Diagnostic Guideline of Crohn's Disease

크론병 진단 가이드라인

Ye, Byong-Duk;Jang, Byung-Ik;Jeen, Yoon-Tae;Lee, Kang-Moon;Kim, Joo-Sung;Yang, Suk-Kyun;IBD Study Group of the Korean Association of the Study of Intestinal Diseases,
예병덕;장병익;진윤태;이강문;김주성;양석균;대한장연구학회 IBD 연구회

  • Published : 20090300

Abstract

Crohn's disease (CD) is a chronic inflammatory bowel disease (IBD) with uncertain etiopathogenesis. CD can involve any site of gastrointestinal tract from mouth to anus and is associated with serious complications such as bowel stricture, perforation, abscess, and fistula formation. The incidence and prevalence rates of CD in Korea are still low compared with those of Western countries, but are rapidly increasing during the past decades. The diagnosis of CD is a challenging issue in some clinical situations and it is often difficult to differentiate CD from intestinal tuberculosis or Behçet’s enterocolitis which are more prevalent in Korea than in Western countries. Therefore, IBD Study Group of KASID has set out to establish the diagnostic guideline of CD in Korea. There is no single gold standard for the diagnosis of CD and diagnosis is made by clinical evaluation including detailed history, physical examination, and combination of endoscopic findings, histology, radiologic findings and laboratory investigations. The typical symptoms of CD are abdominal pain, diarrhea, and weight loss especially in late adolescence or early adulthood. Initial laboratory investigations include CBC, C-reactive protein, and serum chemistry. Ileocolonoscopy and biopsies are recommended as the first line procedures to establish the diagnosis. Typical endoscopic findings of CD are non-continuous distribution of longitudinal ulcers, cobblestone mucosal appearance, and aphthous ulcerations arranged in a longitudinal fashion. The evaluation of small bowel with small bowel follow- through is recommended for suspected CD to establish diagnosis and to determine the extent and location of disease. Focal and patchy chronic inflammation, focal crypt irregularity, and non-caseating granulomas are usual microscopic features of CD. This is the first Korean diagnostic guideline for CD and needs revision with further data on CD in Koreans.

Keywords

References

  1. Kirsner JG. Historical aspects of inflammatory bowel disease. J Clin Gastroenterol 1988;10:286-297. https://doi.org/10.1097/00004836-198806000-00012
  2. Crohn BB, Ginzburg L, Oppenheimer GD. Regional ileitis: a pathologic and clinical entity. JAMA 1932;9:1323-1328.
  3. Yang SK, Yun S, Kim JH, et al. Epidemiology of inflammatory bowel disease in the Songpa-Kangdong district, Seoul, Korea, 1986-2005: a KASID study. Inflamm Bowel Dis 2008;14:542-549. https://doi.org/10.1002/ibd.20310
  4. Carter MJ, Lobo AJ, Travis SP. Guidelines for the management of inflammatory bowel disease in adults. Gut 2004; 3:S1-S16. https://doi.org/10.1136/gut.3.1.1
  5. Stange EF, Travis SP, Vermeire S, et al. European evidence based consensus on the diagnosis and management of Crohn's disease: definitions and diagnosis. Gut 2006;55:1-15. https://doi.org/10.1136/gut.2005.069062
  6. Yao T, Matsui T, Hiwatashi N. Crohn's disease in Japan: diagnostic criteria and epidemiology. Dis Colon Rectum 2000;43:S85-S93. https://doi.org/10.1007/BF02237231
  7. Gollop JH, Phillips SF, Melton LJ 3rd, et al. Epidemiologic aspects of Crohn's disease: a population based study in Olmsted County, Minnesota, 1943-1982. Gut 1988;29:49-56. https://doi.org/10.1136/gut.29.1.49
  8. Loftus EV Jr, Silverstein MD, Sandborn WJ, et al. Crohn's disease in Olmsted County, Minnesota, 1940-1993: incidence, prevalence, and survival. Gastroenterology 1998;14:1161-1168.
  9. Centre for Evidence Based Medicine, Oxford. Levels of evidence and grades of redommendation. http://www.cebm.net/ evles_of_evidence.asp.
