Meat Science 145 (2018) 245–255

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Meat Science
journal homepage: www.elsevier.com/locate/meatsci

Review

Application of plant extracts to improve the shelf-life, nutritional and T

health-related properties of ready-to-eat meat products
⁎
Nooshin Nikmarama,b, , Sravanthi Budarajuc, Francisco J. Barbad, Jose M. Lorenzoe,
⁎⁎
Ryan B. Coxc, Kumar Mallikarjunanc, Shahin Roohinejadc,f,
a
Department of Food and Human Nutritional Sciences, University of Manitoba, Winnipeg, Manitoba, Canada
b
Richardson Centre for Functional Foods and Nutraceuticals (RCFFN), University of Manitoba, Winnipeg, Manitoba, Canada
c
Department of Food Science and Nutrition, University of Minnesota, St. Paul, MN 55108, USA
d
Nutrition and Food Science Area, Preventive Medicine and Public Health, Food Science, Toxicology and Forensic Medicine Department, Universitat de València, Burjassot,
València, Spain
e
Centro Tecnológico de la Carne de Galicia, rúa Galicia n° 4, Parque Tecnológico de Galicia, San Cibrao das Viñas, 32900 Ourense, Spain
f
Burn and Wound Healing Research Center, Division of Food and Nutrition, Shiraz University of Medical Sciences, Shiraz, Iran

A R T I C LE I N FO A B S T R A C T

Keywords: Plant extracts are increasingly becoming important additives in food industry due to their antimicrobial and
RTE meat products antioxidant abilities that delay the development of off-flavors and improve the color stability in ready-to-eat
Plant extracts (RTE) meat products. Due to their natural origin, they are excellent candidates to replace synthetic molecules,
Antimicrobial properties which are generally considered to have toxicological and carcinogenic effects. The efficient extraction of these
Nutritional properties
antioxidant molecules from their natural sources, along with the determination of their activity in the com-
mercialized products, have been a great challenge for researchers and food chain contributors. The objective of
this review is to highlight the application of plant extracts to improve the shelf-life, nutritional and health-
related properties of RTE meat products. The sensory effects of these extracts on RTE meat products as well as
the possible synergistic effects of a combination of extracts are discussed.

1. Introduction foods, antioxidant bioactive compounds can be incorporated into pro-

With the increasing demand for easily prepared ready-to-eat (RTE)
foods and globalization, concerns for food safety and quality are also
increasing. Perishable food products, especially meat products are
subjected to bacterial and fungal contamination causing undesirable
reactions that deteriorate flavor, odor, color, sensory, and textural
properties. Lipid oxidation is the other major issue concerning meat
that deteriorates the quality of products during processing and storage.
Lipid oxidation is the process where an unsaturated fatty acid fraction
of membrane phospholipids is oxidized. Membrane phospholipids are
sensitive to oxidation in meat due to their more unsaturated fatty acids
in comparison with other lipids. However, lipid oxidation is also af-
fected by the degree of unsaturation of the fatty acids in the phospho-
lipid and triglyceride fractions (Igene et al., 1980). As a result, the
formation of hydroperoxides and their secondary products (e.g. short-
chain aldehydes and ketones) causes undesirable flavors in the meat
products (Maqsood & Benjakul, 2011). To inhibit the growth of un-
desirable microorganisms and reduce lipid oxidation in RTE meat-based
duct formulation, coated on its surface, or incorporated into the
packaging material (Horita et al., 2018; Granato, Nunes, & Barba, 2017;
Nikmaram et al., 2017; Lorenzo et al., 2018; Lorenzo, Batlle, & Gómez,
2014). In this regard, synthetic antioxidants such as butylated hydro-
xytoluene (BHT), are extensively used to delay or prevent lipid oxida-
tion by either scavenging the chain-carrying peroxyl radicals or
avoiding the formation of free radicals. With increasing concern over
the safety of these synthetic compounds, research is being carried out to
find novel and naturally occurring compounds that preserve the sensory
and microbial quality of meat products Roohinejad, Mousavi
Khaneghah, et al., 2017; Ciriano et al., 2009; Johnston, Sepe, Miano,
Brannan, & Alderton, 2005). Consumers do not prefer synthetic anti-
oxidants because of their carcinogenicity (EFSA, 2011; EFSA 2012) and
have resulted in the development of “clean label” products. Moreover,
consumer's preference for natural food additives and concern regarding
the safety of synthetic preservatives prompted the food industry to look
for natural alternatives (Roohinejad, Nikmaram, et al., 2017; Aziz &
Karboune, 2018). Therefore, natural antioxidants have greater

⁎
Correspondence to: Nooshin Nikmaram, Department of Food and Human Nutritional Sciences, University of Manitoba, Winnipeg, Manitoba, Canada.
⁎⁎
Correspondence to: Shahin Roohinejad, Department of Food Science and Nutrition, University of Minnesota, St. Paul, MN 55108, USA.
E-mail addresses: nikmaran@myumanitoba.ca (N. Nikmaram), sroohine@umn.edu (S. Roohinejad).

