Estimation of Benefits, Burden, and Harms of Colorectal Cancer Screening Strategies: Modeling Study for the US Preventive Services Task Force.

IMPORTANCE The US Preventive Services Task Force (USPSTF) is updating its 2008 colorectal cancer (CRC) screening recommendations. OBJECTIVE To inform the USPSTF by modeling the benefits, burden, and harms of CRC screening strategies; estimating the optimal ages to begin and end screening; and identifying a set of model-recommendable strategies that provide similar life-years gained (LYG) and a comparable balance between LYG and screening burden. DESIGN, SETTING, AND PARTICIPANTS Comparative modeling with 3 microsimulation models of a hypothetical cohort of previously unscreened US 40-year-olds with no prior CRC diagnosis. EXPOSURES Screening with sensitive guaiac-based fecal occult blood testing, fecal immunochemical testing (FIT), multitarget stool DNA testing, flexible sigmoidoscopy with or without stool testing, computed tomographic colonography (CTC), or colonoscopy starting at age 45, 50, or 55 years and ending at age 75, 80, or 85 years. Screening intervals varied by modality. Full adherence for all strategies was assumed. MAIN OUTCOMES AND MEASURES Life-years gained compared with no screening (benefit), lifetime number of colonoscopies required (burden), lifetime number of colonoscopy complications (harms), and ratios of incremental burden and benefit (efficiency ratios) per 1000 40-year-olds. RESULTS The screening strategies provided LYG in the range of 152 to 313 per 1000 40-year-olds. Lifetime colonoscopy burden per 1000 persons ranged from fewer than 900 (FIT every 3 years from ages 55-75 years) to more than 7500 (colonoscopy screening every 5 years from ages 45-85 years). Harm from screening was at most 23 complications per 1000 persons screened. Strategies with screening beginning at age 50 years generally provided more LYG as well as more additional LYG per additional colonoscopy than strategies with screening beginning at age 55 years. There were limited empirical data to support a start age of 45 years. For persons adequately screened up to age 75 years, additional screening yielded small increases in LYG relative to the increase in colonoscopy burden. With screening from ages 50 to 75 years, 4 strategies yielded a comparable balance of screening burden and similar LYG (median LYG per 1000 across the models): colonoscopy every 10 years (270 LYG); sigmoidoscopy every 10 years with annual FIT (256 LYG); CTC every 5 years (248 LYG); and annual FIT (244 LYG). CONCLUSIONS AND RELEVANCE In this microsimulation modeling study of a previously unscreened population undergoing CRC screening that assumed 100% adherence, the strategies of colonoscopy every 10 years, annual FIT, sigmoidoscopy every 10 years with annual FIT, and CTC every 5 years performed from ages 50 through 75 years provided similar LYG and a comparable balance of benefit and screening burden.

[1]  J. Habbema,et al.  Should colorectal cancer screening be considered in elderly persons without previous screening? A cost-effectiveness analysis. , 2014, Annals of internal medicine.

[2]  Aasma Shaukat,et al.  Long-term mortality after screening for colorectal cancer. , 2013, The New England journal of medicine.

[3]  Oguzhan Alagoz,et al.  Collaborative Modeling of the Benefits and Harms Associated With Different U.S. Breast Cancer Screening Strategies , 2016, Annals of Internal Medicine.

[4]  J. Olsen,et al.  Randomised study of screening for colorectal cancer with faecal-occult-blood test , 1996, The Lancet.

[5]  Onchee Yu,et al.  A hierarchical non‐homogenous Poisson model for meta‐analysis of adenoma counts , 2007, Statistics in medicine.

[6]  Reiko Nishihara,et al.  Long-term colorectal-cancer incidence and mortality after lower endoscopy. , 2013, The New England journal of medicine.

[7]  J. Wardle,et al.  Single flexible sigmoidoscopy screening to prevent colorectal cancer: baseline findings of a UK multicentre randomised trial , 2002, The Lancet.

[8]  Bernadette Mazurek Melnyk,et al.  Screening for colorectal cancer: U.S. Preventive Services Task Force recommendation statement. , 2008, Annals of internal medicine.

[9]  A. Zauber,et al.  The Appropriateness ofMore Intensive Colonoscopy Screening Than Recommended inMedicare Beneficiaries AModeling Study , 2014 .

[10]  Marvin Zelen,et al.  Effects of Mammography Screening Under Different Screening Schedules: Model Estimates of Potential Benefits and Harms , 2009 .

[11]  Tracey L Marsh,et al.  Validation of Models Used to Inform Colorectal Cancer Screening Guidelines , 2016, Medical decision making : an international journal of the Society for Medical Decision Making.

[12]  Rongwei Fu,et al.  Screening for Colorectal Cancer: A Targeted, Updated Systematic Review for the U.S. Preventive Services Task Force , 2008, Annals of Internal Medicine.

