INTRODUCTION

Childhood obesity is a serious health problem worldwide. The prevalence of obesity among United States children and adolescents was 17% in 2011 to 2014 [1]. This is alarming because obesity has deleterious effects on almost every system in the body and childhood obesity tracks strongly into adulthood [2]. Moreover, obesity is an important risk factor for many diseases, such as diabetes, cardiovascular disease, cancers, and obstructive sleep apnea, in adults [3]. Therefore, it is urgent to identify modifiable risk factors for the prevention of obesity, which is important in reducing the risk of chronic disease risk factors later in life.

Recently, accumulating evidence suggests that environmental endocrine disrupting chemicals, including bisphenol A (BPA), may play an important role in the epidemic of obesity [24]. BPA is a synthetic chemical used in canned goods, plastic containers for food and beverage, dental sealants, and thermal paper [5]. The wide use of BPA results in an almost ubiquitous exposure in human populations [4]. Recent studies reported the association of BPA with obesity, diabetes, and cardiovascular disease [6]. In addition, BPA has adverse effects on thyroid function, and neurodevelopment [6]. Since 2010, Europe and Canada have prohibited the use of BPA in plastic food containers, especially in baby products because of the concern for its deleterious health effects [78]. The U.S. Food and Drug Administration also documented that baby bottles and sippy cups could no longer contain BPA in 2012 [9]. Subsequently, BPA-free products began to flood the market, with bisphenol F (BPF) and bisphenol S (BPS) used as a substitute for BPA [10]. Currently BPF and BPS are widely used in the manufacture of plastics, epoxy resins, coatings for various applications, such as liners, adhesives, and food packaging, thermal paper, baby bottles, and personal care products including makeup, toothpaste, and body wash [1011]. However, the health effects of BPF and BPS are unclear. BPF and BPS have similar chemical structures to BPA and have been suggested to be endocrine disrupting chemicals as observed in in vitro and in vivo studies [10]. Experimental studies found that both BPF and BPS are involved in the processes of preadipocytes differentiation and lipid accumulation [1213]. However, studies on health effects of BPF and BPS exposures in children and adolescents are lacking.

In this study, we aimed to examine the associations of BPA, BPF, and BPS exposure with obesity in children and adolescents using data from the U.S. National Health and Nutrition Examination Survey (NHANES), a nationwide, population-based, cross-sectional study.

METHODS

Study population

NHANES is a nationally representative survey of the non-institutionalized United States population, administered by the National Center for Health Statistics at the Centers for Disease Control and Prevention (CDC). NHANES collects data on demographics, socioeconomic status, diet, lifestyle, and medical conditions in addition to specimens for laboratory tests. NHANES data are publicly released in 2-year cycles. A detailed description of NHANES are available elsewhere [14]. NHANES has been approved (Protocol #2011-17) by the National Center for Health Statistics Ethics Review Board. Written informed consent was obtained from all participants.

For this analysis, we used data from NHANES 2013 to 2014, because this was the first and only cycle where urinary levels of BPF and BPS were measured. The study population consisted of children and adolescent aged 6 to 17 years, because bisphenols were measured only in children 6 years and older. We finally identified 745 children and adolescent (mean age 11.1±3.4; 49.8% boys) who had available data on body mass index (BMI) and urinary concentrations of BPA, BPF, and BPS. Fifteen participants did not have data on waist or height; therefore, analyses for abdominal obesity were conducted in 730 children and adolescents (49.8% boys).

Exposure assessment

Urinary concentrations of BPA, BPF, and BPS were measured using on-line solid phase extraction coupled to high performance liquid chromatography and tandem mass spectrometry, at the Division of Laboratory Sciences, National Center for Environmental Health, CDC. The lower limits of detection (LLOD) reported by NHANES were 0.2 ng/mL for BPA, 0.2 ng/mL for BPF, and 0.1 ng/mL for BPS. For those concentrations below the LLOD (1.74% for BPA, 38.79% for BPF, and 10.87% for BPS), NHANES staff assigned a value of the LLOD divided by the square root of 2. To account for urine dilution, levels of all three target analytes were adjusted for urinary creatinine levels in all the analysis models in this study, as NHANES recommended [15].

Outcome ascertainment

Trained health technicians assessed weight, waist, and height according to the NHANES Anthropometry Procedures Manual [14]. BMI was calculated as weight in kilograms divided by the square of height in meters. Obesity was defined as a BMI at or above the sex-specific 95th percentile based on the 2000 CDC sex-specific BMI-for-age growth charts for the United States [16]. Abdominal obesity was defined as waist-to-height ratio ≥0.5 [17].

Covariates

Information on age, sex, race/ethnicity, and family income was collected using questionnaires. Proxy respondents provided this information for children who were under 16 years. Race/ethnicity was categorized into Hispanic, non-Hispanic white, non-Hispanic black, and other. Family income-to-poverty ratio was categorized as ≤1.30, 1.31 to 3.50, and >3.50 [14]. Children aged 12 years or older and proxy respondents for children younger than 11 years answered the question about TV watching. We used daily hours of TV watching to assess sedentary behavioral risk (with a cut point of ≥2 hours/day) [18].

Dietary information was collected by 24-hour dietary recall interview. Interviews of children aged 6 to 8 years were conducted with a proxy and the child present to assist in reporting intake information. Interviews of children aged 9 to 11 years were conducted with the child and the assistance of a proxy familiar with the child's intake. Participants 12 years or older answered for themselves. Total energy intake was calculated using the United States Department of Agriculture Automated Multiple-Pass Method. The 2010 Healthy Eating Index (HEI-2010) score was calculated to represent diet quality, with a higher score indicating a better diet [19].

Statistical analysis

NHANES used a complex, multistage probability sampling design to represent the civilian non-institutionalized United States population. Weighted estimates were applied to account for the differential probability of selection, non-response adjustment, and adjustment to independent population controls. The Taylor series linearization method was used for variance estimation to account for stratification and clustering, following the NHANES Analytic Guidelines [14].

We used chi-square tests and analysis of variance to compare categorical variables and continuous variables, respectively. We log-transformed BPA, BPF, and BPS concentrations before the analyses because they were in skewed distribution. Pearson correlations with sample weights were used to compute correlation coefficients among log-transformed BPA, BPF, and BPS levels. Logistic regression models were used to estimate the odds ratio (OR) of general or abdominal obesity according to quartiles of urinary BPA, BPF, and BPS concentrations. We adjusted for age, sex, and urinary creatinine levels in Model 1. Race/ethnicity, family income-to-poverty ratios, TV watching, total energy intake, and HEI-2010 score were added in Model 2. We considered Model 2 as the main model of this study. BPA, BPF, and BPS levels were mutually adjusted in Model 3. Categorical covariates included a category for missing data if necessary. To test linear trends across categories of BPA, BPF, or BPS concentrations, we assigned the median values for each category and fitted the log-transformed median values as continuous variable in models.

We evaluated effect modification by sex (boy, girl) and race/ethnicity (white, non-white) by conducting stratified analyses. P values for heterogeneity were derived from the multiplicative interaction term coefficient (exposure variable×effect modifier variable) added to the main effects multivariable model.

All statistical analyses were performed with survey modules of SAS software version 9.4 (SAS Institute, Cary, NC, USA). P<0.05 was considered statistically significant.

RESULTS

In this study, the weighted prevalence of general obesity was 21.0% (95% confidence interval [CI], 15.5% to 26.4%), and 35% (95% CI, 28.2% to 41.9%) for abdominal obesity. The median urinary concentration was 1.2 ng/mL (interquartile range [IQR], 0.6 to 2.4 ng/mL) for BPA, 0.3 ng/mL (IQR, 0.1 to 0.9 ng/mL) for BPF, and 0.3 ng/mL (IQR, 0.1 to 0.7 ng/mL) for BPS. Individuals with higher levels of BPA and BPS were more likely to be non-Hispanic blacks (Supplementary Tables 1 and 2). Individuals with higher levels of BPF were more likely to be non-Hispanic whites (Supplementary Table 3). Urinary concentrations of BPA, BPF, and BPS according to population characteristics are present in Supplementary Table 4. The three bisphenols were moderately correlated with each other; the correlation coefficients were 0.25 between BPA and BPF (P<0.001), 0.33 between BPA and BPS (P<0.001), and 0.13 between BPF and BPS (P<0.001).

We observed a significant association of urinary concentrations of BPF, but not BPA or BPS, with general obesity (Table 1). After adjustment for demographic, socioeconomic and lifestyle factors, total energy intake, overall diet quality as indicated by the HEI-2010 score, and urinary creatinine levels, the OR of general obesity comparing the highest with lowest quartile was 1.74 (95% CI, 0.92 to 3.31) for BPA (P for trend=0.08), 1.54 (95% CI, 1.02 to 2.32) for BPF (P for trend=0.05), and 1.36 (95% CI, 0.53 to 3.51) for BPS (P for trend=0.62). The ORs of general obesity per unit increase in BPA, BPF, and BPS levels were 1.29 (95% CI, 0.97 to 1.72), 1.17 (95% CI, 1.00 to 1.37), 1.08 (95% CI, 0.79 to 1.49), respectively (Fig. 1). When we simultaneously included all bisphenols in the same multivariable model for mutual adjustment, the adjusted OR of general obesity comparing the highest with lowest quartile of each bisphenol was 1.65 (95% CI, 0.86 to 3.16) for BPA (P for trend=0.14), 1.48 (95% CI, 0.93 to 2.35) for BPF (P for trend=0.13), and 1.24 (95% CI, 0.48 to 3.21) for BPS (P for trend=0.73).

