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Deep learning algorithms for detection of diabetic retinopathy in retinal fundus photographs: A systematic review and meta-analysis.
Islam, MM, Yang, HC, Poly, TN, Jian, WS, Jack Li, YC
Computer methods and programs in biomedicine. 2020;:105320
Abstract
BACKGROUND Diabetic retinopathy (DR) is one of the leading causes of blindness globally. Earlier detection and timely treatment of DR are desirable to reduce the incidence and progression of vision loss. Currently, deep learning (DL) approaches have offered better performance in detecting DR from retinal fundus images. We, therefore, performed a systematic review with a meta-analysis of relevant studies to quantify the performance of DL algorithms for detecting DR. METHODS A systematic literature search on EMBASE, PubMed, Google Scholar, Scopus was performed between January 1, 2000, and March 31, 2019. The search strategy was based on the Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA) reporting guidelines, and DL-based study design was mandatory for articles inclusion. Two independent authors screened abstracts and titles against inclusion and exclusion criteria. Data were extracted by two authors independently using a standard form and the Quality Assessment of Diagnostic Accuracy Studies (QUADAS-2) tool was used for the risk of bias and applicability assessment. RESULTS Twenty-three studies were included in the systematic review; 20 studies met inclusion criteria for the meta-analysis. The pooled area under the receiving operating curve (AUROC) of DR was 0.97 (95%CI: 0.95-0.98), sensitivity was 0.83 (95%CI: 0.83-0.83), and specificity was 0.92 (95%CI: 0.92-0.92). The positive- and negative-likelihood ratio were 14.11 (95%CI: 9.91-20.07), and 0.10 (95%CI: 0.07-0.16), respectively. Moreover, the diagnostic odds ratio for DL models was 136.83 (95%CI: 79.03-236.93). All the studies provided a DR-grading scale, a human grader (e.g. trained caregivers, ophthalmologists) as a reference standard. CONCLUSION The findings of our study showed that DL algorithms had high sensitivity and specificity for detecting referable DR from retinal fundus photographs. Applying a DL-based automated tool of assessing DR from color fundus images could provide an alternative solution to reduce misdiagnosis and improve workflow. A DL-based automated tool offers substantial benefits to reduce screening costs, accessibility to healthcare and ameliorate earlier treatments.
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Assessment of retinal vascular network in amnestic mild cognitive impairment by optical coherence tomography angiography.
Criscuolo, C, Cennamo, G, Montorio, D, Carotenuto, A, Strianese, A, Salvatore, E, Tranfa, F, Cennamo, G, Lanzillo, R, Brescia Morra, V
PloS one. 2020;(6):e0233975
Abstract
OBJECTIVE To assess the presence of retinal vascular network abnormalities in amnestic mild cognitive impairment (aMCI) patients and healthy subjects (HS) through optical coherence tomography angiography (OCTA). METHODS OCTA and SD-OCT were performed in aMCI patients and cognitive normal HS. A complete neuropsychological evaluation was performed. Differences in vessel density (VD) in each retinal vascular plexus and in foveal avascular zone (FAZ) were evaluated with linear mixed model after correction for age, sex and disease duration. RESULTS Twenty-seven aMCI patients (10 Single domain aMCI, 17 Multidomain aMCI) and 29 HS were enrolled. aMCI patients showed a statistically significant reduced VD in superficial capillary plexus (SCP), deep capillary plexus (DCP) and an increased FAZ compared to controls. When aMCI patients were divided in single domain (SD) and multiple domains (MD) aMCI, SD aMCI showed no VD differences in SCP, DCP and Radial Peripapillary Capillary, while the FAZ area was significantly larger compared to controls. In MD aMCI, VD values were lower and FAZ was increased compared to controls. Comparing both aMCI groups, MD aMCI showed a significant reduction in VD values of SCP. No correlation was found between mini mental state examination (MMSE) scores and OCTA parameters. CONCLUSIONS OCTA is able to detect changes in retinal microvascular network in early cognitive deficits and, the most sensitive alteration seems to be the enlargement of the FAZ. This non-invasive tool provides useful information on retinal involvement patterns in MCI diagnosis and follow up. Vascular network impairment seems to be related to the number of domains affected and not to MMSE.
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Interaction Between the Distribution of Diabetic Retinopathy Lesions and the Association of Optical Coherence Tomography Angiography Scans With Diabetic Retinopathy Severity.
