Incidence of VTE and Bleeding Among Hospitalized Patients With Coronavirus Disease 2019
2020; Elsevier BV; Volume: 159; Issue: 3 Linguagem: Inglês
10.1016/j.chest.2020.11.005
ISSN1931-3543
AutoresDavid Jiménez, Aldara García‐Sánchez, Parth Rali, Alfonso Muriel, Behnood Bikdeli, Pedro Ruiz‐Artacho, Raphaël Le Mao, Carmen Rodríguez, Beverley J. Hunt, Manuel Monréal,
Tópico(s)Cardiovascular Syncope and Autonomic Disorders
ResumoBackgroundIndividual studies have reported widely variable rates for VTE and bleeding among hospitalized patients with coronavirus disease 2019 (COVID-19).Research QuestionWhat is the incidence of VTE and bleeding among hospitalized patients with COVID-19?MethodsIn this systematic review and meta-analysis, 15 standard sources and COVID-19-specific sources were searched between January 1, 2020, and July 31, 2020, with no restriction according to language. Incidence estimates were pooled by using random effects meta-analyses. Heterogeneity was evaluated by using the I2 statistic, and publication bias was assessed by using the Begg and Egger tests.ResultsThe pooled incidence was 17.0% (95% CI, 13.4-20.9) for VTE, 12.1% (95% CI, 8.4-16.4) for DVT, 7.1% (95% CI, 5.3-9.1) for pulmonary embolism (PE), 7.8% (95% CI, 2.6-15.3) for bleeding, and 3.9% (95% CI, 1.2-7.9) for major bleeding. In subgroup meta-analyses, the incidence of VTE was higher when assessed according to screening (33.1% vs 9.8% by clinical diagnosis), among patients in the ICU (27.9% vs 7.1% in the ward), in prospective studies (25.5% vs 12.4% in retrospective studies), and with the inclusion of catheter-associated thrombosis/isolated distal DVTs and isolated subsegmental PEs. The highest pooled incidence estimate of bleeding was reported for patients receiving intermediate- or full-dose anticoagulation (21.4%) and the lowest in the only prospective study that assessed bleeding events (2.7%).InterpretationAmong hospitalized patients with COVID-19, the overall estimated pooled incidence of VTE was 17.0%, with higher rates with routine screening, inclusion of distal DVT, and subsegmental PE, in critically ill patients and in prospective studies. Bleeding events were observed in 7.8% of patients and were sensitive to use of escalated doses of anticoagulants and nature of data collection. Additional studies are required to ascertain the significance of various thrombotic events and to identify strategies to improve patient outcomes.Trial RegistryPROSPERO; No.: CRD42020198864; URL: https://www.crd.york.ac.uk/prospero/. Individual studies have reported widely variable rates for VTE and bleeding among hospitalized patients with coronavirus disease 2019 (COVID-19). What is the incidence of VTE and bleeding among hospitalized patients with COVID-19? In this systematic review and meta-analysis, 15 standard sources and COVID-19-specific sources were searched between January 1, 2020, and July 31, 2020, with no restriction according to language. Incidence estimates were pooled by using random effects meta-analyses. Heterogeneity was evaluated by using the I2 statistic, and publication bias was assessed by using the Begg and Egger tests. The pooled incidence was 17.0% (95% CI, 13.4-20.9) for VTE, 12.1% (95% CI, 8.4-16.4) for DVT, 7.1% (95% CI, 5.3-9.1) for pulmonary embolism (PE), 7.8% (95% CI, 2.6-15.3) for bleeding, and 3.9% (95% CI, 1.2-7.9) for major bleeding. In subgroup meta-analyses, the incidence of VTE was higher when assessed according to screening (33.1% vs 9.8% by clinical diagnosis), among patients in the ICU (27.9% vs 7.1% in the ward), in prospective studies (25.5% vs 12.4% in retrospective studies), and with the inclusion of catheter-associated thrombosis/isolated distal DVTs and isolated subsegmental PEs. The highest pooled incidence estimate of bleeding was reported for patients receiving intermediate- or full-dose anticoagulation (21.4%) and the lowest in the only prospective study that assessed bleeding events (2.7%). Among hospitalized patients with COVID-19, the overall estimated pooled incidence of VTE was 17.0%, with higher rates with routine screening, inclusion of distal DVT, and subsegmental PE, in critically ill patients and in prospective studies. Bleeding events were observed in 7.8% of patients and were sensitive to use of escalated doses of anticoagulants and nature of data collection. Additional studies are required to ascertain the significance of various thrombotic events and to identify strategies to improve patient outcomes. PROSPERO; No.: CRD42020198864; URL: https://www.crd.york.ac.uk/prospero/. FOR EDITORIAL COMMENT, SEE PAGE 908Coronavirus disease 2019 (COVID-19), a viral illness caused by the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), results in substantial respiratory pathology and also causes important manifestations outside the pulmonary parenchyma.1Zaim S. Chong J.H. Sankaranarayanan V. Harky A. COVID-19 and multiorgan response.Curr Probl Cardiol. 