Thromboembolic events as a complication of Covid-19
Abstract
Coronavirus-2 (SARS-CoV2/ Severe Acute Respiratory Syndrome Corona Virus 2) infection has emerged as a global health crisis. The incidence of thromboembolic disease is very high in SARS- CoV2 disease and involves multiple organ systems ranging from cutaneous thrombosis to pulmonary embolism, stroke or coronary thrombosis sometimes with catastrophic outcomes. Evidence points towards a key role of thromboembolism, hypercoagulability and overproductionn of proinflammatory cytokines mimicking a “cytokine storm” which leads to multiorgan failure
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References
• Medicine JHU. Corona Virus Resource Center. 04.28.2020 ed. Baltimore, USA 2020.
• Grasselli G, Pesenti A, Cecconi M. Critical Care Utilization for the COVID-19 Outbreak in Lombardy, Italy: Early Experience and Forecast During an Emergency Response. JAMA 2020.
• Meduri GU, Kohler G, Headley S, Tolley E, Stentz F, Postlethwaite A. Inflammatory cytokines in the BAL of patients with ARDS. Persistent elevation over time predicts poor outcome. Chest. 1995;108:1303–14.
• Tang N, Li D, Wang X, Sun Z. Abnormal coagulation parameters are associated with poor prognosis in patients with novel coronavirus 5.
• Helms J, Tacquard C, Severac F, et al. High risk of thrombosis in patients with severe SARS- CoV-2 infection: a multicenter prospective cohort study. Intensive Care Med 2020.
• Llitjos JF, Leclerc M, Chochois C, et al. High incidence of venous thromboembolic events in anticoagulated severe COVID-19 patients. J Thromb Haemost. 2020.
• Klok FA, Kruip M, van der Meer NJM, et al. Incidence of thrombotic complications in critically ill ICU patients with COVID-19. Thromb Res. 2020;191:145–7.
• Klok FA, Kruip M, van der Meer NJM, et al. Confirmation of the high cumulative incidence of thrombotic complications in critically ill ICU patients with COVID-19: An updated analysis. Thromb Res. 2020;191:148–50.
• Yang Y SC, Li J, Yuan J, Yang M et al. Exuberant elevation of IP-10, MCP-3 and IL-1ra during SARS-CoV-2 infection is associated with disease severity and fatal outcome. medRxiv 2020.
• Faix JD. Biomarkers of sepsis. Crit Rev Clin Lab Sci. 2013;50:23–36.
• Gao T HM, Zhang X, Li H, Zhu L et al. Highly pathogenic coronavirus N protein aggravates lung injury by MASP-2-mediated complement over-activation. medRxiv 2020.
• Chang JC. Hemostasis based on a novel 'two-path unifying theory' and classification of hemostatic disorders. Blood Coagul Fibrinolysis. 2018;29:573–84.
• Chang JC. Sepsis and septic shock: endothelial molecular pathogenesis associated with vascular microthrombotic disease. Thromb J. 2019;17:10.
• Gupta N, Zhao YY, Evans CE. The stimulation of thrombosis by hypoxia. Thromb Res. 2019;181:77–83.
• Kollias A, Kyriakoulis KG, Dimakakos E, Poulakou G, Stergiou GS, Syrigos K. Thromboembolic risk and anticoagulant therapy in COVID-19 patients: emerging evidence and call for action. Br J Haematol. 2020.
• Yao XH, Li TY, He ZC, et al. A pathological report of three COVID-19 cases by minimally invasive autopsies. Zhonghua Bing Li Xue Za Zhi. 2020;49:E009.
• Barton LM, Duval EJ, Stroberg E, Ghosh S, Mukhopadhyay S. COVID-19 Autopsies. USA. Am J Clin Pathol: Oklahoma; 2020.
• Magro C, Mulvey JJ, Berlin D, et al. Complement associated microvascular injury and thrombosis in the pathogenesis of severe COVID-19 infection: A report of five cases. Transl Res. 2020;220:1–13.
• Ciceri F, Beretta L, Scandroglio AM, et al. Microvascular COVID-19 lung vessels obstructive thromboinflammatory syndrome (MicroCLOTS): an atypical acute respiratory distress syndrome working hypothesis. Crit Care Resusc. 2020;22:95–7.
• Dolhnikoff M, Duarte-Neto AN, de Almeida Monteiro RA, et al. Pathological evidence of pulmonary thrombotic phenomena in severe COVID-19. J Thromb Haemost. 2020.
