The detrimental effect of smoking on female fertility and IVF success

Current Women's Health Reviews

Volumn 4, Issue 1, 2008, Pages 16-24

  Neal, Michael S ^a   Foster, Warren G ^a   Younglai, Edward V ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

Cumulus Oocyte Complex; DNA adduct; Nicotine; Oogenesis; Spermatogenesis

Indexed keywords

1,1 DICHLORO 2,2 BIS(4 CHLOROPHENYL)ETHYLENE; 2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; AROMATIC HYDROCARBON RECEPTOR; BENZO[A]PYRENE; CADMIUM; CALCIUM; CATECHOL METHYLTRANSFERASE; CHOLESTEROL MONOOXYGENASE (SIDE CHAIN CLEAVING); CIGARETTE SMOKE; CLOMIFENE CITRATE; COTININE; CYTOCHROME P450 1A1; CYTOCHROME P450 1A2; CYTOCHROME P450 1B1; ESTRADIOL; ESTROGEN RECEPTOR; FOLLITROPIN; GONADOTROPIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 1BETA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; MITOCHONDRIAL DNA; NICOTINE; POLYCHLORINATED BIPHENYL; POLYCYCLIC AROMATIC HYDROCARBON; PROGESTERONE; PROTEIN BAX; PROTEIN BCL 2; UNINDEXED DRUG; VON HIPPEL LINDAU PROTEIN;

AGE; CIGARETTE SMOKING; CUMULUS OOPHORUS; EMBRYO TRANSFER; EMBRYOTOXICITY; ENVIRONMENTAL EXPOSURE; EPIGENETICS; FEMALE INFERTILITY; FERTILIZATION IN VITRO; HEALTH HAZARD; HUMAN; INCIDENCE; INTRACYTOPLASMIC SPERM INJECTION; MENOPAUSE; MORBIDITY; MORTALITY; NIDATION; NONHUMAN; OOCYTE DEVELOPMENT; OOCYTE MATURATION; OOCYTE RETRIEVAL; OVARY FOLLICLE FLUID; OVULATION INDUCTION; OXIDATIVE STRESS; PASSIVE SMOKING; PATHOGENESIS; PREGNANCY; PREGNANCY OUTCOME; PREVALENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; RISK FACTOR; SMOKING; SMOKING HABIT; SPERMATOGENESIS; STEROIDOGENESIS;

EID: 47749146195     PISSN: 15734048     EISSN: None     Source Type: Journal    
DOI: 10.2174/157340408783572088     Document Type: Review

References (125)

1. Klonoff-Colien H, Natarajan L, Marrs R, Yee B. Effects of female and male smoking on success rates of IVF and gamete intra-Fallopian transfer. Hum Reprod 2001; 16: 1382-90.
2. Augood C, Duckitt K, Templeton AA. Smoking and female infertility: a systematic review and meta-analysis. Hum Reprod 1998; 13: 1532-39.
3. Seltzer V. Smoking as a risk factor in the health of women. Int J Gynaecol Obstet 2003; 82: 393-97.
4. Stillman RJ, Rosenberg MJ, Sachs BP. Smoking and reproduction. Fertil Steril 1986; 46: 545-66.
5. Vine MF, Tse CK, Hu P, Truong KY. Cigarette smoking and semen quality. Fertil Steril 1996; 65: 835-42.
6. Weisberg E. Smoking and reproductive health. Clin Reprod Fertil 1985; 3: 175-86.
7. Hughes EG, Brennan BG. Does cigarette smoking impair natural or assisted fecundity? Fertil Steril 1996; 66: 679-89.
8. Hughes EG, Yeo J, Claman P, et al. Cigarette smoking and the outcomes of in vitro fertilization: measurement of effect size and levels of action. Fertil Steril 1994; 62: 807-14.
9. Zenzes MT, Puy LA, Bielecki R. Immunodetection of benzo [a]pyrene adducts in ovarian cells of women exposed to cigarette smoke. Mol Hum Reprod 1998; 4: 159-65.
