Relationships among gastrointestinal mucosal densities of mast cells and eosinophils, helminth infection and diarrhoea in sheep

Abstract

Context Diarrhoea linked to helminth resistance is a major problem in sheep health. Aims To test whether the distribution of mast cells and eosinophils along the gastrointestinal tract is related to helminth resistance and to susceptibility to diarrhoea. Methods At weaning, lambs were selected according to extreme (high or low) estimated breeding values for diarrhoea score (50 lambs per genotype, balanced for sex), and for faecal worm egg counts (FWEC). They grazed in single-sex groups in separate but similar enclosures under normal farm conditions (dry summer, wet winter) from autumn until spring, during which time diarrhoea score and FWEC were recorded monthly. Lambs that presented extreme phenotypic values for diarrhoea score and FWEC in August and September were slaughtered (n = 38) at the age of 14 months. For the abomasum, duodenum, ileum, jejunum, caecum and colon, we recorded the densities of eosinophils and mast cells, the number of helminths, their species and developmental stages. The data were pooled across enclosures/sexes and regression analysis was used to assess the relationships among pre-slaughter phenotype, helminth counts, and densities of mast cells and eosinophils. Results Eosinophil density was five- to seven-fold greater in the ileum and jejunum than in the abomasum, duodenum, or colon. Mast cell density was greatest in the abomasum and duodenum, and gradually declined along the jejunum, ileum, caecum and colon. In the most immunologically active site, the jejunum, increasing eosinophil density was related to a decrease in the number of helminths (P < 0.05). Similarly, in the next most active site, the abomasum, increasing eosinophil density was related to decreases in the numbers of fourth-stage larvae and the total number of helminths (P < 0.05). In the abomasum, increasing mast cell density was related to declines in the numbers of Teladorsagia circumcincta, total helminth counts (P < 0.05) and FWEC, but was not related to diarrhoea score. Conclusions Cell-mediated immune mechanisms in the gastrointestinal mucosa enhance resistance to internal parasites but also increase susceptibility to the diarrhoea in sheep. Implications Eosinophil and mast cell responses to helminth infection help explain ‘hypersensitivity diarrhoea’.