Accepted Manuscript

Natural antioxidants in processing and storage stability of sheep

and goat meat products

Leda C.M. Cunha, Maria Lúcia G. Monteiro, José M. Lorenzo,

Paulo E.S. Munekata, Voster Muchenje, Francisco Allan L. de
Carvalho, Carlos A. Conte-Junior

PII: S0963-9969(18)30409-5
DOI: doi:10.1016/j.foodres.2018.05.041
Reference: FRIN 7631
To appear in: Food Research International
Received date: 27 February 2018
Revised date: 11 May 2018
Accepted date: 18 May 2018

Please cite this article as: Leda C.M. Cunha, Maria Lúcia G. Monteiro, José M. Lorenzo,
Paulo E.S. Munekata, Voster Muchenje, Francisco Allan L. de Carvalho, Carlos A. Conte-
Junior , Natural antioxidants in processing and storage stability of sheep and goat meat
products. The address for the corresponding author was captured as affiliation for all
authors. Please check if appropriate. Frin(2017), doi:10.1016/j.foodres.2018.05.041

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 ACCEPTED MANUSCRIPT

Natural antioxidants in processing and storage stability of sheep and goat

meat products

Leda C. M. Cunhaª, Maria Lúcia G. Monteiroª,b, José M. Lorenzoc , Paulo E. S.

Munekatad, Voster Muchenjee, Francisco Allan L. de Carvalho d and Carlos A.

Conte-Juniorª,b,f*

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a
Departamento de Tecnologia de Alimentos, Faculdade de Veterinária,

Universidade Federal Fluminense, Niterói, RJ 24230‐340, Brasil

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b
Instituto de Química, Centro de Tecnologia, Universidade Federal do Rio de
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Janeiro, Rio de Janeiro, RJ 21941-909, Brasil
c
Centro Tecnológico de la Carne de Galicia, rúa Galicia n° 4, Parque
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Tecnológico de Galicia, San Cibrao das Viñas, 32900 Ourense, Spain

d
Departamento de Engenharia de Alimentos, Faculdade de Zootecnia e
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Engenharia de Alimentos, Universidade de São Paulo, Pirassununga, São

Paulo, SP 13635-900, Brasil

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e
Department of Livestock and Pasture Science, University of Fort Hare, Private

Bag X 1314, Alice, South Africa

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f
Instituto Nacional de Controle de Qualidade em Saúde, Fundação Oswaldo
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Cruz, Rio de Janeiro, RJ 21040-900, Brasil

* Corresponding author:

Professor Carlos Adam Conte Junior, DVM, MSc, Ph.D.

Current Address: Departamento de Tecnologia de Alimentos, Universidade

Federal Fluminense, Niterói, RJ 24230-340, Brazil.

Phone: +55 21 2629-9545; E‐mail: carlosconte@id.uff.br

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Abstract

Oxidative damage is one of the main reasons for loss of quality in sheep and

goat meat and meat products. Synthetic antioxidants are the current solution to

stabilize oxidative process and extend the shelf life of such products; however,

the negative impact on health may impose a risk to consumers. Natural

antioxidants, extracted from several vegetable sources, have been considered

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an attractive alternative for this conflicting situation. Phenolic compounds are

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minor components in herbs, spices, tea and fruits that display potential

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application against the progression of lipid and protein oxidation and their

consequences for meat quality, which can even overcome the protective effect
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of synthetic compounds. This review aims to discuss the mechanisms

associated to lipid and protein oxidation and their implications on meat quality
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attributes and provides recent data regarding the application of natural

antioxidants in sheep and goat meat products, which have a high susceptibility
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to oxidative processes compared to other red meats.

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Keywords: Antioxidants; Caprine meat; Lipid oxidation; Ovine meat; Phenolic

compounds Protein oxidation

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1. Introduction

One of the main causes of meat deterioration is the oxidative processes

that occur in the conversion of muscle to meat, at meat processing or during

storage. The biochemical changes responsible for the conversion of muscle to

meat interrupts the balance of the in vivo prooxidative and antioxidative system,

predisposing the oxidative reactions in the post-slaughter stage (Kumar et al.,

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2015). This phenomenon leads to undesirable changes, causing discoloration,

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texture changes, development of off-flavor and off-odor, loss of nutritional

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quality, limited shelf life and formation of secondary compounds that can be

prejudicial to human health (Gómez, & Lorenzo, 2012; Falowo, Fayemi, &
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Muchenje, 2014).

The oxidative stability of meat depends on various intrinsic and extrinsic

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factors such as the concentration of pro-oxidants, enzymatic activity, pH, and

temperature as well as the composition of the protein and lipid fraction, which
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vary among different animal species (Ladikos & Lougovois, 1990). Sheep and

goat are classified as red meat due to its high myoglobin concentration, which
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predisposes meat oxidation (Faustman, Sun, Mancini, & Suman, 2010; Suman,

Joseph, Li, Steinke, & Fontaine, 2009; Suman & Joseph, 2013). Moreover,
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sheep and goat meat presents similar fatty acid composition whereas
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approximately half of the fatty acid are unsaturated, the monounsaturated fatty

acid (MUFA) accounts for c.a. 45% and the polyunsaturated fatty acid (PUFA)

accounts for c.a. 10% of total fatty acids (Banskalieva, Sahlu, & Goetsch, 2000;

Hajji et al., 2016). The higher amount of unsaturated fatty acids favors oxidative

processes of meat (Kumar, Yadav, Ahmad, & Narsaiah, 2015).

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In order to prevent or delay meat oxidation reactions, the industry adds

antioxidants in the formulation of meat products. However, the majority of these

ingredients are synthetic mainly butylated hydroxyanisole (BHA), butylated

hydroxytoluene (BHT) and propyl gallate (PG). Nevertheless, some studies

have shown the adverse effects of the synthetic antioxidants for the consumer

health, thereby increasing the demand for natural antioxidants (Falowo et al.,

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2014; Maqsood et al., 2006; Lorenzo, González-Rodríguez, Sánchez, Amado, &

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Franco, 2013a; Munekata et al., 2017a; Şahin et al., 2017, Lorenzo et al.,

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2018a). On the other hand, compounds with antioxidant activity can be naturally

found in plants, oils, fruits, nuts, and several studies have shown the efficacy of
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the substitution of natural antioxidants over the synthetic ones (Lorenzo,

Sineiro, Amado, & Franco, 2014a; Lorenzo, Pateiro, García Fontán, & Carballo,
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2014b; Pateiro, Lorenzo, Amado, & Franco, 2014; Franco et al., 2018).

Nonetheless, the effectiveness of natural antioxidants in meat products

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depends mainly on composition of extract vegetable and their antioxidant

activity, application form, food processing, and meat matrix especially the
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composition of the lipid and protein fraction (Aguiar, Estevinho, & Santos, 2016;

Kukula-Koch et al., 2013; Kumar et al., 2015).

