دورية أكاديمية

Persistent hypofibrinolysis in severe COVID-19 associated with elevated fibrinolysis inhibitors activity.

التفاصيل البيبلوغرافية
العنوان: Persistent hypofibrinolysis in severe COVID-19 associated with elevated fibrinolysis inhibitors activity.
المؤلفون: Okazaki E; University of Sao Paulo Medical School, Sao Paulo, Brazil.; Hospital das Clínicas da Faculdade de Medicina de Sao Paulo da USP, 255 - Cerqueira César, Sao Paulo, SP, 05403-000, Brazil., Barion BG; University of Sao Paulo Medical School, Sao Paulo, Brazil.; Hospital das Clínicas da Faculdade de Medicina de Sao Paulo da USP, 255 - Cerqueira César, Sao Paulo, SP, 05403-000, Brazil., da Rocha TRF; Hospital das Clínicas da Faculdade de Medicina de Sao Paulo da USP, 255 - Cerqueira César, Sao Paulo, SP, 05403-000, Brazil., Di Giacomo G; Hospital das Clínicas da Faculdade de Medicina de Sao Paulo da USP, 255 - Cerqueira César, Sao Paulo, SP, 05403-000, Brazil., Ho YL; Hospital das Clínicas da Faculdade de Medicina de Sao Paulo da USP, 255 - Cerqueira César, Sao Paulo, SP, 05403-000, Brazil., Rothschild C; Hospital das Clínicas da Faculdade de Medicina de Sao Paulo da USP, 255 - Cerqueira César, Sao Paulo, SP, 05403-000, Brazil., Fatobene G; University of Sao Paulo Medical School, Sao Paulo, Brazil., de Carvalho Moraes BDG; University of Sao Paulo Medical School, Sao Paulo, Brazil., Stefanello B; Hospital das Clínicas da Faculdade de Medicina de Sao Paulo da USP, 255 - Cerqueira César, Sao Paulo, SP, 05403-000, Brazil., Villaça PR; Hospital das Clínicas da Faculdade de Medicina de Sao Paulo da USP, 255 - Cerqueira César, Sao Paulo, SP, 05403-000, Brazil., Rocha VG; Hospital das Clínicas da Faculdade de Medicina de Sao Paulo da USP, 255 - Cerqueira César, Sao Paulo, SP, 05403-000, Brazil., Orsi FA; Hospital das Clínicas da Faculdade de Medicina de Sao Paulo da USP, 255 - Cerqueira César, Sao Paulo, SP, 05403-000, Brazil. ferorsi@unicamp.br.; Department of Pathology, School of Medical Sciences, University of Campinas (UNICAMP), Campinas, Brazil. ferorsi@unicamp.br.
المصدر: Journal of thrombosis and thrombolysis [J Thromb Thrombolysis] 2024 Apr; Vol. 57 (4), pp. 721-729. Date of Electronic Publication: 2024 Mar 25.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Kluwer Academic Publishers Country of Publication: Netherlands NLM ID: 9502018 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1573-742X (Electronic) Linking ISSN: 09295305 NLM ISO Abbreviation: J Thromb Thrombolysis Subsets: MEDLINE
أسماء مطبوعة: Original Publication: [Dordrecht ; Norwell, MA] : Kluwer Academic Publishers, c1994-
مواضيع طبية MeSH: COVID-19* , Antifibrinolytic Agents* , Thrombophilia*, Humans ; Fibrinolysis ; Plasminogen Activator Inhibitor 1/pharmacology ; Post-Acute COVID-19 Syndrome
مستخلص: Hypercoagulability and reduced fibrinolysis are well-established complications associated with COVID-19. However, the timelines for the onset and resolution of these complications remain unclear. The aim of this study was to evaluate, in a cohort of COVID-19 patients, changes in coagulation and fibrinolytic activity through ROTEM assay at different time points during the initial 30 days following the onset of symptoms in both mild and severe cases. Blood samples were collected at five intervals after symptoms onset: 6-10 days, 11-15 days, 16-20 days, 21-25 days, and 26-30 days. In addition, fibrinogen, plasminogen, PAI-1, and alpha 2-antiplasmin activities were determined. Out of 85 participants, 71% had mild COVID-19. Twenty uninfected individuals were evaluated as controls. ROTEM parameters showed a hypercoagulable state among mild COVID-19 patients beginning in the second week of symptoms onset, with a trend towards reversal after the third week of symptoms. In severe COVID-19 cases, hypercoagulability was observed since the first few days of symptoms, with a tendency towards reversal after the fourth week of symptoms onset. A hypofibrinolytic state was identified in severe COVID-19 patients from early stages and persisted even after 30 days of symptoms. Elevated activity of PAI-1 and alpha 2-antiplasmin was also detected in severe COVID-19 patients. In conclusion, both mild and severe cases of COVID-19 exhibited transient hypercoagulability, reverted by the end of the first month. However, severe COVID-19 cases sustain hypofibrinolysis throughout the course of the disease, which is associated with elevated activity of fibrinolysis inhibitors. Persistent hypofibrinolysis could contribute to long COVID-19 manifestations.
