DOI QR코드

DOI QR Code

Early-life exposure to endocrine disrupting chemicals associates with childhood obesity

  • Yang, Chunxue (State Key Laboratory of Environmental and Biological Analysis, Department of Chemistry, Hong Kong Baptist University) ;
  • Lee, Hin Kiu (State Key Laboratory of Environmental and Biological Analysis, Department of Chemistry, Hong Kong Baptist University) ;
  • Kong, Alice Pik Shan (Department of Medicine and Therapeutics, The Chinese University of Hong Kong, Prince of Wales Hospital) ;
  • Lim, Lee Ling (Department of Medicine and Therapeutics, The Chinese University of Hong Kong, Prince of Wales Hospital) ;
  • Cai, Zongwei (State Key Laboratory of Environmental and Biological Analysis, Department of Chemistry, Hong Kong Baptist University) ;
  • Chung, Arthur C.K. (State Key Laboratory of Environmental and Biological Analysis, Department of Chemistry, Hong Kong Baptist University)
  • Received : 2018.11.24
  • Accepted : 2018.12.18
  • Published : 2018.12.30

Abstract

Increasing prevalence of childhood obesity poses threats to the global health burden. Because this rising prevalence cannot be fully explained by traditional risk factors such as unhealthy diet and physical inactivity, early-life exposure to endocrine disrupting chemicals (EDCs) is recognized as emerging novel risk factors for childhood obesity. EDCs can disrupt the hormone-mediated metabolic pathways, affect children's growth and mediate the development of childhood obesity. Many organic pollutants are recently classified to be EDCs. In this review, we summarized the epidemiological and laboratory evidence related to EDCs and childhood obesity, and discussed the possible mechanisms underpinning childhood obesity and early-life exposure to non-persistent organic pollutants (phthalates, bisphenol A, triclosan) and persistent organic pollutants (dichlorodip henyltrichloroethane, polychlorinated biphenyls, polybrominated diphenyl ethers, per- and polyfluoroalkyl substances). Understanding the relationship between EDCs and childhood obesity helps to raise public awareness and formulate public health policy to protect the youth from exposure to the harmful effects of EDCs.

Keywords

Acknowledgement

Supported by : National Natural Science Foundation of China, Research Grant Council of Hong Kong, Hong Kong Baptist University, Hong Kong Health and Medical Research Fund, HKASO

References

  1. Daniels SR, Arnett DK, Eckel RH, Gidding SS, Hayman LL, Kumanyika S, et al. Overweight in children and adolescents: pathophysiology, consequences, prevention, and treatment. Circulation 2005;111:1999-2012. https://doi.org/10.1161/01.CIR.0000161369.71722.10
  2. Must A. Does overweight in childhood have an impact on adult health? Nutr Rev 2003;61:139-42. https://doi.org/10.1301/nr.2003.apr.139-142
  3. Berenson GS, Srinivasan SR, Bao W, Newman WP 3rd, Tracy RE, Wattigney WA. Association between multiple cardiovascular risk factors and atherosclerosis in children and young adults. The Bogalusa Heart Study. N Engl J Med 1998;338:1650-6. https://doi.org/10.1056/NEJM199806043382302
  4. Lauer RM, Lee J, Clarke WR. Factors affecting the relationship between childhood and adult cholesterol levels: the Muscatine Study. Pediatrics 1988;82:309-18.
  5. Lauer RM, Clarke WR. Childhood risk factors for high adult blood pressure: the Muscatine Study. Pediatrics 1989;84:633-41.
  6. Goodman E, Whitaker RC. A prospective study of the role of depression in the development and persistence of adolescent obesity. Pediatrics 2002;110:497-504. https://doi.org/10.1542/peds.110.3.497
  7. GBD 2015 Obesity Collaborators, Afshin A, Forouzanfar MH, Reitsma MB, Sur P, Estep K, et al. Health effects of overweight and obesity in 195 countries over 25 years. N Engl J Med 2017;377:13-27. https://doi.org/10.1056/NEJMoa1614362
  8. Heymsfield SB, Wadden TA. Mechanisms, pathophysiology, and management of obesity. N Engl J Med 2017;376:254-66. https://doi.org/10.1056/NEJMra1514009
  9. Janssen I, Katzmarzyk PT, Boyce WF, Vereecken C, Mulvihill C, Roberts C, et al. Comparison of overweight and obesity prevalence in school-aged youth from 34 countries and their relationships with physical activity and dietary patterns. Obes Rev 2005;6:123-32. https://doi.org/10.1111/j.1467-789X.2005.00176.x
