Occupational exposures to chemicals as a possible etiology in premature ovarian failure: A critical analysis of the literature

Reproductive Toxicology

Volumn 33, Issue 3, 2012, Pages 269-279

  Béranger, Rémi ^a   Hoffmann, Pascale ^b,c   Christin Maitre, Sophie ^d,e   Bonneterre, Vincent ^a,b,f  

^a LABORATOIRE TIMC IMAG   (France)

^b GRENOBLE UNIVERSITY HOSPITAL   (France)

^c UNIV GRENOBLE ALPES   (France)

^d HÔPITAL SAINT ANTOINE   (France)

^e Assistance publique Hôpitaux de Paris   (France)

^f French National Occupational Diseases Surveillance and Prevention Network (RNV3P)   (France)

Author keywords

Animal experimentation; Endocrine disruptor; Follicular atresia; Occupational exposure; Occupational health; Premature ovarian failure

Indexed keywords

1,3 BUTADIENE; 2 BROMOPROPANE; 2 METHOXYETHANOL; 3 METHYLCHOLANTHRENE; 4 VINYLCYCLOHEXENE; ACETONYLACETONE; BENZO[A]PYRENE; CADMIUM; CARBOSULFAN; CHROMIUM DERIVATIVE; DIBROMONEOPENTYL GLYCOL; DICOFOL; DIMETHYLBENZANTRACENE; HEXABROMOCYCLODODECANE; HEXACHLOROBENZENE; HEXAVALENT CHROMIUM; ISOPRENE; LEAD; MANCOZEB; POLYCYCLIC AROMATIC HYDROCARBON DERIVATIVE; UNCLASSIFIED DRUG;

CHEMICAL ANALYSIS; CHEMICAL STRUCTURE; ENVIRONMENTAL EXPOSURE; FERTILITY; HUMAN; HYPOXIA; INCIDENCE; MALE INFERTILITY; MENSTRUAL CYCLE; NONHUMAN; OCCUPATIONAL EXPOSURE; OVARY FOLLICLE DEVELOPMENT; OVARY FOLLICLE MATURATION; PREMATURE OVARIAN FAILURE; PREVALENCE; REVIEW; RISK ASSESSMENT;

ANIMALS; FEMALE; HUMANS; OCCUPATIONAL EXPOSURE; PRIMARY OVARIAN INSUFFICIENCY;

ANIMALIA;

EID: 84859739011     PISSN: 08906238     EISSN: 18731708     Source Type: Journal    
DOI: 10.1016/j.reprotox.2012.01.002     Document Type: Review

References (78)

