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Colorectal Cancer in Patients With Inflammatory Bowel Disease: The Need for a Real Surveillance Program

Published:February 12, 2016DOI:https://doi.org/10.1016/j.clcc.2016.02.002

      Abstract

      The association between inflammatory bowel disease (IBD) and colorectal cancer (CRC) has been widely shown. This association is responsible for 10% to 15% of deaths in patients with IBD, even if according to some studies, the risk of developing CRC seems to be decreased. An adequate surveillance of patients identified as at-risk patients, might improve the management of IBD-CRC risk. In this article we review the literature data related to IBD-CRC, analyze potential risk factors such as severity of inflammation, duration, and extent of IBD, age at diagnosis, sex, family history of sporadic CRC, and coexistent primary sclerosing cholangitis, and update epidemiology on the basis of new studies. Confirmed risk factors for IBD-CRC are severity, extent, and duration of colitis, the presence of coexistent primary sclerosing cholangitis, and a family history of CRC. Current evidence-based guidelines recommend surveillance colonoscopy for patients with colitis 8 to 10 years after diagnosis, further surveillance is decided on the basis of patient risk factors. The classic white light endoscopy, with random biopsies, is now considered unsatisfactory. The evolution of technology has led to the development of new techniques that promise to increase the effectiveness of the monitoring programs. Chromoendoscopy has already proved highly effective and several guidelines suggest its use with a target biopsy. Confocal endomicroscopy and autofluorescence imaging are currently being tested and for this reason they have not yet been considered as useful in surveillance programs.

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      References

        • Connelly T.M.
        • Koltun W.A.
        The cancer “fear” in IBD patients: is it still real?.
        J Gastrointest Surg. 2014; 18: 213-218
        • Shah S.A.
        • Rubin D.T.
        • Farraye F.A.
        Chromoendoscopy for colorectal cancer surveillance in patients with inflammatory bowel disease.
        Curr Gastroenterol Rep. 2014; 16: 407
        • Dyson J.K.
        • Rutter M.D.
        Colorectal cancer in inflammatory bowel disease: what is the real magnitude of the risk?.
        World J Gastroenterol. 2012; 18: 3839-3848
        • Fornaro R.
        • Frascio M.
        • Denegri A.
        • et al.
        Crohn's disease and cancer.
        Ann Ital Chir. 2009; 80 ([in Italian]): 119-125
        • Denegri A.
        • Paparo F.
        • Fornaro R.
        Crohn's disease and colorectal cancer.
        in: Santoro G.A. Cancer of the Rectum. InTech Janeza Trdine 951000 Rijeka, Croatia - EUROPEAN UNION, 2011: 29-46
        • Schmidt C.
        • Bielecki C.
        • Felber J.
        • Stallmach A.
        Surveillance strategies in inflammatory bowel disease.
        Minerva Gastroenterol Dietol. 2010; 56: 189-201
        • Canavan C.
        • Abrams K.R.
        • Mayberry J.
        Meta-analysis: colorectal and small bowel cancer risk in patients with Crohn's disease.
        Aliment Pharmacol Ther. 2006; 23: 1097-1104
        • Bargen J.A.
        Chronic ulcerative colitis associated with malignant disease. 1928.
        Dis Colon Rectum. 1994; 37: 727-730
        • Andersen N.N.
        • Jess T.
        Has the risk of colorectal cancer in inflammatory bowel disease decreased?.
        World J Gastroenterol. 2013; 19: 7561-7568
        • Paparo F.
        • Denegri A.
        • Revelli M.
        • et al.
        Crohn's Disease: value of diagnostic imaging in the evaluation of anastomotic recurrence.
        Ann Ital Chir. 2014; 85: 271-281
        • Fornaro R.
        • Caratto E.
        • Caratto M.
        • et al.
        Post-operative recurrence in Crohn's disease. Critical analysis of potential risk factors. An update.
        Surgeon. 2015; 13: 330-347
        • Averboukh F.
        • Ziv Y.
        • Kariv Y.
        • et al.
