Initiation of surveillance in IBD

From Cancer Guidelines Wiki


What is the appropriate time to commence surveillance in IBDInflammatory bowel disease patients (ulcerative colitis and Crohn’s patients, and effects of primary sclerosing cholangitis or family history of CRCColorectal cancer)? (SUR1)

Background

American Society for Gastrointestinal Endoscopy guidelines support the commencement of surveillance colonoscopy 8 years after the onset of inflammatory bowel disease (IBDInflammatory bowel disease) symptoms in those with at least left-sided ulcerative colitis (UCUlcerative colitis).[1] 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 (PSCPrimary sclerosing cholangitis), the risk of subclinical colitis and the incremental risk of colorectal cancer (CRCColorectal cancer) support commencement of surveillance immediately upon the diagnosis of PSCPrimary sclerosing cholangitis.[2] Patients with limited ileal Crohn’s disease or proctitis do not have increased risk of CRCColorectal cancer, compared with the general population, so participation in population-based surveillance is recommended.

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Systematic review evidence

A total of 34 studies reported clinical outcomes in IBDInflammatory bowel disease cohorts with varying clinical manifestations including UCUlcerative colitis, Crohn’s disease, or undefined colitis with and without PSCPrimary sclerosing cholangitis.[3][4][5][6][7][8][9][10][11][12][13][14][15][16][17][18][19][20][21][22][23][24][25][26][27][28][29][30][31][32][33][34][35][36] Reported outcomes included CRCColorectal cancer prevalence, dysplasia prevalence, all-cause mortality, colitis-associated neoplasia prevalence and CRCColorectal cancer risk factors.

Ten studies were level III-2 evidence,[6][7][10][13][14][15][22][25][27][36] and 24 studies were level III-3 evidence.[4][3][5][8][9][11][12][16][17][18][19][20][21][23][24][25][26][28][29][30][31][32][33][34][35]

Twenty nine studies were at high-risk of bias,[3][5][6][8][9][10][12][13][14][15][16][17][18][19][21][22][23][24][25][26][28][29][30][31][32][33][34][35][36] four studies were at moderate risk of bias,[7][11][20][27] and one study was at low risk of bias.[4]Back to top

ColorectalReferring to the large bowel, comprising the colon and rectum. cancer prevalence

A large number of studies reported CRCColorectal cancer rates in varying-sized cohorts of patients with UCUlcerative colitis, with follow-up in some studies as long as 40 years. Rates of CRCColorectal cancer were relatively low for the first decade after UCUlcerative colitis diagnosis, after which some studies reported significantly higher CRCColorectal cancer rates in patients with UCUlcerative colitis, compared with the general population.[6][9][10][23][36][8][11][14][15][16][17][30][31] Increasing duration of IBDInflammatory bowel disease after diagnosis was associated with an increasing risk of CRCColorectal cancer, the magnitude of which was higher in patients with Crohn’s disease, compared with those with UCUlcerative colitis. The increase in CRCColorectal cancer risk in these patients was substantial after 10 years post diagnosis.[4][20][28][30]

In these studies, UCUlcerative colitis was shown to be the greater risk factor for CRCColorectal cancer, however other studies have demonstrated PSCPrimary sclerosing cholangitis is also a significant contributing factor (see Risk factors for colorectal cancer in IBDInflammatory bowel disease patients: primary sclerosing cholangitis below).

Those with Crohn’s disease have a greater risk of CRCColorectal cancer 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.[6][10][25][30][8][13][14][16] There is some evidence to suggest that individuals with left-sided colitis, or pancolitis have a higher risk of CRCColorectal cancer. [28][32][23][30]Back to top

ColorectalReferring to the large bowel, comprising the colon and rectum. cancer mortality

Three studies[10][22][29] reported CRCColorectal cancer mortality rates in those with Crohn’s disease. Two studies[22][29] reported a trend towards higher mortality rates (2-fold higher) in those with Crohn’s disease, while only the larger study[10] reported a statistically significant difference.

Three studies reported CRCColorectal cancer mortality rates in those with UCUlcerative colitis, compared with the general population. One study reported a trend towards higher mortality rates (2-fold higher) in those with UCUlcerative colitis, while another study by Herrinton (2012) reported a statistically significant difference.[10][22][29]

Only single studies reported 5-year[33] and 10-year[9] CRCColorectal cancer survival rates in those with IBDInflammatory bowel disease. Five-year survival rates in a small cohort of UCUlcerative colitis patients were not different from those of sporadic CRCColorectal cancer cases. Ten-year survival rates were lower in those with higher-stage CRCColorectal cancer at diagnosis.

