Evaluation of Developmental Toxicity, Developmental Neurotoxicity, and Tissue Dose in Zebrafish Exposed to GenX and Other PFAS

Gaballah, Shaza; Swank, Adam; Sobus, Jon R.; Howey, Xia Meng; Schmid, Judith; Catron, Tara; McCord, James; Hines, Erin; Strynar, Mark; Tal, Tamara

doi:10.1289/ehp5843

Cited by 437Per- and polyfluoroalkyl substances researchZebrafish Biomedical Research ApplicationsToxic Organic Pollutants Impact

Evaluation of Developmental Toxicity, Developmental Neurotoxicity, and Tissue Dose in Zebrafish Exposed to GenX and Other PFAS

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Gaballah, Shaza, Swank, Adam, Sobus, Jon R., Howey, Xia Meng, Schmid, Judith, Catron, Tara, McCord, James, Hines, Erin +2 more·2020·Environmental Health Perspectives

DOI 10.1289/ehp5843PMC PMC7228129

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Abstract

BACKGROUND: Per-and polyfluoroalkyl substances (PFAS) are a diverse class of industrial chemicals with widespread environmental occurrence.Exposure to long-chain PFAS is associated with developmental toxicity, prompting their replacement with short-chain and fluoroether compounds.There is growing public concern over the safety of replacement PFAS.OBJECTIVE: We aimed to group PFAS based on shared toxicity phenotypes.METHODS: Zebrafish were developmentally exposed to 4,8-dioxa-3H-perfluorononanoate (ADONA), perfluoro-2-propoxypropanoic acid (GenX Free Acid), perfluoro-3,6-dioxa-4-methyl-7-octene-1-sulfonic acid (PFESA1), perfluorohexanesulfonic acid (PFHxS), perfluorohexanoic acid (PFHxA), perfluoro-n-octanoic acid (PFOA), perfluorooctanesulfonic acid (PFOS), or 0.4% dimethyl sulfoxide (DMSO) daily from 0-5 d post fertilization (dpf).At 6 dpf, developmental toxicity and developmental neurotoxicity assays were performed, and targeted analytical chemistry was used to measure media and tissue doses.To test whether aliphatic sulfonic acid PFAS cause the same toxicity phenotypes, perfluorobutanesulfonic acid (PFBS; 4-carbon), perfluoropentanesulfonic acid (PFPeS; 5-carbon), PFHxS (6-carbon), perfluoroheptanesulfonic acid (PFHpS; 7-carbon), and PFOS (8-carbon) were evaluated.RESULTS: PFHxS or PFOS exposure caused failed swim bladder inflation, abnormal ventroflexion of the tail, and hyperactivity at nonteratogenic concentrations.Exposure to PFHxA resulted in a unique hyperactivity signature.ADONA, PFESA1, or PFOA exposure resulted in detectable levels of parent compound in larval tissue but yielded negative toxicity results.GenX was unstable in DMSO, but stable and negative for toxicity when diluted in deionized water.Exposure to PFPeS, PFHxS, PFHpS, or PFOS resulted in a shared toxicity phenotype characterized by body axis and swim bladder defects and hyperactivity.CONCLUSIONS: All emerging fluoroether PFAS tested were negative for evaluated outcomes.Two unique toxicity signatures were identified arising from structurally dissimilar PFAS.Among sulfonic acid aliphatic PFAS, chemical potencies were correlated with increasing carbon chain length for developmental neurotoxicity, but not developmental toxicity.This study identified relationships between chemical structures and in vivo phenotypes that may arise from shared mechanisms of PFAS toxicity.These data suggest that developmental neurotoxicity is an important end point to consider for this class of widely occurring environmental chemicals.

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Several studies assessing PFOS exposure in larval zebrafish reported increased swimming speed or hyperactivity in PFOS-exposed adults.
“Several studies assessing PFOS exposure in larval zebrafish reported increased swimming speed or hyperactivity in PFOS-exposed adults (Huang et al., 2010; Chen et al., 2013; Gaballah et al., 2020).”
From A Critical Review and Meta-Analysis of Impacts of Per- and Polyfluorinated Substances on the Brain and Behavior (2022) · cites this paper as Gaballah et al., 2020
The Results section reports hyperactivity after PFOS exposure from 0–5 days post-fertilization, but locomotor activity was measured in larvae at 6 days, not in adults. The Discussion asks whether the effect persists in older animals and mentions a separate study of 14-day-old zebrafish; it does not report hyperactivity in PFOS-exposed adults. Page numbers were not provided in the passages. (LLM, conf=0.91)
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Gaballah et al. (2020) found that concentrations as low as 0.6 μM PFOS and 3.1 μM PFHpS caused hyperactivity in zebrafish, but concentrations up to 80 μM of PFOA, PFESA-1 or ADONA caused no observed neurotoxicological impact.
“Gaballah et al. (2020) found that concentrations as low as 0.6 µM PFOS and 3.1 µM perfluoroheptanesulfonic acid (PFHpS) caused hyperactivity in zebrafish, but concentrations up to 80 µM of PFOA, perfluoro-3,6-dioxa-4-methyl-7-octenesulfonic acid (PFESA-1) or 4,8-dioxa-3H-perfluorononanoate (ADONA) caused no observed neurotoxicological impact.”
From A Critical Review and Meta-Analysis of Impacts of Per- and Polyfluorinated Substances on the Brain and Behavior (2022) · cites this paper as Gaballah et al., 2020
PFHxS exposure at concentrations as low as 4.4 μM induced hyperactivity in zebrafish in a light-dark assay, in addition to 14 μM PFHxA and 3.1 μM PFPeS, however no effect to locomotor activity was observed with 100 μM PFBS exposure.
“PFHxS exposure at concentrations as low as 4.4 µM also induced hyperactivity in zebrafish in a light-dark assay, in addition to 14 µM PFHxA and 3.1 µM perfluropentanesulfonic acid (PFPeS), however no effect to locomotor activity was observed with 100 µM PFBS exposure (Gaballah et al., 2020).”
From A Critical Review and Meta-Analysis of Impacts of Per- and Polyfluorinated Substances on the Brain and Behavior (2022) · cites this paper as Gaballah et al., 2020
PFAS have garnered attention as highly persistent and toxic environmental contaminants.
“per- and polyfluoroalkyl substances (PFAS) have garnered attention as highly persistent12 and toxic13,14 environmental contaminants.”
From Per- and Polyfluoroalkyl Substances (PFAS) in Street Sweepings (2022) · cites this paper as [14]
Alternative substances, like short-chain PFAS and fluoroether compounds, took the place of PFOA and PFOS and are still widely used.
“alternative substances, like short-chain PFAS and fluoroether compounds, took their place and are still widely used”
From Evaluation of per- and polyfluoroalkyl substances (PFAS) in leachate, gas condensate, stormwater and groundwater at landfills (2023) · cites this paper as Gaballah et al., 2020

