Oxidative Stability of Dark Chicken Meat Through Frozen Storage: Influence of Dietary Fat and α-Tocopherol and Ascorbic Acid Supplementation

Oxidative Stability of Dark Chicken Meat Through Frozen Storage: Influence of Dietary Fat and α-Tocopherol and Ascorbic Acid Supplementation A. Grau,* F. Guardiola,*,1 S. Grimpa,* A. C. Barroeta,† and R. Codony* *Nutrition and Food Science Department-CeRTA, Faculty of Pharmacy, University of Barcelona, Avinguda Joan XXIII s/n, E-08028 Barcelona, Spain; and †Unitat Docent de Nutricio´ i Alimentacio´ Animal, Facultat de Veterina`ria, UAB, E-08193 Bellaterra, Spain AA provided no protection, and no synergism between α-TA and AA was observed. Polyunsaturated fatty acidenriched diets (those containing linseed, sunflower, or oxidized sunflower oils) increased meat susceptibility to oxidation. Cooking always involved more oxidation, especially in samples from linseed oil diets. The values of all the oxidative parameters showed a highly significant negative correlation with the α-tocopherol content of meat.

(Key words: ascorbic acid, chicken leg meat, dietary fat, lipid oxidation, α-tocopherol) 2001 Poultry Science 80:1630–1642

INTRODUCTION Meat composition can be modified by diet. Animals fed on diets rich in unsaturated fats have increased the polyunsaturated fatty acid (PUFA) content of their lipid fraction (Lin et al., 1989a; Ajuyah et al., 1993; Ahn et al., 1995; Mooney et al., 1998; Lo´pez-Ferrer et al., 1999). This modification is nutritionally desirable, but it increases susceptibility of meat to oxidation. Nevertheless, this drawback can be overcome by dietary supplementation with antioxidants. Among these, the protective role of αtocopheryl acetate (α-TA) is unquestionable (Jensen et al., 1998), whereas that of other compounds such as carotenoids or ascorbic acid (AA) remains to be established (Pardue and Thaxton, 1986; King et al., 1995; Erickson, 1998; Ruiz et al., 1999). Dietary modulation of the composition of meat may enable us to improve its oxidative stability and thus increase the nutritional value and the shelf life of meat products. The oxidative status of meat can be assessed on the basis of primary oxidation [i.e., through the measurement of lipid hydroperoxide (LHP) value] or secondary oxidation [i.e., through the measurement of malondialdehyde (MDA), or cholesterol oxidation products (COP)]. 2001 Poultry Science Association, Inc. Received for publication December 15, 2000. Accepted for publication July 2, 2001. 1 To whom correspondence should be addressed: e-mail: fibarz@ farmacia.far.ub.es.

The ferrous oxidation-xylenol orange (FOX) method has been reported to be a simple, sensitive, precise, and specific way to measure LHP (Jiang et al., 1992; Shantha and Decker, 1994; Burat and Bozkurt, 1996; NouroozZadeh, 1998). This assay consists of the peroxide-mediated oxidation of ferrous ions in an acidic medium containing the dye xylenol orange, which binds the resulting ferric ions to produce a blue-purple complex with a maximum absorbance between 550 and 600 nm. This method has been adapted for dark chicken meat samples (Grau et al., 2000b) showing a high specificity for LHP. With regard to the measurement of MDA, the aqueous acid extraction methods [reaction of an aqueous acid extract of MDA with 2-thiobarbituric acid (TBA) to give a red complex absorbing at 530 to 537 nm] seem to be the most appropriate for routine assessment of lipid oxidation in meat and meat products (Witte et al., 1970; Pikul et al., 1989; Raharjo and Sofos, 1993). However, these methods have been criticized for their lack of sensitivity and specificity, as compounds other than MDA can also react with TBA, giving interfering complexes with absorption at the same (530 to 537 nm) or similar wave lengths (450 to 460 nm) than the MDA-TBA adduct (Ko-

Abbreviation Key: AA = ascorbic acid; BT = beef tallow; COP = cholesterol oxidation product; FOX = ferrous oxidation-xylenol orange; LHP = lipid hydroperoxide; LO = linseed oil; MDA = malondialdehyde; OSO = oxidized sunflower oil; PUFA = polyunsaturated fatty acid; SO = sunflower oil; α-TA = α-tocopheryl acetate.

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ABSTRACT We used factorial design to ascertain the influence of dietary fat source (linseed, sunflower and oxidized sunflower oils, and beef tallow) and the dietary supplementation with α-tocopheryl acetate (α-TA) (225 mg/kg of feed) and ascorbic acid (AA) (110 mg/kg) on dark chicken meat oxidation (lipid hydroperoxide and TBA values and cholesterol oxidation product content). α-TA greatly protected ground and vacuum-packaged raw or cooked meat from fatty acid and cholesterol oxidation after 0, 3.5, or 7 mo of storage at −20 C. In contrast,

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EFFECT OF DIET ON CHICKEN MEAT OXIDATION TABLE 1. Ingredients and composition of the basal diet Ingredients and composition

Percentage

Corn Corn germ meal Soybean meal, 44% protein Sorghum Sunflower meal Barley Rye Beef tallow Calcium carbonate Dicalcium phosphate Sepiolite Salt Sodium bicarbonate Trace mineral-vitamin mix1 Composition2 Dry matter Crude protein Crude fat Crude fiber Ash

30.0 18.4 17.4 10.0 8.0 5.8 5.0 0.1 1.9 1.4 1.0 0.3 0.1 0.5 88.2 16.0 4.1 5.1 7.4

1

Did not include vitamin E. Metabolizable energy, 2,750 Kcal/kg.

2

randomly placed in 48 pens (five birds per pen). Dietary treatments were randomly distributed; three pens were assigned to each treatment, and broiler chickens were fed ad libitum for 50 d.

MATERIALS AND METHODS Experimental Design A 4 × 2 × 2 × 3 factorial design was planned and conducted in triplicate to study the influence of various dietary factors (four types of fat source and two levels of α-TA and AA supplementation) and storage periods (0, 3.5, and 7 mo) at −20 C on several parameters (α-tocopherol content, fatty acid composition, LHP and TBA values, and COP content) in raw and cooked dark chicken meat.

Dietary Treatments and Animals Sixteen isocaloric dietary treatments were prepared from a basal diet (Table 1) by the following combination of the dietary factors studied (4 × 2 × 2): fat source2 [beef tallow (BT), sunflower oil (SO), oxidized sunflower oil (OSO), and linseed oil (LO); 6% fat supplementation in all cases]; α-TA (0 and 225 mg/kg of feed); and AA (0 and 110 mg/kg of feed).3 Sunflower oil [unrefined; specific absorbances at 232 (K232) and 270 nm (K270) were 2.87 and 0.25, respectively] was oxidized by heating in a fryer for 12 h at 160 C and then leaving the oil in the fryer at room temperature for 6 d (K232 = 4.40, K270 = 0.83). Specific absorbances were measured as described by Guardiola et al. (1995). Two hundred forty female broiler chicks (Ross, 1 d old) were fed a control diet for 6 d. One-week-old birds were

2

Dietary fats supplied by Caila` i Pare´s S.A., E-08040 Barcelona, Spain. α-TA (Rovimix威 E-50 Adsorbate) and AA (Rovimix威 C) were from Hoffmann-La Roche, Ltd., CH-4070 Basel, Switzerland. 3

Sample Preparation Broiler chickens (57 d old) were leg-ringed and slaughtered according to commercial procedures at the Avicola Maria slaughterhouse (Begur, Spain). Carcasses were transported to the Cuit’s processing plant (Cassa` de la Selva, Spain) and stored for 3 d at 4 C in a walk-in cooler. Legs with skin from each pen were divided into two groups. One group of legs was hand deboned, ground, vacuum-packaged in 13.5 × 16-cm polyamide/polyethylene bags and stored for 0, 3.5, or 7 mo at 20 C. The other group of five legs was hand deboned. Two legs of this group were vacuum-packaged in 20 × 40-cm polyamide/ polyethylene bags and cooked at 80 C for 35 min in a pressure cooker. Thereafter, these two cooked legs were ground, vacuum-packaged in 13.5 × 16-cm polyamide/ polyethylene bags, and stored at −20 C for 0, 3.5, or 7 mo. The remaining three legs were vacuum-packaged in 20 × 40-cm polyamide/polyethylene bags, cooked at 80 C for 35 min in a pressure cooker, and stored for 13 mo at −20 C until sensory analysis and TBA value determination (Figure 1). Permeability to oxygen of all bags used was 50 cm3ⴢbarⴢ24 h (Deutsches Institut fu¨r Normung; 53,380, 23 C). Results from sensory analysis have been discussed in a previous work (Bou et al., 2001).

