Download PDF
Thromb Haemost 2009; 102(06): 1259-1264
DOI: 10.1160/TH09-04-0222
Blood Coagulation, Fibrinolysis and Cellular Haemostasis
Schattauer GmbH

Association of influenza vaccination with reduced risk of venous thromboembolism

Tienan Zhu
1   Department of Vascular Medicine, University Paris Descartes and INSERM U765, Paris, France
,
Laure Carcaillon
1   Department of Vascular Medicine, University Paris Descartes and INSERM U765, Paris, France
,
Isabelle Martinez
1   Department of Vascular Medicine, University Paris Descartes and INSERM U765, Paris, France
,
Jean-Pierre Cambou
1   Department of Vascular Medicine, University Paris Descartes and INSERM U765, Paris, France
,
Xavier Kyndt
1   Department of Vascular Medicine, University Paris Descartes and INSERM U765, Paris, France
,
Karine Guillot
1   Department of Vascular Medicine, University Paris Descartes and INSERM U765, Paris, France
,
Marie-Christine Vergnes
1   Department of Vascular Medicine, University Paris Descartes and INSERM U765, Paris, France
,
Pierre-Yves Scarabin
1   Department of Vascular Medicine, University Paris Descartes and INSERM U765, Paris, France
,
Joseph Emmerich
1   Department of Vascular Medicine, University Paris Descartes and INSERM U765, Paris, France
› Author AffiliationsFinancial support: The FARIVE study was supported by Fondation pour la Recherche Médicale, Programme Hospitalier de Recherche Clinique (PHRC), Fondation de France, and the Leducq Foundation (LINAT Leducq International Network Against Thrombosis).
Further Information

Publication History

Received: 03 April 2009

Accepted after major revision: 21 August 2009

Publication Date:
28 November 2017 (online)

Also available at
    Permissions and Reprints

Summary

Influenza vaccination can reduce the risk of cardiovascular events in patients with coronary heart disease, but its impact on the risk of venous thromboembolism (VTE) has not been studied. It was the aim of this study to investigate whether influenza vaccination reduces the risk of VTE. We conducted a case-control study involving 1,454 adults enrolled in 11 French centers between 2003 and 2007, comprising 727 consecutive cases with a first documented episode of VTE and 727 age- and sex-matched controls. In the case and control groups 202 (28.2%) and 233 (32.1%) subjects, respectively, had been vaccinated against influenza during the previous 12 months. After multivariate regression analysis, the odds ratios (OR) for VTE associated with vaccination were 0.74 (95% confidence interval [CI], 0.57–0.97) and 0.52 (95% CI, 0.32–0.85), respectively, for the whole population and for subjects aged 52 years or less. The protective effect of vaccination was similar for deep venous thrombosis (OR 0.9; 95% CI, 0.60–1.35) and pulmonary embolism (OR 0.71; 95% CI, 0.53–0.94) and for both provoked (OR 0.71; 95% CI, 0.53–0.97) and unprovoked VTE (OR 0.85; 95% CI, 0.59–1.23).This case-control study suggests that influenza vaccination is associated with a reduced risk of VTE.

