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Effects of Chito-Oligosaccharide Supplementation on Performance, Nutrient Digestibility, and Serum Composition in Broiler Chickens

X. J. Li^*, X. S. Piao^*,1, S. W. Kim, P. Liu^*, L. Wang^*, Y. B. Shen^*, S. C. Jung and H. S. Lee

^* National Key Lab of Animal Nutrition, China Agricultural University, Beijing, China, 100094; Department of Animal and Food Sciences, Texas Tech University, Lubbock 79409; and National Veterinary Research and Quarantine Service, Ministry of Agriculture and Forestry, Anyang 430-824, Korea

¹ Corresponding author: piaoxsh{at}mafic.ac.cn

	ABSTRACT

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A total of 196 day-old male broiler chicks were randomly allocated to 1 of 4 treatments in a study conducted to determine the effects of dietary supplementation of chito-oligosaccharide (COS) on growth, nutrient digestibility, and serum composition. The experimental diets consisted of an unsupplemented control diet based on corn, soybean meal, and fish meal or similar diets supplemented with either chlortetracycline, 50 mg/kg of COS, or 100 mg/kg of COS. Each treatment was fed to 7 replicate pens of birds, with 7 birds per pen. Broiler performance, nutrient digestibility, cecal microbial concentrations, and serum indices were measured at the end of the starter (d 21) and grower phases (d 42). During the starter period and overall, broilers fed 50 or 100 mg/kg of COS had better (P < 0.05) average daily gain, average daily feed intake, and feed conversion than the control birds. The performance of birds fed chlortetracycline was generally intermediate between that of the control and the 2 COS treatments. Compared with the birds in the control or chlortetracycline treatments, the birds receiving 100 mg/kg of COS had better nutrient digestibility of DM, energy, calcium, and phosphorus; higher (P < 0.05) concentrations of cecal Lactobacillus; and lower (P < 0.05) serum triglyceride and total cholesterol during the starter phase. During the grower phase, the birds fed 100 mg/kg of COS had higher (P < 0.05) calcium digestibility and CP retention than those fed the chlortetracycline treatment, and lower concentrations of cecal Escherichia coli than birds in the control treatment. The serum growth hormone level in birds fed 50 mg/kg of COS was higher (P < 0.05) than in the other treatments. The birds fed 100 mg/kg of COS had lower (P < 0.05) serum triglyceride, higher (P < 0.05) serum high-density lipoprotein cholesterol, and higher serum total protein content than birds in the other treatments. In conclusion, dietary supplementation with COS appeared to improve the average daily gain of broilers by increasing the average daily feed intake and nutrient digestibility and modulating the concentrations of cecal microbial flora. Additionally, COS increased serum protein and high-density lipoprotein cholesterol and decreased serum triglyceride.

Key Words: chito-oligosaccharide • performance • nutrient digestibility • serum composition • broiler

	INTRODUCTION

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Certain types of oligosaccharides have been used as prebiotics to improve animal performance, to enhance immune ability, and to affect gut microbial flora concentrations (White et al., 2002; Lemieux et al., 2003; Smiricky-Tjardes et al., 2003; Flemming et al., 2004). Chito-oligosaccharide (COS) is an oligosaccharide that is easily obtained by chemical and enzymatic hydrolysis of poly-chitosan. Poly-chitosan is the second most abundant carbohydrate polymer found in nature (Knaul et al., 1999). However, its insolubility and high viscosity limit its application for use with animals as a nutrient source. In contrast, COS has low molecular weight, good solubility, and low viscosity (Chae et al., 2005).

The health benefits of COS have recently been identified. Chito-oligosaccharide has been shown to reduce the establishment of pathogens in the intestine (Shigehiro et al., 1990; Yalpani et al., 1992; Vishu Kumar et al., 2005) and improve immune function (Okamoto et al., 2003). It has also been shown to reduce the triglyceride level in obese diabetic mice (Hayashi and Ito, 2002). However, its role in regulating the blood lipid content is still controversial (Sugano et al., 1992; Ikeda et al., 1993).

In the field of animal production, dietary supplementation of COS increased serum growth hormone and the insulin-like growth factor-I (IGF-I) mRNA level and enhanced protein synthesis in early-weaned pigs (Tang et al., 2005). Chito-oligosaccharide was also shown to have antifungal (Hirano and Nagao, 1989) and antimicrobial (Jeon et al., 2000) activities that improved gut health and thus increased nutrient digestibility and weight gain in broilers (Huang et al., 2005). The objective of the current study was to further explore the effects of COS on performance, nutrient digestibility, and serum indices in broilers.

