Advertisement

Women, thrombosis, and cancer

  • Dominique Farge
    Correspondence
    Corresponding author at: Assistance Publique-Hôpitaux de Paris, Hôpital Saint-Louis, Unité de Médecine Interne, Paris, France.
    Affiliations
    Assistance Publique-Hôpitaux de Paris, Hôpital Saint-Louis, Unité de Médecine Interne: Maladies Auto-immunes et Pathologie Vasculaire (UF 04) Centre de Référence des Maladies auto-immunes systémiques Rares d'ile-de-France, Filière FAI2R, F-75010 Paris, France; Département de Médecine, Université McGill, Montreal, Québec, Canada
    Search for articles by this author
  • Christine Le Maignan
    Affiliations
    Assistance Publique-Hôpitaux de Paris, Hôpital Saint-Louis, Service d'Oncologie Médicale, F-75010, Paris, France
    Search for articles by this author
  • Ludovic Doucet
    Affiliations
    Assistance Publique-Hôpitaux de Paris, Hôpital Saint-Louis, Service d'Oncologie Médicale, F-75010, Paris, France
    Search for articles by this author
  • Corinne Frere
    Affiliations
    Assistance Publique Hôpitaux de Paris, Hôpital Pitié-Salpêtrière, Service d'Hématologie Biologique; Sorbonne Université, INSERM UMRS_1166, Institute of Cardiometabolism And Nutrition, F-75013 Paris, France
    Search for articles by this author
  • pour le Groupe Francophone Thrombose et Cancer

      ABSTRACT

      Venous thromboembolism (VTE) is a major common complication in cancer patients. Risk-adapted thromboprophylaxis and antithrombotic therapy for patients diagnosed with VTE can reduce the recurrence of VTE events. Thrombotic risk varies according to cancer type, stage, and comorbidities. The current review analyzes most recent data and provides clinical guidance for the management of women with cancer-associated thrombosis.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Thrombosis Research
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Farge D.
        • Bounameaux H.
        • Brenner B.
        • et al.
        International clinical practice guidelines including guidance for direct oral anticoagulants in the treatment and prophylaxis of venous thromboembolism in patients with cancer.
        Lancet Oncol. 2016; 17: e452-e466
        • Easaw J.C.
        • Shea-Budgell M.A.
        • Wu C.M.J.
        • et al.
        Canadian consensus recommendations on the management of venous thromboembolism in patients with cancer. Part 1: prophylaxis.
        Curr. Oncol. 2015; 22: 133-143
        • Easaw J.C.
        • Shea-Budgell M.A.
        • Wu C.M.J.
        • et al.
        Canadian consensus recommendations on the management of venous thromboembolism in patients with cancer. Part 2: treatment.
        Curr. Oncol. 2015; 22: 144-155
        • Lyman G.H.
        • Bohlke K.
        • Khorana A.A.
        • et al.
        American Society of Clinical Oncology, Venous thromboembolism prophylaxis and treatment in patients with cancer: american society of clinical oncology clinical practice guideline update 2014.
        J. Clin. Oncol. 2015; 33: 654-656
        • Kearon C.
        • Akl E.A.
        • Ornelas J.
        • et al.
        Antithrombotic therapy for VTE disease: CHEST guideline and Expert Panel Report.
        Chest. 2016; 149: 315-352
      1. NCCN Clinical Practice Guidelines in Oncology (NCCN Guidelines®). Venous thromboembolic disease - vte.pdf. http://www.nccn.org/professionals/physicia_gls/pdf/vte.pdf.

        • Bray F.
        • Ferlay J.
        • Soerjomataram I.
        • et al.
        Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries.
        CA. Cancer J. Clin. 2018; 68: 394-424
        • Roach R.E.J.
        • Lijfering W.M.
        • Rosendaal F.R.
        • et al.
        Sex difference in risk of second but not of first venous thrombosis: paradox explained.
        Circulation. 2014; 129: 51-56
        • Yasui M.
        • Ikeda M.
