{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,11,11]],"date-time":"2025-11-11T15:53:23Z","timestamp":1762876403869,"version":"build-2065373602"},"reference-count":34,"publisher":"MDPI AG","issue":"12","license":[{"start":{"date-parts":[[2022,11,28]],"date-time":"2022-11-28T00:00:00Z","timestamp":1669593600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Department of Veterans Affairs Merit Review Award","award":["1I01BX002042","1R01HL144727-01A1","R01 HL141268","EY028038","EY028861","EY028858","EY012601"],"award-info":[{"award-number":["1I01BX002042","1R01HL144727-01A1","R01 HL141268","EY028038","EY028861","EY028858","EY012601"]}]},{"DOI":"10.13039\/100000002","name":"NIH","doi-asserted-by":"publisher","award":["1I01BX002042","1R01HL144727-01A1","R01 HL141268","EY028038","EY028861","EY028858","EY012601"],"award-info":[{"award-number":["1I01BX002042","1R01HL144727-01A1","R01 HL141268","EY028038","EY028861","EY028858","EY012601"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"NIH","doi-asserted-by":"publisher","award":["1I01BX002042","1R01HL144727-01A1","R01 HL141268","EY028038","EY028861","EY028858","EY012601"],"award-info":[{"award-number":["1I01BX002042","1R01HL144727-01A1","R01 HL141268","EY028038","EY028861","EY028858","EY012601"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"NIH","doi-asserted-by":"publisher","award":["1I01BX002042","1R01HL144727-01A1","R01 HL141268","EY028038","EY028861","EY028858","EY012601"],"award-info":[{"award-number":["1I01BX002042","1R01HL144727-01A1","R01 HL141268","EY028038","EY028861","EY028858","EY012601"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"NIH","doi-asserted-by":"publisher","award":["1I01BX002042","1R01HL144727-01A1","R01 HL141268","EY028038","EY028861","EY028858","EY012601"],"award-info":[{"award-number":["1I01BX002042","1R01HL144727-01A1","R01 HL141268","EY028038","EY028861","EY028858","EY012601"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"NIH","doi-asserted-by":"publisher","award":["1I01BX002042","1R01HL144727-01A1","R01 HL141268","EY028038","EY028861","EY028858","EY012601"],"award-info":[{"award-number":["1I01BX002042","1R01HL144727-01A1","R01 HL141268","EY028038","EY028861","EY028858","EY012601"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"NIH","doi-asserted-by":"publisher","award":["1I01BX002042","1R01HL144727-01A1","R01 HL141268","EY028038","EY028861","EY028858","EY012601"],"award-info":[{"award-number":["1I01BX002042","1R01HL144727-01A1","R01 HL141268","EY028038","EY028861","EY028858","EY012601"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Life"],"abstract":"<jats:p>(1) Background: Retinal vascular imaging plays an essential role in diagnosing and managing chronic diseases such as diabetic retinopathy, sickle cell retinopathy, and systemic hypertension. Previously, we have shown that individuals with pulmonary arterial hypertension (PAH), a rare disorder, exhibit unique retinal vascular changes as seen using fluorescein angiography (FA) and that these changes correlate with PAH severity. This study aimed to determine if color fundus (CF) imaging could garner identical retinal information as previously seen using FA images in individuals with PAH. (2) Methods: VESGEN, computer software which provides detailed vascular patterns, was used to compare manual segmentations of FA to CF imaging in PAH subjects (n = 9) followed by deep learning (DL) processing of CF imaging to increase the speed of analysis and facilitate a noninvasive clinical translation. (3) Results: When manual segmentation of FA and CF images were compared using VESGEN analysis, both showed identical tortuosity and vessel area density measures. This remained true even when separating images based on arterial trees only. However, this was not observed with microvessels. DL segmentation when compared to manual segmentation of CF images showed similarities in vascular structure as defined by fractal dimension. Similarities were lost for tortuosity and vessel area density when comparing manual CF imaging to DL imaging. (4) Conclusions: Noninvasive imaging such as CF can be used with VESGEN to provide an accurate and safe assessment of retinal vascular changes in individuals with PAH. In addition to providing insight into possible future clinical translational use.