Health‐related stigma of noncommunicable neurological disease in rural adult populations: A scoping review

Abstract Stigma is a widely recognised public health issue. Many people with neurological disease and their families experience stigmatisation, adding to their burden of illness. Rural populations are typically small, lack anonymity, and often have a higher proportion of older adults with inadequate access to specialised services and resources. Although generally isolated, rural areas can offer benefits such as a sense of familiarity and interconnectedness. The purpose of this scoping review was to map the existing evidence on stigma associated with non‐communicable neurological disease in rural adult populations and identify key findings and gaps in the literature. Our literature search of peer‐reviewed English language articles published from 1 January 1992 to 22 June 2017 was conducted across five databases yielding 8,209 results. After duplicate removal, pairs of reviewers independently screened 6,436 studies according to inclusion criteria developed a priori; 36 articles were identified for inclusion in this review. Study characteristics were described and illustrated by frequency distribution, findings were grouped thematically, and each of the five types of stigma were identified (social, self, health professional, associative, structural). Four factors influencing stigma (knowledge, familiarity, beliefs, and rurality) and four overarching stigma‐related themes (concealment; exclusion; disempowerment, discrimination, and unequal opportunities; and issues related to healthcare systems and providers) emerged. In urban‐rural comparison studies, rural residents were generally less knowledgeable about the neurological disease and more stigmatised. The impact of other factors (i.e., gender, age, and education) on stigma varied and are stated where associations were reported. Three main gaps were identified including: low attention to stigma related to neurological diseases other than epilepsy, limited cross‐cultural comparisons of stigma related to neurological disease, and inclusion of gender as a variable in the analysis of stigma‐related outcomes in only half of the reviewed studies. Further research is recommended.

Although the global population, including the older population, has been rising faster in urban areas relative to rural settings, almost half (46%) of the world's population continues to live in rural locations (UN, 2014). People living in rural areas experience unique circumstances that can present both beneficial and challenging influences on health, including health-related stigma (Gessert et al., 2015). Thus, gaining a better understanding of stigma associated with neurological disease in rural adult populations is warranted.
For this review, five types of stigma are relevant: (a) social stigma, (b) self-stigma, (c) stigma by association, (d) structural stigma, and (e) health professional stigma. According to Bos, Pryor, Reeder, and Stutterheim (2013) stigma can be viewed as taking place on three levels: societal, interpersonal, and individual. Bos et al. (2013) also offer an enhanced description of four interconnected types of stigma identified in the conceptual model of Pryor and Reeder (2011) as public stigma, self-stigma, structural stigma, and stigma by association. Social or public stigma represents the central stigma type and refers to the stigmatising responses of others towards the person who has a stigmatised condition (Bos et al., 2013).
Self-stigma refers to the perceptions and feelings of stigma that are internalised by the person with a stigmatised condition, due to their awareness and experience of social stigma towards them (Corrigan, 2004;Corrigan, Larson, & Rüsch, 2009;Crocker, 1999). Stigma by association refers to the social stigmatisation of individuals simply by virtue of being associated with a stigmatised person (Mehta & Farina, 1988;Neuberg, Smith, Hoffman, & Russell, 1994;Pryor & Reeder, 2012;Werner & Heinik, 2008). Structural stigma refers to the systemic, institutional, policy, and societal structures that fundamentally and disproportionately limit the rights and freedoms of certain groups of people, such as people who have a stigmatised condition (Corrigan, Markowitz, & Watson, 2004;Hatzenbuehler, 2016;Link & Phelan, 2001). Lastly, although the phenomenon of health professional stigma is an understudied type of stigma that could be considered part of the social stigma realm, their position and duty of care places them in a unique situation of importance (Ahmedani, 2011). The attitudes and beliefs of healthcare professionals about certain diseases and toward their patients inarguably play an important role in health-related stigma.
The study objectives were to: map the existing evidence of stigma associated with noncommunicable neurological disease in rural adult populations; identify key findings and gaps in the literature; and make recommendations for future research. The findings from this review contribute to the existing knowledge of stigma related to neurological disease from a rural-centred perspective.
What is known about this topic • Health-related stigma increases the overall burden of illness.
• The stigma of neurological disease is a widely recognised global health issue.
• People living in rural areas experience unique circumstances that warrant particular consideration.

