Systemic Inflammatory Response Syndrome Is a Major Contributor to COVID-19–Associated Coagulopathy
2020; Lippincott Williams & Wilkins; Volume: 142; Issue: 6 Linguagem: Inglês
10.1161/circulationaha.120.048925
ISSN1524-4539
AutoresPaul Masi, Guillaume Hékimian, Manon Lejeune, Juliette Chommeloux, Cyrielle Desnos, Marc Pineton de Chambrun, Isabelle Martin‐Toutain, Ania Nieszkowska, Guillaume Lebreton, Nicolas Bréchot, Matthieu Schmidt, Charles Edouard Luyt, Alain Combes, Corinne Frère,
Tópico(s)Long-Term Effects of COVID-19
ResumoHomeCirculationVol. 142, No. 6Systemic Inflammatory Response Syndrome Is a Major Contributor to COVID-19–Associated Coagulopathy Free AccessLetterPDF/EPUBAboutView PDFView EPUBSections ToolsAdd to favoritesDownload citationsTrack citationsPermissions ShareShare onFacebookTwitterLinked InMendeleyReddit Jump toFree AccessLetterPDF/EPUBSystemic Inflammatory Response Syndrome Is a Major Contributor to COVID-19–Associated CoagulopathyInsights From a Prospective, Single-Center Cohort Study Paul Masi, Guillaume Hékimian, Manon Lejeune, Juliette Chommeloux, Cyrielle Desnos, Marc Pineton De Chambrun, Isabelle Martin-Toutain, Ania Nieszkowska, Guillaume Lebreton, Nicolas Bréchot, Matthieu Schmidt, Charles Edouard Luyt, Alain Combes and Corinne Frere Paul MasiPaul Masi , Guillaume HékimianGuillaume Hékimian , Manon LejeuneManon Lejeune , Juliette ChommelouxJuliette Chommeloux , Cyrielle DesnosCyrielle Desnos , Marc Pineton De ChambrunMarc Pineton De Chambrun https://orcid.org/0000-0002-6321-858X , Isabelle Martin-ToutainIsabelle Martin-Toutain , Ania NieszkowskaAnia Nieszkowska , Guillaume LebretonGuillaume Lebreton , Nicolas BréchotNicolas Bréchot , Matthieu SchmidtMatthieu Schmidt , Charles Edouard LuytCharles Edouard Luyt , Alain CombesAlain Combes https://orcid.org/0000-0002-6030-3957 and Corinne FrereCorinne Frere Corinne Frere, MD, PhD, Department of Haematology, Pitié-Salpêtrière Hospital, Assistance Publique Hôpitaux de Paris, 47-83 Boulevard de l'Hôpital, 75013 Paris, France. Email E-mail Address: [email protected] Originally published17 Jun 2020https://doi.org/10.1161/CIRCULATIONAHA.120.048925Circulation. 2020;142:611–614Other version(s) of this articleYou are viewing the most recent version of this article. Previous versions: June 17, 2020: Ahead of Print Coronavirus disease 2019 (COVID-19) is associated with a systemic coagulopathy1 favoring thromboembolic complications, which occur in 15% to 30% of critically ill patients with COVID-19.2,3 This coagulopathy remains poorly documented and data on thrombin generation and fibrinolysis are lacking.We characterized the coagulation and fibrinolysis profiles of patients with COVID-19 with acute respiratory distress syndrome (ARDS).From October 2019 to April 2020, 28 consecutive patients with severe ARDS were referred to our tertiary intensive care unit and included in this prospective single-center cohort study. The protocol was approved by a research ethics committee (CPP Ouest III, 2019-A01160-57), and the study was conducted in accordance with the Declaration of Helsinki. Informed consent was obtained from patients or their relatives. Blood samples were collected on admission for a comprehensive coagulation/fibrinolytic pathways analysis. To better assess the in vivo dynamics of clot