Differential risks in men and women for first and recurrent venous thrombosis: The role of genes and environment

Journal of Thrombosis and Haemostasis

Volumn 12, Issue 10, 2014, Pages 1593-1600

  Roach, R E J ^a   Cannegieter, S C ^a   Lijfering, W M ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Epidemiology; Pulmonary embolism; Risk factors; Sex; Venous thrombosis

Indexed keywords

ANTICOAGULANT AGENT; BLOOD CLOTTING FACTOR 5 LEIDEN; ESTROGEN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; PROTHROMBIN; TESTOSTERONE; BLOOD CLOTTING FACTOR 5; BLOOD GROUP ABO SYSTEM;

ANTICOAGULANT THERAPY; ARTICLE; ATHEROGENESIS; ATTRIBUTABLE RISK; BLOOD GROUP; BODY HEIGHT; CARDIOVASCULAR RISK; ENVIRONMENTAL FACTOR; FEMALE; GENE MUTATION; GENETIC RISK; GENETIC VARIABILITY; GENOTYPE ENVIRONMENT INTERACTION; HIGH RISK POPULATION; HUMAN; HYPERCOAGULABILITY; INCIDENCE; MALE; MEDICATION COMPLIANCE; PATHOPHYSIOLOGY; PATIENT COMPLIANCE; POPULATION DISTRIBUTION; PREVALENCE; PRIORITY JOURNAL; RECURRENCE RISK; RECURRENT DISEASE; RISK ASSESSMENT; RISK FACTOR; SEX DIFFERENCE; VEIN THROMBOSIS; X CHROMOSOME; ADOLESCENT; ADULT; AGED; BLOOD CLOTTING; BLOOD GROUP ABO SYSTEM; CHEMISTRY; GENETICS; METHODOLOGY; MIDDLE AGED; MUTATION; VENOUS THROMBOSIS; YOUNG ADULT;

ABO BLOOD-GROUP SYSTEM; ADOLESCENT; ADULT; AGED; ANTICOAGULANTS; BLOOD COAGULATION; BODY HEIGHT; FACTOR V; FEMALE; GENE-ENVIRONMENT INTERACTION; HUMANS; INCIDENCE; MALE; MIDDLE AGED; MUTATION; PREVALENCE; PROTHROMBIN; RECURRENCE; RESEARCH DESIGN; RISK FACTORS; SEX FACTORS; VENOUS THROMBOSIS; YOUNG ADULT;

EID: 84907877580     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/jth.12678     Document Type: Article

References (81)

1. Verdonk P, Benschop YW, de Haes HC, Lagro-Janssen TL. From gender bias to gender awareness in medical education. Adv Health Sci Educ Theory Pract 2009; 14: 135-52.
2. Deslandes M. Traite des Accouchements de M. Puzos Paris: Desaint & Saillant, 1759.
3. Rosendaal FR. Causes of venous thrombosis. In: van Beek EJ, Buller HR, Oudkerk M, eds. Deep Vein Thrombosis and Pulmonary Embolism, 2nd edn. Chichester: John Wiley and Sons, 2012:1-26.
4. Virchow R. Phlogose und Trombose im Gefäbsystem Fesammelte Abhandelungen zur Wissenschaftlichen Medizin Frankfurt, Germany: Staatsdruckerei, 1856.
5. Kyrle PA, Minar E, Bialonczyk C, Hirschl M, Weltermann A, Eichinger S. The risk of recurrent venous thromboembolism in men and women. N Engl J Med 2004; 350: 2558-63.
6. Christiansen SC, Lijfering WM, Helmerhorst FM, Rosendaal FR, Cannegieter SC. Sex difference in risk of recurrent venous thrombosis and the risk profile for a second event. J Thromb Haemost 2010; 8: 2159-68.
7. Baglin T, Luddington R, Brown K, Baglin C. High risk of recurrent venous thromboembolism in men. J Thromb Haemost 2004; 2: 2152-5.
