Ridder, William H. III*; Zhang, Yi†; Huang, Jing-Feng†
Dry eye disease (DED) is a disorder of the tear film and ocular surface and is one of the most prevalent ocular conditions that affects as much as 20% of the American population at least some of the time.1 The most recent definition of DED, arising from the 2007 International Dry Eye Workshop (DEWS), states that “Dry eye is a multifactorial disease of the tears and ocular surface that results in symptoms of discomfort, visual disturbance, and tear film instability, with potential damage to the ocular surface. It is accompanied by increased osmolarity of the tear film and inflammation of the ocular surface.”2 This article will focus on the “visual disturbance” component of DED.
Patients with DED often complain of blurred vision, although their best corrected visual acuity (BCVA) is normal when examined with the Snellen chart. It has been suggested that the blurred vision of DED patients may be the result of the decreased tear breakup time (TBUT) causing an irregular tear film.3–8 The tear film is the outermost surface in the optical path for the eye, and an intermittent irregular tear film can result in transient visual defects. This explains why DED patients have normal acuity on Snellen charts that allows extended viewing durations, but with appropriate stimulus conditions, they demonstrate decreased contrast sensitivity.6
Visual disturbances and ocular discomfort caused by DED can interfere with many everyday activities. Miljanović et al.9 examined 589 subjects, 190 (32.3%) of whom had DED, who were enrolled in the Women’s Health Study10 or the Physicians’ Health Study.11 Their study results, based on surveys, indicated that people with DED have a high incidence of reading difficulty. They used a supplemental questionnaire to determine the extent to which eye problems limited the subjects’ ability to read, drive, work at the computer, perform professional activities, and watch television compared with subjects who did not have DED. They showed that after controlling for factors such as age, diabetes, and hypertension, patients with DED were significantly more likely to report limitations in their ability to carry out these activities. The odds ratio for increased likelihood of difficulties caused by DED was the highest for reading (odds ratio, 3.64; 95% confidence interval, 2.45 to 5.4; p < 0.0001). However, these subjective reports of reading difficulty by DED patients have not been evaluated directly with reading tests.
Legge12 has proposed that visual abnormalities, in general, would most likely affect reading rate. The transient visual problems experienced by DED patients would then be expected to reduce reading speed, which is an indirect measure of eye movements during reading. This may occur because reading involves the coordinated interaction of saccades and brief fixations. During these brief fixations, the visual information is encoded. The transient irregular tear film in DED patients can interfere with encoding the visual information during these brief fixations. This could result in longer fixations, shorter saccade lengths, more saccades, or regressions during reading. These alterations in reading behavior would decrease reading speed. The primary purpose of this study was to determine if DED patients exhibit decreases in their reading speed and contrast sensitivity. A second purpose for this study was to examine the association between DED symptoms and objective clinical signs with reading speed and contrast sensitivity.
This was a prospective, nondrug, nonrandomized study enrolling a total of 120 subjects distributed into four groups: a control group (i.e., no DED) and mild, moderate, and severe DED groups (Table 1). A total of 48 subjects were excluded based on the exclusion criteria below (i.e., acuity poorer than 0.1 log of the minimum angle of resolution (logMAR) and the presence of media opacities or ocular disease other than dry eye). Two clinical sites were selected for subject recruitment (Sall Medical Research Center, Inc., Artesia, Calif, and Total Eye Care, P.A., Memphis, Tenn), and each site enrolled approximately one-half of the number of subjects in each of the four groups. This study was conducted in compliance with the ethical principles originating in or derived from the Declaration of Helsinki and in compliance with the International Conference on Harmonization Good Clinical Practice Guidelines.13 The study protocol was approved by the institutional review boards and/or independent ethics committee of each study center. All patients provided written informed consent.
