- 1 Background
- 2 Systematic review evidence
- 2.1 Colorectal cancer prevalence
- 2.2 Colorectal cancer mortality
- 2.3 Dysplasia prevalence
- 2.4 Risk factors for colorectal cancer in IBD patients: family history
- 2.5 Risk factors for colorectal cancer in IBD patients: primary sclerosing cholangitis
- 2.6 Risk factors for CRC in IBD patients: ulcerative colitis or Crohn’s disease
- 2.7 Risk factors for CRC in IBD patients: duration of IBD, degree of inflammation, or extent of IBD
- 2.8 Risk factors for all-cause mortality
- 2.9 Risk factors for dysplasia
- 3 Evidence summary and recommendations
- 4 References
- 5 Appendices
What is the appropriate time to commence surveillance in IBD patients (ulcerative colitis and Crohn’s patients, and effects of primary sclerosing cholangitis or family history of CRC)? (SUR1)
American Society for Gastrointestinal Endoscopy guidelines support the commencement of surveillance colonoscopy 8 years after the onset of inflammatory bowel disease (IBD) symptoms in those with at least left-sided ulcerative colitis (UC). The same recommendation for the timing of commencement of surveillance is made for individuals with more extensive Crohn’s colitis, with prior involvement of at least one-third of the colon. However, in patients with primary sclerosing cholangitis (PSC), the risk of subclinical colitis and the incremental risk of colorectal cancer (CRC) support commencement of surveillance immediately upon the diagnosis of PSC. Patients with limited ileal Crohn’s disease or proctitis do not have increased risk of CRC, compared with the general population, so participation in population-based surveillance is recommended.
Systematic review evidence
A total of 34 studies reported clinical outcomes in IBD cohorts with varying clinical manifestations including UC, Crohn’s disease, or undefined colitis with and without PSC. Reported outcomes included CRC prevalence, dysplasia prevalence, all-cause mortality, colitis-associated neoplasia prevalence and CRC risk factors.
Ten studies were level III-2 evidence, and 24 studies were level III-3 evidence.
Twenty nine studies were at high-risk of bias, four studies were at moderate risk of bias, and one study was at low risk of bias.Back to top
Colorectal cancer prevalence
A large number of studies reported CRC rates in varying-sized cohorts of patients with UC, with follow-up in some studies as long as 40 years. Rates of CRC were relatively low for the first decade after UC diagnosis, after which some studies reported significantly higher CRC rates in patients with UC, compared with the general population. Increasing duration of IBD after diagnosis was associated with an increasing risk of CRC, the magnitude of which was higher in patients with Crohn’s disease, compared with those with UC. The increase in CRC risk in these patients was substantial after 10 years post diagnosis.
In these studies, UC was shown to be the greater risk factor for CRC, however other studies have demonstrated PSC is also a significant contributing factor (see Risk factors for colorectal cancer in IBD patients: primary sclerosing cholangitis below).
Those with Crohn’s disease have a greater risk of CRC than the general population from the same region. The magnitude of the increased risk varied between studies, but was consistently 1.5 to 2.0-fold greater than within 10 years of the diagnosis of Crohn’s disease. There is some evidence to suggest that individuals with left-sided colitis, or pancolitis have a higher risk of CRC. Back to top
Colorectal cancer mortality
Three studies reported CRC mortality rates in those with Crohn’s disease. Two studies reported a trend towards higher mortality rates (2-fold higher) in those with Crohn’s disease, while only the larger study reported a statistically significant difference.
Three studies reported CRC mortality rates in those with UC, compared with the general population. One study reported a trend towards higher mortality rates (2-fold higher) in those with UC, while another study by Herrinton (2012) reported a statistically significant difference.
Only single studies reported 5-year and 10-year CRC survival rates in those with IBD. Five-year survival rates in a small cohort of UC patients were not different from those of sporadic CRC cases. Ten-year survival rates were lower in those with higher-stage CRC at diagnosis.