Analysis of Samples Lipid hydroperoxide values were assessed according to the FOX method described by Grau et al. (2000b). Reaction mixtures containing 75 µL of sample extract were incubated for 4 h.

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sugi et al., 1987; Guille´n and Guzman, 1988; Raharjo and Sofos, 1993; Botsoglou et al., 1994). To overcome these drawbacks, Botsoglou et al. (1994) proposed an acid aqueous extraction method using third-derivative spectrophotometry, which removes the main sources of interference. Their method was further studied in order to be applied to chicken meat samples (Grau et al., 2000c). Finally, the determination of COP content in foods of animal origin has also been used as a parameter to measure lipid oxidation (Paniangvait et al., 1995; Addis et al., 1996). Another interest of this determination relies on the potentially harmful effects of these compounds (Guardiola et al., 1996; Brown and Jessup, 1999). The first choice method for this analysis consists of lipid extraction, COP enrichment, and gas chromatography (Addis et al., 1996; Guardiola et al., 1998). A method following these steps has been adapted to dark chicken meat samples (Grau et al., 2000a). The goal of this paper was to study the influence of the dietary fat source, α-TA and AA supplementations, and cooking on the oxidative stability of dark chicken meat samples vacuum-packaged and stored at −20 C for 0, 3.5, and 7 mo. Our discussion is based on the results of several oxidative parameters (LHP and TBA values and COP content).

1632 GRAU ET AL. FIGURE 1. Experimental design. This experimental design was conducted in triplicate (80 × 3 female broiler chicks were randomly assigned to 16 × 3 treatments). AA = ascorbic acid supplementation in mg/kg of feed; BT = beef tallow; COP = cholesterol oxidation product; LHP = lipid hydroperoxide; LO = linseed oil; OSO = oxidized sunflower oil; SO = sunflower oil; α-TA = α-tocopheryl acetate supplementation in mg/kg of feed. One leg of each bird in each group of legs.

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EFFECT OF DIET ON CHICKEN MEAT OXIDATION

RESULTS AND DISCUSSION Influence of Dietary Factors The dietary fat significantly influenced the values of the oxidation parameters in both raw and cooked dark chicken meat stored for 0, 3.5, or 7 mo at −20 C, except for LHP values in raw samples stored for 0 or 3.5 mo (Table 2). At any storage time, raw and cooked samples from chickens fed BT or LO diets gave the lowest and the highest TBA values, respectively. Other authors also reported higher TBA values for chicken leg meat from unsaturated fat sources (Lin et al., 1989a; Ajuyah et al., 1993; Ahn et al., 1995; Maraschiello et al., 1999; Ruiz et al., 1999), and, as in our case, it is a consequence of the higher PUFA content in meats from unsaturated diets (Table 3). When the fat source significantly influenced LHP values, samples from diets containing unsaturated fat sources also gave the highest values. In contrast, the highest COP content for raw and cooked samples was observed in SO- and BT-fed groups, respectively. The cholesterol content of samples cannot account for this effect of dietary fat on COP content, as there were no significant differences between the cholesterol content of meat from different fat sources (Table 3). Li et al. (1996) also failed to find any differences in cholesterol content in freeze-dried chicken breast meat samples from animals fed diets supplemented with fish, flax, palm, or sunflower oils. Feeding OSO did not significantly increase the oxidation of dark chicken meat (Table 2). However, other stud-

ies carried out with chickens fed on diets containing similar amounts of OSO reported significantly higher TBA values as a result of feeding oxidized oil (Lin et al., 1989b; Galvin et al., 1993, 1997). In addition, Galvin et al. (1993) and Sheehy et al. (1993, 1994) showed that ferrous-ascorbate-induced lipid oxidation in chicken tissue homogenates (measured by TBA values after incubation at 37 C) was much higher for the OSO-fed group than for the SOfed group. This finding is consistent with the finding that in cooked samples TBA values tended to be higher for OSO groups, although it was not significant (Table 2). However, as argued by Monahan et al. (1992), lack of a clear prooxidant effect of dietary OSO could be attributed to an insufficient degree of oxidation of the heated SO. We do not accept the dose of the oxidized oil as a cause of this absence of significant effect, because the amount of oil used by Lin et al. (1989b), Sheehy et al. (1993, 1994), and Galvin et al. (1993, 1997) ranged from 40 to 80 g/kg of feed and that used in our study was 60 g/kg. Specific absorbances at 232 and 270 nm were, respectively, 2.87 and 0.25 for the SO and 4.40 and 0.83 for the OSO, which indicates that conjugated dienes in OSO were only approximately 1.5-fold greater than in SO. Thus, PUFA peroxide content in our OSO is much lower than in OSO used by other authors (Lin et al., 1989b; Galvin et al., 1993, 1997; Sheehy et al., 1994). Moreover, these studies reported that supplying oxidized oils decreased plasma and muscle α-tocopherol levels. This result was attributed to the destruction of the endogenous α-tocopherol of SO during heating, the destruction of α-tocopherol in the gastrointestinal tract by free radicals from the oxidized oil, and the absorption of LHP, resulting in a higher rate of oxidation and higher consumption of α-tocopherol in vivo. Despite that earlier studies indicated that LHP were not absorbed in the intestinal tract (Andrews et al., 1960; Bunyan et al., 1968), it has been recently shown that, in humans, LHP are absorbed and incorporated into chylomicrons to some extent (Naruszewicz et al., 1987; Stapra˜ns et al., 1994). In addition, studies conducted in rats showed that levels of LHP in serum very-low-density lipoprotein plus low-density lipoprotein fraction correlated with LHP in the diet (Stapra˜ns et al., 1993). Thus, chylomicrons could deliver LHP to the liver, where they could be secreted in very-low-density lipoprotein and therefore to reach peripheral tissues. However, in the present study, although the α-tocopherol content of meat samples from OSO diets was slightly lower than that from SO, this difference was not significant (Table 2). This finding is possibly due to the low LHP level of the OSO. Furthermore, Galvin et al. (1997) reported that, in cooked ground breast or leg chicken meat stored for different periods at 4 or −20 C, samples from OSO diets always resulted in higher TBA values than those from SO. In contrast, in our study, no significant differences were detected between OSO- and SO-fed groups during the 7 mo of frozen storage. α-TA supplementation resulted in a significant protection against oxidation for both raw and cooked samples at any storage time, which was reflected by all the oxidation

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Thiobarbituric acid values were determined by an acid aqueous extraction method with third-derivative spectrophotometry, as described by Grau et al. (2000c). Analyses for COP and cholesterol content were performed as described by Grau et al. (2000a). Fatty acid composition and α-tocopherol content were determined as in Grau et al. (2000b). For all analytical methods, reagents and standards used were previously detailed by Grau et al. (2000a,b,c). Statistics. To determine whether the factors studied (fat source, α-TA and AA supplementations, cooking, and storage time) had any significant effect on the responses, 12 multifactor ANOVA were performed as follows: (1 to 3) raw samples at 0, 3.5, and 7 mo, respectively (n = 48); (4) all raw samples (0 + 3.5 + 7 mo, n = 144); (5 to 8) the same for cooked samples; (9) raw + cooked samples at 0 mo (n = 96); (10 and 11) the same at 3.5 and 7 mo, respectively, and (12) all samples (raw + cooked at 0 + 3.5 + 7 mo, n = 288). In all cases, interactions higher than order two were ignored and P ≤ 0.05 were considered to be significant. When dietary fat source or storage time showed a significant effect, the Scheffe´ test for a posteriori contrasts (α = 0.05) was applied to determine statistical differences between least-squares means. Pearson correlation coefficients were used to examine possible linear correlations between responses (LHP values, TBA values, COP content, and α-tocopherol content).

