Materials Science and Engineering C 44 (2014) 278–284

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Materials Science and Engineering C

journal homepage: www.elsevier.com/locate/msec

Review

Antimicrobial activity of the metals and metal oxide nanoparticles

Solmaz Maleki Dizaj a, Farzaneh Lotfipour a, Mohammad Barzegar-Jalali a,
Mohammad Hossein Zarrintan a, Khosro Adibkia b,⁎
a
Drug Applied Research Center and Faculty of Pharmacy, Tabriz University of Medical Sciences, Tabriz, Iran
b
Biotechnology Research Center and Faculty of Pharmacy, Tabriz University of Medical Sciences, Tabriz, Iran

a r t i c l e i n f o a b s t r a c t

Article history: The ever increasing resistance of pathogens towards antibiotics has caused serious health problems in the recent
Received 7 May 2014 years. It has been shown that by combining modern technologies such as nanotechnology and material science
Received in revised form 5 July 2014 with intrinsic antimicrobial activity of the metals, novel applications for these substances could be identified.
Accepted 8 August 2014
According to the reports, metal and metal oxide nanoparticles represent a group of materials which were inves-
Available online 16 August 2014
tigated in respect to their antimicrobial effects. In the present review, we focused on the recent research works
Keywords:
concerning antimicrobial activity of metal and metal oxide nanoparticles together with their mechanism of
Antimicrobial activity action. Reviewed literature indicated that the particle size was the essential parameter which determined the
Metal nanoparticles antimicrobial effectiveness of the metal nanoparticles. Combination therapy with the metal nanoparticles
Metal oxide nanoparticles might be one of the possible strategies to overcome the current bacterial resistance to the antibacterial agents.
Reactive oxygen species However, further studies should be performed to minimize the toxicity of metal and metal oxide nanoparticles
to apply as proper alternatives for antibiotics and disinfectants especially in biomedical applications.
© 2014 Elsevier B.V. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 278
2. Ag and Ag2O nanoparticles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 279
3. ZnO nanoparticles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 280
4. TiO2 nanoparticles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 280
5. Au nanoparticles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 280
6. Si and SiO2 nanoparticles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 281
7. MgO and CaO nanoparticles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 281
8. Cu and CuO nanoparticles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 281
9. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 283
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 283

1. Introduction new and effective antimicrobial agents seems to be of paramount

importance. The antimicrobial activity of metals such as silver (Ag),
Emergence of the antibiotic resistance pathogens has become a copper (Cu), gold (Au), titanium (Ti), and zinc (Zn), each having various
serious health issue and thus, numerous studies have been reported to properties, potencies and spectra of activity, has been known and
improve the current antimicrobial therapies. It is known that over 70% applied for centuries [2].
of bacterial infections are resistant to one or more of the antibiotics Recently, nanotechnology has offered great possibilities in various
that are generally used to eradicate the infection [1]. Development of fields of science and technology. Pharmaceutical nanotechnology with
numerous advantages has growingly attracted the attention of many
researchers [3]. The application of nanomaterials in the drug delivery
⁎ Corresponding author at: Faculty of Pharmacy, Tabriz University of Medical Sciences,
Golgasht Street, Daneshgah Ave., Tabriz, Iran. Tel.: +98 411 3341315; fax: + 98 411
systems has been investigated for more than twenty years bringing
3344798. about innovation of dosage forms with improved therapeutic effects
E-mail address: adibkia@tbzmed.ac.ir (K. Adibkia). and physicochemical characteristics [4,5]. Several types of nanoparticles

