Study protocol: a cluster randomized controlled trial of web-based decision support tools for increasing BRCA1/2 genetic counseling referral in primary care

Thomas B Silverman, Alejandro Vanegas, Awilda Marte, Jennie Mata, Margaret Sin, Juan Carlos Rodriguez Ramirez, Wei-Yann Tsai, Katherine D Crew, Rita Kukafka, Thomas B Silverman, Alejandro Vanegas, Awilda Marte, Jennie Mata, Margaret Sin, Juan Carlos Rodriguez Ramirez, Wei-Yann Tsai, Katherine D Crew, Rita Kukafka

Abstract

Background: BRCA1 and BRCA2 mutations confer a substantial breast risk of developing breast cancer to those who carry them. For this reason, the United States Preventative Services Task Force (USPSTF) has recommended that all women be screened in the primary care setting for a family history indicative of a mutation, and women with strong family histories of breast or ovarian cancer be referred to genetic counseling. However, few high-risk women are being routinely screened and fewer are referred to genetic counseling. To address this need we have developed two decision support tools that are integrated into clinical care.

Method: This study is a cluster randomized controlled trial of high-risk patients and their health care providers. Patient-provider dyads will be randomized to receive either standard education that is supplemented with the patient-facing decision aid, RealRisks, and the provider-facing Breast Cancer Risk Navigation Toolbox (BNAV) or standard education alone. We will assess these tools' effectiveness in promoting genetic counseling uptake and informed and shared decision making about genetic testing.

Discussion: If found to be effective, these tools can help integrate genomic risk assessment into primary care and, ultimately, help expand access to risk-appropriate breast cancer prevention options to a broader population of high-risk women.

Trial registration: This trial is retrospectively registered with ClinicalTrials.gov Identifier: NCT03470402 : 20 March 2018.

Keywords: Breast Cancer prevention; Decision support; Genetic testing; Risk communication.

Conflict of interest statement

This study was approved by the Columbia University Medical Center Institutional Review Board (AAAR3676). Informed written, verbal, or online consent is obtained from all patient and provider participants prior to accrual into the study.

Not Applicable.

The authors declare that they have no competing interests.

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Figures

Fig. 1
Fig. 1
Example of an experience-based, pictographic risk game in RealRisks
Fig. 2
Fig. 2
Example summaries provided by the Patient Action Plan
Fig. 3
Fig. 3
Example of the personalized patient table included in the BNAV Toolbox
Fig. 4
Fig. 4
Example of the Provider Action Plan
Fig. 5
Fig. 5
Example of the electronic health record (EHR)-embedded dashboard notice

