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Effect of Ginkgo biloba Leaf Powder on Growth Performance, Meat Quality and Antioxidant Activity of Muscle in Growing-Finishing Pigs.

Byline: Xianglun Zhang, Peng Lu, Wenyue Xue, Dawei Wu, Chao Wen, Liren Ding and Yanmin Zhou

Abstract

An experiment was conducted to evaluate the effect of Ginkgo biloba (G. biloba) leaf powder on growth performance, meat quality and antioxidant activity of muscle in growing-finishing pigs. A total of 75 finishing barrows were randomly distributed to 5 groups, receiving basal diet (Control), basal diet supplemented with 0.50% coarse G. biloba leaf powder (CG) or basal diet supplemented with 0.05% (UG1), 0.25% (UG2) and 0.50% (UG3) ultrafine G. biloba leaf powder, respectively. Meat quality of longissimus dorsi muscle and leg muscle was improved by addition of UG, which was consistent with the simultaneously enhanced antioxidant capacity of muscles. Additionally, pigs fed diet supplemented with CG also exhibited improved antioxidant status of measured muscles than that of control. The antioxidant capacity of both longissimus dorsi muscle and leg muscle of pigs fed CG and UG especially the UG were better than that of the control.

In conclusion, addition of G. biloba leaf powder resulted in improvement in meat quality and antioxidant capacity of muscle and this effect was more pronounced when supplementing ultrafine G. biloba leaf powder.

Key words: G. biloba leaf powder, Pig, Growth performance, Meat quality, Antioxidant activity

INTRODUCTION

As a traditional natural medicinal herb in China, G. biloba is a sole living member of the family Ginkgoaceae that has survived unchanged for millions of years (Jacobs and Browner, 2000). The extract from G. biloba leaf has been utilized in many fields such as food, biochemistry, as well as in pharmacology, showing high antioxidant activity (Goh et al., 2003; Kobus-Cisowska et al., 2014), antibacterial effect (Lee et al., 2014), and physiological activity in therapies for diseases (Puebla- Perez et al., 2003; Lu et al., 2006). Chemically, the active constituents of the G. biloba leaf are flavonoids (flavone glycosides, primarily composed of quercetin) and terpenoids (ginkolides and bilobalides) (Pietri et al., 1997; van Beek and Montoro, 2009). G. biloba extract also shows high biological activity when fed to animal. Yao et al. (2006) observed that G. biloba extract could provide protection against ethanol-induced oxidative stress on various tissues of male rats.

Sener et al. (2007) also found that G. biloba extract could protect many tissues of rat from suffering oxidative stress induced by mercury (II).

G. biloba extract is prepared in a multistep process (van Beek and Montoro, 2009) that may cause a higher price and many nutrients in G. biloba leaf may be damaged during extraction process. Dietary addition of G. biloba leaf directly may reduce the cost and protect the nutrients in the leaf. At present, there are few researches on the application of G. biloba leaf in the animal production (Cao et al., 2012; Zhang et al., 2012; Yu et al., 2015). The addition level of G. biloba leaf in the feed of the above studies ranges from 0.35% to 0.70%, but the particle size of G. boliba leaf is not definite. Particle size may be an important factor (Fastinger and Mahan, 2003; Li et al., 2008) affecting the bioavailability of G. biloba leaf. Coarse grinding cannot thoroughly break up the cell walls of G. biloba leaf and thus active components in the cell may be difficult to release.

Ultrafine grinding technology is a useful tool for making ultrafine powder with good surface properties like dispersibility and solubility (Tkacova and Stevulova, 1998), and have found applications in some fields (Cordeiro et al., 2009; Ma et al., 2009). The reduction of particle sizes of various materials to micro- or nanosizes brings some new outstanding characteristics including surface effect, quantum effect, magnetic property, mechanical property, chemical and catalytic properties that bulk materials do not possess before (Zhu et al., 2010). Our findings have demonstrated that the dissolution of total flavonoids and terpenoids in ultrafine G. biloba leaf powder was higher than that in coarse G. biloba leaf powder (Zhang et al., 2014). Based on these characteristics, ultrafine G. biloba leaf powder may be more effective when added to animal diets.

