Antioxidants in Muscle Foods

1. Introduction

Lipid oxidation in meat generates products, including hydroperoxides, free radicals, and secondary oxidation products such as aldehydes and ketones that negatively impact flavor, appearance, and protein function. The shelf-life of muscle foods can be restricted by rancidity development resulting from volatile secondary products generated by lipid oxidation (Bekhit et al., 2013). The color of the meat is another indicator that consumers use to determine meat quality. The red color of meat originates primarily from myoglobin. Lipid oxidation products can also impact shelf-life by reacting with myoglobin resulting in an acceleration of discoloration and thus a reduction in shelf-life. 

Antioxidants strategies can help decrease lipid oxidation rates by a variety of mechanisms. These include scavenging of free radicals, chelation of metals, inactivation of reactive oxygen species and reduction of oxygen concentrations. Muscle naturally contains antioxidants, but these are often not adequate to protect the quality, and processing techniques can decrease their concentrations and/or activities. Since lipid oxidation is essential to the quality and shelf-life of muscle foods, additional antioxidant strategies such as dietary interventions, food additives and packaging are often needed to decrease food waste and minimize economic loss.

2. Endogenous antioxidants in muscle foods – inherent oxidative stability

Skeletal muscle contains endogenous antioxidants, including 1) free radical scavengers (e.g., tocopherols, glutathione and ascorbate), 2) enzymes (e.g. superoxide dismutase, glutathione peroxidase and catalase), 3) non-enzyme proteins, and 4) metal chelators (e.g. metal binding proteins and peptides) that provide inherent antioxidative protection to all muscle foods (Elias et al., 2008). The concentration of these endogenous antioxidant varies between muscle types and animal species and can be influenced by the inclusion of antioxidants into animal diets.

2.1 Tocopherols

Tocopherol is a natural free radical scavenger present in all muscle cell membranes. Tocopherol has several isoforms such as a, b, g, and d but a-tocopherol is primarily found in muscle tissue due to the preferred transport of the a isoform from the liver (Brigelius‐Flohé and Traber 1999). Since lipid oxidation in muscle foods initially occurs in the cell membrane, dietary α-tocopherol is a very effective antioxidant. The concentration of α-tocopherol is dependent on animal species, muscle type and diet (see more on diet below).

2.2 Antioxidant enzymes

Superoxide dismutase (SOD), glutathione peroxidase (GSH-Px) and catalase (Cat) are the most common antioxidant enzymes in muscle foods (Petron et al., 2007). They are important to the antioxidant defense of both living muscle tissue as well as muscle foods.

Superoxide anion promotes lipid oxidation by forming perhydroxyl radicals and reducing metals into their more prooxidative state. SOD inactivates superoxide anion by converting it to oxygen and hydrogen peroxide (pathway 1).:

(1) 2 O2 + 2 H+ → O2 +H2O2

Hydrogen peroxide can be formed in muscle by several pathways, including the action of SOD and fatty acid hydroperoxides are formed during lipid oxidation reactions. Since both hydrogen peroxide and fatty acid hydroperoxides can be decomposed by metals into damaging free radicals. CAT and GSH-Px are found in biological tissues to remove these potentially damaging reactive compounds. CAT catalyzes the conversion of hydrogen peroxide to water and oxygen (pathway 2). 

(2) H2O2 → 2 H2O + O2

GSH-Px utilizes selenium and reduced glutathione (GSH) to decompose both fatty acid hydroperoxides and hydrogen peroxide to water or hydroxyl fatty acids (pathway 3) (Elias et al., 2008; Petron et al., 2007). These two pathways also oxidize two glutathiones to a glutathione dimer (GSSG):

(3) H2O2 + 2 GSH → 2 H2O+ GSSG or LOOH + 2 GSH → LOH + 2 H2O + GSSG

The levels of endogenous antioxidant enzymes mainly depend on genetics and muscle type. The content activity of GSH-PX in muscle decreases in the following order: beef > turkey thigh > turkey breast > pork, whereas CAT activity is in the order of beef > pork > turkey thigh > turkey breast (Lee et al., 1996; Mei et al., 1994).

Common meat processing operations may lead to the inactivation of antioxidant enzymes. For example, the addition of salt may inhibit enzyme activities (Gheisari & Motamedi, 2010; Mariutti & Bragagnolo, 2017). In addition, cooking (≥70°C) causes the inactivation of GSH-Px and Cat, but has little impact on the activity of SOD (Lee et al., 1996).

