Endoparasites

World census data for the last 5 years show that for every small ruminant there were 0.76 cattle, and the most recent data, for the year 2000, suggest that for every sheep there were 0.67 goats (FAOSTAT, 2000). Given the variety of agroclimatic zones used in the production of small ruminants, it is hardly surprising that there are a range of different genera implicated in nematodoses; however, economically, the most important genera are Haemonchus, Teladorsagia (Ostertagia), Trichostrongylus, Nematodirus, Cooperia and Oesophagostomum. In animals that are not compromised nutritionally, disease attributable to these nematodes is generally restricted to young stock during their first grazing season or occasionally in second grazing season animals. Although non-reproducing adult sheep on an adequate plane of nutrition generally express an effective acquired immunity, the acquisition and expression of acquired immunity against gastrointestinal nematodes appears to be much more limited in goats (Le Jambre and Royal, 1976; Jallow et al, 1994; Huntley et al, 1995). In many intensive small ruminant production systems, chemoprophylactic control of gastrointestinal nematodoses is rarely attempted using prescriptive regimes of the type described for calves (McKellar, 1994). Small ruminant chemoprophylaxis is generally used to limit the extent of challenge from pasture in order to maintain the productivity and welfare of susceptible stock.

Epidemiological factors influencing treatment strategies

An understanding of the epidemiology of the various nematode species implicated in disease in small ruminants is a crucial prerequisite for anthelmintic control strategies. However, since anthelmintic strategies are required to cope with regional differences in production systems, climate and prevailing parasite species, they inevitably need to be site specific. However, there are some common strategic and epidemiological elements that influence treatment regimes. The principal strategies used in sheep and goat production systems are either to administer treatments during 'epidemiologically' sensitive periods when they are intended to have the greatest effect in reducing pasture contamination, or to use anthelmintics suppressively, within the pre-patent period of the target species, or at frequent intervals to achieve the same effect. Unfortunately, treatments administered suppressively and at these 'epidemiologically' sensitive periods may also select most strongly for anthelmintic resistance, since they both confer considerable advantage to worms carrying the resistance genes.

Temperate production systems

In many temperate production systems in both hemispheres, sheep and goat breeding is seasonal, which usually results in relatively repeatable patterns of pasture contamination and challenge. In those systems where rainfall is non-seasonal or has a summer prevalence, large numbers of infective larvae become available on pasture from mid-summer onwards, usually reaching peak numbers in autumn/early winter. In more arid regions and under drought conditions, these suprapopulation peaks may be shifted towards the wetter periods, often the autumn and/or winter months. In temperate production systems, pasture larval populations tend to decline over the winter months, when temperatures do not suit the development and translation of larvae, and usually reach their minimum values during spring.

Much small ruminant production is also carried on in the Mediterranean climatic zones of the northern hemisphere and in the corresponding climatic zones of southern Australia and southern South Africa. Here, winters are mild and wet, and followed by a reliably hot, dry summer, during which pastures become effectively sterile as far as free-living stages of nematode parasites are concerned. Following the first rains in autumn, eggs passed by adult worms surviving the summer in their hosts are able to hatch and develop to infective larvae, with numbers of infective larvae usually reaching their seasonal peak in late winter or early spring.

There are two main sources of infection for newly born sheep and goats, which are epidemiologically sensitive targets for anthelmintic treatments. The first source of infection derives from eggs and larvae that have survived overwinter on pasture, and the second source of infection derives from contamination deposited during the ewe or doe periparturient relaxation in immunity (PPRI). In fat lamb production systems, early season treatments are aimed at reducing contamination and delaying the incrementation of the pasture larval population. The periparturient increase in faecal egg count derives from an increase in fecundity of established worms, the maturation of previously inhibited populations and an increased susceptibility to new infection (Armour, 1980). It is now an almost universal practice in temperate production systems to include one or more periparturient ewe or doe treatments in order to minimize the epidemiological contribution made by peri-parturient animals, particularly for economically important species such as Teladorsagia (Ostertagia), Trichostrongylus and Haemonchus. Flushing (pre-tupping) treatments are administered routinely to adult females and rams mostly for therapeutic rather than prophylactic reasons, and serve to bring the animals into peak condition prior to mating.

