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      COVID-19 and Thrombotic or Thromboembolic Disease: Implications for Prevention, Antithrombotic Therapy, and Follow-up

      review-article
      , MD, MS 1 , 2 , 3 , # , , , MD 1 , 3 , ## , , , MD, PhD 4 , , PharmD 1 , , MD 1 , , MD 1 , , PharmD 1 , , MD 5 , , MD, MS 6 , , MD, PhD 7 , , MD 8 , , MD 8 , , MD, MPH 9 , 10 , 11 , , MD, MSc 12 , , MD, PhD 13 , , MD 14 , , MD 15 , 16 , , MD 17 , , PhD 18 , 19 , , PhD 20 , , MD, MS 21 , , MD, MS 21 , 22 , , BS 1 , , MPH 3 , , MD 1 , , MD 23 , , MD 24 , , MD 25 , , MD 26 , , MD, MSc 27 , 28 , , MBBS 29 , , MD 30 , , MD, PhD 31 , 43 , 44 , , MD, MSc 32 , , MD, MS 15 , 33 , , MD 34 , , MD 35 , 36 , 37 , , MD 3 , 38 , , MD 39 , , MD 15 , 33 , , MD 1 , 3 , , MD, PhD 40 , , MD, SM 2 , 41 , , MD, PhD 42 , , MD 43 , 44 , , MD 45 , 46
      Journal of the American College of Cardiology
      Published by Elsevier on behalf of the American College of Cardiology Foundation.
      Coronavirus disease 2019, SARS-CoV-2, thrombosis, antithrombotic therapy, anticoagulant, antiplatelet, ACS, acute coronary syndromes, COVID-19, coronavirus disease 2019, DAPT, dual antiplatelet therapy, DIC, disseminated intravascular coagulation, DOAC, direct oral anticoagulant, DVT, deep vein thrombosis, ECMO, extracorporeal membrane oxygenation, LMWH, low-molecular-weight heparin, PE, pulmonary embolism, PERTs, pulmonary embolism response teams, SARS-CoV2, severe acute respiratory syndrome coronavirus 2, STEMI, ST-segment elevation myocardial infarction, UFH, unfractionated heparin, VEGF, vascular endothelial growth factor, VKA, vitamin-K antagonist, VTE, venous thromboembolism

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          Abstract

          Coronavirus disease 2019 (COVID-19), a viral respiratory illness caused by the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), may predispose patients to thrombotic disease, both in the venous and arterial circulations, due to excessive inflammation, platelet activation, endothelial dysfunction, and stasis. In addition, many patients receiving antithrombotic therapy for thrombotic disease may develop COVID-19, which can have implications for choice, dosing, and laboratory monitoring of antithrombotic therapy. Moreover, during a time with much focus on COVID-19, it is critical to consider how to optimize the available technology to care for patients without COVID-19 who have thrombotic disease. Herein, we review the current understanding of the pathogenesis, epidemiology, management and outcomes of patients with COVID-19 who develop venous or arterial thrombosis, and of those with preexisting thrombotic disease who develop COVID-19, or those who need prevention or care for their thrombotic disease during the COVID-19 pandemic.

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          Author and article information

