Skip to main content
Download PDF

The impact of endoscopist performance and patient factors on distal adenoma detection and colorectal cancer incidence

BMC Gastroenterology volume 24, Article number: 44 (2024) Cite this article

Abstract

Background

High quality endoscopy is key for detecting and removing precursor lesions to colorectal cancer (CRC). Adenoma detection rates (ADRs) measure endoscopist performance. Improving other components of examinations could increase adenoma detection.

Aims

To investigate how endoscopist performance at flexible sigmoidoscopy (FS) affects adenoma detection and CRC incidence.

Methods

Among 34,139 participants receiving FS screening by the main endoscopist at one of 13 centres in the UK FS Screening Trial, median follow-up was 17 years. Factors examined included family history of CRC, bowel preparation quality, insertion and withdrawal time, bowel segment reached, patient pain and ADR. Odds ratios (OR) for distal adenoma detection were estimated by logistic regression. Hazard ratios (HR) for distal CRC incidence were estimated by Cox regression.

Results

At screening, 4,104 participants had distal adenomas detected and 168 participants developed distal CRC during follow-up. In multivariable models, a family history of CRC (yes vs. no: OR 1.40, 95%CI 1.21–1.62), good or adequate bowel preparation quality (vs. excellent: OR 0.84, 95%CI 0.74–0.95; OR 0.56, 95%CI 0.49–0.65, respectively) and longer insertion and withdrawal times (≥ 4.00 vs. < 2.00 min: OR 1.96, 95%CI 1.68–2.29; OR 32.79, 95%CI 28.22–38.11, respectively) were associated with adenoma detection. Being screened by endoscopists with low or intermediate ADRs, compared to high ADRs, was positively associated with CRC incidence (multivariable: HR 4.71, 95%CI 2.65–8.38; HR 2.16, 95%CI 1.22–3.81, respectively).

Conclusions

Bowel preparation quality and longer insertion and withdrawal time are key for improving distal adenoma detection. Higher ADRs were associated with a lower risk of distal CRC.

Peer Review reports

Introduction

Colorectal cancer (CRC) is the fourth most common cancer with over 42,000 cases diagnosed in the UK annually [1]. Effective screening for CRC enables the removal of precursor lesions, preventing CRC, and the detection of CRC at an earlier stage, significantly improving patient outcomes [2, 3].

Flexible sigmoidoscopy (FS) involves inserting a thin tube into the rectum to visualise ~ 60 cm of the distal colorectum [4]. FS screening reduces CRC incidence and mortality [5,6,7,8]; in the UK Flexible Sigmoidoscopy Screening Trial (UKFSST), CRC incidence and mortality was reduced by 35% and 41%, respectively, in those screened compared to controls [9].

Endoscopic examination accuracy is dependent on endoscopist skill and experience, with higher quality exams associated with better patient outcomes [10]. Adenoma detection rates (ADRs) are used to assess endoscopist performance [11]. Low ADRs are associated with higher rates of interval CRCs [12] and post-colonoscopy CRC mortality [13]. Large variability exists in ADRs between endoscopists [14,15,16], with quality of bowel preparation [17, 18], depth of endoscope insertion, segment of bowel reached and withdrawal time all related to ADRs [14]. Higher quality withdrawal techniques are associated with lower miss rates for adenomas [19].

The Joint Advisory Group on gastrointestinal endoscopy, the British Society of Gastroenterology and the Association of Coloproctology of Great Britain and Ireland have developed key performance indicators (KPIs) for endoscopy, which include ADRs, bowel preparation quality, withdrawal time, comfort and completeness of examination [20]. These KPIs are accompanied by quality assurance measures, which provide minimal standards and aspirational targets for endoscopists [20]. However, there is a lack of data on KPIs and long-term outcomes. The UKFSST offers the opportunity to examine KPIs in relation to adenoma detection and distal CRC incidence.

Methods

Study design

Between November 1994 and March 1999, the UKFSST recruited men and women aged 55–64 years from general practices serving 14 UK hospitals; details reported previously [9]. Adenoma incidence increases after the age of 50 years but levels out before 60 years [15, 21]; screening around 60 years of age offered the optimum opportunity to detect adenomas [21]. Participants were excluded if they were unable to provide consent; had a history of CRC, adenomas or inflammatory bowel disease; had severe/terminal disease, life expectancy of < 5 years, or a sigmoidoscopy/colonoscopy within the previous 3 years. Eligible individuals were randomised to either the intervention (n = 57,237, invitation to once-only FS screening), or control arm (n = 113,195, no screening and no further contact) (Fig. 1).

