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Adenoma detection rate as a quality indicator for colonoscopy: a descriptive cross-sectional study from a tertiary care hospital in Pakistan

Background and study aims  Adenoma detection rate (ADR) is validated for measuring quality of colonoscopy, however there is lack of colorectal cancer (CRC) screening program in South Asia. The purpose of this study is to analyze and review the polyp detection rate (PDR) and ADR and provide insight into the factors that influence them in Pakistan. Patients and methods  This retrospective, cross-sectional study was performed at the Aga Khan University Hospital, Karachi, Pakistan, on patients ≥ 18 years, who underwent colonoscopy between January 1, 2017 and June 30, 2018. Results  Of 1985 patients, 59 % were male and 41 % female, with mean age of 47.8 ± 16.2 years. The most common indication for colonoscopy was bleeding-per-rectum (28.0 %) and overall PDR and ADR were 17.9 % and 9.9 %, respectively. There was no significant difference between genders for either PDR ( P  = 0.378) or ADR ( P  = 0.574). Significantly higher PDR and ADR were found for patients ≥ 50 years ( P  < 0.001), as well as for suboptimal bowel preparation [PDR (25.7 %; P  = 0.007) and ADR (18.6 %; P  = 0.014)]. Interestingly, endoscopists with < 500 colonoscopy-procedural-experience reported a higher PDR (21.6 %; P  = 0.020) and ADR (14.4 %; P = 0.049), corresponding to a significantly higher PDR (20.6 %; P  = 0.005) and ADR (11.7 %; P  = 0.02) for endoscopists in practice for ≤ 10 years. Conclusions  We have noticed low PDR and ADR, which require further investigation and research. In addition, we believe there should be a different baseline ADR and PDR as a quality indicator for colonoscopy in our region, where no internationally recommended colonoscopic screening programs have been implemented.

Conclusions We have noticed low PDR and ADR, which require further investigation and research. In addition, we believe there should be a different baseline ADR and PDR as a quality indicator for colonoscopy in our region, where no internationally recommended colonoscopic screening programs have been implemented. intubation rate, withdrawal time, quality of bowel preparation, and adenoma detection rate (ADR).
ADR is most frequently used quality indicator and is now designated as an outcome measure of colonoscopy; it is defined as the proportion of screening colonoscopies in patients ≥ 50 years, detecting at least one adenoma or adenocarcinoma, and should ideally be ≥ 25 %. There is compelling evidence to support an inverse correlation between ADR and interval CRC (cancer detected after a screening colonoscopy), which has the potential to lower future mortality from CRC [10]. This is supported by Corley et al, which states that for every 1 % increase in ADR, there is a 3 % predicted decrease in interval CRC (hazard ratio 0.97; 95 % Confidence Interval (CI), 0.96-0.98), and a 5 % decrease in risk of fatal interval CRC (hazard ration 0.95; 95 % CI, 0.94-0.97) [11]. Although the American Society of Gastrointestinal Endoscopy recommends that colonoscopists report their ADRs, current evidence suggests low-level detection, which endangers patients because effective polyp detection and resection help in CRC prevention [12]. Unfortunately, no standard CRC screening program exists in Pakistan, and no established measures have been taken to assess the quality of ADR measurement either.
Our study aimed to focus on and review the ADR of a tertiary care hospital in Pakistan, to provide insight into the ADR and quality of colonoscopy, and the factors that affect it, pertinent to this region of the world.

Patients and methods
We performed a retrospective observational study on patients aged ≥ 18 years who underwent colonoscopy at the Aga Khan University Hospital (AKUH), Karachi, between July 1, 2017 to June 30, 2018. AKUH is a 740-bed private hospital situated in Karachi and one of the largest tertiary care centers in Pakistan. Exemption was acquired from the Ethical Review Committee, and patient data were retrieved using the ICD-10 Coding System.
All colonoscopies were performed by gastroenterologists at AKUH. Patient preparation consisted of clear liquid diet for 24 hours prior to colonoscopy, and 45 mL of bowel preparation solution, given 6 hours apart. This solution was prepared at the AKUH Pharmacy and consisted of sodium phosphate monohydrate and sodium phosphate heptahydrate with preservatives. Patients were consciously sedated by giving 2 to 5 mg midazolam and 2 to 3 mg intravenous nalbuphine. Bowel preparation was classified into good, suboptimal/reasonable, and poor, on the basis of the Boston Bowel Preparation Scale (BBPS), which is a reliable measure of bowel preparation [13], although no scoring system was assigned. All colonoscopies at AKUH were performed using the OLYMPUS manufactured EVIS EXERA III video colonoscopes [CF-H190 L/I (Olympus Corp., Europe) and CF-HQ190 L/I (Olympus Corp., United States)]. Abnormal findings detected during colonoscopy were biopsied for further evaluation. Any and all polyps found were removed and biopsied for histopathology.
A predesigned proforma was used to collect variables such as age, gender, indication of colonoscopy, bowel preparation, colonoscopy findings, and histopathology reports. Patients who underwent sigmoidoscopy only were known cases of familial adenomatous polyposis, or had incomplete data were excluded.

Results
In addition, we classified endoscopists based on the number of years of experience; 13 endoscopists had been in practice for ≤ 10 years and 10 had > 10 years of experience. Endoscopists in practice for ≤ 10 years performed 43.5 % of the colonoscopies (863) while those with > 10 years' experience in the field performed the remaining 56.5 % (1122). The PDR and ADR were found to be significantly higher for endoscopists in practice for ≤ 10 years as compared to those with > 10 years of experience (PDR: 20.6 % versus 15.8 %, P = 0.005; ADR: 11.7 % versus 8.6 %, P = 0.02).
These results are summarized in ▶ Table 2.

