Adjusting Detection Measures for Colonoscopy: How Far Should We Go?

Abstract

The adenoma detection rate (ADR) was proposed as a colonoscopy quality metric in 2002 by the US Multi-Society Task Force (USMSTF).1Rex D.K. Bond J.H. Winawer S. et al.Quality in the technical performance of colonoscopy and the continuous quality improvement process for colonoscopy: recommendations of the U.S. Multi-Society Task Force on Colorectal Cancer.Am J Gastroenterol. 2002; 97: 1296-1308Crossref PubMed Scopus (834) Google Scholar Subsequently, consistent wide variation in ADR among colonoscopists was documented2Barclay R.L. Vicari J.J. Doughty A.S. et al.Colonoscopic withdrawal times and adenoma detection during screening colonoscopy.N Engl J Med. 2006; 355: 2533-2541Crossref PubMed Scopus (1028) Google Scholar,3Chen S.C. Rex D.K. Endoscopist can be more powerful than age and male gender in predicting adenoma detection at colonoscopy.Am J Gastroenterol. 2007; 102: 856-861Crossref PubMed Scopus (324) Google Scholar and the measure was validated as a predictor of postcolonoscopy cancer.4Kaminski M.F. Regula J. Kraszewska E. et al.Quality indicators for colonoscopy and the risk of interval cancer.N Engl J Med. 2010; 362: 1795-1803Crossref PubMed Scopus (1268) Google Scholar,5Corley D.A. Jensen C.D. Marks A.R. et al.Adenoma detection rate and risk of colorectal cancer and death.N Engl J Med. 2014; 370: 1298-1306Crossref PubMed Scopus (971) Google Scholar The ADR is a priority colonoscopy quality measure.6Rex D.K. Schoenfeld P.S. Cohen J. et al.Quality indicators for colonoscopy.Gastrointest Endosc. 2015; 81: 31-53Abstract Full Text Full Text PDF PubMed Scopus (513) Google Scholar Table 1 lists alternatives or possible add-ons to ADR as detection measures, in descending order of their direct relationship to the desired outcome of preventing cancer, together with weaknesses of each measure. Asking endoscopists to measure ADR is an effort to regulate colonoscopy withdrawal technique. Because of this regulatory aspect, from the outset1Rex D.K. Bond J.H. Winawer S. et al.Quality in the technical performance of colonoscopy and the continuous quality improvement process for colonoscopy: recommendations of the U.S. Multi-Society Task Force on Colorectal Cancer.Am J Gastroenterol. 2002; 97: 1296-1308Crossref PubMed Scopus (834) Google Scholar there has been a major emphasis on using a measure that is hard to corrupt under prospective use. If a measure is easily gamed or corrupted, it is frustrating to all participants and can lead to failure of the measure, and potentially of the entire quality effort. In this regard, ADR does certain things well. ADR measures endoscopist performance rather than someone else’s performance, which for certain alternatives is the pathologist (Table 1). Second, ADR measures the detection skill of endoscopists, and not other skills such as size measurement or localization of lesions to colonic segment, both of which notoriously are inaccurate and would be subject to bias and gaming in prospective use. Arguably, the widespread acceptance that ADR accurately reflects detection skills rests on these features and has played a major role in its success.Table 1Alternatives to ADR and Their Weaknesses, Potential Add-Ons (Serrated Measures)AbbreviationWeaknesses PCCRCLong intervals; Extended follow-up period, large databases neededAdenoma measures AAMRLarge tandem study required AMRTandem study required AADRSize errors and size gaming by endoscopists; High interobserver variation among pathologists for high-grade dysplasia and villous elements APCHarder to measure; Could incentivize increased pathology charges ADRSubject to indication gaming (solved by expanding indications); One-and-done gaming possible PDRCould be corrupted in prospective use by removal of clinically unimportant polypsSerrated measures SSLDRaThere are multiple proposed variations of serrated targets, all of which are susceptible to size and colon location errors and gaming and pathology interobserver variation.Measures pathology bias and performance PSPDRaThere are multiple proposed variations of serrated targets, all of which