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A review on nano-antimicrobials: Metal nanoparticles, methods and mechanisms

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REVIEW
ARTICLE

A Review on Nano-Antimicrobials: Metal Nanoparticles, Methods, and Mechanisms

Edris Hoseinzadeh1, Pouran Makhdoumi2, Parisa Taha3 , Hooshyar Hossini4*, John Stelling5,
Mohammad Amjad Kamal6,7,8 and Ghulam Md Ashraf 6,*

1
Young Researchers & Elite Club, Hamedan Branch, Islamic Azad University, Hamedan, Iran; 2Student research Committee, De-
partment of Pharmacology and Toxicology, Faculty of Pharmacy, Mashhad University of Medical Sciences, Mashhad, Iran;
3
Department of Nutrition, Health center of Sabarooi, Shahid Beheshti University of Medical Sciences, Tehran, Iran; 4Department of
Environmental Health Engineering, Faculty of Health, Kermanshah University of Medical Sciences, Kermanshah, Iran; 5Co-
Director, WHO Collaborating Centre for Surveillance of Antimicrobial Resistance Brigham and Women’s Hospital, Boston, MA,
USA; 6King Fahd Medical Research Center, King Abdulaziz University, Jeddah, Saudi Arabia; 7Enzymoic; 8. Novel Global Commu-
nity Educational Foundation [Peterlee Place, Hebersham, NSW 2770, Australia]

ARTICLE HISTORY
Received: August 29, 2016
Revised: October 4, 2016
Accepted: November 10, 2016
DOI:
10.2174/13892002176661612011111
46
Abstract: Nanotechnology is a scientific and engineering technology conducted at the Nano-scale, such as in the fields
of compound fabric manufacturing, food processing, agricultural processing, and engineering, as well as in medical
and medicinal application. In recent decade, nanomaterial applications for antimicrobial works have been interested by
many researchers. Available reports show that some of the metal oxide Nanoparticles including; Al2O3, TiO 2, ZnO,
CuO, Co3O4 , In2O 3, MgO, SiO2 , ZrO2, Cr2O 3, Ni2O 3, Mn2O 3, CoO, and Nickel oxide have toxicity toward several mi-
croorganisms and they could successfully kill numerous bacteria. Based on our literature review there are some effec-
tive factors that can influence the ability of nanomaterial in reducing or killing the cells, and there are mechanisms for
nanomaterial against bacteria, which are briefly listed as follows: surface charge of the metal nanomaterial, shape, type
and material, concentration of nanomaterial, dispersion and contact of nanomaterial to the bacterial cell, presence of
active oxygen, liberation of antimicrobial ions, medium components and pH, physicochemical properties, specific
surface-area-to-volume ratios, size, role of growth rate, role of biofilm formation, cell wall of bacteria, and effect of
UV illumination. It can be considered that in the use of nanomaterial as antimicrobial agents, consideration of the
many factors is in principal. Antibacterial resistance to common chemical antibacterial agents can be due to long pro-
duction–consumption cycle, thereby reducing their efficiency, and use of poor quality or fake medicines in undevel-
oped and developing countries. Nanoparticles as antimicrobial agents have become an emerging approach against this
challenge, which can establish an effective nanostructure to deliver the antimicrobial agent for targeting the bacterial
community efficiently; in addition, they are so potent that microbial pathogens cannot develop resistance to them. On
the other hand, most of the metal oxide nanoparticles have no toxicity toward humans at effective concentrations used
to kill bacterial cells, which thus becomes an advantage for using them in a full scale. However, over the present dec-
ade, several studies have suggested that NPs are excellent antibacterial agents, at least at the research level.

Keywords: Nanoparticle, antimicrobial, susceptibility, metal oxide.

INTRODUCTION Infectious diseases caused by bacteria have attracted the atten-

Parallel to the immediate development of human living, the
control of harmful effects of microorganisms has become unavoid-
able. A wide range of microorganisms coexist in a normal balance
with human body and living environments, but a quick and uncon-
trolled fast thriving of microbes can lead to some serious problems.
Several antimicrobial agents have been used for growth inhibition
or killing of microbial population for several years. Some of the
used antimicrobial agents have no effectiveness against microbes
because of microbial resistance to them that result from using them
over time or overdosing. Hence, we need to use new and more ef-
fective antimicrobial agents. With developing nanotechnology that
leads to the production of nanomaterial's, nanoparticles are one of
the most effective agents to resolve the problem of microbial resis-
tance. The present review aimed to further introduce the application
of nanomaterials.
*Address correspondence to these authors at the King Fahd Medical Re-
search Center, King Abdulaziz University, P. O. Box 80216, Jeddah 21589,
Saudi Arabia; Tel: +966593594931; E-mails: ashraf.gm@gmail.com, gash-
raf@kau.edu.sa
Department of Environmental Health Engineering, Faculty of Health, Ker-
manshah University of Medical Sciences, Kermanshah, Iran; Tel:
+989188594084; E-mail: hoo.hosseini@gmail.com
tion of both the general public and professionals at the global level
because of their impact in causing serious health problems, which
ultimately lead to economic and social implications [1, 2].
Outbreaks caused by pathogenic bacteria because of their resis-
tance to common antibacterial agents, lack of suitable and effective
antimicrobial agents, particularly in the undeveloped and developing
countries, and hospital-acquired infections (HAIs) or nosocomial
infections are the most important health issues that demand discover-
ing new and effective antibacterial agents, at a global level [3-5].
Short Comment
A useful way, which has been developed by WHO, to get more
comprehensive information for laboratory-based surveillance of
infectious diseases and antimicrobial resistance is to use WHONET.
By using this free software we can find the resistance bacteria and
use them to study new antibacterial agents.
In general, by the software we can use laboratory data in more
applicable way and use national or, even international data to find
resistant bacteria. WHONET capability can enable:
• The representation of the local epidemiology of microbial
populations;

1389-2002/17 $58.00+.00 © 2017 Bentham Science Publishers

2 Current Drug Metabolism, 2017, Vol. 18, No. 00
• The choice of antimicrobial agents;
• The identification of hospital and community outbreaks; and
• The recognition of quality assurance problems in laboratory
testing.
For more information about the software you can see these
references [6-8].
The past century has witnessed rapid advances in scientific
knowledge and in the development of medicines, health technolo-
gies, and interventions, and individuals who enter healthcare pro-
fessions can dedicate their lives to the alleviation of suffering and
maintenance of life [5]. However, these advances in healthcare
practices pose new infection risks to vulnerable patient populations
[9]. Surgeries and catheters disrupt protective skin surfaces; che-
motherapeutics and immune system suppressors compromise the
host’s immunological system; and prolonged periods of immobili-
zation lead to pneumonia and infected bedsores. Individuals admit-
ted to a hospital for the management of hypertension or diabetes
may die from multidrug-resistant infections acquired in the hospital.
Thus, unfortunately, our efforts to save lives perversely can in-
crease the patient suffering and risk of death through the acquisition
of healthcare-associated infections [5, 10, 11].
There will always be risks associated with medical interven-
tions–surgical wound infections, bloodstream infections, pneumo-
nias, urine infections, and many others. Therefore, it is necessary to
decrease, to whatever degree possible, the likelihood of such com-
plications through sustained attention to evidence-based hygiene
and disease prevention measures, including the sterilization of
medical equipment, decreasing the length of exposure to catheters
and respirators, vigilance to early signs of infections [11].
Antibacterial resistance to common chemical antibacterial
agents can be due to long production–consumption cycle, thereby
reducing their efficiency, and use of poor quality or fake medicines
in undeveloped and developing countries. Nanoparticles (NPs) as
an antimicrobial agent have become the new approach against this
challenge, which can establish an effective nanostructure to deliver
the antimicrobial agent for targeting the bacterial community effi-
ciently; in addition, they are so potent that microbial pathogens
cannot develop resistance to them. However, over the present dec-
ade, several studies have suggested that NPs are excellent antibacte-
rial agents, at least at the research level [2, 3, 12].
Generally, nanotechnology is a scientific and engineering tech-
nology conducted at the nanoscale, i.e., at approximately 1–100 nm,
such as in the fields of compound fabric manufacturing, food proc-
essing, agricultural processing, and engineering, as well as in medi-
cal and medicinal applications [12-14]. By reducing or developing
at the nanometer level, which results in larger surface-area-to-
volume ratio, new properties and functions could be developed in
the material, such as a change in their chemical, mechanical, elec-
trical, structural, morphological, and optical properties, which
would enhance the physicochemical or biological activity, practi-
cality, and possible new phenomena. The functionalities of nano-
materials allow their use in several areas such as biosensors,
nanomedicine, and bio-nanotechnology [13, 15].
To have an effective review research, the target articles were
extracted from Google Scholar, Scopus, Medline, and other aca-
demic databases between the time periods of 1996 and 2016.
Nanotechnology is a scientific and engineering technology con-
ducted at the Nano-scale, such as in the fields of compound fabric
manufacturing, food and agricultural, and engineering, as well as in
medical and medicinal application. In recent decade, nanomaterial
applications for antimicrobial works have been interested by many
researchers. Available reports show that some of the metal oxide
NPs including; Al2O3, TiO2, ZnO, CuO, Co3O4, In2O3, MgO, SiO2,
ZrO2, Cr2O3, Ni2O3, Mn2O3, CoO, and Nickel oxide have toxicity
toward several microorganisms and they could successfully kill
numerous bacteria. Based on our literature review there are some
Hoseinzadeh et al.
effective factors that can influence the ability of nanomaterial in
reducing or killing the cells, and there are mechanisms for nanoma-
terial against bacteria, which are briefly listed as follows: surface
charge of the metal nanomaterial, shape, type and material, concen-
tration of nanomaterial, dispersion and contact of nanomaterial to
the bacterial cell, presence of active oxygen, liberation of antimi-
crobial ions, medium components and pH, physicochemical proper-
ties, specific surface-area-to-volume ratios, size, role of growth
rate, role of biofilm formation, cell wall of bacteria, and effect of
UV illumination. It can be considered that in the use of nanomate-
rial as antimicrobial agents, consideration of the many factors is in
principal. Antibacterial resistance to common chemical antibacterial
agents can be due to long production–consumption cycle, thereby
reducing their efficiency, and use of poor quality or fake medicines
in undeveloped and developing countries. NPs as an antimicrobial
agent have become the new approach against this challenge, which
can establish an effective nanostructure to deliver the antimicrobial
agent for targeting the bacterial community efficiently; in addition,
they are so potent that microbial pathogens cannot develop resis-
tance to them. On the other hand, most of the metal oxides NPs
have no toxicity toward humans at effective concentrations used to
kill bacterial cells, which thus becomes an advantage for using them
in a full scale. However, over the present decade, several studies
have suggested that NPs are excellent antibacterial agents, at least
at the research level.
Although metal NPs have various synthesizing methods, all the
metal NPs show significant crystallinity, high surface area, and
reactive surfaces. In the emerging field of nanotechnology, the goal
is to create nanostructures or nano-arrays with special characteris-
tics with regard to those of bulk or single particle species[14]. Ox-
ide NPs can exhibit unique physical and chemical characteristics
from their limited size and a high density of corner or edge surface
sites. It is believed that metal oxide NPs display antimicrobial ac-
tivities [2]. Available reports show that some of the metal oxides
NPs (e.g., Al2O3, TiO2, ZnO, CuO, Co3O4, In2O3, MgO, SiO2, ZrO2,
Cr2O3, Ni2O3, Mn2O3, CoO, and Nickel Oxide NPs) have toxicity
toward several microorganisms and they could successfully kill
numerous bacteria. Most of the metal oxide NPs have no toxicity
toward humans at effective concentrations used to kill bacterial
cells, which thus becomes an advantage for using them in a full
scale [16]. As seen from Table 1, some nano-antimicrobial agents
that have been investigated by researches are listed.
Based on the proposed antimicrobial mechanisms of NPs and
reported studies, it has been suggested that bacteria are not able to
develop antimicrobial resistance to metal NPs[2, 16]. Using NPs as
antimicrobial agents has the advantages of low cost and simple
preparation, high efficiency, and less time to kill and overcome
microbial resistance in comparison to conventional antimicrobial
agents [3, 4]. However, development of antimicrobial agents using
NPs is considered as the way of the future, which could bring sev-
eral advantages for those who will be using it, nothing is ever fault-
less and there will always be pros and cons to everything. The ad-
vantages and disadvantages of NP antimicrobials can be easily
enumerated, and some of them are mentioned here:
Advantages of NP Antimicrobial Agents
Using NPs against bacterial cells as an antimicrobial agent is a
new and talented approach, which is an effective and low-cost
measure against pathogenic bacterial cells. In brief, the advantages
of NP antimicrobial agents are as follows:

They can be activated by considering the stimulus for the de-
sired condition such as engineered to active stimulus in special
physicochemical conditions, magnetic field, illumination, tem-
perature, and pH values. Therefore, NPs can be useful in acidic
media that reduce the efficiency of conventional chemical an-
timicrobials.
A Review on Nano-Antimicrobials Current Drug Metabolism, 2017, Vol. 18, No. 00 3

Table 1. Some researches on nano-antimicrobial activity.

Reference Remark Target Nano-antimicrobial agent

Lok et al. The antibacterial activities were related to size, and the Escherichia coli (K12 strain, Silver nanoparticle
[17] smaller particles had higher activities. MG1655)

Liu et al. Under similar conditions, GO dispersion shows the highest Escherichia coli four types of graphene-based materials:
[18] antibacterial activity, sequentially followed by rGO, Gt, and graphite (Gt)
GtO.
graphite oxide (GtO)
graphene oxide (GO)
reduced graphene oxide (rGO)

Jiang et al. Titanium oxide showed higher toxicity. Also, toxicity of ZnO Bacillus subtilis, Escherichia nano- and micro-scaled oxide particles
[19] was the most toxic rather than Al2O3 , SiO2 , causing 100% coli and Pseudomonas fluo- aluminum (Al2O3)
mortality to the three tested bacteria. Al2O3 nanoparticles had rescens
silicon (SiO2)
a mortality rate of 57% to B. subtilis, 36% to E. coli, and
70% to P. fuorescens. SiO2 nanoparticles killed 40% of B. titanium (TiO2)
subtilis, 58% of E. coli, and 70% of P. fluorescens. zinc oxides (ZnO)

Chen et al. Antibacterial results showed that the presence of the TiO2 Gram-negative Escherichia M@TiO2 nanocomposites
[20] matrix enhances the antibacterial effect of silver nanoparti- coli (M = Ag, Pd, Au, Pt)
cles, and the growth of E. coli can be completely inhibited.

Rajendra In order to produce antimicrobial textiles, Zinc oxide Staphylococcus aureus Zinc oxide nanoparticles
et al. [21] nanoparticle was used. The results represented that the fin-
ished fabric demonstrated significant antibacterial activity
against S. aureus.

Kuang et al. The result demonstrated the good antimicrobial activity of Gram-negative Escherichia Nano- Cerium Oxide
[22] cerium oxide. coli

Li et al. [23] The magnesium oxide nano-composite showed the special - Nano-composite MgO
antibacterial activity compared with other antibacterial
materials.

Srivastava It was found that exposure to AgNPs or far lower levels of keratinocyte cell model Silver Nanoparticles (AgNPs)
et al. [24] Ag ions led to a dose-dependent inhibition of selenium me- (HaCat) and a lung cell
tabolism in both cell models. model (A549)

Singh et al. It was demonstrated that the sophorolipid capped Ag Gram-positive and Gram- sophorolipid reduced/capped silver
[25] nanoparticles can be highly potent antibacterial agents for negative bacteria nanoparticles
both Gram-positive and -negative bacteria.

Masoumbaigi Disk diffusion, minimum inhibitory concentration (MIC), Escherichia coli ZnO nanoparticle
et al. [26] and minimum bactericidal concentration (MBC) tests sug-
gested that ZnO nanoparticle could be used as to water-
control systems.

Makhluf The result demonstrated the good antimicrobial activity. Escherichia coli (Gram Nanocrystalline MgO
et al. [27] negative) and Staphylococ-
cus aureus (Gram positive)

NPs can easily penetrate into the bacterial cell. NPs are small
with varying sizes and made of different materials; therefore,
suitable NPs can be selected that could pass through cell barri-
ers and result in disruption of the cell.

Side effects of their use can be minimized because of flexible
physico-chemical properties of NPs.

NP antimicrobials with different mechanisms against bacteria
are capable of overcoming resistance to convention ones. An-
timicrobial resistance may be the result of change or inactiva-
tion of the antimicrobial agent by the bacteria, change of the
special site of the antibiotic, alteration of a metabolic pathway
to avoid the disruptive effect of the antimicrobial agent, and
reduced accumulation of the antimicrobial agent by minimiz-
ing its entry or maximizing clearance from the cell. However,
few microbes have the ability to reduce uptake (such as
Cupriavidus metallidurans CH34 against TiO2 and Al2O3 NPs)
or increase efflux of NPs (e.g., Shewanella oneidensis by pro-
ducing extracellular polymeric substances against Cu NPs) that
result in resistance against them.
Disadvantages of NP Antimicrobials
Although NPs antimicrobials have several advantages and ad-
vances in controlling pathogenic bacteria, there are probable chal-
lenges in using this antimicrobial agent for formal use and some of
them are as follows:
4 Current Drug Metabolism, 2017, Vol. 18, No. 00
• Unknown health effects of liberated NPs as a result of their use
and harmful impact of NPs on cells, tissues, and organs.
• Toxicity of NPs against untargeted microorganisms.
• NPs are stable and could be accumulated in the environment.
They may be spread through air or water and cause several
health problems. Thus, comprehensive laboratory testing is
warranted before using them.
• Agglomeration of NPs due to which the size could be changed.
It is known that small NPs have the strongest bactericidal ef-
fect. On the other hand, the antimicrobial potential of NPs is
size dependent.
The present review aimed to more introduce the Nanomaterial
application for antimicrobial works and more about metal NPs,
their methods and mechanisms.
EFFECTIVE FACTORS OF NP ANTIMICROBIALS
AGAINST BACTERIA
There are some effective factors that can influence the ability of
NPs in reducing or killing the cells, and there are mechanisms for
NPs against bacteria, which are briefly listed as follows:
Surface Charge of the Metal NPs
NPs easily bind to the bacterial cell wall with a negative charge,
and promote penetration into the membrane, which can result in
enhancing NP uptake or attraction toward bacteria that conse-
quently leads to more effectiveness [28-33]. On the other hand,
accumulation of the particles on the bacterial surface occurs due to
electrostatic force. Zeta potential, along with particle size and
chemistry, can be considered as a highly relevant parameter con-
trolling antimicrobial effects. Although Gram-positive (GP) and
Gram-negative (GN) bacteria have differences in their membrane
structure, most of them have a negative charge. The GN bacteria
have a major outer surface membrane components namely
lipopolysaccharide followed by a thin layer of peptidoglycan [34,
35]. In addition, the cell wall in GP bacteria is primarily composed
of a thick layer of peptidoglycan. It has been proved that the cellu-
lar membrane of bacteria has a negative charge due to the presence
of carboxyl, phosphate, and amino groups. Hence, the repulsion
between bacteria and negatively charged NPs could be resulted
from the formation of an electrostatic barrier due to reducing the
interaction between the NPs and bacteria. With a reduction in the
magnitude of the negatively charged NPs, the antibacterial activity
will increase [3, 28, 32, 33]. In addition, the attraction of positively
charged NPs to sulfur- and phosphorus-containing proteins of bac-
teria could be another factor for the dissimilar antibacterial effec-
tiveness of NPs with different surface charges. Surface charge of
NPs can be determined by zeta potential analysis using a zeta po-
tential analyzer or pHZPC test. This attraction probably overcomes
other factors, such as the size and shape that can influence the bac-
terial cell death.
In order to determine pHZPC, the equilibrium technique was
applied in a batch system [3, 36]. This technique is based on the
estimation of H+ and OH
, which are the ions determining the elec-
tric potentials. About 0.1 g of the NP was mixed in the incubator
machine with 20 mL of KNO3 solution in a sealed container for 24
h. Primary pH values were adjusted using 0.1 M KOH and HNO3 in
the pH range of 2–12. The final pH of the each NPs slurry was
measured using the pH meter and their amounts were drawn in the
primary pH. They are given as pH values of filtered solutions after
equilibration (pHf) with the NP as a function of initial pH values
(pHi) of the solution.
The cytoplasm, a jelly-like fluid that fills a cell, includes all the
cellular components except the nucleus. The functions of this or-
ganelle include growth, metabolism, and replication. Consequently,
the cytoplasm contains proteins, nucleic acids, carbohydrates, ions,
Hoseinzadeh et al.
salts and water (approximately 80%). This composition contributes
to the electrical conductivity of the cellular structure.
Surface modification and functionalization are other factors
leading to potential changes in NP antimicrobial activity [37, 38].
Some functionalization can increase the presence of oxygen atoms
on NP surface that can lead to more reactive oxygen species (ROS)
production in the medium. Releasing ions from NPs as a result of
NP modification is possible, which consequently increases NP an-
timicrobial activity through ion toxicity mechanism. In addition, NP
modification can lead to increase of the surface area, and thus it is
increases the surface-area-to-volume ratio that results in increasing
the NP antimicrobial potential. Coating NPs is one of the modifica-
tion approaches, which may be lead to the presence of more toxic
agents or enhances one of the antimicrobial mechanisms of NPs,
and also induces surface defects (such as vacancy defects) in the
NPs. The mechanical damage on the cell wall results from defects
in the corners, edges, and chemistry of NPs. With regard to antimi-
crobial test, NPs are investigated in a medium that contains water,
and most NPs have very low solubility in water that is polar,
wherein NP agglomeration or settling may occur [3]. In general, NP
agglomeration, precipitation, and non-solubility are the challenges
that need to be overcome to use them as additives. These challenges
may have reductive effects on NP antimicrobial activity.
Shape of NPs
Numerous reports have shown that the antimicrobial potential is
under the influence of the shape of NPs [39-41]. Controlling NP
shape can be facilitated by the synthesizing method, controlling
used solvents and concentration, polymers, and bio-molecules, as
well as small molecules such as adsorbed gas, and even atomic
species, such as different metal ions, precursor natures, tempera-
ture, and pH of preparation condition. The shape of NP may be the
result of high atom density (e.g., 111 for nano ZnO) [3]. Different
forms of NP such as spherical, rod-shaped, truncated triangular,
nanotubes, nanorods, nanowires, nanosphere, nanoneedles, and
nanorings have been investigated by researchers [42, 43]. Gener-
ally, reported studies have revealed the shape-dependent antimicro-
bial properties of NPs. Each nanostructure has specific structural,
optical, electrical, and physicochemical properties, permitting re-
markable applications. Each morphology accounts for a certain
mechanism of action. These different morphologies display pro-
nounced antibacterial effect toward the targeted bacteria. In the
oxide form of metallic NPs (such as ZnO), the O:metal ratio on the
surface of NPs can effect ROS generation, which is under the influ-
ence of the amount of oxygen atoms on the NP surface and also
dependent on the shape of NPs [3].
Type and Material of NPs
The kind of materials used for preparing the NPs is one of im-
portant parameters that affect the resultant antimicrobial effective-
ness. The toxicity of parent heavy metals of metal oxide NPs can
have a high impact on their antimicrobial activity [2]. Each mecha-
nism is predominant by the type of NPs. For example, Ag NP can
disrupt bacteria as a result of outer membrane damage. In addition,
killing of the bacterial cell is possible due to disruption of metabolic
processes, which is caused by interaction of released Ag ion with
disulfide or sulfhydryl groups of enzymes. While in the case of
ZnO NPs, ROS generation on the surface of the particles, zinc ion
release, membrane dysfunction, NP internalization, and surface
charge of NPs are the primary routes of ZnO NP interaction with
bacteria cells [4, 34]. In addition, the antibacterial activity of Au
NPs is due to binding of NPs to the outer membrane of the bacterial
cell, which results in ATP decrease, as well as inhibition of tRNA
binding to the ribosome [42].
Concentration of NPs
NPs in higher concentrations display better antibacterial activ-
ity. It may be related to the dysfunction of mitochondria, increased
A Review on Nano-Antimicrobials
lactate dehydrogenase leakage from the cell, and excessive NP
effect on same bacterial populations [3, 34, 37]. In addition, higher
NP concentrations imply the higher surface area, which result in
potential NP antimicrobial activity, as mentioned earlier. Generally,
different NP concentrations contribute to the variation in antimicro-
bial results.
Dispersion and Contact of NPs to the Bacterial Cell
One of the primary factors that influence the biocidal properties
of NPs is the dispersion of the NP on/into the medium, as well as
being in contact with bacteria. NPs by contacting with bacteria can
cause cell wall disruption by internalizing bacteria that can lead to
inhibition of energy metabolism. Direct contact of ZnO-NPs with
cell walls results in destruction of bacterial cell integrity [3, 34, 37].
The physical presence of a NP most likely disrupts cell membranes
in a dose-dependent manner. In this way, NPs assemble in the cyto-
plasmic zone or in the periplasmic space, thus disrupting the cellu-
lar activities and resulting in membrane disturbance and disorder.
Presence of Active Oxygen
One of the other effectiveness factors for the antibacterial activ-
ity is the presence of active oxygen on the surface of NPs. Some
NPs such as CaO and MgO have superoxide on their surface due to
hydration with water content of the medium[2, 16].
Reactive oxygen species (ROS) is highly reactive and oxidiz-
ing, which leads to toxicity to bacteria. One of the possible mecha-
nisms reported in several studies for the NP antibacterial activities
of various metal oxides is ROS generation [42, 43]. By internaliz-
ing ROS species into the bacterial cells, destructive effects on cellu-
lar components (lipids, DNA, proteins, etc.) can occur. In addition,
autoxidation of NADH dehydrogenase II in the respiratory system
may occur as a result of ROSs. It may be due to peroxidation of the
polyunsaturated phospholipid constituent of the lipid membrane.
Superoxide anion (O22
), hydrogen peroxide (H2O2), and hydroxide
(OH
) are some common ROS species that are located on NPs.
ROS and the other mechanisms of antimicrobial activity of the
metal NPs is shown in Fig. (1). Accordingly, it has been found that
the ROS is one of the main bactericides mechanisms.
Fig. (1). ROS and other mechanisms of antimicrobial activity of the metal NPs [2].
Current Drug Metabolism, 2017, Vol. 18, No. 00 5
•
OH and •O2
have negative charges that repulse interaction with the
bacteria cell wall that cannot penetrate into the membrane.
O2 (presence in medium containing NPs and bacteria) =>•O2

•
O2
+ H+ => HO•2
HO•2 + e =>•HO2
•
HO2 + H+ => H2O2 locates on NP surface that has in relation with
the available NP surface => NPs with a small size or high surface-
area-to-volume ratio have increased ability to produce H2O2. Under
light, especially under UV illumination, H2O2 production is en-
hanced.
H2O2 + enter into bacterial cell membrane => damage or kill the
bacteria
Liberation of Antimicrobial Ions
Liberating/releasing ions from NPs in a liquid medium contain-
ing bacteria is an important factor to increase the antibacterial activ-
ity of NPs. It may be related to the inhibition of transportation in
the bacterial cell membrane, as well as dysfunction or poisoning of
amino acids and consequently the enzyme system [3, 37]. On the
other hand, NPs with low-ion realization can lead to bacterial resis-
tance to the ions, and hence determination of the released ions from
used NPs in all antimicrobial studies of NPs is a necessity. Besides
releasing ions, ion species and the ion with the medium origin are
also very important. Several researchers have believed that stabi-
lized or insoluble NPs have limited antimicrobial ability because of
no or low releasing ions into the medium. The pH of medium is an
effective factor than can facilitate the release of ions from NPs. Ion
releasing from NPs enhances in an acidic environment. Some stud-
ies such as that by Peng et al. have shown that release of ions from
NPs is morphology dependent. They concluded that release of Zn2+
6 Current Drug Metabolism, 2017, Vol. 18, No. 00
ions from spherical ZnO-NPs is higher than that from rod-shaped
ZnO-NPs because of high equilibrium solubility.
Medium Components and pH
Available studies show that the pH of medium can influence the
structure of NPs and result in antimicrobial activity. It is believed
that as the pH decreases to acidic range, the releasing ions from
NPs as well as amino acids and peptides from bacteria increase due
to dissolving NPs and consequently the antimicrobial potential of
NPs will be enhanced. Unlike in alkaline pH, the antimicrobial
potential of NPs decrease; the opposite is also true, i.e., with chang-
ing pH from neutral to alkaline, the bacteriostatic activity becomes
better due to changing of NP morphology. It may be because the pH
shifting of the medium has no considerable effect on the antimicro-
bial potential of NPs, but by influencing other effective parameters
of both NPs and biological components, it leads to alteration of NP
antimicrobial activity indirectly. In addition, because of the pres-
ence of negative charge of the bacterial cell wall, attraction of NPs
with a positive charge on bacteria is electrostatic. The pH of a solu-
tion represents the concentration of hydrogen ions, and thus by
changing the pH, the surface charge of NPs will be changed.
Physicochemical Properties
Porosity, morphology, concentration, particle size, temperature,
aeration, and pH are important factors. Temperature, aeration, and
pH of medium containing NPs and bacteria can influence NP ag-
glomeration. In this way, high temperature, aeration at high level,
and decreasing the pH of medium can lead to increase in the NP
antibacterial activity. Agglomerated NPs have low surface area that,
including other related mechanisms, leads to lower antimicrobial
activity.
Specific Surface-Area-to-Volume Ratios
It is known that most of the reactions take place at the surface
of solid materials; in this context, a greater reactivity results from
more available surface area. Larger surface-area-to-volume ratio is
obtained by lowering the size. Higher surface-area-to-volume ratio
because of more available sites in a volume leads to faster perform-
ance of the reaction with more intensity. It should be noted that
concentration, modification, coating, and roughness of NPs can
influence the surface-area-to-volume ratio. Generation of H2O2 and
ROS occurs on the NP surface and their amount is surface area
dependent.
Size of NPs
NP size has a considerable effect on the NPs used as an antimi-
crobial agent. Small NPs (<30 nm) appear to be the most capable of
penetration into bacterial cell bodies. Interference with cell mem-
branes, and the subsequent loss of cell viability, is attributed to
nearly all varieties of NPs, particularly those with a small diameter
and positive zeta potential. Smaller particles are found to have
greater antibacterial activity and are shown to have two benefits:
i They can easily reach the nuclear content of bacteria due to the
structure of the bacterial cell wall, especially in GN ones.
ii They can provide a greater surface area and therefore stronger
bactericidal interactions. Some studies revealed that NPs
greater than 10 nm accumulate on the cellular surface and
compromise cellular permeability; however, NPs <10 nm
penetrate into the bacteria, disturbing the DNA and enzymes,
and consequently leading to cellular death.
Role of Growth Rate
Bacterial growth rate is another factor that affects the antimi-
crobial activity of NPs. In planktonic cultures and biofilms with an
increasing growth rate, susceptibility to antimicrobial agent in-
creases. In biofilms due to slow growth rate of bacteria, resistance
mechanisms against NPs and other antimicrobial agent develop.
Hoseinzadeh et al.
When the growth and dying rates are equal, i.e., in stationary phase,
susceptibility to NPs is minimum. Furthermore, slow-growing bac-
teria with tolerance ability (due to expression of stress-response
genes) against NPs are more resistant than fast-growing ones. How-
ever, the nature of different qualitative NPs can lead to reverse
results. Until now, in many cases, the relation between NP suscep-
tibility and bacterial physiology is uncertain. It is possible that NPs
with irreversible binding have more toxicity in slow-growing bacte-
ria, whereas fast-growing bacteria have high susceptibility to NPs
with reversible binding. An antibacterial agent is considered as
bactericidal if it kills the bacteria or as bacteriostatic if it inhibits
their growth.
Role of Biofilm Formation
Some bacteria are able to form biofilm with resistance against
the antimicrobial agent such as NPs. A biofilm is an accumulation
of surface-attached microbial cells that are placed in an extracellu-
lar polymeric substance matrix. Biofilms can be formed by a single
bacterial species, although biofilms more often consist of many
species of bacteria, as well as algae, fungi, protozoa, corrosion
products, and debris. Essentially, a biofilm may form onto the each
surface exposed to bacteria when some amount of water is existed.
In chronic infection, the biofilm formation is a considerable prob-
lem because the bacteria in the biofilm would be protected against
antimicrobial agents. Effectiveness of antibacterial activity of NPs
on the biofilm depends on NPs attracting to the biofilm, which is
performed electrostatically. Electrostatic attraction of NPs on bacte-
ria has been discussed in the former section. By up taking NPs on
the biofilm, new cell formation on the biofilm is inhibited because
of toxic effects of NPs on bacteria, and biofilm presence will be
depleted or resistance ability develops.
Cell Wall of Bacteria
The shape of bacteria, rigidity of the bacterial cell wall, ruptur-
ing of cell membrane as a result of osmotic or mechanical pressure
are dependent on the bacterial cell wall. One of the methods of
bacterial classification based on structural differences in their cell
walls is the Gram staining technique (developed by the Danish
scientist Hans Christian Gram) [44]. GP (+) and GN (
) are two
classes of Gram division.
In Gram’s test, GP bacteria that have of a thick layer of 20–50
nm peptidoglycan can hold the crystal violet dye, while GN cell
walls with more complexity do not hold the violet dye and the re-
sult of staining is red or pink color. Comparison of the characteris-
tics of GP and GN bacteria is briefly presented in Table 2.
In general, including NPs, the structure of the bacterial cell wall
is one of the primary causes of resistance or susceptibility of bacte-
ria to NPs. It is believed that peptidoglycan is able to pass through
the NPs because of the small size. Because of the presence of
lipopolysaccharides, the negative charge on GN bacteria enhances;
therefore, the effect of surface charge (both bacteria and NPs)
would be a limiting factor of NP effect on the bacteria. Addition-
ally, diffusion of NPs inside the biofilm matrix is affected by the
bacterial cell wall. For example, the GN bacteria have resistance to
hydrophobic antimicrobial agents. However, bacterial susceptibility
to NPs is not related solely to bacteria cell wall. It may be affected
by factors related to NPs (such as NP type), resulting in increase or
decrease of the antimicrobial potential. It should be noted that the
anchored cell wall proteinase PrtP on the microbial surface can alter
the physico-chemical properties of the bacterial cell wall and result
in hydrophilic to an extremely hydrophobic characteristic. It can be
decreased by attracting NPs onto the cell wall or vice versa. Based
on the available results on the antimicrobial NPs, the GN bacteria
are resistant to ZnO-NPs in comparison with the GP ones, while Ag
NPs have better effectiveness against GN bacteria.
A Review on Nano-Antimicrobials Current Drug Metabolism, 2017, Vol. 18, No. 00 7

Table 2. Comparison of GP and GN bacteria.

Characteristic GN bacteria GP bacteria

Gram staining Because of taking counter stain (Safranin or Fuchsine), they In normal Gram staining, the crystal violet dye and dark
protocol result are able to decolorize; if they are washed with absolute alco- violet or purple stain remain, while as a result of washing
hol and acetone, the Gram staining has no result, otherwise with absolute alcohol and water, their staining result is blue
the staining result is red or pink color. or purple color.

Peptidoglycan layer Thin (single-layered) Thick (multilayered)

Teichoic acids Lacking Present in many

Periplasmic space Present Lacking

Outer membrane Present Lacking

Lipopolysaccharide High Virtually none

(LPS) content

Lipid and lipoprotein High (due to presence of outer membrane) Low (acid-fast bacteria have lipids linked to peptidoglycan)
content

Flagellar structure 4 rings in basal body 2 rings in basal body

Toxins produced Primarily endotoxins Primarily exotoxins

Resistance to physical Low High

disruption

Inhibition by basic dyes Low High

Susceptibility to anionic Low High

detergents

Resistance to sodium Low High

azide

Resistance to drying Low High

Cell wall composition The cell wall is 70–120 Angstrom units thick, two-layered. The cell wall is 100–120 Angstrom units thick, single-
The lipid content is 20–30% (High), whereas the murein layered. The lipid content of the cell wall is low, whereas
content is 10–20% (Low). murein content is 70–80% (Higher).

Mesosome Mesosome is less prominent. Mesosome is more prominent.

Antibiotic resistance More resistant to antibiotics. More susceptible to antibiotics

terial resistance to common chemical antibacterial agents can be

Effect of UV Illumination
Some NPs such as ZnO have high photocatalytic activity, and
their electrical conductivity increases due to UV absorbance [41,
45, 46]. Better conductivity property of NPs can enhance the elec-
trostatic attraction of NPs to bacteria. In addition, due to interaction
of UV with H2O molecules, it is assumed that O2
and O22
are
produced and are left on the NP surface and can enhance the ROS
mechanism. Metallic NPs by receiving photons with enough energy
to move electrons from the valence band to the conduction band
will be induced [47]. Electron transfer between the bands leads to
photoreactions, including holes with a positive charge creation.
These holes with the following three pathways can increase the NP
antimicrobial activity [41, 45, 46]:
1). Direct oxidation of bacteria
2). Formation of reactive OH•
3). H2O2 production
CONCLUSION
It can be considered that in the use of nanomaterial as antimi-
crobial agents, consideration to many factor is in principal. Antibac-
due to long production–consumption cycle, thereby reducing their
efficiency, and use of poor quality or fake medicines in undevel-
oped and developing countries. NPs as an antimicrobial agent have
become the new approach against this challenge, which can estab-
lish an effective nanostructure to deliver the antimicrobial agent for
targeting the bacterial community efficiently; in addition, they are
so potent that microbial pathogens cannot develop resistance to
them. On the other hand, most of the metal oxides NPs have no
toxicity toward humans at effective concentrations used to kill bac-
terial cells, which thus becomes an advantage for using them in a
full scale. However, over the present decade, several studies have
suggested that NPs are excellent antibacterial agents, at least at the
research level.
CONFLICT OF INTEREST
The authors confirm that this article content has no conflict of
interest.
ACKNOWLEDGEMENTS
The authors acknowledge all non-financial supports provided
by Kermanshah University of Medical Sciences. Ghulam Md Ash-
8 Current Drug Metabolism, 2017, Vol. 18, No. 00
raf gratefully acknowledges the facilities provided by King Fahd
Medical Research Center (KFMRC) and Deanship of Scientific
Research (DSR), King Abdulaziz University, Jeddah, Saudi Arabia.
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