Early recurrent miscarriage: Evaluation and management;Fausses couches précoces « à répétition »: Bilan et prise en charge

Journal de Gynecologie Obstetrique et Biologie de la Reproduction

Volumn 43, Issue 10, 2014, Pages 812-841

  Gallot, V ^a   Nedellec, S ^a   Capmas, P ^a   Legendre, G ^b   Lejeune Saada, V ^c   Subtil, D ^d   Nizard, J ^e,f   Leveque J ^g   Deffieux, X ^a   Herve B ^h,i   Vialard, F ^h,i  

^a HÔPITAL ANTOINE BÉCLÈRE   (France)

^b ANGERS UNIVERSITY HOSPITAL   (France)

^c Centre Hospitalier d'Auch   (France)

^d LILLE UNIVERSITY HOSPITAL   (France)

^e PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^f UNIVERSITÉ PIERRE ET MARIE CURIE   (France)

^g RENNES UNIVERSITY HOSPITAL   (France)

^h CENTRE HOSPITALIER INTERCOMMUNAL   (France)

ⁱ INRA Institut National de la Recherche Agronomique   (France)

Author keywords

Chronic endometritis; Environment; Recurrent pregnancyloss; Recurrentmiscarriage; Spontaneousabortion; Vitamins; Weight

Indexed keywords

ACETYLSALICYLIC ACID; FOLIC ACID; LEVOTHYROXINE; LOW MOLECULAR WEIGHT HEPARIN; PROGESTERONE; RETINOL;

ANTIPHOSPHOLIPID SYNDROME; ARTICLE; CHROMOSOME ANALYSIS; DIABETES MELLITUS; GLYCEMIC CONTROL; HUMAN; HYPERHOMOCYSTEINEMIA; HYPERPROLACTINEMIA; HYPOTHYROIDISM; OVARIAN RESERVE ALTERATION; OVARY DISEASE; RECURRENT ABORTION; SPONTANEOUS ABORTION; THYROID DISEASE; UTERINE ABNORMALITY; UTERUS DISEASE; VITAMIN DEFICIENCY; ABORTION, HABITUAL; FEMALE; PRACTICE GUIDELINE; PREGNANCY; STANDARDS;

ABORTION, HABITUAL; FEMALE; HUMANS; PRACTICE GUIDELINES AS TOPIC; PREGNANCY;

EID: 84920173054     PISSN: 03682315     EISSN: 17730430     Source Type: Journal    
DOI: None     Document Type: Article

References (163)

