Superficial capillary plexus vessel density/deep capillary plexus vessel density ratio in healthy eyes

doi:10.21203/rs.3.rs-1643620/v1

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Superficial capillary plexus vessel density/deep capillary plexus vessel density ratio in healthy eyes

https://doi.org/10.21203/rs.3.rs-1643620/v1

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Purpose: To identify factors differently affecting the superficial capillary plexus (SCP) and deep capillary plexus (DCP) in healthy eyes using their vessel density (VD) ratio.

Methods: Healthy eyes were enrolled. The ratio between the VD of SCP and DCP (SVD/DVD ratio) was calculated. Pearson correlation analyses were performed to identify the relationships between this ratio and other factors.

Results: The mean SVD and DVD were 36.0 ± 5.9 and 37.4 ± 4.8 %, respectively, and the mean SVD/DVD ratio was 0.96 ± 0.12. The SVD was significantly correlated with the best-corrected visual aucity (BCVA) (coefficient = -0.338, P < 0.001), age (coefficient = -0.389, P < 0.001), and OCTA quality (coefficient = 0.593, P < 0.001). The DVD was significantly correlated with the BCVA (coefficient = -0.194, P = 0.004), age (coefficient = -0.247, P < 0.001), and OCTA quality (coefficient = 0.507, P < 0.001). Among various factors, age (coefficient = -0.274, P < 0.001), the BCVA (coefficient = -2.80, P < 0.001), axial length (coefficient = 0.198, P = 0.003), and OCTA quality (coefficient = 0.271, P < 0.001) were significantly correlated with the SVD/DVD ratio.

Conclusions: Age, BCVA, axial length, and OCTA image quality were significantly correlated with the SVD/DVD ratio. Age, the BCVA, and OCTA quality were more strongly correlated with the SCP, and the axial length was more strongly correlated with the DCP.

Optical coherence tomography angiography

superficial capillary plexus

deep capillary plexus

vessel density

What is known:

Many factors affect the vessel density of the SCP and DCP in healthy eyes.

What we found:

Age, BCVA, axial length, and OCTA image quality were significantly correlated with the SVD/DVD ratio.

Age, the BCVA, and OCTA quality were more strongly correlated with the SCP, and the axial length was more strongly correlated with the DCP.

Fluorescein angiography (FA) has been the gold standard for evaluation of the retinal microcirculation and microvasculature. However, it is invasive, time-consuming, and difficult to observe the retinal microvasculature in detail due to dye diffusion. After the development of optical coherence tomography angiography (OCTA), which is non-invasive and enables visualization of retinal microvasculature with high resolution, OCTA has replaced FA in many clinical fields. One of the advantages of OCTA is that the retinal microvasculature can be examined for each retinal layer and can be quantified. OCTA yields various quantitative parameters including vessel density (VD), vessel length density, and the area of the foveal avascular zone (FAZ) of the superficial capillary plexus (from the internal limiting membrane [ILM] to the inner plexiform layer [IPL]; SCP) and the deep capillary plexus (from the outer border of the IPL to the outer border of the outer plexiform layer [OPL]; DCP) with relatively high reliability.[1–4]

Previous studies have reported impairment of retinal microvasculature in various ophthalmic diseases using OCTA. Chen et al.[5] reported that changes in the fractal dimension in the DCP could be an early indicator of microvasculature changes associated with diabetic retinopathy. Another study found that VD of the DCP (DVD) decreased in abnormal multifocal electroretinography patients using hydroxychloroquine for rheumatoid arthritis, but VD in the SCP (SVD) did not.[6] Meanwhile, Chou et al.[7] reported that there was a more pronounced decrease in macular perfusion density of SCP than of DCP in patients with non-arteritic anterior ischemic optic neuropathy. As such, the SCP and DCP can be differently affected by various conditions.

Therefore, we hypothesized that the factors affecting the normal retinal microvasculature would differ between the SCP and DCP. In this study, We derived the SVD/DVD ratio and identified factors that affect it.

Subjects

This retrospective, cross-sectional study adhered to the tenets of the Declaration of Helsinki and was approved by the Institutional Review Board of Konyang University Hospital, Daejeon, Korea. We reviewed the charts of patients who visited our retinal clinic for a floater, cataract, unilateral epiretinal membrane, macular hole, or intraocular lens dislocation, with fellow eyes without any ophthalmic disease. Written informed consent was waived due to the retrospective nature of the study. We obtained patient information of best-corrected visual acuity (BCVA), intraocular pressure, spherical equivalent, axial length (using an IOL master; Carl Zeiss, Jena, Germany, version 5.02), and parameters of OCT and OCTA. The exclusion criteria consisted of a history of systemic disease including diabetes and hypertension, glaucoma, optic nerve disorder, intraocular pressure ≥ 21 mmHg, axial length ≥ 26 mm, intraocular surgery except for cataract extraction, and a BCVA < 20/40. If both eyes met the inclusion criteria, one eye was randomly selected.

