Isotopically modified silver nanoparticles to assess nanosilver bioavailability and toxicity at environmentally relevant exposures

Marie-Noële Croteau; Agnieszka D. Dybowska; Samuel N. Luoma; Superb K. Misra; Eugenia Valsami-Jones

doi:10.1071/EN13141

RESEARCH FRONT

Isotopically modified silver nanoparticles to assess nanosilver bioavailability and toxicity at environmentally relevant exposures

Marie-Noële Croteau ^A ^E , Agnieszka D. Dybowska ^B , Samuel N. Luoma ^A ^C , Superb K. Misra ^B ^D and Eugenia Valsami-Jones ^B ^D

+ Author Affiliations

- Author Affiliations

^A US Geological Survey, 345 Middlefield Road, MS 496, Menlo Park, CA 94025, USA.

^B Department of Earth Sciences, Natural History Museum, Cromwell Road, London, SW7 5BD, UK.

^C John Muir Institute of the Environment, University of California, One Shields Avenue, Davis, CA 95616, USA.

^D School of Geography, Earth and Environmental Sciences, University of Birmingham, Birmingham, B15 2TT, UK.

^E Corresponding author: mcroteau@usgs.gov

Environmental Chemistry 11(3) 247-256 https://doi.org/10.1071/EN13141
Submitted: 24 July 2013 Accepted: 1 November 2013 Published: 20 May 2014

Environmental context. Predicting the environmental implications of nanotechnology is complex in part because of the difficulty in studying nanoparticle uptake in organisms at environmentally realistic exposures. Typically, high exposure concentrations are needed to detect accumulation and effects. We use labelled Ag nanoparticles to determine whether Ag bioaccumulation responses are linear over concentrations likely to occur in the environment, and whether concentration-dependent changes in agglomeration and dissolution affect bioavailability.

Abstract. A major challenge in understanding the environmental implications of nanotechnology lies in studying nanoparticle uptake in organisms at environmentally realistic exposure concentrations. Typically, high exposure concentrations are needed to trigger measurable effects and to detect accumulation above background. But application of tracer techniques can overcome these limitations. Here we synthesised, for the first time, citrate-coated Ag nanoparticles using Ag that was 99.7 % ¹⁰⁹Ag. In addition to conducting reactivity and dissolution studies, we assessed the bioavailability and toxicity of these isotopically modified Ag nanoparticles (¹⁰⁹Ag NPs) to a freshwater snail under conditions typical of nature. We showed that accumulation of ¹⁰⁹Ag from ¹⁰⁹Ag NPs is detectable in the tissues of Lymnaea stagnalis after 24-h exposure to aqueous concentrations as low as 6 ng L^–1 as well as after 3 h of dietary exposure to concentrations as low as 0.07 μg g^–1. Silver uptake from unlabelled Ag NPs would not have been detected under similar exposure conditions. Uptake rates of ¹⁰⁹Ag from ¹⁰⁹Ag NPs mixed with food or dispersed in water were largely linear over a wide range of concentrations. Particle dissolution was most important at low waterborne concentrations. We estimated that 70 % of the bioaccumulated ¹⁰⁹Ag concentration in L. stagnalis at exposures <0.1 µg L^–1 originated from the newly solubilised Ag. Above this concentration, we predicted that 80 % of the bioaccumulated ¹⁰⁹Ag concentration originated from the ¹⁰⁹Ag NPs. It was not clear if agglomeration had a major influence on uptake rates.

