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Current Respiratory Medicine Reviews

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ISSN (Print): 1573-398X
ISSN (Online): 1875-6387

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Mini-Review Article

Hyper-coagulopathy State in COVID-19: A Pivotal Challenge

Author(s): Najmeh Nameh Goshay Fard, Atena Vaghf, Ekhlas Torfi, Saeid Shahrabi and Seyed Mohammad Sadegh Pezeshki*

Volume 19, Issue 3, 2023

Published on: 31 July, 2023

Page: [170 - 179] Pages: 10

DOI: 10.2174/1573398X19666230703094330

Price: $65

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Abstract

Background: The novel SARS-CoV-2 has caused a global pandemic. COVID-19 infection is described by the adverse impact on the population’s health and economy. Coagulopathy is associated with various thrombotic complications and disease severity. Therefore, this review aims to elucidate the pathophysiology of this coagulopathy.

Methods: Relevant English language literature was searched and retrieved from the Google Scholar search engine and PubMed database. We used “COVID-19”, “SARS-CoV-2”, “Coagulopathy”, “Thrombosis”, “Anticoagulation”, and “ARDS” as keywords.

Results: Several studies showed that the primary targets of SARS-CoV-2 are pneumocytes, immune cells, and vascular endothelial cells. Coagulopathy appears to induce more thrombotic complications than hemorrhagic events. The critically ill patients stimulate the coagulopathy state and thrombosis complication through cytokine storm, systemic inflammation, complement cascade, and platelets. Accordingly, thromboembolic complications cause mortality among COVID-19-infected patients and can negatively affect disease management outcomes and treatment.

Conclusion: A pivotal clinical feature of acute COVID-19 infection is coagulopathy and prothrombotic events, which are associated with excessive arterial and venous thrombosis, microvascular thrombosis, and adverse clinical outcomes. Therefore, adopting an approach for preventing, treating, and reducing thrombotic and bleeding events in these patients is necessary.

