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Self-Reported Visual Complaints in People with Parkinson’s Disease: A Systematic Review

Abstract

Background:

Scientific research increasingly focuses on visual symptoms of people with Parkinson’s disease (PD). However, this mostly involves functional measures, whereas self-reported data are equally important for guiding clinical care.

Objective:

This review provides an overview of the nature and prevalence of self-reported visual complaints by people with PD, compared to healthy controls.

Methods:

A systematic literature search was performed. Studies from three databases (PubMed, PsycInfo, and Web of Science) were screened for eligibility. Only studies that reported results of visual self-reports in people with idiopathic PD were included.

Results:

One hundred and thirty-nine eligible articles were analyzed. Visual complaints ranged from function-related complaints (e.g., blurred vision, double vision, increased sensitivity to light or changes in contrast sensitivity) to activity-related complaints (e.g., difficulty reading, reaching, or driving). Visual complaints were more prevalent in people with PD compared to healthy controls. The presence of visual complaints leads to a reduced quality of life (QoL). Increased prevalence and severity of visual complaints in people with PD are related to longer disease duration, higher disease severity, and off-state.

Conclusion:

A large proportion of people with PD have visual complaints, which negatively affect QoL. Complaints are diverse in nature, and specific and active questioning by clinicians is advised to foster timely recognition, acknowledgement, and management of these complaints.

INTRODUCTION

Parkinson’s disease (PD) is a neurodegenerative disorder characterized by a number of well-known motor and non-motor symptoms, including visual problems [1–5]. During recent years, visual symptoms in PD have received increasing attention in the literature. In clinical practice however, these symptoms are still underrecognized. Visual symptoms are less conspicuous than motor symptoms, and may therefore be overlooked [6, 7]. However, visual symptoms have a substantial impact on the daily lives of people with PD and may already occur in the early and prodromal stages of the disease [1, 4, 8]. Consequently, several studies state the importance of tools to improve the recognition, diagnostic accuracy, and management of non-motor symptoms, including visual symptoms, in clinical practice [2, 9–11].

To date, most tools used to assess visual symptoms are quantitative tests of visual functions. These measurements, in most cases part of an ophthalmological assessment, objectify functions and impairments, such as visual acuity and visual field loss. In contrast, few studies include self-report data, asking people to reflect on their own visual functioning. It is acknowledged that both functional and self-reported data are required to obtain a clear picture of the impact of PD on individuals [9], which is necessary to guide care and rehabilitation [12, 13].

Despite the importance of self-reported data, no reviews have been published on this topic so far. Therefore, this paper presents a systematic review on self-reported visual complaints in PD, compared to healthy controls.

METHODS

Literature search

A literature search was performed according to the guidelines of Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) [14]. The search encompassed the scientific databases PsycInfo, PubMed, and Web of Science (Core Collection) and was performed on literature up to the date of February 5, 2021. The search terms are presented in Table 1. Two complementary searches were performed. The first one focused on subjective dysfunction in general, since the current review was part of a project that also examined self-reported cognitive complaints of people with PD. The second search addressed self-reported visual complaints specifically.

Table 1

Search terms for literature search

Search 1Terms used in all databasesMeSH and thesaurus terms used in PubMed or PsycInfo
First criterionparkinson*aPubMed: “Parkinson Disease”; PsycInfo: “Parkinson’s Disease”
Second criterion“self report”, complaint*, “subjective assessment*”, “subjective measure*”, “subjective problem*”, “subjective dysfunction*”, “subjective deficit*”, “subjective impairment*”, “subjective symptom*”, “report a problem”, “report problem*”, “report a dysfunction”, “report dysfunction*”, “report a deficit”, “report deficit*”, “report an impairment”, “report impairment*”, “report a symptom”, “report symptom*”, “reports a problem”, “reports problem*”, “reports a dysfunction”, “reports dysfunction*”, “reports a deficit”, “reports deficit*”, “reports an impairment”, “reports impairment*”, “reports a symptom”, “reports symptom*”, “reported a problem”, “reported problem*”, “reported a dysfunction”, “reported dysfunction*”, “reported a deficit”, “reported deficit*”, “reported an impairment”, “reported impairment*”, “reported a symptom”, “reported symptom*”, “perceive a problem”, “perceive problem*”, “perceive a dysfunction”, “perceive dysfunction*”, “perceive a deficit”, “perceive deficit*”, “perceive an impairment”, “perceive impairment*”, “perceive a symptom”, “perceive symptom*”, “perceives a problem”, “perceives problem*”, “perceives a dysfunction”, “perceives dysfunction*”, “perceives a deficit”, “perceives deficit*”, “perceives an impairment”, “perceives impairment*”, “perceives a symptom”, “perceives symptom*”, “perceived a problem”, “perceived problem*”, “perceived a dysfunction”, “perceived dysfunction*”, “perceived a deficit”, “perceived deficit*”, “perceived an impairment”, “perceived impairment*”, “perceived a symptom”, “perceived symptom*”, “experience a problem”, “experience problem*”, “experience a dysfunction”, “experience dysfunction*”, “experience a deficit”, “experience deficit*”, “experience an impairment”, “experience impairment*”, “experience a symptom”, “experience symptom*”, “experiences a problem”, “experiences problem*”, “experiences a dysfunction”, “experiences dysfunction*”, “experiences a deficit”, “experiences deficit*”, “experiences an impairment”, “experiences impairment*”, “experiences a symptom”, “experiences symptom*”, “experienced a problem”, “experienced problem*”, “experienced a dysfunction”, “experienced dysfunction*”, “experienced a deficit”, “experienced deficit*”, “experienced an impairment”, “experienced impairment*”, “experienced a symptom”, “experienced symptom*bPubmed: “Self Report”; PsycInfo: “Self Report”, “Self-Report”
Search 2Terms used in all databasesMeSH and thesaurus terms used in PubMed or PsycInfo
First criterionparkinson*aPubMed: “Parkinson Disease”; PsycInfo: “Parkinson’s Disease”
Second criterionquestionnaire*, scale*, survey*, inventor*, interview*bPubMed: “Surveys and Questionnaires”, “Interview, Psychological”; PsycInfo: Questionnaires, Interviews, Surveys, Inventories
Third criterionseeing OR eyesight OR sight OR ophthalmologic* OR “visual perception” OR “visual acuity” OR “visual field*” OR diplopia OR “double vision” OR “depth perception” OR “color vision” OR “colour vision” OR “color perception” OR “colour perception” OR “contrast sensitivity” OR “visual contrast” OR “brightness perception” OR “light sensitivity” OR “sensitive to light” OR “sensitivity to light” OR “oversensitive to light” OR “oversensitivity to light” OR photophobia OR photosensitivity OR glare OR “dark adaptation” OR “visual overload” OR “problems reading” OR “reading problem*” OR “difficulty reading” OR “reading difficult*” OR “painful eyes” OR “dry eyes” OR “eyelid opening” OR blink* OR “facial recognition” OR “face recognition” OR “face perception” OR “object recognition” OR “object perception” OR “figure perception” OR “form perception” OR “shape perception” OR “motion perception” OR “space perception” OR “spatial perception” OR “spatial orientation” OR “spatial disorientation” OR afterimage* OR “visual discrimination” OR “figure ground discrimination” OR “nonmotor symptom*” OR “non-motor symptom*” OR “autonomic dysfunction*” OR “autonomic symptom*” OR “autonomous dysfunction” OR “autonomous symptom*bPubMed: “Visual Perception”, “Vision disorders”, “Vision screening”, “Depth Perception”, “Color vision”; PsycInfo: “Visual perception”, “Vision disorders”, “Diplopia”, “Depth perception”, “Color perception”, “Brightness perception”, “Dark adaptation”, “Face perception”, “Visual acuity”, “Visual contrast”, “Visual discrimination”, “Visual field”, “Figure ground discrimination”

