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Acute Toxicity of Colloidal Silicon Dioxide Nanoparticles on Amphibian Larvae: Emerging Environmental Concern

  • Rafael Carlos Lajmanovich
  • Paola Mariela Peltzer
  • Candela Soledad Martinuzzi
  • Andrés Maximiliano Attademo
  • Carlina Leila Colussi
  • Agustín Bassó
Research paper
  • 69 Downloads

Abstract

Emerging contaminants derive from pharmaceuticals, pesticides, disinfection by-products, home and care products, and wood preservation and industrial chemicals that contain specific drugs, metals, metal oxides and metalloids as nanoparticles (NPs) in their formulations. Although the use of silicon dioxide (SiO2) NPs in commercial products increases, its impacts on the environment and on animal and human health are largely unknown. Thus, the aim of this study was to evaluate the ecotoxicity of colloidal SiO2-NPs in Rhinella arenarum larvae exposed to 0.001, 0.01, 0.1, and 1 mg/L colloidal SiO2-NPs for 48 h. Biotoxicological endpoints (median lethal concentration-LC50; 95% confidence limits), the no-observed-effect concentration (NOEC), the lowest-observed-effect concentration (LOEC), Toxic Units (TU), oxidative stress enzyme activity (glutathione S-transferase-GST), and genotoxicity (frequency of micronuclei, and other erythrocyte nuclear abnormalities-ENAs) were measured in exposed larvae. Scanning electron microscopy equipped with an energy dispersive X-ray system allowed detecting that SiO2-NPs aggregate on the dorsal skin of SiO2-treated larvae. The 48 h LC50 of colloidal SiO2-NPs was 0.0251 mg/L (0.0163- 0.0338 mg/L). The NOEC and LOEC values after 48 h were 0.001 mg/L and 0.01 mg/L, respectively. According to the hazard classification system for wastewaters discharged into the aquatic environment, the colloidal SiO2-NPs evaluated are Class V, i.e., of very high acute toxicity (TU = 3984.06). At 48 h of exposure to NOEC, GST activity and ENAs frequency were significantly increased (118.75 and 58%, respectively) with respect to controls. The results of the present study indicate that, at low concentration, colloidal SiO2-NPs exerted high toxicity on R. arenarum tadpoles.

Keywords

Rhinella arenarum Nanotoxicity Emerging contaminants Biomarkers Personal care products 

Notes

Acknowledgements

The scanning electronic microscope micrographs and the energy dispersive X-ray spectroscopy analysis were conducted at the Instituto de Física de Rosario (IFIR) of the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Rosario, Argentina. We thank Dr. Martina Avalos for her help with micrographs, spectroscopy, and related discussions and Dr. Maria Victoria Eusevi for English Editing Service. This study was supported in part by CONICET, National Agency for Promotion of Science and Technology, and Course of Action for Research and Science Promotion (CAI + D-UNL), Argentina.

