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Leopard-Spot Pattern of Yellowish Subretinal Deposits in Central Serous Chorioretinopathy
Tomohiro Iida, MD;
Richard F. Spaide, MD;
Anton Haas, MD;
Lawrence A. Yannuzzi, MD;
Lee M. Jampol, MD;
Robert L. Lesser, MD
Arch Ophthalmol. 2002;120:37-42.
ABSTRACT
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Objective To describe clinical and angiographic features of patients with central
serous chorioretinopathy (CSC) who had yellowish subretinal deposits forming
a reticulated leopard-spot pattern during fluorescein angiography.
Methods We conducted case studies using the clinical and photographic records
of 5 patients.
Results All 5 patients were older men between the ages of 68 and 81 years who
had been treated with corticosteroids and had bilateral CSC. Nine eyes of
the 5 patients developed yellowish deposits in a reticulated pattern in the
macular region under the chronic detached neurosensory retina. The pattern
of leopard-spot deposits was well demonstrated on the fluorescein angiogram,
with hypofluorescence in most of the deposits and hyperfluorescence from atrophy
of the retinal pigment epithelium. Later phases of the fluorescein angiographic
study showed leaks from the retinal pigment epithelium. During the indocyanine
green angiography evaluation of 4 patients, all had bilateral multifocal patches
of hyperfluorescence in the midphase, findings typical of CSC.
Conclusions Yellowish deposits forming a reticulated leopard-spot pattern may occur
under the neurosensory retina and are associated with chronic neurosensory
detachment caused by CSC. All patients were older men being treated with corticosteroids.
This report described a newly recognized finding: the subretinal deposition
of a yellowish material in a leopard-spot pattern in eyes with CSC.
INTRODUCTION
CENTRAL SEROUS chorioretinopathy (CSC) is characterized by an idiopathic
detachment of the neurosensory retina associated with 1 or several leaks at
the level of the retinal pigment epithelium (RPE), demonstrable on fluorescein
angiography. It typically occurs in young men; however, there are reports
of CSC in patients 50 years and older.1-3
Additional ophthalmoscopic findings in CSC may include pigment epithelial
detachment, alteration in the appearance of the pigmentation in the macular
region, dependent atrophic tracts, capillary telangiectasis and nonperfusion,
retinal neovascularization, choroidal neovascularization, and subretinal deposition.1, 3-10
Patients with CSC may have intraretinal or subretinal deposits. These
occur in 2 forms: gray-white fibrinous subretinal exudates, commonly refered
to as fibrin,3, 7-10
and intraretinal or subretinal lipid.3-4
In this article, we describe 5 men with CSC who had yellowish subretinal deposits
that formed a reticulated pattern on ophthalmoscopy and that had a more dramatic
leopard-spot appearance in the affected areas during fluorescein angiography.
The purpose of this study is to summarize the clinical and angiographic features
of this form of CSC.
PATIENTS AND METHODS
Patients were considered to have CSC if they had (1) ophthalmoscopic
findings of subretinal fluid in the posterior pole; (2) fluorescein angiographic
evidence of leakage from the level of the RPE; and (3) no history or signs
of clinically evident intraocular inflammation, choroidal neovascularization,
or other conditions related to the exudation of subretinal fluid.
After giving their consent, the patients underwent complete ophthalmic
examinations, color fundus photography, contact B-scan ultrasonography, and
fluorescein angiography. Four of them had indocyanine green (ICG) videoangiography
(Topcon TRC-50 IA fundus camera; Topcon ImageNet H 1024 Digital Imaging System;
Topcon USA, Paramus, NJ).
PATIENT 1
A 68-year-old white man had decreased vision in his left eye. He had
a medical history of asthma and polymyalgia rheumatica and had been treated
with systemic corticosteroids for several years. His best-corrected visual
acuity was 20/20 OD and 20/60 OS. The right eye had some pigmentary disturbances
in the macula and several focal leaks during fluorescein angiography consistent
with CSC. There was no evidence of choroidal vascular filling defects. The
left eye had an ovoid neurosensory retinal detachment in the macula with an
underlying pigmentary disturbance and an accumulation of yellowish subretinal
deposits (Figure 1). Fluorescein
angiography of the left eye showed several leaks from the RPE consistent with
CSC.
