Skip to main content
Top
Published in: Thrombosis Journal 1/2021

Open Access 01-12-2021 | Phlebothrombosis | Research

Proximal deep vein thrombosis and pulmonary embolism in COVID-19 patients: a systematic review and meta-analysis

Authors: Gregoire Longchamp, Sara Manzocchi-Besson, Alban Longchamp, Marc Righini, Helia Robert-Ebadi, Marc Blondon

Published in: Thrombosis Journal | Issue 1/2021

Login to get access

Abstract

Background

COVID-19 appears to be associated with a high risk of venous thromboembolism (VTE). We aimed to systematically review and meta-analyze the risk of clinically relevant VTE in patients hospitalized for COVID-19.

Methods

This meta-analysis included original articles in English published from January 1st, 2020 to June 15th, 2020 in Pubmed/MEDLINE, Embase, Web of science, and Cochrane. Outcomes were major VTE, defined as any objectively diagnosed pulmonary embolism (PE) and/or proximal deep vein thrombosis (DVT). Primary analysis estimated the risk of VTE, stratified by acutely and critically ill inpatients. Secondary analyses explored the separate risk of proximal DVT and of PE; the risk of major VTE stratified by screening and by type of anticoagulation.

Results

In 33 studies (n = 4009 inpatients) with heterogeneous thrombotic risk factors, VTE incidence was 9% (95%CI 5–13%, I2 = 92.5) overall, and 21% (95%CI 14–28%, I2 = 87.6%) for patients hospitalized in the ICU. Proximal lower limb DVT incidence was 3% (95%CI 1–5%, I2 = 87.0%) and 8% (95%CI 3–14%, I2 = 87.6%), respectively. PE incidence was 8% (95%CI 4–13%, I2 = 92.1%) and 17% (95%CI 11–25%, I2 = 89.3%), respectively. Screening and absence of anticoagulation were associated with a higher VTE incidence. When restricting to medically ill inpatients, the VTE incidence was 2% (95%CI 0–6%).

Conclusions

The risk of major VTE among COVID-19 inpatients is high but varies greatly with severity of the disease. These findings reinforce the need for the use of thromboprophylaxis in all COVID-19 inpatients and for clinical trials testing different thromboprophylaxis regimens in subgroups of COVID-19 inpatients.

