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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 Veterinaria, UAB, E-08193 Bellaterra, Spain 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, 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
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; Lopez-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.
. 2000c).4 1. and AA (0 and 110 mg/kg of feed).0 0.5 × 16-cm polyamide/ polyethylene bags. and stored at −20 C for 0. Switzerland.. The ﬁrst choice method for this analysis consists of lipid extraction. Ingredients and composition of the basal diet Ingredients and composition Corn Corn germ meal Soybean meal. 1987. and gas chromatography (Addis et al. Dietary treatments were randomly distributed.4 10. The goal of this paper was to study the inﬂuence of the dietary fat source. which removes the main sources of interference. Carcasses were ` transported to the Cuit’s processing plant (Cassa de la Selva. 1999)..1 7. Spain). randomly placed in 48 pens (ﬁve birds per pen). Botsoglou et al. and COP content) in raw and cooked dark chicken meat.25.3 Sunﬂower oil [unreﬁned. To overcome these drawbacks. 3. 1988.40.. 1995. Two hundred forty female broiler chicks (Ross. 1 d old) were fed a control diet for 6 d. ` ´ Dietary fats supplied by Caila i Pares S.0 4. 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 1 2 Percentage 30. speciﬁc absorbances at 232 (K232) and 270 nm (K270) were 2.1 5. 1996). 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. 1994). Another interest of this determination relies on the potentially harmful effects of these compounds (Guardiola et al. cooked at 80 C for 35 min in a pressure cooker. 3 2 . Ltd..83).5.... 2000a).5 88.0 5. Finally.0 8. vacuum-packaged in 13. and linseed oil (LO).750 Kcal/kg. CH-4070 Basel. and cooking on the oxidative stability of dark chicken meat samples vacuum-packaged and stored at −20 C for 0.0 0. E-08040 Barcelona. 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.5 × 16-cm polyamide/polyethylene bags and stored for 0. (1995).2 16. Reaction mixtures containing 75 µL of sample extract were incubated for 4 h.. the determination of COP content in foods of animal origin has also been used as a parameter to measure lipid oxidation (Paniangvait et al. Raharjo and Sofos. 3. sunﬂower oil (SO). (2000b). Brown and Jessup. ground. Legs with skin from each pen were divided into two groups.1 1.380. 53. three pens were assigned to each treatment.5. α-TA and AA supplementations. Guillen and Guzman. (1994) proposed an acid aqueous extraction method using third-derivative spectrophotometry. Guardiola et al. 6% fat supplementation in all cases]. A method following these steps has been adapted to dark chicken meat samples (Grau et al.9 1. Permeability to oxygen of all bags used was 50 cm3 bar 24 h (Deutsches Institut fur Normung. The remaining three legs were vacuum-packaged in 20 × 40-cm polyamide/polyethylene bags.3 0. α-TA (0 and 225 mg/kg of feed). and 7 mo) at −20 C on several parameters (α-tocopherol content. The other group of ﬁve legs was hand deboned. 1993. 2. K270 = 0. TABLE 1. Sample Preparation Broiler chickens (57 d old) were leg-ringed and slaughtered according to commercial procedures at the Avicola Maria slaughterhouse (Begur. α-TA (Rovimix E-50 Adsorbate) and AA (Rovimix C) were from Hoffmann-La Roche. vacuum-packaged in 13. Botsoglou et al. Their method was further studied in order to be applied to chicken meat samples (Grau et al. and stored for 13 mo at −20 C until sensory analysis and TBA value determination (Figure 1). and 7 mo. Results from sensory analysis have been discussed in a previous work (Bou et al. 1996.0 18. Our discussion is based on the results of several oxidative parameters (LHP and TBA values and COP content). and broiler chickens were fed ad libitum for 50 d.4 Did not include vitamin E. Spain. LHP and TBA values. 2001).EFFECT OF DIET ON CHICKEN MEAT OXIDATION 1631 ´ sugi et al. Spain) and stored for 3 d at 4 C in a walk-in cooler. 1996.5. Metabolizable energy.. or 7 mo at 20 C. or 7 mo. these two cooked legs were ground.. 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. One-week-old birds were Analysis of Samples Lipid hydroperoxide values were assessed according to the FOX method described by Grau et al.8 5.. Speciﬁc absorbances were measured as described by Guardiola et al. 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). 3. ¨ 23 C).5. COP enrichment. 1998). fatty acid composition. One group of legs was hand deboned.1 0. Addis et al.87 and 0.4 17.A. 3. oxidized sunﬂower oil (OSO).
