Author + information
- Received April 15, 2020
- Accepted April 15, 2020
- Published online April 17, 2020.
- Behnood Bikdeli, MD, MS1,2,3,#∗ ( )(, )
- Mahesh V. Madhavan, MD1,3,##∗ (, )
- David Jimenez, MD, PhD4,
- Taylor Chuich, PharmD1,
- Isaac Dreyfus, MD1,
- Elissa Driggin, MD1,
- Caroline Der Nigoghossian, PharmD1,
- Walter Ageno, MD5,
- Mohammad Madjid, MD, MS6,
- Yutao Guo, MD, PhD7,
- Liang V. Tang, MD8,
- Yu Hu, MD8,
- Jay Giri, MD, MPH9,10,11,
- Mary Cushman, MD, MSc12,
- Isabelle Quéré, MD, PhD13,
- Evangelos P. Dimakakos, MD14,
- C. Michael Gibson, MD15,16,
- Giuseppe Lippi, MD17,
- Emmanuel J. Favaloro, PhD18,19,
- Jawed Fareed, PhD20,
- Joseph A. Caprini, MD, MS21,
- Alfonso J. Tafur, MD, MS21,22,
- John R. Burton, BS1,
- Dominic P. Francese, MPH3,
- Elizabeth Y. Wang, MD1,
- Anna Falanga, MD23,
- Claire McLintock, MD24,
- Beverley J. Hunt, MD25,
- Alex C. Spyropoulos, MD26,
- Geoffrey D. Barnes, MD, MSc27,28,
- John W. Eikelboom, MBBS29,
- Ido Weinberg, MD30,
- Sam Schulman, MD, PhD31,43,44,
- Marc Carrier, MD, MSc32,
- Gregory Piazza, MD, MS15,33,
- Joshua A. Beckman, MD34,
- P. Gabriel Steg, MD35,36,37,
- Gregg W. Stone, MD3,38,
- Stephan Rosenkranz, MD39,
- Samuel Z. Goldhaber, MD15,33,
- Sahil A. Parikh, MD1,3,
- Manuel Monreal, MD, PhD40,
- Harlan M. Krumholz, MD, SM2,41,
- Stavros V. Konstantinides, MD, PhD42,
- Jeffrey I. Weitz, MD43,44 and
- Gregory Y.H. Lip, MD45,46
- 1NewYork-Presbyterian Hospital/Columbia University Irving Medical Center, New York, New York
- 2Center for Outcomes Research and Evaluation (CORE), Yale School of Medicine, New Haven, Connecticut
- 3Clinical Trials Center, Cardiovascular Research Foundation, New York, New York
- 4Respiratory Department, Hospital Ramón y Cajal and Medicine Department, Universidad de Alcalá (IRYCIS), CIBER de Enfermedades Respiratorias (CIBERES), Madrid, Spain
- 5Department of Medicine and Surgery, University of Insubria, Varese, Italy
- 6McGovern Medical School at The University of Texas Health Science Center at Houston, Houston, Texas
- 7Department of Cardiology, Chinese PLA General Hospital, Beijing, China
- 8Institute of Hematology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China
- 9Cardiovascular Division, Hospital of the University of Pennsylvania, Philadelphia
- 10Penn Cardiovascular Outcomes, Quality, and Evaluative Research Center, Leonard Davis Institute of Health Economics, University of Pennsylvania, Philadelphia
- 11Corporal Michael J. Crescenz VA Medical Center, Philadelphia, Pennsylvania
- 12The University of Vermont Medical Center, Burlington, Vermont
- 13Department of Vascular Medicine, University of Montpellier, Montpellier CHU, InnoVTE F-CRIN network, Montpellier, France
- 14Oncology Unit GPP, Sotiria General Hospital Athens School of Medicine, Athens, Greece
- 15Harvard Medical School, Boston, Massachusetts
- 16Beth Israel Deaconess Medical Center, Boston, Massachusetts
- 17Laboratory of Clinical Chemistry and Hematology, University Hospital of Verona, Verona, Italy
- 18Laboratory Haematology, Institute of Clinical Pathology and Medical Research (ICPMR), NSW Health Pathology, Westmead Hospital, Westmead, NSW, Australia
- 19Sydney Centres for Thrombosis and Haemostasis, Westmead, NSW, Australia
- 20Loyola University Medical Center, Chicago, Illinois
- 21Pritzker School of Medicine at the University of Chicago, Chicago, Illinois
- 22Division of Vascular Medicine, Department of Medicine, NorthShore University HealthSystem, Skokie, Illinois