aTerm should be present in title or abstract, bOne of the terms should be present in the content of the paper.

Eligibility criteria

Only papers fulfilling the following criteria were included: written in English, published in peer-reviewed academic journals, including human participants with idiopathic PD, including a self-report measure for visual functioning, and data (i.e., prevalence) of this measure for the group of people with PD or a comparison (i.e., prevalence or score) with healthy controls. Visual self-report measures were defined as items, subscales or total scores representing an individual’s reflection on their own visual functioning, performance of visual activities or vision-related quality of life (QoL). We made the assumption that a self-report measure was filled out by the patient, unless otherwise stated. Longitudinal or intervention studies were included if relevant baseline measures were presented. Review articles and case reports were excluded, as well as meeting abstracts and letters to editors. Since visual hallucinations in PD are widely recognized and extensively studied [15], these were not incorporated in this review.

Literature extraction

Figure 1 shows the PRISMA outline of papers identified through the literature search. Articles were first screened by title and abstract, and when they seemed relevant, reviewed by the full text. In addition to the database search, reference lists of included papers were screened according to the predefined inclusion criteria. Two authors (IvdL and FH) and a research assistant (EV) systematically judged the eligibility of articles and discussed this in case of doubt. In case uncertainty remained, a third author (GdH) was involved until consensus was reached.

Fig. 1

PRISMA flow diagram of systematic literature search [14].

PRISMA flow diagram of systematic literature search [14].

Analysis

Relevant results were extracted from included papers. Results were categorized per complaint. Complaints were divided amongst three categories: function-related complaints, activity-related complaints, and vision-related QoL. Results were ordered based on the number of studies investigating each complaint. Based on this systematic categorization, a descriptive table was included (Table 2). If data on subgroups of PD were reported (e.g., tremor dominant versus akinetic-rigidity subtypes, or young versus late onset PD), but no total prevalence, it was calculated by the authors. The weighted prevalence of a complaint was calculated for studies using the same method to assess the complaint. Relationships of self-reported visual complaints with demographics and disease-related variables were gathered in an additional table (Table 3).

Table 2

Overview of the prevalence of visual complaints in people with PD and the comparison to healthy controls

