COVID‑19 and ischemic stroke: Mechanisms of hypercoagulability (Review)
- Authors:
- Shuoqi Zhang
- Jinming Zhang
- Chunxu Wang
- Xiaojing Chen
- Xinyi Zhao
- Haijiao Jing
- Huan Liu
- Zhuxin Li
- Lihua Wang
- Jialan Shi
-
Affiliations: Department of Neurology, The Second Hospital, Harbin Medical University, Harbin, Heilongjiang 150001, P.R. China, Department of Hematology, The First Hospital, Harbin Medical University, Harbin, Heilongjiang 150001, P.R. China, Department of Cardiology, The Second Hospital, Harbin Medical University, Harbin, Heilongjiang 150001, P.R. China, Department of Acupuncture and Moxibustion, College of Acupuncture and Moxibustion, Heilongjiang University of Chinese Medicine, Harbin, Heilongjiang 150040, P.R. China - Published online on: January 13, 2021 https://doi.org/10.3892/ijmm.2021.4854
- Article Number: 21
-
Copyright: © Zhang et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
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|
Jamwal S, Gautam A, Elsworth J, Kumar M, Chawla R and Kumar P: An updated insight into the molecular pathogenesis, secondary complications and potential therapeutics of COVID-19 pandemic. Life Sci. 257:1181052020. View Article : Google Scholar : PubMed/NCBI | |
|
Nalleballe K, Reddy Onteddu S, Sharma R, Dandu V, Brown A, Jasti M, Yadala S, Veerapaneni K, Siddamreddy S, Avula A, et al: Spectrum of neuropsychiatric manifestations in COVID-19. Brain Behav Immun. 88:71–74. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Mao L, Jin H, Wang M, Hu Y, Chen S, He Q, Chang J, Hong C, Zhou Y, Wang D, et al: Neurologic manifestations of hospitalized patients with coronavirus disease 2019 in Wuhan, China. JAMA Neurol. 77:683–690. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Han H, Yang L, Liu R, Liu F, Wu KL, Li J, Liu XH and Zhu CL: Prominent changes in blood coagulation of patients with SARS-CoV-2 infection. Clin Chem Lab Med. 58:1116–1120. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Tang N, Li D, Wang X and Sun Z: Abnormal coagulation parameters are associated with poor prognosis in patients with novel coronavirus pneumonia. J Thromb Haemost. 18:844–847. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Yin S, Huang M, Li D and Tang N: Difference of coagulation features between severe pneumonia induced by SARS-CoV2 and non-SARS-CoV2. J Thromb Thrombolysis. 1–4. 2020. | |
|
Helms J, Tacquard C, Severac F, Leonard-Lorant I, Ohana M, Delabranche X, Merdji H, Clere-Jehl R, Schenck M, Fagot Gandet F, et al: High risk of thrombosis in patients with severe SARS-CoV-2 infection: A multicenter prospective cohort study. Intensive Care Med. 46:1089–1098. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Whyte CS, Morrow GB, Mitchell JL, Chowdary P and Mutch NJ: Fibrinolytic abnormalities in acute respiratory distress syndrome (ARDS) and versatility of thrombolytic drugs to treat COVID-19. J Thromb Haemost. 18:1548–1555. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Wichmann D, Sperhake JP, Lütgehetmann M, Steurer S, Edler C, Heinemann A, Heinrich F, Mushumba H, Kniep I, Schröder AS, et al: Autopsy findings and venous thromboembolism in patients With COVID-19: A prospective cohort study. Ann Intern Med. 173:268–277. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Xiong M, Liang X and Wei YD: Changes in blood coagulation in patients with severe coronavirus disease 2019 (COVID-19): A meta-analysis. Br J Haematol. 189:1050–1052. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Lodigiani C, Iapichino G, Carenzo L, Cecconi M, Ferrazzi P, Sebastian T, Kucher N, Studt JD, Sacco C, Bertuzzi A, et al: Venous and arterial thromboembolic complications in COVID-19 patients admitted to an academic hospital in Milan, Italy. Thromb Res. 191:9–14. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Avula A, Nalleballe K, Narula N, Sapozhnikov S, Dandu V, Toom S, Glaser A and Elsayegh D: COVID-19 presenting as stroke. Brain Behav Immun. 87:115–119. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Fara MG, Stein LK, Skliut M, Morgello S, Fifi JT and Dhamoonr MS: Macrothrombosis and stroke in patients with mild Covid-19 infection. J Thromb Haemost. 18:2031–2033. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Beyrouti R, Adams ME, Benjamin L, Cohen H, Farmer SF, Goh YY, Humphries F, Jäger HR, Losseff NA, Perry RJ, et al: Characteristics of ischaemic stroke associated with COVID-19. J Neurol Neurosurg Psychiatry. 91:889–891. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Li YC, Bai WZ and Hashikawa T: The neuroinvasive potential of SARS-CoV2 may play a role in the respiratory failure of COVID-19 patients. J Med Virol. 92:552–555. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Yaghi S, Ishida K, Torres J, Mac Grory B, Raz E, Humbert K, Henninger N, Trivedi T, Lillemoe K, Alam S, et al: SARS-CoV-2 and stroke in a New York healthcare system. Stroke. 51:2002–2011. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Oxley TJ, Mocco J, Majidi S, Kellner CP, Shoirah H, Singh IP, De Leacy RA, Shigematsu T, Ladner TR, Yaeger KA, et al: Large-vessel stroke as a presenting feature of Covid-19 in the young. N Engl J Med. 382:e602020. View Article : Google Scholar : PubMed/NCBI | |
|
Pacha O, Sallman MA and Evans SE: COVID-19: A case for inhibiting IL-17? Nat Rev Immunol. 20:345–346. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Mehta P, McAuley DF, Brown M, Sanchez E, Tattersall RS and Manson JJ; HLH Across Speciality Collaboration UK: COVID-19: Consider cytokine storm syndromes and immunosuppression. Lancet. 395:1033–1034. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Sawdey MS and Loskutoff DJ: Regulation of murine type 1 plasminogen activator inhibitor gene expression in vivo. Tissue specificity and induction by lipopolysaccharide, tumor necrosis factor-alpha, and transforming growth factor-beta. J Clin Invest. 88:1346–1353. 1991. View Article : Google Scholar : PubMed/NCBI | |
|
Fourrier F, Chopin C, Goudemand J, Hendrycx S, Caron C, Rime A, Marey A and Lestavel P: Septic shock, multiple organ failure, and disseminated intravascular coagulation. Compared patterns of antithrombin III, protein C, and protein S deficiencies. Chest. 101:816–823. 1992. View Article : Google Scholar : PubMed/NCBI | |
|
Jose RJ and Manuel A: COVID-19 cytokine storm: The interplay between inflammation and coagulation. Lancet Respir Med. 8:e46–e47. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Hudock KM, Collins MS, Imbrogno M, Snowball J, Kramer EL, Brewington JJ, Gollomp K, McCarthy C, Ostmann AJ, Kopras EJ, et al: Neutrophil extracellular traps activate IL-8 and IL-1 expression in human bronchial epithelia. Am J Physiol Lung Cell Mol Physiol. 319:L137–L147. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Pliyev BK and Menshikov M: Differential effects of the autophagy inhibitors 3-methyladenine and chloroquine on spontaneous and TNF-α-induced neutrophil apoptosis. Apoptosis. 17:1050–1065. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Varga Z, Flammer AJ, Steiger P, Haberecker M, Andermatt R, Zinkernagel AS, Mehra MR, Schuepbach RA, Ruschitzka F and Moch H: Endothelial cell infection and endotheliitis in COVID-19. Lancet. 395:1417–1418. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Leisman DE, Deutschman CS and Legrand M: Facing COVID-19 in the ICU: Vascular dysfunction, thrombosis, and dysregulated inflammation. Intensive Care Med. 46:1105–1108. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Li T, Wang C, Liu Y, Li B, Zhang W, Wang L, Yu M, Zhao X, Du J, Zhang J, et al: Neutrophil extracellular traps induce intestinal damage and thrombotic tendency in inflammatory bowel disease. J Crohns Colitis. 14:240–253. 2020. View Article : Google Scholar | |
