Abstract
Background
Adenoma detection rate (ADR) and sessile serrated polyp detection rate (SSPDR) data in surveillance colonoscopy are limited.
Aims
Our aim was to determine surveillance ADR and SSPDR and identify associated predictors.
Methods
A retrospective review of subjects who underwent surveillance colonoscopy for adenoma and/or SSP at an academic center was performed. The following exclusion criteria were applied: prior colonoscopy ≤ 3 years, incomplete examination, or another indication for colonoscopy. Patient, endoscopist, and procedure characteristics were collected. Predictors were identified using multivariable logistic regression.
Results
Of 3807 colonoscopies, 2416 met inclusion criteria. Surveillance ADR was 49% and, SSPDR was 8%. Higher ADR was associated with: age per year (OR 1.03; 95% CI 1.02–1.04), male gender (OR 1.55; 95% CI 1.29–1.88), BMI per kg/m2 (OR 1.02; 95% CI 1.01–1.04), withdrawal time per minute (OR 1.09; 95% CI 1.07–1.10), and endoscopists’ screening ADR (OR 1.01; 95% CI 1.00–1.03). Years since training (OR 0.99; 95% CI 0.98–0.99) was associated with lower ADR. Family history of CRC (OR 1.58; 95% CI 1.02–2.27) and endoscopists’ screening ADR (OR 1.40; 95% CI 1.15–1.74) were associated with higher SSPDR. African-American race (OR 0.36; 95% CI 0.10–0.75) and diabetes (OR 0.41; 95% CI 0.21–0.76) were associated with lower SSPDR.
Conclusions
For surveillance colonoscopy, nearly half of patients had an adenoma and one in twelve had an SSP. In addition to established factors, BMI, endoscopists’ screening ADR, and years since training were associated with ADR, whereas African-American race and diabetes were inversely associated with SSPDR. Further studies are needed prior to integrating surveillance ADR and SSPDR into quality metrics.
Keywords: Detection rates, Colonoscopy, Quality indicators
Introduction
Colorectal cancer (CRC) remains the third leading cause of cancer-related deaths in the USA [1]. Among the available screening options, colonoscopy is the only modality that has both diagnostic and therapeutic potential, allowing for the reduction in CRC risk by identifying and removing premalignant lesions. However, variation in the quality of colonoscopies performed undoubtedly impacts the efficacy of the examination [2–6].
In the past decade, several procedural factors including adenoma detection rate (ADR), cecal intubation, withdrawal time, and bowel preparation quality have been studied in order to provide benchmarks for a quality screening examination. ADR, defined as the proportion of patients undergoing screening colonoscopy with a finding of at least one adenoma, has been shown to be an independent predictor of the risk of interval CRC after screening [7] and is recognized as a priority quality indicator by all national gastroenterology societies. The most recent benchmark for screening ADR is an average of 25% (women 20% and men 30%) [2]. Though there is currently no benchmark for sessile serrated polyp detection rate (SSPDR), prior studies have found varying rates, reporting up to 18% in screening examinations and up to 15% in surveillance examinations [8–10].
Surveillance colonoscopies account for 20–32% of the total US colonoscopy volume [11]. In an effort to improve the quality of surveillance colonoscopies that are performed, the principle of ADR and SSPDR should be applied to surveillance examinations. However, there are limited and variable data on surveillance ADR and SSPDR or factors that impact these rates [8, 12–14]. Therefore, the purpose of this study was to determine ADR and SSPDR in surveillance colonoscopy and to identify associated patient, endoscopist, and procedural predictors. We hypothesized that ADR and SSPDR would be greater in surveillance colonoscopies as compared to screening colonoscopies.
Methods
Data Collection
This retrospective study was approved by the University of Michigan Institutional Review Board. Using ProVation, MD® we identified all patients who underwent surveillance colonoscopy at the University of Michigan for a history of polyps between January 1, 2014, and September 15, 2015. Patients 40–85 years old with at least one confirmed adenoma and/or sessile serrated polyp (SSP) on prior pathology were included. The following exclusion criteria were applied: colonoscopy for an indication other than surveillance of polyps, a prior colonoscopy within 3 years, incomplete examination, missing pathology, or a personal history of inflammatory bowel disease or CRC. Colonoscopies with missing prior pathology were excluded given the difficulty in assessing for risk factors with unknown polyp history. Only colonoscopies performed by gastroenterologists were included in this study.
