{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,14]],"date-time":"2026-10-14T18:38:11Z","timestamp":1792003091524,"version":"4.4.0"},"reference-count":33,"publisher":"MDPI AG","issue":"15","license":[{"start":{"date-parts":[[2022,7,26]],"date-time":"2022-07-26T00:00:00Z","timestamp":1658793600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["JCM"],"abstract":"<jats:p>Purpose Using a wide-field, high-resolution swept-source optical coherence tomographic angiography (OCTA), this study investigated microvascular abnormalities in patients with pre- and early-stage diabetic retinopathy. Methods 38 eyes of 20 people with diabetes mellitus (DM) type 2 without diabetic retinopathy (DR) and 39 eyes of 21 people with DR were enrolled in this observational and cross-sectional cohort study, and a refractive error-matched group consisting of 42 eyes of 21 non-diabetic subjects of similar age were set as the control. Each participant underwent a wide-field swept-source OCTA. On OCTA scans (1.2 cm \u00d7 1.2 cm), the mean central macular thickness (CMT), the vessel density of the inner retina, superficial capillary plexus (SCP), and deep capillary plexus (DCP) were independently measured in the whole area (1.2 cm diameter) via concentric rings with varying radii (0\u20130.3, 0.3\u20130.6, 0.6\u20130.9, and 0.9\u20131.2 cm). Results Patients whose eyes had pre-and early-stage DR showed significantly decreased vessel density in the inner retina, SCP, DCP and CMT (early-stage DR) compared with the control. In addition, compared with the average values upon wide-field OCTA, the decreases were even more pronounced for concentric rings with a radius of 0.9\u20131.2 cm in terms of the inner retina, SCP, DCP and CMT. Conclusions Widefield OCTA allows for a more thorough assessment of retinal changes in patients with pre- and early-stage DR.; retinal microvascular abnormalities were observed in both groups. In addition, the decreases in retinal vessel density were more significant in the peripheral concentric ring with a radius of 0.9\u20131.2 cm. The application of novel and wide-field OCTA could potentially help to detect earlier diabetic microvascular abnormalities.<\/jats:p>","DOI":"10.3390\/jcm11154332","type":"journal-article","created":{"date-parts":[[2022,7,27]],"date-time":"2022-07-27T04:59:16Z","timestamp":1658897956000},"page":"4332","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":17,"title":["Retinal Microvascular Signs in Pre- and Early-Stage Diabetic Retinopathy Detected Using Wide-Field Swept-Source Optical Coherence Tomographic Angiography"],"prefix":"10.3390","volume":"11","author":[{"given":"Fabao","family":"Xu","sequence":"first","affiliation":[{"name":"Department of Ophthalmology, Qilu Hospital, Shandong University, Jinan 250012, China"},{"name":"Shandong Key Laboratory: Magnetic Field-Free Medicine & Functional Imaging, Jinan 250000, China"},{"name":"Magnetic Field-Free Medicine & Functional Imaging, Research Institute of Shandong University, Jinan 250000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhiwen","family":"Li","sequence":"additional","affiliation":[{"name":"Department of Ophthalmology, Qilu Hospital, Shandong University, Jinan 250012, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yang","family":"Gao","sequence":"additional","affiliation":[{"name":"Shandong Key Laboratory: Magnetic Field-Free Medicine & Functional Imaging, Jinan 250000, China"},{"name":"Magnetic Field-Free Medicine & Functional Imaging, Research Institute of Shandong University, Jinan 250000, China"},{"name":"School of Physics, Beihang University, Beijing 100191, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xueying","family":"Yang","sequence":"additional","affiliation":[{"name":"Department of Ophthalmology, Qilu Hospital, Shandong University, Jinan 250012, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ziyuan","family":"Huang","sequence":"additional","affiliation":[{"name":"Shandong Key Laboratory: Magnetic Field-Free Medicine & Functional Imaging, Jinan 250000, China"},{"name":"Magnetic Field-Free Medicine & Functional Imaging, Research Institute of Shandong University, Jinan 250000, China"},{"name":"School of Physics, Beihang