8. Rodger MA, Kahn SR, Wells PS, Anderson DA, Chagnon I, Le Gal G, Solymoss S, Crowther M, Perrier A, White R, Vickars L, Ramsay T, Betancourt MT, Kovacs MJ. Identifying unprovoked thromboembolism patients at low risk for recurrence who can discontinue anticoagulant therapy. CMAJ 2008; 179: 417-26.
9. McRae S, Tran H, Schulman S, Ginsberg J, Kearon C. Effect of patient's sex on risk of recurrent venous thromboembolism: a meta-analysis. Lancet 2006; 368: 371-8.
10. Douketis J, Tosetto A, Marcucci M, Baglin T, Cosmi B, Cushman M, Kyrle P, Poli D, Tait RC, Iorio A. Risk of recurrence after venous thromboembolism in men and women: patient level meta-analysis. BMJ 2011; 342: d813.
11. Nordstrom M, Lindblad B, Bergqvist D, Kjellstrom T. A prospective study of the incidence of deep-vein thrombosis within a defined urban population. J Intern Med 1992; 232: 155-60.
12. Naess IA, Christiansen SC, Romundstad P, Cannegieter SC, Rosendaal FR, Hammerstrom J. Incidence and mortality of venous thrombosis: a population-based study. J Thromb Haemost 2007; 5: 692-9.
13. Heit JA. The epidemiology of venous thromboembolism in the community: implications for prevention and management. J Thromb Thrombolysis 2006; 21: 23-9.
14. White RH, Zhou H, Murin S, Harvey D. Effect of ethnicity and gender on the incidence of venous thromboembolism in a diverse population in California in 1996. Thromb Haemost 2005; 93: 298-305.
15. Oger E. Incidence of venous thromboembolism: a community-based study in Western France. EPI-GETBP Study Group. Groupe d'Etude de la Thrombose de Bretagne Occidentale. Thromb Haemost 2000; 83: 657-60.
16. Silverstein MD, Heit JA, Mohr DN, Petterson TM, O'Fallon WM, Melton LJ III. Trends in the incidence of deep vein thrombosis and pulmonary embolism: a 25-year population-based study. Arch Intern Med 1998; 158: 585-93.
17. Spencer FA, Emery C, Joffe SW, Pacifico L, Lessard D, Reed G, Gore JM, Goldberg RJ. Incidence rates, clinical profile, and outcomes of patients with venous thromboembolism. The Worcester VTE study. J Thromb Thrombolysis 2009; 28: 401-9.
18. Bezemer ID, Bare LA, Doggen CJ, Arellano AR, Tong C, Rowland CM, Catanese J, Young BA, Reitsma PH, Devlin JJ, Rosendaal FR. Gene variants associated with deep vein thrombosis. JAMA 2008; 299: 1306-14.
19. Rothman KJ, Greenland S. Modern Epidemiology, 2nd edn. Philadelphia: Lippincott-Raven Publishers, 1998.
20. WHO. Medical Eligibility Criteria for Contraceptive Use Geneva: World Health Organization, 2004. ISBN 92 4 156266 8.
21. Kirmeyer SE, Hamilton BE. Transitions between childlessness and first birth: three generations of U.S. women. Vital Health Stat 2011; 2: 1-18.
22. Faber A, Bouvy ML, Loskamp L, van de Berg PB, Egberts TC, de Jong-van den Berg LT. Dramatic change in prescribing of hormone replacement therapy in the Netherlands after publication of the Million Women Study: a follow-up study. Br J Clin Pharmacol 2005; 60: 641-7.
23. Canonico M, Plu-Bureau G, Lowe GD, Scarabin PY. Hormone replacement therapy and risk of venous thromboembolism in postmenopausal women: systematic review and meta-analysis. BMJ 2008; 336: 1227-31.