LHP = lipid hydroperoxide. COP = cholesterol oxidation product. FIGURE 1. .1632 GRAU ET AL. BT = beef tallow. LO = linseed oil. OSO = oxidized sunﬂower oil. SO = sunﬂower oil. One leg of each bird in each group of legs. This experimental design was conducted in triplicate (80 × 3 female broiler chicks were randomly assigned to 16 × 3 treatments). α-TA = α-tocopheryl acetate supplementation in mg/kg of feed. Experimental design. AA = ascorbic acid supplementation in mg/kg of feed.
respectively.05) was applied to determine statistical differences between least-squares means. or sunﬂower oils. 1989b. (1993. respectively (n = 48). (1992). 3. 2. as described by Grau et al. as there were no signiﬁcant differences between the cholesterol content of meat from different fat sources (Table 3).5-fold greater than in SO.5.83 for the OSO. Ahn et al. although the α-tocopherol content of meat samples from OSO diets was slightly lower than that from SO. raw and cooked samples from chickens fed BT or LO diets gave the lowest and the highest TBA values. ﬂax. For all analytical methods. In all cases. (1989b).. 1997. and (12) all samples (raw + cooked at 0 + 3. 1999. lack of a clear prooxidant effect of dietary OSO could be attributed to an insufﬁcient degree of oxidation of the heated SO. COP content.. Li et al. (9) raw + cooked samples at 0 mo (n = 96). 1997). Statistics. this difference was not signiﬁcant (Table 2). PUFA peroxide content in our OSO is much lower than in OSO used by other authors (Lin et al. (2000b).and BT-fed groups. palm. although it was not signiﬁcant (Table 2). cooking. as argued by Monahan et al. Sheehy et al. This ﬁnding is consistent with the ﬁnding that in cooked samples TBA values tended to be higher for OSO groups. In addition. samples from OSO diets always resulted in higher TBA values than those from SO. in the present study. (1993. 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 (Staprans et al.. which was reﬂected by all the oxidation .. Other authors also reported higher TBA values for chicken leg meat from unsaturated fat sources (Lin et al. 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. Galvin et al. Analyses for COP and cholesterol content were performed as described by Grau et al. n = 144). or 7 mo at −20 C.5 + 7 mo.c). and. 1968). This result was attributed to the destruction of the endogenous α-tocopherol of SO during heating. Sheehy et al. At any storage time.. 1989a. the destruction of α-tocopherol in the gastrointestinal tract by free radicals from the oxidized oil. In contrast. and 7 mo. samples from diets containing unsaturated fat sources also gave the highest values. the Scheffe test for a posteriori contrasts (α = 0. When the fat source signiﬁcantly inﬂuenced LHP values.40 and 0.5. (2000c). Ruiz et al.b. respectively.. respectively. except for LHP values in raw samples stored for 0 or 3. α-TA and AA supplementations. Thus. In addition. (4) all raw samples (0 + 3. in cooked ground breast or leg chicken meat stored for different periods at 4 or −20 C. reagents and standards used were previously detailed by Grau et al. where they could be secreted in very-low-density lipoprotein and therefore to reach peripheral tissues. 1993. and storage time) had any signiﬁcant effect on the responses. 1993.. ˜ chylomicrons could deliver LHP to the liver. 1995. and the absorption of LHP. and α-tocopherol content). (2000a). 1994). it has been recently shown that. 1997) ranged from 40 to 80 g/kg of feed and that used in our study was 60 g/kg. (10 and 11) the same at 3. 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. resulting in a higher rate of oxidation and higher consumption of α-tocopherol in vivo. 1993). Speciﬁc absorbances at 232 and 270 nm were. (1993. 1987. (1996) also failed to ﬁnd any differences in cholesterol content in freeze-dried chicken breast meat samples from animals fed diets supplemented with ﬁsh. Pearson correlation coefﬁcients were used to examine possible linear correlations between responses (LHP values. When dietary fat source or storage time ´ showed a signiﬁcant effect. Feeding OSO did not signiﬁcantly increase the oxidation of dark chicken meat (Table 2). Galvin et al. Staprans et al. which indicates that conjugated dienes in OSO were only approximately 1. (2000a. The cholesterol content of samples cannot account for this effect of dietary fat on COP content. Maraschiello et al. 1994). it is a consequence of the higher PUFA content in meats from unsaturated diets (Table 3). Bunyan et al. (5 to 8) the same for cooked samples. However. 1989b. 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. LHP are absorbed and incorporated into chylomicrons to some extent (Naruszewicz et al.. 1999)..87 and 0. in humans. in our study.5 mo (Table 2). However.05 were considered to be signiﬁcant. 12 multifactor ANOVA were performed as follows: (1 to 3) raw samples at 0.5 + 7 mo. 1993.and SO-fed groups during the 7 mo of frozen storage. Ajuyah et al. Thus. α-TA supplementation resulted in a signiﬁcant protection against oxidation for both raw and cooked samples at any storage time.. Despite that earlier studies indicated that LHP were not absorbed in the intestinal tract (Andrews et al. To determine whether the factors studied (fat source. This ﬁnding is possibly due to the low LHP level of the OSO. Fatty acid composition and α-tocopherol content were determined as in Grau et al. n = 288).EFFECT OF DIET ON CHICKEN MEAT OXIDATION 1633 Thiobarbituric acid values were determined by an acid aqueous extraction method with third-derivative spectrophotometry. interactions higher than order two were ignored and P ≤ 0. Moreover. 3. respectively. TBA values. In contrast.. Furthermore. We do not accept the dose of the oxidized oil as a cause of this absence of signiﬁcant effect. Galvin et al. as in our case. no signiﬁcant differences were detected between OSO.5 and 7 mo. and Galvin et al.25 for the SO and 4.. 1960. because the amount of oil used by Lin et al. (1993) and Sheehy et al. these studies reported that supplying oxidized oils decreased plasma and muscle α-tocopherol levels. (1997) reported that... 1994).. the highest COP content for raw and cooked samples was observed in SO. However. Galvin et al.
