Epidemiology and pathophysiology of venous thromboembolism: similarities with atherothrombosis and the role of inflammation

Nicoletta Riva; Marco P. Donadini; Walter Ageno

doi:10.1160/TH14-06-0563

Thrombosis and Haemostasis, Inhaltsverzeichnis

Thromb Haemost 2015; 113(06): 1176-1183
DOI: 10.1160/TH14-06-0563

Theme Issue Article

Schattauer GmbH

Epidemiology and pathophysiology of venous thromboembolism: similarities with atherothrombosis and the role of inflammation

Autoren

Nicoletta Riva

¹Research Center on Thromboembolic Diseases and Antithrombotic Drugs, Department of Clinical and Experimental Medicine, University of Insubria, Varese, Italy
Marco P. Donadini

¹Research Center on Thromboembolic Diseases and Antithrombotic Drugs, Department of Clinical and Experimental Medicine, University of Insubria, Varese, Italy
Walter Ageno

¹Research Center on Thromboembolic Diseases and Antithrombotic Drugs, Department of Clinical and Experimental Medicine, University of Insubria, Varese, Italy

Abstract

Summary

Venous thromboembolism (VTE) is a multifactorial disease. Major provoking factors (e. g. surgery, cancer, major trauma, and immobilisation) are identified in 50–60 % of patients, while the remaining cases are classified as unprovoked. However, minor predisposing conditions may be detectable in these patients, possibly concurring to the pathophysiology of the disease, especially when co-existing. In recent years, the role of chronic inflammatory disorders, infectious diseases and traditional cardiovascular risk factors has been extensively investigated. Inflammation, with its underlying prothrombotic state, could be the potential link between these risk factors, as well as the explanation for the reported association between arterial and venous thromboembolic events.

