Prognostic Value of Optical Coherence Tomography Characteristics in Anterior Visual Pathway Meningiomas

Anterior visual pathway meningiomas (AVPM) represent 2.5%-18% of all meningiomas. They may affect visual function, including visual acuity (VA) and visual field (VF). The principal modes of treatment are surgery and radiotherapy. The prognostic value of macular ganglion cell complex count (GCC) thickness has not been assessed in the literature thus far. The purpose of this study was to evaluate the prognostic value of pre-treatment optical coherence tomography (OCT) parameters (retinal nerve fiber; layer and GCC) for visual outcomes in patients with AVPM.

Original Contribution Section Editors: Clare Fraser, MD Susan Mollan, MD Prognostic Value of Optical Coherence Tomography Characteristics in Anterior Visual Pathway Meningiomas Noa Kapelushnik, MD, Shai Dror, BSc, Ruth Huna-Baron, MD Background: Anterior visual pathway meningiomas (AVPM) represent 2.5%–18% of all meningiomas. They may affect visual function, including visual acuity (VA) and visual field (VF). The principal modes of treatment are surgery and radiotherapy. The prognostic value of macular ganglion cell complex count (GCC) thickness has not been assessed in the literature thus far. The purpose of this study was to evaluate the prognostic value of pre-treatment optical coherence tomography (OCT) parameters (retinal nerve fiber layer and GCC) for visual outcomes in patients with AVPM. Methods: We retrospectively reviewed the medical records of all patients with AVPM who were treated in the Sheba Medical Center between 2011 and 2020. Included were patients with valid data containing preintervention OCT findings on the CIRRUS device and a minimum follow-up of 6 months. Preintervention and postintervention data on comprehensive ophthalmic examinations and OCT parameters of the affected eyes were retrieved. The correlation between preintervention OCT parameters and the visual outcome was assessed. The patients were also divided into 2 groups according to preintervention GCC (thin vs normal), and the visual outcome was compared between groups. Results: In total, 186 patients’ medical records were analyzed, and 38 patients who met the inclusion criteria were included in the study (mean age at diagnosis 52.8 ± 12.2 years, 28 women). Twenty-nine patients had 1 affected eye, and 9 had bilateral insult. A higher preinterventional average GCC was associated with better VA at 6 months, 1 year, and 2 years after intervention (r = 20.5, P # 0.004, 0.005, and 0.03, respectively). There was a significant correlation between preinterventional GCC and VF mean deviation 2 years after intervention (r = 0.7, P # 0.001). The thinner the GCC, the more prominent was the change in VA from before intervention to 2 years after intervention (P # 0.008). Correction for multiple comparisons with the Benjamini– Hochberg procedure did not change the significance of our findings. The Goldschleger Eye Institute and the Arrow Project (NK, SD, RHB), Sheba Medical Center, Tel Hashomer, Ramat Gan, Israel, and the Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel. The authors report no conflicts of interest. N. Kapelushnik and S. Dror have contributed equally to the article. Address correspondence to Ruth Huna-Baron, MD, The Goldschleger Eye Institute, Sheba Medical Center, Ramat Gan 52621, Israel; E-mail: [e-mail] 96 Conclusions: OCT parameters (GCC) have a predictive value in AVPM. There is strong correlation between preinterventional GCC and VA shortly after the intervention. Although a thin GCC is generally considered a negative prognostic factor, improvement in clinical parameters was also evident in patients with thin GCC. The potential of improvement despite preinterventional GCC thinning can add to the clinical discussion of the prognosis, and therefore, we recommend the patients with AVPM to undergo OCT and to be advised that GCC thinning alone should not be used as a major criterion in deciding whether treatment should be pursued. Journal of Neuro-Ophthalmology 2023;43:96–101 doi: 10.1097/WNO.0000000000001652 © 2022 by North American Neuro-Ophthalmology Society M eningiomas are the most common primary intracranial