K. Bairden

How hosts control worms

Nematodes are a major cause of disease and death in humans, domestic animals and wildlife. Understanding why some individuals suffer severely whereas others exposed to the same infection remain healthy may assist in the development of rational and sustainable strategies to control infection. Here, using a quantitative genetic analysis of the parasitic nematode population that had accumulated naturally in lambs, we find no apparent influence of host genetics on nematode numbers but an extremely strong influence on average worm length and fecundity. Our results indicate that in growing lambs the main manifestation of genetic resistance is the control of worm fecundity.

The processes influencing the distribution of parasitic nematodes among naturally infected lambs

The impact of mixed, nematode infection upon a group of animals will depend upon the number of nematodes present, how they are distributed among hosts and whether individuals that are heavily parasitized with one species are more likely to be heavily parasitized with other species. A survey of over 500 six-month-old, Scottish Blackface lambs from a single farm in Southwest Strathclyde identified 7 different categories of nematodes in the abomasum and small intestine. There were considerable differences among years and among nematodes in the prevalence and mean intensity of infection. Ostertagia circumcincta was present in nearly all lambs and judged by prevalence and intensity is one of the most successful of all parasitic nematodes. Each category of nematodes had a skewed distribution; most animals had relatively few worms but a small proportion had many worms. The variance of the number of nematodes in each category were approximately equal to the square of the mean. The counts of adult O. circumcincta followed a negative binomial distribution, but the negative binomial distribution did not provide a good description of the observed values for the other species. These other species had a lower prevalence and possibly some sheep were not exposed to infection. There was no significant genetic variation among lambs in the number of nematodes present and therefore the differences among these lambs were unlikely to be a consequence of genetic differences in host susceptibility. Lambs with increased numbers of one species were more likely to be have increased numbers of the other species, but the correlations were weak and may reflect covariation in exposure to different parasites.

The genetic basis of resistance to Ostertagia circumcincta in lambs

The relationship between Ostertagia (Teladorsagia) circumcincta and sheep is one of the best understood host-parasite relationships in any species. The key components of resistance have been quantified, the extent of genetic control has been established for lambs, and methods now exist to breed lambs which will be both more resistant to worms and more productive than unselected lambs. A major gene for resistance has been identified within or around the major histocompatibility complex, and this gene appears to be the strongest yet identified for resistance to any parasite species. The most important mechanisms of resistance are local IgA responses which regulate worm fecundity and immediate hypersensitivity responses which regulate worm burdens. IgA responses develop before effective immediate hypersensitivity responses. Good simulation models now exist to predict, for example, outbreaks of disease and the response of sheep to selection. The challenge now is to use our improved understanding of the population biology to develop even better simulation models and to produce expert systems based on these models which can be used by veterinarians and others to determine optimal procedures for individual farms to control disease and reduce sub-clinical economic losses.

Influence of supplementation with dietary soyabean meal on resistance to haemonchosis in Hampshire Down lambs

The influence of dietary protein supplementation on resistance to haemonchosis was examined in Hampshire down lambs fed either a basal diet or a diet supplemented with soyabean. At seven months of age the lambs were challenged with an initial loading dose of Haemonchus contortus, followed by a trickle infection three times a week. Blood and faecal samples were collected three times a week and bodyweights were recorded weekly. After 10 weeks the lambs were slaughtered and their worm burdens and carcase composition determined. Although their mean worm burdens were similar, the lambs given the basal diet had higher faecal egg counts, lower packed red cell volumes and lower concentrations of total plasma protein and plasma albumin than the lambs given the supplemented diet. The dietary supplementation also improved the carcase composition of the lambs.

Influence of soyabean meal supplementation on the resistance of Scottish Blackface lambs to haemonchosis

Protein supplementation improves the resistance of sheep to haemonchosis. This experiment investigated the Scottish blackface breed to establish whether dietary protein supplementation is still beneficial in a genetically resistant breed. Lambs were given either a basal diet or a diet supplemented with soyabean meal to give an additional 80 g crude protein kg dry matter-1. The lambs were given an initial loading dose of Haemonchus contortus, followed by a trickle infection for 10 weeks. The weight gains of the lambs given the supplemented diet were greater and their carcases were leaner, irrespective of infection status. Infected animals on the basal diet were more anaemic and hypoalbuminaemic than animals receiving the supplemented diet, although there were no statistically significant differences in mean worm burdens or faecal egg counts.

