Peripapillary Microvascular and Structural Parameters in Atrophic Nonarteritic Anterior Ischemic Optic Neuropathy and Their Unaffected Fellow Eyes

This cross-sectional study aimed to evaluate the peripapillary vessel density (VD), peripapillary retinal nerve fiber layer (RNFL) thickness values of eyes with atrophic nonarteritic anterior ischemic optic neuropathy (NAION), and unaffected fellow eyes.

Original Contribution Section Editors: Clare Fraser, MD Susan Mollan, MD Peripapillary Microvascular and Structural Parameters in Atrophic Nonarteritic Anterior Ischemic Optic Neuropathy and Their Unaffected Fellow Eyes Gozde Hondur, MD, Ozlem Budakoglu, MD Background: This cross-sectional study aimed to evaluate the peripapillary vessel density (VD), peripapillary retinal nerve fiber layer (RNFL) thickness values of eyes with atrophic nonarteritic anterior ischemic optic neuropathy (NAION), and unaffected fellow eyes. Methods: Peripapillary VDs and RNFL thicknesses in the peripapillary region and 4 sectors (superior, inferior, nasal, and temporal) were evaluated using optical coherence tomography angiography among 19 atrophic NAION eyes, 19 unaffected fellow eyes, and 22 age-matched and sexmatched healthy controls. Results: The NAION eyes had lower peripapillary VD and RNFL thickness values in all areas compared with both the fellow and the healthy control eyes (P , 0.001 for all). The fellow eyes also demonstrated lower peripapillary VD values (P = 0.02) despite similar RNFL thickness values (P = 0.99) in the peripapillary region compared with the age-matched and sex-matched healthy controls. The peripapillary RNFL thickness values significantly correlated with peripapillary VD values in both NAION and fellow eyes. Conclusions: Diminished RNFL thickness and peripapillary VD values were observed in atrophic NAION eyes. In addition, a tendency for a lower peripapillary VD despite similar RNFL thickness values in the fellow eyes may indicate the potential vascular risk factors for NAION. Journal of Neuro-Ophthalmology 2022;42:489–494 doi: 10.1097/WNO.0000000000001542 © 2022 by North American Neuro-Ophthalmology Society Department of Ophthalmology (GH), University of Health Sciences, Ulucanlar Eye Training and Research Hospital, Ankara, Turkey; and Department of Ophthalmology (OB), Erzincan Binali Yildirim University School of Medicine, Erzincan, Turkey. The authors report no conflicts of interest All procedures performed in studies involving human participants were in accordance with the ethical standards of the Ankara Education and Research Hospital and with the 1964 Declaration of Helsinki and its later amendments or comparable ethical standards. Informed consent was obtained from all the individual participants included in the study. Address correspondence to Gozde Hondur, MD, Department of Ophthalmology, Ulucanlar Eye Training and Research Hospital, Altindag, 06230 Ankara, Turkey; E-mail: [e-mail] Hondur and Budakoglu: J Neuro-Ophthalmol 2022; 42: 489-494 N onarteritic ischemic optic neuropathy (NAION) is the most common acute optic nerve disease of adulthood. It has an annual incidence of 2.3–10.3 per 100,000 persons older than 50 years, which corresponds to 0.54–10.2 per 100,000 for all ages (1,2). The most common presentation involves a sudden monocular visual loss, disc edema, afferent pupil defect, and an altitudinal visual field defect that is located inferiorly. NAION is presumed to follow transient hypoperfusion in a small “crowded” disc (3,4). Optic nerve head blood supply is derived from different sources (5). Retinal ganglion cell bodies and the nerve fiber layer (the most anterior part of the optic nerve head) are supplied by capillary branches derived primarily from the central retinal artery. By contrast, the prelaminar and laminar portions are mainly supplied by the short posterior ciliary arteries and the choroid. NAION is assumed to be a vascular insufficiency, especially involving the short posterior ciliary artery. Up to now, the precise location of the vasculopathy has not been approved histopathologically in any eye with NAION, despite an assumed ischemic etiology (6). Therefore, the pathogenesis of NAION has remained incompletely understood (7). Optical coherence tomography angiography (OCTA) provides microvascular information that complements structural information and may enhance our comprehension of optic nerve diseases. Diminished peripapillary microvasculature has been already reported in eyes with NAION with OCTA (8–13). Although retinal nerve fiber layer (RNFL) thinning is also common in NAION, the relationship of the microvasculature alterations to the structural changes is not clearly identified. In addition, NAION presents mostly unilaterally, and the fellow eyes were reported to be involved in 15%–27% of the patients within 5 years (14,15). A comparison of the vessel density (VD) between the unaffected fellow eyes of patients with unilateral NAION and healthy controls might be supportive to reflect the potential vascular risk factors for NAION. 