Characteristics of Metallic Nanoparticles (Especially Silver Nanoparticles) as Anti-Biofilm Agents

Li, Hongze; Yang, Zhihe; Khan, Sadaf Aiman; Walsh, Laurence J.; Seneviratne, Chaminda Jayampath; Ziora, Zyta M.

doi:10.3390/antibiotics13090819

Open AccessReview

Characteristics of Metallic Nanoparticles (Especially Silver Nanoparticles) as Anti-Biofilm Agents

by

Hongze Li

¹,

Zhihe Yang

^1,2

,

Sadaf Aiman Khan

^2,3,4,

Laurence J. Walsh

²

,

Chaminda Jayampath Seneviratne

² and

Zyta M. Ziora

^3,4,*

¹

School of Chemistry and Molecular Biosciences, The University of Queensland, St. Lucia, QLD 4072, Australia

²

Oral Health Centre, School of Dentistry, The University of Queensland, Herston, QLD 4006, Australia

³

Institute for Molecular Bioscience, The University of Queensland, St. Lucia, QLD 4072, Australia

⁴

Indian Institute of Technology (IITD) Delhi, New Delhi 110016, India

^*

Author to whom correspondence should be addressed.

Antibiotics 2024, 13(9), 819; https://doi.org/10.3390/antibiotics13090819

Submission received: 4 July 2024 / Revised: 15 August 2024 / Accepted: 20 August 2024 / Published: 28 August 2024

(This article belongs to the Special Issue Antimicrobial Activities and Medicinal Applications of Metal Nanoparticles)

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Abstract

:

Biofilm-associated infections account for a large proportion of chronic diseases and pose a major health challenge. Metal nanoparticles offer a new way to address this problem, by impairing microbial growth and biofilm formation and by causing degradation of existing biofilms. This review of metal nanoparticles with antimicrobial actions included an analysis of 20 years of journal papers and patent applications, highlighting the progress over that time. A network analysis of relevant publications showed a major focus on the eradication of single-species biofilms formed under laboratory conditions, while a bibliometric analysis showed growing interest in combining different types of metal nanoparticles with one another or with antibiotics. The analysis of patent applications showed considerable growth over time, but with relatively few patents progressing to be granted. Overall, this profile shows that intense interest in metal nanoparticles as anti-biofilm agents is progressing beyond the confines of simple laboratory biofilm models and coming closer to clinical application. Looking to the future, metal nanoparticles may provide a sustainable approach to combatting biofilms of drug-resistant bacteria.

Keywords:

antimicrobial agents; biofilm; metallic nanoparticles; bimetallic nanoparticles; silver nanoparticles

Graphical Abstract

1. Introduction

A common treatment for bacterial infections is the administration of an antibiotic. However, once the bacteria have organized themselves into a biofilm, the altered metabolic state within the biofilm reduces the effectiveness of antibiotics and makes the emergence or resistance more likely. Additionally, the extracellular polymeric substances (EPSs) of the biofilm limit the penetration of large molecules such as antibiotics and certain biocides, making those ineffective. Given these challenges, there is interest in using metallic nanoparticles with antimicrobial properties to eradicate biofilms or prevent them from forming. The high surface-area-to-volume ratio and ability to penetrate into microbial biofilms make metal nanoparticles attractive as possible therapeutic agents.

According to the US Centers for Disease Control, up to two-thirds of common bacterial infections involve multiple species [1], with more than one type of pathogenic bacteria cooperating with others to form a biofilm [1,2]. In chronic bacterial infections, biofilms may be found in up to 80% of cases [3]. In the biofilm state, the emergence of antimicrobial resistance (AMR) is more likely, making antibiotics and traditional biocides ineffective [4].

Biofilm Formation and the Interactions between Biofilm Components and Antimicrobial Agents

In the biofilm community, bacteria are embedded in EPSs [5], which is composed of polysaccharides, glycopeptides, DNA, lipids, and proteins. Voids in the EPSs serve as channels for the movement of water, nutrients, and waste products [6]. The EPSs protect bacteria from various physical, chemical, biological, and environmental factors, including extremes of temperature and pH, and host immune responses [7]. As a result, biofilms are not easily disrupted.

Biofilms form from planktonic, autotrophic, and heterotrophic bacteria and archaea, typically with more heterotrophic bacteria than autotrophic bacteria [8]. Once individual microbes attach to a surface, they transition from the free-floating state and produce EPSs to anchor them to the surface and to provide protection from the environment [9] (Figure 1). Adhesion and colonization are then followed by maturation [6]. Bacteria transition from reversible adhesion to the surface using van der Waals forces [10] to form stable anchorage, using adhesins and fimbriae. The growth of the biofilm is coordinated through quorum sensing (QS) [11]. From a mature biofilm, planktonic cells can be dispersed into the local environment, to then form biofilms in new locations [7].

Inter-species interactions are essential within the biofilm for its overall persistence and for the survival of its inhabitants, and the term “Sociomicrobiology” coined in 2005 captures this cooperation between inhabitants [12], which may include QS, signaling molecule transmission, and horizontal gene transfer. Cooperation is beneficial for interacting bacteria, providing the foundation for synergy [13].

Traditional methods used to treat bacterial and fungal biofilms use physical, chemical, or biological agents. Physical agents include ultraviolet light and ionizing radiation, both of which are dangerous for humans and animals. Biocides as chemical agents can pose a risk to health from damage to healthy host tissues [14], while antibiotics can give rise to allergies and systemic toxicity. These concerns have sparked interest in metal nanoparticles with antimicrobial actions [15].

Nanoparticles have a size between 1 and 100 nanometers. Their small size gives them a large surface area and enhanced chemical reactivity [16]. For antimicrobial actions, metallic nanoparticles of silver, gold, copper, iron, and zinc, with a size of 100 nm or less [17], may be suitable for antimicrobial applications [11] and for other health-related applications such as drug delivery [18].

Metal nanoparticles can interact with the EPSs of a biofilm. Metal nanoparticles are usually positively charged, while the polymer molecules of EPSs carry mostly negative charges [6]. As a result, the metal nanoparticles are attracted to the biofilm and can penetrate into the biofilm and attach to the EPSs. Once bound to bacteria or fungi, they cause disintegration of the biofilm matrix [6]. Eradication of existing biofilms will be referred to in this paper as anti-biofilm activity.

This review provides an overview of antimicrobial metallic nanoparticles and their actions on planktonic bacterial cells and on biofilms. This is followed by an analysis of recent publications and an assessment of recent patents.

2. Recent Advances in Nanometal Research

Key metallic nanoparticles of interest are silver, gold, copper, iron, and zinc, with the most extensive literature on silver nanoparticles as antibacterial agents.

2.1. Types of Metallic Nanoparticles and Their Efficacy

Nanoparticles of silver, copper, gold, zinc, titanium, and nickel exert antibacterial actions on both Gram-positive and Gram-negative bacteria [19,20,21,22,23]. They can disrupt bacterial cell walls through oxidative and nitrite stress and impair bacterial metabolism by inhibiting enzyme activity, gene expression, and ATP synthesis [15].

2.1.1. Silver Nanoparticles

Silver nanoparticles (AgNPs) have remarkable antibacterial properties. They inhibit the formation of biofilms [24], including that for Escherichia coli, Staphylococcus aureus, Enterococcus planus, and Pseudomonas aeruginosa [25]. Since AgNPs penetrate into the biofilm matrix, this makes them candidates for carrying other actives (such as fungicides). They can also be used in combination with antibiotics, such as erythromycin, penicillin, or streptomycin [26].

Similar antibacterial activity to AgNPs is shown by silver oxide nanoparticles (AgONPs); however. a common disadvantage of metal oxide nanoparticles from silver, zinc and copper is their degradation by sunlight [27].

2.1.2. Gold Nanoparticles

Gold nanoparticles (AuNPs) penetrate bacterial biofilms, impair metabolic activities of bacteria, and alter bacterial cell membranes [6]. They inhibit the production of EPSs. This effect contributes to the eradication of biofilms of P. aeruginosa [6], E. coli [28], Pseudomonas putidis, and Aeromonas hydrophila. The high price of gold makes these nanoparticles too expensive to be a first-choice antimicrobial agent [6].

2.1.3. Copper Nanoparticles

Copper nanoparticles (CuNPs) are less expensive than silver or gold and have high potency as antimicrobial agents. They release positively charged copper ions (Cu²⁺) that bind to negatively charged carboxyl groups on the lipoproteins of bacterial cell membranes. The resulting increased permeability allows Cu²⁺ ions to enter bacterial cells [27], where they bind to large molecules containing sulfhydryl and phosphate residues, affecting the structure of proteins and DNA, respectively. Normal biochemical activities are impaired, leading to cell death [27]. Since copper is an essential element and is present in many enzymes in the human body, using CuNPs could destabilize normal physiological enzymatic activity. This concern limits the application of CuNPs in humans.