http://dx.doi.org/10.1016/j.msec.2014.08.031
0928-4931/© 2014 Elsevier B.V. All rights reserved.
 S.M. Dizaj et al. / Materials Science and Engineering C 44 (2014) 278–284
and their derivatives have received great attention for their potential
antimicrobial effects. Metal nanoparticles such as Ag, silver oxide
(Ag2O), titanium dioxide (TiO2), silicon (Si), copper oxide (CuO), zinc
oxide (ZnO), Au, calcium oxide (CaO) and magnesium oxide (MgO)
were identified to exhibit antimicrobial activity. In vitro studies
revealed that metal nanoparticles inhibited several microbial species.
The kind of the materials used for preparing the nanoparticles as
well as the particle size were two important parameters that affected
the resultant antimicrobial effectiveness [6,7]. Generally nanoparticles
have different properties compared to the same material with the larger
particles owing to the fact that the surface/volume ratio of the nanopar-
ticles increases considerably with decrease in the particle size [8,9].
Indeed, in the nanometer dimensions, fraction of the surface molecule
is noticeably increased which in turn improves some properties of the
particles e.g. heat treatment, mass transfer, dissolution rate, catalytic
activity [8,10].
The exact mechanisms for antibacterial effect of nanometals are still
being investigated, but there are two more popular proposed possibili-
ties in this regard: (a), free metal ion toxicity arising from dissolution of
the metals from surface of the nanoparticles and (b), oxidative stress via
the generation of reactive oxygen species (ROS) on surfaces of the nano-
particles [11].
Furthermore, morphological and physicochemical characteristics of
the nanometals have been proven to exert an effect on their antimicro-
bial activities [6,12]. It is known that the small nanoparticles have the
strongest bactericidal effect [8,11,13,14]. The positive surface charge of
the metal nanoparticles facilitates their binding to the negatively
charged surface of the bacteria which may result in an enhancement
of the bactericidal effect [6]. The shape of the nanoparticles also influ-
ences their antimicrobial effects [15,16]. In this article, we focused on
the latest findings about antimicrobial activity of the most commonly
employed nanometals and their mechanism of action.
Owing to the promising development and the vast application of
nanoparticles, understanding the nanotoxicity and its outcomes is nec-
essary. For years, pharmaceutical sciences have used nanoparticles to
reduce toxicity and side effects of the drugs; nevertheless, there are
some safety concerns about the nanoparticles. According to the reports,
neurological and respiratory damage, circulatory problems and some
other toxicity effect of nanoparticles are the main concerns in use of
the nanoparticles [17–19]. Indeed, several types of the nanoparticles
appear to be non-toxic and some of them are rendered non-toxic with
beneficial health effects [20]. Appling antimicrobial activity of the
nanoparticles to eradicate bacterial infections could be considered as
one of these valuable health issues.
2. Ag and Ag2O nanoparticles
According to literature Ag nanoparticles are the most popular inor-
ganic nanoparticles used as antimicrobial agents [21]. The antimicrobial
application of Ag additives is widely benefitted in the various injection-
molded plastic products, textiles and coating-based usages [22]. Ag
nanoparticles also possess a range of biomedical applications [2]. It has
been revealed that, Ag nanoparticles show a high antimicrobial activity
comparable with its ionic form [23]. It has also been demonstrated that
Ag nanoparticles are potential antimicrobial agents against drug-
resistant bacteria [1]. According to literature, antibacterial action of Ag
nanoparticles results from damage of the bacterial outer membrane
[24]. Some researchers suppose that, Ag nanoparticles can induce pits
and gaps in the bacterial membrane and then fragment the cell [25,
26]. It has also been known that Ag ions interact with disulfide or sulf-
hydryl groups of enzymes that lead to disruption of metabolic processes
which in turn cause the cell death [22].
Jo et al. investigated the effect of size reduction on the antimicrobial
effect of Ag nanoparticles. They used Ag nanoparticles to control
Bipolaris-sor Okiniana and Magnaporthe Grisea. Similarly, they also eval-
uated the efficacy of Ag nanoparticles on different types of pathogens
279
such as soilborne fungi which rarely produce spores. According to
their results, Ag nanoparticles (20 to 30 nm) could better penetrate
and colonize within the plant tissue. They suggested that, Ag nanoparti-
cles had a great potential for use in controlling spore-producing fungal
plant pathogens. They suggested that these nanoparticles might be
less toxic than synthetic fungicides [23]. In the other study, Mie and
et al. tested the antibacterial activity of their synthesized Ag nanoparti-
cles (19 nm) against eight micro-organisms using the disk diffusion
method. Their results revealed that the Ag nanoparticles showed