Patient, endoscopist, and procedure characteristics were collected. Patient characteristics included demographic data (age, gender, race), body mass index (BMI), smoking status, family history of CRC, and whether or not the patient had a diagnosis of diabetes. Endoscopist characteristics included gender, screening ADR, and number of years in practice. Procedure details consisted of fellow participation, time of colonoscopy (morning or afternoon), bowel preparation quality (based on either the Aronchick Scale or Boston Bowel Preparation Scale (BBPS)), difficulty of procedure, and withdrawal time without polyp removal. Difficulty of procedure is subjectively determined by the performing endoscopist and recorded on all endoscopies performed at our institution. Optimal bowel preparation quality was defined as either BBPS rating of > 2 for all colon segments, Aronchick Scale rating of “excellent,” “good,” and/or where listed as “adequate” on the endoscopy report. Polyp data on the colonoscopy included size (based on estimation provided in endoscopists’ report), location, number, and pathology. Polyps were defined as nonadvanced if < 10 mm and advanced if ≥ 10 mm in size, and presence of mass with pathology indicating cancer. Data were collected by five study members (JM, KJ, DR, CJ, SM).
Statistical Analysis
The primary outcomes were the ADR and SSPDR for surveillance colonoscopy. ADR and SSPDR were defined as the number of subjects in whom at least one adenoma or SSP was identified, each divided by the number of surveillance colonoscopies performed, respectively. Descriptive statistics were obtained for all baseline patient, endoscopist, and procedure characteristics. Chi-square and Student’s t-tests were used to determine whether differences in baseline variables exist between subjects with and without adenomas and SSPs. Random effects multivariable logistic regression models were used to account for the correlated nature of colonoscopies performed by the same endoscopist and provide final estimates of the association between predictors and adenoma and SSP detection by controlling for differences in endoscopists’ number of procedures performed and screening ADRs. All variables that were significant in bivariate analysis (defined by p value< 0.05) were included in the model. Colonoscopies with missing values for any of the relevant variables were removed from the regression analysis. Continuous predictors were mean centered and standardized during the regression procedure. Statistical tests were performed using the statistical software SAS version 9.4 (SAS Institute Inc., Cary, North Carolina) and R (R Foundation for Statistical Computing, Vienna, Austria) version 3.3.2.
Results
Patient Characteristics
A total of 3807 patients who underwent surveillance colonoscopy from January 1, 2014, to September 15, 2015, were reviewed. Of these, 2416 met inclusion criteria and were included in the study. Mean age was 63 years (± 8), and 85% of patients were Caucasian. Mean BMI was 30 kg/m2 (± 6). A total of 418 (17%) patients had a history of diabetes, and 1157 (48%) were smokers (Table 1). Additional patient characteristics based on findings of adenomas and SSPs are listed in Table 2. On prior colonoscopies, 2141 (89%) patients had a history of adenomas, 149 (6%) had SSPs, and 126 (5%) had both adenomas and SSPs.
Table 1.
Overall patient (N = 2416), endoscopist (N = 67), and procedure characteristics
| Patient/procedure features | N (%) |
|---|---|
| Patient characteristics | |
| Age in years, mean (SD) | 62.8 (8.1) |
| Male | 1410 (58.4) |
| White | 2060 (85.3) |
| BMI, mean (SD) | 29.5 (6.0) |
| Diabetes mellitus | 418 (17.3) |
| Smoker (past and present) | 1157 (47.9) |
| Endoscopist characteristics | |
| Male | 42 (60.8) |
| Years since training, mean (SD) | 12.5 (9.4) |
| Screening ADR, mean (SD) | 31.4 (9.1) |
| Withdrawal time, mean (SD) | 14 min 43 s (9 min 57 s) |
| Procedure characteristics | |
| Fellow participation | 207 (8.6) |
| No difficulty | 2048 (95.4) |
| Afternoon colonoscopy | 978 (40.4) |
| Optimal bowel preparation | 2126 (88.0) |
SD standard deviation, BMI body mass index in mg/kg2, ADR adenoma detection rate
Table 2.