33y 41. 1998.9x AA supplementation (mg/kg of feed) 0 201. for raw or cooked samples).7 162.13 22.56 mg/kg for raw and cooked samples. P-values obtained from MANOVA for all raw and cooked samples together (n = 96).9 17.3 20.9 147. In fact.50 3. AA supplementation resulted in a prooxidant effect in terms of TBA values.736x 4. 7β-hydroxycholesterol. TBA values as milligram of malondialdehyde per kilogram of sample.3x 287.459 23.9 159.8 167.509y 2.1 170. cholesterol-5α.45y 20.5 173.5y 225 17.19 and 35. O’Neill et al. P-values obtained from ´ MANOVA. respectively (Table 2). A Interaction of dietary fat source × α-TA supplementation signiﬁcant at P ≤ 0.184y 2. P-values obtained from MANOVA (n = 48) for raw or cooked samples.8y 0.914y 42.7z 0. 25-hydroxycholesterol.1* 162.6β-epoxide.7 17.5 19. Ajuhah et al.05.435x 2.5 21.4Y 182.4 174.024x 3.5x 196. King et al.5 23.40 22.155x 2.0 0.8xy 198.6 156.1 0. c Interaction of α-TA × AA supplementation signiﬁcant at P ≤ 0. no studies have been found concerning LHP values in chicken meat from animals fed tocopherolsupplemented diets. Least-squares grand means (global means) and least-squares means for responses at different times of storage as inﬂuenced by factors1 α-TA supplementation (mg/kg of feed) LO 193.05. 1999).3x 1.8 172.05.396y 3.5* 169.20x 3. the effect of dietary supplementation with AA was not signiﬁcant in any case.0y 135.854 22. Jensen et al.478y 3.05.4 19.3x 0.1634 GRAU ET AL.7 OSO 215.8 212.802yz 26.6 0.9y 21. 1986.6 17. Lauridsen et al. 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 ≤ 0.6y 0.05.0 141.347z 26. 1995.4y 19.7 0.3Y 192.2x 11. Ruiz et al..445x 6.1*. Bartov.7* Fat source BT 183.4*.7 19.Y 1.9 16.15x 4.7y 1.084 23. LHP = lipid hydroperoxide.8 180. TA = tocopheryl acetate.7y 312. 1997a.8 174. King et al.0x 0. and α-tocopherol and COP content (mg/kg of sample)..809x 3.. 1 AA = ascorbic acid.4 20. E Interaction of α-TA supplementation × cooking signiﬁcant at P ≤ 0.26* 22.X 0. COP = cholesterol oxidation products. and 7-ketocholesterol. Determined COP were: cholestanetriol.041x 5.341y 3.59x 24.42 3.778x 21.05).2 a Interaction of dietary fat source × α-TA supplementation signiﬁcant at P ≤ 0. 1996.574x 21.5y 0.192y 2. Li et al.7 190.05. Superscripts obtained by means of the Scheffe test (α = 0. Pardue and Thaxton.31x 20.42x 3. 1993.7y 23. 1975.3 199.0x 0.8 0 381. 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). P-values obtained from multivariate ANOVA (MANOVA) (n = 48) for raw or cooked samples.Y 0.26x 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 Meat Raw Cookeda Rawabc Cookeda Raw Cooked Raw Cookeda Rawabc Cooked Rawa Cookeda Raw Cookeda Rawabc Cooked Rawab Cooked Raw Cooked Global means 199..2 150. 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.584 24. 1995.5y 1.6 19.969*. P-values obtained from MANOVA (n = 48) for raw or cooked samples.571y 2.273y 2.465x 3.407x 5.2 18. Marashiello et al.58 3.9 110 197.760y 1.7y 327. 1989a.8 0.158y 21.7 20.9 186..9y 0.6 0. 1996.3 18. x–z Means in the same row for a certain factor bearing no common superscripts are statistically different (P ≤ 0..0 20.7 124.2xy 0.05.85y 2. B Interaction of dietary fat source × AA supplementation signiﬁcant at P ≤ 0. 1997b). P-values obtained from MANOVA for all raw and cooked samples together (n = 96).8x 1. P-values obtained from MANOVA for all raw and cooked samples together (n = 96).5 167.6α-epoxide. P-values obtained from MANOVA n = 144.4x 344..0 181.092y 2.174x 4.554z 25.X 23.404y 3. 1977.8 150. Low concentrations of AA in meat lead to a prooxidant TABLE 2.436x 5. 1995.610 3.562y 21. *Denotes a statistically signiﬁcant difference between global means for raw and cooked samples (P ≤ 0.683 3. which was only signiﬁcant for raw meat (at all storage times) (Table 2). n = 48.70x 24. Superscripts obtained by means of the Scheffe test (α = 0.530 1. whether AA prevents or promotes lipid oxidation in meat is controversial (Benedict et al.3*.454y 3.521*.. cholesterol-5β.502y 0.4x 11.715x 1.306y 1. In contrast. For the other oxidation parameters.90y 3.0x 1.2 210.577y 44.5X 155.Y 24..05) indicate the inﬂuence of the storage time on global means. Lauridsen et al.407 1.05.. 2 LHP values expressed as mg cumene hydroperoxide/kg of sample.6 153.095x 4. supplementation of broiler diets with 225 mg of α-TA/kg of feed led to an overall increase of tocopherol in meat of 39.9 194. de Winne and Dirinick.092y 1.125y 2.5x 34.Y 0..1x 1. parameters (Table 2).6x 37.9y 1.9 20. 1999.2 SO 205.1x 1.262y 3..8y 0.8x 39.43x 2.7 19. for raw or cooked samples)..6y 0.2 16. 1995. .8 17. Ahn et al.1 21.7x 363. In fact.9 160.566 3.5 Responses2 0 mo of storage LHP valueDE TBA valueABCDE α-Tocopherol contentE 3.5x 0. b Interaction of dietary fat source × AA supplementation signiﬁcant at P ≤ 0.05.743x 3.8 177.2xy 198.558y 3. from our data. P-values obtained from MANOVA for all raw and cooked samples together (n = 96).1x 1.186yz 23.468*.
