2009, Vol. 4 No. 2, Article 39

Exploiting Nutrition-Parasite Interaction for Sustainable Control of Gastrointestinal Nematodosis in Sheep

D. Sumbria and P. K. Sanyal*

Department of Parasitology,
College of Veterinary Science & Animal Husbandry
Indira Gandhi Agricultural University Anjora, Durg-491 001, Chhattisgarh

*Corresponding Author; e-mail address: [email protected]

ABSTRACT

Parasites are a major constraint on animal productivity throughout the world. Gastrointestinal nematodes are ubiquitous parasites of grazing ruminants and cause decreases in survival, live-weight gain, wool and milk production and reproduction performance. These losses can be particularly severe in developing countries where control measures are less readily available. This overview focuses on the interaction between nutritional status and gastrointestinal nematode infection in ruminants and considers: (i) the influence of the parasite on host metabolism; and (ii) the effect of host nutrition on the establishment and survival of parasite populations, the development of the host-immune response and the pathophysiology of infection (Petkevičius, 2007). Gastrointestinal nematodes reduce voluntary feed intake and efficiency of feed utilisation, a key feature being an increased endogenous loss of protein into the gastrointestinal tract. Overall there is movement of protein from productive processes into repair of the gastrointestinal tract, synthesis of plasma proteins and mucoprotein production. Although reduction in feed intake is a major factor contributing to the reduced performance of parasitized ruminants, the underlying mechanisms of the anorexia are poorly understood (Coop and Kyriazakis, 1999). Supplementation of the diet with additional protein does not appear to affect initial establishment of nematode infections but the pathophysiological consequences are generally more severe on lower planes of protein nutrition. The main effect of protein supplementation is to increase the rate of acquisition of immunity and increase resistance to reinfection and this has been associated with an enhanced cellular immune response in the gastrointestinal mucosa. The unresponsiveness of the young lamb can be improved by dietary protein supplementation. Recent trials have shown that growing sheep offered a free choice between a low and a high protein ration (Swarnkar and Singh, 2005) or non-protein nitrogen supplementation through urea molasses mineral blocks (Roy, 2007), are able to modify their diet selection in order to alleviate the increase in protein requirements which result from gastrointestinal nematode infection. Implications of these findings are discussed for the formulation of strategy for sustainable control of parasitic gastroenteritis in small ruminants using nutritional management technology as alternative control option.

KEY WORDS

Gastrointestinal nematodosis, ruminants, nutrition.

INTRODUCTION

Inadequate nutrition and gastrointestinal parasitism are the major factors responsible for reduced productivity of small ruminants. Subclinical helminthosis may cause decline of up to 40% in live weight gain,  6-30% in the food in-take of lambs (Poppi et al., 1990)., 40% in wool production and 15% in milk production in infested sheep (Sykes, 1982). Available feed resources are often low in quality, fibrous and deficient in components which promote efficient rumen function. Under-nutrition in energy, protein and minerals/trace elements has all been implicated directly or indirectly in predisposing the animals to parasitic infection. Because of severe impact of gastrointestinal nematodes on the productivity of animals much research has been concentrated on their control. Anthelmintic dosings have been the only option for effective helminth control in livestock over the last 50 years. However, sole reliance on drugs is currently being questioned especially with prevailing single and multi class resistance in parasites of many livestock species against anthelmintics throughout India and the World (Yadav et al.,1995). To overcome the problem of emergence of anthelmintic resistant among strains of parasites and to meet the consumers demand for animal products free of chemical residues considerable research efforts have been directed at alternative parasite control approaches like grazing management, nutritional management, biological control, genetic control and vaccination (Sanyal, 1998).

Nutritional management

The nutrition influences on the outcome of exposure of sheep to nematodes has been suspected for many years (Gibson, 1963). Recent interest to know the interaction between the nutritional status of the animal and parasitism is stimulated by the need to develop sustainable parasite control which is dependent on frequent anthelmintic interventions (Coop and Kyriazakis, 1999).

