Abstract
Parkinson’s disease can adversely affect visual function, which may limit engagement and participation in everyday activities. Evaluating visual function in people with Parkinson’s disease is recommended, and occupational therapists could play a key role in screening and providing patient education.
Parkinson’s disease (PD) is the second most common neurodegenerative disorder, after Alzheimer’s disease (Dorsey et al., 2007). It is estimated that approximately 1,238,000 people will be living with PD in the United States by 2030 (Marras et al., 2018). The projected PD-associated economic burden is expected to surpass $79 billion by 2037 (Yang et al., 2020). The disease affects the basal ganglia, leading to both motor and nonmotor impairments. This includes bradykinesia, rigidity, tremor, depression, changes in cognition, sleep disorders, and visual dysfunction resulting in activity limitations and decreased quality of life (Bloem et al., 2021; Chaudhuri et al., 2011; Hermanowicz et al., 2019; Kuhlman et al., 2019; Radder et al., 2017; Schapira et al., 2017). Efforts to understand and reduce the effects of these motor and nonmotor symptoms on activity engagement and participation are critical for improving quality of life and alleviating economic burden.
Although motor symptoms have long been the clinical focus in diagnosing and treating PD, the nonmotor symptoms have received growing attention in research (Hermanowicz et al., 2019; Rodriguez- Blazquez et al., 2021; Schapira et al., 2017). Visual dysfunction is one of the nonmotor symptoms that can occur with PD (Borm, Werkmann, et al., 2019; Hamedani et al., 2020; Weil et al., 2016). In general, visual impairments are related to an increased risk of falls and decreased independence (Haymes et al., 2002; Reed-Jones et al., 2013). A general awareness of the effect that PD may have on vision could potentially help persons with PD (PwP) in recognizing such symptomology, conveying concerns to their health care team and, in turn, addressing the symptomology or even intervening to optimize safety and independence.
Visual dysfunction in PwP ranges from dry eyes, blurriness, and double vision to deficits in contrast sensitivity, visual perception, smooth pursuits, and abnormal saccades (Armstrong, 2017; Rodnitzky, 2013; Weil et al., 2016). According to Warren’s model of the hierarchy of visual–perceptual skill development, foundational features of visual function, such as visual acuity and oculomotor control, integrate with more advanced visual–perceptual skills, such as pattern recognition and visual memory (Warren, 1993a, 1993b). Visual dysfunction experienced by PwP can occur at any level of the hierarchy in Warren’s model.
Although visual dysfunction in addition to motor symptoms could exacerbate limitations in activity and participation, studies examining such correlations are sparse. The most recent comprehensive study that describes the effect that visual dysfunction could have on activities of daily living was conducted with 848 PwP in the Netherlands and Austria (Borm et al., 2020). The study reported that 82% of PwP experience one or more ophthalmologic symptoms, compared with 48% of healthy adults. Sixty-eight percent of PwP, compared with 35% of people without PD, reported difficulty with daily activities because of ophthalmologic symptoms (using “yes” and “no” responses). Findings of this study suggest that the prevalence of visual dysfunction in PwP is high. Visual dysfunction could aggravate disability in activities of daily living for this population. However, motor symptoms may overshadow visual dysfunction during health care encounters. In addition, PwP and health care providers may not be aware of the ways in which PD can affect visual functioning. This may be critically important, particularly given the wide use of visual cueing to improve motor performance, such as gait and balance, in PwP (Muthukrishnan et al., 2019).
PwP may differentially benefit from visual cueing as a motor rehabilitation approach on the basis of whether their vision is impaired and the degree to which it is impaired. Recognizing and managing visual dysfunction in PwP could be critical in the rehabilitation process. Therefore, the purposes of this study in PwP are to describe self-reported visual dysfunction, investigate the awareness of disease-related visual dysfunction, and identify the association between visual dysfunction and occupational performance.
Method
Research Design
We used a cross-sectional survey research design. The study received expedited approval from the University of Florida Institutional Review Board. Informed consent was implied with online survey completion and submission.
