Purpose
To study the prevalence and 3-dimensional (3-D) tomographic features of focal choroidal excavations in eyes with central serous chorioretinopathy (CSC) using swept-source optical coherence tomography (OCT).
Design
Prospective, cross-sectional study.
Methods
We examined 116 consecutive eyes with CSC with a prototype 3-D swept-source OCT. 3-D images of the shape of the macular area, covering 6 × 6 mm 2 , were reconstructed by segmentation of the outer surface of the retinal pigment epithelium (RPE).
Results
The 3-D swept-source OCT detected focal choroidal excavations in 9 eyes (7.8%). The 3-D scanning protocol, coupled with en face scans, allowed for clear visualization of the excavation morphology. In 5 eyes with focal excavations, unusual choroidal tissue was found beneath the excavation, bridging the bottom of the excavation and the outer choroidal boundary. Additionally, 3 of those 5 eyes showed a suprachoroidal space below the excavation, as if the outer choroidal boundary is pulled inward by this bridging tissue. The focal choroidal excavations were located within fluorescein leakage points and areas of choroidal hyperpermeability. Eyes with focal choroidal excavations were more myopic (−4.42 ± 2.92 diopters) than eyes without excavations (−0.27 ± 1.80 diopters, P = .001). Subfoveal choroidal thickness was significantly thinner (301.3 ± 60.1 μm) in eyes with focal excavations than in eyes without the excavations (376.6 ± 104.8 μm, P = .036).
Conclusions
Focal choroidal excavations were present in 7.8% of eyes with CSC. In these eyes, focal choroidal excavations may have formed from RPE retraction caused by focal scarring of choroidal connective tissue.
Central serous chorioretinopathy (CSC) is characterized by serous retinal detachment in the macular area, as confirmed by leakage on fluorescein angiography (FA). In eyes with CSC, indocyanine green angiography (ICGA) often shows choroidal vascular abnormalities, such as choroidal filling delay, dilated vasculature, choroidal hyperpermeability, and punctate hyperfluorescent spots. Recent advances in choroidal imaging with optical coherence tomography (OCT), coupled with the enhanced depth imaging technique, have revealed choroidal thickening in eyes with CSC, and such thickening decreased after the treatment with photodynamic therapy. These observations suggest that the underlying pathogenesis of CSC is primarily related to functional abnormalities of the choroidal vasculature.
On the basis of OCT imaging, focal choroidal excavation was recently reported as a localized area of excavation within the submacular choroid. Focal choroidal excavation was first reported to occur in otherwise healthy eyes without any ocular comorbidities. However, later reports showed that focal choroidal excavations are associated with vision-threatening diseases such as CSC, polypoidal choroidal vasculopathy, and choroidal neovascularization. Recently, Margolis and associates reported a case of focal choroidal excavation in an eye with CSC and suggested that there could be an association between the 2 conditions. However, mechanisms underlying this unusual excavation remain unknown. In addition, most previously reported cases of focal choroidal excavations were examined with unidirectional OCT scans and little information is available on the 3-dimensional (3-D) shape of the excavations. So far, the prevalence of focal choroidal excavation remains unknown because previous reports are either single case reports or small case series.
Recent advances in OCT technology include the utilization of a swept-source laser as the light source. The swept-source OCT with a longer-wavelength light source provides better views of the choroid because of improved light penetration into the choroid. Additionally, the tunable laser source of the swept-source OCT shows lower signal decay with depth, further improving the visibility of choroidal details. Furthermore, the higher imaging speed allows for dense scanning and subsequent 3-D image reconstruction of the posterior pole. In the study described herein, we prospectively examined the macular area in a group of consecutive eyes with CSC using a 1-μm-wavelength swept-source OCT to highlight the prevalence, morphology, and 3-D tomographic features of focal choroidal excavation, and the possible correlation between focal choroidal excavation and the pathogenesis of CSC.
Methods
The Ethics Committee at Kyoto University Graduate School of Medicine approved this prospective study, which was conducted in accordance with the tenets of the Declaration of Helsinki. Written informed consent was obtained from each subject before any study procedures or examinations were performed.