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Dysplasia prevalence

Two studies reported dysplasia prevalence in those with UCUlcerative colitis[28][32].

Nowacki (2015)[28] reported risk of dysplasia according to duration of disease in a cohort of 360 UCUlcerative colitis patients followed for more than 15 years. The risk of dysplasia was 5% within the first 8 years of UCUlcerative colitis, 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 ratio (OR) 4.3 (confidence interval [CI] 1.8–10.5, p=0.006).[28]

Stolwijk et al (2013)[32] reported cumulative risk of any dysplasia, or high-grade dysplasia (HGDHigh grade dysplasia) specifically at 10, 15 and 20 years of follow-up post diagnosis of UCUlcerative colitis. 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 HGDHigh grade dysplasia 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.[32]Back to top

Risk factors for colorectal cancer in IBDInflammatory bowel disease patients: family history

Several studies reported risk rates for CRCColorectal cancer in IBDInflammatory bowel disease populations with and without a family history of CRCColorectal cancer.[21][33][5][5][26]

A small (n=186) Belgian study, whose aim was to predict the risk of CRCColorectal cancer in IBDInflammatory bowel disease patients, reported that there was a nonsignificant difference in the presence of a positive family-history of CRCColorectal cancer among IBDInflammatory bowel disease patients with or without a CRCColorectal cancer diagnosis (5% versus 7%).[21]

Another study reported no significant difference (4.9% versus 7.8%) in the rate of positive family-history of CRCColorectal cancer between those diagnosed with both UCUlcerative colitis and CRCColorectal cancer (n=144), and 96,000 cases of sporadic CRCColorectal cancer (p=0.190).[33]

A Dutch study assessing CRCColorectal cancer risk in a cohort of patients with IBDInflammatory bowel disease[5] reported no significant increases in CRCColorectal cancer risk among those with a known family history of CRCColorectal cancer in a first-degree relative (relative risk [RRRelative risk] 1.90; CI 0.88–4.13) or in a second-degree relative (RRRelative risk 1.11; CI 0.40–3.03), compared with those with no family history of CRCColorectal cancer.

Interestingly, this study also reported that the risk of CRCColorectal cancer was significantly higher in IBDInflammatory bowel disease patients with an unknown family history of CRCColorectal cancer (n=199) compared with IBDInflammatory bowel disease patients with no known family history of CRCColorectal cancer (RRRelative risk 1.72; CI 1.27–2.35).[5]

A large cohort study reported the risk of advanced neoplasia (HGDHigh grade dysplasia or CRCColorectal cancer) in a population diagnosed with Crohn’s disease (n=408) or UCUlcerative colitis (n=573) in those with a first-degree relative diagnosed with CRCColorectal cancer, compared with those with no known family history. Family history was significantly associated with the development of advanced neoplasia in both univariate (hazard ratio [HR] 3.2; CI 1.4–7.6) and multivariate analysis (HR 3.9; CI 1.6–9.5).[26]Back to top

Risk factors for colorectal cancer in IBDInflammatory bowel disease patients: primary sclerosing cholangitis

There is further evidence to suggest that PSCPrimary sclerosing cholangitis significantly increases the risk of CRCColorectal cancer (greater than 5-fold increased risk), compared with IBDInflammatory bowel disease alone or with the general population.[7][18][27][19]

Boonstra (2013)[7] compared the risk of CRCColorectal cancer in IBDInflammatory bowel disease patients with PSCPrimary sclerosing cholangitis (n=402), and those with IBDInflammatory bowel disease only (n=772), and reported that PSCPrimary sclerosing cholangitis was associated with increased risk (4.7% versus 0.9%) with standardised incidence ratio (SIRStandardised incidence ratio) of 9.8 (CI 1.9–96.6) at a follow up of up to 15 years. Similarly, Lindstrom 2011[18] compared CRCColorectal cancer risk in Crohn’s disease patients with PSCPrimary sclerosing cholangitis (n=28) and without PSCPrimary sclerosing cholangitis (n=46), and reported that PSCPrimary sclerosing cholangitis was significantly associated with CRCColorectal cancer risk (11% versus 0%, p=0.05). This positive association was also reported for low-grade dysplasia (p=0.02) and advanced neoplasia (HGDHigh grade dysplasia or CRCColorectal cancer, p=0.016), but not HGDHigh grade dysplasia in the same cohort.[7]

