Inflammatory Bowel Disease and Colorectal Cancer

 

 Buy Article Permissions and Reprints

Abstract

The prevalence of inflammatory bowel disease (IBD) continues to rise with the increasing rates in the developing world and the improving longevity of IBD patients. A diagnosis of colonic IBD is associated with an increased risk of colorectal cancer (CRC) and this accounts for approximately 15% of the estimated mortality from IBD. CRC in IBD appears to be a pathologically distinct entity and progress is being made to understand the unique components of this process with a view to better predicting outcomes and potentially improving surveillance, treatments, and eventually modifying risk. In the interim, patients are entered into surveillance programs designed to identify at-risk patients early and improve outcomes. Dramatic evolution of technology in this area has changed the landscape of surveillance and dysplasia management over the last decade and promises to continue to do so. This review aims to provide a contemporary overview of IBD-associated CRC in terms of its epidemiology, pathogenesis, surveillance, and management.

Publication History

Received: 01 December 2022

Accepted: 05 December 2022

Article published online:
19 January 2023

© 2023. Thieme. All rights reserved.

Thieme Medical Publishers, Inc.
333 Seventh Avenue, 18th Floor, New York, NY 10001, USA

• References

• 1 Crohn B, Rosenberg H. The sigmoidoscopic picture of chronic ulcerative colitis (non-specific). Am J Med Sci 1925; 170: 220-228
  Google Scholar
• 2 Eaden JA, Abrams KR, Mayberry JF. The risk of colorectal cancer in ulcerative colitis: a meta-analysis. Gut 2001; 48 (04) 526-535
  Google Scholar
• 3 Lakatos L, Mester G, Erdelyi Z. et al. Risk factors for ulcerative colitis-associated colorectal cancer in a Hungarian cohort of patients with ulcerative colitis: results of a population-based study. Inflamm Bowel Dis 2006; 12 (03) 205-211
  CrossrefPubMedGoogle Scholar
• 4 Jess T, Rungoe C, Peyrin-Biroulet L. Risk of colorectal cancer in patients with ulcerative colitis: a meta-analysis of population-based cohort studies. Clin Gastroenterol Hepatol 2012; 10 (06) 639-645
  CrossrefPubMedGoogle Scholar
• 5 Bernstein CN, Blanchard JF, Kliewer E, Wajda A. Cancer risk in patients with inflammatory bowel disease: a population-based study. Cancer 2001; 91 (04) 854-862
  CrossrefPubMedGoogle Scholar
• 6 Canavan C, Abrams KR, Mayberry J. Meta-analysis: colorectal and small bowel cancer risk in patients with Crohn's disease. Aliment Pharmacol Ther 2006; 23 (08) 1097-1104
  CrossrefPubMedGoogle Scholar
• 7 Gatenby G, Glyn T, Pearson J, Gearry R, Eglinton T. The long-term incidence of dysplasia and colorectal cancer in a Crohn's colitis population-based cohort. Colorectal Dis 2021; 23 (09) 2399-2406
  CrossrefPubMedGoogle Scholar
• 8 Laine L, Kaltenbach T, Barkun A, McQuaid KR, Subramanian V, Soetikno R. SCENIC Guideline Development Panel. SCENIC international consensus statement on surveillance and management of dysplasia in inflammatory bowel disease. Gastrointest Endosc 2015; 81 (03) 489-501.e26
  Google Scholar
