Thrombosis risk associated with COVID-19 infection. A scoping review

Fatimah Al-Ani, Samer Chehade, Alejandro Lazo-Langner, Fatimah Al-Ani, Samer Chehade, Alejandro Lazo-Langner

Abstract

Background: Infection by the 2019 novel coronavirus (COVID-19) has been reportedly associated with a high risk of thrombotic complications. So far information is scarce and rapidly emerging.

Methods: We conducted a scoping review using a single engine search for studies assessing thrombosis and coagulopathy in COVID-19 patients. Additional studies were identified by secondary review and alert services.

Results: Studies reported the occurrence of venous thromboembolism and stroke in approximately 20% and 3% of patients, respectively. A higher frequency seems to be present in severely ill patients, in particular those admitted to intensive care units. The thrombotic risk is elevated despite the use of anticoagulant prophylaxis but optimal doses of anticoagulation are not yet defined. Although an increase of biomarkers such as D-dimer has been consistently reported in severely ill COVID-19, the optimal cut-off level and prognostic value are not known.

Discussion: A number of pressing issues were identified by this review, including defining the true incidence of VTE in COVID patients, developing algorithms to identify those susceptible to develop thrombotic complications and severe disease, determining the role of biomarkers and/or scoring systems to stratify patients' risk, designing adequate and feasible diagnostic protocols for PE, establishing the optimal thromboprophylaxis strategy, and developing uniform diagnostic and reporting criteria.

Keywords: Anticoagulation; COVID-19; Venous thromboembolism.

Conflict of interest statement

Declaration of competing interest Authors declare no conflicts.

Copyright © 2020 Elsevier Ltd. All rights reserved.