Keywords

Venous thromboembolism - etiopathogenesis - inflammation - atherothrombosis

Volltext

Referenzen

References
1 Virchow R. Thrombose und embolie. Gefässentzündung und septische infektion. Gesammelte Abhandlungen zur wissenschaftlichen Medicin. Frankfurt am Main: Von Meidinger & Sohn 1856; pp. 219-732.
2 Naess IA. et al. Incidence and mortality of venous thrombosis: a populationbased study. J Thromb Haemost 2007; 05: 692-699.
3 Rosendaal FR. Venous thrombosis: a multicausal disease. Lancet 1999; 353: 1167-1173.
4 Hansson PO. et al. Deep vein thrombosis and pulmonary embolism in the general population. The Study of Men Born in 1913. Arch Intern Med 1997; 157: 1665-1670.
5 Oger E. Incidence of venous thromboembolism: a community-based study in Western France. Thromb Heamost 2000; 83: 657-660.
6 Silverstein MD. et al. Trends in the incidence of deep vein thrombosis and pulmonary embolism: a 25-years population-based study. Arch Intern Med 1998; 158: 585-593.
7 White RH. The epidemiology of venous thromboembolism. Circulation 2003; 107 (23) (Suppl. 01) I4-I8.
8 Abildstrom SZ. et al. Trends in incidence and case fatality rates of acute myocardial infarction in Denmark and Sweden. Heart 2003; 89: 507-511.
9 Ellekjær H. et al. Epidemiology of stroke in Innherred, Norway, 1994 to 1996. Incidence and 30-day case-fatality rate. Stroke 1997; 28: 2180-2184.
10 Dismuke SE, Wagner EH. Pulmonary embolism as a cause of death. The changing mortality in hospitalized patients. J Am Med Assoc 1986; 255: 2039-2042.
11 Carson JL. et al. The clinical course of pulmonary embolism. N Engl J Med 1992; 326: 1240-1245.
12 Anderson FA Jr. et al. A population-based perspective of the hospital incidence and case-fatality rates of deep vein thrombosis and pulmonary embolism: the Worcester DVT Study. Arch Intern Med 1991; 151: 933-938.
13 Ageno W. et al. Prevalence of risk factors for venous thromboembolism in the Italian population: results of a cross-sectional study from the MASTER registry. Intern Emerg Med 2013; 08: 575-580.
14 Rumley A. et al. Effects of older age on fibrin D- dimer, C-reactive protein and other hemostatic and inflammatory variables in men aged 60-79 years. J Thromb Haemost 2006; 04: 982-987.
15 Mari D. et al. Hemostasis factors and aging. Exp Gerontol 2008; 43: 66-73.
16 White RH. et al. Effect of ethnicity and gender on the incidence on venous thromboembolism in a diverse population in California in 1996. Thromb Hemost 2005; 93: 298-305.
17 Cohen AT. et al; VTE Imapct Assessment Group in Europe (VITAE). Venous thromboembolism (VTE) in Europe. The number of VTE events and associated morbidity and mortality. Thromb Haemost 2007; 98: 756-764.
18 Molina JA. et al. Venous thromboembolism at the National Healthcare Group, Singapore. Ann Acad Med Singapore 2009; 38: 470-478.
19 Zakai NA. et al. Racial and regional differences in venous thromboembolism in the United States in 3 cohorts. Circulation 2014; 129: 1502-1509.
20 Zakai NA, McClure LA. Racial differences in venous thromboembolism. J Thromb Haemost 2011; 09: 1877-1882.
21 Mismetti P. et al. Meta⊠analysis of low molecular weight heparin in the prevention of venous thromboembolism in general surgery. Br J Surg 2001; 88: 913-930.
22 Borgstroem S. et al. Anticoagulant prophylaxis of venous thrombosis in patients with fractured neck of the femur; a controlled clinical trial using venous phlebography. Acta Chir Scand 1965; 129: 500-508.
23 Geerts WH. et al. A prospective study of venous thromboembolism after major trauma. N Engl J Med 1994; 331: 1601-1606.
24 Acosta JA. et al. Lethal injuries and time to death in a level I trauma center. J Am Coll Surg 1998; 186: 528-533.
25 O’Malley KF, Ross SE. Pulmonary embolism in major trauma patients. J Trauma 1990; 30: 748-750.
26 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.
27 Dentali F. et al. Meta-analysis: anticoagulant prophylaxis to prevent symptomatic venous thromboembolism in hospitalized medical patients. Ann. Intern. Med 2007; 146: 278-288.
28 Imberti D. et al; MASTER Investigators. Clinical characteristics and management of cancer-associated acute venous thromboembolism: findings from the MASTER Registry. Haematologica 2008; 93: 273-278.
29 Blom JW. et al. Malignancies, prothrombotic mutations, and the risk of venous thrombosis. J Am Med Assoc 2005; 293: 715-722.
30 Otten HM. et al. Symptomatic venous thromboembolism in cancer patients treated with chemotherapy: an underestimated phenomenon. Arch Intern Med 2004; 164: 190-194.