References

[1] F. Gottschalk, T. Sonderer, R. W. Scholz, B. Nowack, Modeled environmental concentrations of engineered nanomaterials (TiO2, ZnO, Ag, CNT, fullerenes) for different regions. Environ. Sci. Technol. 2009, 43, 9216.
| Modeled environmental concentrations of engineered nanomaterials (TiO₂, ZnO, Ag, CNT, fullerenes) for different regions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlyhtL%2FP&md5=a8a5454d70978de5af6ee6d145a26961CAS | 20000512PubMed |

[2] F. Gottschalk, T. Y. Sun, B. Nowack, Environmental concentrations of engineered nanomaterials: review of modeling and analytical studies. Environ. Pollut. 2013, 181, 287.
| Environmental concentrations of engineered nanomaterials: review of modeling and analytical studies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFSlsrfP&md5=7be267556cba6b63f2cffd78eb64df51CAS | 23856352PubMed |

[3] S. N. Luoma, Old problems or new challenges, in PEN 15 – Silver nanotechnologies and the environment 2008 (Woodrow Wilson International Center for Scholars). Available at http://www.nanotechproject.org/process/assets/files/7036/nano_pen_15_final.pdf [Verified 19 December 2013].

[4] A. Bradford, R. D. Handy, J. W. Readman, A. Atfield, M. Muhling, Impact of silver nanoparticle contamination of natural bacterial assemblages in estuarine sediments. Environ. Sci. Technol. 2009, 43, 4530.
| Impact of silver nanoparticle contamination of natural bacterial assemblages in estuarine sediments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlt1SgurY%3D&md5=cfa973ebd665d74830f7b7c63e3b57cfCAS | 19603673PubMed |

[5] P. V. Asharani, Y. L. Wu, Z. Gong, S. Valiyaveettil, Toxicity of silver nanoparticles in zebrafish models. Nanotechnology 2008, 19, 1.

[6] O. Choi, T. E. Clevenger, B. Deng, R. Y. Surampalli, L. Ross, Z. Hu, Role of sulfide and ligand strength in controlling nanosilver toxicity. Water Res. 2009, 43, 1879.
| Role of sulfide and ligand strength in controlling nanosilver toxicity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXktVCmtb0%3D&md5=c5c4b2970d344e4830a7adb4f756ac72CAS | 19249075PubMed |

[7] J. N. Meyer, C. A. Lord, X. Y. Yang, E. A. Turner, A. R. Badireddy, S. M. Marinakos, A. Chilkoti, M. R. Wiesner, M. Auffan, Intracellular uptake and associated toxicity of silver nanoparticles in Caenorhabditis elegans. Aquat. Toxicol. 2010, 100, 140.
| Intracellular uptake and associated toxicity of silver nanoparticles in Caenorhabditis elegans.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFGjs7bI&md5=40459a41abbeb56b27471610585121bdCAS | 20708279PubMed |

[8] K. J. Lee, P. D. Nallathamby, L. M. Browning, C. J. Osgood, X.-H. N. Xu, In vivo imaging of transport and biocompatibility of single silver nanoparticles in early development of zebrafish embryos. ACS Nano 2007, 1, 133.
| In vivo imaging of transport and biocompatibility of single silver nanoparticles in early development of zebrafish embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFSnsL%2FF&md5=616c585701371085f8c3a940a3ea9749CAS | 19122772PubMed |

[9] A. H. Ringwood, M. McCarthy, T. C. Bates, D. L. Carroll, The effects of silver nanoparticles on oyster embryos. Mar. Environ. Res. 2010, 69, S49.
| The effects of silver nanoparticles on oyster embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1OgtLjK&md5=b9a47a3b81a02d0749b34a87c01c6e78CAS | 19913905PubMed |

[10] P. Borm, F. C. Klaessing, T. D. Landry, B. Moudgil, J. Pauluhn, K. Thomas, R. Trottier, S. Wood, Research strategies for safety evaluation of nanomaterials, Part V. Role of dissolution in biological fate and effects of nanoscale particles. Toxicol. Sci. 2005, 90, 23.
| Research strategies for safety evaluation of nanomaterials, Part V. Role of dissolution in biological fate and effects of nanoscale particles.Crossref | GoogleScholarGoogle Scholar |

