Introduction

Glaucoma is known to have few subjective symptoms, progressing without causing symptoms until the disease is advanced and there is substantial neural damage1. Epidemiological studies in many different populations have repeatedly documented that 50% to 90% of persons with open-angle glaucoma are unaware of their condition2,3,4, possibly due to the lack of subjective symptoms.

Crabb et al. found that glaucoma patients frequently experienced a combination of blurred vision and missing areas of the visual field, which appear to be the primary visual indicators of the condition. Twenty-six percent of patients were unaware of their visual field loss. 5 Hu et al. reported that the most common symptoms reported by glaucoma patients were needing more light and blurry vision. 6 Recently, Shah et al. showed that a subset of specific patient-reported symptoms explained 62% of the variance in the severity of visual field damage.7 However, no previous studies have examined the presence or absence of subjective symptoms during driving.

The relationship between motor vehicle collisions (MVCs) and visual field impairment is still poorly understood. We established the first driving assessment clinic at a Japanese eye hospital to educate drivers with visual field impairment, using a driving simulator (DS), on scenarios that pose MVC risks specific to them with the goal of reducing MVCs caused by visual field impairment.8,9 At this driving assessment clinic, we experienced that many patients were surprised to find out for the first time that they had visual field defects after they overlooked a traffic light or caused an accident when a car suddenly rushed out from the left or right. Therefore, we thought it would be meaningful to investigate what kind of visual field impairment patterns affect the presence or absence of subjective symptoms during driving to teach patients with glaucoma how to drive safely. Thus, in the present study, we investigated subjective symptoms during driving among patients with glaucoma, as well as their clinical characteristics, at a driving assessment clinic.

Results

A total of 227 patients (147 men, 80 women) were included. The mean ± standard deviation (SD) age was 63.2 ± 12.4 years (range 26–87 years), the better-eye MD was -11.83 ± 6.70 dB (range -28.34 to + 5.30 dB), and the mean worse eye MD was -19.51 ± 6.45 dB (range -31.85 to + 0.78 dB), respectively. There were no significant differences in age, sex, or MD between patients from the Nishikasai Inouye Eye Hospital and the Niigata University Hospital. In this study, no patients were suspected of having dementia based on the MMSE assessment for cognitive impairment.

The figure shows an example of results from a glaucoma patient who missed a traffic signal in the DS, causing a motor vehicle collision, due to a superior visual defect (Fig. 1). The patient had no subjective symptoms during daily driving. After learning at our clinic that she had missed the signal due to this superior visual defect (Fig. 2), the patient continued to drive while being careful at traffic signals and had no accidents or violations for two years.

Fig. 1
figure 1

Results from a glaucoma patient who missed a traffic signal in the driving simulator, causing a motor vehicle collision. She had no subjective symptom during driving. (a) The subject was a 77-year-old woman who had no subjective symptom during driving. She had primary open-angle glaucoma with best-corrected visual acuity in the better eye of 20/20. The top left and top right show grayscale plots and visual field values obtained with the Humphrey Field Analyzer 24-2 (HFA 24-2) for the left and right eyes, respectively. The mean deviation of her visual field was -24.69 dB in the right eye and -11.07 dB in the left eye. The integrated visual field (IVF) (lower left) and the Esterman visual field test (lower right) show that this patient’s corresponding monocular visual field damage resulted in a binocular defect in the upper hemifield of the central field of view.

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Fig. 2
figure 2

Screenshots of the simulations and IVF subfield maps. Left: In the screenshots, the red points (indicated with yellow arrows) show the gaze point. The driver’s vehicle had a simulated speed of 50 km/hour. The signal changed from yellow to red. Right: IVF superimposed over a recording of the DS test, centered over the gaze point (red point), to compare it with the area of visual field impairment. The signal is within the area of the visual field defect, suggesting that the patient’s superior visual field defect made it difficult to notice the signal changing from yellow to red, causing her to miss the signal and collide with a vehicle that came from the left.

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Of the 227 patients, 145 (63.9%) did not report subjective symptoms during daily driving.There was no significant difference in the proportion of patients with subjective symptoms by geographical location: 65 of 109 patients (59.6%) lived in Tokyo and 80 of 118 (67.8%) patients lived in Niigata (P = 0.2; Chi-squared test).

