Heparin in human placental development and the prevention of placental complications of pregnancy

Fetal and Maternal Medicine Review

Volumn 21, Issue 3, 2010, Pages 185-203

  Drewlo, Sascha ^a,d   Walker, Melissa ^b   Mcleod, Anne ^c   Dodd, Jodie ^e   Kingdom, John ^a,b,d  

^a MOUNT SINAI HOSPITAL   (Canada)

^b MOUNT SINAI HOSPITAL   (Canada)

^c SUNNYBROOK RESEARCH INSTITUTE   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

^e UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLSALICYLIC ACID; DALTEPARIN; DEXTRAN; ENOXAPARIN; FIBROBLAST GROWTH FACTOR RECEPTOR 2; HEPARIN; LOW MOLECULAR WEIGHT HEPARIN; NADROPARIN; PHOSPHOLIPID ANTIBODY;

ANTICOAGULANT THERAPY; ARTICLE; DNA REPLICATION; DRUG ACTIVITY; DRUG EFFICACY; DRUG HALF LIFE; DRUG MECHANISM; DRUG SAFETY; DRUG STRUCTURE; FERTILIZATION IN VITRO; HUMAN; INTRAUTERINE GROWTH RETARDATION; MITOSIS; MOLECULAR WEIGHT; NONHUMAN; NULLIPARA; PARTIAL THROMBOPLASTIN TIME; PLACENTA DEVELOPMENT; PLACENTA DISORDER; PLACENTA FUNCTION; PLACENTA INSUFFICIENCY; PREECLAMPSIA; PREGNANCY; RANDOMIZED CONTROLLED TRIAL (TOPIC); RISK FACTOR; SOLUTIO PLACENTAE; SPONTANEOUS ABORTION; STILLBIRTH; SYSTEMATIC REVIEW (TOPIC); THROMBOPHILIA; VENOUS THROMBOEMBOLISM;

EID: 79251617533     PISSN: 09655395     EISSN: 14695065     Source Type: Journal    
DOI: 10.1017/S0965539510000070     Document Type: Article

References (87)

