Effectiveness of interventions to identify and manage patients with familial cancer risk in primary care: a systematic review
This systematic review evaluated the effectiveness of strategies to identify and manage patients with familial risk of breast, ovarian, colorectal and prostate cancer in primary care to improve clinical outcomes. MEDLINE, EMBASE, CINAHL and Cochrane library were searched from January 1980 to October 2017. We included randomised controlled trials (RCT) and non-randomised studies of interventions (NRSI). Primary outcomes were cancer incidence, cancer-related clinical outcomes or the identification of cancer predisposition; secondary outcomes were the appropriateness of referral, uptake of preventive strategies and cognitive and psychological effect. From 11,842 abstracts, 111 full texts were reviewed and three eligible studies (nine articles) identified. Two were cluster RCTs and one NRSI; all used risk assessment software. No studies identified our primary outcomes, with no consistent outcome across the three studies. In one RCT, intervention improved the proportion of genetic referrals meeting referral guidelines for breast cancer (OR 4.5, 95% CI 1.6 to 13.1). In the other RCT, there was no difference in screening adherence between the intervention and control group. However, there was borderline increased risk perception (OR 1.89, 95% CI 0.99 to 3.59) in the subgroup that under-estimated their colon cancer risk. In the NRSI, there was no change in psychological distress in patients at increased familial breast cancer risk, but population risk patients had reduced anxiety after intervention (state anxiety mean change − 3, 95% CI − 5 to − 2). Future studies should have better-defined comparator groups and longer follow-up and assess outcomes using validated tools.
KeywordsPrimary health care Genetic predisposition to disease Breast neoplasm Ovarian neoplasms Colorectal neoplasms Prostatic neoplasms
We would like to thank Jeanette Eldridge, senior research librarian at the University of Nottingham for her help with the literature search strategy and Hannah Carpenter, PhD student at the Primary Care Division, University of Nottingham for reviewing the protocol.
SL and MP are National Institute for Health Research (NIHR) funded Academic Clinical Fellows.
Compliance with ethical standards
Conflict of interest
Nadeem Qureshi is a member of the NICE Guideline Development Group for Familial Breast Cancer and the Advisory Board for Journal of Community Genetics. Siang Ing Lee, Mitesh Patel, Brittany Dutton, Stephen Weng and Jocelyn Luveta declare no conflict of interest.
This article does not contain any studies with human participants or animals performed by any of the authors.
- Acheson LS, Wang C, Zyzanski SJ, Lynn A, Ruffin MT 4th, Gramling R, Rubinstein WS, O'Neill SM, Nease de Jr, Family Healthware Impact Trial (FHITr) Group (2010) Family history and perceptions about risk and prevention for chronic diseases in primary care: a report from the family healthware impact trial. Genet Med 12:212–218. https://doi.org/10.1097/GIM.0b013e3181d56ae6 CrossRefGoogle Scholar
- Carbine NE, Lostumbo L, Wallace J, Ko H (2018) Risk-reducing mastectomy for the prevention of primary breast cancer. Cochrane Database Syst Rev (4):CD002748. https://doi.org/10.1002/14651858.CD002748.pub4
- Cuzick J, Sestak I, Bonanni B, Costantino JP, Cummings S, DeCensi A, Dowsett M, Forbes JF, Ford L, LaCroix A, Mershon J, Mitlak BH, Powles T, Veronesi U, Vogel V, Wickerham DL, SERM Chemoprevention of Breast Cancer Overview Group (2013) Selective oestrogen receptor modulators in prevention of breast cancer: an updated meta-analysis of individual participant data. Lancet 381(9880):1827–1834. https://doi.org/10.1016/S0140-6736(13)60140-3 CrossRefPubMedPubMedCentralGoogle Scholar