|
Zubair AS, McAlpine LS, Gardin T, Farhadian S, Kuruvilla DE and Spudich S: Neuropathogenesis and neurologic manifestations of the coronaviruses in the age of coronavirus disease 2019: A review. JAMA Neurol. 77:1018–1027. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Al Saiegh F, Ghosh R, Leibold A, Avery MB, Schmidt RF, Theofanis T, Mouchtouris N, Philipp L, Peiper SC, Wang ZX, et al: Status of SARS-CoV-2 in cerebrospinal fluid of patients with COVID-19 and stroke. J Neurol Neurosurg Psychiatry. 91:846–848. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Chen N, Zhou M, Dong X, Qu J, Gong F, Han Y, Qiu Y, Wang J, Liu Y, Wei Y, et al: Epidemiological and clinical characteristics of 99 cases of 2019 novel coronavirus pneumonia in Wuhan, China: A descriptive study. Lancet. 395:507–513. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Xu P, Zhou Q and Xu J: Mechanism of thrombocytopenia in COVID-19 patients. Ann Hematol. 99:1205–1208. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Hottz ED, Bozza FA and Bozza PT: Platelets in immune response to virus and immunopathology of viral infections. Front Med (Lausanne). 5:1212018. View Article : Google Scholar | |
|
Zhou P, Li T, Jin J, Liu Y, Li B, Sun Q, Tian J, Zhao H, Liu Z, Ma S, et al: Interactions between neutrophil extracellular traps and activated platelets enhance procoagulant activity in acute stroke patients with ICA occlusion. EBioMedicine. 53:1026712020. View Article : Google Scholar : PubMed/NCBI | |
|
Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, Weinrauch Y and Zychlinsky A: Neutrophil extracellular traps kill bacteria. Science. 303:1532–1535. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Martinod K and Wagner DD: Thrombosis: Tangled up in NETs. Blood. 123:2768–2776. 2014. View Article : Google Scholar : | |
|
Barnes BJ, Adrover JM, Baxter-Stoltzfus A, Borczuk A, Cools-Lartigue J, Crawford JM, Dassler-Plenker J, Guerci P, Huynh C, Knight JS, et al: Targeting potential drivers of COVID-19: Neutrophil extracellular traps. J Exp Med. 217:e202006522020. View Article : Google Scholar : PubMed/NCBI | |
|
Zuo Y, Yalavarthi S, Shi H, Gockman K, Zuo M, Madison JA, Blair C, Weber A, Barnes BJ, Egeblad M, et al: Neutrophil extracellular traps in COVID-19. JCI Insight. 5:e1389992020. | |
|
Hargett LA and Bauer NN: On the origin of microparticles: From 'platelet dust' to mediators of intercellular communication. Pulm Circu. 3:329–340. 2013. View Article : Google Scholar | |
|
Yao Z, Wang L, Wu X, Zhao L, Chi C, Guo L, Tong D, Yang X, Dong Z, Deng R, et al: Enhanced procoagulant activity on blood cells after acute ischemic stroke. Transl Stroke Res. 8:83–91. 2017. View Article : Google Scholar | |
|
Yu M, Xie R, Zhang Y, Liang H, Hou L, Yu C, Zhang J, Dong Z, Tian Y, Bi Y, et al: Phosphatidylserine on microparticles and associated cells contributes to the hypercoagulable state in diabetic kidney disease. Nephrol Dial Transplant. 33:2115–2127. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Vance JE and Steenbergen R: Metabolism and functions of phosphatidylserine. Prog Lipid Res. 44:207–234. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Wang Y, Du F, Hawez A, Mörgelin M and Thorlacius H: Neutrophil extracellular trap-microparticle complexes trigger neutrophil recruitment via high-mobility group protein 1 (HMGB1)-toll-like receptors(TLR2)/TLR4 signalling. Br J Pharmacol. 176:3350–3363. 2019.PubMed/NCBI | |
|
Wang Y, Luo L, Braun OÖ, Westman J, Madhi R, Herwald H, Mörgelin M and Thorlacius H: Neutrophil extracellular trap-microparticle complexes enhance thrombin generation via the intrinsic pathway of coagulation in mice. Sci Rep. 8:40202018. View Article : Google Scholar : PubMed/NCBI | |
|
