Abstract
Background and Objectives
Presentation, progression, and treatment of Parkinson disease (PD) can differ based on sex and gender. However, knowledge on PD is limited by the characteristics of research participants, and most of the participants are men. In this study, we aimed to identify the attitudes toward and barriers to research participation for people with PD (PwP) based on their sexual orientation and gender identity.
Methods
Data were obtained from the Fox Insight on March 16, 2023, for PwP who completed the Attitudes and Beliefs Regarding Research and Genetic Testing for PD. Responses were compared between sexual and gender minorities (SGM) (n = 136), cisgender heterosexual women (n = 1,479), and cisgender heterosexual men (n = 1,445). Associations between age, socioeconomic variables, and the responses that differed between the groups were assessed with linear models.
Results
More than 68% of the participants were willing to participate in research; only 43.7% heard about research opportunities, and 52.3% knew where to find a study. Approximately 86.8% of the participants reported hearing about a study from their doctor would make them more likely to participate. A higher percentage of SGM were concerned about transportation and researchers not understanding or respecting their beliefs; a higher percentage of cisgender heterosexual women were concerned about transportation, data privacy, and their family's reaction to genetic results; and a higher percentage of cisgender heterosexual men were concerned about time required for research activities and complex forms. Age and socioeconomic variables were significantly associated with approach toward research that differed between the groups.
Discussion
PwP are willing to participate in research, and health care providers can facilitate their participation. Barriers to research participation related to sexual and gender identity exist and must be addressed to increase our understanding of PD in underrepresented populations.
Introduction
Affecting nearly 10 million people worldwide, Parkinson disease (PD) is the second most common neurodegenerative disorder and the fastest growing neurologic disorder.1 Within recent decades, increasing evidence suggests that sex and gender play a role in the expression and experience of PD.2 Sex refers to the anatomical or genetic characterizations of male and female, while gender refers to a person's identity as an expression of their internal sense of self.3
Research demonstrates that cisgender men have a higher risk of developing PD and generally have an earlier age at onset, a faster progression of disease, and a more severe phenotype compared with cisgender women.4-9 In addition, studies indicate that cisgender women may display higher rates of nonmotor symptoms such as fatigue, mood disorders, and chronic pain and may have more tremor-predominant disease.9,10 Although cisgender women and people who identify as sexual and gender minorities (SGM) with PD may be at a higher risk of discrimination in health care settings, few studies have investigated PD-specific factors such as age at disease onset, predominant symptoms, and treatment response in relation to gender and sexual identity.11 The studies exploring the role of gender identity in PD have mostly investigated quality-of-life measures, finding that people with PD (PwP) who identify as more androgynous or masculine may have higher quality of life.12,13 No studies have explored the impact of sexual orientation on PD outcomes.
It is well known that the characteristics of study participants affect the results from research studies. Recruitment from clinical and community-based samples introduce potential biases due to sampling differences and influence the generalizability of the data. Currently, participants in PD research studies are predominantly male individuals, who identify as White, from higher socioeconomic backgrounds with access to movement disorder specialty centers.14 Female individuals are less likely to participate in research, which limits the generalizability of the findings. Even less is known about the needs of PwP identifying as SGM or lesbian, gay, bisexual, transgender, queer, intersex, and additional sexual and gender diverse identities.15 Systematically collecting information on sex, gender identity, and sexual orientation and supporting efforts to include underrepresented PwP in clinical research can help us understand the pathophysiology and develop more effective treatment approaches for everyone.16
Differences in the presentation, progression, and burden of symptoms, alongside differences in preferred treatments, treatment responses, and side effects for female and male individuals underscore the importance of considering sex, gender identity, and sexual orientation both in the clinic and research for PD.2 Compared with male individuals, female individuals with PD have lower rates of health care utilization, experience a delay in getting a PD diagnosis and referral to a specialist, have less access to advanced therapies, and receive less caregiving support.2,17 SGM with PD are at a higher risk of experiencing discrimination while receiving health care, which can lead to mistrust in health care and a tendency to delay or forego care.11 To increase participation of PwP within underrepresented SGM groups and to initiate efforts to support their inclusion, we aimed to identify the barriers for research participation affecting these groups, using data from Fox Insight, an online study of people living with or without PD.18 Based on the group differences for attitude toward different types of research, we also discuss potential solutions to support participation of underrepresented PwP in research.
Methods
The Fox Insight dataset includes the routine collection of longitudinal assessments and one-time questionnaires from people with and without PD. Fox Insight was formally launched in October, 2017. Data used in the preparation of this study were obtained on March 16, 2023.19 For up-to-date information on the study, visit the Fox Insight website.19
Standard Protocol Approvals, Registrations, and Patient Consents
The Fox Insight study is approved by New England IRB (IRB#: 120160179), and informed consent is obtained from each participant. Our analysis included people reporting a PD diagnosis after the age of 18 years, who completed the Attitudes and Beliefs Regarding Research and Genetic Testing for Parkinson's Disease questionnaire and questions about sex assigned at birth, gender identity, and sexual orientation, which was administered only once (n = 3,060). Participants were allowed to choose only one response for questions on sex assigned at birth, gender identity, and sexual orientation. For sex assigned at birth, participants were asked what sex they were assigned at birth on their original birth certificate with response options including male, female, and prefer not to answer. For gender identity, participants were asked what their current gender identity was with response options including male, female, transgender, something else (gender nonconforming, genderqueer, nonbinary, etc), not sure, and prefer not to answer. For sexual orientation, participants were asked whether they consider themselves to be heterosexual or straight, gay or lesbian, bisexual, something else (pansexual, asexual, etc), not sure, and prefer not to answer. For our analysis, the groups consisted of (1) SGM (discordant sex assigned at birth and gender identity, gender identity other than woman or man, or sexual orientation other than heterosexual, n = 136, eTable 1 for individual identities), (2) cisgender heterosexual women (female for sex assigned at birth, woman for gender identity, heterosexual for sexual orientation, n = 1,479), and (3) cisgender heterosexual men (male for sex assigned at birth, man for gender identity, heterosexual for sexual orientation, n = 1,445).