formation, stabilization, and lysis, we used a global coagulation assay assessing changes in viscoelastic properties of whole blood.We compared 11 patients with ARDS included before the COVID-19 pandemic (influenzapneumonia, n=4; bacterial pneumonia, n=2; other causes of ARDS, n=5) with 17 patients with COVID-19. Baseline characteristics of the patients with and without COVID-19 did not differ and are presented in the Table. Briefly, the median age was 45 years; most patients were men (68%), overweight (32.1%), or obese (57.1%); and a few of them had additional comorbidities. On admission, all patients were receiving thromboprophylaxis according to current guidelines. Pulmonary embolism was incidentally diagnosed in 3 out of 17 patients with COVID-19. Coagulation and fibrinolysis profiles are presented in the Table.Table. Main Clinical and Biological Characteristics of Patients With and Without COVID-19 With Severe Acute Respiratory Distress Syndrome on AdmissionVariablesNormal RangeOverall Population (n=28)Non–COVID-19 Acute Respiratory Distress Syndrome (n=11)COVID-19 Acute Respiratory Distress Syndrome(n=17)P ValueClinical characteristics Age, y—45 (33–56)34 (28–55)48 (42–58)NS Male—19 (68)7 (64)12 (71)NS Body mass index, kg/m2—30.5 (28–35.75)29.3 (26–35)31.0 (28.8–40.5)NS Obesity—16 (57.1)5 (45.5)11 (64.7)NS Current smoker—2 (7)2 (18)0 (0)NS CCI—1 (0–1.75)1 (0–2)1 (0.5–1.5)NS SOFA score—11 (8–17)9 (7–17)12 (9–17)NS SAPS-II score—52 (42 –69)57 (37–81)52 (43–63)NS ISTH DIC score—4 (14)4 (36)0 (0)0.0161 Pao2/FiO2, mm Hg—59 (47–70)64 (50–77)57 (47–66)NS PaCO2, mm Hg—56 (47–61)56 (48–60)56 (47–62)NS pH—7.32 (7.22–7.38)7.32 (7.20–7.35)7.33 (7.23–7.38)NSBiomarkers of inflammatory response and tissue damage C-reactive protein, mg/L<5272.3 (128.6–364.2)136.2 (92.42–314.7)320.2 (158.7–367.3)0.05 α1-acid glycoprotein, g/L0.5–1.22.272 (1.933–2.731)2.123 (1.914–2.255)2.508 (1.909–3.196)0.0228 Ferritin, ng/mL10–250——2001 (1274–2987)— Lactate dehydrogenase, IU/L140–245531.5 (431.3–828.8)451.0(339.0–574.0)606.0 (444.0–901.0)NSComplete blood count Hemoglobin concentration, g/L120–16096 (83–121)110 (78–125)92 (84–116)NS Leucocyte count (×109/L)4–1014.9 (10.8–19.3)17.2 (9.1–24.3)13.2 (10.6–16.4)NS Neutrophil count (×109/L)2–2.7511.3 (8.8–15.3)15.2 (3.4–22.2)10.8 (8.8–13.8)NS Lymphocyte count (×109/L)1.5–40.85 (0.65–1.22)1.05 (0.62–1.28)0.78 (0.66–1.21)NS Platelet count (×109/L)150–400247 (199–277)231 (160–245)262 (224–334)0.05Standard coagulation parameters aPTT, s30–3943.5 (38.7–66.3)52.7 (34.5–150.7)42.4 (38.8–47.6)NS PT, s11–13.515 (14.03–16.28)16.30 (15.0–17.70)14.90 (13.7–15.3)NS Fibrinogen, mg/dL<400770 (600–905)710 (490–790)810 (640–945)0.0322von Willebrand factor levels, IU/mL von Willebrand factor antigen0.55–1.204.44 (3.38–5.20)3.94 (3.28–4.90)4.48 (3.62–5.29)NS von Willebrand factor activity0.55–1.202.86 (1.73–3.51)2.65 (1.67–3.71)3.13 (1.90–3.47)NSExtrinsic pathway parameter, IU/mL Factor VII0.70–1.200.89 (0.76–1.09)0.60 (0.21–0.74)0.84 (0.75–0.91)0.0363Intrinsic pathway parameters, IU/mL Factor VIII0.60–1.202.49 (1.61–3.55)1.61 (1.48–2.53)2.97 (2.14–3.64)0.0318 Factor IX0.60–1.201.71 (1.21–2.14)1.39 (0.96–2.19)1.74 (1.31–2.13)NS Factor XI0.60–1.201.17 (0.94–1.32)1.08 (0.48–1.24)1.21 (1.00–1.39)NS Factor XII0.60–1.200.73 (0.38–0.93)0.76 (0.25.0–98)0.64 (0.39–0.92)NSCommon