1. Regan L, Rai R. Epidemiology and the medical causes of mis-carriage. Baillieres Best Pract Res Clin Obstet Gynaecol 2000; 14: 839-54.
2. Rai R, Regan L. Recurrent miscarriage. Lancet 2006; 368: 601-11.
3. Berry CW, Brambati B, Eskes TK, Exalto N, Fox H, Geraedts JP, et al. The Euro-Team Early Pregnancy (ETEP) protocol forrecurrent miscarriage. Hum Reprod 1995; 10: 1516-20.
4. Hogge WA, Byrnes AL, Lanasa MC, Surti U. The clinical useof karyotyping spontaneous abortions. Am J Obstet Gynecol2003; 189: 397-400 [discussion 400-2].
5. Brigham S, Conlon C, Farquharson R. A longitudinal studyof pregnancy outcome following idiopathic recurrent miscar-riage. Hum Reprod 1999; 11: 2868-71.
6. Ogasawara M, Aoki K, Okada S, Suzumori K. Embryonic karyo-type of abortuses in relation to the number of previousmiscarriages. Fertil Steril 2000; 73: 300-4.
7. Nybo Andersen AM, Wohlfahrt J, Christens P, Olsen J, Mel-Bye M. Maternal age and fetal loss: population based registerlinkage study. BMJ 2000; 320: 1708-12.
8. Stefanidou EM, Caramellino L, Patriarca A, Menato G. Maternal caffeine consumption and sine causa recurrent mis-carriage. Eur J Obstet Gynecol Reprod Biol 2011; 158: 220-4.
9. Delabaere A, Huchon C, Deffieux X, Beucher G, Gal-lot V, Nedellec S, et al. Epidémiologie des pertesde grossesse. J Gynecol Obstet Biol Reprod 2014, http://dx.doi.org/10.1016/j.jgyn.2014.09.011 [in press].
10. Ferraretti AP, La Marca A, Fauser BC, Tarlatzis B, NargundG, Gianaroli L. ESHRE consensus on the definition of "poorresponse" to ovarian stimulation for in vitro fertilization: theBologna criteria. Hum Reprod 2011; 26: 1616-24.
11. Trout SW, Seifer DB. Do women with unexplained recurrentpregnancy loss have higher day 3 serum FSH and estradiolvalues? Fertil Steril 2000; 74: 335-7.
12. Homer HA, Li TC, Cooke ID. The septate uterus: a reviewof management and reproductive outcome. Fertil Steril2000; 73: 1-14.
13. Kowalik CR, Goddijn M, Emanuel MH, Bongers MY, Spinder T, de Kruif JH, et al. Metroplasty versus expectant managementfor women with recurrent miscarriage and a septate uterus. Cochrane Database Syst Rev 2011: CD008576.
14. Jaslow CR, Kutteh WH. Effect of prior birth and miscar-riage frequency on the prevalence of acquired and congenitaluterine anomalies in women with recurrent miscarriage: across-sectional study. Fertil Steril 2013; 99: 1916-22 [e1].
15. Keltz MD, Olive DL, Kim AH, Arici A. Sonohysterographyfor screening in recurrent pregnancy loss. Fertil Steril1997; 67: 670-4.
16. Ventolini G, Zhang M, Gruber J. Hysteroscopy in the evalua-tion of patients with recurrent pregnancy loss: a cohort studyin a primary care population. Surg Endosc 2004; 18: 1782-4.
17. Souza CA, Schmitz C, Genro VK, Martins A, Scheffel C, Opper-mann ML, et al. Office hysteroscopy study in consecutivemiscarriage patients. Rev Assoc Med Bras 2011; 57: 397-401.
18. Cogendez E, Dolgun ZN, Sanverdi I, Turgut A, Eren S. Post-abortion hysteroscopy: a method for early diagnosis ofcongenital and acquired intrauterine causes of abortions. EurJ Obstet Gynecol Reprod Biol 2011; 156: 101-4.
19. Metwally M, Ong KJ, Ledger WL, Li TC. Does high body massindex increase the risk of miscarriage after spontaneous andassisted conception? A meta-analysis of the evidence. FertilSteril 2008; 90: 714-26.
20. Lashen H, Fear K, Sturdee DW. Obesity is associated withincreased risk of first trimester and recurrent miscar-riage: matched case-control study. Hum Reprod 2004; 19: 1644-6.
21. Maconochie N, Doyle P, Prior S, Simmons R. Risk factors forfirst trimester miscarriage-results from a UK-population-based case-control study. BJOG 2007; 114: 170-86.
22. Helgstrand S, Andersen AM. Maternal underweight and therisk of spontaneous abortion. Acta Obstet Gynecol Scand2005; 84: 1197-201.
23. Li TC, Spuijbroek MD, Tuckerman E, Anstie B, Loxley M, Laird S. Endocrinological and endometrial factors in recurrent mis-carriage. BJOG 2000; 107: 1471-9.
24. CNGOF. Extrait des mises à jour en gynécologie médicale. Paris: Masson; 2012.
25. Zolghadri J, Momtahan M, Aminian K, Ghaffarpasand F, Tavana Z. The value of hysteroscopy in diagnosis of chronic endo-metritis in patients with unexplained recurrent spontaneousabortion. Eur J Obstet Gynecol Reprod Biol 2011; 155: 217-20.
26. Cicinelli E, Matteo M, Tinelli R, Pinto V, Marinaccio M, Indrac-Colo U, et al. Chronic endometritis due to common bacteria isprevalent in women with recurrent miscarriage as confirmedby improved pregnancy outcome after antibiotic treatment. Reprod Sci 2013; 21: 640-7.
