PDF herunterladen
CC BY-NC-ND 4.0 · TH Open 2017; 01(01): e66-e72
DOI: 10.1055/s-0037-1603983
Original Article
Georg Thieme Verlag KG Stuttgart · New York

Impact of Venous Thromboembolism on the Formation and Progression of Carotid Atherosclerosis: The Tromsø Study

Caroline Lind
1   K.G. Jebsen Thrombosis Research and Expertise Center (TREC), Department of Clinical Medicine, UiT - The Arctic University of Norway, Tromsø, Norway
2   Division of Internal Medicine, University Hospital of North Norway, Tromsø, Norway
,
Birgit Småbrekke
1   K.G. Jebsen Thrombosis Research and Expertise Center (TREC), Department of Clinical Medicine, UiT - The Arctic University of Norway, Tromsø, Norway
,
Ludvig Balteskard Rinde
1   K.G. Jebsen Thrombosis Research and Expertise Center (TREC), Department of Clinical Medicine, UiT - The Arctic University of Norway, Tromsø, Norway
,
Kristian Hindberg
1   K.G. Jebsen Thrombosis Research and Expertise Center (TREC), Department of Clinical Medicine, UiT - The Arctic University of Norway, Tromsø, Norway
,
Ellisiv Bøgeberg Mathiesen
1   K.G. Jebsen Thrombosis Research and Expertise Center (TREC), Department of Clinical Medicine, UiT - The Arctic University of Norway, Tromsø, Norway
3   Brain and Circulation Research Group, Department of Clinical Medicine, UiT - The Arctic University of Norway, Tromsø, Norway
4   Department of Neurology and Clinical Neurophysiology, University Hospital of North Norway, Tromsø, Norway
,
Stein Harald Johnsen
3   Brain and Circulation Research Group, Department of Clinical Medicine, UiT - The Arctic University of Norway, Tromsø, Norway
4   Department of Neurology and Clinical Neurophysiology, University Hospital of North Norway, Tromsø, Norway
,
Kjell Arne Arntzen
3   Brain and Circulation Research Group, Department of Clinical Medicine, UiT - The Arctic University of Norway, Tromsø, Norway
4   Department of Neurology and Clinical Neurophysiology, University Hospital of North Norway, Tromsø, Norway
,
Inger Njølstad
1   K.G. Jebsen Thrombosis Research and Expertise Center (TREC), Department of Clinical Medicine, UiT - The Arctic University of Norway, Tromsø, Norway
5   Epidemiology of Chronic Diseases Research Group, Department of Community Medicine, UiT - The Arctic University of Norway, Tromsø, Norway
,
Willem Lijfering
6   Department of Clinical Epidemiology, Leiden University Medical Center, Leiden, The Netherlands
,
Sigrid Kufaas Brækkan
1   K.G. Jebsen Thrombosis Research and Expertise Center (TREC), Department of Clinical Medicine, UiT - The Arctic University of Norway, Tromsø, Norway
2   Division of Internal Medicine, University Hospital of North Norway, Tromsø, Norway
,
John-Bjarne Hansen
1   K.G. Jebsen Thrombosis Research and Expertise Center (TREC), Department of Clinical Medicine, UiT - The Arctic University of Norway, Tromsø, Norway
2   Division of Internal Medicine, University Hospital of North Norway, Tromsø, Norway
› Institutsangaben
Weitere Informationen

Publikationsverlauf

Publikationsdatum:
28. Juni 2017 (online)

