{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T06:34:59Z","timestamp":1790836499773,"version":"4.1.0"},"reference-count":43,"publisher":"Elsevier BV","issue":"1","license":[{"start":{"date-parts":[[2024,1,1]],"date-time":"2024-01-01T00:00:00Z","timestamp":1704067200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2024,1,1]],"date-time":"2024-01-01T00:00:00Z","timestamp":1704067200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"},{"start":{"date-parts":[[2025,1,1]],"date-time":"2025-01-01T00:00:00Z","timestamp":1735689600000},"content-version":"vor","delay-in-days":366,"URL":"http:\/\/www.elsevier.com\/open-access\/userlicense\/1.0\/"}],"content-domain":{"domain":["jthjournal.org","elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Journal of Thrombosis and Haemostasis"],"published-print":{"date-parts":[[2024,1]]},"DOI":"10.1016\/j.jtha.2023.09.022","type":"journal-article","created":{"date-parts":[[2023,10,4]],"date-time":"2023-10-04T06:18:00Z","timestamp":1696400280000},"page":"286-299","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":46,"title":["COVID-19 promotes endothelial dysfunction and thrombogenicity: role of proinflammatory cytokines\/SGLT2 prooxidant pathway"],"prefix":"10.1016","volume":"22","author":[{"given":"Ali","family":"Mroueh","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Walaa","family":"Fakih","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Adrien","family":"Carmona","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Antonin","family":"Trimaille","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kensuke","family":"Matsushita","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Benjamin","family":"Marchandot","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Abdul Wahid","family":"Qureshi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dal-Seong","family":"Gong","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Cyril","family":"Auger","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Laurent","family":"Sattler","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Antje","family":"Reydel","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"S\u00e9bastien","family":"Hess","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Walid","family":"Oulehri","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Olivier","family":"Vollmer","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jean-Marc","family":"Lessinger","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nicolas","family":"Meyer","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael Paul","family":"Pieper","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Laurence","family":"Jesel","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Magnus","family":"B\u00e4ck","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Val\u00e9rie","family":"Schini-Kerth","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Olivier","family":"Morel","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.jtha.2023.09.022_bib1","doi-asserted-by":"crossref","first-page":"316","DOI":"10.1016\/j.jacc.2022.04.060","article-title":"Association of blood viscosity with mortality among patients hospitalized with COVID-19","volume":"80","author":"Choi","year":"2022","journal-title":"J\u00a0Am Coll Cardiol"},{"key":"10.1016\/j.jtha.2023.09.022_bib2","doi-asserted-by":"crossref","first-page":"1717","DOI":"10.1016\/j.jacc.2022.02.003","volume":"79","author":"Gluckman","year":"2022","journal-title":"J\u00a0Am Coll Cardiol"},{"key":"10.1016\/j.jtha.2023.09.022_bib3","doi-asserted-by":"crossref","first-page":"3038","DOI":"10.1093\/eurheartj\/ehaa623","article-title":"COVID-19 is, in the end, an endothelial disease","volume":"41","author":"Libby","year":"2020","journal-title":"Eur Heart J"},{"key":"10.1016\/j.jtha.2023.09.022_bib4","doi-asserted-by":"crossref","first-page":"2177","DOI":"10.1093\/cvr\/cvaa230","article-title":"Endothelial dysfunction in COVID-19: a position paper of the esc working group for atherosclerosis and vascular biology, and the esc council of basic cardiovascular science","volume":"116","author":"Evans","year":"2020","journal-title":"Cardiovasc Res"},{"key":"10.1016\/j.jtha.2023.09.022_bib5","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.tcm.2020.10.005","article-title":"COVID-19 - a vascular disease","volume":"31","author":"Siddiqi","year":"2021","journal-title":"Trends Cardiovasc