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GRAU ET AL.

parameters (Table 2). The decrease in TBA and COP values as a consequence of dietary tocopherols has been reported by several authors and has been attributed to the accumulation of the dietary α-tocopherol in muscle tissues of chickens (Lin et al., 1989a; Ajuhah et al., 1993; Ahn et al., 1995; Jensen et al., 1995; King et al., 1995; de Winne and Dirinick, 1996; Li et al., 1996; Lauridsen et al., 1997a; O’Neill et al., 1998; Marashiello et al., 1999; Ruiz et al., 1999). In fact, from our data, supplementation of broiler diets with 225 mg of α-TA/kg of feed led to an overall increase of tocopherol in meat of 39.19 and 35.56 mg/kg for raw and cooked samples, respectively (Table

2). In contrast, no studies have been found concerning LHP values in chicken meat from animals fed tocopherolsupplemented diets. AA supplementation resulted in a prooxidant effect in terms of TBA values, which was only significant for raw meat (at all storage times) (Table 2). For the other oxidation parameters, the effect of dietary supplementation with AA was not significant in any case. In fact, whether AA prevents or promotes lipid oxidation in meat is controversial (Benedict et al., 1975; Bartov, 1977; Pardue and Thaxton, 1986; King et al., 1995; Lauridsen et al., 1997b). Low concentrations of AA in meat lead to a prooxidant

Responses2 0 mo of storage LHP valueDE TBA valueABCDE α-Tocopherol contentE 3.5 mo of frozen storage LHP valueAE TBA valueABDE α-Tocopherol contentA 7 mo of frozen storage LHP valueAD TBA valueABDE Total COPABE α-Tocopherol contentE

α-TA supplementation (mg/kg of feed)

Fat source

AA supplementation (mg/kg of feed)

Meat

Global means

BT

SO

OSO

LO

0

225

0

110

Raw Cookeda Rawabc Cookeda Raw Cooked

199.5X 155.4*,X 0.566 3.969*,X 23.2 18.1*

183.7 124.7z 0.155x 2.554z 25.2 16.0

205.7 162.2xy 0.404y 3.186yz 23.5 21.5

215.6 153.8y 0.262y 3.562y 21.8 17.8

193.0 181.0x 1.445x 6.574x 21.9 16.9

381.3x 287.1x 1.041x 5.024x 3.9y 1.7y

17.7y 23.8y 0.092y 2.914y 42.5x 34.4x

201.9 160.1 0.396y 3.854 22.9 17.6

197.2 150.8 0.736x 4.084 23.3 18.5

Raw Cookeda Rawabc Cooked Rawa Cookeda

162.3Y 192.3*,Y 0.610 3.521*,Y 24.0 20.5*

141.9 147.6y 0.184y 2.347z 26.7 19.8

173.3 199.0x 0.509y 2.802yz 26.5 23.4

174.2 210.0x 0.341y 3.158y 21.3 20.8

159.8 212.8x 1.407x 5.778x 21.7 17.8

312.7x 363.1x 1.095x 4.465x 3.7y 1.7y

11.9y 21.6y 0.125y 2.577y 44.8x 39.2x

156.9 194.7 0.478y 3.459 23.4 20.8

167.7 190.0 0.743x 3.584 24.7 20.1

Raw Cookeda Rawabc Cooked Rawab Cooked Raw Cooked

169.4Y 182.1*,Y 0.683 3.468*,Y 1.50 3.26* 22.5 19.7*

150.0y 135.5y 0.273y 2.306y 1.26x 3.70x 24.6 19.2

174.8xy 198.3x 0.571y 2.760y 1.90y 3.59x 24.1 21.7

180.5x 196.5x 0.454y 3.092y 1.42x 3.31x 20.9 20.2

172.2xy 198.1x 1.436x 5.715x 1.43x 2.45y 20.6 17.8

327.4x 344.3x 1.174x 4.435x 2.15x 4.20x 3.5y 1.5y

11.4y 19.9y 0.192y 2.502y 0.85y 2.33y 41.6x 37.9x

167.9 186.6 0.558y 3.407 1.42 3.40 22.7 19.9

170.8 177.6 0.809x 3.530 1.58 3.13 22.4 19.5

a Interaction of dietary fat source × α-TA supplementation significant at P ≤ 0.05. P-values obtained from multivariate ANOVA (MANOVA) (n = 48) for raw or cooked samples. A Interaction of dietary fat source × α-TA supplementation significant at P ≤ 0.05. P-values obtained from MANOVA for all raw and cooked samples together (n = 96). b Interaction of dietary fat source × AA supplementation significant at P ≤ 0.05. P-values obtained from MANOVA (n = 48) for raw or cooked samples. B Interaction of dietary fat source × AA supplementation significant at P ≤ 0.05. P-values obtained from MANOVA for all raw and cooked samples together (n = 96). c Interaction of α-TA × AA supplementation significant at P ≤ 0.05. P-values obtained from MANOVA (n = 48) for raw or cooked samples. D Interaction of dietary fat source × cooking significant at P ≤ 0.05. P-values obtained from MANOVA for all raw and cooked samples together (n = 96). E Interaction of α-TA supplementation × cooking significant at P ≤ 0.05. P-values obtained from MANOVA for all raw and cooked samples together (n = 96). x–z Means in the same row for a certain factor bearing no common superscripts are statistically different (P ≤ 0.05; P-values obtained from MANOVA, n = 48, for raw or cooked samples). Superscripts obtained by means of the Scheffe´ test (α = 0.05). X–Y Global means for the same response and the same kind of meat (raw or cooked) bearing no common superscripts are statistically different (P ≤ 0.05; P-values obtained from MANOVA n = 144, for raw or cooked samples). Superscripts obtained by means of the Scheffe´ test (α = 0.05) indicate the influence of the storage time on global means. 1 AA = ascorbic acid; COP = cholesterol oxidation products; LHP = lipid hydroperoxide; TA = tocopheryl acetate. Determined COP were: cholestanetriol, cholesterol-5α,6α-epoxide; cholesterol-5β,6β-epoxide, 7β-hydroxycholesterol, 25-hydroxycholesterol, and 7-ketocholesterol. 2 LHP values expressed as mg cumene hydroperoxide/kg of sample, TBA values as milligram of malondialdehyde per kilogram of sample, and α-tocopherol and COP content (mg/kg of sample). *Denotes a statistically significant difference between global means for raw and cooked samples (P ≤ 0.05). P-values obtained from MANOVA for all raw and cooked samples together (n = 96).

