British Poultry Science

ISSN: 0007-1668 (Print) 1466-1799 (Online) Journal homepage: http://www.tandfonline.com/loi/cbps20

Effects of alpha-lipoic acid supplementation in different stages on growth performance, antioxidant capacity and meat quality in broiler chickens Z.Y. Guo, J.L. Li, L. Zhang, Y. Jiang, F. Gao & G.H. Zhou To cite this article: Z.Y. Guo, J.L. Li, L. Zhang, Y. Jiang, F. Gao & G.H. Zhou (2014) Effects of alpha-lipoic acid supplementation in different stages on growth performance, antioxidant capacity and meat quality in broiler chickens, British Poultry Science, 55:5, 635-643, DOI: 10.1080/00071668.2014.958057 To link to this article: http://dx.doi.org/10.1080/00071668.2014.958057

Accepted author version posted online: 27 Aug 2014. Published online: 03 Oct 2014. Submit your article to this journal

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Date: 09 October 2017, At: 09:56

British Poultry Science, 2014 Vol. 55, No. 5, 635–643, http://dx.doi.org/10.1080/00071668.2014.958057

Effects of alpha-lipoic acid supplementation in different stages on growth performance, antioxidant capacity and meat quality in broiler chickens Z.Y. GUO, J.L. LI, L. ZHANG, Y. JIANG1, F. GAO,

AND

G.H. ZHOU

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College of Animal Science and Technology, Key Laboratory of Animal Origin Food Production and Safety Guarantee, Synergetic Innovation Centre of Food Safety and Nutrition, Nanjing Agricultural University, Nanjing 210095, China and 1 Ginling College, Nanjing Normal University, Nanjing 210097, China

Abstract 1. This experiment was conducted to investigate the effect of basal dietary supplementation with 500 mg/kg alpha-lipoic acid (LA) on growth performance, antioxidant capacity and meat quality in different stages in broiler chickens. 2. A total of 240 Arbor Acre chickens were randomly assigned into 4 treatment groups, each treatment containing 6 replicates of 10 chickens each. Group 1 was the control group without LA supplementation; Group 2 was supplied with LA in the starter period; Group 3 was supplied with LA in the grower period; and Group 4 was supplied with LA in the whole period. 3. The results showed that LA supplementation improved average feed intake and body weight gain in all three experimental groups, especially in Group 2. LA supplementation significantly decreased abdominal fat yield in Groups 3 and 4. 4. LA supplementation all improved hepatic total antioxidant capacity, the level of glutathione, the activities of total superoxide dismutase, catalase (CAT) and glutathione peroxidase, in particular in Group 4. LA supplementation decreased the activity of liver xanthine oxidase (XO) in all experimental groups, and that of liver monoamine oxidase in Group 3. The activities of liver CAT and XO in Group 2 were higher than that in Group 3. LA supplementation elevated the pH24 h and decreased drip loss in breast meat in Groups 3 and 4. 5. In conclusion, LA supplementation can improve growth performance, antioxidant properties and meat quality in broiler chicken. LA supplementation in the starter period can improve growth performance and supplementation in the grower – and in the whole period can improve carcass characteristics. There was no significant difference in meat quality of broiler chickens fed on LA-supplemented diet in different stages.

INTRODUCTION Animals are affected by their living condition, including the potential of environmental exposure to metals, air pollution, pesticides and ionising radiation during the production period (Mena et al., 2009; Migliore and Coppedè, 2009). These exogenous factors can give rise to reactive oxygen species (ROS) in the body. ROS can also be endogenously produced during metabolic processes by organelles such as mitochondria and enzymes such as xanthine oxidase

(XO) (Galley et al., 1996). While it is well known that ROS play an important role in diverse biological processes, such as DNA replication and cell proliferation (Finkel, 2011), excessive ROS are harmful to normal metabolism, and the body has evolved a critical antioxidant defence system to remove the excess ROS by both enzymatic and non-enzymatic reactions (Finkel, 2011). Animal health is determined by the balance between production of ROS generated by endogenous and exogenous sources, and by the elimination of these species by antioxidative

