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Poult Sci 2008. 87:1287-1294. doi:10.3382/ps.2008-00023
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ENVIRONMENT, WELL-BEING, AND BEHAVIOR

Effects of Forsythia suspensa Extract on Growth Performance, Nutrient Digestibility, and Antioxidant Activities in Broiler Chickens Under High Ambient Temperature1

L. Wang*, X. L. Piao{dagger}, S. W. Kim*,{ddagger}, X. S. Piao*,2, Y. B. Shen* and H. S. Lee§

* China Agricultural University, State Key Laboratory of Animal Nutrition, Beijing 100094, China; {dagger} China Minority Traditional Medicine Center, Central University for Nationalities, Beijing 100081, China; {ddagger} Department of Animal Science, North Carolina State University, Raleigh 27695; and § National Veterinary Research and Quarantine Service, Anyang 430-824, Korea

2 Corresponding author: piaoxsh{at}mafic.ac.cn


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
A 42-d trial was conducted with 252 broiler chickens (d 1 of age, 38.8 ± 1.3 g of BW) to determine the effects of Forsythia suspensa extract on growth performance, nutrient digestibility, and antioxidant activities under high ambient temperature (32 ± 1°C). The feeding program consisted of a starter diet from d 1 to 21 of age and a finisher diet from d 22 to 42 of age. Dietary treatments included a negative control group (NC) fed a cornsoybean meal based diet without vitamin C or Forsythia suspensa extract, a positive control group fed a diet with 200 mg of vitamin C/kg, and a test group (FS) fed with 100 mg of Forsythia suspensa extract/kg. There were 14 cages per treatment and 6 birds per cage during the study. Birds had free access to diets and water during the entire period. Body weight and feed intake were measured at d 21 and 42. Blood and tissue samples were collected at d 21 and 42 for assay of antioxidant indices. Growth performance did not differ among treatment groups during the starter period. In the finisher phase, birds in FS had greater (P < 0.05) average daily gain, feed conversion, and apparent digestibility of energy, CP, calcium, and phosphorus than birds in NC. Furthermore, birds in FS had greater (P < 0.05) total antioxidant capacity and superoxide dismutase activity and lower (P < 0.05) malondialdehyde activity in the serum than birds in NC. The FS birds had greater (P < 0.05) muscle superoxide dismutase activity and lower (P < 0.05) malondialdehyde than NC birds. During the entire period, hepatic superoxide dismutase activity of FS birds was greater (P < 0.05) than that of NC birds. Dietary supplementation with Forsythia suspensa extract can enhance nutrient digestibility and growth performance possibly by reducing oxidative stress of broiler chickens under high ambient temperatures.

Key Words: Forsythia suspensa • performance • nutrient digestibility • antioxidant • broiler


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Body temperature and metabolism rate of birds are relatively high compared with mammals, which makes birds vulnerable to oxidative stress under high heat environments (Lindstedt and Calde, 1976; Kristal and Yu, 1992). Free radicals are metabolic by-products that potentially damage cell components such as lipids, protein, DNA, and carbohydrates (Payne and Southern, 2005; Zhao and Shen, 2005).

Reactive oxygen species (ROS) is a family of oxygen derivatives including superoxide, hydroxyl radical, hydrogen peroxide, and nitric oxide. In normal conditions, excessive oxidative radicals are eliminated by antioxidant systems including nonenzymatic components and series of antioxidant enzymes. Total antioxidant capacity (TAOC), superoxide dismutase (SOD) activity, and glutathione peroxidase (GSH-Px) activity are the main parameters to assess oxidative status (Wang et al., 2008). Degree of lipid peroxidation can also be used as an indicator of ROS-mediated damages (Kühn and Borchert, 2002). Contents of isolated malondialdehyde (MDA) in urine, blood, and tissues can generally be used as a biomarker for radical-induced damage and endogenous lipid peroxidation (Day, 1996; Wang et al., 2008). Determination of disappearance of free radicals such as 1,1-diphenyl-2-picryl-hydrazyl (DPPH) is a stable and rapid method to assess the antioxidant activity of plant extracts (Samarth et al., 2007).

