Morphologic analysis of the foveal avascular zone for prediction of postoperative visual function in advanced idiopathic epiretinal membrane

doi:10.21203/rs.3.rs-2348296/v1

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Morphologic analysis of the foveal avascular zone for prediction of postoperative visual function in advanced idiopathic epiretinal membrane

https://doi.org/10.21203/rs.3.rs-2348296/v1

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published 27 Jun, 2023

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To investigate the preoperative morphology of the foveal avascular zone (FAZ) for prediction of the postoperative visual function in advanced idiopathic epiretinal membrane (ERM).

21 patients (21 eyes) with unilateral idiopathic ERM who underwent pars plana vitrectomy (PPV) with internal limiting membrane (ILM) peeling were included. Superficial FAZ was measured preoperatively in both eyes using optical coherence tomography angiography (OCTA). Area, perimeter, and circularity of FAZ were achieved, and their rationes between the ERM eyes and the contralateral eyes were calculated to analyze the degree of FAZ distortion in diseased eyes. The best-corrected visual acuity (BCVA) and central foveal thickness (CFT) were measured at baseline and more than 6 months after surgery. The correlations of the preoperative FAZ rationes with BCVA and CFT were assessed.

The FAZ in the eyes with ERM was significantly reduced, and the BCVA was significantly correlated with the area ratio (P = 0.004) and the perimeter ratio (P = 0.005) of the FAZ before surgery. Decimal BCVA changed from 0.326 ± 0.139 to 0.450 ± 0.202 (P = 0.058), and CFT reduced significantly (P = 0.001) after surgery. The preoperative FAZ area and perimeter rationes were significantly correlated with letter score gain (P = 0.001, P < 0.001), and the latter showed significant correlations with the postoperative BCVA (P = 0.031) and CFT reduction ratio (P = 0.008).

The preoperative FAZ perimeter ratio is the best predictor of functional and morphological prognosis after surgery in advanced idiopathic ERM.

Health sciences/Diseases/Eye diseases/Retinal diseases

Physical sciences/Optics and photonics/Optical techniques

Health sciences/Biomarkers/Prognostic markers

Idiopathic epiretinal membrane (ERM) is a common retinal disease. An ERM is fibro-cellular proliferation over the internal limiting membrane (ILM) causing morphological distortion of macula which may lead to metamorphopsia and/or deterioration of visual acuity. The incidence of ERM among Asians was reported as 12.1%, and the rate depends on age and axial length¹.

Pars plana vitrectomy with ERM removal is the mainstay of treatment to reduce traction on the retina for improving morphology and function. The ILM is usually peeled together to avoid the recurrence of ERM². Despite the anatomical improvement after surgery, patients may have persistent visual disturbance. Therefore, several preoperative factors have been researched to predict postoperative visual outcome. Lately, preoperative inner retinal deformation was known to be correlated with postoperative visual improvement³.

Since the early 1990s, optical coherence tomography (OCT) has evolved as an important diagnostic modality for macular diseases. It helps precise and extensive observation of the retinal structures, so the correlation of visual function with distortion of the outer retinal layer could be revealed. In ERM, structural changes of interdigitation and ellipsoid zone within the foveola were first suggested as prognostic factors^4–8. Moreover, OCT has been used to elucidate the correlation of metamorphopsia with structural changes such as thickening of an ectopic inner retinal layer in the fovea due to ERM traction^9–13, and inner retinal changes affecting the pathway of blood vessels^10–14. Although the relationship between the ERM-associated visual disturbance and the retinal structural changes has been revealed by OCT, there is lack of consensus about optimal timing of ERM surgery¹².

