The effects of antioxidant combinations on color and lipid oxidation in n − 3 oil fortified ground beef patties

Meat Science 70 (2005) 683–689 www.elsevier.com/locate/meatsci

The eVects of antioxidant combinations on color and lipid oxidation in n¡3 oil fortiWed ground beef patties S. Lee a, E.A. Decker b, C. Faustman

a,¤

, R.A. Mancini

a

a

b

Department of Animal Science, University of Connecticut, Storrs, CT 06269, USA Department of Food Science, University of Massachusetts, Amherst, MA 01003, USA

Received 30 September 2004; received in revised form 3 February 2005; accepted 3 February 2005

Abstract This study was carried out to determine an eVective combination of chelators, reductants and free radical scavengers for enhancing color stability and minimizing lipid oxidation in muscle foods fortiWed with n ¡ 3 fatty acids. Chelators (sodium tripolyphosphate, STPP; sodium citrate, CIT), reductants (sodium erythorbate, ERY) and radical scavengers (butylhydroxyanisole, BHA; mixed tocopherols from two diVerent sources, 30 or 95TOC; rosemary extract, ROSE) were incorporated in various combinations into ground beef (15% fat) with or without n ¡ 3 oil fortiWcation (n D 8). Individually, STPP and CIT had no signiWcant eVect on a* values except day 4, but showed higher a* values when combined with ERY (STPP + ERY and CIT + ERY) (P < 0.05). CIT had lower hue angle values than STPP on days 4 and 6, but CIT + ERY showed more discoloration than STPP + ERY (P < 0.05). CIT + ERY showed less lipid oxidation than CIT alone (P < 0.05), whereas there was no diVerence between STPP and STPP + ERY. CIT + ERY + ROSE demonstrated higher a* values than CIT + ERY + 95TOC on days 4 and 6 (P < 0.05); there was no diVerence between ROSE and 95TOC groups when n ¡ 3 oil was incorporated into ground beef patties (P > 0.05). The combination of ROSE and ERY appeared to be eVective in slowing the decline of a* values. All antioxidant combinations were eVective at delaying lipid oxidation when compared to CON or n ¡ 3. A combination of CIT, ERY and ROSE was most eVective for stabilizing color and delaying lipid oxidation.  2005 Elsevier Ltd. All rights reserved. Keywords: Sodium citrate; Sodium erythorbate; Rosemary; Color; n ¡ 3; Lipid oxidation

1. Introduction Skeletal muscle contains a multi-component antioxidant system that controls oxidative reactions in the live animal, and retains some activity in many muscle foods. The endogenous antioxidants of skeletal muscle, classiWed as lipid-soluble, cytosolic, or enzymatic, provide a level of natural oxidative stability to muscle in vivo (Decker & Mei, 1996). However, muscle foods are quite susceptible to oxidation and this is a major cause for quality deterioration. Susceptibility of muscle foods

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0309-1740/$ - see front matter  2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.meatsci.2005.02.017

to oxidative reactions is attributed to their high concentrations of prooxidants (i.e., transition metal and heme-containing proteins) (Rhee & Ziprin, 1987) and unsaturated lipids (Asgar, Gray, Buckley, Pearson, & Booren, 1988). Furthermore, meat processing operations facilitate particle size reduction and exposure of increased surface area (i.e., comminution and grinding), addition of potential prooxidant ingredients (i.e., sodium chloride) and heat-induced changes that decrease oxidative stability and overwhelm endogenous antioxidant capacity (Addis & Park, 1989; Xiong & Decker, 1995). Considerable research activity has focused on antioxidant ingredients added exogenously (Ahn, Wolfe, & Sim, 1993; Lee, Djordjevic, Park, Faustman, & Decker, 2003; Rhee, Krahl, Lucia, & AcuV, 1997), or via dietary

