Ophthalmic Surgery, Lasers and Imaging Retina

Clinical Science 

Effect of Age and Myopia on Retinal Microvasculature

Yunxia Leng, MD, PhD; Emily K. Tam, MD, MPH; Khalil Ghasemi Falavarjani, MD; Irena Tsui, MD

Abstract

BACKGROUND AND OBJECTIVE:

To investigate the effect of age and refractive error on changes in the retinal microvascular network.

PATIENTS AND METHODS:

Subjects were recruited from the Doheny Eye Institute. Refractive error and axial length were measured. High myopia was defined as refractive error greater than −6 diopters (D). Optical coherence tomography angiography (OCTA) imaging was performed and images were analyzed using fractal analysis. Primary outcomes were superficial capillary plexus (SCP) vessel density, deep capillary plexus (DCP) vessel density, and foveal avascular zone (FAZ) area.

RESULTS:

One hundred thirty-eight eyes of 69 subjects were included. Twenty-eight (41%) subjects were male and 41 (59%) subjects were female. Mean age was 42.81 years ± 19.91 years (range: 8 years to 87 years). Mean refractive error was −1.74 D ± 3.18 D (range: −15.78 D to 4.25 D), and mean axial length (AL) was 24.29 mm ± 1.35 mm (range: 21.73 mm to 28.32 mm). SCP and DCP vessel densities were negatively correlated to age (r = −0.22, P = .011; and r = −0.49, P < .001). Controlling for age, patients with high myopia and longer AL had decreased SCP density (P = .021 and P = .027, respectively), but no difference in DCP vessel density was observed (P = .065 and P = .058, respectively). FAZ area was not significantly correlated to age, gender, refraction, or AL.

CONCLUSIONS:

SCP and DCP vessel densities decreased with age. In addition, SCP density but not DCP vessel density was reduced in eyes with high myopia and longer AL.

[Ophthalmic Surg Lasers Imaging Retina. 2018;49:925–931.]

Abstract

BACKGROUND AND OBJECTIVE:

To investigate the effect of age and refractive error on changes in the retinal microvascular network.

PATIENTS AND METHODS:

Subjects were recruited from the Doheny Eye Institute. Refractive error and axial length were measured. High myopia was defined as refractive error greater than −6 diopters (D). Optical coherence tomography angiography (OCTA) imaging was performed and images were analyzed using fractal analysis. Primary outcomes were superficial capillary plexus (SCP) vessel density, deep capillary plexus (DCP) vessel density, and foveal avascular zone (FAZ) area.

RESULTS:

One hundred thirty-eight eyes of 69 subjects were included. Twenty-eight (41%) subjects were male and 41 (59%) subjects were female. Mean age was 42.81 years ± 19.91 years (range: 8 years to 87 years). Mean refractive error was −1.74 D ± 3.18 D (range: −15.78 D to 4.25 D), and mean axial length (AL) was 24.29 mm ± 1.35 mm (range: 21.73 mm to 28.32 mm). SCP and DCP vessel densities were negatively correlated to age (r = −0.22, P = .011; and r = −0.49, P < .001). Controlling for age, patients with high myopia and longer AL had decreased SCP density (P = .021 and P = .027, respectively), but no difference in DCP vessel density was observed (P = .065 and P = .058, respectively). FAZ area was not significantly correlated to age, gender, refraction, or AL.

CONCLUSIONS:

SCP and DCP vessel densities decreased with age. In addition, SCP density but not DCP vessel density was reduced in eyes with high myopia and longer AL.

[Ophthalmic Surg Lasers Imaging Retina. 2018;49:925–931.]

Introduction

Myopia is a common eye condition.1–3 Pathological myopia is an important cause of irreversible blindness, as it can lead to abnormalities such as glaucoma, foveal retinoschisis, retinal pigment epithelial atrophy, posterior staphyloma, choroidal neovascularization (CNV), and retinal detachment.4–9 Although there are retinal changes in myopia, less is known regarding retinal microvascular changes in myopic eyes.

