Abstract
The potential for using widespread genetic testing to inform health care has become a viable option, particularly for heritable cancers. Yet, little is known about how to effectively communicate the benefits and risks of both personal genetic testing and participation in biorepositories that aid scientific advancements. Nationwide efforts are engaging communities in large genetic studies to better estimate the populationwide prevalence of heritable cancers but have been met with hesitance or declination to participate in some communities. To successfully engage an Oregon population in longitudinal research that includes predictive genetic testing for pathogenic or likely pathogenic variants associated with an increased risk for cancer, researchers conducted 35 focus groups (two of which were held in Spanish) in 24 of Oregon's 36 counties to better understand knowledge and attitudes related to genetic testing and willingness to participate in longitudinal genetic research. A total of 203 adults (mean = 45.6 years; range 18-88), representing a range of education levels and prior knowledge of genetic research, participated in the focus groups. The majority (85%) of participants reported personal or family diagnoses of cancer (e.g., self, family, friends). A majority (87%) also reported a strong interest in cancer genetic testing and receiving genetic information about themselves. Nearly all focus groups (94%, 33 of 35 sites) included participant discussion citing their families (e.g., children, close relatives, and extended family members) as key motivators for participation in genetic research. For example, participants reported interest in increasing personal knowledge about their own and their families’ cancer risks in order to respond proactively, if a pathogenic variant was found. While most focus groups (94%, 33 of 35 sites) included participant discussion describing barriers to predictive genetic, testing such as concerns about outcomes, the desire to learn about health risks in oneself mitigated or outweighed those fears for many participants. Other commonly reported concerns were related to potential mistrust of insurance companies, researchers, or institutions, or lack of knowledge about genetics, genetic testing, or genetic research. Participants, particularly in rural areas, highlighted critical factors for research recruitment, such as trust, personal interaction, public education about genetic research, and clear communication about study goals and processes. Our statewide findings reflect that public interest in predictive cancer genetic testing and cancer genetic research can surpass lack of knowledge of the complex topics, particularly when benefits for self and family are emphasized and when study considerations are well articulated.
Keywords: disparity, focus groups, genetic testing, heritable, marketing, outreach, pathogenic variants, qualitative, recruitment, rural
1 ∣. INTRODUCTION
Genetic research and the use of genetic specimens are essential components to the advancement of personalized medicine and targeted treatments (Wilson & Nicholls, 2015). Advances in cancer detection and treatment allow oncologists to increasingly apply personalized approaches, including therapies offered based on the presence of germline or somatic genetic variants (i.e., PARP inhibitors for tumors expressing mutations in BRCA1 or BRCA2 and immunotherapy for Lynch syndrome). The presence of a germline pathogenic variant in genes associated with inherited cancer syndromes can confer an increased risk for specific cancers, such as the effect of BRCA1 or BRCA2 pathogenic variants to increase risk for breast, ovarian, prostate, and pancreatic cancers (hereditary breast and ovarian cancer syndrome) or APC pathogenic mutations to increase risk for gastrointestinal polyps and colorectal cancer with (APC-related polyposis conditions) (Huang et al., 2018). Many of these inherited cancer syndromes have medical management recommendations shown to mitigate the associated cancer risks (Dorschner et al., 2013; Jackson & Chester, 2015; Rahman, 2014). Early detection efforts can employ predictive cancer genetic testing to ‘identify mutations that increase a person's risk of developing disorders with a genetic basis, such as certain types of cancers’ (United States National Library of Medicine, 2020).
Knowledge of an increased risk for cancer, due to a pathogenic or likely pathogenic variant in a cancer predisposition gene, enables individuals to take surveillance and preventative measures such as mammography or colonoscopy, which support early detection of cancer before the disease has progressed and has become difficult to treat (Sokolenko et al., 2015). Between 1982 and 2012, 114 genes were discovered that confer moderate to high risk of developing cancer (Rahman, 2014). With further advances in cancer research, it is expected that scientists will find additional genetic risk factors with clinical implications, making the need to bank genetic specimens critically important for supporting longitudinal research about the patterns of cancer development in individuals and under certain conditions.
To ensure that the increasingly diverse population of the United States (US) has the opportunity to experience the benefits of predictive genetic testing, biorepositories must include samples from diverse populations of individuals. While some studies have found that knowledge and attitudes about genetic research and biorepositories have been positive, with participants expressing interest in research participation (Brothers, Morrison, & Clayton, 2011; Etchegary, 2014; Hull et al., 2008), engagement of minority ethnic and racial populations in biomedical research, especially African Americans, Hispanic/Latinos, Native American/American Indians, and rural communities, continues to be disparate (Blake, Moss, Gaysynsky, Srinivasan, & Croyle, 2017; Davis etal., 2017; Dean etal., 2017; Einterz et al., 2007). Cited reasons for the lack of research engagement include potential lack of awareness, restricted access to referrals, or disinterest in participation, though we must acknowledge that historic abuses in research and a mistrust of medical institutions and the government may also contribute to the underrepresentation of minority ethnic and racial populations in biorepositories and biomedical research (George, Duran, & Norris, 2013; Scharff et al., 2010). Obtaining genetic samples from underrepresented groups is especially critical given the disparities in cancer mortality (Blake et al., 2017; Bolin et al., 2015). For example, individuals living in rural communities have a higher all-cancer mortality than those in urban areas, and African Americans in rural communities have higher rates of all-cancer cancer mortality than their White counterparts (Blake et al., 2017; Bolin et al., 2015; Dhillon, Wünsche, & Lutteroth, 2016).
In addition to racial and ethnic diversity, other factors can impact awareness of and interest in biomedical research participation, such as religious beliefs, family structure, community setting, stigma, fear, or shame regarding carrier status (Mellon, Gauthier, Cichon, Hammad, & Simon, 2013; Tkatch et al., 2014; Tong et al., 2014; Underhill, Habin, & Shannon, 2017). For example, a person's decision to participate in biomedical research can be influenced by confusion about genetic terminology, research procedures, protections for research participants, or by a lack of knowledge about what to expect (Brothers et al., 2011; Clayton, Halverson, Sathe, & Malin, 2018; Etchegary, 2014; Hull etal., 2008; Laranjo, 2016; Lemke, Wolf, Hebert-Beirne, & Smith, 2010; Nicholls et al., 2016).
Several recent projects have investigated effective communication and recruitment techniques for specific populations (Davis et al., 2018; Dean et al., 2017; McIntyre et al., 2018; Meloni, 2016; Tong et al., 2014), though none have focused on geographic differences among populations, such as rural, urban, and frontier differences, which may geographically influence beliefs about predictive cancer genetic testing. Oregon has a broad geography with the majority of its counties (26 of 36, 72%) consisting of communities designated as rural or frontier (Figure 1). The Oregon Office of Rural Health defines a rural community as any geographic area ten or more miles from an urban area with a population of 40,000 or more, and a frontier community as any county with six or fewer people per square mile (Oregon Office of Rural Health, 2019a). One third of Oregon's population lives in rural communities (Oregon Office of Rural Health, 2019a), which often have lower access to medical centers, lower employment, higher poverty, and greater health disparities relative to urban communities (Blake et al., 2017; Bolin et al., 2015; Zahnd et al., 2018). In Oregon, individuals within frontier communities have longer drives on average (15.3 min) to access the nearest patient-centered primary care ‘homes’ than do those within rural (12.5 min) or urban areas (10 min), with several areas requiring over 30-min drives or longer, such as in southeast Oregon where residents have to drive over one hour (77 min) to get to a facility (Oregon Office of Rural Health, 2019b). Additionally, Oregon frontier and rural areas have fewer primary care providers, mental health providers, and dentists per 1,000 population than do urban areas. These regions also face higher rates of preventable hospitalizations, emergency department visits associated with mental health or substance abuse, and inadequate prenatal care (Oregon Office of Rural Health, 2019b). Low medical care access and lack of preventive care in Oregon's frontier and rural communities are compounded by higher rates of individuals living between 138% and 200% of the Federal poverty level. Specifically, compared to the state average of 12%, rural and frontier communities face double the poverty rates (ranging from 21% to 27%), highlighting a population ineligible to receive Medicaid, but too poor to pay for insurance independently (Oregon Office of Rural Health, 2019b).
FIGURE 1.
Focus group sites across Oregon. Circles indicate locations of focus groups conducted throughout Oregon to investigate knowledge of and interest in cancer genetic screening, cancer genetic testing, and cancer genetic research. Circles may not add up to 35 (total focus groups conducted) since several locations held multiple focus groups on varying days and times. Black star indicates Portland's location
Currently, there is only one comprehensive cancer center in Oregon, the Knight Cancer Institute in Portland, which is funded by the National Cancer Institute and refers to an institution that conducts cancer research to deliver cutting-edge cancer treatments to patients while integrating training for biomedical researchers and healthcare professionals (National Cancer Institute, 2019). Individuals residing in locations distant from Portland have more geographic barriers to participate in biomedical research and therefore may be less familiar with predictive genetic testing for cancer risk. It is important to understand the perspectives that may be unique to non-urban geographic locations as nearly one fifth of the US population lives in rural areas (United States Census Bureau, 2017).
