Seminars in Perinatology
Volume 31, Issue 3 , Pages 167-175 , June 2007

Thromboembolism in Pregnancy: Recurrence and Its Prevention

References 

  1. Bremme KA. Haemostatic changes in pregnancy. Best Pract Res Clin Haematol. 2003;16:153–168
  2. Medcalf RL, Stasinopoulos SJ. The undecided serpin. The ins and outs of plasminogen activator inhibitor type 2. 2005;4858–4867FEBS J 272
  3. Postpartum hemorrhage. From the Prevention of Postpartum Hemorrhage Initiative Web Site. Office of Health, Infectious Diseases and Nutrition, Bureau for Global Health, USAID. Available at: http://www.pphprevention.org/pph.php. Last accessed January 28, 2007.
  4. Chang J, Elam-Evans LD, Berg CJ, et al. Pregnancy-related mortality surveillance: United States, 1991–1999. MMWR Surv Summ. 2003;52:1–8
  5. Heit JA, Kobbervig CE, James AH, 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
  6. James AH, Bushnell CD, Jamison MG, et al. Incidence and risk factors for stroke in pregnancy and the puerperium. Obstet Gynecol. 2005;106:509–516
  7. James AH, Jamison MG, Biswas MS, et al. Acute myocardial infarction in pregnancy: a United States population-based study. Circulation. 2006;113:1564–1571
  8. Kittner SJ, Stern BJ, Feeser BR, et al. Pregnancy and the risk of stroke. N Engl J Med. 1996;335:768–774
  9. James AH, Jamison MG, Brancazio LR, et al. Venous thromboembolism during pregnancy and the postpartum period: incidence, risk factors, and mortality. Am J Obstet Gynecol. 2006;194:1311–1315
  10. James AH, Tapson VF, Goldhaber SZ. Thrombosis during pregnancy and the postpartum period. Am J Obstet Gynecol. 2005;193:216–219
  11. Pabinger I, Grafenhofer H, Kyrle PA, et al. Temporary increase in the risk for recurrence during pregnancy in women with a history of venous thromboembolism. Blood. 2002;100:1060–1062
  12. Lamy C, Hamon JB, Coste J, et al. French Study Group on Stroke in Pregnancy Ischemic stroke in young women: risk of recurrence during subsequent pregnancies. Neurology. 2000;55:269–274
  13. Brill-Edwards P, Ginsberg JS, Gent M, et al. Safety of withholding heparin in pregnant women with a history of venous thromboembolism (Recurrence of Clot in This Pregnancy Study Group). N Engl J Med. 2000;343:1439–1444
  14. Pabinger I, Grafenhofer H, Kaider A, et al. Risk of pregnancy-associated recurrent venous thromboembolism in women with a history of venous thrombosis. J Thromb Haemost. 2005;3:949–954
  15. De Stefano V, Martinelli I, Rossi E, et al. The risk of recurrent venous thromboembolism in pregnancy and puerperium without antithrombotic prophylaxis. Br J Haematol. 2006;135:386–391
  16. Sanson BJ, Lensing AW, Prins MH, et al. Safety of low-molecular-weight heparin in pregnancy: a systematic review. Thromb Haemost. 1999;81:668–672
  17. Lepercq J, Conard J, Borel-Derlon A, et al. Venous thromboembolism during pregnancy: a retrospective study of enoxaparin safety in 624 pregnancies. Br J Obstet Gynaecol. 2001;108:1134–1140
  18. Dilley A, Austin H, El-Jamil M, et al. Genetic factors associated with thrombosis in pregnancy in a United States population. Am J Obstet Gynecol. 2000;183:1271–1277
  19. Gerhardt A, Scharf RE, Beckmann MW, et al. Prothrombin and factor V mutations in women with a history of thrombosis during pregnancy and the puerperium. N Engl J Med. 2000;342:374–380
  20. Ho WK, Hankey GJ, Quinlan DJ, et al. Risk of recurrent venous thromboembolism in patients with common thrombophilia: a systematic review. Arch Intern Med. 2006;166:729–736
  21. De Stefano V, Simioni P, Rossi E, et al. The risk of recurrent venous thromboembolism in patients with inherited deficiency of natural anticoagulants antithrombin, protein C and protein S. Haematologica. 2006;91:695–698
  22. Christiansen SC, Cannegieter SC, Koster T, et al. Thrombophilia, clinical factors, and recurrent venous thrombotic events. J Am Med Assoc. 2005;293:2352–2361
  23. De Stefano V, Martinelli I, Mannucci PM, et al. The risk of recurrent deep venous thrombosis among heterozygous carriers of both factor V Leiden and the G20210A prothrombin mutation. N Engl J Med. 1999;341:801–806
