Risk factors for venous thromboembolism in women

Т. Н. Тутченко, Т. Ф Татарчук, И. А. Родионова, С. И. Регеда

Abstract


The scientific works of recent years have clearly demonstrated the importance of considering various clinical problems from the perspective of the gender approach, since the pathogenesis of diseases and the metabolism of medications are much different in women and men. This article provides an overview of current scientific literature on etiology and factors predisposing to the development of venous thromboembolism (VTE) in women. The spectrum of factors predisposing to VTE is extremely wide – besides such well known factors as immobilization, oncopathology, estrogen-containing medications, there are many less known influences, but nevertheless capable of playing a critical role for VTE such as the intake of certain non-hormonal drugs. Particular attention is paid to the latest research and key positions of the consensus documents of leading professional societies on the prevention of VTE in users of combined hormonal contraceptives and menopausal hormone therapy, as well as the association of such widespread pathologies as metabolic syndrome and polycystic ovary syndrome with VTE.

In recent years, there has been a reassessment of certain risk factors for VTE, the role of hereditary and acquired forms of thrombophilia as the cause of complications of pregnancy or factor influencing management of gynecological disorders significantly increased.

In women in such clinical situations as family planning counseling, preconception councelling, planning of operative treatment and hospitalization, menopausal replacement therapy, glucocorticoids and certain non-hormonal drugs prescription comprehensive assessment of the combination of VTE risk factors helps prevent the development of this dangerous pathology by correcting the management plan and applying modern anticoagulants.

The purpose of the article is to present new theoretical positions that help physicians understand the causes of venous thrombosis and evaluate the risks of gynecological patients in office and inhospital settings.  


Keywords


venous thromboembolism; risk factors; thrombogenic mutations; hormonal contraception; menopausal hormone therapy; PCOS; metabolic syndrome

References


Wendelboe, A.M., McCumber, M., Hylek, E.M., et al; ISTH Steering Committee for World Thrombosis Day. “Global public awareness of venous thromboembolism.” J Thromb Haemost 13 (2015): 1365–71.

Goldhaber, S.Z. “Venous thromboembolism: epidemiology and magnitude of the problem.” Best Pract Res Clin Haematol 25 (2012): 235–42.

ISTH Steering Committee for World Thrombosis Day. “Thrombosis: a majorcontributor to the global disease burden.” J Thromb Haemost 12 (2014): 1580–9.

Naess, I.A., Christiansen, S.C., Romundstad, P., et al. “Incidence and mortality of venous thrombosis: a population-based study.” J Thromb Haemost 5 (2007): 692–9.

Girolami, A., et al. “Drug-induced thrombophilic or prothrombotic states: an underestimated clinical problem that involves both legal and illegal compounds.” Clinical and Applied Thrombosis/Hemostasis 23.7 (2017): 775–85.

Silverstein, M.D., Heit, J.A., Mohr, D.N., et al. “Trends in the incidence of deep vein thrombosis and pulmonary embolism: a 25-year population based study.” Arch Intern Med 158

(1998): 585–93.

Kearon, C., Akl, E.A., Comerota, A.J., et al. “Antithrombotic therapy for VTE disease.” Chest 141 (2012): e419S–e494S.

Boutitie, F., Pinede, L., Schulman, S., et al. “Influence of preceding length of anticoagulant treatment and initial presentation of venous thromboembolism on risk of recurrence after stopping treatment: analysis of individual participants’ data from seven trials.” BMJ 342 (2011): d3036.

Regitz-Zagrosek, V., Kararigas, G. “Mechanistic pathways of sex differences in cardiovascular disease.” Physiological reviews 97.1 (2016): 1–37.

Anderson, G.D. “Gender differences in pharmacological response.” International review of neurobiology 83 (2008): 1–10.

“Russian clinical guidelines for the diagnosis, treatment and prevention of venous thromboembolic complications (VTEC).” Phlebology 4.9 Vol. 2 (2015): 1.

Zöller, B., et al. “Family history of venous thromboembolism as a risk factor and genetic research tool.” Thrombosis and haemostasis 114.05 (2015): 890–900.

Gerhardt, A., et al. “Hereditary risk factors for thrombophilia and probability of venous thromboembolism during pregnancy and the puerperium.” Blood 128.19 (2016): 2343–9.

Suchon, P., et al. “Risk factors for venous thromboembolism in women under combined oral contraceptive.” Thrombosis and haemostasis 115.1 (2016).

McDaid, A., Logette, E., Buchillier, V., et al. “Risk prediction of developing venous thrombosis in combined oral contraceptive users.” PLoS ONE 12.7 (2017): e0182041.

Preston, A.E., Barr, A. “The plasma concentration of factor VIII in the normal population.” Br J Haematol 10 (1964): 238–45.

Moeller, A., et al. “Influence of ABO blood groups on primary hemostasis.” Transfusion 41 (2001): 56–60.

O’Donnell, J.S., Lasffan, M.A. “The relationship between ABO histo-blood group, factor VIII and von Willebrand factor.” Transfus Med 11 (2001): 343–51.

Gill, J.C., et al. “The effect of ABO blood group on the diagnosis of von Willebrand disease.” Blood 69 (1987): 1691–5.

Jenkins, P.V., O’Donnell, J.S. “ABO blood group determines plasma von Willebrand factor levels: a biologic function after all?” Transfusion 46 (2006): 1836–44.

Dick, W., et al. “Interrelations of thrombo-embolic diseases and blood group distribution.” Thromb Diath Haemorrh 9 (1963): 472–4.

Wu, O., et al. “ABO(H) blood groups and vascular disease: a systematic review and meta-analysis.” J Thromb Haemost 6 (2008): 62–9.

Dentali, F., et al. “Non-O blood type is the commonest genetic risk factor for VTE: results from a meta-analysis of the literature.” Semin Thromb Hemost 38

(2012): 535–48.

Vasan, S.K., et al. “ABO blood group and risk of thromboembolic and arterial

disease: a study of 1.5 million blood donors.” Circulation (2016): CIRCULATIONAHA-115.

Guimaraes, D.A., dos Santos, M.S., Gomes, K.B., et al. “Interaction between Oral Estrogen plus Progestogen Therapy and ABO Blood Groups on Coagulation Activation in Postmenopausal Women.” Menopause 19 (2012): 339–45. DOI: 10.1097/gme.0b013e31822b721f

Gavish, I., Brenner, B. “Air Travel and Risk of Thromboembolism.” Internal and Emergency Medicine 6 (2011): 113–6. DOI: 10.1007/s11739-010-0474-6

Cannegieter, S.C., Doggen, C.J.M., van Houwelingen, H.C., Rosendaal, F.R. “Travel-Related Venous Thrombosis: Results from a Large Population-Based Case Control Study (MEGA Study).” PLoS Medicine 3 (2006): e307. DOI: 10.1371/journal.pmed.0030307

Martinelli, I., Taioli, E., Battaglioli, T., et al. “Risk of Venous Thromboembolism after Air Travel: Interaction with Thrombophilia and Oral Contraceptives.” Archives of Internal Medicine 163 (2003): 2771–4. DOI: 10.1001/archinte.163.22.2771

Svartberg, J., Braekkan, S.K., Laughlin, G.A., Hansen, J.-B. “Endogenous sex hormone levels in men are not associated with risk of venous thromboembolism: the Tromso study.” Eur J Endocrinol 160 (2009): 833–8.

Holmegard, H.N., et al. “Endogenous sex hormones and risk of venous thromboembolism in women and men.” Journal of Thrombosis and Haemostasis 12.3 (2014): 297–305.

Harrington, L.B., et al. “Cross‐sectional association of endogenous steroid hormone, sex hormone‐binding globulin, and precursor steroid levels with hemostatic factor levels in postmenopausal women.” Journal of Thrombosis and Haemostasis 15.1 (2017): 80–90.

Nheu, L., Nazareth, L., Xu, G.Y., et al. “Physiological effects of androgens on human vascular endothelial and smooth muscle cells in culture.” Steroids 76 (2011): 1590–6.

Gavin, K.M., Seals, D.R., Silver, A.E., Moreau, K.L. “Vascular endothelial estrogen receptor alpha is modulated by estrogen status and related to endothelial function and endothelial nitric oxide synthase in healthy women.” J Clin Endocrinol Metab 94 (2009): 3513–20.

Bahamondes, L., Bahamondes, M.V., Shulman, L.P. “Non-contraceptive benefits of hormonal and intrauterine reversible contraceptive methods.” Human reproduction update 21.5 (2015): 640–51.

World Health Organization. Medical Eligibility Criteria for Contraceptive Use, 4th edition. Geneva. WHO (2009). Available from: [http://www.who.int/reproductive_health/publications/mec/family_ planning/9789241563888/en/index.html].