Nowacki (2015) reported risk of dysplasia according to duration of disease in a cohort of 360 UC patients followed for more than 15 years. The risk of dysplasia was 5% within the first 8 years of UC, 7% after 9-15 years and 17% after 15 years' disease duration. The increase in dysplasia risk was significant only when comparing durations of 1–8 years and greater than 15 years: odds ratioA comparison of the odds (probability) of something happening in one group with the odds of it happening in another. (OR) 4.3 (confidence intervalA measure that quantifies the uncertainty in measurement. When reported as 95% CI, it is the range of values within which we can be 95% sure that the true value for the whole population lies. [CI] 1.8–10.5, p=0.006).
Stolwijk et al (2013) reported cumulative risk of any dysplasia, or high-grade dysplasia (HGD) specifically at 10, 15 and 20 years of follow-up post diagnosis of UC. The risk of any dysplasia was 23.5% at 10 years, 33.3% at 15 years and reached 48.3% at 20 years follow-up in a cohort of 293 patients. The cumulative risk of HGD was 6.6% at 10 years, 12.1% at 15 years and reached 19.0% at 20 years of follow-up in the same cohort.Back to top
Risk factors for colorectal cancer in IBD patients: family history
A small (n=186) Belgian study, whose aim was to predict the risk of CRC in IBD patients, reported that there was a nonsignificant difference in the presence of a positive family-history of CRC among IBD patients with or without a CRC diagnosis (5% versus 7%).
Another study reported no significant difference (4.9% versus 7.8%) in the rate of positive family-history of CRC between those diagnosed with both UC and CRC (n=144), and 96,000 cases of sporadic CRC (p=0.190).
A Dutch study assessing CRC risk in a cohort of patients with IBD reported no significant increases in CRC risk among those with a known family history of CRC in a first-degree relative (relative risk [RR] 1.90; CI 0.88–4.13) or in a second-degree relative (RR 1.11; CI 0.40–3.03), compared with those with no family history of CRC.
Interestingly, this study also reported that the risk of CRC was significantly higher in IBD patients with an unknown family history of CRC (n=199) compared with IBD patients with no known family history of CRC (RR 1.72; CI 1.27–2.35).
A large cohort study reported the risk of advanced neoplasia (HGD or CRC) in a population diagnosed with Crohn’s disease (n=408) or UC (n=573) in those with a first-degree relative diagnosed with CRC, compared with those with no known family history. Family history was significantly associated with the development of advanced neoplasia in both univariate (hazard ratioA measure of how often a particular event happens in one group compared to how often it happens in another group, over time. [HR] 3.2; CI 1.4–7.6) and multivariate analysis (HR 3.9; CI 1.6–9.5).Back to top
Risk factors for colorectal cancer in IBD patients: primary sclerosing cholangitis
Boonstra (2013) compared the risk of CRC in IBD patients with PSC (n=402), and those with IBD only (n=772), and reported that PSC was associated with increased risk (4.7% versus 0.9%) with standardised incidence ratio (SIR) of 9.8 (CI 1.9–96.6) at a follow up of up to 15 years. Similarly, Lindstrom 2011 compared CRC risk in Crohn’s disease patients with PSC (n=28) and without PSC (n=46), and reported that PSC was significantly associated with CRC risk (11% versus 0%, p=0.05). This positive association was also reported for low-grade dysplasia (p=0.02) and advanced neoplasia (HGD or CRC, p=0.016), but not HGD in the same cohort.
In a very large Danish study, Jess 2012 reported a nine-fold increased CRC risk comparing UC patients with and without PSC (RR 9.13; CI 4.52–18.5). In contrast, there was no significant association between PSC and CRC in patients with Crohn's disease (RR 2.90; CI 0.40–20.9) or in individuals without IBD (RR 1.05; CI 0.82–1.35).
Baars et al (2011)  reported the risk of CRC with respect to the duration of PSC (0–5 years, 5–10 years and >10 years) in an IBD cohort (n=566). A positive association was only seen after 5 years (RR 5.03; CI 2.36–10.72), and maintained after 10 years (RR 3.05; CI 1.25–7.43), but not for PSC of less than 5 years duration (RR 2.35; CI 0.97–5.75).
In this study, PSC was shown to be the greater risk factor for CRC, however other studies have demonstrated UC is also a significant contributing factor (see Colorectal cancer prevalence above).
