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METABOLISM AND NUTRITION |
Department of Animal Sciences, University of Illinois, Urbana 61801
1 Corresponding author: poultry{at}uiuc.edu
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Key Words: oligosaccharide • prebiotic • metabolizable energy • amino acid digestibility • intestinal microflora • poultry
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Fructooligosaccharides (FOS) that include inulin, oligofructose, and short-chain fructooligosaccharide (SCFOS) can be fermented by bifidobacteria and lactobacilli (Hidaka et al., 1986; Bouhnik et al., 1994; Gibson and Roberfroid, 1995). These 2 bacteria are generally classified as beneficial bacteria (Mizutani and Mitsuoka, 1980; Kawase, 1982; Gibson and Wang, 1994; Flickinger et al., 2003). These FOS also may help control or reduce the growth of harmful bacteria such as Clostridium perfringens, which is especially important to the poultry industry because this bacterium is a primary cause of necrotic enteritis that has been estimated to cost the worldwide poultry industry $2 billion each year (Hofacre et al., 2005).
Transgalactooligosaccharide (TOS) is a relatively unstudied compound in livestock; however, it has been examined for its bifidogenic effect in humans (Ito et al., 1993; Bouhnik et al., 1997). In Japan, it is a compound that is marketed in human nutrition for its bifidogenic effect (Ito et al., 1993). This oligosaccharide is a synthetic compound produced from lactose by enzymatic transga-lactosylation and consists of lactose and several galactose molecules. It passes through to the hindgut undigested due to its β-(1,6) and β-(1,4) linkages that avoid digestion by β-galactosidase (Alles et al., 1999).
Mannanoligosaccharides (MOS) are present in the cell wall of yeast and have been shown to alter microbial populations in livestock. Yeast cell wall contains a high affinity ligand for bacteria and offers a competitive binding site for bacteria (Ofek et al., 1977). Pathogens with the mannose-specific type-1 fimbriae adsorb to the MOS instead of attaching to the intestinal epithelium and, therefore, move through the intestine without colonization (Newman, 1994). Supplemental MOS also has been shown to increase the production of immunoglobulin A in rats (Kudoh et al., 1999), dogs (Swanson et al., 2002), and turkeys (Savage et al., 1996). The production of immunoglobulin A is important to immunity because it inhibits the attachment and penetration of bacteria in the lumen, increases the production of mucus (McKay and Perdue, 1993), and prevents inflammation that would cause epithelial tissue damage (Russell et al., 1989).
Several studies have been conducted to evaluate the feeding of FOS and MOS to poultry. Ammerman et al. (1988) reported that feeding FOS at 2.5 and 5 g/kg of diet to broiler chickens to market weight (46 d) improved feed efficiency. They also reported an increased weight gain when 3.75 g/kg of FOS was fed (Ammerman et al., 1989). Waldroup et al. (1993) studied the use of FOS (3.75 g/ kg) in broiler chickens and found no significant effects on weight gain or feed conversion at 21 or 49 d of age. Wu et al. (1999) determined that the optimal concentration to supplement FOS in broiler chickens was 2.5 to 5.0 g/kg. These doses had positive effects on body weight gain and feed efficiency, whereas providing 10.0 g/kg of FOS resulted in diarrhea, thus decreasing production performance. Xu et al. (2003) evaluated 3 concentrations of FOS (2, 4 and 8 g/kg) in broiler chickens from 1 to 49 d of age. They found that 4.0 g/kg of FOS improved average daily gain while 2.0 and 8.0 g/kg of FOS supplementation had no significant effect on average daily gain. Feed conversion was improved by 5.4 and 9.0% when 2 and 4 g/ kg of FOS were fed to broiler chickens, respectively, but there was no improvement in feed conversion for birds supplemented with 8 g/kg of FOS.
Yeast cell wall containing MOS reduced intestinal Salmonella concentrations by 26% in broiler chicks (Spring et al., 2000) compared with chicks fed an unsupplemented diet and also was shown to improve growth performance from 0 to 21 d of age (Pelicano et al., 2004). In turkeys, MOS at 1 g/kg of diet increased the concentration of bifidobacteria and decreased the concentration of Clostridium perfringens in the large intestines of 6-wk-old turkeys (Finucane et al., 1999). When turkeys were fed 1 g/kg (1 to 6 wk) and 0.5 g/kg (7 to 18 wk) of MOS, live weight was improved at 18 wk of age when compared with the turkeys in the control treatment and was similar to turkeys being fed a diet containing bacitracin methylene disalicylate (Sims et al., 2004). An 8-wk study with 8-wk-old turkeys showed MOS at 1 and 4 g/kg resulted in no significant changes in body weight gain, feed intake, or feed conversion (Stanczuk et al., 2005). Rosen (2005) provided an extensive review of MOS research with turkeys.
