Digestive Diseases and Sciences

, Volume 60, Issue 3, pp 681–691 | Cite as

The Impact of Screening on Colorectal Cancer Mortality and Incidence: Has It Really Made a Difference?

Review

Abstract

About sixty percent of the US population of those age fifty and older are currently up to date with colorectal cancer screening recommendations. Has this level of screening made a difference for reducing colorectal cancer (CRC) incidence and/or mortality? Randomized controlled trials of guaiac-based fecal occult blood tests, which have relatively low sensitivity but high specificity for CRC, have shown a modest effect but with a long-term reduction in CRC mortality. Newer fecal immunochemical tests are expected to have a greater effect. Randomized controlled trials of flexible sigmoidoscopy have also demonstrated a reduction in CRC mortality. Observational studies of screening colonoscopy suggest an effect of greater than fifty percent reduction in CRC mortality. We have assessed past trends of colorectal cancer screening in the US population which suggest that more than fifty percent of the decline in colorectal cancer mortality can be attributed to the increased acceptance and uptake in colorectal cancer screening. Current and future levels of increased screening could provide for even larger reductions for the USA. Colorectal cancer screening has and will continue to make a significant impact on reducing colorectal cancer mortality.

Keywords

Colorectal cancer screening Impact of screening Incidence and mortality 

Notes

Acknowledgments

This work is supported in part from the following grants: U01 CA-152959, U01 CA-151736, U54 CA-163262, R01 CA-079572, and P30 CA008748.

Conflict of interest

None.

