Natural antioxidants in processing and storage stability of sheep and goat meat products

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: DOI: Reference:

S0963-9969(18)30409-5 doi:10.1016/j.foodres.2018.05.041 FRIN 7631

To appear in:

Food Research International

Received date: Revised date: Accepted date:

27 February 2018 11 May 2018 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. ConteJunior , 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

This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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.

RI

PT

Conte-Juniorª,b,f*

a

Departamento de Tecnologia de Alimentos, Faculdade de Veterinária,

SC

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

NU

Instituto de Química, Centro de Tecnologia, Universidade Federal do Rio de

Janeiro, Rio de Janeiro, RJ 21941-909, Brasil

Centro Tecnológico de la Carne de Galicia, rúa Galicia n° 4, Parque

MA

c

Tecnológico de Galicia, San Cibrao das Viñas, 32900 Ourense, Spain d

ED

Departamento de Engenharia de Alimentos, Faculdade de Zootecnia e

Engenharia de Alimentos, Universidade de São Paulo, Pirassununga, São

e

EP T

Paulo, SP 13635-900, Brasil

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

f

AC C

Bag X 1314, Alice, South Africa Instituto Nacional de Controle de Qualidade em Saúde, Fundação Oswaldo

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: [email protected]

ACCEPTED MANUSCRIPT 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

PT

antioxidants, extracted from several vegetable sources, have been considered

RI

an attractive alternative for this conflicting situation. Phenolic compounds are

SC

minor components in herbs, spices, tea and fruits that display potential application against the progression of lipid and protein oxidation and their

NU

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

MA

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

ED

antioxidants in sheep and goat meat products, which have a high susceptibility

EP T

to oxidative processes compared to other red meats.

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

AC C

compounds Protein oxidation

ACCEPTED MANUSCRIPT 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,

PT

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

RI

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

SC

texture changes, development of off-flavor and off-odor, loss of nutritional quality, limited shelf life and formation of secondary compounds that can be

NU

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

MA

The oxidative stability of meat depends on various intrinsic and extrinsic factors such as the concentration of pro-oxidants, enzymatic activity, pH, and

ED

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

EP T

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

AC C

Joseph, Li, Steinke, & Fontaine, 2009; Suman & Joseph, 2013). Moreover, sheep and goat meat presents similar fatty acid composition whereas 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).

ACCEPTED MANUSCRIPT 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

PT

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

RI

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

SC

Franco, 2013a; Munekata et al., 2017a; Şahin et al., 2017, Lorenzo et al., 2018a). On the other hand, compounds with antioxidant activity can be naturally

NU

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

MA

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

ED

Nonetheless, the effectiveness of natural antioxidants in meat products depends mainly on composition of extract vegetable and their antioxidant

EP T

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

AC C

Kukula-Koch et al., 2013; Kumar et al., 2015). The aim of this review is to explore the meat quality changes related to 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

ACCEPTED MANUSCRIPT 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

PT

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

RI

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

SC

presenting more heme pigments and reactive iron, which are known to catalyze the lipid oxidation (Chaijan, 2008; Faustman et al., 2010). Lipid oxidation is a

NU

complex chain reaction process dependent on oxygen that promotes oxidative deterioration of fatty acids with the production of free radicals and happens at

MA

three different phases namely initiation, propagation and termination (Figure 1) (Falowo et al., 2014; Guéraud et al., 2010). The initiation phase occurs in the

ED

presence of favorable conditions like light or thermal reaction, radiation, the presence of pro-oxidants or reactive oxygen species (ROS). In this phase, there

EP T

is the abstraction of a hydrogen radical from an unsaturated fatty acid generating an alkyl radical (R•) that reacts with oxygen leading to the formation

AC C

of peroxide radicals (ROO•). These peroxide radicals react with unsaturated fatty acids and produce hydroperoxides (ROOH), which are the primary 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

ACCEPTED MANUSCRIPT 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

PT

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

RI

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

SC

loss of fatty acids due to oxidation. Nevertheless, the most used methods evaluate the primary and/or secondary lipid oxidation products. For the primary

NU

compounds, there are methods that evaluate the formation of conjugated dienes and hydroperoxides by spectrophotometry, peroxide levels through

MA

titrimetric method and electron spin resonance (ESR) spectroscopy, which measures the free radical formation from the absorption of electromagnetic

ED

energy by a paramagnetic center with unpaired electrons (free radicals) (Eaton & Eaton, 2002; Guyon et al., 2016). There is a new trend to measure through chromatographic

EP T

hydroperoxides

methods since they are more

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

AC C

2016). Fourier Transformed Infrared Spectroscopy (FTIR) is another technique to measure meat oxidation, which identify functional groups of molecules 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

ACCEPTED MANUSCRIPT 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

PT

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

RI

therefore some chromatographic techniques for MDA quantification have been

SC

developed, which present more accuracy, sensitivity and specificity (Barriuso et al., 2013). Another important secondary oxidation products are the volatile

NU

compounds responsible for the off-odor and off-flavor such as propanal, hexanal and pentanal, which can be measured through gas chromatography

MA

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

ED

Likewise, the protein oxidation occurs due to covalent modifications of proteins, whereas the main targets are the functional groups on the side chains

EP T

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

AC C

myoglobin or metal catalysts (Soladoye, Juárez, Aalhus, Shand, & Estévez, 2015; Stadtman & Levine, 2003). The oxidative damage of the amino acids can produce modifications of the side chains, conversion of different amino acids, fragmentation of the peptide backbone and formation of inter and intramolecular 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

ACCEPTED MANUSCRIPT 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

PT

derivatives (Stadtman & Levine, 2003).

