{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,3]],"date-time":"2026-04-03T21:21:23Z","timestamp":1775251283063,"version":"3.50.1"},"reference-count":56,"publisher":"MDPI AG","issue":"7","license":[{"start":{"date-parts":[[2022,7,10]],"date-time":"2022-07-10T00:00:00Z","timestamp":1657411200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Medicina"],"abstract":"<jats:p>Background and Objectives: The aim of this study was to evaluate choroidal structure and vascularity indices in patients with non-proliferative diabetic retinopathy (NPDR). Materials and Methods: Sixty-three eyes from sixty-three patients were evaluated: 21 from healthy subjects, 20 with diabetes mellitus (DM) and no diabetic retinopathy (DR), and 22 with DM and non-proliferative diabetic retinopathy without diabetic macular edema (DME). Each patient underwent ocular examination, macular swept-source ocular coherence tomography (SS-OCT) imaging, glycemic control, and systemic high blood pressure (HBP) evaluation. Subfoveal choroidal thickness (SF-CT) was manually assessed on a line scan. Line scan OCT images were exported to ImageJ program. The areas under a 1.5, 3 and 6 mm horizontal line centered on the fovea were assessed by converting the OCT images to binary images, and total choroidal area (TCA), luminal area (LA), stromal area (SA), LA:SA ratio, and choroidal vascularity index (CVI) were evaluated. SF-CT and choroidal parameters were compared between groups, and correlations with ocular and systemic factors were analyzed. Results: SF-CT, TCA, LA, and SA were similar between groups. CVIs were significantly different between groups for all three studied areas (CVI-1.5: 66.21% vs. 66.06% vs. 63.74%, p = 0.003; CVI-3: 65.88% vs. 66.46% vs. 63.79%, p = 0.008; CVI-6: 64.79% vs. 65.40% vs. 63.61%, p = 0.032). NPDR patients had significantly lower CVIs compared to DM patients (p &lt; 0.05). No association of choroidal parameters with glycemic control, DM duration and HBP was found significant (p &lt; 0.05). Conclusions: Choroidal assessment by SS-OCT and image binarization in healthy subjects, subjects with DM without DR, and subjects with DM and NPDR indicated that CVI changes were identifiable and significant in early DR. The lack of association with ocular and systemic factors suggest that CVIs are reliable assessment parameters of choroidal vascular structure.<\/jats:p>","DOI":"10.3390\/medicina58070918","type":"journal-article","created":{"date-parts":[[2022,7,10]],"date-time":"2022-07-10T22:48:00Z","timestamp":1657493280000},"page":"918","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["Choroidal Assessment in Patients with Type 2 Diabetes Mellitus and Non-Proliferative Diabetic Retinopathy by Swept-Source Ocular Coherence Tomography and Image Binarization"],"prefix":"10.3390","volume":"58","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-2593-0135","authenticated-orcid":false,"given":"Otilia","family":"Obad\u0103","sequence":"first","affiliation":[{"name":"Department of Ophthalmology, \u201cGrigore T. Popa\u201d University of Medicine and Pharmacy, 16 Universit\u0103\u0163ii Street, 700115 Ia\u015fi, Romania"},{"name":"Department of Ophthalmology, \u201cSaint Spiridon\u201d Clinical Emergency Hospital, 1 Independen\u0163ei Street, 700111 Ia\u015fi, Romania"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Anca Delia","family":"Pantalon","sequence":"additional","affiliation":[{"name":"Department of Ophthalmology, \u201cSaint Spiridon\u201d Clinical Emergency Hospital, 1 Independen\u0163ei Street, 700111 Ia\u015fi, Romania"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Gabriela","family":"Rusu-Zota","sequence":"additional","affiliation":[{"name":"Department of Pharmacology, \u201cGrigore T. Popa\u201d University of Medicine and Pharmacy, 16 Universit\u0103\u0163ii Street, 700115 Ia\u015fi, Romania"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Anca","family":"H\u0103isan","sequence":"additional","affiliation":[{"name":"Department of Emergency Medicine, \u201cGrigore T. Popa\u201d University of Medicine and Pharmacy,16 Universit\u0103\u0163ii Street, 700115 Ia\u015fi, Romania"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Smaranda