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New Glaucoma Insights: Original Studies

Lower Cognitive Function in Patients With Functionally and Structurally Severe Glaucoma: The LIGHT Study

Yoshikawa, Tadanobu MD, PhD*; Obayashi, Kenji MD, PhD; Miyata, Kimie MD, PhD*; Saeki, Keigo MD, PhD; Ogata, Nahoko MD, PhD*

Author Information
doi: 10.1097/IJG.0000000000001923
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Abstract

A decrease in cognitive function, including mild cognitive impairment, which is the cognitive status between cognitive decline caused by the normal aging process and early stage of dementia, leads to early mortality and decreased quality of life.1–3 An increasing number of recent reports on the influence of visual disturbance, mainly defined by visual acuity, on cognitive impairment has attracted attention to the association between visual function and cognitive function.4–6 The deprivation of the sensory inputs is considered one of the reasons for cognitive impairment in patients with visual disturbance.5 However, there is limited information regarding whether visual field damage is associated with cognitive function.

Glaucoma is an important cause of irreversible blindness worldwide and is characterized by progressive loss of retinal ganglion cells and subsequent defects related to the visual field.7 With the exception of one study,8 multiple hospital-based and population studies have shown that cognitive function in patients with glaucoma was lower than that in control participants.9–14 A prospective study implementing a 3-year follow-up period revealed that patients with glaucoma had an ~4-fold greater risk for dementia than those without glaucoma.14 However, few studies have investigated the influence of glaucomatous visual field defects on cognitive impairment in patients with glaucoma. One hospital-based study reported lower cognitive function in patients with glaucoma and severe visual field defects,10 but the generalizability of the results was limited by the small sample size.

Low cognitive function has been associated with poor medication adherence in patients with glaucoma,15 and a randomized study confirmed its involvement in the progression of glaucoma.16 Thus, an investigation of the association between glaucomatous visual field defects and cognitive function is important for the clarification and subsequent management of glaucoma.

The purpose of this study was to determine whether functionally and structurally severe glaucoma was related to decreased cognitive function. To this end, we assessed functional glaucoma severity by measuring the visual field mean deviation (MD), structural glaucoma severity by measuring the thickness of the circumpapillary retinal nerve fiber layer (cpRNFL), and cognitive function using the Mini-Mental State Examination (MMSE) and the MMSE-blind in 172 patients with glaucoma.

PATIENTS AND METHODS

Patients With Glaucoma

We recruited 172 patients with glaucoma who had at least 1 glaucoma eye for the LIGHT study between May 2017 and December 2019. As previously described,17 the LIGHT study, whose protocol was approved by the Ethics Committee of Nara Medical University (number; 1314), was “Longitudinal study of biological circadian rhythms In Glaucoma patients: Home Testing of circadian intraocular pressure and biological parameters” that was registered in the University Hospital Medical Information Network Clinical Trials Registry (number: UMIN000027299). All procedures used in the study complied with the principles of the Declaration of Helsinki, and written informed consent was obtained from all patients included in the LIGHT study.

Glaucoma was diagnosed based on the presence of a glaucomatous optic disc and visual field defects by a glaucoma specialist (T.Y.) in accordance with the criteria of an earlier study18 as previously described in detail.19 Briefly, the presence of a glaucomatous optic disc was evaluated using a vertical cup-to disc ratio or rim width or RNFL defects; and visual field defects consistent with the optic disc alterations were assessed using the glaucoma hemifield test or pattern deviation using Humphrey Field Analyzer (Humphrey, Carl Zeiss Meditec, Dublin, CA).19 We performed complete ophthalmic examinations, such as slit-lamp biomicroscopy; indirect ophthalmoscopy; gonioscopy; and measurements of best-corrected visual acuity, intraocular pressure using Goldmann applanation tonometry, spectral-domain optical coherence tomography (OCT), and visual field by standard automated perimetry. We excluded the patients with severe corneal and retinal diseases that affect the visibility of retina and ophthalmic evaluations of the optic disc as described previously.19

Of the 172 patients with glaucoma, 128 (74.4%) had bilateral glaucoma and 44 (25.6%) had unilateral glaucoma. Of the 172 eyes included in the analyses, 135 (78.5%) were primary open-angle glaucoma (including normal-tension glaucoma), 12 (7.0%) were primary angle-closure glaucoma, and 25 (14.5%) were secondary glaucoma (including exfoliation glaucoma). In addition, 6 eyes had epiretinal membrane, 2 eyes had postoperative retinal detachment, and 1 eye had myopic choroidal neovascularization.

