Effects of Organized Colorectal Cancer Screening on Cancer Incidence and Mortality in a Large Community-Based Population

Gastroenterology

Volumn 155, Issue 5, 2018, Pages 1383-1391.e5

  Levin, Theodore R ^a,b   Corley, Douglas A ^b   Jensen, Christopher D ^b   Schottinger, Joanne E ^c   Quinn, Virginia P ^c   Zauber, Ann G ^d   Lee, Jeffrey K ^b   Zhao, Wei K ^b   Udaltsova, Natalia ^b   Ghai, Nirupa R ^c   Lee, Alexander T ^c   Quesenberry, Charles P ^b   Fireman, Bruce H ^b   Doubeni, Chyke A ^e  

^a KAISER PERMANENTE MEDICAL CENTER   (United States)

^b DIVISION OF RESEARCH   (United States)

^c KAISER PERMANENTE   (United States)

^d MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Colon Cancer; Early Detection; FIT; Neoplasm

Indexed keywords

ADULT; AGED; ARTICLE; CANCER DIAGNOSIS; CANCER INCIDENCE; CANCER MORTALITY; CANCER SCREENING; CANCER STAGING; COLONOSCOPY; COLORECTAL CANCER; FEMALE; HUMAN; MAJOR CLINICAL STUDY; MIDDLE AGED; MORTALITY RATE; OCCULT BLOOD TEST; POPULATION RESEARCH; PRIORITY JOURNAL; SIGMOIDOSCOPY; COLORECTAL TUMOR; EARLY CANCER DIAGNOSIS; INCIDENCE; MALE; MORTALITY; OCCULT BLOOD;

AGED; COLONOSCOPY; COLORECTAL NEOPLASMS; EARLY DETECTION OF CANCER; FEMALE; HUMANS; INCIDENCE; MALE; MIDDLE AGED; OCCULT BLOOD;

EID: 85055808039     PISSN: 00165085     EISSN: 15280012     Source Type: Journal    
DOI: 10.1053/j.gastro.2018.07.017     Document Type: Article

References (65)