        Colorectal carcinoma in inflammatory bowel disease: a comparison between Crohn's and ulcerative colitis.
        Colorectal Dis. 2011; 13: 1230-1236
        • Bae S.I.
        • Kim Y.S.
        Colon cancer screening and surveillance in inflammatory bowel disease.
        Clin Endosc. 2014; 47: 509-515
        • Mattar M.C.
        • Lough D.
        • Pishvaian M.J.
        • Charabaty A.
        Current management of inflammatory bowel disease and colorectal cancer.
        Gastrointest Cancer Res. 2011; 4: 53-61
        • Vagefi P.A.
        • Longo W.E.
        Colorectal cancer in patients with inflammatory bowel disease.
        Clin Colorectal Cancer. 2005; 4: 313-319
        • 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: 639-645
        • Castaño-Milla C.
        • Chaparro M.
        • Gisbert J.P.
        Systematic review with meta-analysis: the declining risk of colorectal cancer in ulcerative colitis.
        Aliment Pharmacol Ther. 2014; 39: 645-659
        • Eaden J.A.
        • Abramsb K.R.
        • Mayberry J.F.
        The risk of colorectal cancer in ulcerative colitis: a meta-analysis.
        Gut. 2001; 48: 526-535
        • Von Roon A.
        • Reese G.
        • Teare J.
        • Constantinides V.
        • Darzi A.W.
        • Tekkis P.P.
        The risk of cancer in patients with Crohn's disease.
        Dis Colon Rectum. 2007; 50: 839-855
        • Laukoetter M.G.
        • Mennigen R.
        • Hannig C.M.
        • et al.
        Intestinal cancer risk in Crohn's disease: a meta-analysis.
        J Gastrointest Surg. 2011; 15: 576-583
        • Basseri R.J.
        • Basseri B.
        • Vassilaki M.E.
        • et al.
        Colorectal cancer screening and surveillance in Crohn's colitis.
        J Crohns Colitis. 2012; 6: 824-829
        • Lutgens M.W.
        • van Oijen M.G.
        • van der Heijden G.J.
        • Vleggaar F.P.
        • Siersema P.D.
        • Oldenburg B.
        Declining risk of colorectal cancer in inflammatory bowel disease: an updated meta-analysis of population-based cohort studies.
        Inflamm Bowel Dis. 2013; 19: 789-799
        • Ording A.G.
        • Horváth-Puhó E.
        • Erichsen R.
        • et al.
        Five-year mortality in colorectal cancer patients with ulcerative colitis or Crohn's disease: a nationwide population-based cohort study.
        Inflamm Bowel Dis. 2013; 19: 800-805
        • Jess T.
        • Simonsen J.
        • Jørgensen K.T.
        • Pedersen B.V.
        • Nielsen N.M.
        • Frisch M.
        Decreasing risk of colorectal cancer in patients with inflammatory bowel disease over 30 years.
        Gastroenterology. 2012; 143: 375-381
        • Lutgens M.
        • Vermeire S.
        • Van Oijen M.
        • et al.
        Dutch initiative on Crohn and colitis.
        Clin Gastroenterol Hepatol. 2015; 13: 148-154.e1
        • Parian A.
        • Lazarev M.
        Who and how to screen for cancer in at-risk inflammatory bowel disease patients.
        Expert Rev Gastroenterol Hepatol. 2015; 9: 731-746
        • Choi P.M.
        • Zelig M.P.
        Similarity of colorectal cancer in Crohn's disease and ulcerative colitis: implications for carcinogenesis and prevention.
        Gut. 1994; 35: 950-954
        • Zisman T.L.
        • Rubin D.T.
        Colorectal cancer and dysplasia in inflammatory bowel disease.
        World J Gastroenterol. 2008; 14: 2662-2669
        • 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: 205-211
        • Rutter M.D.
        • Saunders B.P.
        • Wilkinson K.H.
        • et al.
        Thirty-year analysis of a colonoscopic surveillance program for neoplasia in ulcerative colitis.
