Environmental and developmental origins of ovarian reserve

Human Reproduction Update

Volumn 20, Issue 3, 2014, Pages 353-369

  Richardson, M C ^a   Guo, M ^a   Fauser, B C J M ^b   Macklon, N S ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Environmental; Nutrition; Ovarian reserve; Prenatal androgens; Socioeconomic

Indexed keywords

ANDROGEN; ANDROGEN RECEPTOR; ANDROSTANOLONE; AROMATIC HYDROCARBON RECEPTOR; CIGARETTE SMOKE; ESTRADIOL; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FOLLITROPIN; GENISTEIN; MUELLERIAN INHIBITING FACTOR; ORGANOCHLORINE DERIVATIVE; ORGANOCHLORINE PESTICIDE; PHTHALIC ACID; PLASTICIZER; RECEPTOR PROTEIN; TESTOSTERONE; TOBACCO SMOKE; VASCULOTROPIN RECEPTOR 1;

APOPTOSIS; ARTICLE; CELL PROLIFERATION; CELL VIABILITY; CLIMACTERIUM; DEVELOPMENTAL BIOLOGY; DOWN SYNDROME; EMBRYO DEVELOPMENT; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL FACTOR; ESTROGEN ACTIVITY; FEMALE FERTILITY; FETUS DEVELOPMENT; GERMLINE STEM CELL; HORMONE SYNTHESIS; HUMAN; INFERTILITY THERAPY; INTRAUTERINE GROWTH RETARDATION; LOW BIRTH WEIGHT; MATERNAL NUTRITION; MENOPAUSE; MENSTRUAL CYCLE; MENSTRUAL IRREGULARITY; NONHUMAN; OOCYTE; OOCYTE DEVELOPMENT; OOCYTE MATURATION; ORGANOGENESIS; OVARIAN RESERVE; OVARY FOLLICLE; OVARY INSUFFICIENCY; OVARY POLYCYSTIC DISEASE; PRENATAL EXPOSURE; PRENATAL GROWTH; PRIMORDIAL GERM CELL; PRIORITY JOURNAL; SEXUAL MATURITY; SMALL FOR DATE INFANT; SOCIAL STATUS; SOCIOECONOMICS; SPONTANEOUS ABORTION; STEROIDOGENESIS; UTERUS;

ENVIRONMENTAL; NUTRITION; OVARIAN RESERVE; PRENATAL ANDROGENS; SOCIOECONOMIC;

ANDROGENS; ENVIRONMENTAL EXPOSURE; FEMALE; FERTILITY; HUMANS; MENOPAUSE; OVARY; POLYCYSTIC OVARY SYNDROME; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PRENATAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; REPRODUCTION;

EID: 84898665859     PISSN: 13554786     EISSN: 14602369     Source Type: Journal    
DOI: 10.1093/humupd/dmt057     Document Type: Article

References (197)

1. Abbott DH, Barnett DK, Bruns CM, Dumesic DA. Androgen excess fetal programming of female reproduction: a developmental aetiology for polycystic ovary syndrome? Hum Reprod Update 2005;11:357-374.
2. Abbott DH, Padmanabhan V, Dumesic DA. Contributions of androgen and estrogen to fetal programming of ovarian dysfunction. Reprod Biol Endocrinol 2006;4:17.
3. doi:10.1186/1477-7827-4-17.
4. Abell A, Juul S, Bonde JPE. Time to pregnancy among female greenhouse workers. Scand JWork Environ Health 2000;26:131-136.
5. Akahoshi M, Soda M, Nakashima E, Tominaga T, Ichimaru S, Seto S, Yano K. The effects of body mass index on age at menopause. Int J Obes 2002;26:961-968.
6. Akkina JE, Reif JS, Keefe TJ, Bachand AM. Age at natural menopause and exposure to organochlorine pesticides in hispanic women. J Toxicol Environ Health A 2004; 67:1407-1422.
7. AmalfiS, Velez LM, Heber MF, Vighi S, Ferreira SR, Orozco A, Pignatar O, Motta AB. Prenatal Hyperandrogenization Induces Metabolic and Endocrine Alterations Which Depend on the Levels of Testosterone Exposure. PLoS one 2012;7:e37658.
8. Andersen HR, Vinggaard AM, Rasmussen TH, Gjermandsen IM, Bonefeld-Jorgensen EC. Effects of currently used pesticides in assays for estrogenicity, androgenicity, and aromatase activity in vitro. Toxicol Appl Pharmacol 2002;179:1-12.
9. Augood C, Duckitt K, Templeton AA. Smoking and female infertility: a systematic review and meta-analysis. Hum Reprod 1998;13:1532-1539.
10. Baird DD, Wilcox AJ. Future fertility after prenatal exposure to cigarette-smoke. Am J Epidemiol 1986;124:508-509.
11. Baker TG. Aquantitative and cytological study of germ cells in human ovaries. Proc R Soc Lond B Biol Sci 1963;158:417-433.
12. Barker DJP. The fetal and infant origins of disease. Eur J Clin Invest 1995;25:457-463.
13. Barnes RB, Rosenfield RL, Ehrmann DA, Cara JF, Cuttler L, Levitsky LL, Rosenthal IM. Ovarian hyperandrogynism as a result of congenital adrenal virilizing disorders- evidence for perinatal masculinization of neuroendocrine function in women. J Clin Endocrinol Metab 1994;79:1328-1333.
14. Basavarajappa MS, Hernandez-Ochoa I, Wang W, Flaws JA. Methoxychlor inhibits growth and induces atresia through the aryl hydrocarbon receptor pathway in mouse ovarian antral follicles. Reprod Toxicol 2012;34:16-21.
15. Baukloh V, Bohnet HG, Trapp M, Heeschen W, Feichtinger W, Kemeter P. Biocides in human follicular-fluid. Ann N Y Acad Sci 1985;442:240-250.
16. Beischlag TV, Morales JL, Hollingshead BD, Perdew GH. The aryl hydrocarbon receptor complex and the control of gene expression. Crit Rev Eukaryot Gene Expr 2008;18:207-250.
