Review Article

Prevalence of Thromboembolic Events, Including Venous Thromboembolism and Arterial Thrombosis, in Patients with COVID-19: A Systematic Review with Meta-Analysis

Abstract

Background: Many studies have evaluated thromboembolic events in COVID-19 patients, and most of them have reported a high estimation of the prevalence of such events. The present study sought to evaluate the prevalence of thromboembolic events in patients with COVID-19.
Methods: This study is a systematic review with meta-analysis that investigated thromboembolic events in patients with COVID-19 from the start of the pandemic to August 31, 2021. The 4 main databases for collecting articles were Medline, Scopus, Google Scholar, and Web of Science. Deep vein thrombosis, pulmonary embolism, arterial thrombosis, and the overall rate of thromboembolic events were considered primary outcomes.
Results: In a total of 63 studies (104 920 patients with COVID-19), the overall thrombosis rate was 21% (95% CI, 18% to 25%), the rate of deep vein thrombosis was 20% (95% Cl, 16% to 25%), the rate of pulmonary embolism was 8% (95% Cl, 6% to 10%), and the rate of arterial thrombosis was 5% (95% Cl, 3% to 7%). The prevalence of all primary outcomes in critically ill patients admitted to the intensive care unit (ICU) was significantly higher (P<0.05). In older patients, the prevalence of overall thrombosis, pulmonary embolism, or deep vein thrombosis was significantly higher (P<0.05).
Conclusion: This study showed that COVID-19 increases the risk of thromboembolic events, especially in elderly and critically ill patients admitted to the ICU. Therefore, more strategies are needed to prevent thromboembolic events in patients with COVID-19, especially in ICU-admitted and elderly patients.

1. Firouzi A, Hosseini Z, Norouzi Z, Hosseini Z, Amirpour A, Talakoob H, et al. The Pragmatic Role of COVID-19 on the Thrombus Grade of Patients with Contemporary ST-Segment-Elevation Myocardial Infarction. J Tehran Heart Cent 2022;17:103-111.
2. Lai CC, Liu YH, Wang CY, Wang YH, Hsueh SC, Yen MY, Ko WC, Hsueh PR. Asymptomatic carrier state, acute respiratory disease, and pneumonia due to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2): Facts and myths. J Microbiol Immunol Infect 2020;53:404-412.
3. Mehta JL, Calcaterra G, Bassareo PP. COVID-19, thromboembolic risk, and Virchow's triad: Lesson from the past. Clin Cardiol 2020;43:1362-1367.
4. Ren B, Yan F, Deng Z, Zhang S, Xiao L, Wu M, Cai L. Extremely High Incidence of Lower Extremity Deep Venous Thrombosis in 48 Patients With Severe COVID-19 in Wuhan. Circulation 2020;142:181-183.
5. Moher D, Liberati A, Tetzlaff J, Altman DG; PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 2009;6:e1000097.
6. Motaganahalli RL, Kapoor R, Timsina LR, Gutwein AR, Ingram MD, Raman S, Roberts SD, Rahman O, Rollins D, Dalsing MC. Clinical and laboratory characteristics of patients with novel coronavirus disease-2019 infection and deep venous thrombosis. J Vasc Surg Venous Lymphat Disord 2021;9:605-614.e2.
7. Zhang Y, Cao W, Jiang W, Xiao M, Li Y, Tang N, Liu Z, Yan X, Zhao Y, Li T, Zhu T. Profile of natural anticoagulant, coagulant factor and anti-phospholipid antibody in critically ill COVID-19 patients. J Thromb Thrombolysis 2020;50:580-586.
8. Monfardini L, Morassi M, Botti P, Stellini R, Bettari L, Pezzotti S, Alì M, Monaco CG, Magni V, Cozzi A, Schiaffino S, Bnà C. Pulmonary thromboembolism in hospitalised COVID-19 patients at moderate to high risk by Wells score: a report from Lombardy, Italy. Br J Radiol 2020;93:20200407.
9. Zhang L, Feng X, Zhang D, Jiang C, Mei H, Wang J, et al. Deep Vein Thrombosis in Hospitalized Patients With COVID-19 in Wuhan, China: Prevalence, Risk Factors, and Outcome. Circulation 2020;142:114-128.