References

    1. Coronavirus Disease (COVID-19). Situation Report - 118. World Health Organization; 2020.
    1. Richardson S., Hirsch J.S., Narasimhan M. Presenting characteristics, comorbidities, and outcomes among 5700 patients hospitalized with COVID-19 in the New York City area. JAMA. 2020;323(20):2052–2059.
    1. Lippi G., Favaloro E.J. D-dimer is associated with severity of coronavirus disease 2019: a pooled analysis. Thromb. Haemost. 2020;120(5):876–878.
    1. Thachil J., Tang N., Gando S. ISTH interim guidance on recognition and management of coagulopathy in COVID-19. J. Thromb. Haemost. 2020;18:1023–1026.
    1. Bikdeli B., Madhavan M.V., Jimenez D. COVID-19 and thrombotic or thromboembolic disease: implications for prevention, antithrombotic therapy, and follow-up. J. Am. Coll. Cardiol. 2020;27284
    1. 2020. Practical guidance for the prevention of thrombosis and management of coagulopathy and disseminated intravascular coagulation of patients infected with COVID-19. Thrombosis UK. Accessed on May 11, 2020.
    1. Zhang Y., Cao W., Xiao M. Clinical and coagulation characteristics of 7 patients with critical COVID-2019 pneumonia and acro-ischemia. Zhonghua xue ye xue za zhi = Zhonghua xueyexue zazhi. 2020;41
    1. Guan W.J., Ni Z.Y., Hu Y. Clinical characteristics of coronavirus disease 2019 in China. N. Engl. J. Med. 2020;382:1708–1720.
    1. 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;18:844–847.
    1. Wang D., Hu B., Hu C. Clinical characteristics of 138 hospitalized patients with 2019 novel coronavirus-infected pneumonia in Wuhan, China. JAMA. 2020;323(11):1061–1069.
    1. Huang C., Wang Y., Li X. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet (Lond. Engl.) 2020;395:497–506.
    1. Ranucci M., Ballotta A., Di Dedda U. The procoagulant pattern of patients with COVID-19 acute respiratory distress syndrome. J. Thromb. Haemost. 2020 doi: 10.1111/jth.14854.
    1. Liang W., Liang H., Ou L. Development and validation of a clinical risk score to predict the occurrence of critical illness in hospitalized patients with COVID-19. JAMA Intern. Med. 2020 doi: 10.1001/jamainternmed.2020.2033.
    1. Zhou F., Yu T., Du R. Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study. Lancet (Lond. Engl.) 2020;395:1054–1062.
    1. Gao Y., Li T., Han M. Diagnostic utility of clinical laboratory data determinations for patients with the severe COVID-19. J. Med. Virol. 2020 doi: 10.1002/jmv.25770.
    1. Li X., Wang L., Yan S. Clinical characteristics of 25 death cases with COVID-19: A retrospective review of medical records in a single medical center, Wuhan, China. Int. J. Infect. Dis. IJID: Off. Publ. Int. Soc. Infect. Dis. 2020;94:128–132.
    1. Fogarty H., Townsend L., Ni Cheallaigh C. COVID-19 coagulopathy in Caucasian patients. Br. J. Haematol. 2020 doi: 10.1111/bjh.16749.
    1. Yang X., Yang Q., Wang Y. Thrombocytopenia and its association with mortality in patients with COVID-19. J. Thromb. Haemost. 2020 doi: 10.1111/jth.14848.
    1. Zhang Y., Xiao M., Zhang S. Coagulopathy and antiphospholipid antibodies in patients with Covid-19. N. Engl. J. Med. 2020;382
    1. Harzallah I., Debliquis A., Drenou B. Lupus anticoagulant is frequent in patients with Covid-19. J. Thromb. Haemost. 2020 doi: 10.1111/jth.14867.
    1. Devreese K.M.J., Ortel T.L., Pengo V., de Laat B. Laboratory criteria for antiphospholipid syndrome: communication from the SSC of the ISTH. J. Thromb. Haemost. 2018;16:809–813.
    1. Taylor F.B., Jr., Toh C.H., Hoots W.K., Wada H., Levi M. Towards definition, clinical and laboratory criteria, and a scoring system for disseminated intravascular coagulation. Thromb. Haemost. 2001;86:1327–1330.
    1. Ai T., Yang Z., Hou H. Correlation of chest CT and RT-PCR testing in coronavirus disease 2019 (COVID-19) in China: a report of 1014 cases. Radiology. 2020;200642
    1. Deng Y., Liu W., Liu K. Clinical characteristics of fatal and recovered cases of coronavirus disease 2019 (COVID-19) in Wuhan, China: a retrospective study. Chin. Med. J. 2020 doi: 10.1097/cm9.0000000000000824.
    1. Lodigiani C., Iapichino G., Carenzo L. Venous and arterial thromboembolic complications in COVID-19 patients admitted to an academic hospital in Milan, Italy. Thromb. Res. 2020;191:9–14.
    1. Luo W., Yu H., Gou J. 2020020407. Preprints; 2020. Clinical Pathology of Critical Patient with Novel Coronavirus Pneumonia (COVID-19)
    1. Fox S.E., Akmatbekov A., Harbert J.L., Li G., Brown J.Q., Vander Heide R.S. medRxiv; 2020. Pulmonary and Cardiac Pathology in Covid-19: The First Autopsy Series From New Orleans. (2020.04.06.20050575)
    1. Danzi G.B., Loffi M., Galeazzi G., Gherbesi E. Acute pulmonary embolism and COVID-19 pneumonia: a random association? Eur. Heart J. 2020;41(19):1858.
    1. Wichmann D., Sperhake J.P., Lutgehetmann M. Autopsy findings and venous thromboembolism in patients with COVID-19: a prospective cohort study. Ann. Intern. Med. 2020 doi: 10.7326/m20-2003.
    1. Liu Q., Wang R.S., Qu G.Q. Gross examination report of a COVID-19 death autopsy. Fa yi xue za zhi. 2020;36:21–23.
    1. Zhang T., Sun L.X., Feng R.E. Comparison of clinical and pathological features between severe acute respiratory syndrome and coronavirus disease 2019. Zhonghua jie he he hu xi za zhi = Zhonghua jiehe he huxi zazhi = Chin. J. Tuberc. Respir. Dis. 2020;43
    1. Xu J.-F., Wang L., Zhao L. Research Square; 2020. Risk Assessment of Venous Thromboembolism and Bleeding in COVID-19 Patients.
    1. Poissy J., Goutay J., Caplan M. Pulmonary embolism in COVID-19 patients: awareness of an increased prevalence. Circulation. 2020 doi: 10.1161/circulationaha.120.047430.
