See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/248891624

Potential impact of nematode parasitism on nutrient partitioning for wool

production, growth and reproduction in sheep

Article  in  Australian Journal of Experimental Agriculture · January 2003

DOI: 10.1071/EA03017

CITATIONS READS

25 67

3 authors, including:

Shimin Liu David G. Masters

University of Western Australia The Commonwealth Scientific and Industrial Research Organisation
96 PUBLICATIONS   639 CITATIONS    159 PUBLICATIONS   1,744 CITATIONS   

SEE PROFILE SEE PROFILE

Some of the authors of this publication are also working on these related projects:

Identify what attracts L. cuprina to wool sheep View project

Wool growth and quality in seasonally variable environments View project

All content following this page was uploaded by Shimin Liu on 02 June 2015.

The user has requested enhancement of the downloaded file.

CSIRO PUBLISHING
www.publish.csiro.au/journals/ajea Australian Journal of Experimental Agriculture, 2003, 43, 1409–1417

Potential impact of nematode parasitism on nutrient partitioning

for wool production, growth and reproduction in sheep

S. M. LiuA,B, D. G. MastersA and N. R. AdamsA

ACRC for the Australian Sheep Industry and CSIRO Livestock Industries,
Private Bag 5, PO Wembley, WA 6913, Australia
B
Author for correspondence; e-mail: shimin.liu@csiro.au

Abstract. Most ovine studies indicate that protein supply is a key determinant of the ability to mount a strong
immunity-associated response to gastrointestinal parasites. This paper quantifies the demands placed on protein
supply by various physiological states, to determine why this is so. Protein requirements in fast growing lambs and
ewes in late pregnancy and early lactation are substantially increased, amounting to a 1.43-, 0.69- and 2.50-fold
increase in maintenance requirement for dietary protein. Infestation with internal parasites may result in a total net
loss of about 12 g protein/day, which consists of a net loss of about 6 g from the gastrointestinal tract and a further
loss of about 6 g through increased amino acid oxidation in the body. This loss from the infection accounts for about
0.57-, 0.71-, 0.14- and 0.77-fold the protein requirements respectively for body growth, pregnancy, lactation and
wool production, and creates strong competition for protein. Such considerable demands for protein by activation
of immunity-associated response diminishes the animal’s nutrient status in late pregnancy and particularly in early
lactation. The total demand for protein cannot be met by pastures during the reproductive season in Mediterranean
environments, and it is this nutrient deficiency, relative to the demand of sheep, which results in weak immune
responses over these periods. The immunity-associated response requires more protein rather than energy,
particularly sulfur amino acids such as cysteine and probably methionine. Therefore, parasite infection has a more
severe effect on wool- than meat-producing sheep. Body condition of sheep could be a predominant factor in
determining immune status and current intake and quality of pastures needs to be considered to further boost
immunity-associated response. Wool- and meat-producing genotypes, and parasite-resistant sheep in particular,
may have different interactions with nutrition in response to parasite infection. These factors need to be integrated
with anthelmintic treatment to establish an effective strategy to control parasite infection in Mediterranean
environments.

Introduction degradation and associated energy consumption enable us to

It is well known that malnutrition and a high susceptibility
to parasitism often occur concurrently. Most studies indicate
that protein supply is a key determinant of the ability to
mount a strong immunity-associated response to parasite
infection. This paper quantifies the demands placed on
protein supply by various physiological states, to determine
how growth and reproduction can affect immunity. The
emphasis will also be placed upon analysis of some key
issues in improving immunity to parasitic infection,
including nutritional status of animals, special nutrients for
immunity, and interactions between nutrition and genetic
selection.
Protein and energy requirements for body growth, gravid
uterus, lactation and wool growth
Protein metabolism in the tissues that produce animal
products such as milk or wool provides a basis to understand
amino acid competition during growth, reproduction and
accompanying wool growth. Protein synthesis and
understand more accurately the competition for nutrients and
feed efficiency for production. Estimates based on published
work and summarised in Table 1 show that protein accretion
in growing lambs gaining 150 g/day requires 1.43 times the
metabolisable protein (MP) required for maintenance.
Protein accreted in the gravid uterus during the period from
119 to147 days of pregnancy is 0.69 times the corresponding
maintenance requirement for MP. However, the protein
synthesis:accretion ratio in the foetus is high, due to a high
protein turnover rate. For example, the whole-foetus protein
fractional synthesis rate can be estimated to be about 25%
per day (calculated from a total synthesis of 63 g/day at
120 days of gestation (Schaefer and Krishnamurti 1984) and
a protein content of 244 g (Agricultural Research Council
1984) compared with a whole-body fractional synthesis rate
of 6% per day in growing lambs (Liu et al. 1996). The high
turnover rate in the gravid uterus implies that energy costs
for foetal growth could be high. Protein secretion in milk at
2 kg/day amounts to 2.50 times the maintenance

© CSIRO 2003 10.1071/EA03017 0816-1089/03/121409

1410 Australian Journal of Experimental Agriculture S. M. Liu et al.

requirement. Wool protein at a growth rate of 10 g/day
accounts for 0.7 times the maintenance requirement and is
associated with high rates of protein synthesis in the wool
follicles. In addition, the concentration of cysteine (Cys) plus
methionine (Met) in wool protein is 104 g/kg protein, about
3 times that in the whole body (3.1 g/kg protein (MacRae
et al. 1993) and milk (3.3 g/kg protein; Degussa 1996). This
high demand for Met and Cys accounts for more than half the
absorption of Met and Cys from the diet at maintenance
feeding, and creates a unfavourable profile of amino acids in
the metabolic pool for the remaining body protein synthesis
if dietary supply is not adequate.
The energy accreted in tissue, milk and wool, calculated
from protein and fat content, is also presented in Table 1, and
the metabolisable energy (ME) requirements are compared
with the maintenance requirement. In pregnant and dry ewes,
energy retention in the gravid uterus or in wool accounts for
only a small fraction (about 0.1 and 0.05, respectively) of the
maintenance requirement because of their low fat content.
The MP:ME ratios in Table 1 suggest that the
production-related protein requirement is high relative to
that for maintenance, so the MP:ME ratio of a diet should be
increased, particularly for pregnant ewes in late pregnancy.
The lowest ratio is found in growing animals, indicating
energy is more important for growth.
An analysis of body composition of growing sheep as
given by the Agricultural Research Council (1984) indicates
that Merino lambs retain more fat at the same liveweight than
other breeds during growth (Table 1), but similar amounts of
protein to other breeds. Therefore, Merino sheep require
more energy to support their weight gains. Possibly Merinos
have a relatively lower mature weight compared with meat