10. Jick H, Porter J. Relation between smoking and age of natural menopause. Report from the Boston Collaborative Drug Surveillance Program, Boston University Medical Center. Lancet 1977; 1: 1354-55.
11. Werler MM. Teratogen update: smoking and reproductive outcomes. Teratology 1997; 55: 382-88.
12. Van Voorhis BJ, Dawson JD, Stovall DW, Sparks AE, Syrop CH. The effects of smoking on ovarian function and fertility during assisted reproduction cycles. Obstet Gynecol 1996; 88: 785-91.
13. Coste J, Job-Spira N, Fernandez H. Increased risk of ectopic pregnancy with maternal cigarette smoking. Am J Public Health 1991; 81: 199-201.
14. Saraiya M, Berg CJ, Kendrick JS, Strauss LT, Atrash HK, Ahn YW. Cigarette smoking as a risk factor for ectopic pregnancy. Am J Obstet Gynecol 1998; 178: 493-98.
15. Stergachis A, Scholes D, Daling JR, Weiss NS, Chu J. Maternal cigarette smoking and the risk of tubal pregnancy. Am J Epidemiol 1991; 133: 332-37.
16. Joffe M, Key J, Best N, Keiding N, Scheike T, Jensen TK. Studying time to pregnancy by use of a retrospective design. Am J Epidemiol 2005; 162: 115-24.
17. Fredricsson B, Gilljam H. Smoking and reproduction. Short and long term effects and benefits of smoking cessation. Acta Obstet Gynecol Scand 1992; 71: 580-92.
18. Hull MG, North K, Taylor H, Farrow A, Ford WC. Delayed conception and active and passive smoking. The avon longitudinal study of pregnancy and childhood study team. Fertil Steril 2000; 74: 725-33.
19. Neal MS, Hughes EG, Holloway AC, Foster WG. Sidestream smoking is equally as damaging as mainstream smoking on IVF outcomes. Hum Reprod 2005; 20: 2531-35.
20. Neal MS, Zhu J, Holloway AC, Foster WG. Follicle growth is inhibited by benzo-[a]-pyrene, at concentrations representative of human exposure, in an isolated rat follicle culture assay. Hum Reprod 2007; 22: 961-67.
21. Zenzes MT, Wang P, Casper RF. Cigarette smoking may affect meiotic maturation of human oocytes. Hum Reprod 1995; 10: 3213-17.
22. Paszkowski T. [The influence of smoking on the estradiol level in the preovulatory follicular fluid]. Ginekol Pol 2001; 72: 989-92.
23. Sterzik K, Strehler E, De Santo M, et al. Influence of smoking on fertility in women attending an in vitro fertilization program. Fertil Steril 1996; 65: 810-14.
24. Xia P, Younglai EV. Relationship between steroid concentrations in ovarian follicular fluid and oocyte morphology in patients undergoing intracytoplasmic spemi injection (ICSI) treatment. J Reprod Fertil 2000; 118: 229-33.
25. Paszkowski T, Clarke RN, Hornstein MD. Smoking induces oxidative stress inside the Graafian follicle. Hum Reprod 2002; 17: 921-25.
26. Zenzes MT. Smoking and reproduction: gene damage to human gametes and embryos. Hum Reprod Update 2000; 6: 122-31.
27. Plachot M. Chromosomal abnormalities in oocytes. Mol Cell Endocrinol 2001; 183 Suppi 1: S59-63.
28. Rustemeier K, Stabbert R, Haussmann HJ, Roemer E, Carmines EL. Evaluation of the potential effects of ingredients added to cigarettes. Part 2: chemical composition of mainstream smoke. Food Chem Toxicol 2002; 40: 93-104.
29. Swauger JE, Steichen TJ, Murphy PA, Kinsler S. An analysis of the mainstream smoke chemistry of samples of the U.S. cigarette market acquired between 1995 and 2000. Regul Toxicol Pharmacol 2002; 35: 142-56.