High ambient temperature can cause major economic losses to the poultry industry by reducing feed intake and hatchability and by increasing mortality (Gursu et al., 2004; Ryder et al., 2004; Bartlett and Smith, 2003). To alleviate the adverse effects of high ambient temperature, antioxidants can be supplemented in feed (Pardue and Thaxton, 1984; Hussein, 1995). Recently, active components from herbal plants have been explored as possible antioxidants (Halvorsen et al., 2002; Dragland et al., 2003; Wang et al., 2008). Forsythia suspensa extract (FSE) is an herbal antioxidant shown to possess antipyretic, antioxidative, antidotal, and antiinflammatory activities (Schinella et al., 2001; Guo et al., 2006). However, the role of FSE as a dietary antioxidant source in broiler chicken has not been investigated. The objective of this study was to determine supplemental effects of FSE on growth performance, nutrient digestibility, and antioxidant system in broiler chickens.


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Extract Preparation from Forsythia suspensa

Forsythia suspensa is a climbing plant widely distributed in China, Japan, and Korea. In brief, dried fruits of Forsythia suspensa were ground to powder (100 g), extracted with 500 mL of 80% methanol, sonicated for 3 h, filtered, and extracted twice (500 mL each time). The filtrates were combined and dried by rotary vaporization (Büchi, Rotavapor R-124, Flawil, Switzerland).

Determination of DPPH Radical-Scavenging Activity

Free radical scavenging activity was determined by measuring DPPH content. Purified DPPH (Wako Pure Chemical Industries Ltd., Osaka, Japan) was used as a standard in the analysis. The level of oxidation was determined as described by Hatano et al. (1989) with minor modifications. Different concentrations of test samples including FSE and vitamin C (5, 10, 50, 100, and 250 µg/mL) were prepared. Briefly, 100 µL of FSE-ethanol solution sample, 100 µL of vitamin C-ethanol solution sample, or 100 µL of ethanol as the control were added to simple microwells, followed by the addition of 100 µL of DPPH (120 µmol) in ethanol. After gentle mixing and standing (30 min) at room temperature, the DPPH radical level was measured by a microplate reader (SPECTRAmax 340PC, Molecular Devices, Sunnyvale, CA) at 517 nm. The antioxidant activity was expressed as the inhibition rate of DPPH radical.

Inhibition rate of DPPH radical as a percentage (I%) was calculated as follows:


Formula

where A0 is the absorbance of the control reaction (containing all reagents except the test compound) and A1 is the absorbance of the test compound.

Experimental Birds

A total of 252 male broiler chickens (38.8 ± 1.3 g, Arbor Acres, 1 d old) were used in this study. All birds were housed in wire-floored cages in an environmentally controlled room with continuous light. The lighting regimen and ventilation were continuously monitored from d 1 to 42. The birds had access to feed and water ad libitum. During the experimental period, relative humidity was 44 ± 6%. The room temperature was maintained at 35°C for the first 3 d, after which the temperature was gradually reduced to 32°C, which was maintained during the 42-d experiment to generate high ambient temperature. All birds were inoculated with inactivated infectious bursa disease vaccine on d 14 and 21 and with Newcastle disease vaccine on d 7 and 28. The trial was conducted in 2 phases consisting of a starter phase from d 1 to 21 and a finisher phase from d 22 to 42. The animal care protocol in this experiment was approved by the Animal Welfare Committee of China Agricultural University.

Experimental Design and Diets

The broilers were randomly allotted to 1 of 3 dietary treatments (Table 1Go) including a negative control group (NC) fed a cornsoybean meal based diet without vitamin C and FSE; a positive control group (PC) fed a diet with 200 mg of vitamin C/kg of diet; and a test group (FS) fed with 100 mg of FSE/kg of diet. There were 14 cages per treatment with 6 birds per cage. All essential nutrients contained in the basal diet met or slightly exceeded nutrient requirements recommended by NRC (1994). All diets were fed in a mash form.


