Patient and Clinician Decision Support to Increase Genetic Counseling for Hereditary Breast and Ovarian Cancer Syndrome in Primary Care: A Cluster Randomized Clinical Trial

Rita Kukafka, Samuel Pan, Thomas Silverman, Tianmai Zhang, Wendy K Chung, Mary Beth Terry, Elaine Fleck, Richard G Younge, Meghna S Trivedi, Julia E McGuinness, Ting He, Jill Dimond, Katherine D Crew, Rita Kukafka, Samuel Pan, Thomas Silverman, Tianmai Zhang, Wendy K Chung, Mary Beth Terry, Elaine Fleck, Richard G Younge, Meghna S Trivedi, Julia E McGuinness, Ting He, Jill Dimond, Katherine D Crew

Abstract

Importance: To promote the identification of women carrying BRCA1/2 variants, the US Preventive Services Task Force recommends that primary care clinicians screen asymptomatic women for an increased risk of carrying a BRCA1/2 variant risk.

Objective: To examine the effects of patient and clinician decision support about BRCA1/2 genetic testing compared with standard education alone.

Design, setting, and participants: This clustered randomized clinical trial was conducted at an academic medical center including 67 clinicians (unit of randomization) and 187 patients. Patient eligibility criteria included women aged 21 to 75 years with no history of breast or ovarian cancer, no prior genetic counseling or testing for hereditary breast and ovarian cancer syndrome (HBOC), and meeting family history criteria for BRCA1/2 genetic testing.

Interventions: RealRisks decision aid for patients and the Breast Cancer Risk Navigation Tool decision support for clinicians. Patients scheduled a visit with their clinician within 6 months of enrollment.

Main outcomes and measures: The primary end point was genetic counseling uptake at 6 months. Secondary outcomes were genetic testing uptake at 6 and 24 months, decision-making measures (perceived breast cancer risk, breast cancer worry, genetic testing knowledge, decision conflict) based upon patient surveys administered at baseline, 1 month, postclinic visit, and 6 months.

Results: From December 2018 to February 2020, 187 evaluable patients (101 in the intervention group, 86 in the control group) were enrolled (mean [SD] age: 40.7 [13.2] years; 88 Hispanic patients [46.6%]; 15 non-Hispanic Black patients [8.1%]; 72 non-Hispanic White patients [38.9%]; 35 patients [18.9%] with high school education or less) and 164 (87.8%) completed the trial. There was no significant difference in genetic counseling uptake at 6 months between the intervention group (20 patients [19.8%]) and control group (10 patients [11.6%]; difference, 8.2 percentage points; OR, 1.88 [95% CI, 0.82-4.30]; P = .14). Genetic testing uptake within 6 months was also statistically nonsignificant (13 patients [12.9%] in the intervention group vs 7 patients [8.1%] in the control group; P = .31). At 24 months, genetic testing uptake was 31 patients (30.7%) in intervention vs 18 patients (20.9%) in control (P = .14). Comparing decision-making measures between groups at baseline to 6 months, there were significant decreases in perceived breast cancer risk and in breast cancer worry (standard mean differences = -0.48 and -0.40, respectively).

Conclusions and relevance: This randomized clinical trial did not find a significant increase in genetic counseling uptake among patients who received patient and clinician decision support vs those who received standard education, although more than one-third of the ethnically diverse women enrolled in the intervention underwent genetic counseling. These findings suggest that the main advantage for these high-risk women is the ability to opt for screening and preventive services to decrease their cancer risk.

Trial registration: ClinicalTrials.gov Identifier: NCT03470402.

Conflict of interest statement

Conflict of Interest Disclosures: Dr Terry reported receiving grants from the National Institutes of Health during the conduct of the study. No other disclosures were reported.

Figures

Figure.. Study Flow Diagram
Figure.. Study Flow Diagram
EHR indicates electronic health record.