29 ND LO 20. at high concentrations.07 0.65 BT 34.04 2. 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.27 0. in systems with low levels of oxygen.19 1.96 39.13 0.04 2.EFFECT OF DIET ON CHICKEN MEAT OXIDATION TABLE 3. especially LO. 3 TR = traces.47 0.17 25.74 43.80 0.03 ND SO 22. 1986). 1996).04 0. samples from unsaturated diets gave higher oxidation values (Figure 3).73 0.26 0.61 Dietary fat source (BT = beef tallow. and trace-metal catalysis of this reaction has been demonstrated (Gregory.64 0.67 0. whereas at higher concentrations.15 0.03 0. SO = sunﬂower oil.09 34.48 96. anaerobic degradation of AA can take place. Mielche and Bertelsen.01 0. which means that basal level of this compound in feed is insufﬁcient to protect enriched-PUFA meats from oxidation. Decker et al.24 0.03 0.41 47. broilers were slaughtered after 18 h of feed withdrawal.69 0.50 24. Furthermore. such as vacuum-packaged samples.30 32. 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.29 16.25 38.89 0.04 17. as reviewed by Pardue and Thaxton.01 0.5 mo.12 0.36 23. This effect may be caused by the higher PUFA content in meats from these diets (Table 3). Moreover.33 0. In contrast.90 46. PUFA = polyunsaturated fatty acids. this low amount of AA present in raw meat may be easily degraded during cooking.63 40.13 0. at which the catalyst is more active in decomposing LHP to free radicals.22 0. In addition.08 41.13 0. Furthermore.02 0.44 0. This observation has been made when AA is an endogenous meat component and when it has been added postmortem.53 47.5 mo of storage.89 0.26 0. 1996).72 42.38 33.10 42. In contrast. 1990. 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 BT 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 1 2 2 1 1635 Cooked meat LO 20. resulting in no signiﬁcant differences between samples from animals fed α-TA-supplemented diets from the different fat sources.48 0. α-TA supplementation canceled the inﬂuence of the dietary fat.47 98.04 0. In the latter case. AA acts as an antioxidant (Roozen. although a similar trend was observed at the other time .40 0.85 ND4 SO 22. AA tended to prevent oxidation in meat from saturated diets (supplemented with BT).23 0. OSO = oxidized sunﬂower oil.08 0. 1998.14 0.04 0.01 0. 1994.25 0. when this supplement was not added.53 47. although a similar trend was observed.39 20.06 0.12 0.12 0. expressed as compensated area normalization (%). and insoluble protein promoting lipid oxidation (Decker and Welch. 1987. 1993).02 0.68 15.05 0.21 0.70 20.93 OSO 22.16 0.31 35.25 0.89 0. 1998).63 0.26 97. in our study.02 0.01 21.02 0. SFA = saturated fatty acids.05 17.02 0.74 0.24 0.27 0. SO.43 35.03 0.56 0. Frankel. AA shows an antioxidant effect because its ability to scavenge oxygen and lipid free radicals predominates (Decker and Xu.87 0.08 42.01 21.34 99. This process occurs even when only residual oxygen is present in the food package (Greg- ory.83 0. In contrast.02 0.09 0.43 1.47 ND OSO 22.02 0.01 0.22 38.51 0. ascorbate may also release iron from ferritin. leading to the lack of prooxidant effect observed in cooked samples.75 0. AA resulted in a prooxidant effect when an unsaturated fat (LO.12 0. MUFA = monounsaturated fatty acids. 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. effect by reducing free transition metals such as Fe(III) or Cu(II) to lower valence states [Fe(II) and Cu(I)]. Frankel. interaction between dietary fat source and α-TA supplementation was signiﬁcant for all oxidative parameters except for LHP values at 0 and 3.97 33.26 0.15 0.82 0. and plasma AA levels decrease rapidly after the removal of dietary supplementation (Pardue and Thaxton.47 0. 1998.14 0. LO = linseed oil). 1998).26 0. or OSO). In raw samples.03 16. up to 200 to 300 mg of AA/kg of meat results in a prooxidant activity. Fatty acid composition.03 0. Furthermore.23 0.87 0. 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. was fed (Figure 2).47 0.05 42.88 0.04 0.77 0.22 0.92 0.02 TR3 0. 1986) and of the low supplementation applied in this study.04 0.62 34. In addition. which rendered them more labile to prooxidant agents.09 0.04 1. Interactions Between Dietary Factors In raw samples.06 40.29 0..07 18.12 0.44 0.27 0.06 40.08 0. 4 ND = not determined.03 0.24 0. membrane lipids.02 0.16 24.26 0.02 0.05 1.32 0. Decker and Xu.13 0.