For abdominal obesity, the multivariable-adjusted OR of abdominal obesity comparing the highest with lowest quartile of urinary bisphenol levels was 1.47 (95% CI, 0.88 to 2.46; P for trend=0.08) for BPA, 1.48 (95% CI, 0.92 to 2.38; P for trend=0.15) for BPF, and 1.13 (95% CI, 0.55 to 2.32; P for trend=0.71) for BPS (Table 2).

In stratified analyses, the associations of obesity with BPA and BPF levels were much stronger in boys than in girls (Table 3). The multivariable-adjusted OR of general obesity comparing the highest with the lowest quartile of urinary BPA level was 2.78 (95% CI, 1.07 to 7.27) in boys (P for trend=0.02) and 1.10 (95% CI, 0.42 to 2.91) in girls (P for trend=0.92, P for interaction=0.02) (Table 3). For BPF, the corresponding OR was 3.35 (95% CI, 2.02 – 5.53) in boys (P for trend <0.001) and 0.55 (95% CI, 0.25 to 1.25) in girls (P for trend=0.13, P for interaction <0.001) (Table 3). The multivariable-adjusted OR of abdominal obesity comparing the highest with the lowest quartile of urinary BPA level was 2.87 (95% CI, 1.60 to 5.16) in boys (P for trend <0.001) and 0.83 (95% CI, 0.45 to 1.53) in girls (P for trend=0.64, P for interaction=0.003) (Table 3). For BPF, the corresponding OR was 2.11 (95% CI, 1.23 to 3.62) in boys (P for trend=0.01) and 0.99 (95% CI, 0.50 to 1.95) in girls (P for trend=0.79, P for interaction=0.04) (Table 3). No significant interaction effects by sex were found for BPS (P for interaction=0.36 for general obesity; P for interaction=0.62 for abdominal obesity) (Table 3). There was no significant effect modification by age (Supplementary Tables 5 and 6). The ORs of general obesity per unit increase in concentrations of BPA, BPF, and BPS levels in boys and girls were shown in Fig. 1.

We did not observe significant effect modification by race/ethnicity for the relation between bisphenol exposure and general obesity (Supplementary Table 7). However, the associations of abdominal obesity with BPF levels were much stronger in non-Whites than in Whites (Supplementary Table 8). The multivariable-adjusted OR of abdominal obesity comparing the highest with the lowest quartile of urinary BPS level was 1.88 (95% CI, 1.07 to 3.30) in non-Whites (P for trend=0.01) and 0.45 (95% CI, 0.11 to 1.91) in Whites (P for trend=0.36, P for interaction=0.01).

DISCUSSION

In this study, we found positive associations of urinary concentrations of BPF with general and abdominal obesity in United States children and adolescents, especially in boys. In addition, significant associations of urinary BPA levels with general and abdominal obesity were found in boys. However, we did not observe significant associations between BPS exposure at current levels and either general obesity or abdominal obesity.

To our knowledge, this is the first study to evaluate the link between BPF and BPS with obesity in children and adolescents. Our previous study suggested that at current population exposure levels, BPA, but not BPF or BPS, was significantly associated with an increased odds of obesity in United States adults [20]. This may be due to lower dose and shorter duration of BPF and BPS exposure in adults, compared with BPA exposure, because BPF and BPS have only been used in recent years as BPA substitutes. Since children and adolescents are rapidly growing, they may be more susceptible to environmental chemicals than adults [21] and we hypothesized that this would amplify the adverse effects of exposure to BPA and BPA substitutes. In addition, many children may have been exposed to BPA, BPF, and BPS since birth, resulting in similar duration of exposure to BPF and BPS, as compared to BPA [9]. In the present study, we also observed positive associations of BPA, BPF, and BPS with BMI and waist-to-height ratio in children and adolescents, although the associations were generally not statistically significant (data not shown).

Laboratory studies provide strong evidence to support our findings that BPF has obesity-promoting effects similar to BPA [10]. BPF was found to be involved in multiple molecular pathways to obesity. First, BPF has similar estrogenic activities to BPA, such as altering adiponectin production or binding to nuclear estrogen receptors [102223]. BPF was also found to interfere with hormonal regulation by deregulating messenger RNA/long non-coding RNA and micro RNA in a human primary adipocyte model [24]. Moreover, BPF exhibited adverse effects on the hypothalamic-pituitary-gonadal axis, which is crucial for energy storage and consumption [2526]. Second, BPF could promote differentiation of preadipocytes and increase lipid accumulation by affecting the peroxisome proliferator-activated receptor gamma signaling pathway [1227]. Third, BPF was observed to affect adiponectin production and secretion [28].

We observed a positive (although non-significant) association between urinary BPA concentrations and higher odds of general and abdominal obesity in children and adolescents. Similar results were reported in previous studies [18293031]. The non-significant association, in the present study, might because the lower BPA exposure levels compared to previous NHANES reports [18]. Such a declining trend in BPA levels in the United States population is likely related to the policy banning the use of BPA in certain products [932]. The relatively small sample size might be another contributing factor for the non-significant finding in this study. Similarly, there was a positive, but not statistically significant, association between BPS exposure and obesity in this study. Previous in vivo studies and in vitro studies suggested that BPS has similar obesogenic activities to BPA and BPF [1013]. It is possible that the null findings for BPS are due to the relatively low exposure levels and small sample size in this study.

Interestingly, we observed associations of general and abdominal obesity with urinary levels of both BPA and BPF in boys but not in girls. This is consistent with some [1830], although not all [2933], previous studies on BPA exposure and obesity. We hypothesized that sex differences may result from differences in diets of boys and girls, with some diets having more bisphenol-containing packaging than others do. However when we tested this hypothesis, we did not find significant differences of urinary levels of BPA and BPF between boys and girls. It is biologically plausible that sex differences in hormone profiles may lead to different susceptibilities to adverse health outcomes with BPA and BPF exposure [103334]. BPA is a selective estrogen receptor modulator, which means it acts differently in different tissues [35]. A previous study suggested that BPA might act as an estrogenic agonist in males who have low endogenous estrogen levels, and conversely act as an antagonist in females who have higher endogenous estrogen levels [36]. Sex differences in estrogenic activity were also observed for BPF in an animal study [25]. Further investigation is warranted to clarify the health effects of BPA and BPF for each sex.

The current study could be important, being the first report in humans on the association of BPA substitutes, BPF and BPS, with general and abdominal obesity in children and adolescents. More epidemiological and toxicological studies are needed to assess whether and how human exposures to BPA substitutes increase the risk of obesity in children and adolescents. In addition, the positive association between BPA exposure and obesity in children suggested that BPA, even at the current relatively low level, remains to be a concern of health. Continuous monitoring the exposures of BPA and BPA substitutes and measures to reduce human exposure, such as decreasing the use of plastic products, are needed.

A major strength of our study is the use of nationally representative data from NHANES that allowed us to generalize our findings to a broader population. The abundant data from NHANES, including comprehensive information about demographic, socioeconomic, body measure, and lifestyle factors, provided the opportunity to adjust for a variety of risk factors for obesity. However, there were several limitations. First, due to the cross-sectional nature of NHANES, we could not rule out the possibility of reverse causation. Second, NHANES used spot urine samples to measure bisphenol concentrations, because of the challenges to collect 24-hour urine samples in such a large survey study. Although within-person and between person variability exists, previous studies have demonstrated that urinary concentrations of BPA derived from one spot sample may adequately reflect the average exposure of a population to BPA when specimens are collected from a sufficiently large population, with random meal ingestion and bladder emptying times [323738]. Another study detecting the temporal variability of BPA found that one measurement of BPA has moderate sensitivity for predicting multiply measured BPA levels [39]. Moreover, similar assumptions have been made in previous cross-sectional studies [18], which have been confirmed by longitudinal studies [40]. Third, the possibility of residual confounding and unmeasured confounding cannot be ruled out, although we have adjusted for a number of established risk factors for childhood obesity.

In a nationally representative population, BPF exposure was significantly and positively associated with general obesity in United States children and adolescents, especially in boys. BPA exposure was significantly associated with general and abdominal obesity in boys, but not in girls. There was no significant association of BPS at current exposure levels with obesity. Considering the increasing use of BPF and BPS as BPA substitutes, more research is needed to replicate our findings and further investigate their health effects in humans.

Acknowledgements

ACKNOWLEDGMENTS

This research was funded by the National Institute for Environmental Health Sciences through the University of Iowa Environmental Health Sciences Research Center (NIEHS/NIH P30 ES005605).

NOTES

CONFLICTS OF INTEREST: No potential conflict of interest relevant to this article was reported.

The abstract of this study was accepted for presentation at the 2018 Society for Epidemiologic Research Meeting, June 19–22, 2018, Baltimore, MD, USA.