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Figure 1. Patient 1: a 68-year-old man.
At the initial visit, the left eye had a neurosensory detachment (arrows)
and flecks of yellow material (arrowheads) in the superior macula.
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Two and a half years later, the patient developed a central deposit
with reticular flecks of material in an area bounded by the neurosensory detachment
in the left eye (Figure 2A). These
yellowish deposits seemed to be situated under the neurosensory retina. The
right eye had a shallow neurosensory detachment with pigmentary disturbances
and yellowish subretinal deposits in the macula (Figure 2B). The patient's best-corrected visual acuity was 20/30
OD and 20/400 OS. In the fluorescein angiographic evaluation of the left eye,
most of the deposits blocked the underlying choroidal fluorescence, whereas
the areas between the deposits were hyperfluorescent because of RPE atrophy,
producing a negative pattern of the ophthalmoscopic picture and a leopard-spot
pattern (Figure 2C). The fluorescein
angiography also revealed diffuse retinal pigment epitheliopathy with several
subtle leaks from the RPE in both eyes (Figure
2D and 2E). Besides a slight blockage of the fluorescence in the
left eye caused by the yellow material and the neurosensory detachment, ICG
videoangiography revealed only the typical findings of CSC; namely, patchy
areas of hyperfluorescence in the midphase (Figure 2F and 2G) and dispersion of the dye in the late phase in
both eyes. No late staining consistent with choroidal neovascularization was
seen.
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Figure 2. Patient 1: 2 years later.
A, The left fundus shows a central deposit of yellow subretinal material,
with eddies of deposit forming a leopard-spot pattern arranged under the neurosensory
detachment. B, The right eye has a shallow neurosensory retinal detachment
with pigmentary disturbances and yellowish subretinal deposits (arrowheads)
in the macula. Subretinal lipid is also seen. C, Fluorescein angiogram of
the left eye reveals blockage of the underlying fluorescence by most of these
yellow deposits, whereas the areas in between are hyperfluorescent owing to
decompensation of the retinal pigment epithelium (RPE), producing a leopard-spot
pattern. D, The late-phase fluorescein angiogram shows several small leaks
from the RPE and some staining in the left eye. E, In the right eye, fluorescein
angiography shows focal leaks from the RPE. F (left eye) and G (right eye),
The midphase of the indocyanine green angiography shows bilateral patchy hyperfluorescence
due to choroidal vascular hyperpermeability typical of central serous chorioretinopathy.
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Nine months later, the patient was found to have a neurosensory detachment
in both eyes. In the right eye, a reticulated leopard-spot pattern of flecks
was beginning to form under the neurosensory retina. Four years after his
initial symptoms, the central yellowish deposit and reticular flecks in the
left eye had decreased in thickness and had become more fibrotic in appearance
(Figure 3A). The right eye developed
a leopard-spot pattern of yellowish deposits under the detached neurosensory
retina on ophthalmoscopy (Figure 3B).
The visual acuity was 20/40 OD and 20/400 OS. The patient was followed up
for a total of 8 years.
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Figure 3. Patient 1: 4 years after his initial
visit. A, The central yellow deposit has flattened, and there is an area of
metaplasia of the retinal pigment epithelium in the left eye. There are several
new flecks nasal and superior to the optic disc. B, The right eye, which previously
showed only mild affectation with central serous chorioretinopathy, demonstrates
a leopard-spot pattern of yellowish subretinal deposits. A focus of subretinal
lipid can be seen.
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PATIENT 2
An 81-year-old man developed a serous retinal detachment of the macula
from CSC in both eyes. He had a medical history of prostate carcinoma treated
with radiation therapy but had experienced no recurrence. He had developed
radiation neuropathy and pain and had been treated with oral corticosteroids
for several years. His best-corrected visual acuity was 20/50 OD and 20/40
OS. Fluorescein angiography revealed multiple leaks from the RPE in the superior
macula of the right eye and in both the peripapillary and macular regions
of the left eye. Indocyanine green angiography showed patchy areas of hyperfluorescence
in the midphase and dispersion of the dye in the late phase in both eyes.
