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Small Ruminant Research 62 (2006) 79–82

Immunonutrition: Nutritional control of parasites夽


I. Kyriazakis a,b,∗ , J. Houdijk b
a Veterinary Faculty, University of Thessaly, P.O. Box 199, 43100 Karditsa, Greece
b Animal Nutrition and Health Department, Scottish Agricultural College, Kings Buildings, Edinburgh EH9 3JG, UK

Available online 9 September 2005

Abstract

Whilst it has long been known that improved protein nutrition can increase resilience, i.e. reduce the consequences of sub-
clinical gastrointestinal nematode parasitism on sheep performance, improved protein nutrition can also increase resistance, i.e.
immunity to parasites. This would be the case because expression of acquired immunity to parasites is often penalized at times of
nutrient scarcity. A recently developed nutrient-partitioning framework postulates that this penalty arises from prioritized scarce
nutrient allocation to growth and/or reproductive functions. A large body of evidence shows that at times of protein scarcity, an
increased supply of protein, from a wide range of protein sources, can indeed reduce gastrointestinal nematode parasitism in both
growing and periparturient sheep. As such, immunonutrition can play a vital role in sustainable, parasite control strategies, either
on its own but more likely integrated with other non-chemical strategies, including genetic selection for increased resistance,
vaccination and biological control.
© 2005 Elsevier B.V. All rights reserved.

Keywords: Sheep; Nutrition; Parasitism; Control; Immunology; Defence mechanisms

1. Introduction known, or at least suspected that improved nutrition


may detrimentally affect gastrointestinal nematodes in
Gastrointestinal nematode parasitism has major sheep (Taylor, 1935). Nutrition can affect gastroin-
detrimental effects on the efficiency of sheep produc- testinal nematodes through its influence on resistance,
tion; production losses up of to 50% are not uncom- i.e. the ability to regulate gastrointestinal nematode
mon (Sykes, 1994). Gastrointestinal nematode para- establishment, fecundity and survival. This is mainly
sitism reduces sheep performance through affecting mediated through acquired immunity, and thus nutri-
their nutritional status. Conversely, it has also long been tion has the potential to affect the rate of acquisition
and/or the degree of expression of immunity. Most
research into the effects of nutrition on immunity to
夽 This paper is part of a special issue entitled Keynote Lectures of
gastrointestinal nematodes in sheep has concentrated
the 6th International Sheep Veterinary Congress—Guest Edited by
Dr. George C. Fthenakis and Prof. Quintin A. McKellar.
on metabolizable protein (MP). This seems sensi-
∗ Corresponding author. ble since many components of the immune effector
E-mail address: ilias.kyriazakis@sac.ac.uk (I. Kyriazakis). responses are highly proteinaceous in nature (Coop and

0921-4488/$ – see front matter © 2005 Elsevier B.V. All rights reserved.
doi:10.1016/j.smallrumres.2005.07.036
80 I. Kyriazakis, J. Houdijk / Small Ruminant Research 62 (2006) 79–82

Holmes, 1996). Consequently, the immune system can growth and reproduction would be prioritized over
be expected to draw on MP resources. However, like expression of immunity to parasites, as the former
any bodily function, the immune system would also bodily functions ensure preservation of the host’s
have requirements for energy and micronutrients like genetic material (Coop and Kyriazakis, 1999).
vitamins and minerals. In theory, an increased avail- This framework puts forward various hypotheses
ability of each of these resources can be expected to on the effects of MP nutrition on resistance to gas-
improve immunity to gastrointestinal nematodes pro- trointestinal nematodes. The difference between pri-
vided that they are first limiting. We will, however, ority for scarce resource allocation to acquisition and
focus on the role of MP nutrition; moreover, moderate expression of immunity relative to productive func-
changes in energy nutrition do not appear to greatly tions, leads to the hypothesis that changes in MP supply
affect gastrointestinal parasitism (Brown et al., 1991; would not be expected to affect the rate of acquisition
Donaldson et al., 1998; Houdijk and Athanasiadou, of immunity, but would greatly affect expression of
2003). immunity to gastrointestinal nematodes. Also, it can
be hypothesized that expression of immunity will be
penalized at times of increased nutrient requirements
2. A nutrient-partitioning framework of the prioritized reproductive effort. The latter implies
that the periparturient breakdown of immunity to gas-
Effects of MP supply on resistance to gastroin- trointestinal nematodes, which results in increased
testinal nematodes can be viewed within a recently worm burdens and nematode egg excretion around
developed nutrient-partitioning framework, which parturition (Barger, 1993), may have a nutritional
introduces the concept of prioritization for the allo- basis.
cation of scarce resources toward different bodily
functions; the higher the priority, the less likely host
nutrition would affect the bodily function (Coop and 3. Protein supplementation and
Kyriazakis, 1999). Animals would be expected to gastrointestinal parasitism
give the highest priority to the allocation of scarce
resources for maintenance functions, i.e. maintenance The suggestion that acquisition, but not expression,
of body protein, as this will guarantee survival in of immunity takes priority over growth implies that
the short term. This would include the repair and/or changes in MP supply, would be expected to affect
replacement of damaged and/or lost host tissue faecal eggs counts (FEC) and worm burdens only dur-
caused by parasitic infestation. Traditionally, immune ing the phase of expression of immunity. Thus, effects
functions have been regarded as part of the collectively of MP supply on the level of gastrointestinal nema-
termed “maintenance functions”, and hence would be tode parasitism would be expected to show temporal
expected to be prioritized over other bodily functions. effects; an increased MP supply would reduce FEC
However, since at least some aspects of immunity and worm burdens only at later stages in experimen-
are sensitive to changes in MP supply (Coop and tal parasitic infestations. We recently reviewed a large
Kyriazakis, 1999), immune functions are in this frame- body of evidence in support of this view (Houdijk and
work considered separately from maintenance. Thus, Athanasiadou, 2003). Two pivotal studies are briefly
once scarce nutrient allocation to maintenance has described here. Casein infused in the abomasum of
been fulfilled, the remaining scarce resources would growing Trichostrongylus colubriformis infested sheep
need to be allocated to bodily functions associated for 12 weeks reduced worm burdens by 55% at week
with growth, reproduction and immunity to parasites. 12, but worm burdens were not affected at week 6
The growing animal that encounters parasites for (Brown et al., 1991). Fishmeal supplementation to T.
the first time would be expected to prioritize scarce colubriformis infested sheep resulted in 44 and 99%
resource allocation to the acquisition of immunity over reduced worm burdens at weeks 15 and 20, respec-
growth; otherwise it may succumb to the adverse con- tively, but worm burdens did not differ at weeks 5 and
sequences of parasitism before reaching reproductive 10 (van Houtert et al., 1995). Moreover, MP supple-
maturity. However, once immunity has been acquired, mentation has resulted in an increased concentration
I. Kyriazakis, J. Houdijk / Small Ruminant Research 62 (2006) 79–82 81

