C O M P A R A T I V E P H Y S I O L O G Y OF THE H I N D G U T A N D ITS N U T R I T I O N A L SIGNI FICANCE 1
University of Guelph 2, Guelph, Ontario N1 G 2WI
The space within the digestive tract should be considered as an occluded part of the animal's environment. The processes taking place within this space are subject to less precise control and regulation by the animal than the activities which take place in the organs and tissues within the animal's body such as the liver or muscle. The wall of the digestive tract presents a barrier between the animal body and the lumen of the gut and the properties of this barrier are important in maintaining tissue homeostasis: simple molecules can be absorbed, whereas the complex molecules within the tissue fluids are retained. Food materials contain diverse and complex molecules to which the wall of the intestinal tract is impermeable, and thus it is necessary that these complex molecules are broken down to simple molecules suitable for absorption. This simplification of the food occurs either through the action of endogenously produced digestive enzymes or as a result of catabolism by the microorganisms within the digestive tract in a symbiotic relationship with the host animal. This relationship is of great importance in herbivores, and reaches great sophistication in the ruminants. The digestive tract consists of three functional regions: stomach, small intestine and hindgut (figure 1). The low pit and pepsin initiates digestion by denaturing the protein components of the food, but, except in ruminants, nothing is absorbed from the stomach. In the small intestine the food materials are broken down to simple molecules through the action of the endogenous digestive enzymes and these products are absorbed as they are released. Microbial activity is unimportant in the small in-
testine of the healthy animal. In complete contrast, any digestion in the hindgut is microbial The substrate for this fermentation is the material which has escaped hydrolysis and absorption during the passage of the digesta through the small intestine. The conditions within the hindgut: low oxygen tension and an absence of readily fermentable substrates limit the activities of the microflora to scavenging the residues which have escaped enzymic digestion in the small intestine. Under these conditions the microorganisms release volatile fatty acids, amines and ammonia from the nitrogenous compounds. Iterbivorous animals are able to exploit, as an energy source, the vast amounts of cellulose produced by plants, even though the cellulose cannot be hydrolyzed by the endogenously produced carbohydrase enzymes. Thus cellulose passes unchanged into the hindgut where it is hydrolyzed and catabolized by the microflora with the release of volatile fatty acids in the nonruminant herbivores. Parker (1976) found that up to 40% of the energy required by the rabbit at the maintenance level of feeding was derived from the volatile fatty acids, predominantly acetic acid, produced in the hindgut. The symbiosis in the ruminant is more complex in that the microorganisms act upon the food before it has been subjected to the action of the digestive processes in the small intestine. Because of this there is a much richer supply of substrates to these microorganisms which allows a more vigorous fermentation and allows the microflora to make a positive contribution to the supply of essential amino acids and vitamins, as well as rendering available the energy in cellulose. The microflora of the hindgut is similar to that of the rumcn (Salanitro et al., 1977), but there are quantitative t Introduction to a Symposium on Digestion in the differences between the dependence of microHindgut presented at the Joint Regional Meeting of bial growth upon ammonia concentration inthe ADSA-ASAS-CSAS, Fredericton, N.B., July 10 to dicating some regulation of microbial activity 13, 1977. 2 Department of Nutrition. 1800bY the availability of nitrogenous compounds in
.
JOURNAL OF ANIMAL SCIENCE, Vol. 46, No. 6, 1978
Downloaded from https://academic.oup.com/jas/article-abstract/46/6/1800/4699335 by Iowa State University user on 19 January 2019
H. S. Bayley
PHYSIOLOGY OF THE HINDGUT
Duodenum
SMALL
il
Jejunum
INTESTINE
[
Ileum
I
,I
Colon
I
HIND
GUT
Rectum
FECES Figure 1. Three regions of the digestive tract: stomach, small intestine and hindgut forming a continuous space within the animal.
