Abstract:
Nutrition and Helminthosis in Sheep HUGH McL. GORDON* SUMMARY 1. The inter-relationships between nutrition and helminthosis are discussed and ten general principles are stated. 2. The principles are illustrated by the results of experimental work, chiefly with grazing animals. 3. Perhaps the most important principle is the necessity to differentiate between resistance to the establishment of an infestation and resistance to the effects of the established infestation. 4. Recent experiments with Trichostrongylus colubriformis show that a high plane of nutrition does not necessarily prevent the establishment of the infestation, but may mitigate its effects. 5. The precise reasons why sheep on well-established sown pastures often harbour light worm burdens, even though run at a high rate of stocking, remain to be determined. Some of the factors which may be involved are discussed. INTRODUCTION The inter-relationships between the nutrition of the sheep and its resistance to helminthosis provide an attractive field for basic studies on the mechanism of resistance; they are a challenge in animal production; and their implications are an inescapable part of preventive veterinary medicine. Worm infestations adverselv affect the intake and utilisation of food; therefore, special attention to nutrition and management is required to counter their ill-effects. Recent reviews have been made by Hunter (1953), Chandler (1953) and Frye (1955). GENERAL PRINCIPLES On the basis of present knowledge the following principles relating to helminthosis may be enumerated:1. The adequately fed host is more resistant than thte poorly fed host to most parasitic diseases. 2. The size of the worm burden depends on repeated acquisitions of infective forms, usually with ingested food; therefore, the amount, availability and nature of the food directlv affect the size of worm burdens and, indirectly, the nutritional needs of the host constitute the factor that influences thve balance between health and disease. 3. The nature of the food may affect the parasites by altering their environment in the alimentary tract. 4. The infestation may upset the nutritional status of the host, e.g. by decreasing appetite. 5. Resistance to the establishment of an infestation and resistance to the erects must be differentiated. 6. The effects of the parasite on the host range from a reduced productivity and performance, to death. 7. Gastro-intestinal nematodes of the grazing sheep interfere with the nutrition of their host. The biological state of parasitism is thus opposed to economy in production. *' Division of Animal Health, C.S.I.R.O., McMaster Animal Health Laboratory, Sydney, N.S.W. 8. There is a general relationship between the state of nutrition and the development and persistence of resistance; since the maniffestation of immunity are manifold, a wide variety of responses occurs among grazing animals which experience secular and individual fluctuations in nutrition and exposure to infective material. 9. Helminths vary greatly in their habitats and habits; their effects on the host and the host' effects on them are diverse. s 10. The manifestations of health and productivity are relative rather than absolute and they are variable; the responses to disease control measures and to better nutrition and the inter-relationships of these two factors are correspondingly difficult to measure precisely. EXPERIMENTS AND EXAMPLES (i) General Resistance and Production of Antibodies. Some results from a trial with Trichostrongylus colubriformis are shown in Table I. The sheep on the high plane of nutrition developed infestations, some of them heavy, but most were thrown off in less than 50 days, and the remainder did not persist longer than two months (except No. 377). The infestations in the low plane group were heavier, and persisted in the survivors for at least 128 days when a challenge dose of larvae was given; four of the IO sheep died subsequently. There were antibody reactions in the high plane sheep, but practically none in the low plane sheep. The infestations established in the high plane sheep were of economic significance as shown in Table II. TABLE II. Although the sheep had thrown off the greater part of their infestation in less than 50 days, as indicated by egg counts declining to less than 500 e.p.g., weight gains were much less than those of the controls even at 90 days. (ii) Indirect Effects. Grazing time, the size of the area grazed, closeness of grazing and the nature of the pasture plants may influence the intake of larvae. Fig. 1 shows the worm egg counts for groups of 45 