To support the long-term public health of Oregon residents, researchers at Oregon Health & Science University (OHSU) developed a collaborative population health study, the Healthy Oregon Project (HOP), which integrates predictive cancer genetic testing with behavioral risk factors measured over time to create a comprehensive repository of data and specimens that support longitudinal cancer research. The public acceptability of the proposed research was determined in this study, which used qualitative methods to understand public attitudes about genetic research and predictive cancer genetic testing, as well as interest in participation in an Oregonbased biorepository meant to support longitudinal cancer research.
2 ∣. METHODS
2.1 ∣. Participants
This study was reviewed by OHSU’s Institutional Review Board (IRB, STUDY #17573). Participation was open to all Oregonians over 18 years of age. Focus group recruitment was accomplished via paper flyers, social media (e.g., Facebook, Instagram, and Twitter), electronic mailing lists associated with the researching institutions (e.g., Knight Cancer Institute, OHSU-PSU School of Public Health, OHSU, and community partner organizations), personalized e-mails to local stakeholders (i.e., civic and healthcare staff), and institutional websites (e.g., Knight Cancer Institute, OHSU Community Research Hub). Interested individuals were directed to an online sign-up form that collected only names, e-mails or phone numbers, and preferred focus group dates/locations. Focus group locations were chosen with the goal of representing populations across the state, specifically ensuring rural and frontier representation. Selected areas had individuals who could support local recruitment efforts, such as OHSU community liaisons residing in the region (i.e., within a driving range of 60-120 miles) and individuals affiliated with OHSU-Knight Cancer's partnering facilities and organizations (e.g., partnering clinics, Knight Community Partnership Program grantees). Focus group size was kept to the conventionally acceptable size of 6-12 participants (Green & Thorogood, 2014). Only one researcher had access to the data submitted through the online sign-up form. This researcher scheduled focus groups and sent e-mail reminders both 1 week and 1 day prior to the event, but was otherwise not involved in data collection. Prior to each focus group, facilitators were blind to all participant information other than the number of participants scheduled at each focus group site.
2.2 ∣. Procedures
2.2.1 ∣. Facilitator training
Facilitators consisted of one OHSU faculty and seven research staff employed with the Community Research Hub, of the Oregon Clinical and Translational Research Institute (OCTRI), OHSU’s NIH-funded Clinical and Translational Science Award site, and the OHSU Knight Cancer Institute Community Outreach and Engagement Component. Six of the eight facilitators (75%) were OHSU staff who lived in communities distant from the university, specifically outside of the Portland Metro area and were research liaisons between OHSU and their rural region. OCTRI’s Community Research Hub research liaisons work with community leaders and stakeholders in their designated regions to address and improve health issues through capacity building, ensuring community relevance of work being done, and enhancing receptivity of work within the community. All facilitators were trained in human subjects research via CITI.
A preliminary script was drafted by study staff based on the prior work of Lemke and colleagues (2010). A full-day, in-person meeting in October of 2017 was used to collaboratively hone the script (Appendix A), which was projected onto a screen for discussion. Once the script was solidified, facilitators were trained on focus group procedures, which were modeled after both Lemke and colleagues (2010) and standard procedures outlined by Green and Thorogood (2014). All facilitators had bachelor's degrees, with five having advanced degrees in research fields (four master's degrees and one doctor of philosophy degree). All facilitators had experience engaging with communities and obtaining feedback from community members, and two had formal qualitative research training prior to the study. The in-person training, which was led by one of the facilitators who is on faculty at OHSU and teaches qualitative methods at the university, provided facilitators with skills related to group moderation, including active listening, ice-breaking, managing time appropriately, avoiding excessive deviation from relevant topics without limiting discovery, encouraging a story-telling dialogue, and fostering a climate of comfort, trust, and non-judgment. Each facilitator was provided with documents and materials, kept on a secure file-sharing site, to bring to each focus group. For 32 focus groups, a designated note-taker, often a graduate student or facilitator from another region, recorded group climate, interactions, participant reactions, and other meaningful non-verbal observations (Appendix B). For the remainder of the focus groups (n = 3), the facilitator acted as note-taker.
2.2.2 ∣. Focus groups
Audio-recorded focus groups were conducted in reserved rooms in public facilities across the state, with preference given to libraries, community centers, and educational locations accessible by public transportation to help ensure access while providing a familiar setting to enhance overall participant comfort. Each focus group was scheduled for 90 min. The majority of focus groups were conducted on weekday evenings (n = 28) between 5:00 p.m. and 8:00 p.m., with seven conducted during weekend mornings between 10:00 a.m. and noon. Two focus groups in rural communities that had high proportion of Spanish-speaking individuals were held in Spanish using contracted Spanish-speaking facilitators (The Next Door and Hood River Oregon) with a member of the research team present to take notes and to answer questions. This study representative worked with the Spanish-language contractors in advance, ensuring identical IRB-approved consent and facilitation protocols were observed, though they did not facilitate focus groups directly. Light refreshments were provided based on time of day, and participants received no other incentives aside from the university students who received extra-credit in one of their classes for participation. Participants voluntarily provided demographic information, and focus group audio was later transcribed for analysis.
Prior to each focus group commencing, an IRB-approved information sheet, blank sheet of paper for notetaking, and a demographic survey were placed at each seat. Demographic surveys included age, gender, race, ethnicity, education level, presence of medical insurance, and a Likert scale question asking ‘How much do you know about genetic testing?’ with answer options of: ‘I don’t know anything,’ ‘I know a little bit’, ‘Some’, ‘I know a moderate amount’, and ‘I know a lot’. No identifying information was collected from participants and questions were broad enough to ensure participant anonymity, though focus group date and location were recorded on each form. The established predetermined script (Appendix A) was used throughout the focus group to gather specific information and encourage open discussion.
Upon arrival, participants were greeted, directed to refreshments, and invited to sit where preferred, typically in the formation of circle or around a table. Participants were asked to review the information sheet and complete the demographic survey prior to the start of the session. Facilitators announced the beginning of the session, introduced themselves and the designated note-takers, and described their affiliations and roles on the project. Ground rules described by facilitators included encouraging a safe environment where all opinions were valid, avoiding crosstalk and interruptions to ensure respect during discussions, and maintaining anonymity of participants and confidentiality of their opinions after the session. Facilitators reminded participants about the intention to audio record sessions and requested assent, which was verbally reiterated and confirmed before the audio recording was started. Questions and comments prior to recording or after the recording device was turned off were written down by note-takers or facilitators. The template used by the note-takers to record verbal and non-verbal communications is described in Appendix B.
A pre-recorded video (Appendix C) was played to introduce project goals consistently across sites. Participants were asked about their personal familiarity with cancer (e.g., diagnoses or treatments of cancer in themselves, family members, or close friends) prior to engaging in two ‘fist-to-five’ questions about their interest in receiving genetic information about themselves and their familiarity with genetic research studies. The fist-to-five technique has previously been used for consensus building (Fletcher, 2002) and is a physical version of a Likert scale that can be quickly and easily counted and verbally described for the audio recording. In the technique, each participant holds up a fist with a certain number of fingers revealed; the number of fingers raised, between zero and five, indicates approximate level of interest or agreement. Participants were then asked why someone would want, or conversely not want, to participate in genetic research, what they would want to know before participating in such research, and their thoughts about sharing genetic research data with other scientists for additional cancer research. A video was played at the conclusion of the focus group (Appendix D) that reiterated the study goals, described the importance of recruiting healthy controls, and included an IRB research compliance specialist who described ethical considerations, potential discrimination, and other security concerns that participants may have about study participation. After the video, participants were asked about any unresolved questions, administered a fist-to-five about their personal interest in participating in genetic research, and asked if they felt people in their community would be interested in learning more about participating in genetic research projects and what recommendations they had for sharing information with people in their community.
Upon conclusion, facilitators shared a brochure about the HOP study that included contact information for further questions or comments about Knight Cancer Institute projects or genetic research. Facilitators stayed to answer any questions of adjourned participants.
2.2.3 ∣. Data analysis
All focus group recordings were sent to The Last Word (Columbus, OH) for transcription. Transcription text was uploaded to Dedoose (version 8.1.8) for thematic content analysis (Green & Thorogood, 2014). The coding team consisted of one faculty member and two research assistants who met regularly throughout the course of one year to discuss and come to agreement on expansion or collapse of themes. Inter-rater reliability was assessed using Cohen's kappa within Dedoose, with >80% agreement obtained for all major themes (Hallgren, 2012). Coded themes for each focus group were summed within a matrix, which was transferred to Statistical Package for the Social Sciences (SPSS; IBM, version 25) for descriptive analyses of themes across community type (i.e., urban, rural, frontier). Tables describe the number of focus groups in which that theme was discussed as well as the number of mentions of that theme per focus group.
Demographic surveys were entered into Microsoft Excel, with genetic testing knowledge scored from zero (‘I don't know anything’) to four (‘ I know a lot’). Mean genetic testing knowledge and demographics were calculated for each site and recorded in a separate spreadsheet that listed each focus group site, its urban/rural/frontier designation (Oregon Office of Rural Health, 2019a), the number of participants who attended the group, number and percent of attendees affected by cancer (defined as a diagnoses or treatment of cancer in self, family, or close friend), and participants’ fist-to-five ratings of genetic testing interest, genetic research knowledge, and interest in participating in genetic research. Statistical comparisons were analyzed with SPSS using chi-square, ANOVA, and independent-sample t tests.
