Introduction
Staphylococcus aureus was first discovered in the 1880s by Ogston in pus and isolated shortly thereafter by Rosenbach. Over time, through adaptation to the human host and medical environments, S. aureus has evolved into an important opportunistic pathogen for humans. It can asymptomatically colonize various body sites, such as the pharynx, nasal cavity, axillae, and perineum, while also serving as a major cause of skin infections, endocarditis, and bacteremia.1,2 Bacteria have developed complex mechanisms of antibiotic resistance to ensure their survival within the host. The increasing incidence of S. aureus infections has been accompanied by the prevalence of antibiotic-resistant strains, particularly those resistant to methicillin. In the United States, the proportion of infections caused by methicillin-resistant Staphylococcus aureus (MRSA) has steadily increased, now accounting for 60% to 70% of cases. The death toll from MRSA infections has far surpassed the combined deaths caused by acquired immunodeficiency syndrome, tuberculosis, and viral hepatitis.3 In most cases, S. aureus develops antibiotic resistance by acquiring resistance genes. MRSA strains, however, exhibit intrinsic methicillin resistance and increased resistance to conventional antibiotics due to genetic mutations. Given the rapid emergence of antibiotic-resistant S. aureus strains and the lack of new antibiotics in development, there is an urgent need for alternative strategies to combat resistant S. aureus.
Multilocus sequence typing (MLST) technology allows for sequencing analysis of seven housekeeping genes to determine the corresponding sequence types (STs). STs have distinct geographic distribution characteristics; for example, ST5 and ST8 are common in the United States and Japan, while ST80 is widely prevalent in the Middle East.4 MLST in combination with staphylococcal cassette chromosome mec typing has become a critical approach for investigating the global epidemiology of various MRSA clones. A key feature of the pathogenicity of S. aureus is the production of a large number of virulence factors, including secreted proteins, enzymes, and toxins, that are used to establish and sustain infections.5 These virulence factors enable S. aureus to evade host defenses and damage host cells. In the clinical treatment of infectious diseases, MRSA has shown high virulence and resistance to therapy, primarily due to the presence of these virulence factors. Therefore, in-depth studies of virulence factors and their pathogenic mechanisms hold significant potential for advancing the clinical treatment of S. aureus infections.
This study analyzed the distribution and resistance patterns of S. aureus collected from 11 tertiary hospitals in Baotou, Inner Mongolia, China, that participated in the China Antimicrobial Resistance Surveillance System (CARSS) from January 2018 to December 2020. Using MLST to investigate the epidemiological characteristics of all 90 MRSA strains isolated in 2020 from The First Affiliated Hospital of Baotou Medical College, the study aimed to understand the epidemiological and resistance characteristics of S. aureus in this region. Additionally, it examined the presence of 20 virulence genes, including scn, chp, sak, coa, nuc, ebps, eno, cna, tst, and bbp, and their associations with virulence.
Materials and Methods
Materials
Bacterial Strains
Staphylococcus aureus isolates were collected from 11 CARSS member hospitals in Baotou between January 2018 and December 2020. All samples were derived from different patients, resulting in a total of 2453 S. aureus strains. The quality control strain, S. aureus ATCC 25923, was purchased by the National Center for Clinical Laboratories. All 90 MRSA strains isolated in 2020 from The First Affiliated Hospital of Baotou Medical College were selected, and 90 MSSA strains from The First Affiliated Hospital of Baotou Medical College were randomly chosen as controls.
Instruments and Reagents
The bacterial identification and drug susceptibility tests were conducted using the VITEK 2 Compact system (bioMérieux, Craponne, France) or the BD Phoenix-100 system (BD, Mississauga, ON, Canada) with corresponding reagents. MH agar, MH agar containing 5% defibrinated sheep blood, and Columbia blood agar plates were provided by Autobio (Zhengzhou, China). Antimicrobial susceptibility test disks were purchased from Oxoid (Hampshire, UK); E-test strips for penicillin, cefoxitin, linezolid, and vancomycin were obtained from Autobio; and LB broth was obtained from Aobox (Beijing, China).
The bacterial genomic DNA extraction kit was purchased from Tiangen Biotech (Beijing, China). Polymerase chain reaction (PCR) reagents included 2× Taq PCR MasterMix (GreatOcean Biotech, Beijing, China), agarose (Solarbio, Beijing, China), 50× TAE buffer (Solarbio), ethidium bromide staining solution (10 mg/mL; Solarbio), and a 100 bp DNA marker (Solarbio).
