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Capillary density and caliber as assessed by optical coherence tomography angiography may be significant predictors of diabetic retinopathy severity.
Kushner-Lenhoff, S, Kogachi, K, Mert, M, Chu, Z, Shahidzadeh, A, Palejwala, NV, Wolfe, J, Itty, S, Drenser, KA, Capone, A, et al
PloS one. 2022;(1):e0262996
Abstract
PURPOSE To validate retinal capillary density and caliber associations with diabetic retinopathy (DR) severity in different clinical settings. METHODS This cross-sectional study assessed retinal capillary density and caliber in the superficial retinal layer of 3-mm OCTA scans centered on the fovea. Images were collected from non-diabetic controls and subjects with mild or referable DR (defined DR worse than mild DR) between February 2016 and December 2019 at secondary and tertiary eye care centers. Vessel Skeleton Density (VSD), a measure of capillary density, and Vessel Diameter Index (VDI), a measure of vascular caliber, were calculated from these images. Discriminatory performance of VSD and VDI was evaluated using multivariable logistic regression models predicting DR severity with adjustments for sex, hypertension, and hyperlipidemia. Area under the curve (AUC) was estimated. Model performance was evaluated in two different cohorts. RESULTS This study included 594 eyes from 385 subjects. Cohort 1 was a training cohort of 509 eyes including 159 control, 155 mild non-proliferative DR (NPDR) and 195 referable DR eyes. Cohort 2 was a validation cohort consisting of 85 eyes including 16 mild NPDR and 69 referable DR eyes. In Cohort 1, addition of VSD and VDI to a model using only demographic data significantly improved the model's AUC for discrimination of eyes with any DR severity from controls (0.91 [95% CI, 0.88-0.93] versus 0.80 [95% CI, 0.76-0.83], p < 0.001) and eyes with referable DR from mild NPDR (0.90 [95% CI, 0.86-0.93] versus 0.69 [95% CI, 0.64-0.75], p < 0.001). The transportability of this regression model was excellent when implemented in Cohort 2 for the referable DR versus mild NPDR comparison. The odds ratio of having any DR compared to control subjects, and referable DR compared to mild DR decreased by 15% (95% CI: 12-18%), and 13% (95% CI: 10-15%), respectively, for every 0.001 unit increase in VSD after adjusting for comorbidities. CONCLUSION OCTA-derived capillary density has real world clinical value for rapidly assessing DR severity.
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Analysis of Progressive Neovascularization in Diabetic Retinopathy Using Widefield OCT Angiography.
Shiraki, A, Sakimoto, S, Eguchi, M, Kanai, M, Hara, C, Fukushima, Y, Nishida, K, Kawasaki, R, Sakaguchi, H, Nishida, K
Ophthalmology. Retina. 2022;(2):153-160
Abstract
PURPOSE To document enlarged neovascularization elsewhere (NVE) quantitatively and morphologically using widefield swept-source (SS) OCT angiography (OCTA) with vitreoretinal interface (VRI) slab images. DESIGN Retrospective, observational imaging study. PARTICIPANTS The study included 46 NVE examples in 25 eyes of 21 consecutive patients who demonstrated severe proliferative diabetic retinopathy with NVE between March 2018 and June 2020 at Osaka University Hospital. METHODS All patients underwent ophthalmologic examination, including ultra-widefield fluorescein angiography and widefield SS OCTA scans. MAIN OUTCOME MEASURES We evaluated the area and the vascular density (VD) of NVE lesions detected on five 12 × 12-mm2 or two 15 × 9-mm2 SS OCTA panoramic VRI slab images obtained at the first and final visits. RESULTS At baseline, the mean NVE area on OCTA was 1.85 ± 2.81 mm2, and the VD of the NVE lesions was 73.9 ± 14.6%. At the final visit, the mean NVE area on OCTA was 2.14 ± 3.14 mm2, and the mean VD of the NVE lesions was 65.3 ± 17.1%. The average NVE size change (square millimeters per month) was associated significantly with the ischemic index (P = 0.009). Growth of NVE area was classified into 2 patterns: round (61.8%) and ramified (38.2%). The round group tended to have a larger ischemic index at baseline than the ramified group (P = 0.0375). CONCLUSIONS We quantified the size and density of NVE lesions over time. The NVE size increase was associated significantly with the severity of ischemic changes. Furthermore, the round growth pattern was correlated significantly with the ischemic index. These findings suggest that the morphologic features of NVE are associated with more severe ischemia.
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Imaging the eye and its relevance to diabetes care.