Evaluation of Functional Glaucoma Severity by Visual Field Examinations

The Humphrey Field Analyzer was used with the 30-2 Swedish interactive threshold algorithm (SITA) standard program to measure the sensitivity of the visual field. Patients with glaucoma were divided into 2 categories: mild glaucoma according to a visual field MD of >−12 dB and severe glaucoma if the visual field MD was ≤−12 dB.20 In case of bilateral glaucoma, we based the visual field MD on the more severely damaged eye.

We considered a visual field unreliable if the false-positive response was >15% based on the results of an earlier study.21 Owing to unreliable or missing visual field data in the 30-2 SITA standard program, 11 sets of eyes of the 172 patients were replaced using the 30-2 SITA fast program according to the visual field MD. In addition, 5 eyes with unreliable visual field MD data due to central scotoma were initially classified into the severe glaucoma group based on the stage category used in an earlier study20 and were excluded from the statistical analyses of continuous visual field MD data.

Evaluation of Structural Glaucoma Severity Using cpRNFL Thickness Determined by Spectral-Domain OCT

The cpRNFL thickness was measured according using a spectral-domain OCT (Spectralis; Heidelberg Engineering, Heidelberg, Germany) provided by the cpRNFL scan program (1536 A-scans×1 B-scan; a circular diameter of 3.5 mm centered on the optic disc). To determine the severity of structural glaucoma, we used the global cpRNFL thickness with a quality score of >15 dB in the more severe eye in case of a bilateral glaucoma. All cpRNFL images were confirmed by a single glaucoma specialist (T.Y.) to achieve better reliability of the cpRNFL segmentation. The specialist concluded that, based on the results of an earlier study,22 18 images of the 172 cpRNFL images had unreliable data with segmentation errors or had a quality score of ≤15 dB, based on which they were excluded from statistical analyses.

Measurement of Cognitive Function Using MMSE

Cognitive function was evaluated by a medical doctor (T.Y.) using the MMSE scale, which is the most commonly used psychological screening test for cognitive assessment. The MMSE score ranged from 0 to 30, and higher scores represented better cognitive function. The presence of cognitive impairment was defined as an MMSE score of ≤26 based on the results of an earlier study.23 A cut-off MMSE score of ≤26 has been found to provide a better balance of sensitivity (0.89) and specificity (0.91) for dementia.23 The blind version of MMSE (MMSE-blind) was also used to assess cognitive impairment.24 The MMSE-blind cognitive test for patients with visual impairment consists of a score ranging from 0 to 22 and excludes 8 questions directly associated with the visual situation included in the full MMSE, such as the naming of 2 items, 3 stage commands, reading and obeying a sentence, writing a sentence, and copying a figure.24 The cut-off MMSE-blind score of ≤16 for the age group of 75 to 79 years has been reported to have high sensitivity (1.0) and specificity (0.99) for dementia.24

Other Measurements

Body mass index was calculated as kg/m2, and household income and education history were assessed by using a self-administered questionnaire. Hypertension was determined by the current use of antihypertensive drugs, and diabetes mellitus was defined by the current use of diabetes drugs or a fasting plasma glucose level of ≥126 mg/dl or glycated hemoglobin level of ≥6.5%. Depressive symptoms were defined by a geriatric depression scale score of ≥6, and subjective sleep disturbance was determined as a Pittsburgh sleep quality index questionnaire score of ≥6. Daytime physical activity was evaluated using the International Physical Activity Questionnaire. Best-corrected visual acuity was measured using a standard Japanese decimal visual acuity chart, and decimal visual acuity was converted into logarithm of minimum angle of resolution units, which took into account the eye in worse condition.