Patient characteristics by presence of adenoma or sessile serrated polyp (SSP)
| Adenoma | SSP | |||||
|---|---|---|---|---|---|---|
|
|
|
|||||
| Yes* (N = 1174) | No* (N = 1242) | p value | Yes* (N = 190) | No* (N = 2226) | p value | |
| Patient characteristics | ||||||
| Age, year (SD) | 63.6 (8.1) | 62.1 (8.0) | < 0.0001 | 61.4 (7.8) | 63.1 (8.1) | 0.01 |
| Gender (%) | ||||||
| Male | 758 (64.6) | 652 (52.5) | < 0.0001 | 116 (61.0) | 1205 (54.1) | 0.06 |
| Female | 416 (35.4) | 590 (47.5) | 74 (38.9) | 1019 (45.8) | ||
| Race/ethnicity | ||||||
| Caucasian | 1014 (86.4) | 1046 (84.2) | 0.58 | 179 (94.2) | 1881 (84.5) | 0.0006 |
| African-American | 63 (5.4) | 89 (7.2) | 4 (2.1) | 130 (5.8) | ||
| Other** | 73 (6.2) | 84 (6.8) | 4 (2.1) | 175 (7.9) | ||
| BMI, kg/m2 (SD) | 30.0 (6.3) | 29.0 (5.7) | 0.0005 | 29.9 (6.2) | 29.4 (6.0) | 0.36 |
| Smoker (%) | 596 (50.8) | 561 (45.2) | 0.003 | 81 (42.6.) | 1076 (48.3) | 0.13 |
| Diabetic (%) | 233 (19.8) | 185 (14.9) | 0.001 | 20 (10.5) | 398 (17.9) | 0.01 |
| FH of CRC (%) | 150 (12.8) | 168 (13.5) | 0.66 | 37 (19.5) | 281 (12.6) | 0.007 |
| Years since prior colonoscopy (SD) | 5.1 (2.1) | 5.3 (1.9) | 0.05 | 5.5 (2.2) | 5.2 (2.0) | 0.05 |
| Procedure characteristics | ||||||
| Fellow participation | 106 (9.0) | 101 (8.1) | 0.47 | 16 (8.4) | 191 (8.6) | 0.92 |
| Difficulty | 132 (11.2) | 172 (13.8) | 0.06 | 22 (11.6) | 282 (12.7) | 0.64 |
| Afternoon colonoscopy | 483 (41.1) | 495 (39.9) | 0.49 | 76 (40.0) | 902 (40.5) | 0.88 |
| Optimal bowel prep | 1047 (89.2) | 1079 (86.9) | 0.14 | 167 (87.9) | 1959 (88.0) | 0.74 |
| Withdrawal time, minutes, mean (SD) | 20.8 (11.8) | 11.6 (7.1) | < 0.0001 | 24.9 (13.7) | 14.2 (9.4) | < 0.0001 |
| Endoscopist characteristics | ||||||
| Male gender | 643 (54.8) | 678 (54.6) | 0.98 | 115 (60.5) | 1200 (53.9) | 0.06 |
| Years since training, mean (SD) | 11.8 (9.3) | 13.0 (9.5) | 0.003 | 11.6 (9.8) | 12.5 (9.4) | 0.17 |
| Screening ADR, mean (SD) | 32.3 (9.2) | 30.6 (8.9) | < 0.0001 | 34.6 (8.5) | 31.1 (9.1) | < 0.0001 |
SD standard deviation, BMI body mass index, FH family history, CRC colorectal cancer
Numbers may not equal 100% due to missing values
Other = Listed in chart as Asian-American/Pacific Islander, American Indian or Alaskan Native, or Other
Endoscopist Characteristics
Surveillance colonoscopies were performed by 67 gastroenterologists who had been practicing an average of 12.5 years following completion of fellowship. A total of 42 (61%) endoscopists were male. The endoscopists’ overall mean screening ADR was 31.4% (Table 1).
Procedure Characteristics
All procedures were performed by gastroenterologists at the University of Michigan. A gastroenterology fellow was present in 207 (9%) of the procedures. A total of 978 (40%) colonoscopies were performed in the afternoon. Bowel preparation was considered optimal in 2126 (88%) of the colonoscopies, and 2048 (85%) of the procedures were performed without difficulty. The mean withdrawal time without polyp removal was 12 min, 18 s (± 7 min, 18 s) and with polyp removal was 14 min, 43 s (± 9 min, 57 s) (Table 1).