University, Beijing 100191, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhiwei","family":"Li","sequence":"additional","affiliation":[{"name":"Department of Ophthalmology, Jinan Aier Eye Hospital, Jinan 250000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rui","family":"Zhang","sequence":"additional","affiliation":[{"name":"Department of Ophthalmology, Qilu Hospital, Shandong University, Jinan 250012, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shaopeng","family":"Wang","sequence":"additional","affiliation":[{"name":"Department of Ophthalmology, Zibo Central Hospital, Binzhou Medical University, Zibo 250012, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xinghong","family":"Guo","sequence":"additional","affiliation":[{"name":"Department of Endocrinology, Qilu Hospital, Shandong University, Jinan 255000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xinguo","family":"Hou","sequence":"additional","affiliation":[{"name":"Department of Endocrinology, Qilu Hospital, Shandong University, Jinan 255000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaolin","family":"Ning","sequence":"additional","affiliation":[{"name":"Shandong Key Laboratory: Magnetic Field-Free Medicine & Functional Imaging, Jinan 250000, China"},{"name":"Magnetic Field-Free Medicine & Functional Imaging, Research Institute of Shandong University, Jinan 250000, China"},{"name":"School of Physics, Beihang University, Beijing 100191, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jianqiao","family":"Li","sequence":"additional","affiliation":[{"name":"Department of Ophthalmology, Qilu Hospital, Shandong University, Jinan 250012, China"},{"name":"Shandong Key Laboratory: Magnetic Field-Free Medicine & Functional Imaging, Jinan 250000, China"},{"name":"Magnetic Field-Free Medicine & Functional Imaging, Research Institute of Shandong University, Jinan 250000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,7,26]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"409","DOI":"10.1111\/j.1755-3768.1994.tb02787.x","article-title":"Transretinal histopathological changes in capillary-free areas of diabetic retinopathy","volume":"72","author":"Bek","year":"1994","journal-title":"Acta Ophthalmol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"6729","DOI":"10.1167\/iovs.10-5364","article-title":"Impaired retinal circulation in patients with type 2 diabetes mellitus: Retinal laser Doppler velocimetry study","volume":"51","author":"Nagaoka","year":"2010","journal-title":"Investig. Ophthalmol. Vis. Sci."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"374","DOI":"10.1034\/j.1600-0420.2000.078004374.x","article-title":"Screening and prevention of diabetic blindness","volume":"78","author":"Bek","year":"2000","journal-title":"Acta Ophthalmol. Scand."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1016\/S0140-6736(11)60679-X","article-title":"National, regional, and global trends in fasting plasma glucose and diabetes prevalence since 1980: Systematic analysis of health examination surveys and epidemiological studies with 370 country-years and 2.7 million participants","volume":"378","author":"Danaei","year":"2011","journal-title":"Lancet"},{"key":"ref_5","unstructured":"NCD Risk Factor Collaboration (NCD-RisC) (2016). Worldwide trends in diabetes since 1980: A pooled analysis of 751 population-based studies with 4.4 million participants. Lancet, 387, 1513\u20131530."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"556","DOI":"10.2337\/dc11-1909","article-title":"Global prevalence and major risk factors of diabetic retinopathy","volume":"35","author":"Yau","year":"2012","journal-title":"Diabetes Care"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"140","DOI":"10.1016\/S2213-8587(18)30128-1","article-title":"Incidence and progression of diabetic retinopathy: A systematic review","volume":"7","author":"Sabanayagam","year":"2019","journal-title":"Lancet Diabetes Endocrinol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1159\/000442801","article-title":"Optical Coherence Tomography Angiography of Diabetic Retinopathy","volume":"56","author":"Bandello","year":"2016","journal-title":"Dev. Ophthalmol."