Differences in immune responses to Haemonchus contortus infection in the susceptible Ile de France and the resistant Santa Ines sheep under different anthelmintic treatments regimens

Abstract

Understanding the immunological basis of resistance to gastrointestinal nematode infections in livestock is important in order to develop novel methods of parasite control such as vaccination or genetic selection for parasite resistance. The present study aimed to investigate differences in immune response between parasite resistant Santa Ines and susceptible Ile de France sheep breeds to natural Haemonchus contortus infection. Parasitological parameters, humoral immunity, local and circulating cellular immune responses were evaluated in 19 Santa Ines and 19 Ile de France lambs undergoing different anthelmintic treatments regimens: suppressive treatments (SUP) or targeted selective treatments (TST) over a 5-month grazing period. Santa Ines lambs had significantly lower Haemonchus faecal egg count and worm burden compared to Ile de France regardless of treatment regime. In addition, circulating blood eosinophils count and parasite-specific IgG levels were significantly higher and more rapidly induced in Santa Ines lambs. Abomasal immune responses were generally greater in the resistant breed, which had significantly higher levels of parasite-specific IgA in mucus, and elevated number of globule leukocytes and CD3+ T cells within the abomasal mucosal. Furthermore, numbers of POU2F3+ epithelial cells, a tuft-cell specific transcription factor, were also elevated in the Santa Ines breed, suggesting that this breed is better able to initiate T-helper type 2 immune responses within the abomasum. In conclusion, the differential immunological responses detailed here are relevant to understanding resistance to gastrointestinal nematodes in other host breeds, as well as to resistance breeding as a sustainable control approach for parasitic infections.

Haematological variables of Santa Ines and Ile de France suckling lambs: Influence of Haemonchus contortus infection

“…Absence of difference between susceptible and resistant sheep breeds in circulating eosinophil count may thus reflect immune responses to different stages of GIN infection (Bowdridge et al 2015). As supposed by Albuquerque et al (2019), our results suggest that Santa Ines lambs had an increase in eosinophil production, however differences on circulation number were not identified, because they also promote a rapid migration of such cells to the site of parasite infection.…”

“…Rocha et al (2005) in study with Santa Ines and Ile the France suckling lambs naturally infected by gastrointestinal nematodes, observed no significant differences between breeds regarding to eosinophil counts, although Santa Ines lambs had higher means of eosinophils than Ile the France lambs over the trial. In a H. contortus chronic infection, naturally infected Santa Ines lambs (8 months old) had higher mean blood eosinophil counts than Ile de France lambs (Albuquerque et al 2019).…”

“…Several studies have shown that Santa Ines sheep is considered more resistant to GIN infections compared to Ile de France sheep at different age categories (Amarante et al 2004, Rocha et al 2005, mainly because of Santa Ines sheep present an earlier and robust initial Th2 response (Albuquerque et al 2019).…”

“…This is the case of Santa Ines sheep, a native breed from northeastern Brazil, considered more resistant to H. contortus infection when compared to Ile de France sheep (Amarante et al 2004, Rocha et al 2005, Amarante et al 2009. Santa Ines lambs, after weaning, showed a higher resistance against H. contortus infection when compared to lambs of European breeds (Amarante et al 2004, Albuquerque et al 2019.…”

Cellular and humoral immune responses associated with protection in sheep vaccinated against Teladorsagia circumcincta

“…IL-4 is a key cytokine in mast cell maturation and, in agreement with histological data, it was also identified at high levels in ALN cells in all groups, independent of breed or vaccination status, following exposure to L4 and adult antigens. Globule leukocytes have been previously associated with resistance against GIN in animals naturally resistant to T. circumcincta [ 23 , 24 ], generating a rapid larval rejection [ 25 ]. The data obtained here suggest that the vaccine confers protection in these breeds partly through improving mostly “natural mechanisms” of protection.…”