Ashraf, M, Sampani, K, Rageh, A, Silva, PS, Aiello, LP, Sun, JK
JAMA ophthalmology. 2020;(12):1291-1297
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Abstract
IMPORTANCE Studies have not yet determined whether the distribution of lesions in the retinal periphery alters the association between the severity of diabetic retinopathy (DR) and macular vessel density. OBJECTIVE To evaluate the association of DR lesion distribution with optical coherence tomography angiography (OCTA) metrics and DR severity. DESIGN, SETTING, AND PARTICIPANTS This cross-sectional observational study was conducted at a tertiary care center for diabetic eye disease among 225 patients with type 1 or 2 diabetes who had undergone imaging between February 15, 2016, and December 31, 2019. EXPOSURES Optical coherence tomography angiography 3 × 3-mm macular scans and ultra-widefield color imaging. MAIN OUTCOMES AND MEASURES Optical coherence tomography angiography vessel density in the superficial capillary plexus, intermediate capillary plexus, and deep capillary plexus and choriocapillaris flow density. The severity of DR and the predominantly peripheral lesions (PPL) were evaluated from ultra-widefield color imaging. RESULTS The study evaluated 352 eyes (225 patients; 125 men [55.6%]; mean [SD] age, 52.1 [15.1] years), of which 183 eyes (52.0%) had mild nonproliferative diabetic retinopathy (NPDR), 71 eyes (20.2%) had moderate NPDR, and 98 eyes (27.8%) had severe NPDR or proliferative diabetic retinopathy (PDR). In eyes with no PPL (209 [59.4%]), the mean (SD) vessel density in the superficial capillary plexus (mild NPDR, 38.1% [4.7%]; moderate NPDR, 36.4% [4.6%]; severe NPDR or PDR, 34.1% [4.1%]; P < .001) and the deep capillary plexus (mild NPDR, 45.8% [3.0%]; moderate NPDR, 45.8% [2.2%]; severe NPDR or PDR, 44.5% [1.9%]; P = .002), as well as the mean (SD) choriocapillaris flow density (mild NPDR, 69.7% [6.2%]; moderate NPDR, 67.6% [5.6%]; severe NPDR or PDR, 67.1% [5.6%]; P = .01), decreased with increasing DR severity. These associations remained statistically significant even after correcting for age, signal strength index, spherical equivalent, duration of diabetes, type of diabetes, and correlation between eyes of the same patient. In eyes with PPL (143 [40.6%]), mean (SD) vessel density in the superficial capillary plexus (mild NPDR, 34.1% [4.1%]; moderate NPDR, 35.2% [4.1%]; severe NPDR or PDR, 36.0% [4.3%]; P = .42) and the deep capillary plexus (mild NPDR, 44.5% [1.7%]; moderate NPDR, 45.4% [1.4%]; severe NPDR or PDR, 44.9% [1.5%]; P = .81), as well as the mean (SD) choriocapillaris flow density (mild NPDR, 67.1% [5.6%]; moderate NPDR, 69.3% [4.6%]; severe NPDR or PDR, 68.3% [5.6%]; P = .49), did not appear to change with increasing DR severity. CONCLUSIONS AND RELEVANCE These results suggest that central retinal vessel density is associated with DR severity in eyes without, but not with, PPL. These findings suggest a potential need to stratify future optical coherence tomography angiography studies of eyes with DR by the presence or absence of PPL. If DR onset and worsening are associated with the location of retinal nonperfusion, assessment of global retinal nonperfusion using widefield angiography may improve the ability to evaluate DR severity and risk of DR worsening over time.
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Vitreoretinal Interface Slab in OCT Angiography for Detecting Diabetic Retinal Neovascularization.
