Glaucoma is a major cause of low vision, especially in the older population. Understanding how glaucoma affects a person in their everyday life is essential to best provide appropriate support for patients with the disease. Moreover, knowing how disease severity affects problems with everyday visual function provides important information when balancing the risks and benefits of intensifying treatment. The conventional view of the functional impact of glaucoma is centered on the disruption of peripheral vision, with patients only reporting symptoms when visual field (VF) defects become advanced. However, the impact of glaucoma on everyday function, including visual ability required to carry out daily activities, is evident and has been recently reviewed.1–3 Problems with “reading and seeing detail” have been reported recently as one of the main anxieties for patients with glaucoma.4 Difficulties with reading, following lines of text and other near-vision tasks have been consistently reported by patients in other interview and questionnaire studies.5–7 Although self-report measures of difficulties with everyday visual tasks provide invaluable insight about patient experience, they are open to biases involving personality, perception of task difficulty, or demand characteristics.1,8 For example, people will self-report differences in difficulties with tasks even when they have the same clinical condition and visual limitations, based on individual expectations.9 It therefore seems prudent to use functional testing in task-focused situations, to determine the stage at which a disease such as glaucoma affects day-to-day function. Indeed, performance-based testing, or direct objective assessment, has revealed evidence that some patients with glaucoma experience problems with driving, both on road10 and in simulated environments,11 mobility,12 postural sway and balance,13 searching for objects in photographs,14 and hand-eye coordination.15 It has also been suggested that a battery of performance-based measures, such as using the telephone and locating an object might be a useful adjunct to the clinical assessment of glaucoma.16
Surprisingly, there are very few studies on the direct assessment of reading performance in patients with glaucoma. One important study3 provided some evidence that reading performance, assessed in terms of maximum reading speed, is impaired in patients with glaucoma compared with a visually healthy group. A significantly reduced reading speed was demonstrated in those patients with advanced VF defects, and this finding arose only when visual acuity (VA) was accounted for in multivariate statistical analysis. A study by Roberts et al directly assessed reading performance of glaucoma patients and suggested associations between clinical measures of visual function (such as contrast sensitivity [CS]) do not correlate with reading performance.17 Fujita et al revealed difficulties with reading performance in a group of patients with glaucoma,18 but only examined patients with an absolute scotoma within 3 degrees of the central VF. Altangerel et al also identified the reading of small print as one of the most visually demanding tasks for patients with glaucoma and noted a moderate correlation between reading speed and the extent of Esterman binocular VF loss.16
Patients with glaucoma commonly report difficulties under poor contrast conditions in day-to-day life. Studies have reported that the aspects of visual function that best predict the ability of a patient with glaucoma to perform activities of daily living are VA and CS.19 This suggests that a reading experiment examining performance at different levels of contrast might be informative. Therefore, this study aimed to explore the hypothesis that patients with glaucoma will have a greater change in reading speed than age-similar visually healthy people when letter contrast is reduced.
The target population for this prospective case-control study was patients with glaucoma between 50 and 80 years of age, with a range of VF defects in both eyes. Patients were recruited from Moorfields Eye Hospital NHS Foundation Trust, London, and all had either primary open angle or normal tension glaucoma in both eyes. Glaucomatous VF defects were defined as a Glaucoma Hemifield test (GHT) “outside normal limits” classification using the Humphrey Field Analyzer (HFA, Carl Zeiss Meditec, CA) at their most recent clinic visit. The mean deviation (MD) is a standard age-corrected clinical measure of the overall severity of VF loss, with more negative values indicating greater VF loss. MD of the better eye was used as a measure of VF defect severity. An age-similar control group, consisting of people with no history of eye disease and no VF defects (defined by “within normal limits” status on the GHT), was recruited from the City University London Optometry Clinic.
Participants were included only if they had a corrected binocular VA (logMAR BVA) of equal to or better than 0.18 logMAR (Snellen equivalent of 6/9), as measured using an Early Treatment Diabetic Retinopathy Study chart. Participants were excluded if they had any other ocular disease (except for an uncomplicated lens replacement cataract surgery). In order to attempt to minimize media opacity (cataract) and other lens type artifacts as confounding ocular conditions, all participants were required to be within “normal limits” for abnormal light scattering in the eye media using the Oculus C-Quant straylight meter (Oculus Optikgerate GmbH Wetzlar, Germany). Recruitment was also restricted to those who reported good general health established by prior interview based on questions used on the EQ-5D instrument.20 Participants were not enrolled if they had a self-reported reading difficulty such as dyslexia, of if they were taking “significant medication” other than for glaucoma, including antidepressants or treatment for diabetes or use of beta-blocker medication. All participants recruited were native English readers.