References

    1. Dorling L, Carvalho S, Allen J, et al. ; Breast Cancer Association Consortium . Breast cancer risk genes - association analysis in more than 113,000 women. N Engl J Med. 2021;384(5):428-439. doi:10.1056/NEJMoa1913948
    1. Hu C, Hart SN, Gnanaolivu R, et al. . A population-based study of genes previously implicated in breast cancer. N Engl J Med. 2021;384(5):440-451. doi:10.1056/NEJMoa2005936
    1. Risch HA, McLaughlin JR, Cole DE, et al. . 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. Anglian Breast Cancer Study Group . Prevalence and penetrance of BRCA1 and BRCA2 mutations in a population-based series of breast cancer cases. Br J Cancer. 2000;83(10):1301-1308. doi:10.1054/bjoc.2000.1407
    1. Harter P, Hauke J, Heitz F, et al. . Prevalence of deleterious germline variants in risk genes including BRCA1/2 in consecutive ovarian cancer patients (AGO-TR-1). PLoS One. 2017;12(10):e0186043. doi:10.1371/journal.pone.0186043
    1. Sutcliffe S, Pharoah PD, Easton DF, Ponder BA. Ovarian and breast cancer risks to women in families with two or more cases of ovarian cancer. Int J Cancer. 2000;87(1):110-117. doi:10.1002/1097-0215(20000701)87:1<110::AID-IJC16>;2-6
    1. Singletary SE. Rating the risk factors for breast cancer. Ann Surg. 2003;237(4):474-482. doi:10.1097/01.SLA.0000059969.64262.87
    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. Owens DK, Davidson KW, Krist AH, et al. ; US Preventive Services Task Force . Risk assessment, genetic counseling, and genetic testing for BRCA-related cancer: US Preventive Services Task Force Recommendation Statement. JAMA. 2019;322(7):652-665. doi:10.1001/jama.2019.10987
    1. Kuchenbaecker KB, Hopper JL, Barnes DR, et al. ; BRCA1 and BRCA2 Cohort Consortium . 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. Antoniou A, Pharoah PD, Narod S, et al. . Average risks of breast and ovarian cancer associated with BRCA1 or BRCA2 mutations detected in case series unselected for family history: a combined analysis of 22 studies. Am J Hum Genet. 2003;72(5):1117-1130. doi:10.1086/375033
    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. Saslow D, Boetes C, Burke W, et al. ; American Cancer Society Breast Cancer Advisory Group . 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, et al. . 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 AE, 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, et al. . 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, et al. . Mortality after bilateral salpingo-oophorectomy in BRCA1 and BRCA2 mutation carriers: a prospective cohort study. Lancet Oncol. 2006;7(3):223-229. doi:10.1016/S1470-2045(06)70585-X
    1. Domchek SM, Friebel TM, Singer CF, et al. . 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, et al. . 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, et al. . 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, et al. ; National Surgical Adjuvant Breast and Bowel Project . 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, et al. ; Hereditary Breast Cancer Clinical Study Group . 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. Rebbeck TR, Friebel T, Lynch HT, 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. Moyer VA; U.S. Preventive Services Task Force . 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. Moyer VA; U.S. Preventive Services Task Force . 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. 2013;22(4):728-735. doi:10.1158/1055-9965.EPI-12-1280
    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, et al. . Decision support for family history intake to determine eligibility for BRCA testing among multiethnic women. American Society of Clinical Oncology; 2017. doi:10.1200/JCO.2017.35.15_suppl.1586
    1. Joseph G, Kaplan C, Luce J, et al. . 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. Genet Med. 2008;10(6):404-414. 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, et al. . Barriers and facilitators to patient-provider communication when discussing breast cancer risk to aid in the development of decision support tools. Paper presented at: AMIA Annual Symposium Proceedings; 2015.
    1. Pal T, Cragun D, Lewis C, et al. . 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. Genet Med. 2009;11(10):735-741. doi:10.1097/GIM.0b013e3181b2e5eb
