Sex differences in the association of urinary bisphenol-A concentration with selected indices of glucose homeostasis among U.S. adults

Annals of Epidemiology

Volumn 24, Issue 2, 2014, Pages 90-97

  Beydoun, Hind A ^a   Khanal, Suraj ^a   Zonderman, Alan B ^b   Beydoun, May A ^b  

^a EASTERN VIRGINIA MEDICAL SCHOOL   (United States)

^b NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

Bisphenol A; Endocrine disruptor; Glucose homeostasis; Survey

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; CREATININE; GLUCOSE; INSULIN;

ADULT; AGE; ARTICLE; B LYMPHOCYTE; CELL FUNCTION; CREATININE URINE LEVEL; DIETARY INTAKE; EDUCATION; FEMALE; GLUCOSE HOMEOSTASIS; HUMAN; INSULIN RESISTANCE; MAJOR CLINICAL STUDY; MALE; MARRIAGE; MIDDLE AGED; PHYSICAL ACTIVITY; PRIORITY JOURNAL; RACE; SEX DIFFERENCE; SMOKING; UNITED STATES; URINE LEVEL; YOUNG ADULT;

BISPHENOL-A; ENDOCRINE DISRUPTOR; GLUCOSE HOMEOSTASIS; SURVEY;

ADOLESCENT; ADULT; AGED; BENZHYDRYL COMPOUNDS; CREATININE; CROSS-SECTIONAL STUDIES; ENDOCRINE DISRUPTORS; FEMALE; GLUCOSE; HOMEOSTASIS; HUMANS; INSULIN; INSULIN RESISTANCE; LOGISTIC MODELS; MALE; MIDDLE AGED; MULTIVARIATE ANALYSIS; NUTRITION SURVEYS; PHENOLS; PREDICTIVE VALUE OF TESTS; SEX FACTORS; SOCIOECONOMIC FACTORS; UNITED STATES; YOUNG ADULT;

EID: 84892966740     PISSN: 10472797     EISSN: 18732585     Source Type: Journal    
DOI: 10.1016/j.annepidem.2013.07.014     Document Type: Article

References (70)