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supplementation (Faustman, 1993; Mitsumoto, Ozawa, Mitsuhashi, & Koide, 1998; Morrissey, Buckley, & Galvin, 2000). Exogenous antioxidants can be classiWed as chelators, reductants or free radical scavengers. Chelators control the activity of prooxidant metals and commonly include citric acid and phosphates (Badii & Howell, 2002; Trout & Dale, 1990). Ascorbate is one of the reducing agents capable of inhibiting lipid oxidation by inactivation of free radicals (Decker & Mei, 1996); the addition of ascorbate to fresh muscle foods can also maintain the reduced (ferrous) state of myoglobin (Shivas et al., 1984). The ultimate eVect of ascorbate on oxidative stability appears to be concentration-dependent. Low concentrations of ascorbate generate a prooxidant eVect (Ramanathanm & Das, 1992; St. Angelo, Vercellotti, Dupuy, & Spanier, 1988), whereas high concentrations of ascorbate appear to be antioxidative (Shantha, Crum, & Decker, 1994; St. Angelo et al., 1988). Erythorbate (D-isoascorbate) is a stereo-isomer of ascorbate with similar redox properties and is commonly added to foods. Free radical scavenging can be accomplished by synthetic phenolic antioxidants, such as butylated hydroxyanisole (BHA), butylated hydroxytoluene (BHT), propyl gallate and tertiary butylhydroquinone (TBHQ). In the US, the application of these antioxidant additives is limited to certain meat products (e.g., dry sausages, fresh ground pork), at 0.01% (w/w) individually, or 0.02% (w/ w) in combination based on the fat content of meat products. Tocopherols include four diVerent homologs (
, ,  and ) and occur naturally.
-Tocopherol has been reported to be an eVective inhibitor of lipid oxidation, and to stabilize oxymyoglobin when delivered by dietary means (Faustman, 1993). Mixed tocopherol isomers can also be incorporated as ingredients into muscle foods and appear to be more eVective than
-tocopherol (Decker & Crum, 1993). Several other natural phenolic antioxidants have been obtained from various plant extracts, and the most common commercial source of these is rosemary (Mielnik, Aaby, & Skrede, 2003). Long chain polyunsaturated n ¡ 3 fatty acids have been implicated as critical nutrients for human health, and fortiWcation of foods with n ¡ 3 polyunsaturated fatty acids is an emerging area of commercial and academic interest. However, incorporation of n ¡ 3 polyunsaturated fatty acids into food systems is potentially problematic due to their propensity to readily oxidize. A logical approach for countering the oxidative susceptibility would be to utilize a multi-component antioxidant approach to protect against oxidative susceptibility of lipids and neutralize prooxidants present in meat systems. The objective of the present study was to determine an eVective antioxidant combination involving chelators, reductants and free radical scavengers for stabilizing color and lipids in muscle foods fortiWed with n ¡ 3 fatty acids.

2. Materials and methods 2.1. Reagents Thiobarbituric acid (TBA), ethanol, trichloroacetic acid (TCA), and BHA were obtained from Sigma Chem. Co. (St Louis, MO., USA). Trisodium citrate, and mixed tocopherols (30% powered product, w/w; 95% liquid product, w/w) were obtained from DSM Nutritional Products, Inc. (Belvidere, NJ, USA), and sodium erythorbate was obtained from Continental Seasoning, Inc. (Teaneck, NJ, USA). Rosemary extract was obtained from Kalsec, Inc. (Kalamazoo, MI, USA). n ¡ 3 Fish oil (ROPUFA ‘30’; 30% n ¡ 3 polyunsaturated fatty acids including eicosapentaenoic acid, docosapentaenoic acid and docosahexaenoic acid) was obtained from DSM Nutritional Products, Inc. (Belvidere, NJ, USA). All chemicals were reagent/food grade or purer. 2.2. Hunter L*, a*, b*, and HUE angle Colorimetric values were determined by measurement with a Minolta Chroma Meter (Model CR-200b, Osaka, Japan) and Hue angle was calculated as tan¡1 (b*/ a*)*360°/2 (Chan et al., 1996). 2.3. Lipid oxidation The thiobarbituric acid (TBA) procedure of Yin, Faustman, Riesen, and Williams (1993) was used to assess lipid oxidation and reported as TBA-reactive substances (TBARS). 2.4. Sample preparation 2.4.1. Trial 1 Eight coarse ground beef chubs (4.52 kg; 85% lean, 15% fat; 19.2 mm) were obtained locally. Each chub was opened, mixed, and divided into six equally sized batches. Batches within a chub were randomly assigned to a treatment; a total of n D 8 experimental units were used (N D 48 total batches). Ground beef was treated with 0.5% sodium tripolyphosphate (STPP, w/w), 0.5% sodium citrate (CIT, w/w), 0.1% sodium erythorbate (ERY, w/w), STPP + ERY, or CIT + ERY. Antioxidant mixtures were prepared in distilled H2O (3%, w/w), and an equal volume of distilled H2O was added to controls (CON), and mixed by hand for 5 min. Batches of coarse ground beef were mixed with an assigned treatment, Wnely ground (5 mm), and formed into patties (5-cm dia. £1.5-cm thick, 25 g). Each of 4 patties from a batch was packaged on a tray, over-wrapped with oxygen-permeable PVC Wlm (15,500–16,275 cm3O2/m2/24 h at 23 °C), and assigned to a storage time (0, 2, 4 or 6 days; 1 patty per storage time). Color and lipid oxidation were monitored during storage at 4 °C (n D 8 patties per

