Endocrinology and recurrent early pregnancy loss

Seminars in Reproductive Medicine

Volumn 29, Issue 6, 2011, Pages 482-490

  Smith, M Leah ^a   Schust, Danny J ^a  

^a University of Missouri   (United States)

Author keywords

luteal phase defect; polycystic ovarian syndrome; recurrent pregnancy loss; Thyroid autoantibodies

Indexed keywords

CHORIONIC GONADOTROPIN; METFORMIN; PRASTERONE SULFATE; PROGESTERONE;

ARTICLE; AUTOIMMUNITY; ENDOCRINE DISEASE; ENDOCRINOLOGY; ENDOMETRIUM BIOPSY; FIRST TRIMESTER PREGNANCY; GLUCOSE TOLERANCE TEST; HUMAN; HYPOTHYROIDISM; INSULIN RESISTANCE; LUTEAL INSUFFICIENCY; LUTEAL PHASE; NONHUMAN; OBESITY; OVARY POLYCYSTIC DISEASE; OVULATION INDUCTION; PATHOPHYSIOLOGY; PREGNANCY; PREGNANCY DISORDERS OF ENDOCRINE ORIGIN; PREVALENCE; RECURRENT PREGNANCY LOSS; SUPPLEMENTATION; THYROID DISEASE;

ABORTION, HABITUAL; AUTOANTIBODIES; ENDOCRINE SYSTEM DISEASES; FEMALE; HUMANS; HYPOTHYROIDISM; LUTEAL PHASE; POLYCYSTIC OVARY SYNDROME; PREGNANCY; PREGNANCY COMPLICATIONS; PREGNANCY TRIMESTER, FIRST; THYROIDITIS, AUTOIMMUNE;

EID: 83455162288     PISSN: 15268004     EISSN: 15264564     Source Type: Journal    
DOI: 10.1055/s-0031-1293202     Document Type: Article

References (93)

