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The role of dietary fibre in the digestive physiology of the pig
Animal Feed Science and Technology 90 (2001) 21±33
The role of dietary ®bre in the digestive physiology of the pig Caspar Wenk* Institute of Animal Sciences, ETH ZuÈrich, UniversitaÈtstr. 2, CH-8092 ZuÈrich, Switzerland
Abstract Dietary ®bre (DF) is usually de®ned as the sum of plant polysaccharides and lignin that are not hydrolysed by endogenous enzymes of the mammalian digestive system (non-starch polysaccharides and lignin). The amount and composition of DF varies over a wide range between and within feedstuffs. Furthermore, a precise distinction between dietary ®bre and starch is far from easy. Therefore, the analysis as well as the physiological function of DF in the digestive tract of the pig can vary considerably. The age or body mass of the pig also interacts with the digestive processes and there is an adaptation developing in the animal over the time of exposure to ®brous diets. DF is generally considered as a fraction with a low energy content. This diluting effect of the diet is used to increase the feed intake during low performance of animals. DF in¯uences transit time with a reduction in the upper and increase in the lower digestive tract and, therefore, decreases the digestibility of almost all nutrients and energy. On the other hand, it increases the microbial growth in the gastrointestinal tract. This can lead to an increased excretion of nutrients in faeces. Finally, DF bene®cially in¯uences well-being and health. Fibrous feedstuffs give pigs the opportunity to chew the feed over a longer time. More short chain fatty acids are produced and eventually undesired micro-organisms are excluded. A regular peristaltic action avoids the possibility of constipation. # 2001 Elsevier Science B.V. All rights reserved. Keywords: Dietary ®bre; Pigs; Nutrients; Energy; Digestion
1. Digestive system of the pig and its micro¯ora The processes in the digestive tract of farm animals are of great importance in the understanding of the in¯uence of nutrition on metabolism. In comparison to ruminants, non-ruminant animals have a 'simple' stomach, in which only slight microbial modi®cations of available nutrients take place before absorption occurs. Micro-organisms *
Tel.: 41-1-632-32-55; fax: 41-1-632-11-28. E-mail address: [email protected] (C. Wenk). 0377-8401/01/$ ± see front matter # 2001 Elsevier Science B.V. All rights reserved. PII: S 0 3 7 7 - 8 4 0 1 ( 0 1 ) 0 0 1 9 4 - 8
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Fig. 1. Comparison of the digestive tract of cattle, pigs and poultry.
are in contact with undigested materials or endogenous substrates to a considerable degree mainly in the lower parts of the digestive tract, from the terminal ileum to the rectum and the products of this microbial fermentation may partly be absorbed by the host animal. Most digestive processes in non-ruminant animals occur under anaerobic conditions. Feed digestion depends on the quantity and composition of the diet. The size and function of the organs of the digestive tract as well as the digesta retention time in different parts of the GI tract are further important characteristics. In Fig. 1, the digestive tract of the pig is schematically presented in comparison with that of cattle and poultry. The digestive tract of the pig can be divided mainly into three different compartments: the stomach, small intestine and the large intestine. Stomach represents about 30% of the total volume of the digestive tract. In this part, digestion begins with a lowering of the pH. Some microbial activity may occur in the upper part of the stomach, but only if the pig ingests a high quantity of feed. In the stomach only a limited mixing of food occurs. Compared to other farm animals, the small intestine of pigs is long and permits an intensive endogenous digestion at an almost neutral pH. In the lower ileum and especially the caecum and lower large intestine (third compartment), an intensive microbial degradation takes place. In pigs, most available nutrients (protein, carbohydrates, fat, minerals and vitamins) are absorbed in the small intestine. In the large intestine, undigested feed components (mainly dietary ®bre, lipids with a high melting point and insoluble proteins) and endogenous secretions are fermented by micro-organisms. In this part, only short chain fatty acids (SCFA) and some vitamins can be absorbed which can contribute to the nutrient supply of the animal.
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Fig. 2. Types and density of micro-organisms in the digestive tract of pigs.
The chicken, in comparison, has a crop before and a gizzard (a muscular stomach) below the true stomach (proventriculus), in which glands release endogenous secretions. Microbial activity in the crop becomes important if the feed remains for a longer period in this organ. In poultry, the microbial activity is low in the small intestine, due to its small size and the high rate of passage. In the large intestine, the rate of passage in comparison to the pig is also faster, thus, limiting intensive microbial degradation. The pig as a non-ruminant animal has only a small population of micro-organisms in the stomach relative to the lower parts of the digestive tract. Furthermore, it should be noted that ingested feed remains only for a short period of time in the stomach. Therefore, microbial activity is rather limited. In the lower parts of the small intestine and mainly in the large intestine, an increased number of micro-organisms can be found. As shown in Fig. 2, the population density for certain species of micro-organisms in the caecum and colon reaches the level of 1010 (or even higher) per g 1 digesta. Microbial growth and its metabolic turnover depends on several conditions. Body temperature offers optimal conditions. It also depends on the presence of substrates that can be metabolised. The substrates that will be made available can depend on the number of meals and the composition as well as the structure and technological treatment of the diets. These factors particularly in¯uence digestion in the upper part of the digestive tract. In the search for nutrients, the micro-organisms of different species are in a continuous competition. Furthermore, the endogenous digestion processes (with the secreted enzymes) affect microbial growth. The change of pH in the stomach and later in the small intestine is also a limiting factor for micro-organisms. Finally, the rate of passage of digesta does limit microbial processes in different parts of the digestive tract. Jùrgensen and Just (1988) have used ATP-concentration in the digesta at different parts of the digestive tract in pigs fed two different diets as an indicator of microbial activity in the GI tract. One diet was mainly based on wheat ¯our. While, the other contained wheat bran in addition to the wheat ¯our. The second diet contained a higher level of dietary ®bre than the ®rst.
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Fig. 3. ATP-concentration in the digesta of pigs as affected by dietary ®bre.
For both diets, the ATP-concentration in the stomach was low (Fig. 3). With the diet containing only wheat ¯our, a rapid increase in ATP-concentration could already be observed in the jejunum, which reached a maximum at the end of the ileum followed by a sharp decrease in the caecum. There was almost no ATP detected in the colon. The shape of this curve indicates that, in the diet with a low ®bre content, the maximum microbial activity was observed at the end of the small intestine. Obviously due to the lack of substrates, microbial activity decreased rapidly. In line with the ®rst diet, an increased microbial activity was also observed in the small intestine with the second diet, which contained wheat bran. However, the maximum ATP-concentration was observed at the end of caecum which decreased slowly, but continuously during the latter part of the large intestine. This slow decrease of ATP-concentration indicates that a high microbial activity was maintained throughout the large intestine. As a whole, the microbial activity with the diet containing wheat bran was far greater than with the diet that had a low ®bre content. With the secretion of enzymes and other substances for endogenous digestion in different parts of the digestive tract (saliva in the mouth, gastric juice in the stomach, pancreatic juice and secretions of the small intestine), macronutrients are digested so that the monomers for carbohydrates and/or oligomers for protein and lipids can be absorbed in the small intestine (Fig. 4). Micro-organisms synthesise short chain fatty acids (SCFA) from unabsorbed nutrients. These can subsequently be absorbed and metabolised by the pig. According to experiments of MuÈller and Kirchgessner (1985), two-thirds of microbial fermented organic matter can be utilised by the host animal. Beside SCFA, other ®nal end-products of microbial metabolism (like NH3, CH4, H2O) can be found. Some of them are also absorbed, but not utilised in the intermediate metabolism. In the pig, most nutrients that are incorporated in the micro-organisms will be excreted with faeces. These include microbial protein. Since dietary ®bre by de®nition cannot be digested by endogenous processes, it is mainly micro-organisms that will metabolise them. Therefore, it can be concluded that most digested dietary ®bre will be utilised with
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Fig. 4. Competition between enzymes in the digestive tract.
