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Analysis of Retinal Nonperfusion Area and Ganglion Cell Layer Thickness in Branch Retinal Vein Occlusion by OCT-Angiography

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  • Central Lisbon Hospital Center

Abstract and Figures

Purpose: To analyze the area of retinal nonperfusion in branch retinal vein occlusion (BRVO) and its relation to retinal ganglion cell (RGC) layer thickness. Procedures: Patients with ischemic BRVO, with no signs of fluid, were evaluated by Cirrus HD-OCT-A, Zeiss. Nonperfusion findings and RGC layer thickness were evaluated in a 6x6 mm area centered in fovea. Results: 10 eyes (8 patients) were included (mean age of 75.60±12.57years min 60, max 88). Area of ischemia in deep plexus was superior to superficial plexus (p=0.013). There was a strong correlation between ischemic area of superficial and deep plexus (r=0.915; p<0.001) and an important correlation between ischemic area of superficial plexus and area of reduced RGC layer thickness (r=0.661; p=0.038). Conclusions: In ischemic BRVO, deep capillary plexus reveals a greater area of ischemia than superficial plexus. This study suggests that ischemia may cause the decrease of RGC layer thickness. Keywords: BRVO; Capillary plexus; Ischemia; OCT-A; RGC layer thickness
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Research Article
Volume 6 Issue 4 - APRIL 2018
DOI: 10.19080/JOJO.2018.06.555693
JOJ Ophthal
Copyright © All rights are reserved by Rita Flores
Analysis of Retinal Nonperfusion Area and Ganglion
Cell Layer Thickness in Branch Retinal Vein
Occlusion by OCT-Angiography
Ana L Basílio, Luísa Vieira, Lívio Costa, Rita Proença, Sara Crisóstomo, Joana Cardigos, NunoMoura-Coelho and
Rita Flores*
Centro Hospitalar de Lisboa Central, Portugal
Submission: March 16, 2018; Published: April 16, 2018
*Corresponding author: Rita Flores, Ophthalmology Department, Hospital de Santo António dos Capuchos, Alameda de Santo António dos Capuchos,
1169-050 Lisboa, Portugal, Tel: ; Email:
JOJ Ophthal 6(4) JOJO.MS.ID.555693 (2018) 001
Introduction
Retinal vein occlusion (RVO) is a common and sight-
threatening retinal vascular disorder. Location of the
occlusion, presence of macular edema and the extent of retinal
     
and response to treatment. Branch retinal vein occlusion (BRVO)
is an occlusion of either a major branch retinal vein draining one
quadrant of the retina, a macular branch vein draining a portion
of the macula or a peripheral branch vein draining a portion of
the retinal periphery. [1].
The Optical Coherence Tomography-Angiography (OCT-A) is
a noninvasive diagnostic test that allows a better understanding
          
plexus. The OCT-A device allows the integration of abnormalities
in vascularity and structural changes [2-4].
BRVO microvascular changes have been studied through

networks makes it still poorly understood [2]. According to
the literature, OCT-A shows capillary abnormalities (including
disruption) and grayish areas (areas with reduced capillary

BRVO [5].
The aim of our study was to analyze the area of retinal
nonperfusion in eyes with BRVO without macular edema and
to compare the involvement of both plexus and its relation to
retinal ganglion cell (RGC) layer thickness.
Materials and Methods
The authors conducted a retrospective observational study in
agreement with the Declaration of Helsinki for research involving
humans. Patients with the diagnosis of ischemic BRVO involving
the macular area, without macular edema were included. All
patients had been submitted to a ranibizumab scheme in acute
phase of disease and the last treatment was at least 4 months
earlier. Patients with other ocular or systemic diseases that
        
artifacts were excluded. BRVO was diagnosed based on clinical
      
OCT). These eyes were also evaluated by OCT-A (Cirrus HD-OCT
Angiography, Zeiss). The studied variables were: age, gender,
Abstract
Purpose: To analyze the area of retinal nonperfusion in branch retinal vein occlusion (BRVO) and its relation to retinal ganglion cell (RGC)
layer thickness.
Procedures:
layer thickness were evaluated in a 6x6 mm area centered in fovea.
Results: 10 eyes (8 patients) were included (mean age of 75.60±12.57years min 60, max 88). Area of ischemia in deep plexus was superior


Conclusions:     
ischemia may cause the decrease of RGC layer thickness.
Keywords: BRVO; Capillary plexus; Ischemia; OCT-A; RGC layer thickness
How to cite this article: Ana L Basílio, Luísa Vieira, Lívio Costa, Rita Proença, Rita Flores, etal. Analysis of Retinal Nonperfusion Area and Ganglion
Cell Layer Thickness in Branch Retinal Vein Occlusion by OCT-Angiography. JOJ Ophthal. 2018; 6(4): 555693. DOI: 10.19080/JOJO.2018.06.555693
002
JOJ Ophthalmology
follow-up duration and best-corrected visual acuity, converted
  
