Abstract

The dominant paradigm underpinning colonoscopy quality is that an optimized colorectal inspection technique will reduce the risk of missed lesions to insignificant levels, resulting in a negligible risk of postcolonoscopy colorectal cancer (CRC).1Corley 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 (896) Google Scholar This assumption led to more efficient strategies for CRC screening and surveillance where a prolonged 10-year interval is considered appropriate before repeating a screening colonoscopy in patients with a negative initial examination. Similarly, a 5- to 10-year surveillance interval is now recommended after removal of low-risk adenomas.2Lieberman D.A. Rex D.K. Winawer S.J. et al.Guidelines for colonoscopy surveillance after screening and polypectomy: a consensus update by the US Multi-Society Task Force on Colorectal Cancer.Gastroenterology. 2012; 143: 844-857Abstract Full Text Full Text PDF PubMed Scopus (1289) Google Scholar In the European programs a nonendoscopic strategy, based on immunochemical fecal test, is considered a more convenient policy following a negative colonoscopy3Atkin W.S. Valori R. Kuipers E.J. et al.European guidelines for quality assurance in colorectal cancer screening and diagnosis. First edition - colonoscopic surveillance following adenoma removal.Endoscopy. 2012; 44: SE151-SE163PubMed Google Scholar or following removal of low-risk adenomas.3Atkin W.S. Valori R. Kuipers E.J. et al.European guidelines for quality assurance in colorectal cancer screening and diagnosis. First edition - colonoscopic surveillance following adenoma removal.Endoscopy. 2012; 44: SE151-SE163PubMed Google Scholar, 4Hassan C. Quintero E. Dumonceau J.M. et al.Post-polypectomy colonoscopy surveillance: European Society of Gastrointestinal Endoscopy (ESGE) Guideline.Endoscopy. 2013; 45: 842-851Crossref PubMed Scopus (371) Google Scholar Undoubtedly, the shift of endoscopic resources from an intensive surveillance to more of a screening setting has been a major consequence of the quality assurance process in diagnostic colonoscopy. However, this shift is based on the assumption that the initial examination was indeed a high-quality examination. Can we reduce the burden of postpolypectomy surveillance also for high-risk adenomas? There is no apparent reason for high-quality colonoscopy being less effective in finding all lesions in those with high-risk adenomas as compared with low-risk or no adenomas. Encouragingly, a large subgroup of patients with high-risk adenomas (namely those with <20 mm distal lesions without high-grade dysplasia) has been shown to be at very low risk of subsequent cancer, questioning the value of intensive, or indeed any, surveillance.5Atkin W. Wooldrage K. Brenner A. et al.Adenoma surveillance and colorectal cancer incidence: a retrospective, multicentre, cohort study.Lancet Oncol. 2017; 18: 823-834Abstract Full Text Full Text PDF PubMed Scopus (83) Google Scholar This has been well substantiated in the ongoing European Polyp Surveillance trials where a 5-year, rather than 3-year, surveillance interval for high-risk adenomas is being assessed.6Jover R. Bretthauer M. Dekker E. et al.Rationale and design of the European Polyp Surveillance (EPoS) trials.Endoscopy. 2016; 48: 571-578Crossref PubMed Scopus (64) Google Scholar Longer surveillance intervals rely on the assumption of a negligible risk of postcolonoscopy CRC caused by missed or de novo lesions. An alternative consideration is the risk of an incomplete polypectomy at baseline colonoscopy. Incomplete polypectomy accounts for up to one-third of postcolonoscopy CRC,7Rutter M.D. Beintaris I. Valori R. et al.World Endoscopy Organization consensus statements on post-colonoscopy and post-imaging colorectal cancer.Gastroenterology. 