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

JAMA Internal Medicine

Volumn 178, Issue 12, 2018, Pages 1645-1658

  Dougherty, Michael K ^a   Brenner, Alison T ^b   Crockett, Seth D ^a   Gupta, Shivani ^c   Wheeler, Stephanie B ^b,d   Coker Schwimmer, Manny ^b   Cubillos, Laura ^b   Malo, Teri ^b   Reuland, Daniel S ^a,b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^d University of North Carolina at Chapel Hill   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; ATTRIBUTABLE RISK; BLOOD ANALYSIS; CANCER MORTALITY; CANCER RISK; CANCER SCREENING; CLINICAL OUTCOME; COLONOSCOPY; COLORECTAL CANCER; COST EFFECTIVENESS ANALYSIS; DATA ANALYSIS; DATA EXTRACTION; DATA SYNTHESIS; ELECTRONIC MEDICAL RECORD; FECES ANALYSIS; FOLLOW UP; HEALTH CARE COST; HEALTH CARE SYSTEM; HUMAN; INFLUENZA VACCINATION; MEDICAL INFORMATICS; META ANALYSIS; OCCULT BLOOD; OCCULT BLOOD TEST; OUTCOME ASSESSMENT; PATIENT EDUCATION; PREFERRED REPORTING ITEMS FOR SYSTEMATIC REVIEWS AND META-ANALYSES; RANDOMIZED CONTROLLED TRIAL (TOPIC); RISK ASSESSMENT; SCREENING TEST; SENSITIVITY ANALYSIS; SIGMOIDOSCOPY; SYNTHESIS; SYSTEMATIC REVIEW; UNITED STATES; COLORECTAL TUMOR; EARLY CANCER DIAGNOSIS;

COLORECTAL NEOPLASMS; EARLY DETECTION OF CANCER; HUMANS; UNITED STATES;

EID: 85054881302     PISSN: 21686106     EISSN: 21686114     Source Type: Journal    
DOI: 10.1001/jamainternmed.2018.4637     Document Type: Article

References (117)

1. National Cancer Institute. Cancer stat facts: colorectal cancer; 2017. https://seer.cancer.gov/statfacts/html/colorect.html. Accessed June 11, 2017
2. Bibbins-Domingo K, Grossman DC, Curry SJ,; US Preventive Services Task Force. Screening for colorectal cancer: US Preventive Services Task Force recommendation statement. JAMA. 2016; 315 (23): 2564-2575. doi: 10.1001/jama.2016.5989 27304597
3. 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 24922745
4. 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 25984847
5. Rex DK, Boland CR, Dominitz JA, 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 28600070
6. Siegel RL, Miller KD, Fedewa SA, Colorectal cancer statistics, 2017. CA Cancer J Clin. 2017; 67 (3): 177-193. doi: 10.3322/caac.21395 28248415
7. National Colorectal Cancer Roundtable. Working toward the shared goal of 80% screened for colorectal cancer by 2018. http://nccrt.org/tools/80-percent-by-2018/. Accessed June 11, 2016
8. Volk RJ, Linder SK, Lopez-Olivo MA, 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 27593418
9. 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 20388703
10. Sabatino SA, Lawrence B, Elder R,; 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 22704754
11. 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 22798214
12. Moher D, Liberati A, Tetzlaff J, Altman DG; PRISMA Group. Preferred Reporting Items for Systematic Reviews and Meta-analyses: the PRISMA statement. Ann Intern Med. 2009; 151 (4): 264-269, W64. doi: 10.7326/0003-4819-151-4-200908180-00135 19622511
13. US Community Preventive Services Task Force. Increasing colorectal cancer screening: multicomponent interventions. Task Force findings and rationale statement. https://www.thecommunityguide.org/sites/default/files/assets/Cancer-Screening-Multicomponent-Colorectal.pdf. Updated June 19, 2018. Accessed September 25, 2017
14. Potter MB, Ackerson LM, Gomez V, 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 23597357
15. 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 19139445
16. 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 21665058
17. Thompson NJ, Boyko EJ, Dominitz JA, 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 10684748
18. Tu SP, Taylor V, Yasui Y, 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 16865681
19. Singal AG, Gupta S, Tiro JA, Outreach invitations for FIT and colonoscopy improve colorectal cancer screening rates: a randomized controlled trial in a safety-net health system. Cancer. 2016; 122 (3): 456-463. doi: 10.1002/cncr.29770 26535565