Table 1. Estimated requirements of metabolisable protein and energy by growing lambs, pregnant and lactating ewes, and wool growth,
and extra costs from infection of gastrointestinal parasites
The requirements are calculated according to the Agricultural Research Council (1984) and Standing Committee on Agriculture (1990)
The efficiencies of protein for maintenance, growth, pregnancy, lactating and wool growth are 0.7, 0.7, 0.7, 0.75 and 0.45, and energy efficiencies
are 0.7, 0.43, 0.13, 0.6 and 0.18 for a diet containing 10 MJ ME/kg dry matter
Protein composition in growth castrates (g/kg) = 0.2028 LW (kg)–0.1045
Energy composition in growth castrates (MJ/kg), non-Merinos = 0.022 LW (kg) 0.821 × 39.3 MJ/kg + 0.2028 LW–0.1045 × 23.1 MJ/kg, and for
Merinos = 0.0144 LW (kg) 0.024 × 39.3 MJ/kg + 0.2028 LW–0.1045 × 23.1 MJ/kg (derived from the Agricultural Research Council 1984)
Milk energy (MJ/kg) = 0.0329 fat (80 g/kg) + 0.0025 days of lactation (20 days) + 2.203 = 4.885 MJ/kg.
The net cost of protein for infection is estimated to be 12 g/day; the energy cost for protein synthesis = protein accretion (g/day) × 23.1 kJ/g + protein
synthesis (g/day) × 5.4–7.2 kJ/g, plus 5.7–3.6 kJ/g for degradation of protein (Lobley 1994a); an efficiency of 0.7 is used to convert the net protein
and energy costs to metabolisable protein and energy

