Cited by 362Colorectal Cancer Screening and DetectionGlobal Cancer Incidence and ScreeningColorectal Cancer Surgical Treatments

Evaluation of Interventions Intended to Increase Colorectal Cancer Screening Rates in the United States: A Systematic Review and Meta-analysis

Open access
Dougherty, Michael K., Brenner, Alison T., Crockett, Seth D., Gupta, Shivani, Wheeler, Stephanie B., Coker-Schwimmer, Manny, Cubillos, Laura, Malo, Teri +1 more·2018·JAMA Internal Medicine

Abstract

Importance: Colorectal cancer screening (CRC) is recommended by all major US medical organizations but remains underused. Objective: To identify interventions associated with increasing CRC screening rates and their effect sizes. Data Sources: PubMed, Cumulative Index to Nursing and Allied Health Literature, the Cochrane Library, and ClinicalTrials.gov were searched from January 1, 1996, to August 31, 2017. Key search terms included colorectal cancer and screening. Study Selection: Randomized clinical trials of US-based interventions in clinical settings designed to improve CRC screening test completion in average-risk adults. Data Extraction and Synthesis: At least 2 investigators independently extracted data and appraised each study's risk of bias. Where sufficient data were available, random-effects meta-analysis was used to obtain either a pooled risk ratio (RR) or risk difference (RD) for screening completion for each type of intervention. Main Outcomes and Measures: The main outcome was completion of CRC screening. Examination included interventions to increase completion of (1) initial CRC screening by any recommended modality, (2) colonoscopy after an abnormal initial screening test result, and (3) continued rounds of annual fecal blood tests (FBTs). Results: The main review included 73 randomized clinical trials comprising 366 766 patients at low or medium risk of bias. Interventions that were associated with increased CRC screening completion rates compared with usual care included FBT outreach (RR, 2.26; 95% CI, 1.81-2.81; RD, 22%; 95% CI, 17%-27%), patient navigation (RR, 2.01; 95% CI, 1.64-2.46; RD, 18%; 95% CI, 13%-23%), patient education (RR, 1.20; 95% CI, 1.06-1.36; RD, 4%; 95% CI, 1%-6%), patient reminders (RR, 1.20; 95% CI, 1.02-1.41; RD, 3%; 95% CI, 0%-5%), clinician interventions of academic detailing (RD, 10%; 95% CI, 3%-17%), and clinician reminders (RD, 13%; 95% CI, 8%-19%). Combinations of interventions (clinician interventions or navigation added to FBT outreach) were associated with greater increases than single components (RR, 1.18; 95% CI, 1.09-1.29; RD, 7%; 95% CI, 3%-11%). Repeated mailed FBTs with navigation were associated with increased annual FBT completion (RR, 2.09; 95% CI, 1.91-2.29; RD, 39%; 95% CI, 29%-49%). Patient navigation was not associated with colonoscopy completion after an initial abnormal screening test result (RR, 1.21; 95% CI, 0.92-1.60; RD, 14%; 95% CI, 0%-29%). Conclusions and Relevance: Fecal blood test outreach and patient navigation, particularly in the context of multicomponent interventions, were associated with increased CRC screening rates in US trials. Fecal blood test outreach should be incorporated into population-based screening programs. More research is needed on interventions to increase adherence to continued FBTs, follow-up of abnormal initial screening test results, and cost-effectiveness and other implementation barriers for more intensive interventions, such as navigation.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1001/jamainternmed.2018.4637

