Pilot Trial of Streamlined Genetic Education and Traceback Genetic Testing in Prostate Cancer Survivors

Authors:
Marc D. Schwartz Georgetown Lombardi Comprehensive Cancer Center, Georgetown University, Washington, DC
Jess and Mildred Fisher Center for Hereditary Cancer and Clinical Genomics Research, Georgetown University, Washington, DC

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Beth N. Peshkin Georgetown Lombardi Comprehensive Cancer Center, Georgetown University, Washington, DC
Jess and Mildred Fisher Center for Hereditary Cancer and Clinical Genomics Research, Georgetown University, Washington, DC

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Claudine Isaacs Georgetown Lombardi Comprehensive Cancer Center, Georgetown University, Washington, DC
Jess and Mildred Fisher Center for Hereditary Cancer and Clinical Genomics Research, Georgetown University, Washington, DC

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Christopher Grisham Georgetown Lombardi Comprehensive Cancer Center, Georgetown University, Washington, DC
Jess and Mildred Fisher Center for Hereditary Cancer and Clinical Genomics Research, Georgetown University, Washington, DC

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Nora J. Holmes Georgetown Lombardi Comprehensive Cancer Center, Georgetown University, Washington, DC

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Lia J. Sorgen Georgetown Lombardi Comprehensive Cancer Center, Georgetown University, Washington, DC
Jess and Mildred Fisher Center for Hereditary Cancer and Clinical Genomics Research, Georgetown University, Washington, DC

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Sean Collins Georgetown Lombardi Comprehensive Cancer Center, Georgetown University, Washington, DC

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Nancy Dawson Georgetown Lombardi Comprehensive Cancer Center, Georgetown University, Washington, DC

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Colleen McGuire Georgetown Lombardi Comprehensive Cancer Center, Georgetown University, Washington, DC

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Tobechukwu Okobi University of the District of Columbia, Washington, DC

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Kelsey Newell Georgetown Lombardi Comprehensive Cancer Center, Georgetown University, Washington, DC
Jess and Mildred Fisher Center for Hereditary Cancer and Clinical Genomics Research, Georgetown University, Washington, DC

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Kavitha A. Kolla Georgetown Lombardi Comprehensive Cancer Center, Georgetown University, Washington, DC
Jess and Mildred Fisher Center for Hereditary Cancer and Clinical Genomics Research, Georgetown University, Washington, DC

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Veronique Weinstein Georgetown Lombardi Comprehensive Cancer Center, Georgetown University, Washington, DC
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Background: Germline genetic testing is recommended for men with metastatic or high-risk prostate cancer to inform treatment and risk management for other cancers and inform genetic testing in at-risk relatives. However, relatively few patients with prostate cancer undergo genetic testing. Given the low rate of testing and increasing demands on genetic service providers, strategies are needed that reduce barriers to testing while conserving genetic counseling resources. The primary goal of this study was to determine whether a proactive and streamlined “traceback” approach could yield increased genetic testing participation among prostate cancer survivors. Methods: We randomized 107 survivors of metastatic and high-risk prostate cancer to streamlined testing (ST) versus enhanced usual care (EUC). ST participants were proactively provided with print genetic education materials and the option to proceed to genetic testing without pre-test genetic counseling. EUC participants were sent a letter from their physician advising them of their eligibility for genetic testing and recommending they schedule genetic counseling. The primary outcome was genetic testing participation. Secondary outcomes were distress, knowledge, decision satisfaction, and regret. Results: In the ST group, 41.5% of participants completed genetic testing compared with 27.8% in the EUC group. After adjusting for education and marital status, the odds of testing were more than twice as high for the ST group as for the EUC group (odds ratio, 2.57; 95% CI, 1.05–6.29). The groups did not differ on any of the psychosocial outcomes at the 3-month follow-up. Conclusions: Proactive outreach paired with streamlined genetic testing delivery may be a safe, effective, and resource-efficient approach to facilitate traceback genetic testing in prostate cancer survivors.

Background

Of the 288,300 men diagnosed with prostate cancer (PCa) annually in the United States,1 germline pathogenic variants (PVs) are present in 12% to 17% of those with regional or metastatic disease.25 PVs in the BRCA2 gene increase PCa risk up to 6-fold, are associated with poor disease outcomes, and are the most common PVs in individuals with PCa.411 NCCN Clinical Practice Guidelines in Oncology (NCCN Guidelines) for PCa recommend germline genetic testing for individuals with metastatic, regional, and high-risk PCa.1214 Identifying a PV in BRCA2 or other homologous recombination repair genes (eg, BRCA1, ATM, PALB2) is an indication for treatment with PARP inhibitors.1218 Furthermore, when a PV is identified in a patient with PCa, cascade genetic testing of family members provides risk reduction and early-detection options for several different cancers.11,19

Despite these benefits, few individuals with PCa undergo genetic testing.20,21 Limited data on men with PCa suggest that lack of awareness and physician referral drive low test uptake.22,23 This aligns with studies documenting low test uptake among men from families with hereditary breast and/or ovarian cancer.2426 However, evidence also suggests that men report a high interest in genetic testing,22,27 and those who attend a genetic counseling session get tested at rates comparable to women.28 Recent studies in patients with PCa suggest that novel approaches to delivering genetic testing via the internet or in-clinic mainstreaming yield higher test uptake.29,30

Such approaches align with recent changes in genetic service delivery. Given rapidly increasing demand for genetic services, genetic counseling capacity is a rate-limiting factor.31 Although traditional genetic counseling results in positive outcomes,32 the quantity, relevance, and complexity of the information provided by such comprehensive services do not always match patient needs.3336 This may be particularly true for people with a prior cancer diagnosis, for whom many issues covered in traditional genetic counseling may not be of primary concern. Furthermore, because most patients who meet clinical testing criteria will not be found to carry a PV, comprehensive pre-test genetic counseling may not be the most efficient way to meet the needs of patients with PCa and may be a barrier to testing.

In this study, we tested 2 approaches for implementing traceback genetic testing in PCa survivors. “Traceback testing” refers to genetic outreach in previously diagnosed but untested patients with cancer,37,38 and is relevant in PCa for several reasons. First, in addition to low test uptake among patients with PCa,20,21 many PCa survivors became retroactively eligible for testing with the 2018 expansion of NCCN’s recommendations for PCa genetic testing.39 Second, detecting a PV could have treatment implications for survivors who experience disease progression or recurrence. Finally, a PV has surveillance and prevention implications for other cancers for both the survivors and their relatives.

In this pilot randomized trial, we compared streamlined testing (ST) versus enhanced usual care (EUC). In the ST arm, we proactively delivered a print genetic education booklet to PCa survivors to provide sufficient information for informed decision-making regarding genetic testing without requiring pre-test genetic counseling. We compared this approach to EUC, in which participants were contacted via letter or email to inform them of their eligibility for genetic testing and encourage them to schedule genetic counseling. Although similar proactive and streamlined strategies have been described previously,29,40,41 this trial advances the field through its randomized trial design and focus on traceback testing in PCa survivors. We predicted that ST would yield increased genetic testing uptake and that few ST participants would request pre-test genetic counseling. We also compared the arms regarding psychosocial outcomes.

Methods

Participants

From 2020 to early 2021, we recruited PCa survivors into a parallel-group randomized, controlled trial comparing proactive outreach with streamlined genetic education and testing (ST) versus EUC. Eligible participants were diagnosed with metastatic or high-risk PCa in the prior 10 years, were aged 21 to 80 years, were seen for at least 1 follow-up since 2017, had no prior genetic testing, could communicate in English, and did not exhibit cognitive impairment that precluded study engagement (assessed by a trained research assistant [RA]).

As displayed in Figure 1, we identified 225 potentially eligible, investigator-assessed men, of whom 112 (49.8%) agreed to be randomized. However, 5 participants were determined to be ineligible after randomization, resulting in a final sample of 107 participants (ST, 53; EUC, 54). Of the 107 in the final sample, 105 (98.1%; ST, n=53; EUC, n=52) completed the 3-month follow-up assessment. Although blinding to study arm was not possible, we minimized bias through structured data collection via standardized measures.

Figure 1.
Figure 1.

Study participants.

aDue to errors in the baseline survey and/or medical record, 5 ineligible participants were randomized (3 to streamlined testing and 2 to enhanced usual care). Upon determination of these errors, these participants were removed from the trial, received no further follow-up, and were excluded from analysis.

bMissing: n=1.

cMissing: n=2.

Citation: Journal of the National Comprehensive Cancer Network 21, 12; 10.6004/jnccn.2023.7071

Procedure

The Georgetown University Institutional Review Board approved this study. Potentially eligible patients were identified from medical and radiation oncology provider clinic lists. We mailed (and emailed) an introductory letter describing the study, an opt-out postcard, informed consent document, and baseline survey. Two weeks after this mailing, an RA called patients who had neither opted out nor completed the baseline survey. Men contacted by telephone had the option to provide verbal consent and complete the baseline survey by telephone. After completion of the baseline survey, the RA randomized participants via computer-generated random numbers in blocks of 8. Approximately 3 months after randomization, participants completed a follow-up survey.

Streamlined Testing

The ST intervention included proactive outreach to eligible PCa survivors, print pre-test genetic education with streamlined genetic testing, genetic counseling disclosure for patients with a PV or variant of uncertain clinical significance (VUS), and a clinical disclosure letter for patients with a negative result. In place of pretest genetic counseling, ST participants were provided with a genetic education booklet developed by the research team that covered the key components of pretest genetic counseling (supplemental eAppendix 1, available with this article at JNCCN.org). The 12-page booklet, which includes text, images, illustrations, and graphics, could be reviewed in approximately 15 minutes. After reviewing the booklet, ST participants could proceed with genetic testing, decline genetic testing, or schedule a free telephone genetic counseling session. Those who requested genetic counseling were contacted by the study team and scheduled for telegenetic counseling with a board-certified genetic counselor through the telegenetics company GeneMatters. Those wishing to proceed directly to genetic testing notified the study team and were sent a DNA saliva collection kit, which was returned directly to the genetic testing laboratory (Invitae).

Enhanced Usual Care

EUC participants were sent a brief letter from their physician indicating that they meet eligibility criteria for genetic testing, recommending that they schedule a free telephone genetic counseling session, and providing a contact telephone number to schedule this session. After completing pre-test genetic counseling with a board-certified genetic counselor from GeneMatters, EUC participants could proceed to genetic testing.

Genetic Testing

Participants were offered a standard clinical multigene panel of 47 or 84 genes, including BRCA1/2, and genes for which PVs are associated with potential differential diagnoses. Testing was performed by Invitae, a CLIA-certified clinical laboratory. DNA was provided via at-home saliva collection kits and returned directly to Invitae. During this trial, participants were eligible for free genetic testing through Invitae’s Detect Hereditary PCa program.42 The specific panel for each participant was determined based on the panel offered through Invitae’s Detect program at the time of testing. One participant received a custom 85-gene panel.

ST participants found to carry a PV or VUS completed a free telephone disclosure session with a GeneMatters genetic counselor. ST participants with a negative test result were notified by email but had the option to schedule a free telephone disclosure session. EUC participants were scheduled for a free telephone disclosure session regardless of their results.

Measures

Sociodemographics

We assessed age (at study enrollment), race/ethnicity, education, marital status, number and sex of children, and employment status during the baseline survey.

Clinical Variables

We assessed family cancer history in the baseline survey. Time since PCa diagnosis and PCa treatment were obtained from clinic records and confirmed during the baseline survey.

Knowledge

We measured genetic knowledge at baseline and 3 months using 8 items from the KnowGene scale.43 We added 2 items (“Most men with prostate cancer do not have an inherited risk for cancer,” and “A genetic test can tell if someone will definitely get prostate cancer”). All items were answered on a true/false/don’t know scale, and correct items were summed for a total score.

Distress

We measured distress at baseline and 3 months with the Patient-Reported Outcomes Measurement Information System (PROMIS) Depression and Anxiety 6a static short forms.44 Higher scores indicate higher distress. Cronbach α ranged from 0.92 to 0.93.

Decision Regret and Satisfaction

We measured regret and satisfaction regarding the genetic testing decision at 3 months. For regret, we used the 5-item Decisional Regret Scale.45 Scores on this scale range from 5 to 25, with higher scores indicating greater remorse. For satisfaction, we used the 6-item Satisfaction With Decision scale.46 Scores on this scale range from 6 to 30, with higher scores indicating greater satisfaction. Internal consistency of both scales was high (Cronbach α ranged from 0.90 to 0.95).

Genetic Test Uptake

Our primary outcome was medical record–verified genetic testing. Four participants reported that they had received genetic testing outside the study. We verified 2 of these self-reports via medical records. Two self-reports could not be verified and were classified as not being tested.

Statistical Analyses

We compared the groups on genetic testing participation with a chi-square test followed by logistic regression adjusting for education and marital status—demographic factors that have predicted interest in and uptake of genetic counseling and testing in prior studies.4750 Adjustment for baseline variables associated with the primary outcome improves statistical efficiency and is advised by the European Medicines Agency and the FDA.51 In exploratory analyses, we compared the groups on knowledge, distress, decision satisfaction, and decision regret via multiple regression in which we adjusted for the baseline score on distress and knowledge, and Student t tests for decision satisfaction and decision regret, neither of which was measured at baseline. We used SAS 9.4 (SAS Institute Inc.) for all analyses.