1. Blanco-Molina A, Trujillo-Santos J, Criado J, Lopez L, Lecumberri R, Gutierrez R, et al. Venous thromboembolism during pregnancy or postpartum: findings from the RIETE Registry. Thromb Haemost 2007;97:186-90.
2. Hanprasertpong T, Hanprasertpong J, Riabroi K. Cerebral venous sinus thrombosis in early pregnancy: an unusual presentation of primary antiphospholipid syndrome. J Obstet Gynaecol Res 2009;35:1125-128.
3. Yinon Y, Siu SC, Warshafsky C, Maxwell C, McLeod A, Colman JM, et al. Use of low molecular weight heparin in pregnant women with mechanical heart valves. Am J Cardiol 2009;104:1259-263.
4. Mehndiratta S, Suneja A, Gupta B, Bhatt S. Fetotoxicity of warfarin anticoagulation. Arch Gynecol Obstet 2010 Jan 29. (epub ahead of print)
5. Petitou M, Nancy-Portebois V, Dubreucq G, Motte V, Meuleman D, de Kort M, et al. From heparin to EP217609: the long way to a new pentasaccharide-based neutralisable anticoagulant with an unprecedented pharmacological profile. Thromb Haemost 2009;102:804-10.
6. Greer I, Hunt BJ. Low molecular weight heparin in pregnancy: current issues. Br J Haematol 2005;128:593-601.
7. Warkentin TE, Greinacher A. Heparin-induced thrombocytopenia: recognition, treatment, and prevention: the Seventh ACCP Conference on Antithrombotic and Thrombolytic Therapy. Chest 2004;126(3 Suppl): 311S-37S.
8. Carlin AJ, Farquharson RG, Quenby SM, Topping J, Fraser WD. Prospective observational study of bone mineral density during pregnancy: low molecular weight heparin versus control. Hum Reprod 2004;19:1211-214.
9. Backos M, Rai R, Thomas E, Murphy M, Dore C, Regan L. Bone density changes in pregnant women treated with heparin: a prospective, longitudinal study. Hum Reprod 1999;14:2876-880.
10. Rodger MA, Kahn SR, Cranney A, Hodsman A, Kovacs MJ, Clement AM, et al. Long-term dalteparin in pregnancy not associated with a decrease in bone mineral density: substudy of a randomized controlled trial. J Thromb Haemost 2007;5:1600-606.
11. Ekman-Ordeberg G, Akerud A, Dubicke A, Malmstrom A, Hellgren M. Does low molecular weight heparin shorten term labor? Acta Obstet Gynecol Scand 2010;89:147-50.
12. Linhardt RJ, Gunay NS. Production and chemical processing of low molecular weight heparins. Semin Thromb Hemost 1999;25 Suppl 3:5-16.
13. Sasisekharan R, Venkataraman G. Heparin and heparan sulfate: biosynthesis, structure and function. Curr Opin Chem Biol. 2000;4:626-31.
14. Hirsh J, Warkentin TE, Shaughnessy SG, Anand SS, Halperin JL, Raschke R, et al. Heparin and lowmolecular-weight heparin: mechanisms of action, pharmacokinetics, dosing, monitoring, efficacy, and safety. Chest 2001;119(1 Suppl): 64S-94S.
15. Collignon F, Frydman A, Caplain H, Ozoux ML, Le Roux Y, Bouthier J, et al. Comparison of the pharmacokinetic profiles of three low molecular mass heparins-dalteparin, enoxaparin and nadroparin-administered subcutaneously in healthy volunteers (doses for prevention of thromboembolism). Thromb Haemost 1995;73:630-40.
16. Horlocker TT, Wedel DJ, Rowlingson JC, Enneking FK, Kopp SL, Benzon HT, et al. Regional anaesthesia in the patient receiving antithrombotic or thrombolytic therapy: American Society of Regional Anesthesia and Pain Medicine Evidence-Based Guidelines (Third Edition). Reg Anesth Pain Med 2010;35:64-101.
17. Conti S, Guercini F, Iorio A. Low-molecular-weight heparin and cancer survival: review of the literature and pooled analysis of 1, 726 patients treated for at least three months. Pathophysiol Haemost Thromb. 2003;33:197-201.
18. Lazo-Langner A, Goss GD, Spaans JN, Rodger MA. The effect of low-molecular-weight heparin on cancer survival. A systematic review and meta-analysis of randomized trials. J Thromb Haemost 2007;5:729-37.
19. Nishioka J, Goodin S. Low-molecular-weight heparin in cancer-associated thrombosis: treatment, secondary prevention, and survival. J Oncol Pharm Pract 2007;13:85-97.
20. Casu B, Vlodavsky I, Sanderson RD. Non-anticoagulant heparins and inhibition of cancer. Pathophysiol Haemost Thromb 2008;36:195-203.
21. Mohammadi M, Olsen SK, Ibrahimi OA. Structural basis for fibroblast growth factor receptor activation. Cytokine Growth Factor Rev 2005;16:107-37.
