Critical Reviews in Microbiology

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Silver nanoparticles: Synthesis methods, bioapplications and properties Elham Abbasi, Morteza Milani, Sedigheh Fekri Aval, Mohammad Kouhi, Abolfazl Akbarzadeh, Hamid Tayefi Nasrabadi, Parisa Nikasa, San Woo Joo, Younes Hanifehpour, Kazem Nejati-Koshki & Mohammad Samiei To cite this article: Elham Abbasi, Morteza Milani, Sedigheh Fekri Aval, Mohammad Kouhi, Abolfazl Akbarzadeh, Hamid Tayefi Nasrabadi, Parisa Nikasa, San Woo Joo, Younes Hanifehpour, Kazem Nejati-Koshki & Mohammad Samiei (2016) Silver nanoparticles: Synthesis methods, bio-applications and properties, Critical Reviews in Microbiology, 42:2, 173-180, DOI: 10.3109/1040841X.2014.912200 To link to this article: http://dx.doi.org/10.3109/1040841X.2014.912200

Published online: 17 Jun 2014.

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Date: 13 December 2016, At: 03:14

http://informahealthcare.com/mby ISSN: 1040-841X (print), 1549-7828 (electronic) Crit Rev Microbiol, 2016; 42(2): 173–180 ! 2014 Informa Healthcare USA, Inc. DOI: 10.3109/1040841X.2014.912200

REVIEW ARTICLE

Silver nanoparticles: Synthesis methods, bio-applications and properties Elham Abbasi1, Morteza Milani1,3, Sedigheh Fekri Aval5, Mohammad Kouhi2, Abolfazl Akbarzadeh1, Hamid Tayefi Nasrabadi1, Parisa Nikasa3, San Woo Joo4, Younes Hanifehpour4, Kazem Nejati-Koshki1,5, and Mohammad Samiei6 1

Department of Medical Nanotechnology, Faculty of Advanced Medical Sciences, Tabriz University of Medical Sciences, Tabriz, Iran, 2Department of Physics, College of Science, Tabriz Branch, Islamic Azad University, Tabriz, Iran, 3Department of Molecular Medicine, Faculty of Advanced Medical Sciences, Tabriz University of Medical Sciences, Tabriz, Iran, 4School of Mechanical Engineering, Yeungnam University, Gyeongsan 712-749, South Korea, 5Department of Medical Nanotechnology, Faculty of Advanced Medical Sciences, Tabriz University of Medical Sciences, Tabriz, Iran, and 6 Department of Endodontics, Dental School, Tabriz University of Medical Sciences, Tabriz, Iran Abstract

Keywords

Silver nanoparticles size makes wide range of new applications in various fields of industry. Synthesis of noble metal nanoparticles for applications such as catalysis, electronics, optics, environmental and biotechnology is an area of constant interest. Two main methods for Silver nanoparticles are the physical and chemical methods. The problem with these methods is absorption of toxic substances onto them. Green synthesis approaches overcome this limitation. Silver nanoparticles size makes wide range of new applications in various fields of industry. This article summarizes exclusively scalable techniques and focuses on strengths, respectively, limitations with respect to the biomedical applicability and regulatory requirements concerning silver nanoparticles.

Antimicrobial, bactericidal effects, biological labeling, noble metal nanoparticles, photography

Introduction Nanoscience has been established recently as a new interdisciplinary science. It is considered as a whole knowledge on fundamental properties of nano-size objects (Sergeev, 2003; Sergeev, 2008). The prefix ‘‘nano’’ indicates one billionth or 109 units. The nature of this unit being determined by the word that follows. It is widely accepted in the context of nanoscience and nanotechnologies, the units should only be those of dimensions, rather than of any other unit of scientific measurement. It is widely agreed that nanoparticles are clusters of atoms in the size range of 1–100 nm (Williams, 2008). Nanomaterials often show unique and considerably changed physical, chemical and biological properties compared to their macro scaled counterparts (Li et al., 2001). Synthesis of noble metal nanoparticles for applications such as catalysis, electronics, optics, environmental and biotechnology is an area of constant interest ( Burleson et al., 2004; Address for correspondence: Abolfazl Akbarzadeh, Department of Medical Nanotechnology, Faculty of Advanced Medical Science, Tabriz University of Medical Sciences, Tabriz, Iran. E-mail: [email protected] San Woo Joo, School of Mechanical Engineering, WCU Nanoresearch Center, Yeungnam University, Gyeongsan 712-749, South Korea. E-mail: [email protected] Kazem Nejati-Koshki, Department of Medical Nanotechnology, and Department of Medical Biotechnology Faculty of Advanced Medical Science, Tabriz University of Medical Sciences, Tabriz, Iran. E-mail: [email protected] Mohammad Samiei, Department of Endodontics, Dental School, Tabriz University of Medical Sciences, Tabriz, Iran