pathway parameters, IU/mL Factor II0.70–1.200.89 (0.76–1.04)0.78 (0.71–0.89)0.99 (0.87–1.12)0.0084 Factor V0.70–1.201.15 (0.76–1.60)0.73 (0.42–0.91)1.53 (1.22–1.72)<0.0001 Factor X0.70–1.201.02 (0.85–1.18)0.83 (0.78–0.99)1.15 (1.01–1.19)0.0013Coagulation inhibitors, IU/mL Antithrombin activity0.80–1.200.71 (0.64–0.92)0.70 (0.53–0.73)0.83 (0.66–0.94)NS Protein C activity0.70–1.400.88 (0.73–1.02)0.90 (0.45–1.06)0.86 (0.73–1.02)NS Protein S activity0.55–1.200.52 (0.36–0.70)0.52 (0.36–0.65)0.57 (0.35–0.75)NSMarkers of thrombin generation Prothrombin F1+2, pmol/L69–229715.3 (278.3–1019)809.6 (162.8–1235)500.3 (306.1–796.6)NS Thrombin–antithrombin complexes, µg/L0–4.210.21 (4.81–38.55)22.63 (10.44–104.9)7.69 (3.80–23.92)0.0385Fibrinolysis parameters Factor XIII activity, IU/mL0.70–1.400.72 (0.47–0.89)0.74 (0.60–0.84)0.72 (0.36–0.91)NS Plasminogen activity, IU/mL0.80–1.401.22 (1.03–1.70)1.10 (0.92–1.22)1.36 (1.18–1.85)0.0318 α2-Antiplasmin activity, IU/mL0.80–1.401.35 (1.20–1.44)1.31 (0.77–1.55)1.36 (1.26–1.43)NS tPA antigen, ng/mL1–1236.2 (22.5–53.3)26.3 (9.1–52.6)37.8 (30.8–60.0)0.0482 PAI-1 antigen, ng/mL7–4394.3 (60.1–119.1)69.00 (38.8–126.8)95.20 (74.5–118.7)NSFibrin degradation products D-dimer, mg/L<0.56.51 (3.65–14.38)8.39 (5.33–11.18)4.64 (3.20–20.0)NS Fibrin monomer, µg/mL<56.12 (5.0–40.64)14.93 (5.0–71.58)5.0 (5.0–26.61)NSCoagulation profile assessed by viscoelastic tests* Clot time, s113–164147.0 (134.0–172.8)137 (137–193)152 (130–171)NS Heparinase clot time, s109–150130.0 (114.8–150.8)130 (114–150)130 (117–152)NS Clot time ratio<1.21.1 (1.025–1.3)1.1 (1.0–1.2)1.1 (1.1–1.3)NS Clot stiffness, hPA13.0–33.241.85 (24.83–65.0)24.9 (20.2–42.0)49.9 (38.5–68)0.0077 Platelet contribution to clot stiffness, hPA11.9–29.833.2 (20.13–48.80)20.8 (17.9–33.6)38.50 (28.85–51.2)0.014 Fibrinogen contribution to clot stiffness, hPA1.0–3.78.3 (5.6–16.7)6.1 (4.0–8.2)12.8 (6.35–20.85)0.00051Other procoagulants Lupus anticoagulant (dRVVT, number positive)—14 (50)5 (45)9 (53)NS Antiphospholipid antibodies IgM (number positive)†—15 (54)8 (73)9 (53)NS Antiphospholipid antibodies IgG (number positive)†—13 (46)7(64)6 (35.2)NS Antiplatelet factor 4/heparin antibodies (number positive)—0 (0)0 (0)0 (0)NSCategorical variables are reported as number (frequency) and continuous variables as median (interquartile range). Categorical variables were compared with the Fisher exact test and continuous variables with the nonparametric Mann-Whitney test. Spearman test was used to measure the strength of association between two variables. All statistical tests were 2-tailed, and a P value <0.05 was considered statistically significant. Statistical analysis was performed using GraphPad Prism version 8.4.2 for Windows (GraphPad Software, La Jolla, CA). aPTT indicates activated partial thromboplastin time; CCI, Charlson Comorbidity Index; COVID-19, coronavirus disease 2019; DIC, disseminated intravascular coagulation; dRVVT, dilute Russel's viper venom time; IgG, immunoglobulin G; IgM, immunoglobulin M; ISTH, International Society of Hemostasis and Thrombosis; NS, nonsignificant; PAI-1, plasminogen activator inhibitor-1; PT, prothrombin time; SAPS-II, Simplified Acute Physiology Score; SOFA, Sepsis-Related Organ Failure Assessment; and tPA, tissue plasminogen activator.