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Thromb Haemost 2020; 120(12): 1654-1667
DOI: 10.1055/s-0040-1721487
Theme Issue Article

Hypercoagulopathy in Severe COVID-19: Implications for Acute Care

Alicia A. C. Waite
1   Institute for Life Course and Medical Sciences, University of Liverpool, Liverpool, United Kingdom
2   Department of Intensive Care Medicine, Royal Liverpool University Hospital, Liverpool University Hospitals NHS Foundation Trust, Liverpool, United Kingdom
,
David O. Hamilton
2   Department of Intensive Care Medicine, Royal Liverpool University Hospital, Liverpool University Hospitals NHS Foundation Trust, Liverpool, United Kingdom
,
Roberto Pizzi
3   Department of Medicine and Surgery, University of Insubria, Varese, Italy
,
Walter Ageno
3   Department of Medicine and Surgery, University of Insubria, Varese, Italy
,
Ingeborg D. Welters
1   Institute for Life Course and Medical Sciences, University of Liverpool, Liverpool, United Kingdom
2   Department of Intensive Care Medicine, Royal Liverpool University Hospital, Liverpool University Hospitals NHS Foundation Trust, Liverpool, United Kingdom
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Abstract

COVID-19 was first described in late 2019 and has since developed into a pandemic affecting more than 21 million people worldwide. Of particular relevance for acute care is the occurrence of COVID-19-associated coagulopathy (CAC), which is characterised by hypercoagulability, immunothrombosis and venous thromboembolism, and contributes to hypoxia in a significant proportion of patients. This review describes diagnosis and treatment of CAC in the emergency department and in intensive care. We summarise the pathological mechanisms and common complications of CAC such as pulmonary thrombosis and venous thromboembolic events and discuss current strategies for thromboprophylaxis and therapeutic anti-coagulation in the acute care setting.

Keywords

anti-coagulation - coagulopathy - immunothrombosis - severe acute respiratory syndrome - venous thrombosis


Publikationsverlauf

Eingereicht: 16. August 2020

Angenommen: 09. November 2020

Artikel online veröffentlicht:
23. Dezember 2020

© 2020. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 

  • References

  • 1 Zhou F, Yu T, Du R. et al. Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study. Lancet 2020; 395 (10229): 1054-1062
    Google Scholar
  • 2 Zou Y, Guo H, Zhang Y. et al. Analysis of coagulation parameters in patients with COVID-19 in Shanghai, China. Biosci Trends 2020; 14 (04) 285-289
    CrossrefPubMedGoogle Scholar
  • 3 Helms J, Tacquard C, Severac F. et al; CRICS TRIGGERSEP Group (Clinical Research in Intensive Care and Sepsis Trial Group for Global Evaluation and Research in Sepsis). High risk of thrombosis in patients with severe SARS-CoV-2 infection: a multicenter prospective cohort study. Intensive Care Med 2020; 46 (06) 1089-1098
    CrossrefPubMedGoogle Scholar
  • 4 Klok FA, Kruip MJHA, van der Meer NJM. et al. Incidence of thrombotic complications in critically ill ICU patients with COVID-19. Thromb Res 2020; 191: 145-147
    CrossrefPubMedGoogle Scholar
  • 5 Middeldorp S, Coppens M, van Haaps TF. et al. Incidence of venous thromboembolism in hospitalized patients with COVID-19. J Thromb Haemost 2020; 18 (08) 1995-2002
    CrossrefPubMedGoogle Scholar
  • 6 Llitjos JF, Leclerc M, Chochois C. et al. High incidence of venous thromboembolic events in anticoagulated severe COVID-19 patients. J Thromb Haemost 2020; 18 (07) 1743-1746
    CrossrefPubMedGoogle Scholar
  • 7 Zhang L, Feng X, Zhang D. et al. Deep vein thrombosis in hospitalized patients with COVID-19 in Wuhan, China: prevalence, risk factors, and outcome. Circulation 2020; 142 (02) 114-128
    CrossrefPubMedGoogle Scholar
