ABSTRACT
Nonarteritic ischemic optic neuropathy (NAION) is believed to be an ischemic insult to the optic nerve head and is one of the most common acute optic neuropathies of adulthood. Prevention of NAION in the fellow eye has not yet been accomplished. Optical coherence tomography angiography (OCTA) is a new and emerging non-invasive technology that provides microvascular information that complements the structural data. This prospective study is aimed to fill the lacunae in data that is available in the Indian population. We included 36 patients with NAION, their 36 fellow eyes and 37 healthy controls. The peripapillary perfusion index, peripapillary flux, peripapillary retinal nerve fibre layer (RNFL) thickness values and disc volumes of eyes were evaluated. The NAION eyes had lower peripapillary perfusion index, flux and RNFL thickness values in all sectors compared with both the fellow and the healthy control eyes (p = < .05). A statistically significant difference was found in disc volume between control eyes and fellow eyes, which included eyes with disc at risk configuration as well as normal disc configuration. Eyes with disc at risk configuration had a numerically lower disc volume than eyes with normal disc configuration. Fellow eyes overall had numerically lower perfusion index, higher RNFL thickness, and similar flux which was statistically non-significant compared with the healthy eyes. Correlation between the localization of visual field defects and the quadrants showing impairments of perfusion index and peripapillary RNFL were also assessed. These findings may indicate the potential vascular risk factors for the development of NAION in fellow eyes.
KEYWORDS: OCT angiography, NAION, fellow eye, perfusion, flux, peripapillary RNFL
Introduction
Nonarteritic ischemic optic neuropathy (NAION) is believed to be an ischemic insult to the optic nerve head and is one of the most common acute optic neuropathies of adulthood. It has an annual incidence of 2.3–10.3 per 100,000 persons aged more than 50 years.1 The pathophysiology of NAION remains unclear, but it has been proposed to result from hypoperfusion in the microcirculation of the optic disc. The optic nerve head derives its blood supply from different sources. Retinal ganglion cell bodies and the retinal nerve fibre layer are supplied by capillaries from the central retinal artery. The prelaminar and laminar parts of optic nerve are mainly supplied by the short posterior ciliary arteries and the choroidal vasculature.2 NAION is presumed to involve vascular insufficiency in the short posterior ciliary artery.3,4
There is a lack of data describing the microvascular alterations in eyes which have developed NAION and the fellow unaffected eyes amongst the Indian population. Also, the fellow eyes reported also develop the disease in 15%–27% of the patients within 5 years.5 Hence, in this study, we aim to describe and compare peripapillary microvascular and structural parameters in atrophic NAION, unaffected fellow eyes and controls in an Indian population using optical coherence tomography angiography (OCTA). OCTA is a new and emerging non-invasive technology that provides microvascular information that complements the structural data.
Methods
This was a prospective cross-sectional study. We evaluated 80 eyes of 40 patients who presented to our neuro-ophthalmology clinic at a tertiary-care institute in South India from November 2022 to December 2022 (40 eyes with NAION and 40 fellow eyes). Out of these, we included 36 patients with NAION, their 36 fellow eyes and 37 healthy controls. The study population were patients who had developed NAION previously at any point of time and had been on routine follow-up with us as well as patients who presented to us with an atrophic disc following an episode of NAION.
The study was approved by the institutional ethics committee according to the Declaration of Helsinki, and written informed consent was obtained from all of the patients before inclusion in the study (Project code RES2022075CLI).
All the participants underwent a complete ophthalmological examination: best-corrected visual acuity on Snellen charts, anterior and posterior segment examination, non-contact tonometry, visual field analysis by standard automated perimetry, color vision by Ishihara’s chart, and OCT angiography of the peripapillary region.
The inclusion criteria for healthy subjects were patients older than 40 years, no media opacity that interfered with fundus viewing and imaging, normal ocular findings with no sign of any retinal or optic nerve head pathology, an intraocular pressure less than 21 mm Hg and no systemic comorbidities. The criteria for NAION patients inclusion were those more than 40 years of age, with history of painless visual loss accompanied with unilateral disc edema documented previously (at the time of inclusion in the study, optic atrophy had set in) and disc at risk of the other eye or a normal disc configuration determined clinically on ophthalmoscopy with an altitudinal visual field defect compatible with previously occurred NAION.