Quinn, N, Jenkins, A, Ryan, C, Januszewski, A, Peto, T, Brazionis, L
Journal of diabetes investigation. 2021;(6):897-908
Abstract
Diabetes is a major cause of vision loss globally, yet this devastating complication is largely preventable. Early detection and treatment of diabetic retinopathy necessitates screening. Ocular imaging is widely used clinically, both for the screening and management of diabetic retinopathy. Common eye conditions, such as glaucoma, cataracts and retinal vessel thrombosis, and signs of systemic conditions, such as hypertension, are frequently revealed. As well as imaging by a skilled clinician during an eye examination, non-ophthalmic clinicians, such as general practitioners, endocrinologists, nurses and trained health workers, can also can carry out diabetic eye screening. This process usually comprises local imaging with remote grading, mostly human grading. However, grading incorporating artificial intelligence is emerging. In a clinical research context, retinal vasculature analyses using semi-automated software in many populations have identified associations between retinal vessel geometry, such as vessel caliber, and the risk of diabetic retinopathy and other chronic complications of type 1 and type 2 diabetes. Similarly, evaluation of corneal nerves by corneal confocal microscopy is revealing diabetes-related abnormalities, and associations with and predictive power for other chronic diabetes complications. As yet, the value of retinal vessel geometry and corneal confocal microscopy measures at an individual level is uncertain. In this article, targeting non-ocular clinicians and researchers, we review existent and emerging ocular imaging and grading tools, including artificial intelligence, and their associations between ocular imaging findings and diabetes and its chronic complications.
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Diabetic vascular hyperpermeability: optical coherence tomography angiography and functional loss assessments of relationships among retinal vasculature changes.
Arima, M, Nakao, S, Kaizu, Y, Wada, I, Yamaguchi, M, Fujiwara, K, Akiyama, M, Stitt, AW, Sonoda, KH
Scientific reports. 2021;(1):4185
Abstract
Our study assessed the influence of vascular permeability on vascular flow density (FD)-correlated retinal sensitivity (RS) in DR. In this cross-sectional, prospective, consecutive study, RS in the extrafoveal macula of DR patient was measured by microperimetry. FD was measured in the total, superficial, and deep capillary plexus layers (TCP, SCP, and DCP) by optical coherence tomography angiography. All measurement points were classified into four categories according to intensity of fluorescein leakage and FD, and the RS reduction was compared. A stratified analysis by retinal thickness (RT) was also performed. Fourteen eyes (14 patients) were enrolled. FDs at 207 RS measurement points were analyzable. For TCP, SCP and DCP, the leakage did not decrease RS at points where FD was maintained. The greater the leakage, the smaller the RS reduction at points with low FD in TCP (P = .020). Points with high leakage showed a significant smaller RS reduction than points with low leakage (P = .001 for TCP, P = .040 for SCP, and P = .046 for DCP) only in areas with low RT and low FD. Our results suggested that vascular hyperpermeability may inhibit the RS reduction in the non-edematous ischemic diabetic retina.
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Comparison of widefield swept-source optical coherence tomography angiography with ultra-widefield colour fundus photography and fluorescein angiography for detection of lesions in diabetic retinopathy.
Cui, Y, Zhu, Y, Wang, JC, Lu, Y, Zeng, R, Katz, R, Vingopoulos, F, Le, R, Laíns, I, Wu, DM, et al
The British journal of ophthalmology. 2021;(4):577-581
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Abstract
AIMS: To compare widefield swept-source optical coherence tomography angiography (WF SS-OCTA) with ultra-widefield colour fundus photography (UWF CFP) and fluorescein angiography (UWF FA) for detecting diabetic retinopathy (DR) lesions. METHODS This prospective, observational study was conducted at Massachusetts Eye and Ear from December 2018 to October 2019. Proliferative DR, non-proliferative DR and diabetic patients with no DR were included. All patients were imaged with a WF SS-OCTA using a Montage 15×15 mm scan. UWF CFP and UWF FA were taken by a 200°, single capture retinal imaging system. Images were independently evaluated for the presence or absence of DR lesions including microaneurysms (MAs), intraretinal microvascular abnormalities (IRMAs), neovascularisation elsewhere (NVE), neovascularisation of the optic disc (NVD) and non-perfusion areas (NPAs). All statistical analyses were performed using SPSS V.25.0. RESULTS One hundred and fifty-two eyes of 101 participants were included in the study. When compared with UWF CFP, WF SS-OCTA was found to be superior in detecting IRMAs (p<0.001) and NVE/NVD (p=0.007). The detection rates of MAs, IRMAs, NVE/NVD and NPAs in WF SS-OCTA were comparable with UWF FA images (p>0.05). Furthermore, when we compared WF SS-OCTA plus UWF CFP with UWF FA, the detection rates of MAs, IRMAs, NVE/NVD and NPAs were identical (p>0.005). Agreement (κ=0.916) between OCTA and FA in classifying DR was excellent. CONCLUSION WF SS-OCTA is useful for identification of DR lesions. WF SS-OCTA plus UWF CFP may offer a less invasive alternative to FA for DR diagnosis.