However, little information is available concerning the effects of ultrafine G. biloba leaf powder in animal production.

The present work was carried out to investigate the effect of G. biloba leaf powder on growth performance, meat quality, meat composition and antioxidant capacity of muscle in growing-finishing pigs.

MATERIALS AND METHODS

Preparation of G. biloba leaf powder

Air-dried G. biloba leaves were purchased from a local company and were used for this study. The dry leaves are 960.0+-1.16, 135.1+-0.24 and 136.7+-0.19 g/kg, respectively. The leaves were ground into two particle sizes categorised as coarse and ultrafine G. biloba leaf powder. The coarse G. biloba leaf powder was processed by a water type pulverizer (SDHM, Wuxi Zhongya Food Factory, Wuxi, Jiangsu, China) while the ultrafine G. biloba leaf powder was obtained by a micronizer (LHJ-500, Zhengyuan Powder Engineering Equipment Company, Weifang, Shandong, China). The particle sizes of G. biloba leaf powder were determined by using a laser Mastersizer (Instruments 2000, UK) according to of China. The particle sizes of the coarse and ultrafine G. biloba leaf powder were: D50 = 560 um and D50 = 18.1 um, respectively.

The dissolution of flavonoids and terpenoids of the G. biloba leaf powder were measured by spectrophotometric method at 510 nm and 514 nm using Rutin and Ginkgolide A (Shanghai Yuanye Bio- Technology Co., Ltd, Shanghai, China) as standard, respectively. The dissolution of flavonoids of the coarse and ultrafine G. biloba leaf powder were: 1.47+-0.06% and 2.00+-0.06%, and the dissolution of terpenoids were 0.63+-0.07% and 0.96+-0.10%, respectively (Zhang et al., 2014).

Animals and management

The experimental design and procedures were approved by the Animal Care and Use Committee of Nanjing Agricultural University.

Seventy-five [(Landrace Yorkshire) Duroc] finishing barrows with initial body weight of 67.81+-1.33 kg were randomly divided into 5 dietary treatments consisting of 3 replicates of 5 pigs each, balanced for body weight with a randomized complete block design. All pigs were provided with mash feed and water ad libitum and were reared in collective cages with solid concrete floor. The rearing period was 45 d.

Pigs in the control group were fed a basal diet, and pigs in the other four groups were fed the basal diet supplemented with 0.50% coarse G. biloba leaf powder, 0.05%, 0.25% and 0.50% ultrafine G. biloba leaf powder, referred to as CG group, UG1 group, UG2 group, and UG3 group, respectively. Pigs used in the study were all adapted to the experimental diets for 7 d before the experiment started. The compositions of the basal diets and nutrient levels were formulated according to the NRC (1998) nutrient requirements (Table I).

Table I.- Ingredients and nutrient composition of basal diet, air dry basis.

###Calculated

Ingredient###%

###nutrient level

Maize###67.52###Digestible energy###13.64

###(MJ/kg)

Distillers dried grains with###10.45###Crude protein, %###13.71

solubles

Soybean meal###4.48###Calcium, %###0.50

Rice bran###2.59###Available###0.23

###phosphorus, %

Maize germ cake###3.98###Lysine, %###0.80

Wheat middling###3.98###Methionine +###0.49

###cystine, %

Soybean oil###1.00

Soybean phospholipids###1.00

Premix1###5.00

Total###100.00

Growth performance

Body weights were recorded for each replicate at the first day and 45 d of the feeding period. Feed intake was also recorded during the 45-d trial. The body weight gain, feed intake and gain:feed ratio were calculated.

