Effects of Perinatal Exposure to Bisphenol A on Play Behavior of Female and Male Juvenile Rats

Dessì-Fulgheri, Francesco; Porrini, Stefania; Farabollini, Francesca

doi:10.1289/ehp.02110s3403

Cited by 147Effects and risks of endocrine disrupting chemicalsSexual Differentiation and DisordersEstrogen and related hormone effects

Effects of Perinatal Exposure to Bisphenol A on Play Behavior of Female and Male Juvenile Rats

Open access

Dessì-Fulgheri, Francesco, Porrini, Stefania, Farabollini, Francesca·2002·Environmental Health Perspectives

DOI 10.1289/ehp.02110s3403PMC PMC1241190

Open this paper in CoChat — free account

Abstract

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.

Integrity signals

Registry

Crossref · 10.1289/ehp.02110s3403

Cites

17 of 17 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

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?

Perinatal exposure to bisphenol A or diethylstilbestrol dipropionate increases play in female rats and rhesus macaques, respectively.
“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
BPA can influence social interactions and anxiety in rodents.
“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 juvenile female rats, BPA increased both non-social and social investigation.
“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]
When tested with males, juvenile female rats exposed to BPA exhibited reduced play and social grooming.
“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 none of the three studies (Porrini et al., 2005; Dessi-Fulgheri et al., 2002; Wolstenholme et al., 2011) was the litter statistically controlled.
“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

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 1,614 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Our Stolen Future
Colborn, T. L., Dumanoski, D., & Myers, J. P. (1996) · Medical Entomology and Zoology · Cited by 824 · see citing works
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 · see citing works
Organizational 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 805 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Multiple Differences in the Play Fighting of Male and Female Rats. Implications for the Causes and Functions of Play
PELLIS, S. M., FIELD, E. F., SMITH, L. K., & PELLIS, V. C. (1997) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(95)00060-7 · Cited by 234 · see citing works
Environmental estrogens: health implications for humans and wildlife.
Colborn, T. L. (1995) · Environmental Health Perspectives · doi:10.1289/ehp.95103s7135 · Cited by 204 · see citing works
Perinatal Exposure to the Estrogenic Pollutant Bisphenol A Affects Behavior in Male and Female Rats
Farabollini, F. (1999) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(99)00136-7 · Cited by 183 · see citing works
Self-citation
Sexual differentiation of social play in rat pups is mediated by the neonatal androgen-receptor system
Meaney, M. J., Stewart, J., Poulin, P., & McEwen, B. S. (2008) · Neuroendocrinology · doi:10.1159/000123524 · Cited by 144 · see citing works
Reproductive function in rats exposed neonatally to bisphenol A and estradiol benzoate
Nagao, T., Saito, Y., Usumi, K., Kuwagata, M., & Imai, K. (1999) · Reproductive Toxicology · doi:10.1016/s0890-6238(99)00017-9 · Cited by 122 · see citing works
Editorial: Estrogens from Plastic—Are We Being Exposed?
Feldman, D. I. (1997) · Endocrinology · doi:10.1210/endo.138.5.5213 · Cited by 78 · see citing works
Influenza di xenoestrogeni (bisfenolo A) sul sistema a SRIF in alcune aree limbiche di ratto femmina
Facciolo, R. M., Alò, R., Pappaianni, F., M., M., Carelli, A., Canonaco, M., & Dessì‐Fulgheri, F. (2001) · Cited by 1 · see citing works
Self-citation

Flagged first, then by citations

1 of the 18 references couldn’t be matched to a known paper.