10. Stoneham SM, Milne KM, Nuttall E, Frew GH, Sturrock BR, Sivaloganathan H, Ladikou EE, Drage S, Phillips B, Chevassut TJ, Eziefula AC. Thrombotic risk in COVID-19: a case series and case-control study. Clin Med (Lond) 2020;20:e76-e81.
11. Stefely JA, Christensen BB, Gogakos T, Cone Sullivan JK, Montgomery GG, Barranco JP, Van Cott EM. Marked factor V activity elevation in severe COVID-19 is associated with venous thromboembolism. Am J Hematol 2020;95:1522-1530.
12. Roberts LN, Whyte MB, Georgiou L, Giron G, Czuprynska J, Rea C, Vadher B, Patel RK, Gee E, Arya R. Postdischarge venous thromboembolism following hospital admission with COVID-19. Blood 2020;136:1347-1350.
13. Rieder M, Goller I, Jeserich M, Baldus N, Pollmeier L, Wirth L, Supady A, Bode C, Busch HJ, Schmid B, Duerschmied D, Gauchel N, Lother A. Rate of venous thromboembolism in a prospective all-comers cohort with COVID-19. J Thromb Thrombolysis 2020;50:558-566.
14. Piazza G, Campia U, Hurwitz S, Snyder JE, Rizzo SM, Pfeferman MB, Morrison RB, Leiva O, Fanikos J, Nauffal V, Almarzooq Z, Goldhaber SZ. Registry of Arterial and Venous Thromboembolic Complications in Patients With COVID-19. J Am Coll Cardiol 2020;76:2060-2072.
15. Patell R, Bogue T, Koshy A, Bindal P, Merrill M, Aird WC, Bauer KA, Zwicker JI. Postdischarge thrombosis and hemorrhage in patients with COVID-19. Blood 2020;136:1342-1346.
16. Betoule A, Martinet C, Gasperini G, Muller P, Foucher S, Benner P, Renard A. Diagnosis of venous and arterial thromboembolic events in COVID-19 virus-infected patients. J Thromb Thrombolysis 2020;50:302-304.
17. Middeldorp S, Coppens M, van Haaps TF, Foppen M, Vlaar AP, Müller MCA, Bouman CCS, Beenen LFM, Kootte RS, Heijmans J, Smits LP, Bonta PI, van Es N. Incidence of venous thromboembolism in hospitalized patients with COVID-19. J Thromb Haemost 2020;18:1995-2002.
18. Medetalibeyoglu A, Emet S, Senkal N, Aydogan M, Kose M, Tukek T. Cardiovascular view of intermediate and high-risk COVID-19 patients: single-centre experience with low mortality and intensive care hospitalisation rates. Cardiovasc J Afr 2021;32:79-86.
19. Lodigiani C, Iapichino G, Carenzo L, Cecconi M, Ferrazzi P, Sebastian T, Kucher N, Studt JD, Sacco C, Bertuzzi A, Sandri MT, Barco S; Humanitas COVID-19 Task Force. Venous and arterial thromboembolic complications in COVID-19 patients admitted to an academic hospital in Milan, Italy. Thromb Res 2020;191:9-14.
20. 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;18:1743-1746.
21. Kapoor S, Chand S, Dieiev V, Fazzari M, Tanner T, Lewandowski DC, Nalla A, Abdulfattah O, Aboodi MS, Shiloh AL, Gong MN. Thromboembolic Events and Role of Point of Care Ultrasound in Hospitalized Covid-19 Patients Needing Intensive Care Unit Admission. J Intensive Care Med 2021;36:1483-1490.
22. Inciardi RM, Adamo M, Lupi L, Cani DS, Di Pasquale M, Tomasoni D, et al. Characteristics and outcomes of patients hospitalized for COVID-19 and cardiac disease in Northern Italy. Eur Heart J 2020;41:1821-1829.
23. Ierardi AM, Coppola A, Fusco S, Stellato E, Aliberti S, Andrisani MC, et al. Early detection of deep vein thrombosis in patients with coronavirus disease 2019: who to screen and who not to with Doppler ultrasound? J Ultrasound 2021;24:165-173.
24. Le Jeune S, Suhl J, Benainous R, Minvielle F, Purser C, Foudi F, Warzocha U, Dhote R. High prevalence of early asymptomatic venous thromboembolism in anticoagulated COVID-19 patients hospitalized in general wards. J Thromb Thrombolysis 2021;51:637-641.
