Endocrine

, Volume 55, Issue 3, pp 666–681 | Cite as

The influence of phthalates and bisphenol A on the obesity development and glucose metabolism disorders

  • Milica Medic Stojanoska
  • Natasa Milosevic
  • Natasa Milic
  • Ludovico Abenavoli
Review

Abstract

The prevalence of obesity and type 2 diabetes mellitus epidemics presents a great health problem worldwide. Beside the changes in diet and decreased physical activity, there is growing interest in endocrine disrupting chemicals that may have effects on these conditions. Among them, the role of certain phthalates and bisphenol A is confirmed. We have summarized the existing literature on this issue including cross-sectional, follow up epidemiological studies and in vivo and in vitro studies. Most data support the effects of bisphenol A and some phthalates, such as di-2-ethyl-hexyl phthalate, diethyl phthalate, dibuthyl phthalate, dimethyl phthalate, dibenzyl phthalate, diisononyl phthalate and others on the development obesity and type 2 diabetes mellitus. These endocrine disrupting chemicals interfere with different cell signaling pathways involved in weight and glucose homeostasis. Since the data are rather inconsistent, there is a need for new, well-designed prospective studies.

Keywords

Phthalates Bisphenol A Obesity Glucose metabolism Metabolic syndrome 

References

  1. 1.
    World Health Organization, Obesity and overweight. (2015), http://www.who.int/mediacentre/factsheets/fs311/en/. Accessed 03 Mar 2016
  2. 2.
    S.D. De Ferranti, S.K. Osganian, Epidemiology of pediatric metabolic syndrome and type 2 diabetes mellitus. Diabetes Vasc. Dis. Res. 4, 285–296 (1995)CrossRefGoogle Scholar
  3. 3.
    G.A. Bray, T. Bellanger, Epidemiology, trends, and morbidities of obesity and the metabolic syndrome. Endocrine 29, 109–117 (2006)CrossRefPubMedGoogle Scholar
  4. 4.
    P. Almeda-Valdes, C.A. Aguilar-Salinas, M. Uribe, S.C. Quinteros, N. Méndez-Sánchez, Impact of anthropometric cutoff values in determining the prevalence of metabolic alterations. Eur. J. Clin. Investig. (2016). doi:10.1111/eci.12672
  5. 5.
    A. De Lorenzo, L. Soldati, F. Sarlo, M. Calvani, N. Di Lorenzo, L. Di Renzo, New obesity classification criteria as a tool for bariatric surgery indication. World J. Gastroenterol. (2016). 10.3748/wjg.v22.i2.681
  6. 6.
    L. Guariguata, D.R. Whiting, I. Hambleton, J. Beagley, V. Linnenkamp, J.E. Show, IDF Atlas. Global estimates of diabetes prevalence for 2013 and projections for 2035. Diabetes Res. Clin. Pract. (2014). doi:10.1016/j.diabres.2013.11.002
  7. 7.
    R.B. Rosenbloom, J.R. Joe, R.S. Young, W.E. Winter, Emerging epidemic of type 2 diabetes in youth. Diabetes Care 22, 345–354 (1999)CrossRefPubMedGoogle Scholar
  8. 8.
    E. Diamanti-Kandarakis, J.P. Bourguignon, L.C. Giudice, R. Hauser, G.S. Prins, A.M. Soto, R.T. Zoeller, A.C. Gore, Endocrine-disrupting chemicals: an Endocrine Society scientific statement. Endocr. Rev. (2009). doi:10.1210/er.2009-0002
  9. 9.
    International Program for Chemical Safety (IPCS) in Global assessment of the state-of-the-science of endocrine disruptors Chapter 1, Executive Summary. (2010), http://www.who.int/ipcs/publications/en/ch1.pdf. Accessed 03 Mar 2016
  10. 10.
    L.N. Vandenberg, T. Colborn, T.B. Hayes, J.J. Heindel, D.R. Jacobs Jr., D.H. Lee, T. Shioda, A.M. Soto, F.S. vom Saal, W.V. Welshons, R.T. Zoeller, J.P. Myers, Hormones and endocrine-disrupting chemicals: low-dose effects and nonmonotonic dose responses. Endocr. Rev. (2012). doi:10.1210/er.2011-1050
  11. 11.
    I. Bajkin, A. Bjelica, T. Icin, V. Dobric, B.K. Zavisic, M.M. Stojanoska, Effects of phthalic acid esters on fetal health. Med. Pregl. 67, 172–175 (2014)CrossRefPubMedGoogle Scholar
  12. 12.
    A.C. Gore, V.A. Chappell, S.E. Fenton, J.A. Flaws, A. Nadal, G.S. Prins, J. Toppari, R.T. Zoeller, Executive summary to EDC-2: the endocrine society’s second scientific statement on endocrine-disrupting chemicals. Endocr. Rev. (2015). doi:10.1210/er.2015-1010
  13. 13.
    T. Suzuki, K. Yaguchi, S. Suzuki, T. Suga, Monitoring of phthalic acid monoesters in river water by solid-phase extraction and GC-MS determination. Environ. Sci. Technol. 35, 3757–3763 (2001)CrossRefPubMedGoogle Scholar
  14. 14.
    A.O. Earls, I.P. Axford, J.H. Braybrook, Gas chromatography-mass spectrometry determination of the migration of phthalate plasticisers from polyvinyl chloride toys and childcare articles. J. Chromatogr. A 983, 237–246 (2003)CrossRefPubMedGoogle Scholar
  15. 15.
