**1. Introduction**

Central serous chorioretinopathy (CSC) is characterized by localized serous detachment of the neurosensory retina, with or without focal detachments or alterations of the retinal pigment epithelium (RPE) [1,2]. This disorder, mostly seen in young and middleaged males, typically is self-limited, but it may recur or persist in the chronic form of the disease [1]. Although CSC usually manifests in one eye, it may occur as a bilateral condition. Under this light, in the literature, the incidence of bilateral CSC at the initial visit is reported to be between 5% to 18% [3], whereas a bilateral involvement was found to increase with a longer follow-up [3–6].

The alteration of the choroidal vasculature is a well-known factor in the pathogenesis of CSC [7]. The choroidal involvement was firstly demonstrated by the features on an indocyanine angiography (ICGA), such as hyperpermeable dilated choroidal vessels [8], and this is considered a hallmark of the disease. However, while the ICGA is able to better delineate the choroidal vessels, it does not allow to localize the vascular features in their respective tissue layers [9–11]. Therefore the optical coherence tomography (OCT) development and the introduction of novel imaging techniques, such as enhanced-depth

**Citation:** Tatti, F.; Iovino, C.; Demarinis, G.; Siotto Pintor, E.; Pellegrini, M.; Beale, O.; Vupparaboina, K.K.; Rasheed, M.A.; Giannaccare, G.; Chhablani, J.; et al. En Face Choroidal Vascularity in Both Eyes of Patients with Unilateral Central Serous Chorioretinopathy. *J. Clin. Med.* **2023**, *12*, 150. https://

doi.org/10.3390/jcm12010150 Academic Editor: Hitoshi Tabuchi

Received: 11 December 2022 Accepted: 21 December 2022 Published: 24 December 2022

**Copyright:** © 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

imaging (EDI) and swept source (SS), have facilitated the detailed and depth-resolved evaluation of the choroidal morphology in CSC patients [12–14].

Additionally, a choroidal vasculature evaluation in CSC patients was obtained using the choroidal vascularity index (CVI), a new parameter defined as the ratio between the luminal choroidal area (LCA) and the total choroidal area (TCA) on OCT B-scans [15–18]. In a recent study, this parameter allowed to show an increased vascular component compared with the stromal component in eyes affected by CSC. Indeed, an increased choroidal vascularity index was demonstrated in affected eyes compared with fellow ones. However, fellow eyes also showed a higher CVI in comparison with age-matched healthy subjects. As previously reported, the CVI could then be a useful index for early diagnosis of CSC and the assessment of the treatment response after photodynamic therapy [16,17].

Nevertheless, the CVI measured on the foveal cross-sectional B-scan cannot reveal the overall picture of the choroidal status [19–21]. For this reason, the CVI has been recently measured also on en face OCT scans to obtain a more real representation of the choroidal vasculature in healthy or affected eyes [22,23]. The en face CVI evaluation at various levels of the choroid showed a similar trend of changes in acute and chronic CSC patients [23].

The aim of the present study was to evaluate the CVI changes in both eyes of patients with unilateral CSC by analyzing en face OCT images generated through volumetric maps.

#### **2. Materials and Methods**

A consecutive series of 20 patients with diagnoses of unilateral CSC were evaluated in this retrospective study. All subjects were attended to at the Retina Center of the Eye Clinic, University of Cagliari. The study adhered to the tenets of the Declaration of Helsinki and the protocol used was approved by the local Institutional Review Board (NP/2022/3119). A complete ophthalmic examination was performed for each patient, including Snellen best-corrected visual acuity (BCVA), fundus autofluorescence, fluorescein angiography (FA) and ICGA (Heidelberg Spectralis, Heidelberg Engineering), intraocular pressure (IOP) measurement, anterior segment and fundus examination. Unilateral CSC was defined as a prior or active unilateral manifestation of CSC. Thus, patients evidencing any presence or evidence of previous subretinal fluid in the fellow eyes were excluded from the study. The exclusion criteria were also refractive error >±3, macular pathologies other than CSC, as well as the presence of MNV and any ocular surgery. Patients with a history of any treatment in the previous 3 months and of any previous treatment that could affect CVI were also excluded [24,25]. A history of any previous medications that could cause subretinal fluid was also recorded. The patient group was compared with a gender- and age-matched control group (20 eyes of 10 healthy individuals).

## *2.1. Spectral-Domain Optical Coherence Tomography Analysis*

For each eye, a posterior pole volumetric scan containing multiple high density crosssectional scans (49B, 30 × 20◦) was obtained using the spectral-domain (SD) OCT with EDI mode. The scans were obtained for each patient in the afternoon at the set time frame 2–4 pm. These data were exported from the Heidelberg device as images with a 1:1 pixel ratio.

Central macular thickness (CMT) was defined as the average thickness of a 1 mm diameter circle centered on the foveal center, measuring from the internal limiting membrane and the RPE. Subfoveal choroidal thickness (CT) was obtained by measuring the distance between RPE–Bruch's membrane complex and the choroidoscleral interface.

#### *2.2. Choroidal En Face OCT Extraction*

The algorithm involved in obtaining the en face CVI measurement included the choroidal en face OCT extraction and the binarization of the en face OCT scans, following an already tested procedure [22].

The choroid was firstly segmented from the OCT volume. In particular, each B-scan of the volume scan was analyzed to segment choroid on a previously validated algorithm where the RPE–Bruch's membrane complex and the CSI were identified using structural similarity (SSIM), Hessian analysis and tensor voting [26]. Segmented choroidal sections were subsequently stacked to obtain the choroid volume, and multiple 5 micron spacing en face sections were generated for the CVI analysis.