Stegemanet, B.H., et al. “Different combined oral contraceptives and the risk of venous thrombosis: systematic review and network meta-analysis.” BMJ (2013).

Goodyear-Smith, A., Arroll, B. “Termination of pregnancy following panic-stopping of oral contraceptives.” Contraception 66 (2002): 163–7.

Baratloo, A., et al. “The Risk of Venous Thromboembolism with Different Generation of Oral Contraceptives; a Systematic Review and Meta-Analysis.” Emergency 2 (2014).

Martínez, F., et al. “Venous and pulmonary thromboembolism and combined hormonal contraceptives. Systematic review and meta-analysis.” Eur J Contracept Reprod Health Care 17.1 (2012): 7–29.

Pfeifer, S., et al. “Combined hormonal contraception and the risk of venous thromboembolism: a guideline.” Fertility and sterility 107.1 (2017): 43–51.

Bitzer, J., et al. “Statement on combined hormonal contraceptives containing third-or fourth-generation progestogens or cyproterone acetate, and the associated risk of thromboembolism.” J Fam Plann Reprod Health Care 39.3 (2013): 156–9.

Reid, R.L., Westhoff, C., Mansour, D., et al. “Oral contraceptives and venous thromboembolism – Consensus opinion from an international workshop held in Berlin, Germany in December 2009.” J Fam Plann Reprod Health Care 36 (2010): 117–22.

Jensen, J.T., Trussell, J. “Communicating risk: does scientific debate compromise safety.” Contraception 86 (2012): 327–9.

Heinemann, K., Heinemann, L.A. “Comparative risks of venous thromboembolism among users of oral contraceptives containing drospirenone and levonorgestrel.” J Fam Plann Reprod Health Care 37 (2011): 132–5.

Dinger, J., Shapiro, S. “Combined oral contraceptives, venous thromboembolism, and the problem of interpreting large but incomplete datasets.” J Fam Plann Reprod Health Care 38 (2012): 2–6.

Van Hylckama Vlieg, A., Helmerhorst, F., Rosendaal, F. “The Risk of Deep Venous Thrombosis Associated with Injectable Depot-Medroxyprogesterone Acetate Contraceptives or a Levonorgestrel Intrauterine Device.” Arteriosclerosis Thrombosis and Vascular Biology 30 (2010): 2297–300. DOI: 10.1161/ATVBAHA.110.211482

Mantha, S., Karp, R., Raghavan, V., et al. “Assessing the Risk of Venous Thromboembolic Events in Women Taking Progestin-Only Contraception: A Meta-Analysis.” BMJ 345 (2012): e4944. DOI: 10.1136/bmj.e4944

Bergendal, A., Odlind, V., Persson, I., Kieler, H. “Limited Knowledge on Progestogen-Only Contraception and Risk of Venous Thromboembolism.” Acta Obstetricia et Gynecologica 88 (2009): 261–6. DOI: 10.1080/00016340902730375

Rossouw, J.E., Anderson, G.L., Prentice, R.L., et al; Writing Group for the Women’s Health Initiative Investigators. “Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women’s Health Initiative randomized controlled trial.” JAMA 288.3 (2002): 321–33.

Anderson, G.L., Limacher, M., Assaf, A.R., et al; Women’s Health Initiative Steering Committee. “Effects of conjugated equine estrogen in postmenopausal women with hysterectomy: the Women’s Health Initiative randomized controlled trial.” JAMA 291.14 (2004): 1701–12.

Vickers, M.R., MacLennan, A.H., Lawton, B., et al; WISDOM group. “Main morbidities recorded in the women’s international study of long duration oestrogen after menopause (WISDOM): a randomised controlled trial of hormone replacement therapy in postmenopausal women.” BMJ 335.7613 (2007): 239.

Cushman, M., Kuller, L.H., Prentice, R., et al; Women’s Health Initiative Investigators.

“Estrogen plus progestin and risk of venous thrombosis.” JAMA 292.13 (2004):1573–80.

Pérez Gutthann, S., García Rodríguez, L.A., Castellsague, J., Duque Oliart, A. “Hormone replacement therapy and risk of venous thromboembolism: population based case-control study.” BMJ 314.7083 (1997): 796–800.

Høibraaten, E., Qvigstad, E., Arnesen, H., et al. “Increased risk of recurrent venous thromboembolism during hormone replacement therapy – results of the randomized, double-blind, placebo-controlled estrogen in venous thromboembolism trial (EVTET).” Thromb Haemost 84.6 (2000): 961–7.

Canonico, M., Fournier, A., Carcaillon, L., et al. “Postmenopausal hormone therapy and risk of idiopathic venous thromboembolism: results from the E3N cohort study.” Arterioscler Thromb Vasc Biol 30.2 (2010): 340–5.

Eischer, L., Eichinger, S., Kyrle, P.A. “The risk of recurrence in women with venous thromboembolism while using estrogens: a prospective cohort study.” J Thromb Haemost 12.5 (2014): 635–40.

Scarabin, P.Y., Oger, E., Plu-Bureau, G.; EStrogen and THromboEmbolism Risk Study Group. “Differential association of oral and transdermal oestrogen-replacement therapy with venous thromboembolism risk.” Lancet 362.9382 (2003): 428–32.

Roach, R.E., Lijfering, W.M., Helmerhorst, F.M., et al. “The risk of venous thrombosis in women over 50 years old using oral contraception or postmenopausal hormone therapy.” J Thromb Haemost 11.1 (2013): 124–31.

Renoux, C., Dell’Aniello, S., Suissa, S. “Hormone replacement therapy and the risk of venous thromboembolism: a population-based study.” J Thromb Haemost 8.5 (2010): 979–86.

Laliberté, F., Dea, K., Duh, M.S., et al. “Does the route of administration for estrogen hormone therapy impact the risk of venous thromboembolism? Estradiol transdermal system versus oral estrogen-only hormone therapy.” Menopause 18.10 (2011): 1052–9.

Hemelaar, M., Rosing, J., Kenemans, P., et al. “Less effect of intranasal than oral hormone therapy on factors associated with venous thrombosis risk in healthy postmenopausal women.” Arterioscler Thromb Vasc Biol 26.7 (2006): 1660–6.

Baber, R.J., Panay, N., Fenton, A. “2016 IMS Recommendations on women’s midlife health and menopause hormone therapy.” Climacteric 19.2 (2016): 109–50.

Patrassi, G.M., Sartori, M.T., Viero, M.L., et al. “The fibrinolytic potential in patients with Cushing’s disease: a clue to their hypercoagulable state.” Blood Coagul Fibrinolysis 3.6 (1992): 789–93.

Dal Bo Zanon, R., Fornasiero, L., et al. “Clotting changes in Cushing’s syndrome: elevated factor VIII activity.” Folia Haematol Int Mag Klin Morphol Blutforsch 110.2 (1983): 268–77.

Casonato, A., Pontara, E., Boscaro, M., et al. “Abnormalities of von Willebrand factor are also part of the prothrombotic state of Cushing’s syndrome.” Blood Coagul Fibrinolysis 10.3 (1999): 145–51.

Boscaro, M., Sonino, N., Scarda, A., et al. “Anticoagulant prophylaxis markedly reduces thromboembolic complications in Cushing’s syndrome.” J Clin Endocrinol Metab 87.8

(2002): 3662–6.

Mor, Y.S., Schenker, J.G. “Ovarian hyperstimulation syndrome and thrombotic events.” Am J Reprod Immunol 72.6 (2014): 541–8.

Girolami, A., Scandellari, R., Tezza, F., et al. “Arterial thrombosis in young women after ovarian stimulation: case report and review of the literature.” J Thromb Thrombolysis 24.2 (2007): 169–74.

Westerlund, E., Henriksson, P., Wallen, H., et al. “Detection of a procoagulable state during controlled ovarian hyperstimulation for in vitro fertilization with global assays of haemostasis.” Thromb Res 130.4 (2012): 649–53.

Ramot, Y., Nyska, A., Spectre, G. “Drug-induced thrombosis: an update.” Drug Saf 36.8 (2013): 585–603.

Klocking, H.P. “Generation of thrombophilic states by drugs.” Folia Haematol Int Mag Klin Morphol Blutforsch 111.4 (1984): 441–9.

Ramot, Y., Nyska, A. “Drug-induced thrombosis – experimental, clinical, and mechanistic considerations.” Toxicol Pathol 35.2 (2007): 208–25.

Taparia, M., Cordingley, F.T., Leahy, M.F. “Pulmonary embolism associated with tranexamic acid in severe acquired haemophilia.” Eur J Haematol 68.5 (2002): 307–9.

Mihalache, R.M., Ames, P.R. “Deep vein thrombosis, tranexamic acid, and a negative d-Dimer.” Clin Appl Thromb Hemost 18.6 (2012): 666–7.

