Intrauterine growth restriction (IUGR) predisposes newborns
to inflammatory and metabolic disturbance. Disequilibrium
of gut microbiota in early life has been implicated
in the incidence of inflammation and metabolic diseases in
adulthood. This study aimed to investigate the difference in
gut microbiota colonization, cytokines and plasma metabolome
between IUGR and normal birth weight (NBW) piglets
in early life. At birth, reduced (P < 0.05) body, jejunum, and
ileum weights, as well as decreased (P < 0.05) small intestinal
villi and increased (P < 0.05) ileal crypt depth were observed
in IUGR piglets compared with their NBW counterparts. Imbalanced
inflammatory and plasma metabolome profile was
observed in IUGR piglets. Furthermore, altered metabolites
were mainly involved in fatty acid metabolism and inflammatory
response. At 12 h after birth and after suckling colostrum,
reduced (P < 0.05) postnatal growth and the small intestinal
maturation retardation (P < 0.05) continued in IUGR
piglets in comparison with those in NBW littermates. Besides,
the gut microbiota structure was significantly altered
by IUGR. Importantly, the disruption of the inflammatory
profile and metabolic status mainly involved the pro-inflammatory
cytokines (IL-1β and IFN-γ) and amino acid metabolism.
Moreover, spearman correlation analysis showed
that the increased abundance of Escherichia-Shigella and decreased
abundance of Clostridium_sensu_stricto_1 in IUGR
piglets was closely associated with the alterations of slaughter
weight, intestinal morphology, inflammatory cytokines, and
plasma metabolites. Collectively, IUGR significantly impairs
small intestine structure, modifies gut microbiota colonization, and disturbs inflammatory and metabolic profiles during
the first 12 h after birth. The unbalanced gut microbiota
mediated by IUGR contributes to the development of inflammation
and metabolic diseases.