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Poult Sci 2008. 87:2382-2389. doi:10.3382/ps.2007-00506
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PROCESSING, PRODUCTS, AND FOOD SAFETY

Antioxidative Potential of Raw Breast Meat from Broiler Chicks Fed a Dietary Medicinal Herb Extract Mix

A. Jang*,{dagger}, X.-D. Liu{dagger}, M.-H. Shin{dagger}, B.-D. Lee{dagger}, S.-K. Lee{dagger}, J.-H. Lee{dagger} and C. Jo{dagger},1

* Quality Control and Utilization of Animal Products Division, National Institute of Animal Science, RDA, Suwon, 441-706, Republic of Korea; and {dagger} Department of Animal Science and Biotechnology, Chungnam National University, Daejeon, 305-764, Republic of Korea

1 Corresponding author: cheorun{at}cnu.ac.kr


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
This study was performed to evaluate the antioxidative potential and quality of the breast meat of broiler chickens fed a dietary medicinal herb extract mix (MHEM, consisting of mulberry leaf, Japanese honeysuckle, and goldthread at a ratio of 48.5:48.5:3.0). A total of 480 one-day-old male Cobb broiler chicks were randomly allotted to 12 pens, with 40 birds per pen (replicate), and reared for 35 d. Dietary treatments consisted of a corn-soybean meal basal diet (control); a basal diet with 0.3% MHEM (T1); and a basal diet with 1% (T2) MHEM. At the end of the feeding trial, breast meat samples were excised and stored in a refrigerator at 4°C to be analyzed at d 0, 3, and 7. The MHEM did not affect proximate composition of the breast meat. Total phenols content of the breast meats in the T1 and T2 diets was approximately 2 times greater than that of the control diet (P < 0.05). 1,1-Diphenyl-2-picrylhy-drazyl radical-scavenging activity and 2,2-azinobis-(3 ethylbenzothiazoline-6-sulfonic acid) cation-reduction activity were greater in the T2 diet at d 0 and in the T1 diet at d 3 compared with the control diet (P < 0.05). 2-Thiobarbituric acid-reactive substance values in the T1 and T2 diets were lower than in the control diet at d 3 and 7 and did not increase during storage, whereas the value in the control diet increased significantly. The pH of the T1 diet was significantly greater than that of the control diet at d 0 and 3. In a sensory test, panelists preferred the T1 breast meat throughout the 7-d storage period. This research indicates that dietary MHEM could increase the antioxidative potential and overall preference of breast meat during cold storage.

Key Words: medicinal herb extract mix • antioxidative potential • breast meat quality


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
Recently, the use of antibiotics for broilers has been limited to only 4 antibiotics in the European Union (Hernández et al., 2004). As a result, numerous medicinal herbs have been suggested to livestock producers as alternatives to antibiotic growth promoters. Several researchers have reported the possibility of growth-promoting and antioxidative effects for some traditional medicinal herbs (Park and Yoo, 1999; Liu et al., 2006). These medicinal herbs are considered to be natural products, so consumers may willingly allow them to be included in livestock feeds.

Wood and Enser (1997) recommended the use of dietary antioxidants to reduce lipid peroxidation in the feed and animal, and to preserve product quality. Recent research on antioxidants has focused on naturally occurring molecules to eliminate consumers’ concerns about the safety and toxicity of the synthetic counterparts. In this respect, herbs and their extracts with antioxidant capacity are being tested to improve animal performance and the quality and shelf life of meat products therefrom (Lopez-Bote et al., 1998; Simitzis et al., 2008; Vichi et al., 2001).

Goldthread (Coptis chinensis) is one of the famous traditional medicinal herbs because of its significant functions of antibiosis. Berberine, the major active component in goldthread, is an isoquinoline derivative alkaloid and is widely used in the treatment of calf diarrhea and in the clinical treatment of diabetes (Liu et al., 2005). In addition, mulberry leaf (Morus alba L.) is widely cultivated in the Far East and has been reported to have many biological activities, such as antioxidant (Kim et al., 1999), antimicrobial (Nomura et al., 1978), antifungal (Takasuki et al., 1982), antiallergic (Lee et al., 1998), and hypoglycemic activities (Hikino et al., 1985). Furthermore, Japanese honeysuckle (Lonicera flos) has been used as a folk remedy for antiinflammation and as an antidote for liver diseases. The major bioactive compounds of Japanese honeysuckle are luteolin, inositol, saponin, tannin, ginnol, and glycoside (Suh et al., 2005).