Supplementary Materials

REFERENCES

• 1. Ogden CL, Carroll MD, Lawman HG, Fryar CD, Kruszon-Moran D, Kit BK, Flegal KM. Trends in obesity prevalence among children and adolescents in the United States, 1988-1994 through 2013-2014. JAMA 2016;315:2292-2299. ArticlePubMedPMC
• 2. Kumar S, Kelly AS. Review of childhood obesity: from epidemiology, etiology, and comorbidities to clinical assessment and treatment. Mayo Clin Proc 2017;92:251-265. PubMed
• 3. Kelsey MM, Zaepfel A, Bjornstad P, Nadeau KJ. Age-related consequences of childhood obesity. Gerontology 2014;60:222-228. ArticlePubMedPDF
• 4. Legeay S, Faure S. Is bisphenol A an environmental obesogen? Fundam Clin Pharmacol 2017;31:594-609. ArticlePubMedPDF
• 5. Mikołajewska K, Stragierowicz J, Gromadzinska J. Bisphenol A: application, sources of exposure and potential risks in infants, children and pregnant women. Int J Occup Med Environ Health 2015;28:209-241. PubMed
• 6. Gore AC, Chappell VA, Fenton SE, Flaws JA, Nadal A, Prins GS, Toppari J, Zoeller RT. EDC-2: The Endocrine Society's second scientific statement on endocrine-disrupting chemicals. Endocr Rev 2015;36:E1-E150. ArticlePubMedPMC
• 7. Government of Canada. ARCHIVED Health risk assessment of bisphenol a from food packaging applications updated 2008 Aug 13. Available from: https://www.canada.ca/en/health-canada/services/food-nutrition/food-safety/packaging-materials/bisphenol/health-risk-assessment-bisphenol-food-packaging-applications.html.
• 8. European Food Safety Authority. EFSA explains the safety of bisphenol A updated 2015 Jan 21. Available from: https://www.efsa.europa.eu/en/corporate/pub/factsheetbpa150121.
• 9. U.S. Food and Drug Administration. Draft assessment of bisphenol A for use in food contact applications. Bethesda: U.S. Food and Drug Administration; 2008.
• 10. 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;123:643-650. ArticlePubMedPMC
• 11. Wu LH, Zhang XM, Wang F, Gao CJ, Chen D, Palumbo JR, Guo Y, Zeng EY. Occurrence of bisphenol S in the environment and implications for human exposure: a short review. Sci Total Environ 2018;615:87-98. ArticlePubMed
• 12. Zhang J, Zhang T, Guan T, Ruan P, Ren D, Dai W, Yu H, Li T. Spectroscopic and molecular modeling approaches to investigate the interaction of bisphenol A, bisphenol F and their diglycidyl ethers with PPARα. Chemosphere 2017;180:253-258. ArticlePubMed
• 13. Ahmed S, Atlas E. Bisphenol S- and bisphenol A-induced adipogenesis of murine preadipocytes occurs through direct peroxisome proliferator-activated receptor gamma activation. Int J Obes (Lond) 2016;40:1566-1573. ArticlePubMedPDF
• 14. National Center for Health Statistics. Centers for Disease Control and Prevention. National Health and Nutrition Examination Survey updated 2017 Sep 15. Available from: http://www.cdc.gov/nchs/nhanes/about_nhanes.htm.
• 15. Barr DB, Wilder LC, Caudill SP, Gonzalez AJ, Needham LL, Pirkle JL. Urinary creatinine concentrations in the U.S. population: implications for urinary biologic monitoring measurements. Environ Health Perspect 2005;113:192-200. ArticlePubMed
• 16. Ogden CL, Flegal KM. Changes in terminology for childhood overweight and obesity. Natl Health Stat Report 2010;25:1-5.
• 17. Ashwell M, Gibson S. Waist-to-height ratio as an indicator of ‘early health risk’: simpler and more predictive than using a ‘matrix’ based on BMI and waist circumference. BMJ Open 2016;6:e010159.ArticlePubMedPMC
• 18. Trasande L, Attina TM, Blustein J. Association between urinary bisphenol A concentration and obesity prevalence in children and adolescents. JAMA 2012;308:1113-1121. ArticlePubMed
• 19. Guenther PM, Kirkpatrick SI, Reedy J, Krebs-Smith SM, Buckman DW, Dodd KW, Casavale KO, Carroll RJ. The Healthy Eating Index-2010 is a valid and reliable measure of diet quality according to the 2010 dietary guidelines for Americans. J Nutr 2014;144:399-407. ArticlePubMedPMC
• 20. Liu B, Lehmler HJ, Sun Y, Xu G, Liu Y, Zong G, Sun Q, Hu FB, Wallace RB, Bao W. Bisphenol A substitutes and obesity in US adults: analysis of a population-based, cross-sectional study. Lancet Planet Health 2017;1:e114-e122. ArticlePubMedPMC
• 21. Bearer CF. How are children different from adults? Environ Health Perspect 1995;103(Suppl 6):7-12.Article
• 22. Moreman J, Lee O, Trznadel M, David A, Kudoh T, Tyler CR. Acute toxicity, teratogenic, and estrogenic effects of bisphenol a and its alternative replacements bisphenol S, bisphenol F, and bisphenol AF in zebrafish embryo-larvae. Environ Sci Technol 2017;51:12796-12805. ArticlePubMed
• 23. Le Fol V, Ait-Aissa S, Sonavane M, Porcher JM, Balaguer P, Cravedi JP, Zalko D, Brion F. In vitro and in vivo estrogenic activity of BPA, BPF and BPS in zebrafish-specific assays. Ecotoxicol Environ Saf 2017;142:150-156. ArticlePubMed
• 24. Verbanck M, Canouil M, Leloire A, Dhennin V, Coumoul X, Yengo L, Froguel P, Poulain-Godefroy O. Low-dose exposure to bisphenols A, F and S of human primary adipocyte impacts coding and non-coding RNA profiles. PLoS One 2017;12:e0179583. ArticlePubMedPMC
• 25. Yang Q, Yang X, Liu J, Ren W, Chen Y, Shen S. Effects of BPF on steroid hormone homeostasis and gene expression in the hypothalamic-pituitary-gonadal axis of zebrafish. Environ Sci Pollut Res Int 2017;24:21311-21322. ArticlePubMedPDF
• 26. Schneider JE. Energy balance and reproduction. Physiol Behav 2004;81:289-317. ArticlePubMed
• 27. Zheng S, Shi JC, Hu JY, Hu WX, Zhang J, Shao B. Chlorination of bisphenol F and the estrogenic and peroxisome proliferator-activated receptor gamma effects of its disinfection byproducts. Water Res 2016;107:1-10. ArticlePubMed
• 28. Kidani T, Kamei S, Miyawaki J, Aizawa J, Sakayama K, Masuno H. Bisphenol A downregulates Akt signaling and inhibits adiponectin production and secretion in 3T3-L1 adipocytes. J Atheroscler Thromb 2010;17:834-843. ArticlePubMed
• 29. Li DK, Miao M, Zhou Z, Wu C, Shi H, Liu X, Wang S, Yuan W. Urine bisphenol-A level in relation to obesity and overweight in school-age children. PLoS One 2013;8:e65399. ArticlePubMedPMC
• 30. Bhandari R, Xiao J, Shankar A. Urinary bisphenol A and obesity in U.S. children. Am J Epidemiol 2013;177:1263-1270. ArticlePubMedPMC
• 31. Wells EM, Jackson LW, Koontz MB. Association between bisphenol A and waist-to-height ratio among children: National Health and Nutrition Examination Survey, 2003-2010. Ann Epidemiol 2014;24:165-167. ArticlePubMed
• 32. LaKind JS, Naiman DQ. Temporal trends in bisphenol A exposure in the United States from 2003-2012 and factors associated with BPA exposure: spot samples and urine dilution complicate data interpretation. Environ Res 2015;142:84-95. ArticlePubMed
• 33. 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;11:79ArticlePubMedPMCPDF
• 34. Mauvais-Jarvis F. Estrogen and androgen receptors: regulators of fuel homeostasis and emerging targets for diabetes and obesity. Trends Endocrinol Metab 2011;22:24-33. ArticlePubMed
• 35. Vandenberg LN, Colborn T, Hayes TB, Heindel JJ, Jacobs DR Jr, Lee DH, Shioda T, Soto AM, vom Saal FS, Welshons WV, Zoeller RT, Myers JP. Hormones and endocrine-disrupting chemicals: low-dose effects and nonmonotonic dose responses. Endocr Rev 2012;33:378-455. ArticlePubMedPMCPDF
• 36. Xu X, Tan L, Himi T, Sadamatsu M, Tsutsumi S, Akaike M, Kato N. Changed preference for sweet taste in adulthood induced by perinatal exposure to bisphenol A: a probable link to overweight and obesity. Neurotoxicol Teratol 2011;33:458-463. ArticlePubMed
• 37. Dekant W, Volkel W. Human exposure to bisphenol A by biomonitoring: methods, results and assessment of environmental exposures. Toxicol Appl Pharmacol 2008;228:114-134. ArticlePubMed
• 38. Nepomnaschy PA, Baird DD, Weinberg CR, Hoppin JA, Longnecker MP, Wilcox AJ. Within-person variability in urinary bisphenol A concentrations: measurements from specimens after long-term frozen storage. Environ Res 2009;109:734-737. ArticlePubMedPMC
• 39. Mahalingaiah S, Meeker JD, Pearson KR, Calafat AM, Ye X, Petrozza J, Hauser R. Temporal variability and predictors of urinary bisphenol A concentrations in men and women. Environ Health Perspect 2008;116:173-178. ArticlePubMed
• 40. Vafeiadi M, Roumeliotaki T, Myridakis A, Chalkiadaki G, Fthenou E, Dermitzaki E, Karachaliou M, Sarri K, Vassilaki M, Stephanou EG, Kogevinas M, Chatzi L. Association of early life exposure to bisphenol A with obesity and cardiometabolic traits in childhood. Environ Res 2016;146:379-387. ArticlePubMed

Fig. 1

Odds ratio of general obesity per unit increase in concentrations of bisphenol A (BPA), bisphenol F (BPF), and bisphenol S (BPS). Adjusted for age (years), sex (boys or girls; in the analysis of the whole population), urinary creatinine (quartiles), race/ethnicity (Hispanic, non-Hispanic white, non-Hispanic black, and other race), family income (family income to poverty ratio: ≤1.30, 1.31 to 3.50, >3.50, or missing), TV watching (<2 hours/day, ≥2 hours/day), total energy intake (quartiles), and Healthy Eating Index-2010 score (quartiles).