Sundstrom, A., Seaman, H., Kieler, H., Alfredsson, L. “The risk of venous thromboembolism associated with the use of tranexamic acid and other drugs used to treat menorrhagia: a case-control study using the General Practice Research Database.” BJOG 116.1 (2009): 91–7.

Woo, K.S., Tse, L.K., Woo, J.L., Vallance-Owen, J. “Massive pulmonary thromboembolism after tranexamic acid antifibrinolytic therapy.” Br J Clin Pract 43.12 (1989): 465–6.

Endo, Y., Nishimura, S., Miura, A. “Deep-vein thrombosis induced by tranexamic acid in idiopathic thrombocytopenic purpura.” JAMA 259.24 (1988): 3561–2.

Cuzick, J. “Tamoxifen and the factor V Leiden mutation.” J Natl Cancer Inst 102.13 (2010): 918–9.

Erman, M., Abali, H., Oran, B., et al. “Tamoxifen-induced tissue factor pathway inhibitor reduction: a clue for an acquired thrombophilic state?” Ann Oncol 15.11 (2004): 1622–6.

Hutchison, R.L., Rayan, G.M. “Thrombosis of digital arteries associated with tamoxifen use: case report.” J Reconstr Microsurg 28.2 (2012): 145–8.

Shah, V.P., Chegini, H.A., Vishneski, S.R., et al. “Tamoxifen promotes superoxide production in platelets by activation of PI3-kinase and NADPH oxidase pathways.” Thromb Res 129.1 (2012): 36–42.

Dicato, M. “Venous thromboembolic events and erythropoies is stimulating agents: an update.” Oncologist 13 Suppl. 3 (2008): 11–5.

Karabinos, I.K., Koulouris, S., Kranidis, A., et al. “Spontaneous thrombus formation in a normal left ventricle following administration of large doses of epoetin.” Hellenic J Cardiol 48.1 (2007): 44–6.

Lippi, G., Franchini, M., Favaloro, E.J. “Thrombotic complications of erythropoiesis-stimulating agents.” Semin Thromb Hemost 36.5 (2010): 537.

Darnige, L., Lillo-Le Louet, A. “Treatments with immunoglobulin and thrombotic adverse events.” Rev Med Interne 35.1 (2014): 39–44. [Article in French]

Lorenzana, A., Armin, S., Sharma, A., et al. “Cerebral infarctions after intravenous immunoglobulin therapy for ITP in a child.” Pediatr Neurol 50.2 (2014): 188–91.

Amiral, J., Bridey, F., Dreyfus, M., et al. “Platelet factor 4 complexed toheparinisthe target for antibodies generated inheparin-induced thrombocytopenia.” Thromb Haemost 68.1 (1992): 95–6.

Warkentin, T.E., Greinacher, A. “Heparin-induced thrombocytopenia: recognition, treatment, and prevention: the Seventh ACCP Conference on Antithrombotic and Thrombolytic Therapy.” Chest 126 Suppl. 3 (2004): 311–37.

Girolami, B., Girolami, A. “Heparin-induced thrombocytopenia: a review.” Semin Thromb Hemost 32.8 (2006): 803–9.

Warkentin, T.E., Sheppard, J.A., Manheim, J.C. “HIT complicating fondaparinux prophylaxis: fondaparinux-dependent platelet activation as a marker for fondaparinux-induced HIT.” Thromb Haemost 112.6 (2014): 1319–22.

Solak, Y., Demircioglu, S., Polat, I., et al. “Heparin-induced thrombocytopenia in a hemodialysis patient treated with fondaparinux: nephrologists between two fires.” Hemodial Int 17.2 (2013): 320–3.

Marwali, M.R., Mehta, J.L. “COX-2 inhibitors and cardiovascular risk. Inferences based on biology and clinical studies.” Thromb Haemost 96.4 (2006): 401–6.

Nissen, S.E. “Adverse cardiovascular effects of rofecoxib.” N Engl J Med 355.2 (2006): 203–4.

Weir, M.R., Sperling, R.S., Reicin, A., Gertz, B.J. “Selective COX-2 inhibition and cardiovascular effects: a review of the rofecoxib development program.” Am Heart J 146.4 (2003): 591–604.

Krotz, F., Struthmann, L. “A review on the risk of myocardial infarction associated with the NSAID diclofenac.” Cardiovasc Hematol Disord Drug Targets 10.1 (2010): 53–6.

Chen, L.C., Ashcroft, D.M. “Risk of myocardial infarction associated with selective COX-2 inhibitors: meta-analysis of randomised controlled trials.” Pharmacoepidemiol Drug Saf 16.7 (2007): 762–72.

Bergendal, A., et al. “Non‐steroidal anti‐inflammatory drugs and venous thromboembolism in women.” Pharmacoepidemiology and drug safety 22.6 (2013): 658–66.

Parkin, L., et al. “Antidepressants, depression, and venous thromboembolism risk: large prospective study of UK women.” Journal of the American Heart Association 6.5 (2017): e005316.

Pomp, E., Lenselink, A., Rosendaal, F., Doggen, C. “Pregnancy, the Postpartum Period and Prothrombotic Defects: Risk of Venous Thrombosis in the MEGA Study.” Journal of Thrombosis and Haemostasis 6 (2008): 632–7.

Reid, R.L., Westhoff, C., Mansour, D., et al. “Oral Contraceptives and Venous Thromboembolism Consensus Opinion from an International Workshop held in Berlin, Germany in December 2009.” Journal of Family Planning and Reproductive Health Care 36 (2010): 117–22.

Royal College of Obstetricians and Gynaecologists. Green-top Guideline No. 37b (2015). Thromboembolic disease in pregnancy and the puerperium: acute management. Available from: [https://www.rcog.org.uk/en/guidelines-research-services/guidelines/gtg37b/].

Bates, S.M., et al. “Guidance for the treatment and prevention of obstetric-associated venous thromboembolism.” Journal of thrombosis and thrombolysis 41.1 (2016): 92–128.

Tsai, A., Cushman, M., Rosamond, W., et al. “Cardiovascular Risk Factors and Venous Thromboembolism Incidence: The Longitudinal Investigation of Thromboembolism Etiology.” Archives of Internal Medicine 162 (2002): 1182–9. DOI: 10.1001/archinte.162.10.1182

Hoist, A., Jensen, G., Prescott, E. “Risk Factors for Venous Thromboemobolism: A. Waddington et al. Results from the Copenhagen City Heart Study.” Circulation 121 (2010): 1896–1903. DOI: 10.1161/CIRCULATIONAHA.109.921460

Hart, R., Doherty, D.A. “The potential implications of a PCOS diagnosis on a woman’s long-term health using data linkage.” The Journal of Clinical Endocrinology & Metabolism 100.3 (2015): 911–19.

Boumosleh, J.M., et al. “Metabolic Concomitants of Obese and Nonobese Women With Features of Polycystic Ovarian Syndrome.” Journal of the Endocrine Society 1.12 (2017): 1417–27.

Okoroh, E., Hooper, W., Atrash, H., et al. “Is Polycystic Ovary Syndrome another Risk Factor for Venous Thromboembolism? United States, 2003-2008.” American Journal of Obstetrics and Gynecology 207 (2012): 377.e1-377.e8. DOI: 10.1016/j. ajog.2012.08.007

Bird, S.T., Hartzema, A.G., Brophy, J.M., et al. “Risk of Venous Thromboembolism in Women with Polycystic Ovarian Syndrome: A Population-Based Matched Cohort Analysis.” CMAJ 185 (2013): E115–E120. DOI: 10.1503/cmaj.120677

Seaman, H.E., de Vries, C.S., Farmer, R.D.T. “The Risk of Venous Thromboembolism in Women Prescribed Cyproterone Acetate in Combination with Ethinyl Estradiol: A Nested Cohort Analysis and Case Control Study.” Human Reproduction 18 (2003): 522–6. DOI: 10.1093/humrep/deg120

Okoroh, E.M., et al. “Assessing the intersection of cardiovascular disease, venous thromboembolism, and polycystic ovary syndrome.” Thrombosis research 136.6 (2015): 1165–8.

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).” JAMA 285 (2001): 2486–96.

Gami, A.S., Witt, B.J., Howard, D.E., et al. “Metabolic syndrome and risk of incident cardiovascular events and death: a systematic review and meta-analysis of longitudinal studies.” J Am Coll Cardiol 49 (2007): 403–14.

Ageno, W., Prandoni, P., Romualdi, E., et al. “The metabolic syndrome and the risk of venous thrombosis: a case-control study.” J Thromb Haemost 4 (2006): 1914–18.

Ambrosetti, M., Ageno, W., Salerno, M., et al. “Metabolic syndrome as a risk factor for deep vein thrombosis after acute cardiac conditions.” Thromb Res 120 (2007): 815–18.