Risk factors for CRC in IBD patients: ulcerative colitis or Crohn’s disease
In a longitudinal study spanning three decades, Jess et al (2012) reported no significant difference in the risk of CRC (RR 1.07; CI 0.95–1.21) with nearly 8,000,000 participants (n=32,911 with UC).
In a comparison between patients with UC (n=288) and those with Crohn’s disease (n=265), Baars et al (2011) reported CRC risk was greater in those with UC (39.2% versus 21.9%, RR 0.49; CI 0.36–0.68, p<0.001). The same study reported no significant difference in the risk of CRC in 14,463 patients with Crohn’s disease, compared with the general population of Denmark numbering nearly 8 million (RR = 0.85; CI 0.67–1.07).Back to top
Risk factors for CRC in IBD patients: duration of IBD, degree of inflammation, or extent of IBD
Baars et al (2011) reported the risk of CRC in those with IBD of less than 10 years' duration, compared with those with IBD for 10–20 years, more than 20 years. The risk of CRC was significantly greater in those with IBD for 10–20 years (RR 2.26; CI 1.55–3.29) and >20 years (RR 4.42; CI 3.07–6.36).
Matsuoka et al (2013) reported an increased risk of CRC (OR=16.7; CI 5.95–46.88) in those with UC for 70 months or more.
In a cohort of IBD patients (n=1018), Mooiweer et al (2013) reported no significant association between the risk of colitis-associated neoplasia and the degree of inflammation assessed both histologically and endoscopically, with a median follow-up of 2.6 years.
Baars et al (2011) assessed CRC risk according to the degree of inflammation in a cohort of IBD patients (n=565). No significant difference in risk of CRC was seen between those with mild, moderate, or severe inflammation. The only positive risk associated was found between unknown degree of inflammation and mild inflammation (RR 2.80; CI 1.77–4.41) with 15.5 years follow-up. The same study reported risk of CRC in those with left-sided UC versus extensive UC, <50% segmental Crohn’s disease, or >50% segmental Crohn’s disease. The only positive risk association was found between left-sided UC and <50% segmental Crohn’s disease (RR 0.43; CI 0.24–0.77, p<0.001) only after univariate analysis, with 15.5 years of follow-up.
Matsuoka et al (2013) reported that CRC risk was associated only with active phase inflammation (RR 0.04; CI 0.01–0.11), or mild colitis (RR 5.80; CI 3.52–9.55) but not with pancolitis (RR 0.72), at follow-up of 60 months.
Risk factors for all-cause mortality
Only one study reported all-cause mortality risk, in 154 cases with CD or UC followed over 8 years, comparing those with an endoscopic procedure in the past 6–36 months and those without a recent colonoscopy. Recent colonoscopy correlated with reduced mortality (OR 0.34; CI 0.12–0.95) on both univariate and multivariate analyses.Back to top
Risk factors for dysplasia
Only a single study reported risk of dysplasia in a cohort of UC patients (n=293). The presence of pancolitis was positively associated with a high risk of dysplasia, compared with distal colitis (HR 1.922; CI 1.12–3.31, p=0.019) after almost 11 years of follow-up, on both univariate and multivariate analysis.Back to top
Evidence summary and recommendations
| A large number of studies reported CRC rates in varying sized cohorts of patients with UC, with follow-up of up to 40 years in some studies. Rates of CRC were relatively low for the first decade after UC diagnosis, after which some studies reported significantly higher CRC rates in UC patients, compared with the general population.
There is consistent evidence to suggest that those with Crohn’s disease have a greater risk of CRC than the general population from the same region. The magnitude of the increased risk varied between studies, but was consistently 1.5 to 2.0-fold greater than within 10 years of a Crohn’s disease diagnosis.