1. Boklage C E. Survival probability of human conceptions from fertilization to term. Int J Fertil 1990 35 2 75, 79-80, 8194
2. Wilcox A J., Weinberg C R., O'Connor J F. et al. Incidence of early loss of pregnancy. N Engl J Med 1988 319 4 189-194
3. Edmonds D K., Lindsay K S., Miller J F., Williamson E, Wood P J. Early embryonic mortality in women. Fertil Steril 1982 38 4 447-453 (Pubitemid 12034441)
4. Rai R, Regan L. Recurrent miscarriage. Lancet 2006 368 9535 601-611 (Pubitemid 44209184)
5. Suzumori N, Sugiura-Ogasawara M. Genetic factors as a cause of miscarriage. Curr Med Chem 2010 17 29 3431-3437
6. Alberman E. The epidemiology of repeated abortion. In: Beard R W. Sharp F eds. Early Pregnancy Loss: Mechanisms and Treatment. New York, NY Springer-Verlag 1988 9-17
7. Fryns J P., Van Buggenhout G. Structural chromosome rearrangements in couples with recurrent fetal wastage. Eur J Obstet Gynecol Reprod Biol 1998 81 2 171-176 (Pubitemid 28561493)
8. Jaslow C R., Carney J L., Kutteh W H. Diagnostic factors identified in 1020 women with two versus three or more recurrent pregnancy losses. Fertil Steril 2010 93 4 1234-1243
9. Proctor J A., Haney A F. Recurrent first trimester pregnancy loss is associated with uterine septum but not with bicornuate uterus. Fertil Steril 2003 80 5 1212-1215 (Pubitemid 37377753)
10. Propst A M., Hill J A. III. Anatomic factors associated with recurrent pregnancy loss. Semin Reprod Med 2000 18 4 341-350 (Pubitemid 32422753)
11. Homer H A., Li T C., Cooke I D. The septate uterus: a review of management and reproductive outcome. Fertil Steril 2000 73 1 1-14 (Pubitemid 30018013)
12. Miyakis S, Lockshin M D., Atsumi T et al. International consensus statement on an update of the classification criteria for definite antiphospholipid syndrome (APS). J Thromb Haemost 2006 4 2 295-306
13. Ziakas P D., Pavlou M, Voulgarelis M. Heparin treatment in antiphospholipid syndrome with recurrent pregnancy loss: a systematic review and meta-analysis. Obstet Gynecol 2010 115 6 1256-1262
14. Glinoer D. The regulation of thyroid function in pregnancy: pathways of endocrine adaptation from physiology to pathology. Endocr Rev 1997 18 3 404-433 (Pubitemid 27246883)
15. Benhadi N, Wiersinga W M., Reitsma J B., Vrijkotte T G., Bonsel G J. Higher maternal TSH levels in pregnancy are associated with increased risk for miscarriage, fetal or neonatal death. Eur J Endocrinol 2009 160 6 985-991
16. Poppe K, Velkeniers B, Glinoer D. Thyroid disease and female reproduction. Clin Endocrinol (Oxf) 2007 66 3 309-321 (Pubitemid 46239305)
17. Glinoer D. Thyroidal and immune adaptation to pregnancy: focus on maternal hypo- and hyperthyroidism. In: Lazarus J Pirags V Butz S eds. The Thyroid and Reproduction. New York, NY Thieme 2009 46-58
18. Hollowell J G., Staehling N W., Flanders W D. et al. Serum TSH, T(4), and thyroid antibodies in the United States population (1988 to 1994): National Health and Nutrition Examination Survey (NHANES III). J Clin Endocrinol Metab 2002 87 2 489-499 (Pubitemid 34158210)
19. Billingham R E., Brent L, Medawar P B. Actively acquired tolerance of foreign cells. Nature 1953 172 4379 603-606
20. Anjum N, Baker P N., Robinson N J., Aplin J D. Maternal celiac disease autoantibodies bind directly to syncytiotrophoblast and inhibit placental tissue transglutaminase activity. Reprod Biol Endocrinol 2009 7 16
21. Stagnaro-Green A, Roman S H., Cobin R H., el-Harazy E, Alvarez-Marfany M, Davies T F. Detection of at-risk pregnancy by means of highly sensitive assays for thyroid autoantibodies. JAMA 1990 264 11 1422-1425 (Pubitemid 20331938)