31 Heit JA. et al. Relative impact of risk factors for deep vein thrombosis and pulmonary embolism: a population-based study. Arch Intern Med 2002; 162: 1245-1248.
32 Ageno W. et al. Optimal treatment duration of venous thrombosis. J Thromb Haemost 2013; 11 (Suppl. 01) 151-160.
33 Margaglione M, Grandone E. Population genetics of venous thromboembolism. A narrative review. Thromb Haemost 2011; 105: 221-231.
34 Morange PE, Trégouët DA. Current knowledge on the genetics of incident venous thrombosis. J Thromb Haemost 2013; 11 (Suppl. 01) 111-121.
35 Miyawaki Y, Suzuki A, Fujita J. et al. Thrombosis from a prothrombin mutation conveying antithrombin resistance. N Engl J Med 2012; 366: 2390-2396.
36 Simioni P. et al. X-linked thrombophilia with a mutant factor IX (factor IX Padua). N Engl J Med 2009; 361: 1671-1675.
37 Nogami K. et al. Novel FV mutation (W1920R, FVNara) associated with serious deep vein thrombosis and more potent APC resistance relative to FVLeiden. Blood 2014; 123: 2420-2428.
38 Colaizzo D. et al. The JAK2 V617F mutation frequently occurs in patients with portal and mesenteric venous thrombosis. J Thromb Haemost 2007; 05: 55-61.
39 Kralovics R. et al. A gain-of-function mutation of JAK2 in myeloproliferative disorders. N Engl J Med 2005; 352: 1779-1790.
40 De Stefano V. et al. Incidence of the JAK2 V617F mutation among patients with splanchnic or cerebral venous thrombosis and without overt chronic myeloproliferative disorders. J Thromb Haemost 2007; 05: 708-714.
41 Dentali F. et al. JAK2V617F mutation for the early diagnosis of Ph-negative myeloproliferative neoplasms in patients with venous thromboembolism: a meta-analysis. Blood 2009; 113: 5617-5623.
42 Smeeth L. et al. Risk of deep vein thrombosis and pulmonary embolism after acute infection in a community setting. Lancet 2006; 367: 1075-1079.
43 van Stralen KJ. et al. Minor injuries as a risk factor for venous thrombosis. Arch Intern Med 2008; 168: 21-26.
44 Stuijver DJ. et al. Incidence of venous thromboembolism in patients with Cushing’s syndrome: a multicenter cohort study. J Clin Endocrinol Metab 2011; 96: 3525-3532.
45 Squizzato A. et al. Subclinical hypothyroidism and deep venous thrombosis. A pilot cross-sectional study. Thromb Haemost 2007; 97: 803-806.
46 Ludvigsson JF. et al. Risk of thromboembolism in 14,000 individuals with coeliac disease. Br J Haematol 2007; 139: 121-127.
47 Tichelaar YI. et al. Infections and inflammatory diseases as risk factors for venous thrombosis. A systematic review. Thromb Haemost 2012; 107: 827-837.
48 Ageno W. et al. Cardiovascular risk factors and venous thromboembolism: A meta-analysis. Circulation 2008; 117: 93-102.
49 Squizzato A. et al. Clinical review: thyroid dysfunction and effects on coagulation and fibrinolysis: a systematic review. Clin Endocrinol Metab 2007; 92: 2415-2420.
50 Rogers JS II, Stanley RS. Factor VIII activity in normal volunteers receiving oral thyroid hormone. J Lab Clin Med 1983; 102: 444-449.
51 Graninger W. et al. Effect of thyroid hormones on plasma protein concentrations in man. J Clin Endocrinol Metab 1986; 63: 407-411.
52 Debeij J. et al. High levels of procoagulant factors mediate the association between free thyroxine and the risk of venous thrombosis: the MEGA study. J Thromb Haemost 2014; 12: 839-846.
53 Van Zaane B. et al. Hypercoagulable state in Cushing’s syndrome: a systematic review. J Clin Endocrinol Metab 2009; 94: 2743-2750.
54 Erem C. et al. Blood coagulation and fibrinolysis in patients with Cushing’s syndrome: increased plasminogen activator inhibitor-1, decreased tissue factor pathway inhibitor, and unchanged thrombin-activatable fibrinolysis inhibitor levels. J Endocrinol Invest 2009; 32: 169-174.
55 Squizzato A. et al. The coagulation system in endocrine disorders: a narrative review. Intern Emerg Med 2007; 02: 76-83.
56 Lijfering WM. et al. Relationship between venous and arterial thrombosis: a review of the literature from a causal perspective. Semin Thromb Hemost 2011; 37: 885-896.
57 Agnelli G, Becattini C. Venous thromboembolism and atherosclerosis: common denominators or different diseases?. J Thromb Haemost 2006; 04: 1886-1890.
58 Cotran RS. et al. Acute and chronic inflammation. In: Robbins Pathologic Basis of Disease (6th ed.). W. B. Saunders. 1999; pp 57-100.
59 Ross R. Atherosclerosis--an inflammatory disease. N Engl J Med 1999; 340: 115-126.