a reduced ef®ciency as reported by MuÈller and Kirchgessner (1985). Undigested dietary ®bre will be excreted in faeces. Finally, the rate of absorption of different carbohydrates depends directly on the mechanisms available. Na-dependent active transport mechanisms with a high ef®ciency are available for glucose and galactose. Fructose is absorbed with a facilitated mechanism. If high amounts of fructose are present in digesta, the facilitated diffusion will be insuf®cient for an ef®cient absorption, and therefore, a large part of fructose will be passed to the large intestine and metabolised by micro-organisms. Other monosaccharides such as mannose are only absorbed by simple diffusion which is even slower than facilitated diffusion or sodium-dependent active transport mechanisms. Therefore, these monosaccharides will mainly be absorbed and metabolised by microorganisms in the digestive tract. 2. Dietary ®bre and the digestion processes In diets for pigs, dietary ®bre is usually an integral part. It is not added as such and, therefore, the contribution of dietary ®bre to the digestive processes has to be considered in relation to its origin. Usually, an increased ®bre content of a diet is directly related to the amount of available nutrients and energy. A diet with a high ®bre content usually contains less metabolisable energy than a diet with a low ®bre content. This means that a diet with a high ®bre content causes earlier satiety of an animal due to gastric signals than a diet with a low ®bre content caused by elongation of the stomach wall (Langhans, 1999). This earlier satiety is of particular importance in pregnant sows. On the other hand, in growing ®nishing pigs, a diet with a low ®bre content will be preferred as this results in maximum intake of available nutrients and energy. An animal that reaches both satiety physically and nutritionally, is less stressed and, therefore, physical activity may be reduced (Rijnen et al., 1999). A diet with a high content of soluble ®bre will cause more water binding in the stomach than a diet with a low ®bre content or with insoluble ®bre. A high amount of soluble dietary ®bre causes an increased volume of digesta in the stomach and, therefore, reduces both satiety and digesta transit time in this organ. Furthermore, in such situations,
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Fig. 5. Post-prandial pH-values (in stomach fundus) after meals with a low or high ®bre content in pigs (Drochner and Coenen, 1986).
the viscosity of digesta is increased and the pH is stabilised at a low level (Fig. 5) (Drochner and Coenen, 1986; Van der Meulen and Bakker, 1991). In an experiment carried out with growing pigs, Drochner and Coenen (1986) studied the pH in the post-prandial state in the fundus region of the stomach after feeding diets containing low and high levels of ®bre. While, the pH with the high ®bre diet remained almost constant at about 2.5, it rapidly increased to four, when pigs were fed the low ®bre diet. The pH value subsequently decreased gradually to a level similar to that with the high ®bre diet over the next 6 h. Johansen et al. (1996) also reported increased viscosity and water binding capacity of stomach contents in pigs. Dietary ®bre in¯uences the intestinal morphology as well as the rate of intestinal cell turnover in pigs (Jin et al., 1994), which ultimately can affect nutrient digestion, absorption and metabolism. Diets with a high ®bre content also cause a signi®cant increase in the secretion of endogenous ¯uids. This was clearly shown in experiments of Zebrowska et al. (1983) in which pigs were fed two diets with an identical crude ®bre content. In treatment 1, the puri®ed diet contained 50 g kg 1 DF in the form of cellulose, but almost no soluble ®bre. In treatment 2, the diet was based on barley and soybean meal and contained the same amount of crude ®bre, but far more dietary ®bre than in treatment 1. As shown in Table 1, the increase in the dietary ®bre content from 50 to 180 g kg 1 (mainly soluble dietary ®bre) caused a doubling of the secretion of saliva and gastric juice in the pigs of 50 kg liveweight. Not only were the secreted ¯uids of the upper digestive tract increased, but pancreatic juice was almost doubled with the increased dietary ®bre; bile was also signi®cantly increased. The increased amount of secreted digestive ¯uids means an extra metabolic effort or demand for the pig. On the other hand, a more ef®cient digestibility of the feed can be expected. The results of similar experiments reported by Mosenthin et al. (1994) with pectin as a source of soluble dietary ®bre con®rm the ®ndings of Zebrowska et al. (1983). Most probably the increased secretion of digestive ¯uids is associated with a higher activity of secretory organs resulting in enlargement of such organs. Jùrgensen et al. (1996) reported signi®cantly heavier stomach, caecum and colon and also longer colon in growing-®nishing pigs fed diets containing high dietary
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Table 1 Dietary ®bre and endogenous secretions in the digestive tract of pigs weighing approximately 50 kga Ingredients
Crude ®bre Dietary ®bre, g.kg 1 Saliva and gastric juice, 3 per day Pancreatic juice, 3 per day Bile, 3 per day a
Purified diet 1
Normal diet 2
Casein, starch, cellulose, vitamin mineral premix
Barley, soybean meal, fish meal, vitamin mineral premix
Identical 50 4 1.2 1.2
Identical 180 8 2.2 1.7
Adapted from Zebrowska et al., 1983.
®bre (268 g kg 1 DM) as compared to those fed a diet containing low (59 g kg 1 DM) dietary ®bre. Improved digestibilities of protein, dry matter and energy were, however, not associated with this modi®cation, values in fact decreased. A high ®bre content of digesta increases peristaltic action and, therefore, reduces the transit time in the small as well as in the large intestine. Jùrgensen et al. (1996) reported a ®ve to six fold increase in the ¯ow of digesta through the terminal ileum of pigs fed high dietary ®bre. Dietary ®bre is a powerful tool against constipation especially in pregnant sows. Unligni®ed soluble dietary ®bre is a nutrient source for pigs. Dietary ®bre is not digested by endogenous processes by the pig, but ef®ciently by the microbial ¯ora. Although, starch from cereals can be almost completely digested by the time the digesta reaches the ileum, Bach Knudsen (1991) observed that a greater proportion of wheat soluble ®bre passes the ileum in pigs without being digested and, therefore, represents a good substrate for miro-organisms in the large intestine. Similar results have been reported by Gdala et al. (1991), Smits et al. (1991) and Schulz et al. (1998) for other feedstuffs. Therefore, with diets containing a high soluble ®bre content, the microbial activity in the large intestine is generally increased as shown by Jùrgensen and Just (1988) and by Bach Knudsen and Jensen (1991). The increased microbial activity in the digestive tract not only means a better utilisation of feed nutrients, but also an increased excretion of microbial substances. As an ultimate result, soluble dietary ®bre can reduce the absorption of nutrients (Rainbird et al., 1984). However, in pigs, the absorption of trace minerals is mainly reduced. As discussed above, the physiological effects of dietary ®bre on nutrient digestion result in a general reduction in digestibility of energy with increased ®bre content of the diet. This was clearly demonstrated by Wenk (1980), who plotted the results of several digestibility experiments in which different ingredients contributed to an increase in ®bre content, measured as crude ®bre (Fig. 6). In each single experiment a linear reduction of the digestibility of energy was observed with increased ®bre content. In general, a reduction in the coef®cient of gross energy digestibility (d(E)) of 0.025 per 10 g crude ®bre kg 1 dry matter was observed. The reduction of d(E) caused by the crude ®bre content was more pronounced in the diets with dehydrated grass or coffee hulls compared to entire maize plants. The composition of the
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Fig. 6. Coef®cient of digestibility of gross energy of pig diets in relation to the crude ®bre content (Wenk, 1980).