• 9 Magro F, Gionchetti P, Eliakim R. et al; European Crohn's and Colitis Organisation [ECCO]. Third European Evidence-based Consensus on Diagnosis and Management of Ulcerative Colitis. Part 1: Definitions, diagnosis, extra-intestinal manifestations, pregnancy, cancer surveillance, surgery, and ileo-anal pouch disorders. J Crohn's Colitis 2017; 11 (06) 649-670
  CrossrefPubMedGoogle Scholar
• 10 Murthy SK, Feuerstein JD, Nguyen GC, Velayos FS. AGA Clinical Practice Update on endoscopic surveillance and management of colorectal dysplasia in inflammatory bowel diseases: expert review. Gastroenterology 2021; 161 (03) 1043-1051.e4
  CrossrefPubMedGoogle Scholar
• 11 Wilks S. Morbid appearances in the intestine of Miss Bankes. Med Times Gazette 1859; 2 (02) 264-265
  PubMedGoogle Scholar
• 12 Crohn BB, Ginzburg L, Oppenheimer GD. Regional ileitis: a pathologic and clinical entity. J Am Med Assoc 1932; 99 (16) 1323-1329
  CrossrefPubMedGoogle Scholar
• 13 Ng SC, Shi HY, Hamidi N. et al. Worldwide incidence and prevalence of inflammatory bowel disease in the 21st century: a systematic review of population-based studies. Lancet 2017; 390 (10114): 2769-2778
  CrossrefPubMedGoogle Scholar
• 14 Molodecky NA, Soon IS, Rabi DM. et al. Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology 2012; 142 (01) 46-54.e42 , quiz e30
  CrossrefPubMedGoogle Scholar
• 15 Yang S-K, Yun S, Kim J-H. et al. Epidemiology of inflammatory bowel disease in the Songpa-Kangdong district, Seoul, Korea, 1986-2005: a KASID study. Inflamm Bowel Dis 2008; 14 (04) 542-549
  CrossrefPubMedGoogle Scholar
• 16 Manninen P, Karvonen A-L, Huhtala H. et al. The risk of colorectal cancer in patients with inflammatory bowel diseases in Finland: a follow-up of 20 years. J Crohn's Colitis 2013; 7 (11) e551-e557
  CrossrefPubMedGoogle Scholar
• 17 Tranter-Entwistle I, Mullaney TG, Noah K. et al. Long-term incidence of dysplasia and colorectal cancer in an ulcerative colitis population-based cohort. ANZ J Surg 2020; 90 (05) 821-825
  CrossrefPubMedGoogle Scholar
• 18 Kiran RP, Khoury W, Church JM, Lavery IC, Fazio VW, Remzi FH. Colorectal cancer complicating inflammatory bowel disease: similarities and differences between Crohn's and ulcerative colitis based on three decades of experience. Ann Surg 2010; 252 (02) 330-335
  CrossrefPubMedGoogle Scholar
• 19 Jewel Samadder N, Valentine JF, Guthery S. et al. Colorectal cancer in inflammatory bowel diseases: a population-based study in Utah. Dig Dis Sci 2017; 62 (08) 2126-2132
  CrossrefPubMedGoogle Scholar
• 20 Najafimehr H, Aghdaei HA, Pourhoseingholi MA. et al. A systematic review and meta-analysis on the association between inflammatory bowel disease family history and colorectal cancer. Gastroenterol Res Pract 2021; 2021: 4874459
  CrossrefPubMedGoogle Scholar
• 21 Allende D, Elmessiry M, Hao W. et al. Inter-observer and intra-observer variability in the diagnosis of dysplasia in patients with inflammatory bowel disease: correlation of pathological and endoscopic findings. Colorectal Dis 2014; 16 (09) 710-718 , discussion 718
  CrossrefPubMedGoogle Scholar
• 22 Driessen A, Macken E, Moreels T, Jouret-Mourin A. Dysplasia in inflammatory bowel disease. Acta Gastroenterol Belg 2017; 80 (02) 299-308
  PubMedGoogle Scholar
