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Poult Sci 2006. 85:1829-1837
© 2006 Poultry Science Association
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PROCESSING, PRODUCTS, AND FOOD SAFETY

Dietary Functional Ingredients: Performance of Animals and Quality and Storage Stability of Irradiated Raw Turkey Breast

H. J. Yan, E. J. Lee, K. C. Nam, B. R. Min and D. U. Ahn1

Department of Animal Science, Iowa State University, Ames 50011

1 Corresponding author: duahn{at}iastate.edu


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
The objective of this study was to evaluate the effect of dietary functional ingredients vitamin E (VE), Se, and conjugated linoleic acid (CLA), alone or in combination, on the quality of irradiated turkey breast meat. A total of 480 male turkeys (11-wk-old, raised on a cornsoybean basal diet) were randomly allotted to 32 pens and fed 1 of 8 experimental diets (4 pens/treatment) supplemented with none (control), 200 IU/kg of VE (VE), 0.3 ppm Se (Se), 2.5% CLA (CLA), 200 IU/kg of VE + 0.3 ppm Se (VE + Se), 200 IU/kg of VE + 2.5% CLA (VE + CLA), 2.5% CLA + 0.3 ppm Se (CLA + Se), 200 IU/kg of VE + 0.3 ppm Se + 2.5% CLA (VE + Se + CLA) for 4 wk. At 15 wk of age, all birds were slaughtered, and breast muscles of 8 birds from each pen were separated, pooled, and ground. Patties were prepared using the ground meat, aerobically packaged, and irradiated at 0 or 1.5 kGy absorbed dose. Lipid oxidation, color, and volatiles of the patties were measured after 0, 7, and 12 d of storage at 4°C. The content of VE and Se and fatty acid composition of lipids were also determined. Dietary supplementation of VE and CLA increased their concentrations in turkey breast. Dietary CLA decreased monounsaturated and non-CLA polyunsaturated fatty acids content in meat. Irradiation increased (P < 0.05) Hunter color redness value of turkey breast and accelerated lipid oxidation, regardless of dietary treatments. However, dietary VE, Se, and CLA, alone and in combinations, decreased (P < 0.05) lipid oxidation in meat caused by both irradiation and storage. It was concluded that dietary supplementation of VE, Se, and CLA, alone and in combination, improved the storage stability of irradiated turkey breast meat.

Key Words: dietary functional ingredient • irradiation • turkey breast • color • lipid oxidation


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
Irradiation, up to 3 kGy, is permitted for use in poultry meat to control pathogenic microorganisms such as Salmonella, Escherichia coli, and Listeria. A major concern of irradiating poultry meat, however, is its negative effects on meat quality, such as generation of pink color, irradiation off-odor, and acceleration of lipid oxidation (Ahn et al., 1998). Functional ingredients are defined as the components in food or animal feed that can prevent or treat certain disorders and diseases in addition to their nutritional values (Jiménez-Colmenero et al., 2001). There are 2 advantages of using functional ingredients in animal feed: They can directly improve the health of farm animals and the quality of animal-derived foods and indirectly promote human health by providing foods containing functional ingredients. The production of value-added, safe, and healthful meat products, thus, is the primary objective of adding functional ingredients in animal feed.

The role of vitamin E (VE) as a protective antioxidant is well documented, and supranutritional levels of dietary VE have been found to improve the quality of poultry products by reducing the rates of both lipid and heme oxidations (Ahn et al., 1997; Nam et al., 2003b). As a unique mineral, Se has a number of important biological functions that are closely related to the activities of Se-containing proteins. The first identified functional selenoprotein was glutathione peroxidase, which is the major cellular antioxidant defense system in animals (Stadtman, 2002). The function of these enzymes is maintaining low levels of H2O2 within cells, thus decreasing potential free-radical damage. They also provide a second line of defense against hydroperoxides that can damage membranes and other cell structures (Rotruck et al., 1973). In addition, Se and VE have significant interactions: The antioxidant properties of Se and VE differ but are complementary. Within cell membranes, VE scavenges free radicals before they initiate lipid peroxidation. On the other hand, glutathione peroxidase reduces preformed hydroperoxides to alcohols. Thus, VE and Se can work together to prevent cellular and tissue damages caused by oxidation (Combs and Regenstein, 1980).

