Direct measurement of Bisphenol A (BPA), BPA glucuronide and BPA sulfate in a diverse and low-income population of pregnant women reveals high exposure, with potential implications for previous exposure estimates: A cross-sectional study

Environmental Health: A Global Access Science Source

Volumn 15, Issue 1, 2016, Pages

  Gerona, Roy R ^a   Pan, Janet ^a   Zota, Ami R ^a,b   Schwartz, Jackie M ^a   Friesen, Matthew ^a   Taylor, Julia A ^d   Hunt, Patricia A ^c   Woodruff, Tracey J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b GEORGE WASHINGTON UNIVERSITY   (United States)

^c WASHINGTON STATE UNIVERSITY   (United States)

^d UNIVERSITY OF MISSOURI   (United States)

Author keywords

Bisphenol A; Children's environmental health; Exposure sources; Liquid chromatography tandem mass spectrometry (LC MS MS); Pregnant women

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; BISPHENOL A GLUCURONIDE; BISPHENOL A SULFATE; ENDOCRINE DISRUPTOR; UNCLASSIFIED DRUG; BENZHYDRYL DERIVATIVE; GLUCURONIDE; PHENOL DERIVATIVE; POLLUTANT; SULFATE;

CHILD HEALTH; CONCENTRATION (COMPOSITION); ENVIRONMENTAL HAZARD; LIQUID CHROMATOGRAPHY; LOW INCOME POPULATION; MASS SPECTROMETRY; METABOLITE; ORGANIC POLLUTANT; POLLUTANT SOURCE; POLLUTION EXPOSURE; QUESTIONNAIRE SURVEY; RACE; WOMENS HEALTH;

ADULT; ARTICLE; CONCENTRATION (PARAMETERS); CROSS-SECTIONAL STUDY; ETHNICITY; FEMALE; HUMAN; LIQUID CHROMATOGRAPHY; LOWEST INCOME GROUP; METABOLITE; POPULATION EXPOSURE; PREGNANT WOMAN; PRIORITY JOURNAL; SECOND TRIMESTER PREGNANCY; TANDEM MASS SPECTROMETRY; URINE LEVEL; ADOLESCENT; DIET; ENVIRONMENTAL MONITORING; MATERNAL EXPOSURE; MIDDLE AGED; POLLUTANT; POVERTY; PREGNANCY; QUESTIONNAIRE; URINE; YOUNG ADULT;

ADOLESCENT; ADULT; BENZHYDRYL COMPOUNDS; CROSS-SECTIONAL STUDIES; DIET; ENDOCRINE DISRUPTORS; ENVIRONMENTAL MONITORING; ENVIRONMENTAL POLLUTANTS; FEMALE; GLUCURONIDES; HUMANS; MATERNAL EXPOSURE; MIDDLE AGED; PHENOLS; POVERTY; PREGNANCY; SULFATES; SURVEYS AND QUESTIONNAIRES; YOUNG ADULT;

EID: 84964938401     PISSN: None     EISSN: 1476069X     Source Type: Journal    
DOI: 10.1186/s12940-016-0131-2     Document Type: Article

References (73)