of circulating and local inflammatory cells, sheep mast reducing MP demand or increasing MP supply resulted
cell proteases and circulating antibodies, especially in a more than 50% reduction in FEC and worm bur-
during the phase of expression of immunity (Coop and dens within a week (Houdijk and Athanasiadou, 2003;
Holmes, 1996; Israf et al., 1996; van Houtert et al., Houdijk et al., 2004). This strongly suggests that MP
1995). supplementation can be used to rapidly reduce the level
The proposed priority of reproductive effort over of gastrointestinal nematode parasitism.
expression of immunity would be reflected in a greater Compared to non-infested ones, parasitized sheep
penalty on the ewe’s ability to regulate worm burdens would require extra MP to repair or replace dam-
than on milk production at times of MP scarcity. Indeed, aged tissue and to develop and express immunity.
increasing dietary MP supply to Teladorsagia circum- Dose–response experiments in growing lambs and peri-
cincta infested, lactating ewes, from 0.65 to 1.25 times parturient ewes have indicated that MP requirements
their assumed MP requirements, resulted in increased are increased in the order of 20–25% (Datta et al.,
milk production for the first MP increments only, whilst 1998; Donaldson et al., 2001; Houdijk et al., 2003).
only the last increment resulted in a reduced worm bur- Such information can be used to amend the currently
den (Houdijk et al., 2005). Several other studies support used estimations for MP requirements (AFRC, 1993),
the view that protein supplementation to parasitized, accounting for the extra MP requirement due to gas-
periparturient ewes can reduce FEC and worm burdens trointestinal nematode infestations.
(Donaldson et al., 1998, 2001; Houdijk et al., 2000, The large body of evidence on interactions between
2001; Kahn et al., 2003). Unlike in growing lambs, MP nutrition and gastrointestinal nematode parasitism
there is only limited evidence in support of the view strongly suggest that strategic use of MP supplementa-
that protein supplementation affects immune effector tion could greatly contribute towards a non-chemical,
responses in periparturient ewes, although the limited sustainable parasite control in sheep production
evidence available suggest that protein supply results systems. The latter is increasingly being desired,
in increased numbers of globule leukocytes (Houdijk because chemical control of gastrointestinal nematode
et al., 2000, 2005). parasitism is no longer considered sustainable. This
The aforementioned outcomes have been observed is mainly due to the increasing rate of development
through supplementation with a wide range of protein of nematode resistance towards anthelmintic drugs
sources, including soybean meal, fishmeal, cottonseed (Jackson and Coop, 2000), but also to the increasing
meal and urea. The magnitude of these effects would be public concern about potential drug residues in animal
dependent on the degree of MP scarcity (Houdijk and products and need for non-pharmaceutical control
Athanasiadou, 2003; Kahn et al., 2003). As such, it of gastrointestinal nematodes in organic farming
would be expected that the largest benefit from protein systems. It is anticipated that nutritional control of
supplementation would be expected in multiple-rearing gastrointestinal nematodes will be part of an integrated
ewes in a relatively poor body condition and in growing approach for parasite control, e.g. together with
lambs with a high potential for growth. genetic selection for increased resistance, vaccination
and biological control, rather than being applied in
isolation (Waller, 1993; Coop and Kyriazakis, 2001).
4. Implications for parasite control Therefore, any development of non-chemical parasite
control strategies would require a multidisciplinary
The rate at which MP supply can improve expres- approach through close collaboration between nutri-
sion of immunity, will determine to a large extent the tionists, parasitologists, immunologists, geneticists
viability of using MP supplementation under field con- and veterinarians.
ditions. If, for example, it takes many weeks for MP
supplementation to reduce parasitism, then its practical
applicability for parasite control in sheep production References
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