Prediction of human prenatal exposure to bisphenol A and bisphenol A glucuronide from an ovine semi-physiological toxicokinetic model

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Gauderat, Glenn ^a,b   Picard Hagen, Nicole ^a   Toutain, Pierre Louis ^a   Servien, Rémi ^a   Viguié, Catherine ^a   Puel, Sylvie ^a   Lacroix, Marlène Z ^a   Corbel, Tanguy ^a   Bousquet Melou, Alain ^a   Gayrard, Véronique ^a  

^a TOXALIM RESEARCH CENTRE IN FOOD TOXICOLOGY   (France)

^b Agreenium's International Research School (EIR A)   (France)

Author keywords

[No Author keywords available]

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; BENZHYDRYL DERIVATIVE; BISPHENOL A GLUCURONIDE; GLUCURONIDE; PHENOL DERIVATIVE;

ANIMAL; BIOLOGICAL MODEL; FEMALE; FETUS; HUMAN; MATERNAL EXPOSURE; METABOLISM; PATHOLOGY; PREGNANCY; PRENATAL EXPOSURE; SHEEP; TOXICOKINETICS;

ANIMALS; BENZHYDRYL COMPOUNDS; FEMALE; FETUS; GLUCURONIDES; HUMANS; MATERNAL EXPOSURE; MODELS, BIOLOGICAL; PHENOLS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; SHEEP; TOXICOKINETICS;

EID: 85033571622     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-15646-5     Document Type: Article

References (50)

