Virtual Reality Enables Rapid and Multi-Faceted Retinal Function Screening

doi:10.21203/rs.3.rs-2011868/v1

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Virtual Reality Enables Rapid and Multi-Faceted Retinal Function Screening

https://doi.org/10.21203/rs.3.rs-2011868/v1

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Background: Given global population growth and aging, it is imperative to prioritize early eye disease detection and treatment. However, the current eye specialist workforce capacity is not bridging the growing gap, making it important to consider alternative solutions for increasing eye screening capabilities. This study compared virtual reality (VR) vision screening exams that help evaluate retinal health, such as 24-2 perimetry, Ishihara color blindness, and Amsler grid tests, against their in-clinic counterparts.

Methods: 86 subjects were recruited from Mount Sinai’s ophthalmology clinic for a head-to-head comparison trial that was internally controlled across healthy controls and eyes with glaucoma and retinal disease.

Results: Perimetry results from Humphrey Visual Field Analyzer (HVFA) and VR suprathreshold testing demonstrated a good sensitivity both overall (80% OD, 84% OS) and across control (86% OD, 89% OS), glaucoma (69% OD, 78% OS), and retinal disease (76% OD, 80% OS) groups. A Garway-Heath anatomical map showed an overall 70-80% agreement. Ishihara plate tests did not show a significant difference between the two testing modalities (p = 0.12; Mann-Whitney U test), which remained true across groups. Amsler grid testing differences were also non-significant (p = 0.81; Mann-Whitney U test), including each subgroup. Patient time required to complete VR exams was significantly improved (p<0.0001; Wilcoxon) compared to the gold standard tests.

Conclusions: All VR tests showed high sensitivity and percent agreement compared to in-office standards, indicating a promising potential for VR technologies in visual function screening for early identification of prevalent diseases such as glaucoma and retinal conditions.

A general lack of vision specialists and a growing need for vision care that was accentuated by the COVID-19 pandemic contributes to a rising prevalence of undiagnosed, advanced vision disorders.^1–5 In the United States alone, it is estimated that 1.5 and 2 percent of the 40 + year-old population suffers from age-related macular degeneration (AMD) and glaucoma, respectively.^6,7 In the developing world, CMV retinitis presents a high disease burden with a 5–15% of those afflicted developing blindness.⁸ Furthermore, lower socioeconomic status has been associated with more advanced visual function loss in glaucoma and AMD at the time of diagnosis.^9–11 Local availability of specialized vision testing leads to faster disease identification/awareness and successful treatment of retinal diseases like diabetic retinopathy (DR) and AMD.¹²

Several studies have demonstrated the clinically meaningful benefits of empowering adult vision screening or monitoring in a primary care or community setting, particularly in identifying irreversible retinal diseases that could require immediate ophthalmic intervention, such as glaucoma, DR, and AMD.^13,14 The benefits of implementing each test independently of a complete eye examination in a primary care setting have been variable. For example, mixed outcomes have been found for acuity testing in underserved or older populations.^15–18 However, screening tools that can detect functional vision impairment to ensure early-stage treatment have shown more promise. Such tests range from relatively sophisticated technologies, such as tonometers, to growingly available functional technologies, such as perimetry and Amsler grid tests.^19–24 Benefits have also been observed from early treatment and identification of AMD and DR using manual ophthalmoscopy or portable fundus photography and Amsler grid testing.²⁵

Given that many neurologic and endocrine conditions manifest in the eyes, multimodal vision testing tools such as color vision and scotoma testing can enhance a screening potential for these conditions.²⁶ As with the ophthalmic diseases discussed above, non-ocular conditions such as multiple sclerosis, pseudotumor cerebri, cerebral neoplasms, and cerebrovascular accidents have a higher rate of treatment success with early detection and treatment.

Performing rapid vision testing across various clinical environments requires a portable, fast, and easy-to-use technology that allows administration of several vision function exams from the same device.¹² Integrating a series of retinal health screening exams into one platform would allow for multimodal functional testing that can localize abnormalities to a specific anatomical area of the retina while allowing for improved user feasibility within a single device platform.