are susceptible to size and colon location errors and gaming and pathology interobserver variation.,bSerrated polyp may be defined as all serrated class lesions (sessile serrated lesions, hyperplastic polyps, traditional serrated adenomas).Subject to variation in localization and location gaming TSPDRaThere are multiple proposed variations of serrated targets, all of which are susceptible to size and colon location errors and gaming and pathology interobserver variation.,bSerrated polyp may be defined as all serrated class lesions (sessile serrated lesions, hyperplastic polyps, traditional serrated adenomas).Incentivizes removal of diminutive rectosigmoid hyperplastic polypNOTE. Adenoma measures listed in decreasing order of their direct relationship to postcolonoscopy cancer.AADR, advanced adenoma detection rate; AAMR, advanced adenoma miss rate; ADR, adenoma detection rate; AMR, adenoma miss rate; APC, adenomas per colonoscopy; PCCRC, postcolonoscopy colorectal cancer; PDR, polyp detection rate; PSPDR, proximal serrated polyp detection rate; SSLDR, sessile serrated lesion detection rate; TSPDR, total serrated polyp detection rate.a There are multiple proposed variations of serrated targets, all of which are susceptible to size and colon location errors and gaming and pathology interobserver variation.b Serrated polyp may be defined as all serrated class lesions (sessile serrated lesions, hyperplastic polyps, traditional serrated adenomas). Open table in a new tab NOTE. Adenoma measures listed in decreasing order of their direct relationship to postcolonoscopy cancer. AADR, advanced adenoma detection rate; AAMR, advanced adenoma miss rate; ADR, adenoma detection rate; AMR, adenoma miss rate; APC, adenomas per colonoscopy; PCCRC, postcolonoscopy colorectal cancer; PDR, polyp detection rate; PSPDR, proximal serrated polyp detection rate; SSLDR, sessile serrated lesion detection rate; TSPDR, total serrated polyp detection rate. ADR and ADR improvement have been the subject of enormous investigation,6Rex D.K. Schoenfeld P.S. Cohen J. et al.Quality indicators for colonoscopy.Gastrointest Endosc. 2015; 81: 31-53Abstract Full Text Full Text PDF PubMed Scopus (513) Google Scholar which naturally has led to criticisms of ADR and suggestions to improve it. There are several commonly discussed questions about improving colonoscopy detection measures. The 3 broad categories of colonoscopy indications are surveillance, screening, and diagnostic. ADR is highest in surveillance, then screening, and lowest in diagnostic (with the exception of positive fecal screening tests).7Anderson J.C. Butterly L.F. Goodrich M. et al.Differences in detection rates of adenomas and serrated polyps in screening versus surveillance colonoscopies, based on the New Hampshire Colonoscopy Registry.Clin Gastroenterol Hepatol. 2013; 11: 1308-1312Abstract Full Text Full Text PDF PubMed Scopus (69) Google Scholar,8Rex D.K. Ponugoti P.L. Calculating the adenoma detection rate in screening colonoscopies only: is it necessary? Can it be gamed?.Endoscopy. 2017; 49: 1069-1074Crossref PubMed Scopus (40) Google Scholar Because screening ADR is between surveillance and diagnostic, the ADR for all 3 indications combined tends to be quite close to the screening ADR. This principle has been shown previously,8Rex D.K. Ponugoti P.L. Calculating the adenoma detection rate in screening colonoscopies only: is it necessary? Can it be gamed?.Endoscopy. 2017; 49: 1069-1074Crossref PubMed Scopus (40) Google Scholar and is nicely shown in 2 well-done studies in this issue of Clinical Gastroenterology and Hepatology.9Ladabaum U. Shepard J. Mannalithara A. Adenoma and serrated lesion detection by colonoscopy indication: the ADR-ESS (ADR Extended to all Screening/Surveillance) score.Clin Gastroenterol Hepatol. 2021; 19: 1873-1882Abstract Full Text Full Text PDF PubMed Scopus (2) Google Scholar,10Kaltenbach T. Gawron A. Meyer C.S. et al.Adenoma detection rate (ADR) irrespective of indication is comparable to screening ADR: implications for quality monitoring.Clin Gastroenterol Hepatol. 