RGC layer thickness were evaluated in a 6x6 mm macular area
centered in fovea, captured by OCT-A device.
Sketch and CalcTM Software was used to calculate the areas.
 
plexus, the area of capillary density loss was delimited (Figure
1A). To calculate the area of reduced thickness in RGC layer, the
deviation area from the normal (based on the device database)
was considered (Figure 1B). The images of both plexus and the
images of RGC layer thickness were superimposed in order
to analyze the congruence in the location of the alterations
(ischemic areas of the plexus and areas of decrease in RGC layer
        
ophthalmologists, specialized in retina.
Figure 1: Example of delineated area of capillary density loss in supercial plexus (A) and of delineated area of reduced thickness in retinal
ganglion cell layer (B).
Statistical analysis was performed using SPSS software
version 23.0 (SPSS, Chicago, USA), using Wilcoxon test and
Spearman’s correlation. The p-value inferior to 0.05 was

Results
Table 1: Detailed data of patients.
 8
 10
Age (years)
Mean 75.6
Min. 60
Max. 88
SD 12.57
Gender - n (%)
Male 5 (62.5%)
Female 3 (37.5%)
Follow-up duration (months)
Mean 13.43
Min. 8
Max. 25
SD 9.74
BCVA (logMar)
Mean 0.44
Min. 0
Max. 1
SD 0.46
Min: Minimum; Max: Maximum; SD: Standard Deviation; BCVA: Best-
Corrected Visual Acuity
This study included 10 eyes with ischemic BRVO from 8
patients. Patients had a mean age of 75.60±12.57 years (range
60-88 years), 5 were males. Mean duration of follow-up was
13.43±9.74 months (range 8-25 months). Mean best-corrected
visual acuity in logMAR was 0.44±0.46 (range 0-1). Table 1
shows the baseline characteristics of the patients.
Table 2: Ischemic areas of vascular plexus and area of reduction of
RGC layer thickness.
2)
Mean 7.77
Min. 0.76
Max. 21.36
SD 6.72
2)
Mean 10.07
Min. 2.07
Max. 29.13
SD 8.27
Area of reduction of RGC layer thickness (mm2)
Mean 7.164
Min. 0.00
Max. 14.05
SD 4.53
Min: Minimum; Max: Maximum; SD: Standard Deviation; RGC: Retinal
Ganglion Cell
How to cite this article: Ana L Basílio, Luísa Vieira, Lívio Costa, Rita Proença, Rita Flores, etal. Analysis of Retinal Nonperfusion Area and Ganglion
Cell Layer Thickness in Branch Retinal Vein Occlusion by OCT-Angiography. JOJ Ophthal. 2018; 6(4): 555693. DOI: 10.19080/JOJO.2018.06.555693
003
JOJ Ophthalmology
The area of ischemia in deep plexus (mean 10.07±8.27 mm2)
        
7.77±6.72 mm2   
layer thickness was 7.16±4.53 mm2 (Table 2).
There was a strong correlation between the ischemic area
         



of deep plexus and the area of reduction of RGC layer thickness

During the analysis of the coincidence in location of altered
areas, in 6 eyes there were areas of non-ischemia-related
decrease in RGC layer thickness (Figure 2). Areas of ischemia not
related to atrophy were detected in 3 of 10 eyes (Figure 3).
Figure 2: Example of decreased ganglion cell layer thickness in infero-temporal region not coincident to capillary non-perfusion areas
detected in plexus.
Figure 3: Example of capillary non-perfusion areas on plexus images that are not related with a reduction of the ganglion cell layer
thickness.
Discussion
In BRVO eyes, the area of nonperfusion in deep capillary
          
consistent with a recent publication where the authors concluded
that nonperfusion grayish areas were more frequent in deep
      
Bonnin et al. [5] highly suggested in their work that deep
capillary vortexes are aligned along the course of the macular
         
intravascular pressure increases in major veins, promoting
a higher elevation in hydrostatic pressure in deep capillary,
resulting in a perfusion decrease in the retinal tissues drained by

plexus is directly connected to the retinal arterioles, with a
higher perfusion pressure and oxygen supply, and this may lead
  

Our results also suggest that ischemic area, mainly of
 
of inner retina, as it was correlated with the area of decreased
RGC layer thickness. Our study is also in keeping with Lim HB et
al. [8] who concluded that the thickness of macula, ganglion cell-



Other areas of decreased RGC layer thickness, not related to
ischemia, were detected suggesting that other pathophysiological
mechanisms may be involved in the atrophy process (Figure
2). The coexistence of risk factors, like aging, diabetes,
How to cite this article: Ana L Basílio, Luísa Vieira, Lívio Costa, Rita Proença, Rita Flores, etal. Analysis of Retinal Nonperfusion Area and Ganglion
Cell Layer Thickness in Branch Retinal Vein Occlusion by OCT-Angiography. JOJ Ophthal. 2018; 6(4): 555693. DOI: 10.19080/JOJO.2018.06.555693
004
JOJ Ophthalmology