},{"key":"ref_9","first-page":"OCT362-370","article-title":"Quantifying Microvascular Density and Morphology in Diabetic Retinopathy Using Spectral-Domain Optical Coherence Tomography Angiography","volume":"57","author":"Kim","year":"2016","journal-title":"Investig. Ophthalmol. Vis. Sci."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"644","DOI":"10.1001\/jamaophthalmol.2016.0600","article-title":"Select Features of Diabetic Retinopathy on Swept-Source Optical Coherence Tomographic Angiography Compared with Fluorescein Angiography and Normal Eyes","volume":"134","author":"Salz","year":"2016","journal-title":"JAMA Ophthalmol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"e751","DOI":"10.1111\/aos.13404","article-title":"Early microvascular retinal changes in optical coherence tomography angiography in patients with type 1 diabetes mellitus","volume":"95","author":"Simonett","year":"2017","journal-title":"Acta Ophthalmol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"190","DOI":"10.1167\/iovs.16-20531","article-title":"Quantitative Retinal Optical Coherence Tomography Angiography in Patients with Diabetes without Diabetic Retinopathy","volume":"58","author":"Dimitrova","year":"2017","journal-title":"Investig. Ophthalmol. Vis. Sci."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1136\/bjophthalmol-2016-309424","article-title":"Comparison of diabetic retinopathy classification using fluorescein angiography and optical coherence tomography angiography","volume":"101","author":"Soares","year":"2017","journal-title":"Br. J. Ophthalmol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"2575","DOI":"10.1038\/s41598-017-02767-0","article-title":"Determinants of Quantitative Optical Coherence Tomography Angiography Metrics in Patients with Diabetes","volume":"7","author":"Tang","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"5864","DOI":"10.1167\/iovs.10-5333","article-title":"Correlation of histologic and clinical images to determine the diagnostic value of fluorescein angiography for studying retinal capillary detail","volume":"51","author":"Mendis","year":"2010","journal-title":"Investig. Ophthalmol. Vis. Sci."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"3785","DOI":"10.1167\/iovs.17-21461","article-title":"Macular Vascular Fractal Dimension in the Deep Capillary Layer as an Early Indicator of Microvascular Loss for Retinopathy in Type 2 Diabetic Patients","volume":"58","author":"Chen","year":"2017","journal-title":"Investig. Ophthalmol. Vis. Sci."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"e264","DOI":"10.1111\/aos.13510","article-title":"Deep capillary plexus impairment in patients with type 1 diabetes mellitus with no signs of diabetic retinopathy revealed using optical coherence tomography angiography","volume":"96","author":"Scarinci","year":"2018","journal-title":"Acta Ophthalmol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"601","DOI":"10.1016\/j.survophthal.2018.04.003","article-title":"Early detection of diabetic retinopathy","volume":"63","author":"Safi","year":"2018","journal-title":"Surv. Ophthalmol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1016\/j.ajo.2019.01.012","article-title":"Earliest Evidence of Preclinical Diabetic Retinopathy Revealed Using Optical Coherence Tomography Angiography Perfused Capillary Density","volume":"203","author":"Rosen","year":"2019","journal-title":"Am. J. Ophthalmol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"531","DOI":"10.1007\/s00592-019-01288-8","article-title":"Do microvascular changes occur preceding neural impairment in early-stage diabetic retinopathy? Evidence based on the optic nerve head using optical coherence tomography angiography","volume":"56","author":"Li","year":"2019","journal-title":"Acta Diabetol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1747","DOI":"10.1136\/bjophthalmol-2018-313582","article-title":"Early retinal neurovascular impairment in patients with diabetes without clinically detectable retinopathy","volume":"103","author":"Zeng","year":"2019","journal-title":"Br. J. Ophthalmol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"649221","DOI":"10.3389\/fbioe.2021.649221","article-title":"Predicting Post-Therapeutic Visual Acuity and OCT Images in Patients with Central Serous Chorioretinopathy by Artificial Intelligence","volume":"9","author":"Xu","year":"2021","journal-title":"Front. Bioeng. Biotechnol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"106422","DOI":"10.1016\/j.cmpb.2021.106422","article-title":"Multi-path cascaded U-net for vessel segmentation from fundus fluorescein angiography sequential images","volume":"211","author":"Sun","year":"2021","journal-title":"Comput. Methods Programs Biomed."