Food Control 46 (2014) 412e429
Contents lists available at ScienceDirect
Food Control
journal homepage: www.elsevier.com/locate/foodcont
Review
Natural products as antimicrobial agents
Rabin Gyawali a, b, Salam A. Ibrahim b, *
a
b
Energy and Environmental Systems, North Carolina Agricultural and Technical State University, USA
Food Microbiology and Biotechnology Laboratory, 173 Carver Hall, North Carolina Agricultural and Technical State University, Greensboro, NC 27411, USA
a r t i c l e i n f o
a b s t r a c t
Article history:
Received 12 December 2013
Received in revised form
16 May 2014
Accepted 22 May 2014
Available online 8 June 2014
The use of natural antimicrobial compounds in food has gained much attention by the consumers and
the food industry. This is due primarily to two major factors. First, the misuse and mishandling of antibiotics has resulted in the dramatic rise of a group of microorganisms including foodborne pathogens
that are not only antibiotic resistant but also more tolerant to several food processing and preservation
methods. In addition, increasing consumers' awareness of the potential negative impact of synthetic
preservatives on health versus the benefits of natural additives has generated interest among researchers
in the development and use of natural products in foods. This has prompted the food industry to look for
alternative preservatives that can enhance the safety and quality of foods. Compounds derived from
natural sources have the potential to be used for food safety due to their antimicrobial properties against
a broad range of foodborne pathogens. This article reviews the antibacterial activity of natural components from different sources including plants, animals, bacteria, algae and mushrooms, and their potential use in food systems.
© 2014 Elsevier Ltd. All rights reserved.
Keywords:
Natural antimicrobials
Structure-function
Plant by-products
Algae and mushrooms
Foodborne pathogens
Food safety
Contents
1.
2.
3.
4.
5.
6.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 413
Antimicrobials of plant origin . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 413
2.1.
Plant-derived compounds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 413
2.2.
Plant by-products . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 415
Antimicrobials of animal origin . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 417
3.1.
Lactoferrin . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 418
3.2.
Chitosan . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 418
3.3.
Lysozyme . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 419
3.4.
Milk-derived peptides . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 419
Antimicrobials of bacterial origin . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 420
4.1.
Bacteriocin . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 420
4.2.
Reuterin . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 421
Algae and mushrooms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 421
5.1.
Algae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 421
5.2.
Mushrooms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 421
Incorporation of antimicrobials in food systems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 423
6.1.
Direct applications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 423
6.2.
Edible films and coatings . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 423
6.3.
Nanoparticles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 424
* Corresponding author. Tel.: þ1 336 285 4860; fax: þ1 336 334 7239.
E-mail addresses: rgyawali@aggies.ncat.edu (R. Gyawali), ibrah001@ncat.edu
(S.A. Ibrahim).
http://dx.doi.org/10.1016/j.foodcont.2014.05.047
0956-7135/© 2014 Elsevier Ltd. All rights reserved.
R. Gyawali, S.A. Ibrahim / Food Control 46 (2014) 412e429
7.
413
Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 424
Acknowledgment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 425
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 425
1. Introduction
Foodborne illnesses are a major concern for consumers, the food
industry, and food safety authorities. In recent years, considerable
effort has been made to find natural antimicrobials that can inhibit
bacterial and fungal growth in foods in order to improve quality and
shelf-life. Similarly, consumers have become concerned about the
safety of synthetic preservatives used in food. As a result, there is
increasing demand for natural products that can serve as alternative food preservatives (Tajkarimi, Ibrahim, & Cliver, 2010). This, in
turn, has led to a search for antimicrobials derived from a variety of
natural sources. Natural antimicrobials can be obtained from
different sources including plants, animals, bacteria, algae and
fungi. Several studies related to plant antimicrobials have demonstrated the efficacy of plant-derived compounds in food applications, as well as factors influencing this effectiveness (Cowan, 1999;
Gyawali & Ibrahim, 2012; Hayek, Gyawali, & Ibrahim, 2013;
Tajkarimi et al., 2010). However, there has been limited research
related to the structureefunction relationship of these compounds.
As a result, the importance of the chemical composition of plantderived compounds with regard to their antimicrobial activity is
still not well understood. Among several plant-derived compounds,
polyphenolic compounds have great structural diversity and variations in chemical composition, and thus differ in their antibacterial effectiveness against pathogenic microorganisms (Stojkovic
et al., 2013). The antimicrobial activity of plant extracts may thus
be due to the presence of phenolic compounds or other hydrophobic components in the essential oils (EOs) (Dorman & Deans,
2000). It should also be noted that the investigation of possible
antibacterial activity of by-products generated from fruits and
vegetables is very limited in the literature. These by-products can
also be used as sources of antibacterial compounds (Baydar, Sagdic,
Ozkan, & Cetin, 2006; Jayaprakasha, Selvi, & Sakariah, 2003;
Matsumoto et al., 2004) and thus could be a potential source of
low-cost natural antimicrobials. Antimicrobial compounds produced by algae and fungi (mushrooms) against pathogens have
recently received considerable attention as a new source of novel
antimicrobial substances (Bhagavathy, Sumathi, & Jancy Sherene
Bell, 2011; Ramesh & Pattar, 2010). There are many unexplored
sources of such potential compounds that could be used as natural
preservatives in food applications. This paper reviews various antimicrobials from plants, animals, bacteria, algae and mushrooms.
In addition, different methods of incorporating these antimicrobials
into our food systems are discussed.
2. Antimicrobials of plant origin
2.1. Plant-derived compounds
Most of the available studies related to plant-derived antimicrobials found in scientific literature involve the antimicrobial or
antioxidant activity of herbs, spices, and their compounds (Cueva
et al., 2010; Negi, 2012; Tajkarimi et al., 2010). In this section, we
provide an overview of the antimicrobial activity of these compounds mainly based on their structural characteristics. Plantderived compounds from herbs and spices have been used since
ancient times for flavoring food, as traditional medicine, and as
preservatives. In addition to being used in food to impart flavor,
pungency and color, herbs and spices also have antioxidant, antimicrobial, nutritional and pharmaceutical properties (Lai & Roy,
2004). Plant-derived compounds are mostly secondary metabolites, most of which are phenols or their oxygen-substituted derivatives. These secondary metabolites possess various benefits
including antimicrobial properties against pathogenic and spoilage
microbes (Hayek et al., 2013). Major groups of compounds that are
responsible for antimicrobial activity from plants include phenolics,
phenolic acids, quinones, saponins, flavonoids, tannins, coumarins,
ra, 2007; Lai & Roy, 2004).
terpenoids, and alkaloids (Ciocan & Ba
Variations in the structure and chemical composition of these
compounds result in differences in their antimicrobial action
(Savoia, 2012). (Fig. 1).
The structural diversity of plant-dervied compounds is
immense, and, the impact of antimicrobial action they produce
against microorganisms depends on their structural configuration.
Phenolic compounds possess great structural variations and are
one of the most diverse groups of secondary metabolites. The hydroxyl (eOH) groups in phenolic compounds are thought to cause
inhibitory action (Lai & Roy, 2004) as these groups can interact with
the cell membrane of bacteria to disrupt membrane structures and
cause the leakage of cellular components (Xue, Davidson, & Zhong,
2013). The presence of eOH group in the phenolic compounds plays
an important role in the antimicrobial activity of carvacrol and
thymol. Active group such as eOH promotes the delocalization of
electrons which then act as proton exchangers and reduce the
gradient across the cytoplasmic membrane of bacterial cells. This
will cause the collapse of the proton motive force and depletion of
the ATP pool and ultimately leading to cell death (Ultee, Bennik, &
Moezelaar, 2002). Similarly, Farag, Daw, Hewidi, and El-Baroty
(1989) reported that these eOH groups can easily bind the active
site of enzymes by altering the cell metabolism of microorganisms.
This action demonstrates the importance of eOH groups in antimicrobial activity. Phenolic compounds also act as antioxidants.
The presence of a free eOH group in phenolic compounds results in
the antioxidant properties. This property has been reported to
inhibit the generation of reactive oxygen species, as well as the
scavenging of free radicals thereby reducing the redox potential of
the growth medium (Cueva et al., 2010; Stojkovic et al., 2013). This
lowering of redox potential may further restrict the growth of
undesirable microorganisms.
As reported by Dorman and Deans (2000), the position of the
eOH group also influences the components' antimicrobial effectiveness. For example, the structure of thymol is similar to that of
carvacrol; however, difference in antimicrobial effectiveness between thymol and carvacrol against Gram-positive and Gramnegative bacteria was observed when tested in agar medium. This
difference has been attributed to the eOH group located at the meta
position in thymol compared to the ortho position in carvacrol.
Alcaraz, Blanco, Puig, Tomas, and Ferretti (2000) also reported the
importance of the eOH group at position 5 of flavanones and flavones for activity against methicillin-resistant Staphylococcus
aureus strains. Ultee et al. (2002) emphasized the importance of the
eOH group and its system of delocalized electrons present in
carvacrol against foodborne pathogens. Their study compared the
activity of carvacrol to menthol, carvacrol methyl ester, and cymene. The authors concluded that the growth of Bacillus cereus was
not inhibited due to the lack of eOH groups in carvacrol methyl
414
R. Gyawali, S.A. Ibrahim / Food Control 46 (2014) 412e429
Fig. 1. Structural variation among functional groups in plant compounds alters their antimicrobial activity.
ester, and cymene. The strong antimicrobial effect of carvacrol was
therefore hypothesized to be due to the presence of eOH groups
and the presence of a system of delocalized electrons. The specific
mechanism involved here is the destabilization of the cytoplasmic
membrane by compounds with phenolic eOH groups which act as
proton exchangers, thereby reducing the pH gradient across the
cytoplasmic membrane and thus leading to cell death. The authors
further illustrated that even though menthol has an eOH group, it
does not show high antimicrobial activity due to its lack of a system
of delocalized electrons (double bonds). This deficit thereby prevents the eOH group from releasing its proton.
The importance of the number of double bonds in relation to
antimicrobial effectiveness is described by Gochev, Dobreva,
Girova, and Stoyanova (2010). Among citronellol, geraniol, and
nerol, citronellol was found to be less effective due to the presence
of only one double bond whereas geraniol and nerol with two
double bonds, showed higher antimicrobial activity against tested
bacteria (B. cereus, Escherichia coli, S. aureus) and yeast (Candida
albicans). The antimicrobial activity of two pairs of isomeric
phenolic compounds, eugenol-isoeugenol, has also been shown to
differ solely due to the position of the double bond in the aliphatic
side chain. Friedman, Henika, and Mandrell (2002) found eugenol
to be about 13-fold more active than isoeugenol against Campylobacter jejuni and Listeria. By contrast, the 2-carvone optical isomers
(R and S) were equally active against E. coli, Salmonella enterica, and
C. jejuni, but S isomer was found to be 2e3 fold more active than R
isomer against Listeria monocytogenes strains (Friedman et al.,
2002). These results are also supported by Griffin, Wyllie,
Markham, and Leach (1999), who found equal antimicrobial activity of geraniol and nerol isomers indicating that the position of
the eOH group has no significant effect on the antimicrobial
property. These findings indicate that the structureefunction
relationship among these isomers is not well understood.
