Thromboembolism risk following recurrent miscarriage

References

• Wilcox AJ, Weinberg CR, O’Connor JF et al. Incidence of early loss of pregnancy. N. Engl. J. Med. 319, 189–194 (1988).
   PubMed Web of Science ®Google Scholar
• Clark DA, Coulam CB, Daya S, Chaouat G. Unexplained sporadic and recurrent miscarriage in the new millennium: a critical analysis of immune mechanisms and treatments. Hum. Reprod. Update 7, 501–511 (2001).
   PubMed Web of Science ®Google Scholar
• ACOG Practice Bulletin. Management of recurrent early pregnancy loss. Int. J. Gynecol. Obstet. 78, 179–190 (2002).
   PubMed Web of Science ®Google Scholar
• Li TC, Markris M, Tomsu M, Tuckerman E, Laird S. Recurrent miscarriage: aetiology, management and prognosis. Hum. Reprod. Update 8, 463–481 (2002).
   PubMed Web of Science ®Google Scholar
• Rai R, Regan L. Recurrent miscarriage. Lancet 368, 601–611 (2006).
   PubMed Web of Science ®Google Scholar
• D’Uva M, Di Micco P, Strina I, De Placido G. Recurrent pregnancy loss and thrombophilia. J. Clin. Med. Res. 2, 18–22 (2010).
   Google Scholar
• Eldor A. Thrombophilia, thrombosis and pregnancy. Thromb. Haemost. 86, 104–111 (2011).
   Google Scholar
• Carp H, Salomon O, Seidman D, Dardik R, Rosenberg N, Inbal A. Prevalence of genetic markers for thrombophilia in recurrent pregnancy loss. Hum. Reprod. 17, 1633–1637 (2002).
   PubMed Web of Science ®Google Scholar
• Prandoni P, Tormene D, Simioni P, Girolami A. Venous thromboembolism, fetal loss and preclampsia in pregnant women with congenital thrombophilia. Clin. Lab. 47, 155–159 (2001).
   Google Scholar
• Di Micco P, D’Uva M, Strina I et al. Recurrent pregnancy loss and thrombophilia. Clin. Lab. 53, 309–314 (2007).
   Google Scholar
• Lockwood CJ. Pregnancy-associated changes in the hemostatic system. Clin. Obstet. Gynecol. 49, 836–843 (2006).
   PubMed Web of Science ®Google Scholar
• Brenner B. Haemostatic changes in pregnancy. Thromb. Res. 114(5–6), 409–414 (2004).
   PubMed Web of Science ®Google Scholar
• Robertson L, Wu O, Langhorne P et al. Thrombophilia in pregnancy: a systematic review. Br. J. Haematol. 132, 171–196 (2006).
   PubMed Web of Science ®Google Scholar
• Pabinger I. Thrombophilia and its impact on pregnancy. Thromb. Res. 123(S3), 16–21 (2009).
   Google Scholar
• Martínez-Zamora MA, Cervera R, Balasch J. Recurrent miscarriage, antiphospholipid antibodies and the risk of thromboembolic disease. Clinic. Rev. Allerg. Immunol. 43, 265–274 (2012).
   Google Scholar
• Practice Committee of the American Society for Reproductive Medicine. Definitions of infertility and recurrent pregnancy loss. Fertil. Steril. 89, 1603 (2008).
   PubMed Web of Science ®Google Scholar
• Stephenson M, Kutteh W. Evaluation and management of recurrent early pregnancy loss. Clin. Obstet. Gynecol. 1, 132–145 (2007).
   Google Scholar
• Toth B, Jeschke U, Rogenhofer N, et al. Recurrent miscarriage: current concepts in a diagnosis and treatment. J. Reprod. Immunol. 85, 25–32 (2010).
   PubMed Web of Science ®Google Scholar
• Christiansen OB, Steffensen R, Nielsen H, Varming K. Multifactorial etiology of recurrent miscarriage and its scientific and clinical implications. Gynecol. Obstet. Invest. 66, 257–267 (2008).
   PubMed Web of Science ®Google Scholar
• Balasch J, Font J, López-Soto A et al. Antiphospholipid antibodies in unselected patients with repeated abortion. Hum. Reprod. 5, 43–6 (1990).
