Cited by 481Effects and risks of endocrine disrupting chemicalsSexual Differentiation and DisordersHealth, Environment, Cognitive Aging

Prenatal bisphenol A exposure and early childhood behavior.

Open access
Braun, Joe M., Yolton, Kimberly, Dietrich, Kim N., Hornung, Richard, Ye, Xiaoyun, Calafat, Antonia M., Lanphear, Bruce P.·2009·Environmental Health Perspectives

Abstract

Background: Prenatal exposure to bisphenol A (BPA) increases offspring aggression and diminishes differences in sexually dimorphic behaviors in rodents. Objective: We examined the association between prenatal BPA exposure and behavior in 2-year-old children. Methods: We used data from 249 mothers and their children in Cincinnati, Ohio (USA). Maternal urine was collected around 16 and 26 weeks of gestation and at birth. BPA concentrations were quantified using high-performance liquid chromatography–isotope-dilution tandem mass spectrometry. Child behavior was assessed at 2 years of age using the second edition of the Behavioral Assessment System for Children (BASC-2). The association between prenatal BPA concentrations and BASC-2 scores was analyzed using linear regression. Results: Median BPA concentrations were 1.8 (16 weeks), 1.7 (26 weeks), and 1.3 (birth) ng/mL. Mean (± SD) BASC-2 externalizing and internalizing scores were 47.6 ± 7.8 and 44.8 ± 7.0, respectively. After adjustment for confounders, log10-transformed mean prenatal BPA concentrations were associated with externalizing scores, but only among females [β = 6.0; 95% confidence interval (CI), 0.1–12.0]. Compared with 26-week and birth concentrations, BPA concentrations collected around 16 weeks were more strongly associated with externalizing scores among all children (β = 2.9; 95% CI, 0.2–5.7), and this association was stronger in females than in males. Among all children, measurements collected at ≤ 16 weeks showed a stronger association (β = 5.1; 95% CI, 1.5–8.6) with externalizing scores than did measurements taken at 17–21 weeks (β = 0.6; 95% CI, −2.9 to 4.1). Conclusions: These results suggest that prenatal BPA exposure may be associated with externalizing behaviors in 2-year-old children, especially among female children.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1289/ehp.0900979

Cites

7 of 7 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • In humans, a positive association between gestational levels of BPA in mothers and externalizing behaviors in 2 year old girls has been reported.

    “In humans, a positive association between gestational levels of BPA in mothers and externalizing (hyperactivity and aggression) behaviors in 2 year old girls has been reported [19].”

