Food Research International 64 (2014) 171181

Contents lists available at ScienceDirect

Food Research International

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

Review

Natural antioxidants against lipidprotein oxidative deterioration in

meat and meat products: A review
Andrew B. Falowo, Peter O. Fayemi, Voster Muchenje
Department of Livestock and Pasture Science, Faculty of Science and Agriculture, University of Fort Hare, P. Bag X1314, Alice 5700, Eastern Cape Province, South Africa

a r t i c l e

i n f o

Article history:
Received 29 April 2014
Accepted 15 June 2014
Available online 21 June 2014
Keywords:
Free radical
Meat quality
Natural antioxidants
Lipidprotein oxidation
Oxidative stress

a b s t r a c t
Oxidation is a well-known non-microbial cause of quality loss in meat. Oxidative stress occurs due to uneven
generation of free radicals reactive oxygen species (ROS) and reactive nitrogen species (RNS) which triggers
oxidative and/or nitrosative stress and damage of macromolecules including the lipid and protein fractions.
Failure of synthetic antioxidants to combat multiple health risks associated with this stress and maintenance of
functional integrity of oxidised meat hitherto remains a challenge to the meat industry. A search for a viable
alternative amidst the unexploited novel sources of natural antioxidants stands as a sustainable option for
preserving the meat quality. In this paper, the potential use of bioactive compounds in medicinal plants is
reviewed as phytoremedy against lipidprotein oxidation. Synergistic antimicrobial potentials of these natural
antioxidants are also revealed against oxidative deterioration in meat and meat products and, for enhancing
their functional properties.
2014 Elsevier Ltd. All rights reserved.

Contents
1.
2.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Oxidative stress and implications on pre-slaughter welfare of animals . . . . . . . . . .
2.1.
Effects of oxidative stress on meat quality . . . . . . . . . . . . . . . . . . .
3.
Oxidation in meat and meat products . . . . . . . . . . . . . . . . . . . . . . . .
3.1.
Lipid oxidation in meat . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.2.
Protein oxidation in meat . . . . . . . . . . . . . . . . . . . . . . . . . .
3.3.
Natural antioxidant in meat and meat products . . . . . . . . . . . . . . . .
3.4.
Prevention of oxidation in meat using natural antioxidants . . . . . . . . . . .
3.5.
Anti-microbial activities of natural antioxidants on meat preservation and security
3.6.
Antioxidantoxidation reaction in meat sample . . . . . . . . . . . . . . . .
3.7.
Edible medicinal plants as natural antioxidant in meat and future perspectives . .
4.
Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1. Introduction
Oxidation is one of the major causes of quality deterioration in meat.
Meat becomes susceptible to oxidative deterioration due to high
concentrations of unsaturated lipids, heme pigments, metal catalysts and
a range of oxidizing agents in the muscle tissue. Oxidative deterioration
in any type of meat manifests in form of discoloration, development of
off avour, formation of toxic compounds, poor shelf life, nutrient and
Corresponding author. Tel.: +27 406022059; fax: +27 86 628 2967.
E-mail address: vmuchenje@ufh.ac.za (V. Muchenje).

http://dx.doi.org/10.1016/j.foodres.2014.06.022
0963-9969/ 2014 Elsevier Ltd. All rights reserved.

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171
172
172
172
173
174
176
176
176
177
178
178
178
178

drip losses, respectively (Contini et al., 2014; Palmieri & Sblendorio,

2007). Under normal physiologic conditions, the molecular oxygen
undergoes a series of reactions that leads to the generation of free radicals.
A small portion (about 25%) of the oxygen consumed during the
metabolic reaction is converted to free radicals in the form of reactive
oxygen species (ROS). These free radicals, particularly, the reactive
oxygen species (ROS) and reactive nitrogen species (RNS), play key
regulatory roles in several homeostatic processes by interacting with
proteins, fatty acids and nucleic acids. They act as intermediate agents
in essential oxidationreduction reactions (Moylan et al., 2014;
Wiseman and Halliwell, 1996).

