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Lipid and Protein Oxidation of Broiler Meat as Influenced by Dietary Natural Antioxidant Supplementation

K. Smet^*,1, K. Raes^*,2, G. Huyghebaert, L. Haak^*, S. Arnouts and S. De Smet^*,3

^* Laboratory for Animal Nutrition and Animal Product Quality, Department of Animal Production, Ghent University, Proefhoevestraat 10, 9090 Melle, Belgium; Animal Research Unit, Institute for Agricultural and Fisheries Research, Flemish Government, Scheldeweg 68, 9090 Gontrode, Belgium; and INVE Technologies NV, Hoogveld 93, 9200 Dendermonde, Belgium

³ Corresponding author: Stefaan.Desmet{at}UGent.be

	ABSTRACT

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Natural tocopherols (TC), rosemary (RO), green tea (GT), grape seed, and tomato extracts were supplemented in single and in combinations at total concentrations of 100 and 200 mg·kg^–1 of feed in a 4% linseed oil-containing diet to investigate the oxidative stability of broiler breast muscle. Supplementation with 300 mg·kg^–1 of synthetic antioxidants alone and synthetic antioxidants with -tocopheryl acetate at a concentration of 200 mg·kg^–1 (100 IU) feed was used as a control. Fresh patties were prepared and stored under light at 4°C. After freezing for 8 mo and overnight thawing, 3 other patties were prepared and similarly stored under light at 4°C. During display, samples were evaluated for oxidative stability measurements. For lipid oxidation, the treatment with synthetic antioxidants and 200 mg·kg^–1 of -tocopheryl acetate yielded the lowest TBA reactive species (TBARS) values. For TC, grape seed, and tomato extracts, TBARS values for 100 mg·kg^–1 were higher (P < 0.05) than 200 mg·kg^–1 treatments, whereas no differences (P > 0.05) in TBARS values were observed for RO between 100 and 200 mg·kg^–1. In contrast, GT showed higher TBARS values at 200 mg·kg^–1. Administration of combinations of TC, RO, and GT did not reveal synergistic effects but confirmed the increase in TBARS values with increasing doses of GT. No differences (P > 0.05) among the different antioxidant treatments were detected for protein oxidation. The muscle -tocopherol content linearly responded to the feed -tocopherol content and thus there were no indications for a sparing effect on -tocopherol from other antioxidant treatments. In summary, dietary natural antioxidant extracts were less effective than the treatment with synthetic antioxidants combined with -tocopheryl acetate for protecting against oxidation, but there were marked differences between different natural antioxidant extracts.

Key Words: oxidative stability • natural antioxidant • broiler meat • lipid oxidation • protein oxidation

	INTRODUCTION

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Oxidative damage occurs in the living animal due to an imbalance between the production of reactive oxygen or nitrogen species and the defense mechanism of the animal against oxidative stress. Oxidation is inherent to metabolism, but an excessive formation of reactive species in oxidation processes can cause damage to vital components in biological systems (Halliwell et al., 1995). Oxidation increases as a result of a high intake of oxidized lipids, oxidation of sensitive polyunsaturated fatty acids (PUFA) or prooxidants, or a low intake of nutrients involved in the antioxidant defense system (Morrissey et al., 1998). Oxidation is a very general process, which affects lipids, pigments, proteins, DNA, carbohydrates, and vitamins (Kanner, 1994). In muscle and fat tissue, oxidation continues postmortem and affects the shelf-life of meat and meat products.

It is generally accepted that lipid oxidation is one of the primary mechanisms of quality deterioration in foods, especially in meat products (Kanner, 1994; Morrissey et al., 1998). The latter becomes more important because of a trend toward increasing the (long-chain) PUFA content in meat. Although proteins are the major compounds of most biological systems, little research has been performed on protein oxidation. Proteins are complex targets, comparing the backbone and 20 different side chains as potential targets with the more limited number of reactive sites in DNA and lipids. Furthermore, a whole range of reaction products can be formed using very different mechanisms (Davies, 2005).