2.1.4. Zinc Nanoparticles

Zinc oxide nanoparticles (ZnONPs) strongly inhibit the growth of both Gram-positive and Gram-negative bacteria [27], due to the release of Zn²⁺ ions. ZnONPs can prevent biofilm formation through released Zn²⁺ ions as well as by generating reactive oxygen species (ROS), which are toxic for bacteria.

2.1.5. Other Metallic Nanoparticles

Other metal nanoparticles of interest include iron and manganese. These have demonstrated promising effects against Helicobacter pylori and against the fungal organism Candida albicans [15].

2.2. Combinations of Metal Nanoparticles with Other Agents

Combining antibiotics with metallic nanoparticles is a topic of emerging interest. As antibiotics act on different biochemical pathways, not all antibiotics can work synergistically with metal nanoparticles. Combining AgNPs with visible blue light can enhance their antibacterial activity [29,30], and extending this to AgNPs combined with blue light and an antibiotic (amoxicillin) may further increase antimicrobial activity. This approach has been used against methicillin-resistant Staphylococcus aureus [29]. However, it remains to be determined whether this combination approach could still lead to the emergence of resistance to the antibiotic [31].

Another approach is to combine two or three antimicrobial metals together, such as silver with iron. Ag-Fe bimetallic nanoparticles interact with the thiol side chain in cysteine, changing the primary structure of proteins, increasing the permeability of bacterial cell walls, and causing bacterial death. At the same time, Ag⁺ ions released from the nanoparticles into the cytoplasm induce oxidative stress and damage DNA [32]. Synergistic effects may also occur in other bimetallic and trimetallic nanoparticles.

A summary of the literature on metal nanoparticles is provided in Table 1. This shows antibacterial and antifungal actions, as well as anti-biofilm activity (i.e., destruction of existing biofilms).

Of the various types of metal nanoparticles, AgNPs are amongst the most potent antimicrobial agents, both in terms of antibacterial actions on planktonic bacterial cultures and the prevention of biofilm formation, with the lowest MIC (0.06–20 μg/mL). Other non-silver nanoparticles are less active.

Most reported metallic nanoparticles have sizes below 100 nm, especially in the range of less than 50 nm, which is smaller than most peptides [72]. As summarized in Table 1, most metallic nanoparticles were synthesized by chemical methods, including green synthesis using plant extracts.

2.3. Biofilm Inhibition by Metallic Nanoparticles

As shown in Table 1, metallic nanoparticles can impair the growth of bacteria and fungi and the formation of biofilms. They can also cause the destruction of existing biofilms, as an anti-biofilm action. These antimicrobial functions are influenced by nanoparticle type, shape, and size, since these influence their ability to create stress on cell membranes and generate ROS [73,74]. As already noted, metallic nanoparticles also release metal ions, which in turn can impair the functions of various organelles in bacteria. Mitochondrial dysfunction reduces ATP levels, while ribosome dysfunction can lead to enzyme inactivation and protein denaturation (Figure 2) [75].

2.4. Methods for the Synthesis of Silver Nanoparticles

Since AgNPs are currently the most extensively explored type of metal nanoparticle for treating biofilms or preventing their formation, they serve as an exemplar for other metallic nanoparticles. Such particles can be synthesized or fabricated using a range of approaches, which can be divided into “top-down” or “bottom-up” (Figure 3) [76]. In the former method, large particles are reduced in size to particles in the nanoscale range. The second method, also known as the self-assembly method, involves forming nanoparticles from atoms or ions of the metal [77,78]. This can be conducted in a chemical reaction in a laboratory vessel or inside a plant or microorganism. Methods using extracts of plants are becoming popular for “green synthesis” since they may use waste products.

Methods for Synthesis of AgNPs

A.: Chemical methods

In bottom-up chemical synthesis methods, precursors (e.g., silver ions) are transformed using reducing agents [79]. The precursor material (usually silver nitrate) is relatively expensive. The characteristics of the AgNPs that are produced vary according to the starting materials that are selected (precursor, reducing agent, solvent, and stabilizer or end-sealer) [76] and their concentrations, as well as the temperature [80]. Stabilizers or capping agents are usually included to ensure the stability of the AgNPs. Attention must also be paid to by-products that are generated by the synthesis reaction [81]. These issues have driven interest in synthesis methods that are simpler and less expensive and that are still capable of producing AgNPs of a suitable size and that have high stability [82].

B.: Physical methods

These are top-down methods and include using heat [83], plasma [84], electromagnetic radiation [85], arc discharge, and lithography [86]. Physical methods are considered labor-intensive and costly.

C.: Biological methods including green synthesis

As shown in Table 1, a range of methods using plant extracts and microorganisms have been used to convert silver ions into AgNPs. These methods do not require complex equipment and are considered to be more environmentally friendly and lower in cost than physical or chemical methods [87,88,89]. The use of green synthesis methods to prepare metal nanoparticles is an emerging trend in nanotechnology [90].

2.5. Biosafety of AgNPs When Applied onto the Human Body

Unlike zinc, iron, copper, and cobalt, which are essential trace elements in the human body, silver is not an essential component of the human diet and does not play a role in normal human physiological processes. Ingestion of modest amounts of ionic silver can lead to silver accumulation in the human body. For example, a dose of 4.1 g of silver arsphenamine (0.6 g silver) can cause visible discoloration of the skin, known as argyria [91], due to accumulation of silver in the skin [92]. Once ingested, silver may also reach tissues other than the skin [93], including the kidneys and the respiratory system [93], the gastrointestinal system [93,94], the female genitourinary system [95], and the brain [94].

AgNPs applied topically to the skin may penetrate through normal intact tissues. For example, AgNPs smaller than 10 nanometers can pass through the pores of the stratum corneum easily, while AgNPs around 7–20 nm in size can only penetrate sweat glands and at hair follicle sebaceous glands. AgNPs of 20–200 nm tend to stay at the opening of hair follicles and tend not to penetrate the skin [93].

Adverse effects from prolonged exposure to silver are dose-related [94]. Ingestion of AgNPs and ionic silver can lead to liver and kidney damage. The toxicity of AgNPs is influenced by particle size, particle shape, and the presence of a capping or end-sealing agent [92]. Oral toxicity tests using adult male rats have shown that ingested AgNPs can alter the gut microbiome [96], which could have downstream health impacts.

Retained silver in the human body following its ingestion can cause issues, with a notable example being from particles in renal glomeruli [97]. The most clinically noticeable effects are those seen in the skin (Figure 4); however, the accumulation of AgNPs in anyone site of the body is a concern in terms of toxicity [98]. Despite occasional reports of argyria, most studies have concluded that silver does not cause significant injuries that could lead to death [92].

2.6. Analysis of the Literature from 2004 to 2024

An analysis of 20 years of the literature on metallic nanoparticles for antimicrobial treatment was undertaken following the PRISMA model. Searches were made on ScienceDirect, Scopus, and Web of Science databases (Figure 5). After removing duplicates and irrelevant or incomplete reports, this led to 35 publications over the period which were highly related to the topic.

Several trends in publications on metallic nanoparticles are evident over 20 years. There was a steady increase each year in papers on monometallic and bimetallic nanoparticles, with more sharply rising interest in the latter from 2019 onwards (Figure 6).

A patent search for metallic nanoparticles used for anti-biofilm actions was made using the Espacenet patent database for the period of 2003 to 2023 (Figure 7). The number of patent family applications per year rose over the period, with the cumulative count reaching over 3000 by the year 2023. This shows sustained activity in developing and protecting intellectual property around the use of metallic nanoparticles as antimicrobial agents.

An analysis of the inventor country or origin for patent families is shown in Figure 8. Major areas were the US, the EU, and China. A large number of patents (over 2000) had reached the international phase (WO/World Intellectual Property Organization).

Figure 9 presents a summary of patent applications (“reports”) and granted patents over the 20-year period of interest, for metallic nanoparticles used for antimicrobial treatments. This shows strong growth in patent applications, with a relatively steady number of granted patents each year over the most recent decade.

A further approach was to use VOS Viewer network visualization software (version 1.6.20) to identify the bibliometric network for the 35 included papers from the PRISMA screening process. The first analysis was for silver nanoparticles (Figure 10). Two colors were used to denote clusters. Red represents key words around AgNP properties, such as physicochemical characterization and synthesis, while blue represents performance aspects relevant to safety and effectiveness, such as antimicrobial potency, cytotoxicity, and metabolism.

A parallel visualization was prepared for zinc-containing nanoparticles (Figure 11), following the same color coding.

The third visualization was prepared for copper-containing nanoparticles (Figure 12).

The final visualization was prepared for gold nanoparticles (Figure 13).

