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A review of the antibacterial effects of silver nanomaterials and potential implications for human health and the environment

Abstract

Here, we present a review of the antibacterial effects of silver nanomaterials, including proposed antibacterial mechanisms and possible toxicity to higher organisms. For purpose of this review, silver nanomaterials include silver nanoparticles, stabilized silver salts, silver–dendrimer, polymer and metal oxide composites, and silver-impregnated zeolite and activated carbon materials. While there is some evidence that silver nanoparticles can directly damage bacteria cell membranes, silver nanomaterials appear to exert bacteriocidal activity predominantly through release of silver ions followed (individually or in combination) by increased membrane permeability, loss of the proton motive force, inducing de-energization of the cells and efflux of phosphate, leakage of cellular content, and disruption DNA replication. Eukaryotic cells could be similarly impacted by most of these mechanisms and, indeed, a small but growing body of literature supports this concern. Most antimicrobial studies are performed in simple aquatic media or cell culture media without proper characterization of silver nanomaterial stability (aggregation, dissolution, and re-precipitation). Silver nanoparticle stability is governed by particle size, shape, and capping agents as well as solution pH, ionic strength, specific ions and ligands, and organic macromolecules—all of which influence silver nanoparticle stability and bioavailability. Although none of the studies reviewed definitively proved any immediate impacts to human health or the environment by a silver nanomaterial containing product, the entirety of the science reviewed suggests some caution and further research are warranted given the already widespread and rapidly growing use of silver nanomaterials.

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References

  1. Abid J, Wark A, Brevet P, Girault H (2002) Preparation of silver nanoparticles in solution from a silver salt by laser irradiation. Chem Commun 792–793. doi: 10.1039/b200272h

  2. Ahamed M, Posgai R, Gorey TJ, Nielsen M, Hussain SM, Rowe JJ (2010) Silver nanoparticles induced heat shock protein 70, oxidative stress and apoptosis in Drosophila melanogaster. Toxicol Appl Pharmacol 242:263–269. doi:10.1016/j.taap.2009.10.016

  3. Ahmad A, Mukherjee P, Senapati S, Mandal D, Khan M, Kumar R, Sastry M (2003) Extracellular biosynthesis of silver nanoparticles using the fungus Fusarium oxysporum. Colloids Surf B 28:313–318. doi:10.1002/cbic.200700592

  4. Amro N, Kotra L, Wadu-Mesthrige K, Bulychev A, Mobashery S, Liu G (2000) High-resolution atomic force microscopy studies of the Escherichia coli outer membrane: structural basis for permeability. Langmuir 16:2789–2796. doi:10.1021/la991013x

  5. Arora S, Jain J, Rajwade J, Paknikar K (2008) Cellular responses induced by silver nanoparticles: in vitro studies. Toxicol Lett 179:93–100. doi:10.1016/j.toxlet.2008.04.009

  6. Arora S, Jain J, Rajwade JM, Paknikar KM (2009) Interactions of silver nanoparticles with primary mouse fibroblasts and liver cells. Toxicol Appl Pharmacol 236:310–318. doi:10.1016/j.taap.2009.02.020

  7. Asharani P, Wu Y, Gong Z, Valiyaveettil S (2008) Toxicity of silver nanoparticles in zebrafish models. Nanotechnology 19:1–8. doi:10.1088/0957-4484/19/25/255102

  8. Asharani PV, Mun GLK, Hande MP, Valiyaveettil S (2009) Cytotoxicity and genotoxicity of silver nanoparticles in human cells. ACS Nano 3:279–290. doi:10.1021/nn800596w

  9. Auerbach SM (2003) Zeolite science and technology. Marcel Dekker, New York

  10. Bajpai S, Mohan Y, Bajpai M, Tankhiwale R, Thomas V (2007) Synthesis of polymer stabilized silver and gold nanostructures. J Nanosci Nanotechnol 7:2994–3010. doi:10.1166/jnn.2007.911

  11. Balogh L, Swanson D, Tomalia D, Hagnauer G, McManus A (2001) Dendrimer–silver complexes and nanocomposites as antimicrobial agents. Nano Lett 1:18–21. doi:10.1021/nl005502p

  12. Batabyal S, Basu C, Das A, Sanyal G (2007) Green chemical synthesis of silver nanowires and microfibers using starch. J Biobased Mater Bioenergy 1:143–147. doi:10.1166/jbmb.2007.016

  13. Benn T, Westerhoff P (2008) Nanoparticle silver released into water from commercially available sock fabrics. Environ Sci Technol 42:4133–4139. doi:10.1021/es7032718

  14. Braydich-Stolle L, Hussain S, Schlager J, Hofmann M (2005) In vitro cytotoxicity of nanoparticles in mammalian germline stem cells. Toxicol Sci 88:412–419. doi:10.1093/toxsci/kfi256

  15. Brown C, Parchaso F, Thompson J, Luoma S (2003) Assessing toxicant effects in a complex estuary: a case study of effects of silver on reproduction in the bivalve, Potamocorbula amurensis, in San Francisco Bay. Hum Ecol Risk Assess 9:95–119. doi:10.1080/713609854

