{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T01:16:03Z","timestamp":1760145363459,"version":"build-2065373602"},"reference-count":50,"publisher":"MDPI AG","issue":"7","license":[{"start":{"date-parts":[[2024,7,17]],"date-time":"2024-07-17T00:00:00Z","timestamp":1721174400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Diseases"],"abstract":"<jats:p>Background: Cirrhosis causes an imbalance in the coagulation pathway and leads to a tendency for both bleeding and clotting. SARS-CoV-2 has been reported to be associated with a hypercoagulable state. This study examines SARS-CoV-2\u2019s impact on hemostasis in compensated patients with cirrhosis. Methods: We analyzed the US Collaborative Network, which comprises 63 HCOs in the U.S.A. Compensated cirrhosis patients were split into two groups: SARS-CoV-2-positive and -negative. Patients\u2019 baseline characteristics were used in a 1:1 propensity score-matched module to create comparable cohorts. We compared the risk of portal vein thrombosis (PVT), deep venous thrombosis (DVT), and pulmonary embolism (PE) at 6 months, and 1 and 3 years. Results: Of 330,521 patients, 27% tested positive and 73% remained negative. After PSM, both cohorts included 74,738 patients. Patients with SARS-CoV-2 had a higher rate of PVT compared to those without at 6 months (0.63% vs 0.5%, p &lt; 0.05), 1 year (0.8% vs 0.6%, p &lt; 0.05), and 3 years (1% vs. 0.7%, p &lt; 0.05), a higher rate of DVT at 6 months (0.8% vs. 0.4%, p &lt; 0.05), 1 year (1% vs. 0.5%, p &lt; 0.05), and 3 years (1.4% vs. 0.8%, p &lt; 0.05), and a higher rate of PE at 6 months (0.6% vs. 0.3%, p &lt; 0.05), 1 year (0.7% vs. 0.4%, p &lt; 0.05), and 3 years (1% vs. 0.6%, p &lt; 0.05). Conclusions: The presence of SARS-CoV-2 infection in patients with compensated cirrhosis was associated with a higher rate of PVT, DVT, and PE at 6 months, and 1 and 3 years.<\/jats:p>","DOI":"10.3390\/diseases12070161","type":"journal-article","created":{"date-parts":[[2024,7,17]],"date-time":"2024-07-17T15:15:19Z","timestamp":1721229319000},"page":"161","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Thrombotic Long-Term Consequences of SARS-CoV-2 Infection in Patients with Compensated Cirrhosis: A Propensity Score-Matched Analysis of a U.S. Database"],"prefix":"10.3390","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0009-0002-6518-3971","authenticated-orcid":false,"given":"Mark","family":"Ayoub","sequence":"first","affiliation":[{"name":"Department of Internal Medicine, Charleston Area Medical Center, West Virginia University, Charleston, WV 25304, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Carol","family":"Faris","sequence":"additional","affiliation":[{"name":"Department of Internal Medicine, Bayonne Medical Center, Bayonne, NJ 07002, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Tajana","family":"Juranovic","sequence":"additional","affiliation":[{"name":"Department of Internal Medicine, Charleston Area Medical Center, West Virginia University, Charleston, WV 25304, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3222-9454","authenticated-orcid":false,"given":"Rafi","family":"Aibani","sequence":"additional","affiliation":[{"name":"Department of Internal Medicine, Charleston Area Medical Center, West Virginia University, Charleston, WV 25304, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Morgan","family":"Koontz","sequence":"additional","affiliation":[{"name":"Health Services & Outcomes Research, CAMC-WVU Academic Medical Center, Charleston, WV 25304, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Harleen","family":"Chela","sequence":"additional","affiliation":[{"name":"Division of Gastroenterology and Hepatology, Charleston Area Medical Center, West Virginia University, Charleston, WV 25304, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Nadeem","family":"Anwar","sequence":"additional","affiliation":[{"name":"Division of Gastroenterology and Hepatology, Charleston Area Medical Center, West Virginia University, Charleston, WV 25304, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0622-1704","authenticated-orcid":false,"given":"Ebubekir","family":"Daglilar","sequence":"additional","affiliation":[{"name":"Division of Gastroenterology and Hepatology, Charleston Area Medical Center, West Virginia University, Charleston, WV 25304, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2024,7,17]]},"reference":[{"key":"ref_1","unstructured":"(2024, March 24). COVID-19 Cases|WHO COVID-19 Dashboard. Available online: https:\/\/data.who.int\/dashboards\/covid19\/cases?n=c."