Trial registration

The review protocol was registered in PROSPERO International Prospective Register of Systematic Reviews (CRD42020193369).
Appendix
Available only for authorised users
Literature
1.
go back to reference Varga Z, Flammer AJ, Steiger P, Haberecker M, Andermatt R, Zinkernagel AS, et al. Endothelial cell infection and endotheliitis in COVID-19. Lancet. 2020;395(10234):1417–8.PubMedPubMedCentralCrossRef Varga Z, Flammer AJ, Steiger P, Haberecker M, Andermatt R, Zinkernagel AS, et al. Endothelial cell infection and endotheliitis in COVID-19. Lancet. 2020;395(10234):1417–8.PubMedPubMedCentralCrossRef
3.
go back to reference Zhou F, Yu T, Du R, Fan G, Liu Y, Liu Z, et al. 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(10229):1054–62.CrossRef Zhou F, Yu T, Du R, Fan G, Liu Y, Liu Z, et al. 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(10229):1054–62.CrossRef
4.
go back to reference Wang D, Hu B, Hu C, Zhu F, Liu X, Zhang J, et al. Clinical characteristics of 138 hospitalized patients with 2019 novel coronavirus-infected pneumonia in Wuhan, China. JAMA. 2020;323(11):1061–9.PubMedPubMedCentralCrossRef Wang D, Hu B, Hu C, Zhu F, Liu X, Zhang J, et al. Clinical characteristics of 138 hospitalized patients with 2019 novel coronavirus-infected pneumonia in Wuhan, China. JAMA. 2020;323(11):1061–9.PubMedPubMedCentralCrossRef
5.
go back to reference Klok FA, Kruip MJHA, van der Meer NJM, Arbous MS, Gommers DAMPJ, Kant KM, et al. Incidence of thrombotic complications in critically ill ICU patients with COVID-19. Thromb Res. 2020;191:145–7.PubMedPubMedCentralCrossRef Klok FA, Kruip MJHA, van der Meer NJM, Arbous MS, Gommers DAMPJ, Kant KM, et al. Incidence of thrombotic complications in critically ill ICU patients with COVID-19. Thromb Res. 2020;191:145–7.PubMedPubMedCentralCrossRef
6.
go back to reference Ren B, Yan F, Deng Z, Zhang S, Xiao L, Wu M, et al. Extremely high incidence of lower extremity deep venous thrombosis in 48 patients with severe COVID-19 in Wuhan. Circulation. 2020;142(2):181–3.PubMedCrossRef Ren B, Yan F, Deng Z, Zhang S, Xiao L, Wu M, et al. Extremely high incidence of lower extremity deep venous thrombosis in 48 patients with severe COVID-19 in Wuhan. Circulation. 2020;142(2):181–3.PubMedCrossRef
8.
go back to reference Fang Y, Zhang H, Xie J, Lin M, Ying L, Pang P, et al. Sensitivity of chest CT for COVID-19: comparison to RT-PCR. Radiology. 2020;296(2):E115–7.PubMedCrossRef Fang Y, Zhang H, Xie J, Lin M, Ying L, Pang P, et al. Sensitivity of chest CT for COVID-19: comparison to RT-PCR. Radiology. 2020;296(2):E115–7.PubMedCrossRef
9.
go back to reference Konstantinides S, Meyer G, Becattini C, Bueno H, Geersing G, Harjola V, et al. 2019 ESC guidelines for the diagnosis and management of acute pulmonary embolism developed in collaboration with the European Respiratory Society (ERS). Eur Heart J. 2004;41:543–603.CrossRef Konstantinides S, Meyer G, Becattini C, Bueno H, Geersing G, Harjola V, et al. 2019 ESC guidelines for the diagnosis and management of acute pulmonary embolism developed in collaboration with the European Respiratory Society (ERS). Eur Heart J. 2004;41:543–603.CrossRef
11.
go back to reference Blondon M, Casini A, Hoppe KK, Boehlen F, Righini M, Smith NL. Risks of venous thromboembolism after cesarean sections: a meta-analysis. Chest. 2016 Sep;150(3):572–96.PubMedCrossRef Blondon M, Casini A, Hoppe KK, Boehlen F, Righini M, Smith NL. Risks of venous thromboembolism after cesarean sections: a meta-analysis. Chest. 2016 Sep;150(3):572–96.PubMedCrossRef