References

    1. Singletary SE. Rating the risk factors for breast cancer. Ann Surg. 2003;237(4):474.
    1. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2016. CA Cancer J Clin. 2016;66(1):7–30. doi: 10.3322/caac.21332.
    1. Anglian B. Prevalence and penetrance of mutations in BRCA1 and BRCA2 in a population based series of breast cancer cases. Br J Cancer. 2000;83:1301–1308. doi: 10.1054/bjoc.2000.1407.
    1. Kuchenbaecker KB, Hopper JL, Barnes DR, Phillips K-A, Mooij TM, Roos-Blom M-J, Jervis S, Van Leeuwen FE, Milne RL, Andrieu N. Risks of breast, ovarian, and contralateral breast cancer for BRCA1 and BRCA2 mutation carriers. Jama. 2017;317(23):2402–2416. doi: 10.1001/jama.2017.7112.
    1. Risch HA, McLaughlin JR, Cole DE, Rosen B, Bradley L, Fan I, Tang J, Li S, Zhang S, Shaw PA. Population BRCA1 and BRCA2 mutation frequencies and cancer penetrances: a kin–cohort study in Ontario, Canada. J Natl Cancer Inst. 2006;98(23):1694–1706. doi: 10.1093/jnci/djj465.
    1. Pal T, Permuth-Wey J, Betts JA, Krischer JP, Fiorica J, Arango H, LaPolla J, Hoffman M, Martino MA, Wakeley K. BRCA1 and BRCA2 mutations account for a large proportion of ovarian carcinoma cases. Cancer. 2005;104(12):2807–2816. doi: 10.1002/cncr.21536.
    1. Moyer VA. Risk assessment, genetic counseling, and genetic testing for BRCA-related cancer in women: US preventive services task force recommendation statement. Ann Intern Med. 2014;160(4):271–281. doi: 10.7326/M13-2747.
    1. Rebbeck TR, Friebel T, Lynch HT, Neuhausen SL, Lvt V, Garber JE, Evans GR, Narod SA, Isaacs C, Matloff E, et al. bilateral prophylactic mastectomy reduces breast Cancer risk in BRCA1 and BRCA2 mutation carriers: the PROSE study group. J Clin Oncol. 2004;22(6):1055–1062. doi: 10.1200/JCO.2004.04.188.
    1. Saslow D, Boetes C, Burke W, Harms S, Leach MO, Lehman CD, Morris E, Pisano E, Schnall M, Sener S. American Cancer Society guidelines for breast screening with MRI as an adjunct to mammography. CA Cancer J Clin. 2007;57(2):75–89. doi: 10.3322/canjclin.57.2.75.
    1. Warner E, Hill K, Causer P, Plewes D, Jong R, Yaffe M, Foulkes WD, Ghadirian P, Lynch H, Couch F. Prospective study of breast cancer incidence in women with a BRCA1 or BRCA2 mutation under surveillance with and without magnetic resonance imaging. J Clin Oncol. 2011;29(13):1664–1669. doi: 10.1200/JCO.2009.27.0835.
    1. Warner E, Messersmith H, Causer P, Eisen A, Shumak R, Plewes D. Systematic review: using magnetic resonance imaging to screen women at high risk for breast cancer. Ann Intern Med. 2008;148(9):671–679. doi: 10.7326/0003-4819-148-9-200805060-00007.
    1. Isern A, Loman N, Malina J, Olsson H, Ringberg A. Histopathological findings and follow-up after prophylactic mastectomy and immediate breast reconstruction in 100 women from families with hereditary breast cancer. Eur J Surg Oncol. 2008;34(10):1148–1154. doi: 10.1016/j.ejso.2008.03.002.
    1. Kauff ND, Domchek SM, Friebel TM, Robson ME, Lee J, Garber JE, Isaacs C, Evans DG, Lynch H, Eeles RA. Risk-reducing salpingo-oophorectomy for the prevention of BRCA1-and BRCA2-associated breast and gynecologic cancer: a multicenter, prospective study. J Clin Oncol. 2008;26(8):1331–1337. doi: 10.1200/JCO.2007.13.9626.
    1. Rebbeck TR, Kauff ND, Domchek SM. Meta-analysis of risk reduction estimates associated with risk-reducing salpingo-oophorectomy in BRCA1 or BRCA2 mutation carriers. J Natl Cancer Inst. 2009;101(2):80–87. doi: 10.1093/jnci/djn442.
    1. Domchek SM, Friebel TM, Neuhausen SL, Wagner T, Evans G, Isaacs C, Garber JE, Daly MB, Eeles R, Matloff E. Mortality after bilateral salpingo-oophorectomy in BRCA1 and BRCA2 mutation carriers: a prospective cohort study. The lancet oncology. 2006;7(3):223–229. doi: 10.1016/S1470-2045(06)70585-X.