• 23 Kabir M, Fofaria R, Arebi N. et al. Systematic review with meta-analysis: IBD-associated colonic dysplasia prognosis in the videoendoscopic era (1990 to present). Aliment Pharmacol Ther 2020; 52 (01) 5-19
  CrossrefPubMedGoogle Scholar
• 24 Fogt F, Vortmeyer AO, Goldman H, Giordano TJ, Merino MJ, Zhuang Z. Comparison of genetic alterations in colonic adenoma and ulcerative colitis-associated dysplasia and carcinoma. Hum Pathol 1998; 29 (02) 131-136
  CrossrefPubMedGoogle Scholar
• 25 Robles AI, Traverso G, Zhang M. et al. Whole-exome sequencing analyses of inflammatory bowel disease-associated colorectal cancers. Gastroenterology 2016; 150 (04) 931-943
  CrossrefPubMedGoogle Scholar
• 26 Yu LC. Microbiota dysbiosis and barrier dysfunction in inflammatory bowel disease and colorectal cancers: exploring a common ground hypothesis. J Biomed Sci 2018; 25 (01) 79
  CrossrefPubMedGoogle Scholar
• 27 Vogelstein B, Fearon ER, Hamilton SR. et al. Genetic alterations during colorectal-tumor development. N Engl J Med 1988; 319 (09) 525-532
  CrossrefPubMedGoogle Scholar
• 28 Umetani N, Sasaki S, Watanabe T. et al. Genetic alterations in ulcerative colitis-associated neoplasia focusing on APC, K-ras gene and microsatellite instability. Jpn J Cancer Res 1999; 90 (10) 1081-1087
  CrossrefPubMedGoogle Scholar
• 29 Sato A, MacHinami R. p53 immunohistochemistry of ulcerative colitis-associated with dysplasia and carcinoma. Pathol Int 1999; 49 (10) 858-868
  CrossrefPubMedGoogle Scholar
• 30 Burmer GC, Rabinovitch PS, Haggitt RC. et al. Neoplastic progression in ulcerative colitis: histology, DNA content, and loss of a p53 allele. Gastroenterology 1992; 103 (05) 1602-1610
  CrossrefPubMedGoogle Scholar
• 31 Liu X, Goldblum JR, Zhao Z. et al. Distinct clinicohistologic features of inflammatory bowel disease-associated colorectal adenocarcinoma: in comparison with sporadic microsatellite-stable and Lynch syndrome-related colorectal adenocarcinoma. Am J Surg Pathol 2012; 36 (08) 1228-1233
  CrossrefPubMedGoogle Scholar
• 32 Lamb CA, Kennedy NA, Raine T. et al; IBD Guidelines eDelphi Consensus Group. British Society of Gastroenterology consensus guidelines on the management of inflammatory bowel disease in adults. Gut 2019; 68 (Suppl. 03) s1-s106
  CrossrefPubMedGoogle Scholar
• 33 Tytgat GNJ, Dhir V, Gopinath N. Endoscopic appearance of dysplasia and cancer in inflammatory bowel disease. Eur J Cancer 1995; 31A (7-8): 1174-1177
  CrossrefPubMedGoogle Scholar
• 34 Moussata D, Allez M, Cazals-Hatem D. et al; The GETAID. Are random biopsies still useful for the detection of neoplasia in patients with IBD undergoing surveillance colonoscopy with chromoendoscopy?. Gut 2018; 67 (04) 616-624
  PubMedGoogle Scholar
• 35 Chiu K, Riddell RH, Schaeffer DF. DALM, rest in peace: a pathologist's perspective on dysplasia in inflammatory bowel disease in the post-DALM era. Mod Pathol 2018; 31 (08) 1180-1190
  Google Scholar
• 36 Carballal S, Maisterra S, López-Serrano A. et al; EndoCAR Group of the Spanish Gastroenterological Association and Spanish Digestive Endoscopy Society. Real-life chromoendoscopy for neoplasia detection and characterisation in long-standing IBD. Gut 2018; 67 (01) 70-78
  CrossrefPubMedGoogle Scholar
