1H NMR-based metabolomics reveals metabolic changes in porcine ingesta and serum during Ascaris suum infection

BACKGROUND: Roundworm infections are of major importance both for humans and livestock. The porcine roundworm Ascaris suum, the most economically important nematode in pig production worldwide, serves as a valuable model for human ascariosis, yet knowledge of its metabolic impact remains limited. METHODS: Metabolic changes were investigated in pigs infected once with 10,000 A. suum eggs versus trickle-infected pigs (1000 eggs/day over 10 days) compared with uninfected controls. Ingesta and serum samples of six pigs each were collected on days 21, 35, and 49 post infection (pi) for nuclear magnetic resonance (NMR)-based metabolomics analyses. RESULTS: Trickle-infected pigs showed more pronounced metabolic changes than single-infected pigs, following a triphasic temporal pattern with initial changes at day 21 pi, maximal disruption at day 35 pi, and partial recovery by day 49 pi. The colon exhibited the most significant changes in short-chain fatty acids (SCFAs) and amino acids. On day 21 pi, trickle-infected pigs showed increased acetate, butyrate, valerate, and amino acids in the colon, with reversed patterns on day 35 pi. Serum changes mirrored colonic alterations, suggesting the colon as primary driver of systemic responses. Single-infected pigs showed less pronounced changes, with increased lactate and acetate in the ileum and elevated amino acids in the cecum on day 35 pi. CONCLUSIONS: These findings reveal complex, compartment-specific host-parasite-microbiome interactions, with SCFAs as important mediators. Enhanced growth performance in trickle-infected pigs corresponding with metabolic recovery challenges exclusively antagonistic host-parasite relationships. This study deepens the understanding of A. suum pathophysiology and provides crucial insights for human ascariosis, supporting targeted interventions for animal and human health.