The promise of genomics to improve population health has been forecasted for decades. Currently, access to most genomic health services relies on primary care clinicians and specialists to recognize patients eligible for genomic services and either offer genomic testing directly or make referrals to geneticists and genetic counselors [1, 2]. However, this approach is not equitable in reach as it relies on clinicians’ knowledge of genomic services and patients’ ability to access and actively navigate complex health care delivery systems. While there has been incremental improvement in access across various clinical contexts, including presymptomatic testing, diagnostic testing, and carrier screening, genomic health care disparities persist in marginalized populations (e.g., on the basis of socioeconomic status, race, ethnicity, gender identities, sexual orientations, health literacy, English proficiency) [3‒6].

Leveraging patients’ affiliations with health care delivery systems and partnering with the health care system on clinically embedded research is one strategy to improve access to and use of evidence-based genomics care in marginalized populations [7]. While this approach will not reach those who are not affiliated with a health system, it can address gaps for those receiving care within those systems [8]. The recently completed Cancer Health Assessments Reaching Many (CHARM) study used this strategy to evaluate the feasibility and acceptability of interventions designed to address inequities in cancer genetics services for adults and thereby advance the goal of equitable genomic health care [9]. This paper synthesizes lessons from CHARM that we believe illustrate the types of innovations that are needed to expand the reach and inclusivity of genomic medicine.

CHARM was conducted at Kaiser Permanente Northwest, an integrated health system in Oregon and Southwest Washington, and Denver Health, an integrated safety-net health system based in Denver, CO, USA. Both systems include individuals who have income-based health coverage through state assistance programs. The goal of CHARM was to engage patients belonging to marginalized populations who have not historically had access to genomic services in assessment for hereditary cancer risk and, potentially, genetic testing. To achieve this goal, we prioritized recruiting from locations serving patient populations with a high proportion of individuals from minoritized racial and ethnic groups and/or without health insurance; we also specifically considered inclusion of people with limited educational attainment [10, 11] and those who used Spanish as their preferred language for health care [12] in the development of study materials and processes.

To improve reach, CHARM created a novel, system-embedded approach (Fig. 1) to identify people at increased genetic risk for cancer. Traditionally, the initial step in genetic screening for hereditary cancer risk is for clinicians to collect family history to identify those who have a significant family history to warrant further evaluation, followed by referral to a genetic counselor to assess risk and, when indicated, recommend appropriate genetic testing. Testing is then ordered, and patients return to the genetic counselor for results disclosure and follow-up care recommendations [13]. Follow-up care could be arranged by primary care clinicians, geneticists, or the patient themselves (Fig. 1). In contrast to the traditional approach, the CHARM approach, which included twelve interventions intended to streamline the genomics care process (Table 1), simplified the process by allowing most of the steps to be done remotely (without clinician-controlled gatekeeping checkpoints). All aspects of CHARM, including genetic counseling and results disclosure, were available in both English and Spanish.

Fig. 1.

Compared to typical clinical processes, most CHARM study processes were self-directed, and all could be done remotely.

Fig. 1.

Compared to typical clinical processes, most CHARM study processes were self-directed, and all could be done remotely.

Close modal
Table 1.

CHARM approaches address each testing step to identify people for management of hereditary cancer syndromes

Genomic testing stepsCHARM intervention approach
Initial engagement with individuals 1. Email/text/in person 
Family history collection 2. Patient-facing digital tool 
3. Ask about limited family history 
Risk assessment 4. Automated risk assessment 
Test decision 5. Digital informed consent 
6. Decision aid for secondary findings 
Test 7. Home saliva collection 
Results disclosure 8. Genetic counselor ARIA training 
9. ARIA genetic counseling 
10. Conducted by phone 
11. Spanish interpreter genomics training 
12. Normal results conveyed by letter 
Genomic testing stepsCHARM intervention approach
Initial engagement with individuals 1. Email/text/in person 
Family history collection 2. Patient-facing digital tool 
3. Ask about limited family history 
Risk assessment 4. Automated risk assessment 
Test decision 5. Digital informed consent 
6. Decision aid for secondary findings 
Test 7. Home saliva collection 
Results disclosure 8. Genetic counselor ARIA training 
9. ARIA genetic counseling 
10. Conducted by phone 
11. Spanish interpreter genomics training 
12. Normal results conveyed by letter 

ARIA, accessible, inclusive, relational, actionable.