2020; 45: 100618Crossref PubMed Scopus (663) Google Scholar,2Gupta A. Madhavan M.V. Sehgal K. et al.Extrapulmonary manifestations of COVID-19.Nat Med. 2020; 26: 1017-1032Crossref PubMed Scopus (1988) Google Scholar COVID-19 may predispose patients to venous thromboembolic events (DVT and/or pulmonary embolism [PE]) due to hypoxia, excessive inflammation, platelet activation, endothelial dysfunction, and stasis.3Bikdeli B. Madhavan M.V. 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: 2950-2973Crossref PubMed Scopus (2190) Google Scholar Accumulating evidence suggests that hospitalized patients with COVID-19 may have a high incidence of VTE, including those receiving standard thromboprophylaxis according to guidelines for acutely ill medical patients.4Poissy J. Goutay J. Caplan M. et al.Lille ICU Haemostasis COVID-19 groupPulmonary embolism in COVID-19 patients: awareness of an increased prevalence.Circulation. 2020; 142: 184-186Crossref PubMed Scopus (831) Google Scholar, 5Klok F.A. Kruip M.J.H.A. van der Meer N.J.M. et al.Incidence of thrombotic complications in critically ill ICU patients with COVID-19.Thromb Res. 2020; 191: 145-147Abstract Full Text Full Text PDF PubMed Scopus (3310) Google Scholar, 6Fernández-Capitán C, Barba R, Díaz-Pedroche MDC, et al. Presenting characteristics, treatment patterns and outcomes among patients with Venous Thromboembolism during hospitalisation for COVID-19 [published online ahead of print October 21, 2020]. Semin Thromb Hemost. https://doi.org/10.1055/s-0040-1718402..Google Scholar, 7Moores L.K. Tritschler T. Brosnahan S. et al.Prevention, diagnosis, and treatment of VTE in patients with coronavirus disease 2019: CHEST Guideline and Expert Panel Report.Chest. 2020; 158: 1143-1163Abstract Full Text Full Text PDF PubMed Scopus (498) Google Scholar FOR EDITORIAL COMMENT, SEE PAGE 908 However, an accurate estimate of the incidence of VTE in hospitalized patients diagnosed with COVID-19 remains unclear, with incidence rates reported between 4.8% and 85%.5Klok F.A. Kruip M.J.H.A. van der Meer N.J.M. et al.Incidence of thrombotic complications in critically ill ICU patients with COVID-19.Thromb Res. 2020; 191: 145-147Abstract Full Text Full Text PDF PubMed Scopus (3310) Google Scholar,8Al-Samkari H. Karp Leaf R.S. Dzik W.H. et al.COVID and coagulation: bleeding and thrombotic manifestations of SARS-CoV2 infection.Blood. 2020; 136: 489-500Crossref PubMed Scopus (15) Google Scholar, 9Ren B. Yan F. Deng Z. et al.Extremely high incidence of lower extremity deep venous thrombosis in 48 patients with severe COVID-19 in Wuhan.Circulation. 2020; 142: 181-183Crossref PubMed Scopus (173) Google Scholar, 10Thomas W. Varley J. Johnston A. et al.Thrombotic complications of patients admitted to intensive care with COVID-19 at a teaching hospital in the United Kingdom.Thromb Res. 2020; 191: 76-77Abstract Full Text Full Text PDF PubMed Scopus (138) Google Scholar, 11Middeldorp S. Coppens M. van Haaps T.F. et al.Incidence of venous thromboembolism in hospitalized patients with COVID-19.J Thromb Haemost. 2020; 18: 1995-2002Crossref PubMed Scopus (1101) Google Scholar This variability might have been influenced by the type of events counted, the type of testing for VTE, assessment setting, and the use and type of thromboprophylaxis. Furthermore, the assessment of PE in patients with COVID-19 is conflated by the presence of immunothrombosis.12McFadyen J.D. Stevens H. Peter K. The emerging threat of (micro)thrombosis in COVID-19 and its therapeutic implications.Circ Res. 2020; 127: 571-587Crossref PubMed Scopus (410) Google Scholar It is likely that in some patients with COVID-19, local inflammation in the lungs with subsequent endothelial inflammation, complement activation, thrombin generation, platelet and leukocyte recruitment, and the initiation of innate and adaptive immune responses culminate in in situ small pulmonary vessel thrombosis. In addition to an increased risk of thrombosis, patients with COVID-19 might be at risk of excess bleeding due to factors such as imbalances in platelet production and destruction, coagulation factor consumption in the setting of severe inflammation, and use of antiplatelet or anticoagulant agents.13Colling M.E. Kanthi Y. COVID-19-associated coagulopathy: an exploration of mechanisms.Vasc Med. 2020; 25: 471-478Crossref PubMed Scopus (190) Google Scholar A recent retrospective study, which included 144 critically ill patients primarily receiving standard-dose prophylactic anticoagulation, found a major bleeding event rate of 5.6%.14Tang N. Li D. Wang X. Abnormal coagulation parameters are associated with poor prognosis in patients with novel coronavirus pneumonia.J Thromb Haemost. 