Patients with other optic disc diseases or coexisting retinal pathologies were excluded from this study. The exclusion criteria also included a history of previous intraocular surgery except an uncomplicated cataract surgery, ocular trauma, systemic or ocular conditions known to affect the optic nerve structure or visual field, any retinal disease or a visually significant cataract.
Neuroimaging was performed in some patients, particularly ones who presented in the chronic stage to rule out other causes of optic atrophy. Relevant biochemistry and hematological tests were done to look for giant cell arteritis (GCA), vasculitis, or other inflammatory conditions.
OCTA images were acquired by the AngioPlex matrix software on CIRRUS HD-OCT Model 6000 © 2021, Carl Zeiss Meditec, Inc., Dublin, CA. The scanning area captured consisted of 4.5 × 4.5 mm sections centred on the optic nerve head (ONH) and 200 × 200 mm optic disc cube. The software automatically assigns two concentric circles centred on the optic nerve head. The radii of the inner circle is 1 mm and outer circle is 2 mm, with a ring width of 1 mm. The perfusion index and flux of the radial peripapillary capillaries (RPC) can be evaluated between these rings in the peripapillary region and in four sectors (superior, inferior, nasal, and temporal). The number of red blood cells moving through vessel segments per unit area is measured by flux. The peripapillary retinal nerve fibre layer thickness was also evaluated at the peripapillary region and in four sectors using the same analysis software. The segmentation line lies between the internal limiting membrane and the posterior limit of the nerve fibre layer. CIRRUS 6000 automatically centres and optimizes B-Scan settings. CIRRUS 6000 also automatically corrects for the patient’s refraction error and balances fundus brightness and contrast. Eye tracking was done using FastTrac™ for patients with poor fixation.
OCTA scans of poor quality or inadequate signal strength index (SSI; less than 6 on a 10-point scale) were excluded. Scans which had blink or motion artefacts, dense media opacities that interfered with the vessel signals, or any errors in segmentation plane were not included in the study.
Visual field testing was performed using automated (Humphrey, 30–2 SITA standard) perimetry in all cases. Data were not included if the reliability indices were more than 30% fixation losses, 20% false positives, or 20% false negatives. Mean and pattern deviation plots of the Humphrey perimeter report were compared with the optic nerve head angiographic data.
Statistical analysis was done by Stata version 14.2 software (StataCorp LLC USA). Chi-square test was used to test the association between two categorical variables. Independent t-test was used to test the significant difference of the mean of two independent groups. The ANOVA test was used to compare more than two groups and determine whether there was a statistically significant relationship between them. Post hoc analysis was done by Sidak test. A p-value of < .05 was accepted as statistically significant.
Results
Mean age of patients was 57.69 ± 6.50 years and of controls was 60.62 ± 1.23 years. Demographic data, systemic comorbidities, best-corrected visual acuity, and intraocular pressure at presentation is shown in (Table 1).
Table 1.
Demographic data, systemic comorbidities, best-corrected visual acuity, and intraocular pressure at presentation.
| NAION eyes | Fellow eye | Control eye | |
|---|---|---|---|
| Male | 13 (36.11%) | 13 (36.11%) | 13 (35.14) |
| Female | 23 (63.89%) | 23 (63.89%) | 24 (64.86) |
| BCVA | 0.74 ± 0.69 | 0 | |
| IOP | 16.42 ± 3.0 | 16.36 ± 2.57 | 16.14 ± 2.87 |
| Diabetes Mellitus | 20 (55.56%) | 20 (55.56%) | 0 |
| Systemic Hypertension | 16 (44.44%) | 16 (44.44%) | 0 |
| Others (Hyperlipidemia, cardiac disease, epilepsy, myasthenia gravis, asthma, squint) | 22 (61.11%) | 22 (61.11%) | 0 |
BCVA: Best-corrected visual acuity.
IOP: Intraocular pressure.
