The workshop’s fourth session discussed new approaches to ensuring that genetic and genomic services are available to all, including medically underserved populations. The speakers in this session, which was moderated by W. Gregory Feero, faculty in the Maine–Dartmouth Family Medical Residency Program, also identified areas where there are gaps in knowledge and suggested research projects that would help answer open questions. Marc Schwartz, a professor of oncology, a co-director of the cancer prevention and control program, and the research director at Georgetown University’s Fisher Center for Hereditary Cancer and Clinical Genomics Research, discussed alternative approaches to delivering genomic services, such as telemedicine. Rena Pasick, a professor in the department of medicine and the director of the office of community engagement at the University of California, San Francisco, Helen Diller Family Comprehensive Cancer Center, described her research on effective communication in genetic counseling for underserved populations. Jacquelyn Taylor, an associate professor and the Vernice D. Ferguson Chair in Health Equity at the New York University Rory Meyers College of Nursing, discussed the value of forming community collaborations with minority groups. Todd Skaar, an associate professor of medicine at the Indiana University School of Medicine, discussed the role of pharmacogenomics in decreasing genomic health disparities. Following the four presentations, Feero guided an open discussion between the speakers and workshop participants regarding possible approaches to mitigating genomic health disparities.
“Is medical genomics a form of ‘genetic exceptionalism’?” Feero asked in his introduction to the session. He defined the concept of genetic exceptionalism as the belief that genetic information is unique and therefore must be treated differently than other types of medical data or personally identifiable information. Feero argued that because genetic and genomic data are applicable to so much of health care and are not limited to just one disease, it is rational to treat it differently in regard to health disparities.
“We are beginning to ask the question of whether or not our whole health system should be revised to integrate [genomic] information in a systematic way, moving from average-based care or mean-based care to a more individualized approach,” Feero said. “We have to make sure we are doing a better job of carrying all parts of society along for the ride.” Doing so is important because the consequences of needless and preventable disease in a family that has fewer resources are much bigger than they are to an affluent, well-resourced family. “It is very important that we get this right for less-resourced populations,” said Feero.
Marc Schwartz said that there are several reasons why he and his colleagues have been trying to develop and evaluate alternative approaches to genomic services, particularly for hereditary breast and ovarian cancers (HBOCs). These reasons include
- a shortage of providers;
- an uneven geographic distribution of providers, with clusters of genetic providers in urban areas and centered around academic medical centers;
- varied and therefore suboptimal access to services in many parts of the country;
- suboptimal referral rates to genomic services;
- the changing landscape of genomic testing, with expanded indications that cover a growing number of individuals; and
- an increased recognition that “one size does not fit all” regarding the kind of genetic counseling that the health care system needs to deliver.
With all of these considerations, the traditional delivery model for genetic services, which includes one-on-one, in-person counseling before and after testing, may not be tenable, Schwartz said.
His work has focused on addressing some of the more general barriers that lead to disparities, such as a lack of awareness and knowledge, attitudes, suboptimal referrals, and socioeconomic factors, rather than population-specific barriers such as language, culture, and implicit bias. One study, for example, included women under age 50 who were newly diagnosed with breast cancer and therefore were good candidates for genetic testing and counseling1 (Schwartz et al., 2018). The intervention, which he called pro-
active rapid genetic counseling, used an embedded staff member in breast surgery clinics to identify all potentially eligible women at the time they were receiving their biopsy results.
Within 48 hours of a diagnosis, the team informed the patient that she was a good candidate for genetic testing for BRCA1/2, which could better inform her breast cancer treatment decisions. Out of 330 newly diagnosed breast cancer patients recruited from multiple institutions, one-third belonged to racial and ethnic minorities, predominantly African American. The goal of this intervention was to increase the proportion of patients who complete genetic counseling and, because genetic test results may inform any succeeding surgical treatment, complete this counseling prior to the surgical intervention. With the proactive rapid genetic counseling, the proportion of women who took advantage of the counseling services increased from about 40 percent to about 60 percent, Schwartz said. But even though the intervention led to an increase in the number of patients getting genetic counseling, Schwartz and his colleagues observed lower rates of participation in genetic counseling in women of a racial/ethnic minority group compared to non-Hispanic white women. “Despite our effects to reduce a wide range of barriers, and despite our ability to increase the overall use of counseling, we are still seeing differences between groups,” Schwartz said.