The structureefunction relationships of terpenes was investigated by Griffin, Wyllie, and Markham (2005), who found that
slight structural changes differing only in the position of the eOH
group could play a significant role in terpenes' antimicrobial activity. For example, terpinen-4-ol was shown to induce Kþ leakage
from E. coli cells at lower concentrations than a-terpineol. The
mode of antimicrobial action is attributed to the general feature of
oxygenated terpenes and their ability to cause membrane
permeability and Kþ leakage. It was also reported that oxygenated
terpenes, especially phenols such as thymol and carvacrol, showed
higher antibacterial activity compared to hydrocarbon monoterpenes (Sokovic, Glamo
clija, Marin, Brki
c, & Griensven, 2010). It
has been shown that these hydrocarbons have limited hydrogenbonding capacity and low water solubility that limits their diffusion through the agar medium (Griffin, Markham, & Leach, 2000).
A recent investigation showed that caffeic acid had higher antimicrobial activity in comparison to p-coumaric acid due to the
addition of one more eOH group at the phenolic ring of caffeic
acid (Stojkovi
c et al., 2013). This observation was confirmed by
Figueiredo, Campos, de Freitas, Hogg, and Couto (2008), who
demonstrated that adding two or more eOH groups could
enhance the antimicrobial activity of benzaldehyde derivatives.
Benzaldehydes with two or more adjacent eOH groups have been
reported to be more active than aldehydes as benzaldehydes are
thought to act primarily on the external surface of the cells
combining with sulphydryl groups of proteins (Friedman, Henika,
& Mandrell, 2003; Ramos-Nino, Ramirez-Rodriguez, Clifford, &
Adams, 1998).
Cueva et al. (2010) grouped phenolic acids based on their
chemical structure. According to these authors, the position of eOH
substitution in the aromatic ring and the length of the saturated
side chain were influencing factors for antimicrobial activity. The
high antimicrobial activity of phenolic compounds also depends on
the size of added alkyl or alkenyl group. Pelczar, Chan, and Krieg
(1988) reported stronger antimicrobial activity with the presence
of larger size of added alkyl or alkenyl groups. The high activity of
phenolic compounds could be thus due to the alkyl substitution in
the phenol nucleus (Pelczar et al., 1988). The aldehyde group
associated with carbon to carbon double bond has high electronegativity, thus increasing its antibacterial activity (Kurita, Miyaji,
Kurane, Takahara, & Ichimura, 1981; Moleyar & Narasimham,
1986). One possible explanation for this could be that the electronegative compounds interfere with electron transfer and react with
proteins and nucleic acids, thereby inhibiting the growth of microorganisms (Dorman & Deans, 2000).
R. Gyawali, S.A. Ibrahim / Food Control 46 (2014) 412e429
Studies investigating the antimicrobial activity of EOs in plants
and the structural relationships between their compounds and
their antimicrobial activity have been reported (Dorman & Deans,
2000; Ultee et al., 2002). These studies demonstrated that
phenolic structure plays an important part of the antimicrobial
activity. Active groups in the phenolic structure are very critical for
activity. For example, eOH groups and allylic side chains enhance
volatile oils efficacy. Carvacrol with the eOH group had more activity than modified carvacrol with methyl ester. Limonene (1methyl-4-(1-methylethenyl)-cyclohexene) is more effective
compared to p-cymene. This is likely attributable to the type of
alkyl group in nonphenolic compounds indicating that alkenyl has
more influence on antimicrobial activity than alkyl (Dorman &
Deans, 2000). Acetate moieties in volatile oils compounds may
also positively influence the activity of several plant extracts. For
example, Geranyl acetate has been found to be more active against
a range of Gram-positive and negative bacteria than Geraniol
(Dorman & Deans, 2000). Because antimicrobial activity depends
not only on chemical composition but also on lipophilic properties,
the potency of functional groups or aqueous solubility (Dorman &
Deans, 2000) and the mixture of compounds with different
biochemical properties may increase the efficacy of EOs. This action
involves membrane disruption by lipophilic compounds resulting
in inhibition of electron transport, protein translocation, phosphorylation, and other enzymatic activity (Dorman & Deans, 2000)
which ultimately destroy the cell membrane integrity resulting in
the death of microorganisms. This antimicrobial activity of plant
antimicrobials could also vary depending on the type of microorganisms, extraction method, culture medium, size of inoculum, and
method of determination (Tajkarimi et al., 2010).
2.2. Plant by-products
During food processing, oftentimes large amount of by-products
are generated including fruit pomace, seeds, peels, pulps, unused
flesh, and husks. Although these by-products typically have been
considered waste, some studies have shown that the peels, seeds,
husks and kernels are promising sources of valuable components
such as phenolic compounds (polyphenols, tannins, and flavonoids)
and many other bioactive components that have several functionalities including antimicrobial activity (Balasundram, Sundram, &
Samman, 2006; Engels et al., 2009; Tiwari et al., 2009). Byproducts of fruits and vegetables are potentially good sources of
minerals, organic acid, and phenolics that have a wide range of
antimicrobial properties (Chanda, Baravalia, Kaneria, & Rakholiya,
2010). Ayala-Zavala et al. (2011) reported that by-products can
have a similar or even higher proportion of bioactive compounds
than the usable parts of produce. For example, the total phenolics in
peels of lemons, oranges and grapefruits have been found to be 15%
higher than the level found in the peeled fruits (Gorinstein et al.,
2001). Therefore, commercial exploitation of these by-products
for the recovery of these compounds seems promising from a
food safety perspective. As estimated by Oreopoulou and Tzia
(2007), the annual worldwide waste from fruits and vegetables is
substantial (Table 1). Approximately 0.3e67 metric tons of waste
from fruits and vegetables is generated annually. These waste byproducts, if utilized, could be major sources of phenolic compounds that could be used as antimicrobial agents. Hence, the use
of these by-products for further exploitation may be an economically attractive way to enhance food safety. Table 2 lists some plant
by-products and their major components as antimicrobials.
Fruit processing results in various amounts of pomace as a byproduct, which accounts for almost 25e35% of processed fruits
(Schieber et al., 2003). Pomace consists of seeds, skins, and stems,
and is an important by-product that is a rich source of phenolic
415
Table 1
Estimated resulting wastes of selected fruits and vegetables (Adapted from
Oreopoulou & Tzia, 2007).
Fruits/
vegetables
Apple
Carrot
Cooking
banana
Grape
Kiwifruit
Orange and
other citrus
fruits
Peach
(canned)
Pear
Potato
Tomato
By-products/
processed fruit
(%, wet basis)
Estimated annual
waste (million
metric tons)
12.0
23.6
30.0
25e35
30e40
30
3.0e4.2
<10
9
50.0
1.0
31.2
15e20
30.0
50.0
5e9
<0.3
15.6
-
-
15e45
3e7
22e67
0.9e2.1
Annual processed
(million metric
tons)
1.0
1.7
150
30
-Not available.
compounds, flavonoids and non-flavonoids, polyphenols, minerals,
vez, Chiffelle, & Asenjo,
and dietary fiber (Figuerola, Hurtado, Este
2005; Sudha, Baskaran, & Leelavathi, 2007). These phenolic compounds have antibacterial activity against a wide range of microorganisms (Sagdic, Ozturk, Yilmaz, & Yetim, 2011). Ethanolic extract
of grape pomace at 10% has been shown to inhibit the growth of
Enterobacteriaceae, S. aureus, Salmonella, yeasts and molds in beef
patties during 48 h of storage at 4 C indicating that pomace can be
a good choice for extending the microbial shelf-life of food products
(Sagdic et al., 2011). Similarly, spoilage and pathogenic bacteria
including Aeromonas hydrophila, B. cereus, Enterobacter aerogenes,
Enterococcus faecalis, E. coli, E. coli O157:H7, Mycobacterium smegmatis, Proteus vulgaris, Pseudomonas aeruginosa, Pseudomonas fluorescens, Salmonella Enteritidis, Salmonella Typhimurium, S. aureus,
and Yersinia enterocolitica have been inhibited by grape pomace
€
€ktürk Baydar, & Kurumahmutoglu, 2004).
extract (Ozkan,
Sagdiç, Go
The antimicrobial properties of olive pomace and olive juice powder were investigated by Friedman, Henika, and Levin (2013) using
a quantitative bactericidal activity assay against foodborne pathogens E. coli, L. monocytogenes, S. enterica, and S. aureus. The results
indicated that olive pomace showed a similar inhibitory pattern to
olive juice powder due to the presence of phenolic compound
oleocanthal. This was also confirmed by Cicerale, Conlan, Barnett,
and Keast (2011), who reported that olive pomace waste is also a
valuable source of phenolic oleocanthal that is responsible for the
antimicrobial action. Fruit skin contains various sugars and nutrients and also serves as a fermentation medium. Salem et al. (2009)
demonstrated the production of lactic acid from apple skin waste
using lactic acid bacteria. This could be a promising method for the
utilization of fruit skin waste for the production of lactic acid which
can be used as a preservative in a wide range of food applications.
The antimicrobial activity of fruit peels is well documented. For
example, pomegranate fruit peels have been widely used in herbal
remedies for treating several diseases (Al-Zorkey, 2009). Pomegranate fruit peels extracts were shown to inhibit the growth of
several foodborne pathogens including L. monocytogenes, S. aureus,
E. coli, Y. enterocolitica, and B. cereus (Agourram et al., 2013; AlZoreky, 2009; Kanatt, Chander, & Sharma, 2010). Pomegranate
peel extract was more effective against Gram-positive bacteria even
at a concentration of 0.01%. However, in the case of Gram-negative
bacteria, extract was effective against Pseudomonas spp. at a higher
concentration of 0.1% and less effective against E. coli and S.
Typhimurium at the same concentration (Kanatt et al., 2010; Negi &
Jayaprakasha, 2003). It has also been reported that pomegranate
416
R. Gyawali, S.A. Ibrahim / Food Control 46 (2014) 412e429
Table 2
Plant by-products as antimicrobials.
