Meat Science 86 (2010) 86–94

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Review

Myoglobin and lipid oxidation interactions: Mechanistic bases and control

Cameron Faustman a,⁎, Qun Sun b, Richard Mancini a, Surendranath P. Suman c

a Department of Animal Science, University of Connecticut, Storrs, CT 06269, USAb College of Life Sciences, Sichuan University, Chengdu, Sichuan 610064 Chinac Department of Animal and Food Sciences, University of Kentucky, Lexington, KY 40546, USA

⁎ Corresponding author.E-mail address: Cameron.Faustman@uconn.edu (C. F

0309-1740/$ – see front matter © 2010 The Americandoi:10.1016/j.meatsci.2010.04.025

a b s t r a c t

a r t i c l e i n f o

Article history:Received 25 January 2010Received in revised form 15 March 2010Accepted 15 April 2010

Keywords:MyoglobinLipid oxidationMeat color

Lipid oxidation and myoglobin oxidation in meat lead to off-flavor development and discoloration,respectively. These processes often appear to be linked and the oxidation of one of these leads to theformation of chemical species that can exacerbate oxidation of the other. Several investigators have reportedpreservation of fresh meat color following the inclusion of antioxidant ingredients. An understanding of thecomplementary oxidation interaction provides a basis for explaining quality deterioration in meat and alsofor developing strategies to maintain optimal sensory qualities.

© 2010 The American Meat Science Association. Published by Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 862. Lipid oxidation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 873. Myoglobin oxidation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 874. Lipid oxidation as a facilitator of myoglobin oxidation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 875. Myoglobin as a facilitator of lipid oxidation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 876. Evidence for interactive oxidative processes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 887. Lack of a clear tie between the oxidative reactions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 908. Final thoughts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 90Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 92References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 92

1. Introduction

Sensory properties of meat contribute significantly to theperception of quality and value, and this is especially true for thecolor of meat. Meat discoloration compromises its appearance and isdue to the conversion of oxymyoglobin (OxyMb) to metmyoglobin(MetMb). This change results from a decrease in heme redox stabilityrather than the oxidation of specific amino acid residues. Theoxidation of unsaturated fatty acids in phospholipids and triacylgly-cerols, hereafter referred to as lipid oxidation, contributes to off-flavors. The biochemical reactions directly responsible for myoglobinoxidation and lipid oxidation each generate products that can furtheraccelerate oxidation in a reciprocal manner. Greene and colleagues(Greene, 1969; Greene, Hsin, & Zipser, 1971) were among the first

austman).

Meat Science Association. Published

meat scientists to document the concurrent increase in lipid oxidationand discoloration in meat. Significant support for an interactionbetween the processes of lipid oxidation and discoloration has beenprovided by antioxidant mediation of both processes. For example, itwas known for many years that the lipid-soluble antioxidant, α-tocopherol, delayed lipid oxidation in meat from various livestockspecies (Faustman, 2004). However, the observation that α-tocoph-erol also delayed beef discoloration, a process based on oxidation of awater-soluble protein, provided evidence for a strong link betweenthese processes. Chaijan (2008) recently reviewed the relevance ofthis oxidative interaction to muscle foods. This reference should beconsulted for a more extensive discussion of the classical steps of lipidoxidation (i.e., initiation, propagation and termination) and of theproduction of reactive oxygen species from ferrous OxyMb oxidation.The objective of our review is to elucidate the potential mechanismsby which this oxidative interaction may occur and provide examplesof its practical significance to freshmuscle foods of mammalian origin.

by Elsevier Ltd. All rights reserved.

Table 1Changes in HNE content and TBARS values of pork stored at 0 °C (adapted from Sakai,Yamauchi, Kuwazuru and Gotoh, 1998).

Days of storage

0 3 7 12

HNE (nmol/g meat) 6.03±1.39a 7.03±2.04a 7.42±1.88a 27.96±5.59b

TBARS(nmol MDA/g meat)

0.19±0.01a 0.39±0.03ab 0.83±0.12b 3.08±0.28c

Each value is the mean (n=3)±standard deviation. Values in rows with differentsuperscripts are different (Pb0.05).

87C. Faustman et al. / Meat Science 86 (2010) 86–94

2. Lipid oxidation

The process of lipid oxidation has been reviewed extensively inthe meat and food science literature (Decker & Xu, 1998; Faustman,Naveena, Yin, & Tatiyaborworntham, 2010; Monahan, 2000). Sub-strates necessary for this deteriorative reaction include unsaturatedfatty acids, oxygen and chemical species that accelerate oxidation(e.g., iron; Kanner, Shegalovich, Harel, & Hazan, 1988); these areabundant in meat displayed aerobically or in high-oxygen modifiedatmosphere packaging. A variety of intrinsic properties and proces-sing steps can predispose meat to lipid oxidation. For example, meatfrom non-ruminants contains greater relative concentrations ofunsaturated fatty acids within triacylglycerols (Enser, Hallett, Hewett,Fursey, & Wood, 1996) and generally displays more rapid lipidoxidation than that of ruminants (Tichivangana & Morrissey, 1985);muscles with greater proportions of red fibers are susceptible becausethey contain more iron and phospholipid than muscles containingpredominantly white fibers (Wood et al., 2004); ground meatexperiences greater lipid oxidation than whole cuts because thegrinding process incorporates oxygen, mixes reactive components,and increases surface area as a result of particle size reduction (Gray,Gomaa, & Buckley, 1996). The fortification of meat products with n-3polyunsaturated fatty acids to improve its nutritional profile addssusceptible substrate (Apple, Maxwell, Galloway, Hamilton, & Yancey,2009) that requires antioxidant approaches for minimizing oxidation(Lee, Faustman, Djordjevic, Faraji, & Decker, 2006).

Several products of lipid oxidation are responsible for rancidodors and flavors, and some are very reactive. Primary products oflipid oxidation include chemical species formed during the initiationand early propagation steps. Alkyl, alkoxy and peroxy radicals mayall be produced and readily abstract protons from neighboringmolecules. Peroxides are commonly formed as primary productsand can subsequently undergo scission to form lower molecular-weight secondary oxidation products including aldehydes, ketonesand epoxides. Specific and well known examples of these includehexanal, propanal, malondialdehyde (Sakai, Yamauchi, Kuwazuru, &Gotoh, 1998; Siu & Draper, 1978) and 4-hydroxynonenal (Sakai,Kuwazuru, Yamauchi, & Uchida, 1995). Park, Kim, Lee, Yoo, Shim, andChin (2008) recently characterized several volatile and non-volatileproducts of lipid oxidation in pork belly and loin.

3. Myoglobin oxidation

Myoglobin is the heme protein responsible for meat color. Theoxidation of the central iron atom within the heme group isresponsible for discoloration, a change from red OxyMb to brownishMetMb. When ferrous heme iron oxidizes to its ferric form, oxygen isreleased and replaced by a water molecule.

There has been substantial debate in the literature as to whetherthe rate of OxyMb oxidation or the rate of MetMb reduction is thepredominant determinant of meat color stability (Ledward, 1985;O'Keeffe & Hood, 1982). However, the purpose of this review is tofocus on OxyMb oxidation and its contribution to meat discolora-tion. The rate of discoloration in meat is muscle-specific (Jeong et al.,2009; McKenna et al., 2005; O'Keeffe & Hood, 1982). Muscles thatcontain greater relative proportions of red fibers, and thus morelipid and greater oxygen consumption rates, appear to discolor morequickly.

Many factors affect OxyMb oxidation (Faustman & Cassens, 1990;Renerre, 2000). These include temperature, pH, MetMb reducingactivity, partial oxygen pressure and lipid oxidation. OxyMb oxidationis favored by higher temperatures (Brown & Mebine, 1969), lowerpH values (Gotoh & Shikama, 1974) and the presence of non-hemeiron (Allen & Cornforth, 2006). MetMb reducing activity can beenzymically or non-enzymically based and favors maintenance offerrous forms of myoglobin in meat (Bekhit, Simmons, & Faustman,

2005). Partial oxygen pressures (pO2) in which a complete vacuumexists or in which oxygen saturation is attained favor ferrous myo-globin forms. Low non-zero pO2 favors MetMb formation (George &Stratman, 1952; Ledward, 1970; Neill & Hastings, 1925). Lipidoxidation appears to enhance OxyMb oxidation and is discussedbelow.

4. Lipid oxidation as a facilitator of myoglobin oxidation

Several studies have reported that the process of lipid oxidationenhances meat discoloration. Zakrys, Hogan, O'Sullivan, Allen, andKerry (2008) recently investigated quality parameters in beefpackaged under 0%, 10%, 20%, 50% and 80% oxygen (20% CO2,balance nitrogen). They concluded that “changes in OxyMb and a⁎

values appeared to be driven by lipid oxidation and correlatedstrongly with TBARS”. The mechanisms by which lipid oxidationcould enhance myoglobin oxidation have been explained primarilyon the reactivity of primary and secondary products derived fromunsaturated fatty acids. Supplementation of livestock with dietsenriched in polyunsaturated fatty acids leads to the meat sub-sequently obtained from these animals being more susceptible tolipid oxidation and discoloration (Nute et al., 2007). McKenna et al.(2005) reported on the relationship between several endoge-nous factors that affect beef color stability. Muscles with greatercolor stability were characterized by less oxygen consumptionand less lipid oxidation. O'Grady, Monahan, and Brunton (2001)utilized model systems and demonstrated a role for lipid oxidationin myoglobin oxidation. Muscle microsomes with greater degreesof fatty acid unsaturation promoted greater OxyMb oxidation invitro (Yin & Faustman, 1994).

Incubation of specific products of lipid oxidation (e.g., α,β un-saturated aldehydes; Grimsrud, Xie, Griffin, & Bernlohr, 2008) withOxyMb (Faustman, Liebler, McClure, & Sun, 1999) increases MetMbformation. 4-Hydroxynonenal is a secondary product of n-6 fattyacid oxidation (Pryor & Porter, 1990) that is very reactive and hasreceived considerable attention in the medical (Poli, Schaur, Siems,& Leonarduzzi, 2007) and food science literature (Surh & Kwon, 2005;Surh, Lee, & Kwon, 2007). HNE has been identified in meat (Table 1;Sakai et al., 1998) and its formation is favored by freeze-drying(Gase et al., 2007). Pre-incubation of MetMb with HNE rendered it apoorer substrate for enzymatic MetMb reduction than untreatedMetMb (Lynch & Faustman, 2000). Garry and Mammen (2007)recently noted that one of myoglobin's functions in vivo is to serve asa scavenger of reactive oxygen species.

5. Myoglobin as a facilitator of lipid oxidation

The role of heme proteins in general, and myoglobin specifically,in enhancing lipid oxidation has been studied extensively. Consider-able debate in the literature has focused on the relative contributionsof heme and non-heme iron to lipid oxidation in meat (Baron &Andersen, 2002; Carlsen, Moller, & Skibsted, 2005; Love, 1983;Younathan & Watts, 1959). Greater concentrations of iron and myo-globin are associated with greater rates of lipid oxidation (Faustman,

Table 2Effect of addition of FeSO4 (1 µg/g), myoglobin (5 mg/g) and hemoglobin (5mg/g) towater-washed muscle residue (WR) on TBARS development during storage at 4 °C(adapted from Monahan et al., 1993).

Treatment TBARSa,b

Day 0 Day 2 Day 4 Day 6

WR 0.11±0.06 0.11±0.04 0.15±0.04 0.16±0.06WR+FeSO4 0.14±0.04 0.15±0.04 0.18±0.08 0.22±0.07WR+Mb 0.14±0.04 0.19±0.11 0.31±0.35 0.59±0.73WR+Hb 0.15±0.04 0.21±0.11 0.22±0.25 0.76±0.97

a Mean values±standard deviation of three replicates.b Expressed as mg malonaldehyde/kg residue.

Fig. 1. Lipid oxidation (―) and oxymyoglobin oxidation (····) in 25% M. longissimusdorsi homogenates (H).□, H;■H+FeCl3/ascorbate. abcdeOxymyoglobin oxidation, datapoints bearing different superscripts are significantly different, P≤0.05. wxyLipidoxidation, data points bearing different superscripts are significantly different, P≤0.05.Taken from O'Grady, Monahan and Brunton (2001).

88 C. Faustman et al. / Meat Science 86 (2010) 86–94

Yin, & Nadeau, 1992). Rhee and Ziprin (1987) compared the effectsof heme pigments and non-heme iron on lipid oxidation in beef, porkand chicken. Raw beef demonstrated the greatest capacity for lipidoxidation; the authors concluded that heme pigment concentrationwas more important than non-heme iron in predicting lipid oxixda-tion in meat. Monahan, Crackel, Gray, Buckley, and Morrissey (1993)used a model system to study the effects of hemoglobin, myoglobinand FeSO4 on lipid oxidation. Their results demonstrated that TBARSvalues were greatest for the hemoglobin treatment and followedthe order hemoglobinNmyoglobinNFeSO4Ncontrol in raw washedpork muscle (Table 2). In meat, non-heme iron is generally assumedto be associated with low molecular-weight compounds.

