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Somanus oongsuwan, M.D., Sakun Narongkiatikhun, M.D., Nuttawut Rodanant, M.D., Nopasak Phasukkijwatana,
Ph.D., M.D., Rawi Jongpipatchai, M.D., Supalert Prakhunhungsit, M.D.
Department of Ophthalmology, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok, ailand.
Multimodal Imaging of Unaffected Fellow Eyes in
Patients with Polypoidal Choroidal Vasculopathy
and Neovascular Age-Related Macular Degeneration
ABSTRACT
Objective: To identify retinal abnormalities in the unaected fellow eyes of patients with unilateral polypoidal
choroidal vasculopathy (PCV) and neovascular age-related macular degeneration (n-AMD).
Methods: In this cross-sectional, retrospective case series, the medical records of patients with PCV and n-AMD were
reviewed and the baseline patient characteristics recorded. Abnormal ndings on spectral-domain optical coherence
tomography (SD-OCT) (steep/notched pigment epithelial detachment [PED], double-layer sign, hyporeective
lumen within the PED), fundus autouorescence (FAF) (ring/patch patterns), and indocyanine green angiography
(ICGA) (punctate hyperuorescence spot [PHS]) were studied.
Results: Seventy-one fellow eyes of patients with PCV and 64 fellow eyes of patients with n-AMD were included.
FAF showed abnormalities in 26 (36.6%) and 33 (51.6%) fellow eyes of those with PCV and n-AMD, respectively
(p=0.081). SD-OCT detected abnormalities in 25 (35.2%) and 36 (56.3%) fellow eyes of those with PCV and
n-AMD, respectively (p=0.014). ICGA detected PHS in 47 (66.2%) and 34 (53.1%) fellow eyes of PCV and n-AMD,
respectively (p=0.122).
Conclusion: Multimodal imaging showed abnormalities in most asymptomatic fellow eyes of patients with PCV
and n-AMD. Regular and long-term self-monitoring and fundus evaluation are important for these patients. e
current ndings support the dierences in the pathogeneses of PCV and n-AMD.
Keywords: Multimodal imaging; fellow eye; Age-related macular degeneration; Polypoidal choroidal vasculopathy
(Siriraj Med J 2021; 73: 121-127)
Corresponding author: Supalert Prakhunhungsit
E-mail: supalert.pra@gmail.com
Received 2 June 2020 Revised 28 August 2020 Accepted 29 August 2020
ORCID ID: http://orcid.org/0000-0002-0211-113X
http://dx.doi.org/10.33192/Smj.2021.17
INTRODUCTION
Age-related macular degeneration (AMD) is a
bilateral disease characterized by either bilateral drusen
or retinal pigment epithelium (RPE) abnormalities. e
deposition of lipid-rich material in the basal lamina
of the RPE and the inner collagenous layer of Bruch’s
membrane has been reported in histologic studies of
eyes with AMD and associated positively with choroidal
neovascularization.
1,2
An estimated 20% of patients with
AMD have neovascular AMD (n-AMD) and most have
unilateral disease at presentation.
3
e fellow eyes of patients
with n-AMD almost always have clinical abnormalities;
however, the vision is unaected.
Polypoidal choroidal vasculopathy (PCV) with a
presentation of serosanguinous maculopathy is dicult to
distinguish from n-AMD clinically, and many clinicians
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believe that PCV is a subtype of n-AMD. However, recent
multimodal imaging studies have suggested dierent
pathogeneses of PCV and AMD. PCV is a clinical
manifestation within pachychoroid disease, which is
a disease spectrum characterized by attenuation of the
choriocapillaris overlaying dilated choroidal vessels and
associated with pigmentation changes in RPE cells, RPE
dysfunction, and new vessel formation.
4
Unlike AMD,
the fundi of the fellow eyes of patients with PCV are
usually unremarkable.
e fellow eyes of patients with unilateral n-AMD
or PCV are the eyes that are at risk. Results from the
Age Related Eye Disease Study showed that the highest
risk level for progression to an advanced stage in the
fellow eyes of patients with unilateral advanced AMD
was 50% by 5 years and 71% by 10 years.