        • Miyake M.
        • et al.
        Clinical Study Group of Osaka University (CSGO), Colorectal Group, Comparison of bleeding risks related to venous thromboembolism prophylaxis in laparoscopic vs open colorectal cancer surgery: a multicenter study in Japanese patients.
        Am. J. Surg. 2017; 213: 43-49
        • Trujillo-Santos J.
        • Monreal M.
        Thirty-day mortality rate in women with cancer and venous thromboembolism. Findings from the Registro Informatizado de la Enfermedad Trombo Embolica Registry.
        Curr. Opin. Pulm. Med. 2012; 18: 393-398
        • Scheres L.J.J.
        • Brekelmans M.P.A.
        • Beenen L.F.M.
        • et al.
        Sex-specific differences in the presenting location of a first venous thromboembolism.
        J. Thromb. Haemost. 2017; 15: 1344-1350
        • Naess I.A.
        • Christiansen S.C.
        • Romundstad P.
        • et al.
        Incidence and mortality of venous thrombosis: a population-based study.
        J. Thromb. Haemost. 2007; 5: 692-699
        • Canonico M.
        • Plu-Bureau G.
        • Lowe G.D.O.
        • Scarabin P.-Y.
        Hormone replacement therapy and risk of venous thromboembolism in postmenopausal women: systematic review and meta-analysis.
        BMJ. 2008; 336: 1227-1231
        • van Hylckama Vlieg A.
        • Helmerhorst F.M.
        • Vandenbroucke J.P.
        • et al.
        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
        • Pomp E.R.
        • Lenselink A.M.
        • Rosendaal F.R.
        • Doggen C.J.M.
        Pregnancy, the postpartum period and prothrombotic defects: risk of venous thrombosis in the MEGA study.
        J. Thromb. Haemost. 2008; 6: 632-637
        • Bleau N.
        • Patenaude V.
        • Abenhaim H.A.
        Risk of venous thrombo-embolic events in pregnant patients with cancer.
        J. Matern. Fetal Neonatal Med. 2016; 29: 380-384
        • Martin-Martos F.
        • Trujillo-Santos J.
        • Barron M.
        • et al.
        RIETE Investigators, Gender differences in cancer patients with acute venous thromboembolism.
        Thromb. Res. 2015; 135: S12-S15
        • Trujillo-Santos J.
        • Ruiz-Gamietea A.
        • Luque J.M.
        • et al.
        RIETE Investigators, Predicting recurrences or major bleeding in women with cancer and venous thromboembolism. Findings from the RIETE Registry.
        Thromb. Res. 2009; 123: S10-S15
        • Trujillo-Santos J.
        • Martos F.M.
        • Font C.
        • et al.
        Analysis of clinical factors affecting the rates of fatal pulmonary embolism and bleeding in cancer patients with venous thromboembolism.
        Heliyon. 2017; 3: e00229
        • Kahale L.A.
        • Hakoum M.B.
        • Tsolakian I.G.
        • et al.
        Anticoagulation for the long-term treatment of venous thromboembolism in people with cancer.
        Cochrane Database Syst. Rev. 2018; 6: CD006650
        • Schulman S.
        • Kearon C.
        • Kakkar A.K.
        • et al.
        RE-COVER Study Group, Dabigatran versus warfarin in the treatment of acute venous thromboembolism.
        N. Engl. J. Med. 2009; 361: 2342-2352
        • Schulman S.
        • Kakkar A.K.
        • Goldhaber S.Z.
        • et al.
        RE-COVER II Trial Investigators, Treatment of acute venous thromboembolism with dabigatran or warfarin and pooled analysis.
        Circulation. 2014; 129: 764-772
        • Investigators E.I.N.S.T.E.I.N.
        • Bauersachs R.
        • Berkowitz S.D.
        • Brenner B.
        • et al.
        Oral rivaroxaban for symptomatic venous thromboembolism.
        N. Engl. J. Med. 2010; 363: 2499-2510
        • Investigators E.I.N.S.T.E.I.N.-P.E.
