Abstract
We conducted a systematic review and a meta-analysis of observational studies to identify and summarise the level of colorectal cancer (CRC) screening participation for people at increased risk due to family history of the disease. Medline, Cinhal, Embase and PsychInfo databases were comprehensively searched between January 1995 and May 2012 to identify relevant articles. To be included, studies had to report on screening for people who had at least one first-degree relative with CRC and no previous personal diagnosis of the disease. Pooled screening participation levels were calculated for each screening modality. Seventeen studies, accounting for a total of 13,269 subjects with a family history of CRC met the inclusion criteria. Seven studies, including a total of 6,901 subjects had a pooled faecal occult blood testing screening participation (at least once) of 25 % (95 % CI 12–38). Five studies including a total of 5,091 subjects had a pooled sigmoidoscopy-based screening participation (at least once) of 16 % (95 % CI 7–27). Seven studies including a total of 9,965 subjects had pooled participation colonoscopy-based screening (at least once) of 40 % (95 % CI 26–54). There was a significant level of screening heterogeneity between studies. This review identified a substantial underuse of CRC screening for people at increased risk of developing the disease. It highlights the potential opportunity that exists for increasing screening participation among this segment of the population and the need to adjust the current CRC screening policies towards that objective.
Similar content being viewed by others
References
Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM (2010) Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 127(12):2893–2917. doi:10.1002/ijc.25516
Baglietto L, Jenkins MA, Severi G et al (2006) Measures of familial aggregation depend on definition of family history: meta-analysis for colorectal cancer. J Clin Epidemiol 59(2):114–124. doi:10.1016/j.jclinepi.2005.07.018
Johns LE, Houlston RS (2001) A systematic review and meta-analysis of familial colorectal cancer risk. Am J Gastroenterol 96(10):2992–3003. doi:10.1016/S0002-9270%2801%2903239-7
Taylor DP, Burt RW, Williams MS, Haug PJ, Cannon-Albright LA (2010) Population-based family history-specific risks for colorectal cancer: a constellation approach. Gastroenterology 138(3):877–885
Aaltonen L, Johns L, Jarvinen H, Mecklin JP, Houlston R (2007) Explaining the familial colorectal cancer risk associated with mismatch repair (MMR)-deficient and MMR-stable tumors. Clin Cancer Res 13(1):356–361. doi:10.1158/1078-0432.CCR-06-1256
Hampel H, Frankel WL, Martin E et al (2008) Feasibility of screening for Lynch syndrome among patients with colorectal cancer. J Clin Oncol 26(35):5783–5788. doi:10.1200/JCO.2008.17.5950
Jasperson KW, Tuohy TM, Neklason DW, Burt RW (2010) Hereditary and familial colon cancer. Gastroenterology 138(6):2044–2058. doi:10.1053/j.gastro.2010.01.054
Samowitz WS, Curtin K, Lin HH et al (2001) The colon cancer burden of genetically defined hereditary nonpolyposis colon cancer. Gastroenterology 121(4):830–838
Carstensen B, Soll-Johanning H, Villadsen E, Sondergaard JO, Lynge E (1996) Familial aggregation of colorectal cancer in the general population. Int J Cancer 68(4):428–435. doi:10.1002/(SICI)1097-0215(19961115)68:4<428:AID-IJC5>3.0.CO;2-2
Macklin MT (1960) Inheritance of cancer of the stomach and large intestine in man. J Natl Cancer Inst 24:551–571
St John DJ, McDermott FT, Hopper JL, Debney EA, Johnson WR, Hughes ES (1993) Cancer risk in relatives of patients with common colorectal cancer. Ann Intern Med 118(10):785–790
Hardcastle JD, Chamberlain JO, Robinson MH et al (1996) Randomised controlled trial of faecal-occult-blood screening for colorectal cancer. Lancet 348(9040):1472–1477. doi:10.1016/S0140-6736(96)03386-7
Kronborg O, Fenger C, Olsen J, Jorgensen OD, Sondergaard O (1996) Randomised study of screening for colorectal cancer with faecal-occult-blood test. Lancet 348(9040):1467–1471. doi:10.1016/S0140-6736(96)03430-7
Mandel JS, Bond JH, Church TR et al (1993) Reducing mortality from colorectal cancer by screening for fecal occult blood. Minnesota Colon Cancer Control Study. N Engl J Med 328(19):1365–1371. doi:10.1056/NEJM199305133281901
Bradshaw N, Holloway S, Penman I, Dunlop MG, Porteous MEM (2003) Colonoscopy surveillance of individuals at risk of familial colorectal cancer. Gut 52(12):1748–1751. doi:10.1136/gut.52.12.1748