By-products
Major component
Target organisms
References
Pomegranate fruit peels
Phenolics and flavonoids
Pomegranate juice
byproducts
Apple peels
Almond skin extracts
Coconut husk
Phenolics, flavonoids, tannins
L. monocytogenes, S. aureus, E. coli,
Yersinia enterocolitica, P. fluorescens
MRSA ATCC 43300 and E. coli ATCC 35218
Agourram et al. (2013);
Al-Zoreky (2009)
Reddy, Gupta, Jacob,
Khan, & Ferreira (2007)
Agourram et al. (2013)
Mandalari et al. (2010)
Wonghirundecha and
Sumpavapol (2012)
Sung et al. (2012)
Green tea waste
Polyphenolic compounds
Polyphenols
Phytochemical including phenolics
and tannins
Tannins
Acorn, chestnut, and
persimmon hull
Tannins
Tomato seeds
Peels, seeds, and pulp
of mexican lime
Metabolites such as fatty acids,
carotenoids, saponins, phenolic
compounds
Polyphenolic compounds such as
chlorogenic acid, catechin, quercetin
and kaempferol
Chlorogenic, caffeic, gallic, and
protocatechuic acids
Antioxidants such as phenolic compounds
Phenolic compounds, saturated fatty acids,
mono-unsaturated oleic acid, tocopherols,
squalene, and different sterol fractions
Phytochemicals: flavonones,
polymethoxylated flavones, tannins
Grape pomace
Phenolic acids, flavonoids, stilbenes
Olive pomace
Phenolic compounds including oleocanthal,
deoxyloganic acid lauryl ester
Phenolics, flavonoids betacyanins, betaxanthins
Phenolics, flavonoids, antioxidants comprising
tocopherols, rutin, quercetin derivatives
Quince fruit peel
Potato peels
Walnut green husk
Mango seed
kernel extract
Beet root pomace extract
Buckwheat hull extracts
Legume hulls (Vigna
radiate, Cicer arietinum
and Cajanus cajan)
Grapefruit seed extracts
Oriental mustard
(Brassica juncea L.)
seed meal extracts
Coffee pulp
Polyphenolic compounds, flavonoids
Phenolic compounds such as catechins,
epicatechin, epocatechin-3-O-gallate, dimeric,
trimeric and tetrameric procyanidins
Phenolic compounds (sinapic acid and several
sinapoyl conjugates)
Polyphenols such as flavan-3-ols,
hydroxycinnamic acids, flavonols and
anthocyanidins
S. aureus, P. fluorescens
S. aureus, L. monocytogenes
L. monocytogenes, S. aureus and V. cholera
S. aureus, E. coli
L. monocytogenes , Bacillus coagulans, Shigella flexneri
S. aureus, E. coli
L. monocytogenes
B. coagulans, S. flexneri
S. aureus, S. epidermidis, Micrococcus luteus, E. faecalis,
B. cereus, Candida albicans
Sung et al. (2012)
Taveira et al. (2010)
S. aureu, P. aeruginosa, E. coli, C. albicans
Fattouch et al. (2007)
Bacteriostatic effect on E. coli and S. Typhimurium
Sotillo, Hadley, and
Wolf-Hall (1998)
Oliveira et al. (2008)
Abdalla et al. (2007)
S. aureus, B. cereus, B. subtilis
Inhibited total bacterial count, coliforms, and E. coli
E. coli O157:H7, S. Typhimurium, Shigella sonnei
S. aureus, Salmonella, Enterococci, Total aerobic
mesophilic and psychrotrophic bacteria,
yeasts and molds
E. coli O157:H7, S. enterica, L. monocytogenes,
and S. aureus
S. aureus, B. cereus E. coli, P. aeruginosa
Gram-positive (B. cereus, S. aureus, Enterococcus
faecalis) and Gram-negative bacteria (Salmonella
Choleraesuis, E. coli and Proteus mirabillis)
B. cereus, S. aureus
Mathur et al. (2011);
Orue, García, Feng, and
Heredia (2013)
Sagdic et al. (2011)
Friedman et al. (2013)
Djilas and Markov (2011)
Cabarkapa
et al. (2008)
Kanatt et al. (2011)
Pesudomonas spp.
Bevilacqua, Ficelo,Corbo,
& Sinigaglia (2010)
B. subtilis, E. coli, L. monocytogenes,
Pseudomonas fluorescens, and S. aureus
Engels et al. (2012)
Total viable count, coliform, E. coli, and
fungal count
Adebowale et al., (2012);
Ramírez-Coronel et al. (2004);
Ulloa Rojas et al. (2003)
peel extracts have some potential as preservatives in food products.
Kanatt et al. (2010) assessed the shelf-life of chicken products using
pomegranate peel extract. The results showed that the addition of
0.1% extracts in chicken meat reduced the total bacterial count,
coliform, and S. aureus and enhanced the shelf-life by 2e3 weeks
during chilling temperature storage. In addition, pomegranate peel
extract was found to be effective in controlling oxidative rancidity
in these chicken products. Hayrapetyan, Hazeleger, and Beumer
(2012) evaluated the potential of pomegranate peel extract as an
. The extract at 7.5%, v/w (24.7 mg/g)
antilisterial agent in meat pate
inhibited the growth of L. monocytogenes by 4.1 log CFU/g during 46
days of storage at 4 C. However, the bacterial population in the
control sample had reached 9.2 log CFU/g in 18 days from an initial
population of 4 log CFU/g. The authors also demonstrated that the
inhibitory effect was less effective at higher temperatures (7 C and
12 C) indicating that the inhibitory effect of the extract was temperature dependent. The presence of active inhibitors in peels,
phenolics, flavonoids, and tannins exhibit antimicrobial activity
(Machado et al., 2003; Voravuthikunchai et al., 2005). Among
several polyphenols present in pomegranate peel, its antimicrobial
activity has been largely attributed to its hydrolyzable ellagitannins. Recently, the antilisterial effect of tannin-rich fraction from
pomegranate rind was investigated by Li et al. (2014). Results from
an agar dilution assay showed that the minimum inhibitory concentration (MIC) of tannin-rich fraction was 1.25e5.0 mg/ml for
different strains of L. monocytogenes. Li et al. (2014) also demonstrated that these tannin fractions impaired the cell membrane
structure, leading to a loss of cell homeostasis.
Bergamot peel, a by-product of the essential oil (EO) industry
was also found to be effective against Gram-negative foodborne
pathogens (E. coli, S. enterica) and the Gram-positive Bacillus subtilis. The MIC of bergamot ethanolic fraction was in the range of
0.2e0.8 mg/ml (Mandalari et al., 2007). The antimicrobial activity
of quince peel extract was tested against Gram-positive (S. aureus)
and Gram-negative bacteria (E. coli, P. aeruginosa) and yeast
(C. albicans). Fattouch et al. (2007) found quince peel extract to be
the most effective at inhibiting bacterial growth with minimum
inhibitory and bactericide concentrations in the range of
R. Gyawali, S.A. Ibrahim / Food Control 46 (2014) 412e429
0.1e5.0 mg polyphenol/ml. This strong antimicrobial activity was
found to be due to the presence of chlorogenic acid that acts in
synergism with other components of the extracts. The possible
antimicrobial activity by extracts containing phenolics is most
likely due to the disruption of the cell membrane (Kanatt et al.,
2010).
Mango kernel extracts also exhibited a broad antimicrobial
spectrum against several foodborne pathogenic bacteria. Methanolic extract of mango seed kernel at 3000 ppm have shown
antimicrobial activity against E. coli when tested using the agar well
diffusion method (Abdalla, Darwish, Ayad, & El-Hamahmy, 2007).
The same concentration (3000 ppm) of extract added to raw cow
milk reduced the total bacterial count and inhibited coliform
growth during 6 h incubation at room temperature. These results
suggest that mango seed kernel extract could be added to extend
the shelf-life of pasteurized cow milk. Mango seed kernel extract
has also been shown to enhance the oxidative stability of fresh-type
cheese and ghee and to extend their shelf-life (Dinesh, Boghra, &
Sharma, 2000; Parmar & Sharma, 1990; Puravankara, Bohgra, &
Sharma., 2000). Similarly, tannins (Gallotannins) isolated from
mango (Mangifera indica L.) kernels have been shown to inhibt the
growth of Gram-positive food spoilage (B. subtilis), foodborne
pathogenic (S. aureus), and Gram-negative (E. coli) bacteria. The
mechanism for the inhibitory effects of tannins may be due to their
iron-complexing properties (Engels et al., 2009) and their ability to
interact with proteins and to inhibit enzyme activity (Konishi et al.,
1993). The presence of polyphenol compounds in mango kernel
extracts is attributable to this antimicrobial action (Kabuki et al.,
2000). Other fruits such as jackfruit, papaya, plum, guava, and
tamarind and their seed extracts have also shown antimicrobial
activity against both Gram-positive (S. aureus, B. subtilis) and Gramnegative bacterial strains (E. coli, P. aeruginosa) (Debnath et al.,
2011). Tomato seeds, a major by-product of the tomato processing industry, contain organic acids and phenolic compounds. Tomato seed extracts have shown antimicrobial activity against
Gram-positive bacteria and fungi including S. aureus, Staphylococcus epidermidis, Micrococcus luteus, E. faecalis, B. cereus, and
C. albicans (Taveira et al., 2010). Similarly, 20 ml of 50% ethanolic
extracts of stink bean pod were tested against foodborne pathogens
using culture medium. The extract inhibited the growth of B. cereus,
L. monocytogenes, S. aureus, E. coli, Vibrio cholera, and S. Typhimurium (Wonghirundecha & Sumpavapol, 2012). Phytochemical analyses revealed the presence of active inhibitors including
phenolics and tannins in extract that contributed to this antimicrobial activity. In a recent study, Engels, Schieber, and G€
anzle
(2012) identified a phenolic compound in mustard seed meal
called sinapic acid and confirmed its antimicrobial activity against
Gram-negative E. coli, and P. fluorescens and Gram-positive
B. subtilis. The study also showed the effects of sinapic acid
against pathogenic bacteria such as S. aureus, and L. monocytogenes.
Mustard seed meal, a by-product of mustard oil processing, could
thus be used as an effective antimicrobial.
Similarly, fruit husks are by-products that can be used as an
easily accessible source of natural bioactive compounds that
contain antimicrobial properties. Oliveira et al. (2008) investigated
the antimicrobial activity of walnut green husks against Grampositive and Gram-negative bacteria using the agar dilution
method. The aqueous extracted green husks of walnuts inhibited
the growth of Gram-positive bacteria including B. cereus, B. subtilis,
and S. aureus (Oliveira et al., 2008) with MIC of 0.1 mg/ml.
Wonghirundecha and Sumpavapol (2012) reported antimicrobial
activity of 50% ethanolic extract of coconut husks against foodborne
pathogens using the agar well diffusion assay. Coconut husk at 20 ml
of the 50% ethanolic extract showed inhibition against Grampoitive (B. cereus, L. monocytogenes, S. aureus) and Gram-negative
417
bacteria (E. coli, S. Typhimurium, V. cholera). Hulls removed prior
to the utilization of the seeds are also rich in bioactive components.
The antimicrobial properties of flavonoid-rich fractions derived
from almond skins, a by-product of the almond processing industry, were investigated by Mandalari et al. (2010) in culture
medium. Almond skin fractions were found to have antimicrobial
activity against L. monocytogenes and S. aureus in the range
0.25e0.5 mg/ml. The highest antimicrobial potential was for natural almond skins compared to that of blanched skins. This could be
explained by the amount of flavonoids being 10 fold higher in
natural skin than blanched skins. As a result, natural skins at
0.5 mg/ml were able to inhibit Gram-negative S. enterica var.