Optical coherence tomography angiography (OCTA) is one of the methods available that can provide noninvasive, depth-resolved imaging of the retinal microvascular layers. It will provide more detailed and clearer images of the retinal microvascular because of its high-resolution optical imaging.10–13,18 Compared to fluorescein angiography or indocyanine green angiography, OCTA is safer and simpler to perform since it does not require any dye injection.14–17 OCTA has been widely used in the research and diagnosis of various retinal macular diseases, including diabetic retinopathy, retinal vascular occlusion, and CNV.

High myopia is a high-risk factor for CNV. Therefore, we wanted to find the early changes and trends of macular microvascular in myopia. We examined the macular microvascular in different refractive states of the population with OCTA. Our study aims to investigate the effect of age and high myopia on retinal microvasculature using OCTA.

Patients and Methods

This prospective case series study was approved by the UCLA Institutional Review Board and adhered to the tenets of the Declaration of Helsinki and Health Insurance Portability and Accountability Act. Informed consent was obtained from each subject. Healthy subjects with normal ocular examinations and without a known history of ocular disease were recruited from the Doheny Eye Clinic. Patients with a history of hypertension, diabetes mellitus, sickle cell disease, anemia, radiation, or other systemic conditions known to affect the retinal microvasculature were excluded. Patients with eye diseases other than refractive error were excluded. Eyes with 2+ or greater cataract or other media opacity were excluded.

Demographic information collected included age, gender, and race. Ophthalmic examination included Snellen visual acuity, autorefraction (Auto Refractometer RM-8900; Topcon, Tokyo, Japan), and axial length (AL) measurement (IOL-master; Carl Zeiss Meditec, Jena, Germany and Lenstar 900 Optical Biometer; Haag-Streit, Köeniz, Switzerland).

Image Acquisition

OCTA images were acquired with AngioPlex (version 3896, Cirrus HD-OCT 5000; Carl Zeiss Meditec, Dublin, CA). The technical aspects of Angioplex OCTA have been previously described in detail.19 Briefly, the system is an upgrade of the Cirrus model 5000 instrument, which is capable of scanning at a rate 68,000 A-scans per second with an 870 nm wavelength. The angiography is generated by repeated B-scans at the same locations, which is analyzed for both intensity and phase information. The algorithm for processing the blood flow information is OCT microangiography complex, which yields the enface vessel network in different retinal layers. In the present study, a 3 × 3 mm2 angiogram was generated in less than 3 seconds by taking four sequential B-scans in each Y-axis location with approximately 9,000 B-scans, each being composed of 245 A-scans (A scan = 1 pixel). The OCTA system also incorporated a real time retinal tracking technology named FastTrac, which reduces motion artifact.19

Each scan was automatically segmented in order to visualize the superficial capillary plexus (SCP) and deep capillary plexus (DCP). The SCP was segmented with an inner boundary at the internal limiting membrane and an outer boundary set at the inner plexiform layer. The DCP en face OCTA image was segmented with an inner boundary at the inner plexiform layer and an outer boundary at the outer plexiform layer. All scans were reviewed to ensure absence of artifacts including segmentation, motion and blink artifacts, and sufficient image quality.28 Images with a signal strength of 7/10 or less were excluded.

Image Analysis

Quantitative analyses of SCP vessel density, DCP vessel density, and foveal avascular zone (FAZ) area were performed using the en face OCTA projection images. OCTA images were imported into ImageJ version 1.50i software (National Institutes of Health, Bethesda, MD) in order to binarize the images. National Institutes of Health image thresholding was performed before binarization. Vessel density was calculated from the binarized images as (pixels of vessels)/(pixels of whole image) in percentage. FAZ in SCP was manually outlined by two graders (Leng and Tam) in original 3 mm × 3 mm scans, and its area was calculated as [(pixels of FAZ) 9 mm2/(pixels of whole image)] in mm2.

