{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T01:58:40Z","timestamp":1760147920683,"version":"build-2065373602"},"reference-count":43,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2023,3,14]],"date-time":"2023-03-14T00:00:00Z","timestamp":1678752000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Government of the Russian Federation","award":["075-15-2022-1110"],"award-info":[{"award-number":["075-15-2022-1110"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Diagnostics"],"abstract":"<jats:p>Patients with COVID-19 demonstrate higher rates of cardiovascular complications, including thromboses and thromboembolism. One may suppose that the action of SARS-CoV-2 transforms stable atherosclerotic plaques into unstable status. Cardiovascular complications in COVID-19 may be caused by progressive viral alteration of the blood vessels, including Vasa vasorum. A lethal case of ischemic brain disease caused by cerebral atherosclerosis and exacerbated by a stroke during COVID-19 infection is briefly described. The results of the autopsy showed perivascular lymphocytic infiltration and signs of Vasa vasorum vasculitis with thrombi of adventitial microvasculature. The data discussed in the article are interpreted in the context of the concept giving the important role in atherogenesis to Vasa vasorum.<\/jats:p>","DOI":"10.3390\/diagnostics13061097","type":"journal-article","created":{"date-parts":[[2023,3,14]],"date-time":"2023-03-14T06:57:11Z","timestamp":1678777031000},"page":"1097","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["COVID-19 and Vasa vasorum: New Atherogenic Factor? A Case Report and Autopsy Findings"],"prefix":"10.3390","volume":"13","author":[{"given":"Julia A.","family":"Macarova","sequence":"first","affiliation":[{"name":"Laboratory of the Microangiopathic Mechanisms of Atherogenesis, Saint Petersburg State University, 199034 Saint-Petersburg, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0747-7007","authenticated-orcid":false,"given":"Sofia A.","family":"Malakhova","sequence":"additional","affiliation":[{"name":"Laboratory of the Microangiopathic Mechanisms of Atherogenesis, Saint Petersburg State University, 199034 Saint-Petersburg, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Tatiana A.","family":"Novitskaya","sequence":"additional","affiliation":[{"name":"Laboratory of the Microangiopathic Mechanisms of Atherogenesis, Saint Petersburg State University, 199034 Saint-Petersburg, Russia"},{"name":"Department of Experimental Tuberculosis, St. Petersburg State Research Institute of Phthisiopulmonology, 191036 Saint-Petersburg, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Valeria A.","family":"Shapkina","sequence":"additional","affiliation":[{"name":"Laboratory of the Microangiopathic Mechanisms of Atherogenesis, Saint Petersburg State University, 199034 Saint-Petersburg, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6359-0026","authenticated-orcid":false,"given":"Leonid P.","family":"Churilov","sequence":"additional","affiliation":[{"name":"Laboratory of the Microangiopathic Mechanisms of Atherogenesis, Saint Petersburg State University, 199034 Saint-Petersburg, Russia"},{"name":"Department of Experimental Tuberculosis, St. Petersburg State Research Institute of Phthisiopulmonology, 191036 Saint-Petersburg, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2023,3,14]]},"reference":[{"key":"ref_1","unstructured":"World Health Organization (2020, March 01). Coronavirus Disease (COVID-19) Outbreak. Available online: https:\/\/www.who.int."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1089","DOI":"10.1007\/s00134-020-06062-x","article-title":"High risk of thrombosis in patients with severe SARS-CoV-2 infection: A multicenter prospective cohort study","volume":"46","author":"Helms","year":"2020","journal-title":"Intensive Care Med."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Sagris, M., Theofilis, P., Antonopoulos, A.S., Tsioufis, C., Oikonomou, E., Antoniades, C., Crea, F., Kaski, J.C., and Tousoulis, D. (2021). Inflammatory Mechanisms in COVID-19 and Atherosclerosis: Current Pharmaceutical Perspectives. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms22126607"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"745","DOI":"10.3389\/fcvm.2021.745758","article-title":"Long Covid 19 Syndrome: Is It Related to Microcirculation and Endothelial Dysfunction? Insights from TUN-EndCOV Study","volume":"8","author":"Charfeddine","year":"2021","journal-title":"Front. Cardiovasc. Med."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"172","DOI":"10.1186\/s12933-021-01359-7","article-title":"Persistent clotting protein pathology in Long Covid\/Post-Acute Sequelae of COVID-19 (PASC) is accompanied by increased levels of antiplasmin","volume":"20","author":"Pretorius","year":"2021","journal-title":"Cardiovasc. Diabetol."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Tanaka, H., Zaima, N., Sasaki, T., Sano, M., Yamamoto, N., Saito, T., Inuzuka, K., Hayasaka, T., Goto-Inoue, N., and Sugiura, Y. (2015). Hypoperfusion of the adventitial vasa vasorum develops an abdominal aortic aneurysm. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0134386"},{"key":"ref_7","first-page":"6439","article-title":"Aortic vulnerability to COVID-19: Is the microvasculature of vasa vasorum a key factor? A case report and a review of the literature","volume":"25","author":"Faa","year":"2021","journal-title":"Eur. Rev. Med. Pharmacol. Sci."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1109","DOI":"10.1093\/ejcts\/ezaa367","article-title":"Microvasculature dysfunction as the common thread between atherosclerosis, Kawasaki disease, and severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) associated multi-system inflammatory syndrome in children","volume":"58","author":"Boyle","year":"2020","journal-title":"Eur. J. Cardiothorac. Surg."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1161\/CIRCULATIONAHA.116.025407","article-title":"A surgeon\u2019s view on the pathogenesis of atherosclerosis","volume":"135","author":"Haverich","year":"2017","journal-title":"Circulation"},{"key":"ref_10","first-page":"12609","article-title":"Molecular pathways triggered by COVID-19 in different organs: ACE2 receptor-expressing cells under attack? A review","volume":"24","author":"Saba","year":"2020","journal-title":"Eur. Rev. Med. Pharmacol. Sci."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Wirth, K.J., and L\u00f6hn, M. (2022). Orthostatic Intolerance after COVID-19 Infection: Is Disturbed Microcirculation of the Vasa Vasorum of Capacitance Vessels the Primary Defect?. Medicina, 58.","DOI":"10.3390\/medicina58121807"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"706","DOI":"10.3389\/fimmu.2018.00706","article-title":"Vasa Vasorum Angiogenesis: Key Player in the Initiation and Progression of Atherosclerosis and Potential Target for the Treatment of Cardiovascular Disease","volume":"9","author":"Sedding","year":"2018","journal-title":"Front. Immunol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"2950","DOI":"10.1016\/j.jacc.2020.04.031","article-title":"COVID-19 and Thrombotic or Thromboembolic Disease: Implications for Prevention, Antithrombotic Therapy, and Follow-up: JACC state-of-the-art review","volume":"75","author":"Bikdeli","year":"2020","journal-title":"J. Am. Coll. Cardiol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"811","DOI":"10.1001\/jamacardio.2020.1017","article-title":"Cardiovascular Implications of Fatal Outcomes of Patients With Coronavirus Disease 2019 (COVID-19)","volume":"5","author":"Guo","year":"2020","journal-title":"JAMA Cardiol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"2268","DOI":"10.1056\/NEJMc2008597","article-title":"Neurologic Features in Severe SARS-CoV-2 Infection","volume":"382","author":"Helms","year":"2020","journal-title":"N. Engl. J. Med."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"281","DOI":"10.1016\/j.amjms.2021.12.010","article-title":"Endothelial Dysfunction in Covid-19 Infection","volume":"363","author":"Otifi","year":"2022","journal-title":"Am. J. Med. Sci."