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

Abstract

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.

Keywords: Immunity; On-field study; Pathogen exposure; Pig; Weaning.

Fig. 1

White blood cell counts in HS^LOW versus HS^HIGH piglets, before (grey) and after (black) weaning. Neutrophil (A), monocyte (B) and lymphocyte (C) numbers were obtained from the hematology analyser. Emmeans with lower and upper confidence intervals’ limits are shown on graphs. Insets, results of the linear mixed-effects model analyses

Fig. 2

γδ T, naive CD4⁺ T and B lymphocyte counts in HS^LOW versus HS^HIGH piglets before (grey) and after (black) weaning. yδ T lymphocytes (A CD3⁺ CD4⁻ CD8^−/med), naive CD4⁺ Th lymphocytes (B CD3⁺ CD4⁺) and B lymphocytes (C CD3⁻ CD21⁺) were discriminated using flow cytometry and their numbers calculated. Emmeans with lower and upper confidence intervals’ limits are shown on graphs. Insets, results of the linear mixed-effects model analyses

Fig. 3

Plasmatic IgM and IFNα in HS^LOW versus HS^HIGH piglets before (grey) and after (black) weaning. IgM (A) and IFNα (B) levels were measured in blood samples. Emmeans with lower and upper confidence intervals’ limits are shown on graphs. Insets, results of the linear mixed-effects model analyses

Fig. 4

Cytokine secretion and phagocytic capacity of leucocytes issued from HS^LOW versus HS^HIGH piglets after weaning. A Secretion of IL-10, TNFα and IL-8 was measured in response to the ex vivo exposure of blood cells to LPS in WBA. B Fluorescent bacteria phagocytosis by blood cells was analysed by flow cytometry in HS^LOW versus HS^HIGH piglets. Medians are shown on graphs