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The effects of silver nanoparticles on fathead minnow (Pimephales promelas) embryos

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Abstract

Nanoparticles are being used in many commercial applications. We describe the toxicity of two commercial silver (Ag) nanoparticle (NP) products, NanoAmor and Sigma on Pimephales promelas embryos. Embryos were exposed to varying concentrations of either sonicated or stirred NP solutions for 96 h. LC50 values for NanoAmor and Sigma Ag NPs were 9.4 and 10.6 mg/L for stirred and 1.25 and 1.36 mg/L for sonicated NPs, respectively. Uptake of Ag NPs into the embryos was observed after 24 h using Transmission Electron Microscopy and Ag NPs induced a concentration-dependent increase in larval abnormalities, mostly edema. Dissolved Ag released from Ag NPs was measured using Inductively Coupled-Mass Spectrometry and the effects tested were found to be three times less toxic when compared to Ag nitrate (AgNO3). The percentage of dissolved Ag released was inversely proportional to the concentration of Ag NPs with the lowest (0.625 mg/L) and highest (20 mg/L) concentrations tested releasing 3.7 and 0.45% dissolved Ag, respectively and percent release was similar regardless if concentrations were stirred or sonicated. Thus increased toxicity after sonication cannot be solely explained by dissolved Ag. We conclude that both dissolved and particulate forms of Ag elicited toxicity to fish embryos.

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References

  • Ankley GT, Jensen KM, Kahl MD et al (2001) Description and evaluation of a short-term reproduction test with the fathead minnow (Pimephales promelas). Environ Toxicol Chem 20:1276–1290

    Article  CAS  Google Scholar 

  • Asharani PV, Wu YL, Gong Z, Valliyaveettil S et al (2008) Toxicity of silver nanoparticles in zebrafish models. Nanotechnol 19:255102

    Article  CAS  Google Scholar 

  • Baker C, Pradhan A, Pakstis L et al (2005) Synthesis and antibacterial properties of silver nanoparticles. J Nanosci Nanotechnol 5:244–249

    Article  CAS  Google Scholar 

  • Benn TM, Westerhoff P (2008) Nanoparticle silver released into water from commercially available sock fabrics. Environ Sci Technol 42:4133–4139

    Article  CAS  Google Scholar 

  • Blaser SA, Scheringer M, MacLeod M, Hungerbuhler K et al (2008) Estimation of cumulative aquatic exposure and risk due to silver: contribution of nano-functionalized plastics and textiles. Sci Total Environ 360:396–409

    Google Scholar 

  • Braydich-Stolle L, Hussain S, Schlager JJ et al (2005) In vitro cytotoxicity of nanoparticles in mammalian germline stem cells. Toxicol Sci 88:412–419

    Article  CAS  Google Scholar 

  • Brayner R, Ferrari-Iliou R, Brivois N et al (2006) Toxicological impact studies based on Escherichia coli bacteria in ultrafine ZnO nanoparticles colloidal medium. Nano Lett 6:866–870

    Article  CAS  Google Scholar 

  • Brooking J, Davis SS, Illum L (2001) Transport of nanoparticles across the rat nasal mucosa. J Drug Target 9:267–279

    Article  CAS  Google Scholar 

  • Bury NR, Galvez F, Wood CM (1999) Effects of chloride, calcium and dissolved organic carbon on silver toxicity: comparison between rainbow trout and fathead minnows. Environ Toxicol Chem 18:56–62

    Article  CAS  Google Scholar 

  • Chang JS, Chang KL, Hwang DF et al (2007) In vitro cytotoxicitiy of silica nanoparticles at high concentrations strongly depends on the metabolic activity type of the cell line. Environ Sci Technol 41:2064–2068

    Article  CAS  Google Scholar 

  • Chen X, Schluesener HJ (2008) Nanosilver: a nanoproduct in medical application. Toxicol Lett 176:1–12

