Evaluation and management of recurrent early pregnancy loss

Clinical Obstetrics and Gynecology

Volumn 50, Issue 1, 2007, Pages 132-145

  Stephenson, Mary ^a,b   Kutteh, William ^c  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF CHICAGO MEDICAL CENTER   (United States)

^c UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

Antiphospholipid syndrome; Cytogenetic analysis; Inherited thrombophilias; Recurrent miscarriage; Recurrent pregnancy loss; Translocations

Indexed keywords

ACETYLSALICYLIC ACID; ANTIBIOTIC AGENT; ANTICOAGULANT AGENT; BLOOD CLOTTING FACTOR 5 LEIDEN; CD56 ANTIGEN; CLOMIFENE CITRATE; CYANOCOBALAMIN; DOPAMINE RECEPTOR STIMULATING AGENT; FOLIC ACID; HEPARIN; HLA DQ ANTIGEN; IMMUNOGLOBULIN; INSULIN SENSITIZING AGENT; LOW MOLECULAR WEIGHT HEPARIN; METHYLENETETRAHYDROFOLATE REDUCTASE (NADPH2); PROGESTERONE; PYRIDOXINE; STEROID; THYROGLOBULIN ANTIBODY; THYROID ANTIBODY; THYROTROPIN; VITRONECTIN RECEPTOR;

ALCOHOL CONSUMPTION; ANTIBIOTIC THERAPY; ANTIPHOSPHOLIPID SYNDROME; ARTICLE; CHLAMYDIA; CHROMOSOME 13; CHROMOSOME 15; CHROMOSOME 16; CHROMOSOME 21; CHROMOSOME 22; CHROMOSOME REARRANGEMENT; CHROMOSOME TRANSLOCATION; CLINICAL EFFECTIVENESS; CLINICAL TRIAL; DISEASE ASSOCIATION; DISEASE PREDISPOSITION; ENDOCRINE SYSTEM; ENDOMETRIAL DISEASE; ENVIRONMENTAL EXPOSURE; FERTILIZATION IN VITRO; FETUS DISEASE; FIRST TRIMESTER PREGNANCY; GENE EXPRESSION REGULATION; GENETIC COUNSELING; GENETIC PREDISPOSITION; GESTATIONAL AGE; GROUPS BY AGE; HEREDITY; HORMONE DETERMINATION; HUMAN; HYPERHOMOCYSTEINEMIA; HYPERPROLACTINEMIA; HYPOTHALAMUS HYPOPHYSIS SYSTEM; IMMUNOPATHOLOGY; IMMUNOTHERAPY; LOW DRUG DOSE; LUTEAL INSUFFICIENCY; MATERNAL AGE; MATERNAL DISEASE; MONONUCLEAR CELL; MONOSOMY X; MYCOPLASMA HOMINIS; NATURAL KILLER CELL; OUTCOME ASSESSMENT; OVARY POLYCYSTIC DISEASE; POLYPLOIDY; POPULATION RESEARCH; PREGNANCY OUTCOME; PRENATAL DIAGNOSIS; RISK ASSESSMENT; SMOKING; SPONTANEOUS ABORTION; THROMBOPHILIA; TREATMENT INDICATION; TRISOMY; UREAPLASMA UREALYTICUM; UTERINE CERVICITIS; UTERUS BICORNIS; VAGINITIS;

ABORTION, HABITUAL; COUNSELING; CYTOGENETIC ANALYSIS; FEMALE; HUMANS; PREGNANCY; PREGNANCY OUTCOME; PREGNANCY TRIMESTER, FIRST; PREIMPLANTATION DIAGNOSIS; RISK ASSESSMENT; RISK FACTORS; SURROGATE MOTHERS;

EID: 33847167427     PISSN: 00099201     EISSN: None     Source Type: Journal    
DOI: 10.1097/GRF.0b013e31802f1c28     Document Type: Article

References (82)