To maximize the oxidative stability of meat, antioxidants, mostly -tocopheryl acetate (ATA), are added to feeds. The beneficial effect of dietary ATA supplementation for the subsequent enhanced stability of lipids in muscle foods has been extensively reported for poultry, beef cattle, veal calves, and pigs (Gray et al., 1996; Jensen et al., 1998). In addition, an increasing number of studies have reported on the antioxidant properties of plant extracts and compounds in vitro or when added during food processing (Schwarz et al., 2001; Halvorsen et al., 2002; Pellegrini et al., 2003). Furthermore, several studies have been performed investigating the effect of dietary administration of natural antioxidants on the oxidative stability of meat or meat products (Tang et al., 2000; Botsoglou et al., 2002; Mason et al., 2005; Haak et al., 2006; O’Grady et al., 2006; Goni et al., 2007).

The objective of this study was to investigate the effect of supplementation of a diet of broilers with plant-derived extracts, rich in natural antioxidants, on the oxidative stability of meat. The effects of individual extracts were tested, as well as combinations of extracts to infer possible additive or synergistic effects between these antioxidants.

	MATERIALS AND METHODS

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Birds and Experimental Design

Two thousand forty 1-d-old chickens (Ross 308, males) were divided over 60 pens (34 chickens per pen) and were fed a diet containing 4% refined linseed oil and 1 of 20 antioxidants or antioxidant mixtures (3 pens per treatment) for 6 wk. The diets of each phase (3 phases) were prepared a few days before consumption and fed during 2 wk. For the feeding period, the diets were stored in a dark barrel in the stable for a maximum of 7 d. The diets were formulated to an equal protein and energy content (Table 1). In the vitamin-mineral premix, no synthetic antioxidants were added, but a basal amount of 20 mg·kg^–1 (10 IU) of ATA was present to meet the physiological requirements.

The experimental antioxidants were mixed in the refined linseed oil before the feed manufacturing and were supplemented separately in 1 of 2 doses (100 or 200 mg·kg^–1), making 10 treatments. In addition, TC, RO, and GT were supplemented in equal proportions in all combinations 2 by 2, and all 3 were combined at a final concentration of 100 or 200 mg·kg^–1, formulating 8 additional treatments. Supplementation with a mixture of 300 mg·kg^–1 of synthetic antioxidants [160 mg·g^–1 of butylated hydroxytoluene, 100 mg·g^–1 of ethoxyquin, 15 mg·g^–1 of butylated hydroxyanisole, and 725 mg·g^–1 of vegetable oil] alone (SYN) and synthetic antioxidants with 200 mg·kg^–1 (100 IU) of ATA (SYN + ATA) were also included. All extracts were supplemented at 100 or 200 mg of product·kg^–1 of feed and not on an active compound basis. These 20 antioxidant treatments were replicated in 3 pens with 34 chickens per pen (Table 2).

At the time of slaughter (42 d of age), 5 birds per pen close to the average pen weight (mean BW = 2,810 g) were selected and slaughtered on 2 successive days, with each day 1 or 2 pens per treatment handled. The birds were killed by cervical dislocation, bled, eviscerated, and immediately sampled without prior chilling. The right portion of the breast muscle (pectoralis major) of the 5 selected animals was pooled and minced with a conventional meat grinder (Omega TE22, Lima Food Machinery, Evesham, Worcestershire, UK). From this sample, a sub-sample was vacuum-packed and stored at –18°C until determination of the -tocopherol content and the fatty acid profile of the meat, after 8 and 10 mo of frozen storage, respectively. The remainder was used for oxidative stability measurements on fresh and frozen meat. For the measurements on fresh meat, 3 fresh patties (approximately 100 g) were prepared, wrapped in an oxygen-permeable polyethylene film, and placed in an illuminated chill cabinet (illuminance of 1,000 lx, temperature 3°C) for 10 d. After freezing for 8 mo and overnight thawing, 3 other patties (approximately 100 g) were prepared, similarly wrapped in an oxygen-permeable polyethylene film and placed in an illuminated chill cabinet for 11 d. The fresh meat patties were assayed for lipid oxidation after 3, 7, and 10 d of storage in the chill cabinet, whereas protein oxidation was assessed at d 3 and 10. The meat patties from frozen and thawed meat were analyzed for lipid oxidation after 1, 4, and 11 d of storage in the chill cabinet, whereas analyses for protein oxidation were only performed on d 11 of display.

