Evaluation of the retinal vasculature of patients with branch retinal vein occlusion using optical coherence tomography angiography

Moura, Bárbara de Carvalho Freire Santos; Lira, Rodrigo Pessoa Cavalcanti; Arantes, Tiago Eugênio Faria e; Paiva, Isabel Braga; Bravo Filho, Vasco Torres Fernandes

doi:10.5935/0004-2749.20200091

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ORIGINAL ARTICLE • Arq. Bras. Oftalmol. 83 (6) • Nov-Dec 2020 • https://doi.org/10.5935/0004-2749.20200091 copy

Evaluation of the retinal vasculature of patients with branch retinal vein occlusion using optical coherence tomography angiography

Avaliação da vasculatura da retina em pacientes com oclusão de ramo da veia central da retina utilizando a angiografia por tomografia de coerência óptica

Authorship SCIMAGO INSTITUTIONS RANKINGS

ABSTRACT

Purpose:

To evaluate vascular density in superficial and deep capillary plexuses of the retina, measured using optical coherence tomography angiography in patients with branch retinal vein occlusion. Affected eyes were compared with the contralateral eye of the same patient and both were compared with normal eyes.

Methods:

A cross-sectional study including 16 previously untreated patients with branch retinal vein occlusion. Patients with poor quality examinations, bilateral disease, high refractive error, or any other retinal or choroidal disease were excluded. A total of 31 patients without eye disease were also selected as a comparison group. All participants underwent five optical coherence tomography angiographies, and only those with at least two good quality examinations were selected. The Kruskal-Wallis, Wilcoxon signed-rank, and Mann-Whitney U tests were used for the statistical analysis.

Results:

Vascular density was lower in affected eyes compared with contralateral eyes: whole density (p=0.020 for capillary plexuses superficial; p=0.049 for deep capillary plexuses) and parafoveal density (p=0.020 for capillary plexuses superficial; p=0.011 for deep capillary plexuses). Vascular density was also lower in affected eyes compared with normal eyes: whole density (p<0.001 for capillary plexuses superficial and deep) and parafoveal density (p<0.001 for capillary plexuses superficial and deep). Whole density (p=0.001 for capillary plexuses superficial and deep) and parafoveal density (p=0.001 for capillary plexuses superficial; p<0.001 for deep capillary plexuses) were both lower in the contralateral eyes compared with normal eyes. Following adjustment for arterial hypertension, this difference was no longer observed.

Conclusions:

Vascular density in capillary plexuses and deep capillary plexuses was lower in the eyes affected by branch retinal vein occlusion. Furthermore, the lower vascular density noted in the contralateral eyes indicates that changes most likely occurred in these eyes prior to the appearance of any clinically detectable alterations, reflecting the early signs of hypertensive retinopathy.

Keywords:
Retinal vein occlusion; Capillaries/pathology; Retinal vessels/physiopathology; Fovea centralis; Tomography, optical coherence; Fluorescein angiography

	Control (n=31)	Branch retinal vein occlusion (n=16)	p-value^* * The Mann-Whitney U test was used to compare age between the two groups and the chi-squared test to compare the categorical variables.
Age (years), mean ± SD (range)	51.3 ± 13.4 (23-78)	52.1 ± 9.7 (33-66)	0.770
Duration of disease (months), mean ± SD (range)	--	6.4 ± 4.8 (1-17)	--
Sex, n (%)
Male	9 (29)	6 (37.5)	0.555
Female	22 (71)	10 (62.5)
Systemic arterial hypertension, n (%)
No	25 (80.6)	3 (18.8)	<0.001
Yes	6 (19.4)	13 (81.3)
Diabetes mellitus, n (%)
No	28 (90.3)	13 (81.3)	0.395
Yes	3 (9.7)	3 (18.8)
Smoking, n (%)		.
No	29 (93.5)	11 (68.8)	0.036
Yes	2 (6.5)	5 (31.3)
Glaucoma, n (%)
No	28 (90.3)	12 (75.0)	0.208
Yes	3 (9.7)	4 (25.0)
Cardiovascular disease, n (%)
No	30 (96.8)	12 (75.0)	0.040
Yes	1 (3.2)	4 (25.0)
History of thrombosis, n (%)
No	31 (100)	13 (81.3)	0.035
Yes	0 (0)	3 (18.8)
Oral contraceptive use (females), n (%)^† † Data for oral contraceptive use by the female participants refer to 22 females evaluated in the control group and 10 females in the branch retinal vein occlusion group. SD= standard deviation.
No	20 (90.9)	9 (90.0)	<0.999
Yes	2 (9.1)	1 (10.0)

