Meat Science 120 (2016) 107–117

Contents lists available at ScienceDirect

Meat Science

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

Natural antioxidants as food and feed additives to promote health

benefits and quality of meat products: A review
Jiang Jiang a, Youling L. Xiong a,b,⁎
a
School of Food Science and Technology, and Synergetic Innovation Center of Food Safety and Nutrition, Jiangnan University, Wuxi, Jiangsu 214122, China
b
Department of Animal and Food Sciences, University of Kentucky, Lexington, KY 40546, USA

a r t i c l e i n f o a b s t r a c t

Article history: Fresh and processed meats offer numerous nutritional and health benefits and provide unique eating satisfaction
Received 21 January 2016 in the lifestyle of the modern society. However, consumption of red meat including processed products is sub-
Received in revised form 5 April 2016 jected to increasing scrutiny due to the health risks associated with cytotoxins that potentially could be generated
Accepted 6 April 2016
during meat preparation. Evidence from recent studies suggests free radical pathways as a plausible mechanism
Available online 9 April 2016
for toxin formation, and antioxidants have shown promise to mitigate process-generated chemical hazards. The
Keywords:
present review discusses the involvements of lipid and protein oxidation in meat quality, nutrition, safety, and
Meat products organoleptic properties; animal production and meat processing strategies which incorporate natural antioxi-
Meat processing dants to enhance the nutritional and health benefits of meat; and the application of mixed or purified natural an-
Health tioxidants to eliminate or minimize the formation of carcinogens for chemical safety of cooked and processed
Nutrition meats.
Toxins © 2016 Published by Elsevier Ltd.
Oxidation
Antioxidants

1. Introduction International Agency for Research on Cancer (IARC) under World Health
Organization (WHO) issued a monograph classifying processed meat as
Meat is a highly nutritious source of food that provides high-quality carcinogen (Group I) and red meat as probable carcinogen (Group 2A),
proteins, minerals, vitamins, and many other micronutrients. Consump- based on the survey of published human and animal studies on meat
tion of meat, particularly red meat (beef, pork, and lamb), is dated back consumption in relation to colorectal and other types of cancer.
to antiquity and remains to be a dominant lifestyle and usually a nutri- While the IARC's claim remains disputable and the outweighing nu-
tionally indispensable form of life in the modern society. However, de- tritional benefits of processed meats cannot be ignored, innovative pro-
spite the overwhelming nutritional benefits, red meat consumption cessing and ingredient strategies must be developed to minimize the
has been linked with coronary heart diseases and several types of can- health concern and improve the products' overall organoleptic, nutri-
cer. A purported underlying mechanism is the generation of chemical tional, and health qualities. Much of the claim that processed meats
toxins (carcinogens and mutagens) during processing operations, such are unhealthy stems from the ingredients that are added during pro-
as curing, smoking, fermentation, and heat treatment (McAfee et al., cessing as well as the processing condition itself (Jiménez-Colmenero,
2010). Therefore, processed red meat is subjected to particular scrutiny. Carballo, & Cofrades, 2001; Vitaglione & Fogliano, 2004). On this, oxida-
Processed meat encompasses a wide variety of products prepared tion and associated deleterious changes often are viewed as a main
through some degree of muscle structural alterations along with the ap- causative factor. Due to the presence of added salt (NaCl), heme iron,
plication of various functional food ingredients for organoleptic and and the relative abundance of endogenous phospholipids, processed
preservation purposes. Deli-style sliced ham, frankfurters, and fresh muscle foods are very susceptible to oxidative reactions. Indeed,
sausages are examples of common processed products. In spite of the radical-induced lipid and protein oxidation occurring in high-
re-creatable taste, food variety, convenience, and good nutritional temperature cooking contributes to the formation of potentially harm-
value desired by the consumer, processed meats are often perceived ful health hazards. These include a variety of carbonyl-based cytotoxic
to be less healthy than many other types of food. In October, 2015, the and genotoxic compounds known as ‘advanced lipid oxidation end
products (ALEs)’, such as 4-hydroxynonenal (4-HNE) and malonalde-
hyde (MDA) (Kanner, 2007; Negre-Salvayre, Coatrieux, Ingueneau, &
⁎ Corresponding author at: School of Food Science and Technology, and Synergetic
Innovation Center of Food Safety and Nutrition, Jiangnan University, Wuxi, Jiangsu
Salvayre, 2008), mutagenic heterocyclic aromatic amines (HAAs) formed
214122, China. at high temperatures, such as 2-amino-1-methyl-6-phenylimidazo[4,5-b]
E-mail address: [email protected] (Y.L. Xiong). pyridine (PhIP) and 2-Amino-3,8-dimethylimidazo[4,5-f]quinoxaline (8-

http://dx.doi.org/10.1016/j.meatsci.2016.04.005
0309-1740/© 2016 Published by Elsevier Ltd.
108 J. Jiang, Y.L. Xiong / Meat Science 120 (2016) 107–117

MeIQx) (Shabbir, Raza, Anjum, Khan, & Suleria, 2015; Turesky, 2007), and (PUFA) as constituents of membrane phospholipids, the deficiency of
carcinogenic nitrosamines in nitrite-cured products (Toldra, 2010). endogenous antioxidants, such as tocopherols, when compared with
Recent advances in antioxidant research have enabled meat sci- vegetable and other plant oils, yet, high concentrations of pro-
entists to think the possibility of mitigating chemical toxins in oxidants and radical initiators, such as heme species, high concentra-
meat products through different strategies, for example, moderate tions of salt (NaCl) added, and the abundance of molecular oxygen
thermal processing conditions to reduce the toxin formation, bio- that is usually incorporated into blended meats during processing oper-
accessibility restriction technology, and antioxidant interventions ations (Kanner, Harel, & Salan, 1988). Salt has been found to reduce the
(Engel, Ratel, Bouhlel, Planche, & Meurillon, 2015). The latter is of activity of catalase, glutathione peroxidase, and superoxide dismutase
particular interest because it is believed that many of the toxin- (Lee, Mei, & Decker, 1997), which may be one of the reasons why salted
forming reactions involve free radicals in which reactive oxygen spe- fresh meat has poor oxidative stability.
cies (ROS) are particularly implicated. While synthetic antioxidants, During meat processing, oxygen can be converted to various reactive
such as butylated hydroxyanisole (BHA), butylated hydroxytoluene species (ROS), including hydroxyl radical (•OH), superoxide anion
(BHT), propyl gallate (PG), and tertiary butylhydroquinone (O2•−), ferryl and perferryl species [Oxy-Fe(IV)•+], lipid peroxyl radical
(TBHQ), have long been used to inhibit oxidation-induced deleteri- (LOO•), alkoxyl radical (LO•), and many others (Decker & Hultin, 1992;
ous changes in meat, they are under increasing scrutiny due to the Kanner et al., 1988). A variety of secondary products are generated in
potential genotoxic effects. Therefore, the current industrial trend the process of lipid peroxidation, notably reactive carbonyl species,
has shifted toward natural antioxidants derived from various plant such as MDA and 4-HNE. Many of the lipid oxidation end products
materials which are rich in radical-scavenging polyphenols (ALEs) are responsible for oxidative rancidity and can participate in
(Shahidi, Janitha, & Wanasundara, 1992). ‘Nature-origin’ antioxi- heath-hazardous compound formation through reaction with other
dants have also been developed from enzymatic hydrolysis of pro- meat components.
tein (peptides) and cross-linking of small molecules into The advances in meat science research over the past two decades
amphiphilic antioxidants suitable for the interface (in emulsions, have led to a wealth of information indicating that muscle proteins are
foams, etc.) (Elias, Kellerby, & Decker, 2008; Jiang & Xiong, 2015; also susceptible to both radical and non-radical ROS, and, in some
Xiong, 2010). While synthetic antioxidants at high dosage applica- cases, even more labile to radicals than PUFA (Yang & Xiong, 2015).
tion levels can be carcinogenic, there is much less documented evi- The mechanism of protein oxidation has been described in several com-
dence indicating adverse effects of natural antioxidants. Not only prehensive reviews (Stadtman, 2006; Xiong, 2000). Discussion of the
are natural antioxidants capable of neutralizing ROS therefore reduc- specific impact of protein oxidation on the functionality and quality of
ing the probability of toxin formation when high temperatures are meat has been presented by Xiong and Decker (1995) and Estevez
applied (Balogh, Gray, Gomaa, & Booren, 2000), but when used in (2011). In general, the same oxidants that initiate lipid oxidation have
the product formulation they could also augment existing antioxi- been found to cause and propagate protein oxidation, and carbonyl for-
dant potential even if meat is not subjected to extensive processing. mation is a common reaction pathway found in the oxidation process. In
This added health and nutritional benefit could be a distinctive ad- addition, proteins can react with secondary products of lipid peroxida-
vantage of natural antioxidants applied to meat processing. tion, for example, aldehydes and ketones, to produce carbonyl deriva-
In human bodies, the antioxidant defense system includes enzymes tives and protein–protein and protein-lipid complexes (Butterfield &
(e.g., superoxide dismutase, glutathione peroxidases, and catalase), iron Stadtman, 1997). In muscle food systems, •OH is readily generated
and copper-binding extracellular proteins (e.g., albumin, transferrin, through the reaction of H2O2 or lipid peroxide with iron or copper and
lactoferrin, haptoglobin, and ceruloplasmin), antioxidant vitamins causes site-specific modification of amino acids, such as methionine
(e.g., vitamin C, vitamin E, and β-carotene), and other cellular com- and lysine (Park & Xiong, 2007).
pounds (e.g., quinones, glutathione, uric acid, and bilirubin) (Krinsky,
1992). In addition, various exogenous phenolic compounds derived H2O2 + Fe(II)/Cu(I) → • OH+ OH− + Fe(III)/Cu(II)
from dietary fruits, vegetables, legumes, or ingredients added to food,
such as spices and herbs used in processed meats, contribute to the an-
tioxidant pool. These dietary sources of antioxidants are essential when •OH+ Protein(lysine) − NH2 → Protein– COH (carbonyl)
the body is exposed to a high degree of radical stress.
Antioxidants used to preserve raw and precooked meat have re- The formation of protein radicals via reacting with ROS involves the
cently been reviewed. Karre, Lopez, and Getty (2013) analyzed the anti- abstraction of a hydrogen atom from methylene groups (α-carbon)
oxidant effects of several fruit juice and plant extracts on meat and next to the peptide bond (carboxyamide). This is essentially similar to
poultry; Shah, Bosco, and Mir (2014) reviewed the protective role of lipid oxidation where free radicals are formed initially by producing
several plant extracts in the oxidative stability of meat; similarly, an unpaired electron while abstracting a hydrogen from the methylene
Kumar, Yadav, Ahmad, and Narsaiah (2015) described recent trends in group adjacent to the double bond. Many amino acid residue side chains
the use of natural antioxidants for meat and meat product quality pro- are readily modified by ROS. Amino acids with reactive side chains (sulf-
tection. In our present review, we describe the potential efficacy of sev- hydryl, thioether, amino group, imidazole ring, and indole ring) are
eral antioxidant strategies, including those applied to meat animal most susceptible to oxidation initiated by oxidizing lipids and their
production to boost the antioxidant pool in muscle tissue and those di- products (Roubal & Tappel, 1966; Stadtman, 2006). Thus, cysteine, me-
rectly added to meat product formulations, to improve the health and thionine, lysine, arginine, histidine and tryptophan residues are com-
nutritional benefits of meat and meat products. Our focus is on the inhi- mon targets of ROS generated via lipid peroxidation. Other susceptible
bition of toxin formation and the enhancement of nutritional status of amino acids include valine, serine and proline. Electron spin resonance
meat products by natural antioxidants. (ESR) has been used to identify protein and amino acid radicals as direct
evidence of protein oxidation (Lund, Luxford, Skibsted, & Davies, 2008).
2. Lipid and protein oxidation in meat and meat products Common consequences of protein oxidation in complex meat sys-
tems include increased susceptibility to proteolytic enzymes, protein
Lipid peroxidation in meat products occurs primarily through the polymerization which produces soluble aggregates that may promote
radical chain reaction mechanism although singlet oxygen may provide gelation and emulsification, or insoluble aggregates that are
an alternative pathway (Min & Ahn, 2005). The high degree of suscepti- impedimental to water binding and texture (Srinivasan & Hultin,
bility of animal fat to oxidation in such products is due to a variety of fac- 1997; Xiong, Blanchard, Ooizumi, & Ma, 2010; Xiong, Park, & Ooizumi,
tors: the relatively high proportion of polyunsaturated fatty acids
 J. Jiang, Y.L. Xiong / Meat Science 120 (2016) 107–117 109