Hirano, T, Hoshiyama, K, Hirabayashi, K, Wakabayashi, M, Toriyama, Y, Tokimitsu, M, Murata, T
Ophthalmology. Retina. 2020;(6):588-594
Abstract
PURPOSE To compare neovascularization identified in proliferative diabetic retinopathy (PDR) eyes by widefield swept-source (SS) OCT angiography (OCTA) using vitreoretinal interface (VRI) slab images, composed by automated and manual segmentation, with that identified by fluorescein angiography (FA). DESIGN Retrospective study. PARTICIPANTS Forty-two eyes of 30 treatment-naïve PDR patients who visited the outpatient clinic of the Department of Ophthalmology, Shinshu University, from June 2018 through October 2019. METHODS All patients underwent comprehensive ophthalmologic examinations, including SS-OCTA and FA. MAIN OUTCOME MEASURES Neovascularization detected by en face SS-OCTA 15 × 15-mm VRI slab images and by FA in the same 15 × 15-mm areas were compared in terms of number and structure. RESULTS Among 100 neovascularizations detected by FA, 73 also were visualized as neovascularization in SS-OCTA VRI slab images using automated segmentation. The sensitivity of VRI slab images for detecting neovascularization was 73%. Among the remaining 27 neovascularizations detected only by FA, but not by VRI slab, 15 were intraretinal microvascular abnormalities with fluorescence leakage, 1 was a diabetic papillopathy, and 11 were flat neovascularizations on the internal limiting membrane surface that were missed because of segmentation error. Conversely, among the 98 neovascularizations detected on VRI slab images, 25 were not detected as neovascularizations by FA. They included 9 small neovascularizations that exhibited too little leakage on FA and 16 false-positive results that were the result of segmentation errors. After reconstruction of SS-OCTA VRI slab images by means of manual segmentation, the sensitivity of VRI slab images for detecting neovascularizations increased to 84%. CONCLUSIONS The efficacy of SS-OCTA VRI slab images for detecting neovascularizations in PDR was comparable with that of FA. Swept-source OCTA VRI slab images may be better than FA for identifying intraretinal microvascular abnormalities and diabetic papillopathy from neovascularizations. Notably, however, FA and SS-OCTA VRI slab images demonstrated differences in identification efficacy in cases of small and flat neovascularizations. Further exploration of SS-OCTA technology is warranted to address this issue.
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Evaluation of different Swept'Source optical coherence tomography angiography (SS-OCTA) slabs for the detection of features of diabetic retinopathy.
Tian, M, Wolf, S, Munk, MR, Schaal, KB
Acta ophthalmologica. 2020;(4):e416-e420
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PURPOSE To compare different Swept-Source optical coherence tomography angiography (SS-OCTA) slabs for the detection of features of diabetic retinopathy (DR), to find the most suitable slab for grading. METHODS Retrospective cross-sectional study. Consecutive patients with DR were evaluated using SS-OCTA. The central 12 × 12 mm scan was used to generate the retinal, superficial and deep slab. The grading results of the slabs were then compared to determine if one specific slab is superior to detect respective features. RESULTS A total of 348 eyes (190 patients; mean age 58.1 ± 14.5 years) were graded for features of DR. The retinal slab detected most frequently MAs and IRMAs, however with no significant difference compared to the superficial slab (p = 0.93 and p = 0.93, respectively). Small capillary dropout was most frequently found on the superficial slab, but there was no significant difference compared with the retinal (p = 0.78) and deep slab (p = 0.45). The only statistically significant difference was found for large capillary dropout, where the retinal and superficial slab showed a higher detection rate compared with the deep slab (p ≤ 0.0001 and p = 0.001, respectively). CONCLUSIONS The superficial and retinal slabs are equally suitable for grading with no statistically significant difference in the detection rate of the diabetic features examined.
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Longitudinal Panretinal Leakage and Ischemic Indices in Retinal Vascular Disease after Aflibercept Therapy: The PERMEATE Study.
Figueiredo, N, Srivastava, SK, Singh, RP, Babiuch, A, Sharma, S, Rachitskaya, A, Talcott, K, Reese, J, Hu, M, Ehlers, JP
Ophthalmology. Retina. 2020;(2):154-163
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PURPOSE To characterize the longitudinal panretinal retinal vascular dynamics in diabetic macular edema (DME) and retinal vein occlusion (RVO) over a 12-month period while being treated with intravitreal aflibercept injections (IAIs). DESIGN Prospective open-label study (clinicaltrials.gov identifier, NCT02503540). PARTICIPANTS Thirty-one treatment-naive eyes with foveal-involving retinal edema secondary to DME and RVO. METHODS Participants received 2 mg IAI every 4 weeks for the first 6 months, followed by 2 mg every 8 weeks. Ultra-widefield fluorescein angiography (UWFA; California Optos [Optos, Dunfermline, United Kingdom]) and spectral-domain OCT (Cirrus; Zeiss, Oberkochen, Germany) scans were obtained and analyzed using a novel quantitative assessment platform. Visual acuity, central subfield thickness, and adverse events also were collected. MAIN OUTCOME MEASURES The primary end point was the mean change in panretinal leakage index at month 12 from baseline as measured by UWFA. RESULTS Mean age was 67.1 years. At month 12, visual acuity significantly improved by a mean of 18.4±21.4 letters (P < 0.0001), and central subfield thickness also improved significantly, with a mean reduction of 301.3±250.3 μm (P < 0.0001). Mean panretinal leakage index improved significantly, decreasing from 3.4% at baseline to 0.5% at month 6 (P <0.0001) and 0.4% at month 12 (P < 0.0001). Panretinal ischemic index did not demonstrate any significant change but showed a nonsignificant increase from 5.5% at baseline to 6.1% at month 6 (P = 0.315) and 8.7% at month 12 (P = 0.193). Eyes with DME showed a decrease in leakage index from 3.5±2.7% at baseline to 1.6±0.8% at month 12 (P = 0.018) and overall stability in ischemic index from 5.0±4.1% at baseline to 4.7±3.5% at month 12 (P = 0.689). Participants with RVO showed a decrease in leakage index from 3.3±1.1% at baseline to 0.02±0.03% at 12 months (P < 0.0001) and a nonsignificant increase in ischemic index from 5.9±4.5% at baseline to 12.6±9.8% at month 12 (P = 0.172). CONCLUSIONS Intravitreal aflibercept injections resulted in a dramatic reduction in panretinal leakage index. Panretinal ischemic index did not improve and trended toward worsening.
