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Defeating Cancer by Boosting the Adenoma Detection Rate: The Circle of Life

2017; Elsevier BV; Volume: 153; Issue: 1 Linguagem: Inglês

10.1053/j.gastro.2017.05.040

1528-0012

Cesare Hassan, Alessandro Repici,

Genetic factors in colorectal cancer

See “Increased rate of adenoma detection associates with reduced risk of colorectal cancer and death,” by Kaminski MF, Wieszczy P, Rupinski M, et al, on page 98. See “Increased rate of adenoma detection associates with reduced risk of colorectal cancer and death,” by Kaminski MF, Wieszczy P, Rupinski M, et al, on page 98. Primary colonoscopy screening is highly effective in reducing incidence and mortality of colorectal cancer (CRC), a major cause of cancer-related morbidity and mortality.1Kahi C.J. Rex D.K. Imperiale T.F. Screening, surveillance, and primary prevention for colorectal cancer: a review of the recent literature.Gastroenterology. 2008; 135: 380-399Abstract Full Text Full Text PDF PubMed Scopus (118) Google Scholar Irrespective of patient factors, endoscopist skill seems to affect screening efficacy dramatically. A proxy of endoscopist quality of mucosal inspection, namely, the adenoma detection rate (ADR),2Kaminski M.F. Thomas-Gibson S. Bugajski M. et al.Performance measures for lower gastrointestinal endoscopy: a European Society of Gastrointestinal Endoscopy (ESGE) Quality Improvement Initiative.Endoscopy. 2017; 49: 378-397Crossref PubMed Scopus (330) Google Scholar, 3Rex 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 (632) Google Scholar, 4Rex 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 (862) Google Scholar has been inversely associated with the risk of interval cancer and its death, with high detectors being able to reduce such risk by 50%-90%.5Kaminski 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 (1392) Google Scholar, 6Corley 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 (1166) Google Scholar Despite benefitting those screened by high detectors, patients screened by low detectors were left with an unjustified excess risk of CRC, severely undermining the efficacy of a screening intervention at the population level. To improve the ADR of low detectors immediately seemed to be the most logical strategy, and several different technical and technological interventions have been tested.7Corley D.A. Jensen C.D. Marks A.R. Can we improve adenoma detection rates? A systematic review of intervention studies.Gastrointest Endosc. 2011; 74: 656-665Abstract Full Text Full Text PDF PubMed Scopus (91) Google Scholar, 8Gupta N. How to improve your adenoma detection rate during colonoscopy.Gastroenterology. 2017; 151: 1054-1057Abstract Full Text Full Text PDF Scopus (11) Google Scholar Does an improved ADR ensure an equivalent degree of protection as a baseline high ADR? Can we offer low detectors a second chance to remain in an ongoing screening program? In this issue of Gastroenterology, Kaminski et al9Kaminski M.F. Wieszczy P. Rupinski M. et al.Increased rate of adenoma detection associates with reduced risk of colorectal cancer and death.Gastroenterology. 2017; 153: 98-105Abstract Full Text Full Text PDF PubMed Scopus (258) Google Scholar showed a profound reduction in the risk of interval cancer when primary colonoscopy screening was performed by endoscopists in whom ADR actually improved, with this risk remaining unacceptably high by those who failed to improve. Kaminski et al9Kaminski M.F. Wieszczy P. Rupinski M. et al.Increased rate of adenoma detection associates with reduced risk of colorectal cancer and death.Gastroenterology. 2017; 153: 98-105Abstract Full Text Full Text PDF PubMed Scopus (258) Google Scholar used nearly 1 million person-years of follow-up to match possible improvements of approximately 300 endoscopists with the actual incidence and mortality of 168 interval CRC. A relatively simple infrastructure, namely, annual recording of endoscopist ADR, was able to capture clinically relevant changes in endoscopist skill in a nationwide program, including episodic, stable, and continuous ADR improvement or its failure to increase.9Kaminski M.F. Wieszczy P. Rupinski M. et al.Increased rate of adenoma detection associates with reduced risk of colorectal cancer and death.Gastroenterology. 