22. Bussen S, Steck T. Thyroid autoantibodies in euthyroid non-pregnant women with recurrent spontaneous abortions. Hum Reprod 1995 10 11 2938-2940
23. Glinoer D, Soto M F., Bourdoux P et al. Pregnancy in patients with mild thyroid abnormalities: maternal and neonatal repercussions. J Clin Endocrinol Metab 1991 73 2 421-427 (Pubitemid 21921891)
24. Kutteh W H., Yetman D L., Carr A C., Beck L A., Scott R T. Jr. Increased prevalence of antithyroid antibodies identified in women with recurrent pregnancy loss but not in women undergoing assisted reproduction. Fertil Steril 1999 71 5 843-848 (Pubitemid 29206908)
25. Pratt D, Novotny M, Kaberlein G, Dudkiewicz A, Gleicher N. Antithyroid antibodies and the association with non-organ-specific antibodies in recurrent pregnancy loss. Am J Obstet Gynecol 1993 168 3 Pt 1 837-841 (Pubitemid 23096005)
26. Singh A, Dantas Z N., Stone S C., Asch R H. Presence of thyroid antibodies in early reproductive failure: biochemical versus clinical pregnancies. Fertil Steril 1995 63 2 277-281
27. Esplin M S., Branch D W., Silver R, Stagnaro-Green A. Thyroid autoantibodies are not associated with recurrent pregnancy loss. Am J Obstet Gynecol 1998 179 6 Pt 1 1583-1586 (Pubitemid 29028405)
28. Rushworth F H., Backos M, Rai R, Chilcott I T., Baxter N, Regan L. Prospective pregnancy outcome in untreated recurrent miscarriers with thyroid autoantibodies. Hum Reprod 2000 15 7 1637-1639
29. Kaprara A, Krassas G E. Thyroid autoimmunity and miscarriage. Hormones (Athens) 2008 7 4 294-302
30. Matalon S T., Blank M, Ornoy A, Shoenfeld Y. The association between anti-thyroid antibodies and pregnancy loss. Am J Reprod Immunol 2001 45 2 72-77 (Pubitemid 32111901)
31. Lee Y L., Ng H P., Lau K S. et al. Increased fetal abortion rate in autoimmune thyroid disease is related to circulating TPO autoantibodies in an autoimmune thyroiditis animal model. Fertil Steril 2009 91 5, Suppl 2104-2109
32. Imaizumi M, Pritsker A, Kita M, Ahmad L, Unger P, Davies T F. Non-MHC driven exacerbation of experimental thyroiditis in the postpartum period. Autoimmunity 2001 34 2 95-105 (Pubitemid 34149797)
33. Iijima T, Tada H, Hidaka Y, Mitsuda N, Murata Y, Amino N. Effects of autoantibodies on the course of pregnancy and fetal growth. Obstet Gynecol 1997 90 3 364-369 (Pubitemid 27357926)
34. Krassas G E., Poppe K, Glinoer D. Thyroid function and human reproductive health. Endocr Rev 2010 31 5 702-755
35. Negro R, Schwartz A, Gismondi R, Tinelli A, Mangieri T, Stagnaro-Green A. Increased pregnancy loss rate in thyroid antibody negative women with TSH levels between 2.5 and 5.0 in the first trimester of pregnancy. J Clin Endocrinol Metab 2010 95 9 E44-E48
36. De Vivo A, Mancuso A, Giacobbe A et al. Thyroid function in women found to have early pregnancy loss. Thyroid 2010 20 6 633-637
37. Smyth P P., Wijeyaratne C N., Kaluarachi W N. et al. Sequential studies on thyroid antibodies during pregnancy. Thyroid 2005 15 5 474-477 (Pubitemid 40770627)
38. Abalovich M, Gutierrez S, Alcaraz G, Maccallini G, Garcia A, Levalle O. Overt and subclinical hypothyroidism complicating pregnancy. Thyroid 2002 12 1 63-68 (Pubitemid 34106718)
39. Bussen S, Steck T, Dietl J. Increased prevalence of thyroid antibodies in euthyroid women with a history of recurrent in-vitro fertilization failure. Hum Reprod 2000 15 3 545-548 (Pubitemid 30142359)
40. Negro R, Formoso G, Mangieri T, Pezzarossa A, Dazzi D, Hassan H. Levothyroxine treatment in euthyroid pregnant women with autoimmune thyroid disease: effects on obstetrical complications. J Clin Endocrinol Metab 2006 91 7 2587-2591 (Pubitemid 44024622)