489 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution Hence, we compared the peripapillary vascular, structural parameters of eyes with atrophic NAION, unaffected fellow eyes, and age-matched healthy controls. METHODS OCTA images were obtained from subjects who agreed to contribute after the nature of the tests was explained. All investigations followed the principles of the Declaration of Helsinki, and the study received approval from the Institutional Review Board and Ethics Committee. After a detailed anamnesis, all the participants underwent a complete ophthalmological examination. Anterior and posterior segment examination, Goldmann tonometry, RNFL analysis of the peripapillary region on optical coherence tomography ([OCT]; SPECTRALIS, Heidelberg Engineering GmbH, Heidelberg, Germany), and standard automated perimetry were performed. The inclusion criteria for healthy subjects were older than 40 years, a best-corrected visual acuity of 20/30 or better, a spherical equivalent refractive error between +5 and 25 diopters (D), an astigmatism less than 3 D, 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 the absence of glaucomatous damage in peripapillary RNFL thickness analysis using the SPECTRALIS (Heidelberg Engineering) spectral domain OCT, which was complementary to OCTA because it included normative data for RNFL thickness. The inclusion criteria for NAION were defined as a history of acute and painless visual loss accompanying with unilateral swollen disc on ophthalmoscopy and visual field defect compatible with NAION that occurred more than 6 months before and resolved at the time of the study and at least aged 40 years. Other optic disc diseases such as glaucoma, arteritic ischemic optic neuropathy, optic neuritis, or coexisting retinal pathologies were excluded from this study. Erythrocyte sedimentation rate and C-reactive protein tests were performed to exclude arteritic ischemic optic neuropathy in all cases. Neuroimaging was performed in some patients, particularly ones who presented in the chronic stage, hence after the acute optic disc swelling had resolved. Patients who had optic atrophy of the fellow eye or patients with bilateral NAION involvement were correspondingly excluded. 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 including hypertensive or diabetic retinopathy, an epiretinal membrane, or age-related macular degeneration; or a visually significant cataract with a best-corrected visual acuity of less than 20/30. 490 Optical Coherence Tomography Angiography OCTA images were acquired by the initial experienced physician using the AngioVue Imaging System (Optovue XR Avanti, Optovue, 2017.1.0.151). The scanning area captured consisted of 4.5 · 4.5 mm sections centered on the optic nerve head (ONH). The integrated software automatically assigns 2 ONHcentered concentric circles. The radii of the inner and outer circles are 1 and 2 mm, respectively, providing a ring width of 1 mm. The VD of the radial peripapillary capillaries (RPC) can be evaluated between these rings in the peripapillary region and in 4 sectors (superior, inferior, nasal, and temporal) using the OCTA density evaluation tool. The current Angio DiscVue software provides the elimination of the large retinal vessel–related flow signals. The segmentation is between the internal limiting membrane and the posterior limit of the RNFL. The peripapillary RNFL thickness was also evaluated at the peripapillary region and in 4 sectors using the same ONH analysis software (Angio DiscVue) used for the vessel densities of the RPC (Fig. 1). OCTA scans with low quality were disregarded in the incidence of 1 or more of the listed conditions: inadequate signal strength index (SSI; less than 6 on a 10-point scale), incidence of blink artifacts, motion artifacts, media opacities interfering with the vessel signals, or any segmentation errors. Statistical Analysis The SPSS software (SPSS for Windows version 20.0; SPSS Inc, Chicago, IL) was used to perform the statistical analysis. Categorical variables were compared by means of the x2 test. Normal distributed data were analyzed using 1way analysis of variance (ANOVA), and post hoc analysis was performed using the Bonferroni test. Nonparametric data were analyzed using the 1-way ANOVA on ranks, and post hoc analysis was achieved with the Dune test. A P value ,0.05 was accepted as statistically significant. Correlations between the RNFL thickness and the peripapillary VD values were evaluated using Pearson correlation analyses in the NAION and the fellow eyes separately. RESULTS Nineteen eyes with unilateral atrophic NAION, 19 fellow eyes, and 22 eyes of healthy controls were evaluated in this study. There were no intergroup differences in age and axial length and the self-reported history of diabetes mellitus and hypertension. In addition, the visual field MD values and SSI values of fellow eyes and healthy control eyes were similar in post hoc analysis (P . 