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Effect of dietary supplementation of wild grape on the antioxidative potential of the breast and leg meat of broilers

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Effect of dietary supplementation of wild grape on the antioxidative potential of the breast and leg meat of broilers
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  83 Korean J. Food Sci. An.  Vol. 33, No. 1, pp. 83~88(2013) DOI http://dx.do.org/10.5851/kosfa.2013.33.1.83 󰁅󰁦󰁦󰁥󰁣󰁴 󰁯󰁦 󰁄󰁩󰁥󰁴󰁡󰁲󰁹 󰁓󰁵󰁰󰁰󰁬󰁥󰁭󰁥󰁮󰁴󰁡󰁴󰁩󰁯󰁮 󰁯󰁦 󰁗󰁩󰁬󰁤 󰁇󰁲󰁡󰁰󰁥 󰁯󰁮 󰁴󰁨󰁥 󰁁󰁮󰁴󰁩󰁯󰁸󰁩󰁤󰁡󰁴󰁩󰁶󰁥 󰁐󰁯󰁴󰁥󰁮󰁴󰁩󰁡󰁬 󰁯󰁦 󰁴󰁨󰁥 󰁂󰁲󰁥󰁡󰁳󰁴 󰁡󰁮󰁤 󰁌󰁥󰁧 󰁍󰁥󰁡󰁴 󰁯󰁦 󰁂󰁲󰁯󰁩󰁬󰁥󰁲󰁳 Hae In Yong, Hyun Joo Kim, Samooel Jung, Dinesh D. Jayasena,Young Sik Bae, Soo Kee Lee, and Cheorun Jo *  Department of Animal Science and Biotechnology, Chungnam National University, Daejeon 305-764, Korea Abstract This study investigated the effect of wild grape ( Vitis coignetiae ) dietary supplementation on the antioxidative potentialand quality of the breast and leg meat of broilers. A total of 36 one-day-old male Cobb broiler chicks were obtained from a commercial hatchery, and randomly assigned to 9 pens with 4 birds per pen. Then, broilers were fed 3 different dietary sup-plementations, including 0%, 0.25%, or 0.5% wild grape, for 2 wks at the finishing period. After slaughtering, the total phe-nolic content, α , α '-diphenyl- β -picryl-hydrazyl (DPPH) radical scavenging activity, 2-thiobarbituric acid reactive substances(TBARS), and total cholesterol content of broiler breast and leg meat were measured. Higher total phenolic content wasrecorded in the leg meat of broilers fed the wild grape when compared with the control, while breast meat did not show anydifference. Dietary supplementation of 0.25% and 0.5% wild grape significantly increased DPPH radical scavenging activ-ity of both breast and leg meat. TBARS values of both breast and leg meat were decreased by supplementation of 0.5% wildgrape during storage when compared to the control, except for the leg meat at day 7. However, there was no significantdifference found in total cholesterol content in both breast and leg meat. The results indicate that the antioxidative potentialof broiler meat is improved by supplementing the diet with wild grape. Key words:  wild grape, antioxidative potential, lipid oxidation, total cholesterol content Introduction Since ancient times, meat has played a vital role in thehuman diet, mainly as an excellent source of protein withhigh biological value. In addition, meat and meat prod-ucts are important sources of fat, essential amino acids,minerals, and vitamins (Biesalski, 2005). Chicken meat iswell recognized as a nutritional and healthy animal food,due to its relatively low fat, calorie, and cholesterol con-tent, as well as its relatively high concentration of polyun-saturated fatty acids and protein content (Lee et al.,  2012;Liu et al. , 2012). However, oxidation in meat and meat products is a major problem in the meat industry (Kang et al. , 2012). Furthermore, chicken meat is more liable tolipid oxidation, and thereby to the development of “off-flavors,” because it contains higher levels of unsaturatedfatty acids compared to red meat. This issue presents amajor problem with respect to retaining the quality of chicken meat for longer periods of time.For this reason, antioxidants are added to fresh and pro-cessed meat to delay the onset of oxidative processes andloss of meat quality. In effect, antioxidants extend thestorage period of meat by inhibiting the initiation or prop-agation of oxidative chain reactions (Xiong et al. , 1993).In general, natural antioxidants are preferentially used inmany products in the food industry over synthetic antiox-idants, such as butylated hydroxytoluene (BHT) andbutylated