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The interaction between animal nutrition and parasites: Studies with experimental trypanosomiasis in sheep

E. Katunguka-Rwakishaya

Department of Veterinary Medicine, Makerere University
P.O. Box 7062, Kampala, Uganda

Abstract
Introduction
Materials and methods
Results
Discussion
References

Abstract

The present study investigated the role played by improved nutrition in the development of pathophysiological effects of trypanosomiasis in sheep given two levels of protein intake. It was observed that feed intake was not influenced by either the diet or infection. The intensities of parasitaemia as measured by the buffy coat method indicated that there was a tendency for the animals receiving the high protein diet to sustain more parasite numbers than those receiving the low protein diet. The infected animals on a high protein diet gained weight at the same rates as the uninfected controls. However, infected animals on low protein diet showed marked retardation of growth compared to the uninfected controls. Both groups of infected animals exhibited similar degrees of anaemia but following treatment, those on the high protein diet recovered much faster than those on the low protein diet. It was concluded that improved nutrition in form of higher protein intakes ameliorates the adverse effects of trypanosomiasis and also enhances the rate of recovery following chemotherapy.

Introduction

Parasites, particularly gastro-intestinal helminths and protozoa, are a major constraint to animal productivity throughout the world. In many tropical countries protozoan diseases are of major importance. One protozoan disease in particular, trypanosomiasis, is the single most important constraint to animal production in sub-Saharan Africa. It has been frequently suggested that the nutritional status of the host can influence the pathogenesis of parasitic infection and it is generally accepted that well-nourished animals withstand parasitism better than those that are less adequately fed (Whitlock 1949; Gibson 1963).

There have been numerous anecdotal accounts of the importance of host nutrition in the pathogenesis of trypanosomiasis in ruminants, although until very recently these have remained unsubstantiated. Thus, it has been frequently reported from the field that during the dry season trypanosomiasis becomes more severe when the quality and quantity of nutrition is particularly low. This has recently been investigated in The Gambia by offering supplementary feeding during the dry seasons to trypanosome-infected N'Dama cattle (Agyemang et al 1990; Little et al 1990). As a result of the supplementary feeding it was found that the severity of the disease, as judged by the degree of anaemia, was significantly reduced.

It is possible that diet may not only influence host resistance to either the initial infection or re-infection but may also affect the ability of the host to withstand the pathophysiological consequences of infection. Unfortunately, the few studies that have been conducted to examine these interactions in the past have often been unsatisfactory because of inadequate controls or poorly formulated diets. More recently attempts have been made to overcome these difficulties and a clearer picture of the interaction between host nutrition and the pathophysiological consequences of parasitic infections has started to emerge.

The present study was designed to investigate the influence of host nutrition on the pathogenesis of trypanosome infection in sheep.

Materials and methods

Experimental animals, feeding and housing

Male castrate lambs, aged six months, were purchased from a local hill farm in the west of Scotland. The basic diet consisted of a mixture of shredded sugar-beet pulp (SBP), barley siftings and a mineral/vitamin trace element mixture. Soya-bean meal (SBM) was added to the high protein (HP) diet only. The mean proximate analyses of the two diets are shown in Table 1.

Table 1. Mean proximate analyses and calculated metabolisable energy of the high protein (HP) and low protein (LP) experimental diets (g/kg DM).


Dietary composition

Diet

HP

LP

Dry matter (g/kg)

880

880

Crude protein

176

81

Crude fibre

169

192

Ether extract

5

4

Ash

77

80

Organic matter

923

920

ME (Mj/kg DM)

9.8

10.1

The lambs were housed in individual pens on a concrete floor and wood shavings were used as bedding. The daily allowance of 1 kg fresh matter (FM) was offered in two feeds at 0900 and 1600 h. The residue was collected the following morning and weighed to give the actual amount of feed consumed.

Five litres of water were offered each morning and the residue was recorded the following morning.

Chemical analyses of feed

Representative samples of the experimental diets were analysed periodically using standard procedures (MAFF et al 1981).