   PubMed Web of Science ®Google Scholar
• Balasch J, Creus M, Fábregues F, et al. Antiphospholipid antibodies and human reproductive failure. Hum. Reprod. 11, 2310–2315 (1996).
   PubMed Web of Science ®Google Scholar
• Balasch J, Carmona F, Creus M, Font J, Cervera R. Management of reproductive failure in the antiphospholipid syndrome. In: The antiphospholipid syndrome II: Autoimmune thrombosis. Asherson RA, Cervera R, Piette JC, Shoenfeld Y ( Ed.), Elsevier, 375–294 (2002).
   Google Scholar
• Harger JH, Archer DF, Marchese SG, Muracca-Clemens M, Garver KL. Etiology of recurrent pregnancy losses and outcome of subsequent pregnancies. Obstet. Gynecol. 62,574–581 (1983).
   PubMed Web of Science ®Google Scholar
• Coulam CB. Epidemiology of recurrent abortion. Am. J. Reprod. Immunol. 1991; 26, 23–27 (1991).
   PubMed Web of Science ®Google Scholar
• Hatasaka HH. Recurrent miscarriage: epidemiologic factors, definitions, and incidence. Clin. Obstet. Gynecol. 37, 625–634 (1994).
   PubMedGoogle Scholar
• Hill JA. Sporadic and recurrent spontaneous abortion. Curr. Prob. Obstet. Gynecol. Fertil. 17, 116–163 (1994).
   Google Scholar
• Gasbarrini A, Torre ES, Trivellini C et al. Recurrent spontaneous abortion and intrauterine fetal growth retardation as symptoms of celiac disease. Lancet 356, 399–400 (2000).
   PubMed Web of Science ®Google Scholar
• Regan L. Recurrent early pregnancy failure. Curr. Opin. Obstet. Gynecol. 4, 220–228 (1992).
   Google Scholar
• Regan L, Braude PB, Trembath PL. Influence of past reproductive performance on risk of spontaneous abortion. Br. Med. J. 299, 541–546 (1989).
   PubMed Web of Science ®Google Scholar
• Cauchi MN, Coulam CB, Cowchock S et al. Predictive factors in recurrent spontaneous aborters – a multicenter study. Am. J. Reprod. Immunol. 33, 165–170 (1995).
   Google Scholar
• Greaves M. Antiphospholipid syndrome: state of the art with emphasis on laboratory evaluation. Haemostasis 30(S2), 16–25 (2000).
   Google Scholar
• Greaves M, Cohen H, Machin SJ, Mackie I. Guidelines on the investigation and management of the antiphospholipid syndrome. Br. J. Haematol. 109, 704–715 (2000).
   PubMed Web of Science ®Google Scholar
• Vinatier D, Dufour P, Cosson M, Houpeau JL. Antiphospholipid syndrome and recurrent miscarriages. Eur. J. Obstet. Gynecol. 96,37–50 (2001).
   PubMed Web of Science ®Google Scholar
• Lockshin MD. Pregnancy loss in the antiphospholipid syndrome. Thromb. Haemostasis 82, 641–648 (1999).
   Google Scholar
• Ogasawara M, Sasa H, Katano K, Aoyama T, Aoki K, Suzumori K. Recurrent abortion and moderate or strong antiphospholipiod antibody production. Int. J. Gynecol. Obstet. 62, 183–188 (1998).
   Google Scholar
• Miyakis S, Lockshin MD, Atsumi T et al. International consensus statement on an update of the classification criteria for definite antiphospholipid syndrome (APS). J. Thromb. Haemost. 4, 295–306 (2006).
   PubMed Web of Science ®Google Scholar
• O’Riordan MN, Higgins JR. Haemostasis in normal and abnormal pregnancy. Best Pract. Res. Clin. Obstet. Gynaecol. 17, 385–396 (2003).
   PubMed Web of Science ®Google Scholar
• Martinez-Zamora MA, Tassies D, Carmona F et al. Thrombin activatable fibrinolysis inhibitor and clot lysis time in pregnant patients with antiphospholipid syndrome: relationship with pregnancy outcome and thrombosis. Am. J. Reprod. Immunol. 62, 381–389 (2009).
   Google Scholar
• Bretelle F, Sabatier F, Desprez D et al. Circulating microparticles: a marker of procoagulant state in normal pregnancy and pregnancy complicated by preeclampsia or intrauterine growth restriction. Thromb. Haemost. 89, 486–492 (2003).