12.
go back to reference Al-Samkari H, Karp Leaf RS, Dzik WH, Carlson JCT, Fogerty AE, Waheed A, et al. COVID-19 and coagulation: bleeding and thrombotic manifestations of SARS-CoV-2 infection. Blood. 2020;136(4):489–500.PubMedCrossRef Al-Samkari H, Karp Leaf RS, Dzik WH, Carlson JCT, Fogerty AE, Waheed A, et al. COVID-19 and coagulation: bleeding and thrombotic manifestations of SARS-CoV-2 infection. Blood. 2020;136(4):489–500.PubMedCrossRef
13.
go back to reference Annunziata A, Imitazione P, Polistina GE, Lanza M, Coppola A, Fiorentino G. Pulmonary embolism in Covid-19: coagulation parameters, close monitoring to prevent? Turk Thorac J. 2020;21(4):287–8.PubMedPubMedCentralCrossRef Annunziata A, Imitazione P, Polistina GE, Lanza M, Coppola A, Fiorentino G. Pulmonary embolism in Covid-19: coagulation parameters, close monitoring to prevent? Turk Thorac J. 2020;21(4):287–8.PubMedPubMedCentralCrossRef
14.
go back to reference Artifoni M, Danic G, Gautier G, Gicquel P, Boutoille D, Raffi F, 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 Jul;50(1):211–6.PubMedCrossRefPubMedCentral Artifoni M, Danic G, Gautier G, Gicquel P, Boutoille D, Raffi F, 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 Jul;50(1):211–6.PubMedCrossRefPubMedCentral
15.
go back to reference Beun 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(Suppl 1):19–20.PubMedCrossRefPubMedCentral Beun 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(Suppl 1):19–20.PubMedCrossRefPubMedCentral
16.
go back to reference Beyls C, Huette P, Abou-Arab O, Berna P, Mahjoub Y. Extracorporeal membrane oxygenation for COVID-19-associated severe acute respiratory distress syndrome and risk of thrombosis. Br J Anaesth. 2020;125(2):e260–2.PubMedCrossRef Beyls C, Huette P, Abou-Arab O, Berna P, Mahjoub Y. Extracorporeal membrane oxygenation for COVID-19-associated severe acute respiratory distress syndrome and risk of thrombosis. Br J Anaesth. 2020;125(2):e260–2.PubMedCrossRef
17.
go back to reference Campochiaro C, Della-Torre E, Cavalli G, De Luca G, Ripa M, Boffini N, et al. Efficacy and safety of tocilizumab in severe COVID-19 patients: a single-Centre retrospective cohort study. Eur J Intern Med. 2020;76:43–9.PubMedPubMedCentralCrossRef Campochiaro C, Della-Torre E, Cavalli G, De Luca G, Ripa M, Boffini N, et al. Efficacy and safety of tocilizumab in severe COVID-19 patients: a single-Centre retrospective cohort study. Eur J Intern Med. 2020;76:43–9.PubMedPubMedCentralCrossRef
18.
go back to reference Cattaneo M, Bertinato EM, Birocchi S, Brizio C, Malavolta D, Manzoni M, 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(8):1230–2.PubMedPubMedCentralCrossRef Cattaneo M, Bertinato EM, Birocchi S, Brizio C, Malavolta D, Manzoni M, 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(8):1230–2.PubMedPubMedCentralCrossRef
20.
go back to reference Demelo-Rodríguez P, Cervilla-Muñoz E, Ordieres-Ortega L, Parra-Virto A, Toledano-Macías M, Toledo-Samaniego N, et al. Incidence of asymptomatic deep vein thrombosis in patients with COVID-19 pneumonia and elevated D-dimer levels. Thromb Res. 2020 May 13;192:23–6.PubMedPubMedCentralCrossRef Demelo-Rodríguez P, Cervilla-Muñoz E, Ordieres-Ortega L, Parra-Virto A, Toledano-Macías M, Toledo-Samaniego N, et al. Incidence of asymptomatic deep vein thrombosis in patients with COVID-19 pneumonia and elevated D-dimer levels. Thromb Res. 2020 May 13;192:23–6.PubMedPubMedCentralCrossRef