Table 1 shows the demographic characteristics and vision characteristics of the study subjects with or without subjective symptoms during daily driving. The glaucoma patients with subjective symptoms during driving had worse better-eye MD than those who without subjective symptoms (P = 0.012). The mean sensitivity of the superior IVF0-12, superior IVF13-24, and inferior IVF13-24 was also significantly lower in the glaucoma patients with subjective symptoms during driving (P = 0.0002, P = 0.0013, and P = 0.0008, respectively). There were no differences between the groups with and without subjective symptoms during driving in age, gender, MMSE score, driving exposure time, number of MVAs in the previous five years, worse-eye visual acuity, worse-eye MD, Esterman score, or inferior hemifield IVF0-12. The self-reported prevalence of MVAs was 29.3% (24/82) in the group with subjective symptoms during driving and 18.6% (27/145) in the group without subjective symptoms.

Table 1 Comparison of demographic, driving, and vision characteristics of study participants with and without subjective symptoms during driving.
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Table 2 shows the results in DS. Data were not available for 34 cases (14 cases with subjective symptoms during driving and 20 cases without subjective symptoms during driving) due to two reasons: (1) experiencing simulator sickness during the main test, and (2) patients were excluded from the analysis because of poor eye-tracking data (more than 50% of data missing) in video clip recordings. One or more collisions in the DS were observed in 80.9% (55/68) of the group with subjective symptoms during driving and in 72.0% (90/125) in the group without subjective symptoms (P = 0.53). There were no significant differences in the number of collisions in the DS or horizontal and vertical spread of search between the two groups (P = 0.63, 0.93, and 0.18).

Table 2 Result of driving simulator of study participants with and without subjective symptoms during driving.
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Of the 227 patients with glaucoma, 48 were classified as mild, 71 as moderate, and 108 as severe. There was a statistically significant association between glaucoma severity and the rate of subjective symptoms during daily driving: 22.9% of the mild group, 36.6% of the moderate group, and 41.7% of the severe group had subjective symptoms during driving. The presence of subjective symptoms during driving was higher in the severe glaucoma group (P = 0.030, Cochran-Armitage trend test) (Table 3).

Table 3 Presence of subjective symptoms by stage of disease.
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We performed two separate logistic regression analyses of the study participants for different areas of the IVF. Analysis 1 showed that the presence of subjective symptoms was significantly associated with mean sensitivity in the superior IVF0-12 (P = 0.0029; OR: 1.07; 95% CI: 1.02, 1.12) (Table 4). Analysis 2 showed that presence of subjective symptoms was not significantly associated with mean sensitivity in the superior and inferior IVF13-24 (Table 4).

Table 4 Multivariate logistic regression analysis of factors influencing participants with and without subjective symptoms, shown as OR with 95% CI.
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Discussion

In this study, we attempted to investigate subjective symptoms during daily driving by glaucoma patients at a driving assessment clinic. We found that 145 of 227 patients (63.9%) did not report subjective symptoms during daily driving. In a previous study, Shono et al. examined 250 newly diagnosed glaucoma patients in Tajimi Municipal Hospital (Gifu, Japan), of whom 233 (93.2%) reported being unaware of any visual abnormalities.10 Furthermore, they reported that 140 of 149 patients (94.0%) in the mild stage, 51 of 56 patients (91.1%) in the moderate stage, and 41 of 45 patients (91.1%) in the severe stage were previously undiagnosed because they were unaware of the disease. This rate of subjective symptoms is lower than in our study; a difference that may be attributable to the fact that the report by Shono et al. was based on “subjective symptoms,” while our study focused on “subjective symptoms during daily driving.” We specifically investigated the presence or absence of visibility difficulties limited to driving situations. When driving, there are many situations in which people feel danger and need to pay attention, such as checking traffic signals, looking at signs, and watching out for cars and people running out from the left or right, which may explain why people noticed the “difficulty in seeing” in more situations than in daily life.

We also found that as the stage of glaucoma progressed from mild to moderate to severe, the percentage of patients with subjective symptoms increased to 22.9%, 36.6%, and 41.7%, respectively. Sabapathypillai et al11 investigated the relationship between self-perceived driving difficulty, driving avoidance, and negative emotions regarding driving and performance during an on-road driving test. They found that 26 of 109 glaucoma patients (23.8%) self-reported negative emotions, and that the proportion increased with worsening glaucoma severity: 11.3% in mild, 33.3% in moderate, and 42.8% in advanced glaucoma. The proportion of glaucoma patients who had difficulty seeing when driving increased as the disease progressed from early to middle to late stages, a result that is similar to our study. This should be taken into consideration in daily clinical practice by general ophthalmologists.