Results

Table 1 displays the sociodemographic and clinical characteristics of the study sample.

Table 1.

Sample Characteristics

Table 1.

Genetic Testing and Genetic Counseling Participation

A total of 37 (34.6%) participants completed genetic testing: 22 (41.5%) in the ST arm and 15 (27.8%) in the EUC arm (chi-square [df=1; n=107] = 2.23; P=.14). Of the 37 individuals tested, 6 (16.2%; EUC, n=4; ST, n=2) were found to carry a PV (2 with APC and 1 each with ATM, PALB2, RECQL4, and PMS2). Both participants with an APC PV were Ashkenazi Jewish and carried the I1307K founder variant. As shown in supplemental eTable 1, 15 (40.5%) participants received VUS results. Three participants with a VUS result also carried a PV.

In the ST arm (n=53), 19 (35.8%) participants proceeded directly to genetic testing, 3 (5.7%) requested genetic counseling prior to testing, and 31 (58.4%) declined counseling and testing. In the EUC arm (n=54), 15 (27.8%) participants completed genetic counseling prior to genetic testing, 3 (5.6%) declined genetic testing following genetic counseling, and 36 (66.7%) declined counseling and testing.

Multivariate Model of Genetic Testing Uptake

After adjusting for education and marital status (Table 2), the odds of completing genetic testing were more than double for the ST group versus the EUC group (odds ratio [OR], 2.57; 95% CI, 1.05–6.29; P=.039). Higher educational attainment was associated with increased odds of testing (OR, 3.24; 95% CI, 1.29–8.13; P=.012), and being married or partnered was associated with decreased odds of testing (OR, 0.27; 95% CI, 0.10–0.71; P=.008).

Table 2.

Logistic Regression Predicting Genetic Test Uptake

Table 2.

Psychosocial Outcomes

At 3 months (Table 3), after adjusting for baseline scores on the outcome of interest, the groups did not differ on knowledge, anxiety, or depression. For decisional regret and satisfaction, Student t tests at 3 months indicated that the groups did not differ. Both groups exhibited modest distress, low regret, and high decision satisfaction.

Table 3.

Group Comparison on Psychosocial Outcomes

Table 3.

Discussion

In this pilot randomized trial, 41.5% of participants in the ST arm underwent genetic testing compared with 27.8% in the EUC arm, a difference that was statistically significant after adjusting for education and marital status. Only 5.7% of participants in the ST arm pursued optional pre-test genetic counseling, which is consistent with emerging research documenting a preference for alternatives to traditional genetic counseling.27,52 We found no evidence of adverse psychosocial or decision-making outcomes in either arm.

The 41.5% of ST participants who were tested is comparable to 2 recent studies in which 21% to 46% of breast and ovarian cancer survivors opted for traceback testing when it was offered without required pre-test genetic counseling.37,53 This is higher than the 1.2% of ovarian cancer survivors who completed required genetic counseling when contacted as part of a hospital-based traceback program.54 To our knowledge, this is the first trial to demonstrate that a streamlined testing process without required pre-test genetic counseling yields higher uptake of traceback testing compared with a traditional approach. This is also the first study to document the feasibility and acceptability of traceback testing in PCa survivors.

Overall, 6 participants tested positive for a PV (16.2%). Five participants had a PV in a high- or moderate-risk gene and 1 was a heterozygote carrier for RECQL4, which is not known to be associated with an increased cancer risk. Two participants were carriers of PVs in PALB2 and ATM, both of which are associated with metastatic PCa and are indications for treatment with PARP inhibitors.5562 One participant carried a PV in the Lynch syndrome gene PMS2, but had no personal or family history of colon, uterine, or other Lynch-associated cancers. Similarly, 2 Ashkenazi Jewish participants with no reported history of colorectal cancer carried the APC founder I1307K variant, which is associated with a moderately increased colorectal cancer risk.63 These results are consistent with prior studies41,64 in demonstrating that genetic testing using a pan-cancer panel can identify PVs in genes that are not suspected based on personal or family history. Thus, although the 6 PV results may have limited clinical utility for the participants, partly owing to their advanced age or general health, a potential benefit of traceback testing in PCa is the identification of previously unrecognized hereditary cancer predispositions and the relevance this has for at-risk relatives.