References

  1. Åkerlund E, Cappellini F, Di Bucchianico S, Islam S, Skoglund S, Derr R, Odnevall Wallinder I, Hendriks G, Karlsson HL (2017) Genotoxic and mutagenic properties of Ni and NiO nanoparticles investigated by comet assay, γ-H2AX staining, Hprt mutation assay and ToxTracker reporter cell lines. Environ Mol Mutagen.  https://doi.org/10.1002/em.22163 (epub ahead of print) Google Scholar
  2. Al-Odaini NA, Zakaria MP, Yaziz MI, Surif S, Abdulghani M (2013) The occurrence of human pharmaceuticals in wastewater effluents and surface water of Langat River and its tributaries, Malaysia. Int J Environ Anal Chem 93(3):245–264.  https://doi.org/10.1080/03067319.2011.592949 CrossRefGoogle Scholar
  3. Altig R, Whiles MR, Taylor CL (2007) What do tadpoles really eat? Assessing the trophic status of an understudied and imperiled group of consumers in freshwater habitats. Freshw Biol 52:386–395.  https://doi.org/10.1111/j.1365-2427.2006.01694.x CrossRefGoogle Scholar
  4. Ambrosone A, Scotto di Vettimo MR, Malvindi MA, Roopin M, Levy O, Marchesano V, Pompa PP, Tortiglione C, Tino A (2014) Impact of amorphous SiO2 nanoparticles on a living organism: morphological, behavioral, and molecular biology implications. Int J Environ Anal Chem.  https://doi.org/10.3389/fbioe.2014.00037 Google Scholar
  5. Anon. (2008) Working with microspheres, Bangs Laboratories, Inc., 9025 Technology Dr., Fishers, IN 46038-2886, TechNote 201, pp 20Google Scholar
  6. Archer E, Petrie B, Kasprzyk-Hordern B, Wolfaardt GM (2017) The fate of pharmaceuticals and personal care products (PPCPs), endocrine disrupting contaminants (EDCs), metabolites and illicit drugs in a WWTW and environmental waters. Chemosphere 174:437–446.  https://doi.org/10.1016/j.chemosphere.2017.01.101 CrossRefGoogle Scholar
  7. ASIH-American Society of Ichthyologists and Herpetologists (2004) Guidelines for use of live amphibians and reptiles in field and laboratory research. Herpetological Animal Care and Use Committee (HACC), Washington DCGoogle Scholar
  8. Attademo AM, Cabagna Zenklusen M, Lajmanovich RC, Peltzer PM, Junges C, Bassó A (2011) B-Esterase activities and blood cell morphology in the Frog Leptodactylus chaquensis (Amphibia: Leptodactylidae) on rice agroecosystems from Santa Fe Province (Argentina). Ecotoxicology 20:274–282.  https://doi.org/10.1007/s10646-010-0579-8 CrossRefGoogle Scholar
  9. Ayllon F, García-Vazquez E (2000) Induction of micronuclei and other nuclear abnormalities in European minnow Phoxinus phoxinus and mollie Poecilia latipinna: na assessment of the fish micronucleus test. Mutat Res 467:177–186.  https://doi.org/10.1016/S1383-5718(00)00033-4 CrossRefGoogle Scholar
  10. Ayres M Jr, Ayres D, Santos A (2008) BioEstat, Versão5.0. Sociedade Civil Mamirauá, MCT-CNPq, Belém, BrazilGoogle Scholar
  11. Bacchetta C, Ale A, Simoniello MF, Gervasio S, Davico C, Rossi AS, Desimone MF, Poletta G, López G, Monserrat JM, Cazenave J (2017) Genotoxicity and oxidative stress in fish after a short-term exposure to silver nanoparticles. Ecol Indic 76:230–239.  https://doi.org/10.1016/j.ecolind.2017.01.018 CrossRefGoogle Scholar
  12. Barik TK, Sahu B, Swain V (2008) Nanosilica-from medicine to pest control. Parasitol Res 103(2):253–258.  https://doi.org/10.1007/s00436-008-0975-7 CrossRefGoogle Scholar
  13. Barik TK, Kamaraju R, Gowswami A (2012) Silica nanoparticle: a potential new insecticide for mosquito vector control. Parasitol Res 111(3):1075–1083.  https://doi.org/10.1007/s00436-012-2934-6 CrossRefGoogle Scholar
  14. Bhushan B (2004) Springer handbook of nanotechnology. Springer, New YorkCrossRefGoogle Scholar