Participant Recruitment
The Center for Movement Disorders and Neurorestoration INFORM database at the University of Florida Health’s Norman Fixel Institute for Neurological Diseases was accessed to send out survey invitation emails. Patients registered in this single-center database had previously been examined by a movement disorder specialist, had been diagnosed with PD, and consented to be contacted for research purposes. The survey was electronically distributed to these patients by email and made available online in the Institute newsletter. Family members were allowed to help patients complete the survey.
Data Collection
Study data were collected and managed anonymously using Research Electronic Data Capture (REDCap) tools hosted at the University of Florida (Harris et al., 2009, 2019). REDCap is a secure, web-based software platform designed to support data capture for research. Completion of the survey took approximately 40 min.
Survey
The survey contained items to collect information on demographics, self-reported visual difficulties and diagnosed eye conditions (i.e., cataracts, glaucoma, age-related macular degeneration, retinosa pigmentosa, diabetic retinopathy, hypertensive retinopathy, other), and general awareness about whether PD could affect visual functions. Specifically, general awareness was assessed with the question, “Did you know that Parkinson’s disease can affect vision?” The survey also contained items from the Visual Impairment Parkinson’s disease Questionnaire (VIPD–Q) and the Revised Self-Reported Functional Visual Performance Scale (R–SRAFVP).
The VIPD–Q was developed by a group of neurologists and ophthalmologists to identify ophthalmologic symptoms experienced by PwP and healthy older adults. The questionnaire includes 22 items with established face validity (McDowell & Harris, 1997). Items are related to the effect of ophthalmologic symptoms on daily activities; for example, “I have blurry vision when I read or work on a computer.” Response options are referenced throughout the article as frequency, or how often the symptoms occurred: On a 4-point Likert scale, responses were 0 = never, 1 = one to two times per month, 2 = every week, and 3 = daily. The sum of the Likert scores for the scale’s 22 items was used in the analysis. A higher sum score indicates a higher frequency of ophthalmologic symptoms experienced. Seventeen items were further selected and categorized on the basis of the ocular structures to indicate four domains of ophthalmologic disorder: ocular surface (four items), intraocular (four items), oculomotor (four items), and optic nerve (five items). These domains are based on the consensus of three independent ophthalmologists who were asked to group questions of the VIPD–Q according to the anatomical location of a visual disorder (Borm, Werkmann, et al., 2019) and are further discussed in Borm, Smilowska, et al. (2019).
The R–SRAFVP was developed to assess the ability of older adults with age-related eye disease to complete vision-dependent activities of daily living (Snow et al., 2018). The instrument’s reliability and validity previously were established by Snow et al. (2018). Thirty-three items assessed the ability to perform health management, personal grooming, meal preparation, clothing care, financial management, using the telephone, reading, writing, functional mobility, and other personal tasks. The response options included unable, great difficulty, moderate difficulty, minimal difficulty, and independence on a 5-point Likert scale ranging from 0 to 4, respectively. Activities that were applicable to the respondents were scored. The total score was converted to a reverse score to determine a percentage of disability. A higher percentage score indicates a higher level of dependency.
Data Analysis
IBM SPSS Statistics (Version 27) was used for data analysis. We summarized the data using descriptive statistics (range, mean, count, and range) for the demographic information and characteristics of the patients. The descriptive statistics were also used to describe survey respondents’ visual dysfunction. To investigate the awareness of disease-related visual dysfunction, we conducted two tests. First, the Mann–Whitney U test was conducted to examine whether respondents with a longer duration of PD would have more awareness. Second, we conducted Fisher’s exact test to examine whether respondents with an awareness would tend to report having trouble with vision. To examine the association between visual dysfunction (i.e., VIPD–Q) and occupational performance (i.e., R–SRAFVP), we used Spearman’s ρ correlational analysis. Nonparametric statistical tests were conducted because the data did not meet the requirements for normal distribution. The significance level was set to .05. Post hoc analyses were conducted to examine whether age or history of PD was associated with the ophthalmologic symptoms reported in the VIPD–Q.