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Influence of Metabolic Parameters and Treatment Method on OCT Angiography Results in Children with Type 1 Diabetes.
Wysocka-Mincewicz, M, Baszyńska-Wilk, M, Gołębiewska, J, Olechowski, A, Byczyńska, A, Hautz, W, Szalecki, M
Journal of diabetes research. 2020;:4742952
Abstract
AIM: To evaluate the influence of metabolic parameters and the treatment method in children with type 1 diabetes (T1D) on the optical coherence tomography angiography (OCTA) results as early markers of diabetic retinopathy (DR). Material and Methods. This prospective study enrolled 175 consecutive children with T1D. OCTA was performed using AngioVue (Avanti, Optovue). Whole superficial capillary vessel density (wsVD), fovea superficial vessel density (fsVD), parafovea superficial vessel density (psVD), whole deep vessel density (wdVD), fovea deep vessel density (fdVD), parafovea deep vessel density (pdVD), foveal thickness (FT), parafoveal thickness (PFT), and foveal avascular zone (FAZ) in superficial plexus were evaluated and analyzed in relation to individual characteristics, i.e., sex, weight, height, body mass index (BMI), and metabolic factors: current and mean value of glycated hemoglobin A1c (HbA1c). Furthermore, the analysis concerned the diabetes duration, age at the T1D onset, and type of treatment-multiple daily insulin injections (MDI) or continuous subcutaneous insulin infusion (CSII). RESULTS In the study group, we did not identify any patient with DR in fundus ophthalmoscopy. Age at the onset of diabetes correlated negatively with FAZ (r = -0.17, p < 0.05). The higher level of HbA1c corresponded to a decrease of wsVD (r = -0.13, p < 0.05). We found significantly lower fsVD (32.25 ± .1 vs. 33.98 ± .1, p < 0.01), wdVD (57.87 ± .1 vs. 58.64 ± .9, p < 0.01), and pdVD (60.60 ± .2 vs. 61.49 ± .1, p < 0.01) and larger FAZ area (0.25 ± .1 vs. 0.23 ± .1, p < 0.05) in the CSII vs. MDI group. CONCLUSION The metabolic parameters, age of the onset of diabetes, and treatment method affected the OCTA results in children with T1D. Further studies and observation of these young patients are needed to determine if these findings are important for early detection of DR or predictive of future DR severity.
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Relationship Between Retinal Fractal Dimension and Nonperfusion in Diabetic Retinopathy on Ultrawide-Field Fluorescein Angiography.