®bre fraction might be an explanation for these differences. For instance maize plants are known to be of low lignin content. Similar observations were made by Henry (1971); Noblet and Perez (1993) and Wenk et al. (1980) con®rmed dietary ®bre as a predominant factor in the determination of available feed energy in pig diets as digestible, metabolisable or net energy. However, according to Low (1993), who reviewed the effects of dietary ®bre on feed intake, digestion, nutrient absorption and metabolism, it may be dif®cult to express practical responses of pigs to high dietary ®bre levels due to the direct and indirect effects of other nutrients in the diet. The digestibility of dietary ®bre is lower in young animals than in adult animals (Noblet and Bach Knudsen, 1991) and the negative effects of dietary ®bre on the digestibility of energy and nutrients are highest in young animals. With increasing weight and especially in adult animals, the detrimental effect of ®bre is reduced (FernaÂndez et al., 1986). Furthermore, this depressing effect is more pronounced in the precaecal compared to the faecal digestibility of nutrients or energy. Drochner (1991) found a regression coef®cient for the apparent digestibility of organic matter of 2.8 for precaecal and 1.8 for faecal digestibility. Similar observations were made by Wenk (1992) who measured the digestibility of organic matter and neutral detergent ®bre (NDF) in digesta samples at different sites of the intestine of pigs fed a diet with a high ®bre content (500 g entire maize plants kg 1) with or without the supplementation of a carbohydrate (noncommercial cellulose) using the indicator method. In these experiments, an increase in digestibility was observed over the whole digestive tract. Furthermore, the enzyme supplementation increased the digestibility of organic matter especially in the small intestine, but also d(NDF) was higher in all parts of the digestive tract (Fig. 7). Pigs do not have the same ability to utilise dietary ®bre from different sources. Noblet and Bach Knudsen (1991) found that the digestibility of various ®bre fractions in sows was higher for maize ®bre and soybean pulp than for wheat bran; digestibility of dietary ®bre was 0.74 and 0.86 for maize ®bre and soybean pulp, respectively, compared to 0.46 for wheat bran. Therefore, it is not only the level of dietary ®bre that is important, but the
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Fig. 7. Coef®cient of digestibility of organic matter and neutral detergent ®bre of a diet with a high ®bre content (500 g entire maize plants kg 1) with and without the supplementation of a carbohydrate splitting enzyme.
type or the source of ®bre also plays a signi®cant role in digestion and absorption. Feeding similar levels of either wheat bran or sugar beet ®bre to pigs did not alter the absorption rate of glucose and amino nitrogen. However, sugar beet ®bre increased hindgut fermentation and, therefore, the absorption of volatile fatty acids (Michel and Rerat, 1998), thus, indicating the source of ®bre has an important effect. In experiments of Wenk and ZuÈrcher (1990), the in¯uence of the ®bre source (namely soybean hulls, barley hulls, pea hulls and sorghum hulls) on the digestibility of energy was studied. The effect of crude ®bre (CF), acid detergent ®bre (ADF), neutral detergent ®bre (NDF) and dietary ®bre (DF) as well as lignin on digestibility was evaluated. The results are summarised in Fig. 8.
Fig. 8. Coef®cient of digestibility of gross energy in relation to the dietary ®bre content (in dry matter) of different origin (Wenk and ZuÈrcher, 1990).
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The digestibility of energy in the control diet was 0.84 and the lowest (d E 0:07) was recorded for sorghum hulls. With the exception of soybean hulls, an almost linear increase in ®bre content (CF, ADF, NDF and DF) was associated with reduced digestibility. The main exception to this trend was found for soybean hulls which had similar levels of CF, ADF, NDF and DF as in sorghum hulls, but far higher energy digestibility (d E 0:64). Only the lignin content was lower in soybean hulls. Therefore, the conclusion was that the ligni®cation of the dietary ®bre in sorghum hulls was associated the low digestibility of energy. The partition of the dietary ®bre into insoluble (ADF or CF) and soluble dietary ®bre (NDF-ADF) was not able to explain that difference. The in¯uence of lignin per se on the digestibility of energy was evaluated in two further experiments by Wenk et al. (1998). The experimental design is shown in Table 2. The lignin sources used were oak bark powder, calcium lignin sulphonate and sulphatefree lignin. The lignin sources are frequently used as dust binders or pelleting enhancers in pig and poultry diets and were added in amounts which corresponded to the same analysed lignin quantity in the diet of about 25 g kg 1. Furthermore, the in¯uence of a cellulolytic enzyme on the nutrient utilisation in relation to lignin supplementation was studied. The experiments were carried out in a latin square design with 12 growing individually kept pigs over the range of 22±105 kg liveweight. Digestibility of energy was measured with the indicator method (HCl ± insoluble ash as the indicator). As shown in Fig. 9, the supplementation of the control diet with the three lignin sources in all cases (except oak bark powder) caused a signi®cant decrease in the digestibility of energy. The most serious reduction was found for the sulphate free lignin. From these experiments and from the earlier observations, it can be concluded that lignin causes a signi®cant reduction of the digestion processes if it is present in the dietary ®bre like sorghum hulls and oak bark powder as well as in the free form of Ca-lignin sulphonate or S-free lignin, two products which are used as pelleting agents in the feed
Table 2 Treatments to estimate the effect of lignin from different origins in combination with a carbohydrate enzyme in pigs (22±105 kg liveweight) diets on the digestion processes Type of the diet Experiment 1 a
Enzyme supplementation Control diet 1 g Oak bark powder kg 1 25 g Ca-lignin sulphonateb kg 50 g Ca-lignin sulphonate g 1 50 g S-free ligninc kg 1 a
1
C O A
Allzyme cellulose, Alltech Inc., Kentucky, USA. Lignobond, Attisholz AG, Gerla®ngen, CH. c Alcell, Repap Inc., Pennsylvania, USA b
Experiment 2 CE OE AE
C
CE
A L
AE LE
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Fig. 9. Coef®cient of digestibility of gross energy in growing pigs fed diets with different lignin sources and a carbohydrate enzyme.
industry. The supplementation of the control diets with the carbohydrate splitting enzyme had no signi®cant effect on the digestibility of energy. As a more general observation, cellulose and insoluble ligni®ed dietary ®bre mainly reduced the faecal transit time and also digestibility of the nutrients (Table 3); effects on the processes in the stomach and on satiety as well as on microbial activity are limited. On the other hand, dietary ®bres with a high solubility, like those from vegetables or fruits, can reduce the transit time for emptying of the stomach and prolong satiety. They increase the microbial activity and reduce the faecal transit time. The detrimental in¯uence of soluble ®bre on nutrients is usually less pronounced than from insoluble dietary ®bre.