both the rumen and hindgut. The relative volumes of the three regions of the digestive tract in species adapted to different types of diet (table 1) illustrate the specialized function of each region. The carnivore feeds intermittently, gorging itself after a kill and then fasting until it successfully completes a hunt, and so the protein consumed is denatured in the stomach. Little fermentable material from the flesh diet escapes digestion in the small intestine and thus the function of the
TABLE 1. RELATIVE VOLUME OF THE DIFFERENT REGIONS OF TilE DIGESTIVE TRACT IN A CARNIVORE (DOG), TWO NONRUMINANTS (PIG AND IIORSE) AND A RUMINANT (COW) (COLIN 1886)
Species
Total volume of digestive tract (~)
Stomach
Dog Pig Horse Cow
7 27 210 360
63 29 9 71
Relative volume (% of total) Small intestine 23 33 30 18
Hindgut 14 38 61 11
Downloaded from https://academic.oup.com/jas/article-abstract/46/6/1800/4699335 by Iowa State University user on 19 January 2019
hindgut is water and mineral re-absorption from the digesta. The domestic pig receives a starchy diet, and most of this carbohydrate is hydrolyzed in the small intestine, however, pigs do consume diets containing considerable quantities of cellulose and this passes through the small intestine unchanged. The hindgut is well developed, particularly as the pig approaches maturity and therefore has a very active microflora (Elsclen et al., 1946). The pig with its functional hindgut is better able to utilize fibrous cereal milling by-products as an energy resource than poultry. ttorses and cattle normally receive fibrous diets; in the horse these are predominantly digested in the hindgut which comprises the major part of its digestive system, whereas in the cow the diet is predominantly digested in the rumen with little material which can be fermented, passing into the hindgut. Thus the relative size of the hindgut in cattle is much less than that of the pig or horse. The hindgut is the last region of the digestive tract through which the digesta passes before being voided in the feces, and the only changes brought about in the digesta occur as a result of microbial fermentation. In healthy animals the microflora only receives the residues which have escapcd digestion in the stomach and small intestine, and any potentially useful compounds formed by the microorganisms are of no value to the host animal unless they can be absorbed before the digesta is voided. Thus any essential amino acids which are synthesized will not be available to the host animal as they are incorporated into microbial protein. The practice of coprophagy by small herbivores represents a behavioral development which allows the animal to subject the microflora to the digestive process making available to the host
FEED
STOMACH [
1801
1802
BAYLEV only cellulose but other complex polymers which can only be digested through microbial action. Traditionally these feeds have been used in r u m i n a n t diets and there are many ways in which they can be processed to increase their utilization by these animals. One of the objectives of this series of presentations is to summarize what is k n o w n of the functioning of the hindgut to provide a basis for a clearer definition of the role in which this complex system can be exploited to increase the extraction of useful c o m p o u n d s from the digesta to the benefit of the host. In these considerations the potential effects of the toxins produced by the putrefaction of the nitrogen and sulfur c o m p o u n d s in the hindgut should n o t be overlooked.
LITERATURE CITED
Carlson, W. E. and H. S. Bayley. 1968. Utilization of fat by young pigs: fatty acid composition of ingesta in different regions of the digestive tract and apparent and corrected digestibilities of corn oil, lard and tallow. Can. J. Anim. Sci. 48:315-322. Elsden, S. R., M. W. S. Hitchcock, R. A. Marshall and A. T. Phillipson. 1946. Volatile fatty acids in the digesta of ruminants and other animals. J. Exp. Biol. 22:191-202. Colin, G. C. 1886. Traite'de physiologie compare'e des animaux. Paris, Baillie're et Fils. Cited by A. T. Phillipson, 1970. In Dukes' Physiology of Domestic Animals (8th Ed.) M. J. Swenson (Ed.) Comstock Publishing, Ithaca, NY. Holmes, J. H. G., H. S. Bayley, P. A. Leadbeater and F. W. Homey. 1974. Digestion of protein in small and large intestine of the pig. Brit. Nutr. 32:479-489. Parker, D. S. 1976. The measurement of production rates of volatile fatty acids in the caecum of the conscious rabbit. Brit. J. Nutr. 36:61-70. Robinson, D. W. and L. M. Slade. 1974. The current status of knowledge on the nutrition of equines. J. Anita. Sci. 39:1045-1066. Slade, L. M., R. Bishop, J. G. Morris and D. W. Robinson. 1971. Digestion and absorption of l SN-labelled microbial protein in the large intestine of the horse. Brit. Vet. J. 127:xi-xiii. Salanitro, J. P., I. G. Blake and P. A. Muirhead. 1977. Isolation and identification of fecal bacteria from adult swine. App. and Environ. Micro. 33:79-84.