Octa Imaging Protocol

OCTA was performed using a Spectralis OCT2 device (Heidelberg Engineering, Heidelberg, Germany). The Spectralis OCT2 instrument can perform 70000 A-scan/sec using a light source centered at 870 nm, with axial and transverse resolution of 3.0 and 6 µm in tissue, respectively. En face images of the SCP, defined as the layer from the ILM to the IPL, and the DCP, defined as the layer from the outer border of the IPL to the OPL, were visualized automatically by segmenting two separate slabs defined by arbitrary segmentation lines, which are created by the device software. In this study, a 6.0 × 4.5 mm OCTA scans centered on the fovea was acquired. The VD was calculated as the percentage area occupied by blood vessels, with the blood vessels being defined as pixels having decorrelation values above the threshold level using ImageJ software (National Institutes of Health, Bethesda, MD, USA). In particular, 8-bit images were split into red, green, and blue channels, with the red channel used as the reference. The adjusted threshold tool was applied with default settings, and the dark background option was selected. This tool automatically sets the lower and upper threshold values (arbitrarily chosen as 110 and 255, respectively, for every image) and segmented grayscale images into features of interest and background (Fig. 1). Any image exhibiting fixation loss, segmentation errors, motion artifacts, or the value of OCTA quality < 25 dB was excluded.

Statistical Analysis

All statistical analyses were performed using SPSS statistical software (version 18.0; IBM Corp., Armonk, NY, USA). Pearson correlation analyses were performed to identify the relationship between the SVD/DVD ratio and variable factors. Demographic characteristics and ocular parameters were compared using 1-way ANOVA and the chi-squared test between groups divided according to the age.

Demographics and the SVD and the DVD values

A total of 222 eyes were enrolled. The mean age was 57.5 ± 13.5 years, the mean spherical equivalent was − 0.49 ± 2.63 diopters, and the mean axial length was 23.9 ± 1.0 mm (Table 1). The central macular thickness measured by OCT was 266.9 ± 23.5 µm.

Table 1

Demographics and characteristics of participants
Number of cases	222
Age (mean ± SD, years)	57.5 ± 13.5
Sex (male, %)	115 (51.8%)
Laterality (right, %)	114 (51.4)
Lens status (phakic, %)	207 (93.2)
BCVA (mean ± SD, logMAR)	0.05 ± 0.09
Spherical equivalent (mean ± SD, diopter)	-0.49 ± 2.63
Intraocular pressure (mean ± SD, mmHg)	13.1 ± 2.8
Axial length (mean ± SD, mm)	23.9 ± 1.0
Central macular thickness (mean ± SD, µm)	266.9 ± 23.5
BCVA, best-corrected visual acuity.

The mean SVD was 36.0 ± 5.9%, and the mean DVD was 37.4 ± 4.8% (Table 2). The mean OCTA quality was 32.7 ± 3.0 dB. The SVD/DVD ratio was 0.96 ± 0.12.

Table 2

Optical coherence tomography angiography parameters of participants
SVD (mean ± SD, %)	36.0 ± 5.9
DVD (mean ± SD, %)	37.4 ± 4.8
OCTA quality (mean ± SD,dB)	32.7 ± 3.0
SVD/DVD ratio (mean ± SD)	0.96 ± 0.12
SVD, vessel density of the superficial capillary plexus; DVD, vessel density of the deep capillary plexus; OCTA, optical coherence tomography angiography.

Correlations Between Octa Parameters And Various Factors

The SVD was negatively correlated with the BCVA (coefficient = -0.338, P < 0.001) and age (coefficient = -0.389, P < 0.001), and positively correlated with OCTA quality (coefficient = 0.593, P < 0.001). The DVD was also negatively correlated with BCVA (coefficient = -0.194, P = 0.004) and age (coeffieicnt = -0.247, P < 0.001), positively correlated with OCTA quality (coefficient = 0.507, P < 0.001).

Among various factors, age (coefficient = -0.274, P < 0.001) and the BCVA (coefficient = -2.80, P < 0.001) were negatively correlated, and the axial length (coefficient = 0.198, P = 0.003) and OCTA quality (coefficient = 0.271, P < 0.001) were positively correlated with the SVD/DVD ratio (Table 3) (Fig. 2).

