Sustained Gazing Causes Measurable Decline in Visual Function of Patients with Dry Eye





Purpose


To assess the effects of sustained gazing on visual function of dry eye patients.


Design


Prospective, comparative before-and-after study.


Methods


A total of 176 patients with dry eye and 33 control subjects ≥50 years old were included. Dry eye symptomatology along and clinical parameters were assessed. Out-loud reading speed was measured using the International Reading Speed Test (IReST) as words per minute (wpm). Reading speed was repeated using different IReST excerpts following 30-minute silent reading.


Results


At baseline, there were no differences between dry eye patients and control subjects with respect to reading speed (172 vs 180 wpm, respectively; P = 0.21) or the time to read the excerpt (33 vs 30 seconds, respectively; P = 0.17). After silent reading, the dry eye patients had decreased reading speed and increases in the length of time to read the passage compared to baseline (161 vs 172 wpm, respectively; P = 0.002; and 38 vs 33 seconds, respectively; P < 0.001). The control subjects did not show significant differences for either parameter. There were significant differences with respect to both parameters between the dry eye and control groups after sustained gazing (161 vs 188 wpm, respectively; P = 0.006; and 38 vs 31 seconds, respectively; P = 0.003). Each 1-point increase in baseline corneal staining score (0-6) led to a 5-wpm reduction in reading speed (95% confidence interval, −8 to −1; P = 0.01).


Conclusions


Sustained gazing, such as in silent reading, has a measurable negative impact on visual performance of dry eye patients. Corneal staining represents a clinical parameter relevant to visual function.


Highlights





  • There were no differences in reading speed between dry eye and control patients at rest.



  • However, dry eye patients demonstrated decreased reading speed after sustained gazing.



  • This worsening of reading speed is correlated with severity of baseline corneal staining.



Although dry eye is often under-recognized and under-appreciated, it is a growing public health concern affecting up to 30% of the population over the age of 50 years. , The impact of dry eye on quality of life can be substantial due not only to ocular discomfort but also blurred or fluctuating vision and eye fatigue. Visual disturbance caused by dry eye can interfere with many everyday activities. Patients with dry eye frequently complain of difficulty with visual tasks that require sustained gazing such as reading a newspaper, driving, or performing computer-related work, even when they have perfect visual acuity. Indeed, one of the most bothersome symptoms that patients with dry eye experience is difficulty with reading, which is undetectable by conventional vision testing in clinical setting. The present authors previously demonstrated a reduction in reading speed in patients with dry eye compared to age-matched control subjects by using a prolonged silent reading test but not with short text passages. Few other studies also assessed reading function in patients with dry eye. These studies used different reading tests in patients with varying degrees of dry eye severity based on several evaluation methods and reported varying results.


A stable tear film and a smooth corneal epithelium are essential for an optically ideal ocular surface. Visual tasks requiring sustained gazing can disrupt the tear film, eventually degrading visual function. We showed that silent reading for as short as 30 minutes causes alterations of the tear film and ocular surface with a significant increase in corneal staining. In fact, this silent reading task was proposed as a desiccating “ocular surface stress test” by others as it was able to demonstrate measurable changes in ocular surface and tear film parameters. This study sought to quantify the impact of sustained gazing on visual performance of patients with dry eye.


Subjects and Methods


Patients


This prospective, comparative before-and-after clinical study was approved by the Johns Hopkins University Institutional Review Board in accordance with the Declaration of Helsinki. Patients with an established dry eye diagnosis (regardless of severity at the time of enrollment) and who were over the age of 50 years were recruited from the Ocular Surface Diseases and Dry Eye Clinic at the Wilmer Eye Institute, the Johns Hopkins University, Baltimore, Maryland, whereas friends or family members of similar ages, as well as volunteers with no previous diagnosis or symptoms of dry eye were enrolled as control subjects.


Individuals with binocular vision below 20/25, self-reported illiteracy or language problems, contact-lens wearers, and individuals who had had any ocular surgery in the preceding 3 months were not included. Participants did not use any prescription eye drops (including topical cyclosporine, steroids, and antiglaucoma eye drops) for at least 30 days prior to the study visit. Participants using over-the-counter artificial tears were enrolled but were instructed to not use any of the drops for at least 24 hours prior to the study visit.


Measurement of Covariate Data


After an informed consent according to the Health Insurance Portability and Accountability Act were obtained from subjects, subjects were assessed in the order listed here. They were first queried for their demographic information, including last grade completed to assess their education level. Part D of the General Health Questionnaire (Mood Questionnaire) was administered to evaluate depressive symptoms, and Mini-Mental State Examination was administered to assess cognitive ability.