Statistical Analyses

Normally distributed variables were expressed as mean±SD, and asymmetrically distributed variables were expressed as median (interquartile range). The significance of the differences in the means and medians between the 2 groups was determined using unpaired t tests and the Mann-Whitney U test, respectively. The χ2 test was used for categorical data. To calculate regression coefficients and odds ratios (ORs), we performed logistic regression analysis for cognitive impairment with 95% confidence intervals (CIs) between mild and severe glaucoma. The potential confounders for cognitive impairment were age and variables that were marginally associated with the cognitive status in the univariable analyses (P<0.20). The correlation between continuous MMSE scores and glaucoma severity was calculated using the Pearson correlation analysis. All statistical analyses were conducted using SPSS version 25 (IBM SPSS Statistics Inc., Chicago, IL), and the threshold for significance was a P-value of <0.05.

RESULTS

The age of patients with glaucoma was 70.6±10.9 (mean±SD) years, and the number of male patients was 78 (45.3%). The ages of patients with mild and severe glaucoma were 69.2±11.4 and 71.6±10.5 (mean±SD) years, respectively (P=0.15). Of the 172 patients with glaucoma, 45 (26.2%) had cognitive impairment, which was significantly associated with factors such as older age, lower education history, hypertension, diabetes, and the presence of depressive symptoms (Table 1). The median visual field MD (interquartile range) of the mild glaucoma group was −6.3 (−3.8, −8.6) dB, and that of the severe glaucoma group was −20.0 (−14.8, −24.2) dB. The mean cpRNFL thickness (SD) of the mild glaucoma group was 75.2 (12.2) μm, and that of the severe glaucoma group was 53.3 (13.8) μm.

TABLE 1 - Basic and Clinical Parameters by Cognitive Status
Cognitive Status
Preserved (MMSE >26) Impaired (MMSE ≤26) P
No. patients 127 45
Examination score, median (range) 30 (27, 30) 25 (19, 26) <0.001
Basic parameters
 Age, mean (SD) (y) 67.9 (10.9) 78.4 (6.0) <0.001
 Sex, number (%), men 57 (44.9) 21 (46.7) 0.84
 Body mass index, mean (SD) 22.9 (3.2) 22.1 (3.9) 0.19
 Household income (≥4 million JPY per year), number (%) 48 (38.7) 13 (30.2) 0.32
 Education history (≥13 y), number (%) 62 (48.8) 10 (22.2) 0.002
Clinical parameters
 Visual acuity, mean (SD), LogMAR 0.11 (0.32) 0.21 (0.30) 0.069
 Hypertension, number (%) 41 (32.3) 26 (57.8) 0.003
 Diabetes, number (%) 21 (16.5) 13 (28.9) 0.074
 Depressive symptoms (GDS ≥6), number (%) 28 (22.0) 17 (37.8) 0.039
 Subjective sleep quality (PSQI ≥6), number (%) 50 (39.4) 21 (46.7) 0.39
 Subjective daytime physical activity, median (IQR), MET-hour/wk 15.0 (5.8, 34.7) 15.4 (3.4, 24.7) 0.91
GDS indicates Geriatric Depression Scale; IQR, interquartile range; JPY, Japanese Yen; LogMAR, logarithm of minimum angle of resolution; MET, metabolic equivalent; MMSE, Mini-Mental State Examination; PSQI, Pittsburgh Sleep Quality Index.

The prevalence of patients with cognitive impairment (MMSE score ≤26) in the severe glaucoma group was significantly higher than that in the mild glaucoma group (33.3% vs. 15.7%; P=0.010). Similar results were obtained with an MMSE-blind score of ≤16 (14.7% vs. 1.4%; P=0.003; Fig. 1) in the assessment of glaucoma severity and cognitive impairment.

FIGURE 1
FIGURE 1:
Bar graph showing the association between the severity of glaucoma and prevalence of the patients with cognitive impairment defined by the Mini-Mental State Examination (MMSE) scores ≤26 and MMSE-blind scores ≤16. The prevalence of the patients with cognitive impairment in the mild and severe glaucoma group was compared with the χ2 tests.