2.3 Proteins and Peptides

Both endogenous protein and peptides can work as antioxidants in muscle foods by scavenging free radicals and chelating metals (Elias et al., 2008). Many proteins in the living muscle do not have the primary function of antioxidant protection, but in muscle foods they can make important contributions to the total endogenous antioxidant capacity. Proteins can scavenge radicals via amino acids such as cysteine, tyrosine, phenylalanine, and tryptophan. Metal chelation can occur with proteins that specifically bind metals (e.g., ferritin) or by non-specific binding through negatively charged amino acids. Carnosine and anserine are two endogenous histidine-related dipeptides with antioxidative activity from copper chelation and free radical scavenging (Fu et al., 2009; Kohen et al., 1988). The order of carnosine content concentration in raw meat from different species was pork loin> beef fillet> chicken breast> turkey breast> rabbit hindleg. In contrast, the order of anserine was turkey breast> chicken breast> rabbit hindleg> beef fillet> pork loin (Peiretti et al., 2011).

3. Diet approaches to increase antioxidants

The animal diet is an effective strategy for increasing the antioxidant capacity of muscle foods (Decker et al., 2010).

3.1 a-Tocopherol  

Dietary supplementation of α-tocopherol is an effective method to decrease lipid oxidation in muscle foods because it utilizes biological pathways to position the a-tocopherol directly into the cell membrane where oxidation is most prevalent. Though exogenous addition of tocopherol results in higher concentration compared to dietary supplementation, dietary supplementation of tocopherol is more effective than exogenous addition in beef and turkey (Higgins et al. 1998).

For example, dietary α-tocopherol that results in a concentration of 0.04 mg a-tocopherol/kg muscle is more effective than postmortem addition of a-tocopherol at a concentration of 500 mg a-tocopherol /kg muscle in  beef (Angelo et al. 1990; Faustman et al. 1989). Dietary supplementation has been shown to effectively delay lipid oxidation in beef (Sanders et al. 1997; Zerby et al. 1999), turkey (Marusich et al. 1975), fish (Jones and Carton 2015), pork (Monahan et al. 1992), and lamb (González-Calvo et al. 2015). An additional advantage of a-tocopherol supplementation is that it decreases the formation of lipid oxidation aldehydes that can cause myoglobin color to decay. Arnold and coworkers (1993) concluded 3.3 µg of α-tocopherol/g beef was sufficient to enhance lipid and color stability in beef. This level of a-tocopherol could be obtained by feeding 1,300 IU of a-tocopherol/day for 44 days.  

Tocopherol concentration varies between species with turkey < chicken < pork < beef < mutton (Leonhardt et al. 1997; Wilson, Pearson, and Shorland 1976). In pork and poultry, a-tocopherol supplementation inhibited lipid oxidation but did not protect myoglobin color stability (Houben, Eikelenboom, and Hoving-Bolink 1998). In chicken breast muscle, 400 mg α-tocopherol per kg feed for 8 weeks was sufficient to inhibit lipid oxidation in chicken breast meat while 400-600 mg α-tocopherol/kg feed for 8 weeks is required for inhibition of lipid oxidation in chicken thigh meat (Galvin, Morrissey, and Buckley 1998). Turkey dietary supplementation of 200 mg α-tocopherol/kg feed for 4 weeks inhibited lipid oxidation more effectively in breast than thigh muscle (Govaris et al. 2004). Thigh muscle is thought to require more tocopherol than breast because it contains higher amounts of polyunsaturated fatty acids, iron and heme-proteins .   

3.2 Plant Feed Additives

Many plants contain phenolic compounds that can scavenge free radicals. Plant feed additives (PFA) high in antioxidants, such as plant extracts, essential oils, and food production by-products, have also been shown to increase the oxidative stability of meats when included in animal diets. 

Inclusion of PFAs high in antioxidants, such as rosemary extracts, oregano oil and olive leaves, have been shown to increase the oxidative stability of muscle foods (Tsiplakou et al., 2021). For example, dietary oregano oil can also delay lamb meat's lipid oxidation during storage (Simitzis et al., 2008). The addition of rosemary extract to lamb diets was also found to inhibit discoloration, rancidity, and flavor deterioration (Serrano et al., 2014). However, dietary supplementation of rosemary extracts was less effective than dietary a-tocopherol. The rosemary extracts also had antimicrobial activity, making it a promising multifunctional feed additive for animals (Ortuño et al., 2015, 2017).

4. Exogenous antioxidant additives in muscle foods

Both natural and synthetic antioxidants additives have traditionally been used to increase muscle foods' shelf-life. However, increased consumer concerns of synthetic antioxidants have resulted in their decreased use. Hence, natural antioxidant additives are now more common because of consumer preference for cleaner labels.