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TABLE 2. Least-squares grand means (global means) and least-squares means for responses at different times of storage as influenced by factors1

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EFFECT OF DIET ON CHICKEN MEAT OXIDATION TABLE 3. Fatty acid composition, expressed as compensated area normalization (%), and cholesterol content (mg/100 g of sample) of raw and recently cooked dark meat from chickens fed diets containing different fat sources Raw meat 1

2

BT

SO

OSO

LO

BT

SO

OSO

LO

34.41 47.29 16.09 0.16 0.13 0.15 0.56 0.14 0.04 17.26 0.88 0.03 0.01 0.02 0.08 0.05 1.07 18.34 99.61

22.62 34.96 39.69 0.32 0.23 0.25 0.92 0.27 0.08 41.75 0.63 0.02 TR3 0.01 0.04 0.02 0.72 42.47 98.93

22.31 35.25 38.51 0.26 0.22 0.26 0.89 0.23 0.06 40.43 1.83 0.04 0.02 0.03 0.09 0.04 2.05 42.48 96.09

20.38 33.39 20.73 0.06 0.12 0.13 0.27 0.04 0.01 21.36 23.44 0.24 0.12 0.47 0.47 0.16 24.90 46.26 97.65

34.53 47.68 15.82 0.12 0.13 0.14 0.44 0.12 0.03 16.80 0.89 0.02 0.01 0.02 0.07 0.04 1.05 17.85 ND4

22.97 33.63 40.67 0.33 0.25 0.27 0.87 0.26 0.08 42.74 0.64 0.02 0.02 0.01 0.03 0.02 0.74 43.47 ND

22.43 35.22 38.40 0.29 0.22 0.24 0.77 0.21 0.06 40.19 1.89 0.04 0.02 0.03 0.08 0.04 2.10 42.29 ND

20.30 32.70 20.87 0.05 0.12 0.15 0.26 0.03 0.01 21.50 24.04 0.24 0.13 0.47 0.48 0.17 25.53 47.03 ND

Dietary fat source (BT = beef tallow; SO = sunflower oil; OSO = oxidized sunflower oil; LO = linseed oil). SFA = saturated fatty acids; MUFA = monounsaturated fatty acids; PUFA = polyunsaturated fatty acids. 3 TR = traces. 4 ND = not determined. 1 2

effect by reducing free transition metals such as Fe(III) or Cu(II) to lower valence states [Fe(II) and Cu(I)], at which the catalyst is more active in decomposing LHP to free radicals. In contrast, at high concentrations, AA shows an antioxidant effect because its ability to scavenge oxygen and lipid free radicals predominates (Decker and Xu, 1998; Frankel, 1998). This observation has been made when AA is an endogenous meat component and when it has been added postmortem. In the latter case, up to 200 to 300 mg of AA/kg of meat results in a prooxidant activity, whereas at higher concentrations, AA acts as an antioxidant (Roozen, 1987; Mielche and Bertelsen, 1994; Decker and Xu, 1998; Frankel, 1998). In addition, ascorbate may also release iron from ferritin, membrane lipids, and insoluble protein promoting lipid oxidation (Decker and Welch, 1990; Decker et al., 1993). Furthermore, the observation that AA showed a significant activity only in raw samples could be attributed to the low concentrations of AA in meat as a result of the small quantities of AA usually found in chicken muscle tissues proceeding from self-synthesis (40 to 65 mg/kg, as reviewed by Pardue and Thaxton, 1986) and of the low supplementation applied in this study. Moreover, in our study, broilers were slaughtered after 18 h of feed withdrawal, and plasma AA levels decrease rapidly after the removal of dietary supplementation (Pardue and Thaxton, 1986). Furthermore, this low amount of AA present in raw meat may be easily degraded during cooking, leading to the lack of prooxidant effect observed in cooked samples. The degradation of AA during cooking can be due to the fact that AA is readily oxidized by heat in the presence of metal ions. This process occurs even when only residual oxygen is present in the food package (Greg-

ory, 1996). In addition, in systems with low levels of oxygen, such as vacuum-packaged samples, anaerobic degradation of AA can take place, and trace-metal catalysis of this reaction has been demonstrated (Gregory, 1996).

Interactions Between Dietary Factors In raw samples, interaction between dietary fat source and AA supplementation was significant for COP content (only determination at 7 mo was performed) and for TBA values at any storage time. AA resulted in a prooxidant effect when an unsaturated fat (LO, SO, or OSO), especially LO, was fed (Figure 2). This effect may be caused by the higher PUFA content in meats from these diets (Table 3), which rendered them more labile to prooxidant agents. In contrast, AA tended to prevent oxidation in meat from saturated diets (supplemented with BT). In raw samples, interaction between dietary fat source and α-TA supplementation was significant for all oxidative parameters except for LHP values at 0 and 3.5 mo of storage, although a similar trend was observed. α-TA supplementation canceled the influence of the dietary fat, resulting in no significant differences between samples from animals fed α-TA-supplemented diets from the different fat sources. In contrast, when this supplement was not added, samples from unsaturated diets gave higher oxidation values (Figure 3), which means that basal level of this compound in feed is insufficient to protect enriched-PUFA meats from oxidation. Furthermore, α-tocopherol content in muscle from α-TA-supplemented diets was higher for BT and SO than for LO or OSO groups (only significant in samples stored for 3.5 mo, although a similar trend was observed at the other time

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Total SFA Total MUFA C18:2 n-6 C18:3 n-6 C20:2 n-6 C20:3 n-6 C20:4 n-6 C22:4 n-6 C22:5 n-6 Total n-6 PUFA C18:3 n-3 C18:4 n-3 C20:4 n-3 C20:5 n-3 C22:5 n-3 C22:6 n-3 Total n-3 PUFA Total PUFA Cholesterol

Cooked meat

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GRAU ET AL.

In the absence of α-TA, AA resulted in a prooxidant activity, which was canceled by α-TA supplementation (Figure 5). It is noteworthy that, for both raw and cooked samples, and for all the storage periods and parameters studied, no differences were found between samples from α-TA- and from α-TA-plus-AA-supplemented groups. Accordingly, AA supplementation had no influence on α-tocopherol content of meat (Table 2), which was also observed by Lauridsen et al. (1997b) in breast and leg meat from chickens fed different doses of AA (0, 210, 420 or 840 mg/kg of feed).

Influence of Cooking Cooked samples showed significantly higher TBA and COP values (Table 2). Cooking-related oxidation has been reported in the literature for different cooking methods (Love and Pearson, 1974; Pikul et al., 1984; King et al., 1995; Paniangvait et al., 1995; Kesava Rao et al., 1996; Kowale et al., 1996; Galvin et al., 1997; Maraschiello et al., 1998) and has been attributed to various factors. Between them, protein denaturation, which can lead to the loss of antioxidant enzyme activity (e.g., inactivation of catalase and glutathione peroxidase) or the release of iron from metalloproteins (mainly myoglobin); disruption of cell membranes, which brings PUFA and cholesterol into contact with prooxidants; transformation of myoglobin from an antioxidant to a prooxidant species; and thermal decomposition of hydroperoxides to prooxidant species, such as alkoxyl and hydroxyl radicals (Rhee, 1988; Jadhav et al., 1996; Decker and Xu, 1998; Frankel, 1998). Also the loss of endogenous α-tocopherol content observed in cooked samples compared with the raw ones (Table 2) may be related to the higher oxidation in cooked samples.

Interaction Between Cooking and Dietary Factors

FIGURE 2. TBA values and total COP content of raw dark chicken meat samples stored at −20 C for 7 mo as affected by dietary ascorbic acid (AA) (110 mg/kg) and fat supplementation (6%). BT = beef tallow; COP = cholesterol oxidation products; LO = linseed oil; MDA = malondialdehyde; OSO = oxidized sunflower oil; SO = sunflower oil.

Interaction between cooking and dietary fat source was always significant, except for LHP values at 3.5 mo of storage. After cooking (0 mo of storage), the highest difference in TBA values between cooked and raw samples corresponded to meat from LO diets, and the lowest to that from BT diets (Table 2). This higher susceptibility to cooking related oxidation in chicken leg meat from unsaturated diets has also been observed by other authors (Ruiz et al., 1999) and has been attributed to the higher PUFA content of these samples (Table 3). Rhee et al. (1996) compared the lipid oxidation potential of beef, chicken and pork, and concluded that the amount of PUFA was the main determinant of interspecies differences in lipid oxidation rate in cooked meats. Furthermore, Pikul et al. (1984) stated that the initial concentration of TBA-reactive substances in raw chicken meat is a key factor that determines the final content of those compounds in cooked meat. In addition, cooking had a greater influence on TBA values of samples from OSO than SO diets, which was also reported by Galvin et al. (1997) for breast and leg meat.

