Screening colonoscopy and flexible sigmoidoscopy for reduction of colorectal cancer incidence: A case-control study

Autoři: Cynthia W. Ko aff001;  V. Paul Doria-Rose aff002;  Michael J. Barrett aff003;  Aruna Kamineni aff004;  Lindsey Enewold aff002;  Noel S. Weiss aff005
Působiště autorů: Division of Gastroenterology, Department of Medicine, University of Washington School of Medicine, Seattle, Washington, United States of America aff001;  National Cancer Institute, National Institutes of Health, Bethesda, Maryland, United States of America aff002;  Information Management Services, Inc., Calverton, Maryland, United States of America aff003;  Kaiser Permanente Washington Health Research Institute, Seattle, Washington, United States of America aff004;  Department of Epidemiology, University of Washington, Seattle, Washington, United states of America aff005
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0226027



Flexible sigmoidoscopy and colonoscopy are both recommended colorectal cancer screening options, but their relative effectiveness needs clarification. The aim of this study was to compare the effectiveness of colonoscopy and flexible sigmoidoscopy for reduction of colorectal cancer incidence.


We conducted a case-control study within the linked Surveillance, Epidemiology, and End Results (SEER)-Medicare database. Cases were subjects age 70–85 years in the SEER-Medicare database diagnosed with CRC during 2004–2013. Up to 3 controls were matched to each case by birth year, sex, race, and SEER region. Receipt of screening colonoscopy or flexible sigmoidoscopy was ascertained from Medicare claims. Conditional logistic regression models were developed to estimate the odds ratios (ORs) and 95% confidence intervals (CI) for a history of screening in cases vs. controls. We conducted secondary analyses by sex, race, endoscopist characteristics, and with varying timing and duration of the look-back period.


Receipt of screening colonoscopy and sigmoidoscopy was associated with a 59% (OR 0.41, 95%CI 0.39, 0.43) and 22% reduction (OR 0.78, 95%CI 0.67, 0.92) in colorectal cancer incidence, respectively. Colonoscopy was associated with greater reduction in the distal colorectal cancer incidence (OR 0.22, 95%CI 0.20, 0.24) than proximal colorectal cancer incidence (OR 0.62, 95%CI 0.59, 0.66). Sigmoidoscopy was associated with a 52% reduction in distal colorectal cancer incidence (OR 0.48, 95%CI 0.37, 0.63), but with no reduction in proximal colorectal cancer incidence. These associations were stronger in men than in women. No differences by race or endoscopist characteristics were observed.


Both screening colonoscopy and sigmoidoscopy were associated with reductions in overall colorectal cancer incidence, with a greater magnitude of reduction observed with colonoscopy.

Klíčová slova:

Cancer detection and diagnosis – Cancer screening – Colon – Colorectal cancer – Disease surveillance – Endoscopy – Medicare – colonoscopy


1. Wolf AMD, Fontham ETH, Church TR, Flowers CR, Guerra CE, LaMonte SJ, et al. Colorectal cancer screening for average-risk adults: 2018 guideline update from the American Cancer Society. CA Cancer J Clin. 2018;68:250–81. doi: 10.3322/caac.21457 29846947

2. Bibbins-Domingo K, Grossman DC, Curry SJ, Davidson KW, Epling JW Jr., Garcia FA, et al. Screening for Colorectal Cancer: US Preventive Services Task Force Recommendation Statement. JAMA. 2016;315:2564–75. doi: 10.1001/jama.2016.5989 27304597

3. Rex DK, Boland CR, Dominitz JA, Giardiello FM, Johnson DA, Kaltenbach T, et al. Colorectal Cancer Screening: Recommendations for Physicians and Patients from the U.S. Multi-Society Task Force on Colorectal Cancer. Am J Gastroenterol. 2017;112:1016–30. doi: 10.1038/ajg.2017.174 28555630