Growth (20–40 kg, Pregnancy (gravid uterus, Lactation (milk, first Wool growth (dry greasy
castrates) single, 119–147 days) 3 weeks) wool, 3-year-old sheep)
Liveweight (kg) 30 50 50 50
Tissue accretion 150 g/day 96 g/day 2 kg/day 10 g/day
or product output
Protein
MP for maintenance (g/day) 21 35 48 30
MP for productionA (g/day) 52 46 142 22
Total MP (g/day)B 73 81 190 52
Energy
ME for maintenance (MJ/day) 5.1 6.8 6.8 6.7
MP for productionA (MJ/day) 7.4 5.1 17.5 1.3
Total ME (MJ/day)B 12.5 (14.0)C 11.9 24.3 8.0
MP:ME ratio
MP:ME for maintenance 4.1 5.1 7.1 4.5
MP:ME for accretion 4.9 (3.9)C 6.3 7.4 17
Overall MP:ME ratioB 5.8 (5.2)C 6.8 7.8 6.5
Estimated extra costs from parasite infection
MP (g/day 17 17 17 17
ME (MJ/day) 0.8 0.8 0.8 0.8
Overall MP:ME in infected sheep 6.8 7.7 8.2 7.8
A
Including wool growth.
B
Total MP and ME for growing, pregnant and lactating animals include 22 g MP and 1.3 MJ ME for 10 g wool growth/day, and they are also included in
calculation of the overall MP:ME ratios.
C
Merino sheep in parentheses.
Impact of nematode parasitism on nutrient partitioning
breeds, and have higher fat content at the same body weight.
Merinos also deposit more protein for wool growth so the
overall protein:energy ratio may not differ significantly from
other breeds.
Effects of parasite infection on protein metabolism
Direct measurements of changes in protein and energy
metabolism associated with the immune responses,
including both metabolic rates and mass changes in the
immune system, would help to understand nutrient
partitioning and competition during parasite infection.
However, defining and measuring the total mass of the
immune system is difficult. Some analyses of the chemical
composition of the immune response, indicating the major
nutrients required by the system, are briefly outlined below
in order to compare the cost of immunity with the costs for
body growth, reproduction and wool growth.
Changes in the rate of protein turnover in response to
parasite infection
Whole-body changes. The effect of parasite infection on
whole-body protein turnover can be indicated by the amino
acid irreversible loss rate (ILR). If the nutrient intake is
controlled at the same level in both infected and uninfected
animals, the ILR indicates the availability of an amino acid
from both gastrointestinal absorption and breakdown of
body protein. Infection of the small intestine with
Trichostrongylus colubriformis did not significantly affect
ILR of leucine (Leu; Yu et al. 2000), valine (Val;
Bermingham et al. 2000), tyrosine (Tyr; Jones and Symons,
1982) or phenylalanine (Phe; Hoskin et al. 2002) when feed
intakes were controlled to be similar in infected and
uninfected sheep. The ILR of Met (Liu et al. 2002) and Cys
(Bermingham et al. 2000) were reduced by 13–15%, but this
was not statistically significant. Cys ILR per unit nitrogen
(N) intake tended to decline by 8–17% depending on stage of
infection (Hoskin et al. 2002). The lack of any significant
change in the ILR of Leu, Val and Phe at the same intake
level implies that the degradation rate of the body protein
was not altered by infection, or that degradation rate may
have increased to compensate for the decreased absorption,
whereas the reductions of the ILR of Met and Cys are likely
resulted from reduced absorption from the gut. Therefore,
parasite infection does not alter the whole-body turnover
rate, but tends to change the profiles in the free amino pool
of the body by affecting availability of some amino acids
from the gastrointestinal source.
Changes in the gut. Most changes in protein and energy
metabolism attributable to internal parasites occur in the
gastrointestinal tract (GIT) where it is generally accepted
that protein synthesis increases for repairing damaged
tissues. Arterio-venous difference techniques showed that
Leu sequestration by the whole GIT in Suffolk crossbred
lambs increased by 24%, while Leu oxidation also increased
Australian Journal of Experimental Agriculture 1411
during the period from 5 to 7 and 11 to 13 weeks of infection
with T. colubriformis and these changes vanished by
18–20 weeks of infection (Yu et al. 2000), possibly because
the nature of the immune response had changed. Differences
between sequestration and oxidation, which accounts for Leu
used for protein synthesis, did not alter during infection.
Fractional synthesis rate (FSR) of protein, measured as direct
incorporation of an isotope into tissue protein, was
unchanged in the small intestine of guinea pigs infected with
T. colubriformis and N content of the intestinal tissue relative
to liveweight increased (Symons and Jones 1983). These
results indicate that FSR in the GIT may change depending
on a period of infection, probably increasing during the
period of development of immunity. An increase in amino
acid oxidation in the GIT would certainly reduce its
availability to the peripheral tissues.
A recent study using multi-tracers revealed that the GIT
oxidises essential amino acids in a differential manner and
not all essential amino acids are necessarily oxidised by the
GIT (Lobley et al. 2003). The GIT of sheep oxidised Leu and
Met, but not Lys and Phe. Oxidation of Leu and Met by the
GIT accounted for 25 and 9%, respectively, to their
whole-body oxidation, reducing their net appearance across
the portal-drained viscera by 23 and 11%, respectively
(Lobley et al. 2003). Parasite infection enhanced Leu
oxidation, as mentioned above, but reasons for this increase
are not clear. Met oxidation could also be stimulated by
parasite infection, probably during the first pass across the
GIT as indirectly indicated by reduced Met ILR (see above).
The catabolised Met can be used for synthesis of Cys or
spermidine and spermine. Cys is a substrate for the synthesis
of many compounds involved in development of immunity
(Grimble 2002). Spermidine and spermine are associated
with the proliferation rate of cells, and their concentrations
in the jejunum of sheep were significantly increased by
parasite infection (S. M. Liu et al. unpublished data)
indicating an increased demand for Met. Although our
knowledge of utilisation by the GIT is limited to only a few
amino acids in uninfected sheep (Lys, Leu, Met, Phe, see
Lobley et al. 2003), and even fewer amino acids in parasite
infected sheep (Leu, Yu et al. 2000; Cys and Val,
Bermingham et al. 2000), it may be concluded that amino
acid profiles across the GIT are changed by the infection.
However, at this stage it is not possible to give a quantitative
description on changes in all the important individual amino
acids.
Liver and other tissues. Liver protein FSR was increased
by parasite infection in the small intestine of sheep when
compared with pair-fed uninfected animals, while total liver
N content declined or remained unchanged and albumin FSR
increased (Symons and Jones 1975; Jones and Symons
1982). Increase in FSR of liver protein has also been
