Abstract
Background
We recently reported that convergence insufficiency (CI)‐type visual symptomatology was more prevalent in participants with Parkinson's disease (PD), compared to controls. The objective of this work was to determine the prevalence of a confirmed clinical diagnosis of CI in PD, compared to controls.
Methods
Participants with (n = 80) and without (n = 80) PD were recruited and received an eye exam. Published criteria were used to arrive at a clinical diagnosis of CI. The Convergence Insufficiency Symptom Survey (CISS‐15) questionnaire was administered to each participant, with a score of ≥21 being considered positive for CI symptomatology. Student t test, chi‐square, or nonparametric tests at the 0.05 level were used for statistical significance.
Results
A total of 43.8% of participants with versus 16.3% without PD had a clinical diagnosis of CI (P ≤ 0.001). A total of 53.8% of participants with versus 18.8% without PD had scores on the CISS‐15 of ≥21 (P ≤ 0.001).
Conclusions
These results indicate that individuals with PD have a higher prevalence of CI and CI symptomatology than controls. These data provide evidence supporting the notion that treatment for symptomatic CI should be investigated in individuals with PD.
Keywords: convergence insufficiency, Parkinson's disease, prevalence
Although the motor symptoms of Parkinson's disease (PD) have long been documented, nonmotor aspects are less well recognized in clinical practice.1 Among those are the ocular/visual symptoms, which are quite prevalent in patients with PD.2 Many visual problems affecting PD patients, such as the alterations in the blink pattern,3 contrast sensitivity,4 color vision,5, 6 vergence eye movements/ocular motilities,7, 8 flash9 and pattern10 electroretinograms, and visual evoked potentials11 are well documented and have been linked, at least in part, to the dopaminergic deficit found in the disease.
Many patients with PD suffer from eye strain while reading3, 12 that is sometimes accompanied by double vision.1, 12, 13, 14 These two complaints are often linked to convergence insufficiency (CI) with a decreased convergence amplitude. Although CI is described as being common in PD,15 little data exist in the literature. In a 27‐patient study, Repka et al.16 reported that PD patients had significantly more frequent signs and symptoms associated with CI compared to age‐matched controls. Around one‐third of their PD patients had a clinical diagnosis of CI. Lepore17 found that all PD patients with or without diplopia who could be tested had CI, and that those without diplopia had significantly higher convergence amplitudes and shorter disease duration. Other studies on PD often indicate that double vision is prevalent in these patients,1, 3, 13, 14 without mentioning the cause of diplopia. Recently, we reported that CI‐type visual symptomatology was more prevalent in PD, compared to age‐matched individuals without the disease.2 Our objective here was to determine the prevalence of a confirmed clinical diagnosis of CI in PD, in comparison to controls.
Patients and Methods
This study was conducted in collaboration with researchers from the Institut universitaire de gériatrie de Montréal (IUGM), the Centre hospitalier de l'Université de Montréal (CHUM), the Montreal General Hospital (MGH), and the University of Waterloo. The study protocol was approved by the research ethics committee of each of these institutions, and each person signed an informed consent form before participation.
Eighty participants with PD and 80 age‐ (±3 years) and sex‐matched controls were recruited from a pool of 600 participants having participated in another study looking at the prevalence of CI‐type visual symptomatology. The participants with PD were contacted first, starting with the first one in the database onward. Each time a person with PD agreed to participate, the first age‐ and sex‐matched control in the database was contacted, until one agreed to participate. The recruitment continued this way until 80 PD and non‐PD individuals agreed to participate.
An experienced research optometrist performed a complete eye exam, including refractive, binocular vision, and ocular health assessments, on each participant. Clinical tests for CI (horizontal phorias at 6 m and 40 cm, positive fusional vergences [PFVs] at 40 cm and near point of convergence [NPC]) were performed three times each and the average calculated. Diagnosis of CI was based on the published criteria from the “Convergence insufficiency treatment trial (CITT)”18, 19: (1) exophoria at near (0.4 m) at least four prism diopters (∆) greater than at far (6 m); (2) a receded NPC break of 6 cm or greater; and (3) insufficient PFV at near (PFV less than twice the amount of the near phoria) or a break on PFV of ≤15∆ base‐out. A clinical diagnosis of CI was made when a participant met all three criteria.