Supplementation of conjugated linoleic acid (CLA) in bird feed is primarily based on their biological functions and consumers’ preference of value-added and healthful foods. Conjugated linoleic acids can be incorporated into bird tissues via dietary supplementation (Du et al., 2001; Huang et al., 2001; Thiel-Cooper et al., 2001) and can alter the quality of meat. Du et al. (2000) reported that dietary CLA increased total saturated fatty acids and decreased total monounsaturated fatty acids (MUFA) and polyunsaturated fatty acids (PUFA) in breast fillets, which enhanced storage stability of turkey products (Du et al., 2002).

Oxidation of unsaturated fatty acids in biomembranes leads to the disruption of normal membrane structure and functions, in addition to cell injury in living systems, and is a major cause of quality deterioration in muscle foods. Asghar et al. (1990) reported that the rate of NADPH-induced peroxidation in microsomes and mitochondria depended primarily upon fatty acid composition of membrane lipids rather than tocopherol content. If antioxidants such as VE and Se are combined with CLA, they can modify fatty acid composition of cell membranes and improve the antioxidant potential of meat, which may reduce lipid oxidation and abnormal color changes and off-odor production caused by irradiation and storage.

The purposes of this study were to investigate the influence of 3 dietary functional ingredients, VE, Se, and CLA on the performance of finishing turkeys and the quality of irradiated turkey breast meat.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 REFERENCES
 
Dietary Treatments
A 23 factorial design was utilized for the bird experiment. The 3 factors involved were 3 functional ingredients: VE, Se, and CLA at 2 levels each. The 8 dietary treatments included control, 200 IU/kg of DL-{alpha}-tocopherol acetate (VE), 0.3 mg/kg of Se (Se), 2.5% CLA (CLA), 200 IU/kg of DL-{alpha}-tocopherol acetate and 0.3 mg/kg of Se (VE+Se), 200 IU/kg DL-{alpha}-tocopherol acetate + 2.5% CLA (VE + CLA), 2.5% CLA + 0.3 mg/kg of Se (CLA + Se), 200 IU/kg of DL-{alpha}-tocopherol acetate + 2.5% CLA + 0.3 mg/kg of Se (VE + CLA + Se). Each treatment included 4 replications.

The bird experiments were performed in the Poultry Research Center of Iowa State University. A total of 480 0-wk-old male Large White turkeys were randomly assigned to 32 pens and raised on a corn–soybean-based diet (Table 1Go) for 11 wk. At the beginning of wk 12, 4 pens of turkeys were randomly assigned to 1 of the 8 dietary treatments (Table 2Go) and fed until 15 wk of age. Feed consumption, amount of live birds, and bird weight were recorded; weight gain, feed conversion rate (FCR), and mortality were calculated.


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  		Table 1. Corn–soybean-based diets fed to male turkeys from 0 to 12 wk
 

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  		Table 2. Corn–soybean-based diets fed to male turkeys from 12 to 15 wk
 
Sample Preparation
At the end of the feeding trial, all birds were slaughtered and inspected following the USDA guidelines (USDA, 1982). Carcasses of birds from the same pen were pooled and chilled in ice water for 3 h and then drained in a cooler (0°C) until the internal temperature was 4°C for further processing. Breast muscles were deboned, and skin and visible fat were removed. All breast samples of birds from the same pen (4 pens per treatment) were pooled, ground twice through a 3-mm plate, and treated as a replication. Four replications of patties were prepared for the meat quality, fatty acid composition of meat, and concentrations of dietary functional ingredients used in this study.