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Table 1. Composition of basal diets and nutrient levels1
 
Sampling and Sample Processing Procedure

Excreta from each cage were collected from d 19 to 21 and from d 40 to 42, weighed, and dried at 60°C for 72 h. The feed and dried excreta samples were ground to pass through a 40-mesh screen and mixed thoroughly before analysis. The DM, CP, calcium, and phosphorus contents were determined according to AOAC (1990), and gross energy content was measured by using an adiabatic bomb calorimeter (Model 1281, Parr, Moline, IL) to calculate CP retention and apparent nutrient digestibility.

On d 21 and 42, BW and feed intake were measured after a 12-h fast to determine average daily gain (ADG), average daily feed intake (ADFI), and feed conversion (FC). One bird per cage was randomly selected and killed for sampling. Blood was collected (5 mL) by cardiac puncture using a 10-mL anticoagulant-free Vacutainer tube (Greiner Bio-One GmbH, Kremsmunster, Austria), centrifuged at 3,000 x g for 10 min to obtain the serum, and stored at –20°C until analysis. Liver and muscle samples were obtained to measure TAOC, MDA, and antioxidant enzyme activity. The samples were taken immediately after killing, packed carefully, and then frozen by immersion in liquid N2 and stored at –70°C until analysis.

Assay of Antioxidant Indices in Serum, Liver, and Muscle

Assay kits for protein, TAOC, SOD, GSH-Px, and MDA were obtained from Nanjing Jiancheng Bioengineering Institute (Nanjing, China). For biochemical assays, liver and muscle tissues were homogenized in ice-cold isotonic physiological saline to form homogenates at the concentration of 0.1 g/mL. The samples were centrifuged. Then, the supernatants and sera already prepared were subjected to the measurement of TAOC, SOD, GSH-Px, and MDA levels by spectrophotometric methods using a spectrophotometer (Leng Guang SFZ1606017568, Shanghai, China). All of the assays followed the instructions of the kits. The TAOC was measured by the method of ferric reducing-antioxidant power assay (Benzie and Strain, 1996) and detected at 520 nm with the spectrophotometer. Activity of SOD was measured by the xanthine oxidase method, which monitors the inhibition of reduction of nitro blue tetrazolium by the sample (Winterbourn et al., 1975). Activity of GSH-Px was detected with 5,5'-dithiobis-p-nitrobenzoic acid, and the change of absorbance at 412 nm was monitored using a spectrophotometer (Hafeman et al., 1974). The MDA level was analyzed with 2-thiobarbituric acid, monitoring the change of absorbance at 532 nm with the spectrophotometer (Placer et al., 1996). Enzyme activity was expressed as units per milligram of protein for tissues and units per milliliter for serum.

Statistical Analysis

Data were subjected to ANOVA using the GLM procedure of SAS (SAS Institute, 1996). Pen was the experimental unit. Differences among treatments were separated by Duncan’s multiple range tests. Probability values less than 0.05 were considered significant.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
DPPH Radical-Scavenging Activity

Inhibition of DPPH radicals due to the scavenging ability of FSE and vitamin C is shown in Figure 1Go. The scavenging effect of FSE and vitamin C on DPPH radicals increased (P < 0.05) in a dose-dependent manner. The FSE exerted an inhibitory effect on DPPH radical generation, with 77.2% inhibition at 100 µg/mL and 81.3% inhibition at 250 µg/mL.


Figure 1
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Figure 1. 1,1-Diphenyl-2-picryl-hydrazyl (DPPH) scavenging activities of Forsythia suspensa extract (FSE) and vitamin C.