  15. Bionda CL, Kost S, Salas NE, Lajmanovich RC, Sinsch U, Martino AL (2015) Age structure, growth and longevity in the common toad, Rhinella arenarum, from Argentina. Acta Herpetol 10:55–62.  https://doi.org/10.13128/Acta_Herpetol-15142 Google Scholar
  16. Bolognesi C, Perrone E, Roggieri P, Pampanin DM, Sciutto A (2006) Assessment of micronuclei induction in peripheral erythrocytes of fish exposed to xenobiotics under controlled conditions. Aquat Toxicol 78:93–98.  https://doi.org/10.1016/j.aquatox.2006.02.015 CrossRefGoogle Scholar
  17. Bundschuh M, Seitz F, Rosenfeldt RR, Schulz R (2016) Effects of nanoparticles in fresh waters: risks, mechanisms and interactions. Freshw Biol 61:2185–2196.  https://doi.org/10.1111/fwb.12701 CrossRefGoogle Scholar
  18. Calderón-Jiménez B, Johnson M, Montoro Bustos A, Murphy C, Winchester M, Vega Baudrit J (2017) Silver nanoparticles: technological advances, societal impacts, and metrological challenges. Front Chem.  https://doi.org/10.3389/fchem.2017.00006 Google Scholar
  19. Caltagirone C, Bettoschi A, Garau A, Montis R (2015) Silica-based nanoparticles: a versatile ool for the development of efficient imaging agents. Chem Soc Rev 44:4645–4671.  https://doi.org/10.1039/c4cs00270a CrossRefGoogle Scholar
  20. Contado C (2015) Nanomaterials in consumer products: a challenging analytical problem. Front Chem.  https://doi.org/10.3389/fchem.2015.00048 Google Scholar
  21. de Souza TAJ, Rocha TL, Franchi LP (2018) Detection of DNA damage induced by cerium dioxide nanoparticles: from models to molecular mechanism activated. Adv Exp Med Biol 1048:215–226.  https://doi.org/10.1007/978-3-319-72041-8_13 CrossRefGoogle Scholar
  22. Demir E, Castranova V (2016) Genotoxic effects of synthetic amorphous silica nanoparticles in the mouse lymphoma assay. Toxicol Rep 3:807–815.  https://doi.org/10.1016/j.toxrep.2016.10.006 CrossRefGoogle Scholar
  23. Diab R, Canilho N, Pavel IA, Haffner FB, Girardon M, Pasc A (2017) Silica-based systems for oral delivery of drugs, macromolecules and cells. Adv Colloid Interface Sci 249:346–362.  https://doi.org/10.1016/j.cis.2017.04.005 CrossRefGoogle Scholar
  24. Duan J, Yu Y, Shi H, Tian L, Guo C, Huang P, Zhou X, Peng S, Sun Z (2013) Toxic effects of silica nanoparticles on zebrafish embryos and larvae. PLoS ONE 8(9):e74606.  https://doi.org/10.1371/journal.pone.0074606 CrossRefGoogle Scholar
  25. Environmental Protection Agency EPA (2015) Chemical substances when manufactured or processed as nanoscale materials: TSCA reporting and recordkeeping requirements Fed. Regist. 80, 18330. http://www.regulations.gov. Accessed 12 July 2016
  26. Federici G, Shaw BJ, Handy RD (2007) Toxicity of titanium dioxide nanoparticles to rainbow trout (Oncorhynchus mykiss): gill injury, oxidative stress, and other physiological effects. Aquat Toxicol 84:415–430.  https://doi.org/10.1016/j.aquatox.2007.07.009 CrossRefGoogle Scholar
  27. Gandhi PR, Jayaseelan C, Vimalkumar E, Mary RR (2016) Larvicidal and pediculicidal activity of synthesized TiO2 nanoparticles using Vitex negundo leaf extract against blood feeding parasites. Asia Pac Entomol 19:1089–1094.  https://doi.org/10.1016/j.aspen.2016.10.001 CrossRefGoogle Scholar
  28. Gosner KL (1960) A simplified table for staging anuran embryos and larvae, with notes on identification. Herpetologica 16:183–190Google Scholar
  29. Gravato C, Santos MA (2002) B-Naphthoflavone liver EROD and erythrocytic nuclear abnormality induction in juvenile Dicentrarchus labrax L. Ecotoxicol Environ Saf 52:69–74.  https://doi.org/10.1006/eesa.2002.2151 CrossRefGoogle Scholar