41. Vaquero E, Lazzarin N, De Carolis C, Valensise H, Moretti C, Ramanini C. Mild thyroid abnormalities and recurrent spontaneous abortion: diagnostic and therapeutical approach. Am J Reprod Immunol 2000 43 4 204-208 (Pubitemid 30229675)
42. Reid S M., Middleton P, Cossich M C., Crowther C A. Interventions for clinical and subclinical hypothyroidism in pregnancy. Cochrane Database Syst Rev 2010 7 CD007752
43. Alexander E K., Marqusee E, Lawrence J, Jarolim P, Fischer G A., Larsen P R. Timing and magnitude of increases in levothyroxine requirements during pregnancy in women with hypothyroidism. N Engl J Med 2004 351 3 241-249
44. Glinoer D. Thyroid immunity, thyroid dysfunction, and the risk of miscarriage: à propos article by Vaquero et al. Mild thyroid abnormalities and recurrent spontaneous abortion: diagnostic and therapeutical approach. Am J Reprod Immunol 2000 43 4 202-203 (Pubitemid 30229674)
45. Glinoer D, Delange F. The potential repercussions of maternal, fetal, and neonatal hypothyroxinemia on the progeny. Thyroid 2000 10 10 871-887
46. Mandel S J., Larsen P R., Seely E W., Brent G A. Increased need for thyroxine during pregnancy in women with primary hypothyroidism. N Engl J Med 1990 323 2 91-96 (Pubitemid 20221645)
47. Valbuena D, Jasper M, Remohí J, Pellicer A, Simón C. Ovarian stimulation and endometrial receptivity. Hum Reprod 1999 14 Suppl 2 107-111 (Pubitemid 30040669)
48. Csapo A I., Pulkkinen M O., Wiest W G. Effects of luteectomy and progesterone replacement therapy in early pregnant patients. Am J Obstet Gynecol 1973 115 6 759-765
49. Jones G S. The luteal phase defect. Fertil Steril 1976 27 4 351-356
50. Arredondo F, Noble L S. Endocrinology of recurrent pregnancy loss. Semin Reprod Med 2006 24 1 33-39 (Pubitemid 43132673)
51. Horta J L., Fernández J G., de León B S., Cortés-Gallegos V. Direct evidence of luteal insufficiency in women with habitual abortion. Obstet Gynecol 1977 49 6 705-708 (Pubitemid 8131458)
52. Serle E, Aplin J D., Li T C. et al. Endometrial differentiation in the peri-implantation phase of women with recurrent miscarriage: a morphological and immunohistochemical study. Fertil Steril 1994 62 5 989-996 (Pubitemid 24328227)
53. Li T C., Spuijbroek M D., Tuckerman E, Anstie B, Loxley M, Laird S. Endocrinological and endometrial factors in recurrent miscarriage. BJOG 2000 107 12 1471-1479 (Pubitemid 32047478)
54. Tulppala M, Björses U M., Stenman U H., Wahlström T, Ylikorkala O. Luteal phase defect in habitual abortion: progesterone in saliva. Fertil Steril 1991 56 1 41-44
55. Noyes R W., Hertig A T., Rock J. Dating the endometrial biopsy. Am J Obstet Gynecol 1975 122 2 262-263
56. Duggan M A., Brashert P, Ostor A et al. The accuracy and interobserver reproducibility of endometrial dating. Pathology 2001 33 3 292-297 (Pubitemid 32735240)
57. Scott R T., Snyder R R., Strickland D M. et al. The effect of interobserver variation in dating endometrial histology on the diagnosis of luteal phase defects. Fertil Steril 1988 50 6 888-892 (Pubitemid 19017958)
58. Daya S. Efficacy of progesterone support for pregnancy in women with recurrent miscarriage. A meta-analysis of controlled trials. Br J Obstet Gynaecol 1989 96 3 275-280 (Pubitemid 19093250)
59. Scott R T., Snyder R R., Bagnall J W., Reed K D., Adair C F., Hensley S D. Evaluation of the impact of intraobserver variability on endometrial dating and the diagnosis of luteal phase defects. Fertil Steril 1993 60 4 652-657 (Pubitemid 23298509)
