The DOI matches its Crossref record; 17 of the 18 references it cites were found in a registry or an index.
Effects of Perinatal Exposure to Bisphenol A on Play Behavior of Female and Male Juvenile Rats
Open accessAbstract
In higher vertebrates, estrogen can exert an organizational effect on sexually dimorphic areas of the central nervous system (CNS) during the perinatal phase of development. The possibility that estrogenic pollutants may mimic estrogen action on the CNS during development and produce long-lasting or irreversible effects is an issue of great concern. Bisphenol A (BPA), a compound widely used in the food industry and in dentistry, has proven estrogenic actions. To study its potential developmental effects on behavior, we gave female Sprague-Dawley rats 40 microg/kg/day BPA from conception to weaning postnatal day 21 and 400 microg/kg/day BPA from gestation day 14 to postnatal day 6. After exposure, we studied social behavior in a play situation in juvenile male and female offspring. The attempt to use play behavior to study the effects of BPA yielded some interesting results. We observed an early action of BPA on several behavioral categories in both males and females. In particular we observed a masculinization of female behavior in two behavioral categories (play with females and sociosexual exploration), an effect probably mediated by the estrogenic activity of BPA in the CNS. These long-lasting effects of BPA could have important consequences at individual and population levels.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
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 the citing paper
“Perinatal exposure to bisphenol A, an environmental estrogen, or diethylstilbestrol dipropionate, a synthetic estrogen, also increases play in female rats and rhesus macaques, respectively (Dessi-Fulgheri et al., 2002; Goy & Deputte, 1996).”
From Developmental origins of sex differences in the neural circuitry of play (2020) · cites this paper as Dessi-Fulgheri et al., 2002
In the citing paper
“BPA can also influence social interactions and anxiety in rodents [7], [15], [16], [17].”
From Gestational Exposure to Low Dose Bisphenol A Alters Social Behavior in Juvenile Mice (2011) · cites this paper as [15]
In the citing paper
“In juvenile females, BPA increased both non-social and social investigation [15].”
From Gestational Exposure to Low Dose Bisphenol A Alters Social Behavior in Juvenile Mice (2011) · cites this paper as [15]
In the citing paper
“When tested with males, juvenile females exposed to BPA exhibited reduced play and social grooming.”
From Gestational Exposure to Low Dose Bisphenol A Alters Social Behavior in Juvenile Mice (2011) · cites this paper as [15]
In the citing paper
“However, in none of those three studies was the litter statistically controlled.”
From Developmental Treatment with Ethinyl Estradiol, but Not Bisphenol A, Causes Alterations in Sexually Dimorphic Behaviors in Male and Female Sprague Dawley Rats (2014) · cites this paper as Dessi-Fulgheri et al., 2002
In the citing paper
“However, recent research showed that estrogens or estrogenic EDCs are also involved in the development of play behavior in rats [15–19].”
From Developmental exposure to low levels of ethinylestradiol affects social play in juvenile male rats (2020) · cites this paper as [15]
In the citing paper
“and it is associated with cognitive and social impairments in rodents [ 48 , 133–135 ].”
From DNA methylation: a mechanism linking environmental chemical exposures to risk of autism spectrum disorders? (2016) · cites this paper as [133]
Citations
Cites
Bisphenol-A: an estrogenic substance is released from polycarbonate flasks during autoclaving
Krishnan, A. V., Stathis, P., Permuth, S. F., Tokes, L., & Feldman, D. (1993) · Endocrinology · doi:10.1210/endo.132.6.8504731 · Cited by 1,629
Gonadal Steroid Induction of Structural Sex Differences in the Central Nervous System
Arnold, A. P., & Gorski, R. A. (1984) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.07.030184.002213 · Cited by 1,198
Estrogenicity of Resin-Based Composites and Sealants Used in Dentistry
Olea, N., Pulgar, R., Pérez, P., Olea‐Serrano, F., Rivas, A., Novillo-Fertrell, A., Pedraza, V., Soto, A. M., & Sonnenschein, C. (1996) · Environmental Health Perspectives · doi:10.1289/ehp.96104298 · Cited by 1,041
Xenoestrogens Released from Lacquer Coatings in Food Cans
Brotons, J. A., Olea‐Serrano, F., Villalobos, M., Pedraza, V., & Olea, N. (1995) · Environmental Health Perspectives · doi:10.1289/ehp.95103608 · Cited by 942
Colborn, T. L., Dumanoski, D., & Myers, J. P. (1996) · Medical Entomology and Zoology · Cited by 824
Exposure to bisphenol A advances puberty
Howdeshell, K. L., Hotchkiss, A. K., Thayer, K. A., Vandenbergh, J. G., & vom Saal, F. S. (1999) · Nature · doi:10.1038/44517 · Cited by 820 · cited 3×
“Low doses of BPA administered perinatally can modify explorative behavior and anxiety in rats (9) and can advance puberty in female mice (10), although some effects are controversial (11).”