1. Calafat, A. M., Ye, X., Wong, L.-Y., Reidy, J. A. & Needham, L. L. Exposure of the U.S. Population to Bisphenol A and 4-tertiary-Octylphenol: 2003-2004. Environ. Health Perspect. 116, 39-44 (2007).
2. Haines, D. A. & Murray, J. Human biomonitoring of environmental chemicals-early results of the 2007-2009 Canadian Health Measures Survey for males and females. Int. J. Hyg. Environ. Health 215, 133-137 (2012).
3. Covaci, A. et al. Urinary BPA measurements in children and mothers from six European member states: Overall results and determinants of exposure. Environ. Res. 141, 77-85 (2015).
4. EFSA Panel on Food Contact Materials, Enzymes, Flavourings and Processing Aids (CEF). Scientific Opinion on the risks to public health related to the presence of bisphenol A (BPA) in foodstuffs: Opinion on BPA. EFSA J. 13, 3978 (2015).
5. Cabaton, N. J. et al. Perinatal exposure to environmentally relevant levels of bisphenol A decreases fertility and fecundity in CD-1 mice. Environ. Health Perspect. 119, 547-552 (2011).
6. Vandenberg, L. N. et al. Perinatal exposure to the xenoestrogen bisphenol-A induces mammary intraductal hyperplasias in adult CD-1 mice. Reprod. Toxicol. Elmsford N 26, 210-219 (2008).
7. Patel, S. et al. Bisphenol A Exposure, Ovarian Follicle Numbers, and Female Sex Steroid Hormone Levels: Results from a CLARITY-BPA Study. Endocrinology https://doi.org/10.1210/en.2016-1887 (2017).
8. Corbel, T. et al. Bisphenol A disposition in the sheep maternal-placental-fetal unit: mechanisms determining fetal internal exposure. Biol. Reprod. 89, 11 (2013).
9. Patterson, T. A. et al. Concurrent determination of bisphenol A pharmacokinetics in maternal and fetal rhesus monkeys. Toxicol. Appl. Pharmacol. 267, 41-48 (2013).
10. Viguié, C. et al. Maternal and fetal exposure to bisphenol a is associated with alterations of thyroid function in pregnant ewes and their newborn lambs. Endocrinology 154, 521-528 (2013).
11. Vom Saal, F. S. et al. Bisphenol A (BPA) pharmacokinetics with daily oral bolus or continuous exposure via silastic capsules in pregnant rhesus monkeys: Relevance for human exposures. Reprod. Toxicol. Elmsford N 45, 105-116 (2014).
12. Gauderat, G. et al. Bisphenol A glucuronide deconjugation is a determining factor of fetal exposure to bisphenol A. 86, 52-59 (2016).
13. Schönfelder, G. et al. Parent bisphenol A accumulation in the human maternal-fetal-placental unit. Environ. Health Perspect. 110, A703-707 (2002).
14. Chou, W.-C. et al. 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 Glob. Access. Sci. Source 10, 94 (2011).
15. Fénichel, P. et al. Unconjugated bisphenol A cord blood levels in boys with descended or undescended testes. Hum. Reprod. Oxf. Engl. 27, 983-990 (2012).
16. Gerona, R. R. 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. 47, 12477-12485 (2013).
17. Zhang, T., Sun, H. & Kannan, K. Blood and urinary bisphenol A concentrations in children, adults, and pregnant women from china: partitioning between blood and urine and maternal and fetal cord blood. Environ. Sci. Technol. 47, 4686-4694 (2013).
18. Dekant, W. & Völkel, W. Human exposure to bisphenol A by biomonitoring: methods, results and assessment of environmental exposures. Toxicol. Appl. Pharmacol. 228, 114-134 (2008).
19. Aarons, L. Physiologically based pharmacokinetic modelling: a sound mechanistic basis is needed. Br. J. Clin. Pharmacol. 60, 581-583 (2005).
20. Maharaj, A. R. & Edginton, A. N. Physiologically Based Pharmacokinetic Modeling and Simulation in Pediatric Drug Development. CPT Pharmacomet. Syst. Pharmacol. 3, 1-13 (2014).
21. Shin, B. S. et al. Physiologically based pharmacokinetics of bisphenol A. J. Toxicol. Environ. Health A 67, 1971-1985 (2004).
22. Teeguarden, J. G., Waechter, J. M., Clewell, H. J., Covington, T. R. & Barton, H. A. Evaluation of oral and intravenous route pharmacokinetics, plasma protein binding, and uterine tissue dose metrics of bisphenol A: a physiologically based pharmacokinetic approach. Toxicol. Sci. Off. J. Soc. Toxicol. 85, 823-838 (2005).
23. Edginton, A. N. & Ritter, L. Predicting plasma concentrations of bisphenol A in children younger than 2 years of age after typical feeding schedules, using a physiologically based toxicokinetic model. Environ. Health Perspect. 117, 645-652 (2009).
24. Fisher, J. W., Twaddle, N. C., Vanlandingham, M. & Doerge, D. R. Pharmacokinetic modeling: prediction and evaluation of route dependent dosimetry of bisphenol A in monkeys with extrapolation to humans. Toxicol. Appl. Pharmacol. 257, 122-136 (2011).