24. van Hylckama Vlieg A, Helmerhorst FM, Vandenbroucke JP, Doggen CJ, Rosendaal FR. The venous thrombotic risk of oral contraceptives, effects of oestrogen dose and progestogen type: results of the MEGA case-control study. BMJ 2009; 339: b2921.
25. Pomp ER, Lenselink AM, Rosendaal FR, Doggen CJ. Pregnancy, the postpartum period and prothrombotic defects: risk of venous thrombosis in the MEGA study. J Thromb Haemost 2008a; 6: 632-7.
26. Roach RE, Lijfering WM, Rosendaal FR, Cannegieter SC, le Cessie S. Sex difference in risk of second but not of first venous thrombosis: paradox explained. Circulation 2014; 129: 51-6.
27. Lijfering WM, Rosendaal FR, Cannegieter SC. Risk factors for venous thrombosis - current understanding from an epidemiological point of view. Br J Haematol 2010; 149: 824-33.
28. Bezemer ID, Arellano AR, Tong CH, Rowland CM, Ireland HA, Bauer KA, Catanese J, Reitsma PH, Doggen CJ, Devlin JJ, Rosendaal FR, Bare LA. F9 Malmo, factor IX and deep vein thrombosis. Haematologica 2009; 94: 693-9.
29. Charchar FJ, Bloomer LD, Barnes TA, Cowley MJ, Nelson CP, Wang Y, Denniff M, Debiec R, Christofidou P, Nankervis S, Dominiczak AF, Bani-Mustafa A, Balmforth AJ, Hall AS, Erdmann J, Cambien F, Deloukas P, Hengstenberg C, Packard C, Schunkert H, et al. Inheritance of coronary artery disease in men: an analysis of the role of the Y chromosome. Lancet 2012; 379: 915-22.
30. Braekkan SK, Borch KH, Mathiesen EB, Njolstad I, Wilsgaard T, Hansen JB. Body height and risk of venous thromboembolism: the Tromso Study. Am J Epidemiol 2010a; 171: 1109-15.
31. Kluft C, Lansink M. Effect of oral contraceptives on haemostasis variables. Thromb Haemost 1997; 78: 315-26.
32. Middeldorp S, Meijers JC, van den Ende AE, van Enk A, Bouma BN, Tans G, Rosing J, Prins MH, Büller HR. Effects on coagulation of levonorgestrel- and desogestrel-containing low dose oral contraceptives: a cross-over study. Thromb Haemost 2000; 84: 4-8.
33. Vandenbroucke JP, Rosing J, Bloemenkamp KW, Middeldorp S, Helmerhorst FM, Bouma BN, Rosendaal FR. Oral contraceptives and the risk of venous thrombosis. N Engl J Med 2001; 344: 1527-35.
34. Brenner B. Haemostatic changes in pregnancy. Thromb Res 2004; 114: 409-14.
35. van Hylckama Vlieg A, Middeldorp S. Hormone therapies and venous thromboembolism: where are we now? J Thromb Haemost 2011; 9: 257-66.
36. Mahmoodi BK, Gansevoort RT, Næss IA, Lutsey PL, Brækkan SK, Veeger NJ, Brodin EE, Meijer K, Sang Y, Matsushita K, Hallan SI, Hammerstrøm J, Cannegieter SC, Astor BC, Coresh J, Folsom AR, Hansen JB, Cushman M. Association of mild to moderate chronic kidney disease with venous thromboembolism: pooled analysis of five prospective general population cohorts. Circulation 2012; 126: 1964-71.
37. den Heijer M, Koster T, Blom HJ, Bos GM, Briet E, Reitsma PH, Vandenbroucke JP, Rosendaal FR. Hyperhomocysteinemia as a risk factor for deep-vein thrombosis. N Engl J Med 1996; 334: 759-62.
38. de Bree A, Verschuren WM, Blom HJ, Kromhout D. Lifestyle factors and plasma homocysteine concentrations in a general population sample. Am J Epidemiol 2001; 154: 150-4.
