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Published in: BMC Infectious Diseases 1/2022

Open Access 01-12-2022 | Phlebothrombosis | Research article

Venous thromboembolism in COVID-19 patients and prediction model: a multicenter cohort study

Authors: Yi Lee, Qasim Jehangir, Pin Li, Deepthi Gudimella, Pooja Mahale, Chun-Hui Lin, Dinesh R. Apala, Geetha Krishnamoorthy, Abdul R. Halabi, Kiritkumar Patel, Laila Poisson, Venugopal Balijepally, Anupam A. Sule, Girish B. Nair

Published in: BMC Infectious Diseases | Issue 1/2022

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Abstract

Background

Patients with COVID-19 infection are commonly reported to have an increased risk of venous thrombosis. The choice of anti-thrombotic agents and doses are currently being studied in randomized controlled trials and retrospective studies. There exists a need for individualized risk stratification of venous thromboembolism (VTE) to assist clinicians in decision-making on anticoagulation. We sought to identify the risk factors of VTE in COVID-19 patients, which could help physicians in the prevention, early identification, and management of VTE in hospitalized COVID-19 patients and improve clinical outcomes in these patients.

Method

This is a multicenter, retrospective database of four main health systems in Southeast Michigan, United States. We compiled comprehensive data for adult COVID-19 patients who were admitted between 1st March 2020 and 31st December 2020. Four models, including the random forest, multiple logistic regression, multilinear regression, and decision trees, were built on the primary outcome of in-hospital acute deep vein thrombosis (DVT) and pulmonary embolism (PE) and tested for performance. The study also reported hospital length of stay (LOS) and intensive care unit (ICU) LOS in the VTE and the non-VTE patients. Four models were assessed using the area under the receiver operating characteristic curve and confusion matrix.

Results

The cohort included 3531 admissions, 3526 had discharge diagnoses, and 6.68% of patients developed acute VTE (N = 236). VTE group had a longer hospital and ICU LOS than the non-VTE group (hospital LOS 12.2 days vs. 8.8 days, p < 0.001; ICU LOS 3.8 days vs. 1.9 days, p < 0.001). 9.8% of patients in the VTE group required more advanced oxygen support, compared to 2.7% of patients in the non-VTE group (p < 0.001). Among all four models, the random forest model had the best performance. The model suggested that blood pressure, electrolytes, renal function, hepatic enzymes, and inflammatory markers were predictors for in-hospital VTE in COVID-19 patients.