Table 1

Association of urinary BPA, BPF, and BPS concentrations with general obesity in United States children

Variable	Quartile of bisphenol				P for trend	OR per unita
	Quartile 1	Quartile 2	Quartile 3	Quartile 4
BPA
Median, ng/mL	0.46	1.00	1.71	3.98
Cases of obesity/no. of participants	35/196	51/194	40/173	39/182
OR (95% CI)
Model 1	1 (ref)	1.39 (0.83–2.33)	1.74 (0.74–4.07)	1.64 (0.83–3.21)	0.12	1.26 (0.94–1.68)
Model 2b	1 (ref)	1.47 (0.86–2.53)	1.96 (0.88–4.35)	1.74 (0.92–3.31)	0.08	1.29 (0.97–1.72)
Model 3	1 (ref)	1.42 (0.80–2.52)	1.89 (0.83–4.33)	1.65 (0.86–3.16)	0.14	1.24 (0.93–1.66)
BPF
Median, ng/mL	0.14	0.21	0.46	1.55
Cases of obesity/no. of participants	53/289	32/106	36/160	44/190
OR (95% CI)
Model 1	1 (ref)	1.62 (1.08–2.41)	1.18 (0.65–2.17)	1.20 (0.76–1.89)	0.57	1.05 (0.89–1.24)
Model 2b	1 (ref)	1.60 (1.12–2.30)	1.52 (0.87–2.66)	1.54 (1.02–2.32)	0.05	1.17 (1.00–1.37)
Model 3	1 (ref)	1.58 (1.14–2.20)	1.49 (0.83–2.67)	1.48 (0.93–2.35)	0.13	1.14 (0.96–1.36)
BPS
Median, ng/mL	0.07	0.20	0.47	1.30
Cases of obesity/no. of participants	29/156	42/209	45/197	49/183
OR (95% CI)
Model 1	1 (ref)	1.15 (0.57–2.36)	1.12 (0.58–2.15)	1.39 (0.49–3.96)	0.54	1.10 (0.81–1.51)
Model 2b	1 (ref)	1.27 (0.67–2.41)	1.19 (0.63–2.25)	1.36 (0.53–3.51)	0.62	1.08 (0.79–1.49)
Model 3	1 (ref)	1.20 (0.53–1.98)	1.24 (0.48–3.21)	1.24 (0.48–3.21)	0.73	1.06 (0.77–1.45)

Model 1: adjusted for age (in years), sex (boys, girls), and urinary creatinine (quartiles). Model 2: Model 1+race/ethnicity (Hispanic, non-Hispanic white, non-Hispanic black, and other race), family income (family income to poverty ratio: ≤1.30, 1.31 to 3.50, >3.50, or missing), TV watching (<2 hours/day, ≥2 hours/day), total energy intake (quartiles), and Healthy Eating Index-2010 score (quartiles). Model 3: Model 2+mutual adjustment for BPA, BPF, and BPS.

BPA, bisphenol A; BPF, bisphenol F; BPS, bisphenol S; OR, odds ratio; CI, confidence interval.

^aOR of obesity per unit increase in BPA, BPF, and BPS levels, ^bModel 2 is the main model.

Table 2

Association of urinary BPA, BPF, and BPS concentrations with abdominal obesity in United States children

Variable	Quartile of bisphenol				P for trend	OR per unita
	Quartile 1	Quartile 2	Quartile 3	Quartile 4
BPA
Median, ng/mL	0.46	1.01	1.71	3.98
Cases of obesity/no. of participants	69/192	68/190	60/167	65/181
OR (95% CI)
Model 1	1 (ref)	0.83 (0.41–1.66)	1.17 (0.57–2.40)	1.43 (0.80–2.57)	0.16	1.21 (0.93–1.57)
Model 2b	1 (ref)	0.83 (0.41–1.67)	1.24 (0.65–2.35)	1.47 (0.88–2.46)	0.08	1.23 (0.98–1.56)
Model 3	1 (ref)	0.83 (0.40–1.74)	1.21 (0.59–2.48)	1.42 (0.77–2.62)	0.19	1.20 (0.91–1.58)
BPF
Median, ng/mL	0.14	0.21	0.46	1.54
Cases of obesity/no. of participants	94/287	47/104	54/156	67/183
OR (95% CI)
Model 1	1 (ref)	1.48 (1.00–2.18)	0.87 (0.43–1.75)	1.25 (0.79–1.99)	0.46	1.07 (0.90–1.26)
Model 2b	1 (ref)	1.46 (1.02–2.10)	1.01 (0.54–1.88)	1.48 (0.92–2.38)	0.15	1.15 (0.95–1.39)
Model 3	1 (ref)	1.48 (1.05–2.07)	1.03 (0.55–1.92)	1.45 (0.85–2.50)	0.26	1.13 (0.91–1.40)
BPS
Median, ng/mL	0.07	0.20	0.47	1.29
Cases of obesity/no. of participants	56/153	65/207	64/191	77/179
OR (95% CI)
Model 1	1 (ref)	0.85 (0.57–1.29)	0.91 (0.49–1.71)	1.17 (0.53–2.57)	0.61	1.07 (0.83–1.37)
Model 2b	1 (ref)	0.89 (0.58–1.36)	0.93 (0.52–1.65)	1.13 (0.55–2.32)	0.71	1.05 (0.82–1.34)
Model 3	1 (ref)	0.90 (0.59–1.38)	0.85 (0.46–1.57)	1.06 (0.50–2.28)	0.85	1.02 (0.80–1.31)

Model 1: adjusted for age (in years), sex (boys, girls), and urinary creatinine (quartiles). Model 2: Model 1+race/ethnicity (Hispanic, non-Hispanic white, non-Hispanic black, and other race), family income (family income to poverty ratio: ≤1.30, 1.31 to 3.50, >3.50, or missing), TV watching (<2 hours/day, ≥2 hours/day), total energy intake (quartiles), and Healthy Eating Index-2010 score (quartiles). Model 3: Model 2+mutual adjustment for BPA, BPF, and BPS.

BPA, bisphenol A; BPF, bisphenol F; BPS, bisphenol S; OR, odds ratio; CI, confidence interval.

^aOR of obesity per unit increase in BPA, BPF, and BPS levels, ^bModel 2 is the main model.

Table 3

Associations of urinary BPA, BPF, and BPS concentrations with obesity by sex

Variable	Sex	Quartile 1	Quartile 2	Quartile 3	Quartile 4	P for trend	P for interaction
General obesitya
BPA	Boys	1 (ref)	1.20 (0.65–2.20)	2.59 (1.25–5.37)	2.78 (1.07–7.27)	0.02	0.02
	Girls	1 (ref)	2.29 (1.17–4.49)	1.47 (0.49–4.41)	1.10 (0.42–2.91)	0.92
BPF	Boys	1 (ref)	1.78 (0.98–3.25)	1.76 (0.72–4.31)	3.35 (2.02–5.53)	<0.001	<0.001
	Girls	1 (ref)	1.06 (0.50–2.26)	1.01 (0.60–1.71)	0.55 (0.25–1.25)	0.13
BPS	Boys	1 (ref)	0.66 (0.35–1.24)	0.86 (0.35–2.14)	1.01 (0.29–3.48)	0.78	0.36
	Girls	1 (ref)	2.63 (0.86–8.11)	2.20 (0.89–5.42)	2.14 (0.81–5.68)	0.23
Abdominal obesityb
BPA	Boys	1 (ref)	1.03 (0.51–2.08)	1.85 (0.90–3.79)	2.87 (1.60–5.16)	<0.001	0.003
	Girls	1 (ref)	0.71 (0.33–1.52)	0.89 (0.35–2.28)	0.83 (0.45–1.53)	0.64
BPF	Boys	1 (ref)	1.22 (0.64–2.31)	1.19 (0.48–2.96)	2.11 (1.23–3.62)	0.01	0.04
	Girls	1 (ref)	1.61 (0.81–3.19)	0.82 (0.42–1.64)	0.99 (0.50–1.95)	0.79
BPS	Boys	1 (ref)	0.58 (0.31–1.06)	0.72 (0.31–1.66)	1.10 (0.37–3.28)	0.64	0.62
	Girls	1 (ref)	1.34 (0.62–2.89)	1.20 (0.49–2.93)	1.34 (0.61–2.94)	0.55

Values are presented as odds ratio (95% confidence interval). Adjusted for age (in years), urinary creatinine (quartiles), race/ethnicity (Hispanic, non-Hispanic white, non-Hispanic black, and other race), family income (family income to poverty ratio: ≤1.30, 1.31 to 3.50, >3.50, or missing), TV watching (<2 hours/day, ≥2 hours/day), total energy intake (quartiles), and Healthy Eating Index-2010 score (quartiles).