        • Büller H.R.
        • Prins M.H.
        • Lensin A.W.A.
        • et al.
        Oral rivaroxaban for the treatment of symptomatic pulmonary embolism.
        N. Engl. J. Med. 2012; 366: 1287-1297
        • Agnelli G.
        • Buller H.R.
        • Cohen A.
        • et al.
        AMPLIFY Investigators, Oral apixaban for the treatment of acute venous thromboembolism.
        N. Engl. J. Med. 2013; 369: 799-808
        • Investigators Hokusai-VTE
        • Büller H.R.
        • Décousus H.
        • Grosso M.A.
        • et al.
        Edoxaban versus warfarin for the treatment of symptomatic venous thromboembolism.
        N. Engl. J. Med. 2013; 369: 1406-1415
        • Raskob G.E.
        • van Es N.
        • Verhamme P.
        • et al.
        Hokusai VTE Cancer Investigators, Edoxaban for the treatment of cancer-associated venous thromboembolism.
        N. Engl. J. Med. 2018; 378: 615-624
        • Young A.M.
        • Marshall A.
        • Thirlwall J.
        • et al.
        Comparison of an oral factor Xa inhibitor with low molecular weight heparin in patients with cancer with venous thromboembolism: results of a randomized trial (SELECT-D).
        J. Clin. Oncol. 2018; 36: 2017-2023
      2. R. McBane, Apixaban, Dalteparin, in Active Cancer Associated Venous Thromboembolism, the ADAM VTE trial, in: ASH, 2018. https://ash.confex.com/ash/2018/webprogram/Paper118808.html.

        • Kraaijpoel N.
        • Di Nisio M.
        • Mulder F.I.
        • et al.
        Clinical impact of bleeding in cancer- associated venous thromboembolism: results from the Hokusai VTE Cancer Study.
        Thromb. Haemost. 2018; 118: 1439-1449
        • Frere C.
        • Benzidia I.
        • Marjanovic Z.
        • Farge D.
        Recent advances in the management of cancer-associated thrombosis: new hopes but new challenges.
        Cancers (Basel). 2019; 11: E71
        • Frere C.
        • Farge D.
        The best direct-acting oral anticoagulant for treatment of venous thromboembolism?.
        Lancet Haematol. 2019; 6: e4-e5
        • Khorana A.A.
        • Noble S.
        • Lee A.Y.Y.
        • et al.
        Role of direct oral anticoagulants in the treatment of cancer-associated venous thromboembolism: guidance from the SSC of the ISTH.
        J. Thromb. Haemost. 2018; 16: 1891-1894
        • Khorana A.A.
        • Kuderer N.M.
        • Culakova E.
        • et al.
        Development and validation of a predictive model for chemotherapy-associated thrombosis.
        Blood. 2008; 111: 4902-4907
        • Khorana A.
        Rivaroxaban thromboprophylaxis in high-risk ambulatory cancer patients receiving systemic therapy: results of a randomized clinical trial (CASSINI).
        in: ASH. 2018
        • Carrier M.
        • Abou-Nassar K.
        • Mallick R.
        • et al.
        Apixaban to prevent venous thromboembolism in patients with cancer.
        N. Engl. J. Med. 2019; 380: 711-719
        • Walker A.J.
        • Card T.R.
        • West J.
        • et al.
        Incidence of venous thromboembolism in patients with cancer - a cohort study using linked United Kingdom databases.
        Eur. J. Cancer. 2013; 49: 1404-1413
        • Jones A.
        • Stockton D.L.
        • Simpson A.J.
        • Murchison J.T.
        Idiopathic venous thromboembolic disease is associated with a poorer prognosis from subsequent malignancy.
        Br. J. Cancer. 2009; 101: 840-842
        • Paneesha S.
        • McManus A.
        • Arya R.
        • et al.
        VERITY Investigators, Frequency, demographics and risk (according to tumour type or site) of cancer-associated thrombosis among patients seen at outpatient DVT clinics.