RI

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

SC

side chains of arginine, lysine and proline are oxidized by metal-catalyzed reactions and form carbonyl residues, while others amino acids like cysteine or are

more

related

to

cross-linking

or yield sulfur-containing

NU

methionine

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

MA

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

ED

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

EP T

Regarding methods of protein oxidation assessment, the initial and most used method to quantify protein oxidation is the quantification of protein

AC C

carbonyls using the 2,4 dinitrophenylhydrazine (DNPH) method (Estévez, 2011). But later another advanced methodology was developed with the 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;

ACCEPTED MANUSCRIPT 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)

PT

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

RI

spectroscopy represent other methodology for protein oxidation assessment

SC

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

Lipid and protein oxidation begin with similar paths whereas free radicals

NU

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

MA

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

ED

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

EP T

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

AC C

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

ACCEPTED MANUSCRIPT According to Estévez (2011), the reciprocal transfer of ROS and nonreactive 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

PT

same period, which leads to an accelerated oxidative degradation and

RI

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

SC

development. However, these authors evidenced that addition of antioxidants used to inhibit lipid oxidation usually also exhibits effects against myoglobin

NU

oxidation. 3. Use of antioxidants in meat

MA

The use of antioxidants is a primary action taken by the meat industry to increase the shelf life of their products (Lorenzo et al., 2018b). These

ED

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

EP T

species (Figure 3) (Augustyniak et al., 2010). However, the uncertain impact of synthetic sources of antioxidant in health has been considered as a relevant

AC C

downside for consumers due to potential health risk. In this conflicting scenario of large scale use in meat products and health concern, synthetic antioxidants 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

hydroxyanisole,

common butylated

food

antioxidant

hydroxytoluene,

additives

propyl

are

gallate,

butylated and

tert-

ACCEPTED MANUSCRIPT 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 &

PT

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

RI

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

SC

The European Food Safe Authority (EFSA) recognizes the potential harmful effects of synthetic antioxidants for public health and warns about their

NU

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

MA

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

ED

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

EP T

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

AC C

to the gastrointestinal tract.

In the same line, United States Food & Drug Administration (FDA) has 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

ACCEPTED MANUSCRIPT 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

PT

Zealand (2016).

RI

3.2. Natural antioxidants

SC

The search for natural antioxidants became a subject of major research leading to the production of studies that report, in general lines, the content of

NU

main antioxidants and their antioxidant activity (evaluated by at least three distinct methods) (Brewer, 2011; Kumar et al., 2015). Several natural sources

MA

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

ED

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

EP T

compounds, carotenoids, and essential oils (Munekata, Franco, Trindade, & Lorenzo, 2016a). Phenolic compounds are a diverse group of secondary

AC C

metabolites widely distributed in the food of vegetable origin. The antioxidant activity of these compounds is determined by numbers and positions of the 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

ACCEPTED MANUSCRIPT 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

PT

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

RI

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

SC

are normally obtained without heating by hydrodistillation, steam distillation or dry distillation (Brewer, 2011). Essential oils were already extracted from

NU

turmeric (Curcuma longaI), (Rosmarinus officinalis) , ginger (Zingiber officinale) and thyme (Thymus vulgaris) , wherein the main compounds identified are

MA

alcohols, aldehydes, phenylpropanoids, terpenes or ketones, which have a wellknown antioxidant activity through scavenge free radicals or free iron chelation

ED

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

EP T

natural antioxidants are considered. 4. Effect of natural antioxidants on lipid and protein oxidation

AC C

Although several sources and compounds that display antioxidant activity, phenolic compounds are the main studied group in sheep and goat meat and 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

ACCEPTED MANUSCRIPT 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

PT

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

RI

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

SC

g/100 g; rich in rosmarinic, syringic and synapic acids) and green tea (0.005, 0.05, 0.5 and 5 g/100 g; rich in catechin, myricetin, quercetin and kaempferol)

NU

aqueous extracts. Lipid oxidation was remarkably reduced by addition of both borage (5 and 10 g/100 g) and green tea (0.5 and 5 g/100 g) extracts after 13

MA

days of storage (Bellés, Alonso, Roncalés & Beltrán, 2017). In ground sheep meat, the effect of sumac (Rhus coriaria L.) and barberry

ED

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

EP T

reduced by 78% and 62% in Sumac and Barberry treatments, respectively (Aliakbarlu & Mohammadii, 2015). A number of Chinese medicinal herbs can be

AC C

exploited as potential sources of natural antioxidants. A study evaluated the antioxidant effect of 10 commonly consumed herbs in China in ground sheep 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,

ACCEPTED MANUSCRIPT 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,

PT

2015).

RI

Regarding studies that evaluated addition of natural antioxidants in

SC

processed meat, Andrés, Petrón, Adámez, López & Timón (2017b) observed that extracts obtained from agro-industries by-products (olive, pomegranate, red

NU

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

MA

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

ED

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

EP T

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

AC C

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

ACCEPTED MANUSCRIPT 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

PT

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

RI

presented lower protein oxidation assessed by carbonyls quantification.

SC

In sheep burgers packaged under modified atmosphere (80% O2 and 20% CO2) and stored for 20 days at 2 °C, addition of oregano extract (1000 mg/kg)

NU

inhibited the lipid oxidation by 40-50% and protein oxidation by 20-30% assessed by means of TBARS and protein carbonyls values, respectively

MA

(Fernandes, Trindade, Lorenzo, Munekata & Melo, 2016b). Moreover, in this experiment authors observed similar effect to burgers elaborated with BHT (50

ED

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

EP T

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

AC C

lipid and protein oxidation indexes, at the end of the storage time, were obtained for control treatment whereas the evolution of such indexes was 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

ACCEPTED MANUSCRIPT 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

PT

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

RI

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

SC

addition of 1.0 and 1.5 g/100 g of litchi powder extract decreased lipid oxidation throughout storage time in comparison to control treatment. Authors also

NU

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

MA

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

ED

storage. Guava powder at both tested concentration increased the antioxidant status of sheep nuggets, in a concentration-dependent manner, and inhibited by

EP T

40% in comparison to control treatment. The antioxidant activity of natural extracts has also been studied in the

AC C

production of fermented sausages. Bozkurt (2006) studied the effects of green tea (300 mg/kg) and shrub (T. spicata) oil (300 mg/kg), along with the 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

ACCEPTED MANUSCRIPT 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

PT

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

RI

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

SC

also observed that sensory scores were positively correlated with L* and b* values during ripening. In fermented goat sausage treated by rosemary extract

NU

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

MA

addition of 0.050 g/100 g rosemary extract in powder form. Differently, authors indicated that sausages elaborated with 0.025 g/100 g rosemary extract in

ED

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

EP T

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

AC C

concentration-dependent manner from 13.5 (control sausage) to 14.3 and 22.7 𝜇moles of Trolox equivalent/100 g (addition of 1.5 and 3 g/100 g of rice bran, 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.

ACCEPTED MANUSCRIPT 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).

PT

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

RI

rosemary extract treatments preserved instrumental red color after 13 days of

SC

storage. However, in comparison with rosemary extract directly sprayed in meat surface, the same extracted within the film package showed less protection

NU

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

MA

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

ED

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

EP T

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

AC C

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

ACCEPTED MANUSCRIPT 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

PT

to authors (Bellés et al., 2017).