Main Inclusion/Exclusion Criteria
All subjects in this study had to be at least 18 years old (male or female) with BCVA of at least 0.1 logMAR or 20/25 Snellen (Table 1). Each subject had a complete ophthalmological examination to rule out the presence of ocular disease other than DED. A total of 72 subjects (see below for group breakdown) who met the criteria described here were included in the study. Subjects enrolled in the control group could not have a history of self-reported dry eye symptoms during the past 6 months or a history of regular artificial tear use or punctal occlusion to relieve the symptoms of DED. The DED subjects had to have dry eye symptoms with an Ocular Surface Disease Index (OSDI) score of at least 20 and meet the criteria for mild, moderate, or severe DED based on the following criteria. The corneal fluorescein staining (National Eye Institute [NEI] Scale) score from the worse eye (i.e., the study eye) of each subject was used for subject grouping.14 The NEI workshop divided the cornea into five sectors, and each sector was graded on a 0 to 3 scale for staining. Thus, total corneal staining ranged from 0 to 15. At the screening visit, subjects were stratified into four groups:
* Control group (OSDI <13 and no corneal staining), n = 20
* Mild DED (OSDI ≥20 and total corneal staining score <4), n = 17
* Moderate DED (OSDI ≥20 and total corneal staining score 4 to 7), n = 22
* Severe DED (OSDI ≥20 and total corneal staining score >7), n = 13.
Subjects were excluded from the study if they had:
* active ocular infection or active allergic conjunctivitis
* temporary punctal plugs or permanent occlusion of lachrymal puncta within 1 month of enrollment
* used any medication indicated to increase tear production within 30 days of the screening visit or during the study
* been diagnosed as having glaucoma or used any glaucoma medication within 2 months of enrollment or
* undergone laser refractive surgery within 12 months or any other ocular surgery within 6 months of enrollment (e.g., corneal transplant recipient)
* had YAG laser capsulotomy within 3 months of enrollment
* exhibited media opacities
* had retinal disease (i.e., age-related macular degeneration, diabetic retinopathy, etc).
Subjects were able to read and understand English sufficiently to complete the symptom questionnaires unassisted. Stable use of oral medications designed to treat blepharitis was permitted.
A screening visit determined if the subjects were eligible for the study. Subjects first completed three questionnaires (i.e., the OSDI,15 the 25-item version of the National Eye Institute Visual Functioning Questionnaire,16 and the Ocular Comfort Index17) and a reading test. This was followed by a complete examination of both eyes in the following sequence: visual acuity (BCVA with the Early Treatment Diabetic Retinopathy Study [ETDRS] logMAR chart), contrast sensitivity, tear osmolarity, slit lamp examination, Schirmer w/o anesthesia, fluorescein TBUT (average of three repeats), and fluorescein corneal staining. The BCVA was determined with the letter-by-letter method. The tear osmolarity (average of three readings) was determined with the TearLab Osmolarity Test (TearLab Corp., San Diego, Calif). The reading speed was determined using the Wilkins Rate of Reading test kit to measure correct words read per minute following the instructions provided by the manufacturer.18 The Wilkins Rate of Reading test consists of simple words that have no context. The subject reads the words aloud, and their time and errors are recorded. Contrast sensitivity was measured using the Holladay Automated Contrast Sensitivity System (M&S Technologies, Inc., Park Ridge, Ill). The contrast sensitivity and reading tests were performed to familiarize the subjects with the test and minimize any differences in the final data based on a learning effect. Previous studies for the reading test suggested that the learning or practice effect is minimal after the first administration.18,19 The subjects were then placed in one of the four groups (i.e., control, mild, moderate, or severe DED). The study data reported here were collected on a visit that was within 3 days of the screening visit. All subjects underwent the same evaluation that was carried out at the screening visit, followed by conjunctival lissamine green staining (Oxford Scale).20 The subject group data are displayed in Table 1.