Ioana","family":"Lupu\u015foru","sequence":"additional","affiliation":[{"name":"Department of Surgery, \u201cGrigore T. Popa\u201d University of Medicine and Pharmacy, 16 Universit\u0103\u0163ii Street, 700115 Ia\u015fi, Romania"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Dorin","family":"Chiseli\u0163\u0103","sequence":"additional","affiliation":[{"name":"Department of Ophthalmology, \u201cGrigore T. Popa\u201d University of Medicine and Pharmacy, 16 Universit\u0103\u0163ii Street, 700115 Ia\u015fi, Romania"},{"name":"Oftaprof Ophthalmology Clinic, 54 Stejar Street, 700327 Ia\u015fi, Romania"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2022,7,10]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"489","DOI":"10.4239\/wjd.v6.i3.489","article-title":"Diabetic retinopathy\u2014Ocular complications of diabetes mellitus","volume":"6","author":"Nentwich","year":"2015","journal-title":"World J. Diabetes"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"512","DOI":"10.1016\/S0161-6420(85)34013-7","article-title":"Diabetic choroidopathy. Light and electron microscopic observations of seven cases","volume":"92","author":"Hidayat","year":"1985","journal-title":"Ophthalmology"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"589","DOI":"10.1001\/archopht.116.5.589","article-title":"Choriocapillaris degeneration and related pathologic changes in human diabetic eyes","volume":"116","author":"Cao","year":"1998","journal-title":"Arch. Ophthalmol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"436","DOI":"10.1007\/s00417-002-0451-5","article-title":"Risk factors for diabetic choroidopathy in patients with diabetic retinopathy","volume":"240","author":"Shiragami","year":"2002","journal-title":"Graefe\u2019s Arch. Clin. Exp. Ophthalmol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1453","DOI":"10.1007\/s00417-016-3360-8","article-title":"Diabetic choroidopathy: A review of the current literature","volume":"254","author":"Melancia","year":"2016","journal-title":"Graefe\u2019s Arch. Clin. Exp. Ophthalmol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1016\/j.visres.2017.04.011","article-title":"Diabetic choroidopathy","volume":"139","author":"Lutty","year":"2017","journal-title":"Vis. Res."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"144","DOI":"10.1016\/j.preteyeres.2009.12.002","article-title":"The multifunctional choroid","volume":"29","author":"Nickla","year":"2010","journal-title":"Prog. Retin. Eye Res."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"182","DOI":"10.1007\/BF03401566","article-title":"Hypoxic induction of endothelial cell growth factors in retinal cells: Identification and characterization of vascular endothelial growth factor (VEGF) as the mitogen","volume":"1","author":"Shima","year":"1995","journal-title":"Mol. Med."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1538","DOI":"10.1001\/archopht.1995.01100120068012","article-title":"Hypoxic regulation of vascular endothelial growth factor in retinal cells","volume":"113","author":"Aiello","year":"1995","journal-title":"Arch. Ophthalmol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"96","DOI":"10.1016\/j.preteyeres.2017.12.001","article-title":"Neural control of choroidal blood flow","volume":"64","author":"Reiner","year":"2018","journal-title":"Prog. Retin. Eye Res."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1111\/jch.13777","article-title":"Choroidal thickness is associated with renal hemodynamics in essential hypertension","volume":"22","author":"Geraci","year":"2020","journal-title":"J. Clin. Hypertens."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"423","DOI":"10.1097\/IAE.0b013e3182753b5a","article-title":"Choroidal thickness in relation to hypercholesterolemia on enhanced depth imaging optical coherence tomography","volume":"33","author":"Wong","year":"2013","journal-title":"Retina"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"566","DOI":"10.1016\/j.survophthal.2016.02.007","article-title":"State of science: Choroidal thickness and systemic health","volume":"61","author":"Tan","year":"2016","journal-title":"Surv. Ophthalmol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1016\/j.ajo.2017.09.030","article-title":"Diabetic Choroidopathy: Choroidal Vascular Density and Volume in Diabetic Retinopathy with Swept-Source Optical Coherence Tomography","volume":"184","author":"Wang","year":"2017","journal-title":"Am. J. Ophthalmol."