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 Table of Contents  
ORIGINAL ARTICLE
Year : 2021  |  Volume : 33  |  Issue : 3  |  Page : 299-305

Analysis of foveal microvascular abnormalities in various stages of diabetic retinopathy using optical coherence tomography angiography


1 Assistant Professor, Department of Ophthalmology, Bangalore Medical College and Research Institute, Bengaluru, Karnataka, India
2 Professor and HOD, Department of Retina, Bangalore Medical College and Research Institute, Bengaluru, Karnataka, India
3 Junior Resident, Minto Regional Institute of Ophthalmology, Bangalore Medical College and Research Institute, Bengaluru, Karnataka, India

Date of Submission01-Dec-2020
Date of Decision14-Feb-2021
Date of Acceptance22-Feb-2021
Date of Web Publication08-Dec-2021

Correspondence Address:
Dr. B C Hemalatha
House No 156, Kantha Nivas, 3rd Phase, 1st Block, Banashankari 3rd Stage , Bangalore 560085, Karnataka
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/kjo.kjo_195_20

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  Abstract 


Purpose: Diabetic retinopathy (DR) remains a leading cause of vision loss in the adult population. The purpose of our study was to analyze and co-relate diabetic retinopathy-related micro-vascular changes using Optical Coherence Tomography Angiography (OCTA) in various stages of diabetic retinopathy. Methods: One hundred and twenty eyes of diabetic patients were categorized into three groups of forty each. Group-A included eyes without retinopathy, Group-B included eyes with Non-Proliferative Diabetic Retinopathy and Group-C included eyes with proliferative DR. Apart from complete ocular examination, foveal avascular zone parameters were analyzed using OCTA. Results: Statistically significant differences were found concerning vascular density and perfusion density between eyes with DR when compared to eyes without DR (P>0.001). 9 Vascular density (VD) significantly decreases in eyes with the progressive stage of DR. Foveal avascular zone showed a significant increase in area, perimeter, and circularity in the eyes with PDR compared to other groups. Conclusion: FAZ metrics showed significant changes proportional to diabetic retinopathy stages. Vascular density and perfusion density parameter analysis by OCTA could be used as early biomarkers in predicting the risk of diabetic retinopathy progression.

Keywords: Diabetic macular edema, diabetic retinopathy, foveal avascular zone, optical coherence tomography angiography, superficial capillary plexus, vessel density


How to cite this article:
Hemalatha B C, Kalpana B N, Shilpa Y D, Ravi B, Argekar VR, Hithashree H R, Dixith V S. Analysis of foveal microvascular abnormalities in various stages of diabetic retinopathy using optical coherence tomography angiography. Kerala J Ophthalmol 2021;33:299-305

How to cite this URL:
Hemalatha B C, Kalpana B N, Shilpa Y D, Ravi B, Argekar VR, Hithashree H R, Dixith V S. Analysis of foveal microvascular abnormalities in various stages of diabetic retinopathy using optical coherence tomography angiography. Kerala J Ophthalmol [serial online] 2021 [cited 2022 Jan 19];33:299-305. Available from: http://www.kjophthal.com/text.asp?2021/33/3/299/331939




  Introduction Top


Diabetic retinopathy is the leading cause of blindness worldwide owing to its microvascular complications. The predicted worldwide prevalence of diabetes in the recent scenario may reach 430 million by 2030.[1] The long duration of diabetes and poor glycemic control are the major risk factors for retinopathy. Early diagnosis is imperative in preventing the sight-threatening complications. Sight-threatening complications occur as a result of macular involvement, such as in diabetic macular edema (DME) or diabetic macular ischemia (DMI) and due to the development of the proliferative disease. Mere slit lamp bio-microscopy screening may miss retinopathy changes in diabetic patients. Although fluorescein angiography provides functional information regarding the leakage of dye to provide information on the permeability of vessels, it is an invasive procedure with the added risk of the procedure and dye-related events. Repeating the invasive above procedure among renal and cardiac patients is also an additional risk.

