The role of epidemiological knowledge and grazing management for helminth control in small ruminants.

There is no single requirement more crucial to the rational and sustainable control of helminth parasites in grazing animals than a comprehensive knowledge of the epidemiology of the parasite as it interacts with the host in a specific climatic, management and production environment. In its absence, anthelmintic treatment is either given suppressively, which provokes resistance, or therapeutically, which risks clinical disease and production losses. Sustainable parasite-control programmes require knowledge of seasonal larval availability, origin of larvae contributing to any peaks and climatic requirements for worm egg hatching, larval development and survival. Control measures based on this knowledge include strategic anthelmintic treatments and various forms of grazing management. While these measures can reduce the frequency of anthelmintic treatment required, their effect on selection for drench resistance is more problematical, unless they can be combined with other forms of control to reduce our current dependence on anthelmintics.

Prospects for integration of novel parasite control options into grazing systems.

Novel parasite control methods are considered under criteria of efficacy, cost, ease of implementation and sustainability, together with a subjective assessment of when they are likely to become available commercially. It is concluded that vaccines, genetically resistant hosts, biological control, anthelmintics directed against free-living stages, and grazing management will probably satisfy all of these criteria, but that most of these methods are at least 5-10 years away from commercial exploitation. The exception is grazing management, which can be used immediately and at low cost, to minimise current use of anthelmintics. Research is required to assess the possibility of control programs based on grazing management that avoid anthelmintic treatment altogether. Extension of such control programs, in a context of declining government enthusiasm for provision of agricultural extension services, may be their greatest barrier to widespread adoption.

The value of circulating eosinophil count as a selection criteria for resistance of sheep to trichostrongyle parasites.

In merino sheep bred for either increased or decreased resistance to Haemonchus contortus, faecal worm egg counts (FEC) were lower in the resistant line (6,831 vs 17,645 epg, P < 0.01), and circulating eosinophils (EOS) were higher, but not significantly so (3.40 x 10(4) ml(-1) vs 1.40 x 10(4) ml(-1), P = 0.1 1). Another flock was artificially infected with Trichostrongylus colubriformis and significant genetic variation was found in both FEC (heritability 0.40 +/- 0.11) and EOS (0.19 +/- 0.08). In a third flock comprising tropical sheep breeds, a natural challenge with T. colubriformis resulted in significant sire effects on FEC (heritability 0.20 +/- 0.10) but not EOS (heritability inestimable). We conclude that EOS offers no advantage over FEC as it selection criterion for resistance.

Dietary protein for young grazing sheep: interactions with gastrointestinal parasitism.

Effects of protein supplementation and of nematode control on production responses in young grazing sheep and on nematode population dynamics were assessed. Young Merino wether sheep (n = 270) were allocated to one of three supplementation (Su) treatments and one of three regimes of nematode control (drench, Dr) in a factorial design. Each of the nine treatments was replicated three times in a randomised complete block. Animals received no supplement (Su0) or were given supplements at a level equivalent to 200 g day-1, fed three times a week. The supplements contained 25% lucerne meal with either 75% sunflower meal (Su1) or 75% formaldehyde-treated sunflower meal (Su2). Nematode control regimes were: not drenched unless survival of individual animals was threatened (Dr0); drenched according to a strategic drenching programme (Dr1); treatment with a controlled-release albendazole capsule (Dr2). Infections with Haemonchus contortus were suppressed by use of closantel. Due to drought conditions and lack of pasture growth, lucerne hay was fed to all sheep from Week 14 onwards (350 g per head per day, fed twice a week). Supplementation reduced the need for 'survival drenching' in Dr0 sheep considerably. Live-weight gain was increased significantly by supplementation with Su1 or Su2 during the 36-week experiment. Undrenched animals given Su1 or Su2 tended to grow faster than unsupplemented animals in the Dr1 and Dr2 groups. Greasy wool production and fibre diameter were increased by supplementation and anthelmintic treatment. Faecal worm egg counts (FEC) in undrenched sheep were significantly lower for Su1 and Su2 sheep than for Su0 sheep. There were no effects of supplementation on FEC in Dr1 or Dr2 sheep. Worm burden was generally unaffected by supplementation, while the drenching treatments Dr1 and Dr2 reduced worm burden at Week 16 and to a lesser extent at Week 27. Trichostrongylus colubriformis was the predominant nematode species, with smaller numbers of Nematodirus spp., Trichostrongylus vitrinus, Trichostrongylus axei and Ostertagia circumcincta also present. It was concluded that supplementary feeding with protein meal substantially reduced production losses attributable to nematode infections in young grazing sheep. This appears to be due to an enhanced resilience of the host, rather than any major changes in development of protective immunity.