References

  1. 1.
    Howlader N, Noone AM, Krapcho M, et al. SEER Cancer Statistics Review, 1975–2011, National Cancer Institute, Bethesda, MD. http://seer.cancer.gov/csr/1975_2011/, based on November 2013 SEER data submission, posted to the SEER website, April 2014.
  2. 2.
    Hardcastle JD, Chamberlain JO, Robinson MH, et al. Randomised controlled trial of faecal-occult-blood screening for colorectal cancer. Lancet. 1996;348:1472–1477.CrossRefPubMedGoogle Scholar
  3. 3.
    Kronborg O, Fenger C, Olsen J, Jorgensen OD, Sondergaard O. Randomised study of screening for colorectal cancer with faecal-occult-blood test. Lancet. 1996;348:1467–1471.CrossRefPubMedGoogle Scholar
  4. 4.
    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;328:1365–1371.CrossRefPubMedGoogle Scholar
  5. 5.
    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;343:1603–1607.CrossRefPubMedGoogle Scholar
  6. 6.
    Shaukat A, Mongin SJ, Geisser MS, et al. Long-term mortality after screening for colorectal cancer. N Engl J Med. 2013;369:1106–1114.CrossRefPubMedGoogle Scholar
  7. 7.
    Hewitson P, Glasziou P, Watson E, Towler B, Irwig L. Cochrane systematic review of colorectal cancer screening using the fecal occult blood test (hemoccult): an update. Am J Gastroenterol. 2008;103:1541–1549.CrossRefPubMedGoogle Scholar
  8. 8.
    Atkin WS. Single flexible sigmoidoscopy screening to prevent colorectal cancer: baseline findings of a UK multicentre randomised trial. Lancet. 2002;359:1291–1300.CrossRefPubMedGoogle Scholar
  9. 9.
    Segnan N, Armaroli P, Bonelli L, et al. Once-only sigmoidoscopy in colorectal cancer screening: follow-up findings of the Italian Randomized Controlled Trial–SCORE. J Natl Cancer Inst. 2011;103:1310–1322.CrossRefPubMedGoogle Scholar
  10. 10.
    Schoen RE, Pinsky PF, Weissfeld JL, et al. Colorectal-cancer incidence and mortality with screening flexible sigmoidoscopy. N Engl J Med. 2012;366:2345–2357.CrossRefPubMedCentralPubMedGoogle Scholar
  11. 11.
    Holme O, Loberg M, Kalager M, et al. Effect of flexible sigmoidoscopy screening on colorectal cancer incidence and mortality: a randomized clinical trial. JAMA. 2014;312:606–615.CrossRefPubMedGoogle Scholar
  12. 12.
    Klabunde CN, Cronin KA, Breen N, Waldron WR, Ambs AH, Nadel MR. Trends in colorectal cancer test use among vulnerable populations in the United States. Cancer Epidemiol Biomark Prev. 2011;20:1611–1621.CrossRefGoogle Scholar
  13. 13.
    Podolsky DK. Going the distance—the case for true colorectal-cancer screening. N Engl J Med. 2000;343:207–208.CrossRefPubMedGoogle Scholar
  14. 14.
    Quintero E, Castells A, Bujanda L, et al. Colonoscopy versus fecal immunochemical testing in colorectal-cancer screening. N Engl J Med. 2012;366:697–706.CrossRefPubMedGoogle Scholar
  15. 15.
    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;44:695–702.CrossRefPubMedGoogle Scholar
  16. 16.
    Winawer SJ, Fletcher RH, Miller L, et al. Colorectal cancer screening: clinical guidelines and rationale. Gastroenterology. 1997;112:594–642.CrossRefPubMedGoogle Scholar
  17. 17.
    Levin B, Brooks D, Smith RA, Stone A. Emerging technologies in screening for colorectal cancer: CT colonography, immunochemical fecal occult blood tests, and stool screening using molecular markers. CA Cancer J Clin. 2003;53:44–55.CrossRefPubMedGoogle Scholar
  18. 18.
    Levin B, Lieberman DA, McFarland B, 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.CrossRefPubMedGoogle Scholar
  19. 19.
    Lee JK, Liles EG, Bent S, Levin TR, Corley DA. Accuracy of fecal immunochemical tests for colorectal cancer: systematic review and meta-analysis. Ann Intern Med. 2014;160:171.CrossRefPubMedCentralPubMedGoogle Scholar
  20. 20.
    Allison JE, Fraser CG, Halloran SP, Young GP. Population screening for colorectal cancer means getting FIT: the past, present, and future of colorectal cancer screening using the fecal immunochemical test for hemoglobin (FIT). Gut Liver. 2014;8:117–130.CrossRefPubMedCentralPubMedGoogle Scholar
  21. 21.
    Allison JE, Lawson M. Screening tests for colorectal cancer: a menu of options remains relevant. Curr Oncol Rep. 2006;8:492–498.CrossRefPubMedGoogle Scholar
  22. 22.