In 52.78% of patients, the right eye was affected, and in 47.22% patients, the left eye was affected. Totally, 91.67% of patients had red green color vision defect tested by Ishihara chart in the affected eye. Time of presentation to us ranged from 20 days of onset of defective vision to 5 years. (Table 2).
Table 2.
Time of presentation.
| Number of patients-Time since onset of defective vision | Number of patients-Time of OCTA | |
|---|---|---|
| <20 days | 19 | 2 |
| 20–<60 days | 9 | 4 |
| 60–<6 Month | 4 | 5 |
| 6 Month–<1 Year | 3 | 4 |
| 1 Year–<5 Year | 1 | 14 |
| >5 Years | 0 | 7 |
OCTA:Optical coherence tomography angiography.
At presentation, whole disc edema was present in 60.91% of patients, superior sectoral edema was present in 8.34%, 5.56% had inferior sectoral edema, sectoral edema which was not limited to superior or inferior parts of disc was seen in 2.78%. 13.89% presented with whole disc pallor and 8.34% presented with sectoral pallor. Time after presentation at which OCTA was done ranged from 20 days to 5 years. (Table 2).
97.22% of the patients studied had pale disc at the time of OCTA. We excluded the patients who did not have a clinically atrophic disc from the imaging. There were two patients who had a pale disc at as early as 20 days of presentation to us (5.56%) because they did not present to us at onset of defective vision. Best-corrected visual acuity at the time of OCTA was 0.38 ± 0.39 in LogMAR units, and intraocular pressure at time of OCTA was 16.14 ± 2.87 mm Hg.
Perfusion index, flux, and pRNFL thickness of affected eyes, fellow eyes, and control eyes with post hoc analysis are shown in Table 3. We compared disc volumes between fellow eyes and control eyes as well as between disc volume of control eyes, fellow eyes with normal disc configuration, and fellow eyes clinically determined to have disc at risk configuration in Table 4. Statistically significant difference was found between disc volume of control eyes, fellow eyes with normal disc configuration, and fellow eyes clinically determined to have disc at risk configuration. Table 5 compares the means of control, fellow eye (at risk & normal configuration).
Table 3.
Perfusion index, flux, and pRNFL thickness of affected eyes, fellow eyes, and control eyes with post hoc analysis.
| Affected eyes (AE) (n = 36) | Fellow eyes (FE) (n = 36) | Control eyes (CE) (n = 37) | p-value | Post hoc analysis (**Sidak) mean difference - (p-value) |
|||
|---|---|---|---|---|---|---|---|
| CE Vs. FE | CE Vs. AE | AE Vs. FE | |||||
| Perfusion Index | |||||||
| Superior | 35.14 ± 9.61 | 45.29 ± 6.20 | 45.11 ± 10.50 | .0000 | 0.18 (1.00) | 9.97 (0.000) | 10.16 (0.000) |
| Inferior | 37.56 ± 6.07 | 44.55 ± 6.86 | 47.09 ± 6.95 | .0000 | 2.54 (0.284) | 9.53 (0.000) | 6.99 (0.000) |
| Nasal | 42.59 ± 7.63 | 46.62 ± 7.14 | 47.00 ± 11.52 | .0744 | |||
| Temporal | 44.32 ± 5.58 | 47.85 ± 7.29 | 48.17 ± 10.43 | .0827 | |||
| Average | 40.26 ± 5.96 | 45.99 ± 5.90 | 47.87 ± 6.75 | .0000 | 1.87 (0.491) | 7.61 (0.000) | 5.74 (0.000) |
| Flux | |||||||
| Superior | 0.35 ± 0.07 | 0.41 ± 0.47 | 0.40 ± 0.08 | .0001 | 0.013 (0.78) | 0.05 (0.002) | 0.07 (0.000) |