1. Wang Y., Beydoun M.A. The obesity epidemic in the United States-gender, age, socioeconomic, racial/ethnic, and geographic characteristics: a systematic review and meta-regression analysis. Epidemiol Rev 2007, 29:6-28.
2. Grun F., Blumberg B. Perturbed nuclear receptor signaling by environmental obesogens as emerging factors in the obesity crisis. Rev Endocr Metab Disord 2007, 8(2):161-171.
3. Stubbs C.O., Lee A.J. The obesity epidemic: both energy intake and physical activity contribute. Med J Aust 2004, 181(9):489-491.
4. Newbold R.R., Padilla-Banks E., Jefferson W.N. Environmental estrogens and obesity. Mol Cell Endocrinol 2009, 304(1-2):84-89.
5. Karoutsou E., Polymeris A. Environmental endocrine disruptors and obesity. Endocr Regul 2012, 46(1):37-46.
6. Aubert M.L., Nef S., Soto A.M. Special issue on the topic: role of endocrine disruptors from the environment in the aetiology of obesity and diabetes. Mol Cell Endocrinol 2009, 304(1-2):1-2.
7. Elobeid M.A., Allison D.B. Putative environmental-endocrine disruptors and obesity: a review. Curr Opin Endocrinol Diabetes Obes 2008, 15(5):403-408.
8. Hatch E.E., Nelson J.W., Stahlhut R.W., Webster T.F. Association of endocrine disruptors and obesity: perspectives from epidemiological studies. Int J Androl 2010, 33(2):324-332.
9. Heindel J.J. Endocrine disruptors and the obesity epidemic. Toxicol Sci 2003, 76(2):247-249.
10. Newbold R.R., Padilla-Banks E., Jefferson W.N., Heindel J.J. Effects of endocrine disruptors on obesity. Int J Androl 2008, 31(2):201-208.
11. Lang I.A., Galloway T.S., Scarlett A., Henley W.E., Depledge M., Wallace R.B., et al. Association of urinary bisphenol A concentration with medical disorders and laboratory abnormalities in adults. JAMA 2008, 300(11):1303-1310.
12. Melzer D., Rice N.E., Lewis C., Henley W.E., Galloway T.S. Association of urinary bisphenol a concentration with heart disease: evidence from NHANES 2003/06. PLoS One 2010, 5(1):e8673.
13. Shankar A., Teppala S. Relationship between urinary bisphenol A levels and diabetes mellitus. J Clin Endocrinol Metab 2011, 96(12):3822-3826.
14. Silver M.K., O'Neill M.S., Sowers M.R., Park S.K. Urinary bisphenol A and type-2 diabetes in U.S. adults: data from NHANES 2003-2008. PLoS One 2011, 6(10):e26868.
15. Yang M., Ryu J.H., Jeon R., Kang D., Yoo K.Y. Effects of bisphenol A on breast cancer and its risk factors. Arch Toxicol 2009, 83(3):281-285.
16. Fernandez M., Bourguignon N., Lux-Lantos V., Libertun C. Neonatal exposure to bisphenol a and reproductive and endocrine alterations resembling the polycystic ovarian syndrome in adult rats. Environ Health Perspect 2010, 118(9):1217-1222.
17. Goodman J.E., Witorsch R.J., McConnell E.E., Sipes I.G., Slayton T.M., Yu C.J., et al. Weight-of-evidence evaluation of reproductive and developmental effects of low doses of bisphenol A. Crit Rev Toxicol 2009, 39(1):1-75.
18. LaRocca J., Boyajian A., Brown C., Smith S.D., Hixon M. Effects of in utero exposure to Bisphenol A or diethylstilbestrol on the adult male reproductive system. Birth Defects Res B Dev Reprod Toxicol 2011, 92(6):526-533.
19. Maffini M.V., Rubin B.S., Sonnenschein C., Soto A.M. Endocrine disruptors and reproductive health: the case of bisphenol-A. Mol Cell Endocrinol 2006, 254-255:179-186.
20. Mendiola J., Jorgensen N., Andersson A.M., Calafat A.M., Ye X., Redmon J.B., et al. Are environmental levels of bisphenol a associated with reproductive function in fertile menα. Environ Health Perspect 2010, 118(9):1286-1291.
21. Spivey A. Prenatal preview: early bisphenol a exposure may spawn late-life reproductive problems. Environ Health Perspect 2009, 117(6):A256.
22. Ginsberg G., Rice D.C. Does rapid metabolism ensure negligible risk from bisphenol Aα. Environ Health Perspect 2009, 117(11):1639-1643.
23. Vandenberg L.N., Maffini M.V., Sonnenschein C., Rubin B.S., Soto A.M. Bisphenol-A and the great divide: a review of controversies in the field of endocrine disruption. Endocr Rev 2009, 30(1):75-95.