27. Conde-Ferraez L, Chan May Ade A, Carrillo-Martinez JR, Ayora-Talavera G, Gonzalez-Losa Mdel R. Human papillo-mavirus infection and spontaneous abortion: a case-controlstudy performed in Mexico. Eur J Obstet Gynecol Reprod Biol2013; 170: 468-73.
28. Donders GG, Van Bulck B, Caudron J, Londers L, VereeckenA, Spitz B. Relationship of bacterial vaginosis and mycoplas-mas to the risk of spontaneous abortion. Am J Obstet Gynecol2000; 183: 431-7.
29. Oakeshott P, Hay P, Hay S, Steinke F, Rink E, Kerry S. Associa-tion between bacterial vaginosis or chlamydial infection andmiscarriage before 16 weeks' gestation: prospective commu-nity based cohort study. BMJ 2002; 325: 1334.
30. Nigro G, Mazzocco M, Mattia E, Di Renzo GC, Carta G, Anceschi MM. Role of the infections in recurrent spontaneous abortion. J Matern Fetal Neonatal Med 2011; 24: 983-9.
31. Robertson L, Greer I. Thromboembolism in pregnancy. CurrOpin Obstet Gynecol 2005; 17: 113-6.
32. Jaslow CR, Carney JL, Kutteh WH. Diagnostic factors identi-fied in 1020 women with two versus three or more recurrentpregnancy losses. Fertil Steril 2010; 93: 1234-43.
33. Puri M, Kaur L, Walia GK, Mukhopadhhyay R, Sachdeva MP, Trivedi SS, et al. MTHFR C677T polymorphism, folate, vita-min B12 and homocysteine in recurrent pregnancy losses: acase-control study among North Indian women. J Perinat Med2013; 41: 549-54.
34. Sikora J, Magnucki J, Zietek J, Kobielska L, Partyka R, Koko-Cinska D, et al. Homocysteine, folic acid and vitamin B12concentration in patients with recurrent miscarriages. NeuroEndocrinol Lett 2007; 28: 507-12.
35. Reznikoff-Etievant MF, Zittoun J, Vaylet C, Pernet P, Mil-liez J. Low Vitamin B(12) level as a risk factor for veryearly recurrent abortion. Eur J Obstet Gynecol Reprod Biol2002; 104: 156-9.
36. Moller UK, Streym S, Heickendorff L, Mosekilde L, RejnmarkL. Effects of 25OHD concentrations on chances of pregnancyand pregnancy outcomes: a cohort study in healthy Danishwomen. Eur J Clin Nutr 2012; 66: 862-8.
37. Schneuer FJ, Roberts CL, Guilbert C, Simpson JM, Algert CS, Khambalia AZ, et al. Effects of maternal serum 25-hydroxyvitamin D concentrations in the first trimester onsubsequent pregnancy outcomes in an Australian population. Am J Clin Nutr 2014; 99: 287-95.
38. Legendre G, Gicquel M, Lejeune V, Praola E, Def-fieux X, Sentilhes L, et al. Psychologie et pertefoetals. J Gynecol Obstet Biol Reprod 2014, http://dx.doi.org/10.1016/j.jgyn.2014.09.019 [in press].
39. De la Rochebrochard E, Thonneau P. Paternal age andmaternal age are risk factors for miscarriage; resultsof a multicentre European study. Hum Reprod 2002; 17: 1649-56.
40. Belloc S, Cohen-Bacrie P, Benkhalifa M, Cohen-Bacrie M, DeMouzon J, Hazout A, et al. Effect of maternal and pater-nal age on pregnancy and miscarriage rates after intrauterineinsemination. Reprod Biomed Online 2008; 17: 392-7.
41. Belloc S, Benkhalifa M, Cohen-Bacrie M, Dalleac A, Amar E, Zini A. Sperm deoxyribonucleic acid damage in normozoosper-mic men is related to age and sperm progressive motility. Fertil Steril 2014; 101: 1588-93.
42. Sakkas D, Alvarez JG, Sperm DNA. fragmentation: mecha-nisms of origin, impact on reproductive outcome, andanalysis. Fertil Steril 2010; 93: 1027-36.
43. Robinson L, Gallos ID, Conner SJ, Rajkhowa M, Miller D, LewisS, et al. The effect of sperm DNA fragmentation on mis-carriage rates: a systematic review and meta-analysis. HumReprod 2012; 27: 2908-17.
44. Evenson DP, Jost LK, Marshall D, Zinaman MJ, Clegg E, PurvisK, et al. Utility of the sperm chromatin structure assay as adiagnostic and prognostic tool in the human fertility clinic. Hum Reprod 1999; 14: 1039-49.
45. Al-Gubory KH, Fowler PA, Garrel C. The roles of cellularreactive oxygen species, oxidative stress and antioxi-dants in pregnancy outcomes. Int J Biochem Cell Biol2010; 42: 1634-50.
46. Simsek M, Naziroglu M, Simsek H, Cay M, Aksakal M, Kumru S. Blood plasma levels of lipoperoxides, glutathione peroxi-dase, beta carotene, vitamin A and E in women with habitualabortion. Cell Biochem Funct 1998; 16: 227-31.
47. Kumar S, Occupational. environmental and lifestyle fac-tors associated with spontaneous abortion. Reprod Sci2011; 18: 915-30.
48. Li Y, Lin H, Li Y, Cao J. Association between socio-psycho-behavioral factors and male semen quality: systematic reviewand meta-analyses. Fertil Steril 2011; 95: 116-23.
49. Kirkinen P, Jouppila P, Koivula A, Vuori J, Puukka M. The effectof caffeine on placental and fetal blood flow in human pre-gnancy. Am J Obstet Gynecol 1983; 147: 939-42.