39. Nygård O, Vollset SE, Refsum H, Stensvold I, Tverdal A, Nordrehaug JE, Ueland M, Kvåle G. Total plasma homocysteine and cardiovascular risk profile. The Hordaland Homocysteine Study. JAMA 1995; 274: 1526-33.
40. Severinsen MT, Johnsen SP, Tjonneland A, Overvad K, Dethlefsen C, Kristensen SR. Body height and sex-related differences in incidence of venous thromboembolism: a Danish follow-up study. Eur J Intern Med 2010; 21: 268-72.
41. Borch KH, Nyegaard C, Hansen JB, Mathiesen EB, Njølstad I, Wilsgaard T, Brækkan SK. Joint effects of obesity and body height on the risk of venous thromboembolism: the Tromso Study. Arterioscler Thromb Vasc Biol 2011; 31: 1439-44.
42. Glynn RJ, Rosner B. Comparison of risk factors for the competing risks of coronary heart disease, stroke, and venous thromboembolism. Am J Epidemiol 2005; 162: 975-82.
43. Rosengren A, Freden M, Hansson PO, Wilhelmsen L, Wedel H, Eriksson H. Psychosocial factors and venous thromboembolism: a long-term follow-up study of Swedish men. J Thromb Haemost 2008; 6: 558-64.
44. Pomp ER, le Cessie S, Rosendaal FR, Doggen CJ. Risk of venous thrombosis: obesity and its joint effect with oral contraceptive use and prothrombotic mutations. Br J Haematol 2007; 139: 289-96.
45. Lutsey PL, Cushman M, Heckbert SR, Tang W, Folsom AR. Longer legs are associated with greater risk of incident venous thromboembolism independent of total body height. The Longitudinal Study of Thromboembolism Etiology (LITE). Thromb Haemost 2011; 106: 113-20.
46. Lijfering WM, Flinterman LE, Vandenbroucke JP, Rosendaal FR, Cannegieter SC. Relationship between venous and arterial thrombosis: a review of the literature from a causal perspective. Semin Thromb Hemost 2011; 37: 885-96.
47. Holst AG, Jensen G, Prescott E. Risk factors for venous thromboembolism: results from the Copenhagen City Heart Study. Circulation 2010; 121: 1896-903.
48. Severinsen MT, Kristensen SR, Johnsen SP, Dethlefsen C, Tjonneland A, Overvad K. Smoking and venous thromboembolism: a Danish follow-up study. J Thromb Haemost 2009; 7: 1297-303.
49. Pomp ER, Rosendaal FR, Doggen CJ. Smoking increases the risk of venous thrombosis and acts synergistically with oral contraceptive use. Am J Hematol 2008b; 83: 97-102.
50. Wattanakit K, Lutsey PL, Bell EJ, Gornik H, Cushman M, Heckbert SR, Rosamond WD, Folsom AR. Association between cardiovascular disease risk factors and occurrence of venous thromboembolism. A time-dependent analysis. Thromb Haemost 2012; 108: 508-15.
51. Tsai AW, Cushman M, Rosamond WD, Heckbert SR, Polak JF, Folsom AR. Cardiovascular risk factors and venous thromboembolism incidence: the longitudinal investigation of thromboembolism etiology. Arch Intern Med 2002; 162: 1182-9.
52. Braekkan SK, Mathiesen EB, Njolstad I, Wilsgaard T, Stormer J, Hansen JB. Family history of myocardial infarction is an independent risk factor for venous thromboembolism: the Tromso study. J Thromb Haemost 2008; 6: 1851-7.
53. Goldhaber SZ, Grodstein F, Stampfer MJ, Manson JE, Colditz GA, Speizer FE, Willett WC, Hennekens CH. A prospective study of risk factors for pulmonary embolism in women. JAMA 1997; 277: 642-5.
