DOI QR코드

DOI QR Code

Effects of early prepubertal exposure to bisphenol A on the onset of puberty, ovarian weights, and estrous cycle in female mice

  • Nah, Won-Heum (Department of Life Sciences and Institute for Natural Sciences, Hanyang University) ;
  • Park, Mi-Jung (Department of Pediatrics, Sanggye Paik Hospital, Inje University College of Medicine) ;
  • Gye, Myung-Chan (Department of Life Sciences and Institute for Natural Sciences, Hanyang University)
  • Received : 2011.02.21
  • Accepted : 2011.03.14
  • Published : 2011.06.30

Abstract

Objective: Bisphenol A (BPA) is a chemical used extensively to manufacture plastics and epoxy resin liners for food and beverage cans. BPA, with properties similar to estrogen, has endocrine-disrupting effects. In the present study, we examined the effects of early prepubertal BPA exposure on the onset of puberty and reproductive parameters such as estrous cycle and reproductive organ weights in female mice. Methods: Female mice were injected subcutaneously at postnatal day (PND) 8 with BPA (0.1, 1, 10, 100 mg/kg) in sesame oil or with sesame oil alone. Body weight was measured from PND 10 to 70. Vaginal opening and estrous cycle were monitored from PND 20 to 29. Animals were sacrificed at PND 25, 30, and 70, and the ovary and uterus weights were measured. Results: Early prepubertal exposure to BPA (10 and 100 mg/kg) significantly decreased body weight from PND 18 to 30. BPA treated mice at testing dose levels showed early opening of the vagina compared to the control group. The number of estrous cycle and days of estrus were significantly decreased in high dose (100 mg/kg) BPA treated mice. The ovary weight at PND 25 and 30 was significantly decreased in all BPA treatment groups. Conclusion: Early prepubertal exposure to BPA accelerated the onset of puberty but decreased reproductive parameters in female mice.

Keywords

References

  1. Henley DV, Korach KS. Endocrine-disrupting chemicals use distinct mechanisms of action to modulate endocrine system function. Endocrinology 2006;147:S25-32. https://doi.org/10.1210/en.2005-1117
  2. Clark EJ, Norris DO, Jones RE. Interactions of gonadal steroids and pesticides (DDT, DDE) on gonaduct growth in larval tiger salamanders, Ambystoma tigrinum. Gen Comp Endocrinol 1998;109:94-105. https://doi.org/10.1006/gcen.1997.7013
  3. Gray LE Jr. Tiered screening and testing strategy for xenoestrogens and antiandrogens. Toxicol Lett 1998;102-103:677-80. https://doi.org/10.1016/S0378-4274(98)00287-2
  4. Toppari J, Skakkebaek NE. Sexual differentiation and environmental endocrine disrupters. Baillieres Clin Endocrinol Metab 1998;12:143-56. https://doi.org/10.1016/S0950-351X(98)80529-6
  5. Toppari J. Environmental endocrine disrupters and disorders of sexual differentiation. Semin Reprod Med 2002;20:305-12.