Currently, OCT angiography (OCTA) has been renowned as a minimally invasive method for evaluating retinal vessels. Its tomographic nature allows visualization of vascular plexuses layer by layer. It is useful not only in diagnosis of retinal blood vessel diseases, but also in measuring of the foveal avascular zone (FAZ)^15,16. Increase in foveal and decrease in parafoveal vascular density have been discovered by OCTA in eyes with ERM before surgery and vice versa after surgery^17,18. Some recent studies using OCTA have reported the FAZ enlarges and becomes more circular after surgery in eyes with ERM^18–21. However, there is something unrevealed between FAZ morphology and postoperative visual function. Using OCTA in this study, we measured area, perimeter, and circularity of the FAZ before ERM surgery and investigated their associations with postoperative visual functions.

Study population

This is a retrospective observational study which was conducted in the Department of Ophthalmology and Visual Science at Seoul St. Mary’s Hospital, the Catholic University of Korea. This study adheres to the tenets of the Declaration of Helsinki. All protocols were approved by the Institutional Review Board (IRB) of our institution (KC22RISI0584). Written informed consent procedures were exempted based on the provisions of the IRB, due to the retrospective nature and data anonymization of the study.

21 patients with idiopathic ERM suffering from decrease of visual acuity or metamorphopsia detected by Amsler grid findings underwent PPV with ILM peeling and perfluoropropane (C₃F₈) gas tamponade at our clinic from 2021 September to 2022 April.

We excluded patients with a history of ocular trauma, retinal surgery, or intravitreal injection. Also, cases which had diabetic retinopathy, retinal vessel occlusion, ocular inflammatory disease, or any other vitreoretinal and anterior segment diseases were excluded for reliability of data. None of the patients was excluded because of severely compromised BCVA < 0.05.

Study Protocol

Study protocol

At the initial visit, all subjects’ demographic data, medical and ophthalmologic history were collected. They were examined by slit-lamp microscopy, and dilated fundus examination was also done. Axial length (AL) was measured using IOL-Master 700 (Carl Zeiss Meditec, Jena, Germany), and OCTA imaging was performed by DRI Triton SS-OCT (Topcon, Tokyo, Japan) before surgery. Snellen BCVA and OCT images were achieved before and at least 6 months after surgery. All OCT and OCTA images were reviewed and analyzed independently by two experienced independent retinal specialists (Y-H.P. and G-H.K.) who were blinded to each other and to the clinical histories of subjects. Normal contralateral eyes of all subjects were also evaluated as controls considering that the morphology of the FAZ could be influenced by the patient’s demographic characteristics.

Surgical Technique

Under general anesthesia, a standard 25-gauge 3-port PPV (Constellation device, Alcon, Fort Worth, TX, USA) was conducted by the same experienced surgeon (Y-H.P.). Phacoemulsification and posterior chamber intraocular lens (Artis PL E; Cristalens Industrie, Lannion, France) implantation were performed before if necessary. In every patient, vitrectomy was fully performed, so that posterior hyaloid was elevated and trimmed until the peripheral vitreous base. A macular ERM was peeled, and ILM was also peeled off with forceps in an area of at least 2-disc diameter around the fovea after indocyanine green (ICG) staining. The peripheral retina was thoroughly inspected, and barrier photocoagulation by argon laser was conducted around any degenerative lesions, retinal tears or holes. Finally, the vitreous cavity was filled with 14% C₃F₈ gas. Patients were mandated to be in prone position at least for a week after the surgery. At postoperative follow-ups, BCVA was measured. Postoperative OCT was performed at 6 months after the surgery, when the gas tamponade was totally absorbed.

Oct/octa Image Analysis

Preoperative OCT/OCTA images were acquired for both eyes the day before the operation. Postoperative OCT images were taken for the ERM eyes after more than 6 months from the operation day. All images fulfilled an image quality above 65 with no line artifacts or noise.

We analyzed the morphology of macular based on the 12 mm x 12 mm 3D scan mode SS-OCT images. Pre- and postoperative CFT were measured manually using the digital caliper function featured in Topcon image-NET 6 software. We obtained the preoperative FAZ for the superficial layers, between the ILM and the inner plexiform layer, by analyzing 4.5 × 4.5 mm OCTA images with built-in tool of Topcon image-NET 6 software.