What this paper adds
• Although rural areas have characteristics that can both reduce and increase health-related stigma, in general our findings indicated poorer stigma-related outcomes among those living rurally compared to urban.
• Key gaps in the literature, factors that influence stigma, and overarching stigma-related themes were identified.
• These findings can be used to inform future research, policy, and intervention strategies designed specifically for rural areas aimed at reducing the stigma of neurological disease and the negative consequences, thereby improving the lives of this population and their families.

| ME THODS
The protocol used to conduct this scoping review is based on the Arksey and O'Malley (2005) five-step framework which included (a) identifying the research questions, (b) identifying the relevant studies, (c) study selection, (d) data charting, and (e) collating, summarising, and reporting the results. A collaborative research team approach was used, consisting of all authors (VE, JK, AFC, MB, DM), in the iterative process of developing the research questions and search strategies, and creating the data extraction form.

| Stage 1: Identifying the research questions
The purpose of this review was to gain a better understanding of stigma related to noncommunicable neurological disease in rural adult populations and the consequences of this stigmatisation, to potentially inform and assist with future stigma reduction efforts.
We focused on three main questions. Records excluded (n = 6,298) Screening Included Eligibility (MEDLINE, PsycINFO, EMBASE, CINAHL, and SocINDEX) that pertained to both "stigma" and "rural". The intent of this comprehensive approach was to avoid placing narrower restrictions on our search, thereby prematurely limiting our pool of evidence from which to screen. Thus, a keyword search using the multipurpose (.mp) combined set of fields (title, abstract, subject or MESH headings) for all databases included the following search terms: (rural*) AND (stigma* OR attitude OR prejudice* OR stereotyp* OR discrimination or perception*). Search strategies were customised to the specific requirements of each database. The search was limited to English language studies published over a 25-year period, from 1 January 1 1992 to 22 June 2017.

| Stage 3: Study selection
The search terms yielded 8,209 results across five databases ( Figure 1). The studies were exported from the databases into EndNote (Clarivate Analytics, Philadelphia, United States) and duplicate publications removed. Studies were then exported to DistillerSR (Evidence Partners, Ottawa, Canada). After a second deduplication process, 6,436 studies remained to be assessed for inclusion regarding relevance to the research questions.
All types of research designs were considered for inclusion.
Additionally, the inclusion criteria (Table 1) required that the studies address the following: (a) the neurological disease was noncommunicable and was listed in the National Institute of Neurological Diseases and Stroke (NINDS) (Disorders, n.d.), (b) the study focus was on adults aged 18 years or over with a neurological disease, and (c) there was sufficient relevant information regarding stigma (or associated terms) related to neurological disease. Studies that did not focus on or make a comparison to rural participants were excluded.
Only published, original, peer-reviewed research articles were considered for inclusion.
Screening forms were created and piloted in DistillerSR to perform the screening processes at two levels. At the title and abstract level, two authors independently screened studies for inclusion. The first author screened all studies and three coauthors each screened one-third of all studies. Unresolved conflicts at this level were included for screening at the full-text level. Two reviewers independently screened studies for inclusion at the fulltext level (n = 138) and unresolved conflicts were resolved by the second author. Thirty-six studies were included for synthesis.

| Stage 4: Data charting
A data chart was piloted by three reviewers to extract and summarise the relevant information from each study. The first author extracted study characteristics and findings from each of the 36 studies. Data extracted included: author, year, country, objective, population, and design. Additional study information and findings extracted were: neurological disease, definition of rural, definition of stigma, stigma measure, main findings related to the stigma of neurological disease, and the type of stigma identified.

| Stage 5: Collating, summarising, and reporting the results
The extracted data for all 36 studies were collated by year of publication, country, and neurological disease, which are illustrated by frequency distribution (Figures 2, 3, and 4, respectively). Analysis of the study findings identified four major factors influencing stigma and four overarching themes. For a brief description of themes and studies itemised by theme, refer to Table 2.

| Study characteristics
Study characteristics including the publication author, year, and country, in addition to study methods, sample, and stigma measures are presented with the main stigma-related findings and stigma types in Table 3.
The 36 studies were published from 1995 to 2017, with an increase in the number of studies over time ( Figure 2). Included studies were comprised of geographical locations from across the globe (Figure 3).