Fig. 1
figure 1

Study Profile. †784 patients whose FS screening was performed by an endoscopist other than the main endoscopist at that centre, 536 patients screened at one pilot centre that had far fewer participants than the other centres and where there were two main endoscopists rather than one, 367 patients who were screened within the first two months at one centre where the pathologist was found to be over-diagnosing adenomas, 93 participants with CRC diagnosed at baseline and 4,361 participants whose exam was classed as incomplete by the endoscopist. ‡Four patients had incident CRC diagnosed at both sub-sites. §Three patients had CRC as the underlying cause of death but the sub-site specific cause could not be determined as CRC was diagnosed at both sub-sites

Full size image

We excluded those who died or were diagnosed with CRC pre-randomisation, those in a family history study receiving colonoscopy screening, those screened by an endoscopist other than the main endoscopist at each centre, those in the pilot centre, those screened within the first two months at one centre where the pathologist was over-diagnosing adenomas, those diagnosed with CRC at baseline and those with incomplete exams (Fig. 1). Of the 34,139 participants remaining, 1,810 received multiple FS examinations (89% repeated due to poor bowel preparation quality; Supplementary Table 1). Only one exam per participant was included in the analysis; if FS was repeated due to poor bowel preparation, the last complete exam was included, but if FS was repeated for other reasons, the earliest complete exam was used. If any exams had polyps detected, these rules were applied within exams with polyps only.

Endoscopists were registrar-level gastroenterologists/surgeons with 3–8 years of experience post-basic medical qualification and must have performed a minimum of 50 supervised and 100 unsupervised endoscopies [15]. Participants were to administer a single phosphate enema (Fletchers’ phosphate enema; Forest Laboratories UK Ltd., Bexley, Kent), one hour before leaving home for their examination [15]. Sedation was not routinely used during FS examination [15]. All endoscopists were to advance the scope (60 cm Olympus video-endoscope (CF-200S)) as far as possible without causing undue discomfort (normally to the sigmoid colon/descending colon junction) and to remove polyps < 10 mm, leaving intact polyps < 3 mm deemed to be hyperplastic in the distal 4 cm of the rectum [15]. Follow-up colonoscopy was arranged for participants at high risk (≥ 3 adenomas, a polyp ≥ 10 mm, an adenoma with villous/tubulovillous histology, or high-grade dysplasia, malignant disease, or \(\ge\) 20 hyperplastic polyps above the distal rectum) [15].

Exposures

We examined endoscopist-reported variables of bowel preparation quality (Supplementary Table 2), time to maximum point of insertion, withdrawal time from maximum point of insertion, and segment of bowel reached. A pre-examination questionnaire assessed family history of CRC in first-degree relatives and a post-examination questionnaire assessed the level of pain experienced (none, mild, quite a lot, severe) during FS.

UKFSST endoscopists were previously ranked by their ADR (estimated as the proportion of participants that had \(\ge\) 1 distal adenoma detected) into high-, intermediate-, or low-detectors, with corresponding ADRs of 15%, 12% and 9%, respectively [15]; these groups were used in this analysis. The order in which participants were screened revealed a learning effect for the endoscopists’ ADR [15]; thus, we created a variable that grouped participants according to the order of examination occurrence: the first 500 participants examined by each endoscopist and those examined later.

Outcome ascertainment

Information on date, site and morphology of cancers and date of emigrations and deaths were collected from National cancer registries, the National Health Service (NHS) Central Register, National Services Scotland, NHS Digital and the Office for National Statistics.

Primary outcomes were distal adenomas and distal CRC incidence. Distal adenomas included adenomas detected at FS or any distal adenoma detected at follow-up colonoscopy (endoscopists were to leave polyps ≥ 10 mm for removal at colonoscopy). Distal CRCs, defined by the International Classification of Diseases 10th revision (ICD-10) and ICD for Oncology 2nd edition [22], included sites C18.7, C19 and C20 (rectum and sigmoid colon) and morphologies for invasive adenocarcinomas and carcinomas not otherwise specified for cancers diagnosed on clinical grounds only. The earliest distal CRC diagnosed per patient was included and follow-up time was not censored at diagnosis of proximal or unspecified site CRC.

Statistical analysis

Univariable and multivariable logistic regression was used to estimate odds ratios (OR) and 95% confidence intervals (CIs) for associations with distal adenoma detection. For distal CRC incidence, Cox models were used to estimate hazard ratios (HR) and 95% CIs. Time-at-risk started from baseline FS examination and was censored at emigration, death or the end of 2014. Non-proportionality was assessed using the Schoenfeld test; no violations were identified.

Initial univariable analyses included everyone with complete data on each variable, referred to as “full dataset” analyses. Multivariable analyses required data for all variables in the model, referred to as “complete-case” analyses; see Tables 1 and 2 for details. Insertion and withdrawal times were missing in ~ 40% of participants as this was not recorded until partway through the trial. Further sensitivity analyses were conducted excluding participants with multiple FS examinations.

Table 1 Detection of any distal adenoma by patient factors and endoscopist variables
Full size table
Table 2 Long-term distal colorectal cancer incidence by patient factors and endoscopist variables
Full size table

Multivariable models were constructed based on a-priori plans using previous research [14, 23] and included: age, sex, family history of CRC, bowel preparation quality, insertion time, withdrawal time, segment of bowel reached and patient-reported pain. The multivariable model for distal adenoma detection also included centre while that for distal CRC incidence included endoscopist ADR group and centre was omitted due to collinearity with ADR group. Kaplan–Meier estimates show time to distal CRC diagnosis.