1. Siegel, R.L., Miller, K.D., Jemal, A., Cancer statistics, 2017. CA Cancer J Clin 67 (2017), 7–30.
2. Brenner, H., Chang-Claude, J., Seiler, C.M., et al. Protection from colorectal cancer after colonoscopy: a population-based, case-control study. Ann Intern Med 154 (2011), 22–30.
3. Zauber, A.G., Winawer, S.J., O'Brien, M.J., et al. Colonoscopic polypectomy and long-term prevention of colorectal-cancer deaths. N Engl J Med 366 (2012), 687–696.
4. US Preventive Services Task Force, Bibbins-Domingo, K., Grossman, D.C., et al. Screening for Colorectal Cancer: US Preventive Services Task Force Recommendation Statement. JAMA 315 (2016), 2564–2575.
5. National Colorectal Cancer Roundtable. About 80% by 2018. Available at: http://nccrt.org/wp-content/uploads/80-by-2018-TALKINGPOINTS-Final-2.16.17.pdf. Accessed May 30, 2017.
6. Meester, R.G., Doubeni, C.A., Zauber, A.G., et al. Public health impact of achieving 80% colorectal cancer screening rates in the United States by 2018. Cancer 121 (2015), 2281–2285.
7. Colorectal Cancer facts & figures 2017–2019. Available at: https://www.cancer.org/content/dam/cancer-org/research/cancer-facts-and-statistics/colorectal-cancer-facts-and-figures/colorectal-cancer-facts-and-figures-2017-2019.pdf. Accessed November 9, 2017.
8. Screening rates for several cancers miss their targets. Available at: https://www.cancer.gov/news-events/cancer-currents-blog/2015/screening-targets. Accessed November 9, 2017.
9. Benson, V.S., Atkin, W.S., Green, J., et al. Toward standardizing and reporting colorectal cancer screening indicators on an international level: The International Colorectal Cancer Screening Network. Int J Cancer 130 (2012), 2961–2973.
10. Zauber, A.G., Lansdorp-Vogelaar, I., Knudsen, A.B., et al. Evaluating test strategies for colorectal cancer screening: a decision analysis for the U.S. Preventive Services Task Force. Ann Intern Med 149 (2008), 659–669.
11. Lin, J.S., Piper, M.A., Perdue, L.A., et al. Screening for colorectal cancer: updated evidence report and systematic review for the US Preventive Services Task Force. JAMA 315 (2016), 2576–2594.
12. Lin, J.S., Piper, M.A., Perdue, L.A., et al. Screening for Colorectal Cancer: A Systematic Review for the US Preventive Services Task Force. 2016, Agency for Healthcare Research and Quality, Rockville, MD.
13. Atkin, W.S., Edwards, R., Kralj-Hans, I., et al. Once-only flexible sigmoidoscopy screening in prevention of colorectal cancer: a multicentre randomised controlled trial. Lancet 375:9726 (2010), 1624–1633.
14. Schoen, R.E., Pinsky, P.F., Weissfeld, J.L., et al. Colorectal-cancer incidence and mortality with screening flexible sigmoidoscopy. N Engl J Med 366 (2012), 2345–2357.
15. 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 103 (2011), 1310–1322.
16. Atkin, W.S., Cook, C.F., Cuzick, J., et al. Single flexible sigmoidoscopy screening to prevent colorectal cancer: baseline findings of a UK multicentre randomised trial. Lancet 359:9314 (2002), 1291–1300.
17. Holme, O., Loberg, M., Kalager, M., et al. Effect of flexible sigmoidoscopy screening on colorectal cancer incidence and mortality: a randomized clinical trial. JAMA 312 (2014), 606–615.
18. Segnan, N., Senore, C., Andreoni, B., et al. Baseline findings of the Italian multicenter randomized controlled trial of “once-only sigmoidoscopy”—SCORE. J Natl Cancer Inst 94 (2002), 1763–1772.
19. Weissfeld, J.L., Schoen, R.E., Pinsky, P.F., et al. Flexible sigmoidoscopy in the PLCO cancer screening trial: results from the baseline screening examination of a randomized trial. J Natl Cancer Inst 97 (2005), 989–997.
20. Baxter, N.N., Goldwasser, M.A., Paszat, L.F., Saskin, R., Urbach, D.R., Rabeneck, L., Association of colonoscopy and death from colorectal cancer. Ann Intern Med 150 (2009), 1–8.
21. Doubeni, C.A., Corley, D.A., Quinn, V.P., et al. Effectiveness of screening colonoscopy in reducing the risk of death from right and left colon cancer: a large community-based study. Gut 67 (2018), 291–298.
22. Lakoff, J., Paszat, L.F., Saskin, R., et al. Risk of developing proximal versus distal colorectal cancer after a negative colonoscopy: a population-based study. Clin Gastroenterol Hepatol 6 (2008), 1117–1121 quiz 1064.
