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Thromb Haemost 2015; 114(04): 812-818
DOI: 10.1160/TH14-10-0868
Stroke, Systemic or Venous Thromboembolism
Schattauer GmbH

Diabetes increases the risk of deep-vein thrombosis and pulmonary embolism

A population-based cohort study
Wei-Sheng Chung
1   Department of Internal Medicine, Taichung Hospital, Ministry of Health and Welfare, Taichung, Taiwan
2   Department of Healthcare Administration, Central Taiwan University of Science and Technology, Taichung, Taiwan
,
Cheng-Li Lin
3   Management Office for Health Data, China Medical University Hospital, Taichung, Taiwan
4   College of Medicine, China Medical University, Taichung, Taiwan
,
Chia-Hung Kao
5   Graduate Institute of Clinical Medical Science and School of Medicine, College of Medicine, China Medical University, Taichung, Taiwan
6   Department of Nuclear Medicine and PET Center, China Medical University Hospital, Taichung, Taiwan
› Author Affiliations
Further Information

Publication History

Received: 21 October 2014

Accepted after major revision: 25 March 2015

Publication Date:
29 November 2017 (online)

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Summary

We evaluated the effects of diabetes on the risks of developing deep vein thrombosis (DVT) and pulmonary embolism (PE) in a nationwide, population-based cohort study in Taiwan. The patients with newly diagnosed type 2 diabetes mellitus (T2DM) were identified, and DM-free controls were randomly selected from the general population and frequency-matched according to age, sex, and index year by using the records of the Longitudinal Health Insurance Database between 2000 and 2011. Both cohorts were followed up until the end of 2011 to measure the incidence of DVT and PE. We analysed the risks of DVT and PE using Cox proportional-hazards regression models. The overall incidence of VTE was higher in the T2DM patients than in the controls (12.0 vs 7.51 per 10,000 person-years). The T2DM patients exhibited a 1.44-fold adjusted hazard ratio (aHR) of VTE development compared with the controls (95 % confidence interval [CI] = 1.27–1.63). The risks of DVT (aHR = 1.43, 95 % CI = 1.23–1.65) and PE (aHR = 1.52, 95 % CI = 1.22–1.90) were greater in the T2DM than those in the controls. The T2DM patients had a substantially higher risk of DVT (aHR = 5.10, 95 % CI = 3.12–8.32) and PE (aHR = 7.50, 95 % CI = 3.29–17.1) development than the controls did in adults aged 49 years and younger. In conclusion, the longitudinal nationwide cohort study indicated that T2DM patients carried greater risks of developing VTE than did the general population.

Keywords

Diabetes mellitus (DM) - deep vein thrombosis (DVT) - pulmonary embolism (PE)
 