25. 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;4:842-847.
26. Helms J, Tacquard C, Severac F, Leonard-Lorant I, Ohana M, Delabranche X, et al. High risk of thrombosis in patients with severe SARS-CoV-2 infection: a multicenter prospective cohort study. Intensive Care Med.2020;46:1089-1098.
27. Hanif A, Khan S, Mantri N, Hanif S, Saleh M, Alla Y, Chinta S, Shrestha N, Ji W, Attwood K, Adrish M, Jain KR. Thrombotic complications and anticoagulation in COVID-19 pneumonia: a New York City hospital experience. Ann Hematol 2020;99:2323-2328.
28. Tan CW, Fan BE, Teo WZY, Tung ML, Shafi H, Christopher D, et al. Low incidence of venous thrombosis but high incidence of arterial thrombotic complications among critically ill COVID-19 patients in Singapore. Thromb J 2021;19:14.
29. Edler C, Schröder AS, Aepfelbacher M, Fitzek A, Heinemann A, Heinrich F, Klein A, Langenwalder F, Lütgehetmann M, Meißner K, Püschel K, Schädler J, Steurer S, Mushumba H, Sperhake JP. Dying with SARS-CoV-2 infection-an autopsy study of the first consecutive 80 cases in Hamburg, Germany. Int J Legal Med 2020;134:1275-1284.
30. Demelo-Rodríguez P, Cervilla-Muñoz E, Ordieres-Ortega L, Parra-Virto A, Toledano-Macías M, Toledo-Samaniego N, García-García A, García-Fernández-Bravo I, Ji Z, de-Miguel-Diez J, Álvarez-Sala-Walther LA, Del-Toro-Cervera J, Galeano-Valle F. Incidence of asymptomatic deep vein thrombosis in patients with COVID-19 pneumonia and elevated D-dimer levels. Thromb Res 2020;192:23-26.
31. 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;18:1421-1424.
32. Contou D, Pajot O, Cally R, Logre E, Fraissé M, Mentec H, Plantefève G. Pulmonary embolism or thrombosis in ARDS COVID-19 patients: A French monocenter retrospective study. PLoS One 2020;15:e0238413.
33. Chen S, Zhang D, Zheng T, Yu Y, Jiang J. DVT incidence and risk factors in critically ill patients with COVID-19. J Thromb Thrombolysis 2021;51:33-39.
34. Artifoni M, Danic G, Gautier G, Gicquel P, Boutoille D, Raffi F, Néel A, Lecomte R. Systematic assessment of venous thromboembolism in COVID-19 patients receiving thromboprophylaxis: incidence and role of D-dimer as predictive factors. J Thromb Thrombolysis 2020;50:211-216.
35. Chang H, Rockman CB, Jacobowitz GR, Speranza G, Johnson WS, Horowitz JM, Garg K, Maldonado TS, Sadek M, Barfield ME. Deep vein thrombosis in hospitalized patients with coronavirus disease 2019. J Vasc Surg Venous Lymphat Disord 2021;9:597-604.
36. Voicu S, Delrue M, Chousterman BG, Stépanian A, Bonnin P, Malissin I, Deye N, Neuwirth M, Ketfi C, Mebazaa A, Siguret V, Mégarbane B. Imbalance between procoagulant factors and natural coagulation inhibitors contributes to hypercoagulability in the critically ill COVID-19 patient: clinical implications. Eur Rev Med Pharmacol Sci 2020;24:9161-9168.
37. Longhitano Y, Racca F, Zanza C, Piccioni A, Audo A, Muncinelli M, Santi R, Kozel D, Geraci C, Taverna M, Bonato V, Cassini F, Franceschi F. Venous thromboembolism in critically ill patients affected by ARDS related to COVID-19 in Northern-West Italy. Eur Rev Med Pharmacol Sci 2020;24:9154-9160.
38. Cho ES, McClelland PH, Cheng O, Kim Y, Hu J, Zenilman ME, D'Ayala M. Utility of d-dimer for diagnosis of deep vein thrombosis in coronavirus disease-19 infection. J Vasc Surg Venous Lymphat Disord 2021;9:47-53.