The Attitudes and Beliefs Regarding Research and Genetic Testing for PD questionnaire was administered only once and consists of 6 question blocks including: (1) introduction (PD diagnosis and age at diagnosis), (2) knowledge on PD, (3) knowledge, experience on, and attitude toward medical research, (4) knowledge, experience on, and attitude toward genetic testing, (5) knowledge, experience on, and attitude toward exposures, behaviors, and symptoms related to disease risk, and (6) general attitude toward medicine, exercise, and family history for PD, Alzheimer disease, or dementia (see eAppendix 1 for the questionnaire). To investigate awareness about prior experience with and attitudes toward PD research, questions from blocks 3, 4, and 5 were examined.
Statistical analyses were conducted using IBM SPSS version 28.0 (Armonk, NY: IBM Corp) and R version 4.2.2.20 Differences between SGM and cisgender heterosexual PwP groups were compared using χ2 tests for categorical variables, Kruskal-Wallis tests for ordinal variables with Mann-Whitney U tests for pairwise comparisons, and analysis of variance for continuous variables with post hoc tests for pairwise comparisons. For significant group differences regarding research experience, attitude, and awareness; associations between these items and age, age at PD diagnosis, and socioeconomic variables (education, income level, employment status, and location) were investigated with generalized linear models. False discovery rate was used for multiple comparison correction. Listwise deletion was used for missing data. Alpha level was set at 0.05 for significance.
Data Availability
Qualified researchers may request access to all deidentified data in the Fox Insight used for this study.19
Results
In total, 3,060 PwP were included in the analysis with 87.7% from North America and 97.6% identifying as White (Table 1 for demographics). Cisgender heterosexual women and SGM were younger than cisgender heterosexual men. The mean age was similar for cisgender heterosexual women and SGM. Cisgender heterosexual women had lower levels of education than cisgender heterosexual men and SGM. Level of education was similar for SGM and cisgender heterosexual men. Cisgender heterosexual men were less likely to be unemployed than cisgender heterosexual women and SGM. SGM were more likely to be employed full-time and less likely to be retired than cisgender heterosexual men. Cisgender heterosexual men had higher levels of income than cisgender heterosexual women and SGM. Compared with age at PD diagnosis of cisgender heterosexual men (62.4 [9.35] years), SGM (59.9 [10.9] years) and cisgender heterosexual women (60.4 [9.41] years) were younger at PD diagnosis (p ≤ 0.033 for both). There was no significant difference for age at diagnosis between SGM and cisgender heterosexual women (p = 0.91).
Table 1.
Demographics Across the Groups
| Variable | Sexual and gender minorities (SGM) (n = 136) | Cisgender heterosexual women (n = 1,479) | Cisgender heterosexual men (n = 1,445) |
| Age* | 66.8 (9.13)a | 67.9 (8.43)a | 69.6 (8.36)b,c |
| Hispanic ethnicity | 11 (8.1) | 72 (4.9) | 67 (4.6) |
| Race | |||
| American Indian or Alaska Native | 0 (0) | 2 (0.1) | 3 (0.2) |
| Asian | 1 (0.7) | 15 (1.0) | 16 (1.1) |
| Black or African American | 1 (0.7) | 4 (0.3) | 3 (0.2) |
| Native Hawaiian or Other Pacific Islander | 0 (0) | 0 (0) | 0 (0) |
| White | 129 (96.3) | 1,432 (97.6) | 1,410 (97.8) |
| More than 1 race | 3 (2.2) | 14 (1.0) | 9 (0.6) |
| Education level* | c | a ,b | c |
| Less than high school | 1 (0.7) | 13 (0.9) | 11 (0.8) |
| High school degree (GED or equivalent) | 18 (13.2) | 369 (25.1) | 296 (20.5) |
| Associate's degree | 8 (5.9) | 147 (10.0) | 106 (7.4) |
| Bachelor's degree | 45 (33.1) | 416 (28.3) | 436 (30.2) |
| Graduate or professional school degree | 64 (47.1) | 527 (35.8) | 593 (41.1) |
| Employment status* | a | a | b ,c |
| Unemployed | 12 (8.8) | 93 (6.3) | 45 (3.1) |
| Employed part-time | 16 (11.8) | 168 (11.4) | 206 (14.3) |
| Employed full-time | 21 (15.4) | 118 (8.0) | 84 (5.8) |
| Retired | 87 (64.0) | 1,093 (74.3) | 1,103 (76.7) |
| Income level* | a | a | b ,c |
| Less than $20,000 | 5 (4.2) | 76 (6.2) | 45 (3.5) |
| $20,000 to $34,999 | 17 (14.3) | 138 (11.3) | 80 (6.3) |
| $35,000 to $49,000 | 20 (16.8) | 171 (14.0) | 133 (10.4) |
| $50,000 to $74,999 | 27 (22.7) | 242 (19.8) | 249 (19.5) |
| $75,000 to $99,999 | 17 (14.3) | 223 (18.2) | 232 (18.2) |
| More than $100,000 | 33 (27.7) | 374 (30.6) | 536 (42.0) |
| Location based on WHO regions | |||
| Africa | 0 (0) | 3 (0.2) | 5 (0.3) |
| America | 122 (89.7) | 1,284 (86.8) | 1,277 (88.4) |
| Eastern Mediterranean | 0 (0) | 0 (0) | 1 (0.1) |
| Europe | 6 (4.4) | 120 (8.1) | 108 (7.5) |
| South-East Asia | 0 (0) | 2 (0.1) | 7 (0.5) |
| Western Pacific | 8 (5.9) | 70 (4.7) | 47 (3.3) |
Abbreviations: SGM = sexual and gender minorities; WHO = World Health Organization.