  • References

  • 1 Shaw JE, Sicree RA, Zimmet PZ. Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes Res Clin Pract 2010; 87: 4-14.
    CrossrefPubMedGoogle Scholar
  • 2 Jiang YD, Chang CH, Tai TY. et al. Incidence and prevalence rates of diabetes mellitus in Taiwan: analysis of the 2000–2009 Nationwide Health Insurance database. J Formos Med Assoc 2012; 111: 599-604.
    CrossrefPubMedGoogle Scholar
  • 3 Third Report of the National Cholesterol Education Program (NCEP). Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III) final report. Circulation 2002; 106: 3143-421.
    PubMedGoogle Scholar
  • 4 De Backer G, Ambrosioni E, Borch-Johnsen K. et al. European guidelines on cardiovascular disease prevention in clinical practice: third joint task force of European and other societies on cardiovascular disease prevention in clinical practice (constituted by representatives of eight societies and by invited experts). Eur J Cardiovasc Prev Rehabil 2003; 10: S1-S10.
    PubMedGoogle Scholar
  • 5 Wu HT, Lee CH, Liu AB. et al. Arterial stiffness using radial arterial waveforms measured at the wrist as an indicator of diabetic control in the elderly. IEEE Trans Biomed Eng 2011; 58: 243-252.
    CrossrefPubMedGoogle Scholar
  • 6 Charles M, Ejskjaer N, Witte DR. et al. Prevalence of neuropathy and peripheral arterial disease and the impact of treatment in people with screen-detected type 2 diabetes: the ADDITION-Denmark study. Diabetes Care 2011; 34: 2244-9.
    CrossrefPubMedGoogle Scholar
  • 7 Lai YJ, Hu HY, Lin CH. et al. Incidence and risk factors of lower extremity amputations in people with type 2 diabetes in Taiwan, 2001–2010. J Diabetes. 2014 Epub ahead of print.
    PubMedGoogle Scholar
  • 8 Cohen AT, Tapson VF, Bergmann JF. et al. Venous thromboembolism risk and prophylaxis in the acute hospital care setting (ENDORSE study): a multinational cross-sectional study. Lancet 2008; 371: 387-394.
    CrossrefPubMedGoogle Scholar
  • 9 Cushman M, Tsai AW, White RH. et al. Deep vein thrombosis and pulmonary embolism in two cohorts: the longitudinal investigation of thromboembolism etiology. Am J Med 2004; 117: 19-25.
    CrossrefPubMedGoogle Scholar
  • 10 Gromadzinski L, Targonski R, Januszko-Giergielewicz B. et al. The influence of acute pulmonary embolism on early and delayed prognosis for patients with chronic heart failure. Cardiol J 2012; 19: 625-631.
    CrossrefPubMedGoogle Scholar
  • 11 Esmon CT. Basic mechanisms and pathogenesis of venous thrombosis. Blood Rev 2009; 23: 225-229.
    CrossrefPubMedGoogle Scholar
  • 12 Reitsma PH, Versteeg HH, Middeldorp S. Mechanistic view of risk factors for venous thromboembolism. Arterioscl Thromb Vasc Biol 2012; 32: 563-568.
    CrossrefPubMedGoogle Scholar
  • 13 Becattini C, Vedovati MC, Agnelli G. Old and new oral anticoagulants for venous thromboembolism and atrial fibrillation: a review of the literature. Thromb Res 2012; 129: 392-400.
    CrossrefPubMedGoogle Scholar
  • 14 Bembenek J, Karlinski M, Kobayashi A. et al. Early stroke-related deep venous thrombosis: risk factors and influence on outcome. J Thromb Thrombol 2011; 32: 96-102.
    CrossrefPubMedGoogle Scholar
  • 15 Dean SM, Abraham W. Venous thromboembolic disease in congestive heart failure. Congest Heart Fail 2010; 16: 164-169.
    CrossrefPubMedGoogle Scholar
  • 16 Tien WC, Kao HY, Tu YK. et al. A population-based study of prevalence and hospital charges in total hip and knee replacement. Intern Orthop 2009; 33: 949-954.
    CrossrefPubMedGoogle Scholar
  • 17 Prandoni P, Falanga A, Piccioli A. Cancer and venous thromboembolism. Lancet Oncol 2005; 6: 401-410.
    CrossrefPubMedGoogle Scholar
  • 18 Chung WS, Lin CL, Hsu WH. et al. Idiopathic venous thromboembolism: a potential surrogate for occult cancer. 2014; 107: 529-536.
