Mechanisms of Silver Nanoparticle Release, Transformation and Toxicity: A Critical Review of Current Knowledge and Recommendations for Future Studies and Applications
Abstract
:1. Introduction
2. Silver Nanoparticles in Use—Routes of Exposure
2.1. Textiles
2.2. Food Packaging
Product | Function of nanocomponent | Commercial status | Further information | Reference |
---|---|---|---|---|
BlueMoonGoods_ Fresh Box Silver Nanoparticle Food Storage Containers | Antimicrobial | Withdrawn from website | Nanoparticles permanently embedded in the container | [17] |
Nano Care Technology, Ltd. Antibacterial Kitchenware | Antimicrobial | URL no longer available | – | [18] |
Sunriver Industrial nanosilver fresh food bag | Antimicrobial | Commercially available | Ag has been shown to migrate from these bags | [19] |
FresherLonger_ Plastic Storage Bags | Antimicrobial | Commercially available but antimicrobial and Ag nanoparticles have been removed from the description | Resealable zip lock | [18] |
2.3. Implants and Other Medical Devices
2.4. Other Consumer Products
2.5. Silver Nanoparticles in Combination with Other Materials
3. Release of Silver from Functionalized Materials
Method | Silver content (mg/g) |
---|---|
Conventional textile: electrolytically deposited layer of silver (several μm) on fibre | 21.6 |
Plasma-coated fibre with silver nanoparticles (about 100 nm) embedded in polyester matrix | 0.39 |
AgCl (~200 nm) bound to the fibre surface | 0.008 |
AgCl (~200 nm) incorporated in binder on the fibre surface | 0.012 |
Silver nanoparticles bound to the fibre surface | 0.029 |
Silver nanoparticles incorporated into polyester fibre | 0.099 |
Silver nanoparticles incorporated into fibre | 0.242 |
Silver nanoparticles incorporated inside the synthetic fibres (according to manufacturer) | 0.003 |
Nanosized silver incorporated into cotton fibres (according to manufacturer) | 2.66 |
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PEC—Predicted Environmental Concentration, the concentration of the substance which will eventually be found in the environment;
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PNEC—Predicted No Effect Concentration, the concentration of the substance below which adverse effects in the environmental compartment of concern are not expected to occur;
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PEC/PNEC ratio—an indicator of risk.
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All above according to [50]
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PEC/PNEC < 1 = No immediate concern
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PEC/PNEC = 1–10 = Of concern if supply volumes increase
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PEC/PNEC = 10–100 = Further data required
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PEC/PNEC > 100 = Reduce risk immediately
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(According to Denehurst Chemical Safety Ltd. [51])
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Note: PEC/PNEC is sometimes called Risk Characterisation Ratio “RCR”
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Runoff—surface flow of water e.g., down the façade [52];
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Effluent—the waste liquid from domestic sewage, industrial sites or from agricultural processes. Effluents are harmful when they enter the environment, especially in freshwater, because of their polluting chemical composition;
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Pore waters—the water occupying the spaces between sediment particles (U.S. Environmental Protection Agency, 2001, cited from [53]);
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Anoxic—total deprivation of oxygen (U.S. Environmental Protection Agency, 2009, cited from [54]);
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EC50—median effective concentration: concentration at which 50% of the population are effected in whatever end-point is being assessed [50];
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IC50—concentration causing 50% inhibition of a given parameter, e.g., growth [50].
4. Behaviour of Silver Nanoparticles in Wastewater Treatment Plants
5. Characterization of Silver Nanomaterials and Its Importance—Lack of Sufficient and Relevant Characterization of Materials Used in Experiments
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Agglomerate: A collection of weakly bound particles or aggregates or mixtures of the two where the resulting external surface area is similar to the sum of the surface areas of the individual components.
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Note 1: The forces holding an agglomerate together are weak forces, for example “van der Waals” forces, or simple physical entanglement.