1. Schecter A, Malik N, Haffner D, Smith S, Harris TR, Paepke O, et al. Bisphenol A (BPA) in U.S. food. Environ Sci Technol. 2010;44(24):9425-30. doi: 10.1021/es102785d.
2. Vandenberg LN, Hauser R, Marcus M, Olea N, Welshons WV. Human exposure to bisphenol A (BPA). Reprod Toxicol. 2007;24(2):139-77. doi: 10.1016/j.reprotox.2007.07.010.
3. National Toxicology Program. NTP-CERHR Expert Panel Report on the Reproductive and Developmental Toxicity of Bisphenol A. Durham: Research Triangle Park; 2007.
4. Ozaki A, Yamaguchi Y, Fujita T, Kuroda K, Endo G. Chemical analysis and genotoxicological safety assessment of paper and paperboard used for food packaging. Food Chem Toxicol. 2004;42(8):1323-37. doi: 10.1016/j.fct.2004.03.010.
5. Pivnenko K, Pedersen GA, Eriksson E, Astrup TF. Bisphenol A and its structural analogues in household waste paper. Waste Manag. 2015;44:39-47. doi: 10.1016/j.wasman.2015.07.017.
6. Babu S, Uppu SN, Martin B, Agu OA, Uppu RM. Unusually high levels of bisphenol A (BPA) in thermal paper cash register receipts (CRs): development and application of a robust LC-UV method to quantify BPA in CRs. Toxicol Mech Methods. 2015;25(5):410-6. doi: 10.3109/15376516.2015.1045661.
7. Geens T, Goeyens L, Kannan K, Neels H, Covaci A. Levels of bisphenol-A in thermal paper receipts from Belgium and estimation of human exposure. Sci Total Environ. 2012;435-436:30-3. doi: 10.1016/j.scitotenv.2012.07.001.
8. Liao C, Kannan K. Widespread occurrence of bisphenol A in paper and paper products: implications for human exposure. Environ Sci Technol. 2011;45(21):9372-9. doi: 10.1021/es202507f.
9. Liao C, Kannan K. High levels of bisphenol A in paper currencies from several countries, and implications for dermal exposure. Environ Sci Technol. 2011;45(16):6761-8. doi: 10.1021/es200977t.
10. Suciu NA, Tiberto F, Vasileiadis S, Lamastra L, Trevisan M. Recycled paper-paperboard for food contact materials: contaminants suspected and migration into foods and food simulant. Food Chem. 2013;141(4):4146-51. doi: 10.1016/j.foodchem.2013.07.014.
11. Hunt PA, Koehler KE, Susiarjo M, Hodges CA, Ilagan A, Voigt RC, et al. Bisphenol a exposure causes meiotic aneuploidy in the female mouse. Curr Biol. 2003;13(7):546-53.
12. Vom Saal FS, Hughes C. An extensive new literature concerning low-dose effects of bisphenol A shows the need for a new risk assessment. Environ Health Perspect. 2005;113(8):926.
13. Cabaton NJ, Wadia PR, Rubin BS, Zalko D, Schaeberle CM, Askenase MH, et al. Perinatal exposure to environmentally relevant levels of bisphenol A decreases fertility and fecundity in CD-1 mice. Environ Health Perspect. 2011;119(4):547-52. doi: 10.1289/ehp.1002559.
14. Kabuto H, Amakawa M, Shishibori T. Exposure to bisphenol A during embryonic/fetal life and infancy increases oxidative injury and causes underdevelopment of the brain and testis in mice. Life Sci. 2004;74(24):2931-40. doi: 10.1016/j.lfs.2003.07.060.
15. Midoro-Horiuti T, Tiwari R, Watson CS, Goldblum RM. Maternal bisphenol a exposure promotes the development of experimental asthma in mouse pups. Environ Health Perspect. 2010;118(2):273-7. doi: 10.1289/ehp.0901259.
16. Bindhumol V, Chitra KC, Mathur PP. Bisphenol A induces reactive oxygen species generation in the liver of male rats. Toxicology. 2003;188(2-3):117-24. doi:S0300483X03000568 [pii].
