Introduction
Screening colonoscopies can detect and remove polyps [1], and polypectomy during a colonoscopy has been shown to decrease colorectal cancer
incidence [2]. The adenoma detection rate (ADR) is a recognized quality indicator for colonoscopy
[3]. Multiple studies have assessed colonoscopic practice with ADR and found that higher
ADRs were inversely associated with risk of interval colorectal cancer [4]
[5]
[6]. However, there is substantial variability in ADR among endoscopists [7]. One previous study reported that ADR may be insufficient to identify the quality
of a colonoscopy, because an endoscopist may be less inclined to identify and remove
polyps once a single adenoma has been detected [8]. Therefore, two novel quality indicators have been proposed: adenomas per colonoscopy
(APC), and adenomas per positive participant (APP) [8]. One recently published meta-analysis of 43 publications with 15,000 colonoscopies
found that APC and APP were independently associated with adenoma miss rate [9]. However, only one previous study investigated the correlation of APC and APP with
ADR, finding APC strongly correlated with ADR (r = 0.94, P < 0.01), and APP weakly correlated with ADR (r = 0.36, P < 0.36) [10].
Our primary aim was to investigate the correlation of APC and APP with ADR in a large
US screening colonoscopy practice and to elucidate patient-level, endoscopist-level
and procedure factors associated with APC, APP, and ADR.
Patients and methods
Study population and data description
We collected information on all colonoscopy examinations performed within five ambulatory
endoscopy centers (AEC) that were part of a community-based single specialty gastroenterology
practice in the Twin Cities of Minnesota (MNGi Digestive Health) over a 5-year period,
from January 2008 to December 2012. Only complete screening colonoscopies performed
in average-risk individuals 50 years and older were included in this study.
All colonoscopies were performed during 30-minute time slots by endoscopists using
standard bowel preparation with one of several oral lavage regimens. Most procedures
(98 %) were performed using moderate conscious sedation with midazolam and fentanyl.
Endoscopists were not aware of the specific study hypothesis, but all partners had
previously signed a partnership agreement that includes an acknowledgement that results
of their procedures will be monitored for quality purposes and potentially published
without individual attribution. The study was approved by the University of Minnesota
institutional review board.
We identified all procedure reports with the term “screening” in the indications field
(from a drop-down menu), in addition to a detailed algorithm that uses text word search
for all words resembling “screening” or its synonyms that could have been entered
as free text in the indication field [7]. We extracted information on quality of preparation (defined as adequate, including
descriptions of “good,” “excellent,” or “fair”; or inadequate, including descriptions
of “poor”), completeness of procedure, whether polyps were removed and their size,
conscious sedation administered (type and doses) and withdrawal time (defined as time
from reaching the cecum to removal of colonoscope from anal verge). Withdrawal time
was calculated as average of exams where no polyps were removed per provider. Colonoscopy
was defined as “complete” if cecal landmarks were reached and documented. Endoscopist
age was calculated at the time of their first colonoscopy included in the study.
Definition of quality parameters
Adenoma was defined per WHO criteria, as any premalignant lesion that was tubular,
villous, or tubulovillous histology or with low- or high-grade intraepthelial neoplasia.
APC was defined as the number of detected adenomas divided by the total number of
screening colonoscopies.
APP was defined as the number of detected adenomas divided by the number of screening
colonoscopies in which one or more adenomas are detected.
ADR was defined as the number of screening colonoscopies in which one or more adenomas
are detected, divided by the total number of screening colonoscopies.
We excluded colonoscopies with missing information about polyp detection. Hyperplastic
polyps were excluded.
Statistical Analysis
We restricted the analysis to the 60 endoscopists who had performed at least 100 screening
colonoscopies during the study period with adequate preparation. An average of 1703
colonoscopies per endoscopist were performed during the time period (median 1700).
Patients and endoscopists characteristics are described as percentages for categorical
variables or means with standard deviations (SD) for continuous variables. Because
of the small number of female endoscopists for the years selected, we could not perform
analysis by physician gender.
