COVID-19 Associated Coagulopathy and Implications for its Treatment

1. Layton DS, Choudhary A, Bean AGD. Breaking the chain of zoonoses through biosecurity in livestock. Vaccine 2017;35:5967-73.10.1016/j.vaccine.2017.07.110Search in Google Scholar

2. Wu F, Zhao S, Yu B, et al. A new coronavirus associated with human respiratory disease in China. Nature 2020;579:265-9.10.1038/s41586-020-2008-3Search in Google Scholar

3. Hulswit RJ, de Haan CA, Bosch BJ. Coronavirus Spike Protein and Tropism Changes. Adv Virus Res 2016;96:29-57.10.1016/bs.aivir.2016.08.004Search in Google Scholar

4. Lu R, Zhao X, Li J, et al. Genomic characterisation and epidemiology of 2019 novel coronavirus: implications for virus origins and receptor binding. Lancet 2020;395:565-74.10.1016/S0140-6736(20)30251-8Search in Google Scholar

5. Schnittler HJ, Feldmann H. Viral hemorrhagic fever – a vascular disease? Thromb Haemost 2003;89:967-72.Search in Google Scholar

6. Iba T, Levy JH, Thachil J, et al. The progression from coagulopathy to disseminated intravascular coagulation in representative underlying diseases. Thromb Res 2019;179:11-4.10.1016/j.thromres.2019.04.03031059996Search in Google Scholar

7. Iba T, Levy JH, Wada H, et al. Differential diagnoses for sepsis-induced disseminated intravascular coagulation: communication from the SSC of the ISTH. J Thromb Haemost 2019;17:415-9.10.1111/jth.1435430618150Search in Google Scholar

8. Woei AJFJ, van der Starre WE, Tesselaar ME, et al. Procoagulant tissue factor activity on microparticles is associated with disease severity and bacteremia in febrile urinary tract infections. Thromb Res 2014;133:799-803.10.1016/j.thromres.2014.03.00724657035Search in Google Scholar

9. Gould TJ, Lysov Z, Swystun LL, et al. Extracellular Histones Increase Tissue Factor Activity and Enhance Thrombin Generation by Human Blood Monocytes. Shock 2016;46:65562.10.1097/SHK.000000000000068027405066Search in Google Scholar

10. Iba T, Levy JH. Inflammation and thrombosis: roles of neutrophils, platelets and endothelial cells and their interactions in thrombus formation during sepsis. J Thromb Haemost 2018;16:231-41.10.1111/jth.1391129193703Search in Google Scholar

11. Suzuki K, Wada H, Imai H, et al. A re-evaluation of the D-dimer cut-off value for making a diagnosis according to the ISTH overt-DIC diagnostic criteria: communication from the SSC of the ISTH. J Thromb Haemost 2018;16:1442-4.10.1111/jth.1413429846034Search in Google Scholar

12. Iba T, Levy JH, Warkentin TE, et al. Diagnosis and management of sepsis-induced coagulopathy and disseminated intravascular coagulation. J Thromb Haemost 2019.10.1002/ams2.411Search in Google Scholar

13. Taylor FB, Jr., Toh CH, Hoots WK, Wada H, Levi M. Towards definition, clinical and laboratory criteria, and a scoring system for disseminated intravascular coagulation. Thromb Hae-most 2001;86:1327-30.10.1055/s-0037-1616068Search in Google Scholar

14. Iba T, Levy JH, Yamakawa K, et al. Proposal of a two-step process for the diagnosis of sepsis-induced disseminated intravascular coagulation. J Thromb Haemost 2019;17:1265-8.10.1111/jth.14482Search in Google Scholar

15. 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 2020.10.1111/jth.14768Search in Google Scholar

16. 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 2020.10.1111/jth.14817Search in Google Scholar

17. Chen N, Zhou M, Dong X, et al. Epidemiological and clinical characteristics of 99 cases of 2019 novel coronavirus pneumonia in Wuhan, China: a descriptive study. Lancet 2020;395:507-13.10.1016/S0140-6736(20)30211-7Search in Google Scholar

18. Wang D, Hu B, Hu C, et al. Clinical Characteristics of 138 Hospitalized Patients With 2019 Novel Coronavirus-Infected Pneumonia in Wuhan, China. JAMA 2020.10.1001/jama.2020.1585Search in Google Scholar

19. 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;395:1054-62.10.1016/S0140-6736(20)30566-3Search in Google Scholar

20. Guan WJ, Ni ZY, Hu Y, et al. Clinical Characteristics of Coronavirus Disease 2019 in China. N Engl J Med 2020.Search in Google Scholar

21. Metlay JP, Waterer GW, Long AC, et al. Diagnosis and Treatment of Adults with Community-acquired Pneumonia. An Official Clinical Practice Guideline of the American Thoracic Society and Infectious Diseases Society of America. Am J Respir Crit Care Med 2019;200:e45-e67.10.1164/rccm.201908-1581ST681243731573350Search in Google Scholar