    Article  CAS  Google Scholar 

  • Cheng D, Yang J, Zhao Y (2004) Antibacterial materials of silver nanoparticles applications in medical appliances and appliances for daily use. Chin Med Equip J 4:26–32

    Google Scholar 

  • Chithrani BD, Chan WC (2007) Elucidating the mechanism of cellular uptake and removal of protein-coated gold nanoparticles of different sizes and shapes. Nano Lett 7:1542–1550

    Article  CAS  Google Scholar 

  • Chithrani BD, Ghazani AA, Chan WC (2006) Determining the size and shape dependence of gold nanoparticle uptake into mammalian cells. Nano Lett 6:662–668

    Article  CAS  Google Scholar 

  • Cohen MS, Stern JN, Vanni AJ et al (2007) In vitro analysis of nanocrystalline silver-coated surgical mesh. Surg Infect 8:397–403

    Article  Google Scholar 

  • Dethloff GM, Naddy RB, Gorsuch JW (2007) Effects of sodium chloride on chronic silver toxicity to early life stages of rainbow trout (Oncorhynchus mykiss). Environ Toxicol Chem 26:1717–1725

    Article  CAS  Google Scholar 

  • Dreher KL (2004) Health and environmental impact of nanotechnology: toxicological assessment of manufactured nanoparticles. Toxicol Sci 77:3–5

    Article  CAS  Google Scholar 

  • Fabrega J, Fawcett SR, Renshaw JC, Lead JR (2009) Silver nanoparticle impact on bacterial growth: effect of pH, concentration, and organic matter. Environ Sci Technol (in press)

  • Ferin J, Oberdorster G, Penney DP (1992) Pulmonary retention of ultrafine and fine particles in rats. Am J Respir Cell Mol Biol 6:535–542

    CAS  Google Scholar 

  • Glover CN, Wood CM (2005) Accumulation and elimination of silver in Daphnia magna and the effect of natural organic matter. Aquat Toxicol 73:406–417

    Article  CAS  Google Scholar 

  • Greulich C, Kittler S, Epple M, Muhr G, Koller M et al (2009) Studies on the biocompatibilty and interaction of silver nanoparticles with human mesnchymal stem cells (hMSCs). Langenbecks Arch Surg 394:495–502

    Article  CAS  Google Scholar 

  • Griffitt RJ, Lu J, Gao J, Bonzongo JC, Barber DS et al (2008) Effects of particle composition and species on toxicity of metallic nanomaterials in aquatic organisms. Environ Toxicol Chem 27:1972–1978

    Article  CAS  Google Scholar 

  • Gustafsson O, Long CM, Macfarlane J et al (2001) Fate of linear alkylbenzenes released to the coastal environment near Boston harbor. Environ Sci Technol 35:2040–2048

    Article  CAS  Google Scholar 

  • Guzman KA, Taylor MR, Banfield JF (2006) Environmental risks of nanotechnology: national nanotechnology initiative funding, 2000–2004. Environ Sci Technol 40:1401–1407

    Article  CAS  Google Scholar 

  • Gwinn MR, Vallyathan V (2006) Nanoparticles: health effects—pros and cons. Environ Health Perspect 114:1818–1825

    CAS  Google Scholar 

  • Handy RD, Shaw BJ (2007) Ecotoxicity of nanomaterials to fish: challenges for ecotoxicity testing. Integr Environ Assess Manag 3:458–460

    Article  CAS  Google Scholar 

  • Hillyer JF, Albrecht RM (2001) Gastrointestinal persorption and tissue distribution of differently sized colloidal gold nanoparticles. J Pharm Sci 90:1927–1936

    Article  CAS  Google Scholar 

  • Hoet PH, Bruske-Hohlfeld I, Salata OV (2004) Nanoparticles—known and unknown health risks. J Nanobiotechnol 2:12

    Article  CAS  Google Scholar 

  • Hogstrand C, Wood CM (1998) Toward a better understanding of the bioavailability, physiology and toxicity of silver in fish: indications for water quality criteria. Environ Toxicol Chem 17:547–561