24. Kang J.H., Kondo F., Katayama Y. Human exposure to bisphenol A. Toxicology 2006, 226(2-3):79-89.
25. Mahalingaiah S., Meeker J.D., Pearson K.R., Calafat A.M., Ye X., Petrozza J., et al. Temporal variability and predictors of urinary bisphenol A concentrations in men and women. Environ Health Perspect 2008, 116(2):173-178.
26. Brede C., Fjeldal P., Skjevrak I., Herikstad H. Increased migration levels of bisphenol A from polycarbonate baby bottles after dishwashing, boiling and brushing. Food Addit Contam 2003, 20(7):684-689.
27. Factor A. Mechanisms of thermal and photodegredations of bisphenol A polycarbonate. Polymer durability, degradation, stabilization, and lifetime prediction 1998, 59-76. Oxford University Press, New York. R.L. Clough, N.C. Billingham, K.T. Gillen (Eds.).
28. Kang J.H., Kito K., Kondo F. Factors influencing the migration of bisphenol A from cans. J Food Prot 2003, 66(8):1444-1447.
29. Padmanabhan V., Siefert K., Ransom S., Johnson T., Pinkerton J., Anderson L., et al. Maternal bisphenol-A levels at delivery: a looming problemα. J Perinatol 2008, 28(4):258-263.
30. Matthews J.B., Twomey K., Zacharewski T.R. In vitro and in vivo interactions of bisphenol A and its metabolite, bisphenol A glucuronide, with estrogen receptors alpha and beta. Chem Res Toxicol 2001, 14(2):149-157.
31. Wetherill Y.B., Akingbemi B.T., Kanno J., McLachlan J.A., Nadal A., Sonnenschein C., et al. In vitro molecular mechanisms of bisphenol A action. Reprod Toxicol 2007, 24(2):178-198.
32. Alonso-Magdalena P., Morimoto S., Ripoll C., Fuentes E., Nadal A. The estrogenic effect of bisphenol A disrupts pancreatic beta-cell function in vivo and induces insulin resistance. Environ Health Perspect 2006, 114(1):106-112.
33. CDC. IRB approval http://www.cdc.gov/nchs/nhanes/irba98.htm.
34. CDC. NHANES 2005-2006 http://www.cdc.gov/nchs/nhanes/nhanes2005-2006/nhanes05_06.htm.
35. CDC. NHANES 2007-2008 http://www.cdc.gov/nchs/nhanes/nhanes2007-2008/nhanes07_08.htm.
36. CDC. BPA 2005-2006 http://www.cdc.gov/nchs/nhanes/nhanes2005-2006/EPH_D.htm.
37. Phthalates 2007-2008 http://www.cdc.gov/nchs/nhanes/nhanes2007-2008/PHTHTE_E.htm.
38. CDC. BPA 2007-2008 http://www.cdc.gov/nchs/nhanes/nhanes2007-2008/EPH_E.htm.
39. Phthalates 2005-2006 Journal [serial on the Internet]. Date. http://www.cdc.gov/nchs/nhanes/nhanes2005-2006/PHTHTE_D.htm.
40. Ye X., Kuklenyik Z., Needham L.L., Calafat A.M. Automated on-line column-switching HPLC-MS/MS method with peak focusing for the determination of nine environmental phenols in urine. Anal Chem 2005, 77(16):5407-5413.
41. CDC. NHANES http://www.cdc.gov/nchs/nhanes.htm.
42. Trasande L., Attina T.M., Blustein J. Association between urinary bisphenol A concentration and obesity prevalence in children and adolescents. JAMA 2012, 308(11):1113-1121.
43. Grundy S.M., Cleeman J.I., Daniels S.R., Donato K.A., Eckel R.H., Franklin B.A., et al. Diagnosis and management of the metabolic syndrome. An American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement. Executive summary. Cardiol Rev 2005, 13(6):322-327.
44. Yang Q., Liu T., Shrader P., Yesupriya A., Chang M.H., Dowling N.F., et al. Racial/ethnic differences in association of fasting glucose-associated genomic loci with fasting glucose, HOMA-B, and impaired fasting glucose in the U.S. adult population. Diabetes Care 2010, 33(11):2370-2377.
45. Katz A., Nambi S.S., Mather K., Baron A.D., Follmann D.A., Sullivan G., et al. Quantitative insulin sensitivity check index: a simple, accurate method for assessing insulin sensitivity in humans. J Clin Endocrinol Metab 2000, 85(7):2402-2410.
46. Wallace T.M., Levy J.C., Matthews D.R. Use and abuse of HOMA modeling. Diabetes Care 2004, 27(6):1487-1495.
47. Matthews D.R., Hosker J.P., Rudenski A.S., Naylor B.A., Treacher D.F., Turner R.C. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 1985, 28(7):412-419.
48. Carwile J.L., Michels K.B. Urinary bisphenol A and obesity: NHANES 2003-2006. Environ Res 2011, 111(6):825-830.