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points) (Figure 3), but oxidation of these groups was not different, which indicates that feed supplementation with 225 mg of α-TA/kg was more than enough to protect raw meat with a high PUFA content against oxidation. Cooked samples showed behavior similar to raw samples (Figure 4), although this interaction was not significant for TBA and COP values at 3.5 or 7 mo (Table 2). Despite that meat from LO diets showed the greatest decrease in TBA values due to α-TA supplementation, oxidation values were not as low as those from the other fat sources. In addition, at 0 mo, α-tocopherol in raw samples from LO diets was similar to that of samples from BT and OSO groups. Similarly, Ahn et al. (1995) reported that mixed tocopherols (200 mg/kg of feed) did not reduce TBA values of vacuum-packaged cooked chicken meat from a diet containing full-fat flax seeds to those of samples from a diet containing corn-soybean meal. In contrast, α-TA supplementation reduced LHP values to the same level, regardless of the dietary fat source (Figure 4). Interaction between α-TA and AA was only significant for TBA values from raw samples (at any storage time).

EFFECT OF DIET ON CHICKEN MEAT OXIDATION

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On the other hand, LHP values from samples at 0 mo of storage were significantly lower in cooked than in raw meat. This was evident for all fat sources, although the lower decrease, which was not significant, corresponded to meat samples from LO diets (Table 2). This result could be because, during cooking, destruction of LHP to secondary oxidation products predominates over the formation of new LHP molecules. This unbalance is less marked in samples from unsaturated fat sources, which would be more prone to LHP formation. In contrast, at 3.5 and 7 mo of storage, unsaturated diets resulted in cooked samples with higher LHP values than the raw ones (Table 2), because prooxidant conditions favored by cooking involved greater LHP formation during storage of samples with a higher unsaturated fatty acid profile. In addition, it must be remembered that the FOX method used to measure LHP values is, to a certain extent, an induced method (Grau et al., 2000c). In this case, FOX reaction was incubated for 4 h and, during this time, lipids from the sample undergo some oxidation that may be enhanced by the prooxidants released during cooking. While AA did not affect sample oxidation during cooking, α-TA supplementation reduced it (Table 2). For all oxidative parameters (TBA, LHP, and COP), oxidation induced by cooking was significantly lower in α-TA-supplemented groups (Table 2). Oxidative stability toward cooking, given by α-TA, has been also described in terms of TBA values by other authors (King et al., 1995; Galvin et al., 1997). In addition, at 0 mo of storage, meat samples from diets without α-TA supplementation gave lower LHP values after cooking (Table 2), which could be attrib-

uted to the above-mentioned decomposition of LHP to secondary oxidation products during the cooking procedure (Frankel, 1998). In contrast, in samples from supplemented diets, LHP values did not change significantly after cooking, because initial LHP values were much lower and, consequently, thermal decomposition of LHP was much less important.

Influence of the Storage Time and Its Interaction with Other Factors Oxidation of samples was influenced by storage. However, the behavior of LHP and TBA values from raw or cooked samples was different (Figure 6). In raw samples, LHP values significantly decreased during the first 3.5 mo of storage. Besides, TBA values tended to increase during the whole period, although nonsignificantly. Such an increase in TBA values during frozen or chilled storage has also been reported for raw samples packaged in air (Pikul et al., 1984, 1989; Rhee et al., 1996). Differences in the magnitude of this increase [from 4.9 times after 6 mo in the study of Pikul et al. (1989) to 1.2 after 7 mo in the present study] could be attributed to the protective effect of vacuum-packaging (assessed in chicken leg meat by Ang and Huang, 1993). In contrast, in cooked samples, LHP significantly increased after the first 3.5 mo, and TBA values decreased (Figure 6). For both parameters, changes during the second period (3.5 to 7 mo) were not significant. This decrease in TBA values was also observed by other authors (King et al., 1995; Galvin et al., 1997) in non-vacuum-

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FIGURE 3. Lipid hydroperoxide (LHP) and TBA values and total cholesterol oxidation products (COP) and α-tocopherol content of raw dark chicken meat samples stored at −20 C for 7 mo as affected by dietary α-tocopherol acetate (α-TA) (225 mg/kg) and fat supplementation (6%). BT = beef tallow; CHP = cumene hydroperoxide; LO = linseed oil; MDA = malondialdehyde; OSO = oxidized sunflower oil; SO = sunflower oil.

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GRAU ET AL.

packaged raw and cooked chicken meat samples and it may be due to the reaction of MDA with proteins or to MDA polymerization reactions (Buttkus, 1967; Whang et al., 1986; Esterbauer et al., 1991; Aubourg, 1993; Wen et al., 1996). The different behavior of LHP values of raw and cooked samples during storage could be explained by the

FIGURE 5. TBA values of raw dark chicken meat samples stored at −20 C for 0, 3.5, or 7 mo as affected by dietary ascorbic acid (AA) and α-tocopheryl acetate (α-TA) supplementation (110 and 225 mg/kg of feed, respectively).

FIGURE 4. Lipid hydroperoxide (LHP) and TBA values, and αtocopherol content of cooked dark chicken meat samples at 0 mo of storage at −20 C as affected by dietary α-tocopherol acetate (α-TA) (225 mg/kg) and fat supplementation (6%). BT = beef tallow; CHP = cumene hydroperoxide; LO = linseed oil; MDA = malondialdehyde; OSO = oxidized sunflower oil; SO = sunflower oil.

FIGURE 6. Evolution of lipid hydroperoxide (LHP) and TBA values of raw or cooked dark chicken meat as influenced by storage period at −20 C. CHP = cumene hydroperoxide; MDA = malondialdehyde.

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prooxidant conditions induced by cooking, as previously explained (such as liberation of iron and disruption of cellular membranes), which led to a higher LHP production through the storage and during the incubation of the FOX reaction (Grau et al., 2000c). According to this, Rhee et al. (1996) found a higher content of nonheme iron in cooked chicken leg meat compared with raw. Furthermore, this nonheme iron increased during storage of the meat at −20 C from 0 to 2.5 mo, but it remained steady from 2.5 to 5 mo. This agrees with the fact that LHP values in cooked samples increased significantly only during the first period of storage (Table 2). In addition, changes in

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EFFECT OF DIET ON CHICKEN MEAT OXIDATION

Correlations Between Results from the Different Methods Correlations between results are stated in Tables 4 and 5. Only TBA and COP values for cooked samples failed to show a significant correlation. Positive correlation between COP content and TBA values has been reported in cooked samples from chicken and turkey (Park and Addis, 1987; Galvin et al., 1998), beef (Park and Addis, 1987; de Vore, 1988), and pork (Monahan et al., 1992). However, in those works, samples had been trimmed of extramuscular fat, cooked after grinding, non-vacuumpackaged, and stored at 4 C (0 to 12 d). In contrast, our samples containing meat plus skin were ground after cooking, vacuum-packaged, and stored at −20 C for 7 mo. These differences may account for the disagreement in the results. Moreover, for both raw and cooked samples, there was always a highly significant negative correlation between oxidative parameters and α-tocopherol content. Negative correlation between TBA values and plasma or muscular α-tocopherol has also been reported for chickens fed diets containing fresh or heated SO with no α-TA supplementation (Sheehy et al., 1994), and SO or lard supplemented with 200 mg/kg of α-TA (Marashiello et al., 1999). In addition, several studies showed that high levels of tissue or plasma TBA or COP values always correspond to low levels of endogenous α-tocopherol (Lin et al., 1989a; Sheehy et al., 1993; Galvin et al., 1997; Ruiz et al., 1999). To sum up, despite that TBA and COP values are not correlated in cooked samples, all oxidative parameters are inversely correlated with α-tocopherol content, which allows the conclusion that α-tocopherol is a key factor in avoiding the formation of fatty acid and cholesterol oxidation products. Furthermore, the negative correlation between TBA values and α-tocopherol content was more pronounced