Looking across the networks, the busiest networking visualization is for silver-containing nanoparticles, which reflects the more extensive literature on this topic when compared to other metallic nanoparticles.

A common theme across all the network analyses was that assessments of the antibacterial activity of metal nanoparticles were mostly confined to in vitro studies, especially using single-species biofilm models. This reinforces the need for more complex assessments including complex biofilms in the laboratory, followed by appropriate animal studies and human clinical trials.

3. Conclusions and Future Directions

Potential candidates for eradicating biofilms, and preventing their development, include nanoparticles of silver, gold, copper, iron, manganese, nickel, and zinc, and their oxides, used singly or in various combinations. Of these, AgNPs have been the most extensively investigated and appear to have the greatest potency as anti-biofilm agents. Metal nanoparticles are a promising way to prevent the growth of bacteria and fungi, and their formation of biofilms. In addition, metal nanoparticles exhibit useful anti-biofilm actions that lead to the eradication of established biofilms.

More attention should be directed to exploring how well metal nanoparticles penetrate into biofilms of different types and whether they provide any long-term influence on biofilm characteristics, such as through the slow generation of metal ions over long periods of time. Likewise, more exploration into how metal nanoparticles interact with quorum-sensing mechanisms is needed.

Multiple methods exist for synthesizing metal nanoparticles, and the choice of synthesis parameters determined key properties of nanoparticles such as their size and shape. Green synthesis methods offer low cost and simplicity and are used widely. Nanoparticle characteristics can be tuned to optimize antimicrobial actions, whilst maximizing biocompatibility and minimizing toxicity.

Within a biofilm, metal nanoparticles can interact with microorganisms as well as with EPSs. It is possible to combine metal nanoparticles with one another, or with antibiotics, to increase their effects on established biofilms. A review of two decades of literature showed growing interest in bimetallic nanoparticles.

The question of whether metal nanoparticles avoid altogether the problems of resistance requires further study, especially since some nanoparticles are known to bind to bacterial DNA [6], as well as to bacterial cell membranes. The extent to which the same nanoparticles can enter human cells and influence human DNA also requires close examination [15].

A network analysis of publications showed that most research was conducted in laboratory settings using single-species biofilms. The actions of metal nanoparticles as anti-biofilm agents must be tested with more complex biofilms in the laboratory setting and then in animal models and in human clinical trials. In the latter, issues with AgNPs could arise if these are in prolonged contact for sufficient time for the particles to penetrate into the body. Hence, there is a need for careful evaluation of their effects on human health.

The analysis of patent applications and granted patents shows strong interest internationally in extending knowledge regarding metal nanoparticles as antimicrobial agents. There is strong interest in targeted therapies that combine metal nanoparticles with antibiotics to combat drug-resistant infections [92]. This drive to enhance effectiveness must be accompanied by careful exploration of safety aspects, especially mucosal surface absorption and the accumulation of metal nanoparticles in organs, as part of the studies of the safety of using metal nanoparticles as therapeutic agents [15]. An emphasis on establishing comprehensive data on safety aspects is essential before considering their clinical application in human health care.

Author Contributions

Conceptualization, H.L., Z.Y. and Z.M.Z.; methodology and software, Z.Y. and S.A.K.; validation and formal analysis, Z.Y. and S.A.K.; resources, Z.Y. and S.A.K.; writing—original draft preparation, H.L., Z.Y. and Z.M.Z.; writing—review and editing, Z.M.Z., C.J.S. and L.J.W.; visualization, Z.Y. and S.A.K.; supervision, Z.M.Z. and C.J.S. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Acknowledgments

S.A.K. was supported by a scholarship from the UQ-IITD Academy.

Conflicts of Interest

The authors declare no conflicts of interest.

