Lipid Metabolism in Ruminant Animals

451 Pages·1981·37.927 MB·English

by  W. W. Christie

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Review Journal
Progress in Lipid Research
LIPID METABOLISM
IN
RUMINANT ANIMALS
Editor
WILLIAM W. CHRISTIE
Department of Biochemistry
The Hannah Research Institute
Ayr, Scotland
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First edition 1981
British Library Cataloguing in Publication Data
Lipid metabolism in ruminant animals.
1. Ruminants—Physiology
2. Lipids—Metabolism
I. Christie, William Walker
636.2Ό892397 QL737.IJ5 80-41823
ISBN 0-08-023789-4
Published as supplement No. 1 1981 to the review journal
Progress in Lipid Research
Printed in Great Britain by A. Wheat on & Co. Ltd., Exeter
PREFACE
RUMINANT animals, specifically cattle, sheep and goats, constitute one of the more impor­
tant elements of agriculture in most parts of the world and meat and milk products from
these animals are of vital importance in human nutrition. Microbial fermentation in the
rumen or forestomach anterior to the true stomach permits ruminants to efficiently
digest and thrive on low-quality forages, often on land that is unsuitable for any agricul­
tural purpose other than grazing. These fermentation processes in the rumen also modify
the nature of the metabolites, in particular the lipid and lipogenic components, made
available to the host animal so that a number of aspects of lipid metabolism in ruminants
are very different from those in monogastric animals. For example, short-chain fatty
acids are synthesized in the rumen in large amounts and they, rather than glucose, are
the principal substrates for lipogenesis in ruminant tissues. Also, dietary unsaturated
fatty acids are hydrogenated in the rumen and branched- and odd-chain fatty acids are
synthesized there with important consequences for the lipid composition and metabolism
of the tissues of the host animal.
The authors, members of the Departments of Biochemistry and Physiology of the
Hannah Research Institute, believe that these unusual aspects of lipid metabolism in
ruminant animals should be brought to the attention of a wider audience. In preparing
this book, we have taken joint decisions on the material to be included in each chapter
and have read and criticized each other's work in an attempt to ensure uniformity of
treatment and as comprehensive a coverage of the topic as possible with the minimum of
duplication. Although two of our number departed for Australasia after the work was
commenced, we have continued to adhere to this policy.
The chapters appeared separately as they were ready in Progress in Lipid Research but
the earlier ones have been brought up to date (end of 1979) by the inclusion of additional
material prior to publication here.
W. W. CHRISTIE
A. W. BELL
C G. HARFOOT
J. H. MOORE
R. C. NOBLE
R. G. VERNON
V
ANATOMY, PHYSIOLOGY AND MICROBIOLOGY
OF THE RUMINANT DIGESTIVE TRACT
C. G. HARFOOT
Department of Biological Sciences,University of Waikato, Hamilton,
New Zealand
CONTENTS
I. INTRODUCTION 1
11. FEATUROEFS R UMINANTASN D THEIR ALLIES 2
111. ANATOMYOF THE RUMINANFTO RESTOMACH 3
A. Rumen 3
B. Reticulum 4
C. Omasum 5
D. Abomasum 5
IV. PASSAGOEF FOODT HROUGHT HE RUMINANSTT OMACH 6
A. Ingestion and swallowing 6
B. Salivation 6
1. The salivary glands 6
2. Secretion 6
3. Composition of saliva 7
V. MIXINGO F DIGESTAIN THE RETICULC-RUMEN 7
VI. RUMINATION 8
VII. ENTRYO F DIGESTIANT O THE OMASUM AND ABOMASUM 8
VIII. MICROBIAFLE RMENTATINI OTHNE RETICULO-RUMEN 8
A. The rumen environment 8
B. The microbial population of the reticulo-rumen 10
C. The holotrich protozoa 10
D. The entodiniomorph protozoa 10
E. The bacteria 11
F. Metabolic activities of the rumen bacteria 12
G. Utilization of end-products of microbial metabolism by the ruminant 14
H. Unusable metabolic end-products 14
Ix. PROCESSES IN THE OMASUM AND ABOMASUM 15
A. Omasum 15
B. Abomasum 15
x.
