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Review

Biogenic Nanosilver against Multidrug-Resistant Bacteria (MDRB)

Laboratory of Chemical Biology, Institute of Chemistry, State University of Campinas, Campinas 13083-970, Brazil
*
Author to whom correspondence should be addressed.
Present address: School of Bioprocess and Chemical Engineering, University College Dublin, Dublin D04 V1W8, Ireland
Submission received: 28 June 2018 / Accepted: 31 July 2018 / Published: 2 August 2018
(This article belongs to the Special Issue Silver-Based Antimicrobials)

Abstract

:
Multidrug-resistant bacteria (MDRB) are extremely dangerous and bring a serious threat to health care systems as they can survive an attack from almost any drug. The bacteria’s adaptive way of living with the use of antimicrobials and antibiotics caused them to modify and prevail in hostile conditions by creating resistance to known antibiotics or their combinations. The emergence of nanomaterials as new antimicrobials introduces a new paradigm for antibiotic use in various fields. For example, silver nanoparticles (AgNPs) are the oldest nanomaterial used for bactericide and bacteriostatic purposes. However, for just a few decades these have been produced in a biogenic or bio-based fashion. This review brings the latest reports on biogenic AgNPs in the combat against MDRB. Some antimicrobial mechanisms and possible silver resistance traits acquired by bacteria are also presented. Hopefully, novel AgNPs-containing products might be designed against MDR bacterial infections.

Graphical Abstract

1. Introduction

Antimicrobial resistance refers to the evolutionary capacity developed by microorganisms such as bacteria, fungi, viruses, and parasites to fight and neutralize an antimicrobial agent. According to the World Health Organization (WHO) [1], the intensive use and misuse of antimicrobials has led to an expansion of the number and types of resistant organisms. Moreover, the use of sub-therapeutic antibiotic doses to prevent diseases in animal breeding to improve animal growth can select resistant microorganisms, which can possibly disseminate to humans [2].
The number of pathogens presenting multidrug resistance has had an exponential increase in recent times and is considered an important problem for public health [3]. A wide number of bacteria have been reported as multidrug-resistant (MDR), and they present a high cost of management, including medicines, staff capacity, isolation materials [4], and productivity loss [5]. For instance, in the USA, the cost of conventional tuberculosis treatment for the drug-susceptible bacterium is $17,000 and up to $482,000 for the treatment of the MDR bacterium [5]. In 2017, WHO published the first list of antibiotic-resistant pathogens offering risk to human health and, as such, the development of new drugs is crucial. Priority 1 (critical) microorganisms are carbapenem-resistant Acinetobacter baumannii; carbapenem-resistant Pseudomonas aeruginosa; and carbapenem-resistant, ESBL-producing Enterobacteriaceae. Accounting for priority 2 (high) are vancomycin-resistant Enterococcus faecium; methicillin-resistant, vancomycin-intermediate and resistant Staphylococcus aureus; clarithromycin-resistant Helicobacter pylori; fluoroquinolone-resistant Campylobacter spp.; fluoroquinolone-resistant Salmonellae; and cephalosporin-resistant, fluoroquinolone-resistant Neisseria gonorrhoeae. In priority 3 (medium) are penicillin-non-susceptible Streptococcus pneumoniae, ampicillin-resistant Haemophilus influenzae, and fluoroquinolone-resistant Shigella spp. [6].
The use of drugs combinations, two or more antimicrobial drugs to combat MDRB [7], is already employed in cancer therapy [8], HIV-patients [9], and malaria patients [10]. On the other hand, research groups around the globe are suggesting innovative solutions to treat resistant organisms. Xiao et al. [11] synthesized the block copolymer poly (4-piperidine lactone-b-ω-pentadecalactone) with high antibacterial activity against E. coli and S. aureus, and low toxicity to NIH-3T3 cells, and suggested that cationic block copolymer biomaterials can be employed in medicine and implants. Zoriasatein et al. [12] showed that a derivative peptide from the snake (Naja naja) has an antimicrobial effect against S. aureus, B. subtilis, E. coli, and P. aeruginosa. Al-Gbouri and Hamzah [13] reported that an alcoholic extract of Phyllanthus emblica exhibits antimicrobial activity against E. coli, S. aureus, and P. aeruginosa and it inhibits biofilm formation of P. aeruginosa. Naqvi et al. [14] suggested the combined use of biologically synthesized silver nanoparticles (AgNPs) and antibiotics to combat the MDRB.
The increasing utilization and in-depth studies of nanomaterials have brought new perspectives towards new antimicrobial materials and nanocomposites that could add-in to the MDRB pandemic that we are currently facing. Nanoparticles and nanocomposites comprising zinc oxide [15], copper oxide [16], iron oxide [17], and, especially, silver, have been widely used in textiles [18,19], dental care [20], packaging [21], paints [22], and in a whole myriad of applications. Silver nanoparticles are one of the most exploited nanomaterials for this end, as they have been used for over a century in the healing of wounds and burns. Although chemical methods were successfully employed for AgNPs synthesis, with the need to use sustainable and non-toxic methods in chemistry, a biocompatible modality of AgNPs synthesis came about by using biological routes for nanoparticle synthesis (Figure 1). Biosynthesis or bio-based synthesis of AgNPs may occur through three routes: fungal, bacterial, or by plants, for the reduction of Ag+ to Ag0. The saturation of Ag0 monomers in suspension eventually leads to a burst-nucleation process [23] in which nanoclusters of metallic silver are produced and stabilized by biomolecules from the biological extracts.
The demand of products for the combat of MDR bacterial strains such as Pseudomonas aeruginosa, methicillin-resistant Staphylococcus aureus (MRSA), vancomycin-resistant Staphylococcus aureus (VRSA), erythromycin-resistant Streptococcus pyogenes, and ampicillin-resistant Escherichia coli [24] has led to the design of powerful antimicrobial materials that are reinforced with silver nanoparticles [25]. Today, in medicinal practice, there are wound dressings, contraceptive devices, surgical instruments, bone prostheses, and dental implants which are coated or embedded with nanosilver [26,27,28,29,30,31]. In daily life, consumers may find nanosilver in room sprays, laundry detergents, water purification devices and paints [26,32,33]. In the final part of this review, some of the recent advances in patented technologies containing AgNPs that establish viable grounds for the development of biogenic AgNPs-containing products for MDRB eradication purposes are cited and discussed.

2. Antibiotics

Antibiotics gained popularity because of their effectiveness or activities against microorganisms, as described by Selman Waksman [34], and refers to an application, and not a class of compound or its function [35]. The first compound with antibacterial activity discovered was arsphenamine, synthesized in 1907 by Alfred Bertheim in Paul Ehrlich’s laboratory, with antisyphilitic activity identified in 1909 by Sahachiro Hata [36,37]. Classically, the golden era of antibiotics refers to the period between the 50s and 70s, when the discovery of different classes of antibiotics took place [38]. For a more detailed review of antibiotics and antibacterial drugs, see Bbosa et al., 2014 [39]. Figure 2 illustrates the main antibiotic classes and examples of compounds, with corresponding dates of discovery and resistance as first reported.

3. The Emerging of Antimicrobial Resistance

One of the most famous antibiotics, Penicillin, was discovered in 1928 by Alexander Fleming. In 1940, before its public use, the same group identified a bacterial penicillinase [47], an enzyme able to degrade penicillin. This fact can now be related to the number of antibiotic genes that are naturally present in microbial populations [48]. In Japan, during the 50s, genetically transferable antibiotic resistance was identified. This discovery introduced the concept that antibiotic genes could spread among a population of bacterial pathogens using bacterial conjugation [49,50]. This horizontal gene transfer is important throughout genome evolution and currently presents a serious threat [51]. The bacterial genetic elasticity prompts the acquisition of genetic material, mutational adaptations, or changes in gene expression, leading to the survival of the fittest organism and the generation of resistance to antibiotics [52]. For more details regarding antibiotic resistance development, mechanisms, emergence, and spread see further references [52,53,54,55,56,57,58].
Currently, we face a deficiency in the development of new antibiotics to face the growing antimicrobial resistance. The constant increment in the emergence of resistant strains has not been balanced by the availability of new therapeutic agents for many reasons [59,60]. Firstly, policy-makers want to avoid the use of new antibiotics until they are indispensable, because of the resistance development. On the other hand, society needs the pharmaceutical industry to design and develop new drugs, which should not be used. Moreover, antibiotics are used in the short-term, which does not help companies to make a sustained profit. Also, the excessive cost of development and the regulatory onus makes it difficult to attend a demand for cheap antibiotics [61]. Looking at this alarming scenario the design of new therapeutics and/or new approaches is imperative.

4. Biogenic AgNPs as a Weapon against Multidrug-Resistant Bacteria (MDRB)

Traditionally, the synthesis of AgNPs using chemical approaches has been the most explored for a better size and shape control, preparation of nanocomposites and elucidation of electronic properties. However, the necessity of applying the well-known antibacterial activity of AgNPs in biological systems propelled the development of a new synthesis approach. The biological, biogenic, or bio-based methods for AgNPs synthesis present four main advantages: (1) increased biocompatibility, once AgNPs are produced in water and capped with biomolecules such as proteins, sugars or metabolites; (2) diminished toxicity, as the reducing agents are natural compounds that usually have mild reducing strength; (3) easy production, such as preparation of an extract from fungi, bacteria or plants, followed by the addition of a silver salt (typically, silver nitrate); and (4) low cost [62]. Despite positive aspects, the lack of control of shape and size of the nanoparticles is still a challenge for biogenic synthesis methods.
Because every biological synthesis is different from another as a consequence of using distinct species, the capping agents on the surface of the nanoparticles may differ. The concept of “protein corona” [63], for instance, describes the existence and dynamics of a protein shell surrounding nanoparticles in a biological environment or after a biological synthesis [64]. The interaction of biologically synthesized AgNPs with a bacterial cell will inherently involve the contact with the microorganism and the outer biomolecule shell. Thus, this interaction is unique as new joint effects (between biomolecules and the silver itself) can arise and improve the antibacterial action due to a change in toxicity, cell uptake, and bio-distribution [65].
In the case of MDRB, the mechanism of action of AgNPs is distinct from the mechanism by which traditional antibiotics act, and thus resistance does not pose an obstacle that cannot be overcome in most cases. In the following sections, each type of biological synthesis is detailed along with a literature review of biogenic AgNPs being used against MDRB. In most of the papers reviewed, the bacterial strains used for susceptibility and antibacterial tests were clinical isolates from hospital patients, however the list of antibiotics to which the strain is resistant is not always described. Also, in many cases the strain used is standardized (ATCC strains, for example), but no details on the drug resistance capacity are provided. Here, we emphasize the examples where the provenience and description of the bacterial strain are well detailed, along with a robust antibacterial testing methodology.

4.1. Fungal AgNPs against MDRB

The synthesis of AgNPs using fungal cells may be performed outside the cells (extracellular synthesis) or inside the cells (intracellular synthesis) [66]. The former is the most recurrent in the literature, in which a fungal filtrate is obtained after the cultivation of the microorganism and a silver salt solution is added to it. Advantages of extracellular synthesis include ease of purification (as nanoparticles are not inside or attached to the fungus), facilitated downstream processing, and improved size control [67]. Despite usually having high reproducibility, fungal syntheses are time-consuming, as the fungi grow at a slower rate when compared to bacteria or the preparation of a plant extract. Moreover, the reduction of silver ions is also a gradual process, taking up to 96 h for completion. Fusarium oxysporum is perhaps the most studied species for AgNPs biosynthesis [19,68]; the mechanism of nanoparticle formation involves the reduction of silver(I) by a nitrate reductase and a shuttle quinone [69]. Scandorieiro et al. [70] demonstrated the synergistic effect of F. oxysporum produced AgNPs with oregano essential oil against a range of antibiotic-resistant bacterial strains, including MRSA and beta-lactamase producing strains. Naqvi et al. [14] also showed the effectiveness of a synergistic approach by combining Aspergillus flavus produced AgNPs with well-known commercial antibiotics resulting in an increase of up to 7-fold in the area of inhibition against bacterial strains resistant to the same antibiotics. In fact, a combinational therapy is highly desirable taking into consideration the development of AgNPs tolerance in bacteria via genetic evolution [71]. Chowdhury et al. studied the effect of AgNPs synthesized by Macrophomina phaseolina against ampicillin and chloramphenicol resistant E. coli and noted plasmid fragmentation and a decrease of supercoiled plasmid content upon incubation of the circular DNA with nanoparticles [72]. On the other hand, nanoparticle attachment to the cell wall and leakage of cell components induced by Penicillium polinicum-produced AgNPs were observed in transmission micrographs by Neethu et al. [73], which confirms that more than one antibacterial mechanism is possible (this theme is further explored in Section 4.4). Table 1 brings a summary of fungal AgNPs and their activity against MDR bacterial strains.