These medicinal herbs are good sources of polyphenols, which are widely distributed in plants and exhibit various antioxidant properties (Salah et al., 1995; Gladine et al., 2007). From a medical point of view, polyphenolic compounds have great importance against coronary heart disease and exhibit antioxidant and antitumor properties (Gronbaek et al., 1995; Knekt et al., 2002). These biological functions are assumed to result from the radical-scavenging properties of polyphenolic compounds (Wang and Huang, 2004). In our laboratory, we investigated the effect of a dietary medicinal herb extract mix (MHEM) from mulberry leaf, Japanese honeysuckle, and goldthread on the antioxidative potential and quality of chicken breast meat during cold storage.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 REFERENCES
 
Preparation of Medicinal Herb Extract

Mulberry leaf, Japanese honeysuckle, and goldthread were purchased from the Kyung-dong herbal market (Seoul, Korea). The herbs were chopped and pulverized to pass 100 mesh (2 mm). An extract of the medicinal herb was prepared with 75% methanol as described in Figure 1Go. Briefly, 100 kg of each powdered medicinal herb was extracted overnight with 200 L of 75% methanol by using a large-scale extractor (CoBiotech, Seoul, Korea) at room temperature. Each extract was filtered 2 to 3 times with cheesecloth, and the filtrate was concentrated by a rotary evaporator under vacuum. Each concentrate of mulberry leaf, Japanese honeysuckle, and goldthread was redissolved in 1 L of 75% ethanol and mixed at a ratio of 48.5:48.5:3.0, evaporated, freeze-dried, and used as MHEM for the broiler diets (Figure 1Go). This ratio was determined by the cost and the recommendation of the traditional medical doctor for future industrial application.


Figure 1
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  		Figure 1. Preparation procedure of the medicinal herb extract mix. RT = room temperature.

 
Birds and Diets

A total of 480 one-day-old male Cobb broiler chicks were obtained from a local hatchery and randomly allotted to 12 pens (3.0 x1.0 m), with 40 birds per pen (replicate), and reared for 35 d. Dietary treatments consist of a corn-soybean meal basal diet (control), a basal diet with 0.3% MHEM (T1), and a basal diet with 1% MHEM (T2). The birds were fed experimental starter diets (3,100 kcal of ME/kg and 21.0% CP) until 21 d of age and grower diets (3,100 kcal of ME/kg and 19.0% CP) until 35 d of age (Table 1Go). At the end of the feeding trial, 3 chicks from each pen (12 chicks per treatment) were killed by cervical dislocation, and breast meat samples were excised and stored in a refrigerator (4°C). The antioxidative potential and various meat quality characteristics were analyzed on storage d 0, 3, and 7, respectively.


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  		Table 1. Composition of broiler starter and grower diets
 
Proximate Analysis

The moisture (method 942.05), crude fat (method 920.39), CP (method 954.01), crude ash (method 942.05), and crude fiber (method 973.18) composition of the breast meat was determined according to AOAC (1999) methods.

Measurement of Antioxidative Potential

Total Phenols Content. Each breast meat sample (5 g) in distilled water (15 mL) was homogenized at 996 x g for 2 min. Chloroform (9 mL) was added to the homogenates and the mixture was shaken vigorously 2 to 3 times to separate the lipids. Total phenols content in the aqueous supernatant was estimated by the Folin-Ciocalteu method (Subramanian et al., 1965). A 1-mL aliquot of diluted sample (1:4, vol/vol) was added to the Folin-Ciocalteu reagent (500 µL), followed by addition of 1 mL of sodium carbonate solution (10%). The reaction mixture was vortexed and the absorbance was measured with a spectrophotometer (UV 1600 PC, Shimadzu, Tokyo, Japan) at 700 nm after incubation for 1 h at room temperature. Quantification was done based on the standard curve generated with gallic acid.