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Note 2: Agglomerates are also termed secondary particles and the original source particles are termed primary particles.
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Aggregate: A particle comprising of strongly bonded or fused particles where the resulting external surface area may be significantly smaller than the sum of calculated surface areas of the individual components.
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Note 1: The forces holding an aggregate together are strong forces, for example covalent bonds, or those resulting from sintering or complex physical entanglement.
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Note 2: Aggregates are also termed secondary particles and the original source particles are termed primary particles.
5.1. Size
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Light scattering based methods (Dynamic Light Scattering, Nanoparticle Tracking Analysis), in which size is calculated basing on the scattering of light by particles. DLS is widely used to assess the actual hydrodynamic size and nanoparticles behaviour (agglomeration, dissolution) in medium (e.g., [79]). DLS provides also data on nanoparticles size distribution and polydispersity index. DLS suits spherical, not too small particles, best. However it may be difficult or even impossible to analyse heterogeneous mixtures or polydisperse samples, or nanoparticles in the presence of other nanosized entities such as protein clusters. Nanoparticle Tracking Analysis (NTA) allows individual nanoparticles in a suspension to be microscopically visualized (though not, of course, imaged) and their Brownian motion to be separately but simultaneously analysed and from which the particle size distribution (and changes therein) can be obtained on a particle-by-particle basis. This enables separation of particle populations by size and intensity and allows complex and heterogeneous samples to be characterised easier [80].
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Microscopy-based techniques. The most common one is transmission electron microscopy (TEM) [45,59,79,81,82]. The obtained data includes particle and aggregate/agglomerate sizes, shape and potentially crystal structures [79]. Size distribution can be obtained using relevant software, although large numbers of particles must be counted to get statistically relevant data, which is even more difficult in the case of non-spherical or diverse shaped nanoparticles. However, TEM is one of few techniques which can deal with non-spherical particles analysis as there are no assumptions of sphericity inherent in the size calculations. However, due to sample preparation, nanoparticles cannot be observed in suspension, so if TEM is the only method used [83] the behaviour of the particles in suspension remains largely unknown. Still, in some cases TEM can be used to detect nanoparticle dissolution, agglomeration, and reprecipitation [10]. Another issue arising with TEM is a statistical issue- in order to properly assess the size and size distribution several thousand particles need to be analysed, which may be time consuming.
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Sedimentation/centrifugation methods, such as DCS which separates particles in a gradient based on centrifugal force. This method is excellent for complex biofluids such as protein clusters, which typically have quite different density than nanoparticles and thus separation of similarly sized objects of different density is possible. This method gives effective sizes of particles with a biomolecular corona [84]. It could also be used for a dissolution studies. Again, it is suitable mainly for spherical particles, although there is an ellipticity parameter, but limited evaluation of its validity has been undertaken to date.
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UV-Vis based methods (e.g., [27,45]) which utilise the shift in the adsorption maximum as an indicator of particle size. These are effective for metallic particles, such as gold and silver, but are less suitable for non-metallic ones. Also, it is clear that interactions with ions and biomolecules can affect the peak so care in data interpretation is needed. These methods could also be used for dissolution studies.
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Single (Nano) Particle Inductively Coupled Plasma Mass Spectrometry (SP-ICP-MS [43]) which measures the metal ion plumes produced by single particles vaporised in the plasma each second (compared to the measurement in millions of droplets in conventional ICP-MS). Thus, the signal is discontinuous in experimental time, and the mass of the particles determines the peak height and the particle concentration determines the number of peaks per minute. As only one element can be measured at a time, the size of, for example, nanoscale AgCl particles will be interpreted as being much smaller than metallic silver nanoparticles.
