TY - JOUR
AU - Lakatos, Peter, L
AB - Abstract Background Patients with Crohn’s disease [CD] and ulcerative colitis [UC] are at increased risk for colorectal dysplasia [CRD] and colorectal cancer [CRC]. Adherence to CRC surveillance guidelines is reportedly low internationally. Aim To evaluate surveillance practices at the tertiary IBD Center of the McGill University Health Center [MUHC] and to determine CRD/CRC incidence. Methods A representative inflammatory bowel disease cohort with at least 8 years of disease duration [or with primary sclerosing cholangitis] who visited the MUHC between July 1 and December 31, 2016 were included. Adherence to surveillance guidelines was compared to modified 2010 British Society of Gastroenterology guidelines. Incidence rates of CRC, high-grade dysplasia [HGD], low-grade dysplasia [LGD] and colorectal adenomas [CRA] were calculated based on pathology. Results In total, 1356 CD and UC patients (disease duration: 12 [interquartile range: 6–22) and 10 [interquartile range: 5–19] years) were identified. The surveillance cohort consisted of 680 patients [296 UC and 384 CD]. Adherence to surveillance guidelines was 76/82% in UC/colonic CD. An adequate number of biopsies were taken in 54/54% of UC/colonic CD patients. The incidence of CRC/HGD in UC and CD with colonic involvement was 19.5/58.5 and 25.1/37.6 per 100,000 patient-years, respectively. The incidence of dysplasia before 8 years of disease duration was low in both UC/CD [19.5 and 12.5/100,000 patient-years] with no CRC detected. The CRA rate was 30/38% in UC/colonic CD. Conclusion High adherence to surveillance guidelines and low CRC and dysplasia, but not CRA rates were found, suggesting that adhering to updated, stratified, surveillance recommendations may result in low advanced neoplasia rates. The incidence of dysplasia before the start of surveillance was low. Ulcerative colitis, Crohn’s disease, surveillance, colorectal cancer, dysplasia 1. Introduction The development of colorectal dysplasia [CRD] or colorectal cancer [CRC] is one of the most feared complications in patients with inflammatory bowel disease [IBD], for both ulcerative colitis [UC] and Crohn’s disease [CD].1–4 The overall risk is approximately 2-fold greater compared to the age-matched general population.1 Various risk factors for CRC in IBD have been reported.5 These include disease duration, younger age at disease onset [less than 30 years of age], extent of colonic involvement, long-standing inflammatory activity, severity of histological inflammation, presence of strictures and associated primary sclerosing cholangitis [PSC].6–10 Nevertheless, more recent population-based studies suggest a decreased risk of CRC in IBD patients,6,11 partly attributed to the effects of 5-aminosalicylates,12 immunosuppressive drugs13,14 and possibly to the early implementation of CRC surveillance programmes. There are several limitations to CRC surveillance in IBD. First, patients do not have the same CRC risk. CRD can arise in flat mucosa and thus not be readily visible by standard colonoscopy.15 Furthermore, in clinical practice the concept of dysplasia and its pathogenesis specifically in the IBD population is not fully understood.15,16 For these reasons, adherence to surveillance guidelines varies greatly by region and among endoscopists. Variability between regional guideline recommendations as to frequency of surveillance and protocols for random biopsy acquisition also contribute to variability in surveillance strategies. Guideline recommendations for CRC surveillance were published by The British Society of Gastroenterology [BSG], National Institute for Health and Clinical Excellence [NICE] and the European Crohn’s and Colitis Organization [ECCO].17,18 New recommendations suggest that surveillance for CRC in IBD patients is based on risk stratification at the screening colonoscopy or first surveillance 6–8 years after disease onset. Subsequent surveillance depends on the extent of disease, severity of histological and endoscopic inflammation, presence of strictures, pseudopolyps and family history of CRC.17 ECCO guidelines suggest performing colonoscopy every 2–3 years in intermediate-risk patients [extensive colitis with mild to moderate active inflammation, presence of post-inflammatory polyps, or CRC in an immediate family member over 50 years of age]. Low-risk patients without risk factors may have screening colonoscopies performed every 5 years.5 Chromoendoscopy or alternatively white light endoscopy with random biopsies [quadrant biopsies every 10 cm] with additional targeted biopsies from suspicious areas [ulcers, strictures] is recommended. According to an earlier model based on published data, 33 and 64 biopsies would be required to detect dysplasia with 90% and 95% probability, respectively.19 However, recent publications, for example from Japan,20 have confirmed that although more labour-intensive, random [and targeted] biopsies were not inferior in detecting CRD or CRC in IBD patients, suggesting that most dysplasia is visible in UC.21 Our aim here was to evaluate surveillance practices in a tertiary referral IBD centre at McGill University Health Center [MUHC] and to determine the incidence of CRC or CRD. A secondary aim was to identify CRC/CRD risk early during the disease course before the suggested onset of surveillance. 