Abstract
This study investigates the effect of environmental risk factors among North Indian children aged between 6 and 16 years associated with body mass index by comparing fasting and non-fasting urine Bisphenol-A, urine creatinine, and serum thyroid levels with other potential confounding factors. A total of 301 children were enrolled, and term fasting and non-fasting were used based on the sample collection, either first morning or random. Children were grouped into obese, non-obese, and underweight categories based on age- and gender-specific Centre for Disease Control (CDC) 2000 growth chart and grouped according to their body mass index. The overall mean ± SD (standard deviation) of age (years) was 10.45±2.39 (boys age 10.38±2.38 and girls age 10.45±2.40). Urinary Bisphenol-A concentration (ng/mL ± SD) was higher among obese (2.40±4.70) than non-obese (1.30±1.67) and underweight (1.84±3.46) category children. Higher levels of fasting urinary Bisphenol-A (≥2 ng/mL) and thyroid-stimulating hormone (TSH) (≥12.7 μg/dL) were associated with obesity than those of non-fasting children. Being non-fasting among girls at quartile 4 (obese, >2.1800 ng/mL; underweight, >2.1325 ng/mL) had higher odds (obese adjusted odds ratio (aOR) 7.72 (95% CI 0.08–1368.52), underweight adjusted odds ratio (aOR) 12.45 (95% CI 1.55–171.24)] than fasting children. We recommend awareness programs and policy guidelines by engaging teachers and parents for the physical assessment of the presence of Bisphenol-A in food packaging materials to reduce the potential exposure to other chemical migrations sources.
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All data generated or analyzed during this study are included; any additional information is available from the corresponding author on reasonable request.
References
Anderson DJ, Brozek EM, Cox KJ, Porucznik CA, Wilkins DG (2014) Biomonitoring method for bisphenol A in human urine by ultra-high-performance liquid chromatography–tandem mass spectrometry. J Chromatogr B 953–954(March):53–61. https://doi.org/10.1016/j.jchromb.2014.01.039
Bahelka I, Stupka R, Čítek J, Šprysl M (2021) The impact of bisphenols on reproductive system and on offspring in pigs – a review 2011–2020. Chemosphere 263(January):128203. https://doi.org/10.1016/j.chemosphere.2020.128203
Bhandari R, Xiao J, Shankar A (2013) Urinary bisphenol A and obesity in U.S. children. Am J Epidemiol 177(11):1263–1270. https://doi.org/10.1093/aje/kws391
Biedermann-Brem S, Grob K, Fjeldal P (2008) Release of bisphenol A from polycarbonate baby bottles: mechanisms of formation and investigation of worst case scenarios. Eur Food Res Technol 227(4):1053–1060. https://doi.org/10.1007/s00217-008-0819-9
Cao X-L, Perez-Locas C, Dufresne G, Clement G, Popovic S, Beraldin F, Dabeka RW, Feeley M (2011) Concentrations of bisphenol A in the composite food samples from the 2008 Canadian Total Diet Study in Quebec City and dietary intake estimates. Food Addit Contaminants Part A 28(6):791–798. https://doi.org/10.1080/19440049.2010.513015