History Received 28 January 2014 Revised 1 April 2014 Accepted 2 April 2014 Published online 17 June 2014

Cheng, 2004; Hussain et al., 2003; Masciangioli & Zhang, 2003; Obare & Meyer, 2004; Yuan, 2004). Gold, silver and copper have been used mostly for the synthesis of stable dispersions of nanoparticles, which are useful in areas such as photography, catalysis, biological labeling, photonics, optoelectronics and surface-enhanced Raman scattering (SERS) detection (Smith et al., 2006). Silver nanoparticles are of interest due to the exclusive properties (e.g. size and shape depending optical, electrical and magnetic properties) which can be incorporated into antimicrobial applications, biosensor materials, composite fibers, cryogenic superconducting materials, cosmetic products and electronic components (Caro et al., 2010). Silver bio-nanoparticles (AgNPs) have been known to have inhibitory and bactericidal effects. Resistance to antimicrobial agents by pathogenic bacteria has emerged in recent years and is a major health problem (Nanda & Saravanan, 2009). Several physical and chemical methods have been used for synthesizing and stabilizing silver nanoparticles (Klaus-Joerger et al., 2001). The most popular chemical approaches, including chemical reduction using a variety of organic and inorganic reducing agents, electrochemical techniques, physicochemical reduction and radiolysis are widely used for the synthesis of silver nanoparticles. Recently, nanoparticle synthesis is among the most interesting scientific areas of inquiry, and there is growing attention to produce nanoparticles using environmentally friendly methods (green chemistry). Green synthesis approaches include mixed-valence polyoxometalates, polysaccharides, Tollens, biological and irradiation method which have advantages

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over conventional methods involving chemical agents related with environmental toxicity. However, recent developments include means of protecting efficiently silver nanoparticles that offer far improved chemical stabilities. As a result, silver nanoparticles are rapidly gaining in popularity and several research groups have begun to explore alternative strategies for the development of optical sensors and imaging labels based on the unexpected optical properties of these metal nanoparticles (Caro et al., 2010).

Synthesis of silver nanoparticles Conventionally, nanomaterials are synthesized using either chemical or physical methods which include sol process, micelle, chemical precipitation, hydrothermal method, pyrolysis and chemical vapor deposition (Bai et al., 2007; Jung et al., 2006; Kruis et al., 2000; Leela & Vivekanandan, 2008; Mafune et al., 2001; Nickel et al., 2000; Shirtcliffe et al., 1999). Some of these methods are easy and make available control over crystallite size by restoring the reaction environment. But problem still exists with the general stability of the product and in achieving monodisperse nanosize using these methods (Kowshik et al., 2002). Moreover, many of the usual techniques have been found to be capital special and inefficient in materials and energy use. Physical approaches In physical processes, metal nanoparticles are generally synthesized by evaporation–condensation, which could be carried out using a tube furnace at atmospheric pressure. The foundation material within a boat centered at the furnace is vaporized into a carrier gas. Nanoparticles of various materials, such as Ag, Au, PbS and fullerene, have previously been produced using the evaporation/condensation technique (Gurav et al., 1994; Magnusson et al., 1999). Nevertheless, the generation of silver nanoparticles (AgNPs) using a tube furnace has several drawbacks, because a tube furnace occupies a large space, consumes a great deal of energy while raising the environmental temperature around the source material, and requires a lot of time to achieve thermal stability. A typical tube furnace requires power using up of more than several kilowatts and a pre-heating time of several tens of minutes to attain a stable operating temperature. Moreover, AgNPs have been synthesized with laser ablation of metallic bulk materials in solution (Chen & Yeh, 2002; Kabashin & Meunier, 2003; Mafune et al., 2000, 2001; Sylvestre et al., 2004; Tsuji et al., 2001, 2002, 2003). One advantage of laser ablation compared to other conventional method for preparing metal colloids is the absence of chemical reagents in solutions. Therefore, pure colloids, which will be useful for more applications, can be produced by this method (Tsuji et al., 2002). Chemical approaches The most common approach for synthesis of silver nanoparticles is chemical reduction by organic and inorganic reducing agents. In general, different reducing agents, such as sodium citrate, ascorbate, sodium borohydride (NaBH4), elemental hydrogen, polyol process, Tollens reagent,