Statistical Analysis

Statistical analyses were performed by using SPSS software version 16.0 (SPSS, Chicago, IL). Intraclass correlation coefficient (ICC) and 95% confidence interval (CI) were used to measure the reproducibility of FAZ area. The Kolmogorov-Smirnov test was used to test the normality. For non-normal distributions, Mann-Whitney U test and Kruskal-Wallis H test were applied. For normal distributions, t-test and one-way analysis of variance (ANOVA) followed by Student-Newman-Keuls (SNK) test were used. Pearson correlation analysis was conducted to determine associations. Paired t-test was used to measure the differences of refraction, AL, FAZ, SCP, and DCP between the left and right eyes. Paired t-test was used to address the correlation between fellow eyes. High myopia was defined as a refractive error greater than −6 diopters (D) without signs of pathologic myopia. A P value less than .05 was considered statistically significant.

Results

One hundred thirty-eight eyes of 69 subjects including 28 (40.6%) males and (59.4%) 41 females with a mean age of 42.81 years ± 19.91 years (range: 8 years to 87 years) were assessed. Fifty-one patients (73.9%) were Asian and 19 (26.1%) were non-Asian. Mean non-mydriatic automated refraction was −1.74 D ± 3.18 D (interquartile range: −0.75 to 3.31) and mean AL was 24.29 mm ± 1.35 mm (range: 21.73 mm to 28.32 mm). We did the correlation tests between myopia and AL. The Pearson correlation analysis showed that refraction was negatively associated with AL (r = −0.67, P < .001).

Average SCP vessel density was 0.28 ± 0.05. ANOVA showed that SCP was significantly different across age groups (P = .031). The significant findings of ANOVA analysis by results of Student-Newman-Keuls (SNK) test was a P value less than .05 (Table 4). Pearson correlation analysis test for correlations of the SCP with age, the SCP vessel densities were negatively correlated to age (r = −0.22, P = .011) (Table 3, Figure 1). No significant differences in SCP vessel density was found between eyes (P = .355), by gender (P = .517), refractive error groups (P = .118), or AL groups (P = .869) (Table 1).

Quantitative Analysis of Vessel Density and FAZ According to Age, Refraction, and AL

Table 1:

Quantitative Analysis of Vessel Density and FAZ According to Age, Refraction, and AL

Quantitative Analysis of Vessel Density and FAZ According to Refraction and ALWith the Same Age Groups

Table 2:

Quantitative Analysis of Vessel Density and FAZ According to Refraction and ALWith the Same Age Groups

The Correlation Tests Between Age and SCP / DCP / FAZ

Table 3:

The Correlation Tests Between Age and SCP / DCP / FAZ

The Differences of SCP and DCP With Age Groups With SNK Test

Table 4:

The Differences of SCP and DCP With Age Groups With SNK Test

Superficial capillary plexus (SCP) density and deep capillary plexus (DCP) density by age.

Figure 1.

Superficial capillary plexus (SCP) density and deep capillary plexus (DCP) density by age.

Average DCP vessel density was 0.37 ± 0.04. DCP was significantly different across age groups (P < .001). The results of the Student-Newman-Keuls (SNK) test was a P value less than .05 (Table 4). With the Pearson correlation analysis test for correlations of the DCP with age, the DCP vessel densities were negatively correlated to age (r = −0.49, P < .001) (Table 3, Figure 1). No significant differences in DCP vessel density were found between eyes (P = .485), by gender (P = .534), ethnicity (P = .408), refractive error groups (P = .057), or AL groups (P = .393) (Table 1).

The reproducibility of the FAZ measurement was excellent (ICC = 0.96). Average FAZ area was 0.32 μm ± 0.10 μm. We found that the FAZ area was not significantly different across eyes (P = .736), age groups (P = .057), genders (P = .346), ethnicities (P = .435), refraction groups (P = .435), and AL groups (P = .908) (Table 1).

When highly myopic eyes (refraction < −6 D) were compared with the age-matched eyes (refraction > −1 D) SCP vessel density was significantly different (P = .021, Table 2). There was no significant difference in FAZ area (P = .937) or DCP vessel density between highly myopic and control eyes (P = .065).

When longer AL eyes (AL > 26 mm) were compared with age matched group (AL < 23 mm). The mean FAZ and DCP vessel density was similar (P = .594 and P = .058, respectively). However, the SCP was statistically significantly different between the two groups (P = .027) (Table 2, Figure 2).

Superficial capillary plexus (SCP) density and deep capillary plexus (DCP) density by age-matched refractive error.RD = right eye

Figure 2.