4.2. Bacterial AgNPs against MDRB

Similarly to fungal biosynthesis, bacterial AgNPs biosynthesis may also be performed extra- or intracellularly [82]. The former can be done by using the cell biomass, where the reducing agents are secreted by the cells and the nanoparticles formed might be attached to the bacterial wall (which can possibly extend the purification process). In contrast, using a bacterial supernatant/cell-free extract has the advantage of facilitating the downstream process and purification procedures by utilizing a sterile biomolecule-rich mixture to synthesize the nanoparticles, often with the aid of microwave [83] or light irradiation [84]. Conversely, the intracellular AgNPs synthesis takes place inside the cell, often in the periplasmic space [85]. This mechanism requires a certain metal resistance from the bacteria [86] or exposure to very low concentrations of the silver salt, as the Ag+ ion must be imported without causing any major damage. The biggest disadvantage of this method is the purification as the nanoparticles must be removed from the interior of the cells. Ultrasonication is usually the most common method used for this end [87].
Singh et al. [88] prepared AgNPs from the culture supernatant of Aeromonas sp. THG-FG1.2 extracted from soil and obtained inhibition of several bacterial strains otherwise completely insensitive to erythromycin, lincomycin, novobiocin, penicillin G, vancomycin, and oleandomycin. Desai et al. [89] reported a hydrothermal biosynthesis of AgNPs using a cell-free extract of Streptomyces sp. GUT 21 by autoclaving the bacterial extract along with a silver salt solution. The nanoparticles were between 20–50 nm in size and active towards MDRB up to a concentration of 10 µg mL−1. Sunlight exposure is also a good methodology for AgNPs biosynthesis, as demonstrated by Manikprabhu et al. [90]. Nanoparticles were produced from Sinomonas mesophila MPKL 26 cell supernatant in contact with silver nitrate upon up to 20 min of sun exposure. Specific secreted extracellular compounds can also be used for AgNPs synthesis. Santos et al. [91] attribute the formation of AgNPs smaller than 10 nm to xanthan gum produced during the growth of Xanthomonas spp. The nanoparticles could inhibit, to a certain extent, the growth of MDR Acinetobacter baumannii and Pseudomonas aeruginosa. Table 2 brings a summary of AgNPs produced by bacteria with activity against MDRB.

4.3. AgNPs from Plants against MDRB

Production of AgNPs using plant extracts is perhaps the most explored method in biogenic synthesis, probably due to the easiness of the procedure and wide availability of species to work with [101]. The whole plant, the stem, pod, seeds, fruit, flowers, and, most frequently, leaves are used to prepare an extract, which may be done in cold or hot solvent and almost always utilizes water (despite the fact that organic solvent extracts have also been used). The abundance of components such as reducing sugars, ascorbic acid [102], citric acid [103], alkaloids and amino acids [104], along with slightly soluble terpenoids [105], flavonoids [106], and other metabolites in various parts of the plant may easily act as reducing agents, converting Ag+ to AgNPs in shorter times (when compared to fungal or bacterial syntheses). Due to the lower protein content in most plants, the capping biomolecule shell often has a significant contribution of polysaccharides [107] and other molecules. Most reports on plant biosynthesis are studies of plant species found in the surroundings of the university or city where the laboratory is located, however, in vitro-derived culture of plants can also be used for these purposes [108].
Ma et al. [107] reported on the biosynthesis of 60 nm AgNPs using polysaccharide-rich root extract of Astragalus membranaceus and compared the bacterial inhibition against reference strains of E. coli, P. aeruginosa, S. aureus, and S. epidermidis with clinically isolated MDR strains of these bacteria. Interestingly, the nanoparticles were slightly more active toward the resistant strains.
The nanoparticle size is known to play an important role in antibacterial activity [24], and this is no different for MDR strains. AgNPs synthesized by Caesalpinia coriaria leaf extract, which were 50–53 nm were shown to be more active towards MDR bacterial clinical isolates when compared to 79–99 nm AgNPs [109].
Despite the common belief that biological synthesis implies a lack of control for Ag+ reduction and poor shape control, Jinu et al. [110] demonstrated the synthesis of cubic and triangular shaped 20 nm AgNPs using Solanum nigrum leaf extract. The nanoparticles had a contributing effect along with the antimicrobial plant extract towards six MDRB strains. Moreover, these AgNPs showed antibiofilm activity against P. aeruginosa and S. epidermidis. Prasannaraj et al. [111] reported an extensive study using ten different plant species for AgNPs biosynthesis, yielding spherical, cubic, and fiber-like nanoparticles. All of them inhibited bacterial growth of clinically isolated MDR pathogens and some also displayed antibiofilm activity against P. aeruginosa and S. epidermidis. The authors correlate the results with the 3 to 4-fold increase in reactive oxygen species (ROS) by AgNPs.
Intracellular ROS production was also observed by flow cytometry for Ocimum gratissimum leaf extract-produced AgNPs [112]; the authors suggest that the membrane damage caused by the nanoparticles could prevent efficient electronic transport in the respiratory chain. This was confirmed by micrographs of MDR E. coli and S. aureus cells treated with AgNPs, which showed leakage of intracellular content and pits in the membrane.
The antibacterial properties of silver can also be delivered by silver chloride nanoparticles (AgCl-NPs), as shown by Gopinath et al. [113]. AgNPs and AgCl-NPs were produced from Cissus quadrangularis leaf extract and were active towards both Gram-negative and Gram-positive MDR strains. In this case, chloride ions were identified in the extract and attributed to the formation of AgCl nanocrystals.
Table 3 presents the gathered data on plant biosynthesis of AgNPs with the corresponding activity against MDRB.

4.4. Modes of Action of AgNPs against Bacteria

As stated in previous reviews on the subject [24,133,134,135,136,137], the antibacterial action of silver nanoparticles involves a complex mechanism in which more than one factor can act simultaneously to contribute to an overall effect. Moreover, one must consider the existence of more than one silver species, these being the Ag0 in the form of nanoparticles and the Ag+ which is released from the surface of the nanoparticles as they are slowly oxidized.
Proteomic analysis of E. coli proteins expressed after exposure to AgNPs and Ag+ revealed that both have a similar mode of action, such as overexpressing envelope and heat shock proteins. However, the nanoparticles were effective at inhibiting bacteria in the nanomolar concentration, whereas the Ag+ ions were effective only in the micromolar range [138]. On the other hand, further reports point to the opposite direction. Ag+ release depends on oxidation of metallic silver by oxygen in the air; in a study where E. coli was exposed to AgNPs in anaerobic conditions, no bactericidal activity was observed, while in aerobic conditions the usual antimicrobial activity was noticed [139]. This effect can be partially explained by a strong interaction of Ag+ with the cell membrane and cell wall components such as proteins, phospholipids, and thiol-containing groups, as well as by a proton leakage that can induce cell disintegration [140]. As much as the affinity of Ag+ for thiol groups has been known for decades [141], just recently Liao et al. [142] demonstrated how Ag+ can deplete intracellular thiol content of S. aureus and bind to cysteine residues of thioredoxin reductase’s catalytic site. This enzyme is one of the most important ones related to the antioxidant mechanism and reactive oxygen species (ROS) levels regulation in bacteria. Binding to respiratory chain enzymes is also a factor for intracellular ROS increase [143]. It is worth noting, however, that the protein corona that involves AgNPs has a significant effect on silver ions release. According to a study performed by Wen et al. [144], the binding of cytoskeletal proteins to AgNPs led to a decrease in Ag+ leakage, which could suggest that, similarly, biogenic AgNPs that are capped by biomolecules also have a diminished Ag+ release and thus their antimicrobial action would rely much less on this species.
Regarding the action of the nanoparticles, their size, shape and capping molecules may play significant roles when binding to the cell wall, membrane, and their internalization. In a study performed with silver nanospheres, nanocubes, and nanowires, the latter resulted in diminished antimicrobial activity when compared to the first two due to a smaller effective contact area with the cell membrane [145]. The same explanation applies for truncated octahedral AgNPs outperforming spherical AgNPs [146]. Truncated triangular shaped AgNPs had a better performance than all the other shapes in a study conducted against E. coli [147]. Acharya et al. [148] recently reported a study on silver nanospheres and silver nanorods acting against K. pneumoniae and attributed the antibacterial activity to the {111} plane shapes, which contain the highest atomic density. Smaller sizes of nanoparticles also lead to an enhanced bactericidal effect [149,150]. This effect is due to a greater surface area in contact with the bacteria that facilitate membrane rupture and internalization [151].
Perhaps one of the most accepted antibacterial mechanisms involves the association of nanoparticles with the cell wall followed by the formation of “pits” [152] and leakage of cellular contents [153]. This corroborates with the fact that AgNPs are usually more active towards Gram-negative bacteria [154], as Gram-positive bacteria have a thicker peptidoglycan cell wall, which could act as an additional physical barrier. Once inside the bacterial cell (a process that is facilitated by sizes smaller than 5 nm [155]), small nanoparticles are able to interfere with the respiratory chain dehydrogenases [156] and also induce generation of intracellular ROS [112,157], which have the ability to cleave DNA [158] and diminish bacterial life. It must be also pointed out that the interaction of AgNPs with the media which they are suspended in has a great influence on AgNPs physicochemical properties and their action on bacterial cells [159]. Figure 3 illustrates all the major mechanisms by which AgNPs display their antibacterial action.

4.5. Bacterial Resistance to Silver

The increasing application of silver nanomaterials in dressings, packages, and textiles has raised concerns about the development of bacterial resistance to nanosilver, despite the good performance of AgNPs against a range of bacterial strains, as already described. In fact, one of the first reports on resistance to silver was published in 1975, when a strain of Salmonella typhimurium resistant to silver nitrate, mercuric chloride, and a range of common antibiotics was identified in three patients in a burn unit [160]. Decades later, this exogenous type of resistance was unveiled by Gupta et al. [161] through the isolation of the plasmid pMG101. This plasmid was identified as the carrier of a silver resistance gene silE, which encodes a 143-amino-acid periplasmic Ag+-specific protein. Upstream of silE, a series of genes from the Sil system encode silver efflux-related proteins, such as a protein/cation antiporter system and a P-type cation ATPase (Figure 4). Resistance to silver attributed to sil genes was also recently reported for clinical isolates of Klebsiella pneumonia and Enterobacter cloacae [162]. Endogenous (mutational) silver resistance may also be observed, as reported by Li et al. [163], who observed silver resistance induced in E. coli cells by selectively culturing bacterial cells in increasing concentrations of silver nitrate. In this case, mutant cells were deficient in major porins (OmpF and OmpC). Silver efflux is also mediated through a CusCFBA efflux pump system, which has a high amino acid sequence similarity with the Sil system, in spite of being an endogenous type of resistance [164]. Crystal structures of proteins of the CusCFBA system suggest a methionine shuttle efflux mechanism, in which Ag+ ions are ejected from the bacterial periplasm [165,166]. Nuclear magnetic resonance (NMR) and inductively coupled plasma mass spectrometry (ICP-MS) studies have demonstrated that silver ions may induce a histidine kinase (CuS) dimerization and this conformational change may have a reflex on the upregulation of genes encoding the CusCFBA transport system [167]. The E. coli gene ybdE belonging to the K38 chromosome was also pointed out as related exclusively to Ag+ resistance since its deletion in silver-resistant mutant strains had no effect on Cu+ resistance [168]. Graves et al. [71] recently performed an extensive study using a non-resistant E. coli strain for an evolutionary analysis focused on mutations acquired upon exposure to silver nitrate and silver nanoparticles. After 300 generations, the Minimum Inhibitory Concentration (MIC) (using more than one type of AgNPs) of treated bacteria was already between 1.40 and 4.70 times the MIC of control bacteria. Three main mutations were observed: (1) in the cuS gene, which encodes the already mentioned histidine kinase which functions as a sensor for the CusCFBA efflux pump; (2) in the purL gene, which encodes for an enzyme involved in de novo purine nucleotide biosynthesis; and (3) in the rpoB gene, responsible for an RNA polymerase beta subunit.
It is worth noting, however, that most of the studies cited are related to exogenous and endogenous Ag+ resistance. The release of Ag+ ions by AgNPs is only one of the forms by which AgNPs might be antimicrobial, as explained in Section 4.4. Few studies have looked at resistance to silver nanoparticles. For instance, Panacek et al. [169] have observed E. coli resistance to 28 nm AgNPs in sub-MIC concentrations without any genetic changes noted in E. coli. Only a phenotypic change in production of flagellin was noted. Flagellin, an adhesive protein of the flagellum, related to biofilm formation and motility, was found to readily induce nanoparticle aggregation and attenuate their antimicrobial capacity. There is still much to be researched and discovered on outer membrane–metal interactions, especially what accounts for different capping agents, topography, and morphology of AgNPs. Also, other bacterial species and strains must be studied as to map genetic and/or phenotype modifications induced by AgNPs.