Conclusions

Patients with COVID-19 have a high risk for VTE, and patients who developed VTE had a prolonged hospital and ICU stay. This random forest prediction model for VTE in COVID-19 patients identifies predictors which could aid physicians in making a clinical judgment on empirical dosages of anticoagulation.
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Literature
2.
go back to reference Lodigiani C, Iapichino G, Carenzo L, Cecconi M, Ferrazzi P, Sebastian T, Kucher N, Studt JD, Sacco C, Bertuzzi A, 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.CrossRef Lodigiani C, Iapichino G, Carenzo L, Cecconi M, Ferrazzi P, Sebastian T, Kucher N, Studt JD, Sacco C, Bertuzzi A, 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.CrossRef
3.
go back to reference Levi M, Thachil J, Iba T, Levy JH. Coagulation abnormalities and thrombosis in patients with COVID-19. Lancet Haematol. 2020;7(6):e438–40.CrossRef Levi M, Thachil J, Iba T, Levy JH. Coagulation abnormalities and thrombosis in patients with COVID-19. Lancet Haematol. 2020;7(6):e438–40.CrossRef
4.
go back to reference Kunutsor SK, Laukkanen JA. Incidence of venous and arterial thromboembolic complications in COVID-19: a systematic review and meta-analysis. Thromb Res. 2020;196:27–30.CrossRef Kunutsor SK, Laukkanen JA. Incidence of venous and arterial thromboembolic complications in COVID-19: a systematic review and meta-analysis. Thromb Res. 2020;196:27–30.CrossRef
5.
go back to reference Paranjpe I, Fuster V, Lala A, Russak AJ, Glicksberg BS, Levin MA, Charney AW, Narula J, Fayad ZA, Bagiella E, et al. Association of treatment dose anticoagulation with in-hospital survival among hospitalized patients with COVID-19. J Am Coll Cardiol. 2020;76(1):122–4.CrossRef Paranjpe I, Fuster V, Lala A, Russak AJ, Glicksberg BS, Levin MA, Charney AW, Narula J, Fayad ZA, Bagiella E, et al. Association of treatment dose anticoagulation with in-hospital survival among hospitalized patients with COVID-19. J Am Coll Cardiol. 2020;76(1):122–4.CrossRef
6.
go back to reference Wichmann D, Sperhake JP, Lutgehetmann M, Steurer S, Edler C, Heinemann A, Heinrich F, Mushumba H, Kniep I, Schroder AS et al. Autopsy findings and venous thromboembolism in patients with COVID-19. Ann Internal Med. 2020;173(4):268–277. Wichmann D, Sperhake JP, Lutgehetmann M, Steurer S, Edler C, Heinemann A, Heinrich F, Mushumba H, Kniep I, Schroder AS et al. Autopsy findings and venous thromboembolism in patients with COVID-19. Ann Internal Med. 2020;173(4):268–277.
7.
go back to reference Wiersinga WJ, Rhodes A, Cheng AC, Peacock SJ, Prescott HC. Pathophysiology, transmission, diagnosis, and treatment of Coronavirus disease 2019 (COVID-19): a review. JAMA. 2020;324(8):782–93.CrossRef Wiersinga WJ, Rhodes A, Cheng AC, Peacock SJ, Prescott HC. Pathophysiology, transmission, diagnosis, and treatment of Coronavirus disease 2019 (COVID-19): a review. JAMA. 2020;324(8):782–93.CrossRef
8.
go back to reference Ackermann M, Verleden SE, Kuehnel M, Haverich A, Welte T, Laenger F, Vanstapel A, Werlein C, Stark H, Tzankov A, et al. Pulmonary vascular endothelialitis, thrombosis, and angiogenesis in COVID-19. N Engl J Med. 2020;383(2):120–8.CrossRef Ackermann M, Verleden SE, Kuehnel M, Haverich A, Welte T, Laenger F, Vanstapel A, Werlein C, Stark H, Tzankov A, et al. Pulmonary vascular endothelialitis, thrombosis, and angiogenesis in COVID-19. N Engl J Med. 2020;383(2):120–8.CrossRef