observed in guinea pigs infected with T. colubriformis
(Symons and Jones 1978).
1412 Australian Journal of Experimental Agriculture
The effects of parasite infection on protein turnover in the
lymph nodes and the spleen of sheep have not been reported.
The abomasal lymph nodes of Merino hoggets (about 63 kg)
weighed 1.8 g in uninfected sheep and increased to 7.0 g in
sheep infected with T. colubriformis for 18 weeks (S. M. Liu
et al. unpublished data). In 10-day-old chicks protein
synthesis in the thymus was increased by 18–42% and in the
spleen γ-globulin synthesis was 21–52% higher 2–6 days
after chicks were immunised with sporulated oocysts of a
mixture of Eimeria tenella and E. acervulina; protein
synthesis at the infection site in the intestine rose by 22–36%
(Mishin et al. 1982). These responses may be a short term
reaction to coccidial infection, which may differ from
chronic responses to continuous challenge with nematode
larvae.
Muscles. In response to infection with T. colubriformis
muscle protein synthesis was similar to that in uninfected,
pair-fed sheep (Symons and Jones 1975; Jones and Symons
1982). Total N content of muscle was reduced in infected
sheep, indicating a substantial increase in protein
degradation in muscle in response to parasite infection.
Recent measurements of arterio-venous differences across
the hind limbs showed that the net flux of amino acids was
not affected by infection with T. colubriformis for 48 days
(Bermingham et al. 2002), suggesting no change in protein
turnover in the muscle. These results indicate that protein
synthesis rate in skeletal muscle is not altered in response to
parasitic infection, while degradation rate may increase.
Protein synthesis in wool follicle homogenate declined in
sheep infected with a single dose of 60000 T. colubriformis
larvae (Symons and Jones 1975).
Interactions between nutrition and parasitism/immunity —
analyses and suggestions
Possible changes in nutrient demands in parasitised
animals. In order to understand nutrient partitioning during
infection, the overall detrimental effects of parasitism on
production must be separated from the effects of reduced
feed intake, and the effects that are caused directly by
activation of the immune response per se. The latter can be
determined by comparing uninfected sheep pair-fed to
infected animals.
Symons and Jones (1975) compared Merino × Border
Leicester sheep infected with Trichostrongylus with
uninfected pair-fed sheep. While there were no significant
differences in muscle and liver protein synthesis, the weight
gain of infected sheep was 14% lower, plasma urea
concentration 26% higher, and total muscle N was
significantly lower (28%). These results suggest that
immunity-associated response (or pathophysiological
reactions) to larval challenge can result in a loss of
productive performance over and above that caused by a
reduction in food intake. The immunity-associated loss
seems to be related to increased oxidation of amino acids (as
S. M. Liu et al.
indicated by urea concentration in plasma). Leu oxidation in
the GIT of sheep infected with T. colubriformis was
increased (Yu et al. 2000). Urinary N excretion in Scottish
Blackface lambs infected with Haemonchus contortus was
higher compared with their pair-fed controls (Abbott et al.
1985). It is not very clear why oxidation is increased during
infection, and it is speculated that an imbalance of amino
acids related to Cys deficiency could be one of the reasons.
Increase gluconeogenesis from amino acids by the liver may
be another reason (Campbell 1999). Changes in some
hormones, such as cortisol and insulin, may also be involved
in increased catabolism (Adams and Liu 2003). Prichard
et al. (1974) found that plasma cortisol concentration rose
and insulin levels fell at the time sheep became anorexic and
lost weight when infected with T. colubriformis.
In summary, the costs of immunity-associated response to
parasites may be estimated as follows:
(1) Replacement of protein loss from the GIT, including
leakage of plasma proteins, sloughing of epithelial cells and
secretion of mucoproteins. The extra costs caused by
parasitism can be estimated from a range of sources and
information: these include 1.2–0.9 g N/day during weeks
8 to 14 of infection with T. colubriformis (Kimambo et al.
1988); 1.5 g ileal N plus 0.9 g plasma protein N/day in lambs
(Poppi et al. 1981); 0.5–1.2 g N/day (0.44 g enteric plasma
N loss/day in uninfected sheep) depending on severity of
infection (Steel et al. 1980), or about 1 g plasma N/day loss
with Ostertagia circumcincta infection (Symons et al. 1981).
On average, 1 g N/day, equivalent to a net loss of about
6 g protein/day seems probable, although this may change
with stage of infection.
(2) Costs related to changes in the GIT metabolism. As
discussed above, gut FSR does not increase but oxidation of
amino acids does. Small-intestinal infection increased Leu
oxidation by 2.7 mmol/day (Yu et al. 2000), equivalent to 6
g of all amino acids assuming that Leu in plasma accounts
for 0.06 of total amino acids (calculated from arterial
concentrations, Lobley et al. 1996) and the other amino acids
are oxidised in the same proportions as Leu by the GIT.
Poppi et al. (1981) reported an extra 1–1.5 g N lost from
urine in lambs infected with T. colubriformis which is very
close to the estimated 6 g increase in amino acid oxidation in
the GIT.
Components (1) and (2) are equivalent to about 12 g
protein/day, and represent a net cost because they are not
recycled. It should be emphasised that the protein loss could
vary with the stage and level of parasite infection, parasite
species and organ affected, and quantitative relationships
between the nutrient loss and the development and
expression of immunity to infection should be defined when
more information is available. Other demands for amino
acids include increased synthesis of γ-globulin and other
immune proteins, although these may be recycled. Recycling
of proteins will increase losses from oxidation, but this loss
Impact of nematode parasitism on nutrient partitioning
may have been accounted for in increased amino acid
oxidation described above. Some extra energy will be used to
support this recycling.
The net cost of 12 g protein for the immunity-associated
response can be converted to a MP requirement using an
efficiency of 0.7, assuming a similar efficiency for both body
protein gain and immunity associated-protein synthesis.
Therefore 17 g/day of additional MP is needed which is
equivalent to 0.57, 0.71, 0.14 and 0.77 of the MP
requirements for growth, late pregnancy, early lactation and
wool production respectively (see Table 1). These
calculations indicate that the protein costs of development
and expression of an immunity-associated response to
internal parasites will result in a strong competition for
nutrients between the immune response and production. This
