Ileal carbohydrate digestion in broiler chickens and humans.

Abstract

17 Ileal carbohydrate digestion in broiler chickens and humans D. Pettersson, A. M�llertz and A. Ohmann Novo Nordisk A/S, Novo All& DK-2880 Bagsvaerd, Denmark Summary Ileal digestibility trials conducted with the marker technique gives accurate information about the degradation of carbohydrates in the upper gastro intestinal tract. The marker technique gives negative digestibility values for the indigestible fibre polysaccharides, which reflects the actual accumulation of these components that occurs in the small intestine of monogastric animals. For easily absorbed components such as starch, which is almost completely absorbed in the small intestine, the marker technique gives excellent results, which also are corroborated by quantitative digestibility trials with human ileostomists. component) from the dietary fibre definition, although lignin in some cases may be a major cell wall constituent. Supplementation with enzyme preparations to degrade dietary fibre polysaccharide is today a common practice to increase the nutritive and productive value of monogastric diets. Anti-nutritional effects of the dietary fibre are thereby reduced, or eliminated, leading to considerable performance improvements in animals fed diets that are rich in e.g. arabinoxylans or mixed `linked' Pglucans. The current paper will discuss the digestion of starch and structural polysaccharides in monogastric animals, including humans. Introduction Plant Carbohydrates may be divided into two major groups, storage and structural. Starch is the principal storage carbohydrate in cereal grains and in many legumes and is presumably the only polysaccharide formed in the plastids. Starch is the major energy source in cereal based monogastric diets and is easily degraded and efficiently absorbed in the digestive tract. Structural non-starch polysaccharides may also serve as storage carbohydrates and are as such stored in the cell vacuoles or outside the plasmalemma (Meier and Reid, 1982). Such storage polysaccharides may be found e.g. in some seeds, roots, tubers and leaves. Although not available for absorption in the small intestine non-starch polysaccharides of storage or structural type may still to a very large extent determine the nutritive value of monogastric diets by virtue of their physiological effects. Also, the way in which they build up the cell wall architecture may be of great importance. Structural polysaccharides are commonly referred to as dietary fibre. Dietary fibre is defined physiologically as plant polysaccharides plus lignin, which are resistant to hydrolysis by the digestive enzymes of man (Trowel1 et al. 1976). It has however been suggested to exclude lignin (the non-carbohydrate Recent Advances in Animal Nutrition in Australia 7997 University of New England, Armidale NSW 235 7, Australia Experiments In two experiments using the Cr,O, marker technique the effects on carbohydrate digestion were studied in broiler chickens fed diets containing deacetylated chitin, also referred to as chitosan (Trial 1). In Trial 2, a rye bran based diet, with or without supplementation of a dietary fibre degrading enzyme, was fed to broiler chickens. In addition, a total collection study with ileostomy subjects (Trial 3) receiving a high fibre diet containing rye was conducted in order to study the effects on quantitative digestion and excretion of carbohydrate components. Dietary fibres were analysed by the Uppsala method for dietary fibre analysis (Theander et al. 1995) and starch (including glucose, maltose and maltoolgosaccharides) according to Aman et al. (1995). Trial 1 The composition of the diets used in Trial 1 (Razdan and Pettersson 1994) is displayed in Table 1. Production parameters were registered at day 2 1 and the digestibility study was conducted at day 23. One randomly selected bird from each of the four cages allocated per treatment was slaughtered by cervical dislocation. Thereafter, culling occurred every fourth hour for a further 20 h. Contents of the last third of the small intestine (denoted 18 Petterson et al. ileum) were collected separately, pooled for each cage, frozen and freeze-dried. Digestibility rates were calculated relative to the Cr,O, marker included at 4 g/ kg diet. Results fi=om Trial 1 are displayed in Table 2. In general diets containing chitosan significantly reduced broiler chicken live weights and feed conversion was also generally inferior. Chitosan feeding did not influence ileal startch digestibility rates. As indicated by the high negative digestibility rates for arabinose, xylose and glucose residues as well as uranic acids, an apparent accumulation of these components occurred in the small intestine as a result of feeding the viscous chitosan polymer. Trial 2 Table 1 Composition of the control broiler chicken diet. The composition of the diets used in Trial 2 (Pettersson et al. 1994) is displayed in Table 3. Production parameters were registered at day 2 1 and the digestibility study was conducted at day 23. Six randomly selected birds from each of the four cages allocated per treatment were slaughtered by cervical dislocation. Contents of the last third of the small intestine (denoted ileum) were collected separately, pooled for each cage, frozen and fieezedried. Digestibility rates were calculated relative to the Cr,O, marker included at 4.0 g/kg diet. Table 3 Composition of the diets used in the production and ileal digestibility studies. Table 2 Production parameters and ileal carbohydrate digestibility rates (%) in broiler chickens fed deacetylated chitin (chitosan) differing in deacetylation and viscosity. The results from Trial 2 are shown in Table 4. As a result of enzyme supplementation, significant improvements in all production parameters were registered. The digestibility rates of all neutral dietary fibre polysaccharide residues, as well as total dietary fibres, were significantly improved on enzyme supplementation. As a result, positive digestibilty values were obtained for all neutral dietary fibre residues indicating a degradation of these components. Ileal starch digestibilty was also significantly improved by enzyme addition. Ileal carbohydrate digestion in broiler chickens and humans 19 Trial 3 Six men and two women who had been proctocolectomized for ulcerative colitis participated in the study (Pettersson et al. 1996). The subjects received a rye containing diet high in dietary