Ahn et al. Inﬂuence of Cooking Cooked samples showed signiﬁcantly higher TBA and COP values (Table 2). and thermal decomposition of hydroperoxides to prooxidant species. AA supplementation had no inﬂuence on α-tocopherol content of meat (Table 2). and concluded that the amount of PUFA was the main determinant of interspecies differences in lipid oxidation rate in cooked meats. BT = beef tallow. It is noteworthy that. 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. Galvin et al. SO = sunﬂower oil. for both raw and cooked samples. COP = cholesterol oxidation products. 1998). FIGURE 2. (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.. and for all the storage periods and parameters studied. Pikul et al. 1996. Pikul et al. In addition. which was also observed by Lauridsen et al. Jadhav et al. Cooked samples showed behavior similar to raw samples (Figure 4)... no differences were found between samples from α-TA. Decker and Xu. such as alkoxyl and hydroxyl radicals (Rhee. AA resulted in a prooxidant activity. 1988. 1995. Interaction Between Cooking and Dietary Factors Interaction between cooking and dietary fat source was always signiﬁcant. 1998.. 1984. Kesava Rao et al..5 or 7 mo (Table 2). except for LHP values at 3. OSO = oxidized sunﬂower oil. Kowale et al. regardless of the dietary fat source (Figure 4). Frankel. α-TA supplementation reduced LHP values to the same level. 1974. Interaction between α-TA and AA was only signiﬁcant for TBA values from raw samples (at any storage time). although this interaction was not signiﬁcant for TBA and COP values at 3. Between them. (1997b) in breast and leg meat from chickens fed different doses of AA (0. This higher susceptibility to cooking related oxidation in chicken leg meat from unsaturated diets has also been observed by other authors (Ruiz et al.. α-tocopherol in raw samples from LO diets was similar to that of samples from BT and OSO groups. oxidation values were not as low as those from the other fat sources.and from α-TA-plus-AA-supplemented groups. disruption of cell membranes. 1998) and has been attributed to various factors. In contrast. 1995. Maraschiello et al.. In the absence of α-TA. Cooking-related oxidation has been reported in the literature for different cooking methods (Love and Pearson.1636 GRAU ET AL. 420 or 840 mg/kg of feed). transformation of myoglobin from an antioxidant to a prooxidant species. 210. which can lead to the loss of antioxidant enzyme activity (e. 1997. which was canceled by α-TA supplementation (Figure 5). inactivation of catalase and glutathione peroxidase) or the release of iron from metalloproteins (mainly myoglobin). which brings PUFA and cholesterol into contact with prooxidants. protein denaturation. 1996. Accordingly. LO = linseed oil. Despite that meat from LO diets showed the greatest decrease in TBA values due to α-TA supplementation. (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. Paniangvait et al.. 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. In addition. Rhee et al. (1997) for breast and leg meat. the highest difference in TBA values between cooked and raw samples corresponded to meat from LO diets.. but oxidation of these groups was not different. and the lowest to that from BT diets (Table 2).5 mo of storage. cooking had a greater inﬂuence on TBA values of samples from OSO than SO diets. 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%). Furthermore. .g. chicken and pork. After cooking (0 mo of storage). at 0 mo.. points) (Figure 3). MDA = malondialdehyde. 1996. King et al. which was also reported by Galvin et al. Similarly. 1999) and has been attributed to the higher PUFA content of these samples (Table 3). (1996) compared the lipid oxidation potential of beef.
