Metabolic Syndrome During Perinatal Period in Sows and the Link With Gut Microbiota and Metabolites.

Abstract

In humans, the metabolic and immune changes occurring during perinatal period also describe metabolic syndrome. Gut microbiota can cause symptoms of metabolic syndrome in pregnant women. Increased gut permeability is also involved in metabolic disorders in non-pregnant hosts. However, longitudinal studies investigating the changes in metabolic characteristics, gut microbiota, and gut permeability of sows throughout pregnancy and lactation are lacking. The correlation between gut microbiota and metabolic status of sows is also poorly known. The present study was conducted to investigate the temporal variations in sow metabolic characteristics, gut microbiota, gut permeability, and gut inflammation at days 30 (G30) and 109 (G109) of gestation and days 3 (L3) and 14 (L14) of lactation. Results showed that insulin sensitivity was decreased in L3. Circulating concentrations of pro-inflammatory cytokine IL-6 increased in G109 and L3. 16S rRNA gene sequencing of the V3-V4 region showed that gut microbiota changed dramatically across different reproductive stages. The bacterial abundance and alpha diversity in L3 were the lowest. The phyla Proteobacteria and Fusobacteria exhibited the highest relative abundance in L3. Among the genera, Bacteroides, Escherichia_Shigella, and Fusobacterium were highest, but Oscillospira the lowest, in relative abundance in L3. The fecal levels of acetate and total short-chain fatty acids were increased in G109, but fecal butyrate concentrations were markedly decreased in L3. The plasma zonulin concentrations, a biomarker for gut permeability, were increased in G109 and L3. The plasma endotoxin concentrations were increased in L3. Furthermore, levels of fecal lipocalin-2 and pro-inflammatory cytokines IL-6 and TNF-α were increased in G109 and L3. In contrast, fecal levels of anti-inflammatory cytokine IL-10 were significantly decreased in G109 and L3. Additionally, the increased relative abundances of Fusobacterium in L3 were positively correlated with plasma zonulin and fecal endotoxin but negatively correlated with fecal IL-10. These findings indicate that the mother sow exhibits a metabolic syndrome and dramatical changes in gut microbiota during perinatal period, especially in early lactation. Besides, increased gut permeability and plasma endotoxin concentrations caused by negative microbial changes would possibly be the potential mechanisms under which sow’s metabolic disorders and inflammatory status were exacerbated during early lactation.