172

A.B. Falowo et al. / Food Research International 64 (2014) 171181

Fundamentally, when the production of ROS [(superoxide anions

(O
2 ), peroxyl (RO2), alkoxyl (RO ), hydroxyl radicals, singlet
oxygen)] and RNS [(nitric oxide radical (NO), peroxynitrite (ONOO)
and nitrogen dioxide radical NO
2 )] does not exceed the capacity of
endogenous antioxidant barriers in the body, it performs benecial
functions which include: the control of gene expression, regulation of
cell signalling pathways, modulation of skeletal muscle and defence
against invading pathogens. In contrast, when in excess and the activity
of antioxidant defence is low, it potentially causes damage to cellular
components, induces harmful autoimmune responses and causes
oxidative and/or nitrosative stress (Barbieri & Sestili, 2012; Power &
Jackson, 2008). In general, oxidative stress which is caused by an
imbalance between the production of ROS and antioxidant defence
mechanisms in multicellular organism (da Silva, Marques, & Chaveiro,
2010; Sung, Hsu, Chen, Lin, & Wu, 2013) often leads to the modication
of redox cell signalling and activation of pathways, and mechanisms
involved in cardiovascular or chronic health problems (Alfadda &
Sallam, 2012; Gutierrez & Elkind, 2012).
Understanding the activity of free radicals in meat is then important,
since high levels of the ROS in meat could reduce its sensory quality
(Kolakowska & Bratosz, 2010) and cause loss of protein functionality
(Hassan, 2012; Lund, Heinonen, Baron, & Estevez, 2011) and depletion
of essential amino acids like phenylalanine and trypotophan (Ganhao,
Morcuende, & Estevez, 2010). Also, the degradation of unsaponiable
and polyunsaturated fatty acid fractions of meat lipids and the conversion of oxymyoglobin [oxyMb (Fe2 +)] to metmyoglobin [MetMb
(Fe3+)] pigment resulting in the generation of free radicals might lead
to deterioration of meat protein (Suman & Joseph, 2013). Although
antioxidants have the capacity to avert tissue damage by preventing
the formation of radicals, by scavenging them or by promoting their
decomposition, the use of synthetic antioxidants is also found to impose
health risks to man. Consequently, there is a need to explore a suitable
alternative from natural sources, such as plant-derived antioxidants, to
combat the challenges of oxidative instability of lipids and protein in
meat. Aside from this, while the interest in oxidative stress and antioxidant activities continues to grow rapidly, many questions still remain
unanswered as to how the chain of events prior to the conversion of
muscle to meat can reduce oxidative stress in meat. In this review,
attempts were made to address these issues and appraise the potential
use of natural bioactive compounds from medicinal plants to ameliorate
oxidative stress in meat, to prevent lipidprotein oxidation and improve
oxidative stability in meat and meat products.
2. Oxidative stress and implications on pre-slaughter welfare of
animals
The term oxidative stress is used to describe the condition of oxidative
damage as a result of an unfavourable critical balance between free
radical generation and antioxidant defences (Mc Cord, 2000; Rock,
Jacob, & Bowen, 2009). Oxidative stress may occur due to succession of
stimuli that disrupt the homeostatic condition of an animal before
slaughter (Cataldi, 2010). These external stimuli result from stress
imposed on animals during transportation. The effects of rough handling
during traditional slaughter, loading or unloading, poor road conditions,
over-speeding and vibration of the vehicle, distance covered from farm
to the abattoir, overcrowding in the vehicle, deprivation of food and
water, mixing of animals with unfamiliar ones, aggressive behaviour
and stunning are common sources of oxidative stressors (Fayemi &
Muchenje, 2012; Minka & Ayo, 2009; Warriss, 2000, chap. 4). Other
sources include environmental stressors, such as poor or high air velocity,
harsh ambient temperature, relative humidity, lightning, and sound
(Chulayo, Tada, & Muchenje, 2012; Minka & Ayo, 2009).
The cumulative effects of all these stressors on the animals from
farm to slaughter point at the abattoir often result in pains, compromise
their welfare, distort their normal behaviour and cause undesirable
changes in meat quality (Fayemi & Muchenje, 2013). Animals

experiencing these stressors may have fractures in the bones and

bruises in the muscle (Broom, 2000). The stress may also cause an
abnormal rise in heart rate, blood pressure and body temperature.
They can also instigate rapid release of enzymes, cortisols and catecholamines which may lead to the depletion of glycogen, high meat ultimate
pH (pHu) and dark cuts (Chulayo & Muchenje, 2013; Muchenje, Dzama,
Chimonyo, Strydom, & Raats, 2009). Overproduction of ROS (oxidants) in
muscle tissue and the release of stress hormones into the blood stream
also occur in the process (Fergusona & Warner, 2008; Piccione et al.,
2013). The occurrence of lipid oxidation in muscle food, due to oxidative
damage in muscle tissue and the eventual negative effect on meat quality,
has thus been established (Costantini & Bonadonna, 2010; Mapiye et al.,
2012; Sazili et al., 2013) and is summarised in Fig. 1.
2.1. Effects of oxidative stress on meat quality
Oxidative stress in tissues injured by shock, hypertoxia, toxin stress
or several disease conditions, including sepsis, mastitis, enteritis,
pneumonia, respiratory and joint diseases (Lykkesfeldt & Svendsen,
2007) results in functional and/or structural damage to muscle
organelles, cells and tissues. It has been found that myobril protein is
affected by ROS during meat maturation and storage (Martinaud,
Mercier, Marinova, & Tassy, 1997) and that high production of free
radicals and ROS results in degenerative damage of cellular structure
and affect meat quality (Piccione et al., 2013). It has also been demonstrated that oxidative stress affects meat tenderness. Evidence for this is
shown by the ability of ROS to inuence the turnover of the intramuscular
collagen, in terms of the balance between its degradation by the enzyme
matrix metalloproteinase-2 (EMP-2) and synthesis by intramuscular
broblasts derived from bovine muscles (Archile-Contreras & Purslow,
2011). The ndings showed that ROS increased EMP-2 activity and
reduced collagen synthesis in the muscle. This reduction in the collagen
synthesis results in a decrease in collagen solubility and hence increases
meat toughness. The same authors also reported the problem of inconsistency in meat tenderness in the meat industry, which may perhaps have
resulted from an increase in ROS production when farm animals were
exposed to different types and degrees of stresses. However, since no
evidence is available on how the use of medicinal plants could play a
vital role in this regard, it would be necessary to test the efcacy of the
bioactive compounds in their roots, leaves, owers or stem backs on the
moderation of ROS generation, meat tenderness and other quality
parameters
3. Oxidation in meat and meat products
Since the discovery of oxygen in the early 18th century and its
inevitable roles in plants and animals, the necessity to control its levels
and impacts on food and food products, especially during processing,
packaging and distribution, has been a major challenge in the food
industry. Basically, oxidation involves the loss of at least one electron
when chemicals in the food are exposed to oxygen in the air. Oxidation
in lipid and protein fractions of meat has been demonstrated as the
main, non-microbial cause of quality deterioration during processing.
This is because lipids and proteins in meat are easily susceptible to
oxidative damages due to the rapid depletion of endogenous antioxidants after slaughter (Xiao, Zhang, Lee, & Ahn, 2013). However, the
susceptibility of meat to oxidation has also been found to be inuenced
by animal breed and species, muscle types and anatomical location
(Min, Nam, Cordray, & Ahn, 2008). The ndings of Faustman and
Cassens (1991) on two cattle breeds revealed that Holstein meat displays
a higher lipid oxidation (TBA) than cross breed beef meat. Their study
also showed that meat from the gluteus medius muscles had a higher
amount of thiobarbituric acid than the longissimus muscle type.
Different studies have shown that the amount of metal ions, such as
iron from heme compounds, copper, zinc and heavy metals that are
present in enzymes and metalloproteins or those migrated from the

