Subjects

For this prospective cross-sectional study, we recruited consecutive patients with CSC who visited the Macular Service at Kyoto University Hospital between January 2014 and November 2014, as well as age-matched healthy subjects. Healthy eyes were recruited from healthy volunteers and unaffected fellow eyes of patients with unilateral retinal diseases (eg, epiretinal membrane, vitreomacular traction syndrome). All of the subjects underwent a comprehensive ocular examination, including autorefractometry, best-corrected visual acuity measurement with a Landolt C chart, slit-lamp biomicroscopy, intraocular pressure measurement, fundus photography (TRC-NW8F; Topcon Corp, Tokyo, Japan), axial length measurement using ocular biometry (IOLMaster; Carl Zeiss Meditec, Jena, Germany), and SS-OCT imaging (DRI OCT-1; Topcon Corp). All patients with CSC also underwent simultaneous FA and IA using the Spectralis HRA+OCT (Heidelberg Engineering, Heidelberg, Germany). CSC was diagnosed if patients had SRD within the macular area, which was confirmed by OCT, and associated with idiopathic leaks from the RPE during FA/IA, excluding other causes of SRD. The exclusion criteria included other macular abnormalities (eg, retinal vein occlusion, age-related macular degeneration, pathologic myopia, idiopathic choroidal neovascularization [CNV], other secondary CNV, intraocular inflammation, history of ocular trauma, poor image owing to media opacity or poor fixation, or history of vitrectomy, anti–vascular endothelial growth factor administration, and photodynamic therapy).

Classification of Central Serous Chorioretinopathy

Patients with CSC were classified into 3 types: classic CSC, diffuse retinal pigment epitheliopathy (DRPE), and multifocal posterior pigment epitheliopathy (MPPE). Classic CSC was defined as only a few spots of leakage from the RPE. DRPE was defined as broad areas of granular hyperfluorescence during FA associated with many indistinct areas of leakage. MPPE was defined as multiple massive leakages from the choroid.

Each type of CSC was divided into active and resolved eyes. Active eye was indicated when the eye had SRD within the macular area. Resolved eye was indicated as the absence of SRD at the time of SS-OCT measurement, showing SRD at the first visit or at the visit before the time of SS-OCT measurement.

Swept-Source Optical Coherence Tomography

Swept-source OCT examinations were performed by trained examiners after pupil dilation. In each subject, horizontal and vertical line scans (12 mm) were obtained through the fovea. Each 3D volumetric scan covered an area of 3 × 3 mm ² and 6 × 6 mm ² , centered on the fovea. Three-dimensional 3 × 3-mm ² volumetric scans consisted of 512 (horizontal) × 256 (vertical) A-scans and 3D 6 × 6-mm ² volumetric scans comprised 512 (horizontal) × 128 (vertical).

Measurement of Choroidal Thickness

Choroidal thickness was defined as the distance between the line corresponding to the Bruch membrane beneath the RPE and the chorioscleral interface. The choroidal thicknesses at the center of the fovea were manually measured from vertical and horizontal scans with a built-in caliber tool, and each length was averaged.

En Face Imaging

In each B-scan of the 3D data set, the outer surface of the Bruch membrane line was automatically determined by the software, and manual corrections were made as necessary using the built-in segmentation-modifying tool. En face images were automatically reconstructed from the 3D data set using software developed by Topcon Corporation. En face images of the choroid were created by being extracted at varying depths every 2.6 μm from the Bruch membrane and were flattened at the level of the Bruch membrane. In the middle row of Figure 1 , the en face images indicated white region for vascular lumens and black region for the vascular wall and choridal stroma.