1,1-Diphenyl-2-Picrylhydrazyl Radical-Scavenging Assay. 1,1-Diphenyl-2-picrylhydrazyl (DPPH) radical-scavenging activity was estimated with the aqueous supernatant obtained from breast meat according to the method of Blois (1958), with slight modifications. A 200-µL quantity of diluted aqueous supernatant (1%) was added to 800 µL of water and 1 mL of methanolic DPPH solution (0.2 mM). The mixture was vortexed and left to stand at room temperature for 30 min. A tube containing 1 mL of distilled water and 1 mL of methanolic DPPH solution (0.2 mM) served as the control. The absorbance of the solution was measured at 517 nm (UV 1600 PC, Shimadzu). The percentage of DPPH radical scavenging was obtained from the following equation:


Formula

2,2-Azinobis-(3 Ethylbenzothiazoline-6-Sulfonic Acid)-Reducing Activity. 2,2-Azinobis-(3 ethylbenzo-thiazoline-6-sulfonic acid) (ABTS+)-reducing activity was determined following the adapted Trolox-equivalent antioxidant capacity assay as described by Re et al. (1999). 2,2-Azinobis-(3 ethylbenzothiazoline-6-sulfonic acid) was produced by reacting 14 mM ABTS with an equal volume of 4.9 mM potassium persulfate (final concentration: 7 mM ABTS in 2.45 mM potassium persulfate). The mixture was incubated in the dark at room temperature for 12 to 16 h before use. The ABTS+ solution was diluted with 5.5 mM PBS (pH 7.4) to an absorbance of 0.70 ± 0.02 at 734 nm (Sigma Argentina SA, Buenos Aires, Argentina) and equilibrated at 30°C. A 10-µL aliquot of homogenate prepared as described for DPPH or the Trolox standard (0, 0.3, 0.7, 0.9, and 1.2 mM in PBS (Fluka Chemie GmbH, Buchs, Switzerland) was added to 1 mL of the diluted ABTS+ solution, and the absorbance was read at 30°C exactly 6 min after the initial mixing. The percentage inhibition of the blank absorbance (0.70 ± 0.02) was calculated for each Trolox standard and sample, respectively.

2-Thiobarbituric Acid-Reactive Substances. Each meat sample (5 g) from various storage periods was homogenized in 15 mL of distilled water. Sample homogenate (5 mL) was transferred to a test tube and lipid oxidation was determined as the 2-thiobarbituric acid-reactive substance (TBARS) value by using the method described by Ahn et al. (1999). Briefly, 50 µL of butylated hydroxyanisol (7.2%) and 5 mL of TBA-trichloroacetic acid solution (20 mM TBA in 15% trichloroacetic acid) were added to the test tube. Tubes were heated in a boiling water bath for 15 min, cooled, and then centrifuged at 966 x g for 15 min. Absorbance of the supernatant was measured at 532 nm with a spectrophotometer (UV 1600 PC, Shimadzu). The increase in absorbance at 532 nm was taken into consideration to calculate the TBARS values. Lipid oxidation was reported as milligrams of malondialdehyde per kilogram of meat.

Physical Analyses

pH. The pH of the breast meat was determined by homogenizing 5 g of meat with 25 mL of distilled water. The homogenates were filtered, and the pH of each sample was measured with a pH meter at room temperature.

Water-Holding Capacity. One gram of minced breast meat sample was placed on a round plastic plate with small holes. The plate with meat sample on it was then fitted into a 2-mL plastic tube. This tube was centrifuged at 920 x g for 10 min. The released water content was measured and calculated as a percentage of the initial weight.

Color. The lightness (L*), redness (a*), and yellowness (b*) of breast meat was measured with a Minolta Chroma Meter CR-300 (Minolta Inc., Tokyo, Japan). The instrument was calibrated with a white-and-black tile before analysis. Measurements were done perpendicularly to the meat surface at 3 different locations per breast with a medium-sized aperture, and the mean value from each meat was used.