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The aim of this review is to explore the meat quality changes related to
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lipid and protein oxidation as well as the effect of natural antioxidants in replace

to the synthetic ones in sheep and goat meat in terms of oxidative processes,

instrumental parameters and sensorial attributes.

2. Mechanism and analytical methods of meat oxidation

The meat composition has a great influence on its stability during

processing and storage. Lipids of muscle act as structural components of the

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muscle membranes, or as adipose tissue for triacylglycerol storage between

muscle fibers. Differences in the lipid content and the fatty acid composition are

directly related to oxidative stability. A greater amount of lipid and PUFA/SFA

ratio accelerates the lipid oxidation in meat (Kumar et al., 2015). In addition, the

myoglobin and ferrous iron concentration in the protein fraction are factors that

can also influence the meat oxidation rate (Faustman et al., 2010; Ladikos &

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Lougovois, 1990). Red and darker meats have more myoglobin concentration,

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presenting more heme pigments and reactive iron, which are known to catalyze

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the lipid oxidation (Chaijan, 2008; Faustman et al., 2010). Lipid oxidation is a

complex chain reaction process dependent on oxygen that promotes oxidative

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deterioration of fatty acids with the production of free radicals and happens at

three different phases namely initiation, propagation and termination (Figure 1)

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(Falowo et al., 2014; Guéraud et al., 2010). The initiation phase occurs in the

presence of favorable conditions like light or thermal reaction, radiation, the

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presence of pro-oxidants or reactive oxygen species (ROS). In this phase, there

is the abstraction of a hydrogen radical from an unsaturated fatty acid

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generating an alkyl radical (R•) that reacts with oxygen leading to the formation

of peroxide radicals (ROO•). These peroxide radicals react with unsaturated

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fatty acids and produce hydroperoxides (ROOH), which are the primary
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compounds of lipid oxidation and characterize the propagation phase. Although

these primary compounds do not affect the sensory properties of meat

products, they are unstable and susceptible to more free radical chain reactions

and, therefore, are formed the secondary compounds from lipid oxidation such

as aldehydes, ketones, alkanes, and so on. These secondary compounds are

stable products formed in the termination phase and are responsible for the
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sensorial changes of meat like off-flavor and rancid odor (Guéraud et al., 2010;

Kumar et al., 2015).

There are diverse methods of assessment of lipid oxidation in meat, which

are frequently reviewed and modified (Méndez-Cid, Lorenzo, Martínez, &

Carballo, 2017). Some studies correlates the extent of lipid oxidation measuring

the oxidation substrates, such as PUFA by gas chromatography (GC),

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accordingly the diminution of PUFA and increase of SFA proportion suggests a

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loss of fatty acids due to oxidation. Nevertheless, the most used methods

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evaluate the primary and/or secondary lipid oxidation products. For the primary

compounds, there are methods that evaluate the formation of conjugated

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dienes and hydroperoxides by spectrophotometry, peroxide levels through

titrimetric method and electron spin resonance (ESR) spectroscopy, which

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measures the free radical formation from the absorption of electromagnetic

energy by a paramagnetic center with unpaired electrons (free radicals) (Eaton

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& Eaton, 2002; Guyon et al., 2016). There is a new trend to measure

hydroperoxides through chromatographic methods since they are more

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accurate and specific (Barriuso, Astiasarán, & Ansorena, 2013; Guyon et al.,

2016). Fourier Transformed Infrared Spectroscopy (FTIR) is another technique

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to measure meat oxidation, which identify functional groups of molecules

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through vibrations properties of chemical bonds such peroxides and fatty acid

composition (Xiuzhu, Van de Voort, & Sedman, 2007; Maggio et al., 2009;

Lucarini, Durazzo, Sánchez del Pulgar, Gabrielli, & Lombardi-Boccia, 2017).

The formation of secondary oxidation products are the most widely used

assessment for lipid oxidation, especially the thiobarbituric acid (TBA) reactive

substances (TBARS) method that measures the colorimetric reaction of the

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secondary compounds with the TBA by spectrophotometry, and results are

expressed as malondialdehyde (MDA) concentration, since this compound is

one of the most abundant aldehydes generated in the final stage of the lipid

oxidation. This method has few limitations as poor molecular specificity and

quantification sensitivity, hence it can measure other oxidized molecules and

not exclusively MDA, leading to an overestimation of lipid oxidation values, and,

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therefore some chromatographic techniques for MDA quantification have been

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developed, which present more accuracy, sensitivity and specificity (Barriuso et

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al., 2013). Another important secondary oxidation products are the volatile

compounds responsible for the off-odor and off-flavor such as propanal,

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hexanal and pentanal, which can be measured through gas chromatography

and mass spectrometry (Barriuso et al., 2013; Lorenzo, Bedia, & Bañon, 2013b;
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Guyon et al., 2016).

Likewise, the protein oxidation occurs due to covalent modifications of

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proteins, whereas the main targets are the functional groups on the side chains

of the amino acids, and these reactions are induced directly by ROS or
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indirectly by secondary products of oxidative stress such as oxidizing lipids,

myoglobin or metal catalysts (Soladoye, Juárez, Aalhus, Shand, & Estévez,

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2015; Stadtman & Levine, 2003). The oxidative damage of the amino acids can
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produce modifications of the side chains, conversion of different amino acids,

fragmentation of the peptide backbone and formation of inter and intra-

molecular cross-links (Estévez, 2011). The mechanism of protein oxidation

(Figure 2) is similar to lipid, occurring via free radical chain reaction, initiating

when ROS remove a hydrogen atom from the protein, resulting in a protein

carbon-centered radical (P•). In the presence of oxygen, the P• is converted to

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peroxyl radical (POO•) and by abstraction of a hydrogen atom from another

molecule, it is converted to alkyl peroxide (POOH). Further reactions with the

reduced form of iron (Fe2+) or free peroxyl radical (HO2•) could lead to the

formation of alkoxyl radical. In the absence of O2 two protein carbon-centered

radicals (P•) reacts with each other to produce carbon-carbon cross-linked

derivatives (Stadtman & Levine, 2003).

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Some amino acids are more susceptible to ROS, and among them, the

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side chains of arginine, lysine and proline are oxidized by metal-catalyzed

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reactions and form carbonyl residues, while others amino acids like cysteine or

methionine are more related to cross-linking or yield sulfur-containing

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derivatives (Lund et al., 2011). The major changes caused by protein oxidation

in meat are the formation of protein carbonyls, loss of sulfhydryl groups and
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formation of protein cross-linking (Lund et al., 2011), which result in color and

texture changes, loss of nutritional quality including essential amino acids and
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protein digestibility, and loss of protein functionality.