Table 3 Effects of dietary ®bre on the digestion processes in animals Type of effect of dietary fibres Source of Slower the dietary ®bre emptying of stomach
Achieving Shortening satiety faecal transit time
Increasing microbial activity
Energy digestibility
Cellulose Insoluble, ligni®ed Vegetables, fruits Pectins/guar
Weak Weak
Weak Weak
Relevant Not existing Very important Weak
Medium
Medium
Weak
Very important Medium
Weak
Very important Relevant
Weak
Very important Medium
Weak
Ileal
Faecal
Very important Very important Very important Very important
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3. Conclusions Dietary ®bre is integral part of all feedstuffs of plant origin for pigs. It has speci®c effects on all digestive processes of the pig and also indirectly on intermediate metabolism. Long-term feeding of high levels of dietary ®bre can alter the anatomical and physiological characteristics of the digestive tract of pigs. Soluble dietary ®bre increases ileal and post-ileal microbial fermentation and a considerable amount of short chain fatty acids produced will be absorbed. These absorbed short chain fatty acids can also have speci®c effects on intermediate metabolism. The level, source and composition of dietary ®bre can therefore be considered as important factors in¯uencing the occurrence as well as the rate of different mechanisms of feed digestion in pigs. The effects of dietary ®bre on feed digestion and nutrient absorption can be highly in¯uenced by the physio-chemical properties of ®bre. Therefore, just looking at the total dietary ®bre level will not give a clear picture about its in¯uence on the digestive physiology of pigs. References Bach Knudsen, K.E., 1991. Breakdown of plant polysaccharides in the gastrointestinal tract of pigs. In: Verstegen, M.W.A., Huisman, J., den Hartog, L.A. (Eds.), Proceedings of the Fifth International Symposium on Digestive Physiology in Pigs, 24±26 April 1991, Wageningen, The Netherlands, pp. 428±433. Bach Knudsen, K.E., Jensen, B.B., 1991. Effect of source and level of dietary ®bre on microbial fermentation in the large intestine of pigs. In: Verstegen, M.W.A., Huisman, J., den Hartog, L.A. (Eds.), Proceedings of the Fifth International Symposium on Digestive Physiology in Pigs, 24±26 April 1991, Wageningen, The Netherlands, pp. 389±393. Drochner, W., 1991. Digestion of carbohydrates in the pig. In: Verstegen, M.W.A., Huisman, J., den Hartog. L.A. (Eds.), Proceedings of the Fifth International Symposium on Digestive Physiology in Pigs, 24± 26 April 1991, Wageningen, The Netherlands (EAAP publication no. 54, 1991), Pudoc Wageningen, pp. 367± 388. È bers. TierernaÈhrg. 14, Drochner, W., Coenen, M., 1986. P¯anzliche Strukturstoffe in der SchweineernaÈhrung, U 1±50. FernaÂndez, J.A., Jùrgensen, H., Just, A., 1986. Comparative digestibility experiments with growing pigs and adult sows. Anim. Prod. 43, 127±132. Gdala, J., Graham, H., Buraczewska, L., Aman, P., 1991. Ileal and faecal digestibility of polysaccharides in pigs fed diets with different varieties of pea. In: Verstegen, M.W.A., Huisman, J., den Hartog, L.A. (Eds.), Proceedings of the Fifth International Symposium on Digestive Physiology in Pigs, 24±26 April 1991, Wageningen, The Netherlands, pp. 447±451. Henry, Y., 1971. Essai de preÂvision de la valeur en eÂnergie digestible des aliments pour le porc aÁ partir de leur teneur en constituants membranaires. JourneÂes Rech. Porcine en France 9, 57±64. Jin, L., Reynolds, L.P., Redmer, D.A., Caton, J.S., Crenshaw, J.D., 1994. Effects of dietary ®bre on intestinal growth, cell proliferation, and morphology in growing pigs. J. Anim. Sci. 72, 2270±2278. Johansen, H.N., Knudsen, K.E.B., Sandstrom, B., Skjoth, F., 1996. Effects of varying content of soluble dietary ®bre from wheat ¯our and oat milling fractions on gastric emptying in pigs. Br. J. Nutr. 75, 339±351. Jùrgensen, H., Just, A., 1988. Effect of different dietary components on site of absorption/site of disappearance of nutrients. In: Buraczewska, L., Buraczewski, S., Pastuszewska, B., Zebrowska, T. (Eds.), Proceedings of the Fourth International Seminar at the Institute of Animal Physiology and Nutrition, Jablonna, Poland, pp. 230±239. Jùrgensen, H., Zhao, X.-Q., Eggum, B.O., 1996. The in¯uence of dietary ®bre and environmental temperature on the development of the gastrointestinal tract, digestibility, degree of fermentation in the hind-gut and energy
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metabolism in pigs, degree of fermentation in the hind-gut and energy metabolism in pigs. Br. J. Nutr. 75, 365±378. Langhans, W., 1999. Appetite regulation. In: Lobley, G.E., White, A., MacRae, J.C. (Eds.), Protein Metabolism and Nutrition, EAAP publication no. 96, Wageningen Pers., The Netherlands, 225±252. Low, A.G., 1993. Role of dietary ®bre in pig diets. In: Cole, D.J.A., Haresign, W. (Eds.), Recent Developments in Pig Nutrition±2, Nottingham University Press, Loughborough, UK, pp. 137±162. Michel, P., Rerat, A., 1998. Effect of adding sugar beet ®bre and wheat bran to a starch diet on the absorption of glucose, amino nitrogen and volatile fatty acids in the pig. Repro. Nutr. Dev. 38, 49±68. Mosenthin, R., Sauer, W.C., Ahrens, F., 1994. Dietary pectin: effect on ileal and faecal amino acid digestibility and exocrine pancreatic secretion in growing pigs. J. Nutr. 124, 1222±1229. MuÈller, H.L., Kirchgessner, M., 1985. Energetische Verwertung von Pektin bei Sauen. Z. Tierphysiol. TierernaÈhr. Futtermittelkde 54, 14±20. Noblet, J., Bach Knudsen, K.E., 1991. Comparative digestibility of wheat, maize and sugar beet pulp non-starch polysaccharides in adult sows and growing pigs. In: Laplace, J.P., Fevrier, C., Barbeau A. (Eds.), Proceedings of the Seventh International Symposium on Digestive Physiology in Pigs, EAAP publication no. 88, pp. 571± 574. Noblet, J., Perez, J.M., 1993. Prediction of digestibility of nutrients and energy of pig diets from chemical analysis. J. Anim. Sci. 71, 3389±3398. Rainbird, A.L., Low, A.G., Zebrowska, T., 1984. Effect of guar gum on glucose and water absorption from isolated loops of jejunum in conscious growing pigs. Br. J. Nutr. 52, 489±498. Rijnen, M.M.J.A., Heetkamp, J.W., Verstegen, M.W.A., Schrama, J.W., 1999. Effects of dietary fermentable carbohydrates on physical activity and energy metabolism in group-housed sows. In: Proceedings of the ASAS Meeting, p. 182. Schulz, E., Noll, J., Oslage, H.J., 1998. Investigations on the digestion of carbohydrates in the different parts of