  10. Anderson PM, Butcher KE. Childhood obesity: trends and potential causes. Future Child 2006;16:19-45.
  11. La Merrill M, Birnbaum LS. Childhood obesity and environmental chemicals. Mt Sinai J Med 2011;78:22-48. https://doi.org/10.1002/msj.20229
  12. Valvi D, Mendez MA, Martinez D, Grimalt JO, Torrent M, Sunyer J, et al. Prenatal concentrations of polychlorinated biphenyls, DDE, and DDT and overweight in children: a prospective birth cohort study. Environ Health Perspect 2012;120:451-7. https://doi.org/10.1289/ehp.1103862
  13. Scinicariello F, Buser MC. Urinary polycyclic aromatic hydrocarbons and childhood obesity: NHANES (2001-2006). Environ Health Perspect 2014;122:299-303. https://doi.org/10.1289/ehp.1307234
  14. Verhulst SL, Nelen V, Hond ED, Koppen G, Beunckens C, Vael C, et al. Intrauterine exposure to environmental pollutants and body mass index during the first 3 years of life. Environ Health Perspect 2009;117:122-6. https://doi.org/10.1289/ehp.0800003
  15. Halldorsson TI, Rytter D, Haug LS, Bech BH, Danielsen I, Becher G, et al. Prenatal exposure to perfluorooctanoate and risk of overweight at 20 years of age: a prospective cohort study. Environ Health Perspect 2012;120:668-73. https://doi.org/10.1289/ehp.1104034
  16. Zoeller RT, Brown TR, Doan LL, Gore AC, Skakkebaek NE, Soto AM, et al. Endocrine-disrupting chemicals and public health protection: a statement of principles from The Endocrine Society. Endocrinology 2012;153:4097-110. https://doi.org/10.1210/en.2012-1422
  17. Manickum T, John W. Occurrence, fate and environmental risk assessment of endocrine disrupting compounds at the wastewater treatment works in Pietermaritzburg (South Africa). Sci Total Environ 2014;468-469:584-97. https://doi.org/10.1016/j.scitotenv.2013.08.041
  18. Rudel RA, Camann DE, Spengler JD, Korn LR, Brody JG. Phthalates, alkylphenols, pesticides, polybrominated diphenyl ethers, and other endocrine-disrupting compounds in indoor air and dust. Environ Sci Technol 2003;37:4543-53. https://doi.org/10.1021/es0264596
  19. Geyer HJ, Rimkus GG, Scheunert I, Kaune A, Schramm KW, Kettrup A, et al. Bioaccumulation and occurrence of endocrine-disrupting chemicals (EDCs), persistent organic pollutants (POPs), and other organic compounds in fish and other organisms including humans. In: Beek B, Bohling S, editors. Bioaccumulation - New Aspects and Developments. Berlin: Springer; 2000. p. 1-166.
  20. Mendez MA, Garcia-Esteban R, Guxens M, Vrijheid M, Kogevinas M, Goni F, et al. Prenatal organochlorine compound exposure, rapid weight gain, and overweight in infancy. Environ Health Perspect 2011;119:272-8. https://doi.org/10.1289/ehp.1002169
  21. Romano ME, Savitz DA, Braun JM. Challenges and future directions to evaluating the association between prenatal exposure to endocrine disrupting chemicals and childhood obesity. Curr Epidemiol Rep 2014;1:57-66. https://doi.org/10.1007/s40471-014-0007-3
  22. Agay-Shay K, Martinez D, Valvi D, Garcia-Esteban R, Basagana X, Robinson O, et al. Exposure to endocrinedisrupting chemicals during pregnancy and weight at 7 years of age: a multi-pollutant approach. Environ Health Perspect 2015;123:1030-7. https://doi.org/10.1289/ehp.1409049
  23. Schettler T. Human exposure to phthalates via consumer products. Int J Androl 2006;29:134-9. https://doi.org/10.1111/j.1365-2605.2005.00567.x
  24. Trasande L, Sathyanarayana S, Jo Messito M, S Gross R, Attina TM, Mendelsohn AL. Phthalates and the diets of U.S. children and adolescents. Environ Res 2013;126:84-90. https://doi.org/10.1016/j.envres.2013.07.007
  25. Sathyanarayana S, Karr CJ, Lozano P, Brown E, Calafat AM, Liu F, et al. Baby care products: possible sources of infant phthalate exposure. Pediatrics 2008;121:e260-8. https://doi.org/10.1542/peds.2006-3766
  26. Bornehag CG, Lundgren B, Weschler CJ, Sigsgaard T, Hagerhed-Engman L, Sundell J. Phthalates in indoor dust and their association with building characteristics. Environ Health Perspect 2005;113:1399-404. https://doi.org/10.1289/ehp.7809
  27. Braun JM, Just AC, Williams PL, Smith KW, Calafat AM, Hauser R. Personal care product use and urinary phthalate metabolite and paraben concentrations during pregnancy among women from a fertility clinic. J Expo Sci Environ Epidemiol 2014;24:459-66. https://doi.org/10.1038/jes.2013.69
  28. Mankidy R, Wiseman S, Ma H, Giesy JP. Biological impact of phthalates. Toxicol Lett 2013;217:50-8. https://doi.org/10.1016/j.toxlet.2012.11.025
  29. Wolff MS, Engel SM, Berkowitz GS, Ye X, Silva MJ, Zhu C, et al. Prenatal phenol and phthalate exposures and birth outcomes. Environ Health Perspect 2008;116:1092-7. https://doi.org/10.1289/ehp.11007
  30. Agency EP. Assessing and Managing Chemicals under TSCA. Phthalates [Internet]. Washington, DC: U.S. Environmental Protection Agency; 2012 Mar 14 [cited 2018 Nov 7]. Available from: https://www.epa.gov/assessingand- managing-chemicals-under-tsca/phthalates.