LHP signiﬁcantly increased after the ﬁrst 3. In addition. 1996). However... In raw samples. thermal decomposition of LHP was much less important. In contrast. 1995.. LHP values from samples at 0 mo of storage were signiﬁcantly lower in cooked than in raw meat.EFFECT OF DIET ON CHICKEN MEAT OXIDATION 1637 FIGURE 3. FOX reaction was incubated for 4 h and. because initial LHP values were much lower and.. which would be more prone to LHP formation. it must be remembered that the FOX method used to measure LHP values is. SO = sunﬂower oil. in cooked samples.5 and 7 mo of storage. in samples from supplemented diets. which was not signiﬁcant. BT = beef tallow. (1989) to 1. given by α-TA. and COP). This unbalance is less marked in samples from unsaturated fat sources. In contrast. For both parameters. lipids from the sample undergo some oxidation that may be enhanced by the prooxidants released during cooking. In addition. This decrease in TBA values was also observed by other authors (King et al.5 mo. 2000c). α-TA supplementation reduced it (Table 2). TBA values tended to increase during the whole period. LHP.. at 3. Inﬂuence of the Storage Time and Its Interaction with Other Factors Oxidation of samples was inﬂuenced by storage.9 times after 6 mo in the study of Pikul et al. 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%). 1995. meat samples from diets without α-TA supplementation gave lower LHP values after cooking (Table 2). Oxidative stability toward cooking. Differences in the magnitude of this increase [from 4. and TBA values decreased (Figure 6). MDA = malondialdehyde. On the other hand. which could be attrib- uted to the above-mentioned decomposition of LHP to secondary oxidation products during the cooking procedure (Frankel. OSO = oxidized sunﬂower oil. destruction of LHP to secondary oxidation products predominates over the formation of new LHP molecules. Besides. Rhee et al. LO = linseed oil. at 0 mo of storage. LHP values did not change signiﬁcantly after cooking. because prooxidant conditions favored by cooking involved greater LHP formation during storage of samples with a higher unsaturated fatty acid proﬁle. although nonsigniﬁcantly. although the lower decrease. LHP values signiﬁcantly decreased during the ﬁrst 3. 1998). the behavior of LHP and TBA values from raw or cooked samples was different (Figure 6). during this time. during cooking. consequently. unsaturated diets resulted in cooked samples with higher LHP values than the raw ones (Table 2). While AA did not affect sample oxidation during cooking..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. This result could be because. 1984. corresponded to meat samples from LO diets (Table 2). Such an increase in TBA values during frozen or chilled storage has also been reported for raw samples packaged in air (Pikul et al. 1993). 1997). Galvin et al.5 mo of storage. This was evident for all fat sources. 1989. In contrast. an induced method (Grau et al. changes during the second period (3. For all oxidative parameters (TBA. to a certain extent. CHP = cumene hydroperoxide. 1997) in non-vacuum- . In this case..5 to 7 mo) were not signiﬁcant. oxidation induced by cooking was signiﬁcantly lower in α-TA-supplemented groups (Table 2). has been also described in terms of TBA values by other authors (King et al. Galvin et al.
BT = beef tallow. Aubourg. 1993.5. TBA values of raw dark chicken meat samples stored at −20 C for 0.1638 GRAU ET AL. 3. Lipid hydroperoxide (LHP) and TBA values. This agrees with the fact that LHP values in cooked samples increased signiﬁcantly only during the ﬁrst period of storage (Table 2). 1986. FIGURE 6. respectively).5 to 5 mo. Wen et al. LO = linseed oil. The different behavior of LHP values of raw and cooked samples during storage could be explained by the FIGURE 5. 1967. OSO = oxidized sunﬂower oil. MDA = malondialdehyde. . MDA = malondialdehyde. as previously explained (such as liberation of iron and disruption of cellular membranes). Furthermore. or 7 mo as affected by dietary ascorbic acid (AA) and α-tocopheryl acetate (α-TA) supplementation (110 and 225 mg/kg of feed.5 mo. Esterbauer et al. this nonheme iron increased during storage of the meat at −20 C from 0 to 2. Whang et al. Rhee et al. CHP = cumene hydroperoxide.. According to this. 1991. prooxidant conditions induced by cooking.. 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. 1996). Evolution of lipid hydroperoxide (LHP) and TBA values of raw or cooked dark chicken meat as inﬂuenced by storage period at −20 C. but it remained steady from 2.. (1996) found a higher content of nonheme iron in cooked chicken leg meat compared with raw. In addition. changes in FIGURE 4.. CHP = cumene hydroperoxide. which led to a higher LHP production through the storage and during the incubation of the FOX reaction (Grau et al. SO = sunﬂower oil. 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%). 2000c).