    Article  CAS  Google Scholar 

  • Hostynek JJ (2003) Factors determining percutaneous metal absorption. Food Chem Toxicol 41:327–345

    Article  CAS  Google Scholar 

  • Huang XL, Zhang B, Ren L et al (2008) In vivo toxic studies and biodistribution of near infrared sensitive Au–Au(2)S nanoparticles as potential drug delivery carriers. J Mater Sci Mater Med 19:2581–2588

    Article  CAS  Google Scholar 

  • Hussain SM, Hess KL, Gearhart JM et al (2005) In vitro toxicity of nanoparticles in BRL 3A rat liver cells. Toxicol In Vitro 19:975–983

    Article  CAS  Google Scholar 

  • Ji JH, Jung JH, Kim SS et al (2007) Twenty-eight-day inhalation toxicity study of silver nanoparticles in Sprague–Dawley rats. Inhal Toxicol 19:857–871

    Article  CAS  Google Scholar 

  • Kane MD, Sringer JA, Iannotti NV et al (2008) Identification of development and tissue-specific gene expression in the fathead minnow Pimephales promelas, rafinesque using computational and DNA microarray methods. J Fish Biol 72:2341–2353

    Article  CAS  Google Scholar 

  • Karn B, Roco MC, Masciangioli T et al (2003) Nanotechnology and the environment. American Chemical Society, Arlington

  • Kashiwada S (2006) Distribution of nanoparticles in the see-through medaka (Oryzias latipes). Environ Health Perspect 114:1697–1702

    CAS  Google Scholar 

  • Kim JS, Kuk E, Yu KN et al (2007) Antimicrobial effects of silver nanoparticles. Nanomedicine 3:95–101

    CAS  Google Scholar 

  • Kim YS, Kim JS, Cho HS et al (2008) Twenty-eight-day oral toxicity, genotoxicity, and gender-related tissue distribution of silver nanoparticles in Sprague–Dawley rats. Inhal Toxicol 20:575–583

    Article  CAS  Google Scholar 

  • Lansdown AB (2006) Silver in healthcare: antimicrobial effects and safety in use. Curr Probl Dermatol 33:17–34

    Article  CAS  Google Scholar 

  • Larkin P, Villeneuve DL, Knoebl I et al (2007) Development and validation of a 2,000-gene microarray for the fathead minnow (Pimephales promelas). Environ Toxicol Chem 26:1497–1506

    Article  CAS  Google Scholar 

  • LeBlanc GA, Mastone JD, Paradice AP et al (1984) The influence of speciation on the toxicity of silver to fathead minnow (Pimephalies promelas). Environ Toxicol Chem 3:37–47

    Article  CAS  Google Scholar 

  • Lee HY, Park HK, Lee WM et al (2007a) A practical procedure for producing silver nanocoated fabric and its antibacterial evaluation for biomedical applications. Chem Commun 28:2959–2961

    Article  CAS  Google Scholar 

  • Lee KJ, Nallathamby PD, Browning LM, Osgood CJ, Xu XH et al (2007b) In vivo imaging of transport and biocompatibility of single silver nanoparticles in early development of zebrafish embryos. ACS Nano 1:133–143

    Article  CAS  Google Scholar 

  • Lemke AE (1981) Interlaboratory comparison acute testing set. United States Environmental Protection Agency, Washington, DC

    Google Scholar 

  • Limbach LK, Li Y, Grass RN et al (2005) Oxide nanoparticle uptake in human lung fibroblasts: effects of particle size, agglomeration, and diffusion at low concentrations. Environ Sci Technol 39:9370–9376

    Article  CAS  Google Scholar 

  • Lok CN, Ho CM, Chen R et al (2007) Silver nanoparticles: partial oxidation and antibacterial activities. J Biol Inorg Chem 12:527–534

    Article  CAS  Google Scholar 

  • Luoma SN (2008) Silver nanotechnologies and the environment: old problemds or new challenges? edn. Woodrow Wilson International Center for Scholars, Project on Emerging Nanotechnologies, The PEW Charitable Trusts, Washington, DC