tumors, comprising 36% of all central nervous system tumors (1). Anterior visual pathway meningiomas (AVPM) represent 2.5%–18% of all meningiomas (2). Traditional treatment options for AVPM include observation, surgery, and radiotherapy (3,4). Multiple factors that affect the visual outcome of postoperative AVPM have been researched, and duration of symptoms, tumor size, and tumor location were found to be inconsistent in determining visual prognosis (5–7). There has been increasing use of optical coherence tomography (OCT) to assist the evaluation of patients with tumors in proximity to the anterior visual pathway (8). The technological improvement from time-domain OCT to spectral-domain OCT enabled better resolution and the ability to differentiate between individual layers of the retina such that the ganglion cell complex (GCC) can now be measured. Because the macular GCC analysis is centered over the fovea, there is a strong correlation between GCC thinning and visual field (VF) loss in compressive optic neuropathies (9). Specifically, pre-treatment OCT parameters were reported to have a prognostic value for postoperative visual recovery in compressive chiasmal tumors, such as pituitary adenomas. Normal retinal nerve fiber layer (RNFL) thickness (within 95%–99% of Kapelushnik et al: J Neuro-Ophthalmol 2023; 43: 96-101 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution values obtained from the OCT manufacturer) was determined preoperatively to have a positive prognostic value in cases of pituitary adenoma (10,11). One case–control study found thin GCC as a prognostic factor for poor outcome in a group of 23 patients with compressive lesions in the anterior visual pathway (only 2 had meningiomas) while assessing the postoperative VFs (12). Specific AVPM studies showed postoperative improvement both in visual acuity (VA) and VF for normalthickness RNFL compared with thin-thickness RNFL (13,14). There are, however, no data on GCC as a prognostic factor in patients with AVPM. Therefore, the aim of our study was to assess the visual prognostic value of preintervention GCC in cases of AVPM. values and is defined as a thin GCC, as determined by the normative database and with the adjustment to known affecting factors, such as age and sex (Carl Zeiss Meditec) (15). Patients with an average red GCC were labeled as having a thin GCC. The chi-square test and Wilcoxon rank-sum test were used for comparison of baseline characteristics between the 2 groups. The Spearman correlation coefficient was applied to assess the correlation between OCT parameters and the clinical outcome at the postintervention visits. A P value of ,0.05 was considered statistically significant. The Benjamini–Hochberg procedure was applied as correction for multiple comparisons to control the false discovery rate and presented as adjusted P value. Mean values are presented ±SD. Data were analyzed with SPSS software version 25.0 (SPSS Inc, Chicago, IL). METHODS RESULTS Patient Population This is a retrospective cohort study of patients who were diagnosed with AVPM and were evaluated and followed at the Sheba Medical Center’s Neuro-ophthalmology Unit between 2011 and 2020. The study was approved by the medical center’s institutional review board and adheres to the tenets of the Declaration of Helsinki. Informed consent was waived for this retrospective analysis. The study inclusion criteria were: 1. surgery, radiotherapy, or both; 2. documented pre-treatment neuro-ophthalmic evaluation including VF study; 3. an OCT study that included a ganglion cell layer–inner plexiform layer complex (GCC) evaluation; and 4. a minimum follow-up period of 6 months. Patients with ocular diseases which could cause pathological changes in OCT, such as glaucoma, were excluded, as were those whose OCT was of unsatisfactory quality (a signal strength of less than 7). The eye chosen for analysis was based on the location of the meningioma, and the more affected eye was selected in cases of bilateral compression. Details on baseline demographics, meningioma location, time to intervention, and type of intervention were collected. Data including best-corrected visual acuity (BCVA) by means of Snellen chart