Anti-phospholipid antibodies and other immunological causes of recurrent foetal loss - A review of literature of various therapeutic protocols

American Journal of Reproductive Immunology

Volumn 62, Issue 1, 2009, Pages 9-24

  Shetty, Shrimati ^a   Ghosh, Kanjaksha ^a  

^a KEM HOSPITAL   (India)

Author keywords

Anti phospholipid antibodies; Foetal loss; Heparin; HLA G; Natural killer cells; T helper cells

Indexed keywords

ACETYLSALICYLIC ACID; ANTINUCLEAR ANTIBODY; B CELL ACTIVATING FACTOR; CYTOTOXIC ANTIBODY; DALTEPARIN; EFALIZUMAB; ENDOTHELIAL CELL ANTIBODY; ENOXAPARIN; HEPARIN; HLA G ANTIGEN; IDIOTYPIC ANTIBODY; IMMUNOGLOBULIN; INTERLEUKIN 6; LOW MOLECULAR WEIGHT HEPARIN; PHOSPHOLIPID ANTIBODY; PLACEBO; PREDNISOLONE; PROGESTERONE; RITUXIMAB; THYROGLOBULIN; THYROID ANTIBODY; THYROID PEROXIDASE ANTIBODY; TUMOR NECROSIS FACTOR ALPHA;

ALLOIMMUNITY; AUTOIMMUNITY; CLINICAL TRIAL; DRUG DOSE COMPARISON; DRUG DOSE INCREASE; DRUG EFFICACY; FETUS WASTAGE; HUMAN; IMMUNOMODULATION; IMMUNOPATHOLOGY; LIVE BIRTH; LOW DRUG DOSE; LYMPHOCYTE TRANSFER; MEDICAL LITERATURE; MIXED LYMPHOCYTE REACTION; MULTIPLE CYCLE TREATMENT; NATURAL KILLER CELL; NONHUMAN; OUTCOME ASSESSMENT; PLASMAPHERESIS; PREVALENCE; PRIORITY JOURNAL; RECURRENT ABORTION; REVIEW; RISK FACTOR; TH1 CELL; TH2 CELL; THROMBOSIS;

ABORTION, SPONTANEOUS; ANTI-INFLAMMATORY AGENTS; ANTIBODIES, ANTIPHOSPHOLIPID; ASPIRIN; CLINICAL TRIALS AS TOPIC; FEMALE; FIBRINOLYTIC AGENTS; HEPARIN, LOW-MOLECULAR-WEIGHT; HISTOCOMPATIBILITY ANTIGENS CLASS I; HLA ANTIGENS; HUMANS; IMMUNOGLOBULINS, INTRAVENOUS; KILLER CELLS, NATURAL; PREDNISOLONE; PREGNANCY; PREGNANCY COMPLICATIONS, HEMATOLOGIC; PROGESTERONE; PROGESTINS; RECURRENCE; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 67149092186     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/j.1600-0897.2009.00714.x     Document Type: Review

References (111)

1. Adelberg AM, Kuller JA: Thrombophilias and recurrent miscarriage. Obstet Gynecol Surv 2002; 57: 703-709.
2. Kist WJ, Janssen NG, Kalk JJ, Hague WM, Dekker GA, de Vries JI: Thrombophilias and adverse pregnancy outcome -a confounded problem! Thromb Haemost 2008; 99: 77-85.
3. Tharapel AT, Tharapel SA, Bannerman RM: Recurrent pregnancy losses and parental chromosome abnormalities: A review. Br J Obstet Gynaecol 1985; 92: 899-914.
4. Simpson JL: Causes of fetal wastage. Clin Obstet Gynecol 2007; 50: 10-30.
5. Di Simone N, Raschi E, Testoni C, Castellani R, D'Asta M, Shi T, Krilis SA, Caruso A, Meroni PL: Pathogenic role of anti-ß2-glycoprotein I antibodies in antiphospholipid associated fetal loss: Characterisation of ß2-glycoprotein I binding to trophoblast cells and functional effects of anti-ß2-glycoprotein I antibodies in vitro. Ann Rheum Dis 2005; 64: 462-467.
6. Pierangeli SS, Chen PP, Raschi E, Scurati S, Grossi C, Borghi MO, Palomo I, Harris EN, Meroni PL: Antiphospholipid antibodies and the antiphospholipid syndrome: Pathogenic mechanisms. Semin Thromb Hemost 2008; 34: 236-250.
