAS  Google Scholar 

  81. Koskela RM, Karttunen TJ, Niemela SE, Lehtola JK, Ilonen J, Karttunen RA. Human leucocyte antigen and TNFalpha polymorphism association in microscopic colitis. Eur J Gastroenterol Hepatol. 2008;20:276–82.

    PubMed  CAS  Google Scholar 

  82. Jensen L, Munck LK. Elementary diet reduces diarrhoea associated with microscopic colitis. Scand J Gastroenterol. 2005;40:1495–6.

    PubMed  Google Scholar 

  83. Burgel N, Bojarski C, Mankertz J, Zeitz M, Fromm M, Schulzke JD. Mechanisms of diarrhea in collagenous colitis. Gastroenterology. 2002;123:433–43.

    PubMed  Google Scholar 

  84. Lee E, Schiller LR, Vendrell D, Santa Ana CA, Fordtran JS. Subepithelial collagen table thickness in colon specimens from patients with microscopic colitis and collagenous colitis. Gastroenterology. 1992;103:1790–6.

    PubMed  CAS  Google Scholar 

  85. Beaugerie L, Napoleon B, Ponchon T, Boyer J, Canard JM, Dalbies P, et al. Guidelines of the French Society for Digestive Endoscopy (SFED). Role of endoscopy in microscopic colitis. Endoscopy. 2005;37:97–8.

    PubMed  CAS  Google Scholar 

  86. Koulaouzidis A, Saeed AA. Distinct colonoscopy findings of microscopic colitis: not so microscopic after all? World J Gastroenterol. 2011;17:4157–65.

    PubMed  Google Scholar 

  87. Cimmino DG, Mella JM, Pereyra L, Luna PA, Casas G, Caldo I, et al. A colorectal mosaic pattern might be an endoscopic feature of collagenous colitis. J Crohns Colitis. 2010;4:139–43.

    PubMed  Google Scholar 

  88. Robert ME. Microscopic colitis: pathologic considerations, changing dogma. J Clin Gastroenterol. 2004;38:S18–26.

    PubMed  Google Scholar 

  89. Nyhlin N, Bohr J, Eriksson S, Tysk C. Systematic review: microscopic colitis. Aliment Pharmacol Ther. 2006;23:1525–34.

    PubMed  CAS  Google Scholar 

  90. Otegbayo JA, Otegbeye FM, Rotimi O. Microscopic colitis syndrome—a review article. J Natl Med Assoc. 2005;97:678–82.

    PubMed  Google Scholar 

  91. Williams JJ, Beck PL, Andrews CN, Hogan DB, Storr MA. Microscopic colitis—a common cause of diarrhoea in older adults. Age Ageing. 2010;39:162–8.

    PubMed  Google Scholar 

  92. Tagkalidis P, Bhathal P, Gibson P. Microscopic colitis. J Gastroenterol Hepatol. 2002;17:236–48.

    PubMed  Google Scholar 

  93. Muller S, Neureiter D, Stolte M, Verbeke C, Heuschmann P, Kirchner T, et al. Tenascin: a sensitive and specific diagnostic marker of minimal collagenous colitis. Virchows Arch. 2001;438:435–41.

    PubMed  CAS  Google Scholar 

  94. Groisman GM, Lachter J, Vlodavsky E. Amyloid colitis mimicking collagenous colitis. Histopathology. 1997;31:201–2.

    PubMed  CAS  Google Scholar 

  95. Halaby IA, Rantis PC, Vernava AM 3rd, Longo WE. Collagenous colitis: pathogenesis and management. Dis Colon Rectum. 1996;39:573–8.

    PubMed  CAS  Google Scholar 

  96. Jain R, Chetty R. Enterocolic lymphocytic phlebitis and lymphocytic colitis: drug-related coexistent pathology. Int J Colorectal Dis. 2009;24:473–4.

