Neonatal Exposure to Perfluorooctane Sulfonate (PFOS) and Perfluorooctanoic Acid (PFOA) Causes Neurobehavioural Defects in Adult Mice

Johansson, N.; Fredriksson, A.; Eriksson, P.

doi:10.1016/j.neuro.2007.10.008

Cited by 463Per- and polyfluoroalkyl substances researchToxic Organic Pollutants ImpactPesticide Exposure and Toxicity

Neonatal Exposure to Perfluorooctane Sulfonate (PFOS) and Perfluorooctanoic Acid (PFOA) Causes Neurobehavioural Defects in Adult Mice

Johansson, N., Fredriksson, A., Eriksson, P.·2008·NeuroToxicology

DOI 10.1016/j.neuro.2007.10.008

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Abstract

Perfluorinated compounds (PFCs) are found in applications such oil/water repellents for clothing fabrics, carpets, food packaging, lubricants, surfactants and fire extinguishers. PFCs are persistent in the environment. They have been found in humans and in wildlife. We reported earlier that persistent organic pollutants (POPs), such as DDT, PCBs and BFRs, caused developmental neurotoxic defects in mice, manifested as persistent aberrations in spontaneous behaviour, habituation capability, learning and memory, and changes in the cholinergic system in adults, when mice were exposed during a critical period of neonatal brain development. The present study was conducted to see whether PFCs can cause similar developmental neurotoxic effects as earlier observed for POPs as PCBs and PBDEs. NMRI male mice were exposed to a single-oral dose, either 1.4 or 21 micromol/kg body weight of PFOS (0.75 or 11.3 mg), PFOA (0.58 or 8.70 mg), or PFDA (0.72 or 10.8 mg), via a metal gastric-tube at the age of 10 days. The control animals received in the same manner 10 ml/kg body weight of the 20% fat emulsion vehicle. Spontaneous behaviour (locomotion, rearing, and total activity), and habituation were observed in 2- and 4-month-old mice. The susceptibility of the cholinergic system was explored in a nicotine-induced spontaneous behaviour test in 4-month-old mice. Deranged spontaneous behaviour was observed in mice exposed to PFOS and PFOA, manifested as reduced and/or lack of habituation and hyperactivity in adult mice. These effects were also seen to worse with age. Neonatal exposure to PFOS and PFOA affected the cholinergic system, manifested as a hypoactive response to nicotine, compared to a hyperactive response to nicotine in controls. These developmental neurotoxic effects are similar to those we reported earlier for PCBs and PBDEs. This suggests that PFOS and PFOA be included in the group of POPs known to be developmental neurotoxicants.

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Decreased habituation was observed in mice after exposure to 8.7 mg/kg PFOA or 11.3 mg/kg PFOS, whereas altered spontaneous behavior was observed after exposure to 0.58 mg/kg PFOA or 0.75 mg/kg PFOS.
“Decreased habituation was observed in the mice after exposure to 8.7 mg/kg PFOA or 11.3 mg/kg PFOS, whereas altered spontaneous behavior was observed after exposure to 0.58 mg/kg PFOA or 0.75 mg/kg PFOS (Johansson et al., 2008; Hallgren et al., 2015).”
From A Critical Review and Meta-Analysis of Impacts of Per- and Polyfluorinated Substances on the Brain and Behavior (2022) · cites this paper as Johansson et al., 2008
While concentrations of PFAS measured in adult tissues were often low following developmental exposure, those exposures still caused neurobehavioral toxicity persisting into adulthood.
“While concentrations of PFAS measured in adult tissues were often low following developmental exposure, those exposures still caused neurobehavioral toxicity persisting into adulthood (Johansson et al., 2008; Chen et al., 2013).”
From A Critical Review and Meta-Analysis of Impacts of Per- and Polyfluorinated Substances on the Brain and Behavior (2022) · cites this paper as Johansson et al., 2008
While studies on PFAS exposure in adult animals have not reported altered motor activity, several compounds have been shown to elicit developmental impairment of motor activity in mice, rats, and zebrafish.
“While studies on PFAS exposure in adult animals have not reported altered motor activity, several compounds have been shown to elicit developmental impairment of motor activity in mice, rats, and zebrafish (Johansson et al., 2008; Butenhoff et al., 2009b; Huang et al., 2010; Wang M. et al., 2011; Chen et al., 2013; Spulber et al., 2014; Hallgren et al., 2015; Goulding et al., 2017; Guo et al., 201”
From A Critical Review and Meta-Analysis of Impacts of Per- and Polyfluorinated Substances on the Brain and Behavior (2022) · cites this paper as Johansson et al., 2008
In inbred male NMRI mice, a single oral exposure of PFOA or PFOS at PND 10 caused a long-lasting hyperactive phenotype at 2 and 4 months of age, characterized by decreased habituation and altered spontaneous behavior.
“In inbred male NMRI mice, a single oral exposure of PFOA or PFOS at PND 10 caused a long-lasting hyperactive phenotype at 2 and 4 months of age, characterized by decreased habituation and altered spontaneous behavior (Johansson et al., 2008; Hallgren et al., 2015).”
From A Critical Review and Meta-Analysis of Impacts of Per- and Polyfluorinated Substances on the Brain and Behavior (2022) · cites this paper as Johansson et al., 2008