7. Bahar AM, Kwak JYH, Beer AE, Kim JH, Nelson LA, Beaman KD, Gilman Sachs A: Antibodies to phospholipids and nuclear antigens in non-pregnant women with unexplained spontaneous recurrent abortions. J Reprod Immunol 1993; 24: 213-222.
8. Kwak JY, Gilman-Sachs A, Beaman KD, Beer AE: Autoantibodies in women with primary recurrent spontaneous abortion of unknown aetiology. J Reprod Immunol 1992; 22: 15-31.
9. Vinatier D, Dufour P, Cosson M, Houpeau JL: Antiphospholipid syndrome and recurrent miscarriages. Eur J Obstet Gynecol Reprod Biol 2001; 96: 37-50.
10. Rand JH, Wu XX, Andree HA, Ross JB, Rusinova E, Gascon-Lema MG, Calandri C, Harpel PC: Antiphospholipid antibodies accelerate plasma coagulation by inhibiting annexin-V binding to phospholipids: A "lupus procoagulant"phenomenon. Blood 1998; 92: 1652-1660.
11. Bevers EM, Janssen MP, Willems GM, Zwaal RF: No evidence for enhanced thrombin formation through displacement of annexin V by antiphospholipid antibodies. Thromb Haemost 2000; 83: 792-794.
12. Belizna C, Lartigue A, Favre J, Gilbert D, Tron F, Lévesque H, Thuillez C, Richard V: Antiphospholipid antibodies induce vascular functional changes in mice: A mechanism of vascular lesions in antiphospholipid syndrome? Lupus 2008; 17: 185-194.
13. Sebire NJ, Fox H, Backos M, Rai R, Paterson C, Regan L: Defective endovascular trophoblast invasion in primary antiphospholipid antibody syndrome-associated early pregnancy failure. Hum Reprod 2002; 17: 1067-1071.
14. Quenby S, Mountfield S, Cartwright JE, Whitley GS, Chamley L, Vince G: Antiphospholipid antibodies prevent extravillous trophoblast differentiation. Fertil Steril 2005; 83: 691-698.
15. Carp HJ: Antiphospholipid syndrome in pregnancy. Curr Opin Obstet Gynecol 2004; 16: 129-135.
16. Carreras LO, Machin SJ, Deman R: Arterial thrombosis, intrauterine death and lupus anticoagulant detection of immunoglobulin interfering with prostacyclin production. Lancet 1981; 1: 244.
17. Chamley LW, Duncalf AM, Mitchell MD, Johnson PM: Action of anticardiolipin antibodies to beta-2 glycoprotein-1 on trophoblast proliferation as a mechanism for fetal death. Lancet 1998; 352: 1037-1038.
18. Weiler H: Tracing the molecular pathogenesis of antiphospholipid syndrome. J Clin Invest 2008; 118: 3276-3278.
19. Di Simone N, Luigi MP, Marco D, Fiorella DN, Silvia D, Clara DM, Alessandro C: Pregnancies complicated with antiphospholipid syndrome: the pathogenic mechanism of antiphospholipid antibodies: A review of the literature. Ann N Y Acad Sci 2007; 1108: 505-514.
20. Todorova M, Baleva M: Some recent insights into the prothrombogenic mechanisms of antiphospholipid antibodies. Curr Med Chem 2007; 14: 811-826.
21. Oliver-Miñarro D, Sanchez-Ramón S, Rodriguez-Mahou M, Alvarez S, Fernández-Cruz E: Isolated type 5 antimitochondrial autoantibodies are associated with a history of thrombocytopenia and fetal loss. Fertil Steril 2007; 87: 976 e17-18.
22. Bussen SS, Steck T: Thyroid antibodies and their relation to antithrombin antibodies, anticardiolipin antibodies and lupus anticoagulant in women with recurrent spontaneous abortions (antithyroid, anticardiolipin and antithrombin autoantibodies and lupus anticoagulant in habitual aborters. Eur J Obstet Gynecol Reprod Biol 1997; 74: 139-143.
23. Stricker R, Echenard M, Eberhart R, Chevailler MC, Perez V, Quinn FA, Stricker R: Evaluation of maternal thyroid function during pregnancy: the importance of using gestational age-specific reference intervals. Eur J Endocrinol 2007; 157: 509-514.