The ewe appears to play a lesser or negligible role compared with the pasture in the epidemiology of some nematodes. In species of nematodes where this is true, the overwintered suprapopulation serves to transmit infection to newly born animals. Nematodirus battus provides an extreme example of an intergenerational lamb to lamb transmitted disease. In those countries where this species poses a problem, early season (spring) treatments are given to young stock to minimize the risk to the grazing animal and the infectivity of those pastures in the subsequent grazing season. For those temperate climate species where the ewe plays a lesser role in contaminating pastures, intragenerational transmission is important in generating the challenge that leads to disease. In permanently stocked fat lamb production systems, routine chemoprophylaxis is used to minimize the risks from intragenerational transmission and enable lambs to achieve target weights in the shortest possible time. The contribution made by young stock to pasture contamination is influenced by the number of parasite generations that contribute to intragenerational transmission and the minimum generation interval, which varies from species to species. In fat lamb production systems in temperate areas, where genera with relatively short minimum generation intervals such as Teladorsagia, Haemonchus and Trichostrongylus tend to predominate, acquired immunity generally restricts the number of generations that can occur during the grazing season (Waller and Thomas, 1978).

Although the patterns of infection and disease are essentially similar in temperate extensive and intensive production systems, treatments are often administered in the former systems whenever animals are gathered for routine management, that is at lambing, tail docking, weaning and mating.

Tropical/subtropical production systems

In many tropical/subtropical production systems, the population dynamics of the principal parasites and diseases attributable to them may be driven by environmental factors which affect the development, translation and longevity of the suprapopulation. Under these circumstances and particularly in those areas/systems where significant rainfall only occurs on occasions, disease and treatment patterns are often linked to seasonal rainfall patterns. In those production systems where seasonal droughts are a routine occurrence, then hypobiotic larvae and persistent adult stages provide an epidemiologically sensitive target and treatments may be administered at the onset of rainfall or during the middle of the dry season. Treatments administered at these times may be highly selective as far as anthelmintic resistance is concerned since they may 'screen' virtually the entire parasite population. As a consequence of their exposure to intense periodic challenge, indigenous ruminant breeds often display a superior ability to regulate their parasite populations even under the relatively poor nutritional environment that these systems often provide.

In those tropical/subtropical production systems where rainfall is not a limiting factor, ruminants are produced against a background of high continuous challenge and it is difficult to identify specific epidemiologically sensitive treatment times. Intensive large-scale production systems in these areas have often resorted to the use of suppressive (treatment frequency within the pre-patent period) or neo-suppressive (treatment frequency close to the pre-patent period) regimes which have resulted in high levels of anthelmintic resistance. Small-scale producers in many tropical and subtropical regions generally use anthelmintics for therapeutic rather than prophylactic purposes.

One possible consolation to small ruminant producers in wet tropical areas is the fact that, although egg hatching and larval development is rapid and continuous throughout the year, the resulting infective larvae on pasture have a very short life expectancy. Studies in Fiji and Tonga (Banks et al., 1990; Barger et al., 1994) showed that infective larvae of Haemonchus, Trichostrongylus and Oesophagostomum survived for only 3-7 weeks under these conditions, which contrasts strongly with their survival for at least as many months in temperate regions. This short survival of infective larvae can be exploited by simple rotational grazing or tethered or herding husbandry systems that can obviate the need for most and perhaps all anthelmintic treatment.

Persistent efficacy

The persistent efficacy of moxidectin, which varies from 2 to 5 weeks depending on species, formulation and regulatory requirements, gives it a special role in control of haemonchosis (Kerboeuf et al., 1995). Persistent efficacy against H. contortus is always at the upper end of the range, and the ability thus to prevent Haemonchus egg output for several weeks at times of the year when these eggs would otherwise hatch and contribute to pasture infectivity greatly simplifies control of this species. Even longer persistent activity against all susceptible species has been obtained for ivermectin through its incorporation into a controlled-release capsule that lodges in the rumen and releases ivermectin (0.02-0.04 mg kg-1 day-1 for 100 days) over an extended period (Rehbein et al., 2000a). The delivery rate of the ivermectin controlled-release capsules is 0.8 mg ivermectin day-1 for sheep 20-40 kg in weight and 1.6 mg day-1 for sheep weighing 41-80 kg. Hence, on a per kg liveweight basis, the daily dose is 0.02-0.04 mg. Ivermectin controlled-release capsules have been used by sheep producers in Australia and New Zealand as the extended activity offers the opportunity to use treated sheep to prepare clean pastures. Both forms of persistent MLs (moxidectin, and ivermectin capsules) are also used typically in particularly susceptible animals, such as lambing ewes or young animals at weaning (Taylor et al., 1997) or as an alternative to frequent treatment during outbreaks of helminthosis when clean pastures are not available.

Coats

In young goats, the acquisition of immunity is more protracted and the maximum expression of immunity generally occurs during their second grazing season (Vlassoff et al., 1999). The limited capacity of goats to acquire and express immunity against gastrointestinal nematodes has made the treatment of all age classes a common practice in goats used in intensive production systems where they are obliged to graze rather than browse. Intensively grazing goats has been an important factor in accounting for the relatively high incidence and prevalence of anthelmintic resistance in goats.

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