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Obstructive sleep apnea and the retina: a review.
Nakayama, LF, Tempaku, PF, Bergamo, VC, Polizelli, MU, Santos da Cruz, NF, Bittencourt, LRA, Regatieri, CVS
Journal of clinical sleep medicine : JCSM : official publication of the American Academy of Sleep Medicine. 2021;(9):1947-1952
Abstract
CITATION This review's objective was to synthesize the literature on the repercussions of obstructive sleep apnea (OSA) in the retinal vascular system. Two independent investigators conducted a search using the MEDLINE/PubMed database using the following terms: sleep apnea syndrome, obstructive sleep apnea, retina, vascular tortuosity, central serous chorioretinopathy, diabetes mellitus, and subfoveal choroidal thickness. Patients with OSA present increased vascular tortuosity compared with patients without OSA, decreased parafoveal and peripapillary vessel density, and increased retinal vein occlusion incidence. In central serous chorioretinopathy patients and patients who are poor responders to intravitreal anti-VEGF (-vascular endothelial growth factor) treatment for macular edema, OSA is more frequent. Macular choroidal thickness alterations are controversial, and OSA may worsen diabetic maculopathy, thus being a risk factor for diabetic retinopathy, proliferative diabetic retinopathy, and macular edema. OSA is a prevalent syndrome with many systemic vascular changes. The retina and choroid are the most affected ocular structures, with primarily vascular changes. New noninvasive technologies such as optical coherence tomography and optical coherence tomography angiography could help to better understand retinal structures and help clarify the ophthalmological repercussions of OSA. CITATION Nakayama LF, Tempaku PF, Bergamo VC, et al. Obstructive sleep apnea and the retina: a review. J Clin Sleep Med. 2021;17(9):1947-1952.
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Artificial intelligence velocimetry and microaneurysm-on-a-chip for three-dimensional analysis of blood flow in physiology and disease.
Cai, S, Li, H, Zheng, F, Kong, F, Dao, M, Karniadakis, GE, Suresh, S
Proceedings of the National Academy of Sciences of the United States of America. 2021;(13)
Abstract
Understanding the mechanics of blood flow is necessary for developing insights into mechanisms of physiology and vascular diseases in microcirculation. Given the limitations of technologies available for assessing in vivo flow fields, in vitro methods based on traditional microfluidic platforms have been developed to mimic physiological conditions. However, existing methods lack the capability to provide accurate assessment of these flow fields, particularly in vessels with complex geometries. Conventional approaches to quantify flow fields rely either on analyzing only visual images or on enforcing underlying physics without considering visualization data, which could compromise accuracy of predictions. Here, we present artificial-intelligence velocimetry (AIV) to quantify velocity and stress fields of blood flow by integrating the imaging data with underlying physics using physics-informed neural networks. We demonstrate the capability of AIV by quantifying hemodynamics in microchannels designed to mimic saccular-shaped microaneurysms (microaneurysm-on-a-chip, or MAOAC), which signify common manifestations of diabetic retinopathy, a leading cause of vision loss from blood-vessel damage in the retina in diabetic patients. We show that AIV can, without any a priori knowledge of the inlet and outlet boundary conditions, infer the two-dimensional (2D) flow fields from a sequence of 2D images of blood flow in MAOAC, but also can infer three-dimensional (3D) flow fields using only 2D images, thanks to the encoded physics laws. AIV provides a unique paradigm that seamlessly integrates images, experimental data, and underlying physics using neural networks to automatically analyze experimental data and infer key hemodynamic indicators that assess vascular injury.
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Correlation of OCT Angiography Vessel Densities and the Early Treatment Diabetic Retinopathy Study Grading Scale.
Mehta, NS, Lee, JG, Gupta, L, Zhou, DB, Andrade Romo, JS, Castanos, MV, Jansen, M, Ping Chui, TY, Rosen, RB
Ophthalmology. Retina. 2021;(7):714-715
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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.