The distribution of faecal nematode egg counts in Scottish Blackface lambs following natural, predominantly Ostertagia circumcincta infection

Faecal samples were taken in 2 consecutive years from Scottish Blackface lambs on a commercial farm in central Scotland to examine variation among lambs in the number of nematode eggs in their faeces. Samples were taken at intervals of 4 weeks from 1 to 5 months of age. Lambs were treated with a broad-spectrum anthelmintic at each sample date. Ewes and lambs were naturally infected by grazing pasture contaminated with mixed, predominantly Ostertagia circumcincta, nematode species. The ewes were removed from the lambs when the lambs were three months old. Only 3 of the 6 sets of samples taken prior to removal of the ewes fitted a negative binomial distribution but all sets of samples taken after this did so. The mean and the variance differed with the month and year of sampling. The amount of variation among lambs increased as the lambs grew from 3 to 5 months of age, possibly because of heterogeneity in the rate of development of protective responses. Counts taken in August and September, when the lambs were 4 and 5 months of age, were positively correlated with each other. In contrast, counts taken at 1 or 2 months of age were negatively correlated with counts taken when the lambs were 3-5 months old. Sex, date of birth, sire and dam were all associated with variation in faecal egg counts but the size and significance of their influence was dependent upon the date when faecal samples were taken. Four factors: sire, dam, sex and year accounted for over two-thirds of the variation among older lambs in faecal egg counts.

Local and plasma antibody responses to the parasitic larval stages of the abomasal nematode Ostertagia circumcincta

Ovine isotype-specific antibody responses to the parasitic larval stages of the abomasal nematode Ostertagia circumcincta were measured in a simple, indirect enzyme-linked immunosorbent assay. Analysis of variance of replicate tests showed that the assay was very reliable. There was substantial variation among individual sheep in their IgA and IgG1 responses even though the sheep had been matched for breed, age and sex, were born on the same farm, were reared identically and had the same history of exposure and challenge with O. circumcincta. The local IgA responses to a somatic extract of fourth-stage larvae were very similar to responses to excretory-secretory products of fourth-stage larvae. The responses to third stage larvae were correlated with the responses to fourth stage larvae. There was a negative correlation between parasite-specific plasma IgG1 and parasite-specific plasma IgA responses. There was only a moderate association between IgA responses in the mucus and the plasma. Therefore, antibody responses measured in plasma cannot be easily extrapolated to antibody responses in the abomasal mucus.

An ovine lymphocyte antigen is associated with reduced faecal egg counts in four-month-old lambs following natural, predominantly Ostertagia circumcincta infection

Ovine lymphocyte antigen is associated with reduced faecal egg counts in 4-month-old lambs following natural, predominantly Ostertagia circumcincta infection. International Journal for Parasitology 26: 423-428. Ten lymphocyte antigens were defined in a flock of Scottish Blackface sheep known to be naturally exposed to infection with Ostertagia circumcincta. Population and family studies suggested that the 10 antigens were products of class I loci. Antigen G13br was in linkage disequilibrium with allele g2 at the DRB1 locus. The g2 allele has previously been associated with reduced faecal egg counts in a different crop of lambs from the same farm. In this study antigen G13br was also associated with a reduction in faecal egg counts. The results provide partial confirmation of the role of the major histocompatibility complex in resistance to natural, predominantly O. circumcincta infection.

The relationship between IgA activity against 4th-stage larvae and density-dependent effects on the number of 4th-stage larvae of Teladorsagia circumcincta in naturally infected sheep

The number of Teladorsagia circumcincta 4th-stage larvae in naturally infected lambs from a single farm varied among lambs and among different years. Within each year the distribution of 4th-stage larvae among lambs was similar to that expected from a negative binomial distribution. The ratio of 4th-stage larvae to adult T. circumcincta was low in two years with a low mean intensity of infection but high in two years with a higher mean intensity of infection. The negative binomial distribution is defined by the mean and by k, a parameter that measures dispersion; k was low when mean infection intensity was low but higher when mean infection intensity was high. As k is an inverse index of overdispersion this indicated that the distribution of 4th-stage larvae was more overdispersed at low levels of infection. In a combined analysis, the number of adult T. circumcincta and the plasma IgA activity against 4th-stage larvae were both associated with increased numbers of 4th-stage larvae. There was a statistical interaction between the number of adults and IgA activity that moderated their combined effect.

The sequential development of type I and type II ostertagiasis in young cattle with special reference to biochemical and serological changes.

The sequential development of Type I and Type II ostertagiasis over a 2-year period in the same naturally infected cattle is described for the first time. Particular reference is made to biochemical and serological changes. Positive relationships were demonstrated between the clinical signs of both Type I and Type II disease, and marked increases in the levels of plasma pepsinogen, plasma gastrin and antibody titres to adult Ostertagia antigen. At necropsy, there were significant relationships between the combined total of adult and developing 5th stage larvae of Ostertagia spp. and the levels of both plasma pepsinogen and gastrin. By the end of the second grazing season the cattle had acquired an immunity to infection with Ostertagia spp. and had very low burdens of this parasite at necropsy. However some of these cattle maintained elevated plasma pepsinogen levels when under natural challenge by Ostertagia spp. larvae and the aetiology of these changes and the problems of diagnosis using this parameter are discussed. Similar trends of infection were observed for Cooperia oncophora, although resistance to the parasite developed more rapidly.