  31. Dodson RE, Nishioka M, Standley LJ, Perovich LJ, Brody JG, Rudel RA. Endocrine disruptors and asthma-associated chemicals in consumer products. Environ Health Perspect 2012;120:935-43. https://doi.org/10.1289/ehp.1104052
  32. Buser MC, Murray HE, Scinicariello F. Age and sex differences in childhood and adulthood obesity association with phthalates: analyses of NHANES 2007-2010. Int J Hyg Environ Health 2014;217:687-94. https://doi.org/10.1016/j.ijheh.2014.02.005
  33. Zhang Y, Meng X, Chen L, Li D, Zhao L, Zhao Y, et al. Age and sex-specific relationships between phthalate exposures and obesity in Chinese children at puberty. PLoS One 2014;9:e104852. https://doi.org/10.1371/journal.pone.0104852
  34. Kim JH, Park H, Lee J, Cho G, Choi S, Choi G, et al. Association of diethylhexyl phthalate with obesity-related markers and body mass change from birth to 3 months of age. J Epidemiol Community Health 2016;70:466-72. https://doi.org/10.1136/jech-2015-206315
  35. Hatch EE, Nelson JW, Qureshi MM, Weinberg J, Moore LL, Singer M, et al. Association of urinary phthalate metabolite concentrations with body mass index and waist circumference: a cross-sectional study of NHANES data, 1999-2002. Environ Health 2008;7:27. https://doi.org/10.1186/1476-069X-7-27
  36. Teitelbaum SL, Mervish N, Moshier EL, Vangeepuram N, Galvez MP, Calafat AM, et al. Associations between phthalate metabolite urinary concentrations and body size measures in New York City children. Environ Res 2012;112:186-93. https://doi.org/10.1016/j.envres.2011.12.006
  37. Deierlein AL, Wolff MS, Pajak A, Pinney SM, Windham GC, Galvez MP, et al. Longitudinal associations of phthalate exposures during childhood and body size measurements in young girls. Epidemiology 2016;27:492-9. https://doi.org/10.1097/EDE.0000000000000489
  38. Smerieri A, Testa C, Lazzeroni P, Nuti F, Grossi E, Cesari S, et al. Di-(2-ethylhexyl) phthalate metabolites in urine show age-related changes and associations with adiposity and parameters of insulin sensitivity in childhood. PLoS One 2015;10:e0117831. https://doi.org/10.1371/journal.pone.0117831
  39. Schmidt JS, Schaedlich K, Fiandanese N, Pocar P, Fischer B. Effects of di(2-ethylhexyl) phthalate (DEHP) on female fertility and adipogenesis in C3H/N mice. Environ Health Perspect 2012;120:1123-9. https://doi.org/10.1289/ehp.1104016
  40. Valvi D, Casas M, Romaguera D, Monfort N, Ventura R, Martinez D, et al. Prenatal phthalate exposure and childhood growth and blood pressure: evidence from the Spanish INMA-Sabadell Birth Cohort Study. Environ Health Perspect 2015;123:1022-9. https://doi.org/10.1289/ehp.1408887
  41. von Goetz N, Wormuth M, Scheringer M, Hungerbuhler K. Bisphenol a: how the most relevant exposure sources contribute to total consumer exposure. Risk Anal 2010;30:473-87. https://doi.org/10.1111/j.1539-6924.2009.01345.x
  42. Ehrlich S, Calafat AM, Humblet O, Smith T, Hauser R. Handling of thermal receipts as a source of exposure to bisphenol A. JAMA 2014;311:859-60. https://doi.org/10.1001/jama.2013.283735
  43. Geens T, Apelbaum TZ, Goeyens L, Neels H, Covaci A. Intake of bisphenol A from canned beverages and foods on the Belgian market. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 2010;27:1627-37. https://doi.org/10.1080/19440049.2010.508183
  44. Thayer KA, Doerge DR, Hunt D, Schurman SH, Twaddle NC, Churchwell MI, et al. Pharmacokinetics of bisphenol A in humans following a single oral administration. Environ Int 2015;83:107-15. https://doi.org/10.1016/j.envint.2015.06.008
  45. Hoepner LA, Whyatt RM, Widen EM, Hassoun A, Oberfield SE, Mueller NT, et al. Bisphenol A and Adiposity in an Inner-City Birth Cohort. Environ Health Perspect 2016;124:1644-50. https://doi.org/10.1289/EHP205
  46. Volberg V, Harley K, Calafat AM, Dave V, McFadden J, Eskenazi B, et al. Maternal bisphenol a exposure during pregnancy and its association with adipokines in Mexican-American children. Environ Mol Mutagen 2013;54:621-8. https://doi.org/10.1002/em.21803
  47. Trasande L, Attina TM, Blustein J. Association between urinary bisphenol A concentration and obesity prevalence in children and adolescents. JAMA 2012;308:1113-21. https://doi.org/10.1001/2012.jama.11461
  48. Wang HX, Zhou Y, Tang CX, Wu JG, Chen Y, Jiang QW. Association between bisphenol A exposure and body mass index in Chinese school children: a cross-sectional study. Environ Health 2012;11:79. https://doi.org/10.1186/1476-069X-11-79