Results
A total of 108 respondents with a diagnosis of PD completed the survey between May 19, 2021, and August 26, 2021. The electronic survey was closed after no additional responses were received for 4 consecutive weeks. Sixteen respondents were excluded from data analysis because they had other neurological conditions. Table 1 shows the demographic information and characteristics of the included 92 respondents. The respondents’ age ranged from 47 to 84 yr (M = 69.15, SD = 7.68). The duration of PD ranged from 1 to 36 yr (M = 7.70, SD = 6.13). There was no correlation between age and duration of the disease, Spearman’s ρ = −.06, p = .56. There were more male (n = 54) than female (n = 38) respondents. The majority of patients were White. The percentage of respondents with a history of deep brain stimulation surgery was 19.56%.
Patient Demographics and Personal Characteristics
Note. N = 92.
aTwo nonresponses.
bOne nonresponse.
Visual Dysfunction
Visual Dysfunction and General Awareness
More than half of the respondents reported having trouble with their eyes or vision and having been diagnosed with one or more eye conditions. The most frequently reported eye condition was cataracts. However, only half of the respondents had active cataracts (19/41), whereas the other half of the respondents with cataracts reported undergoing surgical correction (22/41). Last, 49 respondents (53.3%) reported that they were aware that PD could affect their vision. There was no difference in the duration of disease between respondents who had an awareness that PD could affect vision and those who did not (U = 902, p = .23). Respondents who were aware that PD could affect visual function tended to report having trouble with vision more than those who were unaware (Fisher’s exact test, p < .05).
Self-Reported Visual Dysfunction
Three respondents did not complete the VIPD–Q. The average VIPD–Q score was 12.76 (SD = 11.48), indicating a low frequency of ophthalmologic symptoms among the respondents. Six respondents did not have any symptoms. A post hoc analysis shows that respondents who lived with a longer history with PD tended to report more symptoms on the basis of the VIPD–Q, Spearman’s ρ = 0.28, p < .05. However, age was not correlated with the VIPD–Q, Spearman’s ρ = 0.09, p = .41. Table 2 shows the prevalence of the four ophthalmologic disorders on the basis of the 17 VIPD–Q items. Symptoms related to ocular surface disorder appeared to be more common than those related to intraocular and oculomotor disorders. Symptoms related to optic nerve disorder were the least common.
Prevalence of Ophthalmologic Symptoms on the Basis of the Visual Impairment in Parkinson’s Disease Questionnaire
aThe count was based on respondents who reported experiencing the symptoms every week or daily (n = 89).
bThe count was based on respondents who reported experiencing the symptoms one to two times per month or more.
Occupational Performance
The majority of respondents reported mild difficulty in performing activities on the R–SRAFVP (M = 85.31, SD = 24.99). Although 25 respondents reported total independence as indicated by the R–SRAFVP, 6 reported 100% dependency. Figure 1 shows a scatterplot of VIPD–Q versus R–SRAFVP scores. Respondents with a higher score on the VIPD–Q tended to have a higher score on the R–SRAFVP, Spearman’s ρ = .49, p < .01. In other words, a higher frequency of ophthalmologic symptoms was positively associated with a higher degree of dependency or difficulty in activities of daily living.
Scatterplot of findings on the Visual Impairment Parkinson’s Disease Questionnaire and the Revised Self-Reported Functional Visual Performance Scale.
Discussion
Findings from this descriptive study demonstrate that nearly half of PwP have a diagnosed eye condition. The ophthalmologic symptoms they experienced could also be related to PD versus age-related eye conditions, because the history of PD, rather than age, is positively associated with self-reported ophthalmologic symptoms. Additionally, PwP who were aware that their PD could affect visual functioning tended to report having trouble with vision relative to those who were not aware. Of these ophthalmologic symptoms reported, most appear related to ocular surface disorder, followed by intraocular or oculomotor disorders, and, last, optic nerve disorder. The more frequent these ophthalmologic symptoms are, the greater the disability on vision-dependent activities of daily living. This study’s assessment of performance in activities of daily living expands our understanding of the implications of visual dysfunction in PwP.