References

Del Pozo, J.; Rouse, M.; Patel, R. Bioelectric effect and bacterial biofilms. A systematic review. Int. J. Artif. Organs 2008, 31, 786–795. [Google Scholar] [CrossRef] [PubMed]
Lazar, V. Quorum sensing in biofilms—How to destroy the bacterial citadels or their cohesion/power? Anaerobe 2011, 17, 280–285. [Google Scholar] [CrossRef] [PubMed]
Madalina Mihai, M.; Maria Holban, A.; Giurcaneanu, C.; Gabriela Popa, L.; Mihaela Oanea, R.; Lazar, V.; Carmen Chifiriuc, M.; Popa, M.; Ioan Popa, M. Microbial biofilms: Impact on the pathogenesis of periodontitis, cystic fibrosis, chronic wounds and medical device-related infections. Curr. Top. Med. Chem. 2015, 15, 1552–1576. [Google Scholar] [CrossRef] [PubMed]
Rajput, N. Methods of preparation of nanoparticles-a review. Int. J. Adv. Eng. Technol. 2015, 7, 1806. [Google Scholar]
Wang, L.; Hu, C.; Shao, L. The antimicrobial activity of nanoparticles: Present situation and prospects for the future. Int. J. Nanomed. 2017, 12, 1227–1249. [Google Scholar] [CrossRef]
Mukherjee, D.; Sil, M.; Goswami, A.; Lahiri, D.; Nag, M. Effectiveness of metal and metal oxide nanoparticles against bacterial biofilms: Perspectives and limitations. J. Basic Microbiol. 2023, 63, 971–985. [Google Scholar] [CrossRef]
Li, B.; Webster, T.J. Bacteria antibiotic resistance: New challenges and opportunities for implant-associated orthopedic infections. J. Orthop. Res. 2018, 36, 22–32. [Google Scholar] [CrossRef]
Flemming, H.-C.; Wuertz, S. Bacteria and archaea on Earth and their abundance in biofilms. Nat. Rev. Microbiol. 2019, 17, 247–260. [Google Scholar] [CrossRef]
Alotaibi, G.F.; Bukhari, M.A. Factors influencing bacterial biofilm formation and development. Am. J. Biomed. Sci. Res. 2021, 12, 617–626. [Google Scholar] [CrossRef]
Hermansson, M. The DLVO theory in microbial adhesion. Colloids Surf. B Biointerfaces 1999, 14, 105–119. [Google Scholar] [CrossRef]
Kumar, L.; Bisen, M.; Harjai, K.; Chhibber, S.; Azizov, S.; Lalhlenmawia, H.; Kumar, D. Advances in Nanotechnology for Biofilm Inhibition. ACS Omega 2023, 8, 21391–21409. [Google Scholar] [CrossRef]
Parsek, M.R.; Greenberg, E. Sociomicrobiology: The connections between quorum sensing and biofilms. Trends Microbiol. 2005, 13, 27–33. [Google Scholar] [CrossRef]
Madsen, J.S.; Røder, H.L.; Russel, J.; Sørensen, H.; Burmølle, M.; Sørensen, S.J. Coexistence facilitates interspecific biofilm formation in complex microbial communities. Environ. Microbiol. 2016, 18, 2565–2574. [Google Scholar] [CrossRef] [PubMed]
Zhao, A.; Sun, J.; Liu, Y. Understanding bacterial biofilms: From definition to treatment strategies. Front. Cell. Infect. Microbiol. 2023, 13, 1137947. [Google Scholar] [CrossRef] [PubMed]
Carmo, P.H.F.d.; Garcia, M.T.; Figueiredo-Godoi, L.M.A.; Lage, A.C.P.; Silva, N.S.d.; Junqueira, J.C. Metal Nanoparticles to Combat Candida albicans Infections: An Update. Microorganisms 2023, 11, 138. [Google Scholar] [CrossRef]
Omietimi, H.B.; Afolalu, S.A.; Kayode, J.F.; Monye, S.I.; Lawal, S.L.; Emetere, M.E. An overview of nanotechnology and its application. In Proceedings of the E3S Web of Conferences, Tamilnadu, India, 22–23 November 2023; p. 01079. [Google Scholar]
Salata, O. Applications of nanoparticles in biology and medicine. J. Nanobiotechnol. 2004, 2, 3. [Google Scholar] [CrossRef] [PubMed]
Mody, V.V.; Siwale, R.; Singh, A.; Mody, H.R. Introduction to metallic nanoparticles. J. Pharm. Bioallied Sci. 2010, 2, 282. [Google Scholar] [CrossRef]
Grass, G.; Rensing, C.; Solioz, M. Metallic copper as an antimicrobial surface. Appl. Environ. Microbiol. 2011, 77, 1541–1547. [Google Scholar] [CrossRef]
Xu, F.F.; Imlay, J.A. Silver (I), mercury (II), cadmium (II), and zinc (II) target exposed enzymic iron-sulfur clusters when they toxify Escherichia coli. Appl. Environ. Microbiol. 2012, 78, 3614–3621. [Google Scholar] [CrossRef]
Dizaj, S.M.; Lotfipour, F.; Barzegar-Jalali, M.; Zarrintan, M.H.; Adibkia, K. Antimicrobial activity of the metals and metal oxide nanoparticles. Mater. Sci. Eng. C 2014, 44, 278–284. [Google Scholar] [CrossRef]
Vimbela, G.V.; Ngo, S.M.; Fraze, C.; Yang, L.; Stout, D.A. Antibacterial properties and toxicity from metallic nanomaterials. Int. J. Nanomed. 2017, 12, 3941–3965. [Google Scholar] [CrossRef] [PubMed]
Mital, M.; Ziora, Z. Biological applications of Ru (II) polypyridyl complexes. Coord. Chem. Rev. 2018, 375, 434–458. [Google Scholar] [CrossRef]
Sun, L.; Liao, K.; Li, Y.; Zhao, L.; Liang, S.; Guo, D.; Hu, J.; Wang, D. Synergy between polyvinylpyrrolidone-coated silver nanoparticles and azole antifungal against drug-resistant Candida albicans. J. Nanosci. Nanotechnol. 2016, 16, 2325–2335. [Google Scholar] [CrossRef]
Hussain, M.A.; Ahmed, D.; Anwar, A.; Perveen, S.; Ahmed, S.; Anis, I.; Shah, M.R.; Khan, N.A. Combination therapy of clinically approved antifungal drugs is enhanced by conjugation with silver nanoparticles. Int. Microbiol. 2019, 22, 239–246. [Google Scholar] [CrossRef] [PubMed]
Punjabi, K.; Mehta, S.; Chavan, R.; Chitalia, V.; Deogharkar, D.; Deshpande, S. Efficiency of biosynthesized silver and zinc nanoparticles against multi-drug resistant pathogens. Front. Microbiol. 2018, 9, 2207. [Google Scholar] [CrossRef]
Nasiri, K.; Masoumi, S.M.; Amini, S.; Goudarzi, M.; Tafreshi, S.M.; Bagheri, A.; Yasamineh, S.; Alwan, M.; Arellano, M.T.C.; Gholizadeh, O. Recent advances in metal nanoparticles to treat periodontitis. J. Nanobiotechnol. 2023, 21, 283. [Google Scholar] [CrossRef]
Cui, Y.; Zhao, Y.; Tian, Y.; Zhang, W.; Lü, X.; Jiang, X. The molecular mechanism of action of bactericidal gold nanoparticles on Escherichia coli. Biomaterials 2012, 33, 2327–2333. [Google Scholar] [CrossRef]
Akram, F.E.; El-Tayeb, T.; Abou-Aisha, K.; El-Azizi, M. A combination of silver nanoparticles and visible blue light enhances the antibacterial efficacy of ineffective antibiotics against methicillin-resistant Staphylococcus aureus (MRSA). Ann. Clin. Microbiol. Antimicrob. 2016, 15, 48. [Google Scholar] [CrossRef]
Nour El Din, S.; El-Tayeb, T.A.; Abou-Aisha, K.; El-Azizi, M. In vitro and in vivo antimicrobial activity of combined therapy of silver nanoparticles and visible blue light against Pseudomonas aeruginosa. Int. J. Nanomed. 2016, 11, 1749–1758. [Google Scholar]
Graves, J.L., Jr.; Thomas, M.; Ewunkem, J.A. Antimicrobial nanomaterials: Why evolution matters. Nanomaterials 2017, 7, 283. [Google Scholar] [CrossRef]
Padilla-Cruz, A.; Garza-Cervantes, J.; Vasto-Anzaldo, X.G.; García-Rivas, G.; León-Buitimea, A.; Morones-Ramírez, J. Synthesis and design of Ag–Fe bimetallic nanoparticles as antimicrobial synergistic combination therapies against clinically relevant pathogens. Sci. Rep. 2021, 11, 5351. [Google Scholar] [CrossRef] [PubMed]
Martínez Espinosa, J.C.; Carrera Cerritos, R.; Ramírez Morales, M.A.; Sánchez Guerrero, K.P.; Silva Contreras, R.A.; Macías, J.H. Characterization of silver nanoparticles obtained by a green route and their evaluation in the bacterium of Pseudomonas aeruginosa. Crystals 2020, 10, 395. [Google Scholar] [CrossRef]
da Cunha, K.F.; Oliveira Garcia, M.; Allend, S.O.; de Albernaz, D.F.T.; Panagio, L.A.; Neto, A.; Larré Oliveira, T.; Hartwig, D.D. Biogenic silver nanoparticles: In vitro activity against Staphylococcus aureus methicillin-resistant (MRSA) and multidrug-resistant coagulase-negative Staphylococcus (CoNS). Braz. J. Microbiol. 2023, 54, 2641–2650. [Google Scholar] [CrossRef]
Garibo, D.; Borbón-Nuñez, H.A.; de León, J.N.D.; García Mendoza, E.; Estrada, I.; Toledano-Magaña, Y.; Tiznado, H.; Ovalle-Marroquin, M.; Soto-Ramos, A.G.; Blanco, A.; et al. Green synthesis of silver nanoparticles using Lysiloma acapulcensis exhibit high-antimicrobial activity. Sci. Rep. 2020, 10, 12805. [Google Scholar] [CrossRef]