  16. Carlson C, Hussain SM, Schrand AM, Braydich-Stolle LK, Hess KL, Jones RL, Schlager JJ (2008) Unique cellular interaction of silver nanoparticles: size-dependent generation of reactive oxygen species. J Phys Chem B 112:13608–13619. doi:10.1021/jp712087m

  17. Chen C, Chiang C (2008) Preparation of cotton fibers with antibacterial silver nanoparticles. Mater Lett 62:3607–3609. doi:10.1016/j.matlet.2008.04.008

  18. Chen X, Schluesener H (2008) Nanosilver: a nanoproduct in medical application. Toxicol Lett 176:1–12. doi:10.1016/j.toxlet.2007.10.004

  19. Chi Z, Liu R, Zhao L, Qin P, Pan X, Sun F, Hao X (2009) A new strategy to probe the genotoxicity of silver nanoparticles combined with cetylpyridine bromide. Spectrochim Acta A 72:577–581. doi:10.1016/j.saa.2008.10.044

  20. Choi O, Hu Z (2008) Size dependent and reactive oxygen species related nanosilver toxicity to nitrifying bacteria. Environ Sci Technol 42:4583–4588. doi:10.1021/es703238h

  21. Choi O, Deng K, Kim N, Ross L, Surampalli R, Hu Z (2008) The inhibitory effects of silver nanoparticles, silver ions, and silver chloride colloids on microbial growth. Water Res 42:3066–3074. doi:10.1016/j.watres.2008.02.021

  22. Choi O, Cleuenger T, Deng B, Surampalli R, Ross L, Hu Z (2009) Role of sulfide and ligand strength in controlling nanosilver toxicity. Water Res 43:1879–1886. doi:10.1016/j.watres.2009.01.029

  23. Cowan M, Abshire K, Houk S, Evans S (2003) Antimicrobial efficacy of a silver-zeolite matrix coating on stainless steel. J Ind Microbiol Biotechnol 30:102–106. doi:10.1007/s10295-002-0022-0

  24. Damm C, Munstedt H (2008) Kinetic aspects of the silver ion release from antimicrobial polyamide/silver nanocomposites. Appl Phys A 91:479–486. doi:10.1007/s00339-008-4434-1

  25. Damm C, Munstedt H, Rosch A (2008) The antimicrobial efficacy of polyamide 6/silver-nano- and microcomposites. Mater Chem Phys 108:61–66. doi:10.1016/j.matchemphys.2007.09.002

  26. Dibrov P, Dzioba J, Gosink K, Hase C (2002) Chemiosmotic mechanism of antimicrobial activity of Ag+ in Vibrio cholerae. Antimicrob Agents Chemother 46:2668–2670. doi:10.1128/AAC.46.8.2668-2670.2002

  27. Dorjnamjin D, Ariunaa M, Shim Y (2008) Synthesis of silver nanoparticles using hydroxyl functionalized ionic liquids and their antimicrobial activity. Int J Mol Sci 9:807–819. doi:10.3390/ijms9050807

  28. Eby D, Schaeublin N, Farrington K, Hussain S, Johnson G (2009) Lysozyme catalyzes the formation of antimicrobial silver nanoparticles. ACS Nano 3:984–994. doi:10.1021/nn900079e

  29. Elechiguerra J, Burt J, Morones J, Camacho-Bragado A, Gao X, Lara H, Yacaman M (2005) Interaction of silver nanoparticles with HIV-1. J Nanobiotechnol 3:6. doi:10.1186/1477-3155-3-6

  30. Falletta E, Bonini M, Fratini E, Lo Nostro A, Pesavento G, Becheri A, Lo Nostro P, Canton P, Baglioni P (2008) Clusters of poly(acrylates) and silver nanoparticles: structure and applications for antimicrobial fabrics. J Phys Chem C 112:11758–11766. doi:10.1021/jp8035814

  31. Feng Q, Wu J, Chen G, Cui F, Kim T, Kim J (2000) A mechanistic study of the antibacterial effect of silver ions on Escherichia coli and Staphylococcus aureus. J Biomed Mater Res 52:662–668

  32. Furno F, Morley KS, Wong B, Sharp BL, Arnold PL, Howdle SM, Bayston R, Brown PD, Winship PD, Reid HJ (2004) Silver nanoparticles and polymeric medical devices: a new approach to prevention of infection? J Antimicrob Chemother 54:1019–1024. doi:10.1093/Jac/Dkh478

  33. Galiano K, Pleifer C, Engelhardt K, Brossner G, Lackner P, Huck C, Lass-Florl C, Obwegeser A (2008) Silver segregation and bacterial growth of intraventricular catheters impregnated with silver nanoparticles in cerebrospinal fluid drainages. Neurol Res 30:285–287. doi:10.1179/016164107x229902

  34. Gao J, Youn S, Hovsepyan A, Llaneza VL, Wang Y, Bitton G, Bonzongo JCJ (2009) Dispersion and toxicity of selected manufactured nanomaterials in Natural River water samples: effects of water chemical composition. Environ Sci Technol 43:3322–3328. doi:10.1021/es803315v