30. Lodovici M, Akpan V, Evangelisti C, Dolara P. Sidestream tobacco smoke as the main predictor of exposure to polycyclic aromatic hydrocarbons. J Appl Toxicol 2004; 24: 277-81.
31. Staessen J, Yeoman WB, Fletcher AE, et al. Blood lead concentration, renal function, and blood pressure in London civil servants. Br J Ind Med 1990; 47: 442-47.
32. Varga B, Zsolnai B, Paksy K, Naray M, Ungvary G. Age dependent accumulation of cadmium in the human ovary. Reprod Toxicol 1993; 7: 225-28.
33. Telisman S, Jurasovic J, Pizent A, Cvitkovic P. Cadmium in the blood and seminal fluid of nonoccupationally exposed adult male subjects with regard to smoking habits. Int Arch Occup Environ Health 1997; 70: 243-48.
34. Smida AD, Valderrama XP, Agostini MC, Furlan MA, Chedrese J. Cadmium stimulates transcription of the cytochrome p450 side chain cleavage gene in genetically modified stable porcine granulosa cells. Biol Reprod 2004; 70: 25-31.
35. Massanyi P, Bardos L, Oppel K, et al. Distribution of cadmium in selected organs of mice: effects of cadmium on organ contents of retinoids and beta-carotene. Acta Physiol Hung 1999; 86: 99-104.
36. Kondoh M, Tasaki E, Araragi S, et al. Requirement of caspase and p38MAPK activation in zinc-induced apoptosis in human leukemia HL-60 cells. Eur J Biochem 2002; 269: 6204-11.
37. Benowitz NL. The use of biologic fluid samples in assessing tobacco smoke consumption. NIDA Res Monogr 1983; 48: 6-26.
38. Weiss T, Eckert A. Cotinine levels in follicular fluid and serum of IVF patients: effect on granulosa-luteal cell function in vitro. Hum Reprod 1989; 4: 482-85.
39. Zenzes MT, Reed TE, Wang P, Klein J. Cotinine, a major metabolite of nicotine, is detectable in follicular fluids of passive smokers in in vitro fertilization therapy. Fertil Steril 1996; 66: 614- 19.
40. Barbieri RL, Gochberg J, Ryan KJ. Nicotine, cotinine, and anabasine inhibit aromatase in human trophoblast in vitro. J Clin Invest 1986; 77: 1727-33.
41. Barbieri RL, McShane PM, Ryan KJ. Constituents of cigarette smoke inhibit human granulosa cell aromatase. Fertil Steril 1986; 46: 232-36.
42. Bodis J, Torok A, Tinneberg HF, Hanf V, Hamori M, Cledon P. Influence of serotonin on progesterone and estradiol secretion of cultured human granulosa cells. Fertil Steril 1992; 57: 1008-11.
43. Miceli F, Minici F, Tropea A, et al. Effects of nicotine on human luteal cells in vitro: a possible role on reproductive outcome for smoking women. Biol Reprod 2005; 72: 628-32.
44. Gocze PM, Freeman DA. Cytotoxic effects of cigarette smoke alkaloids inhibit the progesterone production and cell growth of cultured MA-10 Leydig tumor cells. Eur J Obstet Gynecol Reprod Biol 2000; 93: 77-83.
45. Kaiserman MJ, Rickert WS. Carcinogens in tobacco smoke: benzo[a]pyrene from Canadian cigarettes and cigarette tobacco. Am J Public Health 1992; 82: 1023-26.
46. Mattison DR, Nightingale MS, Shiromizu K. Effects of toxic substances on female reproduction. Environ Health Perspect 1983; 48: 43-52.
47. 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: 2192-98.
48. Cooper GS, Baird DD, Hulka BS, Weinberg CR, Savitz DA, Hughes CL, Jr. Follicle-stimulating hormone concentrations in relation to active and passive smoking. Obstet Gynecol 1995; 85: 407-11.