17. Brieno-Enriquez MA, Robles P, Camats-Tarruella N, Garcia-Cruz R, Roig I, Cabero L, Martinez F, Caldes MG. Human meiotic progression and recombination are affected by Bisphenol A exposure during in vitro human oocyte development. Hum Reprod 2011;26:2807-2818.
18. Broekmans FJ, KnauffEAH, Velde ERT, Macklon NS, Fauser BC. Female reproductive ageing: current knowledge and future trends. Trends Endocrinol Metab 2007; 18:58-65.
19. Broekmans FJ, Soules MR, Fauser BC. Ovarian aging: mechanisms and clinical consequences. Endocrine Reviews 2009;30:465-493.
20. Cabaton NJ, Wadia PR, Rubin BS, Zalko D, Schaeberle CM, Askenase MH, Gadbois JL, Tharp AP, Whitt GS, Sonnenschein C et al. perinatal exposure to environmentally relevant levels of bisphenol A decreases fertility and fecundity in CD-1 mice. Environ Health Perspect 2011;119:547-552.
21. Calafat AM, Kuklenyik Z, Reidy JA, Caudill SP, Ekong J, Needham LL. Urinary concentrations of bisphenol A and 4-nonylphenol in a human reference population. Environ Health Perspect 2005;113:391-395.
22. Can A, Semiz O, Cinar O. Bisphenol-A induces cell cycle delay and alters centrosome and spindle microtubular organization in oocytes during meiosis. Mol Hum Reprod 2005;11:389-396.
23. Canavez FS, Werneck GL, Parente RCM, Celeste RK, Faerstein E. The association between educational level and age at the menopause: a systematic review. Arch Gynecol Obstet 2011;283:83-90.
24. Castelo-Branco C, Palacios S, Mostajo D, Tobar C, von Helde S. Menopausal transition in Movima women, a Bolivian native-American. Maturitas 2005;51:380-385.
25. Chedrese PJ, Feyles F. The diverse mechanism of action of dichlorodiphenyldichloroethylene (DDE) and methoxychlor in ovarian cells in vitro. Reprod Toxicol 2001;15:693-698.
26. Chen Y, Jefferson WN, Newbold RR, Padilla-Banks E, Pepling ME. Estradiol, progesterone, and genistein inhibit oocyte nest breakdown and primordial follicle assembly in the neonatal mouse ovary in vitro and in vivo. Endocrinology 2007; 148:3580-3590.
27. Chen HS, Chiang PH, Wang YC, Kao MC, Shieh TH, Tsai CF, Tsai EM. Benzyl butyl phthalate induces necrosis by AhR mediation of CYP1B1 expression in human granulosa cells. Reprod Toxicol 2012;33:67-75.
28. Cimafranca MA, Davila J, Ekman GC, Andrews RN, Neese SL, Peretz J, Woodling KA, Helferich WG, Sarkar J, Flaws JA et al. Acute and chronic effects of oral genistein administration in neonatal mice. Biol Reprod 2010;83:114-121.
29. Cooper GS, Baird DD, Hulka BS, Weinberg CR, Savitz DA, Hughes CL. follicle-stimulating-hormone concentrations in relation to active and passive smoking. Obstet Gynecol 1995;85:407-411.
30. Crain DA, Janssen SJ, Edwards TM, Heindel J, Ho SM, Hunt P, Iguchi T, Juul A, McLachlan JA, Schwartz J et al. Female reproductive disorders: the roles of endocrine-disrupting compounds and developmental timing. Fertil Steril 2008; 90:911-940.
31. Crellin NK, Kang HG, Swan CL, Chedrese PJ. Inhibition of basal and stimulated progesterone synthesis by dichlorodiphenyldichloroethylene and methoxychlor in a stable pig granulosa cell line. Reproduction 2001;121:485-492.
32. Cresswell JL, Egger P, Fall CHD, Osmond C, Fraser RB, Barker DJP. Is the age of menopause determined in-utero? Early Hum Dev 1997;49:143-148.
33. Dandekar PV, Martin MC, Glass RH. Polyovular follicles associated with human invitro fertilization. Fertil Steril 1988;49:483-486.
34. DaSilva-Buttkus P, van den Hurk R, Velde ERT, Taverne MAM. Ovarian development in intrauterine growth-retarded and normally developed piglets originating from the same litter. Reproduction 2003;126:249-258.
35. de Bruin JP, Nikkels PGJ, Bruinse HW, van Haaften M, Looman CWN, te Velde ER. Morphometry of human ovaries in normal and growth-restricted fetuses. Early Hum Dev 2001;60:179-192.
36. Diamanti-Kandarakis E, Bourguignon JP, Giudice LC, Hauser R, Prins GS, Soto AM, Zoeller RT, Gore AC. Endocrine-disrupting chemicals: an endocrine society scientific statement. Endocr Rev 2009;30:293-342.
37. Dumesic DA, Schramm RD, Peterson E, Paprocki AM, Zhou R, Abbott DH. Impaired developmental competence of oocytes in adult prenatally androgenized female rhesus monkeys undergoing gonadotropin stimulation for in vitro fertilization. J Clin Endocrinol Metab 2002;87:1111-1119.
38. Dumesic DA, Patankar MS, Barnett DK, Lesnick TG, Hutcherson BA, Abbott DH. Early prenatal androgenization results in diminished ovarian reserve in adult female rhesus monkeys. Hum Reprod 2009;24:3188-3195.
39. Eichenlaub-Ritter U, Vogt E, Cukurcam S, Sun FY, Pacchierotti F, Parry J. Exposure of mouse oocytes to bisphenol A causes meiotic arrest but not aneuploidy. Mutat Res-Gen Tox En 2008;651:82-92.
40. Elias SG, van Noord PAH, Peeters PHM, den Tonkelaar I, Grobbee DE. Caloric restriction reduces age at menopause: the effect of the 1944-1945 Dutch famine. Menopause 2003;10:399-405.
