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DOI: 10.1055/a-1151-8691
Are adenoma and serrated polyp detection rates correlated with endoscopists’ sensitivity of optical diagnosis?
Abstract
Introduction Endoscopists with a high adenoma detection rate (ADR) and proximal serrated polyp detection rate (PSPDR) detect these polyps more frequently, which may be attributable to better recognition of their endoscopic features. Little is known about the association between endoscopic lesion detection and differentiation skills. Therefore, we evaluated the correlation between the ADR, PSPDR, and the sensitivity of optical diagnosis for adenomas and serrated polyps.
Methods We performed an exploratory post-hoc analysis of the DISCOUNT-2 study, including complete colonoscopies after a positive fecal immunochemical test (FIT) performed by endoscopists who performed ≥ 50 colonoscopies. The correlations between the ADR, PSPDR, and the sensitivity of optical diagnosis were calculated using Pearson’s rho correlation coefficient.
Results 24 endoscopists performed ≥ 50 colonoscopies, resulting in a total of 2889 colonoscopies. The overall ADR was 84.5 % (range 71.4 % – 95.3 %) and overall PSPDR was 13.7 % (4.3 % – 29.0 %). The sensitivity of optical diagnosis for adenomas and serrated polyps were 94.5 % (83.3 % – 100 %) and 74.0 % (37.5 % – 94.1 %), respectively. No correlation could be demonstrated between the ADR and the sensitivity of optical diagnosis for adenomas (−0.20; P = 0.35) or between the PSPDR and the sensitivity of optical diagnosis for serrated polyps (−0.12; P = 0.57).
Conclusions In a homogeneous FIT-positive population, no correlation between the ADR, PSPDR, and the sensitivity of optical diagnosis for adenomas and serrated polyps could be demonstrated. These exploratory results suggest that lesion detection and differentiation require different endoscopic skills. Further prospective studies are needed; until then, monitoring of both performance indicators is important to secure optimal efficacy of FIT-based colorectal cancer screening.
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Introduction
Colonoscopy is the reference standard for the detection of colorectal cancer (CRC) and for detecting and resecting its precursor lesions [1] [2] [3] [4]. The National Polyp Study demonstrated that, after removal of at least one colorectal adenoma, both CRC incidence and mortality were lower when compared to a reference population [1] [2]. However, colonoscopy is not fully protective for the development of post-colonoscopy CRCs (PCCRCs), which may occur in 2 % – 8 % of patients [5] [6] [7] [8] [9] [10]. The majority of PCCRCs might result from colonoscopy-related factors, such as missed polyps and incomplete polypectomies. Therefore, it is crucial to perform high quality colonoscopy procedures [7] [11] [12] [13] [14] [15] [16] [17].
The adenoma detection rate (ADR) is considered one of the most important colonoscopy quality indicators, as it proved to be inversely correlated with the occurrence of PCCRCs and CRC-related mortality [18] [19]. However, ADR monitoring does not fully capture the performance of endoscopists and can be flawed by the one-and-done phenomenon [20] [21]. Other colonoscopy quality indicators, such as the mean number of adenomas detected per colonoscopy (MAP), are therefore needed to obtain further insights into the quality of the performed procedures [20] [21].
An increasing body of evidence indicates that 15 % – 20 % of all CRCs are derived from serrated polyps. Additionally, a significant proportion of PCCRCs seem to arise from proximally located serrated polyps. High miss rates of these polyps, resulting from their pale color and flat appearance, might be a major cause of PCCRCs [22] [23] [24]. Therefore, the detection rate of proximal serrated polyps (PSPDR) has also been proposed as a colonoscopy quality indicator.
Before embarking on resection of a colorectal polyp, endoscopists should make an accurate optical diagnosis to predict its histopathology. If there is an accurate optical diagnosis, diminutive ( ≤ 5 mm) neoplastic polyps can be removed without histopathological evaluation and non-neoplastic polyps can be left in situ. Virtual chromoendoscopy techniques enable real-time optical diagnosis and could thereby guide this decision-making process [25] [26] [27]. However, before optical diagnosis strategies are ready for implementation, assurance of adequate differentiation between neoplastic and non-neoplastic lesions is warranted [28] [29].
Both the ADR and PSPDR are known to vary among endoscopists [18] [19] [30] [31] [32] [33] [34] [35] [36] [37]. As endoscopists with a high ADR and PSPDR are able to detect adenomas and proximal serrated polyps more frequently, it can be hypothesized that this is caused by better recognition of the endoscopic features of these polyps, resulting in improved detection. If this correlation is present, it may imply that improving the accuracy of optical diagnosis could increase the detection of premalignant polyps. However, little is known about the association between these endoscopy skills and therefore we aimed to evaluate the correlation between the ADR, PSPDR, and the sensitivity of optical diagnosis for adenomas and serrated polyps.
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Methods
Study design
This is an exploratory post-hoc analysis from a prospective randomized observational multicenter study (DISCOUNT-2) which evaluated the duration of establishing and maintaining a clinically acceptable accuracy for the endoscopic optical diagnosis of diminutive neoplastic colorectal polyps [38]. This study was performed between January 2015 and January 2017 in 12 regional centers and one academic center in the Netherlands.
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Colonoscopy setting and participating endoscopists
All colonoscopies were performed in individuals undergoing colonoscopy after a positive fecal immunochemical test (FIT) within the Dutch Bowel Cancer Screening Program (BCSP) [39]. The Dutch BCSP was implemented in 2014 and its complete rollout was phased; each year new birth cohorts were invited until full implementation was achieved in 2019. The program involves biennial FIT screening for individuals aged 55 – 75 years, followed by colonoscopy for all participants with a positive (≥ 275 ng/mL) FIT (FOB gold, Sentinel, Milan, Italy).
Participating endoscopists were accredited to perform colonoscopies within the Dutch BCSP and had performed colonoscopies within the program for at least 1 year prior to the start of the study. During the accreditation process, the knowledge and skills of endoscopists were tested by e-learning, by measuring evidence-based colonoscopy quality indicators, and by evaluating their practical colonoscopy skills [40].
For the sake of the DISCOUNT-2 study, all participating endoscopists were trained in optical diagnosis with the validated Workgroup SerrAted polypS and Polyposis (WASP) module [41]. This training phase consisted of both image-based and real-time training phases. Endoscopists were required to meet predefined thresholds in the training phase before entering the continuation phase. Further details of the training and its predefined thresholds are described elsewhere [38].