4. Hardcastle JD, Chamberlain J, Sheffield J, Balfour TW, Armitage NC, Thomas WM, et al. Randomised, controlled trial of faecal occult blood screening for colorectal cancer: results for first 107,349 subjects. Lancet. 1989;1(8648):1160–4. doi: 10.1016/s0140-6736(89)92750-5 2566735

5. Hardcastle JD, Chamberlain JO, Robinson MHE, Moss SM, Amar SS, Balfour TW, et al. Randomised controlled trial of faecal-occult-blood screening for colorectal cancer. Lancet. 1996;348:1472–7. doi: 10.1016/S0140-6736(96)03386-7 8942775

6. Mandel JS, Bond JH, Church TR, Snover DC, Bradley GM, Schuman LM, et al. Reducing mortality from colorectal cancer by screening for fecal occult blood. N Engl J Med. 1993;328:1365–71. doi: 10.1056/NEJM199305133281901 8474513

7. 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;343:1603–7. doi: 10.1056/NEJM200011303432203 11096167

8. Kronborg O, Fenger C, Olsen J, Jorgensen OD, Sondergaard O. Randomised study of screening for colorectal cancer with faecal-occult-blood test. Lancet. 1996;348:1467–71. doi: 10.1016/S0140-6736(96)03430-7 8942774

9. 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;375:1624–33. doi: 10.1016/S0140-6736(10)60551-X 20430429

10. Schoen RE, Pinsky PF, Weissfeld JL, Yokochi LA, Church T, Laiyemo AO, et al. Colorectal-cancer incidence and mortality with screening flexible sigmoidoscopy. N Engl J Med. 2012;366:2345–57. doi: 10.1056/NEJMoa1114635 22612596

11. Segnan N, Armaroli P, Bonelli L, Risio M, Sciallero S, Zappa M, et al. Once-Only Sigmoidoscopy in Colorectal Cancer Screening: Follow-up Findings of the Italian Randomized Controlled Trial—SCORE. J Natl Cancer Inst. 2011;103:1310–22. doi: 10.1093/jnci/djr284 21852264

12. Holme O, Loberg M, Kalager M, Bretthauer M, Hernan MA, Aas E, et al. Effect of flexible sigmoidoscopy screening on colorectal cancer incidence and mortality: a randomized clinical trial. JAMA. 2014;312:606–15. doi: 10.1001/jama.2014.8266 25117129

13. Doubeni CA, Corley DA, Quinn VP, Jensen CD, Zauber AG, Goodman M, et al. Effectiveness of screening colonoscopy in reducing the risk of death from right and left colon cancer: a large community-based study. Gut. 2018;67:291–8. doi: 10.1136/gutjnl-2016-312712 27733426

14. Doubeni CA, Weinmann S, Adams K, Kamineni A, Buist DS, Ash AS, et al. Screening colonoscopy and risk for incident late-stage colorectal cancer diagnosis in average-risk adults: a nested case-control study. Ann Intern Med. 2013;158:312–20. doi: 10.7326/0003-4819-158-5-201303050-00003 23460054

15. 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. doi: 10.7326/0003-4819-150-1-200901060-00306 19075198

16. Baxter NN, Warren JL, Barrett MJ, Stukel TA, Doria-Rose VP. Association Between Colonoscopy and Colorectal Cancer Mortality in a US Cohort According to Site of Cancer and Colonoscopist Specialty. J Clin Oncol. 2012;30:2664–9. doi: 10.1200/JCO.2011.40.4772 22689809

17. Brenner H, Chang-Claude J, Seiler CM, Rickert A, Hoffmeister M. Protection from colorectal cancer after colonoscopy: a population-based, case-control study. Ann Intern Med. 2011;154:22–30. doi: 10.7326/0003-4819-154-1-201101040-00004 21200035

18. Nishihara R, Wu K, Lochhead P, Morikawa T, Liao X, Qian ZR, et al. Long-term colorectal-cancer incidence and mortality after lower endoscopy. N Engl J Med. 2013;369:1095–105. doi: 10.1056/NEJMoa1301969 24047059