5. Nanosilver Applications in Antimicrobial Products

The well-documented antimicrobial activities of AgNPs have attracted great attention from researchers and companies and caused manufacturing of many products which are in everyday use. For instance, dressings, biomedical equipment, paints, packaging materials, and gels containing nanosilver formulations are widely used. However, the number of AgNPs-containing products that are focused on or have been tested against MDRB is still unexpressive and modest. This is even surprisingly true when it comes to biogenically or bio-based synthesized AgNPs. Nevertheless, among many patents of products containing nanosilver, there are some possible applications of patented formulations in the combat against resistant bacteria, which are summarized in Table 4.
Despite the controversy that involves the oral use of silver nanoparticles, a recent patent has established a preparation involving AgNPs active towards MDRB suggesting many possible forms of administration, including oral, topical, and intravenous [171]. An invention communicated by Holladay et al. [170] postulates compositions containing AgNPs that may be introduced into a hydrogel for the treatment of various types of infections and inflammations, with activity against MDR E. cloacae, K. pneumoniae, E. coli, P. aeruginosa, and A. Acinetobacter. In fact, the well-known wound healing capacity of nanosilver is often exploited in dressings and plasters. Liang et al. [178] developed an AgNPs/chitosan composite with amphiphilic properties—a hydrophobic and waterproof surface and a hydrophilic one with a capacity to interact with water and inhibit the growth of the drugs resistant S. aureus, E. coli, and P. aeruginosa. It is important to point out that these types of dressings with asymmetric wettability properties also enhance re-epithelization and collagen deposition and might be very helpful for wound healing not just because of their antiseptic properties.
Nanocrystalline silver coatings are already available commercially, for example, ACTICOAT™ has been used against MDR P. aeruginosa in burn wound infections in rat models [179]. This dressing has also been proven to be effective against methicillin-resistant S. aureus, by inhibiting bacterial growth in burn wounds. But it also decreases the secretion and swelling of the damaged tissue areas [180], which speeds up processes of wound healing.
An invention deposited by Paknikar (2006) [176] claims the production of biologically stabilized AgNPs, which were produced from various plants parts, and their incorporation into a variety of possible carriers, such as ointments, sprays, membranes, plasters. The nanoparticles were shown to successfully inhibit MDR strains of P. aeruginosa and other highly resistant bacterial strains: E. coli ATCC 117, P. aeruginosa ATCC 9027, S. abony NCTC 6017, S. typhimurium ATCC 23564, K. aerogenes ATCC 1950, P. vulgaris NCBI 4157, S. aureus ATCC 6538P, B. subtilis ATCC 6633., and C. albicans, and, interestingly, were non-cytotoxic towards human leukemic cells (K562), carcinoma cells (HEPG2), and mouse fibroblasts (L929) in the concentrations used against cited MRDB.
Also, there are some reports on materials that contain AgNPs, such as a multipurpose nanocomposite comprising silver nanotriangles and silicon dioxide, which was developed and tested against vancomycin-resistant bacteria E. Faecalis (ATCC 51299) [173]. There is a nanocomposite of silver and silver oxide active towards methicillin-resistant S. aureus and a broad spectrum of pathogenic bacteria associated with common infections and inflammations in humans [177].
Common household objects can also be enriched with AgNPs to enhance their antimicrobial potential; for example, nanosilver has been used as a detergent additive to enhance the antibiotic effect of the surfactant while not inducing any decrease in the detergent capability of a product [174]. The detergent can be used to disinfect resistant E. coli strains. Enhanced hygiene and diminished contamination were also achieved by reinforcing aprons with AgNPs; the material was successful in inhibiting methicillin-resistant S. aureus. Cheng and Yan [172] reported and patented the invention on antimicrobial plant fibers enriched with AgNPs that showed strong antimicrobial activity. This material may be applied in various types of linings, clothing, and even for fabricating laboratory or medical coats with improved disinfection properties and thus avoid bacterial contamination.
As stated, there are still much to be discovered and researched until novel fabrics, commodities, and/or pharmaceuticals based on biogenic or bio-based silver nanoparticles became suitable for everyday applications.

6. Conclusions

Some of the main reasons for observing the multidrug resistance in bacteria were discussed along with an introduction of biogenic silver nanoparticles as an alternative or combined technology to overcome this growing health problem. Even though bio-based silver containing nanomaterials are usually not ingested as known antibiotics, mainly due to a lack of understanding of the nanotoxicology associated with nanosilver in the bloodstream or in organs, AgNPs may be incorporated in products such as dressings, sprays, textiles, and paints for MDRB combat to a certain extent. Topical use of ointments and wound dressings have become quite common, as AgNPs not only inhibit bacteria growth but also stimulate epithelial growth and reduce swelling and secretion. Bacterial resistance to silver is a concerning perspective; however, application of bio-based AgNPs may at least postpone it because the extracts used for their synthesis might have natural antimicrobial effects that can act synergistically with the nanosilver. Moreover, combined therapies based on biogenic AgNPs and known antibiotics might be even more effective than the use of only one of them.
The development of biogenic AgNPs-containing products, which are active against MDRB, finds its main obstacle in discovering a systematic, easy to reproduce, and scaled-up process for the production of the uniform nanoparticles with desirable properties that do not vary, which is extremely hard to achieve considering the biological provenience of the extracts. By the time these processes become viable, controlled, and understood, the incorporation of the biologically synthesized nanomaterials as novel biopharmaceuticals or their use as commercial products should find many opportunities in various fields.

Author Contributions

C.H.N.B., S.F. and D.S. performed bibliographic research and wrote the first version of the manuscript. L.T. idealized and revised the manuscript and coordinated the project.

Funding

The authors acknowledge the financial supports received from the Fundação de Amparo à Pesquisa de São Paulo (Fapesp—Projects N°: 2015/12534-5 and 2014/50867-3) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq—Project N°: 465389/201407).

