Screening for colorectal cancer: Updated evidence report and systematic review for the US preventive services task force

JAMA - Journal of the American Medical Association

Volumn 315, Issue 23, 2016, Pages 2576-2594

  Lin, Jennifer S ^a   Piper, Margaret A ^a   Perdue, Leslie A ^a   Rutter, Carolyn M ^b,c   Webber, Elizabeth M ^a   O'Connor, Elizabeth ^a   Smith, Ning ^a   Whitlock, Evelyn P ^a  

^a CENTER FOR HEALTH RESEARCH   (United States)

^b GROUP HEALTH RESEARCH INSTITUTE   (United States)

^c RAND CORPORATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CANCER INCIDENCE; CANCER MORTALITY; CANCER RISK; CANCER SCREENING; COLONOSCOPY; COLORECTAL CANCER; COMPARATIVE EFFECTIVENESS; COMPUTER ASSISTED TOMOGRAPHY; DIAGNOSTIC ACCURACY; ENDOSCOPY; HUMAN; INTENTION TO TREAT ANALYSIS; IONIZING RADIATION; META ANALYSIS; MORBIDITY; OCCULT BLOOD; PREVENTIVE HEALTH SERVICE; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); RISK FACTOR; SENSITIVITY AND SPECIFICITY; SIGMOIDOSCOPY; SYSTEMATIC REVIEW; UNITED STATES; ADENOMA; ADVERSE EFFECTS; ADVISORY COMMITTEE; ASYMPTOMATIC DISEASE; CHEMISTRY; COLORECTAL NEOPLASMS; COMPUTED TOMOGRAPHIC COLONOGRAPHY; FECES; IMMUNOHISTOCHEMISTRY; INCIDENTAL FINDING; MEASUREMENT ACCURACY; MORTALITY; PRACTICE GUIDELINE; STATISTICS AND NUMERICAL DATA;

DNA;

ADENOMA; ADVISORY COMMITTEES; ASYMPTOMATIC DISEASES; COLONOGRAPHY, COMPUTED TOMOGRAPHIC; COLONOSCOPY; COLORECTAL NEOPLASMS; DATA ACCURACY; DNA; FECES; HUMANS; IMMUNOHISTOCHEMISTRY; INCIDENTAL FINDINGS; OCCULT BLOOD; PREVENTIVE HEALTH SERVICES; RANDOMIZED CONTROLLED TRIALS AS TOPIC; SENSITIVITY AND SPECIFICITY; SIGMOIDOSCOPY; UNITED STATES;

EID: 84975730903     PISSN: 00987484     EISSN: 15383598     Source Type: Journal    
DOI: 10.1001/jama.2016.3332     Document Type: Article

References (210)

1. Cancer Facts and Figures 2013. American Cancer Society. http://www.cancer.org/research/cancerfactsstatistics/cancerfactsfigures2013/. Accessed May 24, 2016.
2. Centers for Disease Control and Prevention (CDC). Vital signs: colorectal cancer screening test use: United States, 2012. MMWR Morb Mortal Wkly Rep. 2013;62(44):881-888.
3. US Preventive Services Task Force. Screening for colorectal cancer: US Preventive Services Task Force recommendation statement. Ann Intern Med. 2008;149(9):627-637.
4. Levin B, Lieberman DA, McFarland B, et al; American Cancer Society Colorectal Cancer Advisory Group; US Multi-Society Task Force; American College of Radiology Colon Cancer Committee. 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):130-160.
5. Lin JS, Piper MA, Perdue LA, et al. Screening for Colorectal Cancer: A Systematic Evidence Review for the US Preventive Services Task Force: Evidence Synthesis No. 135. Rockville, MD: Agency for Healthcare Research and Quality; 2016. AHRQ publication 14-05203-EF-1.
6. Whitlock EP, Lin J, Liles E, et al. Screening for Colorectal Cancer: An Updated Systematic Review. Rockville, MD: Agency for Healthcare Research and Quality; 2008.
7. Pooler BD, Kim DH, Pickhardt PJ. Potentially important extracolonic findings at screening CT colonography: incidence and outcomes data from a clinical screening program. AJR Am J Roentgenol. 2016;206(2):313-318.
8. Sali L, Mascalchi M, Falchini M, et al; SAVE Study Investigators. Reduced and full-preparation CT colonography, fecal immunochemical test, and colonoscopy for population screening of colorectal cancer: a randomized trial. J Natl Cancer Inst. 2015;108(2):108.
9. Redwood DG, Asay ED, Blake ID, et al. Stool DNA testing for screening detection of colorectal neoplasia in Alaska Native people. Mayo Clin Proc. 2016;91(1):61-70.
10. Lijmer JG, Mol BW, Heisterkamp S, et al. Empirical evidence of design-related bias in studies of diagnostic tests. JAMA. 1999;282(11):1061-1066.
11. Whiting P, Rutjes AW, Reitsma JB, Glas AS, Bossuyt PM, Kleijnen J. Sources of variation and bias in studies of diagnostic accuracy: a systematic review. Ann Intern Med. 2004;140(3):189-202.
12. Leeflang MM, Bossuyt PM, Irwig L. Diagnostic test accuracy may vary with prevalence: implications for evidence-based diagnosis. J Clin Epidemiol. 2009;62(1):5-12.
13. Ransohoff DF, Feinstein AR. Problems of spectrum and bias in evaluating the efficacy of diagnostic tests. N Engl J Med. 1978;299(17):926-930.
14. Rutjes AW, Reitsma JB, Di Nisio M, Smidt N, van Rijn JC, Bossuyt PM. Evidence of bias and variation in diagnostic accuracy studies. CMAJ. 2006;174(4):469-476.
15. Zalis ME, Barish MA, Choi JR, et al; Working Group on Virtual Colonoscopy. CT colonography reporting and data system: a consensus proposal. Radiology. 2005;236(1):3-9.
16. Harris RP, Helfand M, Woolf SH, et al; Methods Work Group, Third US Preventive Services Task Force. Current methods of the US Preventive Services Task Force: a review of the process. Am J Prev Med. 2001;20(3)(suppl):21-35.
17. National Institute for Health and Clinical Excellence. The Guidelines Manual. London, UK: National Institute for Health and Clinical Excellence; 2006.
