Fig. 5 presents various eye-tracking measures. Although the limited number of subjects does not allow a robust statistical analysis, several tendencies are found regarding the eye-tracking parameters. Glaucoma patients who passed the test had shorter fixation durations and increased number of fixations per minute when compared with glaucoma patients who failed the test. Such behavior indicates an increased scanning activity in glaucoma patients who passed. Furthermore, glaucoma patients who failed showed a lower ratio of horizontal to vertical fixations, indicating that their scanning behavior was primarily horizontal, whereas patients who passed performed more vertical scanning. In addition, a change in saccadic angle (saccadic orientation to x-axis) indicates a gaze shift because of compensation for the VFD.
Driving Performance Measures
Fig. 6 shows the average lateral lane position. The average lane position of control subjects was considered the optimal one, and in some cases, it deviated from the middle of the lane (curves and evasive driving). Glaucoma drivers did not show a different lane position when compared with the control group.
Time to Line Crossing
Fig. 7 shows the TLC for all participants. Regarding this parameter, which indicates steering stability, there were no differences between the patient group and the control group. Further steering steadiness measures such as lane position variance and steering reversals did not reveal clear trends either and are thus not depicted in the above figure.
The average speed is depicted in Fig. 8 and reveals that most patients do not have difficulties with identifying and keeping speed limits. However, glaucoma patients who passed the driving test drove slower (55 ± 25 km/h; control subjects, 59 ± 27 km/h) than patients who failed the driving test (63 ± 24 km/h), possibly indicating an attempt to increase safety.
Previous on-road and simulator studies7,17,29,30 on the driving ability of subjects with binocular visual field loss either reported the percentage of patients who were fit to drive without recording their eye and head movements or evaluated various aspects of driving behavior (i.e., hazard detection, lane keeping, steering, and head scanning), but without linking them to a driving test outcome measure. This means that patients with glaucoma were usually averaged as one group compared with normal subjects, although there is evidence for differences regarding gaze strategies and several driving components between patients who are fit to drive and patients with unsafe driving behavior. Hence, we tried to identify gaze scanning patterns and driving performance measures associated with successful completion of a simulated driving test.
Fitness to Drive
In the present simulator test, three out of six participants with glaucoma demonstrated a safe driving performance, despite the presence of VFDs within the central 30-degree visual field and the fact that they did not meet the legal requirements for driving. This study included only participants with binocular glaucomatous visual field loss, which would disqualify them from obtaining a driver’s license in many jurisdictions; therefore, our inclusion criteria might be less favorable than in other studies and our sample is not representative of the general glaucoma population. The reason was that we hypothesized that any potential gaze strategies would be more evident in the group with binocular glaucomatous visual field loss. We, thus, aimed to investigate whether patients with binocular VFDs are at increased risk for motor vehicle collisions, as suggested in previous studies based on self-reports and police charts.10,31
The first driving simulator study by Szlyk et al.17 in 2002 with glaucoma patients suggested that there were no significant differences for self-reported and simulator accidents between patients with mild to moderate glaucoma and a normal control group. Our results appear to be at odds with those findings, possibly because in the Szlyk et al. study, many patients had normal or near-normal visual fields in their better-seeing eye. The present results appear to be more consistent with a later study by the same authors, where they found a higher incidence of real-world and simulator accidents for a group with more advanced glaucoma.11 Our findings also appear consistent with a study by Coeckelbergh et al.,32 where 43% of patients with peripheral VFDs passed an on-road test (retinitis pigmentosa and glaucoma; binocular horizontal visual field extent, 84 [±35] degrees). Similar pass rates for patients with binocular glaucomatous visual field loss (40%) were obtained in our recent on-road test, which was also scored according to the German driving license regulations and included patients with similar advanced bilateral glaucomatous VFDs.19 Haymes et al. also found that 60% of glaucoma patients compared with 20% of control subjects had one or more at-fault critical interventions by the driving instructor.33
Gaze Patterns (Head Movements)
A few studies have assessed eye and head compensatory strategies in patients with glaucoma.19,32 We found that glaucoma patients who were safe to drive showed increased exploration activity in terms of more eccentric head movements, compared with glaucoma subjects who failed the test. Thus, the present simulator study replicated the findings of our recent on-road study and the study of Coeckelbergh et al.32 by means of sophisticated eye and head tracking and suggests that active scanning by means of head movements is an efficient way to compensate for a glaucomatous VFD affecting the binocular visual field.19
Gaze Patterns (Eye Movements)
Unsafe glaucoma drivers displayed a tendency for shorter saccadic amplitudes, a gaze bias to the right, and a more straight-ahead eye position. Increased gaze concentration toward the road center with increasing cognitive load, a phenomenon commonly coined as “tunnel vision” or ”cognitive tunneling,” was reported by Engström et al.34 in a driving simulator study and may suggest defective compensational mechanisms in patients who failed the test.