Items covering complaint (N)Criterion presence complaintStudies (N)PD patients (N)Prevalence PD patients (%)Controls (N)Prevalence controls (%)Studies PD > Controlsa (N)Studies PD = Controls or PD < Controlsa (N)
Function-related visual complaints
Visual complaints in general17233726.8 – 982934416.1 – 31.660
  CIRS-G1≥1 on a 0 (‘no problem’) – 4 (‘extremely severe’) scale1 [19]7698N/AN/AN/AN/A
  VFQ-2525At least one complaint3 [18, 25, 26]14583.1 [25, 26]46631.6 [25]30
  Direct asking of the patient according to ICF checklist2≥1 (‘mild difficulty’) on a 0 – 4 scale1 [27]9675.5bN/AN/AN/AN/A
  Interview on autonomic dysfunction4N/A1 [20]2667272210
  Questionnaire on visual complaints (20-item)N/AN/A1 [16]3063.33129.010
  PRO-PD1≥5 on a 0 (‘lack of symptom’) – 100 (‘maximum severity’) scale1 [32]103158.0N/AN/AN/AN/A
  Self-report questionnaire (31-item)N/AAt least one complaint1 [17]8178cN/AN/AN/AN/A
  Survey of Health, Ageing, and Retirement in Europe1≥4 on a 1 (‘excellent’) – 5 (‘poor’) scale1 [21]19146.12882016.110
  Interview using a questionnaire on non-motor symptoms [30]1‘yes’2 [22, 30]7646.1N/AN/AN/AN/A
  Symptom questionnaire1‘yes’1 [28]3943.6N/AN/AN/AN/A
  Question: are you bothered due to vision-related problems?1N/A1 [23]29541N/AN/AN/AN/A
  Structured interviewN/AN/A1 [29]10840.7N/AN/AN/AN/A
  Symptom index (20-item)1‘yes’1 [31]6136.1N/AN/AN/AN/A
  Questions on visual complaintsN/AN/A1 [24]8226.8N/AN/AN/AN/A
Double vision96209947.7 – 53.115562.4 – 19.0153
  Questionnaire on changes in vision1‘sometimes’ or ‘often’2 [118, 119]23753.110019.020
  Self-report questionnaire (31-item)1‘sometimes’ or ‘often’1 [17]8138.0N/AN/AN/AN/A
  VIPD-Q1≥2 (‘weekly’) on a 0 (‘never’) – 3 (‘daily’) scale1 [117]84822250310
  Questionnaire derived from VFQ-25N/AN/A2 [25, 116]17819.81222.420
  Non-motor fluctuations questionnaire1N/A1 [159]1118.2N/AN/AN/AN/A
  NMSQ1≥1 (‘yes’)61 [33– 93]1151113.9d6903.5 [40, 47, 48, 56, 57, 59, 91, 92]6 [47, 48, 56, 57, 59, 91]2 [40, 92]
  NMSS1≥1 (‘mild’) on a 0 (‘none’) – 3 (‘severe’) scale24 [9, 41, 94– 115]754514.2 [9, 41, 94, 96– 107, 109– 115]3632.4 94, 96]3 [95, 96, 108]1 [94]
  Online symptom survey1‘yes’1 [160]43212.7N/AN/AN/AN/A
  Questionnaire on visual complaints (20-item)N/AN/A1 [16]3010.0313.210
  Questions on visual complaintsN/AN/A1 [24]829.8N/AN/AN/AN/A
  Questions on asthenopiaN/AN/A1 [152]397.7N/AN/AN/AN/A
Increased sensitivity to light27631815.0 – 4814800 – 28.3132
  Interview on autonomic dysfunction1N/A1 [20]2648N/AN/AN/AN/A
  VIPD-Q1≥2 (‘weekly’) on a 0 (‘never’) – 3 (‘daily’) scale1 [117]848432502310
  ADS (autonomic dysfunction score)1N/A1 [140]2138.127010
  SCOPA-AUT1≥1 (‘sometimes’) on a 0 (‘never’) – 3 (‘often’) scale19 [120– 138]519531.8 [120, 122, 124– 130, 132– 138]104428.3 [120, 128– 130, 132, 138]8 [120, 121, 123, 128– 130, 132, 138]1 [131]
  COMPASS-315N/A1 [161]4727.7N/AN/AN/AN/A
  Questionnaire derived from VFQ-25N/AN/A1 [25]8823.99011.810
  Questionnaire on changes in vision1‘sometimes’ or ‘often’1 [119]531531310
  VAQ3N/A1 [142]25N/A23N/A01
  COMPASS7N/A1 [139]15N/A15N/A10
Altered color vision913944.1 – 12.78943 – 1044
  Questionnaire on changes in vision1‘sometimes’ or ‘often’2 [118, 119]23712.71004.41 [118]1 [119]
  VIPD-Q1≥2 (‘weekly’) on a 0 (‘never’) – 3 (‘daily’) scale1 [117]84811250310
  Questions on visual complaintsN/AN/A1 [24]826.1N/AN/AN/AN/A
  Interview on prodromal symptoms1‘yes’2 [141, 143]1454.11451002
  VFQ-251N/A2 [18, 26]57N/A376N/A20
  VAQ3N/A1 [142]25N/A23N/A01
Painful/dry eyes917066.1 – 87.58508 – 22.451
  Dry eye symptom assessment‘various’≥2-3 times a week (‘occasionally’)1 [144]5687.53420.610
  VIPD-Q1≥2 (‘weekly’) on a 0 (‘never’) – 3 (‘daily’) scale1 [117]84828250810
  Question on dry eye1N/A1 [162]4344.2N/AN/AN/AN/A
  VFQ-252N/A3 [18, 25, 26]14527.3 [25]46622.4 [25]2 [18, 25]1 [26]
  Online symptom survey (dry eyes)1‘yes’1 [160]43225.7N/AN/AN/AN/A
  Questions on visual complaintsN/AN/A1 [24]826.1N/AN/AN/AN/A
  OSDI12N/A1 [145]100N/A100N/A10
Blurred vision6169519.7 – 466307.4 – 19.040
  VIPD-Q1≥2 (‘weekly’) on a 0 (‘never’) – 3 (‘daily’) scale1 [117]848462501210
  Symptom questionnaire1‘yes’1 [146]18136.226319.010
  ADS (autonomic dysfunction score)1N/A1 [140]2128.6277.410
  Interview on visual symptoms1‘yes’1 [111]12520N/AN/AN/AN/A
Online symptom survey1‘yes’1 [160]43219.7N/AN/AN/AN/A
  Questionnaire derived from VFQ-25N/AN/A1 [25]88N/A90N/A10
Changes in contrast sensitivity311578.8 – 2731910 – 1320
  Questionnaire on changes in vision1‘sometimes’ or ‘often’1 [118]18427691310
  VIPD-Q1≥2 (‘weekly’) on a 0 (‘never’) – 3 (‘daily’) scale1 [117]848262501010
  Interview on visual symptoms1‘yes’1 [111]1258.8N/AN/AN/AN/A
Changes in size and shape perception39823.7 – 192815 – 1320
  Questionnaire on changes in vision1‘sometimes’ or ‘often’1 [119]5319g311310
  VIPD-Q1≥2 (‘weekly’) on a 0 (‘never’) – 3 (‘daily’) scale1 [117]84817250510
  Questions on visual complaintsN/AN/A1 [24]823.7N/AN/AN/AN/A
Changes in depth perception392617 – 263042 – 631
  Questionnaire on changes in vision1‘sometimes’ or ‘often’1 [119]532631610
  VIPD-Q1≥2 (‘weekly’) on a 0 (‘never’) – 3 (‘daily’) scale1 [117]84817250210
  VAQ3N/A1 [142]25N/A23N/A1e1f
Reduced peripheral vision382N/A399N/A31
  VFQ-251N/A2 [18, 26]57N/A376N/A20
  VAQ5N/A1 [142]25N/A23N/A1e1f
Difficulty estimating spatial relations33906.4 – 50692810
  Questionnaire on changes in vision1‘sometimes’ or ‘often’1 [118]18450692810
  Self-report questionnaire (31-item)1‘sometimes’ or ‘often’1 [17]8145.0N/AN/AN/AN/A
  Interview on visual symptoms1‘yes’1 [111]1256.4N/AN/AN/AN/A
Visual field impairment29306.1 – 9250210
  VIPD-Q1≥2 (‘weekly’) on a 0 (‘never’) – 3 (‘daily’) scale1 [117]8489250210
  Questions on visual complaintsN/AN/A1 [24]826.1N/AN/AN/AN/A
Watery eyes293026.8 – 312501510
  VIPD-Q1≥2 (‘weekly’) on a 0 (‘never’) – 3 (‘daily’) scale1 [117]848312501510
  Questions on visual complaintsN/AN/A1 [24]8226.8N/AN/AN/AN/A
Changes in motion perception223723.7100320
  Questionnaire on changes in vision1‘sometimes’ or ‘often’2 [118, 119]23723.7100320
Reduced night vision286916 – 47.62773 – 18.520
  ADS (autonomic dysfunction score)1N/A1 [140]2147.62718.510
  VIPD-Q1≥2 (‘weekly’) on a 0 (‘never’) – 3 (‘daily’) scale1 [117]84816250310
Reduced light/dark adaptation2873272731121
  VIPD-Q1≥2 (‘weekly’) on a 0 (‘never’) – 3 (‘daily’) scale1 [117]848272501110
  VAQ4N/A1 [142]25N/A23N/A1e1f
Floaters2178N/A122N/A02
  Questionnaire derived from VFQ-25N/AN/A2 [25, 116]178N/A122N/A02
Misjudge objects2178N/A122N/A20
  Questionnaire derived from VFQ-25N/AN/A2 [25, 116]178N/A122N/A20
Asthenopia (ocular fatigue)13943.6395.110
  Questions on asthenopiaN/APresence of visual discomfort, diplopia, blurred vision or headache when reading1 [152]3943.6395.110
Hard to follow quick movements with the eyes184825250410
  VIPD-Q1≥2 (‘weekly’) on a 0 (‘never’) – 3 (‘daily’) scale1 [117]84825250410
Need to turn head to side to see peripheral objects15343311410
  Questionnaire on changes in vision1‘sometimes’ or ‘often’1 [119]5343311410
Mucus/slime or particles in eyes or eyelids184820250610
  VIPD-Q1≥2 (‘weekly’) on a 0 (‘never’) – 3 (‘daily’) scale1 [117]84820250610
Reduced acuity/spatial vision125N/A23N/A11
  VAQ4N/A1 [142]25N/A23N/A1e1f
Reduced visual processing speed125N/A23N/A11
  VAQ6N/A1 [142]25N/A23N/A1e1f
Reduced visual search125N/A23N/A01
  VAQ5N/A1 [142]25N/A23N/A01
Activity-related visual complaints
Reading difficulties6117618.3 – 42.04035.6 – 9.740
  Self-report questionnaire (31-item)N/AN/A1 [17]8142.0N/AN/AN/AN/A
  Questionnaire on visual complaints (20-item)N/AN/A1 [16]3026.7319.710
  Questions on asthenopiaN/AN/A1 [152]3923.1N/AN/AN/AN/A
  VIPD-Q1≥2 (‘weekly’) on a 0 (‘never’) – 3 (‘daily’) scale1 [117]84818.3h2505.6h10
  Questionnaire derived from VFQ-25N/AN/A2 [25, 116]178N/A122N/A20
Near activities5187534.5 – 44.31145589.7 – 25.550
  Survey of Health, Ageing, and Retirement in Europe1≥4 on a 1 (‘excellent’) – 5 (‘poor’) scale1 [21]143844.311380225.510
  CISS14≥212 [147, 148]38034.53809.720
  VFQ-253N/A2 [18, 26]57N/A376N/A20
Difficulty/freezing in narrow spaces441567.32221.640
  Questionnaire on changes in vision1‘sometimes’ or ‘often’2 [118, 119]23767.3i1001.6i20
  Questionnaire derived from VFQ-25N/AN/A2 [25, 116]178N/A122N/A20
Distance activities3149538.611417815.030
  Survey of Health, Ageing, and Retirement in Europe1≥4 on a 1 (‘excellent’) – 5 (‘poor’) scale1 [21]143838.611380215.010
  VFQ-253N/A2 [18, 26]57N/A376N/A20
Driving39421.63552.730
  VFQ-252N/A2 [18, 26]57N/A318N/A20
  Self-report driving questionnaire derived from Charlton et al. (2006) [163]N/A‘very difficult’ in low visibility conditions1 [149]3721.6372.710
Difficulty reaching for objects11844669310
  Questionnaire on changes in vision1‘sometimes’ or ‘often’1 [118]1844669310
Problems with visual ADLs125N/A23N/A11
  VAQ33N/A1 [142]25N/A23N/A1e1f
Vision-related QoL
Vision-specific social functioning257N/A376N/A20
  VFQ-252N/A2 [18, 26]57N/A376N/A20
Vision-specific role difficulties257N/A376N/A11
  VFQ-252N/A2 [18, 26]57N/A376N/A1 [18]1 [26]
Vision-specific dependency257N/A376N/A20
  VFQ-253N/A2 [18, 26]57N/A376N/A20
Vision-specific mental health257N/A376N/A20
  VFQ-254N/A2 [18, 26]57N/A376N/A20