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"2033","DOI":"10.1182\/blood.2020006000","article-title":"COVID-19 and its implications for thrombosis and anticoagulation","volume":"135","author":"Connors","year":"2020","journal-title":"Blood"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1178","DOI":"10.1002\/rth2.12439","article-title":"Risk of venous thromboembolism in patients with COVID-19: A systematic review and meta-analysis","volume":"4","author":"Nopp","year":"2020","journal-title":"Res. Pract. Thromb. Haemost."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1859","DOI":"10.1111\/jth.14929","article-title":"Scientific and Standardization Committee communication: Clinical guidance on the diagnosis, prevention, and treatment of venous thromboembolism in hospitalized patients with COVID-19","volume":"18","author":"Spyropoulos","year":"2020","journal-title":"J. Thromb. Haemost."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"872","DOI":"10.1182\/bloodadvances.2020003763","article-title":"American Society of Hematology 2021 guidelines on the use of anticoagulation for thromboprophylaxis in patients with COVID-19","volume":"5","author":"Cuker","year":"2021","journal-title":"Blood Adv."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"997","DOI":"10.1001\/jamainternmed.2021.0488","article-title":"Incidence of 30-Day Venous Thromboembolism in Adults Tested for SARS-CoV-2 Infection in an Integrated Health Care System in Northern California","volume":"181","author":"Roubinian","year":"2021","journal-title":"JAMA Intern. Med."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"e12530","DOI":"10.1002\/emp2.12530","article-title":"Risk of venous thromboembolism in a Swedish healthcare system during the COVID-19 pandemic: A retrospective cross-sectional study","volume":"2","author":"Wretborn","year":"2021","journal-title":"J. Am. Coll. Emerg. Physicians Open"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"811","DOI":"10.1111\/acem.14096","article-title":"Association Between Pulmonary Embolism and COVID-19 in Emergency Department Patients Undergoing Computed Tomography Pulmonary Angiogram: The PEPCOV International Retrospective Study","volume":"27","author":"Freund","year":"2020","journal-title":"Acad. Emerg. Med."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1703","DOI":"10.1001\/jama.2021.17272","article-title":"Effect of Antithrombotic Therapy on Clinical Outcomes in Outpatients with Clinically Stable Symptomatic COVID-19: The ACTIV-4B Randomized Clinical Trial","volume":"326","author":"Connors","year":"2021","journal-title":"JAMA"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1","DOI":"10.15761\/JTS.1000182","article-title":"Hemostasis, bleeding and thrombosis in liver disease","volume":"3","author":"Flores","year":"2017","journal-title":"J. Transl. Sci."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Ayoub, M., Tomanguillo, J., Faris, C., Anwar, N., Chela, H., and Daglilar, E. (2024). SARS-CoV-2 Infection Is an Independent Risk Factor for Decompensation in Cirrhosis Patients. Diseases, 12.","DOI":"10.3390\/diseases12030046"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1016\/j.amjmed.2017.09.015","article-title":"Is Infection an Independent Risk Factor for Venous Thromboembolism? A Population-Based, Case-Control Study","volume":"131","author":"Cohoon","year":"2018","journal-title":"Am. J. Med."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1904","DOI":"10.3390\/cimb46030124","article-title":"COVID-19 Associated Cardiovascular Disease\u2014Risks, Prevention and Management: Heart at Risk Due to COVID-19","volume":"46","author":"Kemerley","year":"2024","journal-title":"Curr. Issues Mol. Biol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1111\/ijlh.13500","article-title":"COVID-19: Thrombosis, thromboinflammation, and anticoagulation considerations","volume":"43","author":"Levy","year":"2021","journal-title":"Int. J. Lab. Hematol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"155","DOI":"10.14797\/mdcj-16-2-155","article-title":"COVID-19: A Potential Risk Factor for Acute Pulmonary Embolism","volume":"16","author":"Martin","year":"2020","journal-title":"Methodist DeBakey Cardiovasc. J."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1016\/j.thromres.2020.04.011","article-title":"Pulmonary embolism in patients with COVID-19: Time to change the paradigm of computed tomography","volume":"190","author":"Rotzinger","year":"2020","journal-title":"Thromb. Res."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1858","DOI":"10.1093\/eurheartj\/ehaa254","article-title":"Acute pulmonary embolism and COVID-19 pneumonia: A random association?","volume":"41","author":"Danzi","year":"2020","journal-title":"Eur. Heart J."},{"key":"ref_18","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":"2020","journal-title":"Trends Cardiovasc. Med."