Methods
Cultivation and Identification of S. aureus
Isolated bacterial strains were streaked onto Columbia blood agar plates and incubated at 35°C for 24 hours. Bacterial identification was conducted using the VITEK 2 Compact or BD Phoenix-100 system.
Antibiotic Susceptibility Testing
Antibiotic susceptibility tests were performed using the VITEK 2 Compact or BD Phoenix-100 system. For antibiotics not covered by these systems, susceptibility tests were conducted using the Kirby-Bauer disk diffusion method or E-test per Clinical and Laboratory Standards Institute (CLSI) guidelines. The results were interpreted following the 2023 CLSI standards.6
Identification of MRSA
MRSA identification was performed using the cefoxitin disk diffusion method in accordance with CLSI standards.6 Strains with an inhibition zone diameter of ≥22 mm were classified as methicillin-sensitive and those with a diameter of ≤21 mm as methicillin-resistant. The strains confirmed to harbour the mecA gene by PCR.7
Bacterial Genomic DNA Extraction
A single bacterial colony was inoculated into 5 mL of LB broth and incubated at 37°C and 150 rpm for 18 hours. Three milliliters of the bacterial culture were centrifuged at 10,000 rpm (~11,500 ×g) for 1 minute. The pellet was treated with 120 μL of lysostaphin (100 mg/mL) at 37°C for 40 minutes. The specific procedure followed the instructions for the genomic DNA extraction kit, and the extracted DNA was stored in aliquots at 4°C for later use.
MLST
DNA sequences of seven housekeeping genes (arcc, aroe, glpf, gmk, pta, tpi, and yqil) were analyzed according to the MLST website (www.mlst.net). A 25 μL PCR mixture was prepared according to the following composition: 2×TaqPCR MasterMix (12.5 μL), DNA (1 μL), Upstream primer (2 μL), downstream primer (2 μL), ddH2O (7.5 μL), and the PCR cycling conditions were set as step one: pre denaturation (95°C, 5 min, 1 cycle), step two: denaturation (95°C, 30 s), annealing (55°C, 33 s), extension (72°C, 1 min), 35 cycles, step three: final extension (72°C, 5 min), 1 cycles. The PCR products were sent to Great Ocean Biotech (Beijing, China) for bidirectional sequencing. STs were identified using the S. aureus MLST database (https://pubmlst.org/organisms/staphylococcus-aureus).
PCR Detection of Virulence Genes
The primer sequences for the 20 virulence genes were scn, chp, sak, coa, nuc, ebps, eno, cna, bbp, fnbB, clfa, clfb, seb, seh, tst, eta, pvl, LukED, hla, and hld, as previously described.6 The names and functions of each virulence gene are shown in Table 1. Sequence of virulence gene primers are shown in Table 2. A 25 μL PCR mixture was prepared according to the following composition: 2×TaqPCR MasterMix (12.5 μL), DNA (1 μL), Upstream primer (2 μL), downstream primer (2 μL), ddH2O (7.5 μL), and the PCR cycling conditions were set as Table 3.
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Table 1 Name and Function of Virulence Genes
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Table 2 Sequence of Virulence Gene Primers
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Table 3 PCR Cycle Conditions of Virulence Genes
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Statistical Methods
Data analysis was conducted using WHONET 5.6 and SPSS 26.0 software. Categorical data were expressed as counts or percentages, and the χ2 test was performed at a significance level of P<0.05.
Results
Isolation of S. aureus and MRSA
From 2018 to 2020, a total of 24,297 bacterial strains were isolated from 11 CARSS member hospitals in Baotou, including 2453 S. aureus strains, at an isolation rate of 10.1%. These isolates were collected from patients who had cough, fever and other clinical symptoms related to infection and whose peripheral white blood cell and/or neutrophil counts were elevated. The annual isolation rates of S. aureus from 2018 to 2020 were 11%, 10.2%, and 8.9%, respectively. Over the three years, 309 MRSA strains were identified at an isolation rate of 12.6%. The annual isolation rates of MRSA from 2018 to 2020 were 11.7%, 13.7%, and 12.4%, respectively, with the highest rate observed in 2019 and the lowest in 2018 (Table 4). The decrease in SAU separation rate from 2019 to 2020 is statistically significant (P=0.004), indicating a significant decrease in SAU prevalence. The isolation rate of MRSA has significantly increased from 2018 to 2019 (P=0.036).