0.05 for all). Table 1 summarizes the clinical features of the participants. Hondur and Budakoglu: J Neuro-Ophthalmol 2022; 42: 489-494 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution FIG. 1. Optical coherence tomography angiography image of a healthy eye organized with radial peripapillary capillary density and RNFL thickness parameters. RNFL, retinal nerve fiber layer. The NAION group had significantly lower peripapillary RNFL thicknesses in all areas (peripapillary, inferior, superior, nasal, and temporal) compared with both the fellow and the control eyes (P , 0.05 for all). NAION eyes had also significantly lower VDs in the peripapillary region, inside the disc region, and all peripapillary sectors (inferior, superior, nasal, and temporal) compared with both the fellow and the control eyes (P , 0.001 for all) (Table 2 and Fig. 2). Fellow eyes had similar RNFL thicknesses in all areas compared with healthy eyes (P . 0.05 for all). However, the fellow eyes had statistically significant lower peripapillary VDs in the whole image and peripapillary regions compared with the control eyes (P = 0.02 for both). The fellow eyes also had lower VDs in the inside disc region, superior, temporal, and nasal sectors compared with healthy control eyes, but the differences were not significant (P . 0.05 for all). Table 2 summarizes the peripapillary RNFL thickness and VD values of the peripapillary region in detail. Among the 19 fellow eyes, 14 eyes (73%) were presented with disc-at-risk configuration with a small cup-to-disc ratio. The mean peripapillary VD was similar in fellow eyes with the disc-at-risk group (50.75%) compared with fellow eyes with normal optic disc configuration (51.04%) (P = 0.43). The mean inside-disc VD tended to be higher in fellow eyes with disc-at-risk configuration (52.40%) compared with fellow eyes with normal optic disc configuration (48.44%) (P = 0.05). Hondur and Budakoglu: J Neuro-Ophthalmol 2022; 42: 489-494 The peripapillary RNFL thickness values demonstrated significant correlations with peripapillary VD values in both NAION and fellow eyes. However, the peripapillary RNFL thickness values demonstrated no correlations with insidedisc VD values in both NAION and fellow eyes (Table 3). CONCLUSIONS In this study, NAION eyes had lower peripapillary RNFL thickness and VD values compared with both fellow and age-matched healthy control eyes. We aimed to focus also on the fellow eyes to describe probable structural or vascular risk factors for NAION development. The fellow eyes have been reported to carry high risk for progression to NAION (14,15). In this study, the fellow eyes demonstrated lower peripapillary VD values in the peripapillary and whole image regions, despite similar RNFL thickness values compared with age-matched healthy control eyes. The lower peripapillary VD in the fellow eyes of NAION may reflect the potential vascular risk factors or alterations underlying the NAION pathogenesis and also may be a precursor of RNFL loss in fellow eyes, although longitudinal studies are needed to validate this hypothesis. NAION is known to be associated with hypertension, diabetes, and hyperlipidemia (7). The peripapillary VD has been demonstrated to be reduced in diabetes and hypertension even without clinically observable retinopathy (16,17). 491 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution TABLE 1. Clinical and demographic features of the study groups Subject eyes (n) Sex (F/M) Age (yr) Visual acuity, logMAR IOP (mm Hg) Axial length (mm) MD (dB) SSI DM (%) HT (%) Controls (1) NAION (2) Fellow Eye (3) P 22 13/9 61.5 ± 8 0.04 ± 0.07 14.35 ± 2.03 23.31 ± 1.10 20.46 ± 0.85 8.1 ± 0.74 27.2 31,8 19 8/11 62.2 ± 7.3 0.49 ± 0.38 14.10 ± 2.72 23.47 ± 0.90 218.50 ± 6.79 6.63 ± 1.46 52.6 42.1 19 8/11 62.2 ± 7.3 0.04 ± 0.06 13.54 ± 1.91 23.42 ± 1.22 20.84 ± 1.02 8.36 ± 0.76 52.6 42.1 0.44* 0.90† ,0.001‡ 0.65† 0.89† ,0.001‡ ,0.001‡ 0.1* 0.7* Post Hoc 1=3,2 1=3.2 1=3.2 *x2 test. † One-way ANOVA and post hoc analysis were performed using the Bonferroni test. ‡ One-way ANOVA on ranks and post hoc analysis were performed using the Dune test. dB, decibel; DM, diabetes