ABSTRACT
Background and Aims
Methicillin‐resistant Staphylococcus aureus (MRSA) is a significant pathogen associated with hospital‐acquired infections, with its global prevalence, including in Indonesia, steadily increasing. However, comprehensive data on MRSA prevalence and antimicrobial susceptibility within Indonesian hospital settings remain limited. This study aimed to assess the prevalence of MRSA and its antimicrobial susceptibility profile among clinical samples isolated from Indonesian patients.
Methods
A cross‐sectional, descriptive‐analytic study was conducted over a 3‐year period (January 2022–December 2024). The study population consisted of clinical specimens obtained from both inpatients and outpatients recorded at the Microbiology Laboratory. MRSA isolates were identified using standard microbiological techniques, and antimicrobial susceptibility testing was performed according to the Clinical and Laboratory Standards Institute (CLSI) guidelines. The multidrug resistance (MDR) profile was determined based on resistance to at least three different antibiotic classes.
Results
Among the clinical samples analyzed (279 S. aureus), MRSA was detected in 258 (92.47%). The highest prevalence was observed in pus samples (77.8%). MRSA and methicillin‐sensitive S. aureus (MSSA) isolates exhibited high susceptibility to Quinupristin/Dalfopristin (98.1% and 100%), Linezolid (96.9% and 95.2%), Vancomycin (93% and 100%), Tigecycline (98.4% and 100%), Nitrofurantoin (98.4% and 100%), and Rifampicin (96.1% and 100%). MDR‐MRSA strains accounted for 55% of all MRSA isolates, a notably higher proportion compared to the 19% observed in MSSA.
Conclusion
The study highlights a notable prevalence of MRSA and MDR‐MRSA among clinical isolates in Semarang, coupled with a concerning level of multidrug resistance. Although certain antibiotics remain effective against MRSA, the findings emphasize the necessity for continuous surveillance and antimicrobial stewardship programs. Strengthened infection control measures and optimized antibiotic management strategies are crucial to mitigating MRSA spread and preserving effective treatment options within Indonesian healthcare settings.
Keywords: antimicrobial resistance, clinical samples, hospital acquired infections, methicillin‐resistant Staphylococcus aureus (MRSA), multidrug resistance
1. Introduction
Methicillin‐resistant Staphylococcus aureus (MRSA) is a significant public health concern worldwide, particularly in healthcare settings where it causes a wide range of infections, from mild skin and soft tissue infections to life‐threatening conditions such as pneumonia, bloodstream infections, and sepsis [1, 2, 3, 4, 5]. The ability of S. aureus to acquire resistance mechanisms, particularly to β‐lactam antibiotics, has led to the emergence of MRSA, making treatment more challenging [6, 7, 8]. Over time, MRSA has developed resistance to multiple classes of antibiotics, leading to the rise of multidrug‐resistant MRSA (MDR‐MRSA), which further limits therapeutic options, leading to increased morbidity, mortality, and increased healthcare costs [1, 9, 10].
The global burden of MRSA varies significantly across regions, with a reported prevalence rate of 37% in India [11], 32.5% in Ethiopia [12], 41% in central Vietnam [13], 11.9%–38% [14] in Saudi Arabia [15], and 26.4% in Nepal [16]. In Southeast Asia, including Indonesia, MRSA infections have been increasingly recognized as a serious threat [17]. However, there is limited comprehensive data on the prevalence, antimicrobial resistance patterns, and multidrug resistance profiles of MRSA isolates in Indonesian healthcare facilities. Existing studies have primarily focused on small sample sizes or specific hospital settings [18, 19, 20], leaving a critical gap in understanding the broader epidemiology of MRSA in Indonesia.
Antimicrobial resistance (AMR) is a growing problem that threatens global public health [21, 22], and Indonesia is no exception. The overuse and misuse of antibiotics, inadequate infection control measures, and limited antibiotic stewardship programs contribute to the increasing prevalence of antibiotic‐resistant pathogens, including MRSA. The presence of MDR‐MRSA, defined as MRSA strains resistant to three or more classes of antibiotics, poses an even greater challenge, as it significantly reduces treatment options and increases the likelihood of treatment failure [23, 24].