Cites

3 of 3 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 57

  1. Brenner H, Stock C, Hoffmeister M. Effect of screening sigmoidoscopy and screening colonoscopy on colorectal cancer incidence and mortality: systematic review and meta-analysis of randomised controlled trials and observational studies. BMJ. 2014;348:g2467. doi:10.1136/bmj .g2467 · DOI
  2. Wilt TJ, Harris RP, Qaseem A; High Value Care Task Force of the American College of Physicians. Screening for cancer: advice for high-value care from the American College of Physicians. Ann Intern Med. 2015;162(10):718-725. doi:10.7326/M14-2326 · DOI
  3. Rex DK, Boland CR, Dominitz JA, et al. Colorectal cancer screening: recommendations for physicians and patients from the US Multi-Society Task Force on Colorectal Cancer. Gastrointest Endosc. 2017;86 (1):18-33. doi:10.1016/j.gie.2017.04.003 · DOI
  4. Siegel RL, Miller KD, Fedewa SA, et al. Colorectal cancer statistics, 2017. CA Cancer J Clin. 2017;67 (3):177-193. doi:10.3322/caac.21395 · DOI
  5. Volk RJ, Linder SK, Lopez-Olivo MA, et al. Patient decision aids for colorectal cancer screening: a systematic review and meta-analysis. Am J Prev Med. 2016;51(5):779-791. doi:10.1016/j.amepre.2016 .06.022 · DOI
  6. Holden DJ, Jonas DE, Porterfield DS, Reuland D, Harris R. Systematic review: enhancing the use and quality of colorectal cancer screening. Ann Intern Med. 2010;152(10):668-676. doi:10.7326/0003-4819-152 -10-201005180-00239 · DOI
  7. Sabatino SA, Lawrence B, Elder R, et al; Community Preventive Services Task Force. Effectiveness of interventions to increase screening for breast, cervical, and colorectal cancers: nine updated systematic reviews for the guide to community preventive services. Am J Prev Med. 2012;43(1):97-118. doi:10.1016/j.amepre.2012.04.009 · DOI
  8. Naylor K, Ward J, Polite BN. Interventions to improve care related to colorectal cancer among racial and ethnic minorities: a systematic review. J Gen Intern Med. 2012;27(8):1033-1046. doi:10 .1007/s11606-012-2044-2 · DOI
  9. Potter MB, Ackerson LM, Gomez V, et al. Effectiveness and reach of the FLU-FIT program in an integrated health care system: a multisite randomized trial. Am J Public Health. 2013;103(6): 1128-1133. doi:10.2105/AJPH.2012.300998 · DOI
  10. Potter MB, Phengrasamy L, Hudes ES, McPhee SJ, Walsh JM. Offering annual fecal occult blood tests at annual flu shot clinics increases colorectal cancer screening rates. Ann Fam Med. 2009;7(1): 17-23. doi:10.1370/afm.934 · DOI
  11. Potter MB, Walsh JM, Yu TM, Gildengorin G, Green LW, McPhee SJ. The effectiveness of the FLU-FOBT program in primary care: a randomized trial. Am J Prev Med. 2011;41(1):9-16. doi:10.1016/j .amepre.2011.03.011 · DOI
  12. Thompson NJ, Boyko EJ, Dominitz JA, et al. A randomized controlled trial of a clinic-based support staff intervention to increase the rate of fecal occult blood test ordering. Prev Med. 2000; 30(3):244-251. doi:10.1006/pmed.1999.0624 · DOI
  13. Tu SP, Taylor V, Yasui Y, et al. Promoting culturally appropriate colorectal cancer screening through a health educator: a randomized controlled trial. Cancer. 2006;107(5):959-966. doi:10.1002 /cncr.22091 2001;16(2):85-88. doi:10.1080 /08858190109528738 · DOI
  14. Lee JK, Reis V, Liu S, et al. Improving fecal occult blood testing compliance using a mailed educational reminder. J Gen Intern Med. 2009;24 (11):1192-1197. doi:10.1007/s11606-009-1087-5 · DOI
  15. Weinberg DS, Myers RE, Keenan E, et al. Genetic and environmental risk assessment and colorectal cancer screening in an average-risk population: a randomized trial. Ann Intern Med. 2014;161(8):537-545. doi:10.7326/M14-0765 · DOI
  16. Arnold CL, Rademaker A, Wolf MS, Liu D, Hancock J, Davis TC. Third annual fecal occult blood testing in community health clinics. Am J Health Behav. 2016;40(3):302-309. doi:10.5993/AJHB.40 .3.2 · DOI