3 ∣. RESULTS
3.1 ∣. Participants
A total of 203 people participated in 35 focus groups conducted in 26 counties throughout Oregon with a mean of 5.8 participants per focus group (SD = 4.2; Table 1). Four additional sites were scheduled to host focus groups but had no participants attend (due to weather in one location and unknown reasons for the other three). The sites with zero attendees included 1 urban location, 2 rural locations, and 1 frontier location.
TABLE 1.
Participant demographics reported on intake forms from 35 focus groups in urban, rural, and frontier regions of Oregon
| Focus group region classification | Urban | Rural | Frontier | Total |
|---|---|---|---|---|
| Number of focus groups | 13 | 20 | 2 | 35 |
| Total number of participants | ||||
| Total np (mean np, SD) | 92 (7.1, 4.7) | 106 (5.3, 3.8) | 5 (2.5, 0.7) | 203 (5.8, 4.2) |
| Age of participants | ||||
| Total np (mean age in years, SD in years) | 91 (37.1, 21.5) | 105 (52.8, 7.1) | 5 (48.8, 8.2) | 201 (45.6, 20.6) |
| Race and ethnicity (np, %) | ||||
| African American/Black | 1 (1.1%) | 0 (0%) | 0 (0%) | 1 (0.5%) |
| Asian | 7 (7.6%) | 3 (2.8%) | 0 (0%) | 10 (4.9%) |
| Hispanic or Latino | 9 (9.8%) | 22 (2.8%) | 0 (0%) | 31 (15.3%) |
| Native American/Alaskan Native | 0 (0%) | 6 (5.7%) | 0 (0%) | 6 (3%) |
| Native Hawaiian/Pacific Islander | 2 (2.2%) | 0 (0%) | 0 (0%) | 2 (1%) |
| More than 1 | 11 (12%) | 7 (6.6%) | 0 (0%) | 18 (8.9%) |
| White | 80 (87%) | 80 (75.5%) | 5 (100%) | 165 (81.3%) |
| Prefer not to answer/Decline | 1 (1.1%) | 2 (1.9%) | 0 (0%) | 3 (1.5%) |
| Education (np, %) | ||||
| Less than HS degree | 1 (1.1%) | 8 (7.5%) | 0 (0%) | 9 (4.4%) |
| HS degree | 45 (48.9%) | 41 (38.7%) | 2 (40%) | 88 (43.3%) |
| 2-year degree | 15 (16.3%) | 22 (20.8) | 1 20%) | 38 (18.7%) |
| 4-year degree | 16 (17.4%) | 9 (8.5%) | 1 (20%) | 26 (12.8%) |
| Graduate degree | 15 (16.3) | 26 (24.5%) | 1 (20%) | 42 (20.7%) |
| Health insurance (np, %) | ||||
| Has health insurance | 88 (97.7%) | 92 (86.8%) | 5 (100%) | 185 (91.1%) |
Note: A significant difference in age was observed between focus group regions (p < .001) as urban sites included four focus groups held at a university campus. Race and ethnicity totals may not add up to 100% as participants could select more than one race/ethnicity option. No significant difference was observed for race/ethnicity (p = .56), education (p = .21), or health insurance status (p = .71) across urban, rural, and frontier sites. Abbreviations: np, number of participants represented at focus group; SD, standard deviation.
The majority of focus group participants identified as female (70%) and White (81.3%) with a mean age of 45.6 years (SD = 20.6 years; range 18-88 years). Most reported having at least a high school degree (95.1%). The majority of participants reported that they had health insurance (91.1%); however, type, extent, and source of insurance were not elucidated. More than half of the focus groups (57%, n = 20) were conducted in rural communities as defined by Office of Rural Health designations, followed by 37% (n = 13) in urban communities, and 6% (n = 2) in frontier communities. Community settings, descriptions, and focus group locations can be found in Appendix E. No statistical differences between community settings were observed for racial/ethnic diversity (p = .56) or health insurance status (p = .71).
3.2 ∣. Focus group themes
3.2.1 ∣. Perceived reasons to participate in genetic research
When participants were asked why they felt someone would choose to participate in genetic research, two main themes emerged: benefit to self and benefit to society (Table 2). Personal benefits were mentioned in all 13 urban sites (100%), 18 of 20 rural sites (90%), and both frontier sites (100%). Personal benefits were perceived as primary motivators for participation in genetic research at the vast majority of sites (94%) and included furthering personal knowledge of health risks, curiosity about health risks affecting themselves and/or their families, and financial benefits/compensation for research involvement. Other personal benefits included the desire to act proactively to benefit from early detection, which was discussed at more than half of sites (60%), and gaining knowledge that could benefit their families or children, which was also discussed at more than half of sites (69%).
TABLE 2.
Reasons people might participate in genetic research as shared by focus group attendees
| Main theme |
Sub-theme/ definition |
Representative quote | Urban sites n (%) describing theme; mentions/site |
Rural sites n (%) describing theme; mentions/ site |
Frontier sites n (%) describing theme; mentions/ site |
Total sites n (%) describing theme; mentions/site |
|---|---|---|---|---|---|---|
| Benefit Self |
|
‘It would be nice to know what's in the genetic code … what you could possibly be passing on to your children and they say the best weapon is information. And so, the more we know about it, the more we know of the risk, then it will help educate the future generation.’— participant in urban community ‘For their own health and well-being … and to gain a greater understanding and knowledge of what you're facing, you know, with your cancer”.—participant in rural community ‘My kids want to have kids, or they do have kids, and they deserve to know, even if you don't want to go through it yourself’.—participant in frontier community |
13 (100%); 3.3 | 18 (90%); 3.8 | 2 (100%); 3.0 | 33 (94%); 3.6 |
| Benefit Society |
|
‘I think I would be a part of genetic testing just to see the progression of science. Cancer's in my family, so I already feel like I check into as much as I can, because it's been consistent in our family, but to be part of a study would be primarily just to make sure that more knowledge was - you know, to progress somewhere, to help other people in the future’.—participant in rural community ‘But I wouldn't see why people wouldn't risk it to have genetic research because if it helps the public … then I don't understand what's wrong with doing genetic research and why not try it out?’—participant in urban community ‘ I would hope that they would want to participate in genetic research … In any way that they could help prevent diseases … I would hope that they would want to participate just to be able to learn from or help people learn from it’.—participant in frontier community |
12 (92%); 1.8 | 14 (70%); 1.7 | 2 (100%); 1.5 | 28 (80%); 1.8 |
Note: Participants were asked ‘Why do you think someone would want to participate in genetic research?’ with observed themes and representative quotes reported. Results are displayed as number and percentage of urban/rural/frontier sites mentioning that theme—not the number of people mentioning them. The number and percentage of sites mentioning a theme were calculated by frequency of sites mentioning a theme divided by total sites in that community setting. Focus groups included 13 urban sites, 20 rural sites, and 2 frontier sites, for a total of 35 statewide focus groups. Mentions/site were calculated by dividing the number of mentions of the theme by the sites describing that theme in focus groups.
Motivators for research participation pertaining to societal benefits were also discussed at most of sites (80%). Focus group attendees discussed the desire of individuals to act altruistically due to alignment with their values, such as furthering science, adding to the general knowledge base, and improving existing treatments. Societal benefits serving as motivators for genetic research participation were mentioned at a larger percentage of focus groups in frontier (100%) and urban (92%) sites than in rural sites (70%).
3.2.2 ∣. Perceived reasons to decline participation in genetic research
Participants were also asked why they felt someone might not want to participate in genetic research. Responses were distilled into five main themes: concerns about outcomes, study considerations, distrust, lack of awareness, and beliefs conflicting with the research and/or genetic study (Table 3). The focus groups at the majority of sites (94%) mentioned concerns about outcomes (e.g., genetic test results) more often than any other theme, with an average of 3.9 mentions/site. Concepts within this theme included: too much or overwhelming information, preference not to know the potential learned information, fear, and denial, all of which were mentioned frequently across urban, rural, and frontier sites.
TABLE 3.