Understanding the resistance patterns of MRSA isolates is crucial for guiding effective treatment strategies and developing targeted interventions to mitigate its spread. Therefore, this study aims to investigate the prevalence of MRSA among clinical samples obtained from healthcare settings in Indonesian patients, evaluate its antimicrobial resistance profile, and assess the extent of multidrug resistance. By utilizing a cross‐sectional study design, MRSA isolates from various clinical sources, including blood, sputum, wound swabs, and other body fluids, will be analyzed to determine their resistance patterns against commonly used antibiotics.
2. Methods
2.1. Study Design, Setting, and Duration
This cross‐sectional observational study was conducted over a 3‐year period, from January 1, 2022 to December 31, 2024, at a provincial healthcare facility in Indonesia.
2.2. Study Site and Justification
The study was conducted at the Microbiology Laboratory of Dr. Adhyatma Hospital, a provincial healthcare facility in Central Java, Indonesia that receives referred and complicated cases from surrounding primary care facilities, in addition to routine inpatient and outpatient services. The hospital is equipped with comprehensive microbiological testing capabilities and adequate research facilities, making it a suitable site for this investigation.
2.3. Sample Size and Sampling Technique
A total of 2795 clinical samples were included using a non‐probability purposive sampling method. A consecutive sample satisfying the inclusion criteria and were collected for the study.
2.4. Sample Population and Selection Criteria
Figure 1 presents the sample inclusion and exclusion criteria. The study population consisted of clinical specimens obtained from both inpatients and outpatients at the Microbiology Laboratory, totaling 2175 samples. Among these, 279 S. aureus isolates were identified from 279 S. aureus‐infected patients, with each patient contributing one isolate. Repeat isolates from the same patient during the study period were excluded; only the first culture‐positive S. aureus isolate per patient was included, ensuring that each of the 279 isolates represents a unique patient.
Figure 1.
Flow diagram of sample inclusion and exclusion criteria.
This study focused on S. aureus isolates, including methicillin‐resistant S. aureus (MRSA) and methicillin‐sensitive S. aureus (MSSA), as the primary outcome variable. Predictor variables included patient age, gender, specimen type, and antibiotic susceptibility profiles.
2.5. Specimen Collection, Isolation, Identification, and Antimicrobial Susceptibility Testing
Data for this study were collected retrospectively from the records of the Microbiology Laboratory. These records documented microbiological procedures, including specimen collection, bacterial isolation, identification, and antimicrobial susceptibility testing.
2.6. Specimen Collection and Culturing
Specimens were collected following standardized protocols to ensure sample integrity. Each specimen was inoculated onto blood agar and incubated at 37°C ± 2°C for 18–24 h to promote bacterial growth.
2.7. Bacterial Isolation and Identification
Significant bacterial growth on culture plates was further processed for identification. The isolated bacteria were characterized based on colony morphology, including type, margin, elevation, size, shape, and color. Identification was performed using the VITEK2 Compact system (bioMérieux, Craponne, France), which automates bacterial identification and antimicrobial susceptibility testing.
2.8. Antimicrobial Susceptibility Testing
Antimicrobial susceptibility testing (AST) was performed exclusively using the VITEK2 Compact automated system (AST‐GP card; bioMérieux), which generates minimum inhibitory concentrations (MICs) that were interpreted as susceptible, intermediate, or resistant according to CLSI (2018) breakpoints [25]. Methicillin resistance was determined using cefoxitin susceptibility as the definitive screening criterion, in accordance with CLSI recommendations, because cefoxitin is a more sensitive and reliable surrogate marker for mecA‐mediated resistance than oxacillin, particularly for detecting isolates with oxacillin heteroresistance. Isolates were classified as MRSA when categorized as cefoxitin‐resistant, irrespective of the oxacillin result; discordant cefoxitin‐resistant/oxacillin‐susceptible isolates (a recognized phenotype attributable to heteroresistant mecA expression) were classified as MRSA on the basis of the cefoxitin result.