From a mechanistic point of view, the oxidation of OxyMb toMetMb generates reactive intermediates capable of enhancingfurther oxidation of OxyMb and/or unsaturated fatty acids. Specifi-cally, superoxide anion is formed (Gotoh & Shikama, 1976) and thisdismutates rapidly to hydrogen peroxide. The latter can react withtheMetMb concurrently generated in this oxidation sequence (Tajima& Shikama, 1987) to form an activated MetMb complex capable ofenhancing lipid oxidation (Kanner & Harel, 1985) that is attributed toferryl myoglobin (George & Irvine, 1952). Alkyl hydroperoxides aresimilar to hydrogen peroxide with respect to their ability to interactwith MetMb (George & Irvine, 1953). MetMb-H2O2 (Harel & Kanner,1985; Kanner & Harel, 1985) and ferryl myoglobin (Baron & Andersen,2002) have been documented as potentially powerful contributorsto lipid oxidation in meat. Chan, Faustman, Yin, and Decker (1997)reported that OxyMb facilitated oxidation of fatty acids in phospha-tidylcholine liposomes to a greater extent than an equimolar con-centration of MetMb. They hypothesized that the process of OxyMboxidation would generate both MetMb and H2O2 which togetherwould be more potent than MetMb only. This was supported by theobservation that addition of catalase but not superoxide dismutasedecreased oxidation of OxyMb and lipid. Richards, Cai, and Grunwald(2009) recently demonstrated that a mutant sperm whale myoglobin(i.e., L29F) with a much slower autoxidation rate than the wild typewas a less potent promoter of lipid oxidation.

In addition to the prooxidative contributions of the myoglobinoxidation process and generation of ferryl myoglobin, the dissoci-ation of both heme from myoglobin and iron from heme may alsocontribute to the mechanism by which myoglobin enhances lipidoxidation. Grunwald and Richards (2006a,b) demonstrated thatsperm whale myoglobin mutants differing in heme affinity enhancelipid oxidation differently in washed fish muscle system. Specifi-cally, myoglobin with high heme affinity was less effective at pro-moting lipid oxidation when compared with low heme affinitymyoglobins (Grunwald & Richards, 2006a); OxyMb has a muchhigher heme affinity than MetMb (Richards et al., 2009). Theauthors also used myoglobin mutants to demonstrate that hemeloss rate had a greater effect on lipid oxidation than did myoglobinautoxidation rate (Grunwald & Richards, 2006b). The propensity forheme dissociation from wild type myoglobins of meat-producinglivestock origin has not been reported. Lynch and Faustman (2000)

reported that pre-incubation with HNE made MetMb a more potentaccelerator of lipid oxidation relative to untreated controls. Thepossibility that HNE modification could lead to greater heme ex-posure, and even heme release, with concomitant enhancement oflipid oxidation was not investigated.

6. Evidence for interactive oxidative processes

The known chemistry associated with oxidation of lipids andmyoglobin provides a fundamental basis by which these reactions canexacerbate each other. Evidence for an interaction between theprocesses of lipid oxidation and myoglobin oxidation in meat hasbeen primarily of two types, (1) reports of concomitant oxidation oflipids and myoglobin in meat or in vitro over some time period (e.g.,storage), and (2) mediation by antioxidants that are recognized forinhibiting lipid oxidation but that also delays discoloration.

The redox chemistry of hemoglobin is similar to that of myo-globin, and results from experiments with this heme protein haveprovided support for the prooxidative effect of lipids. One of theearliest reports of lipid:heme protein interactions was from Haur-owitz, Schwerin, and Yenson (1941). They reported that hemoglobinwas destroyed and heme iron released when incubated in the pres-ence of unsaturated fatty acids and oxygen at 38 °C. Subsequent workby Koizumac, Nonaka, and Brown (1973) showed that OxyMboxidized to MetMb rapidly when combined with arginine linoleate;degradation of the heme moiety was observed. Szebeni andcolleagues investigated the interaction between hemoglobin andphospholipid membranes and reported that the generation of lipidoxidation-derived thiobarbituric acid-reactive substances (TBARS)was positively correlated with oxyhemoglobin (OxyHb) oxidation(Szebeni, Winterbourn, & Carell, 1984). Interactions between OxyHband lipid oxidation was reported by Akhrem, Andreyuk, Kisel, andKiselev (1989).

A number of model studies have demonstrated interaction ofmyoglobin and lipid oxidation in vitro (Chan, Faustman, & Renerre,1996; Gorelik & Kanner, 2001; Hayes, O'Brien, et al., 2009; Hayes,Stepanyan, et al., 2009; Lee, Phillips, Liebler, & Faustman, 2003; Lin &Hultin, 1977; Monahan, Skibsted, & Andersen, 2005; Yin & Faustman,1993; Yin & Faustman, 1994). Yin and Faustman (1993) demonstrated

Table 3Compounds identified in muscle cytoplasm that have demonstrated antioxidantactivity.

Cytosoliccompound

System Reference

Anserine In vitro Fu et al. (2009)Ascorbate Washed cod

muscle systemRichards and Li (2004)

Carnitine In vitro Solarska, Lewinska, Karowicz-Bilinska,and Bartosz (2010)

Carnosine Ground beef Badr (2007)Catalase In vivo He et al. (2008)Cysteine In vitro Benjakul, Visessanguan, and

Tanaka (2006)Glutathione In vitro Tang, Faustman, Lee, and Hoagland (2003)Glutathioneperoxidase

In vivo Cheng, Fu, Porres, Ross, and Lei (1999)

Lactate Beef loins Kim, Keeton, Smith, Maxim, Yang,and Savell (2009)

NADH In vitro Olek, Ziolkowski, Kaczor, Greci,Popinigis, and Antosiewicz (2004)

NADPH In vitro Minard and McAlister-Henn (2001)Putrescine In vivo Yiu, Juang, Fang, Liu, and Wu (2009)Pyruvate In vivo Zlotnik et al. (2008)Spermineand spermidine

In vivo Belle, Dalmolin, Fonini, Rubin,and Rocha (2004)

Superoxidedismutase

In vitro Chen et al. (2009)

Urate Milk Ostdal, Andersen, and Nielsen (2000)

89C. Faustman et al. / Meat Science 86 (2010) 86–94

greater lipid and myoglobin oxidation in liposomes with increasedunsaturation of phosphatidylcholine used to construct liposomes.O'Grady, Monahan and Brunton (2001) utilized bovine musclehomogenates to study the interactions between lipid oxidation andOxyMb oxidation. They reported that OxyMb oxidation was enhancedby the process of lipid oxidation (Fig. 1) and this was likely due toprimary rather than secondary products. Their results also suggestedthat lipid oxidation preceded OxyMb oxidation. Andersen andSkibsted (1991) suggested the reverse order of oxidation (i.e., myo-globin oxidation initiated prior to lipid oxidation) in salted groundpork.

Similar to results obtained in vitro, OxyMb oxidation appears tobe linked with lipid oxidation in beef (Greene, 1969; Greene et al.,1971; Lee, Hendricks, & Cornforth, 1998; McKenna et al., 2005;Mercier, Gatellier, & Renerre, 1995; O'Grady, Monahan, & Mooney,2001), veal (Faustman, Specht, Malkus, & Kinsman, 1992), lamb(Luciano et al., 2009) and chevon (Kannan, Kouakou, & Gelaye, 2001).

Antioxidants may be fed to meat-producing livestock, or addedexogenously to postmortem muscle during processing. The parti-tioning of exogenously added antioxidants within muscle foods iscritical to efficacy (Raghavan & Hultin, 2004, 2006). Some of themost convincing evidence for interplay between lipid and myoglo-bin oxidation in meat was provided by the observation that dietarysupplementation of vitamin E delayed both of these processes inground (Faustman, Cassens, Schaefer, Buege, Williams, & Sheller,1989) and whole-muscle beef cuts (Faustman, Cassens, Schaefer,Buege, & Sheller, 1989; Kerry, Buckley, & Morrissey, 2000). VitaminE, specifically α-tocopherol, was long recognized as a fat-solublelipid antioxidant for meat products prior to 1989 (Faustman et al.,1989). A threshold concentration of α-tocopherol for achievingoptimal protection of both lipid and myoglobin from oxidation wasidentified (Arnold, Arp, Scheller, Williams, & Schaefer, 1993;Faustman, Cassens, Schaefer, Buege, & Sheller, 1989; Faustman,Cassens, Schaefer, Buege, Williams, et al., 1989), and evidence thatdietary delivery of α-tocopherol was significantly more effectivethan exogenous addition for gaining maximal benefit was published(Mitsumoto, 2000; Mitsumoto, Arnold, Schaefer, & Cassens, 1993).The latter was attributed to proper placement of α-tocopherolwithin the lipid bilayer where its normal physiological locationfacilitated its biological antioxidant function in postmortem muscle(Faustman, Burr, & Liebler, 1999). In general, fresh forage containsgreater concentrations of α-tocopherol than concentrate diets.Thus, a number of studies have reported that pasture feeding ofcattle results in beef that has greater lipid and myoglobin redoxstability than concentrate-fed animals (Insani et al., 2008; Lucianoet al., 2009).

An important question has been how α-tocopherol protects theredox stability of myoglobin, a water-soluble protein known to residein the cytoplasm (Faustman & Wang, 2000). This has proven difficultto answer but our work has attempted to provide some potentialmechanisms by which this could occur. Our major effort has fo-cused on the hypothesis that products of phospholipid unsaturatedfatty acid oxidation can bind directly to myoglobin and lower itsredox stability. Heme proteins are capable of binding to membranes(Szebeni, Huser, Eskelson, Watson, & Winterhalter, 1988) and fattyacids (Gotz, Hertel, & Groschel-Stewart, 1994) and this proximitywould enhance the likelihood of interaction with products releasedas a consequence of lipid oxidation. Livingston and Brown (1981)noted that any perturbation in myoglobin conformation would beexpected to predispose the heme protein to more rapid oxidation.

Yin and others (Yin & Faustman, 1993; Yin, Faustman, Riesen, &Williams, 1993) utilized myoglobin:liposomes to construct modelsin which phospholipid fatty acid profile, phospholipid type andpresence/absence of α-tocopherol could be controlled. Their resultsconsistently showed that manipulation of liposomes that led togreater/more rapid oxidation of lipids also resulted in greater/more

rapid myoglobin oxidation. Support for this was provided initially byChan, Faustman, and Decker (1997) when they incubated dialysissacs containing OxyMb in solutions of liposomes differing in fattyacid unsaturation and presence/absence of α-tocopherol. Dialysissacs provided a physical barrier that prevented outward diffusionand direct contact of OxyMb with liposomes, but allowed lipid oxi-dation products (mol. wt.b500 Da) to diffuse inwards and potentiallyreact with OxyMb. Greater degrees of fatty acid unsaturationincreased, and the presence of α-tocopherol decreased, the oxidationof both lipid and OxyMb. Results of this work led to studies of knownsecondary products of lipid oxidation, specifically α,β-unsaturatedaldehydes, as promoters of redox instability in OxyMb. Faustman,Liebler, McClure, and Sun (1999) reported that monounsaturatedaldehydes (i.e., hexenal, heptenal, octenal, nonenal) enhancedMetMbformation from OxyMb more rapidly than their saturated counter-parts (hexanal, heptanal, octanal, and nonanal) or controls. Interest-ingly, monounsaturated aldehydes increased significantly in theirprooxidant capacity as chain length increased from six to ninecarbons. As noted previously, HNE is a well-documented secondaryproduct of linoleic acid oxidation. We have utilized HNE as a modeloxidation product for our studies of interactions with myoglobin.HNE accelerates OxyMb oxidation by binding covalently to specifichistidine residues in the protein's primary sequence. This has beendocumented for bovine (Alderton, Faustman, Liebler, & Hill, 2003;Suman, Faustman, Stamer, & Liebler, 2007), porcine (Suman,Faustman, Stamer, & Liebler, 2006) and chicken and turkeymyoglobins (Maheswarappa et al., 2009; Naveena et al., 2010).Mass spectrometry and its tools have permitted identification ofspecific HNE:histidine adducts in myoglobin. Interestingly, theeffect of HNE alkylation on decreasing OxyMb redox stability isless pronounced at pH 5.6 than at 7.4, a result attributed to greaterautoxidation and potentially decreased nucleophilicity of candidatehistidine residues at this pH.

Incubation of porcine OxyMb with porcine liver microsomesresulted in concurrent oxidation of pigment and lipid (Lee et al.,2003). α-Tocopherol concentration did not exert the same pro-tective effect on OxyMb redox stability that was observedwith similarmodels that included beef-derived microsomes (Chan, Faustman, &Renerre, 1996; Chan, Hakkarainen, et al., 1996); this result was

Table 4Effect of plant extracts on lipid oxidation and myoglobin oxidation in meat.

Plant extract Inhibit lipid oxidation Inhibit myoglobin oxidation Reference

Grape seed Yes NT Mielnik, Olsen, Vogt, Adeline, and Skrede (2006); Ahn, Grün, and Fernando (2002);Nissen, Byrne, Bertelsen, and Skibsted (2004); Ahn, Grün, and Fernando (2002)

Grape seed Yes No Sasse, Colindres, and Brewer (2009); Rojas and Brewer (2008); Rojas and Brewer (2007)Grape seed Yes Yes Ahn, Grün, and Mustapha (2007)

Carpenter, O'Grady, O'Callaghan, O'Brien, and Kerry (2007)Kimchi Yes NT Lee and Kunz (2005)Lycopene Yes Yes Sánchez-Escalante, Torrescano, Djenane, Beltrán, and Roncalés (2003a)Lycopene Yes No Sánchez-Escalante, Torrescano, Djenane, Beltrán, and Roncalés (2003b)Onion Yes No Tang and Cronin (2007)Oregano Yes Yes Sánchez-Escalante, Torrescano, Djenane, Beltrán and Roncalés (2003a,b)Pine bark Yes Yes Ahn et al. (2007); Ahn, Grun, and Mustapha (2004)Plum Yes NT Nunez de Gonzalez, Boleman, Miller, Keeton and Rhee (2008)Plum Yes Yes Lee and Ahn (2005)Red pepper Yes Yes Sánchez-Escalante et al. (2003a)Rice fiber Yes NT Kim, Godber, and Prinaywiwatkul (2000)Rosemary Yes NT Trindade, Mancini-Filho, and Villavicencio (2010); Georgantelis, Ambrosiadis,

