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Poult Sci 2007. 86:1161-1165
© 2007 Poultry Science Association
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METABOLISM AND NUTRITION: Research Note

The Effects of Several Oligosaccharides on True Amino Acid Digestibility and True Metabolizable Energy in Cecectomized and Conventional Roosters

P. Biggs and C. M. Parsons1

Department of Animal Sciences, University of Illinois, 1207 W. Gregory Dr., Urbana 61801

1 Corresponding author: poultry{at}uiuc.edu


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
Prebiotics, such as indigestible oligosaccharides, are considered to be possible dietary alternatives to antibiotic growth promoters in poultry. The effects of indigestible oligosaccharides on nutrient digestibility in poultry are largely unknown. Therefore, an experiment was conducted to evaluate the effects of several oligosaccharides on amino acid digestibility and TMEn in roosters. The dietary treatments consisted of a corn-isolated soy protein control diet or that diet supplemented with 4 or 8 g/kg of inulin, oligofructose, mannanoligosaccharide (MOS), short-chain fructooligosaccharide, or transgalactooligosaccharide (TOS). Each of the 11 diets was tube-fed (30 g) to 4 cecectomized and 4 intact Single Comb White Leghorn roosters that had been fasted for 24 h. Excreta were then collected for the following 48 h, freeze-dried, and analyzed for amino acid content. The true digestibility of lysine and valine was increased (P < 0.05) in cecectomized roosters fed 8 g/kg of MOS or TOS when compared with roosters fed the control diet. In addition, methionine digestibility was improved (P < 0.05) in cecectomized roosters fed 4 g/kg of MOS or short-chain fructooligosaccharide and by 8 g/kg of oligofructose or TOS. The true digestibility of isoleucine was increased (P < 0.05) in cecectomized roosters fed 8 g/kg of MOS or 4 or 8 g/kg of TOS. The magnitude of the increases in amino acid digestibility coefficients for cecectomized roosters ranged from 3 to 9 percentage units. Feeding either 4 or 8 g/kg of inulin to intact roosters decreased (P < 0.05) the true digestibility of methionine. The oligosaccharides generally had no significant effect on TMEn. The results of this study indicated that the indigestible oligosaccharides had no significant effect on the digestibility of most amino acids in a corn-isolated soy protein diet. The digestibility of a few amino acids, however, was increased by some oligosaccharides in cecectomized roosters but not in intact roosters.

Key Words: oligosaccharide • amino acid digestibility • true metabolizable energy • prebiotic


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
Many oligosaccharides are considered to be prebiotic compounds that can improve intestinal health. This is due to the ability of the oligosaccharide to pass through to the hindgut of monogastric animals intact and to be fermented by beneficial bacteria, such as bifidobacteria and lactobacilli, that are stimulated to grow and produce compounds that are beneficial to the host. At the same time, the beneficial bacteria are able to limit or prevent the growth of bacteria such as Escherichia coli and Clostridium perfringens that can be harmful to the host (Gibson and Roberfroid, 1995). Only recently have oligosaccharide prebiotics gained interest in the area of animal nutrition and health. Oligosaccharides are compounds that consist of groups of monosaccharides ranging in length from 2 to 60 and are linked by ß-(2,1) bonds that prevent hydrolytic digestion in the upper gastrointestinal tract of monogastric animals. The majority of oligosaccharide compounds ingested survive intact to the lower gut where colonic and cecal bacteria can ferment them to produce short-chain fatty acids (Molis et al., 1996).

There are several classifications of oligosaccharides, all of which are based upon the monosaccharides (glucose, fructose, galactose, mannose, etc.) that compose the basic structure. The fructooligosaccharides are perhaps the most studied oligosaccharides in the realm of human nutrition. There are 3 compounds that have received the most attention: inulin, oligofructose, and short-chain fructooligosaccharides (SCFOS). These 3 compounds exhibit similar nutritional properties (Carabin and Flamm, 1999). The main difference lies in their varying degrees of polymerization. Inulin is the largest molecule ranging in length from 2 to 70 fructose units and a terminal glucose moiety with an average degree of polymerization of 10. Oligofructose is a product of partial enzymatic hydrolysis of chicory inulin yielding a compound of less than 10 monosaccharide units and has an average degree of polymerization of 4. Finally, SCFOS consists of a sucrose molecule to which 1, 2, or 3 additional fructose units have been enzymatically linked by ß-(2,1) bonds to the fructose unit of sucrose and has an average degree of polymerization of 3.5.