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N,N-dimethylformamide (DMF) and poly(ethylene glycol)block copolymers are used for reduction of silver ions (Ag+) in aqueous or non-aqueous solutions. The aforementioned reducing agents reduce silver ions (Ag+) and lead to the formation of metallic silver (Ag0), which is followed by agglomeration into oligomeric clusters. These clusters eventually lead to formation of metallic colloidal silver particles (Evanoff & Chumanov, 2004; Wiley et al., 2005). It is essential to use protective agents to stabilize nanoparticles during the course of silver nanoparticle preparation, and protect the nanoparticles that can be absorbed on or bind onto nanoparticle surfaces, avoiding their agglomeration (Oliveira et al., 2005). The presence of surfactants comprising functionalities (e.g. thiols, amines, acids and alcohols) for interactions with particle surfaces can stabilize particle growth, and protect particles from sedimentation, agglomeration or losing their surface properties. Polymeric compounds such as poly(vinyl alcohol), poly(vinylpyrrolidone), poly(ethylene glycol), poly(methacrylicacid) and polymethylmethacrylate have been reported to be effective protective agents to stabilize nanoparticles Valizadeh H et al. (2012). Tollens method The Tollens synthesis method gave AgNPs with a controlled size in a one-step process (He et al., 2006; Kvı´tek et al., 2005; Saito et al., 2003; Yin et al., 2002). The basic Tollens reaction involves the reduction of Ag(NH3)2+ (aq), a Tollens reagent, by an aldehyde (Sergeev, 2003). AgðNH3 Þþ2ðaqÞþRCHOðaqÞ ! AgðsÞþRCOOHðaqÞ In the modified Tollens procedure, Ag+ ions are reduced by saccharides in the presence of ammonia, yielding AgNP films with particle sizes from 50 to 200 nm, Ag hydrosols with particles in the order of 20–50 nm, and AgNPs of different shapes ( Kvı´tek et al., 2005; Saito et al., 2003). Ag(NH3)2+ is a stable complex ion resulting from ammonia’s strong affinity for Ag+, therefore the ammonia concentration and nature of the reductant must play a major role in controlling the AgNP size (Kvı´tek et al., 2005). To better understand, the synthesis process let us consider this example. A research study on the saccharide reduction of Ag+ ions by the modified Tollens process revealed that the smallest particles were formed at the lowest ammonia concentration (Kvı´tek e al., 2005). Green synthesis Biological method The development of biologically inspired experimental processes for the synthesis of nanoparticles is evolving into an important branch of nanotechnology (Ahmad et al., 2003; Shankar et al., 2004). Biologically synthesized silver nanoparticles could have many applications such as, they might be used as spectrally selective coatings for solar energy absorption and intercalation material for electrical batteries, as optical receptors, for biolabeling, and as antimicrobials (Dura´n et al., 2005; Kowshik et al., 2003; Souza et al., 2004). There are a number of reports in the literature on the cellassociated biosynthesis of silver nanoparticles using several microorganisms, particularly Fusarium oxyporum (Ahmad

Silver nanoparticles

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et al., 2003; Dura´n et al., 2005; Joerger et al., 2000; Mukherjee et al., 2001). The cell mass of F. oxyporum, and the leached components from these fungi cells (Ahmad et al., 2003; Mukherjee et al., 2001), has been reported to reduce silver ion to silver nanoparticles. Between the environments of natural resources, prokaryotic bacteria have been most generally researched for synthesis of metallic nanoparticles. One of the reasons for ‘‘bacterial preference’’ for nanoparticles synthesis is their relative ease of manipulation. In one of the earliest studies in this technology, Slawson et al. found that a silver-resistant bacterial strain isolated from silver mines, Pseudomonas stutzeri AG259, accumulated AgNPs within the periplasmic space (Thakkar et al., 2010). Recently, a few microorganisms have been explored as potential biofactories for synthesis of metallic nanoparticles such as cadmium sulfide, gold and silver (Hussain et al., 2003; Li et al., 2001; Williams, 2008). Research in nanotechnology provides reliable, eco-friendly processes for the synthesis of nanoscale materials like bioprocesses and ‘‘green’’ chemistry. Inspiration from nature comes through magnetotactic bacteria synthesizing magnetite nanoparticles, diatoms synthesizing siliceous materials and S-layer bacteria producing gypsum and calcium carbonate layers. Duran et al. showed that silver nanoparticles (AgNPs), like their bulk counterpart, are an effective antimicrobial agent against various pathogenic microorganisms (Burleson et al., 2004). Although various chemical and biochemical methods are being explored for production of AgNPs, microbes are exceedingly effective in this process (Nanda & Saravanan, 2009). New enzymatic approaches using bacteria and fungi in the synthesis of nanoparticles both intra- and extra-cellularly have been expected to have a key role in many conventional and emerging technologies. Synthesis of nanoparticles was found to be intracellular in many cases but makes the job of downstream processing difficult (Figure 1). The bioreduction of the Ag+ ions could be associated with metabolic processes utilizing nitrate by reducing nitrate to nitrile and ammonium (Lengke et al., 2007). Cyanobacteria commonly use nitrate as the major source of nitrogen. Nitrate was reduced by cyanobacteria metabolic process. þ   NO 3 þ2H þ2e ¼ NO2 þH2 O