18. Shea BJ, Grimshaw JM, Wells GA, et al. Development of AMSTAR: a measurement tool to assess the methodological quality of systematic reviews. BMC Med Res Methodol. 2007;7:10.
19. Wells GA, Shea B, O'Connell D, et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analysis. Ottawa Hospital Research Institute. http://www.ohri.ca/programs/clinical-epidemiology/oxford.asp. Accessed May 25, 2016.
20. Whiting P, Rutjes AW, Reitsma JB, Bossuyt PM, Kleijnen J. The development of QUADAS: a tool for the quality assessment of studies of diagnostic accuracy included in systematic reviews. BMC Med Res Methodol. 2003;3:25.
21. Whiting PF, Rutjes AW, Westwood ME, et al; QUADAS-2 Group. QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med. 2011;155(8):529-536.
22. Hardy RJ, Thompson SG. A likelihood approach to meta-analysis with random effects. Stat Med. 1996;15(6):619-629.
23. Thompson SG, Sharp SJ. Explaining heterogeneity in meta-analysis: a comparison of methods. Stat Med. 1999;18(20):2693-2708.
24. Guolo A, Varin C. Package metaLik. https://cran.r-project.org/web/packages/metaLik/index.html. Accessed May 25, 2016.
25. Atkin WS, Edwards R, Kralj-Hans I, et al; UK Flexible Sigmoidoscopy Trial Investigators. Once-only flexible sigmoidoscopy screening in prevention of colorectal cancer: a multicentre randomised controlled trial. Lancet. 2010;375 (9726):1624-1633.
26. Berry DP, Clarke P, Hardcastle JD, Vellacott KD. Randomized trial of the addition of flexible sigmoidoscopy to faecal occult blood testing for colorectal neoplasia population screening. Br J Surg. 1997;84(9):1274-1276.
27. Brevinge H, Lindholm E, Buntzen S, Kewenter J. Screening for colorectal neoplasia with faecal occult blood testing compared with flexible sigmoidoscopy directly in a 55-56 years' old population. Int J Colorectal Dis. 1997;12(5):291-295.
28. Faivre J, Dancourt V, Denis B, et al. Comparison between a guaiac and three immunochemical faecal occult blood tests in screening for colorectal cancer. Eur J Cancer. 2012;48(16):2969-2976.
29. Faivre J, Dancourt V, Lejeune C, et al. Reduction in colorectal cancer mortality by fecal occult blood screening in a French controlled study. Gastroenterology. 2004;126(7):1674-1680.
30. Guittet L, Bouvier V, Mariotte N, et al. Comparison of a guaiac and an immunochemical faecal occult blood test for the detection of colonic lesions according to lesion type and location. Br J Cancer. 2009;100(8):1230-1235.
31. Hamza S, Dancourt V, Lejeune C, Bidan JM, Lepage C, Faivre J. Diagnostic yield of a one sample immunochemical test at different cut-off values in an organised screening programme for colorectal cancer. Eur J Cancer. 2013;49(12):2727-2733.
32. Hol L, van Leerdam ME, van Ballegooijen M, et al. Screening for colorectal cancer: randomised trial comparing guaiac-based and immunochemical faecal occult blood testing and flexible sigmoidoscopy. Gut. 2010;59(1):62-68.
33. Kronborg O, Jørgensen OD, Fenger C, Rasmussen M. Randomized study of biennial screening with a faecal occult blood test: results after nine screening rounds. Scand J Gastroenterol. 2004;39(9):846-851.
34. Lindholm E, Brevinge H, Haglind E. Survival benefit in a randomized clinical trial of faecal occult blood screening for colorectal cancer. Br J Surg. 2008;95(8):1029-1036.
35. Malila N, Palva T, Malminiemi O, et al. Coverage and performance of colorectal cancer screening with the faecal occult blood test in Finland. J Med Screen. 2011;18(1):18-23.
36. Nishihara R, Wu K, Lochhead P, et al. Long-term colorectal-cancer incidence and mortality after lower endoscopy. N Engl J Med. 2013;369(12):1095-1105.
37. Quintero E, Castells A, Bujanda L, et al; COLONPREV Study Investigators. Colonoscopy versus fecal immunochemical testing in colorectal-cancer screening. N Engl J Med. 2012; 366(8):697-706.
38. Rasmussen M, Kronborg O, Fenger C, Jørgensen OD. Possible advantages and drawbacks of adding flexible sigmoidoscopy to Hemoccult-II in screening for colorectal cancer: a randomized study. Scand J Gastroenterol. 1999;34(1):73-78.
39. Schoen RE, Pinsky PF, Weissfeld JL, et al; PLCO Project Team. Colorectal-cancer incidence and mortality with screening flexible sigmoidoscopy. N Engl J Med. 2012;366(25):2345-2357.
40. Scholefield JH, Moss SM, Mangham CM, Whynes DK, Hardcastle JD. Nottingham trial of faecal occult blood testing for colorectal cancer: a 20-year follow-up. Gut. 2012;61(7):1036-1040.
41. Segnan N, Armaroli P, Bonelli L, et al; SCORE Working Group. Once-only sigmoidoscopy in colorectal cancer screening: follow-up findings of the Italian Randomized Controlled Trial: SCORE. J Natl Cancer Inst. 2011;103(17):1310-1322.
42. Segnan N, Senore C, Andreoni B, et al; SCORE3 Working Group-Italy. Comparing attendance and detection rate of colonoscopy with sigmoidoscopy and FIT for colorectal cancer screening. Gastroenterology. 2007;132(7):2304-2312.
43. Segnan N, Senore C, Andreoni B, et al; SCORE2 Working Group-Italy. Randomized trial of different screening strategies for colorectal cancer: patient response and detection rates. J Natl Cancer Inst. 2005;97(5):347-357.
44. Shaukat A, Mongin SJ, Geisser MS, et al. Long-term mortality after screening for colorectal cancer. N Engl J Med. 2013;369(12):1106-1114.
45. Stoop EM, de Haan MC, de Wijkerslooth TR, et al. Participation and yield of colonoscopy versus non-cathartic CT colonography in population-based screening for colorectal cancer: a randomised controlled trial. Lancet Oncol. 2012;13(1):55-64.