Analyses

Fat extraction was conducted to prepare the sample for fatty acid analysis using chloroform:methanol (2:1; vol/vol) and a method described by Folch et al. (1957). The extracted fat was methylated, and fatty acid analysis was performed by gas chromatography with a HP 6890 (Agilent, Diegem, Belgium) as described by Raes et al. (2001). Results were expressed as grams per 100 g of fatty acid methyl esters. Lipid oxidation was assessed by the TBA reactive species method (TBARS) based on Tarladgis et al. (1960) and is expressed as micrograms of malondialdehyde (MDA) per gram of tissue. Oxidative damage to proteins was determined by measuring the decrease in the amount of thiol groups. Thiol groups are expressed as nanomoles of free thiol groups per milligram of protein (Mercier et al., 1998). -Tocopherol levels in the breast muscle and the feed were determined using HPLC, as described by Desai (1984). Results are expressed as milligrams of -tocopherol per kilogram of muscle or feed, respectively.

Statistical Analysis

A completely randomized design was used with 3 replicates per treatment. Pen was used as an experimental unit. The broiler performance and the fatty acid composition were analyzed using 1-way ANOVA with antioxidant treatment as a fixed factor. Comparison of means was performed using Duncan’s multiple range test as a post-hoc test (P < 0.05). Lipid and protein oxidation data were analyzed by a linear model including the fixed effects of antioxidant treatment and days of storage. The interaction term was not significant and was therefore not included in the model. The TBARS values were log-transformed to account for heterogeneity of variances. To test specific hypotheses, contrasts were defined. The effect of days of storage was considered across all dietary treatments. All antioxidant treatments were separately tested against the treatment SYN and SYN + ATA (e.g., SYN vs. 200 GS and SYN + ATA vs. 200 GS; for treatments, see Table 2). In addition, the separate antioxidant treatments were compared with each other across both doses for their capacity to slow down lipid oxidation [e.g., (100 TC + 100 RO) vs. (50 TC + 50 RO)]. Also, dose effects were tested (e.g., 100 TC vs. 200 TC), and finally, possible synergistic effects were examined by comparing separate anti-oxidant treatments with the corresponding combined treatment [e.g., (100 TC + 200 TC) vs. (100 RO + 200 RO)]. All statistical analyses were performed in S-Plus 6.1. Unless otherwise stated, all analyses were performed using P < 0.05.

	RESULTS

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Broiler Performance

The results of broiler performance are reported in Table 1. Some significant differences between the different anti-oxidant treatments could be observed (not shown). However, these differences are probably not caused by the antioxidant treatments but are due to random variation and limited replications, resulting in unreliable zootechnical data.

Meat Fatty Acid Composition

The mean total fatty acid content of the chicken muscle was 0.94 (SD 0.19) g of fatty acid methyl esters·100 g^–1 of muscle. The fatty acid composition of the meat is composed of 26.4% saturated fatty acids, 30.5% monounsaturated fatty acids, and 39.4% PUFA. By using 4% linseed oil in the diet, the n-3 PUFA proportion was relatively high (23.1%) at the expense of the n-6 PUFA proportion (16.2%). Supplementary dietary antioxidants did not affect the fatty acid profile of the breast muscle (P > 0.05).