Maintenance of acquired immunity to Trichostrongylus colubriformis in Merino sheep that are losing weight.

The effect of loss of weight on maintenance of acquired immunity to Trichostrongylus colubriformis in Merino sheep was assessed in 2 experiments. Adult Merino sheep with previously acquired immunity to T colubriformis were housed in individual pens. Sheep were infected 3 times weekly with 2000 T colubriformis larvae. A diet based on chopped oaten and lucerne hay (experiment 1) or a pelleted diet based on lucerne hay and grain products (experiment 2), was offered in amounts to sustain a moderate gain in body weight, or was reduced step-wise to cause a loss in body weight. Worm egg counts were determined weekly. The reduction in feed on offer resulted in a mean weight loss of 4.0 kg over 9 weeks (experiment 1) or 4.8 kg over 7 weeks (experiment 2). Based on worm egg counts, there was no indication of a change in immunity to T colubriformis in either of the experiments. These results suggest that acquired immunity to T colubriformis in adult sheep that are exposed to infection is maintained during periods of moderate loss of weight associated with inadequate nutrition.

Anthelmintic resistance in nematode parasites of sheep: learning from the Australian experience.

In recent years the problem of anthelmintic resistance has become of major importance in sheep and goat flocks throughout the world. In Australia, concerted efforts were initiated in the mid 1980s to halt the increase in resistance by the development and promotion of regional worm control programmes. This article outlines the genesis of these programmes, the way in which they were promoted and successfully adopted by farmers, and the concerns for effective parasitic control of sheep and goat flocks in the future. The principles outlined should be applicable in other countries where anthelmintics are relied upon for the control of nematodes in livestock.

Worm control and anthelmintic resistance: adventures with a model.

There are three common questions asked of parasitologists about anthelmintic resistance. Does it matter? How do you prevent it? Can you help me (it's here!)? In short, the respective answers are yes, read on the read on. Elizabeth Barnes, Robert Dobson and Ian Barger examine these issues in the context of nematode parasite control in grazing sheep. With the aid of a model, they examine some important factors that influence drug resistance and how farm management decisions and worm genetics modify these factors. They also explore the likely impact of new technologies on drug resistance and how efficient they need to be to sustain good worm control.

Effects of dietary protein intake on responses of young sheep to infection with Trichostrongylus colubriformis.

The effects of protein supplementation and infection with Trichostrongylus colubriformis on production responses and immune function in young sheep and on nematode population dynamics were assessed. Eighty-four 3-month-old Merino wether sheep were housed in individual pens and fed ad libitum chopped oaten hay containing 0.5% urea, together with 50 g day-1 lucerne meal. Fish meal (FM) was given as a source of protected protein at 0, 50 or 100 g day-1 (FM0, FM50, FM100; from Days --28 to 140). From Days 1 to 140, 0 or 1000 T. colubriformis infective larvae were given on Mondays, Wednesdays and Fridays. Infected sheep were slaughtered after 35, 70, 105, or 140 days of infection. Live-weight gain was reduced significantly by infection with T. colubriformis in sheep given FM0, but not in sheep given FM50 or FM100. Greasy wool production and fibre diameter were increased by FM, whereas the effects of infection with T. colubriformis on wool measurements depended on the level of FM given. Worm egg concentrations in faeces were significantly lower for sheep given FM100 than for those given FM0 or FM50 during the last 28 days of infection. Similarly, the apparent rate of worm expulsion was considerably higher in sheep given FM than in those not given FM. The rate of expulsion of T. colubriformis correlated with levels of circulating eosinophils as well as with the concentration of intestinal sheep mast cell proteases. Levels of parasite-specific and non-specific circulating antibodies were either unaffected or reduced as a result of supplementation with FM, although lymphocyte stimulation in vitro in response to T. colubriformis third stage larval antigen was enhanced significantly in infected animals given FM100. It was concluded that supplementary feeding with FM substantially reduced the production losses attributable to infection with T. colubriformis and was associated with enhanced expulsion of the parasite burden.

Rotational grazing for control of gastrointestinal nematodes of goats in a wet tropical environment.

A preliminary experiment involving contamination of pasture plots with eggs of Haemonchus contortus, Trichostronglyus colubriformis and Oesophagostomum columbianum every month for a year established that in the tropical environment of the Pacific island of Tongatapu, hatching and development of all species was rapid and continuous, with a short survival on pasture (3-7 weeks) of the resulting infective larvae. These results indicated that a rotational grazing system consisting of ten paddocks grazed in sequence for 3.5 days at a time may permit a reduction in the frequency of anthelmintic treatment of goats. In comparison with an adjacent set-stocked flock which required treatment on three occasions during the year when mean flock egg counts exceeded 2000 eggs per gram (EPG), rotationally grazed goats generally maintained mean egg counts of less than 1000 EPG. Anthelmintic treatment was only given to rotationally grazed goats individually as they kidded, and there were indications that even this precaution was unnecessary. Because of the expense of frequent anthelmintic treatment and the resulting selection of strains of anthelmintic-resistant nematodes, rotational grazing of small ruminants through fencing, tethering or herding deserves further investigation as a nematode control option in wet tropical environments.

