Intrauterine growth restriction, defined by an elevated brain-to-liver weight ratio, affects faecal microbiota composition and, to a lesser extent, plasma metabolome profile at different ages in pigs.

Abstract

Background: Intrauterine growth restriction (IUGR) affects up to 30% of piglets in a litter. Piglets exposed to IUGR prioritize brain development during gestation, resulting in a higher brain-to-liver weight ratio (BrW/LW) at birth. IUGR is associated with increased mortality, compromised metabolism, and gut health. However, the dynamic metabolic and microbial shifts in IUGR-affected pigs remain poorly understood. This study aimed to investigate the longitudinal effects of IUGR, defined by a high BrW/LW, on the composition of faecal microbiota and plasma metabolome in pigs from birth to slaughter. One day (± 1) after birth, computed tomography was performed on each piglet to assess their brain and liver weights. The pigs with the highest (IUGR = 12) and the lowest (NORM = 12) BrW/LW were selected to collect faeces and blood during lactation (day 16 ± 0.6, T1) and at the end of the starter period (day 63 ± 8.6, T2) and faeces at the beginning (day 119 ± 11.4, T3) and end of the finisher period (day 162 ± 14.3, T4).

Results: Faecal microbial Alpha diversity remained unaffected by IUGR across all time points. However, the Beta diversity was influenced by IUGR at T1 (P = 0.002), T2 (P = 0.08), and T3 (P = 0.03). Specifically, IUGR pigs displayed higher abundances of Clostridium sensu stricto 1 (P_adj = 0.03) and Romboutsia (P_adj = 0.05) at T1, Prevotellaceae NK3B31 group (P_adj = 0.02), Rikenellaceae RC9 gut group (P_adj = 0.03), and Alloprevotella (P_adj = 0.03) at T2, and p-2534-18B5 gut group (P_adj = 0.03) at T3. Conversely, the NORM group exhibited higher abundances of Ruminococcus (P_adj = 0.01) at T1, HT002 (P_adj = 0.05) at T2, and Prevotella_9 (P_adj < 0.001) at T3. None of the plasma metabolites showed significant differences at T1 between the IUGR and NORM pigs. However, at T2, asparagine was lower in the IUGR compared to the NORM group (P < 0.05).

Conclusions: These findings show that growth restriction in the uterus has a significant impact on the faecal microbiota composition in pigs, from birth to the beginning of the finisher period, but minimally affects the plasma metabolome profile.