    PubMed  Google Scholar 

  97. Mosnier JF, Larvol L, Barge J, Dubois S, De La Bigne G, Henin D, et al. Lymphocytic and collagenous colitis: an immunohistochemical study. Am J Gastroenterol. 1996;91:709–13.

    PubMed  CAS  Google Scholar 

  98. Mohamed N, Marais M, Bezuidenhout J. Microscopic colitis as a missed cause of chronic diarrhea. World J Gastroenterol. 2011;17:1996–2002.

    PubMed  Google Scholar 

  99. Chang F, Deere H, Vu C. Atypical forms of microscopic colitis: morphological features and review of the literature. Adv Anat Pathol. 2005;12:203–11.

    PubMed  Google Scholar 

  100. Ayata G, Ithamukkala S, Sapp H, Shaz BH, Brien TP, Wang HH, et al. Prevalence and significance of inflammatory bowel disease-like morphologic features in collagenous and lymphocytic colitis. Am J Surg Pathol. 2002;26:1414–23.

    PubMed  Google Scholar 

  101. Goff JS, Barnett JL, Pelke T, Appelman HD. Collagenous colitis: histopathology and clinical course. Am J Gastroenterol. 1997;92:57–60.

    PubMed  CAS  Google Scholar 

  102. Goldstein NS, Bhanot P. Paucicellular and asymptomatic lymphocytic colitis: expanding the clinicopathologic spectrum of lymphocytic colitis. Am J Clin Pathol. 2004;122:405–11.

    PubMed  Google Scholar 

  103. Fernandez-Banares F, Casalots J, Salas A, Esteve M, Rosinach M, Forne M, et al. Paucicellular lymphocytic colitis: is it a minor form of lymphocytic colitis? A clinical pathological and immunological study. Am J Gastroenterol. 2009;104:1189–98.

    PubMed  Google Scholar 

  104. Lamps LW, Lazenby AJ. Colonic epithelial lymphocytosis and lymphocytic colitis: descriptive histopathology versus distinct clinicopathologic entities. Adv Anat Pathol. 2000;7:210–3.

    PubMed  CAS  Google Scholar 

  105. Wang N, Dumot JA, Achkar E, Easley KA, Petras RE, Goldblum JR. Colonic epithelial lymphocytosis without a thickened subepithelial collagen table: a clinicopathologic study of 40 cases supporting a heterogeneous entity. Am J Surg Pathol. 1999;23:1068–74.

    PubMed  CAS  Google Scholar 

  106. Carmack SW, Lash RH, Gulizia JM, Genta RM. Lymphocytic disorders of the gastrointestinal tract: a review for the practicing pathologist. Adv Anat Pathol. 2009;16:290–306.

    PubMed  Google Scholar 

  107. 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;20:1102–9.

    PubMed  CAS  Google Scholar 

  108. Yan BM, Shaffer EA. Primary eosinophilic disorders of the gastrointestinal tract. Gut. 2009;58:721–32.

    PubMed  CAS  Google Scholar 

  109. Rothenberg ME. Eosinophilic gastrointestinal disorders (EGID). J Allergy Clin Immunol. 2004;113:11–28 (quiz 9).

    Google Scholar 

  110. Talley NJ, Shorter RG, Phillips SF, Zinsmeister AR. Eosinophilic gastroenteritis: a clinicopathological study of patients with disease of the mucosa, muscle layer, and subserosal tissues. Gut. 1990;31:54–8.

    PubMed  CAS  Google Scholar 

  111. Odze RD, Wershil BK, Leichtner AM, Antonioli DA. Allergic colitis in infants. J Pediatr. 1995;126:163–70.

    PubMed  CAS  Google Scholar 

  112. Machida HM, Catto Smith AG, Gall DG, Trevenen C, Scott RB. Allergic colitis in infancy: clinical and pathologic aspects. J Pediatr Gastroenterol Nutr. 1994;19:22–6.