54. Goldhaber SZ, Savage DD, Garrison RJ, Castelli WP, Kannel WB, McNamara PM, Gherardi G, Feinleib M. Risk factors for pulmonary embolism. The Framingham study. Am J Med 1983; 74: 1023-8.
55. Hansson PO, Eriksson H, Welin L, Svardsudd K, Wilhelmsen L. 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: 1886-90.
56. Lindqvist PG, Epstein E, Olsson H. The relationship between lifestyle factors and venous thromboembolism among women: a report from the MISS study. Br J Haematol 2009; 144: 234-40.
57. Migeon BR. The role of X inactivation and cellular mosaicism in women's health and sex-specific diseases. JAMA 2006; 295: 1428-33.
58. Bouman A, Heineman MJ, Faas MM. Sex hormones and the immune response in humans. Hum Reprod Update 2005; 11: 411-23.
59. Fish EN. The X-files in immunity: sex-based differences predispose immune responses. Nat Rev Immunol 2008; 8: 737-44.
60. Lussana F, Faioni EM, Mavilia C, Bucciarelli P, Brandi ML, Cattaneo M. Association of estrogen receptor-alpha genepolymorphisms with venous thrombosis. Haematologica 2006; 91: 279-80.
61. Oger E, Lacut K, Mercier B, Le Gal G, Leroyer C, Pasquier E, Férec C, Mottier D. Estrogen receptor alpha polymorphism and venous thromboembolism in male and female: data from the EDITH study. Thromb Res 2007; 119: 433-9.
62. Alessio AM, Hoehr NF, Siqueira LH, Ozelo MC, de Padua MA, Annichino-Bizzacchi JM. Association between estrogen receptor alpha and beta gene polymorphisms and deep vein thrombosis. Thromb Res 2007; 120: 639-45.
63. Rezende SM, Lijfering WM, Rosendaal FR, Cannegieter SC. Hematologic variables and venous thrombosis: red cell distribution width and blood monocyte count are associated with an increased risk. Haematologica 2014; 99: 194-200.
64. Eischer L, Tscholl V, Heinze G, Traby L, Kyrle PA, Eichinger S. Hematocrit and the risk of recurrent venous thrombosis: a prospective cohort study. PLoS ONE 2012; 7: e38705.
65. Fernández-Balsells MM, Murad MH, Lane M, Lampropulos JF, Albuquerque F, Mullan RJ, Agrwal N, Elamin MB, Gallegos-Orozco JF, Wang AT, Erwin PJ, Bhasin S, Montori VM. Clinical review 1: Adverse effects of testosterone therapy in adult men: a systematic review and meta-analysis. J Clin Endocrinol Metab 2010; 95: 2560-75.
66. Braekkan SK, Mathiesen EB, Njolstad I, Wilsgaard T, Hansen JB. Hematocrit and risk of venous thromboembolism in a general population. The Tromso study. Haematologica 2010b; 95: 270-5.
67. Svartberg J, Braekkan SK, Laughlin GA, Hansen JB. Endogenous sex hormone levels in men are not associated with risk of venous thromboembolism: the Tromso study. Eur J Endocrinol 2009; 160: 833-8.
68. Lijfering WM, Veeger NJ, Middeldorp S, Hamulyák K, Prins MH, Büller HR, van der Meer J. A lower risk of recurrent venous thrombosis in women compared with men is explained by sex-specific risk factors at time of first venous thrombosis in thrombophilic families. Blood 2009; 114: 2031-6.
69. Prandoni P, Noventa F, Ghirarduzzi A, Pengo V, Bernardi E, Pesavento R, Iotti M, Tormene D, Simioni P, Pagnan A. The risk of recurrent venous thromboembolism after discontinuing anticoagulation in patients with acute proximal deep vein thrombosis or pulmonary embolism. A prospective cohort study in 1, 626 patients. Haematologica 2007; 92: 199-205.