In a very large Danish study, Jess 2012[12] reported a nine-fold increased CRCColorectal cancer risk comparing UCUlcerative colitis patients with and without PSCPrimary sclerosing cholangitis (RRRelative risk 9.13; CI 4.52–18.5). In contrast, there was no significant association between PSCPrimary sclerosing cholangitis and CRCColorectal cancer in patients with Crohn's disease (RRRelative risk 2.90; CI 0.40–20.9) or in individuals without IBDInflammatory bowel disease (RRRelative risk 1.05; CI 0.82–1.35).[12]

Baars et al (2011) [5] reported the risk of CRCColorectal cancer with respect to the duration of PSCPrimary sclerosing cholangitis (0–5 years, 5–10 years and >10 years) in an IBDInflammatory bowel disease cohort (n=566). A positive association was only seen after 5 years (RRRelative risk 5.03; CI 2.36–10.72), and maintained after 10 years (RRRelative risk 3.05; CI 1.25–7.43), but not for PSCPrimary sclerosing cholangitis of less than 5 years duration (RRRelative risk 2.35; CI 0.97–5.75).[5]

In this study, PSCPrimary sclerosing cholangitis was shown to be the greater risk factor for CRCColorectal cancer, however other studies have demonstrated UCUlcerative colitis is also a significant contributing factor (see ColorectalReferring to the large bowel, comprising the colon and rectum. cancer prevalence above).

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Risk factors for CRCColorectal cancer in IBDInflammatory bowel disease patients: ulcerative colitis or Crohn’s disease

In a longitudinal study spanning three decades, Jess et al (2012)[12] reported no significant difference in the risk of CRCColorectal cancer (RRRelative risk 1.07; CI 0.95–1.21) with nearly 8,000,000 participants (n=32,911 with UCUlcerative colitis).

In a comparison between patients with UCUlcerative colitis (n=288) and those with Crohn’s disease (n=265), Baars et al (2011)[5] reported CRCColorectal cancer risk was greater in those with UCUlcerative colitis (39.2% versus 21.9%, RRRelative risk 0.49; CI 0.36–0.68, p<0.001).[12] The same study reported no significant difference in the risk of CRCColorectal cancer in 14,463 patients with Crohn’s disease, compared with the general population of Denmark numbering nearly 8 million (RRRelative risk = 0.85; CI 0.67–1.07).[12]Back to top

Risk factors for CRCColorectal cancer in IBDInflammatory bowel disease patients: duration of IBDInflammatory bowel disease, degree of inflammation, or extent of IBDInflammatory bowel disease

Only two studies reported on the impact of duration of IBDInflammatory bowel disease on the risk of CRCColorectal cancer.[5][26]

Baars et al (2011)[5] reported the risk of CRCColorectal cancer in those with IBDInflammatory bowel disease of less than 10 years' duration, compared with those with IBDInflammatory bowel disease for 10–20 years, more than 20 years. The risk of CRCColorectal cancer was significantly greater in those with IBDInflammatory bowel disease for 10–20 years (RRRelative risk 2.26; CI 1.55–3.29) and >20 years (RRRelative risk 4.42; CI 3.07–6.36).[5]

Matsuoka et al (2013)[24] reported an increased risk of CRCColorectal cancer (OR=16.7; CI 5.95–46.88) in those with UCUlcerative colitis for 70 months or more.

Three studies reported CRCColorectal cancer risk according to degree of inflammation in patients with IBDInflammatory bowel disease[26][5][24]

In a cohort of IBDInflammatory bowel disease patients (n=1018), Mooiweer et al (2013)[26] 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)[5] assessed CRCColorectal cancer risk according to the degree of inflammation in a cohort of IBDInflammatory bowel disease patients (n=565). No significant difference in risk of CRCColorectal cancer 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 (RRRelative risk 2.80; CI 1.77–4.41) with 15.5 years follow-up.[5] The same study reported risk of CRCColorectal cancer in those with left-sided UCUlcerative colitis versus extensive UCUlcerative colitis, <50% segmental Crohn’s disease, or >50% segmental Crohn’s disease. The only positive risk association was found between left-sided UCUlcerative colitis and <50% segmental Crohn’s disease (RRRelative risk 0.43; CI 0.24–0.77, p<0.001) only after univariate analysis, with 15.5 years of follow-up.[5]

Matsuoka et al (2013)[24] reported that CRCColorectal cancer risk was associated only with active phase inflammation (RRRelative risk 0.04; CI 0.01–0.11), or mild colitis (RRRelative risk 5.80; CI 3.52–9.55) but not with pancolitis (RRRelative risk 0.72), at follow-up of 60 months.

