Progestogens and venous thromboembolism in menopausal women: an updated oral versus transdermal estrogen meta-analysis

References

• Stanczyk FZ, Hapgood JP, Winer S, Mishell DR. Jr., Progestogens used in postmenopausal hormone therapy: differences in their pharmacological properties, intracellular actions, and clinical effects. Endocr Rev 2013;34:171–208
   PubMed Web of Science ®Google Scholar
• Rossouw JE, Anderson GL, Prentice RL, et al. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women's Health Initiative randomized controlled trial. JAMA 2002;288:321–33
   PubMed Web of Science ®Google Scholar
• Cushman M, Kuller LH, Prentice R, et al. Estrogen plus progestin and risk of venous thrombosis. JAMA 2004;292:1573–80
   PubMed Web of Science ®Google Scholar
• Manson JE, Chlebowski RT, Stefanick ML, et al. Menopausal hormone therapy and health outcomes during the intervention and extended poststopping phases of the Women's Health Initiative randomized trials. JAMA 2013;310:1353–68
   PubMed Web of Science ®Google Scholar
• Scarabin PY. Hormone therapy and venous thromboembolism among postmenopausal women. Front Horm Res 2014;43:21–32
   PubMed Web of Science ®Google Scholar
• Olie V, Canonico M, Scarabin PY. Risk of venous thrombosis with oral versus transdermal estrogen therapy among postmenopausal women. Curr Opin Hematol 2010;17:457–63
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Scarabin PY, Oger E, Plu-Bureau G. Differential association of oral and transdermal oestrogen-replacement therapy with venous thromboembolism risk. Lancet 2003;362:428–32
   PubMed Web of Science ®Google Scholar
• Canonico M, Oger E, Plu-Bureau G, et al. Hormone therapy and venous thromboembolism among postmenopausal women: Impact of the route of estrogen administration and progestogens: the esther study. Circulation 2007;115:840–5
   PubMed Web of Science ®Google Scholar
• Canonico M, Fournier A, Carcaillon L, et al. Postmenopausal hormone therapy and risk of idiopathic venous thromboembolism: results from the E3N cohort study. Arterioscl Thromb Vasc Biol 2010;30:340–5
   PubMed Web of Science ®Google Scholar
• Renoux C, Dell'Aniello S, Suissa S. Hormone replacement therapy and the risk of venous thromboembolism: a population-based study. J Thromb Haemost 2010;8:979–86
   PubMed Web of Science ®Google Scholar
• Sweetland S, Beral V, Balkwill A, et al. Venous thromboembolism risk in relation to use of different types of postmenopausal hormone therapy in a large prospective study. J Thromb Haemost 2012;10:2277–86
   PubMed Web of Science ®Google Scholar
• Roach RE, Lijfering WM, Helmerhorst FM, Cannegieter SC, Rosendaal FR, van Hylckama Vlieg A. The risk of venous thrombosis in women over 50 years old using oral contraception or postmenopausal hormone therapy. J Thromb Haemost 2013;11:124–31
   PubMed Web of Science ®Google Scholar
• Bergendal A, Kieler H, Sundström A, Hirschberg AL, Kocoska-Maras L. Risk of venous thromboembolism associated with local and systemic use of hormone therapy in peri- and postmenopausal women and in relation to type and route of administration. Menopause 2016;23:593–9
   PubMed Web of Science ®Google Scholar
• DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials 1986;7:177–88
   PubMed Web of Science ®Google Scholar
• Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ 2003;327:557–60
   PubMed Web of Science ®Google Scholar
• Olié V, Plu-Bureau G, Conard J, Horellou MH, Canonico M, Scarabin PY. Hormone therapy and recurrence of venous thromboembolism among postmenopausal women. Menopause 2011;18:488–93
   PubMed Web of Science ®Google Scholar
• Simon JA, Laliberté F, Duh MS, et al. Venous thromboembolism and cardiovascular disease complications in menopausal women using transdermal versus oral estrogen therapy. Menopause 2016;23:600–10
   PubMed Web of Science ®Google Scholar
• Laliberté F, Dea K, Duh MS, Kahler KH, Rolli M, Lefebvre P. 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 2011;18:1052–9
   PubMed Web of Science ®Google Scholar
• Vickers MR, MacLennan AH, Lawton B, et al. 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 2007;335:239
   PubMed Web of Science ®Google Scholar
• Olie V, Canonico M, Scarabin PY. Postmenopausal hormone therapy and venous thromboembolism. Thromb Res 2011;127(Suppl 3):S26–29
   PubMed Web of Science ®Google Scholar
• Smith NL, Heckbert SR, Lemaitre RN, et al. Esterified estrogens and conjugated equine estrogens and the risk of venous thrombosis. JAMA 2004;292:1581–7