potential antibacterial activity against Gram-negative bacteria. Thus,
the authors suggested that these synthesized Ag nanoparticles could
be applied in the pharmaceutical and biomedical industries [27].
Hernández-Sierra et al. reported comparative investigation of the
bactericidal activity of Ag nanoparticles, ZnO, and Au on Streptococcus
mutans (S. mutans). Their results indicated that Ag nanoparticles exhib-
ited the most activity for controlling S. mutans. The authors suggested
that Ag nanoparticles could be used in dental caries since it commonly
is caused by S. mutans [28]. Likewise, Besinis et al. investigated the anti-
bacterial effect of Ag nanoparticles on S. mutans. Their results showed
that the antibacterial effect of Ag nanoparticles against S. mutans was
more superior than that of chlorhexidine [11].
Zarei et al. evaluated antibacterial effect of Ag nanoparticles against
four foodborne pathogens namely Listeria monocytogenes, Escherichia
coli (E. coli), Salmonella typhimurium (S. typhimurium) and Vibrio
parahaemolyticus. According to their results, Ag nanoparticles had great
antibacterial effect on the mentioned pathogens. They concluded that
Ag nanoparticles could be a good alternative for cleaning and disinfection
of equipment and surfaces in the food-related environments [29].
Beside the particle size reduction, shape-dependent properties of
nanoparticles have also been investigated by researchers. Pal et al.
reported the shape dependent antibacterial activity of Ag nanoparticles
(in three different forms: spherical, rod-shaped and truncated tri-
angular). According to their findings, truncated triangular nanoparticles
were more reactive due to their high-atom-density surfaces, and there-
fore showed higher antimicrobial activity [15]. In the other study, Bera
et al. stated the size and shape-dependent antimicrobial activity of fluo-
rescent Ag nanoparticles (1–5 nm) against Gram-positive (Staphylococ-
cus epidermidis and Bacillus megaterium) and Gram-negative bacteria
(Pseudomonas aeruginosa). They emphasized that the shape and size
of the particles controlled their activity. According to these investiga-
tions, the smaller particles easily penetrated the cell wall and showed
the enhanced antimicrobial activity. The authors suggested that these
Ag nanoparticles could be used for different purposes such as clinical
wound dressing, bioadhesives, biofilms and the coating of biomedical
materials [16].
Bahrami prepared Ag–Au alloy nanoparticles to evaluate their
antimicrobial effect against Staphylococcus aureus (S. aureus). The
antibacterial activity of Ag–Au alloy nanoparticles was intensified
when they combined with penicillin G and piperacillin. The authors
suggested that Ag–Au alloy nanoparticles could be used as an adjuvant
in combination therapy of antibiotics [30].
Ag2O nanoparticles have also been discovered to have great antimi-
crobial activity [1]. It is believed that, metal oxide nanoparticles might
be considered as a novel alternative to the most antibiotics [1,31].
Sondi and Salopek-Sondi demonstrated antimicrobial efficacy of Ag2O
nanoparticles against E. coli. They proposed that when E. coli were
exposed to these nanoparticles, DNA lost its replication ability and the
cell cycle halted at the G2/M phase owing to the DNA damage. Then
the cells were affected by oxidative stress, and apoptosis was induced
[32].
Furthermore, Ag had reported to be less toxic than many other dis-
infectants. Marambio-Jones and Hoek had reviewed the antibacterial
mechanisms of the Ag nanoparticles and potential implications for
human health and environment [33]. We think that further research
should be performed to develop Ag compounds, composites and alloys
with the minimum toxicity and maximum antimicrobial effect.
280 S.M. Dizaj et al. / Materials Science and Engineering C 44 (2014) 278–284
3. ZnO nanoparticles
Safety of ZnO and its compatibility with human skin make it a
suitable additive for textiles and surfaces that come in contact with
the human body [34,35]. ZnO nanoparticles showed bactericidal effects
on Gram-positive and Gram-negative bacteria as well as the spores
which are resistant to high temperature and high pressure [36]. The
improved antibacterial activity of ZnO nanoparticles compared to its
microparticles was related to the surface area enhancement in the
nanoparticles [6,37,38]. Padmavathy et al. investigated the antibacterial
activity of ZnO nanoparticles with various particle sizes. Their results
demonstrated that the bactericidal efficacy of ZnO nanoparticles
increased by decreasing particle size [38].
Azam et al. reported comparative investigation of antimicrobial
activity of ZnO, CuO, and Fe2 O 3 nanoparticles against Gram-
negative (E. coli and P. aeruginosa) and Gram-positive (S. aureus
and Bacillus subtilis (B. subtilis)) bacteria. According to their results,
the most bactericidal activity was reported for the ZnO nanoparticles
while Fe2 O3 nanoparticles exhibited the least antibacterial effect
[36].
In particular, ZnO reduces the bacteria viability; however, the exact
mechanism of its antibacterial activity has not been well understood