1. Conway G.S. Premature ovarian failure. Br Med Bull 2000, 56:643-649.
2. Rebar R.W. Premature ovarian failure. Obstet Gynecol 2009, 113:1355-1363.
3. Gosden R.G., Treloar S.A., Martin N.G., Cherkas L.F., Spector T.D., Faddy M.J., et al. Prevalence of premature ovarian failure in monozygotic and dizygotic twins. Hum Reprod 2007, 22:610-615.
4. Christin-Maitre S., Braham R. General mechanisms of premature ovarian failure and clinical check-up. Gynecol Obstet Fertil 2008, 36:857-861.
5. Gallicchio L., Miller S., Greene T., Zacur H., Flaws J.A. Premature ovarian failure among hairdressers. Hum Reprod 2009, 24:2636-2641.
6. Goswami D., Conway G.S. Premature ovarian failure. Hum Reprod Update 2005, 11:391-410.
7. Christin-Maitre S., Bouchard P. Genes and ovarian insufficiency. Ann Endocrinol 1999, 60:118-122.
8. De Vos M., Devroey P., Fauser B.C. Primary ovarian insufficiency. Lancet 2010, 376(9744):911-921.
9. Christin-Maitre S., Pasquier M., Donadille B., Bouchard P. Premature ovarian failure. Ann Endocrinol (Paris) 2006, 67:557-566.
10. Conway GS Considerations for transition from paediatric to adult endocrinology: women with Turner's syndrome. Growth Horm IGF Res 2004, 14(Suppl. A):S77-S84.
11. Matikainen T., Perez G.I., Jurisicova A., Pru J.K., Schlezinger J.J., Ryu H.Y., 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.
12. Mikkelsen T.F., Graff-Iversen S., Sundby J., Bjertness E. Early menopause, association with tobacco smoking, coffee consumption and other lifestyle factors: a cross-sectional study. BMC Public Health 2007, 7:149.
13. Tuttle A.M., Stampfli M., Foster W.G. Cigarette smoke causes follicle loss in mice ovaries at concentrations representative of human exposure. Hum Reprod 2009, 24:1452-1459.
14. Luborsky J.L., Meyer P., Sowers M.F., Gold E.B., Santoro N. Premature menopause in a multi-ethnic population study of the menopause transition. Hum Reprod 2003, 18:199-206.
15. Boekelheide K., Darney S.P., Daston G.P., David R.M., Luderer U., Olshan A.F., et al. NTP-CERHR Expert Panel Report on the reproductive and developmental toxicity of 2-bromopropane. Reprod Toxicol 2004, 18:189-217.
16. Koh J.M., Kim C.H., Hong S.K., Lee K.U., Kim Y.T., Kim O.J., et al. Primary ovarian failure caused by a solvent containing 2-bromopropane. Eur J Endocrinol 1998, 138:554-556.
17. Knox S.S., Jackson T., Javins B., Frisbee S.J., Shankar A., Ducatman A.M. Implications of early menopause in women exposed to perfluorocarbons. J Clin Endocrinol Metab 2011, 96:1747-1753.
18. Jurisicova A., Taniuchi A., Li H., Shang Y., Antenos M., Detmar J., et al. Maternal exposure to polycyclic aromatic hydrocarbons diminishes murine ovarian reserve via induction of Harakiri. J Clin Invest 2007, 117:3971-3978.
19. Xia Y., Zhu P., Han Y., Lu C., Wang S., Gu A., et al. Urinary metabolites of polycyclic aromatic hydrocarbons in relation to idiopathic male infertility. Hum Reprod 2009, 24:1067-1074.
20. Mayer L.P., Devine P.J., Dyer C.A., Hoyer P.B. The follicle-deplete mouse ovary produces androgen. Biol Reprod 2004, 71:130-138.
21. Takai Y., Canning J., Perez G.I., Pru J.K., Schlezinger J.J., Sherr D.H., et al. Bax, caspase-2, and caspase-3 are required for ovarian follicle loss caused by 4-vinylcyclohexene diepoxide exposure of female mice in vivo. Endocrinology 2003, 144:69-74.
22. Hoyer P.B., Devine P.J., Hu X., Thompson K.E., Sipes I.G. Ovarian toxicity of 4-vinylcyclohexene diepoxide: a mechanistic model. Toxicol Pathol 2001, 29:91-99.