According to the protocol of the DISCOUNT-2 study, all detected colorectal lesions were removed, with the exception of multiple ( ≥ 3) diminutive hyperplastic polyps within the rectosigmoid. These diminutive hyperplastic polyps were left in situ and the endoscopist was instructed to biopsy at least one polyp that was representative of those present. The endoscopists recorded their optical diagnosis of all polyps during white-light endoscopy (WLE) and narrow-band imaging (NBI) and included their confidence levels [38].
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Colonoscopy features and polyp data collection
During the continuation phase of the DISCOUNT-2 study, all details of the colonoscopies were recorded by a structured colonoscopy reporting system. Data on the evidence-based quality indicators of colonoscopy, such as depth of insertion of the colonoscope, cleanliness of the bowel assessed with the validated Boston Bowel Preparation Scale (BBPS), and the type of bowel preparation solution, were incorporated as well [42] [43] [44] [45].
For this study we collected data based on patient demographics (age, sex, and American Society of Anesthesiologists (ASA) classification), polyp characteristics (location, lesion size assessed by the endoscopist, morphology, applied treatment, and histological diagnosis), and colonoscopy quality indicators. All data were entered into an online CastorEDC database [46].
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Histopathologic assessment
All resected colorectal lesions were collected in separate numbered containers, which is part of the Dutch BCSP. All lesions were assessed by accredited pathologists with expertise in gastrointestinal pathology in the local hospital. The histopathologic assessment was performed according to the World Health Organisation (WHO) 2010 classification [47].
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Inclusion and exclusion criteria
For this exploratory post-hoc analysis, we included only the complete colonoscopies that were performed by endoscopists who performed at least 50 complete colonoscopies within the continuation phase of the DISCOUNT-2 study. Colonoscopies performed in patients with the endoscopic suspicion of polyposis syndrome and inflammatory bowel disease were excluded.
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Study outcomes and statistical analysis
For each endoscopist, individual premalignant polyp detection rates were calculated. The calculated detection rates consisted of: the ADR (the proportion of colonoscopies wherein at least one histopathologically confirmed adenoma was detected); the MAP (the mean number of histopathologically proven adenomas detected per colonoscopy); the PSPDR (the proportion of colonoscopies wherein at least one histopathologically confirmed proximal serrated polyp, defined as a hyperplastic polyp, sessile serrated lesion (SSL), or traditional serrated adenoma (TSA), was detected); and the mean number of histopathologically proven proximally located serrated polyps detected per colonoscopy. The proximal colon was defined as proximal to the descending colon (splenic flexure to cecum), in accordance with the Dutch guideline for colonoscopy surveillance [48]. All serrated polyps detected in the proximal colon were included to measure the PSPDR, regardless of polyp size and histopathology.
The diagnostic test sensitivities of optical diagnosis were calculated for all diminutive (≤ 5 mm) adenomas and serrated polyps located throughout the entire colon using the histopathological diagnosis as the reference standard. Only endoscopic histology predictions of diminutive polyps with high confidence were used to calculate the sensitivity of optical diagnosis for adenomas and serrated polyps. Owing to the limited number of both detected SSLs and high confidence histopathology predictions of SSLs per individual endoscopist, we decided not to separately analyze the SSL detection rate and the sensitivity of SSL optical diagnosis.
Count variables and categorical variables were reported as percentages. The MAP and the mean number of proximal serrated polyps were considered as Poisson-distributed data and were therefore reported as mean and standard deviation (SD). Generalized estimating equations modeling using binary logistic regression, adjusted for clustering of polyps and patients per endoscopist, was used to compare the categorical ADR, PSPDR, and the sensitivity of optical diagnosis for adenomas and serrated polyps. Generalized estimating equations using Poisson logistic modeling, adjusted for clustering of polyps and patients per endoscopist, was used to compare the Poisson-distributed data, such as the MAP and mean number of proximal serrated polyps detected per colonoscopy.
Funnel plots were created to further investigate the potential variances in the ADR and PSPDR. These were created to evaluate the ADR and PSPDR of each endoscopist with respect to the overall mean ADR and PSPDR by using approximate upper and lower 95 % confidence limits. Furthermore, the ADR and PSPDR were compared between the first 50 complete colonoscopies and the last 50 complete colonoscopies of endoscopists who performed over 100 complete colonoscopies within the study to investigate further the intra-endoscopist variability of these detection rates.
Correlations between the ADR, PSPDR, MAP, mean number of proximal serrated polyps, and sensitivity of optical diagnosis for adenomas and serrated polyps were calculated using the Pearson’s rho (ρ) correlation coefficient. P < 0.05 was regarded as being statistically significant. All statistical analyses were performed using SPSS Statistics version 24 (SPSS, Chicago, Illinois, USA).
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Results
Colonoscopy characteristics
In total, 27 endoscopists performed 3144 colonoscopies in the DISCOUNT-2 study, of which 24 endoscopists performed at least 50 complete colonoscopies. These 24 endoscopists performed a total of 2955 colonoscopies, of which 2889 were complete and were therefore eligible for inclusion in this study ([Fig. 1]). The overall cecal intubation rate was 97.8 % (2889/2995), which was not significantly different among the participating endoscopists (Table 1 s; see online-only Supplementary materials). The median age of the patients was 66 years (interquartile range 63 – 69) and 60.4 % were men. Other patient demographics and the colonoscopy quality indicators of the included colonoscopies are described in [Table 1].
IQR, interquartile range; ASA, American Society of Anesthesiologists; BBPS, Boston Bowel Preparation Scale.
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Endoscopist performance in adenoma and proximal serrated polyp detection
In this cohort of 2889 complete colonoscopies, a total of 6828 adenomas and 1644 serrated polyps (1308 hyperplastic polyps and 336 SSLs) were detected ([Table 2]). For all endoscopists, the overall ADR was 84.5 % (range 71.4 % – 95.3 %), MAP was 2.33 (SD 2.2; range 1.52 [1.84] – 3.64 [3.06]), PSPDR was 13.7 % (range 4.3 % – 29.0 %), and mean number of proximally located serrated polyps detected per colonoscopy was 0.19 (SD 0.55; range 0.04 [0.20] – 0.43 [0.81]). Among endoscopists, all detection rates were significantly different (P < 0.001). Details per endoscopist are shown in [Table 2] and [Table 3].
|
Complete colonoscopies |
|
|
Total number of detected lesions |
9415 |
|
Lesion subtype, n (%) |
|
|
6828 (72.5 %) |
|
1308 (13.9 %) |
|
336 (3.6 %) |
|
37 (0.4 %) |
|
126 (1.3 %) |
|
524 (5.6 %) |
|
293 (3.1 %) |
|
Detection rates |
|
|
2441 (84.5 %) |
|
2.33 (2.2) |
|
396 (13.7 %) |
|
0.19 (0.55) |
|
Diagnostic test sensitivity for adequate endoscopic prediction[*] |
|
|
2233 (94.5 %) |
|
526 (74.0 %) |
SSL, sessile serrated lesion; SD, standard deviation; PSPDR, proximal serrated polyp detection rate.