(© 2024. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.)
References: Soriano JB, Murthy S, Marshall JC, Relan P, Diaz JV (2022) A clinical case definition of post-COVID-19 condition by a Delphi consensus. Lancet Infect Dis 22(4):e102–e107. https://doi.org/10.1016/S1473-3099(21)00703-9. (PMID: 10.1016/S1473-3099(21)00703-934951953)
Plášek J et al (2022) COVID-19 associated coagulopathy: mechanisms and host-directed treatment. Am J Med Sci 363(6):465–475. https://doi.org/10.1016/j.amjms.2021.10.012. (PMID: 10.1016/j.amjms.2021.10.01234752741)
Conway EM et al (2022) Understanding COVID-19-associated coagulopathy. Nat Rev Immunol 22(10):639–649. https://doi.org/10.1038/s41577-022-00762-9. (PMID: 10.1038/s41577-022-00762-9359318189362465)
de Andrade Orsi FL, Campos Guerra JC (2020) Hipercoagulabilidade, eventos tromboembólicos e anticoagulação na COVID-19. Rev da Soc Cardiol do Estado São Paulo 30(4):462–471. https://doi.org/10.29381/0103-8559/20203004462-71. (PMID: 10.29381/0103-8559/20203004462-71)
Zahran AM, El-Badawy O, Ali WA, Mahran ZG, Mahran EEMO, Rayan A (2021) Circulating microparticles and activated platelets as novel prognostic biomarkers in COVID-19; relation to cancer. PLoS ONE 16(2):e0246806. https://doi.org/10.1371/journal.pone.0246806. (PMID: 10.1371/journal.pone.0246806336175307899358)
Whiting D, DiNardo JA (2014) TEG and ROTEM: technology and clinical applications. Am J Hematol 89(2):228–232. https://doi.org/10.1002/ajh.23599. (PMID: 10.1002/ajh.2359924123050)
Görlinger K et al (2021) The role of rotational thromboelastometry during the COVID-19 pandemic: a narrative review. Korean J Anesthesiol 74(2):91–102. https://doi.org/10.4097/kja.21006. (PMID: 10.4097/kja.21006334401148024216)
Gönenli MG, Komesli Z, İncir S, Yalçın Ö, Akay OM (2021) Rotational thromboelastometry reveals distinct coagulation profiles for patients with covid-19 depending on disease severity. Clin Appl Thromb 27:107602962110276. https://doi.org/10.1177/10760296211027653. (PMID: 10.1177/10760296211027653)
Mazzeffi MA, Chow JH, Tanaka K (2021) COVID-19 associated hypercoagulability: manifestations, mechanisms, and management. Shock 55(4):465–471. https://doi.org/10.1097/SHK.0000000000001660. (PMID: 10.1097/SHK.000000000000166032890309)
Wada H, Shiraki K, Shimpo H, Shimaoka M, Iba T, Suzuki-Inoue K (2023) Thrombotic mechanism involving platelet activation, hypercoagulability and hypofibrinolysis in coronavirus disease 2019. Int J Mol Sci 24(9):7975. https://doi.org/10.3390/ijms24097975. (PMID: 10.3390/ijms240979753717568010178520)
Hulshof A-M et al (2021) Serial EXTEM, FIBTEM, and tPA rotational thromboelastometry observations in the maastricht intensive care COVID cohort—persistence of hypercoagulability and hypofibrinolysis despite anticoagulation. Front. Cardiovasc Med 8:654174. https://doi.org/10.3389/fcvm.2021.654174. (PMID: 10.3389/fcvm.2021.654174339817368107372)
van Blydenstein SA et al (2021) Prevalence and trajectory of COVID-19-associated hypercoagulability using serial thromboelastography in a south african population. Crit Care Res Pract 2021:1–9. https://doi.org/10.1155/2021/3935098. (PMID: 10.1155/2021/3935098)
Toomer KH et al (2023) SARS-CoV-2 infection results in upregulation of plasminogen activator inhibitor-1 and neuroserpin in the lungs, and an increase in fibrinolysis inhibitors associated with disease severity. ejHaem 4(2):324–338. https://doi.org/10.1002/jha2.654. (PMID: 10.1002/jha2.6543720629010188457)