2021; 19: 1883-1889Abstract Full Text Full Text PDF Scopus (5) Google Scholar Using all 3 indication categories results in less variation in ADR over time, and narrowed CIs around measured ADR.9Ladabaum U. Shepard J. Mannalithara A. Adenoma and serrated lesion detection by colonoscopy indication: the ADR-ESS (ADR Extended to all Screening/Surveillance) score.Clin Gastroenterol Hepatol. 2021; 19: 1873-1882Abstract Full Text Full Text PDF PubMed Scopus (2) Google Scholar,10Kaltenbach T. Gawron A. Meyer C.S. et al.Adenoma detection rate (ADR) irrespective of indication is comparable to screening ADR: implications for quality monitoring.Clin Gastroenterol Hepatol. 2021; 19: 1883-1889Abstract Full Text Full Text PDF Scopus (5) Google Scholar Changing the measure to include surveillance and diagnostic colonoscopies is a return to the past, because the original proposal in 2002 did not restrict ADR to screening colonoscopies.1Rex D.K. Bond J.H. Winawer S. et al.Quality in the technical performance of colonoscopy and the continuous quality improvement process for colonoscopy: recommendations of the U.S. Multi-Society Task Force on Colorectal Cancer.Am J Gastroenterol. 2002; 97: 1296-1308Crossref PubMed Scopus (834) Google Scholar The screening restriction was added in 2006,11Rex D.K. Petrini J.L. Baron T.H. et al.Quality indicators for colonoscopy.Am J Gastroenterol. 2006; 101: 873-885Crossref PubMed Scopus (45) Google Scholar when it was decided that because the original targets had been derived from screening colonoscopy studies,1Rex D.K. Bond J.H. Winawer S. et al.Quality in the technical performance of colonoscopy and the continuous quality improvement process for colonoscopy: recommendations of the U.S. Multi-Society Task Force on Colorectal Cancer.Am J Gastroenterol. 2002; 97: 1296-1308Crossref PubMed Scopus (834) Google Scholar then ADR measurement should be confined to screening. We now have enough evidence to drop the screening-only restriction.8Rex D.K. Ponugoti P.L. Calculating the adenoma detection rate in screening colonoscopies only: is it necessary? Can it be gamed?.Endoscopy. 2017; 49: 1069-1074Crossref PubMed Scopus (40) Google Scholar, 9Ladabaum U. Shepard J. Mannalithara A. Adenoma and serrated lesion detection by colonoscopy indication: the ADR-ESS (ADR Extended to all Screening/Surveillance) score.Clin Gastroenterol Hepatol. 2021; 19: 1873-1882Abstract Full Text Full Text PDF PubMed Scopus (2) Google Scholar, 10Kaltenbach T. Gawron A. Meyer C.S. et al.Adenoma detection rate (ADR) irrespective of indication is comparable to screening ADR: implications for quality monitoring.Clin Gastroenterol Hepatol. 2021; 19: 1883-1889Abstract Full Text Full Text PDF Scopus (5) Google Scholar Including all indications eliminates the potential for indication gaming of ADR,8Rex D.K. Ponugoti P.L. Calculating the adenoma detection rate in screening colonoscopies only: is it necessary? Can it be gamed?.Endoscopy. 2017; 49: 1069-1074Crossref PubMed Scopus (40) Google Scholar in which the endoscopist decides what the indication is after the procedure is completed (when it is known whether an adenoma was removed) and before the endoscopist creates the procedure report. The revised ADR definition still would exclude patients with inflammatory bowel disease and polyposis syndromes, and it should exclude patients with positive fecal tests such as the fecal immunochemical test (FIT) and DNA-FIT. ADR in FIT-positive patients runs 15% to 20% higher than ADR for primary screening, and minimum ADRs of 35% in women and 45% in men were recommended by the USMSTF.12Robertson D.J. Lee J.K. Boland C.R. et al.Recommendations on fecal immunochemical testing to screen for colorectal neoplasia: a consensus statement by the US Multi-Society Task Force on colorectal cancer.Gastrointest Endosc. 2017; 85: 2-21 e3Abstract Full Text Full Text PDF PubMed Scopus (41) Google Scholar Of the alternatives to ADR, adenomas per colonoscopy (APC) or one of its variants,13Zhao S. Wang S. Pan P. et al.Magnitude, risk factors, and factors associated with adenoma miss rate of tandem colonoscopy: a systematic review and meta-analysis.Gastroenterology. 