Prenatal exposure to bisphenol A and phthalates and infant neurobehavior

Neurotoxicology and Teratology

Volumn 33, Issue 5, 2011, Pages 558-566

  Yolton, Kimberly ^a   Xu, Yingying ^a   Strauss, Donna ^a   Altaye, Mekibib ^a   Calafat, Antonia M ^b   Khoury, Jane ^a  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^b CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

Author keywords

Bisphenol A; Infant neurobehavior; Phthalates; Prenatal exposure

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; PHTHALIC ACID BIS(2 ETHYLHEXYL) ESTER; PHTHALIC ACID DIBUTYL ESTER;

ADULT; AROUSAL; ARTICLE; AUTOREGULATION; CHILD BEHAVIOR; CONTROLLED STUDY; FEMALE; HUMAN; INFANT; MALE; MOTIVATION; MUSCLE HYPOTONIA; NEUROLOGIC EXAMINATION; NEUROMODULATION; NEUROTOXICITY; PRENATAL EXPOSURE; PRIORITY JOURNAL; PSYCHOLOGICAL RATING SCALE; REFLEX; SELF CONTROL;

ADULT; DIBUTYL PHTHALATE; DIETHYLHEXYL PHTHALATE; ENVIRONMENTAL POLLUTANTS; FEMALE; HUMANS; INFANT; MALE; NEUROPSYCHOLOGICAL TESTS; NEUROTOXICITY SYNDROMES; PHENOLS; PHTHALIC ACIDS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; TIME FACTORS;

EID: 80053213006     PISSN: 08920362     EISSN: 18729738     Source Type: Journal    
DOI: 10.1016/j.ntt.2011.08.003     Document Type: Article

References (83)