24. Wilson R, McKillop JH, MacLean M, Walker JJ, Fraser WD, Gray C, Dryburgh F, Thomson JA: Thyroid function tests are rarely abnormal in patients with severe hyperemesis gravidarum. Clin Endocrinol (Oxf) 1992; 37: 331-334.
25. Pijnenborg R, Robertson WB, Brosens I, Dixon G: Trophoblast invasion and the establishment of haemochorial placentation in man and laboratory animals. Placenta 1981; 2: 71-91.
26. Roussev RG, Stern JJ, Kaider BD: Anti-endothelial cell antibodies: another cause for pregnancy loss? Am J Reprod Immunol 1998; 39: 89-95.
27. Wegmann TG, Lin H, Guilbert L, Mosmann TR: Bidirectional cytokine interactions in the maternal-fetal relationship: Is successful pregnancy a TH2 phenomenon? Immunol Today 1993; 14: 353-356.
28. Pandey MK, Rani R, Agrawal S: An update in recurrent spontaneous abortion. Arch Gynecol Obstet 2005; 272: 95-108.
29. McIntyre JA, Coulam CB, Faulk WP: Recurrent spontaneous abortion. Am J Reprod Immunol 1989; 21: 100-104.
30. Tamura M, Takakuwa K, Arakawa M, Yasuda M, Kazama Y, Tanaka K: Relationship between MLR blocking antibodies and the outcome of the third pregnancy in patients with two consecutive spontaneous abortions. J Perinat Med 1998; 26: 49-53.
31. King A, Hiby SE, Verma S, Burrows T, Gardner L, Loke YW: Uterine NK cells and trophoblast HLA class I molecules. Am J Reprod Immunol 1997; 37: 459-462.
32. Odum N, Ledbetter JA, Martin P, Geraghty D, Tsu T, Hansen JA, Gladstone P: Homotypic aggregation of human cell lines by HLA class II-, class Ia- and HLA-G-specific monoclonal antibodies. Eur J Immunol 1991; 21: 2121-2131.
33. Le Bouteiller P: Major breakthrougO in the HLA-G debate: occurrence of pregnancy in human depends on the HLA-G status of preimplantation embryos. Eur J Immunol 2002; 32: 309-310.
34. Le Bouteiller P: HLA-G En the human placenta: expression and potential functions. Biochem Soc Trans 2000; 28: 208-212.
35. Karhukorpi J, Laitinen T, Tiilikainen AS: HLA-G polymorphism in Finnish couples with recurrent spontaneous miscarriage. Br J Obstet Gynaecol 1997; 104: 1212-1214.
36. Pénzes M, Rajczy K, Gyódi E, Réti M, Fehér E, Petrányi G: HLA-G gene polymorphism in the normal population and in recurrent spontaneous abortion in Hungary. Transplant Proc 1999; 31: 1832-1833.
37. van der Ven K, Pfeiffer K, Skrablin S: HLA-G polymorphisms and molecule function-questions and more questions-a review. Placenta 2000; 21 (Suppl. A): S86--S92.
38. Aldrich CL, Stephenson MD, Karrison T, Odem RR, Branch DW, Scott JR, Schreiber JR, Ober C: HLA-G genotypes and pregnancy outcome in couples with unexplained recurrent miscarriage. Mol Hum Reprod 2001; 7: 1167-1172.
39. Pfeiffer KA, Fimmers R, Engels G, van der Ven H, van der Ven K: The HLA-G genotype is potentially associated with idiopathic recurrent spontaneous abortion. Mol Hum Reprod 2001; 7: 373-378.
40. Aoki K, Kajiura S, Matsumoto Y, Ogasawara M, Okada S, Yagami Y, Gleicher N: Preconceptional natural-killer-cell activity as a predictor of miscarriage. Lancet 1995; 345: 1340-1342.
41. Kwak JY, Beaman KD, Gilman-Sachs A, Ruiz JE, Schewitz D, Beer AE: Up-regulated expression of CD56+, CD56+/CD16+, and CD19+ cells in peripheral blood lymphocytes in pregnant women with recurrent pregnancy losses. Am J Reprod Immunol 1995; 34: 93-99.