  • Luoma SN, Ho YB, Bryan GW et al (1995) Fate, bioavailability and toxicity of silver in estuarine environments. Mar Pollut Bull 31:44–54

    Article  CAS  Google Scholar 

  • Masciangioli T, Zhang WX (2003) Environmental technologies at the nanoscale. Environ Sci Technol 37:102A–108A

    Article  CAS  Google Scholar 

  • Maynard AD, Baron PA, Foley M et al (2004) Exposure to carbon nanotube material: aerosol release during the handling of unrefined single walled carbon nanotube material. J Toxicol Environ Health 67:87–107

    Article  CAS  Google Scholar 

  • Morel F, Hering J (1993) Principles and applications of aquatic chemistry. Wiley, New York

    Google Scholar 

  • Morgan IJ, Henry RP, Wood CM (1997) The mechanism of acute silver nitrate toxicity in freshwater rainbow trout Oncorhynchus mykiss is inhibition of gill Na+ and Cl transport. Aquat Toxicol 38:145–163

    Article  CAS  Google Scholar 

  • Morones JR, Elechiguerra JL, Camacho A, Holt K, Kouri JB, Ramirez JT, Yacaman MJ et al (2005) The bactericidal effects of silver nanoparticles. Nanotechnology 16:2346–2353

    Article  CAS  Google Scholar 

  • Murdock RC, Braydich-Stolle L, Schrand AM et al (2008) Characterization of nanomaterial dispersion in solution prior to in vitro exposure using dynamic light scattering technique. Toxicol Sci 101:239–253

    Article  CAS  Google Scholar 

  • Naddy RB, Gorsuch JW, Rehner AB et al (2007a) Chronic toxicity of silver nitrate to Ceriodaphnia dubia and Daphnia magna, and potential mitigating factors. Aquat Toxicol 84:1–10

    Article  CAS  Google Scholar 

  • Naddy RB, Rehner AB, McNerney GR et al (2007b) Comparison of short-term chronic and chronic silver toxicity to fathead minnows in unamended and sodium chloride-amended waters. Environ Toxicol Chem 26:1922–1930

    Article  CAS  Google Scholar 

  • Navarro E, Piccapietra F, Wagner F et al (2008) Toxicity of silver nanoparticles to Chlamydomonas reinhardtii. Environ Sci Technol 42:8959–8964

    Article  CAS  Google Scholar 

  • Nebeker AV, McAuliffe CK, Mshar R et al (1983) Toxicity of silver to steelhead and rainbow trout, fathead minnows and Daphnia magna. Environ Toxicol Chem 2:95–104

    Article  CAS  Google Scholar 

  • Nowack B, Bucheli TD (2007) Occurrence, behavior and effects of nanoparticles in the environment. Environ Pollut 150:5–22

    Article  CAS  Google Scholar 

  • Owen R, Handy RD (2007) Viewpoint: formulating the problems for environmental risk assessment of nanomaterials. Environ Sci Technol 40:5582–5588

    Google Scholar 

  • Pan Y, Neuss S, Leifert A et al (2007) Size-dependent cytotoxicity of gold nanoparticles. Small 11:1941–1949

    Article  CAS  Google Scholar 

  • Rejman J, Oberle V, Zuhorn IS et al (2004) Size-dependent internalization of particles via the pathways of clathrin- and caveolae-mediated endocytosis. Biochem J 377:159–169

    Article  CAS  Google Scholar 

  • Roberts ES, Malstrom SE, Dreher KL (2007) In situ pulmonary localization of air pollution particle-induced oxidative stress. J Toxicol Environ Health A 70:1929–1935

    Article  CAS  Google Scholar 

  • Roco MC (2003) Nanotechnology: convergence with modern biology and medicine. Curr Opin Biotechnol 14:337–346

    Article  CAS  Google Scholar 

  • Roco MC (2005) Environmentally responsible development of nanotechnology. Environ Sci Technol 39:106A–112A