Shaaban, M.T.; Mohamed, B.S.; Zayed, M.; El-Sabbagh, S.M. Antibacterial, antibiofilm, and anticancer activity of silver-nanoparticles synthesized from the cell-filtrate of Streptomyces enissocaesilis. BMC Biotechnol. 2024, 24, 8. [Google Scholar] [CrossRef] [PubMed]
Aisida, S.O.; Ugwu, K.; Nwanya, A.C.; Bashir, A.; Nwankwo, N.U.; Ahmed, I.; Ezema, F.I. Biosynthesis of silver oxide nanoparticles using leave extract of Telfairia Occidentalis and its antibacterial activity. Mater. Today Proc. 2021, 36, 208–213. [Google Scholar] [CrossRef]
D’Lima, L.; Phadke, M.; Ashok, V.D. Biogenic silver and silver oxide hybrid nanoparticles: A potential antimicrobial against multi drug-resistant Pseudomonas aeruginosa. New J. Chem. 2020, 44, 4935–4941. [Google Scholar] [CrossRef]
Lungu, M.; Gavriliu, Ş.; Enescu, E.; Ion, I.; Brătulescu, A.; Mihăescu, G.; Măruţescu, L.; Chifiriuc, M.C. Silver–titanium dioxide nanocomposites as effective antimicrobial and antibiofilm agents. J. Nanoparticle Res. 2014, 16, 2203. [Google Scholar] [CrossRef]
Kamli, M.R.; Alzahrani, E.A.; Albukhari, S.M.; Ahmad, A.; Sabir, J.S.; Malik, M.A. Combination effect of novel bimetallic Ag-Ni nanoparticles with fluconazole against Candida albicans. J. Fungi 2022, 8, 733. [Google Scholar] [CrossRef]
Albayrak, S.; Farajzadeh, N.; Yasemin yenilmez, H.; Özdemir, S.; Gonca, S.; Altuntaş Bayır, Z. Fluorinated Phthalocyanine/Silver Nanoconjugates for Multifunctional Biological Applications. Chem. Biodivers. 2023, 20, e202300389. [Google Scholar] [CrossRef]
El-Behery, R.R.; El-Sayed, E.-S.R.; El-Sayyad, G.S. Gamma rays-assisted bacterial synthesis of bimetallic silver-selenium nanoparticles: Powerful antimicrobial, antibiofilm, antioxidant, and photocatalytic activities. BMC Microbiol. 2023, 23, 224. [Google Scholar] [CrossRef] [PubMed]
Loo, C.-Y.; Rohanizadeh, R.; Young, P.M.; Traini, D.; Cavaliere, R.; Whitchurch, C.B.; Lee, W.-H. Combination of Silver Nanoparticles and Curcumin Nanoparticles for Enhanced Anti-biofilm Activities. J. Agric. Food Chem. 2016, 64, 2513–2522. [Google Scholar] [CrossRef] [PubMed]
Suresh, P.; Doss, A.; Selvi, G.S.A.; Rani, T.P.K.P. Antibiofilm, antibacterial and antioxidant activity of biofabricated bimetallic (Ag-ZnO) nanoparticles from Elephantopus scaber L. Biomass Convers. Biorefin. 2023, 1–11. [Google Scholar] [CrossRef]
Al-Dulaimi, N.M.H.D.; Mohammed, M.J.; Shartooh, S.M. The role of biofilm to isolate the Serratia marcescens in its resistance to antibiotics and study the effect of gold nanoparticles in inhibiting this resistance. Ann. Rom. Soc. Cell Biol. 2021, 1193–1200. [Google Scholar]
Abdel-Raouf, N.; Al-Enazi, N.M.; Ibraheem, I.B. Green biosynthesis of gold nanoparticles using Galaxaura elongata and characterization of their antibacterial activity. Arab. J. Chem. 2017, 10, S3029–S3039. [Google Scholar] [CrossRef]
Vakyly, S.; Sedighian, H.; Jahromi, Z.; Jahangiri, A.; Halabian, R.; Rezaei, A.; Keshmiri, F. A sensitive and selective electrochemical sensor based on gold nanoparticle/multi-walled carbon nanotubes for detection of Staphylococcus aureus Alpha-toxin. Appl. Phys. A 2022, 128, 680. [Google Scholar] [CrossRef]
Ramasamy, M.; Lee, J.-H.; Lee, J. Direct one-pot synthesis of cinnamaldehyde immobilized on gold nanoparticles and their antibiofilm properties. Colloids Surf. B Biointerfaces 2017, 160, 639–648. [Google Scholar] [CrossRef] [PubMed]
Amarasekara, D.L.; Kariyawasam, C.S.; Hejny, M.A.; Torgall, V.B.; Werfel, T.A.; Fitzkee, N.C. Protein-Functionalized Gold Nanospheres with Tunable Photothermal Efficiency for the Near-Infrared Photothermal Ablation of Biofilms. ACS Appl. Mater. Interfaces 2024, 16, 4321–4332. [Google Scholar] [CrossRef]
Naseer, M.; Ramadan, R.; Xing, J.; Samak, N.A. Facile green synthesis of copper oxide nanoparticles for the eradication of multidrug resistant Klebsiella pneumonia and Helicobacter pylori biofilms. Int. Biodeterior. Biodegrad. 2021, 159, 105201. [Google Scholar] [CrossRef]
Gupta, A.; Maruthapandi, M.; Das, P.; Saravanan, A.; Jacobi, G.; Natan, M.; Banin, E.; Luong, J.H.; Gedanken, A. Cuprous Oxide Nanoparticles Decorated Fabric Materials with Anti-Biofilm Properties. ACS Appl. Bio-Mater. 2022, 5, 4310–4320. [Google Scholar] [CrossRef]
Munusamy, T.; Shanmugam, R. Green Synthesis of Copper Oxide Nanoparticles Synthesized by Terminalia chebula Dried Fruit Extract: Characterization and Antibacterial Action. Cureus 2023, 15, e50142. [Google Scholar] [CrossRef] [PubMed]
Sarfraz, M.H.; Zubair, M.; Aslam, B.; Ashraf, A.; Siddique, M.H.; Hayat, S.; Cruz, J.N.; Muzammil, S.; Khurshid, M.; Sarfraz, M.F.; et al. Comparative analysis of phyto-fabricated chitosan, copper oxide, and chitosan-based CuO nanoparticles: Antibacterial potential against Acinetobacter baumannii isolates and anticancer activity against HepG2 cell lines. Front. Microbiol. 2023, 14, 1188743. [Google Scholar] [CrossRef]
Zhao, H.; Maruthupandy, M.; Al-mekhlafi, F.A.; Chackaravarthi, G.; Ramachandran, G.; Chelliah, C.K. Biological synthesis of copper oxide nanoparticles using marine endophytic actinomycetes and evaluation of biofilm producing bacteria and A549 lung cancer cells. J. King Saud Univ. Sci. 2022, 34, 101866. [Google Scholar] [CrossRef]
Khan, M.F.; Husain, F.M.; Zia, Q.; Ahmad, E.; Jamal, A.; Alaidarous, M.; Banawas, S.; Alam, M.M.; Alshehri, B.A.; Jameel, M.; et al. Anti-quorum sensing and anti-biofilm activity of zinc oxide nanospikes. ACS Omega 2020, 5, 32203–32215. [Google Scholar] [CrossRef]
Husain, F.M.; Hasan, I.; Qais, F.A.; Khan, R.A.; Alam, P.; Alsalme, A. Fabrication of zinc oxide-xanthan gum nanocomposite via green route: Attenuation of quorum sensing regulated virulence functions and mitigation of biofilm in gram-negative bacterial pathogens. Coatings 2020, 10, 1190. [Google Scholar] [CrossRef]
McGuffie, M.J.; Hong, J.; Bahng, J.H.; Glynos, E.; Green, P.F.; Kotov, N.A.; Younger, J.G.; VanEpps, J.S. Zinc oxide nanoparticle suspensions and layer-by-layer coatings inhibit staphylococcal growth. Nanomed. Nanotechnol. Biol. Med. 2016, 12, 33–42. [Google Scholar] [CrossRef] [PubMed]
Husain, F.M.; Qais, F.A.; Ahmad, I.; Hakeem, M.J.; Baig, M.H.; Masood Khan, J.; Al-Shabib, N.A. Biosynthesized zinc oxide nanoparticles disrupt established biofilms of pathogenic bacteria. Appl. Sci. 2022, 12, 710. [Google Scholar] [CrossRef]
Shalom, Y.; Perelshtein, I.; Perkas, N.; Gedanken, A.; Banin, E. Catheters coated with Zn-doped CuO nanoparticles delay the onset of catheter-associated urinary tract infections. Nano Res. 2017, 10, 520–533. [Google Scholar] [CrossRef]
Shome, S.; Talukdar, A.D.; Nath, R.; Tewari, S. Curcumin-ZnO nanocomposite mediated inhibition of Pseudomonas aeruginosa biofilm and its mechanism of action. J. Drug Deliv. Sci. Technol. 2023, 81, 104301. [Google Scholar] [CrossRef]
Vidic, J.; Stankic, S.; Haque, F.; Ciric, D.; Le Goffic, R.; Vidy, A.; Jupille, J.; Delmas, B. Selective antibacterial effects of mixed ZnMgO nanoparticles. J. Nanoparticle Res. 2013, 15, 1595. [Google Scholar] [CrossRef]
Alzahrani, K.E.; Niazy, A.A.; Alswieleh, A.M.; Wahab, R.; El-Toni, A.M.; Alghamdi, H.S. Antibacterial activity of trimetal (CuZnFe) oxide nanoparticles. Int. J. Nanomed. 2018, 77–87. [Google Scholar] [CrossRef] [PubMed]
He, W.; Kim, H.-K.; Wamer, W.G.; Melka, D.; Callahan, J.H.; Yin, J.-J. Photogenerated charge carriers and reactive oxygen species in ZnO/Au hybrid nanostructures with enhanced photocatalytic and antibacterial activity. J. Am. Chem. Soc. 2014, 136, 750–757. [Google Scholar] [CrossRef]
Gingasu, D.; Culita, D.C.; Calderon Moreno, J.M.; Marinescu, G.; Bartha, C.; Oprea, O.; Preda, S.; Chifiriuc, M.C.; Popa, M. Synthesis of CoFe₂O₄ through Wet Ferritization Method Using an Aqueous Extract of Eucalyptus Leaves. Coatings 2023, 13, 1250. [Google Scholar] [CrossRef]