<\/jats:p>","DOI":"10.3390\/life12121985","type":"journal-article","created":{"date-parts":[[2022,11,28]],"date-time":"2022-11-28T03:28:49Z","timestamp":1669606129000},"page":"1985","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Comparison of Retinal Imaging Techniques in Individuals with Pulmonary Artery Hypertension Using Vessel Generation Analysis"],"prefix":"10.3390","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-7986-3383","authenticated-orcid":false,"given":"Mariana","family":"DuPont","sequence":"first","affiliation":[{"name":"Department of Optometry and Vision Science, School of Optometry, University of Alabama at Birmingham, Birmingham, AL 35294, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"John","family":"Hunsicker","sequence":"additional","affiliation":[{"name":"Heersink School of Medicine, University of Alabama at Birmingham, Birmingham, AL 35294, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Simona","family":"Shirley","sequence":"additional","affiliation":[{"name":"Department of Political Science and Public Administration, University of Alabama at Birmingham, Birmingham, AL 35294, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9733-9187","authenticated-orcid":false,"given":"William","family":"Warriner","sequence":"additional","affiliation":[{"name":"Research Computing, University of Alabama at Birmingham, Birmingham, AL 35294, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Annabelle","family":"Rowland","sequence":"additional","affiliation":[{"name":"Heersink School of Medicine, University of Alabama at Birmingham, Birmingham, AL 35294, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Reddhyia","family":"Taylor","sequence":"additional","affiliation":[{"name":"Department of Osteopathic Medicine, The Philadelphia College of Osteopathic Medicine, Philadelphia, PA 19131, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"suffix":"Jr.","given":"Michael","family":"DuPont","sequence":"additional","affiliation":[{"name":"Department of Optometry and Vision Science, School of Optometry, University of Alabama at Birmingham, Birmingham, AL 35294, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mark","family":"Lagatuz","sequence":"additional","affiliation":[{"name":"Redline Performance Solutions, Ames Research Center, National Aeronautics and Space Administration, Moffett Field, Mountain View, CA 94043, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Taygan","family":"Yilmaz","sequence":"additional","affiliation":[{"name":"Division of Ophthalmology, Department of Surgery, Alpert Medical School of Brown University, Providence, RI 02903, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Andrew","family":"Foderaro","sequence":"additional","affiliation":[{"name":"Division of Pulmonary, Critical Care and Sleep Medicine, Department of Medicine, Alpert Medical School of Brown University, Providence, RI 02903, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Tim","family":"Lahm","sequence":"additional","affiliation":[{"name":"Department of Medicine, Division of Pulmonary, Critical Care and Sleep Medicine, National Jewish Health, Denver, CO 80206, USA"},{"name":"Department of Medicine, Division of Pulmonary Sciences and Critical Care Medicine, University of Colorado, Aurora, CO 80045, USA"},{"name":"Rocky Mountain Regional VA Medical Center, Aurora, CO 80045, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Corey E.","family":"Ventetuolo","sequence":"additional","affiliation":[{"name":"Department of Health Services, Policy and Practice, Brown University School of Public Health, Providence, RI 02903, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Maria B.","family":"Grant","sequence":"additional","affiliation":[{"name":"Department of Optometry and Vision Science, School of Optometry, University of Alabama at Birmingham, Birmingham, AL 35294, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2022,11,28]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1167\/tvst.9.2.6","article-title":"Insights into Systemic Disease through Retinal Imaging-Based Oculomics","volume":"9","author":"Wagner","year":"2020","journal-title":"Transl. Vis. Sci. Technol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"385","DOI":"10.1097\/IAE.0b013e318164a907","article-title":"Fundus autofluorescence imaging: Review and perspectives","volume":"28","author":"Holz","year":"2008","journal-title":"Retina"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"371","DOI":"10.1016\/j.csbj.2016.10.001","article-title":"A review on automatic analysis techniques for color fundus photographs","volume":"14","author":"Besenczi","year":"2016","journal-title":"Comput. Struct. Biotechnol. J."