J Korean Soc Radiol.  2012 Apr;66(4):385-406. 10.3348/jksr.2012.66.4.385.

Korean Guidelines for Colorectal Cancer Screening and Polyp Detection

• Lee BI
• Hong SP
• Kim SE
• Kim SH
• Kim HS
• Hong SN
• Yang DH
• Shin SJ
• Lee SH
• Kim YH
• Park DI
• Kim HJ
• Yang SK
• Kim HJ
• Jeon HJ
• Multi-Society Task Force for Development of Guidelines for Colorectal Polyp Screening, Surveillance and Management

• KMID: 2208853
• DOI: http://doi.org/10.3348/jksr.2012.66.4.385

Abstract

Colorectal cancer is currently the second most common cancer among Korean males and the fourth most common among females. Since the majority of colorectal cancer case present following the prolonged transformation of adenomas into carcinomas, early detection and removal of colorectal adenomas are vital methods in its prevention. Considering the increasing incidence of colorectal cancer and polyps in Korea, it is very important to establish national guidelines for colorectal cancer screening and polyp detection. The proposed guidelines have been developed by the Korean Multi-Society Task Force using evidence-based methods. Systematic reviews and meta-analyses have been used to form the statements contained in the guidelines. This paper discusses the epidemiology of colorectal cancers and adenomas in Korea as well as optimal methods for screening of colorectal cancer and detection of adenomas including fecal occult blood tests, radiologic tests, and endoscopic examinations.

MeSH Terms

Adenoma
Advisory Committees
Colonoscopy
Colorectal Neoplasms
Early Detection of Cancer
Female
Humans
Incidence
Korea
Male
Mass Screening
Occult Blood
Polyps

Figure

• 

  Fig. 1 Study selection. Note.-CS = colonoscopy, CTC = CT colonography, DCBE = double contrast barium enema, FSG = flexible sigmoidoscopy, KISS = Korean Studies Information System, KMbase = Korean Medical database, RCT = randomized controlled trial

• 

  Fig. 2 Meta-analysis. Detection rate of FIT for advanced colorectal neoplasia according to the number of samples (1 test vs. 2 tests). Note.-CI = confidence interval, FIT = fecal immunochemical test

• 

  Fig. 3 Meta-analysis. Comparison between gFOBT and FIT in detection of colorectal cancer in average risk group. Note.-CI = confidence interval, FIT = fecal immunochemical test, gFOBT = guaiac-based fecal occult blood test

• 

  Fig. 4 Meta-analysis of CT colonography. Reported sensitivity and specificity in the included studies, by polyp size. A. Per-patient sensitivity for CT colonography. B. Per-patient specificity for CT colonography. C. Per-polyp sensitivity for CT colonography.

Reference

1. Jung KW, Park S, Kong HJ, Won YJ, Lee JY, Park EC, et al. Cancer statistics in Korea: incidence, mortality, survival, and prevalence in 2008. Cancer Res Treat. 2011; 43:1–11.

2. Shim JI, Kim Y, Han MA, Lee HY, Choi KS, Jun JK, et al. Results of colorectal cancer screening of the national cancer screening program in Korea, 2008. Cancer Res Treat. 2010; 42:191–198.

3. Winawer SJ, Zauber AG, O'Brien MJ, Ho MN, Gottlieb L, Sternberg SS, et al. The National Polyp Study Workgroup. Randomized comparison of surveillance intervals after colonoscopic removal of newly diagnosed adenomatous polyps. N Engl J Med. 1993; 328:901–906.

4. Levin B, Lieberman DA, McFarland B, Smith RA, Brooks D, Andrews KS, et al. 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; 58:130–160.

5. U.S. Preventive Services Task Force. Screening for colorectal cancer: US Preventive Services Task Force recommendation statement. Ann Intern Med. 2008; 149:627–637.

6. Whitlock EP, Lin JS, Liles E, Beil TL, Fu R. Screening for colorectal cancer: a targeted, updated systematic review for the US Preventive Services Task Force. Ann Intern Med. 2008; 149:638–658.

7. Atkins D, Best D, Briss PA, Eccles M, Falck-Ytter Y, Flottorp S, et al. Grading quality of evidence and strength of recommendations. BMJ. 2004; 328:1490.