        Gastroenterology. 2006; 130: 1030-1038
        • Fireman Z.
        • Grossman A.
        • Lilos P.
        • et al.
        Intestinal cancer in patients with Crohn's disease. A population study in central Israel.
        Scand J Gastroenterol. 1989; 24: 346-350
        • Ekbom A.
        • Helmick C.
        • Zack M.
        • Adami H.O.
        Increased risk of large-bowel cancer in Crohn's disease with colonic involvement.
        Lancet. 1990; 336: 357-359
        • Freeman H.J.
        Colorectal cancer complicating Crohn's disease.
        Can J Gastroenterol. 2001; 15: 231-236
        • Ekbom A.
        • Helmick C.
        • Zack M.
        • Adami H.O.
        Ulcerative colitis and colorectal cancer. A population-based study.
        N Engl J Med. 1990; 323: 1228-1233
        • Söderlund S.
        • Brandt L.
        • Lapidus A.
        • et al.
        Decreasing time-trends of colorectal cancer in a large cohort of patients with inflammatory bowel disease.
        Gastroenterology. 2009; 136 (quiz 1818-1819): 1561-1567
        • Jess T.
        • Horváth-Puhó E.
        • Fallingborg J.
        • Rasmussen H.H.
        • Jacobsen B.A.
        Cancer risk in inflammatory bowel disease according to patient phenotype and treatment: a Danish population-based cohort study.
        Am J Gastroenterol. 2013; 108: 1869-1876
        • van Rijn A.F.
        • Fockens P.
        • Siersema P.D.
        • Oldenburg B.
        Adherence to surveillance guidelines for dysplasia and colorectal carcinoma in ulcerative and Crohn's colitis patients in The Netherlands.
        World J Gastroenterol. 2009; 15: 226-230
        • Greenstein A.J.
        • Sachar D.B.
        • Smith H.
        • et al.
        Cancer in universal and left-sided ulcerative colitis: factors determining risk.
        Gastroenterology. 1979; 77: 290-294
        • Weedon D.D.
        • Shorter R.G.
        • Ilstrup D.M.
        • Huizenga K.A.
        • Taylor W.F.
        Crohn's disease and cancer.
        N Engl J Med. 1973; 289: 1099-1103
        • Gillen C.D.
        • Walmsley R.S.
        • Prior P.
        • Andrews H.A.
        • Allan R.N.
        Ulcerative colitis and Crohn's disease: a comparison of the colorectal cancer risk in extensive colitis.
        Gut. 1994; 35: 1590-1592
        • Peyrin-Biroulet L.
        • Lepage C.
        • Jooste V.
        • Guéant J.L.
        • Faivre J.
        • Bouvier A.M.
        Colorectal cancer in inflammatory bowel diseases: a population-based study (1976-2008).
        Inflamm Bowel Dis. 2012; 18: 2247-2251
        • Soetikno R.M.
        • Lin O.S.
        • Heidenreich P.A.
        • Young H.S.
        • Blackstone M.O.
        Increased risk of colorectal neoplasia in patients with primary sclerosing cholangitis and ulcerative colitis: a meta-analysis.
        Gastrointest Endosc. 2002; 56: 48-54
        • Ngu J.H.
        • Gearry R.B.
        • Wright A.J.
        • Stedman C.A.
        Inflammatory bowel disease is associated with poor outcomes of patients with primary sclerosing cholangitis.
        Clin Gastroenterol Hepatol. 2011; 9 (quiz e135): 1092-1097
        • Broomé U.
        • Bergquist A.
        Primary sclerosing cholangitis, inflammatory bowel disease, and colon cancer.
        Semin Liver Dis. 2006; 26: 31-41
        • de Vries A.B.
        • Janse M.
        • Blokzijl H.
        • Weersma R.K.
        Distinctive inflammatory bowel disease phenotype in primary sclerosing cholangitis.
        World J Gastroenterol. 2015; 21: 1956-1971
        • Torres J.
        • Pineton de Chambrun G.
        • Itzkowitz S.
        • Sachar D.B.
        • Colombel J.F.