RI

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

SC

color acceptability was prevented by clove essential oil, while odor acceptability was preserved by Avishane shirazi essential oil after 9 days. Overall

NU

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

MA

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

ED

(oxidation of myoglobin) which in turn is influenced by the oxidative stability of whole meat (Aliakbarlu & Sadaghiani, 2015). The addition of sumac and

EP T

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

AC C

treatments. According

to

authors, such extracts can contribute to the

preservation and also improve the shelf life of sheep ground meat (Aliakbarlu & 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

ACCEPTED MANUSCRIPT 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

PT

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

RI

the enhanced water holding capacity, which increases tenderness and overall

SC

perception of quality.

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

NU

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

MA

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

ED

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

EP T

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

AC C

received higher scores. The authors also argued that such differences could be explained by the intrinsic sensory properties of hop that has intense smell and 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

ACCEPTED MANUSCRIPT 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 study

with

lamb

burgers,

oregano

extract

at

three

PT

another

different

RI

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

SC

during 120 days of frozen storage. Sensory analysis of flavor, texture, and overall acceptability was significantly higher in oregano treatments, while

NU

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

MA

Regarding natural antioxidant enhancement in nuggets products, the addition of litchi powder extract had no significant effect on sensory attributes

ED

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

EP T

appearance, flavor, texture, juiciness, and

overall acceptability. As for

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

AC C

a*, while L* remained similar among sheep nuggets treatments. Regarding texture analysis, no remarkable changes were observed due to the addition of 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

ACCEPTED MANUSCRIPT 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.

PT

Interestingly, dry sausages elaborated with rosemary powder received with

RI

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

SC

6. Recent approaches for the application of natural antioxidants Due to the instability of the phenolic compounds to light, oxygen, pH and

NU

temperature, recent studies have investigated the use of natural antioxidants under novel application forms such as edible coating or active packaging.

MA

Moreover, studies have evaluated the efficacy of natural antioxidants against oxidative changes promoted by preservation technologies that potentialize meat

ED

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

EP T

antioxidants in sheep and goat meat, there is limited information about it considering these novel technology approaches (Table 4). Therefore, further

AC C

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

ACCEPTED MANUSCRIPT 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

PT

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

RI

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

SC

12% on both ground meats on day 0. After 7 days of storage, lipid oxidation of potato peel extract treatment was reduced by 54% and 74% for leg and rib

NU

meat, respectively, in comparison to non-irradiated meats. Carbonyl formation followed a similar trend wherein protein oxidation was reduced by around 30%

MA

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

ED

protein oxidation compared to BHT also at 0.04 g/100 g. In another study about the antioxidant effect of natural extracts on

EP T

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

AC C

These authors found that mint extract at 0.05 g/100 g partially inhibited the lipid oxidation (around 0.6 mg MDA/kg), while mint extract at 0.1 g/100 g reduced in 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

ACCEPTED MANUSCRIPT 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

PT

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

RI

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

SC

to use in sheep and goat meat without interfering on sensorial parameters, mainly when modern technologies are used in these matrices. There are few

NU

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

products with greater quality.

ED

Acknowledgements

MA

comprehension of the antioxidant mechanisms and the development of

José Manuel Lorenzo and Paulo Munekata are members of the

EP T

MARCARNE network, funded by CYTED (ref. 116RT0503). The authors also thanks the Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro

AC C

(grant number E-26/201.185/2014, FAPERJ, Brazil) and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (grant number 311361/2013-7, CNPq, Brazil), and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (grant number 125, CAPES/Embrapa 2014, CAPES, Brazil) for the financial support.

ACCEPTED MANUSCRIPT References Agregán, R., Munekata, P.E.S., Franco, D., Dominguez, D., Carballo, J., & Lorenzo, J.M. (2017). Proximate composition, phenolic content and in vitro antioxidant activity of aqueous extracts of the seaweeds Ascophyllum nodosum, Bifurcaria bifurcata and Fucus vesiculosus. Effect of addition of

PT

the extracts on the oxidative stability of canola oil under accelerated storage

RI

conditions. Food Research International, 99, 986-994.

Aguiar, J., Estevinho, B. N., & Santos, L. (2016). Microencapsulation of natural

SC

antioxidants for food application – The specific case of coffee antioxidants –

NU

A review. Trends in Food Science & Technology, 58, 21–39. Aliakbarlu, J., & Khalili Sadaghiani, S. (2015). Effect of avishane shirazi (Zataria and

clove

(Syzygium

MA

multiflora)

aromaticum)

essential

oils

on

microbiological, chemical and sensory properties of ground sheep meat

ED

during refrigerated storage. Journal of Food Quality, 38(4), 240-247. Aliakbarlu, J., & Mohammadi, S. (2015). Effect of Sumac (Rhus coriaria L.) and

EP T

Barberry (Berberis vulgaris L.) water extracts on microbial growth and chemical changes in ground sheep meat. Journal of Food Processing and

AC C

Preservation, 39(6), 1859-1866. Andrés, A. I., Petrón, M. J., Adámez, J. D., López, M., & Timón, M. L. (2017b). Food by-products as potential antioxidant and antimicrobial additives in chill stored raw lamb patties. Meat Science, 129, 62-70. Andres, A. I., Petron, M. J., Delgado‐Adamez, J., Lopez, M., & Timon, M. (2017a). Effect of tomato pomace extracts on the shelf‐life of modified atmosphere‐packaged lamb meat. Journal of Food Processing and Preservation, 41(4), 1-11.

ACCEPTED MANUSCRIPT Augustyniak, A., Bartosz, G., Čipak, A., Duburs, G., Horáková, L. U., Łuczaj, … Žarković, N. (2010). Natural and synthetic antioxidants: an updated overview. Free Radical Research, 44(10), 1216-1262. Banskalieva, V., Sahlu, T., & Goetsch, A. L. (2000). Fatty acid composition of goat muscles and fat depots: A review. Small Ruminant Research, 37(3),

PT

255–268.

RI

Baker, I. A., Alkass, J. E., & Saleh, H. H. (2013). Reduction of oxidative

storage

using

SC

rancidity and microbial activities of the Karadi lamb patties in freezing natural antioxidant extracts of rosemary and ginger.