   PubMed Web of Science ®Google Scholar
• Buchholz T, Thaler CJ. Inherited thrombophilia: impact on human reproduction. Am. J. Reprod. Immunol. 50, 20–32 (2003).
   PubMed Web of Science ®Google Scholar
• Rey E, Kahn SR, David M, Shrier I. Thrombophilic disorders and fetal loss: a meta-analysis. Lancet 361, 901–908 (2003).
   PubMed Web of Science ®Google Scholar
• Kovalevsky G, Gracia CR, Berlin JA, Sammel MD, Barnhart KT. Evaluation of the association between hereditary thrombophilias and recurrent pregnancy loss: a meta-analysis. Arch. Intern. Med. 14, 558–563 (2004).
   Google Scholar
• Benedetto C, Marozio L, Tavella AM, Salton L, Grivon S, Di Giampaolo F. Coagulation disorders in pregnancy: acquired and inherited thrombophilias. Ann. N. Y. Acad. Sci. 1205, 106–117 (2010).
   PubMed Web of Science ®Google Scholar
• Martinelli I. Thromboembolism in women. Sem. Thromb. Hemost. 32, 709–715 (2006).
   PubMedGoogle Scholar
• Rodger MA, Betancourt MT, Clark P, et al. The association of factor V Leiden and prothrombin gene mutation and placenta-mediated pregnancy complications: a systematic review and meta-analysis of prospective cohort studies. PLoS Med. 7, e1000292 (2010).
   PubMed Web of Science ®Google Scholar
• Bates SM, Greer IA, Middeldorp S, et al. VTE, thrombophilia, antithombotic therapy , and pregnancy. Antithrombotic therapy and prevention of thrombosis, 9th ed: American College of Chest Physicians evidence-based clinical practice guidelines. Chest 141, e691S–e736S.
   Google Scholar
• Coulam CB, Jeyendran RS, Fishel LA, Roussev R. Multiple thrombophilic gene mutations rather than specific gene mutations are risk factors for recurrent miscarriage. Am. J. Reprod. Immunol. 55, 360–368 (2006).
   PubMed Web of Science ®Google Scholar
• Tulppala M, Viinikka L, Ylikorkaka O. Thromboxane dominance and prostacyclin deficiency in habitual abortion. Lancet 387, 879–381 (1991).
   Google Scholar
• Rai R. Is miscarriage a coagulopathy? Curr. Opin. Obstet. Gynecol. 15, 265–268 (2003).
   Google Scholar
• Woodhams BJ, Candotti G, Shaw R, Kernoff PBA. Changes in coagulation and fibrinolysis during pregnancy: evidence of activation of coagulation preceding spontaneous abortion. Thromb. Res. 55, 99–107 (1989).
   PubMed Web of Science ®Google Scholar
• Martínez-Zamora MA, Creus M, Tassies D et al. Thrombin activatable fibrinolysis inhibitor and clot lysis time in women with recurrent miscarriage associated with the antiphospholipid syndrome. Fertil. Steril. 94, 2437–2440 (2010).
   Google Scholar
• Marchi R, López Ramirez Y, Nagaswami C et al. Haemostatic changes related to fibrin formation and fibrinolysis during the first trimester in normal pregnancy and in recurrent miscarriage. Thromb. Haemost. 97, 552–557 (2007).
   Google Scholar
• Gris JC, Schved JF, Neveu S, Mares P, Aguilar-Martinez P, Dupaigne D. Impaired fibrinolytic capacity and early recurrent spontaneous abortion. BMJ 300, 1500 (1990).
   PubMedGoogle Scholar
• Gris JC, Ripart-Neveu S, Maugard C, et al. Prospective evaluation of the prevalence of haemostasis abnormalities in unexplained primary early recurrent miscarriages. Thromb. Haemost. 77, 1096–1103 (1997).
   PubMed Web of Science ®Google Scholar
• Vincent T, Rai R, Regan L, Cohen H. Increased thrombin generation in women with recurrent miscarriage. Lancet 352, 116 (1998).
   PubMed Web of Science ®Google Scholar
• Rai R, Tuddenham E, Backos M, et al. Thromboelastography, whole-blood haemostasis and recurrent miscarriage. Hum. Reprod. 18, 2540–2503 (2003).