Sorted by citations

Bisphenol-A and the Great Divide: A Review of Controversies in the Field of Endocrine Disruption
Vandenberg, L. N., Maffini, M. V., Sonnenschein, C., Rubin, B. S., & Soto, A. M. (2009) · Endocrine Reviews · doi:10.1210/er.2008-0021 · Cited by 1,407 · see citing works
An Extensive New Literature Concerning Low-Dose Effects of Bisphenol A Shows the Need for a New Risk Assessment
Saal, F. S. V., & Hughes, C. L. (2005) · Environmental Health Perspectives · doi:10.1289/ehp.7713 · Cited by 1,174 · see citing works
In vivo effects of bisphenol A in laboratory rodent studies
Richter, C. A., Birnbaum, L. S., Farabollini, F., Newbold, R. R., Rubin, B. S., Talsness, C. E., Vandenbergh, J. G., Walser-Kuntz, D. R., & vom Saal, F. S. (2007) · Reproductive Toxicology · doi:10.1016/j.reprotox.2007.06.004 · Cited by 1,147 · see citing works
Self-citation
Components of plastic: experimental studies in animals and relevance for human health
Talsness, C. E., Martino‐Andrade, A. J., Kuriyama, S. N., Taylor, J. A., & Saal, F. S. V. (2009) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2008.0281 · Cited by 639 · see citing works
NTP‐CERHR expert panel report on the reproductive and developmental toxicity of bisphenol A
Chapin, R. E., Adams, J., Boekelheide, K., Gray, L. E., Hayward, S. W., Lees, P. S. J., Mcintyre, B., Portier, K. M., Schnorr, T. M., Selevan, S. G., et al. (2008) · Birth Defects Research Part B Developmental and Reproductive Toxicology · doi:10.1002/bdrb.20147 · Cited by 504 · see citing works
Sex-specific epigenetic disruption and behavioral changes following low-dose in utero bisphenol A exposure
Kundakovic, M., Gudsnuk, K., Franks, B., Madrid, J., Miller, R. L., Perera, F. P., & Champagne, F. A. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1214056110 · Cited by 490 · see citing works
Prenatal bisphenol A exposure and early childhood behavior.
Braun, J. M., Yolton, K., Dietrich, K. N., Hornung, R., Ye, X., Calafat, A. M., & Lanphear, B. P. (2009) · Environmental Health Perspectives · doi:10.1289/ehp.0900979 · Cited by 481 · see citing works
Perinatal Exposure to Bisphenol A Alters Early Adipogenesis in the Rat
Somm, E., Schwitzgebel, V. M., Toulotte, A., Cederroth, C. R., Combescure, C., Nef, S., Aubert, M. L., & Hüppi, P. S. (2009) · Environmental Health Perspectives · doi:10.1289/ehp.11342 · Cited by 467 · see citing works
Gestational Exposure to Bisphenol A Produces Transgenerational Changes in Behaviors and Gene Expression
Wolstenholme, J. T., Edwards, M., Shetty, S. R. J., Gatewood, J. D., Taylor, J. A., Rissman, E. F., & Connelly, J. J. (2012) · Endocrinology · doi:10.1210/en.2012-1195 · Cited by 319 · see citing works
The role of bisphenol A in shaping the brain, epigenome and behavior
Wolstenholme, J. T., Rissman, E. F., & Connelly, J. J. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.10.001 · Cited by 309 · see citing works
The role of animal behaviour in the study of endocrine-disrupting chemicals
Clotfelter, E. D., Bell, A. M., & LeVering, K. (2004) · Animal Behaviour · doi:10.1016/j.anbehav.2004.05.004 · Cited by 275 · see citing works
Epigenetic perspective on the developmental effects of bisphenol A
Kundaković, M., & Champagne, F. A. (2011) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2011.02.005 · Cited by 270 · see citing works
Evidence of altered brain sexual differentiation in mice exposed perinatally to low, environmentally relevant levels of bisphenol A.
Rubin, B. S., Lenkowski, J. R., Schaeberle, C. M., Vandenberg, L. N., Ronsheim, P. M., & Soto, A. M. (2006) · Endocrinology · doi:10.1210/en.2006-0189 · Cited by 311 · see citing works
Large effects from small exposures. II. The importance of positive controls in low-dose research on bisphenol A
Saal, F. S. V., & Welshons, W. V. (2005) · Environmental Research · doi:10.1016/j.envres.2005.09.001 · Cited by 257 · see citing works
Bisphenol A prevents the synaptogenic response to estradiol in hippocampus and prefrontal cortex of ovariectomized nonhuman primates
Leranth, C., Hajszán, T., Szigeti‐Buck, K., Bober, J., & MacLusky, N. J. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0806139105 · Cited by 232 · see citing works
Endocrine disruptors: from Wingspread to environmental developmental biology
Markey, C. M., Rubin, B. S., Soto, A. M., & Sonnenschein, C. (2002) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/s0960-0760(02)00272-8 · Cited by 212 · see citing works
Bisphenol A: Human exposure and neurobehavior
Mustieles, V., Pérez‐Lobato, R., Olea, N., & Fernández, M. F. (2015) · NeuroToxicology · doi:10.1016/j.neuro.2015.06.002 · Cited by 203 · see citing works
