Uptake and acceptability of a mainstreaming model of hereditary cancer multigene panel testing among patients with ovarian, pancreatic, and prostate cancer

Jada G Hamilton, Heather Symecko, Kelsey Spielman, Kelsey Breen, Rebecca Mueller, Amanda Catchings, Magan Trottier, Erin E Salo-Mullen, Ibrahim Shah, Anna Arutyunova, Melissa Batson, Rebecca Gebert, Stacy Pundock, Elizabeth Schofield, Kenneth Offit, Zsofia K Stadler, Karen Cadoo, Maria I Carlo, Vivek Narayan, Kim A Reiss, Mark E Robson, Susan M Domchek, Jada G Hamilton, Heather Symecko, Kelsey Spielman, Kelsey Breen, Rebecca Mueller, Amanda Catchings, Magan Trottier, Erin E Salo-Mullen, Ibrahim Shah, Anna Arutyunova, Melissa Batson, Rebecca Gebert, Stacy Pundock, Elizabeth Schofield, Kenneth Offit, Zsofia K Stadler, Karen Cadoo, Maria I Carlo, Vivek Narayan, Kim A Reiss, Mark E Robson, Susan M Domchek

Abstract

Purpose: To address demands for timely germline information to guide treatments, we evaluated experiences of patients with ovarian, pancreatic, and prostate cancer with a mainstreaming genetic testing model wherein multigene panel testing was ordered by oncologists with standardized pretest patient education, and genetic counselors delivered results and post-test genetic counseling via telephone.

Methods: Among 1,203 eligible patients, we conducted a prospective single-arm study to examine patient uptake and acceptability (via self-report surveys at baseline and three weeks and three months following result return) of this mainstreaming model.

Results: Only 10% of eligible patients declined participation. Among 1,054 tested participants, 10% had pathogenic variants (PV), 16% had variants of uncertain significance (VUS), and 74% had no variant identified (NV). Participants reported high initial acceptability, including high satisfaction with their testing decision. Variability over time in several outcomes existed for participants with PV or NV: those with NV experienced a temporary increase in depression (pTime < 0.001; pTime2 < 0.001), and those with PV experienced a small increase in genetic testing distress (p = 0.03). Findings suggested that result type, sex, and cancer type were also associated with outcomes including clinical depression and uncertainty.

Conclusion: This mainstreaming model may offer a feasible approach for extending access to germline genetic information.

Conflict of interest statement

Conflict of Interest Notification

Disclosure: The authors have no conflicts of interest.

© 2021. The Author(s), under exclusive licence to the American College of Medical Genetics and Genomics.

Figures

Figure 1.
Figure 1.
Study enrollment. PV = pathogenic variant; NV = no variant; VUS = variant of uncertain significance. * Thereafter, all percentages taken from total number of consented patients. ** Due to an administrative error, a subset of participants was not sent invitations to complete the 3-month follow-up survey. *** Total value includes participants who missed the 3-week follow-up survey but completed the 3-month follow-up survey.
Figure 2.
Figure 2.
Changes in patient acceptability of the mainstreaming model over time among participants with different MGPT results. T1 = baseline; T2 = 3-week follow-up; T3 = 3-month follow-up; GC = genetic counseling; HADS = Hospital Anxiety and Depression Scale; MICRA = Multidimensional Impact of Cancer Risk Assessment; PV = pathogenic variant; NV = no variant; VUS = variant of uncertain significance. GC Satisfaction and MICRA subscales were only assessed at T2 and T3. Significant (p