Negative examinations were those with no findings in the colorectum (no lesions detected, no biopsies performed). Among those with negative examinations, we examined variation in KPIs, the associations between insertion time and pain and segment reached, and the associations between bowel preparation quality and pain and reaching the splenic flexure (SF). To examine if KPIs were associated with complexity of findings at FS, we investigated associations with the outcome of detection of multiple adenomas and/or any advanced adenoma (defined as adenomas \(\ge\) 10 mm, with high-grade dysplasia, or with villous/tubulovillous histology).

Analyses were performed using STATA/IC V.13.1 (StataCorp LP, 2013; Stata Statistical Software: Release 13; Texas, USA). Two-sided p-values < 0.05 were considered statistically significant. Ethical approval was obtained from local research ethics review committees for each centre (Multicentre Research Ethics Committee reference: 03/01/22). Trial registration: ISRCTN28352761. All individuals who underwent FS provided written informed consent prior to examination. The Patient Information Advisory Group (now Confidentiality Advisory Group) granted permission to obtain and process patient data (PIAG 4–07(j)/2002). All methods were carried out according to the relevant guidelines.

Results

The median age at FS was 60 years, 53% of participants were males and 11% had ≥ 1 first degree relative with CRC (Table 1). Bowel preparation quality was excellent for 43%. Median insertion and withdrawal times were 2.4 (IQR 1.7–3.4) and 1.9 (IQR 1.2–3.4) minutes, respectively. Most examinations reached the descending colon or further (78%) and 29% of participants reported feeling no pain during the examination (Table 1).

Variables were examined by centre, synonymous with endoscopist, among the 70% of participants with negative examinations (Supplementary Table 3). ‘Excellent’ bowel preparation quality varied between 9.6% (centre 9) and 68.2% (centre 4). Median insertion time varied from 1.45 (IQR 1.03–2.07; centre 4) to 3.88 (IQR, 2.92–5.50; centre 10) minutes and median withdrawal time varied from 0.88 (IQR 0.65–1.27; centre 4) to 2.38 (IQR 1.90–3.06; centre 5) minutes. Examinations reaching the descending colon varied between 27.7% (centre 13) and 84.1% (centre 8) and participants reporting severe pain varied between 0.2% (centre 4) and 4.1% (centre 8). Despite these differences between centres, there were no clear associations between these factors and endoscopist ADR when examining by ascending order of ADR (Supplementary Table 3).

Among negative examinations, the proportion of participants reporting quite a lot/severe pain tended to decrease with further segment reached (p-trends < 0.001). Females were more likely to report quite a lot/severe pain than males (15.5% vs. 8.0%, respectively, among exams reaching a maximum of the SF) and to have a longer time to maximum insertion for each section of the bowel reached (SF: median 2.37 min (IQR 1.75–3.45) vs. 2.14 min (IQR 1.58–2.90)) (Supplementary Table 4).

In complete-case analyses, 3,349 (14.4%) negative examinations reached at least the SF. Females were less likely to have an examination reaching the SF (10.9%) than males (18.2%) (multivariable: OR 0.57, 95%CI 0.53–0.62). Among those with negative exams, the odds of reaching the SF were 75% lower with ‘poor’ bowel preparation compared to ‘excellent’ (multivariable: OR 0.25 95%CI 0.13–0.50) and 47% lower with the reporting of severe pain compared to no pain (multivariable: OR 0.53 95%CI 0.38–0.73) (Supplementary Table 5).

Distal adenoma detection

There were 4,104 (12.0%) participants with ≥ 1 distal adenoma detected (Table 1). In all models, there were increased odds of distal adenoma detection with increasing age (multivariable: OR 1.03, 95%CI 1.01–1.04) (Table 1), with a family history of CRC, compared to without (multivariable: OR 1.40, 95%CI 1.21–1.62), and decreased odds in females compared to males (multivariable: OR 0.62, 95%CI 0.56–0.69).

Although there was no association in the full dataset, in complete-case models there were increased odds of distal adenoma detection for those with ‘poor’ bowel preparation compared to ‘excellent’ (multivariable: OR 2.88, 95%CI 1.25–6.60; Table 1), and lower odds for those with ‘good’ (multivariable: OR 0.84, 95%CI 0.74–0.95) or ‘adequate’ bowel preparation (multivariable: OR 0.56, 95%CI 0.49–0.65).

In all models, increasing insertion and withdrawal times were associated with distal adenoma detection (multivariable: OR ≥ 4.00 vs. < 2.00 min: 1.96, 95%CI 1.68–2.29; 32.79, 95%CI 28.22–38.11, respectively). In comparison to reaching the sigmoid/descending junction, reaching more proximally was associated with higher odds of distal adenoma detection in univariable models (full dataset, descending colon: OR 1.43, 95%CI 1.31–1.56; SF: OR 1.66, 95%CI 1.47–1.88); however, this attenuated in multivariable models.