},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Hogea, T., Suciu, B.A., Iv\u0103nescu, A.D., Caras, C., Chinezu, L., Arb\u0103nas, E.M., Russu, E., Kaller, R., Arb\u0103nas, E.M., and Mures, A.V. (2023). Increased Epicardial Adipose Tissue (EAT), Left Coronary Artery Plaque Morphology, and Valvular Atherosclerosis as Risks Factors for Sudden Cardiac Death from a Forensic Perspective. Diagnostics, 13.","DOI":"10.3390\/diagnostics13010142"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"e2021304","DOI":"10.4322\/acr.2021.304","article-title":"The vasa vasorum of the large pulmonary vessels are involved in COVID-19","volume":"11","author":"Daisley","year":"2021","journal-title":"Autops. Case Rep."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1016\/j.xjon.2020.12.012","article-title":"Aortic dissection is a disease of the vasa vasorum","volume":"5","author":"Haverich","year":"2021","journal-title":"JTCVS Open"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1352","DOI":"10.21037\/cdt-20-561","article-title":"Can COVID19 trigger the plaque vulnerability-a Kounis syndrome warning for \u2018asymptomatic subjects\u2019","volume":"10","author":"Saba","year":"2020","journal-title":"Cardiovasc. Diagn. Ther."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"103240","DOI":"10.1016\/j.autrev.2022.103240","article-title":"Immune and non-immune mechanisms that determine vasculitis and coronary artery aneurysm topography in Kawasaki disease and MIS-C","volume":"22","author":"Giryes","year":"2023","journal-title":"Autoimmun. Rev."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"103012","DOI":"10.1016\/j.autrev.2021.103012","article-title":"Autoantibodies and SARS-CoV2 infection: The spectrum from association to clinical implication: Report of the 15th Dresden Symposium on Autoantibodies","volume":"21","author":"Damoiseaux","year":"2022","journal-title":"Autoimmun. Rev."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Grzegorowska, O., and Lorkowski, J. (2020). Possible correlations between atherosclerosis, acute coronary syndromes and COVID-19. J. Clin. Med., 9.","DOI":"10.3390\/jcm9113746"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"E270","DOI":"10.1148\/radiol.2020201933","article-title":"Imaging of Neurologic Disease in Hospitalized Patients with COVID-19: An Italian Multicenter Retrospective Observational Study","volume":"297","author":"Leali","year":"2020","journal-title":"Radiology"},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Savastano, M.C., Santoro, L., Crincoli, E., Fossataro, C., Gambini, G., Savastano, A., De Vico, U., Santoliquido, A., Nesci, A., and Landi, F. (2022). Radial Peripapillary Capillary Plexus Perfusion and Endothelial Dysfunction in Early Post-SARS-CoV-2 Infection. Vision, 6.","DOI":"10.3390\/vision6020026"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"381","DOI":"10.1016\/j.jvs.2020.07.089","article-title":"Early experience with arterial thromboembolic complications in patients with COVID-19","volume":"73","author":"Indes","year":"2021","journal-title":"J. Vasc. Surg."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"108652","DOI":"10.1016\/j.clim.2020.108652","article-title":"Influenza infection, SARS, MERS and COVID-19: Cytokine storm\u2014The common denominator and the lessons to be learned","volume":"223","author":"Ryabkova","year":"2021","journal-title":"Clin. Immunol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"649","DOI":"10.1016\/j.cardiores.2007.06.020","article-title":"The dynamic vasa vasorum","volume":"75","author":"Ritman","year":"2007","journal-title":"Cardiovasc. Res."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"11906","DOI":"10.1073\/pnas.1002569107","article-title":"Improved IL-2 immunotherapy by selective stimulation of IL-2 receptors on lymphocytes and endothelial cells","volume":"107","author":"Krieg","year":"2010","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Makarova, Y.A., Ryabkova, V.A., Salukhov, V.V., Sagun, B.V., Korovin, A.E., and Churilov, L.P. (2023). Atherosclerosis, Cardiovascular Disorders and COVID-19: Comorbid Pathogenesis. Diagnostics, 13.","DOI":"10.3390\/diagnostics13030478"},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Vasuri, F., Ciavarella, C., Collura, S., Mascoli, C., Valente, S., Degiovanni, A., Gargiulo, M., Capri, M., and