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Silver nanotechnology has received tremendous attention in recent years, owing to its wide range of applications in various fields and its intrinsic therapeutic properties. In this review, an attempt is made to critically evaluate the chemical, physical, and biological synthesis of silver nanoparticles (AgNPs) as well as their efficacy in the field of theranostics including microbiology and parasitology. Moreover, an outlook is also provided regarding the performance of AgNPs against different biological systems such as bacteria, fungi, viruses, and parasites (leishmanial and malarial parasites) in curing certain fatal human diseases, with a special focus on cancer. The mechanism of action of AgNPs in different biological systems still remains enigmatic. Here, due to limited available literature, we only focused on AgNPs mechanism in biological systems including human (wound healing and apoptosis), bacteria, and viruses which may open new windows for future research to ensure the versatile application of AgNPs in cosmetics, electronics, and medical fields.
The focus of this review is to provide a comprehensive, well-elaborated, and up-to-date view about what is currently investigated about the antimicrobial and antiparasitic activities and various methods used for the synthesis of AgNPs. Besides, we strive to compile all the most recent investigations about the applications of AgNPs in many fields with a special focus on cancer and viral infection inhibition, and the toxicology of AgNPs. We strongly believe that this review will provide a handy mechanistic framework for the future analysis of AgNPs.
Nowadays, the applications of nanoparticles are tremendously increasing as they possess unique optical, chemical, electrical, electronic, and mechanical properties. These properties are attributed to their large surface area-to-volume ratio, which imparts them unique properties as compared to atoms/molecules as well as the bulk of the same material. Metallic particles, specifically AgNPs, are in focus due to their antimicrobial resistance as metal ions, while antibiotics are losing their effectiveness due to development of resistant strains of microbes. 1 Although the antimicrobial properties of AgNPs are extensively studied, their activities against other types of pathogens such as arthropods and different types of cancer cells have been evaluated only recently. AgNPs as therapeutic agents have achieved remarkable attention in the treatment of cancer, leishmania, malaria, and many other human diseases. However, there still remain many questions that are a matter of discussion for future research.
Currently, different metals including zinc, titanium and copper, 9 magnesium and gold, 10 , 11 and alginate 12 are used as antimicrobial agents, but among these AgNPs have been found to be the most efficient due to their outstanding antimicrobial properties. 13 In particular, nanosilver has been verified to have a great medicinal value attributable to its characteristic antibacterial, 13 , 14 antifungal, 9 antiviral, 15 antiprotozoal, 16 anticatalytic, 17 and antiarthropodal characteristics. 18 In cancer, metastasis is a great challenge to oncologists and clinicians due to the development of resistance to anticancer agents; 19 however, this problem can be overcome by nanoscale materials, especially nanosilver.
Various terminologies are used for silver particles such as colloidal silver, nano-silver, silver nanostructures, and silver nanoparticles (AgNPs). For the sake of convenience, we use the abbreviation AgNPs throughout this review. Nanotechnology is an advanced field dealing with the manufacturing of different kinds of nanomaterials having biomedical applications. 4 Due to a wide range of transmittable diseases caused by different pathogenic bacteria and their enhanced antibiotic resistance, many pharmaceutical companies and researchers are striving for synthesizing novel materials with enhanced antibacterial activity and reduced side effects. Currently, nanoscale materials have achieved considerable attention as novel antimicrobial agents due to their high surface area-to-volume ratio and distinct physical and chemical properties. 5 – 7 The extremely strong broad-spectrum antimicrobial property of AgNPs is the key direction for the improvement of AgNPs-based biomedical products, including bandages, catheters, antiseptic sprayers, textiles, and food storage containers. 8
“Nano” is a Greek word meaning small or dwarf. Nanoparticles can be defined as the particles ranging in size from 1 to 100 nm in either direction but can be considered as ranging up to several hundred nanometers. 1 These are actually aggregates of atoms, ions, or molecules. 1 In other words, “nano” is used to represent one billion of a meter or can be referred to as 10 −9 m. The concept of nanotechnology was first defined by Professor Norio Taniguchi in 1974, and since then, the field of nanotechnology has been receiving immense attention, especially from the early 1980s. 2 , 3
Graphene oxide (GO), an oxidized form of graphene, has been extensively used for various applications since the discovery of graphene in 2004. 207 Recently, GO has been utilized as a platform for growing NPs or attaching pre-synthesized NPs on its surface to produce NP-GO nanocomposites (NCs). Interestingly, NP-GO NCs exhibit enhanced surface enhanced Raman scattering, catalytic, and antibacterial properties compared to bare GO and NP. 208 – 213 Recent studies reported the fabrication of AgNPs-decorated GO as an effective antibacterial agent. 213 – 216
Over the past decade, silk fibroin has been applied in tissue engineering as a degradable surgical suture and scaffold 197 , 198 for its good biocompatibility, controllable biodegradability, and easy fabrication into different forms, such as fibers, films, gels, and three-dimensional scaffolds. 199 Silk fibroin is a good candidate for biomineralization. Previous works have indicated that silk fibroin regulates the morphologies of inorganic nanoparticles during the biomineralization process. 200 , 201 Silk fibroin contains 18 types of amino acid residues, including some polar amino acids such as tyrosine (Tyr). Tyr endows silk fibroin with the electron-donating property. The electron-donating property of the phenolic hydroxyl group of Tyr could directly reduce silver ion to AgNP. 202 Thus, it is possible to synthesize AgNPs through the reduction of Ag + by silk fibroin in situ to prepare the antibacterial silk film. Biopolymer film such as AgNPs silk is limited in its packaging application due to its poor mechanical property. To improve the mechanical property, biopolymer–polymer interaction is developed by blending natural biopolymers with polymers. PVA is a biodegradable, biocompatible, water-soluble, and nontoxic semicrystalline polymer. It offers good thermomechanical property, thermal stability, mechanical strength, and flexibility, as well as good optical and physical properties that are crucial for packaging application. 203 , 204 Moreover, PVA is approved by the US Food and Drug Administration as an indirect food additive for flexible food packaging. 205 , 206 The combination of AgNPs, silk fibroin, and PVA will be promising for active packaging.