[1,9]. On the other hand, ischemia can occur in the absence of
retinal atrophy (Figure 3). Diffusion from adjacent vessels and
the integrity of surrounding vasculature may play an important
role. In addition, the detection of capillary non-perfusion areas
       
areas, below the threshold, giving a false negative result [10].

correlates ischemic areas and reduced RGC layer thickness using
OCT-A, providing new insights into the involvement of capillary
plexus in inner retina atrophy.
Limitations of our study include the small number of cases,
derived from the exclusion of many other patients based on the

of the areas provides some subjectivity to the analysis, although
all delineations were approved by two retinal specialists.
Conclusion
This study suggests that ischemia may cause the decrease
of RGC layer thickness, although other pathophysiological
mechanisms may be involved. Larger sample size and prospective
studies are needed to further support our results.
Conicts of Interest

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DOI: 10.19080/JOJO.2018.06.555693
... Similar results were reported by Basílio et al., but in their study to determine the ischemic area in superficial and deep plexus, the area of capillary density loss was delimited using an additional software Sketch and CalcTM Software and VD and FAZ was not quantified. [26] Our study is also in keeping with Lim et al. who concluded that the thickness of macula, GCL-IPL, and retinal nerve fiber layer (RNFL) in the ischemic BRVO group was significantly reduced compared with the nonischemic BRVO group, especially in the RNFL. [27] However, we did not use FFA to delineate two groups of BRVO. ...
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Purpose: To describe the macular deep capillary plexus (DCP) in normal eyes using optical coherence tomography angiography. Methods: Retrospective study including 41 consecutive normal eyes imaged using optical coherence tomography angiography (RTVue XR Avanti; Optovue Inc). Default autosegmentation of the superficial capillary plexus (SCP) and DCP, and manual adjustments of "deep settings" were used to analyze the organization of the normal macular microvascularization and to investigate in vivo the connection between these capillary networks. Results: Mean age was 31 years (range, 22-55 years). The SCP and DCP had 2 different organizations, but the plexus autosegmentation was imperfect: In 68% of cases, the image of the SCP variably superimposed on the DCP, interfering with its analysis. The SCP was composed on average of 7 pairs of arterioles and venules obvious on each 3-mm × 3-mm optical coherence tomography angiography scanning area. The DCP was composed of a capillary vortex arrangement, whose centers were aligned along the course of the macular superficial venules. Conclusion: The SCP and DCP had two different topographic organizations. The pattern of the capillary units converging into capillary vortexes highly suggests that they drain into the superficial venules. The different structural properties of the SCP and DCP could explain the differences in flow resistance and perfusion.
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Importance The retinal vasculature is involved in many ocular diseases that cause visual loss. Although fluorescein angiography is the criterion standard for evaluating the retina vasculature, it has risks of adverse effects and known defects in imaging all the layers of the retinal vasculature. Optical coherence tomography (OCT) angiography can image vessels based on flow characteristics and may provide improved information.Objective To investigate the ability of OCT angiography to image the vascular layers within the retina compared with conventional fluorescein angiography.Design, Setting, and Participants In this study, performed from March 14, 2014, through June 24, 2014, a total of 5 consecutive, overlapping B-scan OCT angiography images composed of 216 A-scans were obtained at 216 discrete positions within a region of interest, typically a 2 × 2-mm area of the retina. The flow imaging was based on split-spectrum amplitude decorrelation angiography (SSADA), which can dissect layers of vessels in the retina. These distinct layers were compared with the fluorescein angiograms in 12 healthy eyes from patients at a private practice retina clinic to evaluate the ability to visualize the radial peripapillary capillary network. The proportion of the inner vs outer retinal vascular layers was estimated by 3 masked readers and compared with conventional fluorescein angiograms of the same eyes.Main Outcomes and Measures Outcome measures were visualization of the radial peripapillary capillary network in the fluorescein and SSADA scans and the proportion of the inner retinal vascular plexus vs the outer retinal capillary plexus as seen in SSADA scans that would match the fluorescein angiogram.Results In none of the 12 eyes could the radial peripapillary capillary network be visualized completely around the nerve head by fluorescein angiography, whereas the network was readily visualized in the SSADA scans. The fluorescein angiograms were matched, with a mean proportion of the inner vascular plexus being 95.3% (95% CI, 92.2%-97.8%) vs 4.7% (95% CI, 2.6%-5.7%) for the outer capillary plexus from the SSADA scans.Conclusions and Relevance Fluorescein angiography does not image the radial peripapillary or the deep capillary networks well. However, OCT angiography can image all layers of the retinal vasculature without dye injection. Therefore, OCT angiography, and the findings generated, have the potential to affect clinical evaluation of the retina in healthy patients and patients with disease.
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