and converted to logarithm of the minimum angle of resolution (LogMAR) for the purposes of data analysis, and the comprehensive ophthalmological examination findings were recorded. The perimetric mean deviation (MD) as measured in decibels (dB) by the Humphrey VF machine was noted before intervention and at the 6-, 12-, and 24month follow-up visits. OCT was performed with CIRRUS OCT (Carl Zeiss Meditec, Dublin, CA). The analyzed OCT parameters were preinterventional average RNFL thickness and average GCC thickness. Patient Characteristics Thirty-eight suitable patients were identified among 186 potential patients whose medical records were reviewed (Fig. 1). Their mean age at diagnosis was 52.8 ± 12.2 years (range 25–71 years), and 28 were women (74%). The histopathology of the tumor was meningioma Grade I in 20 patients and Grade II in 4 patients who underwent surgery, and histology was available. There were 29 patients with unilateral involvement and 9 patients with bilateral involvement. The right eye was the affected eye in 25 patients. The tumor origin was clinoid in 12 patients (31.6%), tuberculum in 8 patients (21.1%), optic sheath in 5 patients (13.2%), Sellar in 5 patients (13.2%), olfactory in 5 patients (13.2%), and sphenoid in 3 patients (7.9%) (Table 1). The mean duration of symptoms before intervention was 12.95 months (range 0.2– 60). Twenty-four patients (63%) underwent surgery alone, 11 (29%) underwent radiotherapy alone, and 3 (8%) underwent both surgery and radiotherapy. The mean follow-up duration was 3.4 ± 2.3 years (range 0.6–9.2 years). Baseline Ophthalmic Characteristics The preintervention examination findings were as follows: The mean BCVA (LogMar) was 0.25 ± 0.45 (Snellen 20/ 36), and the mean perimetric MD was 210.1 ± 8.2. The optic disc on fundoscopy was described as normal in 23 patients (60.5%) and with pallor in 11 patients (29.9%), Statistical Analysis The patients were divided into 2 groups according to the preintervention GCC measurement on OCT. The instrument’s inner classification is indicated in a color-coded manner in which the color red reflects a value below 95% of normal Kapelushnik et al: J Neuro-Ophthalmol 2023; 43: 96-101 FIG. 1. Flowchart of the study population selection. 97 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution TABLE 1. Baseline clinical characteristics of the study population, divided into thin and normal GCC groups, according to the OCT instrument’s inner classification Thin GCC (N = 25) N (%) Variables Categorical variables Male Female Meningioma location Clinoid Tubercle Optic sheath Sellar Sphenoid Olfactory Treatment Surgery Radiotherapy Combined therapy Optic disc Normal Edematous Continuous variables Age at diagnosis (years) Preintervention LogMar visual acuity Preintervention VF MD (dB) Normal GCC (N = 13) N (%) All Patients (N = 38) N (%) 3 (23.1) 10 (76.9) 10 (26.3) 28 (73.7) P Fisher Exact Test Adjusted P 0.532 7 (28) 18 (72.0) 0.513 6 6 5 3 2 3 (24.0) (24.0) (20.0) (12.0) (8.0) (12.0) 6 (46.2) 2 (15.4) 0 (0.0) 2 (15.4) 1 (7.7) 2 (15.4) 12 8 5 5 3 5 (31.6) (21.1) (13.2) (13.2) (7.9) (13.2) 15 (60.0) 7 (28.0) 3 (12.0) 9 (69.2) 4 (30.8) 0 (0.0) 24 (63.2) 11 (28.9) 3 (7.9) 11 (84.6) 2 (15.4) 34 (89.5) 4 (10.5) 0.657 0.595 23 (92.0) 2 (8.0) Mean (SD) 52.3 (11.56) 0.35 (0.53) 212.5 (8.25) 53.9 (13.9) 0.06 (0.12) 25.8 (6.35) 52.8 (12.27) 0.25 (0.45) 210.1 (8.21) Wilcoxon rank-sum test 0.622 0.001 0.019 0.005 0.047 P , 0.05 is presented in bold. Adjusted P value refers to Benjamini–Hochberg critical value. whereas an edematous optic nerve was observed in the remaining 4 patients (10.5%). Preintervention Optical Coherence Tomography Parameters The preintervention clinical parameters are detailed in Table 1. The average GCC thickness was 65.2 ± 11.7 mm, and the average preintervention RNFL thickness was 88.3 ± 39 mm. According to the OCT device inner classification, 13 eyes were classified as having a normal GCC thickness (mean thickness 75.7 ± 10.6 mm), and 25 eyes were classified as having a thin preintervention GCC (mean thickness 59.7 ± 7.9 mm). There was no significant difference between the normal and thin preintervention GCC groups regarding meningioma location, sex, age at