  17. Green BB, Anderson ML, Chubak J, Fuller S, Meenan RT, Vernon SW. Impact of continued mailed fecal tests in the patient-centered medical home: year 3 of the Systems of Support to Increase Colon Cancer Screening and Follow-up randomized trial. Cancer. 2016;122(2):312-321. doi:10.1002/cncr.29734 · DOI
  18. Weinberg DS, Keenan E, Ruth K, Devarajan K, Rodoletz M, Bieber EJ. A randomized comparison of print and web communication on colorectal cancer screening. JAMA Intern Med. 2013;173(2):122-129. doi:10.1001/2013.jamainternmed.1017 · DOI
  19. Schroy PC III, Emmons KM, Peters E, et al. Aid-assisted decision making and colorectal cancer screening: a randomized controlled trial. Am J Prev Med. 2012;43(6):573-583. doi:10.1016/j.amepre .2012.08.018 · DOI
  20. Sequist TD, Zaslavsky AM, Colditz GA, Ayanian JZ. Electronic patient messages to promote colorectal cancer screening: a randomized controlled trial. Arch Intern Med. 2011;171(7):636-641. doi:10.1001/archinternmed.2010.467 · DOI
  21. Simon SR, Zhang F, Soumerai SB, et al. Failure of automated telephone outreach with speech recognition to improve colorectal cancer screening: a randomized controlled trial. Arch Intern Med. 2010;170(3):264-270. doi:10.1001/archinternmed .2009.522 · DOI
  22. Menon U, Belue R, Wahab S, et al. A randomized trial comparing the effect of two phone-based interventions on colorectal cancer screening adherence. Ann Behav Med. 2011;42(3): 294-303. doi:10.1007/s12160-011-9291-z · DOI
  23. Miller DP Jr, Spangler JG, Case LD, Goff DC Jr, Singh S, Pignone MP. Effectiveness of a web-based colorectal cancer screening patient decision aid: a randomized controlled trial in a mixed-literacy population. Am J Prev Med. 2011;40(6):608-615. doi:10.1016/j.amepre.2011.02.019 · DOI
  24. Mosen DM, Feldstein AC, Perrin N, et al. Automated telephone calls improved completion of fecal occult blood testing. Med Care. 2010;48(7): 604-610. doi:10.1097/MLR.0b013e3181dbdce7 · DOI
  25. Pignone M, Harris R, Kinsinger L. Videotape-based decision aid for colon cancer screening: a randomized, controlled trial. Ann Intern Med. 2000;133(10):761-769. doi:10.7326/0003 -4819-133-10-200011210-00008 · DOI
  26. Aragones A, Schwartz MD, Shah NR, Gany FM. A randomized controlled trial of a multilevel intervention to increase colorectal cancer screening among Latino immigrants in a primary care facility. J Gen Intern Med. 2010;25(6):564-567. doi:10.1007 /s11606-010-1266-4 · DOI
  27. Cameron KA, Persell SD, Brown T, Thompson J, Baker DW. Patient outreach to promote colorectal cancer screening among patients with an expired order for colonoscopy: a randomized controlled trial. Arch Intern Med. 2011;171(7):642-646. doi:10 .1001/archinternmed.2010.468
  28. Hoffman AS, Lowenstein LM, Kamath GR, et al. An entertainment-education colorectal cancer screening decision aid for African American patients: a randomized controlled trial. Cancer. 2017;123(8):1401-1408. doi:10.1002/cncr.30489 · DOI
  29. Ferron P, Asfour SS, Metsch LR, et al. Impact of a multifaceted intervention on promoting adherence to screening colonoscopy among persons in HIV primary care: a pilot study. Clin Transl Sci. 2015;8(4):290-297. doi:10.1111/cts.12276 · DOI
  30. Skinner CS, Halm EA, Bishop WP, et al. Impact of risk assessment and tailored versus nontailored risk information on colorectal cancer testing in primary care: a randomized controlled trial. Cancer Epidemiol Biomarkers Prev. 2015;24(10):1523-1530. doi:10.1158/1055-9965.EPI-15-0122 · DOI
  31. Krok-Schoen JL, Katz ML, Oliveri JM, et al. A media and clinic intervention to increase colorectal cancer screening in Ohio Appalachia. Biomed Res Int. 2015;2015:943152. doi:10.1155/2015 /943152 · DOI
  32. Potter MB, Namvargolian Y, Hwang J, Walsh JM. Improving colorectal cancer screening: a partnership between primary care practices and the American Cancer Society. J Cancer Educ. 2009; 24(1):22-27. doi:10.1080/08858190802665195 · DOI