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[1]
Banerjee A, Kulcsar K, Misra V, Frieman M, Mossman K. Bats and coronaviruses. Viruses 2019; 11(1): 41.
[http://dx.doi.org/10.3390/v11010041] [PMID: 30634396]
[2]
Mustafa NM. A Selim L. Characterisation of COVID-19 pandemic in paediatric age group: A systematic review and meta-analysis. J Clin Virol 2020; 128: 104395.
[http://dx.doi.org/10.1016/j.jcv.2020.104395] [PMID: 32417675]
[3]
Wu D, Wu T, Liu Q, Yang Z. The SARS-CoV-2 outbreak: What we know. Int J Infect Dis 2020; 94: 44-8.
[http://dx.doi.org/10.1016/j.ijid.2020.03.004] [PMID: 32171952]
[4]
Li H, Liu SM, Yu XH, Tang SL, Tang CK. Coronavirus disease 2019 (COVID-19): Current status and future perspectives. Int J Antimicrob Agents 2020; 55(5): 105951.
[http://dx.doi.org/10.1016/j.ijantimicag.2020.105951] [PMID: 32234466]
[5]
Rahman A, Niloofa R, Jayarajah U, De Mel S, Abeysuriya V, Seneviratne SL. Hematological abnormalities in COVID-19: A narrative review. Am J Trop Med Hyg 2021; 104(4): 1188-201.
[http://dx.doi.org/10.4269/ajtmh.20-1536] [PMID: 33606667]
[6]
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.
[http://dx.doi.org/10.1016/j.thromres.2020.04.024] [PMID: 32353746]
[7]
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.
[http://dx.doi.org/10.1016/j.thromres.2020.05.015] [PMID: 32419710]
[8]
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(5): 350-61.
[http://dx.doi.org/10.7326/M20-2566] [PMID: 32422076]
[9]
Stefan N, Birkenfeld AL, Schulze MB, Ludwig DS. Obesity and impaired metabolic health in patients with COVID-19. Nat Rev Endocrinol 2020; 16(7): 341-2.
[http://dx.doi.org/10.1038/s41574-020-0364-6] [PMID: 32327737]
[10]
Poissy J, Goutay J, Caplan M, et al. Pulmonary embolism in COVID-19 patients: Awareness of an increased prevalence. Circulation 2020; 142(2): 184-6.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.120.047430] [PMID: 32330083]
[11]
Baergen RN, Heller DS. Placental pathology in Covid-19 positive mothers: Preliminary findings. Pediatr Dev Pathol 2020; 23(3): 177-80.
[http://dx.doi.org/10.1177/1093526620925569] [PMID: 32397896]
[12]
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(4): 489-500.
[http://dx.doi.org/10.1182/blood.2020006520] [PMID: 32492712]
[13]
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(4): 844-7.
[http://dx.doi.org/10.1111/jth.14768] [PMID: 32073213]
[14]
Middeldorp S, Coppens M, van Haaps TF, et al. Incidence of venous thromboembolism in hospitalized patients with COVID-19. J Thromb Haemost 2020; 18(8): 1995-2002.
[http://dx.doi.org/10.1111/jth.14888] [PMID: 32369666]
[15]
Buioni D, Nardi P, Ruvolo G. Thrombocytopenia and coagulation disorders due to COVID 19 infection with concomitant cardiovascular diseases requiring anti-platelet and anticoagulant therapy, which strategy? Clin Chim Acta 2020; 508: 109.
[http://dx.doi.org/10.1016/j.cca.2020.05.031]
[16]
Rico-Mesa JS, Rosas D, Ahmadian-Tehrani A, White A, Anderson AS, Chilton R. The role of anticoagulation in COVID-19-induced hypercoagulability. Curr Cardiol Rep 2020; 22(7): 53.
[http://dx.doi.org/10.1007/s11886-020-01328-8] [PMID: 32556892]
[17]
Levi M, Thachil J, Iba T, Levy JH. Coagulation abnormalities and thrombosis in patients with COVID-19. Lancet Haematol 2020; 7(6): e438-40.
[http://dx.doi.org/10.1016/S2352-3026(20)30145-9] [PMID: 32407672]
[18]
Asakura H, Ogawa H. Potential of heparin and nafamostat combination therapy for COVID-19. J Thromb Haemost 2020; 18(6): 1521-2.
[http://dx.doi.org/10.1111/jth.14858] [PMID: 32302456]
[19]
