Elsevier

Science of The Total Environment

Volume 420, 15 March 2012, Pages 111-118
Science of The Total Environment

Assessing the potential risks to zebrafish posed by environmentally relevant copper and silver nanoparticles

https://doi.org/10.1016/j.scitotenv.2012.01.023Get rights and content

Abstract

The manufacture of large quantities of engineered nanomaterials (NMs) may lead to unintended contamination of aquatic ecosystems. Biologically based monitoring techniques need to be developed to detect these emerging NMs. The purpose of this study was to develop a risk-based probability model to predict the potential hazards of nanoecotoxicity toward aquatic organisms posed by waterborne copper and silver nanoparticles (Cu/Ag NPs). Published experimental evidence based on Cu/Ag NP-zebrafish (Danio rerio) systems was adopted as the study data. A Hill model was used to reconstruct a concentration–mortality response profile. A cumulative Weibull predictive model was employed to estimate exposure thresholds. The derived probabilistic model can predict the potential risk of environmentally relevant Cu/Ag NPs for major Taiwanese rivers with predicted environmental concentrations of 0.06 (95% confidence interval (CI): 0.01–0.92) mg L 1 for Cu NPs and 0.04 (0.01–0.11) mg L 1 for Ag NPs. The results indicated that estimated thresholds were 0.10–0.48 mg L 1 (95% CI) for Cu NPs and 2.69–2.73 mg L 1 for Ag NPs. The probabilities of a risk quotient (RQ) of > 1 ranged 17%–81% for zebrafish exposed to Cu NPs. This study found that Ag NP exposure scenarios posed no significant risks to zebrafish (RQ  0.1).

Highlights

►A probability risk model can assess the hazards of waterborne nanoparticles. ►Silver nanoparticles posed no significant risks to zebrafish. ►Zebrafish exposed to copper nanoparticles is alarming.

Introduction

The increasing use of engineered nanomaterials (NMs) in numerous industrial applications and consumer products necessitates performing risk assessments for human health and the environment (Mueller and Nowack, 2008, Schrand et al., 2010). NMs are a diverse class of small-scale (< 100-nm) substances formed by molecular-level engineering to achieve unique mechanical, optical, electrical, and magnetic properties.

Most toxicity studies focused on human health, and the environmental aspects are largely unexplored. Assessing the potential entry into and hazards and risks of engineered NMs to ecosystems in order to ensure their safe use and handling are topics of great interest to environmental toxicologists, chemists, and social scientists (Auffan et al., 2009, Kahru and Dubourguier, 2010). Some studies showed that fullerenes, carbon nanotubes, and various metal and metal oxide nanoparticles (NPs) can affect the physiology of different aquatic organisms such as fish (Griffitt et al., 2007, Griffitt et al., 2008, Asharani et al., 2008), algae (Baun et al., 2008), and water fleas (Lovern et al., 2007).

Nanometals of copper (Cu) and silver (Ag) are used in many consumer applications, mostly because of their well-demonstrated and safe use as antimicrobial agents (Lok et al., 2007). Cu/Ag NPs in the sub-50-nm range exhibit increased efficiency in inhibiting a wide range of bacteria and fungi. Although Cu/Ag NPs are already widely found in multiple products, a concrete assessment of their environmental implications is lacking. Yoon et al. (2007) indicated that Cu/Ag NPs can inhibit the activities of bacteria, including Escherichia coli and Bacillus subtilis. Antimicrobial characteristics and acute toxicities to aquatic organisms of Cu/Ag NPs were reported (Griffitt et al., 2007, Asharani et al., 2008, Schrand et al., 2010).

Several studies (Griffitt et al., 2007, Asharani et al., 2008) indicated that Cu NPs caused slightly less mortality to zebrafish (Danio rerio) than did soluble Cu, yet Ag NPs showed an adverse response (toward zebrafish embryos) compared to Ag+ ions. A dose-dependent relation with zebrafish mortality was also found (Griffitt et al., 2007, Asharani et al., 2008). In fact, a mortality effect and also non-mortality effects (e.g., oxidative stress, gill injury, heart rate, hatching rate, edema, and malformations) were found and addressed (Griffitt et al., 2007, Asharani et al., 2008). Based on toxicity tests of Ag NPs, chronic exposure to Ag NPs can cause thickening of epithelia gill tissue and altering gene expression profiles to adult and juvenile sheepshead minnows (Cyprinodon variegatus) (Griffitt et al., 2012). Laban et al. (2010) indicated that Ag NPs had more influence on fish in early life stage and can cause mortality for fathead minnow (Pimephales promelas) embryos. However, Bilberg et al. (2010) found that Ag NPs can reduce the diffusion conductance of gill for Eurasian perch (Perca fluviatilis) which then leads to internal hypoxia during low water oxygen tensions.