mellitus; F/M, female/male; HT, hypertension; IOP, intraocular pressure; MD, mean deviation; n, number of cases; NAION, nonarteritic anterior ischemic optic neuropathy; SSI, signal strength index. In this study, the self-reported prevalence of diabetes and hypertension was statistically similar between the study groups. However, the duration and severity of these vascular diseases may have been different. Hence, the lower VD in the fellow eyes may be the consequence of greater duration or severity of the accompanying vascular diseases and may be a potential risk for the RNFL loss in the fellow eyes of the patients with NAION. Longitudinal studies evaluating the value of the lower baseline peripapillary VD in predicting the risk of NAION development in the fellow eyes are needed. The vascular alterations in NAION in both acute and atrophic stages have been already studied in previous studies using OCTA (8–13). In this study, we enrolled only the TABLE 2. RNFL thickness and peripapillary vessel density (%) of the study groups RNFL thickness (mm) Peripapillary Post hoc comparison Superior Post hoc comparison Inferior Post hoc comparison Temporal Post hoc comparison Nasal Post hoc comparison Peripapillary VD (%) Whole image Post hoc comparison Inside disc Post hoc comparison Peripapillary Post hoc comparison Superior Post hoc comparison Inferior Post hoc comparison Temporal Post hoc comparison Nasal Post hoc comparison (P value) (P value) (P value) (P value) (P value) (P value) (P value) (P value) (P value) (P value) (P value) (P value) Controls (1) NAION (2) Fellow Eye (3) P 115.40 ± 10.48 1 vs 2 (,0.001) 136.86 ± 15.17 1 vs 2 (,0.001) 147.90 ± 16.05 1 vs 2 (,0.001) 74.31 ± 11.26 1 vs 2 (,0.001) 105.68 ± 12.20 1 vs 2 (,0.001) 67.89 ± 14.27 1 vs 3 (0.99) 64.52 ± 23.71 1 vs 3 (0.99) 87.26 ± 22.14 1 vs 3 (0.99) 48.94 ± 14.10 1 vs 3 (0.99) 68.33 ± 25.26 1 vs 3 (0.99) 113.84 ± 15.21 2 vs 3 (,0.001) 133.94 ± 21.79 2 vs 3 (,0.001) 147.22 ± 26.02 2 vs 3 (,0.001) 74.11 ± 11.26 2 vs 3 (,0.001) 102.05 ± 19.19 2 vs 3 (,0.001) ,0.001 51.85 ± 2.05 1 vs 2 (,0.001) 51.23 ± 4.99 1 vs 2 (,0.001) 54.79 ± 2.37 1 vs 2 (,0.001) 54.50 ± 4.36 1 vs 2 (,0.001) 56.77 ± 3.17 1 vs 2 (,0.001) 53.59 ± 4.71 1 vs 2 (,0.001) 55.45 ± 5.95 1 vs 2 (,0.001) 35.06 ± 5.50 1 vs 3 (0.02) 42.98 ± 5.81 1 vs 3 (0.99) 33.59 ± 6.10 1 vs 3 (0.02) 34.52 ± 10.34 1 vs 3 (0.32) 35.47 ± 11.20 1 vs 3 (0.44) 33.89 ± 7.94 1 vs 3 (0.11) 38.94 ± 10.72 1 vs 3 (0.48) 48.52 ± 3.76 2 vs 3 (,0.001) 50.88 ± 4.82 2 vs 3 (,0.001) 50.99 ± 4.22 2 vs 3 (,0.001) 50.73 ± 6.41 2 vs 3 (,0.001) 53.33 ± 5.70 2 vs 3 (,0.001) 49.31 ± 6.54 2 vs 3 (,0.001) 51.73 ± 8.20 2 vs 3 (,0.001) ,0.001 ,0.001 ,0.001 ,0.001 ,0.001 ,0.001 ,0.001 ,0.001 ,0.001 ,0.001 ,0.001 Data are presented as mean ± SD. Statistical significance was calculated using the 1-way analysis of variance, and post hoc analysis was performed using the Bonferroni test. NAION, nonarteritic anterior ischemic optic neuropathy; RNFL, retinal nerve fiber; VD, vessel density. 492 Hondur and Budakoglu: J Neuro-Ophthalmol 2022; 42: 489-494 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution FIG. 2. Peripapillary VD of representative cases for age-matched NAION (A), fellow (B), and healthy control (C) eyes. Areas with attenuated VD are observed in the affected eye (A). NAION, nonarteritic anterior ischemic optic neuropathy; VD, vessel density. atrophic-stage unilateral NAION eyes to prevent the confounding effect of optic disc edema on image acquisition in the acute stage of the disease. Not only the global but also the sectorial RNFL thickness and peripapillary VD loss were observed in atrophic NAION eyes in this study (Table 2). Recent studies also disclosed that the reduced VD of the peripapillary region was significantly correlated with the peripapillary RNFL thickness and visual field defect (8–12) in NAION eyes. The result of this study was in line with a previous study that demonstrated significant correlation between peripapillary RNFL thickness and peripapillary VD but not with inside-disc VD in NAION eyes (12). In this study, the inside-disc VD and the peripapillary VD had been demonstrated to be lower in NAION eyes compared with both the healthy and the fellow eyes. In addition, the fellow eyes demonstrated lower global peripapillary VD, but statistically similar inside-disc VD compared with the healthy eyes. Although OCTA can demonstrate the inside-disc VD, this is not without limitations. Anatomically, the inside-disc capillaries lie in a different plane compared with peripapillary capillaries (18). In addition, the large vessels congregate at the optic disc, and therefore, large vessel artifacts are greatest at the center of the disc. These factors may limit