Table 3

Correlations between the SVD/DVD ratio and other factors
	Coefficient	P value
Age	-0.274	< 0.001
Sex	-0.053	0.430
Laterality	0.025	0.714
BCVA	-0.280	< 0.001
Spherical equivalent	-0.165	0.014
Intraocular pressure	0.074	0.275
Lens status	-0.094	0.162
Axial length	0.198	0.003
Central macular thickness	0.121	0.072
OCTA quality	0.271	< 0.001
BCVA, best-corrected visual acuity; OCTA, optical coherence tomography angiography.

Analyses Of Octa Parameters According To Age

To analyze the difference in OCTA parameters and the SVD/DVD ratio according to age in more detail, subjects were divided into groups based on age by decade: over 70s (n = 43), 60s (n = 76), 50s (n = 35), 40s (n = 33), and 30s (n = 35) (Table 4). Variable factors including sex, laterality, spherical equivalent, intraocular pressure, axial length, central macular thickness, and OCTA quality did not significantly differ among groups except BCVA (P = 0.046). However, this difference was abolished in post hoc analyses. The SVD of each 70s, 60s, 50s, 40s, and 30s was 32.2 ± 5.7, 35.0 ± 5.8, 36.1 ± 5.0, 37.5 ± 5.3, and 40.4 ± 4.8, respectively, and they were significantly different (P < 0.001). The DVD of each group was 35.9 ± 4.4, 36.9 ± 4.1, 37.2 ± 5.1, 38.1 ± 4.9, and 40.1 ± 5.4, respectively, which were also significantly different (P = 0.002). Finally, the SVD/DVD ratio of each group was 0.93 ± 0.13, 0.95 ± 0.11, 0.98 ± 0.11, 0.99 ± 0.12, and 1.01 ± 0.09, respectively, and they significantly differed (P = 0.005) (Fig. 3).

Table 4

Subgroup analysis of optical coherence tomography angiography parameters according to the age
	Group 1 (70s) (n = 43)	Group 2 (60s) (n = 76)	Group 3 (50s) (n = 35)	Group 4 (40s) (n = 33)	Group 5 (30s) (n = 35)	P value
SVD	33.2 ± 5.7	35.0 ± 5.8	36.1 ± 5.0	37.5 ± 5.3	40.4 ± 4.8	< 0.001
DVD	35.9 ± 4.4	36.9 ± 4.1	37.2 ± 5.1	38.1 ± 4.9	40.1 ± 5.4	0.002
SVD/DVD ratio	0.93 ± 0.13	0.95 ± 0.11	0.98 ± 0.11	0.99 ± 0.12	1.01 ± 0.09	0.005
SVD, vessel density of the superficial capillary plexus; DVD, vessel density of the deep capillary plexus.

The SCP is observed as a defined silhouette morphology with a linear and continuous white shape against a black background in the OCTA image, which is lying in the retinal nerve fiber layer (RNFL) and the ganglion cell layer (GCL). The DCP is shown as a regular distribution around the FAZ with more complex multiple tiny radial and horizontal interconnections lying in the boundary plane between the inner nuclear layer (INL) and the OPL.[8] Such differences in the location, size, and morphology between SCP and DCP may cause different impacts by various factors between them. We tried to analyze this using the SVD/DVD ratio in normal eyes and found that age, the BCVA, the axial length, and OCTA quality were significantly correlated with the SVD/DVD ratio.

Previous studies reported a retinal microvascular decrease in eyes with high myopia, which would result from the elongation of eyeballs.[9–11] In our study, the axial length was positively correlated with the SVD/DVD ratio, which could mean that the longer the axial length, the greater the DVD reduction than the SVD reduction. The DCP may be more susceptible to damage caused by axial elongation than the SCP. You et al.[12] reported that longer axial length was significantly associated with the lower DVD, not with the lower SVD in their multivariate analyses, which is consistent with our study. This result would be associated with a previous study about the retinal layer thickness of high myopia. Kim et al.[13] reported that in high myopia, both the inner and outer rings of the ETDRS grid were thinned in INL (where the DCP is located), but only the outer ring was thinned in the inner retinal layer including GCL and IPL (where the SCP is located), indicating that the range of the thinned INL was wider than tha of the thinned inner retinal layer. The density of the smaller vessels in the DCP is greater than that in the SCP, and these smaller vessels may be more vulnerable to elongation damage, potentially leading to a greater decreas of the DVD than SVD compared to normal eyes.[8 14] Further studies including more range of axial length including ≥ 26.0 mm are needed to confirm this hypothesis.