In complete-case univariable models, there were lower odds of distal adenoma detection with increasing pain (severe compared to none: OR 0.69, 95%CI 0.51–0.95; Table 1) but this was not evident in the other models. In the full dataset, individuals whose FS screening occurred after their endoscopist’s first 500 examinations had increased odds of distal adenoma detection compared to those whose took place earlier (OR 1.32, 95%CI 1.20–1.45); multivariable models were not possible due to missing data.

Advanced and/or multiple adenomas

There were 919 (4.8%) participants with multiple and/or advanced distal adenomas in the complete-case dataset (Supplementary Table 6). Age, sex, family history, bowel preparation quality, insertion and withdrawal time, segment reached, patient pain and the order of FS occurrence were similarly associated with the detection of advanced and/or multiple adenomas as of any distal adenoma.

Distal CRC incidence

During a median follow-up of 17 years, 168 (0.5%) distal CRCs were diagnosed (Table 2). In the full dataset, females had a lower risk of distal CRC than males (HR 0.62, 95%CI 0.45–0.85) and those with a family history of CRC had a higher risk than those without (HR 1.65, 95%CI 1.09–2.50) (Table 2, Supplementary Fig. 1A-B); these effects attenuated in complete-case models.

Age, bowel preparation quality, segment of bowel reached, patient-reported pain, and order of examination occurrence were not associated with distal CRC incidence (Table 2, Supplementary Fig. 1C–F). Although overall the associations for insertion and withdrawal times were not statistically significant, those in the top category of ≥ 4.00 min (versus < 2.00 min) had an increased risk of distal CRC (multivariable: HR 1.81, 95%CI 1.00–3.27; HR 1.93, 95%CI 1.14–3.24, respectively) (Table 2, Supplementary Fig. 1G-H).

Compared to those examined by high-detectors, individuals examined by low-detectors had an increased risk of distal CRC (multivariable: HR 4.71, 95%CI 2.65–8.38), as did those examined by intermediate-detectors in complete-case models only (multivariable: HR 2.16, 95%CI 1.22–3.81) (Table 2, Supplementary Fig. 1I).

Excluding participants with multiple FS examinations (n = 1,810) did not materially alter the results for distal adenoma detection or long-term colorectal cancer incidence in any of the models.

Discussion

We investigated factors that could improve the quality of FS examinations, increase adenoma detection, and reduce CRC incidence. We found that multiple variables were associated with adenoma detection, including patient age, sex, family history of CRC, bowel preparation quality, insertion time and withdrawal time. For long-term outcomes, patients who were examined by endoscopists with higher ADRs had a lower risk of distal CRC incidence.

Individuals with a family history of CRC or its precursor lesions are at increased risk of CRC compared to those without [24]; similarly, we found a positive association between family history of CRC and distal adenoma detection at FS screening [25]. Participants provided family history information on the pre-screening questionnaire, which the endoscopist may have accessed, potentially motivating them to conduct a more thorough FS examination.

Bowel preparation plays a crucial role in the quality and completeness of endoscopic examinations, with higher levels of cleanliness associated with optimum views of the colon [26] and improved ADRs [23]. Compared to having ‘excellent’ bowel preparation, we found lower odds of adenoma detection among those having ‘good’ or ‘adequate’ and increased odds among those having ‘poor’. Among participants with poor bowel preparation at first FS, those who had adenomas detected that triggered referral to colonoscopy would not have had a repeat FS to improve the bowel preparation quality; however, those without high-risk adenomas detected would have undergone a repeat FS, likely improving the bowel preparation quality. This could contribute to poor bowel preparation being positively associated with adenoma detection. We were unable to examine poor bowel preparation quality and distal CRC incidence due to a lack of cases, attributed to the fact that we only included complete examinations.

In contrast to previous findings, which either reported no correlation between adenoma detection and longer insertion time [27] or decreased adenoma detection with longer insertion times [28, 29], we found that longer insertion time was associated with greater adenoma detection. Within the UKFSST, endoscopists were to remove polyps ≤ 5 mm during insertion to avoid difficulties relocating them on withdrawal, remove polyps 6-9 mm during withdrawal, and leave polyps ≥ 10 mm for removal at colonoscopy. Therefore, longer insertion times in this study could be associated with the presence of numerous polyps ≤ 5 mm requiring resection and/or very large adenomas needing endoscopic assessment/photo-documentation. We also found increased odds of detecting multiple and/or advanced adenomas in those with longer insertion times. In our study there was no fixed endpoint for FS examinations and further reach of the sigmoidoscope during an examination would naturally lead to longer insertion and withdrawal times and a higher chance of adenoma detection. However, in multivariable models we adjusted for segment reached, insertion time and withdrawal time. Quality of bowel preparation has been associated with longer insertion times [30, 31]. Advancing a sigmoidoscope through a bowel with poorer preparation requires more cleaning to obtain good views of the mucosa, potentially increasing insertion times. However, in our multivariable model including both insertion time and bowel preparation quality, the association between insertion time and adenoma detection remained.