8. Guyatt GH, Oxman AD, Vist GE, Kunz R, Falck-Ytter Y, Alonso-Coello P, et al. GRADE: an emerging consensus on rating quality of evidence and strength of recommendations. BMJ. 2008; 336:924–926.

9. Sung JJ, Lau JY, Goh KL, Leung WK. Asia Pacific Working Group on Colorectal Cancer. Increasing incidence of colorectal cancer in Asia: implications for screening. Lancet Oncol. 2005; 6:871–876.

10. Shin HR, Won YJ, Jung KW, Kong HJ, Yim SH, Lee JK, et al. Nationwide cancer incidence in Korea, 1999~2001; first result using the national cancer incidence database. Cancer Res Treat. 2005; 37:325–331.

11. Jung KW, Won YJ, Park S, Kong HJ, Sung J, Shin HR, et al. Cancer statistics in Korea: incidence, mortality and survival in 2005. J Korean Med Sci. 2009; 24:995–1003.

12. Jung KW, Park S, Kong HJ, Won YJ, Boo YK, Shin HR, et al. Cancer statistics in Korea: incidence, mortality and survival in 2006-2007. J Korean Med Sci. 2010; 25:1113–1121.

13. Choe JW, Chang HS, Yang SK, Myung SJ, Byeon JS, Lee D, et al. Screening colonoscopy in asymptomatic average-risk Koreans: analysis in relation to age and sex. J Gastroenterol Hepatol. 2007; 22:1003–1008.

14. Park HW, Byeon JS, Yang SK, Kim HS, Kim WH, Kim TI, et al. Colorectal Neoplasm in Asymptomatic Average-risk Koreans: The KASID Prospective Multicenter Colonoscopy Survey. Gut Liver. 2009; 3:35–40.

15. Lieberman DA, Weiss DG, Bond JH, Ahnen DJ, Garewal H, Chejfec G. Veterans Affairs Cooperative Study Group 380. Use of colonoscopy to screen asymptomatic adults for colorectal cancer. N Engl J Med. 2000; 343:162–168.

16. Betés M, Muñoz-Navas MA, Duque JM, Angós R, Macías E, Súbtil JC, et al. Use of colonoscopy as a primary screening test for colorectal cancer in average risk people. Am J Gastroenterol. 2003; 98:2648–2654.

17. Regula J, Rupinski M, Kraszewska E, Polkowski M, Pachlewski J, Orlowska J, et al. Colonoscopy in colorectal-cancer screening for detection of advanced neoplasia. N Engl J Med. 2006; 355:1863–1872.

18. Allison JE, Sakoda LC, Levin TR, Tucker JP, Tekawa IS, Cuff T, et al. Screening for colorectal neoplasms with new fecal occult blood tests: update on performance characteristics. J Natl Cancer Inst. 2007; 99:1462–1470.

19. Lieberman DA, Weiss DG. Veterans Affairs Cooperative Study Group 380. One-time screening for colorectal cancer with combined fecal occult-blood testing and examination of the distal colon. N Engl J Med. 2001; 345:555–560.

20. 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; 351:2704–2714.

21. Allison JE, Tekawa IS, Ransom LJ, Adrain AL. A comparison of fecal occult-blood tests for colorectal-cancer screening. N Engl J Med. 1996; 334:155–159.

22. Smith A, Young GP, Cole SR, Bampton P. Comparison of a brush-sampling fecal immunochemical test for hemoglobin with a sensitive guaiac-based fecal occult blood test in detection of colorectal neoplasia. Cancer. 2006; 107:2152–2159.

23. 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; 129:422–428.

24. Park DI, Ryu S, Kim YH, Lee SH, Lee CK, Eun CS, 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; 105:2017–2025.

25. Rozen P, Levi Z, Hazazi R, Waked A, Vilkin A, Maoz E, et al. Quantitative colonoscopic evaluation of relative efficiencies of an immunochemical faecal occult blood test and a sensitive guaiac test for detecting significant colorectal neoplasms. Aliment Pharmacol Ther. 2009; 29:450–457.

26. Rozen P, Comaneshter D, Levi Z, Hazazi R, Vilkin A, Maoz E, et al. Cumulative evaluation of a quantitative immunochemical fecal occult blood test to determine its optimal clinical use. Cancer. 2010; 116:2115–2125.