is particularly so in late pregnancy and early lactation, since
the estimated MP requirements for immune activation plus
production amount already to about 1.2 and 2.8 times
maintenance. Such high demands for protein could not be
matched by pastures in late summer and early spring in
Mediterranean environments, and would effectively reduce
the animal’s nutritional status. The deteriorating body
condition during late pregnancy and early lactation is
accompanied by a relaxation of immunity and consequent
increase in faecal egg count (Adams and Liu 2003). A
protein deficit is apparently more critical to immunity than
an energy deficit by the end of pregnancy since ewes are
highly responsive in wool growth and weight gain to
rumen-protected protein supplementation in late pregnancy
(Masters and Mata 1996).
Protein or energy
The energy cost for the synthesis of 12 g protein is about
0.36 MJ, or 0.51 MJ ME (see note with Table 1 ), less than
5% of the daily ME requirements (Table 1), and includes the
energy value of the protein (23.1 kJ/g) per se, which is
released when amino acids are oxidised and used by the
body. On the other hand, there will be some energy
consumption related to degradation of these proteins, which
is usually about half of that utilised for protein synthesis
(Lobley 1994b). Overall, an estimated 5% increase in ME
requirement seems reasonable. There is no evidence that
changes in fat deposition are associated with activation of the
immune system. The extra energy requirements to cope with
parasitism and increased immune function are not expected
to be as significant as the demands for additional protein.
The consequence of changes in demand for protein and
energy by immunity-associated response are that the
MP:ME ratio required would be further increased to 6.9, 7.9,
8.3 and 8.1, respectively, for growing, pregnant, lactating and
wool-producing animals. Such a high protein:energy ratio
can be provided by feeding legume hays (for example,
lucerne hay provides a MP:ME ratio greater than 10 g/MJ),
but not by feeding grass hays (generally less than 6 g/MJ).
Australian Journal of Experimental Agriculture 1413
A ration that contains 0.1 lupin seeds, 0.2 barley and
0.7 oaten hay gives a MP:ME ratio of 7.1 g/MJ. The
estimated MP:ME ratio provided by pastures comprising
15% capeweed, 15% clover and 70% grass in a
Mediterranean climate from February to May (autumn) is
estimated to be about 4.6 g/MJ (R. Dynes pers. comm.).
There is therefore a significant deficiency of protein for
reproduction if autumn lambing is arranged to be in May.
When rain comes and green pastures start growing, MP:ME
ratio of pastures increases to 7.2–8.9 g/MJ as green growing
pastures contain relatively more protein and also relatively
high proportions of capeweed (Arctotheca calendula) and
clover (Trifolium subterraneum, R. Dynes pers. comm.).
However, because of low pasture intake, a deficiency in the
energy supply from green pastures in late autumn, and in
both energy and protein in late summer and autumn (Allden
1981) is likely to compromise the ability of parasitised sheep
to gain weight or grow wool.
The protein:energy ratio is helpful in determining dietary
protein requirements. However, using the ratio may also lead
to a misunderstanding of energy needs in parasite infected
animals. Both total energy intake and protein:energy ratio
should be simultaneously taken into consideration. There are
two reasons for this. The level of energy intake affects
protein utilisation, and protein efficiency (accretion/intake)
is positively related to non-protein energy intake (Miller
2002). A low level of energy leads to more amino acids being
oxidised to satisfy energy demand and more dietary protein
being required to retain the same amount of body protein.
Therefore, energy should be provided as much as possible to
ensure protein is used efficiently.
Body conditions and current feed intake
Malnutrition and a high susceptibility to parasitism often
occur concurrently, making it difficult to resolve cause and
effect relationships between the malnutrition and parasite
infection (Koski and Scott 2001). A relaxation of immunity
seems to be triggered by a severe nutrient deficiency,
possibly through hormonal mechanisms. However, a
subclinical infection can still be established in sheep fed
ad libitum with a good diet providing 62 g MP/kg and
8.5 MJ ME/kg, and loss of the productivity (weight gain and
wool growth) gradually occurs after 10 weeks of challenge
with parasitic larvae (S. M. Liu et al. unpublished).
Conceptually, it has been well accepted that body condition
affects susceptibility to infection. However, quantitative
relationships between the changes in the body condition,
development of immunity and parasitological epidemiology
have not been fully described. These relationships have to be
defined for developing guidance to parasite control.
Comparing relationships between body condition, feed
intake and susceptibility to infection is important,
particularly in late pregnant — early lactating ewes. During
protein depletion, tissues with high turnover rates such as the
1414 Australian Journal of Experimental Agriculture
gut and skin lose their protein reserves more rapidly than
tissues with low turnover rates (e.g. muscle, Adams and Liu
2003). When animals undergo a sub- to super-maintenance
cycle the proportional loss and gain of splanchnic tissues is
of higher magnitude than the proportional loss and gain of
liveweight and the changes in the small intestines seem to be
attributed to the changes in the epithelium while the weight
of muscular layers remains constant (Ortigues and Doreau
1995). Reduced protein mass in the gut mucosa is likely to
impair development of local immunity, although directly
experimental confirmation of the relationship between the
epithelium mass and the magnitude of immune response has
not been reported. A relaxation of immunity occurs during
this period while feed intake is usually increased, though not
enough to meet nutrient demands as indicated by negative
energy and protein balances (Adams and Liu 2003). This
suggests that the body condition in reproductive period
would be predominant factor responsible for immunity
relaxation.
Young lambs in Mediterranean environments are often
susceptible to parasite infection. This usually occurs during
summer and autumn when pasture supply is reduced
substantially and lambs usually gain little or even lose
weight. There is no doubt that the body condition of animals
deteriorates, which accompanies with a high susceptibility to
parasitism. Coop and Kyriazakis (1999) proposed that when
feed supply is limited, nutrients are partitioned in a priority
order of maintenance of body protein, protein gain,
expression of immunity and gain of body lipid. Young
growing animals not gaining in liveweight are not expressing
their genetic potential for body growth and may be