sheep grazed on natural pasture and provided with a supplemlentary ration. The ration of oaten chaff two parts, cracked maize four parts, meat meal two parts, was provided in bulk at three levels of 4oz., 802. and 160~. per head per day. The sheep were finewool Merino weaners which weighed 401b., and for which 160~. of the mixture would provide almost a full maintenance ration. When infestations with Haemonthus contortus were acquired from August onwards they were hfeavier in the controls than in the group fed 402. of the supplement, and the lightest infestations were in the groups given 802. and 160~. It might be concluded that thfe higher plane of nutrition in the two latter groups conferred resistance to infestation but other evidence suggests the following alternative explanation. In the region concerned, increasing ;inPestations with H. contortus in the spring coincide with a rising plane of nutrition and increasing weight gains. It is possible that the difference between the controls and the 402. 94 group on the one hand, and the better fed groups on the other, was indirectly due to less time spent grazing; the direct cause would be a lower intake of larvae due to the requiremTent for pasture being reduced bv the supplementary feeding. White and Cushnie (1952) recorded lower worm egg counts in grazing lambs provided with a daily supplfement of llb. of oats and linseed-cake meal. Again it is possible that lambs given the supplement needed less pasture, and by spending less time in grazing acquired fewer parasites. Reduction in grazing time by cows given concentrates was reported by Hardison et al. (1956)) Brumby (1956) and Chambers (1959). Selective grazing may also influence indirectly the acquisition of infective larvae. The aioidance by cattle and ` horses of herbage close to faeces is well known (Taylor, 1954) ; the very selective grazing by sheep and calves may be similarly directed. In studies on the acquisition of infective larvae bv sheep by examination of ruminal contents, Whitlock (1959, unpublished data) found wide differences between animals grazing the same pasture; one sheep consistently acquired very few larvae although its fellows picked up large numbers. It was probable that this individual was extremely selective, and avoided, probably fortuitously, aggregations of larvae. Taylor (1944) found four times as many larvae on grass as on the same weight of sainfoin and concluded that the difference was due to the fact that the large topped sainfoin plant has less contact with the ground. The larvae were confined to the under side of the lower leaves of the grass but they readily climbed the smooth petiole 96 of clover plants and reached the leaf. A residue of larvae persisted longer on grass, where they were protected, than on clover, but a greater proportion of recently matured larvae was accessible to animals grazing on clover. Vegors et al. (1955) found heavier infestations with more severe clinical effects in cattle which grazed fescue pasture than in those which grazed a temporary pasture of rye grass, oats and crimson clover and that infective larvae persisted longer in fescue pasture than in other types. Goldberg (1959) fed cattle in pens on forage harvested from pastures and administered infective larvae to them; he found that there were only slight differences in worm burdens and clinical symptoms, irrespective of whether the cattle were fed on fescue hav, lucerne hay, or on fresh fescue and a fresh legumegrass mixture. The results of these trials suggest that the indirect factors relating to the nature of the herbage rather than any direct nutritional factor, influenced the establishment of an infestation. Taylor (1952) described a farm in England where there was very intensive stocking with sheep, but the worm burdens were light. It wa.s suggested that the absence of parasitic disease may have been due to: I. Early exposure of lam.bs to infestation which stimulated early development of resistance. 2. Removal and destruction of most of the infective larvae by close grazing of adult sheep which reduced the numbers available for lambs. 