   PubMed Web of Science ®Google Scholar
• De Saint Martin L, Duchemin J, Bohec C, et al. Increased thrombin generation measured in the presence of thrombomodulin in women with early pregnancy loss. Fertil. Steril. 95, 1813–1815 (2011).
   Google Scholar
• Smith GCS, Pell JP, Walsh D. Pregnancy complications and maternal risk or ischaemic heart disease: a retrospective cohort study of 129290 births. Lancet 257, 2002–2006 (2001).
   Google Scholar
• Smith GCS, Pell JP, Walsh D. Spontaneous loss of early pregnancy and risk of ischaemic heart disease in later life: retrospective cohort study. BMJ 326, 423–424 (2003).
   PubMed Web of Science ®Google Scholar
• Ness RM, Harris T, Cobb J, et al. Number of pregnancies and the subsequent risk of cardiovascular disease. N. Engl. J. Med. 328, 1528–1533 (1993).
   PubMed Web of Science ®Google Scholar
• Smith GCS, Wood AM, Pell JP, Hattie J. Recurrent miscarriage is associated with a family history of ischaemic heart disease: a retrospective cohort study. BJOG 118, 557–563 (2011).
   PubMed Web of Science ®Google Scholar
• Martínez-Zamora MA, Peralta S, Creus M, et al. Risk of thromboembolic events after recurrent spontaneous abortion in antiphospholipid syndrome: a case-control study. Ann. Rheum. Dis. 71, 61–66 (2012).
   PubMed Web of Science ®Google Scholar
• Simioni P, Tormene D, Spiezia L et al. Inherited thrombophilia and venous thromboembolism. Semin. Thromb. Hemost. 32, 700–708 (2006).
   PubMed Web of Science ®Google Scholar
• Finan RR, Tamim H, Ameen G, Sharida HE, Rashid M, Almawi WY. Prevalence of factor V G1691A (factor V-Leiden) and prothrombin G20210A gene mutations in a recurrent miscarriage population. Am. J. Hematol. 71, 300–305 (2002).
   PubMed Web of Science ®Google Scholar
• Wu O, Robertson L, Langhorne P et al. Oral contraceptives, hormone replacement therapy, thrombophilias and risk of venous thromboembolism: a systematic review. Thromb. Haemost. 94, 17–25 (2005).
   PubMed Web of Science ®Google Scholar
• Meroni PL. Pathogenersis of the antiphospholipid syndrome: and additional example for the mosaic of autoimmunity. J. Autoimmun. 30, 99–103 (2008).
   PubMed Web of Science ®Google Scholar
• Meroni PL, Shoenfeld Y. Predicitive, protective, orphan autoantibodies: the example of anti-phospholipid antibodies. Autoimmun. Rev. 2008; 7, 585–587 (2008).
   PubMed Web of Science ®Google Scholar
• Cervera R, Khamashta MA, Shoenfeld Y et al. Morbidity and mortality in the antiphospholipid syndrome during a 5-year period: a multicentre prospective study of 1000 patients. Ann. Rheum. Dis. 68,1428–1432 (2009).
   PubMed Web of Science ®Google Scholar
• Espinosa G, Cervera R. Antiphospholipid syndrome: frequency, main causes and risk factors of mortality. Nat. Rev. Rheumatol. 6, 296–300 (2010).
   PubMedGoogle Scholar
• Rodriguez-Garcia JL, Bertolaccini ML, Cuadrado MJ, Sanna G, Ateka-Barutia O, Khamastha MA. Clinical manifestations of antiphospholipid syndrome (APS) with and without antiphospholipid antibodies (the so-called “seronegative APS”). Ann. Rheum. Dis. 71, 242–244 (2012).
   PubMed Web of Science ®Google Scholar
• Erkan D, Harrison MJ, Levy R et al. Aspirin for primary thrombosis prevention in the antiphospholipid syndrome. A randomized, double-blind, placebo-controlled trial in asymptomatic antiphospholipid antibody-positive individuals. Arthr. Rheum. 56, 2382–2391 (2007).
   PubMed Web of Science ®Google Scholar
• Hereng T, Lambert M, Samor M et al. Influence of aspirin on the clinical outcomes of 103 anti-phospholipid antibodies-positive patients. Lupus 17, 11–15 (2008).