41. El-Nemr A, Al-Shawaf T, Sabatini L, Wilson C, Lower AM, Grudzinskas JG. Effect of smoking on ovarian reserve and ovarian stimulation in in-vitro fertilization and embryo transfer. Hum Reprod 1998;13:2192-2198.
42. Eroschenko VP, Swartz WJ, Ford LC. Decreased superovulation in adult mice following neonatal exposures to technical methoxychlor. Reprod Toxicol 1997;11:807-814.
43. Faddy MJ, Gosden RG, Gougeon A, Richardson SJ, Nelson JF. Accelerated disappearance of ovarian follicles in midlife-implications for forecasting menopause. Hum Reprod 1992;7:1342-1346.
44. Ferreira RV, Gombar FM, Faria TD, Costa WS, Sampaio FJB, Ramos CD. Metabolic programming of ovarian angiogenesis and folliculogenesis by maternal malnutrition during lactation. Fertil Steril 2010;93:2572-2580.
45. Fowden AL, Giussani DA, Forhead AJ. Endocrine and metabolic programming during intrauterine development. Early Hum Dev 2005;81:723-734.
46. Freeman EW, Gracia CR, Sammel MD, Lin H, Lim LCL, Strauss JF. Association of anti-mullerian hormone levels with obesity in late reproductive-age women. Fertil Steril 2007;87:101-106.
47. Freour T, Masson D, Mirallie S, Jean M, Bach K, Dejoie T, Barriere P. Active smoking compromises IVF outcome and affects ovarian reserve. Reprod Biomed Online 2008;16:96-102.
48. Frisch RE. Body fat, menarche, fitness and fertility. Hum Reprod 1987;2:521-533.
49. Fuentes A, Munoz A, Barnhart K, Arguello B, Diaz M, Pommer R. Recent cigarette smoking and assisted reproductive technologies outcome. Fertil Steril 2010;93:89-95.
50. Fulton N, da Silva SJM, Bayne RAL, Anderson RA. Germ cell proliferation and apoptosis in the developing human ovary. J Clin Endocrinol Metab 2005;90:4664-4670.
51. Fuortes L, Clark MK, Kirchner HL, Smith EM. Association between female infertility and agricultural work history. Am J Ind Med 1997;31:445-451.
52. Gaido KW, Leonard LS, Maness SC, Hall JM, McDonnell DP, Saville B, Safe S. Differential interaction of the methoxychlor metabolite 2,2-bis-(p-hydroxyphenyl)- 1,1,1-trichlor with estrogen receptors alpha and beta. Endocrinology 1999; 140:5746-5753.
53. Gold EB. The timing of the age at which natural menopause occurs. Obstet Gynecol ClinN Am 2011;38:425-430.
54. Gold EB, Bromberger J, Crawford S, Samuels S, Greendale GA, Harlow SD, Skurnick J. Factors associated with age at natural menopause in a multiethnic sample of midlife women. Am J Epidemiol 2001;153:865-874.
55. Gougeon A. Frequent occurrence of multi-ovular follicles and multi-nuclear oocytes in the adult human-ovary. Fertil Steril 1981;35:417-422.
56. Grindler NM, Allsworth JE, Roehl KA, Cooper AR. Endocrine disrupting chemicals lead to earlier age at menopause: a cross-sectional study using the US population based NHANES database. Fertil Steril 2012;98:S31.
57. Hague WM, Adams J, Rodda C, Brook CGD, Debruyn R, Grant DB, Jacobs HS. The prevalence of polycystic ovaries in patients with congenital adrenal-hyperplasia and their close relatives. Clin Endocrinol 1990;33:501-510.
58. Hardy R, Kuh D. Does early growth influence timing of the menopause? Evidence from a British birth cohort. Hum Reprod 2002;17:2474-2479.
59. Hardy R, Mishra GD, Kuh D. Body mass index trajectories and age at menopause in a British birth cohort. Maturitas 2008;59:304-314.
60. Harlow BL, Signorello LB. Factors associated with early menopause. Maturitas 2000; 35:3-9.
61. Hart R, Sloboda DM, Doherty DA, Norman RJ, Atkinson HC, Newnham JP, Dickinson JE, Hickey M. Prenatal determinants of uterine volume and ovarian reserve in adolescence. J Clin Endocrinol Metab 2009;94:4931-4937.
62. Hatch EE, Troisi R, Wise LA, Hyer M, Palmer JR, Titus-ErnstoffL, Strohsnitter W, Kaufman R, Adam E, Noller KL et al. Age at natural menopause in women exposed to diethylstilbestrol in utero. Am J Epidemiol 2006;164:682-688.
63. He CY, Kraft P, Chen C, Buring JE, Pare G, Hankinson SE, Chanock SJ, Ridker PM, Hunter DJ, Chasman DI. Genome-wide association studies identify loci associated with age at menarche and age at natural menopause. Nat Genet 2009; 41:724-728.
64. Herbst AL, Cole P, Colton T, Robboy SJ, Scully RE. Age-incidence and risk of diethylstilbestrol-related clear cell adenocarcinoma of vagina and cervix. Am J Obst Gynecol 1977;128:43-50.
65. Hiroi H, Tsutsumi O, Momoeda M, Tatai Y, Osuga Y, Taketani Y. Differential interactions of bisphenol A and 17 beta-estradiol with estrogen receptor alpha (ER alpha) and ER beta. Endocr J 1999;46:773-778.
66. Hirshfield AN. Development of follicles in the mammalian ovary. Int Rev Cytol A Surv Cell Biol 1991;124:43-101.
67. Hoffmann D, Hoffmann I. The changing cigarette, 1950-1995. J Toxicol Environ Health 1997;50:307-364.
68. Holloway AC, Kellenberger LD, Petrik JJ. Fetal and neonatal exposure to nicotine disrupts ovarian function and fertility in adult female rats. Endocrine 2006; 30:213-216.
69. Horie K, Takakura K, Fujiwara H, Suginami H, Liao S, Mori T. Immunohistochemical localization of androgen receptor in the human ovary throughout the menstrual-cycle in relation to estrogen and progesterone-receptor expression. Hum Reprod 1992;7:184-190.