Optical coherence tomography angiography (OCTA) is a promising new noninvasive imaging technique that employs motion contrast imaging to high-resolution volumetric blood flow information generating angiographic images. It compares the differences in backscattered OCT signals between sequential scans. Erythrocyte movement in sequences of B-scans is utilized to map retinal vessels. Also, OCTA is a noninvasive technique that acquires volumetric angiographic information without the usage of dye. The en-face images (OCT angiograms) can then be scrolled outward from the internal limiting membrane to the choroid to visualize the individual vascular plexus and segment the inner retina, outer retina, choriocapillaris, or other areas of interest.[2]

In diabetic retinopathy, OCTA can detect microaneurysms, intraretinal microvascular abnormalities, nonperfusion areas, and neovascularization, and it is able to offer additional information with respect to the localization of these changes. Thus OCTA offers added advantage in detecting microvascular changes even before changes are apparent in the fundoscopic examination.

OCTA has previously been used to describe retinal microvascular lesions in diabetic patients and helps to diagnose macular ischemia.[3] In diabetic patients, macular microvascular changes like asymmetry and enlargement in the foveal avascular zone (FAZ) area, are reported in the literature, in the absence of diabetic retinopathy changes clinically.[4],[5] Quantitative assessments that can be measured in OCTA are, vessel density and perfusion density, which help in better understanding of the pathophysiology, disease activity and help deciding appropriate treatment and follow-up of DR patients.[6]

The aim of this study is to assess the characteristics of foveal microvascular abnormalities in different stages of Diabetic retinopathy. In this study, several OCTA-based macular vascular parameters were analyzed and the results were compared between the eyes without Diabetic Retinopathy, eyes with different stages of diabetic retinopathy i.e., nonproliferative diabetic retinopathy (NPDR), and PDR.


  Materials and Methods Top


An observational cross-sectional study was done to evaluate microvascular changes in diabetic patients attending the retina department of our tertiary care center. The study period was from January 2019 to 2020. The study population included 120 eyes among 72 patients. Majority of study patients were type 2 diabetics. The patients underwent comprehensive ocular examination, including visual acuity, slit-lamp biomicroscopy, fundoscopy, OCT, and OCTA. Diabetic retinopathy grades were based on the Early Treatment Diabetic Retinopathy Study classification.[7] Study eyes were accordingly divided into 3 groups - Group A, B, and C. Each group had forty eyes. Eyes with no frank manifestations of the diabetic retinopathy, neither on clinical examination nor on the common diagnostic tools were included in Group A. While eyes with NPDR changes were included in Group B. And Group C included eyes with PDR.

Inclusion criteria were patients with diabetes mellitus (both type 1 and type 2) with and without diabetic retinopathy. The eyes with diabetic macular edema at any stage of DR and phakic eyes with early cataract changes i.e., grading between NSI to NSII, with media clarity sufficient for good quality OCT/OCTA were included.

Exclusion criteria were eyes with the presence of dense media opacity due to cataract, vitreous hemorrhage, Pseudophakia with dense posterior capsular opacification, macula changes associated with vitreomacular traction, and macular tractional retinal detachment. Eyes that had received previous laser photocoagulation, intravitreal anti-VEGF/triamcinolone injections, and eyes with the history of vitreoretinal surgery in the past were also excluded.

OCT and OCTA were performed to assess the state of patients' neurosensory retina and retinal vasculature. Optical coherence tomographic angiography was performed with a Zeiss CIRRUS™ HD-OCT Model 5000, imaging instrument using the optical microangiography algorithm (Carl Zeiss Meditech). The standard scanning patterns that are available while using ZEISS Angioplex™ OCT angiography include cube scans of 3 mm × 3 mm and 6 mm × 6 mm, along with an increased scan rate of 68,000 A-scans per second and FastTrac™ retinal-tracking technology, for motion correction and reproducible follow-up positioning of scans. The eyes of each participant were scanned with B-scans composed of 1000 A-scans (for Macular Cube 200 × 200) or 1024 A-scans (for Macular Cube 512 × 128). The inner retina was estimated as being the tissue between the inner limiting membrane and an offset from the retinal pigment epithelium of 110 μm. The superficial retinal layer (SRL) was defined as the inner 70% of the inner retina, and the deep retinal layer was the remaining 30% of the inner retina. Scanning results in either a 6 mm × 6 mm/3 mm × 3 mm square cube, similar to the macular 512 × 128/200 × 200 cubes but uses an intensity-based frequency filtering technique to generate images with detailed vasculature.