    Google Scholar 

  113. Clouse RE, Alpers DH, Hockenbery DM, DeSchryver-Kecskemeti K. Pericrypt eosinophilic enterocolitis and chronic diarrhea. Gastroenterology. 1992;103:168–76.

    PubMed  CAS  Google Scholar 

  114. Jakate S, Demeo M, John R, Tobin M, Keshavarzian A. Mastocytic enterocolitis: increased mucosal mast cells in chronic intractable diarrhea. Arch Pathol Lab Med. 2006;130:362–7.

    PubMed  Google Scholar 

  115. Ogilvie-McDaniel C, Blaiss M, Osborn FD, Carpenter J. Mastocytic enterocolitis: a newly described mast cell entity. Ann Allergy Asthma Immunol. 2008;101:645–6.

    PubMed  Google Scholar 

  116. Ramsay DB, Stephen S, Borum M, Voltaggio L, Doman DB. Mast cells in gastrointestinal disease. Gastroenterol Hepatol (NY). 2010;6:772–7.

    Google Scholar 

  117. Raithel M, Winterkamp S, Pacurar A, Ulrich P, Hochberger J, Hahn EG. Release of mast cell tryptase from human colorectal mucosa in inflammatory bowel disease. Scand J Gastroenterol. 2001;36:174–9.

    PubMed  CAS  Google Scholar 

  118. Schwab D, Raithel M, Hahn EG. Evidence for mast cell activation in collagenous colitis. Inflamm Res. 1998;47(Suppl 1):S64–5.

    PubMed  CAS  Google Scholar 

  119. Wingren U, Hallert C, Norrby K, Enerback L. Histamine and mucosal mast cells in gluten enteropathy. Agents Actions. 1986;18:266–8.

    PubMed  CAS  Google Scholar 

  120. Blirando K, Milliat F, Martelly I, Sabourin JC, Benderitter M, Francois A. Mast cells are an essential component of human radiation proctitis and contribute to experimental colorectal damage in mice. Am J Pathol. 2011;178:640–51.

    PubMed  Google Scholar 

  121. Hahn HP, Hornick JL. Immunoreactivity for CD25 in gastrointestinal mucosal mast cells is specific for systemic mastocytosis. Am J Surg Pathol. 2007;31:1669–76.

    PubMed  Google Scholar 

  122. Pardanani A. Systemic mastocytosis in adults: 2011 update on diagnosis, risk stratification, and management. Am J Hematol. 2011;86:362–71.

    PubMed  CAS  Google Scholar 

  123. Feuerstadt P, Brandt LJ. Colon ischemia: recent insights and advances. Curr Gastroenterol Rep. 2010;12:383–90.

    PubMed  Google Scholar 

  124. Higgins PD, Davis KJ, Laine L. Systematic review: the epidemiology of ischaemic colitis. Aliment Pharmacol Ther. 2004;19:729–38.

    PubMed  CAS  Google Scholar 

  125. MacDonald PH. Ischaemic colitis. Best Pract Res Clin Gastroenterol. 2002;16:51–61.

    PubMed  CAS  Google Scholar 

  126. Parks DA, Granger DN. Contributions of ischemia and reperfusion to mucosal lesion formation. Am J Physiol. 1986;250:G749–53.

    PubMed  CAS  Google Scholar 

  127. Wheeldon NM, Grundman MJ. Ischaemic colitis as a complication of colonoscopy. BMJ. 1990;301:1080–1.

    PubMed  CAS  Google Scholar 

  128. Carlson RM, Madoff RD. Is “ischemic” colitis ischemic? Dis Colon Rectum. 2011;54:370–3.

    PubMed  Google Scholar 

  129. Theodoropoulou A, Koutroubakis IE. Ischemic colitis: clinical practice in diagnosis and treatment. World J Gastroenterol. 2008;14:7302–8.

    PubMed  Google Scholar 

  130. Brandt LJ, Feuerstadt P, Blaszka MC. Anatomic patterns, patient characteristics, and clinical outcomes in ischemic colitis: a study of 313 cases supported by histology. Am J Gastroenterol. 2010;105:2245–52 (quiz 53).

    Google Scholar 

  131. Sotiriadis J, Brandt LJ, Behin DS, Southern WN. Ischemic colitis has a worse prognosis when isolated to the right side of the colon. Am J Gastroenterol. 2007;102:2247–52.

    PubMed  Google Scholar 

  132. Flobert C, Cellier C, Berger A, Ngo A, Cuillerier E, Landi B, et al. Right colonic involvement is associated with severe forms of ischemic colitis and occurs frequently in patients with chronic renal failure requiring hemodialysis. Am J Gastroenterol. 2000;95:195–8.

    PubMed  CAS  Google Scholar 

  133. Zou X, Cao J, Yao Y, Liu W, Chen L. Endoscopic findings and clinicopathologic characteristics of ischemic colitis: a report of 85 cases. Dig Dis Sci. 2009;54:2009–15.

    PubMed  Google Scholar 

  134. Scowcroft CW, Sanowski RA, Kozarek RA. Colonoscopy in ischemic colitis. Gastrointest Endosc. 1981;27:156–61.

    PubMed  CAS  Google Scholar 

  135. Fenoglio-Preiser C, Noffsinger A, Stemmermann GN, Lantz PE, Isaacson P. Gastrointestinal pathology. An atlas and text. 3rd ed. Philadelphia: Lippincott Williams & Wilkins; 2008.

  136. Ye H, Losada M, West AB. Diverticulosis coli: update on a “Western” disease. Adv Anat Pathol. 2005;12:74–80.

    PubMed  Google Scholar 

  137. Makapugay LM, Dean PJ. Diverticular disease-associated chronic colitis. Am J Surg Pathol. 1996;20:94–102.

    PubMed  CAS  Google Scholar 

  138. Goldstein NS, Leon-Armin C, Mani A. Crohn’s colitis-like changes in sigmoid diverticulitis specimens is usually an idiosyncratic inflammatory response to the diverticulosis rather than Crohn’s colitis. Am J Surg Pathol. 2000;24:668–75.

    PubMed  CAS  Google Scholar 

  139. Brian West A. The pathology of diverticulosis: classical concepts and mucosal changes in diverticula. J Clin Gastroenterol. 2006;40 Suppl 3:S126–31.

    Google Scholar 

  140. Jani N, Finkelstein S, Blumberg D, Regueiro M. Segmental colitis associated with diverticulosis. Dig Dis Sci. 2002;47:1175–81.

    PubMed  Google Scholar 

  141. Robert ME, Skacel M, Ullman T, Bernstein CN, Easley K, Goldblum JR. Patterns of colonic involvement at initial presentation in ulcerative colitis: a retrospective study of 46 newly diagnosed cases. Am J Clin Pathol. 2004;122:94–9.

    PubMed  Google Scholar 

  142. Ortega AE, Klipfel N, Kelso R, Petrone P, Roman I, Diaz A, et al. Changing concepts in the pathogenesis, evaluation, and management of solitary rectal ulcer syndrome. Am Surg. 2008;74:967–72.

    PubMed  Google Scholar 

  143. Tjandra JJ, Fazio VW, Church JM, Lavery IC, Oakley JR, Milsom JW. Clinical conundrum of solitary rectal ulcer. Dis Colon Rectum. 1992;35:227–34.

    PubMed  CAS  Google Scholar 

  144. Martin CJ, Parks TG, Biggart JD. Solitary rectal ulcer syndrome in Northern Ireland. 1971–1980. Br J Surg. 1981;68:744–7.

    PubMed  CAS  Google Scholar 

  145. Chiang JM, Changchien CR, Chen JR. Solitary rectal ulcer syndrome: an endoscopic and histological presentation and literature review. Int J Colorectal Dis. 2006;21:348–56.

    PubMed  Google Scholar 

  146. Morio O, Meurette G, Desfourneaux V, D’Halluin PN, Bretagne JF, Siproudhis L. Anorectal physiology in solitary ulcer syndrome: a case-matched series. Dis Colon Rectum. 2005;48:1917–22.

    PubMed  Google Scholar 

  147. Womack NR, Williams NS, Mist JH, Morrison JF. Anorectal function in the solitary rectal ulcer syndrome. Dis Colon Rectum. 1987;30:319–23.

    PubMed  CAS  Google Scholar 

  148. Saul SH, Sollenberger LC. Solitary rectal ulcer syndrome. Its clinical and pathological underdiagnosis. Am J Surg Pathol. 1985;9:411–21.

    PubMed  CAS  Google Scholar 

  149. Vaizey CJ, van den Bogaerde JB, Emmanuel AV, Talbot IC, Nicholls RJ, Kamm MA. Solitary rectal ulcer syndrome. Br J Surg. 1998;85:1617–23.

    PubMed  CAS  Google Scholar 

  150. Warren BF, Dankwa EK, Davies JD. ‘Diamond-shaped’ crypts and mucosal elastin: helpful diagnostic features in biopsies of rectal prolapse. Histopathology. 1990;17:129–34.

    PubMed  CAS  Google Scholar 

  151. Franzin G, Scarpa A, Dina R, Novelli P. “Transitional” and hyperplastic-metaplastic mucosa occurring in solitary ulcer of the rectum. Histopathology. 1981;5:527–33.

    PubMed  CAS  Google Scholar 

  152. Gore S, Shepherd NA, Wilkinson SP. Endoscopic crescentic fold disease of the sigmoid colon: the clinical and histopathological spectrum of a distinctive endoscopic appearance. Int J Colorectal Dis. 1992;7:76–81.

    PubMed  CAS  Google Scholar 

  153. du Boulay CE, Fairbrother J, Isaacson PG. Mucosal prolapse syndrome—a unifying concept for solitary ulcer syndrome and related disorders. J Clin Pathol. 1983;36:1264–8.

    PubMed  Google Scholar 

  154. Singh B, Mortensen NJ, Warren BF. Histopathological mimicry in mucosal prolapse. Histopathology. 2007;50:97–102.

    PubMed  CAS  Google Scholar 

  155. Ng WK, Chan KW. Postirradiation colitis cystica profunda. Case report and literature review. Arch Pathol Lab Med. 1995;119:1170–3.

    PubMed  CAS  Google Scholar 

  156. Magidson JG, Lewin KJ. Diffuse colitis cystica profunda. Report of a case. Am J Surg Pathol. 1981;5:393–9.

    PubMed  CAS  Google Scholar 

  157. Herman AH, Nabseth DC. Colitis cystica profunda: localized, segmental, and diffuse. Arch Surg. 1973;106:337–41.

    PubMed  CAS  Google Scholar 

  158. Guest CB, Reznick RK. Colitis cystica profunda. Review of the literature. Dis Colon Rectum. 1989;32:983–8.

    PubMed  CAS  Google Scholar 

  159. Koreishi A, Lauwers GY, Misdraji J. Pneumatosis intestinalis: a challenging biopsy diagnosis. Am J Surg Pathol. 2007;31:1469–75.

    PubMed  Google Scholar 

  160. Heng Y, Schuffler MD, Haggitt RC, Rohrmann CA. Pneumatosis intestinalis: a review. Am J Gastroenterol. 1995;90:1747–58.

    PubMed  CAS  Google Scholar 

  161. Pieterse AS, Leong AS, Rowland R. The mucosal changes and pathogenesis of pneumatosis cystoides intestinalis. Hum Pathol. 1985;16:683–8.

    PubMed  CAS  Google Scholar 

  162. Boerner RM, Fried DB, Warshauer DM, Isaacs K. Pneumatosis intestinalis. Two case reports and a retrospective review of the literature from 1985 to 1995. Dig Dis Sci. 1996;41:2272–85.

    PubMed  CAS  Google Scholar 

  163. Nagata S, Ueda N, Yoshida Y, Matsuda H. Pneumatosis coli complicated with intussusception in an adult: report of a case. Surg Today. 2010;40:460–4.

    PubMed  Google Scholar 

  164. Lawrentschuk N, Nguyen H. Pneumatosis coli in a case of caecal volvulus. Hosp Med. 2002;63:436–7.

    PubMed  Google Scholar 

  165. Duron VP, Rutigliano S, Machan JT, Dupuy DE, Mazzaglia PJ. Computed tomographic diagnosis of pneumatosis intestinalis: clinical measures predictive of the need for surgical intervention. Arch Surg. 2011;146:506–10.

    PubMed  Google Scholar 

  166. Hokama A, Kinjo F, Fujita J. Pneumatosis cystoides intestinalis: radiographic and endoscopic features. Clin Gastroenterol Hepatol. 2009;7:A32.

    PubMed  Google Scholar 

  167. Suarez V, Chesner IM, Price AB, Newman J. Pneumatosis cystoides intestinalis. Histological mucosal changes mimicking inflammatory bowel disease. Arch Pathol Lab Med. 1989;113:898–901.

    PubMed  CAS  Google Scholar 

  168. Edwards CM, George B, Warren B. Diversion colitis—new light through old windows. Histopathology. 1999;34:1–5.

    PubMed  CAS  Google Scholar 

  169. Roe AM, Warren BF, Brodribb AJ, Brown C. Diversion colitis and involution of the defunctioned anorectum. Gut. 1993;34:382–5.

    PubMed  CAS  Google Scholar 

  170. Neut C, Guillemot F, Colombel JF. Nitrate-reducing bacteria in diversion colitis: a clue to inflammation? Dig Dis Sci. 1997;42:2577–80.

    PubMed  CAS  Google Scholar 

  171. Thorsen AJ. Noninfectious colitides: collagenous colitis, lymphocytic colitis, diversion colitis, and chemically induced colitis. Clin Colon Rectal Surg. 2007;20:47–57.

    PubMed  Google Scholar 

  172. Geraghty JM, Talbot IC. Diversion colitis: histological features in the colon and rectum after defunctioning colostomy. Gut. 1991;32:1020–3.

    PubMed  CAS  Google Scholar 

  173. Warren BF, Shepherd NA. Diversion proctocolitis. Histopathology. 1992;21:91–3.

    PubMed  CAS  Google Scholar 

  174. Asplund S, Gramlich T, Fazio V, Petras R. Histologic changes in defunctioned rectums in patients with inflammatory bowel disease: a clinicopathologic study of 82 patients with long-term follow-up. Dis Colon Rectum. 2002;45:1206–13.

    PubMed  Google Scholar 

  175. Griffiths AP, Dixon MF. Microcarcinoids and diversion colitis in a colon defunctioned for 18 years. Report of a case. Dis Colon Rectum. 1992;35:685–8.

    PubMed  CAS  Google Scholar 

  176. Lee KS, Medline A, Shockey S. Indeterminate colitis in the spectrum of inflammatory bowel disease. Arch Pathol Lab Med. 1979;103:173–6.

    PubMed  CAS  Google Scholar 

  177. Bismar MM, Sinicrope FA. Radiation enteritis. Curr Gastroenterol Rep. 2002;4:361–5.

    PubMed  Google Scholar 

  178. Nielsen OH, Vainer B, Rask-Madsen J. Non-IBD and noninfectious colitis. Nat Clin Pract Gastroenterol Hepatol. 2008;5:28–39.

    PubMed  Google Scholar 

  179. Leupin N, Curschmann J, Kranzbuhler H, Maurer CA, Laissue JA, Mazzucchelli L. Acute radiation colitis in patients treated with short-term preoperative radiotherapy for rectal cancer. Am J Surg Pathol. 2002;26:498–504.

    PubMed  Google Scholar 

  180. Gilinsky NH, Burns DG, Barbezat GO, Levin W, Myers HS, Marks IN. The natural history of radiation-induced proctosigmoiditis: an analysis of 88 patients. Q J Med. 1983;52:40–53.

    PubMed  CAS  Google Scholar 

  181. Perrakis N, Athanassiou E, Vamvakopoulou D, Kyriazi M, Kappos H, Vamvakopoulos NC, et al. Practical approaches to effective management of intestinal radiation injury: benefit of resectional surgery. World J Gastroenterol. 2011;17:4013–6.

    PubMed  Google Scholar 

  182. Hasleton PS, Carr N, Schofield PF. Vascular changes in radiation bowel disease. Histopathology. 1985;9:517–34.

    PubMed  CAS  Google Scholar 

  183. Gelfand MD, Tepper M, Katz LA, Binder HJ, Yesner R, Floch MH. Acute irradiation proctitis in man: development of eosinophilic crypt abscesses. Gastroenterology. 1968;54:401–11.

    PubMed  CAS  Google Scholar 

  184. Sedgwick DM, Howard GC, Ferguson A. Pathogenesis of acute radiation injury to the rectum. A prospective study in patients. Int J Colorectal Dis. 1994;9:23–30.

    PubMed  CAS  Google Scholar 

  185. Haboubi NY, Kaftan SM, Schofield PF. Radiation colitis is another mimic of chronic inflammatory bowel disease. J Clin Pathol. 1992;45:272.

    PubMed  CAS  Google Scholar 

  186. Greenson JK, Stern RA, Carpenter SL, Barnett JL. The clinical significance of focal active colitis. Hum Pathol. 1997;28:729–33.

    PubMed  CAS  Google Scholar 

  187. Shetty S, Anjarwalla SM, Gupta J, Foy CJ, Shaw IS, Valori RM, et al. Focal active colitis: a prospective study of clinicopathological correlations in 90 patients. Histopathology. 2011;59:850–6.

    PubMed  Google Scholar 

  188. Xin W, Brown PI, Greenson JK. The clinical significance of focal active colitis in pediatric patients. Am J Surg Pathol. 2003;27:1134–8.

    PubMed  Google Scholar 

  189. Volk EE, Shapiro BD, Easley KA, Goldblum JR. The clinical significance of a biopsy-based diagnosis of focal active colitis: a clinicopathologic study of 31 cases. Mod Pathol. 1998;11:789–94.

    PubMed  CAS  Google Scholar 

  190. Driman DK, Preiksaitis HG. Colorectal inflammation and increased cell proliferation associated with oral sodium phosphate bowel preparation solution. Hum Pathol. 1998;29:972–8.

    PubMed  CAS  Google Scholar 

  191. Goldstein NS, Cinenza AN. The histopathology of nonsteroidal anti-inflammatory drug-associated colitis. Am J Clin Pathol. 1998;110:622–8.

    PubMed  CAS  Google Scholar 

  192. Schneider EN, Havens JM, Scott MA, Goldblum JR, Greenson JK, Shaffer RA, et al. Molecular diagnosis of Campylobacter jejuni infection in cases of focal active colitis. Am J Surg Pathol. 2006;30:782–5.

    PubMed  Google Scholar 

  193. Lee FD. Drug-related pathological lesions of the intestinal tract. Histopathology. 1994;25:303–8.

    PubMed  CAS  Google Scholar 

  194. Wong NA, Penman ID, Campbell S, Lessells AM. Microscopic focal cryptitis associated with sodium phosphate bowel preparation. Histopathology. 2000;36:476–8.

    PubMed  CAS  Google Scholar 

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Khor, T.S., Fujita, H., Nagata, K. et al. Biopsy interpretation of colonic biopsies when inflammatory bowel disease is excluded. J Gastroenterol 47, 226–248 (2012). https://doi.org/10.1007/s00535-012-0539-6

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