Colorectal cancer in inflammatory bowel disease: review of the evidence

Ferlay J, Soerjomataram I, Dikshit R et al (2015) Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 136:E359–E386

Bradley CJ, Lansdorp-Vogelaar I, Yabroff KR et al (2011) Productivity savings from colorectal cancer prevention and control strategies. Am J Prev Med 41:e5–e14

Burisch J, Jess T, Martinato M, Lakatos PL, ECCO E (2013) The burden of inflammatory bowel disease in Europe. J Crohns Colitis 7:322–337

Loftus EVJ (2004) Clinical epidemiology of inflammatory bowel disease: incidence, prevalence, and environmental influences. Gastroenterology 126:1504–1517

Gheorghe C, Pascu O, Gheorghe L et al (2004) Epidemiology of inflammatory bowel disease in adults who refer to gastroenterology care in Romania: a multicentre study. Eur J Gastroenterol Hepatol 16:1153–1159

Mattar MC, Lough D, Pishvaian MJ, Charabaty A (2011) Current management of inflammatory bowel disease and colorectal cancer. Gastrointest Cancer Res 4:53–61

Ekbom A, Helmick C, Zack M, Adami HO (1990) Ulcerative colitis and colorectal cancer. A population-based study. N Engl J Med 323:1228–1233

Brackmann S, Andersen SN, Aamodt G et al (2009) Two distinct groups of colorectal cancer in inflammatory bowel disease. Inflamm Bowel Dis 15:9–16

Bernstein CN, Blanchard JF, Kliewer E, Wajda A (2001) Cancer risk in patients with inflammatory bowel disease: a population-based study. Cancer 91:854–862

Eaden JA, Abrams KR, Mayberry JF (2001) The risk of colorectal cancer in ulcerative colitis: a meta-analysis. Gut 48:526–535

Mellemkjaer L, Olsen JH, Frisch M, Johansen C, Gridley G, McLaughlin JK (1995) Cancer in patients with ulcerative colitis. Int J Cancer 60:330–333

von Roon AC, Reese G, Teare J, Constantinides V, Darzi AW, Tekkis PP (2007) The risk of cancer in patients with Crohn’s disease. Dis Colon Rectum 50:839–855

Canavan C, Abrams KR, Mayberry J (2006) Meta-analysis: colorectal and small bowel cancer risk in patients with Crohn’s disease. Aliment Pharmacol Ther 23:1097–1104

Jess T, Simonsen J, Jørgensen KT, Pedersen BV, Nielsen NM, Frisch M. Decreasing risk of colorectal cancer in patients with inflammatory bowel disease over 30 years. Gastroenterology. 2012;143:375.e1–381.e1 (quiz e13)

Jess T, Loftus EV, Velayos FS et al (2006) Risk of intestinal cancer in inflammatory bowel disease: a population-based study from olmsted county, Minnesota. Gastroenterology 130:1039–1046

Kappelman MD, Farkas DK, Long MD et al. Risk of cancer in patients with inflammatory bowel diseases: a nationwide population-based cohort study with 30 years of follow-up evaluation. Clin Gastroenterol Hepatol. 2014;12:265.e1–273.e1

Tsianos (2000) Risk of cancer in inflammatory bowel disease (IBD). Eur J Intern Med 11:75–78

Lutgens MW, van Oijen MG, van der Heijden GJ, Vleggaar FP, Siersema PD, Oldenburg B (2013) Declining risk of colorectal cancer in inflammatory bowel disease: an updated meta-analysis of population-based cohort studies. Inflamm Bowel Dis 19:789–799

Fornaro R, Caratto M, Caratto E et al (2016) Colorectal cancer in patients with inflammatory bowel disease: the need for a real surveillance program. Clin Colorectal Cancer 15:204–212

Rutter MD, Saunders BP, Wilkinson KH et al (2006) Thirty-year analysis of a colonoscopic surveillance program for neoplasia in ulcerative colitis. Gastroenterology 130:1030–1038