Although these results suggest that proactive outreach and streamlined genetic testing yield increased uptake of genetic testing, it is worth noting that nearly 30% of EUC participants also opted for genetic testing. The EUC condition consisted simply of print or email outreach recommending genetic counseling. Thus, a potential implication is that even a short, written note from the treating physician with information about how to obtain genetic counseling and/or testing could yield increased uptake. Although this study focused on survivors, it may also have implications for new patients with PCa. If oncology providers are willing to provide point-of-care testing to newly diagnosed patients, then brief print materials such as the booklet used in this trial could obviate the need for routine pre-test counseling. Patients could then obtain post-test counseling from their providers or be referred for genetic counseling. In these scenarios, not only would limited genetic counseling resources be conserved but also test uptake would likely increase. It is likely that this approach during the PCa diagnostic or treatment trajectory would yield higher testing rates than in the traceback setting and would be inexpensive to deploy.29,65 The fact that so few participants in the ST arm requested pre-test genetic counseling suggests that this approach is likely to be acceptable to most patients. Based on the needs and preferences of various patient populations, future studies could assess optimal educational modalities and which patients are more likely to benefit from pre-test counseling.

Our results are limited by the modest sample size. Larger trials are needed to determine the best approach for increasing genetic testing in patients with PCa. Although half of eligible patients participated in this trial, those who declined likely had lower interest in testing. Future research is needed to better understand why the majority of PCa survivors who participated in the trial declined testing. The long time since diagnosis for many of our participants may have led to diminished interest; patients diagnosed more recently would likely have greater interest in testing. The availability of free genetic testing for all individuals with PCa at the time of the study likely increased test uptake. Testing costs have declined, and individuals with insurance can usually be tested with low or no out-of-pocket cost, but it is still critical to evaluate these approaches in the absence of free testing. Finally, in contrast to a recent study in men with metastatic PCa,30 married men were less likely to proceed with genetic testing. This unexpected finding should be considered extremely cautiously, given our limited sample size.

Conclusions

Our findings suggest that pre-test genetic counseling may not be necessary if basic educational material is provided, coupled with post-test counseling for patients with positive and VUS results. Proactive outreach paired with streamlined genetic testing delivery may be a safe, effective, and resource-efficient approach to enhance access to and participation in genetic testing in PCa survivors. A similar approach should be tested in patients with newly diagnosed PCa.

Acknowledgments

The authors are grateful to all the patients who participated in this study.

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Submitted March 2, 2023; final revision received July 26, 2023; accepted for publication August 16, 2023.

Author contributions: Conceptualization: Schwartz, Peshkin, Isaacs, Collins, Dawson, Okobi, Newell, Kolla, Weinstein. Data curation: Schwartz, Grisham, Holmes, Sorgen, Collins, Dawson, McGuire. Formal analysis: Schwartz, Okobi. Funding acquisition: Schwartz. Investigation: Schwartz, Peshkin, Issacs, Holmes, Sorgen, McGuire, Newell, Kolla, Weinstein. Methodology: Schwartz, Peshkin, Isaacs, Okobi, Newell, Kolla. Project administration: Peshkin, Grisham, Holmes, Sorgen, McGuire. Resources: Schwartz, Issacs, Collins, Dawson. Supervision: Schwartz, Peshkin, Sorgen, McGuire. Validation: Holmes, Sorgen. Writing—original draft: Schwartz, Peshkin, Grisham. Writing—review & editing: All authors.

Disclosures: Dr. Isaacs has disclosed receiving institutional funding from GSK, Seagen, Pfizer, AstraZeneca, Bristol Myers Squibb, Genentech, and Novartis; serving as a consultant for Genentech, Puma Biotechnology, Inc., Seagen, AstraZeneca, Novartis, Pfizer, and Gilead Sciences, Inc.; and serving on a data safety monitoring board for Novartis. The remaining authors have disclosed that they have not received any financial consideration from any person or organization to support the preparation, analysis, results, or discussion of this article.

Funding: Research reported in this publication was supported by the Jess and Mildred Fisher Center for Hereditary Cancer and Clinical Genomics Research (M.D. Schwartz), and the National Cancer Institute of the National Institutes of Health under award number P30CA051008.

Disclaimer: The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Correspondence: Marc D. Schwartz, PhD, Georgetown Lombardi Comprehensive Cancer Center, Georgetown University, 2115 Wisconsin Avenue NW, Suite 300, Washington, DC 20007. Email: schwartm@georgetown.edu

Supplementary Materials

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  • Figure 1.

    Study participants.

    aDue to errors in the baseline survey and/or medical record, 5 ineligible participants were randomized (3 to streamlined testing and 2 to enhanced usual care). Upon determination of these errors, these participants were removed from the trial, received no further follow-up, and were excluded from analysis.

    bMissing: n=1.

    cMissing: n=2.

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