    J. Bosnir, D. Puntaric, A. Galic, I. Skes, T. Dijanic, M. Klaric, M. Grgic, M. Curkovic, Z. Smit, Migration of phthalates from plastic containers into soft drinks and mineral water. Food Technol. Biotechnol. 45, 91–95 (2007)Google Scholar
  16. 16.
    CDC (Centers for Disease Control and Prevention) Fourth National Report on Human Exposure to Environmental Chemicals, Updates tables.(2015). http://www.cdc.gov/exposurereport/. Accessed 03 March 2016
  17. 17.
    D.W. Liang, T. Zhang, H.H. Fang, J. He, Phthalates biodegradation in the environment. Appl. Microbiol. Biotechnol. (2008). doi:10.1007/s00253-008-1548-5
  18. 18.
    Lowell Center for Sustainable Production UI. Phthalates and their Alternatives. Health and Environmental Concerns. Lowell Center for Sustainable Production, University of Massachusetts, Lowell (2011). http://www.sustainableproduction.org/downloads/DEHP%20Full%20Text.pdf. Accessed 03 Mar 2016
  19. 19.
    R. Mankidy, S. Wiseman, H. Ma, J.P. Giesy, Biological impact of phthalates. Toxicol. Lett. (2013). doi:10.1016/j.toxlet.2012.11.025
  20. 20.
    H. Fredricksen, N.E. Skakkebaek, A.M. Andersson, Metabolism of phthalates in humans. Mol. Nutr. Food Res. 51, 899–911 (2007)CrossRefGoogle Scholar
  21. 21.
    ATSDR, Toxicological profile for di-(2-ethylhexyl) phthalate (DEHP). Atlanta: Agency for toxic substances and disease registry. http://www.atsdr.cdc.gov/toxprofiles Accessed 03 Mar 2016
  22. 22.
    M. Medic Stojanoska, B. Vukovic, J. Novakovic Paro, I. Bajkin, T. Icin, N. Milic, A. Milankov, B. Kovacev Zavisic, Association between urinary phthalate metabolites and diabetes mellitus: a pilot study. Diabetologia. 56, pS164 (2013)Google Scholar
  23. 23.
    H.D. Duntas, Chemical contamination and the thyroid. Endocrine. (2015). doi:10.1007/s12020-014-0442-4
  24. 24.
    M.J. Silva, D.B. Barr, J.A. Reidy, N.A. Malek, C.C. Hodge, S.P. Caudil, W.J. Brock, L.L. Needham, A.M. Calafat, Urinary levels of seven phthalate metabolites in the U.S population from the National Health and Nutrition Examination Survey (NHANES) 1999–2000. Environ. Health Perspect. 112, 331–338 (2004)CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    World Health Organization (WHO), Guidelines for Drinking Water Quality. Chapter 8: Chemical Aspects. 4th edn. Geneva: World Health Organization (2011). http://whqlibdoc.who.int Accessed 05 February 2012
  26. 26.
    US Environmental Protection Agency, Water: basic information about regulated drinking water contaminants. http://water.epa.gov/drink/contaminants/basicinformation/di_2_ethyl_phthalate.com. Accessed 03 Mar 2016
  27. 27.
    ECHA, Evaluation of new scientific evidence concerning the restrictions contained in Annex XVII to regulation (EC) № 1907/2006 (REACH). http://www.echa.europa.eu. Accessed 03 Mar 2016
  28. 28.
    J. Legler, T. Fletcher, E. Govarts, M. Porta, B. Blumberg, J.J. Heindel, L. Trasande, Obesity, diabetes, and associated costs of exposure to endocrine-disrupting chemicals in the European union. J. Clin. Endocrinol. Metab. (2015). doi:10.1210/jc.2014-4326
  29. 29.
    K.E. Zimmer, A.C. Gutleb, S. Ravnum, M. Krayer von Krauss, A.J. Murk, E. Ropstad, J.U. Skaare, G.S. Eriksen, J.L. Lyche, J.G. Koppe, B.L. Magnanti, A. Yang, A. Bartonova, H. Keune, Policy relevant results from an expert elicitation on the health risks of phthalates. Environ. Health (2012). doi:10.1186/1476-069X-11-S1-S6
  30. 30.
    A. Bergman, G. Becher, B. Blumberg, P. Bjerregaard, R. Bornman, I. Brandt, S.C. Casey, H. Frouin, L.C. Giudice, J.J. Heindel, T. Iguchi, S. Jobling, K.A. Kidd, A. Kortenkamp, P.M. Lind, D. Muir, R. Ocheing, E. Ropstad, P.S. Ross, N.E. Skakkebeak, J. Toppari, L.N. Vandenberg, T.J. Woodruff, R.T. Zoller, Disrupter science—a rebuttal of industry-sponsored critical comments on the UNEP/WHO report “State of the Science of Endocrine Disrupting Chemicals 2012”. Regul. Toxicol. Pharmacol. (2015). doi:10.1016/j.yrtph.2015.07.026
  31. 31.
    T. Göen, L. Dobler, J. Koschorreck, J. Müller, G.A. Wiesmüller, H. Drexler, M. Kolossa-Gehring, Trends of the internal phthalate exposure of young adults in Germany—follow-up of a retrospective human biomonitoring study. Int. J. Hyg. Environ. Health (2011). doi:10.1016/j.ijheh.2011.07.011
  32. 32.
    A.R. Zota, A.M. Calafat, T.J. Woodruff, Temporal trends in phthalate exposures: findings from the National Health and Nutrition Examination Survey, 2001–2010. Environ. Health Perspect. (2014). doi:10.1289/ehp.13066811
  33. 33.