NU

International Journal of Agricultural and Food Research, 2(1), 31-42. Barriuso, B., Astiasarán, I., & Ansorena, D. (2013). A review of analytical

MA

methods measuring lipid oxidation status in foods: A challenging task. European Food Research and Technology, 236(1), 1–15.

ED

Bellés, M., Alonso, V., Roncalés, P., & Beltrán, J. A. (2017). Effect of borage and green tea aqueous extracts on the quality of lamb leg chops displayed

EP T

under retail conditions. Meat Science, 129, 153-160. Bozkurt, H. (2006). Utilization of natural antioxidants: Green tea extract and

AC C

Thymbra spicata oil in Turkish dry-fermented sausage. Meat Science, 73(3), 442-450.

Brewer, M. S. (2011). Natural antioxidants: Sources, compounds, mechanisms of action, and potential applications. Comprehensive Reviews in Food Science and Food Safety, 10(4), 221–247. https://doi.org/10.1111/j.15414337.2011.00156.x Camo, J., Beltrán, J. A., & Roncalés, P. (2008). Extension of the display life of lamb with an antioxidant active packaging. Meat Science, 80(4), 1086-1091.

ACCEPTED MANUSCRIPT Canadian Food Inspection Agency. List of Permitted Preservatives (Lists of Permitted

Food

Additives).

(2018).

https://www.canada.ca/en/health-

canada/services/food-nutrition/food-safety/food-additives/lists-permitted/11preservatives.html Accessed 10 May 2018. Carocho, M., & Ferreira, I. C. (2013). A review on antioxidants, prooxidants and

PT

related controversy: natural and synthetic compounds, screening and

RI

analysis methodologies and future perspectives. Food and Chemical

SC

Toxicology, 51, 15-25.

Chaijan, M. (2008). Review: Lipid and myoglobin oxidations in muscle foods.

NU

Songklanakarin Journal of Science and Technology, 1, 47–53. Chávez-Crooker, P., Obreque, J., Vera, J., Moya, K. (2011). Role of astaxanthin

MA

in cosmeceutical applications. In S. K. Kim (Ed.), Marine Cosmeceuticals: Trends and prospects (pp. 119-123). New York: CRC Press.

ED

Cózar, A., Linares, B., Garrido, D., & Vergara, H. (2013). Physicochemical, microbiological quality and oxidative stability in spiced lamb meat burgers.

217-222.

EP T

The Journal of Microbiology, Biotechnology and Food Sciences, 3(3), 217,

AC C

Das, A. K., Rajkumar, V., Nanda, P. K., Chauhan, P., Pradhan, S. R., & Biswas, S. (2016). Antioxidant efficacy of litchi (Litchi chinensis Sonn.) pericarp extract in sheep meat nuggets. Antioxidants, 5(2), 16, 1-10. Eaton, S. S. & Eaton, G. R. (2002). Electron Paramagnetic Resonance Spectroscopy. In E. N. Kaufmann (Ed.), Characterization of Materials doi:10.1002/0471266965.com067 EFSA. (2004). Processing Aids and Materials in contact with food on a request from the Commission related to Tertiary-Butyl Hydroquinone (TBHQ).

ACCEPTED MANUSCRIPT Journal Opinion of the Scientific Panel on Food Additives, Flavorings, 84, 150. EFSA (2011). Panel on food additives and nutrient sources added to food (ANS); scientific opinion on the reevaluation of butylated hydroxyanisoleBHA (E 320) as a food additive. EFSA Journal, 9(10), 2392

PT

EFSA. (2012). Scientific opinion on the re-evaluation of butylated hydroxyl

RI

toluene BHT (E 321) as a food additive. Panel on Food Additives and

SC

Nutrient Sources added to Food (ANS). European Food Safety Authority. EFSA Journal. 10(3), 1-44.

NU

EFSA, 2014. Scientific opinion on the re-evaluation of propyl gallate (E 310) as a food additive. EFSA Journal, 12, 3642–3687.

Science, 89(3), 259–279.

MA

Estévez, M. (2011). Protein carbonyls in meat systems: A review. Meat

ED

Falowo, A. B., Fayemi, P. O., & Muchenje, V. (2014). Natural antioxidants against lipid-protein oxidative deterioration in meat and meat products: A

EP T

review. Food Research International, 64, 171–181. Faustman, C., Sun, Q., Mancini, R., & Suman, S. P. (2010). Myoglobin and lipid

AC C

oxidation interactions: Mechanistic bases and control. Meat Science, 86(1), 86–94.

Fernandes, R. P. P., Trindade, M. A., Lorenzo, J. M., & de Melo, M. P. (2018). Assessment of the stability of sheep sausages with the addition of different concentrations of Origanum vulgare extract during storage. Meat Science, 137, 244-257. Fernandes, R. P. P., Trindade, M. A., Lorenzo, J. M., Munekata, P. E. S., & De Melo, M. P. (2016b). Effects of oregano extract on oxidative, microbiological

ACCEPTED MANUSCRIPT and sensory stability of sheep burgers packed in modified atmosphere. Food Control, 63, 65-75. Fernandes, R.P.P., Trindade, M.A., Tonin, F.G., Lima, C.G., Pugine, S.M.P., Munekata, P.E.S., ... de Melo, M.P. (2016a). Evaluation of antioxidant capacity of 13 plant extracts by three different methods: cluster analyses

PT

applied for selection of the natural extracts with higher antioxidant capacity

RI

to replace synthetic antioxidant in lamb burgers. Journal of Food Science

SC

and Technology, 53, 451-460.

Fernandes, R. P. P., Trindade, M. A., Tonin, F. G., Pugine, S. M. P., Lima, C.

NU

G., Lorenzo, J. M., & de Melo, M. P. (2017). Evaluation of oxidative stability

109.

MA

of lamb burger with Origanum vulgare extract. Food Chemistry, 233, 101-

Food Safety and Standard Authority of India. Food Safety and Standards (2010).

http://www.fssai.gov.in/home/fss-legislation/fss-

ED

Regulations.

regulations.html Accessed 10 May 2018. Standards

Australia

EP T

Food

New

Zealand.

Additives.