Meat patties (about 100 g, 5 cm in diameter, 0.5 cm in thickness) prepared from each replication were packaged in O-permeable bags (polyethylene, Associated Bag Co., Milwaukee, WI). Packaged samples were irradiated using a linear accelerator (Circe IIIR, Thomson CSF Linac, Saint-Aubin, France) at room temperature to an average dose of 0 or 1.5 kGy. Ten million electron volts of energy, 10 kW of power, and 88.1 kGy/min of average dose rate were used. To confirm the target dose, alanine dosimeters were attached to the top and bottom of samples and were read using a 104 electron paramagnetic resonance unit (EMS-104, Bruker Instruments Inc., Billerica, MA). The maximum:minimum ratio was approximately 1.3. Both irradiated and nonirradiated raw meat patties were kept at 4°C; color and lipid oxidation were measured after 0, 7, and 12 d; and volatiles were measured after 0 and 7 d of storage. Concentrations of VE, Se, and fatty acid composition were determined before and after irradiation.

Meat Quality Analyses
Vitamin E content in breast patties was analyzed using the gas chromatography method of Du and Ahn (2002b). {alpha}-Tocopherol concentration was quantified using 5{alpha}-cholestane as an internal standard and expressed as micrograms/kilogram of muscle. Selenium in breast meat was analyzed according to the fluorometric method of AOAC International (1995). Gas chromatography (HP6890, Hewlett-Packard Co., Wilmington, DE) was used to determine fatty acid composition. Fatty acids were identified by comparing the retention times to standards and were expressed as peak area percentage of total fatty acids (Du and Ahn, 2002b).

A Labscan color meter (Hunter Associates Laboratory Inc., Reston, VA) was used to measure color of raw meat patties. Each patty sample in transparent packages was put directly under the light source. Light source was illuminant D 10°, port size was 1 cm, and viewing area was 0.63 cm. Hunter lightness, redness, and yellowness were read 3 times from 3 different areas around the center of each patty sample and were averaged as the measurement of this sample. Lipid oxidation was determined by measuring 2-TBA reactive substances (TBARS) content, as described by Nam et al. (2003a). Volatiles were determined using a dynamic headspace-gas chromatography mass spectrometry method (Nam and Ahn, 2003).

Raw turkey aroma and irradiation off-aroma of both irradiated and nonirradiated samples from birds fed different diets were assessed by 8 trained panelists. Panelists were recruited from faculty, staff, and students, and a 1-h training session was performed before actual samples were presented to panelists. Panelists assessed the differences in aroma characteristics between irradiated and nonirradiated meat and made comments as to the description of sensory terms. Testing was conducted in partitioned booths and under red fluorescent lights. A line scale (numerical value of 15 units) was used with descriptive anchors (none and high) at each end of the line. Data were collected by using a computerized sensory scoring system (Compusense 5, Version 4.4, Compusense Inc., Guelph, Ontario, Canada).

Statistical Analysis
Analyses of variance were conducted using the GLM procedure appropriate for complete randomized block designs (SAS Institute, 1995). Statements of probability are based upon P ≤ 0.05. When significant differences among or between treatment means were found, means were compared using Tukey’s multiple tests mean value, and SEM were reported. Data for each treatment were combined and analyzed using the multivariate (YX) PRINCOP program of SAS 8.2 (SAS Institute, 1995) to determine principal components and correlations.


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
REFERENCES
 
Dietary VE, Se, and CLA on Turkey Performance
Conjugated linoleic acid supplementation (treatment CLA, VE + CLA, Se + CLA, VE + Se + CLA) lowered feed consumption in general, but the decrease was significant only for SE + CLA and VE + SE + CLA treatments (Table 3Go). Results from other studies on CLA supplementation were mixed: Eggert et al. (2001) showed that dietary CLA increased average daily gain of growing pigs, whereas Cook et al. (1998) observed a decrease of average daily gain. Wiegand et al. (2002) reported no effect of dietary CLA on weight gain. Du and Ahn (2002a) found no difference in the live weight of chickens after feeding 1% CLA for 3 wk. However, when dietary CLA levels for chickens were increased to >2% and fed to 5 wk, feed consumption, BW, and daily gain tended to decrease as dietary CLA level increased. Results from the current study agreed with those of Du and Ahn (2002a), confirming that a higher level of CLA decreased live weight as a result of reduced feed consumption (Table 3Go). Park et al. (1999) reported that the effect of CLA on animal growth and feed efficiency was dependent on isomers: cis-9, trans11 CLA isomer was active in enhancing BW gain and appeared also to enhance feed efficiency in weanling mice, but they had no effect on body fat change. However, trans10, cis-12 CLA isomers reduced body fat levels relative to control but did not enhance either body growth or feed efficiency. So the overall effects of CLA on growth, feed efficiency, and body level appeared to be due to the different biological activities of the 2 isomers.