2009). Because of their highly reactive nature, electron-deficient car- Gao, & Oomah, 1998; Yoo, Lee, Lee, Moon, & Lee, 2008). The activity is
bonyls (aldehydes and ketones) in oxidatively-stressed proteins can attributed to various phenolic compounds, which are structurally relat-
cross-link with free amino groups and other nucleophilic moieties to ed but differ in quantity and type, depending on the specific source. The
form heterogeneous polymers (Feeney, Blankenhorn, & Dixon, 1975) major phenolic constituents in spices and herbs are phenolic acids
that not only impair the product quality and nutritional value but also (e.g., gallic acid, caffeic acid, and rosmarinic acid), phenolic diterpenes
generate health concerns due to the potential to modify cellular enzyme (e.g., carnosic acid and carnosol), flavonoids (e.g., catechin, quercetin,
and genetic materials (Butterfield & Stadtman, 1997). Due to chemical apigenin, kaempferol, naringenin, and hesperetin), and volatile oils
modifications of amino acid side chain groups and aggregation or (e.g., eugenol, carvacrol, thymol, menthol) (Brewer, 2011). Other active
cross-linking of proteins, oxidation can change the digestibility of pro- compounds have also been isolated, for example, carotenoids. Among
tein, therefore, affect the nutritional quality. In general, mild oxidation the most widely studied phenolic acids are gallic acid, carnosic acid,
does not influence proteolytic degradation of muscle proteins, but ex- caffeic acid, and chlorogenic acid.
tensive oxidation can decrease proteolytic digestion (Liu & Xiong, A common property of these phenolic compounds is the ability to
2000; Sante-Lhoutellier, Aubry, & Gatellier, 2007; Soladoye, Juárez, break free radical chain reactions by the donation of hydrogen and elec-
Aalhus, Shand, Estévez, 2015). trons (Shahidi et al., 1992). Of particular note are rosemary extract, lic-
orice extract, oregano, black pepper, and clove oil; they have received
3. Variety of natural antioxidants considerable attention for use as flavoring agents in processed meats.
Rosemary extract, a potent antioxidant, is one of the most widely used
3.1. General consideration natural ingredient in the meat industry. Its antioxidant activity has
been associated with the presence of several phenolic diterpenes, such
Natural antioxidants are produced in living cells to maintain a deli- as carnosic acid, carnosol, rosmanol, rosmariquinone, and
cate oxidation–reduction balance in the process of nutrient metabolism rosmaridiphenol (Aruoma, Halliwell, Aeschbach, & Löligers, 1992). For
and immune function. Upon oxidative stress, antioxidants will react licorice, triterpene saponins and flavonoids are major active com-
with radical and non-radical species to initiate defense mechanisms pounds, along with several phenolic acids in minor quantities, of
for the protection of both intracellular and extracellular components. which, liquiritigenin, liquiritin, isoliquiritigenin, isoliquiritin, glabridin,
The plant kingdom is the most abundant source of antioxidants, which glabrene, licochalcone, and glycycoumarin are prevalent (Zhang & Ye,
are richly present in spices (seeds), herbs, and essential oils used in 2009). Oregano extracts contain high concentrations of phenolics, espe-
meat products for organoleptic purposes. Certain fruits and vegetables cially rosmarinic acid.
are also good sources of antioxidants and other phytochemicals. Many Green tea extracts as nutraceutical supplements have been used as
tree leaves, although not used for flavoring, are also good sources of natural antioxidant, antibacterial, and antiviral agents. They have been
phenolic compounds, and tea is an excellent example of this plant anti- reported to exhibit anticarcinogenic and antimutagenic activity (Yang
oxidant family. Some minerals and vitamins function as co-factors of an- & Landau, 2000). The well-known antioxidant power of tea is due to
tioxidant enzymes, therefore, are also considered natural antioxidants. the high content of catechins, tannin, and other flavonoids. The primary
Nature has also produced a number of multi-functional short peptides catechin polyphenol constituents include epigallocatechin gallate
that are capable of neutralizing free radicals and chelating pro- (EGCG), epicatechin gallate (ECG), epigallocatechin (EGC), and epicate-
oxidative metal ions. The latter has led to the preparation of ‘natural’ an- chin (EC) (Bronner & Beecher, 1998). Aside from potent radical scav-
tioxidant peptides through enzymatic hydrolysis of proteins (Table 1). enging ability, these flavonoids are also capable of binding iron to
When used as antioxidants for product quality preservation, these nat- further enhance their antioxidant potential in the cell (Shahidi et al.,
ural compounds may also be regarded as nutraceutical ingredients or 1992). Cocoa leaves are typically discarded during tree pruning, but
supplements for health promotion. Indeed, plant-derived antioxidants are a good source of catechins (Hassan & Fan, 2005).
provide meat processors with the flexibility to develop novel products
with enhanced nutritional value and health benefits, an improved 3.3. Fruits
shelf-life, and an attractive overall quality profile.
Fruits in general are good sources of antioxidants. Apples, blue-
3.2. Herbs, spices, extracts, and active compounds berries, plums, grapes, cranberries, pomegranates, and bearberries con-
tain relatively high concentrations of flavonoids (Brewer, 2011; Shahidi
Antioxidant activity is widely observed in spices and herbs, for ex- et al., 1992). Purees and extracts have been prepared from these fruits
ample, oregano, rosemary, thyme, cinnamon, pepper, nutmeg, licorice, for industry uses, and their antioxidant activity has been well docu-
aniseed, cassia bark, fennel, prickly ash, round cardamom, basil, garlic, mented (Karre et al., 2013). Grape seed proanthocyanidin extract was
coriander, and ginger (Kong, Zhang, & Xiong, 2010; Velioglu, Mazza, reported to provide significantly greater protection against free radicals

Table 1
Natural antioxidants used to inhibit oxidation in processed meat products.

Antioxidant Main active Example Mode of action Treated meat product Reference
category compound

Spices, herbs, Phenolic acids, Gallic acid, rosemarinic acid, Radical scavenger, Breakfast sausage, Jiang et al. (2013); Kong et al. (2010)
and extracts terpenoids canosic acid, caffeic acid, metal ion chelator precooked pork
glabrene
Fruits, leaves, Flavonoids, Procyanidins, quercetin, Radical scavenger Cooked burger patties, raw Ganhão et al. (2010); Jo et al. (2003)
and extracts water-soluble catechin and cooked pork patties
vitamins
Nuts, seeds, and Tocopherols, α-, β-, γ-, and δ-Tocopherols Radical scavenger Restructured steaks, Cofrades et al. (2004); Jiménez-Colmenero et al.
extracts tocotrienols frankfurters (2010)
Essential oils Polyphenols, Eugenol Radical scavenger Turkey meat patties, beef Loizzo et al. (2015); Sharafati-Chaleshtori et al.
terpenoids burgers (2015)
Peptides and Short peptides Carnosine, Tyr-Phe-Glu, Radical scavenger, Cooked beef, meat patties, Cheng et al. (2014); Decker and Crum (1991); Nieto
protein Tyr-Ser-Thr-Ala metal ion chelator meat emulsions, et al. (2009); Sun and Xiong (2015); Wang and Xiong
hydrolysates frankfurters (2005)
110 J. Jiang, Y.L. Xiong / Meat Science 120 (2016) 107–117