49. Sharara FI, Beatse SN, Leonardi MR, Navot D, Scott RT, Jr. Cigarette smoking accelerates the development of diminished ovarian reserve as evidenced by the clomiphene citrate challenge test. Fertil Steril 1994; 62: 257-62.
50. Weinberg CF, Wilcox AJ, Baird DD. Reduced fecundability in women with prenatal exposure to cigarette smoking. Am J Epidemiol 1989; 129: 1072-78.
51. Mattison DR, Singh H, Takizawa K, Thomford PJ. Ovarian toxicity of benzo(a)pyrene and metabolites in mice. RepTod Toxicol 1989; 3: 115-25.
52. Mattison DR, Thorgeirsson SS. Genetic differences in mouse ovarian metabolism of benzo [a]pyrene and oocyte toxicity. Biochem Pharmacol 1977; 26: 909-12.
53. Robles R, Morita Y, Mann KK, et al. 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: 450-53.
54. Tilly JL. Commuting the death sentence: how oocytes strive to survive. Nat Rev Mol Cell Biol 2001; 2: 838-48.
55. Vanderhyden BC, Armstrong DT. Role of cumulus cells and serum on the in vitro maturation, fertilization, and subsequent development of rat oocytes. Biol Reprod 1989; 40: 720-28.
56. Ball GD, Leibfried ML, Lenz RW, Ax RL, Bavister BD, First NL. Factors affecting successful in vitro fertilization of bovine follicular oocytes. Biol Reprod 1983; 28: 717-25.
57. Neal MS, Lim GE, Youngla EV, Holloway AC, Foster WG. Aromatase activity as a predictor of pregnancy potential. Int Congress Series 2004; 1271: 139-42.
58. Vrsanska S, Nagyova E, Mlynarcikova A, Fickova M, Kolena J. Components of cigarette smoke inhibit expansion of oocytecumulus complexes from porcine follicles. Physiol Res 2003; 52: 383-87.
59. Atef A, Francois P, Christian V, Marc-Andre S. The potential role of gap junction communication between cumulus cells and bovine oocytes during in vitro maturation. Mol Reprod Dev 2005; 71: 358-67.
60. Mori K, Noguchi M, Matsuo M, Nomata K, Suematsu T, Kanetake H. Decreased cellular membrane expression of gap junctional protein, connexin 43, in rat detrusor muscle with chronic partial bladder outlet obstruction. Urology 2005; 65: 1254-58.
61. Pattinson HA, Taylor PJ, Pattinson MH. The effect of cigarette smoking on ovarian function and early pregnancy outcome of in vitro fertilization treatment. Fertil Steril 1991; 55: 780-83.
62. Racowsky C, Kaufman ML. Nuclear degeneration and meiotic aberrations observed in human oocytes matured in vitro: analysis by light microscopy. Fertil Steril 1992; 58: 750-55.
63. Neal MS, Holloway AC, Hughes EG, Foster WG. The effect of sidestream and mainstream smoking on IVF outcomes. Annual meeting of the Canadian Fertility and Andrology Society. 2003.
64. Zenzes MT, Puy LA, Bielecki R. Immunodetection of cotinine protein in granulosa-lutein cells of women exposed to cigarette smoke. Fertil Steril 1997; 68: 76-82.
65. Zenzes MT, Puy LA, Bielecki R, Reed TE. Detection of benzo[a]pyrene diol epoxide-DNA adducts in embryos from smoking couples: evidence for transmission by spermatozoa. Mol Hum Reprod 1999; 5: 125-31.
66. Mooney LA, Santella RM, Covey L, et al. Decline of DNA damage and other biomarkers in peripheral blood following smoking cessation. Cancer Epidemiol Biomarkers Prev 1995; 4: 627-34.
67. Zenzes MT, Reed TE, Casper RF. Effects of cigarette smoking and age on the maturation of human oocytes. Hum Reprod 1997; 12: 1736-41.