BPA, bisphenol A; BPF, bisphenol F; BPS, bisphenol S.

^aFor general obesity analysis, the number of participants was 371 for boys and 374 for girls, ^bFor abdominal obesity analysis, the number of participants was 364 for boys and 366 for girls.

Figure & Data

References

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Citations to this article as recorded by  

• Obesogenic effects of six classes of emerging contaminants
  Siying Wu, Chaoyu Tong, Jing Liu
  Journal of Environmental Sciences.2025; 151: 252.     CrossRef
• Bisphenol S, bisphenol F, bisphenol a exposure and body composition in US adults
  Buyun Liu, Yuxiang Yan, Juan Xie, Jian Sun, Hans-Joachim Lehmler, Leonardo Trasande, Robert B. Wallace, Wei Bao
  Chemosphere.2024; 346: 140537.     CrossRef
• Associations of prenatal exposure to bisphenols with BMI growth trajectories in offspring within the first two years: evidence from a birth cohort study in China
  Chao Xiong, Kai Chen, Lu-Li Xu, Yi-Ming Zhang, Hua Liu, Meng-Lan Guo, Zhi-Guo Xia, Yu-Ji Wang, Xiao-Feng Mu, Xiao-Xuan Fan, Jing-Quan Chen, Yu-Ru Liu, Yuan-Yuan Li, Wei Xia, You-Jie Wang, Ai-Fen Zhou
  World Journal of Pediatrics.2024; 20(7): 701.     CrossRef
• Sex and Gender Differences on the Impact of Metabolism-Disrupting Chemicals on Obesity: A Systematic Review
  Massimo D’Archivio, Lucia Coppola, Roberta Masella, Alessia Tammaro, Cinzia La Rocca
  Nutrients.2024; 16(2): 181.     CrossRef
• The Role of Endocrine Disruptors Bisphenols and Phthalates in Obesity: Current Evidence, Perspectives and Controversies
  Maria Dalamaga, Dimitrios Kounatidis, Dimitrios Tsilingiris, Natalia G. Vallianou, Irene Karampela, Sotiria Psallida, Athanasios G. Papavassiliou
  International Journal of Molecular Sciences.2024; 25(1): 675.     CrossRef
• Sex-specific associations of bisphenol A and its substitutes with body fat distribution among US adults: NHANES 2011–2016
  Shili Zhang, Lingyan Dai, Ziyu Wan, Zhiwei Huang, Mengchen Zou, Haixia Guan
  Environmental Science and Pollution Research.2024; 31(5): 7948.     CrossRef
• EDC mixtures during pregnancy and body fat at 7 years of age in a Swedish cohort, the SELMA study
  Katherine Svensson, Chris Gennings, Christian Lindh, Hannu Kiviranta, Panu Rantakokko, Sverre Wikström, Carl-Gustaf Bornehag
  Environmental Research.2024; 248: 118293.     CrossRef
• Chemical Composition of Leachates from Hydraulic Fracturing Proppants from Surficial Releases in Southeastern New Mexico
  Matthew S. Varonka, Terry G. Gregston, Michael Villalobos, Jacqueline P. Green, William H. Orem
  Environmental Science & Technology Letters.2024; 11(3): 243.     CrossRef
• Associations of bisphenol A exposure with metabolic syndrome and its components: A systematic review and meta‐analysis
  Tianli Xiao, Zehua Huang, Chanjuan Zheng, Binh Quach, Yulian Zhu, Feifei Li, Wei Liang, Julien Baker, Christoph Reichetzeder, Berthold Hocher, Yide Yang
  Obesity Reviews.2024;[Epub]     CrossRef
• Relationship of bisphenol A substitutes bisphenol F and bisphenol S with adiponectin/leptin ratio among children from the environment and development of children cohort
  Hye Jin Lee, Yun Jeong Lee, Youn-Hee Lim, Hwa Young Kim, Bung-Nyun Kim, Johanna Inhyang Kim, Yong Min Cho, Yun-Chul Hong, Choong Ho Shin, Young Ah Lee
  Environment International.2024; 185: 108564.     CrossRef
• SWATH-MS reveals that bisphenol A and its analogs regulate pathways leading to disruption in insulin signaling and fatty acid metabolism
  Shabda E. Kulsange, Monika Sharma, Babasaheb Sonawane, Meera R. Jaiswal, Mahesh J. Kulkarni, B. Santhakumari
  Food and Chemical Toxicology.2024; 188: 114667.     CrossRef
• Fetal and Infancy Exposure to Phenols, Parabens, and Phthalates and Anthropometric Measurements up to 36 Months, in the Longitudinal SEPAGES Cohort
  Marion Ouidir, Aminata H. Cissé, Jérémie Botton, Sarah Lyon-Caen, Cathrine Thomsen, Amrit K. Sakhi, Azemira Sabaredzovic, Sam Bayat, Rémy Slama, Barbara Heude, Claire Philippat
  Environmental Health Perspectives.2024;[Epub]     CrossRef
• Unveiling the intricacies of BPA and BPS: comprehensive insights into its toxic effects using a cutting-edge microphysiological system
  Melissa Dibbernn Ganzerla, Nathalia de Carvalho Indolfo, Larissa Cleres Moreira Oliveira, Tabata Renee Doratioto, Thayná Mendonça Avelino, Rafael Junior de Azevedo, Larissa Bueno Tofani, Maiara Ferreira Terra, Giovanna Blazutti Elias, Irene Layane de Sous
  Toxicology in Vitro.2024; 98: 105849.     CrossRef
• A novel bellidifolin intervention mitigates nonalcoholic fatty liver disease-like changes induced by bisphenol F
  Jing Xue, Linwei Zhang, Jingxian Tao, Xuexue Xie, Xi Wang, Linlin Wu, Shuhu Du, Ninghua Tan, Yang Jin, Jianming Ju, Junting Fan, Jun Wang, Fei Huan, Rong Gao
  The Journal of Biomedical Research.2024; 38: 1.     CrossRef
• Experimental toxicological assessment of the degree of hazard of a mixture of chemical compounds migrating from materials intended for use in drinking water supply
  Anna V. Alekseeva, Yuriy A. Rakhmanin, Rufina I. Mikhailova, Natalia A. Egorova, Ludmila V. Khripach, Valentina V. Yurchenko
  Hygiene and sanitation.2024; 103(4): 365.     CrossRef
• Bisphenol F and Bisphenol S in a Complex Biomembrane: Comparison with Bisphenol A
  José Villalaín
  Journal of Xenobiotics.2024; 14(3): 1201.     CrossRef
• Exploring the role of genetic variability and exposure to bisphenols and parabens on excess body weight in Spanish children
  Viviana Ramírez, Yolanda Gálvez-Ontiveros, Vega Almazán Fernández de Bobadilla, Patricia González-Palacios, Inmaculada Salcedo-Bellido, Cristina Samaniego-Sánchez, María Jesús Álvarez-Cubero, Luis Javier Martínez-González, Alberto Zafra-Gómez, Ana Rivas
  Ecotoxicology and Environmental Safety.2024; 286: 117206.     CrossRef
• Dietary bisphenols exposure as an influencing factor of body mass index
  Yolanda Gálvez-Ontiveros, Celia Monteagudo, María Giles-Mancilla, José Joaquín Muros, Vega Almazán, María Alba Martínez-Burgos, Cristina Samaniego-Sánchez, Inmaculada Salcedo-Bellido, Ana Rivas, Alberto Zafra-Gómez
  Environmental Health.2024;[Epub]     CrossRef
• Effects of Bisphenol A on the Risk of Developing Obesity
  Mónica García García, Yolanda Picó, María Morales-Suárez-Varela
  Nutrients.2024; 16(21): 3740.     CrossRef
• Mitigating Dietary Bisphenol Exposure Through the Gut Microbiota: The Role of Next-Generation Probiotics in Bacterial Detoxification
  Paulina Emanowicz, Paulina Średnicka, Michał Wójcicki, Marek Roszko, Edyta Juszczuk-Kubiak
  Nutrients.2024; 16(21): 3757.     CrossRef
• Exposure to Bisphenol A, S, and F and its Association with Obesity and Diabetes Mellitus in General Adults of Korea: Korean National Environmental Health Survey (KoNEHS) 2015–2017
  Min Kyong Moon, Min Joo Kim, Inae Lee, Sunmi Kim, Sohyeon Choi, Jeongim Park, Yoon Hee Cho, Sooyeon Hong, Jiyoung Yoo, Hyunwoong Park, Gi Jeong Cheon, Young Joo Park, Kyungho Choi
  Exposure and Health.2023; 15(1): 53.     CrossRef
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  Mei Li, Tenglong Li, Juan Yin, Chunfeng Xie, Jianyun Zhu
  Toxicology.2023; 484: 153408.     CrossRef
• In silico profiling of endocrine-disrupting potential of bisphenol analogues and their halogenated transformation products
  Karolina Nowak, Žiga Jakopin
  Food and Chemical Toxicology.2023; 173: 113623.     CrossRef
• Transient developmental exposure to low doses of bisphenol F negatively affects neurogliogenesis and olfactory behaviour in adult mice
