The effect of parasitism on nutrient metabolism and productivity in small ruminants

O.O. Akinbamijo

Research output: Thesisinternal PhD, WU


<strong>INTRODUCTION</strong><p>The investigation of voluntary feed intake (VFI) and nitrogen retention (NRET) during parasitic infections in small ruminants is the central theme of this thesis. An attempt was made to examine the effects of trypanosomiasis on feed intake, digestibility, nitrogen retention and animal products. In addition, a similar investigation was conducted during a low to medium level fascioliasis infection in Menz sheep. The relationship between digestible organic matter intake (DOMI) rectal temperature (RT) and maintenance requirements was also studied in healthy goats.<p>The infected subjects manifested an aggregate of some distinct but not mutually exclusive responses. These include anorexia, fever, increased metabolic rate, lowered nitrogen retention and reduced animal productivity characterized by the host's poor growth rate and weight loss. Although the feed intake appears to be a major factor in the disease process, the observed derangements in productivity and physiological response to parasitic infection could not be fully explained by anorexia. Therefore, it seems that survival and the productive performance of infected animals depended on the adaptive measures they are able to employ to meet nitrogen and energy requirements during the periods of insufficient nutrient supply or inefficient feed utilization.<p><strong>PARASITIC INFECTION AND FEED UTILIZATION</strong><p>A depression in feed intake is a common feature in infected subjects, although the mechanisms involved remain unclear. Infection-induced anorexia is a major factor limiting the availability of energy for maintenance and production in parasitized hosts. This phenomenon has been widely reported in both human and animal subjects as one of the earliest signs of a patent infection (Ilemobade and Balogun, 1981; Symons, 1985; Keusch and Farthing, 1986; Holmes, 1987; Akinbamijo, 1988; Verstegen <em>et al</em> 1991; Zwart <em>et al</em> , 1991). Anorexia is an important aspect of parasitic infections, but studies using pair-feeding techniques have demonstrated that infected animals also show reduced feed utilization and energy retention relative to their parasite-free counterparts on the same level of feed intake (Sykes and Coop, 1976; Coop <em>et al</em> , 1982).<p>The onset of infection is characterized by the acute phase response during which anorexia, wasting of body tissues and changes in metabolism of carbohydrates, lipids and proteins occur (Baracos <em>et al</em> , 1987). Fever, a major factor in energy metabolism, is a conventional occurrence in haemo-protozoan infections such as trypanosomiasis (Holmes, 1987; Akker, 1988; Zwart <em>et al</em> , 1991; Verstegen <em>et al</em> , 1991) and malaria (Cohen and Lambert, 1982). This rise in body temperature implies an elevation of heat production caused by increased metabolic rates. Lower nitrogen retention has been reported in infected human and animal subjects during most nutrition-infection interactions (Beisel <em>et al</em> , 1987; Dargie <em>et al</em> , 1979; Morris, 1988). The reduced nitrogen balance observed in parasitized hosts is not only a consequence of the reduced feed intake (Symons, 1985): fever and the related increases in tissue catabolism (Baracos <em>et al</em> , 1987), intestinal and renal protein losses (Ingh <em>et al</em> , 1976; Holmes, 1987), high urea and total proteins concentrations in the serum (Finco, 1989) and high urinary nitrogen excretion (Roseby, 1977; Akinbamijo, 1988) have all been implicated during parasitism.<p>The increased catabolism of proteins during the acute infection is reflected in the increased urea production and nitrogen excretion often seen in infected animals (Finco, 1989). These wasting events, culminating in lower/negative nitrogen retention reduce the productivity of infected animals.<p>During parasitic infections in which anorexia and fever occur concomitantly, lipolysis and ketogenesis are common features (Keusch, 1984). After the glycogen reserve has been exhausted, during the first few hours of anorexia, the fat depot is used as an interim measure to meet the body's energy requirements. High concentrations of free fatty acids and ketone bodies in body fluids are an indication of lipolysis and partly oxidation of lipids. They are at a later phase accompanied by protein mobilization, reflected in increased urea in the urine.<p>The energy deficit during infection boosts the rate of energy needs. Hence, the changes in the composition of the serum often observed during infection-induced anorexia are a reflection of the subnormal caloric intake (Blackburn <em>et al</em> , 1991; Keusch, 1984; Bruss, 1989). These physiological changes occurring in concert, with complementary effects on each other, result in a serious negative energy balance, accompanied by a cumulative depletion of body energy stores, precipitating a lowered or negative energy and nitrogen balances (Clowes <em>et al</em> , 1976; Beisel, 1985; Keusch and Farthing, 1986; Baracos <em>et al</em> , 1987; Blaxter, 1989).