Research paper
Testing the efficacy of broad-acting sorbents for environmental mixtures using isothermal analysis, mammalian cells, and H. vulgaris

https://doi.org/10.1016/j.jhazmat.2020.124425Get rights and content

Highlights

  • Broad-acting and edible sorbents for humans and animals were investigated.

  • Class-specific mixtures were PAHs, pesticides, Aroclors, plasticizers and mycotoxins.

  • Binding efficacy was tested using Langmuir/Freundlich, in vitro and in vivo models.

  • Adsorption isotherms, mammalian cells, and the hydra assay showed high correlation.

  • Medical grade carbon and nutrient-/acid-treated montmorillonite were broadly active.

Abstract

The hazards associated with frequent exposure to polycyclic aromatic hydrocarbons (PAHs), pesticides, Aroclors, plasticizers, and mycotoxins are well established. Adsorption strategies have been proposed for the remediation of soil and water, although few have focused on the mitigation of mixtures. This study tested a hypothesis that broad-acting sorbents can be developed for diverse chemical mixtures. Adsorption of common and hazardous chemicals was characterized using isothermal analysis from Langmuir and Freundlich equations. The most effective sorbents included medical-grade activated carbon (AC), parent montmorillonite clay, acid-processed montmorillonite (APM), and nutrient-amended montmorillonite clays. Next, we tested the ability of broad-acting sorbents to prevent cytotoxicity of class-specific mixtures using 3 mammalian in vitro models (HLF, ESD3, and 3T3 cell lines) and the hydra assay. AC showed the highest efficacy for mitigating pesticides, plasticizers, PAHs, and mycotoxins. Clays, such as APM, were effective against pesticides, Aroclors, and mycotoxins, while amended clays were most effective against plasticizers. Finally, a sorbent mixture was shown to be broadly active. These results are supported by the high correlation coefficients for the Langmuir model with high capacity, affinity, and free energy, as well as the significant protection of cells and hydra (p < 0.05). The protection percentages in 3T3 cells and hydra showed the highest correlation as suggested by both Pearson and Spearman with r = 0.84 and rho = 0.73, respectively (p < 0.0001). Collectively, these studies showed that broad-acting sorbents may be effective in preventing toxic effects of chemical mixtures and provided information on the most effective sorbents based on adsorption isotherms, and in vitro and aquatic organism test methods.

Introduction

Humans and animals are continuously exposed to a multitude of substances. Most studies have focused on the safety and toxicity testing of individual chemicals, but not mixtures. Complex environmental mixtures of concern may include different classes of substances, such as pesticides, Aroclors, plasticizers, polycyclic aromatic hydrocarbons (PAHs), and mycotoxins. Pesticides are widely used in agriculture and household settings, resulting in frequent exposure to pesticide residues from food and drinking water (Damalas and Eleftherohorinos, 2011). Aroclors are complex mixtures of polychlorinated biphenyls (PCBs) that have been extensively used as dielectric fluids in transformers and heat-exchange fluids. Humans can be exposed to Aroclors by eating contaminated fish, meat, and dairy products. Plasticizers are used widely in medical devices, food processing and packaging, and electronics. Dietary consumption is considered as a major route of exposure to plasticizers in humans because they can partition into food and water from packaging or during food processing (Bui et al., 2016). PAHs are widespread environmental contaminants formed during incomplete combustion or pyrolysis of organic materials. The primary source of human exposure to PAHs is food, which contributes 99% (WHO, 1984). Humans and animals can also be exposed to mycotoxins via contaminated food during droughts and extended periods of heat, when fungi reach their optimal growth conditions for the production of mycotoxins.

The most effective and economical approach to remediate chemical contamination of water or other media is through sorbent filtration and purification methods; however, most sorbent studies have focused on the removal of individual chemicals, rather than complex mixtures. Also, methods to remediate contaminated food and feed, which are major routes of exposure to chemicals in both humans and animals, are lacking. Previous studies have reported the development of sorbents for binding specific chemical contaminants with high sorption efficacy. Activated carbon (AC) is known as one of the most effective sorbents. AC is widely used for water purification (Cecen and Aktas, 2011, Zhang et al., 2017); however, few studies have examined the efficacy and suitability of medical grade AC for animal and human consumption against complex chemical mixtures. Clay-derived materials, such as calcium montmorillonite, have a high affinity for binding aflatoxins and similar hydrophilic compounds; these materials are edible and safe for animal and human consumption (Phillips et al., 2019, Wang and Phillips, 2020). To develop broad-acting sorbents with high capacity for diverse environmental chemicals, a base montmorillonite clay has been activated with acid to simulate carbon structure with high surface area and porosity, and amended with organic nutrients to enhance interlayer spacing and surface hydrophobicity (Celis et al., 2007, Wang et al., 2017). These modified sorbents have been shown to bind organophilic chemicals, such as dyes, zearalenone, benzo[a]pyrene, pesticides, and PCBs (Cruz-Guzman et al., 2004, De et al., 2009, Hearon et al., 2020, Ugochukwu and Fialips, 2017, Wang et al., 2019a, Yip et al., 2005). Therefore, their binding efficacy for an even broader range of chemical classes and mixtures was investigated.