4.1 Exogenous tocopherols  

Both a- and mixed tocopherol isomers (a by-product of oil refining) have been shown to inhibit lipid oxidation in beef, pork, chicken, turkey, and fish.  In general, mixed tocopherol isomers are better than a-tocopherol in beef. Wills et al. reported 300 ppm γ-tocopherol dissolved in ethanol carrier was sufficient to inhibit lipid oxidation in ground beef. Addition of 300ppm a-tocopherol to minced beef inhbited lipid oxidation to the same level as 3000 ppm indicating that higher levels are not more effective (O’Grady et al. 2000). Tocopherol effectiveness is dependent on animal species. a-Tocopherol (300 ppm) was  more effective in cooked beef than chicken. This is likely due ot thie higher polyunsaturated fatty acid composition chicken (Tang et al. 2001).  

4.2 Rosemary 

Rosemary essential oil is high in carnosol and carnosic acid which are strong free radical scavengers. However, these extracts also contain monoterpenes that are strong flavor molecules making them unacceptable in some food applications.  For this reason, rosemary extract for use as antioxidants are sometimes processed to remove some of the flavor compounds.  

Rosemary extract (3000 ppm) inhibited both lipid and myoglobin oxidation in ground beef (Balentine et al. 2006). In addition, rosemary (2500 ppm) was effective at decreasing the pro-oxidant effects of 2% NaCl in both raw and cooked beef (Han and Rhee 2005).

Addition of 250 ppm and 500 ppm but not 100 ppm of rosemary extract in cooked turkey significantly inhibited lipid oxidation throughout the 13 days of storage (Yu et al. 2002).

The effectiveness of rosemary extract in chicken was compared to BHA. Rosemary extract (480 ppm) inhibited lipid oxidation in frozen chicken for 120 days showing similar results to the use of 20 ppm BHA (Pires et al. 2017).

Lipid oxidation inhibition was also observed in fresh and frozen pork patties with 200 to 1000 ppm rosemary extract (Mc Carthy et al. 2001). While rosemary efficiently inhibited lipid oxidation it did not increase color stability in pork patties (Haak, Raes, and De Smet 2009).

4.3 Chelators 

Chelators bind to metal prooxidants to decrease thier ability to oxidize lipids . EDTA (2%) effectively bound non-heme iron to reduce lipid oxidation in cooked beef (Gene et al. 1979). EDTA (1%) decreased lipid oxidation in raw beef and cod fillets (Angsupanich and Ledward 1998).

Phosphates used as antioxidants include monomers and mostly linear phosphate anion polymers (Huynh Bach et al., 1987; Pavlovic et al., 2021), including monosodium orthophosphate (NaH2PO4), disodium phosphate (Na2HPO4), tetrasodium pyrophosphate (Na4P2O7), sodium tripolyphosphate (Na5P3O10), Sodium hexametaphosphate ((NaPO3)n). Apolyphosphate mixture, containing sodium tripolyphosphate, tetrasodium pyrophosphate and disodium diphosphate, can decrease the rancidity flavor and prevent oxidative deterioration in precooked chicken (Farr & May, 1970; Landes, 1972). Sodium tripolyphosphate added to ground pork can significantly prevent the lipid oxidation caused by cooking (Michael (Michael Paul, 1991). Furthermore, sodium tripolyphosphate has antioxidation function in uncooked ground turkey and ground beef (Calvert & Decker, 1992; DECKER & CRUM, 1991).

4.3.1 Citric acid

Citric acid is a chelator that binds with metals to inhibit lipid oxidation. The addition of 3.84 g citric acid per kg cooked beef inhibited lipid oxidation (Ke et al. 2009). Citric acid (0.5%; w/w) also inhibits lipid oxidation in fish during 6 months of storage at -18°C (Rostamzad et al. 2011).  

Not only does citric acid inhibit lipid oxidation, but it is also used to inhibit commo pathogenic bacteria in pork sausage (Scannell et al. 1997).

