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

Environmental Chemistry

Volumn 11, Issue 3, 2014, Pages 247-256

  Croteau, Marie Noële ^a   Dybowska, Agnieszka D ^b   Luoma, Samuel N ^a,c   Misra, Superb K ^b,d   Valsami Jones, Eugenia ^b,d  

^a U S GEOLOGICAL SURVEY   (United States)

^b DEPARTMENT OF LIFE SCIENCES   (United Kingdom)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BIOAVAILABILITY; BIOLOGICAL UPTAKE; CONCENTRATION (COMPOSITION); DISSOLUTION; ECOTOXICOLOGY; FRESHWATER ENVIRONMENT; NANOTECHNOLOGY; PARTICLE SIZE; POLLUTION EXPOSURE; SILVER; SNAIL; TOXICITY TEST;

EID: 84903279798     PISSN: 14482517     EISSN: None     Source Type: Journal    
DOI: 10.1071/EN13141     Document Type: Article

References (55)

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. doi.:10.1021/ES9015553
2. F. Gottschalk, T. Y. Sun, B. Nowack, Environmental concentrations of engineered nanomaterials: Review of modeling and analytical studies. Environ. Pollut. 2013, 181, 287. doi.:10.1016/J.ENVPOL. 2013.06.003
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. doi.:10.1021/ ES9001949
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 Jr, Z. Hu, Role of sulfide and ligand strength in controlling nanosilver toxicity. Water Res. 2009, 43, 1879. doi.:10.1016/J.WATRES.2009.01.029
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. doi.:10.1016/J.AQUATOX.2010.07.016
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. doi.:10.1021/NN700048Y
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. doi.:10.1016/J.MARENVRES.2009.10.011
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. doi.:10.1093/TOXSCI/KFJ084
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. doi.:10.1021/ ES071445R
12. N. Maximova, O. Dahl, Environmental implications of aggregation phenomena: Current understanding. Curr. Opin. Colloid Interface Sci. 2006, 11, 246. doi.:10.1016/J.COCIS.2006.06.001
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. doi.:10.1021/ES061349A
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. doi.:10.1016/ J.SCITOTENV.2008.11.022
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. doi.:10.1016/ J.ENVPOL.2010.08.032
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. doi.:10.1021/ES2039757
17. S. N. Luoma, P. S. Rainbow, Why is metal bioaccumulation so variablé Biodynamics as a unifying concept. Environ. Sci. Technol. 2005, 39, 1921. doi.:10.1021/ES048947E
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. doi.:10.1021/ES0155534
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. doi.:10.1021/ES025929T
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. doi.:10.1021/ES049432Q
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
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. doi.:10.3354/MEPS140091
23. R. Cornelis, Use of radiochemical methods as tools for speciation purposes in environmental and biological sciences. Analyst 1992, 117, 583. doi.:10.1039/AN9921700583
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. doi.:10.1007/S00216- 007-1638-8
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. doi.:10.1016/ J.AQUATOX.2007.03.016
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. doi.:10.1002/ETC.663
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. doi.:10.3109/17435390.2010.501914
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. doi.:10.1021/ES3044856
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. doi.:10.1093/TOXSCI/KFQ243
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. doi.:10.1021/ ES302602J
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
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. doi.:10.1021/ES200880C
33. Methods for Measuring the Acute Toxicity pf Effluents and Receiving Waters to freshwater and Marine Organisms, EPA-821-R-02-012 (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
36. W.-X. Wang, N. S. Fisher, Assimilation efficiencies of chemical contaminants in aquatic invertebrates: A synthesis. Environ. Toxicol. Chem. 1999, 18, 2034. doi.:10.1002/ETC.5620180923
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. doi.:10.1021/CM0508017
39. J. Liu, R. Hurt, Ion release kinetics and particle persistence in aqueous nano-silver colloids. Environ. Sci. Technol. 2010, 44, 2169. doi.:10.1021/ES9035557
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. doi.:10.1021/CM100023P
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. doi.:10.1021/NN102272N
42. X. A. Li, J. J. Lenhart, Aggregation and dissolution of silver nanoparticles in natural surface water. Environ. Sci. Technol. 2012, 46, 5378. doi.:10.1021/ES204531Y
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. doi.:10.1002/ASIA.200900387
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. doi.:10.1021/ES104205A
45. M. Hadioui, S. Leclerc, K. J. Wilkinson, Multimethod quantification of Ag release from nanosilver. Talanta 2013, 105, 15. doi.:10.1016/ J.TALANTA.2012.11.048
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. doi.:10.1021/ES902240K
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. doi.:10.1021/ES200157H
48. X. A. Li, J. J. Lenhart, H. W. Walker, Dissolution-accompanied aggregation kinetics of silver nanoparticles. Langmuir 2010, 26, 16690. doi.:10.1021/LA101768N
49. X. A. Li, J. J. Lenhart, H. W. Walker, Aggregation kinetics and dissolution of coated silver nanoparticles. Langmuir 2012, 28, 1095. doi.:10.1021/LA202328N
50. C. Levard, E. M. Hotze, G. V. Lowry, G. E. Brown Jr, Environmental transformations of silver nanoparticles: Impact on stability and toxicity. Environ. Sci. Technol. 2012, 46, 6900. doi.:10.1021/ ES2037405
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. doi.:10.1007/S00775-007-0208-Z
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. doi.:10.1021/JP711616V
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. doi.:10.1021/ES301253S
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. doi.:10.1080/ 713609854
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. doi.:10.1063/ 1.1836764.