Ay, C., Tengler, T., Vormittag, R., et al. “Venous thromboembolism – a manifestation of the metabolic syndrome.” Haematologica 92 (2007): 374–80.

Jang, M.J., Choi, W.I., Bang, S.M., et al. “Metabolic syndrome is associated with venous thromboembolism in the Korean population.” Arterioscler Thromb Vasc Biol 29 (2009): 311–5.

Borch, K.H., Braekkan, S.K., Mathiesen, E.B., et al. “Abdominal obesity is essential for the risk of venous thromboembolism in the metabolic syndrome: the Tromsø study.” J Thromb Haemost 7 (2009): 739–45.

Steffen, L.M., Cushman, M., Peacock, J.M., et al. “Metabolic syndrome and risk of venous thromboembolism: Longitudinal Investigation of Thromboembolism Etiology.” J Thromb Haemost 7 (2009): 746–51.

Vayá, A., Martínez-Triguero, M.L., España, F., et al. “The metabolic syndrome and its individual components: its association with venous thromboembolism in a Mediterranean population.” Metab Syndr Relat Disord 9 (2011): 197–201.

Ageno, W., et al. “Association between the metabolic syndrome, its individual components, and unprovoked venous thromboembolism: results of a patient-level meta-analysis.” Arteriosclerosis, thrombosis, and vascular biology (2014): ATVBAHA-114.

Walker, A.J., et al. “Incidence of venous thromboembolism in patients with cancer – a cohort study using linked United Kingdom databases.” Eur J Cancer 49 (2013): 1404–13.

Heit, J.A., et al. “Risk factors for deep vein thrombosis and pulmonary embolism: a population-based case-control study.” Arch Intern Med 160 (2000): 809–15.

Khorana, A.A., et al. “Thromboembolism is a leading cause of death in cancer patients receiving outpatient chemotherapy.” J Thromb Haemost 5 (2007): 632–4.

Heit, J.A., et al. “Relative impact of risk factors for deep vein thrombosis and pulmonary embolism: a population-based study.” Arch Intern Med 162 (2002): 1245–8.

Cronin-Fenton, D.P., et al. “Hospitalisation for venous thromboembolism in cancer patients and the general population: a population-based cohort study in Denmark, 1997–2006.” Br J Cancer 103 (2010): 947–53.

Riedl, J., et al. “Association of mean platelet volume with risk of venous thromboembolism and mortality in patients with cancer. Results from the Vienna Cancer and Thrombosis Study (CATS).” Thromb Haemost 111 (2014): 670–8.

Ay, C., Pabinger, I., Cohen, A.T. “Cancer-associated venous thromboembolism: burden, mechanisms, and management.” Thrombosis and haemostasis 117.02 (2017): 219–30.

Kearon, C., et al. “Antithrombotic Therapy for VTE Disease: CHEST Guideline and Expert Panel Report.” Chest 149 (2016): 315–52.

Mandala, M., et al. “Venous thromboembolism (VTE) in cancer patients. ESMO clinical recommendations for prevention and management.” Thromb Res 125 Suppl. 2 (2010): S117–119.

NCCN Clinical Practical Guidelines in Oncology. Cancer-associated venous thromboembolic disease version 1.2014. Available from: [http://www.nccn.org/ professionals/physician_gls/f_ guidelines.asp].

Farge, D., et al. “International clinical practice guidelines for the treatment and prophylaxis of venous thromboembolism in patients with cancer.” J Thromb Haemost 11 (2013): 56–70.

Lyman, G.H., et al. “Venous thromboembolism prophylaxis and treatment in patients with cancer: American Society of Clinical Oncology clinical practice guideline update.” J Clin Oncol 31 (2013): 2189–204.

Watson, H.G., et al. “Guideline on aspects of cancer-related venous thrombosis.” Br J Haematol 170 (2015): 640–8.

Stevens, S.M., et al. “Guidance for the evaluation and treatment of hereditary and acquired thrombophilia.” Journal of thrombosis and thrombolysis 41.1 (2016): 154–64.

Christiansen, S.C., Cannegieter, S.C., Koster, T., et al.

“Thrombophilia, clinical factors, and recurrent venous thrombotic events.” JAMA 293 (2005): 2352–61.

Simone, B., De Stefano, V., Leoncini, E., et al. “Risk of venous thromboembolism associated with single and combined effects of factor V Leiden, prothrombin 20210A and methylenetethraydrofolate reductase C677T: a meta-analysis involving over 11,000 cases and 21,000 controls.” Eur J Epidemiol 28 (2013): 621–47.

Mahmoodi, B.K., Brouwer, J.L., Ten Kate, M.K., et al. “A prospective cohort study on the absolute risks of venous thromboembolism and predictive value of screening asymptomatic relatives of patients with hereditary deficiencies of protein S, protein C or antithrombin.” J Thromb Haemost 8 (2010): 1193–200.

Pernod, G., Biron-Andreani, C., Morange, P.E., et al. “Recommendations on testing for thrombophilia in venous thromboembolic disease: a French consensus guideline.” J Mal Vasc 34 (2009): 156–203.

Merriman, L., Greaves, M. “Testing for thrombophilia: an evidence-based approach.” Postgrad Med J 82 (2006): 699–704.

Wu, O., Robertson, L., Twaddle, S., et al. “Screening for thrombophilia in high-risk situations: a meta-analysis and costeffectiveness analysis.” Br J Haematol 131 (2005): 80–90.

Bates, S.M., Greer, I.A., Middeldorp, S., et al. “VTE, thrombophilia, antithrombotic therapy, and pregnancy.” Chest 141 (2012): e691S–e736S.

Cohen, W., Castelli, C., Suchon, P., et al. “Risk assessment of venous thrombosis in families with known hereditary thrombophilia: the MARseilles-NImes prediction model.” J Thromb Haemost 12 (2014): 138–46.

Davis, S.M., Branch, D.W. “Thromboprophylaxis in pregnancy: who and how?” Obstet Gynecol Clin North Am 37 (2010): 333–43.

Wu, O., Robertson, L., Langhorne, P., et al. “Oral contraceptives, hormone replacement therapy, thrombophilias and risk of venous thromboembolism: a systematic review. The thrombosis: risk and Economic Assessment of Thrombophilia Screening (TREATS) Study.” Thromb Haemost 94 (2005): 17–25.

Suchon, P., et al. “Genetic risk factors for venous thrombosis in women using combined oral contraceptives: update of the PILGRIM study.” Clinical genetics 91.1 (2017): 131–6.

Higgins, J.P., Thompson, S.G., Deeks, J.J., Altman, D.G. “Measuring inconsistency in meta analyses.” BMJ 327 (2003): 557–60.

Rinde, L.B., Lind, C., Smabrekke, B., et al. “Impact of incident myocardial infarction on risk of venous thromboembolism: the Tromsö study.” J Thromb Haemost 14 (2016): 1183–91.

Hosseini, S., Kalantar, E., Hosseini, M.S., et al. “Genetic risk factors in patients with deep venous thrombosis, a retrospective case control study on Iranian population.” Thromb J 13 (2015): 35.

Margaglione, M., Cappucci, G., Colaizzo, D., et al. “The PAI-1 gene locus 4G/5G polymorphism is associated with a family history of coronary artery disease.” Arterioscler Thromb Vasc Biol 18 (1998): 152–6.

Sumner, J.A., Kubzansky, L.D., Elkind, M.S., et al. “Trauma exposure and posttraumatic stress disorder symptoms predict onset of cardiovascular events in women.” Circulation 132 (2015): 251–9.

Koupenova, M., et al. “Thrombosis and platelets: an update.” European heart journal 38.11 (2016): 785–91.

Chu, S.G., Becker, R.C., Berger, P.B., et al. “Mean platelet volume as a predictor of cardiovascular risk: a systematic review and meta-analysis.” J Thromb Haemost 8 (2010): 148–56.

Braekkan, S.K., Mathiesen, E.B., Njolstad, I., et al. “Mean platelet volume is a risk factor for venous thromboembolism: the Tromsö Study, Tromsö, Norway.” J Thromb Haemost 8 (2010): 157–62.

Tichelaar, Y.I., Kluin-Nelemans, H.J., Meijer, K. “Infections and inflammatory diseases as risk factors for venous thrombosis. A systematic review.” Thromb Haemost 107 (2012): 827–37.

Bunce, P.E., High, S.M., Nadjafi, M., et al. “Pandemic H1N1 influenza infection and vascular thrombosis.” Clin Infect Dis 52 (2011): e14–e17.

Campbell, L.A., Rosenfeld, M.E. “Infection and atherosclerosis development.” Arch Med Res 46 (2015): 339–50.

Engelmann, B., Massberg, S. “Thrombosis as an intravascular effector of innate immunity.” Nat Rev Immunol 13 (2013): 34–45.