42. Emmer PM, Nelen WL, Steegers EA, Hendriks JC, Veerhoek M, Joosten I: Peripheral natural killer cytotoxicity and CD56(pos)CD16(pos) cells increase during early pregnancy in women with a history of recurrent spontaneous abortion. Hum Reprod 2000; 15: 1163-1169.
43. Coulam CB, Beaman KD: Reciprocal alteration in circulating TJ6+ CD19+ and TJ6+ CD56+ leukocytes in early pregnancy predicts success or miscarriage. Am J Reprod Immunol 1995; 34: 219-224.
44. Higuchi K, Aoki K, Kimbara T, Hosoi N, Yamamoto T, Okada H: Suppression of natural killer cell activity by monocytes following immunotherapy for recurrent spontaneous aborters. Am J Reprod Immunol 1995; 33: 221-227.
45. Yamada H, Kato EH, Kobashi G, Ebina Y, Shimada S, Morikawa M, Sakuragi N, Fujimoto S: High NK cell activity in early pregnancy correlates with subsequent abortion with normal chromosomes in women with recurrent abortion. Am J Reprod Immunol 2001; 46: 132-136.
46. Yamamoto T, Takahashi Y, Kase N, Mori H: Role of decidual natural killer (NK) cells in patients with missed abortion: Differences between cases with normal and abnormal chromosome. Clin Exp Immunol 1999; 116: 449-452.
47. Yamamoto T, Takahashi Y, Kase N, Mori H: Decidual natural killer cells in recurrent spontaneous abortion with normal chromosomal content. Am J Reprod Immunol 1999; 41: 337-342.
48. Quack KC, Vassiliadou N, Pudney J, Anderson DJ, Hill JA: Leukocyte activation in the decidua of chromosomally normal and abnormal fetuses from women with recurrent abortion. Hum Reprod 2001; 16: 949-955.
49. Vassiliadou N, Bulmer JN: Functional studies of human decidua in spontaneous early pregnancy loss: Effect of soluble factors and purified CD56+ lymphocytes on killing of natural killer- and lymphokine-activated killer-sensitive targets. Biol Reprod 1998; 58: 982-987.
50. Lachapelle MH, Miron P, Hemmings R, Roy DC: Endometrial T, B, and NK cells in patients with recurrent spontaneous abortion. Altered profile and pregnancy outcome. J Immunol 1996; 156: 4027-4034.
51. Raghupathy R, Kalinka J: Cytokine imbalance in pregnancy complications and its modulation. Front Biosci 2008; 13: 985-994.
52. Emmer PM, Steegers EA, Kerstens HM, Bulten J, Nelen WL, Boer K, Joosten I: Altered phenotype of HLA-G expressing trophoblast and decidual natural killer cells in pathological pregnancies. Hum Reprod 2002; 17: 1072-1080.
53. Wegmann TG, Lin H, Guilbert L, Mosmann TR: Bidirectional cytokine interactions in the maternal-fetal relationship: Is successful pregnancy a TH2 phenomenon? Immunol Today 1993; 14: 353-356.
54. Shiu HM, Schottenfeld D, McLean B, Fortner JG: Adverse effect of pregnancy in melanoma. Cancer 1976; 37: 181-187.
55. Lichtenstein MR: Tuberculin reaction in tuberclosis during pregnancy. Am Rev Tuberc Pulm Dis 1942; 48: 89-93.
56. Dresser DE: The potentiating effect of pregnancy on humoral immune responses of mice. J Reprod Immunol 1991; 20: 253-266.
57. Piccinni MP, Beloni L, Livi C, Maggi E, Scarselli G, Romagnani S: Defective production of both leukemia inhibitory factor and type 2 T-helper cytokines by decidual T cells in unexplained recurrent abortions. Nat Med 1998; 4: 1020-1024.
58. Lim KJ, Odukoya OA, Ajjan RA, Li TC, Weetman AP, Cooke ID: The role of T-helper cytokines in human reproduction. Fertil Steril 2000; 73: 136-142.
59. Laird SM, Tuckerman EM, Cork BA, Linjawi S, Blakemore AI, Li TC: A review of immune cells and molecules in women with recurrent miscarriage. Hum Reprod Update 2003; 9: 163-174.
60. Elder MG, de Swiet M, Robertson A, Elder MA, Flloyd E, Hawkins DF: Low-dose aspirin in pregnancy. Lancet 1988; 1: 410.
