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Associations Between Thyroid Hormone Levels and Urinary Concentrations of Bisphenol A, F, and S in 6-Year-old Children in Korea

  • Jang, Yoonyoung (Department of Preventive Medicine, Seoul National University College of Medicine) ;
  • Choi, Yoon-Jung (Department of Preventive Medicine, Seoul National University College of Medicine) ;
  • Lim, Youn-Hee (Institute of Environmental Medicine, Seoul National University Medical Research Center) ;
  • Lee, Kyung-Shin (Department of Preventive Medicine, Seoul National University College of Medicine) ;
  • Kim, Bung-Nyun (Division of Child and Adolescent Psychiatry, Department of Psychiatry, Seoul National University College of Medicine) ;
  • Shin, Choong Ho (Department of Pediatrics, Seoul National University College of Medicine) ;
  • Lee, Young Ah (Department of Pediatrics, Seoul National University College of Medicine) ;
  • Kim, Johanna Inhyang (Department of Psychiatry, Hanyang University Medical Center) ;
  • Hong, Yun-Chul (Department of Preventive Medicine, Seoul National University College of Medicine)
  • 투고 : 2020.07.02
  • 심사 : 2020.10.23
  • 발행 : 2021.01.31

초록

Objectives: Bisphenol A (BPA) is used in the electrical, mechanical, medical, and food industries. Previous studies have suggested that BPA is an endocrine disruptor. Regulation of BPA has led to increased use of bisphenol F (BPF) and bisphenol S (BPS). However, few studies have investigated the associations of BPF and BPS with thyroid dysfunction in children. Our study investigated the associations of prenatal BPA and early childhood BPA, BPF, and BPS exposure with thyroid function in 6-year-old children. Methods: Prenatal BPA concentrations were measured during the second trimester of pregnancy in an established prospective birth cohort. We measured urinary BPA, BPF, and BPS concentrations and thyroid hormone levels (thyroid-stimulating hormone, total T3, and free T4) in 6-year-old children (n=574). We examined the associations between urinary bisphenol concentrations and percentage change of thyroid hormone concentrations using multivariate linear regression. We also compared thyroid hormone levels by dividing the cohort according to BPA, BPF, and BPS concentrations. Results: The associations between prenatal BPA and total T3 levels were statistically significant in all models, except for girls when using a crude model. The associations between urinary BPA and BPS concentrations and levels of all thyroid hormones were not statistically significant. However, we observed that lower free T4 levels (-1.94%; 95% confidence interval, -3.82 to -0.03) were associated with higher urinary BPF concentrations in girls only. Conclusions: Our findings identified significant associations between prenatal BPA exposure and total T3 levels in all children and between BPF exposure and free T4 levels in girls only.