Screening for colorectal cancer: U.S. Preventive Services Task Force recommendation statement (2008). Ann Intern Med 149(9):627–637
Cairns SR, Scholefield JH, Steele RJ et al (2010) Guidelines for colorectal cancer screening and surveillance in moderate and high risk groups (update from 2002). Gut 59(5):666–689. doi:10.1136/gut.2009.179804
Levin B, Lieberman DA, McFarland B et al (2008) 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. CA Cancer J Clin 58(3):130–160. doi:10.3322/CA.2007.0018
Rees G, Martin PR, Macrae FA (2008) Screening participation in individuals with a family history of colorectal cancer: a review. Eur J Cancer Care (Engl) 17(3):221–232. doi:10.1111/j.1365-2354.2007.00834.x
Mills EJ, Nachega JB, Buchan I et al (2006) Adherence to antiretroviral therapy in sub-Saharan Africa and North America: a meta-analysis. JAMA, J Am Med Assoc 296(6):679–690. doi:10.1001/jama.296.6.679
Stasi R, Sarpatwari A, Segal JB et al (2009) Effects of eradication of Helicobacter pylori infection in patients with immune thrombocytopenic purpura: a systematic review. Blood 113(6):1231–1240. doi:10.1182/blood-2008-07-167155
Liljegren A, Lindgren G, Brandberg Y et al (2004) Individuals with an increased risk of colorectal cancer: perceived benefits and psychological aspects of surveillance by means of regular colonoscopies. J Clin Oncol 22(9):1736–1742
Higgins JP, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21(11):1539–1558. doi:10.1002/sim.1186
Ait Ouakrim D, Boussioutas A, Lockett T et al (2012) Screening practices of unaffected people at familial risk of colorectal cancer. Cancer Prev Res (Phila) 5(2):240–247. doi:10.1158/1940-6207.CAPR-11-0229
Clavel-Chapelon F, Joseph R, Goulard H (1999) Surveillance behavior of women with a reported family history of colorectal cancer. Prev Med 28(2):174–178
Cockburn J, Paul C, Tzelepis F, McElduff P, Byles J (2002) Screening for bowel cancer among NSW adults with varying levels of risk: a community survey, 3 edn. The Cancer Council NSW Cancer Education Research Program, School of Medical Practice and Population Health, University of Newcastle, Wallsend, New South Wales. jillc@mail.newcastle.edu.au, pp 236–41
Codori AM, Petersen GM, Miglioretti DL, Boyd P (2001) Health beliefs and endoscopic screening for colorectal cancer: potential for cancer prevention. Prev Med 33(2 Pt 1):128–136. doi:10.1006/pmed.2001.0862
Courtney RJ, Paul CL, Sanson-Fisher RW et al (2012) Colorectal cancer screening in Australia: a community-level perspective. Med J Aust 196(8):516–520
Eisinger F, Giordanella JP, Didelot R et al (1996) Screening practices and familial antecedents of colorectal cancer. Survey with a voluntary population. [French]. Gastroenterol Clin Biol 20(8–9):627–632
Fletcher RH, Lobb R, Bauer MR et al (2007) Screening patients with a family history of colorectal cancer. J Gen Intern Med 22(4):508–513
Griffith KA, McGuire DB, Royak-Schaler R, Plowden KO, Steinberger EK (2008) Influence of family history and preventive health behaviors on colorectal cancer screening in African Americans. Cancer 113(2):276–285
Harris MA, Byles JE (1997) A survey of screening compliance among first degree relatives of people with colon cancer in New South Wales. J Med Screen 4(1):29–34
Mack LA, Cook LS, Temple WJ, Carlson LE, Hilsden RJ, Paolucci EO (2009) Colorectal cancer screening among first-degree relatives of colorectal cancer patients: benefits and barriers. Ann Surg Oncol 16(8):2092–2100. doi:10.1245/s10434-009-0528-z
Madlensky L, Esplen MJ, Gallinger S, McLaughlin JR, Goel V (2003) Relatives of colorectal cancer patients: factors associated with screening behavior. Am J Prev Med 25(3):187–194
Manne S, Markowitz A, Winawer S et al (2002) Correlates of colorectal cancer screening compliance and stage of adoption among siblings of individuals with early onset colorectal cancer. Health Psychol 21(1):3–15
Murff HJ, Peterson NB, Fowke JH et al (2008) Colonoscopy screening in African Americans and Whites with affected first-degree relatives. Arch Intern Med 168(6):625–631
Richardson JL, Danley K, Mondrus GT, Deapen D, Mack T (1995) Adherence to screening examinations for colorectal cancer after diagnosis in a first-degree relative. Prev Med 24(2):166–170
Shah M, Zhu K, Palmer RC, Jatoi I, Shriver C, Wu H (2007) Breast, colorectal, and skin cancer screening practices and family history of cancer in U.S. women. J Womens Health 16(4):526–534