60. Gibson M, Badger G J., Byrn F, Lee K R., Korson R, Trainer T D. Error in histologic dating of secretory endometrium: variance component analysis. Fertil Steril 1991 56 2 242-247
61. Smith S, Hosid S, Scott L. Endometrial biopsy dating. Interobserver variation and its impact on clinical practice. J Reprod Med 1995 40 1 1-3
62. Coutifaris C, Myers E R., Guzick D S. et al, NICHD National Cooperative Reproductive Medicine Network. Histological dating of timed endometrial biopsy tissue is not related to fertility status. Fertil Steril 2004 82 5 1264-1272 (Pubitemid 39469442)
63. Sherman B M., Korenman S G. Measurement of plasma LH, FSH, estradiol and progesterone in disorders of the human menstrual cycle: the short luteal phase. J Clin Endocrinol Metab 1974 38 1 89-93
64. Harrison R F. Human chorionic gonadotrophin (hCG) in the management of recurrent abortion; results of a multi-centre placebo-controlled study. Eur J Obstet Gynecol Reprod Biol 1992 47 3 175-179 (Pubitemid 23018382)
65. Li T C., Tuckerman E M., Laird S M. Endometrial factors in recurrent miscarriage. Hum Reprod Update 2002 8 1 43-52 (Pubitemid 34144983)
66. Haas D M., Ramsey P S. Progestogen for preventing miscarriage. Cochrane Database Syst Rev 2008 2 CD003511
67. Glueck C J., Wang P, Goldenberg N, Sieve-Smith L. Pregnancy outcomes among women with polycystic ovary syndrome treated with metformin. Hum Reprod 2002 17 11 2858-2864 (Pubitemid 35350902)
68. Janssen O E., Mehlmauer N, Hahn S, Offner A H., Gärtner R. High prevalence of autoimmune thyroiditis in patients with polycystic ovary syndrome. Eur J Endocrinol 2004 150 3 363-369 (Pubitemid 38443788)
69. Dorman J S., Burke J P., McCarthy B J. et al. Temporal trends in spontaneous abortion associated with type 1 diabetes. Diabetes Res Clin Pract 1999 43 1 41-47 (Pubitemid 29096410)
70. Mills J L., Simpson J L., Driscoll S G. 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 25 1617-1623 (Pubitemid 19015234)
71. Cocksedge K A., Li T C., Saravelos S H., Metwally M. A reappraisal of the role of polycystic ovary syndrome in recurrent miscarriage. Reprod Biomed Online 2008 17 1 151-160
72. Craig L B., Ke R W., Kutteh W H. Increased prevalence of insulin resistance in women with a history of recurrent pregnancy loss. Fertil Steril 2002 78 3 487-490
73. Glueck C J., Phillips H, Cameron D, Sieve-Smith L, Wang P. Continuing metformin throughout pregnancy in women with polycystic ovary syndrome appears to safely reduce first-trimester spontaneous abortion: a pilot study. Fertil Steril 2001 75 1 46-52 (Pubitemid 32041226)
74. Jakubowicz D J., Iuorno M J., Jakubowicz S, Roberts K A., Nestler J E. Effects of metformin on early pregnancy loss in the polycystic ovary syndrome. J Clin Endocrinol Metab 2002 87 2 524-529 (Pubitemid 34158214)
75. Sills E S., Perloe M, Palermo G D. Correction of hyperinsulinemia in oligoovulatory women with clomiphene-resistant polycystic ovary syndrome: a review of therapeutic rationale and reproductive outcomes. Eur J Obstet Gynecol Reprod Biol 2000 91 2 135-141 (Pubitemid 30408320)
76. Zolghadri J, Tavana Z, Kazerooni T, Soveid M, Taghieh M. Relationship between abnormal glucose tolerance test and history of previous recurrent miscarriages, and beneficial effect of metformin in these patients: a prospective clinical study. Fertil Steril 2008 90 3 727-730
77. Legro R S., Barnhart H X., Schlaff W D. et al, Cooperative Multicenter Reproductive Medicine Network. Clomiphene, metformin, or both for infertility in the polycystic ovary syndrome. N Engl J Med 2007 356 6 551-566 (Pubitemid 46220816)