Superficial capillary plexus (SCP) density and deep capillary plexus (DCP) density by age-matched refractive error.RD = right eye

Optical coherence tomography angiography 3 × 3 mm2 scans segmented at the superficial capillary plexus (SCP) (top) and the deep capillary plexus (DCP) (middle). Manual outlining (green) of the borders as foveal avascular zone at the superficial capillary plexus (bottom).

Figure 3.

Optical coherence tomography angiography 3 × 3 mm2 scans segmented at the superficial capillary plexus (SCP) (top) and the deep capillary plexus (DCP) (middle). Manual outlining (green) of the borders as foveal avascular zone at the superficial capillary plexus (bottom).

Discussion

Our study reported on OCTA characteristics of 138 eyes of 69 subjects with age between 8 to 87 years old and refractive errors ranges from −15.75 D to 4.25 D. We studied individuals with an AL ranging from 21.73 mm to 28.34 mm without any pathologic retinal and choroidal lesions. SCP and DCP densities were significantly decreased with increased age, and did not correlate with gender, ethnicity, refraction groups, and AL groups. However, when we compared age- and sex-matched groups, the SCP density was significantly less correlated with high myopia and longer AL.

Previous studies have similarly shown that SCP and DCP decreases with older age.20,21 Yu et al. reported the decrease of SCP parafoveal flow index and vessel area density with increasing age at a rate of 0.6% and 0.4% per year in healthy Chinese patients.22 The study by Wang et al. showed both SCP and DCP decreases with older age. Our results are consistent with these studies.20 The study of 34 eyes of 17 healthy subjects by Shahlaee reported mean parafoveal vascular densities in SCP and DCP were 46% and 52%, respectively.23 However, according to our study, the mean densities in SCP and DCP were 30% and 42%, respectively. At the same time, we also found the DCP decreased more significantly than the SCP with age. Reasons for the discrepancy between us may be due to the difference in the study populations, including ethnic background and age distribution, and different retinal imaging machines.

In an OCTA study by Hassan et al. of 24 eyes, myopia was found to be associated with lower vessel flow density in the DCP compared to SCP, leading to thinning of inner nuclear layer and thickening of the Henle fiber layer and outer nuclear layer, myeloid and ellipsoid zone, and outer segment of photoreceptors.24 Another OCTA study by Yang et al.25 found that both SCP and DCP densities were not correlated with spherical equivalent or AL. These studies are in contrast from our study, which found SCP to be more effected by myopia than DCP. Reasons for this may be related to differences in study populations, inclusion criteria, imaging device, and image analysis protocols. Further studies in larger populations are warranted to clarify the potential role of retinal ischemia in the pathogenesis of pathological myopia.

The size of FAZ was stable in different groups of age, refractive errors, and AL. This is consistent with the study of Li et al., which showed no difference of the area and diameter of the FAZ in myopic eyes and the controlled eyes.26 Our results also showed the area and diameter of the FAZ were not related to age or refractive error.

A limitation of this study is that OCTA is relatively new modality, and there are currently no studies that show that device is the best in providing retinal information on age and myopia, as there are differences in image acquisition and analytics between different OCTA machines.27 However, strengths of the study include rigorous collection of prospective data, including AL and refractive error, in a population with a large age range.

In summary, our study used fractal analysis to evaluate the FAZ, SCP, and DCP, providing more detailed information to elaborate the effect of myopia on vascular changes. We found that age affects DCP more significantly compared to SCP, while refraction and AL effect the SCP more significantly than the DCP.

References

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Quantitative Analysis of Vessel Density and FAZ According to Age, Refraction, and AL

FAZ (µm) P Value SCP (%) P Value DCP (%) P Value

Eyes
  OD (N = 69) 0.31 ± 0.09 .736a 0.29 ± 0.05 .355a 0.37 ± 0.04 .485a
  OS (N = 69) 0.32 ± 0.10 0.28 ± 0.05 0.37 ± 0.04