For our primary aim, we generated scatter plots and performed spearman correlation
analysis for the correlation of APC, APP with ADR. We divided endoscopists into two
groups (ADR ≥ 25 %, or ADR < 25 %), and divided APC, and APP into four groups based
on their quartiles. Then we assessed how many endoscopists with the lowest quartile
of APC, or APP had an ADR ≥ 25 %. For our second aim, we divided APC, and APP into
two groups based on their median, and divided ADR at the cut point of 25 %. We used
unadjusted and adjusted hierarchical logistic regression to assess the association
of patient-level (continuous age, gender: female/male), endoscopist-level (continuous
age), and procedure factor (withdrawal time: < 6 mins/≥ 6 mins) with APC, APP and
ADR. All the analyses were performed using Stata/IC software, version 15.1. All statistical
tests were two-sided with P < 0.05 regarded as statistically significant.
Results
Over 5 years, a total of 80,915 complete screening colonoscopy examinations were performed
in the 5 AEC’s by 60 gastroenterologists. The median (Q1-Q3) APC, APP, and ADR were
0.41 (0.36 – 0.53), 1.33 (1.23 – 1.40), and 0.32 (0.28 – 0.38), respectively. Demographic
data and clinical characteristics for patients and endoscopists are presented in [Table 1]. Younger endoscopists were more likely to have higher APC, APP, and ADR. Endoscopists
with a longer withdrawal time had higher APC, APP, and ADR. Endoscopists with high
APP, ADR and APC were also more likely to be high detectors of sessile serrated adenomas
(detection rates for low vs. high APC, APP, and ADR were 5.1 % vs. 8.8 % (P < 0.001 ), 5.7 % vs. 7.9 % (P < 0.001 ), 3.5 % vs. 7.3 % (P < 0.001 ), respectively) and advanced adenomas (detection rates for low vs. high
APC APP, and ADR were 4.4 % vs. 7.4 % (P < 0.001), 5.1 % vs. 6.4 % (P < 0.001 ), and 3.0 % vs. 6.2 % (P < 0.001), respectively).
Table 1
Demographic data and clinical characteristics of patients and physicians.
|
Low APC
|
High APC
|
Low APP
|
High APP
|
Low ADR
|
High ADR
|
|
Variable[1]
|
(N = 44,692)
|
(N = 36,223)
|
(N = 40,402)
|
(N = 40,513)
|
(N = 11,372)
|
(N = 69,543)
|
|
Patients characteristics
|
|
Age, years ± SD
|
59.22 ± 8.70
|
59.29 ± 8.76
|
59.32 ± 8.75
|
59.19 ± 8.71
|
59.28 ± 8.72
|
59.24 ± 8.73
|
|
Men (%)
|
44.9 %
|
47.5 %
|
45.2 %
|
47.0 %
|
39.7 %
|
47.1 %
|
|
Physician characteristics
|
|
Age, years ± SD
|
52.11 ± 9.28
|
47.04 ± 9.41
|
51.11 ± 8.29
|
48.64 ± 10.73
|
57.73 ± 12.10
|
48.57 ± 8.54
|
|
Procedure Characteristics
|
|
Adequate preparation (%)
|
99.3 %
|
99.2 %
|
99.3 %
|
99.3 %
|
99.3 %
|
99.3 %
|
|
Withdrawal time, mins ± SD
|
9.19 ± 10.53
|
11.39 ± 10.96
|
9.13 ± 8.22
|
11.22 ± 12.75
|
9.50 ± 8.16
|
10.29 ± 11.15
|
|
Histology Type (%)
|
|
Sessile serrated adenoma
|
5.1 %
|
8.8 %
|
5.7 %
|
7.9 %
|
3.5 %
|
7.3 %
|
|
Advanced adenoma
|
4.4 %
|
7.4 %
|
5.1 %
|
6.4 %
|
3.0 %
|
6.2 %
|
|
Cancer
|
0.4 %
|
0.5 %
|
0.5 %
|
0.4 %
|
0.3 %
|
0.4 %
|
APC, adenomas per colonoscopy; APP, adenomas per positive participant; ADR, adenoma
detection rate; N, sample size
1 Continuous variables are represented as mean ± SD and categorical variable are represented
as percentage
Correlation of APC, and APP with ADR
The correlations of APC, and APP with ADR are shown in [Fig. 1] and [Fig. 2]. We found an excellent correlation of APC with ADR (r = 0.97, P < 0.001), and a moderate correlation of APP with ADR (r = 0.59, P < 0.01). The number of endoscopists with the lowest (quartile 1) and highest (quartile
4) APC and APP stratified by higher and lower ADR are shown in [Table 2]. About 47.6 % of endoscopist with the lowest APC had a higher ADR, and no endoscopists
with the highest APC had a lower ADR. About 74.3 % of endoscopists with the lowest
APP had a higher ADR, and about 5.6 % of endoscopists with the highest APP had a lower
ADR.