In a second study, Schwartz’s team compared telephone-delivered genetic counseling with standard genetic counseling in high-risk HBOC populations (Butrick et al., 2015; Schwartz et al., 2014). The 669 high-risk women enrolled in this trial came from four different sites, and 14 percent of the women belonged to a racial or ethnic minority. Schwartz proposed that the reason minority enrollment in this trial was so low was that there was no proactive outreach effort made for recruitment. The main goal of this study was to establish the effectiveness of telephone delivery across a broad range of psychosocial and decision-making outcomes in genetic counseling. The results showed that telephone delivery was no less effective than standard delivery, Schwartz said. However, in a separate analysis looking at the uptake of genetic testing following counseling, he and his colleagues observed that minority participants were substantially less likely than non-minority participants to complete genetic testing following telephone counseling than following standard delivery. In the standard delivery arm of the study, about 90 percent of minority participants who completed genetic counseling were getting tested, but in the telephone counseling arm, only 65 percent of minority participants got tested (Jacobs et al., 2016; Peshkin et al., 2016). These studies imply that proactive identification, referral, and enrollment could increase participation in genetic and genomic services, Schwartz said. This can be done using electronic health records (EHRs) and staff members such as navigators or genetic counseling assistants. Despite an increased rate of counseling following proactive
enrollment with enhanced access, persistent differences remained in both counseling and testing participation between minority participants and non-Hispanic white participants.
While telephone delivery can increase participants’ access to services, significant barriers remain regarding referrals, awareness, and attitudes toward testing. Schwartz acknowledged that the interventions he and his colleagues tested were generic and did not include culturally tailored materials. “I would be concerned about delivering telephone counseling if it is delivered in the exact same way that you try to deliver in-person counseling,” Schwartz said. “There needs to be some sort of modification to make it more effective.” These mismatches could possibly be addressed by cultural and linguistic tailoring.
In his final comments, Schwartz discussed some of the ongoing projects that he and his colleagues are conducting. One project is working with at-risk Latinas to enhance genetic counseling for HBOC risk. This is a community-based project that uses a culturally tailored video to address barriers associated with language, cultural beliefs, lack of referrals, and overall awareness of genetic testing. Other studies are adapting the telephone counseling intervention for use in a Latino population, and some are using an intelligent tutoring system intervention that emulates one-to-one in person tutoring and emphasizes risk messages to enhance genetic risk assessment in underserved African Americans and Latinas for breast cancer. Schwartz’s colleagues have received funding for a 5-year training program for 250 community health educators, navigators, and promotors to develop a cohort that can refer high-risk Latinas to genetic services. In addition, Schwartz recently received funding to increase the uptake of genetic testing among individuals who already have a relative with an identified pathogenic mutation. The goal of this last intervention is to increase the identification of mutations in first- and second-degree relatives of known mutation carriers and to streamline genetic counseling services for them.
If precision medicine is not developed and applied equally among all populations, Rena Pasick told the workshop, it is destined to increase health disparities. “Currently, those with the greatest need have the least opportunity to receive the best care,” she said. The purpose of her research with low-income and other medically underserved populations is to identify those at high risk for HBOC and to employ strategies that improve their access to and use of genetic counseling. “We want to maximize effective communication, which is when two parties engage with one another and
come away with the same meaning,” Pasick said. “That is something that must happen in genetic counseling and currently does not, particularly with people of low health literacy.” She reminded the workshop participants that one-third of U.S. adults have low health literacy and that they are disproportionately concentrated among people of non-European heritage.