intervention, affected eye, and treatment parameters (Fisher exact test). The mean preintervention VA was 0.057 ± 0.12 and 0.35 ± 0.53 LogMar (Snellen 20/23 and 20/45) (P = 0.001, Adj. P = 0.005) for the normal and thin GCC groups, respectively, and the mean preintervention VF MD was 25.8 ± 6.3 and 212.4 ± 8.25 dB, respectively (P = 0.019, Adj. P = 0.047). Optical Coherence Tomography Parameters and Visual Outcomes Correlation Between Ganglion Cell Complex Thickness and Postintervention Visual Acuity The preintervention average GCC thickness correlated with a better VA outcome at 6 months (rho = 20.5, P = 0.004, Adj. P = 0.01), 1 year (rho = 20.5, P = 0.005, Adj. 98 P = 0.015), and 2 years (rho = 20.5, P = 0.028, Adj. P = 0.042) after intervention. Figure 2A presents these correlations graphically. Correlation Between Ganglion Cell Complex Thickness and Postintervention Visual Field Mean Deviation Average preintervention GCC thickness was not found to have a significant correlation with the 6-month outcome VF MD (rho = 0.3, P = 0.06) and with the 1-year outcome VF MD (rho = 0.3, P = 0.09). The average preintervention GCC thickness correlated significantly with the 2-year VF MD (rho = 0.7, P = 0.001, Adj. P = 0.009). Correlation Between Ganglion Cell Complex Thickness and Improvement in Visual Acuity At 6 months after intervention, the mean change in VA (LogMar VA before intervention minus the LogMar VA at 6 months after intervention) was 0.02 ± 0.08 and 0.14 ± 0.49 (Snellen 20/19 and 20/28) in the normal and thin GCC groups, respectively. These differences were not statistically significant (P = 0.138 Wilcoxon rank-sum test). At 1 year after intervention, the mean change in VA (LogMar VA before intervention minus the LogMar VA at 1 year after intervention) was 20.027 ± 0.47 and 0.18 ± 0.47 (Snellen 20/19 and 20/30) in the normal and thin GCC groups, respectively. These differences were statistically significant (P = 0.018 Wilcoxon rank-sum test). Two years after intervention, the mean change in VA was 20.027 ± Kapelushnik et al: J Neuro-Ophthalmol 2023; 43: 96-101 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution FIG. 3. Correlation between visual acuity change (before intervention minus 2 years after intervention) and preintervention average GCC thickness. The clear line represents the equation with the highest r2 value (presented). Dashed lines represent 95% confidence interval. correction for multiple comparisons, these correlations were not statistically significant. FIG. 2. The clear line represents the equation with the utmost accuracy (cubic) r2 value (presented); dashed lines represent 95% confidence interval. A. Correlation between preintervention average GCC (ϻ) and LogMar BCVA at 2 years after intervention. Thicker preintervention GCC correlates with lower 2-year postintervention LogMar BCVA values (better visual acuity). B. Correlation between preintervention average GCC (ϻ) and VF MD at 2 years after intervention. Thicker preintervention GCC correlates with higher 2-year postintervention VF MD (dB). 0.42 and 0.30 ± 0.55 (Snellen 20/19 and 20/40) in the normal and thin GCC groups, respectively, which was also statistically significant (P = 0.008, Wilcoxon rank-sum test).The average preintervention GCC thickness had a significant negative correlation to the change in VA 6 months after intervention (preintervention VA minus the 6-month postintervention VA) (rho = 20.435, P = 0.013, Adj. P = 0.023), 1 year after intervention (preintervention VA minus the 1-year postintervention VA) (rho = 20.411, P = 0.033, Adj. P = 0.042), and 2 years after intervention (preintervention VA minus the 2-year postintervention VA) (rho = 20.578, P = 0.01, Adj. P = 0.022). Figure 3 graphically depicts the correlation between GCC thickness and the change in VA: The thinner the GCC, the more prominent was the change in VA at 2 years after intervention. Correlation Between Retinal Nerve Fiber Layer Thickness and Postintervention Visual Acuity The preintervention average RNFL thickness was correlated with postintervention VA in all time groups, but after Kapelushnik et al: J Neuro-Ophthalmol 2023; 43: 96-101 Correlation Between Retinal Nerve Fiber Layer Thickness