Effect of parasites on host

The interaction of parasites and nutritional status of animal is highly complex however, parasites derange the nutritional status of animals leading to an increased susceptibility to infection. The extent of metabolic impairment by a parasite is influenced predominantly by the level of larval challenge along with number and species of worms, which is established and further influenced by host factors such as age, nutritional, physiological and immune status of host. The patho-physiological responses of parasites in sheep which affect the nutritional status of animals are:
a) Reduction in feed intake: In parasitised animal the reduction in feed intake could be immunostimulatory or allow the host to become more selective in their diet (Kyriazakis et al., 1988). Depression of feed intake may primarily reflect the response to an imbalance of nutrients reaching to liver and peripheral tissues because of the priority sequestration of amino acids by gastrointestinal tract for its repair as well as for development and expression of local cell mediated response. On giving dietary choice to infected lambs, Kyriazakis et al. (1994) observed that lambs would select for higher protein diet. Further, rapid restoration of appetite following anthelmintic treatment suggests that nematode themselves may influence appetite directly through secretion of cytokine-like molecules (Kyriazakis et al., 1996). The reduction in nutrient availability to infested animal through both reductions in feed intake and/or reduction in efficiency of absorbed nutrients depend upon the species of parasites and its location in the GI tract. Sykes and Coop (1977) elucidated reduction in feed intake in lambs continuously challenged with abomasal worms (Ostertagia circumcincta) while Sykes et al. (1988) observed reduction in the efficiency of food utilisation in lambs continuously challenged with intestinal worms (Trichostrongylus colubriformis).
b) Decreased absorption rate in intestine: Intestinal parasites adversely affect the digestion and absorption of dietary nutrients and host metabolism which in turn, affect the host’s immune system and its ability to fight infection. The deficiency of specific amino acids could be due to reduction in net absorption of non-ammonia nitrogens (Coop et al., 1997), secretion of amino acid containing products in GI tract like higher secretion of threonine in intestinal mucus (Neutra and Forstner, 1987), leukotrienes rich in cysteine (Lewis and Austin, 1981) and incomplete reabsorption of these amino acids (Bang et al., 1990).
c) Increased protein requirement by host: In infested animals the protein deficiency occur via two process one leakage across damaged mucosa and two diversion of protein from production to enhance immune response against worms and repair of damaged epithelial tissue of intestine. Larvae and adult stages of nematodes in GI tract are responsible for damage and sloughing of epithelial cell layers, leakage of plasma and extra cellular fluids and increase in mucus production. There appears to be a direct competition between the immune system and other body tissues for nutrients. Withstanding parasite challenge, maintaining immunity and normal animal performance is directly related to a high protein intake. The nutritional cost is also directed towards maintaining the immune response to parasites involving local inflammatory responses, epithelial cell secretion and antibody productions (Sykes and Coop, 1993). The cell-mediated responses are likely to be protein demanding (Mac Rae, 1993) particularly sulphur containing amino acids. Together these, the need to repair damaged tissues, maintain blood or plasma homeostasis and mount an immune response have been shown to increase protein utilisation in splanchnic tissue by 40% (Yu et al., 2000) and reduce the amount of protein available for tissue growth and other functions. These losses in to the GIT can be substantial varying from 20-125 g protein/day in T. colubriformis infected sheep (Poppi et al., 1986) and in Haemonchus contortus infection they can represent as much as 10% of the circulating blood volume/day (Parkins and Holmes, 1989). Since these losses are proteinaceous in nature there is an increased cost of protein synthesis to maintain the tissue integrity and functions, which result in up to 50% reduction in growth for the same feed intake (Sykes and Coop, 1976). To maintain the body growth in infected animal, there is increase in protein requirement due to loss or diversion of endogenous nitrogen. In lambs infected with T. colubriformis the requirement of amino acids was found to be increased by 33% at the expense of peripheral tissues such as muscles (Yu et al., 1998). Thus, in totality GI nematodes decrease the livestock production by absorbing the host’s blood and food, damaging the GI tract, depressing the appetite, decreasing the digestion, reducing energy retention, increasing nitrogen losses, decreasing absorption of amino acids etc.