	BRVO-affected eyes (n=16)		Contralateral eyes (n=16)		p-value^* * Wilcoxon signed-rank test; SD= standard deviation.
	Mean ± SD	Range	Mean ± SD	Range
Signal strength index	58.8 ± 7.8	46.0-69.6	66.3 ± 7.8	51.8-78.4	0.005
Whole density (superficial)	46.4 ± 4.2%	38.5-52.3	49.1 ± 3.9%	41.7-54.7	0.020
Foveal density (superficial)	28.0 ± 5.6%	19.6-40.6	25.4 ± 5.7%	15.3-32.7	0.326
Parafoveal density (superficial)	47.1 ± 5.0%	38.6-54.6	51.0 ± 5.6%	42.1-58.1	0.020
Whole density (deep)	47.8 ± 4.6%	38.6-54.4	50.4 ± 4.2%	42.4-57.6	0.049
Foveal density (deep)	29.4 ± 6.3%	18.7-40.8	24.7 ± 5.6%	15.4-33.1	0.098
Parafoveal density (deep)	48.8 ± 5.4%	38.7-57.2	53.1 ± 5.8%	43.0-61.3	0.011

	BRVO-affected eyes (n=16)		Normal eyes (n=31)		p-value^* * Mann-Whitney U test; SD= standard deviation.
	Mean ± SD	Range	Mean ± SD	Range	p-value^* * Mann-Whitney U test; SD= standard deviation.
Signal strength index	58.8 ± 7.8	46.0-69.6	73.8 ± 6.2	59.0-81.0	<0.001
Whole density (superficial)	46.4 ± 4.2%	38.5-52.3	53.0 ± 3.4%	43.7-57.9	<0.001
Foveal density (superficial)	28.0 ± 5.6%	19.6-40.6	29.4 ± 6.1%	19.5-41.5	0.419
Parafoveal density (superficial)	47.1 ± 5.0%	38.6-54.6	56.3 ± 3.8%	46.2-61.9	<0.001
Whole density (deep)	47.8 ± 4.6%	38.6-54.4	54.6 ± 3.6%	43.7-59.8	<0.001
Foveal density (deep)	29.4 ± 6.3%	18.7-40.8	29.6 ± 7.0%	18.8-46.4	0.928
Parafoveal density (deep)	48.8 ± 5.4%	38.7-57.2	58.6 ± 4.0%	47.4-64.5	<0.001

	Contralateral eyes (n=16)		Normal eyes (n=31)		p-value^* * Mann-Whitney U test; SD= standard deviation.
	Mean ± SD	Range	Mean ± SD	Range	p-value^* * Mann-Whitney U test; SD= standard deviation.
Signal strength index	66.3 ± 7.8	51.8-78.4	73.8 ± 6.2	59.0-81.0	0.001
Whole density (superficial)	49.1 ± 3.9%	41.7-54.7	53.0 ± 3.4%	43.7-57.9	0.001
Foveal density (superficial)	25.4 ± 5.7%	15.3-32.7	29.4 ± 6.1%	19.5-41.5	0.076
Parafoveal density (superficial)	51.0 ± 5.6%	42.1-58.1	56.3 ± 3.8%	46.2-61.9	0.001
Whole density (deep)	50.4 ± 4.2%	42.4-57.6	54.6 ± 3.6%	43.7-59.8	0.001
Foveal density (deep)	24.7 ± 5.6%	15.4-33.1	29.6 ± 7.0%	18.8-46.4	0.037
Parafoveal density (deep)	53.1 ± 5.8%	43.0-61.3	58.6 ± 4.0%	47.4-64.5	<0.001