Lipid Oxidation

Across dietary antioxidant treatments, TBARS values increased significantly with time of storage but remained overall low for the fresh meat patties (<0.8 µg of MDA·g^–1 of muscle). After frozen storage for 8 mo, TBARS values on d 1 of display remained rather low across the dietary antioxidant treatments (<0.25 µg of MDA·g^–1 of meat), although a considerable increase in TBARS values was observed during chilled storage under light (Table 2).

Compared with all other antioxidant treatments, the SYN + ATA treatment resulted in the lowest TBARS values (P < 0.05), which almost remained unchanged during chilled storage under light for fresh meat and hardly increased (to 0.5 µg of MDA·g^–1 of meat) after frozen storage. However, the SYN treatment also showed lower TBARS values than the 100 mg·kg^–1 of GT and TO treatment, the 200 mg·kg^–1 of GT treatment, and the combination of 50 mg·kg^–1 RO and 50 mg·kg^–1 of GT (P < 0.05) for both fresh meat and after frozen storage. When comparing the different antioxidant extracts, the treatments with TC resulted in significantly lower TBARS values than the 4 other antioxidants (P < 0.05). Further, RO also showed significantly lower TBARS values than the GS and GT treatments (P < 0.05), for fresh meat. After frozen storage, significantly lower TBARS values were observed for the treatments with TC than for GT and TO. Further, the RO treatment reduced TBARS more efficiently than TO, and GT resulted in lower TBARS values than TO.

For the different natural antioxidant treatments, some dose effects were observed. For the fresh meat, TC, GS, and TO showed lower TBARS values at 200 vs. 100 mg·kg^–1 (P < 0.05), whereas for the RO treatment, no difference could be observed between the 2 doses (P > 0.05). In contrast, TBARS values were higher for the 200 mg·kg^–1 compared with the 100 mg·kg^–1 GT treatment (P < 0.05). The combination of RO and GT inhibited lipid oxidation more when supplemented in a combined dose of 200 mg·kg^–1 compared with 100 mg·kg^–1 (P < 0.05). No dose effect was observed when TC was supplemented in combination with RO or GT (P > 0.05). The combination of TC, RO, and GT at a combined dose of 200 mg·kg^–1 yielded significantly lower TBARS values compared with the combined dose of 100 mg·kg^–1 (P < 0.05). After frozen storage, similar results were obtained comparing the different doses, although less pronounced.

Investigating possible synergistic actions, the combined treatments were compared with the single antioxidant additions. For fresh meat, the combination of RO and GT at 100 and 200 mg·kg^–1 resulted in significantly (P < 0.05) lower TBARS values than the single doses of RO and GT, whereas the combination of TC and GT at 200 mg·kg^–1 did not result in lower TBARS values compared with the single additions at 100 mg·kg^–1 (P > 0.05). However, this treatment yielded significantly higher TBARS values compared with 200 mg·kg^–1 of TC alone and significantly lower TBARS values compared with 200 mg·kg^–1 of GT alone. Further, for the combination of TC and RO and GT at 200 mg·kg^–1, lower TBARS values were observed than for the 66 mg·kg^–1 TC, RO, or GT treatments alone. In contrast, after frozen storage, the combination of TC and GT at 200 mg·kg^–1 yielded significantly (P < 0.05) lower TBARS values compared with 200 mg·kg^–1 of TC or 200 mg·kg^–1 of GT alone. The combination of RO and GT at 100 mg·kg^–1 resulted in significantly higher TBARS values than 50 mg·kg^–1 of RO or GT alone.

Protein Oxidation

The thiol content of the fresh meat patties did not decrease between d 3 [72.97 (3.66) nmol of free thiol groups·mg^–1 of protein] and d 10 [72.39 (4.67) nmol of free thiol groups·mg^–1 of protein] of display (P > 0.05). In addition, no differences between antioxidant treatments were observed. No measurable increase in protein oxidation occurred in the frozen meat patties, when comparing the values after 11 d [73.75 (5.96) nmol of free thiol groups·mg^–1 of protein] of display to the values of the fresh meat patties. Furthermore, no effect of antioxidant treatment on protein oxidation in the frozen meat patties was observed after 11 d of storage (P > 0.05).