39. Thondapu V, Montes D, Rosovsky R, Dua A, McDermott S, Lu MT, Ghoshhajra B, Hoffmann U, Gerhard-Herman MD, Hedgire S. Venous thrombosis, thromboembolism, biomarkers of inflammation, and coagulation in coronavirus disease 2019. J Vasc Surg Venous Lymphat Disord 2021;9:835-844.e4.
40. Muñoz-Rivas N, Abad-Motos A, Mestre-Gómez B, Sierra-Hidalgo F, Cortina-Camarero C, Lorente-Ramos RM, et al. Systemic thrombosis in a large cohort of COVID-19 patients despite thromboprophylaxis: A retrospective study. Thromb Res 2021;199:132-142.
41. Koleilat I, Galen B, Choinski K, Hatch AN, Jones DB, Billett H, Indes J, Lipsitz E. Clinical characteristics of acute lower extremity deep venous thrombosis diagnosed by duplex in patients hospitalized for coronavirus disease 2019. J Vasc Surg Venous Lymphat Disord 2021;9:36-46.
42. Alfageme M, González Plaza J, Méndez S, Gómez Patiño JA, Collado ML, Abadal JM, González Costero R, Fontanilla T, García Suárez A. Venous Doppler ultrasound in critically Ill COVID-19 patients: game changer in anticoagulation therapy. Ultrasound J 2020;12:54.
43. Ameri P, Inciardi RM, Di Pasquale M, Agostoni P, Bellasi A, Camporotondo R, et al. Pulmonary embolism in patients with COVID-19: characteristics and outcomes in the Cardio-COVID Italy multicenter study. Clin Res Cardiol 2021;110:1020-1028.
44. Atallah B, Sadik ZG, Salem N, El Nekidy WS, Almahmeed W, Park WM, Cherfan A, Hamed F, Mallat J. The impact of protocol-based high-intensity pharmacological thromboprophylaxis on thrombotic events in critically ill COVID-19 patients. Anaesthesia 2021;76:327-335.
45. Avruscio G, Camporese G, Campello E, Bernardi E, Persona P, Passarella C, Noventa F, Cola M, Navalesi P, Cattelan A, Tiberio I, Boscolo A, Spiezia L, Simioni P; COVID-VTE Study Group. COVID-19 and Venous Thromboembolism in Intensive Care or Medical Ward. Clin Transl Sci 2020;13:1108-1114.
46. Mouhat B, Besutti M, Bouiller K, Grillet F, Monnin C, Ecarnot F, Behr J, Capellier G, Soumagne T, Pili-Floury S, Besch G, Mourey G, Lepiller Q, Chirouze C, Schiele F, Chopard R, Meneveau N. Elevated D-dimers and lack of anticoagulation predict PE in severe COVID-19 patients. Eur Respir J 2020;56:2001811.
47. Rashidi F, Barco S, Kamangar F, Heresi GA, Emadi A, Kaymaz C, et al. Incidence of symptomatic venous thromboembolism following hospitalization for coronavirus disease 2019: Prospective results from a multi-center study. Thromb Res 2021;198:135-138.
48. Kampouri E, Filippidis P, Viala B, Méan M, Pantet O, Desgranges F, Tschopp J, 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.
49. Planquette B, Le Berre A, Khider L, Yannoutsos A, Gendron N, de Torcy M, Mohamedi N, Jouveshomme S, Smadja DM, Lazareth I, Goudot G, Fournier L, Bruel C, Diehl JL, Mourad JJ, Meyer G, Priollet P, Messas E, Sanchez O, Beaussier H, Mirault T, Zins M, Chatelier G, Emmerich J. Prevalence and characteristics of pulmonary embolism in 1042 COVID-19 patients with respiratory symptoms: A nested case-control study. Thromb Res 2021;197:94-99.
50. Kerbikov O, Orekhov P, Borskaya E, Nosenko N. High incidence of venous thrombosis in patients with moderate-to-severe COVID-19. Int J Hematol 2021;113:344-347.
51. Giorgi-Pierfranceschi M, Paoletti O, Pan A, De Gennaro F, Nardecchia AL, Morandini R, Dellanoce C, Lombi S, Tala M, Cancelli V, Zambelli S, Bosio G, Romanini L, Testa S. Prevalence of asymptomatic deep vein thrombosis in patients hospitalized with SARS-CoV-2 pneumonia: a cross-sectional study. Intern Emerg Med 2020;15:1425-1433.