Correspondence to: Feng Gao, Department of Animal Nutrition & Feed Science, College of Animal Science & Technology, Nanjing Agricultural University, No. 1 Weigang, Nanjing 210095, P.R. China. E-mail: [email protected] Accepted for publication 22 May 2014

© 2014 British Poultry Science Ltd

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defence mechanisms (Frisard and Ravussin, 2006). Oxidative stress occurs when the production of ROS exceeds the capacity of the antioxidant defence and repair mechanisms, leading to the accumulations of ROS and increased oxidation of lipids, proteins and DNA (Frisard and Ravussin, 2006). In animals consumed by humans, meat quality can be affected by lipid and protein peroxidation induced by ROS (Gao et al., 2010). For example, oxidative stress induced by oxidised oil has been shown to significantly decrease the activity of sarcoplasmic reticulum Ca2+-ATPase (SERCA) in breast muscle, leading to an acceleration in post-mortem glycolysis and increased drip loss (Zhang et al., 2011a). Moreover, protein oxidation may affect the water-holding capacity (WHC) of meat, and oxidative processes may alter the ability of proteins to affect hydrogen, electrostatic and capillary bonds with the water molecules by limiting the surface area available (Traore et al., 2012). Calpain has been shown to play an important role in WHC, and its activity has been shown to be modulated by the redox state, such that oxidative stress significantly decreases calpain activity (Guttmann and Johnson, 1998). Dietary supplementation with antioxidants has positive effects on meat quality (Gao et al., 2010; Skřivan et al., 2012). For example, supplementation of vitamin E (VE) can alleviate oxidative stress induced by dexamethasone and improve meat quality of both Musculus pectoralis major and Musculus biceps femoris in broiler chickens (Gao et al., 2010). In addition, dietary supplementation with vitamin C has been shown to increase the vitamin C content of meat in a dose-dependent manner leading to decreased lipid oxidation in pork stored up to 5 d (ArchileContreras and Purslow, 2011). Alpha-lipoic acid (LA) is a naturally occurring sulfhydryl group-containing short-chain fatty acid (Song et al., 2004) which directly scavenges free radicals and provides a reducing medium for the regeneration of the antioxidant (Podda et al., 1994). Accordingly, LA is commonly used as a biological antioxidant (Packer et al., 1995). Using nicotinamide-adenine dinucleotide phosphate (NADPH) as source of hydrogen, LA can be reduced to dihydrolipoic acid (DHLA) (Shay et al., 2009). More species of ROS can be scavenged by both LA and DHLA (Packer et al., 1997). At the same time, LA was found as a coenzyme for pyruvate dehydrogenase and αketoglutarate dehydrogenase and participated oxidative phosphorylation in mitochondria (Packer et al., 1995), and two optical isomers of LA seem to exist (R/S). Little attention has been paid to the optical activity (Song et al., 2004; Shay et al., 2009; Karaman et al., 2010; Imik et al.,

2012). A variety of studies have been carried out on the effects of LA in rat and mouse models (Shen et al., 2005), but relatively few have been carried out in animals in the human food chain, particularly broiler chickens. LA showed the protective effect to broiler subjected to heat stress (Imik et al., 2012) and experimental aflatoxin toxicosis harmful effects (Karaman et al., 2010). In hypothyroid broiler chickens, the supplementation of LA also showed alleviative effects on acute heat stress-induced thermal panting (Hamano, 2012). A large amount of research on the production of broiler chickens includes two periods: the starter and grower periods. Until now, there have been no data on the effect of LA supplementation in these distinct periods. Therefore, the current experiment was designed to investigate the effect of LA supplementation on growth performance, antioxidant capacity and meat quality in the starter and grower periods in broiler chickens.