5,6
Imaging
studies in those eyes may provide preclinical information
about AMD and PCV and the dierence in the disease
pathogeneses. We used multimodal retinal imaging to
identify the fundus abnormalities.
MATERIALS AND METHODS
e Siriraj Institutional Review Board, Faculty of
Medicine Siriraj Hospital, Mahidol University, Bangkok,
ailand (Si 057/2015) approved the study protocol.
is study complied with the tenets of the Declaration
of Helsinki (1964) and all of its subsequent provisions.
is retrospective chart review was conducted in patients
with PCV and n-AMD in the outpatient unit, Department
of Ophthalmology, Siriraj Hospital, Mahidol University,
between October 2012 and January 2016. All patients
had been diagnosed with PCV or n-AMD based on
fundus photography, spectral-domain optical coherence
tomography (SD-OCT), fundus uorescein angiography
(FFA), and indocyanine green angiography (ICGA). We
used the Everest study criteria to diagnose PCV based
on clinical and ICGA ndings
7
; to diagnose n-AMD, we
adhered to the eligibility criteria given in the Macular
Photocoagulation Study using FFA.
8
e current study included only patients for whom
data from SD-OCT, fundus autouorescence (FAF),
and ICGA from the fellow eyes were available. We
excluded patients who underwent a previous macular
laser treatment, photodynamic therapy, or intravitreous
injections; patient with other macular diseases, such as
macular scars, geographic atrophy, myopic maculopathy,
and macular holes; and those with poor-quality images.
e data collection included the best-corrected
visual acuity (BCVA), intraocular pressure, and any
underlying systemic diseases. e fundus investigations
included SD-OCT, FAF, and ICGA (Heidelberg Retina
Angiography 2, Heidelberg Engineering, Inc., Heidelberg,
Germany).
One co-author (S.P.) reviewed all the images included in
the study. We set up a prototype image of each characteristic
in each investigation as shown in Fig 1. e FAF ndings
were dened as abnormal hypo- or hyperautouorescence,
i.e., a ring pattern (round hypoautouorescence surrounded
by hyperautouorescence ring), and a patch pattern (hypo/
hyperautouorescence patch without identication of
round-shaped hypoautouorescence)
e SD-OCT ndings were categorized into four
patterns
9,10
: 1) a steep pigment epithelium detachment
(PED), dened as a steep, sharp, peak-like, perpendicular
RPE elevation with underlying moderate reectivity in
the peak; 2) a notched PED, a PED with a V-shaped
depression between two PEDs; 3) a double-layer sign;
two highly reective separated layers, dened as an
undulating RPE line and the hyperreective straight line
of Bruch’s membrane, and moderate hyperreectivity
between these two lines; and 4) a hyporeective lumen
within the PED, a delineated round/oval hyporeective
cavity in the PED.
e ICGA ndings were punctate hyperuorescence
spots (PHS) in mid-phase (5 minutes) was the characteristic
in ICGA.
Abnormal ndings in all investigations were graded
as present or absent. Statistical analyses were performed
using SPSS Statistics version 18.0 (SPSS, Inc., Chicago, IL,
USA). Categorical data are presented as the number or
number and percentage, and continuous data are presented
as the mean ± standard deviation. e demographic
data were summarized using descriptive statistics. e
chi-square test was used to evaluate qualitative variables.
P< 0.05 was considered statistically signicant.
RESULTS
Two hundred and thirty-ve eyes were enrolled in
this study. We excluded 34 eyes with uncertain diagnoses,
35 with poor-quality retinal images, 30 with old brotic
scars, and one previously treated eye. Ultimately, 71
unaected fellow eyes of those with PCV (36.6% were
right eyes) and 64 fellow eyes of those with n-AMD
(46.9% were right eyes, p=0.23) were enrolled. e average
patient ages were 64.8 years and 73.3 years for those
with PCV and n-AMD, respectively (p<0.01). irty-
eight patients (53.5%) in the PCV group and 25 (30%)
of n-AMD group were women.
The mean logarithm of the minimum angle of
resolution VA of the fellow eyes of those with PCV
and n-AMD were, respectively, 0.23 and 0.36 (p=0.09).
No signicant dierences among the groups were seen
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in gender, laterality, or BCVA. However, patients with
n-AMD were signicantly older than those with PCV
(Table 1).
