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Effects of CeO2 Nanoparticles on Terrestrial Isopod Porcellio scaber: Comparison of CeO2 Biological Potential with Other Nanoparticles

  • Olga Malev
  • Polonca Trebše
  • Małgorzata Piecha
  • Sara Novak
  • Bojan Budič
  • Miroslav D. Dramićanin
  • Damjana Drobne
Article

Abstract

Nano-sized cerium dioxide (CeO2) particles are emerging as an environmental issue due to their extensive use in automobile industries as fuel additives. Limited information is available on the potential toxicity of CeO2 nanoparticles (NPs) on terrestrial invertebrates through dietary exposure. In the present study, the toxic effects of CeO2 NPs on the model soil organism Porcellio scaber were evaluated. Nanotoxicity was assessed by monitoring the lipid peroxidation (LP) level and feeding rate after 14-days exposure to food amended with nano CeO2. The exposure concentration of 1000 μg of CeO2 NPs g−1 dry weight food for 14 days significantly increased both the feeding rate and LP. Thus, this exposure dose is considered the lowest observed effect dose. At higher exposure doses of 2000 and 5000 μg of CeO2 NPs g−1 dry weight food, NPs significantly decreased the feeding rate and increased the LP level. Comparative studies showed that CeO2 NPs are more biologically potent than TiO2 NPs, ZnO NPs, CuO NPs, CoFe2O4 NPs, and Ag NPs based on feeding rate using the same model organism and experimental setup. Based on comparative metal oxide NPs toxicities, the present results contribute to the knowledge related to the ecotoxicological effects of CeO2 NPs in terrestrial invertebrates exposed through feeding.

Keywords

CeO2 CoFe2O4 Digestive Gland Risk Quotient Cerium Dioxide 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

The authors thank M. Hočevar for SEM images of nanoparticles taken at the Institute of Metals and Technology in Ljubljana, Slovenia. The present work was funded via the European Commission 7th Framework Programme project “NanoMILE” (contract no. NMP4-LA-2013-310451). A part of work was conducted at Center of excellence in Nanoscience and Nanotechnology, Ljubljana, Slovenia.

Supplementary material

244_2017_363_MOESM1_ESM.doc (915 kb)
Supplementary material 1 (DOC 914 kb)