    1. Domchek SM, Friebel TM, Singer CF, Evans DG, Lynch HT, Isaacs C, Garber JE, Neuhausen SL, Matloff E, Eeles R. Association of risk-reducing surgery in BRCA1 or BRCA2 mutation carriers with cancer risk and mortality. Jama. 2010;304(9):967–975. doi: 10.1001/jama.2010.1237.
    1. Kaas R, Verhoef S, Wesseling J, Rookus MA, Oldenburg HS, Peeters M-JV, Rutgers EJ. Prophylactic mastectomy in BRCA1 and BRCA2 mutation carriers: very low risk for subsequent breast cancer. Ann Surg. 2010;251(3):488–492. doi: 10.1097/SLA.0b013e3181c3c36d.
    1. Finch AP, Lubinski J, Møller P, Singer CF, Karlan B, Senter L, Rosen B, Maehle L, Ghadirian P, Cybulski C. Impact of oophorectomy on cancer incidence and mortality in women with a BRCA1 or BRCA2 mutation. J Clin Oncol. 2014;32(15):1547–1553. doi: 10.1200/JCO.2013.53.2820.
    1. King M-C, Wieand S, Hale K, Lee M, Walsh T, Owens K, Tait J, Ford L, Dunn BK, Costantino J. Tamoxifen and breast cancer incidence among women with inherited mutations in BRCA1 and BRCA2: National Surgical Adjuvant Breast and bowel project (NSABP-P1) breast Cancer prevention trial. Jama. 2001;286(18):2251–2256. doi: 10.1001/jama.286.18.2251.
    1. Narod SA, Brunet J-S, Ghadirian P, Robson M, Heimdal K, Neuhausen SL, Stoppa-Lyonnet D, Lerman C, Pasini B, De Los RP. Tamoxifen and risk of contralateral breast cancer in BRCA1 and BRCA2 mutation carriers: a case-control study. Lancet. 2000;356(9245):1876–1881. doi: 10.1016/S0140-6736(00)03258-X.
    1. Moyer VA, On behalf of the USPSTF risk assessment, genetic counseling, and genetic testing for brca-related cancer in women: U.S. preventive services task force recommendation statement. Ann Intern Med. 2014;160(4):271–281. doi: 10.7326/M13-2747.
    1. Bellcross CA, Leadbetter S, Alford SH, Peipins LA. Prevalence and Healthcare Actions of Women in a Large Health System with a Family History Meeting the 2005 USPSTF recommendation for BRCA genetic counseling referral. Cancer Epidemiol Biomarkers Prev. 22(4):728–35.
    1. Willis AM, Smith SK, Meiser B, Ballinger ML, Thomas DM, Young MA. Sociodemographic, psychosocial and clinical factors associated with uptake of genetic counselling for hereditary cancer: a systematic review. Clin Genet. 2017;92(2):121–133. doi: 10.1111/cge.12868.
    1. Ropka ME, Wenzel J, Phillips EK, Siadaty M, Philbrick JT. Uptake rates for breast cancer genetic testing: a systematic review. Cancer Epidemiol Biomarkers Prev. 2006;15(5):840–855. doi: 10.1158/1055-9965.EPI-05-0002.
    1. Levy DE, Garber JE, Shields AE. Guidelines for genetic risk assessment of hereditary breast and ovarian Cancer: early disagreements and low utilization. J Gen Intern Med. 2009;24(7):822–828. doi: 10.1007/s11606-009-1009-6.
    1. McGuinness JE, Trivedi MS, Vanegas A, Colbeth H, Sandoval R, Kukafka R, Crew KD: Decision support for family history intake to determine eligibility for BRCA testing among multiethnic women. In.: American society of Clin Oncol; 2017.
    1. Joseph G, Kaplan C, Luce J, Lee R, Stewart S, Guerra C, Pasick R. Efficient identification and referral of low-income women at high risk for hereditary breast Cancer: a practice-based approach. Public Health Genomics. 2012;15(3–4):172–180. doi: 10.1159/000336419.
    1. Shields AE, Burke W, Levy DE. Differential use of available genetic tests among primary care physicians in the United States: results of a national survey. Genetics in medicine. 2008;10(6):404. doi: 10.1097/GIM.0b013e3181770184.
    1. Hall MJ, Olopade OI. Disparities in genetic testing: thinking outside the BRCA box. J Clin Oncol. 2006;24(14):2197–2203. doi: 10.1200/JCO.2006.05.5889.