BackgroundOrganizational and activational effects of sex steroids on brain and behavior: A reanalysis
Arnold, A. P. (1985) · Hormones and Behavior · doi:10.1016/0018-506x(85)90042-x · Cited by 807
The neurobiology of social play behavior in rats
Vanderschuren, L. J. M. J., Niesink, R. J. M., & Van Pee, J. M. (1997) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(96)00020-6 · Cited by 559
The Environmental Estrogen Bisphenol A Stimulates Prolactin Release in Vitro and in Vivo
Steinmetz, R. W., Brown, N. G., Allen, D. L., Bigsby, R. M., & Ben‐Jonathan, N. (1997) · Endocrinology · doi:10.1210/endo.138.5.5132 · Cited by 520
Bisphenol A interacts with the estrogen receptor α in a distinct manner from estradiol
Gould, J. C., Leonard, L. S., Maness, S. C., Wagner, B. L., Conner, K., Zacharewski, T., Safe, S., McDonnell, D. P., & Gaido, K. W. (1998) · Molecular and Cellular Endocrinology · doi:10.1016/s0303-7207(98)00084-7 · Cited by 510
Flagged first, then by citations
1 of the 18 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Items 101–147 of 147
Alò, R., Facciolo, R. M., Madeo, M., Giusi, G., Carelli, A., & Canonaco, M. (2005) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2005.01.006 · Cited by 22
Panzica, G., Mura, E., Miceli, D., Martini, M., Gotti, S., & Viglietti‐Panzica, C. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2008.03628.x · Cited by 21
Wise, L. M., Hernández‐Saavedra, D., Boas, S. M., Pan, Y., & Juraska, J. M. (2018) · Developmental Neuroscience · doi:10.1159/000494879 · Cited by 20
Is Play Behavior Sexually Dimorphic in Monogamous Species?
Chau, M. J., Stone, A. I., Mendoza, S. P., & Bales, K. L. (2008) · Ethology · doi:10.1111/j.1439-0310.2008.01543.x · Cited by 21
Faith, R. E., & Hessler, J. R. (2006) · Elsevier eBooks · doi:10.1016/b978-012074903-4/50013-3 · Cited by 21
Blake, B. E., & McCoy, K. A. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.04.021 · Cited by 20
Developmental exposure to xenoestrogen enhances spatial learning in male rats
Corrieri, L., Della Seta, D., Canoine, V., & Fusani, L. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.03.002 · Cited by 20
Torres‐Alamilla, P., Castillo-Sánchez, R., Cortés‐Reynosa, P., Gómez, R., & Salazar, E. P. (2023) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2023.111998 · Cited by 19
Children's cognitive health: the influence of environmental chemical exposures.