considered to be in a state of nutrient deficiency. It can be
envisaged that the highly parasitic susceptibility is resulted
from nutrient deficiency. An improvement of nutrition by
supplementation can greatly affect the expression of
immunity of growing animals as reviewed by Coop and
Kyriazakis (1999). The body condition is the result of a
long-term plane of dietary intake. In young growing animals,
the level of body condition and the required body growth rate
that indicates a nutrient supply sufficient to satisfy the
requirement for both body gain and immune response is
unknown. Clarification of the relative importance of body
reserves v. current intake for immune development is needed
to develop effective nutritional strategies for young animals
with parasitism.
Special demands for some amino acids by the immune system
Requirements for specific amino acids may be estimated
from the chemical composition of immune components and
the nutrient demands to maintain the system. It has been
suggested that the Cys requirement for immunity-associated
responses may be high, possibly due to the very high
concentration of Cys in mucins, a component of mucus.
Indeed, Cys accounts for about 4–9% of amino acid
S. M. Liu et al.
sequences of various mucins (mouse and humans), as shown
in the protein database of the National Centre for
Biotechnology Information. These concentrations of Cys are
2–4 times higher than for other body tissue proteins (about
2–3%, except for wool protein). Cys is also used in the
synthesis of acute-phase proteins, leucocytes and
glutathione. Both Cys and glutathione (GSH) are required in
the biosynthesis of the inflammatory mediators, leukotrienes
C, D and E and some cytokines (Grimble 2002).
Supplementation of 2 g/day cysteine to Romney sheep
infected with Haemonchus contortus and T. colubriformis
increased peripheral eosinophilia and abomasal globular
leukocyte counts, both of which have effector roles in
combating parasites, during the infection period of 3 weeks,
indicating that extra Cys can improve certain aspects of
immunocompetency in sheep (Miller et al. 2000). Although
it is expected to be high, the actual consumption of Cys for
these compounds is still unknown and there is no reported
quantification of mucins excreted in uninfected and infected
animals, or of the inflammatory mediators.
Metabolism of amino acids that have been studied in
sheep infected with parasites include Tyr, Leu, Phe, Val, Cys
and Met and of these, the latter 2 seem to be most affected
with whole-body ILR declining by 13–15% (Bermingham
et al. 2000; Liu et al. 2002). Hoskin et al. (2002) observed
that Cys ILR per g N intake declined by 8, 14 and 17% in
weeks 4, 8 and 12, respectively, of infection with
T. colubriformis, compared with the pre-infection period,
and daily abomasal supplementation of 2 g Cys/day partially
reduced the magnitude of the decline. Consistent reports of
reduced Cys ILR with infection indicate a preferential use of
Cys by the immune system and a reduction in the availability
of this amino acid for tissues. A reduction of Met ILR is
attributed to an increased conversion of Met to Cys through
the transsulfuration pathway, supporting the high demand of
Cys during infection. The reduction in Cys and Met ILR
without a change in the other amino acids suggests that either
absorption was reduced or oxidation of these 2 amino acids
is increased disproportionately to the other amino acids. In
addition, there is a reduced absorption of Met from the GIT
as indicated by lower Met available in the mesenteric vein
compared with levels in the artery, hepatic and portal veins
and the vena cava of infected sheep (Liu et al. 2002).
Glutamine (Gln) is another amino acid that is considered
to play an important role in maintaining immune function. It
also serves as a major energy source for the GIT. The
significance of Gln to protein and energy metabolism and
production has been reviewed recently (Lobley et al. 2001).
However, quantitative data on changes in Gln demand by the
immune system have not been reported. Recent work (Reeds
et al. 2000) demonstrates that dietary glutamate, not Gln, is
a major energy contributor to the gut mucosa of fast growing
pigs, and its functions apparently differ from those of arterial
Impact of nematode parasitism on nutrient partitioning
Gln. If this applies in sheep, the function of glutamate in
local immunity of the gut warrants study.
The GIT is the tissue directly affected by nematode
parasite infection. The impact of the infection on host
nutrition depends, at a large extent, on the responsive
magnitude of the GIT over and above its ‘basal’ metabolism,
and the changes related to the inflammatory responses from
the infection. The GIT preferentially takes up essential
amino acids (histidine, isoleucine, Leu, Lys, Phe, Thr and Val
being studied) from the arterial supply and the lumen of the
tract, according to amino acid concentrations of its protein
(MacRae et al. 1997), and the partitioning of sequestrated
amino acids either to protein synthesis or to oxidation differs
significantly between amino acids (Fuller and Reeds 1998;
Lobley et al. 2003). It is not clear how this kind of preferable
use changes with parasite infection, particularly with an
inflammatory response. More information is essential to
optimise nutritional strategies for production in parasitised
animals.
Interactions between immunity and genetics
Wool and meat type sheep. Responses associated with
immunity to parasites demands more protein relative to
energy, similarly to the nutritional physiology of wool
production. It can be expected therefore that there is strong
competition between the immune response and wool growth,
particularly in wool-producing genotypes which grow more
wool totally or per unit skin area and so require more protein.
Protein accretion in weight gain is similar between breeds
(Agricultural Research Council 1984). A high demand of
Cys for wool protein synthesis draws disproportionately on
Cys and Met from the total body amino acid pool and creates
a relative deficiency of Met. Because of this, efficiency of
protein utilisation for weight gain in wool-producing sheep is
likely to be lower than in meat type sheep and parasitic
infection would be expected to have greater impact in the
former at the same protein intake. This expectation has been
demonstrated by (Abbott et al. 1984) where the level of
anaemia, hypoproteinaemia and pathophysiological changes
following H. contortus infection were more marked in
Merino compared with Scottish Blackface lambs. To manage
this impact more dietary protein will be required by wool
producing sheep.
Worm resistant v. susceptible sheep. If the resistance of
sheep to worms is attributed to stronger immunity-associated
responses, then the concomitant nutrient costs of the
responses will be high. The level of specific nutrients, for