2018; 155: 909-925Abstract Full Text Full Text PDF PubMed Scopus (79) Google Scholar, 8Belderbos T.D. Pullens H.J. Leenders M. et al.Risk of post-colonoscopy colorectal cancer due to incomplete adenoma resection: a nationwide, population-based cohort study.United European Gastroenterol J. 2017; 5: 440-447Crossref PubMed Scopus (13) Google Scholar often occurring early after the baseline colonoscopy. This may explain, at least in part, the higher risk of postcolonoscopy CRC in patients with high-risk adenomas without endoscopic surveillance,5Atkin W. Wooldrage K. Brenner A. et al.Adenoma surveillance and colorectal cancer incidence: a retrospective, multicentre, cohort study.Lancet Oncol. 2017; 18: 823-834Abstract Full Text Full Text PDF PubMed Scopus (83) Google Scholar, 9Loberg M. Kalager M. Holme O. et al.Long-term colorectal-cancer mortality after adenoma removal.N Engl J Med. 2014; 371: 799-807Crossref PubMed Scopus (141) Google Scholar and in those with ≥20 mm or proximal lesions.5Atkin W. Wooldrage K. Brenner A. et al.Adenoma surveillance and colorectal cancer incidence: a retrospective, multicentre, cohort study.Lancet Oncol. 2017; 18: 823-834Abstract Full Text Full Text PDF PubMed Scopus (83) Google Scholar There is a widely held belief among endoscopists that the risk is mainly confined to large (ie, ≥20 mm) lesions because piecemeal rather than en bloc resection is used in these cases.10Hassan C. Repici A. Sharma P. et al.Efficacy and safety of endoscopic resection of large colorectal polyps: a systematic review and meta-analysis.Gut. 2016; 65: 806-820Crossref PubMed Scopus (155) Google Scholar This conviction translated in the clinical recommendation of a short-term (ie, 3–6 months) site-check after piecemeal removal of these lesions, before entering patients into a surveillance regimen.2Lieberman D.A. Rex D.K. Winawer S.J. et al.Guidelines for colonoscopy surveillance after screening and polypectomy: a consensus update by the US Multi-Society Task Force on Colorectal Cancer.Gastroenterology. 2012; 143: 844-857Abstract Full Text Full Text PDF PubMed Scopus (1289) Google Scholar, 4Hassan C. Quintero E. Dumonceau J.M. et al.Post-polypectomy colonoscopy surveillance: European Society of Gastrointestinal Endoscopy (ESGE) Guideline.Endoscopy. 2013; 45: 842-851Crossref PubMed Scopus (371) Google Scholar Implementation of new techniques (ie, endoscopic submucosal dissection) for an en bloc resection of these large lesions is expected to minimize the risk of endoscopic recurrence and adverse oncologic outcomes. However, most high-risk adenomas are 10–20 mm in size: can we confidently exclude the risk of incomplete polypectomy for these? As endoscopists, we often have little if any doubt of our ability to completely remove these relatively small lesions, regardless of the morphology or technique. In addition, submucosal injection (ie, endoscopic mucosal resection) facilitates en bloc resection for most of the nonpedunculated lesions, and facilitates careful endoscopic and histologic assessment of the resection margins. Is it not quite rare in our practice to find a recurrence of a previously resected <20 mm lesion? This conviction was recently challenged by the publication of the Complete Adenoma Resection (CARE) study,11Pohl H. Srivastava A. Bensen S.P. et al.Incomplete polyp resection during colonoscopy-results of the complete adenoma resection (CARE) study.Gastroenterology. 2013; 144: 74-80Abstract Full Text Full Text PDF PubMed Scopus (432) Google Scholar unexpectedly showing a high rate of incomplete polypectomy (ie, 17%) for 10–20 mm lesions. However, such evidence was based on an artificial setting (ie, biopsies of the postpolypectomy resection margin) and the cross-sectional design meant it could not assess the clinical implications of the findings.11Pohl H. Srivastava A. Bensen S.P. et al.Incomplete polyp resection during colonoscopy-results of the complete adenoma resection (CARE) study.Gastroenterology. 2013; 144: 74-80Abstract Full Text Full Text PDF PubMed Scopus (432) Google Scholar Does this unexpected rate of incomplete resection for 10- to 20-mm lesions affect the long-term risk of colorectal neoplasia? Previous epidemiologic studies on postcolonoscopy CRC risk (mainly based on whether a polypectomy was previously performed in the same segment where CRC developed) failed to address such an issue because of lack of endoscopic data. For this reason, Adler et al12Adler J. Toy D. Anderson J.C. et al.Metachronous neoplasias arise in a higher proportion of colon segments from which large polyps were previously removed, and can be used to estimate incomplete resection of 10-20 mm colorectal polyps.Clin Gastroenterol Hepatol. 