Determining bad actors: A linear mixed effects model approach to elucidate behavioral toxicity of metal mixtures in drinking water

Mixtures of chemical contaminants can pose a significant health risk to humans and wildlife, even at levels considered safe for each individual chemical. There is a critical need to develop statistical methods to evaluate the drivers of toxic effects in chemical mixtures (i.e., bad actors) from expo...

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Main Authors: Kanchana RK. Dilrukshi, Ilaria R. Merutka, Melissa Chernick, Stephanie Rohrbach, Remy Babich, Niroshan Withanage, Pani W. Fernando, Nishad Jayasundara
Format: Article
Language:English
Published: Elsevier 2024-11-01
Series:Ecotoxicology and Environmental Safety
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Online Access:http://www.sciencedirect.com/science/article/pii/S0147651324013721
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author Kanchana RK. Dilrukshi
Ilaria R. Merutka
Melissa Chernick
Stephanie Rohrbach
Remy Babich
Niroshan Withanage
Pani W. Fernando
Nishad Jayasundara
author_facet Kanchana RK. Dilrukshi
Ilaria R. Merutka
Melissa Chernick
Stephanie Rohrbach
Remy Babich
Niroshan Withanage
Pani W. Fernando
Nishad Jayasundara
author_sort Kanchana RK. Dilrukshi
collection DOAJ
description Mixtures of chemical contaminants can pose a significant health risk to humans and wildlife, even at levels considered safe for each individual chemical. There is a critical need to develop statistical methods to evaluate the drivers of toxic effects in chemical mixtures (i.e., bad actors) from exposure studies. Here, we develop a hierarchical modeling framework to disentangle the toxicity of complex metal mixtures from a screening study of 92 drinking well water samples containing multiple metal elements from Maine and New Hampshire, USA. In order to screen for neurodevelopmental impacts from exposure to these drinking water samples, we use a larval zebrafish (Danio rerio) behavioral assay. Zebrafish are an advantageous toxicological model organism due to combining the complexity of a vertebrate organism and higher-throughput exposure methods. We formulate a linear mixed modeling approach that captures intrinsic complexity in a common larval behavioral assay in order to improve its sensitivity and rigor and identify drivers of behavioral toxicity from the metal mixtures within the drinking water samples. Our analysis identifies lead (Pb), cadmium (Cd), nickel (Ni), copper (Cu), barium (Ba), and uranium (U) as metals that consistently impact larval locomotor activity, individually and across nine pairs of those metals. Our model also elucidates three distinct clusters of metal mixture components that drive behavioral effects: (Ba:Cu:U), (Ni:Pb:U), (Ba:Pb:U). Having identified a set of “bad-actor” metals from the water samples, we conduct exposure experiments for each individual metal (Pb, Cd, Ni, Cu, and Ba) at levels considered safe by the US Environmental Protection Agency drinking water regulatory limits and validate Pb, Ni, Cu, and Ba as behavioral toxicants at these concentrations. Collectively, our modeling approach estimates the impact of metal elements on a complex behavioral outcome in a statistically robust manner and establishes an approach to capture “bad actors” and key chemical interactions in a complex mixture.
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spelling doaj-art-77c2ee7153d0401e91e80ff6d8c7bf0a2024-11-21T06:02:06ZengElsevierEcotoxicology and Environmental Safety0147-65132024-11-01287117296Determining bad actors: A linear mixed effects model approach to elucidate behavioral toxicity of metal mixtures in drinking waterKanchana RK. Dilrukshi0Ilaria R. Merutka1Melissa Chernick2Stephanie Rohrbach3Remy Babich4Niroshan Withanage5Pani W. Fernando6Nishad Jayasundara7Department of Statistics, University of Sri Jayewardenepura, Sri LankaThe Nicholas School of the Environment, Duke University, Durham, NC 27708, USAThe Nicholas School of the Environment, Duke University, Durham, NC 27708, USAThe Nicholas School of the Environment, Duke University, Durham, NC 27708, USADepartment of Molecular and Biomedical Sciences, University of Maine, Orono, ME 04469, USADepartment of Statistics, University of Sri Jayewardenepura, Sri LankaDepartment of Mathematics, University of Sri Jayewardenepura, Sri LankaThe Nicholas School of the Environment, Duke University, Durham, NC 27708, USA; Corresponding author.Mixtures of chemical contaminants can pose a significant health risk to humans and wildlife, even at levels considered safe for each individual chemical. There is a critical need to develop statistical methods to evaluate the drivers of toxic effects in chemical mixtures (i.e., bad actors) from exposure studies. Here, we develop a hierarchical modeling framework to disentangle the toxicity of complex metal mixtures from a screening study of 92 drinking well water samples containing multiple metal elements from Maine and New Hampshire, USA. In order to screen for neurodevelopmental impacts from exposure to these drinking water samples, we use a larval zebrafish (Danio rerio) behavioral assay. Zebrafish are an advantageous toxicological model organism due to combining the complexity of a vertebrate organism and higher-throughput exposure methods. We formulate a linear mixed modeling approach that captures intrinsic complexity in a common larval behavioral assay in order to improve its sensitivity and rigor and identify drivers of behavioral toxicity from the metal mixtures within the drinking water samples. Our analysis identifies lead (Pb), cadmium (Cd), nickel (Ni), copper (Cu), barium (Ba), and uranium (U) as metals that consistently impact larval locomotor activity, individually and across nine pairs of those metals. Our model also elucidates three distinct clusters of metal mixture components that drive behavioral effects: (Ba:Cu:U), (Ni:Pb:U), (Ba:Pb:U). Having identified a set of “bad-actor” metals from the water samples, we conduct exposure experiments for each individual metal (Pb, Cd, Ni, Cu, and Ba) at levels considered safe by the US Environmental Protection Agency drinking water regulatory limits and validate Pb, Ni, Cu, and Ba as behavioral toxicants at these concentrations. Collectively, our modeling approach estimates the impact of metal elements on a complex behavioral outcome in a statistically robust manner and establishes an approach to capture “bad actors” and key chemical interactions in a complex mixture.http://www.sciencedirect.com/science/article/pii/S0147651324013721Mixture toxicologyLinear mixed-effect modelMetal mixturesToxicity screeningZebrafish
spellingShingle Kanchana RK. Dilrukshi
Ilaria R. Merutka
Melissa Chernick
Stephanie Rohrbach
Remy Babich
Niroshan Withanage
Pani W. Fernando
Nishad Jayasundara
Determining bad actors: A linear mixed effects model approach to elucidate behavioral toxicity of metal mixtures in drinking water
Ecotoxicology and Environmental Safety
Mixture toxicology
Linear mixed-effect model
Metal mixtures
Toxicity screening
Zebrafish
title Determining bad actors: A linear mixed effects model approach to elucidate behavioral toxicity of metal mixtures in drinking water
title_full Determining bad actors: A linear mixed effects model approach to elucidate behavioral toxicity of metal mixtures in drinking water
title_fullStr Determining bad actors: A linear mixed effects model approach to elucidate behavioral toxicity of metal mixtures in drinking water
title_full_unstemmed Determining bad actors: A linear mixed effects model approach to elucidate behavioral toxicity of metal mixtures in drinking water
title_short Determining bad actors: A linear mixed effects model approach to elucidate behavioral toxicity of metal mixtures in drinking water
title_sort determining bad actors a linear mixed effects model approach to elucidate behavioral toxicity of metal mixtures in drinking water
topic Mixture toxicology
Linear mixed-effect model
Metal mixtures
Toxicity screening
Zebrafish
url http://www.sciencedirect.com/science/article/pii/S0147651324013721
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