Background: Adenoma Detection Rate (ADR) is a validated colonoscopy quality indicator. In addition to overall ADR, Distal and Proximal Adenoma Detection Rates may provide important colonoscopy quality information. The goal of this study is to determine the association between distal and proximal adenoma detection (AD) and to identify factors contributing to overall, distal, and proximal AD. Methods: This is a retrospective cohort study of patients with a noted family history of CRC or positive fecal occult blood test who underwent a screening colonoscopy at a regional colorectal cancer (CRC) screening center between May 2009 and December 2011. Data regarding patient demographics, procedure details, endoscopist characteristics and polyp histology were captured. The main outcomes measured were overall, distal, and proximal AD. Results: 1907 patients were included. The median age was 60 years and 42% were male. Endoscopist median overall ADR was 25% (30% male, 21% female). Endoscopist distal ADR was only modestly associated with their proximal ADR (Spearman Rank: 0.51 p = 0.11). Highest overall ADR (29 to 45%) was found for endoscopists whose distal and proximal ADRs were above the group median. In multivariate analysis, factors associated with overall, distal, and proximal AD included age, sex, and endoscopist practicing experience. Conclusion: Inclusion of distal and proximal ADRs, in addition to overall ADR, in colonoscopy quality assessment provides the more accurate feedback on endoscopist performance. Keywords: Adenoma detection rate, Adenoma, Colonoscopy, Colorectal cancer Background The quality indicator currently recommended by the Colonoscopy is considered the most effective method for American Society for Gastrointestinal Endoscopy is Aden- the identification and removal of adenomatous polyps oma Detection Rate (ADR) [4, 5]. ADR is defined as the . However, multiple studies have shown significant proportion of colonoscopies where at least one adenoma polyp and adenoma miss rates for colonoscopies , as is found . An endoscopist’s ADR has been shown to be well as lower than expected reduction in mortality for associated with overall patient risk of interval colorectal proximal colorectal cancers . These factors have cancer (colorectal cancer diagnosed within a few years of highlighted the necessity for effective quality indicators to colonoscopy) [7, 8], risk of distal interval colorectal cancer monitor and advance colon cancer screening programs. , and risk of fatal interval colorectal cancer . Little is known about the rate of adenoma detection in * Correspondence: firstname.lastname@example.org specific segments of the colon. Lesions in the distal and Paul James and Mehdi Hegagi contributed equally to this work. 1 proximal colon have been shown to adhere to differing Department of Medicine, The University of Ottawa, Ottawa, Canada Ottawa Hospital Research Institute, The University of Ottawa, Ottawa, patterns of development. Specifically, sessile serrated ad- Canada enomas are primarily observed in the proximal colon. Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. James et al. BMC Gastroenterology (2018) 18:73 Page 2 of 8 These lesions are more difficult to detect and resect and Screening Clinic - a regional colon cancer screening cen- have been proposed to follow a unique serrated pathway ter. Patients between 50 and 75 years of age, who were re- that progresses to carcinogenesis more rapidly than the ferred to the Colon Cancer Screening Clinic with a first APC-linked pathway of other adenomas [10–12]. Whether degree relative with colon cancer or a positive fecal occult this variablity in adenoma presentation in different blood test (FOBT), were included. Colonoscopy Interim segments of the colon is reflected in variable rates of Reporting Tool (CIRT) forms were mandatorily filled out adenoma detection between segments, remains to be by the endoscopist of the screening clinic after each pro- determined. Recent publications and guidelines have cedure. In these forms, procedure indication options in- focused on identifying adenomas in the proximal cluded: symptoms, surveillance, positive FOBT, family colon. To our knowledge, only two studies to date have history of colon cancer in a first-degree relative, and other. examined adenoma detection rates in the distal colon The indications of interest in this study included having a [13, 14]. These have produced inconsistent results. family history in a first-degree relative