Natural antioxidants against lipid–protein oxidative deterioration in meat and meat products: A...
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Review Natural antioxidants against lipid–protein 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 abstract article info Article history: Received 29 April 2014 Accepted 15 June 2014 Available online 21 June 2014 Keywords: Free radical Meat quality Natural antioxidants Lipid–protein oxidation Oxidative stress 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 lipid–protein 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. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 171 2. Oxidative stress and implications on pre-slaughter welfare of animals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 172 2.1. Effects of oxidative stress on meat quality . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 172 3. Oxidation in meat and meat products . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 172 3.1. Lipid oxidation in meat . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 173 3.2. Protein oxidation in meat . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 174 3.3. Natural antioxidant in meat and meat products . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 176 3.4. Prevention of oxidation in meat using natural antioxidants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 176 3.5. Anti-microbial activities of natural antioxidants on meat preservation and security . . . . . . . . . . . . . . . . . . . . . . . . . . 176 3.6. Antioxidant–oxidation reaction in meat sample . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 177 3.7. Edible medicinal plants as natural antioxidant in meat and future perspectives . . . . . . . . . . . . . . . . . . . . . . . . . . . . 178 4. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 178 Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 178 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 178 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 flavour, formation of toxic compounds, poor shelf life, nutrient and 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 2–5%) 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 oxidation–reduction reactions (Moylan et al., 2014; Wiseman and Halliwell, 1996). Food Research International 64 (2014) 171–181 ⁎ Corresponding author. Tel.: +27 406022059; fax: +27 86 628 2967. E-mail address: [email protected] (V. Muchenje). http://dx.doi.org/10.1016/j.foodres.2014.06.022 0963-9969/© 2014 Elsevier Ltd. All rights reserved. Contents lists available at ScienceDirect Food Research International journal homepage: www.elsevier.com/locate/foodres
Transcript of Natural antioxidants against lipid–protein oxidative deterioration in meat and meat products: A...
Food Research International 64 (2014) 171–181
Contents lists available at ScienceDirect
Food Research International
j ourna l homepage: www.e lsev ie r .com/ locate / foodres
Review
Natural antioxidants against lipid–protein oxidative deterioration inmeat 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
⁎ Corresponding author. Tel.: +27 406022059; fax: +2E-mail address: [email protected] (V. Muchenje).
http://dx.doi.org/10.1016/j.foodres.2014.06.0220963-9969/© 2014 Elsevier Ltd. All rights reserved.
a b s t r a c t
a r t i c l e i n f oArticle history:Received 29 April 2014Accepted 15 June 2014Available online 21 June 2014
Keywords:Free radicalMeat qualityNatural antioxidantsLipid–protein oxidationOxidative stress
Oxidation is a well-known non-microbial cause of quality loss in meat. Oxidative stress occurs due to unevengeneration of free radicals reactive oxygen species (ROS) and reactive nitrogen species (RNS) which triggersoxidative 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 offunctional integrity of oxidised meat hitherto remains a challenge to the meat industry. A search for a viablealternative amidst the unexploited novel sources of natural antioxidants stands as a sustainable option forpreserving the meat quality. In this paper, the potential use of bioactive compounds in medicinal plants isreviewed as phytoremedy against lipid–protein oxidation. Synergistic antimicrobial potentials of these naturalantioxidants are also revealed against oxidative deterioration in meat and meat products and, for enhancingtheir functional properties.
© 2014 Elsevier Ltd. All rights reserved.
Contents
1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1712. Oxidative stress and implications on pre-slaughter welfare of animals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 172
2.1. Effects of oxidative stress on meat quality . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1723. Oxidation in meat and meat products . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 172
3.1. Lipid oxidation in meat . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1733.2. Protein oxidation in meat . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1743.3. Natural antioxidant in meat and meat products . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1763.4. Prevention of oxidation in meat using natural antioxidants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1763.5. Anti-microbial activities of natural antioxidants on meat preservation and security . . . . . . . . . . . . . . . . . . . . . . . . . . 1763.6. Antioxidant–oxidation reaction in meat sample . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1773.7. Edible medicinal plants as natural antioxidant in meat and future perspectives . . . . . . . . . . . . . . . . . . . . . . . . . . . . 178
4. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 178Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 178References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 178
1. Introduction
Oxidation is one of themajor causes of quality deterioration inmeat.Meat becomes susceptible to oxidative deterioration due to highconcentrations of unsaturated lipids, heme pigments, metal catalysts anda range of oxidizing agents in the muscle tissue. Oxidative deteriorationin any type of meat manifests in form of discoloration, development ofoff flavour, formation of toxic compounds, poor shelf life, nutrient and
7 86 628 2967.
drip losses, respectively (Contini et al., 2014; Palmieri & Sblendorio,2007). Under normal physiologic conditions, the molecular oxygenundergoes a series of reactions that leads to the generation of free radicals.A small portion (about 2–5%) of the oxygen consumed during themetabolic reaction is converted to free radicals in the form of reactiveoxygen species (ROS). These free radicals, particularly, the reactiveoxygen species (ROS) and reactive nitrogen species (RNS), play keyregulatory roles in several homeostatic processes by interacting withproteins, fatty acids and nucleic acids. They act as intermediate agentsin essential oxidation–reduction reactions (Moylan et al., 2014;Wiseman and Halliwell, 1996).