Experimental infection

The animals were infected with Trypanosoma congolense 1180 (GRVPS 57/6), a cloned derivative of an isolate made in Serengeti, Tanzania, as described by Nantulya et al (1984). The trypanosomes were obtained from irradiated mice during the first rising parasitaemia. Mice were bled by cardiac puncture and their blood was pooled. An estimate of parasitaemia was made on the pooled sample, which was then diluted with phosphate buffered saline (PBS) containing 1.5% glucose at pH 8.0 to give 1x105 trypanosomes in 3 ml of PBS. Each sheep received 3 ml of the inoculum via the jugular vein.

Parasitological, haematological and biochemical techniques

The techniques used to collect blood samples for parasitological, haematological and blood biochemical examination have been described previously (Katunguka-Rwakishaya et al 1992a).

In brief, trypanosomes were detected by the dark ground buffy coat method (Murray et al 1977), and the intensity of parasitaemia was graded from 0 to 5 as described by Paris et al (1982).

Experimental design

Eighteen Scottish Blackface lambs were involved in this study. They were divided into two groups of nine animals each, on the basis of their live weights and PCV, and introduced to either a low protein (LP) or a high protein (HP) diet. After 4 weeks on their respective diets, six animals from the low protein group (LPI group) and six animals from the high protein group (HPI) were infected with T. congolense, while three animals from each dietary group acted as uninfected controls (LPC and HPC).

Seventy days after infection (DAI), three animals from the HPI group (HPIT) and three animals from the LPI group (LPIT) were treated with isometamidium chloride, at a dose rate of 1 mg/kg by deep intramuscular injection, and the animals were monitored for a further 21 days.

Statistical methods

Comparisons between groups were achieved by using one-way analysis of variance followed by the Newman-Keuls multiple range test. Intensities of parasitaemia were evaluated by the non-parametric Mann-Whitney test. These statistics were performed using the Animal Designs 1 (Data International Service, Glasgow) and Minitab (Ryan, Penn State University) Programmes. P values <0.05 were considered significant.

Results

Feed and water intake

The mean feed intake for animals in the HPI group was 0.93±0.03 kg/d while the LPI group consumed 0.98±0.02 kg/d between 0 and 70 DAI. This difference was not statistically significant. Control animals consumed 1 kg/d. The mean water intake of the LPI group was 2.10±0.07 litres/d while HPI group consumed 2.51±0.10 litres/d (P<0.05). Mean water consumption in control groups was not different. The LPC group consumed 2.30±0.11 litres/d while HPI group consumed 2.31±0.10 litres/d.

Parasitaemia

The prepatent period in both groups was the same, i.e. 7-9 days after infection. Following patency, parasitaemia fluctuated considerably with a tendency to be higher in HPI than in LPI group (Figure 1).

Body weight

Infection was associated with greater retardation of growth in the LPI group compared to the LPC group (Figure 2). The gain in live weight of the LPI group was significantly lower than that of the LPC and HPI groups. However the HPI and HPC groups grew at similar rates. There were no significant differences between the weights of control animals.

Packed cell volume (PCV)

Infection caused significant decreases in PCV values of both infected groups compared with their controls (Figure 3). The decline in PCV values commenced with the appearance of trypanosomes in circulation and both groups of infected animals showed similar degrees of anaemia. The PCV values in control animals fluctuated between 0.32 and 0.40 litres/litre. There were no nutritional influences.

Mean corpuscular volume (MCV)

Following infection, both infected groups showed significant increases in MCV compared to their uninfected controls, however the increase was significantly greater in the HPI group than in LPI group. In the HPI group the mean MCV increased from 31.2±0.3 flat 0 DAI to 38.5±1.2 fl at 29 DAI. In the LPI group, the MCV values increased from 31.0±0.7 fl at 0 DAI to 35.0±0.6 flat 36 DAI before decreasing to 32.3±0.7 at 68 DAI.