키워드

참고문헌

  1. Lee J, Choi K, Park J, Moon HB, Choi G, Lee JJ, et al. Bisphenol A distribution in serum, urine, placenta, breast milk, and umbilical cord serum in a birth panel of mother-neonate pairs. Sci Total Environ 2018;626:1494-1501. https://doi.org/10.1016/j.scitotenv.2017.10.042
  2. Harley KG, Gunier RB, Kogut K, Johnson C, Bradman A, Calafat AM, et al. Prenatal and early childhood bisphenol A concentrations and behavior in school-aged children. Environ Res 2013;126:43-50. https://doi.org/10.1016/j.envres.2013.06.004
  3. Roen EL, Wang Y, Calafat AM, Wang S, Margolis A, Herbstman J, et al. Bisphenol A exposure and behavioral problems among inner city children at 7-9 years of age. Environ Res 2015;142: 739-745. https://doi.org/10.1016/j.envres.2015.01.014
  4. Braun JM, Muckle G, Arbuckle T, Bouchard MF, Fraser WD, Ouellet E, et al. Associations of prenatal urinary bisphenol A concentrations with child behaviors and cognitive abilities. Environ Health Perspect 2017;125(6):067008. https://doi.org/10.1289/EHP984
  5. Ghassabian A, Bell EM, Ma WL, Sundaram R, Kannan K, Buck Louis GM, et al. Concentrations of perfluoroalkyl substances and bisphenol A in newborn dried blood spots and the association with child behavior. Environ Pollut 2018;243(Pt B): 1629-1636. https://doi.org/10.1016/j.envpol.2018.09.107
  6. Li F, Yang F, Li DK, Tian Y, Miao M, Zhang Y, et al. Prenatal bisphenol A exposure, fetal thyroid hormones and neurobehavioral development in children at 2 and 4 years: a prospective cohort study. Sci Total Environ 2020;722:137887. https://doi.org/10.1016/j.scitotenv.2020.137887
  7. Lim YH, Bae S, Kim BN, Shin CH, Lee YA, Kim JI, et al. Prenatal and postnatal bisphenol A exposure and social impairment in 4-year-old children. Environ Health 2017;16(1):79. https://doi.org/10.1186/s12940-017-0289-2
  8. Berger K, Eskenazi B, Kogut K, Parra K, Lustig RH, Greenspan LC, et al. Association of prenatal urinary concentrations of phthalates and bisphenol A and pubertal timing in boys and girls. Environ Health Perspect 2018;126(9):97004. https://doi.org/10.1289/EHP3424
  9. Bae S, Lim YH, Lee YA, Shin CH, Oh SY, Hong YC. Maternal urinary bisphenol A concentration during midterm pregnancy and children's blood pressure at age 4. Hypertension 2017; 69(2):367-374. https://doi.org/10.1161/HYPERTENSIONAHA.116.08281
  10. Sanders AP, Saland JM, Wright RO, Satlin L. Perinatal and childhood exposure to environmental chemicals and blood pressure in children: a review of literature 2007-2017. Pediatr Res 2018;84(2):165-180. https://doi.org/10.1038/s41390-018-0055-3
  11. Amin MM, Ebrahim K, Hashemi M, Shoshtari-Yeganeh B, Rafiei N, Mansourian M, et al. Association of exposure to bisphenol A with obesity and cardiometabolic risk factors in children and adolescents. Int J Environ Health Res 2019;29(1):94-106. https://doi.org/10.1080/09603123.2018.1515896
  12. Warembourg C, Maitre L, Tamayo-Uria I, Fossati S, Roumeliotaki T, Aasvang GM, et al. Early-life environmental exposures and blood pressure in children. J Am Coll Cardiol 2019;74(10): 1317-1328. https://doi.org/10.1016/j.jacc.2019.06.069
  13. Buckley JP, Quiros-Alcala L, Teitelbaum SL, Calafat AM, Wolff MS, Engel SM. Associations of prenatal environmental phenol and phthalate biomarkers with respiratory and allergic dis- eases among children aged 6 and 7 years. Environ Int 2018; 115:79-88. https://doi.org/10.1016/j.envint.2018.03.016
  14. Rochester JR, Bolden AL. Bisphenol S and F: a systematic review and comparison of the hormonal activity of bisphenol a substitutes. Environ Health Perspect 2015;123(7):643-650. https://doi.org/10.1289/ehp.1408989
  15. Cabaton N, Chagnon MC, Lhuguenot JC, Cravedi JP, Zalko D. Disposition and metabolic profiling of bisphenol F in pregnant and nonpregnant rats. J Agric Food Chem 2006;54(26):10307- 10314. https://doi.org/10.1021/jf062250q
  16. Clark E. Sulfolane and sulfones. In: Kirk RE, Othmer DF, editors. Kirk-Othmer encyclopedia of chemical technology. New York: Wiley; 2000, p. 4-6.
  17. Liao C, Liu F, Kannan K. Bisphenol S, a new bisphenol analogue, in paper products and currency bills and its association with bisphenol A residues. Environ Sci Technol 2012;46(12):6515-6522. https://doi.org/10.1021/es300876n
  18. Thoene M, Dzika E, Gonkowski S, Wojtkiewicz J. Bisphenol S in food causes hormonal and obesogenic effects comparable to or worse than bisphenol A: a literature review. Nutrients 2020; 12(2):532. https://doi.org/10.3390/nu12020532
  19. Boas M, Feldt-Rasmussen U, Main KM. Thyroid effects of endocrine disrupting chemicals. Mol Cell Endocrinol 2012;355(2): 240-248. https://doi.org/10.1016/j.mce.2011.09.005
  20. Tilley SK, Fry RC. Hormone response pathways as responders to environmental contaminants and their roles in disease. In: Fry RC, editor. Systems biology in toxicology and environmental health. Boston: Academic Press; 2015, p. 225-238.