Mean (standard deviation) or n (%) is reported. Significant group differences are marked with *. Age is compared with analysis of variance with pairwise comparisons, income and education levels are compared with Kruskal-Wallis and Mann-Whitney U tests, and other variables are compared with χ2 tests.
Statistically different from cisgender heterosexual men.
Statistically different from SGM.
Statistically different from cisgender heterosexual women.
Research Experience
In addition to participating in Fox Insight, 52.6% of SGM, 54.8% of cisgender heterosexual women, and 57.6% of cisgender heterosexual men reported that they have or are participating in other PD research studies (p = 0.45). Most of the cohort reported having completed surveys or questionnaires online for PD research (82.5%, Table 2 for individual groups). A higher percentage of cisgender heterosexual men reported having participated in a PD trial with oral medicine compared with SGM and cisgender heterosexual women. A higher percentage of cisgender heterosexual men reported having participated in a PD trial with exercise compared with cisgender heterosexual women. Younger age at PD diagnosis, older age in general, and location (Americas, Western Pacific > Europe) were associated with a history of participating in a PD trial with oral medicine (p ≤ 0.014 for all). Younger age at PD diagnosis, older age in general, and higher income level were associated with a history of participating in a PD trial with exercise (p ≤ 0.033 for all).
Table 2.
Types of Parkinson Disease Research Activities People Reported to Have Done or They Would Be Willing to Do in the Future
| Type of research activity that was done | SGM (n = 70) | Cisgender heterosexual women (n = 768) | Cisgender heterosexual men (n = 787) |
| Surveys or questionnaires online | 56 (80.0) | 629 (81.9) | 656 (83.4) |
| Surveys or questionnaires by phone | 17 (24.3) | 214 (27.9) | 216 (27.4) |
| Surveys or questionnaires in the clinic | 26 (37.1) | 250 (32.6) | 271 (34.4) |
| Medical interview and examination using a computer or smartphone | 16 (22.9) | 194 (25.3) | 217 (27.6) |
| Medical interview and examination in the clinic | 33 (47.1) | 313 (40.8) | 323 (41.0) |
| Oral medicine* | 10 (14.3)a | 173 (22.5)a | 256 (32.5)b,c |
| IV medicine | 3 (4.3) | 53 (6.9) | 69 (8.8) |
| Medicine as a skin patch | 0 (0) | 16 (2.1) | 22 (2.8) |
| Medicine as a muscle injection | 1 (1.4) | 26 (3.4) | 30 (3.8) |
| Medicine through an inhaler | 0 (0) | 15 (2.0) | 18 (2.3) |
| Medicine through a tube into the intestine | 0 (0) | 4 (0.5) | 4 (0.5) |
| Give saliva sample | 23 (32.9) | 262 (34.1) | 226 (28.7) |
| Give blood sample | 24 (34.3) | 285 (37.1) | 280 (35.6) |
| Outpatient procedure such as skin biopsy or lumbar puncture | 11 (15.7) | 90 (11.7) | 100 (12.7) |
| Exercise | 15 (21.4) | 169 (22.0)a | 215 (27.3)c |
| Brain scan | 18 (25.7) | 189 (24.6) | 215 (27.3) |
| Brain surgery | 4 (5.7) | 31 (4.0) | 44 (5.6) |
| Type of research activity willing to do, % | SGM (n = 133) | Cisgender heterosexual women (n = 1,433) | Cisgender heterosexual men (n = 1,411) |
| Surveys or questionnaires online | 126 (94.7) | 1,367 (95.4) | 1,340 (95.0) |
| Surveys or questionnaires by phone | 91 (68.4) | 1,042 (72.7) | 985 (69.8) |
| Surveys or questionnaires in the clinic | 100 (75.2) | 1,105 (70.8) | 990 (70.2) |
| Medical interview and examination using a computer or smartphone | 116 (87.2) | 1,154 (80.5) | 1,115 (79.0) |
| Medical interview and examination in the clinic | 104 (78.2) | 1,076 (75.1) | 1,091 (77.3) |
| Oral medicine* | 85 (63.9)a | 776 (54.2)a | 1,043 (73.9)b,c |
| IV medicine* | 51 (38.3) | 429 (29.9)a | 610 (43.2)c |
| Medicine as a skin patch* | 73 (54.9) | 671 (46.8)a | 849 (60.2)c |
| Medicine as a muscle injection* | 59 (44.4) | 473 (33.0)a | 660 (46.8)c |
| Medicine through an inhaler* | 59 (44.4) | 544 (38.0)a | 714 (50.6)c |
| Medicine through a tube into the intestine* | 12 (9.0) | 112 (7.8)a | 178 (12.6)c |
| Give saliva sample | 113 (85.0) | 1,216 (84.9) | 1,210 (85.8) |
| Give blood sample | 114 (85.7) | 1,190 (83.0) | 1,169 (82.8) |
| Outpatient procedure such as skin biopsy or lumbar puncture* | 49 (36.8) | 374 (26.1)a | 508 (36.0)c |
| Exercise | 101 (75.9) | 1,078 (75.2) | 1,111 (78.7) |
| Brain scan* | 104 (78.2) | 981 (68.5)a | 1,035 (73.4)c |
| X-ray, MRI, ultrasound, or nuclear medicine scan of another area (not the brain) | 94 (70.7) | 945 (65.9) | 987 (70.0) |
| Brain surgery* | 13 (9.8) | 98 (6.8)a | 143 (10.1)c |
Abbreviation: SGM = sexual and gender minorities.
