Linking the degree of intrauterine growth restriction to alterations in metabolism, energy reserves, and gut health in newborn piglets.

In modern swine production, increasing litter size has reduced average birth weight (BtW) and increased the prevalence of intrauterine growth restriction (IUGR). This study aimed to classify piglets by degree of IUGR and evaluate associated morphological, physiological, and behavioral traits. A total of 1,990 piglets were categorized by BtW as IUGR (<0.75 kg), restricted low BtW (R-LBW; 0.75-0.95 kg), non-restricted low BtW (NR-LBW; 0.95-1.15 kg), and normal (N; ≥1.15 kg). A subset of 48 piglets (12/category) was euthanized within 24 h of birth for tissue and blood collection. Data were analyzed by linear mixed models, with piglet category as a fixed effect. Piglets with IUGR had the lowest body weights from birth to weaning, not differing from R-LBW piglets at d 7 and weaning, while N piglets were the heaviest (P < 0.01). Average daily gain was lower (P ≤ 0.03) in IUGR and R-LBW piglets compared with NR-LBW and N piglets throughout lactation. Colostrum intake (CI) differed (P < 0.01), with IUGR piglets consuming 285 g less than N piglets. Consequently, NR-LBW and N piglets showed higher immunoglobulin G concentrations compared with the other categories (P ≤ 0.03). Morphological indicators confirmed growth restriction, with IUGR piglets showing the lowest values. Vitality scores were lowest in IUGR piglets (62.4% scored worst; P < 0.01). Piglets with IUGR had lower albumin concentrations than N piglets (P < 0.01), whereas N piglets exhibited the highest insulin-like growth factor I concentrations (P < 0.01). Metabolomic profiling revealed distinct clustering of IUGR piglets compared with the other categories (P ≤ 0.01), indicating altered amino acid and energy metabolism. Glycogen concentrations were impaired in IUGR piglets, averaging ∼55% lower than in N piglets (P = 0.02). Intestinal function and development were altered in IUGR and low BtW piglets, which exhibited a lower villus height: crypt depth ratio compared with N piglets (P ≤ 0.03), along with a gene expression profile characterized by upregulation of genes associated with inflammatory response and stress. In conclusion, IUGR piglets exhibited impaired growth during lactation, which was associated with low vitality, reduced CI, metabolic alterations, gastrointestinal dysfunction, and limited energy availability at birth. Further indicators should be investigated to better understand the differences among low BtW piglets, which also exhibited poorer growth performance than N piglets.