example Cys, Met and Gln, would be more important than
the overall level of protein and energy. Our recent experiment
(S. M. Liu et al. unpublished data) showed that
worm-resistant sheep had lower blood GSH concentrations
during infection with T. colubriformis compared with
susceptible sheep at the same level of dietary intake. GSH is
involved in a number of regulatory steps of the immune
Australian Journal of Experimental Agriculture 1415
system, including T-cell function. It is also an antioxidant, a
substrate for synthesis of some inflammatory factors,
provides Cys to tissues and also affects the redox potential of
the tissue. All these functions may be related to development
of strong immunity or resistance in the GIT.
Parasites secrete proteases (e.g. cysteine protease, serine
protease) to hydrolyse surface proteins, haemoglobin,
fibrinogen, collagen and immunoglobulin G (Rhoads and
Fetterer 1995), presumably for their amino acid source.
Surface proteins containing free thiol groups are more likely
to be attacked by the proteases compared with their
corresponding disulphides, so surfaces with disulphide
crosslinking are possibly more resistant to proteolytic
digestion (Papanastasiou et al. 1997). Resistant sheep also
excrete high levels of mucins from the GIT (G. E. Lobley
pers. comm.), probably leading to increased demand for Cys.
On the other hand, nutrient costs directly related to tissue
damage by worms per se would be less because of lower
worm egg output and worm burden in resistant genotypes. So
the overall changes of protein and energy demands in worm
resistant and susceptible sheep may be similar, but Cys and
Met requirements by resistant sheep would be higher. Wool
growth rate could be reduced if immunity requires more
sulfur-containing amino acids. Consistent unfavourable
correlations between faecal egg count (FEC) and fleece
weight in Romney sheep (Morris et al. 2000) and Merino
sheep (Eady et al. 1998) support this speculation. The impact
of genetic selection for low FEC on the nutritional status of
sheep is poorly understood and may be important in
determining whether breeding for resistance can be
universally recommended (Adams and Liu 2003).
There seems to be an interaction between the capacity of
sheep to resist parasites and the level of nutrition, and good
nutrition is required to maintain strong resistance. This was
observed in Scottish Blackface lambs (Stear et al. 2000)
where relatively resistant sheep on a normal diet
supplemented with urea allowed fewer larvae to establish,
and a combination of relatively resistant sheep and
nutritional supplementation appeared most efficient at
controlling infection. In contrast, in a recent review on the
influences of nutrition on pathophysiological changes
resulting from infections with Haemonchus in Scottish
Blackface, Finn Dorset, Hampshire Down and Merinos,
Coop and Kyriazakis (1999) concluded that resilience can be
improved more by nutrient supplementation in susceptible
sheep, whereas in relatively resistant sheep the improvement
was more marginal. Further investigation is needed to
determine whether this conclusion can be applied to
infection with other parasite species.
Summary
Infestation of the small intestine with internal parasites
may result in a total net loss of up to 12 g protein/day,
resulting in a strong competition for protein. This
1416 Australian Journal of Experimental Agriculture
considerable demand for protein by immunity-associated
responses reduces nutrient status in late pregnancy and early
lactation. Such increased demand cannot be matched by
pastures during the reproductive season in Mediterranean
environments, and may cause immune relaxation over these
periods. The immunity-associated response requires more
protein rather than energy, particularly sulfur amino acids
such as cysteine and probably methionine, and the body
condition of sheep may be a predominant factor in
determining immune status. Current intake level and quality
of pastures need to be considered to further boost
immunity-associated response. Parasite resistant sheep in
particular have different interactions with nutrition in
response to parasite infection. These factors need to be
integrated with drenching to establish effective strategies to
control parasite infections, particularly in Mediterranean
environments where there are marked seasonal changes in
nutrient availability.
References
Abbott EM, Parkins JJ, Holmes PH (1984) Studies on the
pathophysiology of chronic ovine haemonchosis in Merino and
Scottish Blackface lambs. Parasitology 89, 585–596.
Abbott EM, Parkins JJ, Holmes PH (1985) Influence of dietary protein
on the pathophysiology of ovine haemonchosis in Finn Dorset and
Scottish Blackface lambs given a single moderate infection.
Research in Veterinary Science 38, 54–60.
Adams NR, Liu SM (2003) Principles of nutrient partitioning for wool,
growth and reproduction: implications for nematode parasitism.
Australian Journal of Experimental Agriculture 43, 1399–1407.
Agricultural Research Council (1984) ‘The nutrient requirements of
ruminants livestock.’ (Commonwealth Agricultural Bureaux:
Slough, UK)
Allden WG (1981) Problems of animal production from Mediterranean
pastures. In ‘Nutritional limits of animal production from pastures’.
(Ed. JB Hacker) pp. 45–65. (Commonwealth Agricultural Bureaux:
St Lucia, Qld)
Bermingham EN, McNabb WC, Reynolds GW, Sutherland IA,
Peters JS, Treloar BP, Sinclair BR, Waghorn GC, Revell DK,
Roy NC (2002) Amino acid flux across the hind limbs in lambs feed
fresh lucerne (Medicago sativa) with or without Trichostrongylus
colubriformis infection. Animal Production in Australia 24, 25–28.
Bermingham EN, McNabb WC, Reynolds GW, Waghorn GC,
Sutherland IA, Revell DK, Roy NC (2000) Whole-body irreversible
loss rate of cysteine and valine in sheep with or without a
Trichostrongylus colubriformis infection. Asian–Australian Journal
of Animal Science 13 (Suppl. C), 196–199.
Campbell IT (1999) Limitations of nutrient intake. The effect of
stressors: trauma, sepsis and multiple organ failure. European
Journal of Clinical Nutrition 53 (Suppl. 1), S143–S147.
Coop RL, Kyriazakis I (1999) Nutrition–parasite interaction. Veterinary
Parasitology 84, 187–204.
Degussa (1996) ‘The amino acid composition of feedstuffs.’ (Degussa
Corporation: Frankfurt am Main, Germany)
Eady SJ, Woolaston RR, Lewer RP, Raadsma HW, Swan AA,
Ponzoni RW (1998) Resistance to nematode parasites in Merino
sheep: correlation with production traits. Australian Journal of
Agricultural Research 49, 1201–1211.
Fuller MF, Reeds PJ (1998) Nitrogen cycling in the gut. Annual Reviews
of Nutrition 18, 385–411.
S. M. Liu et al.
Grimble RF (2002) Sulphur amino acids, glutathione and immune
function. In ‘Nutrition and immune function’. (Eds PC Calder,
CJ Field, HS Gill) pp. 133–150. (CABI Publishing: Wallingford,
UK).
Hoskin SO, Lobley GE, Coop RL, Jackson F (2002) The effect of