27. Grazzini G, Visioli CB, Zorzi M, Ciatto S, Banovich F, Bonanomi AG, et al. Immunochemical faecal occult blood test: number of samples and positivity cutoff. What is the best strategy for colorectal cancer screening? Br J Cancer. 2009; 100:259–265.

28. Hardcastle JD, Chamberlain JO, Robinson MH, Moss SM, Amar SS, Balfour TW, et al. Randomised controlled trial of faecal-occult-blood screening for colorectal cancer. Lancet. 1996; 348:1472–1477.

29. Kronborg O, Fenger C, Olsen J, Jørgensen OD, Søndergaard O. Randomised study of screening for colorectal cancer with faecal-occult-blood test. Lancet. 1996; 348:1467–1471.

30. Mandel JS, Church TR, Ederer F, Bond JH. Colorectal cancer mortality: effectiveness of biennial screening for fecal occult blood. J Natl Cancer Inst. 1999; 91:434–437.

31. Mandel JS, Church TR, Bond JH, Ederer F, Geisser MS, Mongin SJ, et al. The effect of fecal occult-blood screening on the incidence of colorectal cancer. N Engl J Med. 2000; 343:1603–1607.

32. Lee KJ, Inoue M, Otani T, Iwasaki M, Sasazuki S, Tsugane S. Japan Public Health Center-based Prospective Study. Colorectal cancer screening using fecal occult blood test and subsequent risk of colorectal cancer: a prospective cohort study in Japan. Cancer Detect Prev. 2007; 31:3–11.

33. Wong BC, Wong WM, Cheung KL, Tong TS, Rozen P, Young GP, et al. A sensitive guaiac faecal occult blood test is less useful than an immunochemical test for colorectal cancer screening in a Chinese population. Aliment Pharmacol Ther. 2003; 18:941–946.

34. Sung JJ, Lau JY, Young GP, Sano Y, Chiu HM, Byeon JS, et al. Asia Pacific consensus recommendations for colorectal cancer screening. Gut. 2008; 57:1166–1176.

35. Lieberman DA. Clinical practice. Screening for colorectal cancer. N Engl J Med. 2009; 361:1179–1187.

36. Zhu MM, Xu XT, Nie F, Tong JL, Xiao SD, Ran ZH. Comparison of immunochemical and guaiac-based fecal occult blood test in screening and surveillance for advanced colorectal neoplasms: a meta-analysis. J Dig Dis. 2010; 11:148–160.

37. Pickhardt PJ, Choi JR, Hwang I, Butler JA, Puckett ML, Hildebrandt HA, et al. Computed tomographic virtual colonoscopy to screen for colorectal neoplasia in asymptomatic adults. N Engl J Med. 2003; 349:2191–2200.

38. Mulhall BP, Veerappan GR, Jackson JL. Meta-analysis: computed tomographic colonography. Ann Intern Med. 2005; 142:635–650.

39. Chaparro M, Gisbert JP, Del Campo L, Cantero J, Maté J. Accuracy of computed tomographic colonography for the detection of polyps and colorectal tumors: a systematic review and meta-analysis. Digestion. 2009; 80:1–17.

40. Johnson CD, Chen MH, Toledano AY, Heiken JP, Dachman A, Kuo MD, et al. Accuracy of CT colonography for detection of large adenomas and cancers. N Engl J Med. 2008; 359:1207–1217.

41. Macari M, Milano A, Lavelle M, Berman P, Megibow AJ. Comparison of time-efficient CT colonography with two- and three-dimensional colonic evaluation for detecting colorectal polyps. AJR Am J Roentgenol. 2000; 174:1543–1549.

42. Macari M, Bini EJ, Jacobs SL, Naik S, Lui YW, Milano A, et al. Colorectal polyps and cancers in asymptomatic average-risk patients: evaluation with CT colonography. Radiology. 2004; 230:629–636.

43. Kim YS, Kim N, Kim SH, Park MJ, Lim SH, Yim JY, et al. The efficacy of intravenous contrast-enhanced 16-raw multi-detector CT colonography for detecting patients with colorectal polyps in an asymptomatic population in Korea. J Clin Gastroenterol. 2008; 42:791–798.