Typhimurium. The hulls from buckwheat grains are more abundant
in total phenolics and flavonoids in comparison to other parts of
grain. According to Cabarkapa,
Sedej, Sakac, Sari
c, and Plavsi
c
(2008), Gram-positive (B. cereus, S. aureus, E. faecalis) and Gramnegative (Salmonella Choleraesuis, E. coli, Proteus mirabilis) bacteria were sensitive to all buckwheat hull extracts. The antimicrobial
activity of different legume hulls was tested against common food
spoilage and pathogenic bacteria showing the potentiality of
legume hulls to be a novel natural additive (Kanatt, Arjun, &
Sharma, 2011). This study showed >2 log CFU reductions of
B. cereus at 0.05% of Cicer arietinum (Bengal gram) and complete
inhibition at 0.1% of hull extracts when tested in 0.85% saline solution. Similarly, a one log reduction of S. aureus was achieved by
0.2% extract of C. arietinum and Cajanus cajan (pigeon pea) extract
while Vigna radiata (mung bean) extract was ineffective against
S. aureus. The presence of high polyphenols in these hull extracts
could account for the microbial inhibitory effect.
Coffee is one of the most important agricultural commodities in
the world. Coffee husks, peel and pulp, which comprises nearly 45%
of the cherry, are one of the main by-products of coffee processing
nez, 2012). Similarly, tea is another popular
(Esquivel & Jime
beverage consumed worldwide. Tea extract powder, a major byproduct of tea processing also contains large amounts of phenolic
compounds. These by-products contain active components such as
caffeine and other polyphenols including tannins, flavanols, flavandiols, flavonoids, and phenol acids (Pandey et al., 2000; Ulloa
Rojas, Verreth, Amato, & Huisman, 2003) and have the potential
to be used as natural food preservatives (Gyawali, Adkins, Minor, &
Ibrahim, 2013). In the last few decades, research interest has
focused on the antibacterial properties of coffee and tea extract. The
antioxidative and antimicrobial effects of coffee pulp were investigated against rancidity and microbial growth on smoked fish
samples. Coffee pulp smoke has shown antioxidative effect on
rancidity in smoked fish and suppression of microbial load (coliform, fungal count) during three weeks of storage at room temperature (Adebowale, Ogunjobi, Olubamiwa, Olusola-Taiwo, &
Omidiran, 2012). However, studies on the antibacterial activity of
coffee by-products including coffee pulp and tea waste have been
very limited.
These studies have provided useful information on the utilization of by-products (peels, seeds, pulps, & husks) of different fruits
and vegetables as natural antimicrobials in foods. These byproducts could be of great benefit from economic and environmental perspectives as sources of low cost natural antimicrobials.
In addition, the waste produced by the processing industry could be
incorporated into antimicrobial packaging or utilized as edible
antimicrobial films (Taveira et al., 2010).
3. Antimicrobials of animal origin
Some of the potential antimicrobials of animal origin which
could be used as food additives are discussed below. In addition,
418
R. Gyawali, S.A. Ibrahim / Food Control 46 (2014) 412e429
other antimicrobials derived from animal sources which are not
discussed in this section are listed in Table 3.
3.1. Lactoferrin
Lactoferrin (Lf), an iron-binding glycoprotein present in milk, is
reported to possess antimicrobial activity against a wide range of
€ nnerdal, 2011). Recently, Lf has been
bacteria and viruses (Lo
approved for application on beef in the United States and has been
applied as an antimicrobial in a variety of meat products (Juneja,
Dwivedi, & Yan, 2012; USDA-FSIS, 2010). The antimicrobial properties of Lf against foodborne microorganisms including Carnobacterium, L. monocytogenes, E. coli, and Klebsiella have been
reported (Al-Nabulsi & Holley, 2005; Murdock, Cleveland,
Matthews, & Chikindas, 2007). Al-Nabulsi et al. (2009) reported a
reduction of 4 log CFU/ml of Cronobacter spp. in the presence of
2.5 mg/ml Lf in 0.2% peptone water within 4 h incubation at 37 C.
The effects of Lf alone and in combination with nisin on the
microbiological quality of meatballs were evaluated by Colak,
Hampikyan, Bingol, and Aksu (2008). Meatballs treated with a
mixture of Lf (0.2 mg/g) and nisin (0.1 mg/g) showed a significant
reduction in spoilage bacterial counts (total aerobic bacteria, coliform, E. coli, total psychrophilic bacteria, Pseudomonas spp., yeast
and molds) and extended shelf-life of up to 10 days. Lf hydrolyzate
has also been shown to reduce the population of E. coli O157:H7 and
L. monocytogenes by approximately 2 log in ultra-high temperature
milk (Murdock & Matthews, 2002). The results suggest that Lf hydrolyzate can limit the growth or reduce the population of pathogenic bacteria in a dairy product. Shimazaki (2000) investigated the
addition of Lf to rehydrated powder infant milk formula as a means
of inhibiting pathogenic microorganisms.
There are several explanations that may accounts for Lf's antimicrobial action. One is that it limits microbial access to nutrients
via iron chelation, which thereby produces an iron deficient melez-Ch
valo-Gallegos, & Rasco
n-Cruz, 2009).
dium. (Gonza
avez, Are
Another possibility is that Lf is capable of destabilizing the outer
membrane of Gram-negative bacteria, which results in liberation of
lipopolysaccharides with increased membrane permeability (Orsi,
2004). Support for this latter explanantion is provided by Jenssen
and Hancock (2009), who demonstrated that Lf can increase the
antibacterial effect of commercial drugs like rifampicin by
damaging the bacterial membrane.
Various published works have shown that Lf can provide iron for
the growth of Bifidobacterium spp. However, under defined environmental condition such as lack of minerals, Lf with bifidobacterial strains acts indirectly against the growth of pathogens (Gyawali
& Ibrahim, 2012). The mechanism enabling this appears to involve
microbial iron uptake (Bezkorovainy, Kot, Miller-Catchpole,
Haloftis, & Furmanov, 1996). Iron acts as a growth promoting factor for bifidobacteria, and bifidobacteria have the ability to bind
iron, thus making it unavailable to pathogens thus negatively
impacting their growth (Bezkorovainy & Miller-Catchpole, 1989).
Under low iron condition, these probiotic bacteria start producing
antimicrobial ‘bifidogenic’ compounds (Gyawali & Ibrahim, 2012;
Ibrahim, 2005) that can inhibit the growth of other harmful microorganisms. Thus, an Lf rich medium with bifidobacterial strains
can be used to improve microbiological safety and quality.
3.2. Chitosan
Among several natural antimicrobials, chitosan has received
considerable interest for commercial applications in food. Chitosan
is a polycationic biopolymer naturally present in the exoskeletons
of crustaceans and arthropods (Tikhonov et al. 2006). The application of chitosan as a food preservative and for other uses has been
limited by its insolubility at neutral and higher pH. Improvement of
its solubility could improve its application as a food preservative
(Du, Zhao, Dai, & Yang, 2009). The antibacterial activity of watersoluble chitosan derivatives prepared by Maillard reactions
against S. aureus, L. monocytogenes, B. cereus, E. coli, Shigella
Table 3
Antimicrobials of animal origin.
Antimicrobial agent
Major component
Major source
Target organisms
References
Lactoferrin
Iron binding glycoprotein
Milk
Chitosan
Polycationic biopolymer
compound
€nnerdal 2011; Perez,Taylor, &
Lo
Taormina (2012)
Leleu et al. (2011); Tiwari et al. (2009)
Lipids
Eicosapentaenoic
acid (EPA) and
Docosahexaenoic
acid (DHA)
Exoskeletons of
crustaceans
and arthropods
Fish and shellfish
Defensins
Cationic peptides
Lactoperoxidase
Glycoprotein
E. coli O157:H7, L. monocytogenes,
Salmonella, Pesudomonas
E. coli, S. aureus Pseudomonas spp.,
E. coli, and L.
monocytogenes
B. subtilis, L. monocytogenes, S. aureus
ATCC 6538, S. aureus KCTC 1916, and
Enterobacter aerogenes, E. coli,
E. coli O157:H7, Pseudomonas aeruginosa,
S. Enteritidis, and S. Typhimurium
Gram-positive and Gram-negative
bacteria, fungi, viruses
Salmonella, E. coli, S. aureus, L. monocytogenes,
Y.entericolitica
Ovotransferrin
Glycoprotein
(peptide OTAP-92)
Lysozyme
Glutamic acid,
aspartic acid
Polypeptides
Pleurocidin
Protamine
Casein and whey
Cationic antimicrobial
peptides
Bioactive peptides
(Isracidin as1 casein
f1-23; Casocidin-I
f150-188; Kappacin)
Mammalian epithelial
cells of chickens, turkeys
Raw milk, colostrum,
saliva and other
biological secretions
Egg albumin
Micrococcus, Bacillus spp., E. coli O157:H7,
L. monocytogenes, S. aureus
Hens' eggs,
mammalian milk
Myeloid cells and
mucosal tissues of
many vertebrates
and invertebrates
Salmon
C. tyrobutyricum, Bacillus, Micrococcus,
L. monocytogenes
L. monocytogenes, E. coli O157:H7, and
pathogenic fungi
Milk protein
Enterobacter sakazakii ATCC 12868,
E. coli DPC5063, S. aureus, L. monocytogenes,
S. Typhimurium, B. subtilis
L. monocytogenes, total bacteria, coliforms
Shin, Bajpai, Kim, and Kang (2007)
Tiwari et al. (2009)
Perez et al. (2012)
Ko, Mendonca, and Ahn (2008);
Ko, Mendonca, Ismail, & Ahn (2009);
Perez et al. (2012)
Juneja et al. (2012); Perez et al. (2012)
Burrowes, Hadjicharalambous,
Diamond, and LEE (2004);
Jung et al. (2007)
Juneja et al. (2012); Potter,
Truelstrup Hansen, and Gill (2005)
Hayes et al. (2006); Korhonen and
Rokka (2010)
R. Gyawali, S.A. Ibrahim / Food Control 46 (2014) 412e429
dysenteriae, and S. Typhimurium have shown to be a promising
commercial substitute for acid-soluble chitosan (Chung, Yeh, & Tsai,
2011). Similarly, the solubility limitation of native chitosan has been
overcome by using N-alkylated disaccharide chitosan derivatives
that exhibited antibacterial activity against E. coli and S. aureus
(Yang, Chou, & Li, 2005). In a study by Du et al. (2009), watersoluble chitosan at 2.0% showed strong inhibitory effects against
E. coli, B. subtilis, and S. aureus with diameters of inhibition zones
greater than 20 mm. Rhodes and Roller (2000) reported that mild
hydrolysis of chitosan improved microbial inactivation in saline and
a greater inhibition of growth of several spoilage yeasts in laboratory media. The addition of 0.3 mg of chitosan per ml eliminated
yeasts entirely for the duration of 13 days in pasteurized appleelderflower juice stored at 7 C. The antibacterial activity of chitosans was examined against several Gram-negative (E. coli,
P. fluorescens, S. Typhimurium, Vibrio parahaemolyticus) and Grampositive bacteria (L. monocytogenes, Bacillus megaterium, B. cereus,
S. aureus) by No, Young Park, Ho Lee, and Meyers (2002). Authors
reported that chitosan inhibited the growth of most of the tested
bacteria showing stronger bactericidal effects against Grampositive bacteria than Gram-negative bacteria at a concentration
of 0.1% in agar medium. Helander, Nurmiaho-Lassila, Ahvenainen,
Rhoades, and Roller (2001) studied the mode of action of chitosan
on Gram-negative bacteria (E. coli and S. Typhimurium) using
electron microscopy. This study showed that chitosan at 0.025%
caused extensive cell surface alterations and covered the outer cell
membrane with vesicular structures, thus explaining the loss of the
bacterial barrier function. Tsai, Wu, and Su (2000) investigated the
antimicrobial activity of a chitosan against various food poisoning
and food spoilage bacteria. The chitosan mixture retarded the
growth of Salmonella spp. and reduced the population of Staphylococcus spp. in raw milk. A chitosan concentration of 5.0 mg/ml
was used to determine the shelf-life of oysters stored at 5 ± 1 C
(Cao, Xue, & Liu, 2009). This study showed that chitosan treatment
extended the shelf-life of oysters from 8e9 days to 14e15 days,
indicating that chitosan has a great potential for seafood preservation. Our literature review indicates that chitosan has been
applied mainly as an antimicrobial packaging films and coatings as
discussed in this review under the section ‘incorporation of antimicrobials in food systems’.