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Table 4 Isolation of Staphylococcus aureus and Methicillin-Resistant Staphylococcus aureus Strains Between 2018 and 2020
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Specimen Types of S. aureus Infections and MRSA Isolation
The 2453 strains of S. aureus were isolated from various sources, with the majority of strains from wound secretions (932, 38.0%), followed by sputum (462, 18.8%), pus (210, 8.6%), and blood (164, 6.7%). The isolation rates of S. aureus from different specimen types showed statistically significant differences (P<0.05). The highest isolation rate of MRSA was observed in sputum (16.7%) and the lowest in pus (8.6%). The MRSA isolation rates also differed significantly among specimen types (P<0.05). The results are shown in Table 5.
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Table 5 Specimen Types of Staphylococcus aureus Infections and Isolation of Methicillin-Resistant Staphylococcus aureus Strains
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Antibiotic Resistance of MRSA and MSSA to Common Antimicrobial Agents
The resistance rates of MRSA to penicillin, erythromycin, and clindamycin were all greater than 70%. MSSA exhibited high resistance rates to penicillin (90.1%) and erythromycin (70.1%). MRSA demonstrated significantly higher resistance rates to penicillin, clindamycin, tetracycline, and ciprofloxacin than MSSA (P<0.05). No strains resistant to vancomycin, linezolid, or teicoplanin were detected (Table 6).
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Table 6 Resistance of Methicillin-Resistant and Methicillin-Sensitive Staphylococcus aureus to Common Antimicrobial Agents
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Antibiotic Resistance of MRSA in Different Specimen Types
In all specimen types, MRSA demonstrated resistance rates exceeding 70% to penicillin, erythromycin, and clindamycin. Resistance rates to rifampin were below 22% across specimen types. Ciprofloxacin resistance was highest in strains isolated from blood specimens (43.8%) and lowest in strains from pus (4.5%). Gentamicin resistance was highest in strains from sputum (32.5%) and lowest in strains from secretions (18.7%). The resistance rates of MRSA to ciprofloxacin, gentamicin, levofloxacin, moxifloxacin, and rifampin varied significantly among specimen types (P<0.05). The results are shown in Table 7.
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Table 7 Resistance of Methicillin-Resistant Staphylococcus aureus to Common Antimicrobial Agents in Different Types of Specimens
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MLST of MRSA
MLST analysis of 90 MRSA strains identified eight STs. The predominant STs were ST59 (54, 60%), ST398 (11, 12.2%), ST239 (7, 7.8%), ST22 (7, 7.8%), ST25 (5,5.6%), ST5 (2,2.2%), ST188 (2,2.2%), ST7 (2,2.2%).
MLST of MRSA Associated with Different Infection Types
When the STs of the 90 MRSA strains were grouped by infection types, ST59 was mainly associated with surgical infections (66.7%, 36/54), followed by respiratory infections (12.5%, 7/54) and other infections (12.5%, 7/54). ST59 strains predominantly originated from orthopedic hand, foot, and ankle surgeries; ostomy wound clinics; and trauma departments. Two ST5 strains were linked to respiratory infections, while two ST188 strains and two ST7 strains were associated with other infections (Table 8).
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Table 8 Multilocus Sequence Typing of Methicillin-Resistant Staphylococcus aureus with Different Infection Types
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Detection of Virulence Genes in MRSA and MSSA
Among the 20 virulence genes tested in 90 MRSA and 90 MSSA strains, all strains carried the hla, hld, nuc, clfa, and clfb genes. Over 90% of the strains carried the sak, scn, and coa genes, among which the coa gene showed a 100% detection rate in MSSA strains. Only 12 strains carried the seh gene, seven carried the bbp gene, four carried the tst gene, and two MRSA strains carried the eta gene. Two MRSA strains each carried 17 virulence genes, while five MSSA strains each carried 14 virulence genes. The detection rate of the fnbB gene was significantly (P<0.05) higher in MSSA (83%) than in MRSA (15%). The detection rate of the ebps gene was 6% in both MRSA and MSSA (Figure 1).
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Figure 1 Virulence Genes in Methicillin-Resistant and Methicillin-Sensitive Staphylococcus aureus.