44. Kim DH, Pickhardt PJ, Taylor AJ, Leung WK, Winter TC, Hinshaw JL, et al. CT colonography versus colonoscopy for the detection of advanced neoplasia. N Engl J Med. 2007; 357:1403–1412.

45. Johnson CD, Fletcher JG, MacCarty RL, Mandrekar JN, Harmsen WS, Limburg PJ, 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; 189:672–680.

46. An S, Lee KH, Kim YH, Park SH, Kim HY, Kim SH, 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:W100–W106.

47. Graser A, Stieber P, Nagel D, Schäfer C, Horst D, Becker CR, 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; 58:241–248.

48. Cotton PB, Durkalski VL, Pineau BC, Palesch YY, Mauldin PD, Hoffman B, et al. Computed tomographic colonography (virtual colonoscopy): a multicenter comparison with standard colonoscopy for detection of colorectal neoplasia. JAMA. 2004; 291:1713–1719.

49. Rockey DC, Paulson E, Niedzwiecki D, Davis W, Bosworth HB, Sanders L, et al. Analysis of air contrast barium enema, computed tomographic colonography, and colonoscopy: prospective comparison. Lancet. 2005; 365:305–311.

50. McFarland EG, Fletcher JG, Pickhardt P, Dachman A, Yee J, McCollough CH, et al. ACR Colon Cancer Committee white paper: status of CT colonography 2009. J Am Coll Radiol. 2009; 6:756–772.e4.

51. Benson M, Dureja P, Gopal D, Reichelderfer M, Pfau PR. A comparison of optical colonoscopy and CT colonography screening strategies in the detection and recovery of subcentimeter adenomas. Am J Gastroenterol. 2010; 105:2578–2585.

52. Edwards JT, Mendelson RM, Fritschi L, Foster NM, Wood C, Murray D, et al. Colorectal neoplasia screening with CT colonography in average-risk asymptomatic subjects: community-based study. Radiology. 2004; 230:459–464.

53. Pickhardt PJ. Incidence of colonic perforation at CT colonography: review of existing data and implications for screening of asymptomatic adults. Radiology. 2006; 239:313–316.

54. Sosna J, Blachar A, Amitai M, Barmeir E, Peled N, Goldberg SN, et al. Colonic perforation at CT colonography: assessment of risk in a multicenter large cohort. Radiology. 2006; 239:457–463.

55. Shinners TJ, Pickhardt PJ, Taylor AJ, Jones DA, Olsen CH. Patient-controlled room air insufflation versus automated carbon dioxide delivery for CT colonography. AJR Am J Roentgenol. 2006; 186:1491–1496.

56. Kimberly JR, Phillips KC, Santago P, Perumpillichira J, Bechtold R, Pineau B, et al. Extracolonic findings at virtual colonoscopy: an important consideration in asymptomatic colorectal cancer screening. J Gen Intern Med. 2009; 24:69–73.

57. Pickhardt PJ, Hanson ME, Vanness DJ, Lo JY, Kim DH, Taylor AJ, et al. Unsuspected extracolonic findings at screening CT colonography: clinical and economic impact. Radiology. 2008; 249:151–159.

58. Gluecker TM, Johnson CD, Wilson LA, Maccarty RL, Welch TJ, Vanness DJ, et al. Extracolonic findings at CT colonography: evaluation of prevalence and cost in a screening population. Gastroenterology. 2003; 124:911–916.

59. Hara AK, Johnson CD, MacCarty RL, Welch TJ. Incidental extracolonic findings at CT colonography. Radiology. 2000; 215:353–357.

60. Ginnerup Pedersen B, Rosenkilde M, Christiansen TE, Laurberg S. Extracolonic findings at computed tomography colonography are a challenge. Gut. 2003; 52:1744–1747.

61. 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; 100:2771–2776.

62. Flicker MS, Tsoukas AT, Hazra A, Dachman AH. Economic impact of extracolonic findings at computed tomographic colonography. J Comput Assist Tomogr. 2008; 32:497–503.

63. 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; 195:677–686.

64. Radiation Risk in Perspective. Position Statement of the Health Physics Society. McLean, VA: Health Physics Society;2004.

65. Brenner DJ, Georgsson MA. Mass screening with CT colonography: should the radiation exposure be of concern? Gastroenterology. 2005; 129:328–337.

