Staphylococcus aureus is a common commensal and opportunistic pathogen that readily colonizes skin and mucosal surfaces, especially the anterior nares (Cheung et al., 2021). When skin or mucosal barriers are breached during surgery, the organism can invade underlying tissues and cause postoperative wound infections that prolong hospital stay and increase medical costs (Troeman et al., 2023). Methicillin-resistant S. aureus (MRSA) strains, which carry mecA or mecC, are resistant to all beta-lactam antibiotics, excluding fifth-generation cephalosporins such as ceftaroline (tested in this study) and ceftobiprole. In addition, they frequently exhibit multidrug resistance, making these infections difficult to treat (Hou et al., 2023a). The emergence of MRSA and antimicrobial resistance (AMR) has been a major concern in community and healthcare settings in recent decades.

Although the molecular epidemiology of MRSA has been well described globally, clonal distributions differ markedly between regions and clinical settings (Lynch and Zhanel, 2023). In China, ST239 has historically dominated hospital-associated MRSA, but recent surveillance indicates a shift toward community-associated clones such as ST59 and ST398 (Wang, 2022). The Department of Hand and Foot Surgery, characterized by open wounds and prolonged wound care, represents a high-risk microenvironment for MRSA acquisition; however, data on the current clonal landscape in this specific department are scarce.

Therefore, this study aimed to characterize the AMR profiles and determine the molecular epidemiology of MRSA isolates recovered from patients with postoperative infections, nasal swabs from healthcare workers and family caregivers, and environmental surfaces in the Department of Hand and Foot Surgery of a tertiary hospital in Shenyang. By combining spa typing and multilocus sequence typing (MLST), we sought to elucidate potential MRSA reservoirs, providing evidence-based guidance for targeted infection-control measures.

MRSA has a broad antibiotic resistance spectrum, presenting significant challenges for clinical treatment (Wang et al., 2022). Because of the rapid mutation rate of MRSA, its molecular type varies across continents (Lynch and Zhanel, 2023). Therefore, summarizing and categorizing MRSA molecular type is crucial. From June 2021 to June 2022, the Department of Hand and Foot Surgery at the Central Hospital Affiliated to Shenyang Medical College identified three main MRSA strains: t078–ST25, t437–ST59, and t034–ST398. These findings suggest that when analyzing MRSA molecular typing, both MLST and spa typing should be considered to more accurately identify distinct strains (O'Hara et al., 2016; Hou et al., 2023b).

Previously, the predominant MRSA clone in most cities in China was ST239 (Wang, 2022). Recent nationwide surveillance has demonstrated a marked epidemiological shift in China, with traditional hospital-associated ST239 declining and community-associated ST59 and livestock-associated ST398 emerging in both community and healthcare settings. Our findings are consistent with this trend, as only three cases involving ST239 were identified, whereas the top three prevalent clones were ST398, ST59, and ST25. Patil et al. (2023) found that the major MRSA clone in regional hospitals of Himachal Pradesh, India was also community-associated MRSA with ST398 (39%), consistent with the predominant strain in this study. Additionally, the t437–ST59 clone identified in this study was consistent with the molecular typing results of S. aureus from orthopedic infections in Shanghai, China, as reported by Chen et al. in 2016 (Chen et al., 2016), and from various retail foods in Hangzhou, China, as studied by Chen et al. in 2021 (Chen et al., 2023). The ST5 clone belongs to the Japan–New York clonal lineage, which initially spread in Japan and the United States before being detected in other Asian countries (Aung et al., 2019). It has also been reported in Shenyang and Dalian. In this study, only two ST5 strains were isolated.