2. Methods A retrospective cohort of consecutive IBD patients who visited the MUHC IBD Center between July 1 and December 31, 2016 was created. Patients with at least 8 years of disease duration [or with concomitant PSC] were deemed eligible for surveillance and constituted the surveillance cohort. Patients with proctitis only were excluded. Among patients with CD, only patients with colonic and ileocolonic [L2 or L3 by the Montreal Classification of CD22] were included given their inherent increased risk for CRC. The following data were captured: demographic variables, IBD-related surgery, medication history, and endoscopy and histopathology. Disease extent was classified using the Montreal Classification for CD and UC. Dates and the number of colonoscopies and chromoendoscopies as well as the number of biopsies per endoscopic surveillance procedure were recorded for each patient, including those performed specifically for surveillance. All surveillance endoscopies were performed using white light Olympus endoscopes. After 2013, high-definition Olympus 190 series, Exera III CV-190 endoscopes were used. The incidence of CRC, high-grade dysplasia [HGD], low-grade dysplasia [LGD] and colorectal adenomas [CRA] were calculated based on pathology reports. Adherence to surveillance guidelines was compared to a modified BSG guideline definition.23 Incidence rates during surveillance and before surveillance were calculated for CRC, HGD, LGD and CRA. Statistical analyses were performed using Statistical Package for the Social Sciences [SPSS 18.0; SPSS Inc.]. All continuous data were expressed as mean ± SD or as a median with interquartile range [IQR]. For univariate analyses, we used a t-test and Wilcoxon rank-sum test for continuous variables and a χ2 test for the proportion of discrete variables. Baseline parameters were examined using regression analysis. Incidence rates were calculated for CRD, CRC and CRA. A p value of <0.05 was regarded as statistically significant. 2.1. Ethical considerations The study protocol was approved by the MUHC Research Ethics Board. 3. Results A total of 1356 patients were identified with CD and UC and at least one documented outpatient visit to the MUHC IBD Center between July 1 and December 31, 2016 [Figure 1]. Median disease duration for the total cohort was 12 years [IQR: 6–22] and 10 years [IQR: 5–19] for CD and UC, respectively. Figure 1. Open in new tabDownload slide Patient identification for the surveillance cohort. Figure 1. Open in new tabDownload slide Patient identification for the surveillance cohort. Of the 1356 IBD cases identified, 680 [384 with L2/L3 CD and 296 with UC, including patients with concomitant PSC] made up the surveillance cohort with a disease duration of >8 years or coexisting PSC. The remaining 676 patients were found to have either L1 [ileal]/L4 [upper gastrointestinal] CD or an insufficient duration of disease [<8 years in the absence of PSC]. The patient characteristics of the surveillance cohort are displayed in Table 1. Table 1. Patient demographic and phenotypic characteristics for IBD patients in the surveillance cohort. Total IBD cohort [n = 1356] IBD patients in the surveillance cohort [n = 680] CD [total n = 873] CD – L2 and L3 surveillance cohort [n = 384] UC [total n = 483] UC surveillance cohort [n = 296] PSC-IBD [n = 28] [CD/UC 15/13] Sex (male/female [%]) 48/52 46/54 46/54 42/58 17/11 Age at onset (years, mean [SD]) 27.7 [13.8] 26.4 [12.6] 33.5 [14] 32 [13.2] 32.8 [14.9] Age at referral to IBD centre (years, mean [SD]) 36.5 [15.3] 37.5 [14.9] 40.3 [15.4] 41.9 [14.7] 42.5 [14.7] Age at index (years, mean [SD]) 43.2 [16] 46.5 [14.8] 46.9 [16.0] 50.6 [14.7] 49.7 [15.1] Montreal Classification for CD patients Localization in CD [L1/L2/L3/L4] [%] 30/20/50/5/5 38/62 – – 20/47/33/0 Disease behaviour in CD [B1/B2/B3] [%] 53/27/20 57/23/20 – – 67/20/13 Perianal disease in CD [%] 25 35 – – 27 Montreal Classification for UC patients Extent of disease [E1/E2/E3] [%] 16/37/46 0/52/48 0/8/92 Severity [S1/S2/S3] [%] 59/27/14 58/28/14 39/23/38 Patients who underwent surgical resection[s] [%] 54 58 40% Patients who underwent colectomy [%] 9 109.6 – – Patients with concomitant primary sclerosing cholangitis [%] 2 2 3 4 – Total IBD cohort [n = 1356] IBD patients in the surveillance cohort [n = 680] CD [total n = 873] CD – L2 and L3 surveillance cohort [n = 384] UC [total n = 483] UC surveillance cohort [n = 296] PSC-IBD [n = 28] [CD/UC 15/13] Sex (male/female [%]) 48/52 46/54 46/54 42/58 17/11 Age at onset (years, mean [SD]) 27.7 [13.8] 26.4 [12.6] 33.5 [14] 32 [13.2] 32.8 [14.9] Age at referral to IBD centre (years, mean [SD]) 36.5 [15.3] 37.5 [14.9] 40.3 [15.4] 41.9 [14.7] 42.5 [14.7] Age at index (years, mean [SD]) 43.2 [16] 46.5 [14.8] 46.9 [16.0] 50.6 [14.7] 49.7 [15.1] Montreal Classification for CD patients Localization in CD [L1/L2/L3/L4] [%] 30/20/50/5/5 38/62 – – 20/47/33/0 Disease behaviour in CD [B1/B2/B3] [%] 53/27/20 57/23/20 – – 67/20/13 Perianal disease in CD [%] 25 35 – – 27 Montreal Classification for UC patients Extent of disease [E1/E2/E3] [%] 16/37/46 0/52/48 0/8/92 Severity [S1/S2/S3] [%] 59/27/14 58/28/14 39/23/38 Patients who underwent surgical resection[s] [%] 54 58 40% Patients who underwent colectomy [%] 9 109.6 – – Patients with concomitant primary sclerosing cholangitis [%] 2 2 3 4 – Abbreviations: IBD, inflammatory bowel disease; UC, ulcerative colitis; CD, Crohn’s disease; PSC, primary sclerosing cholangitis. Open in new tab Table 1. Patient demographic and phenotypic characteristics for IBD patients in the surveillance cohort. Total IBD cohort [n = 1356] IBD patients in the surveillance cohort [n = 680] CD [total n = 873] CD – L2 and L3 surveillance cohort [n = 384] UC [total n = 483] UC surveillance cohort [n = 296] PSC-IBD [n = 28] [CD/UC 15/13] Sex (male/female [%]) 48/52 46/54 46/54 42/58 17/11 Age at onset (years, mean [SD]) 27.7 [13.8] 26.4 [12.6] 33.5 [14] 32 [13.2] 32.8 [14.9] Age at referral to IBD centre (years, mean [SD]) 36.5 [15.3] 37.5 [14.9] 40.3 [15.4] 41.9 [14.7] 42.5 [14.7] Age at index (years, mean [SD]) 43.2 [16] 46.5 [14.8] 46.9 [16.0] 50.6 [14.7] 49.7 [15.1] Montreal Classification for CD patients Localization in CD [L1/L2/L3/L4] [%] 30/20/50/5/5 38/62 – – 20/47/33/0 Disease behaviour in CD [B1/B2/B3] [%] 53/27/20 57/23/20 – – 67/20/13 Perianal disease in CD [%] 25 35 – – 27 Montreal Classification for UC patients Extent of disease [E1/E2/E3] [%] 16/37/46 0/52/48 0/8/92 Severity [S1/S2/S3] [%] 59/27/14 58/28/14 39/23/38 Patients who underwent surgical resection[s] [%] 54 58 40% Patients who underwent colectomy [%] 9 109.6 – – Patients with concomitant primary sclerosing cholangitis [%] 2 2 3 4 – Total IBD cohort [n = 1356] IBD patients in the surveillance cohort [n = 680] CD [total n = 873] CD – L2 and L3 surveillance cohort [n = 384] UC [total n = 483] UC surveillance cohort [n = 296] PSC-IBD [n = 28] [CD/UC 15/13] Sex (male/female [%]) 48/52 46/54 46/54 42/58 17/11 Age at onset (years, mean [SD]) 27.7 [13.8] 26.4 [12.6] 33.5 [14] 32 [13.2] 32.8 [14.9] Age at referral to IBD centre (years, mean [SD]) 36.5 [15.3] 37.5 [14.9] 40.3 [15.4] 41.9 [14.7] 42.5 [14.7] Age at index (years, mean [SD]) 43.2 [16] 46.5 [14.8] 46.9 [16.0] 50.6 [14.7] 49.7 [15.1] Montreal Classification for CD patients Localization in CD [L1/L2/L3/L4] [%] 30/20/50/5/5 38/62 – – 20/47/33/0 Disease behaviour in CD [B1/B2/B3] [%] 53/27/20 57/23/20 – – 67/20/13 Perianal disease in CD [%] 25 35 – – 27 Montreal Classification for UC patients Extent of disease [E1/E2/E3] [%] 16/37/46 0/52/48 0/8/92 Severity [S1/S2/S3] [%] 59/27/14 58/28/14 39/23/38 Patients who underwent surgical resection[s] [%] 54 58 40% Patients who underwent colectomy [%] 9 109.6 – – Patients with concomitant primary sclerosing cholangitis [%] 2 2 3 4 – Abbreviations: IBD, inflammatory bowel disease; UC, ulcerative colitis; CD, Crohn’s disease; PSC, primary sclerosing cholangitis. Open in new tab In the CD group there were 107 patients [38%] with L2 [colonic] disease and 277 patients [62%] with L3 [ileocolonic] disease. The majority of patients in the CD group had B1 [non-stricturing and non-penetrating] [567%] disease. In total, 2% of the CD surveillance cohort had co-existing PSC. Over half of the CD group [58%] had prior resection surgery. In the UC surveillance group, the majority of patients [48%] had extensive [E3] disease extending proximal to the splenic flexure. Patients with co-morbid PSC accounted for 4% of the UC surveillance population. The maximal therapeutic strategy used for CD and UC in the surveillance cohort is illustrated in Figure 2. As expected based on the varying response to pharmacological interventions between CD and UC, the majority of CD patients [51%] were treated with anti-tumour necrosis factor [anti-TNF] agents, whereas UC patients were managed with 5-aminosalicylic acid [26%], corticosteroid [27%] and anti-TNF agents [27%]. Figure 2. Open in new tabDownload slide Maximal therapeutic strategies employed in CD and UC patients in the surveillance cohort. *In total, 23% in CD and 43% in UC were exposed to 5-aminosalicylic acid Figure 2. Open in new tabDownload slide Maximal therapeutic strategies employed in CD and UC patients in the surveillance cohort. *In total, 23% in CD and 43% in UC were exposed to 5-aminosalicylic acid 3.1. Accuracy of endoscopic surveillance After a period of 8 years of disease or concomitant PSC, 92% of the patients in the cohort had at least one colonoscopy and 77% had at least one dedicated surveillance colonoscopy. Chromoendoscopy was performed in only 2% of UC patients and none of the patients with CD or PSC. Adherence to CRC/CRD surveillance was 76% in UC and 66% in CD, with 82% adherence specifically in L2 [colonic] CD, as demonstrated in Figure 3. Adherence to appropriate surveillance in patients with PSC and either CD or UC was only 33%. Figure 3. Open in new tabDownload slide Frequency of adequate endoscopic surveillance after 8 years of disease duration. Figure 3. Open in new tabDownload slide Frequency of adequate endoscopic surveillance after 8 years of disease duration. 3.1.1. Interval between surveillance colonoscopies The median interval between surveillance colonoscopies in this cohort is displayed in Table 2. Table 2. Median interval and IQR between surveillance colonoscopies IBD subtype Median follow-up time [years] [IQR] L2 CD 2.26 [IQR: 1–4.5] L2–3 CD 3.4 [IQR: 1.25–7] UC 3 [IQR: 1.5–5] E3 UC 2.25 [IQR: 1.48–4.5] PSC [and either CD or UC] 2.5 [IQR: 2–6.3] IBD subtype Median follow-up time [years] [IQR] L2 CD 2.26 [IQR: 1–4.5] L2–3 CD 3.4 [IQR: 1.25–7] UC 3 [IQR: 1.5–5] E3 UC 2.25 [IQR: 1.48–4.5] PSC [and either CD or UC] 2.5 [IQR: 2–6.3] Abbreviations: IBD, inflammatory bowel disease; UC, ulcerative colitis; CD, Crohn’s disease; PSC, primary sclerosing cholangitis; IQR, interquartile range. Open in new tab Table 2. Median interval and IQR between surveillance colonoscopies IBD subtype Median follow-up time [years] [IQR] L2 CD 2.26 [IQR: 1–4.5] L2–3 CD 3.4 [IQR: 1.25–7] UC 3 [IQR: 1.5–5] E3 UC 2.25 [IQR: 1.48–4.5] PSC [and either CD or UC] 2.5 [IQR: 2–6.3] IBD subtype Median follow-up time [years] [IQR] L2 CD 2.26 [IQR: 1–4.5] L2–3 CD 3.4 [IQR: 1.25–7] UC 3 [IQR: 1.5–5] E3 UC 2.25 [IQR: 1.48–4.5] PSC [and either CD or UC] 2.5 [IQR: 2–6.3] Abbreviations: IBD, inflammatory bowel disease; UC, ulcerative colitis; CD, Crohn’s disease; PSC, primary sclerosing cholangitis; IQR, interquartile range. Open in new tab 3.1.2. Accuracy of surveillance based on biopsy numbers during surveillance colonoscopies Adherence to the recommended number of biopsies per surveillance colonoscopy, as defined by four-quadrant biopsies every 10 cm of colon or >30 biopsies, and the average number of biopsies per surveillance colonoscopy stratified by disease and phenotype are shown in Table 3. Table 3. Mean number of random biopsies taken per surveillance colonoscopy. Number of biopsies per endoscopy CD L2–L3 [n = 384] CD L2 [n = 107] CD L3 [n = 277] UC [n = 296] <20 biopsies/endoscopy 70% 43.0% 80% 45% 20–30 biopsies/endoscopy 2% 3% 2% 2% >30 biopsies/endoscopy* 29% 54% 19% 54% Number of biopsies per endoscopy CD L2–L3 [n = 384] CD L2 [n = 107] CD L3 [n = 277] UC [n = 296] <20 biopsies/endoscopy 70% 43.0% 80% 45% 20–30 biopsies/endoscopy 2% 3% 2% 2% >30 biopsies/endoscopy* 