|III-2, III-3||, , , , , , , , , , , , , , , |
|Increasing duration of IBD after diagnosis is associated with an increasing risk of CRC, the magnitude of which is higher among patients with Crohn’s disease than among those with UC. The increase in CRC risk in these patients in substantial after 10 years post diagnosis.||III-3||, , , , , |
|There is consistent evidence to suggest that those with IBD and PSC are at significantly higher risk of CRC (greater than 5-fold increased risk) from 10–20 years post PSC diagnosis.||III-2, III-3||, , , , , |
|There is some inconsistent evidence to suggest that a positive family history of CRC increases the risk of CRC in patients with IBD.||III-3||, , , |
|The 5-year survival rate following a diagnosis of CRC in patients with IBD was 61–72%, but this might not be significantly different from that of controls. However, IBD CRC mortality does not appear to have decreased.||III-3||, , , |
|Left-sided colitis, active inflammation, or mild colitis were all associated with significantly increased risk of CRC.||III-3||, |
|The onset of CRC within 8 years after a diagnosis of IBD is uncommon except in those with coexisting PSC or a personal family history of CRC.||III-1||, , , , |
|Surveillance colonoscopy should commence after 8 years of onset of inflammatory bowel disease symptoms in those with at least distal (left-sided) ulcerative colitis or Crohn’s colitis with involvement of at least one third of the colon.||C|
|In the presence of primary sclerosing cholangitis (PSC), surveillance colonoscopy should commence upon the diagnosis of PSC.||B|
A family history of colorectal cancer in a first degree relative represents an intermediate risk factor. Surveillance colonoscopy may begin after 8 years of the onset of symptoms of inflammatory bowel disease, or 10 years before the age of the youngest relative with colorectal cancer,whichever is earliest.
Those with isolated proctitis or small bowel Crohn’s disease do not require surveillance colonoscopy.
Whether the modern approach of treat to target therapy can further reduce colitis-associated dysplasia and CRC is unknown. However, to date there has not been a demonstrable trend of reduction of colitis-associated CRC mortality despite incremental improvement in IBD treatment and surveillance.
- Shergill AK, Lightdale JR, Bruining DH, Acosta RD, Chandrasekhara V, Chathadi KV, et al. The role of endoscopy in inflammatory bowel disease. Gastrointest Endosc 2015 May;81(5):1101-21.e1-13 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/25800660.
- Magro F, Gionchetti P, Eliakim R, Ardizzone S, Armuzzi A, Barreiro-de Acosta M, et al. 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 Crohns Colitis 2017 Jun 1;11(6):649-670 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/28158501.
- Ananthakrishnan AN, Cagan A, Cai T, Gainer VS, Shaw SY, Churchill S, et al. Colonoscopy is associated with a reduced risk for colon cancer and mortality in patients with inflammatory bowel diseases. Clin Gastroenterol Hepatol 2015 Feb;13(2):322-329.e1 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/25041865.
- Averboukh F, Ziv Y, Kariv Y, Zmora O, Dotan I, Klausner JM, et al. Colorectal carcinoma in inflammatory bowel disease: a comparison between Crohn's and ulcerative colitis. Colorectal Dis 2011 Nov;13(11):1230-5 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/21689324.
- Baars JE, Looman CW, Steyerberg EW, Beukers R, Tan AC, Weusten BL, et al. The risk of inflammatory bowel disease-related colorectal carcinoma is limited: results from a nationwide nested case-control study. Am J Gastroenterol 2011 Feb;106(2):319-28 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/21045815.
- Beaugerie L, Svrcek M, Seksik P, Bouvier AM, Simon T, Allez M, et al. Risk of colorectal high-grade dysplasia and cancer in a prospective observational cohort of patients with inflammatory bowel disease. Gastroenterology 2013 Jul;145(1):166-175.e8 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/23541909.
- Boonstra K, Weersma RK, van Erpecum KJ, Rauws EA, Spanier BW, Poen AC, et al. Population-based epidemiology, malignancy risk, and outcome of primary sclerosing cholangitis. Hepatology 2013 Dec;58(6):2045-55 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/23775876.
- Choi CH, Rutter MD, Askari A, Lee GH, Warusavitarne J, Moorghen M, et al. Forty-Year Analysis of Colonoscopic Surveillance Program for Neoplasia in Ulcerative Colitis: An Updated Overview. Am J Gastroenterol 2015 Jul;110(7):1022-34 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/25823771.
- Herrinton LJ, Liu L, Levin TR, Allison JE, Lewis JD, Velayos F. Incidence and mortality of colorectal adenocarcinoma in persons with inflammatory bowel disease from 1998 to 2010. Gastroenterology 2012 Aug;143(2):382-9 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/22609382.