TA B L E 1 Inclusion and exclusion criteria
Neurological diseases of focus in these studies were: epilepsy (n = 21), Alzheimer's disease or other dementia and (n = 7), Parkinson's disease (n = 4), traumatic brain injury (n = 2), Machado-Joseph disease (n = 1), and neurological disease in general (n = 1) ( Figure 4). The majority of studies focused on stigma related to epilepsy (21/36), almost half of which were conducted within the continent of Africa (10/21).
Of the 36 studies, there were 20 quantitative, 10 qualitative, and six mixed methods. Most of the studies specified the involvement of both males and females in their sample (31/36) and of these, 19 considered sex in their analyses regarding stigma-related outcomes. Ten of these found no significant differences in stigma-related outcomes for males versus females; however, one of these (Rafael et al., 2010) reported that significantly more males never married compared to females. Of the nine studies that found significant differences, most (7) reported better stigma-related outcomes for males compared to females.
The majority of included studies (24/36) provided no definition of rural; instead the authors simply stated or implied the area and/or sample under study was rural. Standardised definitions were used in 7/36 studies, such as census data or other government statistics and maps, or national agency resources. Four of the 36 studies stated that the location and/or sample was rural and provided population size, often with the relative distance from an urban centre.
Over half of the studies were rural-focused (20/36); 16/36 included urban participants, 15 of which provided at least some ruralurban comparisons and one in which rural and urban data were not reported separately. Most of these comparative studies reported rural-urban differences in stigma-related findings (13/15). The findings of the 15 studies that included rural-urban comparisons are reported briefly within each section of the findings, and then summarised at the end of the Findings section.