[13]  I CHAPMAN,et al.  Adenomatous Polypi of Large Intestine: Incidence and Distribution , 1963, Annals of surgery.

[14]  P. Bossuyt,et al.  Polyp Miss Rate Determined by Tandem Colonoscopy: A Systematic Review , 2006, The American Journal of Gastroenterology.

[15]  Jennifer S. Lin,et al.  Screening for Colorectal Cancer: An Updated Systematic Review , 2008 .

[16]  D. Ransohoff,et al.  Multitarget stool DNA testing for colorectal-cancer screening. , 2014, The New England journal of medicine.

[17]  H. Brenner,et al.  Protection From Colorectal Cancer After Colonoscopy , 2011, Annals of Internal Medicine.

[18]  J. Bombí,et al.  Polyps of the colon in barcelona, Spain. An autopsy study , 1988, Cancer.

[19]  P. J. Young,et al.  Predictors of presence, multiplicity, size and dysplasia of colorectal adenomas. A necropsy study in New Zealand. , 1992, Gut.

[20]  Christopher D. Jensen,et al.  Fecal Immunochemical Test Program Performance Over 4 Rounds of Annual Screening , 2016, Annals of Internal Medicine.

[21]  N. O. Jacobsen,et al.  Polyps of the large intestine in Aarhus, Denmark. An autopsy study. , 1989, Scandinavian journal of gastroenterology.

[22]  M. Hernán,et al.  Effect of flexible sigmoidoscopy screening on colorectal cancer incidence and mortality: a randomized clinical trial. , 2014, JAMA.

[23]  C. Klabunde,et al.  Trends in Colorectal Cancer Test Use among Vulnerable Populations in the United States , 2011, Cancer Epidemiology, Biomarkers & Prevention.

[24]  E. Kuipers,et al.  Immunochemical Fecal Occult Blood Testing Is Equally Sensitive for Proximal and Distal Advanced Neoplasia , 2012, The American Journal of Gastroenterology.

[25]  Harminder Singh,et al.  Risk of developing colorectal cancer following a negative colonoscopy examination: evidence for a 10-year interval between colonoscopies. , 2006, JAMA.

[26]  M. Vatn,et al.  The prevalence of polyps of the large intestine in Oslo: An autopsy study , 1982, Cancer.

[27]  Y. Niv,et al.  A higher detection rate for colorectal cancer and advanced adenomatous polyp for screening with immunochemical fecal occult blood test than guaiac fecal occult blood test, despite lower compliance rate. A prospective, controlled, feasibility study , 2011, International journal of cancer.

[28]  J. Yee,et al.  Accuracy of ct colonography for detection of large adenomas and cancers , 2009 .

[29]  Chyke A Doubeni,et al.  Screening Colonoscopy and Risk for Incident Late-Stage Colorectal Cancer Diagnosis in Average-Risk Adults , 2013, Annals of Internal Medicine.

[30]  D. Snover Update on the serrated pathway to colorectal carcinoma. , 2011, Human pathology.

[31]  Ewout W Steyerberg,et al.  How much colonoscopy screening should be recommended to individuals with various degrees of family history of colorectal cancer? , 2011, Cancer.

[32]  D. Berry,et al.  Breast Cancer Working Group of the Cancer Intervention and Surveillance Modeling Network. Effects of mammography screening under different screening schedules: Model estimates of potential benefits and harms (Annals of Internal Medicine (2009) 151, (738-747)) , 2010 .

[33]  E. C. Hammond,et al.  Adenomatous lesions of the large bowel: An autopsy survey , 1979, Cancer.

[34]  S. Kulasingam,et al.  Screening for Cervical Cancer: A Decision Analysis for the U.S. Preventive Services Task Force , 2011 .

[35]  E. Kliewer,et al.  The reduction in colorectal cancer mortality after colonoscopy varies by site of the cancer. , 2010, Gastroenterology.

[36]  T C ARMINSKI,et al.  Incidence and distribution of adenomatous polyps of the colon and rectum based on 1,000 autopsy examinations , 1964, Diseases of the colon and rectum.

[37]  Mark P Purdue,et al.  Colorectal-cancer incidence and mortality with screening flexible sigmoidoscopy. , 2012, The New England journal of medicine.

[38]  Eric J Feuer,et al.  Secular trends in colon and rectal cancer relative survival. , 2013, Journal of the National Cancer Institute.

[39]  R. Dittus,et al.  Utility valuations for outcome states of colorectal cancer , 1999, American Journal of Gastroenterology.

[40]  J. Gohagan,et al.  Flexible sigmoidoscopy in the PLCO cancer screening trial: results from the baseline screening examination of a randomized trial. , 2005, Journal of the National Cancer Institute.