Representative images of normal left eye of a 37-year-old man. (Top left) Fundus photograph. (Top right) Horizontal section by swept-source optical coherence tomography. The subfoveal choroidal thickness was 274 μm. (Middle) En face images of choroidal vasculature. (Bottom) Binarized images. The white areas indicate the choroidal vascular area. (Middle left) En face images of 3 × 3 mm at the level of the microvasculature of the inner choroid. (Middle second) En face images of 3 × 3 mm at the level of the large choroidal vessels. (Middle third) En face images of 6 × 6 mm at the level of the microvasculature of the inner choroid. (Middle right) En face images of 6 × 6 mm at the level of the large choroidal vessels. (Bottom left) En face binarized images of 3 × 3 mm at the level of the microvasculature of the inner choroid. (Bottom second) En face binarized images of 3 × 3 mm at the level of the large choroidal vessels. (Bottom third) En face binarized images of 6 × 6 mm at the level of the microvasculature of the inner choroid. (Bottom right) En face binarized images of 6 × 6 mm at the level of the large choroidal vessels.

Measurement of Choroidal Vascular Area

To evaluate the area of choroidal vasculature, 2 en face images were used: 1 at the level of the microvasculature of the inner choroid (26 μm below the Bruch membrane) and 1 at the level of large choroidal vessels (the intermediate level between the Bruch membrane and the deepest site of the chorioscleral interface through the fovea). It is reported that choriocapillaris is located about 5–10 μm below the Bruch membrane, and its diameter is about 15–20 μm. Each en face image was created by extracting from 3-dimensional raster scans at every 2.6 μm depth. Thus, we decided to measure the choroidal microvascular area 26 μm below the Bruch membrane. The area of choroidal vasculature of the adopted images was measured using ImageJ public domain software (Wayne Rasband, National Institutes of Health, Bethesda, Maryland, USA; available at http://rsb.info.nih.gov/ij/index.html ). In ImageJ, the command path Image > Adjust > Threshold > Auto was used to distinguish the vasculature and the choroidal stroma, and the adopted images were binarized ( Figure 1 , Bottom row). Binarization of an en face image was done by the Otsu method, which is an automatic threshold selection method from gray-level histograms. Next, the area of the portion of vascular lumens was calculated in the pixel value by using the command path Analyze > Measure in ImageJ. In the present study, the choroidal vascular area of the adopted images was defined as the percentage of the portion of vascular lumen area against whole scan area.

Statistical Analysis

All values are presented as mean ± standard deviation. The measured visual acuity was converted to the logarithm of the minimum angle of resolution (logMAR) for statistical analyses. χ ² Tests were used to compare the distribution of categorical variables. Unpaired t tests were used to compare with control eyes or between states of CSC. Paired t test was used to compare between affected eyes and unaffected fellow eyes in patients with unilateral CSC. One-way analysis of variance (ANOVA) and post hoc Bonferroni test were used to compare among the 3 subtypes of CSC. Bivariate relationships were examined using Pearson product-moment correlation coefficient test. Statistical significance was set at P < .05.

Central Serous Chorioretinopathy Eyes and Unaffected Fellow Eyes Compared With Control Eyes

CSC patients and healthy subjects were similar in age (55.4 ± 12.1 vs 56.5 ± 20.5, P = .797) and axial length (23.6 ± 1.2 mm vs 24.2 ± 1.2 mm, P = .060). There was no significant difference in sex distribution between the CSC patients and healthy subjects (26 men and 14 women vs 12 men and 14 women, P = .130).

The mean subfoveal choroidal thickness of eyes with CSC (395.9 ± 103.3 μm) was significantly larger compared with control eyes (238.0 ± 81.1 μm). The choroidal vascular area was significantly higher in eyes with CSC than in control eyes both at the level of the microvasculature of the inner choroid (3 × 3 mm: 53.4% ± 2.4% vs 52.2% ± 1.8%, P = .028; 6 × 6 mm: 54.0% ± 1.7% vs 51.9% ± 2.1%, P < .001) and at the level of the large choroidal vessels (3 × 3 mm: 66.9% ± 7.1% vs 54.9% ± 4.4%, P < .001; 6 × 6 mm: 64.8% ± 7.3% vs 53.8% ± 4.3%, P < .001) ( Table 1 , Figures 1 and 2 ).

Representative images of right eye of a 46-year-old man with active classic central serous chorioretinopathy. (Top left) Fundus photograph shows serous retinal detachment. (Top second) Fluorescein angiography shows a few spots of leakage from the retinal pigment epithelium. (Top right) Indocyanine green angiography shows choroidal hyperpermeability. (Middle) En face images of choroidal vasculature. The white areas indicate the choroidal vascular area. (Middle left) En face image of 3 × 3 mm at the level of the microvasculature of the inner choroid. (Middle second) En face image of 3 × 3 mm at the level of the large choroidal vessels shows extreme choroidal dilation. (Middle third) En face images of 6 × 6 mm at the level of the microvasculature of the inner choroid. (Middle right) En face image of 6 × 6 mm at the level of the large choroidal vessels shows choroidal dilation. (Bottom) The horizontal image through the fovea by swept-source optical coherence tomography shows serous retinal detachment and increased choroidal thickness (532 μm).

Unaffected fellow eyes and control eyes were similar in age ( P = .608) and axial length ( P = .690). The mean subfoveal choroidal thickness was larger in the unaffected fellow eyes (339.8 ± 101.9 μm) compared with the control eyes ( P < .001). The choroidal vascular area was significantly higher in unaffected fellow eyes with CSC than in control eyes at the level of the microvasculature of the inner choroid (6 × 6 mm: 53.4% ± 1.7%, P = .006), not at the level of the microvasculature of the inner choroid (3 × 3 mm: 52.9% ± 1.9%, P = .162). The choroidal vascular area in the unaffected fellow eyes was larger at the level of the large choroidal vessels (3 × 3 mm: 62.1% ± 7.1%, P < .001; 6 × 6 mm: 61.0% ± 7.1%, P < .001) than in the control eyes ( Table 1 ).

Affected Eyes Compared With Unaffected Fellow Eyes

Comparisons of parametric data of affected eyes and unaffected fellow eyes of the unilateral CSC patients are shown in Table 2 . The mean subfoveal choroidal thickness in the affected eyes was significantly thicker than in the unaffected fellow eyes (384.8 ± 113.8 μm vs 339.8 ± 101.9 μm, P = .005). There was no significant difference in the choroidal vascular area at the level of the microvasculature of the inner choroid. The choroidal vascular area at the large choroidal vessels level was significantly larger in the affected eyes than in the unaffected fellow eyes (3 × 3 mm: 65.5% ± 7.1% vs 62.1% ± 7.1%, P = .012; 6 × 6 mm: 63.2% ± 7.6% vs 61.0% ± 7.1%, P = .030).

Active Eyes Compared With Resolved Eyes

Thirty-three eyes were active status with SRD involving the macula and 7 were resolved eyes with absence of SRD. Table 3 shows comparative data between active eyes and resolved eyes. There was no significant difference in the subfoveal choroidal thickness and the choroidal vascular area between active eyes and resolved eyes.

Table 3

Choroidal Vascular Areas of Active Eyes Compared With Resolved Eyes in Central Serous Chorioretinopathy

	Active (n = 33)	Resolved (n = 7)	P Value
Age (y)	55.6 ± 11.2	54.3 ± 16.6	.801
Axial length (mm)	23.8 ± 1.1	23.2 ± 1.2	.259
Subfoveal choroidal thickness (μm)	384.8 ± 113.8	438.9 ± 101.9	.229
Vascular area (%)
Microvasculature (3 × 3 mm)	53.6 ± 2.5	52.6 ± 2.0	.293
Large choroidal vessels (3 × 3 mm)	67.0 ± 7.3	66.5 ± 6.8	.871
Microvasculature (6 × 6 mm)	54.0 ± 1.7	53.6 ± 1.8	.583
Large choroidal vessels (6 × 6 mm)	64.7 ± 7.4	65.7 ± 7.1	.748

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