Derivation of a Bisphenol a Oral Reference Dose (RfD) and Drinking-Water Equivalent Concentration∗
Willhite, C. C., Ball, G. L., & McLellan, C. J. (2008) · Journal of Toxicology and Environmental Health Part B · doi:10.1080/10937400701724303 · Cited by 198 · see citing works
Prenatal and postnatal exposure to bisphenol a induces anxiolytic behaviors and cognitive deficits in mice
Tian, Y., Baek, J., Lee, S., & Jang, C. (2010) · Synapse · doi:10.1002/syn.20746 · Cited by 197 · see citing works
The control of sexual differentiation of the reproductive system and brain
WILSON, C. A., & Davies, D. C. (2007) · Reproduction · doi:10.1530/rep-06-0078 · Cited by 184 · see citing works
Bisphenol A exposure and children’s behavior: A systematic review
Ejaredar, M., Lee, Y., Roberts, D. J., Sauve, R. S., & Dewey, D. (2016) · Journal of Exposure Science & Environmental Epidemiology · doi:10.1038/jes.2016.8 · Cited by 170 · see citing works
Gestational Exposure to Low Dose Bisphenol A Alters Social Behavior in Juvenile Mice
Wolstenholme, J. T., Taylor, J. A., Shetty, S. R. J., Edwards, M., Connelly, J. J., & Rissman, E. F. (2011) · PLoS ONE · doi:10.1371/journal.pone.0025448 · Cited by 168 · see citing works
“In juvenile females, BPA increased both non-social and social investigation [15].”
Background
DNA methylation: a mechanism linking environmental chemical exposures to risk of autism spectrum disorders?
Keil, K. P., & Lein, P. J. (2016) · Environmental Epigenetics · doi:10.1093/eep/dvv012 · Cited by 167 · see citing works
Developmental exposure to low-dose estrogenic endocrine disruptors alters sex differences in exploration and emotional responses in mice.
Gioiosa, L., Fissore, E., Ghirardelli, G., Parmigiani, S., & Palanza, P. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.05.006 · Cited by 160 · see citing works
Bisphenol-A: Epigenetic Reprogramming and Effects on Reproduction and Behavior
Mileva, G. R., Baker, S., Konkle, A. T. M., & Bielajew, C. H. (2014) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph110707537 · Cited by 160 · see citing works
Transgenerational effects of prenatal bisphenol A on social recognition
Wolstenholme, J. T., Goldsby, J. A., & Rissman, E. F. (2013) · Hormones and Behavior · doi:10.1016/j.yhbeh.2013.09.007 · Cited by 157 · see citing works
Prenatal exposure to bisphenol A impairs sexual differentiation of exploratory behavior and increases depression-like behavior in rats
Fujimoto, T., Kubo, K., & Aou, S. (2005) · Brain Research · doi:10.1016/j.brainres.2005.11.028 · Cited by 157 · see citing works
Adaptive Cellular Stress Pathways as Therapeutic Targets of Dietary Phytochemicals: Focus on the Nervous System
Lee, J., Jo, D., Park, D., Chung, H. Y., & Mattson, M. P. (2014) · Pharmacological Reviews · doi:10.1124/pr.113.007757 · Cited by 154 · see citing works
Current concepts in neuroendocrine disruption
León‐Olea, M., Martyniuk, C. J., Orlando, E. F., Ottinger, M. A., Rosenfeld, C. S., Wolstenholme, J. T., & Trudeau, V. L. (2014) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2014.02.005 · Cited by 144 · see citing works
Exposure to Bisphenol A Prenatally or in Adulthood Promotes TH2 Cytokine Production Associated with Reduction of CD4+CD25+ Regulatory T Cells
Yan, H., Takamoto, M., & Sugane, K. (2008) · Environmental Health Perspectives · doi:10.1289/ehp.10829 · Cited by 141 · see citing works
Impact of environmental chemicals on the thyroid hormone function in pituitary rat GH3 cells
Ghisari, M., & Bonefeld‐Jørgensen, E. C. (2005) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2005.01.013 · Cited by 134 · see citing works
Relationship Between Urine Bisphenol‐A Level and Declining Male Sexual Function
Li, D., Zhou, Z., Miao, M., He, Y., Qing, D., Wu, T., Wang, J., Weng, X., Ferber, J. R., Herrinton, L. J., et al. (2010) · Journal of Andrology · doi:10.2164/jandrol.110.010413 · Cited by 128 · see citing works
Gestational exposure to bisphenol A and cross-fostering affect behaviors in juvenile mice.
Cox, K. H., Gatewood, J. D., Howeth, C., & Rissman, E. F. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.07.008 · Cited by 127 · see citing works
Behavioral Alterations in Response to Fear-Provoking Stimuli and Tranylcypromine Induced by Perinatal Exposure to Bisphenol A and Nonylphenol in Male Rats
Negishi, T., Kawasaki, K., Suzaki, S., Maeda, H., Ishii, Y., Kyuwa, S., Kuroda, Y., & Yoshikawa, Y. (2004) · Environmental Health Perspectives · doi:10.1289/ehp.6961 · Cited by 126 · see citing works
Brain Sex Differences and the Organisation of Juvenile Social Play Behaviour