Slaughter and sample collection

At 45 d of the feeding period, 3 pigs in each group (one pig per replicate) were randomly selected and weighed after feed deprivation for 12 h. Pigs were transported to the abattoir where they were humanely sacrificed. After killing, longissimus dorsi muscle and hind leg muscle samples were immediately excised from each carcass for the determination of meat quality. Muscle samples were taken and then stored at -20degC for the assay of meat composition and antioxidant indices.

Meat quality

Longissimus dorsi muscle and hind leg muscle were used to determine pH, objective color measurements, drip loss and cooking loss. The pH at 45 min postmortem (pH45 min) and 24 h postmortem (pH24 h) were measured by a portable pH meter (HI9025, Hanna Instruments, Italy) according to Schilling et al. (2008). Color measurements were taken at 45 min and 24 h postmortem. Lightness (L*), redness (a*), and yellowness (b*) values were determined using a Minolta CR410 chroma meter (Konica Minolta, Tokyo, Japan) as described by Cao et al. (2012). Drip loss at 24 h and 48 h postmortem and cooking loss were measured using the methods outlined by Franco et al. (2009, 2014).

Meat composition

Meat samples were prepared for determination of moisture, crude protein, ether extract and crude ash based on Association of Official Analytical Chemists procedures (AOAC, 1990).

Assay of antioxidant indices in muscle

Muscle samples were analyzed for total superoxide dismutase (T-SOD) and glutathione peroxidase (GSH-Px) activities, total antioxidant capacity (T-AOC), and malondialdehyde (MDA) content using commercial kits (Nanjing Jiancheng Bioengineering Institute, Nanjing, China) according to the manufacturer's instructions. Briefly, the activity of T-SOD was determined by following the nitrite method as described by Oyanagui (1984). One unit of SOD was defined as the amount of SOD required to produce 50% inhibition of the rate of nitrite production at 37 degC. The methodology used in determining GSH-Px activity was dithio-nitro benzene method described by Hafeman et al. (1974). One unit of GSH-Px activity was defined as the amount of enzyme that would catalyze the conversion of 1 umol/L of GSH to oxidized GSH at 37 degC in 5 min. The concentration of MDA was determined by following the TBA method as described by Placer et al. (1966).

The activities of antioxidant enzymes and the content of MDA were expressed as units per milligram of protein for muscle.

Statistical analysis

The effects of dietary treatment were statistically analyzed by one-way ANOVA (SPSS 16.0). Differences among treatments were examined by Duncan's multiple range test. Values in the tables were means and pooled SEM. Statistical significance was determined at P0.05) on growth of pigs, but numerically increased the final weight and body weight gain as compared with that of the control pigs (Table II). All pigs appeared healthy and no mortality occurred during the experimental period (data not shown). Our findings were similar with Zhang et al. (2012) who reported that dietary addition of 0.35% G. biloba leaf did not affect the body weight gain and feed conversion compared with the control group in the period of 0 to 21 day of broilers.

Meat quality

The data of meat quality were summarized in Table III and Table IV. The pH45 min of longissimus dorsi muscle in the UG2 group was higher (P0.05) was found in pH24 h of neither longissimus dorsi muscle nor leg muscle among groups, but the pH24 h of both kinds of muscles in UG2 group tended to be the highest numerically. Animal muscle pH is neutral before slaughter, but the pH declines after slaughter because glycolysis causes lactic acid accumulation in muscles (Bai et al., 2013). The results in this trial indicated that dietary addition of G. biloba leaf powder might maintained a relatively higher pH value of meat. Muscle pH is highly correlated with numerous meat quality attributes, such as water-holding-capacity, meat color and so on (Huff-Lonergan et al., 2002).