| Rurality
Rural was also identified as a factor influencing stigma. All five types of stigma were identified within the six studies that remarked on the interconnectedness among people living in rural areas, which reportedly had mixed effects on stigma. Morgan, Semchuk, Stewart, and D'Arcy (2002) and Forbes, Ward-Griffin, and Kloseck (2011) explored the experiences of rural families caring for people with dementia. Forbes et al. (2011) found that rural living offered a close-knit, supportive community that could reduce stigma. However, Forbes et al.
(2011) and Morgan et al. (2002) reported that a lack of privacy experienced by rural dwellers sometimes led to increased stigma. Of the 15 studies that explored differences in stigma-related outcomes between rural and urban participants, only three reported more positive findings for rural than urban (Burgener et al, 2015;Farmer, Clark, & Sherman, 2003;Youssef et al., 2009) and one that reported both better and worse stigma-related findings among rural compared to urban (Yang et al., 2011).
Most of the 11 studies focussed solely on rural populations (8).
In general, these studies reported similar findings of attempts to hide the neurological disease. Of these, two studies found an association between attempts to conceal and the more physical nature of the disease. Guo et al. (2012), who interviewed rural adults in China, found that concealment of epilepsy was associated with not only experiencing physical manifestations of the disease, but also with the belief that epilepsy is hereditary. This finding is similar to that of Morgan et al (2002) who conducted focus groups in their Canadian study with rural caregivers of people with dementia.
They found stigmatic effects of shame and embarrassment associated with the disease, specifically in terms of social behavioural issues, that resulted in concealment and was identified as a potential barrier to care-seeking. San-Juan et al. (2015) however, found that even though almost all adults with epilepsy (94%) who participated in their study in rural Mexico reported having experienced epilepsy-related discrimination, only 24% reported attempts to conceal the disease.
Three of the 11 studies reporting concealment associated with stigma provided urban-rural comparisons, with mixed results (Burgener et al., 2015;Tiamkao, Sawanyawisuth, Singhpoo, Ariyanuchitkul, & Ngamroop, 2013;Yang et al., 2011). For example, Burgener et al. (2015) conducted a longitudinal study to assess stigma among people with Alzheimer's disease or other dementia and found lower levels of internalised shame at baseline among rural participants compared to urban, in addition to rural participants (men in particular) being more accepting of disease concealment than urban. Tiamkao et al. (2013) found more concealment of epilepsy among rural participants in Thailand (who were also less educated, earned a lower income, older, and more likely married) versus urban participants.
Most (  • 365 rural adults without epilepsy Gender: • 235 male, 130 female Age: • 18-74 years (mean age 42 years) • No direct measure of stigma but assesses related aspects including familiarity, knowledge, and beliefs • High familiarity but low accurate knowledge • Cultural influence on inaccurate knowledge (e.g., "demonic possession") associated with more stigmatization • Social exclusion; associated with false beliefs (e.g., "contagious") • Infectious belief associated with increased stigma • Females (especially over age 30 years) were more knowledgeable about epilepsy than men • Social • Self Bain et al. (2013), Republic of Cameroon Methodology: Quantitative • Cross-sectional survey Sample: • 505 rural community members Gender: • 273 male, 232 female Age: • 18 years and older • No direct measure of stigma but assesses related aspects including familiarity, knowledge, beliefs, and practices • High familiarity with epilepsy • Stigmatization positively associated with being older, being female, being less educated and less knowledgeable about epilepsy • Cultural influence on inaccurate knowledge (e.g., "witchcraft") associated