Med"},{"key":"10.1016\/j.jtha.2023.09.022_bib6","first-page":"1651","article-title":"COVID-19 related coagulopathy: a distinct entity?","volume":"9","author":"Marchandot","year":"2020","journal-title":"J\u00a0Clin Med"},{"key":"10.1016\/j.jtha.2023.09.022_bib7","doi-asserted-by":"crossref","first-page":"202","DOI":"10.1016\/j.jacbts.2020.12.009","article-title":"Platelet and endothelial activation as potential mechanisms behind the thrombotic complications of COVID-19 patients","volume":"6","author":"Canzano","year":"2021","journal-title":"JACC Basic Transl Sci"},{"key":"10.1016\/j.jtha.2023.09.022_bib8","doi-asserted-by":"crossref","first-page":"365","DOI":"10.1161\/HYPERTENSIONAHA.121.18295","article-title":"Dysregulation of ACE (angiotensin-converting enzyme)-2 and renin-angiotensin peptides in SARS-CoV-2 mediated mortality and end-organ injuries","volume":"79","author":"Wang","year":"2022","journal-title":"Hypertension"},{"key":"10.1016\/j.jtha.2023.09.022_bib9","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1038\/s41577-021-00536-9","article-title":"Endothelial dysfunction and immunothrombosis as key pathogenic mechanisms in COVID-19","volume":"21","author":"Bonaventura","year":"2021","journal-title":"Nat Rev Immunol"},{"key":"10.1016\/j.jtha.2023.09.022_bib10","doi-asserted-by":"crossref","first-page":"583","DOI":"10.1038\/s41591-022-01689-3","article-title":"Long-term cardiovascular outcomes of COVID-19","volume":"28","author":"Xie","year":"2022","journal-title":"Nat Med"},{"key":"10.1016\/j.jtha.2023.09.022_bib11","doi-asserted-by":"crossref","first-page":"957","DOI":"10.3390\/biomedicines9080957","article-title":"Persistent endothelial dysfunction in post-acute COVID-19 syndrome: a case-control study","volume":"9","author":"Ambrosino","year":"2021","journal-title":"Biomedicines"},{"key":"10.1016\/j.jtha.2023.09.022_bib12","doi-asserted-by":"crossref","DOI":"10.3389\/fcvm.2021.750887","article-title":"Evaluation of endothelial dysfunction and inflammatory vasculopathy after SARS-CoV-2 infection-a cross-sectional study","volume":"8","author":"Jud","year":"2021","journal-title":"Front Cardiovasc Med"},{"key":"10.1016\/j.jtha.2023.09.022_bib13","article-title":"The IL-1\u03b2, IL-6, and TNF cytokine triad is associated with post-acute sequelae of COVID-19","volume":"3","author":"Schultheiss","year":"2022","journal-title":"Cell Rep Med"},{"key":"10.1016\/j.jtha.2023.09.022_bib14","doi-asserted-by":"crossref","first-page":"2546","DOI":"10.1111\/jth.15490","article-title":"Persistent endotheliopathy in the pathogenesis of long covid syndrome","volume":"19","author":"Fogarty","year":"2021","journal-title":"J\u00a0Thromb Haemost"},{"key":"10.1016\/j.jtha.2023.09.022_bib15","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.64909","article-title":"Convalescent COVID-19 patients are susceptible to endothelial dysfunction due to persistent immune activation","volume":"10","author":"Chioh","year":"2021","journal-title":"Elife"},{"key":"10.1016\/j.jtha.2023.09.022_bib16","doi-asserted-by":"crossref","first-page":"336","DOI":"10.1093\/cvr\/cvac115","volume":"119","author":"Gyongyosi","year":"2023","journal-title":"Cardiovasc Res"},{"key":"10.1016\/j.jtha.2023.09.022_bib17","doi-asserted-by":"crossref","first-page":"887","DOI":"10.1001\/jama.2022.12992","article-title":"Association between vaccination and acute myocardial infarction and ischemic stroke after COVID-19 infection","volume":"328","author":"Kim","year":"2022","journal-title":"JAMA"},{"key":"10.1016\/j.jtha.2023.09.022_bib18","doi-asserted-by":"crossref","first-page":"2903","DOI":"10.3390\/molecules27092903","article-title":"The pathophysiology of long covid throughout the renin-angiotensin system","volume":"27","author":"Khazaal","year":"2022","journal-title":"Molecules"},{"key":"10.1016\/j.jtha.2023.09.022_bib19","doi-asserted-by":"crossref","first-page":"1653","DOI":"10.1056\/NEJMsr2005760","article-title":"Renin-angiotensin-aldosterone system inhibitors in patients with COVID-19","volume":"382","author":"Vaduganathan","year":"2020","journal-title":"N\u00a0Engl J Med"},{"key":"10.1016\/j.jtha.2023.09.022_bib20","doi-asserted-by":"crossref","DOI":"10.1016\/j.pupt.2021.102035","article-title":"Endothelin antagonism and sodium glucose co-transporter 2 inhibition. A potential combination therapeutic strategy for COVID-19","volume":"69","author":"Fisk","year":"2021","journal-title":"Pulm Pharmacol