- 23University of Milan Bicocca, Monza, Department of Immunohematology and Transfusion Medicine, Hospital Papa Giovanni XXIII, Bergamo, Italy
- 24Auckland City Hospital, Auckland, New Zealand
- 25St Thomas’ Hospital, London, United Kingdom
- 26The Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, New York, New York
- 27Center for Bioethics and Social Science in Medicine
- 28Frankel Cardiovascular Center, University of Michigan, Ann Arbor, Michigan
- 29Population Health Research Institute, McMaster University and Hamilton Health Sciences, Hamilton, Ontario, Canada
- 30Massachusetts General Hospital, Boston, Massachusetts
- 31Department of Obstetrics and Gynecology, I.M. Sechenov First Moscow State Medical University, Moscow, Russia
- 32The Ottawa Hospital Research Institute, Ottawa, Ontario, Canada
- 33Brigham and Women’s Hospital, Boston, Massachusetts
- 34Vanderbilt University School of Medicine, Nashville, Tennessee
- 35FACT (French Alliance for Cardiovascular Trials), Assistance Publique-Hôpitaux de Paris, Hôpital Bichat, INSERM U1148, Paris, France
- 36Université Paris, Paris, France
- 37Imperial College, Royal Brompton Hospital, London, United Kingdom
- 38The Zena and Michael A. Wiener Cardiovascular Institute, Icahn School of Medicine at Mount Sinai, New York, New York
- 39Department of Cardiology, Heart Center at the University of Cologne, and Cologne Cardiovascular Research Center (CCRC), University of Cologne, Germany
- 40Department of Internal Medicine, Hospital Universitari Germans Trials I Pujol, Universidad Católica de Murcia, Barcelona, Spain
- 41Department of Health Policy and Administration, Yale School of Public Health, New Haven, Connecticut
- 42Center for Thrombosis and Hemostasis, Johannes Gutenberg University of Mainz, Mainz, Germany
- 43McMaster University, Hamilton, Ontario, Canada
- 44Thrombosis & Atherosclerosis Research Institute, Hamilton, Ontario, Canada
- 45Liverpool Centre for Cardiovascular Science, University of Liverpool and Liverpool Heart & Chest Hospital, Liverpool, United Kingdom
- 46Aalborg University, Aalborg, Denmark
- ↵#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.
- ↵##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.
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.
↵∗ Drs. Bikdeli and Madhavan contributed equally to this manuscript.
Endorsed by the International Society on Thrombosis and Haemostasis (ISTH), the North American Thrombosis Forum (NATF), the European Society of Vascular Medicine (ESVM), and the International Union of Angiology (IUA). Supported by the ESC Working Group on the Pulmonary Circulation and Right Ventricular Function (SR, SK).
Dr. Bikdeli reports that he is a consulting expert, on behalf of the plaintiff, for litigation related to a specific type of IVC filters.
Dr. Madhavan reports being supported by an institutional grant by the National Institutes of Health/ National Heart, Lung, and Blood Institute to Columbia University Irving Medical Center (T32 HL007854).
Dr. Jimenez has served as an advisor or consultant for Bayer HealthCare Pharmaceuticals, Boehringer Ingelheim, Bristol-Myers Squibb, Daiichi Sankyo, Leo Pharma, Pfizer, ROVI and Sanofi; served as a speaker or a member of a speakers’ bureau for Bayer HealthCare Pharmaceuticals, Boehringer Ingelheim, Bristol-Myers Squibb, Daiichi Sankyo, Leo Pharma, ROVI and Sanofi; received grants for clinical research from Daiichi Sankyo, Sanofi and ROVI. Dr. Hu has nothing to disclose.