Auch verfügbar auf
   Lizenzen und Reprints

Abstract

Venous thromboembolism (VTE) is associated with increased risk of arterial cardiovascular diseases (CVD), and development of atherosclerosis secondary to VTE may be an intermediate between VTE and CVD. Therefore, we aimed to investigate whether incident VTE was associated with subsequent carotid atherosclerosis formation and progression in a population-based observational study. Subjects attending two or more ultrasound examinations of the right carotid artery, with measurement of total plaque area (TPA), in the Tromsø Study in 1994–1995, 2001–2002, and/or 2007–2008 were eligible. We identified 150 subjects diagnosed with first-lifetime VTE between the initial and follow-up visit, and randomly selected 600 age- and sex-matched subjects without VTE between the visits. Subjects with VTE and carotid plaque(s) at the first visit had 4.1 mm2 (β: 4.13, 95% CI: −1.72 to 9.98) larger change in TPA between the first and second visit compared with subjects without VTE after adjustment for change in high-sensitivity C-reactive protein (hs-CRP) and traditional atherosclerotic risk factors. The association remained after restricting the analyses to VTE events diagnosed in the first half of the time interval between the carotid ultrasounds (β: 4.02, 95% CI: −3.66 to 11.70), supporting that the change in TPA occurred subsequent to the VTE. No association was found between VTE and novel carotid plaque formation. In conclusion, we found a possible association between VTE and atherosclerosis progression in those with already established carotid plaques, but not between VTE and novel plaque formation. The association between VTE and carotid plaque progression was not mediated by low-grade inflammation assessed by hs-CRP.