Ther"},{"key":"10.1016\/j.jtha.2023.09.022_bib21","doi-asserted-by":"crossref","first-page":"210","DOI":"10.1038\/s41590-021-01113-x","article-title":"Immunological dysfunction persists for 8 months following initial mild-to-moderate SARS-CoV-2 infection","volume":"23","author":"Phetsouphanh","year":"2022","journal-title":"Nat Immunol"},{"key":"10.1016\/j.jtha.2023.09.022_bib22","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1016\/j.jacbts.2022.01.013","article-title":"Plasma proteomics of COVID-19-associated cardiovascular complications: implications for pathophysiology and therapeutics","volume":"7","author":"Roh","year":"2022","journal-title":"JACC Basic Transl Sci"},{"key":"10.1016\/j.jtha.2023.09.022_bib23","doi-asserted-by":"crossref","DOI":"10.1183\/23120541.00954-2020","article-title":"Microparticles in COVID-19 as a link between lung injury extension and thrombosis","volume":"7","author":"Morel","year":"2021","journal-title":"ERJ Open Res"},{"key":"10.1016\/j.jtha.2023.09.022_bib24","doi-asserted-by":"crossref","first-page":"280","DOI":"10.1161\/CIRCULATIONAHA.116.017513","article-title":"Endothelial microparticles from acute coronary syndrome patients induce premature coronary artery endothelial cell aging and thrombogenicity: role of the Ang II\/AT1 receptor\/NADPH oxidase-mediated activation of MAPKS and PI3-kinase pathways","volume":"135","author":"Abbas","year":"2017","journal-title":"Circulation"},{"key":"10.1016\/j.jtha.2023.09.022_bib25","doi-asserted-by":"crossref","DOI":"10.3389\/fcvm.2022.847809","article-title":"Plasma angiotensin ii is increased in critical coronavirus disease 2019","volume":"9","author":"Camargo","year":"2022","journal-title":"Front Cardiovasc Med"},{"key":"10.1016\/j.jtha.2023.09.022_bib26","doi-asserted-by":"crossref","first-page":"2109","DOI":"10.1111\/jcmm.14233","article-title":"Angiotensin II-induced redox-sensitive SGLT1 and 2 expression promotes high glucose-induced endothelial cell senescence","volume":"24","author":"Khemais-Benkhiat","year":"2020","journal-title":"J\u00a0Cell Mol Med"},{"key":"10.1016\/j.jtha.2023.09.022_bib27","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1186\/s12933-021-01252-3","article-title":"Angiotensin II-induced upregulation of SGLT1 and 2 contributes to human microparticle-stimulated endothelial senescence and dysfunction: protective effect of gliflozins","volume":"20","author":"Park","year":"2021","journal-title":"Cardiovasc Diab"},{"key":"10.1016\/j.jtha.2023.09.022_bib28","doi-asserted-by":"crossref","DOI":"10.14814\/phy2.14726","article-title":"SARS-CoV-2 related microvascular damage and symptoms during and after COVID-19: consequences of capillary transit-time changes, tissue hypoxia and inflammation","volume":"9","author":"Ostergaard","year":"2021","journal-title":"Physiol Rep"},{"key":"10.1016\/j.jtha.2023.09.022_bib29","doi-asserted-by":"crossref","first-page":"1116","DOI":"10.1038\/s12276-021-00649-0","article-title":"Interplay between interleukin-6 signaling and the vascular endothelium in cytokine storms","volume":"53","author":"Kang","year":"2021","journal-title":"Exp Mol Med"},{"key":"10.1016\/j.jtha.2023.09.022_bib30","doi-asserted-by":"crossref","first-page":"618","DOI":"10.1111\/j.1365-2362.2009.02153.x","article-title":"SARS-coronavirus modulation of myocardial ACE2 expression and inflammation in patients with SARS","volume":"39","author":"Oudit","year":"2009","journal-title":"Eur J Clin Invest"},{"key":"10.1016\/j.jtha.2023.09.022_bib31","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1161\/ATVBAHA.110.215061","article-title":"P53 impairs endothelial function by transcriptionally repressing kruppel-like factor 2","volume":"31","author":"Kumar","year":"2011","journal-title":"Arterioscler Thromb Vasc Biol"},{"key":"10.1016\/j.jtha.2023.09.022_bib32","doi-asserted-by":"crossref","first-page":"19911","DOI":"10.18632\/aging.104097","article-title":"Short telomeres increase the risk of severe COVID-19","volume":"12","author":"Froidure","year":"2020","journal-title":"Aging"},{"key":"10.1016\/j.jtha.2023.09.022_bib33","doi-asserted-by":"crossref","first-page":"1","DOI":"10.18632\/aging.202463","article-title":"Shorter telomere lengths in patients with severe COVID-19 disease","volume":"13","author":"Sanchez-Vazquez","year":"2021","journal-title":"Aging"},{"key":"10.1016\/j.jtha.2023.09.022_bib34","doi-asserted-by":"crossref","first-page":"586","DOI":"10.1016\/S2213-8587(21)00180-7","article-title":"Dapagliflozin