The FAZ measurements were based on the SRL. The area and perimeter of this zone were calculated, and the circularity index was calculated as 4 πA/P, where A is the area and P is the perimeter. The area contained within the boundary of the FAZ mm2. FAZ perimeter the length of the boundary of the FAZ mm. FAZ Circularity How similar the boundary of the FAZ is to a circle. Values range from 0 to 1. A value of 1 means the FAZ forms a perfect circle while a value near zero means that the boundary of FAZ is very different from a circle. All these calculations are performed with the inbuilt software commercially available on the Cirrus high-definition–OCT with AngioPlex [Figure 1]a.
Figure 1: (a) Nonproliferative diabetic retinopathy eye with altered foveal avascular zone parameters and vessel density, (b) proliferative diabetic retinopathy eye with altered foveal avascular zone parameters and perfusion density

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Vascular density was measured using binary reconstruction of images and was defined as the percentage of the sample area occupied by vessel lumens. The percentage of vessels was further measured in each sector (superior, temporal, inferior, and nasal) based on the Early Treatment Diabetic Retinopathy Study (ETDRS) chart with the foveal center being automatically determined from the relevant OCT data. The inner and outer rings with a diameter of 1 and 2.5 mm centered on the fovea were respectively considered for evaluation representing the central 10 degree of the visual field. Density and perfusion values were assessed using in-built OCTA software and ETDRS chart overlay was used to calculate perfusion density (PD in percentage) and vessel density (VD mm/mm2) in all quadrants around the fovea [Figure 1]b.

Statistical analysis

Statistical analysis was done using SPSS version 21.0. All the data were analyzed by descriptive statistics, such as mean and standard deviation. Independent t-test and Chi-square test were used to compare data between the groups. Multivariate analysis was performed to investigate the correlation of FAZ parameters in various stages of diabetic retinopathy. P < 0.05 was considered statistically significant.


  Results Top


Our study consisted of 8 (12%) patients with type 1 diabetes and 64 (88%) patients with type 2 diabetes [Table 1]. The study included 40 eyes in each group, the male and female sex ratio was comparable in all three groups. The duration of diabetes varied in each group, in groups with no DR 80% were <5 years, group with NPDR 50% between 5 and 10 years, and group with PDR 45% of patients had diabetes greater then15 years. The mean duration of diabetes in the NPDR group was 9.80 ± 6.48 years compared to the PDR group 12.12 ± 6.48 years. The difference in the mean duration between Group B and C was statistically significant (P = 0.048). The common systemic comorbidity associated was hypertension. It was seen in one (4.5%) patient of Group A, 10 (41.6%) in Group B, and 14 (53.8%) in Group C patients. History of Ischemic heart disease was noted in one patient (3.8%) of Group B and 5 (19.2%) in Group C patients, suggesting high cardiovascular risk among diabetes patients with Group C. The late systemic complications like chronic kidney disease were seen in 2 (8.3%) patients among Group B and 4 (15.3%) patients in Group C.
Table 1: Description of demographic and clinical parameters (mean±standard deviation)

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The median LOGMAR visual acuity in the NPDR group was 0.31 ± 0.19 compared to 0.46 ± 0.24 in the PDR group. The P value there was significant between the above two groups (0.046). On further comparison of visual acuity among patients with or without DME, there was no statistically significant difference in both NPDR and PDR groups (P = 0.68) [Table 2]a and [Table 2]b. Incidence of macular edema more in NPDR group is 20 eyes (50%) compared PDR group i.e., 18 eyes (45%). Mean central macular thickness in the NPDR group is 360.63 ± 160.65 microns and 333.38 ± 105.23 microns in the PDR group, thus on comparison P value not significant (0.372). Among them, 8 (20%) eyes in NPDR and 7 (17.5%) eyes in the PDR group eyes had serous macular detachment (SMD). DME leads to moderated visual disturbance in both Groups B and C, but severe vision loss more with lesser incidence of DME due to macular ischemic changes in PDR group in 30% of eyes.
Table 2: (a) Comparison of vision groups for nonproliferative diabetic retinopathy (b) comparison of vision groups for proliferative diabetic retinopathy