  Pieter Vancamp, Lucile Butruille, Anni Herranen, Anita Boelen, Jean-Baptiste Fini, Barbara A. Demeneix, Sylvie Remaud
  Environment International.2023; 172: 107770.     CrossRef
• Development of human dermal PBPK models for the bisphenols BPA, BPS, BPF, and BPAF with parallel-layered skin compartment: Basing on dermal administration studies in humans
  Man Hu, Zhichun Zhang, Yining Zhang, Ming Zhan, Weidong Qu, Gengsheng He, Ying Zhou
  Science of The Total Environment.2023; 868: 161639.     CrossRef
• Postnatal exposure to Bisphenol S induces liver injury in mice: Possible implication of PPARγ receptor
  Bessem Mornagui, Raja Rezg, Fadoua Neffati, Mohamed Fadhel Najjar, Ahmed Rejeb
  Toxicology and Industrial Health.2023; 39(5): 237.     CrossRef
• JAK3/STAT5b/PPARγ Pathway Mediates the Association between Di(2-ethylhexyl) Phthalate Exposure and Lipid Metabolic Disorder in Chinese Adolescent Students
  Qi Xu, Shuang Ding, Wen Qi, Xueting Zhang, Meng Zhang, Jiqiang Xing, Aipeng Ju, Liting Zhou, Lin Ye
  Chemical Research in Toxicology.2023; 36(5): 725.     CrossRef
• Bisphenol A substitutes and childhood obesity at 7 years: a cross-sectional study in Shandong, China
  Minyan Chen, Cheng Lv, Shanyu Zhang, Lap Ah Tse, Xinyu Hong, Xi Liu, Yu Ding, Ping Xiao, Ying Tian, Yu Gao
  Environmental Science and Pollution Research.2023; 30(29): 73174.     CrossRef
• Association between Bisphenol A exposure and body composition parameters in children
  Yong Guo, Cui Liu, Yu-Hong Deng, Jing Ning, Li Yu, Jie-Ling Wu
  Frontiers in Endocrinology.2023;[Epub]     CrossRef
• Urinary neonicotinoid insecticides and adiposity measures among 7-year-old children in northern China: A cross-sectional study
  Zhenping Lu, Yi Hu, Lap Ah Tse, Jinxia Yu, Zhuanning Xia, Xiaoning Lei, Yan Zhang, Rong Shi, Ying Tian, Yu Gao
  International Journal of Hygiene and Environmental Health.2023; 251: 114188.     CrossRef
• Mechanism of Bisphenol F Affecting Motor System and Motor Activity in Zebrafish
  Yeonhwa Kim, Seong Soon Kim, Byeong Heon Park, Kyu-Seok Hwang, Myung Ae Bae, Sung-Hee Cho, Suhyun Kim, Hae-Chul Park
  Toxics.2023; 11(6): 477.     CrossRef
• The effects of trans fat diet intake on metabolic parameters and pancreatic tissue in offspring of prenatal bisphenol A exposed rats
  Hala Abulehia, Noor Shafina Mohd Nor, Siti Hamimah Sheikh Abdul Kadir, Mardiana Abdul Aziz, Sarah Zulkifli
  Scientific Reports.2023;[Epub]     CrossRef
• Genetic background in the rat affects endocrine and metabolic outcomes of bisphenol F exposure
  Valerie A Wagner, Katie L Holl, Karen C Clark, John J Reho, Melinda R Dwinell, Hans-Joachim Lehmler, Hershel Raff, Justin L Grobe, Anne E Kwitek
  Toxicological Sciences.2023; 194(1): 84.     CrossRef
• Association of parabens and bisphenols with lung function in children aged 5–12 years from Shanghai, China
  Yi Hu, Hao Chen, Yuan Tian, Dan Wu, Angela Vinturache, Guodong Ding, Guangjun Yu
  International Journal of Hygiene and Environmental Health.2023; 252: 114210.     CrossRef
• Bisphenol A substitutes and obesity: a review of the epidemiology and pathophysiology
  Shane V. Varghese, Julianne M. Hall
  Frontiers in Endocrinology.2023;[Epub]     CrossRef
• Levels of Bisphenol A and its analogs in nails, saliva, and urine of children: a case control study
  Yolanda Gálvez-Ontiveros, Inmaculada Moscoso-Ruiz, Vega Almazán Fernández de Bobadilla, Celia Monteagudo, Rafael Giménez-Martínez, Lourdes Rodrigo, Alberto Zafra-Gómez, Ana Rivas
  Frontiers in Nutrition.2023;[Epub]     CrossRef
• Exposure to Bisphenol A and Its Analogs among Thai School-Age Children
  Nattakarn Numsriskulrat, Thanawan Teeranathada, Chansuda Bongsebandhu-Phubhakdi, Suphab Aroonparkmongkol, Kyungho Choi, Vichit Supornsilchai
  Toxics.2023; 11(9): 761.     CrossRef
• Bisphenol analogues inhibit human and rat 17β-hydroxysteroid dehydrogenase 1: 3D-quantitative structure-activity relationship (3D-QSAR) and in silico docking analysis
  Sailing Chen, Shaowei Wang, Jingyi Zheng, Han Lu, Huiqian Chen, Yunbing Tang, Nan Wang, Yang Zhu, Yiyan Wang, Ping Duan, Ren-shan Ge
  Food and Chemical Toxicology.2023; 181: 114052.     CrossRef
• Ecotoxicological Evaluation of Bisphenol A and Alternatives: A Comprehensive In Silico Modelling Approach
  Liadys Mora Lagares, Marjan Vračko
  Journal of Xenobiotics.2023; 13(4): 719.     CrossRef
• Bisphenol A (BPA) and Cardiovascular or Cardiometabolic Diseases
  Jeong-Hun Kang, Daisuke Asai, Riki Toita
  Journal of Xenobiotics.2023; 13(4): 775.     CrossRef
• Report of the Scientific Committee of the Spanish Agency for Food Safety and Nutrition (AESAN) on the available evidence in relation to the potential obesogenic activity of certain chemical compounds that may be present in foods
  Ana María Rivas Velasco, Irene Bretón Lesmes, Araceli Díaz Perales, Ángel Gil Izquierdo, María José González Muñoz, Victoria Moreno Arribas, María del Puy Portillo Baquedano, Silvia Pichardo Sánchez
  Food Risk Assess Europe.2023;[Epub]     CrossRef
• Regulatory and academic studies to derive reference values for human health: The case of bisphenol S
  Claire Beausoleil, Brigitte Le Magueresse-Battistoni, Catherine Viguié, Sylvie Babajko, Marie-Chantal Canivenc-Lavier, Nicolas Chevalier, Claude Emond, René Habert, Nicole Picard-Hagen, Sakina Mhaouty-Kodja
  Environmental Research.2022; 204: 112233.     CrossRef
• Urinary bisphenol concentrations and its association with metabolic disorders in the US and Korean populations
  Ji Yoon Choi, Jiyun Lee, Da-An Huh, Kyong Whan Moon
  Environmental Pollution.2022; 295: 118679.     CrossRef
• Associations of mid-childhood bisphenol A and bisphenol S exposure with mid-childhood and adolescent obesity
  Priya Gajjar, Yun Liu, Nan Li, Jessie P. Buckley, Aimin Chen, Bruce P. Lanphear, Heidi J. Kalkwarf, Kim M. Cecil, Kimberly Yolton, Joseph M. Braun
  Environmental Epidemiology.2022; 6(1): e187.     CrossRef
• Profile of Environmental Chemicals in the Korean Population—Results of the Korean National Environmental Health Survey (KoNEHS) Cycle 3, 2015–2017
  Sun Kyoung Jung, Wookhee Choi, Sung Yeon Kim, Sooyeon Hong, Hye Li Jeon, Youngkyung Joo, Chulwoo Lee, Kyungho Choi, Sungkyoon Kim, Kee-Jae Lee, Jiyoung Yoo
  International Journal of Environmental Research and Public Health.2022; 19(2): 626.     CrossRef
• The bisphenol F and bisphenol S and cardiovascular disease: results from NHANES 2013–2016
  Ruihua Wang, Qiaoyuan Fei, Shan Liu, Xueqiong Weng, Huanzhu Liang, Yingying Wu, Lin Wen, Guang Hao, Guangwen Cao, Chunxia Jing
  Environmental Sciences Europe.2022;[Epub]     CrossRef
• Bisphenols A and its analogues induce genotoxic damage in marine and freshwater amphipods
  Serena Cosentino, Federica Aureli, Valentina Iannilli
  Environmental Advances.2022; 7: 100183.     CrossRef
• Impact of environmental pollution on the obesogenic environment
  Adriana Martínez-Esquivel, Daniela Joyce Trujillo-Silva, V Gabriela Cilia-López
  Nutrition Reviews.2022; 80(7): 1787.     CrossRef
• Effects of BPZ and BPC on Oxidative Stress of Zebrafish under Different pH Conditions
  Ying Han, Yumeng Fei, Mingxin Wang, Yingang Xue, Yuxuan Liu
  Molecules.2022; 27(5): 1568.     CrossRef
• Race-specific associations of urinary phenols and parabens with adipokines in midlife women: The Study of Women's Health Across the Nation (SWAN)
  Seulbi Lee, Carrie Karvonen-Gutierrez, Bhramar Mukherjee, William H. Herman, Sung Kyun Park
  Environmental Pollution.2022; 303: 119164.     CrossRef