4.4 Nitrite

Nitrite in cured meats have multiple purposes: 1) gives cured meat the characteristic pink color and unique flavor 2) prevent spoilage and C. botulinum 3) Inhibit Fenton reactions by the formation of nitric oxide complexes with iron 4) stabilize unsaturated lipids in membranes 5) protects meat from nucleotide degradation of irradiation

156 mg nitrite per kg of chicken and beef inhibited lipid oxidation and the development of warmed over flavors (Gene et al. 1979). The concern for using nitrite arises in the formation of nitrosamine, which is a carcinogen. This drives for a substitute of nitrite as curing agent. The most common substitute is celery extract and is most widely used for nitrate substitute because it is or natural source. Celery extract are naturally high in nitrate and can be converted into nitrite. Sinder et al. demonstrated the effectiveness celery powder in inhibition of lipid oxidation at 0.2% in ham and sensory attributes were similar to nitrite. The concentration of 0.35% celery powder yielded higher vegetable aroma and is not an ideal concentration for ham.

S-Nitroso-N-acetylcysteine (NAC-SNO) was shown to have better antioxidant effects compared to nitrite in cooked turkey meat after 1 month of storage at 1.0 mM, 1.5 mM, and 2.5 mM. The addition of ascorbic acid (1.14:1 molar ratio) to nitrite and NAC-SNO increased antioxidant effects (Kanner et al. 2019). NAC-SNO is a potential replacement for nitrite with fewer nitrosamines produced during stomach digestion (Shpaizer et al. 2018).

Shahidi et al. proposed to use cooked cured-meat pigment (CCMP) as colorants in nitrite-free products. Heme is extracted from animal red blood cells and added to nitric oxide. CCMP was applied to pork at 1.2 ppm levels and the color was visually similar to nitrite cured pork (Pegg and Shahidi 1997).

4.5 Synthetic antioxidants

The synthetic free radical scavenging antioxidants, butylated hydroxyanisole (BHA), butylated hydroxytoluene (BHT), tert-butylhydroquinone (TBHQ), and propyl gallate (PG) have been used in both raw and cooked meat to inhibit lipid oxidation.   Synthetic antioxidants have been shown to be effective in pork, beef and sheep (Formanek et al., 2001; Jayathilakan et al., 2007). BHA use in foods is restricted by Proposition 65 in California due to its potential carcinogenicity (Felter et al., 2021), therefore its use in muscle foods in the U.S.A. is very uncommon.

5. Control of Oxidation by Packaging

Plastic overwraps (air-permeable) are a common method to package raw muscle foods. Since oxygen is a substrate for lipid oxidation, packaging techniques such as vacuum and modified atmosphere are often used to decrease oxidative rancidity and extend shelf life (McMillin, 2017).

5.1 Vacuum and Modified Atmosphere Packaging

Vacuum packaging is very effective at decreasing lipid oxidation in meats, since it can remove most of the oxygen in the product (Ahn et al., 1993; Veberg et al., 2006; Xiao et al., 2011). However, vacuum packaging converts red oxymyoglobin to purple deoxymyoglobin and this color change is sometimes unacceptable to consumers.

Modified atmosphere packaging (MAP) of muscle foods uses a combination of oxygen, nitrogen, and carbon dioxide to stabilize color, inhibit lipid oxidation and decrease microbial growth (McMillin, 2017). Low headspace O2 concentration (40%) can minimize oxidative deterioration while keeping myoglobin in the red oxygenated state (Li et al., 2022; McMillin, 2008). Low headspace CO2 (30%) concentration is more effective in enhancing oxidation stability and discoloration than high (50–70%) concentration in minced beef (Esmer et al., 2011).

5.2 Future antioxidant packaging

Both vacuum and MAP cannot always completely remove oxygen because of pockets of residual oxygen and oxygen within the muscle tissue.  In addition, some oxygen is often needed to produce the positive color of oxymyoglobin. Active packaging (AP) systems, which utilizes antioxidants impregnated into the packaging materials present a possible technology to further enhance oxidative stability (Ahmed et al., 2017; McMillin, 2017). For example, rosemary extract impregnated packaging protected pork patties from high pressure-induced lipid oxidation more effectively than vacuum packaging or oxygen scavenger packaging (Bolumar et al., 2016). A low-density polyethylene film with butylated hydroxytoluene (BHT-LDPE) was reported to inhibit lipid oxidation as well as minimize protein damage in fresh sierra fish (Torres-Arreola et al., 2007). Contini et al. (Contini et al., 2014) reported that a citrus extract-coated tray could delay lipid oxidation in cooked turkey meat.  

6. Conclusion 

An effective strategy to prevent lipid oxidation in uncooked muscle foods is to feed animals dietarytocopherols. Exogenous addition of various antioxidants such as tocopherols, rosemary extracts, citric acid, nitrite, chelators, and synthetic antioxidants have also been demonstrated to be effective and are commonly applied in muscle foods. Furthermore, packaging development also provides new opportunities to help control oxidation in muscle foods.


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