  10. Best WR, Becktel JM, Singleton JW, et al. Development of a Crohn's disease activity index. National Cooperative Crohn's Disease Study. Gastroenterology 1976;70:439-444.
  11. Harvey RF, Bradshaw JM. A simple index of Crohn's disease activity. Lancet 1980;1:514.
  12. Best WR. Predicting the Crohn’s disease activity index from the Harvey-Bradshaw index. Inflamm Bowel Dis 2006;12: 304-310. https://doi.org/10.1097/01.MIB.0000215091.77492.2a
  13. Gasche C, Scholmerich J, Brynskov J, et al. A simple classification of Crohn's disease: report of the Working Party for the World Congresses of Gastroenterology, Vienna 1998. Inflamm Bowel Dis 2000;6:8-15 https://doi.org/10.1002/ibd.3780060103
  14. Satsangi J, Silverberg MS, Vermeire S, et al. The Montreal classification of inflammatory bowel disease: controversies, consensus, and implications. Gut 2006;55:749-753 https://doi.org/10.1136/gut.2005.082909
  15. Yang SK. Current status and clinical characteristics of inflammatory bowel disease in Korea. Korean J Gastroenterol 2002;40:1-14.
  16. Lapidus A. Crohn's disease in Stockholm County during 1990-2001: an epidemiological update. World J Gastroenterol 2006;12:75-81.
  17. Moum B, Vatn MH, Ekbom A, et al. Incidence of Crohn's disease in four counties in southeastern Norway, 1990-93. A prospective population-based study. The Inflammatory Bowel South-Eastern Norway (IBSEN) Study Group of Gastroenterologists. Scand J Gastroenterol 1996;31:355-361. https://doi.org/10.3109/00365529609006410
  18. Tragnone A, Corrao G, Miglio F, et al. Incidence of inflammatory bowel disease in Italy: a nationwide populationased study. Gruppo Italiano per lo Studio del Colon e del Retto (GISC). Int J Epidemiol 1996;25:1044-1052. https://doi.org/10.1093/ije/25.5.1044
  19. Loftus CG, Loftus EV Jr, Harmsen WS, et al. Update on the incidence and prevalence of Crohn's disease and ulcerative colitis in Olmsted County, Minnesota, 1940-2000. Inflamm Bowel Dis 2007;13:254-261. https://doi.org/10.1002/ibd.20029
  20. Kim CG, Kim JW, Kim HD, et al. Clinical features of Crohn's disease in Korea. Korean J Gastroenterol 2002;40: 173-180.
  21. Park JB, Yang SK, Myung SJ, et al. Clinical characteristics at diagnosis and course of Korean patients with Crohn's disease. Korean J Gastroenterol 2004;43:8-17.
  22. Jiang L, Xia B, Li J, et al. Retrospective survey of 452 patients with inflammatory bowel disease in Wuhan city, central China. Inflamm Bowel Dis 2006;12:212-217. https://doi.org/10.1097/01.MIB.0000201098.26450.ae
  23. Bernstein CN, Wajda A, Svenson LW, et al. The epidemiology of inflammatory bowel disease in Canada: a populationbased study. Am J Gastroenterol 2006;101:1559-1568. https://doi.org/10.1111/j.1572-0241.2006.00603.x
  24. Molinie F, Gower-Rousseau C, Yzet T, et al. Opposite evolution in incidence of Crohn’s disease and ulcerative colitis in northern France (1988-1999). Gut 2004;53:843-848. https://doi.org/10.1136/gut.2003.025346
  25. Jacobsen BA, Fallingborg J, Rasmussen HH, et al. Increase in incidence and prevalence of inflammatory bowel disease in northern Denmark: a population-based study, 1978-2002. Eur J Gastroenterol Hepatol 2006;18:601-606. https://doi.org/10.1097/00042737-200606000-00005
  26. Shivananda S, Lennard-Jones J, Logan R, et al. Incidence of inflammatory bowel disease across Europe: is there a difference between north and south? Results of the European Collaborative Study on Inflammatory Bowel Disease (ECBD). Gut 1996;39:690-697. https://doi.org/10.1136/gut.39.5.690
  27. Leong RW, Lau JY, Sung JJ. The epidemiology and phenotype of Crohn’s disease in the Chinese population. Inflamm Bowel Dis 2004;10:646-651. https://doi.org/10.1097/00054725-200409000-00022
  28. Vind I, Riis L, Jess T, et al. Increasing incidences of inflammatory bowel disease and decreasing surgery rates in Copenhagen City and County, 2003-2005: a population- ased study from the Danish Crohn colitis database. Am J Gastroenterol 2006;101:1274-1282. https://doi.org/10.1111/j.1572-0241.2006.00552.x
  29. Bjornsson S, Johannsson JH. Inflammatory bowel disease in Iceland, 1990-1994: a prospective, nationwide, epidemiological study. Eur J Gastroenterol Hepatol 2000;12:31-38. https://doi.org/10.1097/00042737-200012010-00007
  30. Oriuchi T, Hiwatashi N, Kinouchi Y, et al. Clinical course and longterm prognosis of Japanese patients with Crohn’s disease: predictive factors, rates of operation, and mortality. J Gastroenterol 2003;38:942-953. https://doi.org/10.1007/s00535-003-1177-9
  31. Kim JY, Yang SK, Byeon JS, et al. The incidence and natural history of perianal fistulas in Korean patients with Crohn's disease. Intest Res 2006;4:22-31.