so far. One proposed possibility is the generation of hydrogen peroxide
as a main factor of the antibacterial activity. It is also believed that, the
accumulation of the particles on the bacteria surface due to the electro-
static forces could be another mechanism of the antibacterial effect of
ZnO particles [39]. Besides, ROS generated on the surface of the parti-
cles, zinc ion release, membrane dysfunction, and nanoparticles inter-
nalization could also be taken into account as the possible reasons of
the cell damage [40]. Moreover, interruption of transmembrane
electron transportation has been stated in the case of some metal nano-
particles such as Ag and Zn [41–43].
Xie et al. evaluated antibacterial activity of ZnO nanoparticles against
Campylobacter jejuni (C. jejuni). They suggested that the antibacterial
mechanism of ZnO nanoparticles might be due to disruption of the
cell membrane and oxidative stress in C. jejuni. Their results signified
that ZnO nanoparticles caused morphological changes, measurable
membrane leakage, and increase (up to 52-fold) in oxidative stress
gene expression in C. jejuni [37].
Ag nanoparticles showed antibacterial activity even in the ultra-low
concentrations [44]; however, the antibacterial activity of ZnO nanopar-
ticles depended on the concentration and surface area. Thus ZnO nano-
particles in higher concentrations and larger surface area displayed
better antibacterial activity [8]. Hossein-khani et al. investigated
the antibacterial characteristics of ZnO nanoparticle against Shigella
dysenteriae. Based on their results, a considerable decrease in the bacte-
ria number was observed as a result of particles size reduction [45].
Emami-Karvani et al. investigated the antimicrobial activity of ZnO
nanoparticles against Gram-negative (E. coli) and Gram-positive
(S. aureus) bacteria. They evaluated the effects of concentration and par-
ticle size reduction on the antibacterial activity of ZnO nanoparticles.
They found that the antibacterial activity of ZnO nanoparticles increased
with decreasing particle size and enhancing powder concentration;
nonetheless, ZnO bulk powder showed no significant antibacterial
activity [46].
Some studies have shown that preparation of metal ion doped nano-
particles can improve antimicrobial properties of metal nanoparticles
[47–49]. Sun et al. synthesized the titanium-doped ZnO powders from
different zinc salts. Their results showed that the titanium doped ZnO
powders had the antibacterial action against E. coli and S. aureus. The
authors emphasized that the antibacterial properties of the titanium-
doped ZnO powders were related to the particle size reduction and
the crystallinity [48].
Moreover, ZnO nanoparticles exhibit high photocatalytic properties
which improve their antimicrobial efficiency [44]. ZnO nanoparticles
produce ROS under UV light as well [50].
4. TiO2 nanoparticles
Antimicrobial property of TiO2 is related to its crystal structure,
shape and size [51]. It is proposed that oxidative stress via the genera-
tion of ROS may be a particularly important mechanism for TiO2
nanoparticles (anatase forms). Then ROS cause site specific DNA
damage [44,52].
Roy et al. evaluated the effect of TiO2 nanoparticles with different
antibiotics against methicillin-resistant S. aureus (MRSA). They reprted
that, TiO2 nanoparticles improved the antimicrobial effect of beta
lactums, cephalosporins, aminoglycosides, glycopeptides, macrolids,
lincosamides and tetracycline against MRSA. In another experiment,
their results showed that antimicrobial resistance of MRSA against
various antibiotics decreased in the presence of TiO2 nanoparticles [52].
Haghighi et al. investigated antifungal effect of TiO2 nanoparticles on
the fungal biofilms (fluconazole resistant standard strains of Candida
albicans (C. albicans)). According to their results, the synthesized TiO2
nanoparticles had improved antifungal effect on the fluconazole
resistant strain of C. albicans biofilms. The authors suggested that TiO2
nanoparticles could effectively inhibit the fungal biofilms especially
those formed on the surface of medical devices [51].
Photocatalytic properties of the TiO2 nanoparticles help them to
efficiently eradicate the bacteria. In fact, TiO2 nanoparticles produce
ROS under UV light. Carré et al. considered that the antibacterial photo-
catalytic activity was accompanied by lipid peroxidation that causes to
enhance membrane fluidity and disrupt the cell integrity [53]. However,
the use of TiO2 nanoparticles under UV light is restricted because of
genetic damage in human cells and tissues [1]. It has been proved
that, doping of TiO2 nanoparticles with metal ions can be a good idea
to overcome this problem. In addition, antibacterial and photocatalytic
properties of TiO2 nanoparticles are significantly enhanced by doping
them with metal ions [1,47]. In other words, doping with metal ions
shifts TiO2 nanoparticles' light absorption range to visible light and
therefore, there is no need to irradiate them with UV light [1].
Conjugation of TiO2 nanoparticles with nontoxic polymers is another
approach to overcome toxicity problems of TiO2 nanoparticles. For
instance, Rafailovich et al. reported that TiO2 nanoparticles–polymer
conjugates were harmless to fibroblast cells [1].
5. Au nanoparticles
Au nanoparticles are considered to be so valuable in the develop-
ment of antibacterial agents due to their nontoxicity, high ability
to functionalization, polyvalent effects, ease of detection and
photothermal activity [54–57]. Although generation of ROS is the
main cause of cellular death for most antibiotics and antibacterial
nanomaterials; nevertheless, antimicrobial activity of Au nanoparticles
do not induce any ROS-related process [58]. Cui et al. proved that anti-
bacterial activity of the Au nanoparticles was attributable to 1) attach-
ment of these nanoparticles to the bacterial membrane followed by
membrane potential modification and ATP level decrease and 2) inhibi-
tion of tRNA binding to the ribosome [58].
Tiwari et al. investigated the antibacterial and antifungal activities
of the Au nanoparticles functionalized with 5-fluorouracil against
Micrococcus luteus, S. aureus, P. aeruginosa, E. coli, Aspergillus fumigates
(A. fumigates), and Aspergillus niger (A. niger). The authors reported
that these nanoparticles showed more activity on Gram negative bacte-
ria than Gram positive ones due to their easier internalization into
the Gram negative bacteria. These nanoparticles indicated antifungal
activity against A. fumigates and A. niger as well [55].
Zhou et al. tested antibacterial activities of Au and Ag nanoparticles
against E. coli and bacillus Calmette-Guérin (BCG). They claimed that,
Au and Ag nanoparticles exhibited significant antibacterial activity
against both Gram negative (E. coli) and the Gram positive bacteria
(BCG). They also functionalized Au nanoparticles with a strongly
bound capping (poly-allylamine hydrochloride) and a weakly bound
 S.M. Dizaj et al. / Materials Science and Engineering C 44 (2014) 278–284
capping agent (citrate). Poly-allylamine hydrochloride could directly
contact with the bacterial cell membrane due to its positively charged
nature [59]. Furthermore, Au nanoparticles functionalized with strongly
bound capping agents could self-assemble into 4–5 μm long chains [60].
Zhou et al. explained that these two mentioned processes facilitate the
delivery of a large number of Au nanoparticles on the bacterial cell
wall. Conversely, extra-aggregation of weakly bound capping agents
like citrate causes reduced surface area and so decreased interactions
with the nanoparticles. Accordingly, Au nanoparticle with the same
shape and size but different capping agent exhibits different antimicro-
bial activities [56].
In another study, Lima et al. reported antimicrobial effect of Au
nanoparticles (5 nm) against E. coli and Salmonella typhi (S. typhi) bacte-
ria. Their results showed that, these nanoparticles reduced 90–95% of
E. coli and S. typhi colonies. The authors emphasized that, the main
factors that influenced the biocidal properties were the roughness and
the dispersion of the Au nanoparticles on the medium [54].
It seems that Au nanoparticles are safer to the mammalian cells than
the other nanometals due to the ROS-independent mechanism of their
antimicrobial activity. Moreover, high ability of these nanoparticles
for functionalization makes them ideal nanomaterials to be applied as
targeted antimicrobial agents.
6. Si and SiO2 nanoparticles
Antimicrobial activity of SiO2 would become more significant at
nano-scale owing to the increased surface area [61]. Cousins et al.
found that Si nanoparticles inhibited bacterial adherence to oral
biofilms [62]. Combination use of Si nanoparticles with the other biocid-
al metals such as Ag has been extensively studied in the recent years.
Egger et al. reported the production and investigation of antimicrobial
activity of novel Ag–Si nanocomposite. Their results revealed better an-
timicrobial effect of the nanocomposite against a wide range of microor-
ganisms compared to conventional materials, such as silver nitrate and
silver zeolite [22]. In the other study, Mukha et al. synthesized Ag/SiO2
and Au/SiO2 nanostructures and investigated their antimicrobial
activity. The results showed that Ag/SiO2 nanocomposites indicated
improved antimicrobial properties against E. coli, S. aureus, and
C. albicans while Au/SiO2 nanocomposites did not show any antibacteri-
al activity against the mentioned microorganisms. The authors sug-
gested that these nanocomposites could be used for water disinfection
and for medical and pharmaceutical applications [63].
Several reports showed that Si nanowires could interface with the
living cells and bacteria interrupting cell functions such as cell differen-
tiation, adhesion and spreading. Lee et al. investigated the antibacterial
activity of Ag nanoparticles–Si nanowires. Their results demonstrated
high antibacterial activity for these nanostructures. They also indicated
that, these nanostructures were biocompatible with the human lung
adenocarcinoma epithelial cell line A549 [13,64].
Fellahi et al. reported the preparation and evaluation of antibacterial
activity of Si nanowire substrates decorated with Ag or Cu nanoparti-
cles. According to the authors, their prepared nanoparticles revealed
strong antibacterial activity against E. coli. Ag decorated Si nanowires
found to be biocompatible with human lung adenocarcinoma epithelial
cell line A549 while Cu decorated Si nanowires showed high cytotoxic-
ity [13].
All of these studies signify that development of Si compounds and
composites especially their nanocomposites together with metals such
as Ag shows great potential on the development of antimicrobial agents.
In addition, non-toxicity of Si nanoparticles offers their use as antimi-
crobial agents in the biomedical applications.
7. MgO and CaO nanoparticles
CaO and MgO indicate strong antibacterial activity related to alkalin-
ity and active oxygen species. It has been verified that the antibacterial
281
mechanism of CaO and MgO nanoparticles is brought about by the gen-
eration of superoxide on the surface of these particles, and also an in-
crease in pH value by the hydration of CaO and MgO with water [65].
According to the reports, MgO nanoparticles damage the cell membrane
and then cause the leakage of intracellular contents which in turn lead
to death of the bacterial cells [66].
Hewitt et al. reported that MgO initiated the sensitivity changes in
E. coli induced by active oxygen [67]. However, Leung et al. described
that strong antibacterial activity of the MgO nanoparticles could be ob-
served in the absence of any ROS production. They declared that the
mechanism of antimicrobial activity might be due to the cell membrane
damage [68].
MgO nanoparticles showed the bactericidal activity against both
Gram-positive and Gram-negative bacteria [69]. Sawai et al. investigat-
ed antibacterial activity of MgO against E. coli or S. aureus. They
suggested that the presence of active oxygen, such as superoxide, on
the surfaces of MgO nanoparticles was one of the primary factors that
affects their antibacterial activity [71].
Jin and He also evaluated antibacterial activities of MgO nanoparti-
cles alone or in combination with other antimicrobials (nisin and ZnO
nanoparticles) against E. coli and Salmonella Stanley. MgO nanoparticles
showed strong bactericidal activity against these pathogens (more than
7 log reductions in bacterial counts). In their work, the antibacterial
activity of MgO nanoparticles was improved as the concentrations of
MgO increased. The authors suggested that MgO nanoparticles alone
or in combination with nisin could be utilized as an effective antibacte-
rial agent to enhance food safety [66].
Jeong et al. investigated the antimicrobial efficiency of CaCO3 nano-
particles. According to their results, CaCO3 converted to CaO as a result
of heat treatment. CaO nanoparticles showed bactericidal activity
against E. coli, S. typhimurium, S. aureus and B. subtilis [70].
Yamamoto et al. examined antibacterial activity of CaCO3/MgO
nanocomposites against Gram-positive (S. aureus) and Gram-negative
(E. coli) bacteria. Their results exhibited superior antibacterial action
against S. aureus than E. coli. According to the authors, the mechanism
of antibacterial effect of CaO and MgO was due to the generation of
superoxide on their surface and also an increase in pH value by the
hydration of CaO and MgO with water [65].
Vidic et al. evaluated antimicrobial activity of mixed nanostructure
of ZnO–MgO. They also compared antimicrobial activity of ZnO–MgO
nanoparticles with pure ZnO and MgO nanoparticles. According to
their findings, ZnO nanocrystals showed the high antimicrobial activity
against both Gram-positive (B. subtilis) and Gram-negative (E. coli).
MgO nanoparticles revealed moderate activity and ZnO–MgO nanopar-
ticles indicated high antibacterial activity against Gram-positive bacte-
ria. Their microscopic analysis showed that B. subtilis cells were
damaged after contact with ZnO–MgO nanoparticles. They suggested
that nanostructured ZnO–MgO could be used as a safe new therapeutic
for bacterial infections [69].
Mentioned results indicated that, MgO and CaO nanoparticles alone
or in combination with other disinfectants show excellent antibacterial
effect. These nanoparticles also are low cost, biocompatible and avail-
able materials. These properties make them promising antibacterial
agent [68]. Researchers suggested that, these materials can be utilized
in environmental preservation as well as in food processing and medical
treatments [72].
8. Cu and CuO nanoparticles
Cu nanoparticles due to their unique biological, chemical and phys-
ical properties, antimicrobial activities as well as the low cost of prepa-
ration are of great interest to the scientists [73–75]. Usman et al.
investigated the antimicrobial activities of Cu-chitosan nanoparticles
(2–350 nm). They evaluated antibacterial and antifungal activities of
these nanoparticles on several microorganisms, including methicillin-
resistant S. aureus, B. subtilis, P. aeruginosa, Salmonella choleraesuis, and
282 S.M. Dizaj et al. / Materials Science and Engineering C 44 (2014) 278–284