Siow I, Lee KS, Zhang JJY, Saffari SE, Ng A, Young B. Stroke as a neurological complication of COVID-19: A systematic review and meta-analysis of incidence, outcomes and predictors. J Stroke Cerebrovasc Dis 2021; 30(3): 105549.
[http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2020.105549] [PMID: 33341565]
[20]
Gu SX, Tyagi T, Jain K, Gu VW, Lee SH, Hwa JM, et al. Thrombocytopathy and endotheliopathy: Crucial contributors to COVID-19 thromboinflammation. Nat Rev Cardiol 2021; 18(3): 194-209.
[PMID: 33214651]
[21]
Kalinskaya A, Dukhin O, Molodtsov I, Maltseva A, Sokorev D, Elizarova A. Dynamics of coagulopathy in patients with different COVID-19 severity. medRxiv 2020; 2020; 20145284.
[http://dx.doi.org/10.1101/2020.07.02.20145284]
[22]
Haematology TL. COVID-19 coagulopathy: An evolving story. Lancet Haematol 2020; 7(6): e425.
[http://dx.doi.org/10.1016/S2352-3026(20)30151-4] [PMID: 32470428]
[23]
Wang J, Hajizadeh N, Moore EE, et al. Tissue plasminogen activator (tPA) treatment for COVID-19 associated acute respiratory distress syndrome (ARDS): A case series. J Thromb Haemost 2020; 18(7): 1752-5.
[http://dx.doi.org/10.1111/jth.14828] [PMID: 32267998]
[24]
Saleh J, Peyssonnaux C, Singh KK, Edeas M. Mitochondria and microbiota dysfunction in COVID-19 pathogenesis. Mitochondrion 2020; 54: 1-7.
[http://dx.doi.org/10.1016/j.mito.2020.06.008] [PMID: 32574708]
[25]
Kasinathan G, Sathar J. Haematological manifestations, mechanisms of thrombosis and anti-coagulation in COVID-19 disease: A review. Ann Med Surg 2020; 56: 173-7.
[http://dx.doi.org/10.1016/j.amsu.2020.06.035] [PMID: 32637095]
[26]
Mei H, Luo L, Hu Y. Thrombocytopenia and thrombosis in hospitalized patients with COVID-19. J Hematol Oncol 2020; 13(1): 161.
[http://dx.doi.org/10.1186/s13045-020-01003-z] [PMID: 33261634]
[27]
Connors JM, Levy JH. COVID-19 and its implications for thrombosis and anticoagulation. Blood 2020; 135(23): 2033-40.
[http://dx.doi.org/10.1182/blood.2020006000] [PMID: 32339221]
[28]
Connors JM, Levy JH. Thromboinflammation and the hypercoagulability of COVID-19. J Thromb Haemost 2020; 18(7): 1559-61.
[http://dx.doi.org/10.1111/jth.14849] [PMID: 32302453]
[29]
Mousa-Ibrahim F, Berg S, Od’TPDetola O, Teitcher M, Ruland S. Intracranial hemorrhage in hospitalized SARS-CoV-2 patients: A case series. J Stroke Cerebrovasc Dis 2021; 30(1): 105428.
[http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2020.105428] [PMID: 33161349]
[30]
Melmed KR, Cao M, Dogra S, Zhang R, Yaghi S, Lewis A. Risk factors for intracerebral hemorrhage in patients with COVID-19. J Thromb Thrombolysis 2020; 51(4): 953-60.
[PMID: 32968850]
[31]
Del Borrello G, Giraudo I, Bondone C, Denina M, Garazzino S, Linari C. SARS-CoV-2 associated coagulopathy and thromboembolism prophylaxis in children: A single centre observational study. J Thromb Haemost 2020; 19(2): 522-30.
[PMID: 33305475]
[32]
Dogra S, Jain R, Cao M, et al. Hemorrhagic stroke and anticoagulation in COVID-19. J Stroke Cerebrovasc Dis 2020; 29(8): 104984.
[http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2020.104984] [PMID: 32689588]
[33]
Pavlov V, Beylerli O, Gareev I, Torres Solis LF, Solís Herrera A, Aliev G. COVID-19-related intracerebral hemorrhage. Front Aging Neurosci 2020; 12: 600172.
[http://dx.doi.org/10.3389/fnagi.2020.600172] [PMID: 33192492]
[34]
Vu D, Ruggiero M, Choi WS, et al. Three unsuspected CT diagnoses of COVID-19. Emerg Radiol 2020; 27(3): 229-32.
[http://dx.doi.org/10.1007/s10140-020-01775-4] [PMID: 32285222]
[35]