23. Nishihara, R., Wu, K., Lochhead, P., et al. Long-term colorectal-cancer incidence and mortality after lower endoscopy. N Engl J Med 369 (2013), 1095–1105.
24. Singh, H., Nugent, Z., Demers, A.A., et al. The reduction in colorectal cancer mortality after colonoscopy varies by site of the cancer. Gastroenterology 139 (2010), 1128–1137.
25. Faivre, J., Dancourt, V., Lejeune, C., et al. Reduction in colorectal cancer mortality by fecal occult blood screening in a French controlled study. Gastroenterology 126 (2004), 1674–1680.
26. Kronborg, O., Jorgensen, O.D., Fenger, C., et al. Randomized study of biennial screening with a faecal occult blood test: results after nine screening rounds. Scand J Gastroenterol 39 (2004), 846–851.
27. 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 18 (2011), 18–23.
28. Scholefield, J.H., Moss, S.M., Mangham, C.M., et al. Nottingham trial of faecal occult blood testing for colorectal cancer: a 20-year follow-up. Gut 61 (2012), 1036–1040.
29. Shaukat, A., Mongin, S.J., Geisser, M.S., et al. Long-term mortality after screening for colorectal cancer. N Engl J Med 369 (2013), 1106–1114.
30. Hardcastle, J.D., Chamberlain, J.O., Robinson, M.H., et al. Randomised controlled trial of faecal-occult-blood screening for colorectal cancer. Lancet 348:9040 (1996), 1472–1477.
31. Malila, N., Oivanen, T., Malminiemi, O., et al. Test, episode, and programme sensitivities of screening for colorectal cancer as a public health policy in Finland: experimental design. BMJ, 337, 2008, a2261.
32. Mandel, J.S., Church, T.R., Bond, J.H., et al. The effect of fecal occult-blood screening on the incidence of colorectal cancer. N Engl J Med 343 (2000), 1603–1607.
33. Mandel, J.S., Bond, J.H., Church, T.R., et al. Reducing mortality from colorectal cancer by screening for fecal occult blood. Minnesota Colon Cancer Control Study. N Engl J Med 328 (1993), 1365–1371.
34. Thomas, W., White, C.M., Mah, J., et al. Longitudinal compliance with annual screening for fecal occult blood. Minnesota Colon Cancer Control Study. Am J Epidemiol 142 (1995), 176–182.
35. Lindholm, E., Brevinge, H., Haglind, E., Survival benefit in a randomized clinical trial of faecal occult blood screening for colorectal cancer. Br J Surg 95 (2008), 1029–1036.
36. van Rossum, L.G., van Rijn, A.F., Laheij, R.J., et al. Random comparison of guaiac and immunochemical fecal occult blood tests for colorectal cancer in a screening population. Gastroenterology 135 (2008), 82–90.
37. Allison, J.E., Sakoda, L.C., Levin, T.R., et al. Screening for colorectal neoplasms with new fecal occult blood tests: update on performance characteristics. J Natl Cancer Inst 99 (2007), 1462–1470.
38. Smith, A., Young, G.P., Cole, S.R., 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 107 (2006), 2152–2159.
39. Inadomi, J.M., Vijan, S., Janz, N.K., et al. Adherence to colorectal cancer screening: a randomized clinical trial of competing strategies. Arch Intern Med 172 (2012), 575–582.
40. Gupta, S., Halm, E.A., Rockey, D.C., et al. Comparative effectiveness of fecal immunochemical test outreach, colonoscopy outreach, and usual care for boosting colorectal cancer screening among the underserved: a randomized clinical trial. JAMA Intern Med 173 (2013), 1725–1732.
41. Gordon NP. How does the adult Kaiser Permanente membership in Northern California compare with the larger community? Available at: http://www.dor.kaiser.org/dor/mhsnet/public/kpnc_community.htm. Published 2006. Accessed March 10, 2017.
42. Levin, T.R., Jamieson, L., Burley, D.A., et al. Organized colorectal cancer screening in integrated health care systems. Epidemiol Rev 33 (2011), 101–110.
43. Jensen, C.D., Corley, D.A., Quinn, V.P., et al. Fecal immunochemical test program performance over 4 rounds of annual screening: a retrospective cohort study. Ann Intern Med 164 (2016), 456–463.
44. Mehta, S.J., Jensen, C.D., Quinn, V.P., et al. Race/ethnicity and adoption of a population health management approach to colorectal cancer screening in a community-based healthcare system. J Gen Intern Med 31 (2016), 1323–1330.