22. Ilan N, Elkin M, Vlodavsky I. Regulation, function and clinical significance of heparanase in cancer metastasis and angiogenesis. Int J Biochem Cell Biol 2006;38:2018-39. (Pubitemid 44397619)
23. Azem F, Many A, Ben Ami I, Yovel I, Amit A, Lessing JB, et al. Increased rates of thrombophilia in women with repeated IVF failures. Hum Reprod 2004;19:368-70.
24. Qublan HS, Eid SS, Ababneh HA, Amarin ZO, Smadi AZ, Al-Khafaji FF, et al. Acquired and inherited thrombophilia: implication in recurrent IVF and embryo transfer failure. Hum Reprod 2006;21:2694-698.
25. Kaider BD, Price DE, Roussev RG, Coulam CB. Antiphospholipid antibody prevalence in patients with IVF failure. Am J Reprod Immunol 1996;35:388-93.
26. Geva E, Yaron Y, Lessing JB, Yovel I, Vardinon N, Burke M, et al. Circulating autoimmune antibodies may be responsible for implantation failure in in vitro fertilization. Fertil Steril 1994;62:802-806.
27. Birkenfeld A, Mukaida T, Minichiello L, Jackson M, Kase NG, Yemini M. Incidence of autoimmune antibodies in failed embryo transfer cycles. Am J Reprod Immunol 1994;31:65-68.
28. Coulam CB, Jeyendran RS, Fishel LA, Roussev R. Multiple thrombophilic gene mutations are risk factors for implantation failure. Reprod Biomed Online 2006;12:322-27.
29. Denis AL, Guido M, Adler RD, Bergh PA, Brenner C, Scott RT, Jr. Antiphospholipid antibodies and pregnancy rates and outcome in in vitro fertilization patients. Fertil Steril 1997;67:1084-90.
30. Simur A, Ozdemir S, Acar H, Colakoglu MC, Gorkemli H, Balci O, et al. Repeated in vitro fertilization failure and its relation with thrombophilia. Gynecol Obstet Invest 2009;67:109-12.
31. Martinelli I, Taioli E, Ragni G, Levi-Setti P, Passamonti SM, Battaglioli T, et al. Embryo implantation after assisted reproductive procedures and maternal thrombophilia. Haematologica 2003;88:789-93.
32. Nelson SM, Greer IA. The potential role of heparin in assisted conception. Hum Reprod Update 2008;14:623-45.
33. Chamley LW, Duncalf AM, Mitchell MD, Johnson PM. Action of anticardiolipin and antibodies to beta2-glycoprotein-I on trophoblast proliferation as a mechanism for fetal death. Lancet 1998;352:1037-38.
34. Di Simone N, Meroni PL, de Papa N, Raschi E, Caliandro D, De Carolis CS, et al. Antiphospholipid antibodies affect trophoblast gonadotropin secretion and invasiveness by binding directly and through adhered beta2-glycoprotein I. Arthritis Rheum 2000;43:140-50.
35. Girardi G, Redecha P, Salmon JE. Heparin prevents antiphospholipid antibody-induced fetal loss by inhibiting complement activation. Nat Med 2004;10:1222-226.
36. Qublan H, Amarin Z, Dabbas M, Farraj AE, Beni-Merei Z, Al-Akash H, et al. Low-molecular-weight heparin in the treatment of recurrent IVF-ET failure and thrombophilia: a prospective randomized placebo-controlled trial. Hum Fertil 2008;11:246-53.
37. Urman B, Ata B, Yakin K, Alatas C, Aksoy S, Mercan R, et al. Luteal phase empirical low molecular weight heparin administration in patients with failed ICSI embryo transfer cycles: a randomized openlabeled pilot trial. Hum Reprod 2009;24:1640-647.
38. Horne AW, Alexander CI. Recurrent miscarriage. J Fam Plann Reprod Health Care. 2005;31:103-107.
39. ACOG practice bulletin. Management of recurrent pregnancy loss. Number 24, February 2001. (Replaces Technical Bulletin Number 212, September 1995). American College of Obstetricians and Gynecologists. Int J Gynecol Obstet 2002;78:179-90.
40. Kaandorp S, Di Nisio M, Goddijn M, Middeldorp S. Aspirin or anticoagulants for treating recurrent miscarriage in women without antiphospholipid syndrome. Cochrane Database Syst Rev 2009: CD004734.
41. Rey E, Kahn SR, David M, Shrier I. Thrombophilic disorders and fetal loss: a meta-analysis. Lancet 2003;361:901-908.
42. Levine JS, Branch DW, Rauch J. The antiphospholipid syndrome. N Engl J Med 2002;346:752-63.
43. Empson M, Lassere M, Craig J, Scott J. Prevention of recurrent miscarriage for women with antiphospholipid antibody or lupus anticoagulant. Cochrane Database Syst Rev 2005: CD002859.