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Risk factors for all-cause mortality

Only one study reported all-cause mortality risk, in 154 cases with CD or UCUlcerative colitis followed over 8 years, comparing those with an endoscopic procedure in the past 6–36 months and those without a recent colonoscopy[3]. Recent colonoscopy correlated with reduced mortality (OR 0.34; CI 0.12–0.95) on both univariate and multivariate analyses.[3]Back to top

Risk factors for dysplasia

Only a single study reported risk of dysplasia in a cohort of UCUlcerative colitis 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.[32]Back to top

Evidence summary and recommendations

Evidence summary Level References
A large number of studies reported CRCColorectal cancer rates in varying sized cohorts of patients with UCUlcerative colitis, with follow-up of up to 40 years in some studies. Rates of CRCColorectal cancer were relatively low for the first decade after UCUlcerative colitis diagnosis, after which some studies reported significantly higher CRCColorectal cancer rates in UCUlcerative colitis patients, compared with the general population.

There is consistent evidence to suggest that those with Crohn’s disease have a greater risk of CRCColorectal cancer 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 [6], [9], [10], [23], [36], [8], [11], [13], [14], [15], [16], [17], [30], [31], [34], [25]
Increasing duration of IBDInflammatory bowel disease after diagnosis is associated with an increasing risk of CRCColorectal cancer, the magnitude of which is higher among patients with Crohn’s disease than among those with UCUlcerative colitis. The increase in CRCColorectal cancer risk in these patients in substantial after 10 years post diagnosis. III-3 [4], [20], [28], [30], [5], [24]
There is consistent evidence to suggest that those with IBDInflammatory bowel disease and PSCPrimary sclerosing cholangitis are at significantly higher risk of CRCColorectal cancer (greater than 5-fold increased risk) from 10–20 years post PSCPrimary sclerosing cholangitis diagnosis. III-2, III-3 [7], [18], [27], [19], [12], [5]
There is some inconsistent evidence to suggest that a positive family history of CRCColorectal cancer increases the risk of CRCColorectal cancer in patients with IBDInflammatory bowel disease. III-3 [21], [33], [5], [26]
The 5-year survival rate following a diagnosis of CRCColorectal cancer in patients with IBDInflammatory bowel disease was 61–72%, but this might not be significantly different from that of controls. However, IBDInflammatory bowel disease CRCColorectal cancer mortality does not appear to have decreased. III-3 [4], [9], [33], [31]
Left-sided colitis, active inflammation, or mild colitis were all associated with significantly increased risk of CRCColorectal cancer. III-3 [5], [24]
The onset of CRCColorectal cancer within 8 years after a diagnosis of IBDInflammatory bowel disease is uncommon except in those with coexisting PSCPrimary sclerosing cholangitis or a personal family history of CRCColorectal cancer. III-1 [37], [38], [39], [40], [41]
Evidence-based recommendationA recommendation formulated after a systematic review of the evidence, indicating supporting references.Question mark transparent.png Grade
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
Evidence-based recommendationA recommendation formulated after a systematic review of the evidence, indicating supporting references.Question mark transparent.png Grade
In the presence of primary sclerosing cholangitis (PSCPrimary sclerosing cholangitis), surveillance colonoscopy should commence upon the diagnosis of PSCPrimary sclerosing cholangitis.
B
Practice pointA recommendation on a subject that is outside the scope of the search strategy for the systematic review, based on expert opinion and formulated by a consensus process.Question mark transparent.png

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.

Practice pointA recommendation on a subject that is outside the scope of the search strategy for the systematic review, based on expert opinion and formulated by a consensus process.Question mark transparent.png

Those with isolated proctitis or small bowel Crohn’s disease do not require surveillance colonoscopy.