with more stigmatization • Social exclusion; associated with false beliefs (e.g., "contagious"; "madness" • Inaccurate knowledge positively associated with discrimination and reduced life opportunities • 100 rural adults diagnosed with and receiving treatment for epilepsy (questionnaire) and 20 rural health workers (focus groups) Gender: • 40 male, 60 female Age: • 22-65 years (mean age 37.7 years) • No direct measure of stigma but qualitatively and quantitatively assesses related aspects including beliefs, perceptions, knowledge • High inaccurate knowledge and beliefs (e.g., "contagious"), positively associated with more stigma • Cultural influence on inaccurate knowledge (e.g., "punishment for sins") associated with more stigmatization and traditional care-seeking • Social exclusion; associated with false beliefs (e.g., "contagious"; "madness") • Reduced life opportunities • 93 adults working in "public positions and the institutional sphere" (47 urban, 46 rural) Gender: • 31 male (20 rural), 62 female (29 rural) Age: • ≥45 (n = 32), 35-45 (n = 25), <35 (n = 36) • No direct measure of stigma but qualitatively assesses related aspects including knowledge, attitudes, and beliefs Rural/Urban differences • Rural had more negative attitudes than urban and were more likely than urban to perceive epilepsy as "frightening" • Rural (and men) more accepting of disease concealment vs. urban • Rural were more concerned than urban about marriage prospects (especially for younger people with epilepsy) • Rural respondents were more concerned with feasibility of treatment (costs for epilepsy treatment vs. that of other serious diseases) • Rural respondents were more concerned with psychosocial issues for people with epilepsy versus other serious diseases Across both rural and urban: • Social exclusion • Concealment • Reduced life opportunities • Overall, more positive attitudes by those with medical background • Many health professionals reported that people with epilepsy have an "epileptic character" with negative changes in personality and behaviour and reported the disease as "worse than other serious diseases"; concern with stigmatization • Fewer men than women reported belief of epilepsy as worse relative to other diseases and focused more on physical health issues; women were more focused on the uncontrollability, unpredictability, stigma, and burden of care on others • Fewer women than men reported belief of epilepsy as better than other diseases In general, nonmunicipal people (Rural) in this study were older, had more married persons, and lower levels of education and income, than municipal people (Urban) • More rural cultural influence on inaccurate knowledge (e.g., "spiritual possession," "hereditary") associated with more stigmatization Note. Verbatim information marked within quotations.

TA B L E 3 (Continued)
Three rural-focused studies (two regarding Alzheimer's disease or other dementia and one epilepsy), reported a positive association between social exclusion and the physical and/or behavioural manifestations of the neurological disease (Forbes et al., 2011;Morgan et al., 2002;von Gaudecker, Taylor, Keeling, Buelow, & Benjamin, 2017). Klepac et al. (2007) reported similar findings among individuals with Parkinson's disease where higher levels of social support were strongly associated with having low nonmotor symptoms scores. Similarly, Guo et al. (2012) found that among people with epilepsy, the physical nature of the disease was associated with increased stigma in general and that self-stigma (reportedly tied to self-exclusionary practices) was associated with low education and reduced care-seeking.
Of the eight urban-rural studies that reported social exclusion, three reported urban-rural differences (Burgener et al., 2015;Farmer et al., 2003;Tiamkao et al., 2013). For example, regarding epilepsy, Tiamkao et al (2013) found a positive association between social exclusion and being rural, whereas Farmer et al. (2003) found that experiences of social exclusion were similar across urban, subrural, and rural adults with traumatic brain injury.