* Only endoscopic histology predictions made with high confidence were used to calculate the sensitivity of adenoma and serrated polyp optical detection.
|
Endoscopist |
Number of procedures |
ADR[*], % |
Number of adenomas per colonoscopy[1], mean (SD), % |
PSPDR[*], % |
Number of proximal serrated polyps per colonoscopy[*], mean (SD), % |
|
1 |
82 |
86.6 % |
3.05 (2.64) |
22.0 % |
0.27 (0.57) |
|
2 |
113 |
77.9 % |
2.04 (1.76) |
10.6 % |
0.13 (0.41) |
|
3 |
222 |
86.5 % |
2.45 (2.34) |
13.5 % |
0.18 (0.50) |
|
4 |
155 |
85.8 % |
2.76 (2.44) |
29.0 % |
0.43 (0.81) |
|
5 |
146 |
74.0 % |
1.81 (2.21) |
8.2 % |
0.09 (0.31) |
|
6 |
94 |
91.5 % |
2.54 (1.89) |
10.6 % |
0.24 (0.86) |
|
7 |
168 |
81.0 % |
2.16 (1.90) |
13.1 % |
0.16 (0.47) |
|
8 |
188 |
82.4 % |
2.23 (2.06) |
10.6 % |
0.13 (0.45) |
|
9 |
134 |
88.1 % |
2.26 (1.81) |
11.9 % |
0.14 (0.41) |
|
10 |
124 |
92.7 % |
2.84 (2.12) |
16.1 % |
0.18 (0.44) |
|
11 |
122 |
76.2 % |
1.73 (1.81) |
4.9 % |
0.06 (0.27) |
|
12 |
116 |
87.1 % |
1.64 (1.23) |
4.3 % |
0.04 (0.20) |
|
13 |
110 |
84.5 % |
1.96 (1.70) |
10.0 % |
0.13 (0.41) |
|
14 |
57 |
89.5 % |
2.19 (1.62) |
22.8 % |
0.30 (0.63) |
|
15 |
129 |
95.3 % |
2.99 (2.41) |
17.8 % |
0.20 (0.47) |
|
16 |
92 |
84.8 % |
2.25 (2.11) |
20.7 % |
0.30 (0.71) |
|
17 |
184 |
79.3 % |
2.18 (2.28) |
14.1 % |
0.20 (0.60) |
|
18 |
95 |
84.2 % |
2.20 (1.95) |
14.7 % |
0.18 (0.46) |
|
19 |
160 |
90.0 % |
3.64 (3.06) |
16.9 % |
0.26 (0.72) |
|
20 |
74 |
83.8 % |
2.97 (3.21) |
18.9 % |
0.27 (0.73) |
|
21 |
90 |
78.9 % |
1.69 (1.61) |
7.8 % |
0.13 (0.56) |
|
22 |
70 |
71.4 % |
1.52 (1.84) |
8.6 % |
0.10 (0.35) |
|
23 |
65 |
93.8 % |
2.39 (1.82) |
13.8 % |
0.20 (0.62) |
|
24 |
99 |
86.9 % |
1.96 (1.74) |
11.1 % |
0.19 (0.67) |
|
Overall |
2889 |
84.5 % |
2.33 (2.20) |
13.7 % |
0.19 (0.55) |
ADR, adenoma detection rate; SD, standard deviation; PSPDR, proximal serrated polyp detection rate.
* Probabilities were calculated with generalized estimating equations modeling using either binary logistic or Poisson logistic regression. The highest and lowest detector are shown in bold. Results showed P < 0.001 for all the above parameters.
Funnel plots showing each endoscopist’s ADR and PSPDR with respect to the overall mean of the study are shown in [Fig. 2]. Both show a symmetrical distribution for each individual endoscopist around the overall ADR and PSPDR.
The differences in the ADR and PSPDR between the first 50 complete colonoscopies and the last 50 complete colonoscopies of the endoscopists who performed more than 100 complete colonoscopies within the study are presented in [Table 4] and [Table 5]. No significant differences between the first 50 and last 50 complete colonoscopies were found when assessing the overall ADR (83.7 % vs. 83.9 %; P = 0.94) and PSPDR (12.1 % vs. 14.3 %; P = 0.24), respectively. When assessing the individual endoscopists, the ADR of endoscopist #17 significantly increased from 66.0 % to 86.0 % and the PSPDR of endoscopist #8 significantly increased from 4.0 % to 16.0 %.
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Endoscopists’ diagnostic test sensitivities
Diminutive adenomas and serrated polyps were optically diagnosed correctly with high confidence in 94.5 % (range 83.3 % – 100 %) and 74.0 % of cases (range 37.5 % – 94.1 %), respectively. All diagnostic test sensitivities were significantly different among endoscopists (P < 0.001); details per endoscopist are listed in [Table 6].
|
Endoscopist |
No of procedures |
Sensitivity of optical diagnosis, % |
|
|
Adenomas[*] |
Serrated polyps[*] |
||
|
1 |
82 |
99.0 % |
73.9 % |
|
2 |
113 |
86.9 % |
72.7 % |
|
3 |
222 |
97.5 % |
81.3 % |
|
4 |
155 |
98.4 % |
77.4 % |
|
5 |
146 |
95.0 % |
83.3 % |
|
6 |
94 |
97.6 % |
84.0 % |
|
7 |
168 |
92.5 % |
85.3 % |
|
8 |
188 |
97.2 % |
56.0 % |
|
9 |
134 |
88.9 % |
83.3 % |
|
10 |
124 |
98.5 % |
94.1 % |
|
11 |
122 |
97.3 % |
71.4 % |
|
12 |
116 |
91.2 % |
85.7 % |
|
13 |
110 |
100 % |
37.5 % |
|
14 |
57 |
87.5 % |
53.8 % |
|
15 |
129 |
83.9 % |
66.7 % |
|
16 |
92 |
88.0 % |
65.4 % |
|
17 |
184 |
88.7 % |
73.9 % |
|
18 |
95 |
90.6 % |
82.4 % |
|
19 |
160 |
100 % |
70.8 % |
|
20 |
74 |
96.0 % |
63.6 % |
|
21 |
90 |
94.0 % |
73.3 % |
|
22 |
70 |
97.3 % |
63.2 % |
|
23 |
65 |
83.3 % |
76.5 % |
|
24 |
99 |
97.1 % |
90.9 % |
|
Overall |
2889 |
94.5 % |
74.0 % |
* Probabilities were calculated with generalized estimating equations modeling using either binary logistic or Poisson logistic regression. Only endoscopic histology predictions for polyps 1 – 5 mm and made with high confidence were used to calculate the sensitivity. The highest and lowest detector are shown in bold. Results showed P < 0.001 for both adenomas and serrated polyps.