For data collected from both eyes, the eye from which the stratification was based (the worse eye, study eye) was used for statistical analyses. Statistical significance was set at a level of p < 0.05 (two-sided). As the study was exploratory in nature, values of p were not adjusted for multiple end points or multiple comparisons. The data were analyzed with an analysis of covariance (ANCOVA) model, with age, sex, study site, and group included as independent variables in the model. Pairwise group comparisons were also conducted with the ANCOVA model. A partial correlation coefficient controlling for the age imbalance among the groups, calculated as the Pearson correlation between the residuals from linear regressions of each of the two factors of interest versus age, was used to evaluate the linear relationship between reading speed, contrast sensitivity area under the curve (AUC), and dry eye clinical signs and symptoms.
The ANCOVA model indicated that the subject selection criteria resulted in the OSDI scores being significantly different between control and all DED groups (all values of p < 0.05, Table 1); and corneal staining scores being significantly different for all groups (all values of p < 0.05). The TBUT was significantly shorter for the moderate and severe DED patients than that in the control subjects (both values of p < 0.05). The TBUT was significantly different between the mild and severe DED groups (p = 0.05). The Schirmer test results were greater for the mild DED group than the other groups (all values of p < 0.05). The osmolarity was higher for the moderate and severe DED patients than the control subjects (both values of p < 0.05) and approached significance when the mild and moderate DED groups were compared (p = 0.059).
The logMAR visual acuities of the subject groups are not statistically different (Table 1, all values of p > 0.05). This observation agrees with previous measures of acuity with this test for DED and control subjects.6 Because the acuities are the same across subject groups, this could not account for any differences in contrast sensitivity or reading ability between the control and DED subjects.
The contrast sensitivity data for the different groups are displayed in Fig. 1. Spatial frequency in cycles per degree is displayed on the horizontal axis, and contrast sensitivity (the inverse of contrast threshold) is displayed on the vertical axis. The data at each spatial frequency were assessed. There were no significant differences between the groups found at any spatial frequency (all values of p > 0.05). The AUC was also assessed for differences between the control and DED subjects. No statistically significant differences were identified (all values of p > 0.05). Thus, the DED and control subjects do not have significant differences in acuity or contrast sensitivity for tests that allow extended viewing times of the stimuli.
The control subjects have an average reading speed of 163 ± 34.8 (mean ± SD; range, 96 to 238.4) words per minute. The DED subjects have an average reading speed of 134 ± 30.9 (mean ± SD; range, 47 to 194) words per minute. As a single group, the DED subjects have a statistically significant decrease in reading speed compared with that in the control group (p = 0.046, r2 = 0.2) even after accounting for the imbalance of age among subject groups. The adjusted mean reading speed derived from the ANCOVA model is 158.3 ± 8.44 (mean ± SE) words per minute for the control subjects as compared with 134.9 ± 4.95 words per minute for the DED subjects. When the DED subjects are divided up based on corneal staining and compared with the control subjects, the adjusted mean reading speed in the severe DED group (127.0 ± 9.63 words per minute) is found to be significantly slower than that in the control group (158.3 ± 8.44 words per minute, p = 0.03; Fig. 2). The subject group is shown on the horizontal axis, and the adjusted mean reading speed is plotted on the vertical axis in Fig. 2. The decrease in reading speed with increasing corneal staining severity suggests a trend (p = 0.16). The moderate DED group (136.8 ± 7.15 words per minute) approaches significance (p = 0.07), and the mild DED group (141.0 ± 7.96 words per minute) is not significantly different (p = 0.14) from the control group.
Most DED patients have a mild or moderate condition with some corneal staining, and they exhibit transient fluctuations in vision. To determine if central corneal staining affects reading speed, the DED subjects were divided into two groups: those with central corneal staining and those with only peripheral corneal staining (Fig. 3). To be included in the central corneal staining group, the DED subjects had to have a central corneal staining score of 1.0 or higher. In Fig. 3, the groups are shown on the horizontal axis, and the adjusted reading speed is shown on the vertical axis. The DED subjects with central corneal staining (131.4 ± 7.15 words per minute) have a statistically reduced reading speed compared with that in the control subjects (p = 0.03). The DED subjects with peripheral corneal staining (139.9 ± 6.38 words per minute) approached significance (p = 0.09).