        Thromb. Haemost. 2010; 103: 338-343
        • Du X.L.
        • Zhang Y.
        • Hardy D.
        Associations between hematopoietic growth factors and risks of venous thromboembolism, stroke, ischemic heart disease and myelodysplastic syndrome: findings from a large population-based cohort of women with breast cancer.
        Cancer Causes Control. 2016; 27: 695-707
        • Haas S.K.
        • Freund M.
        • Heigener D.
        • et al.
        TOPIC Investigators, Low-molecular- weight heparin versus placebo for the prevention of venous thromboembolism in metastatic breast cancer or stage III/IV lung cancer.
        Clin. Appl. Thromb. Hemost. 2012; 18: 159-165
        • Levine M.
        • Hirsh J.
        • Gent M.
        • et al.
        Double-blind randomised trial of a very-low- dose warfarin for prevention of thromboembolism in stage IV breast cancer.
        Lancet. 1994; 343: 886-889
      3. Lancet. 2005; 365: 1687-1717
        • Cuzick J.
        • Forbes J.F.
        • Sestak I.
        • et al.
        International Breast Cancer Intervention Study I Investigators, Long-term results of tamoxifen prophylaxis for breast cancer - 96-month follow-up of the randomized IBIS-I trial.
        J. Natl. Cancer Inst. 2007; 99: 272-282
        • Meier C.R.
        • Jick H.
        Tamoxifen and risk of idiopathic venous thromboembolism.
        Br. J. Clin. Pharmacol. 1998; 45: 608-612
        • Hernandez R.K.
        • Sørensen H.T.
        • Pedersen L.
        • et al.
        Tamoxifen treatment and risk of deep venous thrombosis and pulmonary embolism: a Danish population-based cohort study.
        Cancer. 2009; 115: 4442-4449
        • Dowsett M.
        • Cuzick J.
        • Ingle J.
        • et al.
        Meta-analysis of breast cancer outcomes in adjuvant trials of aromatase inhibitors versus tamoxifen.
        J. Clin. Oncol. 2010; 28: 509-518
        • Nabholtz J.M.
        • Buzdar A.
        • Pollak M.
        • et al.
        Anastrozole is superior to tamoxifen as first-line therapy for advanced breast cancer in postmenopausal women: results of a North American multicenter randomized trial. Arimidex Study Group.
        J. Clin. Oncol. 2000; 18: 3758-3767
        • Bonneterre J.
        • Thürlimann B.
        • Robertson J.F.
        • et al.
        Anastrozole versus tamoxifen as first-line therapy for advanced breast cancer in 668 postmenopausal women: results of the Tamoxifen or Arimidex Randomized Group Efficacy and Tolerability study.
        J. Clin. Oncol. 2000; 18: 3748-3757
        • Baum M.
        • Budzar A.U.
        • Cuzick J.
        • et al.
        ATAC Trialists' Group, Anastrozole alone or in combination with tamoxifen versus tamoxifen alone for adjuvant treatment of postmenopausal women with early breast cancer: first results of the ATAC randomised trial.
        Lancet. 2002; 359: 2131-2139
        • Baum M.
        • Buzdar A.
        • Cuzick J.
        • et al.
        ATAC (Arimidex, Tamoxifen Alone or in Combination) Trialists' Group, Anastrozole alone or in combination with tamoxifen versus tamoxifen alone for adjuvant treatment of postmenopausal women with early-stage breast cancer: results of the ATAC (Arimidex, Tamoxifen Alone or in Combination) trial efficacy and safety update analyses.
        Cancer. 2003; 98: 1802-1810
        • Howell A.
        • Cuzick J.
        • Baum M.
        • et al.
        ATAC Trialists' Group, Results of the ATAC (Arimidex, Tamoxifen, Alone or in Combination) trial after completion of 5 years' adjuvant treatment for breast cancer.
        Lancet. 2005; 365: 60-62
        • Debourdeau P.
        • Espié M.
        • Chevret S.
        • et al.