References

    1. Yap TA, Plummer R, Azad NS, Helleday T. The DNA damaging revolution: PARP inhibitors and beyond. American Society of Clinical Oncology Educational Book. 2019(39):185–195.
    1. McCuaig JM, Armel SR, Care M, Volenik A, Kim RH, Metcalfe KA. Next-generation service delivery: A scoping review of patient outcomes associated with alternative models of genetic counseling and genetic testing for hereditary cancer. Cancers (Basel). 2018;10(11).
    1. Buchanan AH, Rahm AK, Williams JL. Alternate service delivery models in cancer genetic counseling: A mini-review. Front Oncol. 2016;6:120.
    1. Cohen SA, Huziak RC, Gustafson S, Grubs RE. Analysis of advantages, limitations, and barriers of genetic counseling service delivery models. J Genet Couns. 2016;25(5):1010–1018.
    1. Greenberg SE, Boothe E, Delaney CL, Noss R, Cohen SA. Genetic counseling service delivery models in the United States: Assessment of changes in use from 2010 to 2017. J Genet Couns. 2020;29(6):1126–1141.
    1. Schwartz MD, Valdimarsdottir HB, Peshkin BN, et al. Randomized noninferiority trial of telephone versus in-person genetic counseling for hereditary breast and ovarian cancer. J Clin Oncol. 2014;32(7):618–626.
    1. Kinney AY, Butler KM, Schwartz MD, et al. Expanding access to BRCA1/2 genetic counseling with telephone delivery: A cluster randomized trial. J Natl Cancer Inst. 2014;106(12).
    1. Bradbury AR, Patrick-Miller LJ, Egleston BL, et al. Randomized noninferiority trial of telephone vs in-person disclosure of germline cancer genetic test results. J Natl Cancer Inst. 2018;110(9):985–993.
    1. Wright S, Porteous M, Stirling D, et al. Patients’ views of treatment-focused genetic testing (TFGT): Some lessons for the mainstreaming of BRCA1 and BRCA2 testing. J Genet Couns. 2018;27(6):1459–1472.
    1. George A, Riddell D, Seal S, et al. Implementing rapid, robust, cost-effective, patient-centred, routine genetic testing in ovarian cancer patients. Sci Rep. 2016;6:29506.
    1. Colombo N, Huang G, Scambia G, et al. Evaluation of a streamlined oncologist-led BRCA mutation testing and counseling model for patients with ovarian cancer. J Clin Oncol. 2018;36(13):1300–1307.
    1. Hoberg-Vetti H, Bjorvatn C, Fiane BE, et al. BRCA1/2 testing in newly diagnosed breast and ovarian cancer patients without prior genetic counselling: The DNA-BONus study. Eur J Hum Genet. 2015;24(6):881–888.
    1. McLeavy L, Rahman B, Kristeleit R, et al. Mainstreamed genetic testing in ovarian cancer: Patient experience of the testing process. Int J Gynecol Cancer. 2019;30(2):221–226.
    1. Scheinberg T, Young A, Woo H, Goodwin A, Mahon KL, Horvath LG. Mainstream consent programs for genetic counseling in cancer patients: A systematic review. Asia Pac J Clin Oncol. 2020.
    1. Quinn VF, Meiser B, Kirk J, et al. Streamlined genetic education is effective in preparing women newly diagnosed with breast cancer for decision making about treatment-focused genetic testing: A randomized controlled noninferiority trial. Genet Med. 2017;19(4):448–456.
    1. Robson ME, Bradbury AR, Arun B, et al. American Society of Clinical Oncology policy statement update: Genetic and genomic testing for cancer susceptibility. J Clin Oncol. 2015;33(31):3660–3667.
    1. Hamilton JG, Robson ME. Psychosocial effects of multigene panel testing in the context of cancer genomics. Hastings Cent Rep. 2019;49 Suppl 1:S44–S52.
    1. Scheinberg T, Goodwin A, Ip E, et al. Evaluation of a mainstream model of genetic testing for men with prostate cancer. JCO Oncology Practice. 2021;17(2):e204–e216.
    1. Oken MM, Creech RH, Tormey DC, et al. Toxicity and response criteria of the Eastern Cooperative Oncology Group. Am J Clin Oncol. 1982;5(6):649–656.
    1. Holmes-Rovner M, Kroll J, Schmitt N, et al. Patient satisfaction with health care decisions: The Satisfaction with Decision scale. Med Decis Making. 1996;16(1):58–64.