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Correlation between the diagnostic test sensitivities and the detection of adenomas and proximal serrated polyps
The correlations between the ADR, MAP, PSPDR, the mean number of proximal serrated polyps, and the diagnostic test sensitivities are presented in [Table 7], and also in Figs. 1 s and 2 s. No significant correlations between the detection of adenomas and the sensitivity of optical diagnosis for adenomas could be demonstrated (ADR and adenoma sensitivity ρ −0.20, P = 0.35; MAP and adenoma sensitivity ρ 0.14, P = 0.50). In addition, no correlation could be demonstrated between the detection of proximal serrated polyps and its associated diagnostic test sensitivities (PSPDR and serrated polyp sensitivity ρ −0.12, P = 0.57; mean number of proximal serrated polyps detected per colonoscopy and serrated polyp sensitivity ρ – 0.08, P = 0.70).
ADR, adenoma detection rate; MAP, mean number of adenomas per colonoscopy; PSPDR, proximal serrated polyp detection rate.
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Discussion
In this exploratory post-hoc analysis of a prospective randomized observational multicenter study of colonoscopies performed in a FIT-positive population, no correlations could be demonstrated between the ADR, MAP, PSPDR, the mean number of proximal serrated polyps, and the sensitivity of optical diagnosis for adenomas and serrated polyps.
We hypothesized that endoscopists with a high ADR and PSPDR might be better at recognizing the endoscopic features of these polyps and would therefore be better at making a correct optical diagnosis. In other words, those endoscopists would perform better in recognizing the specific endoscopic features of adenomas and serrated polyps, which could result in their high polyp detection rates. To our surprise, this correlation could not be demonstrated. Based on our exploratory data, training programs primarily focusing on improving the optical diagnosis of polyps might therefore not help to improve polyp detection rates as a secondary training benefit [38]. There is however very limited evidence on other factors that would help to improve individual polyp detection rates and therefore more studies are needed to target new colonoscopy improvement initiatives [49].
Our study was performed in a unique study setting where data on both optical diagnosis, including confidence levels, and the detection rates of adenomas and proximal serrated polyps were collected in FIT-positive colonoscopies. These procedures were performed according to the current daily practice in the Netherlands and all data were prospectively collected in an era of awareness of the malignant potential of serrated polyps, as well as of the importance of high quality colonoscopy.
The reason that we found no correlation between endoscopic lesion detection and optical diagnosis skills could potentially be explained by the composition of the participating endoscopists. The participating endoscopists consisted of a homogeneous group of high performing endoscopists, as they were all accredited to perform colonoscopies within the Dutch BCSP. Furthermore, they were trained in optical diagnosis by the validated WASP classification and were only enrolled in this study if they met predefined thresholds in the training phase of the DISCOUNT-2 study [40] [41]. In addition, the endoscopists had to perform structured reporting of all polyps in their daily clinical practice, including their optical diagnosis using NBI. Therefore, these requirements possibly resulted in a selected group of endoscopists with a special interest in the subject.
Besides this, all colonoscopies were performed after a positive FIT result and this enriched population could have accelerated the learning curve of optical diagnosis. Possibly, having a more heterogeneous group of endoscopists might have influenced the results of our study.
Pohl et al. [50] published a study with similar findings and found no difference between low and high adenoma detectors in achieving optical diagnosis quality benchmarks according to the Preservation and Incorporation of Valuable Endoscopic Innovations (PIVI) statements. Our two studies may underline that lesion detection and accurate histology prediction require different endoscopic skills and both of these parameters should be monitored to ensure a high quality and effective colonoscopy practice. However, both of our studies consisted of post-hoc analyses of multicenter randomized trials, and both inherit the important limitation that the studies were not originally powered to demonstrate a correlation between endoscopic lesion detection and endoscopic differentiation skills. We could therefore not reject the null hypothesis of a non-existing association between endoscopic lesion detection and endoscopic differentiation skills. It might be possible that our numbers are too small to draw strong conclusions about the investigated correlation and it would therefore be of interest to perform a prospective study that was primarily powered to further investigate our hypothesis.
Furthermore, another limitation of our study also has to be acknowledged. That is the relatively small number of colonoscopies per endoscopist and thus only a limited number of individual observations made with high confidence were available for the assessment of the diagnostic test sensitivities of serrated polyp subtypes. This was the reason we were not able to analyze the correlation between the SSL detection rate and the sensitivity of optical diagnosis for SSLs. Therefore, it was decided to analyze the correlation between the PSPDR and the optical diagnosis of serrated polyps, even though endoscopists were trained in optical diagnosis with the validated WASP, which differentiates between adenomas, hyperplastic polyps, and SSLs.
Both the ADR and PSPDR were highly variable among the participating endoscopists. The funnel plots show a symmetrical distribution for the ADR and PSPDR of each individual endoscopist around the overall mean ADR and PSPDR. These plots may indicate that differences in the distribution of each endoscopist’s ADR and PSPDR decrease when individual endoscopists perform a higher volume of colonoscopies. However, there were limited indications that the high ADR and PSPDR variability was caused by a high intra-individual variability or individual learning curves. There were only two endoscopists who significantly increased their ADR or PSPDR during the course of the study.
The variations in adenoma and serrated polyp detection rates may suggest considerable lesion miss rates for low detecting endoscopists [18] [19] [30] [31] [32] [33] [34] [35] [36] [37]. However, whereas ADR has been inversely correlated with the occurrence of PCCRCs and CRC-related mortality in primary colonoscopy screening cohorts, the long-term consequences of variances in ADR after FIT-screening are not yet known [18] [19]. The consequence of low serrated polyp detection rates for any colonoscopy indication also remains unknown, as the PSPDR has not yet been associated with PCCRCs and CRC-related mortality.