(2016).

http://www.foodstandards.gov.au/consumer/additives/additiveoverview/Pag

AC C

es/default.aspx Accessed 10 May 2018. Franco, D., Rodríguez- Amado, I., Agregán, R., Munekata, P.E.S., Vázquez, J.A., Barba, F.J., & Lorenzo, J.M. (2018). Optimization of antioxidants extraction from peanut skin to prevent oxidative processes during soybean oil storage. LWT-Food Science and Technology, 88, 1-8. Grossi, A., Bolumar, T., Søltoft-Jensen, J., & Orlien, V. (2014). High pressure treatment of brine enhanced pork semitendinosus: Effect on microbial

ACCEPTED MANUSCRIPT stability, drip loss, lipid and protein oxidation, and sensory properties. Innovative Food Science and Emerging Technologies, 22, 11–21. Guéraud, F., Atalay, M., Bresgen, N., Cipak, A., Eckl, P. M., Huc, L., … Uchida, K. (2010). Chemistry and biochemistry of lipid peroxidation products. Free Radical Research, 44(10), 1098–1124.

PT

Guyon, C., Meynier, A., & de Lamballerie, M. (2016). Protein and lipid oxidation

Food Science and Technology, 50, 131–143.

RI

in meat: A review with emphasis on high-pressure treatments. Trends in

SC

Hajji, H., Joy, M., Ripoll, G., Smeti, S., Mekki, I., Gahete, F. M., … Atti, N.

NU

(2016). Meat physicochemical properties, fatty acid profile, lipid oxidation and sensory characteristics from three North African lamb breeds, as

MA

influenced by concentrate or pasture finishing diets. Journal of Food Composition and Analysis, 48, 102–110.

ED

Jongberg, S., Tørngren, M., & Skibsted, L. (2018). Dose-Dependent Effects of Green Tea or Maté Extracts on Lipid and Protein Oxidation in Brine-Injected Pork

EP T

Retail-Packed

Chops.

Medicines,

5(1),

11.

https://doi.org/10.3390/medicines5010011

AC C

Kanatt, S. R., Chander, R., & Sharma, A. (2007). Antioxidant potential of mint (Mentha spicata L.) in radiation-processed lamb meat. Food Chemistry, 100(2), 451-458.

Kanatt, S. R., Chander, R., Radhakrishna, P., & Sharma, A. (2005). Potato peel extract a natural antioxidant for retarding lipid peroxidation in radiation processed lamb meat. Journal of Agricultural and Food Chemistry, 53(5), 1499-1504. Kukula-Koch, W., Aligiannis, N., Halabalaki, M., Skaltsounis, A. L., Glowniak,

ACCEPTED MANUSCRIPT K., & Kalpoutzakis, E. (2013). Influence of extraction procedures on phenolic content and antioxidant activity of Cretan barberry herb. Food Chemistry, 138(1), 406–413. Kumar, Y., Yadav, D. N., Ahmad, T., & Narsaiah, K. (2015). Recent trends in the use of natural antioxidants for meat and meat products. Comprehensive

PT

Reviews in Food Science and Food Safety, 14(6), 796-812.

RI

Ladikos, D., & Lougovois, V. (1990). Lipid oxidation in muscle foods: a review.

SC

Food Chemistry, 35, 295–314.

Lorenzo, J.M., Batlle, R., & Gómez, M. (2014c). Extension of the shelf-life of

NU

foal meat with two antioxidant active packaging systems. LWT-Food Science and Technology, 59, 181-188.

MA

Lorenzo, J.M., Bedia, M., & Bañon, S. (2013b). Relationship between flavour deterioration and the volatile compound profile of semi-ripened sausage.

ED

Meat Science, 93, 614-620.

Lorenzo, J.M., González-Rodríguez, R.M., Sánchez, M., Amado, I.R., & Franco,

EP T

D. (2013a). Effects of natural (grape seed and chestnut extract) and synthetic antioxidants (buthylatedhydroxytoluene, BHT) on the physical,

AC C

chemical, microbiological and sensory characteristics of dry cured sausage “chorizo”. Food Research International, 54, 611-620. Lorenzo, J.M., Munekata, P.E.S., Sant´Ana A.S., Carvalho, R.B., Barba, F.J., Toldrá, F., Mora, L., &Trindade, M.A. (2018a). Main characteristics of peanut skin and its role for the preservation of meat products. Trends in Food Science & Technology, 77, 1-10. Lorenzo, J. M., Pateiro, M., Domínguez, R., Barba, F. J., Putnik, P., Kovačević, D. B., ... & Franco, D. (2018b). Berries extracts as natural antioxidants in

ACCEPTED MANUSCRIPT meat products: A review. Food Research International, 106, 1095-1104. Lorenzo, J.M., Pateiro, M., García-Fontán, M.C., & Carballo, J. (2014b). Effect of fat content on physical, microbial, lipid and protein changes during chill storage of foal liver pâté. Food Chemistry, 155, 57-63. Lorenzo, J.M., Sineiro, J., Amado, I.R., & Franco, D. (2014a). Influence of

PT

natural extracts on the shelf life of modified atmosphere-packaged pork

RI

patties. Meat Science, 96, 526-534.

SC

Lucarini, M., Durazzo, A., Sánchez del Pulgar, J., Gabrielli, P., & Lombardi Boccia, G. (2017). Determination of fatty acid content in meat and meat The

FTIR-ATR

approach.

Food

Chemistry.

In

Press.

NU

products:

https://doi.org/10.1016/j.foodchem.2017.11.042.

MA

Lund, M. N., Heinonen, M., Baron, C. P., & Estévez, M. (2011). Protein oxidation in muscle foods: A review. Molecular Nutrition and Food

ED

Research, 55(1), 83–95.

Luo, H., Lin, S., Ren, F., Wu, L., Chen, L., & Sun, Y. (2007). Antioxidant and

EP T

antimicrobial capacity of Chinese medicinal herb extracts in raw sheep meat. Journal of Food Protection, 70(6), 1440-1445.

AC C

Maggio, R. M., Kaufman, T. S., Carlo, M. D., Cerretani, L., Bendini, A., Cichelli, A., Compagnone, D. (2009). Monitoring of fatty acid composition in virgin olive oil by Fourier transformed infrared spectroscopy coupled with partial least squares. Food Chemistry, 114, 1549-1554. Maiani, G., Periago Castón, M. J., Catasta, G., Toti, E., Cambrodón, I. G., Bysted, A., … Schlemmer, U. (2009). Carotenoids: actual knowledge on food sources, intakes, stability and bioavailability and their protective role in humans. Molecular Nutrition & Food Research, 53(S2), S194 –S218.

