To our knowledge, this is the first longitudinal study equivalent to 10 cross-sectional studies that provides a comprehensive insight into the prevalence of nasal carriage state, resistance phenotype, and genetic characteristics of S. aureus among the community population in China. The average nasal carriage rate of S. aureus was 16.78% among the 10 samplings. This finding coincides with the prevalence rates observed in the cross-sectional studies conducted in Northern China (16.5%) and Guangzhou (23.4%) [15, 16]. Cross-sectional studies conducted outside China found S. aureus prevalence ranging from 21.9% to 47.6% among different populations, with MRSA identified in 0.7–8.81% [17,18,19,20]. The prevalence rates of MRSA and MDRSA carriage in our first cross-sectional study were approximately 6.29% and 7.69%, respectively. Therefore, compared with other countries, the general Chinese population exhibits a lower rate of nasal carriage, but a higher prevalence of MRSA nasal carriage.

In our longitudinal nasal sampling, 14.69% of individuals harbored MRSA at least once, which is twice as the rate perceived in our single cross-sectional MRSA study, and significantly surpassed those reported in both domestic and international cross-sectional studies. This suggested that relying solely on cross-sectional data to determine carrier status may underestimate true prevalence, thereby emphasizing the importance of collecting multiple consecutive samples to determine a more accurate carrier rate. However, accurately determining the persistent carriage rate of MRSA in a healthy community remains challenging because of the absence of comprehensive antibiotic susceptibility testing for all S. aureus isolates.

In this study 8.39% of individuals were identified as persistent carriers, 39.16% as intermittent carriers, and 52.45% as non-carriers. This contrasts with the findings of several longitudinal studies, which indicate 20% persistent carriers, 30% intermittent carriers, and 50% non-carriers [21]. This discrepancy may stem from the use of diverse culture techniques and intervals, different study populations, and varying colonization state definitions. Our research confirmed that the rates of persistent carriers and non-carriers decrease with longer follow-up periods and fewer culture intervals, suggesting potential misclassification of intermittent carriers as either persistent carriers or non-carriers if the follow-up period is brief or if only a few samples are cultured [22]. Previous colonization studies simplified carriage phenotypes into just two categories: persistent carriers and intermittent/non-carriers; however, given the intricate nature of the disparities between persistent and intermittent carriers, we concur that the colonization status should be divided into three categories [23, 24].

Although not statistically significant (p > 0.05), there was a trend for higher S. aureus colonization in the nasal cavity in women, younger individuals, and those with higher BMI. This result was consistent with the findings of Olsen et al., who observed a positive correlation between BMI and colonization in younger women [25]. This discrepancy highlights the need for further research to elucidate variations in carriage rates and patterns of S. aureus and MRSA among different populations.

Our study further demonstrated that persistent carriers are inclined to carry the same S. aureus genotype, while intermittent carriers may carry varying genotypes, owing to decolonization and recolonization over time [21, 22]. This dynamic nature underscores the complexity of S. aureus nasal carriage [26]. Once colonized by stubborn S. aureus for an extended period, decolonization becomes more difficult. Therefore, monitoring and treating nasal carriages is crucial to reduce nosocomial infection rates, thus emphasizing the need for expanded prehospitalization nasal swab testing.

We observed a correlation between the genotype, SNP distance, and SPA results, which confirmed that SPA typing can be used as a quick method for identifying S. aureus carriers. The correlation between SPA typing and MLST was previously assessed, and it was determined that SPA typing could effectively predict MLST clonal complexes, as defined by eBURST [27, 28]. Similarly, all t084 in our study corresponded to CC15. An intriguing discovery was made in both the aforementioned study and ours, indicating a connection between intermittent carriage and t084.