N (%) is reported for variables. Significant group differences with χ2 tests are marked with *.
Statistically different from cisgender heterosexual men.
Statistically different from SGM.
Statistically different from cisgender heterosexual women.
Awareness About Research
Most of the cohort were aware about what clinical studies entailed (84.2%) and that research can help find new treatments or cures (97.9%, Table 3 for individual groups). Less than half of the cohort reported hearing about research opportunities (43.7%). Only half of the cohort knew where to find a study and sign up if they wanted to take part in research (52.3%). Compared with cisgender heterosexual men, a lower percentage of cisgender heterosexual women were knowledgeable about implications of clinical studies and genetic testing. There were no other group differences for items related to awareness about research. Age or socioeconomic variables were not associated with items regarding implications of clinical studies or genetic testing (p > 0.061 for all).
Table 3.
Awareness About and Attitude Toward Research Across the Groups
| Statement, agree | SGM (n = 136) | Cisgender heterosexual women (n = 1,479) | Cisgender heterosexual men (n = 1,445) |
| Clinical studies test the effects of procedures, drugs, or treatments that no one is yet certain about | 115 (94.3) | 1,210 (94.9)a | 1,244 (96.1)b |
| Research studies can help scientists find new treatments or cures for diseases | 133 (97.8) | 1,436 (97.8) | 1,415 (98.1) |
| Anyone who qualifies can take part in medical research studies | 98 (72.6) | 1,047 (71.4) | 1,023 (71.0) |
| I hear about research opportunities in my community | 61 (45.9) | 612 (41.8) | 653 (45.4) |
| If I wanted to take part in a research study, I would know where to find a study and sign up | 74 (54.8) | 759 (51.7) | 758 (52.6) |
| I would take part in a research study that might help people with Parkinson disease, even if it did not benefit me directly* | 119 (100) | 1,160 (96.1)a | 1,235 (98.0)b |
| If a trusted member of my community told me about a research study, it would make me more likely to take part | 84 (86.6) | 948 (87.0)a | 1,000 (88.0)b |
| If my doctor told me about a research study, it would make me more likely to take part | 119 (98.3) | 1,242 (96.1)a | 1,267 (96.3)b |
| If a research study was linked to an academic institution, it would make me more likely to take part | 96 (72.2) | 947 (65.0) | 923 (64.5) |
| If I had a personal connection to the disease being studied in a research study, I would be more likely to take part* | 122 (98.4) | 1,255 (96.1)a | 1,278 (96.0)b |
| Genetic testing could help scientists' efforts to find cures and treatments for Parkinson disease | 103 (100) | 1,232 (99.8)a | 1,238 (99.3)b |
| I have concerns about genetic testing | 17 (13.3) | 199 (13.9) | 176 (12.5) |
| I would be concerned about my family's reaction to my genetic test results* | 16 (13.8)b | 354 (29.5)a,c | 268 (21.8)b |
| I have concerns about participating in a research study on exposures, behaviors, or symptoms that may be linked to Parkinson disease | 7 (5.4) | 105 (7.4) | 95 (6.8) |
Abbreviation: SGM = sexual and gender minorities.
N (%) for agreement is reported for statements. Significant group differences with χ2 tests are marked with *.
Statistically different from cisgender heterosexual men.
Statistically different from cisgender heterosexual women.
Statistically different from SGM.
Attitude Toward Research
Most of the cohort were willing to complete surveys or questionnaires online (95.2%), by phone (71.1%), or in the clinic (70.7%). Most of the participants were also willing to participate in research that entailed a medical interview and examination in the clinic (76.3%), a computer or smartphone (80.1%), saliva collection (85.3%), blood sample (83.1%), exercise (76.9%), a brain scan (71.2%), and an X-ray, MRI, ultrasound, or nuclear medicine scan of another area (not the brain) (68.1%) (Table 2 for individual groups). A higher percentage of cisgender heterosexual men were willing to participate in a PD trial with oral medicine compared with SGM and cisgender heterosexual women. Older age at PD diagnosis, younger age in general, higher education level, and employment status (employed full-time > unemployed) were associated with willingness to participate in a trial with oral medicine (p < 0.047 for all).
Compared with cisgender heterosexual men, a lower percentage of cisgender heterosexual women were willing to participate in a PD trial with a brain scan, brain surgery, outpatient procedures such as a skin biopsy or lumbar puncture, and medicine given through IV, skin patch, muscle injection, inhaler, or an intestinal tube. Younger age, older age at diagnosis, and higher education level were associated with willingness to participate in a trial with a brain scan, skin biopsy, lumbar puncture, IV medication, transdermal medication, and injected medications (p < 0.011 for all). Older age at PD diagnosis, younger age in general, higher education level, and employment status (employed full-time > unemployed) were associated with willingness to participate in a trial with medicine through an inhaler (p ≤ 0.049 for all). Higher education level and location (Europe > Western Pacific and Americas) were associated with willingness to participate in a trial with medicine through an intestinal tube (p < 0.015 for both). Lower income level was associated with willingness to participate in a trial with brain surgery (p = 0.004).
