Foveal Microvascular Changes Based on Optical Coherence Tomography Angiography in Mild Nonproliferative Diabetic Retinopathy

Bokjun Ji; Hyung Chan Kim

doi:10.3341/JKOS.2016.57.11.1723

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Ji and Kim: Foveal Microvascular Changes Based on Optical Coherence Tomography Angiography in Mild Nonproliferative Diabetic Retinopathy

Original Article

J Korean Ophthalmol Soc 2016;57(11):1723-1730.

Published online: 25 September 2016

DOI: https://doi.org/10.3341/JKOS.2016.57.11.1723

Foveal Microvascular Changes Based on Optical Coherence Tomography Angiography in Mild Nonproliferative Diabetic Retinopathy

Bokjun Ji, MD, Hyung Chan Kim, MD, PhD

Department of Ophthalmology, Konkuk University School of Medicine, Seoul, Korea

Address reprint requests to Hyung Chan Kim, MD, PhD Department of Ophthalmology, Konkuk University Medical Center, #120-1 Neungdong-ro, Gwangjin-gu, Seoul 05030, Korea Tel: 82-2-2030-8179, Fax: 82-2-2030-5273 E-mail: eyekim@kuh.ac.kr

Received 4 May 2016 Revised 3 August 2016 Accepted 23 October 2016

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Purpose

To investigate the microvascular change in diabetic patients with no diabetic retinopathy (DR) and mild nonproliferative DR (NPDR) using optical coherence tomography angiography (OCTA).

Methods

We retrospectively reviewed the medical records of 44 eyes of 22 patients with no DR and 34 eyes of 17 patients with mild NPDR. OCTA was performed on a 3 × 3 mm region centered in the fovea and parafoveal areas. The foveal avascular zone (FAZ) and foveal and parafoveal flow density (FD) in superficial and deep vascular plexuses were analyzed using OCTA.

Results

The FAZ of deep capillary plexus in patients with mild NPDR was significantly larger than in patients with no DR (p = 0.008). The parafoveal deep FD, foveal and parafoveal thickness in patients with no DR was significantly larger than in patients with mild NPDR (p = 0.013, p = 0.018 and p = 0.003, respectively). Superficial FAZ, superficial foveal FD, superficial parafoveal FD and deep foveal FD were not significantly different between the patients with no DR and those with mild NPDR.

Conclusions

OCTA allows detection of deep FAZ enlargement, reduction in parafoveal deep FD as well as foveal and parafoveal thickness in patients with mild NPDR compared with patients with no DR.

Keywords: Diabetic retinopathy, Flow density, Foveal avascular zone, Microvascular changes, Optical coherence tomography angiography

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Figure 1.

Optical coherence tomography angiography images of no diabetic retinopathy. 3 × 3 mm optical coherence tomography angiogram in superficial capillary plexus (A, C, E) and in deep capillary plexus (B, D, F). (A, B) Fovea and parafovea area in superficial and deep capillary plexus (inner ring: diameter 1 mm, fovea area, outer ring: diameter 2.5 mm, parafovea area). (C, D) Automated foveal avascular zone measurement of superficial and deep capillary plexus. (E, F) Peudo-color map of flow density of superficial and deep capillary plexus.

Figure 2.

Manual adjustment of the foveal avascular zone (FAZ) boundary. (A) optical coherence tomography angiogram of the macula in the deep capillary plexus. (B) FAZ boundary misidentification by automated program. (C) Manually corrected boundary of FAZ using built-in software.

Table 1.

Baseline characteristics of patients

	No DR	Mild NPDR	p-value^*
Patients (n)	22	17
Mean age (years)	57.18 ± 12.34	63.41 ± 11.60	0.081
Mean duration of DM (months)	75.14 ± 78.85	166.82 ± 95.01	0.002
Male (n, %)	12 (54.5)	7 (41.2)	0.408
Hypertension (n, %)	10 (45.5)	9 (52.9)	0.643
Hyperlipidemia (n, %)	11 (50)	8 (47.1)	0.855

Values are presented as mean ± SD or n (%) unless otherwise indicated. DR = diabetic retinopathy; NPDR = nonproliferative diabetic retinopathy; DM = diabetes mellitus.

^* Mann-Whitney test: mean age, mean duration of DM, Chi-square test: Male, Hypertension, Hyperlipidemia.

Table 2.

Comparison of no DR and mild NPDR

	No DR (n = 44)	Mild NPDR (n = 34)	p-value^*
FAZ (mm²)
Superficial	0.39 ± 0.11	0.43 ± 0.12	0.098
Deep	0.54 ± 0.15	0.68 ± 0.31	0.008
Fovea FD (%)
Superficial	27.16 ± 3.64	26.49 ± 4.70	0.478
Deep	25.58 ± 4.55	24.56 ± 5.36	0.367
Parafovea FD (%)
Superficial	50.51 ± 4.56	49.06 ± 3.61	0.130
Deep	56.93 ± 4.14	54.61 ± 3.83	0.013
Thickness (μ m)
Fovea	243.34 ± 13.69	233.56 ± 21.89	0.018
Parafovea	313.09 ± 12.16	302.09 ± 19.84	0.003
IOP (mm Hg)	14.25 ± 2.70	15.24 ± 2.56	0.106
BCVA (log MAR)	0.04 ± 0.08	0.07 ± 0.11	0.112

Values are presented as mean ± SD unless otherwise indicated. DR = diabetic retinopathy; NPDR = nonproliferative diabetic retinopathy; FAZ = fovea avascular zone; FD = flow density; IOP = intraocular pressure; BCVA = best corrected visual acuity; log MAR = logarithm of the minimum angle of resolution.