Sensory Evaluation

Air-packed breast meat stored at 4°C was boiled (100°C, 20 min) and cooled at room temperature for 10 min. Twelve semitrained panelists, who had at least 1 yr of experience in the sensory analysis of different meat and poultry products, consisting mainly of graduate students (7 males and 5 females) were served diced (2 x 2 x 2 cm) chicken breast with water and an unsalted snack in between to remove the remaining flavor. The panelists were requested to evaluate the cooked breast meat (offered in a randomized order) with a 3-digit code for color, odor, taste, texture, and overall acceptability, on a 9-point hedonic scale (1 = dislike extremely; 5 = neither like nor dislike; 9 = like extremely).

Statistical Analysis

A GLM procedure was performed (SAS Institute, 2000) and the differences among the mean values were tested by the Student-Newman-Keuls multiple-range test when a significant difference was detected at P < 0.05. Mean values and SEM are reported.


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
REFERENCES
 
Antioxidative Potential of Breast Meat

As shown in Table 2Go, supplementation with MHEM did not affect the proximate composition of breast meat. The total phenols content of breast meat was in the range of 48.82 to 99.26 mg of gallic acid equivalent/kg of meat at d 0 of storage. The breast from chickens fed the MHEM supplement (T1 and T2 diets) showed significantly greater total phenols content than the breast of chickens fed the control diet at d 0 (Table 2Go), indicating that the antioxidative activity in the breast meat of broiler chickens can be increased by dietary MHEM.


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  		Table 2. Proximate composition (%) and total phenols content (µg/g) of raw breast meat from chickens fed a dietary medicinal herb extract mix (MHEM) for 35 d
 
To estimate the efficiency of MHEM as an antioxidant, the stable free radical DPPH has been in common use. The free radical-scavenging effect of breast meat from broilers fed MHEM was significantly increased at d 0 (Table 3Go). The DPPH-scavenging effect of the T2 diet was 1.79 times greater (P < 0.05) than that of the control diet. The breast meat of chickens fed the T1 diet showed significantly greater ABTS+-scavenging activity than that of chickens fed the control diet at d 3; however, no significant difference was found between control and T2 breast meat in this respect. 2-Thiobarbituric acid-reactive substance values of T1 and T2 breast meat were lower than that of control breast meat at d 3 and 7 (Table 3Go). In addition, dietary MHEM appeared to delay the lipid oxidation of broiler chicken breast meat, because the TBARS values of T1 and T2 breast meat did not increase significantly during storage, whereas that of control breast meat increased significantly.


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  		Table 3. 1,1-Diphenyl-2-picrylhydrazyl (DPPH)-scavenging activity (%),2,2-azinobis-(3 ethylbenzothiazo-line-6-sulfonic acid) (ABTS+)-reducing activity (%), and changes in 2-thiobarbituric acid reactive substance (TBARS) of raw breast meat from chickens fed a dietary medicinal herb extract mix (MHEM) for 35 d
 
Some spices and herbs contain several compounds, mainly polypehnols, that have antioxidant activities, so they can extend the shelf life and improve the quality of meat products (Farag et al., 1989; Liu et al., 1992; Botsoglou et al., 2002). Phenolic compounds present in natural plant oils react with lipid and hydroxyl radicals and convert them into stable products (Yanishlieva-Maslarova, 2001). Simitzis et al. (2008) reported that phenolic compounds in oregano essential oil were absorbed and entered the systemic circulatory system after ingestion and had significant antioxidant activities in lamb meat. Dietary administration of rosemary and sage essential oil extract to broilers resulted in a decrease in the lipid and cholesterol oxidation of broiler meat during storage for 9 d (Lopez-Bote et al., 1998). Supplementing turkeys with oregano extract increased the oxidative stability and retention of {alpha}-tocopherol in long-term frozen-stored turkey meat (Botsoglou et al., 2003). In the present study, we tried to determine the accumulated amount of the phenolic components berberine (the dominant phenolic compound in gold-thread) and luteolin (the dominant phenolic compound in Japanese honeysuckle) in the breast meat by HPLC (data not shown), but neither berberine nor luteolin was detected. It is still unclear whether the antioxidants consumed can be incorporated into fatty tissues in the same form as when the fat is stabilized in vitro (Vichi et al., 2001). However, the total phenols content of breast meat from chickens fed MHEM (T1 and T2 diets) was significantly greater than that of chickens fed the control diet (Table 2Go). This result indicated that phenolic compounds from MHEM could prevent breast meat from oxidizing. However, other compounds or mechanisms may be responsible for this antioxidant activity.