Ophthalmic tests have successfully been adopted on portable devices such as tablets and virtual reality (VR) headsets.^27–32 To contribute to this progress, our group developed a platform that provides a more comprehensive vision screening method to evaluate retinal health by developing a battery of VR vision tests that are analogous to ophthalmic in-office tests. This study compares the performance of VR analogues (24 − 2 suprathreshold perimetry, Ishihara Tiles, and Amsler Grid tests) against their in-office standards. The primary outcome measure of this study was evaluating outcome similarities between each modality in healthy eyes and those with glaucoma and retinal abnormalities. Secondary outcome was the test time to complete perimetry exam.

Overall Study Design

This study was approved by the Institutional Review Board (IRB) of the Icahn School of Medicine at Mount Sinai (IRB #19–00679). Patient recruitment was conducted at the Mount Sinai 102nd Street ophthalmology clinic on a voluntary basis with randomization of either the clinical gold standard exams followed by the VR counterpart or vice versa. Patients were then stratified into either healthy controls or disease groups for a glaucoma or retinal disease diagnosis. Glaucoma group consists of mild, moderate, and severe stages of primary open angle glaucoma. Retinal group has patients with many posterior chamber diagnoses, including macular degeneration, diabetic retinopathy, retinal tears, detachments, scars, macular changes with drusen, optic nerve head drusen, optic atrophy. Patients with both glaucoma and retinal disease diagnoses (N = 6 patients) were included in each disease group. Table 1 breaks these groups down by age, gender and ethnicity.

Due to factors such as time-restraints or workflow restrictions, not all patients completed all three exams (both in-clinic and VR analogues), resulting in different numbers of participants per test. A comprehensive diagram of the patient data funnel is shown in Fig. 1. Patients’ data were only included for a particular test if they completed both the in-office and VR versions. The time taken to complete perimetry testing was recorded automatically by the Humphrey and VR devices.

VR Hardware and Software

A PICO Neo Eye 2 commercial VR headset was used to demonstrate the hardware-agnostic performance of the three VR tests. This headset has a 4K screen resolution, controllers, and Tobii eye tracking. Eye tracking capabilities are essential for ensuring that the patient’s gaze stays focused on the central target, thereby producing reliable visual field perimetry results. Software was written in Unity Version 2020.3.2.f1 with SDKs on software websites. Tobii Eye tracking technology and SDKs were implemented. Steam VR was used to monitor the progress of the patient during VR testing. At any time, the patient could terminate the exam if they experienced any discomfort.

In-Office Standard Tests

A 24 − 2 perimetry test was conducted on a Humphrey Visual Field Analyzer (HVFA) by trained technicians. A full-threshold 24 − 2 HVFA test was used for increased rigor in comparison to our suprathreshold VR exam, as our group prioritized the effect of increased speed during examinations. For red-green color deficit testing, red-green color and control tiles from a physical Ishihara book were used. For the Amsler Grid, a paper form and pen were given to a participant to draw or circle any abnormalities, such as distortions, holes, vision gaps, and wavy lines. All results were securely uploaded and encrypted on a folder with patients de-identified.

Design of VR Tests Compared to Clinical Standards

The VR analogue for the 24 − 2 perimetry test (VR 24 − 2) was designed with an unchanging stimulus intensity at 25 Apostilibs with 15 non-stimulus points (a point is not shown), testing each point only once. The points were mapped in accordance with the 24 − 2 degrees from the center to minimize the time required to complete the exam. The results of VR 24 − 2 were compared to Humphrey results on a point-by-point analysis to determine % agreement. Eye tracking deviation calibration was performed to equivocate Unity meters to degrees. The four cardinal positions of gaze (left, right, top, bottom) were determined to be 0.4 Unity meters in each direction of the 24-degree field, and thus each 0.1 Unity meter is about 6 degrees, which is an approximate area of the blind spot. Thus, any gaze deviation > 0.1 Unity meters was considered a true deviation. A Garway-Heath Analysis was applied to both 24 − 2 perimetry results to further characterize the VR analogue’s performance based on optical nerve fibers and its percent agreement with Humphrey 24 − 2 results. Patients were encouraged to undergo perimetry testing on both eyes; however, due to time constraints or workflow restrictions, many patients could only perform the test on one eye.