The patients’ driving ability was assessed using a driving simulator. There was no significant difference in the number of collisions in the DS or the horizontal and vertical spread of search between patients with and without subjective symptoms during driving. Horizontal spread of search has been noted to be reduced in novice drivers compared to experienced drivers.12 Glaucoma patients can observe hazardous events by increasing their visual search activity to compensate for visual field impairment, thereby avoiding collisions, as suggested by some studies.13,14,15,16 Our results imply that being aware of glaucomatous change, i.e., having subjective symptoms during driving, does not lead to safer driving, and that detailed explanations are necessary when teaching safe driving.

In the group with subjective symptoms, the mean retinal sensitivity of the superior IVF was decreased. Our results indicate that lower mean sensitivity in the superior IVF hemifield contributes significantly to subjective symptoms during driving. Yamasaki et al. 17investigated the association between driving self-regulation and glaucomatous visual field defect patterns. They reported that only IVF deterioration in the superior area was associated with driving avoidance at night, in rain, and in fog. This finding is consistent with our study. Since there are many objects in high locations that must be observed while driving, such as traffic signals and signs, a worsening superior IVF will lead to subjective symptoms during driving.

We previously reported that the inferior hemifield was associated with the incidence of MVCs with oncoming cars in patients with advanced glaucoma.9 However, the current findings suggest that many of these patients are unaware of their increased risk. In order to ensure safe driving for patients with visual field impairment, it is crucial to identify the specific areas of the visual field in which defects are associated with MVC involvement, considering that “few people have subjective symptoms while driving.”

To the best of our knowledge, this is the first report to study “subjective symptoms during driving.” We found that subjective driving symptoms in patients are associated with decreased superior IVF0-12 mean sensitivity. Since subjective symptoms play an important role in the management of glaucoma, we believe that our study will be useful in providing lifestyle guidance to glaucoma patients.

Our study has several limitations. First, it is based on self-reported “subjective symptoms during driving,” and lacks granularity as to which specific visual symptoms were associated with vision characteristics. In thinking about how this study may shape clinical practice and/or invite further study, we consider that it would be more useful to understand which specific symptoms are correlated with worsening clinical parameters, such as the mean retinal sensitivity of the superior IVF. However, it has been said that asking patients about their symptoms may optimize patient-physician communication, 7 so we believe that it is significant to focus on the “presence or absence of subjective symptoms during driving.” Second, because only patients at a driving assessment clinic were included, there is a potential of bias. The driving assessment clinic deals with patients with severe glaucoma, and better-eye MD in our patients was -11.83 ± 6.70 dB (range, -28.34–5.30 dB). Therefore, it is possible that our patients had more subjective symptoms during driving than glaucoma patients in general clinics. However, it is notable that only 41.7% of patients with severe glaucoma had subjective symptoms during driving. We should guide our patients with the understanding that few patients have subjective symptoms, even when driving.

In Japan, conditions such as epilepsy, dementia, and stroke are explicitly listed as “specified diseases that may impede safe driving and can be grounds for the revocation or suspension of a driver’s license.” However, eye diseases such as glaucoma or retinitis pigmentosa are not included in this category. Therefore, it is not mandatory for an ophthalmologist to report to the authorities if a patient seems unable to drive a car safely. Furthermore, it is likely that, as in other countries, many individuals with glaucoma may not be aware of their visual field impairment due to the lack of symptoms. This emphasizes that the issue of driving with undiagnosed glaucoma is not unique to Japan but may be a global concern.

In conclusion, we believe that our study is a valuable first step toward future, more precise investigations of patterns of visual field impairment that affect the ability to drive safely. An improved understanding of the subjective symptoms of glaucoma during driving will be helpful in glaucoma management.

Materials and methods

Subjects

A total of 227 glaucoma patients (109 patients at Nishikasai Inouye Eye Hospital and 118 patients at Niigata University Hospital) at a driving assessment clinic completed a written questionnaire. The questions were selected from a survey used at a Japanese driving license examination center (DLEC) 18; the questions asked about a range of aspects of driving habits and history (e.g., years since acquisition of first driving license, time spent driving per week) and self-reported motor vehicle accidents (MVAs) in the previous five years. Subjective symptoms during daily driving were defined as the presence of at least one of the following four items: difficulty seeing at night, difficulty seeing in the rain, difficulty seeing traffic signals, and fear of driving. The patients were examined at the Nishikasai Inouye Eye Hospital and the Niigata University Hospital between July 2019 and July 2022. Patients with other diseases with visual field impairment were not included in this analysis. All participants were active drivers who had driven within at least the previous 3 months and were currently licensed to drive in Japan, which requires either 1) binocular visual acuity of 20/30 or 2) monocular visual acuity of 10/30, with a minimum monocular visual field of 150 degrees horizontally on a modified Förster perimeter.