19. Quintero E, Castells A, Bujanda L, Cubiella J, Salas D, Lanas A, et al. Colonoscopy versus fecal immunochemical testing in colorectal-cancer screening. N Engl J Med. 2012;366:697–706. doi: 10.1056/NEJMoa1108895 22356323

20. Bretthauer M, Kaminski MF, Loberg M, Zauber AG, Regula J, Kuipers EJ, et al. Population-Based Colonoscopy Screening for Colorectal Cancer: A Randomized Clinical Trial. JAMA Intern Med. 2016;176:894–902. doi: 10.1001/jamainternmed.2016.0960 27214731

21. Kaminski MF, Bretthauer M, Zauber AG, Kuipers EJ, Adami HO, van Ballegooijen M, et al. The NordICC Study: rationale and design of a randomized trial on colonoscopy screening for colorectal cancer. Endoscopy. 2012;44:695–702. doi: 10.1055/s-0032-1306895 22723185

22. Dominitz JA, Robertson DJ, Ahnen DJ, Allison JE, Antonelli M, Boardman KD, et al. Colonoscopy vs. Fecal Immunochemical Test in Reducing Mortality From Colorectal Cancer (CONFIRM): Rationale for Study Design. Am J Gastroenterol. 2017;112:1736–46. doi: 10.1038/ajg.2017.286 29016565

23. Colon cancer screening in average-risk population: immunochemical fecal occult blood testing versus colonoscopy 2018. Available from: Accessed June 1, 2018.

24. Winawer S, Fletcher R, Rex D, Bond J, Burt R, Ferrucci J, et al. Colorectal cancer screening and surveillance: Clinical guidelines and rationale-Update based on new evidence. Gastroenterology. 2003;124:544–60. doi: 10.1053/gast.2003.50044 12557158

25. Lieberman DA, Weiss DG, Bond JH, Ahnen DJ, Garewal H, Chejfec G. Use of colonoscopy to screen asymptomatic adults for colorectal cancer. Veterans Affairs Cooperative Study Group 380. N Engl J Med. 2000;343:162–8. doi: 10.1056/NEJM200007203430301 10900274

26. Imperiale TF, Wagner DR, Lin CY, Larkin GN, Rogge JD, Ransohoff DF. Risk of advanced proximal neoplasms in asymptomatic adults according to the distal colorectal findings. N Engl J Med. 2000;343:169–74. doi: 10.1056/NEJM200007203430302 10900275

27. Schoenfeld P, Cash B, Flood A, Dobhan R, Eastone J, Coyle W, et al. Colonoscopic screening of average-risk women for colorectal neoplasia. N Engl J Med. 2005;352:2061–8. doi: 10.1056/NEJMoa042990 15901859

28. Levin TR, Conell C, Shapiro JA, Chazan SG, Nadel MR, Selby JV. Complications of screening flexible sigmoidoscopy. Gastroenterology. 2002;123:1786–92. doi: 10.1053/gast.2002.37064 12454834

29. Duthie GS, Drew PJ, Hughes MA, Farouk R, Hodson R, Wedgwood KR, et al. A UK training programme for nurse practitioner flexible sigmoidoscopy and a prospective evaluation of the practice of the first UK trained nurse flexible sigmoidoscopist. Gut. 1998;43:711–4. doi: 10.1136/gut.43.5.711 9824356

30. Schoenfeld P, Lipscomb S, Crook J, Dominguez J, Butler J, Holmes L, et al. Accuracy of polyp detection by gastroenterologists and nurse endoscopists during flexible sigmoidoscopy: a randomized trial. Gastroenterology. 1999;117:312–8. doi: 10.1053/gast.1999.0029900312 10419911

31. Holme O, Loberg M, Kalager M, Bretthauer M, Hernan MA, Aas E, et al. Long-Term Effectiveness of Sigmoidoscopy Screening on Colorectal Cancer Incidence and Mortality in Women and Men: A Randomized Trial. Ann Intern Med. 2018;168:775–82. doi: 10.7326/M17-1441 29710125