<p><strong>DIGESTIBILITY</strong><p>In view of their pathogenesis, it is often assumed that endo-parasitism must be associated with changes in the gastro-intestinal function (Holmes, 1987). However, parasitic infections do not normally seem to affect the digestive and/or absorptive capacity of the host, even when infection rates are high (Parkins <em>et al</em> , 1973; Roseby, 1977; Reveron and Topps, 1970; Reveron <em>et al</em> , 1974). Similar findings have been reported in sheep infected with <em>Fasciola hepatica</em> (Hawkins and Morris, 1978) and in calves infected with lungworms (Verstegen <em>et al</em> , 1989). Holmes (1987) suggested that the digestion and absorption <em>of</em> amino-acids might decrease as a result <em>of</em> endogenous protein draining into the gut <em>of</em> parasitized animals, but this is not a usual event in helminthiasis. In general, it is not impaired digestion and absorption but rather the increased metabolic demands on the hosts that are the important causes of the low productivity of parasitized hosts (Baracos <em>et al</em> , 1987).<p><strong>INFLUENCE OF PARASITISM ON PRODUCTION</strong><p>The net effect of infection on productivity is mediated primarily via a reduction in the energy available for productive purposes. Thus, changes in live body weight are a common yardstick for judging the effects of parasitism on animal productivity. It is generally acknowledged that diseased animals lose or gain weight more slowly than their non-infected counterparts. The low weight gains and differences in the productive capacity in bovine (Schillhorn van Veen, 1974; Kroonen <em>et al</em> , 1986) and ovine (Roseby, 1970; Hawkins and Morris, 1978; Tekelye <em>et al</em> , 1992 a&b) infections are primarily due to reduced voluntary feed intake. In addition to changes in the body weight, alterations in body composition do occur and this can have major implications for productivity. It is well established that under nutrition can cause changes in body composition of healthy red deer (Wolkers, 1993). In sheep, parasitic infection is found to have the same effects (Sykes and Coop, 1976, 1977).<p>The shortfall in energy required for productivity has a direct quantitative effect on animal products during infection. It has been demonstrated that milk yield and composition are affected during infection with trichostrongylosis (Bliss and Todd, 1976; 1977) and fascioliasis (Randell and Bradley, 1980). Both the quality and the quantity of wool have also been reported to be affected by infection (Bliss and Todd, 1977; Barger and Gibbs, 1981; Leyva <em>et al</em> , 1982).<p>Reproductive disorders in male and female humans and animals caused by Trypanosoma infection are widely reported in the literature (Ikede et al, 1988; Akpavie <em>et al</em> , 1987). The effects of infection have been demonstrated on conception rates and pregnancy in cattle (Ogwu and Nuru, 1981; Ogwu <em>et al</em> , 1986; Oakley <em>et al</em> , 1979) and sheep (Reynolds and Ekwuruke, 1988) leading to a lower reproductive index (RI) (Gabina, 1988).<p>Many of the major parasitic diseases such as trypanosomiasis, babesiosis, malaria and fascioliasis are characterized by anaemia. The decline in packed cell volume (PCV) during parasitic infections is often a confirmation that a disease process has set in. The aetiology of parasite-induced anaemia. is possibly the oldest and widely recognised clinical sign of a patent parasitic infection (Soulsby, 1976).<p><strong>OWN INVESTIGATIONS</strong><p>The derangement in host metabolism is the summation of a multitude of processes which leads to quantitative changes in animal productivity. It consists of the totality of all the modifications that make the difference between health and disease. The effect of a reduction in feed intake in healthy animals is considered first.<p>At lower levels of food intake, healthy subjects are able to attain energy balance partly by reducing energy expenditure and by mobilizing fat reserves for energy production indicating the use of non-protein energy sources to meet their energy requirements. As demonstrated (see Chapter 2), this was accomplished by the observed rapid fall in maintenance requirements accompanied by lowered body temperature during starvation or feed restriction. The physiological and/or behavioural strategies employed by energy-restricted subjects for survival are principally based on the reduction in energy expenditure. The findings presented in Chapter 3 indicate a positive correlation between body temperature and digestible organic matter intake (DOMI). This conserving process is a regular adaptive measure in healthy subjects during periods of caloric insufficiency. It concurs with the findings of Shetty (1990); Zwart <em>et</em><em>a/,</em> (1991) and Ketelaars and Tolkamp (1991). The implication is that feed-restricted animals utilize their nutrient resources more efficiently by reducing body temperature and maintenance requirements to a level proportionate to intake. Several such adaptive physiological responses tend to reduce the metabolic activity of tissues in order to improve the efficient use of resources. The animals are therefore able to maintain nitrogen and energy balance at intake levels reasonably lower than those of <em>ad libitum</em> fed animals (Chapter 2).