  • 8 Tang N, Li D, Wang X, Sun Z. Abnormal coagulation parameters are associated with poor prognosis in patients with novel coronavirus pneumonia. J Thromb Haemost 2020; 18 (04) 844-847
    CrossrefPubMedGoogle Scholar
  • 9 Fogarty H, Townsend L, Ni Cheallaigh C. et al. COVID19 coagulopathy in Caucasian patients. Br J Haematol 2020; 189 (06) 1044-1049
    CrossrefPubMedGoogle Scholar
  • 10 Han H, Yang L, Liu R. et al. Prominent changes in blood coagulation of patients with SARS-CoV-2 infection. Clin Chem Lab Med 2020; 58 (07) 1116-1120
    CrossrefPubMedGoogle Scholar
  • 11 Iba T, Levy JH, Connors JM, Warkentin TE, Thachil J, Levi M. The unique characteristics of COVID-19 coagulopathy. Crit Care 2020; 24 (01) 360
    CrossrefPubMedGoogle Scholar
  • 12 Li T, Lu H, Zhang W. Clinical observation and management of COVID-19 patients. Emerg Microbes Infect 2020; 9 (01) 687-690
    CrossrefPubMedGoogle Scholar
  • 13 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; 8 (07) 681-686
    CrossrefPubMedGoogle Scholar
  • 14 Barnes BJ, Adrover JM, Baxter-Stoltzfus A. et al. Targeting potential drivers of COVID-19: Neutrophil extracellular traps. J Exp Med 2020; 217 (06) e20200652
    CrossrefPubMedGoogle Scholar
  • 15 Wichmann D, Sperhake JP, Lütgehetmann M. et al. Autopsy findings and venous thromboembolism in patients with COVID-19: a prospective cohort study. Ann Intern Med 2020; 173 (04) 268-277
    CrossrefPubMedGoogle Scholar
  • 16 Lax SF, Skok K, Zechner P. et al. Pulmonary arterial thrombosis in COVID-19 with fatal outcome : results from a prospective, single-center, clinicopathologic case series. Ann Intern Med 2020; 173 (05) 350-361
    CrossrefPubMedGoogle Scholar
  • 17 Tang N, Bai H, Chen X, Gong J, Li D, Sun Z. Anticoagulant treatment is associated with decreased mortality in severe coronavirus disease 2019 patients with coagulopathy. J Thromb Haemost 2020; 18 (05) 1094-1099
    CrossrefPubMedGoogle Scholar
  • 18 Levi M, Schultz M, van der Poll T. Sepsis and thrombosis. Semin Thromb Hemost 2013; 39 (05) 559-566
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 19 Cook D, Crowther M, Meade M. et al. Deep venous thrombosis in medical-surgical critically ill patients: prevalence, incidence, and risk factors. Crit Care Med 2005; 33 (07) 1565-1571
    CrossrefPubMedGoogle Scholar
  • 20 Beitland S, Wimmer H, Lorentsen T. et al. Venous thromboembolism in the critically ill: a prospective observational study of occurrence, risk factors and outcome. Acta Anaesthesiol Scand 2019; 63 (05) 630-638
    CrossrefPubMedGoogle Scholar
  • 21 Hirsch DR, Ingenito EP, Goldhaber SZ. Prevalence of deep venous thrombosis among patients in medical intensive care. JAMA 1995; 274 (04) 335-337
    CrossrefPubMedGoogle Scholar
  • 22 Harris LM, Curl GR, Booth FV, Hassett Jr JM, Leney G, Ricotta JJ. Screening for asymptomatic deep vein thrombosis in surgical intensive care patients. J Vasc Surg 1997; 26 (05) 764-769
    CrossrefPubMedGoogle Scholar
  • 23 Ibrahim EH, Iregui M, Prentice D, Sherman G, Kollef MH, Shannon W. Deep vein thrombosis during prolonged mechanical ventilation despite prophylaxis. Crit Care Med 2002; 30 (04) 771-774
    CrossrefPubMedGoogle Scholar
  • 24 Minet C, Potton L, Bonadona A. et al. Venous thromboembolism in the ICU: main characteristics, diagnosis and thromboprophylaxis. Crit Care 2015; 19 (01) 287
    CrossrefPubMedGoogle Scholar
  • 25 Zhang C, Zhang Z, Mi J. et al. The cumulative venous thromboembolism incidence and risk factors in intensive care patients receiving the guideline-recommended thromboprophylaxis. Medicine (Baltimore) 2019; 98 (23) e15833
    CrossrefPubMedGoogle Scholar
  • 26 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; 18 (06) 1421-1424
    CrossrefPubMedGoogle Scholar
  • 27 Poissy J, Goutay J, Caplan M. et al; Lille ICU Haemostasis COVID-19 Group. Pulmonary embolism in patients with COVID-19: awareness of an increased prevalence. Circulation 2020; 142 (02) 184-186