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Vascular density is 19.65 ± 0.24 mm/mm2 and perfusion density 36% ± 0.12%, both were altered with no diabetic retinopathy. In NPDR group the results we found were mean FAZ area 0.38 ± 0.16, perimeter 2.91 ± 0.58, circularity 0.59 ± 0.09 compared to PDR group FAZ area 0.48 ± 0.09 and perimeter 3.67 ± 0.82, circularity 0.53 ± 0.08 respectively. On analysis above results, we confirmed significantly altered parameters in PDR group compared to NPDR group. Vascular density mean value in NPDR group 18.89 ± 2.51 in comparison with PDR group 16.59 ± 1.96. The perfusion density mean value is 31.26 ± 7.03 in NPDR group and 23.19 ± 4.35 in PDR group. Thus even vascular density and perfusion density showed a statistically significant difference (0.0001) in different stages of diabetic retinopathy [Table 3].
Table 3: Logarithm of the minimum angle of resolution visual acuity, foveal avascular zone area, perimeter, circularity, vessel density, and perfusion density among Groups A, B, C (mean±standard deviation) and P value of comparison between group B and C

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Among eyes with DME NPDR, FAZ parameters mean area, Perimeter and Circularity were 0.41 ± 0.19 mm2, 2.91 ± 0.59 and 0.61 ± 0.07 respectively while in PDR group Area 0.50 ± 0.09 mm2, Perimeter 4.08 ± 1.03 and Circularity 0.51 ± 0.08, respectively. Quantitative parameters like vascular density and perfusion density in NPDR group 18.60 ± 2.43 and 31.08 ± 9.63 whereas in PDR group VD 16.11 ± 2.46 and PD 21.94 ± 4.62, respectively. Thus P value was significant in all parameters between the above two groups. Among the eyes with SMD, recorded mean values of FAZ metrics like area, perimeter and circularity were comparable between NPDR and PDR group. The vascular density and perfusion density in NPDR group with SMD eyes is 18.60 ± 2.43 and 31.08 ± 9.63. In PDR group VD 16.11 ± 2.46 and PD 21.94 ± 4.62 with SMD eyes [Table 4]. Thus we noted the significant change in vascular density and perfusion density.(P < 0.05) in SMD eyes.
Table 4: Comparison of vessel density and perfusion density changes (mean±standard deviation) in eyes with diabetic macular edema with serous macular detachment in Group B and Group C

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  Discussion Top


According to various population-based studies, the prevalence of DME among patients with type 1 diabetes was between 4.2% and 7.9%. On FAZ analysis, in group A, eyes with no diabetic retinopathy changes parameters FAZ area is 0.26 ± 0.1 mm2, perimeter 2.20 ± 0.52 mm, circularity 0.82 ± 0.04 were comparable with normative data among nondiabetic eyes.[8] In patients with type 2 diabetes, it was between 1.4% and 12.8% of the Asian population.[9] We all know the diabetic macular maculopathy includes ischemic maculopathy along with diabetic macular edema. Current management of DME is based on l SD-OCT-based structural changes but we are not able to distinguish patients with ischemic maculopathy especially if the central retinal thickness is in the normal range.[10] So far the option of evaluating ischemic maculopathy was dependent on fundus fluorescein angiography as a gold standard imaging modality.[11] New imaging modality, OCTA angiography as an alternative noninvasive method of evaluating DME made a significant difference in managing diabetic maculopathy.[12] Yu et al. reported in their study that OCTA is comparable with that of FFA in assessing DMI.[13] The Early Treatment of Diabetic Retinopathy Study clearly mentions the importance of diagnosing macular ischemia as a predictive value for the progression of the disease.[14] Macular ischemic-associated FAZ changes and FAZ parameters measured by OCTA could also be used in the grading of diabetic retinopathy.[15] Many studies have proven ischemic maculopathy cases are usually refractory to either anti-VEGF or macular photocoagulation treatment.[15],[16] Analysis of OCTA FAZ metrics will make a difference in our clinical practice by helping us uncover the eyes with macular ischemia without the need for invasive FFA.