Ghani MU, Kumar M, Ghani U, Sonia F, Abbas SA. Intracranial hemorrhage complicating anticoagulant prophylactic therapy in three hospitalized COVID-19 patients. J Neurovirol 2020; 26(4): 602-4.
[http://dx.doi.org/10.1007/s13365-020-00869-6] [PMID: 32572835]
[36]
Chow LC, Chew LP, Leong TS, Mohamad TEE, Chua HH. Thrombosis and bleeding as presentation of COVID-19 infection with polycythemia vera. A case report. SN Compr Clin Med 2020; 2(11): 2406-10.
[http://dx.doi.org/10.1007/s42399-020-00537-0] [PMID: 33043250]
[37]
Zhang LB, Pang RR, Qiao QH, et al. Successful recovery of COVID-19-associated recurrent diarrhea and gastrointestinal hemorrhage using convalescent plasma. Mil Med Res 2020; 7(1): 45.
[http://dx.doi.org/10.1186/s40779-020-00273-5] [PMID: 32962760]
[38]
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(1): 561.
[http://dx.doi.org/10.1186/s13054-020-03260-3] [PMID: 32948243]
[39]
Nishiga M, Wang DW, Han Y, Lewis DB, Wu JC. COVID-19 and cardiovascular disease: From basic mechanisms to clinical perspectives. Nat Rev Cardiol 2020; 17(9): 543-58.
[http://dx.doi.org/10.1038/s41569-020-0413-9] [PMID: 32690910]
[40]
Jose RJ, Manuel A. COVID-19 cytokine storm: The interplay between inflammation and coagulation. Lancet Respir Med 2020; 8(6): e46-7.
[http://dx.doi.org/10.1016/S2213-2600(20)30216-2] [PMID: 32353251]
[41]
Aryal MR, Gosain R, Donato A, et al. Venous thromboembolism in COVID-19: Towards an ideal approach to thromboprophylaxis, screening, and treatment. Curr Cardiol Rep 2020; 22(7): 52.
[http://dx.doi.org/10.1007/s11886-020-01327-9] [PMID: 32529517]
[42]
Lopes RD, Fanaroff AC. Anticoagulation in COVID-19: It is time for high-quality evidence. J Am Coll Cardiol 2020; 76(16): 1827- 4829.
[http://dx.doi.org/10.1016/j.jacc.2020.09.008]
[43]
Chang H, Rockman CB, Jacobowitz GR, Speranza G, Johnson WS, Horowitz JM. Deep vein thrombosis in hospitalized patients with coronavirus disease 2019. J Vasc Surg Venous Lymphat Disord 2020; 9(3): 597-604.
[PMID: 33039545]
[44]
Alonso-Fernández A, Toledo-Pons N, Cosío BG, et al. Prevalence of pulmonary embolism in patients with COVID-19 pneumonia and high D-dimer values: A prospective study. PLoS One 2020; 15(8): e0238216.
[http://dx.doi.org/10.1371/journal.pone.0238216] [PMID: 32841275]
[45]
Fletcher-Sandersjöö A, Bellander BM. Is COVID-19 associated thrombosis caused by overactivation of the complement cascade? A literature review. Thromb Res 2020; 194: 36-41.
[http://dx.doi.org/10.1016/j.thromres.2020.06.027] [PMID: 32569879]
[46]
Mokhtari T, Hassani F, Ghaffari N, Ebrahimi B, Yarahmadi A, Hassanzadeh G. COVID-19 and multiorgan failure: A narrative review on potential mechanisms. J Mol Histol 2020; 51(6): 613-28.
[http://dx.doi.org/10.1007/s10735-020-09915-3] [PMID: 33011887]
[47]
Nevzorov I, Tulamo R, Albäck A, Lassila R. COVID-19 and SIC. (!) J Vasc Surg 2020; 72(3): 1148-50.
[http://dx.doi.org/10.1016/j.jvs.2020.05.047] [PMID: 32497749]
[48]
Cugno M, Meroni PL, Gualtierotti R, et al. Complement activation and endothelial perturbation parallel COVID-19 severity and activity. J Autoimmun 2021; 116: 102560.
[http://dx.doi.org/10.1016/j.jaut.2020.102560] [PMID: 33139116]
[49]
Magro CM, Mulvey J, Kubiak J, et al. Severe COVID-19: A multifaceted viral vasculopathy syndrome. Ann Diagn Pathol 2021; 50: 151645.
[http://dx.doi.org/10.1016/j.anndiagpath.2020.151645] [PMID: 33248385]
[50]
Hultström M, Frithiof R, Eriksson O, et al. Mannose-binding lectin is associated with thrombosis and coagulopathy in critically ill COVID-19 patients. Thromb Haemost 2020; 120(12): 1720-4.
[http://dx.doi.org/10.1055/s-0040-1715835] [PMID: 32871607]