https://doi.org/10.1016/j.meatsci.2018.06.031
Received 23 March 2018; Received in revised form 21 May 2018; Accepted 25 June 2018
Available online 27 June 2018
0309-1740/ © 2018 Elsevier Ltd. All rights reserved.
N. Nikmaram et al.
Fig. 1. Schematic of application of plant extracts to control the microbiological activity as well as to increase the nutritional and sensory properties in RTE meat-
based products.
application potential in the meat industry because of the consumer's
acceptability over the synthetic antioxidants (Fernandes, Trindade,
Lorenzo, et al., 2016; Munekata et al., 2017; Pateiro, Lorenzo, Amado,
& Franco, 2014). In this context, plant extracts are gaining a wide in-
terest in the food industry for their potential as antimicrobials and
antioxidants since they are also Generally Recognized as Safe (GRAS)
(Vinceković et al., 2017; Kim, Cho, & Han, 2013) and should not ne-
gatively influence sensory properties (e.g. color, odor or flavor); be ef-
ficient at low concentrations (0.001–0.01%); be compatible with the
foods and have the ease of application; be stable during processing and
shelf-life; and economic. Most importantly, these components and their
metabolites must be nontoxic at larger doses than those normally in-
gested by regular diets (Lorenzo et al., 2018). The current review fo-
cuses on the use of natural plant extracts to control the microbiological
activity as well as to increase the nutritional and sensory properties of
RTE meat-based products (Fig. 1).
2. Ready-to-eat meat products
RTE meat is defined as a meat or poultry product that is edible
without additional preparation to achieve food safety (9 Code of
Federal Regulations, Part 430). It may receive additional preparation to
make the product more palatable (e.g., frozen and/or refrigerated meat
and poultry products). These are mainly (but not exclusively) grouped
into two categories, deli meats, and hot dogs. Deli meats are sold at the
delicatessen counter or pre-packaged, which include but are not limited
to: baked or boiled ham, turkey ham, chicken roll, roast beef, corned
beef, bologna, and salamis. These products could be in various forms
such as pre-sliced, intact as a loaf, sandwich, mixed into a salad or
simply cut into pieces. RTE meat products have become increasingly
popular due to the convenience in preparation, time-saving and good
taste. RTE products are manufactured at intermediate temperatures
with the final product temperatures typically in the range of 65–75 °C.
They are different from canned products that are processed at high
temperatures for sterility/total microbial lethality (Horita et al., 2018).
Thus, RTE foods and especially muscle foods require refrigeration and
are generally referred to as cold cuts. Despite the popularity, RTE meat
and poultry are vulnerable to the foodborne outbreak associated with
the pathogens such as Listeria monocytogenes and spoilage micro-
organism such as lactic acid bacteria. The contamination by micro-
organisms in RTE products occurs mostly after the cooking step and it
continues further during the shelf life of the product causing foodborne
diseases (Horita et al., 2018). Listeria monocytogenes can grow at re-
frigeration temperatures and tolerate salts and nitrites (Ivy, Wiedmann,
& Boor, 2012; McClure, Beaumont, Sutherland, & Roberts, 1997). Since
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Meat Science 145 (2018) 245–255
1983, the United States Department of Agriculture (USDA) - Food
Safety and Inspection Service (FSIS) has been conducting regular mi-
crobiological testing on RTE meats to ensure product safety. The risk of
RTE meat and poultry products to L. monocytogenes outbreaks proves to
be a global concern. In order to increase the microbial safety, meat and
meat products are subjected to various treatments during processing.
High-pressure processing is one of these technologies. When meat
samples are subjected to > 30 0Mpa pressure, it results in the formation
of secondary lipid oxidation products which affects on the quality and
shelf life attributes of RTE meat products (Kumar et al., 2015). Tre-
mendous efforts have been made in the food industry on developing
technologies to minimize microbial contamination and to increase the
quality of RTE meat products. The incorporation of plant extracts in the
product formulation has been receiving attention in the meat industry
due to their beneficiary natural antimicrobial and antioxidant proper-
ties. The following sections focus on the application of various plant
extracts as antimicrobial agents and their role in enhancing sensory
properties.
3. Plant extract properties
3.1. Antioxidant potential of plant extracts
Due to potential negative health effects (e.g. toxicological and nu-
tritional) of synthetic antioxidant compounds at high concentrations,
application of natural plant antioxidants has gained attention
(Omidizadeh et al., 2011; Bouaziz, Koubaa, Barba, Roohinejad, &
Chaabouni, 2016; Fernandes et al., 2016; Roohinejad et al., 2016;
Taghvaei & Jafari, 2015; Roohinejad, Everett, & Oey, 2014). Several
compounds with antioxidant activity have been identified in plant ex-
tracts, in which phenolic compounds are considered as the major active
group (Roohinejad et al., 2017; Zhu et al., 2017; Lu, Kelly, & Miao,
2016; Roselló-Soto et al., 2015; Barba, Esteve, & Frígola, 2014). The
highly effective antioxidant properties of phenolic compounds have
been associated with their free radical scavenging capability, their
potential chelation of pro-oxidant metals, their role as reducing agents,
and quenchers of singlet oxygen (Mohajer, Taha, Ramli, & Mohajer,
2016; Roohinejad et al., 2014). Phenolic compounds are categorized
into 4 general groups including phenolic acids (e.g. gallic, proto-
chatechuic, caffeic, and rosmarinic acids), phenolic diterpenes (e.g.
carnosol and carnosic acid), flavonoids (e.g. quercetin and catechin),
and volatile oils (e.g. eugenol, carvacrol, thymol, and menthol) (Şahin
et al., 2018; Barba, Esteve, & Frígola, 2014; Shan, Cai, Sun, & Corke,
2005).
It has been reported that plant pigments such as anthocyanin and
N. Nikmaram et al.
Fig. 2. The main plant phenolic compounds including phenolic acids, flavonoids, and tannins (Guil-Guerrero et al., 2016).
betalains also exhibit antioxidant activity (Koubaa et al., 2016; Barba
et al., 2017). Changes in anthocyanin activity have been linked to the
variation of the metal ions and co-existing colorless compounds such as
co-pigments, flavones, and flavonols. Moreover, a direct link has been
found between anthocyanin level and reduction of cytotoxicity activity
(Mohajer, Taha, Ramli, & Mohajer, 2016). Cai, Sun, & Corke (2003)
revealed that the free radical scavenging activity of betalains from
plants of the Amaranthaceae family usually increase with the numbers
of hydroxyl/amino groups and also depends on the position of hydroxyl
groups and glycosylation of aglycones in the betalain molecules. Car-
otenoids are efficient antioxidants for scavenging singlet molecular
oxygen and peroxyl radicals. They are considered as part of the anti-
oxidant defense system in the human organism (Stahl & Sies, 2003).
Minerals (e.g. selenium, copper, manganese, and zinc) and vitamins
(vitamin E, C, and A) present in plants are well known natural anti-
oxidants. Selenium (Se) is considered the mineral that is most specifi-
cally associated with the antioxidant function. There are at least 35
antioxidant Se-based proteins including selenoprotein P, five glu-
tathione peroxidases and three thioredoxin reductases (Nakamura,
2005). Tocopherols (Vitamin E) acts as a membrane-bound antioxidant,
trapping lipid peroxyl free radicals produced from unsaturated fatty
acids under conditions of “oxidative stress.” Ascorbic acid (Vitamin C)
eliminates peroxyl radicals and easily gives up electrons to provide
stability to reactive species such as reactive oxygen species (McDowell,
Wilkinson, Madison, & Felix, 2007).
There are several factors which affect antioxidant activity such as
concentration, temperature, pH and processing conditions (Falowo,
Fayemi, & Muchenje, 2014). For utilization in food products, a natural
antioxidant should satisfy several requirements (e.g. being heat stable).
For example, the effect of an antioxidant compound should be main-
tained for at least one year at a temperature ranging between 25 and
30 °C (Gazzani, Papetti, Massolini, & Daglia, 1998; Taghvaei & Jafari,
2015). In this regard, the influence of thermal treatment (100 °C in a
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Meat Science 145 (2018) 245–255
furnace and autoclave for 15, 30 and 60 min) on the polyphenolic level
and antioxidant activity in grape pomace and grape seed extract was
evaluated by Chamorro, Goñi, Viveros, Hervert-Hernández, & Brenes
(2012). They observed no changes in the antioxidant activity and total
polyphenols content of grape seed extract or grape pomace during the
thermal process.
3.2. Antimicrobial properties of plant extract
As a result of higher consumer demand for “natural” and “pre-
servative-free” products, the food industry is paying more attention to
natural and/or naturally-derived antimicrobials to control micro-
biological load in food products (Mir et al., 2018). Plant extracts such as
essential oils (EOs) have indicated antimicrobial activity against both
foodborne pathogenic and spoilage microorganisms (Hashemi et al.,
2017; Roohinejad, Koubaa, et al., 2017; Hyldgaard, Mygind, & Meyer,
2012; Monu, Techathuvanan, Wallis, Critzer, & Davidson, 2016).
Application of several EOs (e.g. thyme, clove and cinnamon oils)