The study was approved by research governance committees of the participating institutions in addition to receiving approval from a UK National Health Service, National Research Ethics Service committee. The study conformed to the Declaration of Helsinki, and all participants gave their informed written consent before participation.
Ninety-three participants were recruited for the study: 53 patients with glaucoma with a mean age of 66 (standard deviation 8.5) years and 40 visually healthy age-related controls, with a mean age of 69 (standard deviation 7.5) years. For the study itself, participants first completed a number of vision and non-vision tests before performing the reading experiment. All testing was performed in 1 session, with adequate rest times between tests.
Vision and Non-Vision Tests
All participants completed a binocular distance VA using Early Treatment Diabetic Retinopathy Study charts with the participant's best correction in place, binocular Pelli-Robson CS, and uniocular VF testing using an HFA. VA was tested at 6 m and with a uniform luminance of 120 cd/m2 as recommended by the British Standards Institution. CS was tested at a 1 m distance, with a mean luminance of 65 cd/m2, as recommended by the suppliers. Patients completed an HFA 24-2 Swedish interactive threshold algorithm (SITA) standard and 10-2 SITA standard VF tests in each eye. Controls completed an HFA 24-2 SITA fast test. VF tests for control subjects were all “within normal limits” in each eye as defined by the GHT.
Middlesex Elderly Assessment of Mental State
Middlesex Elderly Assessment of Mental State (MEAMS, Pearson, London, UK) is a comprehensive, psychometric, screening test designed to detect gross impairment of specific cognitive skills such as memory and object recognition in an elderly population. Each section of the MEAMS is scored independently with lower scores indicating a more significant cognitive impairment. The use of MEAMS for screening of impairments has been validated by a number of research studies,21 and it has been considered as more superior to other screening methods such as the mini-mental state test, as it is able to test a wider range of specific cognitive defects.22
Burt Reading Test
Burt Reading Test (Scottish Council for Research in Education) is a standardized reading test designed to measure reading abilities. It has a quick administration time, produces a quantitative value of a reader's ability, and has been used in numerous recent studies to measure a component of reading performance.23 In the interest of reducing test time, a truncated version of the original test was used consisting of the last 80 words from the original 110. This test has previously been used to assess reading skill in an adult population.24,25 Participants read the words out loud in a quiet, brightly lit room starting at the top of a list and reading down to progressively more difficult words. The test score was the number of words correctly read, thus higher scores indicate a better reading ability.
A Lexical Decision Task
This computer-based test was designed specifically for this study and was used as an additional measure to gauge the participant's reading ability. Participants were required to fixate on a target in the center of the monitor for 200 ms. The fixation target was then removed and replaced with a stimulus. This stimulus was either a real word such as “spoon” or “table” or a false pseudo-word such as “sploon” or “talbe.” The words were taken from the Bank of English corpus jointly owned by HarperCollins Publishers and the University of Birmingham, and they were matched for frequency as defined by the corpus. Non-words were matched to the real words with regard to word length. Participants were required to identify if the target word was a real word or a false word by verbally expressing “yes” and “no,” respectively. All stimuli remained on screen until a response was given. A total of 30 words (15 real and 15 false) were presented to participants. Words were presented at 100% contrast in Times New Roman font size 14, subtending a height of 1.14 degrees. Five practice trials were given and following that, all trials were randomized. Scores were recorded as the number of errors made.
To identify how much reading participants did in their daily life, they were asked to choose a reading frequency of “minimal,” “moderate,” or “intensive” amounts. Participants were also required to report their general health from a scale of 1 (very poor) to 10 (excellent).
The reading material consisted of 16 short paragraphs of text (68–79 words per text), adapted from an English fiction book, eight of which were presented at 100% contrast and eight at 20% contrast on a 56-cm cathode ray tube computer monitor at a resolution of 1600 × 1200, with a refresh rate of 100 Hz (Iiyama Vision Master PRO 514, Iiyama Corporation, Tokyo, Japan). All texts were matched for readability according to the Flesch-Kincaid measure,26 and all measured at 8.2. Text was displayed in Arial font size 48 subtending 34 pixels on the screen, which equates to 0.84 degrees (height) for the largest character. Line length subtended 20 degree width. The participant viewed the passages one at a time. A table mounted chin rest maintained a 60-cm viewing distance. Contrasts were calculated by using a Minolta LS-100 Luminance Meter (Konica Minolta Sensing Inc, Tokyo Japan) and measuring the luminance of the screen at each greyscale value. The letters were “black on white” with background screen luminance of 33.4 cd/m2. The mean luminance of the screen for the 20% contrast was 26.9 cd/m2, and the mean luminance of the screen for the 100% contrast was 0.05 cd/m2.