Polok K et al (2023) The temporal changes of hemostatic activity in hospitalized patients with COVID-19: a prospective observational study. Polish Arch Intern Med. https://doi.org/10.20452/pamw.16446. (PMID: 10.20452/pamw.16446)
Yoon U (2023) Native whole blood (TRUE-NATEM) and recalcified citrated blood (NATEM) reference value validation with ROTEM delta. Semin Cardiothorac Vasc Anesth 27(3):108925322311515. https://doi.org/10.1177/10892532231151528. (PMID: 10.1177/10892532231151528)
Meesters MI, Koch A, Kuiper G, Zacharowski K, Boer C (2015) Instability of the non-activated rotational thromboelastometry assay (NATEM) in citrate stored blood. Thromb Res 136(2):481–483. https://doi.org/10.1016/j.thromres.2015.05.026. (PMID: 10.1016/j.thromres.2015.05.02626044665)
Schöchl H, Solomon C, Laux V, Heitmeier S, Bahrami S, Redl H (2012) Similarities in thromboelastometric (ROTEM®) findings between humans and baboons. Thromb Res 130(3):e107–e112. https://doi.org/10.1016/j.thromres.2012.03. (PMID: 10.1016/j.thromres.2012.03.22482831)
Ahmadzia HK et al (2021) Optimal use of intravenous tranexamic acid for hemorrhage prevention in pregnant women. Am J Obstet Gynecol 225(1):85.e1-85.e11. https://doi.org/10.1016/j.ajog.2020.11.035. (PMID: 10.1016/j.ajog.2020.11.03533248975)
Duca S-T, Costache A-D, Miftode R-Ș, Mitu O, Petriș A-O, Costache I-I (2022) Hypercoagulability in COVID-19: from an unknown beginning to future therapies. Med Pharm Rep 95(3):236–242. https://doi.org/10.15386/mpr-2195. (PMID: 10.15386/mpr-2195360604999387574)
Panigada M et al (2020) Hypercoagulability of COVID-19 patients in intensive care unit: a report of thromboelastography findings and other parameters of hemostasis. J Thromb Haemost 18(7):1738–1742. https://doi.org/10.1111/jth.14850. (PMID: 10.1111/jth.14850323024389906150)
Tang N, Li D, Wang X, Sun Z (2020) Abnormal coagulation parameters are associated with poor prognosis in patients with novel coronavirus pneumonia. J Thromb Haemost 18(4):844–847. https://doi.org/10.1111/jth.14768. (PMID: 10.1111/jth.14768320732137166509)
Guan W et al (2020) Clinical characteristics of coronavirus disease 2019 in China. N Engl J Med 382(18):1708–1720. https://doi.org/10.1056/NEJMoa2002032. (PMID: 10.1056/NEJMoa200203232109013)
Huang C et al (2020) Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet 395(10223):497–506. https://doi.org/10.1016/S0140-6736(20)30183-5. (PMID: 10.1016/S0140-6736(20)30183-5319862647159299)
Ali N (2020) Elevated level of C-reactive protein may be an early marker to predict risk for severity of COVID-19. J Med Virol 92(11):2409–2411. https://doi.org/10.1002/jmv.26097. (PMID: 10.1002/jmv.26097325168457301027)
Agrati C et al (2021) Elevated P-selectin in severe Covid-19: considerations for therapeutic options. Mediterr J Hematol Infect Dis 13(1):e2021016. https://doi.org/10.4084/mjhid.2021.016. (PMID: 10.4084/mjhid.2021.016337473977938922)
Aggarwal M, Dass J, Mahapatra M (2020) Hemostatic abnormalities in COVID-19: an update. Indian J Hematol Blood Transfus 36(4):616–626. https://doi.org/10.1007/s12288-020-01328-2. (PMID: 10.1007/s12288-020-01328-2328370537418883)
Corrêa TD et al (2020) Coagulation profile of COVID-19 patients admitted to the ICU: an exploratory study. PLoS ONE 15(12):e0243604. https://doi.org/10.1371/journal.pone.0243604. (PMID: 10.1371/journal.pone.0243604333208747737963)