Per complaint, each self-report measure used to describe this complaint is presented individually, along with the number of visual items it includes and the criterion that must be fulfilled for people to belong to the group with visual complaints. Weighted averages (prevalence of visual complaints) are presented for each complaint. References to the studies are placed in brackets []. ADLs, activities of daily living; CIRS-G, Cumulative Illness Rating Scale-Geriatric; CISS, Convergence Insufficiency Symptom Survey; COMPASS, Composite Autonomic Symptom Score; ICF, International Classification of Functioning; N, number/population size; N/A, not available; NMSQ, Non-Motor Symptoms Questionnaire, NMSS = Non-Motor Symptom Scale, OSDI = Ocular Surface Disease Index, PD = Parkinson’s disease, PRO-PD = Patient Reported outcomes in Parkinson’s Disease; QoL, quality of life; SCOPA-AUT, SCales for Outcomes in PArkinson’s disease– autonomic dysfunction; VAQ, Visual Activities Questionnaire; VFQ-25, Visual Function Questionnaire (25-item); VIPD-Q, Visual Impairment in Parkinson’s Disease Questionnaire. a Difference in score or prevalence between the groups, b Weighted prevalence of complaints on the ICF functions ‘seeing functions’ (72.9%) and ‘difficulty with watching’ (78.2%), c Items that may to some extent have arisen from motor symptoms (e.g., bumping into objects and freezing in narrow spaces) were included in the analysis. Prevalence was 57% after removing these items, dKhedr et al. (2012) [90] & Khedr et al. (2013) [55], and Giorelli et al. (2014) [65] & Giorelli et al. (2014) [66] used the same group of people with PD and reported the same results. For this reason, results of only one of these studies was reported, e Results only account for the non-tremor group (N = 12), f Results only account for the tremor group (N = 13), g Weighted prevalence of complaints on size (17%) and shape perception (21%), h Weighted prevalence of reading related complaints: ‘letters disappear while reading’ (20% in patients and 5% in controls) and ‘read better with one eye closed’ (17% in patients and 6% in controls), iWeighted prevalence of the complaints freezing (60% in patients and 3% in controls) and difficulty at doorways (56% in patients and 3% in controls) [119].