The first of four studies Pasick reported on was a delayed-intervention randomized controlled trial which was conducted in partnership with California’s Every Woman Counts (EWC) program, a statewide phone service that provides low-income women with referrals for free breast and cervical cancer screening (Joseph et al., 2012; Pasick et al., 2016). Thousands of low-income women, speaking 18 different languages, call into EWC every year for referrals to free mammograms and Pap smears, Pasick said. The fact that they are calling the hotline indicates that these women are already aware of the benefits of cancer screening and are concerned about cancer risk. But because genetic counseling and testing services are concentrated in academic medical centers and are largely absent from public health settings, low-income patients—even those at high risk—have not traditionally had access to these services. The goal of Pasick’s study was to ascertain whether callers would agree to answer family and personal history questions when they called EWC and, if they were found to be of high risk, whether they would then obtain free genetic counseling. A parsimonious six-point family history screener that could be carried out over the phone was created. Among 1,212 eligible callers, 709 (58.5 percent) agreed to answer family history questions; of these, 102 (14 percent) were at high risk (25 percent Hispanic, 46 percent white, 10 percent African American, 16 percent Asian, and 3 percent of other racial/ethnic backgrounds). These women were randomly assigned to receive an immediate offer of a free genetic counseling appointment or to be sent a brochure with instructions on how to obtain that service. Nearly 40 percent of the women who were offered the immediate appointment obtained genetic counseling during the intervention period compared with fewer than 5 percent of those who received the brochure. (Following the trial, all high-risk women were offered genetic counseling appointments.) Of note, 54 percent of the women who had been offered genetic counseling reported that they could not attend unless it was delivered by phone. This study showed that integrating risk assessment and counseling referral into an existing service for low-income individuals can reach many whose risk status would otherwise remain unknown.
The second study that Pasick described was an ethnography of genetic counseling with low-income English-, Spanish-, and Cantonese-speaking patients in a public hospital to assess communication effectiveness from the patient’s perspective (Cheng et al., 2018; Joseph et al., 2017a,b; Kamara et al., 2018). Pasick’s colleague Galen Joseph observed and recorded 170 genetic counseling sessions and conducted 65 stimulated-recall patient inter-
views in which segments of counseling sessions were replayed to patients in order to elicit their perceptions about the meaning of key points. Findings revealed a mismatch between the information provided by counselors and the information desired and meaningful to patients; the use of interpreters further exacerbated miscommunication. Based on this, Joseph and Pasick developed a training module for genetic counselors on effective communication that emphasized the avoidance of too much information, the use of plain language, and the use of “teach-back” to allow counselors to better assess patients’ comprehension and information needs. Pasick said that counselors knew they were not getting through to some patients as well as they would like and that they greatly appreciated the guidance even though some of the strategies have proved challenging in actual practice.
The third study was a community-based program with health ministry leaders (HMLs) in African American churches that Pasick has been working with for more than a decade. This was a feasibility study of a culturally tailored education program that sought to identify women at high risk for HBOCs and to connect them with genetic counseling. HMLs were trained to conduct educational workshops because the team found that key messages could be relayed more effectively by known, trusted individuals than by researchers or genetic counselors. Over 4 years, the HMLs held 41 workshops, and the attendees completed the same six-point family history screen used in the first study Pasick discussed. She said that the key messages were refined over time and ultimately resulted in a substantial and significant increase in post-workshop knowledge. Overall, 84 high-risk women were identified, 50 percent of whom obtained counseling. Running the workshops, however, took enormous effort, and attendance was often low. Pasick’s team then asked HMLs to distribute and collect the family history screens at Sunday church services. Surprisingly, among those women who only filled out the family history after church, individuals who were at high risk obtained counseling at a higher rate than those who attended the 2-hour workshop. It is unclear why this was the case.
Pasick’s current study involves three public hospitals in a comparison of telephone, in-person, and video counseling for high-risk women whose primary languages are English, Spanish, or Cantonese. The purpose is to ascertain what is gained and lost via remote counseling and how to achieve effective communication via each mode. At the time of the presentation, 10,000 patients had completed the six-point family history screener over 10 months, resulting in a study enrollment of 242 high-risk individuals. Of these, 167 (69 percent) have been counseled and 144 (86 percent) completed a follow-up survey.