A.B. Falowo et al. / Food Research International 64 (2014) 171181

173

Fig. 1. Interplay between oxidative initiation and the potential of natural antioxidants in preventing oxidation in meat. RH unsaturated fatty acid, R free radical.

processing machine, either by abrasion or due to acidic dissolving of

metals from the surface factors could promote the rate of oxidation in
meat (Jacobsen et al., 2008; Rulsek & Vondrasek, 1998). Moreover,
the type of diet consumed by animals during the production phase
has a great inuence on the susceptibility of meat to oxidation postmortem. Zhang, Xiao, Lee, and Ahn (2011) reported an increase in lipid
and protein oxidation in the breast muscles of birds that had been fed
a dietary oxidized oil diet compared to antioxidant-supplemented and
control diets. Exposure of meat to oxygen, light and temperature, as
well as preservative and processing techniques, such as chilling, freezing, additives (salt, nitrate and spices), cooking, irradiation, high pressure and packaging, could inuence the extent of oxidation. Currently,
lipid and protein oxidation is one of the biggest economic problems in
the meat industry. It compromises the nutritional quality, limits shelf
life, increases toxicity and decreases the market value of meat and
meat products (Sample, 2013). However, the rate and extent of oxidation can be retarded, reduced or prevented through the application of
natural antioxidants (Fig. 1).
Oxidation in meat is usually assessed by measuring the amount of
peroxide value (PV), thiobarbituric acid-reactive substances (TBARS),
sulphydryl and carbonyl group generated during the process. This
analysis is carried out using spectrophotometric or chromatographic
(head space gas chromatographic (GC), high-performance liquid
chromatography (HPLC), liquid chromatographic mass spectrophotometer
[(LCMS) and 2,4 dinitrophenylhy-drazine (DNPH)] methods. Recently,
studies on proteinlipid oxidation have been conducted at a molecular
level using mass spectrophotometry (MS) and liquid chromatography
tandem mass spectrophotometer (LCMS/MS) with proteomic tools to
better understand the mode of mechanism in relation to meat quality. Specically, proteomic techniques have been used to identify unique oxidation
site on creatinase kinase, actin and triosephosphate isomerase in meat
sample (Bernevic et al., 2011) and to investigate the relationship between
post-mortem sarcoplasmic proteome and oxidation generation during

storage and processing, as well as predictive markers that are sensitive to

oxidative stress in meat sample (Promeyrata et al., 2011). The adoption
of advanced instrumentation techniques to extract and isolate bioactive
compounds from plant materials, which have been used for
phytoremediation, might provide an alternative solution to the meat
industry for overcoming the challenge of oxidative instability in meat.
3.1. Lipid oxidation in meat
Lipids are widely distributed in both the intra and extracellular space
of meat as triacylglycerides, phospholipids and sterols. However, lipids
are chemically unstable and, therefore, easily prone to oxidation,
especially during post-mortem handling, and storage. Lipid oxidation results in rancid odour, off-avour development, drip losses, discolouration,
loss of nutrient value, decrease in shelf life, and the accumulation of toxic
compounds, which may be detrimental to the health of consumers
(Chaijan, 2008; Mapiye et al., 2012; Richards, Modra, & Li, 2002).
Oxidation of lipids is a three-step radical chain reaction which consists
of initiation, propagation, and termination with the production of free
radicals (Fig. 3a). Initiation reaction produces the fatty acid (alkyl) radical
(R) which in turn reacts with oxygen to form peroxy radicals (ROO) in
the propagation reaction.
The peroxy radicals react with unsaturated fatty acids and form
hydroperoxides (ROOH), which later decompose to produce the volatile
aromatic compounds that give meat its perceived off-avours and
rancid odour (Chaijan, 2008; Gordon, 2001). The interaction of alkyl
and peroxy radicals leads to the formation of non-radical products
such as aldehydes, alkanes and conjugated dienes (Wsowicz et al.,
2004). Formation of aldehydes has been found to be directly related to
the deterioration of meat colour and avour, protein stability and
functionality (Lynch, Faustman, Silbart, Rood, & Furr, 2001; Min &
Ahn, 2005). The consequence of aldehydes has also been associated
with atherosclerosis, putative mutagens and cancer formation in the