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 47

  1. Adriani W Seta DD Dessi-Fulgheri F Farabollini F Laviola G 2003 Altered profiles of spontaneous novelty seeking, impulsive behavior, and response to D-amphetamine in rats perinatally exposed to bisphenol A Environ Health Perspect 111 395 401 12676589 PMC1241418
  2. Bellinger DC 2004a Assessing environmental neurotoxicant exposures and child neurobehavior: confounded by confounding? Epidemiology 15 4 383 384 15232396
  3. Bellinger DC 2004b What is an adverse effect? A possible resolution of clinical and epidemiological perspectives on neurobehavioral toxicity Environ Res 95 3 394 405 15220073
  4. Bellinger DC Leviton A Sloman J 1990 Antecedents and correlates of improved cognitive performance in children exposed in utero to low levels of lead Environ Health Perspect 89 5 11 2088755 PMC1567781
  5. Brede C Fjeldal P Skjevrak I Herikstad H 2003 Increased migration levels of bisphenol A from polycarbonate baby bottles after dishwashing, boiling and brushing Food Addit Contam 20 7 684 689 12888395
  6. Carr R Bertasi F Betancourt A Bowers S Gandy BS Ryan P 2003 Effect of neonatal rat bisphenol A exposure on performance in the Morris water maze J Toxicol Environ Health A 66 21 2077 2088 14555403
  7. Chapin RE Adams J Boekelheide K Gray LE Jr Hayward SW Lees PS 2008 NTP-CERHR expert panel report on the reproductive and developmental toxicity of bisphenol A Birth Defects Res B Dev Reprod Toxicol 83 3 157 395 18613034
  8. Dietrich KN Eskenazi B Schantz S Yolton K Rauh VA Johnson CB 2005 Principles and practices of neurodevelopmental assessment in children: lessons learned from the Centers for Children’s Environmental Health and Disease Prevention Research Environ Health Perspect 113 1437 1446 16203260 PMC1281293
  9. Engel SM Zhu C Berkowitz GS Calafat AM Silva PA Miodovnik A 2009 Prenatal phthalate exposure and performance on the Neonatal Behavioral Assessment Scale in a multiethnic birth cohort Neurotoxicology 30 4 522 528 19375452 PMC4026936
  10. Farabollini F Porrini S Della Seta D Bianchi F Dessi-Fulgheri F 2002 Effects of perinatal exposure to bisphenol A on sociosexual behavior of female and male rats Environ Health Perspect 110 suppl 3 409 414 12060837 PMC1241191
  11. Fujimoto T Kubo K Aou S 2006 Prenatal exposure to bisphenol A impairs sexual differentiation of exploratory behavior and increases depression-like behavior in rats Brain Res 1068 1 49 55 16380096
  12. Greenland S 2008 Invited commentary: variable selection versus shrinkage in the control of multiple confounders Am J Epidemiol 167 5 523 531 18227100
  13. Greenland S Brumback B 2002 An overview of relations among causal modelling methods Int J Epidemiol 31 5 1030 1037 12435780
  14. Jester JM Nigg JT Adams K Fitzgerald HE Puttler LI Wong MM 2005 Inattention/hyperactivity and aggression from early childhood to adolescence: heterogeneity of trajectories and differential influence of family environment characteristics Dev Psychopathol 17 1 99 125 15971762 PMC2259463
  15. Kamphaus RW Petoskey MD Cody AH Rowe EW Huberty CJ Reynolds CR 1999 A typology of parent rated child behavior for a national U.S. sample J Child Psychol Psychiatry 40 4 607 616 10357166
  16. Kawai K Nozaki T Nishikata H Aou S Takii M Kubo C 2003 Aggressive behavior and serum testosterone concentration during the maturation process of male mice: the effects of fetal exposure to bisphenol A Environ Health Perspect 111 175 178 12573901 PMC1241346
  17. Kubo K Arai O Ogata R Omura M Hori T Aou S 2001 Exposure to bisphenol A during the fetal and suckling periods disrupts sexual differentiation of the locus coeruleus and of behavior in the rat Neurosci Lett 304 1–2 73 76 11335058
  18. Lee YJ Ryu HY Kim HK Min CS Lee JH Kim E 2008 Maternal and fetal exposure to bisphenol A in Korea Reprod Toxicol 25 4 413 419 18577445
  19. Li AA Baum MJ McIntosh LJ Day M Liu F Gray LE Jr 2008 Building a scientific framework for studying hormonal effects on behavior and on the development of the sexually dimorphic nervous system Neurotoxicology 29 3 504 519 18502513
  20. Mink PJ Goodman M Barraj LM Imrey H Kelsh MA Yager J 2004 Evaluation of uncontrolled confounding in studies of environmental exposures and neurobehavioral testing in children Epidemiology 15 4 385 393 15232397
  21. Miyagawa K Narita M Narita M Akama H Suzuki T 2007 Memory impairment associated with a dysfunction of the hippocampal cholinergic system induced by prenatal and neonatal exposures to bisphenol-A Neurosci Lett 418 3 236 241 17467901
  22. Nagao T Saito Y Usumi K Kuwagata M Imai K 1999 Reproductive function in rats exposed neonatally to bisphenol A and estradiol benzoate Reprod Toxicol 13 4 303 311 10453915
  23. Nagin DS Tremblay RE 2001 Analyzing developmental trajectories of distinct but related behaviors: a group-based method Psychol Methods 6 1 18 34 11285809