    T. Geens, D. Aerts, C. Berthot, J.P. Bourguignon, L. Goeyens, P. Lecomte, G. Maghuin-Rogister, A.M. Pironnet, L. Pussemier, M.L, Scippo, J. Van Loco, A. Covaci, A review of dietary and non-dietary exposure to bisphenol-A. Food Chem. Toxicol. (2012). doi:10.1016/j.fct.2012.07.059
  34. 34.
    L.N. Vandenberg, M.V. Maffini, C. Sonnenschein, B.S. Rubin, A.M. Soto, Bisphenol-A and the great divide: a review of controversies in the field of endocrine disruption. Endocr. Rev. 30, 75–95 (2009). doi:10.1210/er.2008-0021 CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    J. Corrales, L.A. Kristofco, W.B. Steele, B.S. Yates, C.S. Breed, E.S. Williams, B.W. Brooks, Global assessment of bisphenol A in the environment: review and analysis of its occurrence and bioaccumulation. Dose-Response 13, 1–29 (2015)CrossRefGoogle Scholar
  36. 36.
    W. Völkel, T. Colnot, G.A. Csanády, J.G. Filser, W. Dekant, Metabolism and kinetics of bisphenol A in humans at low doses following oral administration. Chem. Res. Toxicol. 15, 1281–1287 (2002)CrossRefPubMedGoogle Scholar
  37. 37.
    L.N. Vandenberg, R. Hauser, M. Marcus, N. Olea, W.V. Welshons, Human exposure to bisphenol A (BPA). Reprod. Toxicol. 24, 139–177 (2007)CrossRefPubMedGoogle Scholar
  38. 38.
    R.W. Stahlhut, W.V. Welshons, S.H. Swan, Bisphenol A data in NHANES suggest longer than expected half-life, substantial nonfood exposure, or both. Environ. Health. Perspect. 117, 784–789 (2009). doi:10.1289/ehp.0800376 CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    A.M. Calafat, X. Ye, L.Y. Wong, J.A. Reidy, L.L. Needham, Exposure of the U.S. population to bisphenol A and 4-tertiary-octylphenol: 2003–2004. Environ. Health Perspect. (2008). doi:10.1289/ehp.10753
  40. 40.
    D. Caserta, G. Bordi, F. Ciardo, R. Marci, C. La Rocca, S. Tait, B. Bergamasco, L. Stecca, A. Mantovani, C. Guerranti, E.L. Fanello, G. Perra, F. Borghini, S.E. Focardi, M. Moscarini, The influence of endocrine disruptors in a selected population of infertile women. Gynecol. Endocrinol. (2013). doi:10.3109/09513590.2012.758702
  41. 41.
    T. Takeuchi, O. Tsutsumi, Serum bisphenol A concentrations showed gender differences, possibly linked to androgen levels. Biochem. Biophys. Res. Commun. 291, 76–78 (2002)CrossRefPubMedGoogle Scholar
  42. 42.
    E.S. Barrett, M. Sobolewski, Polycystic ovary syndrome: do endocrine disrupting chemicals play a role? Semin. Reprod. Med. (2014). doi:10.1055/s-0034-1371088
  43. 43.
    J.D. Meeker, A.M. Calafat, R. Hauser, Urinary bisphenol A concentrations in relation to serum thyroid and reproductive hormone levels in men from an infertility clinic. Environ. Sci. Technol. (2010). doi:10.1021/es9028292
  44. 44.
    D. Li, Z. Zhou, D. Qing, Y. He, T. Wu, M. Miao, J. Wang, X. Weng, J.R. Ferber, L.J. Herrinton, Q. Zhu, E. Gao, H. Checkoway, W. Yuan, Occupational exposure to bisphenol-A (BPA) and the risk of self-reported male sexual dysfunction. Hum. Reprod. (2010). doi:10.1093/humrep/dep381
  45. 45.
    J.D. Meeker, S. Ehrlich, T.L. Toth, D.L. Wright, A.M. Calafat, A.T. Trisini, X. Ye, R. Hauser, Semen quality and sperm DNA damage in relation to urinary bisphenol A among men from an infertility clinic. Reprod. Toxicol. (2010). doi:10.1016/j.reprotox.2010.07.005
  46. 46.
    M. Miao, W. Yuan, Y. He, Z. Zhou, J. Wang, E. Gao, G. Li, D.K. Li, In utero exposure to bisphenol-A and anogenital distance of male offspring. Birth Defects Res. A Clin. Mol. Teratol. (2011). doi:10.1002/bdra.22845
  47. 47.
    A.B. Ropero, P. Alonso-Magdalena, E. García-García, C. Ripoll, E. Fuentes, A. Nadal, Bisphenol-A disruption of the endocrine pancreas and blood glucose homeostasis. Int. J. Androl. 31, 194–200 (2008)CrossRefPubMedGoogle Scholar
  48. 48.
    E.R. Hugo, T.D. Brandebourg, J.G. Woo, J. Loftus, J.W. Alexander, N. Ben-Jonathan, Bisphenol A at environmentally relevant doses inhibits adiponectin release from human adipose tissue explants and adipocytes. Environ. Health Perspect. (2008). doi:10.1289/ehp.11537
  49. 49.
    A. Shankar, S. Teppala, Relationship between urinary bisphenol A levels and diabetes mellitus. J. Clin. Endocrinol. Metab. (2011). doi:10.1210/jc.2011-1682
  50. 50.
    M.K. Silver, M.S. O’Neill, M.R. Sowers, S.K. Park, Urinary bisphenol A and type-2 diabetes in U.S. adults: data from NHANES 2003-2008. PLoS One. (2011). doi:10.1371/journal.pone.0026868
  51. 51.