Evaluation of Vision-Related and Dry Eye Measurements


Dry eye-related symptoms were evaluated first by using the Ocular Surface Disease Index (OSDI) questionnaire. A total OSDI score ranging from 0 to 100 (according to the 2004 Walt J. OSDI Administration and Scoring Manual) (Allergan, Inc., Irvine, California.) and 3 subscores: ocular symptoms subscore (questions 1 to 5), vision-related function subscore (questions 6 to 9), and environmental triggers subscore (questions 10 to 12), each ranging from 0 to 100, were calculated as previously described. Distance visual acuity was then measured using the Early Treatment Diabetic Retinopathy Study chart under binocular conditions with the subjects’ habitual distance correction, if any, and transformed to the logarithm of the minimum angle of resolution (logMAR) for statistical analysis. Contrast sensitivity was measured using the Mars Contrast Sensitivity Test Chart (Mars Perceptrix Corp, Chappaqua, New York). A contrast sensitivity level more than 1.50 was considered normal. The Minnesota Low-Vision Reading (MNRead) chart was used to measure the reading acuity and the critical print size.


Dry eye tests were then performed, with 10-minute intervals between tests, in the order mentioned here. The Tear Stability Analysis System incorporated into the Tomey Top-Ref-Keratometer RT-7000 (Tomey, Phoenix, Arizona) corneal topography machine was used to measure tear break-up time. Schirmer’s testing was performed without anesthesia, using sterile strips (Tear Flo; Sigma Pharmaceuticals, Monticello, Iowa), and the length of paper wetting was measured after 5 minutes.


Ocular surface staining was then graded according to Sjögren’s International Collaborative Clinical Alliance grading system. Conjunctival staining was evaluated first by using a neutral density filter over the light source immediately after instillation of lissamine green dye (Green-Glo; HUB Pharmaceuticals, Rancho Cucamonga, California). The nasal and temporal conjunctiva were graded separately with a maximum score of 3 for each area. Corneal staining was evaluated next using the cobalt blue filter at least 2 minutes after instillation of fluorescein dye (Ful-Glo; Akorn, Lake Forest, Illinois). The maximum possible fluorescein score (the punctate epithelial erosions grade plus any extra points for modifiers [central corneal staining, confluent staining, and filaments]) was 6 for each cornea. The total possible maximum ocular staining score, derived by summing the corneal and conjunctival scores, was 12 for each eye.


A visual analog scale was then used for assessment of visual fatigue immediately before reading tests were performed. Participants were instructed to mark a point on a 10-cm scale with markings from 0 to 10, indicating the level of visual fatigue experienced as follows: “If 0 indicates no tiredness and 10 indicates maximum tiredness, what number will you choose to indicate how your eyes feel now?” Participants were specifically instructed not to consider physical fatigue and consider only “tiredness of the eyes.”


Evaluation of Reading


Reading was evaluated using a 77-word International Reading Speed Test (IReST) excerpt. Testing was performed with participants wearing their habitual near-correction spectacles and holding the reading material at a comfortable distance in a room with standardized lighting, with a luminance between 400 and 600 lux. Participants were asked to read the IReST excerpt out loud, fluently, and without correcting mistakes. Reading time was measured in seconds by using a stopwatch. Reading speed was calculated as words per minute (wpm). Details regarding the administration of the reading test and calculation of the reading speed are provided elsewhere. The normal lower reference value for reading speed using the IReST was considered to be 161 wpm, and the clinically significant difference in reading speed to be 10 wpm.


Sustained Gazing Task


A previously validated reading passage that consisted of 7,300 words was used as a sustained gazing task. This task was previously proposed as an “ocular surface stress test.” The passage takes 30 minutes on average to complete. Participants who completed the reading task in less than 20 minutes or who were unwilling to finish reading were excluded from the analysis.


Following the sustained gazing task, repeated out-loud reading speed was measured by using a different 77-word IReST excerpt, followed by visual fatigue assessment, distance visual acuity, and contrast sensitivity measurements in the order mentioned here.


Statistical Methods


The results of the eye with worse corneal staining at baseline were used for the statistical analyses for the tests performed in both eyes, such as break-up time, Schirmer’s testing, and ocular surface staining. In cases with equal corneal staining scores in both eyes, total ocular surface staining score at baseline was considered. The t -test was used to compare the continuous variables, and the chi-square test was used to compare categorical variables between groups. The paired t -test was used to compare before and after observations within the study groups. Linear regression analysis after controlling for age and sex was performed to identify group and dry-eye related predictors of reading speed. Additionally, subgroup analyses were performed based on the contrast sensitivity levels and normal baseline reading speed. Values of P < 0.05 were considered statistically significant. All statistical analyses were performed using SPSS version 23 software (IBM, Armonk, New York).