Auger, A. P., & Olesen, K. M. (2009) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2009.01871.x · Cited by 142 · see citing works
Melatonin ameliorates bisphenol A-induced DNA damage in the germ cells of adult male rats
Wu, H., Liu, C., Duan, W., Xu, S., He, M., Chen, C., Wang, Y., Zhou, Z., Yu, Z., Zhang, L., et al. (2013) · Mutation Research/Genetic Toxicology and Environmental Mutagenesis · doi:10.1016/j.mrgentox.2013.01.005 · Cited by 121 · see citing works
Bisphenol A and phthalate endocrine disruption of parental and social behaviors
Rosenfeld, C. S. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00057 · Cited by 119 · see citing works
Evaluation of Prenatal Exposure to Bisphenol Analogues on Development and Long-Term Health of the Mammary Gland in Female Mice
Tucker, D. K., Bouknight, S. H., Brar, S. S., Kissling, G. E., & Fenton, S. E. (2018) · Environmental Health Perspectives · doi:10.1289/ehp3189 · Cited by 117 · see citing works
Altered profiles of spontaneous novelty seeking, impulsive behavior, and response to D-amphetamine in rats perinatally exposed to bisphenol A.
Adriani, W., Seta, D. D., Dessì‐Fulgheri, F., Farabollini, F., & Giovanni Laviola, A. (2002) · Environmental Health Perspectives · doi:10.1289/ehp.5856 · Cited by 117 · see citing works
Self-citation
Early exposure to a low dose of bisphenol A affects socio-sexual behavior of juvenile female rats
Porrini, S., Belloni, V., Seta, D. D., Farabollini, F., Giannelli, G., & Dessì-Fulgheri, F. (2005) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2004.11.014 · Cited by 114 · see citing works
Self-citation
Bisphenol A in relation to behavior and learning of school‐age children
Hong, S., Hong, Y., Kim, J., Park, E. J., Shin, M., Kim, B., Yoo, H., Cho, I., Bhang, S., & Cho, S.-C. (2013) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.12050 · Cited by 111 · see citing works
Bisphenol A: developmental toxicity from early prenatal exposurea
Golub, M. S., Wu, K. L., Kaufman, F. L., Li, L., Moran, F. M., Zeise, L. A., Alexeeff, G. V., & Donald, J. M. (2010) · Birth Defects Research Part B Developmental and Reproductive Toxicology · doi:10.1002/bdrb.20275 · Cited by 106 · see citing works
Melatonin protects oocyte quality from Bisphenol A‐induced deterioration in the mouse
Zhang, M., Dai, X., Lu, Y., Miao, Y., Zhou, C., Cui, Z., Liu, H., & Xiong, B. (2017) · Journal of Pineal Research · doi:10.1111/jpi.12396 · Cited by 105 · see citing works
Bisphenol A interferes with synaptic remodeling
Hajszan, T., & Leranth, C. (2010) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2010.06.004 · Cited by 101 · see citing works
Prenatal maternal and childhood bisphenol a exposure and brain structure and behavior of young children
the APrON Study Team, Grohs, M. N., Reynolds, J. E., Liu, J., Martin, J. W., Pollock, T., Lebel, C. A., & Dewey, D. (2019) · Environmental Health · doi:10.1186/s12940-019-0528-9 · Cited by 100 · see citing works
Genotoxicity and reproductive toxicity of bisphenol A and X-ray/bisphenol A combination in male mice
Dobrzyńska, M. M., & Radzikowska, J. (2012) · Drug and Chemical Toxicology · doi:10.3109/01480545.2011.644561 · Cited by 98 · see citing works
Bisphenol A Interaction With Brain Development and Functions
Negri‐Cesi, P. (2015) · Dose-Response · doi:10.1177/1559325815590394 · Cited by 89 · see citing works
Pubertal exposure to estrogenic chemicals affects behavior in juvenile and adult male rats
Della Seta, D., Minder, I., Belloni, V., Aloisi, A. M., Dessì-Fulgheri, F., & Farabollini, F. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.03.015 · Cited by 86 · see citing works
Self-citation
Effect of Neonatal Rat Bisphenol a Exposure on Performance in the Morris Water Maze
Carr, R. L., Bertasi, F., Betancourt, A. M., Bowers, S. D., Gandy, B. S., Ryan, P. L., & Willard, S. T. (2003) · Journal of Toxicology and Environmental Health Part A · doi:10.1080/713853983 · Cited by 85 · see citing works
Sex differences in the adult HPA axis and affective behaviors are altered by perinatal exposure to a low dose of bisphenol A.
Chen, F., Zhou, L.-B., Bai, Y., Zhou, R., & Chen, L. (2014) · Brain Research · doi:10.1016/j.brainres.2014.05.010 · Cited by 78 · see citing works
Influence of endocrine active compounds on the developing rodent brain
Patisaul, H. B., & Polston, E. K. (2008) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.06.008 · Cited by 81 · see citing works
Preconception paternal bisphenol A exposure induces sex-specific anxiety and depression behaviors in adult rats