60 Libby P. et al. Inflammation and atherosclerosis. Circulation 2002; 105: 1135-1143.
61 Turpie AG, Esmon C. Venous and arterial thrombosis--pathogenesis and the rationale for anticoagulation. Thromb Haemost 2011; 105: 586-596.
62 Reitsma PH. et al. Mechanistic view of risk factors for venous thromboembolism. Arterioscler Thromb Vasc Biol 2012; 32: 563-568.
63 Mackman N. New insights into the mechanisms of venous thrombosis. J Clin Invest 2012; 122: 2331-2336. Erratum in: J Clin Invest 2012; 122: 3368.
64 Chirinos JA. et al. Elevation of endothelial microparticles, platelets, and leukocyte activation in patients with venous thromboembolism. J Am Coll Cardiol 2005; 45: 1467-1471.
65 Sevitt S. Thrombosis and embolism after injury. J Clin Pathol Suppl (R Coll Pathol) 1970; 04: 86-101.
66 Levi M. et al. Bidirectional relation between inflammation and coagulation. Circulation 2004; 109: 2698-2704.
67 Franco RF. et al. The in vivo kinetics of tissue factor messenger RNA expression during human endotoxemia: relationship with activation of coagulation. Blood 2000; 96: 554-559.
68 Seitz R. et al. The disturbance of hemostasis in septic shock: role of neutrophil elastase and thrombin, effects of antithrombin III and plasma substitution. Eur J Haematol 1989; 43: 22-28.
69 Nawroth PP, Stern DM. Modulation of endothelial cell hemostatic properties by tumor necrosis factor. J Exp Med 1986; 163: 740-745.
70 van der Poll T. et al. Fibrinolytic response to tumor necrosis factor in healthy subjects. J Exp Med 1991; 174: 729-732.
71 De Cicco M.. The prothrombotic state in cancer: pathogenic mechanisms. Crit Rev Oncol Hematol 2004; 50: 187-196.
72 Holley AD, Reade MC. The ‘procoagulopathy’ of trauma: too much, too late?. Curr Opin Crit Care 2013; 19: 578-586.
73 Grainge MJ. et al. Venous thromboembolism during active disease and remission in inflammatory bowel disease: a cohort study. Lancet 2010; 375: 657-663.
74 Novacek G. et al. Inflammatory bowel disease is a risk factor for recurrent venous thromboembolism. Gastroenterology 2010; 139: 779-787 787.e1.
75 Bacani AK. et al. Noncardiac vascular disease in rheumatoid arthritis: increase in venous thromboembolic events?. Arthritis Rheum 2012; 64: 53-61.
76 Chung WS. et al. Rheumatoid arthritis increases the risk of deep vein thrombosis and pulmonary thromboembolism: a nationwide cohort study. Ann Rheum Dis 2014; 73: 1774-1780.
77 Halfdanarson TR. et al. Hematologic manifestations of celiac disease. Blood 2007; 109: 412-421.
78 Johannesdottir SA. et al. Coeliac disease and risk of venous thromboembolism: a nationwide population-based case-control study. Br J Haematol 2012; 157: 499-501.
79 Zöller B. et al. Risk of pulmonary embolism in patients with autoimmune disorders: a nationwide follow-up study from Sweden. Lancet 2012; 379: 244-249.
80 Ahlehoff O. et al. Psoriasis carries an increased risk of venous thromboembolism: a Danish nationwide cohort study. PLoS One 2011; 06: e18125.
81 Undas A. et al. Association between atopic diseases and venous thromboembolism: a case-control study in patients aged 45 years or less. J Thromb Haemost 2011; 09: 870-873.
82 Alikhan R. et al; MEDENOX Study. Risk factors for venous thromboembolism in hospitalized patients with acute medical illness: analysis of the MEDENOX Study. Arch Intern Med 2004; 164: 963-968.
83 Barbar S. et al. A risk assessment model for the identification of hospitalized medical patients at risk for venous thromboembolism: the Padua Prediction Score. J Thromb Haemost 2010; 08: 2450-2457.
84 Dalager-Pedersen M. et al. Venous thromboembolism after community-acquired bacteraemia: a 20-year Danish cohort study. PLoS One 2014; 09: e86094.
85 Keller TT. 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.
86 Zhu T. et al. Association of influenza vaccination with reduced risk of venous thromboembolism. Thromb Haemost 2009; 102: 1259-1264.
87 Holst AG. et al. Risk factors for venous thromboembolism: results from the Copenhagen City Heart Study. Circulation 2010; 121: 1896-1903.
88 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.
89 Tosetto A. et al. Predicting disease recurrence in patients with previous unprovoked venous thromboembolism: a proposed prediction score (DASH). J Thromb Haemost 2012; 10: 1019-1025.
90 Rodger MA. et al. Identifying unprovoked thromboembolism patients at low risk for recurrence who can discontinue anticoagulant therapy. CMAJ 2008; 179: 417-426.