    CrossrefPubMedGoogle Scholar
  • 28 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
    CrossrefPubMedGoogle Scholar
  • 29 van Dam LF, Kroft LJM, van der Wal LI. et al. Clinical and computed tomography characteristics of COVID-19 associated acute pulmonary embolism: a different phenotype of thrombotic disease?. Thromb Res 2020; 193: 86-89
    CrossrefPubMedGoogle Scholar
  • 30 Kwenandar F, Japar KV, Damay V. et al. Coronavirus disease 2019 and cardiovascular system: a narrative review. Int J Cardiol Heart Vasc 2020; 29: 100557
    CrossrefPubMedGoogle Scholar
  • 31 Yuan X, Huang W, Ye B. et al. Changes of hematological and immunological parameters in COVID-19 patients. Int J Hematol 2020; 112 (04) 553-559
    CrossrefPubMedGoogle Scholar
  • 32 Huang C, Wang Y, Li X. et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet 2020; 395 (10223): 497-506
    CrossrefPubMedGoogle Scholar
  • 33 Guan WJ, Ni ZY, Hu Y. et al; China Medical Treatment Expert Group for Covid-19. Clinical characteristics of coronavirus disease 2019 in China. N Engl J Med 2020; 382 (18) 1708-1720
    CrossrefPubMedGoogle Scholar
  • 34 Li Y, Zhao K, Wei H. et al. Dynamic relationship between D-dimer and COVID-19 severity. Br J Haematol 2020; 190 (01) e24-e27
    CrossrefPubMedGoogle Scholar
  • 35 Long H, Nie L, Xiang X. et al. D-dimer and prothrombin time are the significant indicators of severe COVID-19 and poor prognosis. BioMed Res Int 2020; 2020: 6159720
    CrossrefPubMedGoogle Scholar
  • 36 Moreno G, Carbonell R, Bodí M, Rodríguez A. Systematic review of the prognostic utility of D-dimer, disseminated intravascular coagulation, and anticoagulant therapy in COVID-19 critically ill patients [in Spanish]. Med Intensiva 2020; DOI: 10.1016/j.medin.2020.06.006.
    CrossrefPubMedGoogle Scholar
  • 37 Shah S, Shah K, Patel SB. et al. Elevated D-dimer levels are associated with increased risk of mortality in COVID-19: a systematic review and meta-analysis. Cardiol Rev 2020; DOI: 10.1097/CRD.0000000000000330.
    CrossrefPubMedGoogle Scholar
  • 38 Yao Y, Cao J, Wang Q. et al. D-dimer as a biomarker for disease severity and mortality in COVID-19 patients: a case control study. J Intensive Care 2020; 8: 49
    CrossrefPubMedGoogle Scholar
  • 39 Ye W, Chen G, Li X. et al. Dynamic changes of D-dimer and neutrophil-lymphocyte count ratio as prognostic biomarkers in COVID-19. Respir Res 2020; 21 (01) 169
    CrossrefPubMedGoogle Scholar
  • 40 Lippi G, Plebani M, Henry BM. Thrombocytopenia is associated with severe coronavirus disease 2019 (COVID-19) infections: a meta-analysis. Clin Chim Acta 2020; 506: 145-148
    CrossrefPubMedGoogle Scholar
  • 41 Maier CL, Truong AD, Auld SC, Polly DM, Tanksley CL, Duncan A. COVID-19-associated hyperviscosity: a link between inflammation and thrombophilia?. Lancet 2020; 395 (10239): 1758-1759
    CrossrefPubMedGoogle Scholar
  • 42 Stanworth SJ, Walsh TS, Prescott RJ, Lee RJ, Watson DM, Wyncoll DL. Intensive Care Study of Coagulopathy Investigators. Thrombocytopenia and platelet transfusion in UK critical care: a multicenter observational study. Transfusion 2013; 53 (05) 1050-1058
    CrossrefPubMedGoogle Scholar
  • 43 Baughman RP, Lower EE, Flessa HC, Tollerud DJ. Thrombocytopenia in the intensive care unit. Chest 1993; 104 (04) 1243-1247
    CrossrefPubMedGoogle Scholar
  • 44 Chakraverty R, Davidson S, Peggs K, Stross P, Garrard C, Littlewood TJ. The incidence and cause of coagulopathies in an intensive care population. Br J Haematol 1996; 93 (02) 460-463
    CrossrefPubMedGoogle Scholar
  • 45 Besser MW, MacDonald SG. Acquired hypofibrinogenemia: current perspectives. J Blood Med 2016; 7: 217-225
    CrossrefPubMedGoogle Scholar
  • 46 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 (06) 998-1000