Regarding methods of protein oxidation assessment, the initial and most

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used method to quantify protein oxidation is the quantification of protein

carbonyls using the 2,4 dinitrophenylhydrazine (DNPH) method (Estévez,

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2011). But later another advanced methodology was developed with the
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detection of carbonyl using Western blots and immunoblotting aiming the

individual identification of oxidized proteins, which helped to better understand

the occurrence of the protein oxidation (Grossi, Bolumar, Søltoft-Jensen, &

Orlien, 2014; Guyon et al., 2016). Other novel methodologies to detect oxidized

proteins use electron spin resonance (ESR) spectroscopy, fluorescence

spectroscopy and high-performance liquid chromatography (Estévez, 2011;

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Guyon et al., 2016; Lund et al., 2011). However, according to Estévez (2011),

only the measure of the carbonyl group does not represent all the oxidative

damage of proteins and, thus the free thiol analyses started to be used as well.

The free thiols are correlated with the carbonyl compounds and are evaluated

by the reaction of the thiol group with 5,5’-dithiobis (2-nitrobenzoic acid) (DTNB)

(Guyon et al., 2016). The measurement of the protein radical intensity by ESR

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spectroscopy represent other methodology for protein oxidation assessment

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(Guyon et al., 2016; Jongberg, Tørngren, & Skibsted, 2018).

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Lipid and protein oxidation begin with similar paths whereas free radicals

or ROS attacks the target molecule, starting the radical chain reaction. In behalf
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of this similarity, several authors have suggested an interaction between these

oxidative processes (Faustman et al., 2010; Estévez, 2011; Falowo et al., 2014;
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Guyon et al., 2016). Aldehydes, one of the main secondary compounds of lipid

oxidation, can act as pro-oxidant agent and react with proteins leading to
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changes in their physical properties (Guyon et al., 2016). Furthermore, peroxyl

radicals from lipid oxidation are absorbed by the hydrogen atoms of proteins
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forming radicals that are further converted into alkylperoxides, which increases

the formation of alkoxyl radicals and hydroxyl derivatives (Falowo et al., 2014;
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Guyon et al., 2016). The conversion of myoglobin into metmyoglobin due to

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protein oxidation releases iron, which acts as catalysts of the lipid oxidation and,

therefore greater concentrations of iron and myoglobin are often linked to

greater rates of lipid oxidation. In addition, metmyoglobin formation generates

intermediate products such as superoxide anion and hydrogen peroxide, which

increases the rate of oxidation of unsaturated fatty acids (Faustman et al.,

2010).
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According to Estévez (2011), the reciprocal transfer of ROS and non-

reactive species (for example hydrogen peroxide and hydroperoxides) between

lipids and proteins explain the positive correlation of both oxidative processes.

Faustman et al. (2010) studied the interactions between lipid and myoglobin

oxidation and confirmed concomitant oxidation of these compounds during the

same period, which leads to an accelerated oxidative degradation and

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exacerbated loss of sensory quality such as discoloration and off-flavor

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development. However, these authors evidenced that addition of antioxidants

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used to inhibit lipid oxidation usually also exhibits effects against myoglobin

oxidation.
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3. Use of antioxidants in meat

The use of antioxidants is a primary action taken by the meat industry to

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increase the shelf life of their products (Lorenzo et al., 2018b). These

compounds exert a specific role by, for example, break the oxidative chain
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reaction, chelating transition metals and scavenging free radicals and reactive

species (Figure 3) (Augustyniak et al., 2010). However, the uncertain impact of

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synthetic sources of antioxidant in health has been considered as a relevant

downside for consumers due to potential health risk. In this conflicting scenario
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of large scale use in meat products and health concern, synthetic antioxidants
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are suggested to be replaced by natural compounds from vegetables in the

meat industry (Kumar et al., 2015; Carocho & Ferreira, 2013; Fernandes et al.,

2016a).

3.1. Synthetic antioxidants

The most common food antioxidant additives are butylated

hydroxyanisole, butylated hydroxytoluene, propyl gallate, and tert-

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butylhydroquinone (BHA, BHT, PG, and TBHQ, respectively) that are applied up

to 200 ppm in lipid base (USFDA, 2018). Although these compounds show

great efficiency even at lower concentrations, consumers and food industry

have been considering the relation between food composition and health, which

have been increasing the demand and interest for natural ingredients (Shahidi &

Ambigaipalan, 2015; Carocho & Ferreira, 2013; Fernandes, Trindade, Lorenzo

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& Melo, 2018; Munekata et al., 2017b).

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The European Food Safe Authority (EFSA) recognizes the potential

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harmful effects of synthetic antioxidants for public health and warns about their

consumption. The acceptable dose intake (ADI) indicated by EFSA for synthetic
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antioxidants are low and indicates the importance to reduce the ingestion of

such compounds. The ADI values for synthetic antioxidants are 1.0 mg/kg
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bw/day for BHA (EFSA, 2011), 0.25 mg/kg bw/day for BHT (EFSA, 2012), 0.5

mg/kg bw/day for propyl gallate (EFSA, 2014), and 0.7 mg/kg bw/day for TBHQ
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(EFSA, 2004). The opinion and ADI indication presented in EFSA documents is

based scientific studies from both in vitro and in vivo experiments (in rats,
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rabbits, dogs) that indicate a potential health risk to humans, particularly related

to the gastrointestinal tract.

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In the same line, United States Food & Drug Administration (FDA) has
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established limits for addition of antioxidants in food. This agency set the

general limit for BHA, BHT, TBHQ, propyl gallate addition in food at 0.02%

(alone or combined) of fat or oil, which also includes essential oils. It is worth

noting that some food has specific limits such as 0.005% for BHA in dry

breakfast cereals and 0.001% in potato granules (USFDA, 2018). The Food

Safety and Standard Authority of India (FSSAI) regulate the use of BHA, propyl
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gallate, and TBHQ in a similar way as FDA in USA: maximum limit of 0.02% in

fat base alone or in combination (FSSAI, 2011). Canada is another country that

has set the limit of 0.02% for synthetic antioxidants in food (CFIA, 2018). In

addition, other countries have declared that synthetic antioxidants are approved

to use in food formulations such as in Japan (MHLW, 2016), Australia and New

Zealand (2016).

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3.2. Natural antioxidants

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The search for natural antioxidants became a subject of major research

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leading to the production of studies that report, in general lines, the content of

main antioxidants and their antioxidant activity (evaluated by at least three

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distinct methods) (Brewer, 2011; Kumar et al., 2015). Several natural sources

have been studied in the last decades due to the high content of antioxidants
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from fruits, tea, herbs, nuts, spices, vegetables, algae, and even agroindustry

by-products have been assessed (Agregán et al., 2017). The main groups of
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natural phytochemicals capable of exert antioxidant activity are phenolic

compounds, carotenoids, and essential oils (Munekata, Franco, Trindade, &

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Lorenzo, 2016a). Phenolic compounds are a diverse group of secondary

metabolites widely distributed in the food of vegetable origin. The antioxidant

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activity of these compounds is determined by numbers and positions of the

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hydroxyl group in association with the carboxyl functional (Rice-Evans, 1996).