Outreach for CHARM recruitment was conducted via email, text, and in person between August 2018 and March 2020. Family cancer history collection used a literacy- and culturally focused digital tool to identify those at clinically significant risk and therefore eligible to enroll in the study [11]. People were also eligible to enroll if there was insufficient family history information available (limited family size, adoption, or limited knowledge) to assess risk. Eligible patients were immediately directed to the literacy-focused digital consent form. Those who enrolled were provided a saliva collection kit. An exome-based panel evaluated participants for cancer risk and other medically actionable secondary findings [9, 14].

Genetic counselors disclosed results to most participants by phone, using medical interpreters for participants who preferred to communicate in Spanish. For a subset of participants, normal results (defined as no reported variants classified as pathogenic, likely pathogenic, or uncertain significance) were disclosed by mailed letter from a genetic counselor. We compared standard genetic counseling [15] with a novel genetic counseling practice model aimed at making genetic counseling more inclusive [16]. All genetic test results were incorporated into the medical record.

The CHARM study implemented approaches from other fields, namely, multilevel, health system-embedded interventions and communication strategies, and applied them to the challenge of increasing access to genomic medicine, particularly for marginalized populations who experience additional barriers to care. Here, we share our learnings from implementing these key innovations throughout the genomics care delivery process.

A Multilevel Approach Is Essential to Increase Access to Recommended Genomic Care within Integrated Health Care Systems

CHARM implemented multiple interventions designed to work synergistically to improve delivery of genetic services and did this in partnership with health systems [17]. Though many of the interventions were not unique to CHARM, our choice to combine interventions addressing barriers at multiple levels of influence (e.g., health system, clinician, patient) was innovative and grounded in a body of research suggesting that multilevel approaches are essential for reducing barriers to recommended care for marginalized populations [18‒20]. We appreciated that the problem of limited access has many contributing influences, and only addressing a single influence in the process (see Fig. 1; Table 1) may not be sufficient to improve access. CHARM's approach successfully reached patients who may be missed by traditional care pathways. Further attention to using system-embedded approaches with health systems, and especially multilevel approaches that address patient, clinician, institutional, and societal influences is an important future direction for the field of genomic medicine.

By embedding CHARM within two health systems, we were able to increase the likelihood that improvements and lessons learned during the study would be adopted as part of usual care [21, 22]. CHARM helped create and sustain infrastructure for genomics by connecting key clinical partners, helping develop usual care workflows, and providing dedicated time for champions to engage in quality improvement work. Clinician education efforts and experiential learning that occurred as part of CHARM also helped improve clinicians’ abilities to identify patients at risk for hereditary cancer. This was particularly true for Denver Health, where participating in CHARM helped overcome existing genomics care gaps and has created a sustained increase in the number of genetic referrals in the health system, lasting beyond study cessation [23]. Thus, increasing genomics capacity had far-reaching ripple effects that broadened CHARMs benefits beyond study participants, representing an important pathway by which health system-embedded research can help translate genomics to population health improvements.

Relationship-Oriented Communication Strategies Are Important to Engage Marginalized Populations about Genomic Results

For broad reach, communication about genomic risk must be accessible to people of all literacy levels. We created a novel genetic counseling model aimed to make genetic counseling more inclusive by making the communication accessible, relational, and actionable (ARIA) [16]. While the content elements of the genetic counseling visit overlap with usual care, the focus in ARIA is on how the genetic counseling is conducted. The ARIA model emphasizes skills to enhance relationship-building, patient engagement, and comprehension and encourages genetic counselors to respond to patient priorities. A training curriculum for this model was completed by two genetic counselors on the CHARM team. This training included relationship-oriented communication skills such as establishing a few key messages for the visit, explaining those key messages without using genetic jargon, incorporating teach-back to create opportunities for clarification and reiteration of key messages, and making directive, personalized recommendations for next steps. Participants were randomized to ARIA or usual care genetic counseling to receive their test results [24]. Accuracy of recall of test results and perceived understanding were high for all participants; however, ARIA participants endorsed higher levels of relationship-building with their genetic counselor. In subgroup analyses, participants in the ARIA arm with lower health literacy reported less communication difficulty compared to those in the usual care arm. Additionally, participants using medical interpreters reported greater communication ease with ARIA compared to usual care. Collectively these results indicated that ARIA was of particular value for patients of lower health literacy and Spanish speakers using a medical interpreter, yet it can also be effective with patients across all populations. For genetic services to be accessible to broad populations, attention to effective communication approaches is critical and refinement of this work represents an important future direction.