Ullman T, Odze R, Farraye FA (2009) Diagnosis and management of dysplasia in patients with ulcerative colitis and Crohn’s disease of the colon. Inflamm Bowel Dis 15:630–638

van den Heuvel TR, Wintjens DS, Jeuring SF et al (2016) Inflammatory bowel disease, cancer and medication: cancer risk in the Dutch population-based IBDSL cohort. Int J Cancer 139:1270–1280

Scaringi S, Di Martino C, Zambonin D et al (2013) Colorectal cancer and Crohn’s colitis: clinical implications from 313 surgical patients. World J Surg 37:902–910

Nuako KW, Ahlquist DA, Mahoney DW, Schaid DJ, Siems DM, Lindor NM (1998) Familial predisposition for colorectal cancer in chronic ulcerative colitis: a case–control study. Gastroenterology 115:1079–1083

Askling J, Dickman PW, Karlén P et al (2001) Family history as a risk factor for colorectal cancer in inflammatory bowel disease. Gastroenterology 120:1356–1362

Sebastian S, Hernández V, Myrelid P et al (2014) Colorectal cancer in inflammatory bowel disease: results of the 3rd ECCO pathogenesis scientific workshop (I). J Crohns Colitis 8:5–18

Feagins LA, Souza RF, Spechler SJ (2009) Carcinogenesis in IBD: potential targets for the prevention of colorectal cancer. Nat Rev Gastroenterol Hepatol 6:297–305

Itzkowitz SH, Yio X (2004) Inflammation and cancer IV. Colorectal cancer in inflammatory bowel disease: the role of inflammation. Am J Physiol Gastrointest Liver Physiol 287:G7–G17

Westbrook AM, Szakmary A, Schiestl RH (2010) Mechanisms of intestinal inflammation and development of associated cancers: lessons learned from mouse models. Mutat Res 705:40–59

Goel GA, Kandiel A, Achkar JP, Lashner B (2011) Molecular pathways underlying IBD-associated colorectal neoplasia: therapeutic implications. Am J Gastroenterol 106:719–730

McConnell BB, Yang VW (2009) The role of inflammation in the pathogenesis of colorectal cancer. Curr Colorectal Cancer Rep 5:69–74

Dirisina R, Katzman RB, Goretsky T et al (2011) p53 and PUMA independently regulate apoptosis of intestinal epithelial cells in patients and mice with colitis. Gastroenterology 141:1036–1045

Velayos FS, Loftus EV, Jess T et al (2006) Predictive and protective factors associated with colorectal cancer in ulcerative colitis: a case–control study. Gastroenterology 130:1941–1949

Bezzio C, Festa S, Saibeni S, Papi C (2017) Chemoprevention of colorectal cancer in ulcerative colitis: digging deep in current evidence. Expert Rev Gastroenterol Hepatol 11:339–347

Kang M, Martin A (2017) Microbiome and colorectal cancer: unraveling host-microbiota interactions in colitis-associated colorectal cancer development. Semin Immunol 32:3

Grivennikov SI (2013) Inflammation and colorectal cancer: colitis-associated neoplasia. Semin Immunopathol 35:229–244

McCoy AN, Araújo-Pérez F, Azcárate-Peril A, Yeh JJ, Sandler RS, Keku TO (2013) Fusobacterium is associated with colorectal adenomas. PLoS One 8:e53653

Arthur JC, Perez-Chanona E, Mühlbauer M et al (2012) Intestinal inflammation targets cancer-inducing activity of the microbiota. Science 338:120–123

Khan AA, Khan Z, Malik A et al (2017) Colorectal cancer-inflammatory bowel disease nexus and felony of Escherichia coli. Life Sci 180:60

Cooper K, Squires H, Carroll C et al (2010) Chemoprevention of colorectal cancer: systematic review and economic evaluation. Health Technol Assess 14:1–206

Johnson CC, Jankowski M, Rolnick S, Yood MU, Alford SH (2014) Influence of NSAID use among colorectal cancer survivors on cancer outcomes. Am J Clin Oncol

Haggar FA, Boushey RP (2009) Colorectal cancer epidemiology: incidence, mortality, survival, and risk factors. Clin Colon Rectal Surg 22:191–197