20. Goldman SN, Liss DT, Brown T, Comparative effectiveness of multifaceted outreach to initiate colorectal cancer screening in community health centers: a randomized controlled trial. J Gen Intern Med. 2015; 30 (8): 1178-1184. doi: 10.1007/s11606-015-3234-5 25814264
21. Gupta S, Halm EA, Rockey DC, 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. 2013; 173 (18): 1725-1732. doi: 10.1001/jamainternmed.2013.9294 23921906
22. Hendren S, Winters P, Humiston S, Randomized, controlled trial of a multimodal intervention to improve cancer screening rates in a safety-net primary care practice. J Gen Intern Med. 2014; 29 (1): 41-49. doi: 10.1007/s11606-013-2506-1 23818159
23. Green BB, Wang CY, Anderson ML, An automated intervention with stepped increases in support to increase uptake of colorectal cancer screening: a randomized trial. Ann Intern Med. 2013; 158 (5, pt 1): 301-311. doi: 10.7326/0003-4819-158-5-201303050-00002 23460053
24. Myers RE, Bittner-Fagan H, Daskalakis C, A randomized controlled trial of a tailored navigation and a standard intervention in colorectal cancer screening. Cancer Epidemiol Biomarkers Prev. 2013; 22 (1): 109-117. doi: 10.1158/1055-9965.EPI-12-0701 23118143
25. Jean-Jacques M, Kaleba EO, Gatta JL, Gracia G, Ryan ER, Choucair BN. Program to improve colorectal cancer screening in a low-income, racially diverse population: a randomized controlled trial. Ann Fam Med. 2012; 10 (5): 412-417. doi: 10.1370/afm.1381 22966104
26. Levy BT, Xu Y, Daly JM, Ely JW. A randomized controlled trial to improve colon cancer screening in rural family medicine: an Iowa Research Network (IRENE) study. J Am Board Fam Med. 2013; 26 (5): 486-497. doi: 10.3122/jabfm.2013.05.130041 24004700
27. Coronado GD, Golovaty I, Longton G, Levy L, Jimenez R. Effectiveness of a clinic-based colorectal cancer screening promotion program for underserved Hispanics. Cancer. 2011; 117 (8): 1745-1754. doi: 10.1002/cncr.25730 21472722
28. Sequist TD, Zaslavsky AM, Marshall R, Fletcher RH, Ayanian JZ. Patient and physician reminders to promote colorectal cancer screening: a randomized controlled trial. Arch Intern Med. 2009; 169 (4): 364-371. doi: 10.1001/archinternmed.2008.564 19237720
29. Myers RE, Sifri R, Hyslop T, A randomized controlled trial of the impact of targeted and tailored interventions on colorectal cancer screening. Cancer. 2007; 110 (9): 2083-2091. doi: 10.1002/cncr.23022 17893869
30. Fiscella K, Humiston S, Hendren S, A multimodal intervention to promote mammography and colorectal cancer screening in a safety-net practice. J Natl Med Assoc. 2011; 103 (8): 762-768. doi: 10.1016/S0027-9684(15)30417-X 22046855
31. Charlton ME, Mengeling MA, Halfdanarson TR, Evaluation of a home-based colorectal cancer screening intervention in a rural state. J Rural Health. 2014; 30 (3): 322-332. doi: 10.1111/jrh.12052 24164375
32. Ling BS, Schoen RE, Trauth JM, Physicians encouraging colorectal screening: a randomized controlled trial of enhanced office and patient management on compliance with colorectal cancer screening. Arch Intern Med. 2009; 169 (1): 47-55. doi: 10.1001/archinternmed.2008.519 19139323
33. Dietrich AJ, Tobin JN, Cassells A, Telephone care management to improve cancer screening among low-income women: a randomized, controlled trial. Ann Intern Med. 2006; 144 (8): 563-571. doi: 10.7326/0003-4819-144-8-200604180-00006 16618953
34. Dietrich AJ, Tobin JN, Robinson CM, Telephone outreach to increase colon cancer screening in Medicaid managed care organizations: a randomized controlled trial. Ann Fam Med. 2013; 11 (4): 335-343. doi: 10.1370/afm.1469 23835819
35. Dietrich AJ, Tobin JN, Cassells A, Translation of an efficacious cancer-screening intervention to women enrolled in a Medicaid managed care organization. Ann Fam Med. 2007; 5 (4): 320-327. doi: 10.1370/afm.701 17664498
