Peripheral vision and hazard detection with average phakic and pseudophakic optical errors

: The impact of peripheral optical errors induced by intraocular lenses was evaluated by simulating the average phakic and pseudophakic image qualities. An adaptive optics system was used to simulate the optical errors in 20° nasal and inferior visual field in phakic subjects. Peripheral resolution acuity, contrast sensitivity and hazard detection were evaluated. Pseudophakic errors typical for monofocal designs had a negative effect on resolution acuity and contrast sensitivity and the hazard detection task also showed increased false positive and misses and a longer reaction time compared to phakic optical errors. The induced peripheral pseudophakic optical errors affect the peripheral visual performance and thereby impact functional vision.


Introduction
Intraocular lens (IOL) implantation following cataract extraction is the most common ophthalmic surgical procedure across the world. The IOL designs are constantly evolving and the postoperative visual outcomes are also improving significantly [1][2][3]. However, these reported outcomes are measured mainly for the central vision. Similar to other forms of vision correction such as spectacle lenses and contact lenses, IOLs are also designed to provide optimal image quality in the central visual field.
Both theoretical and experimental evidence suggest that the peripheral optical errors are larger in eyes implanted with spherical and aspherical monofocal IOLs than phakic eyes [4][5][6][7]. Tabernero et al., reported an increase in the peripheral optical errors by analysing eyes that were implanted with monofocal IOLs from a variety of manufacturing companies and different optical designs, both spherical and aspherical [4]. The gradient index of the crystalline lens in the phakic eyes is suggested to partly compensate for the peripheral corneal astigmatism and the replacement of the crystalline lens with an IOL of constant index therefore results in higher peripheral astigmatism [7]. Additionally, the peripheral average optical error is shown to be more myopic with an increased astigmatism in pseudophakic eyes [4,7]. It is not yet known how these increased peripheral optical errors affect the peripheral functional vision in eyes implanted with monofocal IOL compared to the phakic condition in non-cataract eyes.
The main limitation in peripheral vision is the neuronal sampling density and this determines the high contrast resolution acuity [8,9]. However, peripheral optical errors affect other forms of vision such as detection and low contrast resolution [10], which are important for normal functional vision. In phakic eyes, astigmatism increases quadratically with eccentricity [11,12]. The further increase in peripheral astigmatism in the pseudophakic eye may have an impact on peripheral visual function and affect functional vision. Furthermore, the quality of the optical image on the peripheral retina is of special importance for people with macular degeneration and dysfunctional central vision [13][14][15].
Considering the effect of proper peripheral optical correction in improving vision in macular degeneration subjects, IOL designs can be further optimized to provide improved peripheral image quality. The optimal solution would be to have a customized lens design that corrects the optical errors in the peripheral preferred retinal locus of individual subjects. Alternatively, lens designs that provide population average phakic image quality could also be a viable solution. The peripheral visual benefits of such IOL designs compared to other monofocal IOL designs can be investigated by simulating the corresponding off-axis errors using an adaptive optics vision simulator [16]. A target image quality can be achieved by continuously monitoring the ocular wavefront with a Hartmann-Shack system and by modifying the wavefront continuously using a deformable mirror. In the present study, we evaluated peripheral vision in young phakic subjects with average phakic and monofocal pseudophakic peripheral optical errors simulated with an adaptive optics system. The vision evaluations were performed in both the nasal and the inferior visual fields to understand the effect of pseudophakic peripheral optical errors and their impact on functional vision. Three different vision tasks were evaluated with both simulated optical conditions. High contrast resolution and contrast sensitivity evaluations were performed in the nasal and the inferior visual field. Additionally, a hazard detection task was developed and performed in the nasal visual field.

Simulated optical errors
An adaptive optics system custom-designed for peripheral vision measurements was used to simulate average phakic and pseudophakic image qualities in the peripheral visual field. The system was set to run in continuous closed-loop to maintain the intended image quality throughout the measurements with each condition, which means that the image quality for a certain condition was the same in all eyes irrespective of the natural aberrations of the individual eye. The main components of the system are, a Hartmann-Shack wavefront sensor (HASO 32, Imagine Eyes, France), an electromagnetic deformable mirror (MIRAO 52d, Imagine Eyes, France) with 52 actuators, and a CRT monitor for presenting visual stimuli. A detailed description of the adaptive optics system can be found in previous literature [16]. Peripheral vision was evaluated in 20°n asal and 20°inferior visual field for each subject with the different simulated image qualities. The following population average peripheral optical error in phakic and pseudophakic eyes was used to simulate the peripheral image quality: • Phakic errors in the 20°nasal visual field: −0.60 D in mean spherical error, −0.50 D in J0 (i.e. a −1 D cylinder with axis 90°) and horizontal coma corresponding to 0.09 µm for a 4 mm pupil diameter [17].
• Phakic errors in the 20°inferior visual field: −0.60 D in mean spherical error, 0.50 D in J0 (i.e. a −1 D cylinder with axis 180°) and vertical coma corresponding to 0.09 µm for a 4 mm pupil diameter.
• Pseudophakic errors typical for monofocal IOL designs in the 20°inferior visual field: −1.20 D in mean spherical error, 1.45 D in J0 (i.e. a −2.90 D cylinder with axis 180°) and vertical coma corresponding to 0.09 µm for a 4 mm pupil diameter.
Because the optical errors in the vertical field behave similarly as a function of angle as in the horizontal field [18], the same magnitude of optical errors were simulated in both fields and only the direction of astigmatism and coma were altered. For the simulation, the intended optical errors were converted to Zernike polynomials and set as target values in the adaptive optics system. The vision measurements were initiated once the closed-loop correction had stabilized. The wavefront was continuously monitored throughout the vision measurements and in case of any deviations from the targeted wavefront the measurements were reset and started again. Trial lenses were used to compensate for foveal refractive error, if any.