2019; 156: 1661-1674 e11Abstract Full Text Full Text PDF PubMed Scopus (111) Google Scholar,14Wang H.S. Pisegna J. Modi R. et al.Adenoma detection rate is necessary but insufficient for distinguishing high versus low endoscopist performance.Gastrointest Endosc. 2013; 77: 71-78Abstract Full Text Full Text PDF PubMed Scopus (79) Google Scholar is arguably the best candidate to replace ADR. ADR is subject to one and done gaming, in which the endoscopist resects 1 adenoma to get credit toward ADR, and then examines the remaining colon less carefully. One instance of one and done has been documented,14Wang H.S. Pisegna J. Modi R. et al.Adenoma detection rate is necessary but insufficient for distinguishing high versus low endoscopist performance.Gastrointest Endosc. 2013; 77: 71-78Abstract Full Text Full Text PDF PubMed Scopus (79) Google Scholar although it likely was gaming of the US reimbursement system that pays only for the first polypectomy, rather than gaming ADR. ADR and APC have mostly had good correlation,2Barclay R.L. Vicari J.J. Doughty A.S. et al.Colonoscopic withdrawal times and adenoma detection during screening colonoscopy.N Engl J Med. 2006; 355: 2533-2541Crossref PubMed Scopus (1028) Google Scholar,3Chen S.C. Rex D.K. Endoscopist can be more powerful than age and male gender in predicting adenoma detection at colonoscopy.Am J Gastroenterol. 2007; 102: 856-861Crossref PubMed Scopus (324) Google Scholar indicating one-and-done gaming is rare. APC is a better measure of clearing the whole colon, and provides greater separation between endoscopists than ADR.2Barclay R.L. Vicari J.J. Doughty A.S. et al.Colonoscopic withdrawal times and adenoma detection during screening colonoscopy.N Engl J Med. 2006; 355: 2533-2541Crossref PubMed Scopus (1028) Google Scholar,3Chen S.C. Rex D.K. Endoscopist can be more powerful than age and male gender in predicting adenoma detection at colonoscopy.Am J Gastroenterol. 2007; 102: 856-861Crossref PubMed Scopus (324) Google Scholar APC might be valuable in populations with a high prevalence of neoplasia such as FIT-positive, in whom ADR is not yet validated for cancer prevention, and very thorough clearing is needed because more patients have multiple advanced lesions. In 2002 it was not clear what the recommended targets would be for APC, but there now probably is enough evidence to establish targets for screening APC.15Rex D.K. Detection measures for colonoscopy: considerations on the adenoma detection rate, recommended detection thresholds, withdrawal times, and potential updates to measures.J Clin Gastroenterol. 2020; 54: 130-135Crossref PubMed Scopus (5) Google Scholar It is not clear that APC can be used across all indications, and the relationship of surveillance to screening to diagnostic APC might be different for APC than ADR because surveillance patients are more likely to have multiple small or diminutive adenomas.16Rex D.K. Repici A. Gross S.A. et al.High-definition colonoscopy versus Endocuff versus EndoRings versus full-spectrum endoscopy for adenoma detection at colonoscopy: a multicenter randomized trial.Gastrointest Endosc. 2018; 88: 335-344 e2Abstract Full Text Full Text PDF PubMed Scopus (64) Google Scholar Reasons to not switch to APC include the following: APC would incentivize the expensive practice of placing each polyp in a separate bottle for pathology, and APC measurement would be more tedious and expensive than measuring ADR, which is a problem considering that cost is already a deterrent to ADR measurement. Given that APC is not established as a better predictor of cancer prevention, it seems reasonable to await the artificial intelligence programs that eventually will make both ADR and APC measurement automatic. Given the recent endorsement of screening all Americans at age 45,17Davidson K.W. Barry M.J. et al.US Preventive Services Task ForceScreening for colorectal cancer: US Preventive Services Task Force recommendation statement.JAMA. 2021; 325: 1965-1977Crossref PubMed Scopus (63) Google Scholar should we change the ADR measure from patients 50 years and older to patients 45 years and older? Because the purpose of ADR is to identify variation in performance and signal