    A. Shankar, S. Teppala, Urinary bisphenol A and hypertension in a multiethnic sample of US adults. J. Environ. Public Health 2012, 481641 (2012)CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    A. Shankar, S. Teppala, C. Sabanayagam, Bisphenol a and peripheral arterial disease: results from the NHANES. Environ. Health Perspect. (2012). doi:10.1289/ehp.1104114
  53. 53.
    J.R. Rochester, Bisphenol A and human health: a review of the literature. Reprod. Toxicol. (2013). doi:10.1016/j.reprotox.2013.08.008
  54. 54.
    C.M. Metz, Bisphenol A: understanding the controversy. Workplace Health Saf. (2016). doi:10.1177/2165079915623790
  55. 55.
    European Food Safety Association, Scientific opinion on the risks to public health related to the presence of bisphenol A (BPA) in foodstuffs. EFSA J. 2015;13(1):3978. doi:10.2903/j.efsa.2015.3978, http://www.efsa.europa.eu/en/topics/topic/bisphenol. Accessed 03 Mar 2016
  56. 56.
    P.F. Baillie-Hamilton, Chemical toxins: a hypothesis to explain global obesity epidemic. J. Altern. Complement. Med. 8, 185–192 (2002)CrossRefPubMedGoogle Scholar
  57. 57.
    R.W. Stahlhut, E. van Wijngaarden, T.D. Dye, S. Cook, S.H. Swan, Concentrations of urinary phthalate metabolites are associated with increased waist circumference and insulin resistance in adult U.S. males. Environ. Health Perspect. 115, 876–882 (2007)CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    E.E. Hatch, J.W. Nelson, M.M. Qureshi, J. Weinberg, L.L. Moore, M. Singer, T.F. Webster, Association of urinary phthalate metabolite concentrations with body mass index and waist circumference: a cross-sectional study of NHANES data, 1999–2002. Environ. Health (2008). doi:10.1186/1476-069X-7-27
  59. 59.
    M. Medic Stojanoska, A. Milankov, B. Vukovic, D. Vukcevic, J. Sudji, I. Bajkin, N. Curic, T. Icin, B. Kovacev Zavisic, N. Milic, Do diethyl phthalate (DEP) and di-2-ethylhexyl phthalate (DEHP) influence the metabolic syndrome parameters? Pilot study. Environ. Monit. Assess. (2015). doi:10.1007/s10661-015-4754-5
  60. 60.
    P.M. Lind, V. Roos, M. Rönn, L. Johansson, H. Ahlström, J. Kullberg, L. Lind, Serum concentrations of phthalate metabolites are related to abdominal fat distribution two years later in elderly women. Environ. Health (2012). doi:10.1186/1476-069X-11-21
  61. 61.
    Y. Song, R. Hauser, F.B. Hu, A.A. Franke, S. Liu, Q. Sun, Urinary concentrations of bisphenol A and phthalate metabolites and weight change: a prospective investigation in US women. Int. J. Obes. (Lond.) (2014). doi:10.1038/ijo.2014.63
  62. 62.
    S.L. Teitelbaum, N. Mervish, E.L. Moshier, N. Vangeepuram, M.P. Galvez, A.M. Calafat, M.J. Silva, B.L. Brenner, M.S. Wolff, Associations between phthalate metabolite urinary concentrations and body size measures in New York city children. Environ. Res. (2012). doi:10.1016/j.envres.2011.12.006
  63. 63.
    A. Smerieri, C. Testa, P. Lazzeroni, F. Nuti, E. Grossi, S. Cesari, L. Montanini, G. Latini, S. Bernasconi, A.M. Papini, M.E. Street, Di-(2-ethylhexyl) phthalate metabolites in urine show age-related changes and associations with adiposity and parameters of insulin sensitivity in childhood. PLoS One (2015). doi:10.1371/journal.pone.0117831
  64. 64.
    C. Philippat, M. Mortamais, C. Chevrier, C. Petit, A.M. Calafat, X. Ye, M.J. Silva, C. Brambilla, I. Pin, M.A. Charles, S. Cordier, R. Slama, Exposure to phthalates and phenols during pregnancy and offspring size at birth. Environ. Health Perspect. (2012). doi:10.1289/ehp.1103634
  65. 65.
    J.H. Kim, H. Park, J. Lee, G. Cho, S. Choi, G. Choi, S.Y. Kim, S.H. Eun, E. Suh, S.K. Kim, H.J. Kim, G.H. Kim, J.J. Lee, Y.D. Kim, S. Eom, S. Kim, S. Kim, Association of diethylhexyl phthalate with obesity-related markers and body mass change from birth to 3 months of age. J. Epidemiol. Community Health (2016). doi:10.1136/jech-2015-206315
  66. 66.
    J. Ashley-Martin, L. Dodds, T.E. Arbuckle, A.S. Ettinger, G.D. Shapiro, M. Fisher, A.S. Morisset, S. Taback, M.F. Bouchard, P. Monnier, R. Dallaire, W.D. Fraser, A birth cohort study to investigate the association between prenatal phthalate and bisphenol A exposures and fetal markers of metabolic dysfunction. Environ. Health (2014). doi:10.1186/1476-069X-13-84
  67. 67.
    S.J. Kwack, E.Y. Han, J.S. Park, J.Y. Bae, I.Y. Ahn, S.K. Lim, D.H. Kim, D.E. Jang, L. Choi, H.J. Lim, T.H. Kim, N. Patra, K.L. Park, H.S. Kim, B.M. Lee, Comparison of the short term toxicity of phthalate diesters and monoesters in sprague-dawley male rats. Toxicol. Res. (2010). doi:10.5487/TR.2010.26.1.075
  68. 68.