17. Li DK, Zhou Z, Miao M, He Y, Wang J, Ferber J, et al. Urine bisphenol-A (BPA) level in relation to semen quality. Fertil Steril. 2011;95(2):625-30. doi: 10.1016/j.fertnstert.2010.09.026. e1-4.
18. Meeker JD, Ehrlich S, Toth TL, Wright DL, Calafat AM, Trisini AT, et al. Semen quality and sperm DNA damage in relation to urinary bisphenol A among men from an infertility clinic. Reprod Toxicol. 2010;30(4):532-9. doi: 10.1016/j.reprotox.2010.07.005.
19. Bloom MS, Vom Saal FS, Kim D, Taylor JA, Lamb JD, Fujimoto VY. Serum unconjugated bisphenol A concentrations in men may influence embryo quality indicators during in vitro fertilization. Environ Toxicol Pharmacol. 2011;32(2):319-23. doi: 10.1016/j.etap.2011.06.003.
20. Fujimoto VY, Kim D, Vom Saal FS, Lamb JD, Taylor JA, Bloom MS. Serum unconjugated bisphenol A concentrations in women may adversely influence oocyte quality during in vitro fertilization. Fertil Steril. 2011;95(5):1816-9. doi: 10.1016/j.fertnstert.2010.11.008.
21. U.S. Department of Commerce. Current Population Survey (CPS) - Definitions. Ann Arbor: Bureau of the Census; 2010. https://www.census.gov/programs-surveys/cps.html. Accessed September 2013.
22. Woodruff TJ, Zota AR, Schwartz JM. Environmental chemicals in pregnant women in the US: NHANES 2003-2004. Environ Health Perspect. 2011;119(6):878-85.
23. Calafat AM, Ye XY, Wong LY, Reidy JA, Needham LL. Exposure of the US population to bisphenol A and 4-tertiary-octylphenol: 2003-2004. Environ Health Perspect. 2008;116(1):39-44. doi: 10.1289/ehp.10753.
24. Nelson JW, Scammell MK, Hatch EE, Webster TF. Social disparities in exposures to bisphenol A and polyfluoroalkyl chemicals: a cross-sectional study within NHANES 2003-2006. Environ Health. 2012;11:10. doi: 10.1186/1476-069X-11-10.
25. Quiros-Alcala L, Eskenazi B, Bradman A, Ye X, Calafat AM, Harley K. Determinants of urinary bisphenol A concentrations in Mexican/Mexican - American pregnant women. Environ Int. 2013;59:152-60. doi: 10.1016/j.envint.2013.05.016.
26. Noonan GO, Ackerman LK, Begley TH. Concentration of bisphenol A in highly consumed canned foods on the U.S. market. J Agric Food Chem. 2011;59(13):7178-85. doi: 10.1021/jf201076f.
27. Braun JM, Kalkbrenner AE, Calafat AM, Bernert JT, Ye X, Silva MJ, et al. Variability and predictors of urinary bisphenol A concentrations during pregnancy. Environ Health Perspect. 2011;119(1):131-7. doi: 10.1289/ehp.1002366.
28. Hehn RS. NHANES data support link between handling of thermal paper receipts and increased urinary bisphenol a excretion. Environ Sci Technol. 2016;50(1):397-404. doi: 10.1021/acs.est.5b04059.
29. Thayer KA, Taylor KW, Garantziotis S, Schurman S, Kissling GE, Hunt D, et al. Bisphenol A, Bisphenol S, and 4-Hydroxyphenyl 4-Isoprooxyphenylsulfone (BPSIP) in Urine and Blood of Cashiers. Environ Health Perspect. 2015. doi: 10.1289/ehp.1409427.
30. Lakind JS, Naiman DQ. Daily intake of bisphenol A and potential sources of exposure: 2005-2006 National Health and Nutrition Examination Survey. J Expo Sci Environ Epidemiol. 2011;21(3):272-9. doi: 10.1038/jes.2010.9.
