Optical Coherence Tomography Angiography in Diabetic Patients: A Systematic Review

Abstract

Background: Diabetic retinopathy (DR) is the leading cause of legal blindness in the working population in developed countries. Optical coherence tomography (OCT) angiography (OCTA) has risen as an essential tool in the diagnosis and control of diabetic patients, with and without DR, allowing visualisation of the retinal and choroidal microvasculature, their qualitative and quantitative changes, the progression of vascular disease, quantification of ischaemic areas, and the detection of preclinical changes. The aim of this article is to analyse the current applications of OCTA and provide an updated overview of them in the evaluation of DR.

Methods: A systematic literature search was performed in PubMed and Embase, including the keywords "OCTA" OR "OCT angiography" OR "optical coherence tomography angiography" AND "diabetes" OR "diabetes mellitus" OR "diabetic retinopathy" OR "diabetic maculopathy" OR "diabetic macular oedema" OR "diabetic macular ischaemia". Of the 1456 studies initially identified, 107 studies were screened after duplication, and those articles that did not meet the selection criteria were removed. Finally, after looking for missing data, we included 135 studies in this review.

Results: We present the common and distinctive findings in the analysed papers after the literature search including the diagnostic use of OCTA in diabetes mellitus (DM) patients. We describe previous findings in retinal vascularization, including microaneurysms, foveal avascular zone (FAZ) changes in both size and morphology, changes in vascular perfusion, the appearance of retinal microvascular abnormalities or new vessels, and diabetic macular oedema (DME) and the use of deep learning technology applied to this disease.

Conclusion: OCTA findings enable the diagnosis and follow-up of DM patients, including those with no detectable lesions with other devices. The evaluation of retinal and choroidal plexuses using OCTA is a fundamental tool for the diagnosis and prognosis of DR.

Keywords: FAZ; OCTA; diabetes mellitus; diabetic macular oedema; diabetic retinopathy; foveal avascular zone; optical coherence tomography angiography.

Figure 1

Morphological changes in the vascular plexuses throughout the human retina. (A) Whole-mount human retina immunostained with an antibody against collagen type IV showing the vascular network from the optic nerve to Ora serrata. (B) Drawings of the different plexuses corresponding to the insets in (A). Four plexuses can be observed in the peripapillary area (RPCN, SCP, ICP, and DCP) close to the optic nerve. The central retina is composed of three plexuses (SCP, ICP, and DCP), except in the fovea where the foveal avascular zone (FAZ) exists. Only two plexuses (SCP and DCP) are present in the far-periphery area. RPCN, radial peripapillary capillary network; SCP, superficial capillary plexus; ICP, intermediate capillary plexus; DCP, deep capillary plexus. Scale bar: 1 mm.

Figure 2

Flow chart explaining the literature selection. A systematic review was performed following PRISMA guidelines. A total of 1456 records were selected (829 in PubMed and 627 in Embase), and after the removal of duplicate studies or articles that did not meet the selection criteria, 107 articles were selected for a full literature review. Ultimately, a total of 135 studies were included after adding important works that were not found in the databases.

Figure 3

Swept source optical coherence tomography angiography (SS-OCTA) showing representative examples of OCTA findings in diabetic patients. OCTA was acquired using DRI-Triton SS-OCT (Topcon, Tokyo, Japan). (A,B) Superficial (SCP) and deep capillary plexuses (DCP) in 3 × 3 mm scans. Figure 3C shows SCP in a 6 × 6 scan. (D,E) The SCP in a 9 × 9 scan and 3F SCP in a 6 × 6 scan protocol. (B) An irregular foveal avascular zone (red arrows) and microaneurysms (red arrowheads) in the superficial and deep capillary plexuses. (C) Nonperfusion areas in the temporal area (green arrows). (D,E) Areas of impaired perfusion associated with intraretinal microvascular abnormalities (yellow arrows). (F) Retinal neovascularization elsewhere (yellow arrowhead). Scale bar represents 1 mm.

Figure 4

Optical coherence tomography angiography (OCTA) of a diabetic patient without detectable diabetic lesions. OCTA was acquired using DRI-Triton SS-OCT (Topcon, Tokyo, Japan) with a 3 × 3 mm scan protocol. (A) Superficial capillary plexus, (B) deep capillary plexus, and (C) choriocapillaris (CC). Red arrow shows a disruption in the foveal avascular zone (FAZ), red arrowheads correspond to microaneurysms, and green arrows correspond to non-perfusion areas in the CC. Scale bar (in yellow) represents 500 microns.

Figure 5

Fluorescein angiography (FA) (A,C,D) vs. swept source optical coherence tomography angiography (SS-OCTA) (B,E,F) showing microaneurysms (MAs) (red arrow and arrowhead) in diabetic patients. (A,C,D) MAs in the superficial and deep capillary plexuses (SCP and DCP) and nonperfusion areas (green and blue arrows) detected by (A,B,E,F) show the same MAs in SCP (E), DCP (F), and nonperfusion areas (B), visualised by OCTA. FA was acquired using a Spectralis-HRA (Heidelberg Engineering, Heidelberg, Germany). (A,C) Arterial time in the FA and (D) tissue times. OCTA was acquired with DRI-Triton SS-OCT (Topcon, Tokyo, Japan). (B) 9 × 9 mm OCTA and (E,F) 3 × 3 mm OCTA of both SCP and DCP, respectively. Scale bar (in yellow) represents 1 mm in Figure 5A,B and 250 microns in Figure 5C,F.