    1. Yi H, Xiao T, Thomas PS, Aguirre AN, Smalletz C, Dimond J, Finkelstein J, Infante K, Trivedi M, David R: Barriers and facilitators to patient-provider communication when discussing breast cancer risk to aid in the development of decision support tools. In: AMIA Annual Symposium Proceedings: 2015: American Medical Informatics Association; 2015: 1352.
    1. Pal T, Cragun D, Lewis C, Doty A, Rodriguez M, Radford C, Thompson Z, Kim J, Vadaparampil ST. A statewide survey of practitioners to assess knowledge and clinical practices regarding hereditary breast and ovarian cancer. Genet Test Mol Biomarkers. 2013;17(5):367–375. doi: 10.1089/gtmb.2012.0381.
    1. Culver JO, Bowen DJ, Reynolds SE, Pinsky LE, Press N, Burke W. Breast cancer risk communication: assessment of primary care physicians by standardized patients. Genetics in Medicine. 2009;11(10):735. doi: 10.1097/GIM.0b013e3181b2e5eb.
    1. Trivers KF, Baldwin L-M, Miller JW, Matthews B, Andrilla CHA, Lishner DM, Goff BA. Reported referral for genetic counseling or BRCA 1/2 testing among United States physicians. Cancer. 2011;117(23):5334–5343. doi: 10.1002/cncr.26166.
    1. Bellcross CA, Kolor K, Goddard KA, Coates RJ, Reyes M, Khoury MJ. Awareness and utilization of BRCA1/2 testing among US primary care physicians. Am J Prev Med. 2011;40(1):61–66. doi: 10.1016/j.amepre.2010.09.027.
    1. Nair N, Bellcross C, Haddad L, Martin M, Matthews R, Gabram-Mendola S, Crane B, Meaney-Delman D. Georgia primary care providers’ knowledge of hereditary breast and ovarian Cancer syndrome. J Cancer Educ. 2017;32(1):119–124. doi: 10.1007/s13187-015-0950-9.
    1. Suther S, Goodson P. Barriers to the provision of genetic services by primary care physicians: a systematic review of the literature. Genetics in Medicine. 2003;5(2):70. doi: 10.1097/01.GIM.0000055201.16487.61.
    1. Murff HJ, Greevy RA, Syngal S. The comprehensiveness of family cancer history assessments in primary care. Public Health Genomics. 2007;10(3):174–180. doi: 10.1159/000101759.
    1. Peters E, Hibbard J, Slovic P, Dieckmann N. Numeracy skill and the communication, comprehension, and use of risk-benefit information. Health Aff. 2007;26(3):741–748. doi: 10.1377/hlthaff.26.3.741.
    1. Guerra CE, Jacobs SE, Holmes JH, Shea JA. Are physicians discussing prostate Cancer screening with their patients and why or why not? A pilot study. J Gen Intern Med. 2007;22(7):901–907. doi: 10.1007/s11606-007-0142-3.
    1. Yi H, Xiao T, Thomas PS, Aguirre AN, Smalletz C, Dimond J, Finkelstein J, Infante K, Trivedi M, David R, et al. Barriers and facilitators to patient-provider communication when discussing breast Cancer risk to aid in the development of decision support tools. AMIA Ann Symp Proc. 2015;2015:1352–1360.
    1. Finkelstein J, Wood J, Crew KD, Kukafka R. Introducing a comprehensive informatics framework to promote breast Cancer risk assessment and chemoprevention in the primary care setting. AMIA Summits on Translational Science Proceedings. 2017;2017:58–67.
    1. Coe AM, Ueng W, Vargas JM, David R, Vanegas A, Infante K, Trivedi M, Yi H, Dimond J, Crew KD: Usability Testing of a Web-Based Decision Aid for Breast Cancer Risk Assessment Among Multi-Ethnic Women. In: AMIA Annual Symposium Proceedings: 2016: American Medical Informatics Association; 2016: 411.
    1. Kukafka R, Yi H, Xiao T, Thomas P, Aguirre A, Smalletz C, David R, Crew K. Why breast Cancer risk by the numbers is not enough: evaluation of a decision aid in multi-ethnic, low-numerate women. J Med Internet Res. 2015;17(7):e165. doi: 10.2196/jmir.4028.