Flavonoid is the main class of phenolic compounds due to the diversity of

structures and sources among vegetables (Brewer, 2011). On the other hand,

non-flavonoid phenolics include several classes as phenolic acids, coumarins,

stilbenes, lignans, tannins and phloroglucinols (Shahidi & Ambigaipalan, 2015).

Carotenoids group is another class of natural antioxidants of great relevance for

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food processing. Carotenoids is a colorant widely used in foods, however, their

antioxidant activity has been studied and related to functional groups and

number of double bonds, which affect the carotenoid-radical interactions

(Chávez-Crooker, Obreque, Vera, Moya, & 2011). The main sources of

carotenoids are carrots, spinach, red pepper, tomato, parsley, and red

watermelon (Maiani et al., 2009). One more group of natural antioxidants is

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essential oils. This group constitutes a small fraction of plants composition and

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are normally obtained without heating by hydrodistillation, steam distillation or

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dry distillation (Brewer, 2011). Essential oils were already extracted from

turmeric (Curcuma longaI), (Rosmarinus officinalis) , ginger (Zingiber officinale)

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and thyme (Thymus vulgaris) , wherein the main compounds identified are

alcohols, aldehydes, phenylpropanoids, terpenes or ketones, which have a well-

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known antioxidant activity through scavenge free radicals or free iron chelation

from hemoproteins (Shahidi, Arachchi, & Jeon, 1999; Peng et al., 2008;
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Sacchetti et al., 2005). For the purpose of this review, only these groups of

natural antioxidants are considered.

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4. Effect of natural antioxidants on lipid and protein oxidation

Although several sources and compounds that display antioxidant activity,

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phenolic compounds are the main studied group in sheep and goat meat and
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meat products (Table 1).

In fresh meat the protective activity of tomato pomace extracts (ethanol

and ethyl acetate) were applied to the surface of lamb (Longissimus thoracis)

steaks packaged under modified atmosphere (51% O2 and 18% CO2). Although

a correlation between lipid and protein oxidation results during storage was

observed, no significant effect was attributed to antioxidant extracts in lipid and

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protein oxidation assays. Authors argued that tomato pomace are relevant

sources of natural antioxidants, particularly lycopene, phenolics compounds and

β-carotene, which could be applied in higher concentrations for future studies

(Andres, Petron, Delgado‐Adamez, Lopez & Timon, 2017a).

Differently, reduction of size can influence the effectiveness of antioxidant

extracts in oxidative meat stability. This effect was observed in an experiment

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with lamb leg chop (20 mm thickness) sprayed with borage (0.5, 5, and 10

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g/100 g; rich in rosmarinic, syringic and synapic acids) and green tea (0.005,

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0.05, 0.5 and 5 g/100 g; rich in catechin, myricetin, quercetin and kaempferol)

aqueous extracts. Lipid oxidation was remarkably reduced by addition of both

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borage (5 and 10 g/100 g) and green tea (0.5 and 5 g/100 g) extracts after 13

days of storage (Bellés, Alonso, Roncalés & Beltrán, 2017).

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In ground sheep meat, the effect of sumac (Rhus coriaria L.) and barberry

(Berberis vulgaris L.) lyophilized water extracts (3 g/100 g) was studied during 9
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days of refrigerated storage. Lipid oxidation, assessed by TBARS value, was

reduced by 78% and 62% in Sumac and Barberry treatments, respectively

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(Aliakbarlu & Mohammadii, 2015). A number of Chinese medicinal herbs can be

exploited as potential sources of natural antioxidants. A study evaluated the

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antioxidant effect of 10 commonly consumed herbs in China in ground sheep

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meat under refrigerated storage for 11 days. Among all herbs extracts, yinchen

(Artemisia capillaris) at 0.25 g/100 g displayed the highest capacity to prevent

lipid oxidation, followed by dangshen (Codonopsis pilosula) and balloon flower

(Platycodon grandiflorum) at 0.10 g/100 g) in comparison to control treatment.

The evolution of peroxide value during storage was 0.99 mEq/kg in both

yinchen (Artemisia capillaris) and dangshen (Codonopsis pilosula) extracts,

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wherein control treatment displayed peroxide value of 3.2 mEq/kg (Luo et al.,

2007). On the topic of essential oils, the use of Avishane shirazi (Zataria

multiflora) and clove (Syzygium aromaticum) essential oils both at 0.25 g/100 g

impaired the evolution of lipid oxidation in ground sheep meat wherein oxidation

index was lower than 0.5 mg MDA/kg after 9 days (Aliakbarlu & Sadaghiani,

2015).

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Regarding studies that evaluated addition of natural antioxidants in

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processed meat, Andrés, Petrón, Adámez, López & Timón (2017b) observed

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that extracts obtained from agro-industries by-products (olive, pomegranate, red

grape, and tomato; 1000 mg/kg) could influence the characteristics of lamb
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patties, depending on its phenolic content. Authors observed that olive pomace

and red grape by-product extracts prevented both lipid and protein oxidation
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along with the loss of redness after 7 days of refrigerated storage. On the other

hand, pomegranate and tomato by-product extracts did not induce significant
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changes in comparison to control treatment. In another experiment with lamb

patties, the antioxidant activity of rosemary and ginger extracts were evaluated
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during frozen storage for up to 150 days. Both extracts at 0.05 g/100 g reduced

lipid oxidation from 3.8 mg MDA/kg (control) to 1.6 and 1.3 mg MDA/kg
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(rosemary and ginger treatments, respectively) at the end of storage.

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Interestingly, in patties prepared with ginger extract and sodium lactate, lipid

oxidation was even more suppressed as observed for this extract alone which

yielded the lowest lipid oxidation value (1.2 mg MDA/kg) among all treatments

(Baker, Alkass & Saleh, 2013). Villalobos-Delgado et al. (2015) evaluated the

oxidative stability of lamb patties stored at different conditions (cooked and

stored under refrigeration for 3 days; raw and stored under refrigeration for 7
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days or raw and frozen stored) and the addition of hop in two different forms

(infusion and powder at 2 g/kg). In their experiment, they found that both of hop

applications exhibited a significant antioxidant effect during refrigeration and

frozen storage, whereas the powder form exerted a stronger lipid oxidation

inhibition measured as TBARS values, but with lower consumer acceptance

than hop infusion and control patties. Samples cooked and treated by hop also

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presented lower protein oxidation assessed by carbonyls quantification.