^* Student t-test.

Table 3.

Comparison of superficial and deep layer

	Superficial	Deep	p-value^*
No DR
FAZ (mm²)	0.39 ± 0.11	0.54 ± 0.15	<0.001
Fovea FD (%)	27.16 ± 3.64	25.58 ± 4.55	0.001
Parafovea FD (%)	50.51 ± 4.56	56.93 ± 4.14	<0.001
Mild NPDR
FAZ (mm²)	0.43 ± 0.12	0.68 ± 0.31	<0.001
Fovea FD (%)	26.49 ± 4.70	24.56 ± 5.36	0.003
Parafovea FD (%)	49.06 ± 3.61	54.61 ± 3.83	<0.001

Values are presented as mean ± SD unless otherwise indicated. DR = diabetic retinopathy; FAZ = fovea avascular zone; FD = flow density; NPDR = nonproliferative diabetic retinopathy.

^* Paired t-test

Table 4.

Subgroup analysis

	Hypertension		p-value^*	Hyperlipidemia		p-value^*	Gender		p-value^*
	With (n = 40)	Without (n = 38)	p-value^*	With (n = 40)	Without (n = 38)	p-value^*	Male (n = 38)	Female (n = 40)	p-value^*
FAZ (mm²)
Superficial	0.40 ± 0.13	0.41 ± 0.11	0.57	0.58 ± 0.14	0.42 ± 0.10	0.45	0.41 ± 0.12	0.63 ± 0.30	0.52
Deep	0.66 ± 0.29	0.54 ± 0.16	0.02	0.62 ± 0.30	0.58 ± 0.17	0.44	0.63 ± 0.30	0.57 ± 0.17	0.29
Fovea FD (%)
Superficial	25.53 ± 4.61	26.21 ± 3.85	0.15	27.36 ± 4.35	26.39 ± 3.89	0.30	26.42 ± 4.03	27.28 ± 4.21	0.36
Deep	24.73 ± 5.24	25.53 ± 4.61	0.47	25.30 ± 5.14	24.99 ± 4.74	0.78	25.19 ± 5.04	25.09 ± 4.84	0.92
Parafovea FD (%	)
Superficial	49.92 ± 3.62	49.84 ± 4.75	0.94	49.52 ± 4.23	50.22 ± 4.22	0.47	48.74 ± 4.65	50.96 ± 3.47	0.02
Deep	55.69 ± 4.81	56.14 ± 3.45	0.64	55.19 ± 4.75	56.62 ± 3.40	0.13	54.29 ± 4.57	57.47 ± 3.02	<0.01
Thickness (μ m)
Fovea	240.42 ± 15.16	237.80 ± 20.93	0.53	240.40 ± 16.11	237.83 ± 20.25	0.54	242.40 ± 20.33	235.93 ± 15.70	0.12
Parafovea	207.32 ± 14.84	309.22 ± 18.57	0.62	306.61 ± 15.27	309.90 ± 18.14	0.39	309.37 ± 18.23	307.32 ± 15.43	0.60

Values are presented as mean ± SD unless otherwise indicated. FAZ = fovea avascular zone; FD = flow density.

^* Student t-test.

Table 5.

Association of superficial fovea avascular zone with parameters

Variables	Univariate		Multivariate^*
Variables	Estimate	p-value	Estimate	p-value
Deep FAZ	0.194	<0.001	0.145	0.008
Fovea thickness	–0.003	<0.001	–0.002	0.010
Parafovea thickness	–0.001	0.068
Age	0.001	0.358	–	–
Duration of DM	<0.001	0.103	–	–
BCVA (log MAR)	0.205	0.152	–	–

FAZ = fovea avascular zone; DM = diabetes mellitus; BCVA = best corrected Visual acuity; log MAR = logarithm of the minimum angle of resolution.

^* Multivariate linear regression analysis with backward elimination; R²: 0.227.

Table 6.

Association of deep fovea avascular zone with parameters

Variables	Univariate		Multivariate^*
Variables	Estimate	p-value	Estimate	p-value
Superficial FAZ	0.792	<0.001	0.677	0.004
Fovea thickness	–0.005	0.002
Parafovea thickness	–0.003	0.070
Age	0.005	0.025
Duration of DM	0.001	0.001	0.001	0.002
BCVA (log MAR)	0.506	0.078

FAZ = fovea avascular zone; DM = diabetes mellitus; BCVA = best corrected visual acuity; log MAR = logarithm of the minimum angle of resolution.

^* Multivariate linear regression analysis with backward elimination; R²: 0.208.

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