We prospectively examined 116 eyes from 99 consecutive CSC patients who presented to the macula clinic at Kyoto University Hospital between the beginning of June 2010 and the end of January 2013. All study subjects were Japanese. All study participants underwent a comprehensive ocular examination, including autorefractometry, best-corrected visual acuity measurement in a Landolt chart, slit-lamp biomicroscopy, intraocular pressure measurement, fundus photography (TRC-NW8F; Topcon Corp, Tokyo, Japan), and 3-D swept-source OCT imaging with a prototype system (Topcon Corp). Simultaneous FA and ICGA, using the Spectralis HRA+OCT (Heidelberg Engineering, Heidelberg, Germany), were performed in most eyes as indicated by the clinical course of the CSC.
Diagnosis and Classification of Central Serous Chorioretinopathy
CSC was diagnosed based on medical history, serous retinal detachment seen on the fundus examination and OCT, and angiographic leakage(s) at the level of retinal pigment epithelium (RPE) in FA. Patients with other causes of fluorescein leakage (eg, age-related macular degeneration, polypoidal choroidal vasculopathy, idiopathic choroidal neovascularization, other secondary neovascular maculopathy) or other causes of serous retinal detachment unrelated to CSC (eg, intraocular inflammation, posterior segment tumors) were excluded from the study.
All CSC cases were classified by FA results into 3 types: classic CSC, chronic CSC, and multifocal posterior pigment epitheliopathy. Eyes showing only 1 or few specific angiographic leakage points at the level of RPE were classified as classic CSC. Eyes with broad areas of granular hyperfluorescence on FA associated with indistinct areas of leakage were classified as chronic CSC. Multifocal posterior pigment epitheliopathy was defined as multiple massive leakages from the choroid into the subretinal space.
All eyes were divided into active and resolved eyes on the basis of the presence of serous retinal detachment at the time of swept-source OCT examination. Active CSC was defined as the presence of a serous retinal detachment and resolved CSC was defined as the absence of a serous retinal detachment. Eyes with resolved CSC that were included in this study had active disease either at the initial clinic visit or at other follow-up visits, but before swept-source OCT examinations.
Swept-source Optical Coherence Tomography and Scan Protocols
The prototype swept-source OCT used in the current study has been previously described in detail. Briefly, this swept-source OCT uses a light source of a wavelength-sweeping laser centered at 1050 nm with a tuning range of 100 nm. This system has a scanning speed of 100 000 A-scans per second and a scan window depth of 2.6 mm. The axial and transverse resolutions are 8 μm and 20 μm in tissue, respectively. The optical power incident on the cornea with the current swept-source laser system is less than 1 mW, which is below the safety requirements for this laser class by the American National Standards Institute.
Swept-source OCT examinations were performed by trained examiners after pupil dilation. In each subject, multi-averaged horizontal and vertical scans of 12 mm were obtained. Fifty single images, where each image consisted of 1024 A-scans, were registered and averaged by software to create a multi-averaged single image. A raster scan protocol of 512 (horizontal) × 128 (vertical) A-scans per data set was acquired in 0.8 seconds to create 3-D data sets (total: 65 536 axial scans/volume). Each raster scan consisted of 128 B-scans and covered an area of 6 × 6 mm, centered on the fovea ( Supplemental Movie , available at AJO.com ). The centration of the scan was achieved with internal fixation target and confirmed by a built-in camera within the swept-source OCT system. Owing to the high speed and the invisible scanning light wavelength, eye movements during the 3-D image acquisition were minimal. To decrease speckle noise, each image was de-noised by the weighted moving average of 3 consecutive original B-scans.
Focal Choroidal Excavation
Diagnosis of focal choroidal excavation was based on the presence of an excavated area into the choroid, along the RPE/Bruch membrane complex line on OCT scans, without any history of prior trauma, infection, or inflammatory episode.
Focal choroidal excavation was classified by OCT as conforming, if photoreceptor tips were attached to the apical surface of the RPE; or as nonconforming, if there was a separation between the photoreceptor tips and the RPE. In terms of location, focal choroidal excavations were classified as foveal, if the foveal center was located within the excavation; or as extrafoveal, if the foveal center was located outside the excavation.
In eyes with focal choroidal excavations, 3-D topographic images were reconstructed from the OCT scans, by segmentation of the line of the outer surface of RPE, to highlight the shape of the excavation. In each B-scan, the outer surface of RPE line was automatically determined by the software and manual corrections were done, as necessary, using the built-in segmentation-modifying tool. The excavation depth and width were measured manually from the 3-D data set in the scan that showed the greatest dimensions. En face OCT scans along the z-axis (C-scans) were obtained from the 3-D data set and the scan showing the excavation at the level of the RPE plane was selected. The excavation boundary in the en face image was marked by a hyper-reflective band, representing the RPE.