Higher quality withdrawal techniques are associated with fewer missed adenomas. Colonoscopists with lower miss rates for adenomas had longer examination times compared to those with higher miss rates [19]. We found that longer withdrawal times were associated with increased adenoma detection, which is unsurprising due to the time taken to remove lesions < 10 mm during FS. Although larger lesions would not have been removed during FS, they would likely increase the examination time. For distal CRC incidence, only the longest withdrawal time category was associated with increased risk; this can likely be attributed to patients with long withdrawal times having more advanced pathology and inherently being at higher risk rather than reflecting the quality of the endoscopist’s withdrawal. There is no minimum recommended withdrawal time for FS, unlike for colonoscopy [20]. A previous study suggested a FS withdrawal time of at least 3.25 min from the SF and, to maximise ADRs, specified an aim of 3.5–4.0 minutes [14]; although this has not been validated, our data supports this recommendation.

FS with a 60 cm maximum scope insertion distance can reach the SF and sometimes beyond [32]. In our study, the majority (78%) of examinations were judged by the endoscopist to have reached at least the descending colon with 15% reaching at least the SF. It is important that the sigmoidoscope reaches as high as comfortably possible to maximise the mucosa examined, increasing the effectiveness of the examination [33, 34]. In our univariable analyses, the chance of detecting an adenoma was greater when at least the descending colon was reached, although this effect attenuated in multivariable models. Previously, inadequate examinations (e.g., insertion of the scope < 50 cm) were associated with female sex and advancing age, with the majority of incomplete examinations due to patient discomfort [34]. In agreement with this, we found decreased odds of reaching the SF for females, those who reported more pain, and those with poorer bowel preparation quality among those with negative examinations [14]. However, we found no clear association between patient-reported pain and adenoma detection or distal CRC incidence. Identifying factors that could reduce levels of pain could result in more complete examinations, lessening the chances of negative experiences that could compromise attendance at future examinations.

We found that adenomas were more likely to be detected at examinations conducted after an endoscopist’s first 500 examinations, suggesting a learning effect, consistent with previous analyses [15]; although we cannot be certain that participants examined within an endoscopist’s first 500 examinations had adenomas missed at baseline. It has been reported that for each 1% increase in the ADR, there is an associated 3% decreased risk of post-colonoscopy CRC [13] and that greater long-term protection from CRC is observed when FS screening is conducted by endoscopists with higher ADRs [35]. We found an almost five-fold increase in distal CRC incidence for individuals screened by low-detectors compared to those screened by high-detectors; this suggests an ADR of 15%, observed among the high-detectors, should be considered as a minimal standard. Other factors could account for differences in ADR, including variations in equipment, screening protocols or endoscopists’ prior experience; these factors were controlled for in the study design/analysis, which lends more weight to the difference in ADRs reflecting real variability in endoscopist performance and consequent effects on CRC incidence [5].

Although seven variables were associated with adenoma detection, only endoscopist ADR group was associated with distal CRC, in addition to insertion and withdrawal times in the top categories only. These differences potentially demonstrate the importance of certain factors in adenoma detection but not necessarily cancer prevention, but differences in findings could be due to a lack of power for the distal CRC analyses.

Strengths of our study include the large, high-quality dataset with multiple KPI measures and long follow-up period. Participants were recruited throughout the UK, resulting in good generalisability of our findings. Complete endoscopic examinations are crucial as incomplete examinations are associated with higher numbers of interval cancers [36, 37]; we only included examinations classed by the endoscopist as complete. In addition, we only included examinations performed by the main endoscopist at each centre, which removed heterogeneity within centres introduced by multiple endoscopists. There were limitations, including missing data for insertion and withdrawal times, potential inaccuracy in classifying depth of insertion since imaging systems were not used and limited statistical power for distal CRC analyses. We were unable to exclude examination time used for polyp removal or endoscopic assessment/photo documentation of polyps, which may have contributed to the association between adenoma detection and longer insertion and withdrawal times. Additionally, since the trial screening was conducted there have been advances in the quality of endoscopic equipment and improvements in endoscopist training and monitoring; therefore, the number of adenomas detected today would likely be higher.

In conclusion, there is a lack of published data on KPIs and long-term CRC outcomes. Examining the impact of KPIs on adenoma detection and distal CRC incidence, we identified several variables associated with patient outcomes. Examinations with good or adequate bowel preparation quality had lower odds of adenoma detection, and longer insertion and withdrawal times had increased odds of adenoma detection. Patients examined by endoscopists with high ADRs had the lowest risk of distal CRC. We suggest an ADR of 15% should be set as a minimal standard. The importance of the detection and removal of adenomas cannot be understated; early detection of abnormalities is key in providing long-term protection against CRC. It is vital that each endoscopic procedure is conducted to the highest standard, so all patients receive the optimum benefit that screening can offer.