and free radical-induced lipid peroxidation and DNA damage than vita- functions has been suggested to be the possible anticarcinogenic mech-
mins C, E and β-carotene (Bagchi et al., 1997; Balogh et al., 2000). The anism of vitamin C.
powerful antioxidant potential is attributed to the extremely high con-
centrations of polyphenols, such as gallic acid, the monomeric flavan-3- 3.5. Peptides and protein hydrolysates
ols catechin, epicatechin, gallocatechin, epigallocatechin, epicatechin 3-
O-gallate, resveratrol, and procyanidin dimers, trimers, and more highly Hydrolyzed protein has long been used for flavor and water binding
polymerized procyanidins (Shi, Yu, Pohorly, & Kakuda, 2003). According in meat products. However, it was not fully recognized until recently
to the study of Zheng and Wang (2003), phenolic constituents and con- that many peptides present in protein hydrolysates exhibit powerful
tents among different berries varied considerably. Anthocyanins were radical scavenging and metal ion-binding capacity, therefore, can be
found to be the main components in blueberry, cranberry, and choke- treated as antioxidants for the inhibition of unwanted oxidative pro-
berry; chlorogenic acid in blueberry, quercetin glycosides in cranberry cesses. Indeed, a myriad of peptides and peptide mixtures prepared
and lingonberry, and caffeic acid and its derivative in chokeberry were from enzymatic hydrolysis of plant proteins of soy, corn, potato, and
also present in relatively high concentrations. These phenolic acids, buckwheat (Chen, Muramoto, Yamauchi, Fujimoto, & Nokihara, 1998;
along with peonidin 3-galactoside, cyanidin 3-galactoside, and cyanidin Cheng, Chen, & Xiong, 2014; Li, Han, & Chen, 2008; Ma, Xiong, Zhai,
3-galactoside, were the most important antioxidants in these berries. Zhu, & Dziubla, 2010; Pihlanto, Akkanen, & Korhonen, 2008) and
Phenolics such as quercetin and cyanidin, with 3′,4′-dihydroxy substit- animal-derived proteins, such as whey (Elias et al., 2006; Peña-Ramos
uents in the B ring and conjugation between the A and B rings, have & Xiong, 2001), casein (Kim, Jang, & Kim, 2007), gelatin (Mendis,
highly effective radical scavenging structures. Rajapakse, & Kim, 2005), egg (Dávalos, Miguel, Bartolomé, &
López-Fandiño, 2004; Xu, Shangguan, Wang, & Chen, 2007), and muscle
3.4. Vitamins and minerals (Raghavan & Kristinsson, 2008; Saiga, Tanabe, & Nishimura, 2003;
Thiansilakul, Benjakul, & Shahidi, 2007).
Vitamins are widely distributed in plant sources and are incorpo- The existence of antioxidant peptide segments within a protein may
rated into foods either in the pure form or as components within food help explain why dietary protein intake can promote health beyond the
additives. For example, when vegetable oils and tree nuts are used as in- normal nutritional benefits. For example, feeding rats the extract of
gredients in reduced-fat meat products, a considerable amount of to- Douchi (a traditional Chinese fermented soybean product that contains
copherols are introduced. Likewise, when apple pomace is added to numerous antioxidant peptides) was found to enhance the superoxide
meat product formulations, the product would be enriched with ascor- dismutase activity in liver and kidney, catalase activity in liver, and glu-
bic acid. Several minerals (as co-factors of antioxidant enzymes) and vi- tathione peroxidase activity in kidney (Wang et al., 2008). Not surpris-
tamins are antioxidative, and their roles in protecting the cell and ingly, the extract also lowered lipid peroxidation in liver. Antioxidant
muscle tissue from radical-mediated structural damage are well peptides have also been isolated from in vitro digests of proteins. A
established (Hercberg et al., 1998). For this reason, antioxidant vitamins 16-amino acid peptide (1.8 kDa) showing strong antioxidant activity
and minerals have been used as nutritional and functional additives in was isolated from peptic hydrolysate of hoki frame protein (Kim, Je, &
animal feed (Radecki, Juhl, & Miller, 1988; Wenk, 2000). Kim, 2007). The protein hydrolysate inhibited lipid peroxidation more
Numerous basic and clinical studies have pointed to the role of ROS, effectively than α-tocopherol, and efficiently quenched different free
particularly free radicals, in many pathologic processes, and indicated radicals, including •OH and O2•−. It also reduced peroxide-induced cyto-
the protective effect of antioxidant vitamins, such as vitamin A (β-caro- toxicity on human embryonic lung fibroblasts as well as protected DNA
tene as precursor), vitamin C (ascorbic acid), and vitamin E (α-tocoph- from radical damage. Our recent study also showed that 0.1–2.8 kDa an-
erol), and minerals, notably selenium and zinc, for cardiovascular health tioxidative peptides isolated from whey protein hydrolysate were
and cancer prevention (Diplock, 1991). In the SU.VI.MAX trial study that strongly protective of lung fibroblast MRC-5 cells against hydrogen
comprised 5141 men randomized to take either a placebo or a supple- peroxide-induced oxidative damage (Kong, Peng, Xiong, & Zhao, 2012).
mentation with nutritional doses of vitamin C, vitamin E, β-carotene, se-
lenium, and zinc daily for 8 years, it was found that these antioxidant 4. Antioxidant feed additive strategies
supplements lowered the incidence of prostate cancer (Meyer et al.,
2005). The same study also led to the conclusion that low-dose antiox- The addition of antioxidants as nutritional supplements in animal
idant supplementation lowered total cancer incidence and all-cause diets is a common practice to improve animal performance, health,
mortality in men but not in women (Hercberg et al., 2004). Supplemen- and welfare. For meat animals, natural antioxidants added to feed not
tation may be effective in men only because of their lower baseline sta- only can improve the oxidative stability and organoleptic properties of
tus of certain antioxidants, especially of beta carotene. The findings meat but they also can enhance the nutritional value and the health
supported the hypothesis that chemoprevention of prostate cancer benefit of meat products (Kasapidou et al., 2012; Lynch, Kerry,
can be achieved with nutritional doses of antioxidant vitamins and min- Buckley, Faustman, & Morrissey, 1999; Phillips et al., 2001). Recently,
erals. On the basis of convincing clinical evidence and the fact that reg- there has been a growing interest in supplementing animal feeds with
ular diets may not provide adequate antioxidant supply, it is strongly plant antioxidant extracts or raw antioxidant plant materials to boost
advised that people at the midlife age take antioxidant vitamin and min- the nutritional value of meat for consumers' health benefits. For exam-
eral supplements to achieve an optimum health (Kesse-Guyot et al., ple, radical-scavenging rosemary leaves (Nieto, Estrada, Jordán, Garrido,
2011). & Bañón, 2011), grape seed extract (Jerónimo et al., 2012), and licorice
Vitamin E (α-tocopherol) is one of the four isomers (the others are extract (Zhang et al., 2015) as animal feed additives have been shown
β-, γ-, δ-tocopherols) of the tocopherol family. In the food industry, to decrease lipid oxidation and improve quality of lamb meat. Lamb
mixed tocopherols, which also include α-, β-, γ-, and δ-tocotrienols, fed distilled rosemary or thyme in the diet for several months showed
are commonly used as natural antioxidants. Aside from their direct an- a higher antioxidant stability of the meat, a higher concentration of
tioxidant role to neutralize of radicals through electron donation (•H), in polyphenolic antioxidants, and a delayed color deterioration in the
biological systems, vitamin C has been shown to scavenge aqueous hy- meat (Nieto, Diaz, Banon, & Garrido, 2010; Serrano, Jordan, & Banon,
droxyl (•OH) and superoxide (O2•−) radicals, and act as a chain-breaker 2014).
in lipid peroxidations (Rock, Jacob, & Bowen, 1996). Ascorbic acid may α-Tocopherol as the most traditional feed additive up to about
also act indirectly in protecting lipid membranes by regeneration of 500 mg/kg feed supplementation levels could maintain the redness of
the active form of membrane-bound vitamin E. The ability to stabilize fresh beef on retail display, and this protective effect is exerted via the
carcinogens or block carcinogenic processes and enhance immune delayed oxidation of oxymyoglobin and the inhibition of PUFA
 J. Jiang, Y.L. Xiong / Meat Science 120 (2016) 107–117 111

oxidation (Faustman, Chan, Schaefer, & Havens, 1998). Similar findings high O2 (80%) modified atmosphere under refrigerated storage condi-
have been documented for lamb (González-Calvo, Ripoll, Molino, Calvo, tions (O'Grady, Maher, Troy, Moloney, & Kerry, 2006).
& Joy, 2015) as well as poultry meat (King, Uijttenboogaart, & Devries,
1995). Moreover, there has been a continuing effort to manipulate the 5. Antioxidant food ingredient strategies
fatty acid composition of meat through feed regimens. The goal of the
livestock producer is to produce nutritionally balanced or enhanced 5.1. Product quality consideration
meat that contains appropriate amounts of n-3 PUFA (from α-
linolenic acid) versus n-6 PUFA formed from linoleic acid (18:2) The demonstrated efficacy of natural antioxidants, in the form of ei-
(Williams, 2000). n-3 Fatty acids, especially long chain n-3 PUFA, are ther a pure extract, a blend of active components, or a powder of the
known to reduce the risk of many diseases, such as arteriosclerosis, cor- original seeds, leaves, etc., to retard lipid oxidation and flavor deteriora-
onary heart disease, inflammatory diseases, and possibly behavioral dis- tion in meat products has stimulated a broad interest within the meat
orders (Connor, 2000). Feeding pigs dried distillers grain with solubles industry to explore nontraditional food ingredient strategies. The atten-
(DDGS) has been shown to increase PUFA iodine value (Soladoye, tion to natural antioxidants is heightened by the recent global trend to
Shand, Aalhus, Gariepy, Juarez, 2015). However, an excessive amount gradually phase out synthetic food additives that have traditionally be
of PUFA deposition could compromise the textural quality of pork utilized in the food chain. Existing and potential natural antioxidant
belly (softness) intended for bacon. Because of the increased suscepti- technologies applied to meat for shelf-life protection are focused on
bility to oxidation, PUFA-enriched meat may have a reduced shelf-life, plant-derived compounds that target primarily on fresh or freshly pre-
therefore, a high-PUFA diet should include an antioxidant supplement pared meat (for review, see Karre et al., 2013; Kumar et al., 2015;
as well. Shah et al., 2014). In comparison, the application of natural antioxidants
Organic minerals as co-factors of antioxidant enzymes offer another in ‘further processed’ meats, which are subjected to considerable mus-
dietary strategy to improve the quality and nutrition of meat. In a recent cle structure alteration, protein extraction, treatment with functional
study conducted in the authors' lab, cross-bred pigs were fed a basal diet ingredients such as salt and phosphate, and different thermal processes,
supplemented with 0.3 mg/kg sodium selenite as control, 0.3 mg/kg or- has been much less investigated.
ganic selenium (Sel-Plex), or 0.3 mg/kg Sel-Plex plus 1.5% linseed oil Jayathilakan, Sharma, Radhakrishna, and Bawa (2007) applied
(rich in n-3 PUFA) during growing-finishing periods. Pork from both ascorbic acid (5 mg/kg), cloves (25 mg/kg), and cinnamon (25 mg/kg)
Sel-Plex diets contained 38.1% more Se than pork from the control to treat precooked sheep, beef and pork, and reported that after storage
diet, indicating more efficient absorption of organic minerals. Pork at 6 °C for 6 days, the production of warmed-over-flavor (WOF,
from the Sel-Plex with linseed oil treatment group also had twice the expressed as n-hexanal formation) was suppressed by more than 50%,
amount of n-3 fatty acids found in other two groups. Apart from the im- and the inhibition was highly correlated with antioxidant potential of
proved nutritional value, drip loss of stored meat (4 °C up to 6 days) was these plant extracts. Colindres and Brewer (2011) evaluated the effect
reduced up to 48% by the dietary Sel-Plex supplement, coinciding with of three natural (grape seed extract, oleoresin rosemary, and oregano
greater glutathione peroxidase activity. The 0.3 mg/kg Sel-Plex plus lin- extract) and three synthetic (PG, BHA, and BHT) antioxidants on sen-
seed oil treatment also produced the most tender pork. Feeding pigs sory, color and oxidative stability of cooked (71 °C), frozen (−18 °C),
with mixed antioxidant organic minerals (Bio-Plex) also produced fur- then reheated ground beef patties, showing the effectiveness of the an-
ther evidence supporting the nutritional and organoleptic benefits. tioxidants in the order of PG ~ grape seed extract N oleoresin
Many of the micronutrients present in Bioplex® are co-factors for mus- rosemary N BHA N oregano extract ~ BHT N control in 6 months of stor-
cle tissue cellular antioxidant enzymes (Se for glutathione peroxidase; age. There are many similar and related studies reporting effective pro-
Zn/Cu or Mn/Fe for superoxide dismutase). Free Fe and Cu can act as tection of cooked meat quality by antioxidant-rich spices, herbs, plant
prooxidants in meat, but this may not be necessarily true for organic phenol extracts, tocopherols, and some fruits and vegetable (Ahn,
minerals. Indeed, cooked pork loin from the Bio-Plex group exhibited Grün, & Mustapha, 2007; Han & Rhee, 2005; Juntachote, Berghofer,
an increased oxidative stability when stored at 4 °C, compared with Siebenhandl, & Bauer, 2006; Thongtan, Toma, Reiboldt, & Daoud,
the inorganic mineral group. 2005). Furthermore, essential oils applied to raw and cooked burgers
Aromatic herbs and essential oils have been used in animal feed to can effectively prevent oxidative rancidity (Loizzo, Tundis, Menichini,
improve the flavor and palatability of meat. Essential oil plants and es- & Duthie, 2015; Sharafati-Chaleshtori, Rokni, Rafieian-Kopaei, Drees, &
sential oils are known for their antioxidant potency which is mainly at- Salehi, 2015).
tributed to phenolic compounds in the oil or in other phytochemical Natural antioxidants have also been shown to provide strong protec-
fractions. Some nonphenolic substances also exhibit antioxidant activ- tion for processed meats. Sebranek, Sewalt, Robbins, and Houser (2005)
ity, for example, caryophyllene, careen, and terpinene (Franz, Baser, & evaluated a commercial rosemary extract for antioxidant effectiveness
Windisch, 2010). Such substances contribute to the protection of feed at concentrations of 1500 and 2500 mg/kg in precooked then frozen
lipids from oxidative damage, since the antioxidant status of the feed pork sausage (2.6% salt; cooked to 71 °C then stored at − 20 °C). The
can have a profound impact on the quality and oxidative shelf-life of rosemary extract was found equally effective to BHA/BHT in maintain-
meat (Delles, Xiong, True, Ao, & Dawson, 2014). A dietary supply of ing low TBARS values of the precooked sausage. In a more recent
thyme oil and thymol to aging rats showed a beneficial effect on the an- study (Kong et al., 2010), we compared 13 common spice extracts for
tioxidant enzymes superoxide dismutase and glutathione peroxidase their antioxidant efficacy and found that clove, rosemary, and cassia
(Youdim & Deans, 2000). In chicken, oregano added in doses of bark extracts (5 mg/kg), all having a high polyphenol content, were re-
50–100 mg/kg to the broiler diet exerted an antioxidant effect in the markably effective in inhibiting lipid peroxidation in cooked (73 °C),
muscle tissue (Youdim & Deans, 2000). Meat and membrane phospho- breakfast pork sausage patties (containing 1.5% salt) during refrigerated
lipids from broilers fed 500 mg/kg rosemary and sage extracts exhibited storage (4 °C). As expected, sensory panel analysis detected significantly
a significantly lower oxidation rate than those fed 200 mg/kg α- less off-flavor in these treated products than untreated. Similarly, we
tocopherol and the control after 9 days of refrigerated storage noted substantial suppression of lipid oxidation in precooked pork sau-
(Govaris et al., 2007). Feeding green tea to livestock has mixed results. sage patties (20% fat) containing 1.5% salt and various concentrations of
Zembayashi, Lunt, and Smith (1999) reported that feeding cattle green licorice and rosemary extracts during refrigerated (2 °C up to 14 days)
tea (0.5 kg/d) reduced the iron content, redness, and intramuscular and frozen (− 20 °C up to 6 months) storage (Jiang, Zhang, True,
lipid content of the muscle tissue. While feeding cattle tea catechins Zhou, & Xiong, 2013). Sausage treated with 0.1% of the spice extracts
and rosemary extract did not improve lipid or color stability, direct ad- showed the same TBARS-inhibitory capacity as 0.01% BHA (fat basis).
dition (1000 mg/kg) can improve color stability of loin slices held in a Sensory panel evaluation confirmed strong inhibition of rancidity and
112 J. Jiang, Y.L. Xiong / Meat Science 120 (2016) 107–117