Ullman TA, Itzkowitz SH (2011) Intestinal inflammation and cancer. Gastroenterology 140:1807–1816

Pinczowski D, Ekbom A, Baron J, Yuen J, Adami HO (1994) Risk factors for colorectal cancer in patients with ulcerative colitis: a case–control study. Gastroenterology 107:117–120

Qiu X, Ma J, Wang K, Zhang H (2017) Chemopreventive effects of 5-aminosalicylic acid on inflammatory bowel disease-associated colorectal cancer and dysplasia: a systematic review with meta-analysis. Oncotarget 8:1031–1045

OʼConnor A, Packey CD, Akbari M, Moss AC (2015) Mesalamine, but Not sulfasalazine, reduces the risk of colorectal neoplasia in patients with inflammatory bowel disease: an agent-specific systematic review and meta-analysis. Inflamm Bowel Dis 21:2562–2569

Chapman CG, Rubin DT (2014) The potential for medical therapy to reduce the risk of colorectal cancer and optimize surveillance in inflammatory bowel disease. Gastrointest Endosc Clin N Am 24:353–365

Poutahidis T, Haigis KM, Rao VP et al (2007) Rapid reversal of interleukin-6-dependent epithelial invasion in a mouse model of microbially induced colon carcinoma. Carcinogenesis 28:2614–2623

Kim YJ, Hong KS, Chung JW, Kim JH, Hahm KB (2010) Prevention of colitis-associated carcinogenesis with infliximab. Cancer Prev Res (Phila) 3:1314–1333

Bassaganya-Riera J, Viladomiu M, Pedragosa M, De Simone C, Hontecillas R (2012) Immunoregulatory mechanisms underlying prevention of colitis-associated colorectal cancer by probiotic bacteria. PLoS One 7:e34676

Neumann H, Vieth M, Langner C, Neurath MF, Mudter J (2011) Cancer risk in IBD: how to diagnose and how to manage DALM and ALM. World J Gastroenterol 17:3184–3191

Guagnozzi D, Lucendo AJ (2012) Colorectal cancer surveillance in patients with inflammatory bowel disease: what is new. World J Gastrointest Endosc 4:108–116

Annese V, Daperno M, Rutter MD et al (2013) European evidence based consensus for endoscopy in inflammatory bowel disease. J Crohns Colitis 7:982–1018

Rex DK, Boland CR, Dominitz JA et al (2017) Colorectal cancer screening: recommendations for physicians and patients from the US Multi-Society Task Force on Colorectal Cancer. Gastroenterology 153:307–323

Cairns SR, Scholefield JH, Steele RJ et al (2010) Guidelines for colorectal cancer screening and surveillance in moderate and high risk groups (update from 2002). Gut 59:666–689

Abraham BP (2016) Cancer surveillance in ulcerative colitis and Crohn’s disease: new strategies. Curr Opin Gastroenterol 32:32–37

Kiesslich R, Goetz M, Lammersdorf K et al (2007) Chromoscopy-guided endomicroscopy increases the diagnostic yield of intraepithelial neoplasia in ulcerative colitis. Gastroenterology 132:874–882

Gabbani T, Manetti N, Bonanomi AG, Annese AL, Annese V (2015) New endoscopic imaging techniques in surveillance of inflammatory bowel disease. World J Gastrointest Endosc 7:230–236

Cheon JH (2015) Advances in the endoscopic assessment of inflammatory bowel diseases: cooperation between endoscopic and pathologic evaluations. J Pathol Transl Med 49:209–217

Lashner BA, Kane SV, Hanauer SB (1990) Colon cancer surveillance in chronic ulcerative colitis: historical cohort study. Am J Gastroenterol 85:1083–1087

Karlén P, Kornfeld D, Broström O, Löfberg R, Persson PG, Ekbom A (1998) Is colonoscopic surveillance reducing colorectal cancer mortality in ulcerative colitis? A population based case control study. Gut 42:711–714

Lutgens MW, Oldenburg B, Siersema PD et al (2009) Colonoscopic surveillance improves survival after colorectal cancer diagnosis in inflammatory bowel disease. Br J Cancer 101:1671–1675