[41]  T. Heeren,et al.  Prevalence of Advanced Colorectal Neoplasia in White and Black Patients Undergoing Screening Colonoscopy in a Safety-Net Hospital , 2013, Annals of Internal Medicine.

[42]  H. Brenner,et al.  Protection from right- and left-sided colorectal neoplasms after colonoscopy: population-based study. , 2010, Journal of the National Cancer Institute.

[43]  L. Bisanti,et al.  Once-only sigmoidoscopy in colorectal cancer screening: follow-up findings of the Italian Randomized Controlled Trial--SCORE. , 2011, Journal of the National Cancer Institute.

[44]  Lester J. Blatt,et al.  Polyps of the colon and rectum , 1961 .

[45]  Yrjö Collan,et al.  Prevalence of polyps in an autopsy series from areas with varying incidence of large‐bowel cancer , 1985, International journal of cancer.

[46]  S. Moss,et al.  Randomised controlled trial of faecal-occult-blood screening for colorectal cancer , 1989, The Lancet.

[47]  L M Schuman,et al.  Reducing mortality from colorectal cancer by screening for fecal occult blood. Minnesota Colon Cancer Control Study. , 1993, The New England journal of medicine.

[48]  D. Ransohoff,et al.  Adverse Events After Outpatient Colonoscopy in the Medicare Population , 2009, Annals of Internal Medicine.

[49]  Perry J. Pickhardt,et al.  CT Colonography for Population Screening: Ready for Prime Time? , 2015, Digestive Diseases and Sciences.

[50]  S. Woolf,et al.  The relative importance of patient-reported barriers to colorectal cancer screening. , 2010, American journal of preventive medicine.

[51]  Cancer,et al.  Once-only flexible sigmoidoscopy screening in prevention of colorectal cancer: a multicentre randomised controlled trial , 2010, The Lancet.

[52]  Iris Lansdorp-Vogelaar,et al.  A Systematic Comparison of Microsimulation Models of Colorectal Cancer , 2011, Medical decision making : an international journal of the Society for Medical Decision Making.

[53]  Amy B. Knudsen,et al.  Evaluating Test Strategies for Colorectal Cancer Screening: A Decision Analysis for the U.S. Preventive Services Task Force , 2008, Annals of Internal Medicine.

[54]  Douglas K Owens,et al.  High-Value, Cost-Conscious Health Care: Concepts for Clinicians to Evaluate the Benefits, Harms, and Costs of Medical Interventions , 2011, Annals of Internal Medicine.

[55]  Ruth Etzioni,et al.  Personalizing age of cancer screening cessation based on comorbid conditions: model estimates of harms and benefits. , 2014, Annals of internal medicine.

[56]  C. Williams,et al.  Depth of insertion at flexible sigmoidoscopy: implications for colorectal cancer screening and instrument design. , 1999, Endoscopy.

[57]  R. Pearson Association of Colonoscopy and Death from Colorectal Cancer , 2009 .

[58]  T. Stukel,et al.  Association between colonoscopy and colorectal cancer mortality in a US cohort according to site of cancer and colonoscopist specialty. , 2012, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[59]  D W Day,et al.  Polyps and cancer of the large bowel: a necropsy study in Liverpool. , 1982, Gut.

[60]  William Hazelton,et al.  Benefits and Harms of Computed Tomography Lung Cancer Screening Strategies: A Comparative Modeling Study for the U.S. Preventive Services Task Force , 2014, Annals of Internal Medicine.

[61]  M. Phipps,et al.  Screening for Colorectal Cancer: US Preventive Services Task Force Recommendation Statement. , 2016, JAMA.

[62]  Perry J Pickhardt,et al.  Screening for colorectal neoplasia with CT colonography: initial experience from the 1st year of coverage by third-party payers. , 2006, Radiology.

[63]  Shalini L Kulasingam,et al.  Screening for Cervical Cancer: A Modeling Study for the US Preventive Services Task Force , 2013, Journal of lower genital tract disease.

[64]  A. Neugut,et al.  Risk of perforation after colonoscopy and sigmoidoscopy: a population-based study. , 2003, Journal of the National Cancer Institute.

[65]  D. Lam-Himlin,et al.  Serrated Lesions of the Colorectum: Review and Recommendations From an Expert Panel , 2013 .

[66]  A. Adrain,et al.  A comparison of fecal occult-blood tests for colorectal-cancer screening. , 1996, The New England journal of medicine.

[67]  L. Rabeneck,et al.  Risk of developing proximal versus distal colorectal cancer after a negative colonoscopy: a population-based study. , 2008, Clinical gastroenterology and hepatology : the official clinical practice journal of the American Gastroenterological Association.

[68]  D. Mark Visualizing cost-effectiveness analysis. , 2002, JAMA.