[51]
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.
[http://dx.doi.org/10.1016/j.trsl.2020.04.007] [PMID: 32299776]
[52]
Magro CM, Mulvey JJ, Laurence J, et al. Docked severe acute respiratory syndrome coronavirus 2 proteins within the cutaneous and subcutaneous microvasculature and their role in the pathogenesis of severe coronavirus disease 2019. Hum Pathol 2020; 106: 106-16.
[http://dx.doi.org/10.1016/j.humpath.2020.10.002] [PMID: 33058948]
[53]
Malaquias MAS, Gadotti AC, da Silva Motta-Junior J, Martins APC, Azevedo MLV, Benevides APK, et al. The role of the lectin pathway of the complement system in SARS-CoV-2 lung injury. Transl Res 2020; 231: 55-63.
[PMID: 33221483]
[54]
Wang C, Xie J, Zhao L, Fei X, Zhang H, Tan Y. Aveolar macrophage activation and cytokine storm in the pathogenesis of severe COVID-19. Res Square 2020.
[http://dx.doi.org/10.21203/rs.3.rs-19346/v1]
[55]
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(3): 167-9.
[PMID: 32281926]
[56]
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(4): 268-77.
[http://dx.doi.org/10.7326/M20-2003] [PMID: 32374815]
[57]
Qi X, Keith KA, Huang JH. COVID-19 and stroke: A review. Brain Hemorrhages 2020; 2(2): 76-83.
[58]
Wadman M, Couzin-Frankel J, Kaiser J, Matacic C. A rampage through the body. Science 2020; 368(6489): 356-60.
[http://dx.doi.org/10.1126/science.368.6489.356] [PMID: 32327580]
[59]
Ayerbe L, Risco C, Ayis S. The association between treatment with heparin and survival in patients with Covid-19. J Thromb Thrombolysis 2020; 50(2): 298-301.
[http://dx.doi.org/10.1007/s11239-020-02162-z] [PMID: 32476080]
[60]
Rapkiewicz AV, Mai X, Carsons SE, et al. Megakaryocytes and platelet-fibrin thrombi characterize multi-organ thrombosis at autopsy in COVID-19: A case series. EClinicalMedicine 2020; 24: 100434.
[http://dx.doi.org/10.1016/j.eclinm.2020.100434] [PMID: 32766543]
[61]
Thachil J, Lisman T. Pulmonary megakaryocytes in coronavirus disease 2019 (COVID-19): Roles in thrombi and fibrosi. Semin Thromb Hemost 2020; 46(7): 831-4.
[http://dx.doi.org/10.1055/s-0040-1714274] [PMID: 32882717]
[62]
Hottz ED, Azevedo-Quintanilha IG, Palhinha L, et al. Platelet activation and platelet-monocyte aggregate formation trigger tissue factor expression in patients with severe COVID-19. Blood 2020; 136(11): 1330-41.
[http://dx.doi.org/10.1182/blood.2020007252] [PMID: 32678428]
[63]
Lichtenberger LM, Vijayan KV. Is COVID-19-induced platelet activation a cause of concern for cancer patients? Cancer Res 2020; 81(5): 1209-11.
[PMID: 33355186]
[64]
Zhang S, Liu Y, Wang X, et al. SARS-CoV-2 binds platelet ACE2 to enhance thrombosis in COVID-19. J Hematol Oncol 2020; 13(1): 120.
[http://dx.doi.org/10.1186/s13045-020-00954-7] [PMID: 32887634]
[65]
Parra-Izquierdo I, Aslan JE, Eds. Perspectives on platelet heterogeneity and host immune response in coronavirus disease 2019 (COVID-19). Semin Thromb Hemost 2020; 46(7): 826-30.
[http://dx.doi.org/10.1055/s-0040-1715093] [PMID: 32882716]
[66]
Levi M, Iba T. COVID-19 coagulopathy: Is it disseminated intravascular coagulation? Intern Emerg Med 2020; 16(2): 309-12.
[PMID: 33368021]
[67]
Takei H, Araki A, Watanabe H, Ichinose A, Sendo F. Rapid killing of human neutrophils by the potent activator phorbol 12-myristate 13-acetate (PMA) accompanied by changes different from typical apoptosis or necrosis. J Leukoc Biol 1996; 59(2): 229-40.
[http://dx.doi.org/10.1002/jlb.59.2.229] [PMID: 8603995]
[68]
Vorobjeva NV, Chernyak BV. NETosis: Molecular mechanisms, role in physiology and pathology. Biochemistry 2020; 85(10): 1178-90.