  49. Durando M, Kass L, Piva J, Sonnenschein C, Soto AM, Luque EH, et al. Prenatal bisphenol A exposure induces preneoplastic lesions in the mammary gland in Wistar rats. Environ Health Perspect 2007;115:80-6. https://doi.org/10.1289/ehp.9282
  50. Somm E, Schwitzgebel VM, Toulotte A, Cederroth CR, Combescure C, Nef S, et al. Perinatal exposure to bisphenol a alters early adipogenesis in the rat. Environ Health Perspect 2009;117:1549-55. https://doi.org/10.1289/ehp.11342
  51. Angle BM, Do RP, Ponzi D, Stahlhut RW, Drury BE, Nagel SC, et al. Metabolic disruption in male mice due to fetal exposure to low but not high doses of bisphenol A (BPA): evidence for effects on body weight, food intake, adipocytes, leptin, adiponectin, insulin and glucose regulation. Reprod Toxicol 2013;42:256-68. https://doi.org/10.1016/j.reprotox.2013.07.017
  52. Zhao C, Xie P, Yong T, Wang H, Chung ACK, Cai Z. MALDI-MS imaging reveals asymmetric spatial distribution of lipid metabolites from bisphenol S-induced nephrotoxicity. Anal Chem 2018;90:3196-204. https://doi.org/10.1021/acs.analchem.7b04540
  53. 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;123:643-50. https://doi.org/10.1289/ehp.1408989
  54. Liu B, Lehmler HJ, Sun Y, Xu G, Liu Y, Zong G, et al. Bisphenol A substitutes and obesity in US adults: analysis of a population-based, cross-sectional study. Lancet Planet Health 2017;1:e114-22. https://doi.org/10.1016/S2542-5196(17)30049-9
  55. Rodricks JV, Swenberg JA, Borzelleca JF, Maronpot RR, Shipp AM. Triclosan: a critical review of the experimental data and development of margins of safety for consumer products. Crit Rev Toxicol 2010;40:422-84. https://doi.org/10.3109/10408441003667514
  56. Sandborgh-Englund G, Adolfsson-Erici M, Odham G, Ekstrand J. Pharmacokinetics of triclosan following oral ingestion in humans. J Toxicol Environ Health A 2006;69:1861-73. https://doi.org/10.1080/15287390600631706
  57. Calafat AM, Ye X, Wong LY, Reidy JA, Needham LL. Urinary concentrations of triclosan in the U.S. population: 2003- 2004. Environ Health Perspect 2008;116:303-7. https://doi.org/10.1289/ehp.10768
  58. James MO, Li W, Summerlot DP, Rowland-Faux L, Wood CE. Triclosan is a potent inhibitor of estradiol and estrone sulfonation in sheep placenta. Environ Int 2010;36:942-9. https://doi.org/10.1016/j.envint.2009.02.004
  59. Rodriguez PE, Sanchez MS. Maternal exposure to triclosan impairs thyroid homeostasis and female pubertal development in Wistar rat offspring. J Toxicol Environ Health A 2010;73:1678-88. https://doi.org/10.1080/15287394.2010.516241
  60. Rabaglino MB, Moreira-Espinoza MJ, Lopez JP, Garcia NH, Beltramo D. Maternal Triclosan consumption alters the appetite regulatory network on Wistar rat offspring and predispose to metabolic syndrome in the adulthood. Endocr J 2016;63:1007-16. https://doi.org/10.1507/endocrj.EJ16-0257
  61. Li S, Zhao J, Wang G, Zhu Y, Rabito F, Krousel-Wood M, et al. Urinary triclosan concentrations are inversely associated with body mass index and waist circumference in the US general population: Experience in NHANES 2003-2010. Int J Hyg Environ Health 2015;218:401-6. https://doi.org/10.1016/j.ijheh.2015.03.004
  62. Shapiro GD, Arbuckle TE, Ashley-Martin J, Fraser WD, Fisher M, Bouchard MF, et al. Associations between maternal triclosan concentrations in early pregnancy and gestational diabetes mellitus, impaired glucose tolerance, gestational weight gain and fetal markers of metabolic function. Environ Res 2018;161:554-61. https://doi.org/10.1016/j.envres.2017.12.001
  63. Kalloo G, Calafat AM, Chen A, Yolton K, Lanphear BP, Braun JM. Early life Triclosan exposure and child adiposity at 8 Years of age: a prospective cohort study. Environ Health 2018;17:24. https://doi.org/10.1186/s12940-018-0366-1
  64. Yang C, Kong APS, Cai Z, Chung ACK. Persistent organic pollutants as risk factors for obesity and diabetes. Curr Diab Rep 2017;17:132. https://doi.org/10.1007/s11892-017-0966-0
  65. La Merrill M, Emond C, Kim MJ, Antignac JP, Le Bizec B, Clement K, et al. Toxicological function of adipose tissue: focus on persistent organic pollutants. Environ Health Perspect 2013;121:162-9. https://doi.org/10.1289/ehp.1205485
  66. Prato M, Polimeni M, Giribaldi G. DDT as anti-malaria tool: the bull in the China shop or the elephant in the room? London: INTECH Open Access Publisher; 2013.
  67. Zhang C, Liu L, Ma Y, Li F. Using isomeric and metabolic ratios of DDT to identify the sources and fate of DDT in Chinese agricultural topsoil. Environ Sci Technol 2018;52:1990-6. https://doi.org/10.1021/acs.est.7b05877
  68. Ben Rhouma K, Tebourbi O, Krichah R, Sakly M. Reproductive toxicity of DDT in adult male rats. Hum Exp Toxicol 2001;20:393-7. https://doi.org/10.1191/096032701682692946
  69. Tiemann U. In vivo and in vitro ef fects of the organochlorine pesticides DDT, TCPM, methoxychlor, and lindane on the female reproductive tract of mammals: a review. Reprod Toxicol 2008;25:316-26. https://doi.org/10.1016/j.reprotox.2008.03.002
  70. Kim J, Sun Q, Yue Y, Yoon KS, Whang KY, Marshall Clark J, et al. 4,4'-Dichlorodiphenyltrichloroethane (DDT) and 4,4'-dichlorodiphenyldichloroethylene (DDE) promote adipogenesis in 3T3-L1 adipocyte cell culture. Pestic Biochem Physiol 2016;131:40-5. https://doi.org/10.1016/j.pestbp.2016.01.005
  71. Strong AL, Shi Z, Strong MJ, Miller DF, Rusch DB, Buechlein AM, et al. Effects of the endocrine-disrupting chemical DDT on self-renewal and differentiation of human mesenchymal stem cells. Environ Health Perspect 2015;123:42-8. https://doi.org/10.1289/ehp.1408188
  72. Tang-Peronard JL, Heitmann BL, Andersen HR, Steuerwald U, Grandjean P, Weihe P, et al. Association between prenatal polychlorinated biphenyl exposure and obesity development at ages 5 and 7 y: a prospective cohort study of 656 children from the Faroe Islands. Am J Clin Nutr 2014;99:5-13. https://doi.org/10.3945/ajcn.113.066720
  73. Valvi D, Mendez MA, Garcia-Esteban R, Ballester F, Ibarluzea J, Goni F, et al. Prenatal exposure to persistent organic pollutants and rapid weight gain and overweight in infancy. Obesity (Silver Spring) 2014;22:488-96. https://doi.org/10.1002/oby.20603
  74. Warner M, Wesselink A, Harley KG, Bradman A, Kogut K, Eskenazi B. Prenatal exposure to dichlorodiphenyltrichloroethane and obesity at 9 years of age in the CHAMACOS study cohort. Am J Epidemiol 2014;179:1312-22. https://doi.org/10.1093/aje/kwu046
  75. La Merrill M, Cirillo PM, Terry MB, Krigbaum NY, Flom JD, Cohn BA. Prenatal exposure to the pesticide DDT and hypertension diagnosed in women before age 50: a longitudinal birth cohort study. Environ Health Perspect 2013;121:594-9. https://doi.org/10.1289/ehp.1205921
  76. Kezios KL, Liu X, Cirillo PM, Cohn BA, Kalantzi OI, Wang Y, et al. Dichlorodiphenyltrichloroethane (DDT), DDT metabolites and pregnancy outcomes. Reprod Toxicol 2013;35:156-64. https://doi.org/10.1016/j.reprotox.2012.10.013
  77. Liu C, Shi Y, Li H, Wang Y, Yang K. p,p'-DDE disturbs the homeostasis of thyroid hormones via thyroid hormone receptors, transthyretin, and hepatic enzymes. Horm Metab Res 2011;43:391-6. https://doi.org/10.1055/s-0031-1277135
  78. Grandone A, Santoro N, Coppola F, Calabro P, Perrone L, Del Giudice EM. Thyroid function derangement and childhood obesity: an Italian experience. BMC Endocr Disord 2010;10:8. https://doi.org/10.1186/1472-6823-10-8
  79. Harrad SJ, Sewart AP, Alcock R, Boumphrey R, Burnett V, Duarte-Davidson R, et al. Polychlorinated biphenyls (PCBs) in the British environment: sinks, sources and temporal trends. Environ Pollut 1994;85:131-46. https://doi.org/10.1016/0269-7491(94)90079-5
  80. Porta M, Zumeta E. Implementing the stockholm treaty on persistent organic pollutants. Occup Environ Med 2002;59:651-2. https://doi.org/10.1136/oem.59.10.651
  81. Muller MH, Polder A, Brynildsrud OB, Karimi M, Lie E, Manyilizu WB, et al. Organochlorine pesticides (OCPs) and polychlorinated biphenyls (PCBs) in human breast milk and associated health risks to nursing infants in Northern Tanzania. Environ Res 2017;154:425-34. https://doi.org/10.1016/j.envres.2017.01.031
  82. Arinaitwe K, Muir DCG, Kiremire BT, Fellin P, Li H, Teixeira C, et al. Prevalence and sources of polychlorinated biphenyls in the atmospheric environment of Lake Victoria, East Africa. Chemosphere 2018;193:343-50. https://doi.org/10.1016/j.chemosphere.2017.11.041
  83. Kania-Korwel I, Lehmler HJ. Toxicokinetics of chiral polychlorinated biphenyls across different species--a review. Environ Sci Pollut Res Int 2016;23:2058-80. https://doi.org/10.1007/s11356-015-4383-0
  84. Terzaghi E, Zanardini E, Morosini C, Raspa G, Borin S, Mapelli F, et al. Rhizoremediation half-lives of PCBs: Role of congener composition, organic carbon forms, bioavailability, microbial activity, plant species and soil conditions, on the prediction of fate and persistence in soil. Sci Total Environ 2018;612:544-60. https://doi.org/10.1016/j.scitotenv.2017.08.189
  85. Bourez S, Van den Daelen C, Le Lay S, Poupaert J, Larondelle Y, Thome JP, et al. The dynamics of accumulation of PCBs in cultured adipocytes vary with the cell lipid content and the lipophilicity of the congener. Toxicol Lett 2013;216:40-6. https://doi.org/10.1016/j.toxlet.2012.09.027
  86. Arsenescu V, Arsenescu RI, King V, Swanson H, Cassis LA. Polychlorinated biphenyl-77 induces adipocyte differentiation and proinflammatory adipokines and promotes obesity and atherosclerosis. Environ Health Perspect 2008;116:761-8. https://doi.org/10.1289/ehp.10554
  87. Lignell S, Aune M, Darnerud PO, Hanberg A, Larsson SC, Glynn A. Prenatal exposure to polychlorinated biphenyls (PCBs) and polybrominated diphenyl ethers (PBDEs) may influence birth weight among infants in a Swedish cohort with background exposure: a cross-sectional study. Environ Health 2013;12:44. https://doi.org/10.1186/1476-069X-12-44
  88. Wohlfahrt-Veje C, Audouze K, Brunak S, Antignac JP, le Bizec B, Juul A, et al. Polychlorinated dibenzo-p-dioxins, furans, and biphenyls (PCDDs/PCDFs and PCBs) in breast milk and early childhood growth and IGF1. Reproduction 2014;147:391-9. https://doi.org/10.1530/REP-13-0422
  89. Dallaire R, Dewailly E, Ayotte P, Forget-Dubois N, Jacobson SW, Jacobson JL, et al. Growth in Inuit children exposed to polychlorinated biphenyls and lead during fetal development and childhood. Environ Res 2014;134:17-23. https://doi.org/10.1016/j.envres.2014.06.023
  90. Iszatt N, Stigum H, Verner MA, White RA, Govarts E, Murinova LP, et al. Prenatal and postnatal exposure to persistent organic pollutants and infant growth: a pooled analysis of seven European birth cohorts. Environ Health Perspect 2015;123:730-6. https://doi.org/10.1289/ehp.1308005
  91. Besis A, Samara C. Polybrominated diphenyl ethers (PBDEs) in the indoor and outdoor environments--a review on occurrence and human exposure. Environ Pollut 2012;169:217-29. https://doi.org/10.1016/j.envpol.2012.04.009
  92. Abbasi G, Buser AM, Soehl A, Murray MW, Diamond ML. Stocks and flows of PBDEs in products from use to waste in the U.S. and Canada from 1970 to 2020. Environ Sci Technol 2015;49:1521-8. https://doi.org/10.1021/es504007v
  93. Geyer HJ, Schramm KW, Darnerud PO, Aune M, Feicht EA, Fried KW, et al. Terminal elimination half-lives of the brominated flame retardants TBBPA, HBCD, and lower brominated PBDEs in humans. Organohalogen Compounds 2004;66:3867-72.
  94. Toms LM, Harden F, Paepke O, Hobson P, Ryan JJ, Mueller JF. Higher accumulation of polybrominated diphenyl ethers in infants than in adults. Environ Sci Technol 2008;42:7510-5. https://doi.org/10.1021/es800719v
  95. Darrow LA, Jacobson MH, Preston EV, Lee GE, Panuwet P, Hunter RE Jr, et al. Predictors of serum polybrominated diphenyl ether (PBDE) concentrations among children aged 1-5 years. Environ Sci Technol 2017;51:645-54. https://doi.org/10.1021/acs.est.6b04696
  96. Erkin-Cakmak A, Harley KG, Chevrier J, Bradman A, Kogut K, Huen K, et al. In utero and childhood polybrominated diphenyl ether exposures and body mass at age 7 years: the CHAMACOS study. Environ Health Perspect 2015;123:636-42. https://doi.org/10.1289/ehp.1408417
  97. Vuong AM, Braun JM, Sjodin A, Webster GM, Yolton K, Lanphear BP, et al. Prenatal polybrominated diphenyl ether exposure and body mass index in children up to 8 years of age. Environ Health Perspect 2016;124:1891-7. https://doi.org/10.1289/EHP139
  98. Tung EW, Boudreau A, Wade MG, Atlas E. Induction of adipocyte differentiation by polybrominated diphenyl ethers (PBDEs) in 3T3-L1 cells. PLoS One 2014;9:e94583. https://doi.org/10.1371/journal.pone.0094583
  99. Kamstra JH, Hruba E, Blumberg B, Janesick A, Mandrup S, Hamers T, et al. Transcriptional and epigenetic mechanisms underlying enhanced in vitro adipocyte differentiation by the brominated flame retardant BDE-47. Environ Sci Technol 2014;48:4110-9. https://doi.org/10.1021/es405524b
  100. Chunxue Yang, Chi-Ming Wong, Juntong Wei, Arthur C.K. Chung, Zongwei Cai. The brominated flame retardant BDE 47 upregulates purine metabolism and mitochondrial respiration to promote adipocyte differentiation. Science of The Total Environment 2018;644:1312-22. https://doi.org/10.1016/j.scitotenv.2018.07.087
  101. McIntyre RL, Kenerson HL, Subramanian S, Wang SA, Kazami M, Stapleton HM, et al. Polybrominated diphenyl ether congener, BDE-47, impairs insulin sensitivity in mice with liver-specific Pten deficiency. BMC Obes 2015;2:3. https://doi.org/10.1186/s40608-014-0031-3
  102. Wang D, Yan J, Teng M, Yan S, Zhou Z, Zhu W. In utero and lactational exposure to BDE-47 promotes obesity development in mouse offspring fed a high-fat diet: impaired lipid metabolism and intestinal dysbiosis. Arch Toxicol 2018;92:1847-60. https://doi.org/10.1007/s00204-018-2177-0
  103. Suvorov A, Battista MC, Takser L. Perinatal exposure to low-dose 2,2',4,4'-tetrabromodiphenyl ether affects growth in rat offspring: what is the role of IGF-1? Toxicology 2009;260:126-31. https://doi.org/10.1016/j.tox.2009.03.018
  104. Ross MG, Desai M, Khorram O, McKnight RA, Lane RH, Torday J. Gestational programming of offspring obesity: a potential contributor to Alzheimer's disease. Curr Alzheimer Res 2007;4:213-7. https://doi.org/10.2174/156720507780362056
  105. Buck RC, Franklin J, Berger U, Conder JM, Cousins IT, de Voogt P, et al. Perfluoroalkyl and polyfluoroalkyl substances in the environment: terminology, classification, and origins. Integr Environ Assess Manag 2011;7:513-41. https://doi.org/10.1002/ieam.258
  106. Olsen GW, Burris JM, Ehresman DJ, Froehlich JW, Seacat AM, Butenhoff JL, et al. Half-life of serum elimination of perfluorooctanesulfonate,perfluorohexanesulfonate, and perfluorooctanoate in retired fluorochemical production workers. Environ Health Perspect 2007;115:1298-305. https://doi.org/10.1289/ehp.10009
  107. Mora AM, Oken E, Rifas-Shiman SL, Webster TF, Gillman MW, Calafat AM, et al. Prenatal exposure to perfluoroalkyl substances and adiposity in early and mid-childhood. Environ Health Perspect 2017;125:467-73. https://doi.org/10.1289/EHP246
  108. Braun JM, Chen A, Romano ME, Calafat AM, Webster GM, Yolton K, et al. Prenatal perfluoroalkyl substance exposure and child adiposity at 8 years of age: The HOME study. Obesity (Silver Spring) 2016;24:231-7. https://doi.org/10.1002/oby.21258
  109. Worley RR, Moore SM, Tierney BC, Ye X, Calafat AM, Campbell S, et al. Per- and polyfluoroalkyl substances in human serum and urine samples from a residentially exposed community. Environ Int 2017;106:135-43. https://doi.org/10.1016/j.envint.2017.06.007
  110. Manzano-Salgado CB, Casas M, Lopez-Espinosa MJ, Ballester F, Iniguez C, Martinez D, et al. Prenatal exposure to perfluoroalkyl substances and cardiometabolic risk in children from the Spanish INMA Birth Cohort Study. Environ Health Perspect 2017;125:097018. https://doi.org/10.1289/EHP1330
  111. Geiger SD, Xiao J, Ducatman A, Frisbee S, Innes K, Shankar A. The association between PFOA, PFOS and serum lipid levels in adolescents. Chemosphere 2014;98:78-83. https://doi.org/10.1016/j.chemosphere.2013.10.005
  112. Fleisch AF, Rifas-Shiman SL, Mora AM, Calafat AM, Ye X, Luttmann-Gibson H, et al. Early-life exposure to perfluoroalkyl substances and childhood metabolic function. Environ Health Perspect 2017;125:481-7. https://doi.org/10.1289/EHP303
  113. Hines EP, White SS, Stanko JP, Gibbs-Flournoy EA, Lau C, Fenton SE. Phenotypic dichotomy following developmental exposure to perfluorooctanoic acid (PFOA) in female CD-1 mice: Low doses induce elevated serum leptin and insulin, and overweight in mid-life. Mol Cell Endocrinol 2009;304:97-105. https://doi.org/10.1016/j.mce.2009.02.021
  114. Wang L, Wang Y, Liang Y, Li J, Liu Y, Zhang J, et al. PFOS induced lipid metabolism disturbances in BALB/c mice through inhibition of low density lipoproteins excretion. Sci Rep 2014;4:4582.
  115. Xu J, Shimpi P, Armstrong L, Salter D, Slitt AL. PFOS induces adipogenesis and glucose uptake in association with activation of Nrf2 signaling pathway. Toxicol Appl Pharmacol 2016;290:21-30. https://doi.org/10.1016/j.taap.2015.11.002
  116. Watkins AM, Wood CR, Lin MT, Abbott BD. The effects of perfluorinated chemicals on adipocyte differentiation in vitro. Mol Cell Endocrinol 2015;400:90-101. https://doi.org/10.1016/j.mce.2014.10.020
  117. Ngo HT, Hetland RB, Sabaredzovic A, Haug LS, Steffensen IL. In utero exposure to perfluorooctanoate (PFOA) or perfluorooctane sulfonate (PFOS) did not increase body weight or intestinal tumorigenesis in multiple intestinal neoplasia (Min/+) mice. Environ Res 2014;132:251-63. https://doi.org/10.1016/j.envres.2014.03.033
  118. Nunnari J, Suomalainen A. Mitochondria: in sickness and in health. Cell 2012;148:1145-59. https://doi.org/10.1016/j.cell.2012.02.035
  119. Itani SI, Ruderman NB, Schmieder F, Boden G. Lipidinduced insulin resistance in human muscle is associated with changes in diacylglycerol, protein kinase C, and IkappaB-alpha. Diabetes 2002;51:2005-11. https://doi.org/10.2337/diabetes.51.7.2005
  120. Lim S, Cho YM, Park KS, Lee HK. Persistent organic pollutants, mitochondrial dysfunction, and metabolic syndrome. Ann N Y Acad Sci 2010;1201:166-76. https://doi.org/10.1111/j.1749-6632.2010.05622.x
  121. Wahlang B, Prough RA, Falkner KC, Hardesty JE, Song M, Clair HB, et al. Polychlorinated biphenyl-xenobiotic nuclear receptor interactions regulate energy metabolism, behavior, and inflammation in non-alcoholic-steatohepatitis. Toxicol Sci 2016;149:396-410. https://doi.org/10.1093/toxsci/kfv250
  122. Ibrahim MM, Fjære E, Lock EJ, Naville D, Amlund H, Meugnier E, et al. Chronic consumption of farmed salmon containing persistent organic pollutants causes insulin resistance and obesity in mice. PLoS One 2011;6:e25170. https://doi.org/10.1371/journal.pone.0025170
  123. Furukawa S, Fujita T, Shimabukuro M, Iwaki M, Yamada Y, Nakajima Y, et al. Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest 2004;114:1752-61. https://doi.org/10.1172/JCI21625
  124. Houstis N, Rosen ED. Reactive oxygen species play a causal role in multiple forms of insulin resistance. 2006;Nature 440:944-8. https://doi.org/10.1038/nature04634
  125. Tormos KV, Anso E, Hamanaka RB, Eisenbart J, Joseph J, Kalyanaraman B, et al. Mitochondrial complex III ROS regulate adipocyte differentiation. Cell Metab 2011;14:537-44. https://doi.org/10.1016/j.cmet.2011.08.007
  126. Sankhla M, Sharma TK, Mathur K, Rathor JS, Butolia V, Gadhok AK, et al. Relationship of oxidative stress with obesity and its role in obesity induced metabolic syndrome. Clin Lab 2012;58:385-92.