  30. Grisolia CK, Rivero CLG, Starling FLRM, Silva ICR, Barbosa AC, Dorea JG (2009) Profile of micronucleus frequencies and DNA damage in different species of fish in a eutrophic tropical lake. Genet Mol Biol 32:138–143.  https://doi.org/10.1590/S1415-47572009005000009 CrossRefGoogle Scholar
  31. Guilherme S, Válega M, Pereira ME, Santos MA, Pacheco M (2008) Erythrocytic nuclear abnormalities in wild and caged fish (Liza aurata) along an environmental Mercury contamination gradient. Ecotoxicol Environ Saf 70:411–421.  https://doi.org/10.1016/j.ecoenv.2007.08.016 CrossRefGoogle Scholar
  32. Habdous M, Vincent-Viry M, Visvikis S, Siest G (2002) Rapid spectrophotometric method for serum glutathione S-transferases activity. Clin Chim Acta 326:131–142.  https://doi.org/10.1016/S0009-8981(02)00329-7 CrossRefGoogle Scholar
  33. Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases, the first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139Google Scholar
  34. Hamilton MA, Russo RC, Thurston RV (1977) Trimmed Spearman-Karber method for estimating median lethal concentrations in toxicity bioassays. Environ Sci Technol 11:714–719.  https://doi.org/10.1021/es60130a004 CrossRefGoogle Scholar
  35. Hasezaki T, Isoda K, Kondoh M, Tsutsumi Y, Yagi K (2011) Hepatotoxicity of silica nanoparticles with a diameter of 100 nm. Pharmazie 66(9):698–703.  https://doi.org/10.1691/ph.2011.1516 Google Scholar
  36. Hinther A, Vawda S, Skirrow RC, Veldhoen N, Collins P, Cullen JT, van Aggelen G, Helbing CC (2010) Nanometals induce stress and alter thyroid hormone action in amphibia at or below North American water quality guidelines. Environ Sci Technol 44:8314–8321.  https://doi.org/10.1021/es101902n CrossRefGoogle Scholar
  37. Jaeger A, Weiss DG, Jonas L, Kriehuber R (2012) Oxidative stress-induced cytotoxic and genotoxic effects of nano-sized titanium dioxide particles in human HaCaT keratinocytes. Toxicology 296:27–36.  https://doi.org/10.1016/j.tox.2012.02.016 CrossRefGoogle Scholar
  38. Jones N, Ray B, Ranjit KT, Manna AC (2008) Antibacterial activity of ZnO nanoparticle suspensions on a broad spectrum of microorganisms. FEMS Microbiol Lett 279:71–76.  https://doi.org/10.1111/j.1574-6968.2007.01012.x CrossRefGoogle Scholar
  39. Kendall RJ, Lacher TE, Cobb GC, Cox SB (2016) Wildlife toxicology: emerging contaminant and biodiversity issues. CRC Press, New YorkGoogle Scholar
  40. Kingsley GR (1942) The direct biuret method for the determination of serum proteins as applied to photoelectric and visual calorimetry. J Lab Clin Med 27:840–845Google Scholar
  41. Kisin ER, Murray AR, Keane MJ, Shi XC, Schwegler-Berry D, Gorelik O, Arepalli S, Castranova V, Wallace WE, Kagan VE, Shvedova AA (2007) Single-walled carbon nanotubes: geno- and cytotoxic effects in lung fibroblast V79 cells. J Toxicol Environ Health A 70(24):2071–2079.  https://doi.org/10.1080/15287390701601251 CrossRefGoogle Scholar
  42. Klavarioti M, Mantzavinos D, Kassinos D (2009) Removal of residual pharmaceuticals from aqueous systems by advanced oxidation processes. Environ Int 35(2):402–417.  https://doi.org/10.1016/j.envint.2008.07.009 CrossRefGoogle Scholar
  43. Kwon JY, Kim HL, Lee JY, Ju YH, Kim JS, Kang SH, Kim YR, Lee JK, Jeong J, Kim MK, Maeng EH, Seo YR (2014) Undetactable levels of genotoxicity of SiO2 nanoparticles in in vitro and in vivo tests. Int J Nanomed 9(Suppl 2):173–1781.  https://doi.org/10.2147/ijn.s57933 Google Scholar
  44. Lajmanovich RC, Cabagna M, Peltzer PM, Stringhini GA, Attademo AM (2005) Micronucleus induction in erythrocytes of the Hyla pulchella tadpoles (Amphibia: Hylidae) exposed to insecticide endosulfan. Mutat Res 10:67–72.  https://doi.org/10.1016/j.mrgentox.2005.08.001 CrossRefGoogle Scholar