3. Destruction by desiccation of the eggs and larvae on the bare pastures. However, Gibson (1956) investigated the hazards of parasitic disease under similar intensive grazing and found that there may be considerable risks depending on climatic conditions and management, and that heavy infestations developed in lambs in spite of a high plane of nutrition. (iii) Effect of Food on Parasites. The worms in the alimentary canal are apparently well protected against changes in the nature of the contents, otherwise their existance would be precarious. However, one of the consequences of domestication has been a great alteration in diet, which may present a very abnormal environment to the parasite. Spindler et al. (1944) and Spindler and Zimmerman (1944) found that when pigs were restricted to a diet of milk or milk products, their infestations with Ascaris suis soon disappeared and reinfestation did not readily occur. Porter (1935) found that rats fed exclusively on milk were less resistant to infestation and reinfestation with Nippostrongylus muris than rats fed on an adequate grain mixture. In suckling lambs heavy infestations with H. contortus, Ostertagia spp. and ,Trichostrongylus spp. can be readily established, so the milk diet does not appear to be inimical to these parasites. When sheep graze a green oat crop most of the Oesophagostomum columbianum are passed within a few weeks, but H. contortus and Trichostrongylus spp. are not affected (Gordon, 1948, Southcott, 1955). Subsequent observations by Whitlock (unpublished data) showed that Trichuris ovis is also' adversely affected by this diet, but to a less extent than Oe. columbianum, and that the passing of worms was associated with a lowering in the pH of the faeces. Diarrhoea is often accompanied by the passing of parasites of the large bowel but, experimentally, purgation does not remove many of the worms and it is considered that the effects of grazing oats are not due to purgation. In Western Australia it has been noted in a number of field trials that worm burdens, especially of Chabertia ovina, are thrown off after the seasonal flush growth of herbage in 97 the autumn, especially when cape weed (Cryptostemma calendulacea) is abundant. This may be analogous to the effects of grazing oats on Oe. columbianum. Further evidence that grazing oats has little effect on Trichostrongylus spp. was provided in a field trial at the McMasCer Field Station. A flock of 28 young sheep was exposed to natural infestations from birth. When 8 months old they were divided into two groups, one to remain on natural pastures, the other to graze a crop of green oats. Worm egg counts were then 100 to 2,300 e.p.g. (Trichostrongylus spp.) and did not change materially during the stures gained next six weeks in either group. The sheep on natural pa' 4.81b. per head; those grazing oats gained 14.31b. After six weeks all of the sheep were dosed with 50000 T. colubriformis larvae. In the next six weeks the oats group gained 5.71b., and the natural pasture group gained 0.21b. per head. Reduced gains were probably due to the effects of the resulting infestations which were as follows: Oats group-heavy infestation in 6 of 13 (46%), light in 3 (23%), nil in 4 (31%): Pasture group -heavy in 9 of 15 (60%), light in 3 @OS), nil It was concluded that exposure to natural infestations for the first eight months of life, sufficient to produce egg counts of Trichostrongylus spp. as great as 2300 e.p.g., was not sufficient to stimulate immunity in about 45 to 60 per cent. of the sheep. After grazing on an oat crop which produced a gain of 14.31b. per head in six weeks, 69 per cent. of that group were still susceptible to the establishment of infestation. Tetley (1953) obtained some evidence that the high hydrocyanic acid content of white clover in New Zealand may be inimical to the development of H. contortus. Heath and Park (1953) found that substance' extracts from clover (Trifolium repens) contained a ' which inhibited cholinesterase. The organic phosphorus compounds used as anthelmintics are anticholinesterases and so it is possible that an exclusive clover diet might be inimical to the parasites also due to this activity. Some of the metabolic changes which occur in sheep transferred to lush spring growth of pasture have been described by Annison et al. (1959a, b) who recorded changes in a wide range of substances found in blood and rumen contents. The effects persisted for some of the substances, e.g. volatile fatty acids, for at least three weeks. It will be of interest to examine the effects of such changes on worm parasites. ( i v ) Interaction between the Effects of Infestation and Nutritional Status. LOSS of appetite occasioned by an infestation (Gordon, 1950, 1958) may be accentuated by a specific dietary deficiency, e.g. cobalt. Even without a spvecific deficiency the consequences of reduced food intake superimposed on a generally poor ration are serious. On the other hand it is conceivable that correction of a dietary deficiency with restored or increased appetite might lead to increased intake of infective larvae. Threlkeld