Results


A total of 224 subjects consented to enroll in the study; 13 (8 with dry eye and 5 control subjects) completed the silent reading task in less than 20 minutes and were excluded. Additionally, 2 subjects who did not complete the second IReST reading test (1 with dry eye and 1 control subject) were excluded. The remaining 209 subjects (176 dry eye patients and 33 control subjects) were included in the analyses. The sociodemographic characteristics, vision-related measurements, and dry eye parameters of the study population are shown in Table 1 . A greater proportion of patients with dry eye had depressive symptoms than control subjects (31% vs 12%, respectively; P = 0.03). Among the vision measurements, distance visual acuity, reading acuity, and critical print size were similar between the 2 groups ( P > 0.05 for all). However, contrast sensitivity levels were significantly lower in patients with dry eye than in control subjects (1.61 vs 1.67, respectively; P = 0.01). Additionally, patients with dry eye were more symptomatic, with higher OSDI scores, and had significantly worse tear film and ocular surface parameters than control subjects ( P < 0.05 for all), with the exception of Schirmer’s test results ( P = 0.12).



Table 1

Demographic and Clinical Characteristics of Participants According to Dry Eye Status a











































































































































Dry Eye (n = 176) Controls (n = 33) P Value
Demographics
Age, y 63.2 ± 8.3 60.6 ± 8.0 0.10
Female 131 (74%) 22 (68%) 0.35
Education, y 15.3 ± 2.1 15.2 ± 2.3 0.83
Depressed mood 54 (31%) 4 (12%) 0.03
MMSE score 25.4 ± 1.0 25.2 ± 1.1 0.34
Vision measures
Visual acuity, logMAR −0.04 ± 0.10 0.00 ± 0.11 0.07
Contrast sensitivity, log 1.61 ± 0.12 1.67 ± 0.10 0.01
MNRead reading acuity, logMAR 0.03 ± 0.14 0.02 ± 0.10 0.92
Critical print size, logMAR 0.16 ± 0.13 0.14 ± 0.16 0.59
Dry eye measures
Total OSDI score, 0-100 31.8 ± 22.1 4.2 ± 4.4 <0.001
Discomfort-related subscore 33.5 ± 22.8 6.0 ± 7.3 <0.001
Visual function-related subscore 25.9 ± 24.7 1.6 ± 4.0 <0.001
Environmental trigger subscore 37.3 ± 31.0 4.9 ± 8.2 <0.001
Reading difficulty reported 105 (61%) 2 (6%) <0.001
Tear break-up time, s 3.6 ± 3.5 5.3 ± 3.7 0.02
Schirmer’s test, mm 12.8 ± 9.1 15.6 ± 9.8 0.12
Total corneal staining, 0-6 2.3 ± 1.7 0.5 ± 0.8 <0.001
Corneal staining, 0-3 1.7 ± 1.2 0.5 ± 0.8 <0.001
Central staining present 43 (24%) 0 0.001
Confluent staining present 52 (29%) 1 (3%) 0.001
Filament present 6 (3%) 0 0.59
Total conjunctival staining, 0-6 2.2 ± 2.1 0.6 ± 1.2 <0.001
Total ocular surface staining, 0-12 4.5 ± 3.3 1.1 ± 1.6 <0.001

logMAR = logarithm of the minimum angle of resolution; log = logarithm; MMSE = Mini-Mental State Examination; MNRead = Minnesota low-vision reading test; OSDI = Ocular Surface Disease Index.

P values in bold indicates statistical significance ( P < 0.05).

a Results are represented as mean ± SD for continuous variables and number (percentage) for binary variables. The t test was used for comparison of continuous variables between groups and chi-squared test for categorical variables.



Table 2 demonstrates a comparison of reading and vision parameters at baseline and after prolonged silent reading. At baseline, there were no differences between patients with dry eye and control subjects with respect to reading speed, time to read the excerpt, visual acuity, or visual fatigue. After the silent reading task, the dry eye patients had a significantly slower reading speed (161 vs 172 wpm, respectively; P = 0.02) and longer reading duration (38 vs 33 seconds, respectively; P < 0.001) than at baseline. Control subjects did not show any change with respect to either parameter ( P > 0.05). In addition, following silent reading, the difference between the patients with dry eye and the control subjects with respect to both reading speed (161 vs 188 wpm; P = 0.006), and the duration of reading (38 vs 31 seconds, respectively; P = 0.003) became statistically significant.