cysteine and glutamine supplementation on sheep infected with
Trichostrongylus colubriformis. Proceedings of the New Zealand
Society of Animal Production 62, 72–76.
Jones WO, Symons LEA (1982) Protein synthesis in the whole body,
liver, skeletal muscle and kidney cortex of lambs infected by the
nematode Trichostrongylus colubriformis. International Journal for
Parasitology 12, 295–301.
Kimambo AE, MacRae JC, Walker A, Watt CF, Coop RL (1988)
Effect of prolonged subclinical infection with Trichostrongylus
colubriformis on the performance and nitrogen metabolism of
growing lambs. Veterinary Parasitology 28, 191–203.
Koski KG, Scott ME (2001) Gastrointestinal nematodes, nutrition and
immunity: breaking the negative spiral. Annual Reviews on
Nutrition 21, 297–321.
Liu SM, Mata G, O’Donoghue H, Masters DG (1996) Protein synthesis
in the skin of Merino lambs, measured by a flooding dose of
2
H5-phenylalanine, using gas chromatography/mass spectrometry.
Proceedings of the Nutrition Society of Australia 20, 196.
Liu SM, Travendale M, Bermingham EN, Roy NC, McNabb WC, Lee J
(2002) The effects of parasite infection on methionine metabolism
in sheep. Animal Production in Australia 24, 133–136.
Lobley GE (1994a) Amino acid and protein metabolism in the whole
body and individual tissues of ruminants. In ‘Principles of protein
nutrition of ruminants’. (Ed. JM Asplund) pp.147–178. (CRC Press:
Boca Raton, FL, USA)
Lobley GE (1994b) Nutritional and endocrine regulation of energy
metabolism. In ‘Energy metabolism of farm animals: the 13th
symposium’. (Ed. Aguilera) pp. 139–149. (Servicio de
Publicaciones: Majorca)
Lobley GE, Connell A, Revell D, Bequette BJ, Brown DS, Calder AG
(1996) Splanchnic-bed transfer of amino acids in sheep blood and
plasma, as monitored through use of a multiple U- 13C-labelled
amino acid mixture. British Journal of Nutrition 75, 217–235.
Lobley GE, Hoskin SO, McNeil CJ (2001) Glutamine in animal science
and production. Journal of Nutrition 131, 2525S–2531S.
Lobley GE, Shen XZ, Le GW, Bremner DM, Milne E, Calder AG,
Anderson SE, Dennison N (2003) Oxidation of essential amino
acids by the ovine gastrointestinal tract. British Journal of Nutrition
89, 1–14.
MacRae JC, Bruce LA, Brown D, Calder AG (1997) Amino acid use by
the gastrointestinal tract of sheep given lucerne forage. American
Journal of Physiology 273 (Gastrointestines and Liver Physiology),
G1200–G1207.
MacRae JC, Walker A, Brown D, Lobley GE (1993) Accretion of total
protein and individual amino acids by organs and tissues of growth
lambs and the ability of nitrogen balance techniques to quantitate
protein retention. Animal Production 57, 237–245.
Masters DG, Mata G (1996) Responses to feeding canola meal or lupin
seed to pregnant, lactating, and dry ewes. Australian Journal of
Agricultural Research 47, 1291–1303.
Miller EL (2002) Protein nutrition, requirements of farmed livestock
and dietary supply. In ‘Expert consultation and workshop on protein
sources for the animal feed industry’. (FAO: Bangkok, Thailand)
Miller FM, Blair HT, Birtles MJ, Reynolds GW, Gill HS, Revell DK
(2000) Cysteine may play a role in the immune response to internal
parasites in sheep. Australian Journal of Agricultural Research 51,
793–799.
 Impact of nematode parasitism on nutrient partitioning
Mishin VS, Kindras NA, Krylova NP, Maksimova OV, Loskot VI (1982)
Immunization of chicks against coccidiosis with application of
thiacoccid. Sbornik Nauchnykh Rabot Leningradskogo
Veterinarnogo Instituta 72, 68–70.
Morris CA, Vlassoff A, Bisset SA, Baker RL, Watson TG, West CJ,
Wheeler M (2000) Continued selection of Romney sheep for
resistance or susceptibility to nematode infection: estimates of
direct and correlated responses. Animal Science 70, 17–27.
Ortigues I, Doreau M (1995) Responses of the splanchnic tissues of
ruminants to changes in intake: absorption of digestion end
products, tissue mass, metabolic activity and implications to whole
animal energy metabolism. Annales de Zootechnie 44, 321–346.
Papanastasiou P, Bruderer T, Li Y, Bommeli C, Kohler P (1997) Primary
structure and biochemical properties of a variant-specific surface
protein of Giardia. Molecular Biochemistry and Parasitology 86,
13–27.
Poppi DP, MacRae JC, Corrigall W (1981) Nitrogen digestion in sheep
infected with intestinal parasites. Proceedings of the Nutrition
Society 40, 116A.
Prichard RK, Hennessy DR, Griffiths DA (1974) Endocrine response of
sheep to infection with Trichostrongylus colubriformis. Research in
Veterinary Science 17, 182–187.
Reeds PJ, Brurrin DG, Stoll B Jahoor, F (2000). Intestinal glutamate
metabolism. Journal of Nutrition 130, 978S–982S.
Rhoads ML, Fetterer RH (1995) Developmentally regulated secretion
of cathepsin L-like cysteine proteases by Haemonchus contortus.
Journal of Parasitology 81, 505–512.
Schaefer AL, Krishnamurti CR (1984) Whole body and tissue
fractional protein synthesis in the ovine foetus in utero. British
Journal of Nutrition 52, 359–369.
Standing Committee on Agriculture RS (1990) ‘Feeding standards for
Australian livestock.’ (CSIRO: Melbourne)
Steel JW, Symons LEA, Jones WO (1980) Effects of level of larval
intake on the productivity and physiological and metabolic
responses of lambs infected with Trichostrongylus colubriformis.
Australian Journal of Agricultural Research 4, 821–838.
http://www.publish.csiro.au/journals/ajea
View publication stats
Australian Journal of Experimental Agriculture 1417
Stear MJ, Bairden K, Duncan JL, Eckersall PD, Fishwick G,
Graham PA, Holmes PH, McKellar QA, Mitchell S, Murray M,
Parkins JJ, Wallace DS (2000) The influence of relative resistance
and urea-supplementation on deliberate infection with Teladorsagia
circumcincta during winter. Veterinary Parasitology 94, 45–54.
Symons LEA, Jones WO (1975) Skeletal muscle, liver and wool protein
synthesis by sheep infected by the nematode Trichostrongylus
colubriformis. Australian Journal of Agricultural Research 26,
1063–1072.
Symons LEA, Jones WO (1978) Protein metabolism. 5.
Trichostrongylus colubriformis: changes of host body mass and
protein synthesis in guinea pigs with light to heavy infections.
Experimental Parasitology 44, 7–13.
Symons LEA, Jones WO (1983) Intestinal protein synthesis in guinea
pigs infected with Trichostrongylus colubriformis. International
Journal for Parasitology 13, 309–312.
Symons LEA, Steel JW, Jones WO (1981) Effects of level of larval
intake on the productivity and physiological and metabolic
responses of lambs infected with Ostertagia circumcincta.
Australian Journal of Agricultural Research 32, 139–148.
Yu F, Bruce LA, Calder AG, Milne E, Coop RL, Jackson F, Horgan GW,
MacRae JC (2000) Subclinical infection with the nematode
Trichostrongylus colubriformis increases gastrointestinal tract
leucine metabolism and reduces availability of leucine for other
tissues. Journal of Animal Science 78, 380–390.
Received 8 January 2003, accepted 9 May 2003