In control groups the MCV fluctuated between 30.0±0.6 and 33.0±0.6 fl with no significant between LPC and HPC groups.

Figure 1. Parasitemia scores of sheep infected with T. congolense and given either a high (dotted line) or a low protein (continuous line).

Plasma albumin concentration

The mean plasma albumin concentration decreased significantly in both groups of infected sheep and also showed dietary influences. In the HPI group, plasma albumin decreased from 36.2±0.4 g/litre at 0 DAI to 28.7±0.9 g/litre at 21 DAI. In the LPI group, it decreased from 30.8±0.7 to 26.3±0.6 g/litre and tended to recover thereafter.

In the control groups, plasma albumin concentration fluctuated between 28.3 and 32.0 g/litre in the LPC and between 32.7 and 36.3 g/litre in the HPC group. The values in the HPC groups were significantly higher than those in the LPC group.

Response to treatment

Body weight. Following treatment both groups of infected animals gained weight. The LPIT group gained 0.7 kg while the HPIT group gained 1.8 kg during the 3 weeks after treatment. The LPC and HPC groups increased by 1.2 and 1.8 kg, respectively, in the same period.

Packed cell volume. Both groups of infected animals showed an improvement in their PCV values following treatment, however, the rate of recovery was moderately faster in the HPIT group. By 20 days after treatment the PCV values of the HPIT group were 0.33±0.01 litres/litre while those of the HPC group were 0.32±0.01 litres/litre. The values in the LPIT group were 0.28±0.01 while controls were 0.32±0.01 litres/litre.

Discussion

In the present study, it was shown that improved nutrition in the form of increased protein intake had a marked influence on rates of growth, intensity of parasitaemia, blood biochemical changes and rate of recovery from anaemia following administration of isometamidium chloride.

In agreement with the findings of Little et al (1990), it was observed that improved nutrition did not affect the prepatent periods. Following the appearance of trypanosomes in circulation, there was a tendency for parasitaemia to be higher in the HPI group. The reasons for this are not clear but may be due to readily available nutrients like proteins and lipids.

Figure 2. Body weights of sheep infected with T. congolense and given either a high (- -- -) or a low (- -- -) protein diet, and of their respective uninfected controls (--, --).

Figure 3. Packed cell volumes (PCV) of sheep infected with T. congolense and given either a high (--) or a low (--) protein diet, and of their respective uninfected controls (- -- -, - -- -).

Greater retardation of growth was observed in the LPI group while HPI and HPC groups grew at similar rates. These findings agree with those of Hecker et al (1991) for Djallonké sheep end those of Agyemang et al (1990) for N'Dama cattle exposed to natural fly challenge. Verstegen et al (1991) and Zwart et al (1991) observed that development of fever during a course of trypanosome infection is associated with increased heat production and increased metabolisable energy for maintenance. The consequence of this is that the proportion of feed that would be used for growth is reduced as it is metabolised to provide extra energy for maintenance. The animals on a low protein diet would suffer this effect much more than those on a high protein diet, and this may manifest in the form of greater retardation of growth than animals on HP diet.

Similar degrees of anaemia were recorded in two groups of infected animals. This observation is in agreement with that of Agyemang et al (1991) for N'Dama cattle. However, Little et al (1990) reported that the rate of development of anaemia in N'Dama cattle inoculated with T. congolense and supplemented with groundnut cake was slower than in unsupplemented cattle. In contrast to this report, the present study has shown that improved nutrition does not influence trypanosome establishment and the rate of development of anaemia. The anaemia in HPI was macrocytic while it was nomacytic in the LPI group. This finding suggests enhanced erythropoietic activity as a response to infection in the HPI group. This may be responsible for the observed faster recovery from anaemia in this group.

Infection caused significant hypoalbuminaemia in both dietary groups but it appeared greater in the LPI than in the HPI group. At the same time control animals on HP diet had significantly higher plasma albumin concentration than those on LP diet. It has been suggested that uptake of albumin-bound fatty acids and lipoproteins (Vickerman and Tetley 1979) and haemodilution (Katunguka-Rwakishaya et al 1992b) may account for the decrease in plasma albumin concentrations in trypanosome infected animals.