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. World Health Organization. 10 Facts on Antimicrobial Resistance. Available online: http://www.who.int/features/factfiles/antimicrobial_resistance/en/ (accessed on 10 June 2018).
  2. Littier, H.M.; Chambers, L.R.; Knowton, K.F. Animal agriculture as a contributor to the global challenge of antibiotic resistance. CAB Rev. 2017, 8, 1–9. [Google Scholar] [CrossRef]
  3. Roca, I.; Akova, M.; Baquero, F.; Carlet, J.; Cavaleri, M.; Coenen, S.; Cohen, J.; Findlay, D.; Gyssens, I.; Heure, O.E.; et al. The global threat of antimicrobial resistance: Science for intervention. New Microbe New Infect. 2015, 6, 22–29. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  4. Huebner, C.; Rogellin, M.; Flessa, S. Economic burden of multidrug-resistant bacteria in nursing homes in Germany: A cost analysis based on empirical data. BJM Open 2016, 6, e008458. [Google Scholar] [CrossRef] [PubMed]
  5. Centers for Disease Control and Prevention. Drug-Resistant TB. Available online: http://www.cdc.gov/tb/topic/drtb/ (accessed on 10 June 2018).
  6. World Health Organization. WHO Publishes List of Bacteria for Which New Antibiotics Are Urgently Needed. Available online: http://www.who.int/en/news-room/detail/27-02-2017-who-publishes-list-of-bacteria-for-which-new-antibiotics-are-urgently-needed (accessed on 10 June 2018).
  7. Worthington, R.J.; Melander, C. Combination approaches to combat multidrug-resistant bacteria. Trends Biotechnol. 2013, 31, 177–184. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  8. Lane, D. Designer combination therapy for cancer. Nat. Biotechnol. 2006, 24, 163–164. [Google Scholar] [CrossRef] [PubMed]
  9. Richman, D.D. HIV chemotherapy. Nature 2001, 410, 995–1001. [Google Scholar] [CrossRef] [PubMed]
  10. Nosten, F.; White, M.J. Artemisinin-based combination treatment of falciparum malaria. Am. J. Trop. Med. Hyg. 2007, 77, 191–192. [Google Scholar]
  11. Xiao, Y.; Wang, D.; Heise, A.; Lang, M. Chemo-enzymatic synthesis of poly (4-piperidine lactone-b-ω-pentadecalactone) block copolymers as biomaterials with antibacterial properties. Biomacromolecules 2018, 19, 2673–2681. [Google Scholar] [CrossRef] [PubMed]
  12. Zoriasatein, M.; Bidhendi, S.M.; Madani, R. Evaluation of antimicrobial properties of derivative peptide of Naja naja snake’s venom. World Fam. Med. J. 2018, 16, 44–62. [Google Scholar]
  13. Al-Gbouri, N.M.; Hamzah, A.M. Evaluation of Phyllanthus emblica extract as antibacterial and antibiofilm against biofilm formation. TIJAS 2018, 49, 142–151. [Google Scholar]
  14. Naqvi, S.Z.H.; Kiran, U.; Ali, M.I.; Jamal, A.; Hameed, A.; Ahmed, S.; Ali, N. Combined efficacy of biologically synthesized silver nanoparticles and different antibiotics against multidrug-resistant bacteria. Int. J. Nanomed. 2013, 8, 3187–3195. [Google Scholar] [CrossRef] [PubMed]
  15. Sirelkhatim, A.; Mahmud, S.; Seeni, A.; Kaus, N.H.M.; Ann, L.C.; Bakhori, S.K.M.; Hasan, H.; Mohamad, D. Review on zinc oxide nanoparticles: Antibacterial activity. Nano-Micro Lett. 2015, 7, 219–242. [Google Scholar] [CrossRef]
  16. Ingle, A.P.; Duran, N.; Rai, M. Bioactivity, mechanism of action, and cytotoxicity of copper-based nanoparticles: A review. Appl. Microbiol. Biotechnol. 2014, 98, 1001–1009. [Google Scholar] [CrossRef] [PubMed]
  17. Dinali, R.; Ebrahiminezhad, A.; Manley-Harris, M.; Ghasemi, Y.; Berenjian, A. Iron oxide nanoparticles in modern microbiology and biotechnology. Crit. Rev. Microb. 2017, 43, 493–507. [Google Scholar] [CrossRef] [PubMed]
  18. Dastjerdi, R.; Montazer, M. A review on the application of inorganic nano-structured materials in the modification of textiles: Focus on anti-microbial properties. Colloids Surf. B Biointerfaces 2010, 79, 5–18. [Google Scholar] [CrossRef] [PubMed]
  19. Ballottin, D.; Fulaz, S.; Cabrini, F.; Tsukamoto, J.; Durán, N.; Alves, O.L.; Tasic, L. Antimicrobial textiles: Biogenic silver nanoparticles against Candida and Xanthomonas. Mater. Sci. Eng. C 2017, 75, 582–589. [Google Scholar] [CrossRef] [PubMed]
  20. Ertem, E.; Guut, B.; Zuber, F.; Allegri, S.; Le Ouay, B.; Mefti, S.; Formentin, K.; Stellacci, F.; Ren, Q. Core-shell silver nanoparticles in endodontic disinfection solutions enable long-term antimicrobial effect on oral biofilms. ACS Appl. Mater. Interfaces 2017, 9, 34762–34772. [Google Scholar] [CrossRef] [PubMed]
  21. Nakazato, G.; Kobayashi, R.; Seabra, A.B.; Duran, N. Use of nanoparticles as a potential antimicrobial for food packaging. In Food Preservation, 1st ed.; Grumezescu, A., Ed.; Academic Press: Cambridge, MA, USA, 2016. [Google Scholar]
  22. Holtz, R.D.; Lima, B.A.; Filho, A.G.S.; Brocchi, M.; Alves, O.L. Nanostructured silver vanadate as a promising antibacterial additive to water-based paints. Nanomed. NBM 2012, 8, 935–940. [Google Scholar] [CrossRef] [PubMed]
  23. LaMer, V.K.; Dinegar, R.H. Theory, production and mechanism of formation of monodispersed hydrosols. J. Am. Chem. Soc. 1950, 72, 4847–4854. [Google Scholar] [CrossRef]
  24. Rai, M.K.; Deshmukh, S.D.; Ingle, A.P.; Gade, A.K. Silver nanoparticles: The powerful nanoweapon against multidrug-resistant bacteria. J. Appl. Microb. 2012, 112, 841–852. [Google Scholar] [CrossRef] [PubMed]
  25. Radetic, M. Functionalization of textile materials with silver nanoparticles. J. Mater. Sci. 2013, 48, 95–107. [Google Scholar] [CrossRef]
  26. Maneerung, T.; Tokura, S.; Rujiravanit, R. Impregnation of silver nanoparticles into bacterial cellulose for antimicrobial wound dressing. Carbohydr. Polym. 2008, 72, 43–51. [Google Scholar] [CrossRef]
  27. Chen, J.; Han, C.M.; Lin, X.W.; Tang, Z.J.; Su, S.J. Effect of silver nanoparticles dressing on second degree burn wound. Zhonghua Wai Ke Za Zhi 2006, 44, 50–52. [Google Scholar] [PubMed]
  28. Muangman, P.; Chuntrasakul, C.; Silthram, S.; Suvanchote, S.; Benhathanung, R.; Kttidacha, S.; Rueksomtawin, S. Comparison of efficacy of 1% silver sulfadiazine and Acticoat for treatment of partial-thickness burn wounds. J. Med. Assoc. Thail. 2006, 89, 953–958. [Google Scholar]
  29. Cohen, M.S.; Stern, J.M.; Vanni, A.J.; Kelley, R.S.; Baumgart, E.; Field, D.; Libertino, J.A.; Summerhayes, I.C. In vitro analysis of a nanocrystalline silver-coated surgical mesh. Surg. Infect. 2007, 8, 397–403. [Google Scholar] [CrossRef] [PubMed]
  30. Lansdown, A.B. Silver in health care: Antimicrobial effects and safety in use. Curr. Probl. Dermatol. 2006, 33, 17–34. [Google Scholar] [PubMed]
  31. Zhang, Z.; Yang, M.; Huang, M.; Hu, Y.; Xie, J. Study on germicidal efficacy and toxicity of compound disinfectant gel of nanometer silver and chlorhexidine acetate. Chin. J. Health Lab. Technol. 2007, 17, 1403–1406. [Google Scholar]
  32. Zhang, Y.; Sun, J. A study on the bio-safety for nano-silver as anti-bacterial materials. Chin. J. Med. Instrum. 2007, 31, 35–38. [Google Scholar]
  33. Nowack, B.; Krug, H.F.; Height, M. 120 Years of nanosilver history: Implications for policy makers. Environ. Sci. Technol. 2011, 45, 1177–1183. [Google Scholar] [CrossRef] [PubMed]
  34. Waksman, S. History of the word ‘antibiotic’. J. Hist. Med. Allied Sci. 1973, 28, 284–286. [Google Scholar] [CrossRef] [PubMed]
  35. Davies, J.; Davies, D. Origins and evolution of antibiotic resistance. Microbiol. Mol. Biol. Rev. 2010, 74, 417–433. [Google Scholar] [CrossRef] [PubMed]
  36. Williams, K. The introduction of ‘chemotherapy’ using arsphenamine—The first magic bullet. J. R. Soc. Med. 2009, 102, 343–348. [Google Scholar] [CrossRef] [PubMed]
  37. Izumi, Y.; Isozumi, K. Modern Japanese medical history and the European influence. Keio J. Med. 2001, 50, 91–99. [Google Scholar] [CrossRef] [PubMed]
  38. Amivov, R. A brief history of the antibiotic era: Lessons learned and challenges for the future. Front. Microbiol. 2010, 1, 134. [Google Scholar]
  39. Bbosa, G.; Mwebaza, N.; Odda, J.; Kyegombe, D.; Ntale, M. Antibiotics/antibacterial drug use, their marketing and promotion during the post-antibiotic golden age and their role in emergence of bacterial resistance. Health 2014, 6, 410–425. [Google Scholar] [CrossRef]
  40. Thal, L.; Zervos, M. Occurrence and epidemiology of resistance to virginiamycin and streptogramins. J. Antimicrob. Chemother. 1999, 43, 171–176. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  41. Manten, A.; Van Wijngaarden, L. Development of drug resistance to rifampicin. Chemotherapy 1969, 14, 93–100. [Google Scholar] [CrossRef] [PubMed]
  42. Chopra, I.; Roberts, M. Tetracycline antibiotics: Mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiol. Mol. Biol. Rev. 2001, 65, 232–260. [Google Scholar] [CrossRef] [PubMed]
  43. Kirst, H. Introduction to the macrolide antibiotics. In Macrolide Antibiotics Milestones in Drug Therapy MDT; Schönfeld, W., Kirst, H., Eds.; Birkhäuser: Basel, Switzerland, 2002; pp. 1–13. [Google Scholar]
  44. Jacoby, G. Mechanisms of resistance to quinolones. Clin. Infect. Dis. 2005, 41, S120–S126. [Google Scholar] [CrossRef] [PubMed]
  45. Madhavan, H.; Bagyalakshmi, R. Farewell, chloramphenicol? Is this true?: A review. J. Microbiol. Biotechnol. 2013, 3, 13–26. [Google Scholar]
  46. Mutnick, A.; Enne, V.; Jones, R. Linezolid resistance since 2001: SENTRY Antimicrobial Surveillance Program. Ann. Pharmacother. 2003, 37, 769–774. [Google Scholar] [CrossRef] [PubMed]
  47. Abraham, E.; Chain, E. An enzyme from bacteria able to destroy penicillin. Rev. Infect. Dis. 1940, 10, 677–678. [Google Scholar] [CrossRef]
  48. D’Costa, V.; McGrann, M.; Hughes, D.; Wright, G. Sampling the antibiotic resistome. Science 2006, 311, 374–377. [Google Scholar] [CrossRef] [PubMed]
  49. Davies, J. Vicious circles: Looking back on resistance plasmids. Genetics 1995, 139, 1465–1468. [Google Scholar] [PubMed]
  50. Helinski, D. Introduction to plasmids: A selective view of their history. In Plasmid Biology; Funnell, B., Philips, G., Eds.; ASM Press: Washington, DC, USA, 2004; pp. 1–21. [Google Scholar]
  51. Hacker, J.; Kaper, J. Pathogenicity islands and the evolution of microbes. Annu. Rev. Microbiol. 2000, 54, 641–679. [Google Scholar] [CrossRef] [PubMed]
  52. Munita, J.M.; Arias, C.A. Mechanisms of Antibiotic Resistance. Microbiol. Spectr. 2016, 4, 1–37. [Google Scholar]
  53. Steward, P.; Costerton, J. Antibiotic resistance of bacteria in biofilms. Lancet 2001, 358, 135–138. [Google Scholar] [CrossRef]
  54. Andersson, D. Persistence of antibiotic resistant bacteria. Curr. Opin. Microbiol. 2003, 6, 452–456. [Google Scholar] [CrossRef] [PubMed]
  55. Nikaido, H. Multidrug Resistance in Bacteria. Annu. Rev. Biochem. 2009, 78, 119–146. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  56. Kirbis, A.; Krizman, M. Spread of antibiotic resistant bacteria from food of animal origin to humans and vice versa. Procedia Food Sci. 2015, 5, 148–151. [Google Scholar] [CrossRef]
  57. Lee Ventola, C. The Antibiotic Resistance Crisis—Part 1: Causes and Threats. Pharm. Ther. 2015, 40, 277–293. [Google Scholar]
  58. Van Duin, D.; Paterson, D. Multidrug resistant bacteria in the community: Trends and lessons learned. Infect. Dis. Clin. N. Am. 2016, 30, 377–390. [Google Scholar] [CrossRef] [PubMed]
  59. The World Is Running out of Antibiotics, WHO Report Confirms. Available online: http://www.who.int/news-room/detail/20-09-2017-the-world-is-running-out-of-antibiotics-who-report-confirms (accessed on 10 June 2018).
  60. Davies, J. Where have all the antibiotics gone? Can. J. Infect. Dis. Med. Microbiol. 2006, 17, 287–290. [Google Scholar] [CrossRef] [PubMed]
  61. Why Are There So Few Antibiotics in the Research and Development Pipeline? Available online: https://www.pharmaceutical-journal.com/news-and-analysis/features/why-are-there-so-few-antibiotics-in-the-research-and-development-pipeline/11130209.article (accessed on 10 June 2018).
  62. Thakkar, K.N.; Mhatre, S.S.; Parikh, R.Y. Biological synthesis of metallic nanoparticles. Nanomed. NBM 2010, 6, 257–262. [Google Scholar] [CrossRef] [PubMed]