Carlsson A, Sørensen K, Andersson A-M, Frederiksen H, Juul A (2018) Bisphenol A, phthalate metabolites and glucose homeostasis in healthy normal-weight children. Endocrine Connections 7(1):232–238. https://doi.org/10.1530/EC-17-0344
Choi J, Eom J, Kim J, Lee S, Kim Y (2014) Association between some endocrine-disrupting chemicals and childhood obesity in biological samples of young girls: a cross-sectional study. Environ Toxicol Pharmacol 38(1):51–57. https://doi.org/10.1016/j.etap.2014.04.004
Cunha SC, Almeida C, Mendes E, Fernandes JO (2011) Simultaneous determination of bisphenol A and bisphenol B in beverages and powdered infant formula by dispersive liquid–liquid micro-extraction and heart-cutting multidimensional gas chromatography-mass spectrometry. Food Addit Contaminants Part A 28(4):513–526. https://doi.org/10.1080/19440049.2010.542551
Duncan S, Duncan EK, Fernandes RA, Buonani C, Bastos KD-N, Segatto AFM, Codogno JS, Gomes IC, Freitas IF (2011) Modifiable risk factors for overweight and obesity in children and adolescents from São Paulo. Brazil. BMC Public Health 11(1):585. https://doi.org/10.1186/1471-2458-11-585
Fernandez MF, Arrebola JP, Taoufiki J, Navalón A, Ballesteros O, Pulgar R, Vilchez JL, Olea N (2007) Bisphenol-A and chlorinated derivatives in adipose tissue of women. Reprod Toxicol 24(2):259–264. https://doi.org/10.1016/j.reprotox.2007.06.007
Flores G, Lin H (2013) Factors predicting overweight in U.S. kindergartners. Am J Clin Nutr 97(6):1178–1187. https://doi.org/10.3945/ajcn.112.052019
Geens T, Aerts D, Berthot C, Bourguignon J-P, Goeyens L, Lecomte P, Maghuin-Rogister G, Pironnet A-M, Pussemier L, Scippo M-L, van Loco J, Covaci A (2012) A review of dietary and non-dietary exposure to bisphenol-A. Food Chem Toxicol 50(10):3725–3740. https://doi.org/10.1016/j.fct.2012.07.059
González-Casanova JE, Pertuz-Cruz SL, Caicedo-Ortega NH, Rojas-Gomez DM (2020) Adipogenesis regulation and endocrine disruptors: emerging insights in obesity. Biomed Res Int 2020(February):1–13. https://doi.org/10.1155/2020/7453786
Goodson A, Summerfield W, Cooper I (2002) Survey of bisphenol A and bisphenol F in canned foods. Food Addit Contam 19(8):796–802. https://doi.org/10.1080/02652030210146837
Gupta N, Goel K, Shah P, Misra A (2012) Childhood obesity in developing countries: epidemiology, determinants, and prevention. Endocr Rev 33(1):48–70. https://doi.org/10.1210/er.2010-0028
Haq MEU, Akash MSH, Sabir S, Mahmood MH, Rehman K (2020) Human exposure to bisphenol A through dietary sources and development of diabetes mellitus: a cross-sectional study in Pakistani population. Environ Sci Pollut Res 27:26262–26275. https://doi.org/10.1007/s11356-020-09044-0
Heppe, Denise H. M., Jessica C. Kiefte-de Jong, Büşra Durmuş, Henriëtte A. Moll, Hein Raat, Albert Hofman, and Vincent W. V. Jaddoe. 2013. “Parental, fetal, and infant risk factors for preschool overweight: the generation R study.” Pediatr Res 73 (1): 120–127. https://doi.org/10.1038/pr.2012.145.