S. Lee et al. / Meat Science 70 (2005) 683–689

treatment per storage time; N D 192 total patties). On a given storage day and for each patty, triplicate and duplicate observations were made for color and lipid oxidation, respectively. Sub-sample averages for each patty were used for statistical analyses. 2.4.2. Trial 2 Raw material and treatment application were similar to Trial 1 except that each chub was divided into eight equally sized batches, each of which was randomly assigned to a treatment. Ground beef was treated with 0.01% BHA (w/w, based on fat content), 0.03% mixed tocopherol (w/w, based on fat content; powdered product; 30TOC), 0.2% rosemary (w/w, ROSE), n ¡ 3 Wsh oil (n ¡ 3, 500 mg/110 g meat,), n ¡ 3 + BHA, n ¡ 3 + 30TOC and n ¡ 3 + ROSE. n ¡ 3 Wsh oil was added to the coarse ground beef directly with or without antioxidants, and mixed by hand for 5 min. BHA and ROSE were dissolved in ethanol (1.5%, w/w), and 30TOC was dissolved in distilled H2O (1.5%, w/w). Equal volumes of ethanol and distilled H2O were mixed, and added to CON. Patties were prepared and packaged as described above, and stored at 4 °C for 0, 2, 4 and 6 days. Color and lipid oxidation measurements were performed similar to Trial 1 (n D 8 patties per treatment per storage time; N D 256 total patties). 2.4.3. Trial 3 Raw material and treatment application were similar to Trial 1. Ground beef was treated with ERY (0.1%, w/w) + CIT (0.5%, w/w) + 0.03% mixed tocopherol (w/ w, based on fat content; liquid product; 95TOC), ERY + CIT + ROSE, n ¡3, n ¡3 + ERY + CIT + 95TOC and n ¡3 + ERY + CIT + ROSE. n ¡ 3 oil was mixed with the coarse ground beef as described in Trial 2. ERY and CIT were dissolved in distilled H2O (1.5%, w/w), and 95TOC and ROSE were dissolved in ethanol (1.5%, w/ w), and mixed by hand for 5 min. Equal volumes of ethanol and distilled H2O were mixed, and added to CON. Patties were prepared and packaged as described above, and stored at 4 °C for 0, 2, 4 and 6 days. Color and lipid oxidation measurements were performed similar to Trial 1 (n D 8 patties per treatment per storage time; N D 192 total patties). 2.5. Statistical analysis For all trials, the experimental design was a split-plot. For the whole plot, batches within each of eight chubs (blocks) were considered experimental units (n D 8) receiving treatments in a randomized complete block set up. The treatments had a one-way structure consisting of a control and antioxidants. From each batch within a chub, 1 of 4 patties (subplot experimental unit) was assigned a storage time (0, 2, 4 or 6 days). Data were analyzed using the mixed procedure of SAS (2001). Fixed eVects included treatment, time, and

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the treatment £ time interaction. Whole plot random eVects (error terms) included chub and chub (treatment). UnspeciWed residual error accounted for subplot time and treatment £ time eVects. Denominator degrees of freedom were estimated using the Satterthwaite procedure. Least square means for protected type three tests of Wxed eVects (F-test at P < 0.05) were separated using the diV option.

3. Results and discussion 3.1. Trial 1 The results for a* value and hue angle are presented in Fig. 1(a) and (b), respectively. There was a signiWcant treatment £ time interaction for a* values and hue angle (P < 0.05). When compared to CON, STPP or CIT alone had no eVect on a* value except at day 4; each combination of chelator plus ERY (STPP + ERY and CIT + ERY) showed higher a* values than the respective chelator alone (P < 0.05). On days 4 and 6, a* values for STPP + ERY were greater than CIT + ERY (P < 0.05). Antioxidant treatments appeared to delay discoloration relative to CON. Hue angle is calculated as a function of the colorimetric a* and b* values and correlates well with sensory panel assessment of meat discoloration (Chan et al., 1996; Giroux et al., 2001; Isdell, Allen, Doherty, & Butler, 1999). CIT alone had lower hue angle values than STPP alone on days 4 and 6, but CIT plus ERY (CIT + ERY) showed greater hue angle values than STPP + ERY (P < 0.05; Fig. 1(b)). There were no eVects of antioxidant treatments on b* values (P > 0.05) (results not shown). The eVects of antioxidant treatments on lipid oxidation (TBARS) in ground beef are presented in Fig. 2. There was a signiWcant treatment £ time interaction in TBARS (P < 0.05). Antioxidant-treated groups delayed lipid oxidation when compared to CON (P < 0.05). CIT + ERY showed less lipid oxidation than CIT alone (P < 0.05). STPP alone tended to minimize lipid oxidation (P < 0.05); there was no diVerence between STPP and STPP + ERY (P > 0.05). These results suggested that when combined with ERY, STPP was more eVective than CIT in delaying lipid oxidation. ERY was utilized as a reducing agent and would be expected to behave similarly to its isomer, ascorbate. Ascorbate has been reported to act as an antioxidant or prooxidant depending on its concentration, the presence of metal ions, and tocopherol concentration (Schaefer, Liu, Faustman, & Yin, 1995). The concentration of ERY in the present study was 1000 ppm, a concentration expected to provide an antioxidant eVect (Kanner & Mendel, 1977; Mitsumoto, Cassens, Schaefer, & Scheller, 1991). Ground beef with ERY alone demonstrated greater TBARS values than ERY combined with chelators. Halliwell and Gutteridge (1985) reported that

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50 CON STPP CIT ERY STPP+ERY CIT+ERY

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a* value

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CON STPP CIT ERY STPP+ERY CIT+ERY

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Fig. 2. Lipid oxidation (TBARS) in control and antioxidant treated ground beef patties during storage at 4 °C. CON, control; sodium tripolyphosphate, STPP; sodium citrate, CIT; sodium erythorbate, ERY; sodium tripolyphosphate with sodium erythorbate, STPP + ERY; sodium citrate with sodium erythorbate, CIT + ERY (n D 8). Standard deviation bars are indicated, and standard error of means (SEM) is 0.004.

160

Hue angle

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CON STPP CIT ERY STPP+ERY CIT+ERY

than when ERY was combined with CIT or STPP is not surprising. These results are supported by Madhavi, Singhal, and Kulkarni (1995) who reported that ascorbic acid could shift the redox potential of a food system to the reducing range and act eVectively with chelators for the purpose of minimizing lipid oxidation.

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3.2. Trial 2 100

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60 0

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Fig. 1. a* Values (redness) (a) and hue angle (b) in control and antioxidant treated ground beef patties during storage at 4 °C. CON, control; sodium tripolyphosphate, STPP; sodium citrate, CIT; sodium erythorbate, ERY; sodium tripolyphosphate with sodium erythorbate, STPP + ERY; sodium citrate with sodium erythorbate, CIT + ERY (n D 8). Standard deviation bars are indicated, and standard error of means (SEM) for a* values is 0.292 and for hue angle is 1.249.

ascorbate could reduce metal ions and scavenge singlet oxygen. In contrast, the involvement of ascorbate in Fenton reactions can stimulate oxidation because ascorbate can donate an electron to Fe3+ to form the more prooxidant reduced ferrous species (Schaefer et al., 1995). In this study, CIT and STPP were added to chelate potential prooxidant metal ions. The observation that more lipid oxidation was observed in ERY alone