Parts of the reported results have been presented as a poster presentation [38].

Availability of data and materials

The data used in this current study is not available as it uses individual-level identifiable data, which is confidential. Requests regarding data should be directed to the corresponding author.

Abbreviations

AC:

Ascending colon

ADR:

Adenoma detection rate

CI:

Confidence interval

CM:

Caecum

CRC:

Colorectal cancer

DC:

Descending colon

FS:

Flexible sigmoidoscopy

HF:

Hepatic flexure

HR:

Hazard ratio

ICD-10:

International Classification of Diseases 10th revision

ISRCTN:

International Standard Randomised Controlled Trial Number

IQR:

Interquartile range

KPIs:

Key performance indicators

Mins:

Minutes

NHS:

National Health Service

OR:

Odds ratio

PIAG:

Patient Information Advisory Group

RM:

Rectum

RS:

Rectosigmoid

SC:

Sigmoid colon

SD:

Sigmoid descending

SF:

Splenic flexure

TC:

Transverse colon

TI:

Terminal ileum

UKFSST:

UK Flexible Sigmoidoscopy Screening Trial

References

  1. Cancer Research UK. Bowel cancer statistics - bowel cancer incidence. Available from: www.cancerresearchuk.org/health-professional/cancer-statistics/statistics-by-cancer-type/bowel-cancer#heading-Zero. Accessed Jan 2021.

  2. Levin B, Lieberman DA, McFarland B, Smith RA, Brooks D, Andrews KS, et al. Screening and surveillance for the early detection of colorectal cancer and adenomatous polyps, 2008: a joint guideline from the American Cancer Society, the US Multi-Society Task Force on Colorectal Cancer, and the American College of Radiology. CA Cancer J Clin. 2008;58(3):130–60.

    Article  PubMed  Google Scholar 

  3. Zauber A, Winawer S, O’Brien M, Landsdorp-Vogelaar I, van Ballegooijen M, Hankey B, et al. Colonoscopic polypectomy and long-term prevention of colorectal-cancer deaths. N Engl J Med. 2012;336(8):687–96.

    Article  Google Scholar 

  4. Cunningham D, Atkin W, Lenz H-J, Lynch H, Minsky B, Nordlinger B, et al. Colorectal cancer. Lancet. 2010;375:1030–47.

    Article  PubMed  Google Scholar 

  5. Atkin WS, Edwards R, Kralj-Hans I, Wooldrage K, Hart AR, Northover JMA, et al. Once-only flexible sigmoidoscopy screening in prevention of colorectal cancer: a multicentre randomised controlled trial. The Lancet. 2010;375(9726):1624–33.

    Article  Google Scholar 

  6. Segnan N, Armaroli P, Bonelli L, Risio M, Sciallero S, Zappa M, et al. Once-only sigmoidoscopy in colorectal cancer screening: follow-up findings of the Italian randomized controlled trial–SCORE. J Natl Cancer Inst. 2011;103(17):1310–22.

    Article  PubMed  Google Scholar 

  7. Schoen RE, Pinsky PF, Weissfeld JL, Yokochi LA, Church T, Laiyemo AO, et al. Colorectal-cancer incidence and mortality with screening flexible sigmoidoscopy. N Engl J Med. 2012;366(25):2345–57.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Holme O, Loberg M, Kalager M, Bretthauer M, Hernan MA, Aas E, et al. Effect of flexible sigmoidoscopy screening on colorectal cancer incidence and mortality: a randomized clinical trial. JAMA. 2014;312(6):606–15.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Atkin W, Wooldrage K, Parkin DM, Kralj-Hans I, MacRae E, Shah U, et al. Long term effects of once-only flexible sigmoidoscopy screening after 17 years of follow-up: the UK flexible sigmoidoscopy screening randomised controlled trial. Lancet. 2017;389(10076):1299–311.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Rutter MD, Rees CJ. Quality in gastrointestinal endoscopy. Endoscopy. 2014;46(6):526–8.

    Article  PubMed  Google Scholar 

  11. Rex DK. Polyp detection at colonoscopy: endoscopist and technical factors. Best Pract Res Clin Gastroenterol. 2017;31(4):425–33.

    Article  PubMed  Google Scholar 

  12. Kaminski MF, Regula JR, Kraszewska E, Polkowski M, Wojciechowska U, Didkowska J, et al. Quality indicators for colonoscopy and the risk of interval cancer. N Engl J Med. 2010;362:1795–803.