TABLE 4. Correlations between oxidative parameters and α-tocopherol content in raw dark chicken meat samples Storage time 0 mo (n = 48)

3.5 mo (n = 48)

7 mo (n = 48)

Whole period (n = 144)

TBA-COP

0.42042 (0.0029) —3

0.5149 (0.0002) —

0.4931 (<0.00005) —

LHP-COP

—

—

−0.4863 (0.0005) −0.9477 (<0.00005) —

−0.5331 (0.0001) −0.9306 (<0.00005) —

0.5928 (<0.00005) 0.6466 (0.0001) 0.8320 (<0.00005) −0.5842 (<0.00005) −0.9329 (<0.00005) −0.7994 (<0.00005)

Oxidation values1 TBA-LHP

TBA-α-tocopherol LHP-α-tocopherol COP-α-tocopherol

— −0.5304 (<0.00005) −0.9287 (< 0.00005) —

COP = cholesterol oxidation products; LHP = lipid hydroperoxide values; TBA = 2-thiobarbituric acid values. Pearson’s correlation coefficient. P-values are stated in parentheses. 3 COP values were only determined in samples stored for 7 mo. 1 2

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nonheme iron of raw leg meat during the 5 mo of frozen storage were not significant (Rhee et al., 1996). In contrast, Kanner et al. (1988) described an increase in free iron in raw turkey and chicken meat (dark and white muscles) during storage at 4 C for 3 or 7 d, which was claimed to be important in lipid oxidation in chilled stored meat. Endogenous α-tocopherol of raw or cooked samples did not change throughout the 7 mo of frozen storage, which justifies the finding that supplemented samples were highly protected from oxidation during the whole study (Table 2). Stability of α-tocopherol during frozen storage has been previously described by King et al. (1995). Several studies also reported beneficial effects of dietary tocopherols on chilled or frozen storage stability of chicken, turkey, and pork raw or cooked meat (reviewed by Jensen et al., 1998). In addition, the protective role of endogenous tocopherols throughout storage seems to be additive to other preservation methods such as vacuum-packaging (Jensen et al., 1998). On the other hand, dietary fat source or AA supplementation did not influence meat stability during storage. Other authors reported that meat samples from chickens fed diets supplemented with unsaturated fatty acids were more susceptible toward oxidation during chilled (Lin et al., 1989a; Ruiz et al., 1999) or frozen storage (Lin et al., 1989a). However, those studies were carried out in nonvacuum-packaged samples, which means an increased amount of oxygen, thus favoring oxidation (Ang and Huang, 1993). In addition, Ahn et al. (1993) reported that total lipid and fatty acid composition of turkey patties affected lipid oxidation only if oxygen was freely accessible to the patties during storage. The influence of AA during storage has been poorly studied. Lauridsen et al. (1997b) also reported a lack of effect of different doses of AA (210 to 840 mg/kg feed) on the oxidative stability of breast or thigh raw chicken meat under chill (4 C, 10 d) or freezer storage (−12 C, 9 mo).

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GRAU ET AL. TABLE 5. Correlations between oxidative parameters and α-tocopherol content in cooked dark chicken meat samples Storage time Oxidation values1 TBA-LHP TBA-COP LHP-COP TBA-α-tocopherol LHP-α-tocopherol COP-α-tocopherol

0 mo (n = 48)

3.5 mo (n = 48)

7 mo (n = 48)

Whole period (n = 144)

0.62122 (<0.00005) —3 —

0.6204 (<0.00005) — —

0.5953 (<0.00005) — —

−0.5236 (0.0001) −0.9056 (<0.00005) —

−0.5845 (<0.00005) −0.9368 (<0.00005) —

0.6250 (<0.00005) NS 0.7048 (<0.00005) −0.5812 (<0.00005) −0.9191 (<0.00005) −0.7260 (<0.00005)

−0.5610 (<0.00005) −0.9094 (<0.00005) —

COP = cholesterol oxidation products; LHP = lipid hydroperoxide values; TBA = 2-thiobarbituric acid values. Pearson’s correlation coefficient. P-values are stated in parentheses. 3 COP values were only determined in samples stored for 7 mo. 1

after 3.5 or 7 mo of storage than at 0 mo, and in cooked than in raw samples (Tables 4 and 5), which indicates that the protective effect of the antioxidant is more relevant when these processing operations are involved.

Conclusions Supplementation of broilers diets with α-TA (225 mg/ kg of feed) resulted in effective protection of meat from fatty acid and cholesterol oxidation, regardless of the dietary fat source (BT, SO, OSO, or LO). On the contrary, AA supplementation (110 mg/kg) was clearly useless and showed no synergism with α-TA. Combining vacuumpackaging and dietary α-TA supplementation seems a feasible approach to greatly reduce fatty acid and cholesterol oxidation of raw or cooked chicken meat during frozen storage (7 mo at −20 C). In addition, the results demonstrate that, in meats, the oxidation values obtained by means of different analytical methods greatly depend on several factors, such as processing and storage conditions, unsaturation degree of the sample, and other intrinsic features (i.e., endogenous natural antioxidants or free iron content). Consequently, it is very difficult to compare oxidation values from different studies.

ACKNOWLEDGMENTS A. Jorda´n, C. Ferrer, D. Alonso, and M. Erra (all from University of Barcelona) helped in laboratory work, and S. Lo´pez-Ferrer (UAB) in breeding animals. HofffmanLa Roche Ltd. provided α-TA and AA. Cuit’s provided slaughter and processing facilities. This work was supported in part by research grants from the Comissio´ Interdepartamental de Recerca i Innovacio´ Tecnolo`gica (CIRIT), the Comisio´n Interministerial de Ciencia y Tecnologı´a (CICYT), and the Instituto Danone.

REFERENCES Addis, P. B., P. W. Park, F. Guardiola, and R. Codony, 1996. Analysis and health effects of cholesterol oxides. Pages 199– 240 in: Food Lipids and Health. R. E. McDonald and D. B. Min, ed. Marcel Dekker, New York, NY. Ahn, D. U., A. Ajuyah, F. H. Wolfe, and J. S. Sim, 1993. Oxygen availability affects in prooxidant catalyzed lipid oxidation of cooked turkey patties. J. Food Sci. 58:278–282. Ahn, D. U., F. H. Wolfe, and J. S. Sim, 1995. Dietary α-linolenic acid and mixed tocopherols, and packaging influences on lipid stability in broiler chicken breast and leg muscle. J. Food Sci. 60:1013–1018. Ajuyah, A. O., D. U. Ahn, R. T. Hardin, and J. S. Sim, 1993. Dietary antioxidants and storage affect chemical characteristics of ω-3 fatty acid enriched broiler chicken meats. J. Food Sci. 58:43–46, 61. Andrews, J. S., W. H. Griffith, J. F. Mead, and R. A. Stein, 1960. Toxicity of air-induced soybean oil. J. Nutr. 70:199–210. Ang, C. Y. W., and Y. W. Huang, 1993. Internal temperature and packaging system affect stability of cooked chicken leg patties during refrigerated storage. J. Food Sci. 58:265–269, 277. Aubourg, S. P., 1993. Review: Interaction of malondialdehyde with biological molecules—New trends about reactivity and significance. Int. J. Food Sci. Technol. 28:323–335. Bartov, I., 1977. Lack of effect of dietary ascorbic acid on stability of carcass fat and meat of broilers. Br. Poult. Sci. 18:553–555. Benedict, R. C., F. D. Strange, and C. E. Swift, 1975. Effect of lipid antioxidants on the stability of meat during storage. J. Agric. Food Chem. 23:167–173. Botsoglou, N. A., D. J. Fletouris, G. E. Papageorgiou, V. N. Vassilopoulos, A. J Mantis, and A. G. Trakatellis, 1994. Rapid, sensitive, and specific thiobarbituric acid method for measuring lipid peroxidation in animal tissue, food, and feedstuff samples. J. Agric. Food Sci. 42:1931–1937. Bou, R., F. Guardiola, A. Grau, S. Grimpa, A. Manich, A. Barroeta, and R. Codony, 2001. Influence of dietary fat source, α-tocopherol, and ascorbic acid supplementation on sensory quality of dark chicken meat. Poultry Sci. 80:800–807. Brown, A. J., and W. Jessup, 1999. Oxysterols and atherosclerosis. Atherosclerosis 142:1–28. Bunyan, J., J. Green, E. A. Murrell, A. T. Dipolck, and M. A. Cawhorne, 1968. On the postulated peroxidation of unsaturated lipids in the tissues of vitamin E-deficient rats. Br. J. Nutr. 22:97–110.