| Inferior | 0.36 ± 0.04 | 0.42 ± 0.04 | 0.41 ± 0.04 | .0000 | 0.005 (0.916) | 0.05 (0.000) | 0.055 (0.000) |
| Nasal | 0.37 ± 0.04 | 0.43 ± 0.05 | 0.41 ± 0.08 | .0001 | 0.017 (0.511) | 0.04 (0.009) | 0.059 (0.000) |
| Temporal | 0.36 ± 0.04 | 0.43 ± 0.05 | 0.42 ± 0.09 | .0000 | 0.009 (0.902) | 0.05 (0.001) | 0.064 (0.000) |
| Average | 0.36 ± 0.04 | 0.42 ± 0.04 | 0.42 ± 0.05 | .0000 | 0.003 (0.990) | 0.055 (0.000) | 0.058 (0.000) |
| RNFL Thickness | |||||||
| Superior | 75.92 ± 53.8 | 117.28 ± 49.10 | 94.30 ± 35.53 | .0013 | 22.98 (0.110) | 18.38 (0.261) | 41.36 (0.001) |
| Inferior | 77.86 ± 50.50 | 120.75 ± 41.20 | 100.30 ± 39.45 | .0004 | 20.45 (0.141) | 22.44 (0.091) | 42.89 (0.00) |
| Nasal | 66.89 ± 32.47 | 84.94 ± 32.55 | 73.27 ± 30.49 | .0551 | |||
| Temporal | 63.47 ± 73.48 | 70.53 ± 45.54 | 57.51 ± 37.39 | .8554 | |||
| Average | 68.94 ± 39.46 | 96.31 ± 36.65 | 84.24 ± 30.95 | .0065 | 12.06 (0.39) | 15.29 (0.198) | 27.36 (0.005) |
pRNFL:Peripapillary RNFL
Table 4.
Disc volume.
| Affected eye | Fellow eye | Control eye | p-value | |
|---|---|---|---|---|
| Disc Volume | 1.70 ± 0.72 | 1.61 ± 0.47 | 1.93 ± 0.62 | .0774 |
|
Disk Volume between Control eye and Fellow eye: | ||
| |
mean ± sd |
p-value |
| Control eye | 1.93 ± 0.62 | 0.015 |
| Fellow eye | 1.61 ± 1.47 | |
| Control eye | Fellow eye with normal disc configuration | Fellow eye with disc at risk configuration | p-value | |
|---|---|---|---|---|
| Disc Volume | 1.93 ± 0.62 | 1.52 ± 0.44 | 1.66 ± 0.43 | .0403 |
|
Mean of Disc volume in Fellow eye with or without disc at risk | ||
| |
Mean ± SD |
p-value |
| Dist at risk (n = 24) | 1.66 ± 0.43 | .367 |
| Dist Not at risk (n = 12) | 1.52 ± 0.44 | |
Table 5.
Comparison between the means of Control, fellow eye(at risk & normal configuration).
| Control eyes (CE) (n = 37) | Fellow eye with normal configuration (n = 12) | Fellow eyes with disc at risk configuration (n = 24) | p-value | |
|---|---|---|---|---|
| Perfusion Index | ANOVA test | |||
| Superior | 45.11 ± 10.50 | 45.72 ± 6.52 | 45.08 ± 6.17 | .9741 |
| Inferior | 47.09 ± 6.95 | 43.56 ± 7.45 | 45.05 ± 6.65 | .2513 |
| Nasal | 47.00 ± 11.52 | 45.35 ± 7.95 | 47.26 ± 6.79 | .8432 |
| Temporal | 48.17 ± 10.43 | 49.12 ± 9.37 | 47.21 ± 6.14 | .8277 |
| Average | 47.87 ± 6.75 | 45.86 ± 6.85 | 46.06 ± 5.53 | .4599 |
| Flux | ||||
| Superior | 0.40 ± 0.08 | 0.41 ± 0.05 | 0.42 ± 0.04 | .6253 |
| Inferior | 0.41 ± 0.04 | 0.41 ± 0.04 | 0.42 ± 0.04 | .5609 |
| Nasal | 0.41 ± 0.08 | 0.42 ± 0.05 | 0.43 ± 0.05 | .4712 |
| Temporal | 0.42 ± 0.08 | 0.42 ± 0.05 | 0.43 ± 0.05 | .8043 |
| Average | 0.42 ± 0.04 | 0.41 ± 0.05 | 0.42 ± 0.05 | .7664 |
| RNFL Thickness | ||||
| Superior | 94.29 ± 35.53 | 122.92 ± 28.29 | 114.46 ± 57.11 | .0699 |
| Inferior | 100.29 ± 39.45 | 121.75 ± 26.33 | 120.25 ± 47.44 | .1058 |
| Nasal | 73.27 ± 30.49 | 87.00 ± 18.71 | 83.92 ± 37.96 | .2864 |
| Temporal | 67.51 ± 37.39 | 75.58 ± 45.74 | 68.00 ± 43.17 | .8287 |
| Average | 84.24 ± 30.95 | 101.92 ± 29.13 | 93.50 ± 42.00 | .2551 |
There was no significant correlation between flux and RNFL and perfusion index and RNFL thickness of fellow eyes and control eyes.