- Domchek SM, Friebel TM, Singer CF, Evans DG, Lynch HT, Isaacs C, Garber JE, Neuhausen SL, Matloff E, Eeles R, Pichert G, van t'veer L, Tung N, Weitzel JN, Couch FJ, Rubinstein WS, Ganz PA, Daly MB, Olopade OI, Tomlinson G, Schildkraut J, Blum JL, Rebbeck TR (2010) Association of risk-reducing surgery in BRCA1 or BRCA2 mutation carriers with cancer risk and mortality. JAMA 304(9):967–975. https://doi.org/10.1001/jama.2010.1237 CrossRefPubMedPubMedCentralGoogle Scholar
- Duffy SW, Mackay J, Thomas S, Anderson E, Chen THH, Ellis I, Evans G, Fielder H, Fox R, Gui G, Macmillan D, Moss S, Rogers C, Sibbering M, Wallis M, Warren R, Watson E, Whynes D, Allgood P, Caunt J (2013) Evaluation of mammographic surveillance services in women aged 40-49 years with a moderate family history of breast cancer: a single-arm cohort study. Health Technol Assess 17(11):vii–xiv, 1-95. https://doi.org/10.3310/hta17110 CrossRefPubMedPubMedCentralGoogle Scholar
- Emery J, Morris H, Goodchild R, Fanshawe T, Prevost AT, Bobrow M, Kinmonth AL (2007) The GRAIDS Trial: a cluster randomised controlled trial of computer decision support for the management of familial cancer risk in primary care. Br J Cancer 97(4):486–493. https://doi.org/10.1038/sj.bjc.6603897 CrossRefPubMedPubMedCentralGoogle Scholar
- Higgins JPT, Green S. (eds). (2011) Cochrane handbook for systematic reviews of interventions version 5.1.0. The Cochrane CollaborationGoogle Scholar
- Hilgart JS, Coles B, Iredale R (2012) Cancer genetic risk assessment for individuals at risk of familial breast cancer. Cochrane Database of Syst Rev (2):CD003721. https://doi.org/10.1002/14651858.CD003721.pub3
- International Standard Randomised Controlled Trials Number (ISRCTN) Registry. (2014) Proactive familial breast cancer risk assessment in primary care (phase 2). http://www.isrctn.com/ISRCTN16117197. Accessed 10th October 2018
- Naicker S, Meiser B, Goodwin A et al (2013) Which tests is best? A randomised controlled trial to evaluate the use of familial phenotype to risk appropriately screen for colorectal cancer in the general population. Psycho-Oncology 22:27Google Scholar
- National Institute for Health and Care Excellence (NICE). (2017) Familial breast cancer: classification care and managing breast cancer and related risks in people with a family history of breast cancer [CG164]. NICE, LondonGoogle Scholar
- NHS England. (2013) Transforming primary care in London: general practice a call to action. NHS England, London. https://www.england.nhs.uk/london/wp-content/uploads/sites/8/2013/11/Call-Action-ACCESSIBLE.pdf Accessed 16th October 2018
- O'Neill SM, Rubinstein WS, Wang C, Yoon PW, Acheson LS, Rothrock N, Starzyk EJ, Beaumont JL, Galliher JM, Ruffin MT 4th, Family Healthware Impact Trial group (2009) Familial risk for common diseases in primary care: the Family Healthware Impact Trial. Am J Prev Med 36(6):506–514. https://doi.org/10.1016/j.amepre.2009.03.002 CrossRefGoogle Scholar
- Orlando LA, Hauser ER, Christianson C, Powell KP, Buchanan AH, Chesnut B, Agbaje AB, Henrich VC, Ginsburg G (2011) Protocol for implementation of family health history collection and decision support into primary care using a computerized family health history system. BMC Health Serv Res 11(264). https://doi.org/10.1186/1472-6963-11-264
- Orlando LA, Wu RR, Beadles C, Himmel T, Buchanan AH, Powell KP, Hauser ER, Henrich VC, Ginsburg GS (2014) Implementing family health history risk stratification in primary care: impact of guideline criteria on populations and resource demand. Am J Med Genet C Semin Med Genet 166C(1):24–33. https://doi.org/10.1002/ajmg.c.31388 CrossRefPubMedGoogle Scholar