the intestine in pigs. In: Buraczewska, L., Buraczewski, S., Pastuszewska, B., Zebrowska T. (Eds.), Proceedings of the Fourth International Seminar on Digestive physiology in pigs, Jablonna, Poland, pp. 196± 202. Smits, C.H.M., Veen, W.A.G., Borggreve, G.J., Heeres-Van der Tol, J.J., 1991. In: Verstegen, M.W.A., Huisman, J., den Hartog, L.A. (Eds.), Proceedings of the Fifth International Symposium on Digestive Physiology in Pigs, 24±26 April 1991, Wageningen, The Netherlands, pp. 471±476. Van der Meulen, J., Bakker, J.G.M., 1991. Effect of various sources of dietary ®bre on chemico-physical characteristics of digesta in the stomach and the small intestine of the pig. In: Verstegen, M.W.A., Huisman, J., den Hartog, L.A. (Eds.), Proceedings of the Fifth International Symposium on Digestive Physiology in Pigs, 24±26 April 1991, Wageningen, The Netherlands, pp. 440±445. Wenk, C., 1980. Zur Verwertung der Energie beim wachsenden, monogastrischen, landwirtschaftlichen Nutztier, Habilitationsschrift, ETH ZuÈrich. Wenk, C., 1992. Enzymes in the nutrition of monogastric farm animals. In: Lyons, T.P. (Ed.), Proceedings of the Eighth Alltech Annual Symposium on Biotechnology in the Feed Industry, pp. 205±218. Wenk, C., Messikommer, R., Bee, G., 1998. Effect of lignin form different origins in combination with carbohydrases in pig diets on digestion processes. J. Anim. Sci. Suppl. 76, 179. Wenk, C., P®rter H.P., Halter, H., Stoll, P., Messikommer, R., 1980. NaÈhrwert von Maisp¯anzen und von unterschiedlich konservierten Maiskolben bei Mastschweinen. In: Proceedings of the 31th Annual Meeting EAAP, 1±4 MuÈnchen, Deutschland, September, pp. 1±7. Wenk, C., ZuÈrcher, U., 1990. Energetische Verwertung nahrungsfaserreicher Nebenprodukte aus der MuÈllereiund Nahrungsmittelindustrie beim Schwein. Arch. Anim. Nutr. 40, 423±430. Zebrowska, T., Low, A.G., Zebrowska, H., 1983. Studies on gastric digestion of protein and carbohydrate, gastric secretion and exocrine pancreatic in the growing pig. Br. J. Nutr. 49, 401±410.
The role of dietary ®bre in the digestive physiology of the pig Caspar Wenk* Institute of Animal Sciences, ETH ZuÈrich, UniversitaÈtstr. 2, CH-8092 ZuÈrich, Switzerland
Abstract Dietary ®bre (DF) is usually de®ned as the sum of plant polysaccharides and lignin that are not hydrolysed by endogenous enzymes of the mammalian digestive system (non-starch polysaccharides and lignin). The amount and composition of DF varies over a wide range between and within feedstuffs. Furthermore, a precise distinction between dietary ®bre and starch is far from easy. Therefore, the analysis as well as the physiological function of DF in the digestive tract of the pig can vary considerably. The age or body mass of the pig also interacts with the digestive processes and there is an adaptation developing in the animal over the time of exposure to ®brous diets. DF is generally considered as a fraction with a low energy content. This diluting effect of the diet is used to increase the feed intake during low performance of animals. DF in¯uences transit time with a reduction in the upper and increase in the lower digestive tract and, therefore, decreases the digestibility of almost all nutrients and energy. On the other hand, it increases the microbial growth in the gastrointestinal tract. This can lead to an increased excretion of nutrients in faeces. Finally, DF bene®cially in¯uences well-being and health. Fibrous feedstuffs give pigs the opportunity to chew the feed over a longer time. More short chain fatty acids are produced and eventually undesired micro-organisms are excluded. A regular peristaltic action avoids the possibility of constipation. # 2001 Elsevier Science B.V. All rights reserved. Keywords: Dietary ®bre; Pigs; Nutrients; Energy; Digestion
1. Digestive system of the pig and its micro¯ora The processes in the digestive tract of farm animals are of great importance in the understanding of the in¯uence of nutrition on metabolism. In comparison to ruminants, non-ruminant animals have a 'simple' stomach, in which only slight microbial modi®cations of available nutrients take place before absorption occurs. Micro-organisms *
Tel.: 41-1-632-32-55; fax: 41-1-632-11-28. E-mail address: [email protected] (C. Wenk). 0377-8401/01/$ ± see front matter # 2001 Elsevier Science B.V. All rights reserved. PII: S 0 3 7 7 - 8 4 0 1 ( 0 1 ) 0 0 1 9 4 - 8
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Fig. 1. Comparison of the digestive tract of cattle, pigs and poultry.
are in contact with undigested materials or endogenous substrates to a considerable degree mainly in the lower parts of the digestive tract, from the terminal ileum to the rectum and the products of this microbial fermentation may partly be absorbed by the host animal. Most digestive processes in non-ruminant animals occur under anaerobic conditions. Feed digestion depends on the quantity and composition of the diet. The size and function of the organs of the digestive tract as well as the digesta retention time in different parts of the GI tract are further important characteristics. In Fig. 1, the digestive tract of the pig is schematically presented in comparison with that of cattle and poultry. The digestive tract of the pig can be divided mainly into three different compartments: the stomach, small intestine and the large intestine. Stomach represents about 30% of the total volume of the digestive tract. In this part, digestion begins with a lowering of the pH. Some microbial activity may occur in the upper part of the stomach, but only if the pig ingests a high quantity of feed. In the stomach only a limited mixing of food occurs. Compared to other farm animals, the small intestine of pigs is long and permits an intensive endogenous digestion at an almost neutral pH. In the lower ileum and especially the caecum and lower large intestine (third compartment), an intensive microbial degradation takes place. In pigs, most available nutrients (protein, carbohydrates, fat, minerals and vitamins) are absorbed in the small intestine. In the large intestine, undigested feed components (mainly dietary ®bre, lipids with a high melting point and insoluble proteins) and endogenous secretions are fermented by micro-organisms. In this part, only short chain fatty acids (SCFA) and some vitamins can be absorbed which can contribute to the nutrient supply of the animal.
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Fig. 2. Types and density of micro-organisms in the digestive tract of pigs.