proved to be useful in controlling many pathogenic and spoilage bac-
teria (Davidson, Critzer, & Taylor, 2013; Kalemba & Kunicka, 2003).
Their activity was reported to be mainly associated with their major
compounds such as thymol, eugenol, carvacrol and trans-cinnamalde-
hyde (Bullerman, Lieu, & Seier, 1977; Kim, Marshall, & Wei, 1995;
Lambert, Skandamis, Coote, & Nychas, 2001). The mechanism of action
of EOs, as with other phenolic compounds, consists of disturbing the
cytoplasmic membrane and disrupting the proton motive force, electron
flow, active transport, and coagulation of cell contents (Burt, 2004).
Phenolic acids are present in a wide variety of plants mainly in
seeds, fruit, peels, and leaves. It has been reported that caffeic acid
exerts effects against viruses, bacteria, and fungi, while eugenol has
been classified as bacteriostatic (Cowan, 1999). The mechanism of ac-
tion for low-molecular-weight phenolic acids is described by the dif-
fusion of the non-dissociated acid across the membrane, causing the
N. Nikmaram et al.
acidification of the cytoplasm and occasionally, cell death (Sánchez-
Maldonado, 2014). It should be noted that several factors (e.g. pH, ring
substitutions, and the saturation of the side chain) play a vital role in
the activity of cinnamic acids (Almajano, Carbó, Delgado, & Gordon,
2007; Sánchez-Maldonado, 2014). Flavonoids have shown antibacterial
activity, inhibition of bacterial virulence and a synergism activity with
antibiotics. The mechanisms by which they exert antimicrobial activity
are attributed to the suppression of several bacterial virulence factors,
quorum-sensing signal receptors, enzymes, and toxins (Cushnie &
Lamb, 2011). Tannins exhibit antimicrobial activity through several
mechanisms; namely prevention of extracellular microbial enzymes
(e.g. carboxymethyl cellulase, proteases, glutamate dehydrogenase),
deprivation of the substrates needed for microbial growth and inhibi-
tion of oxidative phosphorylation, which influences microbial meta-
bolism (Guil-Guerrero et al., 2016). Few authors explained the me-
chanisms of action by which flavanols exert their effects such as the
aggregation of bacterial cells (Cushnie, Hamilton, Chapman, Taylor, &
Lamb, 2007), prevention of virulence phenotypes and gene expression
regulated by quorum sensing (Lee et al., 2009). Fig. 2 shows the main
plant phenolic compounds including phenolic acids, flavonoids, and
tannins.
Alkaloids with a great structural diversity are widely used in the
formulation of important antibacterial drugs including metronidazole
and quinolones. The antibacterial mechanism of action has been eval-
uated among several classes such as indolizidine, isoquinoline, quino-
lone, agelasine and polyamine (Cushnie, Cushnie, & Lamb, 2014). Re-
sults show that the most important mechanisms are related to
intercalation with DNA (Cowan, 1999), prevention of nucleic acid
synthesis in indolizidines (Rao & Venkatachalam, 2000), and inhibition
of cell division in isoquinolines (Beuria, Santra, & Panda, 2005).
Glycosides, another natural antimicrobial compound, occur in 16
dicotyledonous families including a large number of edible species,
mainly in Brassica species (Fahey, Zalcmann, & Talalay, 2001). Che-
micals are stored in the form of inactive glycosides in many plants and
they can be activated through enzyme hydrolysis. The biological effects
of glycosides depend on the concentration and structural types of these
components, which can be toxic, antinutritional or beneficial to health
(Guil-Guerrero et al., 2016). Investigation of products from glucosino-
late hydrolysis indicate their activity against Gram-positive and Gram-
negative bacteria. Among tested species, isothiocyanates have sig-
nificant antimicrobial activities; Pseudomonas aeruginosa being the most
sensitive microorganism, while Listeria monocytogenes being the most
resistant. It was reported that there is a synergy between streptomycin
and allyl isothiocyanate and 2-phenylethyl isothiocyanate against
Gram-negative bacteria (Saavedra et al., 2010).
Derivatives from steroids or triterpenoid glycosides are saponins
with antibacterial and antifungal effects. Their mechanism of action
includes changing the permeability of cell walls, leading to cell lysis
(Godstime, Felix, Augustina, & Christopher, 2014). Since saponins are
structurally diverse compounds, findings obtained from different stu-
dies were varied. According to an investigation conducted by Mandal,
Sinha Babu, & Mandal (2005), saponins (from Acacia auriculiformis)
demonstrate different mechanisms of inhibition against microorgan-
isms. They found an increased specific activity of the enzymes in bac-
teria and a decreased activity in fungi, demonstrating different me-
chanisms of saponins' inhibition.
As reported by Suarez et al. (2005) and Tan, Ayob, & Wan Yaacob
(2013); (Tan et al., 2013), peptides isolated from mango seeds and from
the palm-kernel cake, respectively, have antibacterial activity against
several pathogens. Data obtained confirmed that peptides from mango
seeds lead to bacterial membrane damage and that such activity is lo-
cated in a sequence prone to form a helix-loop-helix structural motif,
without affecting human cells (Suarez et al., 2005).
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Meat Science 145 (2018) 245–255
3.3. Health promotion
Despite the growth of the pharmaceutical industry, the traditional
medicine containing plant extracts, herbal mixtures and natural com-
ponents extracted from different plant species is still of great interest in
primary health care (Granato et al., 2017). Phytonutrients including
polyphenols (flavonoids and stilbenes), carotenoids, plant sterols, and
polyunsaturated fatty acids (PUFAs) play a potentially beneficial role in
the prevention and treatment of diseases. Phytochemicals are thought
to be anti-inflammatory, detoxifying, antioxidant and hormone-balan-
cing compounds that should be eaten every day to help to prevent
diseases and creating optimized health (Mariutti et al., 2011).
There are many non-communicable diseases (e.g. atherosclerosis,
ischemic heart disease, cancer, diabetes mellitus, neurodegenerative
diseases, and aging) which are caused by oxidative stress (Azizova,
2002). The body's non-enzymatic antioxidant defense system includes
some antioxidants, such as vitamin C, vitamin E, vitamin K, and glu-
tathione. Although several synthetic antioxidants are commonly used in
the food industry for protection from oxidation and spoiling, there are
some potential adverse effects due to toxicity and carcinogenicity
(Botterweck, Verhagen, Goldbohm, Kleinjans, & van den Brandt, 2000).
In this respect, natural antioxidants in fruits and vegetables can reduce
the risk of chronic disease (Saljoughian et al., 2018; Leifert &
Abeywardena, 2008). Medicinal plants offer a wide variety of bioactive
substances, antioxidants, flavonoids, and phenolic substances with
multiple health effects (Vinceković et al., 2017; Bahmani et al., 2015).
For example, phenolic compounds, due to their antioxidative activity,
are considered as potential agents for inhibition and treatment of many
oxidative stress-related diseases. The antioxidant activity of poly-
phenols has been attributed to their redox properties, which allow them
to act as reducing agents, hydrogen donors, singlet oxygen quenchers,
metal chelators and reductants of ferryl hemoglobin (Kratchanova,
Denev, Ciz, Lojek, & Mihailov, 2010). Hence, plant extract can be
consumed as a food additive and applied for disease prevention (Liu,
Qiu, Ding, & Yao, 2008; Liu, 2003).
With infectious diseases accounting for approximately 50% of all
deaths in tropical countries and as much as 20% of deaths in the
Americas, they are an important cause of morbidity and mortality
worldwide (WHO 2003). The antibacterial properties of plants have
also been associated with their phenolic compounds (Morris, Khettry, &
Seitz, 1979). Phenolic compounds presented in plants are mostly syn-
thesized from the phenylpropanoid pathway. In vitro antimicrobial
properties of the phenylpropanoid pathway intermediates, (e.g. p-cou-
maric acid, caffeic acid, ferulic acid and sinapic acid), and pathway
derivatives, (e.g. flavonoid aglycones and glycosides), have been re-
ported experimentally (Barber, McConnell, & DeCaux, 2000; Dixon,
2001).
There is some evidence that consumption of flavonoid-rich foods
(e.g. high-soy diet, beverages, and dietary supplements) may be bene-
ficial to cognitive function including improvement of short-term and
long-term memory and mental flexibility. Isoflavones and related fla-
vonoids are likely to mediate their positive influence on the brain,
leading to improved cognitive performance through processes such as
improved cerebral blood flow (via increased nitric oxide release) trig-
gering hippocampal neurogenesis and angiogenesis and scavenging
proinflammatory agents and neurotoxic species (Wiseman, 2013).
4. Application of plant extracts in ready-to-eat meat products
4.1. Antimicrobial and health-related properties
A major concern in ready-to-eat meat products is related to their
contamination by spoilage microorganisms and foodborne pathogens.
Although these products are often combined with antimicrobial agents
(e.g. lactates and diacetates) to prevent the growth of microorganisms,
it has been reported that their application alone is ineffective over time
 Table 1
Application of plant extracts on meat-based products and their antimicrobial effects.
Product type Plant extract type Microorganism type(s) Main results Reference