Table 3

Relationship of demographic and disease-related variables with visual complaints

Visual complaintSignificant positive relationshipSignificant negative relationshipNo significant relationship
Demographic or disease-related variable
1. AgeStudies (N)103
  Double vision002 [66, 111]
  Increased sensitivity to light001 [122]
  Reduced visual health status1 [26]00
2. Gender (+men > women)Studies (N)1012
  Visual complaints in general001 [117]
  Double vision0010 [34, 50, 66, 67, 72, 75, 97, 103, 105, 111
  Increased sensitivity to light001 [122]
  Altered color vision1 [17]00
  Difficulty estimating spatial relations1 [17]a00
3. EducationStudies (N)001
  Double vision001 [111]
4. Disease durationStudies (N)603
  Visual complaints in general2 [32, 117]01 [17]
  Double vision3 [101, 111, 116]01 [17]
  Increased sensitivity to light1 [137]01 [122]
  Altered color vision001 [17]
  Difficulty estimating spatial relations001 [17]
  Asthenopia001 [152]
5. Disease severityStudies (N)1206
  Visual complaints in general001 [17]
  Double vision5 [52, 59, 110, 111, 116]2 [17, 66]
  Increased sensitivity to light4 [120, 132, 138, 151]b4 [122, 131, 133, 151]c
  Altered color vision01 [17]
  Difficulty estimating spatial relations01 [17]
  Asthenopia1 [152]00
  Reduced visual health status2 [18, 26]00
  Bumping into objects001 [17]
6. Motor fluctuationsStudies (N)200
  Double vision2 [104, 111]00
7. Dominant symptom (+PIGD > tremor dominant)Studies (N)207
  Double vision1 [36]06 [50, 55, 66, 81, 93, 96]
  Increased sensitivity to light001 [142]
  Altered color vision001 [142]
  Changes in depth perception1 [142]00
  Reduced peripheral vision001 [142]
  Reduced light/dark adaptation1 [142]00
  Reduced acuity/spatial vision001 [142]
  Reduced visual processing speed001 [142]
  Reduced visual search001 [142]
  Problems with visual ADLs1 [142]00
8. DyskinesiaStudies (N)100
  Double vision1 [104]00
9. Left vs. right onset PDStudies (N)001
  Double vision001 [81]
10. Young vs. late onset PD (+late onset > young onset)Studies (N)202
  Double vision2 [70, 103]d02 [77, 79]
11. Idiopathic PD vs. gene-related parkinsonism (LRRK2 [33], G2385R [161] and PARKIN [79]; +idiopathic PD > gene-related parkinsonism)Studies (N)103
  Double vision1 [79]e02 [33, 79]fg
  Increased sensitivity to light001 [161]
12. CamptocormiaStudies (N)101
  Double vision1 [114]01 [113]
Medical or surgical treatment
13. LEDDStudies (N)115
  Double vision01 [111]1 [54, 59, 82, 94]
  Reduced visual health status1 [26]00
  Increased sensitivity to light001 [132]
14. Off vs. on state (+off state > on state)Studies (N)300
  Visual complaints in general1 [30]00
  Double vision1 [111]00
  Problems focusing1 [119]00
15. Specific medical treatment (Pergolide and Benzhexol [119], and Rotigotine [87, 164])Studies (N)102
  Double vision002 [87, 164]
  Adverse visual effects1 [119]h00
16. DBS (subthalamic nucleus)Studies (N)020
  Double vision02 [22, 61]0
Other variables
17. QoL and ADLStudies (N)051
  Visual complaints in general01 [117]0
  Double vision01 [118]0
  Increased sensitivity to light03 [122, 137, 151]1 [125]
18. Consultation of medical doctor for eye problemStudies (N)101
  Bumping into objects1 [17]00
  Dry eyes001 [162]

Supplementary Table 2 provides an overview of investigated relationships per complaint. >, first group reported more visual complaints than second group; ADL, activities of daily living; DBS, Deep Brain Stimulation; LEDD, Levodopa Equivalent Daily Dose; N, number of studies; PIGD, postural instability and gait disorder; QoL, quality of life. aSide of onset influenced the relationship of gender with difficulty estimating spatial relations; the difference between males and females was bigger (and significant) for the left onset group than right onset group (not significant), bDisease severity measured by Hoehn & Yahr classification and Clinical Impression of Severity Index for Parkinson’s Disease (CISI-PD) [151], cDisease severity measured by Cumulative Illness Rating Scale – Geriatrics (CIRS-G) [151], dOnly significant when adjusted for disease duration and dopaminergic treatment duration and dose [70], eResult accounts for a group of patients with late onset PD [79], fResult accounts for a group of patients with young onset PD [79], gNot significant when adjusted for age, gender, disease duration, disease severity, dopamine agonist, and levodopa [33], hMore colorful dreams were reported after using Pergolide, and relaxation of the eye muscles and blurry vision after using Benzhexol [119].