When analyzing OCTA images, OCTA quality is crucial, which ranges from 0 (no signal) to 40 dB (excellent quality) and is considered good if the value is between 15 and 25 dB. Similar concepts are signal strength or signal strength index in other devices. Previous studies found that these values affected the measurement of VD and its reliability.[1 2 12 15–17] You et al.[12] reported that a lower SVD and DVD were significantly associated with a lower signal strength index, and it was the strongest impact on the measured retinal VD. However, to the best of our knowledge, no study has explored whether the SVD or DVD is more affected by quality values. We found that the SVD/DVD ratio was positively correlated with OCTA quality, indicating that the SVD is more directly affected by OCTA quality than the DVD. Although the exact mechanism is unclear, OCTA quality should be considered when comparing retinal VDs, especially of SCP.

Yu et al.[15] found that the parafoveal flow index and vessel area density decrease with increasing age at a rate of 0.6% and 0.4% per year. Jo et al.[18] also reported that age substantially affected VD in most of the peripapillary and macular areas. In our study, the older group showed a lower SVD and DVD, which is consistent with previous studies. Additionally, the SVD/DVD ratio was significantly correlated with age, which was lower in the older groups. This would result from different locations between SCP and DCP. The thickness of the inner retina including the RNFL, GCL, and IPL, which locates SCP, is known to decrease with increasing age. Previous studies reported the decrease in RNFL, GC-IPL with increasing age not only in diseased eyes but also in healthy eyes.[19–24] Additionally, the close relationship between the inner retinal layer thickness and the SVD has already been known through many studies.[25–28] Therefore, the SVD may interact with a thinning inner retina over time and decrease along with them. Whereas, the DCP lies on the INL and its thickness is relatively less affected by age. Therefore, the SCP could be more sensitive to changes in VD with age than the DCP.

Previous studies reported the relationship between the retinal VD and BCVA in patients with diabetes.[27 29 30] Samara et al.[29] reported that the VD had a moderate negative correlation with logMAR visual acuity at the level of both the SCP and DCP in eyes with diabetic retinopathy. Additionally, You et al.[12] reported that lower SVD and DVD were significantly associated with worse BCVA in a normal population. Our study showed a significant correlation between the BCVA and both the SVD and DVD in healthy eyes, which is consistent with a previous study. We also found that the SVD/DVD ratio was negatively correlated with the BCVA. The SVD located in the inner retina, which was more sensitive to ischemia and lack of oxygen and subsequently contributed to the photoreceptor cell damage and impaired BCVA in patients with diabetes, seemed to be correlated with BCVA more directly than the DVD also in healthy eyes.[30 31] Further studies are needed to confirm this result.

Our study has several limitations. First, the retrospective nature of the work inevitably introduces some selection bias. Second, since eyes with axial length ≥ 26.0 mm were excluded, additional studies including high myopia are needed to more accurately identify the relationship between axial length and the OCTA parameters as we mentioned above. The strength of this study was that we included a relatively large number of patients from a wide range of age groups, and enrolled OCTA images with OCTA quality ≥ 25 dB, allowing accurate analyses. Additionally, this is the first study to identify different impacts on the SCP and DCP by various factors via SVD/DVD ratio.

In conclusion, we investigated through the SVD/DVD ratio that various factors can affect SCP and DCP differently in healthy eyes and found that age, BCVA, axial length, and OCTA quality of OCTA images were significantly correlated with the SVD/DVD ratio. From these results, we were able to infer that age, the BCVA, and OCTA quality were more correlated with the SCP, while the axial length was more correlated with the DCP. Physicians should consider these results when interpreting OCTA images. Our results may also facilitate future OCTA analyses of retinal microvasculature according to retinal layer in eyes with various diseases.

Competing Interests and Funding The authors declare that they have no conflict of interest.

ACKNOWLEDGEMENT

A. Funding/Support : None

B. Financial Disclosures : None

C. Contributions to Authors in each of these areas

Design and conduct of the study (M.W.L., J.Y.K.); Collection of data (M.W.L., K.H.L., J.Y.K.); Analysis and interpretation of data (M.W.L., K.Y.N., J.Y.K.); Writing the article (M.W.L., K.Y.N., J.Y.K.); Critical revision of the article (M.W.L., K.Y.N., J.Y.K.); Final approval of the article (M.W.L., K.Y.N., K.H.L., J.Y.K.);

D. Other Acknowledgment: None

Data Availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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You are reading this latest preprint version

Superficial capillary plexus vessel density/deep capillary plexus vessel density ratio in healthy eyes

Status:

Version 1

Abstract

Figures

Key Messages

Introduction

Methods

Subjects

Octa Imaging Protocol

Statistical Analysis

Results

Demographics and the SVD and the DVD values

Correlations Between Octa Parameters And Various Factors

Analyses Of Octa Parameters According To Age

Discussion

Declarations

References

Status:

Version 1