• 37 Alexandersson B, Hamad Y, Andreasson A. et al. High-definition chromoendoscopy superior to high-definition white-light endoscopy in surveillance of inflammatory bowel diseases in a randomized trial. Clin Gastroenterol Hepatol 2020; 18 (09) 2101-2107
  CrossrefPubMedGoogle Scholar
• 38 Wan J, Wang X, Yang ZP, Wu KC. Systematic review with meta-analysis: chromoendoscopy versus white light endoscopy in detection of dysplasia in patients with inflammatory bowel disease. J Dig Dis 2019; 20 (04) 206-214
  CrossrefPubMedGoogle Scholar
• 39 Iacucci M, Kaplan GG, Panaccione R. et al. A randomized trial comparing high definition colonoscopy alone with high definition dye spraying and electronic virtual chromoendoscopy for detection of colonic neoplastic lesions during IBD surveillance colonoscopy. Am J Gastroenterol 2018; 113 (02) 225-234
  CrossrefPubMedGoogle Scholar
• 40 Bessissow T, Dulai PS, Restellini S. et al. Comparison of endoscopic dysplasia detection techniques in patients with ulcerative colitis: a systematic review and network meta-analysis. Inflamm Bowel Dis 2018; 24 (12) 2518-2526
  CrossrefPubMedGoogle Scholar
• 41 Hu AB, Burke KE, Kochar B, Ananthakrishnan AN. Yield of random biopsies during colonoscopies in inflammatory bowel disease patients undergoing dysplasia surveillance. Inflamm Bowel Dis 2021; 27 (06) 779-786
  CrossrefPubMedGoogle Scholar
• 42 Ahmed T, Monti J, Lashner B. Random versus targeted biopsies for colorectal cancer surveillance in inflammatory bowel disease. Gastroenterol Hepatol (N Y) 2010; 6 (07) 438-442
  PubMedGoogle Scholar
• 43 Watanabe T, Ajioka Y, Mitsuyama K. et al. Comparison of targeted vs random biopsies for surveillance of ulcerative colitis-associated colorectal cancer. Gastroenterology 2016; 151 (06) 1122-1130
  CrossrefPubMedGoogle Scholar
• 44 Soetikno R, East J, Suzuki N. et al. Endoscopic submucosal dissection for nonpolypoid colorectal dysplasia in patients with inflammatory bowel disease: in medias res. Gastrointest Endosc 2018; 87 (04) 1085-1094
  CrossrefPubMedGoogle Scholar
• 45 Lord R, Burr NE, Mohammed N, Subramanian V. Colonic lesion characterization in inflammatory bowel disease: a systematic review and meta-analysis. World J Gastroenterol 2018; 24 (10) 1167-1180
  CrossrefPubMedGoogle Scholar
• 46 Iacucci M, McQuaid K, Gui XS. et al. A multimodal (FACILE) classification for optical diagnosis of inflammatory bowel disease associated neoplasia. Endoscopy 2019; 51 (02) 133-141
  Article in Thieme ConnectPubMedGoogle Scholar
• 47 Buchner AM. Endoscopic management of complex lesions in patients with inflammatory bowel disease. Gastroenterol Hepatol (N Y) 2021; 17 (03) 121-127
  PubMedGoogle Scholar
• 48 Shen B, Kochhar G, Navaneethan U. et al; Global Interventional Inflammatory Bowel Disease Group. Role of interventional inflammatory bowel disease in the era of biologic therapy: a position statement from the Global Interventional IBD Group. Gastrointest Endosc 2019; 89 (02) 215-237
  CrossrefPubMedGoogle Scholar
• 49 Kinoshita S, Uraoka T, Nishizawa T. et al. The role of colorectal endoscopic submucosal dissection in patients with ulcerative colitis. Gastrointest Endosc 2018; 87 (04) 1079-1084
  CrossrefPubMedGoogle Scholar