þ  þ NO 2 þ8H þ6e ¼ NH4 þ2H2 O

It suggests that Ag+ ions could be reduced by an intracellular electron donor (Figure 2; Lengke et al., 2007). Polysaccharide method In this method, AgNPs are prepared using water as an environmentally benign solvent and polysaccharides as a capping agent, or in some cases, polysaccharides serve as both a reducing and a capping agent. For instance, synthesis of starch-AgNPs was carried out with starch as a capping agent and b-D-glucose as a reducing agent in a gently heated system (Raveendran et al., 2003). The starch in the solution mixture avoided using of relatively toxic organic solvents (Amanullah & Yu, 2005). In addition, the binding interactions between starch and AgNPs are weak and can be reversible at higher

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Figure 1. Precipitated silver nanoparticles on the cyanobacteria cell surface.

Figure 2. Cyanobacteria cells with nanoparticles of silver inside the cell (Lengke et al., 2007).

temperatures, allowing separation of the synthesized particles (Akbarzadeh et al., 2012a–d, 2013a,b; Ghasemali et al., 2013; Mollazade et al., 2013; Nejati-Koshki et al., 2013; RezaeiSadabady et al., 2013; Valizadeh et al., 2012 ).

Applications Silver nanoparticles are of interest due to the unique properties (e.g. size and shape depend on optical, electrical and magnetic properties) which can be incorporated into antimicrobial applications, biosensor materials, composite fibers, cryogenic superconducting materials, cosmetic products and electronic components Albrecht et al. (2006). These particles also have many applications in different fields such as medical imaging, nano-composites, filters, drug delivery and hyperthermia of tumors (Pissuwan et al., 2006; Tan et al., 2006). Silver nanoparticles have drawn the attention of researchers due to their extensive applications in areas such as integrated circuits (Kotthaus et al., 1997) sensors, biolabeling, filters (Cao, 2004), antimicrobial deodorant fibers (Zhang & Wang, 2003), cell electrodes (KlausJoerger et al., 2001), low-cost paper batteries (silver nanowires; Hu et al., 2009) and antimicrobials (Cho et al., 2005; Dura´n et al., 2007). Silver nanoparticles have been used extensively as antimicrobial agents in health industry, food storage, textile coatings and a number of environmental applications (Table 1).

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Antibacterial applications Silver nanoparticles have important applications in the field of biology such as antibacterial agents and DNA sequencing Dolgaev et al. (2002). Silver has been known to exhibit strong toxicity to a wide range of microorganisms (antibacterial applications). Scientists have long known that silver ions, which flow from nanoparticles when oxidized, are deadly to bacteria Schmidt-Ott (1988). Silver nanoparticles are used just about everywhere, including in cosmetics, socks, food containers, detergents, sprays and a wide range of other products to stop the spread of germs (Figure 3). Medical applications One use of silver ion or metallic silver as well as silver nanoparticles can be exploited in medicine for burn treatment, dental materials, coating stainless steel materials, water treatment, sunscreen lotions, etc (Dura´n et al., 2007). Catalysis applications Nanocatalysis has recently been a rapidly growing field which involves the use of nanoparticles as catalysts. It is well known that metals such as Au, Ag and Pt and metal ions can catalyzed the decomposition of H2O2 to oxygen Merga et al. (2007). It was observed, when the Ag colloid was injected, chemiluminescence emission from the luminal-H2O2 system was greatly enhanced (Guo et al., 2008). Silver is also the most popular catalyst for the oxidation of ethylene to ethylene Table 1. Applications of silver nanoparticles in pharmaceutics, medicine and dentistry (Caro et al., 2010). Pharmaceutics and medicine