MATERIALS AND METHODS Experimental design A total of 240 one-d-old male healthy Arbor Acres broilers were purchased from a local hatchery (Hewei Agricultural Development Co., Ltd., Anhui, China), then randomly allocated to 4 treatment groups of 6 replicates, each replicate consisting of 10 chickens. The average body weight of chicks was 39.6 ± 1.2 g; no significant differences in initial average body weight were observed between treatments. The experimental design was as follows: Group 1 was the control group without LA supplementation; Group 2 was supplied with LA in the starter period; Group 3 was supplied with LA in the grower period; and Group 4 was supplied with LA in the whole period. The concentration of supplementary LA was 500 mg/kg, and LA was provided by Wuhan Dahua Medical Chemical Co., Ltd (Wuhan, China). LA was the R/S mixed form. Since there was no technique for us to separate the R form from the R/S mix, no special attention was paid on the optical activity of LA. The experiment lasted for 6 weeks and was divided into two periods. The composition and nutrient concentrations of the basal diet are shown in Table 1. The content of metabolisable energy, crude protein, calcium, phosphorus, lysine and methionine was calculated. All chickens were placed in wire cages in a three-level battery. The brooding temperature was maintained at 35°C for the first 2 d, then decreased gradually to 21°C until 28 d of age and maintained as such until the end of the experiment. Relative humidity was maintained at 50 ± 5%. The room was lit continuously during

ALPHA-LIPOIC ACID SUPPLEMENTATION IN BROILER

Table 1. Ingredient composition and nutrient levels of basal diets

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Items Ingredient (g/kg) Maize Soybean meal Maize gluten meal Soybean oil Limestone Dicalcium phosphate Lysine HCl DL-Methionine Choline Sodium chloride Premix1 Total Nutrient levels2(g/kg) Metabolisable energy (MJ/kg) Crude protein Calcium Total phosphorus Available phosphorus Lysine Methionine Methionine + cystine

Starter

Grower

546.5 327 45 32 13 18 2.8 1.5 1.2 3 10 1000

598.5 256 55 43 14 15 2.8 1.5 1.2 3 10 1000

12.44 220.7 9.9 6.64 4.26 11.9 5.20 8.89

13.11 200.8 9.35 5.88 3.72 10.42 4.68 8.08

1

Premix provided per kg of diet: vitamin A (as retinyl acetate), 5.3 mg; vitamin D3 (as cholecalciferol), 87.5 μg; vitamin E (DL-α-tocopheryl acetate), 20 mg; vitamin K (menadione sodium bisulphate), 2.8 mg; thiamin, 2.21 mg; riboflavin, 7.8 mg; nicotinamide, 40 mg; calcium pantothenate, 10 mg; pyridoxine·HCl, 4 mg; biotin, 0.04 mg; folic acid, 1.2 mg; vitamin B12, 0.015 mg; iron, 80 mg; copper, 8 mg; manganese, 110 mg; zine, 65 mg; iodine, 1.1 mg; selenium, 0.3 mg. 2Nutrient levels are calculated.

the whole experimental period. Water and diet were provided for ad libitum consumption. At day one, d 22 and d 42, all chickens in each cage were weighted and feed consumption per cage was calculated by cage over the two periods to calculate feed conversion ratio (FCR). On the morning of 22 d, feed was replaced according to experimental design. All experimental procedures were approved by the Institutional Animal Care and Use Committee of Nanjing Agricultural University.

Sample collection On the morning of 42 d, after an 8-h fast, one chicken with BW near to the average body weight of the cage was selected and killed via exsanguination by manually cutting the carotid artery and jugular vein on the side of the neck. Then, bodies were hung for 10 min and scalded in 55°C hot water for 30 s, and the carcasses were defeathered. After that, we carried out the analysis of carcass characteristics including carcass yield, eviscerated yield, abdominal fat yield, breast muscle yield and leg muscle yield, according to the method of performance terms and measurement for poultry (ICS 01.040.65 2004). The results are expressed as a percentage of body weight. Simultaneously, livers were