- Hou JK, Kramer JR, Richardson P, Mei M, El-Serag HB. Risk of colorectal cancer among Caucasian and African American veterans with ulcerative colitis. Inflamm Bowel Dis 2012 Jun;18(6):1011-7 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/22334479.
- 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 Aug;143(2):375-81.e1; quiz e13-4 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/22522090.
- Jess T, Horváth-Puhó E, Fallingborg J, Rasmussen HH, Jacobsen BA. Cancer risk in inflammatory bowel disease according to patient phenotype and treatment: a Danish population-based cohort study. Am J Gastroenterol 2013 Dec;108(12):1869-76 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/23978954.
- Jussila A, Virta LJ, Pukkala E, Färkkilä MA. Malignancies in patients with inflammatory bowel disease: a nationwide register study in Finland. Scand J Gastroenterol 2013 Dec;48(12):1405-13 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/24131389.
- Kappelman MD, Farkas DK, Long MD, Erichsen R, Sandler RS, Sørensen HT, 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 Feb;12(2):265-73.e1 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/23602821.
- Katsanos KH, Tatsioni A, Pedersen N, Shuhaibar M, Ramirez VH, Politi P, et al. Cancer in inflammatory bowel disease 15 years after diagnosis in a population-based European Collaborative follow-up study. J Crohns Colitis 2011 Oct;5(5):430-42 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/21939917.
- Kekilli M, Dagli U, Kalkan IH, Tunc B, Disibeyaz S, Ulker A, et al. Low incidence of colorectal dysplasia and cancer among patients with ulcerative colitis: a Turkish referral centre study. Scand J Gastroenterol 2010 Apr;45(4):434-9 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/20085438.
- 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 Nov;54(11):1392-7 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/21979184.
- Liu K, Wang R, Kariyawasam V, Wells M, Strasser SI, McCaughan G, et al. Epidemiology and outcomes of primary sclerosing cholangitis with and without inflammatory bowel disease in an Australian cohort. Liver Int 2017 Mar;37(3):442-448 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/27891750.
- Lovasz BD, Lakatos L, Golovics PA, David G, Pandur T, Erdelyi Z, et al. Risk of colorectal cancer in Crohn's disease patients with colonic involvement and stenosing disease in a population-based cohort from Hungary. J Gastrointestin Liver Dis 2013 Sep;22(3):265-8 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/24078982.
- Lutgens M, Vermeire S, Van Oijen M, Vleggaar F, Siersema P, van Assche G, et al. A rule for determining risk of colorectal cancer in patients with inflammatory bowel disease. Clin Gastroenterol Hepatol 2015 Jan;13(1):148-54.e1 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/25041864.
- Manninen P, Karvonen AL, Huhtala H, Rasmussen M, Salo M, Mustaniemi L, et al. Mortality in ulcerative colitis and Crohn's disease. A population-based study in Finland. J Crohns Colitis 2012 Jun;6(5):524-8 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/22398058.
- Manninen P, Karvonen AL, Huhtala H, Aitola P, Hyöty M, Nieminen I, et al. The risk of colorectal cancer in patients with inflammatory bowel diseases in Finland: a follow-up of 20 years. J Crohns Colitis 2013 Dec;7(11):e551-7 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/23619008.
- Matsuoka H, Ikeuchi H, Uchino M, Bando T, Takesue Y, Nishigami T, et al. Clinicopathological features of ulcerative colitis-associated colorectal cancer pointing to efficiency of surveillance colonoscopy in a large retrospective Japanese cohort. Int J Colorectal Dis 2013 Jun;28(6):829-34 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/23080343.
- Mizushima T, Ohno Y, Nakajima K, Kai Y, Iijima H, Sekimoto M, et al. Malignancy in Crohn's disease: incidence and clinical characteristics in Japan. Digestion 2010;81(4):265-70 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/20134166.
- Mooiweer E, van der Meulen AE, van Bodegraven AA, Jansen JM, Mahmmod N, Nijsten J, et al. Neoplasia yield and colonoscopic workload of surveillance regimes for colorectal cancer in colitis patients: a retrospective study comparing the performance of the updated AGA and BSG guidelines. Inflamm Bowel Dis 2013 Nov;19(12):2603-10 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/24030524.