ACCEPTED MANUSCRIPT Malekian, F., Khachaturyan, M., Gebrelul, S., & Henson, J. F. (2014). Composition and fatty acid profile of goat meat sausages with added rice bran. International Journal of Food Science, 2014, 1-9. Maqsood, S., Benjakul, S., Balange, A. K., Faine, L. A., Rodrigues, H. G., Galhardi, C. M., … Novelli, E. L. B. (2006). Butyl hydroxytoluene (BHT)-

PT

induced oxidative stress: Effects on serum lipids and cardiac energy

RI

metabolism in rats. Experimental and Toxicologic Pathology, 57(3), 221–

SC

226.

Méndez-Cid, F.J., Lorenzo, J.M., Martínez, S., & Carballo, J. (2017). Oxidation

NU

of edible animal fats. Comparison of the performance of different quantification methods and of a proposed new semi-objective colour scale-

Ministry

of

Health,

Labour

MA

based method. Food Chemistry, 217, 743-749. and

Welfare.

Food

Additives.

(2016).

ED

http://www.ffcr.or.jp/en/tenka/list-of-designated-additives/list-of-designatedadditives.html Accessed 10 May 2018.

EP T

Munekata, P.E.S., Dominguez, R., Franco, D., Bermúdez, R., Trindade, M.A., & Lorenzo, J.M. (2017a). Effect of natural antioxidants in Spanish salchichón

AC C

elaborated with encapsulated n-3 long chain fatty acids in konjac glucomannan matrix. Meat Science, 124, 54-60. Munekata, P. E. S., Domínguez, R., Campagnol, P. C. B., Franco, D., Trindade, M. A., & Lorenzo, J. M. (2017b). Effect of natural antioxidants on physicochemical

properties

and

lipid

stability

of

pork

liver

pâté

manufactured with healthy oils during refrigerated storage. Journal of Food Science and Technology, 54(13), 4324-4334.

ACCEPTED MANUSCRIPT Munekata, P. E. S., Fernandes, R. D. P. P., de Melo, M. P., Trindade, M. A., & Lorenzo, J. M. (2016b). Influence of peanut skin extract on shelf-life of sheep patties. Asian Pacific Journal of Tropical Biomedicine, 6(7), 586-596. Munekata, P.E.S., Franco, D., Trindade, M.A., & Lorenzo, J.M. (2016a). Characterization of phenolic composition in chestnut leaves and beer

PT

residue by LC-DAD-ESI-MS. LWT-Food Science and Technology, 68, 52-

RI

58.

SC

Nassu, R. T., Gonçalves, L. A. G., da Silva, M. A. A. P., & Beserra, F. J. (2003). Oxidative stability of fermented goat meat sausage with different levels of

NU

natural antioxidant. Meat Science, 63(1), 43-49.

Nieto, A., Isabel, A., O’Grady, M. N., Gutierrez, J. I., & Kerry, J. P. (2010).

MA

Screening of phytochemicals in fresh lamb meat patties stored in modified atmosphere packs: influence on selected meat quality characteristics.

ED

International Journal of Food Science & Technology, 45(2), 289-294. Pateiro, M., Lorenzo, J.M., Amado, I.R., & Franco, D. (2014). Effect of addition

EP T

of green tea, chestnut and grape extract on the shelf-life of pig liver pâté. Food Chemistry, 147, 386-394.

M.

AC C

Peng, X., Cheng, K. W., Ma, J., Chen, B., Ho, C. T., Lo, C., Chen, F., & Wang, (2008).

Cinnamon bark

proanthocyanidins

as

reactive

carbonyl

scavengers to prevent the formation of advanced glycation endproducts. Journal of Agricultural and Food Chemistry, 56(6), 1907-1911. Rice-Evans, C. A. (1996). Structure-antioxidant activity relationships

of

flavonoids and phenolic acids. Free Radical Biology and Medicine, 20 933956.

ACCEPTED MANUSCRIPT Sacchetti, G., Maietti, S., Muzzoli, M., Scaglianti, M., Manfredini, S., Radice, M., & Bruni, R. (2005). Comparative evaluation of 11 essential oils of different origin as functional antioxidants, antiradicals and antimicrobials in foods. Food Chemistry, 91(4), 621-632. Şahin, S., Samli, R., Birteksöz Tan, A.S., Barba, F.J., Chemat, F., Cravotto, G.,

PT

& Lorenzo, J.M. (2017). Solvent-free microwave-assisted extraction of

RI

polyphenols from olive tree leaves: antioxidant and antimicrobial properties.

SC

Molecules, 22, 1056-1068.

Shahidi, F., & Ambigaipalan, P. (2015). Phenolics and polyphenolics in foods,

NU

beverages and spices: Antioxidant activity and health effects - A review. Journal of Functional Foods, 18, 820-897.

MA

Shahidi, F., Arachchi, J. K. V., & Jeon, Y. J. (1999). Food applications of chitin and chitosans. Trends in Food Science and Technology, 10, 37-51.

ED

Soladoye, O. P., Juárez, M. L., Aalhus, J. L., Shand, P., & Estévez, M. (2015). Protein oxidation in processed meat: Mechanisms and potential implications

EP T

on human health. Comprehensive Reviews in Food Science and Food Safety, 14(2), 106–122.

AC C

Stadtman, E. R., & Levine, R. L. (2003). Free radical-mediated oxidation of free amino acids and amino acid residues in proteins. Amino Acids, 25(3–4), 207–218.

Suman, S. P., & Joseph, P. (2013). Myoglobin chemistry and meat color. Annual Review of Food Science and Technology, 4, 79–99. Suman, S. P., Joseph, P., Li, S., Steinke, L., & Fontaine, M. (2009). Primary structure of goat myoglobin. Meat Science, 82(4), 456–460. United States Food & Drug Administration. Food Additive Status List. (2018).

ACCEPTED MANUSCRIPT https://www.fda.gov/Food/IngredientsPackagingLabeling/FoodAdditivesIngr edients/ucm091048.htm Accessed 10 May 2018. Verma, A. K., Rajkumar, V., Banerjee, R., Biswas, S., & Das, A. K. (2013). Guava (Psidium guajava L.) powder as an antioxidant dietary fibre in sheep meat nuggets. Asian-Australasian Journal of Animal Sciences, 26(6), 886-

PT

895.

RI

Xiuzhu, Y., Van de Voort, F. R., & Sedman, J. (2007). Determination of peroxide

SC

value of edible oils by FTIR spectroscopy with the use of the spectral reconstitution technique. Talanta, 74, 241-246.

