The periparturient relaxation of immunity in Merino ewes infected with Trichostrongylus colubriformis: Parasitological and immunological responses

The temporal association between the periparturient rise (PPR) in worm egg count (WEC) of grazing Merino ewes to infection with Trichostrongylus colubriformis and the underlying causal mechanisms was investigated in an experiment that incorporated two levels of pregnancy (pregnant or unmated), two levels of infection (infected with 6000 T. colubriformis L3/week or uninfected) and, following lambing, three levels of lactation (non-lactating/“dry”, early-weaned 2 days after parturition, or suckled). The 128 ewes in the experiment were monitored for a range of parasitological and host systemic and local immune responses from days −50 to 42, relative to the midpoint of lambing (day 0). Unmated/non-lactating (dry) ewes remained largely resistant to T. colubriformis infection with WEC remaining below 200 eggs per gram (epg) throughout the experiment. For infected ewes, the PPR in WEC commenced during late pregnancy and peaked at 1552 epg on day 42. There was evidence of a relaxation of immunity that preceded the rise, as demonstrated by a reduction in circulating eosinophils and plasma total antibody (Tab) and lower titres of Tab and IgG1 in the small intestine in pregnant ewes. Circulating eosinophils and plasma Tab remained low in suckled ewes, and at the local level, lactating ewes also had lower titres of Tab, IgG1, IgM, IgA and IgE as well as fewer mast cells (MC), globule leucocytes (GL) and goblet cells (GC) in intestinal tissue. These effects were associated with higher worm burdens. Weaning at 2 days after lambing resulted in a rapid amelioration of immunological responsiveness and a reduction in WEC, worm burden and parasite establishment rate. A rapid increase in circulating eosinophils and Tab titre followed by an improvement in components of the local immune response was also observed. Over the 6-week period following lambing, weaned ewes exhibited higher titres of Tab, IgG1, IgM, IgA and IgE as well as higher numbers of MC, GL and GC present in the small intestinal tissue, compared to lactating ewes. The results provide a detailed characterisation of the periparturient relaxation of immunity to T. colubriformis, and highlight possible causative factors that deserve further investigation.