Bellinger, D. C. (2007) · PubMed · Cited by 17
Endocrine-disrupting Chemicals (EDCs) in Mammals
Pelch, K. E., Beeman, J. M., Niebruegge, B. A., Winkeler, S. R., & Nagel, S. C. (2011) · Elsevier eBooks · doi:10.1016/b978-0-12-374928-4.10014-8 · Cited by 16
Endocrine-Disrupting Chemicals
Frye, C. A. (2014) · Vitamins & Hormones · doi:10.1016/b978-0-12-800095-3.00003-1 · Cited by 22
Dias, G. R. M., Giusti, F. C. V., de Novais, C. O., de Oliveira, M. A. L., Paiva, A. G., Kalil-Cutti, B., Mahoney, M. M., & Graceli, J. B. (2025) · Frontiers in Endocrinology · doi:10.3389/fendo.2025.1571689 · Cited by 14
Flynn, K. M., Delclos, K. B., Newbold, R. R., & Ferguson, S. A. (2005) · Food and Chemical Toxicology · doi:10.1016/j.fct.2005.03.009 · Cited by 14
Zaccaroni, M., Seta, D. D., Farabollini, F., Fusani, L., & Dessì‐Fulgheri, F. (2016) · Neurotoxicity Research · doi:10.1007/s12640-016-9645-1 · Cited by 16
Self-citationFacciolo, R. M., Madeo, M., Alò, R., Canonaco, M., & Dessì‐Fulgheri, F. (2005) · Toxicological Sciences · doi:10.1093/toxsci/kfi322 · Cited by 14
Self-citationIbroçi, E., Thurston, S. W., Barrett, E. S., Bush, N. R., Nguyen, R. H. N., Sathyanarayana, S., Reichenberg, A., Collett, B. R., Swan, S. H., & Evans, S. F. (2022) · NeuroToxicology · doi:10.1016/j.neuro.2022.05.018 · Cited by 16
Drzewiecki, C. M., Brinks, A. S., Sellinger, E. P., Doshi, A., Koh, J. Y., & Juraska, J. M. (2022) · NeuroToxicology · doi:10.1016/j.neuro.2022.11.011 · Cited by 12
Pandey, A. K., & Deshpande, S. B. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.01.010 · Cited by 11
Early estradiol exposure masculinizes disease‐relevant behaviors in female mice
Seiffe, A., Ramirez, M. F., Barrios, C. D., Albarrán, M. M., & Depino, A. M. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.15130 · Cited by 11
Kubo, I., Yokota, N., Fuchiwaki, Y., & Nakane, Y. (2012) · ISRN Materials Science · doi:10.5402/2012/861643 · Cited by 10
Kubota, A., Hirano, M., Yoshinouchi, Y., Chen, X., Nakamura, M., Wakayama, Y., Lee, J., Nakata, H., Iwata, H., & Kawai, Y. K. (2023) · Comparative Biochemistry and Physiology Part C Toxicology & Pharmacology · doi:10.1016/j.cbpc.2023.109619 · Cited by 9
Chemical Pollutants Threatening Food Safety and Security: An Overview
Mansour, S. A. (2011) · NATO science for peace and security series. A, Chemistry and biology · doi:10.1007/978-94-007-1100-6_6 · Cited by 9
Yu, C., Tai, F., Wu, R., Song, Z., Zhang, X., & An, X. (2010) · Behavioural Pharmacology · doi:10.1097/fbp.0b013e32833aec1a · Cited by 10
Bisphenol A: Understanding Its Health Effects from the Studies Performed on Model Organisms
Ghosh, P., Roy, S. S., Begum, M., & Ghosh, S. (2017) · InTech eBooks · doi:10.5772/intechopen.68971 · Cited by 9
Taherianfard, M., & Ahmadijokani, S. (2023) · Brain and Behavior · doi:10.1002/brb3.2942 · Cited by 7
Morin, A., de Beeck, L. V., Person, E., & Plamondon, H. (2021) · Frontiers in Toxicology · doi:10.3389/ftox.2021.639820 · Cited by 7
Endocrine Disruptors as a Factor in Mental Retardation
Weiss, B. (2005) · International review of research in mental retardation · doi:10.1016/s0074-7750(05)30006-1 · Cited by 7
Determinação de bisfenol A em fórmulas infantis
Bomfim, M. V. J., Bazílio, F. S., Zamith, H. P. D. S., & Abrantes, S. D. M. P. (2014) · Vigilância Sanitária em Debate · doi:10.3395/2317-269x.00415 · Cited by 7
Endocrine-disrupting Chemicals (EDCs) in Mammals
Pelch, K. E., Beeman, J. M., Niebruegge, B. A., Winkeler, S. R., & Nagel, S. C. (2011) · Elsevier eBooks · doi:10.1016/b978-0-12-374932-1.00061-5 · Cited by 6
Developmental exposure to low levels of ethinylestradiol affects social play in juvenile male rats
Zaccaroni, M., Massolo, A., Beani, L., Seta, D. D., Farabollini, F., Giannelli, G., Fusani, L., & Dessì-Fulgheri, F. (2020) · Toxicological Research · doi:10.1007/s43188-019-00035-z · Cited by 5
Self-citationFaith, R. E., Allen, K. P., & Hessler, J. R. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-814338-4.00010-6 · Cited by 6