Beef hot dogs L. monocytogenes Higher extract concentrations, longer rinse times, and longer storage times Higginbotham, Burris, Zivanovic,
N. Nikmaram et al.

Hibiscus flower
S. aureus led to higher L. monocytogenes prevention. Hot dogs rinsing with extracts at Davidson, and Stewart (2014)
120 mg/ml for 60 min and stored for 24 h also resulted in ca. 2 log CFU/g
lowering of both microorganisms
Chicken hot dogs Green tea, Grape seed Pathogens Chemical preservatives were partially replaced by the combination of Perumalla et al. (2013)
extracts and heat treatment
Hot dogs Essential oils (thyme, clove, and pimento) L. monocytogenes Higher antimicrobial inhibitory effect was not observed by using the higher Singh, Singh, Bhunia, and Singh (2003)
concentration of extracts. The effectiveness of the EOs was found to be
lower as the result of increasing the fat level of the hot dog
Ham Commercial EOs Pathogens A significant decrease in the growth rate was observed by the application of Dussault, Vu, & Lacroix, (2014)
oregano (19%) and cinnamon (10%) cassia EOs.
Cooked pork meatballs Grape seed, Green tea Mould and yeast and coliform counts Green tea extracts exhibited significant antimicrobial activity from day 12 Price, Díaz, Bañón, and Garrido (2013)
Jokbal (pig's trotters) Rooibos (tea extract) Clostridium perfringens A combination of 10% rooibos and 4% potassium lactate + sodium Park, Park, and Yoon (2014)
diacetate was significantly lowered the numbers of C. perfringens in the
Jokbal at 10 °C
Ham steak Green and black teas L. monocytogenes Application of green tea extract (4%) resulted in lowering the initial counts (Vodnar, 2012)
from 3.2 to 2.65 log CFU/cm2 during room temperature storage and from
3.2 to 1–1.5 log CFU/cm2 during refrigeration storage.
Beef muscle slices Oregano and pimento essential oils Pseudomonas spp., E. coli O157:H7 Among the extracts, the highest effect was belonged to oregano with a 0.95 Oussalah, Caillet, Salmiéri, Saucier, and
log reduction of Pseudomonas spp. level and a 1.12 log decrement of E. coli Lacroix (2004)
O157:H7
Mortadella sausage Zataria multiflora Boiss essential oil (ZEO), Lactic acid bacteria, aerobic The most sensitive and resistant microorganisms were aerobic mesophiles Moradi, Tajik, Razavi Rohani, and
grape seed extract (GSE) mesophiles, and L. monocytogenes (0.1–1.1 log cycles reduction) and lactic acid bacteria (0.1–0.7 log cycles Oromiehie (2011)
reduction), respectively. The growth of L. monocytogenes was inhibited by
combination of ZEO and GSE.

249
Bologna slices Oregano essential oil E. coli O157:H7 Application of chitosan base edible film incorporated with 1% and 2% of Zivanovic, Chi, and Draughon (2005)
oregano essential oil resulted in 4 logarithmic units reduction in the number
of E. coli O157:H7.
Turkey ham Alpinia galanga (Linn.) Swartz Flower Extract L. monocytogenes and S. aureus. Using GFE resulted in up to 1 log cfu/g S. aureus and L. monocytogenes Cadet, Williams, Simonne, and Sharma
(GFE) population reduction. (2013)
Cooked shrimp Galangal (Alpinia galanga), rosemary L. monocytogenes and S. aureus, aerobic The combination of all extracts resulted in a significant decrease in the Weerakkody, Caffin, Dykes, and Turner
(Rosmarinus officinalis), and lemon iron bark bacteria and lactic acid bacteria numbers of aerobic bacteria (1.6 and 1.59) and lactic acid bacteria (log (2011)
(Eucalyptus staigerana) CFU/g) at 4 °C on day 12. No significant reduction was observed in the
levels of L. monocytogenes or S. aureus.
Meat paté Pomegranate extract's (PE) L. monocytogenes PE inhibited the growth of L. monocytogenes by 4.1 log CFU/g during Hayrapetyan, Hazeleger, and Beumer
46 days at 4 °C reaching to log 9.2 CFU/g on the 18th day. Application of (2012)
higher temperature caused less prevention
Fish Lippia sidoides Cham. (“alecrim pimenta”) L. monocytogenes - The extract was useful to prevent L. monocytogenes in fish peptone broth dos Reis et al. (2011)
and “surubim” homogenate.
- The food matrix was considered as an effective parameter.
Asian sea bass fish (Lates Thyme (Thymus vulgaris) and oregano Spoilage microflora A significant reduction in the numbers of spoilage microflora was observed Harpaz, Glatman, Drabkin, and Gelman
calcarifer) (Origanum vulgare) using thyme and oregano extracts. The initial total bacteriological counts (2003)
decreased to 1.7 × 103 CFU/cm2
Cooked chicken meat Rhodomyrtus tomentosa ethanolic leaf L. monocytogenes - The inhibitory activity of extract increased at higher temperatures or by Odedina, Vongkamjan, and
using microwave treatment. Voravuthikunchai (2016)
- Application of both rinse and injection methods led to a reduction in L.
monocytogenes populations using leaf extract at low (104 CFU/g) and high
(106 CFU/g) inoculum levels
Cooked cured chicken Oriental mustard L. monocytogenes Application of the extract had the positive effect on controlling L. Olaimat and Holley (2016)
breasts Lactic acid bacteria monocytogenes and lactic acid bacteria viability and delaying the growth of
potential spoilage bacteria.
Chicken breasts Oriental mustard Salmonella and C. jejuni Utilization of k-carrageenan/chitosan coated with 1% (v/v) acetic acid and Olaimat, Fang, and Holley (2014);
50 ml/g AITC or 250–300 mg/g Oriental mustard extract reduced the Olaimat & Holley, 2015)
viability of the microorganisms
(continued on next page)
Meat Science 145 (2018) 245–255
N. Nikmaram et al. Meat Science 145 (2018) 245–255