<p>However, these findings are contrary to what has been reported as occuring during infection-induced fever, where metabolic rate is typically not proportionate to intake (Hayashi et <em>al,</em> 1985). Waterlow (1986) showed that the pattern of endogenous fuel substrate utilization differed significantly between healthy feedrestricted subjects and those with a restricted intake caused by an induced infection. Contrary to the depressed values found in <em>Trypanosoma vivax</em> infected goats, no deviation from normal levels was observed in the T3 and T4 concentrations in feedrestricted healthy goats (van Dam, Unpublished). This observation further strengthens the hypothesis that thyroid activity declines following infection with trypanosomiasis, suggesting that other mechanisms might be involved in the regulation of energy metabolism during infection.<p><strong>TRYPANOSOMIASIS</strong><p>As shown in Chapters 1, 2, 4, and 5 trypanosomiasis studied in different physiological stages of the West African Dwarf (WAD) goats and sheep produces varying responses to feed intake. On average, the infection-mediated anorexia observed in these experiments conforms with earlier findings observed during trypanosomiasis (Ilemobade and Balogun, 1981; Akinbamijo, 1988; Zwart, 1989). The decreased intake is mainly responsible for the negative nitrogen balance and reduced productivity.<p>No evidence of a haemorrhagic infection was found during trypanosomiasis in the research reported in this thesis. This observation, confirmed by absence of intestinal and kidney lesions at post-mortem examination, makes nitrogenous losses via intestines or kidneys unlikely (Ingh <em>et al</em> , 1976). In all the studies conducted, the digestive capacity was not affected by trypanosomiasis. The similar faecal nitrogen output obtained in infected and control animals nullifies the possibility of intestinal nitrogenous losses due to infection. The finding that there was no urinary protein agrees completely with post- mortem observations reported in Chapter 2 and no kidney lesions were found.<p>In the trypanosomiasis research reported in this thesis, the infection was always accompanied by fever. This is consistent with the fact that protozoal infections are often accompanied by fever which increases the energy expenditure of the infected host. This contention expressed by Baracos <em>et al</em> , (1987) and Cohen and Lambert (1982) was also supported by Verstegen <em>et al</em> , (199 1) who attributed a 25% increase in the maintenance requirement of <em>Trypanosoma vivax</em> infected goats to fever. In the present research, all infected animals became febrile from the onset of infection and maintained the pyrexia throughout the infection. Fever, increased basal metabolic rate (BMR) and heat production have been identified as factors contributing to increased energy demands characteristic of infected subjects (Keusch and Farthing, 1986).<p>This thesis indicates that the metabolic costs accompanying the infection (Baracos <em>et W</em> , 1987; Verstegen <em>et al</em> , 1991) and anorexia during trypanosomiasis led to increased lipolysis in the host animal. An increased concentration of serum non- esterified fatty acids (NEFA) was observed in infected subjects, confirming that body fat reserves were being used to bridge the energy gap due to anorexia and increased maintenance requirements (Chapter 1). The observed increase in blood urea concentration indicates that a minimal breakdown of body proteins cannot be excluded. This agrees with the findings of Beisel (1985). No evidence was found of increased ketogenesis or excessive breakdown of body proteins, even when feed intake was as low as 40% of maintenance requirements. However, two cases in which increased concentration of serum ketone bodies following extreme anorexia was observed (Chapter 2) deserve mention. A similar metabolic response was described by Symons (1985) and Beisel (1985) during severe starvation.<p>During the post-infection phase, anaemic and anorexic pregnant ewes tended to reduce rate of weight gain and body condition. These derangements during trypanosomiasis have been attributed to a number of factors: a reduction in dry matter intake (Akinbamijo <em>et al</em> , 1990), an increased basal metabolic rate (Zwart <em>et al</em> , 1991; Stephen 1986), an increased catabolism of tissue reserves (Akinbamijo <em>et al</em> , 1992) a reduced nitrogen and energy balance (Zwart <em>et al</em> , 1991; Verstegen <em>et al</em> , 1991) and possibly an uptake of host's nutrient by the parasites (Reynolds, Personal Communications). In the acute phase response and the related wasting physiological events that follow, the increased metabolic rate has severe implications for livestock productivity, such as dam mortality, foetal and neo-natal losses. These three factors attained prominence in earlier reviews on the effect of trypanosomiasis on reproduction (Ogwu and Nuru, 1981; Ogwu <em>et al</em> , 1986; Ikede <em>et al</em> , 1988) and in the findings of Elhassan (1987) and Reynolds and Ekwuruke (1988) in WAD sheep.