Tomographic and Angiographic Features
The tomographic and angiographic features at the area of excavation were examined. Additionally, the correlation between the locations of the excavation and the leakage areas in FA and areas of choroidal hyperpermeability and punctate hyperfluorescent spots in ICGA were analyzed. Choroidal hyperpermeability was defined as cloud-like areas of hyperfluorescence with blurred margins within the choroid in the mid to late phase of ICGA. Punctate hyperfluorescent spots were defined as a cluster of tiny hyperfluorescent spots in the late phase of ICGA within the macular area.
The retinal and choroidal thicknesses at the center of the fovea were manually measured with a built-in caliber tool within the software. Retinal thickness was defined as the distance between the vitreoretinal interface and the outer border of the RPE and choroidal thickness was defined as the distance between the outer border of the RPE and the chorioscleral interface. When the focal choroidal excavation was located within the foveal center, choroidal thickness measurements were made in nearby choroid that was not affected by the excavation.
Statistical Analyses
All values are expressed as mean ± standard deviation. The measured visual acuity was converted to the logarithm of the minimal angle of resolution (logMAR) for statistical analyses. Unpaired t tests were used to compare numerical variable means and Fisher exact tests were used to compare the distribution of categorical variables. Statistical significance was defined as a P < .05.
Results
Of the 116 eyes examined (99 consecutive patients with CSC), 3-D swept-source OCT examination detected focal choroidal excavation in 9 eyes (7.8%) from 8 patients. The mean age of eyes with focal choroidal excavation was 54.9 ± 13.6 years (range: 35-76 years) and all 9 eyes were myopic, with a mean spherical equivalent of −4.42 ± 2.92 diopters. Mean foveal retinal thickness was 194.4 ± 50.6 μm (range: 125-311 μm) and mean foveal choroidal thickness was 301.3 ± 60.9 μm (range: 192-376 μm). Table 1 shows the patient demographics and ocular tomographic features of eyes with focal choroidal excavations. Microperimetry data were available in 3 eyes, all of which had decreased retinal sensitivity at the excavation area.
| Patient | Age (y) | Sex | Visual Acuity b | Refractive Error Spherical Equivalent (Diopters) | Location | Excavation Type | CSC Type | CSC Activity | FRT (μm) | FChT (μm) | Excavation Depth (μm) | Excavation Width (μm) | Previous Treatment | Duration of Follow-up With OCT Examination (mo) |
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| 1 | 76 | M | 1.2 | −0.50 | Extrafoveal | Nonconforming | Chronic | Active | 213 | 331 | 95 | 725 | 0 | 52 |
| 2 | 52 | F | 1.2 | −10.50 | Foveal | Nonconforming | Classic | Active | 311 | 267 | 50 | 902 | rfPDT | 12 |
| 3 | 60 | F | 1.2 | −2.75 | Extrafoveal | Nonconforming => Conforming c | Classic | Resolved | 185 | 228 | 87 | 623 | 0 | 58 |
| 4 a | 35 | M | 1.2 | −3.75 | Extrafoveal | Nonconforming | Chronic | Active | 190 | 376 | 54 | 580 | 0 | 78 |
| 35 | M | 1.5 | −5.75 | Foveal | Nonconforming => Conforming c | Chronic | Resolved | 197 | 328 | 91 | 1237 | 0 | 78 | |
| 5 | 50 | M | 1.5 | −5.50 | Extrafoveal | Nonconforming | Chronic | Active | 195 | 359 | 36 | 414 | 0 | 24 |
| 6 | 62 | F | 1.2 | −5.75 | Extrafoveal | Nonconforming d | Classic | Resolved | 173 | 192 | 69 | 337 | 0 | 73 |
| 7 | 58 | M | 1.0 | −1.75 | Extrafoveal | Nonconforming | Chronic | Active | 161 | 328 | 59 | 547 | 0 | 4 |
| 8 | 66 | M | 0.1 | −3.50 | Foveal | Nonconforming => Conforming c | Chronic | Resolved | 125 | 303 | 82 | 1178 | rfPDT | 6 |
a Patient 4 has bilateral focal choroidal excavation.
c The focal choroidal excavation changed from nonconforming to conforming type upon the resolution of serous detachment in 3 eyes.
d In patient 6, the serous detachment completely resolved, but the photoreceptor tips remained separated from the retinal pigment epithelium at the area of excavation only.