RESULTS

The search procedure resulted in 139 relevant articles. Table 2 presents the prevalence of visual complaints reported by people with PD and the comparison with healthy controls. One hundred and thirty-one studies investigated the prevalence of visual complaints in people with PD. Some studies reported on more than one complaint, resulting in 185 prevalence numbers. Forty-four studies compared the presence of visual complaints between people with PD and healthy controls. Some studies reported group differences for multiple complaints, resulting in 122 numbers on group comparisons. Of these, 102 (83.6%) indicated that people with PD reported more complaints than healthy controls, whilst 20 (16.4%) found either no difference between these groups or reported healthy controls to experience more complaints than people with PD.

Function-related visual complaints

Visual complaints in general

Seventeen studies [16–32] reported on visual complaints in general. Six of these studies compared people with PD with a control group. In all cases, the prevalence of visual complaints was higher among patients than among controls [16, 18, 20, 21, 25, 26]. One study examined the number of complaints experienced. Three out of four patients (77.3%) experienced at least one complaint, and 43.2% experienced multiple visual complaints [25]. Only 31.6% of healthy controls reported a visual complaint [25].

Double vision

Sixty-one studies reported relevant results on double vision based on the Non-Motor Symptoms Questionnaire (NMSQ) [33–93] and 24 studies based on the Non-Motor Symptom Scale (NMSS) [9, 41, 94–115] (see Supplementary Figure 1). The prevalence ranged from 2.9% [72] to 23.5% [59] in studies with a sample size≥150. Studies with a smaller sample size (N < 150) showed a range from 0% [35, 40, 94] to 60.9% [45]. One study found that for most people with PD experiencing double vision (9.6% of total sample) complaints started after motor symptoms had manifested. Only a small proportion (1.8% of total sample) already experienced double vision before the onset of motor symptoms [71].

Most studies (15/18) on double vision showed a higher prevalence in people with PD compared to controls [16, 25, 47, 48, 56, 57, 59, 91, 95, 96, 108, 116–119]. One study reported prevalence numbers in more detail and showed that 16% of people with PD experienced double vision ‘often’, and 36% ‘sometimes’ [118].

Increased sensitivity to light

Nineteen studies included the SCales for Outcomes in PArkinson’s disease–autonomic dysfunction (SCOPA-AUT) [120] and reported relevant results for the item on oversensitivity to light in people with PD [120–138]. The prevalence ranged from 1.9% [130] to 61.0% [120] (see Supplementary Figure 2). Most studies (13/15) showed that the prevalence was higher in people with PD compared to controls [25, 117, 119–121, 123, 128–130, 132, 138–140].

Other light-related complaints were more prevalent in people with PD as well. People with PD had significantly more difficulty adapting to changing light conditions than controls (patients: 27% vs. controls: 11%) [117], and experienced reduced night vision more often (patients: 16%–47.6% vs. controls: 3%–18.5% [117, 140]).

Altered color vision

Prevalence of altered color vision did not significantly differ between people with PD and healthy controls in the majority of studies [18, 26, 118, 119, 141–143]. Three studies indicated a trend toward more complaints among people with PD [18, 26, 118]. Only one study found that significantly more people with PD (11%) reported the perception of colors to be more pale than controls did (3%) [117]. Another study found that 10% of people with PD perceived less color than before, while 5% perceived more color [118].

Painful, dry or watery eyes

Complaints related to painful, dry or watery eyes were more frequently reported by people with PD than by controls (5/6 studies [18, 25, 117, 144, 145]). Also, severity seems to differ. People with PD had ‘moderate dry eye disease’ and controls ‘mild dry eye disease’ [145]. It was reported that 28% of people with PD had a burning sensation or gritty feeling in their eyes, and only 8% of controls [117]. While some studies could not confirm significance [25, 26], painful eyes were present in 27.3% of people with PD compared to 22.4% of controls [25]. Watery eyes were more frequently reported by people with PD (26.8%–31%) than controls (15%) [24, 117].

Blurred vision

The prevalence of blurry vision was higher in people with PD compared to healthy controls (4/4 studies [25, 117, 140, 146]). Patients experiencing blurry vision indicated that their vision was worse in the dark and they needed more light to see clearly [119].

Changes in contrast sensitivity

Changes in contrast sensitivity were more often reported by people with PD compared to controls (2/2 studies [117, 118]). Roughly a quarter of people with PD (27%) reported changes in the perception of contrast (23% perceived less contrast, 4% perceived more contrast) [118]. People with PD (26%) reported more difficulty reading plain text on a colored or gray background compared to controls (10%) [117].

Changes in size, shape, or depth perception

People with PD reported more complaints regarding size, shape, or depth perception than controls [117, 119]. Seventeen percent of people with PD experienced difficulty with size, shape, and depth perception, compared to 2% (depth) – 5% (size/shape) of controls [117].

Peripheral vision

People with PD experienced significantly more limitations in peripheral vision (i.e., ‘noticing objects off to the side’) than controls [18, 26]. People with PD (43%) indicated to need to turn their head to the side to see peripheral objects more often than controls did (14%) [119].