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Unresolved issues

Whether the modern approach of treat to target therapy can further reduce colitis-associated dysplasia and CRCColorectal cancer is unknown. However, to date there has not been a demonstrable trend of reduction of colitis-associated CRCColorectal cancer mortality despite incremental improvement in IBDInflammatory bowel disease treatment and surveillance.

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References

  1. 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.
  2. 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.
  3. 3.03.13.23.33.4 Ananthakrishnan ANAdvanced neoplasia (advanced adenoma or colorectal cancer), 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.
  4. 4.04.14.24.34.44.5 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. ColorectalReferring to the large bowel, comprising the colon and rectum. Dis 2011 Nov;13(11):1230-5 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/21689324.
  5. 5.005.015.025.035.045.055.065.075.085.095.105.115.125.135.145.155.165.175.185.195.20 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.
  6. 6.06.16.26.36.46.5 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.
  7. 7.07.17.27.37.47.57.6 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.
  8. 8.08.18.28.38.48.5 Campos FG, Teixeira MG, Scanavini A, Almeida MG, Nahas SC, Cecconello I. Intestinal and extraintestinal neoplasia in patients with inflammatory bowel disease in a tertiary care hospital. Arq Gastroenterol 2013 Apr;50(2):123-9 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/23903622.
  9. 9.09.19.29.39.49.59.6 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.
  10. 10.010.110.210.310.410.510.610.710.8 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.
  11. 11.011.111.211.311.4 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.
  12. 12.012.112.212.312.412.512.612.712.8 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.
  13. 13.013.113.213.313.4 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.
  14. 14.014.114.214.314.414.5 Jussila A, Virta LJ, Pukkala E, Färkkilä MAMetachronous adenoma. 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.
  15. 15.015.115.215.315.4 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.
  16. 16.016.116.216.316.416.5 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.
  17. 17.017.117.217.317.4 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.
  18. 18.018.118.218.318.418.5 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 ColonThe main part of the large bowel, which absorbs water and electrolytes from undigested food (solid waste). Its four parts are the ascending colon, transverse colon, descending colon and sigmoid colon. RectumThe final section of the large bowel, ending at the anus. 2011 Nov;54(11):1392-7 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/21979184.
  19. 19.019.119.219.319.4 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.
  20. 20.020.120.220.320.4 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.
  21. 21.021.121.221.321.421.5 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.
  22. 22.022.122.222.322.422.5 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.
  23. 23.023.123.223.323.423.5 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.
  24. 24.024.124.224.324.424.524.624.7 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 ColorectalReferring to the large bowel, comprising the colon and rectum. Dis 2013 Jun;28(6):829-34 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/23080343.
  25. 25.025.125.225.325.425.5 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.
  26. 26.026.126.226.326.426.526.626.726.8 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.
  27. 27.027.127.227.327.4 Navaneethan U, Kochhar G, Venkatesh PG, Lewis B, Lashner BA, Remzi FH, et al. Duration and severity of primary sclerosing cholangitis is not associated with risk of neoplastic changes in the colon in patients with ulcerative colitis. Gastrointest Endosc 2012 May;75(5):1045-1054.e1 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/22405258.
  28. 28.028.128.228.328.428.528.628.728.8 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.
  29. 29.029.129.229.329.429.5 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.
  30. 30.030.130.230.330.430.530.630.730.8 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.
  31. 31.031.131.231.331.431.5 Senanayake SM, Fernandopulle ANAdvanced neoplasia (advanced adenoma or colorectal cancer), Niriella MAMetachronous adenoma, Wijesinghe NT, Ranaweera A, Mufeena MNMetachronous neoplasia, 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.
  32. 32.032.132.232.332.432.532.632.7 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.
  33. 33.033.133.233.333.433.533.633.7 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.
  34. 34.034.134.234.3 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.
  35. 35.035.135.2 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.
  36. 36.036.136.236.336.4 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.
  37. 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.
  38. Brentnall TA, Haggitt RC, Rabinovitch PS, Kimmey MB, Bronner MPMalignant polyp, 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.
  39. 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.
  40. 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.
  41. 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.

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Appendices

Jutta's magnifying glass icon.pngPICO question SUR1 View Evidence statement form SUR1Evidence statement form SUR1 View Systematic review report SUR1Systematic review report SUR1
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