et al. (1956) found that the ability of H. contortus larvae to establish themselves in sheep in pens appears to be dependent on the presence of cobalt in the diet, and of the sheep which died as a result of the infestation those fed on the basal ration plus cobalt died sooner, but made better weight gains prior to death than those fed on the basal ration. Shumard et al. (1956) found that sheep on pasture given a lick containing Cu, Co, Mn, Fe, I and NaCl were more severely affected by infestations with H. contortus. Fraser et al. (1936) found a correlation between the worm burden in mixed infestations with H. contortus, Ostertagia spp. and T. axei 98 and the liveweight increase of grazing sheep. They suggested that the lambs that thrive best eat more grass and, consequently, ingest more larvae. The worm counts in the lambs were very low (118 to 1050) and one would not have expected them to influence weight gains adversely. Nevertheless, this is a further example of a complex relationship between nutrition and worm infestation. Todd and Hansen (1951) found that progressive weight gains accompanied increasing numbers of Ascaridia galli in chickens and drew the rather novel conclusion that energy used by the chickens in resisting infestations prevented maximum weight gains-the chickens which harboured the fewest worms having used the most energy. Infestations with T. colubriformis reduce the digestibility of proteins, and the utilisation of calcium and phosphorus. (For results of work at McMaster Laboratory and references to earlier work, see Franklin et al. 1956). Recently at the McMaster Laboratory Symons (unpublished data) showed that in rats infested with Nippostrongylus muris only 36 per cent. of protein in a test meal was digested; controls digested 60 per cent. (v) Resistance to the Establishment of an Infestation and Resistance to the Effects of an Infestation. This differentiation is essential to the understanding of the effect of nutrition on immunity, but is not always clearly stated. Th e adequately fed animal can withstand the effects of established infestation better than a poorly fed animal, especially those infestations which cause direct disturb&es in nutrition, e.g. loss of appetite; reduced digestibility and absorption of nutrients; or diarrhoea. When the main pathogenic effect is anaemia due to blood-sucking worms, generallv less benefit is likely to accrue from providing a better plane of nutrition, ` sheep in prime condition may die from haemonchosis. e.g. The influence of diet on the establishment and on the effects of an infestation are shown in Table I. The initial infestations established in sheep fed on the two diets did not differ greatly as judged by the egg counts on the 24th day, but the subsequent behaviour of the infestations showed clearly that the high plane of nutrition prevented mortality and reduced the intensity and duration of the disease. The sheep were given a challenge dose of larvae 128 days after their initial dose. Those on the better ration resisted the establishment of the challenge dose whereas those in the low plane developed heavy infestations. Under field conditions it is difficult to separate the influence of nutrition on the establishment and on the effects of an infestation, and it is probable that the state of affairs noted by Stewart and Gordon (1953) is common. They stated, ' The opinion, based on field observations, that nutrition is of prime importance in the resistance of sheep to T. colubriformis possibly overlooks other factors concerned. It might well bee that when good nutritive conditions prevail, the development of larvae is also favoured, whereas when poor nutritive conditions prevail, relatively few infective larvae are available to the sheep; sheep which ingest few larvae during their early life have less opportunity to develop an immunity than those which ingest more larvae under more favourable conditions' . It is essential to attempt a differentiation of these effects because an infestation acquired when nutrition is adequate may not become clinically manifest until nutritional conditions have deteriorated. Further, an infestation may be of epidemiological and economic significance even though it is not producing clinical symptoms. (vi) Relative Effects of an Infestation. A light infestation has epidemiological significance, a moderate infestation is of economic consequence and a heavy infestation may be fatal. High productivity is very vulnerable to parasitic disease. . Some of the penalties of parasitic disease in sheep have been illustrated by Gordon (1958). Table 3 provides further