For color deficit testing, a standard red-green/control 12-tile screening was implemented under pre-set VR illumination conditions similar to an office setting were quantified using a light meter. Both the PICO and the VIVE headsets at white-light settings on maximum brightness outputted around 250 nits. Specific tiles testing for red-green color blindness were the focus of analysis rather than magenta-grey controls for a diseased state. Numeric answer choices were presented in a multiple-choice format.

A virtual pen and standard Amsler grid were provided in a virtual environment, with any dysmorphia counted as a “pathologic” result. The patients were asked to color in or circle areas with wavy lines, distortions or spots. The total amount of visible squares in a 20x20 grid was calculated for comparison.

Statistical Analysis

All statistical analyses were conducted in R-4.0.4. Perimetry percent agreement graphs were made with the ggplot2 package and qplot function in R, with sensitivity and specificity calculations used to assess statistical differences in perimetry results between modalities. Mann-Whitney-U (with an alpha value set to 0.05), sensitivity, specificity and accuracy calculations were used to determine the statistical differences for color blindness and Amsler grids tests. Welch’s t-tests were used to compare HVFA testing times against those of VR 24 − 2 and a Wilcoxon signed-rank test compared patient satisfaction between the two testing modalities.

Perimetry

A total of 86 patients were recruited from the Mount Sinai 102nd Street Ophthalmology Clinic. N = 102 eyes completed VR 24 − 2 perimetry and gold standard testing; their results showed 80% sensitivity, 42% specificity in the right eye (n = 43 eyes) and 84% sensitivity, 59% specificity in the left eye (n = 41 eyes) compared with HVFA results (Table 2). When stratified by control (86% OD, n = 16 eyes; 89% OS, n = 15 eyes), glaucoma (69% OD, n = 11 eyes; 78% OS, n = 11 eyes), and retinal disease (76% OD, n = 16 eyes; 80% OS, n = 15 eyes) groups, the sensitivity remained high (Table 2).

VR results underwent Garway-Health analysis. Sensitivity varies by structural region, with all the outcomes listed in Table 2. It is important to note that the quadrant with highest percent sensitivity at a 25 Apostilib threshold is the central part of the retina for the overall (92% OD, 96% OS), control (96% OD, 99% OS), glaucoma (82% OD, 93% OS), and retinal disease (94% OD, 96% OS) groups.

When looking at the percent agreement heat map in Fig. 2, the central retina has the highest agreement percentage. Overall (n = 43 OD, n = 41 OS), patients exhibited > 80% agreement for both eyes, with superior arcuate fibers being the weakest region. For controls (n = 16 OD, n = 15 OS) the central field agreement was generally > 90%, while the superior and inferior arcuate fibers of the outer rim showed the most disagreement in the right eye (60–80%); only superior arcuate fibers showed disagreement on the left eye (40–80%). Eyes with glaucoma (n = 11 OD, n = 11 OS) showed high agreement centrally, ranging from 60–90%. The weakest areas were the superior outer rim for the right eye (40–80%) and the inferior outer rim for the left eye (30–80%). Eyes with retinal disease (n = 16 OD, n = 15 OS) followed a pattern similar to other groups, with the central fields showing 80–100% agreement and peripheral fields displaying 40–70% agreement of the right eye and 60–80% of the left. Notably, disagreement in left eye field was more pronounced than the right.