        Review article: colorectal neoplasia in patients with primary sclerosing cholangitis and inflammatory bowel disease.
        Aliment Pharmacol Ther. 2011; 34: 497-508
        • Lindström L.
        • Lapidus A.
        • Ost A.
        • Bergquist A.
        Increased risk of colorectal cancer and dysplasia in patients with Crohn's colitis and primary sclerosing cholangitis.
        Dis Colon Rectum. 2011; 54: 1392-1397
        • Braden B.
        • Halliday J.
        • Aryasingha S.
        • et al.
        Risk for colorectal neoplasia in patients with colonic Crohn's disease and concomitant primary sclerosing cholangitis.
        Clin Gastroenterol Hepatol. 2012; 10: 303-308
        • Loftus E.V.
        • Harewood G.C.
        • Loftus C.G.
        • et al.
        PSC-IBD: a unique form of inflammatory bowel disease associated with primary sclerosing cholangitis.
        Gut. 2005; 54: 91-96
        • Ullman T.A.
        • Itzkowitz S.H.
        Intestinal inflammation and cancer.
        Gastroenterology. 2011; 140: 1807-1816
        • Rutter M.
        • Saunders B.
        • Wilkinson K.
        • et al.
        Severity of inflammation is a risk factor for colorectal neoplasia in ulcerative colitis.
        Gastroenterology. 2004; 126: 451-459
        • Kim E.R.
        • Chang D.K.
        Colorectal cancer in inflammatory bowel disease: the risk, pathogenesis, prevention and diagnosis.
        World J Gastroenterol. 2014; 20: 9872-9881
        • Askling J.
        • Dickman P.W.
        • Karlén P.
        • et al.
        Colorectal cancer rates among first-degree relatives of patients with inflammatory bowel disease: a population-based cohort study.
        Lancet. 2001; 357: 262-266
        • Velayos F.S.
        • Loftus E.V.
        • Jess T.
        • et al.
        Predictive and protective factors associated with colorectal cancer in ulcerative colitis: a case-control study.
        Gastroenterology. 2006; 130: 1941-1949
        • Matkowskyj K.A.
        • Chen Z.E.
        • Rao M.S.
        • Yang G.Y.
        Dysplastic lesions in inflammatory bowel disease: molecular pathogenesis to morphology.
        Arch Pathol Lab Med. 2013; 137: 338-350
        • Xie J.
        • Itzkowitz S.H.
        Cancer in inflammatory bowel disease.
        World J Gastroenterol. 2008; 14: 378-389
        • Odze R.D.
        What are the guidelines for treating adenoma-like DALMs in UC?.
        Inflamm Bowel Dis. 2008; 14: S243-S244
        • Riddle R.H.
        • Goldman H.
        • Ransohoff D.F.
        • et al.
        Dysplasia in inflammatory bowel disease: standardized classification with provisional clinical applications.
        Hum Pathol. 1983; 14: 931-968
        • Farraye F.A.
        • Odze R.D.
        • Eaden J.
        • et al.
        AGA medical position statement on the diagnosis and management of colorectal neoplasia in inflammatory bowel disease.
        Gastroenterology. 2010; 138: 738-745
        • Kornbluth A.
        • Sachar D.B.
        Ulcerative colitis practice guidelines in adults: American College of Gastroenterology, Practice Parameters Committee.
        Am J Gastroenterol. 2010; 105 (quiz 524): 501-523
        • Annese V.
        • Daperno M.
        • Rutter M.D.
        • et al.
        European evidence based consensus for endoscopy in inflammatory bowel disease.
        J Crohns Colitis. 2013; 7: 982-1018
        • Mowat C.
        • Cole A.
        • Windsor A.
        • et al.
        Guidelines for the management of inflammatory bowel disease in adults.
        Gut. 2011; 60: 571-607
        • Desai D.
        • Desai N.
        Colorectal cancer surveillance in inflammatory bowel disease: a critical analysis.
        World J Gastrointest Endosc. 2014; 6: 541-548
        • Annese V.