50. Benammar A, Sermondade N, Faure C, Dupont C, Cedrin-Durnerin I, Sifer C, et al. Nutrition and miscarriages: aliterature review. Gynecol Obstet Fertil 2012; 40: 162-9.
51. Weng X, Odouli R, Li DK. Maternal caffeine consumptionduring pregnancy and the risk of miscarriage: a prospectivecohort study. Am J Obstet Gynecol 2008; 198: 279 [e1-e8].
52. Ness RB, Grisso JA, Hirschinger N, Markovic N, Shaw LM, Day NL, et al. Cocaine and tobacco use and the risk of spontaneousabortion. N Engl J Med 1999; 340: 333-9.
53. Agarwal A, Aponte-Mellado A, Premkumar BJ, Shaman A, Gupta S. The effects of oxidative stress on female reproduc-tion: a review. Reprod Biol Endocrinol 2012; 10: 49.
54. Correa A, Gray RH, Cohen R, Rothman N, Shah F, Seacat H, et al. Ethylene glycol ethers and risks of spontaneous abortionand subfertility. Am J Epidemiol 1996; 143: 707-17.
55. Wang Q, Cao Z, Qu Y, Peng X, Guo S, Chen L. Residentialexposure to 50 Hz magnetic fields and the association withmiscarriage risk: a 2-year prospective cohort study. PLoS One2013; 8: e82113.
56. Stern JJ, Dorfmann AD, Gutierrez-Najar AJ, Cerrillo M, Cou-lam CB. Frequency of abnormal karyotypes among abortusesfrom women with and without a history of recurrent sponta-neous abortion. Fertil Steril 1996; 65: 250-3.
57. Stephenson MD, Sierra S. Reproductive outcomes in recur-rent pregnancy loss associated with a parental carrierof a structural chromosome rearrangement. Hum Reprod2006; 21: 1076-82.
58. Carp H, Feldman B, Oelsner G, Schiff E. Parental karyotypeand subsequent live births in recurrent miscarriage. FertilSteril 2004; 81: 1296-301.
59. Jauniaux E, Farquharson RG, Christiansen OB, Exalto N. Evidence-based guidelines for the investigation and medi-cal treatment of recurrent miscarriage. Hum Reprod2006; 21: 2216-22.
60. Redline RW, Zaragoza M, Hassold T. Prevalence of develop-mental and inflammatory lesions in nonmolar first trimesterspontaneous abortions. Hum Pathol 1999; 30: 93-100.
61. Benet J, Oliver-Bonet M, Cifuentes P, Templado C, Navarro J. Segregation of chromosomes in sperm of reciprocaltranslocation carriers: a review. Cytogenet Genome Res2005; 111: 281-90.
62. Ferfouri F, Selva J, Boitrelle F, Gomes DM, Torre A, Albert M, et al. The chromosomal risk in sperm from hetero-zygous Robertsonian translocation carriers is related tothe sperm count and the translocation type. Fertil Steril2012; 96: 1337-43.
63. Morel F, Laudier B, Guerif F, Couet ML, Royere D, Roux C, et al. Meiotic segregation analysis in spermatozoa of pericen-tric inversion carriers using fluorescence in situ hybridization. Hum Reprod 2007; 22: 136-41.
64. Pellestor F, Anahory T, Lefort G, Puechberty J, Liehr T, Hedon B, et al. Complex chromosomal rearrangements: origin andmeiotic behavior. Hum Reprod Update 2012; 17: 476-94.
65. De Braekeleer M, Dao TN. Cytogenetic studies in male infer-tility: a review. Hum Reprod 1991; 6: 245-50.
66. Gardner R, Sutherland G. Chromosome abnormalities andgenetic counselling. 2nd ed. Oxford: Oxford University Press; 1996.
67. Franssen MT, Korevaar JC, Leschot NJ, Bossuyt PM, Knegt AC, Gerssen-Schoorl KB, et al. Selective chromosome analysis incouples with two or more miscarriages: case-control study. BMJ 2005; 331: 137-41.
68. Franssen MT, Korevaar JC, van der Veen F, Leschot NJ, Bos-Suyt PM, Goddijn M. Reproductive outcome after chromosomeanalysis in couples with two or more miscarriages: index[corrected]-control study. BMJ 2006; 332: 759-63.
69. Greer IA. Thrombophilia: implications for pregnancy out-come. Thromb Res 2003; 109: 73-81.
70. Rees DC, Cox M, Clegg JB. World distribution of factor V Lei-den. Lancet 1995; 346: 1133-4.
71. Rosendaal FR. Venous thrombosis: prevalence and interactionof risk factors. Haemostasis 1999; 29: 1-9.
72. Bennett SA, Bagot CN, Arya R. Pregnancy loss and thrombo-philia: the elusive link. Br J Haematol 2012; 157: 529-42.
73. Peng F, Labelle LA, Rainey BJ, Tsongalis GJ. Single nucleotidepolymorphisms in the methylenetetrahydrofolate reductasegene are common in US Caucasian and Hispanic Americanpopulations. Int J Mol Med 2001; 8: 509-11.
74. Rey E, Kahn SR, David M, Shrier I. Thrombophilic disorders andfetal loss: a meta-analysis. Lancet 2003; 361: 901-8.
75. Cao Y, Xu J, Zhang Z, Huang X, Zhang A, Wang J, et al. Asso-ciation study between methylenetetrahydrofolate reductasepolymorphisms and unexplained recurrent pregnancy loss: ameta-analysis. Gene 2013; 514: 105-11.