and a positive Whereas Boroff and colleagues observed a lower inter-op- FOBT. Withdrawal time was not captured. Colonoscopies erator (between endoscopists) ADR for the distal colon, as performed for other indications, including symptoms compared to the proximal colon , Schramm and col- and colon cancer surveillance, were excluded. Cases leagues observed higher distal ADR . Intra-operator where the endoscopist performed less than 50 screening (for the same endoscopist) differences for distal and prox- colonoscopies during the study period were also excluded imal detection have not been previously assessed. (Fig. 1). Identifying variability in an endoscopist’s detection of Using the information from the CIRT data collection distal vs proximal adenomas offers an opportunity to en- forms and patient chart review, a database was created hance performance assessment and improve colonoscopy containing patient (age and sex), endoscopist (specialty quality. The aims of the study presented here are to 1) de- and number of years in practice), and procedure (indica- termine if intra-operator differences exist in distal and tion for colonoscopy, bowel preparation, number of polyps proximal ADR and 2) identify factors that predict overall, found, and the location of each polyp in the colon) infor- distal, and proximal adenoma detection. mation. All bowel preparations involved 4 L of polyethyl- ene glycol 3350 (Colyte). In the majority of cases, 2 L split Methods prep dosing was used at the discretion of the endoscopist. Ethics approval Bowel preparation was defined as good when all residue This retrospective study protocol was approved by the was liquid and over 90% of the mucosal surface was vis- Ottawa Hospital Research Ethics Board. ible, fair when there was some semisolid stool that could be suctioned or washed away and over 90% of the mucosa Study protocol surface was visualized, and poor when semisolid stool A retrospective study was performed for all high defin- could not be suctioned or washed away and less than 90% ition white light colonoscopies between May 2009 and of the mucosal surface was visualized . Cases involving December 2011 at the Ottawa Hospital Colorectal Cancer good and fair bowel preparation were grouped together, as Fig. 1 Data Inclusions Flowchart James et al. BMC Gastroenterology (2018) 18:73 Page 3 of 8 they have been shown to be associated with similar levels Distal ADR = proportion of colonoscopies where at of adenoma detection . least one adenoma is found in the distal colon. Pathology reports were reviewed to determine histology Proximal ADR = proportion of colonoscopies where at of each colonic polyp removed. Consistent with previous least one adenoma is found in the proximal colon. studies , all polyps with adenoma or sessile serrated Adenoma to polyp detection rate quotient (ADPRQ) = pathology were included as adenomas. proportion of removed polyps found to be adenomas on At our center, colonoscopy procedures are scheduled histological analysis. into 30-min time slots. To account for cases where 30 min may have been insufficient time to remove all of Statistical analyses the polyps identified during the initial colonoscopy, we Categorical variables were reported as frequencies and determined if an additional colonoscopy was performed proportions while continuous variables were presented as within 12 months of the first (index) screening colonos- medians with interquartile range. Scatter plot and Spear- copy with the use of the Ottawa Hospital Colonoscopy man rank correlation were used to evaluate the association Database. If additional colonoscopies were found, the between ADR, distal ADR, and proximal ADR. Logistic re- number, location and histology of each polyp removed gression models were developed to study univariate and within one year of the index colonoscopy were collected multivariate associations between the independent vari- and pooled for each patient. We also used this database ables and overall, distal, and proximal AD. Only those vari- to calculate each endoscopist’s colonoscopy case volume ables found to have a significant univariate association for the period of October 1st 2011 to March 31st 2012. (p-value cut-off of < 0.05) with the dependent variables Each endoscopist was contacted directly in order to wereincluded in themultivariatemodels. Thedatawas obtain information regarding their practicing specialty analyzed using STATA statistical software version 13.1 and their completion of