WOF-type off-flavor development by licorice extract, corroborating its chlorogenic acid greatly depressed the gelling capacity. The result was
remarkable anti-radical activity due to the presence of multiple pheno- explained by the fact that low and intermediate concentrations of the
lics, including liquiritigenin, glabrene, glabridin, glabrol, isoliquiritin, phenolic acid allowed the production of soluble myosin aggregates
liquiritin apioside, isoliquiritin apioside, licorice glycoside A, which that were conducive to gel networks, and the high concentrations, the
were most abundantly detected (Jiang et al., 2013). It is of interest phenolic promoted the formation of excessive amounts of disulfide link-
that the efficacy of licorice phenolic extract was synergistically en- ages leading to protein insolubilization. Dose-dependent effects of
hanced by the presence of antioxidant peptides prepared from hydro- green tea extract on the textural and oxidative stability of meat emul-
lyzed pea protein (Zhang, Xiong, Chen, & Zhou, 2014). Similarly, sions has also been studied. Jongberg, Terkelsen, Miklos, and Lund
Ginkgo biloba extract was used as a natural antioxidant to inhibit lipid (2015) reported that green tea at 100, 500, and 1500 mg/kg levels all
oxidation in dumplings (Kobus-Cisowska, Flaczyk, & Jeszka, 2010) and inhibited formation of TBARS (lipid) as well as thiol oxidation (protein)
meatballs (Kobus-Cisowska, Flaczyk, Rudzińska, & Kmiecik, 2014), and and myosin cross-linking. However, only the 100 mg/kg green tea ex-
the products' shelf-life was reported to be excellent. Flavonoid extracts tract showed no negative effect on the textural stability of meat emul-
from fruits, such as cloudberry and beetroot, were shown to be effective sion; increasing concentrations of the extract resulted in the
as well to reduce lipid oxidation in cooked pork patties (Rey, Hopia, disruption of meat emulsion properties leading to reduced water-
Kivikari, & Kahkonen, 2005). holding capacity and textural stability.
The incorporation of protein hydrolysates in meat and meat prod-
ucts for the protection against lipid oxidation is a recent trend. In an ex- 5.2. Nutritional and health benefits of antioxidants
ploration study, we developed antioxidant hydrolysates by controlled
Alcalase hydrolysis of potato protein. Cooked beef patties formulated 5.2.1. Health promotion
with 1.5% salt and 5% protein hydrolysate, which showed potent Apart from improving shelf-life and organoleptic qualities, the use of
radical-scavenging and metal ion-binding potential, exhibited 80–90% plant-derived nutraceuticals rich in antioxidant flavonoids and pheno-
reductions in lipid peroxide and TBARS formation over a 7 day storage lics may allow meat processors to develop novel products with en-
period at 4 °C. In a subsequent investigation, we showed that addition hanced nutritional and health benefits (Table 2). For example,
of 2.5% antioxidant potato protein hydrolysate significantly improved incorporation of vegetable food ingredients, such as rice bran and wal-
emulsion stability and decreased cooking losses, and had a significant nut extract that are rich in vitamin E, vitamin B, and polyphenols, into
inhibitory effect on lipid oxidation, in nitrite-free cooked frankfurters vegetable oil-substituted sausage, restructured beef, and other proc-
with 15 and 30% fat (Nieto et al., 2009). These results suggest that essed meats improved the oxidative stability, textural properties, and
mixed peptides have both antioxidant and emulsifying properties nutritional value of the products (Álvarez, Xiong, Castillo, Payne, &
which may be of potential suitability for meat emulsion manufacturing. Garrido, 2012; Álvarez et al., 2011; Cofrades et al., 2004;
Addition of casein peptides (20 mg/mL), obtained by the proteolytic en- Jiménez-Colmenero, Sánchez-Muniz, & Olmedilla-Alonso, 2010). Im-
zymes alcalase and flavourzyme, was shown to completely inhibit lipid provement in color, texture, and vitamin A content of beef patties by
oxidation in ground beef homogenates (Rossini, Noreña, Cladera- the addition of cooked carrot and sweet potato has been reported
Olivera, & Brandelli, 2009). Antioxidant peptides can also protect mus- (Saleh & Ahmed, 1998). Likewise, Csapo, Incze, Kovacs, Zelenak, and
cle proteins from oxidation changes, therefore, are able to modify the Zsigo (2006) developed a variety of meat products with added lutein
functionality of salt-soluble myofibrillar proteins in the process of com- to enrich the pro-vitamin A content thereby promoting the eye health.
minuted meat products (Wang & Xiong, 2008). Similarly, apple pomace as a polyphenol-rich by-product of apple juice
Several studies have also shown efficacy of natural antioxidants for production can be a valuable source of nutraceuticals with antioxidants
preventing protein oxidation under meat processing conditions. Jia, for processed meats (Hyson, 2011; Rather, Akhter, Masoodi, Gani, &
Kong, Liu, Diao, and Xia (2012) applied polyphenol-rich black current Wani, 2015). The presence of dietary fibers in fruit and vegetable ingre-
extract at 5, 10 and 20 g/kg application levels to raw pork patties with dients impart additional benefits to meat products.
2% salt, recording a dose-dependent significant prevention of TBARS When incorporated into meat processing, many of the antioxidant
and protein carbonyl formation and loss of protein sulfhydryls during compounds present in plant extracts are also of therapeutic functions,
refrigerated storage. Ganhão, Morcuende, and Estévez (2010) added fla- and their diverse roles in promoting human health and inhibiting vari-
vonoid and polyphenol-rich fruit extracts (30 g/kg) from arbutus berry, ous physiological disorders and pathological conditions have been
hawthorn, dog rose, and elm-leaf blackberry into emulsified cooked well documented. Consumption of meat products rich in natural antiox-
burger patties, noticing significant inhibition of protein oxidation (car- idants has been shown to reinforce the endogenous antioxidant efficacy
bonyls) in the patties when stored at 2 °C. In addition to donating hy- against oxidative stress and ROS-induced tissue damage and degenera-
drogen to inhibit thiol group oxidation, antioxidant phenolic tive diseases (Valenzuela, Sanhueza, & Nieto, 2003). While natural phe-
compounds can form quinine-thiol adducts via quinones and this has nolic antioxidants as food ingredients are of general effectiveness in
been demonstrated in the mixture of oxidized 4-methylcatechol and promoting the overall health, the protection of the gastrointestinal
isolated myofibrillar protein (Jongberg, Lund, Waterhouse, & Skibsted, tract health seems to be most obvious because absorption is not re-
2011). The blockage of the thiol groups inhibits disulfide bond forma- quired (Halliwell, Rafter, & Jenner, 2005). Unlike most non-protein anti-
tion, thus, prevents excessive covalent aggregation and insolubilization oxidants that have the exclusive role of stabilizing free radicals and
of proteins which may be detrimental to processed meat quality. Simi- inhibiting radical propagation, antioxidant peptides may exert other bi-
larly, using MALDI-TOF/TOF MS, Tang et al. (2015) detected adducts ological functionalities, for example, antihypertensive, anticancer, anti-
formed between quinones (derived from rosmarinic acid) and thiols microbial, immunomodulatory, and opioid activities (Mine, Li-Chan, &
from peptides of a myosin digest under meat processing conditions, Jiang, 2010). Thus, naturally occurring antioxidant peptides and those
and the amount of adducts increased with the cooking temperature. derived from protein hydrolysis are now considered as novel and poten-
The concentration of phenolics used in meat processing must be tial food ingredients to promote human health.
carefully controlled in order to obtain the targeted benefit. For example,
when studying dose-dependent effects of chlorogenic acid on the gela- 5.2.2. Mitigation of chemical toxicity
tion of pork myofibrillar under meat processing conditions (0.6 M NaCl, The formation of cytotoxic compounds in cooked and processed
pH 6.2) in the presence of ROS, Cao and Xiong (2015) noted that at 6 and meats may involve free radicals. Chen, Pearson, and Gray (1990) re-
30 μmol/g application levels, chlorogenic acid, which modified the ported that heterocyclic aromatic amines (HAA) MeIOx and
structure of protein, increased the protein gel network strength by as imidazoquinoxaline (IQ), which have been linked to cancer and other
much as 40%, while treatment of the protein with 150 μmol/g health conditions, were formed in frying ground beef as a result of
 J. Jiang, Y.L. Xiong / Meat Science 120 (2016) 107–117 113

Table 2
Natural antioxidants that inhibit toxin formation in cooked and processed meat.