Nine months later, the right eye had persistent subretinal fluid in
the macula and mild exudates in the inferior macula. The left eye showed peripapillary
subretinal fluid. Both eyes also developed a reticulated pattern of yellowish
deposits under the neurosensory retina. On fluorescein angiography, diffuse
retinal pigment epitheliopathy with multiple subtle leaks in both eyes remained.
The leopard-spot pattern of subretinal deposits was well demonstrated on the
fluorescein angiogram. Eighteen months after the patient's initial examination,
the areas of the leopard-spot pattern increased in size in the right macula
and in the whole posterior pole in the left eye; this was associated with
fluorescein leakage (Figure 4A,
4B, 4C, and 4D). The best-corrected visual acuity was 20/70 OD and 5/400 OS.
The patient was followed up for a total of 18 months.
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Figure 4. Patient 2: an 81-year-old man
who developed chronic central serous chorioretinopathy in both eyes after
using high-dose corticosteroids. A (right eye) and B (left eye), The fundus
photograph shows a deposition of yellow material in a leopard-spot pattern
under both maculas. C (right eye) and D (left eye), Fluorescein angiogram
of both eyes reveals leaks at the level of the retinal pigment epithelium
and a blockage of the underlying fluorescence by most of the yellow deposits.
The pattern of leopard-spot deposits is well-demonstrated on the fluorescein
angiogram.
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PATIENT 3
A 73-year-old man had blurred vision in his right eye. He had a history
of chronic lymphatic leukemia that was in remission. He noted back pain because
of herniated intervertebral disks and had received 3 epidural corticosteroid
injections. He also used nasal corticosteroids for allergic sinusitis. He
developed a decline in visual acuity in the right eye. He had a large serous
detachment associated with subretinal lipid and a reticulated leopard-spot
pattern of yellowish subretinal deposits in the right inferior portion of
the macula in an area of neurosensory retinal detachment (Figure 5A).
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Figure 5. Patient 3. A, A 73-year-old man
developed a serous retinal detachment of the macula associated with subretinal
lipid and a reticulated pattern of yellowish deposits in the right eye. B,
Fluorescein angiography shows diffuse retinal pigment epithelial leaks and
a leopard-spot pattern of subretinal deposits.
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Fluorescein angiography revealed diffuse RPE leaks and a leopard-spot
pattern in the right eye (Figure 5B).
His left eye had a localized serous detachment associated with multiple leakage
from the RPE during fluorescein angiography. Indocyanine green angiography
showed patchy areas of hyperfluorescence in the midphase in both eyes with
no late staining, a finding consistent with CSC. The best-corrected visual
acuity was 20/40 OD and 20/30 OS. After the patient's visual acuity declined
to 20/60 OD, he was treated with laser photocoagulation. Although his acuity
initially improved in the right eye, he continued to have diffuse leakage
and a large serous detachment; subsequently his visual acuity declined to
20/200. He had laser therapy in the left eye with resolution of the serous
detachment, and his acuity remained stable at 20/30 with no evidence of leakage.
The patient was followed up for a total of 4 years.
PATIENT 4
A 68-year-old man had decreased vision in his right eye for several
months and decreased vision in his left eye for 2 weeks. He had undergone
renal transplantation 1 year previously and was treated with oral cyclosporine
and oral corticosteroids. His best-corrected visual acuity was 20/400 OD and
20/40 OS. A fundus examination in the right eye showed serous elevation along
the superotemporal and inferotemporal arcades, with the fluid just reaching
the fovea. There was some serous fluid at the inferotemporal periphery. Yellowish
deposits in a reticulated pattern were present at the posterior pole and inferotemporal
periphery. In the left eye were serous fluid, pigmentary mottling, and yellowish
subretinal deposits inferior to the optic disc. Subretinal lipid was seen
at the macula. Fluorescein angiography showed extensive pigment disruption
of the RPE with leaks along the inferotemporal vessels in the right eye. In
the left eye there was minimal leakage. On fluorescein angiography, the leopard-spot
pattern was demonstrated in the areas of yellowish deposits in both eyes.
Although the amount of fluid fluctuated in both eyes during the 7 years of
follow-up, the area of leopard-spot changes gradually increased. The patient
was followed up for a total of 7 years.