Using an MMSE score of ≤26 in the univariable logistic regression analysis, we showed that the severe glaucoma group had a significantly higher OR for cognitive impairment (OR, 2.68; 95% CI, 1.25-5.76; P=0.011; Table 2). Multivariable logistic regression analyses adjusted for the basic (age, body mass index, and education history) and clinical parameters (visual acuity, hypertension, diabetes, and depressive symptoms) showed significantly higher OR for cognitive impairment in the severe glaucoma group (model 1: OR, 2.65; 95% CI, 1.11-6.35; P=0.029; model 2: OR, 2.74; 95% CI, 1.07-7.02; P=0.036; model 3: OR, 2.62, 95% CI, 1.006-6.84; P=0.049; Table 2), and a similarly significant higher OR for cognitive impairment was found in relation to 1 dB of decreased visual field MD (unadjusted model: OR, 1.07; 95% CI, 1.02-1.11; P=0.003; model 1: OR, 1.08; 95% CI, 1.02-1.14; P=0.004; model 2: OR, 1.08; 95% CI, 1.02-1.14; P=0.011; model 3: OR, 1.07; 95% CI, 1.01-1.13; P=0.015; Table 2). In addition, a higher OR for cognitive impairment was also related to 10 μm of thinning of the cpRNFL (unadjusted model: OR, 1.41; 95% CI, 1.12-1.77; P=0.004; model 1: OR, 1.39; 95% CI, 1.05-1.84; P=0.023; model 2: OR, 1.43; 95% CI, 1.05-1.95; P=0.022; model 3: OR, 1.42; 95% CI, 1.05-1.93; P=0.025; Table 2). Multivariable logistic analysis adjusted for age squared showed a consistent result of a significant association between severe glaucoma and cognitive impairment (OR, 2.59; 95% CI, 1.09-6.13; P=0.031). In the correlation analyses between continuous MMSE scores and glaucoma severity, lower visual field MD and thinner cpRNFL thickness were significantly correlated with lower MMSE scores (r=−0.29; P<0.001 and r=−0.32; P<0.001, respectively).

TABLE 2 - Association Between the Severity of Glaucoma and Cognitive Impairment
OR for Cognitive Impairment (MMSE Scores ≤26)
Adjusted OR
Unadjusted OR Model 1 Model 2 Model 3
Functional severity
 Mild (MD >−12 dB) 1.0 (ref) 1.0 (ref) 1.0 (ref) 1.0 (ref)
 Severe (MD ≤−12 dB) 2.68 (1.25-5.76) 2.65 (1.11-6.35) 2.74 (1.07-7.02) 2.62 (1.006-6.84)
P 0.011 0.029 0.036 0.049
 Decreased visual field MD (per 1 dB) 1.07 (1.02-1.11) 1.08 (1.02-1.14) 1.08 (1.02-1.14) 1.07 (1.01-1.13)
P 0.003 0.004 0.011 0.015
Structural severity
 Thinning of cpRNFL thickness (per 10 μm) 1.41 (1.12-1.77) 1.39 (1.05-1.84) 1.43 (1.05-1.95) 1.42 (1.05-1.93)
P 0.004 0.023 0.022 0.025
Model 1: adjusted for basic parameters associated with cognitive function (P<0.2) (age, body mass index, and education history).
Model 2: adjusted for age plus clinical parameters associated with cognitive function (P<0.2) (visual acuity, hypertension, diabetes, and depressive symptoms).
Model 3: adjusted for basic and clinical parameters associated with cognitive function (P<0.2) (age, body mass index, education, visual acuity, hypertension, diabetes, and depressive symptoms).
cpRNFL indicates circumpapillary retinal nerve fiber layer; dB, decibel; MD, mean deviation; MMSE, Mini-Mental State Examination; OR, odds ratio.

Similar results were obtained on further logistic regression analyses of cognitive impairment using an MMSE-blind score of ≤16. In the logistic regression analyses adjusted for age, the OR for cognitive impairment (MMSE-blind score ≤16) was significantly associated with 1 dB of decreased visual field MD (OR, 1.14; 95% CI, 1.05-1.23; P=0.003) and 10 μm of thinning of the cpRNFL (OR, 1.56; 95% CI, 1.008-2.41; P=0.046).

No significant association between bilateral glaucoma and cognitive impairment (MMSE score ≤26 and MMSE-blind score ≤16) were found (P=0.55 and 0.51, respectively).