Keywords

Deep vein thrombosis - infection - influenza - pulmonary embolism - vaccination
 

  • References

  • 1 Cohen AT, Agnelli G, Anderson FA. et al. Venous thromboembolism (VTE) in Europe. The number of VTE events and associated morbidity and mortality Thromb Haemost 2007; 98: 756-764.
    PubMedGoogle Scholar
  • 2 Silverstein MD, Heit JA, Mohr DN. et al. Trends in the incidence of deep vein thrombosis and pulmonary embolism. A 25-year population-based study. Arch Intern Med 1998; 158: 585-593.
    PubMedGoogle Scholar
  • 3 Kyrle PA, Eichinger S. Deep vein thrombosis. Lancet 2005; 365: 1163-1174.
    CrossrefPubMedGoogle Scholar
  • 4 Rosendaal FR. Venous thrombosis: a multicausal disease. Lancet 1999; 353: 1167-1173.
    CrossrefPubMedGoogle Scholar
  • 5 Ageno W, Dentali F. Venous thromboembolism and arterial thromboembolism. Many similarities, far beyond thrombosis per se. Thromb Haemost 2008; 100: 181-183.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 6 Prandoni P, Bilora F, Marchiori A. et al. An association between atherosclerosis and venous thrombosis. N Engl J Med 2003; 348: 1435-1441.
    CrossrefPubMedGoogle Scholar
  • 7 Goldhaber SZ, Grodstein F, Stampfer MJ. et al. A prospective study of risk factors for pulmonary embolism in women. J Am Med Assoc 1997; 277: 642-645.
    CrossrefPubMedGoogle Scholar
  • 8 Hansson PO, Eriksson H, Welin L. et al. Smoking and abdominal obesity: risk factors for venous thromboembolism among middle-aged men: “the study of men born in 1913”. Arch Intern Med 1999; 159: 1886-1890.
    CrossrefPubMedGoogle Scholar
  • 9 Pomp ER, Rosendaal FR, Doggen CJ. Smoking increases the risk of venous thrombosis and acts synergistically with oral contraceptive use. Am J Hematol 2008; 83: 97-102.
    CrossrefPubMedGoogle Scholar
  • 10 Petrauskiene V, Falk M, Waernbaum I. et al. The risk of venous thromboembolism is markedly elevated in patients with diabetes. Diabetologia 2005; 48: 1017-1021.
    CrossrefPubMedGoogle Scholar
  • 11 Deguchi H, Pecheniuk NM, Elias DJ. et al. High density lipoprotein deficiency and dyslipoproteinemia associated with venous thrombosis in men. Circulation 2005; 112: 893-899.
    CrossrefPubMedGoogle Scholar
  • 12 Eichinger S, Pecheniuk NM, Hron G. et al. Highdensity lipoprotein and the risk of recurrent venous thromboembolism. Circulation 2007; 115: 1609-1614.
    CrossrefPubMedGoogle Scholar
  • 13 Ageno W, Becattini C, Brighton T. et al. Cardiovascular risk factors and venous thromboembolism: a meta-analysis. Circulation 2008; 117: 93-102.
    CrossrefPubMedGoogle Scholar
  • 14 Madjid M, Miller CC, Zarubaev VV. et al. Influenza epidemics and acute respiratory disease activity are associated with a surge in autopsy-confirmed coronary heart disease death: results from 8 years of autopsies in 34 892 subjects. Eur Heart J 2007; 28: 1205-1210.
    CrossrefPubMedGoogle Scholar
  • 15 Smeeth L, Cook C, Thomas S. et al. Risk of deep vein thrombosis and pulmonary embolism after acute infection in a community setting. Lancet 2006; 367: 1075-1079.
    CrossrefPubMedGoogle Scholar
  • 16 Naghavi M, Barlas Z, Siadaty S. et al. Association of influenza vaccination and reduced risk of recurrent myocardial infarction. Circulation 2000; 102: 3039-3045.
    CrossrefPubMedGoogle Scholar
  • 17 Gurfinkel EP, de la Fuente RL, Mendiz O. et al. Influenza vaccine pilot study in acute coronary syndromes and planned percutaneous coronary interventions: the FLU Vaccination Acute Coronary Syndromes (FLUVACS) Study. Circulation 2002; 105: 2143-2147.
    CrossrefPubMedGoogle Scholar
  • 18 Gurfinkel EP, de la Fuente RL, Mendiz O. et al. Flu vaccination in acute coronary syndromes and planned percutaneous coronary interventions (FLUVACS) Study. Eur Heart J 2004; 25: 25-31.
    CrossrefPubMedGoogle Scholar
  • 19 Nichol KL, Nordin J, Mullooly J. et al. Influenza vaccination and reduction in hospitalization for cardiac disease and stroke among the elderly. N Engl J Med 2003; 348: 1322-1332.
    CrossrefPubMedGoogle Scholar
  • 20 Nichol KL, Nordin JD, Nelson DB. et al. Effectiveness of influenza vaccine in the community-dwelling elderly. N Engl J Med 2007; 357: 1373-1381.
    CrossrefPubMedGoogle Scholar
  • 21 Davis MM, Taubert K, Benin AL. et al. Influenza vaccination as secondary prevention for cardiovascular disease: a science advisory from the American Heart Association/American College of Cardiology. Circulation 2006; 114: 1549-1553.
    CrossrefPubMedGoogle Scholar
  • 22 Smith SC, Allen J, Blair SN. et al. AHA/ACC guidelines for secondary prevention for patients with coronary and other atherosclerotic vascular disease: 2006 update: endorsed by the National Heart, Lung, and Blood Institute. Circulation 2006; 113: 2363-2372.
    CrossrefPubMedGoogle Scholar
  • 23 Keller T, Weeda VB, van Dongen CJ. et al. Influenza vaccines for preventing coronary heart disease. Cochrane Database Syst Rev. 2008 16. CD005050.
    PubMedGoogle Scholar
  • 24 Samama MM. An epidemiologic study of risk factors for deep vein thrombosis in medical outpatients: the Sirius study. Arch Intern Med 2000; 160: 3415-3420.
    CrossrefPubMedGoogle Scholar
  • 25 Alikhan R, Cohen AT, Combe S. et al. Risk factors for venous thromboembolism in hospitalized patients with acute medical illness: analysis of the MEDENOX Study. Arch Intern Med 2004; 164: 963-968.
    CrossrefPubMedGoogle Scholar
  • 26 Vormittag R, Hsieh K, Kaider A. et al. Interleukin-6 and interleukin-6 promoter polymorphism (-174) G > C in patients with spontaneous venous thromboembolism. Thromb Haemost 2006; 95: 802-806.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 27 Reitsma PH, Rosendaal FR. Activation of innate immunity in patients with venous thrombosis: the Leiden Thrombophilia Study. J Thromb Haemost 2004; 02: 619-622.
    CrossrefPubMedGoogle Scholar
  • 28 van Wissen M, Keller TT, Ronkes B. et al. Influenza infection and risk of acute pulmonary embolism. Thromb J 2007; 05: 16-20.
    PubMedGoogle Scholar
  • 29 Visseren FL, Bouwman JJ, Bouter KP. et al. Procoagulant activity of endothelial cells after infection with respiratory viruses. Thromb Haemost 2000; 84: 319-324.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 30 Visseren FL, Verkerk MS, Bouter KP. et al. Interleukin-6 production by endothelial cells after infection with influenza virus and cytomegalovirus. J Lab Clin Med 1999; 134: 623-630.
    CrossrefPubMedGoogle Scholar
  • 31 Keller TT, van der Sluijs KF, de Kruif MD. et al. Effects on coagulation and fibrinolysis induced by influenza in mice with a reduced capacity to generate activated protein C and a deficiency in plasminogen activator inhibitor type 1. Circ Res 2006; 99: 1261-1269.
    CrossrefPubMedGoogle Scholar
  • 32 Lina B, Holm MV, Szucs TD. Evolution of influenza vaccination coverage in France from 2001 to 2006. Med Mal Infect 2008; 38: 125-132.
    CrossrefPubMedGoogle Scholar