Downloaded from http://ps.oxfordjournals.org/ at University of Southern Queensland on October 18, 2014

2

EFFECT OF DIET ON CHICKEN MEAT OXIDATION

Su importancia en la rancidez oxidativa y en el perfil del flavor de los alimentos. Grasas Aceites 39:185–189. Jadhav, S. J., S. S. Nimbalkar, A. D. Kulkarni, and D. L. Madhavi, 1996. Lipid oxidation in biological and food systems. Pages 5–63 in: Food Antioxidants. D. L. Madhavi, S. S. Deshpande, and D. K. Salunkhe, ed. Marcel Dekker, New York, NY. Jensen, C., C. Lauridsen, and G. Bertelsen, 1998. Dietary vitamin E: Quality and storage stability of pork and poultry. Trends Food Sci. Technol. 9:62–72. Jensen, C., L. H. Skibsted, K. Jakobsen, and G. Bertelsen, 1995. Supplementation of broiler diets with all-rac-α- or a mixture of natural source RRR-α-, γ-, δ-tocopheryl acetate. 2. Effect on the oxidative stability of raw and precooked broiler meat products. Poultry Sci. 74:2048–2056. Jiang, Z. Y., J. V. Hunt, and S. P. Wolff, 1992. Ferrous ion oxidation in the presence of xylenol orange for detection of lipid hydroperoxide in low density lipoprotein. Anal. Biochem. 202:384–389. Kanner, J., B. Hazan, and L. Doll, 1988. Catalytic “free” iron ions in muscle foods. J. Agric. Food Chem. 36:412–415. Kesava Rao, V., B. N. Kowale, N. P. Babu, and G. S. Bisht, 1996. Effect of cooking and storage on lipid oxidation and development of cholesterol oxidation products in water buffalo meat. Meat Sci. 43:179–185. King, A. J., T. G. Uijttenboogaart, and A. W. Vries, 1995. αTocopherol, β-carotene and ascorbic acid as antioxidants in stored poultry muscle. J. Food Sci. 60:1009–1012. Kosugi, H., T. Kato, and K. Kikugawa, 1987. Formation of yellow, orange, and red pigments in the reaction of alk-2-enals with 2-thiobarbituric acid. Anal. Biochem. 165:456–464. Kowale, B. N., V. Kesava Rao, N. P. Babu, N. Sharma, and G. S. Bisht, 1996. Lipid oxidation and cholesterol oxidation in mutton during cooking and storage. Meat Sci. 43:195–202. Lauridsen, C., D. J. Buckley, and P. A. Morrissey, 1997a. Influence of dietary fat and vitamin E supplementation on αtocopherol levels and fatty acid profiles in chicken muscle membranal fractions and on susceptibility to lipid peroxidation. Meat Sci. 46:9–22. Lauridsen, C., C. Jensen, K. Jakobsen, R. M. Enberg, J. O. Andersen, S. K. Jensen, P. Sorensen, P. Henckel, L. H. Skibsted, and G. Bertelsen, 1997b. The influence of vitamin C on the antioxidative status of chickens in vivo, at slaughter and on the oxidative stability of broiler meat products. Acta Agric. Scand. Sect. A Anim. Sci. 47:187–196. Li, S. X., D. U. Ahn, G. Cherian, T. Y. Chung, and J. S. Sim, 1996. Dietary oils and tocopherol supplementation on cholesterol oxide formation in freeze-dried chicken meat during storage. J. Food Lipids 3:27–42. Lin, C. F., J. I. Gray, A. Asghar, D. J. Buckley, A. M. Booren, and C. J. Flegal, 1989a. Effects of dietary oils and α-tocopherol supplementation on lipid composition and stability of broiler meat. J. Food Sci. 54:1457–1460, 1484. Lin, C. F., J. I. Gray, A. Ashgar, D. J. Buckely, A. M. Booren, R. L. Crakel, and C. J. Flegal, 1989b. Effects of oxidized dietary oil and antioxidant supplementation on broiler growth and meat stability. Br. Poult. Sci. 30:855–864. Lo´pez-Ferrer, S., M. D. Baucells, A. C. Barroeta, and M. A. Grashorn, 1999. Influence of vegetable oil sources on quality parameters of broiler meat. Arch. Geflu¨gelk. 63:29–35. Love, J. A. D., and A. M. Pearson, 1974. Metmyoglobin and nonheme iron as prooxidants in cooked meat. J. Agric. Food Chem. 22:1032–1034. Maraschiello, C., E. Esteve, and J. A. Garcı´a-Regueiro, 1998. Cholesterol oxidation in meat from chickens fed α-tocopherol- and β-carotene-supplemented diets with different unsaturation grades. Lipids 33:705–713. Maraschiello, C., C. Sa´rraga, and J. A. Garcı´a Regueiro, 1999. Glutathione peroxidase activity, TBARS, and α-tocopherol in meat from chickens fed different diets. J. Agric. Food Chem. 47:867–872.

Downloaded from http://ps.oxfordjournals.org/ at University of Southern Queensland on October 18, 2014