Arakha, M.; Pal, S.; Samantarrai, D.; Panigrahi, T.K.; Mallick, B.C.; Pramanik, K.; Mallick, B.; Jha, S. Antimicrobial activity of iron oxide nanoparticle upon modulation of nanoparticle-bacteria interface. Sci. Rep. 2015, 5, 14813. [Google Scholar] [CrossRef] [PubMed]
Rothpan, M.; Chandra Teja Dadi, N.; McKay, G.; Tanzer, M.; Nguyen, D.; Hart, A.; Tabrizian, M. Titanium-Dioxide-Nanoparticle-Embedded Polyelectrolyte Multilayer as an Osteoconductive and Antimicrobial Surface Coating. Materials 2023, 16, 7026. [Google Scholar] [CrossRef]
Alizadeh, S.R.; Abbastabar, M.; Nosratabadi, M.; Ebrahimzadeh, M.A. High antimicrobial, cytotoxicity, and catalytic activities of biosynthesized selenium nanoparticles using Crocus caspius extract. Arab. J. Chem. 2023, 16, 104705. [Google Scholar] [CrossRef]
Hayat, S.; Muzammil, S.; Rasool, M.H.; Nisar, Z.; Hussain, S.Z.; Sabri, A.N.; Jamil, S. In vitro antibiofilm and anti-adhesion effects of magnesium oxide nanoparticles against antibiotic resistant bacteria. Microbiol. Immunol. 2018, 62, 211–220. [Google Scholar] [CrossRef]
Cai, L.; Chen, J.; Liu, Z.; Wang, H.; Yang, H.; Ding, W. Magnesium oxide nanoparticles: Effective agricultural antibacterial agent against Ralstonia solanacearum. Front. Microbiol. 2018, 9, 335574. [Google Scholar] [CrossRef]
Makhluf, S.; Dror, R.; Nitzan, Y.; Abramovich, Y.; Jelinek, R.; Gedanken, A. Microwave-assisted synthesis of nanocrystalline MgO and its use as a bacteriocide. Adv. Funct. Mater. 2005, 15, 1708–1715. [Google Scholar] [CrossRef]
Saleem, S.; Ahmed, B.; Khan, M.S.; Al-Shaeri, M.; Musarrat, J. Inhibition of growth and biofilm formation of clinical bacterial isolates by NiO nanoparticles synthesized from Eucalyptus globulus plants. Microb. Pathog. 2017, 111, 375–387. [Google Scholar] [CrossRef]
Hoshyar, N.; Gray, S.; Han, H.; Bao, G. The effect of nanoparticle size on in vivo pharmacokinetics and cellular interaction. Nanomedicine 2016, 11, 673–692. [Google Scholar] [CrossRef] [PubMed]
Ren, E.; Zhang, C.; Li, D.; Pang, X.; Liu, G. Leveraging metal oxide nanoparticles for bacteria tracing and eradicating. View 2020, 1, 20200052. [Google Scholar] [CrossRef]
Nisar, P.; Ali, N.; Rahman, L.; Ali, M.; Shinwari, Z.K. Antimicrobial activities of biologically synthesized metal nanoparticles: An insight into the mechanism of action. J. Biol. Inorg. Chem. 2019, 24, 929–941. [Google Scholar] [CrossRef] [PubMed]
Gallo, G.; Schillaci, D. Bacterial metal nanoparticles to develop new weapons against bacterial biofilms and infections. Appl. Microbiol. Biotechnol. 2021, 105, 5357–5366. [Google Scholar] [CrossRef] [PubMed]
Khan, S.A.; Jain, M.; Pandey, A.; Pant, K.K.; Ziora, Z.M.; Blaskovich, M.A.; Shetti, N.P.; Aminabhavi, T.M. Leveraging the potential of silver nanoparticles-based materials towards sustainable water treatment. J. Environ. Manag. 2022, 319, 115675. [Google Scholar] [CrossRef]
Pryshchepa, O.; Pomastowski, P.; Buszewski, B. Silver nanoparticles: Synthesis, investigation techniques, and properties. Adv. Colloid Interface Sci. 2020, 284, 102246. [Google Scholar] [CrossRef]
Yadi, M.; Mostafavi, E.; Saleh, B.; Davaran, S.; Aliyeva, I.; Khalilov, R.; Nikzamir, M.; Nikzamir, N.; Akbarzadeh, A.; Panahi, Y.; et al. Current developments in green synthesis of metallic nanoparticles using plant extracts: A review. Artif. Cells Nanomed. Biotechnol. 2018, 46, 336–343. [Google Scholar] [CrossRef]
Zhang, X.-F.; Liu, Z.-G.; Shen, W.; Gurunathan, S. Silver nanoparticles: Synthesis, characterization, properties, applications, and therapeutic approaches. Int. J. Mol. Sci. 2016, 17, 1534. [Google Scholar] [CrossRef]
Chen, Z.; Balankura, T.; Fichthorn, K.A.; Rioux, R.M. Revisiting the polyol synthesis of silver nanostructures: Role of chloride in nanocube formation. ACS Nano 2019, 13, 1849–1860. [Google Scholar] [CrossRef]
Ishak, N.M.; Kamarudin, S.; Timmiati, S. Green synthesis of metal and metal oxide nanoparticles via plant extracts: An overview. Mater. Res. Express 2019, 6, 112004. [Google Scholar] [CrossRef]
Vishwanath, R.; Negi, B. Conventional and green methods of synthesis of silver nanoparticles and their antimicrobial properties. Curr. Res. Green Sustain. Chem. 2021, 4, 100205. [Google Scholar] [CrossRef]
Kibis, L.; Stadnichenko, A.; Pajetnov, E.; Koscheev, S.; Zaykovskii, V.; Boronin, A. The investigation of oxidized silver nanoparticles prepared by thermal evaporation and radio-frequency sputtering of metallic silver under oxygen. Appl. Surf. Sci. 2010, 257, 404–413. [Google Scholar] [CrossRef]
Kylián, O.; Kuzminova, A.; Štefaníková, R.; Hanuš, J.; Solař, P.; Kúš, P.; Cieslar, M.; Choukourov, A.; Biederman, H. Silver/plasma polymer strawberry-like nanoparticles produced by gas-phase synthesis. Mater. Lett. 2019, 253, 238–241. [Google Scholar] [CrossRef]
Kang, W.J.; Cheng, C.Q.; Li, Z.; Feng, Y.; Shen, G.R.; Du, X.W. Ultrafine Ag nanoparticles as active catalyst for electrocatalytic hydrogen production. ChemCatChem 2019, 11, 5976–5981. [Google Scholar] [CrossRef]
Scuderi, M.; Esposito, M.; Todisco, F.; Simeone, D.; Tarantini, I.; De Marco, L.; De Giorgi, M.; Nicotra, G.; Carbone, L.; Sanvitto, D.; et al. Nanoscale study of the tarnishing process in electron beam lithography-fabricated silver nanoparticles for plasmonic applications. J. Phys. Chem. C 2016, 120, 24314–24323. [Google Scholar] [CrossRef]
Koduru, J.R.; Kailasa, S.K.; Bhamore, J.R.; Kim, K.-H.; Dutta, T.; Vellingiri, K. Phytochemical-assisted synthetic approaches for silver nanoparticles antimicrobial applications: A review. Adv. Colloid Interface Sci. 2018, 256, 326–339. [Google Scholar] [CrossRef] [PubMed]
Puiatti, G.A.; de Carvalho, J.P.; de Matos, A.T.; Lopes, R.P. Green synthesis of Fe0 nanoparticles using Eucalyptus grandis leaf extract: Characterization and application for dye degradation by a (Photo) Fenton-like process. J. Environ. Manag. 2022, 311, 114828. [Google Scholar] [CrossRef] [PubMed]
Xiao, C.; Li, H.; Zhao, Y.; Zhang, X.; Wang, X. Green synthesis of iron nanoparticle by tea extract (polyphenols) and its selective removal of cationic dyes. J. Environ. Manag. 2020, 275, 111262. [Google Scholar] [CrossRef]
Jamkhande, P.G.; Ghule, N.W.; Bamer, A.H.; Kalaskar, M.G. Metal nanoparticles synthesis: An overview on methods of preparation, advantages and disadvantages, and applications. J. Drug Deliv. Sci. Technol. 2019, 53, 101174. [Google Scholar] [CrossRef]
Lansdown, A.B. A pharmacological and toxicological profile of silver as an antimicrobial agent in medical devices. Adv. Pharmacol. Sci. 2010, 2010, 910686. [Google Scholar] [CrossRef]
Möhler, J.S.; Sim, W.; Blaskovich, M.A.; Cooper, M.A.; Ziora, Z.M. Silver bullets: A new lustre on an old antimicrobial agent. Biotechnol. Adv. 2018, 36, 1391–1411. [Google Scholar] [CrossRef] [PubMed]
Chen, X.; Schluesener, H.J. Nanosilver: A nanoproduct in medical application. Toxicol. Lett. 2008, 176, 1–12. [Google Scholar] [CrossRef]
Eckhardt, S.; Brunetto, P.S.; Gagnon, J.; Priebe, M.; Giese, B.; Fromm, K.M. Nanobio silver: Its interactions with peptides and bacteria, and its uses in medicine. Chem. Rev. 2013, 113, 4708–4754. [Google Scholar] [CrossRef] [PubMed]
Brandtzaeg, P. Mucosal immunity in the female genital tract. J. Reprod. Immunol. 1997, 36, 23–50. [Google Scholar] [CrossRef]
Javurek, A.B.; Suresh, D.; Spollen, W.G.; Hart, M.L.; Hansen, S.A.; Ellersieck, M.R.; Bivens, N.J.; Givan, S.A.; Upendran, A.; Kannan, R.; et al. Gut dysbiosis and neurobehavioral alterations in rats exposed to silver nanoparticles. Sci. Rep. 2017, 7, 2822. [Google Scholar] [CrossRef]
Hadrup, N.; Lam, H.R. Oral toxicity of silver ions, silver nanoparticles and colloidal silver—A review. Regul. Toxicol. Pharmacol. 2014, 68, 1–7. [Google Scholar] [CrossRef]
Mathur, P.; Jha, S.; Ramteke, S.; Jain, N. Pharmaceutical aspects of silver nanoparticles. Artif. Cells Nanomed. Biotechnol. 2018, 46, 115–126. [Google Scholar] [CrossRef] [PubMed]