66. Macari M, Bini EJ, Xue X, Milano A, Katz SS, Resnick D, et al. Colorectal neoplasms: prospective comparison of thin-section low-dose multi-detector row CT colonography and conventional colonoscopy for detection. Radiology. 2002; 224:383–392.

67. Zalis ME, Barish MA, Choi JR, Dachman AH, Fenlon HM, Ferrucci JT, et al. CT colonography reporting and data system: a consensus proposal. Radiology. 2005; 236:3–9.

68. Pickhardt PJ, Kim DH. Colorectal cancer screening with CT colonography: key concepts regarding polyp prevalence, size, histology, morphology, and natural history. AJR Am J Roentgenol. 2009; 193:40–46.

69. Welin S, Youker J, Spratt JS Jr. The rates and patterns of growth of 375 tumors of the large intestine and rectum observed serially by double contrast enema study (malmoe technique). Am J Roentgenol Radium Ther Nucl Med. 1963; 90:673–687.

70. Hofstad B, Vatn MH, Andersen SN, Huitfeldt HS, Rognum T, Larsen S, et al. Growth of colorectal polyps: redetection and evaluation of unresected polyps for a period of three years. Gut. 1996; 39:449–456.

71. Knoernschild HE. Growth rate and malignant potential of colonic polyps: early results. Surg Forum. 1963; 14:137–138.

72. Stryker SJ, Wolff BG, Culp CE, Libbe SD, Ilstrup DM, MacCarty RL. Natural history of untreated colonic polyps. Gastroenterology. 1987; 93:1009–1013.

73. Smith RA, Cokkinides V, Eyre HJ. American Cancer Society. American Cancer Society guidelines for the early detection of cancer, 2003. CA Cancer J Clin. 2003; 53:27–43.

74. Rex DK, Lieberman D. ACG. ACG colorectal cancer prevention action plan: update on CT-colonography. Am J Gastroenterol. 2006; 101:1410–1413.

75. Rockey DC, Barish M, Brill JV, Cash BD, Fletcher JG, Sharma P, et al. Standards for gastroenterologists for performing and interpreting diagnostic computed tomographic colonography. Gastroenterology. 2007; 133:1005–1024.

76. Lieberman D, Moravec M, Holub J, Michaels L, Eisen G. Polyp size and advanced histology in patients undergoing colonoscopy screening: implications for CT colonography. Gastroenterology. 2008; 135:1100–1105.

77. Gillespie JS, Kelly BE. Double contrast barium enema and colorectal carcinoma: sensitivity and potential role in screening. Ulster Med J. 2001; 70:15–18.

78. Thomas RD, Fairhurst JJ, Frost RA. Wessex regional radiology audit: barium enema in colo-rectal carcinoma. Clin Radiol. 1995; 50:647–650.

79. Johnson CD, Carlson HC, Taylor WF, Weiland LP. Barium enemas of carcinoma of the colon: sensitivity of double- and single-contrast studies. AJR Am J Roentgenol. 1983; 140:1143–1149.

80. Kelvin FM, Gardiner R, Vas W, Stevenson GW. Colorectal carcinoma missed on double contrast barium enema study: a problem in perception. AJR Am J Roentgenol. 1981; 137:307–313.

81. Thorpe CD, Grayson DJ Jr, Wingfield PB. Detection of carcinoma of the colon and rectum by air contrast enema. Surg Gynecol Obstet. 1981; 152:307–309.

82. Fork FT, Lindström C, Ekelund G. Double contrast examination in carcinoma of the colon and rectum. A prospective clinical series. Acta Radiol Diagn (Stockh). 1983; 24:177–188.

83. Reiertsen O, Bakka A, Trønnes S, Gauperaa T. Routine double contrast barium enema and fiberoptic colonoscopy in the diagnosis of colorectal carcinoma. Acta Chir Scand. 1988; 154:53–55.

84. Rex DK, Rahmani EY, Haseman JH, Lemmel GT, Kaster S, Buckley JS. Relative sensitivity of colonoscopy and barium enema for detection of colorectal cancer in clinical practice. Gastroenterology. 1997; 112:17–23.

85. Strøm E, Larsen JL. Colon cancer at barium enema examination and colonoscopy: a study from the county of Hordaland, Norway. Radiology. 1999; 211:211–214.