    Article  CAS  Google Scholar 

  • Salata O (2004) Applications of nanoparticles in biology and medicine. J Nanobiotechnol 2:3

    Article  Google Scholar 

  • Schins RP (2002) Mechanisms of genotoxicity of particles and fibers. Inhal Toxicol 14:57–78

    Article  CAS  Google Scholar 

  • Schnizler MK, Bogdan R, Bennert A et al (2007) Short-term exposure to waterborne free silver has acute effects on membrane current of Xenopus oocytes. Biochim Biophys Acta 1768:317–323

    Article  CAS  Google Scholar 

  • Service RF (2003) Nanomaterials show signs of toxicity. Science 300:243

    Article  Google Scholar 

  • Sondi I, Salopek-Sondi B (2004) Silver nanoparticles as antimicrobial agent: a case study on E. coli as a model for gram-negative bacteria. J Colloid Interface Sci 275:177–182

    Article  CAS  Google Scholar 

  • Suzuki H, Toyooka T, Ibuki Y (2007) Simple and easy method to evaluate uptake potential of nanoparticles in mammalian cells using a flow cytometric light scatter analysis. Environ Sci Technol 41:3018–3024

    Article  CAS  Google Scholar 

  • Takenaka S, Karg E, Roth C et al (2001) Pulmonary and systemic distribution of inhaled ultrafine silver particles in rats. Environ Health Perspect 109:547–551

    Article  CAS  Google Scholar 

  • Terharr C, Ewell W, Dziuba S et al (1972) Toxicity of photographic processing chemicals to fish. Photogr Sci Eng 16:370–377

    Google Scholar 

  • USEPA (1994) Users guide for probit analysis of data from acute and short-term chronic toxicity tests with aquatic organisms. Biological Methods Branch, USEPA, Cincinnati, OH

    Google Scholar 

  • Wood C, Hogstrand C, Galvez F et al (1996) The physiology of waterborne silver toxicity in freshwater rainbow trout (Oncorhynchus mykiss): the effect of ionic Ag+. Aquat Toxicol 35:93–109

    Article  CAS  Google Scholar 

  • Yu C, Zhao J, Guo Y et al (2008) A novel method to prepare water-dispersible magnetic nanoparticles and their biomedical applications: magnetic capture probe and specific cellular uptake. J Biomed Mater Res 2:364–372

    Article  CAS  Google Scholar 

  • Zhu S, Oberdorster E, Haasch ML (2006) Toxicity of an engineered nanoparticle (fullerene, C60) in two aquatic species, Daphnia and fathead minnow. Mar Environ Res 62(Suppl):S5–S9

    Article  CAS  Google Scholar 

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Acknowledgments

We would like to thank Bob Rode, laboratory manager for the aquatic research facility and many students (Nathan Barton, Sonia Johns, Lynn Henneberger, Brett Lowry, Aaron McAlexander, Reid Morehouse, and Brian Sanchez) for their help with the maintenance of the fathead minnow colony. The authors would also like to thank Gary Ankley and Dan Villeneuve (USEPA, Mid-Continent Ecology Division, Duluth, MN) and James Lazorchack and Marke Smith (USEPA, Molecular Indicator Research Branch, Cincinnati, OH) for donating fathead minnow adults that were used to establish our breeding colony. We also thank Steve Sassman and Dr. Nicole Ramlachan (Purdue University) for assistance with LC-MS and data analysis. This work was supported by a grant from the Lilly Endowment, Inc. awarded through Purdue University Center for the Environment at Discovery Park.

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Correspondence to Maria S. Sepúlveda.

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Laban, G., Nies, L.F., Turco, R.F. et al. The effects of silver nanoparticles on fathead minnow (Pimephales promelas) embryos. Ecotoxicology 19, 185–195 (2010). https://doi.org/10.1007/s10646-009-0404-4

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  • DOI: https://doi.org/10.1007/s10646-009-0404-4

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