The FAZ in both eyes of healthy adults is known to be of the same size. Therefore, using the fellow eye as control, we could define the FAZ parameter (area, perimeter, or circularity) ratio as the ratio of the FAZ parameter of the preoperative ERM eyes to the contralateral control eyes as below.

FAZa = FAZ area ratio = FAZ area of the ERM eye / the control eye

FAZp = FAZ perimeter ratio = FAZ perimeter of the ERM eye / the control eye

FAZc = FAZ circularity ratio = FAZ circularity of the ERM eye / the control eye

We investigated the correlations of the FAZ parameter rationes with pre- and postoperative visual acuity, letter score improvement, and CFT. Representative cases are illustrated in Fig. 1.

Statistical analysis

Continuous variables were presented as the mean ± standard deviation (SD). Normal distributions of the data were examined before choosing the statistical analysis methods. Differences from gender or laterality of the study eye on other variables were inspected using Mann–Whitney U test. The measurements of BCVA were converted into the logarithm of the minimum angle of resolution (LogMAR) and Early Treatment Diabetic Retinopathy Study (ETDRS) letter score to analyze changes of BCVA after the operation. Functional and anatomical improvements were analyzed by Wilcoxon signed-rank test. Correlation analysis was performed to figure out any inappropriate dependency among preoperative parameters. Finally, univariate linear regression analysis was performed to show detailed correlations between presumed prognostic factors and postoperative outcomes. Statistical analysis was performed using the Statistical Package for the Social Sciences for Windows (Version 26.0, SPSS Inc., Chicago, IL). P-values of < 0.05 were considered as statistically significant.

Data from 21 eyes of 21 patients (9 males and 12 females) with an age range from 54 to 76 years (mean 63.900 ± 7.120 years) were included in this study. Only one eye (4.762%) was pseudophakia. The others (95.238%) had a clear phakic lens and underwent phacovitrectomy. Demographics, preoperative characteristics of the study eyes are provided in Table 1. Generally, the FAZ was significantly contracted and distorted compared with the contralateral eye preoperatively as shown in Table 2. The mean BCVA seemed to be improved after surgery compared with the preoperative values, but the differences were not enough to be statistically significant. CFT was selected as a representative parameter of the morphology of ERM, and there were significant differences between preoperative and postoperative CFT (Table 3).

Postoperative letter score gain correlated with preoperative BCVA (r = 0.750, P < 0.001), FAZa (r= -0.669, P = 0.001) and FAZp (r = -0.712, P < 0.001). However, postoperative final BCVA was significantly correlated only with preoperative FAZp (r = 0.472, P = 0.031) (Fig. 2) (Table 4). Preoperative CFT had significant correlations with preoperative BCVA (r = 0.658, P = 0.001), FAZa (r = -0.460, P = 0.036), FAZp (r = -0.601, P = 0.004). Postoperative CFT was associated with preoperative FAZc (r = -0.487, P = 0.025). We defined CFT reduction ratio as a ratio of postoperative to preoperative CFT to avoid individual variations and to represent the morphological improvement after the surgical intervention. It was significantly correlated with preoperative FAZp (r = 0.564, P = 0.008) (Fig. 2) and FAZc (r = -0.486, P = 0.025) (Table 5).

Table 1

Demographics of the patients and characteristics of the study eyes.
Total Number of Eyes	21
Age (years)	63.900 ± 7.120
Axial length (mm)	23.774 ± 1.258
Laterality (right : left)	9 : 12
Sex (male : female)	5 : 16
Lens status (phakia : pseudophakia)	20 : 1

Data are presented as the mean ± standard deviation or a ratio, as appropriate.