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 47 Ranucci M, Sitzia C, Baryshnikova E. et al. Covid-19-associated coagulopathy: biomarkers of thrombin generation and fibrinolysis leading the outcome. J Clin Med 2020; 9 (11) E3487
    CrossrefPubMedGoogle Scholar
  • 48 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; 18 (07) 1738-1742
    CrossrefPubMedGoogle Scholar
  • 49 Iba T, Levy JH, Raj A, Warkentin TE. Advance in the management of sepsis-induced coagulopathy and disseminated intravascular coagulation. J Clin Med 2019; 8 (05) E728
    CrossrefPubMedGoogle Scholar
  • 50 Umemura Y, Yamakawa K, Kiguchi T, Nishida T, Kawada M, Fujimi S. Hematological phenotype of COVID-19-induced coagulopathy: far from typical sepsis-induced coagulopathy. J Clin Med 2020; 9 (09) E2875
    CrossrefPubMedGoogle Scholar
  • 51 Hoechter DJ, Becker-Pennrich A, Langrehr J. et al. Higher procoagulatory potential but lower DIC score in COVID-19 ARDS patients compared to non-COVID-19 ARDS patients. Thromb Res 2020; 196: 186-192
    CrossrefPubMedGoogle Scholar
  • 52 Abbasi-Oshaghi E, Mirzaei F, Farahani F, Khodadadi I, Tayebinia H. Diagnosis and treatment of coronavirus disease 2019 (COVID-19): laboratory, PCR, and chest CT imaging findings. Int J Surg 2020; 79: 143-153
    CrossrefPubMedGoogle Scholar
  • 53 Convissar DL, Gibson LE, Berra L, Bittner EA, Chang MG. Application of lung ultrasound during the COVID-19 pandemic: a narrative review. Anesth Analg 2020; 131 (02) 345-350
    CrossrefPubMedGoogle Scholar
  • 54 Smith MJ, Hayward SA, Innes SM, Miller ASC. Point-of-care lung ultrasound in patients with COVID-19 - a narrative review. Anaesthesia 2020; 75 (08) 1096-1104
    CrossrefPubMedGoogle Scholar
  • 55 Szekely Y, Lichter Y, Taieb P. et al. Spectrum of cardiac manifestations in COVID-19: a systematic echocardiographic study. Circulation 2020; 142 (04) 342-353
    CrossrefPubMedGoogle Scholar
  • 56 Pizzi R, Gini G, Caiano L. et al. Coagulation parameters and venous thromboembolism in patients with and without COVID-19 admitted to the emergency department for acute respiratory insufficiency. Thromb Res 2020; 196: 209-212
    CrossrefPubMedGoogle Scholar
  • 57 Sun P, Qie S, Liu Z, Ren J, Li K, Xi J. Clinical characteristics of hospitalized patients with SARS-CoV-2 infection: a single arm meta-analysis. J Med Virol 2020; 92 (06) 612-617
    CrossrefPubMedGoogle Scholar
  • 58 Xu Z, Shi L, Wang Y. et al. Pathological findings of COVID-19 associated with acute respiratory distress syndrome. Lancet Respir Med 2020; 8 (04) 420-422
    CrossrefPubMedGoogle Scholar
  • 59 Clausen TM, Sandoval DR, Spliid CB. et al. SARS-CoV-2 infection depends on cellular heparan sulfate and ACE2. Cell 2020; DOI: 10.1016/j.cell.2020.09.033.
    CrossrefPubMedGoogle Scholar
  • 60 Goshua G, Pine AB, Meizlish ML. et al. Endotheliopathy in COVID-19-associated coagulopathy: evidence from a single-centre, cross-sectional study. Lancet Haematol 2020; S2352–3026(20)30216–7
    PubMedGoogle Scholar
  • 61 O'Sullivan JM, Gonagle DM, Ward SE, Preston RJS, O'Donnell JS. Endothelial cells orchestrate COVID-19 coagulopathy. Lancet Haematol 2020; 7 (08) e553-e555
    CrossrefPubMedGoogle Scholar
  • 62 Antoniak S. The coagulation system in host defense. Res Pract Thromb Haemost 2018; 2 (03) 549-557
    CrossrefPubMedGoogle Scholar
  • 63 Engelmann B, Massberg S. Thrombosis as an intravascular effector of innate immunity. Nat Rev Immunol 2013; 13 (01) 34-45
    CrossrefPubMedGoogle Scholar
  • 64 Frantzeskaki F, Armaganidis A, Orfanos SE. Immunothrombosis in acute respiratory distress syndrome: cross talks between inflammation and coagulation. Respiration 2017; 93 (03) 212-225
    CrossrefPubMedGoogle Scholar
  • 65 Hunt B, Retter A, McClintock C. Practical guidance for the prevention of thrombosis and management of coagulopathy and disseminated intravascular coagulation of patients infected with COVID-19. Accessed May 8, 2020 at: https://thrombosisuk.org/downloads/T&H%20and%20COVID.pdf