  6. Takeyoshi M, Yamasaki K, Sawaki M, Nakai M, Noda S, Takatsuki M. The efficacy of endocrine disruptor screening tests in detecting anti-estrogenic effects downstream of receptor-ligand interactions. Toxicol Lett 2002;126:91-8. https://doi.org/10.1016/S0378-4274(01)00446-5
  7. Rasier G, Toppari J, Parent AS, Bourguignon JP. Female sexual maturation and reproduction after prepubertal exposure to estrogens and endocrine disrupting chemicals: a review of rodent and human data. Mol Cell Endocrinol 2006;254-255:187-201. https://doi.org/10.1016/j.mce.2006.04.002
  8. Nelson JF, Karelus K, Felicio LS, Johnson TE. Genetic influences on the timing of puberty in mice. Biol Reprod 1990;42:649-55. https://doi.org/10.1095/biolreprod42.4.649
  9. Veldhuis JD, Roemmich JN, Richmond EJ, Bowers CY. Somatotropic and gonadotropic axes linkages in infancy, childhood, and the puberty-adult transition. Endocr Rev 2006;27:101-40. https://doi.org/10.1210/er.2005-0006
  10. Ramirez VD, Sawyer CH. Advancement of Puberty in the Female Rat by Estrogen. Endocrinology 1965;76:1158-68. https://doi.org/10.1210/endo-76-6-1158
  11. Ronis MJ, Badger TM, Shema SJ, Roberson PK, Templer L, Ringer D, et al. Endocrine mechanisms underlying the growth effects of developmental lead exposure in the rat. J Toxicol Environ Health A 1998;54:101-20. https://doi.org/10.1080/009841098158944
  12. Whitten PL, Naftolin F. Effects of a phytoestrogen diet on estrogen-dependent reproductive processes in immature female rats. Steroids 1992;57:56-61. https://doi.org/10.1016/0039-128X(92)90029-9
  13. Gellert RJ. Uterotrophic activity of polychlorinated biphenyls (PCB) and induction of precocious reproductive aging in neonatally treated female rats. Environ Res 1978;16:123-30. https://doi.org/10.1016/0013-9351(78)90149-4
  14. Walters LM, Rourke AW, Eroschenko VP. Purified methoxychlor stimulates the reproductive tract in immature female mice. Reprod Toxicol 1993;7:599-606. https://doi.org/10.1016/0890-6238(93)90036-7
  15. Blanck HM, Marcus M, Tolbert PE, Rubin C, Henderson AK, Hertzberg VS, et al. Age at menarche and tanner stage in girls exposed in utero and postnatally to polybrominated biphenyl. Epidemiology 2000;11:641-7. https://doi.org/10.1097/00001648-200011000-00005
  16. de Ridder CM, Thijssen JH, Van 't Veer P, van Duuren R, Bruning PF, Zonderland ML, et al. Dietary habits, sexual maturation, and plasma hormones in pubertal girls: a longitudinal study. Am J Clin Nutr 1991;54:805-13. https://doi.org/10.1093/ajcn/54.5.805
  17. Gladen BC, Ragan NB, Rogan WJ. Pubertal growth and development and prenatal and lactational exposure to polychlorinated biphenyls and dichlorodiphenyl dichloroethene. J Pediatr 2000;136:490-6. https://doi.org/10.1016/S0022-3476(00)90012-X
  18. Karmaus W, Asakevich S, Indurkhya A, Witten J, Kruse H. Childhood growth and exposure to dichlorodiphenyl dichloroethene and polychlorinated biphenyls. J Pediatr 2002;140:33-9. https://doi.org/10.1067/mpd.2002.120764
  19. Denham M, Schell LM, Deane G, Gallo MV, Ravenscroft J, DeCaprio AP, et al. Relationship of lead, mercury, mirex, dichlorodiphenyldichloroethylene, hexachlorobenzene, and polychlorinated biphenyls to timing of menarche among Akwesasne Mohawk girls. Pediatrics 2005;115:e127-34. https://doi.org/10.1542/peds.2004-1161
  20. Morrison JA, Sprecher DL, Barton BA, Waclawiw MA, Daniels SR. Overweight, fat patterning, and cardiovascular disease risk factors in black and white girls: The National Heart, Lung, and Blood Institute Growth and Health Study. J Pediatr 1999;135:458-64. https://doi.org/10.1016/S0022-3476(99)70168-X
  21. Patton GC, Viner R. Pubertal transitions in health. Lancet 2007;369:1130-9. https://doi.org/10.1016/S0140-6736(07)60366-3
  22. Colón I, Caro D, Bourdony CJ, Rosario O. Identification of phthalate esters in the serum of young Puerto Rican girls with premature breast development. Environ Health Perspect 2000;108:895-900.