- Paluch-Shimon S, Cardoso F, Sessa C, Balmana J, Cardoso MJ, Gilbert F, Senkus E, ESMO Guidelines Committee (2016) Prevention and screening in BRCA mutation carriers and other breast/ovarian hereditary cancer syndromes: ESMO Clinical Practice Guidelines for cancer prevention and screening. Ann Oncol 27(suppl 5):v103–v110. https://doi.org/10.1093/annonc/mdw327 CrossRefPubMedGoogle Scholar
- Preventive Services Task Force US (2015) Risk assessment, genetic counseling, and genetic testing for BRCA-related cancer in women: recommendation statement. Am Fam Physician 91(2)Google Scholar
- PROSPERO (2017) International prospective register of systematic review. https://www.crd.york.ac.uk/prospero/display_record.php?RecordID=83418 Accessed 26th September 2017
- Qureshi N, Wilson B, Santaguida P et al (2007) Collection and use of cancer family history in primary care. Evidence Report/Technology Assessment No. 159. AHRQ Publication No. 08-E001. Agency for Healthcare Research and Quality, Rockville, MDGoogle Scholar
- Rubinstein WS, Acheson LS, O'Neill SM, Ruffin MT 4th, Wang C, Beaumont JL, Rothrock N, Family Healthware Impact Trial (FHITr) Group (2011a) Clinical utility of family history for cancer screening and referral in primary care: a report from the Family Healthware Impact Trial. Genet Med 13(11):956–965. https://doi.org/10.1097/GIM.0b013e3182241d88 CrossRefGoogle Scholar
- Rubinstein WS, O'Neill SM, Rothrock N, Starzyk EJ, Beaumont JL, Acheson LS, Wang C, Gramling R, Galliher JM, Ruffin MT (2011b) Components of family history associated with women's disease perceptions for cancer: a report from the Family HealthwareTM Impact Trial. Genet Med 13(1):52–62. https://doi.org/10.1097/GIM.0b013e3181fbe485 CrossRefPubMedPubMedCentralGoogle Scholar
- Schünemann H, Brożek J, Guyatt G, Oxman A. (eds) (2013) GRADE handbook for grading quality of evidence and strength of recommendations. The GRADE Working Group, 2013Google Scholar
- UK Biobank. (2007) Protocol for a large-scale prospective epidemiological resource. http://www.ukbiobank.ac.uk/wp-content/uploads/2011/11/UK-Biobank-Protocol.pdf Accessed 10th October 2018
- Wang C, Sen A, Plegue M, Ruffin MT IV, O'Neill SM, Rubinstein WS, Acheson LS, Yoon PW, Valdez R, Irizarry-de la Cruz M, Khoury MJ, Jorgensen C, Scheuner MT, Rubinstein WS, O'Neill SM, Rothrock N, Beaumont JL, Khan S, Ali D, Ruffin MT, Nease D, Acheson LS, Zyzanski SJ, Wiesner GL, Werner J, Pace WD, Galliher JM, Brandt E, Wang C, Gramling R, Starzyk EJ (2015) Impact of family history assessment on communication with family members and health care providers: a report from the Family Healthware Impact Trial (FHITr). Prev Med 77:28–34. https://doi.org/10.1016/j.ypmed.2015.04.007 CrossRefPubMedPubMedCentralGoogle Scholar
- Wilson BJ, Torrance N, Mollison J et al (2005) Improving the referral process for familial breast cancer genetic counselling: findings of three randomised controlled trials of two interventions. Health Technology Assessment (Winchester, England) 9(3):iii–iv, 1-12Google Scholar
- Wilson BJ, Torrance N, Mollison J, Watson MS, Douglas A, Miedzybrodzka Z, Gordon R, Wordsworth S, Campbell M, Haites N, Grant A (2006) Cluster randomized trial of a multifaceted primary care decision-support intervention for inherited breast cancer risk. Fam Pract 23(5):537–544. https://doi.org/10.1093/fampra/cml026 CrossRefPubMedGoogle Scholar
- World Cancer Research Fund. Worldwide cancer data: global cancer statistics for the most common cancers. https://www.wcrf.org/dietandcancer/cancer-trends/worldwide-cancer-data Accessed 23rd October 2018
- Wu RR, Orlando LA, Himmel TL, Buchanan AH, Powell KP, Hauser ER, Agbaje AB, Henrich VC, Ginsburg GS (2013) Patient and primary care provider experience using a family health history collection, risk stratification, and clinical decision support tool: a type 2 hybrid controlled implementation-effectiveness trial. BMC Fam Pract 14(111). https://doi.org/10.1186/1471-2296-14-111