Surveillance Adenoma Detection Rates
Adenomas were found in 1174 patients for an overall surveillance ADR of 49% (men 65%, women 35%). Assuming a sex-balanced population, the normalized ADR was 48%. Nonadvanced adenomas were found in 45% (1099/2416) of patients undergoing surveillance colonoscopy. Advanced adenomas were found in 6% (145/2416). Adenomas were found in the following distribution based on colon segment: ascending 29% (505/1717), transverse 24% (408/1717), cecum 15% (266/1717), descending 13% (224/1717), sigmoid 13% (219/1717), and rectum 6% (95/1717).
Multivariable analysis was performed to determine patient, endoscopist, and procedure factors associated with ADR. Patient factors associated with higher ADR include: (1) age per year [odds ratio (OR) 1.03; 95% confidence interval (CI) 1.02–1.04], (2) male gender (OR 1.55; 95% CI 1.29–1.88), and (3) BMI per kg/m2 (OR 1.02; 95% CI 1.01–1.04). Endoscopist factors associated with higher ADR include: (1) screening ADR (by percentage point) (OR 1.01; 95% CI 1.00–1.03) and (2) withdrawal time per minute (OR 1.09; 95% CI 1.08–1.12). Endoscopists’ years since training (per year) was associated with lower surveillance ADR (OR 0.99; 95% CI 0.98–0.99) (Table 3).
Table 3.
Factors associated with adenoma detection rate (ADR)
| OR | 95% CI | p value | |
|---|---|---|---|
| Patient characteristics | |||
| Age | 1.03 | 1.02–1.04 | < 0.001 |
| Male gender | 1.55 | 1.29–1.88 | < 0.001 |
| African-American race | 0.75 | 0.51–1.09 | 0.13 |
| BMI | 1.02 | 1.01–1.04 | 0.01 |
| Family history of CRC | 0.99 | 0.76–1.30 | 0.96 |
| Diabetes | 1.29 | 1.00–1.66 | 0.05 |
| Endoscopist characteristics | |||
| Years since training | 0.99 | 0.98–0.99 | 0.04 |
| Screening ADR | 1.01 | 1.00–1.03 | 0.03 |
| Procedure characteristics | |||
| Afternoon colonoscopy | 1.11 | 0.92–1.34 | 0.29 |
| Withdrawal time (in min) | 1.09 | 1.07–1.10 | < 0.001 |
OR odds ratio, CI confidence interval, BMI body mass index in mg/kg2, CRC colorectal cancer
Surveillance Sessile Serrated Polyp Detection Rates
SSPs were found in 190 patients for an overall SSPDR of 8% (190/2416). Of these, 52 (27%) had SSPs on their prior colonoscopies. On the current surveillance colonoscopy of interest, nonadvanced and advanced SSPs were found in 6% (152/2416) and 2% (53/2416) of the surveillance cohort, respectively. SSPs were found in the following distribution based on colon segment: ascending 35% (79/224), transverse 21% (46/224), cecum 17% (37/224), sigmoid 13% (28/224), descending 11% (25/224), and rectum 4% (9/224).
African-American race (OR 0.36; 95% CI 0.10–0.75) and diabetes (OR 0.41; 95% CI 0.21–0.72) were associated with lower SSPDR. Family history of CRC (OR 1.58; 95% CI 1.02–2.27) and endoscopists’ screening ADR (OR 1.40; 95% CI 1.15–1.74) were associated with higher SSPDR (Table 4). Withdrawal time was also associated with higher SSPDR though it did not reach statistical significance (OR 1.14; 95% CI 0.96–1.27). Age, male gender, and BMI were not significantly associated with SSPDR.
Table 4.