22. Engelmann B, Massberg S. Thrombosis as an intravascular effector of innate immunity. Nat Rev Immunol 2013;13:34-45.10.1038/nri334523222502Search in Google Scholar

23. Delabranche X, Helms J, Meziani F. Immunohaemostasis: a new view on haemostasis during sepsis. Annals of intensive care 2017;7:117.10.1186/s13613-017-0339-5571229829197958Search in Google Scholar

24. Jackson SP, Darbousset R, Schoenwaelder SM. Thromboinflammation: challenges of therapeutically targeting coagulation and other host defense mechanisms. Blood 2019;133:90618.10.1182/blood-2018-11-88299330642917Search in Google Scholar

25. Smith SA, Mutch NJ, Baskar D et al. Polyphosphate modulates blood coagulation and fibrinolysis. Proc Natl Acad Sci U S A 2006;103:903-8.10.1073/pnas.0507195103134797916410357Search in Google Scholar

26. Subramaniam S, Jurk K, Hobohm L, et al. Distinct contributions of complement factors to platelet activation and fibrin formation in venous thrombus development. Blood 2017;129:2291-302.10.1182/blood-2016-11-749879539948528223279Search in Google Scholar

27. Noubouossie DF, Reeves BN, Strahl BD, Key NS. Neutrophils: back in the thrombosis spotlight. Blood 2019;133:2186-97.10.1182/blood-2018-10-862243721873130898858Search in Google Scholar

28. Rittirsch D, Flierl MA, Ward PA. Harmful molecular mechanisms in sepsis. Nat Rev Immunol 2008;8:776-87.10.1038/nri2402278696118802444Search in Google Scholar

29. Iba T, Levy JH. Derangement of the endothelial glycocalyx in sepsis. J Thromb Haemost 2019;17:283-94.10.1111/jth.1437130582882Search in Google Scholar

30. Semeraro F, Colucci M, Caironi P, et al. Platelet Drop and Fibrinolytic Shutdown in Patients With Sepsis. Crit Care Med 2018;46:e221-e8.10.1097/CCM.000000000000291929261568Search in Google Scholar

31. Levy JH, Koster A, Quinones QJ, Milling TJ, Key NS. Antifibrinolytic Therapy and Perioperative Considerations. Anesthesiology 2018;128:657-70.10.1097/ALN.0000000000001997581133129200009Search in Google Scholar

32. Iba T, Arakawa M, Ohchi Y, et al. Prediction of Early Death in Patients With SepsisAssociated Coagulation Disorder Treated With Antithrombin Supplementation. Clin Appl Thromb He-most 2018:1076029618797474.10.1177/1076029618797474671484230198317Search in Google Scholar

33. Kienast J, Juers M, Wiedermann CJ, et al. Treatment effects of high-dose antithrombin without concomitant heparin in patients with severe sepsis with or without disseminated intravascular coagulation. J Thromb Haemost 2006;4:90-7.10.1111/j.1538-7836.2005.01697.xSearch in Google Scholar

34. Yamakawa K, Levy JH, Iba T. Recombinant human soluble thrombomodulin in patients with sepsis-associated coagulopathy (SCARLET): an updated meta-analysis. Crit Care 2019;23:302.10.1186/s13054-019-2587-2Search in Google Scholar

35. Chen G, Wu D, Guo W, et al. Clinical and immunologic features in severe and moderate Coronavirus Disease 2019. J Clin Invest 2020.10.1101/2020.02.16.20023903Search in Google Scholar

36. Huang C, Wang Y, Li X, et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet 2020;395:497-506.10.1016/S0140-6736(20)30183-5Search in Google Scholar

37. Levi M, Scully M. How I treat disseminated intravascular coagulation. Blood 2018;131:845-54.10.1182/blood-2017-10-804096Search in Google Scholar

38. Lippi G, Bonfanti L, Saccenti C, Cervellin G. Causes of elevated D-dimer in patients admitted to a large urban emergency department. Eur J Intern Med 2014;25:45-8.10.1016/j.ejim.2013.07.012Search in Google Scholar

39. Mehta P, McAuley DF, Brown M, et al. COVID-19: consider cytokine storm syndromes and immunosuppression. Lancet 2020;395:1033-4.10.1016/S0140-6736(20)30628-0Search in Google Scholar

40. Ranucci M, Ballotta A, Di Dedda U, et al. The procoagulant pattern of patients with COVID-19 acute respiratory distress syndrome. J Thromb Haemost 2020.10.1111/jth.1485432302448Search in Google Scholar

41. Saffarzadeh M, Juenemann C, Queisser MA, et al. Neutro-phil extracellular traps directly induce epithelial and endothelial cell death: a predominant role of histones. PLoS One 2012;7:e32366.10.1371/journal.pone.0032366328964822389696Search in Google Scholar

42. Ferrario CM, Jessup J, Chappell MC, et al. Effect of angiotensin-converting enzyme inhibition and angiotensin II receptor blockers on cardiac angiotensin-converting enzyme 2. Circulation 2005;111:2605-10.10.1161/CIRCULATIONAHA.104.51046115897343Search in Google Scholar