    J.L. Carwile, K.B. Michels, Urinary bisphenol A and obesity: NHANES 2003–2006. Environ. Res. (2011). doi:10.1016/j.envres.2011.05.014
  69. 69.
    A. Shankar, S. Teppala, C. Sabanayagam, Urinary bisphenol a levels and measures of obesity: results from the national health and nutrition examination survey 2003–2008. ISRN Endocrinol. (2012). doi:10.5402/2012/965243
  70. 70.
    T. Wang, M. Li, B. Chen, M. Xu, Y. Xu, Y. Huang, J. Lu, Y. Chen, W. Wang, X. Li, Y. Liu, Y. Bi, S. Lai, G. Ning, Urinary bisphenol A (BPA) concentration associates with obesity and insulin resistance. J. Clin. Endocrinol. Metab. (2012). doi:10.1210/jc.2011-1989
  71. 71.
    T. Takeuchi, O. Tsutsumi, Y. Ikezuki, Y. Takai, Y. Taketani, Positive relationship between androgen and the endocrine disruptor, bisphenol A, in normal women and women with ovarian dysfunction. Endocr. J. 51, 165–169 (2004)CrossRefPubMedGoogle Scholar
  72. 72.
    N. Milić, D. Četojević-Simin, M. Milanović, J. Sudji, N. Milošević, N. Ćurić, L. Abenavoli, Medić-Stojanoska, M., Estimation of in vivo and in vitro exposure to bisphenol A as food contaminant. Food Chem. Toxicol. (2015). doi:10.1016/j.fct.2015.07.003
  73. 73.
    H.Y. Zhao, Y.F. Bi, L.Y. Ma, L. Zhao, T.G. Wang, L.Z. Zhang, B. Tao, L.H. Sun, Y.J. Zhao, W.Q. Wang, X.Y. Li, M.Y. Xu, J.L. Chen, G. Ning, J.M. Liu, The effects of bisphenol A (BPA) exposure on fat mass and serum leptin concentrations have no impact on bone mineral densities in non-obese premenopausal women. Clin. Biochem. (2012). doi:10.1016/j.clinbiochem.2012.08.024
  74. 74.
    T. Bushnik, D. Haines, P. Levallois, J. Levesque, J. Van Oostdam, C. Viau, Lead and bisphenol A concentrations in the Canadian population. Health Rep. 21, 7–18 (2010)PubMedGoogle Scholar
  75. 75.
    R. Bhandari, J. Xiao, A. Shankar, Urinary bisphenol A and obesity in U.S. children. Am. J. Epidemiol. (2013). doi:10.1093/aje/kws391
  76. 76.
    L. Trasande, T.M. Attina, J. Blustein, Association between urinary bisphenol A concentration and obesity prevalence in children and adolescents. JAMA. 308, 1113–1121 (2012)CrossRefPubMedGoogle Scholar
  77. 77.
    D.S. Eng, J.M. Lee, A. Gebremariam, J.D. Meeker, K. Peterson, V. Padmanabhan, Bisphenol A and chronic disease risk factors in US children. Pediatrics. 132, e637–e645 (2013)CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    D.K. Li, M. Miao, Z. Zhou, C. Wu, H. Shi, X. Liu, S. Wang, W. Yuan, Urine bisphenol-A level in relation to obesity and overweight in school-age children. PLoS One (2013). doi:10.1371/journal.pone.0065399s
  79. 79.
    H.X. Wang, Y. Zhou, C.X. Tang, J.G. Wu, Y. Chen, Q.W. Jiang, Association between bisphenol A exposure and body mass index in Chinese school children: a cross-sectional study. Environ. Health (2012). doi:10.1186/1476-069X-11-79
  80. 80.
    J. Xue, Q. Wu, S. Sakthivel, P.V. Pavithran, J.R. Vasukutty, K. Kannan, 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. (2015). doi:10.1016/j.envres.2014.12.007
  81. 81.
    M.S. Wolff, S.L. Teitelbaum, G. Windham, S.M. Pinney, J.A. Britton, C. Chelimo, J. Godbold, F. Biro, L.H. Kushi, C.M. Pfeiffer, A.M. Calafat, Pilot study of urinary biomarkers of phytoestrogens, phthalates, and phenols in girls. Environ. Health Perspect. 115, 116–121 (2007)CrossRefPubMedGoogle Scholar
  82. 82.
    W.C. Chou, J.L. Chen, C.F. Lin, Y.C. Chen, F.C. Shih, C.Y. Chuang, Biomonitoring of bisphenol A concentrations in maternal and umbilical cord blood in regard to birth outcomes and adipokine expression: a birth cohort study in Taiwan. Environ. Health (2011). doi:10.1186/1476-069X-10-94
  83. 83.
    K.G. Harley, R. Aguilar Schall, J. Chevrier, K. Tyler, H. Aguirre, A. Bradman, N.T. Holland, R.H. Lustig, A.M. Calafat, B. Eskenazi, Prenatal and postnatal bisphenol A exposure and body mass index in childhood in the CHAMACOS cohort. Environ. Health Perspect. (2013). doi:10.1289/ehp.1205548
  84. 84.
    P.M. Lind, B. Zethelius, L. Lind, Circulating levels of phthalate metabolites are associated with prevalent diabetes in the elderly. Diabetes Care (2012). doi:10.2337/dc11-2396
  85. 85.
    L. Olsén, L. Lind, P.M. Lind, Associations between circulating levels of bisphenol A and phthalate metabolites and coronary risk in the elderly. Ecotoxicol. Environ. Saf. (2012). doi:10.1016/j.ecoenv.2012.02.023
  86. 86.