Meat product Toxin formed Inhibitory antioxidant Responsible Reference

agent

Fried beef patties HAAs (MeIQx and PhIP) Rosemary, turmeric, fingerroot, galangal, Polyphenols Balogh et al. (2000); Britt et al. (1998);
cherry, vitamin E Puangsombat et al. (2011)
Fried meatballs HAAs (IQ, MeIQx, PhIP) Black pepper Polyphenols Oz and Kaya (2011)
Pan fried beef PhIP Green tea extract EGCG Melo, Viegas, Petisca, Pinho, and Ferreira (2008)
Beef juice HAAs (IQ, MeIQx) Tomato Carotenoid Vitaglione et al. (2002)
Quercetin
Cooked meat ALEs (MDA) oxidized Ginkgo biloba extract Polyphenols Kobus-Cisowska et al. (2014)
cholesterol
Cooked salted pork patties MDA Carnosine Carnosine Decker and Crum (1991, 1993)
Cooked cured meat protein Nitrosamine (NDEA) α-Tocopherol, green tea extract Phenolics Yang et al. (2013)
extracts

reaction between creatinine and radicals of alkylpyridine. Hence, it is The degree of HAA inhibition was significantly correlated to the total
conceivable that cooking and processing meat with antioxidant-rich phenolic content and the scavenging activity of spices, indicating the
spice, herb, and other plant extracts could reduce the formation of antioxidative protection. Fig. 1 presents a proposed mechanism by
such toxic compounds. The natural antioxidant approach is a relatively which phenolic antioxidants inhibit the formation of HAAs in heated
new and interesting concept which may prove valuable as an alterna- and processed meats. Based on the report of Zamora, Alcon, and
tive method to promote meat product health. Hidalgo (2014), it can be suggested that antioxidants can stop reaction
Indeed, a growing number of studies have provided preliminary ev- 1 by diverting to pathway 1′ via binding to the precursor
idence supporting the hypothesis of inhibiting carcinogenic toxin for- (e.g., creatinine) or reaction 2 via stabilization of radicals (pathway 2′)
mation in meat by natural antioxidants (Vitagoline & Fogliano, 2004). since both reactions are thought to be oxidant-driven.
Balogh et al. (2000) investigated the effect of α-tocopherol (vitamin In high-fat meatballs fried at three different frying temperatures
E) and oleoresin rosemary on HAA formation in fried (175, 200, and (175, 200, and 225 °C), the presence of added black pepper drastically
225 °C) ground beef patties. At the concentrations of 1 and 10% (fat- reduced the production of HAAs, including IQ, MeIQx, PhIP, and several
basis), α-tocopherol added to the ground beef patties reduced the con- others (Oz & Kaya, 2011). The highest total amount of HAAs, 37.8 ng/g,
centration of HAAs, including PhIP, the principal HAA in cooked muscle was found in control group meatballs fried at 225 °C (31.8 ng/g of which
foods, in cooked patties by 69% and 72%, respectively. Oleoresin rose- belonging to PhIP), but no PhIP was detected in meatballs with black
mary, when used at the same two concentrations (1 and 10%), reduced pepper. It appears that natural phenolic compounds present in black
PhIP formation by 44%. The same research group also showed that the pepper provided the protection.
concentration of PhIP was reduced 93 and 87% by Montmorency and Antioxidant sulfuro derivatives contained in garlic and onion were
Balaton cherry tissue, respectively (Britt, Gomaa, Gray, & Booren, also found to have an inhibitory effect on HAA formation (Shin,
1998). Puangsombat, Jirapakkul, and Smith (2011) also reported that Strasburg, & Gray, 2002). The catechin derivative EGCG contained in
in fried (204 °C) beef patties, the addition of 0.2% rosemary, turmeric, green tea had a potent inhibitory activity against PhIP, reducing its for-
fingerroot, and galangal lowered the content of HAAs (MeIQx and mation by 70% in pan-fried beef as reported by Melo, Viegas, Petisca,
PhIP) by 43.5, 39.2, 33.5, and 18.4%, respectively. Pinho, and Ferreira (2008). Some more recent studies have confirmed

Fig. 1. Proposed mechanism for the inhibition of HAA formation in cooked meat by phenolic antioxidants. For illustration, gallic acid and 2-amino-1- methyl-6-phenylimidazo[4,5-b]
pyridine (PhIP) are used. The information is partially deduced from Zamora et al. (2014).
114 J. Jiang, Y.L. Xiong / Meat Science 120 (2016) 107–117

that natural antioxidants, for example, G. biloba extract, can inhibit the practical minimum through natural antioxidant ingredient approaches.
formation of oxidized cholesterol derivatives, reduce the production The ability of antioxidant ingredients to inhibit the formation of chem-
and absorption of MDA and HAAs in cooked meat (Kobus-Cisowska ical toxins in cooked meat is in addition to the nutritional benefits that
et al., 2014). Moreover, Vitaglione, Monti, Ambrosino, Skog, and they can impart as well as the flavor and shelf-life that these functional
Fogliano (2002) found that tomatoes significantly inhibited the produc- materials can contribute. In continuing the effort to identify the most ef-
tion of HAAs, especially imidazo quinolines (IQ) and MeIQx, in cooked fective natural antioxidants from spices, herbs, fruits, and other natural
bovine meat (juice). The antioxidant activity of carotenoids in tomatoes sources for this purpose, it is important to investigate the concerted ef-
(e.g., lycopene) and flavonoids (e.g., quercetin) were credited for the fects of processing, and this should include the specific temperature, pH,
HAA inhibition. the ionic strength (salt concentration), and the presence unsaturated
The inhibitory effects of natural antioxidants on advanced lipid oxi- lipids and reducing sugars because the processing environment can pro-
dation end products (ALEs) have also been demonstrated in several foundly affect the efficacy of natural antioxidants. It would also be inter-
studies. Carnosine, a dipeptide of β-alanine and histidine that is natu- esting to monitor the fate of natural antioxidants used in cooked and
rally present in muscle tissue, is a strong cellular antioxidant and car- processed meats, namely, their own chemical changes and impact on
bonyl scavenger. When used as a food antioxidant, carnosine shows a meat quality. Finally, while there is little doubt that dietary intake of
potent inhibition of ALEs such as MDA in cooked meat. According to meat products rich in natural antioxidants can reinforce the endoge-
Decker and Crum (1991, 1993), carnosine (0.5 and 1.5%) strongly nous antioxidant power against oxidative stress, it is still not clear
inhibited formation of MDA in cooked salted and unsalted ground what percentage of antioxidants is actually absorbed into the plasma
pork, and the degree of inhibition by 1.5% carnosine was superior to so- because evidence of in vivo and in situ antioxidant effects of most natu-
dium tripolyphosphate (0.5%), α-tocopherol, and BHT (0.02% of fat con- ral antioxidants is still scant. It is almost certain, however, that dietary
tent). Carnosine was also the most effective at preventing oxidative natural antioxidants will have a significant protective effect on endothe-
rancidity and color changes as determined by a sensory panel, in salted lial cells within the gastrointestinal tract because of the high concentra-
ground pork after 1 month of frozen storage (−15 °C). These data sug- tions present. Further research is warranted to determine the amount
gested that carnosine could be used as a promising natural antioxidant and type(s) of natural antioxidants that are required to meaningfully re-
to inhibit the formation of cytotoxic ALEs in thermally processed meat. duce or totally inhibit the formation of harmful compounds in processed
In in vitro model systems, carnosine was shown to block the forma- meats based on the necessary formulation ingredients and processing
tion of MDA from lipid peroxidation (Hipkiss, Preston, Himswoth, schemes specific for each product.
Worthington, & Abbot, 1997). Moreover, it protected cultured human fi-
broblasts and rat brain endothelial cells against the toxic effects of MDA
and advanced glycation end products (AGEs). Although there has been Acknowledgments
very limited experimental evidence for the inhibition of HAAs, ALEs,
and other toxic compound formation in processed meats by peptides This is publication No. 16-07-011 of the Kentucky Agricultural Ex-
obtained from specific enzymatic hydrolysis of proteins, Petersen and periment Station with the approval of the Director. The work is sup-
Doorn (2004) did observe a high reactivity of the tripeptide glutathione ported by the National Institute of Food and Agriculture, U.S.
(Glu-Cys-Gly) for 4-HNE and its essential role in maintaining α- Department of Agriculture, Hatch project under 1005724.
tocopherol in an active state for protecting the cell against ROS-
mediated oxidative stress. As many short peptides present in protein References
hydrolysates used in meat product formulations are potent radical scav-
engers (Xiong, 2000), research is warranted to explore this potential Ahn, J., Grün, I. U., & Mustapha, A. (2007). Effects of plant extracts on microbial growth,
color change, and lipid oxidation in cooked beef. Food Microbiology, 24, 7–14.
source for the inhibition of toxin formation in processed meats. Resver- Aldini, G., Vistoli, G., Stefek, M., Chondrogianni, N., Grune, T., Sereikaite, J., ... Bartosz, G.
atrol, a polyphenol from red wine, is highly inhibitory of lipid peroxida- (2013). Molecular strategies to prevent, inhibit, and degrade advanced glycoxidation
tion and ALE formation in experimental models for numerous diseases, and advanced lipoxidation end products. Free Radical Research, 47(Suppl. 1), 93–137.
Álvarez, D., Delles, R. M., Xiong, Y. L., Castillo, M., Payne, F. A., & Laencina, J. (2011). Influ-
including atherosclerosis, diabetes, and Alzheimer diseases (Aldini et al.,
ence of canola-olive oils, rice bran and walnut on functionality and emulsion stability
2013). of frankfurters. LWT — Food Science and Technology, 44, 1435–1442.
The effect of antioxidants on the formation of N-nitrosodiethylamine Álvarez, D., Xiong, Y. L., Castillo, M., Payne, F. A., & Garrido, M. D. (2012). Textural and vis-
coelastic properties of pork frankfurters containing canola–olive oils, rice bran, and
(NDEA) in a protein oxidation pathway was investigated in a recent
walnut. Meat Science, 92, 8–15.
study (Yang et al., 2013). Fresh minced pork was untreated (control) Aruoma, O. I., Halliwell, B., Aeschbach, R., & Löligers, J. (1992). Antioxidant and pro-
or treated with 700 mg/kg α-tocopherol or 300 mg/kg tea polyphenol oxidant properties of active rosemary constituents: Carnosol and carnosic acid.
extract, packaged in a high-oxygen atmosphere (78.8% O2), then stored Xenobiotica, 22, 257–268.
Bagchi, D., Garg, A., Krohn, R. L., Bagchi, M., Tran, M. X., & Stohs, S. J. (1997). Oxygen free
at refrigerator temperature for 10 days. Myofibrillar and sarcoplasmic radical scavenging abilities of vitamins C and E, and a grape seed proanthocyanidin
proteins extracted from stored meat were reacted with 43 μM sodium extract in vitro. Research Communications in Molecular Pathology and Pharmacology,
nitrite at 80 °C for 1 h. Lipid oxidation was found to be completely 95, 179–189.
Balogh, Z., Gray, J. I., Gomaa, E. A., & Booren, A. M. (2000). Formation and inhibition of het-
inhibited by tea polyphenols but increased in control and tocopherol erocyclic aromatic amines in fried ground beef patties. Food and Chemical Toxicology,
samples after 10 days. There was significant protein oxidation (loss of 38, 395–401.
sulfhydryls, formation of protein carbonyls) in control meat and the Brewer, M. S. (2011). Natural antioxidants: Sources, compounds, mechanisms of action,
and potential applications. Comprehensive Reviews in Food Science and Food Safety,
heated protein-nitrite solution produced 182 ng/mL NDEA, compared 10, 221–247.
to 120 and 88 ng/mL in sampled treated with tocopherol and tea poly- Britt, C., Gomaa, E. A., Gray, J. I., & Booren, A. M. (1998). Influence of cherry tissue on lipid
phenol extract. Therefore, nitrosamine formation in cured meats can oxidation and heterocyclic aromatic amine formation in ground beef patties. Journal
of Agricultural and Food Chemistry, 46, 4891–4897.
be inhibited by the presence of natural antioxidants.
Bronner, W. E., & Beecher, G. R. (1998). Method for determining the content of catechins
in tea infusions by high-performance liquid chromatography. Journal of
6. Conclusions Chromatography A, 805, 137–142.
Butterfield, D. A., & Stadtman, E. R. (1997). Protein oxidation processes in aging brain.
Advances in Cell Aging and Gerontology, 2, 161–191.
The preparation of palatable and nutritious meat and meat products, Cao, Y., & Xiong, Y. L. (2015). Chlorogenic acid-mediated gel formation of oxidatively
especially from mammalian species, with negligible generation of po- stressed myofibrillar protein. Food Chemistry, 180, 235–243.
tentially health-impact chemical by-products is a great challenge to Chen, H. M., Muramoto, K., Yamauchi, F., Fujimoto, K., & Nokihara, K. (1998). Antioxida-
tive properties of histidine-containing peptides designed from peptide fragments
meat and food scientists. Nevertheless, recent exploratory research found in the digests of a soybean protein. Journal of Agricultural and Food Chemistry,
has demonstrated the feasibility to reduce such health risks to a 46, 49–53.
 J. Jiang, Y.L. Xiong / Meat Science 120 (2016) 107–117 115