body (Duthie, Campbell, Bestwick, Stephen, & Russell, 2013). The rate
and extent of lipid oxidation are inuenced by a number of factors,
which include iron content, distribution of unsaturated fatty acids, pH
and antioxidant levels (Gatellier et al., 2007; Wsowicz et al., 2004).

42
Sheep

Longissimus dorsi

2 C

07

SD

3.2. Protein oxidation in meat

Grape seed extracts

SD = signicantly decrease lipid oxidation.

SD
SD
SD
SD
0 and 1
07
18
20
C
C
C
C
4
2
4
4
Longissimus dorsi
Longissimus dorsi
Breast meat
Breast chicken patties
166
6
35
2124

5 mg/kg
25%
1%, 3% and 5%
30 and
60 mg/kg
2.5%
Lipper species (Verbenacea leaves)
Citrus ladanifer
Moringa oleifera leaf extract
Grape pumace

Pigs
Sheep
Broiler
Broiler

SD
14
4 C
Longissimus dorsi
100
0.5%
Andrographis leaf (Andrographis paniculata Nees powder)

Goat

04
4 C
Deboned back legs meat
240
10 and 20%
Rosemary leaves

Sheep

240
3577
90
Sheep
Rabbit
Pig

SD

Nieto, Ban, and Garrido (2011a).

Bosco et al. (2014)
Botsoglou, Govaris, Ambrosiadis, and
Fletouris (2012)
Nieto, Estrada, Jordan, Garrido, & Banon
(2011b)
Karami, Alimona, Sazili, Goh, and Ivan
(2011)
Rossi et al. (2013).
Jeronimo et al. (2012)
Nkukwana et al. (2014).
Sayago-Ayerdi, Brenes, Viveros, and Goni
(2009)
Jeronimo et al. (2012)
SD
SD
SD
04
1 and 9
09
4 C
4 C
4 C

Gobert et al. (2009)

SD
12
4 C

Longissumusthoracis,
Semitendinosus
Deboned back legs meat
Longissumus dorsi
Longissumus dorsi
101

126 g/animal/
day
3.75 and 7.5%
3%
5 and 10 g/kg
PERP extract (combination of rosemary, grape citrus, marigold)
plus vitamin E
Thyme leaves (Thymus zygis ssp. gracilis
Thyme leaves (Thymus vulgaris)
Olives leaves

Cull cow

Dose in diet
Natural sources

Animal
species

Feeding duration
(days)

Meat types

Storage
(C)

Storage duration
(days)

Effect on
oxidation

References

A.B. Falowo et al. / Food Research International 64 (2014) 171181

Table 1
Effect of dose concentration, feeding duration, storage temperature and time of dietary natural antioxidant on lipid and protein oxidation compared to control diet (without natural antioxidants) in meat.