46. van Roon AH, Goede SL, van Ballegooijen M, et al. Random comparison of repeated faecal immunochemical testing at different intervals for population-based colorectal cancer screening. Gut. 2013;62(3):409-415.
47. van Rossum LG, van Rijn AF, Laheij RJ, et al. Random comparison of guaiac and immunochemical fecal occult blood tests for colorectal cancer in a screening population. Gastroenterology. 2008;135(1):82-90.
48. Verne JECW, Aubrey R, Love SB, Talbot IC, Northover JM. Population based randomized study of uptake and yield of screening by flexible sigmoidoscopy compared with screening by faecal occult blood testing. BMJ. 1998;317(7152):182-185.
49. Zubero MB, Arana-Arri E, Pijoan JI, et al. Population-based colorectal cancer screening: comparison of two fecal occult blood test. Front Pharmacol. 2014;4:175.
50. Atkin WS, Cook CF, Cuzick J, Edwards R, Northover JM, Wardle J; UK Flexible Sigmoidoscopy Screening Trial Investigators. Single flexible sigmoidoscopy screening to prevent colorectal cancer: baseline findings of a UK multicentre randomised trial. Lancet. 2002;359(9314):1291-1300.
51. Atkin WS, Cuzick J, Northover JM, Whynes DK. Prevention of colorectal cancer by once-only sigmoidoscopy. Lancet. 1993;341(8847):736-740.
52. Bretthauer M, Gondal G, Larsen K, et al. Design, organization and management of a controlled population screening study for detection of colorectal neoplasia: attendance rates in the NORCCAP study (Norwegian Colorectal Cancer Prevention). Scand J Gastroenterol. 2002;37(5): 568-573.
53. de Wijkerslooth TR, de Haan MC, Stoop EM, et al. Study protocol: population screening for colorectal cancer by colonoscopy or CT colonography: a randomized controlled trial. BMC Gastroenterol. 2010;10:47.
54. Denters MJ, Deutekom M, Bossuyt PM, Stroobants AK, Fockens P, Dekker E. Lower risk of advanced neoplasia among patients with a previous negative result from a fecal test for colorectal cancer. Gastroenterology. 2012;142(3):497-504.
55. Denters MJ, Deutekom M, Fockens P, Bossuyt PM, Dekker E. Implementation of population screening for colorectal cancer by repeated fecal occult blood test in the Netherlands. BMC Gastroenterol. 2009;9:28.
56. Faivre J, Dancourt V, Manfredi S, et al. Positivity rates and performances of immunochemical faecal occult blood tests at different cut-off levels within a colorectal cancer screening programme. Dig Liver Dis. 2012;44(8):700-704.
57. Guittet L, Bouvier V, Guillaume E, et al. Colorectal cancer screening: why immunochemical faecal occult blood test performs as well with either one or two samples. Dig Liver Dis. 2012;44(8):694-699.
58. Guittet L, Bouvier V, Mariotte N, et al. Performance of immunochemical faecal occult blood test in colorectal cancer screening in average-risk population according to positivity threshold and number of samples. Int J Cancer. 2009;125(5):1127-1133.
59. Hardcastle JD, Chamberlain JO, Robinson MH, et al. Randomised controlled trial of faecal-occult-blood screening for colorectal cancer. Lancet. 1996;348(9040):1472-1477.
60. Holme Ø, Løberg M, Kalager M, et al. Effect of flexible sigmoidoscopy screening on colorectal cancer incidence and mortality: a randomized clinical trial. JAMA. 2014;312(6):606-615.
61. Kewenter J, Brevinge H, Engarås B, Haglind E, Ahrén C. Results of screening, rescreening, and follow-up in a prospective randomized study for detection of colorectal cancer by fecal occult blood testing: results for 68,308 subjects. Scand J Gastroenterol. 1994;29(5):468-473.
62. Malila N, Oivanen T, Malminiemi O, Hakama M. Test, episode, and programme sensitivities of screening for colorectal cancer as a public health policy in Finland: experimental design. BMJ. 2008; 337:a2261.
63. Mandel JS, Church TR, Bond JH, et al. The effect of fecal occult-blood screening on the incidence of colorectal cancer. N Engl J Med. 2000; 343(22):1603-1607.
64. Mandel JS, Bond JH, Church TR, et al. Reducing mortality from colorectal cancer by screening for fecal occult blood: Minnesota Colon Cancer Control Study. N Engl J Med. 1993;328(19):1365-1371.
65. Parra-Blanco A, Nicolas-Perez D, Gimeno-Garcia A, et al. The timing of bowel preparation before colonoscopy determines the quality of cleansing, and is a significant factor contributing to the detection of flat lesions: a randomized study. World J Gastroenterol. 2006;12 (38):6161-6166.
66. Segnan N, Senore C, Andreoni B, et al; SCORE Working Group-Italy. Baseline findings of the Italian multicenter randomized controlled trial of "once-only sigmoidoscopy": SCORE. J Natl Cancer Inst. 2002;94(23):1763-1772.
67. Thomas W, White CM, Mah J, Geisser MS, Church TR, Mandel JS. Longitudinal compliance with annual screening for fecal occult blood: Minnesota Colon Cancer Control Study. Am J Epidemiol. 1995;142(2):176-182.
68. Atkin WS, Cook CF, Cuzick J, Edwards R, Northover JM, Wardle J; UK Flexible Sigmoidoscopy Screening Trial Investigators. Single flexible sigmoidoscopy screening to prevent colorectal cancer: baseline findings of a UK multicentre randomised trial. Lancet. 2002;359(9314):1291-1300.
69. van Roon AH, Wilschut JA, Hol L, et al. Diagnostic yield improves with collection of 2 samples in fecal immunochemical test screening without affecting attendance. Clin Gastroenterol Hepatol. 2011;9(4):333-339.
70. van Dam L, de Wijkerslooth TR, de Haan MC, et al. Time requirements and health effects of participation in colorectal cancer screening with colonoscopy or computed tomography colonography in a randomized controlled trial. Endoscopy. 2013;45(3):182-188.
71. Weissfeld JL, Schoen RE, Pinsky PF, et al; PLCO Project Team. Flexible sigmoidoscopy in the PLCO cancer screening trial: results from the baseline screening examination of a randomized trial. J Natl Cancer Inst. 2005;97(13):989-997.
