Original Article

Evaluation and Comparison of Choroidal Thickness in
Patients with Behçet Disease with versus without

Ocular Involvement
Seyedeh Maryam Hosseini, MD; Negar Morrovatdar, MD; Armin Hemati, MD; Mozghan Dolatkhah, MD

Elham Bakhtiari, MD; Zahra Mirfeizi, MD; Mahdieh Azimizadeh, MD

Department of Ophthalmology, Mashhad University of Medical Sciences, Mashhad, Iran

ORCID:
Seyedeh Maryam Hosseini: https://orcid.org/0000-0002-4233-9243

Mahdieh Azimizadeh: https://orcid.org/0000-0001-9467-4249

Abstract

Purpose: To assess the subfoveal choroidal thickness (SFCT) in patients with Behçet
disease (BD) and compare the SFCT in patients with and without ocular BD (OBD) and
between patients with active and quiescent phases of the Behçet’s posterior uveitis.
Method: This prospective cross-sectional study was conducted on patients with BD (n =
51) between October 2016 and October 2018. Complete ocular examinations including
slit lamp biomicroscopy and fundus examination with dilated pupils were performed
for all patients. The SFCT values were compared between patients with and without
OBD. Enhanced depth imaging optical coherence tomography (EDI–OCT) was done
to measure the SFCT, and wide field fundus fluorescein angiography (WF-FAG) was
performed to evaluate the ocular involvement and determine the active or quiescent
phases of the Behçet’s posterior uveitis. The correlation between the changes of SFCT
and the WF-FAG scores was assessed.
Results: One hundred and two eyes of 51 patients with BD, aged 29 to 52 years were
studied. Of these, 23 patients were male. The mean age ± standard deviation in patients
with OBD and patients without ocular involvement was 38.71 ± 7.8 and 36.22 ± 10.59
years (P = 0.259) respectively. The mean SFCT in patients with OBD was significantly
greater than in patients without OBD (364.17 ± 93.34 vs 320.43 ± 56.70 µm; P = 0.008).
The difference of mean SFCT between the active compared to quiescent phase was not
statistically significant when only WF-FAG criteria were considered for activity (368.12
± 104.591 vs 354.57 ± 58.701 µm, P = 0.579). However, when the disease activity was
considered based on both WF-FAG and ocular exam findings, SFCT in the active group
was higher than the inactive group (393.04 ± 94.88 vs 351.65 ± 58.63 µm, P = 0.060).
This difference did not reach statistical significance, but it was clinically relevant.
Conclusion: Choroidal thickness was significantly increased in BD patients with ocular
involvement; therefore, EDI-OCT could be a noninvasive test for evaluation of ocular
involvement in patients with BD. The increased SFCT was not an indicative of activity
in OBD; however, it could predict possible ocular involvement throughout the disease
course.

Keywords: Behçet’s Disease; Behçet’s Uveitis; Choroidal Thickness; Enhanced Depth Imaging
Optical Coherence Tomography (EDI-OCT); Ocular Behçet; Wide Field Fluorescein Angiography

J Ophthalmic Vis Res 2021; 16 (2): 195–201

© 2021 HOSSEINI ET AL. THIS IS AN OPEN ACCESS ARTICLE DISTRIBUTED UNDER THE CREATIVE COMMONS ATTRIBUTION LICENSE | PUBLISHED BY

KNOWLEDGE E 195

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Choroidal Thickness in Patients with Behçet Disease; Hosseini et al