  32. Hellers G, Bergstrand O, Ewerth S, Holmstrom B. Occurrence and outcome after primary treatment of anal fistulae in Crohn's disease. Gut 1980;21:525-527. https://doi.org/10.1136/gut.21.6.525
  33. Schwartz DA, Loftus EV Jr, Tremaine WJ, et al. The natural history of fistulizing Crohn's disease in Olmsted County, Minnesota. Gastroenterology 2002;122:875-880. https://doi.org/10.1053/gast.2002.32362
  34. van Dongen LM, Lubbers EJ. Perianal fistulas in patients with Crohn's disease. Arch Surg 1986;121:1187-1190. https://doi.org/10.1001/archsurg.1986.01400100099019
  35. Nordgren S, Fasth S, Hulten L. Anal fistulas in Crohn's disease: incidence and outcome of surgical treatment. Int J Colorectal Dis 1992;7:214-218. https://doi.org/10.1007/BF00341224
  36. Farmer RG, Hawk WA, Turnbull RB Jr. Clinical patterns in Crohn's disease: a statistical study of 615 cases. Gastroenterology 1975;68:627-635.
  37. Greenstein AJ, Kark AE, Dreiling DA. Crohn's disease of the colon. I. Fistula in Crohn's disease of the colon, classification presenting features and management in 63 patients. Am J Gastroenterol 1974;62:419-429.
  38. Marks CG, Ritchie JK, Lockhart-Mummery HE. Anal fistulas in Crohn's disease. Br J Surg 1981;68:525-527. https://doi.org/10.1002/bjs.1800680802
  39. Fielding JF. Perianal lesions in Crohn's disease. J R Coll Surg Edinb 1972;17:32-37.
  40. Goebell H. Perianal complications in Crohn's disease. Neth J Med 1990;37(suppl 1):S47-S51.
  41. Hobbiss JH, Schofield PF. Management of perianal Crohn's disease. J R Soc Med 1982;75:414-417.
  42. Rankin GB, Watts HD, Melnyk CS, Kelly ML Jr. National cooperative Crohn's disease study: extraintestinal manifestations and perianal complications. Gastroenterology 1979; 77:914-920.
  43. Tolia V. Peiranal Crohn's disease in children and adolescents. Am J Gatroenterol 1996;91:922-926.
  44. Sands BE. From symptom to diagnosis: clinical distinctions among various forms of intestinal inflammation. Gastroenterology 2004;126:1518-1532. https://doi.org/10.1053/j.gastro.2004.02.072
  45. Epstein D, Watermeyer G, Kirsch R. Review article: the diagnosis and management of Crohn's disease in populations with high-risk rates for tuberculosis. Aliment Pharmacol Ther 2007;25:1373-1388. https://doi.org/10.1111/j.1365-2036.2007.03332.x
  46. Greenstein AJ, Janowith HD, Sachar DB. The extraintestinal manifestations of Crohn’s disease and ulcerative colitis: a study of 700 patients. Medicine 1976;55:401-412. https://doi.org/10.1097/00005792-197609000-00004
  47. Nikolaus S, Schreiber S. Diagnostics of inflammatory bowel disease. Gastroenterology 2007;133:1670-1689. https://doi.org/10.1053/j.gastro.2007.09.001
  48. Palm O, Moum B, Ongre A, et al. Prevalence of ankylosing spondylitis and other spondyloarthropathies among patients with inflammatory bowel disease: a population study (the IBSEN study). J Rheumatol 2002;29:511-515.