172 A.B. Falowo et al. / Food Research International 64 (2014) 171–181
Fundamentally, when the production of ROS [(superoxide anions(O2
−), peroxyl (RO2–), alkoxyl (RO−), hydroxyl radicals, singletoxygen)] and RNS [(nitric oxide radical (NO−), peroxynitrite (ONOO−)and nitrogen dioxide radical NO2
−)] does not exceed the capacity ofendogenous antioxidant barriers in the body, it performs beneficialfunctions which include: the control of gene expression, regulation ofcell signalling pathways, modulation of skeletal muscle and defenceagainst invading pathogens. In contrast, when in excess and the activityof antioxidant defence is low, it potentially causes damage to cellularcomponents, induces harmful autoimmune responses and causesoxidative and/or nitrosative stress (Barbieri & Sestili, 2012; Power &Jackson, 2008). In general, oxidative stress which is caused by animbalance between the production of ROS and antioxidant defencemechanisms in multicellular organism (da Silva, Marques, & Chaveiro,2010; Sung, Hsu, Chen, Lin, &Wu, 2013) often leads to themodificationof redox cell signalling and activation of pathways, and mechanismsinvolved in cardiovascular or chronic health problems (Alfadda &Sallam, 2012; Gutierrez & Elkind, 2012).
Understanding the activity of free radicals inmeat 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 depletionof essential amino acids like phenylalanine and trypotophan (Ganhao,Morcuende, & Estevez, 2010). Also, the degradation of unsaponifiableand polyunsaturated fatty acid fractions of meat lipids and the conver-sion of oxymyoglobin [oxyMb (Fe2+)] to metmyoglobin [MetMb(Fe3+)] pigment resulting in the generation of free radicals might leadto deterioration of meat protein (Suman & Joseph, 2013). Althoughantioxidants have the capacity to avert tissue damage by preventingthe formation of radicals, by scavenging them or by promoting theirdecomposition, the use of synthetic antioxidants is also found to imposehealth risks to man. Consequently, there is a need to explore a suitablealternative from natural sources, such as plant-derived antioxidants, tocombat the challenges of oxidative instability of lipids and protein inmeat. Aside from this, while the interest in oxidative stress and antioxi-dant activities continues to grow rapidly, many questions still remainunanswered as to how the chain of events prior to the conversion ofmuscle to meat can reduce oxidative stress in meat. In this review,attempts were made to address these issues and appraise the potentialuse of natural bioactive compounds from medicinal plants to ameliorateoxidative stress in meat, to prevent lipid–protein oxidation and improveoxidative stability in meat and meat products.
2. Oxidative stress and implications on pre-slaughter welfare ofanimals
The termoxidative stress is used to describe the condition of oxidativedamage as a result of an unfavourable critical balance between freeradical generation and antioxidant defences (Mc Cord, 2000; Rock,Jacob, & Bowen, 2009). Oxidative stress may occur due to succession ofstimuli that disrupt the homeostatic condition of an animal beforeslaughter (Cataldi, 2010). These external stimuli result from stressimposed on animals during transportation. The effects of rough handlingduring traditional slaughter, loading or unloading, poor road conditions,over-speeding and vibration of the vehicle, distance covered from farmto the abattoir, overcrowding in the vehicle, deprivation of food andwater, mixing of animals with unfamiliar ones, aggressive behaviourand stunning are common sources of oxidative stressors (Fayemi &Muchenje, 2012; Minka & Ayo, 2009; Warriss, 2000, chap. 4). Othersources 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 fromfarm to slaughter point at the abattoir often result in pains, compromisetheir welfare, distort their normal behaviour and cause undesirablechanges in meat quality (Fayemi & Muchenje, 2013). Animals
experiencing these stressors may have fractures in the bones andbruises in the muscle (Broom, 2000). The stress may also cause anabnormal rise in heart rate, blood pressure and body temperature.They can also instigate rapid release of enzymes, cortisols and catechol-amines which may lead to the depletion of glycogen, high meat ultimatepH (pHu) and dark cuts (Chulayo & Muchenje, 2013; Muchenje, Dzama,Chimonyo, Strydom, & Raats, 2009). Overproduction of ROS (oxidants) inmuscle tissue and the release of stress hormones into the blood streamalso occur in the process (Fergusona & Warner, 2008; Piccione et al.,2013). The occurrence of lipid oxidation in muscle food, due to oxidativedamage inmuscle tissue and the eventual negative effect onmeat 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 stressor several disease conditions, including sepsis, mastitis, enteritis,pneumonia, respiratory and joint diseases (Lykkesfeldt & Svendsen,2007) results in functional and/or structural damage to muscleorganelles, cells and tissues. It has been found that myofibril protein isaffected by ROS during meat maturation and storage (Martinaud,Mercier, Marinova, & Tassy, 1997) and that high production of freeradicals and ROS results in degenerative damage of cellular structureand affect meat quality (Piccione et al., 2013). It has also been demon-strated that oxidative stress affects meat tenderness. Evidence for this isshownby the ability of ROS to influence the turnover of the intramuscularcollagen, in terms of the balance between its degradation by the enzymematrix metalloproteinase-2 (EMP-2) and synthesis by intramuscularfibroblasts derived from bovine muscles (Archile-Contreras & Purslow,2011). The findings showed that ROS increased EMP-2 activity andreduced collagen synthesis in the muscle. This reduction in the collagensynthesis results in a decrease in collagen solubility and hence increasesmeat toughness. The same authors also reported the problem of inconsis-tency in meat tenderness in the meat industry, which may perhaps haveresulted from an increase in ROS production when farm animals wereexposed to different types and degrees of stresses. However, since noevidence is available on how the use of medicinal plants could play avital role in this regard, it would be necessary to test the efficacy of thebioactive compounds in their roots, leaves, flowers or stem backs on themoderation of ROS generation, meat tenderness and other qualityparameters