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collected and stored at −20°C until analysis. Breast muscles were also collected to measure the meat quality, including meat pH, colour, drip loss, cooking loss (CL) and shear force value (SFV). Antioxidant property in liver measurements The total antioxidant capacity (T-AOC), contents of glutathione (GSH) and MDA, activities of total superoxide dismutase (T-SOD), catalase (CAT), glutathione peroxidase (GSH-Px), XO, monoamine oxidase (MAO), nitric oxide synthetase (NOS) and myeloperoxidase (MPO) were detected using the commercial assay kits from Nanjing Jiancheng Biochemistry Reagent Co (NJBC, Nanjing, Jiangsu, China) according to the instructions of the manufacturer. Meat quality measurements Muscle pH values at 45 min (pH45 min) and 24 h post-mortem (pH24 h) were measured in triply at a depth of 0.5 cm below the muscle surface by using an HI9125 portable waterproof pH/ORP meter (Hanna Instruments, Cluj-Napoca, Romania). Meat colour (L*, relative lightness; a*, relative redness; b*, relative yellowness) was assessed by using a Minolta CR-410 Chroma Meter (Konica Minolta Sensing Inc., Osaka, Japan). Each breast muscle was detected in three positions and the measurements averaged. Drip loss was measured according to the method of Zhang et al. (2011b). Briefly, approximately 30 g of regular shaped muscle, cut from the same location in the right breast, was weighted and placed on transparent polystyrene trays and air-tightly sealed and then hanged for 24 h. All samples were stored at 4° C. After that, surface moisture of the fillets was absorbed with filter paper, and muscles were reweighed. Drip loss was calculated using the formula: [(initial weight − final weight)/initial weight] × 100. CL was measured after finishing drip loss according to the method of Zhang et al. (2011b). Briefly, breast muscles were cooked in an 80°C water bath (HH-42, Guohua, Shanghai, China) until an internal temperature of 75°C was reached. Muscles were cooled by flowing water after which excess moisture was removed by filtering and the muscle was reweighed. CL was calculated by using the formula: [(raw weight − cooked weight)/raw weight] × 100. Shear force were measured according to the method of Zhang et al. (2011b). Briefly, cooked meat was cut from the medial portion muscle, parallel to the longitudinal axis of the myofibres (3.0-cm long, 1.0-cm wide and 0.5-cm thick), and

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sheared by using a 15-kg load and crosshead speed of 150 mm/min with a Digital Meat Tenderness Meter (Model C-LM3, Engineering College Northeast Agricultural University, Harbin, China). Shear force was perpendicular to the axis of muscle fibres in triple, and its value is expressed in newton (N).

Statistical analysis

Growth performance The Figure shows the effects of LA supplementation on growth performance of broiler chickens. In the starter period, dietary LA supplementation significantly increased the average feed intake (AFI) (P < 0.05, Group 1 vs. Group 2; Group 4 vs. Group 3), and through the whole experimental period, compared with the control group, dietary supplementation with LA in the starter period significantly increased the AFI (P < 0.05), but no significant difference was observed in the grower period and the whole period (P > 0.05, Figure A). In the starter period, the supplementation with LA also significantly increased the body weight gain (BWG) (P < 0.05, Group 2 vs. Group 1;

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Results were calculated as mean values and the standard error of the mean (SEM) and analysed using Statistical Package for Social Sciences (SPSS Inc., Chicago, IL, USA), by one-way ANOVA, followed by the least significant difference test. The level of significance was accepted as P < 0.05.

RESULTS

Figure. Effect of alpha-lipoic acid (LA) supplement in different stages on growth performance of broilers. “−”: no LA supplementation, “+”: LA supplementation at 500 mg/kg.