Bye WA, Nguyen TM, Parker CE, Jairath V, East JE (2017) Strategies for detecting colon cancer in patients with inflammatory bowel disease. Cochrane Database Syst Rev 9:CD000279

Eaden JA, Ward BA, Mayberry JF (2000) How gastroenterologists screen for colonic cancer in ulcerative colitis: an analysis of performance. Gastrointest Endosc 51:123–128

van Rijn AF, Fockens P, Siersema PD, Oldenburg B (2009) Adherence to surveillance guidelines for dysplasia and colorectal carcinoma in ulcerative and Crohn’s colitis patients in the Netherlands. World J Gastroenterol 15:226–230

Feuerstein JD, Lewandowski JJ, Martinez-Vazquez M, Leffler DA, Cheifetz AS (2015) Documented compliance with inflammatory bowel disease quality measures is poor. Dig Dis Sci 60:339–344

Mayer R, Wong WD, Rothenberger DA, Goldberg SM, Madoff RD (1999) Colorectal cancer in inflammatory bowel disease: a continuing problem. Dis Colon Rectum 42:343–347

Brackmann S, Andersen SN, Aamodt G et al (2009) Relationship between clinical parameters and the colitis-colorectal cancer interval in a cohort of patients with colorectal cancer in inflammatory bowel disease. Scand J Gastroenterol 44:46–55

Ullman TA (2003) Patients with low-grade dysplasia should be advised to undergo colectomy. Inflamm Bowel Dis 9:267–269 (discussion 273)

Bach JF (2002) The effect of infections on susceptibility to autoimmune and allergic diseases. N Engl J Med 347:911–920

DeRoche TC, Xiao SY, Liu X (2014) Histological evaluation in ulcerative colitis. Gastroenterol Rep (Oxf) 2:178–192

Engelsgjerd M, Farraye FA, Odze RD (1999) Polypectomy may be adequate treatment for adenoma-like dysplastic lesions in chronic ulcerative colitis. Gastroenterology 117:1288–1294; (discussion 1488)

Odze RD, Farraye FA, Hecht JL, Hornick JL (2004) Long-term follow-up after polypectomy treatment for adenoma-like dysplastic lesions in ulcerative colitis. Clin Gastroenterol Hepatol 2:534–541

Rutter MD, Saunders BP, Wilkinson KH, Kamm MA, Williams CB, Forbes A (2004) Most dysplasia in ulcerative colitis is visible at colonoscopy. Gastrointest Endosc 60:334–339

Connell WR, Lennard-Jones JE, Williams CB, Talbot IC, Price AB, Wilkinson KH (1994) Factors affecting the outcome of endoscopic surveillance for cancer in ulcerative colitis. Gastroenterology 107:934–944

Jess T, Loftus EV, Velayos FS et al (2006) Incidence and prognosis of colorectal dysplasia in inflammatory bowel disease: a population-based study from Olmsted County, Minnesota. Inflamm Bowel Dis 12:669–676

Thomas T, Nair P, Dronfield MW, Mayberry JF (2005) Management of low and high-grade dysplasia in inflammatory bowel disease: the gastroenterologists’ perspective and current practice in the United Kingdom. Eur J Gastroenterol Hepatol 17:1317–1324

Althumairi AA, Lazarev MG, Gearhart SL (2016) Inflammatory bowel disease associated neoplasia: a surgeon’s perspective. World J Gastroenterol 22:961–973

Reynolds IS, O’Toole A, Deasy J, McNamara DA, Burke JP (2017) A meta-analysis of the clinicopathological characteristics and survival outcomes of inflammatory bowel disease associated colorectal cancer. Int J Colorectal Dis 32:443–451

Ou B, Zhao J, Guan S, Lu A (2016) Survival of colorectal cancer in patients with or without inflammatory bowel disease: a meta-analysis. Dig Dis Sci 61:881–889

Larsen M, Mose H, Gislum M et al (2007) Survival after colorectal cancer in patients with Crohn’s disease: a nationwide population-based Danish follow-up study. Am J Gastroenterol 102:163–167

