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. 2020 Oct 30;9(11):3514.
doi: 10.3390/jcm9113514.

Early Retinal Changes by OCT Angiography and Multifocal Electroretinography in Diabetes

Luisa Frizziero  1 , Giulia Midena  2 , Evelyn Longhin  3 , Marianna Berton  4 , Tommaso Torresin  3 , Raffaele Parrozzani  3 , Elisabetta Pilotto  3
Affiliations

Early Retinal Changes by OCT Angiography and Multifocal Electroretinography in Diabetes

Luisa Frizziero et al. J Clin Med. .

Abstract

Background: To evaluate the earliest retinal morphological and functional changes in diabetic eyes without or with early signs of diabetic retinopathy (DR).

Methods: Twenty-two eyes with no DR (noDR group), 22 eyes with mild DR (DR group), and 18 healthy nondiabetic eyes (controls) were enrolled. All eyes were studied by means of spectral domain optical coherence tomography (OCT), OCT angiography (OCTA), and multifocal electroretinogram (mfERG).

Results: A significantly higher number of OCT hyperreflective intraretinal foci (HRF) was found in both noDR and DR groups versus controls, but not between DR groups. The OCTA parameters of the superficial vascular plexus (SVP) were significantly reduced in the noDR group both versus controls and DR group (p < 0.05). The OCTA parameters of the intermediate capillary plexus (ICP) were significantly reduced in the DR group versus controls. An increased number of altered hexagons on mfERG was found in the noDR versus the DR group (p = 0.0192).

Conclusions: Retinal vascular and functional parameters are differently involved in diabetic eyes; major vascular changes in the SVP and functional alterations of the mfERG are present in diabetic eyes with no clinical microvascular signs of DR, while ICP is mainly involved when early ophthalmoscopic signs of DR are present. The integrated use of mfERG and OCTA provides new significant insights into the pathogenesis of diabetic related retinal disease.

Keywords: diabetic retinopathy; early stages; hyperreflective intraretinal spots; microaneurysms; morpho-functional correlation; multifocal electroretinography; optical coherence tomography; optical coherence tomography angiography; retinal layers; vascular plexuses.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Linear spectral domain optical coherence tomography scan centered onto the fovea showing hyperreflective intraretinal foci (HRF) detection. The vertical red lines border the area where HRF are counted (3 mm length). The red arrows indicate the boundary between the inner retina (from the inner limiting membrane to the lower border of the inner plexiform layer) and the outer retina (from the upper limit of the outer nuclear layer and the boundary of the retinal pigment epithelium—Bruch’s membrane). White and yellow arrowheads indicate HRF in the inner and outer retina, respectively. Only HRF with small dimension (≤30 micron), intermediate reflectivity (similar to retinal nerve fiber layer) and no back-shadowing were considered.
Figure 2
Figure 2
En-face optical coherence tomography (OCT) angiography of the superficial vascular plexus (SVP), intermediate (ICP) and deep capillary plexus (DCP) with the corresponding slabs at the OCT B scan (a–c). The SVP (A) en-face image was generated by a slab extending from RNFL to inner plexiform layer (IPL)-(IPL-corresponds to 17 μm over IPL), the ICP (B) by a slab extending from IPL− to IPL+ (IPL + corresponds to 22 μm below IPL) and the DCP (C) by a slab extending from IPL + to outer plexiform layer (OPL). Automatically binarized (D–F) and skeletonized (G–I) images of each plexus with ImageJ software.
Figure 3
Figure 3
Representation of mean number of hyperreflective intraretinal foci (HRF) in the inner (IR) and outer retina (OR) in all diabetic eyes versus healthy controls (A,B) and in diabetic eyes without DR (noDr) and with mild DR (DR) versus controls (A’,B’). A significantly increased number of HRF in the IR and OR of all diabetics versus controls and in each diabetic group versus controls was found. * Statistically significant difference compared to controls.
Figure 4
Figure 4
Representation of vessel area density (VAD), vessel length fraction (VLF), vessel diameter index (VDI), and fractal dimension (FD) of the superficial vascular plexus (SVP, a), intermediate (ICP, b) and deep capillary plexus (DCP, c) in all diabetic eyes versus controls (upper row) and in diabetic eyes without diabetic retinopathy DR (noDR) and with DR (DR), separately compared to control group (lower row). (a) significant reduction of VAD, VLF and FD was found in diabetic eyes versus controls. The VAD and VLF of noDR group showed a significant reduction compared to controls and to DR. FD showed a significant reduction in both noDR and DR groups versus controls. (b) significant reduction of VLF and FD was found in diabetic eyes versus controls and confirmed in DR group, when separately evaluated. (c) significant reduction of FD was found in diabetic eyes versus controls and still present in noDR group, when separately evaluated. * Statistically significant difference compared to controls; # statistically significant difference compared to DR group
Figure 5
Figure 5
Representation of the implicit time (IT) on multifocal electroretinography (mfERG) waves in controls, no Diabetic Retinopathy (DR) and DR groups. In hexagon 13 and 16 there is a significantly increased IT in the noDR versus the DR group (p = 0.0273 and p = 0.0471, respectively).
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