72. Allison JE, Sakoda LC, Levin TR, et al. Screening for colorectal neoplasms with new fecal occult blood tests: update on performance characteristics. J Natl Cancer Inst. 2007;99(19):1462-1470.
73. Allison JE, Tekawa IS, Ransom LJ, Adrain AL. A comparison of fecal occult-blood tests for colorectal-cancer screening. N Engl J Med. 1996; 334(3):155-159.
74. Brenner H, Tao S. Superior diagnostic performance of faecal immunochemical tests for haemoglobin in a head-to-head comparison with guaiac based faecal occult blood test among 2235 participants of screening colonoscopy. Eur J Cancer. 2013;49(14):3049-3054.
75. Castiglione G, Visioli CB, Ciatto S, et al. Sensitivity of latex agglutination faecal occult blood test in the Florence District population-based colorectal cancer screening programme. Br J Cancer. 2007;96(11):1750-1754.
76. Chen LS, Yen AM, Chiu SY, Liao CS, Chen HH. Baseline faecal occult blood concentration as a predictor of incident colorectal neoplasia: longitudinal follow-up of a Taiwanese population-based colorectal cancer screening cohort. Lancet Oncol. 2011;12(6):551-558.
77. Cheng TI, Wong JM, Hong CF, et al. Colorectal cancer screening in asymptomatic adults: comparison of colonoscopy, sigmoidoscopy and fecal occult blood tests. J Formos Med Assoc. 2002; 101(10):685-690.
78. Chiu HM, Lee YC, Tu CH, et al. Association between early stage colon neoplasms and false-negative results from the fecal immunochemical test. Clin Gastroenterol Hepatol. 2013;11(7):832-8.e1,2.
79. Church TR, Wandell M, Lofton-Day C, et al; PRESEPT Clinical Study Steering Committee, Investigators and Study Team. Prospective evaluation of methylated SEPT9 in plasma for detection of asymptomatic colorectal cancer. Gut. 2014;63(2):317-325.
80. de Wijkerslooth TR, Stoop EM, Bossuyt PM, et al. Immunochemical fecal occult blood testing is equally sensitive for proximal and distal advanced neoplasia. Am J Gastroenterol. 2012;107(10):1570-1578.
81. Fletcher JG, Silva AC, Fidler JL, et al. Noncathartic CT colonography: image quality assessment and performance and in a screening cohort. AJR Am J Roentgenol. 2013;201(4):787-794.
82. Graser A, Stieber P, Nagel D, et al. Comparison of CT colonography, colonoscopy, sigmoidoscopy and faecal occult blood tests for the detection of advanced adenoma in an average risk population. Gut. 2009;58(2):241-248.
83. Imperiale TF, Ransohoff DF, Itzkowitz SH, et al. Multitarget stool DNA testing for colorectal-cancer screening. N Engl J Med. 2014;370(14):1287-1297.
84. Itoh M, Takahashi K, Nishida H, Sakagami K, Okubo T. Estimation of the optimal cut off point in a new immunological faecal occult blood test in a corporate colorectal cancer screening programme. J Med Screen. 1996;3(2):66-71.
85. Johnson CD, Chen MH, Toledano AY, et al. Accuracy of CT colonography for detection of large adenomas and cancers. N Engl J Med. 2008;359 (12):1207-1217.
86. Johnson CD, Fletcher JG, MacCarty RL, et al. Effect of slice thickness and primary 2D versus 3D virtual dissection on colorectal lesion detection at CT colonography in 452 asymptomatic adults. AJR Am J Roentgenol. 2007;189(3):672-680.
87. Kim YS, Kim N, Kim SH, et al. The efficacy of intravenous contrast-enhanced 16-raw multidetector CT colonography for detecting patients with colorectal polyps in an asymptomatic population in Korea. J Clin Gastroenterol. 2008;42 (7):791-798.
88. Launoy GD, Bertrand HJ, Berchi C, et al. Evaluation of an immunochemical fecal occult blood test with automated reading in screening for colorectal cancer in a general average-risk population. Int J Cancer. 2005;115(3):493-496.
89. Lefere P, Silva C, Gryspeerdt S, et al. Teleradiology based CT colonography to screen a population group of a remote island; at average risk for colorectal cancer. Eur J Radiol. 2013;82(6):e262-e267.
90. Levi Z, Birkenfeld S, Vilkin A, 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. Int J Cancer. 2011;128(10):2415-2424.
91. Levy BT, Bay C, Xu Y, et al. Test characteristics of faecal immunochemical tests (FIT) compared with optical colonoscopy. J Med Screen. 2014;21(3): 133-143.
92. Lin JS, Webber EM, Beil TL, Goddard KA, Whitlock EP. Fecal DNA Testing in Screening for Colorectal Cancer in Average-Risk Adults. Rockville, MD: Agency for Healthcare Research and Quality; 2012. AHRQ publication 12-EHC022-EF.
93. Macari M, Bini EJ, Jacobs SL, et al. Colorectal polyps and cancers in asymptomatic average-risk patients: evaluation with CT colonography. Radiology. 2004;230(3):629-636.
94. Morikawa T, Kato J, Yamaji Y, Wada R, Mitsushima T, Shiratori Y. A comparison of the immunochemical fecal occult blood test and total colonoscopy in the asymptomatic population. Gastroenterology. 2005;129(2):422-428.
95. Nakama H, Yamamoto M, Kamijo N, et al. Colonoscopic evaluation of immunochemical fecal occult blood test for detection of colorectal neoplasia. Hepatogastroenterology. 1999;46(25): 228-231.
96. Nakama H, Kamijo N, Abdul Fattah AS, Zhang B. Validity of immunochemical faecal occult blood screening for colorectal cancer: a follow up study. J Med Screen. 1996;3(2):63-65.
97. Ng SC, Ching JY, Chan V, et al. Diagnostic accuracy of faecal immunochemical test for screening individuals with a family history of colorectal cancer. Aliment Pharmacol Ther. 2013;38 (7):835-841.
98. Park DI, Ryu S, Kim YH, et al. Comparison of guaiac-based and quantitative immunochemical fecal occult blood testing in a population at average risk undergoing colorectal cancer screening. Am J Gastroenterol. 2010;105(9):2017-2025.