In broiler chickens fed a diet containing 2.0 or 4.0 g/kg of fructooligosaccharides (FOS), the cecal concentration of bifidobacteria and lactobacilli was increased and the concentration of E. coli was decreased at 49 d of age (Xu et al., 2003). The same authors found no effect on cecal microbes when FOS was fed at 8 g/kg and further concluded that this level was the highest that could be fed without negatively affecting growth performance. It has been reported that the optimal level to supplement FOS to broiler chickens to increase BW gain and feed efficiency was between 2.5 and 5.0 g/kg (Xu et al., 2003). That study also showed FOS at 10 g/kg caused diarrhea and decreased overall performance of broiler chickens.

In the realm of animal nutrition, the compound that has received the most attention is mannanoligosaccharide (MOS). This compound is derived from the cell wall of yeast organisms (Saccharomyces cerevisiae). Rosen (2005) conducted a holo-analysis for MOS and included an excellent comprehensive evaluation of MOS in turkey research. Likewise, a meta-analysis was conducted by Miguel et al. (2004) and is an excellent comprehensive evaluation of MOS in swine research. Guclu (2003) evaluated MOS at 0.8 and 1.1 g/kg in Japanese quail and found an improvement in weight gain and feed efficiency. Sims et al. (2004) fed 1 g of MOS/kg from 1 to 6 wk of age and 5 g of MOS/kg from 7 to 18 wk to turkeys and found an increase in BW at 18 wk. Stanczuk et al. (2005) tested 1 and 4 g of MOS/kg in turkeys from 8 to 16 wk of age and found no effect on growth performance. Weight gain and feed efficiency were improved in broilers fed 1.7 g of MOS/kg from 1 to 21 d; however, this effect was not carried through to 42 d of age (Pelicano et al., 2004).

Another class of oligosaccharide is transgalactooligosaccharide (TOS). This is a synthetic compound produced from lactose by enzymatic transgalactosylation. Transgalactooligosaccharide consists of lactose and several galactose molecules that are resistant to digestion by intestinal ß-galactosidase and enter the lower gut intact (Alles et al., 1999).

Because the compounds discussed above are indigestible by monogastric animals, there is a concern that supplementing the diet with them could have a negative effect on the digestibilities of other nutrients, particularly when higher levels are fed. The effects of oligosaccharides on nutrient digestibilities in chickens have not been evaluated. Therefore, the purpose of this study was to evaluate the effect of each of the previously discussed oligosaccharides, in a semipurified diet containing little or no oligosaccharides, on the true digestibility of amino acids and TMEn in cecectomized and conventional roosters.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 REFERENCES
 
The University of Illinois Committee on Laboratory Animal Care approved all procedures. This study utilized cecectomized and conventional Single Comb White Leghorn roosters (Parsons, 1985). The use of cecectomized roosters removes most of the fermentative capacity of the avian gastrointestinal tract, allowing for the more accurate measurement of amino acid digestibility without most of the confounding effects of cecal microbes. Amino acid digestibility and TMEn were also determined in conventional roosters, and the nitrogen correction was made using a factor of 8.22, which is the energy content (kcal) of uric acid per gram of nitrogen. A 30-g sample of each of 11 diets was tube-fed to 4 cecectomized roosters and 4 conventional roosters. The roosters were individually housed and fasted for 24 h prior to the start of the experiment (Parsons, 1985). For determination of TMEn and true amino acid digestibility, all excreta voided over the following 48 h were collected and freeze-dried. Feed and excreta samples were then finely ground using a Braun coffee grinder (model KSM2, Gillette, Boston, MA) and analyzed for gross energy using an adiabatic bomb calorimeter (Parr Instrument Co., Moline, IL). Analysis of nitrogen was performed using the Kjeldahl procedures of the Association of Official Analytical Chemists (2000; ; 7.015). Amino acid concentrations in feed and excreta were determined at the University of Missouri—Columbia experiment Station Chemical Laboratory (AOAC, 2000; 982.30 E [a, b]). Performic acid oxidation (AOAC, 2000; 982.30 E [b]) was conducted prior to acid hydrolysis for the determination of methionine and cystine, whereas all other amino acids were determined following acid hydrolysis only.