3.3. Lysozyme
Lysozyme is an enzyme that is naturally present in avian eggs
and mammalian milk and is generally recognized as safe (GRAS) for
direct addition to foods (FDA, 1998). The white lysozyme of hen
eggs is a bacteriolytic enzyme widely reported for its application as
an antimicrobial in food products (Tiwari et al., 2009) and
commonly used as a preservative for meat, meat products, fish, fish
products, milk and dairy products, and fruits and vegetables
(Cegielska-Radziejewska, Lesnierowski, & Kijowski, 2009). The
antimicrobial activity of lysozyme is due to its ability to hydrolyze
the b-1, 4 linkage between N-acetylmuramic acid and N-acetylglucosamine in the peptidoglycan of the microbial cell wall (Juneja
et al., 2012). Lysozyme has been used primarily to prevent lateblowing defect in cheeses, caused by Clostrodium tyrobutyricum
(FDA, 1998). Lysozyme showed the highest antimicrobial activity
against Listeria innocua and Saccharomyces cerevisiae with an inhibition zone of 19.75 and 17.37 mm, respectively (Rawdkuen,
Suthiluk, Kamhangwong, & Benjakul, 2012). Peptides derived
from hen egg lysozyme at a concentration of 0.01 mg/ml showed
an inhibitory effect on both vegetative and spore forms of B. subtilis.
This result may be useful in controlling the growth of Bacillus
spoilage organisms as well as increasing the shelf-life of many food
419
products (Abdou, Higashiguchi, Aboueleinin, Kim, & Ibrahim,
2007).
As reported by Tiwari et al. (2009), the cell wall of Gram-positive
bacteria consists of peptidoglycan, which makes it susceptible to
the activity of lysozyme. This susceptibility is contrary to that of
Gram-negative bacteria which are generally resistant to lysozyme
due to their lipopolysaccharidic layer of outer membrane which
acts as a physical barrier. However, the susceptibility of Gramnegative bacteria to lysozyme can be increased by the use of detergents and chelators (EDTA) as membrane disrupting agents
(Branen & Davidson, 2004). These authors reported the synergistic
effect of lysozyme with EDTA against E. coli. The effect of different
chelating agents (EDTA, disodium pyrophosphate, & pentasodium
tripolyphosphate) in the presence of lysozyme on the inhibition of
E. coli O157:H7 was also investigated by Boland, Davidson, and
Weiss (2003). Their results indicated that the inhibition of E. coli
O157:H7 occurred with each lysozymeechelator combination.
Sinigaglia, Bevilacqua, Corbo, Pati, and Del Nobile (2008) also
studied the effectiveness of lysozyme and EDTA against the growth
of coliforms and Pseudomonadaceae on the microbiological shelflife of mozzarella cheese.
3.4. Milk-derived peptides
Milk-derived bioactive compounds such as casein and whey
proteins have been found to have multifunctional properties
including antimicrobial properties (Phelan, Aherne, FitzGerald, &
O'Bien, 2009; Schanbacher, Talhouk, Murray, Gherman, & Willett,
1998). These peptides have been found to be active against a
broad range of pathogenic microorganisms such as E. coli, Helicobacter, Listeria, Salmonella, Staphylococcus, yeasts, and filamentous fungi (Fadaei, 2012). In this section, we review the literature
pertaining to antimicrobial peptides derived from major milk
proteins such as caseins, a-lactalbumin and b-lactoglobulin upon
hydrolysis either by digestive proteases or by fermentation with
proteolytic lactic acid bacteria.
Casein accounts for 80% of total milk protein and is a rich source
of bioactive peptides. Antibacterial peptides have been identified
from aS1-casein and aS2-casein (McCann et al., 2006). Hydrolysis of
aS2-casein by chymosin released a compound called casocidin. This
has shown antibacterial properties against Staphylococcus spp.,
Sarcina spp., B. subtilis, Diplococcus pneumoniae, and Streptococcus
l, & Litwin
~ czuk,
pyogenes (Szwajkowska, Wolanciuk, Barłowska, Kro
2011). Isracidin is another casein derived peptide that has been
found to be effective against S. aureus, L. monocytogenes, and
C. albicans (Korhonen & Rokka, 2010). Hayes, Ross, Fitzgerald, Hill,
and Stanton (2006) reported antimicrobial activity of peptides
derived from milk proteins. Peptides such as casein A and B at
0.05 mM and 0.22 mM respectively, inhibited the growth of pathogenic strain Enterobacter sakazakii when tested using the agar well
diffusion assay. This indicates the potential application of these
peptides in milk-based formula, which has been linked to
E. sakazakii infection in neonates. Peptides generated from aS2casein, aS1-casein, and k-casein have shown antibacterial effects
against E. coli and B. subtilis (Elbarbary et al., 2012). Yak milk kcasein hydrolyzate at 0.5 mg/ml was also found to be effective
against E. coli (Cheng, Tang, Wang, & Mao, 2013).
The whey protein fraction of bovine milk consists mainly of blactoglobulin (b-LG) and a-lactalbumin (a-LA). Biologically active
antibacterial peptides are released during the digestion of blactoglobulin with trypsin. Szwajkowska et al. (2011) reported that
these peptides demonstrated antimicrobial activity against foodborne pathogens such as S. aureus, L. monocytogenes, Salmonella
spp. and E. coli O157. The antibacterial activity of peptides derived
from b-LG at concentration of 10e20 mg/ml was shown to inhibit
420
R. Gyawali, S.A. Ibrahim / Food Control 46 (2014) 412e429
the growth of L. monocytogenes and S. aureus in culture medium
(Demers-Mathieu et al., 2012). Similarly, peptides obtained by
tryptic hydrolysis and those obtained by chymotryptic hydrolysis of
bovine a-LA were identified as bactericidal to B. subtilis and
S. epidermidis (Pellegrini, Thomas, Bramaz, Hunziker, & von
€la
€ et al. (1999) also showed that
Fellenberg, 1999). Pihlanto-Leppa
bovine b-LG & a-LA hydrolyzate fractions enhanced bacteriostatic
properties against E. coli JM103. Synergistic effects in inhibiting
E. coli, S. Typhimurium, and Shigella flexneri resulted from peptide
fractions containing a-LA and glycomacropeptide at concentrations
of 0.25e0.05 mg/ml (Korhonen & Rokka, 2010). Cheng et al. (2013)
reported peptide accumulation on the cell membrane surface can
lead to increased permeability and accompanied leakage of cytoplasmic components, which ultimately results in cell death. However, the exact mode of action of antimicrobial peptides has not
been established.
4. Antimicrobials of bacterial origin
Microbes, especially lactic acid bacteria (LAB) produce a wide
range of chemicals with antimicrobial activity. Among these, the
proteinaceous compounds called bacteriocins such as nisin have
been shown to inhibit the growth and development of other microbial species. Similarly, reuterin produced from glycerol by some
strains of Lactobacillus reuteri is another widely used broadspectrum antimicrobial agent. Reuterin is also effective against
many pathogenic and spoilage microorganisms. In this section, we
discuss two widely recognized antimicrobials of bacterial origin:
bacteriocin and reuterin as natural preservatives. Some other antimicrobials that are derived from microorganisms are listed in
Table 4.
4.1. Bacteriocin
Nisin, the only bacteriocin approved for use as an antimicrobial
is used in over 50 countries world-wide. It is produced by Lactoccocus lactis and is active against Gram-positive and spore forming
s, Rodríguez, Nun
~ ez, & Medina,
bacteria associated with food (Arque
2011; Lucera, Costa, Conte, & Del Nobile, 2012; O'Sullivan, 2012).
Nisin acts as bactericide against Gram-positive foodborne pathogens or spoilage bacteria such as S. aureus, M. luteus, and B. cereus
(Rajendran, Nagappan, & Ramamurthy, 2013). It achieves this effect
by permeating the cytoplasmic membrane causing leakage of
intracellular metabolites and dissipation of membrane potential
(Lucera et al. 2012). Changes in Bacillus morphology causing
leakage of cytoplasmic contents were also reported in the presence
of nisin (Hyde, Parisot, McNichol, & Bonev, 2006). Davies, Bevis,
and Delves-Broughto (1997) conducted a shelf-life study of
ricotta cheese and found that the incorporation of nisin at
0.0025 mg/ml inhibited the growth of L. monocytogenes during 8
weeks of storage.
Bacteriocin is known to be more effective against Gram-positive
bacteria than Gram-negative bacteria. The resistivity of Gramnegative bacteria is explained by the presence of a protective
outer membrane that forms the outermost layer of the cell membrane. Moreover, researchers have found that nisin's activity
against Gram-negative bacteria can be enhanced when used
together with outer membrane disrupting agents (Belfiore,
Castellano, & Vignolo, 2007). Natural hydrophobic compounds
such as EOs are known to have outer membrane disrupting properties. Therefore, it has been suggested that combining bacteriocin
with EOs may enhance the inhibitory effect against Gram-negative
pez, and Omar
bacteria (Ghrairi & Hani, 2013). G
alvez, Abrioue, Lo
(2007) reported the enhancing effect of nisin by using exposure
to chelating agents (EDTA), sub-lethal heat, and osmotic shock and
freezing, because these treatments make the outer membrane of
Gram-negative microorganisms more permeable and therefore
more susceptible to nisin. Nisin in combination with EDTA has
exhibited antimicrobial activity against some Gram-negative
spoilage and pathogenic bacteria, such as E. coli, P. aeruginosa,
and S. Typhimurium (Martin-Visscher, Van Bleulkum, & Vederas,
2011). The antimicrobial activity against S. Enteritidis in minced
sheep meat was found to be stronger when nisin at 500 IU/g was
combined with oregano EO at 0.9% (Govaris, Solomakos, Pexara, &
Chatzopoulou, 2010). Recently, Field et al. (2012) used a mutagenesis approach by altering the amino acid sequence to develop nisin
derivatives with enhanced activity against both Gram-positive and
Gram-negative bacteria such as S. aureus, E. coli, S. enterica serovar
Typhimurium, and Cronobacter sakazakii. Nisin can be applied
either alone or in combination with other natural compounds as a
food preservative against foodborne pathogens and thus extend
product shelf-life. Nisin in combination with natamycin significantly inhibited fungal growth (yeasts/molds) in table olives
(Hondrodimou Kourkoutas, & Panagou, 2011) and in soft Galotyri
cheese, extending the shelf-life (>28 days) compared to control
samples (14e15 days) (Kallinteri, Kostoula, & Savvaidis, 2013).