23. Charleston J.S., Hansen K.R., Thyer A.C., Charleston L.B., Gougeon A., Siebert J.R., et al. Estimating human ovarian non-growing follicle number: the application of modern stereology techniques to an old problem. Hum Reprod 2007, 22:2103-2110.
24. Wallace W.H., Kelsey T.W. Human ovarian reserve from conception to the menopause. PloS One 2010, 5:e8772.
25. Mattison DR, Stellman JM. Le système reproducteur féminin et les organes cibles. In: BIT, editor. Encyclopédie de sécurité et de santé au travail. Geneva; 2000, p. 9-11.
26. Simon A.M., Goodenough D.A., Li E., Paul D.L. Female infertility in mice lacking connexin 37. Nature 1997, 385(6616):525-529.
27. Mahadevaswami M.P., Kaliwal B.B. Effect of dimethoate administration schedules on compensatory ovarian hypertrophy, follicular dynamics, and estrous cycle in hemicastrated mice. J Basic Clin Physiol Pharmacol 2002, 13:225-248.
28. Hiremath M.B., Kaliwal B.B. Effect of endosulfan on ovarian compensatory hypertrophy in hemicastrated albino mice. Reprod Toxicol 2002, 16:783-790.
29. Nanda N., Kaliwal B.B. Effect of edifenphos on compensatory ovarian hypertrophy, follicular kinetics and estrous cycle in hemicastrated rats. J Basic Clin Physiol Pharmacol 2003, 14:373-386.
30. Math J.R., Jadaramkunti U.C., Kaliwal B.B. Effect of edifenphos on follicular dynamics in albino rats. Indian J Exp Biol 1998, 36:39-42.
31. Bolon B., Bucci T.J., Warbritton A.R., Chen J.J., Mattison D.R., Heindel J.J. Differential follicle counts as a screen for chemically induced ovarian toxicity in mice: results from continuous breeding bioassays. Fundam Appl Toxicol 1997, 39:1-10.
32. Kidder G.M., Mhawi A.A. Gap junctions and ovarian folliculogenesis. Reproduction 2002, 123:613-620.
33. Ke F.C., Fang S.H., Lee M.T., Sheu S.Y., Lai S.Y., Chen Y.J., et al. Lindane, a gap junction blocker, suppresses FSH and transforming growth factor beta1-induced connexin43 gap junction formation and steroidogenesis in rat granulosa cells. J Endocrinol 2005, 184:555-566.
34. Li W., Shibata E., Zhou Z., Ichihara S., Wang H., Wang Q., et al. Dose-dependent neurologic abnormalities in workers exposed to 1-bromopropane. J Occup Environ Med 2010, 52:769-777.
35. Yamada T., Ichihara G., Wang H., Yu X., Maeda K., Tsukamura H., et al. Exposure to 1-bromopropane causes ovarian dysfunction in rats. Toxicol Sci 2003, 71:96-103.
36. Ichihara G. Neuro-reproductive toxicities of 1-bromopropane and 2-bromopropane. Int Arch Occup Environ Health 2005, 78:79-96.
37. Sakurada Y., Shirota M., Mukai M., Inoue K., Akahori F., Watanabe G., et al. Effects of vertically transferred 3,3',4,4',5-pentachlorobiphenyl on gene expression in the ovaries of immature Sprague-Dawley rats. J Reprod Dev 2007, 53:937-943.
38. Riess M.L., Halm J.K. Lead poisoning in an adult: lead mobilization by pregnancy?. J Gen Intern Med 2007, 22:1212-1215.
39. Lorber M., Phillips L. Infant exposure to dioxin-like compounds in breast milk. Environ Health Perspect 2002, 110:A325-A332.
40. Matikainen T.M., Moriyama T., Morita Y., Perez G.I., Korsmeyer S.J., Sherr D.H., et al. Ligand activation of the aromatic hydrocarbon receptor transcription factor drives Bax-dependent apoptosis in developing fetal ovarian germ cells. Endocrinology 2002, 143:615-620.
41. Larsen J. Embryologie humaine 2003, De Boeck, Bruxelles, Belgium, p. 265-313.
42. Bond J.A., Medinsky M.A. Insights into the toxicokinetics and toxicodynamics of 1,3-butadiene. Chem Biol Interact 2001, 135/136:599-614.
43. Anderson D. Genetic and reproductive toxicity of butadiene and isoprene. Chem Biol Interact 2001, 135/136:65-80.