    T. Huang, A.R. Saxena, E. Isganaitis, T. James-Todd, Gender and racial/ethnic differences in the associations of urinary phthalate metabolites with markers of diabetes risk: national health and nutrition examination survey 2001–2008. Environ. Health (2014). doi:10.1186/1476-069X-13-6
  87. 87.
    J.H. Kim, H.Y. Park, S. Bae, Y.H. Lim, Y.C. Hong, Diethylhexyl phthalates is associated with insulin resistance via oxidative stress in the elderly, a panel study. PLoS One (2013). doi:10.1371/journal.pone.0071392
  88. 88.
    T. James-Todd, R. Stahlhut, J.D. Meeker, S.G. Powell, R. Hauser, T. Huang, J. Rich-Edwards, Urinary phthalate metabolite concentrations and diabetes among women in the National Health and Nutrition Examination Survey (NHANES) 2001–2008. Environ. Health Perspect. (2012). doi:10.1289/ehp.11047177
  89. 89.
    Q. Sun, M.C. Cornelis, M.K. Townsend, D.K. Tobias, A.H. Eliassen, A.A. Franke, R. Hauser, F.B. Hu, Association of urinary concentrations of bisphenol A and phthalate metabolites with risk of type 2 diabetes: a prospective investigation in the Nurses’ Health Study (NHS) and NHSII cohorts. Environ. Health Perspect. (2014). doi:10.1289/ehp.1307201
  90. 90.
    K. Svensson, R.U. Hernández-Ramírez, A. Burguete-García, M.E. Cebrián, A.M. Calafat, L.L. Needham, L. Claudio, L. López-Carrillo, Phthalate exposure associated with self-reported diabetes among Mexican women. Environ. Res. (2011). doi:10.1016/j.envres.2011.05.015
  91. 91.
    E.P. Hines, A.M. Calafat, M.J. Silva, P. Mendola, S.E. Fenton, Concentrations of phthalate metabolites in milk, urine, saliva, and serum of lactating North Carolina women. Environ. Health Perspect. (2009). doi:10.1289/ehp.11610
  92. 92.
    T.M. Attina, L. Trasande, Association of exposure to di-2-ethylhexylphthalate replacements with increased insulin resistance in adolescents from NHANES 2009-2012. J. Clin. Endocrinol. Metab. (2015). doi:10.1210/jc.2015-1686
  93. 93.
    M.I. Martinelli, N.O. Mocchiutti, C.A. Bernal, Dietary di(2-ethylhexyl)phthalate-impaired glucose metabolism in experimental animals. Hum. Exp. Toxicol. 25, 531–538 (2006)CrossRefPubMedGoogle Scholar
  94. 94.
    J.N. Feige, A. Gerber, C. Casals-Casas, Q. Yang, C. Winkler, E. Bedu, M. Bueno, L. Gelman, J. Auwerx, F.J. Gonzalez, B. Desvergne, The pollutant diethylhexyl phthalate regulates hepatic energy metabolism via species-specific PPARalpha-dependent mechanisms. Environ. Health Perspect. (2010). doi:10.1289/ehp.0901217
  95. 95.
    C. Hao, X. Cheng, H. Xia, X. Ma, The endocrine disruptor mono-(2-ethylhexyl) phthalate promotes adipocyte differentiation and induces obesity in mice. Biosci. Rep. (2012). doi:10.1042/BSR20120042
  96. 96.
    S. Teppala, S. Madhavan, A. Shankar, Bisphenol A and metabolic syndrome: Results from NHANES. Int. J. Endocrinol. 2012, 598180 (2012). Article IDCrossRefPubMedPubMedCentralGoogle Scholar
  97. 97.
    I.A. Lang, T.S. Galloway, A. Scarlett, W.E. Henley, M. Depledge, R.B. Wallace, D. Melzer, Association of urinary bisphenol A concentration with medical disorders and laboratory abnormalities in adults. JAMA (2008). doi:10.1001/jama.300.11.1303
  98. 98.
    D. Melzer, N.E. Rice, C. Lewis, W.E. Henley, T.S. Galloway, Association of urinary bisphenol a concentration with heart disease: evidence from NHANES 2003/06. PLoS One (2010). doi:10.1371/journal.pone.0008673
  99. 99.
    R. Ahmadkhaniha, M. Mansouri, M. Yunesian, K. Omidfar, M.Z. Jeddi, B. Larijani, A. Mesdaghinia, N. Rastkari, Association of urinary bisphenol a concentration with type-2 diabetes mellitus. J. Environ. Health Sci. Eng. (2014). doi:10.1186/2052-336X-12-64
  100. 100.
    K. Kim, H. Park, Association between urinary concentrations of bisphenol A and type 2 diabetes in Korean adults: a population-based cross-sectional study. Int. J. Hyg. Environ. Health (2013). doi:10.1016/j.ijheh.2012.07.007
  101. 101.
    G. Ning, Y. Bi, T. Wang, M. Xu, Y. Xu, Y. Huang, M. Li, X. Li, W. Wang, Y. Chen, Y. Wu, J. Hou, A. Song, Y. Liu, S. Lai, Relationship of urinary bisphenol A concentration to risk for prevalent type 2 diabetes in Chinese adults: a cross-sectional analysis. Ann. Intern. Med. (2011). doi:10.7326/0003-4819-155-6-201109200-00005
  102. 102.
    F. Grün, B. Blumberg, Endocrine disrupters as obesogens. Mol. Cell. Endocrinol. (2009). doi:10.1016/j.mce.2009.02.018
  103. 103.