DIGESTIVPER OCESSES IN THE RUMINANTH IND-GUT 15
A. Small intestine 15
1. Secretion into the small intestine 15
2. Digestive processes in the small intestine 16
3. Absorption from the small intestine 16
B. Large intestine 17
1. Digestive processes in the large intestine and caecum 17
2. Absorption from the large intestine and caecum 18
XI. REFERENCES 18
I. INTRODUCTION
Ruminants are distinguished from simple-stomached or monogastric animals by the
development of a series of pouches anterior to their true gastric stomach. Of these
pouches, the rumen is the largest and metabolically the most important.
In the rumen, the chemical constituents of plant origin which are ingested by the
ruminant undergo microbial fermentation to produce both microbial cells, which are
subsequently utilized as sources of protein and other nutrients by the host animal,
and the waste products of microbial metabolism, many of which can also be utilized
by the animal for either energy or biosynthesis. As a result of this conversion of plant
cellular constituents into microbial cells, the metabolism of the ruminant animal is
different from that of the simple-stomached animal, and the tissue composition, particu-
larly the lipid composition, of ruminants is distinctive. For example, it is in the rumen
1
2 C. G. Harfoot
that the volatile fatty acids are synthesized that are subsequently utilized for lipogenesis
in the tissues of the host animal. In the rumen, dietary unsaturated fatty acids are
hydrogenated with important consequences for the lipid composition of the tissues of
ruminants.
In the sections of this article which follow, a generalized account is given of the
anatomy and physiology of the ruminant digestive tract, together with a summary of
microbial processes in the rumen. Because of the economic importance of the ruminant
animal, the literature available is very extensive; references have been kept to a minimum
and for those requiring more comprehensive reviews, attention is drawn to the review
articles in the Handbook of Physiology,18,21,35A9>63 to Phillipson's review article in Dukes'
Physiology of Farm Animals54 and to Hungate's book The Rumen and its Microbes.34
II. FEATURES OF RUMINANTS AND THEIR ALLIES
From the viewpoint of digestive physiology, the distinguishing features of the ruminant
animal are as follows: (a) There is extensive enlargement of the cardiac region of the
stomach to form a series of compartments anterior to the region corresponding to
the simple stomach of non-ruminants. These compartments are referred to as the rumen,
reticulum, omasum and abomasum. The abomasum corresponds in both physiology
and anatomy to the simple stomach of non-ruminants, (b) Within the rumen and reticu­
lum, there occurs extensive microbial fermentation of ingested food, (c) During the period
following ingestion of food, there occurs régurgitation of some of the contents of the
rumen. The regurgitated bolus of rumen contents is mixed with saliva in the mouth,
chewed and re-swallowed. This process is referred to as rumination, or more popularly
"chewing the cud", the "cud" being the regurgitated bolus of food. From the viewpoint
of the zoologist, the ruminants (Ruminantia) form a Suborder of the even-toed Ungulates
or "cloven-hoofed" animals (Order Artiodactyla) (Table 1). As zoological classification
is essentially phylogenetic, that is, it is designed to demonstrate evolutionary relation­
ships between organisms as well as arranging the living species into morphologically
similar groups, more emphasis is placed on skeletal structure than on the anatomy
of soft parts which leave no fossil record. The principal distinguishing feature of the
Artiodactyla is the skeleton of the foot, which consists of a number of well-developed
TABLE 1. A Simplified Classification of the Artiodactyla3 Including Some Representative Living Species and
Showing the Degree of Stomach Complexity0
Representative Living
Suborder Family Species Stomach Anatomy, Rumination
Suiformes Suidae Pigs, wart hogs, forest True stomach may have 1 or 2
hogs diverticula. No true rumen
Tayassuidae Peccaries reticulum, omasum or abomasum
Hippopotamidae Hippopotamus Suiformes do not ruminate.
Tylopoda Camelidae Camels, llama, alpaca 3-chambered stomach present;
vicuna corresponding to rumen
reticulum and abomasum.
Equivalent to omasum lacking.
Ruminantia Tragulidae Chevrotains, mouse-deer Camelids and tragulids both
ruminate.