training. This was then corrobo- (StataCorp, College Station, Texas, 2014). rated using the College of Physicians and Surgeons of Ontario’s public register. Results The distribution of colonic polyps was assessed using A total of 1907 patients underwent screening colonos- the following definitions: copies and 11 endoscopists were included in the study Distal colon = splenic flexure, descending colon, sigmoid, (Table 1). The indication for the majority of patients was and rectum. having a first degree relative with colon cancer (63%). Proximal colon = cecum, ascending colon, hepatic The mean age was 60 years old and 42% of patients were flexure, and transverse colon. male. In most cases (83%) the endoscopist was a gastro- ADR = proportion of colonoscopies where at least one enterologist. Very few of the procedures involved poor adenoma is found based on histological analysis. bowel preparation (1%). The cecum was intubated in Table 1 Cohort demographics and procedure details for the entire cohort, n = 1907, and patients found to have at least one adenoma on colonoscopy Total Cohort Min. one adenoma Min. one proximal adenoma Min. one distal adenoma (N = 1907) (N = 467) (N = 248) (N = 308) Age, Median (IQR) years 60 (55–65) 61 (56–66) 62 (56–67) 61 (55–66) Male Sex, n(%) 769 (41.7) 240 (51.4) 128 (51.6) 144 (52.0) Indication, n(%) Family history 1198 (62.8) 263 (56.3) 148 (59.68) 138 (49.8) Positive FOBT 709 (37.2) 204 (43.7) 100 (40.3) 139 (50.2) Poor Bowel Preparation, n(%) 27 (1.4) 5 (1.1) 3 (1.2) 2 (0.7) Colonoscopy Volume , 150 (53–215) 166 (96–215) 174 (147–215) 157 (89–215) Median (IQR) procedures Cecal intubation, n(%) 1857 (97.4) 559 (98.3) 244 (98.4) 273 (98.6) Endoscopist Years of Practice, 26 (22–38) 23 (9–38) 21 (9–32) 24 (9–38) Median (IQR) years Endoscopist Specialty, n(%) Gastroenterology 1580 (83.0) 356 (76.2) 212 (76.5) 181 (73.0) Surgery 327 (17.2) 111 (23.8) 65 (23.5) 67 (27.0) Case volume over a 6 month period (October 1st 2011 to March 31st 2012) Note: IQR interquartile range James et al. BMC Gastroenterology (2018) 18:73 Page 4 of 8 almost all of the cases (97%). More than one colonos- between distal and proximal ADR was 0.51 (P = 0.11), copy was performed within 12 months of the index col- suggesting only a moderate positive association (Fig. 3). onoscopy in 70 patients (4%). Patient demographics and Overall ADR was found to be strongly associated with procedure details are presented in Table 1. both distal (S = 0.78, p < 0.01) and proximal ADR (S = 0.83, p < 0.01). Adenoma detection The overall ADR, distal ADR, and proximal ADRs were Factors associated with adenoma detection 25% (30% for males and 21% for females), 15, and 13%, Univariate logistic regression (Table 2) showed that over- respectively. The overall adenoma to polyp detection all adenoma detection was significantly associated with rate quotient (APDRQ) was 50%. Distal ADPRQ was patient age (1.03 [95% CI: 1.01–1.05]), sex (1.68 [95% CI: 38% and proximal APDRQ was 63%. The median ADR, 1.36–2.07]), endoscopist specialty (1.77 [95% CI: 1.37– distal ADR, and proximal ADRs were 28% (interquartile 2.29]) and years of practice (0.97 [95% CI: 0.97–0.98]). range [IQR] 20–30%), 15% (IQR 11–20%), and 15% (IQR Distal and proximal adenoma detection were also signifi- 10–19%), respectively. cantly associated with these factors. Endoscopist colonos- copy volume was associated with overall and proximal, Proximal, distal, and overall inter-endoscopist ADR but not distal adenoma detection. Having a positive FOBT Figure 2 presents the overall ADR for each endoscopist was associated with overall and distal, but not proximal as well as the proportion of their ADR that is attributed adenoma detection (Table 2). to adenoma detection in the proximal and distal colon. In multivariate analyses, age, sex, and endoscopist There was notable variability in both proximal and distal years of practice remained significantly associated with adenoma detection among endoscopists. Distal adenoma overall, distal, and proximal adenoma detection. While detection remained inconsistent even among higher per- increased age and male sex were associated with higher formance endoscopists with overall ADRs greater than adenoma detection, greater endoscopist years of practice 25%. was related to lower adenoma detection. The association between adenoma detection and endoscopist specialty Correlation between endoscopist overall, distal, and was no longer significant (Table 3). proximal ADR Intra-operator