5 mo (n = 48) 0.7994 (<0. 1987. In contrast. (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.9287 (< 0. despite that TBA and COP values are not correlated in cooked samples. . These differences may account for the disagreement in the results.. Ruiz et al. 1999). 1989a. which allows the conclusion that α-tocopherol is a key factor in avoiding the formation of fatty acid and cholesterol oxidation products.00005) — 7 mo (n = 48) 0. (1995).6466 (0. 1988). beef (Park and Addis.00005) Whole period (n = 144) 0.5304 (<0.0001) 0. Ruiz et al.00005) — COP = cholesterol oxidation products. However.0029) —3 — −0. In addition.. 1989a). Pearson’s correlation coefﬁcient. To sum up. which was claimed to be important in lipid oxidation in chilled stored meat. Correlations between oxidative parameters and α-tocopherol content in raw dark chicken meat samples Storage time Oxidation values1 TBA-LHP TBA-COP LHP-COP TBA-α-tocopherol LHP-α-tocopherol COP-α-tocopherol 1 2 0 mo (n = 48) 0. and stored at −20 C for 7 mo.. 1998). and pork raw or cooked meat (reviewed by Jensen et al.00005) — — −0. 9 mo).. However.4863 (0.00005) −0. and SO or lard supplemented with 200 mg/kg of α-TA (Marashiello et al. which justiﬁes the ﬁnding that supplemented samples were highly protected from oxidation during the whole study (Table 2).00005) −0. 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. Sheehy et al. Galvin et al. for both raw and cooked samples. (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.00005) −0. In contrast...0002) — — −0.9477 (<0. Ahn et al. 1998).. 10 d) or freezer storage (−12 C. 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. and stored at 4 C (0 to 12 d).. thus favoring oxidation (Ang and Huang. which means an increased amount of oxygen.. turkey. 1989a.5928 (<0. Stability of α-tocopherol during frozen storage has been previously described by King et al. Galvin et al.EFFECT OF DIET ON CHICKEN MEAT OXIDATION 1639 nonheme iron of raw leg meat during the 5 mo of frozen storage were not signiﬁcant (Rhee et al. The inﬂuence of AA during storage has been poorly studied.4931 (<0. 1998). dietary fat source or AA supplementation did not inﬂuence meat stability during storage. 1993). 1999) or frozen storage (Lin et al. 1994). 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. Positive correlation between COP content and TBA values has been reported in cooked samples from chicken and turkey (Park and Addis.00005) — 3.00005) 0. in those works. Furthermore.. 1997.5842 (<0.5149 (0. those studies were carried out in nonvacuum-packaged samples..42042 (0. samples had been trimmed of extramuscular fat. the negative correlation between TBA values and α-tocopherol content was more pronounced TABLE 4. and pork (Monahan et al. Several studies also reported beneﬁcial effects of dietary tocopherols on chilled or frozen storage stability of chicken. In addition. 1996). TBA = 2-thiobarbituric acid values. 1992).. cooked after grinding. (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. 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. P-values are stated in parentheses. 1993. Only TBA and COP values for cooked samples failed to show a signiﬁcant correlation. Kanner et al.. On the other hand. LHP = lipid hydroperoxide values.9329 (<0. 1987. there was always a highly signiﬁcant negative correlation between oxidative parameters and α-tocopherol content. de Vore. vacuum-packaged. Endogenous α-tocopherol of raw or cooked samples did not change throughout the 7 mo of frozen storage.0001) −0.00005) −0. Moreover.8320 (<0. non-vacuumpackaged.0005) −0. all oxidative parameters are inversely correlated with α-tocopherol content. our samples containing meat plus skin were ground after cooking.9306 (<0. 3 COP values were only determined in samples stored for 7 mo. Correlations Between Results from the Different Methods Correlations between results are stated in Tables 4 and 5.5331 (0.. Lauridsen et al. 1999).