In vitro toxicity tests have been widely applied for screening environmental chemicals and mixtures (Gibb, 2008, Krewski et al., 2010). The scientific advantages for the broad use of in vitro toxicity tests include assessing chemicals in a more time- and cost-efficient manner while providing more relevant and mechanistic insights (Novakova et al., 2020). Furthermore, to study the toxicity of complex mixtures of chemicals, in vitro cell bioassays represent sensitive and effective tools for toxicological profiling, because they can cover the combined effects of the mixture’s components and enable the prioritization of toxicity drivers (Bandele et al., 2012, Neale et al., 2015). Also, in vitro cell-based assays may serve as biological testing models to evaluate the remediation potential of sorbents for environmental chemicals (Nones et al., 2017).

H. vulgaris, a freshwater cnidarian, is an environmental model used to study the acute effects of toxicants in a living organism (Dash and Phillips, 2012). Adult hydra assays have been utilized previously to accurately predict the safety and efficacy of toxicant-binding sorbents for subsequent studies in animals and plants (Afriyie-Gyawu et al., 2005, Hearon et al., 2021, Marroquin-Cardona et al., 2009). The hydra assay has also been utilized along with an in vitro gastrointestinal model (Lemke et al., 2001) and in silico molecular dynamic simulations (Wang et al., 2019) to screen and validate sorbents.

The objective of this study was to investigate the ability of various sorbents to effectively prevent toxicity of diverse environmental chemicals and their mixtures. Sorbents were characterized using isothermal analysis based on binding capacity, affinity, heterogeneity, correlation coefficients, and free energy of sorption. Furthermore, the efficacy of sorption was characterized using 3 mammalian cell models and a hydra assay to confirm the safety of sorbent inclusion and to verify the ability of sorbents to reduce the toxicity of complex mixtures.

Section snippets

Sorbent materials

Medical grade activated carbon (AC), purity >99%, was obtained from General Carbon Corporation (2000) (Paterson, NJ). It is labeled as a virgin powdered AC derived from a selected grade of coconut shell with 1100 m2/g surface area, 5% moisture, a pH of point of zero charge (pHPZC) equal to 9.57 (Wang et al., 2020a), and a zeta potential of −31 mV (Kumar et al., 2020). Calcium montmorillonite clay was obtained from TxESI, Inc. (Bastrop, Texas) with a total surface area of approximately 850 m2/g,

Adsorption analysis

Equilibrium isotherms were used to describe adsorption isotherms for each test sorbent. Adsorption parameters, coupled with the Gibbs free energy equation, were used to calculate free energy (ΔG° in kJ/mol). Thermodynamic free energy indicated the spontaneity of the adsorption process. Table 1 summarized the binding parameters described by the best fit model of individual chemicals on various sorbents. All of the adsorption isotherms fit either the Langmuir or the Freundlich model with r2

Conclusion

In this study, we characterized various parameters including surface capacity, binding affinity, heterogeneity of binding sites, and free energy of sorption derived from Langmuir or Freundlich models for representative environmental chemicals. The most effective and broad-acting sorbents were identified and selected based on isothermal results. Furthermore, the protective efficacy of broad-acting sorbents against potential toxicity of class-specific chemical mixtures was tested using in vitro

Funding

This work was supported by the Superfund Hazardous Substance Research and Training Program (National Institute of Environmental Health Sciences) [P42 ES027704]; and the USDA National Institute of Food and Agriculture [Hatch 6215].

CRediT authorship contribution statement

Meichen Wang: Formal analysis; Investigation; Software; Writing - original draft. Zunwei Chen: Formal analysis; Investigation; Software; Writing - original draft. Ivan Rusyn: Resources; Validation; Writing - review & editing. Timothy Phillips: Conceptualization; Data curation; Funding acquisition; Methodology; Project administration; Resources; Supervision; Validation; Writing - review & editing.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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