examples with fat lambs. In the earlier stages worm burdens were light and the lambs gained rapidly at 0.41b. per head daily for the first month. In the second month. weight gains were much less, especially in the controls. In the third month weight gains improved and there were only small differences between the groups. There were, however, greater differences between the groups when a comparison was made of the proportion of lambs reaching 801b. or over. The difference between drenched and control groups was greatest in the fourth pneriod. Readiness for market is an important considerati .on in fat lamb production and a delay of one or two weeks might be critical. (vii) Antithesis between Parasitic Disease and Pr*oductive Efficiency. The examples above show that helminthosis reduces the productivity of the host, but it must be emphasised that nutritional disturbances are among the earliest effects of the parasite and add to the costs of feeding and management. Even when it has not been possible to measure a difference in the digestibility of nutrients between control and infested animals, there has often been a clear indication that infested sheep utilised their food less effectively and required more feed per unit of liveweight gain than worm-free controls (Andrews, 1938, for Cooperia curticei, and Andrews et al. 1944 for T. colubriformis). Boughton (1955) wrote a provocative paper on 'Care and Feeding of Livestock Parasites' in which the somewhat facetious , title serves to emphasise the waste of feed occasioned by worm infestation. (viii) Variations in the Response to Infestation. In a field trial with fat lambs this ' stratification' and the in, fluence on it of monthly drenching with phenothiazine were recorded (Table IV.). TABLE IV. Percentage of lambs which gained different amounts of weight. Lambs born in September, from Border Leicester x Merino ewes by Dorset Horn rams. Weight gains from December to April. Controls Phenothiazine' monthly :: 0 to 101b. 40 4 II to 201b. 37.5 47 211b. or more 22.5 49 Forty per cent. of the lambs remained unthrifty during the first six months of life, and 22.5 per cent. gained weight rapidly and steadily. The small proportion of lambs which gained less than 1Olb. in the phenothiazine group shows the beneficial influence of a reduction of the worm infestation. Amo n g the manifestations of immunity and resistance to worm P #arasites are : 1. Prolonged pre-patent period, i.e. the time from the acquisition of infestation to the appearance of eggs in the faeces. 101 2. Reduction, and even inhibition of egg production. 3. Reduced length of life of the parasite. 4. Self-cure-the abrupt loss of an infestation, commonly precipitated by the intake of infective larvae, sometimes followed by resistance (usually in trichostrongylosis), sometimes by a new infestation (often in haemonchosis). Under field conditions, where all of these manifestations may appear, it is difficult to assess the precise effects of any particular regime of nutrition or management on the resistance of grazing animals. This should not be taken as a deterrent to further observations but as a stimulas for more precise observations. (ix) The Variety of Helminth Parasites. Even among the worms which inhabit the gastro-intestinal tract there are wide differences in feteding and metabolic activities, pathogenic effects and immune responses engendered in the host. In the field mixed infestations are the rule but commonly one or two species predominate, and the different species have different, but overlapping, seasonal occurrences. The consequences are the different manifestations of worm infestation and the different responses to control measures which occur from time to time and from flock to flock and even between flocks on the same property; e.g. haemonchosis affects sheep of all ages, whereas trichostrongylosis affects only the young animals. The bloodsucking parasites such as Haemonchus spp. and the hookworms provide an example of a specialised feeding habit. A similar typ*e of anaemia can be produced by bleeding. Blood loss, whether due to deliberate bleeding or to blood-sucking by the worms, depletes the body of iron. If the diet is poor in iron the effects of the parasites are Ienhanced, and it has been found in hookworm disease of man and the dog that supplements of iron may alleviate symptoms while the parasites are still present (Rhoads et al. 1944, Foster and Landsberg, 1934). In experiments at the MeMaster Laboratory with haemonchosis in sheep when the diet was not deficient in iron, the addition of a supplement of ` iron did not influence