• Lodigiani C, Iapichino G, Carenzo L, et al. Venous and arterial thromboembolic complications in COVID-19 patients admitted to an academic hospital in Milan, Italy. Thromb Res. 2020;191:9–14.
• Middeldorp S, Coppens M, van Haaps TF, et al. Incidence of venous thromboembolism in hospitalized patients with COVID-19. J Thromb Haemost. 2020.
• Marone EM, Rinaldi LF. Upsurge of deep venous thrombosis in patients affected by COVID- 19: Preliminary data and possible explanations. J Vasc Surg Venous Lymphat Disord. 2020.
• Wichmann D, Sperhake JP, Lutgehetmann M, et al. Autopsy Findings and Venous Thromboembolism in Patients With COVID-19: A Prospective Cohort Study. Ann Intern Med. 2020.
• Cui S, Chen S, Li X, Liu S, Wang F. Prevalence of venous thromboembolism in patients with severe novel coronavirus pneumonia. J Thromb Haemost. 2020.
• Ackermann M, Verleden SE, Kuehnel M, et al. Pulmonary Vascular Endothelialitis, Thrombosis, and Angiogenesis in Covid-19. N Engl J Med. 2020.
• Demelo-Rodriguez P, Cervilla-Munoz E, Ordieres-Ortega L, et al. Incidence of asymptomatic deep vein thrombosis in patients with COVID-19 pneumonia and elevated D-dimer levels. Thromb Res. 2020;192:23–6.
• Zhang L, Feng X, Zhang D, et al. Deep Vein Thrombosis in Hospitalized Patients with Coronavirus Disease 2019 (COVID-19) in Wuhan, China: Prevalence, Risk Factors, and Outcome. Circulation 2020.
• Ren B, Yan F, Deng Z, et al. Extremely High Incidence of Lower Extremity Deep Venous Thrombosis in 48 Patients with Severe COVID-19 in Wuhan. Circulation. 2020.
• Stoneham SM, Milne KM, Nuttal E, et al. Thrombotic risk in COVID-19: a case series and case-control study. Clin Med (Lond). 2020.
• Voicu S, Bonnin P, Stepanian A, et al. High prevalence of deep vein thrombosis in mechanically ventilated COVID-19 patients. J Am Coll Cardiol. 2020.
• Desborough MJR, Doyle AJ, Griffiths A, Retter A, Breen KA, Hunt BJ. Image-proven thromboembolism in patients with severe COVID-19 in a tertiary critical care unit in the United Kingdom. Thromb Res. 2020;193:1–4.
• Al-Samkari H, Karp Leaf RS, Dzik WH, et al. COVID and Coagulation: Bleeding and Thrombotic Manifestations of SARS-CoV2 Infection. Blood. 2020.
• Fraisse M, Logre E, Pajot O, Mentec H, Plantefeve G, Contou D. Thrombotic and hemorrhagic events in critically ill COVID-19 patients: a French monocenter retrospective study. Crit Care. 2020;24:275.
• Le Berre A, Marteau V, Emmerich J, Zins M. Concomitant acute aortic thrombosis and pulmonary embolism complicating COVID-19 pneumonia. Diagn Interv Imaging. 2020;101:321–2.
• Baldacini M, Pop R, Sattler L, et al. Concomitant hemorrhagic syndrome and recurrent extensive arterial thrombosis in a patient with COVID-19 and acute promyelocytic leukemia. Br J Haematol. 2020.
• Giacomelli E, Dorigo W, Fargion A, Calugi G, Cianchi G, Pratesi C. Acute thrombosis of an aortic prosthetic graft in a patient with severe COVID-19 related pneumonia. Ann Vasc Surg. 2020.
• Lacour T, Semaan C, Genet T, Ivanes F. Insights for increased risk of failed fibrinolytic therapy and stent thrombosis associated with COVID-19 in ST-segment elevation myocardial infarction patients. Catheter Cardiovasc Interv. 2020.
• de Barry O, Mekki A, Diffre C, Seror M, Hajjam ME, Carlier RY. Arterial and venous abdominal thrombosis in a 79-year-old woman with COVID-19 pneumonia. Radiol Case Rep. 2020.
• Mulvey JJ, Magro CM, Ma LX, Nuovo GJ, Baergen RN. Analysis of complement deposition and viral RNA in placentas of COVID-19 patients. Ann Diagn Pathol. 2020;46:151530.
• Griffin DO, Jensen A, Khan M, et al. Pulmonary Embolism and Increased Levels of d-Dimer in Patients with Coronavirus Disease. Emerg Infect Dis. 2020;26.