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A review of the pathways of human exposure to poly- and perfluoroalkyl substances (PFASs) and present understanding of health effects
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Effects of perfluorooctane sulfonate on rat thyroid hormone biosynthesis and metabolism
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Prenatal Exposure to Perfluorooctanoate (PFOA) and Perfluorooctanesulfonate (PFOS) and Maternally Reported Developmental Milestones in Infancy
Fei, C., McLaughlin, J. K., Lipworth, L., & Olsen, J. (2008) · Environmental Health Perspectives · doi:10.1289/ehp.11277 · Cited by 169 · see citing works
A Review of Perfluoroalkyl Acids (PFAAs) in terms of Sources, Applications, Human Exposure, Dietary Intake, Toxicity, Legal Regulation, and Methods of Determination
Sznajder‐Katarzyńska, K., Surma, M., & Cieślik, I. (2019) · Journal of Chemistry · doi:10.1155/2019/2717528 · Cited by 172 · see citing works
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A Critical Review and Meta-Analysis of Impacts of Per- and Polyfluorinated Substances on the Brain and Behavior
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“While studies on PFAS exposure in adult animals have not reported altered motor activity, several compounds have been shown to elicit developmental impairment of motor activity in mice, rats, and zebrafish (Johansson et al., 2008; Butenhoff et al., 2009b; Huang et al., 2010; Wang M. et al., 2011; Chen et al., 2013; Sp…”
Background
Distribution of perfluorochemicals between sera and milk from the same mothers and implications for prenatal and postnatal exposures.
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Neurotransmission targets of per-and polyfluoroalkyl substance neurotoxicity: Mechanisms and potential implications for adverse neurological outcomes
Brown-Leung, J. M., & Cannon, J. R. (2022) · Chemical Research in Toxicology · doi:10.1021/acs.chemrestox.2c00072 · Cited by 164 · see citing works
Cumulative health risk assessment of 17 perfluoroalkylated and polyfluoroalkylated substances (PFASs) in the Swedish population
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Paracetamol (Acetaminophen) Administration During Neonatal Brain Development Affects Cognitive Function and Alters Its Analgesic and Anxiolytic Response in Adult Male Mice
Viberg, H., Eriksson, P., Gordh, T., & Fredriksson, A. (2013) · Toxicological Sciences · doi:10.1093/toxsci/kft329 · Cited by 158 · see citing works
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Blood serum concentrations of perfluorinated compounds in men from Greenlandic Inuit and European populations
Lindh, C. H., Rylander, L., Toft, G. V., Axmon, A., Rignell‐Hydbom, A., Giwercman, A., Pedersen, H. S., Góralczyk, K., Ludwicki, J. K., Zvyezday, V., et al. (2012) · Chemosphere · doi:10.1016/j.chemosphere.2012.03.049 · Cited by 153 · see citing works
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Behavioural effects and bioconcentration of per- and polyfluoroalkyl substances (PFASs) in zebrafish (Danio rerio) embryos
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Attention Deficit/Hyperactivity Disorder and Childhood Autism in Association with Prenatal Exposure to Perfluoroalkyl Substances: A Nested Case–Control Study in the Danish National Birth Cohort
Liew, Z., Ritz, B. R., Ehrenstein, O. S. V., Bech, B. H., Nohr, E. A., Fei, C., Bossi, R., Henriksen, T. B., Bonefeld‐Jørgensen, E. C., & Olsen, J. (2014) · Environmental Health Perspectives · doi:10.1289/ehp.1408412 · Cited by 149 · see citing works
Prenatal Exposure to PFOS or PFOA Alters Motor Function in Mice in a Sex-Related Manner
Onishchenko, N., Fischer, C., Ibrahim, W. N. W., Negri, S., Spulber, S., Cottica, D., & Ceccatelli, S. (2011) · Neurotoxicity research · doi:10.1007/s12640-010-9200-4 · Cited by 152 · see citing works
Chlorinated Polyfluorinated Ether Sulfonates Exhibit Higher Activity toward Peroxisome Proliferator-Activated Receptors Signaling Pathways than Perfluorooctanesulfonate
Li, C.-H., Ren, X., Ruan, T., Cao, L.-Y., Yan, X., Guo, L., & Jiang, G. (2018) · Environmental Science & Technology · doi:10.1021/acs.est.7b06327 · Cited by 144 · see citing works
Gestational and lactational exposure to potassium perfluorooctanesulfonate (K+PFOS) in rats: Developmental neurotoxicity
Butenhoff, J. L., Ehresman, D. J., Chang, S., Parker, G. A., & Stump, D. G. (2009) · Reproductive Toxicology · doi:10.1016/j.reprotox.2008.12.010 · Cited by 142 · see citing works
Breast cancer risk after exposure to perfluorinated compounds in Danish women: a case–control study nested in the Danish National Birth Cohort
Bonefeld‐Jørgensen, E. C., Long, M., Fredslund, S. O., Bossi, R., & Olsen, J. (2014) · Cancer Causes & Control · doi:10.1007/s10552-014-0446-7 · Cited by 142 · see citing works
Effects of Perfluorooctanoic Acid on Metabolic Profiles in Brain and Liver of Mouse Revealed by a High-throughput Targeted Metabolomics Approach