2020; 18: 844-847Crossref PubMed Scopus (4043) Google Scholar Comprehensive assessment of the thrombotic and hemorrhagic event rates is critical in the thorough assessment of the disease course for COVID-19 and for considering strategies to mitigate patient outcomes. Our goal, therefore, was to conduct a comprehensive systematic review and meta-analysis to assess the overall incidence of VTE and bleeding among hospitalized patients with COVID-19. We prospectively submitted the systematic review protocol for registration on PROSPERO (CRD42020198864) (e-Appendix 1). We followed the Reporting Checklist for Meta-analyses of Observational Studies (MOOSE)15Stroup D.F. Berlin J.A. Morton S.C. et al.Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group.JAMA. 2000; 283: 2008-2012Crossref PubMed Scopus (16938) Google Scholar to conduct and report this systematic review (e-Table 1). From January 1, 2020, to July 31, 2020, we included observational studies such as cohort and cross-sectional studies in any geographical area evaluating the incidence of VTE and/or bleeding among hospitalized patients with World Health Organization-defined confirmed or probable COVID-19. Studies enrolling < 10 consecutive patients initially hospitalized for COVID-19 were excluded. We searched MEDLINE (using the Ovid platform), PubMed, Embase, Cumulative Index to Nursing and Allied Health Literature (using the Ovid platform), the Cochrane Library, COVID-19 Open Research Dataset Challenge, COVID-19 Research Database (World Health Organization), Epistemonikos (COVID-19 Living Overview of the Evidence platform), EPPI Centre living systematic map of the evidence, and reference lists of included papers. Preprint servers (bioRxiv, medRxiv, and Social Science Research Network First Look) and coronavirus resource centers of the Lancet, JAMA, and the New England Journal of Medicine (e-Appendix 2) were hand-searched. The search was not limited by language. The search strategy is available in e-Appendix 2. We screened titles and abstracts, reviewed full texts, and extracted data. Risk of bias was assessed by two authors (D. J. and A. G.-S.) and independently using standardized prepiloted forms. Disagreements were resolved by discussion within the wider team (P. R., B. B., and M. M.). The primary outcome was the incidence of nonfatal or fatal VTE during hospitalization for COVID-19, expressed as the proportion of patients with a diagnosis of VTE. VTE included upper and lower limb DVT and PE diagnosed by using accepted imaging tests, either following clinical suspicion or by routine screening. The secondary outcome was the incidence of bleeding during hospitalization for COVID-19. The incidence of major bleeding (including fatal bleeds) was also determined. Definitions of major bleeding were according to definitions in the individual studies. The outcomes data from the first available time point identified as a primary end point from each study were incorporated into the primary analysis. Because of high heterogeneity (as expected and observed), pooled data on the incidence of VTE and major bleeding were analyzed by using a random effects (DerSimonian and Laird method) model approach. 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O'Connell D. et al.The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomized studies in meta-analyses.http://www.ohri.ca/programs/clinical_epidemiology/oxford.aspDate accessed: July 22, 2020Google Scholar The Begg rank correlation method was used to assess for publication bias. Data for subgroup effects were analyzed according to VTE type (ie, DVT vs PE), as well as setting (ward vs ICU), type of assessment for VTE (ie, screening vs clinical diagnosis), intensity of pharmacologic thromboprophylaxis (no pharmacologic thromboprophylaxis [arbitrarily predefined as ≤ 40% of the study population receiving any pharmacologic prophylaxis] vs standard-dose thromboprophylaxis [arbitrarily predefined as ≥ 