Age
  < 20 years (N = 18) 0.26 ± 0.10 .057b 0.29 ± 0.04 .031b* 0.41 ± 0.03 < .001b*
  20–39 years (N = 46) 0.33 ± 0.10 0.31 ± 0.05 0.37 ± 0.04
  40–59 years (N = 42) 0.32 ± 0.10 0.28 ± 0.06 0.37 ± 0.04
  ≥ 60 years (N = 32) 0.32 ± 0.08 0.27 ± 0.05 0.34 ± 0.03

Refraction
  High myopia < − 6.0 D (N = 14) 0.33 ± 0.03 .540e 0.26 ± 0.05 .118e 0.35 ± 0.03 .057b
  Moderate myopia (−6.0 D, −3.0 D) (N = 20) 0.29 ± 0.10 0.28 ± 0.05 0.37 ± 0.05
  Mild myopia (−3.0 D, −1.0 D) (N = 24) 0.30 ± 0.09 0.29 ± 0.05 0.38 ± 0.03
  Emmetropia (−1.0 D, +1.0 D) (N = 64) 0.33 ± 0.11 0.29 ± 0.05 0.36 ± 0.04
  Hyperopia (= +1.0 D) (N = 16) 0.31 ± 0.10 0.30 ± 0.07 0.39 ± 0.04

AL
  < 22 mm (N = 3) 0.34 ± 0.08 .908b 0.30 ± 0.02 .869e 0.38± 0.03 .393b
  22 mm – 24 mm (N = 53) 0.32 ± 0.12 0.29 ± 0.06 0.36 ± 0.04
  24 mm, 26 mm] (N = 65) 0.31 ± 0.10 0.28 ± 0.05 0.37 ± 0.05
  ≥ 26 mm (N = 17) 0.31 ± 0.05 0.27 ± 0.06 0.34 ± 0.03

Total 0.32 ± 0.10 0.28 ± 0.05 0.37 ± 0.04

Quantitative Analysis of Vessel Density and FAZ According to Refraction and ALWith the Same Age Groups

FAZ (µm) P Value SCP (%) P Value DCP (%) P Value

AL With Age-Matched Group
  < 23 mm (N = 15) 0.32 ± 0.11 .594c 0.31 ± 0.05 .027c* 0.37± 0.04 .058c
  > 26 mm (N = 17) 0.31 ± 0.05 0.27 ± 0.06 0.34 ± 0.03

Refraction With Age-Matched Group
  > −1.0 (N = 16) 0.32 ± 0.11 .937c 0.32 ± 0.03 .021c* 0.38± 0.04 .065c
  < −6.0 (N = 14) 0.33 ± 0.03 0.28 ± 0.05 0.35 ± 0.03

The Correlation Tests Between Age and SCP / DCP / FAZ

Age
Coefficient P Value
SCP −0.22 .011*f
DCP −0.49 < .001*f
FAZ 0.14 .112

The Differences of SCP and DCP With Age Groups With SNK Test

Age Groups SCP DCP

Set 1 Set 2 Set 3 Set 1 Set 2 Set 3
  < 20 years (N = 18) 0.29 ± 0.04 0.41 ± 0.03
  20–39 years (N = 46) 0.31 ± 0.05 0.37 ± 0.04
  40–59 years (N = 42) 0.28 ± 0.06 0.37 ± 0.04
  ≥ 60 years (N = 32) 0.27 ± 0.05 0.34 ± 0.03

P Value 1.000 1.000 .356 1.000 .442 1.000
Authors

From Guangzhou First People's Hospital, the Second Affiliated Hospital of South China University of Technology, Guangdong Sheng, China (YL); the Department of Ophthalmology, Boston University, Boston (EKT); the Eye Department, Iran University of Medical Sciences, Tehran, Iran (KGF); and Stein Eye Institute, Doheny Eye Institute, Veterans Affairs Medical Center, University of California, Los Angeles (IT).

This study was supported by an unrestricted grant from Research to Preventing Blindness to the Stein Eye Institute.

The authors report no relevant financial disclosures.

Address correspondence to Irena Tsui, MD, Stein Eye Institute, University of California, 100 Stein Plaza, Los Angeles, CA 90095; email: itsui@jsei.ucla.edu.

Received: March 28, 2018
Accepted: November 02, 2018

10.3928/23258160-20181203-03

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