Koupenova, M., Mick, E., Mikhalev, E., et al. “Sex differences in platelet toll-like receptors and their association with cardiovascular risk factors.” Arterioscler Thromb Vasc Biol 35 (2015): 1030–7.

Bounameaux, H. “Factor V. Leiden paradox: risk of deep-vein thrombosis but not of pulmonary embolism.” Lancet 356 (2000): 182–3.


GOST Style Citations


1. Wendelboe, A.M., McCumber, M., Hylek, E.M., et al; ISTH Steering Committee for World Thrombosis Day.  “Global public awareness of venous thromboembolism.” J Thromb Haemost 13 (2015): 1365–71.

2. Goldhaber, S.Z. “Venous thromboembolism: epidemiology and magnitude of the problem.” Best Pract Res Clin Haematol 25 (2012): 235–42.

3. ISTH Steering Committee for World Thrombosis Day. “Thrombosis: a majorcontributor to the global disease burden.” J Thromb Haemost 12 (2014): 1580–9.

4. Naess, I.A., Christiansen, S.C., Romundstad, P., et al. “Incidence and mortality of venous thrombosis: a population-based study.” J Thromb Haemost 5 (2007): 692–9.

5. Girolami, A., et al. “Drug-induced thrombophilic or prothrombotic states: an underestimated clinical problem that involves both legal and illegal compounds.” Clinical and Applied Thrombosis/Hemostasis 23.7 (2017): 775–85.

6. Silverstein, M.D., Heit, J.A., Mohr, D.N., et al. “Trends in the incidence of deep vein thrombosis and pulmonary embolism: a 25-year population based study.” Arch Intern Med 158

(1998): 585–93.

7. Kearon, C., Akl, E.A., Comerota, A.J., et al. “Antithrombotic therapy for VTE disease.” Chest 141 (2012): e419S–e494S.

8. Boutitie, F., Pinede, L., Schulman, S., et al. “Influence of preceding length of anticoagulant treatment and initial presentation of venous thromboembolism on risk of recurrence after stopping treatment: analysis of individual participants’ data from seven trials.” BMJ 342 (2011): d3036.

9. Regitz-Zagrosek, V., Kararigas, G. “Mechanistic pathways of sex differences in cardiovascular disease.” Physiological reviews 97.1 (2016): 1–37.

10. Anderson, G.D. “Gender differences in pharmacological response.” International review of neurobiology 83 (2008): 1–10.

11. Андрияшкин, А.В. Российские клинические рекомендации по диагностике, лечению и профилактике венозных тромбоэмболических осложнений (ВТЭО) / А.В. Андрияшкин и др. // Флебология. – 2015. – № 4 (9), Т. 2. – С. 1. Andriyashkin, A.V., et al.

12. Zöller, B., et al. “Family history of venous thromboembolism as a risk factor and genetic research tool.” Thrombosis and haemostasis 114.05 (2015): 890–900.

13. Gerhardt, A., et al. “Hereditary risk factors for thrombophilia and probability of venous thromboembolism during pregnancy and the puerperium.” Blood 128.19 (2016): 2343–9.

14. Suchon, P., et al. “Risk factors for venous thromboembolism in women under combined oral contraceptive.” Thrombosis and haemostasis 115.1 (2016).

15. McDaid, A., Logette, E., Buchillier, V., et al. “Risk prediction of developing venous thrombosis in combined oral contraceptive users.” PLoS ONE 12.7 (2017): e0182041.

16. Preston, A.E., Barr, A. “The plasma concentration of factor VIII in the normal population.” Br J Haematol 10 (1964): 238–45.

17. Moeller, A., et al. “Influence of ABO blood groups on primary hemostasis.” Transfusion 41 (2001): 56–60.

18. O’Donnell, J.S., Lasffan, M.A. “The relationship between ABO histo-blood group, factor VIII and von Willebrand factor.” Transfus Med 11 (2001): 343–51.

19. Gill, J.C., et al. “The effect of ABO blood group on the diagnosis of von Willebrand disease.” Blood 69 (1987): 1691–5.

20. Jenkins, P.V., O’Donnell, J.S. “ABO blood group determines plasma von Willebrand factor levels: a biologic function after all?” Transfusion 46 (2006): 1836–44.

21. Dick, W., et al. “Interrelations of thrombo-embolic diseases and blood group distribution.” Thromb Diath Haemorrh 9 (1963): 472–4.

22. Wu, O., et al. “ABO(H) blood groups and vascular disease: a systematic review and meta-analysis.” J Thromb Haemost 6 (2008): 62–9.

23. Dentali, F., et al. “Non-O blood type is the commonest genetic risk factor for VTE: results from a meta-analysis of the literature.” Semin Thromb Hemost 38

(2012): 535–48.

24. Vasan, S.K., et al. “ABO blood group and risk of thromboembolic and arterial

disease: a study of 1.5 million blood donors.” Circulation (2016): CIRCULATIONAHA-115.

25. Guimaraes, D.A., dos Santos, M.S., Gomes, K.B., et al. “Interaction between Oral Estrogen plus Progestogen Therapy and ABO Blood Groups on Coagulation Activation in Postmenopausal Women.” Menopause  19 (2012): 339–45.  DOI: 10.1097/gme.0b013e31822b721f

26. Gavish, I., Brenner, B. “Air Travel and Risk of Thromboembolism.” Internal and Emergency Medicine 6 (2011): 113–6. DOI: 10.1007/s11739-010-0474-6

27. Cannegieter, S.C., Doggen, C.J.M., van Houwelingen, H.C., Rosendaal, F.R. “Travel-Related Venous Thrombosis: Results from a Large Population-Based Case Control Study (MEGA Study).” PLoS Medicine 3 (2006): e307. DOI: 10.1371/journal.pmed.0030307

28. Martinelli, I., Taioli, E., Battaglioli, T., et al. “Risk of Venous Thromboembolism after Air Travel: Interaction with Thrombophilia and Oral Contraceptives.” Archives of Internal Medicine 163 (2003): 2771–4. DOI: 10.1001/archinte.163.22.2771

29. Svartberg, J., Braekkan, S.K., Laughlin, G.A., Hansen, J.-B. “Endogenous sex hormone levels in men are not associated with risk of venous thromboembolism: the Tromso study.” Eur J Endocrinol 160 (2009): 833–8.

30. Holmegard, H.N., et al. “Endogenous sex hormones and risk of venous thromboembolism in women and men.” Journal of Thrombosis and Haemostasis 12.3 (2014): 297–305.

31. Harrington, L.B., et al. “Cross‐sectional association of endogenous steroid hormone, sex hormone‐binding globulin, and precursor steroid levels with hemostatic factor levels in postmenopausal women.” Journal of Thrombosis and Haemostasis 15.1 (2017): 80–90.

32. Nheu, L., Nazareth, L., Xu, G.Y., et al. “Physiological effects of androgens on human vascular endothelial and smooth muscle cells in culture.” Steroids 76 (2011): 1590–6.

33. Gavin, K.M., Seals, D.R., Silver, A.E., Moreau, K.L. “Vascular endothelial estrogen receptor alpha is modulated by estrogen status and related to endothelial function and endothelial nitric oxide synthase in healthy women.” J Clin Endocrinol Metab 94 (2009): 3513–20.

34. Bahamondes, L., Bahamondes, M.V., Shulman, L.P. “Non-contraceptive benefits of hormonal and intrauterine reversible contraceptive methods.” Human reproduction update 21.5 (2015): 640–51.

35. World Health Organization. Medical Eligibility Criteria for Contraceptive Use, 4th edition. Geneva. WHO (2009). Available from: [http://www.who.int/reproductive_health/publications/mec/family_ planning/9789241563888/en/index.html].

36. Stegemanet, B.H., et al. “Different combined oral contraceptives and the risk of venous thrombosis: systematic review and network meta-analysis.” BMJ (2013).

37. Goodyear-Smith, A., Arroll, B. “Termination of pregnancy following panic-stopping of oral contraceptives.” Contraception 66 (2002): 163–7.

38. Baratloo, A., et al. “The Risk of Venous Thromboembolism with Different Generation of Oral Contraceptives; a Systematic Review and Meta-Analysis.” Emergency 2 (2014).

39. Martínez, F., et al. “Venous and pulmonary thromboembolism and combined hormonal contraceptives. Systematic review and meta-analysis.” Eur J Contracept Reprod Health Care 17.1 (2012): 7–29.

40. Pfeifer, S., et al. “Combined hormonal contraception and the risk of venous thromboembolism: a guideline.” Fertility and sterility 107.1 (2017): 43–51.

41. Bitzer, J., et al. “Statement on combined hormonal contraceptives containing third-or fourth-generation progestogens or cyproterone acetate, and the associated risk of thromboembolism.” J Fam Plann Reprod Health Care 39.3 (2013): 156–9.