    1. DeMarco TA, Peshkin BN, Mars BD, Tercyak KP. Patient satisfaction with cancer genetic counseling: A psychometric analysis of the Genetic Counseling Satisfaction Scale. J Genet Couns. 2004;13(4):293–304.
    1. Zigmond AS, Snaith RP. The Hospital Anxiety and Depression Scale. Acta Psychiatr Scand. 1983;67(6):361–370.
    1. Cella D, Hughes C, Peterman A, et al. A brief assessment of concerns associated with genetic testing for cancer: The Multidimensional Impact of Cancer Risk Assessment (MICRA) questionnaire. Health Psychol. 2002;21(6):564–572.
    1. Garamszegi LZ. Comparing effect sizes across variables: Generalization without the need for Bonferroni correction. Behav Ecol. 2006;17(4):682–687.
    1. Chen H, Cohen P, Chen S. How big is a big odds ratio? Interpreting the magnitudes of odds ratios in epidemiological studies. Commun Stat - Simul. 2010;39(4):860–864.
    1. Jagsi R, Griffith KA, Kurian AW, et al. Concerns about cancer risk and experiences with genetic testing in a diverse population of patients with breast cancer. J Clin Oncol. 2015;33(14):1584–1591.
    1. Cragun D, Weidner A, Lewis C, et al. Racial disparities in BRCA testing and cancer risk management across a population-based sample of young breast cancer survivors. Cancer. 2017;123(13):2497–2505.
    1. Nikolaidis C, Duquette D, Mendelsohn-Victor KE, et al. Disparities in genetic services utilization in a random sample of young breast cancer survivors. Genet Med. 2018;21(6):1363–1137.
    1. Rohrmoser A, Pichler T, Letsch A, et al. Cancer patients’ expectations when undergoing extensive molecular diagnostics-A qualitative study. Psychooncology. 2020;29(2):423–429.
    1. Roberts JS, Gornick MC, Le LQ, et al. Next-generation sequencing in precision oncology: Patient understanding and expectations. Cancer Med. 2019;8(1):227–237.
    1. Bauer MR, Bright EE, MacDonald JJ, Cleary EH, Hines OJ, Stanton AL. Quality of life in patients with pancreatic cancer and their caregivers: A systematic review. Pancreas. 2018;47(4):368–375.
    1. Hamilton JG, Lobel M, Moyer A. Emotional distress following genetic testing for hereditary breast and ovarian cancer: A meta-analytic review. Health Psychol. 2009;28(4):510–518.
    1. Vansenne F, Bossuyt PM, de Borgie CA. Evaluating the psychological effects of genetic testing in symptomatic patients: A systematic review. Genet Test Mol Biomarkers. 2009;13(5):555–563.
    1. Culver JO, Ricker CN, Bonner J, et al. Psychosocial outcomes following germline multigene panel testing in an ethnically and economically diverse cohort of patients. Cancer. 2021;127(8):1275–1285.
    1. Idos GE, Kurian AW, Ricker C, et al. Multicenter prospective cohort study of the diagnostic yield and patient experience of multiplex gene panel testing for hereditary cancer risk. JCO Precision Oncology. 2019(3):1–12.
    1. Peters MLB, Stobie L, Dudley B, et al. Family communication and patient distress after germline genetic testing in individuals with pancreatic ductal adenocarcinoma. Cancer. 2019;125(14):2488–2496.
    1. Mighton C, Shickh S, Uleryk E, Pechlivanoglou P, Bombard Y. Clinical and psychological outcomes of receiving a variant of uncertain significance from multigene panel testing or genomic sequencing: A systematic review and meta-analysis. Genet Med. 2021;23(1):22–33.
    1. Medendorp NM, van Maarschalkerweerd PEA, Murugesu L, Daams JG, Smets EMA, Hillen MA. The impact of communicating uncertain test results in cancer genetic counseling: A systematic mixed studies review. Patient Educ Couns. 2020;103(9):1692–1708.
    1. Schupmann W, Jamal L, Berkman BE. Re-examining the ethics of genetic counselling in the genomic era. J Bioeth Inq. 2020;17(3):325–335.
    1. Offit K, Tkachuk KA, Stadler ZK, et al. Cascading after peridiagnostic cancer genetic testing: An alternative to population-based screening. J Clin Oncol. 2020;38(13):1398–1408.

Source: PubMed

Sponsoren und Mitarbeiter

Krankheiten

Drogeninterventionen

3
Abonnieren