Sericin, a globular glue protein, is exclusively produced in the middle silk gland of silkworm when silkworm spins a cocoon for protective and adhesive effects. 195 Silkworm cocoon is usually composed of about 75% fibroin and 25% sericin. However, sericin has been disposed of as a waste during the silk reeling process in the past few thousand years. It is not only a great waste of natural resources but also causes serious environmental pollution. Modern studies propounded that sericin performs a variety of biological activities, such as anticoagulation, antioxidant, antibacterial, and mitogenic effects, on mammalian cells. In regenerative medicines, it is usually mingled with functional polymers to form various scaffolds for biomedical purposes. 195
Cellulose is also one of the most important groups of polysaccharides, and due to its unique properties, cellulose is considered as an excellent template for the nanosilver formation. Both soluble and insoluble cellulose have been employed for the preparation of AgNPs, where alcohol and aldehyde groups performed an important role in the stabilization and reduction of silver ions 191 as presented in . Recently, the green synthesis of AgNPs using hydroxyl propyl cellulose (HPC) has also been reported. HPC plays a dual role (reducer and stabilizer) in the synthesis of AgNPs. 192 , 193 Insoluble cellulose was also investigated for the synthesis of AgNPs. Furthermore, it was indicated that various types of fibers were used in the silver salt solution. Meanwhile, experimental results showed that AgNPs of undetectable size to 160 and 50 nm were deposited on cotton and viscose fibers, respectively. Recently, cotton fabrics were investigated for the synthesis of the AgNPs. Trisodium citrate was used as a reducing agent at 90°C. Experimental results indicated that 20–90 nm AgNPs can be obtained. 194
It was also found that gum ghatti and gum kondagogu can be used as stabilizer and reducing agent for the synthesis of AgNPs. 180 , 181 Using gum ghatti, narrow-sized (4.8–6.4 nm) AgNPs were produced, whereas gum kondagogu produced 2–9 nm AgNPs. 181 Moreover, AgNPs of undetectable size to 25 nm (spherical) were also obtained from alkali-soluble xanthan and acacia. 182 , 183 Schizophyllan 184 and hyaluronic acid (HA) 185 were used as reducer and stabilizing agent for the synthesis of AgNPs. HA was analyzed chemically and thermally, and the results showed that 5–30 nm AgNPs can be obtained. 185 Similarly, carboxymethyl chitosan and N-phthaloyl chitosan were also used in the preparation of nanosilver. 186 – 188 In a recent report, it was investigated that under acidic medium, silver chitosan film was formed due to the mixing of both silver salts and chitosan. 189 Also, acidic medium and chitosan were used as chelating agents for AgNPs. 190
The starch solution (reducing/capping agent) and AgNO 3 (salt) have been used for the synthesis of AgNPs, and using these agents, stable AgNPs sized 10–34 nm were formed. These nanoparticles were stable in the aqueous solution at 25°C for around 3 months. 172 Similarly, small-sized AgNPs (5–20 and ≤10 nm) can be prepared using starch (stabilizer and capping agent) and NaOH solution having glucose (reducing agent). 173 , 174 Small-sized (1–21 nm) and spherical-shaped AgNPs have been synthesized using carboxymethyl starch in aqueous solution with a stability of more than 3 months at 25°C. 175 The alkaline solutions can also be used for solubilization of spherical nanoparticles in starch. 176 Recent studies revealed that ester of alginic acid (sodium and calcium alginate) can be used for the preparation of AgNPs. 177 , 178 Some studies also reported that the spherical-shaped and small-sized (1–4 nm) AgNPs can be obtained in 1 min from sodium alginate using water as solvent at 70°C. 179
Polysaccharides have been widely used for biomedical applications, as they are biocompatible and biodegradable. Polysaccharides are considered as excellent templates for the preparation of nanosilvers. Polysaccharides play a dual role, that is, reductants and/or capping agents, in the synthesis of AgNPs. For more than a decade, gentle heating of starch (capping agent) and β-d-glucose (reducing agent) has resulted in the formation of AgNPs. 171
Algae have been recently studied for the synthesis of AgNPs. Venkatpurwar and Pokharkar reported the formation of AgNPs from aquatic red algae using sulfated polysaccharides. These AgNPs were highly constant at broad pH range (2–10) and showed effective antibacterial activity against Gram-negative than Gram-positive bacteria. 167 El-Rafie et al extracted water-soluble polysaccharides from aquatic microalgae. These polysaccharides were used as both reducing and stabilizing agents for AgNPs formation. The colloidal solutions imparted antimicrobial activity when tested on cotton fabrics. 168 More recently, Salari et al were able to synthesize AgNPs from macroalgae Spirogyra varians through bio-reduction of silver ions. These AgNPs functioned as efficient bactericidal mediators in response to many pathogenic bacteria. 169 Some other algal species, namely Tetraselmis gracilis, Chaetoceros calcitrans, Isochrysis galbana, and Chlorella salina, can be successfully used for the AgNPs biosynthesis. 170