Previous research demonstrated that a wide variation in ADR among endoscopists might be explained by the increased detection of small and flat adenomas by endoscopists with a high ADR. However, the clinical relevance of these small adenomas can be questioned as they harbor a low risk of progressing to advanced disease and any progression tends to be slow [51]. Besides, as the ADR is very high in patients undergoing colonoscopy after a positive FIT, most will receive subsequent surveillance colonoscopies anyways. Therefore, when small low risk adenomas were missed during the initial colonoscopy by a low detecting endoscopist, the lesions might still be expected to harbor low risk features when detected during the subsequent surveillance colonoscopy [48] [51].
No correlation between adenoma and proximal serrated polyp detection and the sensitivity of optical diagnosis for these polyps could be demonstrated. Our exploratory results seem to indicate that achieving quality in these parameters requires different endoscopic skills. However, further prospective studies primarily aiming to investigate a correlation between premalignant polyp detection and lesion differentiation are needed to draw definitive conclusions. Until then, accurate training, monitoring, and auditing of both performance indicators might therefore be important to secure the optimal efficacy of a FIT-based CRC screening program.
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Competing interests
E. Dekker received a research grant and equipment on loan from Olympus, equipment on loan from Fujifilm, and consulting fees for medical advice from Tillots, Olympus, and Fujifilm, all outside the submitted work. P. Fockens received personal fees from Cook Medical, Ethicon Endosurgery, and Medtronic, and received consultancy fees from Fujifilm and Olympus, all outside the submitted work. The authors declare that they have no conflict of interest.
Acknowledgments
Financial support was received from the Dutch Digestive Disease Foundation (FP13 – 10).
The DISCOUNT study group consists of :
M.C.J.M. Becx[1], A.M. van Berkel[2], W. Bruins Slot[3], M. Cazemier[4], A.C.T.M. Depla[5], J.M.J. Geesing[6], T.A. Grool[3], P.G.M. Houben[5], J.M. Jansen[4], K. Kessels[1]
[7], M.E. van Leerdam[8] , N. van Lelyveld[1], R.C. Mallant-Hent[7], W.A. Marsman[9], J. Schmidt[10], E. Schnekenburger[10], B.W. van der Spek[2], E.J. van Soest[9], P.C.F. Stokkers[11], J. Tenthof van Noorden[1], K.T. Tytgat[12], S.A.C. van Tuyl[6], M.T. Uiterwaal[3], R.C. Verdonk[1], M.A.M.T. Verhagen[6], A. Voorburg[6], M. van der Vlugt[12], and C.A. Wientjes[11]
1 Department of Gastroenterology and Hepatology, Sint Antonius Ziekenhuis, Nieuwegein, The Netherlands
2 Department of Gastroenterology and Hepatology, Medisch Centrum Alkmaar, Alkmaar, The Netherlands
3 Department of Gastroenterology and Hepatology, Spaarne Ziekenhuis, Hoofddorp, The Netherlands
4 Department of Gastroenterology and Hepatology, Onze Lieve Vrouwe Gasthuis Oost, Amsterdam, The Netherlands
5 Department of Gastroenterology and Hepatology, Slotervaart Ziekenhuis, Amsterdam, The Netherlands
6 Department of Gastroenterology and Hepatology, Diakonessenhuis, Utrecht, The Netherlands
7 Department of Gastroenterology and Hepatology, Flevoziekenhuis, Almere, The Netherlands
8 Department of Gastroenterology and Hepatology, Antonie van Leeuwenhoek Ziekenhuis, Amsterdam, The Netherlands
9 Department of Gastroenterology and Hepatology, Kennemer Gasthuis, Haarlem, The Netherlands
10 Department of Gastroenterology and Hepatology, West Fries Gasthuis, Hoorn, The Netherlands
11 Department of Gastroenterology and Hepatology, Sint Lucas Andreas Ziekenhuis/Onze Lieve Vrouwe Gasthuis West, Amsterdam, The Netherlands
12 Department of Gastroenterology and Hepatology, Academic Medical Centre, University of Amsterdam, Amsterdam, The Netherlands
-
References
- 1 Zauber AG, Winawer SJ, O'Brien MJ. et al. Colonoscopic polypectomy and long-term prevention of colorectal-cancer deaths. NEJM 2012; 366: 687-696
- 2 Winawer SJ, Zauber AG, Ho MN. et al. Prevention of colorectal cancer by colonoscopic polypectomy. The National Polyp Study Workgroup. NEJM 1993; 329: 1977-1981
- 3 Rex DK, Ahnen DJ, Baron JA. et al. Serrated lesions of the colorectum: review and recommendations from an expert panel. Am J Gastroenterol 2012; 107: 1315-1329 ; quiz 4, 1330
- 4 Bettington M, Walker N, Clouston A. et al. The serrated pathway to colorectal carcinoma: current concepts and challenges. Histopathology 2013; 62: 367-386
- 5 Singh H, Nugent Z, Demers AA. et al. Rate and predictors of early/missed colorectal cancers after colonoscopy in Manitoba: a population-based study. Am J Gastroenterol 2010; 105: 2588-2596
- 6 Bressler B, Paszat LF, Chen Z. et al. Rates of new or missed colorectal cancers after colonoscopy and their risk factors: a population-based analysis. Gastroenterology 2007; 132: 96-102
- 7 le Clercq CM, Bouwens MW, Rondagh EJ. et al. Postcolonoscopy colorectal cancers are preventable: a population-based study. Gut 2014; 63: 957-963
- 8 Stoffel EM, Erichsen R, Froslev T. et al. Clinical and molecular characteristics of post-colonoscopy colorectal cancer: a population-based study. Gastroenterology 2016; 151: 870-878 e3
- 9 Mansouri D, McMillan DC, McIlveen E. et al. A comparison of tumour and host prognostic factors in screen-detected vs nonscreen-detected colorectal cancer: a contemporaneous study. Colorectal Dis 2016; 18: 967-975
- 10 Winawer SJ, Zauber AG, O'Brien MJ. et al. Randomized comparison of surveillance intervals after colonoscopic removal of newly diagnosed adenomatous polyps. The National Polyp Study Workgroup. NEJM 1993; 328: 901-906
- 11 Robertson DJ, Lieberman DA, Winawer SJ. et al. Colorectal cancers soon after colonoscopy: a pooled multicohort analysis. Gut 2014; 63: 949-956