Digital Materials and Remote Technologies Can Streamline the Delivery of Genomic Services to Reach Populations without Requiring In-Person Engagement

CHARM also leveraged patient-facing tools. One tool was developed to collect clinical information about patients and families to identify those who might be interested in genomic health services [25]. By implementing a patient-facing digital tool designed to facilitate population-wide screening within a health care system, we eliminated the need for a clinician to collect this information. A key consideration for this tool was to minimize the time and informational complexity for those using the tool, which was supported through close involvement of our patient advisors [11]. Ultimately, the tool resulted in high rates of completion and moderate agreement with a “gold standard” family history taken by a genetic counselor. We learned that most patients found the tool easy to navigate but reported needing to seek out additional family history information that was not always readily available [26]. We instituted a second tool, a digital genomics education and consent module designed to reduce the need for pre-test genetic counseling for those identified as at-risk based on family history. Pre-test counseling is a considerable demand on genetic counseling resources, which are already scarce. Participants found this literacy-focused tool acceptable and valued access to testing afforded by the study [10].

As noted in Figure 1, the CHARM process did not require in-person visits, in contrast to the traditional approach to genetic testing. The utilization of remote approaches can further reduce barriers and improve reach to people for whom an in-person visit is not feasible given, e.g., employment, transportation, or family caregiving responsibilities. Other remote technologies, such as chatbots, can further augment genetic counseling to support communication about testing decisions or results disclosure, even when people have specific questions [27]. In the future, system-embedded approaches that do not rely on in person primary care visits have great potential to increase reach. While primary care clinicians generally found CHARMs approach acceptable, they also expressed a desire to communicate more directly with the genetic counselors after result disclosure to understand how the patient reacted to their results as well as to discuss recommendations for clinical management.

Testing for Individuals with Limited Family History Is Necessary to Equitably Reach Genomic Testing across the Population

People were eligible to enroll in CHARM even if there was insufficient family history information available (limited family size, adoption, or limited knowledge) to assess risk, inspired by guidelines addressing the consideration of testing in the setting of limited family structure or knowledge [28, 29]. The rationale for these guidelines is that family history knowledge is a privilege; that is, it may vary with family norms, culture, fluency in medical terminology, access to medical care, and other factors. We found that of the 20% of individuals tested that met our criteria of having insufficient family history information, 1% had an abnormal result in a cancer risk gene [14]. For example, some LGBTQ+ participants reported that strained family relationships (e.g., caused by their biological family members’ lack of acceptance surrounding their sexual orientation and/or gender identities) led to limited family history knowledge and lower reported likelihood of sharing test results with genetically related family members [30]. Including those with limited family history information in initial screening eligibility criteria may allow for greater access to testing among patients from these and other marginalized groups [31]. Future health system-based approaches for cancer genomic testing may wish to consider including those with insufficient family history to have access to testing services.

A Diverse Research Workforce and Creating Ongoing Relationships with Patient Advisors Are Critical Aspects of Participant and Community Engagement

CHARMs ability to accomplish our goals related to community and participant engagement was facilitated by a diverse research workforce. For example, the purposeful decision to include native Spanish speakers within the research team, as both investigators and patient-facing research staff, allowed the creation of English materials that were most conducive to translation, creating a more culturally coherent intervention. LGBTQ+ team members also provided essential context based on their lived experience and guided the CHARM approach to expand study eligibility criteria to include people who did not have access to their family history information. To optimize team functioning on our diverse and multidisciplinary study, we intentionally incorporated lessons from team science [32]. Building and supporting a diverse research workforce, across multiple dimensions of diversity, will be essential to increase the reach of genomic medicine.

A critical aspect of community engagement in CHARM was to prioritize working with patient advisors over time rather than in one-time interactions. This allowed for the development of stronger relationships and allowed community members to understand and engage with content at a deeper level. CHARM had an English-speaking and a Spanish-speaking cohort of patient advisors with whom we engaged regularly [33]. The English-speaking cohort met as a group to provide input on study processes and patient-facing materials. Members of the Spanish-speaking cohort individually provided input on language choices and sociocultural acceptability. Additionally, 2 patient advisors remained engaged with the team throughout the project timeline and provided input on an ongoing basis. Incorporating patient advisors’ input highlighted opportunities to improve accessibility and utility of our study processes including the digital family history tool and informed consent process. While not all feedback could be incorporated as a result of differing institutional stakeholders’ perspectives and other constraints, the process of engagement encouraged our team to broaden our perspectives and better appreciate the experiences of our participants while designing and conducting our study [34].