61. Lubbe WF, Butler WS, Palmer SJ, Liggins GC: Fetal survival after prednisone suppression of maternal lupus-anticoagulant. Lancet 1983; 1: 1361-1363.
62. Scott JR, Branch DW, Kochenour NK, Ward K: Intravenous immunoglobulin treatment of pregnant patients with recurrent pregnancy loss caused by antiphospholipid antibodies and Rh immunization. Am J Obstet Gynecol 1988; 159: 1055-1056.
63. Frampton G, Cameron JS, Thom M, Jones S, Raftery M: Successful removal of anti-phospholipid antibody during pregnancy using plasma exchange and low-dose prednisolone. Lancet 1987; 2: 1023-1024.
64. Noble LS, Kutteh WH, Lashey N, Franklin RD, Herrada J: Antiphospholipid antibodies associated with recurrent pregnancy loss: Prospective, multicenter, controlled pilot study comparing treatment with low-molecular-weight heparin versus unfractionated heparin. Fertil Steril 2005; 83: 684-690.
65. Weitz JL: Low molecular weight heparins. N Engl J Med 1997; 337: 688-698.
66. Bazzan M, Donvito V: Low-molecular-weight heparin during pregnancy. Thromb Res 2001; 101: 175-186.
67. Empson M, Lassere M, Craig JC, Scott JR: Recurrent pregnancy loss with antiphospholipid antibody: A systematic review of therapeutic trials. Obstet Gynecol 2002; 99: 135-144.
68. Di Simone N, Caliandro D, Castellani R, Ferrazzani S, De Carolis S, Caruso A: Low-molecular weight heparin restores in-vitro trophoblast invasiveness and differentiation in presence of immunoglobulin G fractions obtained from patients with antiphospholipid syndrome. Hum Reprod 1999; 14: 489-495.
69. Bose P, Black S, Kadyrov M, Bartz C, Shlebak A, Regan L, Huppertz B: Adverse effects of lupus anticoagulant positive blood sera on placental viability can be prevented by heparin in vitro. Am J Obstet Gynecol 2004; 191: 2125-2131.
70. Girardi G: GuAlty as charged: all available evidence implicates compliment's role in fetal demise. Am J Reprod Immunol 2008; 59: 183-192.
71. Shamonki JM, Salmon JE, Hyjek E, Baergen RN: Excessive complement activation is associated with placental injury in patients with antiphospholipid antibodies. Am J Obstet Gynecol 2007; 196: 167 e1-5.
72. David AClark, Gerard Chaouat, Petra CArck, Hans WilliMittruecker, Gary ALevy: CCtting edge: cytokine-dependent abortion in CBA×DBA/2 mice is mediated by the procoagulant fgl2 prothombinase. J Immunol 1998; 160: 545-549.
73. Franklin RD, kutteh WH: Effects of unfractionated and low molecular weight heparin on antiphospholipid binding in vitro. Obstet Gynaecol 2003; 101: 455-462.
74. Rai R, Cohen H, Dave M, Regan L: Randomised controlled trial of aspirin and aspirin plus heparin in pregnant women with recurrent miscarriage associated with phospholipid antibodies (or antiphospholipid antibodies). BMJ 1997; 314: 253-257.
75. Kutteh WH: Antiphospholipid antibody-associated recurrent pregnancy loss: Treatment with heparin and low-dose aspirin is superior to low-dose aspirin alone. Am J Obstet Gynecol 1996; 174: 1584-1588.
76. Kutteh WH, Ermel LD: A clinical trial for the treatment of antiphospholipid antibody-associated recurrent pregnancy loss with lower dose heparin and aspirin. Am J Reprod Immunol 1996; 35: 402-407.
77. Rosove MH, Tabsh K, Wasserstrum N, Howard P, Hahn BH, Kalunian KC: Heparin therapy for pregnant women with lupus anticoagulant or anticardiolipin antibodies. Obstet Gynecol 1990; 75: 630-634.
78. Granger KA, Farquharson RG: Obstetric outcome in antiphospholipid syndrome. Lupus 1997; 6: 509-513.
79. Triolo G, Ferrante A, Ciccia F, Accardo-Palumbo A, Perino A, Castelli A, Giarratano A, Licata G: Randomized study of subcutaneous low molecular weight heparin plus aspirin versus intravenous immunoglobulin in the treatment of recurrent fetal loss associated with antiphospholipid antibodies. Arthritis Rheum 2003; 48: 728-731.