- 12 Brenner H, Chang-Claude J, Seiler CM. et al. Interval cancers after negative colonoscopy: population-based case-control study. Gut 2012; 61: 1576-1582
- 13 Sanduleanu S, le Clercq CM, Dekker E. et al. Definition and taxonomy of interval colorectal cancers: a proposal for standardising nomenclature. Gut 2015; 64: 1257-1267
- 14 Martinez ME, Baron JA, Lieberman DA. et al. A pooled analysis of advanced colorectal neoplasia diagnoses after colonoscopic polypectomy. Gastroenterology 2009; 136: 832-841
- 15 Pohl H, Srivastava A, Bensen SP. et al. Incomplete polyp resection during colonoscopy-results of the complete adenoma resection (CARE) study. Gastroenterology 2013; 144: 74-80.e1
- 16 Singh H, Nugent Z, Demers AA. et al. The reduction in colorectal cancer mortality after colonoscopy varies by site of the cancer. Gastroenterology 2010; 139: 1128-1137
- 17 Baxter NN, Sutradhar R, Forbes SS. et al. Analysis of administrative data finds endoscopist quality measures associated with postcolonoscopy colorectal cancer. Gastroenterology 2011; 140: 65-72
- 18 Kaminski MF, Regula J, Kraszewska E. et al. Quality indicators for colonoscopy and the risk of interval cancer. NEJM 2010; 362: 1795-1803
- 19 Corley DA, Jensen CD, Marks AR. et al. Adenoma detection rate and risk of colorectal cancer and death. NEJM 2014; 370: 1298-1306
- 20 Wang HS, Pisegna J, Modi R. et al. Adenoma detection rate is necessary but insufficient for distinguishing high versus low endoscopist performance. Gastrointest Endosc 2013; 77: 71-78
- 21 Lee TJ, Rutter MD, Blanks RG. et al. Colonoscopy quality measures: experience from the NHS Bowel Cancer Screening Programme. Gut 2012; 61: 1050-1057
- 22 Arain MA, Sawhney M, Sheikh S. et al. CIMP status of interval colon cancers: another piece to the puzzle. Am J Gastroenterol 2010; 105: 1189-1195
- 23 Nishihara R, Ogino S, Chan AT. Colorectal-cancer incidence and mortality after screening. NEJM 2013; 369: 2355
- 24 Hazewinkel Y, Lopez-Ceron M, East JE. et al. Endoscopic features of sessile serrated adenomas: validation by international experts using high-resolution white-light endoscopy and narrow-band imaging. Gastrointest Endosc 2013; 77: 916-924
- 25 Ignjatovic A, East JE, Suzuki N. et al. Optical diagnosis of small colorectal polyps at routine colonoscopy (Detect InSpect ChAracterise Resect and Discard; DISCARD trial): a prospective cohort study. Lancet Oncol 2009; 10: 1171-1178
- 26 Rex DK. Narrow-band imaging without optical magnification for histologic analysis of colorectal polyps. Gastroenterology 2009; 136: 1174-1181
- 27 East JE, Vleugels JL, Roelandt P. et al. Advanced endoscopic imaging: European Society of Gastrointestinal Endoscopy (ESGE) Technology Review. Endoscopy 2016; 48: 1029-1045
- 28 Rex DK, Kahi C, O'Brien M. et al. The American Society for Gastrointestinal Endoscopy PIVI (Preservation and Incorporation of Valuable Endoscopic Innovations) on real-time endoscopic assessment of the histology of diminutive colorectal polyps. Gastrointest Endosc 2011; 73: 419-422
- 29 Kaminski MF, Hassan C, Bisschops R. et al. Advanced imaging for detection and differentiation of colorectal neoplasia: European Society of Gastrointestinal Endoscopy (ESGE) Guideline. Endoscopy 2014; 46: 435-449
- 30 Zorzi M, Senore C, Da Re F. et al. Detection rate and predictive factors of sessile serrated polyps in an organised colorectal cancer screening programme with immunochemical faecal occult blood test: the EQuIPE study (Evaluating Quality Indicators of the Performance of Endoscopy). Gut 2017; 66: 1233-1240
- 31 Hilsden RJ, Bridges R, Dube C. et al. Defining benchmarks for adenoma detection rate and adenomas per colonoscopy in patients undergoing colonoscopy due to a positive fecal immunochemical test. Am J Gastroenterol 2016; 111: 1743-1749
- 32 de Jonge V, Sint Nicolaas J, Cahen DL. et al. Quality evaluation of colonoscopy reporting and colonoscopy performance in daily clinical practice. Gastrointest Endosc 2012; 75: 98-106
- 33 Chen SC, Rex DK. Endoscopist can be more powerful than age and male gender in predicting adenoma detection at colonoscopy. Am J Gastroenterol 2007; 102: 856-861
- 34 Bretagne JF, Hamonic S, Piette C. et al. Variations between endoscopists in rates of detection of colorectal neoplasia and their impact on a regional screening program based on colonoscopy after fecal occult blood testing. Gastrointest Endosc 2010; 71: 335-341
- 35 Imperiale TF, Glowinski EA, Juliar BE. et al. Variation in polyp detection rates at screening colonoscopy. Gastrointest Endosc 2009; 69: 1288-1295
- 36 IJspeert JE, van Doorn SC, van der Brug YM. et al. The proximal serrated polyp detection rate is an easy-to-measure proxy for the detection rate of clinically relevant serrated polyps. Gastrointest Endosc 2015; 82: 870-877
- 37 IJspeert JE, de Wit K, van der Vlugt M. et al. Prevalence, distribution and risk of sessile serrated adenomas/polyps at a center with a high adenoma detection rate and experienced pathologists. Endoscopy 2016; 48: 740-746
- 38 Vleugels JLA, Dijkgraaf MGW, Hazewinkel Y. et al. Effects of training and feedback on accuracy of predicting rectosigmoid neoplastic lesions and selection of surveillance intervals by endoscopists performing optical diagnosis of diminutive polyps. Gastroenterology 2018; 154: 1682-1693.e1
- 39 National Institute for Public Health and the Environment (Ministry of Health, Welfare and Sport). Protocol for the Dutch Bowel Cancer Screening Programme [In Dutch]. 2009
- 40 National Institute for Public Health and the Environment (Ministry of Health, Welfare and Sport). Protocol for the authorization and auditing of colonoscopy centers and endoscopists, version 1. National Screening Programme for Bowel Cancer [In Dutch]. 2012