Pediocin is another type of bacteriocin produced by Pediococcus
strains such as P. acidilactici and P. pentosaceus. Pediocins have been
used as food preservatives in vegetables and meat based products
(Papagianni & Anastasiadou, 2009). Most pediocins are thermostable peptides and function over a wide range of pH values. Pediocins have shown proven efficacy against both spoilage and
pathogenic organisms, including L. monocytogenes, E. faecalis,
S. aureus, and Clostridium perfringens (Juneja et al., 2012; Tiwari
Table 4
Antimicrobials of bacterial origin.
Antimicrobial agent
Source
Target organisms
References
Nisin
Pediocin
Clostridium spp., L. monocytogenes
L. monocytogenes, Enterococcus faecalis,
S. aureus, C. perfringens
Fungi
E. coli strains
Lucera et al. (2012)
Tiwari et al. (2009)
Acidophilin
Lactococcus lactis
Strains of Pediococcus
acidilactici and P. pentosaceus
Streptomyces natalensis
Lactobacillus
curvatus CRL705
L. acidophilus
Bulgaricin
L. bulgaricus
B. cereus, B. subtilis, Listeria ivanovii,
S. aureus
L. monocytogenes, S. aureus, B. subtilis, Helicobacter pylori
Helveticin
L. helviticus
L. monocytogenes, Clostridium botulinum
Plantaricin
L. plantarum
L. monocytogenes, S. aureus, S. Typhimurium, E. coli
Reuterin
Lactobacillus reuteri
L. monocytogenes, S. aureus, E. coli O157:H7, C. jejuni
Natamycin
Lactocin
Juneja et al. (2012)
Belfiore et al. (2007)
Oh, Kim, and Worobo (2000);
Siamansouri,Mozaffari, and Alikhani (2013)
Siamansouri et al. (2013); Simova, Beshkova,
& Dimitrov (2009)
O'sullivan, Ross, and Hill (2002);
Siamansouri et al. (2013)
Gong, Meng, and Wang (2010);
Siamansouri et al. (2013)
s et al. (2004)
Arque
R. Gyawali, S.A. Ibrahim / Food Control 46 (2014) 412e429
et al., 2009). The antimicrobial activity of pediocin against Oenococcus oeni and other wine bacteria has been reported by Diez et al.
(2012).
4.2. Reuterin
Reuterin (b-hydroxypropionaldehyde) is a molecule with antimicrobial activity towards a broad spectrum of foodborne pathogens and spoilage organisms. Its high solubility in water, resistance
to heat, proteolytic and lipolytic enzymes, and stability over a wide
range of pH values makes reuterin ideal bio-preservative for foods.
s et al., 2011; Vollenweider, Grassi, Ko
€ nig, & Puhan, 2003).
(Arque
s et al. (2011) demonstrated the antimicrobial activity of
Arque
reuterin in combination with different bacteriocins from lactic acid
bacteria against foodborne pathogens in milk at refrigerated temperature. A synergistic effect of reuterin in combination with nisin
was observed on L. monocytogenes and S. aureus. Reuterin from
L. reuteri DPC16 showed a significant reduction in bacterial population against Gram-positive (S. aureus, L. monocytogenes) and
Gram-negative (E. coli, S. Typhimurium) bacteria (Bian, Molan,
Maddox, & Shu, 2011). In another study, the effect of reuterin
from L. reuteri strain 12002 was tested against E. coli O157:H7 and
L. monocytogenes in ground pork (El-Ziney, Van Den Tempel,
Debevere, & Jacobsen, 1999). In this study, reuterin at 100 AU/g
reduced a 5 log of E. coli O157:H7 after 1 day of storage at 7 C.
L. monocytogenes was reduced by 3 log after 7 days of storage under
the same conditions. Likewise, reuterin in milk showed an inhibition of Gram-negative as well as Gram-positive pathogenic and
spoilage bacteria (Stevens, Vollenweider, & Lacroix, 2011). The use
of reuterin to control Gram-positive and Gram-negative pathogens
s
has been investigated in milk, dairy, and in meat products (Arque
et al., 2011; El-Ziney et al., 1999). These studies have shown that
reuterin have a higher antimicrobial activity on Gram-negative
than on Gram-positive pathogenic bacteria. Although the mechanism of antimicrobial activity is not yet clear, a recent study reported that the aldehyde form of reuterin is the bioactive agent
which causes an oxidative stress response by modifying thiol
groups in proteins and small molecules (Langa et al. 2013).
5. Algae and mushrooms
In recent years, there have been many reports of algae and
mushrooms as natural sources of bioactive compounds that have a
broad range of biological activity, such as antibiotic, antiviral,
antioxidant, antifouling, anti-inflammatory, cytotoxic, antimitotic
activity and other health promoting benifits (Bhagavathy et al.,
2011; Demirel, Yilmaz-Koz, Karabay-Yavasoglu, Ozdemir, & Sukatar, 2009; Plaza et al., 2010; Willis, Isikhuemhen, & Ibrahim, 2007).
However, there has been limited research devoted to the evaluation
of the antimicrobial activity of algae and mushrooms in food
preservation. The rich diversity of different algae and mushrooms
species could therefore offer a potential source of novel antimicrobials. This section deals with potential applications of these
species in controlling foodborne pathogens. Some examples of
algae and mushrooms, their antimicrobial components, and action
against pathogenic microorganisms are listed in Table 5.
5.1. Algae
The antimicrobial activity of different types of algae against
pathogenic bacteria has been identified by several scientists as
potential antimicrobial agents that may be useful in the food industry. Plaza et al. (2010) reported the antimicrobial activity of
algae (Himanthalia elongate) and microalgae (Synechocystis spp.)
against E. coli and S. aureus. Likewise, the antimicrobial activity of
421
phlorotannins isolated from marine brown algae has been shown to
inhibit the growth of foodborne pathogenic bacteria as well as
antibiotic resistant bacteria (Eom, Kim, & Kim, 2012). The interactions between phlorotannins and bacterial proteins are
considered to play an important role in bacterial inhibition. Salem,
Galal, and Nasr El-deen (2011) tested the antibacterial effects of
several marine algae against both Gram-positive (S. aureus NCIMB
50080 and B. cereus) and Gram-negative bacteria (E. coli NCIMB
50034, E. feacalis NCIMB 50030, Salmonella spp. and P. aeruginosa).
Several photosynthetic pigments and derivatives have been isolated from marine algae and have been found to have bactericidal
effects against the Gram-positive bacterium B. subtilis (Smith,
Desbois, & Dyrynda, 2010). Yamada, Itoh, Murakami, and Izumi
(1985) isolated halogenated compounds such as bromophenols
from different types of algae that have antibacterial properties.
Crude extracts of algae showed a strong inhibition against all tested
pathogens. However, Gram-positive bacteria were found to be
more susceptible to extracts producing a larger zone of inhibition
than Gram-negative bacteria. In a similar study, Devi, Suganthy,
Kesika, and Pandian (2008) reported a significantly higher zone
of inhibition produced by seaweed extract Haligra spp. at 50 mg/ml
concentration against Gram-positive food poisoning bacteria
S. aureus (MTCC 96) than the standard antimicrobial sodium benzoate at 200 mg/ml. Authors also determined the minimum
bactericidal concentration of Haligra spp. extract against S. aureus at
a concentration of 5 mg/ml in skimmed milk, demonstrating the
potential of this algae to be used in foods including dairy products,
raw meats, poultry, salads, shrimp, and ham. Extracts of several
microalgae were screened for their activity against common foodborne pathogens. Among the tested algae, extract of Scenedesmus
obliquus showed strong inhibition against Gram-positive (S. aureus)
and Gram-negative (Salmonella spp., E. coli, P. aeruginosa) bacteria
(Catarina, Barbosa, Amaro, Pereira, & Xavier, 2011).
Compounds reported to be present in algae included terpenoids,
phlorotannins, acrylic acid, phenolic compounds, steroids, halogenated ketones and alkanes, cyclic polysulphides, and fatty acids that
act as bactericidal agents (Watson & Cruz-Rivera, 2003). The
presence of these compounds suggests a number of alternative
mechanisms for antimicrobial action. For example, the presence of
long chain fatty acids may act in a similar fashion as most of the
plant extracts by promoting membrane damage that eventually
permit cell leakage (Catarina, Barbosa, Amaro, Pereira, & Xavier,
2011). The antifungal activity of seaweed extracts can be
explained by the presence of phenolic compounds and their impact
on spore germination. Some algal extracts have also been shown to
inhibit fungal enzyme activity due to the presence of bioactive
metabolites (Gallal, Salem, & Nasr El-deen, 2011).
5.2. Mushrooms
Among fungi, mushrooms are commonly eaten as food and have
been shown to possess antimicrobial properties (Gao et al., 2005;
Ishikawa, Kasuya, & Vanetti, 2001; Turkoglu, Duru, Mercan,
Kivrak, & Gezer, 2007; Willis, King, Iskhuemhen, & Ibrahim,
2009). The potential of several species of macrofungi to be used
as a good source of natural antibiotics and antioxidants and as a
possible food supplement was previously reported by Kalyoncu,
lam, Erdog
an, and Tamer (2010). Many researchers
Oskay, Sag
have identified the antimicrobial activity of different species of
these fungi due to the presence of several bioactive compounds.
Varieties of Australian basidiomycetous macrofungi extracts were
tested against Gram-positive (B. cereus, L. monocytogenes) and
Gram-negative bacteria (P. aeruginosa, Acinetobacter baumannii).
The ethanol extracts of all tested macrofungi inhibited the growth
of one or more of these pathogens at 10 mg/ml (Bala, Aitken,
422
R. Gyawali, S.A. Ibrahim / Food Control 46 (2014) 412e429
Table 5
Antimicrobials from algae and mushrooms.
Origin
Source
Major component
Target organisms
References
Marine algae
Gracilariopsis longissima
Vibrio spp.
Cavallo et al. (2013);
Demirel et al. (2009)
Brown algae
B. subtilis and S. aureus
Demirel et al. (2009)
Green algae
Colpomenia sinuosa, Dictyota dichotoma,
Dictyota dichotoma var. implexa, Petalonia
fascia and Scytosiphon lomentaria
Chlorococcum humicola
Polyphenols, carotenoids, amino acids,
and catechins (e.g., catechin, epigallocatechin,
epigallocatechin).
Hydrocarbons, terpenes, acids, phenols,
sulfur-containing compound, aldehydes
Bhagavathy et al.