2017; 153: 98-105Abstract Full Text Full Text PDF PubMed Scopus (258) Google Scholar This finding puts additional pressure on any health system for having in place policies to audit baseline and longitudinal changes of ADR of the individual endoscopist, as currently recommended.2Kaminski M.F. Thomas-Gibson S. Bugajski M. et al.Performance measures for lower gastrointestinal endoscopy: a European Society of Gastrointestinal Endoscopy (ESGE) Quality Improvement Initiative.Endoscopy. 2017; 49: 378-397Crossref PubMed Scopus (330) Google Scholar, 4Rex 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 (862) Google Scholar Kaminski et al9Kaminski M.F. Wieszczy P. Rupinski M. et al.Increased rate of adenoma detection associates with reduced risk of colorectal cancer and death.Gastroenterology. 2017; 153: 98-105Abstract Full Text Full Text PDF PubMed Scopus (258) Google Scholar also showed that relatively simple strategies, such as quality indicator feedback or benchmarking, resulted in ADR improvement in most (ie, 74.5%) endoscopists. This unexpected propensity for the optimization of technical skills by the endoscopist community mandates the adoption of dedicated policies, irrespectively of the uncertainty on their efficacy: to do nothing should not be an option anymore. The efficacy of these interventional policies is reinforced by the dynamic of ADR improvement in the Polish study. Not only did the majority of endoscopists improve, but approximately one-third experienced progressive improvements, shifting a substantial and equivalent proportion of them from the lowest to the highest quintile of ADR.9Kaminski M.F. Wieszczy P. Rupinski M. et al.Increased rate of adenoma detection associates with reduced risk of colorectal cancer and death.Gastroenterology. 2017; 153: 98-105Abstract Full Text Full Text PDF PubMed Scopus (258) Google Scholar Specifically, the rate of those with the poorest ADR, a real nightmare for any patient, was reduced from 31% to 10%, whereas those with the highest ADR, the desirable target for any program, increased from 8% to 31%.9Kaminski M.F. Wieszczy P. Rupinski M. et al.Increased rate of adenoma detection associates with reduced risk of colorectal cancer and death.Gastroenterology. 2017; 153: 98-105Abstract Full Text Full Text PDF PubMed Scopus (258) Google Scholar However, it could be argued that the success of such interventions was somewhat facilitated by the relatively low baseline ADR in the Polish cohort.9Kaminski M.F. Wieszczy P. Rupinski M. et al.Increased rate of adenoma detection associates with reduced risk of colorectal cancer and death.Gastroenterology. 2017; 153: 98-105Abstract Full Text Full Text PDF PubMed Scopus (258) Google Scholar The clinical outcome of this ADR improvement irreversibly minimizes any residual uncertainty on the efficacy of these interventions. An absolute 6% increase in ADR, from 13.8% to 19.7%, reduced by as much as 37% and 50% the risk of interval CRC incidence and mortality, respectively, in the nationwide Polish screening program.9Kaminski M.F. Wieszczy P. Rupinski M. et al.Increased rate of adenoma detection associates with reduced risk of colorectal cancer and death.Gastroenterology. 2017; 153: 98-105Abstract Full Text Full Text PDF PubMed Scopus (258) Google Scholar Of note, the approximately 6% relative reduction of interval CRC for each 1% increase in ADR is roughly 2-fold higher than the already optimistic estimate of a 3% reduction based on the baseline data of the US study.6Corley 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 (1166) Google Scholar Thus, policies aiming to increase ADR should quickly become a new relevant quality indicator for any screening program, and this should be transparent to patient populations. The dynamic of the association between ADR improvement and interval CRC reduction deserves further analysis. The risk of interval CRC seemed to be affected substantially only when endoscopists improved to the highest quintile, with only a modest protection when reaching the fourth quintile, and nearly none when the improvement was limited to the third quintile.9Kaminski M.F. Wieszczy P. Rupinski M. et al.Increased rate of adenoma detection associates with reduced risk of colorectal cancer and death.Gastroenterology. 