44. Laskin CA, Spitzer KA, Clark CA, Crowther MR, Ginsberg JS, Hawker GA, et al. Low molecular weight heparin and aspirin for recurrent pregnancy loss: results from the randomized, controlled HepASA Trial. J Rheumatol 2009;36:279-87.
45. Dolitzky M, Inbal A, Segal Y, Weiss A, Brenner B, Carp H. A randomized study of thromboprophylaxis in women with unexplained consecutive recurrent miscarriages. Fertil Steril 2006;86:362-66.
46. Kaandorp S, Goddijn M, Van der Post JA, Hutten BA, Verhoeve HR, Hamulyak K, et al. Aspirin and Aspirin Combined with Low-Molecular-Weight Heparin in Women with Unexplained Recurrent Miscarriage: a Randomized Controlled Multicenter Trial (ALIFE Study). Blood 2009;114: Abstract 488.
47. Hull MG, North K, Taylor H, Farrow A, Ford WC. Delayed conception and active and passive smoking. The Avon Longitudinal Study of Pregnancy and Childhood Study Team. Fertil Steril 2000;74:725-33.
48. Berthiller J, Sasco AJ. [Smoking (active or passive) in relation to fertility, medically assisted procreation and pregnancy]. J Gynecol Obstet Biol Reprod 2005;34 Spec No 1:3S47-54.
49. Eggert J, Theobald H, Engfeldt P. Effects of alcohol consumption on female fertility during an 18-year period. Fertil Steril 2004;81:379-83.
50. Clark P, Walker ID, Langhorne P, Crichton L, Thomson A, Greaves M, et al. SPIN: the Scottish Pregnancy Intervention Study: a multicentre randomised controlled trial of low molecular weight heparin and low dose aspirin in women with recurrent miscarriage. Blood 2010;115:4162-167.
51. Ball E, Robson SC, Ayis S, Lyall F, Bulmer JN. Early embryonic demise: no evidence of abnormal spiral artery transformation or trophoblast invasion. J Pathol 2006;208:528-34.
52. Smith GC, Wood AM. Recurrent first trimester spontaneous losses are associated with a family history of ischemic heart disease. Reprod Sci [Abstract]. 2010;17:288A.
53. Ferrazzi E, Bulfamante G, Mezzopane R, Barbera A, Ghidini A, Pardi G. Uterine Doppler velocimetry and placental hypoxic-ischaemic lesion in pregnancies with fetal intrauterine growth restriction. Placenta 1999;20:389-94.
54. Viero S, Chaddha V, Alkazaleh F, Simchen MJ, Malik A, Kelly E, et al. Prognostic value of placental ultrasound in pregnancies complicated by absent end-diastolic flow velocity in the umbilical arteries. Placenta 2004;25:735-41.
55. Toal M, Keating S, Machin G, Dodd J, Adamson SL, Windrim RC, et al. Determinants of adverse perinatal outcome in high-risk women with abnormal uterine artery Doppler images. Am J Obstet Gynecol 2008;198:330 e1-7.
56. Thrombophilia in Pregnancy Prophylaxis study (TIPPS). . 2009.
57. Abou-Nassar K, Kovacs MJ, Kahn SR, Wells P, Doucette S, Ramsay T, et al. The effect of dalteparin on coagulation activation during pregnancy in women with thrombophilia. A randomized trial. Thromb Haemost 2007;98:163-71.
58. Dodd M, Windrim, Kingdom J. Antithrombotic therapy for improving maternal or infant health outcomes in women considered at risk of placental dysfunction. Cochrane Database Syst Rev 2010;6: CD006780.
59. North RA, Ferrier C, Gamble G, Fairley KF, Kincaid-Smith P. Prevention of preeclampsia with heparin and antiplatelet drugs in women with renal disease. Aust N Z J Obstet Gynaecol 1995;35:357-62.
60. Mello G, Parretti E, Fatini C, Riviello C, Gensini F, Marchionni M, et al. Low-molecular-weight heparin lowers the recurrence rate of preeclampsia and restores the physiological vascular changes in angiotensin-converting enzyme DD women. Hypertension 2005;45:86-91.
61. Yu YH, Shen LY, Zhong M, Zhang Y, Su GD, Gao YF, et al. Effect of heparin on fetal growth restriction. Zhonghua Fu Chan Ke Za Zhi 2004;39:793-96.
62. Rey E, Garneau P, David M, Gauthier R, Leduc L, Michon N, et al. Dalteparin for the prevention of recurrence of placental-mediated complications of pregnancy in women without thrombophilia: a pilot randomized controlled trial. J Thromb Haemost 2009;7:58-64.
63. Toal M, Chaddha V, Windrim R, Kingdom J. Ultrasound detection of placental insufficiency in women with elevated second trimester serum alpha-fetoprotein or human chorionic gonadotropin. J Obstet Gynaecol Can 2008;30:198-206.