31. Rudel RA, Gray JM, Engel CL, Rawsthorne TW, Dodson RE, Ackerman JM, et al. Food packaging and bisphenol A and bis (2-ethyhexyl) phthalate exposure: findings from a dietary intervention. Environ Health Perspect. 2011;119(7):914-20.
32. Carwile JL, Luu HT, Bassett LS, Driscoll DA, Yuan C, Chang JY, et al. Polycarbonate bottle use and urinary bisphenol A concentrations. Environ Health Perspect. 2009;117(9):1368-72. doi: 10.1289/ehp.0900604.
33. Carwile JL, Ye X, Zhou X, Calafat AM, Michels KB. Canned soup consumption and urinary bisphenol A: a randomized crossover trial. JAMA. 2011;306(20):2218-20. doi: 10.1001/jama.2011.1721.
34. Ehrlich S, Calafat AM, Humblet O, Smith T, Hauser R. Handling of thermal receipts as a source of exposure to bisphenol A. JAMA. 2014;311(8):859-60. doi: 10.1001/jama.2013.283735.
35. Vandenberg LN, Maffini MV, Sonnenschein C, Rubin BS, Soto AM. Bisphenol-A and the great divide: a review of controversies in the field of endocrine disruption. Endocr Rev. 2009;30(1):75-95. doi: 10.1210/er.2008-0021.
36. Doerge DR, Twaddle NC, Vanlandingham M, Brown RP, Fisher JW. Distribution of bisphenol A into tissues of adult, neonatal, and fetal Sprague-Dawley rats. Toxicol Appl Pharmacol. 2011;255(3):261-70. doi: 10.1016/j.taap.2011.07.009.
37. Ginsberg G, Rice DC. Does rapid metabolism ensure negligible risk from bisphenol A? Environ Health Perspect. 2009;117(11):1639.
38. Stowell CL, Barvian KK, Young PC, Bigsby RM, Verdugo DE, Bertozzi CR, et al. A role for sulfation-desulfation in the uptake of bisphenol a into breast tumor cells. Chem Biol. 2006;13(8):891-7. doi: 10.1016/j.chembiol.2006.06.016.
39. Boucher JG, Boudreau A, Ahmed S, Atlas E. In Vitro Effects of Bisphenol A beta-D-Glucuronide (BPA-G) on Adipogenesis in Human and Murine Preadipocytes. Environ Health Perspect. 2015;123(12):1287-93. doi: 10.1289/ehp.1409143.
40. Brenn-Struckhofova Z, Cichna-Markl M. Determination of bisphenol A in wine by sol-gel immunoaffinity chromatography, HPLC and fluorescence detection. Food Addit Contam. 2006;23(11):1227-35. doi: 10.1080/02652030600654382.
41. Gerona RR, Woodruff TJ, Dickenson CA, Pan J, Schwartz JM, Sen S, et al. Bisphenol-A (BPA), BPA glucuronide, and BPA sulfate in midgestation umbilical cord serum in a Northern and Central California population. Environ Sci Technol. 2013;47(21):12477-85. doi: 10.1021/es402764d.
42. Vandenberg LN, Gerona RR, Kannan K, Taylor JA, van Breemen RB, Dickenson CA, et al. A round robin approach to the analysis of bisphenol a (BPA) in human blood samples. Environ Health. 2014;13(1):25. doi: 10.1186/1476-069X-13-25.
43. Cantonwine D, Meeker JD, Hu H, Sanchez BN, Lamadrid-Figueroa H, Mercado-Garcia A, et al. Bisphenol a exposure in Mexico City and risk of prematurity: a pilot nested case control study. Environ Health. 2010;9:62. doi: 10.1186/1476-069X-9-62.
44. Philippat C, Mortamais M, Chevrier C, Petit C, Calafat AM, Ye X, et al. Exposure to phthalates and phenols during pregnancy and offspring size at birth. Environ Health Perspect. 2012;120(3):464-70. doi: 10.1289/ehp.1103634.
45. Liao C, Kannan K. Determination of free and conjugated forms of bisphenol A in human urine and serum by liquid chromatography-tandem mass spectrometry. Environ Sci Technol. 2012;46(9):5003-9. doi: 10.1021/es300115a.