a need for improvement, and there are plenty of patients 50 years and older, we do not have to make this change. The decision could reasonably go either way. I suspect we eventually will want the starting age to coincide with the screening age and make the change. If we make the change, should we change the targets? In this regard the prevalence of adenomas in the 45- to 49-year age group is about the same as the 50- to 54-year age group.18Butterly L.F. Siegel R.L. Fedewa S. et al.Colonoscopy outcomes in average-risk screening equivalent young adults: data from the New Hampshire Colonoscopy Registry.Am J Gastroenterol. 2021; 116: 171-179Crossref PubMed Scopus (18) Google Scholar Adding in the 45- to 49-year age group to the ADR calculation, assuming they show up for screening colonoscopy in substantial numbers, would pull most endoscopists’ ADR down a bit. In this regard it is relevant to note that the original targets were set somewhat arbitrarily, that is, they were set a bit below the mean prevalence in available screening colonoscopy studies.1Rex D.K. Bond J.H. Winawer S. et al.Quality in the technical performance of colonoscopy and the continuous quality improvement process for colonoscopy: recommendations of the U.S. Multi-Society Task Force on Colorectal Cancer.Am J Gastroenterol. 2002; 97: 1296-1308Crossref PubMed Scopus (834) Google Scholar The thought was that the greatest benefit would accrue from moving the worst performers up to or above the mean. There was also the thought that choosing the highest level performance for the target would make everyone inadequate, which would not be well accepted. Given this history, we could change the age definition to 45 years and older and leave the targets where they are, or make minor adjustments. It is not a huge issue. The current thresholds should be considered minimum acceptable thresholds, below which remedial work should be undertaken to improve technique. The minimum threshold was increased by 5% in 2015,6Rex D.K. Schoenfeld P.S. Cohen J. et al.Quality indicators for colonoscopy.Gastrointest Endosc. 2015; 81: 31-53Abstract Full Text Full Text PDF PubMed Scopus (513) Google Scholar in response to the report by Corley et al.5Corley D.A. Jensen C.D. Marks A.R. et al.Adenoma detection rate and risk of colorectal cancer and death.N Engl J Med. 2014; 370: 1298-1306Crossref PubMed Scopus (971) Google Scholar The choice of 5% for the increase again involved value judgments about feasibility and the perceived fraction of endoscopists who should reasonably fall below the minimum acceptable threshold. However, data5Corley D.A. Jensen C.D. Marks A.R. et al.Adenoma detection rate and risk of colorectal cancer and death.N Engl J Med. 2014; 370: 1298-1306Crossref PubMed Scopus (971) Google Scholar,19Shaukat A. Rector T.S. Church T.R. et al.Longer withdrawal time is associated with a reduced incidence of interval cancer after screening colonoscopy.Gastroenterology. 2015; 149: 952-957Abstract Full Text Full Text PDF PubMed Scopus (101) Google Scholar showing that cancer prevention continued improving as ADRs increased above minimum thresholds has given rise to the idea of aspirational thresholds,20Hilsden R.J. 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: 1743-1749Crossref PubMed Scopus (29) Google Scholar which represent the highest achievable ADRs in a given population. Thus, although minimum acceptable thresholds involve consensus-based judgments, aspirational thresholds would be based on prevalence data from high detectors and the association of that high-level detection with further cancer prevention. It thus could be advantageous to have both minimum acceptable and aspirational targets. Detection of sessile serrated lesions (SSLs) is important. Creating an SSL target is challenging because pathologic differentiation of SSLs from hyperplastic polyps is subject to different definitions of what constitutes an SSL, and interobserver variation among pathologists using similar definitions is high. In some reports, entire centers reported no SSLs.21Payne S.R. Church T.R. Wandell M. et al.Endoscopic detection of proximal serrated lesions and pathologic identification of sessile serrated adenomas/polyps vary on the basis of center.Clin Gastroenterol Hepatol. 