Fan, Y., Tian, C., Liu, Q., Zhen, X., Zhang, H., Zhou, L., Li, T., Zhang, Y., Ding, S., Dong-liang, H., et al. (2018) · PLoS ONE · doi:10.1371/journal.pone.0192434 · Cited by 78 · see citing works
Estrogenic involvement in social learning, social recognition and pathogen avoidance
Choleris, E., Clipperton‐Allen, A. E., Phan, A., Valsecchi, P., & Kavaliers, M. (2012) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2012.02.001 · Cited by 77 · see citing works
Early exposure to low doses of atrazine affects behavior in juvenile and adult CD1 mice
Belloni, V., Dessì-Fulgheri, F., Zaccaroni, M., Di Consiglio, E., De Angelis, G., Testai, E., Santochirico, M., Alleva, E., & Santucci, D. (2011) · Toxicology · doi:10.1016/j.tox.2010.07.002 · Cited by 74 · see citing works
Self-citation
Effect of Bisphenol A on human health and its degradation by microorganisms: a review
Chouhan, S., Yadav, S. K., Prakash, J., Swati, & Singh, S. P. (2013) · Annals of Microbiology · doi:10.1007/s13213-013-0649-2 · Cited by 75 · see citing works
Two-hit exposure to polychlorinated biphenyls at gestational and juvenile life stages: 1. Sexually dimorphic effects on social and anxiety-like behaviors
Bell, M. R., Thompson, L. M., Rodriguez, K. M., & Gore, A. C. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.11.007 · Cited by 74 · see citing works
Developmental Effects of Prenatal Exposure to Bisphenol A on the Uterus of Rat Offspring
Schönfelder, G., Friedrich, K., Paul, M., & Chahoud, I. (2004) · Neoplasia · doi:10.1593/neo.04217 · Cited by 73 · see citing works
Effects of xenoestrogens on the differentiation of behaviorally-relevant neural circuits
Panzica, G., Viglietti‐Panzica, C., Mura, E., Quinn, M. J., Lavoie, E. T., Palanza, P., & Ottinger, M. A. (2007) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2007.07.001 · Cited by 73 · see citing works
Bisphenol A Prevents the Synaptogenic Response to Testosterone in the Brain of Adult Male Rats
Leranth, C., Szigeti‐Buck, K., MacLusky, N. J., & Hajszán, T. (2007) · Endocrinology · doi:10.1210/en.2007-1053 · Cited by 70 · see citing works
Estrogenic chemicals at puberty change ERα in the hypothalamus of male and female rats
Ceccarelli, I., Seta, D. D., Fiorenzani, P., Farabollini, F., & Aloisi, A. M. (2006) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2006.10.011 · Cited by 70 · see citing works
Self-citation
Neurobehavioral toxicity study of dibutyl phthalate on rats following in utero and lactational exposure
Li, Y., Zhuang, M., Li, T., & Shi, N. (2009) · Journal of Applied Toxicology · doi:10.1002/jat.1447 · Cited by 71 · see citing works
Pubertal exposure to di-(2-ethylhexyl) phthalate influences social behavior and dopamine receptor D2 of adult female mice
Wang, R., Xu, X., & Zhu, Q. (2015) · Chemosphere · doi:10.1016/j.chemosphere.2015.10.062 · Cited by 69 · see citing works
Perinatal exposure to bisphenol-A inhibits synaptogenesis and affects the synaptic morphological development in offspring male mice
Xu, X., Xie, L., Hong, X., Ruan, Q., Lü, H., Zhang, Q., Zhang, G., & Liu, X. (2013) · Chemosphere · doi:10.1016/j.chemosphere.2012.12.065 · Cited by 68 · see citing works
Estrogen and environmental estrogenic chemicals exert developmental effects on rat hypothalamic neurons and glias
Yokosuka, M., Ohtani-Kaneko, R., Yamashita, K., Muraoka, D., Kuroda, Y., & Watanabe, C. (2008) · Toxicology in Vitro · doi:10.1016/j.tiv.2007.07.003 · Cited by 62 · see citing works
Mice exposed to bisphenol A exhibit depressive-like behavior with neurotransmitter and neuroactive steroid dysfunction
Xin, F., Fischer, E., Krapp, C. J., Krizman, E. N., Lan, Y., Mesaros, C., Snyder, N. W., Bansal, A., Robinson, M. B., Simmons, R. A., et al. (2018) · Hormones and Behavior · doi:10.1016/j.yhbeh.2018.05.010 · Cited by 61 · see citing works
Sex-biased impact of endocrine disrupting chemicals on behavioral development and vulnerability to disease: Of mice and children
Palanza, P., Paterlini, S., Brambilla, M., Ramundo, G., Caviola, G., Gioiosa, L., Parmigiani, S., Saal, F. S. V., & Ponzi, D. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.11.015 · Cited by 59 · see citing works
Developmental and metabolic brain alterations in rats exposed to bisphenol A during gestation and lactation
Kunz, N., Camm, E. J., Somm, E., Lodygensky, G. A., Darbre, S., Aubert, M. L., Hüppi, P. S., Sizonenko, S. V., & Rolf Gruetter, A. (2010) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2010.09.009 · Cited by 59 · see citing works
Effects of perinatal exposure to bisphenol A on the behavior of offspring in F344 rats