the precise calculation of the inside-disc VD (18). Despite these limitations, the inside-disc VD may still be reflective of the vascular damage in NAION and may be preserved until NAION onset. In this study, interestingly, the mean inside-disc VD tended to be higher in fellow eyes with disc-at-risk configuration compared with fellow eyes with normal optic disc configuration. It has been proposed that the higher vessel densities in the small cups may reflect the need for a higher vascular supply to the thick prelaminar tissue (19). However, this observation may be the result of an OCTA artifact. In eyes with larger cups (i.e., eyes without the disc-at-risk configuration), the inside-disc capillaries may lie in a deeper plane, and this may limit their demonstration by OCTA. Hondur and Budakoglu: J Neuro-Ophthalmol 2022; 42: 489-494 The results of the studies evaluating the role of the peripapillary RNFL alterations in fellow eyes of NAION compared with healthy eyes were controversial (20,21). Our results were in line with an important study that did not find any difference in the peripapillary RNFL thickness between the unaffected fellow eyes of patients with NAION and healthy control eyes (20). On the other hand, a recent previous study reported peripapillary RNFL loss in the fellow eyes of NAION (21), but this probably has resulted from the inclusion of mild cases of NAION in the fellow eyes. The study of the role of peripapillary vascular alterations in fellow eyes of NAION compared with healthy eyes with OCTA has also been limited to only a few reports with small sample sizes and has not reached a common conclusion (9,10). Our results differed from these previous studies that detected similar peripapillary VDs in the fellow eyes compared with healthy eyes (9,10). In this study, we detected lower peripapillary VD values in the fellow eyes compared with age-matched healthy control eyes. To the best of our knowledge, this is the first report that demonstrated a lower baseline peripapillary VD in the unaffected fellow eyes of patients with NAION compared with healthy control eyes. An interesting and noteworthy finding in this study was the presence of significant correlations between peripapillary RNFL thickness and peripapillary VD in both NAION and fellow eyes. A markedly lower VD despite a similar RNFL thickness values compared with the healthy eyes along with the significant correlation between structural and vascular parameters in the fellow eyes may infer the potential importance of the underlying vascular alterations which may pose risk for NAION. However, this study is not without limitations. This study involves a relatively small number of participants. However, it could not be possible to achieve a study with more patients because NAION is relatively an uncommon disease. In addition, we did not include any eyes with acute NAION. As in the acute phase, edema and hemorrhage may cause 493 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution TABLE 3. Correlations between the peripapillary RNFL thickness and the peripapillary and inside-disc vessel densities in NAION and fellow eyes NAION Eyes Peripapillary Inside disc Fellow eyes Peripapillary Inside disc Correlation Coefficient P 0.59 0.28 0.007 0.23 0.68 0.09 0.001 0.68 Statistical significance was calculated by Pearson regression analyses. Bold values indicate statistical significance at the P , 0.05 level. NAION, nonarteritic anterior ischemic optic neuropathy; RNFL, retinal nerve fiber layer. shadowing effect and signal attenuation. The cross-sectional design of our study may have limited the outcomes of our findings as well. Finally, although the prevalences of diabetes and hypertension of the NAION and control group had no statistically significant difference, the prevalences tended to be higher in the NAION group. Another confounding factor related to these vascular diseases develops slowly, and hence, the duration and past severity of these diseases cannot be identified precisely. This may also be a confounding factor when analyzing the peripapillary microvasculature data, but this confounding factor cannot be totally eliminated because the patients with NAION have higher prevalence of accompanying vascular diseases. In conclusion, we demonstrated lower peripapillary VD not only in the NAION eyes but also in the fellow eyes compared with healthy controls. 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Structural changes of macula and optic disk of the fellow eye in patients with nonarteritic anterior ischemic optic neuropathy. Int Ophthalmol. 2019;39:1293–1298. Hondur and Budakoglu: J Neuro-Ophthalmol 2022; 42: 489-494 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited.