Penicillin-susceptible ST398 with strong biofilm-forming ability poses a significant threat to osteoarticular infections

BACKGROUND: Osteoarticular infections (OAIs), primarily caused by Staphylococcus aureus (both MSSA and MRSA), pose significant clinical challenges due to their heterogeneity and complexity. OBJECTIVE: To investigate the epidemiology, clinical characteristics and bacterial features of S. aureus strains isolated from OAI patients treated at a major tertiary hospital in China over a 9-year period, with a focus on biofilm formation and colonization potential. METHODS: A total of 178 S. aureus isolates (56.8% MSSA and 43.2% MRSA) were analyzed using whole-genome sequencing, antibiotic susceptibility testing, biofilm formation assays and phylogenetic analysis. A murine nasal colonization model and in vitro adhesion assays using A549 human epithelial cells were employed to evaluate colonization and adherence capabilities. RESULTS: Penicillin-susceptible Staphylococcus aureus (PSSA) showed a significant rise during the study period, particularly within clonal complex ST398, which exhibited enhanced biofilm-forming capabilities. Phylogenetic analysis revealed minimal transmission events, suggesting independent cases. Comparative genetic analysis demonstrated distinct human-adaptive features in MRSA and MSSA-ST398 strains. PSSA-ST398 strains exhibited superior biofilm formation and increased adherence to human epithelial cells and murine nasal cavities compared with penicillin-resistant counterparts, indicating a potential advantage in colonization and persistence. CONCLUSIONS: Penicillin-susceptible ST398 strains, particularly those with strong biofilm-forming capabilities, which increase their persistence in clinical settings, complicating treatment and eradication efforts, represent a significant threat to OAIs. Despite being penicillin-susceptible, these strains may still pose challenges due to their biofilm-mediated resistance and potential for chronic infection.