  24. Lindmarker P, Schulman S, Sten-Linder M, et al. The risk of recurrent venous thromboembolism in carriers and non-carriers of the G1691A allele in the coagulation factor V gene and the G20210A allele in the prothrombin gene. DURAC Trial Study Group. Duration of Anticoagulation. Thromb Haemost. 1999;81:684–689
  25. Pabinger I, Schneider B. Thrombotic risk in hereditary antithrombin III, protein C, or protein S deficiency. A cooperative, retrospective study. Gesellschaft fur Thrombose- und Hamostaseforschung (GTH) Study Group on Natural Inhibitors. Arterioscler Thromb Vasc Biol. 1996;16:742–748
  26. Conard J, Horellou MH, Van Dreden P, et al. Thrombosis and pregnancy in congenital deficiencies in AT III, protein C or protein S: study of 78 women. Thromb Haemost. 1990;63:319–320
  27. Hellgren M, Tengborn L, Abildgaard U. Pregnancy in women with congenital antithrombin III deficiency: experience of treatment with heparin and antithrombin. Gynecol Obstet Invest. 1982;14:127–141
  28. Krnic-Barrie S, O’Connor CR, Looney SW, et al. A retrospective review of 61 patients with antiphospholipid syndrome (Analysis of factors influencing recurrent thrombosis). Arch Intern Med. 1997;157:2101–2108
  29. Robertson L, Wu O, Langhorne P, et al. Thrombophilia in pregnancy: a systematic review. Br J Haematol. 2006;132:171–196
  30. James AH, Brancazio LR, Gehrig TR, et al. Low-molecular-weight heparin for thromboprophylaxis in pregnant women with mechanical heart valves. J Matern Fetal Neonatal Med. 2006;19:543–549
  31. Rhee E, Beckman M, Dowling N, et al. Protein S levels in normal pregnancy. Am J Obstet Gynecol. 2005;193:S174
  32. Lockwood CJ. Inherited thrombophilias in pregnant patients: detection and treatment paradigm. Obstet Gynecol. 2002;99:333–341
  33. Hellgren M, Blomback M. Studies on blood coagulation and fibrinolysis in pregnancy, during delivery and in the puerperium. I. Normal condition. Gynecol Obstet Invest. 1981;12:141–154
  34. Stirling Y, Woolf L, North WR, et al. Haemostasis in normal pregnancy. Thromb Haemost. 1984;52:176–182
  35. Dahlman T, Hellgren M, Blomback M. Changes in blood coagulation and fibrinolysis in the normal puerperium. Gynecol Obstet Invest. 1985;20:37–44
  36. Gerbasi FR, Bottoms S, Farag A, et al. Increased intravascular coagulation associated with pregnancy. Obstet Gynecol. 1990;75:385–389
  37. Sanchez-Luceros A, Meschengieser SS, Marchese C, et al. Factor VIII and von Willebrand factor changes during normal pregnancy and puerperium. Blood Coagul Fibrinolysis. 2003;14:647–651
  38. Wickstrom K, Edelstam G, Lowbeer CH, et al. Reference intervals for plasma levels of fibronectin, von Willebrand factor, free protein S and antithrombin during third-trimester pregnancy. Scand J Clin Lab Invest. 2004;64:31–40
  39. Faught W, Garner P, Jones G, et al. Changes in protein C and protein S levels in normal pregnancy. Am J Obstet Gynecol. 1995;172:147–150
  40. Cerneca F, Ricci G, Simeone R, et al. Coagulation and fibrinolysis changes in normal pregnancy (Increased levels of procoagulants and reduced levels of inhibitors during pregnancy induce a hypercoagulable state, combined with a reactive fibrinolysis). Eur J Obstet Gynecol Reprod Biol. 1997;73:31–36
  41. Clark P, Brennand J, Conkie JA, et al. Activated protein C sensitivity, protein C, protein S and coagulation in normal pregnancy. Thromb Haemost. 1998;79:1166–1170
  42. Kjellberg U, Andersson NE, Rosen S, et al. APC resistance and other haemostatic variables during pregnancy and puerperium. Thromb Haemost. 1999;81:527–531
  43. Jacques PF, Bostom AG, Williams RR, et al. Relation between folate status, a common mutation in methylenetetrahydrofolate reductase, and plasma homocysteine concentrations. Circulation. 1996;93:7–9
  44. Glueck CJ, Phillips H, Cameron D, et al. The 4G/4G polymorphism of the hypofibrinolytic plasminogen activator inhibitor type 1 gene: an independent risk factor for serious pregnancy complications. Metabolism. 2000;49:845–852