[11] N. M. Franklin, N. J. Rogers, S. C. Apte, G. E. Batley, G. E. Gadd, P. S. Casey, Comparative toxicity of nanoparticulate ZnO, bulk ZnO, and ZnCl2 to a freshwater microalga (Pseudokirchneriella subcapitata): the importance of particle solubility. Environ. Sci. Technol. 2007, 41, 8484.
| Comparative toxicity of nanoparticulate ZnO, bulk ZnO, and ZnCl₂ to a freshwater microalga (Pseudokirchneriella subcapitata): the importance of particle solubility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlWqs7fF&md5=e1d09d97f81f4af57461dee3fda4397cCAS | 18200883PubMed |

[12] N. Maximova, O. Dahl, Environmental implications of aggregation phenomena: current understanding. Curr. Opin. Colloid Interface Sci. 2006, 11, 246.
| Environmental implications of aggregation phenomena: current understanding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1WltLfJ&md5=b4340dcc4bdfa51d8d21ad1e57249981CAS |

[13] T. Phenrat, N. Saleh, K. Sirk, R. D. Tilton, G. V. Lowry, Aggregation and sedimentation of aqueous nanoscale zerovalent iron dispersions. Environ. Sci. Technol. 2007, 41, 284.
| Aggregation and sedimentation of aqueous nanoscale zerovalent iron dispersions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlCit7nJ&md5=37c25286b70e843ec7c9d65450ba0592CAS | 17265960PubMed |

[14] M. Baalousha, Aggregation and disaggregation of iron oxide nanoparticles: influence of particle concentration, pH and natural organic matter. Sci. Total Environ. 2009, 407, 2093.
| Aggregation and disaggregation of iron oxide nanoparticles: influence of particle concentration, pH and natural organic matter.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXit1Sjtb0%3D&md5=15fb8a6d2577e2d5c29fbf6d2f99c636CAS | 19059631PubMed |

[15] A. D. Dybowska, M.-N. Croteau, S. K. Misra, D. Berhanu, S. N. Luoma, P. Christian, P. O'Brien, E. Valsami-Jones, Synthesis of isotopically modified ZnO nanoparticles and their potential as nanotoxicity tracers. Environ. Pollut. 2011, 159, 266.
| Synthesis of isotopically modified ZnO nanoparticles and their potential as nanotoxicity tracers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVahtbbJ&md5=12a90971ba4a12e2c21e19e620d086b1CAS | 20940078PubMed |

[16] S. K. Misra, A. D. Dybowska, D. Berhanu, M.-N. Croteau, S. N. Luoma, A. R. Boccaccini, E. Valsami-Jones, Isotopically modified nanoparticles for enhanced detection in bioaccumulation studies. Environ. Sci. Technol. 2012, 46, 1216.
| Isotopically modified nanoparticles for enhanced detection in bioaccumulation studies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFygt7nM&md5=6e8853378afe863c963c87923be87ce1CAS | 22148182PubMed |

[17] S. N. Luoma, P. S. Rainbow, Why is metal bioaccumulation so variable? Biodynamics as a unifying concept. Environ. Sci. Technol. 2005, 39, 1921.
| Why is metal bioaccumulation so variable? Biodynamics as a unifying concept.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhsF2ntLY%3D&md5=49d172ac5f9cf8e286b6c9b841488fbfCAS | 15871220PubMed |

[18] G. Blackmore, W.-X. Wang, Uptake and efflux of Cd and Zn by the green mussel Perna viridis after metal preexposure. Environ. Sci. Technol. 2002, 36, 989.
| Uptake and efflux of Cd and Zn by the green mussel Perna viridis after metal preexposure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmsVGisg%3D%3D&md5=bebe9998f3cfe9ab02b781e25833389fCAS | 11918030PubMed |

[19] D. S. Shi, G. Blackmore, W.-X. Wang, Effects of aqueous and dietary preexposure and resulting body burden on silver biokinetics in the green mussel Perna viridis. Environ. Sci. Technol. 2003, 37, 936.
| Effects of aqueous and dietary preexposure and resulting body burden on silver biokinetics in the green mussel Perna viridis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXms1yrug%3D%3D&md5=5ba4adfd427922f42de01dbab5104571CAS |