70. Hruska KS, Furth PA, Seifer DB, Sharara FI, Flaws JA. Environmental factors in infertility. Clin Obstet Gynecol 2000;43:821-829.
71. Hu YC, Wang PH, Yeh SY, Wang RS, Xie C, Xu QQ, Zhou XC, Chao HT, Tsai MY, Chang CS. Subfertility and defective folliculogenesis in female mice lacking androgen receptor. Proc Natl Acad Sci USA 2004;101:11209-11214.
72. Hudecova M, Holte J, Olovsson M, Sundstrom Poromaa I. Long-term follow-up of patients with polycystic ovary syndrome: reproductive outcome and ovarian reserve. Hum Reprod 2009;24:1176-1183.
73. Hughes EG, Brennan BG. Does cigarette smoking impair natural or assisted fecundity? Fertil Steril 1996;66:679-689.
74. Hughes FM, Gorospe WC. Biochemical-identification of apoptosis (programmed cell-death) in granulosa-cells-evidence for a potential mechanism underlying follicular atresia. Endocrinology 1991;129:2415-2422.
75. Hulten MA, Patel S, Jonasson J, Iwarsson E. On the origin of the maternal age effect in trisomy 21 Down syndrome: the Oocyte Mosaicism Selection model. Reproduction 2010;139:1-9.
76. Hunt PA, Koehler KE, Susiarjo M, Hodges CA, Ilagan A, Voigt RC, Thomas S, Thomas BF, Hassold TJ. Bisphenol A exposure causes meiotic aneuploidy in the female mouse. Curr Biol 2003;13:546-553.
77. Hunt PA, Lawson C, Gieske M, Murdoch B, Smith H, Marre A, Hassold T, Vandewoort CA. Bisphenol A alters early oogenesis and follicle formation in the fetal ovary of the rhesus monkey. Proc Natl Acad Sci 2012;109:17525-17530.
78. Ibanez L, Potau N, Enriquez G, de Zegher F. Reduced uterine and ovarian size in adolescent girls born small for gestational age. Pediatr Res 2000;47:575-577.
79. Ibanez L, Potau N, Ferrer A, Rodriguez-Hierro F, Marcos MV, de Zegher F. Reduced ovulation rate in adolescent girls born small for gestational age. J Clin Endocrinol Metab 2002a;87:3391-3393.
80. Ibanez L, Valls C, Cols M, Ferrer A, Marcos MV, de Zegher F. Hypersecretion of FSH in infant boys and girls born small for gestational age. J Clin Endocrinol Metab 2002b; 87:1986-1988.
81. Iguchi T, Fukazawa Y, Uesugi Y, Takasugi N. Polyovular follicles in mouse ovaries exposed neonatally to diethylstilbestrol invivo and invitro. Biol Reprod 1990; 43:478-484.
82. Ikezuki Y, Tsutsumi O, Takai Y, Kamei Y, Taketani Y. Determination of bisphenol A concentrations in human biological fluids reveals significant early prenatal exposure. Hum Reprod 2002;17:2839-2841.
83. Jarrell JF, Villeneuve D, Franklin C, Bartlett S, Wrixon W, Kohut J, Zouves CG. Contamination of Human Ovarian Follicular-Fluid and Serum by Chlorinated Organic-Compounds in 3 Canadian Cities. Can Med Assoc J 1993;148:1321-1327.
84. Jefferson WN, Couse JF, Padilla-Banks E, Korach KS, Newbold RR. Neonatal exposure to genistein induces estrogen receptor (ER)alpha expression and multioocyte follicles in the maturing mouse ovary: Evidence for ER beta-mediated and nonestrogenic actions. Biol Reprod 2002;67:1285-1296.
85. Jefferson WN, Padilla-Banks E, Goulding EH, Lao SPC, Newbold RR, Williams CJ. Neonatal exposure to genistein disrupts ability of female mouse reproductive tract to support preimplantation embryo development and implantation. Biol Reprod 2009;80:425-431.
86. Jefferson WN, Patisaul HB, Williams CJ. Reproductive consequences of developmental phytoestrogen exposure. Reproduction 2012;143:247-260.
87. Jensen TK, Henriksen TB, Hjollund NHI, Scheike T, Kolstad H, Giwercman A, Ernst E, Bonde JP, Skakkebaek NE, Olsen J. Adult and prenatal exposures to tobacco smoke as risk indicators of fertility among 430 Danish couples. Am J Epidemiol 1998; 148:992-997.
88. Jensen TK, Joffe M, Scheike T, Skytthe A, Gaist D, Petersen I, Christensen K. Early exposure to smoking and future fecundity among Danish twins. Int J Androl 2006; 29:603-613.
89. Joffe M, Barnes I. Doparental factors affect male and female fertility? Epidemiology 2000; 11:700-705.
90. Johnson J, Canning J, Kaneko T, Pru JK, Tilly JL. Germline stem cells and follicular renewal in the postnatal mammalian ovary. Nature 2004;428:145-150.
91. Jurisicova A, Tanauchi A, Li H. Maternal exposure to polycyclic aromatic hydrocarbons diminishes murine ovarian reserve via induction of Harakiri. J Clin Investig 2007; 117:3971-3978.
92. Kapur P, Sinha B, Pereira BMJ. Measuring climacteric symptoms and age at natural menopause in an Indian population using the Greene Climacteric Scale. Menopause 2009;16:378-384.
93. Kee K, Flores M, Cedars MI, Pera RAR. Human primordial germ cell formation is diminished by exposure to environmental toxicants acting through the AHR Signaling pathway. Toxicol Sci 2010;117:218-224.
94. Kerkhof GF, Leunissen RWJ, Willemsen RH, de Jong FH, Visser JA, Laven JSE, Hokken-Koelega ACS. Influence of preterm birth and small birth size on serum anti-Mullerian hormone levels in young adult women. Eur J Endocrinol 2010; 163:937-944.
95. Kim H, Nakajima T, Hayashi S, Chambon P, Watanabe H, Iguchi T, Sato T. Effects of diethylstilbestrol on programmed oocyte death and induction of polyovular follicles in neonatal mouse ovaries. Biol Reprod 2009;81:1002-1009.