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In sheep burgers packaged under modified atmosphere (80% O2 and 20%

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CO2) and stored for 20 days at 2 °C, addition of oregano extract (1000 mg/kg)

inhibited the lipid oxidation by 40-50% and protein oxidation by 20-30%

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assessed by means of TBARS and protein carbonyls values, respectively

(Fernandes, Trindade, Lorenzo, Munekata & Melo, 2016b). Moreover, in this

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experiment authors observed similar effect to burgers elaborated with BHT (50

mg/kg) in both lipid and protein oxidation assays, which also indicated oregano
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extract as a viable natural alternative. In a study with lamb burgers frozen for

120 days, Fernandes et al. (2017) evaluated the effect of addition of oregano
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extract on the oxidative stability. According to the authors, the highest values for

lipid and protein oxidation indexes, at the end of the storage time, were
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obtained for control treatment whereas the evolution of such indexes was
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controlled due to oregano extract in all tested concentrations (13, 18 and 24 mL

extract/kg of meat product). The mixture of ground spices (rosemary and thyme)

in the formulation of lamb burger can also prevent lipid oxidation, whereas this

protective effect was observed for two burger formulations. Rosemary and

thyme reduced lipid oxidation index by 6 times during 6 days of refrigerated

storage in comparison to control burgers in both burger formulations measured

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by TBARS values. Moreover, authors stated that no significant differences were

observed between antioxidant treatments (Cózar, Linares, Garrido & Vergara,

2013).

Natural antioxidants of fruits can also contribute to the oxidative stability of

sheep nuggets. Das et al. (2016) studied the effect of Litchi pericarp powder

extract during storage of cooked sheep nuggets for 12 days. Although lipid

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oxidation index assessed by TBARS values increased for all treatments, the

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addition of 1.0 and 1.5 g/100 g of litchi powder extract decreased lipid oxidation

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throughout storage time in comparison to control treatment. Authors also

observed that 1.5 g/100 g litchi powder extract and 100 ppm BHT treatment
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displayed similar lipid oxidation index during storage. In a similar study, Verma,

Rajkumar, Banerjee, Biswas & Das (2013) added guava powder extract to
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sheep nuggets and observed a protective effect during 15 days of refrigerated

storage. Guava powder at both tested concentration increased the antioxidant

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status of sheep nuggets, in a concentration-dependent manner, and inhibited by

40% in comparison to control treatment.

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The antioxidant activity of natural extracts has also been studied in the

production of fermented sausages. Bozkurt (2006) studied the effects of green

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tea (300 mg/kg) and shrub (T. spicata) oil (300 mg/kg), along with the
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combination of both extracts (150 mg/kg from each) on the characteristics of

Sucuk sausage (traditional fermented Turkish sausage) during its ripening. The

author observed similar behavior for lipid oxidation during ripening: increasing

from day 0 to 8 followed by a decrease until the end of ripening for all treatment.

However, the addition of natural antioxidants reduced lipid oxidation for most of

the ripening period. Authors also stated that natural antioxidants displayed
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higher capacity to prevent lipid oxidation than BHT (300 mg/kg). Bozkurt (2006)

observed that green tea and shrub (T. spicata) oil extracts either alone or

combined did not induce significant changes in instrumental color (L*, a*, and

b*) of Sucuk (traditional Turkish sausage with lamb and bovine meats). On the

other hand, overall acceptance of Sucuk sausages produced with either natural

or synthetic (BHT) antioxidants received higher scores of sensory attributes

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(flavor, color and ease of cutting) than control treatment. Interestingly, authors

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also observed that sensory scores were positively correlated with L* and b*

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values during ripening. In fermented goat sausage treated by rosemary extract

in powder form, Nassu, Gonçalves, Silva & Beserra (2003) observed that
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evolution of lipid oxidation was partially inhibited for up to 60 days of storage by

addition of 0.050 g/100 g rosemary extract in powder form. Differently, authors

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indicated that sausages elaborated with 0.025 g/100 g rosemary extract in

powder form had similar oxidation level after 30 days of storage. Using a
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different approach, Malekian, Khachaturyan, Gebrelul & Henson (2014)

evaluated the impact of rice bran on the antioxidant status of goat meat
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sausage. In this study, rice bran increased the antioxidant status in a

concentration-dependent manner from 13.5 (control sausage) to 14.3 and 22.7

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𝜇moles of Trolox equivalent/100 g (addition of 1.5 and 3 g/100 g of rice bran,

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respectively). This increase in antioxidant status was attributed to α-tocopherol

(7.37 mg/100 g) in rice bran.

Although the studies with the application of natural antioxidants in sheep

and goat meat are in less quantity than the other type of matrix, they show that

substitution of synthetic antioxidants for natural sources presents great results

in inhibiting and controlling the oxidative processes.

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5. Effect of natural antioxidants on sensorial attributes and instrumental

color parameters

Addition of natural antioxidants can protect meat and meat products

against oxidative damages and changes on sensory properties (Table 2) and

instrumental color parameters (Table 3).

Regarding fresh meat, lamb steaks packaged in oregano film and with

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rosemary extract treatments preserved instrumental red color after 13 days of

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storage. However, in comparison with rosemary extract directly sprayed in meat

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surface, the same extracted within the film package showed less protection

against discoloration. Sensory analysis indicated that after 13 days the lamb
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steaks added of natural antioxidants displayed a slight reduction of red color,

superficial discoloration and had lower level of off odor. Authors also argued
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that such results were in accordance with the results obtained from instrumental

color and lipid oxidation values, which strengthen the potential commercial use
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of oregano extract and rosemary film. In addition, the authors stated that

oregano film was suggested to be applied as a tool to increase the shelf life of
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fresh meat in the retail sale (Camo, Beltrán, & Roncalés, 2008). In lamb leg

chops, the instrumental color was influenced by borage and green tea extracts.
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In this study, reduction in the increase of L* and preservation of a* values during

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13 days of refrigerated storage was attributed to borage (10 g/100 g) and green

tea (0.5 and 5 g/100 g) treatments, while L* value for control treatment

increased and a* decreased until the end of storage. The antioxidant effect of

both extracts was also influenced the sensory properties of storage meat

products. Both oxidation odor and flavor were reduced in 5 g/100 g of green tea

and 10 g/100 g of borage treated lamb leg chops. The authors also explored the
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perception of herb flavor on lamb leg chops elaborated with tea and borage

extract. According to this study, none of the panelists perceived the

characteristic flavor of herbs in lamb leg chops neither right after its preparation

nor during the storage time. These results strengthen the potential use of such

natural extracts as alternative food antioxidants for the meat industry, according

to authors (Bellés et al., 2017).

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In ground sheep meat, the sensory analysis revealed that reduction in

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color acceptability was prevented by clove essential oil, while odor acceptability

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was preserved by Avishane shirazi essential oil after 9 days. Overall

acceptability was also influenced by essential oils. The highest scores were
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attributed to clove essential oil after 9 days, whereas control and Avishane

shirazi essential oil treatments received lower scores. According to authors, loss
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of color characteristics in meat can be attributed to metmyoglobin formation

(oxidation of myoglobin) which in turn is influenced by the oxidative stability of

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whole meat (Aliakbarlu & Sadaghiani, 2015). The addition of sumac and

barberry in ground sheep meat also inhibited the reduction of color, odor and
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overall acceptability after 9 days in comparison to scores attributed to control

treatments. According to authors, such extracts can contribute to the

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preservation and also improve the shelf life of sheep ground meat (Aliakbarlu &
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Mohammadii, 2015).