    1. Trivers KF, Baldwin L-M, Miller JW, et al. . Reported referral for genetic counseling or BRCA 1/2 testing among United States physicians: a vignette-based study. 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 U.S. 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, et al. . 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. Genet Med. 2003;5(2):70-76. 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. Community Genet. 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 (Millwood). 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, et al. . Barriers and facilitators to patient-provider communication when discussing breast cancer risk to aid in the development of decision support tools. AMIA Annu 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 Jt Summits Transl Sci Proc. 2017;2017:58-67.
    1. Coe AM, Ueng W, Vargas JM, et al. . Usability Testing of a Web-Based Decision Aid for Breast Cancer Risk Assessment Among Multi-Ethnic Women. Paper presented at: AMIA Annual Symposium Proceedings; 2016.
    1. Kukafka R, Fang J, Vanegas A, Silverman T, Crew KD. Pilot study of decision support tools on breast cancer chemoprevention for high-risk women and healthcare providers in the primary care setting. BMC Med Inform Decis Mak. 2018;18(1):134. doi:10.1186/s12911-018-0716-5
    1. Kukafka R, Yi H, Xiao T, et al. . 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. Silverman TB, Vanegas A, Marte A, et al. . Study protocol: a cluster randomized controlled trial of web-based decision support tools for increasing BRCA1/2 genetic counseling referral in primary care. BMC Health Serv Res. 2018;18(1):633. doi:10.1186/s12913-018-3442-x
    1. Mazzola E, Blackford A, Parmigiani G, Biswas S. Recent enhancements to the genetic risk prediction model BRCAPRO. Cancer Inform. 2015;14(Suppl 2):147-157. doi:10.4137/CIN.S17292
    1. Vogel KJ, Atchley DP, Erlichman J, et al. . 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. 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 Jt Summits Transl Sci Proc. 2017;2017:58-67.
    1. Silverman TB, Kuperman GJ, Vanegas A, et al. . An applied framework in support of shared decision making about BRCA genetic testing. AMIA Annu Symp Proc. 2018;2018:961-969.
    1. Chew LD, Griffin JM, Partin MR, et al. . 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):e27. doi:10.2196/jmir.8.4.e27
    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 Making. 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. Degner LF, Sloan JA, Venkatesh P. The Control Preferences Scale. Can J Nurs Res. 1997;29(3):21-43.
    1. Hall MA, Zheng B, Dugan E, et al. . Measuring patients’ trust in their primary care providers. Med Care Res Rev. 2002;59(3):293-318. doi:10.1177/1077558702059003004
    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. User manual - decisional conflict scale. Published 1993. Accessed June 22, 2022.
    1. Gurmankin Levy A, Shea J, Williams SV, Quistberg A, Armstrong K. Measuring perceptions of breast cancer risk. Cancer Epidemiol Biomarkers Prev. 2006;15(10):1893-1898. doi:10.1158/1055-9965.EPI-05-0482
    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). 1995. Accessed February 4, 2015.
    1. Marteau TM, Dormandy E, Michie S. A measure of informed choice. Health Expect. 2001;4(2):99-108. doi:10.1046/j.1369-6513.2001.00140.x
    1. Arun BK, Peterson SK, Sweeney LE, et al. . Increasing referral of at-risk women for genetic counseling and BRCA testing using a screening tool in a community breast imaging center. Cancer. 2022;128(1):94-102. doi:10.1002/cncr.33866
    1. Hoskins KF, Tejeda S, Vijayasiri G, et al. . A feasibility study of breast cancer genetic risk assessment in a federally qualified health center. Cancer. 2018;124(18):3733-3741. doi:10.1002/cncr.31635
    1. Morman NA, Byrne L, Collins C, Reynolds K, Bell JG. Breast cancer risk assessment at the time of screening mammography: perceptions and clinical management outcomes for women at high risk. J Genet Couns. 2017;26(4):776-784. doi:10.1007/s10897-016-0050-y
    1. van der Giessen JAM, Ausems MGEM, van den Muijsenbergh METC, van Dulmen S, Fransen MP. Systematic development of a training program for healthcare professionals to improve communication about breast cancer genetic counseling with low health literate patients. Fam Cancer. 2020;19(4):281-290. doi:10.1007/s10689-020-00176-3
    1. Sutton AL, Hurtado-de-Mendoza A, Quillin J, et al. . Reducing disparities in receipt of genetic counseling for underserved women at risk of hereditary breast and ovarian cancer. J Womens Health (Larchmt). 2020;29(8):1131-1135. doi:10.1089/jwh.2019.7984