The research optometrist also administered a Mini–Mental State Examination (MMSE) and the Convergence Insufficiency Symptom Survey (CISS‐15) to each participant. Patients scoring <24 on the MMSE were excluded. The CISS‐15 questionnaire measures the frequency and severity of CI symptoms.18, 19 It contains 15 symptom items with a scale from 0 to 4 (0 = never; 1 = infrequently; 2 = sometimes; 3 = fairly often; 4 = always), for a maximum score of 60 indicating greater symptom severity. A score of ≥21 represents the cutoff for symptomatic individuals.18
Statistical average differences and percentage differences between two independent groups were respectively determined using the Student t test and chi‐square at the 0.05 level of significance. A nonparametric test (Kolmogorov‐Smirnov between two independent groups) was used for comparing data of sample sizes smaller than 30. Statistical relationships between continuous variables and age and duration of PD were tested by the Pearson correlation coefficient.
Results
There were 31 women and 49 men in each of the two study groups. Average age was 67.4 ± 8.5 years in the PD group and 68.2 ± 8.1 years in controls (P > 0.05). Average MMSE score was 27.9 ± 2.1 in PD participants and 28.7 ± 1.3 in controls (P ≤ 0.001). Mean PD duration was 9.0 ± 5.8 years (range: 1–39).
The group‐average NPC was 9.0 ± 6.5 cm in PD and 3.5 ± 4.7 cm in controls (P ≤ 0.001). The group‐average exophoria at 6 m was 1.5 ± 2.7∆ in PD and 0.7 ± 1.7∆ (P ≤ 0.05) in controls. At 40 cm, it was 5.3 ± 3.8∆ in PD and 3.8 ± 3.6∆ in controls (P ≤ 0.01). The group‐average PFV was 7.3 ± 5.2∆ in PD and 12.6 ± 6.3∆ in controls (P ≤ 0.001). NPC, PFV, phoria at 6 m and 40 cm, and CISS‐15 score were not significantly related to age or disease duration in PD (P > 0.05).
Participants (PD and controls) having positive signs or symptoms of CI were divided into three groups based on their results: (1) those who have symptoms only, that is, CISS‐15 scores >21 (labeled: subjective CI); (2) those who have a confirmed clinical diagnosis (labeled: objective CI); and (3) those who have both CISS‐15 > 21 and a confirmed diagnosis (labeled: symptomatic CI). Table 1 shows that the group‐average CISS‐15 score and percent of participants with subjective, objective, and symptomatic CI were all greater in PD than in controls.
Table 1.
CISS‐15 data for PD participants and controls and some characteristics of those having objective CI
| PD participants (n = 80) | Controls (n = 80) | P value | |
|---|---|---|---|
| CISS‐15 mean (range) | 21.6 ± 8.8 (1–41) | 13.4 ± 8.9 (0–42) | *** |
| Subjective CI: % (n) | 53.8 (43) | 18.8 (15) | *** |
| Objective CI: % (n) | 43.8 (35) | 16.3 (13) | *** |
| Age (years) | 69.4 ± 8.7 | 69.2 ± 9.1 | ns |
| MMSE | 27.8 ± 2.4 | 28.2 ± 1.2 | ns |
| CISS‐15 | 24.2 ± 8.3 | 20.8 ± 12.8 | ns |
| Symptomatic CI: % (n) | 31.3 (25) | 7.5 (6) | *** |
***P ≤ 0.001.
ns, not statistically significant.
Among individual CISS symptoms in participants having subjective CI, those that stood out most were “eyes feel tired” and “eyes feel uncomfortable” when reading or doing close work. Those that emerged least were “headache” for PD participants and “double vision” for controls. Similar symptom‐related findings were also found for participants having objective and symptomatic CI (Table S1).
The CI‐defining clinical data of participants having subjective, objective, and symptomatic CI are detailed in Table 2. In each of these three groups, the NPC was more receded for the participants with PD versus controls.
Table 2.