The 24-h drip loss of longissimus dorsi muscle in both the UG2 and UG3 groups was lower (P<0.05) than that of the control group. In addition, lower (P<0.05) 24-h drip loss of leg muscle was found in both the CG and UG2 groups. The water-holding-capacity (drip loss and cooking loss) of meat is related to the intramuscular lipids, moisture content and lipid peroxide contents in the muscle (Macit et al., 2003; Cao et al., 2012). The improvement in drip loss might result from the antioxidant capacity of flavonoids and terpenoids in G. biloba leaf powder which could alleviate lipid oxidation, enhance integrity of cellular membrane, thus decreased drip loss in muscle (Rong et al., 1996; Kobus-Cisowska et al., 2014). The a*45 min of longissimus dorsi muscle in the UG groups was higher (P<0.05) than that of the control group. Meanwhile, pigs fed with G. biloba leaf powder supplemented diets had higher (P0.05) on the content of moisture, crude protein, ether extract or crude ash of neither longissimus dorsi muscle nor leg muscle, indicating that the deposition of these nutrients in muscles might not be affected by G. biloba leaf powder.

Antioxidant enzyme activities and lipid peroxidation levels

Table VI showed the antioxidant enzyme activities and lipid peroxidation of both longissimus dorsi muscle and leg muscle. The T-SOD activity of the longissimus dorsi muscle in UG2 group was higher (P0.05) the T-AOC and GSH-Px activity of neither longissimus dorsi muscle nor leg muscle. SOD plays a vital role in balancing body oxidation and antioxidation (Cao et al., 2012). These results suggested that dietary addition of UG enhanced antioxidant activity of pig muscle by elevating the activity of SOD. Lipid peroxidation is a natural phenomenon involved in the loss of unsaturated lipids by peroxidation, thus, causes lipid degradation and membrane disruption in the muscle (Bai et al., 2013). MDA is widely used as a biomarker for oxidative deterioration of lipid in muscle (Corino et al., 1999; Liu et al., 2009).

In this trial, dietary addition of CG, UG1 and UG2 decreased (P<0.05) the concentration of MDA in longissimus dorsi muscle compared with the control group. The MDA concentration of leg muscle was also decreased (P<0.05) in UG groups. These results indicated that dietary addition of G. biloba leaf powder could alleviate lipid peroxidation in muscle.

Table IV.- Meat quality of leg muscle in pigs fed diets supplemented with G. biloba leaf powder.

###Treatments2

###Item1###SEM3###P-value

###Control###CG###UG1###UG2###UG3

###pH45 min###6.58###6.60###6.53###6.65###6.40###0.05###0.68

###pH24 h###5.79###5.79###5.84###5.86###5.73###0.03###0.71

###24-h drip loss, %###1.65a###1.23b###1.53ab###1.18b###1.50ab###0.06###0.04

###48-h drip loss, %###3.10###2.77###2.73###2.72###3.07###0.11###0.75

###Cooking loss, %###28.97###27.66###25.09###23.31###28.69###1.02###0.36

###a*45 min###3.69b###4.36a###4.77a###4.48a###4.48a###0.14###0.04

###b*45 min###8.89###8.81###8.30###8.79###8.51###0.09###0.20

###L*45 min###42.03###40.42###40.09###41.11###40.21###0.29###0.19

###a*24 h###5.10###5.46###6.21###5.70###6.40###0.23###0.39

###b*24 h###10.38###10.91###10.44###10.13###10.37###0.20###0.86

###L*24 h###45.98###45.51###43.67###43.69###43.50###0.48###0.33

Table V.- Meat composition of longissimus dorsi muscle and leg muscle in pigs fed diets supplemented with G. biloba leaf powder (in living basis, %).