  23. Vasiliu O, Muttineni J, Karmaus W. In utero exposure to organochlorines and age at menarche. Hum Reprod 2004;19:1506-12. https://doi.org/10.1093/humrep/deh292
  24. Krstevska-Konstantinova M, Charlier C, Craen M, Du Caju M, Heinrichs C, de Beaufort C, et al. Sexual precocity after immigration from developing countries to Belgium: evidence of previous exposure to organochlorine pesticides. Hum Reprod 2001;16:1020-6. https://doi.org/10.1093/humrep/16.5.1020
  25. Ouyang F, Perry MJ, Venners SA, Chen C, Wang B, Yang F, et al. Serum DDT, age at menarche, and abnormal menstrual cycle length. Occup Environ Med 2005;62:878-84. https://doi.org/10.1136/oem.2005.020248
  26. Selevan SG, Rice DC, Hogan KA, Euling SY, Pfahles-Hutchens A, Bethel J. Blood lead concentration and delayed puberty in girls. N Engl J Med 2003;348:1527-36. https://doi.org/10.1056/NEJMoa020880
  27. Wu T, Buck GM, Mendola P. Blood lead levels and sexual maturation in U.S. girls: the Third National Health and Nutrition Examination Survey, 1988-1994. Environ Health Perspect 2003;111:737-41. https://doi.org/10.1289/ehp.6008
  28. Hauser R, Sergeyev O, Korrick S, Lee MM, Revich B, Gitin E, et al. Association of blood lead levels with onset of puberty in Russian boys. Environ Health Perspect 2008;116:976-80. https://doi.org/10.1289/ehp.10516
  29. Den Hond E, Roels HA, Hoppenbrouwers K, Nawrot T, Thijs L, Vandermeulen C, et al. Sexual maturation in relation to polychlorinated aromatic hydrocarbons: Sharpe and Skakkebaek's hypothesis revisited. Environ Health Perspect 2002;110:771-6. https://doi.org/10.1289/ehp.02110771
  30. Mol NM, Sorensen N, Weihe P, Andersson AM, Jorgensen N, Skakkebaek NE, et al. Spermaturia and serum hormone concentrations at the age of puberty in boys prenatally exposed to polychlorinated biphenyls. Eur J Endocrinol 2002;146:357-63. https://doi.org/10.1530/eje.0.1460357
  31. Wolff MS, Britton JA, Boguski L, Hochman S, Maloney N, Serra N, et al. Environmental exposures and puberty in inner-city girls. Environ Res 2008;107:393-400. https://doi.org/10.1016/j.envres.2008.03.006
  32. Muhlhauser A, Susiarjo M, Rubio C, Griswold J, Gorence G, Hassold T, et al. Bisphenol A effects on the growing mouse oocyte are influenced by diet. Biol Reprod 2009;80:1066-71. https://doi.org/10.1095/biolreprod.108.074815
  33. Petrovic M, Gonzalez S, Barcelo D. Analysis and removal of emerging contaminants in wastewater and drinking water. Trends Analyt Chem 2003;22:685-96. https://doi.org/10.1016/S0165-9936(03)01105-1
  34. Kot-Wasic A, Debska J, Namiesnik J. Analytical techniques in studies of the environmental fate of pharmaceuticals and personalcare products. Trends Analyt Chem 2007;26:557-68. https://doi.org/10.1016/j.trac.2006.11.004
  35. Gutendorf B, Westendorf J. Comparison of an array of in vitro assays for the assessment of the estrogenic potential of natural and synthetic estrogens, phytoestrogens and xenoestrogens. Toxicology 2001;166:79-89. https://doi.org/10.1016/S0300-483X(01)00437-1
  36. Holmes P, Rumsby P, Harrison PT. Endocrine disrupters and menopausal health. J Br Menopause Soc 2004;10:54-9. https://doi.org/10.1258/136218004774202355
  37. Sun Y, Irie M, Kishikawa N, Wada M, Kuroda N, Nakashima K. Determination of bisphenol A in human breast milk by HPLC with column-switching and fluorescence detection. Biomed Chromatogr 2004;18:501-7. https://doi.org/10.1002/bmc.345
  38. Ye X, Kuklenyik Z, Needham LL, Calafat AM. Measuring environmental phenols and chlorinated organic chemicals in breast milk using automated on-line column-switching-high performance liquid chromatography-isotope dilution tandem mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci 2006;831:110-5. https://doi.org/10.1016/j.jchromb.2005.11.050
  39. 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;17:2839-41. https://doi.org/10.1093/humrep/17.11.2839
  40. Schonfelder G, Wittfoht W, Hopp H, Talsness CE, Paul M, Chahoud I. Parent bisphenol A accumulation in the human maternal-fetal-placental unit. Environ Health Perspect 2002;110:A703-7. https://doi.org/10.1289/ehp.021100703
  41. Meeker JD, Ehrlich S, Toth TL, Wright DL, Calafat AM, Trisini AT, et al. Semen quality and sperm DNA damage in relation to urinary bisphenol A among men from an infertility clinic. Reprod Toxicol 2010;30:532-9. https://doi.org/10.1016/j.reprotox.2010.07.005
  42. Roy JR, Chakraborty S, Chakraborty TR. Estrogen-like endocrine disrupting chemicals affecting puberty in humans: a review. Med Sci Monit 2009;15:RA137-45.