44. Fowler P.A., Dorà N.J., McFerran H., Amezaga M.R., Miller D.W., Lea R.G., et al. In utero exposure to low doses of environmental pollutants disrupts fetal ovarian development in sheep. Mol Hum Reprod 2008, 14:269-280.
45. Cheung C., Gonzalez F.J. Humanized mouse lines and their application for prediction of human drug metabolism and toxicological risk assessment. J Pharmacol Exp Ther 2008, 327:288-299.
46. Flaveny C.A., Perdew G.H. Transgenic humanized AHR mouse reveals differences between human and mouse AHR ligand selectivity. Mol Cell Pharmacol 2009, 1:119-123.
47. Cheng J., Ma X., Pregnane Gonzalez F.J. X receptor- and CYP3A4-humanized mouse models and their applications. Br J Pharmacol 2011, 163:461-468.
48. Johnson J., Canning J., Kaneko T., Pru J.K., Tilly J.L. Germline stem cells and follicular renewal in the postnatal mammalian ovary. Nature 2004, 428(6979):145-150.
49. Minervini F., Giannoccaro A., Fornelli F., Dell'Aquila M.E., Minoia P., Visconti A. Influence of mycotoxin zearalenone and its derivatives (alpha and beta zearalenol) on apoptosis and proliferation of cultured granulosa cells from equine ovaries. Reprod Biol Endocrinol 2006, 4:62.
50. Kok H.S., van Asselt K.M., van der Schouw Y.T., van der Tweel I., Peeters P.H., Wilson P.W., et al. Heart disease risk determines menopausal age rather than the reverse. J Am Coll Cardiol 2006, 47:1976-1983.
51. Verratti V., Berardinelli F., Di Giulio C., Bosco G., Cacchio M., Pellicciotta M., et al. Evidence that chronic hypoxia causes reversible impairment on male fertility. Asian J Androl 2008, 10:602-606.
52. Webster W.S., Abela D. The effect of hypoxia in development. Birth Defects Res C Embryo Today 2007, 81:215-228.
53. Meistrich M.L., Wilson G., Shuttlesworth G.A., Porter K.L. Dibromochloropropane inhibits spermatogonial development in rats. Reprod Toxicol 2003, 17:263-271.
54. Bonneterre V., Faisandier L., Bicout D., Bernardet C., Piollat J., Ameille J., et al. Programmed health surveillance and detection of emerging diseases in occupational health: contribution of the French national occupational disease surveillance and prevention network (RNV3P). Occup Environ Med 2010, 67:178-186.
55. Faisandier L., Bonneterre V., De Gaudemaris R., Bicout D.J. Occupational exposome: a network-based approach for characterizing Occupational Health Problems. J Biomed Inform 2011, 44:545-552.
56. Kim Y., Jung K., Hwang T., Jung G., Kim H., Park J., et al. Hematopoietic and reproductive hazards of Korean electronic workers exposed to solvents containing 2-bromopropane. Scand J Work Environ Health 1996, 22:387-391.
57. Kim Y., Park J., Moon Y. Hematopoietic and reproductive toxicity of 2-bromopropane, a recently introduced substitute for chlorofluorocarbons. Toxicol Lett 1999, 108:309-313.
58. Park J., Kim Y., Park D., Choi K., Park S., Moon Y. An outbreak of hematopoietic and reproductive disorders due to solvents containing 2-bromopropane in an electronic factory, South Korea: epidemiological survey. J Occup Health 1997, 39:138-143.
59. Ichihara G., Ding X., Yu X., Wu X., Kamijima M., Peng S., et al. Occupational health survey on workers exposed to 2-bromopropane at low concentrations. Am J Ind Med 1999, 35:523-531.
60. Gallagher C.M., Moonga B.S., Kovach J.S. Cadmium, follicle-stimulating hormone, and effects on bone in women age 42-60 years, NHANES III. Environ Res 2010, 110:105-111.
61. Taupeau C., Poupon J., Nome F., Lefevre B. Lead accumulation in the mouse ovary after treatment-induced follicular atresia. Reprod Toxicol 2001, 15:385-391.