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Detection of Virulence Genes in Different Types of S. aureus Infections
The virulence genes of 180 strains of Staphylococcus aureus were grouped according to infection type. The bbp, seh, and LukED genes were only present in strains isolated from surgical and bloodstream infections, the tst gene was only present in strains isolated from surgical and respiratory infections, and the eta gene was only detected in strains isolated from other infections. The detection rate of the chp gene in surgical infections (82%) was higher than that in bloodstream infections (50%), P<0.05. The detection rate of the PVL gene in bloodstream infections (50%) was higher than that in surgical infections (18%), P<0.05. The detection rate of the LukED gene in surgical infections (45%) and bloodstream infections (40%) was higher than that in respiratory infections (0%), P<0.05. See Table 9.
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Table 9 Detection of Virulence Genes of Staphylococcus aureus in Different Infection Types
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Detection of Virulence Genes in Different ST Types of MRSA
The virulence genes of 90 MRSA strains were grouped according to ST type. The ebps, bbp, and tst genes were only detected in ST59 type, with detection rates of 25%, 4%, and 4%, respectively. ST398 did not detect seh, and the seb detection rate was only 20%. The detection rate of the PVL gene in ST59 type was 33%, and the detection rate in ST22 type was 67%. ST59 and ST398 MRSA carried at least 10 virulence genes, while ST239 MRSA carried at least 11 virulence genes. See Table 10.
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Table 10 Detection of MRSA Virulence Genes in Different ST Types
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Discussion
Staphylococcus aureus can be carried by patients both prior to and following hospital admission. As a common commensal organism in humans and animals, it is capable of colonizing the nares, axillae, perineum, skin, and numerous other bodily sites. Approximately 15% of the general population is estimated to be persistent carriers of S. aureus in the anterior nares. Patients may already be carriers of S. aureus upon hospital entry; furthermore, they can acquire the bacterium during their inpatient stay, particularly when undergoing surgical interventions or other invasive procedures. Methicillin-resistant Staphylococcus aureus (MRSA) is widely recognized as a dominant nosocomial pathogen, responsible for significant morbidity and mortality on a global scale. MRSA colonization not only elevates the risk of subsequent infection but also contributes to healthcare-associated transmission.2,8
The China Antimicrobial Resistance Surveillance System (CARSS) was established in 2005 and is responsible for monitoring the sensitivity and resistance rates of common clinical pathogens in China to various antibiotics, as well as continuously monitoring the changes in bacterial resistance. A total of 11 tertiary hospitals in Baotou, Inner Mongolia participated in CARSS. We analyzed the data uploaded to CARSS from 2018 to 2020, a total of 2453 S. aureus strains were isolated in Baotou at an isolation rate of 10.1%, significantly lower than the 32.9% observed in the 2020 China Antimicrobial Surveillance Network.9 The isolation rate of S. aureus in Baotou decreased from 11% in 2018 to 8.9% in 2020, as did that in southern China (9.9–9.5%)10 but not that in northwest China, which showed a significant increase (3.7–9.7%).11 The decline in S. aureus isolation rate in 2020 may be related to the COVID-19 pandemic, which led to a reduction in both inpatient and outpatient cases compared to 2019 and consequently fewer specimens, particularly from outpatients.
The incidence of MRSA in Asia is much higher than in other parts of the world,12 with isolation rates in Asia ranging from 28% to 70%.13 In comparison, the average isolation rates of MRSA in Ireland and Canada are 2.2% and 11.8%, respectively.14 In our study, the isolation rates of MRSA from 2018 to 2020 were 11.7%, 13.7%, and 12.4%, respectively, showing no obvious trend, but lower than the results reported by the previous team in 2019.15 The average isolation rate of MRSA was 12.6%, slightly higher than that in Canada but significantly lower than that in Asia (46.9%) and other regions of China (31.6%).16,17 This rate is below the national average reported by the CARSS but close to the average in the Inner Mongolia Autonomous Region (CARSS 2020 National Antimicrobial Resistance Surveillance Report, http://www.carss.cn/Report/Details?aId=808). These findings indicate that the isolation rates of S. aureus and MRSA in Baotou are relatively low.
In the previous study by our team, only the drug resistance analysis of the isolated strains was conducted,15 and the sample sources were not distinguished. In this study, a detailed subdivision was carried out. The 2453 strains of S. aureus in this experiment were derived from secretions, sputum, pus, and blood. Among them, the proportion of Staphylococcus aureus in wound secretions was 38.0%, which was higher than that in other specimen types (P<0.05), consistent with the conclusion of He et al.18 The highest isolation rate of MRSA was observed in sputum (16.7%), which was significantly (P<0.05) higher than that in blood (12.2%), in which the second-highest isolation rate was observed. As these results suggest that surgical operations are the primary source of S. aureus infections, MRSA should be considered in the diagnosis of clinical pulmonary and bloodstream infections, especially as severe cases of bloodstream MRSA infections can be life-threatening.