1. Adewale H., Todd K., Mickens J., Patisaul H. The impact of neonatal bisphenol-A exposure on sexually dimorphic hypothalamic nuclei in the female rat. Neurotoxicology 2010.
2. Adibi J., Hauser R., Williams P., Whyatt R., Calafat A., Nelson H., Herrick R., Swan S. Maternal urinary metabolites of di-(2-ethylhexyl) phthalate in relation to the timing of labor in a US multicenter pregnancy cohort study. Am J Epidemiol 2009, 8:1015.
3. Akingbemi B., Sottas C., Koulova A., Klinefelter G., Hardy M. Inhibition of testicular steroidogenesis by the xenoestrogen bisphenol A is associated with reduced pituitary luteinizing hormone secretion and decreased steroidogenic enzyme gene expression in rat Leydig cells. Endocrinology 2004, 2:592.
4. Andrade A., Grande S., Talsness C., Gericke C., Grote K., Golombiewski A., Sterner-Kock A., Chahoud I. A dose response study following in utero and lactational exposure to di-(2-ethylhexyl) phthalate (DEHP): reproductive effects on adult male offspring rats. Toxicology 2006, 1:85-97.
5. Barr D., Wilder L., Caudill S., Gonzalez A., Needham L., Pirkle J. Urinary creatinine concentrations in the US population: implications for urinary biologic monitoring measurements. Environ Health Perspect 2005, 2:192.
6. Bearer C.F. The special and unique vulnerability of children to environmental hazards. Neurotoxicology 2000, 6:925-934.
7. Beck A., Steer R., Brown G. Manual for the Beck depression inventory-II 1996, 1-82. Psychological Corporation, San Antonio, TX.
8. Berman T., Hochner-Celnikier D., Calafat A., Needham L., Amitai Y., Wormser U., Richter E. Phthalate exposure among pregnant women in Jerusalem, Israel: results of a pilot study. Environ Int 2009, 2:353-357.
9. Biedermann S., Tschudin P., Grob K. Transfer of bisphenol A from thermal printer paper to the skin. Anal Bioanal Chem 2010, 1-6.
10. Braun J., Yolton K., Dietrich K., Hornung R., Ye X., Calafat A., Lanphear B. Prenatal bisphenol A exposure and early childhood behavior 2009.
11. Braun J., Kalkbrenner A., Calafat A., Bernert J., Ye X., Silva M., Barr D., Sathyanarayana S., Lanphear B. Variability and predictors of urinary bisphenol A concentrations during pregnancy. Environ health perspect 2010.
12. Brazelton T and Nugent J Neonatal behavioral assessment scale. 3rd edition. London: MacKeith Press; 1995.
13. Calafat A., Ye X., Wong L., Reidy J., Needham L. Exposure of the US population to bisphenol A and 4-tertiary-octylphenol: 2003-2004. Environ Health Perspect 2008, 1:39.
14. Cantonwine D., Meeker J.D., Hu H., Sánchez B.N., Lamadrid-Figueroa H., Mercado-García A., Fortenberry G.Z., Calafat A.M., Téllez-Rojo M.M. Bisphenol a exposure in Mexico City and risk of prematurity: a pilot nested case control study. Environ Health 2010, 1:62.
15. Centers for Disease Control and Prevention Fourth National Report on Human Exposure to Environmental Chemicals. Atlanta, GA: Department of health and Human Services, Centers for Disease Control and Prevention, Division of Laboratory Sciences; 2009. NCEH Publication No. 05-0570.
16. Cho S.C., Bhang S.Y., Hong Y.C., Shin M.S., Kim B.N., Kim J.W., Yoo H.J., Cho I.H., Kim H.W. Relationship between environmental phthalate exposure and the intelligence of school-aged children. Environ health perspect 2010.
17. Dalsenter P., Santana G., Grande S., Andrade A., Araujo S. Phthalate affect the reproductive function and sexual behavior of male Wistar rats. Hum Exp Toxicol 2006, 6:297.
18. de Moraes Barros M.C., Guinsburg R., de Araújo Peres C., Mitsuhiro S., Chalem E., Laranjeira R.R. Exposure to marijuana during pregnancy alters neurobehavior in the early neonatal period. J Pediatr 2006, 6:781-787.
19. Engel S.M., Zhu C., Berkowitz G.S., Calafat A.M., Silva M.J., Miodovnik A., Wolff M.S. Prenatal phthalate exposure and performance on the Neonatal Behavioral Assessment Scale in a multiethnic birth cohort. Neurotoxicology 2009, 4:522-528.
20. Engel S.M., Miodovnik A., Canfield R.L., Zhu C., Silva M.J., Calafat A.M., Wolff M.S. Prenatal phthalate exposure is associated with childhood behavior and executive functioning. Environ Health Perspect 2010, 4:565-571.
21. Geraghty S.R., Khoury J.C., Morrow A.L., Lanphear B.P. Reporting individual test results of environmental chemicals in breastmilk: potential for premature weaning. Breastfeed Med 2008, 4:207-213.
