Genetic and virulence analysis of carbapenem-resistant Pseudomonas aeruginosa in farm animals in Shandong province, China: implications for human health

中国山东省农场动物中耐碳青霉烯类铜绿假单胞菌的遗传和毒力分析:对人类健康的影响

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Abstract

BACKGROUND: Carbapenem-resistant Pseudomonas aeruginosa (CRPA) poses a significant threat to human health, with animal feces serving as an important reservoir of antibiotic-resistant bacteria and potentially CRPA. However, data on the prevalence and characteristics of CRPA in animals are still lacking. The pathogenic potential of CRPA from animals is also poorly understood. This study investigated the prevalence of CRPA in animals in China, along with the virulence potential and phylogenetic relationships of CRPA from animals and humans. RESULTS: The detection rate of CRPA among the 867 animal samples was 5.07%. Notably, multi-drug resistance was observed in 62% of the 50 animal-derived CRPA, significantly higher than the 23 clinical CRPA isolates in this study (p < 0.05). Furthermore, 20% of the CRPA isolates from animals showed resistance to colistin. Mutations in the oprD gene, rather than carbapenemases, were identified as the primary cause of carbapenem resistance. Phylogeographic analysis revealed that PA isolates were disseminated across 47 countries, and the sequence types (STs) exhibited significant diversity. Furthermore, a higher detection rate of animal-derived CRPA simultaneously carrying multiple virulence factors was observed, surpassing the rate in clinical CRPA. Galleria mellonella assays further confirmed that the CRPA from animals and humans exhibited greater pathogenicity than the hypervirulent Klebsiella pneumonia 18,622. Phylogenetic analysis further revealed that the animal hypervirulent CRPA had only a few SNPs with clinical PA from various countries, including our clinical CRPA, indicating the potential of clonal transmission of CRPA between animals and humans. CONCLUSION: Our findings reveal that animals could be an important reservoir of hypervirulent CRPA and highlight the potential for zoonotic transmission to humans. The emergence of hypervirulent CRPA in animal feces highlights the significance of developing control measures in animal farming environments from a "One Health" perspective.

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