CI‐defining clinical data for PD participants and controls having either subjective CI, objective CI, or symptomatic CI
| PD Participants | Controls | |
|---|---|---|
| SUBJECTIVE CI (n) | 43 | 15 |
| NPC (cm) | 11.2 ± 6.2 | 4.4 ± 3.7*** |
| Horizontal phoriaa @ 6 m (∆) | 1.5 ± 2.7 | 0.8 ± 1.3 ns |
| Horizontal phoria @ 40 cm (∆) | 5.5 ± 4.1 | 4.1 ± 2.6 ns |
| Phoria @ 40 cm − phoria @ 6 m (∆) | 3.9 ± 2.4 | 3.3 ± 1.8 ns |
| PFV @ 40 cm (∆) | 6.2 ± 3.7 | 12.9 ± 6.0*** |
| OBJECTIVE CI (n)/[]b | 35/[27]b | 13/[4]b |
| NPC (cm) | 13.3 ± 4.4 | 10.8 ± 5.2* |
| Horizontal phoria @ 6 m (∆) | 1.8 ± 2.8 | 1.9 ± 1.8 ns |
| Horizontal phoria @ 40 cm (∆) | 7.3 ± 4.0 | 8.1 ± 4.5 ns |
| Phoria @ 40 cm − phoria @ 6 m (∆) | 5.5 ± 2.3 | 6.3 ± 2.9 ns |
| PFV @ 40 cm (∆) | 5.2 ± 3.3 | 8.2 ± 3.9 ns |
| SYMPTOMATIC CI (n)/[]b | 25/[22]b | 6/[0]b |
| NPC (cm) | 14.5 ± 4.4 | 8.2 ± 1.0*** |
| Horizontal phoria @ 6 m (∆) | 2.1 ± 3.1 | 1.3 ± 1.6 ns |
| Horizontal phoria @ 40 cm (∆) | 7.4 ± 4.1 | 6.3 ± 2.8 ns |
| Phoria @ 40 cm − phoria @ 6 m (∆) | 5.3 ± 2.2 | 5.0 ± 1.6 ns |
| PFV @ 40 cm (∆) | 5.4 ± 3.4 | 8.9 ± 3.5 ns |
aGroup‐averaged horizontal phorias are “exophorias.”
bNumber of subjects if an NPC ≥ 10 cm criterion is used, rather than the NPC ≥6 cm criterion. See Discussion for details.
*P ≤ 0.05; ***P ≤ 0.001.
ns, not statistically significant.
Discussion
This study is the largest comprehensive analysis of CI in PD. The present results strengthen earlier reports by Repka et al.16 and Lepore,17 indicating a higher prevalence of subjective and objective CI in individuals with PD. They further indicate that not all CI‐like symptoms (subjective CI = 53.8%) result from CI (objective CI = 43.8%) in PD. Finally, our data show that more PD participants (31.3%) than controls (7.5%) have confirmed symptomatic CI.
These results add to the expanding list of nonmotor symptoms in PD,1 although it could be argued that CI can be interpreted as a “motor” symptom of PD. Nonetheless, the present study highlights the fact that visual symptoms are very prevalent in PD. Although double vision can be reported in PD, it is not the most prevalent visual symptom. Binocular vision anomalies are often accompanied by more subtle symptoms before double vision occurs. We found that only 14.3% of PD participants with objective CI experienced double vision “fairly often or always.” A person with CI may experience symptoms, such as fatigue, blurred vision, or tearing while reading, and choose to stop the activity because of the discomfort, thus avoiding potential double vision. Alternatively, individuals with CI may simply avoid any prolonged near work because of vague discomfort, without knowing why that is the case. This implies that tests like the NMSQuest, aimed at screening for nonmotor symptoms in PD,1 will likely miss many PD patients with visual symptoms, given that only the “double vision” item in the questionnaire relates to vision. Our results indicate that it could be advantageous to add another item, such as “eyes feel tired or uncomfortable while reading or doing close work,” to nonmotor screens to better identify PD individuals with vision problems.
The CISS questionnaire used to determine symptoms was originally developed and validated to serve as an outcome measure of treatment for individuals with objective CI.18, 20, 21 Although this questionnaire has not been validated in PD, it was used because it was the only published one available. It becomes clear from our results, however, that the CISS‐15 picks up a wide range of visual symptoms that may or may not be related to CI, and that it should be used in parallel to a complete eye exam if the intent is to link symptomatology with a diagnosis of CI.
Another point needs to be considered in relation to the diagnosis of CI. One criterion used here was the one published by the CITT group, that is, a receded NPC break of ≥6 cm.19, 22 Clinically, however, the classical criterion of a receded NPC break of ≥10 cm is more often used to judge CI in adults.23 If such a criterion had been used, keeping the other criteria the same, differences between PD and controls would have been even more dramatic; 27 participants with PD and 4 controls (P ≤ 0.001) would have been diagnosed with CI, rather than 35 and 13 (Table 2). Furthermore, 22 participants with PD and 0 controls (P ≤ 0.001) would have had symptomatic CI, rather than 25 and 6 (Table 2).