Abnormalities of retinal imaging were found in 65
(91.5%) patients with PCV and 57 (89.1%) patients with
AMD. Fundus autouorescence showed abnormalities
in 26 (36.6%) of those with PCV and in 33 (51.6%) of the
fellow eyes of those with n-AMD (p=0.081). In the fellow
eyes of those with PCV, a ring pattern was observed in
eight eyes (11.3%) and a patch pattern in 18 eyes (25.4%).
In the fellow eyes of those with n-AMD, ring and patch
patterns were identied in 12 eyes (18.8%) and 21 eyes
(32.8%), respectively.
SD-OCT detected abnormalities in 25 fellow eyes
(35.2%) of those with PCV compared to 36 fellow eyes
(56.3%) of those with n-AMD (p=0.014). In the PCV
group, steep or notched PEDs were seen in 23.9%; whereas
1.4% and 11.3%, respectively, had a hyporeective lumen
or double-layer sign. In the n-AMD group, steep or
notched PEDs and double-layer sign were found 46.9%
and 10.9% respectively.
ICGA identied PHS in 47 (66.2%) fellow eyes of
those with PCV and 34 (53.1%) fellow eyes of those with
n-AMD (p=0.12) (Table 2). ICGA showed the highest
rates of abnormalities compared to FAF and OCT in
PCV (40.8%, 14.1% and 2.8%, respectively) and n-AMD
(25%, 4.7%, and 7.8%, respectively).
Abnormalities in multimodality imaging were shown
in Table 3. Only abnormal ndings in both OCT and
FAF were found signicantly higher in n-AMD patients
comparing with PCV patients, 23.4% and 8.5% respectively
(p<0.01).
DISCUSSION
To the best of our knowledge, this is the rst study
to use multimodal imaging to evaluate the unaected
fellow eyes of patients with PCV and n-AMD. Based on
previous reports, the rates of fellow eye involvement have
Fig 1. Representative images of abnormal imaging ndings. Abnormal ndings on spectral-domain optical coherence tomography (SD-
OCT) images are classied as: (A) a steep pigment epithelial detachment (PED) characterized by steep/sharp peak-like and perpendicular
elevation of the retinal pigment epithelium (RPE) with underlying moderate reectivity in the peak; (B) a notched PED, a PED with a
V-shaped depression between two PEDs; (C) a double-layer sign characterized by two highly reective separated layers, which represent
an undulating RPE line and a hyperreective straight line of Bruch’s membrane, and moderate hyperreectivity between these two lines;
and (D) a hyporeective lumen in PED, which is a delineated round/oval sub-RPE cavity. Abnormal fundus autouorescence is classied
into two patterns: (E) a ring pattern, round hypoautouorescence surrounded by a hyperautouorescence ring and (F) a patch pattern, a
hypo/hyperautouorescence patch without identication of round-shaped hypoautouorescence. (G) An abnormal nding in the indocyanine
green angiography images is punctate hyperuorescence spots characterized by multiple hyperuorescent dots at the 5-minute time point.
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TABLE 1. Demographic data of the patients categorized by disease of aected eye.
PCV n-AMD P-value
Number of eyes 71 64
Gender n (%) 0.12
Male 33 (46.48) 39 (60.94)
Female 38 (53.52) 25 (30.06)
Age; min-max (mean) 2-82 (64.78) 56-90 (73.28) <0.01
Laterality n (%) 0.23
Right 26 (36.62) 30 (46.88)
Left 45 (63.38) 34 (53.12)
BCVA; mean logMAR 0.23 0.36 0.09
Abbreviations: PCV, polypoidal choroidal vasculopathy; n-AMD, neovascular age related macular degeneration; BCVA, best corrected
visual acuity; logMAR, logarithm of the Minimum Angle of Resolution.
TABLE 2. Abnormal ndings in multimodal imaging.