and Postintervention Visual Field Mean Deviation The preintervention average RNFL thickness was not correlated with postintervention VF MD in all time groups (6 months—rho = 0.3, P = 0.062; 1 year—rho = 0.05, P = 0.812; and 2 years—rho = 0.4, P = 0.139, after intervention). These correlations were identical in all treatment modalities. CONCLUSIONS Preservation and improvement of visual function is the primary goal of the management of patients with AVPM. Hence, identifying preoperative visual parameters that predict the visual outcome may assist physicians counseling patients who are considering treatment. Previous studies have used OCT parameters, especially RNFL thickness to predict the visual outcome in patients with various compressive tumors (10,12,14,16). This study aims to determine whether GCC thickness is a useful parameter for predicting the visual outcome in patients with AVPM. Our results show that preintervention GCC thickness can add useful information on the visual outcome. Thicker preintervention GCC correlated with better VA and better results of VF perimetry (Fig. 2). These results are analogous to those of other studies in which the correlation between visual outcome and preintervention RNFL was examined rather than the correlation to GCC (17,18). Although a thin GCC correlated with the inferior visual outcome, patients diagnosed with a thin GCC showed greater improvement in VA after treatment. This could be 99 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution explained by the lower baseline VA among the thin GCC patients. The good baseline VA of patients with normal preintervention GCC (mean Snellen 20/23) creates a "ceiling effect" where patients with near-normal visual have a narrow margin, if any, for improvement. This finding is compatible with the observations of Tieger et al who compared GCC parameters and VF MD between patients with chiasmal compression and normal controls. Similar to our findings, their results showed that despite GCC thinning, the post-treatment visual outcome improved in most patients (12). Loo et al (14) investigated the use of RNFL measurements in predicting the post-treatment visual outcome in AVPM in 12 patients. In their study, the population was divided into normal and thin RNFL groups. The visual outcomes were compared between the groups. They found that patients with thin RNFL did not show significant improvement in VA and in VF MD compared with patients with normal RNFL. When examining correlation between RNFL and VF MD in their study population, without dividing to groups, no significant correlation was found. Some of their findings are similar to ours, and some are different. Like Loo et al we found, before correction for multiple comparisons, that preintervention average RNFL thickness correlated with better postintervention VA. In our study, we did not divide the population to thin and normal RNFL; thus, the significant improvement in VF MD in the normal group was not pointed out in our study as in Loo et al‘s study. Similar to our results, no correlation was found by Loo et al between pre-treatment average RNFL thickness and VF MD outcome (without dividing the population into normal and thin groups).The differences in findings may be explained by the difference in number of patients between our study population (38) and Loo et al‘s (12) and duration of follow-up (mean duration time of 3.4 years vs 11.6 months), respectively. Furthermore, the correction for multiple comparisons was not applied in Loo et al‘s study. Conversely, Loo et al did not study their patients’ GCC parameters, which we focused on. Moon et al (16) also investigated the use of RNFL and GCC as prognostic predictors in chiasmal compression. In their study, 18 patients were prospectively assessed before and after undergoing chiasmal decompression surgery. Those authors concluded that both preintervention RNFL thickness and GCC correlate with VF outcome, and that GCC showed a stronger correlation with the postintervention visual outcome (16). Similar to their study, we found that GCC had the strongest correlation with VF outcome, but we did not observe any correlation between preintervention RNFL thickness and VF