Shah M, Zhu K, Palmer RC, Wu H (2007) Family history of cancer and utilization of prostate, colorectal and skin cancer screening tests in U.S. men. Prev Med 44(5):459–464
Thrasher JF, Cummings KM, Michalek AM, Mahoney MC, Moysich KB, Pillittere DM (2002) Colorectal cancer screening among individuals with and without a family history. J Publ Health Manag Pract JPHMP 8(2):1–9
Vernon SW, Briss PA, Tiro JA, Warnecke RB (2004) Some methodologic lessons learned from cancer screening research. Cancer 101(5 Suppl):1131–1145. doi:10.1002/cncr.20513
Ritvo P, Myers R, Del Giudice ME et al (2009) Fecal occult blood testing: people in Ontario are unaware of it and not ready for it. Can Fam Physician 55(2):176–177.e4
Seeff LC, Nadel MR, Klabunde CN et al (2004) Patterns and predictors of colorectal cancer test use in the adult U.S. population. Cancer 100(10):2093–2103. doi:10.1002/cncr.20276
Shapiro JA, Seeff LC, Thompson TD, Nadel MR, Klabunde CN, Vernon SW (2008) Colorectal cancer test use from the 2005 National Health Interview Survey. Cancer Epidemiol Biomark Prev 17(7):1623–1630. doi:10.1158/1055-9965.EPI-07-2838
Taylor DP, Cannon-Albright LA, Sweeney C et al (2011) Comparison of compliance for colorectal cancer screening and surveillance by colonoscopy based on risk. Genet Med 13(8):737–743. doi:10.1097/GIM.0b013e3182180c71
Imperiale TF (2007) Toward risk stratification for screening and surveillance of colorectal neoplasia: one small step for the colonoscopist. Gastroenterology 133(4):1364–1367. doi:10.1053/j.gastro.2007.08.067
Manne S, Markowitz A, Winawer S et al (2003) Understanding intention to undergo colonoscopy among intermediate-risk siblings of colorectal cancer patients: a test of a mediational model, 1 edn. Prev Med An Int J Devot Pract Theory. Elsevier Science, Netherlands
Antoniou AC, Pharoah PP, Smith P, Easton DF (2004) The BOADICEA model of genetic susceptibility to breast and ovarian cancer. Br J Cancer 91(8):1580–1590. doi:10.1038/sj.bjc.6602175
Fletcher SW (2011) Breast cancer screening: a 35-year perspective. Epidemiol Rev 33(1):165–175. doi:10.1093/epirev/mxr003
Freedman AN, Slattery ML, Ballard-Barbash R et al (2009) Colorectal cancer risk prediction tool for white men and women without known susceptibility. J Clin Oncol 27(5):686–693. doi:10.1200/JCO.2008.17.4797
Imperiale TF, Wagner DR, Lin CY, Larkin GN, Rogge JD, Ransohoff DF (2003) Using risk for advanced proximal colonic neoplasia to tailor endoscopic screening for colorectal cancer. Ann Intern Med 139(12):959–965
Levitzky BE, Brown CC, Heeren TC, Schroy PC 3rd (2011) Performance of a risk index for advanced proximal colorectal neoplasia among a racially/ethnically diverse patient population (risk index for advanced proximal neoplasia). Am J Gastroenterol 106(6):1099–1106. doi:10.1038/ajg.2011.20
Win AK, Macinnis RJ, Hopper JL, Jenkins MA (2012) Risk prediction models for colorectal cancer: a review. Cancer Epidemiol Biomark Prev 21(3):398–410. doi:10.1158/1055-9965.EPI-11-0771
Lin OS (2011) Editorial: risk scoring for colon cancer screening: validated, but still not ready for prime time. Am J Gastroenterol 106(6):1107–1109. doi:10.1038/ajg.2011.25
Hopper JL (2005) Application of genetics to the prevention of colorectal cancer. Recent results in cancer research Fortschritte der Krebsforschung. Progres dans les recherches sur le cancer 166:17–33
Sterne JA, Sutton AJ, Ioannidis JP et al (2011) Recommendations for examining and interpreting funnel plot asymmetry in meta-analyses of randomised controlled trials. BMJ 343:d4002. doi:10.1136/bmj.d4002
Madlensky L, McLaughlin J, Goel V (2003) A comparison of self-reported colorectal cancer screening with medical records. Cancer Epidemiol Biomark Prev 12(7):656–659
Acknowledgments
Driss Ait Ouakrim was supported by a Commonwealth Scientific and Industrial Research Organisation PhD scholarship (CSIRO, Preventative Heath Flagship). The study was conducted independently of funding agencies. Mark Jenkins is supported by a National Health & Medical Research Council, Australia Senior Research Fellow grant. The study was conducted independently of funding agencies.
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ait Ouakrim, D., Lockett, T., Boussioutas, A. et al. Screening participation for people at increased risk of colorectal cancer due to family history: a systematic review and meta-analysis. Familial Cancer 12, 459–472 (2013). https://doi.org/10.1007/s10689-013-9658-3
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10689-013-9658-3