fibre. The content (g/kg diet) in 1 portion ofthis high fibre diet was; protein 97.9, fat 88.8 and carbohydrates (including dietary fibre) 245.9. Subjects received the diet for a period of 3 weeks. Ileostomy effluents were collected during a 24 h collection period. This procedure was repeated at three different occasions (day 3, day 17 and day 18 of the experimental period). Comparisons between intake and excretions were made by Wilcoxon's signed rank matched-pairs test . Differences were considered significant at a probability level of PcO.0 1. The average daily excretion of enzyme available starch was 4.1 g which constituted only 1.6 % of the amount of starch ingested (Figure 1). The three major dietary fibre polysaccharide residues ingested by subjects were arabinose, xylose and glucose (Figure 2). The ileal excretion of uranic acids was 188 % of the arnounts ingested. Discussion In the present three trials the digestibility rates of starch were high, indicating an almost complete absorption of this component by the end of the small intestine. The results regarding starch digestion obtained in the animal experiments using the marker technique were also corroborated by the quantitative sampling technique used in the ileostomy study. These results demonstrate that the marker technique works well for estimating intestinal absorption. However, it produces negative digestibility values for dietary fibre polysaccharide residues which may seem confusing. These values, however, are merely a reflection of the fact that dietary fibre is not absorbed in the small intestine and consequently is enriched relative to the content found in the diet, when calculated per gram freeze dried digesta. Negative values may also be obtained depending on the transit time of the soluble and insoluble dietary fibre polysaccharides but are still not incorrect and actually indicates whether or not passage rates are altered due to the viscous properties of the dietary fibre fraction. This becomes particularly notable when examining the results obtained in Trial 1, where high negative digestibility coefficients were obtained for the major 20 Petterson et al. dietary fibre polysaccharides in birds fed the highly viscous chitosan preparation. Also, in Trial 2, negative digestibility values were obtained for dietary fibre . polysaccharide residues in birds fed the rye bran diet without enzyme supplementation. On enzyme supplementation of this diet, positive digestibility values were obtained, due to the enzyme mediated degradation of the dietary fibre polysaccharides, which would cause degradation of these components into short polysaccharide chains with DP<lO. Such tiagments will not be precipitated in 80 % aqueous ethanol and are consequently not recovered in the dietary fibre analysis. Negative digestibility values for uranic acids were still obtained in both animal experiments due to the endogenous excretion of these components, which also is clearly demonstrated in Trial 3 and well known from human experiments (Danielsson and Sjovall, 1975; Aman et al. 1995). Ileal digestibility trials using modem methods of carbohydrate analyses may considerably improve our knowledge on the mode of action of dietary fibres and also provide information about the efficacy of dietary fibre degrading enzyme preparations used in order to upgrade the nutritive value of diets for monogastrics. It is today, well acknowledged that viscosity measurements of digesta are not always a good predictor for animal performance at low digesta viscosity values (Cowan et al. 1996). Therefore, future development work on enzymes for improving the nutritive value of cereals or oil seeds and pulses will require the use of modem methods for carbohydrate analyses in order to better monitor the release and degradation of the carbohydrates that build up the cell wall matrix in different feed components. Viscosity measurements alone are not a sufficient tool for estimating the efficacy of a dietary fibre degrading enzymes since viscosity is easily reduced by simply breaking a few bonds in a soluble polysaccharide chain. In order to obtain maximum nutrient absorption an efficient solubilisation and degradation of the cell wall matrix in order to release enclosed nutrients is required. This demands a complex blend of different enzymatic activities. As a consequence more complex methods of analysis are required in order to describe the effects of these activities on the dietary carbohydrate fiaction. References Aman P.,Pettersson, D., Zhang, J-X., Tidehag, P. and Hallmans, G. (1995). Excretion and degradation of starch and dietary fiber components in ileostomy subjects consuming mixed diets with bread of wheat or oat-bran. Journal of Nutrition 125,2341-2347. Cowan, W.D., Korsbak, A., Hastrup, T. and Rasmussen, P.B. (1996). Influence of added microbial enzymes on energy and protein availability of selected feed ingredients. Animal Feed Science and Technology 60, 311-319. Danielsson, H. and Sjiivall, J. (1975). Bile acid metabolism. Annual Reviews of Biochemistry 881,233-253. Meier, H. and Reid, J.S.G (1982). Reserve polysaccharides other than starch in higher plants. In Plant Carbohydrates I, Intracellular Carbohydrates, pp. 418-47 1 .(Eds F.A. Loewus and W. Tanner). Springer Verlag: Berlin, Heidelberg and New York. Pettersson, D., Aman, P. and Frig&rd. T. (1996). In vitro and in vivo studies on digestion of dietary fibre components in a broiler chicken diet based on rye. Journal of the Science of Food and Agriculture 66, 267-272. Pettersson, D., Aman, P., Bach Knudsen, K. E., Lundin, E., Zhang, J.-X., Hallmans, G., H%rkonen, H. and Adlercreutz, H. (1995). Intake of rye bread by ileostomists increases ileal excretion of fiber polysaccharide components and organic acids but does not increase plasma or urine lignans and isoflavonoids. Journal of Nutrition 126,1594-l 600. Razdan, A. and Pettersson, D. (1994). Effect of chitin and chitosan on nutrient digestibility and plasma lipid concentrations. British Journal of Nutrition 72,277288. Theander, O., Aman, P., Westerlund, E., Andersson, R. and Pettersson, D. (1995). Total dietary fiber determined as neutral sugar residues, uranic acid residues, and I&son lignin (the Uppsalamethod): Collaborative study. Journal of Association of Oficial Analytical Chemists International 78, 1030-1044. Trowel& H., Southgate, D.A.T., Wolever, T.M. S., Leeds, A.R:, Gassull, M.A. and Jenkins, D.J.A. (1976) Dietary fibre redefined. Lancet i, 967.