Reasons people might not participate in genetic research/predictive cancer genetic testing as shared by focus group attendees
| Main theme | Sub-theme/definition | Representative quotes | Urban sites n (%) describing theme; mentions/ site |
Rural sites n (%) describing theme; mentions/ site |
Frontier sites n (%) describing theme; mentions/ site |
Total sites n (%) describing theme; mentions/ site |
|---|---|---|---|---|---|---|
| Concerns about outcomes |
|
‘I think my concern as well is finding out about that information and then having that fear when you're alone and maybe not having anyone to go to about it. A lot of people in this country particularly, are very individualistic and kind of keep to ourselves’.–participant in rural community ‘And workplace discrimination and getting rental or getting a contract for houses. There's a lot of discrimination out there for that type of thing, too. If somebody finds out that so-and-so has a certain disease, they're totally discriminated, blackballed. Society is set up as that’–participant in rural community ‘I think maybe just because I'd be scared to like, see what they find out about the cells or something like that’.–participants in urban community |
13 (100%); 3.2 | 18 (90%); 4.6 | 2 (100%); 3.0 | 33 (94%); 3.9 |
| Study considerations |
|
‘Some people might not be able to like give blood or take part in some of the tests just due to physical limitations’.–participant at urban college campus ‘Of all the things we said earlier, if there's cost, if there's - you know, travel, if there's - not knowing, like she went through, waiting and waiting and having - not having a decision, not having information and just having to chew on it’.–participant in frontier community |
11 (85%); 2.5 | 15 (75%); 3.3 | 2 (100%); 4.5 | 28 (80%); 3.0 |
| Distrust |
|
‘Well, a lot of people actually who don't have much information or exposure are a little paranoid about things that involve their genes and what somebody might do with that. And also, anything that might be associated with government sponsored or monitored things it might make them feel a little paranoid that they not only have a lot of information about them, but they also have their genetic makeup’.–participant in rural community ‘I worry about just errors being - happening - inputting the data into electronic records…’ participant in urban community |
11 (85%); 3.1 | 15 (75%); 2.6 | 2 (100%); 3.0 | 28 (80%); 2.8 |
| Awareness levels |
|
‘I guess, there seems to be like a lack of education on the subject because a lot of people have no idea that it even exists’.–participant at urban college campus ‘And there - there are people all over that do not understand what it is, …they don't understand, and they just don't care’–participant in urban community ‘So, when my daughter, who is 29, learned that she could get a genetic test, she was 26, I think, when she found that she has a likelihood of this gene, she could go and get tested. Her response was, “Why would I go looking for trouble?” And I said, “Oh, sweetie, genes don't really work that way.” But that was her approach, and she's young and she didn't want to know. And then, of course, as her mom, I'm like, “You know, you can do something, there are some treatments that maybe we could do.”’–participant in urban community |
9 (69%); 1.8 | 11 (55%); 2.0 | 1 (50%); 4.0 | 21 (60%); 2.0 |
| Beliefs |
|
‘Maybe just thinking that God has His own plan and there's no - you know, reason to bear course’.–participant in frontier community | 5 (38%); 1.0 | 8 (40%); 1.6 | 2 (100%); 1.5 | 15 (43%); 1.4 |
Note: Participants were asked ‘Why do you think someone may NOT want to participate in genetic research?’ with observed themes and examples reported. Results are displayed as number and percentage of urban/rural/frontier sites mentioning that theme—not the number of people mentioning them. The number and percentage of sites mentioning a theme were calculated by frequency of sites mentioning a theme divided by total sites in that community setting. Focus groups included 13 urban sites, 20 rural sites, and 2 frontier sites, for a total of 35 statewide focus groups. Mentions/site were calculated by dividing the number of mentions of the theme by the sites describing that theme in focus groups.
Study considerations were mentioned by participants at the majority of sites (80%), with a higher average frequency at frontier sites (4.5 mentions/site) than at urban or rural sites (2.5 and 3.3 mentions/site, respectively; Table 3). Study considerations referred to research processes and procedural specifics, such as an individual's ability to access the study (e.g., geographically, physically, linguistically, financially, and time commitments to participate) as well as privacy and security concerns related to data storage, participant anonymity, and who has access to their resulting data.
Distrust was also mentioned by participants at 80% of sites and included potential distrust of the researching institution or researchers, distrust of insurance companies (expressed specifically as fear of potential discrimination by life and medical insurers), concern about the accuracy of the genetic tests themselves, and misuse of the collected samples. Urban, rural, and frontier communities mentioned distrust to roughly the same extent (Table 3).
Lack of awareness was mentioned as a deterrent for research participation by focus group attendees at 60% of sites and was described as a lack of understanding about potential benefits of genetic testing, unfamiliarity with the risks or science behind genetic testing, apathy toward genetic testing or research, or a perceived inability to change health outcomes for themselves or others. Focus group attendees at frontier sites described lack of awareness (4.0 mentions/site) at twice the rate of urban (1.8 mentions/site) or rural sites (2.0 mentions/site).
Finally, the potential impact of religion and/or beliefs on individuals’ perceived decisions to not participate in genetic research arose least often (43% of sites). The theme of religion/beliefs arose at about one third of urban sites (38%) and at about half of rural sites (45%). While both frontier sites (100%) had discussion emerge about influences of religion/beliefs on research participation, there was no difference in the number of times that the topic of religion/beliefs arose across sites, whether classified as urban, rural, or frontier
3.2.3 ∣. Information needed to consent to participation in genetic research
When asked what type of information they would need before participating in a genetic research study, participants discussed three major themes: consent form considerations, data security and privacy, and ongoing participant support and retention (Table 4). Consent form considerations were mentioned by participants at 100% of the sites, with an overall mention average of 6.1 times per site. Although participants did not explicitly articulate ‘consent form’, this theme included items that are typically found on a consent form. Specifically, concepts surrounding the consent process that participants wanted discussed in greater detail included access (i.e., travel needed, costs, time commitment for study visits), process and procedure for research involvement, information about the study team, and participant access to study results. Frontier sites discussed consent form considerations at a higher frequency (9.5 mentions/site) than in urban (6.1 mentions/site) and rural (5.8 mentions/site) sites.
TABLE 4.
Information needed to participate in genetic research as shared by focus group attendees
| Main theme | Sub-theme/definition | Representative quotes | Urban sites n (%) describing theme; mentions/site |
Rural sites n (%) describing theme; mentions/ site |
Frontier sites n (%) describing theme; mentions/ site |
Total sites n (%) describing theme; mentions/ site |
|---|---|---|---|---|---|---|
| Consent form considerations |
|
‘Would we know what the results were? And would we know what they were testing for? Would it be anything that I was even concerned with’.–participant in rural community ‘It all falls back to who's actually funding this test and who's funding the universities and the doctors to do the tests, too’–participant in rural community ‘I don't think I would have any [reservations about participation], unless it was a painful process’.–participant in frontier community |
13 (100%); 6.1 | 20 (100%); 5.8 | 2 (100%); 9.5 | 35 (100%); 6.1 |
| Data security & privacy |
|
‘I think healthcare, as far as everything else in your life, data privacy is a concern now, everybody's getting breached, the security systems are being breached and I don't want my social security number or my name, my health information out to everybody’.–participant in frontier community ‘I think it's really important to know how your privacy is protected when you're participating in research because it's a very separate issue. And like I'm absolutely interested in doing the testing and getting the information and sharing the information with science, but not interested in those insurance people ever having access’.–participant in rural community |
11 (85%); 2.1 | 12 (60%); 2.5 | 2 (100%); 4.5 | 25 (71%); 2.5 |
| Ongoing participant support & retention |
|
‘I think it would be good if you're doing genetic testing on people, if it was paired with counseling afterwards, so you didn't just have people tested and then just send them out the door’.–participant in rural community [Describing prior cancer genetic testing experience] ‘I was 100% alone. It was terrifying and awful, and I left there, and it was like, go find your doctors. Go find your team of doctors and get screenings scheduled. And no one's looking over that. Just me, I'm the one, you know, kind of managing all this’.–participant in urban community ‘And it sounds like having a nurse navigator as part of the outcome of the research, so having people tested and then diagnosed, even people who are high risk negatives or who have a [variant of unknown significance], having a nurse navigator […] available to help people with these issues would be paramount’.–participant in urban community |
8 (62%); 2.3 | 12 (60%); 2.1 | 1 (50%); 3.0 | 21 (60%); 2.2 |
Note: Participants were asked ‘What information would you need to know before participating in a genetic research study?’ with observed themes and examples reported. Results are displayed as number and percentage of urban/rural/frontier sites mentioning that theme—not the number of people mentioning them. The number and percentage of sites mentioning a theme were calculated by frequency of sites mentioning a theme divided by total sites in that community setting. Focus groups included 13 urban sites, 20 rural sites, and 2 frontier sites, for a total of 35 statewide focus groups. Mentions/site were calculated by dividing the number of mentions of the theme by the sites describing that theme in focus groups.
Data security and privacy discussion included questions about which parties would have access to the data, data sharing permissions, concerns about privacy, anonymity, confidentiality, and concerns about medical and life insurance ramifications. This theme was mentioned in focus groups at 71% of the sites and in the vast majority of urban communities (85%), and with an overall study average of 2.5 mentions/site. This theme was discussed more frequently in frontier communities (average of 4.5 mentions/site).
Ongoing participant support, which included the desire for personalized services such as genetic counseling and being able to speak with other participants in the study about their ongoing experiences or having an advocate on the study team who would help them, was mentioned at 60% of the sites an average of 2.2 times per site, with the highest average frequency of mention in one frontier community (3 mentions/site).
3.2.4 ∣. Recommended marketing approaches by community
When asked for recommendations about how to share information about genetic research study opportunities with people in their communities, participants discussed key themes related to format, marketing approach, and utilization of targeted organizations and locations (Table 5). For example, the format of marketing tools was the most frequently mentioned theme across sites (86% of all sites) and described suggested methods of communication, such as print materials, social media postings, in-person events, broadcast messages, and telecommunications. The frequency that these approaches were described in focus groups by urban, rural, and frontier sites is included in Appendix F.