Dentistry

Treatment of dermatitis; Inhibition of HIV-1 replication Treatment of ulcerative colitis and acne Antimicrobial effects against infectious organisms Remote laser light-induced opening of microcapsules Silver/dendrimer nanocomposite for cell labeling Molecular imaging of cancer cells Enhanced Raman scattering (SERS) spectroscopy Detection of viral structures (SERS and silver nanorods) Coating of hospital textile (surgical gowns, face mask) Coating of catheter for cerebrospinal fluid drainage Coating of surgical mesh for pelvic reconstruction Coating of breathing mask patent Coating of endotracheal tube for mechanical ventilator support Coating of driveline for ventricular assist devices Coating of central venous catheter for monitoring Additive in bone cement Implantable material using clay-layers with starchstabilized AgNPs Coating of intramedullary nail for long bone fractures Coating of implant for joint replacement Orthopedic stockings Superabsorbant hydrogel for incontinence material Hydrogel for wound dressing Additive in polymerizable dental materials patent Silver-loaded SiO2 nanocomposite resin filler (dental resin composite) Polyethylene tubes filled with fibrin sponge embedded with AgNPs dispersion

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oxide and methanol to formaldehyde as catalysts. It is well known that metals such as Au, Ag and Pt and metal ions can catalyzed the decomposition of H2O2 to oxygen. It was observed, when the Ag colloid was injected, chemiluminescence emission from the luminal-H2O2 system was greatly enhanced. Silver is also the most popular catalyst for the oxidation of ethylene to ethylene oxide and methanol to formaldehyde (Guo et al., 2008). Silver nanoparticles immobilized on silica spheres have been tested for their ability to catalyze the reduction of dyes by sodium borohydride (NaBH4). Catalysis of dyes was chosen as it is easy to detect a change in color when the dyes are reduced. In the absence of silver nanoparticles, the sample was almost stationary showing very little or no reduction of the dyes. Figure 4 shows how the absorbance spectrum of the dyes decreases when the dyes are reduced (Jiang et al., 2005). Optical applications The extraordinary optical properties of noble metal nanoparticles have been taken advantage of optical biosensors and chemosensors. One of research subject focused on the measurement of biological binding signal between antigen and antibody using the triangular Ag-nanoparticles (Zhu et al., 2009). Optical sensor of zeptomole (1021) sensitivity is another possible application using the potential of silver nanoparticles. Using the surface Plasmon resonance effect, the silver nanoparticles gain a very high sensitivity and the measurements can be conducted in real-time. Silver nanoparticles showed that a peak in extinction, due to the localized surface Plasmon resonance (LSPR) effect. One of the possible applications of the high sensitivity of the LSPR is for in vivo detection. It is possible to monitor the quantity of chemical species inside a cell as well as monitoring the dynamical processes that occur (Mcfarland & Van Duyne, 2009). Electrochemical applications Furthermore, the electrochemical properties of AgNPs incorporated them in nanoscale sensors that can offer faster

Figure 3. Silver ions delivered by nanoparticles to bacteria promote lysis, the process by which cells break down and ultimately die, which makes silver nanoparticles a superior and widely used antibacterial agent. As anti-bacterial agents, AgNPs were applied in a wide range of applications from disinfecting medical devices and home appliances to water treatment (Bosetti et al., 2002; Cho et al., 2005; Gupta, 1998; Jain et al., 2005; Li et al., 2008).

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Figure 4. (a) Silver nanoparticles immobilized on silica spheres are illustrated. (b) The absorbance spectrum of the dyes decreases as the dyes are reduced by sodium borohydride. This process is catalyzed by silver nanoparticles. The arrow marks the increase of reaction time (Modak et al., 1973).

response times and lower detection limits. For instance electrodeposited AgNPs onto alumina plates gold micropatterned electrode that showed a high sensitivity to hydrogen peroxide (Abou El-Nour et al., 2010).