Ruminantia Cervidae True deer, moose (elk) All cervids, giraffids
caribou (reindeer) antilocaprids and bovids have
Giraffidae Giraffe, okapi true 4-chambered ruminant
Antilocapridae Pronghorn stomach, comprised of rumen,
reticulum, omasum and
abomasum.
Bovidae Cattle, sheep, goats, All species in these four
buffalo, eland, antelopes, families ruminate.
gazelles etc.
a After Simpson.'
"After Walker.6<
Anatomy, physiology and microbiology of the ruminant digestive tract 3
digits with the mid-line passing between digits 3 and 4 (digit 1 is present only in fossil
forms and digits 2 and 5 are either vestigial or absent). This produces the "cloven
hoof" typical of the group.
Table 1 shows the major systematic divisions of the Artiodactyla, and includes the
common names of some representative members of each family. In each of the three
families shown, there has been a tendency for species to evolve multicompartmented
stomachs,46 ranging in complexity from the situation found in the Suiformes where
there are simply diverticula present adjacent to the opening of the oesophagus into
the simple stomach, to the situation in the Tylopoda and the primitive ruminant family
Tragulidae where there is a three-chambered stomach with the equivalent of the omasum
lacking. The greatest complexity is found in the remaining families of the Ruminantia,
all of which possess the characteristic four-chambered stomach. On this basis, the
Ruminantia are sometimes divided into two groups or infra-orders; the Tragulina, con­
sisting of the family Tragulidae, and the Pecora which contains the remaining four
families.62
The three orders show differences in dentition, particularly of the upper jaw. The
Suiformes have well-developed incisors and canines, the latter often tusk-like. In the
Tylopoda, the young animal has a full set of incisors in the upper jaw, but the adult
possesses only the third incisor on each side.46 In the Ruminantia, there is total loss
of the upper incisors. The upper canines are also normally absent, but where they
persist they become much enlarged. The upper incisors and canines are replaced by
a thickened callous pad against which the lower incisors and canines bite. The Ruminan­
tia have retained all the lower incisors and, in general, the lower canines have become
incisor-like; this feature is presumably of evolutionary advantage in that it extends
the length of the row of cropping teeth.
Ruminating is common to both Tylopoda and Ruminantia orders (Table 1), and
although much of the adaptation to the ruminating habit is associated with the muscu­
lature and the neuromuscular reflexes of the rumen and associated organs, one skeletal
adaptation that has taken place is an extreme shallowness of the depression in the
skull into which the mandibular condyle fits. This permits the lower jaw to move from
side to side, resulting in the rotary motion of the lower jaw that can be seen in animals
that are ruminating and which greatly increases the efficiency of grinding of food.
From the above account, it can be seen that the term "ruminant" does not describe
a single zoological group; rumination is not confined to the Ruminantia, neither do
all members of the Ruminantia possess the characteristic four-chambered stomach. The
situation is further complicated by the fact that many herbivorous mammals of diverse
zoological affinities have developed ruminant-like features through convergent evolution;
presumably because the possession of these features confers ecological and evolutionary
advantages.49
III. ANATOMY OF THE RUMINANT FORESTOMACH
In this and subsequent sections of this article, a generalized account is given of
the anatomy and physiology of the ruminant digestive tract and of the microbial fermen­
tation that takes place within it. Most of the findings described have been made with
cattle and sheep because of the economic importance of these animals but, unless other­
wise specified, the following account applies to all true ruminants.
Figure 1 shows in diagrammatic form a section taken through the median vertical
plane of a generalized ruminant stomach viewed from the right-hand side. Arrows indi­
cate the route taken by food during digestion and rumination. The subdivisions of
the stomach will be considered in the order in which food passes through them.