the course of the anaemia or hasten recovery after removal of worms. (x) Measurement of Responses. The reactions of the host to its different species of parasites vary considerably. Accordingly the responses of thle host to control measures will also vary, depending on the parasite concerned, on the efficacy of anthelmintics and on supporting measures such as better nutrition. Unthriftiness is relative. A slow rate of growth might be tolerated in a Merino, but even a slight check to growth rate in a fat lamb mav make its production uneconomic. In a given environment a certain growth rate or wool yield may have been accepted because it was usual, and until the conditions of husbandry (nutrition, disease control) were changed there were no criteria of *comparison. In observations on the growth and productivity of the Merino in New England, N.S.W., weaners on natural pastures gained only 41b. from May to September and cut 21b. wool. Similar weaners fed in pens gained 121b. and produced 4.51b. wool, but remained highly susceptible to infestation with worm parasites. In trials at Cressy Farm in Tasmania, Corriedale lambs gained 441b. in 90 days but were still susceptible to worm infestation. In trials at Oberon with fat lambs in which worm burdens were not heavy, 41 per cent. of the control lambs reached 801b. or more by the time they were six months old, but 60 per cent. of the lambs treated monthly with anthelmintics achieved this weight in the same time. Spedding (1955) in England has produced abundant evidence on the effects of sub-clinical infestations ` growth and production. on 102 These examples show some of the difficulties in measuring the interactions between host and parasite and especially in assessing their relative importance in animal production. REFERENCES Andrews, J. S. (1938). J. Agric. Res. 57: 349. Andrews, J. S., Kaufmann, W., and Davis, R. E. (1944). Amer. J. Vet. Res. 5: 22. Annison, E. F., Lewis D., and Lindsay, D. B. (1959a). J. Agric. Sci. 53: 34. Annison, E. F., Lewis, D., and Lindsay, D. B. (1959b). J. Agric. Sci. 53: 42. Boughton, D. C. (1955). N. Amer. Vet. 36: 26. Brumby, P. (1955). Proc. N.Z. Grassl. Ass. 17: 96. Chambers, D. T. (1959). J. Agric. Sci. 53: 417. Chandler, A. C. (1953). J. Egypt. Med. Ass. 36: 533. Foster, A. O., and Landsberg, J. W. (1934). Amer. J. Hyg. 20: 259. Franklin, M. C., Gordon, H. McL., and Macgregor, C. H. (1946). J. Coun. Sci. Industr. Res. Aust. 19: 46. Fraser, A. H. 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Spindler, L. A., and Zimmerman, H. E. (1944). Proc. Helm. Sot. Wash. 11: 49. Spindler, L. A., Zimmerman, H. E., and Hill, C. H. (1944). Proc. Helm. Sot. Wash. 11: 9. Stewart, D. F., and Gordon, H. McL. (1953). Aust. J. Agric. Res. 4: 340. Taylor, E. L. (1944). In ' Alternate Husbandry' Jt. Publ. Commonw. , Agric. Bur. No. 6. Taylor, E. L. (1952). Publ. Brit. Vet. Ass. No. 23: 112. Taylor, E. L. (1954). Brit. J. Anim. Behav. 2: 61. Tetley, J. H. (1953). Nature, Lond. 171: 311. Threlkeld, W. L., Price, N. O., and Linkous, W. N. (1956). Amer. J. Vet. Res. 17: 246. Todd, A. C., and Hansen, M. F. (1951). Amer. J. Vet. Res. 12: 58. Vegors, H. H., Sell, 0. E., Baird, D. M., and Stewart, T. B. (1955). J. Anim. Sci. 14: 256. White, E. G., and Cushnie, G. H. (1952). Brit. J. Nutr. 6: 376. DISCUSSION L. Williams (N.S.W.) .-How long before the dose of larvae was given were the sheep on different levels of nutrition ? Physiological response to changed nutritional regime could be inter-related with response to infestation. Answer.-Six weeks before they were given the infestation. W. Stephens (Tas.). -Wha t is the effect of Bephenium and which species was involved? Answer. -There was a high proportion of Nematodirus spp. and Bephenium probably killed many immature Nematodirus as well as some other species. Question.-Has there been an upsurge of lungworms in recent years ? Answer.-Apparently there has been an increase in incidence of lungworm infestation over the last few years, probably related to climatic conditions. Virus pneumonia is a factor complicating diagnosis. N. Tulloh (Vie.). -In sheep over 80 lbs. liveweight how did the worm population compare at slaughter in the drenched and undrenched sheep ? Answer.-No information is available from this trial; but the significance of the worm burden depends largely on when worm counts are made, e.g. numbers in various groups may be similar at the end of a trial which lasts some months; but there may have been big differences earlier in the trial. The effects of the parasites are related to the duration of the infestation, as well as the number of worms.