PCV n (%) n-AMD n (%) P-value
Total 71 eyes Total 64 eyes
Abnormal ndings in FAF 26 (36.6) 33 (51.6) 0.081
Ring pattern 8 (11.3) 12 (18.8)
Patch pattern 18 (25.4) 21 (32.8)
Abnormal ndings in SD-OCT 25 (35.2) 36 (56.3) 0.014
Steep and/or notched PED 17 (23.9) 30 (46.9)
Hyporeective lumen within PED 1 (1.4) 0
Double-layer sign 8 (11.3) 7 (10.9)
Abnormal ndings in ICGA
Punctate hyperuorescence spots 47 (66.2) 34 (53.1) 0.122
Abbreviations: PCV, polypoidal choroidal vasculopathy; n-AMD, neovascular age related macular degeneration; FAF, fundus autouorescence;
SD-OCT, spectral domain optical coherence tomography; PED, pigment epithelium detachment; ICGA, indocyanine green angiography.
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ranged from about 6% to 11% in n-AMD and 12% in
PCV.
11-15
is indicated that the unaected fellow eyes of
patients are the eyes at risk. Multimodal investigations
are useful for early detection of diseases in asymptomatic
fellow eyes and understanding disease pathogeneses.
Photoreceptor phagocytosis is a major function of
RPE cells. When the RPE phagocytoses the photoreceptor
outer segments, lipofuscin accumulates as an oxidative
byproduct within the RPE cells. Lipofuscin contains the
pigment A2E, which causes autouorescence. Abnormalities
of the RPE cells are accompanied by loss of A2E and lead
to hypoautouorescence.
16
In conditions in which the
RPE has an incomplete phagocytosis process, excessive
build-up of lipofuscin material and hyperautouorescence
in FAF can result.
10
Dysfunction of the RPE can present
with either hypo or hyperautouorescence depending on
the disease stage. erefore, FAF can indirectly represent
the physiology of the RPE.
e pathogenesis of AMD begins with dysfunction in
the RPE cells and leads to accumulation of both intracellular
and extracellular material. Structural changes in the
basement membrane of the RPE and lipid deposition in
the inner aspect of Bruch’s membrane have been reported
in histologic studies of AMD.
1,2
Impaired permeability
of nutrients and water in Bruch’s membrane causes
metabolic stress in the RPE cells and leads to consequent
cellular atrophy or neovascular formation.
17
While the
pathogenesis of PCV originates from the deep choroidal
vessels, dilatation of the choroidal vessels in Haller’s
layer results in focal or diuse attenuation of the inner
choroidal vessel and choriocapillaris, which ultimately
can aect the overlying RPE.
18-20
erefore, in early-stage
PCV, patients can present with unremarkable fundi if
the RPE is not yet involved.
e current study showed FAF abnormalities in
fewer fellow eyes of those with PCV than in the fellow
eyes of those with n-AMD (36% vs. 51%, respectively).
Moreover, the abnormalities seen on the SD-OCT images
of the fellow eyes of those with PCV also were seen less
oen than in PVC (35% vs. 56%, respectively). Our
explanation is that the pathogenesis of PCV originates in
the choroid and FAF and SD-OCT can detect abnormalities
only when the RPE is involved, not in the very early
stage of PCV in which the RPE is still intact. While the
pathogenesis of AMD begins in the RPE cells in which
FAF can detect physiologic dysfunction and SD-OCT
can visualize structural changes even in early stage,
the current ndings conrmed that the pathogeneses
of AMD and PCV are distinct in origin. Furthermore,
both FAF and SD-OCT can detect early abnormalities
even in asymptomatic eyes.
SD-OCT can detect the structural changes in the
RPE in many patterns and some of them are specic to
PCV such as a steep PED, notched PED, double-layer
sign, and hyporeective lumen inside PEDs.
10
However,
in the current study, all of the aforementioned patterns,
except for the hyporeective lumen inside the PEDs, also
were detected in the fellow eyes of those with n-AMD.
erefore, a steep PED, notched PED, and double-layer
sign may not be specic OCT ndings of PCV.
In our study, fellow eyes with abnormalities in
both OCT and FAF were found signicantly higher in
n-AMD which conrmed the pathogenesis of AMD
originates from RPE dysfunction as mentioned earlier.