  43. Kandaraki E, Chatzigeorgiou A, Livadas S, Palioura E, Economou F, Koutsilieris M, et al. Endocrine disruptors and polycystic ovary syndrome (PCOS): elevated serum levels of bisphenol A in women with PCOS. J Clin Endocrinol Metab 2011;96:E480-4. https://doi.org/10.1210/jc.2010-1658
  44. Della Seta D, Minder I, Dessi-Fulgheri F, Farabollini F. Bisphenol-A exposure during pregnancy and lactation affects maternal behavior in rats. Brain Res Bull 2005;65:255-60. https://doi.org/10.1016/j.brainresbull.2004.11.017
  45. Sakaue M, Ohsako S, Ishimura R, Kurosawa S, Kurohmaru M, Hayashi Y, et al. Bisphenol-A affects spermatogenesis in the adult rat even at a low dose. J Occup Health 2001;43:185-90. https://doi.org/10.1539/joh.43.185
  46. Al-Hiyasat AS, Darmani H, Elbetieha AM. Effects of bisphenol A on adult male mouse fertility. Eur J Oral Sci 2002;110:163-7. https://doi.org/10.1034/j.1600-0722.2002.11201.x
  47. Toyama Y, Suzuki-Toyota F, Maekawa M, Ito C, Toshimori K. Adverse effects of bisphenol A to spermiogenesis in mice and rats. Arch Histol Cytol 2004;67:373-81. https://doi.org/10.1679/aohc.67.373
  48. Goodman JE, McConnell EE, Sipes IG, Witorsch RJ, Slayton TM, Yu CJ, et al. An updated weight of the evidence evaluation of reproductive and developmental effects of low doses of bisphenol A. Crit Rev Toxicol 2006;36:387-457. https://doi.org/10.1080/10408440600758317
  49. Matagne V, Rasier G, Lebrethon MC, Gerard A, Bourguignon JP. Estradiol stimulation of pulsatile gonadotropin-releasing hormone secretion in vitro: correlation with perinatal exposure to sex steroids and induction of sexual precocity in vivo. Endocrinology 2004;145:2775-83. https://doi.org/10.1210/en.2003-1259
  50. McGovern V. Polycarbonate plastics and human BPA exposure: urinary levels rise with use of drinking bottles. Environ Health Perspect 2009;117:A406.