   PubMed Web of Science ®Google Scholar
• Smith NL, Blondon M, Wiggins KL, et al. Lower risk of cardiovascular events in postmenopausal women taking oral estradiol compared with oral conjugated equine estrogens. JAMA Intern Med 2014;174:25–31
   PubMed Web of Science ®Google Scholar
• Mohammed K, Abu Dabrh AM, Benkhadra K, et al. Oral vs transdermal estrogen therapy and vascular events: a systematic review and meta-analysis. J Clin Endocrinol Metab 2015;100:4012–20
   PubMed Web of Science ®Google Scholar
• Scarabin PY, Canonico M, Scarabin-Carre V, Oger E. Transdermal vs oral estrogen therapy and venous thromboembolism: upgrade the level of evidence. J Clin Endocrinol Metab 2016;101:L30–1
   PubMedGoogle Scholar
• Balshem H, Helfand M, Schunemann HJ, et al. GRADE guidelines: 3. rating the quality of evidence. J Clin Epidemiol 2011;64:401–6
   PubMed Web of Science ®Google Scholar
• Scarabin PY, Alhenc-Gelas M, Plu-Bureau G, Taisne P, Agher R, Aiach M. Effects of oral and transdermal estrogen/progesterone regimens on blood coagulation and fibrinolysis in postmenopausal women. A randomized controlled trial. Arterioscler Thromb Vasc Biol 1997;17:3071–8
   PubMed Web of Science ®Google Scholar
• Oger E, Alhenc-Gelas M, Lacut K, et al. Differential effects of oral and transdermal estrogen/progesterone regimens on sensitivity to activated protein C among postmenopausal women: a randomized trial. Arterioscler Thromb Vasc Biol 2003;23:1671–6
   PubMed Web of Science ®Google Scholar
• Scarabin PY, Hemker HC, Clément C, Soisson V, Alhenc-Gelas M. Increased thrombin generation among postmenopausal women using hormone therapy: importance of the route of estrogen administration and progestogens. Menopause 2011;18:873–9
   PubMed Web of Science ®Google Scholar
• Canonico M, Alhenc-Gelas M, Plu-Bureau G, Olie V, Scarabin PY. Activated protein C resistance among postmenopausal women using transdermal estrogens: importance of progestogen. Menopause 2010;17:1122–7
   PubMed Web of Science ®Google Scholar
• Vlieg AVH, Helmerhorst FM, Rosendaal FR. The risk of deep venous thrombosis associated with injectable depot-medroxyprogesterone acetate contraceptives or a levonorgestrel intrauterine device. Arterioscler Thromb Vasc Biol 2010;30:2297–300
   PubMed Web of Science ®Google Scholar
• Cohen AT, Agnelli G, Anderson FA, et al. Venous thromboembolism (VTE) in Europe. The number of VTE events and associated morbidity and mortality. Thromb Haemost 2007;98:756–64
   PubMed Web of Science ®Google Scholar
• Canonico M, Oger E, Conard J, et al. Obesity and risk of venous thromboembolism among postmenopausal women: differential impact of hormone therapy by route of estrogen administration. The ESTHER Study. J Thromb Haemost 2006;4:1259–65
   PubMed Web of Science ®Google Scholar
• Straczek C, Oger E, Yon de Jonage-Canonico MB, et al. Prothrombotic mutations, hormone therapy, and venous thromboembolism among postmenopausal women: impact of the route of estrogen administration. Circulation 2005;112:3495–500
   PubMed Web of Science ®Google Scholar
• Scarabin PY. Hormones and venous thromboembolism among postmenopausal women. Climacteric 2014;17(Suppl 2):34–7
   PubMed Web of Science ®Google Scholar
• Tremollieres F, Brincat M, Erel CT, et al. EMAS position statement: managing menopausal women with a personal or family history of VTE. Maturitas 2011;69:195–8
   PubMed Web of Science ®Google Scholar
• Stuenkel CA, Davis SR, Gompel A, et al. Treatment of symptoms of the menopause: an endocrine society clinical practice guideline. J Clin Endocrinol Metab 2015;100:3975–4011
   PubMed Web of Science ®Google Scholar
• Baber RJ, Panay N, Fenton A. the IMS Writing Group. 2016 IMS Recommendations on women’s midlife health and menopause hormone therapy. Climacteric 2016;19:109–50
   PubMed Web of Science ®Google Scholar
• The NAMS 2017 Hormone Therapy Position Statement Advisory Panel. The 2017 hormone therapy position statement of the North American menopause society. Menopause 2017;24:728–53
   PubMed Web of Science ®Google Scholar
• Archer DF, Oger E. Estrogen and progestogen effect on venous thromboembolism in menopausal women. Climacteric 2012;15:235–40
   PubMed Web of Science ®Google Scholar
• Fournier A, Kernaleguen C, Panjo H, Clavel-Chapelon F, Ringa V. Postmenopausal hormone therapy initiation before and after the women’s health initiative in two French cohorts. Menopause 2011;18:219–23
   PubMed Web of Science ®Google Scholar