| Disempowerment, discrimination, unequal life opportunities
Twenty-one studies reported stigma-related outcomes regarding disempowerment, discrimination, and/or unequal life opportunities.
Over half of the studies (11/21) that reported findings of disempowerment, discrimination, and/or unequal life chances focused on rural populations, most of which (8) were regarding epilepsy. For example, Guo et al. (2012) found most people with epilepsy had been discriminated against, even by distant family members. Employer discrimination was present, most of whom admitted that they would not hire a person with epilepsy Guo et al. (2012). McQueen and Swartz (1995) found similar outcomes among respondents who experienced dependency on others and had difficulty finding employment, other than jobs specifically designed for people with limited capabilities. Bain et al. (2013) reported that most community members surveyed admitted that they would not give equal employment opportunities to people with epilepsy, nor would they allow their children to associate with or marry a person with epilepsy. Bain et al (2013) also noted an association between discrimination and unequal life opportunities with inaccurate knowledge about the disease (Bain et al., 2013). Neni et al. (2010) found that almost half of the participants surveyed reported that people with epilepsy should not participate in sports, driving, or marriage. Rafael et al. (2010) reported similar findings which included dependency on others and difficulty getting married. Difficulties getting married were experienced more among men than women, and more men than women with epilepsy were unmarried and more men than women expressed poorer chances of getting married (Rafael et al., 2010).
Findings of disempowerment, discrimination, and unequal life opportunities were also reported in studies focusing on neurological diseases other than epilepsy among in rural-focused studies (3/11).
For example, Forbes et al. (2011) found disempowerment and discrimination among people with dementia (and often their families) who were treated differently, lacked involvement in decision-making about their care, and felt limited in terms of choices and control. Mshana et al. (2011) found similar results among adults with Parkinson's disease in rural Tanzania, as did Paúl et al. (1999) Birbeck et al. (2006) found that rural participants were less tolerant than urban participants, and intolerance across urban-rural was associated with being younger and less educated. Other studies involving urban-rural comparisons among people with traumatic brain injury, dementia, or Parkinson's disease (3/7) reported intolerance, discrimination and unequal life opportunities. In addition to living rurally, Kartal and Akyildiz (2016) reported that across urban and rural participants, predictors of negative attitudes included being female and less educated.

| Healthcare systems, services, and providers
Nine studies reported stigma-related outcomes regarding healthcare systems, services, and/or providers. Two subthemes (availability and accessibility, and healthcare provider competencies and values) were identified. Within these nine studies, all five types of stigma were present: social (8), self (7), structural (7), associative (4)

Availability and accessibility
Eight studies reported stigma-related outcomes regarding access and availability (rural: n = 4; rural-urban: n = 4). Hsiao et al (2015) noted existing structural stigma in the lack of systems, specialised teams, policies, or plans regarding government, and hospital management for dementia. Cahill et al. (2008) conducted a cross-sectional study of urban and rural general practitioners in Ireland, followed by focus groups with the rural practitioners. Stigma was identified as a key factor in delayed diagnoses, where rural general practitioners felt disadvantaged in terms accessing diagnostic services due to geographic location.
Several studies reported reduced care-seeking and/or service use associated with a lack of available, timely access to affordable healthcare, services, and treatment (Birbeck & Munsat, 2002;Guo et al., 2012;McQueen & Swartz, 1995;Mshana et al., 2011;Paúl et al., 1999). Mshana et al. (2011) reported an additional association between delayed diagnoses and lack of medicalised treatment with increased use of traditional healers due to the belief their illness was due to a curse or witchcraft. The use of traditional healers was also increased due to a lack of locally available Parkinson's disease drugs and the associated costs, even if an individual did obtain a medical diagnosis. Only 2/28 individuals with Parkinson's disease were receiving westernised treatment, both of whom reported the drugs gave them enough relief to lead normal lives, when they could afford to buy them (Mshana et al., 2011). Stansbury, Marshall, Harley, and Nelson (2010) explored the attitudes towards and knowledge about Alzheimer's disease among rural clergymen in the United States, whose congregation often opted to seek their advice for health-related issues.
Clergymen acknowledged that in spite of being able to offer advice on other health issues, they were largely uninformed about Alzheimer's disease-related healthcare services and referral pro- cesses and yet were looked to be responsible for advising their members with the disease.