	MATERIALS AND METHODS

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Preparation and Composition of Chito-oligosaccharide
The COS supplement used in this study was prepared and supplied by GlycoBio Company (Dalian, China) and contained 40% COS and 60% cyclodextrin as a carrier. The COS was composed of several chitosan oligomers with molecular weights averaging 1,500 Da. The water solubility of the COS supplement was greater than 99%.

To separate and quantify the different oligomers contained in the COS supplement, a standard sample was prepared by mixing 6 chitosan oligomers (Sigma, St. Louis, MO) using identical concentrations of each. Separation and quantification of oligomers was done by HPLC using an evaporative light-scattering detector (model 301, ESA, Chelmsford, MA) and Asahipak NH2P-50-4E (4.6 x 250 mm; Shodex, Tokyo, Japan).

The concentration of COS used for HPLC analysis was 20 mg/mL. The mobile phase was acetonitrile and a 0.3% ammonia solution at pH 10. Each run lasted 60 min. The concentration of acetonitrile used for the mobile phase was 75% from 0 to 5 min, which was gradually reduced to 50% by 40 min, followed by a further reduction to 0% by 50 min and then a return to 75% by 60 min. The column was maintained in a column oven at 30°C, and the evaporative light-scattering detector evaporation chamber temperature was maintained at 90°C. The elution flow rate was maintained at 1.0 mL/min.

Experimental Animals
A total of 196 day-old male Arbor Acres broiler chicks were purchased from Arbor Acres Poultry Breeding Company (Beijing, China). All birds were raised in wire-floored cages in an environmentally controlled room with continuous light (10 to 20 lux) and had access to feed and water ad libitum. The room temperature was maintained at 33°C for the first 3 d, after which the temperature was gradually reduced by 3°C a week until reaching 24°C; this temperature was maintained until the end of the 42-d experiment. The lighting regimen and ventilation were monitored continuously from d 1 to 42. All birds were inoculated with Newcastle disease vaccine on d 7 and 28 and with inactivated infectious bursa disease vaccine on d 14 and 21. The trial was conducted in 2 phases consisting of the starter phase from d 1 to 21 and the grower phase from d 22 to 42. The Animal Welfare Committee of China Agricultural University approved the animal care protocol used for this experiment.

Experimental Design and Diets
The broilers were randomly allotted to 1 of 4 dietary treatments (Table 1). The experimental diets consisted of an unsupplemented control diet based on corn, soybean meal, and fish meal or similar diets supplemented with chlortetracycline (80 mg/kg during the starter phase and 50 mg/kg during the grower phase) or COS at either 50 or 100 mg/kg. There were 7 replicate pens per treatment, with 7 birds per pen. All essential nutrients contained in the basal diet met the requirements suggested by the NRC (1994). All diets were fed in mash form.

Excreta from d 19 to 21 and d 40 to 42 were collected from each pen, pooled within pen, 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), whereas the gross energy content was measured by an adiabatic bomb calorimeter (model 1281, Parr, Moline, IL) to calculate the CP retention and the apparent digestibility of other nutrients.

On d 42, one bird per pen was randomly selected and euthanized for sampling. Blood was collected (5 mL) by cardiac puncture into a 10-mL anticoagulant-free Vacutainer tube (Greiner Bio-One GmbH, Kremsmunster, Austria) and then centrifuged at 3,000 x g for 10 min to obtain serum. The serum samples were stored at –20°C until needed for analysis. The contents of the cecum were aseptically collected, pooled, and immediately immersed in liquid nitrogen and preserved at –80°C for later analysis. In vitro survival of Lactobacillus and Escherichia coli was determined using the method described by Zhang et al. (2003).

Measurement of Serum Indices
The concentrations of total protein, triglyceride, total cholesterol, high-density lipoprotein (HDL) cholesterol, and low-density lipoprotein (LDL) cholesterol in serum samples were analyzed by an automatic biochemical analyzer (RA-1000, Bayer Corp., Tarrytown, NY) using colorimetric methods, following the instructions of the manufacturer of the corresponding reagent kit (Zhongsheng Biochemical Co., Ltd., Beijing, China).

Serum growth hormone was measured using a commercially available growth hormone radioimmunoassay kit (SINO-UK, Huaying Institute of Biological Technology, Beijing, China). The antibody was obtained from chicken according to the method of Berghman et al. (1988). It was validated for chicken. Inter- and intra-assay CV were <13 and <9%, respectively. The recovery rate was 95 to 104%.

Serum IGF-I content was measured by a porcine IGF-I radioimmunoassay kit (Diagnostic Systems Laboratories Inc., Webster, TX). The cross-reactivity was <5%. The inter- and intra-assay CV were <8.2 and <3.4%, respectively. The recovery rates of the preextraction and postextraction studies ranged from 79 to 88% and from 89 to 122%, respectively. Both extraction and analysis procedures were conducted according to the instructions of the manufacturer of the radioimmunoassay kit.