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Spulber, S., Kilian, P., Wan Ibrahim, W. N., Onishchenko, N., Ulhaq, M., Norrgren, L., Negri, S., Di Tuccio, M., & Ceccatelli, S. (2014) · PLoS ONE · doi:10.1371/journal.pone.0094227 · Cited by 98 · cited 5× · see citing works
“…tail (Hagenaars et al. 2011; Huang et al. 2010; Jantzen et al. 2016; Ulhaq et al. 2013a), and hyperactivity (Hurley et al. 2018; Khezri et al. 2017; Spulber et al. 2014), whereas results for PFOA exposures are quite mixed for both developmental toxicity and behavior (Hagenaars et al. 2011; Huang…”
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Perflurooctanoic acid induces developmental cardiotoxicity in chicken embryos and hatchlings.
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Effects of subchronic perfluorooctane sulfonate exposure of rats on calcium-dependent signaling molecules in the brain tissue
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A Mixture of Persistent Organic Pollutants and Perfluorooctanesulfonic Acid Induces Similar Behavioural Responses, but Different Gene Expression Profiles in Zebrafish Larvae
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Swimbladder Permeability to Oxygen
Lapennas, G. N., & Schmidt‐Nielsen, K. (1977) · Journal of Experimental Biology · doi:10.1242/jeb.67.1.175 · Cited by 45 · see citing works
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Gestational Exposure to Perfluorooctanoic Acid (PFOA): Alterations in Motor Related Behaviors
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Prenatal exposure to perfluorooctanesulfonate in rat resulted in long‐lasting changes of expression of synapsins and synaptophysin
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“Several studies assessing PFOS exposure in larval zebrafish reported increased swimming speed or hyperactivity in PFOSexposed adults (Huang et al., 2010; Chen et al., 2013; Gaballah et al., 2020).”
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Authors: Gaballah, S., Swank, A., Sobus, J. R., Howey, X. M., Schmid, J., Catron, T., McCord, J., Hines, E., Strynar, M., & Tal, T.
Affiliations: Environmental Protection Agency (US)
Corresponding author: Tal, Tamara
ORCID: Gaballah, Shaza
Sobus, Jon R.
Catron, Tara
McCord, James
Hines, Erin
Strynar, Mark
Tal, Tamara
Venue: Environmental Health Perspectives
Publisher: American Chemical Society (ACS)
Published: 2020-04
Volume: 128
Issue: 4
Pages: 47005-47005
ISSN: 0091-6765 (ISSN-L)
1552-9924
DOI: 10.1289/ehp5843
PMC: PMC7228129
OpenAlex: W3016124517
Cited by: 437
References: 104
Citations by year: 2026: 64 · 2025: 97 · 2024: 81 · 2023: 76 · 2022: 71 · 2021: 35 · 2020: 13
FWCI: 18.17
Type: journal article
Language: en
Open access: gold
doi.org
Licence: public-domain
Locations: Environmental Health Perspectives (publishedVersion, public-domain)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: U.S. Environmental Protection Agency
Office of Research and Development
Topics: Physical Sciences › Environmental Science › Environmental Chemistry › Per- and polyfluoroalkyl substances research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Zebrafish Biomedical Research Applications
Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Toxic Organic Pollutants Impact
Keywords: perfluorinated compounds, GenX, developmental toxicity, developmental neurotoxicity, hyperactivity, tissue dose, PFHxS, PFOS, ADONA, zebrafish embryonic development
MeSH terms: Animals, Dose-Response Relationship, Drug, Fluorocarbons, Neurotoxins, Propionates, Tissue Distribution, Water Pollutants, Chemical, Zebrafish

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Evaluation of Developmental Toxicity, Developmental Neurotoxicity, and Tissue Dose in Zebrafish Exposed to GenX and Other PFAS

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