in patients with cardiometabolic risk factors hospitalised with COVID-19 (dare-19): a randomised, double-blind, placebo-controlled, phase 3 trial","volume":"9","author":"Kosiborod","year":"2021","journal-title":"Lancet Diabetes Endocrinol"},{"key":"10.1016\/j.jtha.2023.09.022_bib35","first-page":"632","article-title":"Mechanisms of cardiovascular benefits of sodium glucose co-transporter 2 (SGLT2) inhibitors: a state-of-the-art review","volume":"5","author":"Lopaschuk","year":"2020","journal-title":"JACC Basic Trans Science"},{"key":"10.1016\/j.jtha.2023.09.022_bib36","article-title":"Emerging roles of sodium glucose cotransporter 2 (SGLT-2) inhibitors in diabetic cardiovascular diseases: focusing on immunity, inflammation and metabolism","volume":"13","author":"Xie","year":"2022","journal-title":"Front Pharmacol"},{"key":"10.1016\/j.jtha.2023.09.022_bib37","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1016\/j.ijcard.2021.05.029","article-title":"Abnormal apelin-ACE2 and SGLT2 signaling contribute to adverse cardiorenal injury in patients with COVID-19","volume":"336","author":"Li","year":"2021","journal-title":"Int J Cardiol"},{"key":"10.1016\/j.jtha.2023.09.022_bib38","doi-asserted-by":"crossref","DOI":"10.1016\/j.vph.2022.107095","article-title":"Empaglifozin prevents angiotensin II induced hypertesnsion related micro and macrovascular endothelial cell activation and diastolic dysfunction in rats despite persistent hypertension: role of endothelial SGLT1 and 2","volume":"146","author":"Bruckert","year":"2022","journal-title":"Vascul Pharmacol"},{"key":"10.1016\/j.jtha.2023.09.022_bib39","article-title":"Anti-inflammatory effects of sodium-glucose co-transporter 2 inhibitors on atherosclerosis","volume":"133\u20134","author":"Kang","year":"2020","journal-title":"Vascul Pharmacol"},{"key":"10.1016\/j.jtha.2023.09.022_bib40","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1016\/j.tcm.2020.10.011","article-title":"Editorial commentary: vascular injury in acute infections and COVID-19: everything old is new again","volume":"31","author":"Levy","year":"2021","journal-title":"Trends Cardiovasc Med"},{"key":"10.1016\/j.jtha.2023.09.022_bib41","doi-asserted-by":"crossref","first-page":"1760","DOI":"10.1161\/ATVBAHA.120.315595","article-title":"Vascular endothelial damage in the pathogenesis of organ injury in severe COVID-19","volume":"41","author":"Dupont","year":"2021","journal-title":"Arterioscler Thromb Vasc Biol"},{"key":"10.1016\/j.jtha.2023.09.022_bib42","doi-asserted-by":"crossref","DOI":"10.1016\/j.rpth.2023.100085","article-title":"Endothelial cell activation, Weibel-Palade body secretion, and enhanced angiogenesis in severe COVID-19","volume":"7","author":"Karampini","year":"2023","journal-title":"Res Pract Thromb Haemost"},{"key":"10.1016\/j.jtha.2023.09.022_bib43","first-page":"2030","article-title":"Exploring sodium glucose co-transporter-2 (SGLT2) inhibitors for organ protection in COVID-19","volume":"9","author":"Fernandez-Fernandez","year":"2020","journal-title":"J\u00a0Clin Med"}],"container-title":["Journal of Thrombosis and Haemostasis"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S1538783623007249?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S1538783623007249?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2025,10,27]],"date-time":"2025-10-27T03:39:50Z","timestamp":1761536390000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S1538783623007249"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,1]]},"references-count":43,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2024,1]]}},"alternative-id":["S1538783623007249"],"URL":"https:\/\/doi.org\/10.1016\/j.jtha.2023.09.022","relation":{},"ISSN":["1538-7836"],"issn-type":[{"value":"1538-7836","type":"print"}],"subject":[],"published":{"date-parts":[[2024,1]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"COVID-19 promotes endothelial dysfunction and thrombogenicity: role of proinflammatory cytokines\/SGLT2 prooxidant pathway","name":"articletitle","label":"Article Title"},{"value":"Journal of Thrombosis and Haemostasis","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.jtha.2023.09.022","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2023 Published by Elsevier Inc. on behalf of International Society on Thrombosis and Haemostasis.","name":"copyright","label":"Copyright"}]}}