While other combinations of imaging did not show
signicant correlation with PCV or n-AMD. Yamagishi
and colleagues
23
described abnormal FAF in PCV as
conuent hypoautouorescence represented by well-
PCV n (%) n-AMD n (%) P-value
Total 71 eyes Total 64 eyes
SD-OCT and FAF 6 (8.5) 15 (23.4) 0.008
SD-OCT and ICGA 8 (11.3) 3 (4.7) 0.149
FAF and ICGA 1 (1.4) 2 (3.1) 0.501
SD-OCT, FAF and ICGA 9 (12.7) 13 (20.3) 0.232
TABLE 3. Abnormal ndings in combined modalities.
Abbreviations: PCV, polypoidal choroidal vasculopathy; n-AMD, neovascular age related macular degeneration; FAF, fundus autouorescence;
SD-OCT, optical coherence tomography; ICGA, indocyanine green angiography.
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demarcated hypoautofluorescence surrounded by
hyperautouorescence, which we refer to as the ring
pattern in the current study. is nding was associated
with the polypoidal lesions seen on ICGA images. is
characteristic was observed in most eyes with PCV and
not in typical n-AMD. ose authors proposed that
the anterior protrusion of polyp lesions may induce
RPE damage.
21
However, in the current study, a ring
pattern also was seen in 18% of the fellow eyes of those
with n-AMD. erefore, this nding in FAF may not be
specic to PCV. Any pathology that involves the RPE
and causes RPE damage can demonstrate a ring pattern
as well, while a patch pattern, represented by hypo/
hyperautouorescence, is a nonspecic FAF nding that
may represent changes in RPE function in early-stage
diseases of the RPE cells and adjacent structures.
ICGA is an invasive investigation. Because of its
longer operating wavelength, ICG can uorescence through
the RPE better than uorescein dye. ICGA is useful for
detecting abnormal choroidal vasculature. e specic
characteristics of ICGA in PCV were reported and used
as diagnostic criteria.
7
However, a non-specic nding
in ICGA, such as PHS, has been described previously in
choroidal vasculopathy disorders. ose punctate spots
were believed to be in the inner choroid and possibly
the RPE layer and were found to be associated with
the hyperpermeability of the choroidal vessels causing
dye leakage in the late phase.
22,23
Park and colleagues
26
reported a higher incidence of PHS in PCV than n-AMD
in aected and contralateral eyes. ose authors suggested
that PCV may arise from choroidopathy and be distinct
from typical n-AMD.
24
In the current study, PHS was
detected in the fellow eyes of those with PCV and n-AMD
and the dierence did not reach signicance (66% in
PCV vs. 53% in n-AMD). Because the punctate spots
can be present in either the inner choroid or RPE, this
nonspecic nding may be associated with both PCV
and AMD. erefore, PHS may not be a nding specic
to PCV, in that it can be detected in AMD as well.
In the current study, compared to FAF and SD-
OCT, ICGA detected the most abnormalities in the fellow
eyes of those with PCV. About two-thirds of the fellow
eyes of those with PCV had abnormalities on ICGA
images compared with only one-third of patients with
abnormalities on FAF or SD-OCT images. is result may
suggest that patients who have normal ndings on FAF
or SD-OCT still have a risk of developing PCV in their
fellow eyes and those eyes should be monitored regularly.
Although ICGA seems to be the best investigation for
detecting choroidal pathologies, especially in early or
even preclinical disease stages, ICGA is not likely to be
performed during routine screenings because it is invasive
and complex. FAF and SD-OCT are noninvasive and
reproducible investigations, so they are more likely to
be used for screening PCV in asymptomatic eyes, even
though their abilities to detect abnormalities are lower
than that of ICGA.
The current study had several limitations. The
retrospective cross-sectional design may cause a systematic
bias toward population selection. e small sample size
and lack of follow-up also were drawbacks. Finally, the
evaluation of all images was lacking in quantitative
analysis results in subjective information.
In conclusion, most asymptomatic fellow eyes
of those with PCV and n-AMD, which are the better
eyes of patients, showed abnormalities in all current
investigations and may represent the eyes at risk. Patients
and physicians should be more concerned about the
status of these eyes. e correlation between abnormal
ndings in each imaging modality may contribute to
important information that can predict possible disease
progression. Additional longitudinal long-term studies
may facilitate a better understanding of the pathogeneses
and course of these diseases.
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