42. Reid, R.L., Westhoff, C., Mansour, D., et al. “Oral contraceptives and venous thromboembolism – Consensus opinion from an international workshop held in Berlin, Germany in December 2009.” J Fam Plann Reprod Health Care 36 (2010): 117–22.

43. Jensen, J.T., Trussell, J. “Communicating risk: does scientific debate compromise safety.” Contraception 86 (2012): 327–9.

44. Heinemann, K., Heinemann, L.A. “Comparative risks of venous thromboembolism among users of oral contraceptives containing drospirenone and levonorgestrel.” J Fam Plann Reprod Health Care 37 (2011): 132–5.

45. Dinger, J., Shapiro, S. “Combined oral contraceptives, venous thromboembolism, and the problem of interpreting large but incomplete datasets.” J Fam Plann Reprod Health Care 38 (2012): 2–6.

46. Van Hylckama Vlieg, A., Helmerhorst, F., Rosendaal, F. “The Risk of Deep Venous Thrombosis Associated with Injectable Depot-Medroxyprogesterone Acetate Contraceptives or a Levonorgestrel Intrauterine Device.” Arteriosclerosis Thrombosis and Vascular Biology 30 (2010): 2297–300. DOI: 10.1161/ATVBAHA.110.211482

47. Mantha, S., Karp, R., Raghavan, V., et al. “Assessing the Risk of Venous Thromboembolic Events in Women Taking Progestin-Only Contraception: A Meta-Analysis.” BMJ 345 (2012): e4944. DOI: 10.1136/bmj.e4944

48. Bergendal, A., Odlind, V., Persson, I., Kieler, H. “Limited Knowledge on Progestogen-Only Contraception and Risk of Venous Thromboembolism.” Acta Obstetricia et Gynecologica 88 (2009): 261–6. DOI: 10.1080/00016340902730375

49. Rossouw, J.E., Anderson, G.L., Prentice, R.L., et al; Writing Group for the Women’s Health Initiative Investigators. “Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women’s Health Initiative randomized controlled trial.” JAMA 288.3 (2002): 321–33.

50. Anderson, G.L., Limacher, M., Assaf, A.R., et al; Women’s Health Initiative Steering Committee. “Effects of conjugated equine estrogen in postmenopausal women with hysterectomy: the Women’s Health Initiative randomized controlled trial.” JAMA 291.14 (2004): 1701–12.

51. Vickers, M.R., MacLennan, A.H., Lawton, B., et al; WISDOM group. “Main morbidities recorded in the women’s international study of long duration oestrogen after menopause (WISDOM): a randomised controlled trial of hormone replacement therapy in postmenopausal women.” BMJ 335.7613 (2007): 239.

52. Cushman, M., Kuller, L.H., Prentice, R., et al; Women’s Health Initiative Investigators.

“Estrogen plus progestin and risk of venous thrombosis.” JAMA 292.13 (2004):1573–80.

53. Pérez Gutthann, S., García Rodríguez, L.A., Castellsague, J., Duque Oliart, A. “Hormone replacement therapy and risk of venous thromboembolism: population based case-control study.” BMJ 314.7083 (1997): 796–800.

54. Høibraaten, E., Qvigstad, E., Arnesen, H., et al. “Increased risk of recurrent venous thromboembolism during hormone replacement therapy – results of the randomized, double-blind, placebo-controlled estrogen in venous thromboembolism trial (EVTET).” Thromb Haemost 84.6 (2000): 961–7.

55. Canonico, M., Fournier, A., Carcaillon, L., et al. “Postmenopausal hormone therapy and risk of idiopathic venous thromboembolism: results from the E3N cohort study.” Arterioscler Thromb Vasc Biol 30.2 (2010): 340–5.

56. Eischer, L., Eichinger, S., Kyrle, P.A. “The risk of recurrence in women with venous thromboembolism while using estrogens: a prospective cohort study.” J Thromb Haemost 12.5 (2014): 635–40.

57. Scarabin, P.Y., Oger, E., Plu-Bureau, G.; EStrogen and THromboEmbolism Risk Study Group. “Differential association of oral and transdermal oestrogen-replacement therapy with venous thromboembolism risk.” Lancet 362.9382 (2003): 428–32.

58. Roach, R.E., Lijfering, W.M., Helmerhorst, F.M., et al. “The risk of venous thrombosis in women over 50 years old using oral contraception or postmenopausal hormone therapy.” J Thromb Haemost 11.1 (2013): 124–31.

59. Renoux, C., Dell’Aniello, S., Suissa, S. “Hormone replacement therapy and the risk of venous thromboembolism: a population-based study.” J Thromb Haemost 8.5 (2010): 979–86.

60. Laliberté, F., Dea, K., Duh, M.S., et al. “Does the route of administration for estrogen hormone therapy impact the risk of venous thromboembolism? Estradiol transdermal system versus oral estrogen-only hormone therapy.” Menopause 18.10 (2011): 1052–9.

61. Hemelaar, M., Rosing, J., Kenemans, P., et al. “Less effect of intranasal than oral hormone therapy on factors associated with venous thrombosis risk in healthy postmenopausal women.” Arterioscler Thromb Vasc Biol 26.7 (2006): 1660–6.

62. Baber, R.J., Panay, N., Fenton, A. “2016 IMS Recommendations on women’s midlife health and menopause hormone therapy.” Climacteric 19.2 (2016): 109–50.

63. Patrassi, G.M., Sartori, M.T., Viero, M.L., et al. “The fibrinolytic potential in patients with Cushing’s disease: a clue to their hypercoagulable state.” Blood Coagul Fibrinolysis 3.6 (1992): 789–93.

64. Dal Bo Zanon, R., Fornasiero, L., et al. “Clotting changes in Cushing’s syndrome: elevated factor VIII activity.” Folia Haematol Int Mag Klin Morphol Blutforsch 110.2 (1983): 268–77.

65. Casonato, A., Pontara, E., Boscaro, M., et al. “Abnormalities of von Willebrand factor are also part of the prothrombotic state of Cushing’s syndrome.” Blood Coagul Fibrinolysis 10.3 (1999): 145–51.

66. Boscaro, M., Sonino, N., Scarda, A., et al. “Anticoagulant prophylaxis markedly reduces thromboembolic complications in Cushing’s syndrome.” J Clin Endocrinol Metab 87.8

(2002): 3662–6.

67. Mor, Y.S., Schenker, J.G. “Ovarian hyperstimulation syndrome and thrombotic events.” Am J Reprod Immunol 72.6 (2014): 541–8.

68. Girolami, A., Scandellari, R., Tezza, F., et al. “Arterial thrombosis in young women after ovarian stimulation: case report and review of the literature.” J Thromb Thrombolysis 24.2 (2007): 169–74.

69. Westerlund, E., Henriksson, P., Wallen, H., et al. “Detection of a procoagulable state during controlled ovarian hyperstimulation for in vitro fertilization with global assays of haemostasis.” Thromb Res 130.4 (2012): 649–53.

70. Ramot, Y., Nyska, A., Spectre, G. “Drug-induced thrombosis: an update.” Drug Saf 36.8 (2013): 585–603.

71. Klocking, H.P. “Generation of thrombophilic states by drugs.” Folia Haematol Int Mag Klin Morphol Blutforsch 111.4 (1984): 441–9.

72. Ramot, Y., Nyska, A. “Drug-induced thrombosis – experimental, clinical, and mechanistic considerations.” Toxicol Pathol 35.2 (2007): 208–25.

73. Taparia, M., Cordingley, F.T., Leahy, M.F. “Pulmonary embolism associated with tranexamic acid in severe acquired haemophilia.” Eur J Haematol 68.5 (2002): 307–9.

74. Mihalache, R.M., Ames, P.R. “Deep vein thrombosis, tranexamic acid, and a negative d-Dimer.” Clin Appl Thromb Hemost 18.6 (2012): 666–7.

75. Sundstrom, A., Seaman, H., Kieler, H., Alfredsson, L. “The risk of venous thromboembolism associated with the use of tranexamic acid and other drugs used to treat menorrhagia: a case-control study using the General Practice Research Database.” BJOG 116.1 (2009): 91–7.

76. Woo, K.S., Tse, L.K., Woo, J.L., Vallance-Owen, J. “Massive pulmonary thromboembolism after tranexamic acid antifibrinolytic therapy.” Br J Clin Pract 43.12 (1989): 465–6.

77. Endo, Y., Nishimura, S., Miura, A. “Deep-vein thrombosis induced by tranexamic acid in idiopathic thrombocytopenic purpura.” JAMA 259.24 (1988): 3561–2.

78. Cuzick, J. “Tamoxifen and the factor V Leiden mutation.” J Natl Cancer Inst 102.13 (2010): 918–9.

79. Erman, M., Abali, H., Oran, B., et al. “Tamoxifen-induced tissue factor pathway inhibitor reduction: a clue for an acquired thrombophilic state?” Ann Oncol 15.11 (2004): 1622–6.