Subjects
Eleven phakic subjects aged between 27 and 47 years participated in the study. The subjects had no known ocular disorders and had best corrected decimal visual acuity of 1,0 or better. None of the subjects had foveal refractive error higher than ± 4.00 DS and −0.5 DC (Subjects 3,6 and 9 were myopes, subject 2 was hyperope and the rest were emmetropes). The study protocol adhered to the tenets of the Declaration of Helsinki and was approved by the regional ethics committee and informed consent was obtained from all subjects.

Vision evaluation
High contrast resolution acuity and contrast sensitivity at 1 cpd were measured in 20°nasal and 20°inferior visual field with both optical conditions. A Maltese cross was used as foveal fixation target and the stimuli for peripheral vision test were presented on a calibrated CRT monitor seen through the adaptive optics system (Fig. 1). The vision evaluations were performed monocularly. The stimuli were sinusoidal Gabor gratings (σ = 1.6°) oriented along the 45°or 135°meridian presented on the calibrated 10-bit grayscale CRT monitor. The mean luminance of the screen was 50 cd/m 2 . The stimulus presentation time was 500 milliseconds. The spatial frequency and the contrast of the gratings were varied to determine the acuity cut-off and the contrast sensitivity, respectively. Contrast sensitivity was evaluated at spatial frequency of 1 cycle/degree. Each measurement had 40 trials. The stimuli were presented in a two-alternative forced choice algorithm utilizing the Bayesian Ψ-method [19]. The subject's task was to identify the orientation of the presented grating and respond with the corresponding key on a keypad. The psychophysical algorithms were implemented in Matlab and Psychophysics toolbox [20]. All the measurements were performed with natural pupils and the optical errors were simulated according to the natural pupil size.
In addition to the resolution acuity and contrast sensitivity measurements, a hazard detection task was developed and performed in the 20°nasal visual field. For this task, we used a stimuli set that contained ten animals, and five rocks and five trees (Fig. 2). The subject had to detect if the approaching stimuli shown in the periphery is a hazard (animals) or not a hazard (rocks or trees), while fixating foveally on a video containing a night-time driving scene on a mountain road. On the stimulus presentation CRT monitor, the different stimuli (hazards and non-hazards) were shown on a neutral grey noise background. The stimuli were presented in a random order. The stimulus presentation time was 4 seconds and the stimuli size changed gradually from 0.8°t o 4°under this time in order to mimic an approaching stimulus during driving situation. This corresponds to hazard visible from about 75-meter (246 feet) distance while driving towards it at 50 km per hour (31 miles per hour). The subject's task was to differentiate if the presented stimulus is a hazard (an animal) or not and press a button (to brake) if it is an animal. Three different parameters were calculated, false positives (Percentage of rocks or trees wrongly identified as animals), misses (Percentage of animals that are missed) and reaction time (Average time taken to detect the animals and press the brake-button).
The nasal and inferior visual field measurements were performed on separate days. The nasal visual field measurements were performed on the left eye and the inferior visual field measurements were performed on the right eye. The foveal fixation target and stimulus presentation set up for both the measurement field are shown in Fig. 1. All the measurements were performed with three repetitions for the nasal visual field and with two repetitions for the inferior visual field. The difference in the number of repetitions is due to the difficulties in fixation upwards during inferior visual field measurements. The optical conditions were randomized for all the measurements. The vision evaluation parameters from the phakic and pseudophakic conditions from the same location were compared with the Wilcoxon paired sample signed-rank test and a significance level of 5% was chosen. The standard error of the mean difference between the two optical conditions was also calculated.

Results
The individual subject's resolution acuity and contrast sensitivity for the two different optical conditions and the two different visual field locations are shown in Fig. 3. Both resolution acuity and contrast sensitivity varied significantly (p<0.05) between the two optical conditions in both visual field locations. The simulated peripheral pseudophakic optical errors had a negative effect on both resolution acuity and contrast sensitivity compared to the phakic optical errors.
On average, the resolution acuity in the 20°nasal visual field was 0.12 and 0.10 with the phakic and pseudophakic optical errors. This corresponds to a difference of 0.08 logMAR with a standard error of 0.02 between the two optical conditions. In the 20°inferior visual field, the average resolution acuity was 0.13 and 0.09 with the phakic and pseudophakic optical errors, corresponding to a change of 0.15 logMAR with a standard error of 0.02.
On average, the log contrast sensitivity in the 20°nasal visual field differed by 0.25 with a standard error of 0.06 between the phakic and pseudophakic optical errors. In the 20°inferior visual field, the average difference was 0.29 with a standard error of 0.06.
The false positives, misses and reaction time measurements from the hazard detection task in 20°nasal visual field is shown in Fig. 4. The false positive and miss percentages varied among the subjects ranging from 0% to 23% with the phakic condition. On average, the false positives increased significantly by 8.2% (standard error, 1.8%) and the misses increased by 12.7% (standard error, 3,7%) with the pseudophakic optical errors. The reaction time also increased by 284 milliseconds (standard error, 94 milliseconds) with the pseudophakic optical errors.

Discussion
Peripheral vision was evaluated with induced average phakic and pseudophakic optical errors at 20°nasal and inferior visual field. Overall, peripheral visual performance with pseudophakic optical errors typical for monofocal IOL designs were clearly reduced compared to the average phakic errors for all subjects.
The present results indicate that peripheral optical errors induced by IOLs can have a negative impact on both high contrast resolution acuity and contrast sensitivity. The reduction in contrast sensitivity was expected as even small amounts of optical errors affect peripheral vision under low contrast conditions [21]. The induced pseudophakic optical errors are larger (about 3 D in cylinder in both 20°nasal and inferior visual field) and therefore our results show a negative impact even for high contrast resolution acuity.
We have evaluated the ability to distinguish hazards and non-hazards with peripheral vision in a simulated condition for driving. Our results show that the performance with the pseudophakic condition was reduced compared with the phakic condition. In addition to the increased false positives and misses, the pseudophakic condition also showed an increased reaction time. Based on the assumed driving speed of 50 km per hour (31 miles per hour), increase in reaction time by 284 milliseconds corresponds a difference of 5 meter (16.4 feet) in detecting the hazard between the phakic and pseudophakic conditions. Though the peripheral high contrast resolution is mainly limited by neural factors, the functional vision goes beyond just the high contrast resolution and can have larger impacts due to optical errors.
The resolution acuity and contrast sensitivity values with average peripheral phakic optical errors reported in the present study are closer to that of previously reported values evaluated with the individuals' own aberrations in the 20°visual field [22,23]. All eleven subjects showed a reduction in peripheral vision with pseudophakic optical condition irrespective of their refractive error. Though we have measured only in younger subjects with no ocular pathologies, we can expect that older subjects will also have a similar tendency. The present results are based on monofocal IOL designs, and the effect may therefore be different for multifocal IOL designs.
It is well known that reduced vision is the major risk factor that increases the possibility of falls and fracture in older people [24,25]. The impact of pseudophakic optical errors should be considered as it reduces the peripheral visual performance which is important for orientation and mobility. In the hazard detection task, the detection reliability reduced with the pseudophakic condition which was shown as increased false positives, misses and reaction time. Failure to detect the hazards and increased reaction time in real life situations can lead to problems in orientation and mobility. Further studies are recommended to evaluate the impact of peripheral optical errors on various aspects of mobility and orientation.
The results of this study may be of even larger importance for people without normal central vision. Previous studies have shown that peripheral low contrast resolution acuity is improved with proper optical correction in subjects with macular degeneration and that the improvement can be larger compared to people with normal macular function [26][27][28][29][30]. However, these studies involved younger phakic subjects with macular degeneration. Age-related macular degeneration (AMD) is the most common cause of vision loss in developed countries, especially for people over 50 years of age, and is estimated to affect 196 million people worldwide in 2020 and increasing to 288 million in 2040 [31]. Due to age, persons with AMD are often also candidates for cataract surgery with lens replacement [32]. As these people rely more on their peripheral vision than pseudophakic people without comorbidities, the peripheral optical errors induced by an IOL may have a larger impact on people with AMD.
In conclusion, the induced peripheral pseudophakic optical errors affect the peripheral visual performance of younger subjects with normal central vision compared to the average phakic peripheral optical errors. Though the IOL implantation after the removal of the cataractous crystalline lens is proven to be effective in restoring foveal vision, the present results emphasize the need for further improvements in the optical design of IOLs to control the optical errors in the periphery. This improvement in peripheral vision will be beneficial in terms of better functional vision in subjects with normal central vision and might facilitate functional vision in subjects with central vision loss even more.