Participants read the text silently. The reading duration was measured as the time from the first fixation on the first word to the last fixation on the final word using an EyeLink 1000 (SR Research Ltd., Mississauga, Ontario, Canada).
The 16 passages were subdivided into 2 sets of 8. One set of 8 texts was always presented at 100% contrast and the other set of 8 texts was always presented at 20% contrast. These texts were displayed in a random order. Participants were given the same verbal instructions to, “… read the text silently, as quickly and accurately as possible” and, “… confirm when they had reached the end of the passage.” Once the participant indicated reaching the end of the text, the experimenter pressed the escape button and the next text followed. Participants were allowed as many breaks between texts as they wanted. Participants were also asked simple comprehension questions about the text.
The primary outcome for this study was the change in reading speed demonstrated by each individual observer as a result of a decrease in letter contrast. Median reading duration in seconds was calculated for each subject for the eight trials for each contrast. The difference between these two median values determined the percent reduction for the individual. Median percent reduction values for the patients were compared with median values for the controls using a Mann-Whitney test. Next, a normal reference range for the percent reduction values was constructed from the distribution of the percent reduction values for the 40 control participants. A 95% upper limit for this normal reference range was set by ranking the percent reduction values for each control and delineating the 38th largest out of the 40 ranked values. Patients with percent reduction values more extreme than this reference point were defined to have a significant reduction in reading speed due to the decrease in letter contrast, beyond what might be observed in the “normal” variability of visually healthy people. Attributes from these patients were then compared with others as a secondary outcome for the study. The attributes considered were summary measures from the non-vision tests and vision tests. For VF defect severity, MD values for 24-2 and 10-2 tests from the patient's better eye were used. In addition, an integrated VF (IVF) using 24-2 results was constructed for each patient27: a simulated binocular VF in which patients' best point-by-point monocular sensitivity is used (PROGRESSOR software: Moorfields Eye Hospital, London, UK/Medisoft Ltd., Leeds, UK). The mean sensitivity of the IVF was also calculated, with lower values suggesting more impaired binocular sensitivity. Minitab v.14 (Minitab Inc., PA) was used for the statistical analysis.
The mean age of the patients and controls did not significantly differ (p = 0.10; two sample t-test). The distribution of the ages did not differ between groups either (p = 0.92; F-test on variances). There were 23 (58%) and 28 (53%) women in each of the patient and control groups, respectively. Patients and controls also had similar average values for general health rating, general reading frequency, performance on the lexical decision task, MEAMS, and Burts test score (Table 1).
Table 2 shows the summary measures of tests of visual function, which were significantly different between the patients and the controls.
Median reading duration at the 100% contrast condition was 16.1 s [interquartile range (IQR), 13.2–20.0] in the patient sample and 16.4 s (IQR, 13.8–19.3) in the control sample. Median reading duration at the 20% contrast condition was 19.2 s (IQR, 16.5–24.3) in the patient sample and 17.1 s (IQR, 15.3–22.5) in the control sample. Control participants read lower contrast text with a median speed that was 11% slower (IQR, 6%–17%) than higher contrast print. Patients with glaucoma read lower contrast text with a median speed that was 20% slower (IQR, 8% to 44%) than higher contrast text. The difference between patients and controls was statistically significantly; p = 0.01, Mann-Whitney test (Fig. 1).
Twenty-five patients (47%; 95% confidence interval: 33%–61%) had a reduction in reading speed due to a decrease in contrast beyond the 95% limit for controls (24.5% reduction). Assuming this sample is representative of an elderly population of patients with VF defects in both eyes, and a range of severity in the “better” of the two eyes, nearly half of them will have impaired reading speed at lower letter contrast when compared with visually healthy people of a similar age. Attributes (vision and non-vision tests) of patients falling within and outside the normal range are listed in Table 3. There was no difference in average age or in average values in any results from the non-vision tests between the two groups of patients. Conversely, patients with impaired reading speed at lower letter contrast had worse CS, worse VA, and worse VFs, when compared with those patients whose performance fell “within the normal limits.”