These findings are at odds with a recent simulator study, which showed that patients with mild to severe glaucoma displayed similar eye scanning behavior with the control group.35 However, the horizontal field of view in the above study was considerably smaller than that in the present study, only 9 of 23 participants had binocular field loss, the driving session lasted considerably shorter, there was no other traffic apart from static obstacles, and the detection task included targets that are not part of a driving scene, namely, verbalization of letters. Our results regarding longer saccadic amplitudes and more lateral eye position in safe drivers are more consistent with recent studies using video-based hazard perception tasks.18 The authors also reported that patients with binocular glaucomatous VFDs performed more eye movements than control participants.18 An increase in saccade rate in patients with glaucoma was also associated with better performance in a search task when viewing images of everyday scenes.36 A recent study investigating the viewing behavior of patients with binocular glaucomatous VFDs during a supermarket shopping task in a real setting reported that an increase in saccade rates strongly correlated with the ability to quickly find the objects of interest, probably an attempt to compensate for their restricted field of view.37
Additionally, patients who failed the test showed a tendency for longer fixation duration and less fixations per minute compared with patients who passed the test. The smaller number of fixations indicates decreased eye scanning activity, and longer fixation duration appears to be associated with an inability to acquire visual information in a quick and effective manner, as observed in patients who passed the test. Because new information is acquired during fixations, the finding that patients who failed made fewer saccades suggests that they were unable to process as much of the visual scene as patients who passed the test. In a recent study,36 patients with glaucoma had longer average fixation duration compared with control subjects when viewing everyday scenes. However, the latter study did not correlate gaze parameters with performance and the nature of the task was substantially different from the present one, as cognitive demands were minimal in that participants were presented with static, consistent information and were tasked to simply “enjoy” the images.36 Conversely, our results are more consistent within another study regarding eye movement behavior when viewing a dynamic driving scene. In the latter study, glaucoma patients produced more and, thus, shorter fixations than the control subjects when searching for hazards in the Hazard Perception Test.38 Hence, viewing behavior appears to be related not only to compensatory potential but also to the task complexity and quantity of visual information.
Interestingly, unsafe glaucoma drivers in our study showed a gaze bias to the right. This was probably an attempt to maintain a stable lane position, because no differences in lane position were found between safe and unsafe drivers. This is in line with Vega et al., who attributed this finding to the optimal control theory of manned-vehicle systems.39,40 A possible explanation is that safe glaucoma drivers paid more attention to avoiding traffic hazards (by gaze scanning), whereas unsafe glaucoma drivers attempted to maintain a stable lane position but failed to recognize traffic hazards because of limited gaze compensatory reserves.
Driving Performance Measures
Lane keeping difficulties and steering unsteadiness in glaucoma patients have been reported more often in on-road studies than in simulator studies. In accordance with previous studies,17 TLC and lane position were similar between glaucoma patients and control participants, probably because of behavioral hypervigilance in the patient group. In contrast to our findings, another simulator study reported that 89% of patients with peripheral VFDs (glaucoma and retinitis pigmentosa) made more lane boundary crossings.39 However, those authors did not include a normal control group or a separate subgroup analysis for glaucoma patients.
Speed control and adaptation to the speed limit is an important skill. Some drivers with glaucoma may try to compensate for their degraded visual ability by reducing their driving speed. We found that safe drivers drove at slower speeds and this strategy possibly provides enough time to scan their visual environment, because eye movements and especially head movements are time-consuming. However, very slow driving can be dangerous, because the vehicle may represent an obstacle for the other drivers.32 Other on-road studies reported adequate speed control in glaucoma subjects, and because of the variable results, we believe that this skill warrants further investigation in larger series of patients.19,33
Despite the total number of 14 participants in this costly study, the number of subjects in each subgroup was relatively small for statistical analysis. Additionally, although we have tried to design and score the driving test as close to real-world conditions as possible, effects arising from the use of a simulator in a virtual environment with a variable degree of fidelity cannot be avoided. We decided to do the experiment in the simulator because of the unique possibility of standardizing the traffic scenario and thereby establishing identical and thus comparable driving conditions for all participants. Finally, the severity of VFDs varied between patients from severe visual field loss to small circumscribed areas. However, a common characteristic was that they fail to meet the European driving regulations.
In conclusion, this study supports the hypothesis that a considerable subgroup of subjects with binocular visual field loss attributed to glaucoma shows a safe driving behavior in a virtual reality environment, because they adapt their viewing behavior by increasing scanning. By means of a driving simulator and sophisticated eye and head tracking, individual performance differences in terms of driving safety were related to visual exploratory behavior. This type of compensation improves traffic safety and may have practical implications in planning individualized driving fitness tests and driver rehabilitation programs.
Department of Computer Engineering
University of Tübingen
Thomas C. Kübler and Enkelejda Kasneci contributed equally to this article.
The authors thank Pfizer and MSD Sharp & Dohme GmbH for supporting and enabling this study. The authors further thank Daimler AG for the use of the moving-base driving simulator, driving instructor Helmut Hanne, and clinicians Christian Heine and Kai Januschowski. The second author gratefully acknowledges financial support from the Margarete-von-Wrangell program of the MWK Baden-Württemberg.
Received September 5, 2014; accepted April 10, 2015.
The Appendix, demographic data and visual fields of glaucoma patients, is available at http://links.lww.com/OPX/A222.
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glaucoma; driving fitness; compensatory gaze; head movements; driving simulator
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