Selective deposition of dietary α-Lipoic acid in mitochondrial fraction and its synergistic effect with α-Tocoperhol acetate on broiler meat oxidative stability
© Parveen et al.; licensee BioMed Central Ltd. 2013
Received: 22 February 2013
Accepted: 18 April 2013
Published: 23 April 2013
The use of bioactive antioxidants in feed of broiler to mitigate reactive oxygen species (ROS) in biological systems is one of promising nutritional strategies. The aim of present study was to alleviate ROS production in mitochondrial fraction (MF) of meat by supplemented dietary antioxidant in feed of broiler. For this purpose, mitochondria specific antioxidant: α-lipoic acid (25 mg, 75 mg and 150 mg) with or without combination of α-tocopherol acetate (200 mg) used in normal and palm olein oxidized oil (4%) supplemented feed. One hundred and eighty one day old broiler birds were randomly divided into six treatments and provided the mentioned feed from third week. Feed intake, feed conversion ratio (FCR) remained statistically same in all groups while body weight decreased in supplemented groups accordingly at the end of study. The broiler meat MF antioxidant potential was significantly improved by feeding supplemented feed estimated as 1,1-di phenyl-2-picrylhydrazyl (DPPH) free radical scavenging activity, 2,2-azinobis-(3- ethylbenzothiazoline-6-sulphonic acid) (ABTS+) and thiobarbituric acid reactive substances (TBARS). The maximum antioxidant activity was depicted in group fed on 150 mg/kg α-lipoic acid (ALA) and 200 mg/kg α-tocopherol acetate (ATA) (T4) in both breast and leg MF. Moreover, TBARS were higher in leg as compared to breast MF. Although, oxidized oil containing feed reduced the growth, lipid stability and antioxidant potential of MF whilst these traits were improved by receiving feed containing ALA and ATA. ALA and ATA showed higher deposition in T4 group while least in group received oxidized oil containing feed (T5). Positive correlation exists between DPPH free radical scavenging activity and the ABTS + reducing activity. In conclusion, ALA and ATA supplementation in feed had positive effect on antioxidant status of MF that consequently diminished the oxidative stress in polyunsaturated fatty acid enriched meat.
Keywordsα-Lipoic acid α-Tocopherol acetate Broiler meat Oxidative stability TBARS Antioxidant activity Sub-cellular membrane (mitochondria)
Polyunsaturated fatty acids e.g. linoleic (C18:2n-6) and linoleinic (C18:3n-3) acids are now classified as conditionally essential for human and class mammalian because of deficient enzyme which is responsible to synthesize these acids in plants . However, the other unsaturated fatty acids such as ararchidonic acid (C20:4n-6), eicosapentaenoic acid (C20:5n-3), docosahexaenoic acid (C22:6n-3) that are essential components of cellular membranes synthesized from them are very prone to autoxidation . This leads towards high production of potential precursor of very reactive cytotoxic aldehydes in tissues and foods and become the source of oxidation stress in tissues [3, 4]. These aldehydes can be major contributing factor in several pathological disorders such as atherosclerosis, inflammation, arthritis, ageing, Alzheimer’s and Parkinson’s diseases  The lipids associated with the subcellular organelles are susceptible to oxidation by reactive oxygen species (ROS). These ROS are generated mainly in mitochondria  and other subcellular organelles are also affected like microsomes  Lysosomes  Peroxisomes . Moreover, mitochondria are known to be a rich source for the production of ROS that leads towards lipid peroxidation (6). Previous studies showed defensive mechanism in tissue that can be strengthened by supplementation of feed with vitamin E (in the form of ATA). To reduce or minimized the lipid peroxiation in meat, numerous synthetic and natural antioxidants and antioxidant enriched plant extracts are used in feeds of broiler. One of these antioxidants, α-tocopherol acetate is major lipophilic free radical scavenger in vivo for the protection of membranal lipids [7, 10]. It has been observed that ATA not only deposit linearly in microsomal membrane to stabilize phospholipids, but also improved the FCR, growth performance  whilst TBARS was reduced . α-Lipoic acid is a one of the most active biological antioxidant plays a pivotal role in energy metabolism. It is unique, among antioxidants, owing to its powerful antioxidant properties in both reduced (dihydrolipoic acid) and oxidized (ALA) condition. Dihydrolipoic acid plays an important role in recycling of other radical scavengers such as glutathione, ascorbate and ATA [13–15] protects membrane from oxidation. Exogenous supply of α-lipoic acid appears to impart a variety of significant positive effects in biological system including free radical scavenging potential . It is well documented that feeding ALA lower oxidative damage thus improves mitochondrial stability . Oxidized oil caused a significant reduction in broiler body & carcass weights that undergo rapid oxidative degradation thus had an adverse effect on stability of membranal lipids . Antioxidants i.e. ATA and Butylated hydroxyl anisole/Butylated hydroxyl toluene supplementation improved growth and oxidative stability of meat especially in microsome than mitochondria fraction . Nature has equipped us and all other eukaryotes with different defense mechanism to guard against these adversaries, sometimes the defense is not enough in biological systems. Hence the present studies we intend to examine the antioxidative potential of mitochondria of meat that fortified by mitochondrial-specific bio antioxidant, ALA supplementation in the feed of broiler as model biological system. Thus resultant meat will be considered healthier and nutritive for human consumption.