9.
go back to reference Li A, Kuderer NM, Hsu C-Y, Shyr Y, Warner JL, Shah DP, Kumar V, Shah S, Kulkarni AA, Fu J, et al. The COVID-TE risk assessment model for venous thromboembolism in hospitalized patients with cancer and COVID-19. J Thromb Haemost. 2021;19(10):2522–32.CrossRef Li A, Kuderer NM, Hsu C-Y, Shyr Y, Warner JL, Shah DP, Kumar V, Shah S, Kulkarni AA, Fu J, et al. The COVID-TE risk assessment model for venous thromboembolism in hospitalized patients with cancer and COVID-19. J Thromb Haemost. 2021;19(10):2522–32.CrossRef
10.
go back to reference Zhou F, Yu T, Du R, Fan G, Liu Y, Liu Z, Xiang J, Wang Y, Song B, Gu X, et al. Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study. Lancet. 2020;395(10229):1054–62.CrossRef Zhou F, Yu T, Du R, Fan G, Liu Y, Liu Z, Xiang J, Wang Y, Song B, Gu X, et al. Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study. Lancet. 2020;395(10229):1054–62.CrossRef
11.
go back to reference Yan L, Zhang H-T, Goncalves J, Xiao Y, Wang M, Guo Y, Sun C, Tang X, Jin L, Zhang M et al. A machine learning-based model for survival prediction in patients with severe COVID-19 infection. medRxiv. 2020:2020.2002.2027.20028027. Yan L, Zhang H-T, Goncalves J, Xiao Y, Wang M, Guo Y, Sun C, Tang X, Jin L, Zhang M et al. A machine learning-based model for survival prediction in patients with severe COVID-19 infection. medRxiv. 2020:2020.2002.2027.20028027.
12.
go back to reference Wynants L, Van Calster B, Collins GS, Riley RD, Heinze G, Schuit E, Bonten MMJ, Dahly DL, Damen JA, Debray TPA, et al. Prediction models for diagnosis and prognosis of COVID-19: systematic review and critical appraisal. BMJ. 2020;369: m1328.CrossRef Wynants L, Van Calster B, Collins GS, Riley RD, Heinze G, Schuit E, Bonten MMJ, Dahly DL, Damen JA, Debray TPA, et al. Prediction models for diagnosis and prognosis of COVID-19: systematic review and critical appraisal. BMJ. 2020;369: m1328.CrossRef
13.
go back to reference Hu H, Yao N, Qiu Y. Comparing rapid scoring systems in mortality prediction of critically ill patients with novel Coronavirus disease. Acad Emerg Med. 2020;27(6):461–8.CrossRef Hu H, Yao N, Qiu Y. Comparing rapid scoring systems in mortality prediction of critically ill patients with novel Coronavirus disease. Acad Emerg Med. 2020;27(6):461–8.CrossRef
14.
go back to reference Vaid A, Somani S, Russak AJ, De Freitas JK, Chaudhry FF, Paranjpe I, Johnson KW, Lee SJ, Miotto R, Zhao S et al. Machine learning to predict mortality and critical events in COVID-19 positive New York City patients. medRxiv. 2020:2020.2004.2026.20073411. Vaid A, Somani S, Russak AJ, De Freitas JK, Chaudhry FF, Paranjpe I, Johnson KW, Lee SJ, Miotto R, Zhao S et al. Machine learning to predict mortality and critical events in COVID-19 positive New York City patients. medRxiv. 2020:2020.2004.2026.20073411.
16.
go back to reference Investigators I. Effect of intermediate-dose vs standard-dose prophylactic anticoagulation on thrombotic events, extracorporeal membrane oxygenation treatment, or mortality among patients with COVID-19 admitted to the intensive care unit: the INSPIRATION randomized clinical trial. JAMA. 2021;325(16):1620–30.CrossRef Investigators I. Effect of intermediate-dose vs standard-dose prophylactic anticoagulation on thrombotic events, extracorporeal membrane oxygenation treatment, or mortality among patients with COVID-19 admitted to the intensive care unit: the INSPIRATION randomized clinical trial. JAMA. 2021;325(16):1620–30.CrossRef