Tomographic Features of Eyes With Focal Choroidal Excavation
The 3-D scanning protocol and en face OCT scans allowed us to detect focal choroidal excavations in the macular area and to clearly visualize their morphology. The focal choroidal excavation had a foveal location in 3 eyes and an extrafoveal location in the remaining 6 eyes. In 2 eyes, extrafoveal excavations were detected with the 3-D scanning protocol, but not with the line scanning protocol ( Figure 1 ). In addition, the 3-D reconstructed images of the macular area showed that focal choroidal excavations can vary in shape, ranging between small dimple-like excavations ( Figure 2 ) to broad irregular excavations ( Figure 3 ). En face images at the level of the RPE showed whether the excavation was filled with outer retinal tissue (conforming excavation) or if the excavation was optically empty, possibly filled with subretinal fluid (nonconforming excavation).
The mean depth of the excavation in the 9 eyes was 69.2 ± 20.7 μm (range: 36-95 μm) and mean excavation width was 727.0 ± 318.0 μm (range: 337-1237 μm). In all 9 eyes, the inner retinal layers appeared physiologically normal and even when the focal choroidal excavation was located subfoveally, the foveal contour remained nearly well preserved. At the excavation, the line of the external limiting membrane was preserved in 8 eyes and disrupted in 1 eye. The line of the junction between the inner and outer segments of the photoreceptors remained continuous in 3 eyes, was partially disrupted in 5 eyes, and was completely disrupted in 1 eye. The RPE line was intact in all 9 eyes, despite some thinning or attenuation.
Swept-source OCT allowed visualization of choroidal structures. Multi-averaged scans often showed an inner choroidal layer with medium-diameter blood vessels and an outermost choroidal layer with larger-diameter blood vessels. In 5 eyes with focal choroidal excavation, unusual choroidal tissue without large vessels was detected beneath the excavation, bridging between the bottom of the excavation and the outer choroidal boundary ( Figure 3 ). In addition, the suprachoroidal space below the focal excavation was observed in 3 of these 5 eyes, as if the outer choroidal boundary was pulled inward by the bridging tissue ( Figure 4 ). The chorioscleral interface was physiologically smooth, with no ectasia, in all 9 eyes.
The mean follow-up duration of eyes with focal choroidal excavation by OCT examination was 42.8 ± 31.4 months (range: 4-78 months). In all 9 eyes, the excavations were located within the serous retinal detachment during the active stage (nonconforming excavation). During the follow-up period, 3 eyes showed resolution of the serous retinal detachment and the photoreceptor tips reattached to the RPE, thus converting the focal choroidal excavation from the nonconforming to the conforming type. In 1 eye, the serous retinal detachment completely resolved, but the photoreceptor tips remained separated from the RPE at the area of excavation. In the 5 eyes that were followed for more than 4 years with OCT, no remarkable changes in excavation size or shape were detected. Additionally, no eye developed new focal choroidal excavation and no eye showed disappearance of the excavation in the macular area during the follow-up.
Fundus and Angiographic Features in Eyes With Central Serous Chorioretinopathy and Focal Choroidal Excavation
All eyes with focal choroidal excavations showed changes in color fundus photographs at the area of the excavation ( Table 2 ). The focal choroidal excavations appeared either as a yellowish lesion with indistinct margins (n = 3 eyes) or as a pigmentary disturbance, which often extended beyond the area of excavation (n = 6 eyes). FA was performed in all 9 eyes, 3 of which showed classic CSC and the remaining 6 with chronic-type leakage. In 8 of the 9 eyes, the focal excavation was located within the area of fluorescein leakage, either as a focal leak (classic CSC) or within the area of granular hyperfluorescence (chronic CSC). In the remaining eye, the focal choroidal excavation was located just adjacent to the focal leakage area in FA. ICGA was performed in 7 eyes, all of which showed choroidal hyperpermeability and punctate hyperfluorescent spots. In all 7 eyes, the focal choroidal excavations were seen within the area of choroidal hyperpermeability ( Figure 3 ).