Our experience in the CHARM Study illustrated the value of adopting multilevel, health system-embedded interventions and applying them to genomic medicine. CHARM demonstrated that relationship-focused communication strategies, as well as digital materials and remote technologies, streamlined delivery of genomic services and improved reach. It also illustrated the opportunity to make testing available for those who have a limited family history. Finally, it showed that longitudinal collaboration with small groups of patients over the course of a study meaningfully operationalized community engaged research in genomic medicine.

Additional research is needed to understand the scalability and long-term impact of innovations used in CHARM to develop analogous approaches in other clinical contexts. Relevant clinical scenarios include children with neurodevelopmental delay that could benefit from testing for an underlying genetic etiology, or adults making reproductive plans for whom carrier testing may be meaningful. The CHARM experience provides instructive examples of innovations needed to expand the reach of genomic discovery, particularly to marginalized populations, who experience additional barriers to genomic care.

We appreciate the assistance in developing this manuscript from Elizabeth Schuster (data), Lisa Fox (graphics), Jill Pope (editing), as well as Cassandra Angus, C. Samuel Peterson, and Summer Rivera (administrative). We are grateful to the CHARM participants, as well as the clinical and administrative leaders at KPNW and Denver Health who made CHARM possible. This manuscript builds on the efforts of the CHARM team that, as non-author contributors include: Jake Allen, Laura M. Amendola, Frank Angelo, Briana L. Arnold, Tiffany Bendelow, Kristin D. Breslin, Kristina F Booker, Mikaella Caruncho, James V. Davis, Sonia Deutsch, Michael O. Dorschner, Devan M. Duenas, Donna J. Eubanks, Amanda S. Freed, Inga Gruß, Claudia Guerra, Boya Guo, Joan Holup, Chalinya L. Ingphakorn, Paige Jackson, Gail Jarvik, Leah S. Karliner, Erin Keast, Alyssa H. Koomas, Mi H. Lee, Robin Lee, Hannah S. Lewis, Nangel M. Lindberg, Frances Lynch, Carmit K. McMullen, Elizabeth Medina, Sonia Okuyama, C. Samuel Peterson, Angela R. Paolucci, Chelese L. Ransom, Ana Reyes, Leslie S. Riddle, Sperry Robinson, Emily Schield, Kelly J. Shipman, Elizabeth Shuster, Sapna Syngal, Britta N. Torgrimson-Ojerio, Chinedu Ukaegbu, Meredith L. Vandermeer, Alexandra M. Varga, David L. Veenstra, W. Chris Whitebirch, and Larissa Lee White.

The authors have no financial or non-financial conflicts of interest to declare that are relevant to the content of this article.

This work was funded as part of the Clinical Sequencing Evidence-Generating Research (CSER) consortium funded by the National Human Genome Research Institute with co-funding from the National Institute on Minority Health and Health Disparities (NIMHD) and the National Cancer Institute (NCI). This work was supported by the National Human Genome Research Institute (U01HG007292; MPIs: Wilfond, Goddard, Leo), with additional support from U24HG007307 (Coordinating Center). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

The key approaches and lessons described in this manuscript were developed by a dissemination working group that included: Katherine Patrice Anderson, Marian J. Gilmore, Sarah Knerr, Joanna E. Bulkley, Beth Devine, Kristin R. Muessig, Alan F. Rope, Benjamin S. Wilfond, and Jamilyn M. Zepp; with input from other authors and non-author contributors who are part of CHARM. The manuscript was drafted by a core writing group that included: Marian J. Gilmore, Stephane A. Kraft, Sarah Knerr, and Benjamin S. Wilfond. The manuscript was reviewed and edited by Joanna E. Bulkley, Katherine Patrice Anderson, Barbara B. Biesecker, Beth Devine, Heather Spencer Feigelson, Katrina Goddard, Jessica Ezzell Hunter, Galen Joseph, Charisma L. Jenkins, Tia L. Kauffman, Sandra Soo-Jin Lee, Elizabeth G. Liles, Michael C. Leo, Kathleen F. Mittendorf, Kristin R. Muessig, Kathryn M. Porter, Bradley A. Rolf, Alan F. Rope, and Jamilyn M. Zepp. The manuscript was finalized by Marian J. Gilmore and Benjamin S. Wilfond, with contributions by Joanna E. Bulkley, Stephane A. Kraft, and Sarah Knerr. All authors reviewed and approved the manuscript.

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