22. Gray L., Ostby J., Furr J., Price M., Veeramachaneni D., Parks L. Perinatal exposure to the phthalates DEHP, BBP, and DINP, but not DEP, DMP, or DOTP, alters sexual differentiation of the male rat. Toxicol Sci 2000, 2:350.
23. Hauser R., Meeker J., Duty S., Silva M., Calafat A. Altered semen quality in relation to urinary concentrations of phthalate monoester and oxidative metabolites. Epidemiology 2006, 6:682.
24. Hauser R., Meeker J., Singh N., Silva M., Ryan L., Duty S., Calafat A. DNA damage in human sperm is related to urinary levels of phthalate monoester and oxidative metabolites. Hum Reprod 2007, 3:688-695.
25. Hornung R. Statistical evaluation of exposure assessment strategies. Appl Occup Environ Hyg 1991, 516-520.
26. Hoshi H., Ohtsuka T. Adult rats exposed to low-doses of di-n-butyl phthalate during gestation exhibit decreased grooming behavior. Bull Environ Contam Toxicol 2009, 1:62-66.
27. Irvin E., Calafat A., Silva M., Aguilar-Villalobos M., Needham L., Hall D., Cassidy B., Naeher L. An estimate of phthalate exposure among pregnant women living in Trujillo, Peru. Chemosphere 2010.
28. Ishido M., Masuo Y., Sayato-Suzuki J., Oka S., Niki E., Morita M. Dicyclohexylphthalate causes hyperactivity in the rat concomitantly with impairment of tyrosine hydroxylase immunoreactivity. J Neurochem 2004, 1:69-76.
29. John E., Savitz D., Shy C. Spontaneous abortions among cosmetologists. Epidemiology 1994, 2:147.
30. Just A., Adibi J., Rundle A., Calafat A., Camann D., Hauser R., Silva M., Whyatt R. Urinary and air phthalate concentrations and self-reported use of personal care products among minority pregnant women in New York city. J Expo Sci Environ Epidemiol 2010.
31. Kim B., Cho S., Kim Y., Shin M., Yoo H., Kim J., Yang Y., Kim H., Bhang S., Hong Y. Phthalates exposure and attention-deficit/hyperactivity disorder in school-age children. Biol Psychiatry 2009, 10:958-963.
32. LaGasse L.L., Wouldes T., Newman E., Smith L.M., Shah R.Z., Derauf C., Huestis M.A., Arria A.M., Grotta S.D., Wilcox T. Prenatal methamphetamine exposure and neonatal neurobehavioral outcome in the USA and New Zealand. Neurotoxicol teratol 2010.
33. Lanphear B.P., Hornung R., Khoury J., Yolton K., Baghurst P., Bellinger D.C., Canfield R.L., Dietrich K.N., Bornschein R., Greene T. Low-level environmental lead exposure and children's intellectual function: an international pooled analysis. Environ Health Perspect 2005, 7:894.
34. Law K.L., Stroud L.R., LaGasse L.L., Niaura R., Liu J., Lester B.M. Smoking during pregnancy and newborn neurobehavior. Pediatrics 2003, 6:1318.
35. Lee H., Chattopadhyay S., Gong E., Ahn R., Lee K. Antiandrogenic effects of bisphenol A and nonylphenol on the function of androgen receptor. Toxicol Sci 2003, 1:40.
36. Lee H., Yamanouchi K., Nishihara M. Effects of perinatal exposure to phthalate/adipate esters on hypothalamic gene expression and sexual behavior in rats. J Reprod Dev 2006, 602200033.
37. Lester B.M., Tronick E.Z., LaGasse L., Seifer R., Bauer C.R., Shankaran S., Bada H.S., Wright L.L., Smeriglio V.L., Lu J. The maternal lifestyle study: effects of substance exposure during pregnancy on neurodevelopmental outcome in 1-month-old infants. Pediatrics 2002, 6:1182.
38. Lester B., Tronick E., LaGasse L., Seifer R., Bauer C., Shankaran S., Bada H., Wright L., Smeriglio V., Lu J. Summary statistics of neonatal intensive care unit network neurobehavioral scale scores from the maternal lifestyle study: a quasinormative sample. Pediatrics 2004, 3:668.
39. Lester B., Tronick E. Using the NNNS TM. NICU Network Neurobehavioral Scale (NNNS) manual 2004, 13.
40. Li Y., Zhuang M., Li T., Shi N. Neurobehavioral toxicity study of dibutyl phthalate on rats following in utero and lactational exposure. J Appl Toxicol 2009, 7:603-611.
41. Li D., Zhou Z., Qing D., He Y., Wu T., Miao M., Wang J., Weng X., Ferber J., Herrinton L. Occupational exposure to bisphenol-A (BPA) and the risk of Self-Reported Male Sexual Dysfunction. Hum Reprod 2010, 2:519.
42. Lottrup G., Andersson A.M., Leffers H., Mortensen G.K., Toppari J., Skakkebaek N.E., Main K.M. Possible impact of phthalates on infant reproductive health. Int J Androl 2006, 1:172-180. discussion 181-5.