INTRODUCTION

Behçet disease (BD) is a chronic, recurrent,
inflammatory, multisystem disease characterized
by occlusive and necrotizing vasculitis.[1–3] The
prevalence of BD is estimated to be 10.3 per
100,000 individuals and is higher in Middle
East, Far East, and Mediterranean countries.[4, 5]
Different classification criteria exist for BD,
including the new “international criteria for BD.”
Ocular involvement is a common consequence
of BD as 70–90% of the patients experience
ocular impairments that are presented in different
forms including posterior uveitis, retinal vasculitis,
anterior uveitis, and optic neuropathy.[6] Loss
of vision has been correlated with the disease
duration.[5] In 50–93% of the patients with ocular
involvement, the posterior segment eye diseases
are observed.[7] Choroidal vessels can be involved
in addition to retinal vessels as the primary
focus or secondary to retinal inflammation.[8]
Recurrent inflammatory phases can severely
impair the retinal structure and function and result
in visual loss.[9–13] Early detection of posterior
segment involvement during the early phase of
the disease is necessary for development of an
effective treatment strategy.[9] Fundus fluorescein
angiography (FFA) is the standard method for
monitoring and evaluating the progression of
ocular Behçet disease (OBD).[10, 11, 13] This imaging
modality has shown high sensitivity for detection
of retinal vasculitis in BD cases.[10] Indocyanine
green angiography (ICGA) has been proposed as
an alternative modality which evaluates choroidal
circulation; however, it does not disclose the
retinal circulation or evidence of retinal vasculitis
as clear as FFA does.[14–16] Several studies have
investigated the choroidal thickness analysis
with EDI-OCT in patients with OBD.[6, 8, 14, 17, 18]
Their findings are controversial regarding the
effects of OBD disease on choroidal thickness.

Correspondence to:

Mahdieh Azimizadeh, MD. Eye Research Center,
Khatam-Al-Anbia Eye Hospital, Abutalib Junction,
Kolahdouz Blvd., Mashhad, Iran
E-mail: azimi57@gmail.com
Received: 15-06-2019 Accepted: 09-01-2021

Access this article online

Website: https://knepublishing.com/index.php/JOVR

DOI: 10.18502/jovr.v16i2.9083

While some studies have reported that choroid
thickness increases in OBD patients,[6, 8, 17, 18]
others have demonstrated that OBD decreases
the choroidal thickness.[14] These discrepancies
in choroidal thickness could be attributed to the
non-homogeneity in patients’ features in terms
of activity, anatomical involvement, and OBD
duration.[8]

In this study, we tried to investigate the subfoveal
choroidal thickness (SFCT) in Behçet’s patients with
and without ocular involvement using EDI-OCT
modality. We also compared SFCT between active
and quiescent phases of OBD and evaluated the
correlations between the changes of SFCT in EDI-
OCT and the WF-FAG scores.

METHODS

This prospective cross-sectional study was
conducted on patients with BD (n = 51; eyes:
102) who had been referred to the uveitis clinic of
Khatam-Al-Anbia tertiary eye center, affiliated to
Mashhad University of Medical Sciences (MUMS)
between October 2016 and October 2018. The
study was approved by the local institutional review
board and ethics committee of MUMS, Mashhad,
Iran, and was in accordance with the ethical
standards and regulations of the Declaration of
Helsinki.

The inclusion criteria of the study were patients
older than 18 years with definite diagnosis of
BD according to the diagnostic criteria of the
International Study Group for BD with or without
ocular involvement. Patients who met the inclusion
criteria were evaluated in three groups:

(i) Patients with ocular involvement and active
uveitis

(ii) Patients with ocular involvement who were in
remission

(iii) Patients without ocular involvement in
examination or WF-FAG

Behçet’s patients with posterior, intermediate,
or pan-uveitis were included in the study. Evidence

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How to cite this article: Hosseini SM, Morrovatdar N, Hemati A, Dolatkhah
M, Bakhtiari E, Mirfeizi Z, Azimizadeh M. Evaluation and Comparison of
Choroidal Thickness in Patients with Behçet Disease with versus without
Ocular Involvement. J Ophthalmic Vis Res 2021;16:195–201.

196 JOURNAL OF OPHTHALMIC AND VISION RESEARCH VOLUME 16, ISSUE 2, APRIL-JUNE 2021

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Choroidal Thickness in Patients with Behçet Disease; Hosseini et al

of posterior uveitis was documented either on
examination by the presence of inflammatory
cells in the vitreous and/or retinitis, or retinal
vasculitis manifesting as perivascular sheathing, or
vascular leakage and/or occlusion on fluorescein
angiograms.

The exclusion criteria were age over 55 years,
history of intraocular surgery, chronic systemic
diseases such as diabetes mellitus, hypertension,
vascular diseases and other rheumatologic
involvement, any ocular diseases like age-
related macular degeneration (AMD), central
serous choroidopathy (CSC), high refractive error
(spherical equivalent >±3.00D), any media opacity
precluding image acquisition, allergy to fluorescein
and non-compliance with follow-up. Patients with
only anterior uveitis were excluded.