  45. Lajmanovich RC, Cabagna Zenklusen M, Attademo AM, Junges CM, Peltzer PM, Bassó A, Lorenzatti E (2014) Induction of micronuclei and nuclear abnormalities in common toad tadpoles (Rhinella arenarum) treated with Liberty® and glufosinate-ammonium. Mutat Res Genet Toxicol Environ Mutagen 15(769):7–12.  https://doi.org/10.1016/j.mrgentox.2014.04.009 CrossRefGoogle Scholar
  46. Landsiedel R, Kapp MD, Schulz M, Wiench K, Oesch F (2009) Genotoxicity investigations on nanomaterials: methods, preparation and characterization of test material, potential artifacts and limitations—many questions, some answers. Mutat Res 681(2–3):241–258.  https://doi.org/10.1016/j.mrrev.2008.10.002 CrossRefGoogle Scholar
  47. Li L, Stoiber M, Wimmer A, Xu Z, Lindenblatt C, Helmreich B, Schuster M (2016) To what extent can full-scale wastewater treatment plant effluent influence the occurrence of silver-based nanoparticles in surface waters? Environ Sci Technol 50:6327–6333.  https://doi.org/10.1021/acs.est.6b00694 CrossRefGoogle Scholar
  48. Lindsey ME, Meyer M, Thurman EM (2001) Analysis of trace levels of sulfonamide and tetracycline antimicrobials in groundwater and surface water using solid-phase extraction and liquid chromatography/mass spectrometry. Anal Chem 73(19):4640–4646.  https://doi.org/10.1021/ac010514w CrossRefGoogle Scholar
  49. Mahdi KNM, Commelin M, Peters RJB, Baartman JEM, Ritsema C, Geissen V (2017) Transport of silver nanoparticles by runoff and erosion—a flume experiment. Sci Total Environ 601–602:1418–1426.  https://doi.org/10.1016/j.scitotenv.2017.06.020 CrossRefGoogle Scholar
  50. Margolin BH, Collings BJ, Mason JM (1983) Statistical analysis and sample- size determinations for mutagenicity experiments with binomial responses. Environ Mutagen 5:705–716.  https://doi.org/10.1002/em.2860050509 CrossRefGoogle Scholar
  51. Martinuzzi C, Peltzer PM, Attademo AM, Junges CM, Lajmanovich RC (2016) Albinism in larvae of the Chacoan frog Leptodactylus chaquensis (Anura, Leptodactylidae) from an urban lake from Argentina. Cuadernos de Herpetología 30(2):69–73Google Scholar
  52. McConnell L, Sparling DW (2010) Emerging contaminants and their potential effects on amphibians and reptiles. In: Sparling DW, Linder G, Bishop C, Krest S (eds) Ecotoxicology of amphibians and reptiles, 2nd edn. SETAC Press, Pensacola, pp 498–513Google Scholar
  53. Melvin SD (2016) Oxidative stress, energy storage, and swimming performance of Limnodynastes peronii tadpoles exposed to a sub-lethal pharmaceutical mixture throughout development. Chemosphere 150:790–797.  https://doi.org/10.1016/j.chemosphere.2015.09.034 CrossRefGoogle Scholar
  54. Munteanu MC, Radu M, Hermenean A, Sima C, Dinu D, Costache M, Grigoriu C, Dinischiotu A (2010) Antioxidative response induced by SiO2 nanoparticles in MRC-5 cell line. Rom Biotech Lett 5(1):5000–5007Google Scholar
  55. Napierska D, Thomassen LCJ, Lison D, Martens JA, Hoet PH (2010) The nanosilica hazard: another variable entity. Fibre Toxicol, Part.  https://doi.org/10.1186/1743-8977-7-39 Google Scholar
  56. Nations S, Long M, Wages M, Maul JD, Theodorakis CW, Cobb GP (2015) Subchronic and chronic developmental effects of copper oxide (CuO) nanoparticles on Xenopus laevis. Chemosphere 135:166–174.  https://doi.org/10.1016/j.chemosphere.2015.03.078 CrossRefGoogle Scholar
  57. Nishimoria H, Kondoha M, Isodaa K, Tsunodabc S, Tsutsumibcd Y, Yagia Y (2009) Silica nanoparticles as hepatotoxicants. Eur J Pharm Biopharm 72(3):496–501.  https://doi.org/10.1016/j.ejpb.2009.02.005 CrossRefGoogle Scholar
  58. Oruç EO, Sevgiler Y, Uner N (2004) Tissue-specific oxidative stress responses in fish exposed to 2,4-D and azinphosmethyl. Comp Biochem Physiol C 137(1):43–51.  https://doi.org/10.1016/j.cca.2003.11.006 CrossRefGoogle Scholar