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Hua, R., Liu, L., Wang, X., and Chen, L. (2013). Imaging Evidence of Diabetic Choroidopathy In Vivo: Angiographic Pathoanatomy and Choroidal-Enhanced Depth Imaging. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0083494"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1023\/B:INTE.0000031744.93778.60","article-title":"Foveolar choroidal hemodynamics in proliferative diabetic retinopathy","volume":"25","author":"Schocket","year":"2004","journal-title":"Int. Ophthalmol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1060","DOI":"10.1136\/bjo.2003.035345","article-title":"Alteration of choroidal circulation in the foveal region in patients with type 2 diabetes","volume":"88","author":"Nagaoka","year":"2004","journal-title":"Br. J. Ophthalmol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1167\/iovs.61.4.29","article-title":"Choroidal Thickness in Diabetes and Diabetic Retinopathy: A Swept Source OCT Study","volume":"61","author":"Wang","year":"2020","journal-title":"Investig. Ophthalmol. Vis. Sci."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Spaide, R.F., Ohno-Matsui, K., and Yannuzzi, L.A. (2014). The choroid. Pathologic Myopia, Springer International Publishing. [2nd ed.].","DOI":"10.1007\/978-1-4614-8338-0"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"921","DOI":"10.2147\/OPTH.S207376","article-title":"Subfoveal choroidal thickness in diabetic macular edema","volume":"13","author":"Mohamed","year":"2019","journal-title":"Clin. Ophthalmol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"795","DOI":"10.1097\/IAE.0000000000001582","article-title":"Choroidal thickness in diabetic patients without diabetic retinopathy","volume":"38","author":"Vicente","year":"2018","journal-title":"Retina"},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Pessoa, B., Heitor, J., Coelho, C., Leander, M., Men\u00e9res, P., Figueira, J., Meireles, A., and Beir\u00e3o, M. (2022). Systemic and vitreous biomarkers\u2014new insights in diabetic retinopathy. Graefe\u2019s Arch. Clin. Exp. Ophthalmol.","DOI":"10.1007\/s00417-022-05624-7"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"e612","DOI":"10.1111\/aos.13044","article-title":"Choroidal vascularity index\u2013A novel optical coherence tomography parameter for disease monitoring in diabetes mellitus?","volume":"94","author":"Tan","year":"2016","journal-title":"Acta Ophthalmol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"21090","DOI":"10.1038\/srep21090","article-title":"Choroidal vascularity index as a measure of vascular status of the choroid: Measurements in healthy eyes from a population-based study","volume":"6","author":"Agrawal","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Iovino, C., Pellegrini, M., Bernabei, F., Borrelli, E., Sacconi, R., Govetto, A., Vagge, A., Di Zazzo, A., Forlini, M., and Finocchio, L. (2020). Choroidal Vascularity Index: An In-Depth Analysis of This Novel Optical Coherence Tomography Parameter. J. Clin. Med., 9.","DOI":"10.3390\/jcm9020595"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1167\/iovs.11-8782","article-title":"Diurnal Variation of Choroidal Thickness in Normal, Healthy Subjects Measured by Spectral Domain Optical Coherence Tomography","volume":"53","author":"Tan","year":"2012","journal-title":"Investig. Ophthalmol. Vis. Sci."},{"key":"ref_27","first-page":"360","article-title":"Diurnal variations in luminal and stromal areas of choroid in normal eyes","volume":"101","author":"Kinoshita","year":"2017","journal-title":"Br. J. Ophthalmol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"174","DOI":"10.1001\/jamaophthalmol.2013.7288","article-title":"Characterization of the choroid-scleral junction and suprachoroidal layer in healthy individuals on enhanced-depth imaging optical coherence tomography","volume":"132","author":"Yiu","year":"2014","journal-title":"JAMA Ophthalmol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"e142","DOI":"10.1111\/aos.12777","article-title":"Relationship of ocular and systemic factors to the visibility of choroidal-scleral interface using spectral domain optical coherence tomography","volume":"94","author":"Gupta","year":"2016","journal-title":"Acta Ophthalmol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"130","DOI":"10.1016\/j.preteyeres.2015.10.002","article-title":"Investigating the choriocapillaris and choroidal vasculature with new optical coherence tomography technologies","volume":"52","author":"Ferrara","year":"2016","journal-title":"Prog. Retin. Eye Res."