ST59 and ST239, two major MRSA clones, differ in virulence and resistance. ST59 carries the chp gene, enhancing immune evasion and virulence but displaying lower resistance, suggesting that supportive therapies might aid treatment (Chen et al., 2021a). By contrast, ST239 exhibits stronger resistance and potentially requires more potent antibiotic combinations. Among other clones, t437-ST59 is prevalent in southern China and highly resistant to clindamycin (82%) and tetracycline (41%) (Chen et al., 2021b). Its treatment is limited by resistance, and chronic infections could require prolonged courses. t548-ST5 (CC5) exhibits reduced sensitivity to vancomycin, with MICs often in the intermediate range, necessitating dosage adjustment or alternative drugs. The t899-ST9 clone, associated with livestock (especially pigs), is prevalent in Asia, and it occasionally infects farm workers, mainly causing skin and soft tissue infections. These findings highlight the risk of resistance spread attributable to antibiotic overuse in agriculture and underscore the need for cross-species monitoring. By contrast, CC1 spreads via human-to-human transmission, and it is linked to severe infections such as sepsis and pneumonia (Elstrom et al., 2019). Its high recombination potential increases resistance risks and complicates treatment, calling for new antimicrobial development. Thus, different MRSA clones vary regarding resistance profiles, virulence, and epidemiology, influencing treatment strategies. For example, ST239 might require broader drug combinations, whereas ST59 might respond to newer agents. Thus, antibiotic susceptibility testing and molecular typing remain essential for guiding clinical decisions.

The sources of MRSA infection can include the patients themselves, family caregivers, healthcare workers, and the hospital environment (Coia et al., 2021). In this study, the infection in patients might be linked to nasal carriage of MRSA, leading to postoperative wound infections. Moreover, family caregivers carrying MRSA in their nasal passages can also contribute to wound infections during patient care (Calderwood et al., 2023). For example, in the analysis of t078–ST25, nasal swabs from patient No. 4 (on February 25, 2022) and her family caregiver (No. 29, on February 24, 2022) obtained in the same ward within a close timeframe shared the same molecular type as the infected specimens, suggesting that caregivers could be a source of infection. Similarly, hospital cleaning staff might carry bacteria while cleaning public areas and restrooms, potentially transmitting the infection to patients (Lena et al., 2021; Alqurashi et al., 2025). In the t437–ST59 strains, nasal swabs from cleaning staff matched the molecular type of patient wound secretions, further supporting this hypothesis. Thus, the combined use of spa typing and MLST enabled detailed comparison of strains from different sources, helping to trace potential transmission reservoirs. For instance, identifying identical spa–MLST types in both nasal swabs and wound specimens suggests clonal dissemination between individuals or from the environment to patients. Conversely, differences in spa types among isolates with the same ST implies genetic diversity within the same lineage, potentially indicating multiple introduction events or microevolution within the hospital setting. This molecular evidence highlights the importance of surveillance among both patients and caregivers and environmental reservoirs.

In hospitals, MRSA primarily spreads through direct contact transmission (Li and Paras, 2024). Direct contact between patients, family caregivers, and healthcare workers, as well as indirect contact with hospital environments, can facilitate MRSA transmission. In this study, 25 of 1,161 nasal-swab samples (2.24%) and 1 of 77 environmental samples were positive for MRSA, indicating a low but persistent presence of the organism among individuals and on surfaces, underscoring the importance of continuous surveillance and strict hygiene measures. For instance, complex patient flow in and out of hospital wards (Sara et al., 2024), coupled with insufficient disinfection in corners, creates a risk for MRSA opportunistic infections. Additionally, if cleaning staff fail to adhere to strict hand hygiene protocols during cleaning or if hand hygiene or environmental disinfection is inadequate, cleaning staff can act as vectors for transmission, as evidenced by the detection of t437–ST59 in a cleaner’s nasal swab, matching the genotype found in six postoperative wound infections in this study. Our hospital currently implements the Hand Hygiene Standard for Healthcare Workers (WS/T 313–2019), which requires the use of fast-drying hand disinfectants before and after patient contact, before aseptic procedures, and after contact with the patient’s environment. Surfaces in wards and corridors and those on medical equipment are required to be wet-cleaned at least twice daily, with additional disinfection using 500 mg/L chlorine solution once daily in high-touch areas. To better control MRSA spread, regular testing and monitoring of all hospital personnel, including doctors, nurses, cleaning staff, patients, and family caregivers, are essential to promptly identify and isolate infection sources.