Fan, W, Nittala, MG, Fleming, A, Robertson, G, Uji, A, Wykoff, CC, Brown, DM, van Hemert, J, Ip, M, Wang, K, et al
American journal of ophthalmology. 2020;:99-106
Abstract
PURPOSE To correlate fractal dimension (FD) of the retinal vasculature with the extent of retinal nonperfusion area in diabetic retinopathy (DR) on ultrawide-field fluorescein angiography (FA). DESIGN Cross-sectional study. METHODS Baseline Optos 200Tx ultrawide-field FA images of 80 eyes with DR from the DAVE (NCT01552408) and RECOVERY (NCT02863354) studies were stereographically projected at the Doheny Image Reading Center. The retinal vasculature was extracted from an early-phase FA frame by exploiting the elongated nature of the vessels and then skeletonized for calculation of FD using a box-counting method. The nonperfusion area was delineated by 2 independent, reading center-certified graders who were masked to the study groups and who were using a standardized protocol and then computed in millimeters squared. RESULTS While no difference in FD was observed for the entire retina in DR compared with normal control subjects, a significantly smaller FD was found in the far-periphery of the DR eyes (P < .001). FD for the entire retina was negatively associated with global nonperfusion area (R = -0.44; P < .001), and this relationship was also present within the 3 concentric retinal zones (posterior: R = -0.31, P = .016; midperiphery: R = -0.35, P = .007; and far periphery: R = -0.31, P = .015). CONCLUSIONS Peripheral FD on ultrawide-field FA is reduced in DR eyes compared with normal eyes and is correlated with severity of retinal nonperfusion. FD can be calculated automatically without the need for correction of peripheral distortion, and therefore it may prove to be a useful surrogate biomarker when precise quantification of nonperfusion is not feasible.
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Changes in choroidal vascular parameters following pan-retinal photocoagulation using swept-source optical coherence tomography.
Kim, JT, Park, N
Graefe's archive for clinical and experimental ophthalmology = Albrecht von Graefes Archiv fur klinische und experimentelle Ophthalmologie. 2020;(1):39-47
Abstract
BACKGROUND To assess the effect of pan-retinal photocoagulation (PRP) on choroidal vascular parameters in eyes with advanced diabetic retinopathy (DR). METHODS Forty patients (65 eyes) with severe nonproliferative DR or proliferative DR who underwent PRP were included. Changes in choroidal vascular parameters were assessed at 3, 6, and 12 months after PRP by using swept-source optical coherence tomography (OCT) and OCT angiography and were compared with baseline values. RESULTS Choroidal vascularity index (CVI) significantly decreased from 66.27% ± 1.55% at baseline to 65.85% ± 1.61%, 65.77% ± 1.29%, and 65.74% ± 1.60% at 3, 6, and 12 months after PRP, respectively. The ratio of luminal area to stromal area (L/S ratio) also significantly decreased from 1.98 ± 0.15 at baseline to 1.94 ± 0.14, 1.95 ± 0.13, and 1.93 ± 0.14 at 3, 6, and 12 months after PRP, respectively. The subfoveal choroidal thickness (SFCT) similarly showed a significant decrease from 319.50 ± 56.64 μm at baseline to 299. 07 ± 51.14 μm, 294.70 ± 58.96 μm, and 280.93 ± 53.57 μm at 3, 6, and 12 months after PRP, respectively. However, the choriocapillaris vessel density in both the fovea and parafovea showed no significant differences following PRP. CONCLUSION Eyes with advanced DR showed a significant reduction in CVI, L/S ratio, and SFCT over 12 months after PRP treatment.
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Characteristic distribution of microaneurysms and capillary dropouts in diabetic macular edema.
Takamura, Y, Yamada, Y, Noda, K, Morioka, M, Hashimoto, Y, Gozawa, M, Matsumura, T, Inatani, M
Graefe's archive for clinical and experimental ophthalmology = Albrecht von Graefes Archiv fur klinische und experimentelle Ophthalmologie. 2020;(8):1625-1630
Abstract
PURPOSE To investigate the distribution pattern of microaneurysms (MAs) and capillary dropouts (CDOs) related to retinal thickness in patients with diabetic macular edema (DME). METHODS We designed a cross-sectional observational study in which we manually merged fluorescein angiography and optical coherence tomography (OCT) map and located MAs and CDOs areas. The density of MAs, the width and the length of circumference of CDOs, and the number of MAs adjacent to CDOs were compared between highly thickened (white area (WA) in OCT map) and border areas (red area (RA)). RESULTS We examined 115 eyes of 115 patients with DME. The density of MAs in RA (1.086 ± 0.616) was significantly higher than that in WA (0.8601 ± 1.086) (p = 0.002). The MA rates adjacent to CDOs in WA and RA were 79.1% and 80.7%, respectively. In the RA, the size of CDO adjacent to MAs was smaller (p = 0.013), but its circumference was longer (p = 0.018), and the number of MAs adjacent to CDOs was larger than those in WA (p = 0.002). The total length of circumference of CDOs was significantly correlated with the number of MAs adjacent to CDOs in WA (p = 0.011, R2 = 0.68) and RA (p = 0.008, R2 = 0.81). CONCLUSION Smaller but more CDOs with longer circumference adjacent to MAs contribute to the higher density of MAs in the surrounding areas of DME.