Dr. Chuich has nothing to disclose.
Dr. Dreyfus has nothing to disclose.
Dr. Driggin has nothing to disclose.
Dr. Der Nigoghossian has nothing to disclose.
Dr. Tang has nothing to disclose.
Dr. Ageno has received honoraria from Boehringer Ingelheim, Bayer Pharmaceuticals, BMS-Pfizer, Daiichi-Sankyo, Aspen, Sanofi, Portola, Janssen. Research support from Bayer Pharmaceuticals.
Dr. Dimakakos receives consulting fees from Sanofi and Leo.
Dr. Lippi has nothing to disclose.
Dr. Favaloro has nothing to disclose.
Dr. Fareed has nothing to disclose.
Dr. Caprini: Steering committee – Janssen R&D; bleeding advisory board – Pfizer; honorarium – Sanofi; consultant – Recovery Force; advisory board – Bristol-Myers Squibb, Alexion Pharmaceuticals.
Dr. Cushman has nothing to disclose.
Dr. Barnes reports consulting for Pfizer/Bristol-Myers Squib, Janssen, Portola, and AMAG Pharmaceuticals. Grant funding from Pfizer/Bristol-Myers Squibb and Blue Cross Blue Shield of Michigan.
Dr. Cushman has nothing to disclose.
Dr. Giri is on the Advisory Boards for Astra Zeneca, Philips Medical, and Inari Medical, receives Research Grants to Institution from Recor Medical and St Jude Medical, and receives Personal Fees for Trial Adjudication from New England Research Institute.
Dr Quéré has received honoraria from Bayer Pharmaceuticals, BMS-Pfizer, Leo Pharma and Aspen.
Dr. Falanga reports being a speaker at corporate symposia for Bayer, Pfizer, and Sanofi.
Dr Spyropoulos reports receiving consulting fees from Boehringer Ingelheim, BMS, Janssen, Bayer, Portola, and the ATLAS Group, and research funding from Boehringer Ingelheim, and Janssen.
Dr. Carrier reports Research funding from BMS, LEO Pharma and Pfizer and consultancy honoraria from BMS, Bayer, Pfizer, LEO Pharma, Servier and Sanofi.
Dr McLintock has nothing to disclose.
Dr. Hunt reports she takes no monies in any form from pharmaceutical companies producing thrombotic drugs. She is chair of the steering group of World Thrombosis Day and Medical Director of Thrombosis UK; two non-for-profit organisations from which she takes no fees.
Dr. Weinberg reports consulting fees for Magneto thrombectomy solutions.
Dr. Piazza has received significant research grant support from BTG International, Bristol Myers Squibb, Daiichi-Sankyo, Bayer, Portola, and Janssen and modest consulting fees from Pfizer and Thrombolex.
Dr. Schulman reports research grants from Octapharma and Boehringer-Ingelheim and honoraria from Alnylam, Bayer, Boehringer-Ingelheim, Bristol-Myers Squibb, Daiichi-Sankyo and Sanofi.
Dr. Beckman is on the Advisory Boards for Amgen, Astra Zeneca, Glaxo Smith Kline, and Janssen, on the DSMB for Bayer, and Novartis, receives consulting fees from JanOne, and personal fees for Trial Adjudication from Sanofi.
Dr. Rosenkranz: reports remunerations for consultancy and/or lectures from Abbott, Acceleron, Actelion, AstraZeneca, Bayer, BMS, Janssen, MSD, Novartis, Pfizer, United Therapeutics. Research grants to institution from Actelion, AstraZeneca, Bayer, Novartis; Deutsche Forschungsgemeinschaft (DFG), Else-Bundesministerium für Bildung und Forschung (BMBF), Kröner-Fresenius-Stiftung (EKFS).