These results provide ample evidence to call for future research aimed at evaluating treatment for symptomatic CI in PD. Prism correction is fast to implement and quite effortless for the patient, but there is little evidence to support its efficacy.24 One study has published results from a presbyopic population,25 but none have been performed in PD. One clinical trial has shown that prisms were no more effective than placebo glasses in eliminating the signs and symptoms associated with CI in children.26 This is likely because prism correction works by realigning the target to match eye position without increasing the degree or amplitude of convergence. Hence, visual symptoms could reappear as soon as the working distance is modified or when the patient experiences any degree of fatigue. Moreover, the severity of CI fluctuates with levodopa fluctuations,27 creating a “moving target” for prismatic correction. Orthoptic treatment has long been accepted as the therapy of choice for symptomatic CI28, 29, 30 and has been listed as a modality of treatment for CI in PD patients.15 To our knowledge, however, it has never been attempted for CI in PD patients (see Fig. 1 for CI algorithm).
Figure 1.
CI algorithm.
One limitation is that the UPDRS ratings or H & Y staging were not available, so that we could not stage the severity of PD. This, however, does not change the results obtained in this study.
In conclusion, this study has shown that symptomatic CI is highly prevalent in individuals with PD. Future studies should evaluate the effectiveness of treatments for PD patients having symptomatic CI.
Author Roles
(1) Research Project: A. Conception, B. Organization, C. Execution; (2) Statistical Analysis: A. Design, B. Execution, C. Review and Critique; (3) Manuscript Preparation: A. Writing of the First Draft, B. Review and Critique.
E.L.I.: 1A, 1B, 3A, 3B
E.C.: 1B, 1C, 3B
C.L.: 1B, 1C, 2C, 3A, 3B
M.‐J.K.: 1A, 1B, 3B
B.‐S.L.: 1A, 2A, 2B, 2C, 3B
M.P.: 1A, 1B, 3B
R.P.: 1B, 3A, 3B
H.K.: 1A, 1B, 1C, 2C, 3A, 3B
Disclosures
Ethical Compliance Statement: We confirm that we have read the Journal's position on issues involved in ethical publication and affirm that this work is consistent with those guidelines.
Funding Sources and Conflicts of Interest: This study was supported by research grants from the Comité aviseur pour la recherche clinique (CAREC) at the Institut universitaire de gériatrie de Montréal (IUGM), the Canadian Institutes of Health Research (# 123462) and the Canadian Optometric Education Trust Fund. The authors report no conflicts of interest.
Financial Disclosures for previous 12 months: E.L.I. received grants from Canadian Optometric Education Trust Fund, Natural Sciences and Engineering Research Council, Canadian Institute of Health Research, College of Optometrists in Vision Development, and University of Waterloo Research Incentive Fund. E.C. received a grant from the Comité aviseur pour la recherche clinique (CAREC) at the Institut universitaire de gériatrie de Montréal (IUGM). M.‐J.K. received grants from the Fonds de la Recherche en Santé Québec‐Fonds d'innovation Pfizer sur la maladie d'Alzheimer et les maladies apparentées, the Canadian Institute of Health Research and the Canadian Consortium on Neurodegeneration in Aging, the Comité aviseur pour la recherche clinique (CAREC) at the Institut universitaire de gériatrie de Montréal (IUGM) and the Alzheimer Society of Canada. B.‐S.L. received grants from the Fonds de recherche du Québec–Société et culture, the Canadian Institute of Health Research, the Social Sciences and Humanities Research Council of Canada, the ARIMA research partnership, the Centre de recherche et de partage des savoirs InterActions of the CIUSSS du Nord‐de‐l’île‐de‐Montréal, and the Alzheimer Society of Canada, as well as grants and contracts from charity and nonprofit organizations. M.P. is on the advisory board of Merz and Allergan and has research support from Medtronic. R.P. received grants from the Fonds de la Recherche en Santé Québec, the Canadian Institute of Health Research, the Parkinson Society, the Weston‐Garfield Foundation, and the Webster Foundation, as well as funding for consultancy from Biotie, Biogen, and Roche and speaker fees from Novartis Canada and Teva Neurosciences. H.K. received grants from Canadian Optometric Education Trust Fund, Comité aviseur pour la recherche clinique (CAREC) at the Institut universitaire de gériatrie de Montréal (IUGM), Natural Sciences and Engineering Research Council, Canadian Institute of Health Research, and the Alzheimer Society of Canada.
Supporting information
Table S1. Occurrence/severity of the most and least frequent symptoms in participants having subjective CI, objective CI, and symptomatic CI.
Relevant disclosures and conflicts of interest are listed at the end of this article.
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Associated Data
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Supplementary Materials
Table S1. Occurrence/severity of the most and least frequent symptoms in participants having subjective CI, objective CI, and symptomatic CI.