References

  1. Arnold MC, Badireddy AR, Wiesner MR, Di Giulio RT, Meyer JN (2013) Cerium oxide nanoparticles are more toxic than equimolar bulk cerium oxide in Caenorhabditis elegans. Arch Environ Contam Toxicol 65:224–233. doi: 10.1007/s00244-013-9905-5 CrossRefGoogle Scholar
  2. Artells E, Issartel J, Auffan M, Borschneck D, Thill A, Tella M, Brousset L, Rose J, Bottero J-Y, Thiéry A (2013) Exposure to cerium dioxide nanoparticles differently affect swimming performance and survival in two daphnid species. PLoS ONE 8:1–11CrossRefGoogle Scholar
  3. Batley GE, Halliburton B, Kirby JK, Doolette CL, Navarro D, McLaughlin MJ, Veitch C (2013) Characterization and ecological risk assessment of nanoparticulate CeO2 as a diesel fuel catalyst. Environ Toxicol Chem 32:1896–1905CrossRefGoogle Scholar
  4. Chen S, Hou Y, Cheng G, Zhang C, Wang S, Zhang J (2013) Cerium oxide nanoparticles protect endothelial cells from apoptosis induced by oxidative stress. Biol Trace Elem Res 154:156–166CrossRefGoogle Scholar
  5. Collin B, Oostveen E, Tsyusko OV, Unrine JM (2014) Influence of natural organic matter and surface charge on the toxicity and bioaccumulation of functionalized ceria nanoparticles in Caenorhabditis elegans. Environ Sci Technol 48:1280–1289CrossRefGoogle Scholar
  6. Cornelis G, Ryan B, McLaughlin MJ, Kirby JK, Beak D, Chittleborough D (2011) Solubility and batch retention of CeO2 nanoparticles in soils. Environ Sci Technol 45:2777–2782CrossRefGoogle Scholar
  7. Drobne D (1997) Terrestrial ispods—a good choice for toxicity testing of pollutants in the terrestrial environment. Environ Toxicol Chem 16:1159–1164Google Scholar
  8. Drobne D, Jemec A, Pipan-Tkalec Z (2009) In vivo screening to determine hazards of nanoparticles: nanosized TiO2. Environ Pollut 157:1157–1164CrossRefGoogle Scholar
  9. Felix LC, Ortega VA, Ede JD, Goss GG (2013) Physicochemical characteristics of polymer-coated metal-oxide nanoparticles and their toxicological effects on zebrafish (Danio rerio) development. ASC Environ Sci Technol 47:6589–6596Google Scholar
  10. Gaiser BK, Biswas A, Rosenkranz P, Jepson MA, Lead JR, Stone V, Tyler CR, Fernandes TF (2011) Effects of silver and cerium dioxide micro- and nano-sized particles on Daphnia magna. J Environ Monit 13:1227–1235CrossRefGoogle Scholar
  11. Gambardella C, Gallus L, Gatti AM, Faimali M, Carbone S, Antisari LV, Falugi C, Ferrando S (2014) Toxicity and transfer of metal oxide nanoparticles from microalgae to sea urchin larvae. Chem Ecol 30:308–316CrossRefGoogle Scholar
  12. García A, Espinosa R, Delgado L, Casals E, González E, Puntes V, Barata C, Font X, Sánchez A (2011) Acute toxicity of cerium oxide, titanium oxide and iron oxide nanoparticles using standardized tests. Desalination 269:136–141CrossRefGoogle Scholar
  13. Golobič M, Jemec A, Drobne D, Romih T, Kasemets K, Kahru A (2012) Upon exposure to Cu nanoparticles, accumulation of copper in the isopod Porcellio scaber is due to the dissolved Cu ions inside the digestive tract. Environ Sci Technol 46:12112–12119CrossRefGoogle Scholar
  14. Gottschalk F, Sun TY, Nowack B (2013) Environmental concentrations of engineered nanomaterials: review of modelling and analytical studies. Environ Pollut 181:287–300CrossRefGoogle Scholar
  15. Karakoti AS, Monteiro-Riviere NA, Aggarwal R, Davis JP, Narayan RJ, McGinnis J, Seal S (2008) Nanoceria as antioxidant: synthesis and biomedical applications. J Miner Met Mater Soc 60:33–37CrossRefGoogle Scholar
  16. Karakoti AS, Munusamy P, Hostetler K, Kodali V, Kuchibhatla S, Orr G, Pounds JG, Teeguarden JG, Thrall BD, Baer DR (2012) Preparation and characterization challenges to understanding environmental and biological impacts of nanoparticles. Surf Interface Anal 44:882–889CrossRefGoogle Scholar
