Effects of aged TiO2 nanomaterial from sunscreen on Daphnia magna exposed by dietary route
Highlights
► Pseudokirchneriella subcapitata were contaminated with artificially aged TiO2 nanocomposites. ► Contaminated algae were used to fed Daphnia magna in a chronic dietary test. ► Dietary chronic exposure of TiO2 nano-residues decreased growth and reproduction. ► These effects could be partly related to the modification of the digestive physiology of daphnids.
Introduction
The recent developments in nanotechnology opened new perspectives for many applications both for industry and society, which therefore lead to their increased use in commercial products. Enhanced production and use of nanomaterial (NM) (SCENIHR, 2006), and therefore the likely direct or indirect exposure to nanoparticles (NP) raise concerns related to environmental hazards and public health (Nel et al., 2006).
Ecotoxicological studies of the impact of nanoparticles (NP) on freshwater organisms are continuously increasing, however most studies usually focus on the hazard of native NP on aquatic organisms. However for most applications NP can be surface modified and generally are embedded in the final product and therefore not coming into direct contact with consumers or the environment. In the case of solar sunscreen containing NP of TiO2, NM are covered, for example, with Al(OH)3 to prevent the generation of reactive oxygen species (ROS) due to TiO2 photocatalytic property and with polydimethylsiloxane (PDMS) to facilitate their dispersion in the lotion. Even if some studies addressed the effects of bare nano-TiO2 (i.e., TiO2 nanoparticle without coating) on the aquatic cladoceran D. magna (Hund-Rinke and Simon, 2006; Lovern and Klaper, 2006; Zhu et al., 2009a), only one study (Wiench et al., 2009) reported the direct effect of this specific surface modified TiO2 NM on D. magna.
Commercialized materials containing modified NP can be degraded over time during their use and life cycle. These aging mechanisms may release residues of nanomaterials (RNM) into the environment (Auffan et al., 2010; Labille et al., 2010) and therefore can lead to indirect exposure to humans or direct exposure to the environment. In the particular case of TiO2 NM used in sunscreen it was shown that artificial aging (effect of light and water over time) alter the surface layers (Auffan et al., 2010; Labille et al., 2010) and thus their aqueous properties (e.g., from hydrophobic to hydrophilic characteristic).
For TiO2 NM used in sunscreen, the indirect exposure corresponds to the washing off of TiO2 NM during swimming or body washing. The main issue is to determine the evolution and alteration of the composite as a function of biotic and abiotic long-term reactions. Consequently it is important to take into account aging scenarios to assess the hazard of NM on organisms (Mueller and Nowack, 2008; Thomas et al., 2006). Yet most studies focus on short-term waterborne exposure (Hassellov et al., 2008; Lovern and Klaper, 2006; Warheit et al., 2007; Zhu et al., 2009b) although the presence of NP associated to suspended particles (e.g., phytoplanctonic algae) is likely to account for an important contamination source for planctonic and benthic consumers during their entire life.
Nanomaterials biological effects detected at sublethal doses may correspond to the first steps for more drastic effects in chronic exposure. Indeed behavioral and physiological changes were measured by Lovern et al. (2007), as well as an induction of oxidative stress biomarkers (Klaper et al., 2009) when daphnia were exposed to functionalized NP suspensions, even during short-term experiments. In the case of dietary exposure to toxic substances, it appears necessary to examine their impact on both ingestion rate and the activity of digestive enzymes (De Coen and Janssen, 1997). Moreover, such early signals confirm the need to implement studies allowing one to address the long-term effects of exposure to NP on organism life traits that control population dynamics.
The aim of the present study was to assess the chronic toxicity of dietary TiO2 RNM, (obtained by the artificially aging T-Lite™ nanomaterial used in sunscreen cream (Labille et al., 2010)), on D. magna taken in by feeding on algae, to reproduce a simple food chain. The algae Pseudokirchneriella subcapitata, previously contaminated with TiO2 RNM, was used to feed D. magna in a 21-day chronic bioassay. Accumulation and effects on survival, growth and reproduction were measured on both adults (11 days) and juveniles (<24 h) daphnia, which were exposed 10 and 21 day respectively. An x-ray spectro-microscopic technique (X-ray fluorescence spectromicroscopy, μ-XRF) was used to determine Ti spatial distribution and to quantify Ti (from TiO2 RNM) content within algae and daphnia. In parallel to the chronic bioassay, complementary experiments were performed to assess ingestion rates and biochemical parameters such as antioxidant and digestive enzyme activities.
Section snippets
Nanoparticles preparation and aging
The initial commercial nanomaterial (T-Lite™ SF, BASF, Germany) consisting of a TiO2 rutile core coated with Al(OH)3 and polydimethylsiloxane (PDMS) layers, was supplied as a dry powder. The aging procedure (Auffan et al., 2010; Labille et al., 2010) consisted in stirring 100 mg of commercial nanomaterial in 250 mL ultrapure water during 48 h under white lamp radiation (sodium discharged 400 W). A stable suspension of colloidal by-products from 50 to 700 nm in size was formed and recovered.
TiO2 RNM characterization
The TiO2 by-product stock solution, used for the algae contamination, was constituted with particles of two sizes classes (Fig. 1) 300 nm and 20 μm. The size distribution is given as relative volume fraction. One should keep in mind that there is a cubic relationship between the size and the volume of a particle. Therefore the volume of one particle of 20 microns (i.e., one aggregate in our case) in diameter corresponds to the volume of ≈3.106 particles of 300 nm in diameter. Even if volume
Discussion
These results highlight the ability of nano-residues formed during the aging and alteration of commercialized Ti-nanomaterial to exert a significant effect on life traits of D. magna, both on reproduction and growth, when brought by food.
Contamination of D. magna by TiO2 RNM and toxic effects could be attributed either to the ingestion of contaminated algae, or by the absorption of nanomaterial dispersed in the daphnia medium after algae addition, or a combination of both. However, the aging
Conclusion
Dietary chronic exposure of residues of NM caused a decrease of growth and reproduction that could be partly related to the modification of the digestive physiology of daphnia. This first ecotoxicological study on by-product of aged TiO2 nanoparticles used in sunscreen cream put into evidence first of all a low mortality level compared to bare nano-TiO2 revealing the high importance of surface modification of nanoparticles. The study also demonstrated an effect from an environmentally relevant
Acknowledgements
The authors thank Ashley Tilghman-Sibille for correcting manuscript, and the French National Programs NANOALTER (INSU/EC2CO/CYTRIX) and ANR CES AGING NANO & TROPH (ANR-08-CESA-001) for funding.
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