17.
go back to reference Moores LK, Tritschler T, Brosnahan S, Carrier M, Collen JF, Doerschug K, Holley AB, Jimenez D, Le Gal G, Rali P, et al. Prevention, diagnosis, and treatment of VTE in patients with coronavirus disease 2019: CHEST guideline and expert panel report. Chest. 2020;158(3):1143–63.CrossRef Moores LK, Tritschler T, Brosnahan S, Carrier M, Collen JF, Doerschug K, Holley AB, Jimenez D, Le Gal G, Rali P, et al. Prevention, diagnosis, and treatment of VTE in patients with coronavirus disease 2019: CHEST guideline and expert panel report. Chest. 2020;158(3):1143–63.CrossRef
18.
go back to reference Jehangir Q, Lee Y, Latack K, Poisson L, Wang DD, Song S, Apala DR, Patel K, Halabi AR, Krishnamoorthy G, et al. Incidence, Mortality, and imaging outcomes of atrial arrhythmias in COVID-19. Am J Cardiol. 2022;S0002-9149(22)00243-0. Jehangir Q, Lee Y, Latack K, Poisson L, Wang DD, Song S, Apala DR, Patel K, Halabi AR, Krishnamoorthy G, et al. Incidence, Mortality, and imaging outcomes of atrial arrhythmias in COVID-19. Am J Cardiol. 2022;S0002-9149(22)00243-0.
19.
go back to reference Klok FA, Kruip M, van der Meer NJM, Arbous MS, Gommers D, Kant KM, Kaptein FHJ, van Paassen J, Stals MAM, Huisman MV, et al. Incidence of thrombotic complications in critically ill ICU patients with COVID-19. Thromb Res. 2020;191:145–7.CrossRef Klok FA, Kruip M, van der Meer NJM, Arbous MS, Gommers D, Kant KM, Kaptein FHJ, van Paassen J, Stals MAM, Huisman MV, et al. Incidence of thrombotic complications in critically ill ICU patients with COVID-19. Thromb Res. 2020;191:145–7.CrossRef
20.
go back to reference Klok FA, Kruip M, van der Meer NJM, Arbous MS, Gommers D, Kant KM, Kaptein FHJ, van Paassen J, Stals MAM, Huisman MV, et al. Confirmation of the high cumulative incidence of thrombotic complications in critically ill ICU patients with COVID-19: an updated analysis. Thromb Res. 2020;191:148–50.CrossRef Klok FA, Kruip M, van der Meer NJM, Arbous MS, Gommers D, Kant KM, Kaptein FHJ, van Paassen J, Stals MAM, Huisman MV, et al. Confirmation of the high cumulative incidence of thrombotic complications in critically ill ICU patients with COVID-19: an updated analysis. Thromb Res. 2020;191:148–50.CrossRef
21.
go back to reference Llitjos JF, Leclerc M, Chochois C, Monsallier JM, Ramakers M, Auvray M, Merouani K. High incidence of venous thromboembolic events in anticoagulated severe COVID-19 patients. J Thromb Haemost. 2020;18(7):1743–6.CrossRef Llitjos JF, Leclerc M, Chochois C, Monsallier JM, Ramakers M, Auvray M, Merouani K. High incidence of venous thromboembolic events in anticoagulated severe COVID-19 patients. J Thromb Haemost. 2020;18(7):1743–6.CrossRef
22.
go back to reference Investigators A, Investigators AC-a, Investigators R-C, Lawler PR, Goligher EC, Berger JS, Neal MD, McVerry BJ, Nicolau JC, Gong MN, et al. Therapeutic anticoagulation with heparin in noncritically ill patients with COVID-19. N Engl J Med. 2021;385(9):790–802. Investigators A, Investigators AC-a, Investigators R-C, Lawler PR, Goligher EC, Berger JS, Neal MD, McVerry BJ, Nicolau JC, Gong MN, et al. Therapeutic anticoagulation with heparin in noncritically ill patients with COVID-19. N Engl J Med. 2021;385(9):790–802.
23.