29% 54% 19% 54% Abbreviations: UC, ulcerative colitis; CD, Crohn’s disease. *More than 30 biopsies/endoscopy or four-quadrant biopsies every 10 cm of colon. Open in new tab Table 3. Mean number of random biopsies taken per surveillance colonoscopy. Number of biopsies per endoscopy CD L2–L3 [n = 384] CD L2 [n = 107] CD L3 [n = 277] UC [n = 296] <20 biopsies/endoscopy 70% 43.0% 80% 45% 20–30 biopsies/endoscopy 2% 3% 2% 2% >30 biopsies/endoscopy* 29% 54% 19% 54% Number of biopsies per endoscopy CD L2–L3 [n = 384] CD L2 [n = 107] CD L3 [n = 277] UC [n = 296] <20 biopsies/endoscopy 70% 43.0% 80% 45% 20–30 biopsies/endoscopy 2% 3% 2% 2% >30 biopsies/endoscopy* 29% 54% 19% 54% Abbreviations: UC, ulcerative colitis; CD, Crohn’s disease. *More than 30 biopsies/endoscopy or four-quadrant biopsies every 10 cm of colon. Open in new tab 3.1.3. Incidence of dysplasia, CRC and CRA during the surveillance period and in the pre-surveillance period Dysplasia was detected on surveillance colonoscopies in 12 [3%] CD patients with L2/L3 disease. In the UC group, dysplasia was detected in 19 [7%] patients and in the PSC group four [10%] were found to have dysplasia on surveillance endoscopy. A total of three patients were diagnosed with CRC by surveillance colonoscopy. Most cases of dysplasia were LGD. Few cases of dysplasia and no CRC was detected prior to 8 years of disease duration in any of the CD, UC or PSC patients. CRA frequency was high on surveillance colonoscopy for all groups. Table 4 summarizes the types of dysplasia detected by disease type and severity. Table 4. Prevalence of dysplasia in the surveillance cohort Type of dysplasia CD L2–L3, n [%] CD L2, n [%] UC, n [%] PSC, n [%] CRC 2 [1%] 0 [0%] 1 [0.3%] 0 [0%] HGD 3 [1%] 0 [0%] 3 [1%] 0 [0%] LGD 10 [3%] 3 [3%] 18 [6%] 3 [11%] Any dysplasia 12 [3%] 3 [3%] 19 [7%] 4 [14%] Any colorectal adenoma 98 [26%] 40 [38%] 89 [30%] 11 [39%] Dysplasia prior to 8 years 1 [0.3%] 0 [0%] 1 [0.3%] 0 [0%] Type of dysplasia CD L2–L3, n [%] CD L2, n [%] UC, n [%] PSC, n [%] CRC 2 [1%] 0 [0%] 1 [0.3%] 0 [0%] HGD 3 [1%] 0 [0%] 3 [1%] 0 [0%] LGD 10 [3%] 3 [3%] 18 [6%] 3 [11%] Any dysplasia 12 [3%] 3 [3%] 19 [7%] 4 [14%] Any colorectal adenoma 98 [26%] 40 [38%] 89 [30%] 11 [39%] Dysplasia prior to 8 years 1 [0.3%] 0 [0%] 1 [0.3%] 0 [0%] Abbreviations: UC, ulcerative colitis; CD, Crohn’s disease; PSC, primary sclerosing cholangitis; CRC, colorectal cancer; HGD, high-grade dysplasia; LGD, low-grade dysplasia. Open in new tab Table 4. Prevalence of dysplasia in the surveillance cohort Type of dysplasia CD L2–L3, n [%] CD L2, n [%] UC, n [%] PSC, n [%] CRC 2 [1%] 0 [0%] 1 [0.3%] 0 [0%] HGD 3 [1%] 0 [0%] 3 [1%] 0 [0%] LGD 10 [3%] 3 [3%] 18 [6%] 3 [11%] Any dysplasia 12 [3%] 3 [3%] 19 [7%] 4 [14%] Any colorectal adenoma 98 [26%] 40 [38%] 89 [30%] 11 [39%] Dysplasia prior to 8 years 1 [0.3%] 0 [0%] 1 [0.3%] 0 [0%] Type of dysplasia CD L2–L3, n [%] CD L2, n [%] UC, n [%] PSC, n [%] CRC 2 [1%] 0 [0%] 1 [0.3%] 0 [0%] HGD 3 [1%] 0 [0%] 3 [1%] 0 [0%] LGD 10 [3%] 3 [3%] 18 [6%] 3 [11%] Any dysplasia 12 [3%] 3 [3%] 19 [7%] 4 [14%] Any colorectal adenoma 98 [26%] 40 [38%] 89 [30%] 11 [39%] Dysplasia prior to 8 years 1 [0.3%] 0 [0%] 1 [0.3%] 0 [0%] Abbreviations: UC, ulcerative colitis; CD, Crohn’s disease; PSC, primary sclerosing cholangitis; CRC, colorectal cancer; HGD, high-grade dysplasia; LGD, low-grade dysplasia. Open in new tab The total follow-up was 17,528 patient-years, and the total and median follow-up times in UC, CD and PSC are displayed in Table 5. Table 5. Patient follow-up details Total follow-up [patient-years] Median follow-up [patient-years] [IQR] IBD surveillance cohort 17,528 CD L2–L3 7966 17 [10–26] CD L2 1823 16 [11–23] UC 5126 17 [11–25] PSC 427 14 [7–26] Total follow-up [patient-years] Median follow-up [patient-years] [IQR] IBD surveillance cohort 17,528 CD L2–L3 7966 17 [10–26] CD L2 1823 16 [11–23] UC 5126 17 [11–25] PSC 427 14 [7–26] Abbreviations: IBD, inflammatory bowel disease; UC, ulcerative colitis; CD, Crohn’s disease; PSC, primary sclerosing cholangitis; IQR, interquartile range. Open in new tab Table 5. Patient follow-up details Total follow-up [patient-years] Median follow-up [patient-years] [IQR] IBD surveillance cohort 17,528 CD L2–L3 7966 17 [10–26] CD L2 1823 16 [11–23] UC 5126 17 [11–25] PSC 427 14 [7–26] Total follow-up [patient-years] Median follow-up [patient-years] [IQR] IBD surveillance cohort 17,528 CD L2–L3 7966 17 [10–26] CD L2 1823 16 [11–23] UC 5126 17 [11–25] PSC 427 14 [7–26] Abbreviations: IBD, inflammatory bowel disease; UC, ulcerative colitis; CD, Crohn’s disease; PSC, primary sclerosing cholangitis; IQR, interquartile range. Open in new tab The incidence rates of CRC and HGD in CD, UC, and PSC are presented in Table 6. None of the patients with PSC and coexisting IBD in our cohort developed CRC during the follow-up period. Of note, dysplasia rates before the suggested start of surveillance were low in both CD and UC [12.5 and 19.5/100,000 patient-years] with none of those patients developing CRC. Table 6. Incidence of dysplasia in the surveillance cohort Type of dysplasia CD L2–L3 [n/100,000 patient-years] UC [n/100,000 patient-years] PSC [n/100,000 patient- years] CRC 25.1 19.5 0 HGD 37.6 58.5 0 LGD 125.5 351.1 702.5 Any dysplasia 150.6 370.6 936.7 Tubular adenoma 1230 1736.2 2576.1 Dysplasia prior to 8 years 12.5 19.5 0 CRC prior to 8 years 0 0 0 Type of dysplasia CD L2–L3 [n/100,000 patient-years] UC [n/100,000 patient-years] PSC [n/100,000 patient- years] CRC 25.1 19.5 0 HGD 37.6 58.5 0 LGD 125.5 351.1 702.5 Any dysplasia 150.6 370.6 936.7 Tubular adenoma 1230 1736.2 2576.1 Dysplasia prior to 8 years 12.5 19.5 0 CRC prior to 8 years 0 0 0 Abbreviations: UC, ulcerative colitis; CD, Crohn’s disease; PSC, primary sclerosing cholangitis; CRC, colorectal cancer; HGD, high-grade dysplasia; LGD, low-grade dysplasia. Open in new tab Table 6. Incidence of