174

Protein oxidation is one of the most innovative issues in meat quality

evaluation. This is because muscle tissue contains high amounts of
proteins which play a pivotal role in meat quality regarding the sensory,
nutritional and physico-chemical properties of meat and meat products.
According to Shacter (2000), protein oxidation is described as the
covalent modication of a protein induced ROS or by reacting with
secondary by-products of oxidative stress. Protein oxidation occurs
through a chain reaction of free radicals like oxidation of lipids in animal
muscle (Lund et al., 2011). According to Lund, Heinonen, Baron, and
Estevez (2011), protein oxidation begins with the initiation processes of
abstracting hydrogen atoms from protein (PH) via ROS to form a protein
carbon-centered radical (P, reaction a) which is consequently converted
into analkylproxyl radical (POO, reaction b) in the presence of oxygen
and to an alkylperoxide (POOH, reaction c) by abstracting hydrogen
atoms from another susceptible molecule. Subsequent reactions with
ROS, such as HO2 or with reduced forms of transition metals (Mn+),
such as Fe2+ or Cu+1, lead to the production of alkoxyl radical (PO, reaction e and f) and its hydroxyl derivative (POH, reaction g). The oxidation
of protein also occurs due to the interaction between proteins, especially
the nitrogen or sulfur centers of reactive amino acid residues of protein
(PH) and lipid hydroperoxide (ROOH) or secondary lipid oxidation products, such as aldhehydes or reducing sugar (reaction h) (Baron, 2010;
Viljanen, 2005). Protein oxidation occurs through a chain reaction of
free radicals like oxidation of lipids in animal muscle. The peroxyl radicals
(ROO), formed during lipid oxidation, is absorbed by hydrogen atoms
from protein molecules (PH) through chains of reactions summarised
in Fig. 3b.
The reaction of radicals (ROS) with muscle protein and peptides in
the presence of oxygen has been found to give rise to the modication
of the amino acid side chain, formation of covalent intermolecular
cross-linked protein and protein fragmentation and aggregation (Lund
et al., 2011). Modication of amino acid side chain protein has been
reported to result in the formation of thiol group, aromatic hydroxylation
and carbonyl groups (Stadtman, 1990). The cross-linked protein has been
described as the formation of disulde and dityrosine through the loss of
cysteine and tyrosine residues (Estevez, Ollilainen, & Heinonen, 2009).
According to a review by Estevez, Kylli, Puolanne, Kivikari, and
Heinonen (2008), the modication of muscle proteins is as a result of denaturation and proteolysis-induces changes in meat quality, including
texture traits, colour, aroma, avour, water-holding capacity, and biological functionality. Protein oxidation induces multiple physico-chemical
changes and nutritional value in meat proteins including a decrease in
the bioavailability of amino acid protein, change in amino acid composition, decrease in protein solubility due to protein polymerisation, loss of
proteolytic activity, and impaired protein digestibility (Levine et al.,
1990; Lund et al., 2011).
From the foregoing, it is clear that lipid and protein oxidations are
closely associated with deteriorative processes that can affect the entire
quality traits of meat and meat products. A proportional rise in the levels
of oxidative indicators for lipid (TBARS) and protein (carbonyl groups)
skeletal meat and meat products (liver pates) showed a signicant
correlation association between muscles response to oxidative rancidity
and protein denaturation (Estevez, Ventanasa, and Cava, 2006; Xiong,
2000). In general, a multidisciplinary meat lipid science network and
utilisation of proteomic applications proposed by Mapiye et al. (2012)
and Udenogwe and Howard (2013) hold the potential of ameliorating
lipid and protein oxidation in meat and meat products. However, a strategic delivery of antioxidants from natural sources into muscle post-mortem
holds a more viable option of enriching meat with health-promoting

Table 2
Effect of dose concentration, storage temperature and time of technological natural antioxidant on lipid and protein oxidation in meat.
Dose in meat

Meat type

Storage (C)

Storage duration

Effect on oxidation

References

Oregano + sage leaves

Black currant extracts
Rosemary extracts
Rosemary extracts
Sage extracts
Olive leaf extracts
Herbal extracts (Marjoram, rosemary, sage)
Broccoli leaf extract
Curry leaf extracts (Murrayakoenigii L.)
Mint leaf extract (Menthaspicata)
Grape seed extracts
Avocado seed extract
Avocado peel extracts
Butterbur leaf extract
Grape seed extracts
Pine bark extracts
Oleoresin rosemary
Grape seed extracts
Bearberry extracts
Broccoli powder extracts
Cocoa leaf extract
Green tea leaf extract
Ginkgo biloba leaf extract

0.2% w/w each

5, 10 or 20 g/kg
0.1%
250, 500, 750 mg/kg
0.1%
100 and 200 g/g
0.04% v/w
0.1% and 0.5% w/w
5 mL extract/500 g

Chicken breast and thigh

Pork patties
Porcine liver patties
Porcine liver patties
Porcine liver patties
Minced beef patties
Ground beef
Ground beef patties
Pork meat

4 C
4 C
4 C
21 C
4 C
4 C
5 C
4 C
4 C

98 hours
9 days
90 days
2 days
90 days
9 and 12 days
41 and 48 days
12 days
012 days

SDL
SDLP
SDP
SDL in a dose dependent manner
SDP
SDL in a dose-dependent manner
SDL
SDL
SDL

Sampaio, Saldanha, Soares, and Torres (2012)

Jia, Kong, Liu, Diao, and Xia (2012).
Estevez, Ventanasa, and Cava (2006)
Doolaege et al. (2012)
Estevez et al. (2006)
Hayes, Stepanyana, Allena, O'Grady, and Kerry (2010)
Mohameda, Mansour, and Farag (2011)
Kim, Cho, and Han (2013), Kim, Min, et al. (2013)
Biswas, Chatli, and Sahoo (2012)

0.1%
50 g extracts/700 g
50 g extracts/700 g
0.1% and 0.5% w/w
1.0%
1.0%
1.0%
400 and 1000 g/g
80 and 1000 g/g
1.5 and 2%
200 mg/kg
200 mg/kg
0.05%
500 ppm
0.0005% 0.001%

Mutton slices
Porcine patties

4 C
4 C

7 days
15 days

SDL
SDLP

Reddy et al. (2013)

Rodriguez-Carpena, Morcuende, and Estvez (2011)

Ground beef patties

Cooked beef

4 C
4 C

12 days
9 days

SDL
SDL

Kim, Cho, et al. (2013), Kim, Min, et al. (2013)