Antibiotic susceptibility analysis of MRSA and MSSA revealed that MRSA had a resistance rate of 73.1% to clindamycin, higher than the results reported by Weiner et al (56.2%)19 and the 2020 CHINET surveillance of bacterial resistance (58.6%). MRSA showed higher resistance rates to penicillin and clindamycin compared to MSSA. These results suggest that although the MRSA isolation rate in Baotou is low, resistance rates to certain antibiotics exceed the national averages. Therefore, clinicians should use antibiotics judiciously, ensuring that empirical treatment aligns with local surveillance data to guide the appropriate selection of antimicrobial agents.
The resistance rates of MRSA to ciprofloxacin, gentamicin, levofloxacin, moxifloxacin, and rifampin varied significantly among the specimen types. Notably, MRSA isolates from blood samples exhibited the highest resistance rate to ciprofloxacin, while those from pus samples demonstrated the lowest. Similarly, gentamicin resistance rate was highest in MRSA strains from sputum and lowest in those from wound secretions. These variations reflect the heterogeneity of S. aureus in antibiotic resistance and virulence systems, which are closely linked to host conditions, treatment regimes, and infection severity. Therefore, clinical treatment strategies should be tailored based on specimen type and resistance profiles to avoid the overuse of antimicrobial agents, which could lead to the proliferation of resistant strains.
In previous studies by our team, only drug resistance monitoring was conducted, without molecular epidemiological and virulence mechanism studies on the isolated S. aureus.15 Based on the previous findings, our team has carried out further research. The MLST analysis of 90 MRSA strains identified eight STs, including ST59, ST398, ST239, ST22, ST25, ST5, ST188, and ST7. Among them, ST59 was the predominant type, representing 60.0% of the isolates, consistent with the findings of Cui et al (63.7%).20 ST59 was first reported in Taiwan in 2004 and has since evolved into one of the most prevalent STs in East Asia. Although ST59 has also been reported in Europe and North America, it remains uncommon in those regions. In Taiwan, ST59 accounts for 56% of CA-MRSA infections in children, and ST59-related sepsis has been observed in nearly 70% of pediatric CA-MRSA infections. Furthermore, 66.7% of ST59 infections in our study were linked to surgical operations, primarily in orthopedic hand, foot, and ankle surgeries; ostomy wound clinics; and trauma departments, indicating that skin and soft tissue remain the primary sites of ST59 infections.
The virulence factors of S. aureus are crucial during pathogenesis.21,22 Consistent with most studies from mainland China,23,24 nearly all strains in our study carried the hla, hld, nuc, clfa and clfb genes, confirming these as the most common virulence factors in S. aureus and indicating no regional variation in their distribution. Over 90% of the strains carried the sak, scn, and coa genes. Only 12 strains carried the seh gene, seven carried the bbp gene, four carried the tst gene, and two MRSA strains carried the eta gene. The detection rate is lower than that reported by Li et al.25 Two MRSA strains each carried 17 virulence genes, while five MSSA strains each carried 14 virulence genes.
The detection rate of the fnbB gene was significantly higher in MSSA (83%) than in MRSA (15%). The fibronectin-binding proteins expressed by fnbA and fnbB act as mediators for cell signaling and actin cytoskeleton rearrangement and facilitate the invasion of S. aureus into tissues. The fnbB gene is frequently detected in strains from keratitis, osteomyelitis, medical device surfaces, and orthopedic infections. In the current study, the detection rate of fnbB was 49%, which is consistent with the 43.6% detection rate reported by Soltani et al26 but higher than the 29.5% detection rate reported in a study on bloodstream infections.27 These findings indicate that fnbB exhibits heterogeneity in detection rates across specimen types. Contrary to previous studies showing higher biofilm production and fnbA/fnbB expression in MRSA strains compared to MSSA,28 we found a significantly higher fnbB detection rate of 83% in MSSA than 15% in MRSA (P<0.05). Further investigation is needed to determine whether this difference is related to variable expression of biofilm-associated genes and regulatory elements in MRSA genomes.
The detection rate of the bbp gene in the current study was only 4%, consistent with the findings of Kot et al.29 Previous studies have shown that S. aureus strains carrying the bbp gene have a greater ability to produce biofilms than those with other biofilm-related genes, although its low prevalence limits further research. The bbp gene encodes a protein with high affinity for bone sialoprotein and has been linked to hematogenous osteomyelitis and arthritis. These factors explain its detection in three patients in the present study, including two with lumbar spinal stenosis and one with acute osteomyelitis.