Texture analysis of lamb patties elaborated with natural extracts (olive,

pomegranate, grape and tomato by-product) induced slight, but significant,

increase on hardness, gumminess, and chewiness after 7 days of refrigerated

storage. In addition, L* values of lamb patties during storage was not influenced

by natural extracts (Andrés et al., 2017b). Moreover, natural extracts can also
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increase the sensory attributes of lamb patties. This outcome was observed by

Baker et al (2013) who obtained higher scores for color, flavor, tenderness,

juiciness, and overall acceptance of lamb patties added of either rosemary or

ginger extract than those of control after 150 days of frozen storage.

Interestingly, this positive effect was improved by adding of sodium lactate to

antioxidant treatments. Authors also argued that sodium lactate is involved in

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the enhanced water holding capacity, which increases tenderness and overall

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perception of quality.

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The addition of hop at powder and infusion forms (2 g/kg) improved the

color stability of raw lamb patties stored under refrigeration, displaying higher
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redness and lower discoloration than control patties. This improvement on color

stability was also observed on raw lamb patties frozen stored. Sensory
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evaluation also revealed that the flavor of hop was perceived only on patties

elaborated with its powder form. Patties added of hop infusion received the
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same score for hop flavor as that attributed to control patties. This effect on

flavor of lamb patties also influenced the flavor acceptance, leading to lower
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scores for hop powder treatment, whereas control and hop infusion patties

received higher scores. The authors also argued that such differences could be
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explained by the intrinsic sensory properties of hop that has intense smell and
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bitter taste caused by essential oil and resins (Villalobos-Delgado et al., 2015).

The physicochemical evaluation of sheep burgers elaborated with oregano

extracted (1000 mg/kg) was not associated with changes in L* value, while a*

value reduction during storage was partially prevented. In the sensory analysis,

authors observed loss of red color, surface discoloration, and off-odor formation

for all treatments although lower scores were attributed to oregano extract
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burgers after 20 days of storage (Fernandes et al., 2016b). In lamb burgers

studied by Cózar et al. (2013), rosemary and thyme extracts did not influence

characteristics of burgers (L*, a* and shear force) during 6 days of refrigerated

storage. In addition, characteristics related to cooking (cooking yield, cooking

loss, and diameter reduction) were found similar between all treatments. In

another study with lamb burgers, oregano extract at three different

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concentrations did not influence L* value and partially prevented loss of a* value

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during 120 days of frozen storage. Sensory analysis of flavor, texture, and

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overall acceptability was significantly higher in oregano treatments, while

acceptability of aroma and juiciness received similar scores after 120 days
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according to authors (Fernandes et al., 2017).

Regarding natural antioxidant enhancement in nuggets products, the

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addition of litchi powder extract had no significant effect on sensory attributes

and cooking yield of sheep nuggets (Das et al., 2016). Similarly, Verma et al.
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(2013) indicated that guava powder did not influence the sensory attributes:

appearance, flavor, texture, juiciness, and overall acceptability. As for

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instrumental color, the authors argued that addition of guava powder increased

a*, while L* remained similar among sheep nuggets treatments. Regarding

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texture analysis, no remarkable changes were observed due to the addition of

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guava powder except by shear force that was lower in 3 g/100 g guava powder

nuggets in comparison to other treatments.

Fermented sausages elaborated from goat meat have also been

considered as potential meat products in studies of natural antioxidants. Nassu

et al. (2003) observed that formulation of fermented goat sausage with

rosemary powder at 0.05 g/100 g received the highest amount of high scores
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for overall acceptance in sensory analysis. In addition, sensory evaluation of red

color and oxidized aroma indicated that 0.050 g/100 g rosemary powder

treatment reduced the loss of redness and prevented off-flavor formation. Such

results indicated the elevated acceptability of panelists for this treatment in

comparison to control and 0.025 g/100 g rosemary powder sausages.

Interestingly, dry sausages elaborated with rosemary powder received with

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contrasting comments regarding its flavor such as “too much spice” and “tangy”.

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6. Recent approaches for the application of natural antioxidants

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Due to the instability of the phenolic compounds to light, oxygen, pH and

temperature, recent studies have investigated the use of natural antioxidants

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under novel application forms such as edible coating or active packaging.

Moreover, studies have evaluated the efficacy of natural antioxidants against

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oxidative changes promoted by preservation technologies that potentialize meat

oxidation such as irradiation (gamma, electron beam, UV-C light) and high-
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pressure processing (HPP). Although the successful application of natural

antioxidants in sheep and goat meat, there is limited information about it

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considering these novel technology approaches (Table 4). Therefore, further

studies are needed to better understand the effect the natural antioxidants
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under different conditions.

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Rosemary extract (sprayed over steak surface) and oregano and rosemary

films were able of preventing the lipid oxidation in fresh lamb steaks stored for

13 days under retail conditions (24 h under uninterrupted illumination at 1 °C).

Both, oregano film and rosemary extract maintained level of lipid oxidation

bellow the acceptable limit (< 2 mg MDA/kg) at the end of storage. Rosemary

film treatment showed partial inhibition of lipid oxidation, reaching the

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concentration of 2 mg MDA/kg at day 9 of storage, while fresh lamb steaks

without antioxidant enhancement exceed the acceptable limit for MDA on 6 day

of storage (Camo et al., 2008).

Kanatt, Chander, Radhakrishna & Sharma (2005) investigated the addition

of irradiated potato peel extract (rich in chlorogenic acid) in irradiated ground

lamb leg and rib meat. These authors observed that potato peel extract at 0.04

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g/100 g reduced initial lipid oxidation even after irradiation treatment (5 kGy) by

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12% on both ground meats on day 0. After 7 days of storage, lipid oxidation of

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potato peel extract treatment was reduced by 54% and 74% for leg and rib

meat, respectively, in comparison to non-irradiated meats. Carbonyl formation

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followed a similar trend wherein protein oxidation was reduced by around 30%

after 7 days of refrigerated storage in both leg and rib meat. In addition, this
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extract from potato peel exhibited similar protective effect against lipid and

protein oxidation compared to BHT also at 0.04 g/100 g.

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In another study about the antioxidant effect of natural extracts on

irradiated meat, Kanatt, Chander & Sharma (2007) observed that pre-treatment
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of ground lamb leg meat before irradiation (2.5 kGy) impaired the lipid oxidation.

These authors found that mint extract at 0.05 g/100 g partially inhibited the lipid
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oxidation (around 0.6 mg MDA/kg), while mint extract at 0.1 g/100 g reduced in
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50% the formation of TBARS (around 0.4 mg MDA/kg) in comparison to control

samples (0 kGy; >0.8 mg MDA/kg) after 4 weeks of refrigerated storage.