However, our study uncovered widespread resistance to penicillin and ampicillin in all strains, likely attributed to their extensive use. Furthermore, 24.30% of the strains demonstrated oxacillin resistance and all strains displayed sensitivity to ceftaroline. Oxacillin and ceftaroline were the most suitable choices for treating CA-MSSA. Linezolid, teicoplanin, and vancomycin were effective against all strains, indicating their potential as last-resort options for MRSA treatment. Clindamycin and erythromycin are commonly utilized to treat SSTIs [29]; but, our CA-MRSA strains exhibited substantial resistance to clindamycin and erythromycin, underscoring the critical need for judicious antibiotic selection. Furthermore, we identified 41 MDR strains, of which approximately 68.29% of the MDRSA strains originated from the persistent carriers. Prolonged colonization by MDRSA poses an increased potential risk for carriers as it renders treatment more challenging once infected. This finding underscores the need for regular testing of healthy individuals and timely eradication of staphylococcal carriage to prevent S. aureus infection.

Our study found that ARs are consistent with resistance phenotypes, such as tet(L) and erm(C) genes, which are associated with tetracycline and MLS antibiotic resistance, respectively, and consistent with previous research [30]. Besides, all 26 MRSA strains carried mecA and were resistant to oxacillin, which aligns with the definition of MRSA. β-lactam resistance profiles are generally biased by MRSA status. In addition, our findings suggest that the presence of ARs in ICEs/IMEs may contribute to the spread of antibiotic resistance among bacterial populations. Overall, our study emphasizes the need for a more comprehensive approach to address antibiotic resistance, considering the role of ICEs/IMEs [31].

ST59 was identified as the most prevalent ST, closely followed by ST398. Notably, 91.7% of the ST59 strains were identified as MRSA. ST59-MRSA has long been acknowledged as one of the most successful and enduring CA-MRSA clones in Asia, including China [32]. Furthermore, ST59 strains frequently harbor ARs to macrolides and β-lactams (ermB and mecA, respectively), and present significant challenges for treating infections caused by these strains [32]. All ST59 strains belonged to MDRSA, which is consistent with previous findings. Additionally, the ST59 strains carried the highest number of VFs. ST59-t437, a prominent strain in our study, has been extensively documented in China and has been associated with severe inflammatory reactions, ultimately leading to patient mortality [33]. Therefore, our findings underscore the importance of maintaining heightened vigilance regarding ST59 colonization in our healthy population. Our study revealed that the proportion of ST398-MRSA strains was comparable to that of ST398-MSSA strains, indicating an increasing prevalence of ST398-MRSA among healthy adults in Jiangsu. Furthermore, we noted a predominance of ST398 strains among intermittent colonizers, with a significant proportion of these strains carrying ICEs, thus reinforcing our hypothesis regarding the association between intermittent colonization and ICE carriage. We noted an interesting phenomenon among the intermittent colonizers (67, 137, and 140), wherein ST59 and ST398 were observed as alternating strains carried by these individuals. This observation prompts further investigations into the potential connection between these two STs.

The pathogenesis of toxic shock syndrome (TSS) is closely linked to S. aureus, which produces tsst-1. All the ST508-t015-CC45 isolates in our study carried this toxin and were classified as MDRSA. However, previous studies conducted in China have primarily associated CC5 and CC398 genotypes with tsst-1 [34]. A strong association between PVL and CA-MRSA has already been demonstrated [35, 36]. However, contrary to these findings, our results revealed that only 38.46% of CA-MRSA strains carried the PVL toxin. Similarly, during the same period as our research in Germany, 40.4% of CA-MRSA isolates harbored the virulence factor PVL [37], indicating a probability similar to ours. Therefore, we believe that solely relying on the presence of PVL cannot definitively determine MRSA strain as CA-MRSA. MRSA strains possessing both lukS and lukF genes are considered more virulent and have been associated with the development of severe necrotizing pneumonia [38]. Notably, all MRSA strains carrying both lukS and lukF genes in this study belonged to the ST59-MRSA lineage and also carried the seb-selk-selq genes, highlighting their pathogenic potential within the ST59 lineage.

Notably, S. aureus collected from individuals within the same household exhibited close genetic relatedness, suggesting the possibility of intra-household transmission, and therefore, aligning with findings from previous research [5]. Within these households, we identified both persistent and intermittent carriers, with persistent colonizers potentially serving as sources of infection, thereby facilitating transmission within the household setting. Consequently, cohabitation with persistent carriers represents a significant risk factor for healthy individuals in communities, which increases the likelihood of S. aureus infection.