A total of 17 antibiotics were tested against S. aureus, covering multiple antibiotic classes: penicillins (BEN: benzylpenicillin, OXA: oxacillin), 3rd‐generation cephalosporins (CTX: cefotaxime), aminoglycosides (GM: gentamicin), fluoroquinolones (CIP: Ciprofloxacin, LEV: levofloxacin, MXF: moxifloxacin), macrolides (ERY: erythromycine rythromycin); lincosamides (DA: clindamycin), Quinupristin/Dalfopristin (QDA), oxazolidinones (LNZ: linezolid), glycopeptides (VAN: vancomycin), tetracyclines (TET: tetracycline), glycylcyclines (TGC: tigecycline), nitrofurans(NIT); rifamycin (RIF: rifampicin), and sulfonamides‐trimethoprim (SXT: trimethoprim + sulfamethoxazole).
2.9. Multidrug Resistance: Definition, Grouping, and Classification of Antimicrobial Agents
Table 1 presents the grouping and classification of antimicrobial agents for MDR. Multidrug resistance (MDR) was defined as nonsusceptibility to ≥ 1 agent in ≥ 3 antimicrobial categories [26]. For the MDR, one or more of these drugs have been applied. An MRSA is always considered MDR by virtue of being an MRSA; Nonsusceptibility to ≥ 1 agent in ≥ 3 antimicrobial categories
Table 1.
Classification and grouping of antimicrobial drugs.
| Antimicrobial category | Antimicrobial agent | Results of antimicrobial susceptibility (S or NS) |
|---|---|---|
| Aminoglycoside | Gentamicin | |
| Ansamycins | Rifampin/rifampicin | |
| Anti‐MRSA cephalosporins | Ceftraroline | |
| Anti‐staphlyllococcal beta lactams (for cephamycins) | Oxacillin (or cefoxitin) | |
| Fluoroquinolone |
|
Quality assurance: To ensure the reliability of the study findings, standard microbiological procedures were strictly followed, as outlined by the CLSI guideline, 2018 [25]. Quality control was implemented by using S. aureus ATCC 6538 and E. coli ATCC 25922 as control strains on the VITEK2 Compact system.
2.10. Data Processing and Analysis
Data were systematically coded, entered, and analyzed using the Statistical Package for Social Sciences (SPSS) software, version V.26 (SPSS, Chicago, Illinois, USA). Descriptive statistics were presented as frequencies and percentages for categorical variables. Continuous data were summarized as mean ± standard deviation (SD). Frequency tables were generated for categorical data. For comparison of categorical variables, the χ 2 test was used, with Fisher's exact test applied when necessary. Multivariable regression analysis was not performed, as none of the demographic or clinical variables (gender, age group, specimen type) showed a statistically significant association with MRSA/MSSA status in bivariate analysis (all p > 0.05); multivariable modeling was therefore not considered appropriate for this dataset.
All analyses were performed with a 95% confidence interval (CI) and a 5% margin of error. All tests were two tailed, and a p‐value of < 0.05 was considered statistically significant.
2.11. Ethical Consideration
The study was conducted in accordance with the Declaration of Helsinki. The study protocol was approved by the ethics committee of Dr. Adhyatma Hospital, with ethical clearance no. 082/KEPK. EC/VI/2022.
3. Results
Table 2 summarizes the demographic characteristics and sample distribution among the study participants. A total of 2795 clinical samples were collected, from which S. aureus was identified in 279 cases (10%). Among the S. aureus‐positive cases, 145 (51.9%) were male, and 134 (48.0%) were female, indicating a nearly equal distribution between genders.
Table 2.
Demographic characteristics of the study population.
| Parameters | Inference |
|---|---|
| Total clinical samples, n | 2795 |
| S. aureus, n (%) | 279 (100.0) |
| Gender | |
| Male | 145 (51.9) |
| Female | 134 (48.0) |
| Types of samples, n (%) | |
|
217 (77.0) |
|
18 (6.5) |
|
17 (6.1) |
|
5 (1.8) |
|
22 (7.9) |
Regarding sample types, pus was the most frequently isolated specimen, accounting for 217 (77.8%) of the S. aureus cases. Other specimen types included sputum (7.9%), blood (6.5%), body fluid (6.1%), and urine (1.8%).