  33. Cohen-Cline H, Wernli KJ, Bradford SC, Boles-Hall M, Grossman DC. Use of interactive voice response to improve colorectal cancer screening. Med Care. 2014;52(6):496-499. doi:10.1097/MLR .0000000000000116 · DOI
  34. Costanza ME, Luckmann R, Stoddard AM, et al. Using tailored telephone counseling to accelerate the adoption of colorectal cancer screening. Cancer Detect Prev. 2007;31(3):191-198. doi:10.1016/j.cdp .2007.04.008 · DOI
  35. Katz ML, Fisher JL, Fleming K, Paskett ED. Patient activation increases colorectal cancer screening rates: a randomized trial among low-income minority patients. Cancer Epidemiol Biomarkers Prev. 2012;21(1):45-52. doi:10.1158 /1055-9965.EPI-11-0815 · DOI
  36. Jerant A, Kravitz RL, Sohler N, et al. Sociopsychological tailoring to address colorectal cancer screening disparities: a randomized controlled trial. Ann Fam Med. 2014;12(3):204-214. doi:10.1370/afm.1623 · DOI
  37. Dolan JG, Frisina S. Randomized controlled trial of a patient decision aid for colorectal cancer screening. Med Decis Making. 2002;22(2):125-139. doi:10.1177/02729890222063017 · DOI
  38. Phillips L, Hendren S, Humiston S, Winters P, Fiscella K. Improving breast and colon cancer screening rates: a comparison of letters, automated phone calls, or both. J Am Board Fam Med. 2015;28 (1):46-54. doi:10.3122/jabfm.2015.01.140174 · DOI
  39. Fortuna RJ, Idris A, Winters P, et al. Get screened: a randomized trial of the incremental benefits of reminders, recall, and outreach on cancer screening. J Gen Intern Med. 2014;29(1): 90-97. doi:10.1007/s11606-013-2586-y · DOI
  40. Muller CJ, Robinson RF, Smith JJ, et al. Text message reminders increased colorectal cancer screening in a randomized trial with Alaska Native and American Indian people. Cancer. 2017;123(8): 1382-1389. doi:10.1002/cncr.30499 · DOI
  41. Chan EC, Vernon SW. Implementing an intervention to promote colon cancer screening through e-mail over the Internet: lessons learned from a pilot study. Med Care. 2008;46(9)(suppl 1): S117-S122. doi:10.1097/MLR.0b013e3181805e3c · DOI
  42. Gupta S, Miller S, Koch M, et al. Financial incentives for promoting colorectal cancer screening: a randomized, comparative effectiveness trial. Am J Gastroenterol. 2016;111(11): 1630-1636. doi:10.1038/ajg.2016.286 · DOI
  43. Kullgren JT, Dicks TN, Fu X, et al. Financial incentives for completion of fecal occult blood tests among veterans: a 2-stage, pragmatic, cluster, randomized, controlled trial. Ann Intern Med. 2014; 161(10)(suppl):S35-S43. doi:10.7326/M13-3015 · DOI
  44. Inadomi JM, Vijan S, Janz NK, et al. Adherence to colorectal cancer screening: a randomized clinical trial of competing strategies. Arch Intern Med. 2012;172(7):575-582. doi:10.1001/archinternmed .2012.332 · DOI
  45. Liang PS, Wheat CL, Abhat A, et al. Adherence to competing strategies for colorectal cancer screening over 3 years. Am J Gastroenterol. 2016;111 (1):105-114. doi:10.1038/ajg.2015.367 · DOI
  46. Chubak J, Bogart A, Fuller S, Laing SS, Green BB. Uptake and positive predictive value of fecal occult blood tests: a randomized controlled trial. Prev Med. 2013;57(5):671-678. doi:10.1016/j.ypmed .2013.08.032 · DOI
  47. Hoffman RM, Steel S, Yee EF, Massie L, Schrader RM, Murata GH. Colorectal cancer screening adherence is higher with fecal immunochemical tests than guaiac-based fecal occult blood tests: a randomized, controlled trial. Prev Med. 2010;50(5-6):297-299. doi:10.1016/j .ypmed.2010.03.010 · DOI
  48. Mosen DM, Liles EG, Feldstein AC, et al. Participant uptake of the fecal immunochemical test decreases with the two-sample regimen compared with one-sample FIT. Eur J Cancer Prev. 2014;23(6):516-523. doi:10.1097/CEJ .0000000000000084 · DOI
  49. Roetzheim RG, Christman LK, Jacobsen PB, et al. A randomized controlled trial to increase cancer screening among attendees of community health centers. Ann Fam Med. 2004;2(4):294-300. doi:10.1370/afm.101 · DOI
  50. Goldberg D, Schiff GD, McNutt R, Furumoto-Dawson A, Hammerman M, Hoffman A. Mailings timed to patients' appointments: a controlled trial of fecal occult blood test cards. Am J Prev Med. 2004;26(5):431-435. doi:10.1016/j .amepre.2004.02.009 · DOI
  51. Ganz PA, Farmer MM, Belman MJ, et al. Results of a randomized controlled trial to increase colorectal cancer screening in a managed care health plan. Cancer. 2005;104(10):2072-2083. doi:10.1002/cncr.21434 103. · DOI
  52. Humphrey LL, Shannon J, Partin MR, O'Malley J, Chen Z, Helfand M. Improving the follow-up of positive hemoccult screening tests: an electronic intervention. J Gen Intern Med. 2011;26(7):691-697. doi:10.1007/s11606-011-1639-3 104. · DOI
  53. Green BB, Anderson ML, Wang CY, et al. Results of nurse navigator follow-up after positive colorectal cancer screening test: a randomized trial. J Am Board Fam Med. 2014;27(6):789-795. doi:10 .3122/jabfm.2014.06.140125 105. Raich PC, Whitley EM, Thorland W, Valverde P, Fairclough D; Denver Patient Navigation Research Program. Patient navigation improves cancer diagnostic resolution: an individually randomized clinical trial in an underserved population. Cancer Epidemiol Biomarkers Prev. 2012;21(10):1629-1638. doi:10.1158/1055-9965.EPI-12-0513 106. · DOI
  54. Myers RE, Turner B, Weinberg D, et al. Impact of a physician-oriented intervention on follow-up in colorectal cancer screening. Prev Med. 2004;38 (4):375-381. doi:10.1016/j.ypmed.2003.11.010 107. · DOI
  55. Walsh JM, Salazar R, Terdiman JP, Gildengorin G, Pérez-Stable EJ. Promoting use of colorectal cancer screening tests: can we change physician behavior? J Gen Intern Med. 2005;20(12):1097-1101. doi:10.1111/j.1525-1497.2005.0245.x 108. Singal AG, Gupta S, Skinner CS, et al. Effect of colonoscopy outreach vs fecal immunochemical test outreach on colorectal cancer screening completion: a randomized clinical trial. JAMA. 2017; 318(9):806-815. doi:10.1001/jama.2017.11389 109. Lipkus IM, Skinner CS, Dement J, et al. Increasing colorectal cancer screening among individuals in the carpentry trade: test of risk communication interventions. Prev Med. 2005;40 (5):489-501. doi:10.1016/j.ypmed.2004.09.019 110. Ruffin MT IV, Gorenflo DW. Interventions fail to increase cancer screening rates in community-based primary care practices. Prev Med. 2004;39(3):435-440. doi:10.1016/j.ypmed.2004.04 .055 111. Roetzheim RG, Christman LK, Jacobsen PB, Schroeder J, Abdulla R, Hunter S. Long-term results from a randomized controlled trial to increase cancer screening among attendees of community health centers. Ann Fam Med. 2005;3(2):109-114. doi:10.1370/afm.240 112. Ornstein S, Nemeth LS, Jenkins RG, Nietert PJ. Colorectal cancer screening in primary care: translating research into practice. Med Care. 2010; 48(10):900-906. doi:10.1097/MLR .0b013e3181ec5591 113. Ferreira MR, Dolan NC, Fitzgibbon ML, et al. Health care provider-directed intervention to increase colorectal cancer screening among veterans: results of a randomized controlled trial. J Clin Oncol. 2005;23(7):1548-1554. doi:10.1200 /JCO.2005.07.049 114. · DOI
  56. Dignan M, Shelton B, Slone SA, et al. Effectiveness of a primary care practice intervention for increasing colorectal cancer screening in Appalachian Kentucky. Prev Med. 2014; 58:70-74. doi:10.1016/j.ypmed.2013.10.018 115. National Cancer Institute. Research-tested interventions programs: moving from research to programs for people. http://rtips.cancer.gov/rtips. Accessed March 7, 2018. 116. Selby K, Baumgartner C, Levin TR, et al. Interventions to improve follow-up of positive results on fecal blood tests: a systematic review. Ann Intern Med. 2017;167(8):565-575. doi:10.7326 /M17-1361 117. · DOI
  57. Davis MM, Freeman M, Shannon J, et al. A systematic review of clinic and community intervention to increase fecal testing for colorectal cancer in rural and low-income populations in the United States-how, what and when? BMC Cancer. 2018;18(1):40. doi:10.1186/s12885-017-3813-4 · DOI