Jacobson MH, Woodward M, Bao W, Liu B, Trasande L (2019) Urinary bisphenols and obesity prevalence among U.S. children and adolescents. J Endocrine Soc 3(9):1715–1726. https://doi.org/10.1210/js.2019-00201
Junge KM, Leppert B, Jahreis S, Wissenbach DK, Feltens R, Grützmann K, Thürmann L, Bauer T, Ishaque N, Schick M, Bewerunge-Hudler M, Röder S, Bauer M, Schulz A, Borte M, Landgraf K, Körner A, Kiess W, von Bergen M, Stangl GI, Trump S, Eils R, Polte T, Lehmann I (2018) MEST mediates the impact of prenatal bisphenol A exposure on long-term body weight development. Clin Epigenetics 10(1):58. https://doi.org/10.1186/s13148-018-0478-z
Khader Y, Irshaidat O, Khasawneh M, Amarin Z, Alomari M, Batieha A (2009) Overweight and obesity among school children in Jordan: prevalence and associated factors. Matern Child Health J 13(3):424–431. https://doi.org/10.1007/s10995-008-0362-0
Kim KY, Lee E, Kim Y (2019) The association between bisphenol A exposure and obesity in children—a systematic review with meta-analysis. Int J Environ Res Public Health 16(14):2521. https://doi.org/10.3390/ijerph16142521
Link K, Moëll C, Garwicz S, Cavallin-Ståhl E, Björk J, Thilén U, Ahrén B, Erfurth EM (2004) Growth hormone deficiency predicts cardiovascular risk in young adults treated for acute lymphoblastic leukemia in childhood. J Clin Endocrinol Metab 89(10):5003–5012. https://doi.org/10.1210/jc.2004-0126
Malik VS, Attri SV, Khaiwal R, Bhalla AK, Dayal D, Bharti B, Kaur H, Singh S, Didwal G (2018) Relationship of high sensitive C-reactive protein levels to BMI and use of food packaging materials in North Indian obese children. In: 45th National Conference of Association of Clinical Biochemists of India. Kala Academy, Goa, India, 24th–27th October, 2018. Indian J Clin Biochem (Springer Nature) P106. https://doi.org/10.1007/s12291-018-0795-1
Malik VS, Attri SV, Khaiwal R, Dayal D, Bharti B, Bhalla AK, Singh S (2019) Relationship of thyroid hormone levels to anthropometric indices and use of food packaging materials in North Indian obese children. In: 2nd International Conference on Endocrinology and Metabolic Disorder, Berlin, Germany, May 20–21. J Pharm Sci Emerg Drugs 7:41. https://doi.org/10.4172/2380-9477-C1-030
Mansouri V, Ebrahimpour K, Poursafa P, Riahi R, Shoshtari-Yeganeh B, Hystad P, Kelishadi R (2019) Exposure to phthalates and bisphenol A is associated with higher risk of cardiometabolic impairment in normal weight children. Environ Sci Pollut Res 26:18604–18614. https://doi.org/10.1007/s11356-019-05123-z
McGuinn LA, Ghazarian AA, Joseph Su L, Ellison GL (2015) Urinary bisphenol A and age at menarche among adolescent girls: Evidence from NHANES 2003–2010. Environ Res 136(January):381–386. https://doi.org/10.1016/j.envres.2014.10.037
Misra A, Singhal N, Sivakumar B, Bhagat N, Jaiswal A, Khurana L (2011) Nutrition transition in India: secular trends in dietary intake and their relationship to diet-related non-communicable diseases: Nutrition Transition in India. J Diabetes 3(4):278–292. https://doi.org/10.1111/j.1753-0407.2011.00139.x
National Family Health Survey (NFHS-3) (2017) Ministry of Health and Family Welfare, Government of India. http://dhsprogram.com/pubs/pdf/frind3/00frontmatter00.pdf.
Noonan GO, Ackerman LK, Begley TH (2011) Concentration of bisphenol A in highly consumed canned foods on the U.S. market. J Agric Food Chem 59(13):7178–7185. https://doi.org/10.1021/jf201076f
“Obesity and Overweight Fact Sheet. IOTF Report.” 2015. World Health Organization. http://www.who.int/mediacentre/factsheets/fs311/en/.