<p>In the present research, infected ewes ending pregnancy with low maternal weights and depressed intake, had lambs with lower birth weights that suffered considerable neonatal mortality. Consequently, 85% of lambs from ewes infected at late pregnancy died within seven days after birth. The relation in non-infected ewes, between lamb birth weight and growth rate and maternal effects of pregnancy nutrition and dam weight at parturition are widely reported (Gibb and Treacher, 1980 & 1982, Pearl 1967, Treacher 1970, Adu and Olaloku, 1979). In the event of a severe nutritional stress, incidences of sporadic abortion have been reported (Osuagwuh and Akpokodje, 1986; Osuagwuh and Aire, 1990). Hence if dam and foetal nutrition is inadequate, it can induce results such as were obtained in infected ewes (Chapter 4). The maternal effects on the low lamb birth weights were reflected in the low weaning weights of the lambs from infected dams.<p>In spite of the infection, ewes infected after lambing had sufficient body reserves to meet the daily milk yield observed in all animals during early lactation. Lactation is often associated with an increase in feed intake (Blaxter, 1989), and this may have masked the effect of infection on intake and milk yield during early lactation in the infected dams (Chapter 5). In relation to the live weight pattern, it could be deduced that infected lactating sheep catabolized body reserves to supplement the dietary nutrients required for milk production as established by Gibb and Treacher (1982). Since milk yield did not differ during early lactation, the growth rate did not differ between lamb groups. The difference in milk yield observed during late lactation had no effect on lamb growth rate, as lambs had commenced the weaning process and were supplementing their milk intake with forage.<p><strong>FASCIOLIASIS</strong><p>As intended, the clinical observations of the low to medium level infection mimic those of the sub-clinical infection usually experienced by grazing stock. No evidence was found of changes in the feed intake and digestive capacity of the hosts post infection. This concurs with the finding of Hawkins and Morris (1978) obtained using graded levels of infection doses, that there is a negative relationship between fluke burden and digestibility coefficients. Considering the infection dose used in this thesis, the infection level was too low to initiate digestive disturbances. The costs of infection (inefficient feed utilization) were evident. This conforms with the reports of Berry and Dargie (1976) and Dargie <em>et al</em> , (1979).<p>The sub-clinical fascioliasis had no effect on the voluntary feed intake of open and pregnant Menz ewes. However, this finding conflicts with what occurs during parasitism, where anorexia is reported as one of the earliest symptoms (Berry and Dargie, 1976; Murray and Murray, 1979; Symons, 1985, Keusch and Farthing, 1986; Holmes, 1987; Morris 1988). The explanation of this finding can only be a conjecture: in our experiment, it is probably connected with factors such as breed and age of the host, the viability and number of metacercariae administered and the presence of an undetermined level of pre- infection immunity (Sinclair, 1971; Berry and Dargie, 1976; Leyva <em>et al</em> , 1982).<p>The digestive capacity of the ewes was found not to be affected by infection or pregnancy either. This conforms with most findings during parasitism (Dargie <em>et al</em> , 1979; Berry and Dargie, 1976) but contrasts with reports by Holmes (1987) who suggested the possibility of impaired digestive and absorptive processes especially due to loss of intestinal proteins into the gastro-intestinal tract during helminth infections. However, as already noted, in the present study, the similarity of the faecal nitrogen in infected and control animals invalidates the chances of such an occurrence.<p>Despite the low to medium level fascioliasis imposed on them, the infected Menz ewes indicated a decline in PCV about eight weeks post-infection. This is similar to the observations of Sinclair (1971) and Dow <em>et al</em> (1968). The decline in PCV post infection substantiated the presence of an infection effect in inoculated ewes.