All participants received a complete ophthalmologic examination, including best-corrected visual acuity, a slit lamp examination, intraocular pressure measurement with Goldmann applanation tonometry, gonioscopy, a stereoscopic fundus examination, and standard automated perimetry with the Humphrey Visual Field Analyzer Swedish Interactive Threshold Algorithm–Standard 24–2 program (HFA 24–2: Carl Zeiss Meditec, Dublin, CA, USA) and the binocular Esterman program. The patients who had glaucomatous visual field defect in at least one eye were included in this study. The definition of glaucomatous visual field defects was based on the Anderson and Patella criteria. 19 We excluded patients with cataract or other non-glaucoma ocular diseases that could cause visual field defects after a basic ophthalmic exam. Participants were also excluded if they had unreliable visual fields, defined as fixation loss > 33%, a false-positive rate > 15%, or a false-negative rate > 20%. The severity of glaucoma was classified using the better-eye visual field mean deviation (MD) as follows: -6 dB or more (mild), from -6 dB or less to -12 dB or more (moderate), and -12 dB or less (severe). 19.

The binocular integrated visual field (IVF) was calculated by merging pairs of results from monocular HFA 24–2 tests. The patients’ best point-by-point monocular sensitivity was used20,21. We evaluated mean IVF sensitivity in the central area of the inferior and superior hemifields within 0º to 12º (IVF0-12) and within 13º to 24º (IVF13-24) of the fixation point.

Cognitive function was assessed to screen for potential cognitive impairment among participants using the Mini-Mental State Examination (MMSE). This test was developed by Folstein et al. in 1975 and is widely used as a brief screening test for dementia and as a measure of global cognitive function. The MMSE total score ranged from 0 to 30, with lower scores indicating poorer cognitive ability.22.

This study was performed following the principles outlined in the Declaration of Helsinki and was approved by the Inouye Eye Hospital Ethics Committee (approval number: 202109–4) and the Ethics Committee of Niigata University (approval number: 2015–2566). All patients provided written informed consent after receiving an explanation of the study procedures and possible risks.

Driving simulator

All participants in this study underwent DS (Honda Motor Co., Tokyo) testing with eye tracking (Tobii Pro Nano). The DS, previously described in detail,9 included 15 driving scenarios. The examinees undertook a 2-min practice session followed by the 5-min main test. The simulated car ran at a constant speed. The subjects had no steering wheel control and only applied the brakes when they felt in danger. If an examinee reported feeling simulator sickness during the practice session, further testing was immediately abandoned. The main test contained 15 scenarios depicting such situations as coming to a stop sign, traffic light, or road hazard, or another car suddenly rushing out in front. The number of collisions in all 15 scenarios was recorded.

Eye movements during DS testing were measured with eye tracking, and data for the horizontal and vertical spread of search12,23 were obtained from the standard deviation of the x and y coordinates, respectively, of eye movement during the 5-min test.

Statistical analysis

The patients were divided into two groups: those with subjective symptoms during daily driving and those without symptoms. Differences in demographic characteristics between the two groups were determined using the t-test, χ2 test, and the Wilcoxon rank-sum test. We assessed the relationship between glaucoma severity and the rate of subjective symptoms during driving using the Cochran-Armitage test.

We also performed a multivariate logistic regression analysis of the glaucoma patients. The dependent parameter was the presence or absence of subjective symptoms during driving and the independent parameters were age, driving exposure time, visual acuity, Esterman score, and mean sensitivity of the IVF subfields (analysis 1: the superior and inferior IVF0-12; analysis 2: the superior and inferior IVF13-24). All statistical analyses were made with JMP (version 14.0). P values less than 0.05 were considered statistically significant.

Author contributors

The authors who contributed to the design and conduct of the study were S.KS.; to the collection, management, analysis, and interpretation of data were S.KS, T.F.; and to the preparation, review, and approval of the manuscript was S.KS, T.F., M.T, A.M., K.I.