Calvet L et al (2022) Hypercoagulability in critically ill patients with COVID 19, an observational prospective study. PLoS ONE 17(11):e0277544. https://doi.org/10.1371/journal.pone.0277544. (PMID: 10.1371/journal.pone.0277544364174769683576)
Ibañez C et al (2021) High D dimers and low global fibrinolysis coexist in COVID19 patients: what is going on in there? J Thromb Thrombolysis 51(2):308–312. https://doi.org/10.1007/s11239-020-02226-0. (PMID: 10.1007/s11239-020-02226-032671609)
Mitrovic M et al (2021) Rotational thromboelastometry (ROTEM) profiling of COVID-19 patients. Platelets 32(5):690–696. https://doi.org/10.1080/09537104.2021.1881949. (PMID: 10.1080/09537104.2021.188194933561381)
van Veenendaal N, Scheeren TWL, Meijer K, van der Voort PHJ (2020) Rotational thromboelastometry to assess hypercoagulability in COVID-19 patients. Thromb Res 196:379–381. https://doi.org/10.1016/j.thromres.2020.08.046. (PMID: 10.1016/j.thromres.2020.08.046329806217462575)
Boss K, Kribben A, Tyczynski B (2021) Pathological findings in rotation thromboelastometry associated with thromboembolic events in COVID-19 patients. Thromb J 19(1):10. https://doi.org/10.1186/s12959-021-00263-0. (PMID: 10.1186/s12959-021-00263-0335736707877314)
Kruse JM et al (2020) Thromboembolic complications in critically ill COVID-19 patients are associated with impaired fibrinolysis. Crit Care 24(1):676. https://doi.org/10.1186/s13054-020-03401-8. (PMID: 10.1186/s13054-020-03401-8332878777719734)
Elaa A et al (2022) Assessment of coagulation profiles by rotational thromboelastometry in COVID 19 patients. Clin Lab 68(8):2022. https://doi.org/10.7754/Clin.Lab.2021.211026. (PMID: 10.7754/Clin.Lab.2021.211026)
Gando S, Levi M, Toh C-H (2016) Disseminated intravascular coagulation. Nat Rev Dis Prim 2(1):16037. https://doi.org/10.1038/nrdp.2016.37. (PMID: 10.1038/nrdp.2016.3727250996)
Iba T, Levy JH (2020) Sepsis-induced coagulopathy and disseminated intravascular coagulation. Anesthesiology 132(5):1238–1245. https://doi.org/10.1097/ALN.0000000000003122. (PMID: 10.1097/ALN.000000000000312232044801)
Iba T, Levy JH, Thachil J, Wada H, Levi M (2019) The progression from coagulopathy to disseminated intravascular coagulation in representative underlying diseases. Thromb Res 179:11–14. https://doi.org/10.1016/j.thromres.2019.04.030. (PMID: 10.1016/j.thromres.2019.04.03031059996)
Tsantes AG et al (2023) Sepsis-induced coagulopathy: an update on pathophysiology, biomarkers, and current guidelines. Life 13(2):350. https://doi.org/10.3390/life13020350. (PMID: 10.3390/life13020350368367069961497)
Sungurlu S, Kuppy J, Balk RA (2020) Role of antithrombin III and tissue factor pathway in the pathogenesis of sepsis. Crit Care Clin 36(2):255–265. https://doi.org/10.1016/j.ccc.2019.12.002. (PMID: 10.1016/j.ccc.2019.12.00232172812)
Levi M, van der Poll T (2017) Coagulation and sepsis. Thromb Res 149:38–44. https://doi.org/10.1016/j.thromres.2016.11.007. (PMID: 10.1016/j.thromres.2016.11.00727886531)
Degen JL, Bugge TH, Goguen JD (2007) Fibrin and fibrinolysis in infection and host defense. J Thromb Haemost 5:24–31. https://doi.org/10.1111/j.1538-7836.2007.02519.x. (PMID: 10.1111/j.1538-7836.2007.02519.x17635705)
Creel-Bulos C et al (2021) Fibrinolysis shutdown and thrombosis in a COVID-19 ICU. Shock 55(3):316–320. https://doi.org/10.1097/SHK.0000000000001635. (PMID: 10.1097/SHK.0000000000001635327698228858425)