  49. Mintz R, Feller ER, Bahr RL, et al. Ocular manifestations of inflammatory bowel disease. Inflamm Bowel Dis 2004; 10:135-139. https://doi.org/10.1097/00054725-200403000-00012
  50. Ahmad J, Slivka A. Hepatobiliary disease in inflammatory bowel disease. Gastroenterol Clin North Am 2002;31:329-345. https://doi.org/10.1016/S0889-8553(01)00020-6
  51. Talwalkar JA, Lindor KD. Primary sclerosing cholangitis. Inflamm Bowel Dis 2005;11:62-72. https://doi.org/10.1097/00054725-200501000-00009
  52. Terreblanche J. Fistula in ano: a five year survey at Groote Schuur Hospital and a review of the literature. S Afr Med J 1964;403-408.
  53. Chen WS, Leu SY, Hsu H, et al. Trend of large bowel tuberculosis and the relation with pulmonary tuberculosis. Dis Colon Rectum 1992;35:189-192. https://doi.org/10.1007/BF02050677
  54. Bridger S, Lee JC, Bjarnason I, et al. In siblings with similar genetic susceptibility for inflammatory bowel disease, smokers tend to develop Crohn’s disease and non-smokers develop ulcerative colitis. Gut 2002;51:21-25. https://doi.org/10.1136/gut.51.1.21
  55. 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. https://doi.org/10.1097/01.MPG.0000163736.30261.82
  56. Tanner J. Growth at adolescence. 2nd ed. Oxford: Blackwell Scientific, 1962.
  57. Podolsky DK. Inflammatory bowel disease. N Engl J Med 2002;347:417-429. https://doi.org/10.1056/NEJMra020831
  58. Yang SK. Intestinal Behcet's disease. Intest Res 2005;3:1-10. https://doi.org/10.1111/j.1432-1033.1967.tb19491.x
  59. Gasche C, Reinisch W, Lochs H, et al. Anemia in Crohn’s disease. Importance of inadequate erythropoietin production and iron deficiency. Dig Dis Sci 1994;39:1930-1934. https://doi.org/10.1007/BF02088127
  60. Gasche C, Berstad A, Befrits R, et al. Guidelines on the diagnosis and management of iron deficiency and anemia in inflammatory bowel diseases. Inflamm Bowel Dis 2007; 13:1545-1553. https://doi.org/10.1002/ibd.20285
  61. Colombel JF, Solem CA, Sandborn WJ, et al. Quantitative measurement and visual assessment of ileal Crohn's disease activity by computed tomography enterography: correlation with endoscopic severity and C reactive protein. Gut 2006; 55:1561-1567. https://doi.org/10.1136/gut.2005.084301
  62. Vermeire S, Van Assche G, Rutgeerts P. Laboratory markers in IBD: useful, magic, or unnecessary toys? Gut 2006;55: 426-431. https://doi.org/10.1136/gut.2005.069476
  63. Vermeire S, Van Assche G, Rutgeerts P. C-reactive protein as a marker for inflammatory bowel disease. Inflamm Bowel Dis 2004;10:661-665. https://doi.org/10.1097/00054725-200409000-00026
  64. Sachar DB, Luppescu NE, Bodian C, et al. Erythrocyte sedimentation as a measure of Crohn’s disease activity: opposite trends in ileitis versus colitis. J Clin Gastroenterol 1990;12:643-646. https://doi.org/10.1097/00004836-199012000-00009
  65. North American Society for Pediatric Gastroenterology, Hepatology, and Nutrition; Colitis Foundation of America, Bousvaros A, Antonioli DA, Colletti RB, et al. Differentiating ulcerative colitis from Crohn disease in children and young adults: report of a working group of the North American Society for Pediatric Gastroenterology, Hepatology, and Nutrition and the Crohn's and Colitis Foundation of America. J Pediatr Gastroenterol Nutr 2007;44:653-674. https://doi.org/10.1097/MPG.0b013e31805563f3
  66. Reese GE, Constantinides VA, Simillis C, et al. Diagnostic precision of anti-Saccharomyces cerevisiae antibodies and perinuclear antineutrophil cytoplasmic antibodies in inflammatory bowel disease. Am J Gastroenterol 2006;101: 2410-2422. https://doi.org/10.1111/j.1572-0241.2006.00840.x
  67. Kim BG, Kim YS, Kim JS, et al. The diagnostic role of anti- Saccharomyces cerevisiae antibody combined with antineutrophil cytoplasmic antibody in patients with inflammatory bowel disease. Gastroenterology 2002;122(suppl 1):A177.