    PubMedGoogle Scholar
  • 66 McGonagle D, O'Donnell JS, Sharif K, Emery P, Bridgewood C. Immune mechanisms of pulmonary intravascular coagulopathy in COVID-19 pneumonia. Lancet Rheumatol 2020; 2 (07) e437-e445
    CrossrefPubMedGoogle Scholar
  • 67 Price LC, McCabe C, Garfield B, Wort SJ. Thrombosis and COVID-19 pneumonia: the clot thickens!. Eur Respir J 2020; 56 (01) 2001608
    CrossrefPubMedGoogle Scholar
  • 68 Pons S, Fodil S, Azoulay E, Zafrani L. The vascular endothelium: the cornerstone of organ dysfunction in severe SARS-CoV-2 infection. Crit Care 2020; 24 (01) 353
    CrossrefPubMedGoogle Scholar
  • 69 Varga Z, Flammer AJ, Steiger P. et al. Endothelial cell infection and endotheliitis in COVID-19. Lancet 2020; 395 (10234): 1417-1418
    CrossrefPubMedGoogle Scholar
  • 70 Tay MZ, Poh CM, Rénia L, MacAry PA, Ng LFP. The trinity of COVID-19: immunity, inflammation and intervention. Nat Rev Immunol 2020; 20 (06) 363-374
    CrossrefPubMedGoogle Scholar
  • 71 Silk E, Zhao H, Weng H, Ma D. The role of extracellular histone in organ injury. Cell Death Dis 2017; 8 (05) e2812
    CrossrefPubMedGoogle Scholar
  • 72 Abrams ST, Zhang N, Manson J. et al. Circulating histones are mediators of trauma-associated lung injury. Am J Respir Crit Care Med 2013; 187 (02) 160-169
    CrossrefPubMedGoogle Scholar
  • 73 Qaddoori Y, Abrams ST, Mould P. et al. Extracellular histones inhibit complement activation through interacting with complement component 4. J Immunol 2018; 200 (12) 4125-4133
    CrossrefPubMedGoogle Scholar
  • 74 Zuo Y, Yalavarthi S, Shi H. et al. Neutrophil extracellular traps in COVID-19. JCI Insight 2020; 5 (11) 138999
    PubMedGoogle Scholar
  • 75 Middleton EA, He XY, Denorme F. et al. Neutrophil extracellular traps contribute to immunothrombosis in COVID-19 acute respiratory distress syndrome. Blood 2020; 136 (10) 1169-1179
    CrossrefPubMedGoogle Scholar
  • 76 Abrams ST, Morton B, Alhamdi Y. et al. A novel assay for neutrophil extracellular trap formation independently predicts disseminated intravascular coagulation and mortality in critically ill patients. Am J Respir Crit Care Med 2019; 200 (07) 869-880
    CrossrefPubMedGoogle Scholar
  • 77 Alhamdi Y, Toh CH. Recent advances in pathophysiology of disseminated intravascular coagulation: the role of circulating histones and neutrophil extracellular traps. F1000 Res 2017; 6: 2143
    CrossrefPubMedGoogle Scholar
  • 78 Porto BN, Stein RT. Neutrophil extracellular traps in pulmonary diseases: too much of a good thing?. Front Immunol 2016; 7: 311
    CrossrefPubMedGoogle Scholar
  • 79 Ammollo CT, Semeraro F, Xu J, Esmon NL, Esmon CT. Extracellular histones increase plasma thrombin generation by impairing thrombomodulin-dependent protein C activation. J Thromb Haemost 2011; 9 (09) 1795-1803
    CrossrefPubMedGoogle Scholar
  • 80 Cheng Z, Abrams ST, Alhamdi Y. et al. Circulating histones are major mediators of multiple organ dysfunction syndrome in acute critical illnesses. Crit Care Med 2019; 47 (08) e677-e684
    CrossrefPubMedGoogle Scholar
  • 81 Ackermann M, Verleden SE, Kuehnel M. et al. Pulmonary vascular endothelialitis, thrombosis, and angiogenesis in Covid-19. N Engl J Med 2020; 383 (02) 120-128
    CrossrefPubMedGoogle Scholar
  • 82 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
    CrossrefPubMedGoogle Scholar
  • 83 Yao XH, Li TY, He ZC. et al. A pathological report of three COVID-19 cases by minimal invasive autopsies [in Chinese]. Zhonghua Bing Li Xue Za Zhi 2020; 49 (05) 411-417
    CrossrefPubMedGoogle Scholar
  • 84 Carsana L, Sonzogni A, Nasr A. et al. Pulmonary post-mortem findings in a series of COVID-19 cases from northern Italy: a two-centre descriptive study. Lancet Infect Dis 2020; 20 (10) 1135-1140
    CrossrefPubMedGoogle Scholar