Ag NPs are extensively used in detergents and wound dressings due to their antimicrobial properties (Yoon et al., 2007). Cu NPs are also widely used as bactericides for air and liquid filtration, as coatings on integrated circuits and batteries, and to increase the thermal and electrical conductivity of coatings and sealants (Cioffi et al., 2005). These diverse applications of NMs such as antimicrobial coatings, in fuel cells, for water electrolysis, and as biomedical imaging contrast agents will very likely result in release to aquatic environments (Mueller and Nowack, 2008, Schrand et al., 2010). Possibly, NPs associating with naturally occurring colloids and particles should be considered together to determine how this could affect the bioavailability to aquatic animals and uptake into cells and organisms. Uptake by endocytotic routes is identified as a probable major mechanism of entry into cells; leading potentially to various types of cell toxicity and injury (Moore, 2006).

Given the likelihood of exposure to metals which are toxic to aquatic species resulting from the release of NMs into aquatic systems, many studies evaluated the potential toxic effects of NMs toward aquatic species. These include the effects of C60 fullerenes on large-mouth bass (Micropterus Salmoides) (Oberdöster, 2004), daphnid (Daphnia magna) (Lovern and Klaper, 2006), and fathead minnow (Pimephales promelas) (Oberdörster et al., 2006). The effects of carbon nanotubes (CNTs) (Smith et al., 2007) and titanium dioxide (TiO2) NPs or nTiO2 on rainbow trout (Oncorhynchus mykiss) (Federici et al., 2007) and on D. magna (Hund-Rinke and Simon, 2006) were also studied. Those studies identified significant toxicities for NPs. Griffitt et al. (2008) used zebrafish, daphnia, and algal (Pseudokirchneriella subcapitata) species as the test organisms in a mortality study with 48 h of exposure to Ag, Cu, aluminum, nickel, cobalt, and TiO2 NPs, and indicated that Cu/Ag NPs were strongly toxic to all aquatic organisms.

Mueller and Nowack (2008) carried out a quantitative risk assessment of engineered NPs in the environment. They showed that the predicted environmental concentrations of carbon nanotubes and Ag NPs in the environment posed little risk, whereas the effects of nTiO2 might be alarming in water bodies. Morgan (2005) developed a preliminary framework for performing risk assessment and management of the ecological and human-health risks of exposure to NPs.

Meanwhile, the major factors affecting the risks of environmental impacts, such as particle-related characteristics, surface chemistry, the presence of NPs, the uptake capacity, transport, fate, and toxic effects, were considered. Baun et al. (2008) also presented an integrated framework for human health and ecological risk assessments of ecotoxicity of engineered nanoparticles based on risk assessment protocols proposed by the USEPA (1992).

The objectives of this study were fourfold: (1) to obtain dose–response profiles based on published laboratory zebrafish exposure experiments by applying the Hill model, (2) to reanalyze acceptable levels of Cu/Ag NPs by employing the Weibull cumulative threshold model based on data of lethal concentrations yielding 10% mortality (LC10) to zebrafish, (3) to estimate the risk quotient (RQ) associated with uncertainties for possible exposure scenarios to Cu/Ag NPs in Taiwanese rivers using a probabilistic risk assessment, and (4) to integrate a risk-based framework to show that zebrafish can be a suitable bioindicator for monitoring the nanoecotoxicity of Cu/Ag NPs in aquatic ecosystems.

Section snippets

Study data

Study data related to relationships between concentrations of Cu/Ag NPs and the mortality of zebrafish were obtained from recently published studies (Griffitt et al., 2007, Griffitt et al., 2008, Asharani et al., 2008), which provided suitable datasets to reconstruct and validate the present model. Two datasets designated respectively as CuNP-G07 and CuNP-G08, adopted from Griffitt et al., 2007, Griffitt et al., 2008, were used for the Cu NP-zebrafish system. For the Ag NP-zebrafish system,

Concentration–mortality assessment

Fig. 2 shows the particle size-specific concentration–mortality relationships in the Cu NP-zebrafish system. In scenario CuNP-G07, the reconstructed concentration–mortality profile (Fig. 2a) and corresponding size distribution of the Cu NPs suspension (Fig. 2b) were well fitted (r2 = 0.96). The fitted LC50 value was estimated to be 1.68 (95% CI: 0.54–2.81) mg L 1 with a fitted Hill coefficient (n) of 1.28. Based on Fig. 2a, the LC10 was also estimated to be 0.3 (95% CI: 0.1–0.5) mg L 1. The size

Aquatic organisms exposed to NPs/NMs

Recently, most nanotoxicology experiments on adult and embryo life stages of zebrafish also demonstrated that Cu/Ag NPs can cause acute toxicity to zebrafish (Griffitt et al., 2007, Asharani et al., 2008). Furthermore, toxicological research reports proved that Ag NPs were more lethal to cell-based in vitro systems than were other metal NPs screened (Schrand et al., 2010). In our study, we provided an integrated risk-based framework to evaluate and protect the safety of aquatic organism exposed

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