36. Percac-Lima S, Grant RW, Green AR, A culturally tailored navigator program for colorectal cancer screening in a community health center: a randomized, controlled trial. J Gen Intern Med. 2009; 24 (2): 211-217. doi: 10.1007/s11606-008-0864-x 19067085
37. Percac-Lima S, Ashburner JM, Zai AH, Patient navigation for comprehensive cancer screening in high-risk patients using a population-based health information technology system: a randomized clinical trial. JAMA Intern Med. 2016; 176 (7): 930-937. doi: 10.1001/jamainternmed.2016.0841 27273602
38. Basch CE, Zybert P, Wolf RL, A randomized trial to compare alternative educational interventions to increase colorectal cancer screening in a hard-to-reach urban minority population with health insurance. J Community Health. 2015; 40 (5): 975-983. doi: 10.1007/s10900-015-0021-5 25850386
39. Basch CE, Wolf RL, Brouse CH, Telephone outreach to increase colorectal cancer screening in an urban minority population. Am J Public Health. 2006; 96 (12): 2246-2253. doi: 10.2105/AJPH.2005.067223 17077394
40. Lasser KE, Murillo J, Lisboa S, Colorectal cancer screening among ethnically diverse, low-income patients: a randomized controlled trial. Arch Intern Med. 2011; 171 (10): 906-912. doi: 10.1001/archinternmed.2011.201 21606094
41. Reuland DS, Brenner AT, Hoffman R, Effect of combined patient decision aid and patient navigation vs usual care for colorectal cancer screening in a vulnerable patient population: a randomized clinical trial. JAMA Intern Med. 2017; 177 (7): 967-974. doi: 10.1001/jamainternmed.2017.1294 28505217
42. Baker DW, Brown T, Buchanan DR, Comparative effectiveness of a multifaceted intervention to improve adherence to annual colorectal cancer screening in community health centers: a randomized clinical trial. JAMA Intern Med. 2014; 174 (8): 1235-1241. doi: 10.1001/jamainternmed.2014.2352 24934845
43. DeGroff A, Schroy PC III, Morrissey KG, Patient navigation for colonoscopy completion: results of an RCT. Am J Prev Med. 2017; 53 (3): 363-372. doi: 10.1016/j.amepre.2017.05.010 28676254
44. Wells KJ, Battaglia TA, Dudley DJ,; Patient Navigation Research Program. Patient navigation: state of the art or is it science? Cancer. 2008; 113 (8): 1999-2010. doi: 10.1002/cncr.23815 18780320
45. Davis TC, Arnold CL, Bennett CL, Strategies to improve repeat fecal occult blood testing cancer screening. Cancer Epidemiol Biomarkers Prev. 2014; 23 (1): 134-143. doi: 10.1158/1055-9965.EPI-13-0795 24192009
46. Braschi CD, Sly JR, Singh S, Villagra C, Jandorf L. Increasing colonoscopy screening for Latino Americans through a patient navigation model: a randomized clinical trial. J Immigr Minor Health. 2014; 16 (5): 934-940. doi: 10.1007/s10903-013-9848-y 23736964
47. Atlas SJ, Zai AH, Ashburner JM, Non-visit-based cancer screening using a novel population management system. J Am Board Fam Med. 2014; 27 (4): 474-485. doi: 10.3122/jabfm.2014.04.130319 25002002
48. Jandorf L, Braschi C, Ernstoff E, Culturally targeted patient navigation for increasing African Americans' adherence to screening colonoscopy: a randomized clinical trial. Cancer Epidemiol Biomarkers Prev. 2013; 22 (9): 1577-1587. doi: 10.1158/1055-9965.EPI-12-1275 23753039
49. Greiner KA, Daley CM, Epp A, Implementation intentions and colorectal screening: a randomized trial in safety-net clinics. Am J Prev Med. 2014; 47 (6): 703-714. doi: 10.1016/j.amepre.2014.08.005 25455115
50. Miller DP Jr, Kimberly JR, Case LD, Wofford JL. Using a computer to teach patients about fecal occult blood screening: a randomized trial. J Gen Intern Med. 2005; 20 (11): 984-988. doi: 10.1111/j.1525-1497.2005.0081.x 16307621
51. Stokamer CL, Tenner CT, Chaudhuri J, Vazquez E, Bini EJ. Randomized controlled trial of the impact of intensive patient education on compliance with fecal occult blood testing. J Gen Intern Med. 2005; 20 (3): 278-282. doi: 10.1111/j.1525-1497.2005.40023.x 15836533
52. Wilkins T, Gillies RA, Panchal P, Patel M, Warren P, Schade RR. Colorectal cancer risk information presented by a nonphysician assistant does not increase screening rates. Can Fam Physician. 2014; 60 (8): 731-738. 25122819
53. Davis SN, Christy SM, Chavarria EA, A randomized controlled trial of a multicomponent, targeted, low-literacy educational intervention compared with a nontargeted intervention to boost colorectal cancer screening with fecal immunochemical testing in community clinics. Cancer. 2017; 123 (8): 1390-1400. doi: 10.1002/cncr.30481 27906448
54. Denberg TD, Coombes JM, Byers TE, Effect of a mailed brochure on appointment-keeping for screening colonoscopy: a randomized trial. Ann Intern Med. 2006; 145 (12): 895-900. doi: 10.7326/0003-4819-145-12-200612190-00006 17179058
55. Friedman LC, Everett TE, Peterson L, Ogbonnaya KI, Mendizabal V. Compliance with fecal occult blood test screening among low-income medical outpatients: a randomized controlled trial using a videotaped intervention. J Cancer Educ. 2001; 16 (2): 85-88. doi: 10.1080/08858190109528738 11440068
56. Lee JK, Reis V, Liu S, 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 19774423
57. Weinberg DS, Myers RE, Keenan E, 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 25329201
58. 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 27103409
59. 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 26488332
60. 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 23128366
61. Schroy PC III, Emmons KM, Peters E, 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 23159252
62. 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 21149743
63. Simon SR, Zhang F, Soumerai SB, 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 20142572
64. Menon U, Belue R, Wahab S, 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 21826576
65. 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 21565651
66. Mosen DM, Feldstein AC, Perrin N, Automated telephone calls improved completion of fecal occult blood testing. Med Care. 2010; 48 (7): 604-610. doi: 10.1097/MLR.0b013e3181dbdce7 20508529
67. 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 11085838
68. Vernon SW, Bartholomew LK, McQueen A, A randomized controlled trial of a tailored interactive computer-delivered intervention to promote colorectal cancer screening: sometimes more is just the same. Ann Behav Med. 2011; 41 (3): 284-299. doi: 10.1007/s12160-010-9258-5 21271365
69. 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 20213208
70. 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 21149742
71. Hoffman AS, Lowenstein LM, Kamath GR, 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 28001305
72. Ferron P, Asfour SS, Metsch LR, 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 25996255
73. Skinner CS, Halm EA, Bishop WP, 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 26265201
74. Krok-Schoen JL, Katz ML, Oliveri JM, A media and clinic intervention to increase colorectal cancer screening in Ohio Appalachia. Biomed Res Int. 2015; 2015: 943152. doi: 10.1155/2015/943152 26509172
75. 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 19259861
76. 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 24638119
77. Costanza ME, Luckmann R, Stoddard AM, 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 17646058
78. 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 22068288
79. Jerant A, Kravitz RL, Sohler N, 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 24821891
80. 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 11958495
81. 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 25567822
82. Fortuna RJ, Idris A, Winters P, 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 24002626
83. Muller CJ, Robinson RF, Smith JJ, 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 28001304
84. 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 18725823
85. Gupta S, Miller S, Koch M, 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 27481306
86. Kullgren JT, Dicks TN, Fu X, 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 25402401
87. Inadomi JM, Vijan S, Janz NK, 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 22493463