Properties Human beings are often infected by microorganisms such as bacteria, molds, yeasts and viruses in the living environment. Research in antibacterial material containing various natural and inorganic substances (Cho et al., 2005; Kim et al., 1998) has been intensive. Metal nanoparticles (Me-NPs), which have a high specific surface area and a high fraction of surface atoms, have been studied extensively due to their unique physicochemical characteristics including catalytic activity, optical properties, electronic properties, antimicrobial activity and magnetic properties (Dura´n et al., 2005; Kowshik et al., 2003; Souza et al., 2004). Among Me-NPs, silver nanoparticles (Ag-NPs) have been known to have inhibitory and bactericidal effects (Cho et al., 2005). It can be expected that the high specific surface area and high fraction of surface atoms of Ag-NPs will lead to high antimicrobial activity as compared with bulk silver metal (Cho et al., 2005). The combined effects of Ag-NPs with the antibacterial activity of antibiotics have not been studied. Silver nanoparticle – optical properties There is growing interest in utilizing the optical properties of silver nanoparticles as the functional component in various products and sensors. Silver nanoparticles are extraordinarily efficient at absorbing and scattering light and, unlike many dyes and pigments, have a color that depends upon the size and the shape of the particle. The strong interaction of the silver nanoparticles with light occurs as the conduction electrons on the metal surface undergo a collective oscillation when excited by light at specific wavelengths known as a surface Plasmon resonance (SPR), this oscillation results in unusually strong scattering and absorption properties. In fact, silver nanoparticles can have effective extinction (scattering + absorption) cross sections up to 10 times larger than their physical cross section. The strong scattering cross section

allows for sub 100 nm nanoparticles to be easily visualized with a conventional microscope. When 60 nm silver nanoparticles are illuminated with white light they appear as bright blue point source scatters under a dark field microscope. The bright blue color is due to an SPR that is peaked at a 450 nm wavelength. A unique property of spherical silver nanoparticles is that this SPR peak wavelength can be tuned from 400 nm (violet light) to 530 nm (green light) by changing the particle size and the local refractive index near the particle surface. Even larger shifts of the SPR peak wavelength out into the infrared region of the electromagnetic spectrum can be achieved by producing silver nanoparticles with rod or plate shapes (Abou El-Nour et al., 2010). Silver nanoparticle – surface chemistry When nanoparticles are, in solution, molecules associate with the nanoparticle surface to establish a double layer of charge that stabilizes the particles and prevents aggregation. Aldrich Materials Science offers several silver nanoparticles suspended in a dilute aqueous citrate buffer, which weakly associates with the nanoparticle surface (Abou El-Nour et al., 2010). Biological properties of silver nanoparticles Agent is not new, and silver compounds were shown to be effective against both aerobic and anaerobic bacteria by precipitating bacterial cellular proteins and by blocking the microbial respiratory chain system (Barreiro et al., 2007; Bragg & Rainnie, 1974; George et al., 1997; Leaper, 2006; Modak & Fox, 1973; Thomas et al., 2007). Before the advent of silver nanoparticles, silver nitrate was an effective antibacterial agent used clinically (Chen & Schluesener, 2008; Chu et al., 1988; Gravante et al., 2009; Monteiro et al., 2009). The possible mechanisms of action are: (1) Better contact with the microorganism nanometer scale, silver provided an extremely large surface area for contact with bacteria. The nanoparticles get attached to the cell membrane and also penetrate inside the bacteria (Feng et al., 2000; Rai et al., 2009).

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Figure 5. Schematic drawing showing the various mechanisms of antibacterial activities exerted by silver nanoparticles.

(2) Bacterial membranes contain sulfur-containing proteins and AgNPs, like Ag+, interact with them as well as with phosphorus-containing compounds like DNA, inhibit the function (Liau et al., 1997; Matsumura et al., 2003). (3) Silver (nanoparticles or Ag+) can attack the respiratory chain in bacterial mitochondria and lead to cell death (Sondi & Salopek-Sondi, 2004). (4) AgNPs can have a sustained release of Ag+ once inside the bacterial cells (in an environment with lower pH), which may create free radicals and induce oxidative stress, thus further enhancing their bactericidal activity (Figure 5; Morones et al., 2005; Song et al., 2006). Furthermore, a recent study showed that yeast and E. coli were inhibited at a low concentration of AgNPs, study of mechanisms revealed that free radicals and oxidative stress were responsible for the antibacterial activities (Kim et al., 2006).

Authors contributions SWJ conceived the study and participated in its design and coordination. AA, and MM participated in the sequence alignment and drafted the manuscript. EA, HT, KN and YH helped in drafting the manuscript. All authors read and approved the final manuscript.

Acknowledgements The authors thank the Department of Medical Nanotechnology, Faculty of Advanced Medical Science of Tabriz University for all the support provided. This work is funded by Grant 2011-0014246 of National Research Foundation of Korea.

Declaration of interest The authors declare that they have no competing interests.

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