        • Beaugerie L.
        • Egan L.
        • et al.
        European evidence-based consensus: inflammatory bowel disease and malignancies.
        J Crohns Colitis. 2015; 9: 945-965
        • Rubin C.E.
        • Haggitt R.C.
        • Burmer G.C.
        • et al.
        DNA aneuploidy in colonic biopsies predicts future development of dysplasia in ulcerative colitis.
        Gastroenterology. 1992; 103: 1611-1620
        • Bojarski C.
        Malignant transformation in inflammatory bowel disease: prevention, surveillance and treatment - new techniques in endoscopy.
        Dig Dis. 2009; 27: 571-575
        • Eaden J.A.
        • Ward B.A.
        • Mayberry J.F.
        How gastroenterologists screen for colonic cancer in ulcerative colitis: an analysis of performance.
        Gastrointest Endosc. 2000; 51: 123-128
        • Gearry R.B.
        • Wakeman C.J.
        • Barclay M.L.
        • et al.
        Surveillance for dysplasia in patients with inflammatory bowel disease: a national survey of colonoscopic practice in New Zealand.
        Dis Colon Rectum. 2004; 47: 314-322
        • Kaltz B.
        • Bokemeyer B.
        • Hoffmann J.
        • Porschen R.
        • Rogler G.
        • Schmiegel W.
        Surveillance colonoscopy in ulcerative colitis patients in Germany.
        Z Gastroenterol. 2007; 45 ([in German]): 325-331
        • Naymagon S.
        • Marion J.F.
        Surveillance in inflammatory bowel disease: chromoendoscopy and digital mucosal enhancement.
        Gastrointest Endosc Clin N Am. 2013; 23: 679-694
        • Repici A.
        • Laterra M.A.
        • Cisaro F.
        • Pellicano R.
        • Fini L.
        • Ishaq S.
        Unveiling cancer in IBD: screening colonoscopy or chromoendoscopy.
        Curr Drug Targets. 2012; 13: 1268-1272
        • Kiesslich R.
        • Fritsch J.
        • Holtmann M.
        • et al.
        Methylene blue-aided chromoendoscopy for the detection of intraepithelial neoplasia and colon cancer in ulcerative colitis.
        Gastroenterology. 2003; 124: 880-888
        • Rutter M.D.
        • Saunders B.P.
        • Schofield G.
        • Forbes A.
        • Price A.B.
        • Talbot I.C.
        Pancolonic indigo carmine dye spraying for the detection of dysplasia in ulcerative colitis.
        Gut. 2004; 53: 256-260
        • Hurlstone D.P.
        • Sanders D.S.
        • Lobo A.J.
        • McAlindon M.E.
        • Cross S.S.
        Indigo carmine-assisted high-magnification chromoscopic colonoscopy for the detection and characterisation of intraepithelial neoplasia in ulcerative colitis: a prospective evaluation.
        Endoscopy. 2005; 37: 1186-1192
        • Marion J.F.
        • Waye J.D.
        • Present D.H.
        • et al.
        Chromoendoscopy-targeted biopsies are superior to standard colonoscopic surveillance for detecting dysplasia in inflammatory bowel disease patients: a prospective endoscopic trial.
        Am J Gastroenterol. 2008; 103: 2342-2349
        • Wu L.
        • Li P.
        • Wu J.
        • Cao Y.
        • Gao F.
        The diagnostic accuracy of chromoendoscopy for dysplasia in ulcerative colitis: meta-analysis of six randomized controlled trials.
        Colorectal Dis. 2012; 14: 416-420
        • Subramanian V.
        • Mannath J.
        • Ragunath K.
        • Hawkey C.J.
        Meta-analysis: the diagnostic yield of chromoendoscopy for detecting dysplasia in patients with colonic inflammatory bowel disease.
        Aliment Pharmacol Ther. 2011; 33: 304-312
        • Dekker E.
        • van den Broek F.J.
        • Reitsma J.B.
        • et al.
        Narrow-band imaging compared with conventional colonoscopy for the detection of dysplasia in patients with longstanding ulcerative colitis.
