Oxidation of Muscle Foods

The Authors: Xiaoyan Hu, Jianfei Shen and Eric A. Decker, Department of Food Science, University of Massachusetts, Amherst, MA 01003, USA

1. Why is lipid oxidation is a problem in muscle foods

Lipid oxidation is one of the main non-microbial cause of quality deterioration in meat and meat products (Lorenzo & Gomez, 2012; Min & Ahn, 2005). Lipid oxidation results in loss of sensory quality in muscle foods as it does in other foods. 

Many muscle foods are high in prooxidant metals which can make these products very susceptible to lipid oxidation. These include free iron, iron bound to protein and heme-iron from myoglobin and hemoglobin (George & Stratmann, 1954; Joseph Kanner, Hazan, & Doll, 1988).  The processing and formulation of muscle foods can also increase lipid oxidation rates such as cooking that can release protein-bound iron and heme and increase their reactivity, salting which can increase iron reactivity and particle size reduction which can increase oxygen concentrations in the muscle. (Amaral, da Silva, & Lannes, 2018). Unique to muscle foods is how lipid oxidation products can also interact with the pigment myoglobin to cause loss of the desirable red color (Purrinos, Bermudez, Franco, Carballo, & Lorenzo, 2011).

2. Meat composition

A. Lipid composition

The phospholipid content of most muscle foods is typically 1% of the tissue weight (Hornstein, 1961). Triacylglycerol concentrations, which are typically much greater than phospholipid concentrations, are dependent on factors such as animal species, muscle type, muscle source used in processed meats and animal diet (Hornstein I, 1967; O’Keefe PW 1968; Kuchmak M, 1965). Despite the much lower concentration of phospholipids than triacyclglycerols, they are the major target of lipid oxidation reactions (Jane D. Love, 1971).  The high susceptibility of phospholipids to oxidation is due to their higher levels of polyunsaturated fatty acids such as arachidonic and omega-3 fatty acids and their high surface area which puts them in close contact to the prooxidants in the tissue (EI-Gharbawi, 1965). For example, Hornstein (1961) reported that unsaturated fatty acids make up 10% of the triglyceride fraction and 50% of the phospholipid fraction in beef and pork. The major difference in unsaturated fatty acids is arachidonic acid which has a concentration of 150 mg/100 g in beef and 100 mg/100 g in pork originating from the phospholipid fraction while arachidonic acid is low or absent in the triglyceride fraction (Hornstein I, 1961).     

The fatty acid composition of phospholipids in muscle foods is also dependent on animal species and muscle type. The degree of unsaturation of the fatty acids in phospholipids is in the order of trout > turkey > chicken > pork > beef (Craw Ford, 1975; Wilson, 1976; Melton 1983).  Phospholipid fatty acid composition also varies by muscle type with dark muscle having a higher amount of polyunsaturated fatty acids (Francis E. Luddy, 1970).  Phospholipid fatty acid content is also dependent on diet (Xu, 2020).

3. Prooxidants in muscle foods

A. Transition metals

Iron and copper are strong prooxidants in muscle foods. The amount of free, unbound, iron and copper are typically low in biological tissues. Most transition metals are bound to proteins such as transferrin, ferritin, or heme proteins to decrease their ability to promote lipid oxidation (Ahn, Wolfe, & Sim, 1993). Free iron and copper can interact with reducing agents such as superoxide anion, ascorbic acid and glutathione in muscle to increase their prooxidative activity. Iron and copper accelerate lipid oxidation in muscle foods by promoting the decomposition of hydrogen (Fenton reaction, reactions 1 and 2) and lipid hydroperoxides (reactions 3 and 4) to free radicals such as hydroxyl and alkoxyl radicals (J. Kanner, German, & Kinsella, 1987). The reduced states of copper and iron are stronger prooxidants than the oxidized states

Fe2+ + H2O2→ Fe3+ + HO•  + OH-   (1)

Fe3+ + H2O2→ FeO2+ + HO•  + H+   (2)

Lipid hydroperoxides react with metals in a similar to hydrogen peroxide.

Fe2+ + LOOH→ Fe2+ + LO•  + OH-   (3)

Fe3+ + LOOH→ Fe2+ + LOO•  + H+  (4)

Cu(I) decomposes hydrogen peroxide faster (k = 73 M-1s-1) than Fe(II)(k = 12.6  sM-1s-1) (Barb, Baxendale, George, & Hargrave, 1951; Letelier, Sánchez-Jofré, Peredo-Silva, Cortés-Troncoso, & Aracena-Parks, 2010; Moffett & Zika, 1987; Pham, Xing, Miller, & Waite, 2013; Thanonkaew, Benjakul, Visessanguan, & Decker, 2006). However, iron concentrations are generally higher in muscle making it a more important prooxidant (Demirezen & Uruç, 2006). For example, in anchovy, chicken and beef, iron is 12, 6 and 20 fold higher than copper, respectively (Demirezen & Uruç, 2006; Kurnaz & Filazi, 2011; Pilarczyk, 2014).

B. Myoglobin/hemoglobin induced lipid oxidation

Hemoglobin in blood and myoglobin in tissue both contain iron in a porphyrin ring know as hematin. Myoglobin is the main pigment in muscle foods. The color of myoglobin is dependent on the oxidation/reduction state of the iron in the heme and whether or not oxygen is bound to the heme group. Myoglobin is physiologically active in the deoxygenated (deoxymyoglobin, Fe(II), purple color) and oxygenated (oxymyoglobin, Fe(II), red color) states (Baron & Andersen, 2002). When the heme iron is oxidized to the ferric state, this forms metmyoglobin (brown color).  The iron in metmyoglobin can be reduced by enzymes and agents such as ascorbic acid to reform deoxymyoglobin and restore color. The ability of muscle to keep iron reduced decreases post mortem resulting in the loss of red color. 