General Awareness of Disease-Related Visual Dysfunction
To the best of our knowledge, this is the first study to assess the prevalence of general awareness in PwP that PD can affect visual function. In PwP, this awareness is critical, given the spectrum of motor and nonmotor symptoms that can occur (Hermanowicz et al., 2019; Rodriguez-Blazquez et al., 2021; Schapira et al., 2017) and the use of visual cueing to address disease-related motor impairments in rehabilitation (Bryant et al., 2010; Nieuwboer et al., 2007; Nonnekes et al., 2015). Such awareness can help PwP adequately convey their symptomology to their health care providers, address the dysfunction when possible, and optimize functional outcomes and independence. This study indicated that nearly 50% of the respondents were unaware that PD could affect their vision and visual functioning. There was no difference in the duration of disease between respondents who had an awareness versus those who did not. Possibly, the PwP without awareness either did not yet have any visual related difficulties or attributed these difficulties to aging. Alternatively, PwP who were aware and experienced visual difficulties unexplained by ophthalmologic examination may have sought the underlying explanation.
Visual Dysfunction in Persons With Parkinson’s Disease
In the general population, there is an increased incidence of ocular disease and/or difficulty with vision associated with increasing age (Centers for Disease Control and Prevention, n.d.). Similarly, respondents in this study who reported having a diagnosed eye condition were older. However, PD can occur before late adulthood (Willis, 2013). Our post hoc analysis results show that the ophthalmologic symptoms were not age associated but disease associated. These findings attempt to rule out confounding factors by demonstrating that the visual dysfunction in PwP can occur early in the disease progression and may be related to the disease process in addition to aging. Although age may underlie some of the visual changes that occur in PwP, PD may accelerate or exacerbate visual dysfunction. Previous literature describes changes ranging from the retina to the higher cortical brain regions in the visual network in PwP (Weil et al., 2016). Specifically, depletion of dopamine at the level of the retina, as well as dopaminergic innervation of the visual cortex, has been linked to the various visual disorders in PwP (Archibald et al., 2009).
Our results in the prevalence of ophthalmologic symptoms revealed trends similar to those reported by Borm et al. (2020). Symptoms related to ocular surface disorders were most common, while symptoms related to optic nerve disorder were least common. Furthermore, PwP tend to report having ophthalmologic symptoms more than persons without PD. The common symptoms related to the ocular surface may be closely related to PD. The decrease in dopamine can impair the motor control of the blink response, thereby resulting in a decreased blink rate (Biousse et al., 2004). The decreased blink rate can lead to dry eyes and offers one explanation why ocular surface symptoms such as blurriness (e.g., impaired acuity) were detected most frequently in PwP. In Mary Warren’s hierarchy of visual–perceptual skill development model, oculomotor control (e.g., decreased blink rate) and acuity constitute the foundational features of visual function (Warren, 1993a, 1993b). Evidence demonstrates that more advanced skills such as visual perception may be affected in PwP (Flowers & Robertson, 1995). On the basis of the hierarchical model, these foundational features may affect the more advanced visual–perceptual skills associated with visual functioning, thereby warranting further research in this area.
Visual Dysfunction and Occupational Performance in Persons With Parkinson’s Disease
Figure 1 shows that most respondents experienced low frequency of ophthalmological symptoms and mild dependence or little difficulty with vision-related activities of daily living. However, the frequency of ophthalmological symptoms is positively associated with the performance in vision dependent activities of daily living. In other words, frequent complaints of visual difficulties are associated with increased dependence or difficulty with activities of daily living. Taken together, when PwP experience ophthalmologic symptoms on a weekly or daily basis, these symptoms are likely to limit their occupational performance.
Figure 1 also indicates the data of three respondents who reported fewer complaints of ophthalmologic symptoms but total disability in vision-dependent activities of daily living. This finding suggests that factors other than visual dysfunction significantly contributed to the disability in these three respondents. The R–SRAFVP was developed to assess the ability of older adults with age-related eye disease to complete vision-dependent activities of daily living (Snow et al., 2018). The assessment is not able to separate the effects of motor impairment, such as tremor or rigidity, from those of visual dysfunction in PwP on the performance of vision-dependent daily activities, such as trimming fingernails and toenails.