45. Sarfaty, M., Myers, R.E., The effect of HEDIS measurement of colorectal cancer screening on insurance plans in Pennsylvania. Am J Manag Care 14 (2008), 277–282.
46. HEDIS & Performance Measurement. Available at: http://www.ncqa.org/hedis-quality-measurement. Accessed June 8, 2017.
47. Chu, K.C., Miller, B.A., Feuer, E.J., et al. A method for partitioning cancer mortality trends by factors associated with diagnosis: an application to female breast cancer. J Clin Epidemiol 47 (1994), 1451–1461.
48. Corley, D.A., Jensen, C.D., Marks, A.R., et al. Adenoma detection rate and risk of colorectal cancer and death. N Engl J Med 370 (2014), 1298–1306.
49. Lee, J.K., Jensen, C.D., Lee, A., et al. Development and validation of an algorithm for classifying colonoscopy indication. Gastrointest Endosc 81 (2015), 575–582 e574.
50. National Institutes of Health, National Cancer Institute. Surveillance, Epidemiology, and End Results Program. SEER Program Coding and Staging Manual 2013. Available at: http://seer.cancer.gov/manuals/2013/SPCSM_2013_maindoc.pdf. Accessed March 10, 2017.
51. National Institutes of Health, National Cancer Institute. Surveillance, Epidemiology, and End Results Program. Standard populations–single ages. https://seer.cancer.gov/stdpopulations/stdpop.singleages.html.
52. Zorzi, M., Fedeli, U., Schievano, E., et al. Impact on colorectal cancer mortality of screening programmes based on the faecal immunochemical test. Gut 64 (2015), 784–790.
53. Chiu, H.M., Chen, S.L., Yen, A.M., et al. Effectiveness of fecal immunochemical testing in reducing colorectal cancer mortality from the One Million Taiwanese Screening Program. Cancer 121 (2015), 3221–3229.
54. National Institutes of Health, National Cancer Institute. Surveillance, Epidemiology, and End Results Program. SEER stat fact sheets: colon and rectum cancer. Available at: http://seer.cancer.gov/statfacts/html/colorect.html. Accessed June 8, 2017.
55. Siegel, R.L., Ward, E.M., Jemal, A., Trends in colorectal cancer incidence rates in the United States by tumor location and stage, 1992–2008. Cancer Epidemiol Biomarkers Prev 21 (2012), 411–416.
56. Mandel, J.S., Church, T.R., Ederer, F., et al. Colorectal cancer mortality: effectiveness of biennial screening for fecal occult blood. J Natl Cancer Inst 91 (1999), 434–437.
57. Murphy, C.C., Sandler, R.S., Sanoff, H.K., et al. Decrease in incidence of colorectal cancer among individuals 50 years or older after recommendations for population-based screening. Clin Gastroenterol Hepatol 15 (2017), 903–909 e906.
58. Siegel, R.L., Miller, K.D., Fedewa, S.A., et al. Colorectal cancer statistics, 2017. CA Cancer J Clin 67 (2017), 177–193.
59. Colorectal Cancer Screening. Cancer Trends Progress Report. Available at: https://progressreport.cancer.gov/detection/colorectal_cancer. Accessed September 27, 2017.
60. Edwards, B.K., Ward, E., Kohler, B.A., 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 116 (2010), 544–573.
61. Rauscher, G.H., Johnson, T.P., Cho, Y.I., et al. Accuracy of self-reported cancer-screening histories: a meta-analysis. Cancer Epidemiol Biomarkers Prev 17 (2008), 748–757.
62. Pinsky, P.F., Miller, A., Kramer, B.S., et al. Evidence of a healthy volunteer effect in the prostate, lung, colorectal, and ovarian cancer screening trial. Am J Epidemiol 165 (2007), 874–881.
63. Horne, H.N., Phelan-Emrick, D.F., Pollack, C.E., et al. Effect of patient navigation on colorectal cancer screening in a community-based randomized controlled trial of urban African American adults. Cancer Causes Control 26 (2015), 239–246.
64. May, F.P., Yano, E.M., Provenzale, D., Neil Steers, W., Washington, D.L., The association between primary source of healthcare coverage and colorectal cancer screening among US veterans. Dig Dis Sci 62 (2017), 1923–1932.
65. Castaneda, S.F., Bharti, B., Espinoza-Giacinto, R.A., et al. Evaluating two evidence-based intervention strategies to promote crc screening among latino adults in a primary care setting. J Racial Ethn Health Disparities 5 (2018), 530–535.