    1. Pasick RJ, Joseph G, Stewart S, et al. . Effective referral of low-income women at risk for hereditary breast and ovarian cancer to genetic counseling: a randomized delayed intervention control trial. Am J Public Health. 2016;106(10):1842-1848. doi:10.2105/AJPH.2016.303312
    1. Law WK, Yaremych HE, Ferrer RA, Richardson E, Wu YP, Turbitt E. Decision-making about genetic health information among family dyads: a systematic literature review. Health Psychol Rev. Published online September 29, 2021. 2021. doi:10.1080/17437199.2021.1980083
    1. Lin JL, Lipstein EA, Wittenberg E, et al. . Intergenerational decision making: the role of family relationships in medical decision making. MDM Policy Pract. 2021;6(2):23814683211039468. doi:10.1177/23814683211039468
    1. Turbitt E, Lin JL. Genetic testing decisions in non-western cultures: an opportunity for intergenerational decision making. Eur J Hum Genet. 2022;30(4):391. doi:10.1038/s41431-021-01008-3
    1. Grimmett C, Pickett K, Shepherd J, et al. . Systematic review of the empirical investigation of resources to support decision-making regarding BRCA1 and BRCA2 genetic testing in women with breast cancer. Patient Educ Couns. 2018;101(5):779-788. doi:10.1016/j.pec.2017.11.016
    1. Mai PL, Vadaparampil ST, Breen N, McNeel TS, Wideroff L, Graubard BI. Awareness of cancer susceptibility genetic testing: the 2000, 2005, and 2010 National Health Interview Surveys. Am J Prev Med. 2014;46(5):440-448. doi:10.1016/j.amepre.2014.01.002
    1. Chapman-Davis E, Zhou ZN, Fields JC, et al. . Racial and ethnic disparities in genetic testing at a hereditary breast and ovarian cancer center. J Gen Intern Med. 2021;36(1):35-42. doi:10.1007/s11606-020-06064-x
    1. Chen L, Li CI. Racial disparities in breast cancer diagnosis and treatment by hormone receptor and HER2 status. Cancer Epidemiol Biomarkers Prev. 2015;24(11):1666-1672. doi:10.1158/1055-9965.EPI-15-0293
    1. Miller KD, Siegel RL, Lin CC, et al. . Cancer treatment and survivorship statistics, 2016. CA Cancer J Clin. 2016;66(4):271-289. doi:10.3322/caac.21349
    1. DeSantis CE, Fedewa SA, Goding Sauer A, Kramer JL, Smith RA, Jemal A. Breast cancer statistics, 2015: Convergence of incidence rates between Black and White women. CA Cancer J Clin. 2016;66(1):31-42. doi:10.3322/caac.21320
    1. Ooi SL, Martinez ME, Li CI. Disparities in breast cancer characteristics and outcomes by race/ethnicity. Breast Cancer Res Treat. 2011;127(3):729-738. doi:10.1007/s10549-010-1191-6
    1. DeSantis CE, Ma J, Goding Sauer A, Newman LA, Jemal A. Breast cancer statistics, 2017, racial disparity in mortality by state. CA Cancer J Clin. 2017;67(6):439-448. doi:10.3322/caac.21412
    1. Goedhart NS, Zuiderent-Jerak T, Woudstra J, Broerse JEW, Betten AW, Dedding C. Persistent inequitable design and implementation of patient portals for users at the margins. J Am Med Inform Assoc. 2021;28(2):276-283. doi:10.1093/jamia/ocaa273
    1. Bradway M, Pfuhl G, Joakimsen R, Ribu L, Grøttland A, Årsand E. Analysing mHealth usage logs in RCTs: explaining participants’ interactions with type 2 diabetes self-management tools. PLoS One. 2018;13(8):e0203202. doi:10.1371/journal.pone.0203202
    1. Holmen H, Torbjørnsen A, Wahl AK, et al. . A mobile health intervention for self-management and lifestyle change for persons with type 2 diabetes, part 2: one-year results from the Norwegian randomized controlled trial RENEWING HEALTH. JMIR Mhealth Uhealth. 2014;2(4):e57. doi:10.2196/mhealth.3882
    1. Wyatt KD, Branda ME, Anderson RT, et al. . Peering into the black box: a meta-analysis of how clinicians use decision aids during clinical encounters. Implement Sci. 2014;9:26. doi:10.1186/1748-5908-9-26
    1. Raphael Daniela DB, Russell NS, van Werkhoven E, et al. . Implementing a patient decision aid, a process evaluation of a large-scale pre- and post-implementation trial. Breast Cancer Res Treat. 2021;185(3):685-695. doi:10.1007/s10549-020-05975-x
    1. Joseph-Williams N, Abhyankar P, Boland L, et al. . What works in implementing patient decision aids in routine clinical settings? a rapid realist review and update from the international patient decision aid standards collaboration. Med Decis Making. 2021;41(7):907-937. doi:10.1177/0272989X20978208
    1. Herrmann A, Mansfield E, Hall AE, Sanson-Fisher R, Zdenkowski N. Wilfully out of sight? a literature review on the effectiveness of cancer-related decision aids and implementation strategies. BMC Med Inform Decis Mak. 2016;16:36. doi:10.1186/s12911-016-0273-8

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