for inhibition of Listeria growth (Horita et al., 2018; Perumalla et al.,

(Sivarooban, Hettiarachchy, & Johnson,

(Lara-Lledó, Olaimat, & Holley, 2012)

2013). Hence, to inhibit pathogens (e.g. Listeria), it is common to apply

(Gadang, Hettiarachchy, Johnson, &

treatments that aim to decrease water activity, alter the pH and/or use

(Theivendran, Hettiarachchy, &

some post-processing treatment such as steam pasteurization. Natural
antimicrobial agents can be applied before or after heating treatment.
Table 1 shows several plant extracts that benefit different RTE meat-
based products due to their antimicrobial effects.
Johnson, 2006)
Higginbotham, Burris, Zivanovic, Davidson, & Stewart (2014)

Owens, 2008)
evaluated the antimicrobial effect of lyophilized Hibiscus flower extracts
Reference

as a rinse on all-beef hot dogs against Listeria monocytogenes and me-

2007)

thicillin-resistant Staphylococcus aureus (MRSA). After deep inoculation

of beef hot dogs in overnight cultures of 1:1 mixtures of L. mono-
After 28 d at 4 °C, a significant reduction in L. monocytogenes from 5.5 log/g

cytogenes strain Scott A and 101 or MRSA strains ATCC 33591 and
Application of polymeric film incorporated with Oriental mustard extract

A significant decrease in L. monocytogenes population (7.1 CFU/g) by > 2

with 5% (w/w) sinigrin resulted in lowering L. monocytogenes cells to an

(10,000 IU) combined with either GSE (1%) or GTE (1%), was observed.

to 2.3 log/g were observed using nisin (6000 IU/g) combined with GSE

ATCC 33593, they were placed at 4 °C overnight in order to achieve

log cycle after 28 d at 4 °C and 10 °C, in the samples containing nisin
The combination of nisin and grape seed significantly reduced the L.

bacterial attachment. Hot dogs were rinsed with extracts (120, 240 mg/
ml) or water (control) for 5, 15, 30, or 60 min and then plated instantly
monocytogenes population to undetectable levels after 21 days

(0 h; no storage) or stored overnight (4 °C) and plated at 24 h. The most

undetectable level (< 1.6 log10 CFU/g) after 52 d at 4 °C.

effective prevention and/or reduction of L. monocytogenes and MRSA on

hot dogs was achieved by higher extract concentrations, longer rinse
times, and longer storage times. There was a significant reduction of L.
monocytogenes (approximately 1.5 log CFU/g) and MRSA (to un-
detectable levels) through rinsing of hot dogs with extracts at 240 mg/
ml for 60 min and stored for 24 h. Rinsing of hot dogs with extracts at
120 mg/ml for 60 min and stored for 24 h also led to ca. 2 log CFU/g
(0.5%) and malic acid (1.0%).

reduction of both microorganisms.

The effects of natural extracts of green tea (0.35%) and grape seed
(0.22%) along with two antimicrobial preservatives including po-
tassium lactate (1.5%) and sodium diacetate (0.15%) on inhibiting and/
or controlling pathogens on hot dogs were investigated (Perumalla
Main results

et al., 2013). The maximum growth inhibitions (c. 2.0 CFU/g) were
found by implementing both chemical preservatives and plant extracts,
however, the application of the antimicrobial preservatives alone was
not effective. Moreover, post-packaging heat treatment (65 °C for 104 s)
L. monocytogenes, E. coli O157:H7, and

in combination with using both plant extracts along with chemical

preservatives resulted in the more inhibitory effect on the growth of L.
monocytogenes survivors in chicken hotdog samples. Therefore, natural
plant extracts combined with heat treatment can partially replace
chemical preservatives.
Salmonella typhimurium
Microorganism type(s)

Essential oils (EOs) are volatile liquids that are extracted from
L. monocytogenes

L. monocytogenes

L. monocytogenes

plants. Various EOs have demonstrated antimicrobial, antiviral, anti-

mycotic, antitoxigenic, antiparasitic and insecticidal properties
(Hyldgaard, Mygind & Meyer, 2012). EOs have the greatest effect on
the Gram-positive bacteria (i.e. B. cereus, S. aureus and L. mono-
cytogenes) followed by Gram-negative bacteria (i.e. E. coli, S. Typhi-
murium and P. aeruginosas) (Burt, 2004). In this respect, the efficiency
of plant essential oils (thyme, clove, and pimento) against L. mono-
cytogenes were evaluated on hotdogs containing different fat levels
(zero-, low-, and full-fat) (Singh, Singh, Bhunia, & Singh, 2003). Bac-
Grape seed (GSE), green tea (GTE)

terial populations were remarkably decreased using thyme essential oil

at 1 ml/l level in zero- and low-fat hotdogs, but not in full-fat hotdogs.
Clove essential oil at 1 ml/l in all hotdogs also indicated antimicrobial
activity and had a greater effect than thyme at 5 ml/l. As the higher
Grape seed, green tea

concentration of essential oil (10 ml/l) did not lead to more bacterial
Plant extract type

Oriental mustard

population lowering, they demonstrated that essential oils efficacy was

decreased in a food system as a result of interaction with food com-
Grape seed

pounds. They also observed the lower effectiveness of the EOs with
increasing fat level of the hot dog. Dussault, Vu, & Lacroix (2014) se-
lected 67 commercial EOs and oleoresins (ORs) to investigate their
antimicrobial activity in vitro against six food pathogens. They observed
a decrement of the growth rate by 19 and 10% when oregano and
Table 1 (continued)