  24. Narita M Miyagawa K Mizuo K Yoshida T Suzuki T 2006 Prenatal and neonatal exposure to low-dose of bisphenol-A enhance the morphine-induced hyperlocomotion and rewarding effect Neurosci Lett 402 3 249 252 16678967
  25. Narita M Miyagawa K Mizuo K Yoshida T Suzuki T 2007 Changes in central dopaminergic systems and morphine reward by prenatal and neonatal exposure to bisphenol-A in mice: evidence for the importance of exposure period Addict Biol 12 2 167 172 17508988
  26. Needleman HL 1990 What can the study of lead teach us about other toxicants? Environ Health Perspect 86 183 189 2205488 PMC1567769
  27. Nerin C Fernandez C Domeno C Salafranca J 2003 Determination of potential migrants in polycarbonate containers used for microwave ovens by high-performance liquid chromatography with ultraviolet and fluorescence detection J Agric Food Chem 51 19 5647 5653 12952414
  28. Padmanabhan V Siefert K Ransom S Johnson T Pinkerton J Anderson L 2008 Maternal bisphenol-A levels at delivery: a looming problem? J Perinatol 28 4 258 263 18273031 PMC4033524
  29. Palanza P Gioiosa L vom Saal FS Parmigiani S 2008 Effects of developmental exposure to bisphenol A on brain and behavior in mice Environ Res 108 2 150 157 18949834
  30. Palanza P Morellini F Parmigiani S vom Saal FS 1999 Prenatal exposure to endocrine disrupting chemicals: effects on behavioral development Neurosci Biobehav Rev 23 7 1011 1027 10580314
  31. Pocock SJ Ashby D Smith MA 1987 Lead exposure and children’s intellectual performance Int J Epidemiol 16 1 57 67 3570623
  32. Reynolds CR Kamphaus RW 2002 The Clinician’s Guide to the Behavior Assessment System for Children (BASC) New York Guilford Press
  33. Ris MD Dietrich KN Succop PA Berger OG Bornschein RL 2004 Early exposure to lead and neuropsychological outcome in adolescence J Int Neuropsychol Soc 10 2 261 270 15012846
  34. Rothman KJ Greenland S 1998 Modern Epidemiology 2nd ed Philadelphia, PA Lippincott Williams & Wilkins
  35. Savitz DA Olshan AF 1995 Multiple comparisons and related issues in the interpretation of epidemiological data Am J Epidemiol 142 9 904 908 7572970
  36. Schonfelder G Wittfoht W Hopp H Talsness CE Paul M Chahoud I 2002 Parent bisphenol A accumulation in the human maternal–fetal–placental unit Environ Health Perspect 110 A703 A707 12417499 PMC1241091
  37. Stahlhut RW Welshons WV Swan SH 2009 Bisphenol A data in NHANES suggest longer than expected half-life, substantial nonfood exposure, or both Environ Health Perspect 117 784 789 19479022 PMC2685842
  38. Suzuki T Mizuo K Nakazawa H Funae Y Fushiki S Fukushima S 2003 Prenatal and neonatal exposure to bisphenol-A enhances the central dopamine D1 receptor-mediated action in mice: enhancement of the methamphetamine-induced abuse state Neuroscience 117 3 639 644 12617968
  39. Tan BL Mustafa AM 2003 Leaching of bisphenol A from new and old babies’ bottles, and new babies’ feeding teats Asia Pac J Public Health 15 2 118 123 15038686
  40. Tremblay RE Nagin DS Seguin JR Zoccolillo M Zelazo PD Boivin M 2004 Physical aggression during early childhood: trajectories and predictors Pediatrics 114 1 e43 e50 15231972 PMC3283570
  41. Volkel W Colnot T Csanady GA Filser JG Dekant W 2002 Metabolism and kinetics of bisphenol A in humans at low doses following oral administration Chem Res Toxicol 15 10 1281 1287 12387626
  42. Vreugenhil HJI Slijper FME Mulder PGH Weisglas-Kuperus N 2002 Effects of perinatal exposure to PCBs and dioxins on play behavior in Dutch children at school age Environ Health Perspect 110 593 598 PMC1241045 12361940
  43. Welshons WV Thayer KA Judy BM Taylor JA Curran EM vom Saal FS 2003 Large effects from small exposures. I. Mechanisms for endocrine-disrupting chemicals with estrogenic activity Environ Health Perspect 111 994 1006 12826473 PMC1241550
  44. Wolff MS Engel SM Berkowitz GS Ye X Silva MJ Zhu C 2008 Prenatal phenol and phthalate exposures and birth outcomes Environ Health Perspect 116 1092 1097 18709157 PMC2516577
  45. Ye X Bishop AM Reidy JA Needham LL Calafat AM 2007 Temporal stability of the conjugated species of bisphenol A, parabens, and other environmental phenols in human urine J Expo Sci Environ Epidemiol 17 6 567 572 17410114
  46. Ye X Kuklenyik Z Needham LL Calafat AM 2005a Automated on-line column-switching HPLC-MS/MS method with peak focusing for the determination of nine environmental phenols in urine Anal Chem 77 16 5407 5413 16097788
  47. Ye X Kuklenyik Z Needham LL Calafat AM 2005b Quantification of urinary conjugates of bisphenol A, 2,5-dichlorophenol, and 2-hydroxy-4-methoxybenzophenone in humans by online solid phase extraction-high performance liquid chromatography-tandem mass spectrometry Anal Bioanal Chem 383 4 638 644 16132150