  63. Durán, N.; Silveira, C.P.; Durán, M.; Martinez, D.S.T. Silver nanoparticle protein corona and toxicity: A mini-review. J. Nanobiotechnol. 2015, 13, 1–17. [Google Scholar] [CrossRef] [PubMed]
  64. Ballottin, D.; Fulaz, S.; Souza, M.L.; Corio, P.; Rodrigues, A.G.; Souza, A.O.; Marcato, P.G.; Gomes, A.F.; Gozzo, F.; Tasic, L. Elucidating protein involvement in the stabilization of the biogenic silver nanoparticles. Nanoscale Res. Lett. 2016, 11, 1–9. [Google Scholar] [CrossRef] [PubMed]
  65. Shannahan, J.H.; Podila, R.; Aldossari, A.A.; Emerson, H.; Powell, B.A.; Ke, P.C.; Rao, A.M.; Brown, J.M. Formation of a protein corona on silver nanoparticles mediates cellular toxicity via scavenger receptors. Toxicol. Sci. 2014, 143, 136–146. [Google Scholar] [CrossRef] [PubMed]
  66. Rai, M.; Yadav, A.; Gade, A.K. Myconanotechnology: A new and emerging science. In Applied Mycology; Rai, M., Bridge, P.D., Eds.; CABI: Wallingford, UK, 2009; pp. 258–267. [Google Scholar]
  67. Zhao, X.; Zhou, L.; Rajoka, M.S.R.; Yan, L.; Jiang, C.; Shao, D.; Zhu, J.; Shi, J.; Huang, Q.; Yang, H.; et al. Fungal silver nanoparticles: Synthesis, application and challenges. Crit. Rev. Biotechnol. 2017, 38, 817–835. [Google Scholar] [CrossRef] [PubMed]
  68. Ahmad, A.; Mukherjee, P.; Senapati, S.; Mandal, D.; Khan, M.I.; Kumar, R.; Sastry, M. Extracellular biosynthesis of silver nanoparticles using the fungus Fusarium oxysporum. Colloids Surf. B 2003, 28, 313–318. [Google Scholar] [CrossRef]
  69. Durán, N.; Marcato, P.D.; Alves, O.L.; De Souza, G.I.H.; Esposito, E. Mechanistic aspects of biosynthesis of silver nanoparticles by several Fusarium oxysporum strains. J. Nanobiotechnol. 2005, 3, 8. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  70. Scandorieiro, S.; de Camargo, L.C.; Lancheros, C.A.C.; Yamada-Ogatta, S.F.; Nakamura, C.V.; de Oliveira, A.G.; Andrade, C.G.T.J.; Durán, N.; Nakazato, G.; Kobayashi, R.K.T. Synergistic and additive effect of oregano essential oil and biological silver nanoparticles against multidrug-resistant bacterial strains. Front. Microbiol. 2016, 7, 760. [Google Scholar] [CrossRef] [PubMed]
  71. Graves, J.L., Jr.; Tajkarimi, M.; Cunningham, Q.; Campbell, A.; Nonga, H.; Harrison, S.H.; Barrick, J.E. Rapid evolution of silver nanoparticle resistance in Escherichia coli. Front. Genet. 2015, 6, 42. [Google Scholar] [CrossRef] [PubMed]
  72. Chowdhury, S.; Basu, A.; Kundu, S. Green synthesis of protein capped silver nanoparticles from phytopathogenic fungus Macrophomina phaseolina (Tassi) Goid with antimicrobial properties against multidrug-resistant bacteria. Nanoscale Res. Lett. 2014, 9, 365. [Google Scholar] [CrossRef] [PubMed]
  73. Neethu, S.; Midhun, S.J.; Radhakrishnan, E.K.; Jyothis, M. Green synthesized silver nanoparticles by marine endophytic fungus Penicillium polonicum and its antibacterial efficacy against biofilm forming, multidrug-resistant Acinetobacter baumanii. Microb. Pathog. 2018, 116, 263–272. [Google Scholar] [CrossRef] [PubMed]
  74. Gopinath, P.M.; Narchonai, G.; Dhanasekaran, D.; Ranjani, A.; Thajuddin, N. Mycosynthesis, characterization and antibacterial properties of AgNPs against multidrug resistant (MDR) bacterial pathogens of female infertility cases. Asian J. Pharm. Sci. 2015, 10, 138–145. [Google Scholar] [CrossRef]
  75. Fayaz, A.M.; Balaji, K.; Girilal, M.; Yadav, R.; Kalaichelvan, P.T.; Venketesan, R. Biogenic synthesis of silver nanoparticles and their synergistic effect with antibiotics: A study against gram-positive and gram-negative bacteria. Nanomed. NBM 2010, 6, 103–109. [Google Scholar] [CrossRef] [PubMed]
  76. Bhat, M.A.; Nayak, B.K.; Nanda, A. Exploitation of filamentous fungi for biosynthesis of silver nanoparticle and its enhanced antibacterial activity. Int. J. Pharm. Biol. Sci. 2015, 6, 506–515. [Google Scholar]
  77. Ray, S.; Sarkar, S.; Kundu, S. Extracellular biosynthesis of silver nanoparticles using the mycorrhizal mushroom Tricholoma crassum (Berk.) SACC: Its antimicrobial activity against pathogenic bacteria and fungus, including multidrug resistant plant and human bacteria. Dig. J. Nanomater. Biostruct. 2011, 6, 1289–1299. [Google Scholar]
  78. Dhanasekaran, D.; Latha, S.; Saha, S.; Thajuddin, N.; Panneerselvam, A. Extracellular biosynthesis, characterisation and in-vitro antibacterial potential of silver nanoparticles using Agaricus bisporus. J. Exp. Nanosci. 2013, 8, 579–588. [Google Scholar] [CrossRef]
  79. Saravanan, M.; Nanda, A. Extracellular synthesis of silver bionanoparticles from Aspergillus clavatus and its antimicrobial activity against MRSA and MRSE. Colloids Surf. B Biointerfaces 2010, 77, 214–218. [Google Scholar] [CrossRef] [PubMed]
  80. Dar, M.A.; Ingle, A.; Rai, M. Enhanced antimicrobial activity of silver nanoparticles synthesized by Cryphonectria sp. evaluated singly and in combination with antibiotics. Nanomed. NBM 2013, 9, 105–110. [Google Scholar] [CrossRef] [PubMed]
  81. Hiremath, J.; Rathod, V.; Ninganagouda, S.; Singh, D.; Prema, K. Antibacterial activity of silver nanoparticles from Rhizopus spp against Gram negative E. coli-MDR strains. J. Pure Appl. Microbiol. 2014, 8, 555–562. [Google Scholar]
  82. Singh, R.; Shedbalkar, U.U.; Wadhwani, S.A.; Chopade, B.A. Bacteriagenic silver nanoparticles: Synthesis, mechanism, and applications. Appl. Microbiol. Biotechnol. 2015, 99, 4579–4593. [Google Scholar] [CrossRef] [PubMed]
  83. Saifuddin, N.; Wong, C.W.; Yasumira, A.A.N. Rapid biosynthesis of silver nanoparticles using culture supernatant of bacteria with microwave irradiation. E-J. Chem. 2009, 6, 61–70. [Google Scholar] [CrossRef]
  84. Zhang, X.; Yang, C.; Yu, H.; Sheng, G. Light-induced reduction of silver ions to silver nanoparticles in aquatic environments by microbial extracellular polymeric substances (EPS). Water Res. 2016, 106, 242–248. [Google Scholar] [CrossRef] [PubMed]
  85. Klaus, T.; Joerger, R.; Olsson, E.; Granqvist, C. Silver-based crystalline nanoparticles, microbially fabricated. Proc. Natl. Acad. Sci. USA 1999, 96, 13611–13614. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  86. Klaus-Joerger, T.; Joerger, R.; Olsson, E.; Granqvist, C. Bacteria as workers in the living factory: Metal-accumulating bacteria and their potential for materials science. Trends Biotechnol. 2001, 19, 15–20. [Google Scholar] [CrossRef]
  87. Kalishwaralal, K.; Deepak, V.; Pandian, S.R.K.; Kottaisamy, M.; BarathManiKanth, S.; Kartukeyan, B.; Gurunathan, S. Biosynthesis of silver and gold nanoparticles using Brevibacterium casei. Colloids Surf. B 2010, 77, 257–262. [Google Scholar] [CrossRef] [PubMed]
  88. Singh, H.; Du, J.; Yi, T. Biosynthesis of silver nanoparticles using Aeromonas sp. THG-FG1.2 and its antibacterial activity against pathogenic microbes. Artif. Cells Nanomed. Biotechnol. 2017, 45, 584–590. [Google Scholar] [CrossRef] [PubMed]
  89. Desai, P.P.; Prabhurajeshwar, C.; Chandrakanth, K.R. Hydrothermal assisted biosynthesis of silver nanoparticles from Streptomyces sp. GUT 21 (KU500633) and its therapeutic antimicrobial activity. J. Nanostruct. Chem. 2016, 6, 235–246. [Google Scholar] [CrossRef] [Green Version]
  90. Manikprabhu, D.; Cheng, J.; Chen, W.; Sunkara, A.K.; Mane, S.B.; Kumar, R.; Das, M.; Hozzein, W.N.; Duan, Y.; Li, W. Sunlight mediated synthesis of silver nanoparticles by a novel actinobacterium (Sinomonas mesophila MPKL 26) and its antimicrobial activity against multi drug resistant Staphylococcus aureus. J. Photochem. Photobiol. 2016, 158, 202–205. [Google Scholar] [CrossRef] [PubMed]
  91. Santos, K.S.; Barbosa, A.M.; Costa, L.P.; Pinheiro, M.S.; Oliveira, M.B.P.P.; Padilha, F.F. Silver nanocomposite biosynthesis: Antibacterial activity against multidrug-resistant strains of Pseudomonas aeruginosa and Acinetobacter baumannii. Molecules 2016, 21, 1255. [Google Scholar] [CrossRef] [PubMed]
  92. Subashini, J.; Khanna, V.G.; Kannabiran, K. Anti-ESBL activity of silver nanoparticles biosynthesized using soil Streptomyces species. Bioprocess Biosyst. Eng. 2014, 37, 999–1006. [Google Scholar] [CrossRef] [PubMed]
  93. Thomas, R.; Nair, A.P.; Mathew, J.; Ek, R. Antibacterial activity and synergistic effect of biosynthesized AgNPs with antibiotics against multidrug-resistant biofilm-forming coagulase-negative Staphylococci isolated from clinical samples. Appl. Biochem. Biotechnol. 2014, 173, 449–460. [Google Scholar] [CrossRef] [PubMed]
  94. Arul, D.; Balasubramani, G.; Balasubramanian, V.; Natarajan, T.; Perumal, P. Antibacterial efficacy of silver nanoparticles and ethyl acetate’s metabolites of the potent halophilic (marine) bacterium, Bacillus cereus A30 on multidrug resistant bacteria. Pathog. Glob. Health 2017, 111, 367–382. [Google Scholar] [CrossRef] [PubMed]
  95. Lateef, A.; Ojo, S.A.; Akinwale, A.S.; Azeez, L.; Gueguim-Kana, E.B.; Beukes, L.S. Biogenic synthesis of silver nanoparticles using cell-free extract of Bacillus safensis LAU 13: Antimicrobial, free radical scavenging and larvicidal activities. Biologia 2015, 70, 1295–1306. [Google Scholar] [CrossRef]
  96. Jain, D.; Kachhwaha, S.; Jain, R.; Srivastava, G.; Kothari, S.L. Novel microbial route to synthesize silver nanoparticles using spore crystal mixture of Bacillus thuringiensis. Indian J. Exp. Biol. 2010, 48, 1152–1156. [Google Scholar] [PubMed]
  97. Singh, G.; Babele, P.K.; Shahi, S.K.; Sinha, R.P.; Tyagi, M.B.; Kumar, A. Green synthesis of silver nanoparticles using cell extracts of Anabaena doliolum and screening of its antibacterial and antitumor activity. J. Microbiol. Biotechnol. 2014, 24, 1354–1367. [Google Scholar] [CrossRef] [PubMed]
  98. Saravanan, M.; Vemu, A.K.; Barik, S.K. Rapid biosynthesis of silver nanoparticles from Bacillus megaterium (NCIM 2326) and their antibacterial activity on multi drug resistant clinical pathogens. Colloids Surf. B Biointerfaces 2011, 88, 325–331. [Google Scholar] [CrossRef] [PubMed]
  99. Priyadarshini, S.; Gopinath, V.; Priyadharsshini, N.M.; MubarakAli, D.; Velusamy, P. Synthesis of anisotropic silver nanoparticles using novel strain, Bacillus flexus and its biomedical application. Colloids Surf. B Biointerfaces 2013, 102, 232–237. [Google Scholar] [CrossRef] [PubMed]
  100. Saravanan, M.; Barik, S.K.; MubarakAli, D.; Prakash, P.; Pugazhendhi, A. Synthesis of silver nanoparticles from Bacillus brevis (NCIM 2533) and their antibacterial activity against pathogenic bacteria. Microb. Pathog. 2018, 116, 221–226. [Google Scholar] [CrossRef] [PubMed]
  101. Ahmed, S.; Ahmad, M.; Swami, B.L.; Ikram, S. A review on plants extract mediated synthesis of silver nanoparticles for antimicrobial applications: A green expertise. J. Adv. Res. 2016, 7, 17–28. [Google Scholar] [CrossRef] [PubMed]
  102. Prathna, T.C.; Chandrasekaran, N.; Raichur, A.M.; Mukherjee, A. Biomimetic synthesis of silver nanoparticles by Citrus limon (lemon) aqueous extract and theoretical prediction of particle size. Colloids Surf. B Biointerfaces 2011, 82, 152–159. [Google Scholar] [CrossRef] [PubMed]
  103. Jiang, X.C.; Chen, C.Y.; Chen, W.M.; Yu, A.B. Role of citric acid in the formation of silver nanoplates through a synergistic reduction approach. Langmuir 2010, 26, 4400–4408. [Google Scholar] [CrossRef] [PubMed]
  104. Makarov, V.; Love, A.; Sinitsyna, O.; Yaminsky, S.M.; Taliansky, M.; Kalinina, N. Green nanotechnologies: Synthesis of metal nanoparticles using plants. Acta Naturae 2014, 6, 35–44. [Google Scholar] [PubMed]
  105. Singh, A.K.; Talat, M.; Singh, D.P.; Srivastava, O.N. Biosynthesis of gold and silver nanoparticles by natural precursor clove and their functionalization with amine group. J. Nanopart. Res. 2010, 12, 1667–1675. [Google Scholar] [CrossRef]
  106. Barros, C.H.N.; Cruz, G.C.F.; Mayrink, M.; Tasic, L. Bio-based synthesis of silver nanoparticles from orange waste: Effects of distinct biomolecule coatings on size, morphology, and antimicrobial activity. Nanotechnol. Sci. Appl. 2018, 11, 1–14. [Google Scholar] [CrossRef] [PubMed]