62. Nampoothiri L.P., Gupta S. Simultaneous effect of lead and cadmium on granulosa cells: a cellular model for ovarian toxicity. Reprod Toxicol 2006, 21:179-185.
63. Banu S.K., Samuel J.B., Arosh J.A., Burghardt R.C., Aruldhas M.M. Lactational exposure to hexavalent chromium delays puberty by impairing ovarian development, steroidogenesis and pituitary hormone synthesis in developing Wistar rats. Toxicol Appl Pharmacol 2008, 232:180-189.
64. American Society of Human Genetics, American Society for Reproductive Medicine, Endocrine Society; Genetics Society of America, Society for Developmental Biology, Society for Pediatric Urology, Society for the Study of Reproduction, et al. Assessing chemical risk: societies offer expertise. Science 2011, 331(6021):1136.
65. Yu X., Kamijima M., Ichihara G., Li W., Kitoh J., Xie Z., et al. 2-Bromopropane causes ovarian dysfunction by damaging primordial follicles and their oocytes in female rats. Toxicol Appl Pharmacol 1999, 159:185-193.
66. Siracusa G., Bastone A., Sbraccia M., Settimi L., Mallozzi C., Monaco E., et al. Effects of 2,5-hexanedione on the ovary and fertility. An experimental study in mice. Toxicology 1992, 75:39-50.
67. Alvarez L., Randi A., Alvarez P., Piroli G., Chamson-Reig A., Lux-Lantos V., et al. Reproductive effects of hexachlorobenzene in female rats. J Appl Toxicol 2000, 20:81-87.
68. Baligar P.N., Kaliwal B.B. Induction of gonadal toxicity to female rats after chronic exposure to mancozeb. Ind Health 2001, 39:235-243.
69. Parimala M.D., Kaliwal B.B. Dose-dependent estrous cycle, ovarian follicles and biochemical contents reversal in albino mice after exposure to mancozeb. Caspian J Environ Sci 2005, 3:118-131.
70. Jadarmkunti U.C., Kaliwal B.B. Effect of dicofol formulation on estrous cycle and follicular dynamics in albino rats. J Basic Clin Physiol Pharmacol 1999, 10:305-314.
71. Ksheerasagar R.L., Kaliwal B.B. Effects of carbosulfan administration schedules on estrous cycle and follicular dynamics in albino mice. Ind Health 2008, 46:210-216.
72. Appt S.E., Kaplan J.R., Clarkson T.B., Cline J.M., Christian P.J., Hoyer P.B. Destruction of primordial ovarian follicles in adult cynomolgus macaques after exposure to 4-vinylcyclohexene diepoxide: a nonhuman primate model of the menopausal transition. Fertil Steril 2006, 86(4 Suppl.):1210-1216.
73. Ema M., Fujii S., Hirata-Koizumi M., Matsumoto M. Two-generation reproductive toxicity study of the flame retardant hexabromocyclododecane in rats. Reprod Toxicol 2008, 25:335-351.
74. Doerr J.K., Hollis E.A., Sipes I.G. Species difference in the ovarian toxicity of 1,3-butadiene epoxides in B6C3F1 mice and Sprague-Dawley rats. Toxicology 1996, 113:128-136.
75. Doerr J.K., Hooser S.B., Smith B.J., Sipes I.G. Ovarian toxicity of 4-vinylcyclohexene and related olefins in B6C3F1 mice: role of diepoxides. Chem Res Toxicol 1995, 8:963-969.
76. Borman S.M., Christian P.J., Sipes I.G., Hoyer P.B. Ovotoxicity in female Fischer rats and B6 mice induced by low-dose exposure to three polycyclic aromatic hydrocarbons: comparison through calculation of an ovotoxic index. Toxicol Appl Pharmacol 2000, 167:191-198.
77. Armenti A.E., Zama A.M., Passantino L., Uzumcu M. Developmental methoxychlor exposure affects multiple reproductive parameters and ovarian folliculogenesis and gene expression in adult rats. Toxicol Appl Pharmacol 2008, 233:286-296.
78. Rodriguez H.A., Santambrosio N., Santamaria C.G., Munoz-de-Toro M., Luque E.H. Neonatal exposure to bisphenol A reduces the pool of primordial follicles in the rat ovary. Reprod Toxicol 2010, 30:550-557.