21.
go back to reference Desborough MJR, Doyle AJ, Griffiths A, Retter A, Breen KA, Hunt BJ. Image-proven thromboembolism in patients with severe COVID-19 in a tertiary critical care unit in the United Kingdom. Thromb Res. 2020;193:1–4.PubMedPubMedCentralCrossRef Desborough MJR, Doyle AJ, Griffiths A, Retter A, Breen KA, Hunt BJ. Image-proven thromboembolism in patients with severe COVID-19 in a tertiary critical care unit in the United Kingdom. Thromb Res. 2020;193:1–4.PubMedPubMedCentralCrossRef
22.
go back to reference Faggiano P, Bonelli A, Paris S, Milesi G, Bisegna S, Bernardi N, et al. Acute pulmonary embolism in COVID-19 disease: Preliminary report on seven patients. Int J Cardiol. 2020;313:129–31.PubMedPubMedCentralCrossRef Faggiano P, Bonelli A, Paris S, Milesi G, Bisegna S, Bernardi N, et al. Acute pulmonary embolism in COVID-19 disease: Preliminary report on seven patients. Int J Cardiol. 2020;313:129–31.PubMedPubMedCentralCrossRef
23.
go back to reference Fraissé M, Logre E, Pajot O, Mentec H, Plantefève G, Contou D. Thrombotic and hemorrhagic events in critically ill COVID-19 patients: a French monocenter retrospective study. Crit Care. 2020;24(1):275.PubMedPubMedCentralCrossRef Fraissé M, Logre E, Pajot O, Mentec H, Plantefève G, Contou D. Thrombotic and hemorrhagic events in critically ill COVID-19 patients: a French monocenter retrospective study. Crit Care. 2020;24(1):275.PubMedPubMedCentralCrossRef
24.
go back to reference Galeano-Valle F, Oblitas CM, Ferreiro-Mazón MM, Alonso-Muñoz J, Del Toro-Cervera J, di Natale M, et al. Antiphospholipid antibodies are not elevated in patients with severe COVID-19 pneumonia and venous thromboembolism. Thromb Res. 2020;192:113–5.PubMedPubMedCentralCrossRef Galeano-Valle F, Oblitas CM, Ferreiro-Mazón MM, Alonso-Muñoz J, Del Toro-Cervera J, di Natale M, et al. Antiphospholipid antibodies are not elevated in patients with severe COVID-19 pneumonia and venous thromboembolism. Thromb Res. 2020;192:113–5.PubMedPubMedCentralCrossRef
25.
go back to reference Grandmaison G, Andrey A, Périard D, Engelberger RP, Carrel G, Doll S, et al. Systematic screening for venous thromboembolic events in COVID-19 pneumonia. Thromb Haemost Open. 2020;4(2):e113–5. Grandmaison G, Andrey A, Périard D, Engelberger RP, Carrel G, Doll S, et al. Systematic screening for venous thromboembolic events in COVID-19 pneumonia. Thromb Haemost Open. 2020;4(2):e113–5.
26.
go back to reference 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;23:201544. 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;23:201544.
28.
go back to reference Hippensteel JA, LaRiviere WB, Colbert JF, Langouët-Astrié CJ, Schmidt EP. Heparin as a therapy for COVID-19: current evidence and future possibilities. Am J Physiol Lung Cell Mol Physiol. 2020;319(2):L211–7.PubMedPubMedCentralCrossRef Hippensteel JA, LaRiviere WB, Colbert JF, Langouët-Astrié CJ, Schmidt EP. Heparin as a therapy for COVID-19: current evidence and future possibilities. Am J Physiol Lung Cell Mol Physiol. 2020;319(2):L211–7.PubMedPubMedCentralCrossRef
31.
go back to reference Lodigiani C, Iapichino G, Carenzo L, Cecconi M, Ferrazzi P, Sebastian T, et al. Venous and arterial thromboembolic complications in COVID-19 patients admitted to an academic hospital in Milan, Italy. Thromb Res. 2020;191:9–14.PubMedPubMedCentralCrossRef Lodigiani C, Iapichino G, Carenzo L, Cecconi M, Ferrazzi P, Sebastian T, et al. Venous and arterial thromboembolic complications in COVID-19 patients admitted to an academic hospital in Milan, Italy. Thromb Res. 2020;191:9–14.PubMedPubMedCentralCrossRef