68. Sbrana I, Puliti A, Seidel A, Glatt H, Turchi G. Induction of chromosomal aberrations and spindle disturbances in Chinese hamster epithelial liver cells in culture by pyrene and benzo[a]pyrene quinones. Mutagenesis 1995; 10: 505-12.
69. Jensen TK, Jorgensen N, Punab M, et al. Association of in utero exposure to maternal smoking with reduced semen quality and testis size in adulthood: a cross-sectional study of 1,770 young men from the general population in five European countries. Am J Epidemiol 2004; 159: 49-58.
70. Shi Q, Ko E, Barclay L, Hoang T, Rademaker A, Martin R. Cigarette smoking and aneuploidy in human sperm. Mol Reprod Dev 2001; 59: 417-21.
71. Fraga CG, Motchnik PA, Wyrobek AJ, Rempel DM, Ames BN. Smoking and low antioxidant levels increase oxidative damage to sperm DNA. Mutat Res 1996; 351: 199-203.
72. Shen HM, Chia SE, Ni ZY, New AL, Lee BL, Ong CN. Detection of oxidative DNA damage in human sperm and the association with cigarette smoking. Reprod Toxicol 1997; 11: 675-80.
73. Zenzes MT, Bielecki R, Reed TE. Detection of benzo(a)pyrene diol epoxide-DNA adducts in sperm of men exposed to cigarette smoke. Fertil Steril 1999; 72: 330-35.
74. Bernstein L, Pike MC, Lobo RA, Depue RH, Ross RK, Henderson BE. Cigarette smoking in pregnancy results in marked decrease in maternal hCG and oestradiol levels. Br J Obstet Gynaecol 1989; 96: 92-96.
75. Boyce A, Schwartz D, Hubert C, Cedard L, Dreyfus J. Smoking, human placental lactogen and birth weight. Br J Obstet Gynaecol 1975; 82: 964-67.
76. Mochizuki M, Maruo T, Masuko K, Ohtsu T. Effects of smoking on fetoplacental-maternal system during pregnancy. Am J Obstet Gynecol 1984; 149: 413-20.
77. Vidal JD, VandeVoort CA, Marcus CB, Lazarewicz NR, Conley AJ. In vitro exposure to environmental tobacco smoke induces CYP1B1 expression in human luteinized granulosa cells. Reprod Toxicol 2006; 22: 731-37.
78. Westhoff C, Gentile G, Lee J, Zacur H, Helbig D. Predictors of ovarian steroid secretion in reproductive-age women. Am J Epidemiol 1996; 144: 381-88.
79. Weigert M, Hofstetter G, Kaipl D, et al. The effect of smoking on oocyte quality and hormonal parameters of patients undergoing in vitro fertilization-embryo transfer. J Assist Reprod Genet 1999; 16: 287-93.
80. Shiverick KT, Salafia C. Cigarette smoking and pregnancy I: ovarian, uterine and placental effects. Placenta 1999; 20: 265-72.
81. Neri A, Eckerling B. Influence of smoking and adrenaline (epinephrine) on the uterotubal insufflation test (Rubin test). Fertil Steril 1969; 20: 818-28.
82. Raine-Fenning NJ, Campbell BK, Kendall NF, Clewes JS, Johnson IR. Quantifying the changes in endometrial vascularity throughout the normal menstrual cycle with three-dimensional power Doppler angiography. Hum Reprod 2004; 19: 330-38.
83. Soares SR, Simon C, Remohi J, Pellicer A. Cigarette smoking affects uterine receptiveness. Hum Reprod 2007; 22: 543-47.
84. Abluwalia IB, Grummer-Strawn L, Scanlon KS. Exposure to environmental tobacco smoke and birth outcome: increased effects on pregnant women aged 30 years or older. Am J Epidemiol 1997; 146: 42-47.
85. Ananth CV, Savitz DA, Luther ER. Maternal cigarette smoking as a risk factor for placental abruption, placenta previa, and uterine bleeding in pregnancy. Am J Epidemiol 1996; 144: 881-89.