hydroxyanisole (BHA), which may be carcino-genic to consumers (Branen, 1975; Huang et al. , 2011;Reishe et al. , 1998). Therefore, research in this field isnow primarily focused on natural antioxidants, whichultimately provide higher consumer acceptability, palat-ability, safety, and potential to improve the functionalaspects of meat (Brenes et al. , 2008; Jo et al. , 2009; Jung et al. , 2010). Recent studies have demonstrated the beneficial effectof plant srcinated phenolic compounds, which containantioxidant potential via redox properties, in addition tohaving several beneficial actions on human health (Cathe-rine et al. , 1997; Fraga et al. , 2010; Kafakaya, 2004).Grape and tea are of special interest as natural polyphenol *Corresponding author: Cheorun Jo, Department of AnimalScience and Biotechnology, Chungnam National University,Daejeon 305-764, Korea. Tel: 82-42-821-5774, Fax: 82-42-825-9754, E-mail: cheorun@cnu.ac.kr  ARTICLE  84 Korean J. Food Sci. An., Vol. 33, No. 1 (2013) antioxidants, due to their high phenolic compound con-tent (Banon et al. , 2007). These polyphenols are wellknown for their beneficial functions, such as the inhibi-tion of lipid oxidation, cancer, or microbial growth, inaddition to the suppression of blood pressure or athero-sclerosis, prevention of diabetes, and the reduction of allergenicity (Byun et al. , 2004; Catherine et al. , 1996;Fraga et al. , 2010; Mazza, 1998). Furthermore, the anti-oxidant potential of grape polyphenols has been con-firmed in studies conducted using fish oil, frozen fish,cooked pork patties, and cooked turkey stored under retaildisplay conditions (Banon et al. , 2007). Previous studieshave demonstrated that the negative outcome of lipid oxi-dation in chicken meat may be reduced by supplementingthe diet of live chicken with antioxidants, such as medic-inal herb mix and grape pomace (Jung et al. , 2010).Wild grape ( Vitis coignetiae ) is considered to be a richsource of mineral, dietary fiber, organic acids, water-sol-uble vitamins, and phenolic compounds, including resver-atrol, epicatechin, catechin, procianidin, and anthocyanin(Cheon, 1999; Jeong et al. , 2007; Kim et al. , 2006). In astudy conducted by Yoon and Kim (2007) on total phenoliccompounds and antioxidant activity of fruits (includingstrawberry, kiwi, apple, and wild grape), wild grape con-tained the highest amount of phenolic compounds, andexhibited over twice the antioxidant activity of a grapecultivar ( Vitis labrusca ). In addition, feeding fermentedwild grape by-products to pigs decreased the 2-thiobarbi-turic acid-reactive substances   (TBARS) values and cho-lesterol content of pork, as well as increasing its color,taste, flavor, and juiciness (Park and Jung, 2005). Won(2009) reported that wild grape juice increased the anti-oxidative activity of the blood and liver of rats that werefed high oxidized lipids. Furthermore, Yong et al.  (2012)recently reported an improvement in the quality and fresh-ness of eggs from layers that were fed wild grape powder.Thus, the objective of this study was to investigate theeffect of providing wild grape as a dietary supplement onthe antioxidative potential of broiler breast and leg meat. Materials and Methods Preparation of animals and samples A total of 36 one-day-old male Cobb broiler chicks(Cobb strain) were obtained from a commercial hatchery,and randomly assigned to 9 pens with 4 birds per pen.During the entire experiment, broilers were housed under24 h fluorescent lighting, standard temperature, humidity,and ventilation conditions, and had ad libitum  access towater and food. The broiler chicks were fed a commercialbroiler starter diet (0-6 d), then, fed grower diets (7-21 d).At the end of week 3, broilers were reassigned to 3 differ-ent dietary treatments, and