3. Oxidation in meat and meat products
Since the discovery of oxygen in the early 18th century and itsinevitable roles in plants and animals, the necessity to control its levelsand impacts on food and food products, especially during processing,packaging and distribution, has been a major challenge in the foodindustry. Basically, oxidation involves the loss of at least one electronwhen chemicals in the food are exposed to oxygen in the air. Oxidationin lipid and protein fractions of meat has been demonstrated as themain, non-microbial cause of quality deterioration during processing.This is because lipids and proteins in meat are easily susceptible tooxidative damages due to the rapid depletion of endogenous antioxi-dants after slaughter (Xiao, Zhang, Lee, & Ahn, 2013). However, thesusceptibility of meat to oxidation has also been found to be influencedby animal breed and species, muscle types and anatomical location(Min, Nam, Cordray, & Ahn, 2008). The findings of Faustman andCassens (1991) on two cattle breeds revealed that Holsteinmeat displaysa higher lipid oxidation (TBA) than cross breed beef meat. Their studyalso showed that meat from the gluteus medius muscles had a higheramount of thiobarbituric acid than the longissimusmuscle type.
Different studies have shown that the amount of metal ions, such asiron from heme compounds, copper, zinc and heavy metals that arepresent in enzymes and metalloproteins or those migrated from the
Fig. 1. Interplay between oxidative initiation and the potential of natural antioxidants in preventing oxidation in meat. RH — unsaturated fatty acid, R — free radical.
173A.B. Falowo et al. / Food Research International 64 (2014) 171–181
processing machine, either by abrasion or due to acidic dissolving ofmetals from the surface factors could promote the rate of oxidation inmeat (Jacobsen et al., 2008; Rulısek & Vondrasek, 1998). Moreover,the type of diet consumed by animals during the production phasehas a great influence on the susceptibility of meat to oxidation post-mortem. Zhang, Xiao, Lee, and Ahn (2011) reported an increase in lipidand protein oxidation in the breast muscles of birds that had been feda dietary oxidized oil diet compared to antioxidant-supplemented andcontrol diets. Exposure of meat to oxygen, light and temperature, aswell as preservative and processing techniques, such as chilling, freez-ing, additives (salt, nitrate and spices), cooking, irradiation, high pres-sure and packaging, could influence the extent of oxidation. Currently,lipid and protein oxidation is one of the biggest economic problems inthe meat industry. It compromises the nutritional quality, limits shelflife, increases toxicity and decreases the market value of meat andmeat products (Sample, 2013). However, the rate and extent of oxida-tion can be retarded, reduced or prevented through the application ofnatural antioxidants (Fig. 1).
Oxidation in meat is usually assessed by measuring the amount ofperoxide value (PV), thiobarbituric acid-reactive substances (TBARS),sulphydryl and carbonyl group generated during the process. Thisanalysis is carried out using spectrophotometric or chromatographic(head space gas chromatographic (GC), high-performance liquidchromatography (HPLC), liquid chromatographicmass spectrophotometer[(LC–MS) and 2,4 dinitrophenylhy-drazine (DNPH)] methods. Recently,studies on protein–lipid oxidation have been conducted at a molecularlevel using mass spectrophotometry (MS) and liquid chromatography–tandem mass spectrophotometer (LC–MS/MS) with proteomic tools tobetter understand themode ofmechanism in relation tomeat quality. Spe-cifically, proteomic techniques have beenused to identify unique oxidationsite on creatinase kinase, actin and triosephosphate isomerase in meatsample (Bernevic et al., 2011) and to investigate the relationship betweenpost-mortem sarcoplasmic proteome and oxidation generation during
storage and processing, as well as predictive markers that are sensitive tooxidative stress in meat sample (Promeyrata et al., 2011). The adoptionof advanced instrumentation techniques to extract and isolate bioactivecompounds from plant materials, which have been used forphytoremediation, might provide an alternative solution to the meatindustry for overcoming the challenge of oxidative instability in meat.
3.1. Lipid oxidation in meat
Lipids arewidely distributed in both the intra and extracellular spaceof meat as triacylglycerides, phospholipids and sterols. However, lipidsare chemically unstable and, therefore, easily prone to oxidation,especially during post-mortem handling, and storage. Lipid oxidation re-sults in rancid odour, off-flavour development, drip losses, discolouration,loss of nutrient value, decrease in shelf life, and the accumulation of toxiccompounds, 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 consistsof initiation, propagation, and termination with the production of freeradicals (Fig. 3a). Initiation reaction produces the fatty acid (alkyl) radical(R•) which in turn reacts with oxygen to form peroxy radicals (ROO•) inthe propagation reaction.