The objectives of this study were to evaluate a wider array of prebiotic oligosaccharides than evaluated in earlier studies. In addition to measuring growth performance, which was the emphasis of most of the earlier studies with poultry, the effects of several oligosaccharides on MEn and amino acid (AA) digestibility in chicks at different ages and cecal microbial populations of Bifidobacterium and Lactobacillus spp., E. coli, and C. perfringens at 21 d of age were determined.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The Institutional Animal Care and Use Committee approved all procedures. Three experiments were conducted using New Hampshire x Columbian male chicks. The chicks were housed in thermostatically controlled starter batteries with raised wire floors in an environmentally controlled building. The wire floors of the batteries were left uncleaned from previous experiments in an attempt to provide increased bacterial exposure to chicks. At hatch, chicks were weighed, wing-banded and randomly allotted to 5 pens of 8 chicks per treatment so that each pen of chicks had a similar initial weight and weight distribution. Each experiment was 21 d in length, and body weights and feed intakes were measured at the end of wk 1 and 3. Weight gain, feed efficiency (G:F), and mortality were calculated for each pen replicate. No mortality occurred in any of the experiments.
Apparent Metabolizable Energy and Amino Acid Analysis
In experiments where apparent metabolizable energy and amino acid digestibility were measured, the following procedures were followed. Excreta from each pen were collected over a 24-h period on d 3 and 4 (3–4), 7, 14, and 21 posthatching and freeze-dried. Feed and excreta samples then were finely ground and analyzed for gross energy using an adiabatic bomb calorimeter. Analysis for nitrogen was performed using the Kjeldahl procedure of the Association of Official Analytical Chemists (AOAC, 1980). Amino acid concentrations in feed and excreta were determined for select ages at the University of Missouri—Columbia Experiment Station Chemical Laboratory. The concentration of acid insoluble ash (Celite) in the feed and excreta was determined by the method of Vogtmann et al. (1975), and the MEn of the diets was calculated using the equation described by Hill and Anderson (1958).
Cecal Microbial Populations
In experiments where cecal microbial populations were evaluated, the following procedures were followed. At 21 d, 4 chicks from each pen replicate were euthanized via CO2 inhalation prior to extraction of cecal contents. The cecal contents from 1 cecum of each bird were pooled together for serial dilution. The content of the other cecum was utilized to determine dry matter content. Microbial populations were determined by serial dilution (10–4 to 10–7) of cecal samples in anaerobic diluent before inoculation onto Petri dishes of sterile agar as described by Bryant and Burkey (1953). The selective media for bifidobacteria (BIM-25) was prepared using reinforced clostridial agar according to Mu
oa and Pares (1988). Lactobacilli were grown on Rogosa SL agar, and E. coli were grown on EMB agar. Agars used to grow C. perfringens were prepared according to the FDA Bacteriological Analytical Manual (1992). Plates for Bifidobacterium and Lactobacillus spp., and C. perfringens were incubated anaerobically (73% N: 20% CO2: 7% H2) at 37°C. Escherichia coli were incubated aerobically at 37°C. Plates were counted between 24 and 48 h after inoculation. Colony forming units (cfu) were defined as being distinct colonies measuring at least 1 mm in diameter.
Experiments 1 and 2
The objective of these experiments was to measure the effects of 5 oligosaccharides on growth performance, MEn, and AA digestibility in chicks fed a corn-soybean meal diet (Table 1
). The 5 oligosaccharides were inulin (Orafti Company, Tienen, Belgium), oligofructose (Orafti Company), SCFOS (GTC Nutrition Company, Golden, CO), MOS (Alltech, Nicholasville, KY), and TOS (Borculo Domo Ingredients, Borulo, the Netherlands; 6 total diets with the unsupplemented basal diet). The oligosaccharides were fed at 8 g/kg in experiment 1 and 4 g/kg in experiment 2. Cecal microbial populations were measured in experiment 2.