Fig. 1 Correlation of APC with ADR (r = 0.97, P < 0.001).
Fig. 2 Correlation of APP with ADR (r = 0.57, P < 0.01).
Table 2
Number of physicians with lowest quartile and highest quartile had lower and higher
ADR.
|
ADR
|
|
< 25 %
|
≥ 25 %
|
|
APC
|
|
Q1, N(%)
|
11,372 (52.4 %)
|
10,332 (47.6 %)
|
|
Q4, N %)
|
0 (0.0 %)
|
19,192 (100.0 %)
|
|
APP
|
|
Q1, N(%)
|
5,224 (25.7 %)
|
15,087 (74.3 %)
|
|
Q4, N(%)
|
1,104 (5.6 %)
|
18,459 (94.4 %)
|
APC, adenomas per colonoscopy; APP, adenomas per positive participant; ADR, adenoma
detection rate; Q1, highest quartile; Q4, lowest quartile; N, sample size.
Association of factors with APC, APP, and ADR
The unadjusted and adjusted association of patient-level, endoscopist-level, and procedure
factors with APC, APP, and ADR were presented in [Table 3], [Table 4], and [Table 5], respectively. Factors associated with higher APC after adjusting multivariable
including: older patients age (OR 1.003; 95 % CI 1.002 – 1.005), male patients (OR
1.123; 95 % CI 1.090 – 1.156), younger endoscopist age (OR 0.943; 95 % CI 0.941 – 0.945),
and longer withdrawal time (OR 3.434; 95 % CI 2.941 – 4.010). Factors associated with
higher APP after adjusting multivariable including: male patients (OR 1.059; 95 %
CI 1.039 – 1.099), younger endoscopist age (OR 0.972; 95 % CI 0.971 – 0.974), and
longer withdrawal time (OR 2.538; 95 % CI 2.218 – 2.902). Factors associated with
higher ADR after adjusting multivariable including: older patients age (OR 1.005;
95 % CI 1.002 – 1.007), male patients (OR 1.485; 95 % CI 1.421 – 1.553), younger endoscopist
age (OR 0.893; 95 % CI 0.891 – 0.895), and longer withdrawal time (OR 1.390; 95 %
CI 1.176 – 1.644).
Table 3
Unadjusted and adjusted[*] association of factors with adenoma per colonoscopy.
|
Low APC
|
High APC
|
Unadjusted
|
Adjusted
|
|
N
|
N
|
OR (95 % CI)
|
P value
|
OR (95 % CI)
|
P value
|
|
Patients characteristics
|
|
Age
|
44,692
|
36,223
|
1.000 (0.999, 1.003)
|
0.235
|
1.003 (1.002, 1.005)
|
< 0.001
|
|
Gender
|
|
Female
|
24,619
|
19,025
|
1.000 (ref)
|
|
1.000 (ref)
|
|
|
Male
|
20,072
|
17,196
|
1.108 (1.078, 1.140)
|
< 0.001
|
1.123 (1.090, 1.156)
|
< 0.001
|
|
Physicians characteristics
|
|
Age
|
44,692
|
35,319
|
0.944 (0.942, 0.945)
|
< 0.001
|
0.943 (0.941, 0.945)
|
< 0.001
|
|
Procedure characteristics
|
|
Withdrawal time
|
|
< 6 mins
|
863
|
248
|
1.000 (ref)
|
|
1.000 (ref)
|
|
|
≥ 6 mins
|
42,269
|
34,858
|
2.870 (2.490, 3.307)
|
< 0.001
|
3.434 (2.941, 4.010)
|
< 0.001
|
APC, adenomas per colonoscopy for each physician; N, sample size; OR, odds ratio;
CI, confidence interval.