  17. Lahive E, Jurkschat K, Shaw BJ, Handy RD, Spurgeon DJ, Svendsen C (2014) Toxicity of cerium oxide nanoparticles to the earthworm Eisenia fetida: subtle effects. Environ Chem 11:268–278CrossRefGoogle Scholar
  18. Lee SW, Kim SM, Choi J (2009) Genotoxicity and ecotoxicity assays using the freshwater crustacean Daphnia magna and the larva of the aquatic midge Chironomus riparius to screen the ecological risks of nanoparticle exposure. Environ Toxicol Pharmacol 28:86–91CrossRefGoogle Scholar
  19. Lynch I, Weiss C, Valsami-Jones E (2014) A strategy of grouping nanomaterials based on physico-chemical descriptors as a basis for safer-by-design NMs. Nanotoday 9:266–270CrossRefGoogle Scholar
  20. Malev O, Sauerborn Klobučar R, Fabbretti E, Trebše P (2012) Comparative toxicity of imidacloprid and its transformation product 6-chloronicotinic acid to non-target aquatic organisms: Microalgae Desmodesmus subspicatus and Gammarus fossarum. Pestic Biochem Physiol 204:178–186CrossRefGoogle Scholar
  21. Manier N, Bado-Nilles A, Delalain P, Aguerre-Chariol O, Pandard P (2013) Ecotoxicity of non-aged and aged CeO2 nanomaterials towards freshwater microalgae. Environ Pollut 180:63–70CrossRefGoogle Scholar
  22. McShane H, Sarrazin M, Whalen JK, Hendershot WH, Sunahara GI (2012) Reproductive and behavioral responses of earthworms exposed to nano-sized titanium dioxide in soil. Environ Toxicol Chem 31:184–193CrossRefGoogle Scholar
  23. Novak S, Drobne D, Valant J, Pipan-Tkalec Ž, Pelicon P, Vavpetič P, Grlj N, Falnoga I, Mazej D, Remškar M (2012a) Cell membrane integrity and internalization of ingested TiO2 nanoparticles by digestive gland cells of a terrestrial isopod. Environ Toxicol Chem 31:1083–1090CrossRefGoogle Scholar
  24. Novak S, Drobne D, Menard A (2012b) Prolonged feeding of terrestrial isopod (Porcellio scaber, Isopoda, Crustacea) on TiO2 nanoparticles. Absence of toxic effect. Zookeys 273:261–273CrossRefGoogle Scholar
  25. Novak S, Drobne D, Valant J, Pelicon P (2012c) Internalization of consumed nanoparticles by a model invertebrate organism. J Nanomater 2012:1–8. doi: 10.1155/2012/658752 CrossRefGoogle Scholar
  26. Novak S, Drobne D, Golobič M, Zupanc J, Romih T, Gianoncelli A, Kiskinova M, Kaulich B, Pelicon P, Vavpetič P, Jeromel L, Ogrinc N, Makovec D (2013) Cellular internalization of dissolved cobalt ions from ingested CoFe2O4 nanoparticles: in vivo experimental evidence. Environ Sci Technol 47:5400–5408CrossRefGoogle Scholar
  27. Organization for Economic Cooperation and Development (OECD) (2013) OECD Environment, Health and Safety Publications, Series on the Safety of Manufactured Nanomaterials, Document No. 37, Current developments in delegations on the safety of the manufactured nanomaterials—tour de table. ENV/JM/MONO(2013)2Google Scholar
  28. Park EJ, Choi J, Park YK, Park K (2008) Oxidative stress induced by cerium oxide nanoparticles in cultured BEAS-2B cells. Toxicology 245:90–100CrossRefGoogle Scholar
  29. Pipan-Tkalec Ž, Drobne D, Jemec A, Romih T, Zidar P, Bele M (2010) Zinc bioaccumulation in a terrestrial invertebrate fed a diet treated with particulate ZnO or ZnCl2 solution. Toxicology 269:198–203CrossRefGoogle Scholar
  30. Rodea-Palomares I, Boltes K, Fernández-Piñas F, Leganés F, García-Calvo E, Santiago J, Rosal R (2011) Physicochemical characterization and ecotoxicological assessment of CeO2 nanoparticles using two aquatic microorganisms. Toxicol Sci 119:135–145CrossRefGoogle Scholar