Figure 3. Two main strategies for the synthesis of metallic nanoparticles. Biological methods such as green synthesis follow the bottom-up approach and reduce metal ions to metal nanoparticles. Image created using ©2024 Biorender.

Figure 5. PRISMA flow diagram for the included studies from 2004 to 2024.

Figure 6. Publications per year on single metallic nanoparticles and bimetallic nanoparticles over 2004–2024. This graph was prepared using Prism 10 software. Note that for 2024, only the period from January to June 2024 is included.

Figure 7. The yearly and cumulative patent trend in last two decades. Data is obtained from searching the Espacenet database.

Figure 8. Metallic nanoparticle patent numbers by jurisdiction. This figure was prepared using Prism 10 software.

Figure 9. Patent applications (“reports”) and granted patents per year from 2004 to 2024 for metallic nanoparticles used for antimicrobial treatments. This figure was prepared using Prism 10 software.

Figure 10. Network analysis for silver nanoparticles, showing nodes for nanoparticle characterization (red) and for antimicrobial potency aspects (blue). This figure was prepared using VOS Viewer.

Figure 11. Network analysis for zinc nanoparticles showing characterization (red) and performance (blue). This figure was prepared using VOS Viewer software.

Figure 12. Network analysis for copper nanoparticles, showing characterization (red) and performance (blue). This figure was prepared using VOS Viewer software.

Figure 13. Network analysis for gold nanoparticles, showing characterization (red) and performance (blue). This figure was prepared using VOS Viewer software.

Table 1. Metallic nanoparticles as antimicrobial agents used alone and in complexes to treat planktonic bacteria and to reduce or eradicate existing biofilms.

Metallic Nanoparticles (Reference)		Size (nm) and Shape	Synthesis Resource	MIC (μg/mL) Reduction Ratio Inhibition Zone (mm)	Microorganism	Comments
Silver	Silver (AgNPs) [33]	50 Hexagonal	AgNO₃ + leaves of Geranium	0.18 - 8.5	P. aeruginosa ATCC-27853	Antibacterial actions
	Silver (AgNPs) [34]	100 Spherical	AgNO₃ + malt extract	3.75–15 60–100% -	S. aureus ATCC 25904	For standard strains and MDR isolates and reduced and eradicated biofilms. Anti-biofilm actions.
	Silver (AgNPs) [35]	1.2–62 Spherical	AgNO₃ + L. acapulcensis extract	0.06 99.9% 16	S. aureus ATCC 49476	Significant antimicrobial effects on S. aureus and P. aeruginosa
	Silver (AgNPs) [35]	1.2–62 Spherical	AgNO₃ + L. acapulcensis extract	0.06 99.9% 15	P. aeruginosa ATCC 27853
	Silver (AgNPs) [36]	32.2 Spherical	AgNO₃ + starch broth medium	- 10.7% 34.6% 39.08% 34.75% -	P. aeruginosa ATCC 9027	Antibacterial and anti-biofilm actions
					S. typhi ATCC 12023
					S. aureus ATCC 6598
					E. coli ATCC 8739
Silver oxide	Silver oxide (AgONPs) [37]	10–25 Spherical	Fresh Telfairia occidentalis leaves + AgNO₃	20 - 15	K. pneumoniae isolated from humans	Strong antibacterial activity
Silver oxide	Silver oxide (AgONPs) [38]	10–50 Spherical	Actinomycetes spp. + AgNO₃	500 - 15	MDR P. aeruginosa	Antibacterial activity
Silver-containing nanoparticles	Ag–TiO₂ NPs [39]	31.3 ± 0.5 or 23.4 ± 0.4 -	TiO₂ nanopowder	150 - -	B. subtilis IC 12488	Antibacterial and anti-biofilm activity
			TiO₂ nanopowder	150 -	S. aureus IC 13204
			AgNO₃	1200 -	E. coli IC 13529
			AgNO₃	1200 -	K. pneumoniae IC 13420
			PSSA-co-MA	1200 -	P. aeruginosa IC 13202
	Ag-Fe NPs [32]	13 -	G. jasminoides	65 - -	C. albicans	Growth inhibition
			AgNO₃
			Fe(NO₃)₃
	Ag-Ni nanoparticles [40]	31.84–47.85 -	AgNO₃	1.56 - -	C. albicans SC 5314	Growth inhibition and anti-biofilm activity
			Ni(NO₃)₂·6H₂O			Inhibition of morphogenesis
			Salvia officinalis			Reduced efflux pump genes
			Salvia officinalis			ROS production
	Fluorinated Phthalocyanine–silver NPs [41]	15–20 -	Silver nanoparticles	8 95–100% -	P. aeruginosa ATCC 27853	Antioxidant effects
			Phthalonitrile	8 99–100% -	E. coli ATCC 25922	Antimicrobial and anti-biofilm actions
			Phthalocyanines	8 99–100% -	E. coli ATCC 25922	Antimicrobial photodynamic therapy activities
	Ag-Se nanoparticles [42]	66.5 -	AgNO₃	62.5 90.7% -	C. albicans ATCC 10231	Antifungal
			Sodium selenite	62.5 90.6% -	C. albicans ATCC 10231	Antibacterial activity
				62.5 90.6% -	E. coli ATCC 11229	Anti-biofilm actions
				125 86.2% -	P. aeruginosa ATCC 6538	Free radical scavenging
	Silver–curcumin NPs [43]	30 -	AgNO₃	3 - -	P. aeruginosa PA01	Antibacterial and anti-biofilm actions
			Gallic acid	3 - -	P. aeruginosa PA01
			Curcumin	50 - -	S. aureus ATCC 25923
			PVP	50 - -	S. aureus ATCC 25923
	Ag-ZnO NPs [44]	28 -	E. scaber leaves	0.125 62.5% -	S. aureus	Antibacterial actions
			Zinc nitrate		B. subtilis	Anti-biofilm actions
			AgNO₃		B. subtilis	Antioxidant
Gold	Gold (AuNPs) [45]	5–50 Spherical	Trisodium citrate HAuCl₄·4H₂O	18.71 80.4% 6.3	S. marcescens Clinical collection	Antibacterial and anti-biofilm activity, through production of ROS
	Gold(AuNPs) [46]	20–100 Hexagonal	Marine alga G. elongate HAuCl₄ aqueous solution	- - 13–17	K. pneumoniae ATCC 27738	Antibacterial activity
	Gold(AuNPs) [47]	18 Spherical	HAuCl₄·4H₂O Trisodium citrate solution	- - -	S. aureus collected from volunteer	/
	Gold(AuNPs) [48]	11 ± 3 Spherical	Cinnamaldehyde HAuCl₄·4H₂O	- 93% -	C. albicans DAY185	Anti-biofilm actions
	Gold(AuNPs) [49]	43 Spherical	Chloroauric acid Citrate	120 - -	E. coli ATCC25992	Antibacterial and anti-biofilm actions
				120 - -	S. epidermidis 1301
				1 - 15.5	C. krusei not determined
				1 - 20.5	C. glabrata not determined
Copper	Copper (CuNPs) [50]	28.3 (C), 43.8 (M) Spherical	Cassia fistula (C) and Melia azedarach (M) leaves + cupric nitrate trihydrate	1000 99.8%,92.5% 15.13	K. pneumonia from collection center	Antibacterial and anti-biofilm actions toward both species
Copper	Copper (CuNPs) [50]	28.3 (C), 43.8 (M) Spherical		1000 100%,99.5% 2.6	H. pylori from collection center	Antibacterial and anti-biofilm actions toward both species
Copper oxide	Copper oxide (CuONPs) [51]	80–300 Spherical	Cu₂O microparticles + ethanol	- 98% -	MDR E. coli	Antibacterial and anti-biofilm actions
	Copper oxide (CuONPs) [51]	80–300 Spherical	Cu₂O microparticles + ethanol	- 99.2% -	MDR S. aureus	Antibacterial and anti-biofilm actions
	Copper oxide (CuONPs) [52]	10–12 Spherical	Copper sulfate T. chebula extract	1000 – 15.67	E. coli not determined	Antibacterial and anti-biofilm actions
				1000 - 16	S. aureus not determined
				750 - 17	P. aeruginosa not determined
	Copper oxide(CuONPs) [53]	28–33 Spherical	Copper sulfate solution Leaf extract	125 - 12–13	A. baumannii MH 605335	Antibacterial and anti-biofilm actions
	Copper oxide(CuONPs) [54]	20 Spherical	Copper sulfate (CuSO₄∙5H₂O) Cell free supernatant	1000 96% -	E. coli from mat	Anti-biofilm actions
Zinc oxide	Zinc oxide (ZnONPs) [55]	40–130 Spikes	Zinc acetate Dihydrate DDW CTAB	800 80–85% -	P. aeruginosa PAO 1	Anti-biofilm actions and inhibition of QS for resistant P. aeruginosa
	Zinc oxide (ZnONPs) [55]	40–130 Spikes	Zinc acetate Dihydrate DDW CTAB	500 80% -	C. violaceum CVO26
	Zinc oxide–Xanthan nanocomposite [56]	16 Rod	Zn(NO₃)₂∙6H₂O + xanthan gum + NaOH	256 70% -	C. violaceum ATCC 12472	Anti-biofilm actions
	Zinc oxide–Xanthan nanocomposite [56]	16 Rod	Zn(NO₃)₂∙6H₂O + xanthan gum + NaOH	256 75% -	S. marcescens ATCC 13880	Anti-biofilm actions
	Zinc oxide (ZnONPs) [57]	4.4 Spherical hexagonal	Zn(Ac)₂∙2H₂O Anhydrous methanol KOH	500 98.5% -	S. aureus SH 1000	Antibacterial and anti-biofilm actions
	Zinc oxide (ZnONPs) [57]	4.4 Spherical hexagonal	Zn(Ac)₂∙2H₂O Anhydrous methanol KOH	500 - -	E. coli UT 189	Antibacterial and anti-biofilm actions
	Zinc oxide (ZnONPs) [58]	24.62 Spherical spheroidal	Plumbago zeylanica L. Zinc acetate	- 52.69% -	E. coli ATCC 25922	Inhibition of biofilm growth and anti-biofilm actions
				- 59.79% -	S. aureus MTCC 3160
				- 67.22% -	P. aeruginosa PAO 1
Zinc-containing nanoparticles	Zn-doped CuO NPs [59]	- -	Copper zinc acetates	- 91% -	E. coli ATCC 25922	Inhibition of biofilm formation and anti-biofilm actions
			Aqueous ammonium hydroxide	- 92% -	S. aureus ATCC 29213
			Ethanol	- 95% -	P. mirabilis not determined
	Curcumin-ZnO NPs [60]	110.51 -	Zinc nitrate hexahydrate	62.5 45–90% -	P. aeruginosa PAO 1	Anti-biofilm actions
	Curcumin-ZnO NPs [60]	110.51 -	2-Thiobarbituric acid	62.5 45–90% -	P. aeruginosa PAO 1	Anti-biofilm actions
	ZnMgO NPs [61]	10 -	MgO	- 61% -	E. coli BL21 DE3	Antibacterial actions
	ZnMgO NPs [61]	10 -	ZnO	- 25% -	B. subtilis 168	Antibacterial actions
	ZnCuFe NPs [62]	42 -	Zinc acetate dihydrate	150 85% -	E. coli from chronic infection	Antibacterial and anti-biofilm activity
			Copper acetate hydrate	150 85% -	E. coli from chronic infection
			Iron nitrate nonahydrate	150 55% -	E. faecalis from chronic infection
			n-propyl amine	150 55% -	E. faecalis from chronic infection
	ZnO-Au hybrid NPs [63]	30 -	ZnO	- 90% -	S. aureus not determined	Antibacterial effects
	ZnO-Au hybrid NPs [63]	30 -	AuCl₄⁻	- 90% -	E. coli not determined	Antibacterial effects
Cobalt-containing nanoparticles	CoFe₂O₄ NPs [64]	10 -	Iron nitrate	5000 - -	C. albicans ATCC 10231	Antimicrobial effects and anti-biofilm actions
			Cobalt nitrate	5000 - -	P. aeruginosa ATCC 27853
			Eucalyptus plant extract	5000 - -	E. coli ATCC 25922
Iron oxide	Iron oxide NPs [65]	10–11 Spherical	Ferrous chloride tetrahydrate (FeCl₂∙4H₂O)	50 - -	E. coli not determined	Antimicrobial effects and anti-biofilm actions
Iron oxide	Iron oxide NPs [65]	10–11 Spherical	Ferric chloride hexahydrate (FeCl₃∙6H₂O)	50 - -	E. coli not determined	Antimicrobial effects and anti-biofilm actions
Titanium Dioxide	TiO₂ NPs [66]	39.2 Rods	Titanium rods, Chitosan, Alginic acid sodium salt	400 - -	S. aureus DNC274 ATCC 29213	Antibacterial and anti-biofilm actions
Selenium	Se NPs [67]	23.47 Red spherical	Sodium selenite DPPH Sodium borohydride	25 - -	C. albicans IFRC 1873	Antifungal activity against tested fungi strains
					F. proliferatum IFRC 1871
					F. equiseti IFRC 1872
					T. mentagrophytes FR5_22130
					A. fumigatus IFRC 1649
Magnesium oxide	MgO NPs [68]	50–70 spherical	NaOH, NaNO₃, MgCl₂	250 82.9% 28 ± 0.33 mm (2000 μg/mL) 21 ± 0.288 mm (1000 μg/mL) 17.5 ± 0.288 mm (500 μg/mL)	E. coli KT273995	Antibacterial activity and anti-biofilm actions
				125 82.9% 35.5 ± 0.33 mm (2000 μg/mL) 35.5 ± 0.288 mm (1000 μg/mL) 30.5 ± 1.90 mm (500 μg/mL)	Klebsiella pneumoniae KT273996
				500 82.9% 25.5 ± 0.268 mm (2000 μg/mL) 23.5 ± 1.32 mm (1000 μg/mL) 20.5 ± 2.18 mm (500 μg/mL)	Staphylococcus aureus KT250728
	[69]	50–100 irregular but spherical particle-like shapes	Purchased from Sigma Aldrich Chemical Co. (Saint Louis, MO, USA)	200 93.40 to 95.60% 14.30 mm	R. solanacearum from infected tobacco	Bacteriostatic at low concentrations and anti-biofilm activity
	[70]	4 square and polyhedral shape	Mg(CH₃COO)₂, Aerogel AP-MgO	625 99.9% -	E. coli not determined	Antibacterial effects and anti-biofilm activity
	[70]	4 square and polyhedral shape	Mg(CH₃COO)₂, Aerogel AP-MgO	625 95% -	S. aureus not determined	Antibacterial effects and anti-biofilm activity
Nickle oxide	NiO NPs [71]	14 ± 5.8 polymorphic	Eucalyptus leaf extract (ELE), Ni(NO₃)₂·6H₂O	800 - 15	Methicillin sensitive S. aureus-06	Antibacterial and anti-biofilm activity against the tested strains
				800 - 13	Methicillin sensitive S. aureus-02
				800 - 15	P. aeruginosa-48
				800 - 14	P. aeruginosa-64
				1.600 - 17	E. coli-60
				800 - 17	E. coli-52
				800 - 15	Methicillin-resistant S. aureus-10
				800 - 14	Methicillin-resistant S. aureus-31