AC C

EP T

ED

MA

NU

.

ACCEPTED MANUSCRIPT Table 1 – Effect of natural antioxidants on lipid and protein oxidative stability of sheep/goat meat and meat products TPC

Lipid oxidation*

Protein References oxidation*

0.991.10 mg GAE/g extract

No effect

No effect

Andres et al. (2017a)

Lamb leg chops

Green tea (0.005, 0.05, 0.5, and 5 g/100 g)

Inhibition in 0.5 and 5 g/100 g

NA

Lamb leg chops

Borage seed (0.5, 5, and 10 g/100 g)

0.1520.0 mg GAE/ml extract 0.3-3.3 mg GAE/ml extract

Ground sheep meat

Sumac and Barberry water extracts (3 g/100 g) Red grape byproduct (1000 mg/kg)

Ground sheep meat

Tomato byproduct (1000 mg/kg)

Ground sheep meat

Chinese medicinal herbs (0.10 or 0.25 g/100 g)

Bellés et al. (2017)

Reduced by 78% (Sumac) and 62% (Barberry) Inhibition

NA

Aliakbarlu & Mohammadii (2015)

Inhibition

Aliakbarlu & Mohammadii (2015)

No effect

No effect

Aliakbarlu & Mohammadii (2015)

NA

Reduced by up to 67% (0.25 g/100 g Artemisia capillaris)

NA

Luo et al. (2007)

NA

EP T

AC C

RI NA

32.2 mg GAE/g extract 85.4 mg GAE/g extract

ED

Ground sheep meat

Bellés et al. (2017)

SC

Inhibition in 5 and 10 g/100 g

NU

Fresh lamb steaks

PT

Source of antioxidants (concentration) Tomato pomace

MA

Meat/meat product

Ground sheep meat

Avishane shirazi and clove essential oils (0.25 g/100 g)

NA

<0.5 mg MDA/kg after 9 days

NA

Aliakbarlu & Sadaghiani (2015)

Sheep patties

Peanut skin extract (1000 mg/kg)

32 mg GAE/g

Reduced by almost 50%

Reduced by 10%

Munekata et al. (2016b)

Lamb patties (cooked and refrigeratedstored)

Hop infusion (2 g/kg)

NA

Inhibition

Inhibition

VillalobosDelgado et al. (2015)

ACCEPTED MANUSCRIPT Hop infusion (2 g/kg) or hop powder (2 g/kg)

NA

Inhibition for both applications, which was stronger for hop powder

Lamb patties (raw and refrigeratedstored)

Hop infusion (2 g/kg) or hop powder (2 g/kg)

NA

Inhibition for both applications, which was stronger for hop powder

Lamb Hop infusion (2 patties (raw, g/kg) or hop frozenpowder (2 g/kg) stored and thawed)

NA

Inhibition

Lamb patties

Ginger and rosemary extract (0.05 and 0.5 g/100 g)

NA

Reduced by 66% (ginger) and 59% (rosemary)

Lamb patties

Resveratrol, citroflavan-3-ol (50, 100, 200, 300, and 400 mg/kg) Olive leaf and Echinacea (Echinacea purpurea) extract (50, 100, 200, 300, and 400 mg/kg)

NA

Oregano extract (13, 18, and 24 mL extract/kg)

VillalobosDelgado et al. (2015)

NA

PT

Lamb patties (cooked and refrigeratedstored)

NA

NU

SC

RI

No effect

VillalobosDelgado et al. (2015)

VillalobosDelgado et al. (2015)

Alkass et al. (2013)

Nieto et al. (2010)

Pro-oxidant effect

NA

Nieto et al. (2010)

9.1472.3 mg GAE/g dw

Reduced by 67% (18 mL/kg) and 81% (24 mL/kg)

Partial reduction

Fernandes et al. (2017)

Rosemary and thyme (0.1 g/100 g)

NA

Reduced by 6 times

NA

Cózar et al. (2013)

Sheep burger

Oregano extract (1000 mg/kg)

52.1 mg GAE/g dw

Reduced by 40-50%

Reduced Fernandes by 20-30% et al. (2016b)

Sheep nuggets

Litchi powder extract (1.0 and 1.5 g/100 g)

18.4 mg GAE/g dw

Inhibition (1.0 and 1.5 g/100 g)

NA

Das et al. (2016)

Sheep

Guava powder

44.0

Reduced by

NA

Verma et al.

Lamb burger

NA

ED

EP T

Lamb burger

AC C

Lamb patties

MA

Inhibition for NA all concentrations

ACCEPTED MANUSCRIPT (0.5 and 1 g/100 g)

mg GAE/g

40% (0.5 and 1 g/100 g)

(2013)

Sucuk sausage

Green tea (300 mg/kg), shrub (T. spicata) oil (300 mg/kg), and combined extracts (150 mg/kg each)

NA

Inhibition throughout ripening period

NA

Bozkurt (2006)

Goat fermented sausage

Rosemary powder (0.025 and 0.050 g/100 g)

NA

Inhibition with antioxidant treatments

NA

Nassu et al. (2003)

PT

nuggets

AC C

EP T

ED

MA

NU

SC

RI

TPC: Total phenolic content; GAE: gallic acid equivalent; NA: not available; MDA: malondialdehyde; CE catechin equivalent; dw: dry weight * in comparison to control treatment

ACCEPTED MANUSCRIPT Table 2 – Effect of natural antioxidants on sensory attributes of sheep/goat meat and meat products Meat/meat product

Source of antioxidants (concentration) Fresh lamb Rosemary extract (4 steaks g/100 g) and Oregano and Rosemary films chops

References

Preservation of red color and Camo et al. inhibition of discoloration and (2008) off-odor formation

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) seed (10 g/100 g) and borage 10 g/100 g)

PT

Lamb leg

Effect on sensory attributes

Avishane shirazi and Preservation of color (clove Aliakbarlu & clove essential oils at essential oil), odor and overall Sadaghiani 0.25 g/100 g acceptability (Avishane shirazi (2015) essential oil) after 9 days

Ground sheep meat

Sumac and Barberry Preservation of color, odor and Aliakbarlu & water extracts (3 overall acceptability after 9 days Mohammadii g/100 g) (2015)

Sheep patties

Peanut skin extract (1000 mg/kg)

Red color loss, superficial Munekata et discoloration and off-odor al (2016b) formation partially inhibited

Lamb patties (cooked and refrigeratedstored)

Hop infusion (2 g/kg) or hop powder (2 g/kg)