Nieri D, Neri T, Petrini S, Vagaggini B, Paggiaro P and Celi A: Cell-derived microparticles and the lung. Eur Respir Rev. 25:266–277. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Balvers K, Curry N, Kleinveld DJ, Böing AN, Nieuwland R, Goslings JC and Juffermans NP: Endogenous microparticles drive the proinflammatory host immune response in severely injured trauma patients. Shock. 43:317–321. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Riedl M, Fakhouri F, Le Quintrec M, Noone DG, Jungraithmayr TC, Fremeaux-Bacchi V and Licht C: Spectrum of complement-mediated thrombotic microangiopathies: Pathogenetic insights identifying novel treatment approaches. Semin Thromb Hemost. 40:444–464. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Cugno M, Meroni PL, Gualtierotti R, Griffini S, Grovetti E, Torri A, Panigada M, Aliberti S, Blasi F, Tedesco F and Peyvandi F: Complement activation in patients with COVID-19: A novel therapeutic target. J Allergy Clin Immunol. 146:215–217. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Magro C, Mulvey JJ, Berlin D, Nuovo G, Salvatore S, Harp J, Baxter-Stoltzfus A and Laurence J: Complement associated microvascular injury and thrombosis in the pathogenesis of severe COVID-19 infection: A report of five cases. Transl Res. 220:1–13. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Stites E, Renner B, Laskowski J, Le Quintrec M, You Z, Freed B, Cooper J, Jalal D and Thurman JM: Complement fragments are biomarkers of antibody-mediated endothelial injury. Mol Immunol. 118:142–152. 2020. View Article : Google Scholar | |
|
Heydenreich N, Nolte MW, Göb E, Langhauser F, Hofmeister M, Kraft P, Albert-Weissenberger C, Brede M, Varallyay C, Göbel K, et al: C1-inhibitor protects from brain ischemia-reperfusion injury by combined antiinflammatory and antithrombotic mechanisms. Stroke. 43:2457–2467. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Pugh CW and Ratcliffe PJ: New horizons in hypoxia signaling pathways. Exp Cell Res. 356:116–121. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Cameron SJ, Mix DS, Ture SK, Schmidt RA, Mohan A, Pariser D, Stoner MC, Shah P, Chen L, Zhang H, et al: Hypoxia and ischemia promote a maladaptive platelet phenotype. Arterioscler Thromb Vasc Biol. 38:1594–1606. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Gupta N, Zhao YY and Evans CE: The stimulation of thrombosis by hypoxia. Thromb Res. 181:77–83. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Frangou E, Chrysanthopoulou A, Mitsios A, Kambas K, Arelaki S, Angelidou I, Arampatzioglou A, Gakiopoulou H, Bertsias GK, Verginis P, et al: REDD1/autophagy pathway promotes thromboinflammation and fibrosis in human systemic lupus erythematosus (SLE) through NETs decorated with tissue factor (TF) and inter-leukin-17A (IL-17A). Ann Rheum Dis. 78:238–248. 2019. View Article : Google Scholar | |
|
Zhang Y, Xiao M, Zhang S, Xia P, Cao W, Jiang W, Chen H, Ding X, Zhao H, Zhang H, et al: Coagulopathy and antiphospholipid antibodies in patients with Covid-19. N Engl J Med. 382:e382020. View Article : Google Scholar : PubMed/NCBI | |
|
Müller-Calleja N, Hollerbach A, Ritter S, Pedrosa DG, Strand D, Graf C, Reinhardt C, Strand S, Poncelet P, Griffin JH, et al: Tissue factor pathway inhibitor primes monocytes for antiphospholipid antibody-induced thrombosis. Blood. 134:1119–1131. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Gašperšič N, Zaletel M, Kobal J, Žigon P, Čučnik S, Šemrl SS, Tomšič M and Ambrožič A: Stroke and antiphospholipid syndrome-antiphospholipid antibodies are a risk factor for an ischemic cerebrovascular event. Clin Rheumatol. 38:379–384. 2019. View Article : Google Scholar | |
|