reared for a further 2 wks.Each treatment had 3 replicates, with 4 broilers in eachreplicate (total n = 36). Dietary treatments consisted of acontrol (commercial finisher diet with no supplementa-tion), and finisher diets supplemented with 0.25% (WG-0.25), and 0.5% wild grape powder (WG-0.5), respec-tively.At the end of the feeding trial, broilers from each penwere slaughtered, and the feathers and entrails (eviscera-tion) were removed from the carcasses. Breast and legmeat were then dissected from each carcass, vacuum packaged, and stored in a deep freezer at -50 o C until theanalysis. Measurement of antioxidative activity The meat samples (3 g) were homogenized (T25b, IkaWorks (Asia), Sdn, Bhd, Malaysia) in 15 mL of distilledwater at 16,000 rpm for 20 s. The samples were centri-fuged (Union 32R, Hanil Co., Ltd., Korea) at 3,000 rpmfor 10 min, and then filtered through Whatman No. 1 fil-ter paper (Whatman Ltd., England). Chloroform (10 mL)was added to the homogenates to remove fat, and themixture was shaken 3 times. The mixture was then sepa-rated into lipids and aqueous supernatant by centrifuga-tion (Union 32R, Hanil Co., Ltd., Korea) at 3,000 rpm for10 min. The supernatant was used for the analysis of total phenolic content and α , α '-diphenyl- β -picryl-hydrazyl(DPPH) radical scavenging activity. Total phenolic content Total phenolic content was measured using the Folin-Ciocalteu method (Subramanian et al. , 1965). A 0.1-mLaliquot was added to 0.2 mL Folin-Ciocalteu reagent andallowed to react for 1 min. Sodium carbonate (5%, 3 mL)was added to the mixture and vortexed. The mixture wasthen incubated at 23 o C in the dark for 2 h. The absor-bance was measured using a spectrophotometer (DU 530,Beckman Instruments Inc., USA) at 765 nm. The natural phenolics were quantified using a standard curve gener-ated for gallic acid, and were expressed as gallic acidequivalents. DPPH radical scavenging activity DPPH radical scavenging activity was estimated ac-cording to the method described by Jung et al.  (2010). A0.2-mL aliquot was mixed with 0.8 mL distilled water   Antioxidative Potential of Wild Grape on Broiler Meat  85 and 1 mL of 0.2 mM methanolic DPPH solution. For thecontrol, the aliquot solution (0.2 mL) was replaced withdistilled water. The mixture was vortexed and maintainedat room temperature for 30 min. The absorbance of thesolution was measured using a spectrophotometer (Beck-man Instruments Inc., USA) at 517 nm. The percentage of DPPH radical scavenging was obtained from the followingequation:DPPH radical scavenging activity=[1  − (absorbance of sample/absorbance of control)]×100 2-Thiobarbituric acid-reactive substances (TBARS)value TBARS values of meat samples were analyzed afterstorage at 4 o C for 0, 3, and 7 d, according to the methodof Jung et al  . (2011). Nine milliliters distilled water and50 µ L BHT (7.2% in ethanol) were added to each meatsample (3 g). The mixture was homogenized (T25b, IkaWorks (Asia), Sdn, Bhd, Malaysia) at 16,000 rpm for 20s. The homogenate (1 mL) was transferred to a test tube,and then thiobarburic acid (TBA)/trichloroacetic acid(TCA) solution (20 mM TBA in 15% TCA, 2 mL) wasadded. The test tubes were heated in a water bath at 90 o Cfor 15 min, cooled in cold water, and then centrifuged(Union 32R, Hanil Co., Ltd., Korea) at 3,000 rpm for 10min. The absorbance of the supernatant was measuredusing a spectrophotometer (Beckman Instruments Inc.) at532 nm. TBARS values were reported as mg malondial-dehyde per kg meat. Cholesterol content Meat samples (1 g) were mixed with 20 mL Folch solu-tion (chloroform:methanol = 2:1), and separated into 2layers by centrifugation (Union 32R, Hanil Co., Ltd.,Korea) at 3,100 rpm for 5 min. The chloroform layer con-taining total lipids was dehydrated using anhydrous Na 2 SO 4 , and the resulting solution was evaporated usingnitrogen. Subsequently, 2 mL of 2 N ethanolic KOH wasadded to the sample, which was then placed in a 90 o Cwater bath for 15 min for saponification. The aliquot wasthen cooled in cold water, and 1 mL of distilled water wasadded. Cholesterol in unsaponifiable fractions was extracted3 times using 1 mL hexane. The resulting hexane aliquotwas dried up to 1.5 mL using nitrogen, dehydrated usinganhydrous Na 2 SO 4 , and injected into a gas chromato-graph (GC-17A, Simazu, Japan). 