* Assessed using the Quantra Hemostasis analyzer (Quantra System, HemoSonics LLC, Charlottesville, VA) with the QPlus Cartridge.† PHOSPO–LISA IgG/IgM (Theradiag; Marne-la-Vallée, France); includes antiphosphatidyl serin, antiphosphatidyl ethanolamine, anticardiolipin S, and antib2GP1 antibodies.In addition, von Willebrand factor antigen and activity did not differ between groups and were 3- to 4-fold higher than the upper limit of normal range (median, 4.44 and 2.86 IU/mL, respectively, in the overall population). Compared with patients without COVID-19, patients with COVID-19 exhibited significantly higher levels of procoagulant factors, mainly fibrinogen (median, 810 mg/dL versus 710; P=0.03), factor V (median, 1.53 IU/mL versus 0.73; P<0.0001), factor VIII (median, 2.97 IU/mL versus 1.61; P=0.03), and acute phase reactants including C-reactive protein (P=0.05) and α1-acid glycoprotein (P=0.02). All of these measures were strongly correlated with each other (P<0.05 for all correlations). In contrast, antithrombin, protein C, and protein S levels were within the normal range and did not differ between groups. Prothrombin fragment 1 and 2 levels did not differ between patients with and without COVID-19 and were 2- to 3-fold higher than the upper limit of normal range. Thrombin–antithrombin complex levels were increased in both groups but significantly lower in patients with COVID-19 (median, 7.69 µg/L versus 22.63; P=0.03). Fibrinolysis profiles showed factor XIII, plasminogen, and α2-antiplasmin activities within the normal range in both groups, whereas tissue plasminogen activator and PAI-1 (plasminogen activator inhibitor-1) antigen levels were increased in both groups, with significantly higher tissue plasminogen activator values in patients with COVID-19 (median, 37.8 ng/mL versus 26.3; P=0.048). Tissue plasminogen activator and PAI-1 levels were closely correlated (r=0.65, P<0.001), and both measures correlated with lactate dehydrogenase levels (P=0.006 and P=0.03, respectively). Fibrin degradation products, including D-dimer and fibrin monomers, were similarly increased in both groups. None of the patients with COVID-19 presented disseminated intravascular coagulation. Compared with patients without COVID-19, patients with COVID-19 exhibited twice higher values of clot strength (median, 49.9 versus 24.9 hPa; P=0.0077), platelet contribution to clot strength (median, 38.5 versus 20.8 hPa; P=0.014), and fibrinogen contribution to clot strength (median, 12.8 versus 6.1 hPa; P<0.001). Clot strength was strongly correlated with fibrinogen (r=0.425, P=0.02), factor V (r=0.385, P=0.043), and factor VIII (r=0.497, P<0.001), but not with PAI-1 levels (r=−0.102; P=0.606). Antiphospholipid antibodies and lupus anticoagulant were found positive in almost half of patients, without difference between groups.We observed that unlike non–COVID-19 ARDS, COVID-19 ARDS was associated with a significant increase in procoagulants, which closely correlates with the elevation of acute phase reactants. This led to a pronounced imbalance between procoagulants and anticoagulants and uncontrolled thrombin generation. Endothelial dysfunction, reflected by von Willebrand factor release, and hypoxia-mediated hypercoagulability also participate in the procoagulant state1,4 but are nonspecific because they were observed in all