99. Pickhardt PJ, Choi JR, Hwang I, et al. Computed tomographic virtual colonoscopy to screen for colorectal neoplasia in asymptomatic adults. N Engl J Med. 2003;349(23):2191-2200.
100. Sohn DK, Jeong SY, Choi HS, et al. Single immunochemical fecal occult blood test for detection of colorectal neoplasia. Cancer Res Treat. 2005;37(1):20-23.
101. Zalis ME, Blake MA, Cai W, et al. Diagnostic accuracy of laxative-free computed tomographic colonography for detection of adenomatous polyps in asymptomatic adults: a prospective evaluation. Ann Intern Med. 2012;156(10):692-702.
102. Chiang TH, Chuang SL, Chen SL, et al. Difference in performance of fecal immunochemical tests with the same hemoglobin cutoff concentration in a nationwide colorectal cancer screening program. Gastroenterology. 2014; 147(6):1317-1326.
103. Hernandez V, Cubiella J, Gonzalez-Mao MC, et al; COLONPREV Study Investigators. Fecal immunochemical test accuracy in average-risk colorectal cancer screening. World J Gastroenterol. 2014;20(4):1038-1047.
104. Lee YH, Hur M, Kim H, et al. Optimal cut-off concentration for a faecal immunochemical test for haemoglobin by Hemo Techt NS-Plus C15 system for the colorectal cancer screening. Clin Chem Lab Med. 2015;53(3):e69-e71.
105. Cologuard summary of safety and effectiveness data (SSED). US Food and Drug Administration. http://www.accessdata.fda.gov/cdrh-docs/pdf13/P130017b.pdf. Accessed May 25, 2016.
106. Ahlquist DA, Sargent DJ, Loprinzi CL, et al. Stool DNA and occult blood testing for screen detection of colorectal neoplasia. Ann Intern Med. 2008;149(7):441-450, W81.
107. Brenner H, Haug U, Hundt S. Inter-test agreement and quantitative cross-validation of immunochromatographical fecal occult blood tests. Int J Cancer. 2010;127(7):1643-1649.
108. Brenner H, Haug U, Hundt S. Sex differences in performance of fecal occult blood testing. Am J Gastroenterol. 2010;105(11):2457-2464.
109. Grazzini G, Castiglione G, Ciabattoni C, et al. Colorectal cancer screening programme by faecal occult blood test in Tuscany: first round results. Eur J Cancer Prev. 2004;13(1):19-26.
110. Haug U, Kuntz KM, Knudsen AB, Hundt S, Brenner H. Sensitivity of immunochemical faecal occult blood testing for detecting left- vs right-sided colorectal neoplasia. Br J Cancer. 2011; 104(11):1779-1785.
111. Haug U, Hillebrand T, Bendzko P, et al. Mutant-enriched PCR and allele-specific hybridization reaction to detect K-ras mutations in stool DNA: high prevalence in a large sample of older adults. Clin Chem. 2007;53(4):787-790.
112. Hundt S, Haug U, Brenner H. Comparative evaluation of immunochemical fecal occult blood tests for colorectal adenoma detection. Ann Intern Med. 2009;150(3):162-169.
113. Imperiale TF, Ransohoff DF, Itzkowitz SH, Turnbull BA, Ross ME; Colorectal Cancer Study Group. Fecal DNA versus fecal occult blood for colorectal-cancer screening in an average-risk population. N Engl J Med. 2004;351(26):2704-2714.
114. Johnson CD, Herman BA, Chen MH, et al. The National CT Colonography Trial: assessment of accuracy in participants 65 years of age and older. Radiology. 2012;263(2):401-408.
115. Morikawa T, Kato J, Yamaji Y, et al. Sensitivity of immunochemical fecal occult blood test to small colorectal adenomas. Am J Gastroenterol. 2007;102 (10):2259-2264.
116. Adeyemo A, Bannazadeh M, Riggs T, Shellnut J, Barkel D, Wasvary H. Does sedation type affect colonoscopy perforation rates? Dis Colon Rectum. 2014;57(1):110-114.
117. Adler A, Wegscheider K, Lieberman D, et al. Factors determining the quality of screening colonoscopy: a prospective study on adenoma detection rates, from 12,134 examinations (Berlin colonoscopy project 3, BECOP-3). Gut. 2013;62(2): 236-241.
118. An S, Lee KH, Kim YH, et al. Screening CT colonography in an asymptomatic average-risk Asian population: a 2-year experience in a single institution. AJR Am J Roentgenol. 2008;191(3): W100-W106.
119. Arora G, Mannalithara A, Singh G, Gerson LB, Triadafilopoulos G. Risk of perforation from a colonoscopy in adults: a large population-based study. Gastrointest Endosc. 2009;69(3 Pt 2):654-664.
120. Bair D, Pham J, Seaton MB, Arya N, Pryce M, Seaton TL. The quality of screening colonoscopies in an office-based endoscopy clinic. Can J Gastroenterol. 2009;23(1):41-47.
121. Berhane C, Denning D. Incidental finding of colorectal cancer in screening colonoscopy and its cost effectiveness. Am Surg. 2009;75(8):699-703.
122. Bielawska B, Day AG, Lieberman DA, Hookey LC. Risk factors for early colonoscopic perforation include non-gastroenterologist endoscopists: a multivariable analysis. Clin Gastroenterol Hepatol. 2014;12(1):85-92.
123. Blotière PO, Weill A, Ricordeau P, Alla F, Allemand H. Perforations and haemorrhages after colonoscopy in 2010: a study based on comprehensive French health insurance data (SNIIRAM). Clin Res Hepatol Gastroenterol. 2014;38 (1):112-117.
124. Bokemeyer B, Bock H, Hüppe D, et al. Screening colonoscopy for colorectal cancer prevention: results from a German online registry on 269000 cases. Eur J Gastroenterol Hepatol. 2009;21(6):650-655.
125. Cash BD, Riddle MS, Bhattacharya I, et al. CT colonography of a Medicare-aged population: outcomes observed in an analysis of more than 1400 patients. AJR Am J Roentgenol. 2012;199(1): W27-W34.