    E.E. Hatch, J.W. Nelson, R.W. Stahlhut, T.F. Webster, Association of endocrine disruptors and obesity: perspectives from epidemiological studies. Int. J. Androl. (2010). doi:10.1111/j.1365-2605.2009.01035.x
  104. 104.
    M. Grimaldi, A. Boulahtouf, V. Delfosse, E. Thouennon, W. Bourguet, P. Balaguer, Reporter cell lines for the characterization of the interactions between human nuclear receptors and endocrine disruptors. Front. Endocrinol. (Lausanne) (2015). doi:10.3389/fendo.2015.00062
  105. 105.
    J.R. Barrett, To each his own: DEHP yields species-specific metabolic phenotypes. Environ. Health Perspect. (2010). doi:10.1289/ehp.118-a81a
  106. 106.
    B. Migliarini, C.C. Piccinetti, A. Martella, F. Maradonna, G. Gioacchini, O. Carnevali, Perspectives on endocrine disruptor effects on metabolic sensors. Gen. Comp. Endocrinol. (2011). doi:10.1016/j.ygcen.2010.11.025
  107. 107.
    J. Boberg, S. Metzdorff, R. Wortziger, M. Axelstad, L. Brokken, A.M. Vinggaard, M. Dalgaard, C. Nellemann, Impact of diisobutyl phthalate and other PPAR agonists on steroidogenesis and plasma insulin and leptin levels in fetal rats. Toxicology (2008). doi:10.1016/j.tox.2008.05.020
  108. 108.
    J. Kwintkiewicz, Y. Nishi, T. Yanase, L.C. Giudice, Peroxisome proliferator-activated receptor-gamma mediates bisphenol A inhibition of FSH-stimulated IGF-1, aromatase, and estradiol in human granulosa cells. Environ. Health Perspect. (2010). doi:10.1289/ehp.0901161
  109. 109.
    A. Riu, M. Grimaldi, A. le Maire, G. Bey, K. Phillips, A. Boulahtouf, E. Perdu, D. Zalko, W. Bourguet, P. Balaguer, Peroxisome proliferator-activated receptor γ is a target for halogenated analogs of bisphenol A. Environ. Health Perspect. (2011). doi:10.1289/ehp.1003328
  110. 110.
    P. Alonso-Magdalena, S. Morimoto, C. Ripoll, E. Fuentes, A. Nadal, The estrogenic effect of bisphenol A disrupts pancreatic beta-cell function in vivo and induces insulin resistance. Environ. Health. Perspect. 114, 106–112 (2006)CrossRefPubMedGoogle Scholar
  111. 111.
    M.K. Moon, I.K. Jeong, T. Jung Oh, H.Y. Ahn, H.H. Kim, Y.J. Park, H.C. Jang, K.S. Park, Long-term oral exposure to bisphenol A induces glucose intolerance and insulin resistance. J. Endocrinol. (2015). doi:10.1530/JOE-14-0714
  112. 112.
    H. Masuno, T. Kidani, K. Sekiya, K. Sakayama, T. Shiosaka, H. Yamamoto, K. Honda, Bisphenol A in combination with insulin can accelerate the conversion of 3T3-L1 fibroblasts to adipocytes. J. Lipid. Res. 43, 676–684 (2002)PubMedGoogle Scholar
  113. 113.
    S.H. Swan, Environmental phthalate exposure in relation to reproductive outcomes and other health endpoints in humans. Environ. Res. 108, 177–184 (2008)CrossRefPubMedPubMedCentralGoogle Scholar
  114. 114.
    N.K. Chaturvedi, S. Kumar, S. Negi, R.K. Tyagi, Endocrine disruptors provoke differential modulatory responses on androgen receptor and pregnane and xenobiotic receptor:potential implications in metabolic disorders. Mol. Cell. Biochem. (2010). doi:10.1007/s11010-010-0583-6
  115. 115.
    F.S. Vom Saal, S.C. Nagel, B.L. Coe, B.M. Angle, J.A. Taylor, The estrogenic endocrine disrupting chemical bisphenol A (BPA) and obesity. Mol. Cell. Endocrinol. (2012). doi:10.1016/j.mce.2012.01.001
  116. 116.
    P. Thomas, J. Dong, Binding and activation of the seven-transmembrane estrogen receptor GPR30 by environmental estrogens: a potential novel mechanism of endocrine disruption. J. Steroid Biochem. Mol. Biol. 102, 175–179 (2006)CrossRefPubMedGoogle Scholar
  117. 117.
    H. Okada, T. Tokunaga, X. Liu, S. Takayanagi, A. Matsushima, Y. Shimohigashi, Direct evidence revealing structural elements essential for the high binding ability of bisphenol A to human estrogen-related receptor-gamma. Environ. Health Perspect. (2008). doi:10.1289/ehp.10587
  118. 118.
    É. Audet-Walsh, V. Giguére, The multiple universes of estrogen-related receptor α and γ in metabolic control and related diseases. Acta Pharmacol. Sin. (2015). doi:10.1038/aps.2014.121
  119. 119.
    Y. Sui, N. Ai, S.H. Park, J. Rios-Pilier, J.T. Perkins, W.J. Welsh, C. Zhou, Bisphenol A and its analogues activate human pregnane X receptor. Environ. Health Perspect. (2012). doi:10.1289/ehp.1104426
  120. 120.
    K. Ibhazehiebo, N. Koibuchi, Thyroid hormone receptor-mediated transcription is suppressed by low dose phthalate. Niger. J. Physiol. Sci. 26, 143–149 (2006)Google Scholar
  121. 121.