  • 85 Schaller T, Hirschbühl K, Burkhardt K. et al. Postmortem examination of patients with COVID-19. JAMA 2020; 323 (24) 2518-2520
    CrossrefPubMedGoogle Scholar
  • 86 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
    CrossrefPubMedGoogle Scholar
  • 87 Musoke N, Lo KB, Albano J. et al. Anticoagulation and bleeding risk in patients with COVID-19. Thromb Res 2020; 196: 227-230
    CrossrefPubMedGoogle Scholar
  • 88 Patell R, Bogue T, Koshy A. et al. Postdischarge thrombosis and hemorrhage in patients with COVID-19. Blood 2020; 136 (11) 1342-1346
    CrossrefPubMedGoogle Scholar
  • 89 National Institute for Health and Care Excellence. Venous thromboembolism in over 16s: reducing the risk of hospital-acquired deep vein thrombosis or pulmonary embolism. (NICE Guideline 89). Accessed May 8, 2020 at: https://www.nice.org.uk/guidance/ng89
    PubMedGoogle Scholar
  • 90 Najem MY, Couturaud F, Lemarié CA. Cytokine and chemokine regulation of venous thromboembolism. J Thromb Haemost 2020; 18 (05) 1009-1019
    CrossrefPubMedGoogle Scholar
  • 91 Flaczyk A, Rosovsky RP, Reed CT, Bankhead-Kendall BK, Bittner EA, Chang MG. Comparison of published guidelines for management of coagulopathy and thrombosis in critically ill patients with COVID 19: implications for clinical practice and future investigations. Crit Care 2020; 24 (01) 559
    CrossrefPubMedGoogle Scholar
  • 92 Kreuziger LB, Lee AI, Garcia D. et al. COVID-19 and VTE/Anticoagulation: Frequently Asked Questions, Version 4.0. Accessed August 1, 2020 at: https://www.hematology.org/covid-19/covid-19-and-vte-anticoagulation
    PubMedGoogle Scholar
  • 93 Intensive Care Society, Faculty of Intensive Care Medicine, Royal College of Anaesthetists, Royal College of Physicians. Clinical guide for the prevention, detection and management of thromboembolic disease in patients with COVID-19. Accessed June 30, 2020 at: https://icmanaesthesiacovid-19.org/clinical-guide-prevention-detection-and-management-of-vte-in-patients-with-covid-19
    PubMedGoogle Scholar
  • 94 Cattaneo M, Bertinato EM, Birocchi S. et al. Pulmonary embolism or pulmonary thrombosis in COVID-19? Is the recommendation to use high-dose heparin for thromboprophylaxis justified?. Thromb Haemost 2020; 120 (08) 1230-1232
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 95 Fraissé M, Logre E, Pajot O, Mentec H, Plantefève G, Contou D. Thrombotic and hemorrhagic events in critically ill COVID-19 patients: a French monocenter retrospective study. Crit Care 2020; 24 (01) 275
    CrossrefPubMedGoogle Scholar
  • 96 Al-Samkari H, Gupta S, Karp RLeaf, Wang W, Rosovsky R, Bauer K, Leaf D. STOP-COVID Investigators. Thrombosis, bleeding, and the effect of anticoagulation on survival in critically ill patients with COVID-19 in the United States [abstract]. Res Pract Thromb Haemost 2020;(04, Suppl 1). Accessed November 27, 2020 at: https://abstracts.isth.org/abstract/thrombosis-bleeding-and-the-effect-of-anticoagulation-on-survival-in-critically-ill-patients-with-covid-19-in-the-united-states/
    PubMedGoogle Scholar
  • 97 Susen S, Tacquard CA, Godon A. et al; GIHP and GFHT. Prevention of thrombotic risk in hospitalized patients with COVID-19 and hemostasis monitoring. Crit Care 2020; 24 (01) 364
    CrossrefPubMedGoogle Scholar
  • 98 Atallah B, Mallah SI, AlMahmeed W. Anticoagulation in COVID-19. Eur Heart J Cardiovasc Pharmacother 2020; 6 (04) 260-261
    CrossrefPubMedGoogle Scholar
  • 99 Moores LK, Tritschler T, Brosnahan S. et al. Prevention, diagnosis, and treatment of VTE in patients with coronavirus disease 2019: CHEST guideline and expert panel report. Chest 2020; 158 (03) 1143-1163
    CrossrefPubMedGoogle Scholar
  • 100 Spyropoulos AC, Levy JH, Ageno W. et al; Subcommittee on Perioperative, Critical Care Thrombosis, Haemostasis of the Scientific, Standardization Committee of the International Society on Thrombosis and Haemostasis. Scientific and Standardization Committee communication: clinical guidance on the diagnosis, prevention, and treatment of venous thromboembolism in hospitalized patients with COVID-19. J Thromb Haemost 2020; 18 (08) 1859-1865