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1186\/s40942-020-00230-3","article-title":"Optical coherence tomography features of neovascularization in proliferative diabetic retinopathy: A systematic review","volume":"6","author":"Marques","year":"2020","journal-title":"Int. J. Retin. Vitr."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"100965","DOI":"10.1016\/j.preteyeres.2021.100965","article-title":"Artificial intelligence in OCT angiography","volume":"85","author":"Hormel","year":"2021","journal-title":"Prog. Retin. Eye Res."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"698644","DOI":"10.3389\/fmed.2021.698644","article-title":"Widefield Swept-Source Optical Coherence Tomography Angiography Assessment of Choroidal Changes in Vogt-Koyanagi-Harada Disease","volume":"8","author":"Qian","year":"2021","journal-title":"Front. Med."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"370","DOI":"10.1097\/OPX.0000000000001506","article-title":"Validation of an Automated Early Treatment Diabetic Retinopathy Study Low-contrast Letter Acuity Test","volume":"97","author":"Pang","year":"2020","journal-title":"Optom. Vis. Sci."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1001\/jamaophthalmol.2018.4982","article-title":"Comparison of Early Treatment Diabetic Retinopathy Study Standard 7-Field Imaging with Ultrawide-Field Imaging for Determining Severity of Diabetic Retinopathy","volume":"137","author":"Aiello","year":"2019","journal-title":"JAMA Ophthalmol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"e213859","DOI":"10.1001\/jamaophthalmol.2021.3859","article-title":"Widefield Swept-Source Optical Coherence Tomography Angiography of a \u201cPolypoidal-Like\u201d Retinal Arteriovenous Anastomosis in Proliferative Diabetic Retinopathy","volume":"139","author":"Shen","year":"2021","journal-title":"JAMA Ophthalmol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"534","DOI":"10.1136\/bjophthalmol-2020-317983","article-title":"Detection of neovascularisation in the vitreoretinal interface slab using widefield swept-source optical coherence tomography angiography in diabetic retinopathy","volume":"106","author":"Lu","year":"2022","journal-title":"Br. J. Ophthalmol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"577","DOI":"10.1136\/bjophthalmol-2020-316245","article-title":"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","volume":"105","author":"Cui","year":"2021","journal-title":"Br. J. Ophthalmol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1097\/IAE.0000000000001938","article-title":"Vascular Abnormalities in Diabetic Retinopathy Assessed with Swept-Source Optical Coherence Tomography Angiography Widefield Imaging","volume":"39","author":"Schaal","year":"2019","journal-title":"Retina"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"370","DOI":"10.1001\/jamaophthalmol.2017.0080","article-title":"Quantification of Retinal Microvascular Density in Optical Coherence Tomographic Angiography Images in Diabetic Retinopathy","volume":"135","author":"Durbin","year":"2017","journal-title":"JAMA Ophthalmol."}],"container-title":["Journal of Clinical Medicine"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2077-0383\/11\/15\/4332\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T23:56:50Z","timestamp":1760140610000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2077-0383\/11\/15\/4332"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,7,26]]},"references-count":33,"journal-issue":{"issue":"15","published-online":{"date-parts":[[2022,8]]}},"alternative-id":["jcm11154332"],"URL":"https:\/\/doi.org\/10.3390\/jcm11154332","relation":{},"ISSN":["2077-0383"],"issn-type":[{"value":"2077-0383","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,7,26]]}}}