5.2. Surface Area
5.3. Coating and Surface Charge
6. Transformation of Silver Nanoparticles in the Environment
6.1. Transformation of Silver Nanoparticles in Living Systems
7. Mechanisms of Silver Nanoparticle Action in Bacteria and Potential for Bacterial Resistance
- (1)
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Adhesion of nanoparticles to the bacteria surface, altering the membrane properties. The small size and extremely large surface area of nanoparticles enables them to make strong contact with the microorganism surface [5]. As stated by Cao et al. [31] who studied the antibacterial properties of silver nanoparticles embedded in titanium (Ag-PIII-originated surface), the attachment of bacteria to such a surface correlates with the surface zeta potential of the nanoparticles. All studied Ag-PIII surfaces reduced the proliferation of both types of bacteria studied (Gram-positive Staphylococcus aureus and Gram-negative Escherichia coli).
- (2)
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Silver nanoparticles penetrating inside the bacterial cell, resulting in DNA damage. In the study of Choi and Hu [59] the inhibition of nitrifying organisms was correlated with the fraction of silver nanoparticles less than 5 nm, which was more toxic than any other form of silver (silver ions, AgCl colloids). The authors suggest that this may be due to easier (active) transport through the cell membrane of uncharged silver nanoparticles than of charged silver ions.
- (3)
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Dissolution of silver nanoparticles releases antimicrobial Ag+ ions which can interact with sulphur-containing proteins in the bacterial cell wall, which may lead to compromised functionality. This phenomenon is often considered as the main mechanism of the antimicrobial activity of nanosilver [6,111,112], so we can presume that the vast knowledge of antimicrobial properties of silver ions can be applied to the nanosilver case. At the same time, the problem of bacterial resistance to silver ions remains meaningful for at least some usages of silver nanoparticles. Interaction of dissolved Ag+ ions with cell wall and cytoplasmic proteins was also proposed by Cao et al. [22], who also highlight the fact that silver ions interaction with the thiol group of vital enzymes may result in their impaired function or inactivation. The exchange of silver ions between inorganic sulphur complexes and thiols was also proposed by [55,89] and others. Disruption of respiration and establishment of proton motive force as an effect of interactions with thiol groups of enzymes and other proteins is also stated by Hall Sedlak et al. [113]. According to Lee et al. [70], silver ions inhibit enzymes acting in the phosphorus, sulphur, and nitrogen cycles of nitrifying bacteria. Silver ions can enter from the environment or originate from sustained dissolution of silver nanoparticles taken up by bacteria.
- (4)
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As described in detail by Cao et al. [31], the proton electrochemical gradient in bacteria is established and maintained by respiratory processes (net transfer of protons from inside to outside of bacteria). ATP synthesis takes place when protons enter the cell (via ATPase), so the electrochemical gradient is an essential driving force for ATP synthesis in bacteria (similar processes occur in mitochondria). If those processes are interrupted, essential energy for all energy-dependent reactions cannot be provided, which leads to the (microbial) cell death. According to the authors, the proton-depleted regions formed around silver nanoparticles embedded in titanium (due to micro-galvanic effect, which causes proton consumption) may disrupt the electrochemical gradient in the bacteria’s intermembrane space and interfere with adhesion and proliferation [31]. The disruption of transmembrane electrochemical gradient, the importance of which is described above, leads eventually to cell death. As stated by the authors, the hypothesis mentioned above is supported by another study, where proteomic analysis results indicated that silver nanoparticles of average diameter 9.3 nm may accumulate in the protein precursors leading to depleted intracellular ATP levels [115].
8. Cytotoxicity, Genotoxicity, Oxidative Stress, Inflammation in Mammalian Cells
9. Cell Cycle Effects and Link to Reproductive/Developmental Toxicity/Neurotoxicity/Immune and other Less Well Understood Effects
10. Disentangling Impacts from Silver Ions versus Silver Nanoparticles
10.1. Particle Uptake and Localization Mechanisms
10.2. Silver Ions versus Silver Nanoparticles
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The lack of selectivity of citrate-coated silver nanoparticles toward DNA versus protein synthesis in undifferentiated cells, whereas silver ion is highly selective towards DNA.
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The inability of ascorbate (antioxidant) to protect cells from oxidative stress and cell loss caused by citrate-coated silver nanoparticles, whereas the same antioxidant is protective against silver ions [138], which implies that cell loss from citrate-coated silver nanoparticles reflects a different underlying mechanism and that, for the nanomaterial, oxidative stress is a result of cytotoxicity, not a cause of it.
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The greater inhibition of protein synthesis at lower concentrations of citrate-coated silver nanoparticles and a loss of effect at higher concentrations, totally distinct from the monotonic dose–effect relationship for silver ions [138] which indicates that low concentrations of citrate-coated silver nanoparticles disrupt protein synthesis through a mechanism unrelated to freely dissolved silver ions.
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The limited effectiveness of citrate-coated silver nanoparticles at suppressing the acetylcholine phenotype whereas silver ions affect both acetylcholine and dopamine phenotypes.
11. Conclusions
Abbreviations
Ag-PIII |
Single Step Silver Plasma Immersion Ion Implantation
|
ALF |
Artificial Lysosomal Fluid
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ATP |
Adenosine-5′-triphosphate
|
CEN |
Comité Européen de Normalisation (European Committee for Standardization)
|
CVC |
Central Venous Catheter
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DLS |
Dynamic Light Scattering
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DLVO |
Dejaguin–Landau–Verwey–Overbeek (theory)
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DMEM |
Dulbecco’s Modified Eagle Medium
|
EDTA |
Ethylenediaminetetraacetic acid
|
EDX |
Energy-dispersive X-ray spectroscopy
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EFSA |
European Food Safety Authority
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EPS |
Exopolysaccharides, extracellular polymeric substances
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GIT |
Gastrointestinal tract
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HSA |
Human Serum Albumin
|
ISO |
International Organization for Standardization
|
ISO/TS |
International Organization for Standardization/Technical Specification
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ICP-MS |
Inductively coupled plasma mass spectrometry
|
OECD |
Organisation for Economic Co-operation and Development
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PVP |
Polyvinylpyrrolidone
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ROS |
Reactive Oxygen Species
|
RPMI |
Roswell Park Memorial Institute medium
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SEM |
Scanning Electron Microscopy
|
TEM |
Transmission Electron Microscopy
|
USEPA |
The United States Environmental Protection Agency
|
WWTP |
Wastewater Treatment Plant
|
Acknowledgements
Appendices
Study | Material | Environment | Kind of transformation | Factors influencing transformations |
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Kittler et al. [69] |
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Liu et al. [93] |
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Liu et al. [94] |
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Akaighe et al. [99] |
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Chappell et al. [81] |
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Glover et al. [10] |
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Khan 45 [58] |
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Stebounova et al. [82] |
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Unrine et al. [97] |
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Study | Shape | Size (nm) | Coating | IC50 | Organism | Main outcomes |
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Lee et al. 2007 [65] | spherical | 11.6 ± 3.5 | citrate | ~0.3 nM | Danio rerio (zebra fish), embryos |
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Rahman et al. 2009 [132] | Mainly spherical | 25 | Not stated (negatively charged) | Not provided | C57BL/6N mice |
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Lankveld et al. 2010 [62] | Not stated | 20, 80, 110 | Not stated | Not provided | Wistar rats |
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Lee et al. 2012 [70] | spherical | 60–100 (powder type), 10 (citrate stabilized) | Citrate, not stated for powder type | EC50 (48h): powder-type: 0.75μg/L total Ag and 0.37μg/L dissolved Ag; Citrate stabilised AgNPs: 7.98μg/L total Ag and 0.88 μg/L dissolved Ag. | Daphnia magna |
|
Yang et al. 2012 [78] | spherical | 5, 8, 17, 22, 38, additional large and small | Citrate, PVP, gum arabic | 0.6–463 μM range depending on coating and medium (EC50—50% growth inhibition) | C. elegans |
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Study | Shape | Size (nm) | Coating | IC50 | Cell line | Main outcomes |
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Arora et al. 2009 [129] | spherical | 7–20 | Not stated | 61 μg/mL (fibroblasts) and 449 μg/mL (liver cells) | primary fibroblasts and primary liver cells from Swiss albino mice |
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Braydich-Stolle et al. 2010 [68] | spherical | 10, 15, 25–30, 80 nm | Hydrocarbon, polysaccharide | Not provided | mouse spermatogonial stem cells |
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Trickler et al. 2010 [77] | spherical | 28.3 ± 9.6, 47.5 ± 5.6, 102.2 ± 32.8 | PVP | Not assessed (above concentrations used) | primary rat brain microvessel endothelial cells (rBMEC) |
|
Bouwmeester et al. 2011 [66] | spherical | 20 ± 2, 34 ± 3, 61 ± 5, 113 ± 8 | Not stated | Not provided, but below concentrations studied (5 μg/mL) | Caco-2 and M-cells co-culture |
|
[31] | Ag NPs embedded in titanium | AgNPs – 5–8 | – | no toxic effect | osteoblast-like cell line MG63 | – |
Foldbjerg et al. 2011 [63] | – | 60–70 (depending on method) 149 ± 37 in medium | PVP | ~5 μg/mL | A549 |
|
Haase et al. 2011 [102] | spherical | 20; 40 | Small peptide | (μg/mL) 24 h–110; 140 48 h–18; 30 |
THP-1 cells |
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Hackenberg et al. 2011 [128] | Mainly spherical | 46 ± 21 | Not stated (The mean diameter of NP aggregates was 404 nm) | significant cytotoxicity at 10 μg/mL | human mesenchymal stem cells |
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Powers et al. 2010 [138] | Mainly spherical | Citrate – 6, PVP-21 and 75 | Citrate, PVP | Not provided | PC12 cell line |
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Haase et al. 2012 [67] | spherical | 20, 40 | Peptide | Not provided due to data complexity | Mixed primary cell model (mainly neurons and astrocytes) from Wistar rats |
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Kermanizadeh et al. 2012 [79] | Mainly euhedral; elongated or sub-spherical | <20 | polyoxylaurat Tween-20 | LC50 between 1.25 and 5 mg/cm2 (depending on method used) | Liver C3A cells |
|
Suresh et al. 2012 [91] | spherical | TEM <10, DLS in medium 77–164 | poly(diallyldimethylammonium) chloride-Ag, biogenic-Ag, uncoated Ag and oleate-Ag | (μg/mL) 0.1/0.45 0.125/0.7 4.9/6.3 1.1/1.6 |
mice macrophage RAW-264.7/mice lung epithelial C-10 |
|
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Reidy, B.; Haase, A.; Luch, A.; Dawson, K.A.; Lynch, I. Mechanisms of Silver Nanoparticle Release, Transformation and Toxicity: A Critical Review of Current Knowledge and Recommendations for Future Studies and Applications. Materials 2013, 6, 2295-2350. https://doi.org/10.3390/ma6062295
Reidy B, Haase A, Luch A, Dawson KA, Lynch I. Mechanisms of Silver Nanoparticle Release, Transformation and Toxicity: A Critical Review of Current Knowledge and Recommendations for Future Studies and Applications. Materials. 2013; 6(6):2295-2350. https://doi.org/10.3390/ma6062295
Chicago/Turabian StyleReidy, Bogumiła, Andrea Haase, Andreas Luch, Kenneth A. Dawson, and Iseult Lynch. 2013. "Mechanisms of Silver Nanoparticle Release, Transformation and Toxicity: A Critical Review of Current Knowledge and Recommendations for Future Studies and Applications" Materials 6, no. 6: 2295-2350. https://doi.org/10.3390/ma6062295