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"e14340","DOI":"10.1111\/ijcp.14340","article-title":"Imaging approach to COVID-19 associated pulmonary embolism","volume":"75","author":"Trunz","year":"2021","journal-title":"Int. J. Clin. Pract."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"e32887","DOI":"10.1097\/MD.0000000000032887","article-title":"Pulmonary embolism in COVID-19, risk factors and association with inflammatory biomarkers","volume":"102","author":"Yousaf","year":"2023","journal-title":"Medicine"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1016\/j.hrtlng.2022.02.003","article-title":"High incidence of pulmonary thromboembolism in hospitalized SARS-CoV-2 infected patients despite thrombo-prophylaxis","volume":"53","author":"Barreda","year":"2022","journal-title":"Heart Lung"},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Lobbes, H., Mainbourg, S., Mai, V., Douplat, M., Provencher, S., and Lega, J.-C. (2021). Risk factors for venous thromboembolism in severe COVID-19: A study-level meta-analysis of 21 studies. Int. J. Environ. Res. Public Health, 18.","DOI":"10.3390\/ijerph182412944"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"225","DOI":"10.3390\/hematolrep15020024","article-title":"Risk of Thrombosis during and after a SARS-CoV-2 Infection: Pathogenesis, Diagnostic Approach, and Management","volume":"15","author":"Sutanto","year":"2023","journal-title":"Hematol. Rep."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"7161","DOI":"10.3390\/cimb45090453","article-title":"Pathological Effects of SARS-CoV-2 Associated with Hematological Abnormalities","volume":"45","author":"Shama","year":"2023","journal-title":"Curr. Issues Mol. Biol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1016\/j.thromres.2019.07.013","article-title":"The stimulation of thrombosis by hypoxia","volume":"181","author":"Gupta","year":"2019","journal-title":"Thromb. Res."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1738","DOI":"10.1111\/jth.14850","article-title":"Hypercoagulability of COVID-19 patients in intensive care unit: A report of thromboelastography findings and other parameters of hemostasis","volume":"18","author":"Panigada","year":"2020","journal-title":"J. Thromb. Haemost."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"The Lancet Haematology (2020). COVID-19 coagulopathy: An evolving story. Lancet Haematol., 7, e425.","DOI":"10.1016\/S2352-3026(20)30151-4"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1743","DOI":"10.1111\/jth.14869","article-title":"High incidence of venous thromboembolic events in anticoagulated severe COVID-19 patients","volume":"18","author":"Llitjos","year":"2020","journal-title":"J. Thromb. Haemost."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1177\/17539447221105013","article-title":"Predictors and mortality risk of venous thromboembolism in patients with COVID-19: Systematic review and meta-analysis of observational studies","volume":"16","author":"Agarwal","year":"2022","journal-title":"Ther. Adv. Cardiovasc. Dis."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"101061","DOI":"10.1016\/j.eclinm.2021.101061","article-title":"Cerebral venous thrombosis and portal vein thrombosis: A retrospective cohort study of 537,913 COVID-19 cases","volume":"39","author":"Taquet","year":"2021","journal-title":"EClinicalMedicine"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1155\/2022\/5900468","article-title":"COVID-19 in Cirrhotic Patients: Is Portal Vein Thrombosis a Potential Complication?","volume":"2022","author":"Hassnine","year":"2022","journal-title":"Can. J. Gastroenterol. Hepatol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"132","DOI":"10.1016\/j.thromres.2020.12.024","article-title":"Systemic thrombosis in a large cohort of COVID-19 patients despite thromboprophylaxis: A retrospective study","volume":"199","year":"2021","journal-title":"Thromb. Res."},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Mu\u00f1oz-Rivas, N., Aibar, J., Gabara-Xanc\u00f3, C., Trueba-Vicente, \u00c1., Urbelz-P\u00e9rez, A., Olmo, V.G.