(2011)
Brown algae
Himanthalia elongata
E. coli, S. aureus,
S. Typhiumurium,
P. aeruginosa,
V. cholerae
E. coli, S. aureus
Plazaa et al. (2010)
Red algae
Asparagopsis taxiformis, Laurencia
ceylanica, Laurencia brandenii, Hypnea
valentiae
Chlamydomonas
reinhardi, Chlorella vulgaris, Scendesmus
quadricauda
Ecklonia cava, E. kurome, E. stolonifera,
Eisenia aborea, Eisenia bicyclis,
Ishige okamurae, Pelvetia siliquosa
Fomitopsis lilacinogilva, Psathyrella spp.,
Ramaria spp., Hohenbuehelia spp.,
Agaricus spp., Lentinus spp.,
Strobilomyces spp.
Lycoperdon perlatum, Cantharellus
cibarius, Clavaria vermiculris,
Ramaria Formosa Quel, Marasmius oreades,
Pleurotus pulmonarius
Agaricus spp.
Pathogenic Vibrio strains
Manilal et al. (2009)
B. subtilis
Smith et al. (2010)
Phlorotannins
S. aureus, MRSA,
Salmonella spp., E. coli
Eom et al. (2012)
Grifolin, pleuromutilin, striatins A, B & C,
oudemansin, scorodonin, ganomycins,
retapamulin
S. aureus, B. cereus,
L. monocytogenes, E. coli
Bala et al. (2012)
Total phenols, flavonoid and ascorbic acid
S. aureus (ATCC 25923),
B. subtilis (ATCC 6633);
E. coli (ATCC 25922),
P. aeruginosa (ATCC 27853)
Micrococcus luteus,
Micrococcus flavus,
B. subtilis, B. cereus
B. cereus, B. subtilis
P. aeruginosa, E. coli
Ramesh and
Pattar (2010)
Flavonoid components, palmitic acid, linoleic
acid, ergosterol
Micrococcus luteus, B. cereus
Polysaccharides, triterpenes
Phenolics and flavonoids
B. subtilis, S. epidermidis
P. aeruginosa, S. Enteritidis,
E. coli, Y. enterecolitica,
S. aureus, B. cereus
^nia
Kitzberger, Sma
Jr,Pedrosa, and
Ferreira (2007)
Ren et al. (2014)
Turkoglu et al. (2007)
Marine algae
Marine
brown algae
Macrofungi
Non-gilled
fungal group
Edible mushroom
Edible mushroom
Edible mushroom
Lactarius deliciosus, Lactarius piperatu
Sarcodon imbricatus and Tricholoma
portentosum
Lentinula edodes
Edible mushroom
Fungi
C. sinensis, P. australis
Laetiporus sulphureus (Bull.) Murrill
Phytochemicals such as saponins, tannins,
carotenoids, flavonoids, alkaloids, glycosides
Phytol, fucosterol, neophytadiene or palmitic,
palmitoleic and oleic acids
Lipophilic compound (pyrrole-2-carboxylic
acid, pentadecanoic acid and
octadecanoic acid)
Chlorophyll derivatives
Fatty acids, b-carotene-linoleic acid, phenols,
& flavonoids
Total phenols, flavonoids, ascorbic acid,
b-carotene, lycopene
Cusack, & Steadman, 2012) indicating fungi as a potential source of
antimicrobials. Edible mushroom extract from the non-gilled
fungal group of Aphyllophorales were found to exhibit antimicrobial effects against pathogenic bacteria (Ramesh & Pattar, 2010).
The extract of these fungi produced zones of inhibition in the range
of 10e24 mm against tested Gram-positive (B. subtilis, S. aureus)
and Gram-negative bacteria (E. coli, P. aeruginosa). The antimicrobial effects of methanol extract of edible musrooms from Agaricus
spp. were tested against Gram-positive and Gram-negative bacteria. These extracts were found to be effective on Gram-positive
bacteria, especially against M. luteus, Micrococcus flavus, B. subtilis,
and B. cereus (Ozturk et al., 2011). The antimicrobial properties of
phenolic extracts of Portuguese wild edible mushroom species
(Lactarius deliciosus, Sarcodon imbricatus, and Tricholoma portentosum) against pathogens were also investigated by Barros et al.
(2007). These mushrooms showed a higher inhibition of Grampositive bacteria (B. cereus, B. subtilis), while Gram-negative bacteria (E. coli) were found to be resistant. The antimicrobial properties of shiitake mushrooms (Lentinula edodes) have been shown
against a wide range of Gram-positive and negative bacteria
including B. subtilis, B. cereus, P. aeruginosa, E. coli O157, and
methicillin-resistant S. aureus (Rao, Millar, & Moore, 2009). The
compound lentinan in shiitake mushrooms reportedly is the basis
for its antimicrobial action. Recently, Ren et al. (2014) tested the
antimicrobial effect of polysaccharide extracts of edible mushroom
Ozturk et al. (2011)
Barros et al. (2007)
species. The polysaccharide extracts from Cordyceps sinensis
inhibited the growth of Gram-positive strains B. subtilis, and
S. epidermidis. Another mushroom species, Pleurotus australis,
showed inhibition only against S. epidermidis while two other
Gram-negative strains (E. aerogenes, E. coli 916) were resistant to
mushroom extracts. The sensitivity of Gram-positive bacteria to
mushroom extracts is explained by the absence of membrane
bound periplasm. Instead, Gram-positive bacteria possess hydrophilic porus structure making cell walls more permeable. Similarly,
Venturini, Rivera, Gonzalez, and Blanco (2008) also reported the
resistivity of Gram-negative E. coli to extract of the mushroom
L. edodes.
The antimicrobial activity of mushrooms may be attributed to
the presence of various bioactive secondary metabolites, volatile
compounds, some phenols, gallic acids, free fatty acids and their
derivatives (Bala et al., 2012; Ramesh & Pattar, 2010). Thus,
mushrooms producing these bioactive components could support applications in the food industry as an effective source of
natural substances that could be used as preservatives in order
to ensure food preservation and safety. Considering the wide
biodiversity of mushrooms, they could easily become accessible
sources of antimicrobial compounds. Further investigation into
the potential use of mushrooms as food preservatives is warranted due to increasing interest in the search for more natural
alternatives.
R. Gyawali, S.A. Ibrahim / Food Control 46 (2014) 412e429
6. Incorporation of antimicrobials in food systems
Antimicrobials in foods can be added in different forms to
control the growth of pathogenic and spoilage microorganisms.
These can be either added directly or through slow release from
packaging materials. In this section, we highlight three major
methods of incorporating antimicrobials in food systems. These
methods could play an important role in reducing harmful microorganisms and thus extending product shelf-life.
6.1. Direct applications
Researchers have demonstrated the antimicrobial activity of
different natural compounds against a wide range of pathogenic
microorganisms. There have been a number of studies conducted in
culture media and tested in food products. These antimicrobial
compounds have been directly applied in food systems either in the
form of a powder or a liquid. In this section, we highlight the antimicrobial activity of compounds derived from plants in model food
systems. However, only a few natural antimicrobials have found
practical application in the food industry and their use in foods as
preservatives is often limited due to the strong smell and taste they
impart to these foods. In addition, natural antimicrobials' solubility
in complex food matrices is another limitation (Sokovi
c et al., 2010).
Budka and Khan (2010) demonstrated the effect of EOs from
basil, thyme, and oregano against B. cereus in rice-based foods.
Carvacrol (EO of oreganum and thyme) at 0.15 mg/g inhibited the
growth of B. cereus on rice (Ultee, Slump, Steging, & Smid, 2000).
Freshly ground garlic at a concentration of 1% was shown to reduce
Salmonella count when added to mayonnaise (Leuschner &
Zamparini, 2002). The antimicrobial activitiy of phenolic compounds from several plant species has been shown to inhibit
S. aureus in chicken soup (Had
zifejzovic et al., 2013). Yuste and Fung
(2002) reported 6 log CFU/ml reductions of L. monocytogenes in
pasteurized apple juice with 0.1e0.3% (w/v) of ground cinnamon
after 1 h of incubation, and no further growth of the microorganism
occurred during 7 days of storage. Cava Nowak, Taboada, and
Marin-Iniesteta (2007) evaluated the efficacy of EOs of cinnamon
bark, cinnamon leaf, and clove against L. monocytogenes in semi
skimmed milk incubated at 7 C for 14 days. They observed that the
MIC was 500 ppm for cinnamon bark EO and 3000 ppm for the
cinnamon leaf and clove EOs. These results indicated the possibility
of using these EOs in milk beverages as natural antimicrobials.
Similarly, Smith-Palmer, Stewart, and Fyfe (2001) reported the inhibition of L. monocytogenes and S. Enteritidis in both low fat and
full fat cheese in the presence of 1% clove, cinnamon, thyme, and
bay oil. The antimicrobial effect of rosemary extract against
L. monocytogenes was asssesd by Muneoz et al. (2009). When rosemary extract at 0.1 ml/100 ml concentration obtained by super
critical fluid extraction method was tested against L. monocytogenes
at 30 C in broccoli juice and incubated for 30 days, a bactericidal
effect was observed.
The use of natural antibacterial compounds such as extracts of
spices, herbs, and EOs, has been reported in the literature to
improve the shelf-life of meat. The shelf-life of meat-based products increased when products were dipped in thyme and oregano
oil at 0.1 and 0.3% (Karabagias, Badeka, & Kontominas, 2011). The
combination of thyme EO at 0.6% with nisin at 1000 IU/g significantly decreased the population of L. monocytogenes in minced beef
during storage at 4 and 10 C (Solomakosa, Govaris, Koidis, &
Botsoglou, 2008). A synergistic effect of rosemary extracts with
pre-freezing was shown to reduce C. jejuni populations by more
than 2.0 logs in chicken meat (Piskernik, Klancnik, Riedel,
Brøndsted, & Mo
zina, 2011). Xi, Sullivan, Jackson, Zhou, and
Sebranek (2011) investigated the effect of cranberry powder
423
against L. monocytogenes growth in meat model system. The results
showed a 2e4 log CFU/g reduction in bacterial population at concentrations of 1e3% when compared to the control sample treated
with nitrite. This showed a possibility of using natural ingredients
such as cranberry powder instead of sodium nitrite to enhance the
antibacterial quality and shelf-life of naturally cured meat.
Overall, plant extracts could be used as natural antimicrobial
additives to prolong the shelf-life of foods. However, the level of
these preservatives required for sufficient inhibition of microorganisms in foods may be considerably higher in comparison to
laboratory media. Because this higher concentration may negatively impact the organoleptic properties of food, the use of natural
compounds in combination with other natural preservatives or
with other technologies could produce synergistic effects against
foodborne pathogens.
6.2. Edible films and coatings
In recent years, food-packaging industries have shown an interest in edible films and coatings from natural antimicrobials.
Edible films also improve food quality by providing barriers to
moisture, and oxygen, and could serve as a barrier to surfacecontaminating microorganisms (Cao et al., 2009; Jang, Shin, &
Song, 2011; Joerger, 2007). In addition, edible films and coatings
help reduce environmental concerns created by conventional
plastic packaging. Various approaches have been proposed and
demonstrated for the use of edible films and coatings to deliver
antimicrobial compounds to a variety of food surfaces, including
fruits, vegetables, and meat products (Devlieghere, Vermeulen, &
Debevere, 2004; Ye, Neetoo, & Chen, 2008).
