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. 2017 Jul 1;58(9):3804-3817.
doi: 10.1167/iovs.17-21460.

Age-Related Alterations in the Retinal Microvasculature, Microcirculation, and Microstructure

Yantao Wei  1   2 , Hong Jiang  2   3 , Yingying Shi  2 , Dongyi Qu  2 , Giovanni Gregori  2 , Fang Zheng  2 , Tatjana Rundek  3 , Jianhua Wang  2
Affiliations

Age-Related Alterations in the Retinal Microvasculature, Microcirculation, and Microstructure

Yantao Wei et al. Invest Ophthalmol Vis Sci. .

Erratum in

  • Erratum.
    [No authors listed] [No authors listed] Invest Ophthalmol Vis Sci. 2017 Aug 1;58(10):4247. doi: 10.1167/iovs.17-21460a. Invest Ophthalmol Vis Sci. 2017. PMID: 28846774 Free PMC article. No abstract available.

Abstract

Purpose: To characterize age-related alterations in the retinal microcirculation, microvascular network, and microstructure in healthy subjects.

Methods: Seventy-four healthy subjects aged from 18 to 82 years were recruited and divided into four age groups (G1 with age <35 years, G2 with age 35 ∼ 49 years, G3 with age 50 ∼ 64 years, and G4 with age ≥65 years). Custom ultra-high resolution optical coherence tomography (UHR-OCT) was used to acquire six intraretinal layers of the macula. OCT angiography (OCTA) was used to image the retinal microvascular network. The retinal blood flow velocity (BFV) was measured using a Retinal Function Imager (RFI).

Results: Compared to G1, G2 had significant thinning of the retinal nerve fiber layer (RNFL) (P < 0.05), while G3 had thinning of the RNFL and ganglion cell and inner plexiform layer (GCIPL) (P < 0.05), in addition to thickening of the outer plexiform layer (OPL) and photoreceptor layer (PR) (P < 0.05). G4 had loss in retinal vessel density, thinning in RNFL and GCIPL, and decrease in venular BFV, in addition to thickening of the OPL and PR (P < 0.05). Age was negatively related to retinal vessel densities, the inner retinal layers, and venular BFV (P < 0.05). By contrast, age was positively related to OPL and PR (P < 0.05).

Conclusions: During aging, decreases in retinal vessel density, inner retinal layer thickness, and venular BFV were evident and impacted each other as observed by simultaneous changes in multiple retinal components.

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Figures

Figure 1
Figure 1
Image processing and separation of large and small vessels. The raw OCTA enface view image of the SVP (A) with a field of view 3 × 3 mm2 was processed to extract the large vessels with a diameter > ∼25 μm (B). Both the small vessels (C) and large vessels (D) were skeletonized for fractal analyses. For the DVP (E), the shadowgraphic project artifacts (F) from the SVP (A) were removed. The remaining small vessels were skeletonized (G) for analyses.
Figure 2
Figure 2
Annulus for quantification of vessel density. The annular zone (0.6–2.5 mm) of the 3 × 3 mm2 OCTA enface image (A) and the annulus (0.6–5.0 mm) of the 6 × 6 mm2 OCTA enface image (B) were used for fractal analysis.
Figure 3
Figure 3
The RVN from 3 × 3 mm2 OCTA scans. A–C belongs to a 30-year-old subject, while D–F belongs to a 69-year-old subject. (A, D) Total RVN. (B, E) SVP. (C, F) DVP.
Figure 4
Figure 4
Retinal blood flow (RBF) velocity imaged using the RFI. The field of view is 7.3 × 7.3 mm2. BFV (unit: mm/s) of the secondary and tertiary branches of retinal arteries (red) and veins (purple) was measured. (A) A 32-year-old subject. (B) A 65-year-old subject.
Figure 5
Figure 5
Intraretinal layers and corresponding thickness maps. (A) A B-scan. (B) Automated segmentation of seven anatomical interfaces. (C) Six thickness maps over a disk of 6 mm in diameter obtained from the automated segmentation.
Figure 6
Figure 6
Intraretinal thickness for the different age groups. Compared to G1, G2 showed significant thinning of the RNFL (P < 0.05). G3 showed significant thinning of the TRT, RNFL, and GCIPL (P < 0.05), in addition to thickening of the PR (P < 0.05). G4 showed significant thinning in the RNFL and GCIPL, in addition to thickening of the OPL and PR (P < 0.05). Asterisk (*) denotes P < 0.05 compared to G1. Bars = SD.
Figure 7
Figure 7
Retinal microvascular densities for the different age groups. Compared to G1, G4 showed significantly lesser small vessels in the RVN, the SVP and DVP in both annuli from 0.6 to 2.5 mm and 0.6 to 5.0 mm (A, P < 0.05). There were no significant differences of the large vessels among groups in both RVN and SVP in both annuli (B, P > 0.05). The ratios of the small vessel density to the large vessel density were significantly smaller in G4 compared to G2 in both annuli (C, P < 0.05). Note the large vessels extracted from the DVP are regarded as the shadowgraphic project artifacts; therefore, the density was not measured. 3RVD, total retinal vessel density in the annulus from 0.6 to 2.5 mm; 3SVD, superficial vessel density in the annulus from 0.6 to 2.5 mm; 3DVD, deep vessel density in the annulus from 0.6 to 2.5 mm; 6RVD, total retinal vessel density in the annulus from 0.6 to 5.0 mm; 6SVD, superficial vessel density in the annulus from 0.6 to 5.0 mm; 6DVD, deep vessel density in the annulus from 0.6 to 5.0 mm. Asterisk (*) denotes P < 0.05 compared to G1. Bars = SD.
Figure 8
Figure 8
Retinal BFV for the different age groups. G3 showed an increase in arteriolar BFV (P < 0.05) compared to G1. G4 showed a significant decrease in venular BFV (P < 0.05). Asterisk (*) denotes P < 0.05 compared to G1. Bars = SD.
Figure 9
Figure 9
Relationship between age and retinal vessel density. (A, D) Total retinal vessel density. (B, E) Superficial retinal vessel density. (C, F) Deep retinal vessel density. The plots on the left (A–C) correspond to an annulus from 0.6 to 2.5 mm in the perifoveal region. The plots on the right (D–F) correspond to an annulus from 0.6 to 5 mm in the perifoveal region.
Figure 10
Figure 10
Relationship between age and the thicknesses of inner retinal layers. (A) Plot using the TRT. (B) Plot using the thickness of the RNFL. (C) Plot using the thickness of the GCIPL. (D) Plot using the thickness of the INL.
Figure 11
Figure 11
Relationship between age and the thicknesses of outer retinal layers. (A) Plot using the thicknesses of the OPL. (B) Plot using the thickness of the PR. (C) Plot using the thickness of the ONL.
Figure 12
Figure 12
Relationship between age and retinal BFVs. (A) Venular BFV. (B) Arteriolar BFV.
Figure 13
Figure 13
Relationship between deep vessel density and the thickness of retinal layers. (A) TRT. (B) GCIPL thickness. (C) INL thickness. (D) ONL thickness.
Figure 14
Figure 14
Relationship between retinal vessel density and retinal BFV. (A) Venular BFV. (B) Arteriolar BFV.
Figure 15
Figure 15
The age-related changes and interlink among retinal microstructure, microvasculature, and microcirculation. Overall, aging played a role in the thinning of the retinal inner segment, loss of retinal microvasculature, and decreased venular BFV. The changes in microvasculature were related to thinning of the inner retina and venular blood flow.
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