80. Hutchison, R.L., Rayan, G.M. “Thrombosis of digital arteries associated with tamoxifen use: case report.” J Reconstr Microsurg 28.2 (2012): 145–8.

81. Shah, V.P., Chegini, H.A., Vishneski, S.R., et al. “Tamoxifen promotes superoxide production in platelets by activation of PI3-kinase and NADPH oxidase pathways.” Thromb Res 129.1 (2012): 36–42.

82. Dicato, M. “Venous thromboembolic events and erythropoies is stimulating agents: an update.” Oncologist 13 Suppl. 3 (2008): 11–5.

83. Karabinos, I.K., Koulouris, S., Kranidis, A., et al. “Spontaneous thrombus formation in a normal left ventricle following administration of large doses of epoetin.” Hellenic J Cardiol 48.1 (2007): 44–6.

84. Lippi, G., Franchini, M., Favaloro, E.J. “Thrombotic complications of erythropoiesis-stimulating agents.” Semin Thromb Hemost 36.5 (2010): 537.

85. Darnige, L., Lillo-Le Louet, A. “Treatments with immunoglobulin and thrombotic adverse events.” Rev Med Interne 35.1 (2014): 39–44. [Article in French]

86. Lorenzana, A., Armin, S., Sharma, A., et al. “Cerebral infarctions after intravenous immunoglobulin therapy for ITP in a child.” Pediatr Neurol 50.2 (2014): 188–91.

87. Amiral, J., Bridey, F., Dreyfus, M., et al. “Platelet factor 4 complexed toheparinisthe target for antibodies generated inheparin-induced thrombocytopenia.” Thromb Haemost 68.1 (1992): 95–6.

88. Warkentin, T.E., Greinacher, A. “Heparin-induced thrombocytopenia: recognition, treatment, and prevention: the Seventh ACCP Conference on Antithrombotic and Thrombolytic Therapy.” Chest 126 Suppl. 3 (2004): 311–37.

89. Girolami, B., Girolami, A. “Heparin-induced thrombocytopenia: a review.” Semin Thromb Hemost 32.8 (2006): 803–9.

90. Warkentin, T.E., Sheppard, J.A., Manheim, J.C. “HIT complicating fondaparinux prophylaxis: fondaparinux-dependent platelet activation as a marker for fondaparinux-induced HIT.” Thromb Haemost 112.6 (2014): 1319–22.

91. Solak, Y., Demircioglu, S., Polat, I., et al. “Heparin-induced thrombocytopenia in a hemodialysis patient treated with fondaparinux: nephrologists between two fires.” Hemodial Int 17.2 (2013): 320–3.

92. Marwali, M.R., Mehta, J.L. “COX-2 inhibitors and cardiovascular risk. Inferences based on biology and clinical studies.” Thromb Haemost 96.4 (2006): 401–6.

93. Nissen, S.E. “Adverse cardiovascular effects of rofecoxib.” N Engl J Med 355.2 (2006): 203–4.

94. Weir, M.R., Sperling, R.S., Reicin, A., Gertz, B.J. “Selective COX-2 inhibition and cardiovascular effects: a review of the rofecoxib development program.” Am Heart J 146.4 (2003): 591–604.

95. Krotz, F., Struthmann, L. “A review on the risk of myocardial infarction associated with the NSAID diclofenac.” Cardiovasc Hematol Disord Drug Targets 10.1 (2010): 53–6.

96. Chen, L.C., Ashcroft, D.M. “Risk of myocardial infarction associated with selective COX-2 inhibitors: meta-analysis of randomised controlled trials.” Pharmacoepidemiol Drug Saf 16.7 (2007): 762–72.

97. Bergendal, A., et al. “Non‐steroidal anti‐inflammatory drugs and venous thromboembolism in women.” Pharmacoepidemiology and drug safety 22.6 (2013): 658–66.

98. Parkin, L., et al. “Antidepressants, depression, and venous thromboembolism risk: large prospective study of UK women.” Journal of the American Heart Association 6.5 (2017): e005316.

99. Pomp, E., Lenselink, A., Rosendaal, F., Doggen, C. “Pregnancy, the Postpartum Period and Prothrombotic Defects: Risk of Venous Thrombosis in the MEGA Study.” Journal of Thrombosis and Haemostasis 6 (2008): 632–7.

100.  Reid, R.L., Westhoff, C., Mansour, D., et al. “Oral Contraceptives and Venous Thromboembolism Consensus Opinion from an International Workshop held in Berlin, Germany in December 2009.” Journal of Family Planning and Reproductive Health Care 36 (2010): 117–22.

101.  Royal College of Obstetricians and Gynaecologists. Green-top Guideline No. 37b (2015). Thromboembolic disease in pregnancy and the puerperium: acute management. Available from: [https://www.rcog.org.uk/en/guidelines-research-services/guidelines/gtg37b/].

102.  Bates, S.M., et al. “Guidance for the treatment and prevention of obstetric-associated venous thromboembolism.” Journal of thrombosis and thrombolysis 41.1 (2016): 92–128.

103.  Tsai, A., Cushman, M., Rosamond, W., et al. “Cardiovascular Risk Factors and Venous Thromboembolism Incidence: The Longitudinal Investigation of Thromboembolism Etiology.” Archives of Internal Medicine 162 (2002): 1182–9.  DOI: 10.1001/archinte.162.10.1182

104.  Hoist, A., Jensen, G., Prescott, E. “Risk Factors for Venous Thromboemobolism: A. Waddington et al. Results from the Copenhagen City Heart Study.” Circulation 121 (2010): 1896–1903. DOI: 10.1161/CIRCULATIONAHA.109.921460

105.  Hart, R., Doherty, D.A. “The potential implications of a PCOS diagnosis on a woman’s long-term health using data linkage.” The Journal of Clinical Endocrinology & Metabolism 100.3 (2015): 911–19.

106.  Boumosleh, J.M., et al. “Metabolic Concomitants of Obese and Nonobese Women With Features of Polycystic Ovarian Syndrome.” Journal of the Endocrine Society 1.12 (2017): 1417–27.

107.  Okoroh, E., Hooper, W., Atrash, H., et al. “Is Polycystic Ovary Syndrome another Risk Factor for Venous Thromboembolism? United States, 2003-2008.” American Journal of Obstetrics and Gynecology 207 (2012): 377.e1-377.e8.  DOI: 10.1016/j. ajog.2012.08.007

108.  Bird, S.T., Hartzema, A.G., Brophy, J.M., et al. “Risk of Venous Thromboembolism in Women with Polycystic Ovarian Syndrome: A Population-Based Matched Cohort Analysis.” CMAJ 185 (2013): E115–E120. DOI: 10.1503/cmaj.120677

109.  Seaman, H.E., de Vries, C.S., Farmer, R.D.T. “The Risk of Venous Thromboembolism in Women Prescribed Cyproterone Acetate in Combination with Ethinyl Estradiol: A Nested Cohort Analysis and Case Control Study.” Human Reproduction 18 (2003): 522–6. DOI: 10.1093/humrep/deg120

110.  Okoroh, E.M., et al. “Assessing the intersection of cardiovascular disease, venous thromboembolism, and polycystic ovary syndrome.” Thrombosis research 136.6 (2015): 1165–8.

111.  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).” JAMA 285 (2001): 2486–96.

112.  Gami, A.S., Witt, B.J., Howard, D.E., et al. “Metabolic syndrome and risk of incident cardiovascular events and death: a systematic review and meta-analysis of longitudinal studies.” J Am Coll Cardiol 49 (2007): 403–14.

113.  Ageno, W., Prandoni, P., Romualdi, E., et al. “The metabolic syndrome and the risk of venous thrombosis: a case-control study.” J Thromb Haemost 4 (2006): 1914–18.

114.  Ambrosetti, M., Ageno, W., Salerno, M., et al. “Metabolic syndrome as a risk factor for deep vein thrombosis after acute cardiac conditions.” Thromb Res 120 (2007): 815–18.

115.  Ay, C., Tengler, T., Vormittag, R., et al. “Venous thromboembolism – a manifestation of the metabolic syndrome.” Haematologica 92 (2007): 374–80.

116.  Jang, M.J., Choi, W.I., Bang, S.M., et al. “Metabolic syndrome is associated with venous thromboembolism in the Korean population.” Arterioscler Thromb Vasc Biol 29 (2009): 311–5.

117.  Borch, K.H., Braekkan, S.K., Mathiesen, E.B., et al. “Abdominal obesity is essential for the risk of venous thromboembolism in the metabolic syndrome: the Tromsø study.” J Thromb Haemost 7 (2009): 739–45.

118.  Steffen, L.M., Cushman, M., Peacock, J.M., et al. “Metabolic syndrome and risk of venous thromboembolism: Longitudinal Investigation of Thromboembolism Etiology.” J Thromb Haemost 7 (2009): 746–51.