43. Ma M., Kondo T., Ban S., Umemura T., Kurahashi N., Takeda M., Kishi R. Exposure of prepubertal female rats to inhaled di(2-ethylhexyl)phthalate affects the onset of puberty and postpubertal reproductive functions. Toxicol Sci 2006, 1:164-171.
44. Mahalingaiah S., Meeker J., Pearson K., Calafat A., Ye X., Petrozza J., Hauser R. Temporal variability and predictors of urinary bisphenol A concentrations in men and women. Environ Health Perspect 2008, 2:173.
45. McKee R., Pavkov K., Trimmer G., Keller L., Stump D. An assessment of the potential developmental and reproductive toxicity of di-isoheptyl phthalate in rodents. Reprod Toxicol 2006, 3:241-252.
46. Meeker J., Calafat A., Hauser R. Di (2-ethylhexyl) phthalate metabolites may alter thyroid hormone levels in men. Environ Health Perspect 2007, 7:1029.
47. Meeker J., Calafat A., Hauser R. Urinary metabolites of di (2-ethylhexyl) phthalate are associated with decreased steroid hormone levels in adult men. J Androl 2009, 3:287.
48. Meeker J., Hu H., Cantonwine D., Lamadrid-Figueroa H., Calafat A., Ettinger A., Hernandez-Avila M., Loch-Caruso R., Téllez-Rojo M. Urinary phthalate metabolites in relation to preterm birth in Mexico City. Environ Health Perspect 2009, 10:1587.
49. Meeker J., Ehrlich S., Toth T., Wright D., Calafat A., Trisini A., Ye X., Hauser R. Semen quality and sperm DNA damage in relation to urinary bisphenol A among men from an infertility clinic. Reprod Toxicol 2010.
50. Mendiola J., Jørgensen N., Andersson A., Calafat A., Ye X., Redmon J., Drobnis E., Wang C., Sparks A., Thurston S. are environmental levels of bisphenol A associated with reproductive function in fertile men?. Environ Health Perspect 2010, 9:1286.
51. Miodovnik A., Engel S.M., Zhu C., Ye X., Soorya L.V., Silva M.J., Calafat A.M., Wolff M.S. Endocrine disruptors and childhood social impairment. Neurotoxicology 2010.
52. Mok Lin E., Ehrlich S., Williams P., Petrozza J., Wright D., Calafat A., Ye X., Hauser R. Urinary bisphenol A concentrations and ovarian response among women undergoing IVF. Int J Androl 2010, 2:385-393.
53. Moore R., Rudy T., Lin T., Ko K., Peterson R. Abnormalities of sexual development in male rats with in utero and lactational exposure to the antiandrogenic plasticizer Di (2-ethylhexyl) phthalate. Environ Health Perspect 2001, 3:229.
54. Noriega N., Howdeshell K., Furr J., Lambright C., Wilson V., Gray L. Pubertal administration of DEHP delays puberty, suppresses testosterone production and inhibits reproductive tract development in male Sprague-Dawley and Long-Evans Rats. Toxicol Sci 2009.
55. Palanza P., Howdeshell K., Parmigiani S., Vom Saal F. Exposure to a low dose of bisphenol A during fetal life or in adulthood alters maternal behavior in mice. Environ Health Perspect 2002, 3(Suppl.):415.
56. Palanza P., Gioiosa L., vom Saal F., Parmigiani S. Effects of developmental exposure to bisphenol A on brain and behavior in mice. Environ Res 2008, 2:150-157.
57. Pant N., Shukla M., Kumar Patel D., Shukla Y., Mathur N., Kumar Gupta Y., Saxena D. Correlation of phthalate exposures with semen quality. Toxicol Appl Pharmacol 2008, 1:112-116.
58. Parks L., Ostby J., Lambright C., Abbott B., Klinefelter G., Barlow N., Gray L. The plasticizer diethylhexyl phthalate induces malformations by decreasing fetal testosterone synthesis during sexual differentiation in the male rat. Toxicol Sci 2000, 2:339.
59. Paz M.S., Smith L.M., LaGasse L.L., Derauf C., Grant P., Shah R., Arria A., Huestis M., Haning W., Strauss A. Maternal depression and neurobehavior in newborns prenatally exposed to methamphetamine. Neurotoxicol Teratol 2009, 3:177-182.
60. Peck J., Sweeney A., Symanski E., Gardiner J., Silva M., Calafat A., Schantz S. Intra-and inter-individual variability of urinary phthalate metabolite concentrations in Hmong women of reproductive age. J Expo Sci Environ Epidemiol 2009, 1:90-100.
61. Poimenova A., Markaki E., Rahiotis C., Kitraki E. Corticosterone-regulated actions in the rat brain are affected by perinatal exposure to low dose of bisphenol A. Neuroscience 2010.
62. Preau J., Wong L., Silva M., Needham L., Calafat A. Variability over one week in the urinary concentrations of metabolites of diethyl phthalate and Di (2-Ethylhexyl) phthalate among 8 adults: an observational study. Environ Health Perspect 2010, doi.