Katikou, Blekas, and Georgakis (2007); Nissen, Byrne, Bertelsen, and Skibsted (2004);Tanabe, Yoshida, and Tomita (2002)

Rosemary Yes No Haak, Raes and De Smet (2009); Sasse, Colindres, and Brewer (2009);Hernandez-Hernandez, Ponce-Alquicira, Jaramillo-Flores, and Legarreta (2009);McBride, Hogan, and Kerry (2007); Lund, Hviid, and Skibsted (2007); Georgantelis, Blekas,Katikou, Ambrosiadis, and Fletouris (2007); Ahn, Grün, and Mustapha (2007)

Rosemary Yes Yes Camo, Beltran and Roncales (2008); Keokamnerd, Han, Acton and Dawson (2008);Balentine, Crandall, O'Bryan, Duong and Pohlman (2006); Estevez, Ventanas and Cava (2005);Fernández-Ginés, Fernández-López, Sayas-Barberá, Sendra, and Pérez-Alvarez (2003);Sánchez-Escalante, Djenane, Torrescano, Beltrán, and Roncales (2003)

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interesting because of the previously noted inconsistent effect ofvitamin E supplementation on pork color stability relative to beefcolor stability (Cannon et al., 1996; Houben, Eikelenboom, & Hoving-Bolink, 1998). Suman et al. (2006) provided evidence that differencesin the primary sequences of bovine and porcine myoglobins, specifi-cally the number and location of nucleophilic histidine residues, couldbe responsible, in part, for the observed differences in α-tocopherolefficacy for stabilizing meat color in pork and beef obtained fromvitamin E-supplemented livestock. Ramanathan, Konda, Mancini, andFaustman (2009) subsequently reported that sarcoplasmic extractsof pork affected myoglobin redox stability less than beef sarcoplasmicextracts.

Antioxidants have been identified in the cytoplasm of postmortemmuscle (Table 3) and have also been obtained from exogenous plant-based sources (Table 4). The inclusion of a variety of antioxidants infresh (Mitsumoto et al., 1991) and irradiated (Duong et al., 2008)meat/meat products has led to decreased lipid and myoglobin oxi-dation. Specific examples have included the addition of carnosine(Decker, Chan, Livisay, Buterfield, & Faustman, 1995); rosemary(Balentine, Crandall, O'Bryan, Duong, & Pohlman, 2006), tea catechins(Tang et al., 2006) and honey bee propolis (Sánchez-Escalante et al.,2009). Lee, Faustman, Djordjevic, Faraji, and Decker (2006) utilizedan antioxidant cocktail containing a radical quencher (rosemary),chelator (citrate) and reductant (erythorbate) to stabilize groundmeat enriched with an n-3 fatty acid emulsion. In addition tominimizing lipid oxidation, enhanced redness was also observed infresh pork sausage and ground turkey.

7. Lack of a clear tie between the oxidative reactions

Not all studies that have measured lipid oxidation and myo-lobin oxidation in meat have produced results demonstrating thatthe two processes are linked. For example, meat from red deer(Cervus elaphus) that were allowed to graze versus those that wereconcentrate-fed had greater color stability but showed no differ-ences in lipid oxidation measured as TBARS (Wiklund, Sampels,Manley, Pickova, & Littlejohn, 2005). Alternatively, meat obtained

from lambs raised on pasture demonstrated less lipid oxidationthan animals fed a concentrate diet while no differences in colorstability were noted (Sante-Lhoutellier, Engel, & Gatellier, 2008).Sesamol addition to porcine and bovine meat systems led todecreased lipid oxidation but enhanced OxyMb oxidation; additionof ellagic acid and olive leaf extract led to decreases in both oxi-dative processes (Hayes, O'Brien, et al., 2009; Hayes, Stepanyan, etal., 2009). McBride, Hogan, and Kerry (2007) reported that extractsof rosemary minimized lipid oxidation, but were without effectrelative to preservation of redness in fresh ground beef. Xiong et al.(2007) investigated the effect of cattle age on lipid and myoglobinstability in beef. They reported that meat from older animals hadan increased rate of lipid oxidation, whereas OxyMb oxidation wasonly slightly impacted; meat from older animals has been noted tocontain greater proportions of unsaturated fatty acids as a result ofcertain feeding regimens (Warren et al., 2008).