78. Moll E, Bossuyt P M., Korevaar J C., Lambalk C B., van der Veen F. Effect of clomifene citrate plus metformin and clomifene citrate plus placebo on induction of ovulation in women with newly diagnosed polycystic ovary syndrome: randomised double blind clinical trial. BMJ 2006 332 7556 1485
79. Palomba S, Orio F Jr, Falbo A, Russo T, Tolino A, Zullo F. Plasminogen activator inhibitor 1 and miscarriage after metformin treatment and laparoscopic ovarian drilling in patients with polycystic ovary syndrome. Fertil Steril 2005 84 3 761-765 (Pubitemid 41317745)
80. Glueck C J., Wang P, Fontaine R N., Sieve-Smith L, Tracy T, Moore S K. Plasminogen activator inhibitor activity: an independent risk factor for the high miscarriage rate during pregnancy in women with polycystic ovary syndrome. Metabolism 1999 48 12 1589-1595
81. Glueck C J., Goldenberg N, Pranikoff J, Loftspring M, Sieve L, Wang P. Height, weight, and motor-social development during the first 18 months of life in 126 infants born to 109 mothers with polycystic ovary syndrome who conceived on and continued metformin through pregnancy. Hum Reprod 2004 19 6 1323-1330 (Pubitemid 38807703)
82. Conway G S., Jacobs H S., Holly J M., Wass J A. Effects of luteinizing hormone, insulin, insulin-like growth factor-I and insulin-like growth factor small binding protein 1 in the polycystic ovary syndrome. Clin Endocrinol (Oxf) 1990 33 5 593-603 (Pubitemid 20346607)
83. Liddell H S., Sowden K, Farquhar C M. Recurrent miscarriage: screening for polycystic ovaries and subsequent pregnancy outcome. Aust N Z J Obstet Gynaecol 1997 37 4 402-406 (Pubitemid 27511371)
84. Rai R, Backos M, Rushworth F, Regan L. Polycystic ovaries and recurrent miscarriagea reappraisal. Hum Reprod 2000 15 3 612-615 (Pubitemid 30142371)
85. Okon M A., Laird S M., Tuckerman E M., Li T C. Serum androgen levels in women who have recurrent miscarriages and their correlation with markers of endometrial function. Fertil Steril 1998 69 4 682-690 (Pubitemid 28188464)
86. van Wely M, Bayram N, van der Veen F, Bossuyt P M. Predicting ongoing pregnancy following ovulation induction with recombinant FSH in women with polycystic ovary syndrome. Hum Reprod 2005 20 7 1827-1832 (Pubitemid 40932363)
87. Metwally M, Ong K J., Ledger W L., Li T C. Does high body mass index increase the risk of miscarriage after spontaneous and assisted conception? A meta-analysis of the evidence. Fertil Steril 2008 90 3 714-726
88. Lashen H, Fear K, Sturdee D W. Obesity is associated with increased risk of first trimester and recurrent miscarriage: matched case-control study. Hum Reprod 2004 19 7 1644-1646 (Pubitemid 38997196)
89. Al-Azemi M, Omu F E., Omu A E. The effect of obesity on the outcome of infertility management in women with polycystic ovary syndrome. Arch Gynecol Obstet 2004 270 4 205-210
90. Hamilton-Fairley D, Kiddy D, Watson H, Paterson C, Franks S. Association of moderate obesity with a poor pregnancy outcome in women with polycystic ovary syndrome treated with low dose gonadotrophin. Br J Obstet Gynaecol 1992 99 2 128-131
91. Clark A M., Ledger W, Galletly C et al. Weight loss results in significant improvement in pregnancy and ovulation rates in anovulatory obese women. Hum Reprod 1995 10 10 2705-2712
92. Rotterdam ESHRE/ASRM-Sponsored PCOS Consensus Workshop Group. Revised 2003 consensus on diagnostic criteria and long-term health risks related to polycystic ovary syndrome. Fertil Steril 2004 81 1 19-25
93. Zawadski J K., Dunaif A. Diagnostic criteria for polycystic ovary syndrome: towards a rational approach. In: Dunaif A Givens J R. Haseltine F P. Merriam G R. eds. Polycystic Ovary Syndrome. Boston, MA Blackwell Scientific 1992 377-384