        Incidence, risk factors, and outcomes of central venous catheter-related thromboembolism in breast cancer patients: the CAVECCAS study.
        Cancer Med. 2017; 6: 2732-2744
        • Shai A.
        • Rennert H.S.
        • Rennert G.
        • et al.
        Statins, aspirin and risk of thromboembolic events in ovarian cancer patients.
        Gynecol. Oncol. 2014; 133: 304-308
        • Rodriguez A.O.
        • Wun T.
        • Chew H.
        • et al.
        Venous thromboembolism in ovarian cancer.
        Gynecol. Oncol. 2007; 105: 784-790
        • Rauh-Hain J.A.
        • Hariton E.
        • Clemmer J.
        • et al.
        Incidence and effects on mortality of venous thromboembolism in elderly women with endometrial cancer.
        Obstet. Gynecol. 2015; 125: 1362-1370
        • Stâlberg K.
        • Svensson T.
        • Lonn S.
        • Kieler H.
        The influence of comorbidity on mortality in ovarian cancer patients.
        Gynecol. Oncol. 2014; 133: 298-303
        • Ebina Y.
        • Uchiyama M.
        • Imafuku H.
        • et al.
        Risk factors for deep venous thrombosis in women with ovarian cancer.
        Medicine (Baltimore). 2018; 97: e11009
        • Abu Saadeh F.
        • Norris L.
        • O'Toole S.
        • Gleeson N.
        Venous thromboembolism in ovarian cancer: incidence, risk factors and impact on survival.
        Eur. J. Obstet. Gynecol. Reprod. Biol. 2013; 170: 214-218
        • Mokri B.
        • Mariani A.
        • Heit J.A.
        • et al.
        Incidence and predictors of venous thromboembolism after debulking surgery for epithelial ovarian cancer.
        Int. J. Gynecol. Cancer. 2013; 23: 1684-1691
        • Fotopoulou C.
        • du Bois A.
        • Karavas A.N.
        • et al.
        Arbeitsgemeinschaft Gynaekologische Onkologie Ovarian Cancer Study Group, Incidence of venous thromboembolism in patients with ovarian cancer undergoing platinum/paclitaxel-containing first-line chemotherapy: an exploratory analysis by the Arbeitsgemeinschaft Gynaekologische Onkologie Ovarian Cancer Study Group.
        J. Clin. Oncol. 2008; 26: 2683-2689
        • Fotopoulou C.
        • Karavas A.
        • Trappe R.
        • et al.
        Venous thromboembolism in recurrent ovarian cancer-patients: a systematic evaluation of the North-Eastern German Society of Gynaecologic Oncology Ovarian Cancer Study Group (NOGGO).
        Thromb. Res. 2009; 124: 531-535
        • Einstein M.H.
        • Pritts E.A.
        • Hartenbach E.M.
        Venous thromboembolism prevention in gynecologic cancer surgery: a systematic review.
        Gynecol. Oncol. 2007; 105: 813-819
        • Schmeler K.M.
        • Wilson G.L.
        • Cain K.
        • et al.
        Venous thromboembolism (VTE) rates following the implementation of extended duration prophylaxis for patients undergoing surgery for gynecologic malignancies.
        Gynecol. Oncol. 2013; 128: 204-208
        • Kushnir C.L.
        • Diaz-Montes T.P.
        Perioperative care in gynecologic oncology.
        Curr. Opin. Obstet. Gynecol. 2013; 25: 23-28
        • Felder S.
        • Rasmussen M.S.
        • King R.
        • et al.
        Prolonged thromboprophylaxis with low molecular weight heparin for abdominal or pelvic surgery.
        Cochrane Database Syst. Rev. 2018; 11: CD004318
        • Martino M.A.
        • Williamson E.
        • Rajaram L.
        • et al.
        Defining practice patterns in gynecologic oncology to prevent pulmonary embolism and deep venous thrombosis.
        Gynecol. Oncol. 2007; 106: 439-445
        • Uppal S.
        • Hernandez E.