86. McDonald S, Lyall P, Israel L, Coates R, Frizelle F. Why barium enemas fail to identify colorectal cancers. ANZ J Surg. 2001; 71:631–633.

87. Connolly DJ, Traill ZC, Reid HS, Copley SJ, Nolan DJ. The double contrast barium enema: a retrospective single centre audit of the detection of colorectal carcinomas. Clin Radiol. 2002; 57:29–32.

88. Leslie A, Virjee JP. Detection of colorectal carcinoma on double contrast barium enema when double reporting is routinely performed: an audit of current practice. Clin Radiol. 2002; 57:184–187.

89. Tawn DJ, Squire CJ, Mohammed MA, Adam EJ. National audit of the sensitivity of double-contrast barium enema for colorectal carcinoma, using control charts For the Royal College of Radiologists Clinical Radiology Audit Sub-Committee. Clin Radiol. 2005; 60:558–564.

90. Toma J, Paszat LF, Gunraj N, Rabeneck L. Rates of new or missed colorectal cancer after barium enema and their risk factors: a population-based study. Am J Gastroenterol. 2008; 103:3142–3148.

91. Williams CB, Macrae FA, Bartram CI. A prospective study of diagnostic methods in adenoma follow-up. Endoscopy. 1982; 14:74–78.

92. Winawer SJ, Stewart ET, Zauber AG, Bond JH, Ansel H, Waye JD, et al. National Polyp Study Work Group. A comparison of colonoscopy and double-contrast barium enema for surveillance after polypectomy. N Engl J Med. 2000; 342:1766–1772.

93. Glick SN. Comparison of colonoscopy and double-contrast barium enema. N Engl J Med. 2000; 343:1728. author reply 1729-1730.

94. Kewenter J, Brevinge H. Endoscopic and surgical complications of work-up in screening for colorectal cancer. Dis Colon Rectum. 1996; 39:676–680.

95. Blakeborough A, Sheridan MB, Chapman AH. Complications of barium enema examinations: a survey of UK Consultant Radiologists 1992 to 1994. Clin Radiol. 1997; 52:142–148.

96. Winawer SJ, Fletcher RH, Miller L, Godlee F, Stolar MH, Mulrow CD, et al. Colorectal cancer screening: clinical guidelines and rationale. Gastroenterology. 1997; 112:594–642.

97. U.S. Preventive Services Task Force. Screening for colorectal cancer: recommendation and rationale. Ann Intern Med. 2002; 137:129–131.

98. Levin TR, Zhao W, Conell C, Seeff LC, Manninen DL, Shapiro JA, et al. Complications of colonoscopy in an integrated health care delivery system. Ann Intern Med. 2006; 145:880–886.

99. Rex DK, Cutler CS, Lemmel GT, Rahmani EY, Clark DW, Helper DJ, et al. Colonoscopic miss rates of adenomas determined by back-to-back colonoscopies. Gastroenterology. 1997; 112:24–28.

100. Pickhardt PJ, Nugent PA, Mysliwiec PA, Choi JR, Schindler WR. Location of adenomas missed by optical colonoscopy. Ann Intern Med. 2004; 141:352–359.

101. Bressler B, Paszat LF, Vinden C, Li C, He J, Rabeneck L. Colonoscopic miss rates for right-sided colon cancer: a population-based analysis. Gastroenterology. 2004; 127:452–456.

102. Choi KY, Lee BI, Lee SY, Lee WC, Bae SS, Kim BW, et al. Colonoscopic miss-rate of colorectal polyp and adenoma. Korean J Gastrointest Endosc. 2003; 26:199–204.

103. Rex DK, Petrini JL, Baron TH, Chak A, Cohen J, Deal SE, et al. Quality indicators for colonoscopy. Gastrointest Endosc. 2006; 63:S16–S28.

104. Chung IK. Process assessment for quality control of upper and lower endoscopy. Korean J Gastrointest Endosc. 2010; 41:Suppl 2. 230–234.

105. Barclay RL, Vicari JJ, Doughty AS, Johanson JF, Greenlaw RL. Colonoscopic withdrawal times and adenoma detection during screening colonoscopy. N Engl J Med. 2006; 355:2533–2541.