ALPHA-LIPOIC ACID SUPPLEMENTATION IN BROILER

supplementation with LA significantly increased T-AOC in all three treatment groups (P < 0.05) and concentrations of liver GSH in the whole period (P < 0.05). Relative to control group, dietary supplementation with LA increased the activities of T-SOD, CAT and GSH-Px in all treatment groups, especially in the whole period (P < 0.05). The LA supplementation decreased the concentration of MDA in liver, but no significant difference was observed in treatment groups (P > 0.05). Compared to the control group, LA supplementation decreased the activity of XO in liver in all treatment groups (P < 0.05), as well as that of MAO, especially in the grower period (P < 0.05). In addition, supplementation with LA increased the activity of NOS in the whole period (P < 0.05), but no significant difference in the activity of liver MPO was observed in all three administration treatment groups (P > 0.05).

Group 4 vs. Group 3), and through the whole experimental period, compared with the control group and the grower group, LA supplementation in the starter period significantly increased the BWG (P < 0.05), but no significant change was observed in the grower period and the whole period (P > 0.05, Figure B). The supplementation with LA did not affect the FCR for all three administration treatments (P > 0.05, Figure C).

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Carcass characteristics Table 2 shows the effects of LA supplementation on carcass characteristics of broilers. The supplementation with LA in the grower period and whole period significantly decreased abdominal fat yield compared to control group (P < 0.05). However, no significant differences in carcass yield, eviscerated yield, breast muscle yield and leg muscle yield were observed in all three administration treatment groups (P > 0.05).

Meat quality Table 4 shows the effects of LA supplementation on meat quality of broiler chickens. Relative to the control group, LA supplementation significantly increased the pH24 h (P < 0.05) in the grower

Antioxidant property in liver Table 3 shows the effects of LA supplementation on the antioxidant properties of broiler livers. The Table 2.

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Effect of alpha-lipoic acid (LA) supplement in different stages on carcass characteristics of broilers (n = 6) Treatments1

Items Carcass yield Eviscerated yield Abdominal fat yield Breast muscle yield Leg muscle yield

Group 1

Group 2

Group 3

Group 4

Pooled SEM

P-value

85.64 68.06 2.65a 26.60 20.17

86.26 69.90 2.73a 27.76 20.11

86.67 70.11 1.82b 28.97 19.82

86.72 69.73 1.74b 28.12 20.23

0.206 0.320 0.182 0.351 0.250

0.712 0.438 0.016 0.211 0.178

1

Group 1 = the control; Group 2 = the starter pried diet with 500 mg/kg LA supplementation; Group 3 = the grower period diet with 500 mg/kg LA supplementation; Group 4 = the whole feeding stage diet with 500 mg/kg LA supplementation. a,bMeans within the same row with no common superscript differ significantly (P < 0.05).

Table 3.

Effect of alpha-lipoic acid (LA) supplement in different stages on antioxidant property in liver of broilers (n = 6) Treatments2

Items1

Group 1

Group 2

Group 3

Group 4

Pooled SEM

P-value

T-AOC (U/mg protein) GSH (mg/g protein) T-SOD (U/mg protein) CAT (U/mg protein) GSH-Px (U/mg protein) MDA (nmol/mg protein) XO (U/g protein) MAO(U/mg protein) NOS (U/mg protein) MPO (U/g protein)

1.40c 4.60b 225.6b 9.58b 34.60b 1.13 42.58a 3.28a 0.45b 0.34

1.56a,b 4.63b 243.7a 12.2a 35.55b 1.03 36.59b 2.98a,b 0.43b 0.33

1.49b 4.85b 250.6a 10.16b 35.70b 1.05 33.30c 2.75b 0.44b 0.34

1.67a 5.76a 246.2a 12.32a 38.42a 1.02 33.91c 2.99a,b 0.51a 0.32

0.034 0.151 3.784 0.362 1.627 0.025 1.158 0.075 0.011 0.007

0.003 0.024 0.036 0.012 0.018 0.121 0.009 0.013 0.018 0.327

1

T-AOC = total antioxidant capacity; GSH = glutathione; T-SOD = total superoxide dismutase; CAT = catalase; GSH-Px = glutathione peroxidase; MDA = malondialdehyde; XO = xanthine oxidase; MAO = monoamine oxidase; NOS = nitric oxide synthase; MPO = myeloperoxidase. 2Group 1 = the control; Group 2 = the starter pried diet with 500 mg/kg LA supplementation; Group 3 = the grower period diet with 500 mg/kg LA supplementation; Group 4 = the whole feeding stage diet with 500 mg/kg LA supplementation. a,b,cMeans within the same row with no common superscript differ significantly (P < 0.05).