},{"key":"ref_31","unstructured":"(2020, November 20). ImageJ, Available online: https:\/\/imagej.nih.gov\/ij\/."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1123","DOI":"10.1016\/j.ajo.2015.03.005","article-title":"Luminal and stromal areas of choroid determined by binarization method of optical coherence tomographic images","volume":"159","author":"Sonoda","year":"2015","journal-title":"Am. J. Ophthalmol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1088","DOI":"10.1038\/s41598-020-57788-z","article-title":"Semantic Segmentation of the Choroid in Swept Source Optical Coherence Tomography Images for Volumetrics","volume":"10","author":"Tsuji","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1186\/s40942-021-00355-z","article-title":"Choroidal changes and associations with visual acuity in diabetic patients","volume":"8","author":"Marques","year":"2022","journal-title":"Int. J. Retin. Vitr."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"244","DOI":"10.1097\/IAE.0000000000000281","article-title":"Suprachoroidal layer and suprachoroidal space delineating the outer margin of the choroid in swept-source optical coherence tomography","volume":"35","author":"Michalewska","year":"2015","journal-title":"Retina"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1097\/IAE.0000000000001516","article-title":"Choroidal thickness in diabetic retinopathy assessed with swept-source optical coherence tomography","volume":"38","author":"Talcott","year":"2018","journal-title":"Retina"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"2023","DOI":"10.1016\/j.ophtha.2013.03.009","article-title":"Subfoveal choroidal thickness in diabetes and diabetic retinopathy","volume":"120","author":"Xu","year":"2013","journal-title":"Ophthalmology"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1016\/j.exer.2014.02.016","article-title":"The effect of hyperglycaemia on permeability and the expression of junctional complex molecules in human retinal and choroidal endothelial cells","volume":"121","author":"Saker","year":"2014","journal-title":"Exp. Eye Res."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"912","DOI":"10.4103\/0301-4738.176024","article-title":"Choroidal thickness in diabetic patients of Indian ethnicity","volume":"63","author":"Sudhalkar","year":"2015","journal-title":"Indian J. Ophthalmol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"6803","DOI":"10.1167\/iovs.12-10314","article-title":"Choroidal Thinning in Diabetes Type 1 Detected by 3-Dimensional 1060 nm Optical Coherence Tomography","volume":"53","author":"Esmaeelpour","year":"2012","journal-title":"Investig. Ophthalmol. Vis. Sci."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"3378","DOI":"10.1167\/iovs.12-11503","article-title":"Changes in choroidal thickness in relation to the severity of retinopathy and macular edema in type 2 diabetic patients","volume":"54","author":"Kim","year":"2013","journal-title":"Investig. Ophthalmol. Vis. Sci."},{"key":"ref_42","first-page":"e10871","article-title":"Choroidal Changes in Diabetic Patients With Different Stages of Diabetic Retinopathy","volume":"12","author":"Hamadneh","year":"2020","journal-title":"Cureus"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1016\/j.ophtha.2012.07.048","article-title":"Subfoveal choroidal thickness: The Beijing Eye Study","volume":"120","author":"Wei","year":"2013","journal-title":"Ophthalmology"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"474","DOI":"10.1159\/000506381","article-title":"The Effect of Glycemia on Choroidal Thickness in Different Stages of Diabetic Retinopathy","volume":"63","author":"Abalem","year":"2020","journal-title":"Ophthalmic Res."