The role of human-pig interactions in modulating gut microbiota, stress, and performance.

BACKGROUND: The microbiota‒gut‒brain axis modulates pigs' stress response, behavior, and overall welfare. Stressful management practices can disrupt gut microbiota (GM), negatively impacting pigs' health and welfare. This study evaluated how the quality of human handling influences stress-related physiological responses, productive performance, and gut microbiota (GM) composition in pigs during the nursery phase. RESULTS: Female pigs (n= 36, 21 days old) were randomly assigned to three experimental groups (12 pigs/group, four pens per treatment): positive human handling (PHH), negative human handling (NHH), and a control group (CG). The PHH group experienced gentle tactile interactions, whereas the NHH group was subjected to chronic intermittent stress through acute stressors, and the CG group received minimal handling for routine practices. Hair cortisol concentrations were measured as an indicator of chronic stress (days 15 and 64). Productive performance was assessed through body weight (BW), average daily gain (ADG), average daily feed intake (ADFI), and feed conversion (FC). Fecal samples were collected at baseline (T0, day 16), mid-study (T1, day 37), and end of the study (T2, day 65) and analyzed using 16S rRNA gene amplicon sequencing to assess GM changes over time. Pigs in the PHH group showed a significant reduction in cortisol levels from baseline to post-treatment (P < 0.0001), while no significant changes were observed in the NHH group (P = 0.26). A smaller but significant decrease was also detected in the CG group (P = 0.001). PHH pigs had higher BW (P = 0.0009) and ADG (P = 0.03) during the later growth phase compared to NHH pigs. At T2, PHH pigs exhibited greater diversity and richness compared to NHH pigs, indicating a restorative effect on GM composition. Differential abundance analyses identified four bacterial genera that distinguished treatment groups: Blautia, Megasphaera, and Subdoligranulum were enriched in PHH pigs, while Terrisporobacter was enriched in NHH pigs. Additionally, bacterial interaction networks exhibited the least complex network in the NHH group, with ecological associations primarily involving Clostridium and Terrisporobacter. CONCLUSIONS: The quality of human handling influenced stress physiology, performance, and gut microbiota in pigs. Positive handling reduced cortisol levels, improved growth, and promoted microbial diversity, while negative handling was linked to decreased performance and reduced microbial network complexity. These results highlight the potential of positive interactions to enhance welfare and productivity, and identify specific bacterial genera as potential biomarkers differentiating negative and positive handling conditions.