The chicken, in comparison, has a crop before and a gizzard (a muscular stomach) below the true stomach (proventriculus), in which glands release endogenous secretions. Microbial activity in the crop becomes important if the feed remains for a longer period in this organ. In poultry, the microbial activity is low in the small intestine, due to its small size and the high rate of passage. In the large intestine, the rate of passage in comparison to the pig is also faster, thus, limiting intensive microbial degradation. The pig as a non-ruminant animal has only a small population of micro-organisms in the stomach relative to the lower parts of the digestive tract. Furthermore, it should be noted that ingested feed remains only for a short period of time in the stomach. Therefore, microbial activity is rather limited. In the lower parts of the small intestine and mainly in the large intestine, an increased number of micro-organisms can be found. As shown in Fig. 2, the population density for certain species of micro-organisms in the caecum and colon reaches the level of 1010 (or even higher) per g 1 digesta. Microbial growth and its metabolic turnover depends on several conditions. Body temperature offers optimal conditions. It also depends on the presence of substrates that can be metabolised. The substrates that will be made available can depend on the number of meals and the composition as well as the structure and technological treatment of the diets. These factors particularly in¯uence digestion in the upper part of the digestive tract. In the search for nutrients, the micro-organisms of different species are in a continuous competition. Furthermore, the endogenous digestion processes (with the secreted enzymes) affect microbial growth. The change of pH in the stomach and later in the small intestine is also a limiting factor for micro-organisms. Finally, the rate of passage of digesta does limit microbial processes in different parts of the digestive tract. Jùrgensen and Just (1988) have used ATP-concentration in the digesta at different parts of the digestive tract in pigs fed two different diets as an indicator of microbial activity in the GI tract. One diet was mainly based on wheat ¯our. While, the other contained wheat bran in addition to the wheat ¯our. The second diet contained a higher level of dietary ®bre than the ®rst.
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Fig. 3. ATP-concentration in the digesta of pigs as affected by dietary ®bre.
For both diets, the ATP-concentration in the stomach was low (Fig. 3). With the diet containing only wheat ¯our, a rapid increase in ATP-concentration could already be observed in the jejunum, which reached a maximum at the end of the ileum followed by a sharp decrease in the caecum. There was almost no ATP detected in the colon. The shape of this curve indicates that, in the diet with a low ®bre content, the maximum microbial activity was observed at the end of the small intestine. Obviously due to the lack of substrates, microbial activity decreased rapidly. In line with the ®rst diet, an increased microbial activity was also observed in the small intestine with the second diet, which contained wheat bran. However, the maximum ATP-concentration was observed at the end of caecum which decreased slowly, but continuously during the latter part of the large intestine. This slow decrease of ATP-concentration indicates that a high microbial activity was maintained throughout the large intestine. As a whole, the microbial activity with the diet containing wheat bran was far greater than with the diet that had a low ®bre content. With the secretion of enzymes and other substances for endogenous digestion in different parts of the digestive tract (saliva in the mouth, gastric juice in the stomach, pancreatic juice and secretions of the small intestine), macronutrients are digested so that the monomers for carbohydrates and/or oligomers for protein and lipids can be absorbed in the small intestine (Fig. 4). Micro-organisms synthesise short chain fatty acids (SCFA) from unabsorbed nutrients. These can subsequently be absorbed and metabolised by the pig. According to experiments of MuÈller and Kirchgessner (1985), two-thirds of microbial fermented organic matter can be utilised by the host animal. Beside SCFA, other ®nal end-products of microbial metabolism (like NH3, CH4, H2O) can be found. Some of them are also absorbed, but not utilised in the intermediate metabolism. In the pig, most nutrients that are incorporated in the micro-organisms will be excreted with faeces. These include microbial protein. Since dietary ®bre by de®nition cannot be digested by endogenous processes, it is mainly micro-organisms that will metabolise them. Therefore, it can be concluded that most digested dietary ®bre will be utilised with
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Fig. 4. Competition between enzymes in the digestive tract.
a reduced ef®ciency as reported by MuÈller and Kirchgessner (1985). Undigested dietary ®bre will be excreted in faeces. Finally, the rate of absorption of different carbohydrates depends directly on the mechanisms available. Na-dependent active transport mechanisms with a high ef®ciency are available for glucose and galactose. Fructose is absorbed with a facilitated mechanism. If high amounts of fructose are present in digesta, the facilitated diffusion will be insuf®cient for an ef®cient absorption, and therefore, a large part of fructose will be passed to the large intestine and metabolised by micro-organisms. Other monosaccharides such as mannose are only absorbed by simple diffusion which is even slower than facilitated diffusion or sodium-dependent active transport mechanisms. Therefore, these monosaccharides will mainly be absorbed and metabolised by microorganisms in the digestive tract. 2. Dietary ®bre and the digestion processes In diets for pigs, dietary ®bre is usually an integral part. It is not added as such and, therefore, the contribution of dietary ®bre to the digestive processes has to be considered in relation to its origin. Usually, an increased ®bre content of a diet is directly related to the amount of available nutrients and energy. A diet with a high ®bre content usually contains less metabolisable energy than a diet with a low ®bre content. This means that a diet with a high ®bre content causes earlier satiety of an animal due to gastric signals than a diet with a low ®bre content caused by elongation of the stomach wall (Langhans, 1999). This earlier satiety is of particular importance in pregnant sows. On the other hand, in growing ®nishing pigs, a diet with a low ®bre content will be preferred as this results in maximum intake of available nutrients and energy. An animal that reaches both satiety physically and nutritionally, is less stressed and, therefore, physical activity may be reduced (Rijnen et al., 1999). A diet with a high content of soluble ®bre will cause more water binding in the stomach than a diet with a low ®bre content or with insoluble ®bre. A high amount of soluble dietary ®bre causes an increased volume of digesta in the stomach and, therefore, reduces both satiety and digesta transit time in this organ. Furthermore, in such situations,
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Fig. 5. Post-prandial pH-values (in stomach fundus) after meals with a low or high ®bre content in pigs (Drochner and Coenen, 1986).
the viscosity of digesta is increased and the pH is stabilised at a low level (Fig. 5) (Drochner and Coenen, 1986; Van der Meulen and Bakker, 1991). In an experiment carried out with growing pigs, Drochner and Coenen (1986) studied the pH in the post-prandial state in the fundus region of the stomach after feeding diets containing low and high levels of ®bre. While, the pH with the high ®bre diet remained almost constant at about 2.5, it rapidly increased to four, when pigs were fed the low ®bre diet. The pH value subsequently decreased gradually to a level similar to that with the high ®bre diet over the next 6 h. Johansen et al. (1996) also reported increased viscosity and water binding capacity of stomach contents in pigs. Dietary ®bre in¯uences the intestinal morphology as well as the rate of intestinal cell turnover in pigs (Jin et al., 1994), which ultimately can affect nutrient digestion, absorption and metabolism. Diets with a high ®bre content also cause a signi®cant increase in the secretion of endogenous ¯uids. This was clearly shown in experiments of Zebrowska et al. (1983) in which pigs were fed two diets with an identical crude ®bre content. In treatment 1, the puri®ed diet contained 50 g kg 1 DF in the form of cellulose, but almost no soluble ®bre. In treatment 2, the diet was based on barley and soybean meal and contained the same amount of crude ®bre, but far more dietary ®bre than in treatment 1. As shown in Table 1, the increase in the dietary ®bre content from 50 to 180 g kg 1 (mainly soluble dietary ®bre) caused a doubling of the secretion of saliva and gastric juice in the pigs of 50 kg liveweight. Not only were the secreted ¯uids of the upper digestive tract increased, but pancreatic juice was almost doubled with the increased dietary ®bre; bile was also signi®cantly increased. The increased amount of secreted digestive ¯uids means an extra metabolic effort or demand for the pig. On the other hand, a more ef®cient digestibility of the feed can be expected. The results of similar experiments reported by Mosenthin et al. (1994) with pectin as a source of soluble dietary ®bre con®rm the ®ndings of Zebrowska et al. (1983). Most probably the increased secretion of digestive ¯uids is associated with a higher activity of secretory organs resulting in enlargement of such organs. Jùrgensen et al. (1996) reported signi®cantly heavier stomach, caecum and colon and also longer colon in growing-®nishing pigs fed diets containing high dietary
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Table 1 Dietary ®bre and endogenous secretions in the digestive tract of pigs weighing approximately 50 kga Ingredients
Crude ®bre Dietary ®bre, g.kg 1 Saliva and gastric juice, 3 per day Pancreatic juice, 3 per day Bile, 3 per day a
Purified diet 1
Normal diet 2
Casein, starch, cellulose, vitamin mineral premix
Barley, soybean meal, fish meal, vitamin mineral premix
Identical 50 4 1.2 1.2
Identical 180 8 2.2 1.7
Adapted from Zebrowska et al., 1983.