  21. Wu Y, Beland FA, Fang JL. Effect of triclosan, triclocarban, 2,2', 4,4'-tetrabromodiphenyl ether, and bisphenol A on the iodide uptake, thyroid peroxidase activity, and expression of genes involved in thyroid hormone synthesis. Toxicol In Vitro 2016; 32:310-319. https://doi.org/10.1016/j.tiv.2016.01.014
  22. Lee S, Kim C, Youn H, Choi K. Thyroid hormone disrupting potentials of bisphenol A and its analogues - in vitro comparison study employing rat pituitary (GH3) and thyroid follicular (FRTL-5) cells. Toxicol In Vitro 2017;40:297-304. https://doi.org/10.1016/j.tiv.2017.02.004
  23. Gentilcore D, Porreca I, Rizzo F, Ganbaatar E, Carchia E, Mallardo M, et al. Bisphenol A interferes with thyroid specific gene expression. Toxicology 2013;304:21-31. https://doi.org/10.1016/j.tox.2012.12.001
  24. Zhang DH, Zhou EX, Yang ZL. Waterborne exposure to BPS causes thyroid endocrine disruption in zebrafish larvae. PLoS One 2017;12(5):e0176927. https://doi.org/10.1371/journal.pone.0176927
  25. Mustieles V, Williams PL, Fernandez MF, Minguez-Alarcon L, Ford JB, Calafat AM, et al. Maternal and paternal preconception exposure to bisphenols and size at birth. Hum Reprod 2018;33(8):1528-1537. https://doi.org/10.1093/humrep/dey234
  26. Sanlidag B, Dalkan C, Yetkin O, Bahceciler NN. Evaluation of dose dependent maternal exposure to bisphenol A on thyroid functions in newborns. J Clin Med 2018;7(6):119. https://doi.org/10.3390/jcm7060119
  27. Kim W, Jang Y, Lim YH, Kim BN, Shin CH, Lee YA, et al. The effect of prenatal cadmium exposure on attention-deficit/hyperactivity disorder in 6-year-old children in Korea. J Prev Med Public Health 2020;53(1):29-36. https://doi.org/10.3961/jpmph.19.175
  28. Yang M, Kim SY, Lee SM, Chang SS, Kawamoto T, Jang JY, et al. Biological monitoring of bisphenol a in a Korean population. Arch Environ Contam Toxicol 2003;44(4):546-551. https://doi.org/10.1007/s00244-002-2124-0
  29. Bae S, Kim JH, Lim YH, Park HY, Hong YC. Associations of bi sphenol A exposure with heart rate variability and blood pressure. Hypertension 2012;60(3):786-793. https://doi.org/10.1161/HYPERTENSIONAHA.112.197715
  30. Hornung RW, Reed LD. Estimation of average concentration in the presence of nondetectable values. Appl Occup Environ Hyg 1990;5(1):46-51. https://doi.org/10.1080/1047322X.1990.10389587
  31. Mian AN, Schwartz GJ. Measurement and estimation of glomerular filtration rate in children. Adv Chronic Kidney Dis 2017; 24(6):348-356. https://doi.org/10.1053/j.ackd.2017.09.011
  32. Santos-Silva AP, de Moura EG, Pinheiro CR, Oliveira E, Lisboa PC. Short-term and long-term effects of bisphenol A (BPA) exposure during breastfeeding on the biochemical and endocrine profiles in rats. Horm Metab Res 2018;50(6):491-503. https://doi.org/10.1055/a-0628-6708
  33. Ullah A, Pirzada M, Jahan S, Ullah H, Razak S, Rauf N, et al. Prenatal BPA and its analogs BPB, BPF, and BPS exposure and reproductive axis function in the male offspring of Sprague Dawley rats. Hum Exp Toxicol 2019;38(12):1344-1365. https://doi.org/10.1177/0960327119862335
  34. Zhou B, Yang P, Deng YL, Zeng Q, Lu WQ, Mei SR. Prenatal exposure to bisphenol a and its analogues (bisphenol F and S) and ultrasound parameters of fetal growth. Chemosphere 2020;246:125805. https://doi.org/10.1016/j.chemosphere.2019.125805
  35. McCabe C, Anderson OS, Montrose L, Neier K, Dolinoy DC. Sexually dimorphic effects of early-life exposures to endocrine disruptors: sex-specific epigenetic reprogramming as a potential mechanism. Curr Environ Health Rep 2017;4(4):426-438. https://doi.org/10.1007/s40572-017-0170-z
  36. Jabbar A, Pingitore A, Pearce SH, Zaman A, Iervasi G, Razvi S. Thyroid hormones and cardiovascular disease. Nat Rev Cardiol 2017;14(1):39-55. https://doi.org/10.1038/nrcardio.2016.174
  37. Sur U, Erkekoglu P, Bulus AD, Andiran N, Kocer-Gumusel B. Oxidative stress markers, trace elements, and endocrine disrupting chemicals in children with Hashimoto's thyroiditis. Toxicol Mech Methods 2019;29(9):633-643. https://doi.org/10.1080/15376516.2019.1646367
  38. Derakhshan A, Shu H, Peeters RP, Kortenkamp A, Lindh CH, Demeneix B, et al. Association of urinary bisphenols and triclo- san with thyroid function during early pregnancy. Environ Int 2019;133(Pt A):105123. https://doi.org/10.1016/j.envint.2019.105123
  39. Higashihara N, Shiraishi K, Miyata K, Oshima Y, Minobe Y, Yamasaki K. Subacute oral toxicity study of bisphenol F based on the draft protocol for the "Enhanced OECD Test Guideline no. 407". Arch Toxicol 2007;81(12):825-832. https://doi.org/10.1007/s00204-007-0223-4
  40. Kibble JD. The big picture physiology: medical course & step 1 review; 2020 [cited Jul 1]. Available from: https://accessmedicine.mhmedical.com/content.aspx?bookid=2914§ionid=245544050.

피인용 문헌

  1. The Impact of Bisphenol A on Thyroid Function in Neonates and Children: A Systematic Review of the Literature vol.14, pp.1, 2021, https://doi.org/10.3390/nu14010168