32.
go back to reference Longchamp A, Longchamp J, Manzocchi-Besson S, Whiting L, Haller C, Jeanneret S, et al. Venous thromboembolism in critically ill patients with Covid-19: results of a screening study for deep vein thrombosis. Res Pract Thromb Haemost. 2020 Jul;4(5):842–7.PubMedCrossRefPubMedCentral Longchamp A, Longchamp J, Manzocchi-Besson S, Whiting L, Haller C, Jeanneret S, et al. Venous thromboembolism in critically ill patients with Covid-19: results of a screening study for deep vein thrombosis. Res Pract Thromb Haemost. 2020 Jul;4(5):842–7.PubMedCrossRefPubMedCentral
33.
go back to reference Maatman TK, Jalali F, Feizpour C, Douglas A, McGuire SP, Kinnaman G, et al. Routine venous thromboembolism prophylaxis may be inadequate in the Hypercoagulable state of severe coronavirus disease 2019. Crit Care Med. 2020;48(9):e783–90.PubMedCrossRef Maatman TK, Jalali F, Feizpour C, Douglas A, McGuire SP, Kinnaman G, et al. Routine venous thromboembolism prophylaxis may be inadequate in the Hypercoagulable state of severe coronavirus disease 2019. Crit Care Med. 2020;48(9):e783–90.PubMedCrossRef
35.
go back to reference Middeldorp S, Coppens M, van Haaps TF, Foppen M, Vlaar AP, Müller MCA, et al. Incidence of venous thromboembolism in hospitalized patients with COVID-19. J Thromb Haemost JTH. 2020;18(8):1995–2002.PubMedCrossRef Middeldorp S, Coppens M, van Haaps TF, Foppen M, Vlaar AP, Müller MCA, et al. Incidence of venous thromboembolism in hospitalized patients with COVID-19. J Thromb Haemost JTH. 2020;18(8):1995–2002.PubMedCrossRef
36.
go back to reference Nahum J, Morichau-Beauchant T, Daviaud F, Echegut P, Fichet J, Maillet J-M, et al. Venous Thrombosis Among Critically Ill Patients With Coronavirus Disease 2019 (COVID-19). JAMA Netw Open. 2020;3(5):e2010478.PubMedPubMedCentralCrossRef Nahum J, Morichau-Beauchant T, Daviaud F, Echegut P, Fichet J, Maillet J-M, et al. Venous Thrombosis Among Critically Ill Patients With Coronavirus Disease 2019 (COVID-19). JAMA Netw Open. 2020;3(5):e2010478.PubMedPubMedCentralCrossRef
39.
go back to reference Tavazzi G, Civardi L, Caneva L, Mongodi S, Mojoli F. Thrombotic events in SARS-CoV-2 patients: an urgent call for ultrasound screening. Intensive Care Med. 2020;46(6):1121–3.PubMedCrossRefPubMedCentral Tavazzi G, Civardi L, Caneva L, Mongodi S, Mojoli F. Thrombotic events in SARS-CoV-2 patients: an urgent call for ultrasound screening. Intensive Care Med. 2020;46(6):1121–3.PubMedCrossRefPubMedCentral
40.
go back to reference Thomas W, Varley J, Johnston A, Symington E, Robinson M, Sheares K, et al. Thrombotic complications of patients admitted to intensive care with COVID-19 at a teaching hospital in the United Kingdom. Thromb Res. 2020 Apr 25;191:76–7.PubMedPubMedCentralCrossRef Thomas W, Varley J, Johnston A, Symington E, Robinson M, Sheares K, et al. Thrombotic complications of patients admitted to intensive care with COVID-19 at a teaching hospital in the United Kingdom. Thromb Res. 2020 Apr 25;191:76–7.PubMedPubMedCentralCrossRef
41.