Like free iron, hematin also promotes the decomposition of hydrogen peroxide and lipid hydroperoxides into free radicals that will accelerate lipid oxidation (reactions 5 and 6) (Carlsen, Møller, & Skibsted, 2005)

Heme-Fe(II) + H2O2 → Heme-Fe(III)  +  HO•   +  OH-   (5)

Heme-Fe(III) + H2O2 → Heme-Fe(II)  + HOO•  + H+  (6)

The metmyoglobin binds water which causes conformational changes in the protein. This protein reconfirmation can increase heme iron exposure which allow it more easy access to peroxides and thus increases it’s prooxidant activity. 

The interaction of hydrogen peroxide with metmyoglobin [Fe (III)] has also been observed to increase free radical production (J. Kanner & Harel, 1985).  This was proposed to be due to the ability of Fe(III) to react with hydrogen peroxide to form Fe(IV) which can rapidly cleave lipid hydroperoxides to peroxyl radicals (LOO·) (Everse, 1998; Kanner & Harel, 1985).  

The prooxidant activity of myoglobin is also related to the release of hematin from the protein (Grunwald & Richards, 2006). The higher affinity of myoglobin to hemin group leads to stronger binding of hemin which decreases its ability to promote lipid oxidization in muscle (Grunwald & Richards, 2006). Hematine tends to have higher affinity to mammalian myoglobin than fish.The lower affinity of hematin to myoglobin has been suggested to make a more important prooxidant in fish (Lee, Tatiyaborworntham, Grunwald, & Richards, 2015).  

4. Processing factors affect oxidation

      The processing steps in muscle food production range from slaughter to particle size reduction to formulation to cooking. The most important steps in processing that increases lipid oxidation in muscle foods are particle size reduction, addition of sodium chloride, irradiation and cooking (Ladikos D & Lougocois V., 1990, Rhee 1983, Harel & Kanner 1985, Ahn 2001)

A. Particle size reduction

After slaughter and loss of oxygen transportation, the interior of skeletal muscle becomes anaerobic.  Muscle foods are commonly cut, ground and emulsified which introduces oxygen into the tissue and increases lipid oxidation rates (Ladikos D & Lougocois V., 1990). For example, USDA recommends that frozen uncooked beef roasts and steaks have a shelf life of 4-12 months while uncooked ground beef has a shelf-life of 3-4 months.（USDA 2013）

B. Cooking

Cooking is another major factor that increases lipid oxidation rates. There are several factors by which cooking increases oxidation rates including release of protein bound metals and hematin, inactivation of antioxidant enzymes and disruption of cell membrane structure.  During the cooking process, the level of non-protein bound iron increases. Low temperature long time heating compared to high temperature heating can release more iron and promote more oxidation (Igene 1979, Rhee 1987, Harel 1988). Heating myoglobin also increases its prooxidant activity releasing hematin and by promoting the conversion of oxymyoglobin or oxyhemoglobin to metmyoglobin or methemoglobin which generates H2O2 as a by-product. (Harel and Kanner, 1985).  This H2O2 can then be decomposed into free radicals.

C. Salting

Salting is one of the most important steps in the meat industry because it solubilizes myofibrillar proteins which improves their functionality, inhibits microbial growth and provides flavor (Rhee 1999). From a lipid oxidation point of view, the concentration of NaCl would largely determine its role as prooxidant. (B. Min & D.U. Ahn, 2005). Rhee found that lipid oxidation increased at 2% NaCl concentration but no prooxidant effect was observed at 3% NaCl (Rhee 1983). The prooxidant effect of NaCl has been proposed to be due to the release of protein-bound iron (Rhee, 2001), chloride increasing the prooxidant activity of iron (J.E. Osinchak, 1992) and the decrease of antioxidant enzyme activity.(S.K. Lee,L. Mei, E.A. Decker 1997)

D. Irradiation

Irradiation technology had been approved as a safe food processing technique by USDA for poultry in 1992 and red meat in 1999. Irradiation is an efficient way to control the pathogenic microorganisms in meat products such as Listeria, Salmonella Enteritidis and S. Typhimurium  (Cabeza, 2009Foong, 2004).

Water molecules can generate hydroxyl radicals, the most reactive oxygen species, when subjected to ionizing radiation (Thakur and Singh, 1994; Diehl 1995). These hydroxyl radicals can promote lipid oxidation in meat and meat products (Ahn, 2011).

5. Myoglobin color and lipid oxidation

Aldehydes produced by lipid oxidation can form adducts with proteins through amino acids such as cysteine, histidine and lysine (Uchida & Stadtman, 1992).  Lipid oxidation aldehydes can conjugate with the proximal and distal histidine’s in myoglobin resulting in a modification of protein structure and heme binding which can expose the heme group to the environment resulting in more rapid oxidation of the iron in the heme and thus discoloration (Faustman, Liebler, McClure, & Sun, 1999).   In turn, when aldehydes alter the structure of metmyglobin, this exposes the hematin which increases its prooxidant activity (Faustman et al., 1999).

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