Several diVerent radical scavengers were incorporated into ground beef patties with and without n ¡ 3 oil. There was a signiWcant treatment £ time interaction for a* values (P < 0.05), but no interaction found in hue angle (P > 0.05). The n ¡ 3 + ROSE combination showed greater a* values than n ¡ 3 + 30TOC on days 4 and 6 (P < 0.05) (Fig. 3(a)), and lower hue angle values were observed in n ¡ 3 + ROSE compared to n ¡ 3 + 30TOC (P < 0.05) (Fig. 3(b)). No treatment by time interaction was observed for L* values (P > 0.05; results not shown). There was a signiWcant treatment £ time interaction for TBARS (P < 0.05). BHA and ROSE inhibited lipid oxidation when ground meat was fortiWed with n ¡ 3 oil (P < 0.05); 30 TOC did not minimize lipid oxidation regardless of n ¡ 3 oil fortiWcation (P > 0.05) (Fig. 4(a) and (b)). ROSE appeared to be as eVective as BHA for minimizing lipid oxidation (P < 0.05). ROSE contains several phenolic compounds that possess antioxidant activity including carnosic acid, carnosol, rosmarinic acid, rosmanol and rosmaridiphenol (Shahidi & Wanasundara, 1992). The variety of these, their polyphenolic nature, and the fact that all antioxidative ingredients were applied based on manufacturer recommendations rather than on an equimolar basis, contributed to the observation of their apparent eVectiveness in delaying lipid oxidation

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0.25

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160 CON BHA 30TOC ROSE n-3 n-3+BHA n-3+30TOC n-3+ROSE

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Fig. 4. Lipid oxidation (TBARS) in control and antioxidant treated ground beef patties without (a) or with n ¡ 3 Wsh oil (b) during storage at 4 °C. CON, control; butylated hydroxyanisole, BHA; 30% mixed tocopherol, 30TOC; rosemary, ROSE; n ¡ 3 Wsh oil, n ¡ 3 (500 mg/ 110 g meat); n ¡ 3 Wsh oil with BHA, n ¡ 3 + BHA; n ¡ 3 Wsh oil with 30% mixed tocopherol, n ¡ 3 + 30TOC; n ¡ 3 Wsh oil with rosemary, n ¡ 3 + ROSE (n D 8). Standard deviation bars are indicated, and standard error of means (SEM) is 0.004.

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Fig. 3. a* Values (redness) (a) and hue angle (b) in control and antioxidant treated ground beef patties during storage at 4 °C. CON, control; butylated hydroxyanisole, BHA; 30% mixed tocopherol, 30TOC; rosemary, ROSE; n ¡ 3 Wsh oil, n ¡ 3 (500 mg/110 g meat); n ¡ 3 Wsh oil with BHA, n ¡ 3 + BHA; n ¡ 3 Wsh oil with 30% mixed tocopherol, n ¡ 3 + 30TOC; n ¡ 3 Wsh oil with rosemary, n ¡ 3 + ROSE (n D 8). Standard deviation bars are indicated, and standard error of means (SEM) for a* values is 0.466 and for hue angle is 0.991.

n ¡ 3 Wsh oil added to ground beef patties in this study contained long chain polyunsaturated fatty acids that are very susceptible to lipid oxidation. In this study, n ¡ 3 addition was expected to result in more lipid oxidation than CON, but CON showed more lipid oxidation than n ¡ 3 (P < 0.05; Fig. 4(a) and (b)). It is possible that the small amount of mixed tocopherols incorporated into the Wsh oil preparation for emulsion stabilization was suYcient to minimize oxidation relative to CON. 3.3. Trial 3

especially when compared to 30TOC. In addition, ROSE is dispersible in aqueous solutions and might be expected to more readily incorporate into meat products than vitamin E or BHA preparations (Trout & Dale, 1990). It has been reported that ROSE is a powerful natural antioxidant, more eVective than synthetic antioxidants (Houlihan, Ho, & Chang, 1985; Nakatani & Inatani, 1984). The

A signiWcant treatment £ time interaction was observed in a* values and hue angle (P < 0.05). CIT + ERY + ROSE demonstrated greater a* values than CIT + ERY + 95TOC without n ¡3 oil on days 4 and 6 (P < 0.05; Fig. 5(a)); there was no diVerence between ROSE and 95TOC treatments when combined with n ¡3