outcome. After correction for multiple comparisons, no significant correlation was found between RNFL and VA. This could be explained by differences in study populations and the postintervention duration of follow-up. We investigated patients with AVPM in different locations who had a postintervention follow-up of 2 100 years, whereas chiasmatic compressive tumors were investigated 3 months after intervention in Moon et al‘s (16) study. In addition, our patient population is larger, which may also explain the outcome differences between the studies. Our study did not show significant correlation between RNFL thickness and VA after correction for multiple comparisons. Before correction, our results were similar to other cited studies (10,12,14,16). It was suggested that adjustment for multiple comparisons may reduce the statistical significance by increasing the chances for type II errors that may lead to missing potential important findings (19,20). Our average GCC thickness findings showed a strong correlation with the VF MD at 2 years after intervention. That correlation was weaker and insignificant at 6 months and 1 year after intervention. These results partly match those of Ali et al (21) whose study included 30 patients who were treated for AVPM and were followed for 1 year. Their patients’ VF significantly improved over time, with the most significant improvement having been achieved at 6 months after intervention, followed by additional improvement over the remaining 6 months until study closure (21). This long duration of improvement in VF after intervention, albeit to a greater extent occurring a short time after treatment, is in agreement with the high correlation of preintervention GCC thickness recorded 2 years after intervention in our study. The reason for the improvement in VF MD over time might be because VF continues to improve even a long time after the treatment. Another possible hypothesis is that because VF perimetry is a subjective test, influenced by the examiner, patients improve in taking the test over time, rather than improving their real VF. Another possible reason for the long-duration improvement in VF MD is that VF MD might be improving faster in patients who underwent surgery compared with those treated with radiation. However, when we re-examined the data, we did not find any significant differences between the surgery and radiotherapy groups; therefore, our data do not support such hypothesis. This study has several limitations. Although it has a larger number of participants (n = 38) than most comparable studies in the literature, the sample size is still relatively small, and the study population is very diverse—in tumor location, different treatment modalities, and laterality of optic nerve injury. Finally, its retrospective design is an inherent drawback. The findings of this investigation show a correlation between preinterventional GCC thinning and postintervention VA and VF, in cases of AVPM. The relevance of GCC as a prognostic parameter of the visual outcome in AVPM had not been previously demonstrated in a relatively large group of patients. Moreover, the potential of improvement despite preinterventional GCC thinning can add to the clinical discussion of the prognosis. We recommend that patients with AVPM be advised that OCT evidence of a thin GCC may be a negative prognostic factor, but visual recovery may still occur, and that GCC thinning alone Kapelushnik et al: J Neuro-Ophthalmol 2023; 43: 96-101 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution should not be used as a major criterion in deciding whether treatment should be pursued. STATEMENT OF AUTHORSHIP Conception and design: N. Kapelushnik, R. Huna-Baron, S. Dror. Acquisition of data: S. Dror. Analysis and interpretation of data: N. Kapelushnik R. Huna-Baron. Drafting the manuscript: N. Kapelushnik, S. Dror, R. Huna-Baron. Revising the manuscript for intellectual content: R. Huna-Baron N. Kapelushnik. Final approval of the completed manuscript: N. Kapelushnik, R. Huna-Baron, S. Dror. REFERENCES 1. Ostrom QT, Gittleman H, Liao P, Vecchione-Koval T, Wolinsky Y, Kruchko C, Barnholtz-Sloan JS. 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