Turkey frankfurters

Turkey frankfurters

Turkey frankfurters

cinnamon cassia EOs were added in ham at a concentration of 500 ppm,

respectively.
Bologna slices
Product type

Although the use of sodium nitrite in meat-based products has some

benefits (e.g. increased shelf-life and improvement of flavor and lipid
stability), it is classified as a chemical preservative and its application in
either natural or organic processed meat and/or poultry products is

250
N. Nikmaram et al.
restricted.
Price, Díaz, Bañón, & Garrido (2013) compared grape seed and
green tea extracts with sodium ascorbate and their effects on bacterial
spoilage in cooked pork meatballs during refrigerated storage (4 °C in
aerobic packaging for 0, 4, 8, 12 and 16 days under retail display
conditions). The total viable count indicated irregular behavior during
the storage time and among all the samples, green tea extracts exhibited
significant antimicrobial activity (p < .05) from day 12. Another study
evaluated the antimicrobial effects of rooibos (tea extract) potassium
lactate (PL) and sodium diacetate (SDA) mixture alone or in combina-
tions on the growth of Clostridium perfringens vegetative cells and spores
in RTE Jokbal (pig's trotters) (Park, Park, & Yoon, 2014). Rooibos
contains several components such as aspalathin, isoorientin, orientin,
and rutin that could contribute to antimicrobial activity (Almajano
et al., 2007). Authors reported that a combination of 10% rooibos and
4% PL + SDA significantly reduced the populations of C. perfringens in
the Jokbal stored at 10 °C. During the storage period, there was a re-
markable prevention on the germination and the growth of C. perfrin-
gens spores in the Jokbal treated with a combination of 10% rooibos
and 4% PL + SDA. Therefore, rooibos tea was proved to have a great
potential to inhibit the growth of C. perfringens as well as the germi-
nation and the outgrowth of C. perfringens spores.
There have been several studies demonstrating the antimicrobial
properties of edible films incorporating natural extracts. For example,
Vodnar (2012) incorporated bioactive compounds from green and black
teas into chitosan as an antimicrobial film on ham steak to control L.
monocytogenes ATCC 19115 growth. Compared to chitosan-coated films
without the addition of tea extracts, those containing the natural ex-
tracts exhibited a significant effect on the growth prevention of L.
monocytogenes. The most effective antimicrobial films were reported to
be those containing 4% green tea extract, lowering the initial counts
from 3.2 to 2.65 log CFU/cm2 during room temperature storage and
from 3.2 to 1–1.5 log CFU/cm2 during refrigerated storage. Another
antimicrobial chitosan film was developed by Moradi, Tajik, Razavi
Rohani, & Oromiehie (2011) containing Zataria multiflora Boiss essen-
tial oil (ZEO) (5 and 10 g/kg) and grape seed extract (GSE) (10 g/kg).
They tested the effectiveness of these films on different microorganisms
including lactic acid bacteria, aerobic mesophiles and L. monocytogenes
of mortadella sausage at 4 °C for 21 days. The most sensitive and re-
sistant microorganisms were aerobic mesophiles (0.1–1.1 log cycles
reduction) and lactic acid bacteria (0.1–0.7 log cycles reduction), re-
spectively. Those films containing ZEO-GSE prevented the growth of L.
monocytogenes remarkably during storage of the sausages for 6 days.
Thymol, a phenolic compound with a hydroxyl group, is the main
compound in ZEO that exhibit antimicrobial activity (Saei-Dehkordi,
Tajik, Moradi, & Khalighi-Sigaroodi, 2010). To control the growth of
pathogenic bacteria and extend the shelf-life of beef slices during sto-
rage at 4 °C, milk protein-based edible films incorporated with 1.0% (w/
v) oregano, 1.0% (w/v) pimento, or 1.0% oregano-pimento (1:1) es-
sential oils mix were investigated (Oussalah, Caillet, Salmiéri, Saucier,
& Lacroix, 2004). Based on the obtained data, the edible film containing
oregano had the highest antimicrobial activity against both bacteria;
however, the least effect was observed in the film containing pimento
oils. Compared to the control sample, there was a 0.95 log reduction of
Pseudomonas spp. by application of films containing oregano extracts. A
significant decrease (1.12 log) of E. coli O157:H7 level was observed in
samples coated with oregano-based films. Zivanovic, Chi, & Draughon
(2005) also reported a 1–3 log decrease in pathogen number through
using chitosan film alone. Chitosan-based edible film incorporated with
1% and 2% of oregano essential oil resulted in a reduction of 4 log units
of E. coli O157:H7 on bologna slices at 10 °C during 5-day storage.
Cadet, Williams, Simonne, & Sharma (2013) investigated the anti-
microbial efficiency of Alpinia galanga (Linn.) Swartz Flower Extract
(GFE) in RTE turkey ham product inoculated with L. monocytogenes and
S. aureus. In comparison with the inoculated control sample, GFE
showed a significant antimicrobial activity in which up to 1.00 log cfu/
251
Meat Science 145 (2018) 245–255
g in S. aureus and L. monocytogenes counts were reduced. GFE exhibited
no adverse effect on color and pH of the samples. In an investigation
conducted by Weerakkody, Caffin, Dykes, & Turner (2011), the anti-
microbial activities of two spice and herb extract combinations from
galangal (A. galanga), rosemary (Rosmarinus officinalis), and lemon ir-
onbark (Eucalyptus staigerana) were examined. RTE shrimp were in-
oculated by L. monocytogenes and S. aureus in the presence of natural
spoilage microflora and stored for 16 days at either 4 or 8 °C. Using the
combination of galangal, rosemary and lemon iron bark significantly
decreased the levels of aerobic bacteria and lactic acid bacteria at 4 °C
on day 12 by 1.6 and 1.59 log CFU/g, respectively. During the storage
period, no significant effect was observed on levels of L. monocytogenes
or S. aureus as well as the color parameters or pH values of the shrimp.
Hayrapetyan, Hazeleger, & Beumer (2012) evaluated the feasibility
of using pomegranate extract's (PE) as a preservative in RTE meat-based
products. The presence of 7.5% v/v of the liquid PE (or 24.7 mg dry PE/
ml) as the Minimal Bactericidal Concentration (MBC) of the tested PE
resulted in detection of no viable cells of L. monocytogenes. The effect of
PE in a concentration equal to the measured MBC was tested against L.
monocytogenes in meat pâté at different temperatures. In comparison
with the control sample, PE prevented the growth of meat pâté by 4.1
log CFU/g during 46 days at 4 °C. The reduction reached log 9.2 CFU/g
on the 18th day of storage and higher temperature decreased inhibition.
These results were in agreement with Glass, Mcdonnell, Rassel, & Zierke
(2007) who demonstrated the temperature dependent inhibition of L.
monocytogenes benzoate, propionate, and sorbate in sliced ham and
turkey products. They found a higher inhibitory effect at 4 °C rather
than 7 and 10 °C. Li, Chikindas, Ludescher, & Montville (2002) sug-
gested that the altered sensitivity to the components could be due to
changes in membrane fluidity of L. monocytogenes at different tem-
peratures.