-D., Demelo-Rodr\u00edguez, P., Rivera-Gallego, A., Bosch-Nicolau, P., and Perez-Pinar, M. (2022). Efficacy and Safety of Tinzaparin in Prophylactic, Intermediate and Thera-peutic Doses in Non-Critically Ill Patients Hospitalized with COVID-19: The PROTHROMCOVID Randomized Controlled Trial. J. Clin. Med., 11.","DOI":"10.1101\/2022.05.03.22274594"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1182\/blood.2020006520","article-title":"COVID-19 and coagulation: Bleeding and thrombotic manifestations of SARS-CoV-2 infection","volume":"136","author":"Leaf","year":"2020","journal-title":"Blood"},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Zhang, B., Zhou, X., Qiu, Y., Song, Y., Feng, F., Feng, J., Song, Q., Jia, Q., and Wang, J. (2020). Clinical characteristics of 82 cases of death from COVID-19. PLoS ONE, 15.","DOI":"10.1371\/journal.pone.0235458"},{"key":"ref_36","first-page":"1182","article-title":"Incidence of VTE and Bleeding Among Hospitalized Patients with Coronavirus Disease 2019: A Systematic Review and Meta-analysis","volume":"159","author":"Rali","year":"2020","journal-title":"Chest"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1831","DOI":"10.1053\/j.gastro.2020.02.055","article-title":"Evidence for Gastrointestinal Infection of SARS-CoV-2","volume":"158","author":"Xiao","year":"2020","journal-title":"Gastroenterology"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"184","DOI":"10.1182\/blood.2021012247","article-title":"Clinical features of thrombosis and bleeding in COVID-19","volume":"140","author":"Thomas","year":"2022","journal-title":"Blood"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"e403","DOI":"10.1097\/TXD.0000000000000843","article-title":"Hypercoagulability in End-stage Liver Disease: Review of Epidemiology, Etiology, and Management","volume":"4","author":"Verbeek","year":"2018","journal-title":"Transplant. Direct"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1154","DOI":"10.1111\/j.1365-2036.2010.04454.x","article-title":"The epidemiology and clinical features of portal vein thrombosis: A multicentre study","volume":"32","author":"Rajani","year":"2010","journal-title":"Aliment. Pharmacol. Ther."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"e13074","DOI":"10.1002\/jgh3.13074","article-title":"Safety of DOACs in patients with Child-Pugh Class C cirrhosis and trial fibrillation","volume":"8","author":"Ayoub","year":"2024","journal-title":"JGH Open"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1332","DOI":"10.1016\/j.jhep.2017.07.001","article-title":"Changes in hemostasis in liver disease","volume":"67","author":"Intagliata","year":"2017","journal-title":"J. Hepatol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1417","DOI":"10.1016\/S0140-6736(20)30937-5","article-title":"Endothelial cell infection and endotheliitis in COVID-19","volume":"395","author":"Varga","year":"2020","journal-title":"Lancet"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"3022","DOI":"10.3748\/wjg.v27.i22.3022","article-title":"Liver injury in COVID-19: Detection, pathogenesis, and treatment","volume":"27","author":"Cai","year":"2021","journal-title":"World J. Gastroenterol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"998","DOI":"10.1055\/s-0040-1714350","article-title":"COVID-19-Related Severe Hypercoagulability in Patients Admitted to Intensive Care Unit for Acute Respiratory Failure","volume":"120","author":"Spiezia","year":"2020","journal-title":"Thromb. Haemost."},{"key":"ref_46","first-page":"3017","article-title":"Portal vein thrombosis in patients with COVID-19: A systematic review","volume":"46","author":"Elfarargy","year":"2022","journal-title":"Asian J. Surg."},{"key":"ref_47","unstructured":"Samant, H., Asafo-Agyei, K.O., and Garfield, K. (2021). Portal Vein Thrombosis, Springer Nature."},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Boccatonda, A., Gentilini, S., Zanata, E., Simion, C., Serra, C., Simioni, P., Piscaglia, F., Campello, E., and Ageno, W. (2024). Portal Vein Thrombosis: State-of-the-Art Review. J. Clin. Med., 13.","DOI":"10.3390\/jcm13051517"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"e069590","DOI":"10.1136\/bmj-2021-069590","article-title":"Risks of deep vein thrombosis, pulmonary embolism, and bleeding after COVID-19: Nationwide self-controlled cases series and matched cohort study","volume":"377","author":"Katsoularis","year":"2022","journal-title":"BMJ"},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"Papic, I., Bistrovic, P., Cikara, T., Busic, N., Keres, T., Hadziabdic, M.O., and Lucijanic, M. (2024). Corticosteroid Dosing Level, Incidence and Profile of Bacterial Blood Stream Infections in Hospitalized COVID-19 Patients. Viruses, 16.","DOI":"10.3390\/v16010086"}],"container-title":["Diseases"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2079-9721\/12\/7\/161\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T15:18:32Z","timestamp":1760109512000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2079-9721\/12\/7\/161"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,7,17]]},"references-count":50,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2024,7]]}},"alternative-id":["diseases12070161"],"URL":"https:\/\/doi.org\/10.3390\/diseases12070161","relation":{},"ISSN":["2079-9721"],"issn-type":[{"type":"electronic","value":"2079-9721"}],"subject":[],"published":{"date-parts":[[2024,7,17]]}}}