Molecular insights into the persistence and ward-specific distribution of two co-circulating carbapenem-resistant Pseudomonas aeruginosa lineages in pediatric respiratory isolates

Background Carbapenem-resistant Pseudomonas aeruginosa (CRPA) represents a critical cause of refractory infection and nosocomial transmission in pediatric populations. Genomic surveillance and epidemiological investigations into respiratory CRPA isolates from pediatric patients remain scarce. This study sought to elucidate the clinical characteristics, resistance mechanisms, molecular epidemiology, virulence factors, and nosocomial transmission dynamics of pediatric respiratory CRPA. Methods A total of 113 respiratory CRPA isolates collected from a tertiary children’s hospital during 2019–2025 were retrospectively analyzed. Antimicrobial susceptibility testing, MLST, O-serogroup typing, resistance and virulence gene detection, plasmid replicon identification, and whole-genome phylogenetic analysis were systematically performed. Results Most isolates were derived from ICU patients with respiratory underlying diseases. All strains were fully susceptible to colistin with low aminoglycoside resistance. The isolates exhibited high polyclonal diversity encompassing over 40 sequence types, dominated by ST244, with O5, O1 and O6 as major serogroups. The carriage rate of acquired carbapenemase genes was merely 7.96%, with no metallo-β-lactamase genes detected. OXA-type genes tended to accumulate in ICU isolates without statistical significance, and only three plasmid replicon types were sporadically identified. Phylogeny defined two clades with distinct ward-specific endemic patterns, and the exoU⁻/exoS⁺ T3SS pathotype was predominant. Conclusions Pediatric respiratory CRPA presents high genetic heterogeneity and differentiated intra-hospital transmission. Non-carbapenemase-mediated mechanisms predominantly contribute to carbapenem resistance. Continuous genomic surveillance targeting ICU-endemic clones is essential to prevent persistent CRPA transmission in pediatric healthcare settings.