   PubMed Web of Science ®Google Scholar
• Galli M, Luciani D, Bertolini G, Barbui T. Anti-β2-glycoprotein I, antiprothrombin antibodies, and the risk of thrombosis in the antiphospholipid syndrome. Blood 102, 2717–2723 (2003).
   PubMed Web of Science ®Google Scholar
• Galli M. The antiphospholipid triangle. J. Thromb. Haemost. 8,234–236 (2009).
   Google Scholar
• Tincani A, Andreoli L, Casu C, Cattaneo R, Meroni P. Antiphospholipid antibody profile: implications for the evaluation and management of patients. Lupus 19, 432–435 (2010).
   Google Scholar
• Urbanus RT, de Groot PG. Antiphospholipid antibodies – We are not quite there yet. Blood Reviews. 25, 97–106 (2011).
   Google Scholar
• Ruffati A, T Del Ross, Ciprian M, et al. Risk factors for a first thrombotic event in antiphospholipid antibody carriers. A multicentre, retrospective follow-up study. Ann. Rheum. Dis. 68, 397–399 (2009).
   PubMed Web of Science ®Google Scholar
• Ruffatti A, Del Ross T, Ciprian M et al. Risk factors for a first thrombotic event in antiphospholipid antibody carriers: a prospective multicentre follow-up study. Ann. Rheum. Dis. 70, 1083–1086 (2011).
   PubMed Web of Science ®Google Scholar
• Erkan D, Yazici Y, Peterson MG, Sammaritano L, Lockshin MD. A cross-sectional study of clinical thrombotic risk factors and preventive treatments in antiphospholipid syndrome. Rheumatology 41, 924–929 (2002).
   PubMed Web of Science ®Google Scholar
• Pengo V, Ruffatti A, Legnani C, et al. Clinical course of high-risk patients diagnosed with antiphospholipid syndrome. J. Thromb. Haemost. 8, 237–242 (2010).
   PubMed Web of Science ®Google Scholar
• Quenby S, Farquharson RG, Dawood F, Hughes AM, Topping J. Recurrent miscarriage and long-term thrombosis risk: a case-control study. Hum. Reprod. 20, 1729–1732 (2005).
   PubMed Web of Science ®Google Scholar
• Silver RM, Draper ML, Scott JR, Lyon JL, Reading J, Branch W. Clinical consequences of antiphospholipid antibodies: an historic cohort study. Obstet. Gynecol. 83, 372–377 (1994).
   Google Scholar
• Tincani A, Taglietti M, Biasini C, Frassi M, Gorla R, Balestrieri G. Thromboembolic events after fetal loss in patients with antiphospholipid syndrome. Arthritis. Rheum. 46, 1126–1127 (2001).
   Google Scholar
• Erkan D, Merrill JT, Yazici Y, Sammaritano L, Buyon JP, Lockshin MD. High thrombosis rate after fetal loss in antiphospholipid syndrome: effective prophylaxis with aspirin. Arthritis. Rheum. 44, 1466–1467 (2001).
   PubMed Web of Science ®Google Scholar
• Gris JC, Bouvier S, Molinari et al. Comparative incidence of a first thrombotic event in purely obstetric antiphospholipid syndrome with pregnancy loss: the NOH-APS observational study. Blood 119, 2624–2632 (2012).
   PubMed Web of Science ®Google Scholar
• Ruffatti A, Tonello M, Del Ross T, et al. Antibody profile and clinical course in primary antiphospholipid syndrome with pregnancy morbidity. Thromb. Haemost. 96, 337–341 (2006).
   PubMed Web of Science ®Google Scholar
• Simioni P, Tormene D, Spiezia L, et al. Inherited thrombophilia and venous thromboembolism. Semin, Thromb. Hemost. 32, 700–708 (2006).
   PubMed Web of Science ®Google Scholar
• Ruiz-Irastoriza G, Cuadrado MJ, Ruiz-Arruza I, et al. Evidence-based recommendations for the prevention and long-term management of thrombosis in antiphospholipid antibody-postive patients: Report of a Task Force at the 13th International Congress on Antiphospholipid Antibodies. Lupus 20, 206–218 (2011).
   Google Scholar