Ayala-Zavala et al. (2013) demonstrated the antimicrobial activity of an edible film formulated with cinnamon leaf oil that can
be useful in preserving the quality of fresh-cut peaches. Similarly,
Raybaudi-Massilia, Rojas-Grau, Mosqueda-Melgar, and MartinBelloso (2008) reported the reduction of E. coli O157:H7 population by >4 logs on fresh cut Fuji apples with cinnamon, clove, and
lemongrass oils at 0.7%, or their active compounds, cinnamaldehyde, eugenol, and citral, at 0.5% incorporated into alginate films. In
another study, the addition of grapefruit seed extract to the rapeseed proteinegelatin film inhibited the growth of E. coli O157:H7
and L. monocytogenes in strawberries (Jang, et al., 2011). The antimicrobial activity of the polypropylene/ethylene-vinyl alcohol
copolymer (PP/EVOH) films with 5% oregano EO against pathogenic
microorganisms E. coli, S. enterica and L. monocytogenes and natural
microflora was recently investigated by Muriel-Galet et al. (2012)
on packaged salads. The authors' findings showed a reduction in
spoilage flora as well as inhibition of the growth of pathogens on
contaminated salads. The antimicrobial activity of apple-based
edible films containing plant antimicrobials (cinnamaldehyde and
carvacrol) was also investigated by Ravishankar, Zhu, Olsen,
McHugh, and Friedman (2009). These films were shown to be
effective against S. enterica and E. coli O157:H7 on poultry, and
against L. monocytogenes on ham.
Similarly, chitosan based films have proven to be very effective
in food preservation. The shelf-life of carrot sticks coated with
chitosan was evaluated. An edible coating containing 0.005 ml/ml
chitosan applied to carrot sticks under modified atmospheric
packaging over 12 days at 4 C was shown to maintain quality and
~es, Tudela, Allende, Puschman, & Gil,
prolong the shelf-life (Simo
2009). The antimicrobial effects of edible chitosan films contain,
ing nisin, peptide P34, and natamycin were investigated by Ce
~ a, and Brandelli (2012) against L. monocytogenes, B. cereus,
Noren
S. aureus, E. coli, S. Enteritidis, C. perfringens, Aspergillus phoenicis,
and Penicillium stoloniferum. These chitosan films were effective in
controlling microbial growth in minimally processed pears and
424
R. Gyawali, S.A. Ibrahim / Food Control 46 (2014) 412e429
could thus be a feasible method for the biopreservation of food.
Chitosan was also shown to possess a film-forming property, to
decrease water vapor and oxygen transmission, diminish respiration rate, and increase the shelf-life of fruit (Jiang & Li, 2001).
Incorporation of chitosan-coated films with green tea extracts (4%)
inhibited the growth of L. monocytogenes on ham steak during
storage at room and refrigerated temperature (Vodnar, 2012).
Similarly, Leleu et al. (2011) reported the use of chitosan coatings to
reduce bacterial contamination of egg contents resulting from
trans-shell penetration by S. Enteritidis and other bacteria, such as
Pseudomonas spp., E. coli, and L. monocytogenes.
The antibacterial activity of soy protein edible films incorporated with oregano or thyme EOs was tested on fresh ground beef
patties at 4 C. Films with 5% of EOs significantly inhibited the
lu, Yemiş,
growth of Pseudomonas spp. and coliform counts (Emirog
an, 2010). Increased concentrations of catechin in
Coşkun, & Candog
a film used during storage of sausages resulted in a decrease in
E. coli O157:H7 and L. monocytogenes populations (Ku, Hong, &
Song, 2008). Nisin-incorporated polymer films have shown to
control the growth of undesirable bacteria, thereby extending the
shelf-life and enhancing the microbial safety of meats (Cutter,
Willett, & Siragusa, 2001). The effectiveness of active films using
antibacterial peptides of Bacillus licheniformis Me1 against
L. monocytogenes in dairy products was recently demonstrated by
Nithya, Murthy, and Halami (2013). Their results showed that
antimicrobial peptide from films diffused slowly into the foodmatrix (paneer) during the storage period, thereby extending the
shelf-life of the product.
The incorporation of antimicrobials in food packaging as films
and coatings could prevent surface growth in foods where a large
portion of spoilage and contamination occurs. This approach also
reduces the addition of larger quantities of antimicrobials that are
usually incorporated into the bulk of the food. The gradual release
of an antimicrobial compound from packaging films and coatings to
the food surface could have an advantage over direct application of
antimicrobials in food systems (Appendini & Hotchkiss, 2002).
Franssen, Krochta, and Roller (2003) reported that food packaging
prepared from edible antimicrobial coatings containing polypeptides, such as lysozyme, peroxides, and lactoferrins have been
shown to extend the shelf-life of food products and make them
safer for human consumption, in addition to providing physical
protection for the food. These studies suggest that the food industry
and consumers could use these films and coatings to control surface contamination by foodborne pathogenic microorganisms.
6.3. Nanoparticles
Nanotechnology has been developing rapidly as one of the most
significant technological advances of our time. Nanoscience and
nanotechnology have already been applied in various fields
including medicine and the food industry (Sozer & Kokini, 2009). In
the last few years, the application of nanotechnology to food safety
has attracted the attention of many researchers due to its considerable potential for the development of antimicrobial delivery
systems (Zou, Lee, Seo, & Ahn, 2012). This technology could be used
to improve antimicrobial stability and could be applied directly or
as a coating or packaging in different food systems to inhibit the
growth of foodborne pathogens. Applications of nanotechnology to
deliver antimicrobials have been reported in several studies.
However, the study of nanoparticles as antimicrobials in food
models is very limited due to the complexity of food components.
Some of the recent studies that have been effectively applied in
food models using natural compounds are discussed in this section.
Zou et al. (2012) demonstrated the potential use of liposomal
nanoparticles for enhancing the antimicrobial efficacy of nisin
against L. monocytogenes and S. aureus in food systems. The antimicrobial activity of free nisin and nisin loaded solid lipid nanoparticles
was also studied by Prombutara, Kulwatthanasal, Supaka, Sramala,
and Chareonpornwattana (2012). The results of their study showed
stable and longer antimicrobial activity of nisin loaded nanoparticles
against L. monocytogenes DMST 2871 compared to free nisin, indicating that the nisin was released from nanoparticles throughout the
storage period. In raw and cooked chicken meat systems, naturally
occurring phenolic compounds delivered by nanoparticles were
proven to be more effective against S. Typhimurium and
L. monocytogenes at much lower concentrations than when delivered
individually without nanoparticles (Ravichandran, Hettiarachchy,
Ganesh, Ricke, & Singh, 2011). These findings demonstrate the potential for nanoparticles to be used for food safety applications such
as the delivery of phenolic compounds for pathogen reduction.
EOs are widely used natural compounds of plant origin. However, the poor water-solubility of EOs makes it difficult to incorporate them into foods and reduces antimicrobial action (Weiss,
Gaysinsky, Davidson, & McClements, 2009). Therefore, a higher
concentration of EOs is required to achieve higher antimicrobial
efficacy which could alter the sensory properties of foods. In a
recent study, Shah, Davidson and Zhong (2012a, 2012b) reported a
nanodispersion method to overcome this challenge. A follow-up
study by Shah et al. (2012b) reported improved antimicrobial activity of nanodispered eugenol against E. coli O157:H7 and
L. monocytogenes in bovine milk. Thymol-containing nano-dispersions are also effective against pathogens in food applications. Shah
et al. (2012a) also investigated the efficacy of thymol dispersed in
whey protein isolate and maltodextrin nanocapsules to inhibit
E. coli O157:H7 and L. monocytogenes in apple cider and 2% reducedfat milk. More recently, Xue et al. (2013) demonstrated the higher
antilisterial activity of nanoemulsified thymol in milk compared to
free thymol. In this study, authors reported the reduction of
L. monocytogenes from ~5 log CFU/ml to below the detection limit in
6 h by nanoemulsified thymol in skim and 2% fat milk. In full fat
milk, the bacterial population was reduced to undetectable limits
after 48 h of incubation at room temperature. In all tested food
systems, nano-encapsulated EOs were more evenly distributed
even at higher concentrations above the solubility limit than free
EOs, thus resulting in higher antimicrobial efficacy.
The application of antimicrobial compounds that have been
widely applied to microbial control in food products and processing
environments has met with several limitations including undesirable flavor, low solubility, and instability (Zou et al., 2012). The
efficacy of such antimicrobial properties is exhausted due to interactions with food components (proteins and lipids), inactivation
by enzymatic degradation or uneven distribution of antimicrobial
compounds within the complex food systems (Prombutara et al.,
2012). Nanoscale antimicrobial delivery systems could enhance
the efficacy of antimicrobials by improving their solubility and
dispersibility and thus improve the quality of food products.
Nanotechnology is also being developed in the areas of food
packaging. The incorporation of nanomaterials into food packaging
has been shown to improve food quality in fresh fruits and vegetables, bakery products and confectionery by protecting food from
moisture, lipids, gases, off-flavors and odors (Sozer & Kokini, 2009).
Despite all of the potential applications, nanotechnology is still a
new subject in the field of food safety. The specific properties and
characteristics of nanomaterial used in food applications need to be
carefully examined for any potential health risks.
7. Conclusion
Since, there is a growing demand for food that is free of synthetic chemicals as preservatives, it is necessary to examine and
R. Gyawali, S.A. Ibrahim / Food Control 46 (2014) 412e429
identify alternative and safe approaches for controlling foodborne
pathogens. Even though many natural products are currently being
used for the preservation and extension of the shelf-life of foods,
there are still many unexplored sources. The use of natural compounds from plant by-products, algae, and mushrooms could open
up the possibility of using these compounds as novel antimicrobials. Utilization of these products could also be a more costeffective way to produce antimicrobials. However, despite their
potential, the use of natural antimicrobials in food systems remains
limited mainly due to the side effects of undesirable flavor or
aroma. Therefore, further research is needed to determine the optimum levels of antimicrobials that can be safely applied in food
systems without unduly altering any sensory characteristics. An
alternative approach would be to utilize one or more compounds
that could produce synergistic effects at low concentrations
without altering any sensory characteristics of the food.
In complex food matrices, active natural compounds could bind
with other hydrophobic compounds such as some proteins and
lipids. This interaction could limit the availability of the natural
compound as an antimicrobial. In addition, processing steps could
also reduce the antimicrobial activity of such compounds. Nanoparticles hold tremendous potential as an effective antimicrobial
delivery system and could be employed to incorporate natural
antimicrobials that result in safer food products. However, the use
of nanotechnology in food has raised a number of concerns over
their safety to the consumers. Therefore, there continues to be a
need to develop a more practical and effective delivery system for
these antimicrobial compounds in food products. Furthermore,
safety and health risks of natural antimicrobials need to be assessed
before future applications in food products.
Acknowledgment
This work was made possible by grant number NC.X-267-5-12170-1 from the USDA, National Institute of Food and Agriculture
and its contents are solely the responsibility of the authors and do
not necessarily response the official view of the National Institute of
Food and Agriculture. The authors would like to thank Dr. Keith
Schimmel for his support while conducting this work.
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