TABLE 5.
Marketing approach recommended by community setting
| Main theme | Sub-theme/definition | Representative quotes | Urban sites n (%) describing theme; mentions/ site |
Rural sites n (%) describing theme; mentions/ site |
Frontier sites n (%) describing theme; mentions/ site |
Total sites n (%) describing theme; mentions/ site |
|---|---|---|---|---|---|---|
| Format |
|
‘Your best chance is being [on] local television. If you want the local audience, then some sort of an advertisement outreach to say, “We're looking for people to participate in this kind of thing, this kind of study’, but word of mouth or social media is very powerful these days. If you talk to your coworkers or former coworkers, I think it's really powerful. The first thing that people talk to me about when I first told them I had cancer is,” Geez, is there something I can do?’–participant in urban community ‘I'm talking like an ad in the paper for like 2 weeks’.—participant in rural community ‘But the personal one-on-one invitations will have to be the way to go because it could be potentially threatening or scary. It seems intensely personal to people’—participant in rural community |
10 (77%); 3.5 | 19 (95%); 3.9 | 1 (50%); 2 | 30 (86%); 3.7 |
| Organizations and location |
|
Examples: Genentech (Hillsboro), American Cancer Society/Relay for Life (Coos Bay), Public Health office (Burns), Lions Club/Elks Club (Astoria), Virginia Garcia Medical Center (McMinnville), Nike (Beaverton), Lions Club/Kiwanis (The Dalles), Survivors, caregivers, family members, employers, coworkers, friends (Coos Bay), Dr. Henderson, OHSU-Knight Cancer Center (Coos Bay), Department of Health and Human Services (Klamath Falls), Community Cancer Center (Roseburg), Cancer Center; St. Charles, Cascade Cancer Care, Bend Memorial Clinic (Bend), Elkhorn Media (La Grande), Chamber of Commerce (Grants Pass), Health Dept. (The Dalles), Red Cross/St. Jude's (McMinnville), Farmworker advocates (Hood River), American Cancer Society (Eugene), Rotary (McMinnville), community political groups/ churches (Klamath Falls) | 9 (69%); 2.7 | 19 (95%); 4.3 | 1 (50%); 7 | 29 (83%); 3.9 |
| Marketing approach |
|
‘Well, sometimes, because I've got three kids at home and I work, and my [spouse] works, and my kids are old enough where I was - I'm able to leave them home for a couple - you know, a half an hour to an hour, but between the time that I left to come here and my [spouse] got home. And so - but it would be nicer to have a little bit more of a notice. That way, if we did have to find somewhere to put the kids - you know, not just stash the kids in a closet somewhere - you know. Also - you know, this is - this is an economically depressed area. Being an economically depressed area, two weeks is not enough time to make sure you can get time off work, if you have a lower-end job’.–participant in rural community ‘Again, though, it depends how we sell it. We have to have the - you know, this is how it benefits the greater good, this is how it could benefit you, kind of that - what's in it for you, because a lot of people are, for a lack of a better word, self-centered’–participant in rural community ‘I think the word cancer definitely scares a lot of people so, yeah, I think just the message and how you describe the study definitely will help’.–participant in urban community |
9 (69%); 5.1 | 17 (85%); 3.7 | 2 (100%); 4 | 28 (80%); 4.2 |
Note: Participants were asked ‘Do you have any recommendations for sharing the information with people in your community?’ with observed themes and examples reported. Results are displayed as number and percentage of urban/rural/frontier sites mentioning that theme—not the number of people mentioning them. The number and percentage of sites mentioning a theme were calculated by frequency of sites mentioning a theme divided by total sites in that community setting. Focus groups included 13 urban sites, 20 rural sites, and 2 frontier sites, for a total of 35 statewide focus groups. Mentions/site were calculated by dividing the number of mentions of the theme by the sites describing that theme in focus groups.
The importance of utilizing certain organizations and locations for marketing was mentioned often by focus groups (83% of all sites) and described the attendees’ voiced ideas to target marketing to community and publicly available spaces (e.g., libraries, schools, community centers, and health centers), private spaces (e.g., grocery stores, gyms, offices), and other relevant stakeholders or organizations (e.g., Lion's Club International, Benevolent and Protective Order of Elks, Rotary Clubs). Participants also commonly mentioned cancer survivor organizations and networks (e.g., local or national groups, Facebook groups) and cancer-oriented organizations (e.g., American Cancer Society) as potential marketing ‘hubs’ to contact. The number of times partnering organizations was mentioned within discussion was higher in frontier (7.0 mentions/site) and rural (4.3 mentions/site) sites than in urban sites (2.7 mentions/site).
Marketing approach was mentioned by participants at 80% of sites and referred to the type of messaging that outreach materials should include, such as discussing the convenience and benefits of genetic research participation, targeting specific audiences for representation, describing relevance of the research study to the advance health understanding, and providing education that mitigates possible fear and stigma associated with potentially carrying a pathogenic or likely pathogenic variant. These marketing approaches can emphasize personal benefits associated with predictive genetic testing, such as the knowledge gained that can enhance adoption of proactive cancer screening practices (e.g., mammography or colonoscopy; Appendix F).
3.2.5 ∣. Quantitative analysis findings
On demographic surveys, participants rated their level of knowledge regarding genetic testing using a five-point Likert scale (0 representing ‘I don't know anything’ to 4 representing ‘ I know a lot’). Participants’ self-reported mean level of knowledge about genetic testing was 1.90 (SD = 0.7), with only 2 people declining or failing to answer (Table 6). No significant differences were observed between urban, rural, and frontier sites in participants’ self-reported genetic testing knowledge (p = .84), the percent of focus group participants affected by cancer (p = .30), participants’ interest in receiving genetic information (p = .82), their familiarity with genetic research (p = .77), or interest in participating in this genetic research study (p = .56).
TABLE 6.
Self-reported knowledge of, experiences with, and interest in cancer genetic research or testing among focus group participants in Oregon
| Item | Measurement approach |
Urban sites | Rural sites | Frontier sites | Total sites |
|---|---|---|---|---|---|
| Self-reported genetic testing knowledge (M, SD, n) | Intake forms (0-4 Likert scale) | 1.9 ± 0.8, 13 | 1.8 ± 0.7, 20 | 2.1 ± 0.8, 2 | 1.9 ± 0.7, 35 |
| Familiarity with genetic research M, SD, n) | ‘Fist-to-Five’ (0-5 Likert scale) | 1.9 ± 1.0, 12 | 2.0 ± 1.1, 20 | 1.5 ± 0.7, 2 | 1.9 ± 1.0, 34 |
| Interest in receiving genetic information M, SD, n) | ‘Fist-to-Five’ (0-5 Likert scale) | 4.2 ± 0.9, 13 | 4.4 ± 0.8, 20 | 4.2 ± 0.2, 2 | 4.3 ± 0.8, 35 |
| Participants affected by cancer (M %, SD, n) | % of focus group who raised hands | 83.2% ± 23.9%, 13 | 91.8% ± 14.5%, 20 | 100% ± 0%, 2 | 89.1% ± 18.5%, 35 |
| Interest in participating in this genetic research study (M %, SD, n) | % of participants raising hands or reporting above 3 on ‘Fist-to-Five’ (0-5 Likert scale) | 77.9% ± 21.4%, 9 | 86.2% ± 24.7%, 15 | 100% ± 0%, 1 | 83.8% ± 23.1%, 25 |
Note: Relationship between cancer prevalence, familiarity with genetic testing, familiarity with genetic research, and interest in participating in genetic research. Results displayed as mean, standard deviation, and total number of sites—not total number of participants—answering the question. Self-reported genetic testing knowledge was calculated from intake forms at each focus group site, with responses scored on a Likert scale from 0 to 4; 0 = I don't know anything, 1 = I know a little bit; 2 = Some; 3 = I know a moderate amount; 4 = I know a lot.
Interest in receiving genetic information was asked using the script in Appendix A and calculated by counting the number of fingers raised for each person (0–5, with higher numbers denoting more interest) and then calculating the mean number of fingers raised per site. Familiarity with genetic research (also in script; Appendix A) was tabulated using the fist-to-five response for each person (0–5) which was averaged for each site. Participants affected by cancer were calculated by counting hands raised divided by total number of site participants; interest in participating in this genetic research study was reported as a percentage of participants raising their hands or individuals reporting above a 3 in a fist-to-five. Not all focus groups asked about interest in participating in this genetic research study; therefore, totals do not add to 35. No significant differences were observed for any of these five items between urban, rural, and frontier sites (all p ≥ .30).
Abbreviations: M, mean rating; n, number of focus group sites; SD, standard deviation.