Addition of hop powder Villalobospromoted a slight decrease of Delgado et consumer acceptance al. (2015)

Sheep burger

Oregano extract (1000 Partial inhibition of red color Fernandes mg/kg) loss, superficial discoloration et al. and off-odor formation (2016b)

Lamb burger

Oregano extract (13, Preservation of flavor, texture, Fernandes 18, and 24 mL and overall acceptability for all et al. (2017) extract/kg) treatments

Sheep nuggets

NU

MA

ED

EP T

AC C

Sheep nuggets

SC

RI

Ground sheep meat

Litchi powder extract No effect on sensory attributes (1.0 and 1.5 g/100 g) Guava powder and 1 g/100 g)

Das et al. (2016)

(0.5 No effect on appearance, flavor, Verma et al. texture, juiciness, and overall (2013) acceptability

Sucuk sausage

Green tea (300 Increased overall acceptability Bozkurt mg/kg), shrub (T. after ripening (2006) spicata) oil (300 mg/kg), and combined extracts (150 mg/kg from each)

Goat fermented sausage

Rosemary powder Increased overall acceptance, Nassu et al. (0.025 and 0.050 reduced the loss of redness and (2003) g/100 g) prevented off-flavor formation (rosemary powder 0.050 g/100

ACCEPTED MANUSCRIPT

AC C

EP T

ED

MA

NU

SC

RI

PT

g)

ACCEPTED MANUSCRIPT Table 3 – Effect of natural antioxidants on instrumental color parameters of sheep/goat meat and meat products Source of L* antioxidants (concentration) lamb Oregano film and NA rosemary extract (4 g/100 g) lamb Rosemary film NA

a*

References

Fresh steaks

Inhibition

Camo et al. (2008)

Partial inhibition

Camo et al. (2008)

Lamb leg chops

(5 Inhibition Bellés et al. (0.5 and 5 (2017) g/100g) Borage seed (0.5, 5, Reduction (10 Inhibition Bellés et al. and 10 g/100 g) g/100 g) (10 (2017) g/100g) Inhibition

Andrés et al. (2017b)

No effect

Andrés et al. (2017b)

Resveratrol, citroflavan- No effect 3-ol (50, 100, 200, 300, and 400 mg/kg) Olive leaf and No effect Echinacea (Echinacea purpurea) extract (50, 100, 200, 300, and 400 mg/kg)

Partial loss inhibition No effect

Nieto et al. (2010)

Lamb patties Hop infusion (2 g/kg) or Hop powder Inhibition (raw and hop powder (2 g/kg) presented refrigeratedhigher L* than stored) infusion and control patties

VillalobosDelgado et al. (2015)

Sheep patties

Peanut skin extract (1000 mg/kg)

No effect

Partial inhibition

Munekata et al (2016b)

Sheep burger

Oregano extract (1000 No effect mg/kg)

Partial inhibition

Fernandes et al. (2016b)

Lamb burger

Oregano extract (13, No effect 18, and 24 mL extract/kg)

Partial loss

Fernandes et al. (2017)

Lamb burger

Rosemary and thyme No effect (0.1 g/100 g)

No effect

Cózar et al. (2013)

Sheep nuggets

Litchi powder extract NA (1.0 and 1.5 g/100 g)

NA

Das et (2016)

Sheep nuggets

Guava powder (0.5 and No effect 1 g/100 g)

Increase Verma et al. (1 g/100 (2013)

Lamb patties

Lamb patties

AC C

EP T

ED

Lamb patties

NU

Olive pomace and red No effect grape by-product (1000 mg/kg) Pomegranate and No effect tomato by-product (1000 mg/kg)

MA

Lamb patties

Green tea (0.005, 0.05, Reduction 0.5, and 5 g/100 g) g/100g)

RI

Lamb leg chops

SC

Fresh steaks

PT

Meat/meat product

Nieto et al. (2010)

al.

ACCEPTED MANUSCRIPT

Sucuk sausage

Green tea (300 mg/kg), No effect shrub (T. spicata) oil (300 mg/kg), and combined extracts (150 mg/kg from each)

Goat fermented sausage

Rosemary powder NA (0.025 and 0.050 g/100 g)

g) No effect

NA

AC C

EP T

ED

MA

NU

SC

RI

PT

NA: Not available.

Bozkurt (2006)

Nassu et al. (2003)

ACCEPTED MANUSCRIPT Table 4 –Natural antioxidants on lipid and protein oxidative stability of sheep/goat meat and meat products Meat/meat

Source of

Novel

Lipid

Protein

product

antioxidants

approach

oxidation*

oxidation*

(concentration)

used

Fresh

Rosemary film (4

Antioxidant

Partial

NA

lamb

g/100 g)

film

inhibition (>

Camo et al. (2008)

2 mg

PT

steaks

References

MDA/kg) Oregano film and

Antioxidant

< 2 mg

lamb

rosemary extract

film

MDA/kg

steaks

(4 g/100 g)

Irradiated

Irradiated potato

Gamma

Reduced by

Reduced

Kanatt et al.

lamb leg

peel extract (0.04

irradiation

54% (leg)

by around

(2005)

and rib

g/100 g)

(2.5 kGy)

SC

NU

MA

meat

NA

RI

Fresh

and 74%

30% (leg

(rib)

and rib) NA

Mint extract (0.05

Gamma

Reduced by

lamb

g/100 g)

irradiation

25%

(5 kGy)

(around 0.6

EP T

ED

Irradiated

(2008)

Kanatt et al. (2007)

mg MDA/kg)

Irradiated

Mint extract (0.1

Gamma

Reduced by

lamb

g/100 g)

irradiation

50% lipid

(5 kGy)

oxidation

AC C

Camo et al.

NA

Kanatt et al. (2007)

(around 0.4 mg MDA/kg)

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

ACCEPTED MANUSCRIPT Figure Captions Figure 1. Process of lipid oxidation of unsaturated fatty acids

Figure 3. The three mechanisms of antioxidant action

PT

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

RI

(A) Free radical scavenging, that can occur in the initiation, propagation and termination (during the hydroperoxides breakdown) phases; (B) Binding with catalyzers metal ions; (C) Electron

SC

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

AC C

EP T

ED

MA

NU

polyphenols.

ACCEPTED MANUSCRIPT Highlights

PT

RI SC NU



MA



ED



EP T



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

AC C



Figure 1

Figure 2

Figure 3