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Table 4.

Effect of alpha-lipoic acid (LA) supplement in different stages on breast meat quality of broilers (n = 6) Treatments2

Items1 pH45 min pH24 h L* a* b* Drip loss, % Cooking loss, % Shear force value (N)

Group 1

Group 2

Group 3

Group 4

Pooled SEM

P-value

6.20 5.98b 46.52 3.91 9.18 1.62a 15.77 15.39

6.22 6.08a,b 45.46 3.87 8.78 1.16b 15.77 14.85

6.20 6.11a 44.78 3.97 8.10 1.21b 16.40 14.24

6.19 6.12a 47.03 4.09 8.98 1.29b 15.22 14.03

0.025 0.030 1.268 0.081 0.203 0.074 0.730 0.578

0.619 0.015 0.341 0.370 0.169 0.008 0.477 0.144

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1 pH45 min = pH at 45-min post-mortem; pH24 h = pH at 24-h post-mortem. 2Group 1 = the control; Group 2 = the starter pried diet with 500 mg/kg LA supplementation; Group 3 = the grower period diet with 500 mg/kg LA supplementation; Group 4 = the whole feeding stage diet with 500 mg/kg LA supplementation. a,bMeans within the same row with no common superscript differ significantly (P < 0.05).

period and in whole period and decreased the drip loss in all treatment groups (P < 0.05). In addition, compared to the control group, the supplementation with LA decreased the SFV, but no significant difference was observed (P > 0.05). However, LA supplementation had no significant effect on pH45 min, meat colour (L*, a*, b*) or CL (P > 0.05).

DISCUSSION LA and its reduced form, DHLA, are potent scavengers of ROS; they react with ROS such as superoxide radicals, hydroxyl radicals, hypochlorous acid, peroxyl radicals and singlet oxygen (Packer et al., 1995). The antioxidant capacity of LA enables it not only to directly scavenge free radicals, but also to provide the reducing medium for the regeneration of the antioxidant. In VE-deficient adult hairless mice, the supplementation with LA prevented symptoms of VE deficiency (Podda et al., 1994), indicating that LA has a higher reduction capacity than VE. In the present study, LA supplementation improved both AFI and BWG, especially in the starter period. Although dietary supplementation at the concentration of 300 mg/kg LA has been shown not to affect growth performance of broiler chickens, average daily LA intake was significantly increased (Chen et al., 2011). In addition, dietary supplementation with 900 mg/kg LA had been shown to result in a lower growth performance (Zhang et al., 2009; El-Senousey et al., 2013). This result indicates that higher doses of LA may inhibit growth performance of broilers. The LA supplementation above the concentrations of 900 mg/kg showed a negative effect on chicken growth performance (Zhang et al., 2009; El-Senousey et al., 2013). Therefore, we chose 500 mg/kg as the expected ideal supplementation concentration in the present study, and our results showed that 500 mg/kg was a good level for improving broiler growth performance and