A. Rumen
This is the largest compartment of the adult ruminant stomach although its size
relative to other compartments varies from species to species (Table 2). The rumen
4 C. G. Harfoot
DRF
DCP
VRF
VCP
R00
FIG. 1. Section through the median vertical plane of a generalized ruminant stomach viewed
from the right-hand side. ABO, abomasum; ATF, anterior transverse fold; ATP, anterior trans­
verse pillar; D, duodenum; DBS, dorsal blind sac; DCP, dorsal coronary pillar; DRF, dorsal
reticular fold; DSR, dorsal sac of the rumen; LP, longitudinal pillar; OAO, omaso-abomasal
orifice; OES, oesophagus; OM, omasum; RET, reticulum; ROO, reticulo-omasal orifice; VBS,
ventral blind sac; VCP, ventral coronary pillar; VRF, ventral reticular fold; VSR, ventral sac
of the rumen; —►, route taken by food during ingestion and passage through digestive tract;
►, route taken by digesta during rumination.
is roughly ovoid, somewhat compressed laterally and is divided internally into dorsal
and ventral sacs by a series of shelf-like pillars (Fig. 1).
The whole of the internal surface is covered with heavily keratinized projections (papil­
lae) which greatly increase the surface area available for absorption. The papillae differ
in size both with the species and also with respect to their location in the rumen,
ranging in size fron small cones approximately 1-3 mm in height to large flattened
leaf-shaped structures which may be up to 1 cm in length in the ox. The distribution
of the papillae is not uniform; in most ruminants, the sides of the dorsal and ventral
sacs of the rumen are the most densely papillated and also have the largest papillae.
The borders of the pillars of the rumen on the other hand, along with the dorsal
region of the dorsal sac bear only small, widely separated papillae.
B. Reticulum
The most anterior of the compartments of the ruminant stomach, the reticulum, is
TABLE 2. Weights and Proportions of Regions of the Gastro-intestinal Tract in Domestic Ruminant Species
Milk cow; 7 -month old bull; Sheep;
body wt 520 kga body wt 204 kga body wt 80 kgb
% % %
total total total
Wt stomach Wt % stomach Wt stomach
/o /o
Organ (kg) live wt wt (kg) live wt (kg) live wt wt
Reticulo-rumen 65.4 12.6 87.5 40.0 19.6 92.0 17 21.3 84.9
Omasum 7.5 1.4 9.7 2.5 1.2 5.6 1 1.3 5.1
Abomasum 2.3 0.4 2.8 1.1 0.5 2.4 2 2.5 10.0
Total 75.2 14.4 100 43.6 21.3 100 20 25.1 100
Small intestine 6.3 1.2 c 3.5 1.7 6 7.5
Caecum d — — — 1 1.3
Large intestine 5.4 1.0 2.9 1.4 3 1.8
Total gastro­
intestinal tract 86.9 16.6 50.0 24.4 30 37.6
aData compiled from Hungate.34
bData compiled from Maynard and Loosli.48
c Not applicable.
d No data.
Anatomy, physiology and microbiology of the ruminant digestive tract 5
FIG. 2. Interior view of right side of reticulum and portion of the adjoining rumen. C, cardia;
DRF, dorsal reticular fold; LOG, lips of oesophageal groove; O, oesophagus; OG, oesophageal
groove; ROO, reticulo-omasal orifice; VRF, ventral reticular fold.
separated from the rumen by a ridge of tissue called the rumino-reticular fold which
extends from the ventral right side, transversely to the left, up the left side and partially
across the dorsal region from left to right. As the rumino-reticular fold does not extend
to the right lateral wall of the stomach, there is no demarcation of the reticulum from
the rumen on this side. In consequence of this incomplete anatomical separation and
the functional similarities of the reticulum and rumen, the two compartments are fre­
quently referred to as the reticulo-rumen, the reticulum being regarded simply as an
anterior pouch of the rumen.
In addition to its communication with the rumen, the reticulum also communicates
in its dorsal region with the oesophagus via the cardia and with the omasum via the
reticulo-omasal orifice (Fig. 2). The cardia and reticulo-omasal orifice are situated at
either end of two bands of tissue between which lies the oesophageal groove (see below).
The mucosal lining of the reticulum is raised into a honeycomb-like pattern and is
more or less uniformly covered with small conical papilla, which, like those of the
rumen, are heavily keratinized.