Nutritional manipulation to increase resistance / resilience to GIN

In ruminants resistance to both infective larvae and adult nematodes has been associated with the development of acquired immunity (Balic et al., 2000) and expressed by increasing host ability to reject incoming larvae, to depress worm fecundity and to expel adult worms.
Nutrition can have a major influence on the severity of parasitism and some influence on the extent of acquired immunity. Parasites drain the sheep of nutrients particularly iron, trace elements and protein. Sheep on a diet deficient of these nutrients or pregnant ewes whose feed intake has not kept up with increasing demands from the foetus will suffer diseases sooner than sheep fed adequately. Young growing animals are more susceptible to GI nematodes than adult animals and often can’t get enough protein from pasture. Animals in poor body condition have a poor immunity. Research has shown that increased dietary intake of metabolisable protein and energy and high quality pasture can directly promote the host resistance and host resilience to worm infection (Knox, 2000). Protein – energy deficiency is an important cause of defective T-cell function (Chandra, 1984) and T-cells have been shown to play pivotal role in mediating acquired resistance to haemonchosis in sheep (Gill et al., 1993). Increasing digestible protein intake appears to have little effect on acquisition of host resistance in the early stage of nematode infection. A number of studies indicated that protein supplementation appears to be most effective in enhancing particular immune response associated with latter stages in the acquisition of host resistance (van Houtert et al., 1995). Improving host resistance and / or resilience to infection through nutritional management can be one component in an integrated worm management approaches. The improved nutrition will always increase host resilience. In lambs acquisition of immunity has a greater priority than growth while in adult animal expression of immunity has lower priority than reproductive efforts. By nutritional management the increase in resistance/resilience to worms has been seen.
a) Decreased establishment of incoming larvae and reduction in worm number: Young sheep infected with black scour worms and given extra protein were found to have 45% less number of worms in small intestine compared to those of non-supplemented sheep. (Bown et al., 1991b). Further, up to 50% reduction in faecal egg count (FEC) and worm burden was observed following infusion of casein in abomasum of T. colubriformis infested sheep (Bown et al., 1991b). The rise (3-fold) in mast cell proteases activity in abomasum was found to associate with decreased establishment of larvae in sheep provided high protein supplementation (Coop et al., 1995).
b) Rejection of established worms: The parasite rejection can be antigenic in nature but may also involve processes such as mechanical or enzymatic damage inflicted by the host on larvae or adult parasites. The effect of supplementation on established worms was found to occur in later phase.    van Houtert et al. (1995) observed that after 10 weeks of infection with worms, protein supplemented sheep had the same number of worms as non-supplemented sheep, however by 15 weeks of infection the animals which received fish meal had fewer worms.
c) Reduction in faecal egg count: Supplementation with a protein rich concentrate like cotton seed meal, urea etc. have a major impact on the development of acquired immunity to GIN in young sheep. This could be either through an effect on the number of adult parasites in the gut or through suppression of egg output of individual worms (Shaw et al., 1995). Reduced FEC in animals offered high protein diet further helps in reducing the pasture contamination rate and subsequent re-infection. d) Increase in body weight/growth rate of animals: The animals maintained on high plane of nutrition had more live weight gain while under weight animals are less able to mount protective immunity. A strong negative correlation has been observed between initial live weight and T. colibriformis worm count after challenge in 8-month old Merino lambs. Lambs with an initial body weight less than 22 kg had higher FEC and worm count compared to those with over 22 Kg body weight (Mc Claure et al., 1999). A 60% increase in the protein content of diet found to increase growth rate by 50% and 20% in the energy content of sheep diet led to doubling of growth rate over a 10 week period in weaned Merino sheep infected with black scour worms (Khan et al., 2000). Similarly van Hutert et al. (1996) also observed increase in live weight gain on supplementation with protein or energy equivalent to that achieved by deworming.
e) Reduced severity of infection and drench frequency: Higher FEC and greater clinical severity of haemonchosis has been observed in sheep on low protein diet compared to high protein diet (Preston and Allonby, 1978). It has been demonstrated that lambs receiving 1.6% of body weight supplementation were able to ameliorate the influence of GI nematodes on performance and reduce the frequency of anthelmintics for worm control (Ginting, 1998). On provision of additional protein infested animals are able to maintain normal rate of growth suggesting that if protein supply is high enough than it may possible to keep animal performance in the face of larval challenge (Knox and Steel, 1996).

Interaction between parasites and host’s protein energy

Trichostrongylosis in sheep is found to reduce surface area of small intestine. The tiny finger like projections that help nutrient absorption in the intestine disappear resulting in malabsorption of nutrients. It has been estimated that around 100g protein/day got lost in sheep infected with black scour worms. Strain and Stear (2001) observed that lambs on diet with additional protein had shorter adult H. contortus and produce significantly more antiparasitic IgA. The IgA mediated suppression of worm growth and fecundity was assigned a major protective mechanism in sheep. The adverse effect of haemonchosis on production were minimised by feeding extra dietary protein to the infested animal (Datta et al., 1998). Lower FEC and higher Packed cell volume and growth rate was observed in H. contortus infested lambs supplemented with cotton seed cake as extra protein compared to those which were fed wheat bran (Amynalem et al., 2002). Supplementation particularly with high quality protein is often necessary to maintain the adequate productivity but high cost limits their widespread use. In such situation low cost technologies based on incorporation of by-pass protein are useful. A large number of experiments have demonstrated that animals supplemented with a source of by-pass protein have increased resistance and resilience to GIP. When livestock are grazed on low quality roughage the most critical nutritional deficiency is of nitrogen. Provision of non-protein nitrogen (NPN) such as urea in the diet can compensate for the deficiency and stimulate feed intake, enhance ruminal digestion, elevate ammonia-nitrogen level in rumen leading to increased ruminal microbial protein synthesis and availability to the intestine. Sheep on diet containing 3% urea gained more weight, consumed more feed and grow more wool of high fiber diameter than their counterparts given no urea (Knox and Steal, 1999). The in-vivo studies demonstrated that sheep with urea in their diet had lower FEC when infested with H. contortus and/or T. colubriformis, but there was no effect of urea on egg count of sheep infected with Trichostrongylus alone. In contrast, Trichostrongylus numbers on slaughter were reduced in sheep fed diet containing urea whereas H. contortus numbers were not affected.

Conclusion

i) In face of speedy increase in emergence of AR, sole and frequent use of anthelmintics is not a suitable option.
ii) Changing dietary components to prevent disease is not a new concept.
iii) The studies indicated that supplementation enhances resistance/resilience to GIN in sheep and may lessen the dependence on anthelmintics.
iv) Need to determine the quantity of nutrients that is beneficial in prevention v/s the quantity that can cause adverse effect.
v) Need to determine how best to incorporate nutrient recommendations for disease prevention in to existing nutrient requirement scheme.
vi) Need to determine cost effectiveness of nutritional input in worm management.
vii) In India the work on the role of nutrition in the management of parasitic diseases is yet to be initiated
viii) Sporadic studies in this aspect need to be systematized to translate them in fruitful technology .

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