• Zhou B, She J, Wang Y, Ma X. Venous thrombosis and arteriosclerosis obliterans of lower extremities in a very severe patient with 2019 novel coronavirus disease: a case report. J Thromb Thrombolysis. 2020.
• Zhou B, She J, Wang Y, Ma X. A Case of Coronavirus Disease 2019 With Concomitant Acute Cerebral Infarction and Deep Vein Thrombosis. Front Neurol. 2020;11:296.
• Dominguez-Erquicia P, Dobarro D, Raposeiras-Roubin S, Bastos-Fernandez G, Iniguez-Romo
• Multivessel coronary thrombosis in a patient with COVID-19 pneumonia. Eur Heart J. 2020.
• Martinelli I, Ferrazzi E, Ciavarella A, et al. Pulmonary embolism in a young pregnant woman with COVID-19. Thromb Res. 2020;191:36–7.
• Bozzani A, Arici V, Franciscone MM, et al. Severe Acute Respiratory Syndrome Coronavirus 2 Infection and the Upper Limb Deep Vein Thrombosis Risk. Ann Vasc Surg. 2020.
• Poggiali E, Bastoni D, Ioannilli E, Vercelli A, Magnacavallo A. Deep Vein Thrombosis and Pulmonary Embolism: Two Complications of COVID-19 Pneumonia? Eur J Case Rep Intern Med. 2020;7:001646.
• Hughes C, Nichols T, Pike M, Subbe C, Elghenzai S. Cerebral Venous Sinus Thrombosis as a Presentation of COVID-19. Eur J Case Rep Intern Med. 2020;7:001691.
• Kashi M, Jacquin A, Dakhil B, et al. Severe arterial thrombosis associated with Covid-19 infection. Thromb Res. 2020;192:75–7.
• Garaci F, Di Giuliano F, Picchi E, Da Ros V, Floris R. Venous cerebral thrombosis in COVID- 19 patient. J Neurol Sci. 2020;414:116871.
• Lax SF, Skok K, Zechner P, et al. Pulmonary Arterial Thrombosis in COVID-19 With Fatal Outcome: Results From a Prospective. Clinicopathologic Case Series. Ann Intern Med: Single- Center; 2020.
• Mestres G, Puigmacia R, Blanco C, Yugueros X, Esturrica M, Riambau V. Risk of peripheral arterial thrombosis in COVID-19. J Vasc Surg. 2020.
• Gomez-Arbelaez D, Ibarra-Sanchez G, Garcia-Gutierrez A, Comanges-Yeboles A, Ansuategui-Vicente M, Gonzalez-Fajardo JA. Covid-19-Related Aortic Thrombosis: A Report of Four Cases. Ann Vasc Surg. 2020.
• Davoodi L, Jafarpour H, Taghavi M, Razavi A. COVID-19 Presented With Deep Vein Thrombosis: An Unusual Presenting. J Investig Med High Impact Case Rep. 2020;8:2324709620931239.
• Viguier A, Delamarre L, Duplantier J, Olivot JM, Bonneville F. Acute ischemic stroke complicating common carotid artery thrombosis during a severe COVID-19 infection. J Neuroradiol. 2020.
• Rey JR, Valero SJ, Pinedo DP, Llorens JLM, Lopez-Sendon JL, Caro-Codon J. [COVID-19 and simultaneous thrombosis of two coronary arteries]. Rev Esp Cardiol 2020.
• Bhayana R, Som A, Li MD, et al. Abdominal Imaging Findings in COVID-19: Preliminary Observations. Radiology. 2020;201908.
• Hemasian H, Ansari B. First case of Covid-19 presented with cerebral venous thrombosis: A rare and dreaded case. Rev Neurol (Paris). 2020;176:521–3.
• Fara MG, Stein LK, Skliut M, Morgello S, Fifi JT, Dhamoon MS. Macrothrombosis and stroke in patients with mild Covid-19 infection. J Thromb Haemost. 2020.
• Azouz E, Yang S, Monnier-Cholley L, Arrive L. Systemic arterial thrombosis and acute mesenteric ischemia in a patient with COVID-19. Intensive Care Med. 2020.
• Nauka PC, Oran E, Chekuri S. Deep venous thrombosis in a non-critically ill patient with novel COVID-19 infection. Thromb Res. 2020;192:27–8.
• Seif S, Ayuna A, Kumar A, Macdonald J. Massive coronary thrombosis caused primary percutaneous coronary intervention to fail in a COVID-19 patient with ST-elevation myocardial infarction. Catheter Cardiovasc Interv. 2020.