  68. Geboes K, Ectors N, D’Haens G, et al. Is ileoscopy with biopsy worthwhile in patients presenting with symptoms of inflammatory bowel disease? Am J Gastroenterol 1998;93: 201-206. https://doi.org/10.1111/j.1572-0241.1998.00201.x
  69. Coremans G, Rutgeerts P, Geboes K, et al. The value of ileoscopy with biopsy in the diagnosis of intestinal Crohn’s disease. Gastrointest Endosc 1984;30:167-172. https://doi.org/10.1016/S0016-5107(84)72358-3
  70. Pera A, Bellando P, Caldera D, et al. Colonoscopy in inflammatory bowel disease. Diagnostic accuracy and proposal of an endoscopic score. Gastroenterology 1987;92:181-185.
  71. Yao T. Criteria for diagnosis of Crohn's disease (preliminary proposal). In: Muto T, ed. Annual report of the Research Committee of Inflammatory Bowel Disease. Tokyo: The Ministry of Health and Welfare of Japan, 1996:63-66.
  72. Yao T. New criteria for the diagnosis of Crohn's disease. Stomach Intestine 1996;31:451-464.
  73. Yang SK, Min YI. Colonoscopic diagnosis. 1st ed. Seoul: Koonja, 1999.
  74. Fuchigami T, Osamura T, Sakai Y. Intestinal Behçet and simple ulcer. Stomach Intestine 1997;32:451-458.
  75. Kojima N, Tominaga M, Okabe N, et al. Typhoid fever with multiple ulcers in the colon, report of a case. Stomach Intestine 1992;27:1451-1456
  76. Lee YJ, Yang SK, Byeon JS, et al. Analysis of colonoscopic findings in the differential diagnosis between intestinal tuberculosis and Crohn's disease. Endoscopy 2006;38:592-597. https://doi.org/10.1055/s-2006-924996
  77. Lennard-Jones JE, Shivananda S. Clinical uniformity of inflammatory bowel disease at presentation and during the first year of disease in the north and south of Europe. EC-IBD Study Group. Eur J Gastroenterol Hepatol 1997; 9:353-359. https://doi.org/10.1097/00042737-199704000-00007
  78. Wagtmans MJ, van Hogezand RA, Griffioen G, et al. Crohn’s disease of the upper gastrointestinal tract. Neth J Med 1997;50:S2-S7. https://doi.org/10.1016/S0300-2977(96)00063-0
  79. Witte AM, Veenendaal RA, Van Hogezand RA, et al. Crohn's disease of the upper gastrointestinal tract: the value of endoscopic examination. Scand J Gastroenterol 1998;225: S100-S105.
  80. Rutgeerts P, Onette E, Vantrappen G, et al. Crohn’s disease of the stomach and duodenum: a clinical study with emphasis on the value of endoscopy and endoscopic biopsies. Endoscopy 1980;12:288-294. https://doi.org/10.1055/s-2007-1021762
  81. Kang MS, Park DI, Park JH, et al. Bamboo joint-like appearance of stomach in Korean patients with Crohn's disease. Korean J Gastroenterol 2006;48:395-400.
  82. Yokota K, Saito Y, Einami K, et al. A bamboo joint-like appearance of the gastric body and cardia: possible association with Crohn's disease. Gastrointest Endosc 1997;46:268-272. https://doi.org/10.1016/S0016-5107(97)70100-7
  83. Hirokawa M, Shimizu M, Terayama K, et al. Bamboo-joint like appearance of the stomach: a histopathological study. APMIS 1999;107:951-956. https://doi.org/10.1111/j.1699-0463.1999.tb01496.x
  84. Morimoto N, Kato J, Shiratori Y. Characteristic findings of gastroduodenoscopy in Crohn's disease patients; bamboo joint-like appearance, gastric erosions, and duodenal lesions. Gastroenterology 2005;128(suppl 2):M1168.