2019; 17: 2277-2284Abstract Full Text Full Text PDF PubMed Scopus (16) Google Scholar applied the same segmental methodology to an endoscopic setting by comparing the risk of metachronous neoplasia during surveillance colonoscopy in segments based on whether 10- to 20-mm lesions had or had not been removed. First, the more than 2-fold increase in metachronous lesions in segments where a 10- to 20-mm lesion had been removed depressingly confirmed the high rate of incomplete resection previously shown in the CARE study.11Pohl H. Srivastava A. Bensen S.P. et al.Incomplete polyp resection during colonoscopy-results of the complete adenoma resection (CARE) study.Gastroenterology. 2013; 144: 74-80Abstract Full Text Full Text PDF PubMed Scopus (432) Google Scholar Second, by acting as a proxy for the risk of postcolonoscopy CRC, the 13% rate of metachronous neoplasia attributed to incomplete resection of 10- to 20-mm lesions suddenly elevated incomplete polypectomy within this size range as the putative factor for an adverse oncologic outcome. The advantage of an endoscopic11Pohl H. Srivastava A. Bensen S.P. et al.Incomplete polyp resection during colonoscopy-results of the complete adenoma resection (CARE) study.Gastroenterology. 2013; 144: 74-80Abstract Full Text Full Text PDF PubMed Scopus (432) Google Scholar rather than epidemiologic7Rutter M.D. Beintaris I. Valori R. et al.World Endoscopy Organization consensus statements on post-colonoscopy and post-imaging colorectal cancer.Gastroenterology. 2018; 155: 909-925Abstract Full Text Full Text PDF PubMed Scopus (79) Google Scholar, 8Belderbos T.D. Pullens H.J. Leenders M. et al.Risk of post-colonoscopy colorectal cancer due to incomplete adenoma resection: a nationwide, population-based cohort study.United European Gastroenterol J. 2017; 5: 440-447Crossref PubMed Scopus (13) Google Scholar design was illustrated by the ability to explore possible predictors for incomplete polypectomy, which revealed a more than 5-fold increase in metachronous neoplasia following piecemeal resection of a 10- to 20-mm (nonpedunculated) lesion, accounting for around half of all the metachronous neoplasia detected at surveillance.12Adler J. Toy D. Anderson J.C. et al.Metachronous neoplasias arise in a higher proportion of colon segments from which large polyps were previously removed, and can be used to estimate incomplete resection of 10-20 mm colorectal polyps.Clin Gastroenterol Hepatol. 2019; 17: 2277-2284Abstract Full Text Full Text PDF PubMed Scopus (16) Google Scholar These data clearly show how the completeness of endoscopic resection remains a critical prerequisite before planning endoscopic surveillance, especially now that prolongation of surveillance intervals is under scrutiny. Regrettably, more intensive surveillance may not be an effective solution to the problem of incomplete resection, because malignant progression may occur before or irrespective of the surveillance. The 28% incomplete resection rate estimated by Adler et al12Adler J. Toy D. Anderson J.C. et al.Metachronous neoplasias arise in a higher proportion of colon segments from which large polyps were previously removed, and can be used to estimate incomplete resection of 10-20 mm colorectal polyps.Clin Gastroenterol Hepatol. 2019; 17: 2277-2284Abstract Full Text Full Text PDF PubMed Scopus (16) Google Scholar for piecemeal resection of a 10- to 20-mm lesion is simply unacceptable, especially considering similar or lower rates have been shown for ≥20-mm lesions.10Hassan C. Repici A. Sharma P. et al.Efficacy and safety of endoscopic resection of large colorectal polyps: a systematic review and meta-analysis.Gut. 2016; 65: 806-820Crossref PubMed Scopus (155) Google Scholar If early work-up of any ≥10 mm lesion with piecemeal or incomplete resection is to be considered, a standardization of the snare-based technique to ensure en bloc resection of these lesions would be needed to avoid unnecessary additional procedures. Unfortunately, few studies have addressed the technical efficacy of removing 10- to 20-mm lesions,13Ferlitsch M. Moss A. Hassan C. et al.Colorectal polypectomy and endoscopic mucosal resection (EMR): European Society of Gastrointestinal Endoscopy (ESGE) Clinical Guideline.Endoscopy. 