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  		Table 3. Effect of dietary functional ingredients on weight gain, feed consumption, and feed conversion rate (FCR) of male turkeys during the 12- to 15-wk feeding period
 
Decrease in weight gain by CLA was reduced when CLA was combined with VE (VE + CLA) or both VE and Se (VE + Se + CLA; P < 0.05). When CLA was fed along with VE, or VE + Se, the birds had a better growth rate than CLA alone and control, even though feed consumption was not increased. As a result, feed efficiency of treatments VE + CLA and VE + Se + CLA decreased (P < 0.05) as compared with control and CLA alone.

Increasing dietary concentration of VE from 48 to 178 IU/kg resulted in improved performance and economic returns from flocks inflicted with subclinical infectious diseases (McIlroy et al., 1993). Guo et al. (2001) reported that addition of VE at 100 mg/kg significantly (P < 0.05) improved the growth and FCR of broilers fed the control diet during 0 to 3 wk of age. In this study, 200 IU/kg of added VE showed no influence on performance (total weight gain, feed consumption, and feed efficiency) of birds, but the reduced weight gain caused by dietary CLA was improved by VE. Selenium was required for maximum poultry performance (Scott et al., 1965). With Se supplementation (0.3 mg/kg), however, there was no significant performance improvement except that FCR was decreased when Se was supplemented along with VE (Table 3Go).

Meat Composition
Supplementation of tocopherol acetate in turkey diets singly or in combination with other functional ingredients (Se and CLA) increased VE levels in breast muscles (Table 4Go). The levels of VE in breast meat increased by more than 4-fold over the control and the treatments without VE. When VE was combined with Se (treatments VE + Se and VE + Se + CLA), muscle accumulations of VE were higher than that of single supplementation; when VE was combined with CLA, the average accumulation was lower but was not statistically significant (P > 0.05). Dietary Se increased the tissue accumulations of Se, but VE or CLA had no effect on its concentration (Table 4Go).


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  		Table 4. Concentration of vitamin E (VE) and Se in turkey breast with different diets
 
Dietary CLA changed the composition of other fatty acids, both total MUFA and total non-CLA PUFA were decreased (P < 0.05; Table 5Go). Among PUFA, all n3 fatty acids, including C20:5 n3 and C22:6 n3, were increased. Two long-chain n6 fatty acids (C20:4 n6 and C22:5 n6) were decreased, but no consistent change in arachidonic acid (C22:4 n6) was observed. There were no differences in total saturated fatty acid between CLA-supplemented groups and other groups, except a decrease in saturated fatty acids, such as C14:0, C18:0, and C22:0 by CLA. Du et al. (2000) reported similar changes in fatty acid composition by dietary CLA. The decreases in C18:1 n9, C18:1 n7, and C20:1 n9 and increases in C14:0 and C18:0 were very likely due to the inhibition of stearoyl-CoA desaturase, a key enzyme involved in the synthesis of MUFA by CLA (Lee et al., 1998), activity. The decreases of long-chain n6 PUFA could be caused by the competitive inhibition of {Delta}6-desaturase by CLA (Liu and Belury, 1998). {Delta}6-Desaturase is required for long-chain PUFA synthesis from either linoleic acid (n6 precursor) or {alpha}-linolenic acids (n3 precursor). If {Delta}6-desaturase was inhibited by CLA, n3 long-chain fatty acids would also be decreased. But results from this study, as well as others, showed that n3 fatty acids were increased. So not only is inhibition of {Delta}6-desaturase involved in CLA modulated fatty acids metabolism, but also other mechanisms that cause eicosapentaenoic acid and docosahexaenoic acid accumulations are involved. These fatty acid composition changes are also important to improve storage stability of meat by minimizing lipid oxidation.