86. Cnattingius S, Axelsson O, Eklund G, Lindmark G. Smoking, maternal age, and fetal growth. Obstet Gynecol 1985; 66: 449-52.
87. Economides D, Braithwaite J. Smoking, pregnancy and the fetus. J R Soc Health 1994; 114: 198-201.
88. Wang X, Tager IB, Van Vunakis H, Speizer FE, Hanrahan JP. Maternal smoking during pregnancy, urine cotinine concentrations, and birth outcomes. A prospective cohort study. Int J Epidemiol 1997; 26: 978-88.
89. Andres RL. The association of cigarette smoking with placenta previa and abruptio placentae. Semin Perinatol 1996; 20: 154-59.
90. Genbacev O, McMaster MT, Lazic J, et al. Concordant in situ and in vitro data show that maternal cigarette smoking negatively regulates placental cytotrophoblast passage through the cell cycle. Reprod Toxicol 2000; 14: 495-506.
91. Zdravkovic T, Genbacev O, McMaster MT, Fisher SJ. The adverse effects of maternal smoking on the human placenta: a review. Placenta 2005; 26 Suppl A: S81-86.
92. Genbacev O, Zhou Y, Ludlow JW, Fisher SJ. Regulation of human placental development by oxygen tension. Science 1997; 277: 1669-72.
93. Castro LC, Allen R, Ogunyemi D, Roll K, Platt LD. Cigarette smoking during pregnancy: acute effects on uterine flow velocity waveforms. Obstet Gynecol 1993; 81: 551-55.
94. Zbar B, Kaelin W, Maher E, Richard S. Third International Meeting on von Hippel-Lindau disease. Cancer Res 1999; 59: 2251-53.
95. Genbacev O, McMaster MT, Zdravkovic T, Fisher SJ. Disruption of oxygen-regulated responses underlies pathological changes in the placentas of women who smoke or who are passively exposed to smoke during pregnancy. Reprod Toxicol 2003; 17: 509-18.
96. Jeffrey AM, Weinstein IB, Jennette KW, et al. Structures of benzo(a)pyrene-nucleic acid adducts formed in human and bovine bronchial explants. Nature 1977; 269: 348-50.
97. Shamsuddin AK, Gan R. Immunocytochemical localization of benzo(a)pyrene-DNA adducts in human tissue. Hum Pathol 1988; 19: 309-15.
98. Cheek AO, McLachlan JA. Environmental hormones and the male reproductive system. J Androl 1998; 19: 5-10.
99. Sharpe RM. Hormones and testis development and the possible adverse effects of environmental chemicals. Toxicol Lett 2001; 120: 221-32.
100. Rowlands JC, Gustafsson JA. Aryl hydrocarbon receptor-mediated signal transduction. Crit Rev Toxicol 1997; 27: 109-34.
101. Gozgit JM, Nestor KM, Fasco MJ, Pentecost BT, Arcaro KF. Differential action of polycyclic aromatic hydrocarbons on endogenous estrogen-responsive genes and on a transfected estrogenresponsive reporter in MCF-7 cells. Toxicol Appl Pharmacol 2004; 196: 58-67.
102. Gonzalez FJ, Fernandez-Salguero P. The aryl hydrocarbon receptor: studies using the AHR-null mice. Drug Metab Dispos 1998; 26: 1194-98.
103. Safe SH. Modulation of gene expression and endocrine response pathways by 2,3,7,8-tetrachlorodibenzo-p-dioxin and related compounds. Pharmacol Ther 1995; 67: 247-81.
104. Pocar P, Fischer B, Klonisch T, Hombach-Klonisch S. Molecular interactions of the aryl hydrocarbon receptor and its biological and toxicological relevance for reproduction. Reproduction 2005; 129: 379-89.
105. Safe S, Wang F, Porter W, Duan R, McDougal A. Ah receptor agonists as endocrine disruptors: antiestrogenic activity and mechanisms. Toxicol Lett 1998; 102-103: 343-47.