  35. Gong P, Li HM, He XX, Wang KM, Hu JB, Tan WH, Zhang SC, Yang XH (2007) Preparation and antibacterial activity of Fe3O4@Ag nanoparticles. Nanotechnology 18. doi: 10.1088/0957-4484/18/28/285604

  36. Gulrajani M, Gupta D, Periyasamy S, Muthu S (2008) Preparation and application of silver nanoparticles on silk for imparting antimicrobial properties. J Appl Polym Sci 108:614–623. doi:10.1002/app.27584

  37. Gupta A, Silver S (1998) Molecular genetics—silver as a biocide: Will resistance become a problem? Nat Biotechnol 16: 888. doi: 10.1038/nbt1098-888

  38. Gupta A, Maynes M, Silver S (1998) Effects of halides on plasmid-mediated silver resistance in Escherichia coli. Appl Environ Microbiol 64:5042–5045

  39. Gupta A, Matsui K, Lo JF, Silver S (1999) Molecular basis for resistance to silver cations in Salmonella. Nat Med 5:183–188. doi:10.1038/5545

  40. Gupta A, Phung LT, Taylor DE, Silver S (2001) Diversity of silver resistance genes in IncH incompatibility group plasmids. Microbiology 147:3393–3402

  41. Ha H, Xu W, An J, Li D, Zhao B (2006) A simple method to synthesize triangular silver nanoparticles by light irradiation. Spectrochim Acta A 64:956–960. doi:10.1016/j.saa.2005.09.004

  42. Hernandez-Sierra J, Ruiz F, Pena D, Martinez-Gutierrez F, Martinez A, Guillen A, Tapia-Perez H, Castanon G (2008) The antimicrobial sensitivity of Streptococcus mutants to nanoparticles of silver, zinc oxide, and gold. Nanomed Nanotechnol 4:237–240. doi:10.1016/j.nano.2008.04.005

  43. Hlidek P, Biederman H, Choukourov A, Slavinska D (2008) Behavior of polymeric matrices containing silver inclusions. 1—Review of adsorption and oxidation of hydrocarbons on silver surfaces/interfaces as witnessed by FT-IR spectroscopy. Plasma Process Polym 5:807–824. doi:10.1002/ppap.200800083

  44. Holt K, Bard A (2005) Interaction of silver(I) ions with the respiratory chain of Escherichia coli: an electrochemical and scanning electrochemical microscopy study of the antimicrobial mechanism of micromolar Ag. Biochemistry 44:13214–13223. doi:10.1021/bi0508542

  45. Hsin Y, Chena C, Huang S, Shih T, Lai P, Chueh P (2008) The apoptotic effect of nanosilver is mediated by a ROS- and JNK-dependent mechanism involving the mitochondrial pathway in NIH3T3 cells. Toxicol Lett 179:130–139. doi:10.1016/j.toxlet.2008.04.015

  46. Huang H, Yang X (2004) Synthesis of polysaccharide-stabilized gold and silver nanoparticles: a green method. Carbohydr Res 339:2627–2631. doi:10.1016/j.carres.2004.08.005

  47. Hussain S, Hess K, Gearhart J, Geiss K, Schlager J (2005) In vitro toxicity of nanoparticles in BRL 3A rat liver cells. Toxicol In Vitro 19:975–983. doi:10.1016/j.tiv.2005.06.034

  48. Hwang E, Lee J, Chae Y, Kim Y, Kim B, Sang B, Gu M (2008) Analysis of the toxic mode of action of silver nanoparticles using stress-specific bioluminescent bacteria. Small 4:746–750. doi:10.1002/smll.200700954

  49. Ingle A, Gade A, Pierrat S, Sonnichsen C, Rai M (2008) Mycosynthesis of silver nanoparticles using the fungus Fusarium acuminatum and its activity against some human pathogenic bacteria. Curr Nanosci 4:141–144. doi:10.2174/157341308784340804

  50. Inoue Y, Hoshino M, Takahashi H, Noguchi T, Murata T, Kanzaki Y, Hamashima H, Sasatsu M (2002) Bactericidal activity of Ag-zeolite mediated by reactive oxygen species under aerated conditions. J Inorg Biochem 92:37–42. doi:10.1016/S0162-0134(02)00489-0

  51. Jain P, Pradeep T (2005) Potential of silver nanoparticle-coated polyurethane foam as an antibacterial water filter. Biotechnol Bioeng 90:59–63. doi:10.1002/bit.20368

  52. Jin W, Jeon H, Kim J, Youk J (2007) A study on the preparation of poly(vinyl alcohol) nanofibers containing silver nanoparticles. Synthetic Met 157:454–459. doi:10.1016/j.synthmet.2007.05.011

  53. Jung W, Koo H, Kim K, Shin S, Kim S, Park Y (2008) Antibacterial activity and mechanism of action of the silver ion in Staphylococcus aureus and Escherichia coli. Appl Environ Microbiol 74:2171–2178. doi:10.1128/AEM.02001-07

  54. Jung R, Kim Y, Kim H, Jin H (2009) Antimicrobial properties of hydrated cellulose membranes with silver nanoparticles. J Biomater Sci Polym Ed 20:311–324. doi:10.1163/156856209X412182

  55. Kalishwaralal K, Deepak V, Ramkumarpandian S, Nellaiah H, Sangiliyandi G (2008) Extracellular biosynthesis of silver nanoparticles by the culture supernatant of Bacillus licheniformis. Mater Lett 62:4411–4413. doi:10.1016/j.matlet.2008.06.051

  56. Kasthuri J, Veerapandian S, Rajendiran N (2009) Biological synthesis of silver and gold nanoparticles using apiin as reducing agent. Colloids Surf B 68:55–60. doi:10.1016/j.colsurfb.2008.09.021

  57. Kim J (2007) Antibacterial activity of Ag+ ion-containing silver nanoparticles prepared using the alcohol reduction method. J Ind Eng Chem 13:718–722

  58. Kim J, Kuk E, Yu K, Kim J, Park S, Lee H, Kim S, Park Y, Park Y, Hwang C, Kim Y, Lee Y, Jeong D, Cho M (2007) Antimicrobial effects of silver nanoparticles. Nanomed Nanotechnol 3:95–101. doi:10.1016/j.nano.2006.12.001

  59. Kim K, Sung W, Moon S, Choi J, Kim J, Lee D (2008a) Antifungal effect of silver nanoparticles on dermatophytes. J Microbiol Biotechnol 18:1482–1484

  60. Kim Y, Kim J, Cho H, Rha D, Kim J, Park J, Choi B, Lim R, Chang H, Chung Y, Kwon I, Jeong J, Han B, Yu I (2008b) Twenty-eight-day oral toxicity, genotoxicity, and gender-related tissue distribution of silver nanoparticles in Sprague-Dawley rats. Inhal Toxicol 20:575–583. doi:10.1080/08958370701874663

  61. Kim J, Lee J, Kwon S, Jeong S (2009a) Preparation of biodegradable polymer/silver nanoparticles composite and its antibacterial efficacy. J Nanosci Nanotechnol 9:1098–1102. doi:10.1166/jnn.2009.C096

  62. Kim K, Sung W, Suh B, Moon S, Choi J, Kim J, Lee D (2009b) Antifungal activity and mode of action of silver nano-particles on Candida albicans. Biometals 22:235–242. doi:10.1007/s10534-008-9159-2

  63. Kutschera U (2009) Symbiogenesis, natural selection, and the dynamic Earth. Theory Biosci 128:191–203. doi:10.1007/s12064-009-0065-0

  64. Kvitek L, Panacek A, Soukupova J, Kolar M, Vecerova R, Prucek R, Holecova M, Zboril R (2008) Effect of surfactants and polymers on stability and antibacterial activity of silver nanoparticles (NPs). J Phys Chem C 112:5825–5834. doi:10.1021/jp711616v

  65. Le Pape H, Solano-Serena F, Contini P, Devillers C, Maftah A, Leprat P (2002) Evaluation of the anti-microbial properties of an activated carbon fibre supporting silver using a dynamic method. Carbon 40:2954. doi:10.1016/S0008-6223(02)00246-4

  66. Le Pape H, Solano-Serena F, Contini P, Devillers C, Maftah A, Leprat P (2004) Involvement of reactive oxygen species in the bactericidal activity of activated carbon fibre supporting silver bactericidal activity of ACF(Ag) mediated by ROS. J Inorg Biochem 98:1054–1060. doi:10.1016/j.jinorgbio.2004.02.025

  67. Lesniak W, Bielinska A, Sun K, Janczak K, Shi X, Baker J, Balogh L (2005) Silver/dendrimer nanocomposites as biomarkers: fabrication, characterization, in vitro toxicity, and intracellular detection. Nano Lett 5:2123–2130. doi:10.1021/nl051077u

  68. Li Y, Kim Y, Lee E, Cai W, Cho S (2006) Synthesis of silver nanoparticles by electron irradiation of silver acetate. Nucl Instrum Methods B 251:425–428. doi:10.1016/j.nimb.2006.06.019

  69. Li S, Shen Y, Xie A, Yu X, Qiu L, Zhang L, Zhang Q (2007) Green synthesis of silver nanoparticles using Capsicum annuum L. extract. Green Chem 9:852–858. doi:10.1039/b615357g

  70. Liau S, Read D, Pugh W, Furr J, Russell A (1997) Interaction of silver nitrate with readily identifiable groups: relationship to the antibacterial action of silver ions. Lett Appl Microbiol 25:279–283. doi:10.1046/j.1472-765X.1997.00219.x

  71. Lind ML, Jeong BH, Subramani A, Huang XF, Hoek EMV (2009) Effect of mobile cation on zeolite-polyamide thin film nanocomposite membranes. J Mater Res 24:1624–1631. doi:10.1557/Jmr.2009.0189

  72. Lok C, Ho C, Chen R, He Q, Yu W, Sun H, Tam P, Chiu J, Che C (2006) Proteomic analysis of the mode of antibacterial action of silver nanoparticles. J Proteome Res 5:916–924. doi:10.1021/pr0504079