Table 3 presents the prevalence of S. aureus, including its methicillin‐resistant (MRSA) and methicillin‐sensitive (MSSA) strains, among the 279 research participants. The overall prevalence of MRSA was 92.5% (n = 258), with a 95% confidence interval (CI) ranging from 89.2% to 95.3%. In contrast, MSSA accounted for only 7.5% (n = 21) of the isolates, with a CI of 4.7% to 10.8%.
Table 3.
Prevalence of Staphylococcus aureus, MRSA, and MSSA.
| S. aureus (n = 279) | Prevalence | CI 95% (LL‐UL) | ||
|---|---|---|---|---|
| LL | UL | |||
| MRSA | n = 258 | 92.5% | 89.2 | 95.3 |
| MSSA | n = 21 | 7.5% | 4.7 | 10.8 |
Abbreviations: MRSA, methicillin‐resistant Staphylococcus aureus; MSSA, methicillin‐sensitive Staphylococcus aureus.
Table 4 presents the correlation between S. aureus, categorized as methicillin‐resistant S. aureus (MRSA) and methicillin‐sensitive S. aureus (MSSA), among 279 research participants in relation to demographic variables and clinical specimen types.
Table 4.
Correlation of S. aureus (characterized as MRSA and MSSA) among research participants with demographic variables and other clinical specimens.
| Variable | Type of S. aureus, n = 279 | ||
|---|---|---|---|
| MRSA | MSSA | p value (χ 2 ) | |
| Gender | |||
| Male 145 (51.9) | 137 (53.1%) | 8 (38.1%) | 0.136 |
| Female 134 (48.03) | 121 (46.9%) | 13 (61.9%) | |
| Age groups, years | |||
| Children (0–14 years) | 27 (10.5%) | 3 (14.3%) | 0.821 |
| Youth (15–24 years) | 27 (10.5%) | 1 (4.8%) | |
| Adults (25–64 years) | 182 (70.5%) | 15 (71.4%) | |
| Seniors (65 years and over) | 22 (8.5%) | 2 (9.5%) | |
| Specimen type | |||
| Pus | 201 (77.9%) | 16 (76.2%) | 0.572 |
| Blood | 16 (6.2%) | 2 (9.5%) | |
| Body fluid | 17 (6.6%) | 0 (0%) | |
| Urine | 4 (1.6%) | 1 (4.8%) | |
| Sputum | 20 (7.8) | 2 (9.5%) | |
Among the participants, 145 (51.9%) were male, with MRSA detected in 137 (53.1%) and MSSA in 8 (38.1%). Females constituted 134 (48.0%) of the total, with MRSA in 121 (46.9%) and MSSA in 13 (61.9%). However, the association between gender and S. aureus type was not statistically significant (p = 0.136).
Regarding age distribution, the majority of S. aureus isolates were from adults aged 25–64 years (70.5%), followed by children (0–14 years, 10.5%), youth (15–24 years, 10.5%), and seniors (≥ 65 years, 8.5%). The proportion of MRSA and MSSA was relatively similar across age groups, with no significant correlation observed (p = 0.821).
In terms of specimen type, pus was the most common source of S. aureus isolates, accounting for 217 (77.8%) cases, with 201 (77.9%) identified as MRSA and 16 (76.2%) as MSSA. Other sources included blood (6.4%), body fluid (6.1%), sputum (7.9%), and urine (1.8%). The distribution of MRSA and MSSA across specimen types did not show significant variation (p = 0.572).
Table 5 presents the antimicrobial susceptibility profiles of S. aureus isolates (n = 279) against a range of antibiotics. The data highlight high resistance rates to β‐lactam antibiotics, particularly benzylpenicillin (92.5%), oxacillin (33%), and cefotaxime (42.7%). Among aminoglycosides and fluoroquinolones, resistance to gentamicin was observed in 19% of isolates, while ciprofloxacin, levofloxacin, and moxifloxacin exhibited resistance rates of 33.4%, 36.6%, and 22.3%, respectively. Macrolide and lincosamide resistance was relatively low, with erythromycin and clindamycin resistance observed in 15.4% and 14.7% of isolates, respectively. The streptogramin combination quinupristin/dalfopristin showed the highest susceptibility rate (98.2%).