    CrossrefPubMedGoogle Scholar
  • 101 Condliffe R, Bunclark K, Hurdman J. et al. BTS Guidance on Venous Thromboembolic Disease in patients with COVID-19. Accessed May 8, 2020 at: https://www.brit-thoracic.org.uk/document-library/quality-improvement/covid-19/bts-guidance-on-venous-thromboembolic-disease-in-patients-with-covid-19/
    PubMedGoogle Scholar
  • 102 Testa S, Paoletti O, Giorgi-Pierfranceschi M, Pan A. Switch from oral anticoagulants to parenteral heparin in SARS-CoV-2 hospitalized patients. Intern Emerg Med 2020; 15 (05) 751-753
    CrossrefPubMedGoogle Scholar
  • 103 Duplaga BA, Rivers CW, Nutescu E. Dosing and monitoring of low-molecular-weight heparins in special populations. Pharmacotherapy 2001; 21 (02) 218-234
    CrossrefPubMedGoogle Scholar
  • 104 Kufel WD, Seabury RW, Darko W, Probst LA, Miller CD. Clinical feasibility of monitoring enoxaparin anti-Xa concentrations: are we getting it right?. Hosp Pharm 2017; 52 (03) 214-220
    CrossrefPubMedGoogle Scholar
  • 105 Wei MY, Ward SM. The anti-factor Xa range for low molecular weight heparin thromboprophylaxis. Hematol Rep 2015; 7 (04) 5844
    CrossrefPubMedGoogle Scholar
  • 106 Dutt T, Simcox D, Downey C. et al. Thromboprophylaxis in COVID-19: anti-FXa-the missing factor?. Am J Respir Crit Care Med 2020; 202 (03) 455-457
    CrossrefPubMedGoogle Scholar
  • 107 Connors JM, Levy JH. COVID-19 and its implications for thrombosis and anticoagulation. Blood 2020; 135 (23) 2033-2040
    CrossrefPubMedGoogle Scholar
  • 108 Lippi G, Favaloro EJ. D-dimer is associated with severity of coronavirus disease 2019: a pooled analysis. Thromb Haemost 2020; 120 (05) 876-878
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 109 Li X, Ma X. Acute respiratory failure in COVID-19: is it “typical” ARDS?. Crit Care 2020; 24 (01) 198
    CrossrefPubMedGoogle Scholar
  • 110 Mycroft-West C, Su D, Elli S. et al. The 2019 coronavirus (SARS-CoV-2) surface protein (Spike) S1 receptor binding domain undergoes conformational change upon heparin binding. bioRxiv 2020: 2020.02.29.971093
    PubMedGoogle Scholar
  • 111 van Haren FMP, Page C, Laffey JG. et al. Nebulised heparin as a treatment for COVID-19: scientific rationale and a call for randomised evidence. Crit Care 2020; 24 (01) 454
    CrossrefPubMedGoogle Scholar
  • 112 Al-Samkari H, Karp Leaf RS, Dzik WH. et al. COVID-19 and coagulation: bleeding and thrombotic manifestations of SARS-CoV-2 infection. Blood 2020; 136 (04) 489-500
    CrossrefPubMedGoogle Scholar
  • 113 Bompard F, Monnier H, Saab I. et al. Pulmonary embolism in patients with COVID-19 pneumonia. Eur Respir J 2020; 56 (01) 2001365
    CrossrefPubMedGoogle Scholar
  • 114 Grillet F, Behr J, Calame P, Aubry S, Delabrousse E. Acute pulmonary embolism associated with COVID-19 pneumonia detected with pulmonary CT angiography. Radiology 2020; 296 (03) E186-E188
    CrossrefPubMedGoogle Scholar
  • 115 Hékimian G, Lebreton G, Bréchot N, Luyt C-E, Schmidt M, Combes A. Severe pulmonary embolism in COVID-19 patients: a call for increased awareness. Crit Care 2020; 24 (01) 274
    CrossrefPubMedGoogle Scholar
  • 116 Hippensteel JA, Burnham EL, Jolley SE. Prevalence of venous thromboembolism in critically ill patients with COVID-19. Br J Haematol 2020; 190 (03) e134-e137
    CrossrefPubMedGoogle Scholar
  • 117 Léonard-Lorant I, Delabranche X, Séverac F. et al. Acute pulmonary embolism in patients with COVID-19 at CT angiography and relationship to D-dimer levels. Radiology 2020; 296 (03) E189-E191
    CrossrefPubMedGoogle Scholar
  • 118 Lodigiani C, Iapichino G, Carenzo L. et al; Humanitas COVID-19 Task Force. Venous and arterial thromboembolic complications in COVID-19 patients admitted to an academic hospital in Milan, Italy. Thromb Res 2020; 191: 9-14