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Current Review of Increasing Animal Health Threat of Per- and Polyfluoroalkyl Substances (PFAS): Harms, Limitations, and Alternatives to Manage Their Toxicity
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Glucose and lipid homeostasis in adult rat is impaired by early-life exposure to perfluorooctane sulfonate
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Accumulation of Perfluoroalkylated Substances in Oceanic Plankton
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Bioconcentration and Metabolic Effects of Emerging PFOS Alternatives in Developing Zebrafish
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Comparative toxicometabolomics of perfluorooctanoic acid (PFOA) and next-generation perfluoroalkyl substances
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Per- and Polyfluoroalkyl Substances in Food Packaging: Migration, Toxicity, and Management Strategies
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Prenatal Exposure to Perfluorinated Chemicals and Behavioral or Coordination Problems at Age 7 Years
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Adult Dose-dependent Behavioral and Cognitive Disturbances after a Single Neonatal PFHxS Dose
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Binding of PFOS to Serum Albumin and DNA: Insight into the Molecular Toxicity of Perfluorochemicals
Zhang, X., Chen, L., Fei, X.-C., Ma, Y.-S., & Gao, H.-W. (2009) · BMC Molecular Biology · doi:10.1186/1471-2199-10-16 · Cited by 119 · see citing works
Gestational and Lactational Exposure to Potassium Perfluorooctanesulfonate (K+PFOS) in Rats: Toxicokinetics, Thyroid Hormone Status, and Related Gene Expression
Chang, S.-C., Ehresman, D. J., Bjork, J. A., Wallace, K. B., Parker, G. A., Stump, D. G., & Butenhoff, J. L. (2009) · Reproductive Toxicology · doi:10.1016/j.reprotox.2009.01.005 · Cited by 118 · see citing works
Prenatal exposure to perfluorinated chemicals and neurodevelopment in early infancy: The Hokkaido Study
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Brain Region-specific Perfluoroalkylated Sulfonate (PFSA) and Carboxylic Acid (PFCA) Accumulation and Neurochemical Biomarker Responses in East Greenland Polar Bears (Ursus maritimus)
Eggers Pedersen, K., Basu, N., Letcher, R., Greaves, A. K., Sonne, C., Dietz, R., & Styrishave, B. (2015) · Environmental Research · doi:10.1016/j.envres.2015.01.015 · Cited by 116 · see citing works
Prenatal and childhood exposure to per- and polyfluoroalkyl substances (PFASs) and child cognition
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High-performance photocatalytic decomposition of PFOA by BiOX/TiO2 heterojunctions: Self-induced inner electric fields and band alignment
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Perfluorinated Compound Levels in Cord Blood and Neurodevelopment at 2 Years of Age
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Effects of perfluorinated compounds on development of zebrafish embryos
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Effect of surfactants on the degradation of perfluorooctanoic acid (PFOA) by ultrasonic (US) treatment
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Prenatal polybrominated diphenyl ether and perfluoroalkyl substance exposures and executive function in school-age children
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Neonatal exposure to deca-brominated diphenyl ether (PBDE 209) causes dose–response changes in spontaneous behaviour and cholinergic susceptibility in adult mice
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Prenatal Perfluorooctanoic Acid Exposure in CD-1 Mice: Low-Dose Developmental Effects and Internal Dosimetry
Macon, M. B., Villanueva, L. R., Tatum-Gibbs, K. R., ZEHR, R. D. J., Strynar, M. J., Stanko, J. P., White, S. S., Helfant, L., & Fenton, S. E. (2011) · Toxicological Sciences · doi:10.1093/toxsci/kfr076 · Cited by 110 · see citing works
Neurotoxicity of Perfluorooctane Sulfonate to Hippocampal Cells in Adult Mice
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PFAS profiles in three North Sea top predators: metabolic differences among species?
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Chronic Exposure to Perfluorooctane Sulfonate Induces Behavior Defects and Neurotoxicity through Oxidative Damages, In Vivo and In Vitro
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Self-citation
Neonatal exposure to perfluorooctane sulfonate (PFOS) and perfluorooctanoic acid (PFOA) causes deranged behaviour and increased susceptibility of the cholinergic system in adult mice
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Perfluorinated chemicals (PFOA) can, by interacting with highly brominated diphenyl ethers (PBDE 209) during a defined period of neonatal brain development, exacerbate neurobehavioural defects
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Neonatal Exposure to PFOS and PFOA in Mice Results in Changes in Proteins which are Important for Neuronal Growth and Synaptogenesis in the Developing Brain
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Self-citation