Cited by

Sorted by citations

Authors
Dougherty, M. K., Brenner, A. T., Crockett, S. D., Gupta, S., Wheeler, S. B., Coker-Schwimmer, M., Cubillos, L., Malo, T., & Reuland, D. S.
Affiliations
  • University of North Carolina at Chapel Hill (US)
  • Icahn School of Medicine at Mount Sinai (US)
Corresponding author
Reuland, Daniel S.
Venue
JAMA Internal Medicine
Published
2018-12-01
Volume
178
Issue
12
Pages
1645
ISSN
2168-6106 (ISSN-L)
OpenAlex
W2897894473
Cited by
362
References
3
Citations by year
2026: 53 · 2025: 44 · 2024: 51 · 2023: 58 · 2022: 39 · 2021: 51 · 2020: 44 · 2019: 19 · 2018: 1
FWCI
3.00
Type
journal article
Language
en
Open access
Locations
  • JAMA Internal Medicine (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • National Institutes of Health (KL2TR001109)
  • National Cancer Institute (P30CA016086)
  • National Institute of Diabetes and Digestive and Kidney Diseases (T32DK007634)
  • National Center for Advancing Translational Sciences
Topics
  • Health Sciences › Medicine › Oncology › Colorectal Cancer Screening and Detection
  • Health Sciences › Medicine › Oncology › Global Cancer Incidence and Screening
  • Health Sciences › Medicine › Oncology › Colorectal Cancer Surgical Treatments
Keywords
colorectal cancer screening, screening completion, screening interventions, patient navigation, patient education, patient reminders, academic detailing, colonoscopy, effect size, risk of bias, quality improvement, health disparities, health equity, low-income populations, rural population, racial and ethnic minorities
MeSH terms
Humans, United States, Colorectal Neoplasms, Early Detection of Cancer

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review