Burat, K. M., and O. Bozkurt, 1996. Improvement of calibration curve for determining peroxide values of food lipids by the modified ferrous oxidation-xylenol orange method. J. AOAC Int. 79:995–997. Buttkus, H., 1967. The reaction of myosine with malonaldehyde. J. Food Sci. 32:432–434. De Vore, V. R., 1988. TBA values and 7-ketocholesterol in refrigerated raw and cooked ground beef. J. Food Sci. 53:1058–1061. De Winne, A., and P. Dirinck, 1996. Studies on vitamin E and meat quality. 2. Effect of feeding high vitamin E levels on chicken meat quality. J. Agric. Food Chem. 44:1691–1696. Decker, E. A., A. D. Crum, N. C. Shantha, and P. A. Morrissey, 1993. Catalysis of lipid oxidation by iron from an insoluble fraction of beef diaphragm muscle. J. Food Sci. 58:233–236, 258. Decker, E. A., and B. Welch, 1990. Role of ferritin as a lipid oxidation catalyst in muscle food. J. Agric. Food Chem. 28:674–677. Decker, E. A., and Z. Xu, 1998. Minimizing rancidity in muscle foods. Food Technol. 52:54–59. Erickson, M. C., 1998. Lipid oxidation of muscle foods. Pages 297–332 in: Food Lipids. Chemistry, Nutrition and Biotechnology. C. C. Akoh and D. B. Min, ed. Marcel Dekker, New York, NY. Esterbauer, H., R. J. Schaur, and H. Zollner, 1991. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic. Biol. Med. 11:81–128. Frankel, E. N., 1998. Foods. Pages 187–225 in: Lipid Oxidation. The Oily Press Ltd., Dundee, Scotland. Galvin, K., P. A. Morrissey, and D. J. Buckley, 1997. Influence of dietary vitamin E and oxidized sunflower oil on the storage stability of cooked chicken muscle. Br. Poult. Sci. 38:499–504. Galvin, K., P. A. Morrissey, and D. J. Buckley, 1998. Cholesterol oxides in processed chicken muscle as influenced by dietary alpha-tocopherol supplementation. Meat Sci. 48:1–9. Galvin, K., P. A. Morrissey, D. J. Buckley, and M. Frigg, 1993. Influence of oil quality and α-tocopheryl acetate supplementation on α-tocopherol and lipid oxidation on chicken tissues. Pages 423–429 in: Proceedings of the 11th European Symposium on the Quality of Poultry Meat. World’s Poultry Science Association, Tours, France. Grau, A., R. Codony, S. Grimpa, M. Baucells, and F. Guardiola, 2000a. Cholesterol oxidation in frozen dark chicken meat: Influence of dietary fat source, and α-tocopherol and ascorbic acid supplementation. Meat Sci. 57:197–208. Grau, A., R. Codony, M. Rafecas, A. Barroeta, and F. Guardiola, 2000b. Lipid hydroperoxide determination in dark chicken meat through a ferrous oxidation-xylenol orange method. J. Agric. Food Chem. 48:4136–4143. Grau, A., F. Guardiola, J. Boatella, A. Barroeta, and R. Codony, 2000c. Measurement of 2-thiobarbituric acid values in dark chicken meat through derivative spectrophotometry: Influence of various parameters. J. Agric. Food Chem. 48:1155– 1159. Gregory, J. F., III, 1996. Vitamins. Pages 531–616 in: Food Chemistry. O. R. Fennema, ed. Marcel Dekker, New York, NY. Guardiola, F., R. Codony, P. B. Addis, M. Rafecas, and J. Boatella, 1996. Biological effects of oxysterols: Current status. Food Chem. Toxicol. 34:193–211. Guardiola, F., R. Codony, D. Miskin, M. Rafecas, and J. Boatella, 1995. Oxysterol formation in egg powder and relationship with other quality parameters. J. Agric. Food Chem. 43:1903–1907. Guardiola, F., A. Jordan, A. Grau, S. Garcia, J. Boatella, M. Rafecas, and R. Codony, 1998. Recent methodological advances in oxysterol determination. Pages 77–88 in: Recent Research Developments in Oil Chemistry. S. G. Pandalai, ed. Transworld Research Network, Trivandrum, India. Guille´n Sans, R., and M. Guzma´n Chozas, 1988. Reactividad del a´cido 2-tiobarbitu´rico (ATB) con compuestos carbonı´licos.

1641

1642

GRAU ET AL. Raharjo, S., and J. N. Sofos, 1993. Methodology for measuring malonaldehyde as a product of lipid peroxidation in muscle tissues: A review. Meat Sci. 35:145–169. Rhee, K. S., 1988. Enzymic and nonenzymic catalysis of lipid oxidation in muscle foods. Food Technol. 42:127–132. Rhee, K. S., L. M. Anderson, and A. R. Sams, 1996. Lipid oxidation potential of beef, chicken, and pork. J. Food Sci. 61:8–12. Roozen, J. P., 1987. Effects of types I, II and III antioxidants on phospholipid oxidation in a meat model for warmed over flavor. Food Chem. 24:167–185. Ruiz, J. A., A. M. Pe´rez-Vendrell, and E. Esteve-Garcı´a, 1999. Effect of β-carotene and vitamin E on oxidative stability in leg meat of broilers fed different supplemental fats. J. Agric. Food Chem. 47:448–454. Shantha, N. C., and E. A. Decker, 1994. Rapid, sensitive, ironbased spectrophotometric methods for determination of peroxide values of food lipids. J. AOAC Int. 77:421–424. Sheehy, P. J. A., P. A. Morrissey, and A. Flynn, 1993. Influence of heated vegetable oils and α-tocopheryl acetate supplementation on α-tocopherol, fatty acids and lipid peroxidation in chicken muscle. Br. Poult. Sci. 34:367–381. Sheehy, P. J. A., P. A. Morrissey, and A. Flynn, 1994. Consumption of thermally-oxidized sunflower oil by chicks reduces α-tocopherol status and increases susceptibility of tissues to lipid oxidation. Br. J. Nutr. 71:53–65. Stapra˜ns, I., J. H. Rapp, X. Pan, and K. R. Feingold, 1993. The effect of oxidized lipids in the diet on serum lipoprotein peroxides in control and diabetic rats. J. Clin. Invest. 92:638–643. Stapra˜ns, I., J. H. Rapp, X. Pan, K. Y. Kim, and K. R. Feingold, 1994. Oxidized lipids in the diet are a source of oxidized lipid in chylomicrons of human serum. Arterioscler. Thromb. 14:1900–1905. Wen, J., P. A. Morriseey, D. J. Buckley, and P. J. A. Sheehy, 1996. Oxidative stability and α-tocopherol retention in turkey burgers during refrigerated and frozen storage as influenced by dietary α-tocopheryl acetate. Br. Poult. Sci. 37:787–795. Whang, K., E. D. Aberle, M. D. Judge, and I. C. Peng, 1986. Antioxidant activity of α-tocopherol in cooked and uncooked ground pork. Meat Sci. 17:235–249. Witte, V. C., G. F. Krause, and M. E. Bailey, 1970. A new extraction method for determining 2-thiobarbituric acid values of pork and beef during storage. J. Food Sci. 35:582–585.

Downloaded from http://ps.oxfordjournals.org/ at University of Southern Queensland on October 18, 2014

Mielche, M. M., and G. Bertelsen, 1994. Approaches to the prevention of warmed-over flavor. Trends Food Sci. Technol. 5:322–327. Monahan, F. J., J. I. Gray, A. M. Booren, E. R. Miller, D. J. Buckley, P. A. Morrissey, and E. A. Gomaa, 1992. Influence of dietary treatment on lipid and cholesterol oxidation in pork. J. Agric. Food Chem. 40:1310–1315. Mooney, J. W., E. M. Hirschler, A. K. Kennedy, A. R. Sams, and M. E. Van Elswyk, 1998. Lipid and flavor quality of stored breast meat from broilers fed marine algae. J. Food Sci. Agric. 78:134–140. Naruszewicz, M., E. Wo´zny, E. Mirkiewicz, G. Nowicka, and W. B. Szostak, 1987. The effect of thermally oxidized soya bean oil on metabolism of chylomicrons. Increased uptake and degradation of oxidized chylomicrons in cultured mouse macrophages. Atherosclerosis 66:45–53. Nourooz-Zadeh, J., 1998. Measurement of hydroperoxides in edible oils and fats using the ferrous-oxidation in xylenol orange (FOX) assay and application of the method to estimation of dietary hydroperoxide intakes in the United Kingdom. Pages 53–61 in: Recent Research Developments in Oil Chemistry. S. G. Pandalai, ed. Transworld Research Network, Trivandrum, India. O’Neill, L. M., K. Galvin, P. A. Morrissey, and D. J. Buckley, 1998. Comparison of effects of dietary oil, tallow and vitamin E on the quality of broiler meat and meat products. Br. Poult. Sci. 39:365–371. Paniangvait, P., A. J. King, A. D. Jones, and B. G. German, 1995. Cholesterol oxides in foods of animal origin. J. Food Sci. 60:1159–1174. Pardue, S. L., and J. P. Thaxton, 1986. Ascorbic acid in poultry: A review. World’s Poult. Sci. J. 42:107–123. Park, S. W., and P. B. Addis, 1987. Cholesterol oxidation products in some muscle foods. J. Food Sci. 52:1500–1503. Pikul, J., D. E. Leszczynski, P. J. Bechtel, and F. A. Kummerow, 1984. Effects of frozen storage and cooking on lipid oxidation in chicken meat. J. Food Sci. 49:838–843. Pikul, J., D. E. Leszczynski, and F. A. Kummerow, 1989. Evaluation of three modified TBA methods for measuring lipid oxidation in chicken meat. J. Agric. Food Chem. 37:1309– 1313.