Ahna, Grun, and Mustaphab (2007)

Pork patties

4 C

12 days

SDL

Carpenter, O'Grady, O'Callaghan, O'Brien, and Kerry (2007)

Goat meat nugget

Deboned Chicken meat

4 C
4 C

416 days
21 days

SDL
SDL

Banerjee et al. (2012)

Hassan and Fan (2005)

Meat dumplings
Meat ball
Pork meat

18 C
4 C
2 C 2

180 days
21 days
50 days

SDL
SDL
SDL

Kobus-Cisowska, Flaczyk, and Jeszka (2010)

Kobus-Cisowska et al. (2014)
Sanchez-Muniz et al. (2012)

Hypericum perforatum L. extract

A.B. Falowo et al. / Food Research International 64 (2014) 171181

Natural sources

SDL = signicantly decrease lipid oxidation, SDP = signicantly decrease protein oxidation, SDPL = signicantly decrease lipid and protein oxidation.

175

A.B. Falowo et al. / Food Research International 64 (2014) 171181

Kurcubic et al. (2014)
Piskernik, Klancnik, Riedel, Brondsted, and Mozina (2011)
Bukvicki et al. (2014)
Kim, Cho, et al. (2013), Kim, Min, et al. (2013)

Cruz-Galvez et al. (2013)

060 days

7 days
5 2 C

It reduces the growth of Escherichia coli.

It reduces the growth of Campylobacter jejuni.
It reduces the growth of Listeria monocytogenes.
It greatly reduces the count of lactic acid bacteria,
coliform bacteria, yeast and mold.
It reduces the multiplication of Salmonella typhimurium,
Escherichia coli,
Listeria monocytogenes, and Staphylococcus aureusin.
Fermented dry sausage
Chicken meat model
Pork meat
Ground beef patties

Raw beef meat

It reduces the growth of Pseudomonas species, Enterobacteriaceae 1% v/w

(psychrotrophic), and lactic acid bacteria.
Raw chicken meat

Effect on foodborne pathogenic organisms

Meat type

12.5 g/kg of meat dough

0.20 mg/mL
0.1620 mg/mL
0.1% and 0.5% (w/w)

4 C
8 C
25 C
4 C

4 days
012 days

Krishnan et al. (2014)

3.3. Natural antioxidant in meat and meat products

Syzygium aromaticum extracts

Cinnmomum cassia extracts
Origanum vulgare extracts
Brassica nigra extracts
Kitaibelia vitifolia extract
Rosemary extracts
Satureja horvatii essential oil
Chamnamul leaf extract
Fatsia leaf extract
Artemisia absinthium L. extract

4 C

015 days

bioactive compounds and preventing the tendency towards oxidative

rancidity/deterioration in meat and meat products.

Plants materials

Table 3
Antimicrobial activities of medicinal plants on meat and meat products compared to control.

Dosages

Storage degrees Storage time References

176

In recent years, special attention has been paid to a number of

medicinal plants that could be used as potential sources of antioxidants
for muscle food preservation and nutritional quality improvement.
Most of the plant materials (herbs and spices) possess relatively high
chemical nutrients (such as protein, fat, carbohydrate), mineral
contents (calcium, potassium, iron, phosphorus) and less anti-nutritional
properties. Moreover, the addition of natural antioxidant extracts has
been reported to increase meat tenderness (Contini et al., 2014). This
could probably mean that some natural antioxidants contain tenderizing
compounds. However, information on this nding is rarely available and
this will require a further study to investigate the tenderizing mechanisms
of natural antioxidants in meat and meat products.
3.4. Prevention of oxidation in meat using natural antioxidants
Natural antioxidants can be applied either through dietary or
technological strategies to reduce or prevent oxidative process in
muscle food (Fig. 1). In dietary manipulations, antioxidants are introduced into the muscle via the animal feed or diet. The inclusion of natural
antioxidants in animal diet as shown in Table 1 has been reported by
various authors to not only slow down oxidation, but also to greatly
improve meat quality when compared to diets with no antioxidants.
However, the concentration of antioxidant-compounds in plant materials
varies considerably and hence their dosage application in diets and meat
products varies from plant to plant (Moyo, Oyedemi, Masika, & Muchenje,
2012; Nkukwana et al., 2014). Antioxidant compounds are usually added
at a moderate dosage level (Tables 1 and 2), since high level of inclusion
may mechanistically cause adverse effects through pro-oxidative action
(Martin & Appel, 2010). Technological strategies involve the application
of antioxidants directly into the meat and meat products or by coating
packaging materials with plant extracts to improve the oxidative stability
of the products.
Most natural antioxidants are obtained from plant resources, such as
culinary herbs, spices, vegetables, as well as fruits and oilseed products
(Table 2; Shahidi & Zhong, 2010). Synthetic antioxidants, such as
butylated hydroxyanisole (BHA), butylated hydroxytoluene (BHT),
and tertiary butyl hydroquinone (TBHQ), have been used in inhibiting
meat oxidation (Fasseas, Mountzouris, Tarantilis, Polissiou, & Zervas,
2007) but with side effects. The potential of synthetic antioxidants causing toxicological effects has created demand for natural antioxidants by
consumers and the meat industry (Karre, Lopez, & Getty, 2013). Several
authors have reported the efcacy of different natural antioxidants for
reducing lipids and protein oxidation, discolouration and microbial
growth in some types of meat (Camo, Beltrn, & Roncales, 2008;
Fasseas et al., 2007; Zinoviadou, Koutsoumanis, & Biliaderis, 2009).
Phenolic compounds are the major constituents of plant materials that
contribute to their antioxidant capacity. Plants, fruits and their extracts
that reect concentrations of phenolic compounds are thus regarded as
effective sources of antioxidants to inhibit oxidation in muscle foods
(Pennington & Fisher, 2009). Some of the recent works on natural
antioxidants in meat during processing are presented in Table 2.
3.5. Anti-microbial activities of natural antioxidants on meat preservation
and security
Globally, approximately 1.3 billion tons of food, including meat, is
spoiled or wasted per year throughout the supply chain, from production
down to nal household consumption (FAO, 2011). This massive wastage
which has become a major concern to consumers, governments and food
industries is however associated with the outbreak of foodborne diseases
(Sant'Ana, 2012). Close to 50% of the total meat spoilage and wastage