<p>At comparable levels of voluntary feed intake, infected ewes retained less nitrogen, gained less weight, and produced lighter lambs and had poorer body condition (Chapter 6). This is probably because of differences in the efficiency of utilization or conversion of feed into desired animal products. The difference in growth rate between infected and healthy goats (Chapter 1) illustrates the nutrient drain that accompanies the infection. Inefficient feed utilization and wasting of this type during parasitic infections is also widely reported in the literature quoted above. The nitrogen retention differed remarkably in the early part of the infection and gradually reverted as the infection progressed. An upturn in PCV observed towards the end of the study may also be related to the acquired resistance phenomenon suggested earlier by Sinclair (1971). The reduced nitrogen retention reported by Dargie <em>et al</em> (1979) at eight weeks post-infection, was principally due to high urinary nitrogen. In our study, the findings with respect to the time schedule, the lower nitrogen retention and high urinary nitrogen observed in the infected ewes, are similar to those reported by Dargie and his co-workers (1979). The observed similarity in feed intake and digestibility in control and infected ewes indicate that other insidious losses must have had a major effect on the overall nitrogen retention and lower rate of weight gain in infected ewes. This is largely borne out by the nitrogen balance and body weight data that put the infected sheep on the lower limit. Although our study provides no clues about the extra nitrogen excreted by infected ewes, its appearance in the urine rather than in faeces confirms the contention that the host's digestive and absorptive capacity was not impaired during the low to medium fascioliasis.<p>Live weight gain in the animals was also considerably affected in the infected animals. It has been reported that sheep infected with Fasciola hepatica failed to maintain the rate of body weight gain observed in uninfected counterparts (Reid <em>et al</em> , 1970; Holmes, 1987; Blackburn, 1991). Lamb birth weight was lower in infected ewes than the control ewes. The low nitrogen retention found in infected pregnant ewes strengthens the contention that there was less nitrogen accretion in the foetus. Such deleterious effects of parasitism on the productive potential and the efficient use of resources have been demonstrated earlier (Ogwu <em>et al</em> , 1986;lkede <em>et al</em> , 1988; Reynolds and Ekwuruke, 1988; Akinbamijo <em>et al</em> , 1994).<p><strong>IMPLICATIONS FOR ANIMAL PRODUCTIVITY</strong><p>In the studies with <em>Trypanosoma</em> and <em>Fasciola spp.</em> reported in this thesis, absence of digestive disturbances was clear but in neither case did infected animals utilize their food as well as non-parasitized controls. The onset of infection coincided with reduced nitrogen retention resulting from a combined effect of reduced voluntary feed intake and/or increased excretion of urinary nitrogen. As productivity is governed not only by the gross intake but also by the efficiency of conversion into desired products, the evidence obtained in this research suggests that the reduced productivity of parasitized animals is the direct result of infection depressing the utilization of feed intake.<p>In quantitative terms, less digested nitrogen was retained in the tissues or products of the infected animals. This is typified by the findings reported in the first chapter, where it was shown that trypanosomiasis was responsible for the low growth rate. No carcass analyses were conducted in this research, but other researchers have reported changes in body composition during undernutrition (Wolkers, 1993) and infection (Sykes and Coop, 1976). Both undernutrition and infection were observed in the present research (see Chapters 1 and 2).<p>Reproductive wastage generally traceable to infections is considered to be substantial during infection (Osuagwuh and Aire, 1990; Osuagwuh and Akpokoje, 1986). It is usually characterized by embryonic or foetal death, abortion, premature birth, still birth, birth of weak offspring and neonatal deaths (see Chapter 4). It seems rational that if the dam is in good body condition pre-partum, then the offspring will have a good chance of surviving. However, this is often not the case during parasitism. Depending on the severity of infection, if the nutritional stress becomes extreme, most or all of the conditions mentioned above will occur, and reproductive wastage will result. The degree of reproductive wastage is therefore related to the level of dam nutrition and parasite load. Considering the findings of lkede and Losos, (1972) in sheep and Ogwu <em>et al</em> , (1986) in cattle, the possibility of intra-uterine infection cannot be ruled out in this study.<p>At sub-clinical levels, infection resulted in an appreciable degree of poor nutrient utilization that may have serious consequences on productivity (Chapters 4 and 6). Infection of pregnant ewes was characterized by low nitrogen retention, poor weight gains, and poor body condition and foetal development culminating in low lamb birth weight. Even when the dam was treated post-partum, the carry-over effects from gestation were reflected in the lamb performance.