- 41 IJspeert JE, Bastiaansen BA, van Leerdam ME. et al. Development and validation of the WASP classification system for optical diagnosis of adenomas, hyperplastic polyps and sessile serrated adenomas/polyps. Gut 2016; 65: 963-970
- 42 Rees CJ, Bevan R, Zimmermann-Fraedrich K. et al. Expert opinions and scientific evidence for colonoscopy key performance indicators. Gut 2016; 65: 2045-2060
- 43 Rees CJ, Thomas GibsonS, Rutter MD. et al. UK key performance indicators and quality assurance standards for colonoscopy. Gut 2016; 65: 1923-1929
- 44 Ekkelenkamp VE, Dowler K, Valori RM. et al. Patient comfort and quality in colonoscopy. World J Gastroenterol 2013; 19: 2355-2361
- 45 Lai EJ, Calderwood AH, Doros G. et al. The Boston bowel preparation scale: a valid and reliable instrument for colonoscopy-oriented research. Gastrointest Endosc 2009; 69: 620-625
- 46 Castor Electronic Data Capture. Amsterdam: 2016 Available from: Accessed: 30 March 2020 https://www.castoredc.com/
- 47 Bosman FT, Carneiro F, Hruban RH. et al. WHO Classification of Tumours of the Digestive System. 4th. edn. Lyon, France: IARC; 2010
- 48 Dekker EL, van Leerdam ME, Hazewinkel Y. et al. Nederlandse Richtlijn Coloscopie Surveillance. Available from: Accessed: 25 March 2020 2013 http://wwwmdlnl/uploads/240/1308/Richtlijn_Coloscopie_Surveillance_definitief_2013.pdf
- 49 Atkins L, Hunkeler EM, Jensen CD. et al. Factors influencing variation in physician adenoma detection rates: a theory-based approach for performance improvement. Gastrointest Endosc 2016; 83: 617-626 e2
- 50 Pohl H, Bensen SP, Toor A. et al. Quality of optical diagnosis of diminutive polyps and associated factors. Endoscopy 2016; 48: 817-822
- 51 Vleugels JL, Hazewinkel Y, Fockens P. et al. Natural history of diminutive and small colorectal polyps: a systematic literature review. Gastrointest Endosc 2017; 85: 1169-1176.e1
Corresponding author
Publication History
Received: 28 March 2018
Accepted: 10 March 2020
Article published online:
29 April 2020
© Georg Thieme Verlag KG
Stuttgart · New York
-
References
- 1 Zauber AG, Winawer SJ, O'Brien MJ. et al. Colonoscopic polypectomy and long-term prevention of colorectal-cancer deaths. NEJM 2012; 366: 687-696
- 2 Winawer SJ, Zauber AG, Ho MN. et al. Prevention of colorectal cancer by colonoscopic polypectomy. The National Polyp Study Workgroup. NEJM 1993; 329: 1977-1981
- 3 Rex DK, Ahnen DJ, Baron JA. et al. Serrated lesions of the colorectum: review and recommendations from an expert panel. Am J Gastroenterol 2012; 107: 1315-1329 ; quiz 4, 1330
- 4 Bettington M, Walker N, Clouston A. et al. The serrated pathway to colorectal carcinoma: current concepts and challenges. Histopathology 2013; 62: 367-386
- 5 Singh H, Nugent Z, Demers AA. et al. Rate and predictors of early/missed colorectal cancers after colonoscopy in Manitoba: a population-based study. Am J Gastroenterol 2010; 105: 2588-2596
- 6 Bressler B, Paszat LF, Chen Z. et al. Rates of new or missed colorectal cancers after colonoscopy and their risk factors: a population-based analysis. Gastroenterology 2007; 132: 96-102
- 7 le Clercq CM, Bouwens MW, Rondagh EJ. et al. Postcolonoscopy colorectal cancers are preventable: a population-based study. Gut 2014; 63: 957-963
- 8 Stoffel EM, Erichsen R, Froslev T. et al. Clinical and molecular characteristics of post-colonoscopy colorectal cancer: a population-based study. Gastroenterology 2016; 151: 870-878 e3
- 9 Mansouri D, McMillan DC, McIlveen E. et al. A comparison of tumour and host prognostic factors in screen-detected vs nonscreen-detected colorectal cancer: a contemporaneous study. Colorectal Dis 2016; 18: 967-975
- 10 Winawer SJ, Zauber AG, O'Brien MJ. et al. Randomized comparison of surveillance intervals after colonoscopic removal of newly diagnosed adenomatous polyps. The National Polyp Study Workgroup. NEJM 1993; 328: 901-906
- 11 Robertson DJ, Lieberman DA, Winawer SJ. et al. Colorectal cancers soon after colonoscopy: a pooled multicohort analysis. Gut 2014; 63: 949-956
- 12 Brenner H, Chang-Claude J, Seiler CM. et al. Interval cancers after negative colonoscopy: population-based case-control study. Gut 2012; 61: 1576-1582
- 13 Sanduleanu S, le Clercq CM, Dekker E. et al. Definition and taxonomy of interval colorectal cancers: a proposal for standardising nomenclature. Gut 2015; 64: 1257-1267
- 14 Martinez ME, Baron JA, Lieberman DA. et al. A pooled analysis of advanced colorectal neoplasia diagnoses after colonoscopic polypectomy. Gastroenterology 2009; 136: 832-841
- 15 Pohl H, Srivastava A, Bensen SP. et al. Incomplete polyp resection during colonoscopy-results of the complete adenoma resection (CARE) study. Gastroenterology 2013; 144: 74-80.e1
- 16 Singh H, Nugent Z, Demers AA. et al. The reduction in colorectal cancer mortality after colonoscopy varies by site of the cancer. Gastroenterology 2010; 139: 1128-1137
- 17 Baxter NN, Sutradhar R, Forbes SS. et al. Analysis of administrative data finds endoscopist quality measures associated with postcolonoscopy colorectal cancer. Gastroenterology 2011; 140: 65-72
- 18 Kaminski MF, Regula J, Kraszewska E. et al. Quality indicators for colonoscopy and the risk of interval cancer. NEJM 2010; 362: 1795-1803
- 19 Corley DA, Jensen CD, Marks AR. et al. Adenoma detection rate and risk of colorectal cancer and death. NEJM 2014; 370: 1298-1306
- 20 Wang HS, Pisegna J, Modi R. et al. Adenoma detection rate is necessary but insufficient for distinguishing high versus low endoscopist performance. Gastrointest Endosc 2013; 77: 71-78
- 21 Lee TJ, Rutter MD, Blanks RG. et al. Colonoscopy quality measures: experience from the NHS Bowel Cancer Screening Programme. Gut 2012; 61: 1050-1057
- 22 Arain MA, Sawhney M, Sheikh S. et al. CIMP status of interval colon cancers: another piece to the puzzle. Am J Gastroenterol 2010; 105: 1189-1195