Statistical Analyses
Data were subjected to ANOVA using the GLM procedure of SAS (SAS Institute, 1996). The pen was the experimental unit. Differences among treatments were separated by Duncan’s multiple range test. Results were expressed as least squares means and SEM. Probability values less than 0.05 were considered significant.

	RESULTS

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Composition of Experimental Chito-oligosaccharide
The mixture of chitosan oligomer standards was subjected to HPLC, and the retention time of the standards was recorded (Figure 1). Peaks were identified as N-ace-tylglucosamine, chitobiose, chitotriose, chitotetrose, chitopentose, and chitohexose.

View larger version (9K): [in this window] [in a new window]   Figure 1. Chromatogram of the chitosan oligomers standard mixture determined by HPLC. Peaks represented: 1, N-acetylglucosamine; 2, chitobiose, consisting of 2 ß-(1–4)-linked N-acetylglucosamine units; 3, chitotriose, consisting of 3 ß-(1–4)-linked N-acetylglucosamine units; 4, chitotetrose, consisting of 4 ß-(1–4)-linked N-acetylglucosamine units; 5, chitopentose, consisting of 5 ß-(1–4)-linked N-acetylglucosamine units; 6, chitohexose, consisting of 6 ß-(1–4)-linked N-acetylglucosamine units.

View larger version (7K): [in this window] [in a new window]   Figure 2. Chromatogram of the chito-oligosaccharide (COS) supplement (20 mg/mL of COS) determined by HPLC. The oligomers were identified according to the retention time of the standard sample chromatogram. The concentrations of the 5 oligomers were: 2, chitobiose, 0.58; 3, chitotriose, 2.51; 4, chitotetrose, 4.49; 5, chitopentose, 5.80; 6, chitohexose, 2.21 mg/mL.

Over the entire experimental period, the ADG of birds fed 50 mg/kg of COS, 100 mg/kg of COS, and chlortetracycline were 7.4, 5.9, and 4.7% greater (P < 0.01) than that of the control. The ADFI and FC of birds in the 50 and 100 mg/kg of COS treatments were also better (P < 0.05) than those of the control. The ADFI of birds in the 50 and 100 mg/kg of COS treatments were 2.9 and 2.5% greater, whereas FC were 4.4 and 3.4% better than those of the control, respectively.

Apparent Digestibility and Intestinal Microbial Flora
Crude protein retention in the starter diets was not affected by COS supplementation (Table 3). However, the apparent digestibility of DM, energy, phosphorus, and calcium was improved (P < 0.05) by supplementation with 100 mg/kg of COS compared with the control and chlortetracycline treatments. Birds in the 100 mg/kg of COS treatment significantly increased concentrations of Lactobacillus in the cecum compared with those in the other treatments.

Serum Indices
On d 21, both serum triglyceride and cholesterol levels of birds fed 100 mg/kg of COS were lower (P < 0.05) than those of birds in the chlortetracycline and control treatments, whereas only the serum triglyceride level of birds in the 50 mg/kg of COS treatment was lower than that of birds in the chlortetracycline treatment (Table 4). The serum LDL cholesterol level of birds fed 50 mg/kg of COS was lower (P < 0.05) than that of birds fed chlortetracycline. There was no difference in HDL cholesterol levels between treatments. Serum total protein and HDL cholesterol were not different among the treatments.

Serum Growth Hormone and IGF-I
On d 21, the serum growth hormone level of birds fed 100 mg/kg of COS was lower (P < 0.05) than that of birds fed chlortetracycline, although the serum IGF-I level did not differ (Table 5). On d 42, COS supplementation did not affect the serum IGF-I level. However, the serum growth hormone level of birds fed 50 mg/kg of COS was higher (P < 0.05) than for the other treatments.

	DISCUSSION

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In comparison with the control group, dietary supplementation with both levels of COS improved the growth of broilers during both the starter and grower periods as well as over the entire experimental period. However, at either d 21 or 42, the serum growth hormone level for birds fed 100 mg/kg of COS did not differ from the control, whereas the 50 mg/kg of COS treatment increased the growth hormone level only during the last 3 wk of the grower period. The serum IGF-I level was unaffected by treatment on both d 21 and 42. In mammals, growth hormone functions use 2 signal pathways. One is through binding to its receptor to cascade downstream signals, whereas the other pathway is to stimulate the production of IGF-I to produce growth effects indirectly (Florini et al., 1996). Tang et al. (2005) concluded that dietary supplementation of 0.025% COS improved the performance of weaning pigs by improving growth hormone secretion, which subsequently increased IGF-I synthesis and secretion. However, in the avian species, Buyse and Decuypere (1999) concluded that growth hormone had little, if any, potential for improving the growth rate and feed efficiency of rapidly growing broilers.