dysplasia in the surveillance cohort Type of dysplasia CD L2–L3 [n/100,000 patient-years] UC [n/100,000 patient-years] PSC [n/100,000 patient- years] CRC 25.1 19.5 0 HGD 37.6 58.5 0 LGD 125.5 351.1 702.5 Any dysplasia 150.6 370.6 936.7 Tubular adenoma 1230 1736.2 2576.1 Dysplasia prior to 8 years 12.5 19.5 0 CRC prior to 8 years 0 0 0 Type of dysplasia CD L2–L3 [n/100,000 patient-years] UC [n/100,000 patient-years] PSC [n/100,000 patient- years] CRC 25.1 19.5 0 HGD 37.6 58.5 0 LGD 125.5 351.1 702.5 Any dysplasia 150.6 370.6 936.7 Tubular adenoma 1230 1736.2 2576.1 Dysplasia prior to 8 years 12.5 19.5 0 CRC prior to 8 years 0 0 0 Abbreviations: UC, ulcerative colitis; CD, Crohn’s disease; PSC, primary sclerosing cholangitis; CRC, colorectal cancer; HGD, high-grade dysplasia; LGD, low-grade dysplasia. Open in new tab 4. Discussion In the present study, we report a high adherence to surveillance guidelines in parallel with an overall low incidence of CRC and dysplasia in the screened population. In addition, rates of CRC and dysplasia incidentally detected prior to the suggested start of surveillance were low. The present study is the second to report on CRD/CRC surveillance practices in UC in Canada24 and the first study to investigate CRC/CRD and CRA incidence and its relationship to adherence to CRC surveillance guidelines in a tertiary care IBD centre. The majority of patients with colonic CD or UC and at least 8 years of disease duration or PSC underwent at least one dedicated surveillance colonoscopy. Adherence rates for surveillance in UC and colonic [L2] CD were high, in line with the adherence rates [74%] reported in another Canadian centre24 in a much smaller IBD cohort. The median intervals between CRD/CRC surveillance colonoscopies in both the UC and the CD population fell within the recommended time intervals as per modified BSG guidelines for surveillance in IBD except for patients with coexisting PSC. None of the PSC patients was found to have CRC, although the incidence of dysplasia was high [936.1/100,000 patient-years]. PSC is one of the most extensively studied risk factors for CRC, and it was associated with a 9- and 2.9-fold elevated CRC risk in UC and CD, respectively, in a nationwide Danish study.11 Overall, rates of adherence to CRD/CRC surveillance guideline recommendations were high in the context of both appropriate intervals and number of random biopsies during surveillance colonoscopies in our centre. In more than half of the cases, endoscopists in the present study complied with the recommended four biopsies every 10 cm or at least 30 biopsies in L2 CD and UC. When compared to published data,24–29 the adherence to biopsy guidelines at the MUHC IBD centre is one of the highest reported for colitis-predominant CD [L2] and UC. A survey-based study by Kaltz et al.27 found that in UC patients belonging to the German Crohn’s Disease/Ulcerative Colitis Association, only 9.2% underwent a colonoscopy that conformed with guidelines, and in 50% of those surveillance endoscopies fewer than ten biopsies were taken. Similarly, a survey-based study conducted in England by Eaden et al. found that among 298 academic and community gastroenterologists undertaking surveillance for CRD/CRC in UC patients, 50% take 6–10 biopsies per surveillance endoscopy, while only 2% take over 20 biopsies.29 An earlier publication from a Canadian centre by Kottachchi et al.24 found that 22.8% of UC patients had an appropriate number of biopsies with increasing adherence after guideline publication.24 In our cohort, 53.7% of UC patients had at least 30 biopsies per surveillance colonoscopy. The utility of random biopsies for the detection of dysplasia has been called into question by previous studies that show that the diagnostic yield for dysplasia is lower compared to targeted biopsies and does not necessarily lead to a change in management. A study by van den Broek et al. in 2014 looked at 11,772 random biopsies in UC patients and found that the yield was low for dysplasia in addition to the observation that diagnosed neoplasia was macroscopically visible in 94% of cases.30 A recent publication from Japan came to partly different conclusions and reported that although being more labour-intensive, random biopsies were not inferior in detecting CRD or CRC in IBD.20 In fact, our current practice at MUHC is to take targeted biopsies from visible lesions in addition to the random quadrant biopsies from macroscopically normal looking colon. The importance of the number of biopsies was studied by Awais et al.31 According to their model, taking 32 random biopsies provides 80% confidence that dysplasia involving 5% or more of the colon can be detected, while taking ten biopsies only may be associated with failure to detect an area with 21% of dysplastic surface. The importance of random biopsies is further supported by a recent study from France reporting that 12.8% of colorectal neoplasias were only detected after random biopsies in patients undergoing chromoendoscopy.32 In the latter study, dysplasia identified by random biopsies was associated with PSC, a personal history of dysplasia and tubular-appearing colon on endoscopy.32 Of note, the chromoendoscopy rate was low in the present study, preventing a separate analysis of these patients. In parallel with the high rates of adherence to surveillance recommendations, the incidence of CRC and HGD was relatively low in both the screened CD and the UC cohort at 25.1 and 19.5/100,000 patient-years, lower than the reported incidence of CRC in the background population in both Canada and the United States. According to data published in 2011 by the Canadian Cancer Society, the incidence of CRC in the general population is 79.6/100,000 patient-years in men and 54.9/100,000 patient-years in women, which is significantly higher than the incidence in our cohort.33 In the United States, the