When treating MRSA infections, it is essential to select appropriate antibiotics based on susceptibility test results rather than relying solely on empirical treatment (Liu et al., 2022). This study found that MRSA strains in nasal swabs were resistant to penicillin and oxacillin but sensitive to vancomycin, cefalothin, tigecycline, and trimethoprim–sulfamethoxazole. Resistance rates for erythromycin and clindamycin exceeded 80%, whereas greater sensitivity was noted for linezolid, teicoplanin, and gentamicin. Strains exhibited high sensitivity to levofloxacin, moxifloxacin, rifampin, and trimethoprim–sulfamethoxazole. In addition, although vancomycin-resistant S. aureus Staphylococcus aureus was not detected in this study, there have been reports in China of heterogeneous vancomycin-intermediate S. aureus, which is vancomycin-sensitive but can produce subcolonies with varying vancomycin susceptibility on vancomycin-containing agar plates (Cheng et al., 2024). This warrants attention, highlighting the need for rational antibiotic use to delay the emergence of vancomycin-resistant MRSA. Therefore, when treating infections in patients undergoing hand and foot surgery, clinicians should refer to susceptibility results to formulate personalized treatment plans, thereby improving therapeutic outcomes and reducing the emergence of resistant strains (Nandhini et al., 2022).

Notably, the MRSA strains isolated in this study exhibited high levels of resistance to both erythromycin and clindamycin. The resistance rates among nasal swab isolates exceeded 80% for both antibiotics, whereas those from postoperative infections reached as high as 86.21%. These findings are consistent with recent multicenter surveillance data in China, suggesting that the macrolide–lincosamide–streptogramin (MLS) resistance phenotype has become widely prevalent in this region. High-level MLS resistance is primarily mediated by erm genes, which encode methyltransferases that modify ribosomal target sites, leading to constitutive resistance (cMLSB phenotype). As this resistance mechanism is irreversible, erythromycin and clindamycin—either alone or in combination—should be avoided in the treatment of suspected or confirmed MRSA infections, particularly in high-risk departments treating postoperative skin and soft tissue infections.

Strengthening hospital infection control is crucial for preventing and reducing MRSA infections (Coia et al., 2021). First, medical staff, especially cleaning staff, should receive continuous training in hand hygiene and disinfection protocols to ensure strict adherence. Second, educating patients and their family caregivers about MRSA infection and prevention before and after surgery is essential for raising awareness. Additionally, hospitals should regularly clean and disinfect patient rooms to reduce MRSA contamination in the environment. For high-risk populations, such as long-term hospitalized patients or immunocompromised individuals, active screening and monitoring might be necessary to detect and isolate infection sources early, thereby preventing MRSA transmission in healthcare settings (Liang et al., 2021).

This study has several limitations. First, the sample size was relatively small, with only 55 MRSA strains analyzed, which may have limited the detection of less prevalent molecular types. Second, although sampling was performed prospectively, the 1-year study period did not allow for longitudinal analysis of strain dynamics, seasonal variation, or temporal linkage between colonization and infection events. Third, molecular resolution was restricted to spa typing and MLST, which provide lineage-level information but do not enable high-resolution genomic comparison or inference of transmission relatedness; whole-genome sequencing (WGS) would be required to confirm clonal transmission. Finally, the study was conducted in a single specialized department (Hand and Foot Surgery) within one hospital, which may limit the generalizability of the findings to other clinical settings or geographic regions.

In conclusion, this study identified three main MRSA strains based on the results of spa typing and MLST typing in the Department of Hand and Foot Surgery: t078–ST25, t437–ST59, and t034–ST398. Our findings demonstrated clonal overlaps between postoperative infection isolates and MRSA colonization among patients, caregivers, and healthcare workers, suggesting the presence of potential in-hospital reservoirs. The results of antibiotic resistance of MRSA strains suggest it is essential to select appropriate antibiotics based on susceptibility test results rather than relying solely on empirical treatment. These findings highlight the importance of active surveillance and targeted infection-control strategies in surgical wards.