  51. Parent AS, Teilmann G, Juul A, Skakkebaek NE, Toppari J, Bourguignon JP. The timing of normal puberty and the age limits of sexual precocity: variations around the world, secular trends, and changes after migration. Endocr Rev 2003;24:668-93. https://doi.org/10.1210/er.2002-0019
  52. Honma S, Suzuki A, Buchanan DL, Katsu Y, Watanabe H, Iguchi T. Low dose effect of in utero exposure to bisphenol A and diethylstilbestrol on female mouse reproduction. Reprod Toxicol 2002;16:117-22. https://doi.org/10.1016/S0890-6238(02)00006-0
  53. Newbold RR, Jefferson WN, Padilla-Banks E. Long-term adverse effects of neonatal exposure to bisphenol A on the murine female reproductive tract. Reprod Toxicol 2007;24:253-8. https://doi.org/10.1016/j.reprotox.2007.07.006
  54. Newbold RR, Jefferson WN, Padilla-Banks E. Prenatal exposure to bisphenol a at environmentally relevant doses adversely affects the murine female reproductive tract later in life. Environ Health Perspect 2009;117:879-85. https://doi.org/10.1289/ehp.0800045

Cited by

  1. Dental Composites and Amalgam and Physical Development in Children vol.91, pp.11, 2011, https://doi.org/10.1177/0022034512458691
  2. Salivary Bisphenol-A Levels due to Dental Sealant/Resin: A Case-Control Study in Korean Children vol.27, pp.9, 2012, https://doi.org/10.3346/jkms.2012.27.9.1098
  3. Endocrine Disrupting Chemicals and Pubertal Development vol.27, pp.1, 2012, https://doi.org/10.3803/enm.2012.27.1.20
  4. Preconceptional omega-3 fatty acid supplementation on a micronutrient-deficient diet improves the reproductive cycle in Wistar rats vol.25, pp.7, 2011, https://doi.org/10.1071/rd12210
  5. Mouse Strain Does Not Influence the Overall Effects of Bisphenol A-Induced Toxicity in Adult Antral Follicles1 vol.89, pp.5, 2011, https://doi.org/10.1095/biolreprod.113.111864
  6. Early Neuroendocrine Disruption in Hypothalamus and Hippocampus: Developmental Effects Including Female Sexual Maturation and Implications for Endocrine Disrupting Chemical Screening vol.25, pp.11, 2011, https://doi.org/10.1111/jne.12107
  7. Estrogenic Endocrine-Disrupting Chemicals: Molecular Mechanisms of Actions on Putative Human Diseases vol.17, pp.3, 2011, https://doi.org/10.1080/10937404.2014.882194
  8. Effects of Korean red ginseng ( Panax Ginseng Meyer ) on bisphenol A exposure and gynecologic complaints: single blind, randomized clinical trial of efficacy and safety vol.14, pp.None, 2011, https://doi.org/10.1186/1472-6882-14-265
  9. Bisphenol a and the female reproductive tract: an overview of recent laboratory evidence and epidemiological studies vol.12, pp.None, 2011, https://doi.org/10.1186/1477-7827-12-37
  10. Neuroendocrine and behavioral effects of maternal exposure to oral bisphenol A in female mice vol.220, pp.3, 2011, https://doi.org/10.1530/joe-13-0607
  11. Bisphenol A and Reproductive Health: Update of Experimental and Human Evidence, 2007–2013 vol.122, pp.8, 2011, https://doi.org/10.1289/ehp.1307728
  12. Solar CPC pilot plant photocatalytic degradation of bisphenol A in waters and wastewaters using suspended and supported-TiO2. Influence of photogenerated species vol.21, pp.21, 2011, https://doi.org/10.1007/s11356-014-2723-0
  13. EDC-2: The Endocrine Society's Second Scientific Statement on Endocrine-Disrupting Chemicals vol.36, pp.6, 2011, https://doi.org/10.1210/er.2015-1010
  14. Scientific Opinion on the risks to public health related to the presence of bisphenol A (BPA) in foodstuffs : Opinion on BPA vol.13, pp.1, 2015, https://doi.org/10.2903/j.efsa.2015.3978