Compared with cisgender heterosexual men, a lower percentage of cisgender heterosexual women reported they would take part in PD research, and hearing about a research study from a trusted member of their community, their doctor or having a personal connection to the disease being studied would make them more likely to take part. Older age at PD diagnosis, younger age in general, and higher education level were associated with a higher likelihood of participating in PD research even if it did not benefit them (p < 0.037 for all). Older age at PD diagnosis and younger age in general were associated with higher likelihood of participating in PD research if a trusted member of my community told them about it (p ≤ 0.009 for both). Location (Americas, Western Pacific > Europe) was associated with a higher likelihood of participating in PD research if their doctor told them about it (p = 0.003). Higher education level was associated with a higher likelihood of participating in PD research if they had a personal connection to the disease being studied (p < 0.001).
Overall, 78.7% of SGM, 76.7% of cisgender heterosexual women, and 73.1% of cisgender heterosexual men reported that they have concerns about taking part in research (p = 0.13; Figure 1 for specific concerns). Compared with cisgender heterosexual men, a higher percentage of SGM had concerns about transportation to and from the research center and that researchers may not understand and respect their religious or cultural beliefs; a higher percentage of cisgender heterosexual women had concerns about transportation and privacy of their health information; a lower percentage of cisgender heterosexual women had concerns about the time it takes to do research activities, complex instructions, or consent forms (p ≤ 0.033 for all).
Figure 1. Percentage of PwP in Each Group Reporting Concerns About Taking Part in Research.
Statistically significant group differences with χ2 tests are marked with *.
Younger age at PD diagnosis, older age in general, lower income level, employment status (unemployed > retired > employed part-time > employed full-time), and location (Americas, Western Pacific > Europe) were associated with concerns about transportation (p ≤ 0.009 for all). Lower income level was associated with concerns of PwP about researchers not respecting their religious or cultural beliefs (p = 0.011). Older age, higher education level, employment status (employed full-time > employed part-time, retired, unemployed), and location (Americas, Western Pacific > Europe) were associated with concerns about the time it takes to do research activities (p < 0.047 for all). Location (Americas, Western Pacific > Europe) was associated with the concerns of PwP about the privacy of their health information (p = 0.022). Lower education level and location (Americas > Europe, Western Pacific) were associated with concerns about complex instructions or consent forms (p < 0.018 for both).
Of the overall cohort, 13.2% had concerns about genetic testing and 7.1% had concerns about participating in a research study on exposures, behavior, or symptoms that may be linked to PD (Table 3 for individual groups; Figures 2 and 3 for specific concerns). Compared with cisgender heterosexual men and SGM, a higher percentage of cisgender heterosexual women were concerned about their family's reaction to their genetic test results (p ≤ 0.004 for both). Younger age at PD diagnosis, older age in general, and location (Europe > Americas, Western Pacific) were associated with the concerns of PwP about their family's reaction to their genetic test results (p ≤ 0.007 for all). There were no other group differences for specific concerns about genetic testing or participating in research on exposures, behavior, or symptoms that may be linked to PD.
Figure 2. Percentage of PwP in Each Group Reporting Specific Concerns About Genetic Testing.
Figure 3. Percentage of PwP in Each Group Reporting Specific Concerns About Participating in a Research Study on Exposures, Behavior, or Symptoms That May Be Linked to PD.
Discussion
In this study, we assessed attitude toward and barriers for research participation across PwP from different sexual orientation and gender identity (SOGI) backgrounds, including SGM and cisgender heterosexual women and men, using the Fox Insight dataset. Potential barriers and facilitators to research participation for SGM with PD based on existing findings are outlined in Table 4 and eFigure 1.21,22 Most of our cohort were aware about what research entails and were willing to participate in various types of research. However, only half of the cohort knew where to find a study and sign up and less than half reported hearing about research opportunities. A higher proportion of cisgender heterosexual men were willing to participate in a PD trial with medication delivered in different ways, including different imaging and invasive approaches. Hearing about a study from a trusted member of their community or their doctor or having a personal connection to the disease made cisgender heterosexual men more likely to take part in research. There were also group differences for barriers underscored in relation to research participation. Transportation and researchers not understanding and respecting their religious or cultural beliefs were brought up as concerns by a higher percentage of SGM with PD. Transportation, privacy of health information, and family's reaction to genetic test results were brought up as concerns by a higher percentage of cisgender heterosexual women. The time it takes to complete research, complex instructions, or consent forms was brought up as a concern by a higher percentage of cisgender heterosexual men. Age in general, age at PD diagnosis, and other socioeconomic variables included in the models were associated with the approach toward research, which differed between groups. These findings suggest that there may be various ways to overcome barriers to support inclusion of underrepresented PwP in research.
Table 4.