Participants’ knowledge of genetic testing measured at the time of intake significantly correlated with their familiarity with genetic research (r = .59; p < .001), which was asked as a physical Likert scale (via fist-to-five technique) during focus groups. Participants’ self-reported knowledge of genetic testing at intake did not significantly correlate with interest in genetic testing (r = −.15, p = .39) or interest in participating in genetic research (r = .31, p = .14). The mean percentage of focus group participants affected by cancer did not correlate with participants’ self-reported knowledge of genetic testing (r = .24, p = .17) nor with the group's interest in participating in the proposed genetic research study (r = .31, p = .14). Likewise, familiarity with genetic research did not correlate with interest in participating in genetic research (r = −.04, p = .84), nor did interest in receiving genetic information about oneself correlate with interest in participation in genetic research (r = −.003, p = .99).
4 ∣. DISCUSSION
Statewide focus groups in Oregon, representing geographic regions classified as urban, rural, or frontier, collectively revealed that attendees were interested in participating in genetic research, primarily to benefit themselves and their families, such as their children and the next generation. These personal benefits were mentioned at nearly all sites (94%) and are consistent with findings from Tong et al. (2014) showing that participants were most likely to donate biospecimens if asked by their families or if they believed a family member would benefit. Our results show that individuals expressed high levels of interest in participating in genetic research to better understand their cancer risk, a desire that was not influenced by self-reported knowledge of genetic testing, familiarity with genetic research, nor prior history of cancer. Our statewide findings highlight that public interest in participating in genetic research can outweigh lack of knowledge individuals might face, particularly when potential benefits for self and family are clearly articulated.
4.1 ∣. Promoting family engagement in predictive cancer genetic testing as an important motivator
In our study, participants described being interested in proactive measures of cancer prevention and screening, having curiosity about their genetic risk, and desiring information about their genetic risk in order to help their families be better informed about their risk of heritable cancers. Participants were keenly interested in knowing which family members carried medically actionable cancer risk gene variants and expressed interest in going through the predictive cancer genetic testing process together. With an increased focus on personalized medicine in science, engaging families together may be a strong motivator for genetic testing participation, as they could share stories of family history and may be better able to support each other should a gene variant of concern be discovered. Several participants expressed dismay when learning children (under age 18) are typically ineligible for predictive cancer genetic testing of adult-onset conditions, as they hoped to learn about cancer risks for their entire family, including (and especially) for their children. Societal benefits of genetic research, such as improving treatment, cures and advancing science, were also discussed, albeit to a lesser extent (80% of sites) than possible personal benefits (94% of sites). Recruitment efforts should emphasize the familial benefits of genetic research participation when possible.
4.2 ∣. Concerns about outcomes as a barrier to genetic research participation
Five barriers to genetic research participation were described, including concerns about outcomes (94% of sites), study considerations (80%), distrust (80%), lack of awareness (60%), and beliefs (43%). These barriers should be mitigated through purposeful marketing and education, which we believe may help to enhance public participation in genetic research studies. The most prevalent barrier–concerns about outcomes–included knowing the results of predictive cancer genetic testing, which were perceived as overwhelming and too much information. Participants also described fear of receiving results, which included stress of waiting and knowing carrier status. Researchers could alleviate stress by providing estimated wait times for individuals to receive their genetic test results as well as the approximate prevalence of a pathogenic variant being found, since the actual rate of positive tests may be much lower (~5%) than focus groups concerns may suggest. Individuals also described a fear of potential treatment (e.g., cost, physical toll), with many describing a preference not to know their genetic risk for cancer and a preference to live in ignorance, preferring to avoid hard or scary decisions, while others were fearful of the decisions they would have to make if a pathogenic or likely pathogenic gene variant was found. These reasons were cited by the research team for excluding minors in the proposed research, since potential psychological ramifications could arise from receiving genetic risk information at such a young age (American Academy of Pediatrics, 2013). However, these psychological ramifications affect adults as well, therefore, including study team members who can help participants make sense of their results and navigate next steps would make great strides toward reducing psychological impact of positive test results. Likewise, researchers should emphasize how screening practices (e.g., mammography, colonoscopy) can shift based on knowing one's genetic test results. Participants also described concern of personal discrimination (e.g., personal stigma, work, insurance) stemming from knowing their results, as many participants were vocal about their distrust of insurance companies and worried about insufficient coverage of screening and treatment, including concerns that they would be denied coverage based on their predictive cancer genetic testing results (e.g., life, health). As such, genetic researchers should communicate protections in place for preventing potential discrimination based on genetic test results.
4.3 ∣. Distrust as a barrier to genetic research participation
Our study suggests communicating about protections is necessary, but may not be sufficient, as distrust was a common barrier to participation (80% of sites; Table 3), with 71% of sites indicating that data security and privacy needed to be clearly described prior to their participation (Table 4). Participants in all community settings mentioned concerns about personal information being compromised by hacking or being used for discriminatory purposes such as denial of medical or life insurance, or employment. Consistent with prior research conducted on attitudes toward genetic research and biobanking, our research shows a generally positive outlook and interest in participating if personal information is protected (Clayton et al., 2018; Hull et al., 2008; Lemke et al., 2010; Sanderson et al., 2017). Many participants shared concerns about data breaches or data sharing with groups they did not approve of, particularly medical insurance companies via electronic health records. Many people mentioned that although there are current protections in place to limit insurance companies from denying coverage, dropping members, or raising costs (e.g., 2008 Genetic Information Nondiscrimination Act, GINA), they did not trust those protections to remain indefinitely. As such, genetic researchers should place heighted protections on data that could be used to adversely impact insurance coverage if protections were removed and clearly describe how information is being stored and shared, ranging from inclusion within the electronic health record to being shared with other researchers and under what conditions, giving participants the opportunity to opt out of future research. It should be noted that distrust and hesitancy to participate in genetic research may be heightened in some communities due to histories of oppression, abuse, and misinformation. Moving forward, it is of incredible importance that potential participants are not only approached respectfully but also protected by researchers who provide clear information about potential risks prior to participation. Careful and thorough communication, addressing concerns and needs on a community basis, and building trust are key themes to ensuring widespread participation in genetic research and collection of data from a diverse sample, according to our statewide research.
4.4 ∣. Mitigating barriers by describing study considerations
Study design considerations were a prominent theme in our research, both in the context of reasons not to participate (Table 3) and what individuals would want to know before participating in a genetic research study (Table 4). Consent form considerations were discussed in 100% of sites (Table 4) and included items that are typically described during the consenting process, such as procedures, risks, privacy/security of data, and access (e.g., time commitment, frequency of visits, and cost). For example, participants wanted to know, in advance, the specifics of the procedures and process of participating in genetic research, including sample collection, inclusion/exclusion criteria, risks/benefits, and planned use of specimens. Participants discussed the preference for non-invasive procedures and minimal time commitments as facilitating factors to their research participation. Participants wanted to know the goals of the research, as well as information about the credibility of the study team (e.g., scientists, study institution, and funding sources). They also discussed concerns about sample and data storage, but generally had positive feelings about information sharing with other scientists as long as their privacy, security, and confidentiality were protected. Several participants discussed unease at participating in genetic research if it benefits pharmaceutical companies, underscoring the importance of building trust when conducting research in communities. While researchers may already include these details in their consent forms, we offer that these details are helpful to also include as ‘Frequently Asked Questions’ on a public-facing study website, giving individuals sufficient time to review details and ask questions of the study team before engaging in the formal consent process. As descriptions to many questions can make a webpage lengthy, including a ‘search’ function on the site can help potential participants find needed information in a timely manner.
4.5 ∣. Geographic isolation, poverty, and lack of healthcare services as barriers to participation
Participants in rural and frontier areas, in particular, cited concerns about geographic access and time commitment/frequency due to living in remote communities. Oregon, like many Western, Midwestern, or Southern states, has a large number of communities designated as rural (23 of 36) or frontier (10 of 36) which can make study travel burdensome (Oregon Office of Rural Health, 2019a; United States Census Bureau, 2000, 2010). Although rural communities are defined differently by government groups, they comprise 15%-19% of the US population and 72%-95% of US land (Rural Health Research Center, 2019; United States Census Bureau, 2017; United States Department of Agriculture, 2019). Rural communities often experience geographic isolation, high poverty rates, and lack of services, particularly in regard to health care (Blake et al., 2017; Singh, Williams, Siahpush, & Mulhollen, 2011; Zahnd et al., 2018). It is noteworthy that many metropolitan communities can still experience geographic isolation and/or health service shortages (Health Resources & Services Administration, 2018). These geographic and economic factors may impede participants seeking medical attention or preventive screenings (e.g., mammography, colonoscopy) should a pathogenic or likely pathogenic gene variant associated with cancer risk be found.
4.6 ∣. Improving access to genetic research by describing time and cost
Participants commonly mentioned wanting information about study access, such as geographic distances needed to travel, physical demands (e.g., due to disability or advanced age), time commitment, and financial burdens like gas, childcare, and testing costs. Cost was a commonly discussed barrier to participation in our study and cited in reference to predictive cancer genetic testing, early detection screenings, travel needed for study visits, and the cost of cancer treatment, if needed. Cost and affordability factors were repeatedly cited among participants at many rural and frontier sites who would have long distances to drive to receive care. Oregon’s only National Cancer Institute (NCI)-designated comprehensive cancer center is located in Portland, which is a 6- to 8-hr drive for many rural and frontier communities in Oregon. As described in Table 5, one rural participant cited their region's low socioeconomics and needing to arrange childcare as critical factors impacting their decision to participate. Study considerations related to access (e.g., cost, frequency of visits) are especially important for researchers to describe when recruiting in communities with low socioeconomic status, such as rural/frontier sites or some communities of color. These concerns were partially mitigated, however, by high interest in participation if predictive cancer genetic testing was offered at no cost to participants. Participants were more eager to participate in the proposed genetic research study when they learned predictive cancer genetic testing would be a no-cost incentive of participation, with genetic counselors providing positive test results through personal phone calls rather than an in-person visit, thereby reducing access barriers in remote sites.