[http://dx.doi.org/10.1134/S0006297920100065] [PMID: 33202203]
[69]
Remijsen Q, Berghe TV, Wirawan E, et al. Neutrophil extracellular trap cell death requires both autophagy and superoxide generation. Cell Res 2011; 21(2): 290-304.
[http://dx.doi.org/10.1038/cr.2010.150] [PMID: 21060338]
[70]
Clark SR, Ma AC, Tavener SA, et al. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat Med 2007; 13(4): 463-9.
[http://dx.doi.org/10.1038/nm1565] [PMID: 17384648]
[71]
Galluzzi L, Vitale I, Aaronson SA, et al. Molecular mechanisms of cell death: Recommendations of the nomenclature committee on cell death 2018. Cell Death Differ 2018; 25(3): 486-541.
[http://dx.doi.org/10.1038/s41418-017-0012-4] [PMID: 29362479]
[72]
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): 1169-79.
[http://dx.doi.org/10.1182/blood.2020007008] [PMID: 32597954]
[73]
Hidalgo A. A NET-thrombosis axis in COVID-19. Blood 2020; 136(10): 1118-9.
[http://dx.doi.org/10.1182/blood.2020007951] [PMID: 32882018]
[74]
Barnes BJ, Adrover JM, Baxter-Stoltzfus A, et al. Targeting potential drivers of COVID-19: Neutrophil extracellular traps. J Exp Med 2020; 217(6): e20200652.
[http://dx.doi.org/10.1084/jem.20200652] [PMID: 32302401]
[75]
Ram Kumar Pandian S, Arunachalam S, Deepak V, Kunjiappan S, Sundar K. Targeting complement cascade: An alternative strategy for COVID-19. 3 Biotech 2020; 10(11): 479.
[http://dx.doi.org/10.1007/s13205-020-02464-2]
[76]
Maxwell AJ, Ding J, You Y, Dong Z, Chehade H, Alvero A, et al. Identification of key signaling pathways induced by SARS-CoV2 that underlie thrombosis and vascular injury in COVID-19 patients. J Leukoc Biol 2020; 109(1): 35-47.
[PMID: 33242368]
[77]
Aid M, Busman-Sahay K, Vidal SJ, Maliga Z, Bondoc S, Starke C, et al. Vascular disease and thrombosis in SARS-CoV-2-infected Rhesus macaques. Cell 2020; 183(5): 1354.e13-.
[http://dx.doi.org/10.1016/j.cell.2020.10.005] [PMID: 33065030]
[78]
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.
[http://dx.doi.org/10.1016/j.carpath.2020.107233] [PMID: 32434133]
[79]
Canonico ME, Siciliano R, Scudiero F, Sanna GD, Parodi G. The tug-of-war between coagulopathy and anticoagulant agents in patients with COVID-19. Eur Heart J Cardiovasc Pharmacother 2020; 6(4): 262-4.
[http://dx.doi.org/10.1093/ehjcvp/pvaa048] [PMID: 32383737]
[80]
Nadkarni GN, Lala A, Bagiella E, et al. Anticoagulation, bleeding, mortality, and pathology in hospitalized patients with COVID-19. J Am Coll Cardiol 2020; 76(16): 1815-26.
[http://dx.doi.org/10.1016/j.jacc.2020.08.041] [PMID: 32860872]
[81]
Asakura H, Ogawa H. COVID-19-associated coagulopathy and disseminated intravascular coagulation. Int J Hematol 2020; 113(1): 45-57.
[PMID: 33161508]
[82]
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; 75(23): 2950-73.
[http://dx.doi.org/10.1016/j.jacc.2020.04.031] [PMID: 32311448]
[83]
Hess DC, Eldahshan W, Rutkowski E. COVID-19-related stroke. Transl Stroke Res 2020; 11(3): 322-5.
[http://dx.doi.org/10.1007/s12975-020-00818-9] [PMID: 32378030]
[84]
Hajra A, Mathai SV, Ball S, et al. Management of thrombotic complications in COVID-19: An update. Drugs 2020; 80(15): 1553-62.
[http://dx.doi.org/10.1007/s40265-020-01377-x] [PMID: 32803670]
[85]
Kamel AM, Sobhy M, Magdy N, Sabry N, Farid S. Anticoagulation outcomes in hospitalized Covid-19 patients: A systematic review and meta-analysis of case-control and cohort studies. Rev Med Virol 2021; 31(3): e2180.
[http://dx.doi.org/10.1002/rmv.2180] [PMID: 33022834]
[86]