  45. 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. 2006;4:295–306
  46. Gordon M. Maternal physiology in pregnancy. In:  Gabbe S,  Niebyl J,  Simpson J editor. Normal and Problem Pregnancies. 4. New York, NY: Churchill Livingstone; 2002;p. 63–92
  47. Naimi TS, Lipscomb LE, Brewer RD, et al. Binge drinking in the preconception period and the risk of unintended pregnancy: implications for women and their children. Pediatrics. 2003;111:1136–1141
  48. Moore K. Organogenetic period: the fourth to eighth weeks. In: The Developing Human: Clinically Oriented Embryology. ed 6. Philadelphia, PA: WB Saunders Company; 1998;p. 83–106
  49. Nassar AH, Hobeika EM, Abd Essamad HM, et al. Pregnancy outcome in women with prosthetic heart valves. Am J Obstet Gynecol. 2004;191:1009–1013
  50. Chan WS, Anand S, Ginsberg JS. Anticoagulation of pregnant women with mechanical heart valves: a systematic review of the literature. Arch Intern Med. 2000;160:191–196
  51. Blickstein D, Blickstein I. The risk of fetal loss associated with Warfarin anticoagulation. Int J Gynaecol Obstet. 2002;78:221–225
  52. Vural KM, Ozatik MA, Uncu H, et al. Pregnancy after mechanical mitral valve replacement. J Heart Valve Dis. 2003;12:370–376
  53. Sadler L, McCowan L, White H, et al. Pregnancy outcomes and cardiac complications in women with mechanical, bioprosthetic and homograft valves. Br J Obstet Gynaecol. 2000;107:245–253
  54. Cotrufo M, De Feo M, De Santo LS, et al. Risk of warfarin during pregnancy with mechanical valve prostheses. Obstet Gynecol. 2002;99:35–40
  55. Schaefer C, Hannemann D, Meister R, et al. A multi-centre prospective study Vitamin K antagonists and pregnancy outcome. Thromb Haemost. 2006;95:949–957
  56. Iturbe-Alessio I, Fonseca MC, Mutchinik O, et al. Risks of anticoagulant therapy in pregnant women with artificial heart valves. N Engl J Med. 1986;315:1390–1393
  57. Srivastava AK, Gupta AK, Singh AV, et al. Effect of oral anticoagulant during pregnancy with prosthetic heart valve. Asian Cardiovasc Thorac Ann. 2002;10:306–309
  58. Meschengieser SS, Fondevila CG, Santarelli MT, et al. Anticoagulation in pregnant women with mechanical heart valve prostheses. Heart. 1999;82:23–26
  59. Chen WW, Chan CS, Lee PK, et al. Pregnancy in patients with prosthetic heart valves: an experience with 45 pregnancies. Q J Med. 1982;51:358–365
  60. Wesseling J, Van Driel D, Heymans HS, et al. Coumarins during pregnancy: long-term effects on growth and development of school-age children. Thromb Haemost. 2001;85:609–613
  61. Bates SM, Greer IA, Hirsh J, et al. Use of antithrombotic agents during pregnancy: the Seventh ACCP Conference on Antithrombotic and Thrombolytic Therapy. Chest. 2004;126(suppl):627S–644S
  62. Flessa HC, Kapstrom AB, Glueck HI, et al. Placental transport of heparin. Am J Obstet Gynecol. 1965;93:570–573
  63. Harenberg J, Schneider D, Heilmann L, et al. Lack of anti-factor Xa activity in umbilical cord vein samples after subcutaneous administration of heparin or low molecular mass heparin in pregnant women. Haemostasis. 1993;23:314–320
  64. Schneider D, Heilmann L, Harenberg J. [Placental transfer of low-molecular weight heparin]. Geburtshilfe Frauenheilkd. 1995;55:93–98
  65. Ginsberg JS, Kowalchuk G, Hirsh J, et al. Heparin therapy during pregnancy. Risks to the fetus and mother. Arch Intern Med. 1989;149:2233–2236
  66. Dahlman TC, Sjoberg HE, Ringertz H. Bone mineral density during long-term prophylaxis with heparin in pregnancy. Am J Obstet Gynecol. 1994;170:1315–1320
  67. Barbour LA, Kick SD, Steiner JF, et al. A prospective study of heparin-induced osteoporosis in pregnancy using bone densitometry. Am J Obstet Gynecol. 1994;170:862–869
  68. Casele H, Haney EI, James A, et al. Bone density changes in women who receive thromboprophylaxis in pregnancy. Am J Obstet Gynecol. 2006;195:1109–1113
  69. Dahlman TC. Osteoporotic fractures and the recurrence of thromboembolism during pregnancy and the puerperium in 184 women undergoing thromboprophylaxis with heparin. Am J Obstet Gynecol. 1993;168:1265–1270