2014; 12: 1119-1126Abstract Full Text Full Text PDF PubMed Scopus (93) Google Scholar We could set targets based on prevalence studies by expert pathologists and endoscopists,22Abdeljawad K. Vemulapalli K.C. Kahi C.J. et al.Sessile serrated polyp prevalence determined by a colonoscopist with a high lesion detection rate and an experienced pathologist.Gastrointest Endosc. 2015; 81: 517-524Abstract Full Text Full Text PDF PubMed Scopus (110) Google Scholar,23IJspeert J.E. 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: 740-746Crossref PubMed Scopus (54) Google Scholar but quality measurement might necessitate evaluation of both endoscopists and pathologists to understand low performance. Another approach is to measure SSL performance at the local institution (within which pathologist interobserver variation might be less), and then set local minimally acceptable and aspirational targets for the endoscopists. This question is not directly relevant to whether detection targets should be adjusted, but to whether ADRs should be used to formulate postpolypectomy surveillance recommendations. In this issue of Clinical Gastroenterology and Hepatology, Waldmann et al24Waldmann E. Kammerlander A.A. Gessl I. et al.Association of adenoma detection rate and adenoma characteristics with colorectal cancer mortality after screening colonoscopy.Clin Gastroenterol Hepatol. 2021; 19: 1890-1898Abstract Full Text Full Text PDF Scopus (3) Google Scholar show that ADR does predict cancer mortality risk after polypectomy, similar to a previously reported result.25Wieszczy P. Waldmann E. Loberg M. et al.Colonoscopist performance and colorectal cancer risk after adenoma removal to stratify surveillance: two nationwide observational studies.Gastroenterology. 2021; 160: 1067-1074 e6Abstract Full Text Full Text PDF PubMed Scopus (7) Google Scholar The USMSTF dealt with this issue in its recent recommendations by saying that use of the recommended intervals assumes a complete examination, an adequate bowel preparation, and a colonoscopist with an ADR above minimum thresholds.26Gupta S. Lieberman D. Anderson J.C. et al.Recommendations for follow-up after colonoscopy and polypectomy: a consensus update by the US Multi-Society Task Force on Colorectal Cancer.Gastrointest Endosc. 2020; 91: 463-485 e5Abstract Full Text Full Text PDF PubMed Scopus (44) Google Scholar That is not the same as incorporating ADR into the interval determinations. Although it makes perfect sense to adjust intervals based on ADR, there is a fairness challenge in a fee-for-service payment system. It will not work for endoscopists who perform poorly to be rewarded with performing a colonoscopy on patients more frequently. We need meaningful financial incentives for high-quality colonoscopy. Although ADR has functioned well as a measure of colonoscopy detection, there is new evidence to make changes in ADR recommendations. Expanding indications to include surveillance and diagnostic examinations exclusive of positive fecal tests appears justified and valuable.9Ladabaum U. Shepard J. Mannalithara A. Adenoma and serrated lesion detection by colonoscopy indication: the ADR-ESS (ADR Extended to all Screening/Surveillance) score.Clin Gastroenterol Hepatol. 2021; 19: 1873-1882Abstract Full Text Full Text PDF PubMed Scopus (2) Google Scholar,10Kaltenbach T. Gawron A. Meyer C.S. et al.Adenoma detection rate (ADR) irrespective of indication is comparable to screening ADR: implications for quality monitoring.Clin Gastroenterol Hepatol. 2021; 19: 1883-1889Abstract Full Text Full Text PDF Scopus (5) Google Scholar The concept of adding aspirational thresholds20Hilsden R.J. 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: 1743-1749Crossref PubMed Scopus (29) Google Scholar to current minimum acceptable thresholds carries an important message. We can continue to minimize the potential for gaming, avoid adding new costs or complexities to a measure that already is challenging for some endoscopists, and keep on preventing colon cancers.