  59. Ostroumov SA, Kotelevtsev SV (2011) Toxicology of nanomaterials and environment. Ecologica 18:3–10Google Scholar
  60. Pacheco M, Santos MA (1997) Induction of EROD activity and genotoxic effects by polycyclic aromatic hydrocarbons and resin acids on the juvenile eell (Anguilla anguilla L.). Ecotoxicol Environ Saf 38:252–259.  https://doi.org/10.1006/eesa.1997.1585 CrossRefGoogle Scholar
  61. Peltzer PM, Lajmanovich RC, Attademo AM, Junges CM, Teglia CM, Martinuzzi C, Curi L, Culzoni MJ, Goicoechea HC (2017) Ecotoxicity of veterinary enrofloxacin and ciprofloxacin antibiotics on anuran amphibian larvae. Environ Toxicol Pharmacol 51:114–123.  https://doi.org/10.1016/j.etap.2017.01.021 CrossRefGoogle Scholar
  62. Persoone G, Marsalek B, Blinova I, Törökne A, Zarina D, Manusadzianas L, Nalecz-Jawecki G, Tofan L, Stepanova N, Tothova L, Kolar B (2003) A practical and user-friendly toxicity classification system with microbiotests for natural waters and wastewaters. Environ Toxicol 18(6):395–402.  https://doi.org/10.1002/tox.10141 CrossRefGoogle Scholar
  63. Petrache Voicu SN, Dinu D, Sima C, Hermenean A, Ardelean A, Codrici E, Stan MS, Zărnescu O, Dinischiotu A (2015) Silica nanoparticles induce oxidative stress and autophagy but not apoptosis in the MRC-5 cell line. Int J Mol Sci 16(12):29398–29416.  https://doi.org/10.3390/ijms161226171 CrossRefGoogle Scholar
  64. Phan VN, Gomes V, Passos MJACR, Ussami KA, Campos DYF, Rocha AJS, Pereira BA (2007) Biomonitoring of the genotoxic potential (micronucleus and erythrocyte nuclear abnormalities assay) of the Admiralty Bay water surrounding the Brazilian Antarctic Research Station Comandante Ferraz King George Island. Polar Biol 30(2):209–217.  https://doi.org/10.4322/apa.2015.020 CrossRefGoogle Scholar
  65. Ray PC, Yu H, Fu PP (2009) Toxicity and environmental risks of nanomaterials: challenges and future needs. J Environ Sci Health C 27(1):1–35.  https://doi.org/10.1080/10590500802708267 CrossRefGoogle Scholar
  66. Ryu HJ, Seong NW, So BJ, Seo H, Kim JH, Hong JS, Park MK, Kim MS, Kim YR, Cho KB, Seo MY, Kim MK, Maeng EH, Son SW (2014) Evaluation of silica nanoparticle toxicity after topical exposure for 90 days. Int J Nanomed 9(Suppl 2):127–136.  https://doi.org/10.2147/IJN.S57929 Google Scholar
  67. Sajid M, Ilyas M, Basheer C, Tariq M, Daud M, Baig N, Shehzad F (2015) Impact of nanoparticles on human and environment: review of toxicity factors, exposures, control strategies, and future prospects. Environ Sci Pollut Res Int 22(6):4122–4143.  https://doi.org/10.1007/s11356-014-3994-1 CrossRefGoogle Scholar
  68. Salvaterra T, Alves MG, Domingues I, Pereira R, Rasteiro MG, Carvalho RA, Soares AMVM, Lopes I (2013) Biochemical and metabolic effects of a short-term exposure to nanoparticles of titanium silicate in tadpoles of Pelophylax perezi (Seoane). Aquat Toxicol 128–129:190–192.  https://doi.org/10.1016/j.aquatox.2012.12.014 CrossRefGoogle Scholar
  69. Sauvé S, Desrosiers M (2014) A review of what is an emerging contaminant. Chem Cent J 8:15.  https://doi.org/10.1186/1752-153X-8-15 CrossRefGoogle Scholar
  70. Scherzad A, Meyer T, Kleinsasser N, Hackenberg S (2017) Molecular mechanisms of zinc oxide nanoparticle-induced genotoxicity. Materials (Basel) 10:1427.  https://doi.org/10.3390/ma10121427 CrossRefGoogle Scholar
  71. Sferratore A, Garnier J, Billen G, Conley DI, Pinault S (2006) Diffuse and point sources of silica in the Seine River watershed. Environ Sci Technol 40(21):6630–6635.  https://doi.org/10.1021/es060710q CrossRefGoogle Scholar