Pasick concluded by saying that progress is being made with regard to understanding the issues that affect reach in low-income communities, building trust across cultures, and how to communicate effectively about
genetics and risk, but it takes time, money, and a great deal of effort on the part of skilled professionals and community leaders. “There is no sexy, easy, high-tech way to achieve these critical objectives,” she said. “What is imperative is providing information and services to people from highly trusted others, in places where they already are, with words they understand, and with messages that are meaningful to them.” There is also a need to educate the public with participation from all sectors, a real investment of money, and a more diverse public health workforce. It is particularly important to get more diversity among genetic counselors, she said.
Jacquelyn Taylor told the workshop participants that she studies health equity and genomics and is also a pediatric nurse practitioner. She said that she is interested in the genetic and environmental factors that contribute to disease in minority populations, particularly African Americans. The first study Taylor reported on compared gene and environment interactions and their effects on blood pressure in three generations of African American women in Detroit, Michigan (Taylor, 2009a,b). The study was replicated with three generations of Dogon women in Mali, members of an African population that has maintained the same lifestyle and diet since the early 1400s and that was a large part of the trans-Atlantic slave trade (Taylor et al., 2013). After controlling for diet and physical activity, Taylor and her colleagues found that both the Michigan and Mali populations exhibited the same genetic factors related to increases in blood pressure. This work was then replicated in larger epidemiological samples of African Americans as well as in genetic epidemiological studies of atherosclerosis, showing that racial differences play a unique role in the genetic and environmental interactions that contribute to disease.
Currently, Taylor said, she is collecting data on African American women and their young children to study the impact of genetic and psychological factors—such as perceived racism, discrimination, symptoms of depression, and parenting stress—on blood pressure in mother/child dyads. Recruitment is based in Head Start programs across Connecticut, which allows researchers to meet participants in a community setting (see later in this chapter). “What is innovative about this study is that it extends the notion of race to what society makes you feel, looking at how racism and discrimination can affect your health,” Taylor said. She is also working with a group of investigators in Flint, Michigan, to study the interplay of genetic risks and environmental factors, including racism, discrimination, trauma, resiliency, and coping skills, and how those might increase the risk for common and chronic diseases.
All of these studies are grounded in community-based collaborations,
and Taylor described some keys to success in implementing this recruitment technique. First, she said, take advantage of the participant resource pools and registries that many universities have already compiled. In the first three-generation study, a registry managed by the Institute of Gerontology at Wayne State University gave Taylor access to the grandmothers who participated in the study. This was extremely helpful, she said, because once the grandmothers were contacted, the other two generations came into line and were willing to participate in the study.
According to Taylor, another great resource was Alpha Kappa Alpha Sorority Incorporated, the historically black sorority with more than 200,000 members across the United States, and Jack and Jill of America, an organization dedicated to nurturing future African American leaders that has a membership of more than 40,000 African American families across the United States. For her current study, Taylor said, she is recruiting from Head Start programs and YMCAs across Connecticut, and her team is engaged in community outreach efforts, such as participating in health fairs and engaging with local chapters of the National Association for the Advancement of Colored People (NAACP) to make their presence known and form relationships with communities. By participating in and including community outreach groups, researchers can make their presence known, get to know the community, and reassure the people in the community that they care and are there to stay. This helps foster good relationships, she said.
It is imperative to steer away from waiting for people to come to the clinic, Taylor said in regard to addressing inequities in access to health care. “We have to go where the people are,” she said. “Go to the community, reach out to the community and find out what they want and what they feel they need and actually provide those services in a community-based manner.” The physical nature of an academic medical center, with multiple parking lots, buildings, and clinics, can be a major barrier to accessing care. Mobile health and telehealth will be more effective, she said, especially when there are already established relationships between the health care system and a community. Patients are then more open not only to participating in research, but also to coming to see clinicians when they are interested in health care screening.