  107. Ma, Y.; Liu, C.; Qu, D.; Chen, Y.; Huang, M.; Liu, Y. Antibacterial evaluation of silver nanoparticles synthesized by polysaccharides from Astragalus membranaceus roots. Biomed. Pharmacother. 2017, 89, 351–357. [Google Scholar] [CrossRef] [PubMed]
  108. Anjum, S.; Abbasi, B.H. Biomimetic synthesis of antimicrobial silver nanoparticles using in vitro-propagated plantlets of a medicinally important endangered species: Phlomis bracteosa. Int. J. Nanomed. 2016, 11, 1663–1675. [Google Scholar]
  109. Jeeva, K.; Thiyagarajan, M.; Elangovan, V.; Geetha, N.; Venkatachalam, P. Caesalpinia coriaria leaf extracts mediated biosynthesis of metallic silver nanoparticles and their antibacterial activity against clinically isolated pathogens. Ind. Crops Prod. 2012, 52, 714–720. [Google Scholar] [CrossRef]
  110. Jinu, U.; Jayalakshmi, N.; Anbu, A.S.; Mahendran, D.; Sahi, S.; Venkatachalam, P. Biofabrication of cubic phase silver nanoparticles loaded with phytochemicals from Solanum nigrum leaf extracts for potential antibacterial, antibiofilm and antioxidant activities against MDR human pathogens. J. Clust. Sci. 2017, 28, 489–505. [Google Scholar] [CrossRef]
  111. Prasannaraj, G.; Venkatachalam, P. Enhanced antibacterial, anti-biofilm and antioxidant (ROS) activities of biomolecules engineered silver nanoparticles against clinically isolated Gram positive and Gram negative microbial pathogens. J. Clust. Sci. 2017, 28, 645–664. [Google Scholar] [CrossRef]
  112. Das, B.; Dash, S.K.; Mandal, D.; Ghosh, T.; Chattopadhyay, S.; Tripathy, S.; Das, S.; Dey, S.K.; Das, D.; Roy, S. Green synthesized silver nanoparticles destroy multidrug resistant bacteria via reactive oxygen species mediated membrane damage. Arab. J. Chem. 2017, 10, 862–876. [Google Scholar] [CrossRef] [Green Version]
  113. Gopinath, V.; Priyadarshini, S.; Priyadharsshini, N.M.; Pandian, K.; Velusamy, P. Biogenic synthesis of antibacterial silver chloride nanoparticles using leaf extracts of Cissus quadrangularis Linn. Mater. Lett. 2013, 91, 224–227. [Google Scholar] [CrossRef]
  114. Khalil, M.M.H.; Ismail, E.H.; El-Baghdady, K.Z.; Mohamed, D. Green synthesis of silver nanoparticles using olive leaf extract and its antibacterial activity. Arab. J. Chem. 2014, 7, 1131–1139. [Google Scholar] [CrossRef]
  115. Singh, K.; Panghal, M.; Kadyan, S.; Chaudhary, U.; Yadav, J.P. Green silver nanoparticles of Phyllanthus amarus: As an antibacterial agent against multi drug resistant clinical isolates of Pseudomonas aeruginosa. J. Nanobiotechnol. 2014, 12, 40. [Google Scholar] [CrossRef] [PubMed]
  116. Kasithevar, M.; Periakaruppan, P.; Muthupandian, S.; Mohan, M. Antibacterial efficacy of silver nanoparticles against multi-drug resistant clinical isolates from post-surgical wound infections. Microb. Pathog. 2017, 107, 327–334. [Google Scholar] [CrossRef] [PubMed]
  117. Gopinath, V.; MubarakAli, D.; Priyadarshini, S.; Priyadharsshini, N.M.; Thajuddin, N.; Velusamy, P. Biosynthesis of silver nanoparticles from Tribulus terrestris and its antimicrobial activity: A novel biological approach. Colloids Surf. B Biointerfaces 2012, 96, 69–74. [Google Scholar] [CrossRef] [PubMed]
  118. Veerasamy, R.; Xin, T.Z.; Gunasagaran, S.; Xiang, T.F.W.; Yang, E.F.C.; Jeyakumar, N.; Dhanaraj, S.A. Biosynthesis of silver nanoparticles using mangosteen leaf extract and evaluation of their antimicrobial activities. J. Saudi Chem. Soc. 2011, 15, 113–120. [Google Scholar] [CrossRef]
  119. Singh, A.; Mittal, S.; Shrivastav, R.; Dass, S.; Srivastava, J.N. Biosynthesis of silver nanoparticles using Ricinus communis L. leaf extract and its antibacterial activity. Dig. J. Nanomater. Biostruct. 2012, 7, 1157–1163. [Google Scholar]
  120. Prakash, P.; Gnanaprakasam, P.; Emmanuel, R.; Arokiyaraj, S.; Saravanan, M. Green synthesis of silver nanoparticles from leaf extract of Mimusops elengi, Linn. for enhanced antibacterial activity against multi drug resistant clinical isolates. Colloids Surf. B Biointerfaces 2013, 108, 255–259. [Google Scholar] [CrossRef] [PubMed]
  121. Garg, M.; Devi, B.; Devi, R. In vitro antibacterial activity of biosynthesized silver nanoparticles from ethyl acetate extract of Hydrocotyle sibthorpioides against multidrug resistant microbes. Asian J. Pharm. Clin. Res. 2017, 10, 263–266. [Google Scholar] [CrossRef]
  122. Li, K.; Ma, C.; Jian, T.; Sun, H.; Wang, L.; Xu, H.; Li, W.; Su, H.; Cheng, X. Making good use of the byproducts of cultivation: Green synthesis and antibacterial effects of silver nanoparticles using the leaf extract of blueberry. J. Food Sci. Technol. 2017, 54, 3569–3576. [Google Scholar] [CrossRef] [PubMed]
  123. Miri, A.; Sarani, M.; Bazaz, M.R.; Darroudi, M. Plant-mediated biosynthesis of silver nanoparticles using Prosopis farcta extract and its antibacterial properties. Spectrochim. Acta A Mol. Biomol. Spectrosc. 2015, 141, 287–291. [Google Scholar] [CrossRef] [PubMed]
  124. Das, J.; Das, M.P.; Velusamy, P. Sesbania grandiflora leaf extract mediated green synthesis of antibacterial silver nanoparticles against selected human pathogens. Spectrochim. Acta A Mol. Biomol. Spectrosc. 2013, 104, 265–270. [Google Scholar] [CrossRef] [PubMed]
  125. Lateef, A.; Azeez, M.A.; Asafa, T.B.; Yekeen, T.A.; Akinboro, A.; Oladipo, I.C.; Azeez, L.; Ajibade, S.E.; Ojo, S.A.; Gueguim-Kana, E.B.; et al. Biogenic synthesis of silver nanoparticles using a pod extract of Cola nitida: Antibacterial and antioxidant activities and application as a paint additive. J. Taibah Univ. Sci. 2016, 10, 551–562. [Google Scholar] [CrossRef]
  126. Kagithoju, S.; Godishala, V.; Nanna, R.S. Eco-friendly and green synthesis of silver nanoparticles using leaf extract of Strychnos potatorum Linn.F. and their bactericidal activities. 3 Biotech 2015, 5, 709–714. [Google Scholar] [CrossRef] [PubMed]
  127. Prabakar, K.; Sivalingam, P.; Rabeek, S.I.M.; Muthuselvam, M.; Devarajan, N.; Arjunan, A.; Karthick, R.; Suresh, M.M.; Wembonyama, J.P. Evaluation of antibacterial efficacy of phyto fabricated silver nanoparticles using Mukia scabrella (Musumusukkai) against drug resistance nosocomial gram negative bacterial pathogens. Colloids Surf. B Biointerfaces 2013, 104, 282–288. [Google Scholar] [CrossRef] [PubMed]
  128. Meva, F.E.; Ebongue, C.O.; Fannang, S.V.; Segnou, M.L.; Ntoumba, A.A.; Kedi, P.B.E.; Loudang, R.N.; Wanlao, A.Y.; Mang, E.R.; Mpondo, E.A.M. Natural substances for the synthesis of silver nanoparticles against Escherichia coli: The case of Megaphrynium macrostachyum (Marantaceae), Corchorus olitorus (Tiliaceae), Ricinodendron heudelotii (Euphorbiaceae), Gnetum bucholzianum (Gnetaceae), and Ipomoea batatas (Convolvulaceae). J. Nanomater. 2017, 2017, 6834726. [Google Scholar]
  129. Shruthi, G.; Prasad, K.S.; Vinod, T.P.; Balamurugan, V.; Shivamallu, C. Green synthesis of biologically active silver nanoparticles through a phyto-mediated approach using Areca catechu leaf extract. ChemistrySelect 2017, 2, 10354–10359. [Google Scholar] [CrossRef]
  130. Azeez, M.A.; Lateef, A.; Asafa, T.B.; Yekeen, T.A.; Akinboro, A.; Oladipo, I.C.; Gueguim-Kana, E.B.; Beukes, L.S. Biomedical applications of cocoa bean extract-mediated silver nanoparticles as antimicrobial, larvicidal and anticoagulant agents. J. Clust. Sci. 2017, 28, 149–164. [Google Scholar] [CrossRef]
  131. Lateef, A.; Azeez, M.A.; Asafa, T.B.; Yekeen, T.A.; Akinboro, A.; Oladipo, I.C.; Azeez, L.; Ojo, S.A.; Gueguim-Kana, E.B.; Beukes, L.S. Cocoa pod husk extract-mediated biosynthesis of silver nanoparticles: Its antimicrobial, antioxidant and larvicidal activities. J. Nanostruct. Chem. 2016, 6, 159–169. [Google Scholar] [CrossRef]
  132. Swamy, M.K.; Akhtar, M.S.; Mohanty, S.K.; Sinniah, U.R. Synthesis and characterization of silver nanoparticles using fruit extract of Momordica cymbalaria and assessment of their in vitro antimicrobial, antioxidant and cytotoxicity activities. Spectrochim. Acta A Mol. Biomol. Spectrosc. 2015, 151, 939–944. [Google Scholar] [CrossRef] [PubMed]
  133. Durán, N.; Durán, M.; Jesus, M.B.; Seabra, A.B.; Fávaro, W.J.; Nakazato, G. Silver nanoparticles: A new view on mechanistic aspects on antimicrobial activity. Nanomed. NBM 2016, 12, 789–799. [Google Scholar] [CrossRef] [PubMed]
  134. Li, Q.; Mahendra, S.; Lyon, D.Y.; Brunet, L.; Liga, M.V.; Li, D.; Alvarez, P.J.J. Antimicrobial nanomaterials for water disinfection and microbial control: Potential applications and implications. Water Res. 2008, 42, 4591–4602. [Google Scholar] [CrossRef] [PubMed]
  135. Manke, A.; Wang, L.; Rojanasakul, Y. Mechanisms of nanoparticle-induced oxidative stress and toxicity. BioMed Res. Int. 2013, 2013, 942916. [Google Scholar] [CrossRef] [PubMed]
  136. Siddiqi, K.S.; Husen, A.; Rao, R.A.K. A review on biosynthesis of silver nanoparticles and their biocidal properties. J. Nanobiotechnol. 2018, 16, 14. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  137. Zheng, K.; Setyawati, M.I.; Leong, D.T.; Xie, J. Antimicrobial silver nanomaterials. Coord. Chem. Rev. 2018, 357, 1–17. [Google Scholar] [CrossRef]
  138. Lok, C.; Ho, C.M.; Chen, R.; He, Q.Y.; Yu, W.Y.; Sun, H.; Tam, P.K.; Chiu, J.F.; Che, C.M. Proteomic analysis of the mode of antibacterial action of silver nanoparticles. J. Proteome Res. 2006, 5, 916–924. [Google Scholar] [CrossRef] [PubMed]
  139. Xiu, Z.; Zhang, Q.; Puppala, H.L.; Colvin, V.L.; Alvarez, P.J.J. Negligible particle-specific antibacterial activity of silver nanoparticles. Nano Lett. 2012, 12, 4271–4275. [Google Scholar] [CrossRef] [PubMed]
  140. Dibrov, P.; Dzioba, J.; Gosink, K.K.; Hase, C.C. Chemiosmotic mechanism of antimicrobial activity of Ag+ in Vibrio cholerae. Antimicrob. Agents Chemother. 2002, 46, 2668–2670. [Google Scholar] [CrossRef] [PubMed]
  141. Liau, S.Y.; Read, D.C.; Pugh, W.J.; Furr, J.R.; Russell, A.D. Interaction of silver nitrate with readily identifiable groups: Relationship to the antibacterial action of silver ions. Lett. Appl. Microbiol. 1997, 25, 279–283. [Google Scholar] [CrossRef] [PubMed]
  142. Liao, X.; Yang, F.; Li, H.; So, P.K.; Yao, Z.; Wia, W.; Sun, H. Targeting the thioredoxin reductase–thioredoxin system from Staphylococcus aureus by silver ions. Inorg. Chem. 2017, 56, 14823–14830. [Google Scholar] [CrossRef] [PubMed]
  143. Holt, K.B.; Bard, A.J. 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 2005, 44, 13214–13223. [Google Scholar] [CrossRef] [PubMed]
  144. Wen, Y.; Geitner, N.K.; Chen, R.; Ding, F.; Chen, P.; Andorfer, R.E.; Govindan, P.N.; Ke, P.C. Binding of cytoskeletal proteins with silver nanoparticles. RSC Adv. 2013, 3, 22002–22007. [Google Scholar] [CrossRef]
  145. Hong, X.; Wen, J.; Xiong, X.; Hu, Y. Shape effect on the antibacterial activity of silver nanoparticles synthesized via a microwave-assisted method. Environ. Sci. Pollut. Res. 2016, 23, 4489–4497. [Google Scholar] [CrossRef] [PubMed]
  146. Alshareef, A.; Laird, K.; Cross, R.B.M. Shape-dependent antibacterial activity of silver nanoparticles on Escherichia coli and Enterococcus faecium bacterium. Appl. Surf. Sci. 2017, 424, 310–315. [Google Scholar] [CrossRef]
  147. Pal, S.; Tak, Y.K.; Song, J.M. 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. Microb. 2007, 73, 1712–1720. [Google Scholar] [CrossRef] [PubMed]
  148. Acharya, D.; Singha, K.M.; Pandey, P.; Mohanta, B.; Rajkumari, J.; Singha, L.P. Shape dependent physical mutilation and lethal effects of silver nanoparticles on bacteria. Sci. Rep. 2018, 8, 201. [Google Scholar] [CrossRef] [PubMed]
  149. Ivask, A.; Kurvet, I.; Kasemets, K.; Blinova, I.; Aruoja, V.; Suppi, S.; Vija, H.; Kakinen, A.; Titma, T.; Heinlaan, M.; et al. Size-dependent toxicity of silver nanoparticles to bacteria, yeast, algae, crustaceans and mammalian cells in vitro. PLoS ONE 2014, 9, e102108. [Google Scholar] [CrossRef] [PubMed]