Meat -Tocopherol Content

A close relationship between the dietary -tocopherol content and the amount of -tocopherol deposited in the muscle tissue was observed (mg of -tocopherol·kg^–1 of breast meat = 0.0699 x mg of -tocopherol·kg^–1 of feed + 0.9064; R² = 0.927). The supplementation of -tocopherol, delivered as natural or as acetate form, did not result in a different incorporation. The other antioxidants, combined with TC, did not influence the -tocopherol deposition in muscle tissue.

	DISCUSSION

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Compared with other meats, chicken meat is relatively abundant in PUFA, including the key n-3 fatty acids, because diets of fast-growing broilers are generally rich in PUFA (Asghar et al., 1990; Rhee et al., 1996). Furthermore, the fatty acid composition of the diet is reflected in the fatty acid composition of the meat. In this study, the -linolenic acid content was high as a result of 4% linseed oil feeding. This high-PUFA content was chosen to induce oxidation.

An increase in PUFA content influences lipid oxidation and can affect color, flavor, and, subsequently, oxidative stability during suboptimal storage (Basmacioglu et al., 2004). However, lipid oxidation can be retarded by the use of dietary antioxidants. It has been shown that dietary ATA supplementation results in good oxidative stability (Lopez-Bote et al., 1998; Cortinas et al., 2005). Recently, however, the potential beneficial effects of dietary supplementation with plant extracts rich in antioxidants have been investigated.

The TC had the greatest antioxidant action against lipid oxidation, followed by rosemary, when comparing the different natural antioxidant extracts. However, caution is required when applying the results of the different antioxidant treatments, because commercial extracts were used that were not fully characterized and may contain different levels of active compounds.

The TBARS values of the patties from fresh as well as from frozen meat were by far the lowest for the SYN + ATA treatment, demonstrating that none of the applied natural antioxidant extracts performed better in retarding lipid oxidation in meat postmortem than dietary ATA. In addition, the SYN treatment resulted in TBARS values comparable to or even lower than the values of the other treatments, suggesting that either several natural antioxidant extracts stimulated rather than retarded lipid oxidation or that the synthetic antioxidants did have an antioxidant action in meat postmortem. Koreleski et al. (2003) also observed stabilizing properties of butylated hydroxytoluene, butylated hydroxyanisole, and ethoxyquin in egg yolk after supplementation in feed. When setting up the study, we hypothesized that the synthetic antioxidants would protect the feed against oxidation during storage but would have no antioxidant action in muscle tissue in vivo and postmortem. This reasoning does not seem justified, and the lack of a negative control in which no antioxidants are added to the linseed oil does not allow determining if the natural extracts had any positive or negative effects at all in respect to oxidation. However, in view of the differences between the treatments, it is unlikely that the natural antioxidants did not have any effect at all.

There was more oxidative protection when TC, TO, and GS were included in the diet at a level of 200 compared with 100 mg·kg^–1. These findings confirm the work of Lau and King (2003) for GS and of Coetzee and Hoffman (2001) for TC. For GT, on the other hand, higher TBARS values were observed with increasing dose. This is in contrast with the results of Tang et al. (2000), who observed a clear antioxidant dose-response effect at levels of 100 to 300 mg of catechins·kg^–1 of feed. Differences between our study and the one of Tang et al. (2000) could be due to a different content of catechins present in the GT extracts. Dietary administration of tea catechins to cattle and pigs at levels of 1,000 mg·d^–1 and 200 mg·kg^–1, respectively, did not show any effect on lipid oxidation of meat (Mason et al., 2005; O’Grady et al., 2006). Other authors have reported positive effects of other plant extracts on the oxidative stability of chicken meat: rosemary and sage extracts at 500 mg·kg^–1 (Lopez-Bote et al., 1998), oregano and rosemary essential oils at 150 and 300 mg·kg^–1 (Basmacioglu et al., 2004) or at 100 and 200 mg·kg^–1 (Papageorgiou et al., 2003), or a mixture of marigold, purple coneflower, black currant, and yellow bark at 1,000 mg·kg^–1 (Botsoglou et al., 2004).