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  		Table 5. Fatty acid composition of turkey breast as affected by dietary vitamin E (VE), Se, and conjugated linoleic acid (CLA)
 
Lipid Oxidation
The TBARS values of raw meat increased by storage in both irradiated and nonirradiated raw meat, but not all of the increases were significant. Irradiated meat produced greater amounts of TBARS than nonirradiated ones, and the TBARS increase over storage was also greater in irradiated than nonirradiated meat. In nonirradiated meat, treatments containing VE (VE, VE + Se, VE + CLA, and VE + Se + CLA) prevented oxidative changes during storage. In irradiated meat, combinations of VE with Se, CLA, or both (VE + Se, VE + CLA, and VE + Se + CLA) also minimized oxidative changes during the 12-d storage (Table 6Go). Dietary functional ingredients, singly or in combination, improved storage stability of both irradiated and nonirradiated meat after storage, but some of them (Se, CLA, and Se + CLA for nonirradiated meat) were not significant.


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  		Table 6. Effect of functional ingredients on lipid oxidation of aerobically packaged raw turkey breast
 
Ahn et al. (1997) reported that dietary VE at >200 IU/ kg decreased lipid oxidation and total volatiles of raw turkey patties after 7 d of storage. Nam et al. (2003b) indicated that dietary VE at 100 IU/kg significantly improved the storage stability of turkey breast, which was more distinct in irradiated than nonirradiated meats. Du et al. (2000) observed decreased lipid oxidation by dietary CLA in chicken meat during storage and attributed it to the reduced PUFA in the meat. Supplementation of feed with Se was found to decrease lipid oxidation in chicken meat (Combs and Regenstein, 1980). However, our results indicated that only dietary VE provided significant antioxidant property to raw meat. However, combinations of VE and Se; VE and CLA; and VE, Se, and CLA provided better protection from lipid oxidation than their single supplementations.

Meat Color
Regardless of dietary treatments, irradiation improved Hunter color redness value of raw meat, and the color changes remained over the 12-d storage period (Table 7Go). Dietary supplementation of functional ingredients also had some effects on the redness value of meat, but their effects were marginal compared with irradiation. However, Nam et al. (2003b) reported that dietary VE at >100 IU/kg was effective in stabilizing turkey breast meat color with aerobic packaging. Dietary CLA in general reduced (P < 0.05) both lightness value and redness value of nonirradiated raw meat, but the changes were significant only in stored meats.


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  		Table 7. CIE color values of raw turkey breast patties during storage
 
Volatile Profiles
Compared with nonirradiated meat, irradiation of raw turkey breast created new S-containing compounds such as dimethyl disulfide. The amount of S compounds from control, VE, and Se diets increased after 7 d of storage (Table 8Go). No S compounds were detected in treatments VE + Se, VE + CLA, and VE + Se + CLA after 7 d of storage, and the levels in treatments CLA and Se + CLA were lower than that at d 0. Ahn et al. (2000) reported that S-containing volatile compounds that were responsible for irradiated meat off-odor were highly volatile and easily evaporated under aerobic conditions.


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  		Table 8. Volatiles of raw turkey breast patties as affected by different diet treatments, irradiation, and storage time.
 
Irradiation also increased the amounts of total hydrocarbons, aldehydes, alcohols, and ketones (P < 0.05; Table 8Go). Dietary supplementation of VE, VE + Se, VE + CLA, and VE + Se + CLA reduced (P < 0.05) the production of hydrocarbons and aldehydes at d 0 and 7 (except for dietary VE at d 0). However, there was no significant pattern in the changes of alcohols and ketones by dietary treatments. Hydrocarbons, aldehydes, alcohols, and ketones are volatiles that are derived from lipids. Autooxidation of unsaturated fatty acids is not only responsible for rancid off-flavors during storage, known as "warmed-over flavor," but for characteristic meat flavor due to complex volatile compounds produced by lipid oxidation (Mottram and Edwards, 1983). Shahidi and Pegg (1994) indicated that some aldehydes, like hexanal and pentanal, were good indicators of lipid oxidation. Our study showed that aldehydes and hydrocarbons were generally increased by storage and irradiation.

