Prenatal lipopolysaccharide stimulation modulates gastrointestinal immunity and oxidative status in weaned pigs.

Abstract

Gastrointestinal immunity and antioxidant defenses may be bolstered in young animals through prenatal immune stimulation (PIS), but this is largely uninvestigated in swine. This study tested the hypothesis that PIS could regulate offspring's gastrointestinal immune response and oxidative stress profile. To this end, a PIS model was utilized in sows, delivering low-dose lipopolysaccharide (LPS) during the final third of gestation to target the developing immune system. On day 78 ± 1.8 of gestation, 14 Camborough sows (parity = 2.6 ± 1.4) received either saline (Control, CON) or LPS from Escherichia coli O111:B4 (2.5 µg/kg of body wt). A subset of 34 weaned barrows (n = 17 CON, PIS), weaned at 21 ± 1.3 days, were anesthetized for subcutaneous temperature loggers and jugular catheter placement. Following recovery, all pigs received an intravenous injection of LPS (10 µg/kg·body wt) from E. coli O111:B4. Our findings demonstrate that PIS enhances the gut immune response by upregulating key inflammatory cytokines, indicative of a proinflammatory profile. Consistently across the jejunum and ileum, stem cell factor was modulated with heightened expression in PIS than CON (P ≤ 0.05). In the ileum alone, PIS exhibited heightened expression of proinflammatory cytokines and chemokines, including TNFα, IL-6, IL-1β, and CCL3L1, compared with CON (P ≤ 0.05). Exposure to PIS resulted in reduced systemic total antioxidant capacity at hours 2 and 4 postchallenge (P = 0.004). Piglets exposed to PIS had decreased jejunal tissue malondialdehyde concentrations (P = 0.049). Together, these data indicate that exposure to PIS alters the inflammatory profile of the gastrointestinal immune response and oxidative status in weaned pigs.NEW & NOTEWORTHY These studies represent novel investigations into the influence of prenatal immune stimulation (PIS) in swine on the gastrointestinal immune response and oxidative status of offspring following subsequent immune challenge. Notable alterations were observed in gut protein biomarkers, particularly the upregulation of proinflammatory cytokines TNFα, IL-6, and IL-1β in PIS-exposed pigs, but has variable effects on oxidative status. Altered intestinal immune development may contribute to an increased risk for inflammatory disease associated with prenatal immune stimulation.