Demographic information of the patients
and the ophthalmologic examinations data
including best-corrected visual acuity (BCVA),
slit lamp biomicroscopy, tonometry, and dilated
indirect ophthalmoscopy were collected for further
analysis. BCVA was measured by decimal Snellen
scale and then converted to the logarithm of the
minimal angle of resolution (log MAR) for statistical
analysis. All patients underwent EDI-OCT and
WF-FAG imaging modalities.

The SFCT was measured using digital caliper
provided by EDI-OCT (Heidelberg Engineering,
Heidelberg, Germany). Choroidal thickness was
measured from the outer portion of the hyper-
reflective line corresponding to the retina pigment
epithelium (RPE) to the inner surface of the sclera.
To avoid diurnal variations, measurements of SFCT
with EDI-OCT were performed from 9 am to 1 pm. To
reduce the bias, two expert ophthalmologists who
were masked to the patient grouping measured
the choroidal thickness independently in each
eye. Any case with 15% difference in the two
measurements by the two experts was excluded
from the study. All patients underwent WF-FAG
(Heidelberg Engineering, Heidelberg, Germany)
procedure following intravenous (IV) administration
of 2.5 mL sodium fluorescein 10% (Fluorescite;
Alcon, Inc, Fort Worth, TX). The angiographic
scoring method described by Tugal-Tutkun et al[19]
was used to score the FA. In this scoring method,
they assigned scores to the fluorescein and
ICG angiographic signs that represented active
inflammatory process in the posterior segment. A
total maximum score of 40 was assigned to the
FA signs, including optic disc hyperfluorescence,

macular edema, retinal vascular staining and/or
leakage, capillary leakage, retinal capillary
nonperfusion, neovascularization of the optic
disc, neovascularization elsewhere, pinpoint leaks,
and retinal staining and/or subretinal pooling.
A total maximum score of 20 was assigned to
the ICGA signs, including early stromal vessel
hyperfluorescence, choroidal vasculitis, dark
dots or areas (excluding atrophy), and optic disc
hyperfluorescence.

RESULTS

Table 1 shows demographic information, age,
gender, BCVA, and SFCT in the studied patients.
There was no significant difference in terms of
gender and age between the groups with and
without ocular involvement.

Fifty-one patients (102 eyes) participated in this
study (23 males and 28 females). Twenty-eight
eyes showed no ocular involvement. Seventy-
four eyes had ocular involvement in WF-FAG or
clinical examination; of these, twenty-eight eyes
(37.8% ) demonstrated active ocular inflammation
manifesting as posterior uveitis in ophthalmic
examination, whereas the uveitis was quiescent
in 46 eyes corresponding with 62.2% of patients
with ocular involvement. However, in the WF-FAG
evaluation, 53 eyes (71.6% of patients with OBD)
had active uveitis (score >0) and 21 eyes (28.4%)
showed inactive uveitis (score of 0) (WF-FAG score
range, 1–29). In evaluation of both ophthalmic
examination and WF-FAG in patients with ocular
involvement, 26 eyes (36.5%) showed to be active
and 20 eyes (27%) were inactive.

The mean age of patients in the group without
ocular involvement was 38.71 ± 7.8 years (29–52
years) and in the group with ocular involvement was
36.22 ± 10.59 (21–55 years) (P = 0.259). The mean
duration of BD was 5.34 ± 4.6 years in all patients.
The minimum duration of disease was in new cases
and the maximum duration was 22 years.

The mean BCVA (Log MAR) in the BD patients
with and without ocular involvement was 0.1403 ±
0.24 and 0.0035 ± 0.018 (P = 0.005), respectively.

There was no eye with >15% variation
in measurement of SFCT between the
ophthalmologists. The mean SFCT in patients
without ocular involvement measured on EDI-
OCT was 320.43 ± 56.70 µm (222–452 µm) and
in patients with ocular involvement on clinical

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Choroidal Thickness in Patients with Behçet Disease; Hosseini et al

Table 1. Demographic and clinical finding of patients

Without ocular involvement With ocular involvement P-value

Age 38.71 ± 7.8 (29–52 years) 36.22 ± 10.59 (21–55 years) 0.259
Sex (M:F) 5:9 16:19 0.241

BCVA 0.1403 ± 0.24 0.0035 ± 0.018 0.005
Mean SFCT (μm) 320.43 ± 567 364.17 ± 93.34 0.008