Tang N, Bai H, Chen X, Gong J, Li D and Sun Z: Anticoagulant treatment is associated with decreased mortality in severe coronavirus disease 2019 patients with coagulopathy. J Thromb Haemost. 18:1094–1099. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Oudkerk M, Buller HR and Kuijpers D: Diagnosis, prevention, and treatment of thromboembolic complications in COVID-19: Report of the National Institute for Public Health of the Netherlands. Radiology. 297:E216–E222. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Klok FA, Kruip MJHA, van der Meer NJM, Arbous MS, Gommers DAMPJ, Kant KM, Kaptein FHJ, van Paassen J, Stals MAM, Huisman MV and Endeman H: Incidence of thrombotic complications in critically ill ICU patients with COVID-19. Thromb Res. 191:145–147. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Bikdeli B, Madhavan MV, Jimenez D, Chuich T, Dreyfus I, Driggin E, Nigoghossian C, Ageno W, Madjid M, Guo Y, et al: COVID-19 and thrombotic or thromboembolic disease: Implications for prevention, antithrombotic therapy, and follow-up. J Am Coll Cardiol. 75:2950–2973. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Hermans C and Lambert C: Impact of the COVID-19 pandemic on therapeutic choices in thrombosis-hemostasis. J Thromb Haemost. 18:1794–1795. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Wang J, Hajizadeh N, Moore EE, McIntyre RC, Moore PK, Veress LA, Yaffe MB, Moore HB and Barrett CD: Tissue plasminogen activator (tPA) treatment for COVID-19 associated acute respiratory distress syndrome (ARDS): A case series. J Thromb Haemost. 18:1752–1755. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Quiros Roldan E, Biasiotto G, Magro P and Zanella I: The possible mechanisms of action of 4-aminoquinolines (chloroquine/hydroxychloroquine) against Sars-Cov-2 infection (COVID-19): A role for iron homeostasis? Pharmacol Res. 158:1049042020. View Article : Google Scholar : PubMed/NCBI | |
|
Rodrigues-Diez RR, Tejera-Muñoz A, Marquez-Exposito L, Rayego-Mateos S, Sanchez LS, Marchant V, Santamaria LT, Ramos AM, Ortiz A, Egido J and Ruiz-Ortega M: Statins: Could an old friend help the fight against COVID-19? Br J Pharmacol. 177:4873–4886. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Ascierto PA, Fox BA, Urba WJ, Anderson AC, Atkins MB, Borden EC, Brahmer JR, Butterfield LH, Cesano A, Chen DC, et al: Insights from immuno-oncology: The Society for Immunotherapy of Cancer Statement on access to IL-6-targeting therapies for COVID-19. J Immunother Cancer. 8:e0008782020. View Article : Google Scholar : PubMed/NCBI | |
|
Paniri A and Akhavan-Niaki H: Emerging role of IL-6 and NLRP3 inflammasome as potential therapeutic targets to combat COVID-19: Role of lncRNAs in cytokine storm modulation. Life Sci. 118114:2020. | |
|
Alhenc-Gelas F and Drueke TB: Blockade of SARS-CoV-2 infection by recombinant soluble ACE2. Kidney Int. 97:1091–1093. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Haschke M, Schuster M, Poglitsch M, Loibner H, Salzberg M, Bruggisser M, Penninger J and Krähenbühl S: Pharmacokinetics and pharmacodynamics of recombinant human angiotensin-converting enzyme 2 in healthy human subjects. Clin Pharmacokinet. 52:783–792. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Khan A, Benthin C, Zeno B, Albertson TE, Boyd J, Christie JD, Hall R, Poirier G, Ronco JJ, Tidswell M, et al: A pilot clinical trial of recombinant human angiotensin-converting enzyme 2 in acute respiratory distress syndrome. Crit Care. 21:2342017. View Article : Google Scholar : PubMed/NCBI | |
|
Sardu C, Gambardella J, Morelli MB, Wang X, Marfella R and Santulli G: Hypertension, thrombosis, kidney failure, and diabetes: Is COVID-19 an endothelial disease? A comprehensive evaluation of clinical and basic evidence. J Clin Med. 9:14172020. View Article : Google Scholar : | |
|