        Endoscopy. 2007; 39: 216-221
        • van den Broek F.J.
        • Fockens P.
        • van Eeden S.
        • et al.
        Narrow-band imaging versus high-definition endoscopy for the diagnosis of neoplasia in ulcerative colitis.
        Endoscopy. 2011; 43: 108-115
        • Ignjatovic A.
        • East J.E.
        • Subramanian V.
        • et al.
        Narrow band imaging for detection of dysplasia in colitis: a randomized controlled trial.
        Am J Gastroenterol. 2012; 107: 885-890
        • Pellisé M.
        • López-Cerón M.
        • Rodríguez de Miguel C.
        • et al.
        Narrow-band imaging as an alternative to chromoendoscopy for the detection of dysplasia in longstanding inflammatory bowel disease: a prospective, randomized, crossover study.
        Gastrointest Endosc. 2011; 74: 840-848
        • Kiesslich R.
        • Burg J.
        • Vieth M.
        • et al.
        Confocal laser endoscopy for diagnosing intraepithelial neoplasias and colorectal cancer in vivo.
        Gastroenterology. 2004; 127: 706-713
        • Iacucci M.
        • Uraoka T.
        • Fort Gasia M.
        • Yahagi N.
        Novel diagnostic and therapeutic techniques for surveillance of dysplasia in patients with inflammatory bowel disease.
        Can J Gastroenterol Hepatol. 2014; 28: 361-370
        • Gabbani T.
        • Manetti N.
        • Bonanomi A.G.
        • Annese A.L.
        • Annese V.
        New endoscopic imaging techniques in surveillance of inflammatory bowel disease.
        World J Gastrointest Endosc. 2015; 7: 230-236
        • van den Broek F.J.
        • van Es J.A.
        • van Eeden S.
        • et al.
        Pilot study of probe-based confocal laser endomicroscopy during colonoscopic surveillance of patients with longstanding ulcerative colitis.
        Endoscopy. 2011; 43: 116-122
        • East J.E.
        Colonoscopic cancer surveillance in inflammatory bowel disease: what's new beyond random biopsy?.
        Clin Endosc. 2012; 45: 274-277
        • Guagnozzi D.
        • Lucendo A.J.
        Colorectal cancer surveillance in patients with inflammatory bowel disease: what is new?.
        World J Gastrointest Endosc. 2012; 4: 108-116
        • Hurlstone D.P.
        • Kiesslich R.
        • Thomson M.
        • Atkinson R.
        • Cross S.S.
        Confocal chromoscopic endomicroscopy is superior to chromoscopy alone for the detection and characterisation of intraepithelial neoplasia in chronic ulcerative colitis.
        Gut. 2008; 57: 196-204
        • Kiesslich R.
        • Goetz M.
        • Lammersdorf K.
        • et al.
        Chromoscopy-guided endomicroscopy increases the diagnostic yield of intraepithelial neoplasia in ulcerative colitis.
        Gastroenterology. 2007; 132: 874-882
        • Günther U.
        • Kusch D.
        • Heller F.
        • et al.
        Surveillance colonoscopy in patients with inflammatory bowel disease: comparison of random biopsy vs. targeted biopsy protocols.
        Int J Colorectal Dis. 2011; 26: 667-672
        • Rispo A.
        • Castiglione F.
        • Staibano S.
        • et al.
        Diagnostic accuracy of confocal laser endomicroscopy in diagnosing dysplasia in patients affected by long-standing ulcerative colitis.
        World J Gastrointest Endosc. 2012; 4: 414-420
        • Kiesslich R.
        • Neurath M.F.
        What new endoscopic imaging modalities will become important in the diagnosis of IBD?.
        Inflamm Bowel Dis. 2008; 14: S172-S176
        • Fusco V.
        • Ebert B.
        • Weber-Eibel J.
        • et al.
        Cancer prevention in ulcerative colitis: long-term outcome following fluorescence-guided colonoscopy.
        Inflamm Bowel Dis. 2012; 18: 489-495