106. Simmons DT, Harewood GC, Baron TH, Petersen BT, Wang KK, Boyd-Enders F, et al. Impact of endoscopist withdrawal speed on polyp yield: implications for optimal colonoscopy withdrawal time. Aliment Pharmacol Ther. 2006; 24:965–971.

107. Ahn SB, Han DS, Kim SM, Cho HS, Byun TJ, Kim TY, et al. The colonoscopic withdrawal time is correlated with the rate of detecting polyps when performing colonoscopy. Korean J Gastrointest Endosc. 2009; 38:75–79.

108. Kaminski MF, Regula J, Kraszewska E, Polkowski M, Wojciechowska U, Didkowska J, et al. Quality indicators for colonoscopy and the risk of interval cancer. N Engl J Med. 2010; 362:1795–1803.

109. Rabeneck L, Paszat LF, Saskin R, Stukel TA. Association between colonoscopy rates and colorectal cancer mortality. Am J Gastroenterol. 2010; 105:1627–1632.

110. Kahi CJ, Imperiale TF, Juliar BE, Rex DK. Effect of screening colonoscopy on colorectal cancer incidence and mortality. Clin Gastroenterol Hepatol. 2009; 7:770–775. quiz 711

111. Arain MA, Sawhney M, Sheikh S, Anway R, Thyagarajan B, Bond JH, et al. CIMP status of interval colon cancers: another piece to the puzzle. Am J Gastroenterol. 2010; 105:1189–1195.

112. Bianco MA, Cipolletta L, Rotondano G, Buffoli F, Gizzi G, Tessari F. Flat Lesions Italian Network (FLIN). Prevalence of nonpolypoid colorectal neoplasia: an Italian multicenter observational study. Endoscopy. 2010; 42:279–285.

113. Newcomb PA, Storer BE, Morimoto LM, Templeton A, Potter JD. Long-term efficacy of sigmoidoscopy in the reduction of colorectal cancer incidence. J Natl Cancer Inst. 2003; 95:622–625.

114. Selby JV, Friedman GD, Quesenberry CP Jr, Weiss NS. A case-control study of screening sigmoidoscopy and mortality from colorectal cancer. N Engl J Med. 1992; 326:653–657.

115. Brenner H, Haug U, Arndt V, Stegmaier C, Altenhofen L, Hoffmeister M. Low risk of colorectal cancer and advanced adenomas more than 10 years after negative colonoscopy. Gastroenterology. 2010; 138:870–876.

116. Imperiale TF, Glowinski EA, Lin-Cooper C, Larkin GN, Rogge JD, Ransohoff DF. Five-year risk of colorectal neoplasia after negative screening colonoscopy. N Engl J Med. 2008; 359:1218–1224.

117. Lakoff J, Paszat LF, Saskin R, Rabeneck L. Risk of developing proximal versus distal colorectal cancer after a negative colonoscopy: a population-based study. Clin Gastroenterol Hepatol. 2008; 6:1117–1121. quiz 1064

118. Leung WK, Lau JY, Suen BY, Wong GL, Chow DK, Lai LH, et al. Repeat-screening colonoscopy 5 years after normal baseline-screening colonoscopy in average-risk Chinese: a prospective study. Am J Gastroenterol. 2009; 104:2028–2034.

119. Singh H, Turner D, Xue L, Targownik LE, Bernstein CN. Risk of developing colorectal cancer following a negative colonoscopy examination: evidence for a 10-year interval between colonoscopies. JAMA. 2006; 295:2366–2373.

120. Rex DK, Cummings OW, Helper DJ, Nowak TV, McGill JM, Chiao GZ, et al. 5-year incidence of adenomas after negative colonoscopy in asymptomatic average-risk persons [see comment]. Gastroenterology. 1996; 111:1178–1181.

121. Singh H, Nugent Z, Mahmud SM, Demers AA, Bernstein CN. Predictors of colorectal cancer after negative colonoscopy: a population-based study. Am J Gastroenterol. 2010; 105:663–673. quiz 674

122. Baxter NN, Sutradhar R, Forbes SS, Paszat LF, Saskin R, Rabeneck L. Analysis of administrative data finds endoscopist quality measures associated with postcolonoscopy colorectal cancer. Gastroenterology. 2011; 140:65–72.

123. Ben-Horin S, Bar-Meir S, Avidan B. The impact of colon cleanliness assessment on endoscopists' recommendations for follow-up colonoscopy. Am J Gastroenterol. 2007; 102:2680–2685.