Healthcare provider competencies and values
Three studies reported findings regarding the capabilities and willingness of healthcare providers to provide adequate care, one regarding neurological diseases in general where urban-rural data were not reported separately (Birbeck et al., 2002) and two regarding dementia (Cahill et al., 2008;Hsiao et al., 2015). All three studies were conducted among urban and rural populations. In general, a lack of sufficient time, experience, training, education, and confidence among primary healthcare professionals to diagnose and treat neurological diseases were reported (Birbeck et al., 2002;Cahill et al, 2008;Hsiao et al., 2015). For both urban and rural populations, this often resulted in delayed diagnoses or under-diagnosis, where rural residents were underdiagnosed more frequently than urban (Cahill et al., 2008;Hsiao et al., 2015).
Other underlying reasons for delayed diagnosis or underdiagnoses attributed to healthcare professions in rural areas included: long-term familiarity with patients as a potential barrier to noticing minor dementia-related changes over time until more obvious changes occur, scepticism of benefits to early diagnosis, and avoidance of labelling a person with dementia until a time of crisis or approached by the family (Cahill et al., 2008). Hsiao et al. (2015) also reported that relative to urban, rural health providers often perceived dementia-related cognitive issues as lower priority than physical issues of other diseases. Moreover, rural providers were less empathetic, expressed greater difficulty communicating with patients and families about diagnosis, and offered more life and culture-focused advice for dementia treatment and management.

| Summary of rural-urban differences in stigma-related outcomes.
Sixteen studies examined both rural and urban individuals including one in which rural/urban data were not reported separately (Birbeck et al., 2002), one with no findings of stigma-related differences between rural and urban participants (Cahill et al., 2008), and 14 that reported rural-urban differences in stigma-related outcomes. Of those 14, one study reported both a worse and a better stigma-related outcome for rural compared to urban participants (Yang et al., 2011), and only three studies reported some better stigma-related outcomes for rural versus urban participants (Burgener et al., 2015;Farmer et al., 2003;Youssef et al., 2009). Overall, 12/14 reported not only worse, but also more stigma-related outcomes for rural versus urban. Seven (7/12) of the studies that reported poorer stigma-related findings for rural participants versus urban focussed on epilepsy.
Compared to urban, rural was generally: less tolerant (Atadzhano et al., 2006;Birbeck et al., 2006); less familiar and less knowledgeable Kartal & Akyildiz, 2016); more concerned with marriage prospects (especially younger adults), feasibility of treatment, and psychosocial issues (Yang et al., 2011); more negative in terms of attitudes (Kartal & Akyildiz, 2016;Yang et al, 2011); more likely to be influenced by cultural beliefs, more likely to conceal, be socially excluded, and discriminated against (Tiamkao et al., 2013); and more likely to experience a reduction in life opportunities (Deresse et al., 2016;Kartal & Akyildiz, 2016;Tiamkao et al., 2013). Tegegne and Awoke (2016) found that rural people with epilepsy were twice as likely to experience stigma in general compared to urban.
Only 2/8 epilepsy studies that reported urban-rural differences found stigma-related outcomes that were better for rural participants relative to urban. Youssef et al (2009) found that rural people experienced less stigmatisation in general than their subrural and urban counterparts. In addition to the poorer stigma-related outcomes for rural versus urban participants noted above, Yang et al. (2011) also found that rural participants (men in particular) were more accepting of disease concealment versus their urban counterparts.
Of the studies that involved rural and urban participants focusing on other neurological diseases (n = 8), one did not report rural-urban data separately (Birbeck et al., 2002), and one found no differences (Cahill et al., 2008). Four (n = 3 Parkinson's disease; n = 1 dementia) found worse stigma-related outcomes for rural participants versus urban. Rural individuals, especially females, with Parkinson's disease reported poorer quality of life, poorer emotional well-being, and greater bodily discomfort (Klepac et al., 2007;Wu et al., 2014) and rural adults in general were less knowledgeable about the disease (Kaddumukasa, 2015). Regarding dementia, Hsiao et al. (2015) found a range of stigma-related issues among rural versus urban general practitioners in China. Specifically, rural practitioners were less experienced, knowledgeable, and empathic, more concerned with physical than cognitive issues, and reported more difficulty and frustration communicating with patients and families.
Two (2/8) nonepilepsy studies reported better stigma-related outcomes among rural than urban participants. Farmer et al. (2003) found that urban participants had more negative attitudes and beliefs towards adults living with traumatic brain injury and living rurally was significantly associated with a better quality of life and seeking social support. Burgener et al. (2015) found that rural participants with Alzheimer's disease or other dementia, and their informal caregivers, had less "internalised shame" at baseline. Across both rural and urban, the authors reported a decline in overall stigma after 18 months and an inverse association between overall stigma and age. Of the 16 studies included in this scoping review that included both rural and urban populations in their studies, one study did not explore urban-rural differences in stigma-related outcomes and one study found no differences. Of the other 14 urban-rural studies, three reported better stigma-related outcomes for rural participants compared to urban and 11 reported worse stigma-related outcomes for rural participants versus urban. However, although one of these studies (1/11) reported primarily worse stigma-related outcomes for rural versus urban participants, the authors also reported that rural participants were more accepting of concealment compared to urban participants. While this finding could be interpreted as a positive outcome for rural versus urban, it is possible that it could indicate increased stigma for this population where concealment reflects a need or expectation to do so. Overall, inaccurate knowledge was highly influenced by cultural beliefs and rural populations were, in general, less familiar with and less knowledgeable about the neurological disease and individuals with neurological conditions experienced more stigmatisation than their urban counterparts.