Fig. 1. Various mechanisms of antimicrobial activity of the metal nanoparticles.

C. albicans. Their results indicated the high potential of these nanoparti-
cles as antimicrobial agents [74].
However, rapid oxidation of the Cu nanoparticles on exposure to
the air limits their application [74,76]. Mahapatra et al. tested antibacte-
rial activity of CuO nanoparticles against Klebsiella pneumoniae,
P. aeruginosa, Salmonella paratyphi and Shigella strains. According to
their report, these nanoparticles indicated suitable antibacterial activity
against the mentioned bacteria. The authors believed that crossing of
nanoparticles through the bacterial cell membrane and then damaging
the vital enzymes of bacteria were the critical factors that trigger cell
death. They also indicated that these nanoparticles were not cytotoxic
on HeLa cell line [76].
Azam et al. reported size-dependent antibacterial activity of CuO
nanoparticles. They investigated the antibacterial activities of CuO
nanoparticles against two Gram-positive bacteria (S. aureus and
B. subtilis) and two Gram-negative bacteria (Pseudomonas aeruginosa
and E. coli). According to their results, CuO nanoparticles exhibited
inhibitory effects against both groups of the mentioned bacteria. The
authors concluded that bactericidal activity of these nanoparticles
depended on their size, stability, and concentration added to the growth
medium. The authors stated that, the metal nanoparticles restrict bacte-
rial growth via passing through nanometric pores exist on the cellular
membranes of most bacteria [77].
Ahamed et al.'s studies revealed that CuO nanoparticles (23 nm) had
significant antimicrobial activity against various bacterial strains (E. coli,
P. aeruginosa, K. pneumoniae, Enterococcus faecalis, Shigella flexneri,
S. typhimurium, Proteus vulgaris, and S. aureus). Among these pathogens,
E. coli and E. faecalis showed the highest sensitivity to CuO nanoparticles
while K. pneumoniae was almost resistant to these nano formulations
[75].

Table 1
Commonly used nanometals as antimicrobial agent, their mechanisms of action and characteristics.

Type of the Proposed mechanism of antimicrobial action Main characteristics as antimicrobial agent The main factors that influence Reference
nanoparticles antimicrobial activity

Ag nanoparticles Ion release; induction of pits and gaps in the
bacterial membrane; interact with disulfide
or sulfhydryl groups of enzymes that lead to
disruption of metabolic processes.
DNA loses its replication ability and the cell
cycle halts at the G2/M phase owing to the
DNA damage (in the case of Ag2O).
ZnO nanoparticles ROS generation on the surface of the
particles; zinc ion release, membrane
dysfunction; and nanoparticles
internalization into cell.
TiO2 nanoparticles Oxidative stress via the generation of ROS;
lipid peroxidation that cause to enhance
membrane fluidity and disrupt the cell
integrity.
Au nanoparticles Attachment of these nanoparticles to
membrane which change the membrane
potential and then cause the decrease the
ATP level; and inhibition of tRNA binding to
the ribosome
Si nanoparticles Influencing the cell functions such as cell
differentiation, adhesion and spreading.
CuO nanoparticles Crossing of nanoparticles from the bacteria
cell membrane and then damaging the vital
enzymes of bacteria.
MgO and CaO Damaging the cell membrane and then
nanoparticles causing the leakage of intracellular contents
and death of the bacterial cells.
High antimicrobial activity against both Particle size and shape of [8,15,22,25,26]
bacteria and drug-resistant bacteria, particles.
antifungal activity on spore-producing
fungal plant pathogens, high stability,
nontoxicity.
Photocatalytic activity; high stability; Particle size and concentration. [10,34–36,44,50]
bactericidal effects on both Gram-positive
and Gram-negative bacteria; antibacterial
activity against spores which are resistant to
high temperature and high pressure.
Suitable photocatalytic properties; high Crystal structure, shape and size. [1,44,51–53]
stability; effective antifungal for fluconazole
resistant strains.
Nontoxicity, not inducing any ROS-related Roughness and particle size. [54,55,57,58]
process; high ability to functionalization,
polyvalent effects; ease of detection;
photothermal activity.
Non-toxicity; stability. Particle size and shape. [52,61,63,65]
Effective against Gram-positive and Particle size and concentration. [36,75,76]
Gram-negative bacteria; high stability;
antifungal activity.
Effective against both Gram-positive and Particle size, pH and [65–69]
Gram-negative bacteria; high stability; low concentration.
cost; availability.
 S.M. Dizaj et al. / Materials Science and Engineering C 44 (2014) 278–284
As a final point, there are several proposed mechanisms in respect to
antimicrobial activities of the metal nanoparticles. Fig. 1 shows the
different proposed antimicrobial mechanisms of the nanometals. The
common nanometals used as antimicrobial agents together with their
mechanisms of action are summarized in Table 1 as well.
9. Conclusion
Due to ever-increasing microbial resistance to the common disinfec-
tants and antibiotics, numerous studies have been performed to im-
prove antimicrobial strategies. Several valuable studies have been
documented in the field of antibacterial nanoparticles in the recent
years. Application of metal and metal oxide nanoparticles could be con-
sidered as a suitable alternative for some antimicrobial methods. The
antimicrobial nanoparticles could be benefitted in the pharmaceutical
and biomedical industries for sterilization of the medical devices.
These nanostructures could also be directed for preparation of chemical
disinfectants, coating-based applications and food preparation process-
es. Metal nanoparticles (especially metal oxide nanoparticles) show
great antimicrobial effects. Improved effectiveness of the metal oxide
nanoparticles on the resistant strains of microbial pathogens as well as
their heat resistance offer them as potent antimicrobial agents. Howev-
er, application of some of the metal oxide nanoparticles is limited be-
cause of their toxicity at higher concentrations. It has also proposed
that functionalization; ion doping and polymer conjugates of these
nanoparticles could be helpful to decrease the associated toxicity. Final-
ly it may be concluded that, the metal oxide nanoparticles with the min-
imized toxicity possibly will be extensively used in the near future for
eradicating several infectious conditions. We believe that development
of the simple and low cost inorganic antimicrobial agents such as metal
and metal oxide nanoparticles as alternative of traditional antibiotics
might be promising for future of pharmaceutics and medicine.
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