differences in distal vs proximal ADR were Discussion observed. Two of the endoscopists who had above the me- In this study, we demonstrate a notable variability in en- dian proximal ADR, had below the median distal ADR, doscopist distal and proximal adenoma detection. Our while the opposite was observed for two of the other findings suggest that distal and proximal ADR, used in higher performance endoscopists. The highest overall conjunction with overall ADR, can improve the assess- ADR (ADR range 29 to 45%) was found for the four ment of colonoscopy quality. endoscopists whose distal and proximal ADRs were The observed variability in adenoma detection rates above the median. The Spearman rank correlation (S) between the distal and proximal colon may be attributable Fig. 2 Adenoma Detection of Each Endoscopist. *Proximal ADR Exclusively = cases where ADR is solely made up of proximal ADR. Distal ADR Exclusively = cases where ADR is solely made up distal ADR James et al. BMC Gastroenterology (2018) 18:73 Page 5 of 8 we observed markedly lower distal ADPRQ, as compared to proximal APDRQ (38 and 63%, respectively). Adenoma detection is also dependent on skill, training and experience, as demonstrated by significant variability in ADR between endoscopists . Interestingly, adenoma miss rates between endoscopists have been previously found to differ for the distal and proximal colon, suggest- ing that different skills may be required for these segments . In accordance with this observation, our study demonstrates that proficiency in distal adenoma detec- tion does not directly correlate with proximal adenoma detection for the same endoscopist. This observation was independent of endoscopist overall performance Fig. 3 The association between proximal ADR and distal ADR (as indicated by overall ADR). Section-specific operator skills necessary for adenoma detection may relate to variances in polyp morphology , frequency , to both physiological differences between colon segments and the extent of blind spots in certain parts of the dis- and the varibility in operator skill sets. For instance, there tal and proximal colon . are reported differences in segment-specific adenoma oc- Some specific operator skill measures found to be as- currence rate [13, 17]. Boroff and colleagues found that sociated with overall ADR include endoscopist accredit- while only 30% of distal polyps are diagnosed as adenomas ation and colonoscopy volume , as well as years of on histology, adenomas correspond to 76% of polyps in experience . Here we confirm that overall ADR is the proximal colon . Consistent with these findings, correlated with all of these operator characteristics. Table 2 Univariate Analysis for Predictors of Overall, Proximal, and Distal Overall AD Proximal AD Distal AD OR 95% CI p-value OR 95% CI p-value OR 95% CI p-value Age: 1.03 1.01–1.05 < 0.01 1.04 1.02–1.07 < 0.01 1.02 1.00–1.04 0.01 (per year) Sex: 1.68 1.36–2.07 < 0.01 1.58 1.21–2.07 < 0.01 1.62 1.26–2.10 < 0.01 Male vs Female Indication: 1.44 1.16–1.78 < 0.01 1.16 0.89–1.53 0.27 1.89 1.45–2.42 < 0.01 Family history vs Positive FOBT Bowel preparation: 0.67 0.26–1.85 0.47 0.83 0.25–2.80 0.77 0.47 0.11–1.98 0.30 Poor vs Good or fair Colonoscopy volume 1.00 1.00–1.00 < 0.01 1.00 1.00–1.01 < 0.01 1.00 1.00–1.00 0.15 (per procedure) Intubation: 1.72 0.80–3.70 0.16 1.74 0.62–4.88 0.29 1.98 0.48–2.19 0.19 Cecal vs Incomplete Years of practice 0.97 0.97–0.98 < 0.01 0.96 0.95–0.97 < 0.01 0.98 0.71–5.55 < 0.01 (per year) Endoscopist Specialty: 1.77 1.37–2.29 < 0.01 2.00 1.46–2.72 < 0.01 1.60 1.18 - 2.18 < 0.01 Gastroenterology vs Surgery Note: AD Adenoma detection James et al. BMC Gastroenterology (2018) 18:73 Page 6 of 8 Table 3 Multivariate Analysis for Predictors of Overall, Proximal experience are more likely to complete the colonoscopy and Distal to the cecum and are better attuned to detecting sessile Overall AD serrated adenomas . In the setting of limited endos- copy time, if more time is attributed to identifying and OR 95% CI p-value removing polyps the proximal colon, the withdrawal Age 1.03 1.02–1.05 < 0.01 (per year) time for the distal colon may be compromised, resulting in reduced distal adenoma detection . Sex 1.59 1.29–1.95 < 0.01 Male vs Adenoma detection also showed a weak inverse associ- Female ation with endoscopy years of practice. This is consistent Indication 1.31 1.06–1.63 0.01 with previous research demonstrating that optimal ADR Family history vs occurs with a