<p>There were no profound effects of infection on lamb growth rates, but infected dams lost more weight at lactation and retained less nitrogen. In the context of livestock health and productivity, parasitism lowers the production potential or offtake of the infected animals. As observed from this thesis, elements of the productivity and reproductive indices mainly growth rate (or weight gain), ewe mortality, abortion ratelfoetal loss, birth weight, weaning weight, neonatal loss, nitrogen retention and body condition, and milk yield were appreciably affected by parasitism. Others which should have been included are weight of offspring weaned per dam, the number of lambs produced and number of lambs born per 100 ewes.<p>Concurrent with findings of Ogwu et a] (1986) in cattle, Elhassan, (1987) and Reynolds and Ekwuruke (1988) in sheep, abortion occurred in infected ewes during the third trimester. The effect of chronic clinical or sub-clinical trypanosomiasis on reproduction and fertility such as anoestrus, failure to conceive, poor libido have been reported by the authors cited above. These disorders have a direct bearing on the productivity index (PI) described by Bosman <em>et al</em> (1988) and the reproductive index (RI) described by Burfening <em>et al</em> (1993). According to the indices of productivity described by these workers, the incidence of parasitic diseases in small ruminant husbandry has a multiplier effect on productivity as the two indices (PI and RI) are direct determinants of prolificacy (Gabina, 1988). This implies that the factors affected by parasitism are the determinants of productivity and hence are responsible for the reduction in the expression of the genetic potential and the optimum offtake per livestock unit. As shown by this thesis, the consequences of infection do not stop at morbidity alone but also flow through to incidence of mortality (Anene <em>et al</em> , 1991). In general, the findings in this thesis corroborate the suggestion of Smith <em>et al</em> (1988) that the problem of tropical livestock is clearly not one of inadequate number of livestock units but of low productivity.<p>The pathogenesis and clinical observations recorded during this thesis are similar to those frequently seen on the field during natural challenges. The subclinical infection keeps the host in an apparently healthy state but the overall cost of infection on productivity is substantial. A sub-clinical infection is more important to productivity than clinical infection. The latter, when it occurs, is often easily recognized and treated, or death results. In sub-clinical infections, however, such as are present in some breeds with varying degrees of resistance, the effect on the productivity and economics of production can be very grave.<p>Based on the findings in this thesis, it can be concluded that feed- restricted healthy animals make physiological adjustments by reducing body temperature and maintenance requirements to compensate for the reduced voluntary feed intake. The body temperature in such subjects is also positively related to the digestible organic matter intake. However, the relationship between DOMI and NRET is not affected by infection or artificial feed restriction.<p>The VFI was lower in the acute phase of infection in open, pregnant and dry parasitized animals, leading to reduced NRET and productivity. However, this was not the case during a low to medium fascioliasis in adult ewes: in the latter, the digestive capacity was not affected. However, low NRET and productivity were observed in all cases of infection investigated.<br/>The infection of pregnant animals resulted in reproductive wastage and low productivity. Milk yield and composition of non-dairy sheep during trypanosomiasis did not after and hence have no effect on the lamb growth rate.<p><strong>FUTURE PROSPECT</strong><p>This research has demonstrated the importance of anorexia and the compensatory role of the accompanying lipolysis in parasitized animals. Nutrient wasting is found to be reinforced by the incidence of fever during trypanosomiasis. A prominent feature in trypanosomiasis, and fascioliasis is the reduced nitrogen retention caused by anorexia and/or increased losses of urinary nitrogen.<p>Future work should be directed at unveiling the strategies for feed intake during infection (trypanosomiasis) and the effect of higher levels of infection during fascioliasis. Additional research should be directed towards studies that will identify physiological responses associated with nitrogen metabolism during pathologic conditions.
Original languageEnglish
QualificationDoctor of Philosophy
Awarding Institution
  • Zwart, D., Promotor, External person
  • Wensing, T., Promotor, External person
Award date27 Sep 1994
Place of PublicationS.l.
Print ISBNs9789054852957
Publication statusPublished - 1994


  • veterinary science
  • ruminants
  • parasitoses
  • parasites
  • trypanosomiasis
  • feeds
  • nutritive value
  • animal nutrition

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