80. Backos M, Rai R, Baxter N, Chilcott IT, Cohen H, Regan L: Pregnancy complications in women with recurrent miscarriage associated with antiphospholipid antibodies treated with low dose aspirin and heparin. Br J Obstet Gynaecol 1999; 106: 102-107.
81. Cowchock FS, Reece EA, Balaban D, Branch DW, Plouffe L: Repeated fetal losses associated with antiphospholipid antibodies: A collaborative randomized trial comparing prednisone with low-dose heparin treatment. Am J Obstet Gynecol 1992; 166: 1318-1323.
82. Farquharson RG, Quenby S, Greaves M: Antiphospholipid syndrome in pregnancy: A randomized, controlled trial of treatment. Obstet Gynecol 2002; 100: 408-413.
83. Ruiz JE, Kwak JY, Baum L, Gilman-sachs A, Beaman KD, Kim YB, Beer AE: Effects of intravenous immunoglobulin G on natural killer cell cytotoxicity in vitro in women with recurrent spontaneous abortion. J Reprod Immunol 1996; 31: 125-141.
84. Kwak JY, Kwak FM, Ainbinder SW, Ruiz AM, Beer AE: Elevated peripheral blood natural killer cells are effectively suppressed by immunoglobulin G infusions in women with recurrent spontaneous abortion. Am J Reprod Immunol 1996; 35: 363-369.
85. Morikawa M, Yamada H, Kato EH, Shimada S, Kishi T, Yamada T, Kobashi G, Fujimoto S: Massive intravenous immunoglobulin treatment in women with four or more recurrent spontaneous abortions of unexplained etiology: down-regulation of NK cell activity and subsets. Am J Reprod Immunol 2001; 46: 399-404.
86. Aoki K: Abstracts of contributors'individual data submitted to the worldwide prospective observation study on immunotherapy for treatment of recurrent spontaneous abortion. Am J Reprod Immunol 1994; 32: 268.
87. Sewell WA, Jolles S: Immunomodulatory action of intravenous immunoglobulin. Immunology 2002; 107: 387-393.
88. Wright GJ, Cherwinski H, Foster-Cuevas M, Brooke G, Puklavec MJ, Bigler M, Song Y, Jenmalm M, Gorman D, McClanahan T, Liu MR, Brown MH, Sedgwick JD, Phillips JH, Barclay AN: Characterization of the CD200 receptor family in mice and humans and their interactions with CD200. J Immunol 2003; 171: 3034-3306.
89. Aluvihare VR, Kallikourdis M, Betz AG: Regulatory T cells mediate maternal tolerance to the fetus. Nat Immunol 2004; 5: 266-271.
90. Yamada H, Morikawa M, Furuta I, Kato EH, Shimada S, Iwabuchi K, Minakami H: Intravenous immunoglobulin treatment in women with recurrent abortions: Increased cytokine levels and reduced Th1/Th2 lymphocyte ratio in peripheral blood. Am J Reprod Immunol 2003; 49: 84-89.
91. Laskin CA, Bombardier C, Hannah ME, Mandel FP, Ritchie JW, Farewell V, Farine D, Spitzer K, Fielding L, Soloninka CA, Yeung M: Prednisone and aspirin in women with autoantibodies and unexplained recurrent fetal loss. N Engl J Med 1997; 337: 148-153.
92. Daya S, Gunby J, Clark DA: Intravenous immunoglobulin therapy for recurrent spontaneous abortion: A meta-analysis. Am J Reprod Immunol 1998; 39: 69-76.
93. Daya S, Gunby J, Porter F, Scott J, Clark DA: Critical analysis of intravenous immunoglobulin therapy for recurrent miscarriage. Hum Reprod Update 1999; 5: 475-482.
94. Christiansen OB, Pedersen B, Rosgaard A, Husth M: A randomized, double-blind, placebo-controlled trial of intravenous immunoglobulin in the prevention of recurrent miscarriage: Evidence for a therapeutic effect in women with secondary recurrent miscarriage. Hum Reprod 2002; 17: 809-816.