enhancing antioxidant capacity. However, dietary LA (500 mg/kg) has been shown to decrease weight gain in mice by 15%; at a dietary concentration of 1000 mg/kg, the decrease in weight was 30% (Shen et al., 2005). The decrease in weight gain affected by LA in this instance might be related to the use of 2-m-old adult mice as experimental animals. FCR was not affected by dietary LA content (Zhang et al., 2009; El-Senousey et al., 2013), which is in agreement with the present results. The present study shows that supplementation with LA in the grower period and in whole period decreased abdominal fat yield. A similar change was shown in respect of LA supplementation at the concentration of 900 mg/kg (Zhang et al., 2009) and at the concentration of 800 mg/kg and 1200 mg/kg (El-Senousey et al., 2013). The explanation of LA effects on decreased abdominal fat is highly controversial about the activation of AMP-activated protein kinase (AMPK) signalling pathway. The decreased phosphorylation of AMPK α subunit at Thr172 in response to dietary LA supplementation has been linked to decreased fat accumulation in mice (Shen et al., 2005). Another explanation of LA on metabolic changes was mediated via inhibition of hypothalamic AMPK activity while activating the peripheral AMPK signalling pathway (Song et al., 2013). It has been speculated that weight loss caused by LA, a cofactor of mitochondrial enzymes, was due to enhanced energy expenditure through increased expression of uncoupling protein-1 (UCP-1) (Kim et al., 2004). UCP-1 catalyses the net transfer of protons across the mitochondrial inner membrane, dissipating force as heat in mammalian brown adipose tissue (Oelkrug et al., 2010). Another explanation of this phenomenon is that in skeletal muscle, LA increases energy expenditure by enhancing the adenosine monophosphate–activated protein kinase (AMPK)–peroxisome proliferator-activated receptor-γ (PPARr-γ) coactivator-1α (PGC-1α) signalling pathway (Wang et al., 2010). That supplementation of LA decreased the abdominal fat might be related to the alteration of glucose

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availability and the whole-body insulin sensitivity (Rhoads et al., 2013). The precise mechanism of the LA-effected decrease in abdominal fat yield requires further studies. In the present study, livers were chosen as representative samples for evaluating the antioxidant capacity of the whole body. In this study, the results showed that supplementation with LA improved the hepatic antioxidant capacity via an increase in the concentration of GSH and the activities of T-SOD, CAT and GSH-Px and a decrease in the oxidase activity of XO and MAO. T-AOC has been shown to increase in response to the supplementation with LA at 300 mg/kg, and LA has also been shown to increase hepatic SOD activity and significantly decrease MDA concentrations (Chen et al., 2011). Similar results were reported (Zhang et al., 2009). The current study indicated that birds in the whole period had a higher antioxidant capacity than those in starter and grower periods. This phenomenon might be due to the accumulation of LA or the regeneration of the antioxidant (Podda et al., 1994) and the clearance of ROS by LA (Packer et al., 1997). In aged rats, supplementation with LA has been shown to improve antioxidant status and ameliorate mitochondrial antioxidant defence systems, through a decrease in the production of free radical and the concentrations of MDA (Savitha et al., 2005), which is in agreement with the current experiment. The results in this study further showed that there was no marked difference between the supplemented starter and grower periods with respect to T-AOC, GSH and the activities of T-SOD, CAT and GSH-Px. Xanthine oxidoreductase (XOR) has two functional forms, including xanthine dehydrogenase (XDH) that couples the production of uric acid and XO, generating the free radical superoxide in the production of uric acid (Bainbridge et al., 2009). These two forms could turn over with the redox state of the body (Sakuma et al., 2009). In this study, supplementation with LA markedly decreased the activity of XO, especially in the grower period which may be attributable to (1) decreased activity of XO while there was no change between XDH and XO; (2) a decrease in the protein level at which XO decreased and reduced change in the activity of XO with the change of redox state provided by LA; and (3) a decrease in the protein level and the XO activity decrease in response to supplementation with LA. Further research is needed to investigate XO content in different redox states by using western blot. However, due to our experimental condition, we have not done this in the present experiment. MAO that includes MAO-A and MAO-B (Bortolato et al., 2008) could catalyse the oxidative deamination of amines. The products of this reaction included aldehyde, hydrogen peroxide and