- 23 Nishihara R, Ogino S, Chan AT. Colorectal-cancer incidence and mortality after screening. NEJM 2013; 369: 2355
- 24 Hazewinkel Y, Lopez-Ceron M, East JE. et al. Endoscopic features of sessile serrated adenomas: validation by international experts using high-resolution white-light endoscopy and narrow-band imaging. Gastrointest Endosc 2013; 77: 916-924
- 25 Ignjatovic A, East JE, Suzuki N. et al. Optical diagnosis of small colorectal polyps at routine colonoscopy (Detect InSpect ChAracterise Resect and Discard; DISCARD trial): a prospective cohort study. Lancet Oncol 2009; 10: 1171-1178
- 26 Rex DK. Narrow-band imaging without optical magnification for histologic analysis of colorectal polyps. Gastroenterology 2009; 136: 1174-1181
- 27 East JE, Vleugels JL, Roelandt P. et al. Advanced endoscopic imaging: European Society of Gastrointestinal Endoscopy (ESGE) Technology Review. Endoscopy 2016; 48: 1029-1045
- 28 Rex DK, Kahi C, O'Brien M. et al. The American Society for Gastrointestinal Endoscopy PIVI (Preservation and Incorporation of Valuable Endoscopic Innovations) on real-time endoscopic assessment of the histology of diminutive colorectal polyps. Gastrointest Endosc 2011; 73: 419-422
- 29 Kaminski MF, Hassan C, Bisschops R. et al. Advanced imaging for detection and differentiation of colorectal neoplasia: European Society of Gastrointestinal Endoscopy (ESGE) Guideline. Endoscopy 2014; 46: 435-449
- 30 Zorzi M, Senore C, Da Re F. et al. Detection rate and predictive factors of sessile serrated polyps in an organised colorectal cancer screening programme with immunochemical faecal occult blood test: the EQuIPE study (Evaluating Quality Indicators of the Performance of Endoscopy). Gut 2017; 66: 1233-1240
- 31 Hilsden RJ, Bridges R, Dube C. et al. Defining benchmarks for adenoma detection rate and adenomas per colonoscopy in patients undergoing colonoscopy due to a positive fecal immunochemical test. Am J Gastroenterol 2016; 111: 1743-1749
- 32 de Jonge V, Sint Nicolaas J, Cahen DL. et al. Quality evaluation of colonoscopy reporting and colonoscopy performance in daily clinical practice. Gastrointest Endosc 2012; 75: 98-106
- 33 Chen SC, Rex DK. Endoscopist can be more powerful than age and male gender in predicting adenoma detection at colonoscopy. Am J Gastroenterol 2007; 102: 856-861
- 34 Bretagne JF, Hamonic S, Piette C. et al. Variations between endoscopists in rates of detection of colorectal neoplasia and their impact on a regional screening program based on colonoscopy after fecal occult blood testing. Gastrointest Endosc 2010; 71: 335-341
- 35 Imperiale TF, Glowinski EA, Juliar BE. et al. Variation in polyp detection rates at screening colonoscopy. Gastrointest Endosc 2009; 69: 1288-1295
- 36 IJspeert JE, van Doorn SC, van der Brug YM. et al. The proximal serrated polyp detection rate is an easy-to-measure proxy for the detection rate of clinically relevant serrated polyps. Gastrointest Endosc 2015; 82: 870-877
- 37 IJspeert JE, de Wit K, van der Vlugt M. et al. Prevalence, distribution and risk of sessile serrated adenomas/polyps at a center with a high adenoma detection rate and experienced pathologists. Endoscopy 2016; 48: 740-746
- 38 Vleugels JLA, Dijkgraaf MGW, Hazewinkel Y. et al. Effects of training and feedback on accuracy of predicting rectosigmoid neoplastic lesions and selection of surveillance intervals by endoscopists performing optical diagnosis of diminutive polyps. Gastroenterology 2018; 154: 1682-1693.e1
- 39 National Institute for Public Health and the Environment (Ministry of Health, Welfare and Sport). Protocol for the Dutch Bowel Cancer Screening Programme [In Dutch]. 2009
- 40 National Institute for Public Health and the Environment (Ministry of Health, Welfare and Sport). Protocol for the authorization and auditing of colonoscopy centers and endoscopists, version 1. National Screening Programme for Bowel Cancer [In Dutch]. 2012
- 41 IJspeert JE, Bastiaansen BA, van Leerdam ME. et al. Development and validation of the WASP classification system for optical diagnosis of adenomas, hyperplastic polyps and sessile serrated adenomas/polyps. Gut 2016; 65: 963-970
- 42 Rees CJ, Bevan R, Zimmermann-Fraedrich K. et al. Expert opinions and scientific evidence for colonoscopy key performance indicators. Gut 2016; 65: 2045-2060
- 43 Rees CJ, Thomas GibsonS, Rutter MD. et al. UK key performance indicators and quality assurance standards for colonoscopy. Gut 2016; 65: 1923-1929
- 44 Ekkelenkamp VE, Dowler K, Valori RM. et al. Patient comfort and quality in colonoscopy. World J Gastroenterol 2013; 19: 2355-2361
- 45 Lai EJ, Calderwood AH, Doros G. et al. The Boston bowel preparation scale: a valid and reliable instrument for colonoscopy-oriented research. Gastrointest Endosc 2009; 69: 620-625
- 46 Castor Electronic Data Capture. Amsterdam: 2016 Available from: Accessed: 30 March 2020 https://www.castoredc.com/
- 47 Bosman FT, Carneiro F, Hruban RH. et al. WHO Classification of Tumours of the Digestive System. 4th. edn. Lyon, France: IARC; 2010
- 48 Dekker EL, van Leerdam ME, Hazewinkel Y. et al. Nederlandse Richtlijn Coloscopie Surveillance. Available from: Accessed: 25 March 2020 2013 http://wwwmdlnl/uploads/240/1308/Richtlijn_Coloscopie_Surveillance_definitief_2013.pdf
- 49 Atkins L, Hunkeler EM, Jensen CD. et al. Factors influencing variation in physician adenoma detection rates: a theory-based approach for performance improvement. Gastrointest Endosc 2016; 83: 617-626 e2
- 50 Pohl H, Bensen SP, Toor A. et al. Quality of optical diagnosis of diminutive polyps and associated factors. Endoscopy 2016; 48: 817-822
- 51 Vleugels JL, Hazewinkel Y, Fockens P. et al. Natural history of diminutive and small colorectal polyps: a systematic literature review. Gastrointest Endosc 2017; 85: 1169-1176.e1