Fan E, Brodie D and Slutsky AS: Acute respiratory distress syndrome: Advances in diagnosis and treatment. JAMA. 319:698–710. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Pulavendran S, Rudd JM, Maram P, Thomas PG, Akhilesh R, Malayer JR, Chow VTK and Teluguakula N: Combination therapy targeting platelet activation and virus replication Protects mice against lethal influenza pneumonia. Am J Respir Cell Mol Biol. 61:689–701. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
De Meyer SF, Suidan GL, Fuchs TA, Monestier M and Wagner DD: Extracellular chromatin is an important mediator of ischemic stroke in mice. Arterioscler Thromb Vasc Biol. 32:1884–1891. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Papayannopoulos V, Staab D and Zychlinsky A: Neutrophil elastase enhances sputum solubilization in cystic fibrosis patients receiving DNase therapy. PLoS One. 6:e285262011. View Article : Google Scholar : PubMed/NCBI | |
|
Laridan E, Denorme F, Desender L, François O, Andersson T, Deckmyn H, Vanhoorelbeke K and De Meyer SF: Neutrophil extracellular traps in ischemic stroke thrombi. Ann Neurol. 82:223–232. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Mistry P, Carmona-Rivera C, Ombrello AK, Hoffmann P, Seto NL, Jones A, Stone DL, Naz F, Carlucci P, Dell'Orso S, et al: Dysregulated neutrophil responses and neutrophil extracellular trap formation and degradation in PAPA syndrome. Ann Rheum Dis. 77:1825–1833. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Kim SW, Lee H, Lee HK, Kim ID and Lee JK: Neutrophil extracellular trap induced by HMGB1 exacerbates damages in the ischemic brain. Acta Neuropathol Commun. 7:942019. View Article : Google Scholar : PubMed/NCBI | |
|
Neri T, Scalise V, Passalacqua I, Sanguinetti C, Lombardi S, Pergoli L, Bollati V, Pedrinelli R, Paggiaro P and Celi A: Tiotropium inhibits proinflammatory microparticle generation by human bronchial and endothelial cells. Sci Rep. 9:116312019. View Article : Google Scholar : PubMed/NCBI | |
|
Neri T, Lombardi S, Faìta F, Petrini S, Balìa C, Scalise V, Pedrinelli R, Paggiaro P and Celi A: Pirfenidone inhibits p38-mediated generation of procoagulant microparticles by human alveolar epithelial cells. Pulm Pharmacol Ther. 39:1–6. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Gralinski LE, Sheahan TP, Morrison TE, Menachery VD, Jensen K, Leist SR, Whitmore A, Heise MT and Baric RS: Complement activation contributes to severe acute respiratory syndrome coronavirus pathogenesis. mBio. 9:e01753–18. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Mastellos DC, Ricklin D and Lambris JD: Clinical promise of next-generation complement therapeutics. Nat Rev Drug Discov. 18:707–729. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Hadanny A, Rittblat M, Bitterman M, May-Raz I, Suzin G, Boussi-Gross R, Zemel Y, Bechor Y, Catalogna M and Efrati S: Hyperbaric oxygen therapy improves neurocognitive functions of post-stroke patients-a retrospective analysis. Restor Neurol Neurosci. 38:93–107. 2020. | |
|
Beyls C, Huette P, Abou-Arab O, Berna P and Mahjoub Y: Extracorporeal membrane oxygenation for COVID-19-associated severe acute respiratory distress syndrome and risk of thrombosis. Br J Anaesth. 125:e260–e262. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Fan H, Zhang L, Huang B, Zhu M, Zhou Y, Zhang H, Tao X, Cheng S, Yu W, Zhu L and Chen J: Cardiac injuries in patients with coronavirus disease 2019: Not to be ignored. Inter J Infect Dis. 96:294–297. 2020. View Article : Google Scholar | |
|