    1. Alge D, on Behalf on the New York Presbyterian Ambulatory Care Network: Ambulatory Care Network: 2016 Annual Report. In.: New York Presbyterian Hospital 2017.
    1. Ancker JS, Weber EU, Kukafka R. Effect of arrangement of stick figures on estimates of proportion in risk graphics. Med Decis Mak. 2011;31(1):143–150. doi: 10.1177/0272989X10369006.
    1. Deci EL, Ryan R: RM (1985): Intrinsic motivation and self-determination in human behavior. N Y 1997.
    1. Elwyn G, Frosch D, Thomson R, Joseph-Williams N, Lloyd A, Kinnersley P, Cording E, Tomson D, Dodd C, Rollnick S. Shared decision making: a model for clinical practice. J Gen Intern Med. 2012;27(10):1361–1367. doi: 10.1007/s11606-012-2077-6.
    1. Mazzola E, Blackford A, Parmigiani G, Biswas S: Recent enhancements to the genetic risk prediction model BRCAPRO. Cancer informatics 2015, 14:CIN. S17292.
    1. Vogel KJ, Atchley DP, Erlichman J, Broglio KR, Ready KJ, Valero V, Amos CI, Hortobagyi GN, Lu KH, Arun B. BRCA1 and BRCA2 genetic testing in Hispanic patients: mutation prevalence and evaluation of the BRCAPRO risk assessment model. J Clin Oncol. 2007;25(29):4635–4641. doi: 10.1200/JCO.2006.10.4703.
    1. Marteau TM, Dormandy E, Michie S. A measure of informed choice. Health Expectations : An International Journal of Public Participation in Health Care and Health Policy. 2001;4(2):99–108. doi: 10.1046/j.1369-6513.2001.00140.x.
    1. Lerman C, Narod S, Schulman K, et al. Brca1 testing in families with hereditary breast-ovarian cancer: a prospective study of patient decision making and outcomes. JAMA. 1996;275(24):1885–1892. doi: 10.1001/jama.1996.03530480027036.
    1. O'Connor AM. Validation of a decisional conflict scale. Med Decis Mak. 1995;15(1):25–30. doi: 10.1177/0272989X9501500105.
    1. Linder SK, Swank PR, Vernon SW, Mullen PD, Morgan RO, Volk RJ. Validity of a low literacy version of the decisional conflict scale. Patient Educ Couns. 2011;85(3):521–524. doi: 10.1016/j.pec.2010.12.012.
    1. Kriston L, Scholl I, Hölzel L, Simon D, Loh A, Härter M. The 9-item shared decision making questionnaire (SDM-Q-9). Development and psychometric properties in a primary care sample. Patient Educ Couns. 2010;80(1):94–99. doi: 10.1016/j.pec.2009.09.034.
    1. Scholl I, Kriston L, Dirmaier J, Buchholz A, Härter M. Development and psychometric properties of the shared decision making questionnaire–physician version (SDM-Q-doc) Patient Educ Couns. 2012;88(2):284–290. doi: 10.1016/j.pec.2012.03.005.
    1. Chew LD, Griffin JM, Partin MR, Noorbaloochi S, Grill JP, Snyder A, Bradley KA, Nugent SM, Baines AD, VanRyn M. Validation of screening questions for limited health literacy in a large VA outpatient population. J Gen Intern Med. 2008;23(5):561–566. doi: 10.1007/s11606-008-0520-5.
    1. Norman CD, Skinner HA: eHEALS: the eHealth literacy scale. J Med Internet Res 2006, 8(4).
    1. Zikmund-Fisher BJ, Smith DM, Ubel PA, Fagerlin A. Validation of the subjective numeracy scale: effects of low numeracy on comprehension of risk communications and utility elicitations. Med Decis Mak. 2007;27(5):663–671. doi: 10.1177/0272989X07303824.
    1. Marin G, Sabogal F, Marin BV, Otero-Sabogal R, Perez-Stable EJ. Development of a short acculturation scale for Hispanics. Hisp J Behav Sci. 1987;9(2):183–205. doi: 10.1177/07399863870092005.
    1. Levy AG, Shea J, Williams SV, Quistberg A, Armstrong K. Measuring perceptions of breast cancer risk. Cancer Epidemiology and Prevention Biomarkers. 2006;15(10):1893–1898. doi: 10.1158/1055-9965.EPI-05-0482.
    1. Hall MA, Zheng B, Dugan E, Camacho F, Kidd KE, Mishra A, Balkrishnan R. Measuring patients’ trust in their primary care providers. Med Care Res Rev. 2002;59(3):293–318. doi: 10.1177/1077558702059003004.