• Morales MH, Leigh CL, Simon EL. COVID-19 infection with extensive thrombosis: A case of phlegmasia cerulea dolens. Am J Emerg Med. 2020.
• Kaur P, Qaqa F, Ramahi A, et al. Acute upper limb ischemia in a patient with COVID-19. Hematol Oncol Stem Cell Ther. 2020.
• Fox SE, Akmatbekov A, Harbert JL, Li G, Quincy Brown J, Vander Heide RS. Pulmonary and cardiac pathology in African American patients with COVID-19: an autopsy series from New Orleans. Lancet Respir Med. 2020.
• Hinterseer M, Zens M, Wimmer RJ, et al. Acute myocardial infarction due to coronary stent thrombosis in a symptomatic COVID-19 patient. Clin Res Cardiol. 2020.
• Vulliamy P, Jacob S, Davenport RA. Acute aorto-iliac and mesenteric arterial thromboses as presenting features of COVID-19. Br J Haematol. 2020.
• L AB, Pacioni C, Ponton S, Francavilla S, Cuzzoli A. Arterial Mesenteric Thrombosis as a Complication of SARS-CoV-2 Infection. Eur J Case Rep Intern Med. 2020;7:001690.
• Faggiano P, Bonelli A, Paris S, et al. Acute pulmonary embolism in COVID-19 disease: Preliminary report on seven patients. Int J Cardiol. 2020.
• Szekely Y, Lichter Y, Taieb P, et al. The Spectrum of Cardiac Manifestations in Coronavirus Disease 2019 (COVID-19) - a Systematic Echocardiographic Study. Circulation. 2020.
• Harari R, Bangalore S, Chang E, Shah B. COVID-19 complicated by acute myocardial infarction with extensive thrombus burden and cardiogenic shock. Catheter Cardiovasc Interv. 2020.
• Andrea V, Gianluca F, Rodolfo P, Paolo T, Alessandro P, Mauro G. Unheralded Lower Limb Threatening Ischemia in a COVID-19 Patient. Int J Infect Dis. 2020.
• La Mura V, Artoni A, Martinelli I, et al. Acute Portal Vein Thrombosis in SARS-CoV-2 Infection: A Case Report. Am J Gastroenterol. 2020.
• Horowitz JM, Yuriditsky E, Henderson IJ, Stachel MW, Kwok B, Saric M. Clot in Transit on Transesophageal Echocardiography in a Prone Patient with COVID-19 Acute Respiratory Distress Syndrome. CASE (Phila). 2020.
• Buja LM, Wolf DA, Zhao B, et al. The emerging spectrum of cardiopulmonary pathology of the coronavirus disease 2019 (COVID-19): Report of 3 autopsies from Houston, Texas, and review of autopsy findings from other United States cities. Cardiovasc Pathol. 2020;48:107233.
• Qanadli SD, Gudmundsson L, Rotzinger DC. Catheter-directed thrombolysis in COVID-19 pneumonia with acute PE: Thinking beyond the guidelines. Thromb Res. 2020;192:9–11.
• Vitali C, Minniti A, Caporali R, Del Papa N. Occurrence of pulmonary embolism in a patient with mild clinical expression of COVID-19. Thromb Res. 2020;192:21–2.
• Zayet S, Klopfenstein T, Kovacs R, Stancescu S, Hagenkotter B. Acute Cerebral Stroke with Multiple Infarctions and COVID-19, France, 2020. Emerg Infect Dis. 2020;26.
• Baergen RN, Heller DS. Placental Pathology in Covid-19 Positive Mothers: Preliminary Findings. Pediatr Dev Pathol. 2020;23:177–80.
• Malentacchi M, Gned D, Angelino V, et al. Concomitant brain arterial and venous thrombosis in a COVID-19 patient. Eur J Neurol. 2020.
• Ding S, Lin Q, Zhu T, et al. Is there a correlation between inflammatory markers and coagulation parameters in women with advanced ovarian endometriosis? BMC Womens Health. 2019;19:169.
• Zhang L, Yan X, Fan Q, et al. D-dimer levels on admission to predict in-hospital mortality in patients with Covid-19. J Thromb Haemost. 2020;18:1324–9.
• Connors JM, Levy JH. COVID-19 and its implications for thrombosis and anticoagulation. Blood. 2020;135:2033–40.
• Seirafianpour F, Sodagar S, Mohammad AP, et al. Cutaneous manifestations and considerations in COVID-19 pandemic: A systematic review. Dermatol Ther. 2020.