76. Baumann K, Beuter-Winkler P, Hackethal A, Strowitzki T, Toth B, Bohlmann MK. Maternal factor V Leiden and prothrombinmutations do not seem to contribute to the occurrence oftwo or more than two consecutive miscarriages in Caucasianpatients. Am J Reprod Immunol 2013; 70: 518-21.
77. Cao Y, Zhang Z, Xu J, Wang J, Yuan W, Shen Y, et al. Gene-tic association studies of endothelial nitric oxide synthasegene polymorphisms in women with unexplained recurrentpregnancy loss: a systematic and meta-analysis. Mol Biol Rep2014; 41: 3981-9.
78. Nair RR, Khanna A, Singh K. Association of GSTT1 andGSTM1 polymorphisms with early pregnancy loss in an Indianpopulation and a meta-analysis. Reprod Biomed Online2013; 26: 313-22.
79. Tang W, Zhou X, Chan Y, Wu X, Luo Y. p53 codon 72 polymor-phism and recurrent pregnancy loss: a meta-analysis. J AssistReprod Genet 2011; 28: 965-9.
80. Su MT, Lin SH, Chen YC. Genetic association studies ofangiogenesis- and vasoconstriction-related genes in womenwith recurrent pregnancy loss: a systematic review and meta-analysis. Hum Reprod Update 2011; 17: 803-12.
81. Li J, Chen Y, Wu H, Li L, Apolipoprotein E. (Apo E) gene poly-morphisms and recurrent pregnancy loss: a meta-analysis. JAssist Reprod Genet 2014; 31: 139-48.
82. Yang C, Fangfang W, Jie L, Yanlong Y, Jie W, Xuefei L, et al. Angiotensin-converting enzyme insertion/deletion (I/D) poly-morphisms and recurrent pregnancy loss: a meta-analysis. JAssist Reprod Genet 2013; 29: 1167-73.
83. Wang Z, Wang P, Wang X, He X, Wang Z, Xu D, et al. Signi-ficant association between angiotensin-converting enzymegene insertion/deletion polymorphism and risk of recurrentmiscarriage: a systematic review and meta-analysis. Metabo-lism 2013; 62: 1227-38.
84. Hatakeyama C, Anderson CL, Beever CL, Penaherrera MS, Brown CJ, Robinson WP. The dynamics of X-inactivation ske-wing as women age. Clin Genet 2004; 66: 327-32.
85. Knudsen GP, Pedersen J, Klingenberg O, Lygren I, Orstavik KH. Increased skewing of X-chromosome inactivation withage in both blood and buccal cells. Cytogenet Genome Res2007; 116: 24-8.
86. Su MT, Lin SH, Chen YC. Association of sex hormonereceptor gene polymorphisms with recurrent pregnancyloss: a systematic review and meta-analysis. Fertil Steril2011; 96: 1435-44 [e1].
87. Pasquier E, Bohec C, De Saint Martin L, Le Marechal C, LeMartelot MT, Roche S, et al. Strong evidence that skewedX-chromosome inactivation is not associated with recurrentpregnancy loss: an incident paired case-control study. HumReprod 2007; 22: 2829-33.
88. Hogge WA, Prosen TL, Lanasa MC, Huber HA, Reeves MF. Recur-rent spontaneous abortion and skewed X-inactivation: is therean association? Am J Obstet Gynecol 2007; 196: 384 [e1-6; discussion 384 e6-8].
89. Vialard F, Hammoud I, Molina-Gomes D, Wainer R, Bergere M, Albert M, et al. Gamete cytogenetic study in couples withimplantation failure: aneuploidy rate is increased in bothcouple members. J Assist Reprod Genet 2008; 25: 539-45.
90. Ferfouri F, Clement P, Gomes DM, Minz M, Amar E, SelvaJ, et al. Is classic pericentric inversion of chromosome 2inv(2)(p11q13) associated with an increased risk of unbalan-ced chromosomes? Fertil Steril 2009; 92: 1497 [e1-4].
91. Pereza N, Crnjar K, Buretic-Tomljanovic A, Volk M, Kapovic M, Peterlin B, et al. Y chromosome azoospermia factor regionmicrodeletions are not associated with idiopathic recurrentspontaneous abortion in a Slovenian population: associationstudy and literature review. Fertil Steril 2013; 99: 1663-7.
92. Nizard J, Guettrot-Imbert G, Plu-Bureau G, Ciangura C, Jac-queminet S, Leenhardt L, et al. Pathologies maternelleschroniques et pertes de grossesse. J Gynecol Obstet BiolReprod 2014, http://dx.doi.org/10.1016/j.jgyn.2014.09.017[in press].
93. Heijnen EM, Eijkemans MJ, Hughes EG, Laven JS, Macklon NS, Fauser BC. A meta-analysis of outcomes of conventional IVF inwomen with polycystic ovary syndrome. Hum Reprod Update2006; 12: 13-21.
94. Capri E. Health and fertility in World Health Organiza-tion group 2 anovulatory women. Hum Reprod Update2012; 18: 586-99.
95. Koivunen R, Pouta A, Franks S, Martikainen H, Sovio U, Har-tikainen AL, et al. Fecundability and spontaneous abortionsin women with self-reported oligo-amenorrhea and/or hirsu-tism: Northern Finland Birth Cohort 1966 Study. Hum Reprod2008; 23: 2134-9.
96. Hirahara F, Andoh N, Sawai K, Hirabuki T, Uemura T, Minagu-Chi H. Hyperprolactinemic recurrent miscarriage and resultsof randomized bromocriptine treatment trials. Fertil Steril1998; 70: 246-52.