BPA Effects In Vivo: Evidence from Animal Studies
Kitraki, E. (2013) · Springer eBooks · doi:10.1007/978-3-642-29687-1_4 · Cited by 5
Problems In Assessing Low Dose Effects Of Endocrine Disrupters
Gies, A. (2007) · Springer eBooks · doi:10.1007/1-4020-4829-7_13 · Cited by 4
Goodman, J. E., & Rhomberg, L. R. (2009) · Elsevier eBooks · doi:10.1533/9781845695743.4.406 · Cited by 3
ENVIRONMENT-DEPENDENT HUMAN DISEASES: THE EPIGENETIC MECHANISMS OF THEIR DEVELOPMENT AND INHERITANCE
Patkin, E. L., & Софронов, Г. А. (2015) · Medical academic journal · doi:10.17816/maj1537-23 · Cited by 4
In Utero Bisphenol A Exposure and Epigenetic Programming of Neurobehavioral Outcomes
Kundaković, M. (2016) · Springer eBooks · doi:10.1007/978-3-319-25325-1_3 · Cited by 3
Lian, T., Zhang, X., Wang, X., Wang, R., Gao, H., Tai, F., & Yu, Q. (2020) · Toxicology Research · doi:10.1093/toxres/tfaa014 · Cited by 2
(NTP), N. T. P. (2019) · Chemical Effects in Biological Systems (CEBS) · doi:10.22427/ntp-data-021-00004-0001-0000-8 · Cited by 2
Early prenatal sex steroids and sex-typed play behavior at 4 years of age
Sethuram, S., Raymond, S., Wang, C., Barrett, E. S., Bush, N. R., Nguyen, R. H. N., Sathyanarayana, S., Swan, S. H., & Evans, S. F. (2023) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2023.106288 · Cited by 1
Developmental Exposure to Environmental Estrogens Alters Adult Behavior in Female Rodents
Ryan, B. C. (2005) · NCSU Libraries Repository (North Carolina State University Libraries) · Cited by 1
Sadowski, R. N. (2013) · Illinois Digital Environment for Access to Learning and Scholarship (University of Illinois at Urbana-Champaign)
Review Article Bisphenol A: Developmental Toxicity from Early Prenatal Exposure
Golub, M. S., Wu, K. L., Kaufman, F. L., Li, L., Moran, F. M., Zeise, L. A., Alexeeff, G. V., & Donald, J. M. (2010)
왕승문, 황규근, & Jong-Min, K. (2011) · Annals of Child Neurology · doi:10.26815/jkcns.2011.19.3.218
Harbison, R. D., & Conaway, C. C. (2015) · John Wiley & Sons, Inc. eBooks · doi:10.1002/9781118834015.ch57
Yumurta sarısına enjekte edilen bisfenol A nın tavuklarda iskelet kası gelişimi üzerindeki etkileri
Öznurlu, Y., Özaydın, T., Sur, E., & Kuşat, T. (2022) · Eurasian journal of veterinary sciences · doi:10.15312/eurasianjvetsci.2022.369
(2013) · PubMed · Cited by 22
Metadata
- Authors
- Dessì-Fulgheri, F., Porrini, S., & Farabollini, F.
- Affiliations
- University of Florence (IT)
- Venue
- Environmental Health Perspectives
- Publisher
- American Chemical Society (ACS)
- Published
- 2002-03-27
- Volume
- 110
- Issue
- s3
- Pages
- 403-407
- ISSN
- 0091-6765 (ISSN-L)
- PMC
- PMC1241190
- OpenAlex
- W1983073558
- Cited by
- 146
- References
- 18
- Citations by year
- 2025: 1 · 2023: 5 · 2022: 3 · 2021: 4 · 2020: 4 · 2019: 6 · 2018: 5 · 2017: 4 · 2016: 6 · 2015: 9 · 2014: 8 · 2013: 11 · 2012: 7
- FWCI
- 5.63
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Environmental Health Perspectives (publishedVersion)
- Environmental Health Perspectives (publishedVersion, public-domain)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Florence Research (University of Florence) (submittedVersion)
- Topics
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Effects and risks of endocrine disrupting chemicals
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Sexual Differentiation and Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Estrogen and related hormone effects
- Keywords
- bisphenol A, perinatal exposure, xenoestrogens, social play, sex differences in behavior, endocrine disruptors, young rats
- MeSH terms
- Bisphenol A Compounds, Administration, Oral, Animals, Animals, Newborn, Behavior, Animal, Benzhydryl Compounds, Central Nervous System, Endocrine System, Environmental Exposure, Estrogens, Non-Steroidal, Female, Male, Phenols, Play and Playthings, Pregnancy, Prenatal Exposure Delayed Effects, Sex Characteristics, Social Behavior, Rats, Sprague-Dawley, Rats
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