* Adjusted logistic regression adjusted for patient age, patient gender, physician
age, and withdrawal time. The number of colonoscopies for adjusted multivariable is
77,357.
Table 4
Unadjusted and adjusted[*] association of factors with adenoma per positive colonoscopy.
|
Low APP
|
High APP
|
Unadjusted
|
Adjusted
|
|
N
|
N
|
OR (95 % CI)
|
P value
|
OR (95 % CI)
|
P value
|
|
Patients characteristics
|
|
Age
|
40,402
|
40,513
|
0.998 (0.997, 1.000)
|
0.036
|
1.000 (0.998, 1.001)
|
0.760
|
|
Gender
|
|
Female
|
22,160
|
21,484
|
1.000 (ref)
|
|
1.000 (ref)
|
|
|
Male
|
18,241
|
19,027
|
1.076 (1.047, 1.106)
|
< 0.001
|
1.069 (1.039, 1.099)
|
< 0.001
|
|
Physician characteristics
|
|
Age
|
39,912
|
40,099
|
0.974 (0.972, 0.975)
|
< 0.001
|
0.973 (0.971, 0.974)
|
< 0.001
|
|
Procedure characteristics
|
|
Withdrawal time
|
|
< 6 mins
|
794
|
317
|
1.000 (ref)
|
|
1.000 (ref)
|
|
|
≥ 6 mins
|
38,526
|
38,871
|
2.545 (2.233, 2.901)
|
< 0.001
|
2.538 (2.218, 2.902)
|
< 0.001
|
APP, adenomas per colonoscopy for each physician; N, sample size; OR, odds ratio;
CI, confidence interval.
* Adjusted logistic regression adjusted for patient age, patient gender, physician
age, and withdrawal time. The number of colonoscopies for adjusted multivariable is
77,357.
Table 5
Unadjusted and adjusted[*] association of factors with adenoma detection rate.
|
Low ADR
|
High ADR
|
Unadjusted
|
Adjusted
|
|
N
|
N
|
OR (95 % CI)
|
P value
|
OR (95 % CI)
|
P value
|
|
Patient characteristics
|
|
Age
|
11,372
|
69,543
|
1.000 (0.997, 1.002)
|
0.677
|
1.005 (1.002, 1.007)
|
< 0.001
|
|
Gender
|
|
Female
|
6,854
|
36,790
|
1.000 (ref)
|
|
1.000 (ref)
|
|
|
Male
|
4,517
|
32,751
|
1.351 (1.297, 1.406)
|
< 0.001
|
1.485 (1.421, 1.553)
|
< 0.001
|
|
Physician characteristics
|
|
Age
|
11,372
|
68,639
|
0.896 (0.894, 0.898)
|
< 0.001
|
0.893 (0.891, 0.895)
|
< 0.001
|
|
Procedure characteristics
|
|
Withdrawal time
|
|
< 6 mins
|
215
|
896
|
1.000 (ref)
|
|
1.000 (ref)
|
|
|
≥ 6 mins
|
10,771
|
66,356
|
1.478 (1.272, 1.718)
|
< 0.001
|
1.390 (1.176, 1.644)
|
< 0.001
|
ADR, adenomas per colonoscopy for each physician; N, sample size; OR, odds ratio;
CI, confidence interval.
* Adjusted logistic regression adjusted for patient age, patient gender, physician
age, and withdrawal time. The number of colonoscopies for adjusted multivariable is
77,357.