7. Conclusion

The use of natural antioxidants can improve the shelf life of sheep and

goat cuts, ground meat and muscle products. Spraying antioxidant extracts over

cuts and steaks are less effective in preventing lipid and protein oxidation than
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mixing such extracts with meat in small pieces or ground. In meat products,

grinding and homogenization of meat with food ingredients and natural

antioxidants enhance the contact between susceptible compounds and

antioxidants. In such condition, numerous studies support the use of phenolic

compounds, under specific concentrations, as natural alternatives to synthetic

antioxidants. Further studies are need to find the optimal conditions (type and

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concentration of natural antioxidants, extraction method, and application form)

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to use in sheep and goat meat without interfering on sensorial parameters,

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mainly when modern technologies are used in these matrices. There are few

studies that evaluate the different application form and modern technologies
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used for meat processing, which should be further explored for better

comprehension of the antioxidant mechanisms and the development of

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products with greater quality.

Acknowledgements
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José Manuel Lorenzo and Paulo Munekata are members of the

MARCARNE network, funded by CYTED (ref. 116RT0503). The authors also

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thanks the Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro

(grant number E-26/201.185/2014, FAPERJ, Brazil) and the Conselho Nacional

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de Desenvolvimento Científico e Tecnológico (grant number 311361/2013-7,

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CNPq, Brazil), and Coordenação de Aperfeiçoamento de Pessoal de Nível

Superior (grant number 125, CAPES/Embrapa 2014, CAPES, Brazil) for the

financial support.
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Table 1 – Effect of natural antioxidants on lipid and protein oxidative stability of

sheep/goat meat and meat products
Meat/meat Source of TPC Lipid Protein References
product antioxidants oxidation* oxidation*
(concentration)
Fresh lamb Tomato pomace 0.99- No effect No effect Andres et al.
steaks 1.10 (2017a)
mg
GAE/g
extract
Lamb leg Green tea 0.15- Inhibition in NA Bellés et al.

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chops (0.005, 0.05, 0.5, 20.0 0.5 and 5 (2017)
and 5 g/100 g) mg g/100 g
GAE/ml

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extract
Lamb leg Borage seed 0.3-3.3 Inhibition in 5 NA Bellés et al.

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chops (0.5, 5, and 10 mg and 10 g/100 (2017)
g/100 g) GAE/ml g
extract
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Ground Sumac and NA Reduced by NA Aliakbarlu &
sheep meat Barberry water 78% (Sumac) Mohammadii
extracts (3 g/100 and 62% (2015)
g) (Barberry)
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Ground Red grape by- 32.2 Inhibition Inhibition Aliakbarlu &

sheep meat product (1000 mg Mohammadii
mg/kg) GAE/g (2015)
extract
Ground Tomato by- 85.4 No effect No effect Aliakbarlu &
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sheep meat product (1000 mg Mohammadii

mg/kg) GAE/g (2015)
extract
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Ground Chinese NA Reduced by NA Luo et al.

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sheep meat medicinal herbs up to 67% (2007)

(0.10 or 0.25 (0.25 g/100 g
g/100 g) Artemisia
capillaris)
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Ground Avishane shirazi NA <0.5 mg NA Aliakbarlu &

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sheep meat and clove MDA/kg after Sadaghiani

essential oils 9 days (2015)
(0.25 g/100 g)
Sheep Peanut skin 32 mg Reduced by Reduced Munekata et
patties extract (1000 GAE/g almost 50% by 10% al. (2016b)
mg/kg)
Lamb Hop infusion (2 NA Inhibition Inhibition Villalobos-
patties g/kg) Delgado et
(cooked al. (2015)
and
refrigerated-
stored)
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Lamb Hop infusion (2 NA Inhibition for Villalobos-

patties g/kg) or hop both Delgado et
(cooked powder (2 g/kg) applications, al. (2015)
and which was
refrigerated- stronger for
stored) hop powder
Lamb Hop infusion (2 NA Inhibition for NA Villalobos-
patties (raw g/kg) or hop both Delgado et
and powder (2 g/kg) applications, al. (2015)
refrigerated- which was
stored) stronger for
hop powder

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Lamb Hop infusion (2 NA Inhibition No effect Villalobos-
patties (raw, g/kg) or hop Delgado et

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frozen- powder (2 g/kg) al. (2015)
stored and
thawed)

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Lamb Ginger and NA Reduced by NA Alkass et al.
patties rosemary extract 66% (ginger) (2013)
(0.05 and 0.5 and 59%
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g/100 g) (rosemary)
Lamb Resveratrol, NA Inhibition for NA Nieto et al.
patties citroflavan-3-ol all (2010)
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(50, 100, 200, concentrations

300, and 400
mg/kg)
Lamb Olive leaf and NA Pro-oxidant NA Nieto et al.
patties Echinacea effect (2010)
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(Echinacea
purpurea) extract
(50, 100, 200,
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300, and 400

mg/kg)
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Lamb Oregano extract 9.1- Reduced by Partial Fernandes

burger (13, 18, and 24 472.3 67% (18 reduction et al. (2017)
mL extract/kg) mg mL/kg) and
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GAE/g 81% (24

dw mL/kg)
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Lamb Rosemary and NA Reduced by 6 NA Cózar et al.

burger thyme (0.1 g/100 times (2013)
g)
Sheep Oregano extract 52.1 Reduced by Reduced Fernandes
burger (1000 mg/kg) mg 40-50% by 20-30% et al.
GAE/g (2016b)
dw
Sheep Litchi powder 18.4 Inhibition (1.0 NA Das et al.
nuggets extract (1.0 and mg and 1.5 g/100 (2016)
1.5 g/100 g) GAE/g g)
dw
Sheep Guava powder 44.0 Reduced by NA Verma et al.
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nuggets (0.5 and 1 g/100 mg 40% (0.5 and (2013)

g) GAE/g 1 g/100 g)
Sucuk Green tea (300 NA Inhibition NA Bozkurt
sausage mg/kg), shrub (T. throughout (2006)
spicata) oil (300 ripening
mg/kg), and period
combined
extracts (150
mg/kg each)
Goat Rosemary NA Inhibition with NA Nassu et al.
fermented powder (0.025 antioxidant (2003)

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sausage and 0.050 g/100 treatments
g)
TPC: Total phenolic content; GAE: gallic acid equivalent; NA: not available; MDA: malondialdehyde; CE
catechin equivalent; dw: dry weight * in comparison to control treatment

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Table 2 – Effect of natural antioxidants on sensory attributes of sheep/goat meat and

meat products
Meat/meat Source of Effect on sensory attributes References
product antioxidants
(concentration)
Fresh lamb Rosemary extract (4 Preservation of red color and Camo et al.
steaks g/100 g) and Oregano inhibition of discoloration and (2008)
and Rosemary films off-odor formation
Lamb leg Green tea (0.5 and 5 Lowest scores for oxidation odor Bellés et al.
g/100 g) and Borage and flavor (green tea 5 g/100 g (2017)
chops
seed (10 g/100 g) and borage 10 g/100 g)