        • Dutta M.
        • et al.
        Prolonged postoperative venous thromboembolism prophylaxis is cost-effective in advanced ovarian cancer patients.
        Gynecol. Oncol. 2012; 127: 631-637
        • Moliterno A.R.
        • Williams D.M.
        • Rogers O.
        • Spivak J.L.
        Molecular mimicry in the chronic myeloproliferative disorders: reciprocity between quantitative JAK2 V617F and Mpl expression.
        Blood. 2006; 108: 3913-3915
        • Spivak J.L.
        • Considine M.
        • Williams D.M.
        • et al.
        Two clinical phenotypes in polycythemia vera.
        N. Engl. J. Med. 2014; 371: 808-817
        • Stein B.L.
        • Williams D.M.
        • Wang N.-Y.
        • et al.
        Sex differences in the JAK2 V617F allele burden in chronic myeloproliferative disorders.
        Haematologica. 2010; 95: 1090-1097
        • Marchioli R.
        • Finazzi G.
        • Landolfi R.
        • et al.
        Vascular and neoplastic risk in a large cohort of patients with polycythemia vera.
        J. Clin. Oncol. 2005; 23: 2224-2232
        • Patrono C.
        • Rocca B.
        • De Stefano V.
        Platelet activation and inhibition in polycythemia vera and essential thrombocythemia.
        Blood. 2013; 121: 1701-1711
        • Hultcrantz M.
        • Bjorkholm M.
        • Dickman P.W.
        • et al.
        Risk for arterial and venous thrombosis in patients with myeloproliferative neoplasms: a population-based cohort study.
        Ann. Intern. Med. 2018; 168: 317-325
        • Tefferi A.
        • Rumi E.
        • Finazzi G.
        • et al.
        Survival and prognosis among 1545 patients with contemporary polycythemia vera: an international study.
        Leukemia. 2013; 27: 1874-1881
        • Cote D.J.
        • Smith T.R.
        Venous thromboembolism in brain tumor patients.
        J. Clin. Neurosci. 2016; 25: 13-18
        • Smith T.R.
        • Nanney A.D.
        • Lall R.R.
        • et al.
        Development of venous thromboembolism (VTE) in patients undergoing surgery for brain tumors: results from a single center over a 10 year period.
        J. Clin. Neurosci. 2015; 22: 519-525
        • Britton L.
        Unintended pregnancy: a systematic review of contraception use and counseling in women with cancer.
        Clin. J. Oncol. Nurs. 2017; 21: 189-196
        • Suissa S.
        • Blais L.
        • Spitzer W.O.
        • et al.
        First-time use of newer oral contraceptives and the risk of venous thromboembolism.
        Contraception. 1997; 56: 141-146
        • Farley T.M.
        • Meirik O.
        • Marmot M.G.
        • et al.
        Oral contraceptives and risk of venous thromboembolism: impact of duration of use.
        Contraception. 1998; 57: 61-65
        • Roach R.E.J.
        • 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. 2013; 11: 124-131
        • Sweetland S.
        • Beral V.
        • Balkwill A.
        • et al.
        Million Women Study Collaborators, Venous thromboembolism risk in relation to use of different types of postmenopausal hormone therapy in a large prospective study.
        J. Thromb. Haemost. 2012; 10: 2277-2286
        • Jacobsen A.F.
        • Sandset P.M.
        Venous thromboembolism associated with pregnancy and hormonal therapy.
        Best Pract. Res. Clin. Haematol. 2012; 25: 319-332
        • Weill A.
        • Dalichampt M.
        • Raguideau F.
        • et al.
        Low dose oestrogen combined oral contraception and risk of pulmonary embolism, stroke, and myocardial infarction in five million French women: cohort study.
        BMJ. 2016; 353: i2002
        • 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. 2014; 12: 635-640
        • de Bastos M.
        • Stegeman B.H.
        • Rosendaal F.R.
        • et al.
        Combined oral contraceptives: venous thrombosis.