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"145","DOI":"10.4103\/0974-9233.151887","article-title":"Imaging in diabetic retinopathy","volume":"22","author":"Salz","year":"2015","journal-title":"Middle East Afr. J. Ophthalmol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"498","DOI":"10.1167\/iovs.09-3968","article-title":"Oscillation of angiogenesis with vascular dropout in diabetic retinopathy by VESsel GENeration analysis (VESGEN)","volume":"51","author":"Radhakrishnan","year":"2010","journal-title":"Investig. Ophthalmol. Vis. Sci."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"285","DOI":"10.2147\/IJGM.S107241","article-title":"Retinal vascular changes in hypertensive patients in Ibadan, Sub-Saharan Africa","volume":"9","author":"Oluleye","year":"2016","journal-title":"Int. J. Gen. Med."},{"key":"ref_7","unstructured":"Modi, P., and Arsiwalla, T. (2022). Hypertensive Retinopathy. StatPearls, StatPearls Publishing."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"679","DOI":"10.1016\/j.survophthal.2019.02.004","article-title":"Adverse reactions to fluorescein angiography: A comprehensive review of the literature","volume":"64","author":"Kornblau","year":"2019","journal-title":"Surv. Ophthalmol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"321","DOI":"10.1016\/j.jcjo.2016.03.015","article-title":"Intravenous fluorescein angiography-associated adverse reactions","volume":"51","author":"Xu","year":"2016","journal-title":"Can. J. Ophthalmol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"611","DOI":"10.1016\/S0161-6420(86)33697-2","article-title":"Fluorescein angiography complication survey","volume":"93","author":"Yannuzzi","year":"1986","journal-title":"Ophthalmology"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"740","DOI":"10.1111\/j.1600-0420.2006.00728.x","article-title":"Adverse effects of fluorescein angiography in hypertensive and elderly patients","volume":"84","author":"Musa","year":"2006","journal-title":"Acta Ophthalmol. Scand."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"508","DOI":"10.1097\/00007611-198104000-00040","article-title":"Hypertensive crisis and myocardial infarction after fluorescein angiography","volume":"74","author":"McAllister","year":"1981","journal-title":"South. Med. J."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"472","DOI":"10.2500\/aap.2007.28.3024","article-title":"Skin testing and adverse reactions in fluorescein: A prospective study","volume":"28","author":"Kalogeromitros","year":"2007","journal-title":"Allergy Asthma Proc."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1016\/j.ophtha.2009.11.046","article-title":"Retinal examination and photography are safe...is anyone surprised?","volume":"117","author":"Mainster","year":"2010","journal-title":"Ophthalmology"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"950","DOI":"10.1016\/j.ajo.2015.01.027","article-title":"Color fundus photography versus fluorescein angiography in identification of the macular center and zone in retinopathy of prematurity","volume":"159","author":"Patel","year":"2015","journal-title":"Am. J. Ophthalmol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"420","DOI":"10.1097\/00006982-199805000-00006","article-title":"Peripheral retinal evaluation comparing fundus photographs with fluorescein angiograms in patients with diabetes mellitus","volume":"18","author":"Agardh","year":"1998","journal-title":"Retina"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"101905","DOI":"10.1016\/j.media.2020.101905","article-title":"A review of machine learning methods for retinal blood vessel segmentation and artery\/vein classification","volume":"68","author":"Mookiah","year":"2021","journal-title":"Med. Image Anal."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"111985","DOI":"10.1109\/ACCESS.2021.3102176","article-title":"Retinal Vessel Segmentation Using Deep Learning: A Review","volume":"9","author":"Chen","year":"2021","journal-title":"IEEE Access"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"e12035","DOI":"10.1002\/pul2.12035","article-title":"Retinal vessel changes in pulmonary arterial hypertension","volume":"12","author":"DuPont","year":"2022","journal-title":"Pulm. Circ."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"320","DOI":"10.1002\/ar.20862","article-title":"VESGEN 2D: Automated, user-interactive software for quantification and mapping of angiogenic and lymphangiogenic trees and networks","volume":"292","author":"Vickerman","year":"2009","journal-title":"Anat. Rec."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1159\/000514211","article-title":"Vascular patterning as integrative readout of complex molecular and physiological signaling by vessel generation analysis","volume":"58","author":"Lagatuz","year":"2021","journal-title":"J. Vasc. Res."