FAZ parameters were quantified by measuring the area A, perimeter P, and circularity index C. In our study all FAZ parameters were within the normal range in eyes with no diabetic retinopathy, similar findings were noted in studies by Goudot et al.[17] Although in a study by Freiberg et al., stated similar results with predominant changes in superficial capillary plexus in comparison to our study, they reported early changes of FAZ were obvious in the deep capillary plexus.[18] When we compared the FAZ parameters between the eyes with no DR, eyes with NPDR, and eyes showing PDR, all the FAZ parameters showed a linear positive correlation with the stage of DR. FAZ parameters were normal in the eyes without DR while they were significantly altered in the eyes with PDR. The mean FAZ area of the SCP increased from 0.25 mm2 in eyes without DR to up to 0.41 mm2 in NPDR with DME and 0.50 mm2 in cases with PDR with DME, eyes with DME showed larger FAZ area compared with eyes without DME. Our results are comparable to study by Dimitrova et al., study which reported a mean FAZ area of 0.51 mm2 in PDR without DME and 0.58 mm2 in cases with DME. A study by Lee et al. has also reported that the mean circularity index and mean FAZ area show a positive correlation with severity of DR.[19] The mean FAZ area size was also found to be inversely associated with visual function in the study by Freiberg et al., our results too showed a similar inverse correlation with respect to visual acuity.[18] Similarly, Arend et al.[20] reported a visual acuity score of 20/50 (0.4 in logmar) consistently in patients with DMI with a FAZ ≥0.55 mm2, which is comparable with our findings PDR group of 0.4 with FAZ area >0.49 ± 0.09 mm2.

When we compared FAZ metrics in eyes with or without DME, eyes with DME showed significantly deranged changes in FAZ metrics. On further subcategorizing eyes with DME cases into those with SMD and those without SMD in both NPDR and PDR groups we found no difference in visual acuity between the groups with or without SMD. Similar results were reported in a study by Hwang et al.[18] However, on the OCTA, FAZ metrics our data analysis revealed very interesting results. Among all FAZ metrics, only VD and PD were more affected in eyes with SMD while the FAZ area showed no change between the eyes with SMD and eyes without SMD. This finding may be due to the altered decreased vessel and perfusion density in eyes showing SMD, It is also reported by Hwang et al., that eyes showing SMD had significantly higher aqueous levels of vascular endothelial growth factor and pigment epithelial-derived factors.[21] These facts may indicate that ischemic retinal conditions are more in eyes with SMD and these eyes could be more prone for early progression of DR. This finding of using VD and PD on OCTA could be used in NPDR to predict higher risk of progression to develop PDR or worsening of PDR. These questions would be best answered by longitudinal studies in the future.

In our cross-sectional study, Quantitative analysis of parafoveal vessel density and perfusion density showed a correlation with the stage of diabetic retinopathy. A study by Schottenhamml reported that VD may predict DR severity with a relatively high sensitivity and specificity.[22] Durbin et al.[6] found that the mean perfusion density for the healthy group in the SRLs was 41, the mean vascular density was 22.5. In our study, we observed a PD of 36 and VD of 19.65 being reduced in diabetes patients' eyes with no evidence of diabetic retinopathy, Similar study reported by Dimitrova et al.[23] Dimitrova et al. also reported similar changes happening simultaneously in deep capillary layers.[23] However, according to the study by Al-Sheikh et al., alterations in vascular density in SCP correlated better with DR severity and their findings were comparable to our results in both NPDR and PDR groups.[24] Identifying eyes of diabetic patients that show lower vascular density in the macula on OCTA can potentially be useful to prognosticate the progression of retinopathy. This would alert the clinician that these patients are at risk of worsening of the DR and hence would require appropriate management of the systemic diabetic status by a multispecialty approach. The well-known factor is, 1-year risk of patients with DMI to develop progressive diabetic retinopathy was found to be almost 42%, which is significantly higher than the individual without DMI.[14] Thus OCTA guides us in diagnosing DMI, which further helps in planning our follow-up and appropriate treatment for eyes at risk.