Discussion
In this large, community-based study of 60 endoscopists performing screening colonoscopies,
rates APC, APP, and ADR for individual endoscopists were variable. For the two new
quality indicators in colonoscopy, APC was highly correlated with ADR and APP was
moderately correlated with ADR. Factors associated with higher APC, APP, and ADR were
younger patients age, male patients, younger endoscopist age, and longer withdrawal
time (≥ 6 mins).
We found APC highly correlated with ADR (r = 0.97, P < 0.001). Our results are consistent with other reports in the literature. In a prospective
study in Korea (28 colonoscopists), Park et al. found that APC was significantly correlated
with ADR (r = 0.82, P < 0.001) [11]. In a US study with 21,766 colonoscopies performed by 20 endoscopists, Kahi et al.
found that APC and ADR were highly correlated (r = 0.91, P < 0.001) [12]. In an Austrian study with 44,142 colonoscopies performed by 202 endoscopists, Gessl
et al. found that APC was strongly correlated with ADR (r = 0.94, P < 0.01) [10]. We also found that APP was moderately correlated with ADR (r = 0.57, P < 0.01). A retrospective study including 2116 colonoscopies performed by 6 endoscopists
found that APP was not correlated with ADR [13]. We found no endoscopist with highest APC had a lower ADR. However, we also performed
analyses stratified by high and low APC and AAP, which provide additional information
beyond the correlation alone. We found that 47.6 % of endoscopists with low APC and
74 % of endoscopists with low APP had a higher ADR, suggesting these endoscopists
are good at finding one polyp but not multiple polyps, lending support to the “one
and done” phenomenon and that both APP and APC may be a good measure beyond ADR, to
distinguish high performers. Taken together, our findings suggest that although ADR
may be sufficient in capturing the quality of colonoscopy, both APC and APP further
distinguish high performers beyond an adequate ADR. With advances in technology, adoption
of artificial intelligence and other computer-aided assistance for polyp detection,
ADR alone may no longer be sufficient in distinguishing high from low performers,
and there is an unmet need to develop and validate newer quality indicators.
We found that endoscopist age was statistically significantly associated with APC,
AAP and ADR. Ours is the first study to report physician age and association with
APC and AAP. Several previous studies investigated the association of endoscopist’
age with ADR, but the results were inconsistent. In a retrospective study with 104,618
colonoscopies performed by 201 physicians, Mehrotra et al. found that physicians with
less than 9 years since their residency have a higher ADR than physicians who have
25 to 51 years of practice (P = 0.004) [14]. Whether this is due to enhanced training of colonoscopy procedure for younger endoscopists,
or technical skills of younger endoscopist is not known. However, in the COLONPREV
study (3,838 colonoscopies performed by 48 endoscopists), Jover et al. found that
older physician age was associated with higher ADR (OR 1.06; 95 % CI 1.01 – 1.11)
[15]. Our findings need to be confirmed in future studies and the role of endoscopist
age on performance of colonoscopy needs to be further studied.
The strengths of our study are the large sample size of colonoscopies, community dwelling,
average risk screening population and prospectively collected data. We collected information
on patient-level, endoscopist-level and procedure-level factors and detailed information
on histology of polyps and withdrawal times. The first limitation of these results
is that we only included 60 endoscopists in a single practice. Second, there may be
residual confounding of the association of factors with APC, APP, and ADR for which
we are unable to account or control, such as patient race, diet, body mass index,
family history, and lifestyle. Finally, although this is one of the largest community-based
endoscopy practices in the United States, whether our results are generalizable to
the population is unknown.
Conclusion
In summary, APC and ADR were highly correlated, and adenomas per positive participant
and ADR was moderately correlated. Younger endoscopist age and longer withdrawal time
(≥ 6 mins) were statistically significantly associated with colonoscopy quality. These
findings suggest that in addition to ADR, APC and APP provide additional information
on endoscopist performance and need to be validated as potential quality indicators.