},{"key":"ref_45","first-page":"285","article-title":"Choroidal Thickness and Hemoglobin A1c Levels in Patients with Type 2 Diabetes Mellitus","volume":"14","author":"Torabi","year":"2019","journal-title":"J. Ophthalmic Vis. Res."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1863","DOI":"10.1007\/s10792-017-0668-2","article-title":"Influence of glycosylated hemoglobin on the choroidal thickness","volume":"38","author":"Canan","year":"2018","journal-title":"Int. Ophthalmol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1183","DOI":"10.4103\/ijo.IJO_1994_20","article-title":"Comparison of choroidal thickness in systemic hypertensive subjects with healthy individuals by spectral domain optical coherence tomography","volume":"69","author":"Waghamare","year":"2021","journal-title":"Indian J. Ophthalmol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"152","DOI":"10.5301\/ejo.5000675","article-title":"Choroidal thickness in systemic arterial hypertension","volume":"26","author":"Akay","year":"2016","journal-title":"Eur. J. Ophthalmol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"239","DOI":"10.4103\/0301-4738.156928","article-title":"Evaluation of choroidal thickness via enhanced depth-imaging optical coherence tomography in patients with systemic hypertension","volume":"63","author":"Karabas","year":"2015","journal-title":"Indian J. Ophthalmol."},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"Ghassemi, F., Berijani, S., Babeli, A., Faghihi, H., Gholizadeh, A., and Sabour, S. (2022). The quantitative measurements of choroidal thickness and volume in diabetic retinopathy using optical coherence tomography and optical coherence tomography angiography; correlation with vision and foveal avascular zone. BMC Ophthalmol., 22.","DOI":"10.1186\/s12886-021-02178-w"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"6488","DOI":"10.1167\/iovs.12-9758","article-title":"Reduced Ocular Blood Flow as an Early Indicator of Diabetic Retinopathy in a Mouse Model of Diabetes","volume":"53","author":"Muir","year":"2012","journal-title":"Investig. Ophthalmol. Vis. Sci."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"e001295","DOI":"10.1136\/bmjdrc-2020-001295","article-title":"Decrease in Choroidal Vascularity Index of Haller\u2019s layer in diabetic eyes precedes retinopathy","volume":"8","author":"Foo","year":"2020","journal-title":"BMJ Open Diabetes Res. Care"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1038\/s41598-017-18511-7","article-title":"Choroidal vascularity index in type-2 diabetes analyzed by swept-source optical coherence tomography","volume":"8","author":"Kim","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_54","doi-asserted-by":"crossref","unstructured":"Damian, I., Roman, G., and Nicoar\u0103, S.D. (2021). Analysis of the Choroid and Its Relationship with the Outer Retina in Patients with Diabetes Mellitus Using Binarization Techniques Based on Spectral-Domain Optical Coherence Tomography. J. Clin. Med., 10.","DOI":"10.3390\/jcm10020210"},{"key":"ref_55","first-page":"11206721211035615","article-title":"Choroidal structural changes and choroidal vascularity index in patients with systemic hypertension","volume":"27","author":"Temel","year":"2021","journal-title":"Eur. J. Ophthalmol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"e770","DOI":"10.1111\/aos.13442","article-title":"Influence of scanning area on choroidal vascularity index measurement using optical coherence tomography","volume":"95","author":"Agrawal","year":"2017","journal-title":"Acta Ophthalmol."}],"container-title":["Medicina"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1648-9144\/58\/7\/918\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T23:47:41Z","timestamp":1760140061000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1648-9144\/58\/7\/918"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,7,10]]},"references-count":56,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2022,7]]}},"alternative-id":["medicina58070918"],"URL":"https:\/\/doi.org\/10.3390\/medicina58070918","relation":{},"ISSN":["1648-9144"],"issn-type":[{"value":"1648-9144","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,7,10]]}}}