          Contributors
          Journal
          J Am Coll Cardiol
          J. Am. Coll. Cardiol
          Journal of the American College of Cardiology
          Published by Elsevier on behalf of the American College of Cardiology Foundation.
          0735-1097
          1558-3597
          17 April 2020
          17 April 2020
          Affiliations
          [1 ]NewYork-Presbyterian Hospital/Columbia University Irving Medical Center, New York, New York
          [2 ]Center for Outcomes Research and Evaluation (CORE), Yale School of Medicine, New Haven, Connecticut
          [3 ]Clinical Trials Center, Cardiovascular Research Foundation, New York, New York
          [4 ]Respiratory Department, Hospital Ramón y Cajal and Medicine Department, Universidad de Alcalá (IRYCIS), CIBER de Enfermedades Respiratorias (CIBERES), Madrid, Spain
          [5 ]Department of Medicine and Surgery, University of Insubria, Varese, Italy
          [6 ]McGovern Medical School at The University of Texas Health Science Center at Houston, Houston, Texas
          [7 ]Department of Cardiology, Chinese PLA General Hospital, Beijing, China
          [8 ]Institute of Hematology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China
          [9 ]Cardiovascular Division, Hospital of the University of Pennsylvania, Philadelphia
          [10 ]Penn Cardiovascular Outcomes, Quality, and Evaluative Research Center, Leonard Davis Institute of Health Economics, University of Pennsylvania, Philadelphia
          [11 ]Corporal Michael J. Crescenz VA Medical Center, Philadelphia, Pennsylvania
          [12 ]The University of Vermont Medical Center, Burlington, Vermont
          [13 ]Department of Vascular Medicine, University of Montpellier, Montpellier CHU, InnoVTE F-CRIN network, Montpellier, France
          [14 ]Oncology Unit GPP, Sotiria General Hospital Athens School of Medicine, Athens, Greece
          [15 ]Harvard Medical School, Boston, Massachusetts
          [16 ]Beth Israel Deaconess Medical Center, Boston, Massachusetts
          [17 ]Laboratory of Clinical Chemistry and Hematology, University Hospital of Verona, Verona, Italy
          [18 ]Laboratory Haematology, Institute of Clinical Pathology and Medical Research (ICPMR), NSW Health Pathology, Westmead Hospital, Westmead, NSW, Australia
          [19 ]Sydney Centres for Thrombosis and Haemostasis, Westmead, NSW, Australia
          [20 ]Loyola University Medical Center, Chicago, Illinois
          [21 ]Pritzker School of Medicine at the University of Chicago, Chicago, Illinois
          [22 ]Division of Vascular Medicine, Department of Medicine, NorthShore University HealthSystem, Skokie, Illinois
          [23 ]University of Milan Bicocca, Monza, Department of Immunohematology and Transfusion Medicine, Hospital Papa Giovanni XXIII, Bergamo, Italy
          [24 ]Auckland City Hospital, Auckland, New Zealand
          [25 ]St Thomas’ Hospital, London, United Kingdom
          [26 ]The Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, New York, New York
          [27 ]Center for Bioethics and Social Science in Medicine
          [28 ]Frankel Cardiovascular Center, University of Michigan, Ann Arbor, Michigan
          [29 ]Population Health Research Institute, McMaster University and Hamilton Health Sciences, Hamilton, Ontario, Canada
          [30 ]Massachusetts General Hospital, Boston, Massachusetts
          [31 ]Department of Obstetrics and Gynecology, I.M. Sechenov First Moscow State Medical University, Moscow, Russia
          [32 ]The Ottawa Hospital Research Institute, Ottawa, Ontario, Canada
          [33 ]Brigham and Women’s Hospital, Boston, Massachusetts
          [34 ]Vanderbilt University School of Medicine, Nashville, Tennessee
          [35 ]FACT (French Alliance for Cardiovascular Trials), Assistance Publique-Hôpitaux de Paris, Hôpital Bichat, INSERM U1148, Paris, France
          [36 ]Université Paris, Paris, France
          [37 ]Imperial College, Royal Brompton Hospital, London, United Kingdom
          [38 ]The Zena and Michael A. Wiener Cardiovascular Institute, Icahn School of Medicine at Mount Sinai, New York, New York
          [39 ]Department of Cardiology, Heart Center at the University of Cologne, and Cologne Cardiovascular Research Center (CCRC), University of Cologne, Germany
          [40 ]Department of Internal Medicine, Hospital Universitari Germans Trials I Pujol, Universidad Católica de Murcia, Barcelona, Spain
          [41 ]Department of Health Policy and Administration, Yale School of Public Health, New Haven, Connecticut
          [42 ]Center for Thrombosis and Hemostasis, Johannes Gutenberg University of Mainz, Mainz, Germany
          [43 ]McMaster University, Hamilton, Ontario, Canada
          [44 ]Thrombosis & Atherosclerosis Research Institute, Hamilton, Ontario, Canada
          [45 ]Liverpool Centre for Cardiovascular Science, University of Liverpool and Liverpool Heart & Chest Hospital, Liverpool, United Kingdom
          [46 ]Aalborg University, Aalborg, Denmark
          Author notes
          [# ]Corresponding Author: Behnood Bikdeli, MD, MS New York-Presbyterian Hospital/ Columbia University Irving Medical Center 622 West 168th St, PH 3-347, New York, NY 10032 Phone/ Fax: 212-305-6354, , Twitter handle: @bbikdeli. bb2813@ 123456cumc.columbia.edu Behnood.bikdeli@ 123456yale.edu
          [## ]Corresponding Author: Mahesh Vasantha Madhavan, MD, New York-Presbyterian Hospital/ Columbia University Irving Medical Center, 622 West 168th St, PH 3-347, New York, NY 10032, Phone/ Fax: 212-305-6354, , Twitter handle: @MVMadhavanMD. mvm2122@ 123456cumc.columbia.edu
          [∗]

          Drs. Bikdeli and Madhavan contributed equally to this manuscript.

          Article
          S0735-1097(20)35008-7
          10.1016/j.jacc.2020.04.031
          7164881
          32311448
          4d8e5fe4-73a0-4066-b295-9fc1f4e08b6b
          © 2020 Published by Elsevier on behalf of the American College of Cardiology Foundation.

          Since January 2020 Elsevier has created a COVID-19 resource centre with free information in English and Mandarin on the novel coronavirus COVID-19. The COVID-19 resource centre is hosted on Elsevier Connect, the company's public news and information website. Elsevier hereby grants permission to make all its COVID-19-related research that is available on the COVID-19 resource centre - including this research content - immediately available in PubMed Central and other publicly funded repositories, such as the WHO COVID database with rights for unrestricted research re-use and analyses in any form or by any means with acknowledgement of the original source. These permissions are granted for free by Elsevier for as long as the COVID-19 resource centre remains active.

          History
          : 15 April 2020
          : 15 April 2020
          Categories
          Article

          Cardiovascular Medicine
          coronavirus disease 2019,sars-cov-2,thrombosis,antithrombotic therapy,anticoagulant,antiplatelet,acs, acute coronary syndromes,covid-19, coronavirus disease 2019,dapt, dual antiplatelet therapy,dic, disseminated intravascular coagulation,doac, direct oral anticoagulant,dvt, deep vein thrombosis,ecmo, extracorporeal membrane oxygenation,lmwh, low-molecular-weight heparin,pe, pulmonary embolism,perts, pulmonary embolism response teams,sars-cov2, severe acute respiratory syndrome coronavirus 2,stemi, st-segment elevation myocardial infarction,ufh, unfractionated heparin,vegf, vascular endothelial growth factor,vka, vitamin-k antagonist,vte, venous thromboembolism

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