96. Koch HM, Preuss R, Drexler H, Angerer J. Exposure of nursery school children and their parents and teachers to di-n-butylphthalate and butylbenzylphthalate. Int Arch Occup Environ Health 2005;78:223-229.
97. Kruger T, Long M, Bonefeld-Jorgensen EC. Plastic components affect the activation of the aryl hydrocarbon and the androgen receptor. Toxicology 2008;246:112-123.
98. Kuiper GGJM, Lemmen JG, Carlsson B, Corton JC, Safe SH, van der Saag PT, van der Burg P, Gustafsson JA. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 1998;139:4252-4263.
99. La Marca A, Broekmans FJ, Volpe A, Fauser BC, Macklon NS. Anti-Mullerian hormone (AMH): what do we still need to know? Hum Reprod 2009;24:2264-2275.
100. Lamb J, Bloom M, Vom saal F, Taylor J, Sandler J, Fujimoto V. Serum bisphenol A (BPA) and reproductive outcomes in couples undergoing IVF. Fertil Steril 2008;90:s186.
101. Lea RG, Andrade LP, Rae MT, Hannah LT, Kyle CE, Murray JF, Rhind SM, Miller DW. Effects of maternal undernutrition during early pregnancy on apoptosis regulators in the ovine fetal ovary. Reproduction 2006;131:113-124.
102. Lee C, Mishra G, Kuh D. Country of birth, country of residence, and menopausal transitions and symptoms: British birth cohort and Australian Longitudinal Study on Women's Health. Aust N Z J Public Health 2004;28:144-151.
103. Lem AJ, Boonstra VH, Renes JS, Breukhoven PE, de Jong FH, Laven JSE, Hokken-Koelega ACS. Anti-Mullerian hormone in short girls born small for gestational age and the effect of growth hormone treatment. Hum Reprod 2011; 26:898-903.
104. Lenie S, Cortvrindt R, Eichenlaub-Ritter U, Smitz J. Continuous exposure to bisphenol A during in vitro follicular development induces meiotic abnormalities. Mutat Res-Gen Tox En 2008;651:71-81.
105. Losa SM, Todd KL, Sullivan AW, Cao JY, Mickens JA, Patisaul HB. Neonatal exposure to genistein adversely impacts the ontogeny of hypothalamic kisspeptin signaling pathways and ovarian development in the peripubertal female rat. Reprod Toxicol 2011;31:280-289.
106. Lutterodt MC, Sorensen KP, Larsen KB, Skouby SO, Andersen CY, Byskov AG. The number of oogonia and somatic cells in the human female embryo and fetus in relation to whether or not exposed to maternal cigarette smoking. Hum Reprod 2009;24:2558-2566.
107. Macdonald PC, Edman CD, Hemsell DL, Porter JC, Siiteri PK. Effect of obesity on conversion of plasma androstenedione to estrone in post-menopausal women with and without endometrial cancer. Am J Obst Gynecol 1978;130:448-455.
108. Macklon N, Guo M, Richardson M. Smoking is associated with a reduced age of final pregnancy, consistent with a detrimental effect on ovarian reserve. Hum Reprod 2011;26(Suppl. 1):P-301.
109. Mark-Kappeler CJ, Hoyer PB, Devine PJ. Xenobiotic effects on ovarian preantral follicles. Biol Reprod Biol Reprod 2011;85:871-883.
110. Matikainen T, Perez GI, Jurisicova A, Pru JK, Schlezinger JJ, Ryu HY, Laine J, Sakai T, Korsmeyer SJ, Casper RF et al. Aromatic hydrocarbon receptor-driven Bax gene expression is required for premature ovarian failure caused by biohazardous environmental chemicals. Nat Genet 2001;28:355-360.
111. Matikainen TM, Moriyaia T, Morita Y, Perez GI, Korsmeyer SJ, Sherr DH, Tilly JL. Ligand activation of the aromatic hydrocarbon receptor transcription factor drives bax-dependent apoptosis in developing fetal ovarian germ cells. Endocrinology 2002;143:615-620.
112. Mattison DR. The effects of smoking on fertility from gametogenesis to implantation. Environ Res 1982;28:410-433.
113. Mattison DR. The mechanisms of action of reproductive toxins. Am J Ind Med 1983; 4:65-79.
114. Mattison DR, Shiromizu K, Nightingale MS. Oocyte destruction by polycyclic aromatic-hydrocarbons. Am J Ind Med 1983;4:191-202.
115. Mattison DR, Plowchalk DR, Meadows MJ, Miller MM, Malek A, London S. The effect of smoking on oogenesis, fertilization, and implantation. Semin Reprod Endocrinol 1989; 7:291-304.
116. McKnight KK, Wellons MF, Sites CK, Roth DL, Szychowski JM, Halanych JH, Cushman M, Safford MM. Racial and regional differences in age at menopause in the United States: findings from the REasons for Geographic And Racial Differences in Stroke (REGARDS) study. Am J Obst Gynecol 2011;205:353. e1-8.
117. McLachlan JA, Newbold RR, Shah HC, Hogan MD, Dixon RL. Reduced fertility in female mice exposed transplacentally to diethylstilbestrol (Des). Fertil Steril 1982; 38:364-371.
118. Mellembakken JR, Berga SL, Kilen M, Tanbo TG, Abyholm T, Fedorcsak P. Sustained fertility from 22 to 41 years of age in women with polycystic ovarian syndrome. Hum Reprod 2011;26:2499-2504.
119. Mizejewski GJ. Biological roles of alpha-fetoprotein during pregnancy and perinatal development. Exp Biol Med 2004;229:439-463.
120. Mlynarcikova A, Kolena J, Fickova M, Scsukova S. Alterations in steroid hormone production by porcine ovarian granulosa cells caused by bisphenol A and bisphenol A dimethacrylate. Mol Cell Endocrinol 2005;244:57-62.