Partial correlations between contrast sensitivity (AUC) and reading speed with DED symptoms (i.g., from the OSDI, the 25-item version of the National Eye Institute Visual Functioning Questionnaire, and the Ocular Comfort Index) and clinical objective signs (i.e., corneal staining, conjunctival staining, TBUT, Schirmer test without anesthesia, and tear osmolarity) were determined from linear regression analysis and, as shown in Table 2, the highest correlation (−0.345) found was between reading speed and corneal staining, suggesting that as the corneal staining increases, the reading speed decreases.
In this prospective study, visual function was measured in control and DED subjects, and correlations with patient-reported DED symptoms and clinically measured objective signs were made. The DED patients had reduced reading speeds compared with the control subjects, and there seemed to be a trend of lower reading speed as DED severity, defined by corneal staining scores, increased. Consistent with that, the highest correlation was found between corneal staining and reading speed, although the correlations between the DED signs and symptoms are low. Previous studies have demonstrated this poor relationship between the signs and symptoms of DED.21–25 The difference in reading speed between the control and DED subjects was observed after adjusting for the potential confounding effects of age imbalance.
The control and DED groups did not have any significant differences in acuity or contrast sensitivity. Based on the case history, ophthalmological examination, normal contrast sensitivity, and normal acuity, the DED subjects did not have any ocular abnormalities other than the dry eye. These observations suggest that any reading speed differences observed are not the result of a sensory deficit.
As a group, the DED subjects had slower reading times than those in the control subjects (p = 0.046). The control subjects had an average reading speed of 163 ± 34.8 (mean ± SD) words per minute. These rates are comparable to previous reports of reading speed in young adults.26,27 Evans and Joseph27 reported an average reading speed on this test for 100 college students of 162.1 (SD, 36.0) words per minute. Firth et al.26 reported an average reading speed of 164.7 (SD, 28.8) words per minute for 30 normal subjects with an average age of 20.3 years. The DED subjects had an average reading speed of 134 ± 30.9 (mean ± SD) words per minute. When the DED subjects were stratified by corneal staining, with higher staining scores indicating more severe disease, only the severe DED subjects exhibited a significant reading speed deficit compared with control subjects.
Severe DED patients may have more extensive corneal staining that results in a continuous decrease in acuity and contrast sensitivity.28–30 This may be the result of an irregular corneal epithelium that distorts the light rays as they pass through the cornea. If the damaged epithelium causes distortion of the image projected on the retina, then central corneal staining may have a greater effect than peripheral corneal staining on reading speed. In our study, the reading speed results were similar when the DED subjects were segregated based on severity as defined by total corneal staining score or based on central/peripheral corneal staining. The reading speed for the severe DED group (127.0 words per minute) was slightly lower than the central corneal staining group (131.4 words per minute). The two groups were examined to determine if this similarity is the result of the same DED subjects being in both groups. A significant number of the same subjects were found in both groups (χ2, p < 0.001). This finding is consistent with the clinical observation that more severe DED patients tend to have central corneal staining (see table 5 in Behrens et al.31). For this population of DED subjects, as the dry eye severity increases, the central corneal staining severity increases. Thus, it is not possible to state that central corneal staining alone results in the decreased reading rate. There may be some other aspect of the dry eye (i.g., the transient tear layer disruption) that causes the decreased reading speed.
In addition to the dry eye, there are several other factors, such as age, English proficiency, cognitive function, and other health conditions unrelated to vision, that could also result in the lower reading rates for the DED subjects. The effect of age on reading speed is not clear in the literature. Some studies have found an age effect,32–34 where others have not.35,36 Akutsu et al.35 compared the reading speed of a young (mean age, 21.6 years) and an old (mean age, 67.8 years) age group. Both groups had reading speeds more than 300 words per minute and were not significantly different. However, a study from the same laboratory did find a difference in reading speed between young and old readers.36 This laboratory has hypothesized that the discrepancy in the literature may result from subtle subclinical abnormalities in the older population.12 The control subjects in the present study have a lower average age than the DED subjects, thus, it is possible that the older age of the DED subjects resulted in the lower reading speeds because of undetected sensory, motor, or cognitive deficits caused by age.