Material and methods
Reagents, chemicals and materials
ALA and ATA were purchased from Puritan’s Pride, United States of America and Merck (Merck K Ga A, Darmstadt, Germany), respectively. The reagents used for the present study were 1,1-di phenyl-2-picrylhydrazyl (DPPH), 2,2-azinobis-(3- ethylbenzothiazoline-6-sulfonic acid) ABTS+, hydrogen peroxide, ferrous sulphate, trichloroacetic acid, thiobarbituric acid, hydrochloric acid, ascorbic acid, urea, sodium dodecyl sulfate (SDS), pyrogallol, acetonitrile, methanol, ethanol and other reagents were purchased from Sigma-Aldrich Tokyo, Japan. The oxidized oil was prepared from palm olein oil (purchased from a local store) by heating at 180°C for 8.5 h. The composition of the control feed was 39 g of corn, 6.0 g of wheat, 2.07 g of broken rice, 5.60 g of polished rice, 2.20 g of cottonseed meal, 2.0 g of canola meal, 2.30 g of corn gluten 60%, 12.40 g of sunflower meal, 15.0 g of soybean meal, 6.60 g of fish meal, 3.0 g of soya oil, 0.15 g of L-lysine, 0.08 g of DL-methionine, 1.20 g of dicalcium phosphate, 0.90 g of limestone, 0.50 g of premix, and 4.0 g of molasses (total 100 g). The metabolized energy feed was 2900 kcal/kg, crude protein (21.03%), and fiber (6.50%). After acclimation, the experimental birds were fed for 21 days with the standard diet-containing placebo (Group 1, control).
Treatments plan of feed supplemented with α-lipoic acid and α-tocopherol acetate
Description of feed
α-Lipoic acid (25 mg) + α-tocopherol acetate (200 mg)/ Kg of feed
α-Lipoic acid (75 mg) + α-tocopherol acetate (200 mg)/ Kg of feed
α-Lipoic acid (150 mg) + α-tocopherol acetate (200 mg)/ Kg of feed
Oxidized oil (4%)/ Kg of feed
Oxidized oil (4%) + α-Lipoic acid (150 mg) + α-tocopherol acetate (200 mg)/ Kg of feed
Isolation of mitochondrial fractions of meat
Mitochondrial fraction of meat was isolated by following the method of  and briefly described herein.
Breast and leg meat sample (6 ± 0.01 g) was homogenized by using 20 mL of 0.1 M phosphate buffer containing ethylene diamine tetra acetic acid (EDTA) at 7.4 pH in 50 mL polypropylene tube for 10 min at 4000 g in ice containing backer, 15 sec rest was given after 60 sec. Connective tissues were removed from meat homogenate through filtration by using muslin cloth.
The filtrate was centrifuged at 1,000 × g for ten min at 4°C to remove the nuclear fraction from meat filter homogenate. Supernatant (40 mL) was separated and centrifuged to sediment mitochondria at 10,000 × g. Mitochondria was collected and stored at −80°C for further analysis. Mitochondrial fraction was subjected to estimate the protein content by follow the Lowry method  for equalization of mitochondrial fraction (MF) sample on the basis of protein content of breast and leg meat. Stock solution of standard was prepared 1 mg/ml of bovine albumin serum for protein quantification.
Antioxidant potential of mitochondrial fraction of breast and leg meat
Antioxidant potential of the mitochondrial fraction of breast and leg meat was measured by DPPH free radical scavenging activity, ABTS + reducing activity and TBARS methods.