Influence of sex and reproductive status on susceptibility of ruminants to nematode parasitism.

Bulls and rams are notorious among stockmen and stud breeders for their apparently greater susceptibility than cows, ewes, steers or wethers to diseases caused by excessive infection with parasitic nematodes. Extension advice given to farmers generally includes a recommendation to treat entire male animals as though they were weaners. In contrast, the scientific literature contains little documentation of this fact, although the phenomenon has been well-described in laboratory animals. Scientific interest in the susceptibility of lactating cows and especially ewes to nematode parasitism has been more extensive, but unproductive in terms of elucidating responsible mechanisms. Where ewes have acquired immunity to nematode infection, they tend to lose it around the time of parturition and during lactation, with important epidemiological and productivity consequences. In strains of sheep selected for resistance to nematode infection, principally through a more rapidly acquired immune response, resistant ewes still undergo a periparturient loss of immunity but retain their relative superiority over unselected or susceptible ewes. The mechanisms involve effects of hormones associated with lactation on the immune system, but an unequivocal role for prolactin or any other hormone has not yet been identified. Collaboration between immunologists, endocrinologists and parasitologists is required.

Control of gastrointestinal nematodes in Australia in the 21st century.

Because the Australian livestock industries rely overwhelmingly on year-round grazing of pastures, nematode parasites are of major concern. Nematode parasitism is recognized as the cause of the most economically important diseases of sheep, while in cattle, the relative importance of nematode parasitism will probably increase following the eradication of diseases such as brucellosis and tuberculosis. The extraordinarily high prevalence of resistance to benzimidazoles, levamisole and morantel in nematodes parasitising sheep has stimulated the formulation and, to a surprisingly large extent, adoption by farmers of strategic control programmes aimed at preserving the useful life of ivermectin. Even so, it is highly likely that we will enter the 21st century with ivermectin resistance. Current research aimed at control in the next century is progressing in three broad directions. First, towards better control using existing anthelmintics through modifications to pharmacokinetics, together with integrated management aided by computer simulation models of nematode population biology. Secondly, towards immunological control arising from a better understanding of the ruminant immune response to helminths, particularly in young animals, and finally, a coordinated investigation of genetic resistance, within breeds, of sheep to nematode parasitism. The appearance in the 21st century of novel anthelmintic compounds, most probably as a result of research by the international pharmaceutical industry, may well reduce the sense of urgency driving current Australian research. Nevertheless, success in one or more of these three lines of endeavour will mean a longer and more profitable life for the next generation of anthelmintics marketed in Australia.

Effects of a controlled-release albendazole capsule on parasitism and production from grazing Merino ewes and lambs.

Effects of a controlled-release albendazole capsule (CRC) on nematode parasitism and production of Merino ewes and lambs were investigated in a replicated grazing experiment between August 1986 and July 1989. The experiment was conducted on a site where the naturally occurring parasites were benzimidazole-resistant, with double the recommended dose of oxfendazole reducing faecal egg counts of Trichostrongylus colubriformis by less than 50%. Two CRC treatments were compared with a minimal treatment control and the widely-used strategic control program, Wormkill. Egg counts and worm burdens of major parasite species of ewes and of lambs before and after weaning were significantly reduced by use of the CRC in ewes before lambing or in lambs at weaning. These parasitological effects were reflected in increased productivity of CRC ewes and lambs. Ewes given CRCs lost less weight and grew more wool during lactation than ewes given Wormkill or control treatments, while their lambs gained more weight and had heavier fleeces than lambs from Wormkill or control treatments. Where lambs were weaned by removing ewes from the lambing paddock, administration of the CRC at weaning to lambs whose dams had also been treated with the CRC did not result in improved production when compared with lambs from ewes dosed with CRCs and treated after weaning according to the Wormkill program. Some possible uses for the CRC in ewes and lambs were identified.

Parasitological and immunological responses of genetically resistant Merino sheep on pastures contaminated with parasitic nematodes.