Limitations of our study

Our study was confined only to the analysis of superficial retinal plexus, due to limitations of software availability. The study involving analysis of the deep capillary plexus and the choriocapillaris will be more informative in understanding the microvascular changes in diabetic retinopathy. Choroidal thickness analysis is recent studies suggest a decreased choroidal perfusion in eyes with diabetic retinopathy. Choroidal thickness was not assessed in our study. Future studies trying to correlate Choroidal thickness with macular changes in diabetic retinopathy may help us to understand the pathogenesis in greater detail. Since the standard normative database of VD, PD, and FAZ values based on ethnicity is not available, it is difficult to compare various published studied, also same parameters being measured using different machines i.e. AngioVue and Cirrus HDOCT may not be comparable. The size of the study was not large enough to account for confounding factors such as glycemic control. Further large-scale studies with the study of various FAZ parameters in a longitudinal study with long-term follow-up are required to validate the correlations that are indicated in our cross-sectional study.


  Conclusion Top


OCTA is a promising noninvasive tool to accurately assess the macular changes in various stages of diabetic retinopathy. It can reveal the underlying microvascular changes which helps in diagnosing ischemic maculopathy apart from diabetic macular edema. Thus FAZ parameters can be used as a biomarker for assessing various degrees of DME and DMI to help predict the progression of disease before its clinical manifestations. OCTA can be used to visualize and quantify the FAZ metric changes early and hence may help us for accurate disease severity and staging than what could be made out clinically. It also helps to prognosticate DR progression, vision, and assists in appropriate patient counseling along with informed treatment decisions. Serial quantitative measurements on OCTA are an added advantage that would avoid the potential risks of Fluorescein sodium dye injection in diabetic patients with end-stage complications. Thus OCTA is a useful noninvasive investigation tool in clinical settings, would certainly help in planning the follow-up, counseling, and choosing the appropriate treatment for eyes at risk.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Korobelnik JF, Do DV, Schmidt-Erfurth U, Boyer DS, Holz FG, Heier JS, et al. Intravitreal aflibercept for diabetic macular edema. Ophthalmology 2014;121:2247-54.  Back to cited text no. 1
    
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Khan HA, Mehmood A, Khan QA, Iqbal F, Rasheed F, et al. A major review of optical coherence tomography angiography. Expert Rev Ophthalmol 2017;12:373-85.  Back to cited text no. 2
    
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Agemy SA, Scripsema NK, Shah CM, Chui T, Garcia PM, Lee JG, et al. Retinal vascular perfusion density mapping using optical coherence tomography angiography in normals and diabetic retinopathy patients. Retina 2015;35:2353-63.  Back to cited text no. 3
    
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Di G, Weihong Y, Xiao Z, Zhikun Y, Xuan Z, Yi Q, et al. A morphological study of the foveal avascular zone in patients with diabetes mellitus using optical coherence tomography angiography. Graefes Arch Clin Exp Ophthalmol 2016;254:873-9.  Back to cited text no. 4
    
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de Carlo TE, Chin AT, Bonini Filho MA, Adhi M, Branchini L, Salz DA, et al. Detection of microvascular changes in eyes of patients with diabetes but not clinical diabetic retinopathy using optical coherence tomography angiography. Retina 2015;35:2364-70.  Back to cited text no. 5
    
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Durbin MK, An L, Shemonski ND, Soares M, Santos T, Lopes M, et al. Quantification of retinal microvascular density in optical coherence tomographic angiography images in diabetic retinopathy. JAMA Ophthalmol 2017;135:370-6.  Back to cited text no. 6
    
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Classification of diabetic retinopathy from fluorescein angiograms. ETDRS report number 11. Early Treatment Diabetic Retinopathy Study Research Group. Ophthalmology. 1991 May;98(5 Suppl):807-22. PMID: 2062514.  Back to cited text no. 7
    