Ishihara

N = 116 eyes underwent both in-office and VR test versions of color testing. No significant difference was observed between the two modalities overall (p = 0.12, U = 1253.5), with sensitivity = 100%, specificity = 79%, and test accuracy = 82% (Table 3). Differences between results were also non-significant among the control and disease groups, including eyes with glaucoma and retinal abnormalities. Control eyes showed 100% sensitivity and 89% specificity with 89% accuracy and non-inferior testing (p = 0.49, U = 324). Glaucomatous eyes displayed 100% sensitivity, 45% specificity, and 57% accuracy, while also demonstrating inter-test comparability (p = 0.051, U = 55). The retinal disease group showed 100% sensitivity, 89% specificity and 93% accuracy (p = 0.8, U = 92).

Amsler grid

Amsler grid testing of N = 108 eyes showed no significant difference between the two tests (p = 0.81, U = 4514.5); sensitivity = 100%, specificity = 98%, and accuracy = 98%) as shown in Table 4. When comparing the controls and disease groups, the VR test remains non-inferior for the control (p = 0.74, U = 1352.5), glaucoma (p = 1, U = 264), and retinal disease groups (p = 0.99, U = 200). The sensitivities were 100% for each respective group while specificity varied slightly with 96% for control and 100% for diseased groups. Accuracy was 96% for the control group and 100% for the glaucoma and retina groups.

Exam Efficiency Measured

When asked to testing speed, the time required to complete the HVFA was 336.2 seconds per eye and was significantly longer compared to the VR perimetry time of 86.7 seconds, as expected with a suprathreshold examination (p < 0.0001; Welch’s t-test). Given that the HVFA used in this study was a full field perimetry exam, the threshold version takes approximately half the time, which would be 168.1 seconds per eye. The time difference between each test remains significant (p < 0.001; Welch’s t-test).

Global vision testing disparities necessitate the introduction of validated, affordable screening and diagnostic technologies that are developed or adapted for ocular testing, such as VR headsets, to address the problem. To-date, few groups have performed direct comparison using several VR vision screening tests against in-office standards within a single clinical trial. In the present study, our group performed a non-inferiority trial between in-office and VR analogues of 24 − 2 perimetry (HVFA vs. suprathreshold single contrast value), Ishihara (book vs. multiple choice), and Amsler grid (paper vs. digital free-handing) tests.

All three VR tests showed high sensitivity compared to in-office tests, although VR perimetry performance showed some level of geographical dependence on a Garway-Heath map. The central field showed the highest percentage sensitivity and agreement between the VR and HVFA results at a 25 Apostilb threshold. Overall, perimetry VR results have a moderately high sensitivity that remained after patients were stratified into control and disease groups for glaucoma and retinal diseases. It is important to note that control eyes had higher sensitivity than glaucoma and retinal disease eyes, suggesting that this technology can serve as a screening device. Additionally, in the glaucoma group, the superior and inferior nasal regions that are known to provide a characteristic pattern of glaucomatous field loss have the highest overall sensitivity.³³ On the other hand, the retina group had a high percent sensitivity in the central region of the field that is known to be most at-risk in conditions such as macular degeneration.³⁴

VR analogues of Ishihara and Amsler tests also proved comparable to gold standards in overall and within both healthy control and disease groups. Of note, while each group had high sensitivity, the specificity and accuracy did vary, with the glaucoma group having the lowest figures. This could be due to peripheral vision field loss interfering with answer selection since each answer choice is positioned inferior to the Ishihara letter on the screen.

The transition to value-based care in the United States has emphasized empowering as well as financially and technically supporting primary care providers. Recent advancements in portable imaging and machine learning have enabled the adoption of handheld retinal cameras, with diabetic retinopathy diagnostic algorithms, in primary care settings. While studies on vision screening for various conditions with different testing modalities present mixed conclusions, the literature largely supports increasing vision testing capabilities in rural and under-resourced populations, as well as for populations at risk of progressive diseases such as glaucoma, AMD, and DR.^13,14

Several studies have now documented VR-mediated perimetry examinations.^29,35,36 Most of these tests, however, are direct analogues of existing perimetry tests that modify visual stimulus signal intensity and some measure intratest outcomes to demonstrate reproducibility. Furthermore, some studies that have tested directly against HVFA report poor inter-device agreement.^{35 32} Those that do correlate strongly with HVFA outputs do not show improvement in test time.^29,36 To our knowledge, this is a unique advantage of the accelerated analogue presented here. While uneven sensitivities across Garway-Heath geographic retinal regions were observed to a certain degree, the lowest sensitivities were comparable to those of other studies. This result can be improved in the future by moderately increasing the number of stimuli presented or adding another stimulus intensity threshold, while still keeping the exam substantially shorter than the HVFA version. When comparing speed of the current analogue exam, the VR 24 − 2 perimetry was approximately 2x faster than the HVFA suprathreshold time.

The use cases for color vision deficit testing are growing every year, with its indications including Alzheimer’s, Parkinson’s, stroke, multiple sclerosis, AMD, glaucoma, and diabetes.^29,37−43 Specifically, several studies have documented the usefulness of Ishihara tile implementation in characterizing neurodegenerative disorders, supporting its use as a readily available screening technology.^44–46 A limitation of the multiple-choice approach presented here is the increased probability of a false positive. While alternative methods, such as verbal response recording, can be implemented within existing VR systems, there is a higher risk of technical complications due to factors obstructing communication such as language barriers. Future studies with this test will involve performance of this VR analogue among patients with specific neurodegenerative disorders to assess the viability of multiple-choice testing, particularly in patients with declining mental status.

The Amsler grid has been an essential tool for measuring chronic ophthalmic disease progression, including AMD.⁴⁷ Metamorphopsia also presents as a prevalent symptom of neurodegenerative and demyelinating conditions such as optic neuritis in multiple sclerosis.^48,49 The Amsler grid has also been effective at characterizing stroke-induced visual field deficits.⁵⁰ These functionalities warrant its presence on a retinal VR platform.

Altogether, the delivery of a multi-faceted retinal function examination on a single device, such as a VR headset, can improve the accessibility of vision screening as well as clinical decision-making in specialties such as neurology, neurosurgery and endocrinology, while also providing the patient with more comfort than that afforded by standard in-office retinal examinations. Future work will include continued adaptation of existing tests as well as the development of novel tests that will improve the adoption of VR technologies in spaces beyond vision specialist practices.

A head-to-head comparison between traditional and VR-based 24 − 2 suprathreshold perimetry, Ishihara and Amsler grid testing showed good agreement across testing methods for both healthy patients and those with previously diagnosed glaucoma and retinal pathologies. Improving vision screening accessibility can help achieve earlier diagnoses, promoting value-based treatments and ameliorating population health. VR-based screening allows for a more comfortable and speedy testing experience.

Acknowledgements

We would like to thank our statistician, Nicholas Kissel, for his help with representing the data in this manuscript. This research was supported (in part) by an Alpha Omega Alpha Carolyn L. Kuckein Student Research Fellowship.

Conflict of Interests Statement

Margarita Labkovich, MS, Andrew J. Warburton, MD, Randal A. Serafini, MS, and Aly A.A. Valliani, BA are co-founders of Retina Technologies. Their involvement has been declared as a Conflict of Interest to the Institutional Review Board at Mount Sinai.

Funding

This study has been supported by the Icahn School of Medicine CTSA grant, number UL1TR001433. The grant was provided by the National Center for Advancing Translational Sciences, National Institutes of Health.

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Tables 1 to 4 are available in the Supplementary Files section.

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Table1To4.docx

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Virtual Reality Enables Rapid and Multi-Faceted Retinal Function Screening

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Abstract

Figures

Introduction

Methods

Overall Study Design

VR Hardware and Software

In-Office Standard Tests

Design of VR Tests Compared to Clinical Standards

Statistical Analysis

Results

Perimetry

Ishihara

Amsler grid

Exam Efficiency Measured

Discussion

Conclusion

Declarations

References

Tables 1 To 4

Additional Declarations

Supplementary Files

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