91 Eichinger S. et al. Risk assessment of recurrence in patients with unprovoked deep vein thrombosis or pulmonary embolism: the Vienna prediction model. Circulation 2010; 121: 1630-1636.
92 Varraso R. et al. Prospective Study of Diet and Venous Thromboembolism in US Women and Men. Am J Epidemiol 2012; 175: 114-126.
93 Bhoopat L. et al. Low vegetable intake is strongly associated with venous thromboembolism in Thai population. Blood Coagul Fibrinolysis 2010; 21: 758-763.
94 Borch KH. et al. Physical activity and risk of venous thromboembolism. The Tromso study. Haematologica 2010; 95: 2088-2094.
95 Enga KF. et al. Coffee consumption and the risk of venous thromboembolism: the Tromsø study. J Thromb Haemost 2011; 09: 1334-1339.
96 Hansen-Krone IJ. et al. Alcohol consumption, types of alcoholic beverages and risk of venous thromboembolism - the Tromsø Study. Thromb Haemost 2011; 106: 272-278.
97 Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults. Executive Summary of The 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). J Am Med Assoc 2001; 285: 2486-2497.
98 Mottillo S. et al. The metabolic syndrome and cardiovascular risk a systematic review and meta-analysis. J Am Coll Cardiol 2010; 56: 1113-1132.
99 Ageno W. et al. The metabolic syndrome and the risk of venous thrombosis: a case-control study. J Thromb Haemost 2006; 04: 1914-1918.
100 Dentali F. et al. The role of the metabolic syndrome in patients with provoked venous thromboembolic events. Thromb Haemost 2013; 109: 759-761.
101 Jang MJ. et al. Metabolic syndrome is associated with venous thromboembolism in the Korean population. Arterioscler Thromb Vasc Biol 2009; 29: 311-315.
102 Borch KH. et al. Abdominal obesity is essential for the risk of venous thromboembolism in the metabolic syndrome: the Tromsø study. J Thromb Haemost 2009; 07: 739-745.
103 Steffen LM. et al. Metabolic syndrome and risk of venous thromboembolism: Longitudinal Investigation of Thromboembolism Etiology. J Thromb Haemost 2009; 07: 746-751.
104 Darvall KA. et al. Obesity and thrombosis. Eur J Vasc Endovasc Surg 2007; 33: 223-233.
105 Freeman AL. et al. Prevention of venous thromboembolism in obesity. Expert Rev Cardiovasc Ther 2010; 08: 1711-1721.
106 Samad F, Ruf W. Inflammation, obesity, and thrombosis. Blood 2013; 122: 3415-3422.
107 Morange PE, Alessi MC. Thrombosis in central obesity and metabolic syndrome: mechanisms and epidemiology. Thromb Haemost 2013; 110: 669-680.
108 Ageno W. et al. Association Between the Metabolic Syndrome, Its Individual Components, and Unprovoked Venous Thromboembolism: Results of a Patient- Level Meta-Analysis. Arterioscler Thromb Vasc Biol 2014; 34: 2478-2485.
109 Hess K, Grant PJ. Inflammation and thrombosis in diabetes. Thromb Haemost 2011; 105 (Suppl. 01) S43-54.
110 Gotto Jr. AM. Jeremiah Metzger Lecture: cholesterol, inflammation and Atherosclerotic cardiovascular disease: is it all LDL?. Trans Am Clin Climatol Assoc 2011; 122: 256-289.
111 Schiffrin EL. The immune system: role in hypertension. Can J Cardiol 2013; 29: 543-548.
112 Lowe GD. Common risk factors for both arterial and venous thrombosis. Br J Haematol 2008; 140: 488-495.
113 Prandoni P. et al. An association between atherosclerosis and venous thrombosis. N Engl J Med 2003; 348: 1435-1441.
114 Hong C. et al. Coronary artery calcification and risk factors for atherosclerosis in patients with venous thromboembolism. Atherosclerosis 2005; 183: 169-174.
115 Becattini C. et al. Incidence of arterial cardiovascular events after venous thromboembolism: a systematic review and a meta-analysis. J Thromb Haemost 2010; 08: 891-897.
116 Sørensen HT. et al. Venous thromboembolism and subsequent hospitalisation due to acute arterial cardiovascular events: a 20-year cohort study. Lancet 2007; 370: 1773-1779.
117 Lind C. et al. Impact of incident venous thromboembolism on risk of arterial thrombotic diseases. Circulation 2014; 129: 855-863.
118 Reich LM. et al. Prospective study of subclinical atherosclerosis as a risk factor for venous thromboembolism. J Thromb Haemost 2006; 04: 1909-1913.
119 van der Hagen PB. et al. Subclinical atherosclerosis and the risk of future venous thrombosis in the Cardiovascular Health Study. J Thromb Haemost 2006; 04: 1903-1908.
120 Hald EM. et al. Carotid atherosclerosis predicts future myocardial infarction but not venous thromboembolism: the Tromso study. Arterioscler Thromb Vasc Biol 2014; 34: 226-230.