121. Mok-Lin E, Ehrlich S, Williams PL, Petrozza J, Wright DL, Calafat AM, Ye X, Hauser R. Urinary bisphenol A concentrations and ovarian response among women undergoing IVF. Int J Androl 2010;33:385-393.
122. Morton MS, Arisaka O, Miyake N, Morgan LD, Evans BAJ. Phytoestrogen concentrations in serum from Japanese men and women over forty years of age. J Nutr 2002;132:3168-3171.
123. Mossa F, Carter F, Walsh SW, Kenny DA, Smith GW, Ireland JLH, Hildebrandt TB, Lonergan P, Ireland JJ, Evans ACO. Maternal undernutrition in cows impairs ovarian and cardiovascular systems in their offspring. Biol Reprod Advance Access published 20 February 2013, doi:10.1095/biolreprod 112.107235.
124. Motejlek K, Palluch F, Neulen J, Grummer R. Smoking impairs angiogenesis during maturation of human oocytes. Fertil Steril 2006;86:186-191.
125. Murdoch WJ, Van Kirk EA, Vonnahme KA, Ford SP. Ovarian responses to undernutrition in pregnant ewes. Reprod Biol Endocrinol 2003;1:6.
126. Nagel G, Altenburg HP, Nieters A, Boffetta P, Linseisen J. Reproductive and dietary determinants of the age at menopause in EPIC-Heidelberg. Maturitas 2005; 52:337-347.
127. Nikolaou D, Gilling-Smith C. Early ovarian ageing: are women with polycystic ovaries protected? Hum Reprod 2004;19:2175-2179.
128. Palacios S, Henderson VW, Siseles N, Tan D, Villaseca P. Age of menopause and impact of climacteric symptoms by geographical region. Climacteric 2010;13:419-428.
129. Palmer JR, Rosenberg L, Wise LA, Horton NJ, dams-Campbell LL. Onset of natural menopause in African American women. Am J Public Health 2003;93:299-306.
130. Pellatt L, Hanna L, Brincat M, Galea R, Brain H, Whitehead S, Mason H. Granulosa cell production of anti-Mullerian hormone is increased in polycystic ovaries. J Clin Endocrinol Metab J Clin Endocrinol Metab 2007;92:240-245.
131. Pepling ME. Follicular assembly: mechanisms of action. Reproduction 2012; 143:139-149.
132. Pepling ME, Spradling AC. Mouse ovarian germ cell cysts undergo programmed breakdown to form primordial follicles. Dev Biol 2001;234:339-351.
133. Perry JRB, Stolk L, Franceschini N, Lunetta KL, Zhai GJ, McArdle PF, Smith AV, Aspelund T, Bandinelli S, Boerwinkle E et al. Meta-analysis of genome-wide association data identifies two loci influencing age at menarche. Nat Genet 2009; 41:648-650.
134. Plante BJ, Cooper GS, Baird DD, Steiner AZ. The impact of smoking on antimullerian hormone levels in women aged 38 to 50 years. Menopause (New York) 2010; 17:571-576.
135. Pru JK, Kaneko-Tarui T, Jurisicova A, Kashiwagi A, Selesniemi K, Tilly JL. Induction of Proapoptotic Gene Expression and Recruitment of p53 Herald Ovarian Follicle Loss Caused by Polycyclic Aromatic Hydrocarbons. Reprod Sci 2009;16:347-356.
136. Rae MT, Palassio S, Kyle CE, Brooks AN, Lea RG, Miller DW, Rhind SM. Effect of maternal undernutrition during pregnancy on early ovarian development and subsequent follicular development in sheepfetuses. Reproduction 2001;122:915-922.
137. Rae MT, Kyle CE, Miller DW, Hammond AJ, Brooks AN, Rhind SM. The effects of undernutrition, in utero, on reproductive function in adult male and female sheep. Anim Reprod Sci 2002;72:63-71.
138. Rhind SM. Effects of maternal nutrition on fetal and neonatal reproductive development and function. Anim Reprod Sci 2004;82:169-181.
139. Richards M, Kuh D, Hardy R, Wadsworth M. Lifetime cognitive function and timing of the natural menopause. Neurology 1999;53:308-314.
140. Rivera OE, Varayoud J, Rodriguez HA, Munoz-de-Toro M, Luque EH. Neonatal exposure to bisphenol A or diethylstilbestrol alters the ovarian follicular dynamics in the lamb. Reprod Toxicol 2011;32:304-312.
141. Robles R, Morita Y, Mann KK, Perez GI, Yang S, Matikainen T, Sherr DH, Tilly JL. The aryl hydrocarbon receptor, a basic helix-loop-helix transcription factor of the PAS gene family, is required for normal ovarian germ cell dynamics in the mouse. Endocrinology 2000;141:450-453.
142. Rodriguez HA, Santambrosio N, Santamaria CG, Munoz-de-Toro M, Luque EH. Neonatal exposure to bisphenol A reduces the pool of primordial follicles in the rat ovary. Reprod Toxicol 2010;30:550-557.
143. Roy P, Salminen H, Koskimies P, Simola J, Smeds A, Saukko P, Huhtaniemi IT. Screening of some anti-androgenic endocrine disruptors using a recombinant cell-based in vitro bioassay. J Steroid Biochem Mol Biol 2004;88:157-166.
144. Sanderson JT, Seinen W, Giesy JP, van den Berg M. 2-chloro-s-triazine herbicides induce aromatase (CYP19) activity in H295R human adrenocortical carcinoma cells: A novel mechanism for estrogenicity? Toxicol Sci 2000;54:121-127.
145. Sanderson JT, Boerma J, Lansbergen GWA, van den Berg M. Induction and inhibition of aromatase (CYP19) activity by various classes of pesticides in H295R human adrenocortical carcinoma cells. Toxicol Appl Pharmacol 2002;182:44-54.
146. Santoro N, Lasley B, McConnell D, Allsworth J, Crawford S, Gold LB, Finkelstein JS, Greendale GA, Kelsey J, Korenman S et al. Body size and ethnicity are associated with menstrual cycle alterations in women in the early menopausal transition: the study of women's health across the nation (SWAN) daily hormone study. J Clin Endocrinol Metab 2004;89:2622-2631.