5 α -Cholestane (Sigma-Aldrich) was used as an internal standard. A split inlet(split ratio, 50:1) was used to inject the samples into aHP-5 capillary column (30m  × 0.25mm  × 0.25  µ m), anda ramped oven temperature was used (200 o C for 5 min,increased to 300 o C at 10 o C/min). The injector tempera-ture was 270 o C, and the flame ionization detector temper-ature was 300 o C. N 2  served as the carrier gas at a constantflow rate of 2.0 mL/min. Statistical analysis Statistical analysis was performed using one-way anal- ysis of variance (ANOVA). Differences among the meanwere determined using Duncan’s multiple range test withthe significance defined as  p <0.05. Results and Discussion Antioxidative activity and lipid oxidation The total phenolic content of WG-0.5 was 0.75 mg/gfor broiler leg meat, which was significantly higher com- pared to the other treatments (Table 1). The breast meatexhibited higher total phenolic content (1.13-1.14 mg/g)compared to the leg meat (0.69-0.75 mg/g), which wasdue to the low fat content of breast meat compared to legmeat (Jo et al. , 2009). However, no significant differencein the total phenolic content of breast meat was foundamong the 3 treatments. These results indicate that WG-0.5 increases the antioxidative activity of broiler leg meat.To evaluate the antioxidative effect of wild grape onbroiler meat, DPPH radical scavenging activity was deter-mined (Table 2). The breast and leg meat of broilers fedWG-0.25 and WG-0.5 produced significantly higher DPPHvalues compared to the control. This finding indicates theutility of wild grape as a dietary supplement in whichelectron donors neutralize free radicals.Table 3 shows the TBARS values of the breast and legmeat of broilers fed wild grape dietary supplements after Table 1.Total phenolic contents (mg/g) of the meat frombroilers fed wild grape Treatment 1) Breast meatLeg meatControl1.130.69 b WG-0.251.130.66 b WG-0.51.140.75 a SEM 2) 0.0140.013 1) Control, commercial finisher diet; WG-0.25, finisher diet withdietary supplementation of 0.25% wild grape; WG-0.5, finisherdiet with dietary supplementation of 0.5% wild grape 2) Standard error of means (n=9) a,b Means with different letters within the same column differ sig-nificantly (  p <0.05).  86 Korean J. Food Sci. An., Vol. 33, No. 1 (2013) storage at 4 o C for 0, 3, and 7 d at 4 o C. Generally, TBARSvalues increased with storage time, due to the auto-oxida-tion of fat in the presence of oxygen. During the entirestorage period, the TBARS value of the breast meat frombroilers fed WG-0.5 was significantly lower compared tothe other 2 treatments. The leg meat from the broilers fedWG-0.25 and WG-0.5 exhibited significantly lower TBARSvalues compared to the control during initial stage of stor-age. After 3 d of storage, the lowest (  p <0.05) TBARS valuewas exhibited by leg meat from the WG-0.5 treatment.However, there was no significant difference amongtreatments for TBARS values of the leg meat after 7 d of storage. The WG-0.5 treatment was the most effective at preventing lipid oxidation, except for leg meat stored for7 d.The presence of polyphenols in meat is closely relatedto total antioxidant capacity (Prasad et al. , 2009). Forinstance, broilers