Negishi, T., Kawasaki, K., Takatori, A., Ishii, Y., Kyuwa, S., Kuroda, Y., & Yoshikawa, Y. (2003) · Environmental Toxicology and Pharmacology · doi:10.1016/s1382-6689(03)00044-9 · Cited by 57 · see citing works
Influence of the presence of heavy metals and surface-active compounds on the sorption of bisphenol A to sediment
Li, J., Zhou, B., Shao, J., Yang, Q., Liu, Y., & Cai, W. (2007) · Chemosphere · doi:10.1016/j.chemosphere.2007.01.045 · Cited by 57 · see citing works
Implications for human health of the extensive bisphenol A literature showing adverse effects at low doses: A response to attempts to mislead the public
Saal, F. S. V., Nagel, S. C., Timms, B. G., & Welshons, W. V. (2005) · Toxicology · doi:10.1016/j.tox.2005.05.006 · Cited by 55 · see citing works
Early exposure to bisphenol A alters neuron and glia number in the rat prefrontal cortex of adult males, but not females
Sadowski, R. N., Wise, L. M., Park, P. Y., Schantz, S. L., & Juraska, J. M. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.08.038 · Cited by 54 · see citing works
Changes in estrogen receptors α and β expression in the brain of mice exposed prenatally to bisphenol A
Kawai, K., Murakami, S., Senba, E., Yamanaka, T., Fujiwara, Y., Arimura, C., Nozaki, T., Takii, M., & Kubo, C. (2007) · Regulatory Toxicology and Pharmacology · doi:10.1016/j.yrtph.2006.04.002 · Cited by 53 · see citing works
Building a scientific framework for studying hormonal effects on behavior and on the development of the sexually dimorphic nervous system
Li, A. A., Baum, M. J., McIntosh, L. J., Day, M., Liu, F., & Gray, L. E. (2008) · NeuroToxicology · doi:10.1016/j.neuro.2008.02.015 · Cited by 51 · see citing works
Bisphenol-A rapidly promotes dynamic changes in hippocampal dendritic morphology through estrogen receptor-mediated pathway by concomitant phosphorylation of NMDA receptor subunit NR2B
Xu, X., Ye, Y., Li, T., Chen, L., Dong, T., Luo, Q., & Lü, M. (2010) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2010.09.007 · Cited by 51 · see citing works
Exposure to bisphenol-A affects fear memory and histone acetylation of the hippocampus in adult mice
Zhang, Q., Xu, X., Li, T., Lu, Y., Ruan, Q., Lu, Y., Wang, Q., Dong, F., Yang, Y., & Zhang, G. (2014) · Hormones and Behavior · doi:10.1016/j.yhbeh.2013.12.004 · Cited by 51 · see citing works
The degradation of alkylphenols by Sphingomonas sp. strain TTNP3 – a review on seven years of research
Kolvenbach, B. A., & Corvini, P. F.-X. (2012) · New Biotechnology · doi:10.1016/j.nbt.2012.07.008 · Cited by 50 · see citing works
The influence of study design and sex-differences on results from developmental neurotoxicity studies of bisphenol A, implications for toxicity testing
Beronius, A., Johansson, N., Rudén, C., & Hanberg, A. (2013) · Toxicology · doi:10.1016/j.tox.2013.02.012 · Cited by 50 · see citing works
Pubertal exposure to bisphenol A disrupts behavior in adult C57BL/6J mice
Yu, C., Tai, F., Song, Z., Wu, R., Zhang, X., & He, F. (2010) · Environmental Toxicology and Pharmacology · doi:10.1016/j.etap.2010.09.009 · Cited by 48 · see citing works
Early developmental exposure to bisphenol A and bisphenol S disrupts socio-cognitive function, isotocin equilibrium, and excitation-inhibition balance in developing zebrafish
Naderi, M., Puar, P., JavadiEsfahani, R., & Kwong, R. W. M. (2021) · NeuroToxicology · doi:10.1016/j.neuro.2021.11.009 · Cited by 47 · see citing works
Inhibition of staurosporine-induced neuronal cell death by bisphenol A and nonylphenol in primary cultured rat hippocampal and cortical neurons
Negishi, T., Ishii, Y., Kyuwa, S., Kuroda, Y., & Yoshikawa, Y. (2003) · Neuroscience Letters · doi:10.1016/j.neulet.2003.09.031 · Cited by 42 · see citing works
When Disaster Strikes: Rethinking Caging Materials
Koehler, K. E., Voigt, R. C., Thomas, S., Lamb, B. T., Urban, C., Hassold, T. J., & Hunt, P. A. (2003) · Lab Animal · doi:10.1038/laban0403-24 · Cited by 39 · see citing works
Non‐genomic modulation of dopamine release by bisphenol‐A in PC12 cells
Yoneda, T., Hiroi, T., Osada, M., Asada, A., & Funae, Y. (2003) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2003.02131.x · Cited by 37 · see citing works
The “Low Dose” Hypothesis: Validity and Implications for Human Risk
Kamrin, M. A. (2007) · International Journal of Toxicology · doi:10.1080/10915810601117968 · Cited by 36 · see citing works
Bisphenol A and cognitive function in school-age boys: Is BPA predominantly related to behavior?
Rodríguez‐Carrillo, A., Mustieles, V., Pérez‐Lobato, R., Molina-Molina, J.-M., Reina-Pérez, I., Vela-Soria, F., Rubio, S., Olea, N., & Fernández, M. F. (2019) · NeuroToxicology · doi:10.1016/j.neuro.2019.06.006 · Cited by 35 · see citing works