2017; 49: 270-297Crossref PubMed Scopus (333) Google Scholar generating uncertainty on the optimal technique. In addition, there is significant interendoscopist variability in the performance of polypectomy or endoscopic mucosal resection, further questioning its generalizability in community-based endoscopy.11Pohl H. Srivastava A. Bensen S.P. et al.Incomplete polyp resection during colonoscopy-results of the complete adenoma resection (CARE) study.Gastroenterology. 2013; 144: 74-80Abstract Full Text Full Text PDF PubMed Scopus (432) Google Scholar Assurance of high levels of completeness of polypectomy is necessary to minimize the risk of metachronous neoplasia, and ultimately of postcolonoscopy CRC, at surveillance. However, it is challenging in clinical practice because it requires adequate endoscopic and histologic information. In this regard, the segmental methodology by Adler et al12Adler J. Toy D. Anderson J.C. et al.Metachronous neoplasias arise in a higher proportion of colon segments from which large polyps were previously removed, and can be used to estimate incomplete resection of 10-20 mm colorectal polyps.Clin Gastroenterol Hepatol. 2019; 17: 2277-2284Abstract Full Text Full Text PDF PubMed Scopus (16) Google Scholar simplifies this assessment. By performing a Copernican revolution, the authors exploited the first postpolypectomy surveillance examination to infer the completeness of resection rate at the baseline colonoscopy. This methodology offers unique advantages. First, no major deviation from clinical practice or additional resources are required. Of note, the focus should not be restricted to 10- to 20-mm lesions in clinical practice, further simplifying its assessment. Second, the retrospective assessment prevents operator-related bias at the time of the baseline polypectomy, and the intrapatient intersegmental comparison prevents bias caused by disease prevalence distribution. Third, possible improvements in resection technique may be identified by periodic auditing of this indicator. Potential drawbacks include misclassification of the segment at the time of polypectomy or surveillance, misdiagnosis of de novo or missed lesions as residual polyp, and suboptimal compliance of patients with surveillance. However, these are likely to represent systematic bias with no effect on the relative distribution of individual endoscopists according to their technical expertise. In addition, these preliminary data need confirmation in future studies; they also underscore the potential need to retrain pathologists to report on the R0 resection also for <20-mm lesions. In conclusion, the dramatic improvement in our diagnostic accuracy has been effective in minimizing the need for endoscopic surveillance in those with no or low-risk lesions. However, effort is now required in polypectomy competency to ensure a high rate of en bloc resection for 10- to 20-mm lesions. Such a step seems critical to reduce the risk of postcolonoscopy CRC in these patients, and the associated burden of surveillance. Metachronous Neoplasias Arise in a Higher Proportion of Colon Segments From Which Large Polyps Were Previously Removed, and Can be Used to Estimate Incomplete Resection of 10–20 mm Colorectal PolypsClinical Gastroenterology and HepatologyVol. 17Issue 11PreviewIncomplete resection of polyps could be an important cause of post-colonoscopy colorectal cancer. However, it is difficult to study progression of incompletely removed polyps or their clinical importance. We aimed to estimate incomplete polyp resection using risk of metachronous neoplasia per colon segment. Full-Text PDF

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