46. European Food Safety Authority. Opinion of the Scientific Panel on Food Additives, Flavourings, Processing Aids and Materials in Contact with Food on a request from the Commission related to 2,2-BIS(4-HYDROXYPHENYL)PROPANE (Bisphenol A): Question No EFSA-Q-2005-100. EFSA J. 2006;428:1-75.
47. U.S. Food and Drug Administration (FDA). Bisphenol A (BPA): Use in Food Contact Application. Silver Spring: U.S. Food and Drug Administration (FDA); 2013. http://www.fda.gov/NewsEvents/PublicHealthFocus/ucm064437.htm. Accessed 1 December 2013.
48. Nahar MS, Liao C, Kannan K, Dolinoy DC. Fetal liver bisphenol A concentrations and biotransformation gene expression reveal variable exposure and altered capacity for metabolism in humans. J Biochem Mol Toxicol. 2013;27(2):116-23. doi: 10.1002/jbt.21459.
49. Levy G, Khanna NN, Soda DM, Tsuzuki O, Stern L. Pharmacokinetics of acetaminophen in the human neonate: formation of acetaminophen glucuronide and sulfate in relation to plasma bilirubin concentration and D-glucaric acid excretion. Pediatrics. 1975;55(6):818-25.
50. Miller RP, Roberts RJ, Fischer LJ. Acetaminophen elimination kinetics in neonates, children, and adults. Clin Pharmacol Ther. 1976;19(3):284-94.
51. Court MH, Hao Q, Krishnaswamy S, Bekaii-Saab T, Al-Rohaimi A, von Moltke LL, et al. UDP-glucuronosyltransferase (UGT) 2B15 pharmacogenetics: UGT2B15 D85Y genotype and gender are major determinants of oxazepam glucuronidation by human liver. J Pharmacol Exp Ther. 2004;310(2):656-65. doi:jpet.104.067660 [pii].
52. Menard V, Girard H, Harvey M, Perusse L, Guillemette C. Analysis of inherited genetic variations at the UGT1 locus in the French-Canadian population. Hum Mutat. 2009;30(4):677-87. doi: 10.1002/humu.20946.
53. Hanioka N, Oka H, Nagaoka K, Ikushiro S, Narimatsu S. Effect of UDP-glucuronosyltransferase 2B15 polymorphism on bisphenol A glucuronidation. Arch Toxicol. 2011;85(11):1373-81. doi: 10.1007/s00204-011-0690-5.
54. Nagar S, Walther S, Blanchard RL. Sulfotransferase (SULT) 1A1 polymorphic variants∗1,∗2, and∗3 are associated with altered enzymatic activity, cellular phenotype, and protein degradation. Mol Pharmacol. 2006;69(6):2084-92. doi: 10.1124/mol.105.019240.
55. Hormann AM, Vom Saal FS, Nagel SC, Stahlhut RW, Moyer CL, Ellersieck MR, et al. Holding thermal receipt paper and eating food after using hand sanitizer results in high serum bioactive and urine total levels of bisphenol A (BPA). PLoS ONE. 2014;9(10):e1105-9. doi: 10.1371/journal.pone.0110509.
56. Biedermann S, Tschudin P, Grob K. Transfer of bisphenol A from thermal printer paper to the skin. Anal Bioanal Chem. 2010;398(1):571-6. doi: 10.1007/s00216-010-3936-9.
57. Lu SY, Chang WJ, Sojinu SO, Ni HG. Bisphenol A in supermarket receipts and its exposure to human in Shenzhen. China Chemosphere. 2013;92(9):1190-4. doi: 10.1016/j.chemosphere.2013.01.096.
58. Mendum T, Stoler E, VanBenschoten H, Warner JC. Concentration of bisphenol A in thermal paper. Green Chem Lett Rev. 2011;4(1):81-6. doi: 10.1080/17518253.2010.502908.
59. Sathyanarayana S, Alcedo G, Saelens BE, Zhou C, Dills RL, Yu J, et al. Unexpected results in a randomized dietary trial to reduce phthalate and bisphenol A exposures. Journal of exposure science & environmental epidemiology. 2013;23(4):378-84. doi: 10.1038/jes.2013.9.