Downloaded from https://academic.oup.com/jas/article-abstract/46/6/1800/4699335 by Iowa State University user on 19 January 2019
some of the a m i n o acids synthesized by the microorganisms. There is less possibility of the microflora in the hindgut of the large domestic, n o n r u m i n a n t herbivores making such a positive c o n t r i b u t i o n to the amino acid status of the host, b u t R o b i n s o n and Slade (1974) conclude that the horse does enjoy some e n h a n c e m e n t of its dietary protein quality as a result of the activities of the microflora in the hindgut, possible through direct absorption of a m i n o acids from the hindgut (Slade et al., 1971). Classically nutritionists have measured digestibilities of feeds as an indication of their potential nutritonal value for different species of animals, and at the superficial level of total digestibility, or even of the ill defined 'proximate c o m p o n e n t s ' such measures provided a valuable basis for classifying feeds and gave an indication of the species best equipped to utilize them. However, the application of more sophisticated analyses to measure the digestibilities of specific n u t r i e n t c o m p o u n d s invokes the complexity of molecular changes brought a b o u t in the hindgut by the microflora which are unrelated to the n u t r i t i o n of the host animal. The simplest example of such changes is the h y d r o g e n a t i o n of unsaturated fatty acids (Carlson and Bayley, 1968) which results in the conversion of linoleic and oleic acid residues to stearic acid. Similarly the synthesis of an amino acid such as m e t h i o n i n e and arginine in the hind-gut reduces the estimate of its digestibility in a feedstuff, whereas destruction of other amino acids, such as isoleucine, leucine, valine and lysine increases their digestibility, overestimating their availability (Holmes et al., 1974). Animal agriculture must maintain or increase the supply of meat, milk and eggs in a world in which" there is ever increasing demands for the direct use of high quality plant products to feed the h u m a n population. This challenge focuses a t t e n t i o n u p o n the evaluation of materials which c a n n o t be digested by the endogenous digestive enzymes used to assimilate foods by man. These materials are fibrous containing n o t
University of Guelph 2, Guelph, Ontario N1 G 2WI
The space within the digestive tract should be considered as an occluded part of the animal's environment. The processes taking place within this space are subject to less precise control and regulation by the animal than the activities which take place in the organs and tissues within the animal's body such as the liver or muscle. The wall of the digestive tract presents a barrier between the animal body and the lumen of the gut and the properties of this barrier are important in maintaining tissue homeostasis: simple molecules can be absorbed, whereas the complex molecules within the tissue fluids are retained. Food materials contain diverse and complex molecules to which the wall of the intestinal tract is impermeable, and thus it is necessary that these complex molecules are broken down to simple molecules suitable for absorption. This simplification of the food occurs either through the action of endogenously produced digestive enzymes or as a result of catabolism by the microorganisms within the digestive tract in a symbiotic relationship with the host animal. This relationship is of great importance in herbivores, and reaches great sophistication in the ruminants. The digestive tract consists of three functional regions: stomach, small intestine and hindgut (figure 1). The low pit and pepsin initiates digestion by denaturing the protein components of the food, but, except in ruminants, nothing is absorbed from the stomach. In the small intestine the food materials are broken down to simple molecules through the action of the endogenous digestive enzymes and these products are absorbed as they are released. Microbial activity is unimportant in the small in-
testine of the healthy animal. In complete contrast, any digestion in the hindgut is microbial The substrate for this fermentation is the material which has escaped hydrolysis and absorption during the passage of the digesta through the small intestine. The conditions within the hindgut: low oxygen tension and an absence of readily fermentable substrates limit the activities of the microflora to scavenging the residues which have escaped enzymic digestion in the small intestine. Under these conditions the microorganisms release volatile fatty acids, amines and ammonia from the nitrogenous compounds. Iterbivorous animals are able to exploit, as an energy source, the vast amounts of cellulose produced by plants, even though the cellulose cannot be hydrolyzed by the endogenously produced carbohydrase enzymes. Thus cellulose passes unchanged into the hindgut where it is hydrolyzed and catabolized by the microflora with the release of volatile fatty acids in the nonruminant herbivores. Parker (1976) found that up to 40% of the energy required by the rabbit at the maintenance level of feeding was derived from the volatile fatty acids, predominantly acetic acid, produced in the hindgut. The symbiosis in the ruminant is more complex in that the microorganisms act upon the food before it has been subjected to the action of the digestive processes in the small intestine. Because of this there is a much richer supply of substrates to these microorganisms which allows a more vigorous fermentation and allows the microflora to make a positive contribution to the supply of essential amino acids and vitamins, as well as rendering available the energy in cellulose. The microflora of the hindgut is similar to that of the rumcn (Salanitro et al., 1977), but there are quantitative t Introduction to a Symposium on Digestion in the differences between the dependence of microHindgut presented at the Joint Regional Meeting of bial growth upon ammonia concentration inthe ADSA-ASAS-CSAS, Fredericton, N.B., July 10 to dicating some regulation of microbial activity 13, 1977. 2 Department of Nutrition. 1800bY the availability of nitrogenous compounds in
.