go back to reference Voicu S, Bonnin P, Stépanian A, Chousterman BG, Le Gall A, Malissin I, et al. High prevalence of deep vein thrombosis in mechanically ventilated COVID-19 patients. J Am Coll Cardiol. 2020 Jul 28;76(4):480–2.PubMedPubMedCentralCrossRef Voicu S, Bonnin P, Stépanian A, Chousterman BG, Le Gall A, Malissin I, et al. High prevalence of deep vein thrombosis in mechanically ventilated COVID-19 patients. J Am Coll Cardiol. 2020 Jul 28;76(4):480–2.PubMedPubMedCentralCrossRef
42.
go back to reference Li Z, Xiaokai F, Danqing Z, Chunguo J, Heng M, Wang J, et al. Deep vein thrombosis in hospitalized patients with coronavirus disease 2019 (COVID-19) in Wuhan, China: prevalence, risk factors, and outcome. Circulation. 2020;142(2):114–28.PubMed Li Z, Xiaokai F, Danqing Z, Chunguo J, Heng M, Wang J, et al. Deep vein thrombosis in hospitalized patients with coronavirus disease 2019 (COVID-19) in Wuhan, China: prevalence, risk factors, and outcome. Circulation. 2020;142(2):114–28.PubMed
43.
go back to reference Zotzmann V, Lang CN, Bamberg F, Bode C, Staudacher DL. Are subpleural consolidations indicators for segmental pulmonary embolism in COVID-19? Intensive Care Med. 2020;46(6):1109–10.PubMedCrossRefPubMedCentral Zotzmann V, Lang CN, Bamberg F, Bode C, Staudacher DL. Are subpleural consolidations indicators for segmental pulmonary embolism in COVID-19? Intensive Care Med. 2020;46(6):1109–10.PubMedCrossRefPubMedCentral
44.
go back to reference Porfidia A, Valeriani E, Pola R, Porreca E, Rutjes AWS, Di Nisio M. Venous thromboembolism in patients with COVID-19: systematic review and meta-analysis. Thromb Res. 2020 Dec;196:67–74.PubMedPubMedCentralCrossRef Porfidia A, Valeriani E, Pola R, Porreca E, Rutjes AWS, Di Nisio M. Venous thromboembolism in patients with COVID-19: systematic review and meta-analysis. Thromb Res. 2020 Dec;196:67–74.PubMedPubMedCentralCrossRef
46.
go back to reference Lu Y, Pan L, Zhang W-W, Cheng F, Hu S-S, Zhang X, et al. A meta-analysis of the incidence of venous thromboembolic events and impact of anticoagulation on mortality in patients with COVID-19. Int J Infect Dis. 2020 Nov 1;100:34–41.PubMedPubMedCentralCrossRef Lu Y, Pan L, Zhang W-W, Cheng F, Hu S-S, Zhang X, et al. A meta-analysis of the incidence of venous thromboembolic events and impact of anticoagulation on mortality in patients with COVID-19. Int J Infect Dis. 2020 Nov 1;100:34–41.PubMedPubMedCentralCrossRef
48.
go back to reference Eichinger S, Heinze G, Jandeck LM, Kyrle PA. Risk assessment of recurrence in patients with unprovoked deep vein thrombosis or pulmonary embolism: the Vienna prediction model. Circulation. 2010 Apr 13;121(14):1630–6.PubMedCrossRef Eichinger S, Heinze G, Jandeck LM, Kyrle PA. Risk assessment of recurrence in patients with unprovoked deep vein thrombosis or pulmonary embolism: the Vienna prediction model. Circulation. 2010 Apr 13;121(14):1630–6.PubMedCrossRef
49.
go back to reference Righini M, Galanaud J-P, Guenneguez H, Brisot D, Diard A, Faisse P, et al. Anticoagulant therapy for symptomatic calf deep vein thrombosis (CACTUS): a randomised, double-blind, placebo-controlled trial. Lancet Haematol. 2016 Dec;3(12):e556–62.PubMedCrossRef Righini M, Galanaud J-P, Guenneguez H, Brisot D, Diard A, Faisse P, et al. Anticoagulant therapy for symptomatic calf deep vein thrombosis (CACTUS): a randomised, double-blind, placebo-controlled trial. Lancet Haematol. 2016 Dec;3(12):e556–62.PubMedCrossRef
50.
go back to reference Robert-Ebadi H, Righini M. Management of distal deep vein thrombosis. Thromb Res. 2017;149:48–55.PubMedCrossRef Robert-Ebadi H, Righini M. Management of distal deep vein thrombosis. Thromb Res. 2017;149:48–55.PubMedCrossRef