        Cochrane Database Syst. Rev. 2014; (CD010813)
        • Brenner B.
        • Avivi I.
        • Lishner M.
        Haematological cancers in pregnancy.
        Lancet. 2012; 379: 580-587
        • 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. 2012; 345: e4944
        • Lidegaard O.
        • Nielsen L.H.
        • Skovlund C.W.
        • Løkkegaard E.
        Venous thrombosis in users of non-oral hormonal contraception: follow-up study, Denmark 200-10.
        BMJ. 2012; 344: e2990
        • Holst A.G.
        • Jensen G.
        • Prescott E.
        Risk factors for venous thromboembolism: results from the Copenhagen City Heart Study.
        Circulation. 2010; 121: 1896-1903
        • Olié V.
        • Zhu T.
        • Martinez I.
        • et al.
        Sex-specific risk factors for recurrent venous thromboembolism.
        Thromb. Res. 2012; 130: 16-20
        • Walker A.J.
        • West J.
        • Card T.R.
        • et al.
        When are breast cancer patients at highest risk of venous thromboembolism? A cohort study using English health care data.
        Blood. 2016; 127 (quiz 953): 849-857
        • Pomp E.R.
        • le Cessie S.
        • Rosendaal F.R.
        • Doggen C.J.M.
        Risk of venous thrombosis: obesity and its joint effect with oral contraceptive use and prothrombotic mutations.
        Br. J. Haematol. 2007; 139: 289-296
        • Abdollahi M.
        • Cushman M.
        • Rosendaal F.R.
        Obesity: risk of venous thrombosis and the interaction with coagulation factor levels and oral contraceptive use.
        Thromb. Haemost. 2003; 89: 493-498
        • Zuurbier S.M.
        • Arnold M.
        • Middeldorp S.
        • et al.
        Risk of cerebral venous thrombosis in obese women.
        JAMA. Neurol. 2016; 73: 579-584
        • Turan V.
        • Quinn M.M.
        • Dayioglu N.
        • et al.
        The impact of malignancy on response to ovarian stimulation for fertility preservation: a meta-analysis.
        Fertil. Steril. 2018; 110: 1347-1355
        • von Wolff M.
        • Bruckner T.
        • Strowitzki T.
        • Germeyer A.
        Fertility preservation: ovarian response to freeze oocytes is not affected by different malignant diseases-an analysis of 992 stimulations.
        J. Assist. Reprod. Genet. 2018; 35: 1713-1719
        • Lefebvre T.
        • Mirallié S.
        • Leperlier F.
        • et al.
        Ovarian reserve and response to stimulation in women undergoing fertility preservation according to malignancy type.
        Reprod. Biomed. Online. 2018; 37: 201-207
        • Srikanthan A.
        • Amir E.
        • Bedard P.
        • et al.
        Fertility preservation in post-pubescent female cancer patients: a practical guideline for clinicians.
        Mol. Clin. Oncol. 2018; 8: 153-158
        • Loren A.W.
        • Mangu P.B.
        • Beck L.N.
        • et al.
        American Society of Clinical Oncology, Fertility preservation for patients with cancer: American Society of Clinical Oncology clinical practice guideline update.
        J. Clin. Oncol. 2013; 31: 2500-2510
        • Peccatori F.A.
        • Azim H.A.
        • Orecchia R.
        • et al.
        ESMO Guidelines Working Group, Cancer, pregnancy and fertility: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up.
        Ann. Oncol. 2013; 24 (vi): 160-170
        • Donnez J.
        • Dolmans M.-M.
        Fertility preservation in women.
        Nat. Rev. Endocrinol. 2013; 9: 735-749
        • Roberts J.
        • Ronn R.
        • Tallon N.
        • Holzer H.
        Fertility preservation in reproductive-age women facing gonadotoxic treatments.
        Curr. Oncol. 2015; 22: e294-e304
        • Muñoz M.
        • Santaballa A.
        • Seguí M.A.
        • et al.
        SEOM Clinical Guideline of fertility preservation and reproduction in cancer patients (2016).