88. Liang PS, Wheat CL, Abhat A, 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 26526080
89. 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 24029556
90. 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 20307568
91. Mosen DM, Liles EG, Feldstein AC, 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 25203483
92. Roetzheim RG, Christman LK, Jacobsen PB, 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 15335126
93. 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 15165660
94. Ganz PA, Farmer MM, Belman MJ, 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 16216030
95. Ford ME, Havstad S, Vernon SW, Enhancing adherence among older African American men enrolled in a longitudinal cancer screening trial. Gerontologist. 2006; 46 (4): 545-550. 16921009
96. Christie J, Itzkowitz S, Lihau-Nkanza I, Castillo A, Redd W, Jandorf L. A randomized controlled trial using patient navigation to increase colonoscopy screening among low-income minorities. J Natl Med Assoc. 2008; 100 (3): 278-284. 18390020
97. Muller D, Logan J, Dorr D, Mosen D. The effectiveness of a secure email reminder system for colorectal cancer screening. In: AMIA Annual Symposium Proceedings, 2009. American Medical Informatics Association, November 18, 2009;457
98. Price-Haywood EG, Harden-Barrios J, Cooper LA. Comparative effectiveness of audit-feedback versus additional physician communication training to improve cancer screening for patients with limited health literacy. J Gen Intern Med. 2014; 29 (8): 1113-1121. 24590734
99. Shankaran V, Luu TH, Nonzee N, Costs and cost effectiveness of a health care provider-directed intervention to promote colorectal cancer screening. J Clin Oncol. 2009; 27 (32): 5370-5375. doi: 10.1200/JCO.2008.20.6458 19826133
100. Shaw EK, Ohman-Strickland PA, Piasecki A, Effects of facilitated team meetings and learning dcollaboratives on colorectal cancer screening rates in primary care practices: a cluster randomized trial. Ann Fam Med. 2013; 11 (3): 220-228, S1-S8. doi: 10.1370/afm.1505 23690321
101. Wells KJ, Lee JH, Calcano ER, A cluster randomized trial evaluating the efficacy of patient navigation in improving quality of diagnostic care for patients with breast or colorectal cancer abnormalities. Cancer Epidemiol Biomarkers Prev. 2012; 21 (10): 1664-1672. doi: 10.1158/1055-9965.EPI-12-0448 23045541
102. Paskett ED, Katz ML, Post DM,; Ohio Patient Navigation Research Program. The Ohio Patient Navigation Research Program: does the American Cancer Society patient navigation model improve time to resolution in patients with abnormal screening tests? Cancer Epidemiol Biomarkers Prev. 2012; 21 (10): 1620-1628. doi: 10.1158/1055-9965.EPI-12-0523 23045536
103. 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 21327529
104. Green BB, Anderson ML, Wang CY, 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 25381076
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 23045537
106. Myers RE, Turner B, Weinberg D, 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 15020170
107. 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 16423097
108. Singal AG, Gupta S, Skinner CS, 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 28873161
109. Lipkus IM, Skinner CS, Dement J, 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 15749130
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 15313081
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 15798035
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 20808257
113. Ferreira MR, Dolan NC, Fitzgibbon ML, 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 15735130
114. Dignan M, Shelton B, Slone SA, 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 24212061
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, 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 29049756
117. Davis MM, Freeman M, Shannon J, 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 29304835