1. Edmonds DK, Lindsay KS, Miller JF, et al. Early embryonic mortality in women. Fertil Steril. 1982;38:447-453.
2. Wilcox AJ, Weinberg CR, O'Connor JF, et al. Incidence of early loss of pregnancy. N Engl J Med. 1988;319:189-194.
3. Jacobs PA, Hassold T. Chromosome abnormalities: origin and etiology in abortions and livebirths. In: Vogel F, Sperling K, eds. Human Genetics. Berlin: Springer-Verlag; 1987:233-244.
4. Roman E. Fetal loss rates and their relation to pregnancy order. J Epidemiol Community Health. 1984;38:29-35.
5. Stephenson MD. Frequency of factors associated with habitual abortion in 197 couples. Fertil Steril. 1996;66:24-29.
6. Stray-Pedersen B, Stray-Pedersen S. Etiologic factors and subsequent reproductive performance in 195 couples with a prior history of habitual abortion. Am J Obstet Gynecol. 1984;148:140-146.
7. Carson SA, Branch DW. Management of recurrent early pregnancy loss. ACOG Practice Bulletin. 2001;24:1-12.
8. Stephenson MD, Awartani KA, Robinson WP. Cytogenetic analysis of miscarriages from couples with recurrent miscarriage: a case-control study. Hum Reprod. 2002;17:446-451.
9. Ness RB, Grisso JA, Hirschinger N, et al. Cocaine and tobacco use and the risk of spontaneous abortion. N Engl J Med. 1999;340:333-339.
10. Kline J, Stein ZA, Susser M, et al. Smoking: a risk factor for spontaneous abortion. N Engl J Med. 1977;297:793-796.
11. Venners SA, Wang X, Chen C, et al. Paternal smoking and pregnancy loss: a prospective study using a biomarker of pregnancy. Am J Epidemiol. 2004;159:993-1001.
12. Rasch V. Cigarette, alcohol, and caffeine consumption: risk factors for spontaneous abortion. Acta Obstet Gynecol Scand. 2003;82:182-188.
13. Fishel SB, Edwards RG, Evans CJ. Human chorionic gonadotropin secreted by preimplantation embryos cultured in vitro. Science. 1984;223:816-818.
14. Hassold T, Chiu D. Maternal agespecific rates of numerical chromosome abnormalities with special reference to trisomy. Hum Genet. 1985;70:11-17.
15. Regan L, Braude PR, Trembath PL. Influence of past reproductive performance on risk of spontaneous abortion. BMJ. 1989;299:541-545.
16. Ohno M, Maeda T, Matsunobu A. A cytogenetic study of spontaneous abortions with direct analysis of chorionic villi. Obstet Gynecol. 1991;77:394-398.
17. Simpson JL. Incidence and timing of pregnancy losses: relevance to evaluating safety of early prenatal diagnosis. Am J Med Genet. 1990;35:165-173.
18. Warburton D, Kline J, Stein Z, et al. Does the karyotype of a spontaneous abortion predict the karyotype of a subsequent abortion? Evidence from 273 women with two karyotyped spontaneous abortions. Am J Hum Genet. 1987;41:465-483.
19. 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.
20. Franklin RD, Kutteh WH. Antiphospholipid antibodies (APA) and recurrent pregnancy loss: treating a unique APA positive population. Hum Reprod. 2002;17:2981-2985.
21. De Wolf F, Carreras LO, Moerman P, et al. Decidual vasculopathy and extensive placental infarction in a patient with repeated thromboembolic accidents, recurrent fetal loss, and a lupus anticoagulant. Am J Obstet Gynecol. 1982;142:829-834.
22. Adler RR, Ng AK, Rote NS. Monoclonal antiphosphatidylserine antibody inhibits intercellular fusion of the choriocarcinoma line, JAR. Biol Reprod. 1995;53:905-910.
23. Katsuragawa H, Kanzaki H, Inoue T, et al. Monoclonal antibody against phosphatidylserine inhibits in vitro human trophoblastic hormone production and invasion. Biol Reprod. 1997;56:50-58.
24. Quenby S, Mountfield S, Cartwright JE, et al. Antiphospholipid antibodies prevent extravillous trophoblast differentiation. Fertil Steril. 2005;83:691-698.
25. Rai R, Cohen H, Dave M, et al. 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.
26. 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;174:1584-1589.
27. Empson M, Lassere M, Craig JC, et al. Recurrent pregnancy loss with antiphospholipid antibody: a systematic review of therapeutic trials. Obstet Gynecol. 2002;99:135-144.
28. Stephenson MD, Ballem PJ, Tsang P, et al. Treatment of antiphospholipid antibody syndrome (aps) in pregnancy: a randomized pilot trial comparing low molecularweight heparin to unfractionated heparin. J Obstet Gynaecol Can. 2004;26:729-734.
29. Noble LS, Kutteh WH, Lashey N, et al. 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.
30. Cowchock FS, Reece EA, Balaban D, et al. 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.
31. Laskin CA, Bombardier C, Hannah ME, et al. Prednisone and aspirin in women with autoantibodies and unexplained recurrent fetal loss. N Engl J Med. 1997;337:148-153.
32. Triolo G, Ferrante A, Ciccia F, et al. 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.
33. Kutteh WH. Antiphospholipid antibodies and reproduction. J Reprod Immunol. 1997;35:151-171.
34. Lockshin MD, Druzin M, Goei S, et al. Antibody to cardiolipin as a predictor of fetal distress or death in pregnant patients with systemic lupus erythematosus. N Engl J Med. 1985;313:152-156.
35. Bobrie G, Liote F, Houillier P, et al. Pregnancy in lupus nephritis and related disorders. Am J Kidney Dis. 1987;9:339-343.
36. Hayslett JP, Lynn RI. Effect of pregnancy in patients with lupus nephropathy. Kidney Int. 1980;18:207-220.
37. Sugiura-Ogasawara M, Ozaki Y, Sato T, et al. Poor prognosis of recurrent aborters with either maternal or paternal reciprocal translocations. Fertil Steril. 2004;81:367-373.
38. Goddijn M, Joosten JH, Knegt AC, et al. Clinical relevance of diagnosing structural chromosome abnormalities in couples with repeated miscarriage. Hum Reprod. 2004;19:1013-1017.
39. Stephenson MD, Sierra S. Reproductive outcomes in recurrent pregnancy loss associated with a parental carrier of a structural chromosome rearrangement. Hum Reprod. 2006;21:1076-1082.
40. Castelbaum AJ, Lessey BA. Infertility and implantation defects. Infertility and reproductive. Med Clin North Am. 2001;12:427-446.
41. Wilcox AJ, Baird DD, Weinberg CR. Time of implantation of the conceptus and loss of pregnancy. N Engl J Med. 1999;340:1796-1799.
42. Abalovich M, Gutierrez S, Alcaraz G, et al. Overt and subclinical hypothyroidism complicating pregnancy. Thyroid. 2002;12:63-68.
43. Rushworth FH, Backos M, Rai R, et al. Prospective pregnancy outcome in untreated recurrent miscarriers with thyroid autoantibodies. Hum Reprod. 2000;15:1637-1639.
44. Esplin MS, Branch DW, Silver R, et al. Thyroid autoantibodies are not associated with recurrent pregnancy loss. Am J Obstet Gynecol. 1998;179:1583-1586.
45. Hirahara F, Andoh N, Sawai K, et al. Hyperprolactinemic recurrent miscarriage and results of randomized bromocriptine treatment trials. Fertil Steril. 1998;70:246-252.
46. Hanson U, Persson B, Thunell S. Relationship between haemoglobin A1C in early type 1 (insulin-dependent) diabetic pregnancy and the occurrence of spontaneous abortion and fetal malformation in Sweden. Diabetologia. 1990;33:100-104.
47. Mills JL, Simpson JL, Driscoll SG, et al. Incidence of spontaneous abortion among normal women and insulin-dependent diabetic women whose pregnancies were identified within 21 days of conception. N Engl J Med. 1988;319:1617-1623.
48. Craig LB, Ke RW, Kutteh WH. Increased prevalence of insulin resistance in women with a history of recurrent pregnancy loss. Fertil Steril. 2002;78:487-490.
49. Sills ES, Perloe M, Palermo GD. Correction of hyperinsulinemia in oligo-ovulatory women with clomiphene-resistant polycystic ovary syndrome: a review of therapeutic rationale and reproductive outcomes. Eur J Obstet Gynecol Reprod Biol. 2000;91:135-141.
50. Lin PC. Reproductive outcomes in women with uterine anomalies. J Women's Health. 2004;13:33-39.
51. Carp H, Dolitzky M, Tur-Kaspa I, et al. Hereditary thrombophilias are not associated with a decreased live birth rate in women with recurrent miscarriage. Fertil Steril. 2002;78:58-62.
52. Rey E, Kahn SR, David M, et al. Thrombophilic disorders and fetal loss: a meta-analysis. Lancet. 2003;361:901-908.
53. Kovalevsky G, Gracia CR, Berlin JA, et al. Evaluation of the association between hereditary thrombophilias and recurrent pregnancy loss: a meta-analysis. Arch Intern Med. 2004;164:558-563.
54. Krabbendam I, Franx A, Bots ML, et al. Thrombophilias and recurrent pregnancy loss: a critical appraisal of the literature. Eur J Obstet Gynecol Reprod Biol. 2005;118:143-153.
55. Rai R, Backos M, Elgaddal S, et al. Factor V Leiden and recurrent miscarriage-prospective outcome of untreated pregnancies. Hum Reprod. 2002;17:442-445.
56. Preston FE, Rosendaal FR, Walker ID, et al. Increased fetal loss in women with heritable thrombophilia. Lancet. 1996;348:913-916.
57. Quere I, Mercier E, Bellet H, et al. Vitamin supplementation and pregnancy outcome in women with recurrent early pregnancy loss and hyperhomocysteinemia. Fertil Steril. 2001;75:823-825.
58. Penta M, Lukic A, Conte MP, et al. Infectious agents in tissues from spontaneous abortions in the first trimester of pregnancy. New Microbiol. 2003;26:329-337.
59. Ober C, Karrison T, Odem RR, et al. Mononuclear-cell immunisation in prevention of recurrent miscarriages: a randomised trial. Lancet. 1999;354:365-369.
60. Laird SM, Tuckerman EM, Cork BA, et al. A review of immune cells and molecules in women with recurrent miscarriage. Hum Reprod Update. 2003;9:163-174.
61. Wegmann TG, Lin H, Guilbert L, et al. Bidirectional cytokine interactions in the maternal-fetal relationship: is successful pregnancy a TH2 phenomenon? Immunol Today. 1993;14:353-356.
62. Clark DA, Vince G, Flanders KC, et al. CD56+ lymphoid cells in human first trimester pregnancy decidua as a source of novel transforming growth factorbeta 2-related immunosuppressive factors. Hum Reprod. 1994;9:2270-2277.
63. Szekeres-Bartho J, Autran B, Debre P, et al. Immunoregulatory effects of a suppressor factor from healthy pregnant women's lymphocytes after progesterone induction. Cell Immunol. 1989;122:281-294.
64. Mowbray JF, Gibbings C, Liddell H, et al. Controlled trial of treatment of recurrent spontaneous abortion by immunisation with paternal cells. Lancet. 1985;1:941-943.
65. Ho HN, Gill TJ III, Hsieh HJ, et al. Immunotherapy for recurrent spontaneous abortions in a Chinese population. Am J Reprod Immunol. 1991;25:10-15.
66. Cauchi MN, Lim D, Young DE, et al. Treatment of recurrent aborters by immunization with paternal cells-controlled trial. Am J Reprod Immunol. 1991;25:16-17.
67. The German RSA/IVIG Group. Intravenous immunoglobulin in the prevention of recurrent miscarriage. Br J Obstet Gynaecol. 1994;101:1072-1077.
68. Coulam CB, Krysa L, Stern JJ, et al. Intravenous immunoglobulin for treatment of recurrent pregnancy loss. Am J Reprod Immunol. 1995;34:333-337.
69. Christiansen OB, Mathiesen O, Husth M, et al. Placebo-controlled trial of treatment of unexplained secondary recurrent spontaneous abortions and recurrent late spontaneous abortions with i.v. immunoglobulin. Hum Reprod. 1995;10:2690-2695.
70. Stephenson MD, Dreher K, Houlihan E, et al. 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.
71. Rubio C, Simon C, Vidal F, et al. Chromosomal abnormalities and embryo development in recurrent miscarriage couples. Hum Reprod. 2003;18:182-188.
72. Carp HJA, Dirnfeld M, Dor J, et al. ART in recurrent miscarriage: preimplantation genetic diagnosis/screening or surrogacy? Hum Reprod. 2004;19:1502-1505.
73. Munne S, Chen S, Fischer J, et al. Preimplantation genetic diagnosis reduces pregnancy loss in women aged 35 years and older with a history of recurrent miscarriages. Fertil Steril. 2005;84:331-335.
74. Platteau P, Staessen C, Michiels A, et al. Preimplantation genetic diagnosis for aneuploidy screening in patients with unexplained recurrent miscarriages. Fertil Steril. 2005;83:393-397.
75. Brigham SA, Conlon C, Farquharson RG. A longitudinal study of pregnancy outcome following idiopathic recurrent miscarriage. Hum Reprod. 1999;14:2868-2871.
76. Clifford K, Rai R, Regan L. Future pregnancy outcome in unexplained recurrent first trimester miscarriage. Hum Reprod. 1997;12:387-389.
77. Lockwood CJ. Inherited thrombophilias in pregnant patients: detection and treatment paradigm. Obstet Gynecol. 2002;99:333-341.
78. Zetterberg H. Methylenetetrahydrofolate reductase and transcobalamin genetic polymorphisms in human spontaneous abortion: biological and clinical implications. Reprod Biol Endocrinol. 2004;2:7.
79. Ueland PM, Refsum H. Plasma homocysteine, a risk factor for vascular disease: plasma levels in health, disease, and drug therapy. J Lab Clin Med. 1989;114:473-501.
80. Rai R, Shlebak A, Cohen H, et al. Factor V Leiden and acquired activated protein C resistance among 1000 women with recurrent miscarriage. Hum Reprod. 2001;16:961-965.
81. Rodeghiero F, Tosetto A. Activated protein C resistance and factor V Leiden mutation are independent risk factors for venous thromboembolism. Ann Intern Med. 1999;130:643-650.
82. British Society for Haematology. Investigation and management of heritable thrombophilia. Br J Haematol. 2001;114:512-528.