        Clin. Transl. Oncol. 2016; 18: 1229-1236
        • Font-Gonzalez A.
        • Mulder R.L.
        • Loeffen E.A.H.
        • et al.
        PanCareLIFE Consortium, Fertility preservation in children, adolescents, and young adults with cancer: Quality of clinical practice guidelines and variations in recommendations.
        Cancer. 2016; 122: 2216-2223
        • Goldfarb S.B.
        • Kamer S.A.
        • Oppong B.A.
        • et al.
        Fertility preservation for the young breast cancer patient.
        Ann. Surg. Oncol. 2016; 23: 1530-1536
        • Azim A.A.
        • Costantini-Ferrando M.
        • Oktay K.
        Safety of fertility preservation by ovarian stimulation with letrozole and gonadotropins in patients with breast cancer: a prospective controlled study.
        J. Clin. Oncol. 2008; 26: 2630-2635
        • Somigliana E.
        • Peccatori F.A.
        • Filippi F.
        • et al.
        Risk of thrombosis in women with malignancies undergoing ovarian stimulation for fertility preservation.
        Hum. Reprod. Update. 2014; 20: 944-951
        • Rova K.
        • Passmark H.
        • Lindqvist P.G.
        Venous thromboembolism in relation to in vitro fertilization: an approach to determining the incidence and increase in risk in successful cycles.
        Fertil. Steril. 2012; 97: 95-100
        • Cakmak H.
        • Katz A.
        • Cedars M.I.
        • Rosen M.P.
        Effective method for emergency fertility preservation: random-start controlled ovarian stimulation.
        Fertil. Steril. 2013; 100: 1673-1680
        • Sighinolfi G.
        • Sunkara S.K.
        • La Marca A.
        New strategies of ovarian stimulation based on the concept of ovarian follicular waves: from conventional to random and double stimulation.
        Reprod. Biomed. Online. 2018; 37: 489-497
        • Moustafa F.
        • Fernández S.
        • Fernández-Capitán C.
        • et al.
        RIETE Investigators, Uterine bleeding during anticoagulation in women with venous thromboembolism.
        Thromb. Res. 2017; 151: S1-S5
        • James A.H.
        Venous thromboembolism in pregnancy.
        Arterioscler. Thromb. Vasc. Biol. 2009; 29: 326-331
        • Jacobsen A.F.
        • Skjeldestad F.E.
        • Sandset P.M.
        Incidence and risk patterns of venous thromboembolism in pregnancy and puerperium - a register-based case-control study.
        Am. J. Obstet. Gynecol. 2008; 198: 233.e1-233.e7
        • Heit J.A.
        • Kobbervig C.E.
        • James A.H.
        • et al.
        Trends in the incidence of venous thromboembolism during pregnancy or postpartum: a 30-year population-based study.
        Ann. Intern. Med. 2005; 143: 697-706
        • Bates S.M.
        Pregnancy-associated venous thromboembolism: prevention and treatment.
        Semin. Hematol. 2011; 48: 271-284
        • Middeldorp S.
        How I treat pregnancy-related venous thromboembolism.
        Blood. 2011; 118: 5394-5400
        • Bates S.M.
        • Greer I.A.
        • Middeldorp S.
        • et al.
        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-e736S
        • Horowitz N.A.
        • Lavi N.
        • Nadir Y.
        • Brenner B.
        Haematological malignancies in pregnancy: An overview with an emphasis on thrombotic risks.
        Thromb. Haemost. 2016; 116: 613-617
        • Greer I.A.
        • Nelson-Piercy C.
        Low-molecular-weight heparins for thromboprophylaxis and treatment of venous thromboembolism in pregnancy: a systematic review of safety and efficacy.
        Blood. 2005; 106: 401-407
        • Schaefer C.
        • Hannemann D.
        • Meister R.
        • et al.
        Vitamin K antagonists and pregnancy outcome. A multi-centre prospective study.
        Thromb. Haemost. 2006; 95: 949-957