95. Hutton B, Sharma R, Fergusson D, Tinmouth A, Hebert P, Jamieson J, Walker M: Use of intravenous immunoglobulin for treatment of recurrent miscarriage: A systematic review. BJOG 2007; 114: 134-142.
96. Silver RK, MacGregor SN, Sholl JS, Hobart JM, Neerhof MG, Ragin A: Comparative trial of prednisone plus aspirin versus aspirin alone in the treatment of anticardiolipin antibody-positive obstetric patients. Am J Obstet Gynecol 1993; 169: 1411-1417.
97. Branch DW, Peaceman AM, Druzin M, Silver RK, El-Sayed Y, Silver RM, Esplin MS, Spinnato J, Harger J: A multicenter, placebo-controlled pilot study of intravenous immune globulin treatment of antiphospholipid syndrome during pregnancy. The Pregnancy Loss Study Group. Am J Obstet Gynecol 2000; 182: 122-127.
98. Hasegawa I, Takakuwa K, Goto S, Yamada K, Sekizuka N, Kanazawa K, Tanaka K: Effectiveness of prednisolone/aspirin therapy for recurrent aborters with antiphospholipid antibody. Hum Reprod 1992; 7: 203-207.
99. Vaquero E, Lazzarin N, Valensise H, Menghini S, Di Pierro G, Cesa F, Romanini C: Pregnancy outcome in recurrent spontaneous abortion associated with antiphospholipid antibodies: A comparative study of intravenous immunoglobulin versus prednisone plus low-dose aspirin. Am J Reprod Immunol 2001; 45: 174-179.
100. Stephenson MD, Dreher K, Houlihan E, Wu V: Prevention of unexplained recurrent spontaneous abortion using intravenous immunoglobulin: A prospective, randomized, double-blinded, placebo-controlled trial. Am J Reprod Immunol 1998; 39: 82-88.
101. Coulam CB, Krysa L, Stern JJ, Bustillo M: Intravenous immunoglobulin for treatment of recurrent pregnancy loss. Am J Reprod Immunol 1995; 34: 333-337.
102. Smith JW, WeinsteAn R: Therapeutic apheresis: a summary of current indication categories endorsed by the AABB and the American Society of Apheresis. Transfusion 2003; 43: 820-822.
103. Frampton G, Cameron JS, Thom M, Jones S, Raftery M: Successful removal of anti-phospholipid antibody during pregnancy using plasma exchange and low-dose prednisolone. Lancet 1987; 31: 1023-1024.
104. Fulcher D, Stewart G, Exner T, Trudinger B, Jeremy R: Plasma exchange and the anticardiolipin syndrome in pregnancy. Lancet 1989; 2: 171.
105. El-Haieg DO, Zanati MF, El-Foual FM: Plasmapheresis and pregnancy outcome in patients with antiphospholipid syndrome. Int J Gynecol Obstet 2007; 99: 236-241.
106. Daya S, Gunby J: The effectiveness of allogeneic leukocyte immunization in unexplained primary recurrent spontaneous abortion. Am J Reprod Immunol 1994; 32: 294-302.
107. Pandey MK, Thakur S, Agrawal S: Lymphocyte immunotherapy and its probable mechanism in the maintenance of pregnancy in women with recurrent spontaneous abortion. Arch Gynecol Obstet 2004; 269: 161-172.
108. Gatenby PA, Cameron K, Simes RJ, Adelstein S, Bennett MJ, Jansen RP, Shearman RP, Stewart GJ, Whittle M, Doran TJ: Treatment of recurrent spontaneous abortion by immunization with paternal lymphocytes: Results of a controlled trial. Am J Reprod Immunol 1993; 29: 88-94.
109. Di Renzo GC, Mattei A, Gojnic M, Gerli S: Progesterone and pregnancy. Curr Opin Obstet Gynecol 2005; 17: 598-600.
110. Choi BC, Polgar K, Xiao L, Hill JA: Progesterone inhibits in vitro embryotoxic Th 1 cytokine production of trophoblast in women with recurrent pregnancy loss. Hum Reprod 2000; 15 (Suppl. L): 46-59.
111. Siiteri PK, Febres F, Clemens LE, Chang RJ, Gondos B, Stites D: Progesterone and maintenance of pregnancy: Is progesterone nature's immunosuppressant? Ann N Y Acad Sci 1977; 286: 384-397.