49. Ning G., Bi Y., Wang T., Xu M., Xu Y., Huang Y., et al. Relationship of urinary bisphenol A concentration to risk for prevalent type 2 diabetes in Chinese adults: a cross-sectional analysis. Ann Intern Med 2011, 155(6):368-374.
50. Ropero A.B., Alonso-Magdalena P., Garcia-Garcia E., Ripoll C., Fuentes E., Nadal A. Bisphenol-A disruption of the endocrine pancreas and blood glucose homeostasis. Int J Androl 2008, 31(2):194-200.
51. Shankar A., Teppala S. Urinary bisphenol A and hypertension in a multiethnic sample of US adults. J Environ Public Health 2012, 2012:481641.
52. vom Saal F.S., Myers J.P. Bisphenol A and risk of metabolic disorders. JAMA 2008, 300(11):1353-1355.
53. Wang T., Li M., Chen B., Xu M., Xu Y., Huang Y., et al. Urinary bisphenol A (BPA) concentration associates with obesity and insulin resistance. J Clin Endocrinol Metab 2012, 97(2):E223-E227.
54. Wei M. Association of bisphenol A with diabetes and other abnormalities. JAMA 2009, 301(7):720. author reply 1-2.
55. Hatch E.E., Nelson J.W., Qureshi M.M., Weinberg J., Moore L.L., Singer M., et al. Association of urinary phthalate metabolite concentrations with body mass index and waist circumference: a cross-sectional study of NHANES data, 1999-2002. Environ Health 2008, 7:27.
56. Stahlhut R.W., van Wijngaarden E., Dye T.D., Cook S., Swan S.H. Concentrations of urinary phthalate metabolites are associated with increased waist circumference and insulin resistance in adult U.S. males. Environ Health Perspect 2007, 115(6):876-882.
57. CDC. NHANES Analytical Guidelines http://www.cdc.gov/nchs/nhanes/nhanes2003-2004/analytical_guidelines.htm.
58. Sugiura-Ogasawara M., Ozaki Y., Sonta S., Makino T., Suzumori K. Exposure to bisphenol A is associated with recurrent miscarriage. Hum Reprod 2005, 20(8):2325-2329.
59. Zhou R., Zhang Z., Zhu Y., Chen L., Sokabe M. Deficits in development of synaptic plasticity in rat dorsal striatum following prenatal and neonatal exposure to low-dose bisphenol A. Neuroscience 2009, 159(1):161-171.
60. Crinnion W.J. Toxic effects of the easily avoidable phthalates and parabens. Altern Med Rev 2010, 15(3):190-196.
61. Grun F. Obesogens. Curr Opin Endocrinol Diabetes Obes 2010, 17(5):453-459.
62. Newbold R.R. Impact of environmental endocrine disrupting chemicals on the development of obesity. Hormones (Athens) 2010, 9(3):206-217.
63. Sakurai K., Kawazuma M., Adachi T., Harigaya T., Saito Y., Hashimoto N., et al. Bisphenol A affects glucose transport in mouse 3T3-F442A adipocytes. Br J Pharmacol 2004, 141(2):209-214.
64. Marmugi A., Ducheix S., Lasserre F., Polizzi A., Paris A., Priymenko N., et al. Low doses of bisphenol A induce gene expression related to lipid synthesis and trigger triglyceride accumulation in adult mouse liver. Hepatology 2012, 55(2):395-407.
65. Miyawaki J., Sakayama K., Kato H., Yamamoto H., Masuno H. Perinatal and postnatal exposure to bisphenol a increases adipose tissue mass and serum cholesterol level in mice. J Atheroscler Thromb 2007, 14(5):245-252.
66. Ben-Jonathan N., Hugo E.R., Brandebourg T.D. Effects of bisphenol A on adipokine release from human adipose tissue: implications for the metabolic syndrome. Mol Cell Endocrinol 2009, 304(1-2):49-54.
67. Wei J., Lin Y., Li Y., Ying C., Chen J., Song L., et al. Perinatal exposure to bisphenol A at reference dose predisposes offspring to metabolic syndrome in adult rats on a high-fat diet. Endocrinology 2011, 152(8):3049-3061.
68. Alonso-Magdalena P., Vieira E., Soriano S., Menes L., Burks D., Quesada I., et al. Bisphenol A exposure during pregnancy disrupts glucose homeostasis in mothers and adult male offspring. Environ Health Perspect 2010, 118(9):1243-1250.
69. O'Reilly E.J., Mirzaei F., Forman M.R., Ascherio A. Diethylstilbestrol exposure in utero and depression in women. Am J Epidemiol 2010, 171(8):876-882.
70. Kang E.S., Yun Y.S., Park S.W., Kim H.J., Ahn C.W., Song Y.D., et al. Limitation of the validity of the homeostasis model assessment as an index of insulin resistance in Korea. Metabolism 2005, 54(2):206-211.