Difficulty estimating spatial relations

Half of the patients (50%) reported misjudging spaces (5% ‘often’ and 45% ‘sometimes’), compared to 28% of controls [118]. Most people with PD (27%) indicated that spaces appear smaller, while 17% noted that spaces seem larger.

Visual field impairment

People with PD experienced visual field impairments more often (6.1% [24] – 9% [117]) than healthy controls (2% [117]).

Changes in motion perception

Changes in motion perception were reported by a significantly higher number of people with PD (19%–25%) than controls (3%) [118, 119]. Eight percent of people with PD had difficulties ‘often’, and 17% ‘sometimes’. Most people with PD perceived motion as faster (13%), while few perceived motion to be slower (4%). Others perceived motion to be less smooth (3%) [118]. In addition, people with PD had more difficulty following quick movements with their eyes (patients: 25% vs. controls: 4%) [117].

Activity-related visual complaints

Reading difficulties

People with PD reported more difficulty reading than controls (4/4 studies [16, 25, 116, 117]). While one study could not confirm significance, a higher prevalence was found in people with PD (26.7%) compared to controls (9.7%) [16]. Compared to controls, people with PD reported significantly more often that letters disappeared while reading (patients: 20% vs. controls: 5%) and that they had fewer reading difficulties when having one eye closed while reading (patients: 17% vs. controls: 6%) [117].

Near and distant visual activities

People with PD reported more problems with near (patients: 44.3% vs. controls: 25.5%) and distant visual activities (patients: 38.6% vs. controls: 15.0%) than controls [21]. All five studies confirmed this result [18, 21, 26, 147, 148]. Most individuals who had difficulty working nearby reported that their eyes felt tired or uncomfortable [147, 148]. In contrast, people with PD ‘often’ do not have trouble judging close (95%) or distant objects (87%), comparable to healthy controls, of which 96% and 99% did not have problems judging close or distant objects, respectively [118].

Difficulty/freezing in narrow spaces

People with PD had more difficulty in narrow spaces than controls (4/4 studies [25, 116, 118, 119]). Walking through narrow spaces was difficult for 70% of people with PD, compared to 1% of controls [118]. Eighteen percent of people with PD indicated to have difficulties ‘often’, and 52% ‘sometimes’. People with PD indicated to freeze (26%), bump (29%), feel uneasy (10%), or have other problems (3%) while walking through narrow spaces.

Freezing (patients: 60% vs. controls: 3%) and difficulty at doorways (patients: 56% vs. controls: 3%) was also significantly more common in people with PD compared to controls [119]. Half of the people with PD reported to bump into objects [17].

Driving

People with PD experienced more driving difficulties compared to controls (3/3 studies [18, 26, 149]). This could be attributed to poor vision, especially at night. Along with that, people with PD reported difficulties with reading maps or using navigational devices [17]. Besides finding driving more difficult in low visibility conditions (patients: 21.6% vs. controls: 2.7%), people with PD avoid these situations more frequently compared to controls (patients: 35.1% vs. controls: 5.4%) [149].

Difficulty reaching for objects

People with PD reported significantly more difficulty reaching for objects (46%) than controls (3%). Nine percent of people with PD had difficulties ‘often’, and 37% ‘sometimes’. Most patients indicated to not reach far enough (27%), while others reached too far (7%) or reached off to one side of the object (8%) [118].

Vision-related QoL

People with PD scored significantly worse than controls on vision-related QoL (Visual Function Questionnaire; VFQ [150]) [18, 26]. Social functioning and mental health are influenced, role difficulties exist, and people with PD are more dependent on others due to their visual problems. Except for role difficulties, vision-related QoL was influenced to a greater extent in people with PD than in controls.

Relationship of demographic or disease-related variables with visual complaints

Table 3 reports on the relationship of demographic and disease-related characteristics with self-reported visual complaints. Visual complaints did not relate to age (3/4 studies [66, 111, 122]) and gender (12/13 studies [34, 50, 66, 67, 72, 75, 97, 103, 105, 111, 117, 122]). Most studies did find a relationship with disease duration (6/9 studies [32, 101, 111, 116, 117, 137]) and severity (12/18 studies [18, 26, 52, 59, 110, 111, 116, 120, 132, 138, 151, 152]), indicating that visual complaints were more prevalent in patients with a longer disease duration and a more severe disease. Dominant symptoms of the disease (7/9 studies [50, 55, 66, 81, 93, 96, 142]), as well as side of onset (1/1 study [81]) did not relate to visual complaints.

A higher Levodopa Equivalent Daily Dose (LEDD) was not related to visual complaints (5/7 studies [54, 59, 82, 94, 132]), while patients did report more complaints during off-state (3/3 studies [30, 111, 119]). Some medicaments (i.e., Pergolide and Benzhexol) led to visual adverse effect (1/1 study [119]). Deep Brain Stimulation (DBS) was found to relieve double vision (2/2 studies [22, 61]).

The relationship of visual complaints with objectified visual disorders and non-motor symptoms was also investigated (see Supplementary Table 1). Double vision was related to abnormal ocular alignment and aberrant movements of the eyes [116]. Regarding painful or dry eyes, decreased tear production, abnormalities in Meibomian glands, and ocular surface problems could confirm the complaint [16, 145], but it was not related to decreased tear film break-up time or tear osmolarity [145]. Visual complaints were not related to cognitive functioning (3/4 studies [102, 111, 151]), but it did co-occur with psychotic symptoms (e.g., hallucinations; 3/3 studies [24, 111, 151]).

Visual complaints were found to negatively relate to the performance of activities of daily living (ADL) and QoL (5/6 studies [117, 118, 122, 137, 151]).

Supplementary Table 2 presents an overview of investigated relationships with demographic and disease-related variables per visual complaint (an aid for understanding Table 3 and Supplementary Table 1).

DISCUSSION

This systematic review aimed to provide an overview of the literature on self-reported visual complaints in people with PD. Visual complaints occur in a wide variety in people with PD. Moreover, there is a fundamental difference between people with PD and healthy controls. More than 80% of comparisons showed that visual complaints were more common in people with PD than in controls.