Park C, Song H, Choi J, Sim S, Kojima H, Park J, Iida M, Lee YJ (2020) The mixture effects of bisphenol derivatives on estrogen receptor and androgen receptor. Environ Pollut 260(May):114036. https://doi.org/10.1016/j.envpol.2020.114036
Rudel RA, Gray JM, Engel CL, Rawsthorne TW, Dodson RE, Ackerman JM, Rizzo J, Nudelman JL, Brody JG (2011) Food packaging and bisphenol A and bis(2-Ethyhexyl) phthalate exposure: findings from a dietary intervention. Environ Health Perspect 119(7):914–920. https://doi.org/10.1289/ehp.1003170
Sajiki J, Miyamoto F, Fukata H, Mori C, Yonekubo J, Hayakawa K (2007) Bisphenol A (BPA) and its source in foods in Japanese markets. Food Addit Contam 24(1):103–112. https://doi.org/10.1080/02652030600936383
Sashindran VK, Dudeja P (2020) Obesity in school children in India. In: Public health in developing countries - challenges and opportunities [Working Title]. IntechOpen. https://doi.org/10.5772/intechopen.89602
Seltenrich N (2015) A hard nut to crack: reducing chemical migration in food-contact materials. Environ Health Perspect 123(7):A174–A179. https://doi.org/10.1289/ehp.123-A174
Shawky RM, Sadik DI (2012) Genetics of obesity. Egypt J Med Human Genet 13(1):11–17. https://doi.org/10.1016/j.ejmhg.2011.08.005
Trasande L, Attina TM, Blustein J (2012) Association between urinary bisphenol A concentration and obesity prevalence in children and adolescents. JAMA 308(11):1113–1121. https://doi.org/10.1001/2012.jama.11461
Vilarinho F, Sendón R, van der Kellen A, Vaz MF, Sanches Silva A (2019) Bisphenol A in food as a result of its migration from food packaging. Trends Food Sci Technol 91(September):33–65. https://doi.org/10.1016/j.tifs.2019.06.012
Wang B, Wang H, Zhou W, He Y, Zhou Y, Chen Y, Jiang Q (2014) Exposure to bisphenol A among school children in Eastern China: a multicenter cross-sectional study. J Exposure Sci Environ Epidemiol 24(6):657–664. https://doi.org/10.1038/jes.2014.36
Wolff MS, Teitelbaum SL, Windham G, Pinney SM, Britton JA, Chelimo C, Godbold J, Biro F, Kushi LH, Pfeiffer CM, Calafat AM (2007) Pilot study of urinary biomarkers of phytoestrogens, phthalates, and phenols in girls. Environ Health Perspect 115(1):116–121. https://doi.org/10.1289/ehp.9488
Xue J, Wu Q, Sakthivel S, Pavithran PV, Vasukutty JR, Kannan K (2015) Urinary levels of endocrine-disrupting chemicals, including bisphenols, bisphenol A diglycidyl ethers, benzophenones, parabens, and triclosan in obese and non-obese Indian children. Environ Res 137(February):120–128. https://doi.org/10.1016/j.envres.2014.12.007
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The Indian Council of Medical Research New Delhi provided fellowship grants (3/1/2(5)/OBS/2015/NCD-II).
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Vivek Singh Malik: methodology, formal analysis, writing, reviewing, and editing; Khaiwal Ravindra: conceptualization, methodology, formal analysis, writing, reviewing, and editing; Preety Rattan: methodology and formal analysis; Devi Dayal: discussion, validation, writing, reviewing, and editing; Savita Verma Attri: methodology, validation, discussion, writing, reviewing, and editing.
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The study was approved by the Institutional Ethics Committee (N.K./3639/PhD/8326). All the measures followed during the study adhered to the Helsinki Declaration of 1975, as revised in 2008.
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Highlights:
• First investigation of urinary Bisphenol-A in Indian children association with BMI.
• The study urges a cautious interpretation of fasting and non-fasting biological samples.
• Bisphenol-A could lead to both, i.e., obesity and underweight among children.
• An odds ratio shows an association among the obese, non-obese, and underweight children.
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Malik, V.S., Ravindra, K., Rattan, P. et al. Environmental exposure to urinary Bisphenol-A in North Indian children aged between 6 and 16 years and its association with body mass index. Environ Sci Pollut Res 28, 29085–29095 (2021). https://doi.org/10.1007/s11356-021-12555-z
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DOI: https://doi.org/10.1007/s11356-021-12555-z