DISCUSSION

This cross-sectional study investigated the association between glaucomatous visual field defects and cognitive function after adjusting for basic and clinical parameters. After adjusting for potential confounders, including age and visual acuity, we showed that functional and structural glaucomatous damage was associated with lower cognitive function in a glaucoma cohort. The strength of this study relies on the quantitative association between the glaucoma severity and cognitive function in 172 patients with glaucoma.

Our results were consistent with the findings of earlier studies that showed lower cognitive function in patients with glaucoma compared with nonglaucoma controls.11–13,25 However, little is known about the association between the severity of glaucoma (as indicated by visual field loss and RNFL thickness) and cognitive function. A cross-sectional study of 70 patients with glaucoma reported that visual field loss in glaucoma was related to lower cognitive function, as evaluated using the Montreal Cognitive Assessment, but no significant association between RNFL thickness and cognitive function was found.10 However, our study demonstrated that a decrease in both visual field sensitivity and RNFL thickness was associated with cognitive impairment. This inconsistency may be caused by insufficient statistical power, given the relatively small number of patients with glaucoma with RNFL thickness data (n=66) in the earlier study.

The neural mechanism linked to lower cognitive function in patients with glaucoma may be due to the reduction of sensory inputs induced by visual field defects. Two population-based studies, one in the United States (n=2520) and another in Singapore (n=2478), analyzed visual impairment associated with lower cognitive test scores using MMSE and the abbreviated mental test, respectively.5,6 The prospective results of the Women’s Health Initiative cohort after a mean follow-up period of 3.8 years (n=1061) demonstrated that participants with baseline visual impairment had an ~5- to 6-fold increased risk of dementia and mild cognitive impairment.4 These earlier studies indicated that visual disturbance due to poor visual acuity led to cognitive impairment.4–6 In addition, our results showed that visual field defects were associated with lower cognitive function independent of visual acuity. Thus, the treatment of glaucoma may have a preventive effect on cognitive impairment by helping maintain good visual function. However, further longitudinal studies are needed to confirm the specific influence of glaucoma treatments on cognitive function.

Glaucoma may be involved in the pathogenesis of cognitive impairment by causing circadian disruption due to the loss of intrinsically photosensitive retinal ganglion cells. In patients with glaucoma, decreased transmission of light signals from the intrinsically photosensitive retinal ganglion cells to the suprachiasmatic nuclei leads to misalignment of circadian biological rhythms.26 Our previous study demonstrated that melatonin secretion, which is a known internal indicator of circadian biological rhythms, was lower in patients with glaucoma.17 The results of a previous cross-sectional study further indicated that lower physiological melatonin levels were associated with a higher prevalence of cognitive impairment.27

There are several limitations to the present study. First, owing to the cross-sectional design, we could not determine the causal relationship between glaucoma severity and lower cognitive function. Second, although the evaluation of cognitive impairment using MMSE scores proved to have high sensitivity and specificity,23 the assessment of cognitive impairment based on MMSE scores without a previous clinical diagnosis may lead to a misclassification of cognitive function status. Third, the number of patients with cognitive impairment (MMSE, n=45; MMSE-blind, n=16) was relatively small, which resulted in restricted adjustment for potential confounders in the multivariable analysis and possibly led to inaccurate ORs because of the wide range of 95% CIs. Finally, the variability and reliability of visual field examinations may be influenced by cognitive function status.28,29 Considering these aspects, our results regarding the association between visual field defects and cognitive impairment are consistent with those of the relationship between structural severity (based on cpRNFL thickness) and cognitive impairment.

In conclusion, this cross-sectional analysis evaluated the cognitive function of 172 patients with glaucoma based on MMSE scores and demonstrated a significant association between functional and structural glaucoma damage and cognitive impairment independent of known risk factors such as age and visual acuity.

ACKNOWLEDGMENTS

The authors would like to thank Michiru Higuchi and Yuki Ouchi for their help with data collection.

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Keywords:

glaucoma; cognitive impairment; cognitive function; visual disturbance; visual field

Copyright © 2021 The Author(s). Published by Wolters Kluwer Health, Inc.