| D ISCUSS I ON
While an influence of culture per se was not mentioned, the rural-urban study of Farmer et al. (2003) and two rural-focused studies of Morgan et al. (2002) and Forbes et al. (2011) reported that the supportive social networks of rural societies could reduce stigma, while the latter two authors also referred to a lack of privacy in rural settings that could increase stigma. Morgan et al. (2002)  Some studies in our review found a positive association between the visible, physical nature of the neurological disease and the degree of stigmatisation. Scambler (1998) refers to illnesses with highly visible, obtrusive symptoms as being highly stigmatised. This is well-supported within the literature across various types of diseases, along with the implications of forced or unintentional disease disclosure including psychological distress and reduced care-seeking, for both the person with the disease and their families (Brener, Callander, Slavin, & de Wit, 2013;Maffoni, Giardini, Pierobon, Ferrazzoli, & Frazzitta, 2017;Phelan, Bromet, & Link, 1998;Scholl & Sabat, 2008;Stutterheim et al., 2012).
In addition to the association between concealment and the visibility of the neurological disease symptoms, concealment was associated with the stigma attached to what people believed to be the etiology of the disease. For example, neurological diseases were more stigmatised (resulting in more attempts to conceal) if they were thought to be hereditary, contagious, evidence of madness, or divine punishment. Attempts to conceal were often related to exclusionary practices, which were also often associated with misbeliefs about causality and the visibility of disease symptoms. Furthermore, concealment was associated with a reduction in care-seeking and inadequate treatment and disease management. The effects of health-related stigma on concealment has been supported in the literature, where even anticipated stigma increases attempts to conceal the disease. For example, Cook, Germano, and Stadler (2016) explored the association between stigma and concealment among a group of American adults with multiple sclerosis and found that anticipatory stigma was a strong predictor of concealment and that data trends indicated concealment was associated with delays in doctor visits and treatment therapy (Cook et al., 2016).
Findings of concealment and exclusionary practices in our review were also related to findings of disempowerment, discrimination, and unequal life opportunities. In general, findings included dependency on others for care and financial management, a lack of being involved in decision-making about care, discrimination in terms of employability, marriageability, capacity to drive, and participate in sports. Marriage discrimination was reported in one epilepsy study as worse for males than females, however, no conclusions were drawn as to why (Rafael et al., 2010). Previous research supports these stigmatic effects of epilepsy in terms marriageability; however, the differential impacts for males versus females in general were mixed. Mixed findings could be influenced by culture, which appeared to play a role, especially in contexts of arranged marriages. A review of the literature on arranged marriage prospects among people with epilepsy in India found that females were impacted more negatively than males (Singh et al., 2016). According to the World Health Organization (2018), both China and India currently permit epilepsy as a valid reason to deny marriage. Perhaps people with epilepsy or other neurological disease are perceived as less employable and more likely to produce children with similar diseases.
In rural-urban comparison studies included in this review, rural populations in general reported either similar or more intolerance, discrimination, and unequal life chances relative to their urban counterparts. Yang et al. (2011) found that women more frequently than men reported that stigma of epilepsy was worse than stigma of other chronic diseases. However, compared to urban participants, rural residents were more negative towards epilepsy in general, more concerned about marriage prospects (especially younger participants), and more accepting of concealment (especially males) (Yang et al., 2011).
Differences in measures used to assess stigma existed across the studies included in our review. Future quantitative research to examine stigma associated with neurological disease might utilise a standardised measure such as the Stigma Scale for Chronic Illness (SSCI) developed by Rao et al. (2009). The SSCI is a nonillness-specific stigma measure developed as part of a study regarding health-related quality of life for people with neurological disorders.
Consistent use of a validated measure in future research of healthrelated stigma of neurological disease in rural (and urban) populations would allow for more accurate comparisons of differences on various levels. However, it is noteworthy that such a scale may not account for differences in particular contexts and across cultures.
Cultural context clearly plays a role in stigma and most likely "methods of cultural epidemiology" (Weiss, Jadhav, Raguram, Vounatsou, & Littlewood, 2001, p.72) are required, with locale-specific approaches that may be effective.
In addition, although most of the studies included in this review explicitly stated the number of males and females included in samples, gender was often not included as a variable in analysis of stigma-related outcomes. Approximately half of the studies that considered sex in the analysis of stigma-related outcomes found no differences; however, most of the studies that found differences were regarding epilepsy and were generally less favourable for females compared to males. Including gender-based analysis in future research is important to explore potential differences in the ways in which stigma is experienced, and in the ways in which stigmatisation occurs, to develop and implement the most effective stigma-reducing strategies.
In general, across all neurological diseases, stigmatising processes were involved in outcomes of discrimination, isolation, disempowerment, reduced care-seeking, late diagnosis, and poor disease man- The following limitations of this scoping review warrant comment.
The search strategy was limited to studies published in English language only, from 1992 forward, which could limit the generalisability of the findings. Also, grey literature (i.e., unpublished or nonpeer reviewed; see itemised list within Table 1) was not included, which could introduce potential for publication bias. Furthermore, as this is a scoping review and not a systematic review, the authors opted not to conduct a critical appraisal of study quality. Lastly, the authors did not attempt to address cross-cultural comparative differences in the literature, which is a limitation of this review.

| CON CLUS ION
This scoping review highlights both important gaps in the existing literature, and recommendations for future research regarding stigma related to noncommunicable neurological diseases in rural areas.
Three main gaps identified were limited attention to stigma related to neurological diseases other than epilepsy, few cross-cultural comparisons of stigma related to neurological disease, and the inclusion of gender as a variable in the analysis of stigma-related outcomes in only half of the reviewed studies. In addition, several key themes associated with stigma and stigma-related concepts were identified.
The body of evidence synthesised in this review contributes to the knowledge available to policy makers, program planners, healthcare providers, and researchers. This knowledge can be used to inform future research and for the development of relevant, effective policy and intervention strategies designed specifically for rural areas, such as public awareness campaigns, to address the key issues and contributing factors that exist for this population. The overall goal of developing such strategies is to improve the lives of rural adults living with neurological disease and their families by reducing health-related stigma and its negative consequences including exclusionary practices, reduced care-seeking and service use, late diagnoses, and nonadherence to disease management and treatment strategies.