DPPH free radical scavenging activity
ABTS + reducing activity
Lipid peroxidation stability determine by thiobarbituric acid reactive substances (TBARS)
Quantification of α-tocopherol acetate from mitochondrial fraction of breast and leg meat by HPLC isocratic system
Alpha-tocopherol acetate was estimated by HPLC according to method described by  with slightly modifications. Mitochondrial sample (500 mg) was mixed with 5% ascorbic acid (0.5 mL) prepared in nitrogen saturated water followed by 6 M urea (1 mL). Solution was flushed with nitrogen gas and vortexed for 1–2 min to dissolve the sample. One mL of 0.1 M sodium dodecyl sulphate (SDS) solution was added and vortex again followed by the addition of 4 mL ethanol (95%) contain 1% pyrogallol. Sample was vortexed for 30 sec for de-proteination and freeing of ATA from membrane of the cell. After that, petroleum ether (8–10 mL) was added and vortexed for 2 min followed by centrifuged at 5000 × g for 4–5 min. Transferred upper solvent layer to a vial or glass and evaporated under nitrogen stream. The pooled solvent layer was added 200 to 500 μl ethyl alcohol flush to facilitate the solubilization of ATA. Samples were filter through microfilter (anspec 0.45 μm) and stored in the dark until further analysis. After the addition of 500 μL methanol, the solution was heated for 1 min at 45°C to dissolve the ATA. The solution was centrifuged at 2,000 × g for 5 min and then the liquid layer was filtered. The filtrate was analyzed for ATA using a Shimadzu HPLC (Kyoto, Japan) equipped with 8 cm × 4.6 mm × 5 μm Shim-Pack CLC (C18) column (Shinwa Chemicals, Kyoto, Japan) at 290 wavelength UV-detectors and one mL flow rate was used and sample (20 μl) was injected. Mobile phase was methanol (100%) used to quantify ATA by using a UV-isocratic chromatographic system.
Quantification of α-lipoic acid from mitochondrial fraction of breast and leg meat by HPLC gradient system
α-Lipoic acid content was measured from mitochondrial fraction of breast and leg meat by HPLC gradient system  with slightly modifications. On protein basis, mitochondrial sample were taken for each treatment in the glass tubes and mixed with 3 mL hexane containing 250 μL isopropanol and vortexed for 30 min. Sample was centrifuged at 1500 × g and upper hexane layer was collected in glass tube. This step was repeated twice and pooled the resultant n-hexane layer. For derivatization of ALA, 0.2 mL (1 mg protein/mL) sample was mixed with methanolic sulphric acid (2 mL) and shaken well. The resultant adduct was heat at 80°C for one hour in water bath and vortexed 15 min. Two milliliter of distilled water added to stop the reaction and ALA was separated by petroleum ether (1 mL) thrice and then evaporated the ether content under nitrogen stream and stored. α-Lipoic acid was estimated by injecting 20 μL sample in Shimadzu HPLC (Kyoto, Japan) equipped with a 15 cm × 4.6 mm × 5 μm Shim-Pack CLC (C18) column (Shinwa Chemicals, Kyoto, Japan). The fluorescence detector was operated at excitation and emission wave lengths of 343 and 423 nm, respectively. The mixture of acetonitrile/water (80:20 v/v) used as a mobile phase with flow rate 1.0 mL/min.
Data obtained from various parameters were subjected to one way analysis of variance (ANOVA). Mean and standard deviation of the mean was measured by Statistic 8.1 Program (Analytical Software). Difference among the treatments were calculated by the least-squared difference with a significance level (p < 0.05).
The animals were slaughtered according to the Halal ethical guidelines and the approval is given by the head of the National Institute of Food Science and Technology, University of Agriculture, Faisalabad, Pakistan.