• Are BPA Substitutes as Obesogenic as BPA?
  Fabiana Oliviero, Alice Marmugi, Catherine Viguié, Véronique Gayrard, Nicole Picard-Hagen, Laila Mselli-Lakhal
  International Journal of Molecular Sciences.2022; 23(8): 4238.     CrossRef
• Aptamer-Based Biosensors for the Analytical Determination of Bisphenol A in Foodstuffs
  Marica Erminia Schiano, Avazbek Abduvakhidov, Michela Varra, Stefania Albrizio
  Applied Sciences.2022; 12(8): 3752.     CrossRef
• Bisphenol A exposure induces multiple effects in DOPC membrane models
  Mateus D. Maximino, Cibely S. Martin, Priscila Aléssio
  Journal of Molecular Liquids.2022; 359: 119253.     CrossRef
• Bisphenol S induces Agrp expression through GPER1 activation and alters transcription factor expression in immortalized hypothalamic neurons: A mechanism distinct from BPA-induced upregulation
  Katherine J. Xu, Neruja Loganathan, Denise D. Belsham
  Molecular and Cellular Endocrinology.2022; 552: 111630.     CrossRef
• Bisphenol S Alters the Steroidome in the Preovulatory Follicle, Oviduct Fluid and Plasma in Ewes With Contrasted Metabolic Status
  Ophélie Téteau, Philippe Liere, Antoine Pianos, Alice Desmarchais, Olivier Lasserre, Pascal Papillier, Claire Vignault, Marie-Emilie Lebachelier de la Riviere, Virginie Maillard, Aurélien Binet, Svetlana Uzbekova, Marie Saint-Dizier, Sebastien Elis
  Frontiers in Endocrinology.2022;[Epub]     CrossRef
• Relationship between bisphenol A, bisphenol S, and bisphenol F and serum uric acid concentrations among school-aged children
  Yun Jeong Lee, Youn-Hee Lim, Choong Ho Shin, Bung-Nyun Kim, Johanna Inhyang Kim, Yun-Chul Hong, Yong Min Cho, Young Ah Lee, Pasquale Avino
  PLOS ONE.2022; 17(6): e0268503.     CrossRef
• Associations of bisphenol exposure with thyroid hormones in pregnant women: a prospective birth cohort study in China
  Huishen Huang, Jun Liang, Peng Tang, Chuanxiang Yu, Haoran Fan, Qian Liao, Jinghua Long, Dongxiang Pan, Xiaoyun Zeng, Shun Liu, Dongping Huang, Xiaoqiang Qiu
  Environmental Science and Pollution Research.2022; 29(58): 87170.     CrossRef
• Association between urinary concentrations of bisphenol A substitutes and diabetes in adults
  Rafael Moreno-Gómez-Toledano, Esperanza Vélez-Vélez, María I Arenas, Marta Saura, Ricardo J Bosch
  World Journal of Diabetes.2022; 13(7): 521.     CrossRef
• Uncovering the functions of plasma proteins in ulcerative colitis and identifying biomarkers for BPA-induced severe ulcerative colitis: A plasma proteome analysis
  Chen Huang, Yuqin Wang, Xiao Lin, Ting Fung Chan, Keng Po Lai, Rong Li
  Ecotoxicology and Environmental Safety.2022; 242: 113897.     CrossRef
• Relationship between emergent BPA-substitutes and renal and cardiovascular diseases in adult population
  Rafael Moreno-Gómez-Toledano
  Environmental Pollution.2022; 313: 120106.     CrossRef
• Climate change and the water quality threats posed by the emerging contaminants per- and polyfluoroalkyl substances (PFAS) and microplastics
  Malcolm J. Gander
  Water International.2022; : 1.     CrossRef
• Endocrine disruptor chemicals as obesogen and diabetogen: Clinical and mechanistic evidence
  Niyazi Emre Kurşunoğlu, Banu Pinar Sarer Yurekli
  World Journal of Clinical Cases.2022; 10(31): 11226.     CrossRef
• Exposure to Bisphenol A Substitutes, Bisphenol S and Bisphenol F, and Its Association with Developing Obesity and Diabetes Mellitus: A Narrative Review
  Hend F. Alharbi, Raya Algonaiman, Rana Alduwayghiri, Thamer Aljutaily, Reham M. Algheshairy, Abdulkarim S. Almutairi, Razan M. Alharbi, Leena A. Alfurayh, Amjad A. Alshahwan, Amjad F. Alsadun, Hassan Barakat
  International Journal of Environmental Research and Public Health.2022; 19(23): 15918.     CrossRef
• Influence of BPA exposure, measured in saliva, on childhood weight
  Leticia Heras-González, Diana Espino, Maria Jose Jimenez-Casquet, Alejandro Lopez-Moro, Fatima Olea-Serrano, Miguel Mariscal-Arcas
  Frontiers in Endocrinology.2022;[Epub]     CrossRef
• Bisphenol S enhances gap junction intercellular communication in ovarian theca cells
  Jeremy Gingrich, Yong Pu, Brad L. Upham, Madeline Hulse, Sarah Pearl, Denny Martin, Anita Avery, Almudena Veiga-Lopez
  Chemosphere.2021; 263: 128304.     CrossRef
• Exposure to bisphenols and asthma morbidity among low-income urban children with asthma
  Lesliam Quirós-Alcalá, Nadia N. Hansel, Meredith McCormack, Antonia M. Calafat, Xiaoyun Ye, Roger D. Peng, Elizabeth C. Matsui
  Journal of Allergy and Clinical Immunology.2021; 147(2): 577.     CrossRef
• Evaluation of the effects of low nanomolar bisphenol A-like compounds’ levels on early human embryonic development and lipid metabolism with human embryonic stem cell in vitro differentiation models
  Xiaoxing Liang, Renjun Yang, Nuoya Yin, Francesco Faiola
  Journal of Hazardous Materials.2021; 407: 124387.     CrossRef
• Young children’s exposure to phenols in the home: Associations between house dust, hand wipes, silicone wristbands, and urinary biomarkers
  Jessica L. Levasseur, Stephanie C. Hammel, Kate Hoffman, Allison L. Phillips, Sharon Zhang, Xiaoyun Ye, Antonia M. Calafat, Thomas F. Webster, Heather M. Stapleton
  Environment International.2021; 147: 106317.     CrossRef
• Endocrine disrupting chemicals: Impacts on human fertility and fecundity during the peri-conception period
  Mark P. Green, Alexandra J. Harvey, Bethany J. Finger, Gerard A. Tarulli
  Environmental Research.2021; 194: 110694.     CrossRef
• Environmental Factors Involved in Maternal Morbidity and Mortality
  Abee L. Boyles, Brandiese E. Beverly, Suzanne E. Fenton, Chandra L. Jackson, Anne Marie Z. Jukic, Vicki L. Sutherland, Donna D. Baird, Gwen W. Collman, Darlene Dixon, Kelly K. Ferguson, Janet E. Hall, Elizabeth M. Martin, Thaddeus T. Schug, Alexandra J. W
  Journal of Women's Health.2021; 30(2): 245.     CrossRef
• Bisphenol-S and Bisphenol-F alter mouse pancreatic β-cell ion channel expression and activity and insulin release through an estrogen receptor ERβ mediated pathway
  Laura Marroqui, Juan Martinez-Pinna, Manuel Castellano-Muñoz, Reinaldo S. dos Santos, Regla M. Medina-Gali, Sergi Soriano, Ivan Quesada, Jan-Ake Gustafsson, José A. Encinar, Angel Nadal
  Chemosphere.2021; 265: 129051.     CrossRef
• Urinary bisphenol A concentrations and the risk of obesity in Korean adults
  Shinje Moon, Moon Young Seo, Kyungho Choi, Yoon-seok Chang, Shin-Hye Kim, Mi Jung Park
  Scientific Reports.2021;[Epub]     CrossRef
• Transcriptomic pathway and benchmark dose analysis of Bisphenol A, Bisphenol S, Bisphenol F, and 3,3',5,5'-Tetrabromobisphenol A in H9 human embryonic stem cells
  Vian Peshdary, Cheryl A. Hobbs, Timothy Maynor, Kim Shepard, Remi Gagné, Andrew Williams, Byron Kuo, Nikolai Chepelev, Leslie Recio, Carole Yauk, Ella Atlas
  Toxicology in Vitro.2021; 72: 105097.     CrossRef
• Prenatal exposure to bisphenols and cognitive function in children at 7 years of age in the Swedish SELMA study
  Carl-Gustaf Bornehag, Elin Engdahl, Maria Unenge Hallerbäck, Sverre Wikström, Christian Lindh, Joëlle Rüegg, Eva Tanner, Chris Gennings
  Environment International.2021; 150: 106433.     CrossRef
• Urinary bisphenol A levels in prepubertal children with exogenous obesity according to presence of metabolic syndrome
  Esra Aktağ, Kadriye Yurdakök, Siddika Songül Yalçın, Nurgün Kandemir
  Journal of Pediatric Endocrinology and Metabolism.2021; 34(4): 495.     CrossRef