43. Varga Z, Flammer AJ, Steiger P, et al. Endothelial cell infection and endotheliitis in COVID-19. Lancet 2020.10.1016/S0140-6736(20)30937-5Search in Google Scholar

44. Stein PD, Kayali F, Olson RE, Milford CE. Pulmonary thromboembolism in Asians/Pacific Islanders in the United States: analysis of data from the National Hospital Discharge Survey and the United States Bureau of the Census. Am J Med 2004;116:435-42.10.1016/j.amjmed.2003.11.02015047032Search in Google Scholar

45. Zakai NA, McClure LA. Racial differences in venous thromboembolism. J Thromb Haemost 2011;9:1877-82.10.1111/j.1538-7836.2011.04443.x21797965Search in Google Scholar

46. Danzi GB, Loffi M, Galeazzi G, Gherbesi E. Acute pulmonary embolism and COVID-19 pneumonia: a random association? European Heart Journal 2020.10.1093/eurheartj/ehaa254718440632227120Search in Google Scholar

47. Xie Y, Wang X, Yang P, Zhang S. COVID-19 Complicated by Acute Pulmonary Embolism. Radiology: Cardiothoracic Imaging 2020;2:e200067.10.1148/ryct.2020200067723343133778561Search in Google Scholar

48. Tian S, Hu W, Niu L, Liu H, Xu H, Xiao S-Y. Pulmonary Pathology of Early-Phase 2019 Novel Coronavirus (COVID-19) Pneumonia in Two Patients With Lung Cancer. Journal of Thoracic Oncology.Search in Google Scholar

49. Klok FA, Kruip M, van der Meer NJM, et al. Incidence of thrombotic complications in critically ill ICU patients with COVID-19. Thromb Res 2020.10.1016/j.thromres.2020.04.013714671432291094Search in Google Scholar

50. Poissy J, Goutay J, Caplan M, et al. Pulmonary Embolism in COVID-19 Patients: Awareness of an Increased Prevalence. Circulation 2020.10.1161/CIRCULATIONAHA.120.04743032330083Search in Google Scholar

51. Pannucci CJ, Fleming KI, Holoyda K, Moulton L, Prazak AM, Varghese TK, Jr. Enoxaparin 40 mg per Day Is Inadequate for Venous Thromboembolism Prophylaxis After Thoracic Surgical Procedure. Ann Thorac Surg 2018;106:404-11.10.1016/j.athoracsur.2018.02.08529626461Search in Google Scholar

52. Wang TF, Milligan PE, Wong CA, Deal EN, Thoelke MS, Gage BF. Efficacy and safety of high-dose thromboprophylaxis in morbidly obese inpatients. Thromb Haemost 2014;111:8893.10.1160/TH13-01-0042450572624136071Search in Google Scholar

53. Wada H, Thachil J, Di Nisio M, et al. Guidance for diagnosis and treatment of DIC from harmonization of the recommendations from three guidelines. J Thromb Haemost 2013.10.1111/jth.1215523379279Search in Google Scholar

54. Lin L, Lu L, Cao W, Li T. Hypothesis for potential pathogenesis of SARS-CoV-2 infection-a review of immune changes in patients with viral pneumonia. Emerg Microbes Infect 2020;9:727-32.10.1080/22221751.2020.1746199717033332196410Search in Google Scholar

55. Iba T, Levy JH, Raj A, Warkentin TE. Advance in the Management of Sepsis-Induced Coagulopathy and Disseminated Intravascular Coagulation. J Clin Med 2019;8.10.3390/jcm8050728657223431121897Search in Google Scholar

56. Vicenzi E, Canducci F, Pinna D, et al. Coronaviridae and SARS-associated coronavirus strain HSR1. Emerg Infect Dis 2004;10:413-8.10.3201/eid1003.030683332280715109406Search in Google Scholar

57. Du L, Kao RY, Zhou Y, et al. Cleavage of spike protein of SARS coronavirus by protease factor Xa is associated with viral infectivity. Biochem Biophys Res Commun 2007;359:174-9.10.1016/j.bbrc.2007.05.092232397717533109Search in Google Scholar

58. Kam YW, Okumura Y, Kido H et al. Cleavage of the SARS coronavirus spike glycoprotein by airway proteases enhances virus entry into human bronchial epithelial cells in vitro. PLoS One 2009;4:e7870.10.1371/journal.pone.0007870277342119924243Search in Google Scholar

59. Smyth SS, McEver RP, Weyrich AS, et al. Platelet functions beyond hemostasis. J Thromb Haemost 2009;7:1759-66.10.1111/j.1538-7836.2009.03586.x19691483Search in Google Scholar

60. Levy JH, Goodnough LT. How I use fibrinogen replacement therapy in acquired bleeding. Blood 2015;125:1387-93.10.1182/blood-2014-08-55200025519751Search in Google Scholar

61. Thachil J, Tang N, Gando S, et al. ISTH interim guidance on recognition and management of coagulopathy in COVID-19. J Thromb Haem, 2020.10.1111/jth.1481032338827Search in Google Scholar