52. Hill JB, Garcia D, Crowther M, Savage B, Peress S, Chang K, Deitelzweig S. Frequency of venous thromboembolism in 6513 patients with COVID-19: a retrospective study. Blood Adv 2020;4:5373-5377.
53. Jonmarker S, Hollenberg J, Dahlberg M, Stackelberg O, Litorell J, Everhov ÅH, Järnbert-Pettersson H, Söderberg M, Grip J, Schandl A, Günther M, Cronhjort M. Dosing of thromboprophylaxis and mortality in critically ill COVID-19 patients. Crit Care 2020;24:653.
54. Daughety MM, Morgan A, Frost E, Kao C, Hwang J, Tobin R, Patel B, Fuller M, Welsby I, Ortel TL. COVID-19 associated coagulopathy: Thrombosis, hemorrhage and mortality rates with an escalated-dose thromboprophylaxis strategy. Thromb Res 2020;196:483-485.
55. Chen S, Zheng T, Wang S, Yu Y, Wang P, Song Y, Jiang J. Association between risk of venous thromboembolism and mortality in patients with COVID-19. Int J Infect Dis 2021;108:543-549.
56. Chen B, Jiang C, Han B, Guan C, Fang G, Yan S, Wang K, Liu L, Conlon CP, Xie R, Song R. High prevalence of occult thrombosis in cases of mild/moderate COVID-19. Int J Infect Dis 2021;104:77-82.
57. Boyd S, Martin-Loeches I. The incidence of venous thromboembolism in critically ill patients with COVID-19 compared with critically ill non-COVID patients. Ir J Med Sci 2021;190:1317-1320.
58. Lee E, Krajewski A, Clarke C, O'Sullivan D, Herbst T, Lee S. Arterial and venous thromboembolic complications of COVID-19 detected by CT angiogram and venous duplex ultrasound. Emerg Radiol 2021;28:469-476.
59. Budimir Mršić D, Perković-Tabak L, Ćavar M, Luetić A, Petričević M, Dolić K. Pulmonary Embolism Associated with COVID-19 Occurs in Predominantly Elderly Patients with Comorbidities: A Single Center Retrospective Study. Gerontol Geriatr Med 2021;7:23337214211017398.
60. Miró Ò, Jiménez S, Mebazaa A, Freund Y, Burillo-Putze G, Martín A, Martín-Sánchez FJ, et al. Pulmonary embolism in patients with COVID-19: incidence, risk factors, clinical characteristics, and outcome. Eur Heart J 2021;42:3127-3142.
61. Calabrese C, Annunziata A, Coppola A, Pafundi PC, Guarino S, Di Spirito V, Maddaloni V, Pepe N, Fiorentino G. ACE Gene I/D Polymorphism and Acute Pulmonary Embolism in COVID19 Pneumonia: A Potential Predisposing Role. Front Med (Lausanne) 2021;7:631148.
62. Taccone FS, Gevenois PA, Peluso L, Pletchette Z, Lheureux O, Brasseur A, Garufi A, Talamonti M, Motte S, Nobile L, Grimaldi D, Creteur J, Vincent JL. Higher Intensity Thromboprophylaxis Regimens and Pulmonary Embolism in Critically Ill Coronavirus Disease 2019 Patients. Crit Care Med 2020;48:e1087-e1090.
63. Faqihi F, Alharthy A, Balhamar A, Nasim N, Alanezi K, Alaklobi F, Memish ZA, Blaivas M, Alqahtani SA, Karakitsos D. A Retrospective Analysis of Thromboembolic Phenomena in Mechanically Ventilated Patients with COVID-19. Crit Care Res Pract 2021;2021:8737580.
64. Hendren NS, de Lemos JA, Ayers C, Das SR, Rao A, Carter S, Rosenblatt A, Walchok J, Omar W, Khera R, Hegde AA, Drazner MH, Neeland IJ, Grodin JL. Association of Body Mass Index and Age With Morbidity and Mortality in Patients Hospitalized With COVID-19: Results From the American Heart Association COVID-19 Cardiovascular Disease Registry. Circulation 2021;143:135-144.