    Article  CAS  PubMed  Google Scholar 

  13. Corley DA, Jensen CD, Marks AR, Zhao WK, Lee JK, Doubeni CA, et al. Adenoma detection rate and risk of colorectal cancer and death. N Engl J Med. 2014;370(14):1298–306.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Bevan R, Blanks R, Nickerson C, Saunders B, Stebbing J, Tighe R, et al. Factors affecting adenoma detection rate in a national flexible sigmoidoscopy screening programme: a retrospective analysis. Lancet Gastroenterol Hepatol. 2019;4(3):239–47.

    Article  PubMed  Google Scholar 

  15. Atkin W, Rogers P, Cardwell C, Cook C, Cuzick J, Wardle J, et al. Wide variation in adenoma detection rates at screening flexible sigmoidoscopy. Gastroenterology. 2004;126(5):1247–56.

    Article  PubMed  Google Scholar 

  16. Pinsky PF, Schoen RE, Weissfeld JL, Kramer B, Hayes RB, Yokochi L; PLCO Project Team. Variability in flexible sigmoidoscopy performance among examiners in a screening trial. Clin Gastroenterol Hepatol. 2005;3(8):792–7.

  17. Lebwohl B, Kastrinos F, Glick M, Rosenbaum AJ, Wang T, Neugut AI. The impact of suboptimal bowel preparation on adenoma miss rates and the factors associated with early repeat colonoscopy. Gastrointest Endosc. 2011;73(6):1207–14.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Issa IA, Noureddine M. Colorectal cancer screening: An updated review of the available options. World J Gastroenterol. 2017;23(28):5086–96.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Rex DK. Colonoscopic withdrawal technique is associated with adenoma miss rates. Gastrointest Endosc. 2000;51:3.

    Article  Google Scholar 

  20. Rees CJ, Thomas Gibson S, Rutter MD, Baragwanath P, Pullan R, Feeney M, et al. UK key performance indicators and quality assurance standards for colonoscopy. Gut. 2016;65(12):1923–9.

    Article  PubMed  Google Scholar 

  21. Atkin WS, Cuzick J, Northover JM, Whynes DK. Prevention of colorectal cancer by once-only sigmoidoscopy. Lancet. 1993;341(8847):736–40.

    Article  CAS  PubMed  Google Scholar 

  22. Percy C, Holten VV, Muir CS. International classification of diseases for oncology. Percy C, Holten V, Muir C, editors, 2nd. Geneva: World Health Organization; 1990.

  23. Thomas-Gibson S, Rogers P, Cooper S, Man R, Rutter MD, Suzuki N, et al. Judgement of the quality of bowel preparation at screening flexible sigmoidoscopy is associated with variability in adenoma detection rates. Endoscopy. 2006;38(5):456–60.

    Article  CAS  PubMed  Google Scholar 

  24. Song M, Emilsson L, Roelstraete B, Ludvigsson JF. Risk of colorectal cancer in first degree relatives of patients with colorectal polyps: nationwide case-control study in Sweden. BMJ. 2021;373:n877.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Fracchia M, Senore C, Armaroli P, Ferraris R, Placido RD, Musso A, et al. Assessment of the multiple components of the variability in the adenoma detection rate in sigmoidoscopy screening, and lessons for training. Endoscopy. 2010;42(6):448–55.

    Article  CAS  PubMed  Google Scholar 

  26. Froehlich F, Wietlisbach V, Gonvers J-J, Burnand B, Vader J-P. Impact of colonic cleansing on quality and diagnostic yield of colonoscopy- the European panel of appropriateness of gastrointestinal endoscopy European multicenter study. Gastrointest Endosc. 2005;61(3):378–84.

    Article  PubMed  Google Scholar 

  27. Fritz CDL, Smith ZL, Elsner J, Hollander T, Early D, Kushnir V. Prolonged cecal insertion time is not associated with decreased adenoma detection when a longer withdrawal time is achieved. Dig Dis Sci. 2018;63(11):3120–5.

    Article  PubMed  Google Scholar 

  28. von Renteln D, Robertson DJ, Bensen S, Pohl H. Prolonged cecal insertion time is associated with decreased adenoma detection. Gastrointest Endosc. 2017;85(3):574–80.

    Article  Google Scholar 

  29. Yang MH, Cho J, Rampal S, Choi EK, Choi Y-H, Lee JH, et al. The association between cecal insertion time and colorectal neoplasm detection. BMC Gastroenterol. 2013;13(1):124.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Wong MCS, Ching JYL, Chan VCW, Lam TYT, Luk AKC, Tang RSY, et al. Determinants of bowel preparation quality and its association with adenoma detection: a prospective colonoscopy study. Medicine (Baltimore). 2016;95(2):e2251.

    Article  PubMed  Google Scholar 

  31. Kim WH, Cho YJ, Park JY, Min PK, Kang JK, Park IS. Factors affecting insertion time and patient discomfort during colonoscopy. Gastrointest Endosc. 2000;52(5):600–5.