  15. Report on the two‐phase public consultation on the draft EFSA scientific opinion on bisphenol A (BPA) vol.12, pp.1, 2011, https://doi.org/10.2903/sp.efsa.2015.en-740
  16. Delay of the Onset of Puberty in Female Rats by Prepubertal Exposure to T-2 Toxin vol.7, pp.11, 2011, https://doi.org/10.3390/toxins7114668
  17. 내분비계장애물질 대체소재의 안전성 vol.33, pp.4, 2011, https://doi.org/10.11626/kjeb.2015.33.4.361
  18. Increase in endogenous estradiol in the progeny of obese rats is associated with precocious puberty and altered follicular development in adulthood vol.53, pp.1, 2011, https://doi.org/10.1007/s12020-016-0858-0
  19. The relation of urinary bisphenol A with kisspeptin in girls diagnosed with central precocious puberty and premature thelarche vol.29, pp.3, 2011, https://doi.org/10.1515/jpem-2015-0235
  20. Delayed Neuroendocrine Sexual Maturation in Female Rats After a Very Low Dose of Bisphenol A Through Altered GABAergic Neurotransmission and Opposing Effects of a High Dose vol.157, pp.5, 2011, https://doi.org/10.1210/en.2015-1937
  21. Stereological study on the effect of vitamin C in preventing the adverse effects of bisphenol A on rat ovary vol.14, pp.6, 2011, https://doi.org/10.29252/ijrm.14.6.403
  22. Associations between Dietary Intake and Urinary Bisphenol A and Phthalates Levels in Korean Women of Reproductive Age vol.13, pp.7, 2011, https://doi.org/10.3390/ijerph13070680
  23. The effect of maternal exposure to endocrine disrupting chemicals on fetal and neonatal development: A review on the major concerns vol.108, pp.3, 2016, https://doi.org/10.1002/bdrc.21137
  24. Evidence for bisphenol A-induced female infertility: a review (2007-2016) vol.106, pp.4, 2011, https://doi.org/10.1016/j.fertnstert.2016.06.027
  25. Possible effects of melatonin against rat uterus exposure to bisphenol A during neonatal period vol.24, pp.34, 2011, https://doi.org/10.1007/s11356-017-0187-8
  26. Postnatal feeding with high-fat diet induces obesity and precocious puberty in C57BL/6J mouse pups: a novel model of obesity and puberty vol.11, pp.2, 2017, https://doi.org/10.1007/s11684-017-0530-y
  27. A case–control study of bisphenol A and endometrioma among subgroup of Iranian women vol.22, pp.1, 2011, https://doi.org/10.4103/1735-1995.199086
  28. Bisphenol A and Ovarian Reserve among Infertile Women with Polycystic Ovarian Syndrome vol.14, pp.1, 2011, https://doi.org/10.3390/ijerph14010018
  29. Pubertal exposure to ethinylestradiol promotes different effects on the morphology of the prostate of the male and female gerbil during aging vol.32, pp.2, 2011, https://doi.org/10.1002/tox.22252
  30. Inhalation Toxicity of Bisphenol A and Its Effect on Estrous Cycle, Spatial Learning, and Memory in Rats upon Whole-Body Exposure vol.33, pp.2, 2017, https://doi.org/10.5487/tr.2017.33.2.165
  31. The Effect of Bisphenol A on Puberty: A Critical Review of the Medical Literature vol.14, pp.9, 2011, https://doi.org/10.3390/ijerph14091044
  32. A single neonatal administration of Bisphenol A induces higher tumour weight associated to changes in tumour microenvironment in the adulthood vol.7, pp.None, 2017, https://doi.org/10.1038/s41598-017-10135-1
  33. Urinary bisphenol A and pubertal development in Chinese school-aged girls: a cross-sectional study vol.16, pp.None, 2011, https://doi.org/10.1186/s12940-017-0290-9
  34. 비스페놀류의 사용 현황과 위해성: 소고 vol.35, pp.4, 2011, https://doi.org/10.11626/kjeb.2017.35.4.581
  35. Impact of Cold Exposure on the Reproductive Function in Female Rats vol.2018, pp.None, 2018, https://doi.org/10.1155/2018/3674906