lower number of years of experience , Positive FOBT suggesting that training plays a more important role in Colonoscopy volume 1.00 1.00–1.00 < 0.01 the quality of adenoma detection than years of experi- (per procedure) ence . Years of practice 0.98 0.97–0.99 < 0.01 Patient-related overall ADR determinants are known (per year) to include patient age and gender . Our findings Endoscopist Specialty 1.26 0.90–1.76 0.18 Gastroenterology vs confirm these observations and demonstrate similar as- Surgery sociations for both distal and proximal ADR. Proximal AD Certain study limitations should be noted. First, the study was carried out in a single institution setting. Future OR 95% CI p-value investigations should determine if our observations are Age 1.05 1.03–1.07 < 0.01 (per year) applicable elsewhere. On the other hand, our observed variability in proximal and distal adenoma detection is Sex 1.65 1.25–2.17 < 0.01 Male vs consistent with what has been previously observed . Female Second, we were unable to examine certain procedural Colonoscopy volume 1.01 1.00–1.01 < 0.01 factors that have been previously associated with ADR (per procedure) such as withdrawal time  and time of day [28, 29]. The Years of practice 0.96 0.95–0.98 < 0.01 influence of colonoscopy queue position during the day, (per year) insertion time, and withdrawal time on proximal and dis- Endoscopist Specialty 1.13 0.73–1.74 0.58 tal adenoma detection warrant further study. Finally, we Gastroenterology vs did not differentiate between sessile and non-sessile aden- Surgery omas. Sessile polyps have been shown to be more difficult Distal AD to detect and may represent higher risk lesions [30, 31]. OR 95% CI p-value However, our approach is consistent with the existing en- Age 1.02 1.00–1.04 0.03 doscopy quality literature, which includes sessile serrated (per year) polyps as adenomas . Finally, the overall ADR for this Sex 1.52 1.17–1.97 < 0.01 study was 25% which, although within the acceptable Male vs quality standards for ADR recommended by the American Female Society for Gastrointestinal Endocopy and the American Indication 1.68 1.30–2.18 < 0.01 Family history vs College of Gastroenterology [1, 5], are lower than ADRs Positive FOBT presented elsewhere. We believe that the two main factors Years of practice 0.99 0.97–1.00 0.035 contributed our observed lower ADR: the high number of (per year) years in practice and low median annual volume of the Endoscopist Specialty 1.15 0.77–1.74 0.49 practicing endoscopists. Both of these factors were associ- Gastroenterology vs ated with lower ADR in this study. This may limit the Surgery generalizability of our results and future research should Note: AD Adenoma detection determine whether our findings are reproducible in other centres. However, while proximal adenoma detection was associ- For future investigations, we also recommend the ana- ated with endoscopist procedure volume, that was not lysis of advanced technologies such as EndoCuff, EndoR- the case for distal ADR. This indicates that the increase ings, G-EYE™, FUSE, and cap-assisted colonoscopy. These in ADR among higher volume endoscopists may be re- techniques have been related to ADR rates of up 69%. It lated to their ability to detect adenomas in the proximal has been proposed that using these devices to flatten folds colon. Endoscopists with a higher degree of skill and and improving endoscope stability can lead to narrowing James et al. BMC Gastroenterology (2018) 18:73 Page 7 of 8 the adenoma detection differences between the distal and Received: 1 July 2017 Accepted: 15 May 2018 proximal colon , however these technologies may be more applicable to augmenting ADR is specific areas of the colon. It has been previously demonstrated that feed- References 1. Rex DK, Johnson DA, Lieberman DA, et al. Colorectal cancer prevention back regarding overall ADR results in improvement in 2000: screening recommendations of the American College of proximal but not distal adenoma detection . An add- Gastroenterology. American College of Gastroenterology Am J itional question of interest would be whether colon Gastroenterol. 2000;95(4):868–77. 2. van Rijn JC, Reitsma JB, Stoker J, et al. Polyp miss rate determined by tandem segment-specific performance feedback to colonoscopists colonoscopy: a systematic review. Am J Gastroenterol. 2006;101(2):343–50. can produce a more even distribution of improvement. 3. 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Published: May 30, 2018