4.7 ∣. Participant support and advocacy reduces barriers to participation
Participants also cited a desire for ongoing support after receiving their test results, such as how to navigate health care and insurance after learning of an increased genetic risk for cancer. These suggestions were incorporated into HOP, and the study team hired both genetic counselors and a patient navigator to help Oregonians navigate next steps. While genetic counselors would describe test results, patient navigators would serve as a resource for participants on how to manage their care, communicate with insurance companies, and connect participants with resources including support groups and educational materials. Furthermore, results from this study have been used to develop frequently asked questions presented on the website, guide marketing materials and approaches for reaching different community settings, as well as support educational materials that would inform individuals about benefits and ethical implications of predictive genetic testing for cancer risk.
4.8 ∣. Education, marketing, and outreach about cancer genetic research
When discussing marketing approaches for sharing information about genetic research in their communities (Table 5; Appendix F), participants commented often about the public's lack of knowledge, ignorance, or apathy in regard to receiving genetic information or participating in genetic research. Some participants cited a lack of basic genetic literacy, such as understanding the difference between genetics, genetic testing, and genetic research, which is consistent with prior research (Hann et al., 2017; Krakow, Ratcliff, Hesse, & Greenberg-Worisek, 2018). However, lack of education about these topics did not correlate with interest in participating in cancer genetic research. While individuals did want to learn more, they cited other factors to emphasize when recruiting for genetic studies, such as convenience, personal benefits, and relevance (Table 5; Appendix F). Many participants cited a lack of perceived benefit and were unaware how predictive cancer genetic testing was of relevance to their life. Of the 127 individual mentions by participants who cited concern about outcomes, 14 (11%) also cited lack of awareness as a barrier to participation, highlighting an opportunity to educate individuals about genetic risk factors for cancer while also empowering them to take preventive action in their own lives and their families’ lives.
Knowing that people are often motivated by their families but may potentially lack genetic literacy highlights an important opportunity to incorporate community education into outreach and marketing materials for genetic studies. Like prior studies (Lemke et al., 2010; Tong et al., 2014), our findings underscore that family, children, and future generations are motivating factors associated with a higher willingness to participate in genetic research and would be an effective marketing approach when talking with communities across the state (Appendix F). Consistent with prior research describing the importance of community-based participatory research or community-engaged approaches (Davis et al., 2018; Dean et al., 2017; Kwan et al., 2018), our participants described local, in-person recruitment, and snowball (i.e., chain referral) sampling recruitment as being the most effective strategies in their communities. Print format, such as flyers, brochures, and posters, was recommended in public areas and utilization of local news, radio, and television stations was recommended for the best local reach, especially in rural regions (Appendix F). Having a strong presence at community events, town halls, and health fairs was noted as important when connecting with the local community, demonstrating the importance of building and fostering community connections and trust when recruiting for genetic research. In rural and frontier locations, in particular, participants cited partnering organizations and locations as key to reaching their community.
4.9 ∣. Study limitations
Oregon demographics are not representative of the United States with regard to the African American/Black population and other demographic groups, so these results may not be applicable to populations in other states. Although our sample was representative of Oregon's current demographic makeup, Oregon is less diverse than the United States in general, with just under 24% of the population belonging to a minority racial and/or ethnic group. However, Oregon's Hispanic/Latino population increased sevenfold between 1980 and 2000, with increases in Asian and Pacific Island populations since 2010 as well (State of Oregon Economic Analysis Office, 2019). Oregon's population is expected to further shift in the next 40 years (State of Oregon Economic Analysis Office, 2019), consistent with the U.S. Census Bureau estimates that by 2044, the United States will become a minority majority country (Colby & Ortman, 2014). Although this study held the majority of focus groups in rural and frontier areas to ensure adequate representation of those communities, and multiple focus groups were held in Spanish to obtain Hispanic/Latino perspectives in rural farming communities, key urban neighborhoods did not include as much racial/ethnic diversity as desired in our study.
Our sampling approach to a major Oregon university increased the racial and ethnic diversity of our urban sample (p < .03), as 28.8% of university participants reported non-white race/ethnicity compared to 7.5% of participants in other urban settings. While these university students were significantly younger (mean 21.2 years, 6.1 SD) than other urban participants (mean 58.2 years, 15.5 SD) and were expected to have less familiarity with cancer, no significant differences were found in their familiarity with cancer (p = .99), genetic research knowledge (p = .28), interest in receiving their predictive cancer genetic testing results (p = .11), or interest in participating in this future genetic research study (p = .14) compared to other urban participants. Therefore, our urban findings may be representative of Oregonians as a whole, though the extent to which our findings would extend to younger adults without personal familiarity with cancer remains to be determined. Oregon's change in population demographics will require that marketing teams and researchers conduct outreach and recruitment for genetic studies in ways that are meaningful, culturally relevant, and inclusive.
Although work was done to mitigate potential bias in what participants shared in focus groups (see Facilitator Training in the Methods section), it is possible that how the facilitators were perceived by participants (e.g., demographics or role on the research team) may have influenced participants’ comfort or level of sharing.
The majority of communication for this study utilized computer technology such as Facebook, e-mails, and listservs. This may have been a barrier for some without access to computers or smartphones, reliable internet connections, or those with limited computer literacy. This may have impacted who found out about our study as well as who signed up and participated. In order to reach a wide variety of participants, future research should utilize a mix of digital/technology based and analog or in-person recruitment methods. Many of the recommendations for more appropriate outreach are discussed in Table 5. Additionally, the majority of our participants reported they had personal familiarity with cancer, which may point to a high level of self-selection bias as those individuals may be more prone to discuss subjects related to cancer, predictive cancer genetic testing, and cancer genetic research, than those without personal familiarity with cancer. Self-selection bias may have influenced participation of individuals with deeply held religious beliefs, potentially limiting their participation and representation. Future research should prioritize recruitment of individuals across different ideologies, cancer background, and racial/ethnic backgrounds in order to gain a more thorough understanding of the public's level of knowledge, attitudes about, and interest in, predictive cancer genetic testing and research. Finally, timing of focus groups may have excluded people with conflicting schedules (e.g., parents of small children, non ‘9-to-5’ schedules), as the majority were scheduled just after the common business hours of 5:00 p.m. Traffic, childcare, and familial responsibilities may have interfered with participation. Likewise, focus groups offered during Saturday mornings were poorly attended (mean 3.43; SD 2.64; versus p.m. = mean 6.39; SD 4.29). Additionally, daylight savings time in October of 2018, when clocks turned back one hour in the United States, may have limited focus group attendance at one site, as increased darkness coincided with poor weather.
4.10 ∣. Practice implications
Our study data highlight opportunities to include genetic counselors not only in the results process, but also in the consent and marketing processes, which may alleviate some community concerns and encourage participation. As the demand for personalized medicine grows, the demand for genetic counselors will also grow as genetic counselors receive specialized training in medical genetics and counseling in order to support patients through interpretation and decision making in regard to their genetic cancer risk. These efforts can be extended by including patient navigators on study teams, who can direct participants to needed services and reduce time burdens on genetic counselors, who are less concentrated in rural and frontier areas (Cohen et al., 2013; Emmet, Stein, Thorpe, & Campion, 2018).
Marketing approaches should emphasize the convenience of participating (e.g., cost, time commitments) and provide education about personal relevance, including possible benefits to family members. Online surveys or web meetings may offer a flexible way to encourage higher participation in the future while respecting diverse work and family commitments, as well as a method for keeping costs low and increasing services in rural and frontier areas. However, this may be a barrier for those with low computer literacy or limited technology access. When budget allows, childcare, bus or parking vouchers, or gift cards would likely increase participation without risking coercion or inducement, as has been reported in other studies (Bonevski et al., 2014; Leach, Schoenberg, & Hatcher, 2011; Loftin, Barnett, Bunn, & Sullivan, 2005).
ACKNOWLEDGMENTS
This project was supported by the Center for Early Detecting and Advanced Research (CEDAR; GCNCR0865A1 ‘Widespread Testing for Cancer Risk Syndromes' to J. Shannon), the Oregon Clinical and Translational Research Institute (1UL1TR002369 to D. Ellison), the OHSU-Knight Cancer Institute Community Outreach and Engagement Component (P30CA069533 to B. Druker) and had student support for the project funded by BUILD EXITO (5RL5GM118963 and TL4GM228965 to C. Crespo). This work was conducted as part of graduate training and incorporates science communication practices developed through a Science Education Partnership Award (R25GM129840 to L. Marriott). We thank The Next Door interpreters, in particular Martha Zapien, Liliana Lachino, and Todd Dierker for their work on the Spanish-language focus groups; as well as Cody Solomon, Racyne Parker, Leigh Coppola, and Shelley Vandehey for help with notetaking during focus groups.
