Abstract
Purpose: To provide clinical evidence of the associations between retinal neuronal degeneration and microvasculopathy in diabetic retinopathy (DR).Methods: This case-control study included 76 patients (76 eyes) with type 2 diabetes mellitus (DM), and refraction error between −3.0 and +3.0 D. The eyes were assigned into DM (without DR), non-proliferative DR (NPDR), and proliferative DR (PDR) groups. Age-, sex-, and refractive error-matched normal subjects were enrolled as controls. The mean retinal thickness (mRT), the relative mean thickness of the retinal nerve fiber layer (rmtRNFL, mtRNFL/mRT), ganglion cell layer (rmtGCL), ganglion cell complex (rmtGCC) layer, foveal avascular zone area (FAZa), FAZ perimeter (FAZp), FAZ circularity index (FAZ-CI), and vessel density (VD) in superficial capillary plexus (SCP) and deep capillary plexus (DCP) were assessed by swept-source optical coherence tomography (OCT) and OCT angiography (OCTA). Group comparison and Spearman's partial correlation coefficient analysis were applied to evaluate the correlation between these morphological parameters.Results: rmtRNFL, FAZa, and FAZp in SCP and DCP increased with the DR severity (prmtRNFL < 0.001; pFAZa, SCP = 0.001; pFAZa, DCP = 0.005; pFAZp, SCP < 0.001; pFAZp, DCP < 0.001). The rmtGCL, FAZ-CI in SCP and DCP, and VD in DCP decreased with the DR severity (prmtGCL = 0.002, pFAZ−CI, SCP = 0.002; pFAZ−CI, DCP < 0.001, pVD, DCP < 0.001). After controlling age, sex, duration of diabetes, and hypertension, the rmtRNFL, FAZa in SCP and DCP, and FAZp in SCP and DCP were correlated with the severity of DR (p < 0.05), while VD in SCP and DCP, FAZ-CI, and rmtGCL were negatively correlated with the severity of DR (p < 0.05). The rmtGCL was negatively correlated with the FAZa in SCP (r = −0.34, p = 0.002) and DCP (r = −0.23, p = 0.033), and FAZp in SCP (r = −0.37, p = 0.001) and DCP (r = −0.32, p = 0.003), but positively correlated with VD in SCP (r = 0.26, p = 0.016), VD in DCP (r = 0.28, p = 0.012), and FAZ-CI in DCP (r = 0.31, p = 0.006).Conclusions: rmtRNFL, FAZ-CI in SCP and DCP, and FAZp in SCP are strong predictors of the severity of DR. The ganglion cell body loss is highly correlated with increased FAZp and FAZa, decreased FAZ-CI, and reduced VD with the severity of DR.
Highlights
Diabetic retinopathy (DR) is among the most significant and disabling chronic complications of diabetes mellitus [1, 2]
We found that the superficial capillary plexus (SCP) vessel density decreased with diabetic retinopathy severity while there was no significant difference between the four groups (29.12 ± 3.98% vs. 27.88 ± 4.18% vs. 26.25 ± 4.94% vs. 26.25 ± 3.72%, pall = 0.067) (Figure 4A, Table 2)
We found that increased relative mean thickness of retinal nerve fiber layer (RNFL) (rmtRNFL), foveal avascular zone area (FAZa), and FAZ perimeter (FAZp), decreased rmtGCL, vessel density (VD), and Foveal avascular zone (FAZ)-CI are correlated with the severity of DR. rmtRNFL, FAZ circularity index (FAZ-CI) in SCP and deep capillary plexus (DCP), and FAZp in SCP are stronger predictors of the severity of DR than the FAZa
Summary
Diabetic retinopathy (DR) is among the most significant and disabling chronic complications of diabetes mellitus [1, 2]. Clinical studies further confirmed that retinal neurons dysfunction occurred before retinal microvasculopathy using electroretinography (ERG) and visual field examinations [9,10,11]. In this study, advanced swept-source optical coherence tomography (SS-OCT) and OCT angiography (OCTA) were used to further investigate the correlation between the early and sensitive parameters of retinal microvasculopathy including the foveal avascular zone area (FAZa), FAZ perimeter (FAZp), FAZ circularity index (FAZ-CI), and retinal vessel density (VD) in superficial capillary plexus (SCP) and deep capillary plexus (DCP), and the parameters for evaluation of the early morphological changes of ganglion cells including the relative mean thickness of the Abbreviations: ADA, American Diabetes Association; ANOVA, One-way analysis of variance; BCVA, Best-corrected visual acuity; CBF, Cerebral blood flow; D, Diopter; DCP, Deep capillary plexus; DM, Diabetes mellitus; DR, Diabetic retinopathy; ERG, Electroretinography; ETDRS, Early Treatment Diabetic Retinopathy Study Classification; FAZ, Foveal avascular zone; FAZa, Foveal avascular zone area; FAZ-CI, Foveal avascular zone-circularity index; FAZp, Foveal avascular zone perimeter; FFA, Fundus fluorescein angiography; GCC, Ganglion cell complex; GCL, Ganglion cell; ICP, Intracranial pressure; IIH, Idiopathic intracranial hypertension; IQR, Interquartile; mRT, Mean retinal thickness; NPDR, Non-proliferative diabetic retinopathy; NVU, Neurovascular unit; OCT, Optical coherence tomography; OCTA, Optical coherence tomography angiography; PDR, Proliferative diabetic retinopathy; rmtGCC, Relative mean thickness of the ganglion cell complex; rmtGCL, Relative mean thickness of the ganglion cell; rmtRNFL, Relative mean thickness of the retinal nerve fiber; RNFL, Retinal nerve fiber; RNVU, Retinal neuronal vascular unit; SCP, Superficial capillary plexus; SS-OCT, Swept-source optical coherence tomography; T2DM, Type 2 diabetes mellitus; TABS, TOPCON Advanced Boundary Segmentation; VD, Vessel density; VEP, Visual evoked potential
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