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Sex-specific associations of bisphenol A and its substitutes with body fat distribution among US adults: NHANES 2011–2016

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Abstract

Bisphenol A (BPA) and its structural analogs (bisphenol S (BPS) and bisphenol F (BPF)) are widely consumed endocrine disrupting chemicals that may contribute to the etiology of obesity. To date, few studies have directly investigated the sex-related associations between bisphenols and body fat distribution in adults. In this study, we included 2669 participants from the National Health and Nutrition Examination Survey (NHANES) 2011–2016 to evaluate and compare sex-specific differences of the associations of BPA, BPS, and BPF with body fat distribution. We found that there were significant positive correlations between BPS and body fat indices (STFAT [adjustedβ=1.94, 95% CI: (0.24, 3.64)], TAF [0.18 (0.04, 0.32)], SAT [0.15 (0.03, 0.27)], android fat mass [0.20 (0.004, 0.40)], BMI [1.63 (0.61, 2.65)], and WC [3.19 (0.64, 5.73)] in the highest quartiles of BPS), but not in BPA and BPF. Stratified analyses suggested that the significant associations of BPS with body fat indices were stronger in women than men (STFAT [adjustedβ=3.75, 95% CI: (1.04, 6.45) vs. adjustedβ=−0.06, 95% CI: (−2.23, 2.11), P for interaction < 0.001], TAF [ 0.32 (0.09, 0.54) vs. 0.01 (−0.17, 0.19), P for interaction < 0.001], SAT [0.27 (0.09, 0.45) vs. 0.01 (−0.14, 0.16), P for interaction < 0.001], android fat mass [0.41 (0.12, 0.71) vs. −0.02 (−0.28, 0.24), P for interaction < 0.001], gynoid fat mass [0.56 (0.11, 1.01) vs. −0.05 (−0.41, 0.31), P for interaction = 0.002], BMI [2.76 (1.08, 4.44) vs. 0.47 (−0.80, 1.74), P for interaction < 0.001], and WC [5.51 (1.44, 9.58) vs. 0.61 (−2.67, 3.88), P for interaction < 0.001]), and positive associations between BPS with fat distribution were also observed in non-smoking women. Our study indicated that in women, higher concentration of urinary BPS was associated with increased body fat accumulation, except for visceral adipose tissue mass. These findings emphasize the role of environmental BPS exposure in the increasing fat deposits, and confirm the need for more prospective cohort studies on a sex-specific manner.

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Data availability

Publicly available data sets were analyzed in this study. This data can be found here: https://www.cdc.gov/nchs/nhanes/index.htm.

References

  • Alharbi H, Algonaiman R, Alduwayghiri R, Aljutaily T, Algheshairy R, Almutairi A, Alharbi R, Alfurayh L, Alshahwan A, Alsadun A, Barakat H (2022) Exposure to bisphenol a substitutes, bisphenol s and bisphenol f, and its association with developing obesity and diabetes mellitus: a narrative review. Int J Environ Res Public Health 19:15918

  • Barr D, Wilder L, Caudill S, Gonzalez A, Needham L, Pirkle J (2005) Urinary creatinine concentrations in the U.S. population: implications for urinary biologic monitoring measurements. Environ Health Perspect 113:192–200

    Article  CAS  Google Scholar 

  • Bousoumah R, Leso V, Iavicoli I, Huuskonen P, Viegas S, Porras S, Santonen T, Frery N, Robert A, Ndaw S (2021) Biomonitoring of occupational exposure to bisphenol A, bisphenol S and bisphenol F: a systematic review. Sci Total Environ 783:146905

    Article  CAS  Google Scholar 

  • Bulka C, Mabila S, Lash J, Turyk M, Argos M (2017) Arsenic and obesity: a comparison of urine dilution adjustment methods. Environ Health Perspect 125:087020

    Article  Google Scholar 

  • Carwile J, Michels K (2011) Urinary bisphenol A and obesity: NHANES 2003-2006. Environ Res 111:825–830

    Article  CAS  Google Scholar 

  • Choi J, Lee J, Huh D, Moon K (2022) Urinary bisphenol concentrations and its association with metabolic disorders in the US and Korean populations. Environ Pollut 295:118679

    Article  CAS  Google Scholar 

  • Czernichow S, Kengne A, Stamatakis E, Hamer M, Batty G (2011) Body mass index, waist circumference and waist-hip ratio: which is the better discriminator of cardiovascular disease mortality risk?: evidence from an individual-participant meta-analysis of 82 864 participants from nine cohort studies. Obes Rev 12:680–687

    Article  CAS  Google Scholar 

  • Gajjar P, Liu Y, Li N, Buckley J, Chen A, Lanphear B, Kalkwarf H, Cecil K, Yolton K, Braun J (2022) Associations of mid-childhood bisphenol A and bisphenol S exposure with mid-childhood and adolescent obesity. Environ epidemiol 6:e187

    Article  Google Scholar 

  • Goossens G (2017) The metabolic phenotype in obesity: fat mass, body fat distribution, and adipose tissue function. Obes Facts 10:207–215

    Article  CAS  Google Scholar 

  • Gore A, Chappell V, Fenton S, Flaws J, Nadal A, Prins G, Toppari J, Zoeller R (2015) EDC-2: the endocrine society’s second scientific statement on endocrine-disrupting chemicals. Endocr Rev 36:E1–E150

    Article  CAS  Google Scholar 

  • Hahladakis J, Iacovidou E, Gerassimidou S (2023) An overview of the occurrence, fate, and human risks of the bisphenol-A present in plastic materials, components, and products. Integr Environ Assess Manag 19:45–62

    Article  CAS  Google Scholar 

  • Hocking S, Samocha-Bonet D, Milner K, Greenfield J, Chisholm D (2013) Adiposity and insulin resistance in humans: the role of the different tissue and cellular lipid depots. Endocr Rev 34:463–500

    Article  CAS  Google Scholar 

  • Hong S, Sung Y, Hong Y, Ha E, Jeong K, Chung H, Lee H (2017) Urinary bisphenol A is associated with insulin resistance and obesity in reproductive-aged women. Clin Endocrinol 86:506–512

    Article  CAS  Google Scholar 

  • Howdeshell K, Hotchkiss A, Thayer K, Vandenbergh J, vom Saal F (1999) Exposure to bisphenol A advances puberty. Nature 401:763–764

    Article  CAS  Google Scholar 

  • Ibrahim M (2010) Subcutaneous and visceral adipose tissue: structural and functional differences. Obes Rev 11:11–18

    Article  Google Scholar 

  • Jacobson M, Woodward M, Bao W, Liu B, Trasande L (2019) Urinary bisphenols and obesity prevalence among U.S. children and adolescents. J Endocr Soc 3:1715–1726

    Article  CAS  Google Scholar 

  • Lee I, Park Y, Kim M, Kim S, Choi S, Park J, Cho Y, Hong S, Yoo J, Park H, Cheon G, Choi K, Moon M (2021) Associations of urinary concentrations of phthalate metabolites, bisphenol A, and parabens with obesity and diabetes mellitus in a Korean adult population: Korean National Environmental Health Survey (KoNEHS) 2015-2017. Environ Int 146:106227

    Article  CAS  Google Scholar 

  • Lee M, Wu Y, Fried S (2013) Adipose tissue heterogeneity: implication of depot differences in adipose tissue for obesity complications. Mol Asp Med 34:1–11

    Article  CAS  Google Scholar 

  • Liu B, Lehmler H, Sun Y, Xu G, Liu Y, Zong G, Sun Q, Hu F, Wallace R, Bao W (2017) Bisphenol A substitutes and obesity in US adults: analysis of a population-based, cross-sectional study. Lancet Planet Health 1:e114–e122

    Article  Google Scholar 

  • Liu B, Lehmler H, Sun Y, Xu G, Sun Q, Snetselaar L, Wallace R, Bao W (2019) Association of bisphenol A and its substitutes, bisphenol F and bisphenol S, with obesity in United States children and adolescents. Diabetes Metab J 43:59–75

    Article  Google Scholar 

  • Ma Q, Deng P, Lin M, Yang L, Li L, Guo L, Zhang L, He M, Lu Y, Pi H, Zhang Y, Yu Z, Chen C, Zhou Z (2021) Long-term bisphenol A exposure exacerbates diet-induced prediabetes via TLR4-dependent hypothalamic inflammation. J Hazard Mater 402:123926

    Article  CAS  Google Scholar 

  • Mage D, Allen R, Kodali A (2008) Creatinine corrections for estimating children’s and adult’s pesticide intake doses in equilibrium with urinary pesticide and creatinine concentrations. J Expo Sci Environ Epidemiol 18:360–368

    Article  CAS  Google Scholar 

  • Martínez M, Blanco J, Rovira J, Kumar V, Domingo J, Schuhmacher M (2020) Bisphenol A analogues (BPS and BPF) present a greater obesogenic capacity in 3T3-L1 cell line. Food chem toxicol : int j publ British Ind Biologic Res Assoc 140:111298

    Article  Google Scholar 

  • Masuno H, Kidani T, Sekiya K, Sakayama K, Shiosaka T, Yamamoto H, Honda K (2002) Bisphenol A in combination with insulin can accelerate the conversion of 3T3-L1 fibroblasts to adipocytes. J Lipid Res 43:676–684

    Article  CAS  Google Scholar 

  • Matsushita Y, Nakagawa T, Yamamoto S, Takahashi Y, Yokoyama T, Noda M, Mizoue T (2010) Associations of visceral and subcutaneous fat areas with the prevalence of metabolic risk factor clustering in 6,292 Japanese individuals: the Hitachi Health Study. Diabetes Care 33:2117–2119

    Article  Google Scholar 

  • Mauvais-Jarvis F (2011) Estrogen and androgen receptors: regulators of fuel homeostasis and emerging targets for diabetes and obesity. Trends Endocrinol Metab 22:24–33

    Article  CAS  Google Scholar 

  • Meng Z, Wang D, Liu W, Li R, Yan S, Jia M, Zhang L, Zhou Z, Zhu W (2019) Perinatal exposure to Bisphenol S (BPS) promotes obesity development by interfering with lipid and glucose metabolism in male mouse offspring. Environ Res 173:189–198

    Article  CAS  Google Scholar 

  • Palmer B, Clegg D (2015) The sexual dimorphism of obesity. Mol Cell Endocrinol 402:113–119

    Article  CAS  Google Scholar 

  • Pan X, Wang L, Pan A (2021) Epidemiology and determinants of obesity in China. Lancet Diabetes Endocrinol 9:373–392

    Article  Google Scholar 

  • Pedersen S, Kristensen K, Hermann P, Katzenellenbogen J, Richelsen B (2004) Estrogen controls lipolysis by up-regulating alpha2A-adrenergic receptors directly in human adipose tissue through the estrogen receptor alpha. Implications for the female fat distribution. J Clin Endocrinol Metab 89:1869–1878

    Article  CAS  Google Scholar 

  • Ratajczak-Wrona W, Garley M, Rusak M, Nowak K, Czerniecki J, Wolosewicz K, Dabrowska M, Wolczynski S, Radziwon P, Jablonska E (2021) Sex-dependent dysregulation of human neutrophil responses by bisphenol A. Environ Health 20:5

    Article  CAS  Google Scholar 

  • Reina-Pérez I, Olivas-Martínez A, Mustieles V, Ruiz-Ojeda F, Molina-Molina J, Olea N, Fernández M (2021) Bisphenol F and bisphenol S promote lipid accumulation and adipogenesis in human adipose-derived stem cells. Food chem toxicol : int j publ British Ind Biologic Res Assoc 152:112216

    Article  Google Scholar 

  • Rönn M, Lind L, Örberg J, Kullberg J, Söderberg S, Larsson A, Johansson L, Ahlström H, Lind P (2014) Bisphenol A is related to circulating levels of adiponectin, leptin and ghrelin, but not to fat mass or fat distribution in humans. Chemosphere 112:42–48

    Article  Google Scholar 

  • Sari C, Eikelis N, Head G, Schlaich M, Meikle P, Lambert G, Lambert E (2019) Android fat deposition and its association with cardiovascular risk factors in overweight young males. Front Physiol 10:1162

    Article  Google Scholar 

  • Trasande L, Attina T, Blustein J (2012) Association between urinary bisphenol A concentration and obesity prevalence in children and adolescents. JAMA 308:1113–1121

    Article  CAS  Google Scholar 

  • Wang B, Li M, Zhao Z, Lu J, Chen Y, Xu Y, Xu M, Wang W, Wang T, Bi Y, Ning G (2019) Urinary bisphenol A concentration and glucose homeostasis in non-diabetic adults: a repeated-measures, longitudinal study. Diabetologia 62:1591–1600

    Article  CAS  Google Scholar 

  • Wang T, Li M, Chen B, Xu M, Xu Y, Huang Y, Lu J, Chen Y, Wang W, Li X, Liu Y, Bi Y, Lai S, Ning G (2012) Urinary bisphenol A (BPA) concentration associates with obesity and insulin resistance. J Clin Endocrinol Metab 97:E223–E227

    Article  CAS  Google Scholar 

  • Wang W, Zhang X, Wang Z, Qin J, Wang W, Tian H, Ru S (2018) Bisphenol S induces obesogenic effects through deregulating lipid metabolism in zebrafish (Danio rerio) larvae. Chemosphere 199:286–296

    Article  CAS  Google Scholar 

  • Wang Y, Zhu L, James-Todd T, Sun Q (2022) Urinary polycyclic aromatic hydrocarbon excretion and regional body fat distribution: evidence from the U.S. National Health and Nutrition Examination Survey 2001-2016. Environ Health 21:75

    Article  CAS  Google Scholar 

  • World Health Organization. Office of Occupational H (1996) Biological monitoring of chemical exposure in the workplace : guidelines. World Health Organization, Geneva https://apps.who.int/iris/handle/10665/41856

    Google Scholar 

  • Zeng J, Li J, Liu S, Yang Z, Zhong Y, Chen X, Li G, Li J (2021) Lipidome disturbances in preadipocyte differentiation associated with bisphenol A and replacement bisphenol S exposure. Sci Total Environ 753:141949

    Article  CAS  Google Scholar 

  • Zhou X, Ye X, Calafat A (2012) Automated on-line column-switching HPLC-MS/MS method for the quantification of triclocarban and its oxidative metabolites in human urine and serum. J Chromatogr B Analyt Technol Biomed Life Sci 881:27–33

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Acknowledgements

A special thanks to all of the NHANES participants who freely gave their time to make this and other studies possible. The authors are grateful to Di Wu, MD (Duke-NUS Medical School, Singapore), who provided comments and professional help with linguistic editing of this article.

Funding

This work was supported by the GDPH Supporting Fund for Talent Program (No. KJ012020629).

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Author notes

  1. Shili Zhang and Lingyan Dai contributed equally to the research.

Authors and Affiliations

  1. Department of Endocrinology, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, 510080, China

    Shili Zhang, Ziyu Wan & Haixia Guan

  2. Global Health Research Center, Guangdong Provincial People’s Hospital, Guangdong Academy of Medical Sciences, Southern Medical University, Guangzhou, 510080, China

    Lingyan Dai

  3. Department of Epidemiology, Guangdong Provincial Key Laboratory of Tropical Disease Research, School of Public Health, Southern Medical University, Guangzhou, 510515, China

    Zhiwei Huang

  4. Department of Endocrinology and Metabolism, Nanfang Hospital, Southern Medical University, Guangzhou, 510515, China

    Mengchen Zou

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Contributions

Haixia Guan designed this study and carried out the overall planning. Shili Zhang and Lingyan Dai collected the data, analyzed the data, and drafted the manuscript. Haixia Guan and Mengchen Zou revised the manuscript. Ziyu Wan and Zhiwei Huang contributed to the collection of data. Shili Zhang and Lingyan Dai had the same contribution to this research. All authors read and approved the final manuscript.

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Correspondence to Haixia Guan.

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The National Center for Health Statistics (NCHS) Research Ethics Review Board approved the NHANES, in which written informed consent had been obtained from the survey respondents.

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Zhang, S., Dai, L., Wan, Z. et al. Sex-specific associations of bisphenol A and its substitutes with body fat distribution among US adults: NHANES 2011–2016. Environ Sci Pollut Res 31, 7948–7958 (2024). https://doi.org/10.1007/s11356-023-31589-z

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