Proposed Barriers and Facilitators for Research Participation in Sexual and Gender Minority (SGM) Populations
| Barriers |
| More likely to be unemployed |
| More likely to have lower income |
| Younger age at PD diagnosis |
| Higher rates of poor health outcomes |
| Higher rates of mistrust in the health care system and in health care professionals and research teams |
| Higher rates of concern that researchers will not respect their cultural and religious beliefs |
| Facilitators |
| Inclusive clinical spaces, including but not limited to asking gender identity/pronouns at intake appointment and posting signs/flags demonstrating that clinic is a safe space for SGM |
| Clinical and research team education on cultural competence, sexual and gender identity, health disparities for SGM, and respectful communication strategies |
| Partnership with community clinics and community health care workers |
| Involving community stakeholders in the creation and execution of research |
| Allocating study funds for person-specific barriers (i.e., transportation) |
Education-level difference across the groups in our cohort, with lower years of education for cisgender heterosexual women, is in line with the global gender disparities for educational attainment. Although the global gender gap for educational attainment has been improving over the years, the gap for the older adults likely remains.23 The impact of education on trial participation is an important finding. People with higher levels of education were more willing to participate in research and had less concerns about complex instructions or consent forms in studies. Cisgender heterosexual women were less aware of the implications of clinical trials and genetic testing and had more concerns about privacy of their health information. Thus, investing in general education and research-related health literacy and education should be considered to support greater inclusion in research. Investing in outreach activities and training of community health workers, promotoras, and community members can help educate and engage underrepresented communities to participate in research.24,25
Income and employment status are other important factors for research participation, which differed across the groups. Both SGM and cisgender heterosexual women had lower income than cisgender heterosexual men. Lower income in general was associated with barriers for research participation, including concerns about transportation and researchers not understanding and respecting their religious or cultural beliefs. Both income and employment status can limit the ability to travel for a research visit. Taking time off to travel or complete a research visit may not be as feasible for low-income persons who must work full-time. Cisgender heterosexual women and SGM with PD were significantly younger than the cisgender heterosexual men with PD in our cohort. Previous studies have reported missing work and long-time commitments as barriers for younger people to participate in research.26 Transportation is often noted as an important barrier for research participation among older adults,27 and an estimated 70% of participants have been reported to live more than 2 hours away from a research site.26 Our findings show that transportation was a barrier reported more frequently by SGM and cisgender heterosexual women compared with cisgender heterosexual men. Employment status and income level likely contribute to this difference across the groups. Cisgender heterosexual men reported concerns about the time it takes for research and the complexity of research instructions or consent forms. To overcome these barriers, study designs can implement more remote visits to limit travel by providing the necessary equipment because resources at one's home will also differ based on socioeconomic status, implement the use of wearable devices to collect data, offer visits outside of 9-to-5 work hours, and use plain and education-level appropriate language in research materials and ensure extra time to describe and answer questions/concerns about the research. Financial incentives to reimburse for transportation and lodging and compensation for participating can also help reduce the burden and improve participation.28,29
Minority groups and individual-level differences within these minority groups should be considered given there may be unique barriers for research participation and likely one size does not fit all.30 PwP identifying as cisgender heterosexual women or SGM are at a higher risk of discrimination while receiving health care compared with cisgender heterosexual men.11 The clinical team plays an important role in raising awareness about research, and experiences of discrimination during a clinical visit result in minority groups avoiding research participation. It is well known that there has been significant underrepresentation of certain populations in clinical research, including cisgender heterosexual women and SGM.31 Although these disparities are improving through regulatory efforts by the US Food and Drug Administration and NIH, there are still high levels of underrepresentation of these populations, especially in particular fields of medicine. Neurology has the second highest rate of female underrepresentation in clinical research relative to the burden of neurologic disease in this population.32 As our findings point out, cisgender heterosexual women and SGM are willing to participate in PD research, but still have concerns about privacy, transportation, and researchers respecting their cultural and religious beliefs. There are multiple approaches to overcome these barriers, including involvement of cisgender heterosexual women and SGM in the design and execution of research studies, partnerships with community clinics to allow for increased accessibility to research in academic centers, and allocation of study funds toward clinician education on health disparities and transportation costs. Within the more marginalized populations of PwP, efforts to increase awareness of research opportunities from health care providers is greatly needed.33 Providers should not assume disinterest, but instead provide opportunities and inquire about barriers for participation that can possibly be mitigated with appropriate measures and plans to assist these groups with overcoming addressable barriers.
Even in this cohort with potentially more access and awareness about research due to their concurrent enrollment in the Fox Insight study, we found that half of the participants did not know how to find a study and enroll. This raises significant concerns in the accessibility of PD research. Because women and SGM have less access to specialty care and experience more health disparities, community health care providers can play an important role in raising awareness about research opportunities.34,35 Thus, engaging community health care providers serving minoritized groups and building diverse and representative teams with proper training and competence to communicate, educate, and support these groups can increase the inclusion of underrepresented populations in PD and related research.30,36
Our study has several strengths, including leveraging data from the Fox Insight study, which allowed us to analyze data on a wide variety of experiences from a large population of PwP. Due to fears of discrimination, SGM may underreport their SOGI during clinical or research visits, and self-report surveys in Fox Insight can provide a better insight to the SGM participants. Our study has several limitations as well. Participants in the Fox Insight dataset likely represent those with more access to and awareness about research. In addition, it is possible that our findings may overestimate or underestimate the true prevalence of factors related to research participation due to selection bias within self-reported questionnaires. Most of our cohort identified as White and had a high level of education, which not only demonstrates the significant racial and ethnic disparities present in PD research but likely affects the generalizability of our findings. It is possible that barriers and facilitators to research participation for PwP not identifying as White are different than those found in this study. Furthermore, only a small portion of participants in our cohort identified as SGM, and individuals who identify as SGM were grouped together for analysis due to the limited sample size. Within the SGM group, 89% of the participants identified as cisgender and bisexual, lesbian, or gay. We were unable to investigate attitudes toward and experiences in research by more nuanced identities that likely vary. Although there were several socioeconomic differences across the groups, we did not control for these factors in our models to not disregard the disparities experienced by the participants based on their SOGI and to avoid overfitting and introducing further selection bias. Future research, including qualitative studies, is needed to more deeply investigate the relationships that PwP have with research and further understand the barriers and facilitators to research participation for underrepresented groups.
In conclusion, we found that there were group differences in the types of concerns PwP had about research participation, highlighting that social identities and cultural norms may play an important role in barring and facilitating participation in research. There is need for more community outreach and efforts from all stakeholders to recruit PwP underrepresented in research. Clinical research forms the basis of developing standard-of-care for diagnosis and treatment; however, there may be problems with current findings being limited to predominantly White and cisgender heterosexual male cohorts. More inclusive studies that explore the epidemiology, risk factors, symptoms, and disease progression among PwP who have not routinely been included in research can provide a better insight to the disease pathophysiology, guide clinical trials, and ensure there is a cure for PD for all people. It is extremely important that investigators move toward a more inclusive approach to ensure that underrepresented groups are engaged, are recruited, participate, and benefit from future research and treatments.
