Methods

We prospectively investigated a consecutive series of patients that presented with peripheral exudative hemorrhagic chorioretinopathy in the oncology unit of the Jules Gonin University Eye Hospital Lausanne between October 1, 2007 and April 30, 2011. Assessments were made with dynamic ultrawide-field FA and ICGA, using the Staurenghi 230 SLO Retina Lens (Ocular Instruments, Inc, Bellevue, Washington, USA) and the HRA 2 (Heidelberg Engineering GmbH, Heidelberg, Germany), combined in the Spectralis instrument with an optical coherence tomography (OCT).

Patients underwent ultrawide-field imaging of both eyes, but dynamic imaging of the early phase was carried out only in the affected eye. In cases of bilateral involvement, dynamic imaging was performed on the eye with more active disease. The dynamic sequence began as soon as the dye reached the eye (about 10 seconds after injection). The HRA captured 8.8 frames per second during 30 to 40 seconds of dynamic angiography. The 2 seconds before the manual start of the film were automatically included in the film. Late-frame images were taken up to 30 minutes after dye injection. All images were taken with the high-speed mode (image resolution 768 × 768 pixels).

A complete ophthalmic examination and systemic history were obtained before angiography. The ophthalmic examination included best-corrected Snellen visual acuity (BCVA), slit-lamp examination, intraocular pressure measurement, and dilated fundus examination. Fundus color photographs were taken with the Panoret 1000M camera (Medibel/CMT Technology, Haifa, Israel), using its 100-degree optic contact lens and indirect trans-scleral illumination. B-scan ultrasonography was performed by a retinal specialist with the Quantel Medical CineScan (Version S 5.06; Quantel Medical, Clermont-Fernand, France), using both the 10- and 20-MHz probe.

The diagnosis of peripheral exudative hemorrhagic chorioretinopathy was based on the following inclusion criteria: peripheral mass lesion associated with subretinal or sub–retinal pigment epithelium (RPE) blood or exudation, or evidence of a peripheral fibrotic mass lesion. Peripheral fundus was classified as outside the macula (>3 mm from the fovela). No patient had a history of ocular trauma, inflammation, tumor, or developmental abnormality. Patients with a condition reducing the angiographic image quality (eg, poor dilation, vitreous hemorrhage, advanced cataract, severe corneal opacities) were excluded.

Collected data from the clinical charts and fundus color images included age and sex, laterality, BCVA, macular status, lesion thickness of the lesion on B-scan ultrasonography, number and clinical characteristics of the peripheral exudative hemorrhagic chorioretinopathy lesions, and their location. The angiographic images were analyzed for the choroidal arteriovenous hemodynamics of the choroid on ICGA. This included morphologic characteristics of the choroidal vessels (early frames; ie, 1–5 minutes) and any other pathologic features. In the absence of normative data, the choroidal veins were arbitrarily considered dilated when the diameter was estimated as 5 times larger than that of the retinal veins. The choroidal veins were considered denser when for a group of adjacent choroidal veins (usually about 10 veins; minimum of 5 veins), the distance between the veins was less than their diameter. The vortex veins were arbitrarily considered dilated when larger than 1 disc area.

As a control group for the choroidal vasculature, the quadrants of 30 age-matched unaffected fellow eyes in choroidal nevi patients were examined applying the same criteria. The number of quadrants with fulfilled criterion was counted for each eye and the means (± SD) were compared between pathologic study eyes and control eyes, using the Wilcoxon test (quantitative nonparametrical data). A P value <.05 was considered significant.

Results

Between November 2007 and March 2011, 48 eyes of 40 patients with peripheral exudative hemorrhagic chorioretinopathy (bilateral involvement in 8 cases) underwent dynamic ultrawide-field (150-degree) FA and ICGA. The study population included 22 (55%) female and 18 (45%) male patients, and 27 (56%) right eyes and 21 (44%) left eyes. The mean patient age was 78.1 years (SD 6.6; range, 62 to 90 years). All patients were of white race and had been referred to the ocular oncology unit because of a peripheral mass lesion.

Systemic history revealed treatment with antihypertensive drugs in 22 of the 40 patients (55%), oral anticoagulants in 9 patients (23%), and platelet aggregation inhibitors in 15 patients (38%).