[20] M.-N. Croteau, S. N. Luoma, B. R. Topping, C. B. Lopez, Stable metal isotopes reveal copper accumulation and loss dynamics in the freshwater bivalve Corbicula. Environ. Sci. Technol. 2004, 38, 5002.
| Stable metal isotopes reveal copper accumulation and loss dynamics in the freshwater bivalve Corbicula.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmvVyqtbw%3D&md5=b3f909f30533a0f940634ae7b327e778CAS | 15506192PubMed |

[21] M.-N. Croteau, D. J. Cain, C. C. Fuller, Novel and nontraditional use of stable isotope tracers to study metal bioavailability from natural particles. Environ. Sci. Technol. 2013, 47, 3424.
| 1:CAS:528:DC%2BC3sXjsVWrtLk%3D&md5=3dfc6a4b4f26613239864978b70aa592CAS | 23458345PubMed |

[22] W.-X. Wang, N. S. Fisher, S. N. Luoma, Kinetic determinations of trace element bioaccumulation in the mussel Mytilus edulis. Mar. Ecol. Prog. Ser. 1996, 140, 91.
| Kinetic determinations of trace element bioaccumulation in the mussel Mytilus edulis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XmtlKjt70%3D&md5=751aa0518b18041ed77a474dbff5ceffCAS |

[23] R. Cornelis, Use of radiochemical methods as tools for speciation purposes in environmental and biological sciences. Analyst 1992, 117, 583.
| Use of radiochemical methods as tools for speciation purposes in environmental and biological sciences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xis1Oquro%3D&md5=7d616ef2b0836d257c288245034b4c67CAS | 1580405PubMed |

[24] S. Stürup, H. R. Hansen, P. Gammelgarrd, Application of enriched stable isotopes as tracers in biological systems: a critical review. Anal. Bioanal. Chem. 2008, 390, 541.
| Application of enriched stable isotopes as tracers in biological systems: a critical review.Crossref | GoogleScholarGoogle Scholar | 17917720PubMed |

[25] M.-N. Croteau, S. N. Luoma, B. Pellet, Determining metal assimilation efficiency in aquatic invertebrates using enriched stable metal isotope tracers. Aquat. Toxicol. 2007, 83, 116.
| Determining metal assimilation efficiency in aquatic invertebrates using enriched stable metal isotope tracers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlsFKjt70%3D&md5=9d4587e3e8ba042713e34ef85c7cc13cCAS | 17467071PubMed |

[26] D. J. Cain, M.-N. Croteau, S. N. Luoma, Bioaccumulation dynamics and exposure routes of Cd and Cu among species of aquatic mayflies. Environ. Toxicol. Chem. 2011, 30, 2532.
| Bioaccumulation dynamics and exposure routes of Cd and Cu among species of aquatic mayflies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtl2gur%2FK&md5=6c4e58dd6f9e7ec97ec4c9a202ead67aCAS |

[27] M.-N. Croteau, A. D. Dybowska, S. N. Luoma, E. Valsami-Jones, A novel approach reveals that zinc oxide nanoparticles are bioavailable and toxic after dietary exposures. Nanotoxicology 2011, 5, 79.
| A novel approach reveals that zinc oxide nanoparticles are bioavailable and toxic after dietary exposures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVKqsrvI&md5=3379a0b752337de8e4a8a4756aadb045CAS | 21417690PubMed |

[28] D. J. Cain, M.-N. Croteau, C. C. Fuller, Dietary bioavailability of Cu adsorbed to colloidal hydrous ferric oxide. Environ. Sci. Technol. 2013, 47, 2869.
| Dietary bioavailability of Cu adsorbed to colloidal hydrous ferric oxide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXitl2ks7c%3D&md5=febf28cded63b430debed55a800c20e9CAS | 23402601PubMed |

[29] B. Gulson, M. McCall, M. Korsch, L. Gomez, P. Casey, Y. Oytam, A. Taylor, M. McCulloch, J. Trotter, L. Kinsley, G. Greenoak, Small amounts of zinc oxide particles in sunscreens applied outdoors are absorbed through human skin. Toxicol. Sci. 2010, 118, 140.
| Small amounts of zinc oxide particles in sunscreens applied outdoors are absorbed through human skin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlSmtbnE&md5=f1bf11b9fce05478984ee16b95691081CAS | 20705894PubMed |

[30] F. Larner, Y. Dogra, A. Dybowska, J. Fabrega, B. Stolpe, L. J. Bridgestock, R. Goodhead, D. J. Weiss, J. Moger, J. R. Lead, E. Valsami-Jones, C. R. Tyler, T. S. Galloway, M. Rehkamper, Tracing bioavailability of ZnO nanoparticles using stable isotope labeling. Environ. Sci. Technol. 2012, 46, 12137.
| Tracing bioavailability of ZnO nanoparticles using stable isotope labeling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVyltb7F&md5=a3d8653c7725588a2074147f2d1c7197CAS | 23050854PubMed |

[31] F. R. Khan, A. Laycock, A. Dybowska, F. Larner, B. D. Smith, P. S. Rainbow, S. N. Luoma, M. Rehkamper, E. Valsami-Jones, Stable isotope tracer to determine uptake and efflux dynamics of ZnO nano- and bulk particles and dissolved Zn to an estuarine snail. Environ. Sci. Technol. 2013, 47, 8532.
| 1:CAS:528:DC%2BC3sXhtVWhurzJ&md5=b8362b5b25c17114c1fea03b3e1f5cf4CAS | 23802799PubMed |

[32] M.-N. Croteau, S. K. Misra, S. N. Luoma, E. Valsami-Jones, Silver bioaccumulation dynamics in a freshwater invertebrate after aqueous and dietary exposures to nanosized and ionic Ag. Environ. Sci. Technol. 2011, 45, 6600.
| Silver bioaccumulation dynamics in a freshwater invertebrate after aqueous and dietary exposures to nanosized and ionic Ag.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXosVSrsr8%3D&md5=e530ba987072b8b611f3a72f2ed26bc2CAS | 21667957PubMed |

[33] Methods for Measuring the Acute Toxicity pf Effluents and Receiving Waters to freshwater and Marine Organisms, EPA-821-R-02–012 2002 (US Environmental Protection Agency: Washington, DC).

[34] D. L. Parkust, C. A. J. Appelo, User’s guide to PHREEQC (version 2) – a computer program for speciation, batch-reaction, onedimensional transport, and inverse geochemical calculations. Water Resources Investigative Report 99–4259 1999 (US Geological Survey, Denver, CO).

[35] E. C. Irving, D. J. Baird, J. M. Culp, Ecotoxicological responses of the mayfly Baetis tricaudatus to dietary and waterborne cadmium: implications for toxicity testing. Environ. Toxicol. Chem. 2003, 22, 1058.
| 1:CAS:528:DC%2BD3sXjtFCmsro%3D&md5=8e32d9ab4ee381a91e97077dedb3c608CAS | 12729215PubMed |

[36] W.-X. Wang, N. S. Fisher, Assimilation efficiencies of chemical contaminants in aquatic invertebrates: a synthesis. Environ. Toxicol. Chem. 1999, 18, 2034.
| Assimilation efficiencies of chemical contaminants in aquatic invertebrates: a synthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXls1Sqs7g%3D&md5=737d8b3c49ae3f256416bff18e94b265CAS |

[37] S. N. Luoma, P. S. Rainbow, Metal Contamination in Aquatic Environments: Science and Lateral Management 2008 (Cambridge University Press: Cambridge, UK).