126. Castro G, Azrak MF, Seeff LC, Royalty J. Outpatient colonoscopy complications in the CDC's Colorectal Cancer Screening Demonstration Program: a prospective analysis. Cancer. 2013;119(suppl 15):2849-2854.
127. Chin M, Mendelson R, Edwards J, Foster N, Forbes G. Computed tomographic colonography: prevalence, nature, and clinical significance of extracolonic findings in a community screening program. Am J Gastroenterol. 2005;100(12):2771-2776.
128. Chukmaitov A, Bradley CJ, Dahman B, Siangphoe U, Warren JL, Klabunde CN. Association of polypectomy techniques, endoscopist volume, and facility type with colonoscopy complications. Gastrointest Endosc. 2013;77(3):436-446.
129. Cooper GS, Kou TD, Rex DK. Complications following colonoscopy with anesthesia assistance: a population-based analysis. JAMA Intern Med. 2013;173(7):551-556.
130. Cotterill M, Gasparelli R, Kirby E. Colorectal cancer detection in a rural community: development of a colonoscopy screening program. Can Fam Physician. 2005;51:1224-1228.
131. Crispin A, Birkner B, Munte A, Nusko G, Mansmann U. Process quality and incidence of acute complications in a series of more than 230,000 outpatient colonoscopies. Endoscopy. 2009;41(12):1018-1025.
132. Dancourt V, Lejeune C, Lepage C, Gailliard MC, Meny B, Faivre J. Immunochemical faecal occult blood tests are superior to guaiac-based tests for the detection of colorectal neoplasms. Eur J Cancer. 2008;44(15):2254-2258.
133. Dominitz JA, Baldwin LM, Green P, Kreuter WI, Ko CW. Regional variation in anesthesia assistance during outpatient colonoscopy is not associated with differences in polyp detection or complication rates. Gastroenterology. 2013;144(2): 298-306.
134. Durbin JM, Stroup SP, Altamar HO, L'esperance JO, Lacey DR, Auge BK. Genitourinary abnormalities in an asymptomatic screening population: findings on virtual colonoscopy. Clin Nephrol. 2012;77(3):204-210.
135. Edwards JT, Mendelson RM, Fritschi L, et al. Colorectal neoplasia screening with CT colonography in average-risk asymptomatic subjects: community-based study. Radiology. 2004;230(2):459-464.
136. Ferlitsch M, Reinhart K, Pramhas S, et al. Sex-specific prevalence of adenomas, advanced adenomas, and colorectal cancer in individuals undergoing screening colonoscopy. JAMA. 2011; 306(12):1352-1358.
137. Flicker MS, Tsoukas AT, Hazra A, Dachman AH. Economic impact of extracolonic findings at computed tomographic colonography. J Comput Assist Tomogr. 2008;32(4):497-503.
138. Ginnerup Pedersen B, Rosenkilde M, Christiansen TE, Laurberg S. Extracolonic findings at computed tomography colonography are a challenge. Gut. 2003;52(12):1744-1747.
139. Gluecker TM, Johnson CD, Wilson LA, et al. Extracolonic findings at CT colonography: evaluation of prevalence and cost in a screening population. Gastroenterology. 2003;124(4):911-916.
140. Hamdani U, Naeem R, Haider F, et al. Risk factors for colonoscopic perforation: a population-based study of 80118 cases. World J Gastroenterol. 2013;19(23):3596-3601.
141. Hara AK, Johnson CD, MacCarty RL, Welch TJ. Incidental extracolonic findings at CT colonography. Radiology. 2000;215(2):353-357.
142. Ho JM, Gruneir A, Fischer HD, et al. Serious events in older Ontario residents receiving bowel preparations for outpatient colonoscopy with various comorbidity profiles: a descriptive, population-based study. Can J Gastroenterol. 2012; 26(7):436-440.
143. Hoff G, Thiis-Evensen E, Grotmol T, Sauar J, Vatn MH, Moen IE. Do undesirable effects of screening affect all-cause mortality in flexible sigmoidoscopy programmes? experience from the Telemark Polyp Study 1983-1996. Eur J Cancer Prev. 2001;10(2):131-137.
144. Hsieh TK, Hung L, Kang FC, Lan KM, Poon PW, So EC. Anesthesia does not increase the rate of bowel perforation during colonoscopy: a retrospective study. Acta Anaesthesiol Taiwan. 2009;47(4):162-166.
145. Iafrate F, Iussich G, Correale L, et al. Adverse events of computed tomography colonography: an Italian National Survey. Dig Liver Dis. 2013;45(8): 645-650.
146. Jain A, Falzarano J, Jain A, Decker R, Okubo G, Fujiwara D. Outcome of 5,000 flexible sigmoidoscopies done by nurse endoscopists for colorectal screening in asymptomatic patients. Hawaii Med J. 2002;61(6):118-120.
147. Kamath AS, Iqbal CW, Sarr MG, et al. Colonoscopic splenic injuries: incidence and management. J Gastrointest Surg. 2009;13(12): 2136-2140.
148. Kang HY, Kang HW, Kim SG, et al. Incidence and management of colonoscopic perforations in Korea. Digestion. 2008;78(4):218-223.
149. Kao KT, Jain A, Sheinbaum A. Ischemic colitis following routine screening colonoscopy: a case report. Endoscopy. 2009;41(suppl 2):E100.
150. Kim DH, Pickhardt PJ, Taylor AJ, et al. CT colonography versus colonoscopy for the detection of advanced neoplasia. N Engl J Med. 2007;357 (14):1403-1412.
151. Kim JS, Kim BW, Kim JI, et al. Endoscopic clip closure versus surgery for the treatment of iatrogenic colon perforations developed during diagnostic colonoscopy: a review of 115,285 patients. Surg Endosc. 2013;27(2):501-504.
152. Kim YS, Kim N, Kim SY, et al. Extracolonic findings in an asymptomatic screening population undergoing intravenous contrast-enhanced computed tomography colonography. J Gastroenterol Hepatol. 2008;23(7 Pt 2):e49-e57.
153. Ko CW, Riffle S, Shapiro JA, et al. Incidence of minor complications and time lost from normal activities after screening or surveillance colonoscopy. Gastrointest Endosc. 2007;65(4): 648-656.