PATIENT 5
A 73-year-old man had bilateral decreased vision that had reportedly
started 2 months previously. He had a history of prostate carcinoma treated
with radiation but no recurrence. He also had a medical history of chronic
obstructive pulmonary disease and asthma and had been treated with oral corticosteroids
for the asthma. His best-corrected visual acuity was 20/80 OD and 20/70 OS.
He developed a serous retinal detachment, subretinal lipid, and yellowish
deposits of the macula with multiple subtle fluorescein leaks from the RPE
in both eyes. The pattern of leopard-spot subretinal deposits was well demonstrated
on the fluorescein angiogram. Indocyanine green angiography showed patchy
areas of hyperfluorescence in the midphase and dispersion of the dye in the
late phase in both eyes. The patient was followed up for a total of 3 years.
RESULTS
All 5 patients in our study were older men who were treated with corticosteroids
for a long-term period and subsequently developed bilateral CSC. The mean
age of the patients when first seen was 72.6 years with a range of 68 to 81
years. The patients were followed up for a mean period of 4 years and 9 months
(range, 1.5-8.5 years). The patients had yellowish deposits on ophthalmoscopy,
and during fluorescein angiography a dramatic leopard-spot pattern was discernable
that seemed to be located under the chronic detached neurosensory retina as
a result of CSC. One patient had a unilateral and 4 patients had bilateral
leopard-spot pattern deposits. During the follow-up period, 4 eyes of 2 patients
developed a leopard-spot pattern of yellowish deposits under the chronically
detached neurosensory retina. Although the remaining 3 patients had the leopard-spot
changes initially, evidence suggested that the chronic detachment was caused
by a long-term visual disturbance, subretinal lipid, or both. There was no
hemorrhage, subretinal fibrin, or inflammatory cells in the eyes of any patient.
Ophthalmoscopic and ultrasonographic studies failed to show evidence of ciliochoroidal
detachment or choroidal thickening.
During the fluorescein angiographic evaluation, all patients were found
to have diffuse retinal pigment epitheliopathy with subtle leaks. Most of
the deposits blocked the underlying choroidal fluorescence, whereas the areas
between the deposits were hyperfluorescent because of RPE atrophy, producing
a leopard-spot pattern. Fluorescein angiography also revealed multiple leaks
from the RPE. The pattern of subretinal reticular leopard-spot deposits was
well demonstrated on the fluorescein angiogram and was easier to discern using
this technique than with ophthalmoscopy. During the ICG angiographic evaluation
of 4 patients, all demonstrated bilateral multifocal patches of hyperfluorescence
in the midphase and dispersion of the dye with silhouetting of the larger
choroidal vessels in the late phase, findings typical of CSC.11
No occlusion of the choriocapillaris was apparent, and no late staining consistent
with choroidal neovascularization was seen.
COMMENT
We describe 5 men ranging in age from 68 to 81 years with chronic CSC
and yellowish deposits under a detached neurosensory retina in the macular
region (seen during ophthalmoscopy) that caused a leopard-spot pattern on
fluorescein angiography. The fluorescein angiographic findings were characterized
by hypofluorescence of most of the deposits and mottled hyperfluorescence
from the atrophy of the RPE. Later this evaluation revealed several leaks
consistent with diffuse retinal pigment epitheliopathy. The pattern of subretinal
leopard-spot deposits was well demonstrated on fluorescein angiography. Indocyanine
green angiography revealed multifocal choroidal vascular hyperpermeability
in a pattern characteristic of CSC11-13
but did not show findings typical of choroidal neovascularization or infarction
of the choriocapillaris.14 Although the literature
contains reports of CSC in patients with subretinal deposits,3-4,7-10
to the best of our knowledge, the yellowish deposits located at the level
of the RPE that form a leopard-spot pattern, as found in our study, have not
been described in CSC.