• Spiezia L, Boscolo A, Poletto F, et al. COVID-19-Related Severe Hypercoagulability in Patients Admitted to Intensive Care Unit for Acute Respiratory Failure. Thromb Haemost. 2020;120:998–1000.
• Panigada M, Bottino N, Tagliabue P, et al. Hypercoagulability of COVID-19 patients in Intensive Care Unit. A Report of Thromboelastography Findings and other Parameters of Hemostasis. J Thromb Haemost 2020.
• Dugar S, Duggal A, Bassel A, Soliman M, Moghekar A. Spontaneous echo contrast in venous ultrasound of severe COVID-19 patients. Intensive Care Med. 2020.
• Bikdeli B, Madhavan MV, Jimenez D, et al. COVID-19 and Thrombotic or Thromboembolic Disease: Implications for Prevention, Antithrombotic Therapy, and Follow-up. J Am Coll Cardiol. 2020.
• Thachil J, Tang N, Gando S, et al. Type and dose of heparin in COVID-19. J Thromb Haemost. 2020.
• Belen-Apak FB, Sarialioglu F. The old but new: Can unfractioned heparin and low molecular weight heparins inhibit proteolytic activation and cellular internalization of SARS-CoV2 by inhibition of host cell proteases? Med Hypotheses. 2020;142:109743.
• Paranjpe I, Fuster V, Lala A, et al. Association of Treatment Dose Anticoagulation with In- Hospital Survival Among Hospitalized Patients with COVID-19. J Am Coll Cardiol. 2020.
• Streiff MB, Agnelli G, Connors JM, et al. Guidance for the treatment of deep vein thrombosis and pulmonary embolism. J Thromb Thrombolysis. 2016;41:32–67.
• Kumar P, Mediwake R, Rhead C. A matter of time: duration and choice of venous thromboprophylaxis in patients diagnosed with COVID-19. Br J Hosp Med (Lond). 2020;81:1–2.
• Testa S, Prandoni P, Paoletti O, et al. Direct oral anticoagulant plasma levels striking increase in severe COVID-19 respiratory syndrome patients treated with antiviral agents. The Cremona experience J Thromb Haemost. 2020.
• Marullo AG, Cavarretta E, Biondi-Zoccai G, et al. Extracorporeal membrane oxygenation for critically ill patients with coronavirus-associated disease 2019: an updated perspective of the European experience. Minerva Cardioangiol. 2020.
• Zochios V, Brodie D, Charlesworth M, Parhar KK. Delivering extracorporeal membrane oxygenation for patients with COVID-19: what, who, when and how? Anaesthesia; 2020.
• Koeckerling D, Pan D, Mudalige NL, Oyefeso O, Barker J. Blood transfusion strategies and ECMO during the COVID-19 pandemic. Lancet Respir Med. 2020.
• Lukito P, Wong A, Jing J, et al. Mechanical circulatory support is associated with loss of platelet receptors glycoprotein Ibalpha and glycoprotein VI. J Thromb Haemost. 2016;14:2253–60.
• Horiuchi H, Doman T, Kokame K, Saiki Y, Matsumoto M. Acquired von Willebrand Syndrome Associated with Cardiovascular Diseases. J Atheroscler Thromb. 2019;26:303–14.
• Hashmi NK, Ghadimi K, Srinivasan AJ, et al. Three-factor prothrombin complex concentrates for refractory bleeding after cardiovascular surgery within an algorithmic approach to haemostasis. Vox Sang. 2019;114:374–85.
• Piacente C, Martucci G, Miceli V, et al. A narrative review of antithrombin use during veno- venous extracorporeal membrane oxygenation in adults: rationale, current use, effects on anticoagulation, and outcomes. Perfusion. 2020;267659120913803.
• Kurihara C, Walter JM, Karim A, et al. Feasibility of veno-venous extracorporeal membrane oxygenation without systemic anticoagulation. Ann Thorac Surg 2020.
• Chen L, Li Q, Zheng D, et al. Clinical Characteristics of Pregnant Women with Covid-19 in Wuhan. China N Engl J Med. 2020.
• Dashraath P, Wong JLJ, Lim MXK, et al. Coronavirus disease 2019 (COVID-19) pandemic and pregnancy. Am J Obstet Gynecol. 2020;222:521–31.
• Simcox LE, Ormesher L, Tower C, Greer IA. Thrombophilia and Pregnancy Complications. Int J Mol Sci. 2015;16:28418–28.