The composition of the basal corn-isolated soy protein (ISP) diet [Ardex AF (66-960), Archer Daniels Midland Co., Decatur, IL] is shown in Table 1Go. Isolated soy protein was used instead of soybean meal to remove any confounding effects of the oligosaccharides found in soybean meal. The oligosaccharides evaluated were inulin, oligofructose, SCFOS, MOS, and TOS. Each oligosaccharide was added to the corn-ISP basal diet at 4 and 8 g/kg in place of cornstarch. Because Xu et al. (2003) reported that 8 g/kg of an oligosaccharide was the highest level that could be included in a diet without reducing the performance of broilers, it was of interest to determine if nutrient digestibility would be influenced when an oligosaccharide was included in the diet at this level.


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  		Table 1. Composition of the basal diet fed to cecectomized and conventional roosters
 
All data were analyzed by the GLM procedure of SAS (SAS Institute Inc., 1990). If the F-test for treatment effects was significant, differences among treatment means compared to the basal diet were determined using the least significant difference test (Carmer and Walker, 1985). Significance was noted when P < 0.05.


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
REFERENCES
 
In general, the prebiotic additions had little overall effect on amino acid digestibilities in cecectomized and intact roosters, although improvements in isoleucine, lysine, methionine, and valine digestibilities were observed, primarily in cecectomized birds fed MOS or TOS, whereas inulin depressed methionine digestibility in intact roosters (Table 2Go). The true digestibility of lysine and valine was increased (P < 0.05) in cecectomized roosters fed 8 g/kg of MOS or TOS when compared with roosters fed the control diet. In addition, methionine digestibility was improved (P < 0.05) in cecectomized roosters fed 4 g/kg of MOS or SCFOS and 8 g/kg of oligofructose or TOS. The true digestibility of isoleucine was increased (P < 0.05) in cecectomized roosters fed 8 g/kg of MOS or 4 or 8 g/kg of TOS. The magnitude of the increases in amino acid digestibility coefficients for cecectomized roosters ranged from 3 to 9 percentage units. Thus, there was no negative impact of an oligosaccharide on true amino acid digestibility in cecectomized roosters, and, in some cases, amino acid digestibility and absorption in the small intestine were improved when an oligosaccharide was included in the diet, even at the higher concentration of 8 g/kg. The reason for the improvement in amino acid digestibility is unknown. It is possible that the oligosaccharides improved the microbial ecology of the intestine, thereby reducing digesta passage rate and improving amino acid digestibility.


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  		Table 2. True amino acid digestibility coefficients (%) for cecectomized and conventional roosters and TMEn (kcal/g of DM) for conventional roosters fed oligosaccharides1
 
In conventional roosters, the only significant effect on true amino acid digestibility was found for methionine in roosters being provided inulin at 4 or 8 g/kg (88.7 and 90.0%, respectively, vs. 93.3% in the basal diet). Thus, methionine digestibility was lower in these 2 treatments than the basal diet; however, for all other amino acids, digestibility coefficients were similar (P > 0.05) to the basal diet. The negative effect of inulin on methionine digestibility in conventional roosters may have been due to increased bacterial mass and protein in the feces (see later discussion).