64. Proctor LK, Toal M, Keating S, Chitayat D, Okun N, Windrim RC, et al. Placental size and the prediction of severe early-onset intrauterine growth restriction in women with low pregnancyassociated plasma protein-A. Ultrasound Obstet Gynecol 2009;34:274-82.
65. Toal M, Chan C, Fallah S, Alkazaleh F, Chaddha V, Windrim RC, et al. Usefulness of a placental profile in high-risk pregnancies. Am J Obstet Gynecol 2007;196:363 e1-7.
66. Dugoff L, Hobbins JC, Malone FD, Vidaver J, Sullivan L, Canick JA, et al. Quad screen as a predictor of adverse pregnancy outcome. Obstet Gynecol 2005;106:260-67.
67. Pasupathy D, Dacey A, Cook E, Charnock-Jones DS, White IR, Smith GC. Study protocol. A prospective cohort study of unselected primiparous women: the pregnancy outcome prediction study. BMC Pregnancy Childbirth 2008;8:51.
68. Kaufman P. Vergleichend-anatomische und funktionelle Aspekte des Placenta-Baues. Funkt Biol Med 1983:71-79.
69. Cross JC, Nakano H, Natale DR, Simmons DG, Watson ED. Branching morphogenesis during development of placental villi. Differentiation 2006;74:393-401.
70. Huppertz B. IFPA Award in Placentology Lecture: Biology of the placental syncytiotrophoblast-myths and facts. Placenta 2010;31 Suppl: S75-81.
71. Aplin JD. Developmental cell biology of human villous trophoblast: current research problems. Int J Dev Biol 2010;54:323-29.
72. Burton GJ, Woods AW, Jauniaux E, Kingdom JC. Rheological and physiological consequences of conversion of the maternal spiral arteries for uteroplacental blood flow during human pregnancy. Placenta 2009;30:473-82.
73. Nevo O, Soleymanlou N, Wu Y, Xu J, Kingdom J, Many A, et al. Increased expression of sFlt-1 in in vivo and in vitro models of human placental hypoxia is mediated by HIF-1. Am J Physiol Regulatory Integrative Comp Physiol 2006;291: R1085-93.
74. Benirschke K, Kaufmann P. Pathology of the Human Placenta. 4th Edition ed. New York: Springer-Verlag; 2006;47-55.
75. Baczyk D, Drewlo S, Proctor L, Dunk C, Lye S, Kingdom J. Glial cell missing-1 transcription factor is required for the differentiation of the human trophoblast. Cell Death Differ 2009;16:719-27.
76. Baczyk D, Dunk C, Huppertz B, Maxwell C, Reister F, Giannoulias D, et al. Bi-potential behaviour of cytotrophoblasts in first trimester chorionic villi. Placenta 2006;27:367-74.
77. Facchinetti F, Marozio L, Frusca T, Grandone E, Venturini P, Tiscia GL, et al. Maternal thrombophilia and the risk of recurrence of preeclampsia. Am J Obstet Gynecol 2009;200:46 e1-5.
78. Gris JC, Lissalde-Lavigne G, Quere I, Dauzat M, Mares P. Prophylaxis and treatment of thrombophilia in pregnancy. Curr Opin Hematol 2006;13:376-81.
79. Sood R, Kalloway S, Mast AE, Hillard CJ, Weiler H. Fetomaternal cross talk in the placental vascular bed: control of coagulation by trophoblast cells. Blood 2006;107:3173-80.
80. Munoz EM, Linhardt RJ. Heparin-binding domains in vascular biology. Arterioscler Thromb Vasc Biol 2004;24:1549-557.
81. Drewlo S, Levytska K, Baczyk D, Sobel M, Kingdom J. Heparin elevates sFLT-1 secretion and impairs villous trophoblast physiology in a dose-dependent manner: Implications for the prevention of severe preeclampsia? Reprod Sci 2010;17(3 (Supplement)): 121A.
82. Tanaka S, Kunath T, Hadjantonakis AK, Nagy A, Rossant J. Promotion of trophoblast stem cell proliferation by FGF4. Science 1998;282:2072-75.
83. Bose P, Black S, Kadyrov M, Bartz C, Shlebak A, Regan L, et al. Adverse effects of lupus anticoagulant positive blood sera on placental viability can be prevented by heparin in vitro. Am J Obstet Gynecol 2004;191:2125-131.
84. Haimov-Kochman R, Friedmann Y, Prus D, Goldman-Wohl DS, Greenfield C, Anteby EY, et al. Localization of heparanase in normal and pathological human placenta. Mol Hum Reprod 2002;8:566-73.
85. Vlodavsky I, Ilan N, Nadir Y, Brenner B, Katz BZ, Naggi A, et al. Heparanase, heparin and the coagulation system in cancer progression. Thromb Res 2007;120 Suppl 2: S112-20.
86. Fux L, Ilan N, Sanderson RD, Vlodavsky I. Heparanase: busy at the cell surface. Trends Biochem Sci 2009;34:511-19.
87. Fox H. Morphological changes in the human placenta following fetal death. J Obstet Gynaecol Br Commonw 1968;75:839-43.