Physical Aspects of Breast Meat

The pH was significantly greater in T1 and T2 breast meat than in control breast meat at d 0 and 3 (Table 4Go). This pH difference disappeared at d 7. No significant difference was found in the water-holding capacity (WHC) of breast meat during storage (Table 4Go). Generally, meat with high pH has a high WHC, although this was not proven to be so in this study.


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  		Table 4. Change in pH and water-holding capacity of raw breast meat during cold storage from chickens fed a dietary medicinal herb extract mix (MHEM) for 35 d
 
Dietary MHEM decreased the L* value of breast meat during cold storage (Table 5Go), and at d 3, this decrease in the L* value was significant. Additionally, there was no significant difference among treatments in the a* values of breast meat during storage. No consistent trend in the b* values of breast meat was found among treatments.


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  		Table 5. Color change of raw breast meat from chickens fed a dietary medicinal herb extract mix (MHEM) for 35 d
 
Simitzis et al. (2008) reported that the pH of female lamb meat was increased (P < 0.05) after supplementation with dietary oregano essential oil. One explanation was that the greater pH of meat might have reflected different glycogen reserves preslaughter (Simitzis et al., 2008) because the nutritional treatment influenced muscle glycogen levels in cattle (Tudor et al., 1996). Similarly, dietary garlic increased the pH in pork (Chen et al., 2008). However, Park and Yoo (1999) reported that the dietary Chinese medicine by-products at levels of 4 and 8% decreased the pH of thigh muscle in broiler chicks.

Dietary MHEM resulted in lower L* values of breast meat in our study at d 3 (Table 5Go). The lower L* values may be related to the high pH values. Dietary garlic decreased L*, a*, and b* values in pork (Chen et al., 2008) but dietary oregano extract showed greater a* and b* values in chicken meat than in the meat of control chickens (Young et al., 2003). Simitzis et al. (2008) explained that dietary oregano essential oil supplementation indirectly modifies the meat color, probably by decreasing hemoglobin oxidation and activating mechanisms that modify pigment distribution in animal tissues.

Sensory Evaluation

A color difference in breast meat among treatments was not found during storage (Table 6Go). However, the flavor of T1 and T2 breast meat was more favorable than that of control breast meat at d 3. The taste and texture of T1 breast meat were preferred to those of control and T2 breast meat at d 0 (P < 0.05). For those sensory parameters, panelists scored the T1 breast meat as more acceptable than the control and T2 breast meat during the whole storage period (P < 0.05). This result indicates that dietary MHEM at a 0.3% level could enhance the sensory quality of breast meat. There is limited information on the sensory quality of meat after dietary administration of medicinal herbs to animals. Simitzis et al. (2008) reported that dietary oregano essential oil did not influence the shear force and sarcomere length in lamb meat. Dietary garlic powder increased the WHC of pork, but no difference was found in color, marbling, and firmness by a sensory test.


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  		Table 6. Sensory properties of cooked breast meat from chickens fed a dietary medicinal herb extract mix (MHEM) for 35 d
 


   ACKNOWLEDGMENTS
 
This study was supported by Technology Development Program for Agriculture and Forestry, Ministry of Agriculture and Forestry (Suwon, Korea), and was partially supported by a Korea Science and Engineering Foundation grant (Daejeon, Korea) funded by the Korean government (no. R01-2007-000-10753-0).

Received for publication December 16, 2007. Accepted for publication June 24, 2008.


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 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
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