Table 2

Comparison of Reading and Vision Parameters at Baseline and after Sustained Gazing






































































































































Dry Eye (n = 176) Controls (n = 33) P Value
Reading speed, wpm
Baseline 172 ± 35 180 ± 28 0.21
After sustained gazing 161 ± 50 188 ± 51 0.006
P value, baseline vs. after sustained gazing 0.002 0.28
Change from baseline −11 ± 47 7 ± 39 0.03
Duration of reading test, s
Baseline 33 ± 10 30 ± 5 0.17
After sustained gazing 38 ± 16 31 ± 10 0.003
P value, baseline vs. after sustained gazing <0.001 0.68
Change from baseline 9 ± 18 4 ± 9 0.02
Visual fatigue score, 0-10
Baseline 2.4 ± 2.4 1.5 ± 2.0 0.06
After sustained gazing 4.2 ± 2.8 2.9 ± 2.8 0.02
P value, baseline vs. after sustained gazing <0.001 0.001
Change from baseline 1.8 ± 2.3 1.4 ± 2.1 0.33
Visual acuity, logMAR
Baseline −0.04 ± 0.10 0.00 ± 0.11 0.07
After sustained gazing −0.02 ± 0.11 0.02 ± 0.14 0.10
P value, baseline vs. after sustained gazing <0.001 0.24
Change from baseline 0.04 ± 0.13 0.03 ± 0.17 0.83
Contrast sensitivity, log
Baseline 1.62 ± 0.12 1.67 ± 0.10 0.01
After sustained gazing 1.64 ± 0.12 1.69 ± 0.10 0.02
P value, baseline vs. after sustained gazing <0.001 0.11
Change from baseline −0.01 ± 0.46 0.02 ± 0.07 0.70

wpm = words per minute.

Results are represented as mean ± standard deviation. The t test was used for comparison of continuous variables between groups and paired t-test for comparison of repeated measures.

P values in bold indicates statistical significance ( P < 0.05).


Visual fatigue increased in both dry eye patients (4.2 vs 2.4, respectively; P < 0.001) and in control subjects (2.9 vs 1.5, respectively; P = 0.001) following the silent reading task. In addition, although mean visual fatigue scores were not significantly different between the dry eye and control groups at baseline ( P = 0.06), the difference became significant following silent reading (4.2 vs 2.9, respectively; P = 0.02). The distance visual acuity was not statistically different within and between the patients with dry eye and control subjects both at baseline and following the silent reading task ( P > 0.05 for all). The contrast sensitivity levels were significantly lower in dry eye patients than in control subjects both at baseline and following the prolonged silent reading ( P < 0.05 for both), although the differences were not clinically meaningful (1.5 and above is considered normal).


To evaluate associations between vision and dry eye parameters at baseline and change in reading speed following the prolonged silent reading, linear regression analyses were performed after controlling for age and sex ( Table 3 ). Contrast sensitivity was an independent predictor of reduction in reading speed (138-wpm change for each log unit; 95% confidence interval [CI], 84-193; P < 0.001), but visual acuity was not ( P > 0.05). The subjective and objective measurements of dry eye also were individually tested. Among dry eye measurements, corneal staining was the only measurement associated with a significant decreases in reading speed after silent reading. For every 1-point increase in corneal staining score (0-6), participants read 5 wpm slower following silent reading task (95% CI, −8 to −1; P = 0.01).



Table 3

Multivariate Analysis of Baseline Parameters as Predictors of the Change in Reading Speed Following Sustained Gazing


























































Change in Reading Speed after Sustained Gazing
wpm Change (95% CI) P Value
Vision Measures
Visual acuity, logMAR −44.9 (-104.6 to 14.7) 0.14
Contrast sensitivity, log 138.3 (83.7 to 192.9) <0.001
Visual fatigue score, 0-10 2.3 (−0.7 to 5.2) 0.13
Total OSDI score, 0-100 −0.1 (−0.4 to 0.1) 0.38
Discomfort-related subscore −0.1 (−0.4 to 0.1) 0.34
Visual function-related subscore −0.1 (−0.3 to 0.2) 0.58
Environmental trigger subscore −0.05 (−0.3 to 0.2) 0.62
Tear break-up time, seconds 0.3 (−1.5 to 2.2) 0.70
Schirmer’s test, mm 0.3 (−0.4 to 1.0) 0.35
Corneal staining (0-6) −4.6 (−8.4 to −0.9) 0.01
Conjunctival staining (0-6) −1.0 (−4.1 to 2.0) 0.50

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Mar 14, 2020 | Posted by in OPHTHALMOLOGY | Comments Off on Sustained Gazing Causes Measurable Decline in Visual Function of Patients with Dry Eye
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