    Z.G. Sheng, Y. Tang, Y.X. Liu, Y. Yuan, B.Q. Zhao, X.J. Chao, B.Z. Zhu, Low concentrations of bisphenol a suppress thyroid hormone receptor transcription through a nongenomic mechanism. Toxicol. Appl. Pharmacol. (2012). doi:10.1016/j.taap.2011.12.018
  122. 122.
    R.T. Zoeller, R. Bansal, C. Parris, Bisphenol-A, an environmental contaminant that acts as a thyroid hormone receptor antagonist in vitro, increases serum thyroxine, and alters RC3/neurogranin expression in the developing rat brain. Endocrinology. 146, 607–612 (2005)CrossRefPubMedGoogle Scholar
  123. 123.
    P. Rajesh, S. Sathish, C. Srinivasan, J. Selvaraj, K. Balasubramanian, Phthalate is associated with insulin resistance in adipose tissue of male rat: role of antioxidant vitamins. J. Cell Biochem. (2013). doi:10.1002/jcb.24399
  124. 124.
    W. Wang, Z.R. Craig, M.S. Basavarajappa, K.S. Hafner, J.A. Flaws, Mono-(2ethylhexyl) phthalate induces oxidative stress and inhibits growth of mouse ovarian antral follicles. Biol. Reprod. (2012). doi:10.1095/biolreprod.112.102467
  125. 125.
    N. Ben-Jonathan, E.R. Hugo, T.D. Brandebourg, Effects of bisphenol A on adipokine release from human adipose tissue: implications for the metabolic syndrome. Mol. Cell. Endocrinol. (2009). doi:10.1016/j.mce.2009.02.022
  126. 126.
    D. Kamimura, K. Ishihara, T. Hirano, IL-6 signal transduction and its physiological roles: the signal orchestration model. Rev. Physiol. Biochem. Pharmacol. 149, 1–38 (2003)PubMedGoogle Scholar
  127. 127.
    M. Rydén, P. Arner, Tumour necrosis factor-alpha in human adipose tissue—from signalling mechanisms to clinical implications. J. Intern. Med. 262, 431–438 (2007)CrossRefPubMedGoogle Scholar
  128. 128.
    Y. Masuo, M. Ishido, M. Morita, S. Oka, Effects of neonatal treatment with 6-hydroxydopamine and endocrine disruptors on motor activity and gene expression in rats. Neural Plast. 11, 59–76 (2004)CrossRefPubMedPubMedCentralGoogle Scholar
  129. 129.
    S. Singh, S.S. Li, Phthalates: toxicogenomics and inferred human diseases. Genomics (2011). doi:10.1016/j.ygeno.2010.11.008
  130. 130.
    Y. Lin, J. Wei, Y. Li, J. Chen, Z. Zhou, L. Song, Z. Wei, Z. Lv, X. Chen, W. Xia, S. Xu, Developmental exposure to di(2-ethylhexyl) phthalate impairs endocrine pancreas and leads to long-term adverse effects on glucose homeostasis in the rat. Am. J. Physiol. Endocrinol. Metab. (2011). doi:10.1152/ajpendo.00233.2011
  131. 131.
    W.J. Crinnion, Toxic effects of the easily avoidable phthalates and parabens. Altern. Med. Rev. 15, 190–196 (2010)PubMedGoogle Scholar
  132. 132.
    J. Wei, Y. Lin, Y. Li, C. Ying, J. Chen, L. Song, Z. Zhou, Z. Lv, W. Xia, X. Chen, S. Xu, Perinatal exposure to bisphenol A at reference dose predisposes offspring to metabolic syndrome in adult rats on a high-fat diet. Endocrinology. (2011). doi:10.1210/en.2011-0045
  133. 133.
    J. Miyawaki, K. Sakayama, H. Kato, H. Yamamoto, H. Masuno, Perinatal and postnatal exposure to bisphenol a increases adipose tissue mass and serum cholesterol level in mice. J. Atheroscler. Thromb. 14, 245–252 (2007)CrossRefPubMedGoogle Scholar
  134. 134.
    E. Somm, V.M. Schwitzgebel, A. Toulotte, C.R. Cederroth, C. Combescure, S. Nef, M.L. Aubert, P.S. Hüppi, Perinatal exposure to bisphenol A alters early adipogenesis in the rat. Health Perspect. (2009). doi:10.1289/ehp.11342
  135. 135.
    B.M. Angle, R.P. Do, D. Ponzi, R.W. Stahlhut, B.E. Drury, S.C. Nagel, W.V. Welshons, C.L. Besch-Williford, P. Palanza, S. Parmigiani, F.S. vom Saal, J.A. Taylor, Metabolic disruption in male mice due to fetal exposure to low but not high doses of bisphenol A (BPA): evidence for effects on body weight, food intake, adipocytes, leptin, adiponectin, insulin and glucose regulation. Reprod. Toxicol. (2013). doi:10.1016/j.reprotox.2013.07.0177
  136. 136.
    G. Li, H. Chang, W. Xia, Z. Mao, Y. Li, S. Xu, F0 maternal BPA exposure induced glucose intolerance of F2 generation through DNA methylation change in Gck. Toxicol. Lett. (2014). doi:10.1016/j.toxlet.2014.04.012

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  1. 1.University of Novi Sad, Faculty of Medicine, Clinic for Endocrinology, Diabetes and Metabolic Diseases, Clinical Center of VojvodinaNovi SadSerbia
  2. 2.University of Novi Sad, Faculty of Medicine, Department of PharmacyNovi SadSerbia
  3. 3.University Magna Graecia, Department of Health Sciences, Campus GermanetoCatanzaroItaly

Personalised recommendations