70% of the study population receiving standard-dose thromboprophylaxis] vs intermediate-dose thromboprophylaxis or therapeutic anticoagulation), geographical area (North America vs Europe vs rest of the world), and study design (prospective vs retrospective). We also analyzed the incidence of PE and DVT after excluding episodes of isolated subsegmental PE (ISSPE) and catheter-associated thrombosis (CAT)/isolated distal DVT (IDDVT), respectively. Two sensitivity analyses were conducted to test the robustness of the study findings. First, outcomes were analyzed from the longest available follow-up points in studies reporting outcomes at multiple time points to ensure no significant changes in outcome estimates. Second, supplemental analyses with inverse variance fixed effects models were run. Analyses were conducted by using Stata version 14.2 (StataCorp). The searches yielded 10,141 citations. After duplicates were removed and the titles and abstracts reviewed, 9,889 articles were excluded. Of the remaining 252 studies, 203 were excluded after reviewing the full-text manuscript. A total of 49 studies reporting the incidence of venous thrombosis (n = 44), bleeding (n = 1), or both (n = 4) were included in the review.4Poissy J. Goutay J. 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Prevalence, risk factors, and outcome.Circulation. 2020; 142: 114-128Crossref PubMed Scopus (332) Google Scholar Two studies included overlapping patient populations,5Klok F.A. Kruip M.J.H.A. van der Meer N.J.M. et al.Incidence of thrombotic complications in critically ill ICU patients with COVID-19.Thromb Res. 2020; 191: 145-147Abstract Full Text Full Text PDF PubMed Scopus (3310) Google Scholar,39Koleilat I, Galen B, Choinski K, et al. Clinical characteristics of acute lower extremity deep venous thrombosis diagnosed by duplex in patients hospitalized for coronavirus disease 2019.Google Scholar and only outcomes data from the first publication were considered for the analyses (Fig 1). This review is based on a pooled sample of 18,093 patients with reported information related to VTE, 1,273 of whom experienced a VTE event (47 studies),4Poissy J. Goutay J. Caplan M. et al.Lille ICU Haemostasis COVID-19 groupPulmonary embolism in COVID-19 patients: awareness of an increased prevalence.Circulation. 2020; 142: 184-186Crossref PubMed Scopus (831) Google Scholar,5Klok F.A. Kruip M.J.H.A. van der Meer N.J.M. et al.Incidence of thrombotic complications in critically ill ICU patients with COVID-19.Thromb Res. 2020; 191: 145-147Abstract Full Text Full Text PDF PubMed Scopus (3310) Google Scholar,8Al-Samkari H. Karp Leaf R.S. Dzik W.H. et al.COVID and coagulation: bleeding and thrombotic manifestations of SARS-CoV2 infection.Blood. 2020; 136: 489-500Crossref PubMed Scopus (15) Google Scholar, 9Ren B. Yan F. Deng Z. et al.Extremely high incidence of lower extremity deep venous thrombosis in 48 patients with severe COVID-19 in Wuhan.Circulation. 2020; 142: 181-183Crossref PubMed Scopus (173) Google Scholar, 10Thomas W. Varley J. Johnston A. et al.Thrombotic complications of patients admitted to intensive care with COVID-19 at a teaching hospital in the United Kingdom.Thromb Res. 2020; 191: 76-77Abstract Full Text Full Text PDF PubMed Scopus (138) Google Scholar, 11Middeldorp S. Coppens M. van Haaps T.F. et al.Incidence of venous thromboembolism in hospitalized patients with COVID-19.J Thromb Haemost. 2020; 18: 1995-2002Crossref PubMed Scopus (1101) Google Scholar,20Artifoni M. Danic G. Gautier G. et al.Systematic assessment of venous thromboembolism in COVID-19 patients receiving thromboprophylaxis: incidence and role of D-dimer as predictive factors.J Thromb Thrombolysis. 2020; 50: 211-216Crossref PubMed Scopus (188) Google Scholar, 21Beun R. Kusadasi N. Sikma M. Westerink J. Huisman A. Thromboembolic events and apparent heparin resistance in patients infected with SARS-CoV-2.Int J Lab Hematol. 2020; 42: 19-20Crossref PubMed Scopus (120) Google Scholar, 22Bilaloglu S. Aphinyanaphongs Y. Jones S. Iturrate E. Hochman J. Berger J.S. Thrombosis in hospitalized patients with COVID-19 in a New York City Health System.JAMA. 2020; 324: 799-801Crossref PubMed Scopus (561) Google Scholar, 23Cattaneo M. Bertinato E.M. Birocchi S. et al.Pulmonary embolism or pulmonary thrombosis in COVID-19? Is the recommendation to use high-dose heparin for thromboprophylaxis justified?.Thromb Haemost. 2020; 120: 1230-1232Crossref PubMed Scopus (240) Google Scholar, 24Che
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