Dr. Steg reports receiving research grants from Amarin, Bayer, Sanofi, and Servier, and is in the Steering Committee, DSMB or CEC for clinical trials for: Amarin, AstraZeneca, Bayer, Boehringer Ingelheim, Bristol-Myers Squibb, Idorsia, Novartis, Pfizer, Sanofi, Servier, and receives speaker or consultant fees from: Amarin, AstraZeneca, Bayer, Boehringer Ingelheim, Bristol-Myers Squibb, Idorsia, Novartis, Pfizer, Sanofi, and Servier.
Dr. Stone has received speaker or other honoraria from Cook, Terumo, QOOL Therapeutics and Orchestra Biomed; has served as a consultant to Valfix, TherOx, Vascular Dynamics, Robocath, HeartFlow, Gore, Ablative Solutions, Miracor, Neovasc, V-Wave, Abiomed, Ancora, MAIA Pharmaceuticals, Vectorious, Reva, Matrizyme; and has equity/options from Ancora, Qool Therapeutics, Cagent, Applied Therapeutics, Biostar family of funds, SpectraWave, Orchestra Biomed, Aria, Cardiac Success, MedFocus family of funds, Valfix.
Dr. Parikh reports institutional grants/research support from Abbott Vascular, Shockwave Medical, TriReme Medical, Surmodics, and Silk Road Medical; consulting fees from Terumo and Abiomed; and Advisory Board participation for Abbott, Boston Scientific, CSI, Janssen, Medtronic and Philips.
Dr. Monreal reports that he served as an advisor or consultant for Sanofi, Leo Pharma and Daiichi Sankyo. Also, he received a nonrestricted educational grant by Sanofi and Bayer to sponsor the RIETE registry.
Dr. Krumholz works under contract with the Centers for Medicare & Medicaid Services to support quality measurement programs; was a recipient of a research grant, through Yale, from Medtronic and the U.S. Food and Drug Administration to develop methods for post-market surveillance of medical devices; was a recipient of a research grant from Johnson & Johnson, through Yale University, to support clinical trial data sharing; was a recipient of a research agreement, through Yale University, from the Shenzhen Center for Health Information for work to advance intelligent disease prevention and health promotion; collaborates with the National Center for Cardiovascular Diseases in Beijing; receives payment from the Arnold & Porter Law Firm for work related to the Sanofi clopidogrel litigation, from the Martin Baughman Law Firm for work related to the Cook Celect IVC filter litigation, and from the Siegfried and Jensen Law Firm for work related to Vioxx litigation; chairs a Cardiac Scientific Advisory Board for UnitedHealth; was a member of the IBM Watson Health Life Sciences Board; is a member of the Advisory Board for Element Science, the Advisory Board for Facebook, and the Physician Advisory Board for Aetna; and is the co-founder of HugoHealth, a personal health information platform, and co-founder of Refactor Health, an enterprise healthcare AI-augmented data management company.
Dr. Konstantinides reports research grants from Bayer AG, Boehringer Ingelheim, Actelion - Janssen; educational grants from Biocompatibles Group UK - Boston Scientific, Daiichi Sankyo; lecture fees from Bayer AG, Pfizer-Bristol-Myers Squibb, MSD, all outside the submitted work.
Dr. Weitz serves as a consultant and received honoraria from Bayer, Janssen, JnJ, BMS, Pfizer, Boehringer Ingelheim, Novartis, Daiichi-Sankyo, Merck, Servier, Anthos, Ionis, and PhaseBio.
Dr. Lip reports that he is a Consultant for Bayer/Janssen, BMS/Pfizer, Medtronic, Boehringer Ingelheim, Novartis, Verseon and Daiichi-Sankyo and a speaker for Bayer, BMS/Pfizer, Medtronic, Boehringer Ingelheim, and Daiichi-Sankyo. No fees are directly received personally.
- Received April 15, 2020.
- Accepted April 15, 2020.