106. Ohtake F, Takeyama K, Matsumoto T, et al. Modulation of oestrogen receptor signalling by association with the activated dioxin receptor. Nature 2003; 423: 545-50.
107. Kharat I, Saatcioglu F. Antiestrogenic effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin are mediated by direct transcriptional interference with the liganded estrogen receptor. Cross-talk between aryl hydrocarbon- and estrogen-mediated signaling. J Biol Chem 1996; 271: 10533-37.
108. Khan S, Barhoumi R, Burghardt R, Liu S, Kim K, Safe S. Molecular mechanism of inhibitory aryl hydrocarbon receptor-estrogen receptor/Sp1 cross talk in breast cancer cells. Mol Endocrinol 2006; 20: 2199-14.
109. Wehling M, Schultz A, Losel R. To be or not to be (a receptor). Steroids 2007; 72: 107-10.
110. Younglai EV, Kwan TK, Kwan CY, Lobb DK, Foster WG. Dichlorodiphenylchloroethylene elevates cytosolic calcium concentrations and oscillations in primary cultures of human granulosalutein cells. Biol Reprod 2004; 70: 1693-1700.
111. Younglai EV, Wu YJ, Kwan TK, Kwan CY. Non-genomic action of estradiol and progesterone on cytosolic calcium concentrations in primary cultures of human granulosa-lutein cells. Hum Reprod 2005; 20: 2383-90.
112. Matsuura I, Saitoh T, Tani E, et al. Evaluation of a two-generation reproduction toxicity study adding endpoints to detect endocrine disrupting activity using lindane. J Toxicol Sci 2005; 30 Spec No.: 135-61.
113. Titus-Ernstoff L, Troisi R, Hatch EE, et al. Menstrual and reproductive characteristics of women whose mothers were exposed in utero to diethylstilbestrol (DES). Int J Epidemiol 2006; 35: 862-68.
114. Herbst AL, Ulfelder H, Poskanzer DC. Adenocarcinoma of the vagina. Association of maternal stilbestrol therapy with tumor appearance in young women. N Engl J Med 1971; 284: 878-81.
115. Goldberg JM, Falcone T. Effect of diethylstilbestrol on reproductive function. Fertil Steril 1999; 72: 1-7.
116. Cook JD, Davis BJ, Cai SL, Barrett JC, Conti CJ, Walker CL. Interaction between genetic susceptibility and early-life environmental exposure determines tumor-suppressor-gene penetrance. Proc Natl Acad Sci U S A 2005; 102: 8644-49.
117. Anway MD, Skinner MK. Epigenetic transgenerational actions of endocrine disruptors. Endocrinology 2006; 147: S43-49.
118. Anway MD, Cupp AS, Uzumcu M, Skinner MK. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 2005; 308: 1466-69.
119. Shiota K, Yamada S. Assisted reproductive technologies and birth defects. Congenit Anom (Kyoto) 2005; 45: 39-43.
120. Maher ER, Afhan M, Barratt CL. Epigenctic risks related to assisted reproductive technologies: epigenetics, imprinting, ART and icebergs? Hum Reprod 2003; 18: 2508-11.
121. Maher ER. Imprinting and assisted reproductive technology. Hum Mol Genet 2005; 14 Spec No 1: R133-38.
122. Horsthemke B, Ludwig M. Assisted reproduction: the epigenetic perspective. Hum Reprod Update 2005; 11: 473-82.
123. Sepaniak S, Forges T, Gerard H, Foliguet B, Bene MC, Monnier-Barbarino P. The influence of cigarette smoking on human sperm quality and DNA fragmentation. Toxicology 2006; 223: 54-60.
124. DeMarini DM. Genotoxicity of tobacco smoke and tobacco smoke condensate: a review. Murat Res 2004; 567: 447-74.
125. McConnell JM, Petrie L. Mitochondrial DNA turnover occurs during preimplantation development and can be modulated by environmental factors. Reprod Biomed Online 2004; 9: 418-24.