154. Korman LY, Overholt BF, Box T, Winker CK. Perforation during colonoscopy in endoscopic ambulatory surgical centers. Gastrointest Endosc. 2003;58(4):554-557.
155. Layton JB, Klemmer PJ, Christiansen CF, et al. Sodium phosphate does not increase risk for acute kidney injury after routine colonoscopy, compared with polyethylene glycol. Clin Gastroenterol Hepatol. 2014;12(9):1514-1521.
156. Levin TR, Zhao W, Conell C, et al. Complications of colonoscopy in an integrated health care delivery system. Ann Intern Med. 2006; 145(12):880-886.
157. Levin TR, Conell C, Shapiro JA, Chazan SG, Nadel MR, Selby JV. Complications of screening flexible sigmoidoscopy. Gastroenterology. 2002;123 (6):1786-1792.
158. Loffeld RJ, Engel A, Dekkers PE. Incidence and causes of colonoscopic perforations: a single-center case series. Endoscopy. 2011;43(3):240-242.
159. Lorenzo-Zúñiga V, Moreno de Vega V, Doménech E, Mañosa M, Planas R, Boix J. Endoscopist experience as a risk factor for colonoscopic complications. Colorectal Dis. 2010;12 (10 online):e273-e277.
160. Macari M, Nevsky G, Bonavita J, Kim DC, Megibow AJ, Babb JS. CT colonography in senior versus nonsenior patients: extracolonic findings, recommendations for additional imaging, and polyp prevalence. Radiology. 2011;259(3):767-774.
161. Mansmann U, Crispin A, Henschel V, et al. Epidemiology and quality control of 245 000 outpatient colonoscopies. Dtsch Arztebl Int. 2008; 105(24):434-440.
162. Multicentre Australian Colorectal-neoplasia Screening (MACS) Group. A comparison of colorectal neoplasia screening tests: a multicentre community-based study of the impact of consumer choice. Med J Aust. 2006;184(11):546-550.
163. Nelson DB, McQuaid KR, Bond JH, Lieberman DA, Weiss DG, Johnston TK. Procedural success and complications of large-scale screening colonoscopy. Gastrointest Endosc. 2002;55(3):307-314.
164. O'Connor SD, Pickhardt PJ, Kim DH, Oliva MR, Silverman SG. Incidental finding of renal masses at unenhanced CT: prevalence and analysis of features for guiding management. AJR Am J Roentgenol. 2011;197(1):139-145.
165. Parente F, Boemo C, Ardizzoia A, et al. Outcomes and cost evaluation of the first two rounds of a colorectal cancer screening program based on immunochemical fecal occult blood test in northern Italy. Endoscopy. 2013;45(1):27-34.
166. Pickhardt PJ, Boyce CJ, Kim DH, Hinshaw LJ, Taylor AJ, Winter TC. Should small sliding hiatal hernias be reported at CT colonography? AJR Am J Roentgenol. 2011;196(4):W400-W404.
167. Pickhardt PJ, Kim DH, Meiners RJ, et al. Colorectal and extracolonic cancers detected at screening CT colonography in 10,286 asymptomatic adults. Radiology. 2010;255(1):83-88.
168. Pickhardt PJ, Kim DH, Taylor AJ, Gopal DV, Weber SM, Heise CP. Extracolonic tumors of the gastrointestinal tract detected incidentally at screening CT colonography. Dis Colon Rectum. 2007;50(1):56-63.
169. Pickhardt PJ. Incidence of colonic perforation at CT colonography: review of existing data and implications for screening of asymptomatic adults. Radiology. 2006;239(2):313-316.
170. Pox CP, Altenhofen L, Brenner H, Theilmeier A, Von Stillfried D, Schmiegel W. Efficacy of a nationwide screening colonoscopy program for colorectal cancer. Gastroenterology. 2012;142(7): 1460-1467.
171. Quallick MR, Brown WR. Rectal perforation during colonoscopic retroflexion: a large, prospective experience in an academic center. Gastrointest Endosc. 2009;69(4):960-963.
172. Rabeneck L, Paszat LF, Hilsden RJ, et al. Bleeding and perforation after outpatient colonoscopy and their risk factors in usual clinical practice. Gastroenterology. 2008;135(6):1899-1906.
173. Rathgaber SW, Wick TM. Colonoscopy completion and complication rates in a community gastroenterology practice. Gastrointest Endosc. 2006;64(4):556-562.
174. Rutter CM, Johnson E, Miglioretti DL, Mandelson MT, Inadomi J, Buist DS. Adverse events after screening and follow-up colonoscopy. Cancer Causes Control. 2012;23(2):289-296.
175. Sagawa T, Kakizaki S, Iizuka H, et al. Analysis of colonoscopic perforations at a local clinic and a tertiary hospital. World J Gastroenterol. 2012;18 (35):4898-4904.
176. Senore C, Ederle A, Fantin A, et al. Acceptability and side-effects of colonoscopy and sigmoidoscopy in a screening setting. J Med Screen. 2011;18(3):128-134.
177. Sieg A, Hachmoeller-Eisenbach U, Eisenbach T. Prospective evaluation of complications in outpatient GI endoscopy: a survey among German gastroenterologists. Gastrointest Endosc. 2001;53 (6):620-627.
178. Singh H, Penfold RB, DeCoster C, et al. Colonoscopy and its complications across a Canadian regional health authority. Gastrointest Endosc. 2009;69(3 Pt 2):665-671.
179. Sosna J, Blachar A, Amitai M, et al. Colonic perforation at CT colonography: assessment of risk in a multicenter large cohort. Radiology. 2006;239 (2):457-463.
180. Stock C, Ihle P, Sieg A, Schubert I, Hoffmeister M, Brenner H. Adverse events requiring hospitalization within 30 days after outpatient screening and nonscreening colonoscopies. Gastrointest Endosc. 2013;77(3):419-429.
181. Strul H, Kariv R, Leshno M, et al. The prevalence rate and anatomic location of colorectal adenoma and cancer detected by colonoscopy in average-risk individuals aged 40-80 years. Am J Gastroenterol. 2006;101(2):255-262.
182. Suissa A, Bentur OS, Lachter J, et al. Outcome and complications of colonoscopy: a prospective multicenter study in northern Israel. Diagn Ther Endosc. 2012;2012:612542.
