Ophthalmic Surgery, Lasers and Imaging Retina

Clinical Science 

Quantitative Evaluation of the Retinal Vascular Parameters With OCTA in Patients With Behçet Disease Without Ocular Involvement

Mehmet Fatih Kağan Değirmenci, MD; Emine Temel, MD; F. Nilüfer Yalçındağ, MD

Abstract

BACKGROUND AND OBJECTIVE:

To evaluate the optical coherence tomography angiography (OCTA) features of patients with Behçet disease (BD) without ocular involvement.

PATIENTS AND METHODS:

Twenty-three patients with BD without ocular involvement and 29 healthy age/sex-matched control subjects were involved. The authors measured foveal avascular zone (FAZ) area, vessel density in the parafoveal region, and flow area (fovea-centered 3-mm radius area) in the superficial and deep capillary plexuses evaluated by OCTA.

RESULTS:

FAZ area was significantly larger in eyes with BD in both the superficial and deep capillary plexuses (0.331 vs. 0.240 mm2 [P = .004] and 0.352 vs. 0.257 mm2 [P = .003], respectively). Although mean capillary vessel density in parafoveal region and mean flow area were lower in eyes with BD for both superficial and deep capillary plexuses, these findings were not statistically significant.

CONCLUSION:

Microvascular changes in macular region can be identified in patients with BD without ocular manifestation.

[Ophthalmic Surg Lasers Imaging Retina. 2020;51:31–34.]

Abstract

BACKGROUND AND OBJECTIVE:

To evaluate the optical coherence tomography angiography (OCTA) features of patients with Behçet disease (BD) without ocular involvement.

PATIENTS AND METHODS:

Twenty-three patients with BD without ocular involvement and 29 healthy age/sex-matched control subjects were involved. The authors measured foveal avascular zone (FAZ) area, vessel density in the parafoveal region, and flow area (fovea-centered 3-mm radius area) in the superficial and deep capillary plexuses evaluated by OCTA.

RESULTS:

FAZ area was significantly larger in eyes with BD in both the superficial and deep capillary plexuses (0.331 vs. 0.240 mm2 [P = .004] and 0.352 vs. 0.257 mm2 [P = .003], respectively). Although mean capillary vessel density in parafoveal region and mean flow area were lower in eyes with BD for both superficial and deep capillary plexuses, these findings were not statistically significant.

CONCLUSION:

Microvascular changes in macular region can be identified in patients with BD without ocular manifestation.

[Ophthalmic Surg Lasers Imaging Retina. 2020;51:31–34.]

Introduction

Behçet disease (BD) is a multisystem inflammatory disorder characterized by vasculitis. Ocular involvement occurs in more than 50% of the patients with BD, and it is characterized by unilateral or bilateral iridocyclitis, hypopyon or panuveitis with a chronic, and relapsing course.1 Recently, a national registry report from Turkey reported that BD was the leading cause of uveitis among the noninfectious cases.2

There were previous studies related to orbital Doppler ultrasound findings in BD with or without ocular involvement. In the studies, the authors reported decrease in ocular blood flow values in non-ocular BD patients.3–6 Optical coherence tomography angiography (OCTA) is a relatively new tool that provides depth-resolved scanning of the retinal and choroidal microvasculature.7 OCTA helps us to evaluate features of the retinal and choroidal vessels quantitatively in diseases such as age-related macular degeneration,8 polypoidal choroidal vasculopathy,9 diabetic maculopathy,10 retinal vein occlusion,11 and macular telangiectasia.12

The purpose of this study is to determine whether there are microvascular changes in the macular region of patients with BD without ocular involvement. Therefore, we investigated the OCTA findings of patients with BD without ocular involvement and compared the findings with those of healthy volunteers.

Patients and Methods

This research was approved by the institutional ethics committee and conducted in accordance with the tenets of the Declaration of Helsinki. A total of 23 patients with BD without ocular involvement and 29 healthy age- and sex-matched control subjects were involved in the study. BD was diagnosed based on the diagnostic criteria of the International Study Group for BD.13 All participants underwent detailed ophthalmic examination, including measurement of best-corrected visual acuity (BCVA), slit-lamp examination, tonometry, and dilated fundus examination. Spectral-domain optical coherence tomography (SD-OCT) and OCTA (RTVue XR Avanti; Optovue, Fremont, CA) imaging was performed on all participants. Central macular thickness (CMT) and central choroidal thickness (CCT) were analyzed by SD-OCT images. OCTA software was used to evaluate retinal tissue layer by layer. We measured the foveal avascular zone (FAZ) area and the mean capillary vessel density in the parafoveal region automatically (Figure 1). The flow area value was measured as the detected flow signals within the fovea-centered 3-mm radius area (Figure 2). The quantitative parameters were assessed separately for both superficial and deep capillary plexuses (SCP, DCP). All parameters were compared between patients with BD without ocular involvement and the healthy control group. Two eyes of two patients with BD without ocular involvement and nine eyes of nine control subjects were not included due to poor-quality OCT angiograms. Patients with other forms of ocular pathology, systemic hypertension, and diabetes mellitus were excluded from the study.

Optical coherence tomography angiography measurements of a patient with Behçet disease in the superficial capillary plexus level. Foveal avascular zone area (A) and capillary vessel density in the parafoveal region (B, C).

Figure 1.

Optical coherence tomography angiography measurements of a patient with Behçet disease in the superficial capillary plexus level. Foveal avascular zone area (A) and capillary vessel density in the parafoveal region (B, C).

Same patient's (above) flow area measurement in the superficial capillary plexus by optical coherence tomography angiography.

Figure 2.