  85. Triester SL, Leighton JA, Leontiadis GI, et al. Meta-analysis of the yield of capsule endoscopy compared to other diagnostic modalities in patients with non-stricturing small bowel Crohn's disease. Am J Gastroenterol 2006;101:954-964. https://doi.org/10.1111/j.1572-0241.2006.00506.x
  86. Patel N, Amarapurkar D, Agal S, et al. Gastrointestinal luminal tuberculosis: establishing a diagnosis. J Gastroenterol Hepatol 2004;19:1240-1246. https://doi.org/10.1111/j.1440-1746.2004.03485.x
  87. Leung VKS, Law ST, Lam CW, et al. Intestinal tuberculosis in a regional hospital in Hong Kong: a 10 year experience. Hong Kong Med J 2006;12:264-271.
  88. Shah S, Thomas V, Mathan M, et al. Colonoscopic study of 50 patients with colonic tuberculosis. Gut 1992;33:347-351. https://doi.org/10.1136/gut.33.3.347
  89. Singh V, Kumar P, Kamal J, et al. Clinicocolonoscopic profile of colonic tuberculosis. Am J Gastroenterol 1996;3: 565-568.
  90. Alvares JF, Devarbhavi H, Makhija P, et al. Clinical, colonoscopic, and histological profile of colonic tuberculosis in a tertiary hospital. Endoscopy 2005;37:351-356. https://doi.org/10.1055/s-2005-861116
  91. Toms AP, Barltrop A, Freeman AH. A prospective randomised study comparing enteroclysis with small bowel follow- through examinations in 244 patients. Eur Radiol 2001; 11:1155-1160. https://doi.org/10.1007/s003300000746
  92. Bernstein CN, Boult IF, Greenberg HM, et al. A prospective randomized comparison between small bowel enteroclysis and small bowel follow-through in Crohn's disease. Gastroenterology 1997;113:390-398. https://doi.org/10.1053/gast.1997.v113.pm9247455
  93. Maglinte DD, Chernish SM, Kelvin FM, et al. Crohn disease of the small intestine: accuracy and relevance of enteroclysis. Radiology 1992;184:541-545.
  94. Cirillo LC, Camera L, Della NM, et al. Accuracy of enteroclysis in Crohn’s disease of the small bowel: a retrospective study. Eur Radiol 2000;10:1894-1898. https://doi.org/10.1007/s003300000473
  95. Barloon TJ, Lu CC, Honda H, et al. Does a normal small-bowel enteroclysis exclude small-bowel disease? A long-term follow-up of consecutive normal studies. Abdom Imaging 1994;19:113-115. https://doi.org/10.1007/BF00203483
  96. Dijkstra J, Reeders JW, Tytgat GN. Idiopathic inflammatory bowel disease: endoscopic-radiologic correlation. Radiology 1995;197:369-375.
  97. Scotiniotis I, Rubesin SE, Ginsberg GG. Imaging modalities in inflammatory bowel disease. Gastroenterol Clin North Am 1999;28:391-421. https://doi.org/10.1016/S0889-8553(05)70062-5
  98. Maglinte DD, Reyes BL, Harmon BH, et al. Reliability and role of plain film radiography and CT in the diagnosis of small-bowel obstruction. Am J Roentgenol 1996;167:1451-1455. https://doi.org/10.2214/ajr.167.6.8956576
  99. Maglinte DD, Sandrasegaran K, Lappas JC, Chiorean M. CT enteroclysis. Radiology 2007;245:661-671. https://doi.org/10.1148/radiol.2453060798
  100. Rollandi GA, Curone PF, Biscaldi E, et al. Spiral CT of the abdomen after distention of small bowel loops with transparent enema in patients with Crohn’s disease. Abdom Imaging 1999;24:544-549. https://doi.org/10.1007/s002619900559
  101. Raptopoulos V, Schwartz RK, McNicholas MM, et al. Multiplanar helical CT enterography in patients with Crohn's disease. Am J Roentgenol 1997;169:1545-1550. https://doi.org/10.2214/ajr.169.6.9393162
  102. Andersen K, Vogt C, Blondin D, et al. Multi-detector CT-colonography in inflammatory bowel disease: prospective analysis of CT-findings to high-resolution video colonoscopy. Eur J Radiol 2006;58:140-146. https://doi.org/10.1016/j.ejrad.2005.11.004
  103. Masselli G, Brizi GM, Parrella A, et al. Crohn disease: magnetic resonance enteroclysis. Abdom Imaging 2004;29: 326-334.