One hundred and twenty lambs were grazed continuously from weaning until 9 months of age on 12 plots contaminated with larvae of three nematode species (Haemonchus contortus, Trichostrongylus colubriformis and Ostertagia circumcincta). The lambs were sired by either a genetically resistant ram or susceptible rams (determined by the response of previous progeny to artificial H. contortus infection). Half the resistant and half the susceptible lambs were given strategic anthelmintic treatment and the remainder remained untreated. Faecal egg counts and blood packed cell volume were measured frequently in all animals. One and 5 months after weaning, two lambs from each plot were slaughtered, and worm burdens and larval establishment rates of the three species of nematode were estimated. At the second slaughter, leukotriene levels and larval migration inhibitory (LMI) activity were measured in mucus collected from the small intestine. The dominant species in all faecal samples and the gastrointestinal tract was T. colubriformis. Lambs of the resistant genotype had lower faecal worm egg counts, lower worm burdens and higher levels of resistance to larval establishment. There were no differences in larval migration inhibition (LMI) activity, but resistant lambs had higher levels of the leukotriene LTC4/D4/E4. Further, the resistant genotype, identified on responsiveness to artificial infections with H. contortus, was more resistant to infections of three important species acquired naturally from contaminated pastures. All these genetic differences were maintained while the lambs were subject to strategic anthelmintic treatment.

No adaptation of Haemonchus contortus to genetically resistant sheep.

A composite population of Haemonchus contortus was established with larvae from seven diverse sources, then maintained in Merino sheep bred to have either increased or decreased resistance to Haemonchus. After five, seven and 14 parasite generations, the two resulting lines of parasites were used to infect sheep from the increased resistance line, an unselected control line and the decreased resistance line. Line of sheep had a highly significant effect on average faecal egg counts 4 and 5 weeks after infection (geometric means 329, 735 and 1490 epg, respectively after the 14th generation), but the two lines of parasites yielded similar egg counts. There was no significant interaction between line of sheep and line of parasite, indicating that the parasite populations had not diverged significantly in their reproductive fitness, as measured by faecal egg count.

Response to helminth infection of sheep selected for resistance to Haemonchus contortus.

Lines of Merino sheep selected for increased (IRH) and decreased (DRH) resistance to Haemonchus contortus were compared with an unselected (CH) line, after approximately four generations of selection. Measurements were recorded on 69 IRH, 47 DRH and 84 CH animals. Following artificial challenge with H. contortus, the IRH line had significantly (P less than 0.001) lower faecal egg counts than the CH and DRH lines (2730, 12,720 and 17,400 epg, respectively). Significant differences (P less than 0.05) were found between all lines in the minimum packed cell volumes during artificial infection (25.7, 22.0 and 20.3%) and in faecal egg counts after natural infection (140, 3590 and 8750 epg). Differences were also recorded (P less than 0.05) following artificial challenge with Trichostrongylus colubriformis (490, 840 and 1340 epg). On a percentage basis, faecal egg counts in the IRH line deviated less from the CH line following artificial infection with T. colubriformis (42%) than with H. contortus (79%). The reverse was true for the DRH line (60 and 37%, respectively). Differences in egg output of this magnitude should have a marked effect on requirements for anthelmintic treatment, rate of development of drug resistance and level of pasture contamination when the lines are grazed separately.

Development and survival of infective larvae of Haemonchus contortus and Trichostrongylus colubriformis on pasture in a tropical environment.

A trial to determine the seasonal pattern of egg hatching and larval survival on pasture was carried out in representative wet and dry zones of Fiji. Fourteen plots were established on parasite-free pasture at each of two sites. One plot at each site was contaminated every month with faeces from naturally infected goats containing a known proportion of Haemonchus contortus and Trichostrongylus colubriformis eggs. Pasture was sampled at regular intervals after contamination and infective larvae identified and counted. Larvae of both species developed throughout the year in the wet zone but development was more sporadic in the dry zone. Larval counts generally declined to below detectable levels within 9 weeks of contamination between September and March but longevity increased during the cooler weather from April to August. The comparatively short larval survival times noted in this experiment may present opportunities for manipulation of parasite population dynamics in the wet tropics.

Genetic resistance of hosts and its influence on epidemiology.

Evidence for the genetic control of resistance of sheep to gastrointestinal nematode infections was reviewed and compared with that of cattle to infestation with the cattle tick. Variation within sheep breeds in resistance to nematode infection is as great as that between breeds, is moderately heritable, and selection of lines of resistant sheep should result in animals carrying worm burdens around 10%-20% of those of unselected animals. The consequences of genetically resistant sheep for the epidemiology of Trichostrongylus colubriformis infection were examined with the aid of a simulation model. Predicted results were similar to those observed in cattle herds resistant to Boophilus microplus; seasonal peaks in parasite burdens were greatly reduced, and larval numbers on pasture were reduced even further. The use of genetically resistant hosts should permit a reduced frequency of anthelmintic treatment, and hence reduce the rate of development of anthelmintic resistance in the parasite.