incidence of CRC is lower, reported at 38.6/100,000 patient-years as per the 2013 SEER Database.34 It is prudent to note that the incidence reported for our IBD patients cannot be directly compared to the background incidence in the population given that this study was performed in a tertiary referral centre and was not population-based. However, the comparison can potentially be used as a marker of surveillance performance. In addition, the concept that more severe inflammation may lead to higher cancer rates is appealing, so the low rates reported from a specific IBD centre in patients with a high disease burden in parallel with high rates of surveillance accuracy are encouraging. Nevertheless, a recent paper from the St. Marks’ Hospital35 reported a strong association between the cumulative inflammatory burden and CRC risk. Each 10, 5 or 3.3 years of continuous mild, moderate or severe active microscopic inflammation was associated with a 2.1-fold increased hazard ratio for the development of colorectal neoplasia. Previous studies have reported a decline in the incidence of CRC in IBD patients over the last 40 years11,36 as well as a decreased risk of death from CRC in population-based cohorts.37 While the reason for such observed trends is multifactorial, our data suggest that high adherence to surveillance in terms of both frequency and number of biopsies obtained may be a contributory factor. Over the last 40 years the implementation and evolution of society guidelines is also a salient factor.24 The innovation of surveillance methods in terms of white-light endoscopy with improved optics is an additional significant consideration.38 An important auxiliary finding of the present study for everyday practice is that the incidence of CRD prior to 8 years of disease duration was low in both UC and CD at 12.5/100,000 and 19.5/100,000 patient-years for L2–L3 CD and UC respectively, which indicates that surveillance before 8 years in the absence of PSC is probably not indicated. This is concordant with previous data showing that the average time to development of CRD in IBD is 10 years in most populations.15 Of note, the median duration of disease was 17 years for the surveillance cohort. Chromoendoscopy for CRD/CRC surveillance was only used in 2.4% of the UC surveillance group and in none of the CD or PSC patients, demonstrating under-utilization of this modality. Importantly, chromoendoscopy has emerged as an alternative modality of surveillance of dysplasia according to the guidelines39 and it has been reported to be associated with increased dysplasia detection rates of 1.8-fold per patient.38 The reported increased dysplasia detection rates has led to it being the preferred modality of surveillance in the BSG guidelines18 and as an acceptable alternative to white-light endoscopy in the American Gastroenterological Association surveillance guidelines.40 However, chromoendoscopy may be under-utilized due to resource, time and expertise barriers in real-life cohorts as seen also in our centre. We found higher CRA rates in contrast to previous studies.41–44 It has been suggested that although chronic colonic inflammation increases the risk for IBD-related CRC development in the affected area, this same inflammation might prevent the usual sequential adenoma–carcinoma development. Of note, the primary molecular pathway is different in patients with chronic colonic inflammation.45,46 We believe that the high adherence to surveillance guidelines in the present cohort is an important factor leading to higher CRA detection rates. The strengths of the present study include that data were obtained in a tertiary referral centre with harmonized care practices and a strong emphasis on delivering quality care to our patients, as reflected by the objective patient monitoring and quality indicators of our centre during follow-up47 resulting in less practice variation and a high adherence to surveillance guidelines. In addition, consecutive patients were included to avoid selection bias. The study has multiple limitations, including its retrospective nature as well as potential bias given that patients with poor adherence to follow-up, including utilizing surveillance endoscopy, might have been missed due to the type of inclusion process. In addition, treatment practices and results obtained in an IBD centre may not be directly applicable or reproducible in other [e.g. community practice] settings. Despite the cited limitations, the data presented here are directly applicable to clinical practice, as they reinforce that adherence to surveillance guidelines translates directly into improved outcomes. 5. Conclusions The results from the present study demonstrate a high level of adherence to surveillance guidelines in parallel with overall low CRC and dysplasia but not CRA rates in the screened population, despite the underuse of chromoendoscopy. Our findings suggest that meeting current, stratified, less labour-intensive surveillance recommendations may result in low CRC rates in all IBD patients. In addition, CRC and dysplasia rates detected before the recommended start of the surveillance were low, suggesting that an earlier start of surveillance is probably not indicated. Funding The study was supported by the McGill CAS Research Support Program, the Kimberly Sue McCall Award in IBD Research, the Nesbitt-McMaster Award and the WI230654 Pfizer unrestricted research grant. Conflict of Interest None of the contributing authors has any conflicts of interest to declare. Author Contributions KS and PLL created the concept and designed the study. KS identified and assessed eligible patients, extracted data and wrote the manuscript. AA co-wrote the manuscript. PLL analysed and interpreted the data and co-authored the manuscript. ZK, RK, WA, CV, JR, LG, TB, ES, GW and AB revised the article for intellectual content. All authors approved the final version of the submitted manuscript. References 1. 