Funding information
Center for Early Detecting and Advanced Research, Grant/Award Number: GCNCR0865A1; Oregon Clinical and Translational Research Institute, Grant/ Award Number: 1UL1TR002369; OHSU-Knight Cancer Institute Community Outreach and Engagement Component, Grant/Award Number: P30CA069533; BUILD EXITO, Grant/Award Number: 5RL5GM118963 and TL4GM228965; Science Education Partnership Award, Grant/Award Number: R25GM129840
Appendix
APPENDIX A.
Focus group script with questions adapted from Lemke et al. (2010)
| Question | Type of answer |
|---|---|
| How many of you are personally familiar with cancer? | Count |
| To what extent does receiving genetic information about yourself and your cancer risk interest you? | Scale of 0-5, 0 being not at all interested and 5 being highest level of interest |
| How familiar are you with genetic research studies? | Scale of 0-5, o is not at all familiar and 5 is most familiar |
| What comes to mind when you think of genetic research? | Open-ended |
| Why do you think someone would want to participate in genetic research? | Open-ended |
| Why do you think someone may NOT want to participate in genetic research? | Open-ended |
| What information would you need to know before participating in a genetic research study? | Open-ended |
| In most research studies, individuals can give additional consent for their information to be shared with other scientists…. What are your thoughts about your data being shared with other scientists for research on cancer risk? | Open-ended |
| Do you have any other thoughts or questions about genetic research that you would like to share? | Open-ended |
| (video played) What do you think about the information in this video? Did it leave you with any lingering questions? | Open-ended |
| Does the idea of participating in genetic research interest you? | Open-ended |
| Do you think people in your community would be interested in learning more about this project? | Open-ended |
| Do you have any recommendations for sharing this information with people in your community? | Open-ended |
APPENDIX B.
Note-taker template used to record items not be picked up through an audio recording
| Discussion | Note-taker instructions |
|---|---|
| Upon participant arrival | Description of people; gender, approximate age, diagram of where people are seated, labeled in order as they entered by gender, other non-identifying info as it arises |
| Video 1 | Watch and record reactions |
| Hand raise/count questions | Record total hands raised, who did and who didn't |
| ‘Fist-to-five’ questions | Record numbers 0-5 |
| Discussion questions | Record who said what/great quotes |
| Video 2 | Watch and record reactions |
| General observations | Nods of affirmation or disagreement, sarcasm, laughter, looks of confusion, restlessness, disinterest, hand gestures, other important non-verbal cues |
APPENDIX C.
Introductory video (2:40)
| Description | Introduction to how genetics can influence many cancers; introduction to CEDAR as part of OHSU; introduction to research project proposal to collect genetic samples from Oregonians to better understand cancer; discuss need to collect large sample; introduction to focus groups across Oregon to discuss heritable cancers, genetic testing, genetic research, and interest in participating in genetic research; Paul Spellman, PhD introduces self, affiliation, and why focus groups are important for this research project; Jackilen Shannon PhD introduces self, affiliation, and intention of focus groups; encourage open discussion, opinions, and assures confidentiality. |
| Link | https://ohsu.box.com/s/4iq3tgnetlqcqjkv1ep3he6bknv7cy7l |
APPENDIX D.
Concluding video (2:43)
| Description | Introduction to heritable cancers and population sampling; genetic testing able to flag heritable cancers; discussion of concerns and risks associated with genetic testing; discussion of increased risk of cancer with specific genes and recommended actions; project interest in developing low-cost genetic tests to identify genes; project interest in public input about concerns or ideas; assurance of anonymity for focus groups |
| Link | https://ohsu.box.com/s/kaobz2hb3mbn75y5saxylgl3v92l7rov |
APPENDIX E.
Focus group community settings, definitions, and locations
| Community setting | Community setting definitiona | Locations of focus groups |
|---|---|---|
| Urban (n = 13) | A population center with 40,000 or more people | Beaverton Bend Corvallis Eugene (n = 5; 1 adults; 4 with University of Oregon students) Gresham Medford Portland (x2) Salem |
| Rural (n = 20) | A geographic area 10 miles or more from the centroid of a population center with 40,000 or more people | Astoria Coos Bay Florence (not held; no show)b Grants Pass Hood River (English) Hood River (Spanish) Klamath Falls (x2) La Grande (1-not held/no show; 2-rescheduled and held) Lincoln City Madras Me Minnville Pendleton Prineville Redmond Roseburg St Helens The Dalles (x2 English) The Dalles (Spanish) Tillamook Woodburn (Not held; no show)b |
| Frontier (n = 2) | a county with 6 people or less per square mile | Baker City Burns (1 was a no show; rescheduled and held) Lakeview (Not held; no show)b |
Community setting definitions obtained from (Oregon Office of Rural Health, 2019a).
Denotes that focus groups were not held at those locations due to participants not attending.
APPENDIX F.
Specific marketing approaches recommended by community settings
| Main theme | Sub-theme | Examples | Urban (n = 13) | Rural (n = 20) | Frontier (n = 2) | Total (n = 35) |
|---|---|---|---|---|---|---|
| Format | Includes things such as mail, flyers/brochures/posters, billboard, and newspaper/ magazines | 5 (38%); 1.2 | 16 (80%); 1.7 | 0 (0%); 0 | 21 (60%); 1.6 | |
| Social Media | Includes things such as surveys, e-mail, Facebook/ Instagram/Twitter, and websites | 9 (69%); 1.9 | 11 (55%); 1.6 | 1 (50%); 1.0 | 21 (60%); 1.7 | |
| In person | Word of mouth and social networks, tabling at community events, health fairs, and public meetings/ town hall | 5 (38%); 2.2 | 14 (70%); 1.7 | 1 (50%); 1.0 | 20 (57%); 1.8 | |
| Broadcasting | Includes things such as television and radio ads | 3 (23%); 1.7 | 10 (50%); 1.2 | 0 (0%); 0 | 13 (37%); 1.3 | |
| Telecommunication | Includes things such as Google hangouts or Skype | 1 (8%); 1.0 | 1 (5%); 1.0 | 0 (0%); 0 | 2 (6%); 1.0 | |
| Organizations and location | Community public spaces and groups | Includes places such as religious/spiritual centers, medical/wellness clinics, learning institutions, and senior centers | 7 (54%); 1.71 | 16 (80%); 2.56 | 1 (50%); 5.00 | 24 (69%); 2.42 |
| Private spaces and groups | Includes places such as gyms, grocery stores, or offices | 1 (8%); 1.0 | 4 (20%); 1.0 | 0 (0%); 0 | 5 (14%); 1.0 | |
| Marketing approach | Convenience/ benefits/concerns | Messages that highlight the incentives for participating (both incentive and result benefits), access to resources, credibility of the researching organization, and costs. | 7 (54%); 3.6 | 12 (60%); 2.7 | 1 (50%); 3.0 | 20 (57%); 3.0 |
| Target audience | Language used and outreach methods for recruitment of specific demographic groups including age, sex/ gender, cancer survivors, or messaging that speaks to altruistic individuals. | 6 (46%); 2.3 | 11 (55%); 1.6 | 1 (50%); 2.0 | 18 (51%); 1.9 | |
| Provide education | Messages that are more educational to aid in reduction of stigma/fear about the subject. | 4 (31%); 2.3 | 5 (25%); 1.5 | 1 (50%); 1.5 | 10 (29%); 1.8 | |
| Relevance | Messages that highlight the connection to, or importance of, cancer, family history, and cancer genetic screenings to the individual. | 3 (23%); 2.7 | 7 (35%); 1.6 | 0 (0%); 0 | 10 (29%); 1.9 |
Note: Participants were asked ‘Do you have any recommendations for sharing the information with people in your community?’ with observed sub-themes and definitions reported as a companion to Table 5. Results are displayed as number and percentage of urban/rural/frontier sites mentioning that theme—not the number of people mentioning the theme—along with average number of mentions by community setting. The number of sites mentioning a theme and percent was calculated by frequency of sites mentioning a theme divided by total sites in that community setting. Average mentions by site were calculated by dividing total mentions of a theme by the total sites mentioning that theme.
Footnotes
Conflicts of interest
Teala W. Alvord, Lisa K. Marriott, Phuc T. Nguyen Autumn Shafer, Kim Brown, Wesley Stoller, Jennifer L. Volpi, Jill Vandehey-Guerrero, Laura K. Ferrara, Steven Blakesley, Erin Solomon, Hannah Kuehl, Amy J. Palma, Paige E. Farris, Kelly J. Hamman, Madisen Cotter, and Jackilen Shannon have no conflicts of interest to report.
Human studies and informed consent
This study was reviewed by OHSU’s Institutional Review Board (IRB, STUDY #17573). Potential participants reviewed an information sheet and were given time to ask questions of the research team. All participants provided verbal assent prior to participating in focus groups in order to maintain participant privacy.
Animal studies
No non-human animal studies were carried out by the authors for this article.
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