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This experiment evaluated the ability of each oligosaccharide to alter the cecal microbial populations in chicks fed a dextrose-isolated soy protein diet (Table 1
). The latter diet was used because it contains little or no indigestible oligosaccharides, whereas a corn-soybean meal diet contains large amounts of indigestible oligosaccharides, mostly from the soybean meal. Each oligosaccharide (inulin, oligofructose, SCFOS, MOS, or TOS) was included at 4 g/kg, and results were compared with chicks fed a diet containing no supplemental oligosaccharides.
Statistical Analysis
All data were analyzed by the GLM procedure of SAS for a completely randomized design (SAS Institute Inc., 1990). If the F-test for treatment effect was significant, differences among treatment means were determined with the least significant difference test (Carmer and Walker, 1985). Differences were considered significant when P <0.05.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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At 8 g/kg, there was no significant effect of any oligosaccharide on weight gain, feed intake, or feed efficiency at 7 or 21 d of age (Table 2). The addition of inulin at 8 g/kg reduced (P <0.05) MEn at 7, 14, and 21 d when compared with chicks fed the basal diet (Table 3), and SCFOS reduced (P <0.05) MEn at 7 and 14 d. In general, oligofructose, MOS, and TOS had no effect on MEn when compared with the basal diet. The MEn values of all diets increased between 3–4 and 14 d.
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), oligofructose was the only oligosaccharide that had no negative impact on the digestibility of any AA at any age. Inulin, SCFOS, and TOS had a negative effect (P <0.05) on AA digestibility at 7 and 21 d compared with chicks fed the basal diet. Although MOS reduced AA digestibility at 7 d, there was no effect at 21 d. As with MEn, AA digestibility increased with increasing age.
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When the concentration of oligosaccharides was lowered from 8 to 4 g/kg, there was no effect on weight gain, feed intake, and feed efficiency (Table 5). As was observed in experiment 1, the MEn values of the diets were lowest during the first week and then increased and reached a plateau at 14 d of age (Table 6). At 4 d, SCFOS, MOS, and TOS reduced (P <0.05) MEn when compared with chicks fed the basal diet. At 7 and 14 d, there was a significant increase (P <0.05) in MEn when chicks were fed diets supplemented with 4 g/kg inulin, oligofructose, or MOS. All oligosaccharides improved (P <0.05) MEn at 21 d. Amino acid digestibility was improved (P <0.05) at 21 d for chicks fed 4 g/kg MOS (Table 7). Slight reductions (P <0.05) in AA digestibility for at least 1 age period were observed for the remaining oligosaccharides. These reductions were generally small at 21 d but were larger at 3–4 d. The effect of age on AA digestibility in this experiment was similar to that of the previous experiment with AA digestibility increasing with increasing age. No significant increase or decrease was observed for any cecal microbe tested when an oligosaccharide was supplemented at 4 g/kg in a corn-soybean meal diet (Table 8).
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There was a decrease (P <0.05) in cecal C. perfringens populations in chicks fed a dextrose-isolated soy protein diet containing 4 g/kg of SCFOS or MOS when compared with chicks fed the unsupplemented basal diet (Table 8). There was no effect of dietary treatment on cecal bifidobacteria, lactobacilli, or E. coli populations.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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As has been previously reported by our lab (Batal and Parsons, 2002) and also observed herein, the ability of the chick to utilize energy and AA in a corn-soybean meal diet increases until the chick is approximately 14 d old. At this point, MEn and AA digestibility plateau, suggesting that digestibility or utilization has reached a maximum.
The inclusion of an oligosaccharide at 8 g/kg probably approaches the highest tolerable concentration that can be fed to poultry without detrimental effects (e.g., diarrhea). Wu et al. (1999) demonstrated that the optimal concentration for supplementation of FOS to poultry diets was between 2.5 and 5 g/kg, and if fed at a higher concentration of 10 g/kg, growth performance was depressed. Xu et al. (2003) also concluded that feeding 8 g/kg of FOS resulted in poorer performance than feeding 2 or 4 g/kg of FOS. Although there was no effect on growth performance in the current study, when inulin and SCFOS were included in a corn-soybean meal diet at 8 g/kg, there may have been a negative impact on the MEn of the diet because the values were lower than the basal diet at 7, 14, and 21 d of age. However, with few exceptions, MEn values for the diets containing oligofructose, MOS, or TOS were not different than that for the basal diet. When considering the effect of diet on apparent AA digestibility, oligofructose (8 g/kg) was the only nondigestible oligosaccharide that had no negative impact on the digestibility of any AA at any age. All other oligosaccharides yielded digestibility values that were lower than those for the basal diet at some age. The negative impact of several of the oligosaccharides at 8 g/kg on MEn and AA digestibility suggests that this concentration may be decreasing nutrient utilization and probably exceeds the concentration that should be fed to chicks.