Chen, C., Pearson, A. M., & Gray, J. I. (1990). Meat mutagens. Advances in Food and Jayathilakan, K., Sharma, G. K., Radhakrishna, K., & Bawa, A. S. (2007). Antioxidant poten-
Nutrition Research, 34, 387–449. tial of synthetic and natural antioxidants and its effect on warmed-over-flavour in
Cheng, Y., Chen, J., & Xiong, Y. L. (2014). Interfacial adsorption of peptides in oil-in-water different species of meat. Food Chemistry, 105, 908–916.
emulsions costabilized by Tween 20 and antioxidative potato peptides. Journal of Jerónimo, E., Alfaia, C. M. M., Alves, S. P., Dentinho, M. T. P., Prates, J. A. M., Vasta, V., ...
Agricultural and Food Chemistry, 62, 11575–11581. Bessa, R. J. B. (2012). Effect of dietary grape seed extract and Cistus ladanifer L. In com-
Cofrades, S., Serrano, A., Ayo, J., Solas, M. T., Carballo, J., & Jiménez-Colmenero, F. (2004). bination with vegetable oil supplementation on lamb meat quality. Meat Science, 92,
Restructured beef with different proportions of walnut as affected by meat particle 841–847.
size. European Food Research Technology, 218, 230–236. Jia, N., Kong, B., Liu, Q., Diao, X., & Xia, X. (2012). Antioxidant activity of black currant
Colindres, P., & Brewer, M. S. (2011). Oxidative stability of cooked, frozen, reheated beef (Ribes nigrum L.) extract and its inhibitory effect on lipid and protein oxidation of
patties: Effect of antioxidants. Journal of the Science of Food and Agriculture, 91, pork patties during chilled storage. Meat Science, 91, 533–539.
963–968. Jiang, J., & Xiong, Y. L. (2015). Role of interfacial protein membrane in oxidative stability of
Connor, W. E. (2000). Importance of n-3 fatty acids in health and disease. American Jour- vegetable oil substitution emulsions applicable to nutritionally modified sausage.
nal of Clinical Nutrition, 71(1), 171S–175S. Meat Science, 109, 56–65.
Csapo, I., Incze, K., Kovacs, L., Zelenak, L., & Zsigo, J. (2006). Development of meat products Jiang, J., Zhang, X., True, A. D., Zhou, L., & Xiong, Y. L. (2013). Inhibition of lipid oxidation
with lutein for eye health. In D. Troy, R. Pearce, B. Byrne, & J. Kerry (Eds.), Proceedings and rancidity in precooked pork patties by radical-scavenging licorice (Glycyrrhiza
of 52nd international congress of meat science and technology (pp. 687–688). glabra) extract. Journal of Food Science, 78, C1686–C1694.
Wageningen, The Netherlands: Wageningen Academic Publishers. Jiménez-Colmenero, F., Carballo, J., & Cofrades, S. (2001). Healthier meat and meat prod-
Dávalos, A., Miguel, M., Bartolomé, B., & López-Fandiño, R. (2004). Antioxidant activity of ucts: Their role as functional foods. Meat Science, 59, 5–13.
peptides derived from egg white proteins by enzymatic hydrolysis. Journal of Food Jiménez-Colmenero, F., Sánchez-Muniz, F. J., & Olmedilla-Alonso, B. (2010). Design and
Protection, 67, 1939–1944. development of meat-based functional foods with walnut: Technological, nutritional
Decker, E. A., & Crum, A. D. (1991). Inhibition of oxidative rancidity in salted ground pork and health impact. Food Chemistry, 123, 959–967.
by carnosine. Journal of Food Science, 56, 1179–1181. Jo, C., Son, J. H., Son, C. B., & Byun, M. W. (2003). Functional properties of raw and cooked
Decker, E. A., & Crum, A. D. (1993). Antioxidant activity of carnosine in cooked ground pork patties with added irradiated, freeze-dried green tea leaf extract powder during
pork. Meat Science, 34(2), 245–253. storage at 4 ºC. Meat Science, 64, 13–17.
Decker, E. A., & Hultin, H. O. (1992). Lipid oxidation in muscle foods via redox iron. In A. J. Jongberg, S., Lund, M. N., Waterhouse, A. L., & Skibsted, L. H. (2011). 4-Methylcatechol in-
St. Angelo (Ed.), Lipid oxidation in food (pp. 33–54). Washington DC., USA: American hibits protein oxidation in meat but not disulfide formation. Journal of Agricultural
Chemical Society. and Food Chemistry, 59, 10329–10335.
Delles, R. M., Xiong, Y. L., True, A. D., Ao, T., & Dawson, K. A. (2014). Dietary antioxidant Jongberg, S., Terkelsen, L. D. S., Miklos, R., & Lund, M. N. (2015). Green tea extract impairs
supplementation enhances lipid and protein oxidative stability of chicken broiler meat emulsion properties by disturbing protein disulfide cross-linking. Meat Science,
meat through promotion of antioxidant enzyme activity. Poultry Science, 93, 100, 2–9.
1561–1570. Juntachote, T., Berghofer, E., Siebenhandl, S., & Bauer, F. (2006). The antioxidative proper-
Diplock, A. T. (1991). Antioxidant nutrients and disease prevention: An overview. The ties of holy basil and galangal in cooked ground pork. Meat Science, 72, 446–456.
American Journal of Clinical Nutrition, 53(Suppl. 1), 189S–193S. Kanner, J. (2007). Dietary advanced lipid oxidation endproducts are risk factors to human
Elias, R. J., Bridgewater, J. D., Vachet, R. W., Waraho, T., McClements, D. J., & Decker, E. health. Molecular Nutrition & Food Research, 51, 1094–1101.
A. (2006). Antioxidant mechanisms of enzymatic hydrolysates of beta- Kanner, J., Harel, S., & Salan, A. M. (1988). The generation of ferryl or hydroxyl radicals
lactoglobulin in food lipid dispersions. Journal of Agricultural and Food during interaction of hemeproteins with hydrogen peroxide. In M. G. Simic, K. A.
Chemistry, 54, 9565–9572. Taylor, J. F. Ward, & C. von Sonntag (Eds.), Oxygen radicals in biology and medicine
Elias, R. J., Kellerby, S. S., & Decker, E. A. (2008). Antioxidant activity of proteins and pep- (pp. 145–148). New York, NY, USA: Springer.
tides. Critical Reviews in Food Science and Nutrition, 48, 430–441. Karre, L., Lopez, K., & Getty, K. J. K. (2013). Natural antioxidants in meat and poultry prod-
Engel, E., Ratel, J., Bouhlel, J., Planche, C., & Meurillon, M. (2015). Novel approaches to im- ucts. Meat Science, 94, 220–227.
proving the chemical safety of the meat chain towards toxicants. Meat Science, 109, Kasapidou, E., Wood, J. D., Richardson, R. I., Sinclair, L. A., Wilkinson, R. G., & Enser, M.
75–85. (2012). Effect of vitamin E supplementation and diet on fatty acid composition and
Estevez, M. (2011). Protein carbonyls in meat systems: A review. Meat Science, 89(3), on meat colour and lipid oxidation of lamb leg steaks displayed in modified atmo-
259–279. sphere packs. Meat Science, 90, 908–916.
Faustman, C., Chan, W. K., Schaefer, D. M., & Havens, A. (1998). Beef color update: The role Kesse-Guyot, E., Amieva, H., Castetbon, K., Henegar, A., Ferry, M., Jeandel, C., ... Galan, P., ...
for vitamin E. Journal of Animal Science, 78, 1019–1026. Group, T. S. V. M. R. (2011). Adherence to nutritional recommendations and subse-
Feeney, R. E., Blankenhorn, G., & Dixon, H. B. (1975). Carbonyl-amine reactions in protein quent cognitive performance: Findings from the prospective Supplementation with
chemistry. Advances in Protein Chemistry, 29, 135–203. Antioxidant Vitamins and Minerals 2 (SU.VI.MAX 2) study. The American Journal of
Franz, C., Baser, K. H. C., & Windisch, W. (2010). Essential oils and aromatic plants in an- Clinical Nutrition, 93, 200–210.
imal feeding — a European perspective. A review. Flavour and Fragrance Journal, 25, Kim, G. N., Jang, H. D., & Kim, C. I. (2007). Antioxidant capacity of caseinophosphopeptides
327–340. prepared from sodium caseinate using alcalase. Food Chemistry, 104(4), 1359–1365.
Ganhão, R., Morcuende, D., & Estévez, M. (2010). Protein oxidation in emulsified cooked Kim, S. Y., Je, J. Y., & Kim, S. K. (2007). Purification and characterization of antioxidant pep-
burger patties with added fruit extracts: Influence on colour and texture deteriora- tide from hoki (Johnius belengerii) frame protein by gastrointestinal digestion. The
tion during chill storage. Meat Science, 85, 402–409. Journal of Nutritional Biochemistry, 18, 31–38.
González-Calvo, L., Ripoll, G., Molino, F., Calvo, J. H., & Joy, M. (2015). The relationship be- King, A. J., Uijttenboogaart, T. G., & Devries, A. W. (1995). Alpha-tocopherol, beta-carotene
tween muscle α-tocopherol concentration and meat oxidation in light lambs fed vi- and ascorbic-acid as antioxidants in stored poultry muscle. Journal of Food Science, 60,
tamin E supplements prior to slaughter. Journal of the Science of Food and Agriculture, 1009–1012.
95, 103–110. Kobus-Cisowska, J., Flaczyk, E., & Jeszka, M. (2010). Antioxidant activities of Ginkgo biloba
Govaris, A., Florou-Paneri, P., Botsoglou, E., Giannenas, I., Amvrosiadis, I., & Botsoglou, N. extracts: Application in freeze stored meat dumplings. Zastosowanie Ekstrakt w Z
(2007). The inhibitory potential of feed supplementation with rosemary and/or Miłorzębu Dwuklapowego Jako Przeciwutleniaczy W Pierogach Mięsnych
alpha-tocopheryl acetate on microbial growth and lipid oxidation of turkey breast Przechowywanych W Warunkach Zamrażalniczych., 9, 161–170.
during refrigerated storage. LWT-Food Science and Technology, 40, 331–337. Kobus-Cisowska, J., Flaczyk, E., Rudzińska, M., & Kmiecik, D. (2014). Antioxidant proper-
Halliwell, B., Rafter, J., & Jenner, A. (2005). Health promotion by flavonoids, tocopherols, ties of extracts from Ginkgo biloba leaves in meatballs. Meat Science, 97, 174–180.
tocotrienols, and other phenols: Direct or indirect effects? Antioxidant or not? The Kong, B., Peng, X., Xiong, Y. L., & Zhao, X. (2012). Protection of lung fibroblast MRC-5 cells
American Journal of Clinical Nutrition, 81(1), 268S–276S. against hydrogen peroxide-induced oxidative damage by 0.1–2.8 kDa antioxidative
Han, J., & Rhee, K. S. (2005). Antioxidant properties of selected Oriental non-culinary/ peptides isolated from whey protein hydrolysate. Food Chemistry, 135, 540–547.
nutraceutical herb extracts as evaluated in raw and cooked meat. Meat Science, 70, Kong, B., Zhang, H., & Xiong, Y. L. (2010). Antioxidant activity of spice extracts in a lipo-
25–33. some system and in cooked pork patties and the possible mode of action. Meat
Hassan, O., & Fan, L. S. (2005). The anti-oxidation potential of polyphenol extract from Science, 85, 772–778.
cocoa leaves on mechanically deboned chicken meat (MDCM). LWT - Food Science Krinsky, N. I. (1992). Mechanism of action of biological antioxidants. Experimental Biology
and Technology, 38, 315–321. and Medicine, 200, 248–254.
Hercberg, S., Galan, P., Preziosi, P., Bertrais, S., Mennen, L., Malvy, D., ... Briancon, S. Kumar, Y., Yadav, D. N., Ahmad, T., & Narsaiah, K. (2015). Recent trends in the use of nat-
(2004). The SU.VI.MAX study: A randomized, placebo-controlled trial of the ural antioxidants for meat and meat products. Comprehensive Reviews in Food Science
health effects of antioxidant vitamins and minerals. Archives of Internal and Food Safety, 14, 796–812.
Medicine, 164, 2335–2342. Lee, S. K., Mei, L., & Decker, E. A. (1997). Influence of sodium chloride on antioxidant en-
Hercberg, S., Preziosi, P., Briançon, S., Galan, P., Triol, I., Malvy, D., ... Favier, A. (1998). A pri- zyme activity and lipid oxidation in frozen ground pork. Meat Science, 46, 349–355.
mary prevention trial using nutritional doses of antioxidant vitamins and minerals in Li, X., Han, L., & Chen, L. (2008). In vitro antioxidant activity of protein hydrolysates pre-
cardiovascular diseases and cancers in a general population: The SU.VI.MAX study— pared from corn gluten meal. Journal of the Science of Food and Agriculture, 88,
Design, methods, and participant characteristics. Controlled Clinical Trials, 19, 1660–1666.
336–351. Liu, G., & Xiong, Y. L. (2000). Electrophoretic pattern, thermal denaturation, and in vitro
Hipkiss, A. R., Preston, J. E., Himswoth, D. T. M., Worthington, V. C., & Abbot, N. J. (1997). digestibility of oxidized myosin. Journal of Agricultural and Food Chemistry, 48,
Protective effects of carnosine against malondialdehyde-induced toxicity towards 624–630.
cultured rat brain endothelial cells. Neuroscience Letters, 238, 135–138. Loizzo, M. R., Tundis, R., Menichini, F., & Duthie, G. (2015). Anti-rancidity effect of es-
Hyson, D. A. (2011). A comprehensive review of apples and apple components and their sential oils, application in the lipid stability of cooked turkey meat patties and
relationship to human health. Advances in Nutrition: An International Review Journal, potential implications for health. International Journal of Food Science and
2, 408–420. Nutrition, 66, 50–57.
116 J. Jiang, Y.L. Xiong / Meat Science 120 (2016) 107–117