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oil in ground beef patties (P > 0.05). Sanchez-Escalante, Djenane, Torrescano, Beltran, and Roncales (2001) reported that rosemary powder stabilized the redness of beef patties during 12 days of storage, and this eVect was further enhanced by the presence of ascorbic acid. Our results also showed that the combination of ROSE and 50 CON CIT+ERY+95TOC CIT+ERY+ROSE n-3 n-3+CIT+ERY+95TOC n-3+CIT+ERY+ROSE

45

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a* value

35

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ERY appeared to have a protective eVect on redness during storage. No diVerences were observed for hue angle values (P > 0.05; Fig. 5(b)) between ROSE and 95TOC groups, however, antioxidant treatments were remarkably eVective in preventing discoloration when compared to CON and n ¡3 only treatments (Fig. 5(b)). CIT + ERY + ROSE had greater L* values than CIT + ERY + 95TOC during storage; there was no treatment £ time eVect for b* values (P > 0.05; results not shown). A signiWcant treatment £ time interaction was observed for TBARS (P < 0.05). All antioxidant combinations delayed lipid oxidation when compared to CON or n ¡3 only treatments (P < 0.05; Fig. 6), and eVects on minimizing lipid oxidation were readily observed. As observed in Trial 2, CON patties had more lipid oxidation than n ¡3 treated patties, and our only explanation for this observation was the presence of mixed tocopherols, added commercially to the Wsh oil preparation for stabilization.

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4. Conclusion

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Dietary n ¡3 polyunsaturated fatty acids are important for promotion and maintenance of good health, and the fortiWcation of muscle foods represents a potentially eVective dietary delivery mechanism for n ¡3 polyunsaturated fatty acids. However, an eVective antioxidant approach is necessary for protecting n ¡3 polyunsaturated fatty acids against lipid oxidation due to their unsaturated nature and prooxidants present in meat systems. Various chelators (sodium tripolyphosphate; sodium citrate), radical scavengers (BHA; mixed tocopherols;

Hue angle

0.20 CON CIT+ERY+95TOC CIT+ERY+ROSE n-3 n-3+CIT+ERY+95TOC n-3+CIT+ERY+ROSE

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Fig. 5. a* Values (redness) (a) and hue angle (b) in control and antioxidant treated ground beef patties during storage at 4 °C. CON, control; sodium erythorbate with sodium citrate and 95% mixed tocopherol ERY + CIT + 95TOC; sodium erythorbate with sodium citrate and rosemary, ERY + CIT + ROSE; n ¡ 3 Wsh oil, n ¡ 3 (500 mg/110 g meat); n ¡ 3 Wsh oil with sodium erythorbate, sodium citrate and 95% mixed tocopherol, n ¡ 3 + ERY + CIT + 95TOC; n ¡ 3 Wsh oil with sodium erythorbate, sodium citrate and rosemary, n ¡ 3 + ERY + CIT + ROSE (n D 8). Standard deviation bars are indicated, and standard error of means (SEM) for a* values is 0.560 and for hue angle is 1.293.

0.00 0

2

4

6

Days of Storage Fig. 6. Lipid oxidation (TBARS) in control and antioxidant treated ground beef patties during storage at 4 °C. CON, control; sodium erythorbate with sodium citrate and 95% mixed tocopherol ERY + CIT + 95TOC; sodium erythorbate with sodium citrate and rosemary, ERY + CIT + ROSE; n ¡ 3 Wsh oil, n ¡ 3 (500 mg/110 g meat); n ¡ 3 Wsh oil with sodium erythorbate, sodium citrate and 95% mixed tocopherol, n ¡ 3 + ERY + CIT + 95TOC; n ¡ 3 Wsh oil with sodium erythorbate, sodium citrate and rosemary, n ¡ 3 + ERY + CIT + ROSE (n D 8). Standard deviation bars are indicated, and standard error of means (SEM) is 0.002.

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rosemary extract), and reductants (sodium erythorbate) were incorporated in various combinations into ground beef (15% fat) with or without n ¡ 3 oil fortiWcation. Antioxidant combinations in the present study had beneWcial eVects on stabilizing color and lipids. Our results suggest that a combination of CIT (sodium citrate), ERY (sodium erythorbate), and ROSE (rosemary) was most eVective.

Acknowledgements This work was supported by the USDA-IFAFS program, and the Storrs Agricultural Experiment Station, University of Connecticut, Storrs, Connecticut.

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