fed a dietary medicinal herb extract mixexhibited higher total phenols and DPPH values at day 0of storage compared to the control, indicating that theantioxidant activity of medicinal plants is transferred tobroilers (Jang et al. , 2008; Jo et al. , 2009). Furthermore,the dietary supplementation of grape pomace was shownto improve antioxidant activity in chicken (Goni et al. ,2007).Dietary phenolic sources, such as fermented wild grape,grape seed extract, and grape pomace also decrease TBARSvalues in pork, lamb meat, and chicken (Goni et al. ,2007; Jeronimo et al. , 2012; Park and Jung, 2005), withthese results also being supported by the present study.This is because polyphenols donate hydrogen and elec-trons to free radicals, which results in oxidative chainreactions delaying lipid oxidation (Fraga et al. , 2010).Another reason why lipid oxidation is inhibited is relatedto corticosterone causing a decline in oxidative stress(Ohtsuka et al. , 1998). Grape leaf extract and tea poly- phenol have been reported to induce oxidative stress inrats and broilers, with broilers exhibiting low TBARSvalues compared to the control (Eid et al. , 2003; Pari andSuresh, 2008).The results of this study indicate that the dietary sup- plementation of wild grape might enhance antioxidantactivity and delay lipid oxidation in broiler meat. Cholesterol content Cholesterol is an important component of human cellmembranes; however, foods with high cholesterol con-tests might lead to cardiovascular diseases (Kang andSong, 1997; Park and Jung, 2005). Cholesterol is synthe-sized in the liver through acetyl-CoA, 3-hydroxy-3-meth- ylglutaryl coenzyme A (HMG-CoA), mevalonate, squalene,lanosterol, and over 30 intermediate substances, to main-tain blood cholesterol concentrations (Kim. 1992; Park et al. , 1997). It has been reported that dietary fiber, vitaminC, and polyphenols including catechin and quercetininhibit the synthesis of cholesterol or increase the extrac-tion of bile acid, which is the only pathway for choles-terol excretion (Kang and Song, 1997; Kwon et al. , 1993;Paolisso et al. , 1995; Yokota et al. , 1996). Fermentedwild gape by-product, Eosungcho powder, and onion peelcontain large amounts of antioxidants, which have beenshown to decrease the cholesterol content of pork meat bydelaying lipid absorption (Joo et al. , 1999; Kang et al. ,2006; Park and Jung, 2005). However, the cholesterol Table 2.  α , α '-Diphenyl- β -picryl-hydrazyl radical scavengingactivity (%) of the meat from broilers fed wild grape Treatment 1) Breast meatLeg meatControl15.63 b 23.66 b WG-0.2519.51 a 27.74 a WG-0.518.60 a 27.95 a SEM 2) 0.4380.947 1) Control, commercial finisher diet; WG-0.25, finisher diet withdietary supplementation of 0.25% wild grape; WG-0.5, finisherdiet with dietary supplementation of 0.5% wild grape 2) Standard error of means (n=9) a,b Means with different letters within the same column differ sig-nificantly (  p <0.05). Table 3.2-Thiobarbituric acid reactive substances (mg mal-ondialdehyde/kg meat) values of meat from broilersfed wild grape Treatment 1) Storage (d)037SEM 2) Breast meatControl0.39 cx 0.52 bx 0.65 ax 0.011WG-0.250.38 cx 0.48 bxy 0.62 ax 0.025WG-0.50.30 by 0.43 ay 0.44 ay 0.010SEM 2) 0.0100.0160.022Leg meatControl0.55 cx 0.82 bx 0.88 ax 0.012WG-0.250.40 by 0.82 ax 0.88 ax 0.071WG-0.50.38 cy 0.52 by 0.75 ax 0.025SEM 2) 0.0120.0610.044 1) Control, commercial finisher diet; WG-0.25, finisher diet withdie]tary supplementation of 0.25% wild grape; WG-0.5, finisherdiet with dietary supplementation of 0.5% wild grape 2) Standard error of means (n=9) a-c Means with different letters within the same row differ signifi-cantly (  p <0.05). x,y Means with different letters within the same column differ sig-nificantly (  p <0.05).   