Researchers have reported the effects of oligosaccharides on digestive enzyme activities, intestinal microflora, gut morphology, and growth performance of various animals, but to our knowledge, this is the first study evaluating digestibility of individual amino acids in poultry. Several reports have been published in companion animals evaluating the apparent total tract digestibility of CP. These reports using dogs have shown that supplementing oligofructose at 9 g/kg of the diet decreased total-tract crude protein digestibility (Flickinger et al., 2003; Propst et al., 2003). Propst et al. (2003) also reported that dogs fed inulin (9 g/kg) had a decreased total-tract CP digestibility (79.0 vs. 81.7%) when compared with an unsupplemented basal diet. In contrast, Swanson et al. (2002a, b) reported no effects of lower levels of fructooligosaccharide or MOS (2 g of each per day) on ileal and total-tract apparent CP digestibility. Wolf et al. (1998) hypothesized that when a fermentable carbohydrate, such as inulin or oligofructose, reached the hindgut, the bacterial mass in the hindgut increased due to increased energy (the oligosaccharide) reaching the hindgut. When carbohydrates are limited in the hind-gut, bacteria increase fermentation of amino acids to short-chain fatty acids and ammonia to obtain energy (Russell et al., 1991); however, when energy is sufficient, the luminal concentration of nitrogenous compounds decreases and the concentration of fecal nitrogen (bacterial mass) increases (Cummings et al., 1979; Cummings and Bingham, 1987). The latter caused a decrease in amino acid digestibility, particularly when high levels of an oligosaccharide were fed and may explain why the oligosaccharides generally had a more positive effect on amino acid digestibility in cecectomized roosters than in conventional roosters in the current study.

The TMEn of diets supplemented with 4 or 8 g/kg of select oligosaccharides was not significantly (P > 0.05) affected (Table 2Go), although roosters fed the diet containing 4 g/kg of inulin had higher (P = 0.06) values when compared with the basal diet (4.077 vs. 3.674 kcal/g). All other dietary treatments were similar to the basal.

In conclusion, adding several oligosaccharides at 4 or 8 g/kg to a corn-ISP diet generally had little overall effect on true amino acid digestibility and TMEn in cecectomized or conventional roosters. Moreover, in some instances amino acid digestibility was improved by the oligosaccharides in cecectomized roosters. Therefore, these oligosaccharides can be supplemented at 4 or 8 g/kg without compromising the ability of adult poultry to digest or utilize amino acids and energy.

Received for publication October 27, 2006. Accepted for publication February 3, 2007.


   REFERENCES
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 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
Alles, M. S., R. Hartemink, S. Meyboom, J. L. Harryvan, K. M. Van Laere, F. M. Nagengast, and J. G. Hautvast. 1999. Effect of transgalactooligosaccharides on the composition of the human intestinal microflora and on putative risk markers for colon cancer. Am. J. Clin. Nutr. 69:980–991.[Abstract/Free Full Text]

Association of Official Analytical Chemists. 2000. Official Methods of Analysis. 17th ed. Assoc. Off. Anal. Chem., Arlington, VA.

Carabin, I. G., and W. G. Flamm. 1999. Evaluation of safety of inulin and oligofructose as dietary fiber. Regul. Toxicol. Pharmacol. 30:268–282.[ISI][Medline]

Carmer, S. G., and W. M. Walker. 1985. Pairwise multiple comparisons of treatment means in agronomic research. J. Agron. Educ. 14:19–26.[Medline]

Cummings, J. H., and S. A. Bingham. 1987. Dietary fiber, fermentation and large bowel cancer. Cancer Surv. 6:601–621.[ISI][Medline]

Cummings, J. H., M. J. Hill, E. S. Bones, W. J. Branch, and D. J. A. Jenkins. 1979. The effect of meat protein and dietary fiber on colonic function and metabolism. II. Bacterial metabolites in feces and urine. Am. J. Clin. Nutr. 32:2094–2101.[Free Full Text]

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Gibson, G. R., and M. B. Roberfroid. 1995. Dietary modulation of the human colonic microbiota—Introducing the concept of prebiotics. J. Nutr. 125:1401–1412.[Abstract/Free Full Text]

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Parsons, C. M. 1985. Influence of caecectomy on digestibility of amino acids by roosters fed distillers’ dried grains with solubles. J. Agric. Sci. (Camb.) 104:469.

Pelicano, E. R. L., P. A. de Souza, H. B. A. de Souza, F. R. Leonel, N. M. B. L. Zeola, and M. M. Boiago. 2004. Productive traits of broiler chickens fed diets containing different growth promoters. Rev. Bras. Cienc. Avic. 6:177–182.

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Russell, J. B., R. Onodera, and T. Hino. 1991. Ruminal protein fermentation: new perspectives on previous contradictions. Pages 681–697 in Physiological Aspects of Digestion and Metabolism in Ruminants. Proc. Seventh Int. Symp. Rumin. Physiol. Academic Press, New York, NY.

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