However, the effect of the age difference across the subject groups was accounted for in the statistical analysis by including age as a covariate in the ANCOVA model. The age factor was not significant (p = 0.31) in the ANCOVA model for reading speed, whereas subject group was a significant factor for reading speed (p = 0.046). Nonetheless, because there was not a large overlap in ages between the subject groups, future studies should age match the subject groups to eliminate this possible confounding variable in the final analysis. Race was not included in the final analysis because of the small sample size. When race was evaluated in the ANCOVA model, its effect was not significant (p = 0.23, data not shown in the Results).
Proficiency in the English language could also result in a reading rate difference between the control and DED subjects. English proficiency, IQ, and education level were not determined in this study. However, all subjects were required to read and complete the symptom questionnaires and the subject consent form unassisted. The subject’s reading speed was determined with the Wilkins Rate of Reading test. This test consists of 15 randomly arranged words per line, and the same 15 words are repeated for each line. The words were taken from a set of 110 common words found in children’s books and the Flesch-Kincaid grade level for the 15 words was 3.37,38 Because the reading difficulty of the test is at a third grade level, the reading rate difference between the control and DED subjects is unlikely the result of differences in English proficiency. However, it is possible that the older subjects in the DED group had a lower IQ, had cognitive abnormalities, or had subtle undetected health problems resulting in the lower reading rate.
The specific cause of the decreased reading speed in the DED patients is not known. Reading requires the coordinated interaction of saccades and brief fixations. The visual information acquired during reading is encoded during these brief fixations. Because the DED subjects had normal acuity and contrast sensitivity and did not seem to have other ocular diseases, these variables should not affect reading speed. The decreased reading speed may be the result of the abnormal tear film in the DED subjects. The abnormal tear film and decreased TBUT of the DED subjects may limit the time during which visual information can be encoded during a fixation. The DED subjects may compensate for the visual effects of the abnormal tear film by (1) increasing their blink frequency to reform the tear film, (2) having longer fixation times to encode the information, or (3) making more regressions during reading. Blink rate measured manually in this study was higher in the severe group compared with those in the control, mild DED, or moderate DED groups, although not statistically significant (data not shown). All of these compensations would decrease the reading speed. Future studies that monitor eye movements during reading in DED subjects will be necessary to determine if any or all of the above variables result in the slower reading speeds. Findings from this study, however, suggest that clinical reading tests such as the Wilkins Rate of Reading test may be used to monitor treatment effectiveness in DED patients. This would provide an objective indicator of functional improvement in these patients.
This is the first report, to the best of our knowledge, measuring and comparing reading speed in control subjects and DED patients of different disease severities, which was prospectively defined. The findings in this study indicate that DED has a significant impact on a patient’s reading performance. This agrees with the survey results from Miljanovic et al.9 that DED patients have a high incidence of reading difficulty. These results should be confirmed in future studies with control and DED patients that are matched for age and cognitive abilities, as well as level of English proficiency. These results also agree with previous reports that DED patients experience transient visual deficits.6 Thus, this study provides direct evidence of the impact of DED on patients’ reading ability or visual performance. Furthermore, the results from this study suggest that reading tests may be used to measure the impact of DED and monitor potential therapeutic treatment benefits in DED patients. Future studies that use tests that require rapid integration of visual information may also demonstrate visual deficits in DED patients.
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The authors thank Dr Andrew Loc Nguyen for his helpful input in statistical analysis.
Sponsored by Pfizer Inc. Yi Zhang and Jing-Feng Huang were Pfizer employees at the time of study. None of the authors have any other conflict of interest.
Received January 1, 2012; accepted September 12, 2012.
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