63. Salian S., Doshi T., Vanage G. Perinatal exposure of rats to bisphenol A affects the fertility of male offspring. Life Sci 2009, 21-22:742-752.
64. Silva M., Preau J., Needham L., Calafat A. Cross validation and ruggedness testing of analytical methods used for the quantification of urinary phthalate metabolites. J Chromatogr B 2008, 2:180-186.
65. Somm E., Schwitzgebel V., Toulotte A., Cederroth C., Combescure C., Nef S., Aubert M., Hüppi P. Perinatal exposure to bisphenol A alters early adipogenesis in the rat 2009.
66. Stroud L.R., Paster R.L., Papandonatos G.D., Niaura R., Salisbury A.L., Battle C., Lagasse L.L., Lester B. Maternal smoking during pregnancy and newborn neurobehavior: effects at 10 to 27days. J Pediatr 2009, 1:10-16.
67. Swan S.H., Liu F., Hines M., Kruse R.L., Wang C., Redmon J.B., Sparks A., Weiss B. Prenatal phthalate exposure and reduced masculine play in boys. Int J Androl 2010, 2:259-269.
68. Tanaka T. Reproductive and neurobehavioural toxicity study of bis (2-ethylhexyl) phthalate (DEHP) administered to mice in the diet. Food Chem Toxicol 2002, 10:1499-1506.
69. Tanaka T. Reproductive and neurobehavioural effects of bis (2-ethylhexyl) phthalate (DEHP) in a cross-mating toxicity study of mice. Food Chem Toxicol 2005, 4:581-589.
70. Tian Y., Baek J., Lee S., Jang C. Prenatal and postnatal exposure to bisphenol a induces anxiolytic behaviors and cognitive deficits in mice. Synapse 2010, 6:432-439.
71. Tronick E., Olson K., Rosenberg R., Bohne L., Lu J., Lester B. Normative neurobehavioral performance of healthy infants on the neonatal intensive care unit network neurobehavioral scale. Pediatrics 2004, 3:676.
72. Völkel W., Kiranoglu M., Fromme H. Determination of free and total bisphenol A in urine of infants. Environ Res 2010.
73. von Goetz N., Wormuth M., Scheringer M., Hungerbühler K. Bisphenol A: how the most relevant exposure sources contribute to total consumer exposure. Risk Anal 2010, 3:473-487.
74. Vorhees C Principles of behavioral teratology. In: Riley E, Vorhees C, editors. Handbook of Teratology. New York: Plenum Press; 1986.
75. Whyatt R., Adibi J., Calafat A., Camann D., Rauh V., Bhat H., Perera F., Andrews H., Just A., Hoepner L. Prenatal di (2-ethylhexyl) phthalate exposure and length of gestation among an inner-city cohort. Pediatrics 2009, 6:e1213.
76. Wolff M.S., Engel S.M., Berkowitz G.S., Ye X., Silva M.J., Zhu C., Wetmur J., Calafat A.M. Prenatal phenol and phthalate exposures and birth outcomes. Environ Health Perspect 2008, 8:1092-1097.
77. Wolff M., Teitelbaum S., Pinney S., Windham G., Liao L., Biro F., Kushi L., Erdmann C., Hiatt R., Rybak M. Investigation of relationships between urinary biomarkers of phytoestrogens, phthalates, and phenols and pubertal stages in girls. Environ Health Perspect 2010, 7:1039.
78. Wormuth M., Scheringer M., Vollenweider M., Hungerbühler K. What are the sources of exposure to eight frequently used phthalic acid esters in Europeans?. Risk Anal 2006, 3:803-824.
79. Xu X., Zhang J., Wang Y., Ye Y., Luo Q. Perinatal exposure to bisphenol-A impairs learning-memory by concomitant down-regulation of N-methyl-d-aspartate receptors of hippocampus in male offspring mice. Horm Behav 2010.
80. Ye X., Kuklenyik Z., Needham L., Calafat A. Automated on-line column-switching HPLC-MS/MS method with peak focusing for the determination of nine environmental phenols in urine. Anal Chem 2005, 16:5407-5413.
81. Ye X., Pierik F.H., Hauser R., Duty S., Angerer J., Park M.M., Burdorf A., Hofman A., Jaddoe V.W.V., Mackenbach J.P. Urinary metabolite concentrations of organophosphorous pesticides, bisphenol A, and phthalates among pregnant women in Rotterdam, the Netherlands: the Generation R study. Environ Res 2008, 2:260-267.
82. Yolton K., Dietrich K., Auinger P., Lanphear B.P., Hornung R. Exposure to environmental tobacco smoke and cognitive abilities among US children and adolescents. Environ Health Perspect 2005, 1:98.
83. Yolton K., Khoury J., Xu Y., Succop P., Lanphear B., Bernert J., Lester B. Low-level prenatal exposure to nicotine and infant neurobehavior. Neurotoxicol Teratol 2009, 6:356-363.