Pasquinelli, G. (2021). Adventitial Microcirculation Is a Major Target of SARS-CoV-2-Mediated Vascular Inflammation. Biomolecules, 11.","DOI":"10.3390\/biom11071063"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1648","DOI":"10.1161\/CIRCULATIONAHA.120.046941","article-title":"COVID-19 and Cardiovascular Disease","volume":"141","author":"Clerkin","year":"2020","journal-title":"Circulation"},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Mures, A.V., H\u0103lmaciu, I., Arb\u0103nas, E.V., Kaller, R., Arb\u0103nas, E.M., Budis, O.A., Melinte, R.M., Vunvulea, V., Rares, C.F., and M\u0103rginean, L. (2022). Prognostic Nutritional Index, Controlling Nutritional Status (CONUT) Score, and Inflammatory Biomarkers as Predictors of Deep Vein Thrombosis, Acute Pulmonary Embolism, and Mortality in COVID-19 Patients. Diagnostics, 12.","DOI":"10.3390\/diagnostics12112757"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1056\/NEJMoa0912321","article-title":"Stenting versus endarterectomy for treatment of carotid-artery stenosis","volume":"363","author":"Brott","year":"2010","journal-title":"N. Engl. J. Med."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"242","DOI":"10.1056\/NEJM199201233260406","article-title":"The pathogenesis of coronary artery disease and the acute coronary syndromes (1)","volume":"326","author":"Fuster","year":"1992","journal-title":"N. Engl. J. Med."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"310","DOI":"10.1056\/NEJM199201303260506","article-title":"The pathogenesis of coronary artery disease and the acute coronary syndromes (2)","volume":"326","author":"Fuster","year":"1992","journal-title":"N. Engl. J. Med."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"497","DOI":"10.1016\/S0140-6736(20)30183-5","article-title":"Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China","volume":"395","author":"Huang","year":"2020","journal-title":"Lancet"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"640","DOI":"10.1016\/j.cardiores.2007.06.023","article-title":"The role of the adventitia in vascular inflammation","volume":"75","author":"Maiellaro","year":"2007","journal-title":"Cardiovasc. Res."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"325","DOI":"10.5551\/jat.E489","article-title":"Distribution of inflammatory cells in adventitia changed with advancing atherosclerosis of human coronary artery","volume":"14","author":"Watanabe","year":"2007","journal-title":"J. Atheroscler. Thromb."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"2096","DOI":"10.1007\/s42399-020-00558-9","article-title":"Kawasaki Disease and Multisystem Inflammatory Syndrome in Children with COVID-19","volume":"2","author":"Sarzaeim","year":"2020","journal-title":"SN Compr. Clin. Med."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1728","DOI":"10.1093\/rheumatology\/ken329","article-title":"Vasa-vasoritis of the aorta and fatal myocarditis in fulminant Churg-Strauss syndrome","volume":"47","author":"Hervier","year":"2008","journal-title":"Rheumatology"},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Numano, F. (2000). Vasa vasoritis, vasculitis and atherosclerosis. Int. J. Cardiol., 75.","DOI":"10.1016\/S0167-5273(00)00196-0"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"802","DOI":"10.1001\/jamacardio.2020.0950","article-title":"Association of Cardiac Injury with Mortality in Hospitalized Patients with COVID-19 in Wuhan, China","volume":"5","author":"Shi","year":"2020","journal-title":"JAMA Cardiol."}],"container-title":["Diagnostics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2075-4418\/13\/6\/1097\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T18:54:48Z","timestamp":1760122488000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2075-4418\/13\/6\/1097"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,3,14]]},"references-count":43,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2023,3]]}},"alternative-id":["diagnostics13061097"],"URL":"https:\/\/doi.org\/10.3390\/diagnostics13061097","relation":{},"ISSN":["2075-4418"],"issn-type":[{"type":"electronic","value":"2075-4418"}],"subject":[],"published":{"date-parts":[[2023,3,14]]}}}