In conclusion, this study has shown that improvement of host nutrition is important in moderating the severity of pathophysiological effects of trypanosomiasis and also influences the rate of recovery from anaemia following chemotherapy.

References

Agyemang K., Dwinger R.H., Touray B.N., Jeannin P., Fofana D. and Grieve A.S. 1990. Effects of nutrition on degree of anaemia and liveweight changes in N'Dama cattle infected with trypanosomes. Livestock Production Science 26:39-51.

Gibson T.E. 1963. The influence of nutrition on the relationships between gastrointestrel parasites and their hosts. Proceedings of the Nutrition Society 22:15-20.

Hecker P.A., Coulibaly L., Rowlands G.S., Nagda S.M. and d'Ieteren G.D.M. 1991. Effect of plane of nutrition of trypanosome prevalence and mortality of Djallonké sheep exposed to high tsetse challenge. In: Proceedings of the 21st Meeting of International Scientific Council for Trypanosomiasis Research and Control (ISCTRC), Yamoussoukro, Côte d'Ivoire, 21-25 October 1991.

Katunguka-Rwakishaya E., Murray M. and Holmes P.H. 1992a. The pathophysiology of ovine trypanosomiasis: Haematological and blood biochemical changes. Veterinary Parasitology 45:17-32.

Katunguka-Rwakishaya E., Murray M. and Holmes P.H. 1992b. The pathophysiology of ovine trypanosomiasis: ferrokinetic and erythrocyte survival studies. Research in Veterinary Science 53:80-86.

Little D.A., Dwinger R.H., Clifford D.J., Grieve A.S., Kora S. and Bojang M.1990. Effect of nutritional level and body condition on susceptibility of N'Dama cattle to Trypanosoma congolense infection in The Gambia. Proceedings of the Nutrition Society 49:209A.

MAFF, DAFS and DANI (Ministry of Agriculture, Fisheries and Food, Department of Agriculture and Fisheries for Scotland and Department of Agriculture for Northern Ireland). 1981. The Analysis of Agricultural Materials. Technical Bulletin RB427. Her Majesty's Stationery Office, London, UK. 226 pp.

Murray M., Murray P.K. and McIntyre W.I.M. 1977. An improved parasitological technique for the diagnosis of African trypanosomiasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 71:325-326.

Nantulya V.M., Musoke A.J., Rurangirwa R.F. and Moloo A.K. 1984. Resistance of cattle to tsetse-transmitted challenge with Trypanosoma brucei or Trypanosoma congolense after spontaneous recovery from syringe-passaged infections. Infection and Immunity 43:735-738.

Paris J., Murray M. and McOdimba F.A. 1982. A comparative evaluation of the parasitological techniques currently available for the diagnosis of African trypanosomiasis in cattle. Acta Tropica 39:307-316.

Verstegen M.W.A., Zwart D., Van der Hel W., Brouwer B.O. and Wensing T. 1991. Effect of Trypanosoma vivax infection on energy and nitrogen metabolism of West African dwarf goats. Journal of Animal Science 69:1667-1677.

Vickerman K. and Tetley L. 1979. Biology and ultrastructure of trypanosomes in relation to pathogenesis. In: Losos G. and Chouinard A. (eds), Pathogenicity of Trypanosomes. IDRC (International Development Research Centre), Ottawa, Canada. pp. 23-31.

Whitlock J.H. 1949. The relationship of nutrition to the development of trichostrongylides. Cornell Veterinarian 39:146-182.

Zwart D., Brouwer B.O., Van den Hel W., van den Akker H.N. and Verstegen M.W.A. 1991. Effect of Trypanosoma vivax infections on body temperature, feed intake and metabolic rate of West African Dwarf goats. Journal of Animal Science 69:3780-3788.


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