Discussion
In vitro and in vivo studies previously conducted have demonstrated that flux can serve as a supportive variable to the standard vessel density measurements and can also be a potentially useful measure of retinal perfusion in addition to other vascular parameters derived by OCTA. It is also practical for detecting any subclinical changes in the vascular perfusion of the optic nerve head.3,6
In our study, we enrolled only the atrophic-stage unilateral NAION eyes to prevent the confounding effect of optic disc edema seen in the acute stage of NAION on image quality and acquisition.
In this study, atrophic NAION eyes had significantly lower peripapillary RNFL thickness and perfusion index values compared with both fellow and age-matched healthy control eyes. This was in line with most cross-sectional studies involving the late-stage atrophic disc of NAION which have reported a significant reduction of peripapillary radial capillaries.7–9 Also, the changes in capillary density in the peripapillary capillaries seen on OCTA correlate with the severity of visual field defect and the corresponding thinning of the peripapillary RNFL.7–9
In our study, the NAION eyes showed a lower flux compared to fellow eyes and controls. Studies that have analyzed the flux index in atrophic NAION are limited. In a recently published study, authors have concluded that flux is a good indicator of optic nerve and retinal vascular changes in NAION.10 This parameter has not been reported previously to the best of our knowledge in an Indian population.
Most of previous learnings on unilateral NAION have concentrated on imaging features of the diseased eye; however, data about unaffected fellow eye compared with healthy controls in an Indian population are limited. Since the fellow eyes of such patients have been reported to be at high risk for development of NAION,11,12 we also aimed to focus on the fellow eyes and to describe probable structural or microvascular risk factors for NAION progression.
In this study, fellow eyes demonstrated numerically lower perfusion compared to controls in all sectors and globally. However, there was no statistical difference. In a recent study done in Turkey, fellow eyes demonstrated lower global peripapillary vessel density, but statistically similar inside-disc vessel density compared with the healthy control eyes.13
Our study results with respect to perfusion index were similar to previous studies that detected similar peripapillary vessel densities in the fellow eyes compared with healthy control eyes.6,14,15
We did not find any statistically significant difference in the flux between fellow eyes and control eyes globally or sectorally in our study. In another study which measured the mean capillary flux index in the four sectors of the optic nerve head – superior, inferior, nasal, temporal – the flux was found to be significantly higher in the diseased eyes than in the healthy control eyes. This unanticipated result observed during the course of this disease believed to be due to an ischemic process could reflect the dilatation of the capillaries that has been detected in the radial peripapillary capillaries. It could also be due to an autoregulatory mechanism that occurs within the choroidal vasculature to compensate for the acute drop in blood flow.16
Fellow eyes had a numerically greater pRNFL thickness globally and sectorally than control eyes which has not been previously reported.
The previous studies that have evaluated the role of the peripapillary RNFL in fellow eyes of NAION compared with healthy eyes have not reached any consistent inferences. Several recent studies did not find any difference in the peripapillary RNFL thickness between the unaffected fellow eyes of patients with NAION and healthy control eyes.13,17 On the other hand, a recent study reported peripapillary RNFL loss in the fellow eyes of NAION in superior and nasal quadrant in spite of minimal or no visual symptoms.18
In this study, interestingly,19 the perfusion index was numerically higher in fellow eyes with disc-not at-risk configuration compared with fellow eyes with normal optic disc configuration. It has been suggested that the higher vessel densities recorded in the smaller cups of the disc at risk eyes may reflect the necessity for a higher blood supply to the thick prelaminar tissue, but this was not so in our study.20
In this study, there was no significant correlation between flux and RNFL and perfusion index and RNFL thickness of fellow eyes and control eyes.