32. Atkin W, Wooldrage K, Parkin DM, Kralj-Hans I, MacRae E, Shah U, et al. Long term effects of once-only flexible sigmoidoscopy screening after 17 years of follow-up: the UK Flexible Sigmoidoscopy Screening randomised controlled trial. Lancet. 2017;389:1299–311. doi: 10.1016/S0140-6736(17)30396-3 28236467

33. 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. doi: 10.1093/jnci/djp436 20042716

34. Singh H, Nugent Z, Demers AA, Kliewer EV, Mahmud SM, Bernstein CN. The reduction in colorectal cancer mortality after colonoscopy varies by site of the cancer. Gastroenterology. 2010;139:1128–37. doi: 10.1053/j.gastro.2010.06.052 20600026

35. Weiss NS, Doria-Rose VP. The effectiveness of colonoscopy in reducing mortality from colorectal cancer. Ann Intern Med. 2009;150:817–8.

36. Weiss NS, Doria-Rose VP. Colorectal cancer risk following a negative colonoscopy. Jama. 2006;296:2436–7; author reply 7–8. doi: 10.1001/jama.296.20.2436-b 17119135

37. Inadomi JM. Why you should care about screening flexible sigmoidoscopy. N Engl J Med. 2012;366:2421–2. doi: 10.1056/NEJMe1204099 22612597

38. Neugut AI, Lebwohl B. Colonoscopy vs sigmoidoscopy screening: getting it right. JAMA. 2010;304:461–2. doi: 10.1001/jama.2010.1001 20664047

39. Brett AS. Flexible sigmoidoscopy for colorectal cancer screening: more evidence, persistent ironies. JAMA. 2014;312:601–2. doi: 10.1001/jama.2014.8613 25117127

40. SEER Program Overview. Available from: Accessed June 1, 2018.

41. Ko CW, Dominitz JA, Neradilek M, Polissar N, Green P, Kreuter W, et al. Determination of Colonoscopy Indication From Administrative Claims Data. Med Care. 2014;52:e21–9. doi: 10.1097/MLR.0b013e31824ebdf5 22437619

42. Medicare Claims Processing Manual. Available from: Accessed June 1, 2018.

43. SEER-Medicare: Summary Table of Available Medicare Data for Cancer & Non-cancer Cases 2017. Available from: Accessed June 1, 2018.

44. Weiss NS. Case-control studies of the efficacy of screening tests designed to prevent the incidence of cancer. Am J Epidemiol. 1999;149:1–4. doi: 10.1093/oxfordjournals.aje.a009721 9883787

45. Kuntz KM, Lansdorp-Vogelaar I, Rutter CM, Knudsen AB, van Ballegooijen M, Savarino JE, et al. A systematic comparison of microsimulation models of colorectal cancer: the role of assumptions about adenoma progression. Med Decis Making. 2011;31:530–9. doi: 10.1177/0272989X11408730 21673186

46. Hofstad B, Vatn M, Larsen S, Osnes M. Growth of colorectal polyps: recovery and evaluation of unresected polyps of less than 10 mm, 1 year after detection. Scand J Gastroenterol. 1994;29:640–5. doi: 10.3109/00365529409092485 7939401

47. 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;39:449–56. doi: 10.1136/gut.39.3.449 8949653

48. Stryker SJ, Wolff BG, Culp CE, Libbe SD, Ilstrup DM, MacCarty RL. Natural history of untreated colonic polyps. Gastroenterology. 1987;93:1009–13. doi: 10.1016/0016-5085(87)90563-4 3653628

49. Brenner H, Hoffmeister M, Stegmaier C, Brenner G, Altenhofen L, Haug U. Risk of progression of advanced adenomas to colorectal cancer by age and sex: estimates based on 840,149 screening colonoscopies. Gut. 2007;56:1585–9. doi: 10.1136/gut.2007.122739 17591622