®bre (268 g kg 1 DM) as compared to those fed a diet containing low (59 g kg 1 DM) dietary ®bre. Improved digestibilities of protein, dry matter and energy were, however, not associated with this modi®cation, values in fact decreased. A high ®bre content of digesta increases peristaltic action and, therefore, reduces the transit time in the small as well as in the large intestine. Jùrgensen et al. (1996) reported a ®ve to six fold increase in the ¯ow of digesta through the terminal ileum of pigs fed high dietary ®bre. Dietary ®bre is a powerful tool against constipation especially in pregnant sows. Unligni®ed soluble dietary ®bre is a nutrient source for pigs. Dietary ®bre is not digested by endogenous processes by the pig, but ef®ciently by the microbial ¯ora. Although, starch from cereals can be almost completely digested by the time the digesta reaches the ileum, Bach Knudsen (1991) observed that a greater proportion of wheat soluble ®bre passes the ileum in pigs without being digested and, therefore, represents a good substrate for miro-organisms in the large intestine. Similar results have been reported by Gdala et al. (1991), Smits et al. (1991) and Schulz et al. (1998) for other feedstuffs. Therefore, with diets containing a high soluble ®bre content, the microbial activity in the large intestine is generally increased as shown by Jùrgensen and Just (1988) and by Bach Knudsen and Jensen (1991). The increased microbial activity in the digestive tract not only means a better utilisation of feed nutrients, but also an increased excretion of microbial substances. As an ultimate result, soluble dietary ®bre can reduce the absorption of nutrients (Rainbird et al., 1984). However, in pigs, the absorption of trace minerals is mainly reduced. As discussed above, the physiological effects of dietary ®bre on nutrient digestion result in a general reduction in digestibility of energy with increased ®bre content of the diet. This was clearly demonstrated by Wenk (1980), who plotted the results of several digestibility experiments in which different ingredients contributed to an increase in ®bre content, measured as crude ®bre (Fig. 6). In each single experiment a linear reduction of the digestibility of energy was observed with increased ®bre content. In general, a reduction in the coef®cient of gross energy digestibility (d(E)) of 0.025 per 10 g crude ®bre kg 1 dry matter was observed. The reduction of d(E) caused by the crude ®bre content was more pronounced in the diets with dehydrated grass or coffee hulls compared to entire maize plants. The composition of the
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Fig. 6. Coef®cient of digestibility of gross energy of pig diets in relation to the crude ®bre content (Wenk, 1980).
®bre fraction might be an explanation for these differences. For instance maize plants are known to be of low lignin content. Similar observations were made by Henry (1971); Noblet and Perez (1993) and Wenk et al. (1980) con®rmed dietary ®bre as a predominant factor in the determination of available feed energy in pig diets as digestible, metabolisable or net energy. However, according to Low (1993), who reviewed the effects of dietary ®bre on feed intake, digestion, nutrient absorption and metabolism, it may be dif®cult to express practical responses of pigs to high dietary ®bre levels due to the direct and indirect effects of other nutrients in the diet. The digestibility of dietary ®bre is lower in young animals than in adult animals (Noblet and Bach Knudsen, 1991) and the negative effects of dietary ®bre on the digestibility of energy and nutrients are highest in young animals. With increasing weight and especially in adult animals, the detrimental effect of ®bre is reduced (FernaÂndez et al., 1986). Furthermore, this depressing effect is more pronounced in the precaecal compared to the faecal digestibility of nutrients or energy. Drochner (1991) found a regression coef®cient for the apparent digestibility of organic matter of 2.8 for precaecal and 1.8 for faecal digestibility. Similar observations were made by Wenk (1992) who measured the digestibility of organic matter and neutral detergent ®bre (NDF) in digesta samples at different sites of the intestine of pigs fed a diet with a high ®bre content (500 g entire maize plants kg 1) with or without the supplementation of a carbohydrate (noncommercial cellulose) using the indicator method. In these experiments, an increase in digestibility was observed over the whole digestive tract. Furthermore, the enzyme supplementation increased the digestibility of organic matter especially in the small intestine, but also d(NDF) was higher in all parts of the digestive tract (Fig. 7). Pigs do not have the same ability to utilise dietary ®bre from different sources. Noblet and Bach Knudsen (1991) found that the digestibility of various ®bre fractions in sows was higher for maize ®bre and soybean pulp than for wheat bran; digestibility of dietary ®bre was 0.74 and 0.86 for maize ®bre and soybean pulp, respectively, compared to 0.46 for wheat bran. Therefore, it is not only the level of dietary ®bre that is important, but the
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Fig. 7. Coef®cient of digestibility of organic matter and neutral detergent ®bre of a diet with a high ®bre content (500 g entire maize plants kg 1) with and without the supplementation of a carbohydrate splitting enzyme.
type or the source of ®bre also plays a signi®cant role in digestion and absorption. Feeding similar levels of either wheat bran or sugar beet ®bre to pigs did not alter the absorption rate of glucose and amino nitrogen. However, sugar beet ®bre increased hindgut fermentation and, therefore, the absorption of volatile fatty acids (Michel and Rerat, 1998), thus, indicating the source of ®bre has an important effect. In experiments of Wenk and ZuÈrcher (1990), the in¯uence of the ®bre source (namely soybean hulls, barley hulls, pea hulls and sorghum hulls) on the digestibility of energy was studied. The effect of crude ®bre (CF), acid detergent ®bre (ADF), neutral detergent ®bre (NDF) and dietary ®bre (DF) as well as lignin on digestibility was evaluated. The results are summarised in Fig. 8.
Fig. 8. Coef®cient of digestibility of gross energy in relation to the dietary ®bre content (in dry matter) of different origin (Wenk and ZuÈrcher, 1990).