go back to reference Iftimie S, López-Azcona AF, Vallverdú I, Hernández-Flix S, de Febrer G, Parra S, Hernández-Aguilera A, Riu F, Joven J, Andreychuk N, et al. First and second waves of coronavirus disease-19: a comparative study in hospitalized patients in Reus, Spain. PLoS ONE. 2021;16(3): e0248029.CrossRef Iftimie S, López-Azcona AF, Vallverdú I, Hernández-Flix S, de Febrer G, Parra S, Hernández-Aguilera A, Riu F, Joven J, Andreychuk N, et al. First and second waves of coronavirus disease-19: a comparative study in hospitalized patients in Reus, Spain. PLoS ONE. 2021;16(3): e0248029.CrossRef
24.
go back to reference Cohen SL, Gianos E, Barish MA, Chatterjee S, Kohn N, Lesser M, Giannis D, Coppa K, Hirsch JS, McGinn TG, et al. Prevalence and predictors of venous thromboembolism or mortality in hospitalized COVID-19 patients. Thromb Haemost. 2021;121(8):1043–53.CrossRef Cohen SL, Gianos E, Barish MA, Chatterjee S, Kohn N, Lesser M, Giannis D, Coppa K, Hirsch JS, McGinn TG, et al. Prevalence and predictors of venous thromboembolism or mortality in hospitalized COVID-19 patients. Thromb Haemost. 2021;121(8):1043–53.CrossRef
25.
go back to reference Dalager-Pedersen M, Lund LC, Mariager T, Winther R, Hellfritzsch M, Larsen TB, Thomsen RW, Johansen NB, Sogaard OS, Nielsen SL, et al. Venous thromboembolism and major bleeding in patients with Coronavirus Disease 2019 (COVID-19): a nationwide population-based cohort study. Clin Infect Dis. 2021;73(12):2283–93.CrossRef Dalager-Pedersen M, Lund LC, Mariager T, Winther R, Hellfritzsch M, Larsen TB, Thomsen RW, Johansen NB, Sogaard OS, Nielsen SL, et al. Venous thromboembolism and major bleeding in patients with Coronavirus Disease 2019 (COVID-19): a nationwide population-based cohort study. Clin Infect Dis. 2021;73(12):2283–93.CrossRef
26.
go back to reference Freund Y, Drogrey M, Miro O, Marra A, Feral-Pierssens AL, Penaloza A, Hernandez BAL, Beaune S, Gorlicki J, Vaittinada Ayar P, et al. Association between pulmonary embolism and COVID-19 in emergency department patients undergoing computed tomography pulmonary angiogram: the PEPCOV international retrospective study. Acad Emerg Med. 2020;27(9):811–20.CrossRef Freund Y, Drogrey M, Miro O, Marra A, Feral-Pierssens AL, Penaloza A, Hernandez BAL, Beaune S, Gorlicki J, Vaittinada Ayar P, et al. Association between pulmonary embolism and COVID-19 in emergency department patients undergoing computed tomography pulmonary angiogram: the PEPCOV international retrospective study. Acad Emerg Med. 2020;27(9):811–20.CrossRef
27.
go back to reference Mei F, Fan J, Yuan J, Liang Z, Wang K, Sun J, Guan W, Huang M, Li Y, Zhang WW. Comparison of venous thromboembolism risks between COVID-19 pneumonia and community-acquired pneumonia patients. Arterioscler Thromb Vasc Biol. 2020;40(9):2332–7.CrossRef Mei F, Fan J, Yuan J, Liang Z, Wang K, Sun J, Guan W, Huang M, Li Y, Zhang WW. Comparison of venous thromboembolism risks between COVID-19 pneumonia and community-acquired pneumonia patients. Arterioscler Thromb Vasc Biol. 2020;40(9):2332–7.CrossRef
28.
go back to reference Poissy J, Goutay J, Caplan M, Parmentier E, Duburcq T, Lassalle F, Jeanpierre E, Rauch A, Labreuche J, Susen S, et al. Pulmonary embolism in patients with COVID-19: awareness of an increased prevalence. Circulation. 2020;142(2):184–6.CrossRef Poissy J, Goutay J, Caplan M, Parmentier E, Duburcq T, Lassalle F, Jeanpierre E, Rauch A, Labreuche J, Susen S, et al. Pulmonary embolism in patients with COVID-19: awareness of an increased prevalence. Circulation. 2020;142(2):184–6.CrossRef