patients with ARDS. In patients with COVID-19, tissue plasminogen activator and PAI-1 correlated with lactate dehydrogenase, suggesting a potential role of pulmonary endothelial cell dysfunction in the local regulation of coagulation/fibrinolysis balance and in situ pulmonary thrombosis. We did not observe any fibrinolysis shutdown. A role for antiphospholipid antibodies in COVID-19–associated coagulopathy has been suggested, but we observed a high frequency of antiphospholipid antibodies in all patients with ARDS.We acknowledge that this study has several limitations, including its small sample size, its single-center design, the use of a single time point for biomarkers evaluation, and comparison between two groups of patients with ARDS who may have different clinical courses. Therefore, our results cannot be generalized to all patients with COVID-19.In conclusion, our findings suggest that the systemic inflammatory response is a major contributor to COVID-19–associated coagulopathy, supporting the concept of thromboinflammation.5AcknowledgmentsThe authors thank Inés Colmegna (McGill University) for support and help in interpreting the data and Isabelle Lefèvre, Catherine Pedrosa, Audrey Carlo, and François Depasse (Stago BioCare) for providing the QPlus cartridges.DisclosuresNone.Footnoteshttps://www.ahajournals.org/journal/circCorinne Frere, MD, PhD, Department of Haematology, Pitié-Salpêtrière Hospital, Assistance Publique Hôpitaux de Paris, 47-83 Boulevard de l'Hôpital, 75013 Paris, France. Email corinne.frere@aphp.frReferences1. Connors JM, Levy JH. COVID-19 and its implications for thrombosis and anticoagulation.Blood. 2020; 135:2033–2040. doi: 10.1182/blood.2020006000CrossrefMedlineGoogle Scholar2. 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; 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.Intens Care Med. 2020; 46:1089–1098. doi: 10.1007/s00134-020-06062-xCrossrefMedlineGoogle Scholar3. Poissy J, Goutay J, Caplan M, Parmentier E, Duburcq T, Lassalle F, Jeanpierre E, Rauch A, Labreuche J, Susen S, Lille ICU Haemostasis COVID-19 Group. Pulmonary embolism in patients with COVID-19: awareness of an increased prevalence.Circulation. 2020; 142:184–186. doi: 10.1161/CIRCULATIONAHA.120.047430LinkGoogle Scholar4. Joly BS, Siguret V, Veyradier A. Understanding pathophysiology of hemostasis disorders in critically ill patients with COVID-19 [published online May 15, 2020].Intens Care Med. doi: 10.1007/s00134-020-06088-1. https://link.springer.com/article/10.1007/s00134-020-06088-1CrossrefGoogle Scholar5. Jackson SP, Darbousset R, Schoenwaelder SM. Thromboinflammation: challenges of therapeutically targeting coagulation and other host defense mechanisms.Blood. 2019; 133:906–918. doi: 10.1182/blood-2018-11-882993CrossrefMedlineGoogle Scholar eLetters(0)eLetters should relate to an article recently published in the journal and are not a forum for providing unpublished data. Comments are reviewed for appropriate use of tone and language. Comments are not peer-reviewed. Acceptable comments are posted to the journal website only. Comments are not published in an issue and are not indexed in PubMed. Comments should be no longer than 500 words and will only be posted online. References are limited to 10. 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