Interventions to Address Visual Dysfunction in Persons With Parkinson’s Disease
To date, there have been no formal studies to investigate interventions to address visual dysfunction in PwP. In many rehabilitation clinics, the emphasis for treatment approaches continues to be placed on motor deficits (e.g., gait and tremor) and not activities of daily living. It is interesting to note that many of these approaches capitalize on visual cues to compensate for motor deficits. For example, floor stripes and laser lights offer strategies to reduce freezing (Bryant et al., 2010; Nieuwboer et al., 2007; Nonnekes et al., 2015); and the U-step walker also can be very useful in reducing freezing, festination, and small steps. The effect that disease-associated visual dysfunction may have on the efficacy of these treatment strategies in PwP remains unknown. It may be possible to borrow and adapt strategies used in low-vision rehabilitation (Whittaker et al., 2015). The occupational therapists at the University of Florida’s Norman Fixel Institute for Neurological Diseases have started to do this by introducing visual compensatory strategies to improve patients’ participation in activities of daily living. However, more research is needed to support the application of the low-vision rehabilitation approaches in this population.
Limitations
The results of this study should be interpreted with caution. One major limitation was that all data were self-reported and, therefore, subject to reporting bias. The use of email and electronic newsletters may have skewed recruitment of PwP toward those with adequate vision; and the online response method may have made it more difficult for people with tremors to participate. In turn, participation may have been biased toward PwP with less severe disease or slower disease progression. The Fixel Institute’s health care providers are well versed on the PD-related changes in vision that can occur; in turn, they often assess or evaluate visual function. It is possible that the participants in this study may have received more education related to visual function than the average person with PD. Therefore, general awareness among the general population of PwP may be even lower than 50%. The R–SRAFVP was developed for use in adults with low vision and not for PwP. It is necessary to consider the potential influence of cognitive and/or motor impairments in the interpretation of this scale’s score. Last, the sample studied lacked ethnic and racial diversity, which may have skewed results on the basis of potential differences in access to health care and/or incidence rates related to PD or ophthalmologic conditions. Therefore, future studies may benefit from focusing on more diverse samples of people with young-onset PD to limit confounding ocular comorbidities that tend to occur in older adults. In addition, it will be important to investigate any potential associations between diagnosed visual dysfunction and common medications prescribed for PD.
Implications for Occupational Therapy Practice
The results of this study have the following implications for occupational therapy practice: This study provides increased understanding of the relationship between visual dysfunction and occupational performance in PwP. Incorporating the screening of visual function during occupational therapy assessment and evaluation in PwP may help identity additional barriers to occupational performance. Improved education and resources about visual dysfunction should be made available to PwP to increase general awareness about visual dysfunction. The application and investigation of therapeutic strategies addressing visual dysfunction are critical in providing comprehensive care and improving activity participation in PwP.
Conclusion
Many PwP experience some degree of visual dysfunction, yet many remain unaware that the disease they live with may be the culprit. If the effect that PD can have on visual function is not understood by PwP or is overlooked by their health care provider, the underlying cause of difficulties engaging in daily occupations may be missed or mistaken. Assessing and evaluating visual function in PwP may aid in elucidating changes in occupational performance and help guide targeted treatment approaches as they become available. Intervening early on when symptoms are mild may offer a wide range of benefits. To more wholistically and comprehensively address functional performance in PwP, occupational therapists can screen for visual dysfunction and increase their clients’ awareness that PD can affect vision through education.
Footnotes
Acknowledgments
We acknowledge Chuck Jacobson, the database manager at the University of Florida Norman Fixel Institute for Neurological Diseases, for extracting registrant email addresses from the INFORM database. In addition, we thank the Norman Fixel Institute’s physicians and the University of Florida Health Rehabilitation’s occupational therapists. Specifically, we acknowledge Dr. Michael Okun (neurologist) and Dr. Kelly Foote (neurosurgeon) for their important medical and administrative contributions related to the dataset used in this study. Grant support for the use of REDCap was provided by the National Institutes of Health (NIH) National Center for Advancing Translational Sciences under award number UL1TR001427. The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH.