Global epidemiology of high priority and pandemic Pseudomonas aeruginosa in pets, livestock, wild, and aquatic animals: a systematic review and meta-analysis.

High-priority and international high-risk Pseudomonas aeruginosa (PA) are emergent strains. Here, we performed the first systematic review and meta-analysis of studies that reported the frequency of PA, carbapenem (CARBR), and colistin (COLR) resistant PA in healthy and sick livestock (A), pets (B), wild (C), and aquatic animals (D) from January 2013 to January 2023, globally. Following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines, 57 cross-sectional and eight prospective studies were found eligible. Random-effect models were used to determine the pooled prevalences. Phylogenetic analyses based on core-genome single nucleotide polymorphisms (SNPs) were performed using CSI Phylogeny 1.4. The overall pooled prevalence of PA, COLR-PA, and CARBR-PA were 18.6%, 4%, and 11.7%, respectively. Wild animals had the highest pooled prevalence of PA, 33.5%. The pooled prevalence of COLR was significantly higher in PA strains from sick than healthy animals (P < 0.0001). Furthermore, COLR was significantly highest in PA strains from wild animals, 9.8% [95% confidence interval (CI): 0.8-58.9], while CARBR was highest in PA strains from pets, 14.8% (95% CI: 6.7-29.8). Seven (ST235, ST111, ST233, ST244, ST357, ST308, and ST277) of the 10 high-risk CARBR-PA clones carrying ExoS/U were reported in animals. The SNP-based phylogenetic analysis of 23 genomes of CARBR-PA from animals obtained from publicly available databases revealed two closely related blaGES-carrying strains (<100 SNPs) in sick pets, suggesting a transmission event. A higher frequency of high-risk carbapenem than colistin-resistant PA strains exists in animals. These findings highlight the roles of different animal species, especially pets and wild animals in the persistence and dissemination of high-priority PA.