  72. Sgroi M, Roccaro P, Korshin GV, Vagliasindi FG (2017) Monitoring the behavior of emerging contaminants in wastewater-impacted rivers based on the use of fluorescence excitation emission matrixes (EEM). Environ Sci Technol 51(8):4306–4316.  https://doi.org/10.1021/acs.est.6b05785 CrossRefGoogle Scholar
  73. Shrivastava S, Bera T, Roy A, Singh G, Ramachandrarao P, Dash D (2007) Characterization of enhanced antibacterial effects of novel silver nanoparticles. Nanotechnology 18(22):1–9.  https://doi.org/10.1088/0957-4484/18/22/225103 CrossRefGoogle Scholar
  74. Thompson LB, Carfagno GLF, Andresen K, Sitton AJ, Bury T, Lee LL, Lerner KT, Fong PP (2017) Differential uptake of gold nanoparticles by 2 species of tadpole, the wood frog (Lithobates sylvaticus) and the bullfrog (Lithobates catesbeianus). Environ Toxicol Chem.  https://doi.org/10.1002/etc.3909 (epub ahead of print) Google Scholar
  75. Tiwari DK, Behari J (2009) Biocidal nature of treatment of Ag-nanoparticle and ultrasonic irradiation in Escherichia coli dh5. Adv Biol Res 3(3–4):89–95Google Scholar
  76. U.S.EPA (U.S. Environmental Protection Agency) (1989) Short-term methods for estimating the chronic toxicity of effluents and receiving waters to fresh water organisms, Report EPA/600/4-89/001. Environmental Protection Agency, CincinnatiGoogle Scholar
  77. Vance ME, Kuiken T, Vejerano EP, McGinnis SP, Hochella MF Jr, Rejeski D (2015) Nanotechnology in the real world: redeveloping the nanomaterial consumer products inventory. Beilstein J Nanotechnol 6:1769–1780.  https://doi.org/10.3762/bjnano.6.181 CrossRefGoogle Scholar
  78. Venturino A, Rosenbaum E, Caballero De Castro A, Anguiano O, Gauna L, Fonovich de Schroeder T, Pechen de D’Angelo AM (2003) Biomarkers of effect in toads and frogs. Biomarkers 8(3–4):167–186.  https://doi.org/10.1080/1354700031000120116 CrossRefGoogle Scholar
  79. Wang JJ, Sanderson BJS, Wang H (2007) Cytotoxicity and genotoxicity of ultrafine crystalline SiO2 particulate in cultured human lymphoblastoid cells. Environ Mol Mutagen 48:151–157.  https://doi.org/10.1002/em.20287 CrossRefGoogle Scholar
  80. Wijnhoven SWP, Peijnenburg WJGM, Herberts CA, Hagens WI, Oomen AG, Heugens EHW, Roszek B, Bisschops J, Gosens I, van de Meent D, Dekkers S, de Jong WH, van Zijverden M, Sips AJAM, Geertsma RE (2009) Nano-silver: a review of available data and knowledge gaps in human and environmental risk assessment. Nanotoxicology 3(2):109–138.  https://doi.org/10.1080/17435390902725914 CrossRefGoogle Scholar
  81. Ye RF, Yu XW, Yang SY, Yuan JL, Yang X (2013) Effects of silica dioxide nanoparticles on the embryonic development of zebrafish. Integr Ferroelectr 147:166–174.  https://doi.org/10.1080/10584587.2013.792625 CrossRefGoogle Scholar
  82. Zhang HY, Dunphy DR, Jiang XM, Meng H, Sun BB, Tarn D, Xue M, Wang X, Lin S, Ji Z, Li R, Garcia FL, Yang J, Kirk ML, Xia T, Zink JI, Nel A, Brinker CJ (2012) Processing pathway dependence of amorphous silica nanoparticle toxicity: colloidal vs pyrolytic. J Am Chem Soc 134(38):15790–15804.  https://doi.org/10.1021/ja304907c CrossRefGoogle Scholar

Copyright information

© University of Tehran 2018

Authors and Affiliations

  • Rafael Carlos Lajmanovich
    • 1
    • 2
  • Paola Mariela Peltzer
    • 1
    • 2
  • Candela Soledad Martinuzzi
    • 1
    • 2
  • Andrés Maximiliano Attademo
    • 1
    • 2
  • Carlina Leila Colussi
    • 1
  • Agustín Bassó
    • 1
  1. 1.Ecotoxicology Laboratory, Faculty of Biochemistry and Biological Sciences, FBCB-UNLCiudad UniversitariaSanta FeArgentina
  2. 2.National Council for Scientific and Technical Research (CONICET)Buenos AiresArgentina

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