    PubMedGoogle Scholar
  • 19 Stein PD, Goldman J, Matta F. et al. Diabetes mellitus and risk of venous thromboembolism. Am J Med Sci 2009; 337: 259-264.
    CrossrefPubMedGoogle Scholar
  • 20 Piazza G, Goldhaber SZ, Kroll A. et al. Venous thromboembolism in patients with diabetes mellitus. Am J Med 2012; 125: 709-716.
    CrossrefPubMedGoogle Scholar
  • 21 Heit JA, Leibson CL, Ashrani AA. et al. Is diabetes mellitus an independent risk factor for venous thromboembolism?: a population-based case-control study. Arterioscl Thromb Vasc Biol 2009; 29: 1399-1405.
    CrossrefPubMedGoogle Scholar
  • 22 Cheng TM. Taiwan’s National Health Insurance system: high value for the dollar. In: Okma, KGH and Crivelli, L ed Six Countries, Six Reform Models: The Health Reform Experience of Israel, the Netherlands, New Zealand, Singapore, Switzerland and Taiwan. New Jersey: World Scientific; 2009: 71-204.
    Google Scholar
  • 23 Cheng CL, Kao YH, Lin SJ. et al. Validation of the National Health Insurance Research Database with ischemic stroke cases in Taiwan. Pharmacoepidemiol Drug Saf 2011; 20: 236-242.
    CrossrefPubMedGoogle Scholar
  • 24 Cheng CL, Lee CH, Chen PS. et al. Validation of acute myocardial infarction cases in the national health insurance research database in taiwan. J Epidemiol 2014; 24: 500-507.
    CrossrefPubMedGoogle Scholar
  • 25 Grant PJ. Diabetes mellitus as a prothrombotic condition. J Intern Med 2007; 262: 157-172.
    CrossrefPubMedGoogle Scholar
  • 26 Ferreiro JL, Gomez-Hospital JA, Angiolillo DJ. Platelet abnormalities in diabetes mellitus. Diabetes Vasc Dis Res 2010; 7: 251-259.
    CrossrefPubMedGoogle Scholar
  • 27 Avogaro A, Albiero M, Menegazzo L, de Kreutzenberg S, Fadini GP. Endothelial dysfunction in diabetes: the role of reparatory mechanisms. Diabetes Care 2011; 34 (Suppl. 02) S285-290.
    CrossrefPubMedGoogle Scholar
  • 28 Carr ME. Diabetes mellitus: a hypercoagulable state. J Diabetes Compl 2001; 15: 44-54.
    CrossrefPubMedGoogle Scholar
  • 29 Garcia Frade LJ, de la Calle H, Alava I. et al. Diabetes mellitus as a hypercoagulable state: its relationship with fibrin fragments and vascular damage. Thromb Res 1987; 47: 533-540.
    CrossrefPubMedGoogle Scholar
  • 30 Esmon CT. Protein C anticoagulant system--anti-inflammatory effects. Semin Immunopathol 2012; 34: 127-132.
    CrossrefPubMedGoogle Scholar
  • 31 Stavenuiter F, Bouwens EA, Mosnier LO. Down-regulation of the clotting cascade by the protein C pathway. Hematology education / Congress of the European Hematology Association European Hematology Association Congress Education Program 2013; 7: 365-374.
    PubMedGoogle Scholar
  • 32 Whitmont K, Fulcher G, Reid I. et al. Low circulating protein C levels are associated with lower leg ulcers in patients with diabetes. BioMed Res Internat 2013; 2013: 719570.
    PubMedGoogle Scholar
  • 33 Brazionis L, Rowley K, Jenkins A. et al. Plasminogen activator inhibitor-1 activity in type 2 diabetes: a different relationship with coronary heart disease and diabetic retinopathy. Arterioscl Thromb Vasc Biol 2008; 28: 786-791.
    CrossrefPubMedGoogle Scholar
  • 34 Kawada T. Body mass index is a good predictor of hypertension and hyperlipidemia in a rural Japanese population. Int J Obes Relat Metab Disord 2002; 26: 725-729.
    CrossrefPubMedGoogle Scholar
  • 35 Tesfaye F, Nawi NG, Van Minh H. et al. Association between body mass index and blood pressure across three populations in Africa and Asia. J Hum Hypertens 2007; 21: 28-37.
    CrossrefPubMedGoogle Scholar
  • 36 Song YM, Sung J, Davey Smith G. et al. Body mass index and ischemic and hemorrhagic stroke: a prospective study in Korean men. Stroke 2004; 35: 831-836.
    CrossrefPubMedGoogle Scholar