2017; 153: 98-105Abstract Full Text Full Text PDF PubMed Scopus (258) Google Scholar This somewhat exponential figure between the highest detectors and the decrease in interval CRC risk was not unexpected. In a previous Polish study, which was performed before implementing ADR improvement policies, a strikingly similar association was shown, because only endoscopists in the highest quintile displayed a profound reduction in CRC risk.5Kaminski 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 (1392) Google Scholar Albeit less evident, a similar type of association was also shown in the US study.6Corley 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 (1166) Google Scholar This suggests that policies aiming at improving the ADR may succeed in shifting endoscopists from one quintile to the other, but not in affecting the underlying profile of the association between ADR and interval CRC, acting as an independent law of screening colonoscopy. This is further confirmed by evidence that patients screened by endoscopists who reached the highest ADR quintile gained a similar degree of CRC prevention as those screened by endoscopists with an already high baseline ADR.9Kaminski M.F. Wieszczy P. Rupinski M. et al.Increased rate of adenoma detection associates with reduced risk of colorectal cancer and death.Gastroenterology. 2017; 153: 98-105Abstract Full Text Full Text PDF PubMed Scopus (258) Google Scholar From a clinical perspective, the message of this dynamic cannot be neglected. To target ADR improvement may be a necessary but not sufficient condition. Any health system should pursue technical improvement until most of the endoscopists are allowed to reach what it should be defined—before intervention—as the maximum desirable target. Kaminski et al suggestively showed that such a target should be carefully updated, increasing from 20% to 25% in the narrow interval between 2000 and 2004 and 2004 and 2008.5Kaminski 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 (1392) Google Scholar, 9Kaminski M.F. Wieszczy P. Rupinski M. et al.Increased rate of adenoma detection associates with reduced risk of colorectal cancer and death.Gastroenterology. 2017; 153: 98-105Abstract Full Text Full Text PDF PubMed Scopus (258) Google Scholar These data were—at least partially—incorporated in the increase of the performance target for ADR from 20% to 25% by the new US recommendation.3Rex 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 (632) Google Scholar The fully expected and plausible association between ADR improvement and interval cancer definitively closes our understanding on the role of what was once considered as a mere technical factor on the degree of a relevant clinical outcome, such as the degree of CRC prevention. However, new issues must be addressed, although—as already stressed—this should never delay the immediate application of policies aiming at monitoring and improving ADR in a screening program. As outlined by the same authors,9Kaminski M.F. Wieszczy P. Rupinski M. et al.Increased rate of adenoma detection associates with reduced risk of colorectal cancer and death.Gastroenterology. 2017; 153: 98-105Abstract Full Text Full Text PDF PubMed Scopus (258) Google Scholar the higher the ADR, the higher the proportion of patients who may potentially deserve to enter a surveillance program. It could be argued that cost-effective simulations universally showed how the relatively small cost of such additional surveillance would be in the long term reabsorbed by huge savings in the cost of CRC chemotherapy and palliation.10Meester R.G. Doubeni C.A. Lansdorp-Vogelaar I. et al.Variation in Adenoma detection rate and the lifetime benefits and cost of colorectal cancer screening: a microsimulation model.JAMA. 2015; 313: 2349-2358Crossref PubMed Scopus (54) Google Scholar, 11Hassan C. Rex D.K. Zullo A. et al.Efficacy and cost-effectiveness of screening colonoscopy according to the adenoma detection rate.United European Gastroenterol J. 2015; 3: 200-207Crossref PubMed Scopus (17) Google Scholar However, this is unlikely to be the real issue. From a practical standpoint, to offer nationwide screening programs, and, at the same time, to substantially increase the burden of colonoscopy surveillance would seem to be unrealistic, when considering the paucity and rigidity of the endoscopy capacity. For this reason, programs aiming at reliably improving the technical performance of colonoscopy should be balanced appropriately by a conservative approach on surveillance, especially for those with low-risk adenoma.12Hassan 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 (417) Google Scholar, 13Lieberman 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 (1425) Google Scholar This is especially true when shifting our attention by the 20% mean ADR of this Polish population to the 40%-60% ADR of enriched-disease populations, such as European fecal testing programs or primary screening colonoscopy performed by high detectors.14Zorzi M. Senore C. Da Re F. et al.Quality of colonoscopy 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. 