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Li, H.; Yang, Z.; Khan, S.A.; Walsh, L.J.; Seneviratne, C.J.; Ziora, Z.M. Characteristics of Metallic Nanoparticles (Especially Silver Nanoparticles) as Anti-Biofilm Agents. Antibiotics 2024, 13, 819. https://doi.org/10.3390/antibiotics13090819

AMA Style

Li H, Yang Z, Khan SA, Walsh LJ, Seneviratne CJ, Ziora ZM. Characteristics of Metallic Nanoparticles (Especially Silver Nanoparticles) as Anti-Biofilm Agents. Antibiotics. 2024; 13(9):819. https://doi.org/10.3390/antibiotics13090819

Chicago/Turabian Style

Li, Hongze, Zhihe Yang, Sadaf Aiman Khan, Laurence J. Walsh, Chaminda Jayampath Seneviratne, and Zyta M. Ziora. 2024. "Characteristics of Metallic Nanoparticles (Especially Silver Nanoparticles) as Anti-Biofilm Agents" Antibiotics 13, no. 9: 819. https://doi.org/10.3390/antibiotics13090819

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Characteristics of Metallic Nanoparticles (Especially Silver Nanoparticles) as Anti-Biofilm Agents

Abstract

1. Introduction

Biofilm Formation and the Interactions between Biofilm Components and Antimicrobial Agents

2. Recent Advances in Nanometal Research

2.1. Types of Metallic Nanoparticles and Their Efficacy

2.1.1. Silver Nanoparticles

2.1.2. Gold Nanoparticles

2.1.3. Copper Nanoparticles

2.1.4. Zinc Nanoparticles

2.1.5. Other Metallic Nanoparticles

2.2. Combinations of Metal Nanoparticles with Other Agents

2.3. Biofilm Inhibition by Metallic Nanoparticles

2.4. Methods for the Synthesis of Silver Nanoparticles

Methods for Synthesis of AgNPs

2.5. Biosafety of AgNPs When Applied onto the Human Body

2.6. Analysis of the Literature from 2004 to 2024

3. Conclusions and Future Directions

Author Contributions

Funding

Institutional Review Board Statement

Informed Consent Statement

Acknowledgments

Conflicts of Interest

References

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