Lund, M. N., Luxford, C., Skibsted, L. H., & Davies, M. J. (2008). Oxidation of myosin by Sante-Lhoutellier, V., Aubry, L., & Gatellier, P. (2007). Effect of oxidation on in vitro digest-
haem proteins generates myosin radicals and protein cross-links. Biochemical ibility of skeletal muscle myofibrillar proteins. Journal of Agricultural and Food
Journal, 410, 565–574. Chemistry, 55, 5343–5348.
Lynch, M. P., Kerry, J. P., Buckley, D. J., Faustman, C., & Morrissey, P. A. (1999). Effect of di- Sebranek, J. G., Sewalt, V. J. H., Robbins, K. L., & Houser, T. A. (2005). Comparison of a nat-
etary vitamin E supplementation on the colour and lipid stability of fresh, frozen and ural rosemary extract and BHA/BHT for relative antioxidant effectiveness in pork sau-
vacuum-packaged beef. Meat Science, 52, 95–99. sage. Meat Science, 69, 289–296.
Ma, Y. Y., Xiong, Y. L., Zhai, J., Zhu, H., & Dziubla, T. (2010). Fractionation and evaluation of Serrano, R., Jordan, M. J., & Banon, S. (2014). Use of dietary rosemary extract in ewe and
radical-scavenging peptides from in vitro digests of buckwheat protein. Food lamb to extend the shelf life of raw and cooked meat. Small Ruminant Research,
Chemistry, 118, 582–588. 116, 144–152.
McAfee, A. J., McSorley, E. M., Cuskelly, G. J., Moss, B. W., Wallace, J. M., Bonham, M. P., & Shabbir, M. A., Raza, A., Anjum, F. M., Khan, M. R., & Suleria, H. A. R. (2015). Effect
Fearon, A. M. (2010). Red meat consumption: An overview of the risks and benefits. of thermal treatment on meat proteins with special reference to heterocyclic
Meat Science, 84, 1–13. aromatic amines (HAAs). Critical Reviews in Food Science and Nutrition, 55,
Melo, A., Viegas, O., Petisca, C., Pinho, O., & Ferreira, I. M. P. L. V. O. (2008). Effect of beer/ 82–93.
red wine marinades on the formation of heterocyclic aromatic amines in pan-fried Shah, M. A., Bosco, S. J. D., & Mir, S. A. (2014). Plant extracts as natural antioxidants in
beef. Journal of Agricultural and Food Chemistry, 56, 10625–10632. meat and meat products. Meat Science, 98, 21–33.
Mendis, E., Rajapakse, N., & Kim, S. K. (2005). Antioxidant properties of a radical- Shahidi, F., Janitha, P. K., & Wanasundara, P. D. (1992). Phenolic antioxidants. Critical
scavenging peptide purified from enzymatically prepared fish skin gelatin hydroly- Reviews in Food Science and Nutrition, 32, 67–103.
sate. Journal of Agricultural and Food Chemistry, 53, 581–587. Sharafati-Chaleshtori, R., Rokni, N., Rafieian-Kopaei, M., Drees, F., & Salehi, E. (2015). An-
Meyer, F., Galan, P., Douville, P., Bairati, I., Kegle, P., Bertrais, S., ... Hercberg, S. (2005). An- tioxidant and antibacterial activity of basil (Ocimum basilicum l.) essential oil in beef
tioxidant vitamin and mineral supplementation and prostate cancer prevention in burger. Journal of Agricultural Science and Technology, 17, 817–826.
the SU.VI.MAX trial. International Journal of Cancer, 116, 182–186. Shi, J., Yu, J., Pohorly, J. E., & Kakuda, Y. (2003). Polyphenolics in grape seeds—Biochemis-
Min, B., & Ahn, D. U. (2005). Mechanism of lipid peroxidation in meat and meat prod- try and functionality. Journal of Medicinal Food, 6, 291–299.
ucts — A review. Food Science and Biotechnology, 14(1), 152–163. Shin, H. -S., Strasburg, G. M., & Gray, J. I. (2002). A model system study of the inhibition of
Mine, Y., Li-Chan, E. C. Y., & Jiang, B. (2010). Biologically active food proteins and peptides heterocyclic aromatic amine formation by organosulfur compounds. Journal of
in health: An overview. In Y. Mine, E. C. Y. Li-Chan, & B. Jiang (Eds.), Bioactive proteins Agricultural and Food Chemistry, 50, 7684–7690.
and peptides as functional foods and neutraceuticals (pp. 5–11). Hoboken, NJ, U.S.A.: Soladoye, O. P., Juárez, M. L., Aalhus, J. L., Shand, P., & Estévez, M. (2015). Protein oxidation
Wiley-Blackwell. in processed meat: Mechanisms and potential implications on human health.
Negre-Salvayre, A., Coatrieux, C., Ingueneau, C., & Salvayre, R. (2008). Advanced lipid per- Comprehensive Reviews in Food Science and Food Safety, 14, 106–122.
oxidation end products in oxidative damage to proteins. Potential role in diseases and Soladoye, P. O., Shand, P. J., Aalhus, J. L., Gariepy, C., & Juarez, M. (2015). Review: Pork belly
therapeutic prospects for the inhibitors. British Journal of Pharmacology, 153, 6–20. quality, bacon properties and recent consumer trends. Canadian Journal of Animal
Nieto, G., Castillo, M., Xiong, Y. L., Alvarez, D., Payne, F. A., & Garrido, M. D. (2009). Antiox- Science, 95, 325–340.
idant and emulsifying properties of alcalase-hydrolyzed potato proteins in meat Srinivasan, S., & Hultin, H. O. (1997). Chemical, physical, and functional properties of cod
emulsions with different fat concentrations. Meat Science, 83, 24–30. proteins modified by a nonenzymic free-radical-generating system. Journal of
Nieto, G., Diaz, P., Banon, S., & Garrido, M. D. (2010). Effect on lamb meat quality of Agricultural and Food Chemistry, 45, 310–320.
including thyme (Thymus zygis ssp gracilis) leaves in ewes' diet. Meat Science, Stadtman, E. R. (2006). Protein oxidation and aging. Free Radical Research, 40,
85, 82–88. 1250–1258.
Nieto, G., Estrada, M., Jordán, M. J., Garrido, M. D., & Bañón, S. (2011). Effects in ewe diet of Sun, W., & Xiong, Y. L. (2015). Stabilization of cooked cured beef color by radical-
rosemary by-product on lipid oxidation and the eating quality of cooked lamb under scavenging pea protein and its hydrolysate. LWT-Food Science and Technology, 61,
retail display conditions. Food Chemistry, 124, 1423–1429. 352–358.
O'Grady, M. N., Maher, M., Troy, D. J., Moloney, A. P., & Kerry, J. P. (2006). An assessment of Tang, C. B., Zhang, W. G., Dai, C., Li, H. X., Xu, X. L., & Zhou, G. H. (2015). Identification and
dietary supplementation with tea catechins and rosemary extract on the quality of quantification of adducts between oxidized rosmarinic acid and thiol compounds by
fresh beef. Meat Science, 73, 132–143. UHPLC-LTQ-orbitrap and MALDI-TOF/TOF tandem mass spectrometry. Journal of
Oz, F., & Kaya, M. (2011). The inhibitory effect of black pepper on formation of heterocy- Agricultural and Food Chemistry, 63, 902–911.
clic aromatic amines in high-fat meatball. Food Control, 22, 596–600. Thiansilakul, Y., Benjakul, S., & Shahidi, F. (2007). Antioxidative activity of protein hydro-
Park, D., & Xiong, Y. L. (2007). Oxidative modification of amino acids in porcine myofibril- lysate from round scad muscle using alcalase and flavourzyme. Journal of Food
lar protein isolates exposed to three oxidizing systems. Food Chemistry, 103, 607–616. Biochemistry, 31, 266–287.
Peña-Ramos, E. A., & Xiong, Y. L. (2001). Antioxidative activity of whey protein hydroly- Thongtan, K., Toma, R. B., Reiboldt, W., & Daoud, A. Z. (2005). Effect of rosemary extract on
sates in a liposomal system. Journal of Dairy Science, 84, 2577–2583. lipid oxidation and sensory evaluation of frozen, precooked beef patties. Foodservice
Petersen, D. R., & Doorn, J. A. (2004). Reactions of 4-hydroxynonenal with proteins and Research International, 16, 93–104.
cellular targets. Free Radical Biology and Medicine, 37, 937–945. Toldra, F. (2010). Handbook of meat processing. Hoboken, New Jersey, USA: John Wiley &
Phillips, A. L., Faustman, C., Lynch, M. P., Govoni, K. E., Hoagland, T. A., & Zinn, S. A. (2001). Sons.
Effect of dietary α-tocopherol supplementation on color and lipid stability in pork. Turesky, R. J. (2007). Formation and biochemistry of carcinogenic heterocyclic aromatic
Meat Science, 58, 389–393. amines in cooked meats. Toxicology Letters, 168, 219–227.
Pihlanto, A., Akkanen, S., & Korhonen, H. J. (2008). ACE-inhibitory and antioxidant prop- Valenzuela, A., Sanhueza, J., & Nieto, S. (2003). Natural antioxidants in functional foods:
erties of potato (Solanum tuberosum). Food Chemistry, 109, 104–112. From food safety to health benefits. Grasas y Aceites, 54, 295–303.
Puangsombat, K., Jirapakkul, W., & Smith, J. S. (2011). Inhibitory activity of Asian spices on Velioglu, Y. S., Mazza, G., Gao, L., & Oomah, B. D. (1998). Antioxidant activity and total
heterocyclic amines formation in cooked beef patties. Journal of Food Science, 76, phenolics in selected fruits, vegetables, and grain products. Journal of Agricultural
T174–T180. and Food Chemistry, 46, 4113–4117.
Radecki, S. V., Juhl, M. R., & Miller, E. R. (1988). Fumaric and citric acids as feed additives in Vitaglione, P., & Fogliano, V. (2004). Use of antioxidants to minimize the human health
starter pig diets: Effect on performance and nutrient Balance1. Journal of Animal risk associated to mutagenic/carcinogenic heterocyclic amines in food. Journal of
Science, 66, 2598–2605. Chromatography B, 80, 189–199.
Raghavan, S., & Kristinsson, H. G. (2008). Antioxidative efficacy of alkali-treated tilapia Vitaglione, P., Monti, S. M., Ambrosino, P., Skog, K., & Fogliano, V. (2002). Carotenoids from
protein hydrolysates: A comparative study of five enzymes. Journal of Agricultural tomatoes inhibit heterocyclic amine formation. European Food Research and Technol-
and Food Chemistry, 56, 1434–1441. ogy, 215, 108–113.
Rather, S. A., Akhter, R., Masoodi, F. A., Gani, A., & Wani, S. M. (2015). Utilization of Wang, D., Wang, L., Zhu, F., Zhu, J., Chen, X., Zou, L., & Saito, M. (2008). In vitro and in vivo
apple pomace powder as a fat replacer in goshtaba: A traditional meat product studies on the antioxidant activities of the aqueous extracts of Douchi (a traditional
of Jammu and Kashmir, India. Journal of Food Measurement and Characterization, 9, Chinese salt-fermented soybean food). Food Chemistry, 107, 1421–1428.
389–399. Wang, L. L., & Xiong, Y. L. (2005). Inhibition of lipid oxidation in cooked beef patties by
Rey, A. I., Hopia, A., Kivikari, R., & Kahkonen, M. (2005). Use of natural food/plant extracts: hydrolyzed potato protein is related to its reducing and radical scavenging ability.
Cloudberry (Rubus chamaemorus), beetroot (Beta vulgaris “vulgaris”) or willow herb Journal of Agricultural and Food Chemistry, 53, 9186–9192.
(Epilobium angustifolium) to reduce lipid oxidation of cooked pork patties. LWT - Wang, L. L., & Xiong, Y. L. (2008). Inhibition of oxidant-induced biochemical changes of
Food Science and Technology, 38, 363–370. pork myofibrillar protein by hydrolyzed potato protein. Journal of Food Science, 73,
Rock, C. L., Jacob, R. A., & Bowen, P. E. (1996). Update on the biological characteristics of C482–C487.
the antioxidant micronutrients: Vitamin C, vitamin E, and the carotenoids. Journal Wenk, C. (2000). Recent advances in animal feed additives such as metabolic modifiers,
of the American Dietetic Association, 96, 693–702. antimicrobial agents, probiotics, enzymes and highly available minerals. Asian Aus-
Rossini, K., Noreña, C. P. Z., Cladera-Olivera, F., & Brandelli, A. (2009). Casein peptides with tralasian Journal of Animal Sciences, 13, 86–95.
inhibitory activity on lipid oxidation in beef homogenates and mechanically deboned Williams, C. M. (2000). Dietary fatty acids and human health. Annales de Zootechnie, 49,
poultry meat. LWT - Food Science and Technology, 42, 862–867. 165–180.
Roubal, W. T., & Tappel, A. L. (1966). Damage to proteins, enzymes, and amino acids by Xiong, Y. L. (2000). Protein oxidation and implications for muscle food quality. In E. A.
peroxidizing lipids. Archives of Biochemistry and Biophysics, 113, 5–8. Decker, C. L. Faustman, & C. J. Lopez-Bote (Eds.), Antioxiants in muscle foods
Saiga, A., Tanabe, S., & Nishimura, T. (2003). Antioxidant activity of peptides obtained (pp. 85–111). New York, NY, USA: John Wiley & Sons.
from porcine myofibrillar proteins by protease treatment. Journal of Agricultural and Xiong, Y. L. (2010). Antioxidant peptides. In Y. Mine, E. C. Y. Li-Chan, & B. Jiang (Eds.), Bio-
Food Chemistry, 51, 3661–3667. active proteins and peptides as functional foods and neutraceuticals (pp. 29–42). Hobo-
Saleh, N. T., & Ahmed, Z. S. (1998). Impact of natural sources rich in provitamin a on ken, NJ, USA: Wiley-Blackwell.
cooking characteristics, color, texture and sensory attributes of beef patties. Meat Xiong, Y. L., & Decker, E. A. (1995). Alterations of muscle protein functionality by oxidative
Science, 50, 285–293. and antioxidative processes. Journal of Muscle Foods, 6, 139–160.
 J. Jiang, Y.L. Xiong / Meat Science 120 (2016) 107–117 117