    1. Klok F.A., Kruip M., van der Meer N.J.M. Incidence of thrombotic complications in critically ill ICU patients with COVID-19. Thromb. Res. 2020 doi: 10.1016/j.thromres.2020.04.013.
    1. Klok F.A., Kruip M., van der Meer N.J.M. Confirmation of the high cumulative incidence of thrombotic complications in critically ill ICU patients with COVID-19: an updated analysis. Thromb. Res. 2020 doi: 10.1016/j.thromres.2020.04.041.
    1. Middeldorp S., Coppens M., van Haaps T.F. 2020040345. Preprints; 2020. Incidence of Venous Thromboembolism in Hospitalized Patients with COVID-19.
    1. Middeldorp S., Coppens M., van Haaps T.F. Incidence of venous thromboembolism in hospitalized patients with COVID-19. J. Thromb. Haemost. 2020 doi: 10.1111/jth.14888. (n/a)
    1. Helms J., Tacquard C., Severac F., Leonard-Lorant I., Ohana M., Delabranche X. High risk of thrombosis in patients in severe SARS-CoV-2 infection: a multicenter prospective cohort study. Intensive Care Med. 2020 doi: 10.1007/s00134-020-06062-x.
    1. Iba T., Levy J.H., Warkentin T.E., Thachil J., van der Poll T., Levi M. Diagnosis and management of sepsis-induced coagulopathy and disseminated intravascular coagulation. J. Thromb. Haemost. 2019;17:1989–1994.
    1. Llitjos J.F., Leclerc M., Chochois C. High incidence of venous thromboembolic events in anticoagulated severe COVID-19 patients. J. Thromb. Haemost. 2020 doi: 10.1111/jth.14869.
    1. 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 doi: 10.1111/jth.14830. (n/a)
    1. Thomas W., Varley J., Johnston A. Thrombotic complications of patients admitted to intensive care with COVID-19 at a teaching hospital in the United Kingdom. Thromb. Res. 2020 doi: 10.1016/j.thromres.2020.04.028. (In press)
    1. Leonard-Lorant I., Delabranche X., Severac F. Acute pulmonary embolism in COVID-19 patients on CT angiography and relationship to D-dimer levels. Radiology. 2020;201561
    1. Grillet F., Behr J., Calame P., Aubry S., Delabrousse E. Acute pulmonary embolism associated with COVID-19 pneumonia detected by pulmonary CT angiography. Radiology. 2020;201544
    1. Cattaneo M., Bertinato E.M., Birocchi S. Pulmonary embolism or pulmonary thrombosis in COVID-19? Is the recommendation to use high-dose heparin for thromboprophylaxis justified? Thromb. Haemost. 2020 doi: 10.1055/s-0040-1712097.
    1. Oxley T.J., Mocco J., Majidi S. Large-vessel stroke as a presenting feature of Covid-19 in the young. N. Engl. J. Med. 2020;382
    1. Mao L., Jin H., Wang M. Neurologic manifestations of hospitalized patients with coronavirus disease 2019 in Wuhan, China. JAMA Neurol. 2020 doi: 10.1001/jamaneurol.2020.1127.
    1. Dominguez-Erquicia P., Dobarro D., Raposeiras-Roubin S., Bastos-Fernandez G., Iniguez-Romo A. Multivessel coronary thrombosis in a patient with COVID-19 pneumonia. Eur. Heart J. 2020 doi: 10.1093/eurheartj/ehaa393.
    1. Oudkerk M., Buller H.R., Kuijpers D. Diagnosis, prevention, and treatment of thromboembolic complications in COVID-19: report of the National Institute for Public Health of the Netherlands. Radiology. 2020;201629
    1. Chen J., Wang X., Zhang S. Société Française d'Anesthésie et de Réanimation; 2020. Findings of Acute Pulmonary Embolism in COVID-19 Patients.
    1. Zuckier L.S., Moadel R.M., Haramati L.B., Freeman L. Diagnostic evaluation of pulmonary embolism during the COVID-19 pandemic. J. Nucl. Med. Off. Publ. Soc. Nucl. Med. 2020;61:630–631.
    1. 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):1094–1099.
    1. Paranjpe I., Fuster V., Lala A. Association of treatment dose anticoagulation with in-hospital survival among hospitalized patients with COVID-19. J. Am. Coll. Cardiol. 2020 doi: 10.1016/j.jacc.2020.05.001.
    1. Wu Y., Wang T., Guo C. Plasminogen improves lung lesions and hypoxemia in patients with COVID-19. QJM: Mon. J. Assoc. Phys. 2020 doi: 10.1093/qjmed/hcaa121.
    1. Testa S., Prandoni P., Paoletti O. Direct oral anticoagulant plasma levels' striking increase in severe COVID-19 respiratory syndrome patients treated with antiviral agents: the Cremona experience. J. Thromb. Haemost. 2020 doi: 10.1111/jth.14871.
    1. Ten V.S., Pinsky D.J. Endothelial response to hypoxia: physiologic adaptation and pathologic dysfunction. Curr. Opin. Crit. Care. 2002;8:242–250.
    1. Kamikura Y., Wada H., Sase T. Hemostatic abnormalities and leukocyte activation caused by infection in patients with malignant lymphoma during chemotherapy. Thromb. Res. 2006;117:671–679.
    1. Mullier F., Vanpee D., Jamart J. Comparison of five D-dimer reagents and application of an age-adjusted cut-off for the diagnosis of venous thromboembolism in emergency department. Blood Coagul. Fibrinolysis Int. J. Haemost. Thromb. 2014;25:309–315.
    1. Rodger M.A., Le Gal G., Langlois N.J. "HERDOO2" clinical decision rule to guide duration of anticoagulation in women with unprovoked venous thromboembolism. Can I use any d-Dimer? Thromb. Res. 2018;169:82–86.
    1. Kaplan D., Casper T.C., Elliott C.G. VTE Incidence and risk factors in patients with severe sepsis and septic shock. Chest. 2015;148:1224–1230.
    1. Zhang C., Zhang Z., Mi J. The cumulative venous thromboembolism incidence and risk factors in intensive care patients receiving the guideline-recommended thromboprophylaxis. Medicine. 2019;98
    1. Dolhnikoff M., Duarte-Neto A.N., de Almeida Monteiro R.A. Pathological evidence of pulmonary thrombotic phenomena in severe COVID-19. J. Thromb. Haemost. 2020 doi: 10.1111/jth.14844.
    1. Thachil J., Cushman M., Srivastava A. A proposal for staging COVID-19 coagulopathy. Res. Pract. Thromb. Haemost. 2020 doi: 10.1002/rth2.12372.

Source: PubMed

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