Mottled or leopard-spot hyperpigmentation and secondary retinal detachment
may develop in patients with chronic serous detachment of the choroid and
ciliary body in idiopathic uveal effusion syndrome.15
None of our 5 patients had either ophthalmoscopic or ultrasonographic evidence
of ciliochoroidal detachment or choroidal thickening. All 5 of our patients
had multiple fluorescein leaks from the RPE, which are not usually seen in
uveal effusion syndrome. Although leopard spots are seen in uveal effusion
syndrome, they are caused by mottling of the RPE. Our patients had deposits
of a yellowish material at the level of the RPE. Furthermore, there was no
shifting of the subretinal fluid.
Gass et al16 described 4 patients with
serous retinal detachment associated with RPE derangement in the posterior
pole after organ transplantation. These patients appeared to have a deposition
of subretinal yellow-orange flecks as well as multiple pinpoint areas of fluorescein
leaks. Gass and colleagues speculated that localized intravascular coagulation
induced by subclinical graft rejection affected the choroid, causing the findings
observed in their patients. Our patients had similar fundus findings, but
only patient 4 underwent organ transplantation. None had systemic conditions
associated with intravascular coagulation. Neither the fluorescein angiographic
evaluation nor the ICG videoangiographic examination suggested any filling
defect in the choriocapillaris. In addition, the ophthalmoscopic appearance
and natural course of our patients were different from those of patients with
intravascular coagulopathies caused by neoplasm or sepsis.17-18
The patients described by Gass et al16 had
organ transplantation; these patients are treated with drugs such as corticosteroids
to produce chronic immunosuppression. Corticosteroids have been associated
with the production, exacerbation, and prolongation of CSC, especially diffuse
retinal pigment epitheliopathy.19-24
All patients in our series were being treated with corticosteroids and had
diffuse retinal pigment epitheliopathy. Corticosteroid use is undoubtedly
important in the appearance of these fundus findings.
The leopard-spot pigmentation was also similar in appearance to that
occurring in some patients with systemic large cell lymphoma, leukemia, or
bilateral diffuse uveal melanocytic proliferation.25-28
Infiltration of the choroid and sub-RPE space by lymphomatous cells and leukemic
cells may cause the RPE changes.25-26
Vitreous cellular infiltration and choroidal thickening, frequent features
of ocular involvement by lymphomatous and leukemic cells, were not present
in our patients. The leopard-spot changes seen in lymphomas are caused by
pigmentary clumping, in contrast to the yellowish material seen in our patients.
Patient 3 had a history of chronic lymphatic leukemia, but it was in remission
at the onset of ocular symptoms. The other patients had no systemic conditions
associated with neoplasm.
The 5 men we describe had yellow deposits forming a leopard-spot pattern
under the neurosensory retina associated with chronic neurosensory detachment
caused by CSC. All patients were older men being treated with corticosteroids.
Subretinal fibrin may occur in acute or chronic CSC, and subretinal lipid
may also be seen,3 especially in more chronic
cases such as those in this study. These subretinal deposits may reflect the
subretinal milieu in these patients; there were probably a large amount of
macromolecules present. The yellowish material in our patients appeared to
lie deeper, at the level of the RPE. Certainly macrophages and RPE cells containing
melanin granules may occur,29 but the flecks
seen in our patients were yellow. It is possible that the flecks were composed
of aggregates of RPE cells or macrophages laden with material, perhaps including
macromolecules such as protein or lipid that led to the yellow color.
AUTHOR INFORMATION
Accepted for publication September 5, 2001.
This study was supported in part by the Macula Foundation Inc and by
an unrestricted grant from Research to Prevent Blindness Inc, New York, NY
(Northwestern University).
Corresponding author and reprints: Richard F. Spaide, MD, Vitreous-Retina-Macula
Consultants of New York, 519 E 72nd St, Suite 203, New York, NY 10021 (e-mail: vrmny{at}aol.com).
From the LuEsther T. Mertz Retinal Research Center, Manhattan Eye,
Ear and Throat Hospital, and the Vitreous-Retina-Macula Consultants of New
York, New York, NY (Drs Iida, Spaide, Haas, and Yannuzzi); the Department
of Ophthalmology, Northwestern University Medical School, Chicago, Ill (Dr
Jampol); and the Department of Ophthalmology and Visual Science, Yale University
School of Medicine, New Haven, Conn (Dr Lesser). The authors have no
financial interest in any device or medication discussed in this article.
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