The peroxy radicals react with unsaturated fatty acids and formhydroperoxides (ROOH), which later decompose to produce the volatilearomatic compounds that give meat its perceived off-flavours andrancid odour (Chaijan, 2008; Gordon, 2001). The interaction of alkyland peroxy radicals leads to the formation of non-radical productssuch as aldehydes, alkanes and conjugated dienes (Wsowicz et al.,2004). Formation of aldehydes has been found to be directly related tothe deterioration of meat colour and flavour, protein stability andfunctionality (Lynch, Faustman, Silbart, Rood, & Furr, 2001; Min &Ahn, 2005). The consequence of aldehydes has also been associatedwith atherosclerosis, putative mutagens and cancer formation in the
Table1
Effect
ofdo
seco
ncen
tration,
feed
ingdu
ration
,storage
tempe
rature
andtimeof
dietaryna
turala
ntioxida
nton
lipid
andproteinox
idationco
mpa
redto
controld
iet(w
itho
utna
turala
ntioxida
nts)
inmeat.
Natural
sources
Dosein
diet
Animal
species
Feed
ingdu
ration
(day
s)Meattype
sStorag
e(°C)
Storag
edu
ration
(day
s)Effect
onox
idation
Referenc
es
PERP
extract(
combina
tion
ofrosemary,grap
ecitrus
,marigold)
plus
vitamin
E12
6g/an
imal/
day
Cullco
w10
1Long
issumusthoracis,
Semite
ndinosus
4°C
12SD
Gob
ertet
al.(20
09)
Thym
eleav
es(Thy
mus
zygisssp.
gracilis
3.75
and7.5%
Shee
p24
0Deb
oned
back
legs
mea
t4°C
0–4
SDNieto,B
añón
,and
Garrido
(201
1a).
Thym
eleav
es(Thy
mus
vulgaris)
3%Ra
bbit
35–77
Long
issumus
dorsi
4°C
1an
d9
SDBo
scoet
al.(20
14)
Oliv
esleav
es5an
d10
g/kg
Pig
90Long
issumus
dorsi
4°C
0–9
SDBo
tsog
lou,
Gov
aris,A
mbrosiadis,an
dFletou
ris(201
2)Ro
semaryleav
es10
and20
%Sh
eep
240
Deb
oned
back
legs
mea
t4°C
0–4
SDNieto,E
strada
,Jorda
n,Garrido
,&Ba
non
(201
1b)
Androg
raph
isleaf
(And
rograp
hispa
niculata
Nee
spo
wde
r)0.5%
Goa
t10
0Long
issimus
dorsi
4°C
14SD
Karam
i,Alim
ona,Sazili,
Goh
,and
Ivan
(201
1)Lipp
ersp
ecies(V
erbe
nacealeav
es)
5mg/kg
Pigs
166
Long
issimus
dorsi
4°C
0an
d1
SDRo
ssie
tal.(201
3).
Citrus
lada
nifer
25%
Shee
p6
Long
issimus
dorsi
2°C
0–7
SDJeronimoet
al.(20
12)
Moringa
oleifera
leaf
extract
1%,3
%an
d5%
Broiler
35Brea
stmea
t4°C
1–8
SDNku
kwan
aet
al.(20
14).
Grape
pumace
30an
d60
mg/kg
Broiler
21–24
Brea
stch
icke
npa
tties
4°C
20SD
Saya
go-A
yerdi,Bren
es,V
iveros,and
Gon
i(200
9)Grape
seed
extracts
2.5%
Shee
p42
Long
issimus
dorsi
2°C
0–7
SDJeronimoet
al.(20
12)
SD=
sign
ificantly
decrease
lipid
oxidation.
174 A.B. Falowo et al. / Food Research International 64 (2014) 171–181
body (Duthie, Campbell, Bestwick, Stephen, & Russell, 2013). The rateand extent of lipid oxidation are influenced by a number of factors,which include iron content, distribution of unsaturated fatty acids, pHand antioxidant levels (Gatellier et al., 2007; Wsowicz et al., 2004).
3.2. Protein oxidation in meat
Protein oxidation is oneof themost innovative issues inmeat qualityevaluation. This is because muscle tissue contains high amounts ofproteinswhich play a pivotal role inmeat quality regarding the sensory,nutritional and physico-chemical properties ofmeat andmeat products.According to Shacter (2000), protein oxidation is described as thecovalent modification of a protein induced ROS or by reacting withsecondary by-products of oxidative stress. Protein oxidation occursthrough a chain reaction of free radicals like oxidation of lipids in animalmuscle (Lund et al., 2011). According to Lund, Heinonen, Baron, andEstevez (2011), protein oxidation begins with the initiation processes ofabstracting hydrogen atoms from protein (PH) via ROS to form a proteincarbon-centered radical (P•, reaction a) which is consequently convertedinto analkylproxyl radical (POO•, reaction b) in the presence of oxygenand to an alkylperoxide (POOH, reaction c) by abstracting hydrogenatoms from another susceptible molecule. Subsequent reactions withROS, 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•, reac-tion e and f) and its hydroxyl derivative (POH, reaction g). The oxidationof protein also occurs due to the interaction between proteins, especiallythe nitrogen or sulfur centers of reactive amino acid residues of protein(PH) and lipid hydroperoxide (ROOH) or secondary lipid oxidation prod-ucts, such as aldhehydes or reducing sugar (reaction h) (Baron, 2010;Viljanen, 2005). Protein oxidation occurs through a chain reaction offree radicals like oxidation of lipids in animalmuscle. The peroxyl radicals(ROO•), formed during lipid oxidation, is absorbed by hydrogen atomsfrom protein molecules (PH) through chains of reactions summarisedin Fig. 3b.