  104. Bernstein CN, Greenberg H, Boult I, et al. A prospective comparison study of MRI versus small bowel follow-through in recurrent Crohn’s disease. Am J Gastroenterol 2005; 100:2493-2502. https://doi.org/10.1111/j.1572-0241.2005.00239.x
  105. Rieber A, Wruk D, Potthast S, et al. Diagnostic imaging in Crohn’s disease: comparison of magnetic resonance imaging and conventional imaging methods. Int J Colorectal Dis 2000;15:176-181. https://doi.org/10.1007/s003840000219
  106. Schwartz DA, Wiersema MJ, Dudiak KM, et al. A comparison of endoscopic ultrasound, magnetic resonance imaging, and exam under anesthesia for evaluation of Crohn's perianal fistulas. Gastroenterology 2001;121:1064-1072 https://doi.org/10.1053/gast.2001.28676
  107. Bozkurt T, Richter F, Lux G. Ultrasonography as a primary diagnostic tool in patients with inflammatory disease and tumors of the small intestine and large bowel. J Clin Ultrasound 1994;22:85-91. https://doi.org/10.1002/jcu.1870220204
  108. Sheridan MB, Nicholson DA, Martin DF. Transabdominal ultrasonography as the primary investigation in patients with suspected Crohn’s disease or recurrence: a prospective study. Clin Radiol 1993;48:402-404. https://doi.org/10.1016/S0009-9260(05)81109-2
  109. Solvig J, Ekberg O, Lindgren S, et al. Ultrasound examination of the small bowel: comparison with enteroclysis in patients with Crohn disease. Abdom Imaging 1995;20:323-326. https://doi.org/10.1007/BF00203364
  110. Tarjan Z, Toth G, Gyorke T, et al. Ultrasound in Crohn’s disease of the small bowel. Eur J Radiol 2000;35:176-182. https://doi.org/10.1016/S0720-048X(00)00240-0
  111. Bremner AR, Pridgeon J, Fairhurst J, et al. Ultrasound scanning may reduce the need for barium radiology in the assessment of small-bowel Crohn’s disease. Acta Paediatr 2004;93:479-481. https://doi.org/10.1080/08035250410023089
  112. Pulimood AB, Peter S, Ramakrishna B, et al. Segmental colonoscopic biopsies in the differentiation of ileocolic tuberculosis from Crohn’s disease. J Gastroenterol Hepatol 2005; 20:688-696. https://doi.org/10.1111/j.1440-1746.2005.03814.x
  113. Bhargava DK, Tandon HD, Chawla TC, et al. Diagnosis of ileocecal and colonic tuberculosis by colonoscopy. Gastrointest Endosc 1985;31:68-70. https://doi.org/10.1016/S0016-5107(85)71995-5
  114. 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;55:955-960. https://doi.org/10.1136/jcp.55.12.955
  115. Dejaco C, Osterreicher C, Angelberger S, et al. Diagnosing colitis: a prospective study on essential parameters for reaching a diagnosis. Endoscopy 2003;35:1004-1008. https://doi.org/10.1055/s-2003-44593
  116. Seldenrijk CA, Morson BC, Meuwissen SGM, et al. Histopathological evaluation of colonic mucosal biopsy specimens in chronic inflammatory bowel disease: diagnostic implications. Gut 1991;32:1514-1520. https://doi.org/10.1136/gut.32.12.1514
  117. Theodossi A, Spiegelhalter DJ, Jass J, et al. Observer variation and discriminatory value of biopsy features in inflammatory bowel disease. Gut 1994;35:961-968. https://doi.org/10.1136/gut.35.7.961
  118. Wolfson DM, Sachar DB, Cohen A, et al. Granulomas do not affect postoperative recurrence rates in Crohn's disease. Gastroenterology 1982;83:405-409.