119.  Vayá, A., Martínez-Triguero, M.L., España, F., et al. “The metabolic syndrome and its individual components: its association with venous thromboembolism in a Mediterranean population.” Metab Syndr Relat Disord 9 (2011): 197–201.

120.  Ageno, W., et al. “Association between the metabolic syndrome, its individual components, and unprovoked venous thromboembolism: results of a patient-level meta-analysis.” Arteriosclerosis, thrombosis, and vascular biology (2014): ATVBAHA-114.

121.  Walker, A.J., et al. “Incidence of venous thromboembolism in patients with cancer – a cohort study using linked United Kingdom databases.” Eur J Cancer 49 (2013): 1404–13.

122.  Heit, J.A., et al. “Risk factors for deep vein thrombosis and pulmonary embolism: a population-based case-control study.” Arch Intern Med 160 (2000): 809–15.

123.  Khorana, A.A., et al. “Thromboembolism is a leading cause of death in cancer patients receiving outpatient chemotherapy.” J Thromb Haemost 5 (2007): 632–4.

124.  Heit, J.A., et al. “Relative impact of risk factors for deep vein thrombosis and pulmonary embolism: a population-based study.” Arch Intern Med 162 (2002): 1245–8.

125.  Cronin-Fenton, D.P., et al. “Hospitalisation for venous thromboembolism in cancer patients and the general population: a population-based cohort study in Denmark, 1997–2006.” Br J Cancer 103 (2010): 947–53.

126.  Riedl, J., et al. “Association of mean platelet volume with risk of venous thromboembolism and mortality in patients with cancer. Results from the Vienna Cancer and Thrombosis Study (CATS).” Thromb Haemost 111 (2014): 670–8.

127.  Ay, C., Pabinger, I., Cohen, A.T. “Cancer-associated venous thromboembolism: burden, mechanisms, and management.” Thrombosis and haemostasis 117.02 (2017): 219–30.

128.  Kearon, C., et al. “Antithrombotic Therapy for VTE Disease: CHEST Guideline and Expert Panel Report.” Chest 149 (2016): 315–52.

129.  Mandala, M., et al. “Venous thromboembolism (VTE) in cancer patients. ESMO clinical recommendations for prevention and management.” Thromb Res 125 Suppl. 2 (2010): S117–119.

130.  NCCN Clinical Practical Guidelines in Oncology. Cancer-associated venous thromboembolic disease version 1.2014. Available from: [http://www.nccn.org/ professionals/physician_gls/f_ guidelines.asp].

131.  Farge, D., et al. “International clinical practice guidelines for the treatment and prophylaxis of venous thromboembolism in patients with cancer.” J Thromb Haemost 11 (2013): 56–70.

132.  Lyman, G.H., et al. “Venous thromboembolism prophylaxis and treatment in patients with cancer: American Society of Clinical Oncology clinical practice guideline update.” J Clin Oncol 31 (2013): 2189–204.

133.  Watson, H.G., et al. “Guideline on aspects of cancer-related venous thrombosis.” Br J Haematol 170 (2015): 640–8.

134.  Stevens, S.M., et al. “Guidance for the evaluation and treatment of hereditary and acquired thrombophilia.” Journal of thrombosis and thrombolysis 41.1 (2016): 154–64.

135.  Christiansen, S.C., Cannegieter, S.C., Koster, T., et al.

“Thrombophilia, clinical factors, and recurrent venous thrombotic events.” JAMA 293 (2005): 2352–61.

136.  Simone, B., De Stefano, V., Leoncini, E., et al. “Risk of venous thromboembolism associated with single and combined effects of factor V Leiden, prothrombin 20210A and methylenetethraydrofolate reductase C677T: a meta-analysis involving over 11,000 cases and 21,000 controls.” Eur J Epidemiol 28 (2013): 621–47.

137.  Mahmoodi, B.K., Brouwer, J.L., Ten Kate, M.K., et al. “A prospective cohort study on the absolute risks of venous thromboembolism and predictive value of screening asymptomatic relatives of patients with hereditary deficiencies of protein S, protein C or antithrombin.” J Thromb Haemost 8 (2010): 1193–200.

138.  Pernod, G., Biron-Andreani, C., Morange, P.E., et al. “Recommendations on testing for thrombophilia in venous thromboembolic disease: a French consensus guideline.” J Mal Vasc 34 (2009): 156–203.

139.  Merriman, L., Greaves, M. “Testing for thrombophilia: an evidence-based approach.” Postgrad Med J 82 (2006): 699–704.

140.  Wu, O., Robertson, L., Twaddle, S., et al. “Screening for thrombophilia in high-risk situations: a meta-analysis and costeffectiveness analysis.” Br J Haematol 131 (2005): 80–90.

141.  Bates, S.M., Greer, I.A., Middeldorp, S., et al. “VTE, thrombophilia, antithrombotic therapy, and pregnancy.” Chest 141 (2012): e691S–e736S.

142.  Cohen, W., Castelli, C., Suchon, P., et al. “Risk assessment of venous thrombosis in families with known hereditary thrombophilia: the MARseilles-NImes prediction model.” J Thromb Haemost 12 (2014): 138–46.

143.  Davis, S.M., Branch, D.W. “Thromboprophylaxis in pregnancy: who and how?” Obstet Gynecol Clin North Am 37 (2010): 333–43.

144.  Wu, O., Robertson, L., Langhorne, P., et al. “Oral contraceptives, hormone replacement therapy, thrombophilias and risk of venous thromboembolism: a systematic review. The thrombosis: risk and Economic Assessment of Thrombophilia Screening (TREATS) Study.” Thromb Haemost 94 (2005): 17–25.

145.  Suchon, P., et al. “Genetic risk factors for venous thrombosis in women using combined oral contraceptives: update of the PILGRIM study.” Clinical genetics 91.1 (2017): 131–6.

146.  Higgins, J.P., Thompson, S.G., Deeks, J.J., Altman, D.G. “Measuring inconsistency in meta analyses.” BMJ 327 (2003): 557–60.

147.  Rinde, L.B., Lind, C., Smabrekke, B., et al. “Impact of incident myocardial infarction on risk of venous thromboembolism: the Tromsö study.” J Thromb Haemost 14 (2016): 1183–91.

148.  Hosseini, S., Kalantar, E., Hosseini, M.S., et al. “Genetic risk factors in patients with deep venous thrombosis, a retrospective case control study on Iranian population.” Thromb J 13 (2015): 35.

149.  Margaglione, M., Cappucci, G., Colaizzo, D., et al. “The PAI-1 gene locus 4G/5G polymorphism is associated with a family history of coronary artery disease.” Arterioscler Thromb Vasc Biol 18 (1998): 152–6.

150.  Sumner, J.A., Kubzansky, L.D., Elkind, M.S., et al. “Trauma exposure and posttraumatic stress disorder symptoms predict onset of cardiovascular events in women.” Circulation 132 (2015): 251–9.

151.  Koupenova, M., et al. “Thrombosis and platelets: an update.” European heart journal 38.11 (2016): 785–91.

152.  Chu, S.G., Becker, R.C., Berger, P.B., et al. “Mean platelet volume as a predictor of cardiovascular risk: a systematic review and meta-analysis.” J Thromb Haemost 8 (2010): 148–56.

153.  Braekkan, S.K., Mathiesen, E.B., Njolstad, I., et al. “Mean platelet volume is a risk factor for venous thromboembolism: the Tromsö Study, Tromsö, Norway.” J Thromb Haemost 8 (2010): 157–62.

154.  Tichelaar, Y.I., Kluin-Nelemans, H.J., Meijer, K. “Infections and inflammatory diseases as risk factors for venous thrombosis. A systematic review.” Thromb Haemost 107 (2012): 827–37.

155.  Bunce, P.E., High, S.M., Nadjafi, M., et al. “Pandemic H1N1 influenza infection and vascular thrombosis.” Clin Infect Dis 52 (2011): e14–e17.

156.  Campbell, L.A., Rosenfeld, M.E. “Infection and atherosclerosis development.” Arch Med Res 46 (2015): 339–50.

157.  Engelmann, B., Massberg, S. “Thrombosis as an intravascular effector of innate immunity.” Nat Rev Immunol 13 (2013): 34–45.

158.  Koupenova, M., Mick, E., Mikhalev, E., et al. “Sex differences in platelet toll-like receptors and their association with cardiovascular risk factors.” Arterioscler Thromb Vasc Biol 35 (2015): 1030–7.

159.  Bounameaux, H. “Factor V. Leiden paradox: risk of deep-vein thrombosis but not of pulmonary embolism.” Lancet 356 (2000): 182–3.





DOI: https://doi.org/10.18370/2309-4117.2018.41.12-24

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