Cited by

Sorted by citations

Authors
Braun, J. M., Yolton, K., Dietrich, K. N., Hornung, R., Ye, X., Calafat, A. M., & Lanphear, B. P.
Affiliations
  • University of North Carolina at Chapel Hill (US)
  • Cincinnati Children's Hospital Medical Center (US)
  • University of Cincinnati (US)
  • Centers for Disease Control and Prevention (US)
Corresponding author
Lanphear, Bruce P.
Venue
Environmental Health Perspectives
Published
2009-10-06
Volume
117
Issue
12
Pages
1945-1952
ISSN
  • 0091-6765 (ISSN-L)
  • 1552-9924
OpenAlex
W1965966912
Cited by
481
References
7
Citations by year
2026: 5 · 2025: 17 · 2024: 22 · 2023: 23 · 2022: 13 · 2021: 31 · 2020: 32 · 2019: 23 · 2018: 26 · 2017: 29 · 2016: 41 · 2015: 45 · 2014: 36 · 2013: 42 · 2012: 37
FWCI
22.49
Type
journal article
Language
en
Open access
Locations
  • Environmental Health Perspectives (publishedVersion, public-domain)
  • Europe PMC (PubMed Central) (publishedVersion, public-domain)
  • PubMed Central (publishedVersion, public-domain)
  • PubMed (publishedVersion)
  • Carolina Digital Repository (University of North Carolina at Chapel Hill) (submittedVersion)
  • UNC Libraries
Funders
  • U.S. Environmental Protection Agency (P01 ES11261)
  • Centers for Disease Control and Prevention (P01 ES11261)
  • National Institute of Environmental Health Sciences (P01 ES11261, P01ES011261)
  • National Institute of Child Health and Human Development
  • Eunice Kennedy Shriver National Institute of Child Health and Human Development (T32-HD052468-01, T32HD052468)
Topics
  • Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Effects and risks of endocrine disrupting chemicals
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Sexual Differentiation and Disorders
  • Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Health, Environment, Cognitive Aging
Keywords
bisphenol A, prenatal exposure, endocrine disruptors, child behavior, externalizing problems, internalizing problems, maternal urine, sex differences, early childhood, developmental neurotoxicity
MeSH terms
Bisphenol A Compounds, Adult, Benzhydryl Compounds, Child Behavior, Child, Preschool, Female, Fetus, Humans, Male, Phenols, Pregnancy, Sex Characteristics

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review