Same patient's (above) flow area measurement in the superficial capillary plexus by optical coherence tomography angiography.

Statistical analyses were performed using SPSS version 20.0 for Windows (IBM, Armonk, NY). The normality of the data was tested by Kolmogorov-Smirnov test. Independent t-test and Mann-Whitney U test were used to compare quantitative data of the two groups. Statistical significance was set at a P value of less than .05.

Results

The patient cohort comprised 44 eyes of 23 patients with BD without ocular involvement (mean age: 45.7 years ± 5.3 years; 49.5% female) and 49 eyes of 29 healthy control subjects (mean age: 51.4 years ± 7.1 years; 46.7% female). There was no significant difference in BCVA and intraocular pressure (IOP) between the two groups. CMT and CCT measurements by SD-OCT images were also similar between the two groups. The mean BCVA, IOP, CMT, and CCT measurements of the groups are summarized in Table 1.

Baseline Characteristics of the Patients With Non-Ocular Behçet Diseaseand Healthy Subjects

Table 1:

Baseline Characteristics of the Patients With Non-Ocular Behçet Diseaseand Healthy Subjects

The OCTA findings and statistical significances are summarized in Table 2. The mean FAZ area was significantly larger in patients with BD than in the healthy control group in both the SCP and DCP (0.331 mm2 vs. 0.240 mm2 [P = .004] and 0.352 mm2 vs. 0.257 mm2 [P = .003], respectively). The mean capillary vessel density in the parafoveal region was similar in the two groups for both the SCP and DCP. Although the mean flow area was lower in patients with BD than in the healthy control group in the SCP and DCP, the difference was not statistically significant (13.29 mm2 vs. 13.43 mm2 [P = .242] and 14.46 mm2 vs. 14.58 mm2 [P = .278], respectively).

Comparisons of the Optical Coherence Tomography Angiography FindingsBetween the Two Groups

Table 2:

Comparisons of the Optical Coherence Tomography Angiography FindingsBetween the Two Groups

Discussion

It is known that the basic pathology of BD is occlusive vasculitis, which is caused by the circulation of abnormal immunocomplexes and endothelial cell proliferation.14,15 OCTA allows us to evaluate retinal microvascular parameters, including vessel density and flow area, without using any dye.16 The advantage of OCTA is to measure the FAZ and evaluate inner retinal circulation (SCP and DCP) quantitatively. In two prior studies that investigated retinal microvascular structural changes in patients with ocular BD using OCTA, the authors found decreased capillary density in patients with ocular BD compared to healthy controls.17,18 Unlike our study, Khairallah et al.18 found that the area of FAZ was not significantly larger in patients with active Behçet uveitis in comparison to healthy subjects. However, they excluded six eyes in the measurement of FAZ because the FAZ area was not measurable due to extensive disruption of the perifoveal anastomotic capillary arcade with poorly defined borders. If these patients had not been excluded, the results could have been like those found in the present study. In the literature, there are few recent studies about OCTA findings in non-ocular BD. Rafaat et al. found significant difference in average capillary density between non-ocular Behçet patients and a healthy control group.19 Further, there was no significant difference in the mean of FAZ area in two groups.19 In another study, the FAZ area in the SCP was significantly higher, and vessel densities of the foveal region in the SCP and DCP were significantly lower in the BD group.20 In our study, the FAZ areas in both the SCP and DCP were significantly larger in Behçet patients without ocular involvement. Similarly, capillary density measurements in the SCP and DCP were lower in our patients with BD, although the results were not statistically significant. The different results may be related to the different number of patients between the studies and the duration of BD, which was neither assessed in our study nor in the previous two studies. We consider that the inclusion of both eyes of the patients in the previous two studies was a limitation that could cause a selection bias.

In conclusion, the retinal microvasculature appears to be affected in eyes of patients with BD without clinical ophthalmologic involvement. In this study, we found that the FAZ area was larger in patients with BD without ocular involvement. Further longitudinal studies are needed to clarify that the microvascular changes might be an early sign of future ocular involvement.

References

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Baseline Characteristics of the Patients With Non-Ocular Behçet Diseaseand Healthy Subjects

Study GroupControl GroupSignificance (P Value)
BCVA (logMAR)−0.10 ± 0.02−0.12 ± 0.01.892*
IOP (mm Hg)18.1 ± 2.319.3 ± 1.9.756*
CMT (μm)255.4 ± 14.1242.9 ± 11.5.211*
CCT (μm)267.2 ± 23.2249.1 ± 19.4.156*

Comparisons of the Optical Coherence Tomography Angiography FindingsBetween the Two Groups

Study GroupControl GroupSignificance (P Value)

FAZ Area (mm2)SCP0.331 ± 0.1210.24 ± 0.072.004*
DCP0.352 ± 0.1260.257 ± 0.07.003*

Vascular Density (%)SCP54.5 (50.1–68.7)55.6 (48.7–60.8).602
DCP63.9 (60.8–68.7)64.1 (58–68.5).992

Flow Area (mm2)SCP13.29 (11.5–14.6)13.43 (11.9–14.9).242
DCP14.46 (11.4–15.8)14.58 (12.6–16.2).278
Authors

From Ankara University Faculty of Medicine Department of Ophthalmology, Ankara, Turkey.

The authors report no relevant financial disclosures.

Address correspondence to Mehmet Fatih Kağan Değirmenci, MD, Ankara University Faculty of Medicine Department of Ophthalmology, Vehbi Koç Eye Hospital, Mamak Street, Dikimevi, Ankara, Turkey; email: mfkdegirmenci@ankara.edu.tr.

Received: January 21, 2019
Accepted: July 29, 2019

10.3928/23258160-20191211-04

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