Developmental origins of sex differences in the neural circuitry of play
VanRyzin, J. W., Marquardt, A. E., & McCarthy, M. M. (2020) · International Journal of Play · doi:10.1080/21594937.2020.1723370 · Cited by 34 · see citing works
The Effects of Low-Dose Bisphenol A and Bisphenol F on Neural Differentiation of a Fetal Brain-Derived Neural Progenitor Cell Line
Fujiwara, Y., Miyazaki, W., Koibuchi, N., & Katoh, T. (2018) · Frontiers in Endocrinology · doi:10.3389/fendo.2018.00024 · Cited by 34 · see citing works
Effects of maternal or paternal bisphenol A exposure on offspring behavior
Harris, E. P., Allardice, H. A., Schenk, A. K., & Rissman, E. F. (2018) · Hormones and Behavior · doi:10.1016/j.yhbeh.2017.09.017 · Cited by 33 · see citing works
Developmental Treatment with Ethinyl Estradiol, but Not Bisphenol A, Causes Alterations in Sexually Dimorphic Behaviors in Male and Female Sprague Dawley Rats
Ferguson, S. A., Law, C. D., & Kissling, G. E. (2014) · Toxicological Sciences · doi:10.1093/toxsci/kfu077 · Cited by 32 · see citing works
“The same lab had earlier reported BPA-induced masculinization of females when behavior was analyzed from minutes 2 and 3 only of a 7-min test session (Dessi-Fulgheri et al., 2002).”
Background
Review of the Effects of Perinatal Exposure to Endocrine-Disrupting Chemicals in Animals and Humans
Nelson, W., Wang, Y., Sakwari, G. H., & Ding, Y. (2019) · Reviews of Environmental Contamination and Toxicology · doi:10.1007/398_2019_30 · Cited by 32 · see citing works
Early-Life Exposure to a Mixture of Phenols and Phthalates in Relation to Child Social Behavior: Applying an Evidence-Based Prioritization to a Cohort with Improved Exposure Assessment
Mustieles, V., Rolland, M., Pin, I., Thomsen, C., Sakhi, A. K., Sabaredzovic, A., Muckle, G., Guichardet, K., Slama, R., & Philippat, C. (2023) · Environmental Health Perspectives · doi:10.1289/ehp11798 · Cited by 32 · see citing works
Perinatal exposure to low-dose bisphenol A disrupts learning/memory and DNA methylation of estrogen receptor alpha in the hippocampus
Chang, H., Wang, M., Xia, W., Chen, T., Huo, W., Mao, Z., Zhu, Y., Li, Y., & Xu, S. (2016) · Toxicology Research · doi:10.1039/c5tx00449g · Cited by 31 · see citing works
In vitro effects of bisphenol A on developing hypothalamic neurons
Iwakura, T., Iwafuchi, M., Muraoka, D., Yokosuka, M., Shiga, T., Watanabe, C., & Ohtani‐Kaneko, R. (2010) · Toxicology · doi:10.1016/j.tox.2010.04.005 · Cited by 27 · see citing works
The effects of pubertal exposure to bisphenol-A on social behavior in male mice
Gao, T., Yin, Z., Wang, M., Fang, Z., Zhong, X., Li, J., Hu, Y., Wu, D., Jiang, K., & Xu, X. (2019) · Chemosphere · doi:10.1016/j.chemosphere.2019.125494 · Cited by 27 · see citing works
Effects of early pubertal exposure to di-(2-ethylhexyl) phthalate on social behavior of mice
Wang, R., Xu, X., Weng, H., Yan, S., & Sun, Y. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2016.01.012 · Cited by 25 · see citing works
Bisphenol A depresses compound action potential of frog sciatic nerve in vitro involving Ca2+-dependent mechanisms
Pandey, A. K., & Deshpande, S. B. (2012) · Neuroscience Letters · doi:10.1016/j.neulet.2012.04.044 · Cited by 24 · see citing works
Chronic exposure to low doses bisphenol A interferes with pair-bonding and exploration in female Mongolian gerbils
Razzoli, M., Valsecchi, P., & Palanza, P. (2004) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2004.11.013 · Cited by 24 · see citing works
Endocrine-disrupting chemicals and behaviour: A high risk to take?
Bakoyiannis, I., Kitraki, E., & Stamatakis, A. (2021) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2021.101517 · Cited by 23 · see citing works
Level of Bisphenol A in Follicular Fluid and Serum and Oocyte Morphology in Patients Undergoing IVF Treatment
Poormoosavi, S. M., Behmanesh, M. A., Janati, S., & Najafzadehvarzi, H. (2019) · Journal of Family & Reproductive Health · doi:10.18502/jfrh.v13i3.2129 · Cited by 23 · see citing works
Effects of prenatal chlordecone on sexually differentiated behavior in adult rats
Laessig, S. A., Auger, A. P., McCarthy, M. M., & Silbergeld, E. K. (2006) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2006.10.003 · Cited by 23 · see citing works
Effects of perinatal daidzein exposure on subsequent behavior and central estrogen receptor α expression in the adult male mouse.
Yu, C.-J., Tai, F.-D., Zeng, S., & Zhang, X. (2013) · Progress in Neuro-psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2012.12.015 · Cited by 20 · see citing works