51.
go back to reference Spirk D, Sebastian T, Barco S, Banyai M, Beer JH, Mazzolai L, et al. Clinical outcomes of incidental venous thromboembolism in Cancer and noncancer patients: the SWIss venous ThromboEmbolism registry (SWIVTER). Thromb Haemost. 2020. https://doi.org/10.1055/s-0040-1720977. Spirk D, Sebastian T, Barco S, Banyai M, Beer JH, Mazzolai L, et al. Clinical outcomes of incidental venous thromboembolism in Cancer and noncancer patients: the SWIss venous ThromboEmbolism registry (SWIVTER). Thromb Haemost. 2020. https://​doi.​org/​10.​1055/​s-0040-1720977.
52.
go back to reference Cook D, Crowther M, Meade M, Rabbat C, Griffith L, Schiff D, et al. Deep venous thrombosis in medical-surgical critically ill patients: prevalence, incidence, and risk factors. Crit Care Med. 2005 Jul;33(7):1565–71.PubMedCrossRef Cook D, Crowther M, Meade M, Rabbat C, Griffith L, Schiff D, et al. Deep venous thrombosis in medical-surgical critically ill patients: prevalence, incidence, and risk factors. Crit Care Med. 2005 Jul;33(7):1565–71.PubMedCrossRef
53.
go back to reference PROTECT Investigators for the Canadian Critical Care Trials Group and the Australian and New Zealand Intensive Care Society Clinical Trials Group, Cook D, Meade M, Guyatt G, Walter S, Heels-Ansdell D, et al. Dalteparin versus unfractionated heparin in critically ill patients. N Engl J Med. 2011;364(14):1305–14.CrossRef PROTECT Investigators for the Canadian Critical Care Trials Group and the Australian and New Zealand Intensive Care Society Clinical Trials Group, Cook D, Meade M, Guyatt G, Walter S, Heels-Ansdell D, et al. Dalteparin versus unfractionated heparin in critically ill patients. N Engl J Med. 2011;364(14):1305–14.CrossRef
54.
go back to reference Blondon M, Spirk D, Kucher N, Aujesky D, Hayoz D, Beer JH, et al. Comparative performance of clinical risk assessment models for hospital-acquired venous thromboembolism in medical patients. Thromb Haemost. 2018;118(1):82–9.PubMedCrossRef Blondon M, Spirk D, Kucher N, Aujesky D, Hayoz D, Beer JH, et al. Comparative performance of clinical risk assessment models for hospital-acquired venous thromboembolism in medical patients. Thromb Haemost. 2018;118(1):82–9.PubMedCrossRef
55.
go back to reference Tritschler T, Mathieu M-E, Skeith L, Rodger M, Middeldorp S, Brighton T, et al. Anticoagulant interventions in hospitalized patients with COVID-19: a scoping review of randomized controlled trials and call for international collaboration. J Thromb Haemost JTH. 2020. https://doi.org/10.1111/jth.15094. Tritschler T, Mathieu M-E, Skeith L, Rodger M, Middeldorp S, Brighton T, et al. Anticoagulant interventions in hospitalized patients with COVID-19: a scoping review of randomized controlled trials and call for international collaboration. J Thromb Haemost JTH. 2020. https://​doi.​org/​10.​1111/​jth.​15094.
Metadata
Title
Proximal deep vein thrombosis and pulmonary embolism in COVID-19 patients: a systematic review and meta-analysis
Authors
Gregoire Longchamp
Sara Manzocchi-Besson
Alban Longchamp
Marc Righini
Helia Robert-Ebadi
Marc Blondon
Publication date
01-12-2021
Publisher
BioMed Central
Published in
Thrombosis Journal / Issue 1/2021
Electronic ISSN: 1477-9560
DOI
https://doi.org/10.1186/s12959-021-00266-x

Other articles of this Issue 1/2021

Thrombosis Journal 1/2021 Go to the issue