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 – 45 . Google Scholar Crossref Search ADS PubMed WorldCat 2. Jess T , Gamborg M , Matzen P , Munkholm P , Sørensen TI . Increased risk of intestinal cancer in Crohn’s disease: a meta-analysis of population-based cohort studies . Am J Gastroenterol 2005 ; 100 : 2724 – 9 . Google Scholar Crossref Search ADS PubMed WorldCat 3. Eaden JA , Abrams KR , Mayberry JF . The risk of colorectal cancer in ulcerative colitis: a meta-analysis . Gut 2001 ; 48 : 526 – 35 . Google Scholar Crossref Search ADS PubMed WorldCat 4. Rutter MD , Saunders BP , Wilkinson KH , et al. . Thirty-year analysis of a colonoscopic surveillance program for neoplasia in ulcerative colitis . Gastroenterology 2006 ; 130 : 1030 – 8 . Google Scholar Crossref Search ADS PubMed WorldCat 5. Sengupta N , Yee E , Feuerstein JD . Colorectal cancer screening in inflammatory bowel disease . Dig Dis Sci 2016 ; 61 : 980 – 9 . Google Scholar Crossref Search ADS PubMed WorldCat 6. Lutgens MW , van Oijen MG , van der Heijden GJ , Vleggaar FP , Siersema PD , 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 – 99 . Google Scholar Crossref Search ADS PubMed WorldCat 7. Beaugerie L , Svrcek M , Seksik P , et al. . Risk of colorectal high-grade dysplasia and cancer in a prospective observational cohort of patients with inflammatory bowel disease . Gastroenterology 2013 ; 145 : 166 – 75.e8 . Google Scholar Crossref Search ADS PubMed WorldCat 8. Flores BM , O’Connor A , Moss AC . Impact of mucosal inflammation on risk of colorectal neoplasia in patients with ulcerative colitis: a systematic review and meta-analysis . Gastrointest Endosc 2017 ; 86 : 1006 – 1011.e8 . Google Scholar Crossref Search ADS PubMed WorldCat 9. Fumery M , Pineton de Chambrun G , Stefanescu C , et al. . Detection of dysplasia or cancer in 3.5% of patients with inflammatory bowel disease and colonic strictures . Clin Gastroenterol Hepatol 2015 ; 13 : 1770 – 5 . Google Scholar Crossref Search ADS PubMed WorldCat 10. Zheng HH , Jiang XL . Increased risk of colorectal neoplasia in patients with primary sclerosing cholangitis and inflammatory bowel disease: a meta-analysis of 16 observational studies . Eur J Gastroenterol Hepatol 2016 ; 28 : 383 – 90 . Google Scholar Crossref Search ADS PubMed WorldCat 11. 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 – 81.e1 ; quiz e13–4. Google Scholar Crossref Search ADS PubMed WorldCat 12. Velayos FS , Terdiman JP , Walsh JM . Effect of 5-aminosalicylate use on colorectal cancer and dysplasia risk: a systematic review and metaanalysis of observational studies . Am J Gastroenterol 2005 ; 100 : 1345 – 53 . Google Scholar Crossref Search ADS PubMed WorldCat 13. Baars JE , Looman CW , Steyerberg EW , 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 ; 106 : 319 – 28 . Google Scholar Crossref Search ADS PubMed WorldCat 14. van Schaik FD , van Oijen MG , Smeets HM , van der Heijden GJ , Siersema PD , Oldenburg B . Thiopurines prevent advanced colorectal neoplasia in patients with inflammatory bowel disease . Gut 2012 ; 61 : 235 – 40 . Google Scholar Crossref Search ADS PubMed WorldCat 15. Beaugerie L , Itzkowitz SH . Cancers complicating inflammatory bowel disease . N Engl J Med 2015 ; 372 : 1441 – 52 . Google Scholar Crossref Search ADS PubMed WorldCat 16. Obrador A , Ginard D , Barranco L . Review article: colorectal cancer surveillance in ulcerative colitis - what should we be doing? Aliment Pharmacol Ther 2006 ; 24 [ Suppl 3 ]: 56 – 63 . Google Scholar Crossref Search ADS PubMed WorldCat 17. Van Assche G , Dignass A , Bokemeyer B , et al. . ; European Crohn’s and Colitis Organisation . Second European evidence-based consensus on the diagnosis and management of ulcerative colitis part 3: special situations . J Crohns Colitis 2013 ; 7 : 1 – 33 . Google Scholar Crossref Search ADS PubMed WorldCat 18. Cairns , S.R. , et al. . , Guidelines for colorectal cancer screening and surveillance in moderate and high risk groups (update from 2002) . Gut 2010 ; 59 : 666 – 89 . Google Scholar Crossref Search ADS PubMed WorldCat 19. Itzkowitz SH , Harpaz N . Diagnosis and management of dysplasia in patients with inflammatory bowel diseases . Gastroenterology 2004 ; 126 : 1634 – 48 . Google Scholar Crossref Search ADS PubMed WorldCat 20. Watanabe T , Ajioka Y , Mitsuyama K , et al. . Comparison of targeted vs random biopsies for surveillance of ulcerative colitis-associated colorectal cancer . Gastroenterology 2016 ; 151 : 1122 – 30 . Google Scholar Crossref Search ADS PubMed WorldCat 21. Rubin DT , Rothe JA , Hetzel JT , Cohen RD , Hanauer SB . Are dysplasia and colorectal cancer endoscopically visible in patients with ulcerative colitis? Gastrointest Endosc 2007 ; 65 : 998 – 1004 . Google Scholar Crossref Search ADS PubMed WorldCat 22. Satsangi J , Silverberg MS , Vermeire S , Colombel JF . The Montreal classification of inflammatory bowel disease: controversies, consensus, and implications . Gut 2006 ; 55 : 749 – 53 . Google Scholar Crossref Search ADS PubMed WorldCat 23. Mowat C , Cole A , Windsor A , et al. . ; IBD Section of the British Society of Gastroenterology . Guidelines for the management of inflammatory bowel disease in adults . Gut 2011 ; 60 : 571 – 607 . Google Scholar Crossref Search ADS PubMed WorldCat 24. Kottachchi D , Yung D , Marshall JK . Adherence to guidelines for surveillance colonoscopy in patients with ulcerative colitis at a Canadian quaternary care hospital . Can J Gastroenterol 2009 ; 23 : 613 – 7 . Google Scholar Crossref Search ADS PubMed WorldCat 25. Gearry RB , Wakeman CJ , Barclay ML , 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 – 22 . Crossref Search ADS PubMed 26. Ahmed T , Monti J , Lashner B . Random versus targeted biopsies for colorectal cancer surveillance in inflammatory bowel disease . Gastroenterol Hepatol (N