29.
go back to reference Rieder M, Goller I, Jeserich M, Baldus N, Pollmeier L, Wirth L, Supady A, Bode C, Busch HJ, Schmid B, et al. Rate of venous thromboembolism in a prospective all-comers cohort with COVID-19. J Thromb Thrombolysis. 2020;50(3):558–66.CrossRef Rieder M, Goller I, Jeserich M, Baldus N, Pollmeier L, Wirth L, Supady A, Bode C, Busch HJ, Schmid B, et al. Rate of venous thromboembolism in a prospective all-comers cohort with COVID-19. J Thromb Thrombolysis. 2020;50(3):558–66.CrossRef
30.
go back to reference Sabaka P, Koščálová A, Straka I, Hodosy J, Lipták R, Kmotorková B, Kachlíková M, Kušnírová A. Role of interleukin 6 as a predictive factor for a severe course of COVID-19: retrospective data analysis of patients from a long-term care facility during COVID-19 outbreak. BMC Infect Dis. 2021;21(1):308.CrossRef Sabaka P, Koščálová A, Straka I, Hodosy J, Lipták R, Kmotorková B, Kachlíková M, Kušnírová A. Role of interleukin 6 as a predictive factor for a severe course of COVID-19: retrospective data analysis of patients from a long-term care facility during COVID-19 outbreak. BMC Infect Dis. 2021;21(1):308.CrossRef
31.
go back to reference Kampouri E, Filippidis P, Viala B, Mean M, Pantet O, Desgranges F, Tschopp J, Regina J, Karachalias E, Bianchi C, et al. Predicting venous thromboembolic events in patients with Coronavirus Disease 2019 Requiring hospitalization: an observational retrospective study by the COVIDIC initiative in a Swiss university hospital. Biomed Res Int. 2020;2020:9126148.CrossRef Kampouri E, Filippidis P, Viala B, Mean M, Pantet O, Desgranges F, Tschopp J, Regina J, Karachalias E, Bianchi C, et al. Predicting venous thromboembolic events in patients with Coronavirus Disease 2019 Requiring hospitalization: an observational retrospective study by the COVIDIC initiative in a Swiss university hospital. Biomed Res Int. 2020;2020:9126148.CrossRef
32.
go back to reference Dujardin RWG, Hilderink BN, Haksteen WE, Middeldorp S, Vlaar APJ, Thachil J, Müller MCA, Juffermans NP. Biomarkers for the prediction of venous thromboembolism in critically ill COVID-19 patients. Thromb Res. 2020;196:308–12.CrossRef Dujardin RWG, Hilderink BN, Haksteen WE, Middeldorp S, Vlaar APJ, Thachil J, Müller MCA, Juffermans NP. Biomarkers for the prediction of venous thromboembolism in critically ill COVID-19 patients. Thromb Res. 2020;196:308–12.CrossRef
33.
go back to reference Tsaplin S, Schastlivtsev I, Zhuravlev S, Barinov V, Lobastov K, Caprini JA. The original and modified Caprini score equally predicts venous thromboembolism in COVID-19 patients. J Vasc Surg Venous Lymphat Disord. 2021;9(6):1371–81.CrossRef Tsaplin S, Schastlivtsev I, Zhuravlev S, Barinov V, Lobastov K, Caprini JA. The original and modified Caprini score equally predicts venous thromboembolism in COVID-19 patients. J Vasc Surg Venous Lymphat Disord. 2021;9(6):1371–81.CrossRef
34.
go back to reference Spyropoulos AC, Cohen SL, Gianos E, Kohn N, Giannis D, Chatterjee S, Goldin M, Lesser M, Coppa K, Hirsch JS, et al. Validation of the IMPROVE-DD risk assessment model for venous thromboembolism among hospitalized patients with COVID-19. Res Pract Thromb Haemost. 2021;5(2):296–300.CrossRef Spyropoulos AC, Cohen SL, Gianos E, Kohn N, Giannis D, Chatterjee S, Goldin M, Lesser M, Coppa K, Hirsch JS, et al. Validation of the IMPROVE-DD risk assessment model for venous thromboembolism among hospitalized patients with COVID-19. Res Pract Thromb Haemost. 2021;5(2):296–300.CrossRef