 
Growth Performance

In the starter phase, dietary supplementation of FSE and vitamin C did not affect ADG, ADFI, or FC of broiler chickens (Table 2Go). In the finisher phase, ADG of the FS group was greater (10.6%, P < 0.05) than that of the NC group, and the FC of the FS group was improved (6.3%, P < 0.05) compared with NC (Table 2Go). Compared with the PC group, the ADG of FS was increased (P < 0.01) by 4.3%, but ADFI and FC showed no differences in the finisher phase. For the overall period, the ADG of FS was 8.6 and 4.4% greater (P < 0.01) than the NC and PC groups, respectively. The FC of the FS group was 4.6% greater (P < 0.05) than that of the NC group.


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Table 2. Effects of dietary Forsythia suspensa extract (FSE) supplement on the growth performance of broilers
 
Apparent Digestibility

The results of the apparent digestibility of DM, energy, CP, calcium, and phosphorus are shown in Table 3Go. In both the starter and finishing phases, none of these parameters were changed except for the enhancement of energy, CP, calcium, and phosphorus in the finisher phase. Apparent digestibility of energy, CP, calcium, and phosphorus was greater (P < 0.05) in the FS group compared with the NC group, and apparent digestibility of CP and calcium was enhanced (P < 0.05) in the FS group compared with the PC group.


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Table 3. Effects of dietary Forsythia suspensa extract (FSE) supplement on the apparent digestibility (%) of DM, energy, calcium, and phosphorus and CP retention in broilers
 
Lipid Peroxidation and Antioxidant Enzyme Activities

The results of antioxidant indices in serum are shown in Table 4Go. In the starter phase, FS birds had greater (P < 0.05) TAOC and SOD and lower (P < 0.05) MDA than NC birds. The SOD activity of the FS group was greater (P < 0.01) than that of the PC group, whereas TAOC and MDA did not differ between FS and PC birds. In the finisher phase, FS birds had greater (P < 0.05) TAOC and lower (P < 0.05) MDA than NC birds. The activity of GSH-Px did not differ among treatments.


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Table 4. Effects of dietary Forsythia suspensa extract (FSE) supplement on total antioxidant capacity (TAOC), superoxide dismutase (SOD), glutathione peroxidase (GSH-Px), and malondialdehyde (MDA) concentrations of serum in broilers
 
Table 5Go shows hepatic antioxidant indices of birds. In the starter phase, only SOD activity was greater (P < 0.05) in FS compared with NC. In the finisher phase, FS birds had greater (P < 0.01) SOD and lower (P < 0.05) MDA than NC birds. Antioxidant indices in the muscle are shown in Table 6Go. In the starter phase, no differences were observed among treatments. In the finisher period, FS birds had greater (P < 0.05) SOD and lower (P < 0.05) MDA than NC birds. The SOD of FS birds was greater (P < 0.05) than that of PC birds.


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Table 5. Effects of dietary Forsythia suspensa extract (FSE) supplement on total antioxidant capacity (TAOC), superoxide dismutase (SOD), glutathione peroxidase (GSH-Px), and malondialdehyde (MDA) concentrations of liver in broilers
 

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Table 6. Effects of dietary Forsythia suspensa extract (FSE) supplement on total antioxidant capacity (TAOC), superoxide dismutase (SOD), glutathione peroxidase (GSH-Px), and malondialdehyde (MDA) concentrations of muscle in broilers
 

    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
High ambient temperature of birds is a major economic concern in poultry production due to its adverse effects on feed consumption, growth rate, hatchability, mortality, and health of birds (Bartlett and Smith, 2003; Ryder et al., 2004). When exposed to an environmental temperature of 32°C, broilers showed a 14% decrease in feed intake by 4 wk of age and a 24% reduction by 6 wk of age, lower growth rate, and a reduction in feed efficiency (Geraert et al., 1996). Broiler chickens under current closed production systems may be under high ambient temperatures during summer unless a cooling system is fully operational.