It is also important for researchers to participate in community activities, Taylor said. For example, she said, her team participates in parent meetings and sets up information tables for parents to view when dropping off or picking up their children at Head Start. She and her collaborators ask these parents about their concerns regarding their children’s and their own health, and they ask for their opinions about genetic testing. Taylor said that she and her colleagues talk directly to the parents to see what it is that they as clinicians can do to be of service to the community. In addi-
tion, she said, she and her team present the results of their studies at parent meetings and produce newsletters for the community that not only outline study results but also ask for help in recruiting for a study. Taylor also has invited people from these communities, such as the NAACP, to speak at events at her research institution. It is a reciprocal relationship, Taylor said. All of these efforts have the result of keeping the community engaged with what her team is doing, how far they have come in their research, what they plan to do in the future, and how these results will affect them and future generations.
The bottom line, Taylor said, is to be present, to let people know that they are important for more than just providing the data to write a report. It is also important to make it clear that the team’s community involvement is focused not only on the present, but also on the future health of the community. Taylor said that she even shares a great deal about her personal life with community partners and the families participating in her studies. “I talk about the fact that I have had my DNA tested and my children tested,” she said. This allows her to make a deeper connection with the community.
To overcome health care barriers, one must become a community advocate, Taylor said. It is important to expand genomic screening programs to community venues and community organizations and also to include more underrepresented minorities as principal investigators and key personnel in these studies. Minorities are consistently asked to serve as consultants for a study, Taylor said, but that does not provide the leadership that is needed to effectively recruit minority populations. It is important to have someone or a group of people who are connected to the community to make sure that things are done correctly and to guide the other investigators that have not had the opportunity to work with these populations. Increasing the number of genomic training programs, in both graduate and undergraduate programs and also in K–12 settings, would also be useful in decreasing genomic disparities, Taylor said. Genomic training for current clinicians and researchers through continuing education requirements and license renewals would also help in reducing these disparities.
The idea behind the Indiana Genomics Implementation Opportunity for the Underserved (InGenIOUS) study, Todd Skaar told the workshop, is to test the effect of pharmacogenetic genotyping on the number of adverse effects to medication use—and consequently the total health care costs—in patients who are genotyped versus those who just receive standard-of-care drug therapy. The study, conducted in two health systems in Indiana, has enrolled 1,312 patients in the genotype-guided therapy arm and 3,145 in
the standard-of-care arm. Of the nearly 4,500 patients recruited for the study, 61 percent were white and 29 percent were African American. The recruited patients had been prescribed 1 of 27 medications with potential pharmocogenetic impact.
This study plays an important role in addressing disparities in genetic and genomic health care, Skaar said, because it is known that the routine monitoring of drug response is more difficult for individuals from underserved populations. This is often due to the need for low-income, rural populations to travel much farther to get to clinics, which can result in higher transportation costs and lost wages. If it means one less box of cereal on the table for their kids or something else they may have to sacrifice in order to make multiple clinic visits, Skaar said, patients will be less likely to come back for routine monitoring of efficacy and toxicity of drugs. By determining the right drug and the right dose for a patient at the start of therapy, pharmacogenomic testing may help to address that problem and thus be even more effective in underserved populations than in the general population.
The two health systems from which the participants were recruited span a large proportion of the state, which made it difficult to use traditional recruitment methods. “It was not feasible to drive clear across the state for every one of those enrollees,” Skaar said. So the research team used phone recruitment and then established an online consent form through the Indiana University (IU) medical care system. To receive pharmocogenetic testing, participants could then go to any hospital in the IU system to get their blood drawn. This made it more feasible for individuals in low-income and rural communities to participate in the study, therefore increasing the study sample.
After Skaar and his colleagues received the genotyping information and the medication data for an individual, an adjudication committee reviewed the results and, when appropriate, made a recommendation for providers to alter the drug therapy. Out of 1,313 subjects who were genotyped, 439, or one-third, had an actionable result (i.e., had a genotype that affected responses to medication and therefore had clinical utility). Levels of action-ability differed from medication to medication; for example, 42 percent of individuals who were prescribed tramadol had an actionable result, while only 9 percent of those prescribed nortriptyline had actionable genotype results. All actionable results were returned directly to the participant’s health care provider, with relevant recommendations for clinical management. Skaar and his collaborators are now extracting data on adverse health events to the drug therapies from EHRs as well as economic data in order to determine the effects of pharmacogenomic testing on these factors.