Factors associated with sessile serrated polyp detection rate (SSPDR)
| OR | 95% CI | p value | |
|---|---|---|---|
| Patient characteristics | |||
| Age | 0.87 | 0.73–1.03 | 0.09 |
| Male gender | 0.91 | 0.67–1.28 | 0.61 |
| African-American race | 0.36 | 0.10–0.75 | 0.05 |
| BMI | 1.16 | 0.98–1.36 | 0.07 |
| Diabetes | 0.41 | 0.21–0.72 | < 0.001 |
| Family history of CRC | 1.58 | 1.02–2.27 | 0.03 |
| Endoscopist characteristics | |||
| Screening ADR | 1.40 | 1.15–1.74 | < 0.001 |
| Procedure characteristic | |||
| Withdrawal time (in min) | 1.14 | 0.96–1.27 | 0.02 |
OR odds ratio, CI confidence interval, BMI body mass index in mg/kg2, CRC colorectal cancer
Colorectal Cancer Rates
Interval colon cancer was found in five cases for a 0.2% prevalence in our cohort. The locations of the adenocarcinomas were the following: ascending (2), transverse (2), and rectum (1). Two patients presented with large masses, two presented with sessile polyps 25–35 mm in size, and one with an 8-mm pedunculated polyp. The mean number of years of prior colonoscopy for these cases was 5.2 years (range 3–8 years) with two cases having had a colonoscopy 3 years prior.
Discussion
Based on data from a large tertiary care center, the surveillance ADR and SSPDR in our study were found to be 49 and 8%, respectively. Adenomas and SSPs were more likely to be found in the proximal colon compared to the distal colon. Factors associated with a higher ADR include increasing patient age and BMI, male gender, endoscopists’ screening ADR, and withdrawal time, while increasing endoscopists’ years since training was associated with lower ADR. Family history of CRC and screening ADR were associated with a higher SSPDR, while diabetes and African-American race were associated with lower SSPDR.
Previous studies have also reported a higher ADR in those with a personal history of polyps compared to the average-risk ADR for screening colonoscopies [8, 13]. However, the surveillance ADR in our study was greater than previously reported in a single tertiary center by Sanaka et al. who found an ADR of 33% [13]. This difference may be due to the fact that only those with a confirmed history of adenoma, SSP, or both were included in our study, whereas those with a history of non-neoplastic polyps (i.e., hyperplastic polyps) were included in the study by Sanaka et al. Anderson and colleagues previously investigated SSPDR in those undergoing colonoscopy for screening as compared to surveillance purposes. The authors found a surveillance SSPDR of 10%, which is in the range of that found in our cohort (8%) [15]. A more recent multicenter study by Anderson and colleagues investigated proximal colon SSPDR for surveillance colonoscopy and found that among endoscopists with > 35% ADRs, median proximal SSPDR was 14.7% [10]. Our data are congruent as we also found that greater endoscopists’ screening ADR is associated with greater SSPDR.
Several prior studies have investigated the impact of patient and procedural factors on ADR and SSPDR though they comprised a mix of screening and surveillance colonoscopies with several also including diagnostic examination and high-risk patients. Age, male gender, and diabetes are all associated with increased overall ADR [4, 11, 13, 14, 16–20]. In addition, a withdrawal time of 6 min or greater is associated with a higher ADR [3, 21, 22]. Similarly, in our surveillance cohort, we also found that increasing age and male gender were significantly associated with higher ADR. For example, when controlling for other covariates, a 60-year-old patient is, on average, 31% more likely than a 50-year-old to have an adenoma discovered on examination (OR 1.31). In our cohort, diabetes was also associated with higher ADR though it did not reach statistical significance (OR 1.29; p = 0.05). Fellow participation occurred in 9% of our cohort, but did not have significantly increased surveillance ADR relative to other screening ADR studies [23–25].
In contrast to Anderson et al. [26], who found that diabetes may be a risk factor for sessile serrated adenomas, we found diabetes to be protective against SSPs. Even though our SSPDR was not congruent with Anderson et al., our cohort of patients with SSPs was larger with diabetes remaining significant when considering other covariates; therefore, this may reflect a more accurate association though further studies are required. In addition, BMI was found to be associated with both ADR and SSPDR. For example, a patient with a BMI of 30 is 20% more likely than a patient with a BMI of 22 to have an adenoma on examination (OR 1.20). Similarly, a patient with a BMI 30 is 15% more likely to have an SSP on examination as compared to a patient with a BMI of 22. Finally, prior studies regarding race have shown a general trend toward lower risk of SSPs among African-Americans though findings have been limited due to low enrollment of non-White patients [27]. A total of 7% (156/2416) of our study cohort was African-American and when adjusting for covariates, we found that African-American race was in fact protective against SSPs (OR 0.36; 95% CI 0.10–0.75). The etiology for this protective effect is unknown though it may be related to genetic, dietary, or environmental exposures that may influence SSP development.