• Metabolic pathways, alterations in miRNAs expression and effects of genetic polymorphisms of bisphenol a analogues: A systematic review
  Viviana Ramírez, Yolanda Gálvez-Ontiveros, Patricia Porras-Quesada, Luis Javier Martinez-Gonzalez, Ana Rivas, María Jesús Álvarez-Cubero
  Environmental Research.2021; 197: 111062.     CrossRef
• Dietary quality and bisphenols: trends in bisphenol A, F, and S exposure in relation to the Healthy Eating Index using representative data from the NHANES 2007–2016
  Irene van Woerden, Devon C Payne-Sturges, Corrie M Whisner, Meg Bruening
  The American Journal of Clinical Nutrition.2021; 114(2): 669.     CrossRef
• Bisphenol A and its effects on the systemic organs of children
  Sarah Zulkifli, Amirah Abdul Rahman, Siti Hamimah Sheikh Abdul Kadir, Noor Shafina Mohd Nor
  European Journal of Pediatrics.2021; 180(10): 3111.     CrossRef
• Bisphenols' occurrence in bivalves as sentinel of environmental contamination
  Elena Baralla, Valeria Pasciu, Maria Vittoria Varoni, Maria Nieddu, Roberto Demuro, Maria Piera Demontis
  Science of The Total Environment.2021; 785: 147263.     CrossRef
• Bisphenol F Exposure in Adolescent Heterogeneous Stock Rats Affects Growth and Adiposity
  Valerie A Wagner, Karen C Clark, Leslie Carrillo-Sáenz, Katie A Holl, Miriam Velez-Bermudez, Derek Simonsen, Justin L Grobe, Kai Wang, Andrew Thurman, Leah C Solberg Woods, Hans-Joachim Lehmler, Anne E Kwitek
  Toxicological Sciences.2021; 181(2): 246.     CrossRef
• Factors Associated with Exposure to Dietary Bisphenols in Adolescents
  Virginia Robles-Aguilera, Yolanda Gálvez-Ontiveros, Lourdes Rodrigo, Inmaculada Salcedo-Bellido, Margarita Aguilera, Alberto Zafra-Gómez, Celia Monteagudo, Ana Rivas
  Nutrients.2021; 13(5): 1553.     CrossRef
• Comparative Neurodevelopment Effects of Bisphenol A and Bisphenol F on Rat Fetal Neural Stem Cell Models
  Santokh Gill, V. M. Ruvin Kumara
  Cells.2021; 10(4): 793.     CrossRef
• Impact of short-term change of adiposity on risk of high blood pressure in children: Results from a follow-up study in China
  Yi-de Yang, Ming Xie, Yuan Zeng, Shuqian Yuan, Haokai Tang, Yanhui Dong, Zhiyong Zou, Bin Dong, Zhenghe Wang, Xiangli Ye, Xiuqin Hong, Qiu Xiao, Jun Ma, Raffaella Buzzetti
  PLOS ONE.2021; 16(9): e0257144.     CrossRef
• Life-Time Environmental Chemical Exposure and Obesity: Review of Epidemiological Studies Using Human Biomonitoring Methods
  Nayan Chandra Mohanto, Yuki Ito, Sayaka Kato, Michihiro Kamijima
  Frontiers in Endocrinology.2021;[Epub]     CrossRef
• Italian Children Exposure to Bisphenol A: Biomonitoring Data from the LIFE PERSUADED Project
  Sabrina Tait, Fabrizia Carli, Luca Busani, Demetrio Ciociaro, Veronica Della Latta, Annalisa Deodati, Enrica Fabbrizi, Anna Paola Pala, Francesca Maranghi, Roberta Tassinari, Giacomo Toffol, Stefano Cianfarani, Amalia Gastaldelli, Cinzia La Rocca
  International Journal of Environmental Research and Public Health.2021; 18(22): 11846.     CrossRef
• Bisphenol A disrupts apolipoprotein E expression through estrogen-related receptor gamma and DNA methlylation in the liver of male rare minnow Gobiocypris rarus
  Yingying Zhang, Zhu Zhu, Qiao Liu, Meng Zhang, Hui Yang, Wenzhi Wei
  Ecotoxicology and Environmental Safety.2021; 228: 113041.     CrossRef
• Metabolic Syndrome and Endocrine Disrupting Chemicals: An Overview of Exposure and Health Effects
  Elsi Haverinen, Mariana F. Fernandez, Vicente Mustieles, Hanna Tolonen
  International Journal of Environmental Research and Public Health.2021; 18(24): 13047.     CrossRef
• Obesogens in Children—An Uncharted Territory
  Mirjam Močnik, Nataša Marčun Varda
  Metabolites.2021; 11(12): 882.     CrossRef
• Synthetic Chemicals and Cardiometabolic Health Across the Life Course Among Vulnerable Populations: a Review of the Literature from 2018 to 2019
  Symielle A. Gaston, Linda S. Birnbaum, Chandra L. Jackson
  Current Environmental Health Reports.2020; 7(1): 30.     CrossRef
• Bisphenol A analogues (BPS and BPF) present a greater obesogenic capacity in 3T3-L1 cell line
  M.Á. Martínez, J. Blanco, J. Rovira, V. Kumar, J.L. Domingo, M. Schuhmacher
  Food and Chemical Toxicology.2020; 140: 111298.     CrossRef
• Urinary bisphenol A and its analogues and haemato-biochemical alterations of pregnant women in Korea
  Sora Kang, Bo Hye Shin, Jeoung A Kwon, Chan Wha Lee, Eun Kyo Park, Eun Young Park, Byungmi Kim
  Environmental Research.2020; 182: 109104.     CrossRef
• Historical exposure to non-persistent environmental pollutants and risk of type 2 diabetes in a Spanish sub-cohort from the European Prospective Investigation into Cancer and Nutrition study
  E. Salamanca-Fernández, L.M. Iribarne-Durán, M. Rodríguez-Barranco, F. Vela-Soria, N. Olea, M.J. Sánchez-Pérez, J.P. Arrebola
  Environmental Research.2020; 185: 109383.     CrossRef
• Association Between Bisphenol A Exposure and Risk of All-Cause and Cause-Specific Mortality in US Adults
  Wei Bao, Buyun Liu, Shuang Rong, Susie Y. Dai, Leonardo Trasande, Hans-Joachim Lehmler
  JAMA Network Open.2020; 3(8): e2011620.     CrossRef
• Using three statistical methods to analyze the association between exposure to 9 compounds and obesity in children and adolescents: NHANES 2005-2010
  Bangsheng Wu, Yi Jiang, Xiaoqing Jin, Li He
  Environmental Health.2020;[Epub]     CrossRef
• How was the Diabetes Metabolism Journal added to MEDLINE?
  Hye Jin Yoo
  Science Editing.2020; 7(2): 201.     CrossRef
• Adipogenic effects of prenatal exposure to bisphenol S (BPS) in adult F1 male mice
  Young-Ah Ahn, Hwayoung Baek, Miso Choi, Junbo Park, Soo Jin Son, Hyun Ju Seo, Jaeyun Jung, Je Kyung Seong, Jaehyouk Lee, Sungkyoon Kim
  Science of The Total Environment.2020; 728: 138759.     CrossRef
• Bisphenol A Analogues in Food and Their Hormonal and Obesogenic Effects: A Review
  Natalia Andújar, Yolanda Gálvez-Ontiveros, Alberto Zafra-Gómez, Lourdes Rodrigo, María Jesús Álvarez-Cubero, Margarita Aguilera, Celia Monteagudo, Ana Rivas
  Nutrients.2019; 11(9): 2136.     CrossRef
• Toxicological considerations of nano-sized plastics
  PA Stapleton
  AIMS Environmental Science.2019; 6(5): 367.     CrossRef
• Bisphenol A and adiposity measures in peripubertal boys from the INMA-Granada cohort
  Vicente Mustieles, Maribel Casas, Patricia Ferrando-Marco, Olga Ocón-Hernández, Iris Reina-Pérez, Andrea Rodríguez-Carrillo, Fernando Vela-Soria, Rocío Pérez-Lobato, Eva María Navarrete-Muñoz, Carmen Freire, Nicolás Olea, Mariana F. Fernández
  Environmental Research.2019; 173: 443.     CrossRef
• Trends and disparities in urinary BPA concentrations among U.S. emerging adults
  Irene van Woerden, Meg Bruening, Jessica Montresor-López, Devon C. Payne-Sturges
  Environmental Research.2019; 176: 108515.     CrossRef
• Concern about the Safety of Bisphenol A Substitutes
  Min Kyong Moon
  Diabetes & Metabolism Journal.2019; 43(1): 46.     CrossRef
• Urinary Bisphenols and Obesity Prevalence Among U.S. Children and Adolescents
  Melanie H Jacobson, Miriam Woodward, Wei Bao, Buyun Liu, Leonardo Trasande
  Journal of the Endocrine Society.2019; 3(9): 1715.     CrossRef

About this article

Liu B, Lehmler HJ, Sun Y, Xu G, Sun Q, Snetselaar LG, Wallace RB, Bao W. Association of Bisphenol A and Its Substitutes, Bisphenol F and Bisphenol S, with Obesity in United States Children and Adolescents. Diabetes Metab J. 2019;43(1):59-75.

Received: Mar 15, 2018; Accepted: Jun 04, 2018

DOI: https://doi.org/10.4093/dmj.2018.0045.

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