The lack of a consistent effect of COS on growth hormone and IGF-I levels suggested that the improved ADG observed in the present study was not due to increased growth hormone but was more likely due to the increased feed intake and improved nutrient digestibility in broilers. In the present study, the 100 mg/kg of COS treatment had improved DM, energy, calcium, and phosphorus digestibility in the starter phase and increased CP retention and calcium digestibility in the grower phase, which was greater than or equal to the response obtained for the antibiotic treatment. The finding of improved nutrient digestibility agreed with the results of Huang et al. (2005), who found that supplementation of 100 mg/kg of COS to the diet improved nutrient digestibility and feed efficiency in broiler chickens. Tuohy et al. (2003) reported that the nutrient digestibility enhancement in broilers supplied with as oligosaccharide diet was due to an improvement in gut health. Wang et al. (2005) also reported that dietary supplementation of 125 mg/kg of COS increased ADG by 5.9% and improved nutrient digestibility by improving gut health. The COS used in this study had a molecular weight of 1,500 Da, and COS with that molecular weight has been shown to have strong antimicrobial activity, immunity enhancement, and growth-promoting effects in broiler chickens (Xia and Wu, 1996; Du et al., 2001).

In the present study, dietary supplementation of 100 mg/kg of COS increased the concentrations of cecal Lactobacillus in the starter phase and reduced the concentrations of cecal Escherichia coli in the grower phase. Our results are similar to the reports of Shibasaki et al. (1988) and Yalpani et al. (1992). Those documents indicated that COS may also serve as a growth promoter in broiler production by modulating the concentrations of intestinal microbial flora.

In this study, we found that dietary supplementation of COS can lower blood lipids in broilers. Chito-oligosaccharide not only decreased the levels of serum triglyceride and total cholesterol in the starter broilers, but also reduced the serum triglyceride and increased serum HDL cholesterol levels of the grower broilers. These findings are in agreement with the reports of Sugano et al. (1988) and Tang et al. (2005) showing that blood lipid levels were decreased by COS supplementation. Interestingly, we also found that the serum total cholesterol and LDL cholesterol levels of the grower broilers fed COS were increased. These findings are in agreement with Sugano et al. (1992), who reported that COS with a high degree of depolymerization was not effective in lowering cholesterol levels.

More and more consumers are strongly demanding safe and healthy by-products, which is the main reason that low-fat chickens are popular products in national markets. The lipid-lowering effect of chitosan was documented in earlier studies (Jameela et al., 1994; Kanauchi et al., 1995). However, the mechanism of the cholesterol-lowering effect of COS is controversial (Ikeda et al., 1993; Tanaka et al., 1997; Remunan-Lopez et al., 1998). The most important mechanism by which chitosan eliminates cholesterol would likely be through reducing lipid absorption in the intestine by binding bile acids, which results in increased cholesterol elimination and induced hepatic synthesis of new bile acid (Zhen et al., 2003).

In the process of protein anabolism and proteolysis, the serum protein level usually reflects the protein metabolism and immunity function situation in vivo. Serum total protein contains albumin and globulin, both of which were shown to reflect the hepatic protein metabolic status in response to dietary treatments in early-weaned piglets (Stoll et al., 1998). In the current study, we found that dietary supplementation of COS significantly increased the serum total protein compared with the chlortetracycline and control treatments. This result implies that dietary supplementation of COS can improve whole-body protein anabolism in growing broilers.

In conclusion, dietary supplementation of 50 or 100 mg/kg of COS improved the growth rate of broilers. This increase was likely mediated through the effects of COS on ADFI and nutrient digestibility. Thus, COS is a potential alternative to the use of antibiotics as a growth promoter. However, further study is needed to elucidate the mechanism by which COS improves the performance and immune function in broilers.

	ACKNOWLEDGMENTS

 
The authors gratefully acknowledge Shuguang Li (Dalian Chemical and Physical Institute, the Chinese Academy of Science, Dalian, People’s Republic of China) for analyzing the molecular weight of the chito-oligosaccharide. The investigation was financially supported by the National Nature Science Foundation of China (NSFC 30671522) and the National Basal Research Program (2004 CB 117503).

Received for publication October 11, 2006. Accepted for publication February 24, 2007.

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via ISI Web of Science (1) Citing Articles via Google Scholar Google Scholar Articles by Li, X. J. Articles by Lee, H. S. Search for Related Content PubMed PubMed Citation Articles by Li, X. J. Articles by Lee, H. S.