[38] R. C. Doty, T. R. Tshikhudo, M. Brust, D. G. Fernig, Extremely stable water-soluble Ag nanoparticles. Chem. Mater. 2005, 17, 4630.
| Extremely stable water-soluble Ag nanoparticles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXntVChtr4%3D&md5=8c5d336b3ec66a1e3ab7fc7a0e340f09CAS |

[39] J. Liu, R. Hurt, Ion release kinetics and particle persistence in aqueous nano-silver colloids. Environ. Sci. Technol. 2010, 44, 2169.
| Ion release kinetics and particle persistence in aqueous nano-silver colloids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXit1Wqsrc%3D&md5=eda8eefb62b5e038312ad7a39ce5d935CAS | 20175529PubMed |

[40] S. Kittler, C. Greulich, J. Diendorf, M. Koller, M. Epple, Toxicity of silver nanoparticles increases during storage because of slow dissolution under release of silver ions. Chem. Mater. 2010, 22, 4548.
| Toxicity of silver nanoparticles increases during storage because of slow dissolution under release of silver ions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpsV2ltbo%3D&md5=22d2ff31e22b7d8515908241adbb5e5aCAS |

[41] J. Y. Liu, D. A. Sonshine, S. Shervani, R. H. Hurt, Controlled release of biologically active silver from nanosilver surfaces. ACS Nano 2010, 4, 6903.
| Controlled release of biologically active silver from nanosilver surfaces.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlaitb3L&md5=f74a2c9fb88e9b8a96314791af98dfb3CAS |

[42] X. A. Li, J. J. Lenhart, Aggregation and dissolution of silver nanoparticles in natural surface water. Environ. Sci. Technol. 2012, 46, 5378.
| Aggregation and dissolution of silver nanoparticles in natural surface water.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XlsFemsLk%3D&md5=609388f4bb944bc4f5c354e4018e892fCAS |

[43] C. M. Ho, S. K. W. Yau, C. N. Lok, M. H. So, C. M. Che, Oxidative dissolution of silver nanoparticles by biologically relevant oxidants: a kinetic and mechanistic study. Chem. Asian J. 2010, 5, 285.
| Oxidative dissolution of silver nanoparticles by biologically relevant oxidants: a kinetic and mechanistic study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVGqsLY%3D&md5=9f8694e62338e431765a66c0ca056615CAS | 20063340PubMed |

[44] W. Zhang, Y. Yao, N. Sullivan, Y. Chen, Modeling the primary size effects of citrate-coated silver nanoparticles on their ion release kinetics. Environ. Sci. Technol. 2011, 45, 4422.
| Modeling the primary size effects of citrate-coated silver nanoparticles on their ion release kinetics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXltVGgsb0%3D&md5=dbb9e1cadbe810bbc0df0c57b73c3d95CAS | 21513312PubMed |

[45] M. Hadioui, S. Leclerc, K. J. Wilkinson, Multimethod quantification of Ag+ release from nanosilver. Talanta 2013, 105, 15.
| Multimethod quantification of Ag⁺ release from nanosilver.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmt1WjurY%3D&md5=a2cd9d269a709af1c2d216816cd619e6CAS | 23597981PubMed |

[46] A. M. El Badawy, T. D. Luxton, R. G. Silva, K. G. Scheckel, M. T. Suidan, T. M. Talaymat, Impact of environmental conditions (pH, ionic strength, and electrolyte type) on the surface charge and aggregation of silver nanoparticles suspensions. Environ. Sci. Technol. 2010, 44, 1260.
| Impact of environmental conditions (pH, ionic strength, and electrolyte type) on the surface charge and aggregation of silver nanoparticles suspensions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXptl2qtg%3D%3D&md5=6edf1d6fd0c8d4db699b6aca49a9f591CAS | 20099802PubMed |

[47] K. A. Huynh, K. L. Chen, Aggregation kinetics of citrate and polyvinylpyrrolidone coated silver nanoparticles in monovalent and divalent electrolyte solutions. Environ. Sci. Technol. 2011, 45, 5564.
| Aggregation kinetics of citrate and polyvinylpyrrolidone coated silver nanoparticles in monovalent and divalent electrolyte solutions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmvVWkurw%3D&md5=8a7b8461f4e3ad391fdbbb7119cdbcecCAS | 21630686PubMed |

[48] X. A. Li, J. J. Lenhart, H. W. Walker, Dissolution-accompanied aggregation kinetics of silver nanoparticles. Langmuir 2010, 26, 16690.
| Dissolution-accompanied aggregation kinetics of silver nanoparticles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1ahtbbN&md5=5bdfe4601f8800f0443d5ed66c43294dCAS |

[49] X. A. Li, J. J. Lenhart, H. W. Walker, Aggregation kinetics and dissolution of coated silver nanoparticles. Langmuir 2012, 28, 1095.
| Aggregation kinetics and dissolution of coated silver nanoparticles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsF2lsLvL&md5=67c234af5c1b3e895d938921df686cd0CAS |

[50] C. Levard, E. M. Hotze, G. V. Lowry, G. E. Brown, Environmental transformations of silver nanoparticles: impact on stability and toxicity. Environ. Sci. Technol. 2012, 46, 6900.
| Environmental transformations of silver nanoparticles: impact on stability and toxicity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XitlGjt7o%3D&md5=4dae6e02caa0d9ab4a861e91882a1b9dCAS | 22339502PubMed |

[51] C. N. Lok, C. M. Ho, R. Chen, Q. Y. He, W. Y. Yu, H. Sun, P. K. H. Tam, J. F. Chiu, C. M. Che, Silver nanoparticles: partial oxidation and antibacterial activities. J. Biol. Inorg. Chem. 2007, 12, 527.
| Silver nanoparticles: partial oxidation and antibacterial activities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkvVaitLc%3D&md5=4edecd2af31c043e8d3dcccd68d342feCAS | 17353996PubMed |

[52] L. Kvitek, A. Panacek, J. Soukupova, M. Kolar, R. Vecerova, R. Prucek, M. Holecova, R. Zboril, Effect of surfactants and polymers on stability and antibacterial activity of silver nanopartciles (NPs). J. Phys. Chem. C 2008, 112, 5825.
| Effect of surfactants and polymers on stability and antibacterial activity of silver nanopartciles (NPs).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjsF2rsL0%3D&md5=f70b0937c1446fdc3b7100e6247fef3fCAS |

[53] F. R. Khan, S. K. Misra, J. Garcia-Alonso, B. D. Smith, S. Strekopytov, P. S. Rainbow, S. N. Luoma, E. Valsami-Jones, Bioaccumulation dynamics and modeling in an estuarine invertebrate following aqueous exposure to nanosized and dissolved silver. Environ. Sci. Technol. 2012, 46, 7621.
| Bioaccumulation dynamics and modeling in an estuarine invertebrate following aqueous exposure to nanosized and dissolved silver.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XosFersrg%3D&md5=99eb60bd4c9ee5e253469d3e0566f06fCAS | 22697255PubMed |

[54] C. L. Brown, F. Parchaso, J. K. Thompson, S. N. Luoma, Assessing toxicant effects in a complex estuary: a case of study of effects of silver on reproduction in the bivalve, Potamocorbula amurensis, in San Francisco Bay. Hum. Ecol. Risk Assess. 2003, 9, 95.
| Assessing toxicant effects in a complex estuary: a case of study of effects of silver on reproduction in the bivalve, Potamocorbula amurensis, in San Francisco Bay.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXitlWjt70%3D&md5=ee3ed45fef9ed3e8eaf78c5b761cf2a4CAS |

[55] J. K. Böhlke, J. R. de Laeter, P. De Bièvre, H. Hidaka, H. S. Peiser, K. J. R. Rosman, P. D. P. Taylor, Isotopic compositions of the elements, 2001. J. Phys. Chem. Ref. Data 2005, 34, 57.
| Isotopic compositions of the elements, 2001.Crossref | GoogleScholarGoogle Scholar |