  73. Lok C, Ho C, Chen R, He Q, Yu W, Sun H, Tam P, Chiu J, Che C (2007) Silver nanoparticles: partial oxidation and antibacterial activities. J Biol Inorg Chem 12:527–534. doi:10.1007/s00775-007-0208-z

  74. Long D, Wu G, Chen S (2007) Preparation of oligochitosan stabilized silver nanoparticles by gamma irradiation. Radiat Phys chem 76:1126–1131. doi:10.1016/j.radphyschem.2006.11.001

  75. Lu L, Sun R, Chen R, Hui C, Ho C, Luk J, Lau G, Che C (2008) Silver nanoparticles inhibit hepatitis B virus replication. Antivir Ther 13:253–262

  76. Mahapatra S, Bogle K, Dhole S, Bhoraskar V (2007) Synthesis of gold and silver nanoparticles by electron irradiation at 5–15 keV energy. Nanotechnology 18. doi: 10.1088/0957-4484/18/13/135602

  77. Maneerung T, Tokura S, Rujiravanit R (2008) Impregnation of silver nanoparticles into bacterial cellulose for antimicrobial wound dressing. Carbohydr Polym 72:43–51. doi:10.1016/j.carbpol.2007.07.025

  78. Manno D, Filippo E, Di Giulio M, Serra A (2008) Synthesis and characterization of starch-stabilized Ag nanostructures for sensors applications. J Non-Cryst Solids 354:5515–5520. doi:10.1016/j.jnoncrysol.2008.04.059

  79. Manzi AE, van Halbeek H (1999) Saccharide structure and nomenclature. In: Varki A, Cummings R, Esko J, Freeze H, Hart G, Marth J (eds) Essentials of glycobiology, 1st edn. Cold Spring Harbor Laboratory Press, New York

  80. Martinez-Castanon GA, Nino-Martinez N, Martinez-Gutierrez F, Martinez-Mendoza JR, Ruiz F (2008) Synthesis and antibacterial activity of silver nanoparticles with different sizes. J Nanopart Res 10:1343–1348. doi:10.1007/s11051-008-9428-6

  81. Martinez-Castanon G, Nino-Martinez N, Loyola-Rodriguez J, Patino-Marin N, Martinez-Mendoza J, Ruiz F (2009) Synthesis of silver particles with different sizes and morphologies. Mater Lett 63:1266–1268. doi:10.1016/j.matlet.2009.02.061

  82. Mayo JT, Yavuz C, Yean S, Cong L, Shipley H, Yu W, Falkner J, Kan A, Tomson M, Colvin VL (2007) The effect of nanocrystalline magnetite size on arsenic removal. Sci Technol Adv Mater 8:71–75. doi:10.1016/j.stam.2006.10.005

  83. McDonnell AMP, Beving D, Wang AJ, Chen W, Yan YS (2005) Hydrophilic and antimicrobial zeolite coatings for gravity-independent water separation. Adv Funct Mater 15:336–340. doi:10.1002/adfm.200400183

  84. Mendis E, Rajapakse N, Byun H, Kim S (2005) Investigation of jumbo squid (Dosidicus gigas) skin gelatin peptides for their in vitro antioxidant effects. Life Sci 77:2166–2178. doi:10.1016/j.lfs.2005.03.016

  85. Mokhtari N, Daneshpajouh S, Seyedbagheri S, Atashdehghan R, Abdi K, Sarkar S, Minaian S, Shahverdi H, Shahverdi A (2009) Biological synthesis of very small silver nanoparticles by culture supernatant of Klebsiella pneumonia: the effects of visible-light irradiation and the liquid mixing process. Mater Res Bull 44:1415–1421. doi:10.1016/j.materresbull.2008.11.021

  86. Morones J, Elechiguerra J, Camacho A, Holt K, Kouri J, Ramirez J, Yacaman M (2005) The bactericidal effect of silver nanoparticles. Nanotechnology 16:2346–2353. doi:10.1088/0957-4484/16/10/059

  87. Mukherjee P, Ahmad A, Mandal D, Senapati S, Sainkar S, Khan M, Parishcha R, Ajaykumar P, Alam M, Kumar R, Sastry M (2001) Fungus-mediated synthesis of silver nanoparticles and their immobilization in the mycelial matrix: a novel biological approach to nanoparticle synthesis. Nano Lett 1:515–519. doi:10.1021/nl0155274

  88. Naidu B, Park J, Kim S, Park S, Lee E, Yoon K, Lee S, Lee J, Gal Y, Jin S (2008) Novel hybrid polymer photovoltaics made by generating silver nanoparticles in polymer: fullerene bulk-heterojunction structures. Sol Energy Mater Sol Cells 92:397–401. doi:10.1016/j.solmat.2007.09.017

  89. Navarro E, Piccapietra F, Wagner B, Marconi F, Kaegi R, Odzak N, Sigg L, Behra R (2008) Toxicity of Silver Nanoparticles to Chlamydomonas reinhardtii. Environ Sci Technol 42:8959–8964. doi:10.1021/es801785m

  90. Neal AL (2008) What can be inferred from bacterium-nanoparticle interactions about the potential consequences of environmental exposure to nanoparticles? Ecotoxicology 17:362–371. doi:10.1007/s10646-008-0217-x

  91. Nel A, Xia T, Madler L, Li N (2006) Toxic potential of materials at the nanolevel. Science 311:622–627. doi:10.1126/science.1114397

  92. Nel AE, Madler L, Velegol D, Xia T, Hoek EMV, Somasundaran P, Klaessig F, Castranova V, Thompson M (2009) Understanding biophysicochemical interactions at the nano–bio interface. Nat Mater 8:543–557. doi:10.1038/nmat2442

  93. Nita T (2008) Synthesis of antimicrobial polymer composition and in vitro drugs release study. e-Polymers

  94. Ogden J, Bogdanchikova N, Corker J, Petranovskii V (1999) Structure of silver clusters embedded in erionite channels. Eur Phys J D 9:605–608. doi:10.1007/s100530050509

  95. Pal S, Tak Y, Song J (2007) Does the antibacterial activity of silver nanoparticles depend on the shape of the nanoparticle? A study of the gram-negative bacterium Escherichia coli. Appl Environ Microbiol 73:1712–1720. doi:10.1128/AEM.02218-06

  96. Pal S, Tak YK, Joardar J, Kim W, Lee JE, Han MS, Song JM (2009) Nanocrystalline silver supported on activated carbon matrix from hydrosol: antibacterial mechanism under prolonged incubation conditions. J Nanosci Nanotechnol 9:2092–2103. doi:10.1166/jnn.2009.427

  97. Panacek A, Kvitek L, Prucek R, Kolar M, Vecerova R, Pizurova N, Sharma V, Nevecna T, Zboril R (2006) Silver colloid nanoparticles: synthesis, characterization, and their antibacterial activity. J Phys Chem B 110:16248–16253. doi:10.1021/jp063826h

  98. Panyala NR, Peña-Méndez EM, Havel J (2008) Silver or silver nanoparticles: a hazardous threat to the environment and human health? J Appl Biomed 6:117–129

  99. Park H, Kim J, Kim J, Lee J, Hahn J, Gu M, Yoon J (2009) Silver-ion-mediated reactive oxygen species generation affecting bactericidal activity. Water Res 43:1027–1032. doi:10.1016/j.watres.2008.12.002

  100. Petering H (1976) Pharmacology and toxicology of heavy-metals-silver. Pharmacol Ther A 1:127–130. doi:10.1016/0362-5478(76)90002-4

  101. Pillai Z, Kamat P (2004) What factors control the size and shape of silver nanoparticles in the citrate ion reduction method? J Phys Chem B 108:945–951. doi:10.1021/jp037018r

  102. Raffi M, Hussain F, Bhatti T, Akhter J, Hameed A, Hasan M (2008) Antibacterial characterization of silver nanoparticles against E. coli ATCC-15224. J Mater Sci Technol 24:192–196

  103. Rejeski D (2009) Nanotechnology and consumer products. http://www.nanotechproject.org/publications/archive/nanotechnology_consumer_products/. Accessed 22 February 2010

  104. Roe D, Karandikar B, Bonn-Savage N, Gibbins B, Roullet J (2008) Antimicrobial surface functionalization of plastic catheters by silver nanoparticles. J Antimicrob Chemother 61:869–876. doi:10.1093/jac/dkn034

  105. Ruparelia J, Chatteriee A, Duttagupta S, Mukherji S (2008) Strain specificity in antimicrobial activity of silver and copper nanoparticles. Acta Biomater 4:707–716. doi:10.1016/j.actbio.2007.11.006

  106. Saito Y, Wang J, Batchelder D, Smith D (2003) Simple chemical method for forming silver surfaces with controlled grain sizes for surface plasmon experiments. Langmuir 19:6857–6861. doi:10.1021/la0301240

  107. Sambhy V, Sen A (2008) Novel process of incorporating silver biocides into polymers. Chim Oggi 26:16–18

  108. Sanghi R, Verma P (2009) Biomimetic synthesis and characterisation of protein capped silver nanoparticles. Bioresour Technol 100:501–504. doi:10.1016/j.biortech.2008.05.048

  109. Sanpui P, Murugadoss A, Prasad P, Ghosh S, Chattopadhyay A (2008) The antibacterial properties of a novel chitosan-Ag-nanoparticle composite. Int J Food Microbiol 124:142–146. doi:10.1016/j.ijfoodmicro.2008.03.004

  110. Schneider S, Halbig P, Grau H, Nickel U (1994) Reproducible preparation of silver sols with uniform particle-size for application in surface-enhanced raman-spectroscopy. Photochem Photobiol 60:605–610. doi:10.1111/j.1751-1097.1994.tb05156.x

  111. Schrand A, Braydich-Stolle L, Schlager J, Dai L, Hussain S (2008) Can silver nanoparticles be useful as potential biological labels? Nanotechnology 19. doi: 10.1088/0957-4484/19/23/235104

  112. Schreurs W, Rosenberg H (1982) Effect of silver ions on transport and retention of phosphate by Escherichia coli. J Bacteriol 152:7–13

  113. Senapati S, Mandal D, Ahmad A, Khan M, Sastry M, Kumar R (2004) Fungus mediated synthesis of silver nanoparticles: a novel biological approach. Indian J Phys A 78A:101–105

  114. Shankar SS, Ahmad A, Sastry M (2003) Geranium leaf assisted biosynthesis of silver nanoparticles. Biotechnol Progr 19:1627–1631. doi:10.1021/Bp034070w

  115. Sharma S, Thakur M, Deb M (2007) Synthesis of silver nanoparticles using N-1, N-2-diphenylbenzamidine by microwave irradiation method. J Exp Nanosci 2:251–256. doi:10.1080/17458080701753744

  116. Sharma S, Thakur M, Deb MK (2008) Preparation of silver nanoparticles by microwave irradiation. Curr Nanosci 4:138–140

  117. Sharma VK, Yngard RA, Lin Y (2009) Silver nanoparticles: green synthesis and their antimicrobial activities. Adv Colloid Interface Sci 145:83–96. doi:10.1016/j.cis.2008.09.002

  118. Shirtcliffe N, Nickel U, Schneider S (1999) Reproducible preparation of silver sols with small particle size using borohydride reduction: for use as nuclei for preparation of larger particles. J Colloid Interface Sci 211:122–129. doi:10.1006/jcis.1998.5980

  119. Shrivastava S, Bera T, Roy A, Singh G, Ramachandrarao P, Dash D (2007) Characterization of enhanced antibacterial effects of novel silver nanoparticles. Nanotechnology 18. doi: 10.1088/0957-4484/18/22/225103

  120. Silver S (2003) Bacterial silver resistance: molecular biology and uses and misuses of silver compounds. FEMS Microbiol Rev 27:341–353. doi:10.1016/S0168-6445(03)00047-0

  121. Silver S, Phung LT, Silver G (2006) Silver as biocides in burn and wound dressings and bacterial resistance to silver compounds. J Ind Microbiol Biotechnol 33:627–634. doi:10.1007/s10295-006-0139-7

  122. Singh M, Sinha I, Mandal R (2009) Role of pH in the green synthesis of silver nanoparticles. Mater Lett 63:425–427. doi:10.1016/j.matlet.2008.10.067

  123. Slonczewski J, Foster J (2009) Microbiology: an evolving science. W. W. Norton & Co, New York

  124. Smetana A, Klabunde K, Sorensen C (2005) Synthesis of spherical silver nanoparticles by digestive ripening, stabilization with various agents, and their 3-D and 2-D superlattice formation. J Colloid Interface Sci 284:521–526. doi:10.1016/j.jcis.2004.10.038

  125. Smetana A, Klabunde K, Marchin G, Sorensen C (2008) Biocidal activity of nanocrystalline silver powders and particles. Langmuir 24:7457–7464. doi:10.1021/la800091y

  126. 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. doi:10.1016/j.jcis.2004.02.012

  127. Song J, Kim B (2009) Rapid biological synthesis of silver nanoparticles using plant leaf extracts. Bioproc Biosyst Eng 32:79–84. doi:10.1007/s00449-008-0224-6

  128. Stoeva S, Klabunde K, Sorensen C, Dragieva I (2002) Gram-scale synthesis of monodisperse gold colloids by the solvated metal atom dispersion method and digestive ripening and their organization into two- and three-dimensional structures. J Am Chem Soc 124:2305–2311. doi:10.1021/ja012076g

  129. Stohs SJ, Bagchi D (1995) Oxidative mechanisms in the toxicity of metal-ions. Free Radic Biol Med 18:321–336. doi:10.1016/0891-5849(94)00159-H

  130. Sun L, Singh A, Vig K, Pillai S, Singh S (2008) Silver nanoparticles inhibit replication of respiratory syncytial virus. J Biomed Nanotechnol 4:149–158. doi:10.1166/jbn.2008.012

  131. Sung J, Ji J, Yoon J, Kim D, Song M, Jeong J, Han B, Han J, Chung Y, Kim J, Kim T, Chang H, Lee E, Lee J, Yu I (2008) Lung function changes in Sprague-Dawley rats after prolonged inhalation exposure to silver nanoparticles. Inhal Toxicol 20:567–574. doi:10.1080/08958370701874671

  132. Teeguarden J, Hinderliter P, Orr G, Thrall B, Pounds J (2007) Particokinetics in vitro: dosimetry considerations for in vitro nanoparticle toxicity assessments. Toxicol Sci 95:300–312. doi:10.1093/toxsci/kfl165

  133. Tomsic B, Simoncic B, Orel B, Zerjav M, Schroers H, Simoncic A, Samardzija Z (2009) Antimicrobial activity of AgCl embedded in a silica matrix on cotton fabric. Carbohydr Polym 75:618–626. doi:10.1016/j.carbpol.2008.09.013

  134. Venediktov E, Padokhin V (2008) Synthesis of silver nanoclusters in starch aqueous solutions. Russ J Appl Chem 81:2040–2042. doi:10.1134/S1070427208110323

  135. Vertelov G, Krutyakov Y, Efremenkova O, Olenin A, Lisichkin G (2008) A versatile synthesis of highly bactericidal Myramistin® stabilized silver nanoparticles. Nanotechnology 19. doi: 10.1088/0957-4484/19/35/355707

  136. Vigneshwaran N, Ashtaputre N, Varadarajan P, Nachane R, Paralikar K, Balasubramanya R (2007) Biological synthesis of silver nanoparticles using the fungus Aspergillus flavus. Mater Lett 61:1413–1418. doi:10.1016/j.matlet.2006.07.042

  137. West JL, Halas NJ (2003) Engineered nanomaterials for biophotonics applications: improving sensing, imaging, and therapeutics. Annu Rev Biomed Eng 5:285–292. doi:10.1146/annurev.bioeng.5.011303.120723

  138. Xu X, Brownlow W, Kyriacou S, Wan Q, Viola J (2004) Real-time probing of membrane transport in living microbial cells using single nanoparticle optics and living cell imaging. Biochemistry 43:10400–10413. doi:10.1021/bi036231a

  139. Xu X, Yang Q, Wang Y, Yu H, Chen X, Jing X (2006) Biodegradable electrospun poly(l-lactide) fibers containing antibacterial silver nanoparticles. Eur Phys J D 42:2081–2087. doi:10.1016/j.eurpolymj.2006.03.032

  140. Yanagihara N, Tanaka Y, Okamoto H (2001) Formation of silver nanoparticles in poly(methyl methacrylate) by UV irradiation. Chem Lett 30:796–797

  141. Yang W, Shen C, Ji Q, An H, Wang J, Liu Q, Zhang Z (2009) Food storage material silver nanoparticles interfere with DNA replication fidelity and bind with DNA. Nanotechnology 20. doi: 10.1088/0957-4484/20/8/085102

  142. Yavuz CT, Mayo JT, Yu WW, Prakash A, Falkner JC, Yean S, Cong L, Shipley HJ, Kan A, Tomson M, Natelson D, Colvin VL (2006) Low-field magnetic separation of monodisperse Fe3O4. Nanocrystals 314:964–967. doi:10.1126/science.1131475

  143. Yeo M, Kang M (2008) Effects of nanometer sized silver materials on biological toxicity during zebrafish embryogenesis. Bull Korean Chem Soc 29:1179–1184

  144. Yeo M, Yoon J (2009) Comparison of the effects of nano-silver antibacterial coatings and silver ions on zebrafish embryogenesis. Mol Cell Toxicol 5:23–31

  145. Yin H, Yamamoto T, Wada Y, Yanagida S (2004) Large-scale and size-controlled synthesis of silver nanoparticles under microwave irradiation. Mater Chem Phys 83:66–70. doi:10.1016/j.matchemphys.2003.09.006

  146. Yoon K, Byeon J, Park C, Hwang J (2008a) Antimicrobial effect of silver particles on bacterial contamination of activated carbon fibers. Environ Sci Technol 42:1251–1255. doi:10.1021/es0720199

  147. Yoon K, Byeon J, Park J, Ji J, Bae G, Hwang J (2008b) Antimicrobial characteristics of silver aerosol nanoparticles against Bacillus subtilis bioaerosols. Environ Eng Sci 25:289–293. doi:10.1089/ees.2007.0003

  148. Yu D (2007) Formation of colloidal silver nanoparticles stabilized by Na+-poly(gamma-glutamic acid)-silver nitrate complex via chemical reduction process. Colloids Surf B 59:171–178. doi:10.1016/j.colsurfb.2007.05.007

  149. Yu D, Yam V (2004) Controlled synthesis of monodisperse silver nanocubes in water. J Am Chem Soc 126:13200–13201. doi:10.1021/ja046037r

  150. Zeng H, Zhao C, Qiu J, Yang Y, Chen G (2007) Preparation and optical properties of silver nanoparticles induced by a femtosecond laser irradiation. J Cryst Growth 300:519–522. doi:10.1016/j.jcrysgro.2006.11.308

  151. Zhang Y, Peng H, Huang W, Zhou Y, Yan D (2008) Facile preparation and characterization of highly antimicrobial colloid Ag or Au nanoparticles. J Colloid Interface Sci 325:371–376. doi:10.1016/j.jcis.2008.05.063

  152. Zodrow K, Brunet L, Mahendra S, Li D, Zhang A, Li QL, Alvarez PJJ (2009) Polysulfone ultrafiltration membranes impregnated with silver nanoparticles show improved biofouling resistance and virus removal. Water Res 43:715–723. doi:10.1016/j.watres.2008.11.014

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Acknowledgments

Financial support for this research was provided by the University of California Toxic Substances Research and Training Program: Lead Campus Program in Nanotoxicology.

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Correspondence to Eric M. V. Hoek.

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Marambio-Jones, C., Hoek, E.M.V. A review of the antibacterial effects of silver nanomaterials and potential implications for human health and the environment. J Nanopart Res 12, 1531–1551 (2010). https://doi.org/10.1007/s11051-010-9900-y

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Keywords

  • Silver
  • Nanoparticle
  • Antimicrobial
  • Antibacterial
  • Nanotechnology
  • Nanotoxicology
  • Safety
  • EHS