Keywords

atherosclerosis - epidemiological studies - risk factors - venous thrombosis
 

  • References

  • 1 Lind C, Flinterman LE, Enga KF. , et al. Impact of incident venous thromboembolism on risk of arterial thrombotic diseases. Circulation 2014; 129 (08) 855-863
    CrossrefPubMedSuche in Google Scholar
  • 2 Sørensen HT, Horvath-Puho E, Pedersen L, Baron JA, Prandoni P. Venous thromboembolism and subsequent hospitalisation due to acute arterial cardiovascular events: a 20-year cohort study. Lancet 2007; 370 (9601): 1773-1779
    CrossrefPubMedSuche in Google Scholar
  • 3 van den Oord SC, Sijbrands EJ, ten Kate GL. , et al. Carotid intima-media thickness for cardiovascular risk assessment: systematic review and meta-analysis. Atherosclerosis 2013; 228 (01) 1-11
    CrossrefPubMedSuche in Google Scholar
  • 4 Davidsson L, Fagerberg B, Bergström G, Schmidt C. Ultrasound-assessed plaque occurrence in the carotid and femoral arteries are independent predictors of cardiovascular events in middle-aged men during 10 years of follow-up. Atherosclerosis 2010; 209 (02) 469-473
    CrossrefPubMedSuche in Google Scholar
  • 5 Prandoni P, Bilora F, Marchiori A. , et al. An association between atherosclerosis and venous thrombosis. N Engl J Med 2003; 348 (15) 1435-1441
    CrossrefPubMedSuche in Google Scholar
  • 6 Jezovnik MK, Poredos P, Lusa L. Idiopathic venous thrombosis is associated with preclinical atherosclerosis. J Atheroscler Thromb 2010; 17 (03) 304-311
    CrossrefPubMedSuche in Google Scholar
  • 7 Roumen-Klappe EM, den Heijer M, van Uum SH, van der Ven-Jongekrijg J, van der Graaf F, Wollersheim H. Inflammatory response in the acute phase of deep vein thrombosis. J Vasc Surg 2002; 35 (04) 701-706
    CrossrefPubMedSuche in Google Scholar
  • 8 Jezovnik MK, Fareed J, Poredos P. Subjects with a history of idiopathic deep venous thrombosis have long-term increased levels of inflammatory markers and markers of endothelial damage. Clin Appl Thromb Hemost 2017; 23 (02) 124-131
    CrossrefPubMedSuche in Google Scholar
  • 9 Zhang YX, Cliff WJ, Schoefl GI, Higgins G. Coronary C-reactive protein distribution: its relation to development of atherosclerosis. Atherosclerosis 1999; 145 (02) 375-379
    CrossrefPubMedSuche in Google Scholar
  • 10 Jacobsen BK, Eggen AE, Mathiesen EB, Wilsgaard T, Njølstad I. Cohort profile: the Tromso Study. Int J Epidemiol 2012; 41 (04) 961-967
    CrossrefPubMedSuche in Google Scholar
  • 11 Braekkan SK, Borch KH, Mathiesen EB, Njølstad I, Wilsgaard T, Hansen JB. Body height and risk of venous thromboembolism: the Tromsø Study. Am J Epidemiol 2010; 171 (10) 1109-1115
    CrossrefPubMedSuche in Google Scholar
  • 12 Brækkan SK, Hald EM, Mathiesen EB. , et al. Competing risk of atherosclerotic risk factors for arterial and venous thrombosis in a general population: the Tromso study. Arterioscler Thromb Vasc Biol 2012; 32 (02) 487-491
    CrossrefPubMedSuche in Google Scholar
  • 13 Horvei LD, Grimnes G, Hindberg K. , et al. C-reactive protein, obesity, and the risk of arterial and venous thrombosis. J Thromb Haemost 2016; 14 (08) 1561-1571
    CrossrefPubMedSuche in Google Scholar
  • 14 Johnsen SH, Mathiesen EB, Fosse E. , et al. Elevated high-density lipoprotein cholesterol levels are protective against plaque progression: a follow-up study of 1952 persons with carotid atherosclerosis the Tromsø study. Circulation 2005; 112 (04) 498-504
    CrossrefPubMedSuche in Google Scholar
  • 15 Joakimsen O, Bønaa KH, Stensland-Bugge E. Reproducibility of ultrasound assessment of carotid plaque occurrence, thickness, and morphology. The Tromsø Study. Stroke 1997; 28 (11) 2201-2207
    CrossrefPubMedSuche in Google Scholar
  • 16 Stensland-Bugge E, Bønaa KH, Joakimsen O. Reproducibility of ultrasonographically determined intima-media thickness is dependent on arterial wall thickness. The Tromsø Study. Stroke 1997; 28 (10) 1972-1980
    CrossrefPubMedSuche in Google Scholar
  • 17 Fosse E, Johnsen SH, Stensland-Bugge E. , et al. Repeated visual and computer-assisted carotid plaque characterization in a longitudinal population-based ultrasound study: the Tromsø study. Ultrasound Med Biol 2006; 32 (01) 3-11
    CrossrefPubMedSuche in Google Scholar
  • 18 Inaba Y, Chen JA, Bergmann SR. Carotid plaque, compared with carotid intima-media thickness, more accurately predicts coronary artery disease events: a meta-analysis. Atherosclerosis 2012; 220 (01) 128-133
    CrossrefPubMedSuche in Google Scholar
  • 19 Plichart M, Celermajer DS, Zureik M. , et al. Carotid intima-media thickness in plaque-free site, carotid plaques and coronary heart disease risk prediction in older adults. The Three-City Study. Atherosclerosis 2011; 219 (02) 917-924
    CrossrefPubMedSuche in Google Scholar