• 50 Suzuki N, Toyonaga T, East JE. Endoscopic submucosal dissection of colitis-related dysplasia. Endoscopy 2017; 49 (12) 1237-1242
  Article in Thieme ConnectPubMedGoogle Scholar
• 51 Bernstein CN, Shanahan F, Weinstein WM. Are we telling patients the truth about surveillance colonoscopy in ulcerative colitis?. Lancet 1994; 343 (8889): 71-74
  Google Scholar
• 52 Vogel JD, Eskicioglu C, Weiser MR, Feingold DL, Steele SR. The American Society of Colon and Rectal Surgeons Clinical Practice Guidelines for the treatment of colon cancer. Dis Colon Rectum 2017; 60 (10) 999-1017
  CrossrefPubMedGoogle Scholar
• 53 Rubin DT, Ananthakrishnan AN, Siegel CA, Sauer BG, Long MD. ACG clinical guideline: ulcerative colitis in adults. Am J Gastroenterol 2019; 114 (03) 384-413
  CrossrefPubMedGoogle Scholar
• 54 Maser EA, Sachar DB, Kruse D, Harpaz N, Ullman T, Bauer JJ. High rates of metachronous colon cancer or dysplasia after segmental resection or subtotal colectomy in Crohn's colitis. Inflamm Bowel Dis 2013; 19 (09) 1827-1832
  PubMedGoogle Scholar
• 55 Bogach J, Pond G, Eskicioglu C, Simunovic M, Seow H. Extent of surgical resection in inflammatory bowel disease associated colorectal cancer: a population-based study. J Gastrointest Surg 2021; 25 (10) 2610-2618
  Google Scholar
• 56 Kiran RP, Nisar PJ, Goldblum JR. et al. Dysplasia associated with Crohn's colitis: segmental colectomy or more extended resection?. Ann Surg 2012; 256 (02) 221-226
  CrossrefPubMedGoogle Scholar
• 57 Axelrad J, Kriplani A, Ozbek U. et al. Chemotherapy tolerance and oncologic outcomes in patients with colorectal cancer with and without inflammatory bowel disease. Clin Colorectal Cancer 2017; 16 (03) e205-e210
  CrossrefPubMedGoogle Scholar
• 58 Johnson DB, Sullivan RJ, Menzies AM. Immune checkpoint inhibitors in challenging populations. Cancer 2017; 123 (11) 1904-1911
  CrossrefPubMedGoogle Scholar
• 59 Bogach J, Pond G, Eskicioglu C, Seow H. Age-related survival differences in patients with inflammatory bowel disease-associated colorectal cancer: a population-based cohort study. Inflamm Bowel Dis 2019; 25 (12) 1957-1965
  Google Scholar
• 60 Taylor CC, Millien VO, Hou JK, Massarweh NN. Association between inflammatory bowel disease and colorectal cancer stage of disease and survival. J Surg Res 2020; 247: 77-85
  CrossrefPubMedGoogle Scholar
• 61 Lu C, Schardey J, Zhang T. et al. Survival outcomes and clinicopathological features in inflammatory bowel disease-associated colorectal cancer: a systematic review and meta-analysis. Ann Surg 2022; 276 (05) e319-e330
  CrossrefPubMedGoogle Scholar
• 62 Saraggi D, Fassan M, Mescoli C. et al. The molecular landscape of colitis-associated carcinogenesis. Dig Liver Dis 2017; 49 (04) 326-330
  CrossrefPubMedGoogle Scholar
• 63 Bojarski C, Waldner M, Rath T. et al. Innovative diagnostic endoscopy in inflammatory bowel diseases: from high-definition to molecular endoscopy. Front Med (Lausanne) 2021; 8: 655404
  CrossrefPubMedGoogle Scholar
• 64 The National Institute for Health and Care Excellence. Colorectal cancer prevention: colonoscopic surveillance in adults with ulcerative colitis, Crohn's disease or adenomas (CG118). March 23, 2011. Accessed December 22, 2022: https://www.nice.org.uk/guidance/cg118
  PubMedGoogle Scholar