97. Negro R, Schwartz A, Gismondi R, Tinelli A, Mangieri T, Stagnaro-Green A. Universal screening versus case findingfor detection and treatment of thyroid hormonal dysfunc-tion during pregnancy. J Clin Endocrinol Metab 2010; 95: 1699-707.
98. Cleary-Goldman J, Malone FD, Lambert-Messerlian G, SullivanL, Canick J, Porter TF, et al. Maternal thyroid hypofunctionand pregnancy outcome. Obstet Gynecol 2008; 112: 85-92.
99. Bernardi LA, Cohen RN, Stephenson MD. Impact of subclini-cal hypothyroidism in women with recurrent early pregnancyloss. Fertil Steril 2013; 100: 1326-31.
100. Stagnaro-Green A, Abalovich M, Alexander E, Azizi F, Mest-man J, Negro R, et al. Guidelines of the American ThyroidAssociation for the diagnosis and management of thy-roid disease during pregnancy and postpartum. Thyroid2011; 21: 1081-125.
101. Hollowell JG, Staehling NW, Flanders WD, Hannon WH, Gunter EW, Spencer CA, et al. Serum TSH, T(4), and thyroid antibo-dies in the United States population (1988 to 1994): NationalHealth and Nutrition Examination Survey (NHANES III). J ClinEndocrinol Metab 2002; 87: 489-99.
102. van den Boogaard E, Vissenberg R, Land JA, van Wely M, vander Post JA, Goddijn M, et al. Significance of (sub)clinicalthyroid dysfunction and thyroid autoimmunity before concep-tion and in early pregnancy: a systematic review. Hum ReprodUpdate 2011; 17: 605-19.
103. Thangaratinam S, Tan A, Knox E, Kilby MD, Franklyn J, Cooma-rasamy A. Association between thyroid autoantibodies andmiscarriage and preterm birth: meta-analysis of evidence. BMJ 2011; 342: d2616.
104. Norman RJ. Editorial: Metformin-comparison with othertherapies in ovulation induction in polycystic ovary syndrome. J Clin Endocrinol Metab 2004; 89: 4797-800.
105. Clark AM, Ledger W, Galletly C, Tomlinson L, Blaney F, WangX, et al. Weight loss results in significant improvement in pre-gnancy and ovulation rates in anovulatory obese women. HumReprod 1995; 10: 2705-12.
106. Clark AM, Thornley B, Tomlinson L, Galletley C, Norman RJ. Weight loss in obese infertile women results in improvementin reproductive outcome for all forms of fertility treatment. Hum Reprod 1998; 13: 1502-5.
107. Marceau P, Kaufman D, Biron S, Hould FS, Lebel S, Marceau S, et al. Outcome of pregnancies after biliopancreatic diversion. Obes Surg 2004; 14: 318-24.
108. Gindler J, Li Z, Berry RJ, Zheng J, Correa A, Sun X, et al. Folicacid supplements during pregnancy and risk of miscarriage. Lancet 2001; 358: 796-800.
109. Centers for Disease Control (CDC). Use of folic acid for pre-vention of spina bifida and other neural tube defects -1983-1991. MMWR Morb Mortal Wkly Rep 1991; 40: 513-6.
110. Berry RJ, Li Z, Erickson JD, Li S, Moore CA, Wang H, et al. Prevention of neural tube defects with folic acid in China. China-US Collaborative Project for Neural Tube Defect Pre-vention. N Engl J Med 1999; 341: 1485-90.
111. Quere I, Mercier E, Bellet H, Janbon C, Mares P, Gris JC. Vita-min supplementation and pregnancy outcome in women withrecurrent early pregnancy loss and hyperhomocysteinemia. Fertil Steril 2001; 75: 823-5.
112. Amin AF, Shaaban OM, Bediawy MA. N-acetyl cysteine fortreatment of recurrent unexplained pregnancy loss. ReprodBiomed Online 2008; 17: 722-6.
113. Rai R, Backos M, Baxter N, Chilcott I, Regan L. Recur-rent miscarriage-an aspirin a day? Hum Reprod 2000; 15: 2220-3.
114. Kaandorp SP, Goddijn M, van der Post JA, Hutten BA, Verhoeve HR, Hamulyak K, et al. Aspirin plus heparin or aspirinalone in women with recurrent miscarriage. N Engl J Med2010; 362: 1586-96.
115. Di Nisio M, Peters L, Middeldorp S. Anticoagulants for thetreatment of recurrent pregnancy loss in women withoutantiphospholipid syndrome. Cochrane Database Syst Rev2005: CD004734.
116. Tulppala M, Marttunen M, Soderstrom-Anttila V, Foudila T, Ailus K, Palosuo T, et al. Low-dose aspirin in preventionof miscarriage in women with unexplained or autoimmunerelated recurrent miscarriage: effect on prostacyclin andthromboxane A2 production. Hum Reprod 1997; 12: 1567-72.
117. De Jong PG, Kaandorp S, Di Nisio M, Goddijn M, Middeldorp S. Aspirin and/or heparin for women with unexplained recur-rent miscarriage with or without inherited thrombophilia. Cochrane Database Syst Rev 2014; 7: CD004734.
118. Carp H, Dolitzky M, Inbal A. Thromboprophylaxis improvesthe live birth rate in women with consecutive recurrent mis-carriages and hereditary thrombophilia. J Thromb Haemost2003; 1: 433-8.