  • 20 Johnsen SH, Mathiesen EB, Joakimsen O. , et al. Carotid atherosclerosis is a stronger predictor of myocardial infarction in women than in men: a 6-year follow-up study of 6226 persons: the Tromsø Study. Stroke 2007; 38 (11) 2873-2880
    CrossrefPubMedSuche in Google Scholar
  • 21 Herder M, Johnsen SH, Arntzen KA, Mathiesen EB. Risk factors for progression of carotid intima-media thickness and total plaque area: a 13-year follow-up study: the Tromsø Study. Stroke 2012; 43 (07) 1818-1823
    CrossrefPubMedSuche in Google Scholar
  • 22 Milan M, Vedovetto V, Bilora F, Pesavento R, Prandoni P. Further evidence in support of the association between venous thrombosis and atherosclerosis: a case-control study. Thromb Res 2014; 134 (05) 1028-1031
    CrossrefPubMedSuche in Google Scholar
  • 23 Hald EM, Lijfering WM, Mathiesen EB. , et al. Carotid atherosclerosis predicts future myocardial infarction but not venous thromboembolism: the Tromso study. Arterioscler Thromb Vasc Biol 2014; 34 (01) 226-230
    CrossrefPubMedSuche in Google Scholar
  • 24 Rabinovich A, Cohen JM, Cushman M, Kahn SR. ; BioSOX Investigators. Association between inflammation biomarkers, anatomic extent of deep venous thrombosis, and venous symptoms after deep venous thrombosis. J Vasc Surg Venous Lymphat Disord 2015; 3 (04) 347-53.e1
    PubMedSuche in Google Scholar
  • 25 Buckley DI, Fu R, Freeman M, Rogers K, Helfand M. C-reactive protein as a risk factor for coronary heart disease: a systematic review and meta-analyses for the U.S. Preventive Services Task Force. Ann Intern Med 2009; 151 (07) 483-495
    CrossrefPubMedSuche in Google Scholar
  • 26 Ridker PM, Cushman M, Stampfer MJ, Tracy RP, Hennekens CH. Inflammation, aspirin, and the risk of cardiovascular disease in apparently healthy men. N Engl J Med 1997; 336 (14) 973-979
    CrossrefPubMedSuche in Google Scholar
  • 27 Kaptoge S, Di Angelantonio E, Lowe G. , et al; Emerging Risk Factors Collaboration. C-reactive protein concentration and risk of coronary heart disease, stroke, and mortality: an individual participant meta-analysis. Lancet 2010; 375 (9709): 132-140
    CrossrefPubMedSuche in Google Scholar
  • 28 Willeit P, Thompson SG, Agewall S. , et al; PROG-IMT Study Group. Inflammatory markers and extent and progression of early atherosclerosis: Meta-analysis of individual-participant-data from 20 prospective studies of the PROG-IMT collaboration. Eur J Prev Cardiol 2016; 23 (02) 194-205
    CrossrefPubMedSuche in Google Scholar
  • 29 Halvorsen DS, Johnsen SH, Mathiesen EB, Njølstad I. The association between inflammatory markers and carotid atherosclerosis is sex dependent: the Tromsø Study. Cerebrovasc Dis 2009; 27 (04) 392-397
    CrossrefPubMedSuche in Google Scholar
  • 30 Schillinger M, Exner M, Mlekusch W. , et al. Inflammation and Carotid Artery--Risk for Atherosclerosis Study (ICARAS). Circulation 2005; 111 (17) 2203-2209
    CrossrefPubMedSuche in Google Scholar
  • 31 van der Meer IM, Iglesias del Sol A, Hak AE, Bots ML, Hofman A, Witteman JC. Risk factors for progression of atherosclerosis measured at multiple sites in the arterial tree: the Rotterdam Study. Stroke 2003; 34 (10) 2374-2379
    CrossrefPubMedSuche in Google Scholar
  • 32 Schmidt R, Schmidt H, Pichler M. , et al. C-reactive protein, carotid atherosclerosis, and cerebral small-vessel disease: results of the Austrian Stroke Prevention Study. Stroke 2006; 37 (12) 2910-2916
    CrossrefPubMedSuche in Google Scholar
  • 33 Ye Z, Liu EH, Higgins JP. , et al. Seven haemostatic gene polymorphisms in coronary disease: meta-analysis of 66,155 cases and 91,307 controls. Lancet 2006; 367 (9511): 651-658
    CrossrefPubMedSuche in Google Scholar
  • 34 den Heijer M, Rosendaal FR, Blom HJ, Gerrits WB, Bos GM. Hyperhomocysteinemia and venous thrombosis: a meta-analysis. Thromb Haemost 1998; 80 (06) 874-877
    Thieme ConnectPubMedSuche in Google Scholar
  • 35 Mahmoodi BK, Gansevoort RT, Veeger NJ. , et al; Prevention of Renal and Vascular End-stage Disease (PREVEND) Study Group. Microalbuminuria and risk of venous thromboembolism. JAMA 2009; 301 (17) 1790-1797
    CrossrefPubMedSuche in Google Scholar
  • 36 Chambless LE, Folsom AR, Davis V. , et al. Risk factors for progression of common carotid atherosclerosis: the atherosclerosis risk in communities study, 1987-1998. Am J Epidemiol 2002; 155 (01) 38-47
    CrossrefPubMedSuche in Google Scholar
  • 37 Kuijpers MJ, van der Meijden PE, Feijge MA. , et al. Factor XII regulates the pathological process of thrombus formation on ruptured plaques. Arterioscler Thromb Vasc Biol 2014; 34 (08) 1674-1680
    CrossrefPubMedSuche in Google Scholar
  • 38 Lewis MR, Callas PW, Jenny NS, Tracy RP. Longitudinal stability of coagulation, fibrinolysis, and inflammation factors in stored plasma samples. Thromb Haemost 2001; 86 (06) 1495-1500
    Thieme ConnectPubMedSuche in Google Scholar