A.B. Falowo et al. / Food Research International 64 (2014) 171181

177

Fig. 2. Antioxidant reaction with lipid oxidation at propagation stage to terminate oxidation cycle.

occurs at the household consumption level due to poor preservative

technique and facilities. Meat wastages are caused through microbial
and chemical spoilage with the consequence of foodborne illnesses,
economic loss and food insecurity. It has been determined that different
bacteria, like psychrophile, psychrotrophic, mesophile and thermophile,
are able to survive under various processing conditions to cause spoilage
and wastage. However, meat spoilage bacteria can be reduced by
applying natural antioxidants directly into the meat products. The
use of natural compounds such as organic acids and essential oils
has been identied for decontamination of beef, pork and poultry
products against Salmonella (Mani-Lpez, Garcia, & Lpez-Malo, 2012;
Sant'Ana, Franco, & Schaffner, 2014). The antimicrobial activities of the
essential oils and/or crude extracts from most of the natural antioxidant
plants in Tables 2 and 3, respectively, have been reported in several
studies. The effectiveness of these medicinal plants for example: Artemisia
absinthium, Hypericum perforatum, oleoresin rosemary, Origanum vulgare,
Satureja horvatii, Syzygium aromaticum, Fatsia spp., and olive among
others, against microbial growth in meat and meat products has been
reported in several studies (Table 3; Kim, Cho, et al., 2013; Kim, Min,
et al., 2013; Kurcubic et al., 2014; Sanchez-Muniz et al., 2012). Some
interesting results were however found by combining different plants
together to test their efcacy against food borne organisms that are prevalent in meat and meat products (Table 3). Krishnan et al. (2014) found a
stronger antimicrobial effect of the combination of S. aromaticum,
Cinnmomum cassia and O. vulgare extracts in chicken meat than individual
spices, and they attributed this to synergistic actions of each specic
compounds present in the mixed spices. The presence and level of
concentration of different phytochemical compounds such as phenolic,
avonoid, alkaloids, saponins, tannins, carvacrol, terpenes, and thymol
among others, have been recognised as the potential source of antimicrobial activities in plant materials (Sharma et al., 2012). Further
study should be concentrated on the combination and application of
different natural antioxidants to reduce meat spoilage and to extend
the storage time, as these will greatly help to reduce nancial loss,
labour costs, ensure safety and ultimately improve the functional
properties of the meat.

3.6. Antioxidantoxidation reaction in meat sample

Phenolic-compounds are known as secondary metabolites in plant
samples and are capable of inhibiting or delaying oxidation while they
get oxidized in the process. These compounds consist of a hydroxyl
group (OH) bonded directly to an aromatic hydrocarbon group
(Kricher, 2011, chap. 8). The numbers and positions of the OH
(which are linked to the aromatic ring) in relation to the carboxyl
functional group determines the capacity of antioxidant activities from
each plant material (Rice-Evans, 1996; Robards, 1999). Based on the
aromatic ring structures, phenolic-compounds are classied into
phenolic acid (hydroxybenzoic and hydroxycinnamic acids), avonoid
(anthocyanins, avonols, avones), diterpernes tannins (hydrolysable
and condensed tannins), stilbenes, curcuminoids, coumarins, lignans,
quinones, and others (phenolic alkaloids, phenolic terpenoids, phenolic
glycosides, volatile oil) (Fresco, Borges, Diniz, & Marques, 2006; Huang,
Cai, & Zhang, 2009).
The reaction of antioxidants with oxidation is believed to occur
through two major pathways. First is by donating electrons to break
and terminate the oxidation cycle at the propagation step and thereby
preventing additional lipid and protein radicals from forming (Allen &
Cornforth, 2010; Dangles & Dufour, 2006, Figs. 2 and 3 (Reaction 2)).
However, in the absence of antioxidants, the reaction becomes
auto-propagative leading to the production of non-radical products
(Fig. 2). Second is by removing free radical (ROS) initiators in order to
quench chain-initiating catalysts (radicals) (Antolovich, Prenzler,
Patsalides, Mc Donald, & Robards, 2002) or limiting the radicals
initiators by binding metals such as iron and copper as metal chelators
to stabilise them in an inactive or insoluble form (Allen & Cornforth,
2010; Dai & Mumper, 2010; Fig. 4a and b). Moreover, the antioxidant
free radical (oxidized antioxidant) formed in reaction b (Fig. 4) may
further interfere with chain propagation reactions by forming peroxy
antioxidant compounds as shown in reaction c (Antolovich et al.,
2002). The metal chelating power of plant materials has been proposed
to be associated with chemical composition of the sample (Goncalves,
Battistin, Pauletti, Rota, & Serani, 2009), including the presence of

178

a)

A.B. Falowo et al. / Food Research International 64 (2014) 171181

Initiation:
RH

Propagation:
R + O2ROO
ROO + RH

ROOH +R

Termination:
R + R RR
R + ROO

Non radical products

ROOR

ROO + ROO ROOR + O2

b)

PH + HO

P + H2O

(a)

P +O2

POO

(b)

POO + PH

POOH + P

(c)

medicinal plants rich-antioxidants can act as functional or nutraceutical

food to promote consumers' health and wellness compared to the use
of vitamins and synthetic antioxidants (Fig. 1). Functional foods are
food or food products that provide essential nutrients or biologically
active components beyond the basic nutrition necessary for health or
well-being of the consumers (IFT, 2014), and when it aids in prevention,
management or treatment of health disorders, are known as nutraceuticals
(El Sohaimy, 2012). According to Lobo, Patil, Phatak, and Chandra (2010),
functional food contains ingredients such as dietary bers, vitamins,
minerals, antioxidants, essential fatty acids (omega-3) and lignins while
nutraceutical contains nontoxic food extract supplement. Numerous
medicinal plants, vegetables and spices have been identied to function
in this capacity, and their application in meat can provide functional or
nutraceutical meat or meat products. The benecial effect of producing
meat products containing medicinal plant extracts would be to combat
different health related problems that have been associated with
consumption of meat over the years. Duthie et al. (2013) found that
including vegetable powder in the formulation of processed turkey
meat patties increase the antioxidant content, and this may contribute
to the prevention of meat related diseases. It has also been demonstrated
that the consumption of food (meat) rich in natural antioxidant can
reinforce the activity of the endogenous antioxidants against degenerative
diseases linked to oxidative stress and ROS-related tissue damage
(Valenzuela, Sanhueza, & Nieto, 2003). However, information on production and consumption of functional or nutraceutical meats is still scanty.
Further research will be needed to determine the amount of natural
antioxidants that is required to produce functional and nutraceutical meat.
4. Conclusion

POO +H2O

PO + O2 +H2O

POOH +Mn+

PO +HO-1 + M(n+1)+ (e)

PO +HO2

POH +O2

(f)

PO +H+ +Mn-1

POH + M(n-1)+

(g)

ROO + PH

P + ROOH or

(h)

ROOH + PH [ROOH---HP]

(d)

RO + P + H2O

Fig. 3. a: Radical-chain of processes involved in lipid oxidation in biological systems. b:

Radical-chain of processes involved in protein oxidation in biological systems. (a)
Chelating power of antioxidant. (b) Reaction of antioxidants with lipid and protein at initiation stage.

compounds, such as phytate and oxalates. Mirzaei and Khatami (2013)

found that the extract of Coriander sativum possesses higher iron
chelating activity than Petroselium crispum, while the addition of
Menthagentilis L. showed higher chelating activity than other menthe
species (Goncalves et al., 2009).

The use of bioactive compounds in plant materials as natural

antioxidants has a great antimicrobial potential to preserve meat from
oxidative deterioration. The application of natural antioxidants is
presumed necessary to boost the endogenous antioxidant against
oxidative stress in farm animals and prevent lipidprotein oxidation
in meat and meat products. However, since the effect of oxidative stress
on meat quality has not been adequately investigated, there is a need to
explore this area to curb the challenges of quality losses due to oxidation.
Possibility of getting a viable solution to this challenge still lies in efcient
use of medicinal-plant-rich antioxidants to preserve the functionality of
meat and ensure production of meat products with nutraceutical
properties.
Acknowledgements
The authors are grateful to Govan Mbeki Research and Development
Centre (GMRDC) of the University of Fort Hare (UFH) for providing
nancial assistance for this work as part of the UFH's support to the
Department of Science and Technology/National Research Foundation
(DST/NRF) South African Research Chairs Initiative (SARChI) Chair in
Meat Science: Genomics to Nutriomics which is jointly hosted by the
Universities of Stellenbosch and Fort Hare. We are also grateful to Dr.
Oyedemi Sunday for his initial criticism of the article.

3.7. Edible medicinal plants as natural antioxidant in meat and future

perspectives

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