Similar to prior studies, greater withdrawal time was associated with both higher ADR and SSPDR, though the latter did not reach statistical significance. When controlling for patient characteristics, an endoscopist is 97% more likely to discover an adenoma when withdrawal time is 14 min as compared to 6 min (OR 1.97). Similarly, an endoscopist is 52% more likely to discover an SSP on examination when withdrawal time is 14 min rather than 6 min, when controlling for patient characteristics (OR 1.52). This data support existing evidence that careful inspection is an essential component of surveillance colonoscopies [3].
Our study differs from prior studies in that we specifically investigated ADR and SSPDR in surveillance colonoscopies alone and not only studied patient and procedure characteristics, but also investigated the impact of endoscopist factors on these rates. This led to the finding that endoscopists’ screening ADRs were associated with a higher surveillance ADR and SSPDR, which is particularly important from a quality indicator standpoint given the increased risk of CRC in the setting of adenomas and SSPs and further supports benchmark goals for these rates.
Our study has several strengths including that the data were collected from a large tertiary center, and unlike prior studies, all colonoscopies were performed by gastroenterologists. In addition, fellow participation was low (9% of procedures) and confirmed to have no impact on adenoma or SSP detection rates, which minimizes the chance that fellow participation may be a potential confounder for increased polyp detection rates [28]. Finally, all surveillance colonoscopies had confirmed existing adenoma or SSP based on pathology reports.
Limitations of this study include its single center, retrospective study design. Patient characteristics (i.e., family history, smoking status, and diabetes history) were based on details recorded in electronic health records, which may not always be complete. In addition, prior colonoscopy details were based on those performed and available at our site only. Any patients that did not have prior pathology available were excluded from the study. It is possible that these excluded patients may have had prior colonoscopies with adenomas and/or SSPs outside of our institution and inclusion of these patients’ colonoscopy findings may result in fluctuation of ADR and SSPDR. Finally, potential exclusion of unknown patient, endoscopist, and procedure factors is possible in this retrospective chart review.
Conclusions
This study is a comprehensive review of surveillance colonoscopies performed by gastroenterologists to determine both ADR and SSPDR. No prior studies, to our knowledge, have investigated patient, endoscopist, and procedure factors concurrently to see how these may impact ADR and SSPDR. In addition, most prior studies have investigated ADR and SSPDR among screening colonoscopies. Future confirmatory studies are needed as surveillance colonoscopy accounts for a significant proportion of colonoscopies performed annually. When assessing the quality of surveillance colonoscopy, endoscopists’ surveillance ADR and SSPDR will need to be incorporated into future quality measures.
Abbreviations
- ADR
Adenoma detection rate
- BMI
Body mass index
- CI
Confidence interval
- CRC
Colorectal cancer
- FH
Family history
- OR
Odds ratio
- SD
Standard deviation
- SSP
Sessile serrated polyp
- SSPDR
Sessile serrated polyp detection rate
- US
United States
Footnotes
Author’s contribution Stacy Menees, Joseph Dickens, and Jennifer Maratt had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. SM was involved in study concept and design. SM, JD, JM, DR, CE, and KJ were involved in acquisition, analysis, or interpretation of data. JM, JD, and SM were involved in drafting of the manuscript. All authors were involved in critical revision of the manuscript for important intellectual content. JD, SM, JM, and KJ were involved in statistical analysis. SM was involved in study supervision.
Compliance with ethical standards
Conflict of interest Grace Elta has been a consultant for Olympus Medical. Philip Schoenfeld has been a consultant, a member of the advisory board, and on the speaker bureau for Ironwood Pharmaceuticals, Allergan Pharmaceuticals, Salix Pharmaceuticals, and a consultant and member of the advisory board for Synergy Pharmaceuticals. All other authors have no conflicts of interest to report.
Ethical Approval All procedures performed in this study involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. For this retrospective study, formal consent was not required. This article does not contain any studies with animals performed by any of the authors.
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