Acknowledgment
The authors thank the Parkinson community for participating in this study to make this research possible. The authors also thank Frida Güneş, Tar, and San for their support and commitment to improving the lives of people from minoritized groups.
Appendix. Authors
| Name | Location | Contribution |
| Ece Bayram, MD, PhD | Parkinson and Other Movement Disorders Center, Department of Neurosciences, University of California, San Diego | Drafting/revision of the article for content, including medical writing for content; major role in the acquisition of data; study concept or design; and analysis or interpretation of data |
| Nicole Rigler, MD | School of Medicine, University of California, San Diego | Drafting/revision of the article for content, including medical writing for content |
| Kevin T. Wang | Parkinson and Other Movement Disorders Center, Department of Neurosciences, University of California, San Diego | Analysis or interpretation of data |
| Andrew Tsai | Parkinson and Other Movement Disorders Center, Department of Neurosciences, University of California, San Diego | Analysis or interpretation of data |
| Jason D. Flatt, PhD | Department of Environmental and Occupational Health, School of Public Health, University of Nevada, Las Vegas | Drafting/revision of the article for content, including medical writing for content |
Study Funding
The Fox Insight Study is funded by the Michael J. Fox Foundation for Parkinson's Research. E. Bayram is supported by the National Institute on Aging (K99AG073453). J.D. Flatt is supported by the National Institute on Aging (K01AG056669; R24AG066599; R01AG083177) and Michael J. Fox Foundation for Parkinson's Research (MJFF-020943).
Disclosure
The authors report no relevant disclosures. Full disclosure form information provided by the authors is available with the full text of this article at Neurology.org/cp.
References
- 1.GBD 2016 Parkinson's Disease Collaborators, Elbaz A, Nichols E, et al. Global, regional, and national burden of Parkinson's disease, 1990-2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet Neurol. 2018;17(11):939-953. doi: 10.1016/S1474-4422(18)30295-3 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Subramanian I, Mathur S, Oosterbaan A, Flanagan R, Keener AM, Moro E. Unmet needs of women living with Parkinson's disease: gaps and controversies. Mov Disord. 2022;37(3):444-455. doi: 10.1002/mds.28921 [DOI] [PubMed] [Google Scholar]
- 3.Walker PL, Cook DC. Brief communication: gender and sex: vive la difference. Am J Phys Anthropol. 1998;106(2):255-259. doi: 10.1002/(SICI)1096-8644(199806)106:2<255::AID-AJPA11>3.0.CO;2-# [DOI] [PubMed] [Google Scholar]
- 4.Baldereschi M, Di Carlo A, Rocca WA, et al. Parkinson's disease and parkinsonism in a longitudinal study: two-fold higher incidence in men. ILSA Working Group. Italian longitudinal study on aging. Neurology. 2000;55(9):1358-1363. doi: 10.1212/wnl.55.9.1358 [DOI] [PubMed] [Google Scholar]
- 5.Haaxma CA, Bloem BR, Borm GF, et al. Gender differences in Parkinson's disease. J Neurol Neurosurg Psychiatry. 2007;78(8):819-824. doi: 10.1136/jnnp.2006.103788 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Miller IN, Cronin-Golomb A. Gender differences in Parkinson's disease: clinical characteristics and cognition. Mov Disord. 2010;25(16):2695-2703. doi: 10.1002/mds.23388 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Cholerton B, Johnson CO, Fish B, et al. Sex differences in progression to mild cognitive impairment and dementia in Parkinson's disease. Parkinsonism Relat Disord. 2018;50:29-36. doi: 10.1016/j.parkreldis.2018.02.007 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Tremblay C, Abbasi N, Zeighami Y, et al. Sex effects on brain structure in de novo Parkinson's disease: a multimodal neuroimaging study. Brain. 2020;143(10):3052-3066. doi: 10.1093/brain/awaa234 [DOI] [PubMed] [Google Scholar]
- 9.Turcano P, Savica R. Sex differences in movement disorders. Handb Clin Neurol. 2020;175:275-282. doi: 10.1016/B978-0-444-64123-6.00019-9 [DOI] [PubMed] [Google Scholar]
- 10.Tranchevent LC, Halder R, Glaab E. Systems level analysis of sex-dependent gene expression changes in Parkinson's disease. NPJ Parkinsons Dis. 2023;9(1):8. doi: 10.1038/s41531-023-00446-8 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Bayram E, Weigand AJ, Flatt JD. Perceived discrimination in health care for LGBTQIA+ people living with Parkinson's disease. J Gerontol B Psychol Sci Soc Sci. 2023;78(9):1459-1465. doi: 10.1093/geronb/gbad046 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Moore O, Kreitler S, Ehrenfeld M, Giladi N. Quality of life and gender identity in Parkinson's disease. J Neural Transm. 2005;112(11):1511-1522. doi: 10.1007/s00702-005-0285-5 [DOI] [PubMed] [Google Scholar]
- 13.Göttgens I, Darweesh SKL, Bloem BR, Oertelt-Prigione S. The impact of multiple gender dimensions on health-related quality of life in persons with Parkinson's disease: an exploratory study. J Neurol. 2022;269(11):5963-5972. doi: 10.1007/s00415-022-11228-2 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Dobkin RD, Amondikar N, Kopil C, et al. Innovative recruitment strategies to increase diversity of participation in Parkinson's disease research: the fox insight cohort experience. J Parkinsons Dis. 2020;10(2):665-675. doi: 10.3233/JPD-191901 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Lin CYR, Rosendale N, Deeb W. Expanding sexual and gender minority research in movement disorders: more than awareness and acceptance. Parkinsonism Relat Disord. 2021;87:162-165. doi: 10.1016/J.PARKRELDIS.2021.05.019 [DOI] [PubMed] [Google Scholar]