Results and discussion
Feed consumption (kg) and Feed Conversion ratio (FCR) of broilers used in the study
Feed consumption (kg)
6.17 ± 0.30
1.98 ± 0.099
5.98 ± 0.27
1.83 ± 0.098
6.08 ± 0.32
1.97 ± 0.101
6.19 ± 0.37
2.01 ± 0.095
5.98 ± 0.29
1.93 ± 0.094
6.19 ± 0.34
1.93 ± 0.096
Antioxidant potential of mitochondrial fraction of leg and breast broiler meat
DPPH free radical scavenging activity and ABTS + reducing activity of mitochondrial fraction of broiler meat
DPPH free radical scavenging activity (%)
ABTS + reducing activity (%)
67.01 ± 3.56b
66.79 ± 3.15b
29.12 ± 1.41c
30.65 ± 1.39d
68.18 ± 3.98b
67.01 ± 3.37b
32.27 ± 1.56b
31.89 ± 1.50c
70.09 ± 4.01ab
69.81 ± 3.77ab
33.98 ± 1.63b
34.04 ± 1.56b
73.51 ± 4.25a
72.99 ± 4.03a
36.01 ± 1.66a
37.56 ± 1.69a
61.98 ± 3.79d
61.81 ± 3.65d
27.91 ± 1.39d
28.18 ± 1.23e
64.01 ± 3.67 c
64.10 ± 3.36c
29.98 ± 1.33c
30.05 ± 1.37d
α-Lipoic acid contents and α-Tocopherol acetate in breast and leg mitochondrial fraction of broiler meat
Alpha-lipoic acid content
Alpha-tocopherol acetate content
13.69 ± 0.66d
14.56 ± 0.69d
11.01 ± 0.62d
12.31 ± 0.67d
15.99 ± 0.69d
17.23 ± 0.77c
14.98 ± 0.68c
16.42 ± 0.78c
21.31 ± 0.75b
22.01 ± 0.81b
20.86 ± 0.72b
22.67 ± 0.86b
27.41 ± 1.13 a
30.06 ± 1.25a
26.04 ± 1.09a
28.95 ± 1.27a
10.88 ± 0.53e
11.54 ± 0.60e
9.87 ± 0.54d
10.75 ± 0.56d
17.59 ± 0.76 c
18.34 ± 0.79c
15.93 ± 0.69c
17.54 ± 0.78c
Lipid peroxidation stability of mitochondrial fraction measured by TBARS
α-Tocopherol acetate (ATA) and α-lipoic acid (ALA) contents in leg and breast mitochondrial fraction of broiler meat
Earlier, it is well documented that antioxidant are more absorbed in microsomes as compared to mitochondrial fraction of meat . The present study is conducted to evaluate the effect of mitochondrial-specific antioxidant i.e. α-lipoic acid on mitochondria stability that is very prone to auto-oxidation due to higher accumulation of polyunsaturated fatty acids in its membranes. ATA content increased as the level of ALA increased in the feed of broilers which is evident from Table 4. ATA contents present in the control which showed that it is also naturally present in the meat tissues. The result showed that maximum ALA deposited in T4 and of mitochondrial membrane of breast and leg meat, respectively (Table 4). Control and oxidized treatments also deposited α-lipoic acid but the amount is significant less. Likewise, the accumulation trend of ALA was same as in breast mitochondria meat. It also deposits in control and oxidized oil treatment but deposition rate was progressively elevated in groups that were fed with higher level of ALA. It is suggested from present study results that mitochondrial-specific antioxidants can deposit in mitochondria of the cell and minimized the rate of lipid oxidation and ultimately enhance the quality of meat and meat products. α-Tocopherol acetate concentration was higher in T4 followed by T3, T2 as compared to control. Similarly, ATA contents were higher in T4 of both leg and breast mitochondrial fraction supplemented with ALA (200 mg/kg feed) with constant level of ATA. Gradually the ALA concentration increases, the ATA deposition also increases which is evident from Table 4[13, 33]. reported that ALA has synergistic effect with α-tocopherol acetate. But in the leg mitochondria the deposition was higher as compared to breast. Synergistic effect of α-lipoic acid and α-tocopherol acetate was also higher in all supplemented feed treatments of broiler. These results also indicate that two antioxidants have positive effect on the tissues especially mitochondria of meat. Oxidized oil in the feed of broiler was inhibited the deposition of ATA and ALA in meat mitochondrial fraction of meat. In the treatments T2, T3 and T4 the deposition rate of ALA were in increasing pattern as the progressively increased the ALA in the feed (Table 4). Similar trend was observed in the microsomes fractions of the breast and leg meat that were published in elsewhere . The ATA is a biological antioxidant which protects the membranes from oxidation. The supplementation of ATA in feed of animal increase its deposition as in tissues [25, 29] reported that free radical production and lipid per-oxidation were significantly decreased/ minimized in muscle as well as has protective effect on lipid peroxidation in mitochondrial fraction animal fed on ATA supplemented diet [34, 35]. Moreover, results of ALA obtained in the present study, which are consistent with a previous report, suggest that the ALA has a positive influence on the ATA deposition in meat cell membranes because both synergistically quench ROS, subsequently inhibit oxidative damage in biological systems .
The ALA and ATA significantly enhanced the antioxidant potential of mitochondrial fraction of broiler meat. It was concluded from the present research that supplementation of ALA with ATA improved the lipid stability and mitigate the ROS in mitochondria of the meat tissues thus meat quality of broiler meat is improved. Further, studies are designed to evaluate the storage stability of antioxidants enriched meat, that will consequently helpful for meat industry as well as consumers.
Authors are highly thankful to Higher Education Commission, Government of Pakistan for the financial assistance of a project entitled “Selective deposition of bio-antioxidants in skeletal muscles of meat animals by dietary supplementation in feed to enhance the quality of meat and meat products”.
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