Few data are available about possible synergistic effects of natural extracts on the oxidative stability of meat. Basmacioglu et al. (2004) reported a synergistic effect for oregano and rosemary essential oils in broilers at a dose of 300 mg·kg^–1, whereas Haak et al. (2006) did not observe a synergistic action between rosemary and tocopherol in pork. A synergistic action between oregano oil and ATA (200 mg·kg^–1) resulted in a higher oxidative stability than when 200 mg·kg^–1 of ATA alone was fed to turkeys (Papageorgiou et al., 2003).

Comparing the TBARS values from fresh meat and frozen meat patties showed that freezing for 8 mo did not increase the oxidation process. However, the sensitivity to oxidation and thus the level of oxidation during display afterwards is strongly influenced, because overall mean TBARS values increased approximately 10-fold in frozen compared with fresh meat patties. The TBARS values on fresh broiler meat samples from the same treatments similarly increased during display, but the increase was much more marked for the frozen-thawed samples. Because lipid-free radicals are soluble in the lipid fraction and more soluble at lower temperatures, it allows them to diffuse over longer distances and to stimulate the oxidation reaction once the conditions are favorable again (Kanner, 1994).

After 10 d of storage under light, no protein oxidation could be measured. This is in agreement with Mercier et al. (1998), Haak et al. (2006), and Petron et al. (2007), who reported slight differences in protein oxidation during storage of pork, turkey, or lamb, respectively, when measuring the free thiol content. In contrast, for prepared meat products with a longer storage time, such as porcine liver pâté and frankfurters, significant protein oxidation could be observed after 60 d of storage (Estévez and Cava, 2004, 2006).

The -tocopherol content of meat can be enriched by the supplementation of ATA or TC in the feed. The ATA is only effective after hydrolysis in the gut and does not protect the feed from oxidation (Jensen et al., 1998). From the response of muscle -tocopherol levels to dietary ATA or -tocopherol levels, no preference was observed for deposition of -tocopherol from either source. Although the refined linseed oil was not stabilized, there appeared to be no consumption of -tocopherol in the feed to protect it from oxidation to the extent that muscle deposition was affected. More general, there was no sparing effect on -tocopherol by the addition of other antioxidants as indicated by the close relationship between -tocopherol levels in the feed and the breast muscle. In contrast, Goni et al. (2007) observed a linear relationship between the -tocopherol content in the liver of broilers and the concentration of dietary grape pomace, suggesting a sparing effect of grape pomace on vitamin E in the intestine.

In summary, dietary natural antioxidant extracts were less effective than the treatment with synthetic antioxidants combined with ATA for protecting against oxidation, but there were marked differences between different natural antioxidant extracts.

	ACKNOWLEDGMENTS

 
K. Smet is grateful to Ghent University for the PhD grant. The authors would like thank the animal caretakers of the Animal Research Unit and the technical staff of the Laboratory for Animal Nutrition and Animal Product Quality for their assistance.

	FOOTNOTES

 
¹ Present address: Technology and Food Unit, Institute for Agricultural and Fisheries Research, Flemish Government, Brusselsesteenweg 370, 9090 Melle, Belgium.

² Present address: Research Group EnBiChem, Department PIH, University College of West-Flanders, Graaf Karel de Goedelaan 5, 8500 Kortrijk, Belgium.

Received for publication September 14, 2007. Accepted for publication March 28, 2008.

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