JOURNAL OF ANIMAL SCIENCE, Vol. 46, No. 6, 1978
Downloaded from https://academic.oup.com/jas/article-abstract/46/6/1800/4699335 by Iowa State University user on 19 January 2019
H. S. Bayley
PHYSIOLOGY OF THE HINDGUT
Duodenum
SMALL
il
Jejunum
INTESTINE
[
Ileum
I
,I
Colon
I
HIND
GUT
Rectum
FECES Figure 1. Three regions of the digestive tract: stomach, small intestine and hindgut forming a continuous space within the animal.
both the rumen and hindgut. The relative volumes of the three regions of the digestive tract in species adapted to different types of diet (table 1) illustrate the specialized function of each region. The carnivore feeds intermittently, gorging itself after a kill and then fasting until it successfully completes a hunt, and so the protein consumed is denatured in the stomach. Little fermentable material from the flesh diet escapes digestion in the small intestine and thus the function of the
TABLE 1. RELATIVE VOLUME OF THE DIFFERENT REGIONS OF TilE DIGESTIVE TRACT IN A CARNIVORE (DOG), TWO NONRUMINANTS (PIG AND IIORSE) AND A RUMINANT (COW) (COLIN 1886)
Species
Total volume of digestive tract (~)
Stomach
Dog Pig Horse Cow
7 27 210 360
63 29 9 71
Relative volume (% of total) Small intestine 23 33 30 18
Hindgut 14 38 61 11
Downloaded from https://academic.oup.com/jas/article-abstract/46/6/1800/4699335 by Iowa State University user on 19 January 2019
hindgut is water and mineral re-absorption from the digesta. The domestic pig receives a starchy diet, and most of this carbohydrate is hydrolyzed in the small intestine, however, pigs do consume diets containing considerable quantities of cellulose and this passes through the small intestine unchanged. The hindgut is well developed, particularly as the pig approaches maturity and therefore has a very active microflora (Elsclen et al., 1946). The pig with its functional hindgut is better able to utilize fibrous cereal milling by-products as an energy resource than poultry. ttorses and cattle normally receive fibrous diets; in the horse these are predominantly digested in the hindgut which comprises the major part of its digestive system, whereas in the cow the diet is predominantly digested in the rumen with little material which can be fermented, passing into the hindgut. Thus the relative size of the hindgut in cattle is much less than that of the pig or horse. The hindgut is the last region of the digestive tract through which the digesta passes before being voided in the feces, and the only changes brought about in the digesta occur as a result of microbial fermentation. In healthy animals the microflora only receives the residues which have escapcd digestion in the stomach and small intestine, and any potentially useful compounds formed by the microorganisms are of no value to the host animal unless they can be absorbed before the digesta is voided. Thus any essential amino acids which are synthesized will not be available to the host animal as they are incorporated into microbial protein. The practice of coprophagy by small herbivores represents a behavioral development which allows the animal to subject the microflora to the digestive process making available to the host
FEED
STOMACH [
1801
1802
BAYLEV only cellulose but other complex polymers which can only be digested through microbial action. Traditionally these feeds have been used in r u m i n a n t diets and there are many ways in which they can be processed to increase their utilization by these animals. One of the objectives of this series of presentations is to summarize what is k n o w n of the functioning of the hindgut to provide a basis for a clearer definition of the role in which this complex system can be exploited to increase the extraction of useful c o m p o u n d s from the digesta to the benefit of the host. In these considerations the potential effects of the toxins produced by the putrefaction of the nitrogen and sulfur c o m p o u n d s in the hindgut should n o t be overlooked.