High ambient temperature is shown to induce extended production of oxidative free radicals by Halliwell and Gutteridge (1989). High ambient temperature is one of the environmental stresses that have been demonstrated to cause an increase in oxidative stress and an imbalance in antioxidant status (Gursu et al., 2004). Oxidative free radicals can cause oxidation of cellular lipid, DNA, and carbohydrates and consequently damage the function of normal cells (Dröge, 2002). Dietary supplementation of antioxidants, therefore, has been suggested as an effective way of alleviating high ambient temperature by reducing oxidative free radicals (Njoku, 1986; Sahin and Kucuk, 2003; Gursu et al., 2004). In this study, FSE was used as a natural source of antioxidants. The FSE was obtained from Forsythia suspensa and was shown to possess a free-radical scavenging effect as determined by reduced DPPH activity.

This study demonstrated that dietary supplementation of FSE improved growth performance (ADG and FC) of birds under high ambient temperature possibly due to improvement of nutrient digestibility (energy, CP, calcium, and phosphorus) and enhancement of antioxidant activities during the finishing phase as well as overall. High ambient temperature is shown to decrease nutrient digestibility (Mahmoud and Edens, 2003) possibly because of excessive ROS that oxidize and destroy cellular biological molecules, and finally cause a variety of impairments to intestinal tissues (Payne and Southern, 2005; Zhao and Shen, 2005). Impaired intestinal function can, therefore, cause reduced nutrient digestibility and, in turn, reduced growth performance. Antioxidants with effective free-radical scavenging properties may solve problems associated with intestinal impairment from high ambient temperature.

High ambient temperature may also cause reduced growth due to reduced appetite. Teeter et al. (1985) found that a reduction in feed intake of broilers lowered the production of metabolic heat. Supplementation of antioxidant can improve feed intake of birds under high ambient temperature (Njoku, 1986; Lohakare et al., 2005). High ambient temperature can also reduce growth of birds as they undergo oxidative stress at the cellular, tissue, and whole-body levels (Mahmoud and Edens, 2003), which can harm the health of birds. Improved antioxidant activities would alleviate ROS-induced oxidative stress (Wang et al., 2008).

Improvement of growth performance observed from this study can, therefore, be attributed to both enhanced health and improved nutrient digestibility. Considering the effective antioxidant property of FSE (Schinella et al., 2001; Guo et al., 2006), dietary supplementation of FSE did improve both nutrient digestibility and growth performance of broiler chickens in this study. Zhang et al. (2003a, b) and Yang et al. (2004) also demonstrated the free-radical scavenging effects of FSE by measuring DPPH activity and this was further confirmed by measuring MDA, SOD, GSH-Px, and TAOC activities in this study. In the present study, FSE showed a free-radical scavenging effect by measurement of DPPH activity, which is consistent with the previous reports (Zhang et al., 2003a,b; Yang et al., 2004). Additionally, effects on antioxidant enhancement of FSE in vivo were shown for some antioxidant parameters such as SOD, GSH-Px, TAOC, and MDA.

Several enzymatic factors such as SOD and GSH-Px can scavenge formed ROS to function as antioxidants. Superoxide can first be degraded into hydrogen peroxide by SOD and subsequently catalyzed to convert water by a series of enzymes including GSH-Px (Blokhina et al., 2003). This could be beneficial for the birds because increased antioxidant activity ensures proper and rapid elimination of ROS that could be formed under high ambient temperatures. In the present study, FSE increased SOD levels in both phases across serum, liver, and muscle but GSH-Px levels were not altered. Supplementation with FSE, therefore, may enhance the ROS scavenging by elevating the SOD level rather than the GSH-Px level. A similar result was found in the study of Hou and Yang (2006), in which FSE was demonstrated to increase cardiac SOD level in mice after exhaustive exercise. We also assayed serum TAOC levels to evaluate total antioxidative capacity: when the diet was supplemented with FSE, TAOC levels were elevated. The results indicated that the FSE enhancement on body total antioxidant capacity may include nonenzymatic and enzymatic antioxidant systems. In the present study, FSE decreased MDA levels in the sera, liver, and muscle in the finisher phase. These results confirmed the antioxidant effect of FSE in broilers under high ambient temperature. A similar finding of the effect of FSE on lipid peroxidation was reported by Hou and Yang (2006) in mice. In the present study, the results showed that the contents of SOD and TAOC were increased, and MDA was decreased; thus, FSE displayed a significant effect on antibiotic enhancement of boiler chickens under high ambient temperature. This enhancement correlates with the good free radical scavenging effect of FSE.