50. Hoff G, Foerster A, Vatn MH, Sauar J, Larsen S. Epidemiology of polyps in the rectum and colon. Recovery and evaluation of unresected polyps 2 years after detection. Scand J Gastroenterol. 1986;21:853–62. doi: 10.3109/00365528609011130 3775252

51. Hoff G, Larsen S. Epidemiology of polyps in the rectum and sigmoid colon. Discriminant analysis for identification of individuals at risk of developing colorectal neoplasia. Scand J Gastroenterol. 1986;21:848–52. doi: 10.3109/00365528609011129 3775251

52. Berrino F, Gatta G, d'Alto M, Crosignani P, Riboli E. Efficacy of screening in preventing invasive cervical cancer: a case-control study in Milan, Italy. IARC Sci Publ. 1986:111–23.

53. Schenck AP, Klabunde CN, Warren JL, Peacock S, Davis WW, Hawley ST, et al. Evaluation of claims, medical records, and self-report for measuring fecal occult blood testing among medicare enrollees in fee for service. Cancer Epidemiol Biomarkers Prev. 2008;17:799–804. doi: 10.1158/1055-9965.EPI-07-2620 18381471

54. Economic Research Service. Rural-Urban Continuum Codes: United States Department of Agriculture; 2013. Available from: Accessed June 29, 2018.

55. NCI Comorbidity Index Overview Bethesda, MD: National Cancer Institute. Available from: Accessed May 4, 2018.

56. Ko CW, Dominitz JA, Green P, Kreuter W, Baldwin LM. Specialty differences in polyp detection, removal, and biopsy during colonoscopy. Am J Med. 2010;123:528–35. doi: 10.1016/j.amjmed.2010.01.016 20569759

57. Ko CW, Dominitz JA, Green P, Kreuter W, Baldwin LM. Utilization and predictors of early repeat colonoscopy in Medicare beneficiaries. Am J Gastroenterol. 2010;105:2670–9.

58. Ko CW, Dominitz JA, Green P, Kreuter W, Baldwin LM. Accuracy of Medicare claims for identifying findings and procedures performed during colonoscopy. Gastrointest Endosc. 2011;73:447–53. doi: 10.1016/j.gie.2010.07.044 20950800

59. Garcia-Albeniz X, Hsu J, Bretthauer M, Hernan MA. Effectiveness of Screening Colonoscopy to Prevent Colorectal Cancer Among Medicare Beneficiaries Aged 70 to 79 Years: A Prospective Observational Study. Ann Intern Med. 2017;166:18–26. doi: 10.7326/M16-0758 27669524

60. Baxter NN, Warren JL, Barrett MJ, Stukel TA, Doria-Rose VP. The association between colonoscopy and colorectal cancer mortality in a U.S. cohort according to site of cancer and colonoscopist. Gastroenterology. 2011;140 (Suppl 1):S74–S5.

61. Schoen RE, Razzak A, Yu KJ, Berndt SI, Firl K, Riley TL, et al. Incidence and mortality of colorectal cancer in individuals with a family history of colorectal cancer. Gastroenterology. 2015;149:1438–45 e1. doi: 10.1053/j.gastro.2015.07.055 26255045

62. Boroff ES, Gurudu SR, Hentz JG, Leighton JA, Ramirez FC. Polyp and adenoma detection rates in the proximal and distal colon. Am J Gastroenterol. 2013;108:993–9. doi: 10.1038/ajg.2013.68 23567353

63. Francis DL, Rodriguez-Correa DT, Buchner A, Harewood GC, Wallace M. Application of a conversion factor to estimate the adenoma detection rate from the polyp detection rate. Gastrointest Endosc. 2011;73:493–7. doi: 10.1016/j.gie.2011.01.005 21353846

64. Patel NC, Islam RS, Wu Q, Gurudu SR, Ramirez FC, Crowell MD, et al. Measurement of polypectomy rate by using administrative claims data with validation against the adenoma detection rate. Gastrointest Endosc. 2013;77:390–4. doi: 10.1016/j.gie.2012.09.032 23199647

Článek vyšel v časopise


2019 Číslo 12