LITERATURE CITED
Carlson, W. E. and H. S. Bayley. 1968. Utilization of fat by young pigs: fatty acid composition of ingesta in different regions of the digestive tract and apparent and corrected digestibilities of corn oil, lard and tallow. Can. J. Anim. Sci. 48:315-322. Elsden, S. R., M. W. S. Hitchcock, R. A. Marshall and A. T. Phillipson. 1946. Volatile fatty acids in the digesta of ruminants and other animals. J. Exp. Biol. 22:191-202. Colin, G. C. 1886. Traite'de physiologie compare'e des animaux. Paris, Baillie're et Fils. Cited by A. T. Phillipson, 1970. In Dukes' Physiology of Domestic Animals (8th Ed.) M. J. Swenson (Ed.) Comstock Publishing, Ithaca, NY. Holmes, J. H. G., H. S. Bayley, P. A. Leadbeater and F. W. Homey. 1974. Digestion of protein in small and large intestine of the pig. Brit. Nutr. 32:479-489. Parker, D. S. 1976. The measurement of production rates of volatile fatty acids in the caecum of the conscious rabbit. Brit. J. Nutr. 36:61-70. Robinson, D. W. and L. M. Slade. 1974. The current status of knowledge on the nutrition of equines. J. Anita. Sci. 39:1045-1066. Slade, L. M., R. Bishop, J. G. Morris and D. W. Robinson. 1971. Digestion and absorption of l SN-labelled microbial protein in the large intestine of the horse. Brit. Vet. J. 127:xi-xiii. Salanitro, J. P., I. G. Blake and P. A. Muirhead. 1977. Isolation and identification of fecal bacteria from adult swine. App. and Environ. Micro. 33:79-84.
Downloaded from https://academic.oup.com/jas/article-abstract/46/6/1800/4699335 by Iowa State University user on 19 January 2019
some of the a m i n o acids synthesized by the microorganisms. There is less possibility of the microflora in the hindgut of the large domestic, n o n r u m i n a n t herbivores making such a positive c o n t r i b u t i o n to the amino acid status of the host, b u t R o b i n s o n and Slade (1974) conclude that the horse does enjoy some e n h a n c e m e n t of its dietary protein quality as a result of the activities of the microflora in the hindgut, possible through direct absorption of a m i n o acids from the hindgut (Slade et al., 1971). Classically nutritionists have measured digestibilities of feeds as an indication of their potential nutritonal value for different species of animals, and at the superficial level of total digestibility, or even of the ill defined 'proximate c o m p o n e n t s ' such measures provided a valuable basis for classifying feeds and gave an indication of the species best equipped to utilize them. However, the application of more sophisticated analyses to measure the digestibilities of specific n u t r i e n t c o m p o u n d s invokes the complexity of molecular changes brought a b o u t in the hindgut by the microflora which are unrelated to the n u t r i t i o n of the host animal. The simplest example of such changes is the h y d r o g e n a t i o n of unsaturated fatty acids (Carlson and Bayley, 1968) which results in the conversion of linoleic and oleic acid residues to stearic acid. Similarly the synthesis of an amino acid such as m e t h i o n i n e and arginine in the hind-gut reduces the estimate of its digestibility in a feedstuff, whereas destruction of other amino acids, such as isoleucine, leucine, valine and lysine increases their digestibility, overestimating their availability (Holmes et al., 1974). Animal agriculture must maintain or increase the supply of meat, milk and eggs in a world in which" there is ever increasing demands for the direct use of high quality plant products to feed the h u m a n population. This challenge focuses a t t e n t i o n u p o n the evaluation of materials which c a n n o t be digested by the endogenous digestive enzymes used to assimilate foods by man. These materials are fibrous containing n o t