BCVA, best-corrected visual acuity (logMAR); SFCT, sub-foveal choroidal thickness

Table 2. Demographic and clinical finding of patients with ocular involvement only in WF-FAG

Active uveitis Inactive uveitis P-value

AGE 35.60 ± 10.906 37.76 ± 9.833 0.433
Sex (M:F) 33:20 3:18 0.001

BCVA 0.2002 ± 0.28 0.0120 ± 0.038 0.003
Duration of disease (yr) 5.018 ± 6.28 5.119 ± 3.65 0.945
5Mean SFCT (μm) 368.12 ± 104.591 354.57 ± 58.701 0.579

WF-FAG, wide field fundus fluorescein angiography; BCVA, best corrected visual acuity; SFCT, subfoveal choroidal thickness

examination or WF-FAG was 364 ± 93.34 µm
(88–519µm) (P = 0.008). The Mann–Whitney
test showed significant correlations (P = 0.008)
between SFCT and ocular involvement (Table 1).

The SFCT measured by EDI-OCT in the patients
with active OBD demonstrating only in WF-FAG
was 368.12 ± 16.64 µm (range: 88–519 µm), and in
inactive eyes it was 354.57 ± 58.701 (range, 222–
452 µm) (P = 0.579) (Table 2). The SFCT values
did not show significant correlation with WF-FAG
activity (P = 0.579). SFCT values in the active group
according to both WF-FAG and clinical examination
was higher than in the inactive group but it was
not statistically significant regardless of the clinical
relevance (393.04 ± 94.88 vs 351.65 ± 58.63) P =
0.060 (Table 3).

Spearman correlation test showed significant
negative correlation between SFCT and BD
duration (P = 0.013, r = –0.249) indicating inverse
relationship between BD duration and SFCT.

The mean ± SD WF-FAG score of active uveitis
cases was 18 ± 7. There was an association
between total WF-FAG score and mean SFCT
in EDI-OCT so that higher total WF-FAG scores
resulted in higher mean SFCT values, but the
association was not statistically significant (P =
0.579).

In addition, we evaluated the association
between BCVA and gender in the patients. The

mean Log MAR BCVA was 0.153 and 0.057 in males
and females, respectively. BCVA was significantly
better in females and the Mann–Whitney test
showed significant correlations between BCVA
and gender (P = 0.002).

DISCUSSION

In the current study, patients with OBD had
thicker choroid compared to patients without
ocular involvement, and the subfoveal choroid was
thicker in patients with active disease compared
to those with quiescent disease. To the best of
our knowledge, this is the first report of choroidal
thickness measurement in BD with and without
ocular involvement in Iran.

Choroidal involvement in OBD has been
demonstrated in histopathology, ophthalmic
ultrasonography, ICGA, and WF-FAG.[20–22]

EDI–OCT is a technique that provides
noninvasive, in vivo, cross-sectional, histologic
information of the choroid and retina with high
resolution.[12, 16]

WF-FAG is the gold standard technique for
evaluation of posterior involvement in OBD.
However, this technique is poorly sensitive for
detailed evaluation of the choroidal circulation.[14]
ICGA has been proposed for the assessment of

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Choroidal Thickness in Patients with Behçet Disease; Hosseini et al

Table 3. Demographic and clinical finding of patients with ocular involvement in both WF-FAG and clinical exam

Active uveitis Inactive uveitis P-value

Number (eyes) 26 20

AGE 36.56 ± 8.85 36.34 ± 9.573 0.385
SEX (M:F) 12:14 8:12 0.259

BCVA 0.2210 ± 0.14 0.0095 ± 0.056 0.03
Mean SFCT (μm) 393.04 ± 94.88 351.65 ± 58.63 0.060

BCVA, best corrected visual acuity; SFCT, subfoveal choroidal thickness

choroidal circulation, but it shows low sensitivity
for the evaluation of retinal circulation.[15, 16]