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The digestibility of energy in the control diet was 0.84 and the lowest (d E 0:07) was recorded for sorghum hulls. With the exception of soybean hulls, an almost linear increase in ®bre content (CF, ADF, NDF and DF) was associated with reduced digestibility. The main exception to this trend was found for soybean hulls which had similar levels of CF, ADF, NDF and DF as in sorghum hulls, but far higher energy digestibility (d E 0:64). Only the lignin content was lower in soybean hulls. Therefore, the conclusion was that the ligni®cation of the dietary ®bre in sorghum hulls was associated the low digestibility of energy. The partition of the dietary ®bre into insoluble (ADF or CF) and soluble dietary ®bre (NDF-ADF) was not able to explain that difference. The in¯uence of lignin per se on the digestibility of energy was evaluated in two further experiments by Wenk et al. (1998). The experimental design is shown in Table 2. The lignin sources used were oak bark powder, calcium lignin sulphonate and sulphatefree lignin. The lignin sources are frequently used as dust binders or pelleting enhancers in pig and poultry diets and were added in amounts which corresponded to the same analysed lignin quantity in the diet of about 25 g kg 1. Furthermore, the in¯uence of a cellulolytic enzyme on the nutrient utilisation in relation to lignin supplementation was studied. The experiments were carried out in a latin square design with 12 growing individually kept pigs over the range of 22±105 kg liveweight. Digestibility of energy was measured with the indicator method (HCl ± insoluble ash as the indicator). As shown in Fig. 9, the supplementation of the control diet with the three lignin sources in all cases (except oak bark powder) caused a signi®cant decrease in the digestibility of energy. The most serious reduction was found for the sulphate free lignin. From these experiments and from the earlier observations, it can be concluded that lignin causes a signi®cant reduction of the digestion processes if it is present in the dietary ®bre like sorghum hulls and oak bark powder as well as in the free form of Ca-lignin sulphonate or S-free lignin, two products which are used as pelleting agents in the feed
Table 2 Treatments to estimate the effect of lignin from different origins in combination with a carbohydrate enzyme in pigs (22±105 kg liveweight) diets on the digestion processes Type of the diet Experiment 1 a
Enzyme supplementation Control diet 1 g Oak bark powder kg 1 25 g Ca-lignin sulphonateb kg 50 g Ca-lignin sulphonate g 1 50 g S-free ligninc kg 1 a
1
C O A
Allzyme cellulose, Alltech Inc., Kentucky, USA. Lignobond, Attisholz AG, Gerla®ngen, CH. c Alcell, Repap Inc., Pennsylvania, USA b
Experiment 2 CE OE AE
C
CE
A L
AE LE
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Fig. 9. Coef®cient of digestibility of gross energy in growing pigs fed diets with different lignin sources and a carbohydrate enzyme.
industry. The supplementation of the control diets with the carbohydrate splitting enzyme had no signi®cant effect on the digestibility of energy. As a more general observation, cellulose and insoluble ligni®ed dietary ®bre mainly reduced the faecal transit time and also digestibility of the nutrients (Table 3); effects on the processes in the stomach and on satiety as well as on microbial activity are limited. On the other hand, dietary ®bres with a high solubility, like those from vegetables or fruits, can reduce the transit time for emptying of the stomach and prolong satiety. They increase the microbial activity and reduce the faecal transit time. The detrimental in¯uence of soluble ®bre on nutrients is usually less pronounced than from insoluble dietary ®bre.
Table 3 Effects of dietary ®bre on the digestion processes in animals Type of effect of dietary fibres Source of Slower the dietary ®bre emptying of stomach
Achieving Shortening satiety faecal transit time
Increasing microbial activity
Energy digestibility
Cellulose Insoluble, ligni®ed Vegetables, fruits Pectins/guar
Weak Weak
Weak Weak
Relevant Not existing Very important Weak
Medium
Medium
Weak
Very important Medium
Weak
Very important Relevant
Weak
Very important Medium
Weak
Ileal
Faecal
Very important Very important Very important Very important
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3. Conclusions Dietary ®bre is integral part of all feedstuffs of plant origin for pigs. It has speci®c effects on all digestive processes of the pig and also indirectly on intermediate metabolism. Long-term feeding of high levels of dietary ®bre can alter the anatomical and physiological characteristics of the digestive tract of pigs. Soluble dietary ®bre increases ileal and post-ileal microbial fermentation and a considerable amount of short chain fatty acids produced will be absorbed. These absorbed short chain fatty acids can also have speci®c effects on intermediate metabolism. The level, source and composition of dietary ®bre can therefore be considered as important factors in¯uencing the occurrence as well as the rate of different mechanisms of feed digestion in pigs. The effects of dietary ®bre on feed digestion and nutrient absorption can be highly in¯uenced by the physio-chemical properties of ®bre. Therefore, just looking at the total dietary ®bre level will not give a clear picture about its in¯uence on the digestive physiology of pigs. References Bach Knudsen, K.E., 1991. Breakdown of plant polysaccharides in the gastrointestinal tract of pigs. In: Verstegen, M.W.A., Huisman, J., den Hartog, L.A. (Eds.), Proceedings of the Fifth International Symposium on Digestive Physiology in Pigs, 24±26 April 1991, Wageningen, The Netherlands, pp. 428±433. Bach Knudsen, K.E., Jensen, B.B., 1991. Effect of source and level of dietary ®bre on microbial fermentation in the large intestine of pigs. In: Verstegen, M.W.A., Huisman, J., den Hartog, L.A. (Eds.), Proceedings of the Fifth International Symposium on Digestive Physiology in Pigs, 24±26 April 1991, Wageningen, The Netherlands, pp. 389±393. Drochner, W., 1991. Digestion of carbohydrates in the pig. In: Verstegen, M.W.A., Huisman, J., den Hartog. L.A. (Eds.), Proceedings of the Fifth International Symposium on Digestive Physiology in Pigs, 24± 26 April 1991, Wageningen, The Netherlands (EAAP publication no. 54, 1991), Pudoc Wageningen, pp. 367± 388. È bers. TierernaÈhrg. 14, Drochner, W., Coenen, M., 1986. P¯anzliche Strukturstoffe in der SchweineernaÈhrung, U 1±50. FernaÂndez, J.A., Jùrgensen, H., Just, A., 1986. Comparative digestibility experiments with growing pigs and adult sows. Anim. Prod. 43, 127±132. Gdala, J., Graham, H., Buraczewska, L., Aman, P., 1991. Ileal and faecal digestibility of polysaccharides in pigs fed diets with different varieties of pea. In: Verstegen, M.W.A., Huisman, J., den Hartog, L.A. (Eds.), Proceedings of the Fifth International Symposium on Digestive Physiology in Pigs, 24±26 April 1991, Wageningen, The Netherlands, pp. 447±451. Henry, Y., 1971. Essai de preÂvision de la valeur en eÂnergie digestible des aliments pour le porc aÁ partir de leur teneur en constituants membranaires. JourneÂes Rech. Porcine en France 9, 57±64. Jin, L., Reynolds, L.P., Redmer, D.A., Caton, J.S., Crenshaw, J.D., 1994. Effects of dietary ®bre on intestinal growth, cell proliferation, and morphology in growing pigs. J. Anim. Sci. 72, 2270±2278. Johansen, H.N., Knudsen, K.E.B., Sandstrom, B., Skjoth, F., 1996. Effects of varying content of soluble dietary ®bre from wheat ¯our and oat milling fractions on gastric emptying in pigs. Br. J. Nutr. 75, 339±351. Jùrgensen, H., Just, A., 1988. Effect of different dietary components on site of absorption/site of disappearance of nutrients. In: Buraczewska, L., Buraczewski, S., Pastuszewska, B., Zebrowska, T. (Eds.), Proceedings of the Fourth International Seminar at the Institute of Animal Physiology and Nutrition, Jablonna, Poland, pp. 230±239. Jùrgensen, H., Zhao, X.-Q., Eggum, B.O., 1996. The in¯uence of dietary ®bre and environmental temperature on the development of the gastrointestinal tract, digestibility, degree of fermentation in the hind-gut and energy
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