  70. Fausett MB, Vogtlander M, Lee RM, et al. Heparin-induced thrombocytopenia is rare in pregnancy. Am J Obstet Gynecol. 2001;185:148–152
  71. Carlin AJ, Farquharson RG, Quenby SM, et al. Prospective observational study of bone mineral density during pregnancy: low molecular weight heparin versus control. Hum Reprod. 2004;19:1211–1214
  72. Casele H, Haney E. Bruising in women undergoing thromboprophylaxis in pregnancy. Am J Obstet Gynecol. 2006;193:S81
  73. Matziolis G, Perka C, Disch A, et al. Effects of fondaparinux compared with dalteparin, enoxaparin and unfractionated heparin on human osteoblasts. Calcif Tissue Int. 2003;73:370–379
  74. Lagrange F, Brun JL, Vergnes MC, et al. Fondaparinux sodium does not cross the placental barrier: study using the in-vitro human dually perfused cotyledon model. Clin Pharmacokinet. 2002;41(suppl 2):47–49
  75. Dempfle CE. Minor transplacental passage of fondaparinux in vivo. N Engl J Med. 2004;350:1914–1915
  76. Mazzolai L, Hohlfeld P, Spertini F, et al. Fondaparinux is a safe alternative in case of heparin intolerance during pregnancy. Blood. 2006;108:1569–1570
  77. ACOG. Thromboembolism in Pregnancy. American College of Obstetrician and Gynecologists, 2000:1-9
  78. Coppage KH, Hinton AC, Moldenhauer J, et al. Maternal and perinatal outcome in women with a history of stroke. Am J Obstet Gynecol. 2004;190:1331–1334
  79. Ray JG, Chan WS. Deep vein thrombosis during pregnancy and the puerperium: a meta-analysis of the period of risk and the leg of presentation. Obstet Gynecol Surv. 1999;54:265–271
  80. Ansell J, Hirsh J, Poller L, et al. The pharmacology and management of the vitamin K antagonists: the Seventh ACCP Conference on Antithrombotic and Thrombolytic Therapy. Chest. 2004;126(suppl):204S–233S
  81. Stewart JA, Hamilton PJ, Murdoch AP. Thromboembolic disease associated with ovarian stimulation and assisted conception techniques. Hum Reprod. 1997;12:2167–2173
  82. Warkentin TE, Levine MN, Hirsh J, et al. Heparin-induced thrombocytopenia in patients treated with low-molecular-weight heparin or unfractionated heparin. N Engl J Med. 1995;332:1330–1335
  83. McCrae KR, Bussel JB, Mannucci PM, et al. Platelets: an update on diagnosis and management of thrombocytopenic disorders. Hematology (Am Soc Hematol Educ Program). 2001;282–305
  84. Horlocker TT. Low molecular weight heparin and neuraxial anesthesia. Thromb Res. 2001;101:141–154
  85. Baker WH, Mahler DK, Foldes MS, et al. Pneumatic compression devices for prophylaxis of deep venous thrombosis (DVT). Am Surg. 1986;52:371–373
  86. Orme ML, Lewis PJ, de Swiet M, et al. May mothers given warfarin breast-feed their infants?. Br Med J. 1977;1:1564–1565
  87. American Academy of Pediatrics Committee on Drugs. Transfer of drugs and other chemicals into human milk. Pediatrics. 2001;108:776–789
  88. World Health Organization Collaborative Study of Cardiovascular Disease and Steroid Hormone Contraception. Cardiovascular disease and use of oral and injectable progestogen-only contraceptives and combined injectable contraceptives (Results of an international, multicenter, case-control study). Contraception. 1998;57:315–324
  89. Kupferminc MJ, Eldor A, Steinman N, et al. Increased frequency of genetic thrombophilia in women with complications of pregnancy. N Engl J Med. 1999;340:9–13
  90. James A, Brancazio L, Ortel T. Thrombophilia in pregnancy: maternal and fetal implications. Curr Womens Health Rev. 2006;2:51–59
  91. Badaracco MA, Vessey MP. Recurrence of venous thromboembolic disease and use of oral contraceptives. Br Med J. 1974;1:215–217
  92. Tengborn L, Bergqvist D, Matzsch T, et al. Recurrent thromboembolism in pregnancy and puerperium. Is there a need for thromboprophylaxis? Am J Obstet Gynecol. 1989;160:90–94
  93. James AH, Brancazio LR, Ortel TL. Thrombosis, thrombophilia, and thromboprophylaxis in pregnancy. Clin Adv Hematol Oncol. 2005;3:187–197

PII: S0146-0005(07)00033-X

doi: 10.1053/j.semperi.2007.03.002

Seminars in Perinatology
Volume 31, Issue 3 , Pages 167-175 , June 2007

Article Tools