Sensory Evaluation
Irradiation significantly (P < 0.05) reduced raw turkey aroma and increased irradiation off-aroma of turkey breast meat (Table 9Go). Dietary VE and VE + Se significantly reduced raw turkey aroma in nonirradiated meat, but all dietary functional ingredients reduced raw turkey aroma in irradiated meat. Sensory panels easily detected irradiation off-aroma, but dietary VE + Se and VE + Se + CLA treatments significantly lowered irradiation off-aroma in irradiated meat. Nonirradiated meat had little irradiation off-aroma. During training sessions, sensory panels described irradiation off-aroma of irradiated raw meat as "sulfury," "vegetable," "hospital-like," or "wet-dog," which was different from that of nonirradiated meat. When the scores for irradiation off-aroma were high, the scores for turkey aroma were low (Table 9Go).


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  		Table 9. Sensory scores of breast meats from turkeys supplemented with different dietary functional ingredients
 
Principal Component Analysis
The purposes of principal component analysis are as follows:1) to derive a small number of independent linear combinations (principal components) that retain as much of the information in the original variables as possible, and 2) to explore polynomial relationship. Thus, principal component analysis, a multidimensional modeling method, provides an interpretable overview of the key information through the loading plot. In the loading plot, components (so-called principal components) that are close together are positively correlated, whereas those lying opposite to each other tend to have negative correlation (Næs et al., 1996).

Principal component analysis of volatiles showed that 94% (2 principal components: Pc1, 38% and Pc2, 56%) of the total variability was derived from irradiation and storage. The variation of Pc1 was mainly generated by total hydrocarbons, total aldehydes, pentane, hexanal, 1-octen-3-ol, and nonanal. Hydrocarbons and aldehydes weighed heavier than other compounds. The variation of Pc2 was mainly attributed to dimethyl disulfide, and S-containing compounds contrasted to other compounds (Table 10Go).


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  		Table 10. The variation sources of the first 2 principal components (PC) for volatile analysis
 
Table 11Go shows the correlation coefficients by principal component analysis procedure among lipid oxidation, 2 sensory attributes (raw turkey aroma and irradiation off-aroma), volatile components, and concentrations of VE, Se, and CLA. Several significant correlations between the chemical and sensory parameters of turkey patties with different treatments were detected. Lipid oxidation (TBARS) was positively correlated (P < 0.05) with total hydrocarbons, total aldehydes, total alcohols, pentane, 2-butanone, octane, hexanal, 1-hexen-3-ol, 1-hexanol, 1-octen-3-ol, and nonenal and was negatively correlated (P < 0.05) with total ketones and 2-propanone. Turkey meat aroma was negatively correlated (P < 0.05) with irradiation aroma, total hydrocarbons, total S compounds, pentane, ethanol, 2-propanol, 2-butanone, and dimethyl disulfide. Irradiation off-aroma was positively correlated with dimethyl disulfide as well as total hydrocarbons, total aldehydes, total S compounds, pentane, ethanol, 2-butanone, and hexanal (Table 11Go).


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  		Table 11. Correlation coefficients among lipid oxidation, sensory attributes, volatile profiles, and concentrations of vitamin E (VE), Se, and conjugated linoleic acid (CLA)
 
Vitamin E had negative relations (P < 0.05) with lipid oxidation and production of total hydrocarbons, total aldehydes, total alcohols, and total ketones. The individual representative compounds were pentane, hexanal, 1-octen-3-ol, and nonanal. 2-Propanone and 2-propanol were positively related to VE concentration. Both Se and CLA had negative correlations (P < 0.05) with the production of S-containing compounds.

In conclusion, dietary functional ingredients (VE, Se, and CLA) improved the feed efficiency of turkeys during the finishing period. Lipid oxidation and off-odor of turkey breast meat caused by storage and ionizing irradiation were reduced by dietary functional ingredients, especially when VE was combined with Se or with both Se and CLA.


   ACKNOWLEDGMENTS
 
This work was supported by the National Integrated Food Safety Initiative (USDA grant 2002-5110-01957), Washington, DC.

Received for publication December 21, 2005. Accepted for publication June 17, 2006.


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 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
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