Wright FL et al (2020) Fibrinolysis shutdown correlation with thromboembolic events in severe COVID-19 infection. J Am Coll Surg 231(2):193-203e1. https://doi.org/10.1016/j.jamcollsurg.2020.05.007. (PMID: 10.1016/j.jamcollsurg.2020.05.007324223497227511)
Venkatesan P (2021) NICE guideline on long COVID. Lancet Respir Med 9(2):129. https://doi.org/10.1016/S2213-2600(21)00031-X. (PMID: 10.1016/S2213-2600(21)00031-X334531627832375)
Ambaglio C et al (2022) Role of hemostatic biomarkers for the identification of patients with LONG-COVID19 syndrome: results from the ‘Accordi’ study. Blood 140(Supplement 1):2652–2653. https://doi.org/10.1182/blood-2022-162206. (PMID: 10.1182/blood-2022-162206)
Pretorius E et al (2021) Persistent clotting protein pathology in long COVID/post-acute sequelae of COVID-19 (PASC) is accompanied by increased levels of antiplasmin. Cardiovasc Diabetol 20(1):172. https://doi.org/10.1186/s12933-021-01359-7. (PMID: 10.1186/s12933-021-01359-7344258438381139)
Baycan OF (2022) Plasminogen activator inhibitor-1 levels as an indicator of severity and mortality for COVID-19. North Clin Istanbul. https://doi.org/10.14744/nci.2022.09076. (PMID: 10.14744/nci.2022.09076)
Nougier C et al (2020) Hypofibrinolytic state and high thrombin generation may play a major role in SARS-COV2 associated thrombosis. J Thromb Haemost 18(9):2215–2219. https://doi.org/10.1111/jth.15016. (PMID: 10.1111/jth.15016326680587405476)
Whyte CS et al (2022) The suboptimal fibrinolytic response in COVID-19 is dictated by high PAI-1. J Thromb Haemost 20(10):2394–2406. https://doi.org/10.1111/jth.15806. (PMID: 10.1111/jth.1580635780481)
Kang S et al (2020) IL-6 trans-signaling induces plasminogen activator inhibitor-1 from vascular endothelial cells in cytokine release syndrome. Proc Natl Acad Sci 117(36):22351–22356. https://doi.org/10.1073/pnas.2010229117. (PMID: 10.1073/pnas.2010229117328263317486751)
Zuo Y et al (2021) Plasma tissue plasminogen activator and plasminogen activator inhibitor-1 in hospitalized COVID-19 patients. Sci Rep 11(1):1580. https://doi.org/10.1038/s41598-020-80010-z. (PMID: 10.1038/s41598-020-80010-z334522987810990)
Henry BM, Benoit SW, Hoehn J, Lippi G, Favaloro EJ, Benoit JL (2020) Circulating plasminogen concentration at admission in patients with coronavirus disease 2019 (COVID-19). Semin Thromb Hemost 46(07):859–862. https://doi.org/10.1055/s-0040-1715454. (PMID: 10.1055/s-0040-1715454328827187645831)
Gando S, Kameue T, Nanzaki S, Nakanishi Y (1996) Disseminated intravascular coagulation is a frequent complication of systemic inflammatory response syndrome. Thromb Haemost 75(02):224–228. https://doi.org/10.1055/s-0038-1650248. (PMID: 10.1055/s-0038-16502488815564)
Zeerleder S, Schroeder V, Hack CE, Kohler HP, Wuillemin WA (2006) TAFI and PAI-1 levels in human sepsis. Thromb Res 118(2):205–212. https://doi.org/10.1016/j.thromres.2005.06.007. (PMID: 10.1016/j.thromres.2005.06.00716009400)
معلومات مُعتمدة: 88887.679326/2023-00 Coordenação de Aperfeiçoamento de Pessoal de Nível Superior; 038018/2021 Ministério da Saúde
فهرسة مساهمة: Keywords: COVID-19; Hypercoagulability; Hypofibrinolysis; Rotational thromboelastometry; SARS-CoV-2
المشرفين على المادة: 0 (Plasminogen Activator Inhibitor 1)
0 (Antifibrinolytic Agents)
تواريخ الأحداث: Date Created: 20240325 Date Completed: 20240419 Latest Revision: 20240419
رمز التحديث: 20240419
DOI: 10.1007/s11239-024-02961-8
PMID: 38523179
قاعدة البيانات: MEDLINE
الوصف
تدمد:1573-742X
DOI:10.1007/s11239-024-02961-8