Skaar also has used ethnic, racial, and geographic data to determine how many of the patients in the study come from medically underserved
areas and populations. Of the patients in the genotyped arm, 37 percent are from medically underserved areas or populations, which, he said, should allow his team to generate some hypotheses regarding location and disparities in access and then test them. He noted that of the two health systems that participated in the study, the enrollment success rate was three times higher and completion took one-fifth as many phone calls at Indiana University Health than at Eskenazi Health, which has a higher proportion of Medicaid and low-income payers. Eskenazi is the safety net health care system in Indiana, meaning that it provides medical care to patients with no insurance or with Medicaid. Despite these differences, more than 80 percent of the participants, regardless of where they lived, agreed that it was a good idea to get genetic testing to determine how they would respond to certain medications. Many participants also said that they would share their test results with family members and their providers.
This study shows that remote recruitment for genomic medicine studies can successfully enroll patients and collect samples from medically underserved areas and populations, Skaar said. Direct-to-patient recruitment, he added, may also reach patients in underserved areas without needing to engage large numbers of providers. Tools exist to identify patients in underserved areas and to ensure that those patients are represented in studies, although more resources may be needed to recruit patients from safety net hospital systems. The final lesson from his work so far, he said, is that despite patient demographics, subjects want their genetic data and also want their providers to have access to it.
It is important to think about what a community’s perceptions are regarding the benefits and harms of genomic medicine, one workshop participant said. “If those kinds of questions are not addressed, the uptake of genetic testing may not be as high as you have expected post-genetic counseling,” the participant continued. She asked the panelists if any of their studies included questions aimed at trying to understand community beliefs about genetic testing. Schwartz said that his study did not ask those questions, and Skaar said he recognized that the lack of genetic testing uptake may be due to the fears and anxieties common in communities, but it is also likely due to financial concerns. He also mentioned that some bioethicists have found that the anxiety related to genetic testing is usually short lived, but more research needs to be done to learn why it exists and how to address it better. Pasick said that training genetic counselors to communicate better can address this issue and increase the uptake of testing.
Another workshop participant asked how the field can detangle clinical use and access to genetic tests from the lack of evidence of its clinical util-
ity in diverse populations, referring to the fact that dosing algorithms for the warfarin may not work well in African Americans because of a lack of understanding of CYP2C9 variants in this population. Skaar replied that studies must include all populations because of that very issue. “We need to include a broad population in those studies,” he said.
Cathy Wicklund, the director of Northwestern University’s graduate program in genetic counseling, said that her program works hard to change the perception of what genetic counseling is and what genetic counselors need to be able to explain to their patients. She teaches that genetic counselors must be focused on the person sitting in front of them and what that person needs to know at that particular time. She also said that nondirectiveness (providing accurate information to a patient, but not trying to influence decisions) is a relic of the profession and that genetic counselors are encouraged to provide guidance and not simply take a passive role in patient decision making. “I want to assure that there are programs that are embracing this effort in effective communication training so that you are not retraining genetic counselors once they are out of school,” Wicklund said. Taking part in workshops such as this one and going to hear speakers on various topics in genomics is one approach providers can take to incorporate genomics into their training. Skaar said that there are fellowships available to get practical training in genomics.
“If you could have one research question answered to get a better handle on health care disparities in genomic medicine, what would that be?” asked Feero. Skaar said that he would like to know how the implementation of genomic medicine differs when it is done in pragmatic trials that include a diverse population or a broad diversity of populations. Taylor said she would ask study participants how they think genomic testing can help them. Schwartz proposed looking at genetic tests that have demonstrated clear clinical utility and seeing if it is possible to identify and refer patients in a routine way to ensure that they are obtaining whatever genetic services they need.
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