124. Lebwohl B, Kastrinos F, Glick M, Rosenbaum AJ, Wang T, Neugut AI. The impact of suboptimal bowel preparation on adenoma miss rates and the factors associated with early repeat colonoscopy. Gastrointest Endosc. 2011; 73:1207–1214.

125. Levin B, Lieberman DA, McFarland B, Andrews KS, Brooks D, Bond J, et al. 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. Gastroenterology. 2008; 134:1570–1595.

126. Atkin WS, Edwards R, Kralj-Hans I, Wooldrage K, Hart AR, Northover JM, et al. Once-only flexible sigmoidoscopy screening in prevention of colorectal cancer: a multicentre randomised controlled trial. Lancet. 2010; 375:1624–1633.

127. 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.

128. Bini EJ, Unger JS, Rieber JM, Rosenberg J, Trujillo K, Weinshel EH. Prospective, randomized, single-blind comparison of two preparations for screening flexible sigmoidoscopy. Gastrointest Endosc. 2000; 52:218–222.

129. Sharma VK, Chockalingham S, Clark V, Kapur A, Steinberg EN, Heinzelmann EJ, et al. Randomized, controlled comparison of two forms of preparation for screening flexible sigmoidoscopy. Am J Gastroenterol. 1997; 92:809–811.

130. Underwood D, Makar RR, Gidwani AL, Najfi SM, Neilly P, Gilliland R. A prospective randomized single blind trial of Fleet phosphate enema versus glycerin suppositories as preparation for flexible sigmoidoscopy. Ir J Med Sci. 2010; 179:113–118.

131. Atkin WS, Hart A, Edwards R, Cook CF, Wardle J, McIntyre P, et al. Single blind, randomised trial of efficacy and acceptability of oral picolax versus self administered phosphate enema in bowel preparation for flexible sigmoidoscopy screening. BMJ. 2000; 320:1504–1508. discussion 1509

132. Osgard E, Jackson JL, Strong J. A randomized trial comparing three methods of bowel preparation for flexible sigmoidoscopy. Am J Gastroenterol. 1998; 93:1126–1130.

133. Levin TR, Farraye FA, Schoen RE, Hoff G, Atkin W, Bond JH, et al. Quality in the technical performance of screening flexible sigmoidoscopy: recommendations of an international multi-society task group. Gut. 2005; 54:807–813.

134. Lewis JD, Ng K, Hung KE, Bilker WB, Berlin JA, Brensinger C, et al. Detection of proximal adenomatous polyps with screening sigmoidoscopy: a systematic review and meta-analysis of screening colonoscopy. Arch Intern Med. 2003; 163:413–420.

135. Schoen RE, Weissfeld JL, Pinsky PF, Riley T. Yield of advanced adenoma and cancer based on polyp size detected at screening flexible sigmoidoscopy. Gastroenterology. 2006; 131:1683–1689.

136. Doria-Rose VP, Levin TR, Selby JV, Newcomb PA, Richert-Boe KE, Weiss NS. The incidence of colorectal cancer following a negative screening sigmoidoscopy: implications for screening interval. Gastroenterology. 2004; 127:714–722.

137. Burke CA, Elder K, Lopez R. Screening for colorectal cancer with flexible sigmoidoscopy: is a 5-yr interval appropriate? A comparison of the detection of neoplasia 3 yr versus 5 yr after a normal examination. Am J Gastroenterol. 2006; 101:1329–1332.

138. Rex DK, Johnson DA, Anderson JC, Schoenfeld PS, Burke CA, Inadomi JM. American College of Gastroenterology. American College of Gastroenterology guidelines for colorectal cancer screening 2009 [corrected]. Am J Gastroenterol. 2009; 104:739–750.

139. Baxter NN, Goldwasser MA, Paszat LF, Saskin R, Urbach DR, Rabeneck L. Association of colonoscopy and death from colorectal cancer. Ann Intern Med. 2009; 150:1–8.

140. Brenner H, Hoffmeister M, Arndt V, Stegmaier C, Altenhofen L, Haug U. Protection from right- and left-sided colorectal neoplasms after colonoscopy: population-based study. J Natl Cancer Inst. 2010; 102:89–95.