C. Omasum
This compartment lies on the right-hand side of the stomach and connects with the
reticulum and abomasum via the reticulo-omasal and omaso-abomasal orifices, respect­
ively. Projecting into the omasum are a large number of plate-like folds or laminae
attached to the greater curvature of the omasum and to its ends, in a manner akin
to the pages of a book being attached to a binding that extends from the spine across
the top and bottom of the pages. The omasal laminae bear heavily keratinized papillae
that point in the general direction of the abomasum; this arrangement ensures that
food material present in the omasum is propelled towards the abomasum irrespective
of the muscular activity taking place in the omasum.18
D. Abomasum
The abomasum is a tubular organ connecting the omasum with the small intestine.
The mucosa of the abomasal wall is folded into longitudinal ridges not dissimilar from
the laminae present in the omasum. The arrangement of these ridges is such that they
possibly serve to prevent the contents of the abomasum from flowing back into the
omasum.34 The abomasum corresponds in function to the fundic and pyloric regions
6 C. G. Harfoot
of the stomach in non-ruminant animals in that the epithelium is supplied with secretory
cells which produce hydrochloric acid and pepsin in the fundic region, and in the pyloric
region, mucus. The peptic activity of the secretion from the pyloric region is low.54
It is in the abomasum that food is first subjected to digestive processes which are
of ruminant rather than microbial origin.
IV. PASSAGE OF FOOD THROUGH THE RUMINANT STOMACH
A. Ingestion and Swallowing
Ruminants, in common with other large herbivores, require a large bulk of food
in order to satisfy their demands for substrates for biosynthesis and energy. Field studies
have shown that cows spend approximately equal amounts of time grazing, ruminating
and resting.73 However, the proportion of time spent in the ingestion of food is markedly
less under conditions in which the animals are fed concentrates and ground and pelleted
foodstuffs.
During feeding, the food is briefly chewed, mixed with saliva to form a bolus, which
in cattle weighs approximately 100 g, and swallowed. The bolus is propelled down the
oesophagus by peristaltic contractions of the latter with such force that it falls into
the rumen rather than into the reticulum (Fig. I).5 This rapid propulsion of the bolus
is achieved through the action of striated muscle in the oesophageal wall of the ruminant.
In contrast, smooth muscle is present in the oesophageal wall of non-ruminants. In
the rumen, muscular contractions serve to mix the bolus with previously ingested
material.
B. Salivation
1. The Salivary Glands
There are two types of salivary gland in ruminants, alkaligenic glands which comprise
the paired parotid, inferior molar and buccal salivary glands and which secrete a fluid
containing a high concentration of HCO^ ions with little mucoprotein and mucogenic
glands, which comprise the paired submaxillary, sublingual and labial salivary glands
as well as the unpaired pharyngeal gland and the numerous glands in the buccal epithe­
lium.32 The secretions of the mucogenic glands are predominantly mucoprotein. The
composition of the secretion of some of these salivary glands is shown in Table 3. Of
the glands secreting alkaline saliva, the most important are the parotid glands which
secrete about half the salivary output in cattle.36
TABLE 3. Ionic Composition of the Saliva Secreted by Bovine Salivary Glands (Concentration in m-equiv/1
with percentage composition in parentheses)3
Salivary gland HCO3 ΗΡΟΓ c\- Na + K + Ca2 +
Parotid 110.8 (38.9) 22.4 (7.9) 10.6 (3.7) 123.0(43.2) 14.7 (5.2) 3.4 (1.2)
Submaxillary 15.7 (19.2) 0.5 (0.6) 30.9 (37.8) 13.6 (16.6) 13.9 (17.0) 7.1 (8.7)
Sublingual 104.3 (34.4) 17.0 (5.6) 17.6 (5.8) 142.0 (46.8) 19.4 (6.4) 3.2(1.1)
aData from Phillipson and Mangan.55
2. Secretion
During the period when the animal is not feeding, there is a basal level of secretion
of alkaline saliva but little secretion of mucoproteins. Feeding stimulates secretion of
alkaline saliva and greatly stimulates that of mucoproteins. This stimulation was greatest
with coarse fibrous food,20 and appeared to result from reflexes initiated by stimulation
of the walls of the rumen by coarse food particles, especially those in the vicinity of
the rumino-reticular fold.19'28 To a lesser extent, salivation was stimulated by pressures
within the rumen.56