  36. The association between the environmental endocrine disruptor bisphenol A and polycystic ovary syndrome: a systematic review and meta-analysis vol.34, pp.5, 2018, https://doi.org/10.1080/09513590.2017.1405931
  37. Endocrine disruption induced by bisphenol A in young and adult female Sprague Dawley rats vol.27, pp.4, 2011, https://doi.org/10.1007/s00580-018-2689-2
  38. Association of Prenatal Urinary Concentrations of Phthalates and Bisphenol A and Pubertal Timing in Boys and Girls vol.126, pp.9, 2011, https://doi.org/10.1289/ehp3424
  39. Environmental toxins and the impact of other endocrine disrupting chemicals in women's reproductive health vol.23, pp.2, 2011, https://doi.org/10.5935/1518-0557.20190016
  40. 化学暴露与青春期之间复杂关系的新证据 vol.127, pp.4, 2011, https://doi.org/10.1289/ehp4524-zh
  41. The Neurochemical Characterization of Parasympathetic Nerve Fibers in the Porcine Uterine Wall Under Physiological Conditions and After Exposure to Bisphenol A (BPA) vol.35, pp.4, 2019, https://doi.org/10.1007/s12640-019-00013-1
  42. Bisphenol A in dental materials – existence, leakage and biological effects vol.5, pp.5, 2011, https://doi.org/10.1016/j.heliyon.2019.e01711
  43. Dose exposure of Bisphenol- A on female Wistar rats fertility vol.38, pp.2, 2019, https://doi.org/10.1515/hmbci-2018-0061
  44. Dose exposure of Bisphenol- A on female Wistar rats fertility vol.38, pp.2, 2019, https://doi.org/10.1515/hmbci-2018-0061
  45. Chemical Exposures and Pubertal Timing: New Evidence in a Complex Area vol.127, pp.7, 2019, https://doi.org/10.1289/ehp4524
  46. Environmentally Relevant Perinatal Exposures to Bisphenol A Disrupt Postnatal Kiss1/NKB Neuronal Maturation and Puberty Onset in Female Mice vol.127, pp.10, 2011, https://doi.org/10.1289/ehp5570
  47. Exposure of BPA and its alternatives like BPB, BPF, and BPS impair subsequent reproductive potentials in adult female Sprague Dawley rats vol.30, pp.1, 2020, https://doi.org/10.1080/15376516.2019.1652873
  48. Catalytic Properties of Microporous Zeolite Catalysts in Synthesis of Isosorbide from Sorbitol by Dehydration vol.10, pp.2, 2020, https://doi.org/10.3390/catal10020148
  49. Impact of Bisphenol A on Gonadotropic Hormone Levels in Children with Autism Spectrum Disorders vol.35, pp.2, 2011, https://doi.org/10.1007/s12291-018-0801-7
  50. Effects of endocrine disruptor furan on reproductive physiology of Sprague Dawley rats: An F1 Extended One-Generation Reproductive Toxicity Study (EOGRTS) vol.39, pp.8, 2011, https://doi.org/10.1177/0960327120911416
  51. Cellular and molecular features of EDC exposure: consequences for the GnRH network vol.17, pp.2, 2011, https://doi.org/10.1038/s41574-020-00436-3
  52. Bisphenol A and Metabolites in Meat and Meat Products: Occurrence, Toxicity, and Recent Development in Analytical Methods vol.10, pp.4, 2021, https://doi.org/10.3390/foods10040714
  53. Endocrine-Disrupting Compounds: An Overview on Their Occurrence in the Aquatic Environment and Human Exposure vol.13, pp.10, 2011, https://doi.org/10.3390/w13101347
  54. Multi- and Transgenerational Outcomes of an Exposure to a Mixture of Endocrine-Disrupting Chemicals (EDCs) on Puberty and Maternal Behavior in the Female Rat vol.129, pp.8, 2011, https://doi.org/10.1289/ehp8795
  55. Urinary Bisphenol A Concentrations and Parameters of Ovarian Reserve among Women from a Fertility Clinic vol.18, pp.15, 2011, https://doi.org/10.3390/ijerph18158041
  56. Endocrine Disruptors Driven Female Reproductive Ailments vol.74, pp.4, 2011, https://doi.org/10.1007/s12595-021-00406-1
  57. Release of Bisphenol A from Pit and Fissure Sealants According to Different pH Conditions vol.14, pp.1, 2022, https://doi.org/10.3390/polym14010037