  150. Kumari, M.; Pandey, S.; Giri, V.P.; Bhattacharya, A.; Shukla, R.; Mishra, A.; Nautiyal, C.S. Tailoring shape and size of biogenic silver nanoparticles to enhance antimicrobial efficacy against MDR bacteria. Microb. Pathog. 2017, 105, 346–355. [Google Scholar] [CrossRef] [PubMed]
  151. Lu, Z.; Rong, K.; Li, J.; Yang, H.; Chen, R. Size-dependent antibacterial activities of silver nanoparticles against oral anaerobic pathogenic bacteria. J. Mater. Sci. Mater. Med. 2013, 24, 1465–1471. [Google Scholar] [CrossRef] [PubMed]
  152. Chen, M.; Yang, Z.; Wu, H.; Pan, X.; Xie, X.; Wu, C. Antimicrobial activity and the mechanism of silver. Int. J. Nanomed. 2011, 6, 2873–2877. [Google Scholar]
  153. Kora, A.J.; Sashidhar, R.B. Biogenic silver nanoparticles synthesized with rhamnogalacturonan gum: Antibacterial activity, cytotoxicity and its mode of action. Arab. J. Chem. 2018, 11, 313–323. [Google Scholar] [CrossRef]
  154. Kim, J.S.; Kuk, E.; Yu, N.K.; Kim, J.; Park, S.J.; Lee, H.J.; Kim, S.H.; Park, Y.K.; Park, Y.H.; Hwang, C.; et al. Antimicrobial effects of silver nanoparticles. Nanomed. NBM 2007, 3, 95–101. [Google Scholar] [CrossRef] [PubMed]
  155. Choi, O.; Hu, Z. Size dependent and reactive oxygen species related nanosilver toxicity to nitrifying bacteria. Environ. Sci. Technol. 2008, 42, 4583–4588. [Google Scholar] [CrossRef] [PubMed]
  156. Li, W.; Xie, X.; Shi, Q.; Zeng, H.; OU-Yang, Y.; Chen, Y. Antibacterial activity and mechanism of silver nanoparticles on Escherichia coli. Appl. Microbiol. Biotechnol. 2010, 85, 1115–1122. [Google Scholar] [CrossRef] [PubMed]
  157. Ahmad, A.; Wei, Y.; Syed, F.; Rehman, A.U.; Khan, A.; Ullah, S.; Yuan, Q. The effects of bacteria-nanoparticles interface on the antibacterial activity of green synthesized silver nanoparticles. Microb. Pathog. 2017, 102, 133–142. [Google Scholar] [CrossRef] [PubMed]
  158. Qayyum, S.; Oves, M.; Khan, A.U. Obliteration of bacterial growth and biofilm through ROS generation by facilely synthesized green silver nanoparticles. PLoS ONE 2017, 12, e0181363. [Google Scholar] [CrossRef] [PubMed]
  159. Pareek, V.; Gupta, R.; Panwar, J. Do physico-chemical properties of silver nanoparticles decide their interaction with biological media and bactericidal action? A review. Mater. Sci. Eng. C 2018, 90, 739–749. [Google Scholar] [CrossRef] [PubMed]
  160. Mchugh, G.L.; Moellering, R.C.; Hopkins, C.C.; Swartz, M.N. Salmonella typhimurium resistant to silver nitrate, chloramphenicol, and ampicillin. Lancet 1975, 1, 235–240. [Google Scholar] [CrossRef]
  161. Gupta, A.; Matsui, K.; Lo, J.; Silver, S. Molecular basis for resistance to silver cations in Salmonella. Nat. Med. 1999, 5, 183–185. [Google Scholar] [CrossRef] [PubMed]
  162. Finley, P.J.; Norton, R.; Austin, C.; Mitchell, A.; Zank, S.; Durham, P. Unprecedented silver resistance in clinically isolated Enterobacteriaceae: Major implications for burn and wound management. Antimicrob. Agents Chemother. 2015, 59, 4734–4741. [Google Scholar] [CrossRef] [PubMed]
  163. Li, X.; Nikaido, H.; Williams, K.E. Silver-resistant mutants of Escherichia coli display active efflux of Ag+ and are deficient in porins. J. Bacteriol. 1997, 179, 6127–6132. [Google Scholar] [CrossRef] [PubMed]
  164. Randall, C.P.; Gupta, A.; Jackson, N.; Busse, D.; O’Neill, A.J. Silver resistance in Gram-negative bacteria: A dissection of endogenous and exogenous mechanisms. J. Antimicrob. Chemother. 2015, 70, 1037–1046. [Google Scholar] [CrossRef] [PubMed]
  165. Su, C.; Long, F.; Zimmermann, M.T.; Rajashankar, K.R.; Jernigan, R.L.; Yu, E.W. Crystal structure of the CusBA heavy-metal efflux complex of Escherichia coli. Nature 2011, 470, 558–563. [Google Scholar] [CrossRef] [PubMed]
  166. Xue, Y.; Davis, A.V.; Balakrishnan, G.; Stasser, J.P.; Staehlin, B.M.; Focia, P.; Spiro, T.G.; Penner-Hahn, J.E.; O’Halloran, T.V. Cu(I) recognition via cation-π and methionine interactions in CusF. Nat. Chem. Biol. 2008, 4, 107–109. [Google Scholar] [CrossRef] [PubMed]
  167. Gudipaty, S.A.; McEvoy, M.M. The histidine kinase CusS senses silver ions through direct binding by its sensor domain. Biochim. Biophys. Acta 2014, 1844, 1656–1661. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  168. Franke, S.; Grass, G.; Nies, D.H. The product of the ybdE gene of the Escherichia coli chromosome is involved in detoxification of silver ions. Microbiology 2001, 147, 965–972. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  169. Panáček, A.; Kvítek, L.; Smékalová, M.; Večeřová, R.; Kolář, M.; Röderová, M.; Dyčka, F.; Šebela, M.; Prucek, R.; Tomanec, O.; et al. Bacterial resistance to silver nanoparticles and how to overcome it. Nat. Nanotechnol. 2018, 13, 65–71. [Google Scholar] [CrossRef] [PubMed]
  170. Holladay, R.; Moeller, W.; Mehta, D.; Brooks, J.H.J.; Roy, R.; Mortenson, M. Silver/Water, Silver Gels and Silver-Based Compositions; and Methods for Making and Using the Same. World Intellectual Property Organization 2006074117A2, 5 January 2005. [Google Scholar]
  171. Jinjun, L.; Qiangbai, L.; Jianchao, S. Use of Medicinal Nanomaterial Composition Dg-5 Applied to Anti-Drug Resistant Bacteria. World Intellectual Property Organization 2018010403A1, 13 July 2016. [Google Scholar]
  172. Jiachong, C.; Jixiong, Y. Manufacturing Methods and Applications of Antimicrobial Plant Fibers Having Silver Particles. U.S. Patent 20100003296, 7 January 2010. [Google Scholar]
  173. Nano Silver and Perfume Contain an Apron. Korean Patent 200384433Y1, 16 May 2005.
  174. Method for Preparing Nano-Silver Particle and Detergent Composition by Using Them. Korean Patent 100933736B1, 26 June 2008.
  175. Composite Nanometer Antibacterial Material Used for Treating Vancomycin Drug Resistant Pathogenic Bacteria. Chinese Patent 105412940A, 2 December 2015.
  176. Paknikar, K.M. Anti-Microbial Activity of Biologically Stabilized Silver Nano Particles. World Intellectual Property Organization 2005120173A2, 22 December 2005. [Google Scholar]
  177. Holladay, R.J.; Christensen, H.; Moeller, W.D. Treatment of Humans with Colloidal Silver Composition. U.S. Patent 7135195B2, 14 November 2006. [Google Scholar]
  178. Liang, D.; Lu, Z.; Yang, H.; Gao, J.; Chen, R. Novel asymmetric wettable AgNPs/chitosan wound dressing: In vitro and in vivo evaluation. ACS Appl. Mater. Interfaces 2016, 8, 3958–3968. [Google Scholar] [CrossRef] [PubMed]
  179. Yabanoglu, H.; Basaran, O.; Aydogan, C.; Azap, O.K.; Karakayali, F.; Moray, G. Assessment of the effectiveness of silver-coated dressing, chlorhexidine acetate (0.5%), citric acid (3%), and silver sulfadiazine (1%) for topical antibacterial effects against the multi-drug resistant Pseudomonas aeruginosa infecting full-skin thickness burn wounds on rats. Int. Surg. 2013, 98, 416–423. [Google Scholar] [PubMed]
  180. Huang, Y.; Li, X.; Liao, Z.; Zhang, G.; Liu, Q.; Tang, J.; Peng, Y.; Liu, X.; Luo, Q. A randomized comparative trial between Acticoat and SD-Ag in the treatment of residual burn wounds, including safety analysis. Burns 2007, 33, 161–166. [Google Scholar] [CrossRef] [PubMed]
Figure 1. Biological extracts may be prepared from any part of plant material, or via extracellular/intracellular processes using fungi and bacteria cultures. The extracts are rich in biomolecules such as sugars, proteins, nucleic acids, and metabolites that either have a stabilizing potential or reducing and stabilizing potential for the formation of silver nanoparticles.
Figure 1. Biological extracts may be prepared from any part of plant material, or via extracellular/intracellular processes using fungi and bacteria cultures. The extracts are rich in biomolecules such as sugars, proteins, nucleic acids, and metabolites that either have a stabilizing potential or reducing and stabilizing potential for the formation of silver nanoparticles.
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Figure 2. Illustration of different classes of antibiotics. Antibiotics that act as bactericidal agents, i.e., cause cell death, are shown in rectangles with orange borders; antibiotics that act as bacteriostatic agents, i.e., restrict growth and reproduction, are shown in rectangles with dashed line orange borders. Years shown in blue indicate when the antibiotic class was discovered (the first number), and when resistance was first reported (the second number). The structure and years of discovery and resistance refer to the first antibiotic from each class [35,40,41,42,43,44,45,46].
Figure 2. Illustration of different classes of antibiotics. Antibiotics that act as bactericidal agents, i.e., cause cell death, are shown in rectangles with orange borders; antibiotics that act as bacteriostatic agents, i.e., restrict growth and reproduction, are shown in rectangles with dashed line orange borders. Years shown in blue indicate when the antibiotic class was discovered (the first number), and when resistance was first reported (the second number). The structure and years of discovery and resistance refer to the first antibiotic from each class [35,40,41,42,43,44,45,46].
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Figure 3. Summary of the factors affecting the antimicrobial capacity of AgNPs and main antibacterial mechanisms. Size, shape and capping agents have a significant influence on the activity against bacterial cells, which are susceptible to nanoparticles because of a strong affinity of the metal with the cell wall and membrane, as well as due to interference in the respiratory chain and generation of reactive oxygen species (ROS).
Figure 3. Summary of the factors affecting the antimicrobial capacity of AgNPs and main antibacterial mechanisms. Size, shape and capping agents have a significant influence on the activity against bacterial cells, which are susceptible to nanoparticles because of a strong affinity of the metal with the cell wall and membrane, as well as due to interference in the respiratory chain and generation of reactive oxygen species (ROS).
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Figure 4. Silver efflux system found in Gram-negative silver-resistant bacteria. SilE is a periplasmic, histidine-rich Ag+ binding protein; SilS belongs to a two-component (SilRS) transcription regulation system; SilA, SilB, and SilC comprise a three-component chemiosmotic bacterial proton/cation antiporter.
Figure 4. Silver efflux system found in Gram-negative silver-resistant bacteria. SilE is a periplasmic, histidine-rich Ag+ binding protein; SilS belongs to a two-component (SilRS) transcription regulation system; SilA, SilB, and SilC comprise a three-component chemiosmotic bacterial proton/cation antiporter.
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Table 1. Fungi-mediated AgNPs biosynthesis and their activity against (MDRB).
Table 1. Fungi-mediated AgNPs biosynthesis and their activity against (MDRB).
FungusAgNPs Size (nm)Target MDR MicroorganismTest Type aTest Result bReference
Aspergillus flavus5–30E. coliZI15 ± 1.5 mm[14]
S. aureusZI16 ± 2 mm
M. luteusZI14 ± 1 mm
P. aeruginosaZI14 ± 1.5 mm
E. faecalisZI15 ± 1.5 mm
A. baumaniiZI15 ± 1 mm
K. pneumoniaeZI14 ± 0.6 mm
Bacillus spp.ZI15 ± 1.5 mm
Fusarium oxysporum NGD16.3–70Enterobacter sp.ZI31 mm[74]
P. aeruginosaZI20 mm
K. pneumoniaeZI19 mm
E. coliZI2 mm
Trichoderma viride5–40E. coliZI16–28 mm (*)[75]
S. typhiZI19–36 mm (*)
S. aureusZI10–19 mm (*)
M. luteusZI9–17 mm (*)
Aspergillus niger30–40S. aureusZI15 ± 0.23 mm[76]
B. cereusZI16 ± 0.32 mm
P. vulgarisZI14 ± 0.26 mm
E. coliZI14 ± 0.44 mm
V. choleraeZI13 ± 0.51 mm
Tricholoma crassum5–50E. coli (DH5 α)ZI17.5 ± 0.5 (**)[77]
A. tumifaciens (LBA4404)ZI20.0 ± 0.5 (**)
Agaricus bisporus-E. coliZI14 mm[78]
Klebsiella sp.ZI15 mm
Pseudomonas sp.ZI-
Enterobacter sp.ZI18 mm
Proteus sp.ZI20 mm
S. aureusZI17 mm
S. typhiZI22 mm
S. paratyphiZI17 mm
Aspergillus clavatus550–650 (AFM)S. aureusZI20.5 mm[79]
S. epidermidisZI19 mm
Penicilium polonicum10–15A. baumaniiMIC, MBC, ZI15.62 μg mL−1 (MIC),