In the present study, high ambient temperature (32°C) was used to induce oxidative stress during the 6-wk feeding period. High ambient temperature was proposed to induce body oxidative status, which consequently oxidized lipid, DNA, and carbohydrates to damage normal cells. High ambient temperatures generated excessive ROS that destroyed biological molecules in cells, oxidized biomacromolecules, and finally caused a variety of impairments to tissue. These factors can induce intestinal malfunction. Decreased nutrient digestibility is one of the negative effects of high ambient temperature. Finally, growth performance decreased. Antioxidants with good free-radical scavenging properties may solve this problem. In the present study, FSE showed a significant effect on antioxidant enhancement in broiler chickens under high ambient temperature in the finisher phase, and apparent digestibility of energy, CP, calcium, and phosphorus was greater (P < 0.05) in FS birds than in NC birds. These results were consistent with the improvements in growth performance (ADG and FC) in the finisher phase and overall under high ambient temperature. Thus, FSE with effective free-radical scavenging properties may solve problems associated with intestinal impairments caused by high ambient temperature, thereby improving nutrient digestibility and enhancing growth performance.

Njoku (1986) and Lohakare et al.(2005) found that supplementation of antioxidant can improve the feed intake of birds under high ambient temperatures. In the present study, supplementing FSE increased, although not significantly, feed intake compared with NC in the finisher phase and overall. Good antioxidant activity of FSE may play a role in the enhancement of feed intake.

In the present study, effects of FSE on SOD and MDA are consistent with the results of Hou and Yang (2006) who found that FSE increased the cardiac SOD level and decreased the cardiac MDA level in mice after exhaustive exercise. The present study showed that supplemental FSE can improve growth performance. This is similar to studies by Njoku (1986) and Lohakare et al. (2005), which found improved growth and feed efficiency in broiler chicks supplemented with vitamin C. Wang et al. (2008) found the similar effect of bovine lactoferrin, an antioxidant, can improve antioxidant enzyme activity and performance of piglets.

In the present study, assays of SOD, GSH-Px, TAOC, MDA, and DPPH were conducted. These measurements were used because they reflect the effect of FSE on antioxidant activities. First, MDA can endogenously reflect lipid peroxidation, which is the consequence of diminished antioxidant protection as levels of ROS increase. Also, SOD and GSH-Px are the main parameters used to assess oxidative status in the enzymatic system. Finally, we assayed the TAOC level, which reflects the nonenzymatic antioxidant defense system. Determination of disappearance of free radicals such as DPPH is a stable and rapid method to assess the antioxidant activity of plant extracts in vitro (Samarth et al., 2007). In the present study, a DPPH assay was used to evaluate the antioxidant activity of FSE.

In conclusion, FSE can be used under the stress situation induced by high temperature to reduce the risks of peroxidation and improve nutrient digestibility and growth performance, especially during the finisher phase (d 22 to 42). In view of FSE’s good antioxidative and free-radical scavenging properties, we expect that FSE would have wide application in situations of stress. However, further study is needed to elucidate the optimum addition of FSE and its effects related to growth performance.


    FOOTNOTES
 
1 This investigation was financially supported by the Ministry of Science and Technology of the People’s Republic of China (2006 BAD12B05-10; Nyhyzx07-034), the National Natural Science Foundation of China (NSFC 30671522), and National Veterinary Research and Quarantine Service of Korea. Back

Received for publication January 15, 2008. Accepted for publication March 26, 2008.


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 DISCUSSION
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