Authors: Johansson, N., Fredriksson, A., & Eriksson, P.
Affiliations: Uppsala University (SE)
Corresponding author: Eriksson, P.
ORCID: Johansson, N.
Fredriksson, A.
Eriksson, P.
Venue: NeuroToxicology
Publisher: Elsevier BV
Published: 2008-01
Volume: 29
Issue: 1
Pages: 160-169
ISSN: 0161-813X (ISSN-L)
DOI: 10.1016/j.neuro.2007.10.008
OpenAlex: W2086492898
Cited by: 463
References: 84
Citations by year: 2026: 19 · 2025: 30 · 2024: 28 · 2023: 44 · 2022: 31 · 2021: 27 · 2020: 29 · 2019: 20 · 2018: 27 · 2017: 22 · 2016: 23 · 2015: 27 · 2014: 22 · 2013: 20 · 2012: 27
FWCI: 11.10
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: NeuroToxicology (publishedVersion)
PubMed (publishedVersion)
Funders: Vetenskapsrådet
Topics: Physical Sciences › Environmental Science › Environmental Chemistry › Per- and polyfluoroalkyl substances research
Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Toxic Organic Pollutants Impact
Life Sciences › Agricultural and Biological Sciences › Plant Science › Pesticide Exposure and Toxicity
Keywords: PFOS, perfluorooctanoic acid, perfluorodecanoic acid, perfluorinated compounds, developmental neurotoxicity, neonatal exposure, persistent organic pollutants, spontaneous behavior, habituation, hyperactivity, cholinergic system, learning and memory, persistent environmental pollutants
MeSH terms: Analysis of Variance, Animals, Animals, Newborn, Behavior, Animal, Mental Disorders, Brain Diseases, Caprylates, Disease Models, Animal, Dose-Response Relationship, Drug, Exploratory Behavior, Female, Fluorocarbons, Locomotion, Male, Nicotine, Pregnancy, Time Factors, Alkanesulfonic Acids, Nicotinic Agonists, Maze Learning, Mice

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Neonatal Exposure to Perfluorooctane Sulfonate (PFOS) and Perfluorooctanoic Acid (PFOA) Causes Neurobehavioural Defects in Adult Mice

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