Previous studies have demonstrated the presence of significant correlations between peripapillary RNFL thickness and peripapillary perfusion index in both NAION and fellow eyes.20
In the current study, we observed that the peripapillary perfusion index and RNFL thickness were reduced at the corresponding location of the visual field defects in the NAION eyes, which is consistent with other studies showing correlation of vessel densities with visual field.9,15,21,22 The final visual acuity in patients who had a higher perfusion in the temporal quadrant was better than those who had a lower perfusion index in the temporal sector probably due to sparing of the watershed zone. The severity of vision loss after NAION is believed to be directly correlated with the extent of the damage to the fibres of the papillomacular bundle.6
We found that the overall disc volume in the fellow eye was statistically significantly reduced as compared to the control eyes. Statistically significant difference was found between disc volume of control eyes, fellow eyes with normal disc configuration and fellow eyes clinically determined to have disc at risk configuration. However, no statistically significant difference was found between volume of at-risk discs and normal configuration discs.
Saito et al. have suggested that a smaller disk area and smaller cupping are predisposing factors for the development of NAION.17 In our study, although we found a smaller disc volume in the fellow eyes, we did not find any statistically significant differences in the vascular parameters measured that would suggest that a smaller disc has lesser perfusion and hence is more predisposed to ischemia which is similar to another study which proposed that crowded optic disc appearance of fellow eyes is not related to differences in vessel densities and vascular parameters.6
In our study, among the patients who had a carotid Doppler study done, 66.66% had significant stenosis causing haemodynamic changes. Zhu et al. demonstrated that the presence of carotid artery plaques was more frequent in the patients with NAION, compared to either the hypertensive group or the normal controls, indicating that NAION may be associated with atherosclerosis of carotid artery.23
We started all the patients on Aspirin 75 milligrams once a day. Seven patients developed NAION in fellow eye on follow-up.
Limitations
We did not include data about axial length and refractive error in this study.
We did not measure the thickness of the ganglion cell complex, which may be a better indicator than RNFL thickness of early damage to axons in ischemic diseases.
NAION is known to be associated with systemic vascular insufficiencies like hypertension, diabetes, and hyperlipidaemia.23 The peripapillary vascular density has been reported to be reduced in diabetes and hypertension even without clinically diagnosable retinopathy.24,25 Another confusing factor is that these systemic vascular diseases develop slowly hence the duration or severity of these diseases cannot be precisely identified. In these patients, the cross-sectional design of our study may have limited the outcomes of our findings.
We used an automated software which did not differentiate between the microvasculature and major retinal vessels. OCT-A is not able to show the short posterior ciliary arteries with our current technology. Unfortunately, commercial software was not available to us for quantitative analysis. The inner and outer limits of the segmentation curve could not be modulated by our software; it only allowed movements up or down using the inbuilt segmentation lines, calculated automatically based on the contour of ILM. However, the AngioPlex software requires a shorter time for execution and provides a higher number of images with lesser artefacts as compared to other softwares like Angiovue software.26
Conclusion
Despite a lack of visual complaints in fellow eye, it should be kept in mind that some structural and vascular changes also occur during the disease process in the fellow eye, and measurement of perfusion index, flux, and peripapillary RNFL thickness may give an idea about future outcomes.27
We recommend performing an OCTA of the fellow eye when a patient presents with a unilateral disc edema clinically indicative of NAION or optic atrophy due to the chronic stage of NAION. If the fellow eyes show lower values of the structural and vascular parameters, the patient should be closely monitored with stricter systemic control. Future studies including larger sample sizes will continue to shed light on the microvasculopathy of NAION further in the Indian population.
Funding Statement
The author(s) reported there is no funding associated with the work featured in this article.
Disclosure statement
No potential conflict of interest was reported by the author(s).
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