Table 2

Preoperative FAZ parameters in the ERM eyes and the control eyes
	ERM eyes	Control eyes	Ratio	P
FAZa	0.154 ± 0.116	0.362 ± 0.088	0.448 ± 0.341	< 0.001
FAZp	1.810 ± 0.671	2.697 ± 0.406	0.687 ± 0.282	< 0.001
FAZc	0.511 ± 0.078	0.618 ± 0.066	0.842 ± 0.194	0.002
Data are presented as the mean ± standard deviation

FAZa, FAZ area ratio; FAZp, FAZ perimeter ratio; FAZc, FAZ circularity ratio

Table 3

Visual function and morphology before and after surgery in the ERM eyes
	Preoperative	Postoperative	P
BCVA (Decimal)	0.326 ± 0.139	0.450 ± 0.202	0.058
BCVA (LogMAR)	0.538 ± 0.228	0.400 ± 0.225	0.094
ETDRS letter score	58.095 ± 11.389	65.000 ± 11.233	0.094
CFT	530.143 ± 98.734	412.095 ± 83.113	0.001
Data are presented as the mean ± standard deviation

Statistically significant P-value is shown in bold.

BCVA, Best-Corrected Visual Acuity; ETDRS, Early Treatment Diabetic Retinopathy Study; CFT, Central Foveal Thickness

Table 4

Correlations of visual function with preoperative parameters
Preoperative	Preoperative BCVA (LogMAR)		Postoperative BCVA (LogMAR)		ETDRS letter score gain
Preoperative	r	P	r	P	r	P
BCVA (LogMAR)	-	-	-0.112	0.630	-0.750	< 0.001
FAZa	-0.598	0.004	0.399	0.073	-0.669	0.001
FAZp	-0.589	0.005	0.472	0.031	-0.712	< 0.001
FAZc	-0.233	0.310	-0.175	0.449	-0.041	0.861
Axial length	-0.111	0.632	-0.034	0.884	-0.052	0.822

Statistically significant P-value is shown in bold.

BCVA, Best-Corrected Visual Acuity; FAZa, FAZ area ratio; FAZp, FAZ perimeter ratio; FAZc, FAZ circularity ratio

Letter score gain = Postoperative ETDRS letter score - Preoperative ETDRS letter score

r = correlation coefficient, P = significant value.

Table 5

Correlations of morphology with preoperative parameters
Preoperative	Preoperative CFT		Postoperative CFT		CFT reduction ratio
Preoperative	r	P	r	P	r	P
BCVA (LogMAR)	0.658	0.001	-0.044	0.850	-0.402	0.071
FAZa ratio	-0.460	0.036	-0.136	0.558	0.398	0.074
FAZp ratio	-0.601	0.004	0.245	0.285	0.564	0.008
FAZc ratio	0.192	0.406	-0.487	0.025	-0.486	0.025
Axial length	-0.166	0.472	-0.095	0.683	0.089	0.702

Statistically significant P-value is shown in bold.

BCVA, Best-Corrected Visual Acuity; FAZa, FAZ area ratio; FAZp, FAZ perimeter ratio; FAZc, FAZ circularity ratio

CFT reduction ratio = Postoperative CFT / Preoperative CFT

r = correlation coefficient, P = significant value.

The indications for the surgical intervention for idiopathic ERM have not been agreed²². Surgical patient selection depends on the symptoms of patients, their visual requirements, and technical proficiency of the surgeon. But ERM patients usually have moderately good preoperative vision²². Therefore, the selection should be careful, and importance of preoperative predictors for postoperative visual outcome has been raised.