119. Brenner B, Bar J, Ellis M, Yarom I, Yohai D, Samueloff A. Effects of enoxaparin on late pregnancy complications andneonatal outcome in women with recurrent pregnancy lossand thrombophilia: results from the Live-Enox study. FertilSteril 2005; 84: 770-3.
120. Bouvier S, Cochery-Nouvellon E, Lavigne-Lissalde G, MercierE, Fabbro-Peray P, Balducchi JP, et al. Comparative incidenceof pregnancy outcomes in thrombophilia-positive women fromthe NOH-APS observational study. Blood 2014; 123: 414-21.
121. Rodger MA, Hague WM, Kingdom J, Kahn SR, Karo-vitch A, Sermer M, et al. Antepartum dalteparin versusno antepartum dalteparin for the prevention of pre-gnancy complications in pregnant women with thrombophilia(TIPPS): a multinational open-label randomised trial. Lancet2014, http://dx.doi.org/10.1016/S0140-6736(14)60793-5 [inpress].
122. Clark P, Walker ID, Langhorne P, Crichton L, Thomson A, Greaves M, et al. SPIN (Scottish Pregnancy Intervention)study: a multicenter, randomized controlled trial of low-molecular-weight heparin and low-dose aspirin in women withrecurrent miscarriage. Blood 2010; 115: 4162-7.
123. Rai R, Cohen H, Dave M, Regan L. Randomised controlled trialof aspirin and aspirin plus heparin in pregnant women withrecurrent miscarriage associated with phospholipid antibo-dies (or antiphospholipid antibodies). BMJ 1997; 314: 253-7.
124. Mak A, Cheung MW, Cheak AA, Ho RC. Combination of hepa-rin and aspirin is superior to aspirin alone in enhancing livebirths in patients with recurrent pregnancy loss and positiveantiphospholipid antibodies: a meta-analysis of randomizedcontrolled trials and meta-regression. Rheumatology (Oxford)2010; 49: 281-8.
125. Clark CA, Spitzer KA, Laskin CA, Crowther MR, Ginsberg JS. Heparin treatment in antiphospholipid syndrome with recur-rent pregnancy loss. Obstet Gynecol 2010; 116: 997-8 [authorreply 998].
126. Visser J, Ulander VM, Helmerhorst FM, Lampinen K, Morin-Papunen L, Bloemenkamp KW, et al. Thromboprophylaxis forrecurrent miscarriage in women with or without thrombo-philia. HABENOX: a randomised multicentre trial. ThrombHaemost 2011; 105: 295-301.
127. Laskin CA, Bombardier C, Hannah ME, Mandel FP, RitchieJW, Farewell V, et al. Prednisone and aspirin in women withautoantibodies and unexplained recurrent fetal loss. N Engl JMed 1997; 337: 148-53.
128. Ata B, Tan SL, Shehata F, Holzer H, Buckett W. A systematicreview of intravenous immunoglobulin for treatment of unex-plained recurrent miscarriage. Fertil Steril 2011; 95: 1080-5[e1-2].
129. Vaquero E, Lazzarin N, De Carolis C, Valensise H, Moretti C, Ramanini C. Mild thyroid abnormalities and recurrent sponta-neous abortion: diagnostic and therapeutical approach. Am JReprod Immunol 2000; 43: 204-8.
130. Vissenberg R, van den Boogaard E, van Wely M, van der PostJA, Fliers E, Bisschop PH, et al. Treatment of thyroid disor-ders before conception and in early pregnancy: a systematicreview. Hum Reprod Update 2012; 18: 360-73.
131. Rosenfeld H, Ornoy A, Shechtman S, Diav-Citrin O. Pregnancyoutcome, thyroid dysfunction and fetal goitre after in uteroexposure to propylthiouracil: a controlled cohort study. Br JClin Pharmacol 2009; 68: 609-17.
132. Di Gianantonio E, Schaefer C, Mastroiacovo PP, Cournot MP, Benedicenti F, Reuvers M, et al. Adverse effects of prenatalmethimazole exposure. Teratology 2001; 64: 262-6.
133. Phuapradit W, Saropala N, Rajatanavin R, Hotrakit S. Graves' disease complicating pregnancy. J Med Assoc Thai1993; 76: 380-4.
134. Haas DM, Ramsey PS. Progestogen for preventing miscarriage. Cochrane Database Syst Rev 2013; 10: CD003511.
135. El-Zibdeh MY. Dydrogesterone in the reduction of recur-rent spontaneous abortion. J Steroid Biochem Mol Biol2005; 97: 431-4.
136. Goldzieher JW. Double-blind trial of a progestin in habitualabortion. JAMA 1964; 188: 651-4.
137. Levine L. Habitual abortion. A controlled study of progesta-tional therapy. West J Surg Obstet Gynecol 1964; 72: 30-6.
138. Swyer GI, Daley D. Progesterone implantation in habitualabortion. Br Med J 1953; 1: 1073-7.
139. Carmichael SL, Shaw GM, Laurent C, Croughan MS, Olney RS, Lammer EJ. Maternal progestin intake and risk of hypospa-dias. Arch Pediatr Adolesc Med 2005; 159: 957-62.
140. Haas DM, Ramsey PS. Progestogen for preventing miscarriage. Cochrane Database Syst Rev 2008: CD003511.
141. Mastenbroek S, Twisk M, van der Veen F, Repping S. Preimplantation genetic screening: a systematic reviewand meta-analysis of RCTs. Hum Reprod Update 2011; 17: 454-66.