183. Tam MS, Abbas MA. Perforation following colorectal endoscopy: what happens beyond the endoscopy suite? Perm J. 2013;17(2):17-21.
184. Veerappan GR, Ally MR, Choi JH, Pak JS, Maydonovitch C, Wong RK. Extracolonic findings on CT colonography increases yield of colorectal cancer screening. AJR Am J Roentgenol. 2010;195 (3):677-686.
185. Viiala CH, Olynyk JK. Outcomes after 10 years of a community-based flexible sigmoidoscopy screening program for colorectal carcinoma. Med J Aust. 2007;187(5):274-277.
186. Wallace MB, Kemp JA, Meyer F, et al. Screening for colorectal cancer with flexible sigmoidoscopy by nonphysician endoscopists. Am J Med. 1999;107(3):214-218.
187. Warren JL, Klabunde CN, Mariotto AB, et al. Adverse events after outpatient colonoscopy in the Medicare population. Ann Intern Med. 2009;150 (12):849-857, W152.
188. Xirasagar S, Hurley TG, Sros L, Hebert JR. Quality and safety of screening colonoscopies performed by primary care physicians with standby specialist support. Med Care. 2010;48(8):703-709.
189. Zafar HM, Harhay MO, Yang J, Armstron K. Adverse events following computed tomographic colonography compared to optical colonoscopy in the elderly. Prev Med Rep. 2014;1:3-8.
190. Ko CW, Riffle S, Michaels L, et al. Serious complications within 30 days of screening and surveillance colonoscopy are uncommon. Clin Gastroenterol Hepatol. 2010;8(2):166-173.
191. Atkin WS, Hart A, Edwards R, et al. Uptake, yield of neoplasia, and adverse effects of flexible sigmoidoscopy screening. Gut. 1998;42(4):560-565.
192. Gondal G, Grotmol T, Hofstad B, Bretthauer M, Eide TJ, Hoff G. The Norwegian Colorectal Cancer Prevention (NORCCAP) screening study: baseline findings and implementations for clinical work-up in age groups 50-64 years. Scand J Gastroenterol. 2003;38(6):635-642.
193. Hoff G, Grotmol T, Skovlund E, Bretthauer M; Norwegian Colorectal Cancer Prevention Study Group. Risk of colorectal cancer seven years after flexible sigmoidoscopy screening: randomised controlled trial. BMJ. 2009;338:b1846.
194. Hoff G, Sauar J, Vatn MH, et al. Polypectomy of adenomas in the prevention of colorectal cancer: 10 years' follow-up of the Telemark Polyp Study I: a prospective, controlled population study. Scand J Gastroenterol. 1996;31(10):1006-1010.
195. Kim DH, Pickhardt PJ, Hanson ME, Hinshaw JL. CT colonography: performance and program outcome measures in an older screening population. Radiology. 2010;254(2):493-500.
196. Miles A, Wardle J, McCaffery K, Williamson S, Atkin W. The effects of colorectal cancer screening on health attitudes and practices. Cancer Epidemiol Biomarkers Prev. 2003;12(7):651-655.
197. Pickhardt PJ, Kim DH, Robbins JB. Flat (nonpolypoid) colorectal lesions identified at CT colonography in a US screening population. Acad Radiol. 2010;17(6):784-790.
198. Pickhardt PJ, Hanson ME, Vanness DJ, et al. Unsuspected extracolonic findings at screening CT colonography: clinical and economic impact. Radiology. 2008;249(1):151-159.
199. Regula J, Polkowski M. CT colonography versus colonoscopy for the detection of advanced neoplasia. N Engl J Med. 2008;358(1):88-89.
200. Thiis-Evensen E, Hoff GS, Sauar J, Langmark F, Majak BM, Vatn MH. Population-based surveillance by colonoscopy: effect on the incidence of colorectal cancer: Telemark Polyp Study I. Scand J Gastroenterol. 1999;34(4):414-420.
201. Lord SJ, Irwig L, Simes RJ. When is measuring sensitivity and specificity sufficient to evaluate a diagnostic test, and when do we need randomized trials? Ann Intern Med. 2006;144(11):850-855.
202. Exact Sciences: additional update on CMS reimbursement for Cologuard [press release]. http://investor.exactsciences.com/investor-relations/press-releases/press-release-details/2015/Exact-Sciences-Additional-Update-on-CMS-Reimbursement-for-Cologuard/default.aspx. Accessed May 25, 2016.
203. Kaminski MF, Bretthauer M, Zauber AG, et al. The NordICC Study: rationale and design of a randomized trial on colonoscopy screening for colorectal cancer. Endoscopy. 2012;44(7):695-702.
204. Castells A, Quintero E. Programmatic screening for colorectal cancer: the COLONPREV study. Dig Dis Sci. 2015;60(3):672-680.
205. Álvarez C, Andreu M, Castells A, et al; ColonPrev study investigators. Relationship of colonoscopy-detected serrated polyps with synchronous advanced neoplasia in average-risk individuals. Gastrointest Endosc. 2013;78(2):333-341.
206. Colonoscopy Versus Fecal Immunochemical Test in Reducing Mortality From Colorectal Cancer (CONFIRM). ClinicalTrials.gov. https://clinicaltrials.gov/ct2/show/NCT01239082. Accessed May 25, 2016.
207. Committee to Assess Health Risks from Exposure to Low Levels of Ionizing Radiation, Board on Radiation Effects Research, Division on Earth and Life Studies, National Research Council of the National Academies. Health Risks From Exposure to Low Levels of Ionizing Radiation: BEIR VII Phase 2. Washington, DC: National Academies Press; 2006.
208. Cardis E, Vrijheid M, Blettner M, et al. Risk of cancer after low doses of ionising radiation: retrospective cohort study in 15 countries. BMJ. 2005;331(7508):77.
209. Brenner DJ, Hall EJ. Computed tomography: an increasing source of radiation exposure. N Engl J Med. 2007;357(22):2277-2284.
210. Knudsen AB, Zauber AG, Rutter CM, et al. Estimation of benefits, burden, and harms of colorectal cancer screening strategies: modeling study for the US Preventive Services Task Force. JAMA. doi:10.1001/jama.2016.6828.