147. Schreuder M, de Waal HDV, van Wijk A. Consequences of intrauterine growth restriction for the kidney. Kidney Blood Press Res 2006;29:108-125.
148. Shanle EK, Xu W. Endocrine disrupting chemicals targeting estrogen receptor signaling: identification and mechanisms of action. Chem Res Toxicol 2011;24:6-19.
149. Sharara FI, Beatse SN, Leonardi MR, Navot D, Scott RT. Cigarette-smoking accelerates the development of diminished ovarian reserve as evidenced by the clomiphene citrate challenge test. Fertil Steril 1994;62:257-262.
150. Sharpe RM. Environmental/lifestyle effects on spermatogenesis. Philos Trans R Soc B Biol Sci 2010;365:1697-1712.
151. Shayeb A, Harrild K, Bhattacharya S. Birthweight and ovulatory dysfunction. Br J Obstet Gynaecol. Advance access published 20 May 2013, doi: 10.1111/1471-0528.12262 Shiverick KT, Salafia C. Cigarette smoking and pregnancy-I: ovarian, uterine and placental effects. Placenta 1999;20:265-272.
152. Silva MJ, Samandar E, Preau JL, Reidy JA, Needham LL, Calafat AM. Automated solid-phase extraction and quantitative analysis of 14 phthalate metabolites in human serum using isotope dilution-high-performance liquid chromatographytandem mass spectrometry. J Anal Toxicol 2005;29:819-824.
153. Sir-Petermann T, Maliqueo M, Angel B, Lara HE, Perez-Bravo F, Recabarren SE. Maternal serum androgens in pregnant women with polycystic ovarian syndrome: possible implications in prenatal androgenization. HumReprod 2002;17:2573-2579.
154. Skinner MK. Regulation of primordial follicle assembly and development. Hum Reprod Update 2005;11:461-471.
155. Smith P, Steckler TL, Veiga-Lopez A, Padmanabhan V. Developmental programming: differential effects of prenatal testosterone and dihydrotestosterone on follicular recruitment, depletion of follicular reserve, and ovarian morphology in sheep. Biol Reprod 2009;80:726-736.
156. Sonnenschein C, Soto AM. An updated review of environmental estrogen and androgen mimics and antagonists. J Steroid Biochem Mol Biol 1998;65:143-150.
157. Soto AM, Chung KL, Sonnenschein C. The pesticides endosulfan, toxaphene, and dieldrin have estrogenic effects on human estrogen-sensitive cells. Environ Health Perspect 1994;102:380-383.
158. Sotomayor-Zarate R, Tiszavari M, Cruz G, Lara HE. Neonatal exposure to single doses of estradiol or testosterone programs ovarian follicular development-modified hypothalamic neurotransmitters and causes polycystic ovary during adulthood in the rat. Fertil Steril 2011;96:1490-1496.
159. Souter I, Smith KW, Dimitriadis I, Keller MG, Petrozza JC, Hauser R. The association of urinary phthalate monoester concentrations with measures of ovarian reserve among patients undergoing fertility treatments. Fertil Steril 2011;96:S5.
160. Sowers MR, McConnell D, Yosef M, Jannausch ML, Harlow SD, Randolph JF. Relating smoking, obesity, insulin resistance, and ovarian biomarker changes to the final menstrual period. Reprod Aging 2010;1204:95-103.
161. Spandorfer SD, Kump L, Goldschlag D, Brodkin T, Davis OK, Rosenwaks Z. Obesity and in vitro fertilization-Negative influences on outcome. J Reprod Med 2004; 49:973-977.
162. Steckler T, Wang JR, Bartol FF, Roy SK, Padmanabhan V. Fetal programming: Prenatal testosterone treatment causes intrauterine growth retardation, reduces ovarian reserve and increases ovarian follicular recruitment. Endocrinology 2005;146: 3185-3193.
163. Steiner AZ, D'Aloisio AA, Deroo LA, Sandler DP, Baird DD. Association of intrauterine and early-life exposures with age at menopause in the sister study. Am J Epidemiol 2010;172:140-148.
164. Stolk L, Zhai G, van Meurs JBJ, Verbiest MMPJ, Visser JA, Estrada K, Rivadeneira F, Williams FM, Cherkas L, Deloukas P et al. Loci at chromosomes 13, 19 and 20 influence age at natural menopause. Nat Genet 2009;41:645-647.
165. Stolk L, Perry JRB, Chasman DI, He CY, Mangino M, Sulem P, Barbalic M, Broer L, Byrne EM, Ernst F et al. Meta-analyses identify 13 loci associated with age at menopause and highlight DNA repair and immune pathways. Nat Genet 2012; 44:260-268.
166. Strohsnitter WC, Hatch EE, Hyer M, Troisi R, Kaufman RH, Robboy SJ, Palmer JR, Titus-ErnstoffL, Anderson D, Hoover RN et al. The association between in utero cigarette smoke exposure and age at menopause. Am J Epidemiol 2008;167: 727-733.
167. Sugiura-Ogasawara M, Ozaki Y, Sonta SI, Makino T, Suzumori K. Exposure to bisphenol A is associated with recurrent miscarriage. Hum Reprod 2005; 20:2325-2329.
168. Sun L, Tan LJ, Yang F, Luo Y, Li X, Deng HW, Dvornyk V. Meta-analysis suggests that smoking is associated with an increased risk of early natural menopause. Menopause 2012;19:126-132.
169. Susiarjo M, Hassold TJ, Freeman E, Hunt PA. Bisphenol a exposure in utero disrupts early oogenesis in the mouse. Plos Genet 2007;3:e5.
170. Suzuki A, Sugihara A, Uchida K, Sato T, Ohta Y, Katsu Y, Watanabe H, Iguchi T. Developmental effects of perinatal exposure to bisphenol-A and diethylstilbestrol on reproductive organs in female mice. Reprod Toxicol 2002;16:107-116.
171. te Velde ER, Pearson PL. The variability of female reproductive ageing. Hum Reprod Update 2002;8:141-154.