Antioxidative Potential of Wild Grape on Broiler Meat  87 content of breast and leg meat was not significantlyaffected by wild grape dietary supplementation (Table 4).Similar findings to our study have been reported for greentea by-products, wild grape juice, and wild grape, whichwere found to have no effect on the cholesterol content of chicken, blood cholesterol content of rats fed high oxi-dized lipid, or chicken eggs (Yang et al. 2003; Yong et al  ., 2012; Won , 2009).The extraction of bile acid contributes towards reducingthe amount of cholesterol in the body. However, this effectis not entirely related to the reabsorption of bile acids.Triglycerides, cholesterol, and other nutritional ingredi-ents also have an additional effect (Kang and Song, 1997).Hence, further studies are required to better understandthe synthesis of cholesterol and the factors that influencethe cholesterol content of broiler meat. In conclusion, the present study demonstrated the bio-availability of wild grape as an antioxidative dietarysource for broilers. Acknowledgement  This work was supported by a grant from the Next-Generation BioGreen 21 Program (No. PJ0081330), RuralDevelopment Administration, Republic of Korea. References 1.Banon, S., Diaz, P., Rodriguez, M., Garrido, M. D., and Price,A. (2007) Ascorbate, green tea and grape seed extracts increasethe shelf life of low sulphite beef patties.  Meat Sci.   77 , 626-633. 2.Biesalski, H. K. 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(1996) Struc-ture-Antioxidant activity relations of flavonoids and phe-nolic acids.  Free Radical Biol. Med  . 20 , 933-956.8.Cheon, K. B. (1999) Screening of antioxidant from Vitis Coi- gnetae, Vitis Vinifera L. and comparison of its antioxidantactivity. MS Thesis. Kon-Kuk University, Seoul. 9.Eid, Y. Z., Ohtsuka, A., and Hayashi, K. (2003) Tea polyphe-nols reduce glucocorticoid-induced growth inhibition andoxidative stress in broiler chickens.  Br. Poult. Sci.   44 , 127-132.10.Fraga, C. G., Galleano, M., Verstraeten, S. V., and Oteiza. P.I. (2010). Basic biochemical mechanisms behind the healthbenefits of polyphenols.  Mol. Aspects Med. 31 , 435-445.11.Goni. I., Brenes, A., Centeno, C., Viveros, A., Saura-Calixto,F., Rebole, A., Arija, I., and Estevez, R. (2007) Effect of dietary grape pomace and vitamin E on growth performance,nutrient digestibility, and susceptibility to meat lipid oxida-tion in chickens.  Poultry Sci.   86 , 508-516.12.Huang, B., He, J., Ban, X., Zeng, H., Yao, X., and Wang, Y.(2011) Antioxidant activity of bovine and porcine meattreated with extracts from edible lotus (  Nelumbo nucifera )rhizome knot and leaf.  Meat Sci.   87 , 46-53.13.Jang, A., Liu, X. D., Shin, M. H., Lee, B. D., Lee, S. K., Lee,J. H., and Jo. C (2008) Antioxidative potential of raw breastmeat from broiler chicks fed a dietary medicinal herb extractmix.  Poultry Sci.   87 , 2382-2389.14.Jeong, H. J., Park, S. B., Kim, S., and Kim, H. K. (2007)Total polyphenol content and antioxidative activity of wildgrape ( Vitis coignetiae ) extracts depending on ethanol con-centrations . J. Korean Soc. Food. Sci. Nutr.   36 , 1491-1496.15.Jeronimo, E., Alfaia, C. M. M., Alves, S. P., Dentinho, M. T.P., Prates, J. A. 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(2010) Effect of dietary mixture of gallic acid and linoleic Table 4.Total cholesterol contents (mg/g) of the meat frombroilers fed wild grape Treatment 1) Breast meatLeg meatControl0.501.33WG-0.250.371.27WG-0.50.361.34SEM 2) 0.0340.078 1) Control, commercial finisher diet; WG-0.25, finisher diet withdietary supplementation of 0.25% wild grape; WG-0.5, finisherdiet with dietary supplementation of 0.5% wild grape 2) Standard error of means (n=9)
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