Aoyama T, Ino Y, Ozeki M, et al. Pharmacological studies of FUT-175, nafamstat mesilate. I. Inhibition of protease activity in in Vitro and in Vivo experiments. Jpn J Pharmacol 1984; 35(3): 203-27.
[http://dx.doi.org/10.1254/jjp.35.203] [PMID: 6482087]
[87]
Takahashi W, Yoneda T, Koba H, Ueda T, Tsuji N, Ogawa H, et al. Potential mechanisms of nafamostat therapy for severe COVID-19 pneumonia with disseminated intravascular coagulation. Int J Infect Dis 2020; 102: 529-31.
[PMID: 33157292]
[88]
Ahmed S, Zimba O, Gasparyan AY. Thrombosis in Coronavirus disease 2019 (COVID-19) through the prism of Virchow’s triad. Clin Rheumatol 2020; 39(9): 2529-43.
[http://dx.doi.org/10.1007/s10067-020-05275-1] [PMID: 32654082]
[89]
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(5): 1094-9.
[http://dx.doi.org/10.1111/jth.14817] [PMID: 32220112]
[90]
Guo W, Li M, Dong Y, et al. Diabetes is a risk factor for the progression and prognosis of COVID -19. Diabetes Metab Res Rev 2020; 36(7): e3319.
[http://dx.doi.org/10.1002/dmrr.3319] [PMID: 32233013]
[91]
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(10223): 507-13.
[http://dx.doi.org/10.1016/S0140-6736(20)30211-7] [PMID: 32007143]
[92]
Garg S. Hospitalization rates and characteristics of patients hospitalized with laboratory-confirmed coronavirus disease 2019-COVID-NET, 14 States, March 1-30, 2020. MMWR 2020; 69(15): 1-7.
[93]
Yang J, Zheng Y, Gou X, et al. Prevalence of comorbidities and its effects in patients infected with SARS-CoV-2: A systematic review and meta-analysis. Int J Infect Dis 2020; 94: 91-5.
[http://dx.doi.org/10.1016/j.ijid.2020.03.017] [PMID: 32173574]
[94]
Ibañez C, Perdomo J, Calvo A, Ferrando C, Reverter J, Tassies D. High D dimers and low global fibrinolysis coexist in COVID19 patients: What is going on in there? J Thromb Thrombolysis 2020; 51(2): 308-12.
[PMID: 32671609]
[95]
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; 7(8): e575-82.
[http://dx.doi.org/10.1016/S2352-3026(20)30216-7] [PMID: 32619411]
[96]
Cattaneo M, Bertinato EM, Birocchi S, Brizio C, Malavolta D, Manzoni M. Pulmonary embolism or pulmonary thrombosis in COVID-19? Is the recommendation to use high-dose heparin for thromboprophylaxis justified? Thromb Haemost 2020; 120(8): 1230-2.
[http://dx.doi.org/10.1055/s-0040-1712097] [PMID: 32349132]
[97]
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(6): 1421-4.
[http://dx.doi.org/10.1111/jth.14830] [PMID: 32271988]
[98]
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: 145-7.
[http://dx.doi.org/10.1016/j.thromres.2020.04.013]
[99]
Dolhnikoff M, Duarte-Neto AN, de Almeida MRA, et al. Pathological evidence of pulmonary thrombotic phenomena in severe COVID-19. J Thromb Haemost 2020; 18(6): 1517-9.
[http://dx.doi.org/10.1111/jth.14844] [PMID: 32294295]
[100]
Hanif A, Khan S, Mantri N, et al. Thrombotic complications and anticoagulation in COVID-19 pneumonia: A New York City hospital experience. Ann Hematol 2020; 99(10): 2323-8.
[http://dx.doi.org/10.1007/s00277-020-04216-x] [PMID: 32808105]
[101]
Bilaloglu S, Aphinyanaphongs Y, Jones S, Iturrate E, Hochman J, Berger JS. Thrombosis in hospitalized patients with COVID-19 in a New York City health system. JAMA 2020; 324(8): 799-801.
[http://dx.doi.org/10.1001/jama.2020.13372] [PMID: 32702090]
[102]
Vabret N, Britton GJ, Gruber C, et al. Immunology of COVID-19: Current state of the science. Immunity 2020; 52(6): 910-41.
[http://dx.doi.org/10.1016/j.immuni.2020.05.002] [PMID: 32505227]
[103]
Chen G, Wu D, Guo W, et al. Clinical and immunological features of severe and moderate coronavirus disease 2019. J Clin Invest 2020; 130(5): 2620-9.