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Ground Avishane shirazi and Preservation of color (clove Aliakbarlu &
sheep meat clove essential oils at essential oil), odor and overall Sadaghiani

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0.25 g/100 g acceptability (Avishane shirazi (2015)
essential oil) after 9 days

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Ground Sumac and Barberry Preservation of color, odor and Aliakbarlu &
sheep meat water extracts (3 overall acceptability after 9 days Mohammadii
g/100 g) (2015)
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Sheep Peanut skin extract Red color loss, superficial Munekata et
patties (1000 mg/kg) discoloration and off-odor al (2016b)
formation partially inhibited
Lamb Hop infusion (2 g/kg) Addition of hop powder Villalobos-
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patties or hop powder (2 g/kg) promoted a slight decrease of Delgado et

(cooked consumer acceptance al. (2015)
and
refrigerated-
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stored)
Sheep Oregano extract (1000 Partial inhibition of red color Fernandes
burger mg/kg) loss, superficial discoloration et al.
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and off-odor formation (2016b)

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Lamb Oregano extract (13, Preservation of flavor, texture, Fernandes

burger 18, and 24 mL and overall acceptability for all et al. (2017)
extract/kg) treatments
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Sheep Litchi powder extract No effect on sensory attributes Das et al.

nuggets (1.0 and 1.5 g/100 g) (2016)
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Sheep Guava powder (0.5 No effect on appearance, flavor, Verma et al.

nuggets and 1 g/100 g) texture, juiciness, and overall (2013)
acceptability
Sucuk Green tea (300 Increased overall acceptability Bozkurt
sausage mg/kg), shrub (T. after ripening (2006)
spicata) oil (300
mg/kg), and combined
extracts (150 mg/kg
from each)
Goat Rosemary powder Increased overall acceptance, Nassu et al.
fermented (0.025 and 0.050 reduced the loss of redness and (2003)
sausage g/100 g) prevented off-flavor formation
(rosemary powder 0.050 g/100
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Table 3 – Effect of natural antioxidants on instrumental color parameters of sheep/goat

meat and meat products
Meat/meat Source of L* a* References
product antioxidants
(concentration)
Fresh lamb Oregano film and NA Inhibition Camo et al.
steaks rosemary extract (4 (2008)
g/100 g)
Fresh lamb Rosemary film NA Partial Camo et al.
steaks inhibition (2008)

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Lamb leg Green tea (0.005, 0.05, Reduction
(5 Inhibition Bellés et al.
chops 0.5, and 5 g/100 g) g/100g) (0.5 and 5 (2017)
g/100g)
Lamb leg Borage seed (0.5, 5, Reduction (10 Inhibition Bellés et al.

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chops and 10 g/100 g) g/100 g) (10 (2017)
g/100g)

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Lamb patties Olive pomace and red No effect Inhibition Andrés et al.
grape by-product (1000 (2017b)
mg/kg)
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Lamb patties Pomegranate and No effect No effect Andrés et al.
tomato by-product (2017b)
(1000 mg/kg)
Lamb patties Resveratrol, citroflavan- No effect Partial Nieto et al.
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3-ol (50, 100, 200, 300, loss (2010)

and 400 mg/kg) inhibition
Lamb patties Olive leaf and No effect No effect Nieto et al.
Echinacea (Echinacea (2010)
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purpurea) extract (50,

100, 200, 300, and 400
mg/kg)
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Lamb patties Hop infusion (2 g/kg) or Hop powder Inhibition Villalobos-

(raw and hop powder (2 g/kg) presented Delgado et
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refrigerated- higher L* than al. (2015)

stored) infusion and
control patties
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Sheep patties Peanut skin extract No effect Partial Munekata et

(1000 mg/kg) inhibition al (2016b)
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Sheep burger Oregano extract (1000 No effect Partial Fernandes et

mg/kg) inhibition al. (2016b)
Lamb burger Oregano extract (13, No effect Partial Fernandes et
18, and 24 mL loss al. (2017)
extract/kg)
Lamb burger Rosemary and thyme No effect No effect Cózar et al.
(0.1 g/100 g) (2013)
Sheep Litchi powder extract NA NA Das et al.
nuggets (1.0 and 1.5 g/100 g) (2016)
Sheep Guava powder (0.5 and No effect Increase Verma et al.
nuggets 1 g/100 g) (1 g/100 (2013)
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g)
Sucuk Green tea (300 mg/kg), No effect No effect Bozkurt
sausage shrub (T. spicata) oil (2006)
(300 mg/kg), and
combined extracts (150
mg/kg from each)
Goat Rosemary powder NA NA Nassu et al.
fermented (0.025 and 0.050 g/100 (2003)
sausage g)
NA: Not available.

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Table 4 –Natural antioxidants on lipid and protein oxidative stability of sheep/goat meat
and meat products
Meat/meat Source of Novel Lipid Protein References
product antioxidants approach oxidation* oxidation*
(concentration) used
Fresh Rosemary film (4 Antioxidant Partial NA Camo et al.
lamb g/100 g) film inhibition (> (2008)
steaks 2 mg

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MDA/kg)
Fresh Oregano film and Antioxidant < 2 mg NA Camo et al.

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lamb rosemary extract film MDA/kg (2008)
steaks (4 g/100 g)

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Irradiated Irradiated potato Gamma Reduced by Reduced Kanatt et al.
lamb leg peel extract (0.04 irradiation 54% (leg) by around (2005)
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and rib g/100 g) (2.5 kGy) and 74% 30% (leg
meat (rib) and rib)
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Irradiated Mint extract (0.05 Gamma Reduced by NA Kanatt et al.

lamb g/100 g) irradiation 25% (2007)
(5 kGy) (around 0.6
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mg
MDA/kg)
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Irradiated Mint extract (0.1 Gamma Reduced by NA Kanatt et al.

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lamb g/100 g) irradiation 50% lipid (2007)

(5 kGy) oxidation
(around 0.4
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mg
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MDA/kg)

MDA: Malondialdehyde; NA: not available; kGy: kilogray. *in comparison to control treatment.
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Figure Captions

Figure 1. Process of lipid oxidation of unsaturated fatty acids

Figure 2. Process of protein oxidation and the major compounds formed

Figure 3. The three mechanisms of antioxidant action

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(A) Free radical scavenging, that can occur in the initiation, propagation and termination (during

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the hydroperoxides breakdown) phases; (B) Binding with catalyzers metal ions; (C) Electron

donation in the propagation and termination phases, stabilizing the lipid molecule. *Examples of

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polyphenols.
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Highlights
 This review explore the use of natural antioxidants (NAOX) in sheep and
goat meat and meat products
 Sheep and goat meat are prone to oxidative processes due to its
composition
 NAOX can prevent oxidation and sensory changes in sheep and goat
meat and meat products
 NAOX hindered lipid oxidation even after novel approaches such as
irradiation

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 Application of NAOX in sheep and goat meat need more scientific
information

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Figure 1
Figure 2
Figure 3