The positive effects of 4 g/kg of select oligosaccharides on nutrient digestion indicates that this concentration may be better suited for feeding poultry as suggested by Wu et al. (1999) and Xu et al. (2003). At 7, 14, and 21 d, MEn of a corn-soybean meal diet was improved for chicks fed diets supplemented with inulin, oligofructose, and MOS, and at 21 d, SCFOS and TOS (4 g/kg) also produced an improvement in MEn values. When MOS was fed at 4 g/kg, AA digestibility for all AA was improved (P <0.05) 1 to 6 percentage units compared with the chicks fed the basal diet at 21 d. In contrast, SCFOS and TOS generally reduced AA digestibility of all AA at 21 d by 1 to 4 percentage units. Xu et al. (2003) evaluated the effects of FOS on small intestinal digestive enzyme activities of total protease, amylase, and lipase in 49-d-old broilers and found that proteolytic and amylolytic activity were improved by 27 and 75%, respectively, compared with unsupplemented broilers when FOS was supplemented at 4 g/kg. Thus, the improvements in MEn from the oligosaccharides in the current study may have been due to increases in amylase activity in the small intestine. The current results for MEn and AA digestibility suggest that supplementing 4 g/kg of an oligosaccharide can improve energy digestion but may not be stimulating intestinal changes associated with protein digestion and AA absorption, or at least not as much as for MEn.
Controlling the growth of intestinal microflora is important for improving the well being of the host. Many bacteria compete with the host for nutrients within the gastrointestinal tract, elicit an immune response that causes a reduction in appetite and an increase in muscle catabolism to maintain the immune response, cause disease, and reduce nutrient absorption in the intestine (Bedford, 2000). For these reasons, it is important to promote the growth of bacteria that are able to provide nutrients to the host and/or are able to limit the growth of bacteria that are detrimental to the well-being of the host. The 2 bacteria that have received the most attention for promoting health are bifidobacteria and lactobacilli. These bacteria are able to limit the growth of E. coli and C. perfringens through bacteriostatic and bacteriocidal effects (Fuller, 1977; Gibson and Roberfroid, 1995). Campbell et al. (1997) fed rats diets containing 6% oligofructose or SCFOS and found that cecal concentrations of bifidobacteria were increased compared with the control diet. Numerous human studies have been conducted that showed an increase in bifidobacteria populations when oligofructose was fed in doses ranging from 5 to 20 g/d (Niness, 1999). In a study with broiler chickens, Xu et al. (2003) fed FOS at 2 or 4 g/kg in a corn-soybean meal diet and reported that cecal lactobacilli was increased and the concentration of E. coli was decreased at 49 d of age. The cecal concentration of bifidobacteria was increased when FOS was fed at 4 g/kg. These researchers found no effect on cecal microbes when FOS was fed to chickens at 8 g/kg.
In the first 2 experiments, corn-soybean meal diets were used to determine the effects of each oligosaccharide in a conventional diet. When cecal microbe populations were evaluated in the second experiment, no significant effects were detected for any of the dietary treatments. Because soybean meal contains approximately 6% raffinose plus stachyose (Coon et al., 1990), the lack of response in cecal microbial numbers may have resulted because the dietary soybean meal already provided a large amount of indigestible oligosaccharides. In an attempt to better detect the effects of each oligosaccharide on cecal microbes, a third experiment was conducted utilizing a dextrose-isolated soy protein diet that contained little or no indigestible oligosaccharides. With the latter diets, SCFOS and MOS reduced the concentration of cecal C. perfringens, suggesting that this diet may be more sensitive than a corn-soybean meal diet for detecting the effects of oligosaccharides on microbial populations. However, even in the absence of soybean meal, the dietary effects on cecal microbes were limited, with only a difference being detected for C. perfringens and not for the other 3 microbes.
The results of the current study indicate that feeding 4 or 8 g/kg of various oligosaccharides had no negative impact on the growth performance of young chicks. There may, however, be an advantage to providing only 4 g/ kg of an indigestible oligosaccharide in a corn-soybean meal diet because 8 g/kg depressed MEn and amino acid digestibility.
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ACKNOWLEDGMENTS |
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Received for publication December 11, 2006. Accepted for publication April 21, 2007.
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