The unique relationship between pO2 and myoglobin redoxform such that low non-zero pO2 favors met-heme formation(Ledward, 1970) provides conditions in which the oxidative interac-tion is not tightly interconnected. The extent of lipid oxidation inmeat is proportional to the concentration of oxygen present andwould be expected to be minimal in low pO2 environments. OxyMbredox stability is favored in high-oxygen atmospheres; lipid oxi-dation would occur readily in these conditions. Thus, atmospherescontaining very high or very low concentrations of oxygen provideconditions in which the oxidative interaction between lipid andmyoglobin is not tightly linked.

8. Final thoughts

Meat is a complex food system and any interactions betweenmyoglobin and lipid oxidation (Fig. 2) must be considered withinthe context of all biochemical activity occurring in postmortemmuscle. For example, Monahan, Skibsted, and Andersen (2005)published results that considered a role for oxygen concentration inoxidative interactions. They utilized a beef homogenate in whichthe controlled introduction of oxygen was combined with a ferric

Fig. 2. Summary of potential interacting oxidation reactions between OxyMb and unsaturated fatty acids in lipid bilayers.

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chloride/sodium ascorbate oxidation initiator to elucidate themechanism of oxidative interactions. The model accommodated ahigh-oxygen environment that favored lipid oxidation and OxyMbstability, and the authors concluded that dissolved oxygenconcentration was a critical consideration for OxyMb redoxstability. They suggested that the consumption of oxygen resultingfrom the process of lipid oxidation was sufficient to accelerateOxyMb oxidation through the localized lowering of partial oxygenpressure. This very interesting study should be followed up bymodels that differ in dissolved oxygen concentration across theentire continuum from anoxic to saturating conditions. This studysuggests that lipid oxidation would need to precede OxyMboxidation if the processes were indeed linked.

Dissolved oxygen in meat would not only be decreased by lipidoxidation, but also would be impacted by mitochondrial/sub-mitochondrial activity and metabolism of aerobic psychrotrophs.Tang et al. (2005) simultaneously measured lipid oxidation andMetMb formation in a model containing OxyMb and mitochondriathat differed in concentration of α-tocopherol. Interestingly,mitochondria that contained greater tocopherol concentrationsdemonstrated greater oxygen consumption. This observationwould make interpretation of antioxidant effects more difficult.

That is, as per Monahan, Skibsted, and Andersen (2005), the pres-ence of α-tocopherol would be hypothesized to slow lipid oxidationand the associated consumption of oxygen, however, mitochondriacould be expected to be more active due presumably to theprotective effect of the antioxidant on their membrane lipids andassociated metabolism. Carefully designed experiments are neededto simultaneously address the different processes that contribute tothe oxidative outcomes observed in meat. These would include aconsideration of oxygen consumption by all possible candidates(i.e., mitochondrial activity, bacterial metabolism, lipid oxidation),and generation of reactive products of lipid oxidation and by theprocess of OxyMb oxidation.

One area ripe for future research is the careful characterizationof the myofiber sarcoplasm and the role of its constituents on bothinhibiting and enhancing oxidative reactions. Investigators haveexamined the role of sarcoplasmic extracts (e.g., low molecular-and high molecular-weight fractions; Gopalakrishnan, Decker, &Means, 1999; Kanner, Salan, Harel, & Shegalovich, 1991; Min & Ahn,2009; Yin & Faustman, 1994), and several studies have sought toidentify prooxidants (Johns, Birkinshaw, & Ledward, 1989) and/orantioxidant compounds (Chan & Decker, 1994) present in the sar-coplasm of postmortem muscle. In some cases, these investigations

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have been done to better characterize the components primarilyresponsible for lipid and/or myoglobin oxidation in meat. In othercases, strategies have been suggested for selectively removingprooxidant species (e.g., by precipitating iron-binding proteins;Gopalakrishnan et al., 1999) or enhancing the concentration andactivity of naturally occurring antioxidants (Chan, Decker, & Means,1993; Decker & Xu, 1998). There are a large number of chemicalcompounds present in the sarcoplasm (Decker & Mei, 1996) andthe interactions between those in the low molecular- and highmolecular-weight fractions is complex (Li, Richards, & Undeland,2005) and remains poorly understood. A complicating factor insuch considerations is the fact that myoglobin is a sarcoplasmicprotein (Min & Ahn, 2009; Ramanathan et al., 2009); a method forselectively removing it from the muscle of meat-producing speciesas has been demonstrated in mice (Garry et al., 1998) wouldprovide an interesting model for future study.

Acknowledgements

We are grateful to the many investigators that have publishedresearch in this area. This publication was supported by the NationalResearch Initiative Grant no. 2007-35503-18482 from the USDACooperative State Research, Education, and Extension Service Im-proving Food Quality and Value Program.

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