60. Lakind JS, Naiman DQ. Bisphenol A (BPA) daily intakes in the United States: Estimates from the 2003-2004 NHANES urinary BPA data. Journal of exposure science & environmental epidemiology. 2008. doi: 10.1038/jes.2008.20.
61. He Y, Miao M, Herrinton LJ, Wu C, Yuan W, Zhou Z, et al. Bisphenol A levels in blood and urine in a Chinese population and the personal factors affecting the levels. Environ Res. 2009;109(5):629-33. doi: 10.1016/j.envres.2009.04.003.
62. Braun JM, Smith KW, Williams PL, Calafat AM, Berry K, Ehrlich S, et al. Variability of urinary phthalate metabolite and bisphenol A concentrations before and during pregnancy. Environ Health Perspect. 2012;120(5):739-45. doi: 10.1289/ehp.1104139.
63. Braun JM, Kalkbrenner AE, Calafat AM, Yolton K, Ye X, Dietrich KN, et al. Impact of early-life bisphenol A exposure on behavior and executive function in children. Pediatrics. 2011;128(5):873-82. doi:peds.2011-1335 [pii].
64. Perera F, Vishnevetsky J, Herbstman JB, Calafat AM, Xiong W, Rauh V, et al. Prenatal bisphenol a exposure and child behavior in an inner-city cohort. Environ Health Perspect. 2012;120(8):1190-4. doi: 10.1289/ehp.1104492.
65. Wolff MS, Engel SM, Berkowitz GS, Ye X, Silva MJ, Zhu C, et al. Prenatal phenol and phthalate exposures and birth outcomes. Environ Health Perspect. 2008;116(8):1092-7. doi: 10.1289/ehp.11007.
66. Arbuckle TE, Marro L, Davis K, Fisher M, Ayotte P, Belanger P, et al. Exposure to free and conjugated forms of bisphenol A and triclosan among pregnant women in the MIREC cohort. Environ Health Perspect. 2015;123(4):277-84. doi: 10.1289/ehp.1408187.
67. Martina CA, Weiss B, Swan SH. Lifestyle behaviors associated with exposures to endocrine disruptors. Neurotoxicology. 2012;33(6):1427-33. doi: 10.1016/j.neuro.2012.05.016.
68. Meeker JD, Cantonwine DE, Rivera-Gonzalez LO, Ferguson KK, Mukherjee B, Calafat AM, et al. Distribution, variability, and predictors of urinary concentrations of phenols and parabens among pregnant women in Puerto Rico. Environ Sci Technol. 2013;47(7):3439-47. doi: 10.1021/es400510g.
69. Casas M, Valvi D, Luque N, Ballesteros-Gomez A, Carsin AE, Fernandez MF, et al. Dietary and sociodemographic determinants of bisphenol A urine concentrations in pregnant women and children. Environ Int. 2013;56:10-8. doi: 10.1016/j.envint.2013.02.014.
70. Ye X, Pierik FH, Hauser R, Duty S, Angerer J, Park MM, et al. Urinary metabolite concentrations of organophosphorous pesticides, bisphenol A, and phthalates among pregnant women in Rotterdam, the Netherlands: The Generation R study. Environ Res. 2008.
71. Callan AC, Hinwood AL, Heffernan A, Eaglesham G, Mueller J, Odland JO. Urinary bisphenol A concentrations in pregnant women. Int J Hyg Environ Health. 2013;216(6):641-4. doi: 10.1016/j.ijheh.2012.10.002.
72. Lee BE, Park H, Hong YC, Ha M, Kim Y, Chang N, et al. Prenatal bisphenol A and birth outcomes: MOCEH (Mothers and Children's Environmental Health) study. Int J Hyg Environ Health. 2013. doi: 10.1016/j.ijheh.2013.07.005.
73. Chen MJ, Tang R, Ding GD, Chen XJ, Han XM, Zhou K, et al. Associations of prenatal exposure to phenols with birth outcomes. Environ Pollut. 2013;178:115-20. doi: 10.1016/j.envpol.2013.03.023.