	Control (after adjustment for SAH) (n=7)	Branch retinal vein occlusion (n=16)	p-value^* * The Mann-Whitney U test was used to compare age between the two groups and the chi-squared test to compare the categorical variables.
Age (years), mean ± SD (range)	59.3 ± 11.0 (48-74)	52.1 ± 9.7 (33-66)	0.216
Duration of disease (months), mean ± SD (range)	--	6.4 ± 4.8 (1-17)	--
Sex, n (%)			>0.99
Male	2 (28.6)	6 (37.5)
Female	5 (71.4)	10 (62.5)
Systemic arterial hypertension, n (%)			>0.99
No	1 (14.3)	3 (18.8)
Yes	6 (85.7)	13 (81.3)
Diabetes mellitus, n (%)			0.62
No	5 (71.4)	13 (81.3)
Yes	2 (28.6%)	3 (18.8)
Smoking, n (%)		.	0.27
No	7 (100)	11 (68.8)
Yes	0 (0)	5 (31.3)
Glaucoma, n (%)			>0.99
No	5 (71.4)	12 (75.0)
Yes	2 (28.6)	4 (25.0)
Cardiovascular disease, n (%)			>0.99
No	6 (85.7)	12 (75.0)
Yes	1 (14.3)	4 (25.0)
History of thrombosis, n (%)			0.53
No	7 (100)	13 (81.3)
Yes	0 (0)	3 (18.8)
Oral contraceptive use (females), n (%)^† † Data for oral contraceptive use by the female participants refer to five females evaluated in the control group and 10 females in the branch retinal vein occlusion group. SD= standard deviation.			>0.99
No	5 (100)	9 (90.0)
Yes	0 (0)	1 (10.0)

	BRVO-affected eyes (n=16)		Control (after adjustment for SAH)		p-value^* * Mann-Whitney U test; SD= standard deviation.
	Mean ± SD	Range	Mean ± SD	Range	p-value^* * Mann-Whitney U test; SD= standard deviation.
Signal strength index	58.8 ± 7.8	46.0-69.6	71.1 ± 6.6	60.0-79.0	0.004
Whole density (superficial)	46.4 ± 4.2%	38.5-52.3	50.4 ± 3.0%	47.4-54.9	0.042
Foveal density (superficial)	28.0 ± 5.6%	19.6-40.6	27.1 ± 4.3%	20.4-31.7	<0.99
Parafoveal density (superficial)	47.1 ± 5.0%	38.6-54.6	53.5 ± 4.2%	47.3-58.7	0.013
Whole density (deep)	47.8 ± 4.6%	38.6-54.4	51.8 ± 2.8%	48.2-55.5	0.061
Foveal density (deep)	29.4 ± 6.3%	18.7-40.8	27.3 ± 4.7%	20.1-32.2	0.442
Parafoveal density (deep)	48.8 ± 5.4%	38.7-57.2	55.4 ± 4.2%	48.9-59.7	0.011

	Contralateral eyes (n=16)		Control (after adjustment for SAH)		p-value^* * Mann-Whitney U test; SD= standard deviation.
	Mean ± SD	Range	Mean ± SD	Range	p-value^* * Mann-Whitney U test; SD= standard deviation.
Signal strength index	66.3 ± 7.8	51.8-78.4	71.1 ± 6.6	60.0-79.0	0.132
Whole density (superficial)	49.1 ± 3.9%	41.7-54.7	50.4 ± 3.0%	47.4-54.9	0.316
Foveal density (superficial)	25.4 ± 5.7%	15.3-32.7	27.1 ± 4.3%	20.4-31.7	0.593
Parafoveal density (superficial)	51.0 ± 5.6%	42.1-58.1	53.5 ± 4.2%	47.3-58.7	0.385
Whole density (deep)	50.4 ± 4.2%	42.4-57.6	51.8 ± 2.8%	48.2-55.5	0.504
Foveal density (deep)	24.7 ± 5.6%	15.4-33.1	27.3 ± 4.7%	20.1-32.2	0.285
Parafoveal density (deep)	53.1 ± 5.8%	43.0-61.3	55.4 ± 4.2%	48.9-59.7	0.242

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[1] Corresponding author: Bárbara de C. F. S. Moura. E-mail: barbaracarvalhofreire@gmail.com