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Falavarjani KG, Shenazandi H, Naseri D, Anvari P, Kazemi P, Aghamohammadi F, et al. Foveal avascular zone and vessel density in healthy subjects: An optical coherence tomography angiography study. J Ophthalmic Vis Res 2018:13:260-5.  Back to cited text no. 8
    
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Virgili G, Menchini F, Casazza G, Hogg R, Das RR, Wang X, et al. Optical coherence tomography (OCT) for detection of macular oedema in patients with diabetic retinopathy. Cochrane Database Syst Rev 2015;1:CD008081.  Back to cited text no. 10
    
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Hemalatha BC, Sathyendranath Shetty B. Analysis of foveal avascular zone in different stages of non/proliferative diabetic retinopathy at a tertiary eye care hospital. Indian J Clin Exp Ophthalmol 2015;1:202-17.  Back to cited text no. 11
    
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de Barros Garcia JM, Isaac DL, Avila M. Diabetic retinopathy and OCT angiography: Clinical findings and future perspectives. Int J Retina Vitreous 2017;3:14.  Back to cited text no. 12
    
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Yu S, Lu J, Cao D, Liu R, Liu B, Li T, et al. The role of optical coherence tomography angiography in fundus vascular abnormalities. BMC Ophthalmol 2016;16:107.  Back to cited text no. 13
    
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Fluorescein angiographic risk factors for progression of diabetic retinopathy. ETDRS report number 13. Early Treatment Diabetic Retinopathy Study Research Group. Ophthalmology 1991;98:834-40.  Back to cited text no. 14
    
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Choi W, Waheed NK, Moult EM, Adhi M, Lee B, De Carlo T, et al. Ultrahigh speed swept source optical coherence tomography angiography of retinal and choriocapillaris alterations in diabetic patients with and without retinopathy. Retina 2017;37:11-21.  Back to cited text no. 15
    
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Diabetic Retinopathy Clinical Research Network, Wells JA, Glassman AR, Ayala AR, Jampol LM, Aiello LP, et al. Aflibercept, bevacizumab, or ranibizumab for diabetic macular edema. N Engl J Med 2015;372:1193-203.  Back to cited text no. 16
    
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Goudot MM, Sikorav A, Semoun O, Miere A, Jung C, Courbebaisse B, Srour M, et al. Parafoveal OCT angiography features in diabetic patients without clinical diabetic retinopathy: A qualitative and quantitative analysis. Hindawi J Ophthalmol 2017;2017:14.  Back to cited text no. 17
    
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Freiberg FJ, Pfau M, Wons J, Wirth MA, Becker MD, Michels S, et al. Optical coherence tomography angiography of the foveal avascular zone in diabetic retinopathy. Graefes Arch Clin Exp Ophthalmol 2016;254:1051-8.  Back to cited text no. 18
    
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Lee H, Lee M, Chung H, Kim HC. Quantification of retinal vessel tortuosity in diabetic retinopathy using optical coherence tomography angiography. Retina 2018;38:976-85.  Back to cited text no. 19
    
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Hwang HB, Jee D, Kwon JW. Characteristics of diabetic macular edema patients with serous retinal detachment. Medicine (Baltimore) 2019;98:e18333.  Back to cited text no. 21
    
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Schottenhamml J, Moult EM, Ploner S, Lee B, Novais EA, Cole E, et al. An automatic, intercapillary area-based algorithm for quantifying diabetes-related capillary dropout using optical coherence tomography angiography. Retina 2016;36 Suppl 1:S93-S101.  Back to cited text no. 22
    
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Dimitrova G, Chihara E, Takahashi H, Amano H, Okazaki K. Quantitative retinal optical coherence tomography angiography in patients with diabetes without diabetic retinopathy. Invest Ophthalmol Vis Sci 2017;58:190-6.  Back to cited text no. 23
    
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Al-Sheikh M, Akil H, Pfau M, Sadda SR. Swept-source OCT angiography imaging of the foveal avascular zone and macular capillary network density in diabetic retinopathy. Invest Ophthalmol Vis Sci 2016;57:3907-13.  Back to cited text no. 24
    


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