We obtained automated quantitative FAZ measurements on superficial plexuses by OCTA images with built-in tool of Topcon image-NET 6 software. In this study, the preoperative FAZ area was generally smaller and more distorted in the ERM eyes compared with the corresponding control eyes as reported previously. Preoperative FAZ reduction may reflect degree of retinal structural abnormality due to ERM contraction nearby the foveal center. In accordance with previous studies, we also found that eyes with thicker CFT prone to have smaller FAZ^21,23. Yoshida et al. reported that there was inverse correlation between the FAZ area and stage of ERM, suggesting that the retinal structure changes both vertically and horizontally due to the contraction force by an ERM²⁴. And this is not just about the morphology but also about the visual function. In eyes with smaller FAZ, visual acuity was more severely compromised than eyes with relatively larger FAZ²³. More contracted FAZ (smaller FAZa and FAZp) seems to be related with higher mechanical stress on the outer retina. A higher preoperative FAZ contraction rate was also associated with a more significant improvement in visual acuity after surgery^23,24. According to the previous study, FAZ was known to enlarge and become more circular postoperatively^23,24. Hence, if the ERM is only associated with FAZ contraction but has not yet caused fragmentation of ellipsoid zone, surgical removal of the ERM may improve the visual acuity proportionally to the degree of the mechanical stress caused by the ERM. However, there is only one previous study about the relationship between preoperative FAZ measurements and final visual function after ERM surgery, and the result was also inconsistent because the correlation between preoperative FAZ circularity and BCVA was established only at 3 months after the operation²⁵. In this study, we unprecedentedly discovered the preoperative parameter which shows statistically significant correlation with the relative long-term final postoperative BCVA, the preoperative FAZ perimeter ratio.

The reason for our new discovery would be the characteristics of our study population. Compared to the previous studies, which had mean baseline Snellen BCVA 0.63, 0.48, and 0.59^22–24, our study population has considerably lower preoperative visual acuity. And the improvement in visual function after surgery was not even statistically significant in this study, unlike previous reports^22–24. Our study population has generally more advanced ERM, and surgical patient selection in our clinic seems to be more conservative. Geometrically, shape of FAZ can be categorized into four types; small and circular; small and irregular; large and circular; large and irregular (Fig. 3). In the population of more severe ERM patients, proportion of large but circular (normal) FAZ would decrease. Then, long perimeter of FAZ statistically means large and irregular FAZ in this population. Therefore, decorrelation between preoperative FAZ perimeter and postoperative visual function can be established.

Our new discovery would give theoretical understanding about statistics of FAZ morphology in ERM and provide practical application to the clinics of conservative surgical patient selection. Especially, technical simplicity of our pragmatic method would facilitate actual use in the clinical office.

There are some limitations in this study. First one is its retrospective nature with a relatively small number of cases and a short follow-up period. Second, errors in segmentation process may occur due to disruption of the retinal structure by ERM contraction, and this leads to incorrect FAZ analysis. Using built-in automatic tool of Topcon image-NET 6 software, our FAZ analysis could be free from human bias, but, on the other hand, it might suffer from inadvertent technical errors. In the future, more cases should be analyzed including not only the superficial retinal plexuses but also the deep retinal vessels. Third, postoperative FAZ analysis was not conducted in our study for economic reasons. Despite consistent results from previous studies about comparison between pre- and postoperative FAZ in ERM^23,24, it would be better to verify it again in our study. Further evaluation of various stages of ERM cases using OCTA before and after surgery would provide deeper understanding of our new findings.

Acknowledgements: This study was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF-2020R1F1A1074898).

Author contributions: K.G.H., P.Y.H.; Designed and performed experiments, analysed data and co-wrote the paper. K.G.H., H.B.E., C.H., K.J.Y; Performed experiments and analysed data. K.R.Y., K.M.; Performed statistical analyses. P.Y.G., P.Y.H.: Supervised the whole research.

Data availability statement: The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Additional Information: None of the authors have any conflicting interests to disclose.

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No competing interests reported.

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Morphologic analysis of the foveal avascular zone for prediction of postoperative visual function in advanced idiopathic epiretinal membrane

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Abstract

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Introduction

Methods

Study population

Study Protocol

Surgical Technique

Oct/octa Image Analysis

Statistical analysis

Results

Discussion

Declarations

References

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