31.24 μg mL−1 (MBC),
21.2 ± 0.4 mm (ZI)
[73]
Cryphonectria sp.30–70S. aureus (ATCC-25923)ZI16 ± 0.69 mm[80]
S. typhi (ATCC-51812)ZI12 ± 0.29 mm
E. coli (ATCC-39403)ZI13 ± 1.54 mm
Rhizoppus spp.27–50E. coliZI15–22 mm (***)[81]
Fusarium oxysporum77.68S. aureus (MRSA 101)MIC, MBC250 μM (MIC),
500 μM (MBC)
[70]
S. aureus (MRSA 107)MIC, MBC250 μM (MIC),
500 μM (MBC)
E. coli (ESBL 167)MIC, MBC125 μM (MIC),
125 μM (MBC)
E. coli (ESBL 169)MIC, MBC125 μM (MIC),
125 μM (MBC)
E. coli (ESBL 176)MIC, MBC125 μM (MIC),
125 μM (MBC)
E. coli (ESBL 192)MIC, MBC125 μM (MIC),
125 μM (MBC)
E. coli (KPC 131)MIC, MBC125 μM (MIC),
125 μM (MBC)
E. coli (KPC 133)MIC, MBC125 μM (MIC),
125 μM (MBC)
A. baumannii (CR 01)MIC, MBC125 μM (MIC),
125 μM (MBC)
Aspergillus flavus5–30E. coliZI15 ± 1.5 mm[14]
S. aureusZI16 ± 2 mm
M. luteusZI14 ± 1 mm
P. aeruginosaZI14 ± 1.5 mm
E. faecalisZI15 ± 1.5 mm
A. baumanniiZI15 ± 1 mm
K. pneumoniaeZI14 ± 0.6 mm
Bacillus spp.ZI15 ± 1.5 mm
Macrophomina phaseolina5–40E. coli (DH5α-MDR)ZI3.0 ± 0.2 mm (**)[72]
A. tumefaciens (LBA4404-MDR)ZI3.3 ± 0.2 mm (**)
a ZI = zone of inhibition; MIC = Minimum Inhibitory Concentration; MBC = Minimum Bactericidal Concentration.; b For tests in which more than one concentration of AgNPs was used, the best results are shown; (*) Values related to a synergistic effect with distinct antibiotics; (**) Values estimated from graphs; (***) More than one bacterial isolate was used.
Table 2. Bacteria-mediated AgNPs biosynthesis and their activity against MDRB.
Table 2. Bacteria-mediated AgNPs biosynthesis and their activity against MDRB.
BacteriaAgNPs Size (nm)Target MDR MicroorganismTest Type aTest Result bReference
Streptomyces20–70K. pneumoniae (ATCC 100603)MIC4 μg mL−1[92]
K. pneumoniaeMIC1.4 μg mL−1
E. coliMIC2 μg mL−1
CitrobacterMIC2 μg mL−1
Bacillus sp.14–42S. epidermidis strain 73 (pus)ZI15 mm[93]
S. epidermidis strain 145 (catheter tips)ZI19 mm
S. epidermidis strain 152 (blood)ZI19 mm
S. aureus (MTCC 87)ZI18 mm
S. typhiZI13 mm
S. paratyphiZI15 mm
V. cholerae (MTCC 3906)ZI18 mm
Bacillus cereus24–46E. coliMIC, ZI6.25 μg mL−1 (MIC),
16 ± 1 mm (ZI)
[94]
S. aureusMIC, ZI12.5 μg mL−1 (MIC),
14 ± 1 (ZI)
K. pneumoniaeMIC, ZI>3.12 μg mL−1 (MIC),
17 ± 1 mm (ZI)
P. aeruginosaMIC, ZI3.12 μg mL−1 (MIC),
23 ± 1 mm (ZI)
Bacillus safensis (LAU 13)5–95E. coliZI11–19 mm[95]
K. granulomatisZI11–19 mm
P. vulgarisZI11–19 mm
P. aeruginosaZI11–19 mm
S. aureusZI11–19 mm
Aeromonas sp. THG-FG1.28–16B. cereus (ATCC 14579)ZI13.5 ± 0.5 mm[88]
B. subtilis (KACC 14741)ZI13 ± 1.0 mm
S. aureus (ATCC 6538)ZI15.5 ± 0.5 mm
E. coli (ATCC 10798)ZI13 ± 0.2 mm
P. aeruginosa (ATCC 6538)ZI16 ± 0.1 mm
V. parahaemolyticus (ATCC 33844)ZI16 ± 0.1 mm
S. enterica (ATCC 13076)ZI11 ± 0.2 mm
C. albicans (KACC 30062)ZI20 ± 0.1 mm
C. tropicalis (KCTC 7909)ZI15 ± 0.5 mm
Bacillus thuringiensis15E. coliZI12 ± 1 mm (*)[96]
P. aeruginosaZI16 ± 1 mm (*)
S. aureusZI9 ± 1 mm (*)
Anabaena diololum10–50K. pneumoniae DF12SA (HQ114261)ZI36 ± 0.82 mm[97]
10–50E. coli DF39TA (HQ163793)ZI33 ± 1.63 mm
10–50S. aureus DF8TA (JN642261)ZI34 ± 0.81 mm
Streptomyces sp. GUT 2123–48E. coli (MTCC 9537)MIC, ZI14 μg mL−1 (MIC),
27.05 ± 3.20 mm (ZI)
[89]
K. pneumoniae (MTCC 109)MIC, ZI12 μg mL−1 (MIC),
28.50 ± 2.60 mm (ZI)
S. aureus (MTCC 96)MIC, ZI15 μg mL−1 (MIC),
24.25 ± 2.09 mm (ZI)
P. aeruginosa (MTCC 1688)MIC, ZI10 μg mL−1 (MIC),
10.05 ± 3.60 mm (ZI)
Bacillus megaterium80–98.56 (AFM)S. pneumoniaeZI21 mm[98]
S. typhiZI18 mm
Xanthomonas spp.5–40P. aeruginosaZI10.0 ± 1.0 mm[91]
baumanniiZI10.6 ± 0.6 mm
Sinomonas mesophila MPKL 264–50S. aureusZI12 mm[90]
Bacillus flexus12–65E. coliZI11.55 mm[99]
P. aeruginosaZI11.05 mm
S. pyogenesZI11.65 mm
subtilisZI11.55 mm
Bacillus brevis (NCIM 2533)41–68S. aureusZI19 mm[100]
S. typhiZI7.5 mm
a ZI = zone of inhibition; MIC = Minimum Inhibitory Concentration; MBC = Minimum Bactericidal Concentration; b For tests in which more than one concentration of AgNPs was used, the best results are shown; (*) Values estimated from graphs.
Table 3. Plant-mediated AgNPs biosynthesis and their activity against MDRB.
Table 3. Plant-mediated AgNPs biosynthesis and their activity against MDRB.
PlantPartAgNPs Size (nm)Target MDR MicroorganismTest Type aTest Result bReference
Oliveleaf20–25S. aureusZI2.4 ± 0.2 cm (*)[114]
P. aeruginosaZI2.4 ± 0.2 cm (*)
E. coliZI1.8 ± 0.2 cm (*)
Phyllanthus amarusWhole plant24 ± 8P. aeruginosaMIC, ZI6.25–12.5 μg mL−1 (MIC),
10 ± 0.53 to 21 ± 0.11 mm (ZI)
[115]
Corchorus capsularisleaf5–45P. aeruginosaZI17 mm[116]
S. aureusZI21 mm
Coagulase negative staphylococciZI20 mm
Tribulus terrestrisfruit16–28S. pyogensZI10 mm[117]
E. coliZI10.75 mm
P. aeruginosaZI9.25 mm
B. subtilisZI9.25 mm
S. aureusZI9.75 mm
Garcinia mangostanaleaf35E. coliZI15 mm[118]
S. aureusZI20 mm
Ricinus communisleaf29.18 (X-ray diffraction)B. fusiformisZI2.90 cm[119]
E.coliZI2.89 cm
Caesalpinia coriarialeaf40–52E. coliZI12.0 ± 0.50 mm[109]
P. aeruginosaZI18.3 ± 0.80 mm
K. pneumoniaZI14.6 ± 1.20 mm
S. aureusZI10.3 ± 1.20 mm
78–98E. coliZI9.6 ± 0.80 mm[109]
P. aeruginosaZI18.3 ± 1.20 mm
K. pneumoniaZI13.3 ± 0.30 mm
S. aureusZI11.0 ± 0.00 mm
Mimusops elengileaf55–83K. pneumoniaeZI18 mm[120]
S. aureusZI10 mm
M. luteusZI11 mm
Ocimum gratissimumleaf16 ± 2E. coli (MC-2)MIC, MBC, ZI4 μg mL−1 (MIC),
8 μg mL−1 (MBC),
12 ± 0.6 mm (ZI)
[112]
S. aureus (MMC-20)MIC, MBC, ZI8 μg mL−1 (MIC),
16 μg mL−1 (MBC),
16 ± 1.0 mm (ZI)
Hydrocotyle sibthorpioidesWhole plant13.37 ± 10K. pneumoniaZI3.0 ± 0.17 mm[121]
P. aeruginosaZI2.7 ± 0.32 mm
S. aureusZI3.6 ± 0.57 mm
Vaccinium corymbosumleaf10–30E. coli (ATCC 25922)MIC, MBC, ZI11.22 ± 0.29 mm[122]
S. aureus (ATCC 25923)MIC, MBC, ZI13.1 ± 1.1 mm
P. aeruginosa (ATCC 27853)MIC, MBC, ZI11.6 ± 0.32 mm
B. subtilis (ATCC 21332)MIC, MBC, ZI12.4 ± 0.40 mm
Prosopis farctaleaf10.8 ± 3.54S. aureus (PTCC 1431)ZI9.5 mm[123]
B. subtilis (PTCC 1420)ZI9 mm
E. coli (PTCC 1399)ZI9.5 mm
P. aeruginosa (PTCC 1074)ZI9.5 mm
Sesbania gradifloraleaf10–25S. entericaZI15.67 ± 0.09 mm[124]
S. aureusZI10.54 ± 0.23 mm
Solanum nigrumleaf20K. pneumoniaeZI21.5 mm[110]
P. aeruginosaZI21.3 mm
S. epidermidisZI19.6 mm
E. coliZI15.3 mm
P. vulgarisZI13.3 mm
S. aureusZI9.6 mm
Cissus quadrangularisleaf15–23 (**)S. pyogensMIC, ZI4 μg mL−1 (MIC),
7.77 ± 0.25 mm (ZI)
[113]
S. aureusMIC, ZI3 μg mL−1 (MIC),
8.83 ± 0.26 mm (ZI)
E. coliMIC, ZI5 μg mL−1 (MIC),
7.9 ± 0.31 mm (ZI)
P. vulgarisMIC, ZI7 μg mL−1 (MIC),
8.4 ± 0.40 mm (ZI)
Cola nitidapod12–80E. coliZI19 ± 0.9 mm[125]
K. granulomatisZI11 ± 0.8 mm
P. aeruginosaZI28 ± 0.1 mm
Strychnos potatorumleaf28S. aureusZI8 mm[126]
K. pneumoniaeZI10 mm
Alstonia scholarisleaf80E. coliZI10.0 ± 2.8 mm[111]
P. aeruginosaZI8.0 ± 1.4 mm
K. pneumoniaeZI11.0 ± 1.0 mm
S. aureusZI10.0 ± 3.0 mm
P. vulgarisZI8.3 ± 0.6 mm
S. epidermidisZI10.6 ± 1.2 mm
Andrographis paniculataleaf70E. coliZI8.0 ± 1.4 mm[111]
P. aeruginosaZI6.7 ± 0.7 mm
K. pneumoniaeZI9.3 ± 0.6 mm
S. aureusZI8.0 ± 1.0 mm
P. vulgarisZI8.3 ± 0.6 mm
S. epidermidisZI9.0 ± 1.0 mm
Aegle marmelosleaf70E. coliZI11.0 ± 2.8 mm[111]
P. aeruginosaZI9.0 ± 1.4 mm
K. pneumoniaeZI9.3 ± 1.6 mm
S. aureusZI9.7 ± 1.5 mm
P. vulgarisZI9.7 ± 0.6 mm
S. epidermidisZI8.0 ± 1.0 mm
Centella asiaticaleaf90E. coliZI12.7 ± 0.7 mm[111]
P. aeruginosaZI8.0 ± 1.4 mm
K. pneumoniaeZI12.0 ± 1.0 mm
S. aureusZI13.0 ± 2.0 mm
P. vulgarisZI9.7 ± 0.6 mm
S. epidermidisZI14.0 ± 1.0 mm
Eclipta prostrataleaf70E. coliZI10.0 ± 4.0 mm[111]
P. aeruginosaZI8.3 ± 2.5 mm
K. pneumoniaeZI10.0 ± 5.2 mm
S. aureusZI12.6 ± 4.9 mm
P. vulgarisZI6.6 ± 0.5 mm
S. epidermidisZI8.0 ± 0.0 mm
Moringa oleiferaleaf50E. coliZI7.7 ± 0.6 mm[111]
P. aeruginosaZI8.0 ± 1.7 mm
K. pneumoniaeZI7.0 ± 1.0 mm
S. aureusZI9.0 ± 2.6 mm
P. vulgarisZI7.0 ± 2.0 mm
S. epidermidisZI7.0 ± 0.0 mm
Thespesia populneabark70E. coliZI9.0 ± 1.7 mm[111]
P. aeruginosaZI10.3 ± 2.1 mm
K. pneumoniaeZI11.3 ± 1.2 mm
S. aureusZI9.3 ± 2.4 mm
P. vulgarisZI8.6 ± 1.2 mm
S. epidermidisZI8.6 ± 0.7 mm
Terminalia arjunabark70E. coliZI8.0 ± 0.7 mm[111]
P. aeruginosaZI9.0 ± 2.0 mm
K. pneumoniaeZI14.0 ± 1.0 mm
S. aureusZI12.7 ± 1.1 mm
P. vulgarisZI8.3 ± 0.6 mm
S. epidermidisZI9.0 ± 2.0 mm
Plumbago zeylanicaRoot bark90E. coliZI8.0 ± 1.4 mm[111]
P. aeruginosaZI14.7 ± 0.7 mm
K. pneumoniaeZI8.3 ± 0.8 mm
S. aureusZI7.7 ± 0.6 mm
P. vulgarisZI8.3 ± 0.6 mm
S. epidermidisZI8.0 ± 1.0 mm
Semecarpus anacardiumnuts60E. coliZI10.0 ± 2.0 mm[111]
P. aeruginosaZI9.3 ± 1.5 mm
K. pneumoniaeZI10.0 ± 1.0 mm
S. aureusZI7.7 ± 1.1 mm
P. vulgarisZI8.3 ± 0.6 mm
S. epidermidisZI9.3 ± 1.5 mm
Mukia scabrellaleaf18–21Acinetobacter sp.ZI22 mm[127]
K. pneumoniaeZI19 mm
P. aeruginosaZI20 mm
Phyllanthus amarusWhole plant24 ± 8P. aeruginosa (***)MIC, ZI6.25–12.5 μg mL−1 (MIC),
21 ± 0.11 mm (ZI)
[115]
Ricinodendron heudelottiSeed kernel89.0E. coliMIC, MBC1.68 μg mL−1 (MIC),
6.75 μg mL−1 (MBC)
[128]
Gnetum bucholzianumleaf67.4E. coliMIC, MBC1.687 μg mL−1 (MIC),
1.687 μg mL−1 (MBC)
[129]
Megaphrynium macrostachyumleaf33.7 (Ag), 44.2 (AgCl)E. coliMIC, MBC0.515 μg mL−1 (MIC),
4.12 μg mL−1 (MBC)
[129]
Corchorus olitorusleaf30.0 (nm), 37.9 (AgCl)E. coliMIC, MBC8.25 μg mL−1 (MIC),
16.5 μg mL−1 (MBC)
[129]
Ipomoea batatasleaf67.3 (Ag), 37.9 (AgCl)E. coliMIC, MBC5.3 μg mL−1 (MIC),
5.3 μg mL−1 (MBC)
[129]
Areca catechuleaf22–40E. coliZI20 mm[129]
P. aeruginosaZI24 mm
S. typhiZI19 mm
P. vulgarisZI23 mm
K. pneumoniaeZI26 mm
Cocoabean8.96–54.22S. aureusZI12 mm (*)[130]
K. pneumoniae (wound)ZI12 mm (*)
K. pneumoniae (urine)ZI13 mm (*)
E. coliZI14 mm (*)
CocoaPod husk4–32K. pneumoniaeZI10–14 mm[131]
E. coliZI10–14 mm
Phomis bracteosaWhole plant22.41E. coli (ATCC 15224)ZI13.2 ± 0.12[108]
S. aureus (ATCC 6538)ZI11.1 ± 0.10
K. pneumoniae (ATCC 4619)ZI10.3 ± 0.11
Momordica cymbalariafruit15.5E. coliZI24.0 ± 1.0[132]
M. luteusZI20.0 ± 1.4
B. cereusZI22.0 ± 1.0
K. pneumoniaeZI26.0 ± 1.4
S. pneumoniaeZI26.0 ± 1.7
Astragalus membranaceusroot65.08S. aureus (MRSA)MIC, ZI0.063 mg mL−1 (MIC),
12.83 ± 1.04 mm (ZI)
[107]
S. epidermidis (MRSE)MIC, ZI0.063 mg mL−1 (MIC),
12.33 ± 0.29 mm (ZI)
P. aeruginosaMIC, ZI0.032 mg mL−1 (MIC),
15.17 ± 0.76 mm (ZI)
E. coliMIC, ZI0.032 mg mL−1 (MIC),
14.67 ± 0.76 mm (ZI)
a ZI = zone of inhibition; MIC = Minimum Inhibitory Concentration; MBC = Minimum Bactericidal Concentration; b For tests in which more than one concentration of AgNPs was used, the best results are shown; (*) Values estimated from graphs; (**) Silver chloride nanoparticles; (***) 15 strains were tested
Table 4. Patents of AgNPs-based products tested against resistant bacterial strains.
Table 4. Patents of AgNPs-based products tested against resistant bacterial strains.
Patent NumberApplicationResistant BacteriaReference
WO2006074117A2HydrogelE. cloacae, K. pneumoniae, E. coli, P. aeruginosa, A. Acinetobacter[170]
WO2018010403A1PharmaceuticalsE. cloacae, K. pneumoniae, E. coli, P. aeruginosa, A. Acinetobacter[171]
US20100003296A1TextilesMethicillin-resistant S. aureus (MRSA)[172]
KR200384433Y1Apron, perfumeMethicillin-resistant S. aureus (MRSA)[173]
KR100933736B1Detergent additiveE. coli[174]
CN105412940AGeneralVancomycin-resistant Enterococcus faecalis[175]
WO2005120173A2GeneralP. aeruginosa[176]
US7135195B2GeneralMethicillin-resistant S. aureus (MRSA)[177]

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Barros, C.H.N.; Fulaz, S.; Stanisic, D.; Tasic, L. Biogenic Nanosilver against Multidrug-Resistant Bacteria (MDRB). Antibiotics 2018, 7, 69. https://0-doi-org.brum.beds.ac.uk/10.3390/antibiotics7030069

AMA Style

Barros CHN, Fulaz S, Stanisic D, Tasic L. Biogenic Nanosilver against Multidrug-Resistant Bacteria (MDRB). Antibiotics. 2018; 7(3):69. https://0-doi-org.brum.beds.ac.uk/10.3390/antibiotics7030069

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Barros, Caio H. N., Stephanie Fulaz, Danijela Stanisic, and Ljubica Tasic. 2018. "Biogenic Nanosilver against Multidrug-Resistant Bacteria (MDRB)" Antibiotics 7, no. 3: 69. https://0-doi-org.brum.beds.ac.uk/10.3390/antibiotics7030069

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