    CrossrefPubMedGoogle Scholar
  • 119 Longchamp A, Longchamp J, Manzocchi-Besson S. et al. Venous thromboembolism in critically Ill patients with COVID-19: results of a screening study for deep vein thrombosis. Res Pract Thromb Haemost 2020; 4 (05) 842-847
    CrossrefPubMedGoogle Scholar
  • 120 Maatman TK, Jalali F, Feizpour C. et al. Routine venous thromboembolism prophylaxis may be inadequate in the hypercoagulable state of severe coronavirus disease 2019. Crit Care Med 2020; 48 (09) e783-e790
    CrossrefPubMedGoogle Scholar
  • 121 Mei F, Fan J, Yuan J. et al. Comparison of venous thromboembolism risks between COVID-19 pneumonia and community-acquired pneumonia patients. Arterioscler Thromb Vasc Biol 2020; 40 (09) 2332-2337
    CrossrefPubMedGoogle Scholar
  • 122 Nahum J, Morichau-Beauchant T, Daviaud F. et al. Venous thrombosis among critically ill patients with coronavirus disease 2019 (COVID-19). JAMA Netw Open 2020; 3 (05) e2010478
    CrossrefPubMedGoogle Scholar
  • 123 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; 142 (02) 181-183
    CrossrefPubMedGoogle Scholar
  • 124 Shah A, Donovan K, McHugh A. et al. Thrombotic and haemorrhagic complications in critically ill patients with COVID-19: a multicentre observational study. Crit Care 2020; 24 (01) 561
    CrossrefPubMedGoogle Scholar
  • 125 Thomas W, Varley J, Johnston A. et al. Thrombotic complications of patients admitted to intensive care with COVID-19 at a teaching hospital in the United Kingdom. Thromb Res 2020; 191: 76-77
    CrossrefPubMedGoogle Scholar
  • 126 Voicu S, Bonnin P, Stépanian A. et al. High prevalence of deep vein thrombosis in mechanically ventilated COVID-19 patients. J Am Coll Cardiol 2020; 76 (04) 480-482
    CrossrefPubMedGoogle Scholar
  • 127 Barnes GD, Burnett A, Allen A. et al. Thromboembolism and anticoagulant therapy during the COVID-19 pandemic: interim clinical guidance from the anticoagulation forum. J Thromb Thrombolysis 2020; 50 (01) 72-81
    CrossrefPubMedGoogle Scholar
  • 128 Bikdeli B, Madhavan MV, Jimenez D. et al; Global COVID-19 Thrombosis Collaborative Group, Endorsed by the ISTH, NATF, ESVM, and the IUA, Supported by the ESC Working Group on Pulmonary Circulation and Right Ventricular Function. COVID-19 and thrombotic or thromboembolic disease: implications for prevention, antithrombotic therapy, and follow-up: JACC state-of-the-art review. J Am Coll Cardiol 2020; 75 (23) 2950-2973
    CrossrefPubMedGoogle Scholar
  • 129 Zhai Z, Li C, Chen Y. et al; Prevention Treatment of VTE Associated with COVID-19 Infection Consensus Statement Group. Prevention and treatment of venous thromboembolism associated with coronavirus disease 2019 infection: a consensus statement before guidelines. Thromb Haemost 2020; 120 (06) 937-948
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 130 Marietta M, Ageno W, Artoni A. et al. COVID-19 and haemostasis: a position paper from Italian Society on Thrombosis and Haemostasis (SISET). Blood Transfus 2020; 18 (03) 167-169
    PubMedGoogle Scholar
  • 131 National Institute of Health. Antithrombotic Therapy in Patients with COVID-19. Accessed August 1, 2020 at: https://www.covid19treatmentguidelines.nih.gov/adjunctive-therapy/antithrombotic-therapy/
    PubMedGoogle Scholar
  • 132 Oudkerk M, Büller HR, Kuijpers D. et al. Diagnosis, prevention, and treatment of thromboembolic complications in COVID-19: report of the National Institute for Public Health of the Netherlands. Radiology 2020; 297 (01) E216-E222
    CrossrefPubMedGoogle Scholar
  • 133 Casini A, Alberio L, Angelillo-Scherrer A. et al. Thromboprophylaxis and laboratory monitoring for in-hospital patients with COVID-19 - a Swiss consensus statement by the Working Party Hemostasis. Swiss Med Wkly 2020; 150: w20247
    PubMedGoogle Scholar