    1. Han PKJ, Joekes K, Elwyn G, Mazor KM, Thomson R, Sedgwick P, Ibison J, Wong JB. Development and evaluation of a risk communication curriculum for medical students. Patient Educ Couns. 2014;94(1):43–49. doi: 10.1016/j.pec.2013.09.009.
    1. Watson E, Clements A, Yudkin P, Rose P, Bukach C, Mackay J, Lucassen A, Austoker J. Evaluation of the impact of two educational interventions on GP management of familial breast/ovarian cancer cases: a cluster randomised controlled trial. Br J Gen Pract. 2001;51(471):817–821.
    1. Marzuillo C, De Vito C, Boccia S, D’Addario M, D’Andrea E, Santini P, Boccia A, Villari P. Knowledge, attitudes and behavior of physicians regarding predictive genetic tests for breast and colorectal cancer. Prev Med. 2013;57(5):477–482. doi: 10.1016/j.ypmed.2013.06.022.
    1. Wilson BJ, Islam R, Francis JJ, Grimshaw JM, Permaul JA, Allanson JE, Blaine S, Graham ID, Meschino WS, Ramsay CR. Supporting genetics in primary care: investigating how theory can inform professional education. Eur J Hum Genet. 2016;24(11):1541. doi: 10.1038/ejhg.2016.68.
    1. Krupat E, Rosenkranz SL, Yeager CM, Barnard K, Putnam SM, Inui TS. The practice orientations of physicians and patients: the effect of doctor–patient congruence on satisfaction. Patient Educ Couns. 2000;39(1):49–59. doi: 10.1016/S0738-3991(99)00090-7.
    1. O’Connor AM, Stacey D, Entwistle V, Llewellyn-Thomas H, Rovner D, Holmes-Rovner M, Tait V, Tetroe J, Fiset V, Barry M. Decision aids for people facing health treatment or screening decisions. Cochrane Database Syst Rev. 2003;2
    1. Armstrong K, Micco E, Carney A, Stopfer J, Putt M. Racial differences in the use of brca1/2 testing among women with a family history of breast or ovarian cancer. JAMA. 2005;293(14):1729–1736. doi: 10.1001/jama.293.14.1729.
    1. Lu KH, Wood ME, Daniels M, Burke C, Ford J, Kauff ND, Kohlmann W, Lindor NM, Mulvey TM, Robinson L, et al. American Society of Clinical Oncology expert statement: collection and use of a Cancer family history for oncology providers. J Clin Oncol. 2014;32(8):833–840. doi: 10.1200/JCO.2013.50.9257.
    1. Elwyn G, Scholl I, Tietbohl C, Mann M, Edwards AGK, Clay C, Légaré F, Weijden Tvd, Lewis CL, Wexler RM et al: “many miles to go …”: a systematic review of the implementation of patient decision support interventions into routine clinical practice. BMC Medical Informatics and Decision Making 2013, 13(Suppl 2):S14-S14.
    1. Bowen DJ, Robbins R, Bush N, Meischke H, Ludwig A, Wooldridge J. Effects of a web-based intervention on women’s breast health behaviors. Translational Behavioral Medicine. 2017;7(2):309–319. doi: 10.1007/s13142-016-0439-z.
    1. Lerman C, Kash K, Stefanek M. Younger women at increased risk for breast cancer: perceived risk, psychological well-being, and surveillance behavior. J Natl Cancer Inst Monogr. 1994;16:171–176.
    1. O’Connor A: User manual-decision self-efficacy scale. Patient Decision Aids, Ottawa Hospital Research Institute (OHIR) Web site https://decisionaid ohri ca/docs/develop/Tools/Decision_SelfEfficacy pdf (accessed 4 Feb 2015) 1995.
    1. Brehaut JC, O'Connor AM, Wood TJ, Hack TF, Siminoff L, Gordon E, Feldman-Stewart D. Validation of a decision regret scale. Med Decis Mak. 2003;23(4):281–292. doi: 10.1177/0272989X03256005.
    1. Bouhnik A-D, N’Diaye K, Evans DG, Harris H, Tibben A, van Asperen C, Schmidtke J, Nippert I, Mancini J, Julian-Reynier C. Validation of a scale for assessing attitudes towards outcomes of genetic cancer testing among primary care providers and breast specialists. PLoS One. 2017;12(6):e0178447. doi: 10.1371/journal.pone.0178447.

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