    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;99:1462–1470.CrossRefPubMedGoogle Scholar
  23. 23.
    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.CrossRefPubMedGoogle Scholar
  24. 24.
    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 (Oxford, England). 1990;2013:3049–3054.Google Scholar
  25. 25.
    Imperiale TF, Ransohoff DF, Itzkowitz SH, et al. Multitarget stool DNA testing for colorectal-cancer screening. N Engl J Med. 2014;370:1287–1297.CrossRefPubMedGoogle Scholar
  26. 26.
    Winawer SJ, Flehinger BJ, Schottenfeld D, Miller DG. Screening for colorectal cancer with fecal occult blood testing and sigmoidoscopy. J Natl Cancer Inst. 1993;85:1311–1318.CrossRefPubMedGoogle Scholar
  27. 27.
    Johnson CD, Chen MH, Toledano AY, et al. Accuracy of CT colonography for detection of large adenomas and cancers. N Engl J Med. 2008;359:1207–1217.CrossRefPubMedCentralPubMedGoogle Scholar
  28. 28.
    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;349:2191–2200. doi:10.1007/s1620-014-3454-2.CrossRefPubMedGoogle Scholar
  29. 29.
    Bertario L, Russo A, Crosignani P, et al. Reducing colorectal cancer mortality by repeated faecal occult blood test: a nested case-control study. Eur J Cancer (Oxford, England). 1990;1999:973–977.Google Scholar
  30. 30.
    Faivre J, Tazi MA, El Mrini T, Lejeune C, Benhamiche AM, Dassonville F. Faecal occult blood screening and reduction of colorectal cancer mortality: a case-control study. Br J Cancer. 1999;79:680–683.CrossRefPubMedCentralPubMedGoogle Scholar
  31. 31.
    Lazovich D, Weiss NS, Stevens NG, White E, McKnight B, Wagner EH. A case-control study to evaluate efficacy of screening for faecal occult blood. J Med Screen. 1995;2:84–89.PubMedGoogle Scholar
  32. 32.
    Nakama H. A study on the efficacy of a screening program for colorectal cancer in a small Japanese village. Clin Invest. 1994;72:117–121.Google Scholar
  33. 33.
    Selby JV, Friedman GD, Quesenberry CP Jr, Weiss NS. Effect of fecal occult blood testing on mortality from colorectal cancer. A case–control study. Ann Int Med. 1993;118:1–6.CrossRefPubMedGoogle Scholar
  34. 34.
    Wahrendorf J, Robra BP, Wiebelt H, Oberhausen R, Weiland M, Dhom G. Effectiveness of colorectal cancer screening: results from a population-based case-control evaluation in Saarland. Germany Eur J Cancer Prev. 1993;2:221–227.CrossRefGoogle Scholar
  35. 35.
    Zappa M, Castiglione G, Grazzini G, et al. Effect of faecal occult blood testing on colorectal mortality: results of a population-based case-control study in the district of Florence, Italy. Int J Cancer. 1997;73:208–210.CrossRefPubMedGoogle Scholar
  36. 36.
    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.CrossRefPubMedGoogle Scholar
  37. 37.
    Newcomb PA, Norfleet RG, Storer BE, Surawicz TS, Marcus PM. Screening sigmoidoscopy and colorectal cancer mortality. J Natl Cancer Inst. 1992;84:1572–1575.CrossRefPubMedGoogle Scholar
  38. 38.
    Baxter NN, Goldwasser MA, Paszat LF, Saskin R, Urbach DR, Rabeneck L. Association of colonoscopy and death from colorectal cancer. Ann Int Med. 2009;150:1–8.CrossRefPubMedGoogle Scholar
  39. 39.
    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;30:2664–2669.CrossRefPubMedCentralPubMedGoogle Scholar
  40. 40.
    Doubeni CA, Weinmann S, Adams K, et al. Screening colonoscopy and risk for incident late-stage colorectal cancer diagnosis in average-risk adults: a nested case-control study. Ann Int Med. 2013;158:312–320.CrossRefPubMedCentralPubMedGoogle Scholar
  41. 41.
    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.Google Scholar
  42. 42.
    Nishihara R, Wu K, Lochhead P, et al. Long-term colorectal-cancer incidence and mortality after lower endoscopy. N Engl J Med. 2013;369:1095–1105.CrossRefPubMedGoogle Scholar
  43. 43.
    Hixson LJ, Fennerty MB, Sampliner RE, Garewal HS. Prospective blinded trial of the colonoscopic miss-rate of large colorectal polyps. Gastrointest Endosc. 1991;37:125–127.CrossRefPubMedGoogle Scholar
  44. 44.
    Hixson LJ, Fennerty MB, Sampliner RE, McGee D, Garewal H. Prospective study of the frequency and size distribution of polyps missed by colonoscopy. J Natl Cancer Inst. 1990;82:1769–1772.CrossRefPubMedGoogle Scholar
  45. 45.
    Rex DK, Cutler CS, Lemmel GT, et al. Colonoscopic miss rates of adenomas determined by back-to-back colonoscopies. Gastroenterology. 1997;112:24–28.CrossRefPubMedGoogle Scholar
  46. 46.
    Zauber AG, Winawer SJ, O’Brien MJ, et al. Colonoscopic polypectomy and long-term prevention of colorectal-cancer deaths. N Engl J Med. 2012;366:687–696.CrossRefPubMedCentralPubMedGoogle Scholar
  47. 47.
    Loberg M, Kalager M, Holme O, Hoff G, Adami HO, Bretthauer M. Long-term colorectal-cancer mortality after adenoma removal. N Engl J Med. 2014;371:799–807.CrossRefPubMedGoogle Scholar
  48. 48.
    Loeve F, van Ballegooijen M, Boer R, Kuipers EJ, Habbema JD. Colorectal cancer risk in adenoma patients: a nation-wide study. Int J Cancer. 2004;111:147–151.CrossRefPubMedGoogle Scholar
  49. 49.
    Robertson DJ, Greenberg E, Beach M, et al. Colorectal cancer in patients under close colonoscopic surveillance. Gastroenterol. 2005;129:34–41.CrossRefGoogle Scholar
  50. 50.
    Zauber AG, Winawer SJ. High-quality colonoscopies must be an integral part of screening and surveillance programs. Gastroenterology. 2006;130:620–621; author reply 621–622.Google Scholar
  51. 51.
    Lieberman DA, Weiss DG, Harford WV, et al. Five-year colon surveillance after screening colonoscopy. Gastroenterology. 2007;133:1077–1085.CrossRefPubMedGoogle Scholar
  52. 52.
    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.CrossRefPubMedGoogle Scholar
  53. 53.
    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.Google Scholar
  54. 54.
    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.CrossRefPubMedGoogle Scholar
  55. 55.
    Corley DA, Jensen CD, Marks AR, et al. Adenoma detection rate and risk of colorectal cancer and death. N Engl J Med. 2014;370:1298–1306.CrossRefPubMedCentralPubMedGoogle Scholar
  56. 56.
    Kaminski MF, Regula J, Kraszewska E, et al. Quality indicators for colonoscopy and the risk of interval cancer. N Engl J Med. 2010;362:1795–1803.CrossRefPubMedGoogle Scholar
  57. 57.
    Zauber AG, Lansdorp-Vogelaar I, Knudsen AB, Wilschut J, van Ballegooijen M, Kuntz KM. Evaluating test strategies for colorectal cancer screening: a decision analysis for the U.S. Preventive Services Task Force. Ann Intern Med. 2008;149:659–669.CrossRefPubMedCentralPubMedGoogle Scholar
  58. 60.
    Vogelaar I, van Ballegooijen M, Schrag D, et al. How much can current interventions reduce colorectal cancer mortality in the U.S.? Mortality projections for scenarios of risk-factor modification, screening, and treatment. Cancer. 2006;107:1624–1633.CrossRefPubMedGoogle Scholar
  59. 59.
    Edwards BK, Ward E, Kohler BA, et al. Annual report to the nation on the status of cancer, 1975-2006, featuring colorectal cancer trends and impact of interventions (risk factors, screening, and treatment) to reduce future rates. Cancer. 2010;116:544–573.CrossRefPubMedCentralPubMedGoogle Scholar
  60. 60.
    Meester RG, Doubeni C, Lansdorp-Vogelaar I, et al. Colorectal deaths attributable to non-use of screening in the United States. Ann Epidemiol. 2015;25:208–213.CrossRefPubMedGoogle Scholar
  61. 61.
    Lee JK, Levin TR, Corley DA. The road ahead: what if gastroenterologists were accountable for preventing colorectal cancer? Clin Gastroenterol Hepatol. 2013;11:204–207.CrossRefPubMedCentralPubMedGoogle Scholar
  62. 62.
    Lansdorp-Vogelaar I, Kuntz KM, Knudsen AB, van Ballegooijen M, Zauber AG, Jemal A. Contribution of screening and survival differences to racial disparities in colorectal cancer rates. Cancer Epidemiol Biomark Prev. 2012;21:728–736.CrossRefGoogle Scholar
  63. 63.
    Jemal A, Siegel RL, Ma J, et al. Inequalities in premature death from colorectal cancer by state. J Clin Oncol. 2014. doi:10.1200/JCO.2014.58.7519.Google Scholar
  64. 64.
    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.CrossRefPubMedGoogle Scholar
  65. 65.
    Atkin WS, Edwards R, Kralj-Hans I, et al. Once-only flexible sigmoidoscopy screening in prevention of colorectal cancer: a multicentre randomised controlled trial. Lancet. 2010;375:1624–1633.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  1. 1.Department of Epidemiology and BiostatisticsMemorial Sloan Kettering Cancer CenterNew YorkUSA

Personalised recommendations