According to the literature found, the prevalence of visual complaints varies greatly. Nevertheless, we can conclude that visual complaints were more often present in people with PD than in controls. Visual complaints in general appear to occur in at least a quarter of people with PD, with prevalence ranging from 26.8%–98%. Other complaints with a relatively high prevalence are blurred vision (19.7%–46%), watery eyes (26.8%–31%), light-related complaints (reduced night vision (16%–47.6%) and light/dark adaptation (27%)), ocular fatigue (43.6%), and all activity related complaints (> 21.6%; i.e., reading, driving, reaching, near or distant activities, and difficulty/freezing in narrow spaces). Complaints that appear less prevalent are altered color vision (4.1%–12.7%), and visual field deficits (6.1%–9%).

Vision-related QoL in people with PD appears to be affected in a variety of ways. This is not surprising given that vision is essential in performing a wide variety of activities. Moreover, people with PD need their vision to compensate for their motor loss [6]. Therefore, vision loss may lead to even more difficulties in daily life.

Strengths and limitations

We conducted a systematic literature search and selected all articles that met the inclusion criteria. By involving at least three researchers in the process of data extraction, we sought to ensure reliable and standardized data extraction.

We aimed at providing a comprehensive overview of the literature on self-reported visual complaints in PD. The inclusion of lower quality studies may have biased the results. The prevalence of a complaint was sometimes determined by only few studies and small sample sizes (e.g., asthenopia prevalence was determined in 39 patients [152]). Moreover, the studies used different methods, response options and criteria to assess the complaints in patient groups with different disease characteristics. Therefore, the results presented should be interpreted with caution and results cannot be directly compared. For example, the two lowest rates of double vision are found in de novo PD patients [72, 94], which is in line with the reported increase of visual complaints with disease duration and severity (see Table 3). Also, it was not always clear in the phrasing of questions that problems were attributed to vision [17, 118, 119]. People might have involved other symptoms when answering the questions (i.e., reading difficulties were attributed to both visual problems and difficulties with concentration [17]). For the sake of transparency, we listed the (number of) references, the number of participants in whom a complaint was investigated, and the criterion on which the prevalence was based.

Some visual complaints are reported relatively often, while there are also complaints that are hardly ever reported. An important explanation for this is that former complaints are addressed in frequently used self-reports or questionnaires, while the latter are not. This does not mean that visual complaints not included in those instruments are less common or should be taken less seriously. The majority of 139 included studies (N = 85, 61.2%) reported double vision, an item in the NMSS and NMSQ. Similarly, oversensitivity to light constitutes an item in the SCOPA-AUT and was therefore reported in multiple studies (N = 19, 13.7%). Only 35 articles (25.2%) investigated visual complaints using other measures. For example, only few studies asked for experienced visual field loss or reduced contrast sensitivity, which might nevertheless be relevant in the light of known visual field and contrast sensitivity deficits in PD [4, 153]. To obtain a more complete picture of the prevalence, nature, and severity of visual complaints in people with PD and the characteristics of people who experience these complaints, future research should systematically examine a broad range of visual complaints in a large group of people with PD.

Clinical implications

Detection of visual complaints is necessary to prevent unnecessary limitations in QoL. With knowledge of the visual complaints a patient experiences, clinicians are able to select treatments based on the patient’s priorities [12, 154]. In addition, the use of self-report measures within rehabilitation may provide insight into the changes a patient is experiencing and can indicate when individual goals have been achieved [13].

Visual complaints may be an indication of a treatable underlying disorder, which requires assessment and treatment by an ophthalmologist. Complaints may also relate to underlying disorders that cannot be treated, in which case vision-related rehabilitation may be recommended. As an example, complaints of double vision may be caused by cataract, ptosis, or corneal surface abnormalities. These conditions may be treated with cataract extraction, surgery, or artificial tears, respectively. Another possible cause of double vision is convergence insufficiency, which may require prism glasses or advice on how to compensate while reading.

In some cases, objectified functional disorders may not fully reflect self-reported complaints. For example, even though color vision deficits are more common in people with PD compared to controls [155, 156], people with PD do not tend to report more complaints with regard to color vision. In this example, treatment seems irrelevant because patients do not suffer from the underlying disorder. Therefore, care should always be based on self-reported complaints as well.

Although the literature is scarce, visual complaints seem to be related to disease duration and severity. In addition, visual complaints might be influenced by certain types of treatment. Therefore, we suggest that people with PD should be questioned more frequently and more thoroughly about these complaints in clinical practice, especially in advanced disease stages or with medication changes.

The importance of active questioning is also evident from the fact that visual problems might not always be spontaneously reported to healthcare professionals [48, 49], given that people with PD and their family members are often unaware of the relationship between visual complaints and PD [50]. In addition, Martinez-Martin et al. (2007) argued that these complaints may not be recognized unless detected by a questionnaire [60]. Recently developed visual self-report questionnaires may be used to improve the visual care for people with PD [157, 158].

Conclusion

This overview illustrates that a substantial number of people with PD report complaints in a variety of visual domains. These complaints are related to disease duration and severity and may be influenced by medication use. Since visual complaints have a clear negative impact on QoL, attention to and management of these complaints is essential. Active questioning is advised for timely recognition and treatment of visual complaints.

ACKNOWLEDGMENTS

This work was supported by Stichting NOVUM, Amsterdam, The Netherlands, ZonMw grant 637005001 (Expertisefunctie Zintuiglijk Gehandicapten, Meerjarig deelsectorplan 2020-2022 Visueel).

Research support: E. Vooijs (BSc), Psychology student at the University of Groningen; K.C. Klaassen (MSc) and J.E.M. Meijerink (MSc), Patient-Res-earchers for the Dutch Parkinson’s Disease Association.

CONFLICT OF INTEREST

The authors have no conflict of interest to report.

SUPPLEMENTARY MATERIAL

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