  119. Keller KM, Bender SW, Kirchmann H, et al. Diagnostic significance of epithelioid granulomas in Crohn’s disease in children. Multicenter Paediatric Crohn’s Disease Study Group. J Pediatr Gastroenterol Nutr 1990;10:27-32. https://doi.org/10.1097/00005176-199001000-00005
  120. Mahadeva U, Martin JP, Patel NK, et al. Granulomatous ulcerative colitis: a re-appraisal of the mucosal granuloma in the distinction of Crohn’s disease from ulcerative colitis. Histopathology 2002;41:50-55. https://doi.org/10.1046/j.1365-2559.2002.01416.x
  121. 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;50:93-105. https://doi.org/10.1136/jcp.50.2.93
  122. Lennard-Jones JE. Crohn's disease: definition, pathogenesis, aetiology. Clin Gastroenterol 1980;I:S173-S189.
  123. Kim KM, Lee A, Choi KY, et al. Intestinal tuberculosis: clinicopathologic analysis and diagnosis by endoscopic biopsy. Am J Gastroenterol 1998;93:606-609. https://doi.org/10.1111/j.1572-0241.1998.173_b.x
  124. Gan HT, Chen YQ, Ouyang Q, et al. Differentiation between intestinal tuberculosis and Crohn’s disease in endoscopic biopsy specimens by polymerase chain reaction. Am J Gastroenterol 2002;97:1446-1451. https://doi.org/10.1111/j.1572-0241.2002.05686.x
  125. Kirsch R, Pentecost M, Hall Pde M, et al. Role of colonoscopic biopsy in distinguishing between Crohn’s disease and intestinal tuberculosis. J Clin Pathol 2006;59:840-844. https://doi.org/10.1136/jcp.2005.032383
  126. Pulimood AB, Ramakrishna BS, Kurian G, et al. Endoscopic mucosal biopsies are useful in distinguishing granulomatous colitis due to Crohn's disease from tuberculosis. Gut 1999; 45:537-541. https://doi.org/10.1136/gut.45.4.537
  127. Kumar NB, Nostrant TT, Appelman HD. The histopathological spectrum of acute self-limited colitis (acute infectioustype colitis). Am J Surg Pathol 1982;6:523-529. https://doi.org/10.1097/00000478-198209000-00004
  128. Surawicz CM, Belic L. Rectal biopsy helps to distinguish acute self-limited colitis from idiopathic inflammatory bowel disease. Gastroenterology 1984;85:104-113.
  129. Nostrant TT, Kumar NB, Appelman HD. Histopathology differentiates acute self-limited colitis from ulcerative colitis. Gastroenterology 1987;92:318-328.
  130. Sharif F, McDermott M, Dillon M, et al. Focally enhanced gastritis in children with Crohn’s disease and ulcerative colitis. Am J Gastroenterol 2002;97:1415-1420. https://doi.org/10.1111/j.1572-0241.2002.05785.x
  131. Xin W, Greenson JK. The clinical significance of focally enhanced gastritis. Am J Surg Pathol 2004;28:1347-1351. https://doi.org/10.1097/01.pas.0000138182.97366.b4
  132. Sheehan AL, Warren BF, Gear MW, et al. Fat-wrapping in Crohn’s disease: pathological basis and relevance to surgical practice. Br J Surg 1992;79:955-958. https://doi.org/10.1002/bjs.1800790934
  133. Borley NR, Mortensen NJ, Jewell DP, et al. The relationship between inflammatory and serosal connective tissue change in ileal Crohn’s disease: evidence for a possible causative link. J Pathol 2000;190:196-202. https://doi.org/10.1002/(SICI)1096-9896(200002)190:2<196::AID-PATH513>3.0.CO;2-5
  134. Kapoor VK. Abdominal tuberculosis. Postgrad Med J 1998; 74:459-467. https://doi.org/10.1136/pgmj.74.874.459
  135. Bhansali SK. Abdominal tuberculosis: experience with 300 cases. Am J Gastroenterol 1977;67:324-337.
  136. Tandon HD, Prakash A. Pathology of intestinal tuberculosis and its distinction from Crohn’s disease. Gut 1972;13:260-269. https://doi.org/10.1136/gut.13.4.260