The clinical features of peripheral exudative hemorrhagic chorioretinopathy are shown in Table 1 for all included eyes. Mean BCVA was logMAR 0.36 (SD 0.47), which corresponds with Snellen BCVA of about 20/45, ranging from <20/400 to 20/20. Reduced BCVA was mostly attributable to macular pathologies, including age-related macular degeneration in 12 eyes (5 eyes with drusen, 4 eyes with choroidal neovascularization, and 3 eyes with geographic atrophy), macular edema associated with peripheral exudative hemorrhagic chorioretinopathy in 6 eyes, retinal detachment associated with peripheral exudative hemorrhagic chorioretinopathy in 2 eyes, and vitreomacular traction in 1 eye. The presence of cataract explained a mild-to-moderate reduction of BCVA (20/40–20/25) in 4 eyes, still allowing good image quality.

The peripheral exudative hemorrhagic chorioretinopathy lesions were found in all quadrants, with a predilection for the temporal quadrants. The temporal inferior and superior quadrants were involved in 41 and 32 eyes respectively, and the nasal inferior and superior quadrants in 22 and 8 eyes respectively. A single quadrant was affected in 16 of the 48 eyes (33%), while 15 (31%), 11 (23%) and 6 eyes (13%) showed involvement of 2, 3, and 4 quadrants respectively.

The lesions in the 48 eyes included a peripheral pigment epithelium detachment (PED) in 40 eyes (83%) and an RPE tear in 5 eyes (10%). Hemorrhage was found in 39 of the 48 eyes (81%), including 21 eyes with sub-PED hemorrhage (44%). Lipid exudation was found in 25 of 48 eyes (52%) and subretinal fibrosis in 27 of 48 eyes (56%). Extended RPE alterations (including atrophic changes) were found in the adjacent retinal periphery in 33 of the 48 eyes (69%).

Lesion height was measured on B-scan ultrasound. The mean lesion elevation was 2.1 mm (SD 0.9) and ranged from 1.0 mm to 4.6 mm. No choroidal excavation was found.

Prominent pathologic features on 150-degree FA included window defects (37 eyes) in areas of peripheral atrophic RPE changes, blockage phenomena (34 eyes) attributable to subretinal/sub-RPE hemorrhage or extensive lipid exudation, and staining of subretinal fibrosis (27 eyes). However, no eye revealed any typical sign of choroidal neovascularization on 150-degree FA. The retinal hemodynamic was normal in most patients, although abnormal retinal circulation occurred in 3 cases. One eye showed peripheral areas of retinal nonperfusion (Patient 20), another eye showed concomitant ischemic hemi-central vein occlusion (Patient 8), and a third eye (Patient 11) showed severely delayed retinal filling (>50 seconds).

An overview of the data obtained from the dynamic ultrawide-field ICGA is shown in Table 2 . A predominant finding was the frequent presence of a singular or multiple (up to 7) hyperfluorescent polyp-like spots (33 of 48 eyes, 69%) ( Figures 1 through 6 ). These filled in the venous phase of the ICGA, as shown in Table 2 , and were located at the border of the peripheral exudative hemorrhagic chorioretinopathy lesion (26 of 33 eyes, 79% of the visualized polyp-like spots) and/or under the exudative lesion area (9 of 33 eyes, 27%). These polyp-like vascular dilations were slightly larger than the adjacent choroidal vessels. Their size, filling characteristics, and location in relation to the exudative lesion corresponded with the choroidal vascular polyps that are known to occur in the posterior pole. We therefore called them “peripheral polyp-like choroidal telangiectases.” No comparable observation was made in any control eye. The last patient in the series of study eyes (Patient 40) underwent a peripheral optical coherence tomography examination using the OCT Spectralis. The result showed a dome-like elevation of the RPE over the hyperfluorescent peripheral polyp-like choroidal telangiectasis ( Figure 4 ).

Extensive abnormal choroidal vascular network and numerous peripheral polyp-like choroidal telangiectasis in a patient (Patient 17) with bilateral peripheral exudative hemorrhagic chorioretinopathy. (Top left) Right eye with peripheral fibrosis in the temporal superior quadrant and hemorrhagic and lipid exudation in the temporal inferior quadrant. (Top right) Left eye with extensive serosanguineous exudation in the temporal and inferior quadrants. (Bottom left) Wide-field indocyanine green angiography of the right eye at 3 minutes revealed 2 areas of abnormal choroidal vascular networks (line), associated with 5 polyp-like telangiectatic lesions (arrows) at the border (slightly better visible on later frames; images not shown). (Bottom right) Indocyanine green angiography revealed 7 polyp-like lesions (arrows) in the left eye, seen only on the late frames (image shown: 14 min) because of partial masking by the subretinal hemorrhage.

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