142. Harper JC, Wilton L, Traeger-Synodinos J, Goossens V, Moutou C, SenGupta SB, et al. The ESHRE PGD Consortium: 10 yearsof data collection. Hum Reprod Update 2012; 18: 234-47.
143. Franssen MT, Musters AM, van der Veen F, Repping S, Les-chot NJ, Bossuyt PM, et al. Reproductive outcome after PGDin couples with recurrent miscarriage carrying a structuralchromosome abnormality: a systematic review. Hum ReprodUpdate 2011; 17: 467-75.
144. Hammoud I, Molina-Gomes D, Albert M, Bergere M, Bailly M, Wainer R, et al. Are zona pellucida laser drilling and polarbody biopsy safe for in vitro matured oocytes? J Assist ReprodGenet 2010; 27: 423-7.
145. Molina-Gomes D, Hammoud I, Bailly M, Bergere M, WainerR, Selva J, et al. Preconceptional diagnosis for Robertsoniantranslocation as an alternative to preimplantation geneticdiagnosis in two situations: a pilot study. J Assist Reprod Genet2009; 26: 113-7.
146. Budak E, Garrido N, Soares SR, Melo MA, Meseguer M, Pellicer A, et al. Improvements achieved in an oocyte dona-tion program over a 10-year period: sequential increase inimplantation and pregnancy rates and decrease in high-ordermultiple pregnancies. Fertil Steril 2007; 88: 342-9.
147. Jungheim ES, Schon SB, Schulte MB, DeUgarte DA, FowlerSA, Tuuli MG. IVF outcomes in obese donor oocyte reci-pients: a systematic review and meta-analysis. Hum Reprod2013; 28: 2720-7.
148. Christiansen OB, Nybo Andersen AM, Bosch E, Daya S, Delves PJ, Hviid TV, et al. Evidence-based investigationsand treatments of recurrent pregnancy loss. Fertil Steril2005; 83: 821-39.
149. Litta P, Spiller E, Saccardi C, Ambrosini G, Caserta D, Cosmi E. Resectoscope or Versapoint for hysteroscopic metroplasty. Int J Gynaecol Obstet 2008; 101: 39-42.
150. Agostini A, De Guibert F, Salari K, Crochet P, Bre-Telle F, Gamerre M. Adverse obstetric outcomes at termafter hysteroscopic metroplasty. J Minim Invasive Gynecol2009; 16: 454-7.
151. Sentilhes L, Sergent F, Berthier A, Catala L, Descamps P, Mar-Peau L. Uterine rupture following operative hysteroscopy. Gynecol Obstet Fertil 2006; 34: 1064-70.
152. Giacomucci E, Bellavia E, Sandri F, Farina A, Scagliarini G. Term delivery rate after hysteroscopic metroplasty in patientswith recurrent spontaneous abortion and T-shaped, arcuateand septate uterus. Gynecol Obstet Invest 2011; 71: 183-8.
153. Fernandez H, Garbin O, Castaigne V, Gervaise A, Levaillant JM. Surgical approach to and reproductive outcome aftersurgical correction of a T-shaped uterus. Hum Reprod2011; 26: 1730-4.
154. Ludwin A, Pitynski K, Ludwin I, Banas T, Knafel A. Two-and three-dimensional ultrasonography and sonohysterogra-phy versus hysteroscopy with laparoscopy in the differentialdiagnosis of septate, bicornuate, and arcuate uteri. J MinimInvasive Gynecol 2013; 20: 90-9.
155. Saravelos SH, Cocksedge KA, Li TC. Prevalence and diagnosisof congenital uterine anomalies in women with repro-ductive failure: a critical appraisal. Hum Reprod Update2008; 14: 415-29.
156. Ghi T, Casadio P, Kuleva M, Perrone AM, Savelli L, Giunchi S, et al. Accuracy of three-dimensional ultrasound in diagnosisand classification of congenital uterine anomalies. Fertil Steril2009; 92: 808-13.
157. Faivre E, Fernandez H, Deffieux X, Gervaise A, Frydman R, Levaillant JM. Accuracy of three-dimensional ultrasono-graphy in differential diagnosis of septate and bicornuateuterus compared with office hysteroscopy and pelvic magne-tic resonance imaging. J Minim Invasive Gynecol 2012; 19: 101-6.
158. Devroey P, Fauser BC, Diedrich K. Approaches to improve thediagnosis and management of infertility. Hum Reprod Update2009; 15: 391-408.
159. Dewailly D, Andersen CY, Balen A, Broekmans F, DilaverN, Fanchin R, et al. The physiology and clinical utilityof anti-Mullerian hormone in women. Hum Reprod Update2014; 20: 370-85.
160. Zhang B, Liu T, Wang Z. Association of tumor necrosis factor-alpha gene promoter polymorphisms (-308G/A, -238G/A) withrecurrent spontaneous abortion: a meta-analysis. Hum Immu-nol 2012; 73: 574-9.
161. Zhang B, Dai B, Zhang X, Wang Z. Vascular endothelial growthfactor and recurrent spontaneous abortion: a meta-analysis. Gene 2012; 507: 1-8.
162. Agrawal S, Parveen F, Faridi RM, Prakash S. Interleukin-1 genecluster variants and recurrent pregnancy loss among NorthIndian women: retrospective study and meta-analysis. ReprodBiomed Online 2012; 24: 342-51.
163. Su MT, Lin SH, Chen YC, Kuo PL. Genetic association studiesof ACE and PAI-1 genes in women with recurrent pregnancyloss: a systematic review and meta-analysis. Thromb Haemost2013; 109: 8-15.