J. Internal temperature and packaging system affect stability of cooked chicken leg patties during refrigerated storage. U. Lopez-Ferrer (UAB) in breeding animals. α-tocopherol. Alonso. Hardin. Guardiola. N. 58:278–282. On the contrary. Jessup. 1993. SO. E. S. 61.. Sim. TBA = 2-thiobarbituric acid values. Food Sci. P-values are stated in parentheses. W. J.. Green.. Nutr. This work was supported in part by research grants ´ from the Comissio Interdepartamental de Recerca i Inno´ ` ´ vacio Tecnologica (CIRIT). TABLE 5. AA supplementation (110 mg/kg) was clearly useless and showed no synergism with α-TA. H. Vassilopoulos. Consequently. 1993. or LO). endogenous natural antioxidants or free iron content). Poultry Sci. D.00005) −0. and J. F.7048 (<0. 1994. NY. 1999. S. R.. 1993. W. Papageorgiou. Int. F. and the Instituto Danone. Dietary antioxidants and storage affect chemical characteristics of ω-3 fatty acid enriched broiler chicken meats. O. A. D. 2001. 58:265–269. R. and M.6204 (<0. D.00005) — 3.5953 (<0. the oxidation values obtained by means of different analytical methods greatly depend on several factors. Grau. such as processing and storage conditions.00005) — — −0. F. Nutr. J. and ascorbic acid supplementation on sensory quality of dark chicken meat.00005) NS 0. and A. Erra (all from University of Barcelona) helped in laboratory work. Huang. 1977. T.00005) — COP = cholesterol oxidation products. A. A. Agric. Rapid.00005) Whole period (n = 144) 0. P. and in cooked than in raw samples (Tables 4 and 5).9094 (<0. Murrell. 18:553–555. Ajuyah.00005) — — −0. and packaging inﬂuences on lipid stability in broiler chicken breast and leg muscle. Brown. J. 42:1931–1937. Swift. Codony. Ahn. New York. H.1640 GRAU ET AL. 1995. Inﬂuence of dietary fat source. it is very difﬁcult to compare oxidation values from different studies. Br. C. Review: Interaction of malondialdehyde with biological molecules—New trends about reactivity and signiﬁcance. and J. Codony. Botsoglou. and R. Jordan. Grifﬁth.62122 (<0. Guardiola. I. Trakatellis. 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 1 2 0 mo (n = 48) 0. F. Ang. V. Sci. Marcel Dekker. Y.6250 (<0. Food Sci. which indicates that the protective effect of the antioxidant is more relevant when these processing operations are involved. J.. C.. ACKNOWLEDGMENTS ´ A. Barroeta.. Oxysterols and atherosclerosis.. and R. B. G.9191 (<0. W.00005) −0. Benedict. and speciﬁc thiobarbituric acid method for measuring lipid peroxidation in animal tissue. S. Food Sci. R. 1996. 80:800–807. 277. A.. Food Chem.5 mo (n = 48) 0. C. . Ahn. J. J.5236 (0. Br.00005) −0. and Y. and J. Toxicity of air-induced soybean oil. Food Sci.. in meats. R. A. Wolfe. Andrews. D. G.00005) −0. Pearson’s correlation coefﬁcient. the results demonstrate that. McDonald and D. and ´ S. B. Analysis and health effects of cholesterol oxides. S.5845 (<0. and R. and feedstuff samples. J. A. A. H. unsaturation degree of the sample. after 3. regardless of the dietary fat source (BT. 1975.5812 (<0. J. 1960.5610 (<0.00005) — 7 mo (n = 48) 0. 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.9368 (<0. Park. U. Sim. LHP = lipid hydroperoxide values. A. Wolfe. 23:167–173. Food Sci. Dietary α-linolenic acid and mixed tocopherols. Bartov. T. Technol. Stein. 70:199–210.. Aubourg. Oxygen availability affects in prooxidant catalyzed lipid oxidation of cooked turkey patties. 1993.. P. S. U. A.00005) —3 — −0. D.5 or 7 mo of storage than at 0 mo. 60:1013–1018. 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). Poult. Sim. and W. D.7260 (<0. ed. J. Ajuyah. 28:323–335. F. P. 3 COP values were only determined in samples stored for 7 mo. Grimpa. N. S. In addition. Ferrer. Bunyan. E. W. Cawhorne. A. Effect of lipid antioxidants on the stability of meat during storage.. Bou. OSO.. Lack of effect of dietary ascorbic acid on stability of carcass fat and meat of broilers. Pages 199– 240 in: Food Lipids and Health. Min. J. provided α-TA and AA. 22:97–110. and C. A. J. Ahn. Manich. Agric. J. 58:43–46. E. food. the Comision Interministerial ´ de Ciencia y Tecnologıa (CICYT). Dipolck.9056 (<0. F. sensitive. Atherosclerosis 142:1–28. HofffmanLa Roche Ltd. A. and M.e. Cuit’s provided slaughter and processing facilities.0001) −0. E. Mead. Food Sci. Fletouris. J.00005) −0. J. and other intrinsic features (i. J Mantis. 1968. On the postulated peroxidation of unsaturated lipids in the tissues of vitamin E-deﬁcient rats. REFERENCES Addis. Strange.
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