70. Eischer L, Eichinger S, Kyrle PA. Age at first venous thromboembolism and risk of recurrence: a prospective cohort study. Medicine (Baltimore) 2009; 88: 366-70.
71. Lidegaard O, Nielsen LH, Skovlund CW, Skjeldestad FE, Lokkegaard E. Risk of venous thromboembolism from use of oral contraceptives containing different progestogens and oestrogen doses: Danish cohort study, 2001-9. BMJ 2011; 343: d6423.
72. Bates SM, Greer IA, Middeldorp S, Veenstra DL, Prabulos AM, Vandvik PO. VTE, thrombophilia, antithrombotic therapy, and pregnancy: Antithrombotic Therapy and Prevention of Thrombosis, 9th ed: American College of Chest Physicians Evidence-Based Clinical Practice Guidelines. Chest 2012; 141: e691S-736S.
73. Arnsten JH, Gelfand JM, Singer DE. Determinants of compliance with anticoagulation: a case-control study. Am J Med 1997; 103: 11-7.
74. Gadisseur AP, Christiansen SC, van der Meer FJ, Rosendaal FR. The quality of oral anticoagulant therapy and recurrent venous thrombotic events in the Leiden Thrombophilia Study. J Thromb Haemost 2007; 5: 931-6.
75. Kovacs MJ, Kahn SR, Wells PS, Anderson DA, Chagnon I, LE Gal G, Solymoss S, Crowther M, Perrier A, Ramsay T, Betancourt MT, White RH, Vickars L, Rodger MA. Patients with a first symptomatic unprovoked deep vein thrombosis are at higher risk of recurrent venous thromboembolism than patients with a first unprovoked pulmonary embolism. J Thromb Haemost 2010; 8: 1926-32.
76. Pinede L, Ninet J, Duhaut P, Chabaud S, Demolombe-Rague S, Durieu I, Nony P, Sanson C, Boissel JP; Investigators of the "Durée Optimale du Traitement AntiVitamines K" (DOTAVK) Study. Comparison of 3 and 6 months of oral anticoagulant therapy after a first episode of proximal deep vein thrombosis or pulmonary embolism and comparison of 6 and 12 weeks of therapy after isolated calf deep vein thrombosis. Circulation 2001; 103: 2453-60.
77. Schulman S, Rhedin AS, Lindmarker P, Carlsson A, Lärfars G, Nicol P, Loogna E, Svensson E, Ljungberg B, Walter H. A comparison of six weeks with six months of oral anticoagulant therapy after a first episode of venous thromboembolism. Duration of Anticoagulation Trial Study Group. N Engl J Med 1995; 332: 1661-5.
78. Anderson FA Jr, Wheeler HB, Goldberg RJ, Hosmer DW, Patwardhan NA, Jovanovic B, Forcier A, Dalen JE. 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: 933-8.
79. Lango Allen H, Estrada K, Lettre G, Berndt SI, Weedon MN, Rivadeneira F, Willer CJ, Jackson AU, Vedantam S, Raychaudhuri S, Ferreira T, Wood AR, Weyant RJ, Segrè AV, Speliotes EK, Wheeler E, Soranzo N, Park JH, Yang J, Gudbjartsson D, et al. Hundreds of variants clustered in genomic loci and biological pathways affect human height. Nature 2010; 467: 832-8.
80. Eichinger S, Heinze G, Jandeck LM, Kyrle PA. Risk assessment of recurrence in patients with unprovoked deep vein thrombosis or pulmonary embolism: the Vienna prediction model. Circulation 2010; 121: 1630-6.
81. Tosetto A, Iorio A, Marcucci M, Baglin T, Cushman M, Eichinger S, Palareti G, Poli D, Tait RC, Douketis J. Predicting disease recurrence in patients with previous unprovoked venous thromboembolism: a proposed prediction score (DASH). J Thromb Haemost 2012; 10: 1019-25.