- Nowacki TM, Brückner M, Eveslage M, Tepasse P, Pott F, Thoennissen NH, et al. The risk of colorectal cancer in patients with ulcerative colitis. Dig Dis Sci 2015 Feb;60(2):492-501 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/25280558.
- Selinger CP, Andrews J, Dent OF, Norton I, Jones B, McDonald C, et al. Cause-specific mortality and 30-year relative survival of Crohn's disease and ulcerative colitis. Inflamm Bowel Dis 2013 Aug;19(9):1880-8 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/23765177.
- Selinger CP, Andrews JM, Titman A, Norton I, Jones DB, McDonald C, et al. Long-term follow-up reveals low incidence of colorectal cancer, but frequent need for resection, among Australian patients with inflammatory bowel disease. Clin Gastroenterol Hepatol 2014 Apr;12(4):644-50 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/23707778.
- Senanayake SM, Fernandopulle AN, Niriella MA, Wijesinghe NT, Ranaweera A, Mufeena MN, et al. The long-term outcomes of a cohort of Sri Lankan patients with ulcerative colitis: a retrospective study at two national referral centers and review of literature. Clin Exp Gastroenterol 2013;6:195-200 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/24068873.
- Stolwijk JA, Langers AM, Hardwick JC, Veenendaal RA, Verspaget HW, van Hogezand RA, et al. A thirty-year follow-up surveillance study for neoplasia of a dutch ulcerative colitis cohort. ScientificWorldJournal 2013;2013:274715 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/24379739.
- Watanabe T, Konishi T, Kishimoto J, Kotake K, Muto T, Sugihara K, et al. Ulcerative colitis-associated colorectal cancer shows a poorer survival than sporadic colorectal cancer: a nationwide Japanese study. Inflamm Bowel Dis 2011 Mar;17(3):802-8 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/20848547.
- Wei SC, Shieh MJ, Chang MC, Chang YT, Wang CY, Wong JM. Long-term follow-up of ulcerative colitis in Taiwan. J Chin Med Assoc 2012 Apr;75(4):151-5 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/22541142.
- Yoshino T, Nakase H, Takagi T, Bamba S, Okuyama Y, Kawamura T, et al. Risk factors for developing colorectal cancer in Japanese patients with ulcerative colitis: a retrospective observational study-CAPITAL (Cohort and Practice for IBD total management in Kyoto-Shiga Links) study I. BMJ Open Gastroenterol 2016 Nov 24;3(1):e000122 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/27933204.
- Zhang Q, Sha S, Xu B, Liang S, Wu K. Prevalence of colorectal cancer in patients with ulcerative colitis: A retrospective, monocenter study in China. J Cancer Res Ther 2015 Oct;11(4):899-903 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/26881538.
- Eaden JA, Abrams KR, Mayberry JF. The risk of colorectal cancer in ulcerative colitis: a meta-analysis. Gut 2001 Apr;48(4):526-35 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/11247898.
- Brentnall TA, Haggitt RC, Rabinovitch PS, Kimmey MB, Bronner MP, Levine DS, et al. Risk and natural history of colonic neoplasia in patients with primary sclerosing cholangitis and ulcerative colitis. Gastroenterology 1996 Feb;110(2):331-8 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/8566577.
- Askling J, Dickman PW, Karlén P, Broström O, Lapidus A, Löfberg R, et al. Family history as a risk factor for colorectal cancer in inflammatory bowel disease. Gastroenterology 2001 May;120(6):1356-62 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/11313305.
- Shetty K, Rybicki L, Brzezinski A, Carey WD, Lashner BA. The risk for cancer or dysplasia in ulcerative colitis patients with primary sclerosing cholangitis. Am J Gastroenterol 1999 Jun;94(6):1643-9 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/10364038.
- Lutgens MW, Vleggaar FP, Schipper ME, Stokkers PC, van der Woude CJ, Hommes DW, et al. High frequency of early colorectal cancer in inflammatory bowel disease. Gut 2008 Sep;57(9):1246-51 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/18337322.
|PICO question SUR1||Evidence statement form SUR1||Systematic review report SUR1|