2015; 64: 1389-1396Crossref PubMed Scopus (64) Google Scholar, 15Lee T.J. Rutter M.D. Blanks R.G. et al.Colonoscopy quality measures: experience from the NHS Bowel Cancer Screening Programme.Gut. 2012; 61: 1050-1057Crossref PubMed Scopus (230) Google Scholar, 16Rex D.K. Helbig C.C. High yields of small and flat adenomas with high-definition colonoscopes using either white light or narrow band imaging.Gastroenterology. 2007; 133: 42-47Abstract Full Text Full Text PDF PubMed Scopus (368) Google Scholar Second, the most suitable intervention to improve the ADR remains to be determined. Despite a long-lasting and clinically relevant ADR improvement was achieved in this Polish study,9Kaminski M.F. Wieszczy P. Rupinski M. et al.Increased rate of adenoma detection associates with reduced risk of colorectal cancer and death.Gastroenterology. 2017; 153: 98-105Abstract Full Text Full Text PDF PubMed Scopus (258) Google Scholar there was no control for the implemented interventions, leaving uncertainty on their actual efficacy. However, a relatively simple intervention, such as leadership training, resulted in a 4%-7% absolute ADR increase in a controlled study performed in the same Polish screening program.17Kaminski M.F. Anderson J. Valori R. et al.Leadership training to improve adenoma detection rate in screening colonoscopy: a randomised trial.Gut. 2016; 65 (616–624)Crossref PubMed Scopus (100) Google Scholar There is also uncertainty on whether the ADR improvement achieved by technical interventions, such as longer withdrawal time and split preparation, has the same clinical outcome as ADR improvement targeted by technological innovations, such as high-definition endoscopy, chromoendoscopy, and add-on devices.8Gupta N. How to improve your adenoma detection rate during colonoscopy.Gastroenterology. 2017; 151: 1054-1057Abstract Full Text Full Text PDF Scopus (11) Google Scholar Third, in the Polish study, a minority of endoscopists remain poor detectors, despite the implementation of quality assurance programs.8Gupta N. How to improve your adenoma detection rate during colonoscopy.Gastroenterology. 2017; 151: 1054-1057Abstract Full Text Full Text PDF Scopus (11) Google Scholar The most suitable policy for these cases remains to be defined, but specifically targeted retraining programs are likely to be needed. When its association with interval cancer came about, the ADR paralyzed the medical and nonmedical community. Low detectors suddenly became the strongest predictor of the same cancer they were expected to prevent, and patients with a negative colonoscopy feared to be screened by suboptimal endoscopists. The circular association between ADR improvement and interval cancer offers a completely new perspective (Figure 1). Endoscopists will gain confidence by boosting their ADR, and patients will be reassured by quality assurance programs. Where there was a monotonic line relating baseline ADR with the risk of interval cancer, there is now a revitalizing circle offering a new and better life to endoscopists and patients altogether. Increased Rate of Adenoma Detection Associates With Reduced Risk of Colorectal Cancer and DeathGastroenterologyVol. 153Issue 1PreviewThe quality of endoscopists' colonoscopy performance is measured by adenoma detection rate (ADR). Although ADR is associated inversely with interval colorectal cancer and colorectal cancer death, the effects of an increasing ADR have not been shown. We investigated whether increasing ADRs from individual endoscopists is associated with reduced risks of interval colorectal cancer and subsequent death. Full-Text PDF Covering the CoverGastroenterologyVol. 153Issue 1PreviewIn a prospective study of a national colorectal cancer screening program, increasing the adenoma detection rate of endoscopists was associated with a reduced risk of interval colorectal cancer and colorectal cancer death. Full-Text PDF