172. Tiemann U. In vivo and in vitro effects of the organochlorine pesticides DDT, TCPM, methoxychlor, and lindane on the female reproductive tract of mammals: A review. Reprod Toxicol 2008;25:316-326.
173. Tom SE, Cooper R, Kuh D, Guralnik JM, Hardy R, Power C. Fetal environment and early age at natural menopause in a British birth cohort study. Hum Reprod 2010; 25:791-798.
174. Trapp M, Baukloh V, Bohnet HG, Heeschen W. Pollutants in human follicular-fluid. Fertil Steril 1984;42:146-148.
175. Treloar AE, Boynton RE, Behn B, Brown BW. Variation of the human menstrual cycle through reproductive life. Int J Fertil 1967;76:77-126.
176. Treloar SA, Sadrzadeh S, Do KA, Martin NG, Lambalk CB. Birth weight and age at menopause in Australian female twin pairs: exploration of the fetal origin hypothesis. Hum Reprod 2000;15:55-59.
177. Vandenberg LN, Maffini MV, Sonnenschein C, Rubin BS, Soto AM. Bisphenol-A and the great divide: a reviewof controversies in the field of endocrine disruption. Endocr Rev 2009;30:75-95.
178. van Noord PAH, Dubas JS, Dorland M, Boersma H, te Velde E. Age at natural menopause in a population-based screening cohort: the role of menarche, fecundity, and lifestyle factors. Fertil Steril 1997;68:95-102.
179. Vaskivuo TE, Anttonen M, Herva R, Billig H, Dorland M, te Velde ER, Stenback F, Heikinheimo M, Tapanainen JS. Survival of human ovarian follicles from fetal to adult life: Apoptosis, apoptosis-related proteins, and transcription factor GATA-4. J Clin Endocrinol Metab 2001;86:3421-3429.
180. Velez MP, Alvarado BE, Zunzunegui MV. Life course social adversity and age at menopause in women from Latin America and the Caribbean. Am J Epidemiol 2009;169:S75.
181. Voorhuis M, Onland-Moret NC, van der Schouw YT, Fauser BCJM, Broekmans FJ. Human studies on genetics of the age at natural menopause: a systematic review. Hum Reprod Update 2010;16:364-377.
182. Wallace WHB, Kelsey TW. Human ovarian reserve from conception to the menopause. Plos One 2010;5:e8772.
183. Wang H, Kazumichi A, Hagiwara H, Xiaowei L, Kikuchi N, Abe Y, Yamada K, Fatima R, Mizunuma H. Effect of adrenal and ovarian androgenson type 4 follicles unresponsive to FSH in immature mice. Endocrinology 2001;142:4930-4936.
184. Waylen AL, Metwally M, Jones GL, Wilkinson AJ, Ledger WL. Effects of cigarette smoking upon clinical outcomes of assisted reproduction: a meta-analysis. Hum Reprod Update 2009;15:31-44.
185. Webber LJ, Stubbs S, Stark J, Trew GH, Margara R, Hardy K, Franks S. Formation and early development of follicles in the polycystic ovary. Lancet 2003;362:1017-1021.
186. Webber LJ, Stubbs SA, Stark J, Margara RA, Trew GH, Lavery SA, Hardy K, Franks S. Prolonged survival in culture of preantral follicles from polycystic ovaries. J Clin Endocrinol Metab 2007;92:1975-1978.
187. Weinberg CR, Wilcox AJ, Baird DD. Reduced fecundability in women with prenatal exposure to cigarette-smoking. Am J Epidemiol 1989;129:1072-1078.
188. Wu XY, Li ZL, Wu CY, Liu YM, Lin H, Wang SH, Xiao WF. Endocrine traits of polycystic ovary syndrome in prenatally androgenized female Sprague-Dawley rats. Endocr J 2010;57:201-209.
189. Xita N, Tsatsoulis A. Review: fetal programming of polycystic ovary syndrome by androgen excess: evidence from experimental, clinical, and genetic association studies. J Clin Endocrinol Metab 2006;91:1660-1666.
190. Xu JP, Osuga Y, Yano T, Morita Y, Tang XH, Fujiwara T, Takai Y, Matsumi H, Koga K, Taketani Y et al. Bisphenol A induces apoptosis and G2-to-M arrest of ovarian granulosa cells. Biochem Biophys Res Commun 2002;292:456-462.
191. Younglai EV, Foster WG, Hughes EG, Trim K, Jarrell JF. Levels of environmental contaminants in human follicular fluid, serum, and seminal plasma of couples undergoing in vitro fertilization. Arch Environ Contam Toxicol 2002;43:121-126.
192. Younglai EV, Holloway AC, Lim GE, Foster WG. Synergistic effects between FSH and 1,1-dichloro-2,2-bis(P-chlorophenyl)ethylene (P, P'-DDE) on human granulosa cell aromatase activity. Hum Reprod 2004;19:1089-1093.
193. Yu YS, Sui HS, Han ZB, Li W, Luo MJ, Tan JH. Apoptosis in granulosa cells during follicular atresia: relationship with steroids and insulin-like growth factors. Cell Res 2004;14:341-346.
194. Zenzes MT, Reed TE, Casper RF. Effects of cigarette smoking and age on the maturation of human oocytes. Hum Reprod 1997;12:1736-1741.
195. Zhang S, Qin CH, Safe SH. Flavonoids as aryl hydrocarbon receptor agonists/antagonists: Effects of structure and cell context. Environ Health Perspect 2003; 111:1877-1882.
196. Zhou W, Liu HY, Liao LM, Han SP, Liu JY. Effect of bisphenol A on steroid hormone production in rat ovarian theca-interstitial and granulosa cells. Mold Cell Endocrinol 2008;283:12-18.
197. Zou K, Yuan Z, Yang ZJ, Luo HC, Sun KJ, Zhou L, Xiang J, Shi LJ, Yu QS, Zhang Y et al. Production of offspring from a germline stem cell line derived from neonatal ovaries. Nat Cell Biol 2009;11:631-636.