Zou Y, Guo H, Zhang Y, Zhang Z, Liu Y, Wang J, Lu H and Qian Z: Analysis of coagulation parameters in patients with COVID-19 in Shanghai, China. Biosci Trends. 14:285–289. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Fogarty H, Townsend L, Ni Cheallaigh C, Bergin C, Martin-Loeches I, Browne P, Bacon CL, Gaule R, Gillett A, Byrne M, et al: COVID19 coagulopathy in Caucasian patients. Br J Haematol. 189:1044–1049. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Huang C, Wang Y, Li X, Ren L, Zhao J, Hu Y, Zhang L, Fan G, Xu J, Gu X, et al: Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet. 395:497–506. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Wu C, Chen X, Cai Y, Xia J, Zhou X, Xu S, Huang H, Zhang L, Zhou X, Du C, et al: Risk factors associated with acute respiratory distress syndrome and death in patients with coronavirus disease 2019 pneumonia in Wuhan, China. JAMA Intern Med. 180:934–943. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Cui S, Chen S, Li X, Liu S and Wang F: Prevalence of venous thromboembolism in patients with severe novel coronavirus pneumonia. J Thromb Haemost. 18:1421–1424. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Stoneham SM, Milne KM, Nuttall E, Frew GH, Sturrock BR, Sivaloganathan H, Ladikou EE, Drage S, Phillips B, Chevassut TJ and Eziefula AC: Thrombotic risk in COVID-19: A case series and case-control study. Clin Med (Lond). 20:e76–e81. 2020. View Article : Google Scholar | |
|
Léonard-Lorant I, Delabranche X, Séverac F, Helms J, Pauzet C, Collange O, Schneider F, Labani A, Bilbault P, Molière S, et al: Acute pulmonary embolism in COVID-19 patients on CT angiography and relationship to D-Dimer levels. Radiology. 296:E189–E191. 2020. View Article : Google Scholar | |
|
Llitjos JF, Leclerc M, Chochois C, Monsallier JM, Ramakers M, Auvray M and Merouani K: High incidence of venous thromboembolic events in anticoagulated severe COVID-19 patients. J Thromb Haemost. 18:1743–1746. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Poillon G, Obadia M, Perrin M, Savatovsky J and Lecler A: Cerebral venous thrombosis associated with COVID-19 infection: Causality or coincidence? J Neuroradiol. S0150-986:30167–X. 2020. | |
|
Paranjpe I, Fuster V, Lala A, Russak AJ, Glicksberg BS, Levin MA, Charney AW, Narula J, Fayad ZA, Bagiella E, et al: Association of treatment dose anticoagulation with in-hospital survival among hospitalized patients with COVID-19. J Am Coll Cardiol. 76:122–124. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
White D, MacDonald S, Bull T, Hayman M, de Monteverde-Robb R, Sapsford D, Lavinio A, Varley J, Johnston A, Besser M and Thomas W: Heparin resistance in COVID-19 patients in the intensive care unit. J Thromb Thrombolysis. 50:287–291. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Arachchillage DJ, Remmington C, Rosenberg A, Xu T, Passariello M, Hall D, Laffan M and Patel BV: Anticoagulation with argatroban in patients with acute antithrombin deficiency in severe COVID-19. Br J Haematol. 190:e286–e288. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Ranucci M, Ballotta A, Di Dedda U, Bayshnikova E, Dei Poli M, Resta M, Falco M, Albano G and Menicanti L: The procoagulant pattern of patients with COVID-19 acute respiratory distress syndrome. J Thromb Haemost. 18:1747–1751. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Thachil J, Tang N, Gando S, Falanga A, Cattaneo M, Levi M, Clark C and Iba T: ISTH interim guidance on recognition and management of coagulopathy in COVID-19. J Thromb Haemost. 18:1023–1026. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Connors JM and Levy JH: COVID-19 and its implications for thrombosis and anticoagulation. Blood. 135:2033–2040. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Thachil J, Tang N, Gando S, Falanga A, Cattaneo M, Levi M, Clark C and Iba T: DOACs and 'newer' haemophilia therapies in COVID-19. J Thromb Haemost. 18:1795–1796. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Bikdeli B, Madhavan MV, Gupta A, Jimenez D, Burton JR, Der Nigoghossian C, Chuich T, Nouri SN, Dreyfus I, Driggin E, et al: Pharmacological agents targeting thromboinflammation in COVID-19: Review and implications for future research. Thromb Haemost. 120:1004–1023. 2020. View Article : Google Scholar : PubMed/NCBI |