The reaction of radicals (ROS) with muscle protein and peptides inthe presence of oxygen has been found to give rise to the modificationof the amino acid side chain, formation of covalent intermolecularcross-linked protein and protein fragmentation and aggregation (Lundet al., 2011). Modification of amino acid side chain protein has beenreported to result in the formation of thiol group, aromatic hydroxylationand carbonyl groups (Stadtman, 1990). The cross-linkedprotein has beendescribed as the formation of disulfide and dityrosine through the loss ofcysteine and tyrosine residues (Estevez, Ollilainen, & Heinonen, 2009).According to a review by Estevez, Kylli, Puolanne, Kivikari, andHeinonen (2008), themodification of muscle proteins is as a result of de-naturation and proteolysis-induces changes in meat quality, includingtexture traits, colour, aroma, flavour, water-holding capacity, and biolog-ical functionality. Protein oxidation induces multiple physico-chemicalchanges and nutritional value in meat proteins including a decrease inthe bioavailability of amino acid protein, change in amino acid composi-tion, decrease in protein solubility due to protein polymerisation, loss ofproteolytic activity, and impaired protein digestibility (Levine et al.,1990; Lund et al., 2011).
From the foregoing, it is clear that lipid and protein oxidations areclosely associatedwith deteriorative processes that can affect the entirequality traits ofmeat andmeat products. A proportional rise in the levelsof oxidative indicators for lipid (TBARS) and protein (carbonyl groups)skeletal meat and meat products (liver pates) showed a significantcorrelation association betweenmuscles response to oxidative rancidityand protein denaturation (Estevez, Ventanasa, and Cava, 2006; Xiong,2000). In general, a multidisciplinary “meat lipid science network” andutilisation of proteomic applications proposed by Mapiye et al. (2012)and Udenogwe and Howard (2013) hold the potential of amelioratinglipid and protein oxidation inmeat andmeat products. However, a strate-gic delivery of antioxidants fromnatural sources intomuscle post-mortemholds a more viable option of enriching meat with health-promoting
Table 2Effect of dose concentration, storage temperature and time of technological natural antioxidant on lipid and protein oxidation in meat.
Natural sources Dose in meat Meat type Storage (°C) Storage duration Effect on oxidation References
Oregano + sage leaves 0.2% w/w each Chicken breast and thigh 4 °C 98 hours SDL Sampaio, Saldanha, Soares, and Torres (2012)Black currant extracts 5, 10 or 20 g/kg Pork patties 4 °C 9 days SDLP Jia, Kong, Liu, Diao, and Xia (2012).Rosemary extracts 0.1% Porcine liver patties 4 °C 90 days SDP Estevez, Ventanasa, and Cava (2006)Rosemary extracts 250, 500, 750 mg/kg Porcine liver patties −21 °C 2 days SDL in a dose dependent manner Doolaege et al. (2012)Sage extracts 0.1% Porcine liver patties 4 °C 90 days SDP Estevez et al. (2006)Olive leaf extracts 100 and 200 μg/g Minced beef patties 4 °C 9 and 12 days SDL in a dose-dependent manner Hayes, Stepanyana, Allena, O'Grady, and Kerry (2010)Herbal extracts (Marjoram, rosemary, sage) 0.04% v/w Ground beef 5 °C 41 and 48 days SDL Mohameda, Mansour, and Farag (2011)Broccoli leaf extract 0.1% and 0.5% w/w Ground beef patties 4 °C 12 days SDL Kim, Cho, and Han (2013), Kim, Min, et al. (2013)Curry leaf extracts (Murrayakoenigii L.)Mint leaf extract (Menthaspicata)
5 mL extract/500 g Pork meat 4 °C 0–12 days SDL Biswas, Chatli, and Sahoo (2012)
Grape seed extracts 0.1% Mutton slices 4 °C 7 days SDL Reddy et al. (2013)Avocado seed extract 50 g extracts/700 g Porcine patties 4 °C 15 days SDLP Rodriguez-Carpena, Morcuende, and Estévez (2011)Avocado peel extracts 50 g extracts/700 gButterbur leaf extract 0.1% and 0.5% w/w Ground beef patties 4 °C 12 days SDL Kim, Cho, et al. (2013), Kim, Min, et al. (2013)Grape seed extracts 1.0% Cooked beef 4 °C 9 days SDL Ahna, Grun, and Mustaphab (2007)Pine bark extracts 1.0%Oleoresin rosemary 1.0%Grape seed extracts 400 and 1000 μg/g Pork patties 4 °C 12 days SDL Carpenter, O'Grady, O'Callaghan, O'Brien, and Kerry (2007)Bearberry extracts 80 and 1000 μg/gBroccoli powder extracts 1.5 and 2% Goat meat nugget 4 °C 4–16 days SDL Banerjee et al. (2012)Cocoa leaf extract 200 mg/kg Deboned Chicken meat 4 °C 21 days SDL Hassan and Fan (2005)Green tea leaf extract 200 mg/kgGinkgo biloba leaf extract 0.05% Meat dumplings –18 °C 180 days SDL Kobus-Cisowska, Flaczyk, and Jeszka (2010)
500 ppm Meat ball 4 °C 21 days SDL Kobus-Cisowska et al. (2014)Hypericum perforatum L. extract 0.0005% 0.001% Pork meat 2 °C ± 2 50 days SDL Sanchez-Muniz et al. (2012)
SDL = significantly decrease lipid oxidation, SDP = significantly decrease protein oxidation, SDPL = significantly decrease lipid and protein oxidation.
175A.B.Falow
oetal./Food
ResearchInternational64
(2014)171
–181
Table3
Antim
icrobial
activities
ofmed
icinal
plan
tson
mea
tand
meatprod
ucts
compa
redto
control.
Plan
tsmaterials
Mea
ttype
Effect
onfood
bornepa
thog
enicorga
nism
sDosag
esStorag
ede
gree
sStorag
etime
Referenc
es
Syzygium
arom
aticum
extracts
Cinn
mom
umcassia
extracts
Origa
num
vulgareex
tracts
Brassica
nigraex
tracts
Raw
chicke
nmeat
Itredu
cesthegrow
thof
Pseu
domon
assp
ecies,En
teroba
cteriaceae
(psych
rotrop
hic),and
lactic
acid
bacteria.
1%v/w
4°C
0–15
days
Krish
nanet
al.(20
14)
Kita
ibelia
vitifolia
extract
Ferm
enteddrysaus
age
Itredu
cesthegrow
thof
Escherichiacoli.
12.5
g/kg
ofmeatd
ough
4°C
0–60
days
Kurcu
bicet
al.(20
14)
Rosemaryex
tracts
Chicke
nmea
tmod
elItredu
cesthegrow
thof
Campy
loba
cter
jejuni.
0.20
mg/mL
8°C
Piskernik,Klanc
nik,Ried
el,B
rond
sted
,and
Moz
ina(201
1)Satureja
horvatiiessentialo
ilPo
rkmeat
Itredu
cesthegrow
thof
Listeria
mon
ocytog
enes.
0.16
–20
mg/mL
25°C
4da
ysBu
kvicki
etal.(20
14)
Cham
namul
leaf
extract
Fatsia
leaf
extract
Groun
dbe
efpa
tties
Itgreatlyredu
cesthecoun
tof
lacticacid
bacteria,
coliform
bacteria,y
east
andmold.
0.1%
and0.5%
(w/w
)4°C
0–12
days
Kim
,Cho
,eta
l.(201
3),K
im,M
in,eta
l.(201
3)
Artemisia
absinthium
L.ex
tract
Raw
beef
meat
Itredu
cesthemultiplicationof
Salm
onella
typh
imurium,
Escherichiacoli,
Listeria
mon
ocytog
enes,and
Stap
hylococcus
aureusin.
5±
2°C
7da
ysCruz
-Galve
zet
al.(20
13)
176 A.B. Falowo et al. / Food Research International 64 (2014) 171–181
bioactive compounds and preventing the tendency towards oxidativerancidity/deterioration in meat and meat products.
3.3. Natural antioxidant in meat and meat products
In recent years, special attention has been paid to a number ofmedicinal plants that could be used as potential sources of antioxidantsfor muscle food preservation and nutritional quality improvement.Most of the plant materials (herbs and spices) possess relatively highchemical nutrients (such as protein, fat, carbohydrate), mineralcontents (calcium, potassium, iron, phosphorus) and less anti-nutritionalproperties. Moreover, the addition of natural antioxidant extracts hasbeen reported to increase meat tenderness (Contini et al., 2014). Thiscould probably mean that some natural antioxidants contain tenderizingcompounds. However, information on this finding is rarely available andthis will require a further study to investigate the tenderizingmechanismsof 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 ortechnological strategies to reduce or prevent oxidative process inmuscle food (Fig. 1). In dietary manipulations, antioxidants are intro-duced into themuscle via the animal feed or diet. The inclusion of naturalantioxidants in animal diet as shown in Table 1 has been reported byvarious authors to not only slow down oxidation, but also to greatlyimprove meat quality when compared to diets with no antioxidants.However, the concentration of antioxidant-compounds in plantmaterialsvaries considerably and hence their dosage application in diets andmeatproducts varies fromplant to plant (Moyo, Oyedemi,Masika, &Muchenje,2012; Nkukwana et al., 2014). Antioxidant compounds are usually addedat a moderate dosage level (Tables 1 and 2), since high level of inclusionmay mechanistically cause adverse effects through pro-oxidative action(Martin & Appel, 2010). Technological strategies involve the applicationof antioxidants directly into the meat and meat products or by coatingpackagingmaterials with plant extracts to improve the oxidative stabilityof the products.
Most natural antioxidants are obtained fromplant resources, such asculinary herbs, spices, vegetables, as well as fruits and oilseed products(Table 2; Shahidi & Zhong, 2010). Synthetic antioxidants, such asbutylated hydroxyanisole (BHA), butylated hydroxytoluene (BHT),and tertiary butyl hydroquinone (TBHQ), have been used in inhibitingmeat oxidation (Fasseas, Mountzouris, Tarantilis, Polissiou, & Zervas,2007) butwith side effects. The potential of synthetic antioxidants caus-ing toxicological effects has created demand for natural antioxidants byconsumers and themeat industry (Karre, Lopez, & Getty, 2013). Severalauthors have reported the efficacy of different natural antioxidants forreducing lipids and protein oxidation, discolouration and microbialgrowth in some types of meat (Camo, Beltrán, & Roncales, 2008;Fasseas et al., 2007; Zinoviadou, Koutsoumanis, & Biliaderis, 2009).Phenolic compounds are the major constituents of plant materials thatcontribute to their antioxidant capacity. Plants, fruits and their extractsthat reflect concentrations of phenolic compounds are thus regarded aseffective sources of antioxidants to inhibit oxidation in muscle foods(Pennington & Fisher, 2009). Some of the recent works on naturalantioxidants in meat during processing are presented in Table 2.
3.5. Anti-microbial activities of natural antioxidants on meat preservationand security
Globally, approximately 1.3 billion tons of food, including meat, isspoiled or wasted per year throughout the supply chain, from productiondown tofinal household consumption (FAO, 2011). Thismassivewastagewhich has become amajor concern to consumers, governments and foodindustries is however associatedwith the outbreak of foodborne diseases(Sant'Ana, 2012). Close to 50% of the total meat spoilage and wastage
Fig. 2. Antioxidant reaction with lipid oxidation at propagation stage to terminate oxidation cycle.
177A.B. Falowo et al. / Food Research International 64 (2014) 171–181
occurs at the household consumption level due to poor preservativetechnique and facilities. Meat wastages are caused through microbialand chemical spoilage with the consequence of foodborne illnesses,economic loss and food insecurity. It has been determined that differentbacteria, like psychrophile, psychrotrophic, mesophile and thermophile,are able to survive under various processing conditions to cause spoilageand wastage. However, meat spoilage bacteria can be reduced byapplying natural antioxidants directly into the meat products. Theuse of natural compounds such as organic acids and essential oilshas been identified for decontamination of beef, pork and poultryproducts against Salmonella (Mani-López, Garcia, & López-Malo, 2012;Sant'Ana, Franco, & Schaffner, 2014). The antimicrobial activities of theessential oils and/or crude extracts from most of the natural antioxidantplants in Tables 2 and 3, respectively, have been reported in severalstudies. The effectiveness of thesemedicinal plants for example:Artemisiaabsinthium,Hypericum perforatum, oleoresin rosemary,Origanum vulgare,Satureja horvatii, Syzygium aromaticum, Fatsia spp., and olive amongothers, against microbial growth in meat and meat products has beenreported in several studies (Table 3; Kim, Cho, et al., 2013; Kim, Min,et al., 2013; Kurcubic et al., 2014; Sanchez-Muniz et al., 2012). Someinteresting results were however found by combining different plantstogether to test their efficacy against food borne organisms that are prev-alent inmeat andmeat products (Table 3). Krishnan et al. (2014) found astronger antimicrobial effect of the combination of S. aromaticum,Cinnmomumcassia andO. vulgare extracts in chickenmeat than individualspices, and they attributed this to synergistic actions of each specificcompounds present in the mixed spices. The presence and level ofconcentration of different phytochemical compounds such as phenolic,flavonoid, alkaloids, saponins, tannins, carvacrol, terpenes, and thymolamong others, have been recognised as the potential source of antimi-crobial activities in plant materials (Sharma et al., 2012). Furtherstudy should be concentrated on the combination and application ofdifferent natural antioxidants to reduce meat spoilage and to extendthe storage time, as these will greatly help to reduce financial loss,labour costs, ensure safety and ultimately improve the functionalproperties of the meat.
3.6. Antioxidant–oxidation reaction in meat sample
Phenolic-compounds are known as secondary metabolites in plantsamples and are capable of inhibiting or delaying oxidation while theyget oxidized in the process. These compounds consist of a hydroxylgroup (–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 carboxylfunctional group determines the capacity of antioxidant activities fromeach plant material (Rice-Evans, 1996; Robards, 1999). Based on thearomatic ring structures, phenolic-compounds are classified intophenolic acid (hydroxybenzoic and hydroxycinnamic acids), flavonoid(anthocyanins, flavonols, flavones), diterpernes tannins (hydrolysableand condensed tannins), stilbenes, curcuminoids, coumarins, lignans,quinones, and others (phenolic alkaloids, phenolic terpenoids, phenolicglycosides, volatile oil) (Fresco, Borges, Diniz, & Marques, 2006; Huang,Cai, & Zhang, 2009).
The reaction of antioxidants with oxidation is believed to occurthrough two major pathways. First is by donating electrons to breakand terminate the oxidation cycle at the propagation step and therebypreventing 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 becomesauto-propagative leading to the production of non-radical products(Fig. 2). Second is by removing free radical (ROS) initiators in order toquench chain-initiating catalysts (radicals) (Antolovich, Prenzler,Patsalides, Mc Donald, & Robards, 2002) or limiting the radicalsinitiators by binding metals such as iron and copper as metal chelatorsto stabilise them in an inactive or insoluble form (Allen & Cornforth,2010; Dai & Mumper, 2010; Fig. 4a and b). Moreover, the antioxidantfree radical (oxidized antioxidant) formed in reaction b (Fig. 4) mayfurther interfere with chain propagation reactions by forming peroxyantioxidant compounds as shown in reaction c (Antolovich et al.,2002). Themetal chelating power of plant materials has been proposedto be associated with chemical composition of the sample (Goncalves,Battistin, Pauletti, Rota, & Serafini, 2009), including the presence of
Initiation:
RH R•
Propagation:
R• + O2ROO•
ROO• + RH ROOH +R•
Termination:
R• + R• RR
R• + ROO ROOR
ROO• + ROO• ROOR + O2
Non radical products
PH + HO• P• + H2O (a)
P• +O2 POO• (b)
POO• + PH POOH + P• (c)
POO• +H2O PO• + O2 +H2O (d)
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] RO· + P· + H2O
a)
b)
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 ini-tiation stage.
178 A.B. Falowo et al. / Food Research International 64 (2014) 171–181
compounds, such as phytate and oxalates. Mirzaei and Khatami (2013)found that the extract of Coriander sativum possesses higher ironchelating activity than Petroselium crispum, while the addition ofMenthagentilis L. showed higher chelating activity than other menthespecies (Goncalves et al., 2009).
3.7. Edible medicinal plants as natural antioxidant in meat and futureperspectives
The use of natural antioxidant in meat is multifunctional. It plays ananti-oxidative, anti-microbial and preservative role in meat duringprocessing and storage. The addition of natural antioxidants stabilizescholesterol levels, inhibits the formation of cholesterol oxidizedproducts, and reduces the formation and absorption of malondialdehydeand heterocyclic amine (HCA) in cookedmeat (Kobus-Cisowska, Flaczyk,Rudzinska, & Kmiecik, 2014; Megan-Tempest, 2012). The HCAs havebeen noted to be mutagenic by causing changes in DNA which mayincrease the risk of cancer. In some cases, supplementing meat with
medicinal plants rich-antioxidants can act as functional or nutraceuticalfood to promote consumers' health and wellness compared to the useof vitamins and synthetic antioxidants (Fig. 1). Functional foods arefood or food products that provide essential nutrients or biologicallyactive components beyond the basic nutrition necessary for health orwell-being of the consumers (IFT, 2014), and when it aids in prevention,management or treatment of health disorders, are knownas nutraceuticals(El Sohaimy, 2012). According to Lobo, Patil, Phatak, and Chandra (2010),functional food contains ingredients such as dietary fibers, vitamins,minerals, antioxidants, essential fatty acids (omega-3) and lignins whilenutraceutical contains nontoxic food extract supplement. Numerousmedicinal plants, vegetables and spices have been identified to functionin this capacity, and their application in meat can provide functional ornutraceutical meat or meat products. The beneficial effect of producingmeat products containing medicinal plant extracts would be to combatdifferent health related problems that have been associated withconsumption of meat over the years. Duthie et al. (2013) found thatincluding vegetable powder in the formulation of processed turkeymeat patties increase the antioxidant content, and this may contributeto the prevention ofmeat related diseases. It has also been demonstratedthat the consumption of food (meat) rich in natural antioxidant canreinforce the activity of the endogenous antioxidants against degenerativediseases linked to oxidative stress and ROS-related tissue damage(Valenzuela, Sanhueza, & Nieto, 2003). However, information on produc-tion and consumption of functional or nutraceutical meats is still scanty.Further research will be needed to determine the amount of naturalantioxidants that is required to produce functional and nutraceutical meat.
4. Conclusion
The use of bioactive compounds in plant materials as naturalantioxidants has a great antimicrobial potential to preserve meat fromoxidative deterioration. The application of natural antioxidants ispresumed necessary to boost the endogenous antioxidant againstoxidative stress in farm animals and prevent lipid–protein oxidationinmeat andmeat products. However, since the effect of oxidative stressonmeat quality has not been adequately investigated, there is a need toexplore this area to curb the challenges of quality losses due to oxidation.Possibility of getting a viable solution to this challenge still lies in efficientuse of medicinal-plant-rich antioxidants to preserve the functionality ofmeat and ensure production of meat products with nutraceuticalproperties.
Acknowledgements
The authors are grateful to GovanMbeki Research and DevelopmentCentre (GMRDC) of the University of Fort Hare (UFH) for providingfinancial assistance for this work as part of the UFH's support to theDepartment of Science and Technology/National Research Foundation(DST/NRF) South African Research Chairs Initiative (SARChI) Chair inMeat Science: Genomics to Nutriomics which is jointly hosted by theUniversities of Stellenbosch and Fort Hare. We are also grateful to Dr.Oyedemi Sunday for his initial criticism of the article.
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