Y) 2010 ; 6 : 438 – 42 . Google Scholar PubMed WorldCat 27. Kaltz B , Bokemeyer B , Hoffmann J, Porschen R, Rogler G, Schmiegel W . Surveillance colonoscopy in ulcerative colitis patients in Germany . Z Gastroenterol 2007 ; 45 : 325 – 31 . Google Scholar Crossref Search ADS PubMed WorldCat 28. Rubin CE , Haggitt RC , Burmer GC , et al. . DNA aneuploidy in colonic biopsies predicts future development of dysplasia in ulcerative colitis . Gastroenterology 1992 ; 103 : 1611 – 20 . Google Scholar Crossref Search ADS PubMed WorldCat 29. Eaden JA , Ward BA , Mayberry JF . How gastroenterologists screen for colonic cancer in ulcerative colitis: an analysis of performance . Gastrointest Endosc 2000 ; 51 : 123 – 8 . Google Scholar Crossref Search ADS PubMed WorldCat 30. van den Broek FJ , Stokkers PC , Reitsma JB , et al. . Random biopsies taken during colonoscopic surveillance of patients with longstanding ulcerative colitis: low yield and absence of clinical consequences . Am J Gastroenterol 2014 ; 109 : 715 – 22 . Google Scholar Crossref Search ADS PubMed WorldCat 31. Awais D , Siegel CA , Higgins PD . Modelling dysplasia detection in ulcerative colitis: clinical implications of surveillance intensity . Gut 2009 ; 58 : 1498 – 503 . Google Scholar Crossref Search ADS PubMed WorldCat 32. Moussata D , Allez M , Cazals-Hatem D , et al. . ; the GETAID . Are random biopsies still useful for the detection of neoplasia in patients with IBD undergoing surveillance colonoscopy with chromoendoscopy? Gut 2018 ; 67 : 616 – 24 . Google Scholar PubMed WorldCat 33. Canadian Cancer Society . Colorectal Cancer Statistics . Toronto : Canadian Cancer Society ; 2017 . WorldCat COPAC 34. Noone AM , Howlader N , Krapcho M , Miller D , Brest A , Yu M , et al. . (eds). SEER Cancer Statistics Review , 1975–2015. Bethesda, MD: National Cancer Institute; November 2017 SEER data submission, posted to the SEER web site, April 2018. https://seer.cancer.gov/csr/ 1975_2015/ COPAC 35. Choi CR , Al Bakir I , Ding NJ . Cumulative burden of inflammation predicts colorectal neoplasia risk in ulcerative colitis: a large single-centre study . Gut 2019;68:414–422 . WorldCat 36. Soderlund S , Rungoe C , Peyrin-Biroulet L . Risk of colorectal cancer in patients with ulceratirve colitis: a meta-analysis of population-based cohort studies . Clin Gastroenterol Hepatol 2009 ; 10 : 639 – 645 . WorldCat 37. Jess T , Frisch M , Simonsen J . Trends in overall and cause-specific mortality among patients with inflammatory bowel disease from 1982 to 2010 . Clin Gastroenterol Hepatol 2013 ; 11 : 43 – 48 . Google Scholar Crossref Search ADS PubMed WorldCat 38. Naymagon S , Ullman TA . Chromoendoscopy and dysplasia surveillance in inflammatory bowel disease: past, present, and future . Gastroenterol Hepatol (N Y) 2015 ; 11 : 304 – 11 . Google Scholar PubMed WorldCat 39. Laine L , Kaltenbach T , Barkun A , McQuaid KR , Subramanian V , Soetikno R ; SCENIC Guideline Development Panel . SCENIC international consensus statement on surveillance and management of dysplasia in inflammatory bowel disease . Gastroenterology 2015 ; 148 : 639 – 51.e28 . Google Scholar Crossref Search ADS PubMed WorldCat 40. Farraye FA , Odze RD , Eaden J , et al. . ; AGA Institute Medical Position Panel on Diagnosis and Management of Colorectal Neoplasia in Inflammatory Bowel Disease . AGA medical position statement on the diagnosis and management of colorectal neoplasia in inflammatory bowel disease . Gastroenterology 2010 ; 138 : 738 – 45 . Google Scholar Crossref Search ADS PubMed WorldCat 41. Sonnenberg A , Genta RM . Low prevalence of colon polyps in chronic inflammatory conditions of the colon . Am J Gastroenterol 2015 ; 110 : 1056 – 61 . Google Scholar Crossref Search ADS PubMed WorldCat 42. Kitiyakara T , Bailey DM , McIntyre AS , Gorard DA . Adenomatous colonic polyps are rare in ulcerative colitis . Aliment Pharmacol Ther 2004 ; 19 : 879 – 87 . Google Scholar Crossref Search ADS PubMed WorldCat 43. Dixon A , Wurm P , Hart A , Robinson R . Distal adenomatous polyps are rare in patients with inflammatory bowel disease . Postgrad Med J 2006 ; 82 : 76 – 8 . Google Scholar Crossref Search ADS PubMed WorldCat 44. Ben-Horin S , Izhaki Z , Haj-Natur O , Segev S , Eliakim R , Avidan B . Rarity of adenomatous polyps in ulcerative colitis and its implications for colonic carcinogenesis . Endoscopy 2016 ; 48 : 215 – 22 . Google Scholar Crossref Search ADS PubMed WorldCat 45. Lakatos PL , Lakatos L . Risk for colorectal cancer in ulcerative colitis: changes, causes and management strategies . World J Gastroenterol 2008 ; 14 : 3937 – 47 . Google Scholar Crossref Search ADS PubMed WorldCat 46. Gajewski TF , Schreiber H , Fu YX . Innate and adaptive immune cells in the tumor microenvironment . Nat Immunol 2013 ; 14 : 1014 – 22 . Google Scholar Crossref Search ADS PubMed WorldCat 47. Kurti Z , Restellini S , Gonczi L , et al. . Quality of care and outcomes in a tertiary hospital inflammatory bowel disease (IBD) centre: monitoring and treatment algorithms during follow-up. In: 13th Congress of the European Crohn’s and Colitis Organization ; Vienna, Austria ; 2018 . WorldCat Author notes Equal first-authors. Copyright © 2019 European Crohn’s and Colitis Organisation (ECCO). Published by Oxford University Press. All rights reserved. For permissions, please email: journals.permissions@oup.com This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model)
TI - High Adherence to Surveillance Guidelines in Inflammatory Bowel Disease Patients Results in Low Colorectal Cancer and Dysplasia Rates, While Rates of Dysplasia are Low Before the Suggested Onset of Surveillance
JO - Journal of Crohn's and Colitis
DO - 10.1093/ecco-jcc/jjz066
DA - 2019-09-27
UR - https://www.deepdyve.com/lp/oxford-university-press/high-adherence-to-surveillance-guidelines-in-inflammatory-bowel-tqnHkoa7rT
SP - 1343
VL - 13
IS - 10
DP - DeepDyve
ER -