Discussion
Our focused study aimed to provide insight into the quality of colonoscopies performed in a part of the world where no routine colonoscopy screening program is available. We report a PDR and ADR of 17.9 % and 9.9 %, respectively. Our PDR seems to be lower compared to Western populations, as demonstrated by Cooper et al., which reported a PDR of 23.9 % to 35.7 % [14]. This variation might suggest a lower population incidence of polyps or is a result of poor practices due to lack of a stringent criteria to follow QI in colonoscopy, as well as poor knowledge about the importance of these validated QI. Our lower PDR is supported by regional studies from Rehman et al. and Saleh et al., which report a PDR of 11.3 % (57/505), and 7.9 % (28/354), respectively [15,16]. However, certain limitations such as a smaller sample size, and sub-standard cecal intubation rate of Rehman et al., might have contributed to missed lesions and overlooked positive detection within samples. Furthermore, no reports of ADR were present in either article, preventing us from conclusively inferring on the PDR and ADR of our population.
In addition, the lower ADR and PDR of our population may be due to a younger presenting age of patients, i. e. 47.8 ± 16.2 years. Although this supports decreasing the minimum recommended age of colonoscopy screening from 50 to 45 [17], it is lower than the age after which most people undergo screening colonoscopy for CRC [18]; this can contribute to missed diagnoses within our broad population. Both ADR and PDR were significantly higher in our patients ≥ 50 years (P < 0.001), supporting that increasing age is a predictor of adenoma at colonoscopy [19].
Our study does not report a significant predominance of polyps based on gender (P = 0.378), contradicting reports from Cooper et al. which showed that PDR was higher in males (P < 0.0001). Lee and colleagues from the United Kingdom found their ADR to be 46.5 %, which was similarly increased in the elderly (age > 65) (P < 0.001), but comparatively higher in men (52.9 %) than in women (36.5 %) (P < 0.001) [20], signifying the difference in results from our population. We are unable to conclude any biological plausibility for this difference in gender, warranting a more detailed look into the subjects themselves.
Another factor that affects the quality of colonoscopy, hence the ADR, is bowel preparation; it has been reported that approximately 20 % to 25 % of all colonoscopies are in patients who have poor or inadequate bowel preparation, leading to multiple adverse events, including a lower ADR [21,22]. While 94.4 % of our colonoscopy preparations were good, the remaining 5.6 % were either suboptimal or poor, as result of decreased patient compliance, failure to comprehend and follow through with the instructions provided. It is interesting to note, however, that a higher ADR (P = 0.014) and PDR (25.7 %; P = 0.007) were found for suboptimal bowel preparation. This association has been found in only a handful of other studies, and multiple reasons have been hypothesized for an explanation; residual stool in a suboptimal bowel preparation may attach to mucus caps of serrated polyps, allowing for better visualization. Additional washing by the endoscopist results in a higher attention ▶ to mucosa, subsequently increasing incidental PDR. Moreover, an excellent preparation may falsely increase confidence of the endoscopist, resulting a decreased quality of inspection [23][24][25]. Multiple previous studies have documented an association of higher PDR and ADR with greater experience of endoscopists. Pace et al. reported increased rates of polyp and adenoma detection with high annual case volumes (> 530) (P < 0.001) [26], while another study found more experienced endoscopists were able to detect a higher number of smallersized polyps (< 3 mm), as well as adenomas with advanced histology (P < 0.0001) [27]. Hence, the most surprising difference is that our study showed that endoscopists with experience performing < 500 colonoscopies, had a statistically significant higher PDR (21.6 %; P = 0.02) and ADR (14.4 %; P = 0.049) as compared to those with experience with > 500 procedures, corresponding to a significantly higher PDR (20.6 %; P = 0.005) and ADR (11.7 %; P = 0.02) for endoscopists in practice for ≤ 10 years. This disparity may be attributed to a higher-volume patient load and efficiency demands for more experienced endoscopists, resulting in a shorter withdrawal time and less meticu-lous examination [28]. Furthermore, endoscopists with less experience are expected to perform a more extensive examination during their training and practice, and hence, they have a greater incidental finding rate. Endoscopist fatigue also should be taken into consideration, since a significant association has been documented between progress of the day/endoscopy shift and reduced PDR [29][30][31]. As there is contradictory evidence for this postulation [32,33], further investigations to define, measure, and identify factors related to endoscopist fatigue are greatly needed.
Our study has several limitations. Because it was a singlecenter study, the results are limited by external validity. In addition, no numerical or objective documentation about bowel preparation on the BBPS was performed; thus, we recommend modifying regional institutional practices to include such an objective outcome when assessing quality of bowel preparation. We were also unable to quantify the number of continuing-medical-education (CME) meetings attended by our endoscopists. These hands-on educational sessions can increase understanding of polyp morphology and examination techniques, which subsequently results in better colonoscopy performance ▶ with a higher ADR. This is supported by a report by Adler et al., which showed that the number of CME meetings attended (P = 0.012) as well as colonoscopy scope generation (P = 0.001) accounted for approximately 40 % of the inter-physician variability for ADR [34]. We consider the generation of instruments used as a strength of our study because the latest generation of wide-angle, high-definition colonoscopes can improve ADR by 22 %, as compared with mixed, older endoscopes [35].

Conclusions
In summary, we report low PDR and ADR, although multifactorial causes may be implicated as discussed above. We strongly urge implementation of a regional screening colonoscopy program and notification of endoscopists about their ADRs and their importance as a quality indicator for colonoscopy. Although our data can be used to provide a baseline for comparison by other regional endoscopists, future multicenter, prospective studies need to be conducted to generate conclusive evidence and establish a baseline PDR and ADR. Further research must be undertaken to evaluate other quality indicators, as a step towards improvement of the overall quality of colonoscopies performed.