The spherical nanosilver can also be synthesized using Coriolus versicolor, but the reduction of AgNPs is time consuming (ie, 72 h; however, the duration could be reduced to 1 h by tailoring the reaction conditions using alkaline media at pH 10). The alkaline media play a vital role in the bio-reduction of silver ions, water hydrolysis, and interaction with protein functionalities. Furthermore, the S–H group from the protein plays an excellent role in the bio-reduction, whereas glucose molecule also plays a significant role in the reduction of AgNPs. 165 Aspergillus flavus can also be used to obtain stable nanosilver with more than 3 months of stability in aqueous solution. Meanwhile, the stabilizing agents released by fungal species ensure prevention of aggregation. 166
Balaji et al used an extracellular solution of Cladosporium cladosporiodes for the reduction of AgNO 3 to form spherical-shaped AgNPs of 10–100 nm size. They further reported that C. cladosporiodes released some organic materials, including polysaccharides, organic acids, and proteins, which were responsible for the formation of spherical crystalline AgNPs. 126 Penicillium spp. were also used for the production of AgNPs. 163 Soil-isolated Penicillium spp. J3 which has the ability to produce silver nanoparticles was used for the synthesis, and the AgNPs formation took place on the surface of the cells in which proteins acted as stabilizing agents. 164
Recent studies showed that AgNPs of size 5–25 and 5–50 nm could be extracellularly synthesized using Aspergillus fumigatus and Fusarium oxysporum, respectively. 161 , 162 The authors further reported that most of the nanoparticles were spherical in shape; however, rare triangular-shaped nanoparticles were also noticed. 161
Green and/or biogenic synthesis of any type of nanoparticles involves natural processes occurring in microorganisms like fungi, bacteria, and plants, as shown in . These organisms generate biocompatible nanostructures having excellent therapeutic potential. 131 Fungi-based synthesis of AgNPs is also eco-friendly and of low cost. In a recent study, two fungal strains, namely Penicillium expansum HA2N and Aspergillus terreus HA1N, were reported for the synthesis of AgNPs. The transmission electron microscopy result showed that 14–25 nm AgNPs were obtained from P. expansum, while 10–18 nm AgNPs were obtained from A. terreus. The efficacy of these AgNPs was further examined against different fungal species which demonstrated their strong antifungal potential. 62
Like other methods, metal precursors or silver salts are also used in the preparation of silver nanostructure from bacterial cultures. The production of AgNPs using sulfide (Ag 2 S) and oxide (Ag 2 O) of silver has also been reported by various studies. 31 , 156 In a recent report, the culture supernatant of bacterium Bacillus licheniformis was used to produce 40 and 50 nm AgNPs, respectively. 157 , 158 AgNPs of 1–6 nm size has also been produced using visible light emission from the supernatants of Klebsiella pneumoniae. 159 Furthermore, it was also found that Lactobacillus strains can be used for the production of AgNPs. 155 , 160 Recently, the bacterial strains of Aeromonas spp. SH10 and Corynebacterium spp. SH09 were screened for the biosynthesis of AgNPs. The authors concluded from their results that the bio-reduction of [Ag(NH 3 ) 2 ] + resulted in the production of monodispersed and stable AgNPs. 153
Klaus et al were the first to explore the ability of the bacterium Pseudomonas stutzeri AG259 to synthesize AgNPs. The bacteria exhibited a remarkable property of surviving in an extreme silver-rich environment, which might be the possible explanation for the accumulation of nanosilver. 150 Nanosilver particles have been synthesized using both Gram-positive and Gram-negative bacteria including the silver-resistant bacteria to form AgNPs. 151 Some bacteria have the ability to produce extracellular AgNPs, while others can synthesize intracellular AgNPs. Interestingly, some bacteria including Calothrix pulvinata, Anabaena flos-aquae, 152 Vibrio alginolyticus, 33 Aeromonas spp. SH10, 153 Plectonema boryanum UTEX 485, 154 and Lactobacillus spp. 155 have the ability to produce both extra- and intracellular AgNPs.
The biosynthesis of AgNPs was reported for the first time using identified antimicrobial molecules (gallic acid + apocynin) and (gallic acid +
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