Endocrine Disruptors Effects of Perinatal Exposure to Bisphenol A on Play Behavior of Female and Male Juvenile Rats
Dessì‐Fulgheri, F., Porrini, S., & Farabollini, F. (2013)
Self-citation
Early exposure to a low dose of bisphenol A affects socio-sexual behavior of juvenile female rats
Porrini, S., Belloni, V., Seta, D. D., Farabollini, F., Giannelli, G., & Dessì-Fulgheri, F. (2005) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2004.11.014 · Cited by 114 · see citing works
Self-citation
Perinatal Exposure to the Estrogenic Pollutant Bisphenol A Affects Behavior in Male and Female Rats
Farabollini, F. (1999) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(99)00136-7 · Cited by 183 · see citing works
Self-citation
Effects of perinatal exposure to bisphenol A on sociosexual behavior of female and male rats.
Farabollini, F., Porrini, S., Seta, D. D., Bianchi-Jassir, F., & Dessì‐Fulgheri, F. (2002) · Environmental Health Perspectives · doi:10.1289/ehp.02110s3409 · Cited by 204 · see citing works
Self-citation
Endocrine Disruptors Effects of Perinatal Exposure to Bisphenol A on Sociosexual Behavior of Female and Male Rats
Farabollini, F., Porrini, S., Seta, D. D., Bianchi, F., & Dessì‐Fulgheri, F. (2013)
Self-citation

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)
DOI: 10.1289/ehp.02110s3403
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
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Sexual Differentiation and Disorders
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › 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

Effects of Perinatal Exposure to Bisphenol A on Play Behavior of Female and Male Juvenile Rats

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks