J Nanopart Res (2011) 13:6877–6885
DOI 10.1007/s11051-011-0595-5
RESEARCH PAPER
Antibacterial activities of magnesium oxide (MgO)
nanoparticles against foodborne pathogens
Tony Jin • Yiping He
Received: 5 April 2011 / Accepted: 27 September 2011 / Published online: 15 October 2011
Ó Springer Science+Business Media B.V. (outside the USA) 2011
Abstract The antibacterial activities of magnesium
oxide nanoparticles (MgO NP) alone or in combina-
tion with other antimicrobials (nisin and ZnO NP)
against Escherichia coli O157:H7 and Salmonella
Stanley were investigated. The results show that MgO
NP have strong bactericidal activity against the
pathogens, achieving more than 7 log reductions in
bacterial counts. The antibacterial activity of MgO NP
increased as the concentrations of MgO increased. A
synergistic effect of MgO in combination with nisin
was observed as well. However, the addition of ZnO
NP to MgO NP did not enhance the antibacterial
activity of MgO against both pathogens. Scanning
electron microscopy was used to characterize the
Mention of trade names or commercial products in this article
is solely for the purpose of providing specific information and
does not imply recommendation or endorsement by the U.S.
Department of Agriculture. USDA is an equal opportunity
provider and employer.
T. Jin (&)
Residue Chemistry and Predictive Microbiology Research
Unit, U.S. Department of Agriculture, Agricultural
Research Service, Eastern Regional Research Center,
600 East Mermaid Lane, Wyndmoor, PA 19038, USA
e-mail: tony.jin@ars.usda.gov
Y. He
Molecular Characterization of Foodborne Pathogens
Research Unit, U.S. Department of Agriculture,
Agricultural Research Service, Eastern Regional Research
Center, 600 East Mermaid Lane, Wyndmoor, PA 19038,
USA
morphological changes of E. coli O157:H7 before and
after antimicrobial treatments. It was revealed that
MgO NP treatments distort and damage the cell
membrane, resulting in a leakage of intracellular
contents and eventually the death of bacterial cells.
These results suggest that MgO NP alone or in
combination with nisin could potentially be used as an
effective antibacterial agent to enhance food safety.
Keywords Magnesium oxide
Nanoparticles

Foodborne pathogens
Antibacterial activity

Environmental and health effects
Introduction
Outbreaks of foodborne pathogens continue to draw
public attention to food safety. The Center for Disease
Control and Prevention (CDC, Atlanta GA) estimates
that approximately 48 million cases of foodborne
diseases occur in the United States, and there are
127,839 hospitalizations and 3,037 deaths related to
foodborne diseases each year (Morris 2011). The most
commonly recognized foodborne infections are those
caused by enteric bacteria including Salmonella and
Escherichia coli O157: H7. Therefore, there is a need
to develop effective antimicrobials to ensure food
safety and extend shelf-life.
In recent years, the use of inorganic antimicrobial
agents in non food applications has attracted much
interest for the control of microorganisms (Okouchi
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et al. 1995; Wilczynski 2000). The key advantages of
inorganic antimicrobial agents, as compared to their
organic counterparts, are the improved safety and
stability under high temperature treatments (Wang
et al. 1998; Hewitt et al. 2001; Fu et al. 2005; Makhluf
et al. 2005). Presently, some of the common antibac-
terial inorganic materials are TiO2 (Shirashi et al.
1999; Huang et al. 2000) and ceramics immobilized
antimicrobial metals, such as silver and copper
(Kourai 1993; Wang et al. 1995). Sawai et al. (1995,
1998, 1999, 2000) evaluated the antibacterial activity
of 26 ceramic powders, and found that MgO, CaO and
ZnO exhibited strong antibacterial activities. Antibac-
terial activities of metal oxide (ZnO, MgO and CaO)
powders against Staphylococcus aureus, E. coli or
fungi were quantitatively evaluated in culture media as
well (Sawai 2003; Sawai and Yoshikawa 2004).
The size of metallic nanoparticles ensures that a
significantly large surface area of the particles is in
contact with the bacterial effluent. Considering a
hypothetical case with spherical particles of uniform
size, a reduction in the particle size from 10 lm to
10 nm will increase the contact surface area by 109. As
the size of a particle decreases, its surface area
increases and also allows a greater proportion of its
atoms or molecules to be displayed on the surface
rather than the interior of the material (Nel et al. 2006).
The increase in surface area determines the potential
number of reactive groups on the particle surface,
which is expected to enhance the extent of bacterial
elimination (Pal et al. 2007).
Nanoparticles made from metal oxides with sizes
less than 100 nm exhibit significantly enhanced anti-
microbial activities due to their special characteristics
(e.g. small particle size, large surface area) that micro-
or macro-sized particles do not possess. Yamamoto
(2001) and Huang et al. (2005) reported that antibac-
terial activity increased with a decrease in particle size
of the oxide ceramic. The size-dependent interaction
of silver nanoparticles with gram-negative bacteria
has also been reported by Morones et al. (2005).
Stoimenov et al. (2002) prepared nano-scale MgO
powder, which showed a pronounced bactericidal
action against vegetative cells and spores of bacteria.
Koper et al. (2002) found that the nano-scale MgO
powder possessing active forms of halogens inacti-
vated viruses and aflatoxins. Several researchers (Jin
et al. 2009c, d; Liu et al. 2009; Xie et al. 2011)
demonstrated the antibacterial activities of ZnO NP
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J Nanopart Res (2011) 13:6877–6885
against food borne pathogens. However, there are few
reports on the antimicrobial activity of MgO NP in the
literature describing the use of MgO NP alone or in
combination with other antimicrobials to kill or inhibit
the growth of foodborne pathogens (Shi et al. 2010).
Nisin is a 35-amino acid cationic peptide bacterio-
cin (naturally occurring antimicrobial peptide) pro-
duced as a fermentation byproduct by certain strains of
Lactococcus lactis (Chandrapati and O’Sullivan
1998). Nisin alone or in combination with other
antimicrobial agents such as organic acids and chela-
tors against various microorganisms has been exten-
sively studied, and it can be used directly in foods, or it
can be incorporated into food packaging materials and
then released onto foods (Al-Holy et al. 2006; Fang
and Tsai 2003; Jin and Zhang 2008; Jin 2010; Jin and
Gurtler 2011; Jin et al. 2009a, b, 2010; Dawson et al.
2002; Liu et al. 2010; McCormick et al. 2005; Millette
et al. 2007; Sheldon 2001; Ukuku and Fett 2004).
However, few studies have been reported on the use of
nisin in combination with MgO NP.
The objective of this study was to investigate the
antibacterial activities of MgO NP and its synergistic
effect in combination with other antimicrobials (ZnO
NP and nisin) against foodborne pathogens (E. coli
O157:H7 and Salmonella Stanley). The results of this
study are expected to gather sufficient knowledge to
develop new antimicrobial strategies on food products.
Materials and methods
Materials
MgO nanoparticles (average particle size: 20 nm) and
ZnO nanoparticles (average particle size: 20 nm) were
from Nanostructured & Amorphous Materials, Inc.
(Houston, TX). Nisin (2.5% purity) was purchased
from Sigma Chemical Co. (St. Louis, MO).
Cultures
Escherichia coli O157:H7 Oklahoma and Salmonella
Stanley H0558 were obtained from the culture
collection of the U.S. Department of Agriculture,
Agricultural Research Service, Eastern Regional
Research Center. Prior to the inoculum preparation,
E. coli O157:H7 and S. Stanley cells were grown in
tryptic soy broth (TSB) (Remel, Inc., Lenexa, KS)
J Nanopart Res (2011) 13:6877–6885
aerobically at 37 °C for 16–18 h. A 10 lL loop
transfer was performed and the strains were grown at
37 °C for another 24 h to achieve a population of ca.
9 log CFU mL-1. Serial tenfold dilutions were per-
formed in sterile 0.1% peptone water and inoculated
into TSB so as to achieve target populations of ca. 4
and 8 log CFU mL-1, respectively.
Antibacterial challenge test
Predetermined amounts of MgO NP, nisin, or ZnO NP
were accurately weighed and dispersed in glass tubes
containing 10 mL of TSB inoculated with overnight
cultures of E. coli O157:H7 or Salmonella Stanley
with final cell concentrations of ca. 1 9 104
CFU mL-1 (low inoculum) or 1 9 108 CFU mL-1
(high inoculum). The inoculated media in test tubes
were held at 22 °C with shaking at 100 rpm and were
sampled at 0, 7 and 24 h. Specimens were serially
diluted with sterile Butterfield’s phosphate buffer (pH
7.2, Hardy Diagnostics, Santa Maria, CA), and surface
plated (100 ll per plate and three plates per dilution)
onto Tryptic Soy Agar (TSA) (Difco/Becton–Dickin-
son, Sparks, MD). Plates were incubated at 37 8C for
24 h. Inoculated samples without antimicrobials
served as controls. Each experiment was conducted
in triplicate.
Examination of cell morphology by scanning
electron microscopy (SEM)
Escherichia coli O157:H7 cultures in the mid-log
phase of growth were treated with 8 mg mL-1 MgO
NP, 25 mg mL-1 nisin, or 4 mg mL-1 MgO NP ?
12.5 mg mL-1 nisin for 12 h. Aliquots of 1 mL
treated and untreated cell suspensions were centri-
fuged at 10,000 rpm for 5 min and the cell pellets
were resuspended in 100 lL TSB. Twenty microliter
of cell suspensions were deposited on each glass
coverslip. After air drying for 45 min, the coverslips
were fixed with a primary fixative solution containing
2.5% glutaraldehyde and 0.1 M imidazole buffer
solution (pH 7.2) for 2 h. Subsequently, the fixative
solution was exchanged with 0.1 M imidazole buffer,
followed by dehydration with a series of ethanol
solutions (50, 80 and 100%) with three changes at each
concentration. Finally, the coverslips were dried with
liquid CO2 in a DCP-1 Critical Point Dryer (Denton
Vacuum, Inc., Cherry Hill, NJ). The coverslips were
6879
mounted on SEM stubs with carbon adhesive tabs,
then sputter-coated with a thin layer of gold using a
Scancoat Six Sputter Coater (BOC Edwards, Wil-
mington, MA). Digital images of the treated and
untreated E. coli O157:H7 cells were acquired using a
Quanta 200 FEG scanning electron microscope (FEI
Inc., Hillsboro, OR) at an accelerating voltage of
10 kV and instrumental magnifications of 925000.
Statistical analysis
Antimicrobial experiments were conducted in tripli-
cate. Data points were expressed as the mean ± stan-
dard deviation. Data were analyzed using analysis of
variance from SAS version 9.1 software (SAS Insti-
tute, Cary, NC). Duncan’s multiple range tests were
used to determine the significant difference of mean
values. Unless stated otherwise, significance was
expressed at 5% level.
Results
Antibacterial effect of MgO NP on E. coli
O157:H7
The first experiment tested the antimicrobial efficacy
of MgO NP at different concentrations (1 to
8 mg mL-1) against E. coli O157:H7. It is commonly
accepted that more antimicrobial inhibitor is needed to
inhibit a larger initial microbial load (Steels et al.
2000). Therefore, two different initial populations (104
or 108 CFU mL-1) of E. coli O157:H7 in TSB were
evaluated at 22 °C for 24 h.
Figures 1 and 2 show the survival of E. coli
O157:H7 after treatments with different concentra-
tions of MgO NP in TSB when the cells were
inoculated at high and low levels, respectively. At
the high inoculation level, all treatments significantly
reduced the populations, except 1 and 2 mg mL-1
MgO NP. As expected, the anti-E. coli O157:H7
activity of MgO NP was dependent on its concentra-
tion in the test range; higher MgO NP concentrations
resulted in greater bacterial inactivation (Fig. 1).
Approximate seven log reductions in E. coli
O157:H7 were achieved by 8 mg mL-1 MgO NP
treatment at 24 h. Similarly, except 1 mg mL-1 MgO
NP treatment, all other treatments significantly
reduced E. coli O157:H7 populations inoculated at
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the low inoculum level (Fig. 2). At 7 h, the anti-E. coli

O157:H7 activity of MgO NP was dependent on its
concentration as in the case of low inoculum level.
However, the treatments with 3 mg mL-1 or higher
MgO NP significantly reduced cell concentrations to
undetectable levels (\10 CFU mL-1) after 24 h at
room temperature, indicating that 3 mg mL-1 MgO
NP would be enough to kill all cells.

Antibacterial effect of MgO NP and nisin

on E. coli O157:H7

It is interesting to find that the combination of

12.5 mg mL-1 of nisin and 4 mg mL-1 MgO NP
resulted in a bacterial reduction that was equivalent to Fig. 2 Effects of varying concentrations of MgO NP on the
the effect of 8 mg mL-1 MgO NP alone as shown in viability of E. coli O157:H7 at low inoculum levels in TSB at
Figs. 1 and 2, indicating a possible synergistic effect of 22 8C. The minimum detection limit was 10 CFU mL-1
the mixture. Therefore, the nisin and MgO NP combi-
nations were further investigated. Figure 3 presents the
survival of E.coli O157:H7 after treatments with MgO
NP, nisin and their combinations. Based on the cell
reductions at 7 and 24 h, the eight treatments could be
divided to three groups: the treatments in group I were
not effective (12.5 and 25 mg mL-1 nisin); the treat-
ments in group II were less effective and reduced
1–2.5 log CFU mL-1 cells (2 mg mL-1 MgO, 12.5
mg mL-1 nisin ? 2 mg mL-1 MgO, and 4 mg mL-1
MgO), and those in group III were most effective and
reduced the cells to undetectable levels (12.5 mg mL-1
nisin ? 4 mg mL-1 MgO, 25 mg mL-1 nisin ? 2 mg
mL-1 MgO, and 25 mg mL-1 nisin ? 4 mg mL-1

Fig. 3 Effects of MgO NP and nisin treatments on the viability

of E. coli O157:H7 at low inoculum levels in TSB at 22 8C. The
minimum detection limit was 10 CFU mL-1

MgO). These results demonstrated that nisin alone in

group I or MgO alone in group II had either no effect or
less effect on bacteria reduction. However, the combi-
nation (group III) of these two groups dramatically
decreased the viable cell counts. Apparently, the
synergistic antibacterial effects existed and were
significant.

Antibacterial effect of MgO NP and ZnO NP

on E. coli O157:H7
Fig. 1 Effects of varying concentrations of MgO NP on the
viability of E. coli O157:H7 at high inoculum levels in TSB at Our previous results have demonstrated that ZnO
22 8C. The minimum detection limit was 10 CFU mL-1 nanoparticles inhibited growth of some foodborne

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pathogens in liquid foods or media (Jin et al. 2009c, d;
Xie et al. 2011). Therefore, the synergistic antimicro-
bial effect of MgO combined with ZnO against E. coli
O157:H7 was further investigated in this study.
Figure 4 shows the survival of E. coli O157:H7
exposed to MgO NP, ZnO NP or their combinations.
The antibacterial effects of MgO NP were similar to
those in Fig. 2. ZnO NP reduced the growth of E. coli
about 1 log CFU mL-1 as compared to the controls at
7 and 24 h, but its antimicrobial activity was not
effective as MgO NP corresponding to the same
concentrations used. Moreover, unlike nisin, the
addition of ZnO NP to MgO NP (MgO ? ZnO) did
not further enhance the overall antimicrobial activity,
as there was no significant difference between the
MgO treatment and MgO ? ZnO treatment in reduc-
tion of E. coli O157:H7 cells.
Antibacterial effect of MgO NP and nisin
on Salmonella Stanley
Figure 5 shows the survival of Salmonella Stanley
treated by MgO NP, nisin, or their combinations.
Similar to E. coli O157:H7, the effect of anti-
Salmonella was dependent on the concentrations of
MgO NP, and adding nisin to MgO (MgO ? nisin)
significantly increased the antimicrobial efficacy of
MgO against Salmonella. In addition, Salmonella cells
were more susceptible to MgO NP treatments than
Fig. 4 Effects of MgO NP and ZnO NP treatments on the
viability of E. coli O157:H7 at low inoculum levels in TSB at
22 8C. The minimum detection limit was 10 CFU mL-1
6881
Fig. 5 Effects of MgO NP and nisin treatments on the viability
of Salmonella at high inoculum levels in TSB at 22 8C. The
minimum detection limit was 10 CFU mL-1
E. coli O157:H7 as it was observed that the MgO NP
treatment at the same concentrations achieved greater
reduction of Salmonella than E. coli O157:H7 at 7 and
24 h.
Morphological analysis of E. coli O157:H7
To gain direct evidence of the antibacterial action of
MgO NP, SEM analyses were performed on E. coli
O157:H7 samples with and without antibacterial
treatments. Figure 6 shows the SEM images with no
treatment (Fig. 6a), MgO treatment (Fig. 6b), nisin
treatment (Fig. 6c), and MgO ? nisin treatment
(Fig. 6d) for 12 h in TSB. As a control, the untreated
cells were clearly shown in rod shapes in normal sizes
with intact cell structures (Fig. 6a). The treatment of
the cells with MgO NP led to considerable damage to
E. coli O157:H7 cells and resulted in the formation of
irregular cell surfaces and alteration of membrane
integrity (Fig. 6b). The treatment of nisin caused the
formation of doughnut shapes in some cells but
elicited no significant change on cell surface and
membrane (Fig. 6c). With the combination of
MgO ? nisin, the cells shrunk and formed smaller
and rounded shapes (Fig. 6d) as compared with the
untreated cells. It is interesting that the cells treated
with MgO ? nisin exhibited unique cell morphology,
which has neither irregular rough surfaces as shown in
MgO NP-treated cells, nor doughnut shapes as formed
nisin-treated cells.
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Discussion
The results in this study have demonstrated that MgO
NP have extremely strong antibacterial activity
against foodborne E. coli O157:H7 and Salmonella
Stanley (Figs. 1, 2, 3, 4, 5). Other researchers also
reported that MgO nanoparticles in dry powder or
aqueous slurries are effective for killing certain Gram-
positive, Gram-negative bacteria, spore cells and
viruses (Stoimenov et al. 2002; Koper et al. 2002;
Sawai 2003). Taken together, these results suggest that
MgO NP can be used as an antimicrobial agent against
a broad spectrum of microorganisms.
The SEM images obtained in this work clearly show
that the presence of MgO NP or MgO ? nisin leads to
significant changes in cell morphology and membrane
integrity (Fig. 6). Viability studies showed that the
MgO-treated E. coli cells were no longer culturable,
suggesting disruption of bacterial membrane structure
or integrity could be the cause of cell death.
A number of mechanisms have been proposed to
interpret the antibacterial behaviour of metal oxides.
Makhluf et al. (2005) investigated the antibacterial
Fig. 6 Scanning electron
micrographs of E. coli
O157:H7 following
treatments with MgO NP
and nisin. Bacteria were
incubated with a TSB alone
(control), b 8 mg mL-1
MgO NP, c 25 mg mL-1
nisin, or d 4 mg mL-1 MgO
NP ? 12.5 mg mL-1 nisin,
as described under Materials
and methods
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J Nanopart Res (2011) 13:6877–6885
behaviour of MgO and proposed the following mech-
anisms: production of active oxygen species due to the
presence of MgO, interaction between MgO particles
and membrane cell wall, penetration of individual
MgO particles into cells and reformation of MgO
within the cell. Stoimenov et al. (2002), on the other
hand, suggested that the cell death is caused by
electrostatic interactions between the bacteria surface
and MgO nanoparticles. Sawai et al. (1998) studied the
antibacterial behaviour of ZnO particles by using a
chemiluminescence and oxygen electrode analysis.
They reported that H2O2 was produced in a ZnO slurry
and the concentration of H2O2 produced was linearly
proportional to the ZnO particle concentration of the
slurry. Xie et al. (2011) suggested the following action
model of ZnO NP against Campylobacter jejuni, a
microaerobic bacterium highly sensitive to oxidative
stress: direct interaction between ZnO NP and cell
surface increases membrane permeability; subse-
quently, the nanoparticles enter and induce oxidative
stress in bacterial cells, which results in the inhibition
of cell growth and eventually cell death. In this study,
the ZnO NP treatment was not as effective as MgO NP
J Nanopart Res (2011) 13:6877–6885
against E. coli O157:H7 (Fig. 4). It could be that
E. coli O157:H7 is less sensitive to oxidative stress
than Campylobacter or the antibacterial mechanism of
MgO may be different from ZnO, which needs to be
further investigated.
Escherichia coli O157: H7 and Salmonella Stanley,
both Gram-negative bacteria, showed less suscepti-
bility to nisin treatments (Figs. 3, 5). It is well-
understood that the antimicrobial effect of nisin is
caused by its interaction with phospholipid compo-
nents of the cytoplasmic membrane followed by an
interference with the membrane function (Henning
et al. 1986). Nisin causes cell death as a result of the
formation of relatively large pores in the membrane of
sensitive cells, resulting in the release of ions, amino
acids and ATP and the subsequent collapse of proton
motive force (Moll et al. 1997). Nisin has been proven
more effective against Gram-positive than Gram-
negative bacteria because of the difference in cell wall
structure (Hauben et al. 1996). In general, the protec-
tive outer membrane, surrounding the cytoplasmic
membrane and peptidoglycan layer of Gram-negative
cells, are difficult to be damaged with nisin. The low
susceptibility of E. coli O157: H7 and Salmonella
Stanley to nisin observed in this study (Figs. 3, 5)
provides further support for the mode of action of nisin
on Gram-negative bacteria. Although some E. coli
O157: H7 cells treated with nisin changed to doughnut
shapes, indicating some degree of cell disruption
(Fig. 6c), such injury can be subsequently repaired if
the cell is not severely damaged (Boziaris and Adams
2001), which is supported by the fact that all the nisin-
treated cells are viable and culturable in this study.
When MgO NP was combined with nisin, the
synergistic effect was obtained (Figs. 1, 2); this may
be explained that they have different antimicrobial
mechanisms. However, ZnO and MgO are both metal
oxides and may have similar antimicrobial mecha-
nisms; it could be a reason that the addition of ZnO to
MgO did not show a synergistic or additional effect
against the pathogen, as shown in Fig. 4.
As mentioned earlier, the E. coli O157: H7 cells
treated with MgO ? nisin did not show similar mor-
phological changes to the cells treated with MgO or
nisin alone. Uniquely, the cells treated with MgO ?
nisin were transformed into a smaller size with smoother
membrane surfaces. Although the mechanisms for the
synergistic effect of MgO ? nisin are not clear, it might
be explained that the large pores in the membrane
6883
caused by nisin treatment facilitate either MgO mole-
cules penetration into microbial cells to express their
antibacterial activity or release of intercellular compo-
nents, resulting in the changes of morphologies and
structures of outer membrane such as blebs, vesiculation
and disruption of lipopolysaccharides.
Compared with TiO2, silver, copper and other kinds
of solid bactericides, nano-MgO, which is less toxic
and prepared from readily available materials, has
great potential as a novel solid bactericidal material
under simple conditions (Huang et al. 2005). Magne-
sium is an essential nutrient for the human body and
is present in almost all foods. The Food and Nutrition
Board (1997) lists the recommended dietary
allowances (RDA) for magnesium as 420 and
320 mg day-1 for healthy adult men and women,
respectively. Nisin was affirmed GRAS (Generally
Recognized as Safe) by the U.S. Food and Drug
Administration (FDA) in 1988 (Food and Drug
Administration (FDA) 1988), and is now used as a
biopreservative in 57 countries around the world.
Therefore, as the rapid growth in nanotechnology has
spurred significant interest in the application of
nanomaterials as antimicrobials, MgO alone or in
combination with nisin can potentially be used in food
products as bactericides to improve microbiological
food safety.
Conclusions
In this study, MgO NP has shown strong antibacterial
activity against important foodborne pathogens,
E. coli O157:H7 and Salmonella Stanley; higher
MgO NP concentrations resulted in greater bacterial
inactivation. The bactericidal effect of MgO was
synergistically enhanced by its combination with
nisin. Because of this synergism, it may be possible
that the concentration of each preservative in formula
could be reduced while a similar reduction of patho-
genic microorganisms could be achieved. The nano-
particles appear to directly interact with the microbial
cells, subsequently inducing considerable changes in
cell morphology and disrupting normal cell structure
and function; therefore, resulting in cell growth
inhibition and death. The antibacterial mechanisms
of MgO NP need to be further confirmed. These results
suggest that MgO NP alone or in combination with
nisin could potentially be used as an effective
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antibacterial agent in food formulations directly or
through the slow release from packaging materials to
kill or inhibit pathogens in foods.
Acknowledgments The authors wish to thank Anita
Parameswaran and Gaoping Bao for technical support. We
would also like to thank our reviewers, Drs. Joshua Gurtler and
Dike Ukuku for careful critiques.
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