Difficulties with reading have been shown to diminish quality of life,28 and reading impairment resulting from various eye conditions is often a central concern of people with low vision. There are very few studies that have directly assessed reading performance in patients with glaucoma.3,17,18 This study provides evidence that low contrast between the text and background reduces reading speed in patients with glaucomatous VF defects in both eyes. Moreover, this effect on reading speed with low contrast letters was more pronounced than that observed in visually healthy people of a similar age.
By measuring a difference in reading speed from high to low contrast in each subject, the experiment reduced error variance due to individual differences in reading speed. Moreover, the patients and controls were well matched in term of potential confounders such as general health, reading frequency and ability, and cognitive ability. The implication is that the differences between the patients and controls are likely explained by the poorer visual function in the patient group.
There was considerable variability in the extent of reading speed reduction due to a decreased contrast of letters in the patient group. Some patients were completely unaffected, whereas others (n = 4) were twice as slow at reading when letter contrast was decreased. A secondary analysis of the group of patients with a significant reduction in reading speed at low contrast indicated that the effect is related to the severity of decrease in visual function. These patients had more severe VF defects, poorer VA, and poorer CS. These results point to the potential usefulness of better eye VF MD values and summary measures from the IVF in identifying patients that are more at risk of having problems with reading, especially when letter contrast is decreased. Group comparisons of patients within and outside normal limits revealed no significant differences in non-vision measures. This suggests that it is the quality of vision alone, and not some other cognitive deficit, which is causing a greater reduction in reading speed. Non-glaucomatous causes for the lower VA in patients were ruled out either by clinical examination or stray light readings. Although VA loss is generally considered a late finding in glaucoma, subtle VA and CS loss may manifest before clinically significant loss in earlier stages of the disease.29 All subjects in this study had acuity of equal to or better than 6/9 and the difference between patients and controls, although significant, was small. The significant difference may have been because there was more variability in the patient group than in the visually normal group. Furthermore, performance of patients with glaucoma on day-to-day objective tasks is strongly associated with binocular CS and binocular VA.19 It is therefore important to consider even minor deterioration in VA and CS as potentially debilitating for patients with glaucoma.
Classic reading experiments,30 using stationary text, have shown that limitations in a field of view less than about 20 characters can significantly impact reading. The print size relative to acuity levels reported in our study is well within the “visual requirements” for maximum reading rates. However, in the low-contrast reading condition, the derived print contrast relative to measured individual contrast threshold is close to the threshold relating contrast reserve to reading rates, so that any decline in measured CS would be expected to affect reading rate.
A potential limitation of the results from this study relates to the difference between contrasts of text used (100% and 20%) and contrasts of text experienced in the “real world.” It may be that patients with glaucoma only encounter conditions of 20% contrast infrequently and a higher level or a wider range of contrasts should have been used to reflect a more likely contrast condition. Further research would benefit from testing a wider range of contrasts. An informal attempt was made to engage the participants in the task by asking comprehension-type questions between texts. Still, the within-subject experimental design minimizes the impact of this issue on the reported conclusions. Another potential weakness of the study is the sensitivity of the cognitive tests included; the MEAMS, lexical decision task, and Burts reading test provide some information of general cognitive and reading ability, but they may not be sensitive enough to expose more subtle cognitive deficits. Additionally, volunteers for research studies tend to be healthier than the general population.31
In conclusion, this study measured reading speed in patients with glaucoma with VF defects in both eyes and found that they were more affected by a decrease in contrast in letters of text than age-related visually healthy people. Patients who were more affected than others were generally those with more severe VF defects and poorer VA and CS. These results are important because they corroborate findings from self-report studies, suggesting that patients with glaucoma complain of difficulties with reading in day-to-day life. The results from this report suggest simple increases in luminance for glaucoma patients could reduce the prevalence of “reading disability.” Further research exploring the mechanisms by which glaucoma leads to difficulties with reading will be invaluable to aid clinical management of the disease, raise awareness of the functional difficulties caused by glaucoma, and encourage rehabilitation aids for reading.
Department of Optometry and Visual Science
City University London, Northampton Square
London, EC1V 0HB
This study was conducted as part of a program of work funded by unrestricted grants from the Special Trustees of Moorfields Eye Hospital, the Merck Investigator-Initiated Studies Programme and an Independent Investigator Research Grant from Pfizer Inc. David Garway-Heath receives a proportion of his funding from the Department of Health's National Institute for Health Research Biomedical Research Centre at Moorfields Eye Hospital and the UCL Institute of Ophthalmology.
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reading; glaucoma; visual fields; contrast sensitivity