###Treatments1

###Item###SEM2###P-value

###Control###CG###UG1###UG2###UG3

###Longissimus dorsi muscle

###Moisture###71.27###71.78###70.61###71.95###71.96###0.25###0.42

###Crude protein###20.81###20.68###20.48###21.17###21.11###0.20###0.84

###Ether extract###4.14###4.12###4.37###4.47###4.24###0.09###0.80

###Crude ash###1.16###1.16###1.23###1.15###1.13###0.01###0.33

###Leg muscle

###Moisture###72.40###73.39###72.48###73.79###73.73###0.30###0.45

###Crude protein###23.91###22.40###23.62###22.64###22.56###0.28###0.35

###Ether extract###1.56###1.47###1.71###1.32###1.47###0.06###0.43

###Crude ash###1.11###1.23###1.13###1.29###1.18###0.03###0.39

Some studies reported that flavonoids could inhibit the formation of oxygen radicals (superoxide ions and hydroxyl radicals) and scavenge superoxide radicals which are strong peroxidative agents (Facino et al., 1990; Jia et al., 1999), and terpenoids could protect rat heart through inhibiting the formation of free radical (Pietri et al., 1997). These support our proposition that antioxidant improvement in muscle might be due to the antioxidant capacity of flavonoids and terpenoids in G. biloba leaf. In our study, UG inclusion increased the activity of T-SOD in longissimus dorsi muscle and decreased the content of MDA in leg muscle, whereas CG inclusion exerted no significant effect on this compared with the control group, implying that pigs in UG groups had better ability in enhancing body antioxidant status than those in CG group.

These results accorded with the studies of Zhang et al. (2009), who observed that dietary addition of ginger powder ranging from 300 to 8.4 um increased T-SOD activity and decreased serum MDA concentration in serum of broilers. Similar results were found by Wu et al. (2014), who demonstrated that fine but not coarse oolong tea (Camellia sinensis) powder significantly increased SOD activity and decreased MDA content in serum compared with the control group.

Table VI.- Antioxidant enzyme activities and lipid peroxidation levels in longissimus dorsi muscle and leg muscle of pigs fed diets supplemented with G. biloba leaf powder.

###Treatments2

###Item1###SEM3###P-value

###Control###CG###UG1###UG2###UG3

###Longissimus dorsi muscle

###T-SOD, U/mg prot###31.35b###32.31b###35.30ab###37.23a###33.76ab###0.72###0.03

###GSH-Px, U/mg prot###6.67###7.34###7.30###8.29###8.60###0.33###0.38

###T-AOC, U/mg prot###0.19###0.23###0.20###0.20###0.23###0.01###0.73

###MDA, nmol/mg prot###0.78a###0.67b###0.67b###0.65b###0.70ab###0.02###0.04

###Leg muscle

###T-SOD, U/mg prot###26.14###25.10###26.98###26.64###27.57###0.67###0.86

###GSH-Px, U/mg prot###2.21###2.23###2.61###2.56###2.90###0.23###0.91

###T-AOC, U/mg prot###0.06###0.06###0.07###0.07###0.06###0.01###0.97

###MDA, nmol/mg prot###1.06a###0.96ab###0.93b###0.91b###0.94b###0.02###0.04

As it is known that flavonoids and terpenoids are the active components in G. biloba leaf influencing its antioxidant activity, both of which are present in leaf cells, coarse grinding may not be able to thoroughly break up the cell walls (Zhao et al., 2009) of G. biloba leaf and thus active components may be difficult to release.

CONCLUSION

In conclusion, dietary supplementation of G. biloba leaf powder had no significant effect on neither growth performance nor meat chemical composition in growing- finishing pigs. Addition of G. biloba leaf powder could improve meat quality and enhance antioxidant capacity of muscle and this effect was more pronounced when supplementing ultrafine G. biloba leaf powder.

ACKNOWLEDGEMENTS

This study was supported by the Science and Technology Development Plan of Jiangsu province in China (BN2012043). The technical assistance of our labmates are gratefully acknowledged. All authors have approved the submission of this manuscript and declared no conflict of interest.

Statement of conflict of interest

Authors have declared no conflict of interest.

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Author:Zhang, Xianglun; Lu Peng; Xue, Wenyue; Wu, Dawei; Wen, Chao; Ding, Liren; Zhou, Yanmin
Publication:Pakistan Journal of Zoology
Article Type:Report
Date:Oct 31, 2016
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