Panton-Valentine leukocidin is an endogenous factor in clinical infections that exerts significant cytotoxic effects on neutrophils. As the reported positivity rate of the pvl gene ranges from 2% to 35%, the 29% positivity rate in the present study is close to the upper limit. Elevated pvl expression increases MRSA virulence, causing necrotizing pneumonia with mortality rates as high as 75%.30 Our study found that the detection rate of pvl was significantly higher (P<0.05) in S. aureus strains from bloodstream infections (50%) than those from surgical infections (18%), suggesting that the pvl gene is frequently associated with deep infections. Additionally, the pvl gene was slightly more prevalent in MRSA (33%) than in MSSA (25%). Early studies suggested that the pvl gene was a genetic marker for MRSA identification. However, Motamedi et al31 found no significant association between pvl and mecA in S. aureus, and MSSA may secrete a relatively high level of toxins, particularly Panton-Valentine leukocidin.32 Leukocidin ED induces the death of neutrophils and lymphocytes by forming oligomeric pore-like structures.
The chp, sak, and scn genes are specific to and commonly found in S. aureus strains derived from humans.33 In our study, the prevalence rates of chp, sak, and scn were 79%, 90%, and 94%, respectively, which supports this conclusion. Additionally, the detection rate of chp was significantly higher (P<0.05) in S. aureus strains from surgical infections (82%) than those from bloodstream infections (50%).
Conclusions
This study reveals distinct epidemiological and molecular characteristics of S. aureus and MRSA in the region. While isolation rates are lower than national averages, elevated resistance to key antibiotics underscores the need for tailored antimicrobial stewardship. Clinical management should account for source-specific resistance patterns, particularly given MRSA’s higher resistance across most antibiotics and its predominance in respiratory specimens. The dominance of the ST59 lineage—strongly associated with healthcare-associated skin and soft tissue infections in high-risk surgical settings (orthopedics, trauma, wound care)—demands intensified infection control in these units, including strict antisepsis protocols, environmental decontamination, and preoperative MRSA screening.
Notably, the near-universal carriage of virulence genes (hla, hld, nuc, clfa, clfb, sak, scn, coa) among isolates indicates significant pathogenic potential, amplifying concerns for severe surgical site infections or outbreaks. Public health efforts must prioritize surveillance of these hypervirulent strains, especially in vulnerable surgical populations. The stark contrast in fnbB gene prevalence between MSSA (83%) and MRSA (15%) warrants investigation into its role in adhesion or immune evasion. Future studies should: (1) expand regional surveillance to track ST59 spread and virulence gene distribution; (2) correlate ST59 infections with clinical outcomes (eg, treatment failure, mortality); and (3) evaluate targeted decolonization protocols in high-risk surgical cohorts to mitigate ST59-associated infections.
Abbreviations
CA, community-acquired; CARSS, China Antimicrobial Resistance Surveillance System; CC, clonal complex; CLSI, Clinical and Laboratory Standards Institute; CNA, collagen-binding adhesin; HA, hospital-acquired; MLST, Multilocus sequence typing; MRSA, methicillin-resistant Staphylococcus aureus; MSSA, methicillin-sensitive Staphylococcus aureus; PCR, Polymerase chain reaction; SAU, Staphylococcus aureus; ST, sequence type.
Data Sharing Statement
Experimental data related to this study are available from the corresponding author upon reasonable request.
Ethics Approval and Consent to Participate
This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the Ethics Committee of The First Affiliated Hospital of Baotou Medical College, Inner Mongolia University of Science & Technology (2025-1-20/K018-01). The data are anonymous, and the requirement for informed consent was therefore waived.
Acknowledgments
The authors would like to express their gratitude to all staff members of the Clinical Microbiology Laboratory of The First Affiliated Hospital of Baotou Medical College, Inner Mongolia University of Science & Technology for their support.
Author Contributions
All authors made a significant contribution to the work reported, whether that is in the conception, study design, execution, acquisition of data, analysis and interpretation, or in all these areas; took part in drafting, revising or critically reviewing the article; gave final approval of the version to be published; have agreed on the journal to which the article has been submitted; and agree to be accountable for all aspects of the work.
Funding
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Disclosure
The authors declare no competing interests.
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