Panis Y (1998) Is there a place for ileal pouch-anal anastomosis in patients with Crohn’s colitis. Neth J Med 53:S47–S51

Ramsey M, Krishna SG, Stanich PP et al (2017) Inflammatory bowel disease adversely impacts colorectal cancer surgery short-term outcomes and health-care resource utilization. Clin Transl Gastroenterol 8:e127

Coviello LC, Stein SL (2014) Surgical management of nonpolypoid colorectal lesions and strictures in colonic inflammatory bowel disease. Gastrointest Endosc Clin N Am 24:447–454

Svrcek M, Cosnes J, Beaugerie L et al (2007) Colorectal neoplasia in Crohn’s colitis: a retrospective comparative study with ulcerative colitis. Histopathology 50:574–583

Deutsch AA, McLeod RS, Cullen J, Cohen Z (1991) Results of the pelvic-pouch procedure in patients with Crohn’s disease. Dis Colon Rectum 34:475–477

Keighley MR (2000) The final diagnosis in pouch patients for presumed ulcerative colitis may change to Crohn’s disease: patients should be warned of the consequences. Acta Chir Iugosl 47:27–31

Melton GB, Fazio VW, Kiran RP et al (2008) Long-term outcomes with ileal pouch-anal anastomosis and Crohn’s disease: pouch retention and implications of delayed diagnosis. Ann Surg 248:608–616

Tekkis PP, Heriot AG, Smith O, Smith JJ, Windsor AC, Nicholls RJ (2005) Long-term outcomes of restorative proctocolectomy for Crohn’s disease and indeterminate colitis. Colorectal Dis 7:218–223

Lightner AL, Fletcher JG, Pemberton JH, Mathis KL, Raffals LE, Smyrk T (2017) Crohn’s disease of the pouch: a true diagnosis or an oversubscribed diagnosis of exclusion. Dis Colon Rectum 60:1201–1208

Panis Y, Poupard B, Nemeth J, Lavergne A, Hautefeuille P, Valleur P (1996) Ileal pouch/anal anastomosis for Crohn’s disease. Lancet 347:854–857

Gentilini L, Coscia M, Laureti S, Poggioli G (2011) Surgery in presence of dysplasia in IBD. Ann Ital Chir 82:37–40

Liu X, Goldblum JR, Zhao Z et al (2012) 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 36:1228–1233

Tiersten A, Saltz LB (1996) Influence of inflammatory bowel disease on the ability of patients to tolerate systemic fluorouracil-based chemotherapy. J Clin Oncol 14:2043–2046

Dugum M, Lin J, Lopez R et al (2017) Recurrence and survival rates of inflammatory bowel disease-associated colorectal cancer following postoperative chemotherapy: a comparative study. Gastroenterol Rep (Oxf) 5:57–61

Axelrad J, Kriplani A, Ozbek U et al (2017) Chemotherapy tolerance and oncologic outcomes in patients with colorectal cancer with and without inflammatory bowel disease. Clin Colorectal Cancer 16:e205–e210

Renz BW, Thasler WE, Preissler G et al (2013) Clinical outcome of IBD-associated versus sporadic colorectal cancer: a matched-pair analysis. J Gastrointest Surg 17:981–990

Hrabe JE, Byrn JC, Button AM, Zamba GK, Kapadia MR, Mezhir JJ (2014) A matched case–control study of IBD-associated colorectal cancer: IBD portends worse outcome. J Surg Oncol 109:117–121

Kim BJ, Yang SK, Kim JS et al (2009) Trends of ulcerative colitis-associated colorectal cancer in Korea: a KASID study. J Gastroenterol Hepatol 24:667–671

Kim AH, Roberts C, Feagan BG et al (2017) Developing a standard set of patient-centred outcomes for inflammatory bowel disease—an international, cross-disciplinary consensus. J Crohns Colitis 12:408

Annese V, Beaugerie L, Egan L et al (2015) European evidence-based consensus: inflammatory bowel disease and malignancies. J Crohns Colitis 9:945–965