  127. Matsuda M, Shimomura I. Increased oxidative stress in obesity: implications for metabolic syndrome, diabetes, hypertension, dyslipidemia, atherosclerosis, and cancer. Obes Res Clin Pract 2013;7:e330-41. https://doi.org/10.1016/j.orcp.2013.05.004
  128. Savini I, Gasperi V, Catani MV. In: Marcello MA, Cunha LL, Batista FD, Ward LS. Oxidative stress and obesity. Cham (Switzerland): Springer International Publishing; 2016:65-86.
  129. Aly HA, Domenech O. Cytotoxicity and mitochondrial dysfunction of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in isolated rat hepatocytes. Toxicol Lett 2009;191:79-87. https://doi.org/10.1016/j.toxlet.2009.08.008
  130. Madsen MS, Siersbæk R, Boergesen M, Nielsen R, Mandrup S. Peroxisome proliferator-activated receptor ${\gamma}$ and $C/EBP{\alpha}$ synergistically activate key metabolic adipocyte genes by assisted loading. Mol Cell Biol 2014;34:939-54. https://doi.org/10.1128/MCB.01344-13
  131. Ali AT, Hochfeld WE, Myburgh R, Pepper MS. Adipocyte and adipogenesis. Eur J Cell Biol 2013;92:229-36. https://doi.org/10.1016/j.ejcb.2013.06.001
  132. Valavanidis A, Vlachogianni T, Fiotakis C. 8-hydroxy-2'-deoxyguanosine (8-OHdG): A critical biomarker of oxidative stress and carcinogenesis. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev 2009;27:120-39. https://doi.org/10.1080/10590500902885684
  133. Tagliaferri S, Caglieri A, Goldoni M, Pinelli S, Alinovi R, Poli D, et al. Low concentrations of the brominated flame retardants BDE-47 and BDE-99 induce synergistic oxidative stress-mediated neurotoxicity in human neuroblastoma cells. Toxicol In Vitro 2010;24:116-22. https://doi.org/10.1016/j.tiv.2009.08.020
  134. He P, He W, Wang A, Xia T, Xu B, Zhang M, et al. PBDE-47-induced oxidative stress, DNA damage and apoptosis in primary cultured rat hippocampal neurons. Neurotoxicology 2008;29:124-9. https://doi.org/10.1016/j.neuro.2007.10.002
  135. Bastos Sales L, Kamstra JH, Cenijn PH, van Rijt LS, Hamers T, Legler J. Effects of endocrine disrupting chemicals on in vitro global DNA methylation and adipocyte differentiation. Toxicol In Vitro 2013;27:1634-43. https://doi.org/10.1016/j.tiv.2013.04.005
  136. Rusiecki JA, Baccarelli A, Bollati V, Tarantini L, Moore LE, Bonefeld-Jorgensen EC. Global DNA hypomethylation is associated with high serum-persistent organic pollutants in Greenlandic Inuit. Environ Health Perspect 2008;116:1547-52. https://doi.org/10.1289/ehp.11338

Cited by

  1. Risk Assessment of Cosmetics Using Triclosan on Future Generation’s Germ Cell Maturation via Lactating Mother Rats vol.17, pp.4, 2018, https://doi.org/10.3390/ijerph17041143
  2. Real‐world data reveal unmet clinical needs in insulin treatment in Asian people with type 2 diabetes: the Joint Asia Diabetes Evaluation (JADE) Register vol.22, pp.4, 2018, https://doi.org/10.1111/dom.13950
  3. Adipose Tissue Transcriptome Is Related to Pollutant Exposure in Polar Bear Mother-Cub Pairs from Svalbard, Norway vol.54, pp.18, 2018, https://doi.org/10.1021/acs.est.0c01920
  4. Machine Learning for Investigation on Endocrine-Disrupting Chemicals with Gestational Age and Delivery Time in a Longitudinal Cohort vol.2021, pp.None, 2018, https://doi.org/10.34133/2021/9873135
  5. Environmental contaminant body burdens and the relationship with blood pressure measures among Indigenous adolescents using Bayesian Kernel Machine Regression: Results from the Nituuchischaayihtitaau vol.4, pp.None, 2021, https://doi.org/10.1016/j.envadv.2021.100048