We investigated mean SFCT with EDI–OCT in
102 eyes of 51 patients with definite BD and found
that choroid was thicker in patients with ocular
involvement in both active and inactive uveitic
phases compared to the choroidal thickness in
patients without ocular involvement. SFCT was also
greater during an active uveitis in comparison to
the cases in remission, but the difference was
not statistically significant. This can be explained
by either the possible subclinical involvement of
the choroid in quiescent phase that results in an
increase in the SFCT or that attacks of uveitis may
cause lasting changes in the choroidal structure
and thickness. The mean age of patients with and
without ocular involvement did not significantly
differ and the age of patients in this study
was similar to the age of patients in previously
conducted studies that were in their third and fourth
decades of life.[23]

Previous studies evaluated choroidal changes
by EDI–OCT in BD. Ishikawa et al[17] and Kim
et al[6, 9] reported that SFCT in the active phase
of OBD was significantly greater than in remission
phase. Moreover, the choroidal thickness in both
active and remission phases of OBD was greater
than the healthy subjects. This difference could be
attributed to the subclinical inflammatory activity
of the choroid during the quiescent phase, which
could exacerbate, leading to an acute recurrent
attack of uveitis.[6] Their findings correlate with the
findings of the current study. Results of the study
by Atas et al also support our findings[18]. They
reported that the SFCT in the eyes in the remission
phase of OBD was greater than the healthy
control eyes, but the difference was not statistically
significant. In contrast, some studies contradicted
our findings.[8] Coskun et al[14] demonstrated that

the choroid was significantly thinner in the eyes
of Behçet patients with active posterior uveitis
compared to patients in remission and control
healthy individuals after excluding patients with
macular edema. They concluded that because of
long duration of eye disease in the studied patients
(4.1 years), prolonged inflammation resulted in
choroidal fibrosis and shrinkage and decreased
thickness.[14]

Onal et al analyzed the morphology of subfoveal
choroid during an active OBD phase.[8] They
quantitatively segmented the choroid into
choroidal stroma and choroidal vessel lumen
in EDI–OCT images collected from patients
with <4 year history of BD and acute posterior
uveitis. Patients with OBD had a significantly
higher choroidal stroma to choroidal vessel
lumen compared to the healthy control group.
Choroidal stromal expansion in eyes with active
OBD was observed. However, choroidal stroma
expansion was not associated with thickening of
the choroid.[8]

Interestingly, Kim et al reported no significant
difference in SFCT between the two eyes of BD
patients with unilateral active uveitis because the
choroid thickness was greater than the normal
values in the uninvolved fellow eyes.[6]

The discrepancies in choroidal thickness in
these studies could be attributed to the non-
homogeneity in activity, anatomical involvement,
and duration of OBD.[8]

We used the wide field angiographic scoring
system to score WF-FAG[19, 24–26] and observed an
association between choroidal thickness and WF-
FAG activity score so that higher WF-FAG activity
results in greater SFCT but the association was not
statistically significant. The results of the current
study contradicted the findings of Kim et al[6] and
Onal et al[8] who reported significant correlations

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Choroidal Thickness in Patients with Behçet Disease; Hosseini et al

between SFCT values and total WF-FAG score,
retinal vascular staining, and/or leakage.

The other interesting finding of the present study
was the negative correlation between choroidal
thickness and duration of the disease; the plausible
explanation for this finding may be replacement of
choroidal stroma by fibrosis in the chronic phase
of BD that results in thinning of choroid in cases
with longer duration of OBD in contrast to early
involved patients.[14] In the current study, BCVA
was significantly better in females, which could be
explained by the more severe course and more
frequent involvement of the posterior segment in
male patients with Behcet ocular involvement.[5]

In conclusion, our findings showed a significant
change of SFCT in BD. Moreover, this study
demonstrated that EDI–OCT modality is useful for
evaluating the subclinical choroidal involvement
even during the quiescent phase of the OBD.
This technique can be used to monitor the activity
of disease in association with the angiographic
findings.[6]

This study has some limitations including
small sample size and non-homogeneity of
cases. Although EDI–OCT is a good modality
for assessment of ocular involvement in BD
patients, the commercially available tools can
not automatically calculate the SFCT; manual
measurements are tedious and time-consuming,
and delineating the choroidal–scleral interface
in subjects with a thick choroid is difficult.
Moreover, opaque ocular media due to significant
vitreous haziness and/or cataract impedes smooth
acquisition of the images. Future developments in
SS-OCT may provide more effective assessment
of the choroid in ocular Behcet disease.

Financial Support and Sponsorship

None.

Conflicts of Interest

The authors have no conflicts of interest to declare.

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