Xiong, Y. L., Blanchard, S. P., Ooizumi, T., & Ma, Y. (2010). Hydroxyl radical and ferryl- Youdim, K. A., & Deans, S. G. (2000). Effect of thyme oil and thymol dietary supplementa-
generating systems promote gel network formation of myofibrillar protein. Journal tion on the antioxidant status and fatty acid composition of the ageing rat brain.
of Food Science, 75, C215–C221. British Journal of Nutrition, 83, 87–93.
Xiong, Y. L., Park, D., & Ooizumi, T. (2009). Variation in the cross-linking pattern of porcine Zamora, R., Alcon, E., & Hidalgo, F. J. (2014). Ammonia and formaldehyde participate in
myofibrillar protein exposed to three oxidative environments. Journal of Agricultural the formation of 2-amino-1-methyl-6-phenylimidazo 4,5-b pyridine (PhIP) in addi-
and Food Chemistry, 57, 153–159. tion to creati(ni)ne and phenylacetaldehyde. Food Chemistry, 155, 74–80.
Xu, M., Shangguan, X., Wang, W., & Chen, J. (2007). Antioxidative activity of hen egg ov- Zembayashi, M., Lunt, D. K., & Smith, S. B. (1999). Dietary tea reduces the iron content of
albumin hydrolysates. Asia Pacific Journal of Clinical Nutrition, 16(Suppl. 1), 178–182. beef. Meat Science, 53, 221–226.
Yang, C. S., & Landau, J. M. (2000). Effects of tea consumption on nutrition and health. The Zhang, Q., & Ye, M. (2009). Chemical analysis of the Chinese herbal medicine Gan-Cao
Journal of Nutrition, 130, 2409–2412. (licorice). Journal of Chromatography A, 1216, 1954–1969.
Yang, J., & Xiong, Y. L. (2015). Inhibition of lipid oxidation in oil-in-water emulsions by Zhang, Y. W., Luo, H. L., Liu, K., Jia, H. N., Chen, Y., & Wang, Z. Z. (2015). Antioxidant effects
interface-adsorbed myofibrillar protein. Journal of Agricultural and Food Chemistry, of liquorice (Glycyrrhiza uralensis) extract during aging of longissimus thoracis mus-
63, 8896–8904. cle in Tan sheep. Meat Science, 105, 38–45.
Yang, H., Meng, P., Xiong, Y. L., Ma, L., Wang, C., & Zhu, Y. (2013). Oxidation in HiOx- Zhang, X., Xiong, Y. L., Chen, J., & Zhou, L. (2014). Synergy of licorice extract and pea pro-
packaged pork longissimus muscle predisposes myofibrillar and sarcoplasmic pro- tein hydrolysate for oxidative stability of soybean oil-in-water emulsions. Journal of
teins to N-nitrosamine formation in nitrite-curing solution. Meat Science, 95, Agricultural and Food Chemistry, 62, 8204–8213.
465–471. Zheng, W., & Wang, S. Y. (2003). Oxygen radical absorbing capacity of phenolics in blue-
Yoo, K. M., Lee, C. H., Lee, H., Moon, B., & Lee, C. Y. (2008). Relative antioxidant and berries, cranberries, chokeberries, and lingonberries. Journal of Agricultural and Food
cytoprotective activities of common herbs. Food Chemistry, 106, 929–936. Chemistry, 51, 502–509.