    Article  CAS  PubMed  Google Scholar 

  32. Adebogun AO, Berg CD, Laiyemo AO. Concerns and challenges in flexible sigmoidoscopy screening. Colorectal Cancer. 2012;1(4):309–19.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Doria-Rose VP, Newcomb PA, Levin TR. Incomplete screening flexible sigmoidoscopy associated with female sex, age, and increased risk of colorectal cancer. Gut. 2005;54(9):1273–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Laiyemo AO, Doubeni C, Pinsky PF, Doria-Rose VP, Sanderson AK 2nd, Bresalier R, et al. Factors associated with inadequate colorectal cancer screening with flexible sigmoidoscopy. Cancer Epidemiol. 2012;36(4):395–9.

    Article  PubMed  Google Scholar 

  35. Cross AJ, Robbins EC, Saunders BP, Duffy SW, Wooldrage K. Higher adenoma detection rates at screening associated with lower long-term colorectal cancer incidence and mortality. Clin Gastroenterol Hepatol. 2022;20(2):e148–67.

  36. Brenner H, Chang-Claude J, Seiler CM, Hoffmeister M. Interval cancers after negative colonoscopy: population-based case-control study. Gut. 2012;61(11):1576–82.

    Article  PubMed  Google Scholar 

  37. Kaminski MF, Thomas-Gibson S, Bugajski M, Bretthauer M, Rees CJ, Dekker E, et al. Performance measures for lower gastrointestinal endoscopy: a European Society of Gastrointestinal Endoscopy (ESGE) Quality Improvement Initiative. Endoscopy. 2017;49(4):378–97.

    Article  PubMed  Google Scholar 

  38. Power S, Wooldrage K, Cross A. P190 The impact of endoscopist performance on distal adenoma detection and colorectal cancer incidence. Gut. 2022;71(Suppl 1):A133.

    Google Scholar 

Download references

Acknowledgements

CSPRG: Wendy Atkin, Mariano Perdices Kalfors, Paul Greliak, Iain Stenson, Salman Shahrezaei. Trial Steering Committee: M Parmar (Chair), R Valori, A Gray, J Patnick, A Mackie, L Berkman.

We thank the general practitioners, hospital staff, and the men and women who took part in this study.

Funding

Currently, this trial is funded by the National Institute for Health Research (NIHR) Health Technology Assessment (HTA) ref: 16/65/01. The work of the Cancer Screening and Prevention Research Group (CSPRG) at Imperial College London is also supported by Cancer Research UK (C53889/A25004). SP is funded by a Cancer Research UK studentship award (A27007).

Author information

Authors and Affiliations

  1. Cancer Screening and Prevention Research Group (CSPRG), Department of Surgery and Cancer, St Mary’s Hospital, Imperial College London, London, W2 1NY, UK

    Sharon Power, Kate Wooldrage & Amanda J. Cross

  2. Department of Surgery and Cancer, Imperial College London, London, UK

    Brian P. Saunders

  3. Department of Gastroenterology, St Mark’s Hospital and Academic Institute, London, UK

    Brian P. Saunders

Authors
  1. Sharon Power
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kate Wooldrage
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Brian P. Saunders
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Amanda J. Cross
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

SP, KW and AJC: conception and design; analysis and interpretation of the data; drafting of the article; All authors: critical revision of the article for important intellectual content and final approval of the article.

Corresponding author

Correspondence to Sharon Power.

Ethics declarations

Ethics approval and consent to participate

Ethical approval was obtained from local research ethics review committees for each centre (Multicentre Research Ethics Committee reference: 03/01/22). Trial registration: ISRCTN28352761. All individuals who underwent FS provided written informed consent prior to examination. The Patient Information Advisory Group (now Confidentiality Advisory Group) granted permission to obtain and process patient data (PIAG 4–07(j)/2002). All the methods were carried out according to the relevant guidelines.

Consent for publication

Not applicable.

Competing interests

BPS has done consultancy work, been a speaker for, had loan equipment and a research grant from Olympus in the last 3 years; all other authors report no conflicts of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Additional file 1: Supplementary Table 1.

Reasons for repeat flexible sigmoidoscopy. Supplementary Table 2. Protocol guidelines for the categorisation of bowel preparation quality. Supplementary Table 3. Endoscopist variables by endoscopist for negative examinations*. Supplementary Table 4. Patient-reported pain and insertion time by extent of examination in negative examinations*. Supplementary Table 5. Reaching the splenic flexure in negative examinations* by age, sex, bowel preparation quality, and pain. Supplementary Table 6. Detection of multiple and/or advanced distal adenomas by patient factors and endoscopist variables. Supplementary Figure 1. Cumulative distal colorectal cancer incidence in all eligible participants by patient factors and endoscopist variables (the full dataset).

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Power, S., Wooldrage, K., Saunders, B.P. et al. The impact of endoscopist performance and patient factors on distal adenoma detection and colorectal cancer incidence. BMC Gastroenterol 24, 44 (2024). https://doi.org/10.1186/s12876-024-03125-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s12876-024-03125-x

Keywords

BMC Gastroenterology

ISSN: 1471-230X

Contact us