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ammonia (Bortolato et al., 2008). The activity of MAO also decreased, and we speculated that the decreased activity of MAO in response to LA might be due to the alteration of redox states with LA supplementation. A selective irreversible MAO inhibitor, rasagiline, has the ability of increasing the activity of SOD and CAT enzymes (Carrillo et al., 2000). Nitric oxide (NO), which can be thought of as a kind of ROS, has a short half-life in the body, and the concentration of NO can be indirectly measured by the activity of NOS (Luiking et al., 2010). NO has been shown to react with superoxide to form the highly reactive oxidant, peroxynitrite, ONOO−, which can cause tissue injury (Zweier and Talukder, 2006). One explanation of the increased NOS activity is that with the improvement in antioxidant capacity and the lower concentration of ROS, the less chance there will be for the reaction of ROS and NO to form peroxynitrite. However, the activity of NOS did not change between the starter period and grower period. MPO is a molecule of 146– 150 kDa (Anatoliotakis et al., 2013) and utilises hydrogen peroxide (H2O2) and chloride ions as substrate to produce a highly deleterious hypochlorous acid (HOCl) (Guilpain et al., 2008; Loria et al., 2008; Anatoliotakis et al., 2013). Because there was no change following the different treatments, it reflects the fact that the chickens were fed in normal condition with no inflammation and state of oxidative stress. Supplementation of LA shows the ability to improve the antioxidant property, which is related to the improvement in meat quality. In the present study, supplementation with LA increased the pH24 h, decreased the drip loss and showed a tendency to reduce shearing force of breast meat. In the experiment in mice, dietary supplementation with LA has been shown to suppress the activation of AMPK in post-mortem muscles (Shen and Du, 2005). The inactivation of AMPK decreases the rate of glycolysis, such that in postmortem muscle the ultimate pH appears to be relatively higher. In this study, supplementation of LA increased the pH24 h, similar to the result in the pH of Zhang et al. (2009), who reported dietary LA supplementation significantly increased breast and thigh muscle pH value at 24-h post-mortem. The improvements in antioxidant property ameliorate meat quality through different methods. The SERCA activity of breast muscle, which accelerates post-mortem glycolysis and increases drip loss, has been shown to be significantly decreased by oxidative stress induced by oxidised oil (Zhang et al., 2011a). ROS has been shown to increase matrix metalloproteinase-2 (MMP2) activity and reduce collagen synthesis, suggesting that they play a negative role in meat quality (Archile-Contreras and Purslow, 2011). In the present experiment, the decline of

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MDA was an indirect amelioration of the antioxidant capacity of the whole body, which might be another reason for the improvement in meat quality. LA supplementation had no effect on the pH24 h between the groups. The decline of phosphorylation of AMPK not only reflects the inhibition of glycolysis, but also reflects the improvement in WHC. The inhibition of glycolysis by the decline of phosphorylation of AMPK played a predominant role in affecting the drip loss. At the same time with the supplementation of LA, the improvement in antioxidant might be another explanation, since the calpain activity, which plays important role in WHC, can be modulated by redox state (Guttmann and Johnson, 1998). The decline of drip loss in this experiment was a marker of the improvement in the WHC. Supplementation with LA has been shown to decrease the SFV in breast muscle and thigh muscle in broiler chickens (Zhang et al., 2009), and the improvement in antioxidant capacity has also been shown to decrease SFV in finishing pigs (Ma et al., 2010). In the present results, supplementation with LA in different periods showed a tendency to reduce SFV, suggesting that LA supplementation also plays a role in improving breast tenderness of broiler chickens. In conclusion, LA supplementation can improve the growth performance, increase antioxidant properties and improve meat quality. In addition, LA supplementation in the starter period can improve growth performance, and LA supplementation in the grower period and in whole period is beneficial for improving carcass characteristic through decreased abdominal fat. There was no significant difference in the meat quality of broiler chickens fed on LA supplementation diets in any of the different stages.

FUNDING This research was funded by the National Science & Technology Pillar Program during the Twelfth Fiveyear Plan Period of China [grant number 2012BAD28B03]; Three Agricultural Projects of Jiangsu province of China [grant number SX(2011) 146]; and the Fundamental Research Funds for the Central Universities of China [grant number KYZ201222].

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