35.
go back to reference Kollias A, Kyriakoulis KG, Lagou S, Kontopantelis E, Stergiou GS, Syrigos K. Venous thromboembolism in COVID-19: a systematic review and meta-analysis. Vasc Med. 2021;26(4):415–25.CrossRef Kollias A, Kyriakoulis KG, Lagou S, Kontopantelis E, Stergiou GS, Syrigos K. Venous thromboembolism in COVID-19: a systematic review and meta-analysis. Vasc Med. 2021;26(4):415–25.CrossRef
36.
go back to reference Cuker A, Tseng EK, Nieuwlaat R, Angchaisuksiri P, Blair C, Dane K, Davila J, DeSancho MT, Diuguid D, Griffin DO, et al. American Society of Hematology 2021 guidelines on the use of anticoagulation for thromboprophylaxis in patients with COVID-19. Blood Adv. 2021;5(3):872–88.CrossRef Cuker A, Tseng EK, Nieuwlaat R, Angchaisuksiri P, Blair C, Dane K, Davila J, DeSancho MT, Diuguid D, Griffin DO, et al. American Society of Hematology 2021 guidelines on the use of anticoagulation for thromboprophylaxis in patients with COVID-19. Blood Adv. 2021;5(3):872–88.CrossRef
37.
go back to reference Vaughn VM, Yost M, Abshire C, Flanders SA, Paje D, Grant P, Kaatz S, Kim T, Barnes GD. Trends in venous thromboembolism anticoagulation in patients hospitalized with COVID-19. JAMA Netw Open. 2021;4(6):e2111788–e2111788.CrossRef Vaughn VM, Yost M, Abshire C, Flanders SA, Paje D, Grant P, Kaatz S, Kim T, Barnes GD. Trends in venous thromboembolism anticoagulation in patients hospitalized with COVID-19. JAMA Netw Open. 2021;4(6):e2111788–e2111788.CrossRef
38.
go back to reference Investigators A, Investigators AC-a, Investigators R-C, Lawler PR, Goligher EC, Berger JS, Neal MD, McVerry BJ, Nicolau JC, Gong MN, et al. Therapeutic anticoagulation with heparin in noncritically ill patients with COVID-19. N Engl J Med. 2021;385(9):790–802.CrossRef Investigators A, Investigators AC-a, Investigators R-C, Lawler PR, Goligher EC, Berger JS, Neal MD, McVerry BJ, Nicolau JC, Gong MN, et al. Therapeutic anticoagulation with heparin in noncritically ill patients with COVID-19. N Engl J Med. 2021;385(9):790–802.CrossRef
39.
go back to reference Investigators R-C, Investigators AC-a, Investigators A, Goligher EC, Bradbury CA, McVerry BJ, Lawler PR, Berger JS, Gong MN, Carrier M, et al. Therapeutic anticoagulation with heparin in critically ill patients with COVID-19. N Engl J Med. 2021;385(9):777–89.CrossRef Investigators R-C, Investigators AC-a, Investigators A, Goligher EC, Bradbury CA, McVerry BJ, Lawler PR, Berger JS, Gong MN, Carrier M, et al. Therapeutic anticoagulation with heparin in critically ill patients with COVID-19. N Engl J Med. 2021;385(9):777–89.CrossRef
Metadata
Title
Venous thromboembolism in COVID-19 patients and prediction model: a multicenter cohort study
Authors
Yi Lee
Qasim Jehangir
Pin Li
Deepthi Gudimella
Pooja Mahale
Chun-Hui Lin
Dinesh R. Apala
Geetha Krishnamoorthy
Abdul R. Halabi
Kiritkumar Patel
Laila Poisson
Venugopal Balijepally
Anupam A. Sule
Girish B. Nair
Publication date
01-12-2022
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2022
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-022-07421-3

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