25. Yang, X., Doerge, D. R., Teeguarden, J. G. & Fisher, J. W. Development of a physiologically based pharmacokinetic model for assessment of human exposure to bisphenol A. Toxicol. Appl. Pharmacol. 289, 442-456 (2015).
26. Sarigiannis, D. A. et al. Integrated exposure and risk characterization of bisphenol-A in Europe. Food Chem. Toxicol. Int. J. Publ. Br. Ind. Biol. Res. Assoc. 98, 134-147 (2016).
27. Thayer, K. A. et al. Pharmacokinetics of bisphenol A in humans following a single oral administration. Environ. Int. 83, 107-115 (2015).
28. Taylor, J. A. et al. Similarity of Bisphenol A Pharmacokinetics in Rhesus Monkeys and Mice: Relevance for Human Exposure. Environ. Health Perspect. 119, 422-430 (2010).
29. Pharmacokinetics, Second Edition. (CRC Press, 1982).
30. Collet, S. H. et al. Allometric scaling for predicting human clearance of bisphenol A. Toxicol. Appl. Pharmacol. 284, 323-329 (2015).
31. Barry, J. S. & Anthony, R. V. The pregnant sheep as a model for human pregnancy. Theriogenology 69, 55-67 (2008).
32. Kumar, S. et al. Estimation of transplacental and nonplacental diphenhydramine clearances in the fetal lamb: the impact of fetal first-pass hepatic drug uptake. J. Pharmacol. Exp. Ther. 282, 617-632 (1997).
33. Ngamprasertwong, P. et al. Propofol Pharmacokinetics and Estimation of Fetal Propofol Exposure during Mid-Gestational Fetal Surgery: A Maternal-Fetal Sheep Model. PloS One 11, e0146563 (2016).
34. Völkel, W., Colnot, T., Csanády, G. A., Filser, J. G. & Dekant, W. Metabolism and kinetics of bisphenol a in humans at low doses following oral administration. Chem. Res. Toxicol. 15, 1281-1287 (2002).
35. Corbel, T. et al. Bidirectional placental transfer of Bisphenol A and its main metabolite, Bisphenol A-Glucuronide, in the isolated perfused human placenta. Reprod. Toxicol. Elmsford N 47, 51-58 (2014).
36. Doerge, D. R., Twaddle, N. C., Woodling, K. A. & Fisher, J. W. Pharmacokinetics of bisphenol A in neonatal and adult rhesus monkeys. Toxicol. Appl. Pharmacol. 248, 1-11 (2010).
37. Gayrard, V. et al. High bioavailability of bisphenol A from sublingual exposure. Environ. Health Perspect. 121, 951-956 (2013).
38. Guignard, D. et al. Characterization of the contribution of buccal absorption to internal exposure to bisphenol A through the diet. Food Chem. Toxicol. Int. J. Publ. Br. Ind. Biol. Res. Assoc. 93, 82-88 (2016).
39. Corbel, T. et al. Conjugation and deconjugation reactions within the fetoplacental compartment in a sheep model: a key factor determining bisphenol A fetal exposure. Drug Metab. Dispos. Biol. Fate Chem. 43, 467-476 (2015).
40. Edelstone, D. I., Rudolph, A. M. & Heymann, M. A. Liver and ductus venosus blood flows in fetal lambs in utero. Circ. Res. 42, 426-433 (1978).
41. Divakaran, K., Hines, R. N. & McCarver, D. G. Human hepatic UGT2B15 developmental expression. Toxicol. Sci. Off. J. Soc. Toxicol. 141, 292-299 (2014).
42. Haugen, G., Kiserud, T., Godfrey, K., Crozier, S. & Hanson, M. Portal and umbilical venous blood supply to the liver in the human fetus near term. Ultrasound Obstet. Gynecol. Off. J. Int. Soc. Ultrasound Obstet. Gynecol. 24, 599-605 (2004).
43. Grigsby, P. L. Animal Models to Study Placental Development and Function throughout Normal and Dysfunctional Human Pregnancy. Semin. Reprod. Med. 34, 11-16 (2016).
44. Veiga-Lopez, A. et al. Gender-Specific Effects on Gestational Length and Birth Weight by Early Pregnancy BPA Exposure. J. Clin. Endocrinol. Metab. 100, E1394-1403 (2015).
45. Yamamoto, J. et al. Quantifying bisphenol A in maternal and cord whole blood using isotope dilution liquid chromatography/tandem mass spectrometry and maternal characteristics associated with bisphenol A. Chemosphere 164, 25-31 (2016).
46. Smith, B. P. et al. Confidence interval criteria for assessment of dose proportionality. Pharm. Res. 17, 1278-1283 (2000).
47. Collet, S. H. et al. Estrogenicity of bisphenol a: a concentration-effect relationship on luteinizing hormone secretion in a sensitive model of prepubertal lamb. Toxicol. Sci. Off. J. Soc. Toxicol. 117, 54-62 (2010).
48. Lacroix, M. Z. et al. Simultaneous quantification of bisphenol A and its glucuronide metabolite (BPA-G) in plasma and urine: applicability to toxicokinetic investigations. Talanta 85, 2053-2059 (2011).
49. Beal, S. L. Ways to fit a PK model with some data below the quantification limit. J. Pharmacokinet. Pharmacodyn. 28, 481-504 (2001).
50. Bonate, P. L. Pharmacokinetic-Pharmacodynamic Modeling and Simulation. (Springer US, https://doi.org/10.1007/978-1-4419-9485-1 (2011).