[http://dx.doi.org/10.1172/JCI137244] [PMID: 32217835]
[104]
Mehta P, McAuley DF, Brown M, Sanchez E, Tattersall RS, Manson JJ. COVID-19: Consider cytokine storm syndromes and immunosuppression. Lancet 2020; 395(10229): 1033-4.
[http://dx.doi.org/10.1016/S0140-6736(20)30628-0] [PMID: 32192578]
[105]
Al-Ani F, Chehade S, Lazo-Langner A. Thrombosis risk associated with COVID-19 infection. A scoping review. Thromb Res 2020; 192: 152-60.
[http://dx.doi.org/10.1016/j.thromres.2020.05.039] [PMID: 32485418]
[106]
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): 1135-40.
[http://dx.doi.org/10.1016/S1473-3099(20)30434-5] [PMID: 32526193]
[107]
Demelo-Rodríguez P, Cervilla-Muñoz 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.
[http://dx.doi.org/10.1016/j.thromres.2020.05.018] [PMID: 32405101]
[108]
Cho ES, McClelland PH, Cheng O, Kim Y, Hu J, Zenilman ME, et al. Utility of d-dimer for diagnosis of deep vein thrombosis in coronavirus disease-19 infection. J Vasc Surg Venous Lymphat Disord 2020; 9(1): 47-53.
[PMID: 32738407]
[109]
Mouhat B, Besutti M, Bouiller K, et al. Elevated D-dimers and lack of anticoagulation predict PE in severe COVID-19 patients. Eur Respir J 2020; 56(4): 2001811.
[http://dx.doi.org/10.1183/13993003.01811-2020] [PMID: 32907890]
[110]
Obi AT, Barnes GD, Wakefield TW, Eliason JL, Arndt E, Henke PK. Practical diagnosis and treatment of suspected venous thromboembolism during COVID-19 pandemic. J Vasc Surg Venous Lymphat Disord 2020; 8(4): 526-34.
[http://dx.doi.org/10.1016/j.jvsv.2020.04.009] [PMID: 32305585]
[111]
Roncon L, Zuin M, Barco S, et al. Incidence of acute pulmonary embolism in COVID-19 patients: Systematic review and meta-analysis. Eur J Intern Med 2020; 82: 29-37.
[http://dx.doi.org/10.1016/j.ejim.2020.09.006] [PMID: 32958372]
[112]
Thachil J, Tang N, Gando S, et al. ISTH interim guidance on recognition and management of coagulopathy in COVID-19. J Thromb Haemost 2020; 18(5): 1023-6.
[http://dx.doi.org/10.1111/jth.14810] [PMID: 32338827]
[113]
Ackermann M, Verleden SE, Kuehnel M, et al. Pulmonary vascular endothelialitis, thrombosis, and angiogenesis in Covid-19. N Engl J Med 2020; 383(2): 120-8.
[http://dx.doi.org/10.1056/NEJMoa2015432] [PMID: 32437596]
[114]
Brosnahan SB, Smilowitz NR, Amoroso NE, Barfield M, Berger JS, Goldenberg R, et al. Thrombosis at hospital presentation in patients with and without COVID-19. J Vasc Surg Venous Lymphat Disord 2020; 9(4): 845-52.
[http://dx.doi.org/10.1016/j.jvsv.2020.11.004] [PMID: 33186750]
[115]
Altschul DJ, Unda SR, de La Garza Ramos R, et al. Hemorrhagic presentations of COVID-19: Risk factors for mortality. Clin Neurol Neurosurg 2020; 198: 106112.
[http://dx.doi.org/10.1016/j.clineuro.2020.106112] [PMID: 32738585]
[116]
Motaganahalli RL, Kapoor R, Timsina LR, Gutwein AR, Ingram MD, Raman S. Clinical and laboratory characteristics of patients with novel coronavirus disease-2019 infection and deep venous thrombosis. J Vasc Surg Venous Lymphat Disord 2021; 9(3): 605.e2-14.e2.
[117]
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; 76(1): 122-4.
[http://dx.doi.org/10.1016/j.jacc.2020.05.001] [PMID: 32387623]
[118]
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(7): 1743-6.
[http://dx.doi.org/10.1111/jth.14869] [PMID: 32320517]
[119]
Yin S, Huang M, Li D, Tang N. Difference of coagulation features between severe pneumonia induced by SARS-CoV2 and non-SARS-CoV2. J Thromb Thrombolysis 2020; 51(4): 1111-2.
[PMID: 32246317]

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