  31. Roh JY, Park YK, Park K, Choi J (2010) Ecotoxicological investigation of CeO2 and TiO2 nanoparticles on the soil nematode Caenorhabditis elegans using gene expression, growth, fertility, and survival as endpoints. Environ Toxicol Pharmacol 29:167–172CrossRefGoogle Scholar
  32. Schlich K, Klawonn T, Terytze K, Hund-Rinke K (2012a) Effects of silver nanoparticles and silver nitrate. Environ Toxicol Chem 32:181–188CrossRefGoogle Scholar
  33. Schlich K, Terytze K, Hund-Rinke K (2012b) Effect of TiO2 nanoparticles in the earthworm reproduction test. Environ Sci Europe 24:1–10CrossRefGoogle Scholar
  34. Šećerov B, Andrić Ž, Abazović N, Krsmanović R, Mitrić M, Montone A, Dramićanin M (2008) Combustion synthesis and characterization of CeO2 nanopowder. Acta Chim Slov 55:486–491Google Scholar
  35. Shoults-Wilson WA, Reinsch BC, Tsyusko OV, Bertsch PM, Lowry GV, Unrine JM (2011a) Role of particle size and soil type in toxicity of silver nanoparticles to earthworms evidence for avoidance of Ag nanoparticles by earthworms (Eisenia fetida). Soil Sci Soc Am J 75:365–377CrossRefGoogle Scholar
  36. Shoults-Wilson WA, Reinsch BC, Tsyusko OV, Bertsch PM, Lowry GV, Unrine JM (2011b) Effect of silver nanoparticle surface coating on bioaccumulation and reproductive toxicity in earthworms (Eisenia fetida). Nanotoxicology 5:432–444CrossRefGoogle Scholar
  37. Unrine JM, Tsyusko OV, Hunyadi SE, Judy JD, Bertsch PM (2010a) Effects of particle size on chemical speciation and bioavailability of copper to earthworms (Eisenia fetida) exposed to copper nanoparticles. J Environ Qual 39:1942–1953CrossRefGoogle Scholar
  38. Unrine JM, Hunyadi SE, Tsyusko OV, Rao W, Shoults-Wilson WA, Bertsch PM (2010b) Evidence for bioavailability of Au nanoparticles from soil and biodistribution within earthworms (Eisenia fetida). Environ SciTechnol 44:8308–8313CrossRefGoogle Scholar
  39. US EPA (2004) Interim registration eligibility decision. Prevention pesticides and toxic substances (7508C). 738-R-04-006. http://envirocancer.cornell.edu/turf/pdf/diazinon_ired.pdf. Accessed 2 May 2015Google Scholar
  40. Valant J, Drobne D, Novak S (2012) Effect of ingested titanium dioxide nanoparticles on the digestive gland cell membrane of terrestrial isopods. Chemosphere 87:19–25CrossRefGoogle Scholar
  41. Van Hoecke K, Quik JTK, Mankiewicz-Boczek J, De Schamphelaere KC, Elsaesser A, Van der Meeren P (2009) Fate and effects of CeO2 nanoparticles in aquatic ecotoxicity tests. Environ Sci Technol 43:4537–4546CrossRefGoogle Scholar
  42. Xia T, Kovochich M, Liong M, Madler L, Gilbert B, Shi H, Yeh JI, Zink JI, Nel AE (2008) Comparison of the mechanism of toxicity of zinc oxide and cerium oxide nanoparticles based on dissolution and oxidative stress properties. ACS Nano 2:2121–2134CrossRefGoogle Scholar
  43. Xia J, Zhao HZ, Lu GH (2013) Effects of selected metal oxide nanoparticles on multiple biomarkers in Carassius auratus. Biomed Environ Sci 26:742–749Google Scholar
  44. Xu C, Qu X (2014) Cerium oxide nanoparticle: a remarkably versatile rare earth nanomaterial for biological applications. NPG Asia Mater 6:1–16CrossRefGoogle Scholar
  45. Zhang H, He X, Zhang Z, Zhang P, Li Y, Ma Y, Kuang Y, Zhao Y, Chai Z (2011) Nano-CeO2 exhibits adverse effects at environmental relevant concentrations. Environ Sci Technol 45:3725–3730CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  1. 1.University of Nova GoricaNova GoricaSlovenia
  2. 2.Department of Biology, Biotechnical FacultyUniversity of LjubljanaLjubljanaSlovenia
  3. 3.National Institute of ChemistryLjubljanaSlovenia
  4. 4.Institute of Nuclear Sciences - VinčaBeogradSerbia

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