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Meat Science 86 (2010) 86 94

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Meat Science

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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, USA

b College of Life Sciences, Sichuan University, Chengdu, Sichuan 610064 China

c Department of Animal and Food Sciences, University of Kentucky, Lexington, KY 40546, USA

article info

Article history:

Received 25 January 2010 Received in revised form 15 March 2010 Accepted 15 April 2010

Keywords:

Myoglobin

Lipid oxidation

Meat color

Contents

abstract

Lipid oxidation and myoglobin oxidation in meat lead to off- avor development and discoloration, respectively. These processes often appear to be linked and the oxidation of one of these leads to the formation of chemical species that can exacerbate oxidation of the other. Several investigators have reported preservation of fresh meat color following the inclusion of antioxidant ingredients. An understanding of the complementary oxidation interaction provides a basis for explaining quality deterioration in meat and also for developing strategies to maintain optimal sensory qualities. © 2010 The American Meat Science Association. Published by Elsevier Ltd. All rights reserved.

1. Introduction

 

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2. Lipid oxidation

 

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3. Myoglobin oxidation

 

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4. Lipid oxidation as a facilitator of myoglobin oxidation

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5. Myoglobin as a facilitator of lipid oxidation

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6. Evidence for interactive oxidative processes

 

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7. Lack of a clear tie between the oxidative reactions

 

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8. Final thoughts

 

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Acknowledgements

 

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References

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1. Introduction

Sensory properties of meat contribute signi cantly to the perception of quality and value, and this is especially true for the color of meat. Meat discoloration compromises its appearance and is due to the conversion of oxymyoglobin (OxyMb) to metmyoglobin (MetMb). This change results from a decrease in heme redox stability rather than the oxidation of speci c amino acid residues. The oxidation of unsaturated fatty acids in phospholipids and triacylgly- cerols, hereafter referred to as lipid oxidation, contributes to off- avors. The biochemical reactions directly responsible for myoglobin oxidation and lipid oxidation each generate products that can further accelerate oxidation in a reciprocal manner. Greene and colleagues ( Greene, 1969; Greene, Hsin, & Zipser, 1971) were among the rst

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

meat scientists to document the concurrent increase in lipid oxidation and discoloration in meat. Signicant support for an interaction between the processes of lipid oxidation and discoloration has been provided by antioxidant mediation of both processes. For example, it was known for many years that the lipid-soluble antioxidant, α- tocopherol, delayed lipid oxidation in meat from various livestock species ( Faustman, 2004). However, the observation that α-tocoph- erol also delayed beef discoloration, a process based on oxidation of a water-soluble protein, provided evidence for a strong link between these processes. Chaijan (2008) recently reviewed the relevance of this oxidative interaction to muscle foods. This reference should be consulted for a more extensive discussion of the classical steps of lipid oxidation (i.e., initiation, propagation and termination) and of the production of reactive oxygen species from ferrous OxyMb oxidation. The objective of our review is to elucidate the potential mechanisms by which this oxidative interaction may occur and provide examples of its practical signicance to fresh muscle foods of mammalian origin.

0309-1740/$ see front matter © 2010 The American Meat Science Association. Published by Elsevier Ltd. All rights reserved. doi: 10.1016/j.meatsci.2010.04.025

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

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2. Lipid oxidation

The process of lipid oxidation has been reviewed extensively in the meat and food science literature ( Decker & Xu, 1998; Faustman, Naveena, Yin, & Tatiyaborworntham, 2010; Monahan, 2000). Sub- strates necessary for this deteriorative reaction include unsaturated fatty acids, oxygen and chemical species that accelerate oxidation (e.g., iron; Kanner, Shegalovich, Harel, & Hazan, 1988); these are abundant in meat displayed aerobically or in high-oxygen modi ed atmosphere packaging. A variety of intrinsic properties and proces- sing steps can predispose meat to lipid oxidation. For example, meat from non-ruminants contains greater relative concentrations of unsaturated fatty acids within triacylglycerols ( Enser, Hallett, Hewett, Fursey, & Wood, 1996) and generally displays more rapid lipid oxidation than that of ruminants ( Tichivangana & Morrissey, 1985 ); muscles with greater proportions of red bers are susceptible because they contain more iron and phospholipid than muscles containing predominantly white bers ( Wood et al., 2004 ); ground meat experiences greater lipid oxidation than whole cuts because the grinding process incorporates oxygen, mixes reactive components, and increases surface area as a result of particle size reduction ( Gray, Gomaa, & Buckley, 1996). The fortication of meat products with n-3 polyunsaturated fatty acids to improve its nutritional prole adds susceptible 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 rancid odors and avors, and some are very reactive. Primary products of lipid oxidation include chemical species formed during the initiation and early propagation steps. Alkyl, alkoxy and peroxy radicals may all be produced and readily abstract protons from neighboring molecules. Peroxides are commonly formed as primary products and can subsequently undergo scission to form lower molecular- weight secondary oxidation products including aldehydes, ketones and epoxides. Specic and well known examples of these include hexanal, propanal, malondialdehyde ( Sakai, Yamauchi, Kuwazuru, & Gotoh, 1998; Siu & Draper, 1978 ) and 4-hydroxynonenal ( Sakai, Kuwazuru, Yamauchi, & Uchida, 1995). Park, Kim, Lee, Yoo, Shim, and Chin (2008) recently characterized several volatile and non-volatile products of lipid oxidation in pork belly and loin.

3. Myoglobin oxidation

Myoglobin is the heme protein responsible for meat color. The oxidation of the central iron atom within the heme group is responsible for discoloration, a change from red OxyMb to brownish MetMb. When ferrous heme iron oxidizes to its ferric form, oxygen is released and replaced by a water molecule. There has been substantial debate in the literature as to whether the rate of OxyMb oxidation or the rate of MetMb reduction is the predominant determinant of meat color stability (Ledward, 1985; O'Keeffe & Hood, 1982 ). However, the purpose of this review is to focus on OxyMb oxidation and its contribution to meat discolora- tion. The rate of discoloration in meat is muscle-speci c ( Jeong et al., 2009; McKenna et al., 2005; O'Keeffe & Hood, 1982 ). Muscles that contain greater relative proportions of red bers, and thus more lipid and greater oxygen consumption rates, appear to discolor more quickly. Many factors affect OxyMb oxidation ( Faustman & Cassens, 1990; Renerre, 2000 ). These include temperature, pH, MetMb reducing activity, partial oxygen pressure and lipid oxidation. OxyMb oxidation is favored by higher temperatures ( Brown & Mebine, 1969), lower pH values ( Gotoh & Shikama, 1974 ) and the presence of non-heme iron ( Allen & Cornforth, 2006). MetMb reducing activity can be enzymically or non-enzymically based and favors maintenance of ferrous forms of myoglobin in meat ( Bekhit, Simmons, & Faustman,

2005). Partial oxygen pressures (pO 2 ) in which a complete vacuum exists or in which oxygen saturation is attained favor ferrous myo- globin forms. Low non-zero pO 2 favors MetMb formation ( George & Stratman, 1952; Ledward, 1970; Neill & Hastings, 1925 ). Lipid oxidation appears to enhance OxyMb oxidation and is discussed below.

4. Lipid oxidation as a facilitator of myoglobin oxidation

Several studies have reported that the process of lipid oxidation enhances meat discoloration. Zakrys, Hogan, O'Sullivan, Allen, and Kerry (2008) recently investigated quality parameters in beef packaged under 0%, 10%, 20%, 50% and 80% oxygen (20% CO 2 , balance nitrogen). They concluded that changes in OxyMb and a values appeared to be driven by lipid oxidation and correlated strongly with TBARS . The mechanisms by which lipid oxidation could enhance myoglobin oxidation have been explained primarily on the reactivity of primary and secondary products derived from unsaturated fatty acids. Supplementation of livestock with diets enriched in polyunsaturated fatty acids leads to the meat sub- sequently obtained from these animals being more susceptible to lipid 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 greater color stability were characterized by less oxygen consumption and less lipid oxidation. O'Grady, Monahan, and Brunton (2001) utilized model systems and demonstrated a role for lipid oxidation in myoglobin oxidation. Muscle microsomes with greater degrees of fatty acid unsaturation promoted greater OxyMb oxidation in vitro ( Yin & Faustman, 1994 ). Incubation of speci c products of lipid oxidation (e.g., α,β un- saturated aldehydes; Grimsrud, Xie, Grifn, & Bernlohr, 2008) with OxyMb ( Faustman, Liebler, McClure, & Sun, 1999 ) increases MetMb formation. 4-Hydroxynonenal is a secondary product of n-6 fatty acid oxidation ( Pryor & Porter, 1990) that is very reactive and has received considerable attention in the medical ( Poli, Schaur, Siems, & Leonarduzzi, 2007) and food science literature ( Surh & Kwon, 2005; Surh, Lee, & Kwon, 2007). HNE has been identied 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 a poorer substrate for enzymatic MetMb reduction than untreated MetMb ( Lynch & Faustman, 2000). Garry and Mammen (2007) recently noted that one of myoglobin's functions in vivo is to serve as a scavenger of reactive oxygen species.

5. Myoglobin as a facilitator of lipid oxidation

The role of heme proteins in general, and myoglobin specically, in enhancing lipid oxidation has been studied extensively. Consider- able debate in the literature has focused on the relative contributions of 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 1 Changes 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± 1.39 a 7.03± 2.04 a

7.42±1.88 a 27.96± 5.59 b

 

0.19± 0.01 a 0.39± 0.03 ab 0.83±0.12 b

3.08± 0.28 c

TBARS (nmol MDA/g meat)

 

Each value is the mean ( n = 3)± standard deviation. Values in rows with different superscripts are different (P b 0.05).

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

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

Treatment

TBARS a,b

Day 0

Day 2

Day 4

Day 6

WR WR+ FeSO 4 WR+Mb WR+Hb

0.11± 0.06

0.11± 0.04

0.15±0.04

0.16± 0.06

0.14± 0.04

0.15± 0.04

0.18±0.08

0.22± 0.07

0.14± 0.04

0.19± 0.11

0.31±0.35

0.59± 0.73

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.

   

Yin, & Nadeau, 1992). Rhee and Ziprin (1987) compared the effects of heme pigments and non-heme iron on lipid oxidation in beef, pork and chicken. Raw beef demonstrated the greatest capacity for lipid oxidation; the authors concluded that heme pigment concentration was 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, myoglobin and FeSO 4 on lipid oxidation. Their results demonstrated that TBARS values were greatest for the hemoglobin treatment and followed the order hemoglobin N myoglobin N FeSO 4 N control in raw washed pork muscle (Table 2). In meat, non-heme iron is generally assumed to be associated with low molecular-weight compounds. From a mechanistic point of view, the oxidation of OxyMb to MetMb generates reactive intermediates capable of enhancing further oxidation of OxyMb and/or unsaturated fatty acids. Speci- cally, superoxide anion is formed ( Gotoh & Shikama, 1976) and this dismutates rapidly to hydrogen peroxide. The latter can react with the MetMb concurrently generated in this oxidation sequence ( Tajima & Shikama, 1987) to form an activated MetMb complex capable of enhancing lipid oxidation ( Kanner & Harel, 1985) that is attributed to ferryl myoglobin (George & Irvine, 1952). Alkyl hydroperoxides are similar to hydrogen peroxide with respect to their ability to interact with MetMb ( George & Irvine, 1953). MetMb-H 2 O 2 ( Harel & Kanner, 1985; Kanner & Harel, 1985) and ferryl myoglobin ( Baron & Andersen, 2002) have been documented as potentially powerful contributors to 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 OxyMb oxidation would generate both MetMb and H 2 O 2 which together would be more potent than MetMb only. This was supported by the observation that addition of catalase but not superoxide dismutase decreased 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 type was a less potent promoter of lipid oxidation. In addition to the prooxidative contributions of the myoglobin oxidation process and generation of ferryl myoglobin, the dissoci- ation of both heme from myoglobin and iron from heme may also contribute to the mechanism by which myoglobin enhances lipid oxidation. Grunwald and Richards (2006a,b) demonstrated that sperm whale myoglobin mutants differing in heme af nity enhance lipid oxidation differently in washed sh muscle system. Speci - cally, myoglobin with high heme af nity was less effective at pro- moting lipid oxidation when compared with low heme af nity myoglobins ( Grunwald & Richards, 2006a ); OxyMb has a much higher heme af nity than MetMb ( Richards et al., 2009 ). The authors also used myoglobin mutants to demonstrate that heme loss rate had a greater effect on lipid oxidation than did myoglobin autoxidation rate ( Grunwald & Richards, 2006b ). The propensity for heme dissociation from wild type myoglobins of meat-producing livestock origin has not been reported. Lynch and Faustman (2000)

reported that pre-incubation with HNE made MetMb a more potent accelerator of lipid oxidation relative to untreated controls. The possibility that HNE modi cation could lead to greater heme ex- posure, and even heme release, with concomitant enhancement of lipid oxidation was not investigated.

6. Evidence for interactive oxidative processes

The known chemistry associated with oxidation of lipids and myoglobin provides a fundamental basis by which these reactions can exacerbate each other. Evidence for an interaction between the processes of lipid oxidation and myoglobin oxidation in meat has been primarily of two types, (1) reports of concomitant oxidation of lipids and myoglobin in meat or in vitro over some time period (e.g., storage), and (2) mediation by antioxidants that are recognized for inhibiting 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 have provided support for the prooxidative effect of lipids. One of the earliest reports of lipid:heme protein interactions was from Haur- owitz, Schwerin, and Yenson (1941) . They reported that hemoglobin was destroyed and heme iron released when incubated in the pres- ence of unsaturated fatty acids and oxygen at 38 °C. Subsequent work by Koizumac, Nonaka, and Brown (1973) showed that OxyMb oxidized to MetMb rapidly when combined with arginine linoleate; degradation of the heme moiety was observed. Szebeni and colleagues investigated the interaction between hemoglobin and phospholipid membranes and reported that the generation of lipid oxidation-derived thiobarbituric acid-reactive substances (TBARS) was positively correlated with oxyhemoglobin (OxyHb) oxidation ( Szebeni, Winterbourn, & Carell, 1984). Interactions between OxyHb and lipid oxidation was reported by Akhrem, Andreyuk, Kisel, and Kiselev (1989). A number of model studies have demonstrated interaction of myoglobin 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

Faustman, 1994 ). Yin and Faustman (1993) demonstrated Fig. 1. Lipid oxidation ( ― ) and

Fig. 1. Lipid oxidation () and oxymyoglobin oxidation (····) in 25% M. longissimus dorsi homogenates (H). , H; H+ FeCl 3 /ascorbate. abcde Oxymyoglobin oxidation, data points bearing different superscripts are signicantly different, P 0.05. wxy Lipid oxidation, data points bearing different superscripts are signi cantly different, P 0.05. Taken from O'Grady, Monahan and Brunton (2001) .

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

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greater lipid and myoglobin oxidation in liposomes with increased unsaturation of phosphatidylcholine used to construct liposomes. O'Grady, Monahan and Brunton (2001) utilized bovine muscle homogenates to study the interactions between lipid oxidation and OxyMb oxidation. They reported that OxyMb oxidation was enhanced by the process of lipid oxidation (Fig. 1) and this was likely due to primary rather than secondary products. Their results also suggested that lipid oxidation preceded OxyMb oxidation. Andersen and Skibsted (1991) suggested the reverse order of oxidation (i.e., myo- globin oxidation initiated prior to lipid oxidation) in salted ground pork. Similar to results obtained in vitro, OxyMb oxidation appears to be 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 added exogenously to postmortem muscle during processing. The parti- tioning of exogenously added antioxidants within muscle foods is critical to ef cacy ( Raghavan & Hultin, 2004, 2006 ). Some of the most convincing evidence for interplay between lipid and myoglo- bin oxidation in meat was provided by the observation that dietary supplementation of vitamin E delayed both of these processes in ground ( Faustman, Cassens, Schaefer, Buege, Williams, & Sheller, 1989 ) and whole-muscle beef cuts ( Faustman, Cassens, Schaefer, Buege, & Sheller, 1989; Kerry, Buckley, & Morrissey, 2000 ). Vitamin E, speci cally α -tocopherol, was long recognized as a fat-soluble lipid antioxidant for meat products prior to 1989 ( Faustman et al., 1989 ). A threshold concentration of α -tocopherol for achieving optimal protection of both lipid and myoglobin from oxidation was identi ed ( Arnold, Arp, Scheller, Williams, & Schaefer, 1993; Faustman, Cassens, Schaefer, Buege, & Sheller, 1989; Faustman, Cassens, Schaefer, Buege, Williams, et al., 1989 ), and evidence that dietary delivery of α -tocopherol was signi cantly more effective than exogenous addition for gaining maximal bene t was published ( Mitsumoto, 2000; Mitsumoto, Arnold, Schaefer, & Cassens, 1993 ). The latter was attributed to proper placement of α -tocopherol within the lipid bilayer where its normal physiological location facilitated its biological antioxidant function in postmortem muscle ( Faustman, Burr, & Liebler, 1999 ). In general, fresh forage contains greater concentrations of α -tocopherol than concentrate diets. Thus, a number of studies have reported that pasture feeding of cattle results in beef that has greater lipid and myoglobin redox stability than concentrate-fed animals ( Insani et al., 2008; Luciano et al., 2009 ). An important question has been how α-tocopherol protects the redox stability of myoglobin, a water-soluble protein known to reside in the cytoplasm ( Faustman & Wang, 2000). This has proven difcult to answer but our work has attempted to provide some potential mechanisms by which this could occur. Our major effort has fo- cused on the hypothesis that products of phospholipid unsaturated fatty acid oxidation can bind directly to myoglobin and lower its redox stability. Heme proteins are capable of binding to membranes ( Szebeni, Huser, Eskelson, Watson, & Winterhalter, 1988 ) and fatty acids ( Gotz, Hertel, & Groschel-Stewart, 1994) and this proximity would enhance the likelihood of interaction with products released as a consequence of lipid oxidation. Livingston and Brown (1981) noted that any perturbation in myoglobin conformation would be expected 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 models in which phospholipid fatty acid prole, phospholipid type and presence/absence of α-tocopherol could be controlled. Their results consistently showed that manipulation of liposomes that led to greater/more rapid oxidation of lipids also resulted in greater/more

rapid myoglobin oxidation. Support for this was provided initially by Chan, Faustman, and Decker (1997) when they incubated dialysis sacs containing OxyMb in solutions of liposomes differing in fatty acid unsaturation and presence/absence of α-tocopherol. Dialysis sacs provided a physical barrier that prevented outward diffusion and direct contact of OxyMb with liposomes, but allowed lipid oxi- dation products (mol. wt. b 500 Da) to diffuse inwards and potentially react with OxyMb. Greater degr ees of fatty acid unsaturation increased, and the presence of α -tocopherol decreased, the oxidation of both lipid and OxyMb. Results of this work led to studies of known secondary products of lipid oxidation, specically α,β-unsaturated aldehydes, as promoters of redox instability in OxyMb. Faustman, Liebler, McClure, and Sun (1999) reported that monounsaturated aldehydes (i.e., hexenal, heptenal, octenal, nonenal) enhanced MetMb formation from OxyMb more rapidly than their saturated counter- parts (hexanal, heptanal, octanal, and nonanal) or controls. Interest- ingly, monounsaturated aldehydes increased signicantly in their prooxidant capacity as chain length increased from six to nine carbons. As noted previously, HNE is a well-documented secondary product of linoleic acid oxidation. We have utilized HNE as a model oxidation product for our studies of interactions with myoglobin. HNE accelerates OxyMb oxidation by binding covalently to speci c histidine residues in the protein's primary sequence. This has been documented for bovine ( Alderton, Faustman, Liebler, & Hill, 2003; Suman, Faustman, Stamer, & Liebler, 2007 ), porcine ( Suman, Faustman, Stamer, & Liebler, 2006 ) and chicken and turkey myoglobins ( Maheswarappa et al., 2009; Naveena et al., 2010 ). Mass spectrometry and its tools have permitted identi cation of speci c HNE:histidine adducts in myoglobin. Interestingly, the effect of HNE alkylation on decreasing OxyMb redox stability is less pronounced at pH 5.6 than at 7.4, a result attributed to greater autoxidation and potentially decreased nucleophilicity of candidate histidine residues at this pH. Incubation of porcine OxyMb with porcine liver microsomes resulted 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 observed with similar models that included beef-derived microsomes ( Chan, Faustman, & Renerre, 1996; Chan, Hakkarainen, et al., 1996); this result was

Table 3

Compounds

identi ed

in muscle cytoplasm

that have

demonstrated antioxidant

activity.

Cytosolic

System

Reference

compound

Anserine

In vitro

Fu et al. (2009) Richards and Li (2004)

Ascorbate

Washed cod

muscle system

Carnitine

In vitro

Solarska, Lewinska, Karowicz-Bilinska, and Bartosz (2010) Badr (2007) He et al. (2008) Benjakul, Visessanguan, and Tanaka (2006) Tang, Faustman, Lee, and Hoagland (2003) Cheng, Fu, Porres, Ross, and Lei (1999)

Carnosine

Ground beef

Catalase

In vivo

Cysteine

In vitro

Glutathione

In vitro

Glutathione

In vivo

peroxidase

 

Lactate

Beef loins

Kim, Keeton, Smith, Maxim, Yang, and Savell (2009) Olek, Ziolkowski, Kaczor, Greci, Popinigis, and Antosiewicz (2004) Minard and McAlister-Henn (2001) Yiu, Juang, Fang, Liu, and Wu (2009) Zlotnik et al. (2008) Belle, Dalmolin, Fonini, Rubin, and Rocha (2004) Chen et al. (2009)

NADH

In vitro

NADPH

In vitro

Putrescine

In vivo

Pyruvate

In vivo

Spermine

In vivo

and spermidine

Superoxide

In vitro

dismutase

Urate

Milk

Ostdal, Andersen, and Nielsen (2000)

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

Table 4 Effect 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) Sasse, Colindres, and Brewer (2009); Rojas and Brewer (2008); Rojas and Brewer (2007) Ahn, Grün, and Mustapha (2007) Carpenter, O'Grady, O'Callaghan, O'Brien, and Kerry (2007) Lee and Kunz (2005) Sánchez-Escalante, Torrescano, Djenane, Beltrán, and Roncalés (2003a) Sánchez-Escalante, Torrescano, Djenane, Beltrán, and Roncalés (2003b) Tang and Cronin (2007) Sánchez-Escalante, Torrescano, Djenane, Beltrán and Roncalés (2003a,b) Ahn et al. (2007); Ahn, Grun, and Mustapha (2004) Nunez de Gonzalez, Boleman, Miller, Keeton and Rhee (2008) Lee and Ahn (2005) Sánchez-Escalante et al. (2003a) Kim, Godber, and Prinaywiwatkul (2000) Trindade, Mancini-Filho, and Villavicencio (2010); Georgantelis, Ambrosiadis, Katikou, Blekas, and Georgakis (2007); Nissen, Byrne, Bertelsen, and Skibsted (2004); Tanabe, Yoshida, and Tomita (2002) 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) 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)

Grape seed

Yes

No

Grape seed

Yes

Yes

Kimchi

Yes

NT

Lycopene

Yes

Yes

Lycopene

Yes

No

Onion

Yes

No

Oregano

Yes

Yes

Pine bark

Yes

Yes

Plum

Yes

NT

Plum

Yes

Yes

Red pepper

Yes

Yes

Rice ber

Yes

NT

Rosemary

Yes

NT

Rosemary

Yes

No

Rosemary

Yes

Yes

interesting because of the previously noted inconsistent effect of vitamin E supplementation on pork color stability relative to beef color stability ( Cannon et al., 1996; Houben, Eikelenboom, & Hoving- Bolink, 1998). Suman et al. (2006) provided evidence that differences in the primary sequences of bovine and porcine myoglobins, speci- cally the number and location of nucleophilic histidine residues, could be responsible, in part, for the observed differences in α-tocopherol efcacy for stabilizing meat color in pork and beef obtained from vitamin E-supplemented livestock. Ramanathan, Konda, Mancini, and Faustman (2009) subsequently reported that sarcoplasmic extracts of pork affected myoglobin redox stability less than beef sarcoplasmic extracts. Antioxidants have been identied in the cytoplasm of postmortem muscle ( Table 3) and have also been obtained from exogenous plant- based sources ( Table 4). The inclusion of a variety of antioxidants in fresh ( Mitsumoto et al., 1991) and irradiated ( Duong et al., 2008) meat/meat products has led to decreased lipid and myoglobin oxi- dation. Specic examples have included the addition of carnosine ( Decker, Chan, Livisay, Butereld, & 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) utilized an antioxidant cocktail containing a radical quencher (rosemary), chelator (citrate) and reductant (erythorbate) to stabilize ground meat enriched with an n-3 fatty acid emulsion. In addition to minimizing lipid oxidation, enhanced redness was also observed in fresh 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 that the two processes are linked. For example, meat from red deer ( Cervus elaphus ) that were allowed to graze versus those that were concentrate-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 oxidation than animals fed a concentrate diet while no differences in color stability were noted ( Sante-Lhoutellier, Engel, & Gatellier, 2008 ). Sesamol addition to porcine and bovine meat systems led to decreased lipid oxidation but enhanced OxyMb oxidation; addition of ellagic acid and olive leaf extract led to decreases in both oxi- dative processes ( Hayes, O'Brien, et al., 2009; Hayes, Stepanyan, et al., 2009 ). McBride, Hogan, and Kerry (2007) reported that extracts of rosemary minimized lipid oxidation, but were without effect relative to preservation of redness in fresh ground beef. Xiong et al. (2007) investigated the effect of cattle age on lipid and myoglobin stability in beef. They reported that meat from older animals had an increased rate of lipid oxidation, whereas OxyMb oxidation was only slightly impacted; meat from older animals has been noted to contain greater proportions of unsaturated fatty acids as a result of certain feeding regimens ( Warren et al., 2008 ). The unique relationship between pO 2 and myoglobin redox form such that low non-zero pO 2 favors met-heme formation ( Ledward, 1970 ) provides conditions in which the oxidative interac- tion is not tightly interconnected. The extent of lipid oxidation in meat is proportional to the concentration of oxygen present and would be expected to be minimal in low pO 2 environments. OxyMb redox stability is favored in high-oxygen atmospheres; lipid oxi- dation would occur readily in these conditions. Thus, atmospheres containing very high or very low concentrations of oxygen provide conditions in which the oxidative interaction between lipid and myoglobin is not tightly linked.

8. Final thoughts

Meat is a complex food system and any interactions between myoglobin and lipid oxidation ( Fig. 2 ) must be considered within the context of all biochemical activity occurring in postmortem muscle. For example, Monahan, Skibsted, and Andersen (2005) published results that considered a role for oxygen concentration in oxidative interactions. They utilized a beef homogenate in which the controlled introduction of oxygen was combined with a ferric

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

91

C. Faustman et al. / Meat Science 86 (2010) 86 – 94 91 Fig. 2. Summary

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

chloride/sodium ascorbate oxidation initiator to elucidate the mechanism of oxidative interactions. The model accommodated a high-oxygen environment that favored lipid oxidation and OxyMb stability, and the authors concluded that dissolved oxygen concentration was a critical consideration for OxyMb redox stability. They suggested that the consumption of oxygen resulting from the process of lipid oxidation was suf cient to accelerate OxyMb oxidation through the localized lowering of partial oxygen pressure. This very interesting study should be followed up by models that differ in dissolved oxygen concentration across the entire continuum from anoxic to saturating conditions. This study suggests that lipid oxidation would need to precede OxyMb oxidation if the processes were indeed linked. Dissolved oxygen in meat would not only be decreased by lipid oxidation, but also would be impacted by mitochondrial/sub- mitochondrial activity and metabolism of aerobic psychrotrophs. Tang et al. (2005) simultaneously measured lipid oxidation and MetMb formation in a model containing OxyMb and mitochondria that differed in concentration of α -tocopherol. Interestingly, mitochondria that contained greater tocopherol concentrations demonstrated greater oxygen consumption. This observation would make interpretation of antioxidant effects more dif cult.

That is, as per Monahan, Skibsted, and Andersen (2005) , the pres- ence of α -tocopherol would be hypothesized to slow lipid oxidation and the associated consumption of oxygen, however, mitochondria could be expected to be more active due presumably to the protective effect of the antioxidant on their membrane lipids and associated metabolism. Carefully designed experiments are needed to simultaneously address the different processes that contribute to the oxidative outcomes observed in meat. These would include a consideration 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 the process of OxyMb oxidation. One area ripe for future research is the careful characterization of the myo ber sarcoplasm and the role of its constituents on both inhibiting and enhancing oxidative reactions. Investigators have examined 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 to identify prooxidants ( Johns, Birkinshaw, & Ledward, 1989 ) and/or antioxidant 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 primarily responsible for lipid and/or myoglobin oxidation in meat. In other cases, strategies have been suggested for selectively removing prooxidant species (e.g., by precipitating iron-binding proteins; Gopalakrishnan et al., 1999 ) or enhancing the concentration and activity of naturally occurring antioxidants ( Chan, Decker, & Means, 1993; Decker & Xu, 1998 ). There are a large number of chemical compounds present in the sarcoplasm ( Decker & Mei, 1996 ) and the interactions between those in the low molecular- and high molecular-weight fractions is complex ( Li, Richards, & Undeland, 2005 ) and remains poorly understood. A complicating factor in such considerations is the fact that myoglobin is a sarcoplasmic protein ( Min & Ahn, 2009; Ramanathan et al., 2009 ); a method for selectively removing it from the muscle of meat-producing species as has been demonstrated in mice ( Garry et al., 1998 ) would provide an interesting model for future study.

Acknowledgements

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

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