Different kinds of fish can also be commercialized as an RTE mini-
mally processed product. High microbiological risk of these products
threatens human health since their microbiological safety relies mostly
on low temperature and modified atmosphere packaging, which are not
restrictive to anaerobic and psychrotolerant bacteria such as L. mono-
cytogenes (De Martinis, Alves, & Franco, 2002). In this regard, dos Reis
et al. (2011) evaluated the effect of hydroalcoholic extract of the plant
Lippia sidoides Cham, in combination with cultures of LAB, on inhibiting
L. monocytogenes in fish model systems at 5 °C during 35 days. They
considered food matrix as an effective parameter since the plant extract
was useful in preventing L. monocytogenes in fish peptone broth and
“surubim” homogenate, while it failed in “surubim” broth. To extend
the shelf-life of freshwater-reared Asian sea bass fish (Lates calcarifer),
the effect of herbs-thyme (Thymus vulgaris) and oregano (Origanum
vulgare) essential oils at a concentration of 0.05% (v/v) was investigated
(Harpaz, Glatman, Drabkin, & Gelman, 2003). Application of these
herbal essential oils resulted in a significant reduction in the numbers of
spoilage microflora. Compared to the control sample (107 CFU/cm2),
the initial total bacteriological counts decreased to 1.7 × 103 CFU/cm2
on the fish surface using essential oils after 33 days of storage at 0 to
2 °C.
Recently, Odedina, Vongkamjan, & Voravuthikunchai (2016) stu-
died the effect of Rhodomyrtus tomentosa ethanolic leaf extract for the
bio-control of L. monocytogenes post-cooking contamination in cooked
chicken meat. The plant extract had better antilisterial activity under
microwave condition (inner temperature of 80 °C) and enhanced by
increasing the storage temperature from 4 to 37 °C. L. monocytogenes
numbers were decreased using the extract at low (104 CFU/g) and high
(106 CFU/g) inoculum levels in cooked samples by both rinse and in-
jection methods. Rinsing for 5 min in 8% w/v R. tomentosa extract
lowered the bacterial number by ≥2-log before storage and ≥ 3-log
after storage at 4 °C for 5 days. Injection with 0.4% w/w R. tomentosa
extract led to an approximate 2-log reduction in the cell numbers both
before and after storage at 4 °C for 5 days. In another study, the positive
effect of allyl isothiocyanate (AITC) on controlling L. monocytogenes and
N. Nikmaram et al.
lactic acid bacteria viability and delaying the growth of potential
spoilage bacteria on cooked cured chicken breasts was demonstrated
(Olaimat & Holley, 2016). AITC can be obtained through hydrolysis of
the glucosinolate sinigrin, present in Oriental mustard, by endogenous
plant myrosinase upon physical injury in the presence of moisture
(Barba et al., 2016). The lethality of AITC against major foodborne
pathogens including E. coli O157:H7, L. monocytogenes, Salmonella spp.
and Campylobacter jejuni was reported in several studies (Luciano &
Holley, 2009; Olaimat & Holley, 2013; Olaimat, Fang, & Holley, 2014).
They evaluated the incorporation of 25–50 ml/g AITC directly or
100–250 mg/g Oriental mustard extract in 0.5% (w/v) κ-carrageenan/
2% (w/v) chitosan-based coatings using 1.5% malic or acetic acid.
Generally, the higher inhibitory effect was observed by application of κ-
carrageenan/chitosan coatings prepared using 1.5% (w/v) malic acid
compared to those prepared using 1.5% (v/v) acetic acid. Olaimat,
Fang, & Holley (2014) and Olaimat & Holley (2015) confirmed that the
preparation of κ-carrageenan/chitosan coatings with 1% (v/v) acetic
acid and 50 ml/g AITC or 250–300 mg/g Oriental mustard extract led to
the viability reduction of Salmonella and C. jejuni on fresh, vacuum
packed chicken breasts stored at 4 °C for 21 d. Similarly, a polymeric
film containing Oriental mustard extract with 5% (w/w) sinigrin re-
sulted in lowering L. monocytogenes cells on bologna slices to an un-
detectable level (< 1.6 log10 CFU/g) after 52 d at 4 °C (Lara-Lledó,
Olaimat, & Holley, 2012).
Sivarooban, Hettiarachchy, & Johnson (2007) examined the anti-
microbial ability of nisin (6400 IU/ ml), grape seed extract (GSE; 1%),
and the combination of nisin and GSE both in tryptic soy broth with
0.6% yeast extract (TSBYE) against L. monocytogenes on the surface of
full-fat turkey frankfurters. The highest inhibitory effect was reported
by combining nisin and GSE in both TSBYE and turkey frankfurters with
reductions of L. monocytogenes numbers to undetectable levels after
15 h and 21 days, respectively. Nisin alone showed no significant effect
after 72 h in TSBYE. Ineffectiveness of nisin compared to other bac-
teriocins (e.g. pediocin) against L. monocytogenes was demonstrated in
another study (Montville & Chen, 1998). Similar research was con-
ducted by Theivendran, Hettiarachchy, & Johnson (2006) who assessed
the effectiveness of grape seed extract (GSE), green tea extract (GTE),
nisin and their combinations (nisin with either GSE or GTE) against L.
monocytogenes on turkey frankfurters. The inoculated frankfurters were
dipped into soy protein film-forming solutions with and without the
addition of antimicrobial agents (GSE 1% or GTE 1% or nisin 10,000 IU
or combinations). The results showed a remarkable decrease in L.
monocytogenes population (7.1 CFU/g) by > 2 log cycle after 28 d at
4 °C and 10 °C, in the samples containing nisin (10,000 IU) combined
with either GSE (1%) or GTE (1%). In another study, the effect of
protein isolate (WPI) coatings incorporated with grape seed extract
(GSE), nisin (N), malic acid (MA), and ethylenediaminetetraacetic acid
(EDTA) on the inactivation of L. monocytogenes, E. coli O157:H7, and
Salmonella Typhimurium in Turkey frankfurter was investigated
(Gadang, Hettiarachchy, Johnson, & Owens, 2008). The inoculated
frankfurters were dipped into WPI film forming solutions both with and
without the addition of antimicrobial agents (GSE, MA, or N and EDTA,
or combinations). After 28 d at 4 °C, a significant reduction in L.
monocytogenes from 5.5 log/g to 2.3 log/g were observed by using nisin
(6000 IU/g) combined with GSE (0.5%) and MA (1.0%). S. Typhimurium
population was lowered by 1 log after coating with WPI containing a
combination of N, MA, GSE, and EDTA. In terms of E. coli O157:H7,
application of WPI coating incorporated with N, MA, and EDTA resulted
in reducing the population by 4.6 log cycles after 28 days.
4.2. Nutritional and sensory properties
In addition to antimicrobial properties, plant extracts can enhance
the shelf-life and nutritional properties of RTE meat-based foods. These
natural plant extracts can be added to the fresh/processed meat and
meat products to prevent lipid oxidation, delay the development of off-
252
Meat Science 145 (2018) 245–255
flavors, and improve color stability (Fernandes, Trindade, Lorenzo,
Munekata, & de Melo, 2016; Lorenzo, Sineiro, Amado, & Franco, 2014).
Various natural antioxidants have been shown to exert a positive or
negative effect on the color and sensory properties of the meat pro-
ducts. The effect and efficiency of plant extracts also depend on the
extraction method, processing treatment the samples are subjected to,
and post-packaging treatment. Park et al. (2014) studied the anti-
oxidant effect of water and methanolic garlic extracts in pork patties at
refrigerated storage conditions and observed that methanolic extracts
had higher total phenolic content and antioxidant activity. Addition of
garlic extracts (both water and methanolic extracts) in pork patties had
decreased the lipid oxidation using TBARS analysis, redness, and the pH
values of patties.
Mariutti, Nogueira, & Bragagnolo (2011) reported that the addition
of garlic extracts, in the presence of salt (0.5 g of salt/100 g), to the
chicken breast meat, did not affect on the antioxidant levels and even
accelerated the lipid oxidation of the product during storage at −18 °C
for 90 days. However, using sage extract was effective in controlling
lipid and cholesterol oxidation, minimizing the pro-oxidant effects of
salt, cooking, and storage. Chan et al. (2014) reported that in chicken
meatballs when treated with cinnamon extracts at 200 ppm under
chilled conditions, peroxide values were reduced throughout the sto-
rage period without any effect on sensory properties. Moreover,
Moarefian, Barzegar, & Sattari (2013) also observed that when Cinna-
momum zeylanicum essential oil was added to cooked sausage, the
concentrations as low as 20 and 40 ppm resulted in lower peroxide
values without affecting sensory characteristics of the samples.
Trindade et al. (2009) reported that cooked pork meat patties
(under refrigerated conditions) treated with Rosemary (Rosmarinus of-
ficinalis L.) and lemon balm (Melissa officinalis L.) in combination with
modified atmospheric conditions (70% N2 + 30% CO2) had higher
redness (a*) than non-treated samples. However, no significant differ-
ence in the sensory attributes between treated and non-treated samples
was observed by panel members. Gök, Obuz, Şahin, & Sertwser, (2011)
investigated the effect of rosemary powder, rosemary extract and α-
tocopherol on oxidative quality of Turkish sucuk during ripening and
storage. The combination treatment of rosemary extract and α-toco-
pherol (1:1) resulted in highest antioxidant activity and was effective in
preserving color compared to the control. Camo, Lorés, Djenane,
Beltrán, & Roncalés (2011) evaluated the effect of oregano extract on
antioxidant activity of fresh beef steaks under an active packaging
system. Application of 1% oregano extract increased the shelf-life from
14 to 23 days while using 4% oregano extract resulted in producing
unacceptable oregano odor during the 1st day. The optimum packaging
conditions were obtained by extracts at 1% and 2% concentrations.
Price, Díaz, Bañón, & Garrido (2013) reported that the addition of
green tea and grape seed extract into pork meatballs at refrigerated
storage conditions resulted in brown shades. Although the addition of
plant extracts was efficient in reducing lipid oxidation, they sig-
nificantly affected sensory attributes. In another study conducted by
Jia, Kong, Liu, Diao, & Xia (2012), condensed black currant (Ribes ni-
grum L.) extract (BCE) was added at 5, 10, or 20 g/kg to pork patties
under chilled conditions to evaluate the antioxidant potential. The BCE
treatment decreased the carbonyl formation, sulfhydryl loss, and
TBARS value by 91.7% with 20 g/kg dosage. The treated patties had
significantly higher redness than untreated samples.
The application of supercritical fluid extraction (SFE) was reported
to increase the protective action of plant extracts against lipid oxidation
in cooked chicken meat (Gallo, Ferracane, & Naviglio, 2012). They
observed that SFE extracts of Echinacea angustifolia were able to prevent
lipid oxidation with higher efficiency than extracts obtained by con-
ventional extraction method. Another effective application of plant
extracts to increase the nutritional value of RTE meat-based products is
in the production of antioxidant food packaging. A study was conducted
by Contini et al. (2012) who evaluated the effect of citrus extract,
coated at the density of 0.45 mg/cm2, on the lipid oxidation of cooked
N. Nikmaram et al.
turkey meat. The results were compared with standard α-tocopherol
(coating density of 0.28 mg/cm2) coated packaging films. The effec-
tiveness of the citrus extract coating compared with the α-tocopherol
coating was attributed to its higher surface roughness (demonstrated by
optical profilometry) and antioxidant release (solubility) in water.
Encapsulation can be defined as a technological process to in-
corporate a compound, known as active compound or core (solid, liquid
or gas) within another substance(s) known as wall material, coating
wall or membrane (Vinceković et al., 2017). Thus, encapsulation is an
excellent choice to stabilize biological compounds, and in particular
antioxidants, and mask their strong flavors and odors. In particular,
spray drying is one of the most economical and common encapsulation
technologies. In this regard, Baldin et al. (2016) assessed the addition of
microencapsulated jabuticaba extract (MJE) to the fresh sausage as a
natural antioxidant and they noticed that MJE at 2% and 4% con-
tributed to a reduction in lipid oxidation of fresh pork sausages during
15 days of storage. However, the inclusion of 4% MJE negatively af-
fected sensory color, texture and overall acceptability of the sausages,
which did not happen with 2% MJE addition.
5. Conclusions and future direction
Several studies reported the application of natural antioxidants ex-
tracted from fruits, vegetables, by-products, and other plant materials
in RTE meat products. The extracts from these sources, not only inhibit
lipid oxidation but also affect (positively/negatively) the quality attri-
butes of the meat products. Some extracts may add strong flavors to the
RTE meat product making it unacceptable by consumers and some of
the extracts may contain anti-nutritional or even toxicological factors
causing health-related issues. In other words, the overall acceptability
of the product should be taken into consideration when evaluating the
antioxidant potential rather than just evaluating lipid oxidation/anti-
microbial activity. Moreover, before commercializing a food product
supplemented with natural bioactive molecules, a detailed study of the
effect of processing parameters (e.g. cooking, pressure, product in-
gredients, etc.) on the antioxidant/antibacterial activity of the com-
pounds should be carried out. Application of micro- and nano-en-
capsulation of active compounds can be a suitable technique to
minimize the required doses and improve the effectiveness of natural
extracts. Further research needs to be conducted to evaluate the sy-
nergistic effect of different natural extracts, extracted from various
plant sources, on improving the shelf-life, nutritional and health-related
properties of RTE meat products.
Acknowledgment
Sravanthi Budaraju would like to acknowledge the University of
Minnesota for her Ph.D. Scholarship award. Jose M. Lorenzo is the
member of the MARCARNE network funded by CYTED (ref.
116RT0503).
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