},{"key":"ref_22","first-page":"34","article-title":"RV-GAN: Segmenting Retinal Vascular Structure in Fundus Photographs Using a Novel Multi-scale Generative Adversarial Network","volume":"Volume 12908","author":"Cattin","year":"2021","journal-title":"Proceedings of the Medical Image Computing and Computer Assisted Intervention\u2014MICCAI 2021: 24th International Conference"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1109\/42.845178","article-title":"Locating blood vessels in retinal images by piecewise threshold probing of a matched filter response","volume":"19","author":"Hoover","year":"2000","journal-title":"IEEE Trans. Med. Imag."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"951","DOI":"10.1109\/TMI.2003.815900","article-title":"Locating the optic nerve in a retinal image using the fuzzy convergence of the blood vessels","volume":"22","author":"Hoover","year":"2003","journal-title":"IEEE Trans. Med. Imag."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"141","DOI":"10.11613\/BM.2015.015","article-title":"Understanding Bland Altman analysis","volume":"25","author":"Giavarina","year":"2015","journal-title":"Biochem. Med."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1167\/iovs.61.14.34","article-title":"Decreased Vascular Patterning in the Retinas of Astronaut Crew Members as New Measure of Ocular Damage in Spaceflight-Associated Neuro-ocular Syndrome","volume":"61","author":"Vyas","year":"2020","journal-title":"Investig. Ophthalmol. Vis. Sci."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1038\/s41526-021-00165-5","article-title":"Opposite response of blood vessels in the retina to 6\u00b0 head-down tilt and long-duration microgravity","volume":"7","author":"Taibbi","year":"2021","journal-title":"NPJ Microgravity"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1007\/s11892-015-0577-6","article-title":"Automated retinal image analysis for diabetic retinopathy in telemedicine","volume":"15","author":"Sim","year":"2015","journal-title":"Curr. Diab. Rep."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"15163","DOI":"10.1038\/s41598-018-33580-y","article-title":"Novel Classification of Early-stage Systemic Hypertensive Changes in Human Retina Based on OCTA Measurement of Choriocapillaris","volume":"8","author":"Takayama","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1184","DOI":"10.1167\/iovs.07-1329","article-title":"Selective inhibition of angiogenesis in small blood vessels and decrease in vessel diameter throughout the vascular tree by triamcinolone acetonide","volume":"49","author":"McKay","year":"2008","journal-title":"Investig. Ophthalmol. Vis. Sci."},{"key":"ref_31","first-page":"2","article-title":"For Application to Human Spaceflight and ISS Experiments: VESGEN Mapping of Microvascular Network Remodeling during Intestinal Inflammation","volume":"26","author":"Reinecker","year":"2012","journal-title":"Gravit. Space Biol. Bull."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1007\/BF02347689","article-title":"Progress towards automated diabetic ocular screening: A review of image analysis and intelligent systems for diabetic retinopathy","volume":"40","author":"Teng","year":"2002","journal-title":"Med. Biol. Eng. Comput."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"407","DOI":"10.1016\/S1361-8415(02)00058-0","article-title":"Characterization of changes in blood vessel width and tortuosity in retinopathy of prematurity using image analysis","volume":"6","author":"Heneghan","year":"2002","journal-title":"Med. Image Anal."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1292","DOI":"10.1007\/s10439-022-03058-0","article-title":"Retinal vessel segmentation, a review of classic and deep methods","volume":"50","author":"Khandouzi","year":"2022","journal-title":"Ann. Biomed. Eng."}],"container-title":["Life"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2075-1729\/12\/12\/1985\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T01:28:03Z","timestamp":1760146083000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2075-1729\/12\/12\/1985"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,11,28]]},"references-count":34,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2022,12]]}},"alternative-id":["life12121985"],"URL":"https:\/\/doi.org\/10.3390\/life12121985","relation":{},"ISSN":["2075-1729"],"issn-type":[{"type":"electronic","value":"2075-1729"}],"subject":[],"published":{"date-parts":[[2022,11,28]]}}}