65. Erben Y, Franco-Mesa C, Gloviczki P, Stone W, Quinones-Hinojoas A, Meltzer AJ, et al. Deep vein thrombosis and pulmonary embolism among hospitalized coronavirus disease 2019-positive patients predicted for higher mortality and prolonged intensive care unit and hospital stays in a multisite healthcare system. J Vasc Surg Venous Lymphat Disord 2021;9:1361-1370.e1.
66. Trigonis RA, Holt DB, Yuan R, Siddiqui AA, Craft MK, Khan BA, Kapoor R, Rahman O. Incidence of Venous Thromboembolism in Critically Ill Coronavirus Disease 2019 Patients Receiving Prophylactic Anticoagulation. Crit Care Med 2020;48:e805-e808.
67. Núñez-Gil IJ, Fernández-Ortiz A, Maroud Eid C, Huang J, Romero R, Becerra-Muñoz VM, Uribarri A, Feltes G, Trabatoni D, Fernandez-Rozas I, et al. Underlying heart diseases and acute COVID-19 outcomes. Cardiol J 2021;28:202-214.
68. 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;18:1094-1099.
69. Huang C, Wang Y, Li X, Ren L, Zhao J, Hu Y, Zhang L, Fan G, Xu J, Gu X, Cheng Z, Yu T, Xia J, Wei Y, Wu W, Xie X, Yin W, Li H, Liu M, Xiao Y, Gao H, Guo L, Xie J, Wang G, Jiang R, Gao Z, Jin Q, Wang J, Cao B. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet 2020;395:497-506.
70. Foley JH, Conway EM. Cross Talk Pathways Between Coagulation and Inflammation. Circ Res 2016;118:1392-1408.
71. Joly BS, Siguret V, Veyradier A. Understanding pathophysiology of hemostasis disorders in critically ill patients with COVID-19. Intensive Care Med 2020;46:1603-1606.
72. Cheruiyot I, Kipkorir V, Ngure B, Misiani M, Munguti J, Ogeng'o J. Arterial Thrombosis in Coronavirus Disease 2019 Patients: A Rapid Systematic Review. Ann Vasc Surg 2021;70:273-281.
73. Yu HH, Qin C, Chen M, Wang W, Tian DS. D-dimer level is associated with the severity of COVID-19. Thromb Res 2020;195:219-225.
74. Goldhaber SZ, Piazza G. Pulmonary Embolism and Deep Vein Thrombosis. In: Eugene Braunwald, ed. Braunwald’s Heart Disease: A Textbook of Cardiovascular Medicine. 12th ed. Philadelphia: Elsevier; 2022. p. 1635-1655.
75. Singh R, Rathore SS, Khan H, Karale S, Chawla Y, Iqbal K, Bhurwal A, Tekin A, Jain N, Mehra I, Anand S, Reddy S, Sharma N, Sidhu GS, Panagopoulos A, Pattan V, Kashyap R, Bansal V. Association of Obesity With COVID-19 Severity and Mortality: An Updated Systemic Review, Meta-Analysis, and Meta-Regression. Front Endocrinol (Lausanne) 2022;13:780872.
76. Wang SY, Singh A, Eder MD, Vadlamani L, Lee AI, Chun HJ, Desai NR. Association of obesity with venous thromboembolism and myocardial injury in COVID-19. Obes Res Clin Pract 2021;15:512-514.
77. Ridker PM, Rifai N, Clearfield M, Downs JR, Weis SE, Miles JS, Gotto AM Jr; Air Force/Texas Coronary Atherosclerosis Prevention Study Investigators. Measurement of C-reactive protein for the targeting of statin therapy in the primary prevention of acute coronary events. N Engl J Med 2001;344:1959-1965.
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IssueVol 18 No 3 (2023): J Teh Univ Heart Ctr QRcode
SectionReview Article(s)
DOI https://doi.org/10.18502/jthc.v18i3.14110
Keywords
COVID-19 Venous thromboembolism Pulmonary embolism

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Bagheri B, Alipour A, Yousefi M, Jalalian R, Moghimi M, Mohammadi M, Hassanpour N, Iranian M. Prevalence of Thromboembolic Events, Including Venous Thromboembolism and Arterial Thrombosis, in Patients with COVID-19: A Systematic Review with Meta-Analysis. J Tehran Heart Cent. 2023;18(3):154-169.