- 16.Patel RA, Stebbins G, Witek N. Sexual orientation and gender identity documentation at an academic movement disorders neurology clinic. Clin Park Relat Disord. 2022;7:100164. doi: 10.1016/j.prdoa.2022.100164 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Patel R, Kompoliti K. Sex and gender differences in Parkinson's disease. Neurol Clin. 2023;41(2):371-379. doi: 10.1016/j.ncl.2022.12.001 [DOI] [PubMed] [Google Scholar]
- 18.Smolensky L, Amondikar N, Crawford K, et al. Fox Insight collects online, longitudinal patient-reported outcomes and genetic data on Parkinson's disease. Sci Data. 2020;7(1):67. doi: 10.1038/s41597-020-0401-2 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Fox Insight Research Tool. Accessed March 16, 2024. foxinsight-info.michaeljfox.org/insight/explore/insight.jsp
- 20.R Core Team. R: A Language and Environment for Statistical Computing; 2022. Accessed August 10, 2023. r-project.org/ [Google Scholar]
- 21.Trinh MH, Agénor M, Austin SB, Jackson CL. Health and healthcare disparities among U.S. women and men at the intersection of sexual orientation and race/ethnicity: a nationally representative cross-sectional study. BMC Public Health. 2017;17(1):964. doi: 10.1186/s12889-017-4937-9 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Martell ME, Roncolato L. Economic vulnerability of sexual minorities: evidence from the US household pulse survey. Popul Res Policy Rev. 2023;42(2):28. doi: 10.1007/s11113-023-09778-y [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.World Economic Forum. Global Gender Gap Report 2023; 2023. Accessed January 24, 2024. weforum.org/reports/global-gender-gap-report-2023/digest [Google Scholar]
- 24.Johnson CM, Sharkey JR, Dean WR, St John JA, Castillo M. Promotoras as research partners to engage health disparity communities. J Acad Nutr Diet. 2013;113(5):638-642. doi: 10.1016/j.jand.2012.11.014 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Varma DS, Samuels E, Piatt G, et al. Community health workers and promotoras' perspectives of a research best practice course: a focus group study. J Clin Transl Sci. 2022;6(1):e137. doi: 10.1017/cts.2022.464 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Anderson A, Borfitz D, Getz K. Global public attitudes about clinical research and patient experiences with clinical trials. JAMA Netw Open. 2018;1(6):e182969. doi: 10.1001/jamanetworkopen.2018.2969 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Rigatti M, DeGurian AA, Albert SM. “Getting There”: transportation as a barrier to research participation among older adults. J Appl Gerontol. 2022;41(5):1321-1328. doi: 10.1177/07334648211072537 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Bentley JP, Thacker PG. The influence of risk and monetary payment on the research participation decision making process. J Med Ethics. 2004;30(3):293-298. doi: 10.1136/jme.2002.001594 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29.Halpern SD, Karlawish JHT, Casarett D, Berlin JA, Asch DA. Empirical assessment of whether moderate payments are undue or unjust inducements for participation in clinical trials. Arch Intern Med. 2004;164(7):801-803. doi: 10.1001/archinte.164.7.801 [DOI] [PubMed] [Google Scholar]
- 30.Adrissi J, Fleisher J. Moving the dial toward equity in Parkinson's disease clinical research: a review of current literature and future directions in diversifying PD clinical trial participation. Curr Neurol Neurosci Rep. 2022;22(8):475-483. doi: 10.1007/s11910-022-01212-8 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31.Bibbins-Domingo K, Helman A, Dzau VJ. The Imperative for diversity and inclusion in clinical trials and health research participation. JAMA. 2022;327(23):2283-2284. doi: 10.1001/jama.2022.9083 [DOI] [PubMed] [Google Scholar]
- 32.Steinberg JR, Turner BE, Weeks BT, et al. Analysis of female enrollment and participant sex by burden of disease in US clinical trials between 2000 and 2020. JAMA Netw Open. 2021;4(6):e2113749. doi: 10.1001/jamanetworkopen.2021.13749 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33.Sanchez AV, Ison JM, Hemley H, et al. Designing the fostering inclusivity in research engagement for underrepresented populations in Parkinson's disease study. Contemp Clin Trials. 2022;115:106713. doi: 10.1016/j.cct.2022.106713 [DOI] [PubMed] [Google Scholar]
- 34.Pearson C, Hartzman A, Munevar D, et al. Care access and utilization among medicare beneficiaries living with Parkinson's disease. NPJ Parkinsons Dis. 2023;9(1):108. doi: 10.1038/s41531-023-00523-y [DOI] [PMC free article] [PubMed] [Google Scholar]
- 35.Lund EM, Burgess CM. Sexual and gender minority health care disparities: barriers to care and strategies to bridge the gap. Prim Care. 2021;48(2):179-189. doi: 10.1016/j.pop.2021.02.007 [DOI] [PubMed] [Google Scholar]
- 36.Vaswani PA, Tropea TF, Dahodwala N. Overcoming barriers to Parkinson disease trial participation: increasing diversity and novel designs for recruitment and retention. Neurotherapeutics. 2020;17(4):1724-1735. doi: 10.1007/s13311-020-00960-0 [DOI] [PMC free article] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
Qualified researchers may request access to all deidentified data in the Fox Insight used for this study.19