Pathogen exposure influences immune parameters around weaning in pigs reared in commercial farms

BACKGROUND: Multiple antigenic stimulations are crucial to immune system training during early post-natal life. These stimulations can be either due to commensals, which accounts for the acquisition and maintenance of tolerance, or to pathogens, which triggers immunity. In pig, only few works previously explored the influence of natural exposition to pathogens upon immune competence. We propose herein the results of a multicentric, field study, conducted on 265 piglets exposed to contrasted pathogen levels in their living environment. Piglets were housed in 15 different commercial farms, sorted in two groups, low (HS(LOW))- and high (HS(HIGH))-health status farms, depending on their recurrent exposition to five common swine pathogens. RESULTS: Using animal-based measures, we compared the immune competence and growth performances of HS(LOW) and HS(HIGH) pigs around weaning. As expected, we observed a rise in the number of circulating leucocytes with age, which affected different cell populations. Monocyte, antigen-experienced and cytotoxic lymphocyte subpopulation counts were higher in piglets reared in HS(LOW) farms as compared to their HS(HIGH) homologs. Also, the age-dependent evolution in γδ T cell and neutrophil counts was significantly affected by the health status. With age, circulating IFNα level decreased and IgM level increased while being greater in HS(LOW) piglets at any time. After weaning, LPS-stimulated blood cells derived from HS(LOW) piglets were more prone to secrete IL-8 than those derived from HS(HIGH) pigs did. Monocytes and granulocytes issued from HS(LOW) pigs also exhibited comparable phagocytosis capacity. Altogether our data emphasize the more robust immunophenotype of HS(LOW) piglets. Finally, piglets raised under higher pathogen pressure grew less than HS(HIGH) piglets did and exhibited a different metabolic profile. The higher cost of the immune responses associated with the low farm health status may account for lower HS(LOW) piglet performances. CONCLUSIONS: Altogether, our data, obtained in field conditions, provide evidence that early exposure to pathogens shapes the immune competence of piglets. They also document the negative impact of an overstimulation of the immune system on piglets’ growth. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12865-022-00534-z.