Table 5.
Susceptibility profiles of Staphylococcus aureus isolates.
| Antibiotics | S. aureus. n = 279 | |
|---|---|---|
| Resistant | Sensitive | |
| Benzylpenicillin (BEN) | 258 (92.5%) | 21 (7.5%) |
| Oxacillin (OXA) | 91 (33%) | 188 (67%) |
| Cefotaxime (CTX) | 119 (42.7%) | 160 (57.3%) |
| Gentamicin (GM) | 53 (19%) | 226 (81%) |
| Ciprofloxacin (CIP) | 93 (33.4%) | 186 (66.7%) |
| Levofloxacin (LEV) | 102 (36.6%) | 177 (63.4%) |
| Moxifloxacin (MFX) | 62 (22.3%) | 217 (77.8%) |
| Erythromycin (ERY) | 43 (15.4%) | 236 (84.6%) |
| Clindamycin (DA) | 41 (14.7%) | 238 (85.3%) |
| Quinupristin/dalfopristin (QDA) | 5 (1.8%) | 274 (98.2%) |
| Linezolid (LNZ) | 9 (3.2%) | 270 (96.8%) |
| Vancomycin (VA) | 18(6.5%) | 261 (93.5%) |
| Tetracycline (TET) | 114 (40.9) | 165 (59.1%) |
| Tigecycline (TGC) | 4 (1.4%) | 275 (98.6%) |
| Nitrofurantoin (NIT) | 4 (1.4%) | 275 (98.6%) |
| Rifampicin (RIF) | 10 (3.6%) | 269 (96.4%) |
| Trimethoprim/sulfamethoxazole (SXT) | 46 (16.5%) | 233 (83.5%) |
Notably, resistance to vancomycin, linezolid, and rifampicin remained low at 6.5%, 3.2%, and 3.6%. Tigecycline and nitrofurantoin demonstrated the highest susceptibility rates (98.6%), while trimethoprim/sulfamethoxazole maintained an 83.5% susceptibility rate.
The antibiotic resistance profile of 279 S. aureus isolates, including 258 methicillin‐resistant S. aureus (MRSA) and 21 methicillin‐susceptible S. aureus (MSSA), was assessed against various antimicrobial agents (Table 6). The results reveal significant differences in resistance patterns between MRSA and MSSA strains.
Table 6.
Antibiotic resistance profile of MRSA and MSSA to different antimicrobial agents.
| Antibiotics | S. aureus, n = 279 | |
|---|---|---|
| MRSA, n = 258 (92.47%) | MSSA, n = 21 (7.53%) | |
| Benzylpenicillin (BEN) | ||
| Resistant | 258 (100%) | 0 (0.0%) |
| Sensitive | 0 (0.0%) | 21 (100%) |
| Oxacillin (OXA) | ||
| Resistant | 91 (35.3%) | 0 (0.0%) |
| Sensitive | 167 (64.7%) | 21 (100%) |
| Cefotaxime (CTX) | ||
| Resistant | 111 (43%) | 8 (38.1%) |
| Sensitive | 147 (57%) | 13 (61.9%) |
| Gentamicin (GM) | ||
| Resistant | 53 (20.5%) | 0 (0%) |
| Sensitive | 205 (79.5%) | 21 (100%) |
| Ciprofloxacin (CIP) | ||
| Resistant | 88 (34.1%) | 5 (23.8%) |
| Sensitive | 170 (65.9%) | 16 (76.2%) |
| Levofloxacin (LEV) | ||
| Resistant | 96 (37.2%) | 6 (28.6%) |
| Sensitive | 162 (62.8%) | 15 (71.4%) |
| Moxifloxacin (MFX) | ||
| Resistant | 60 (23.3%) | 2 (2.5%) |
| Sensitive | 198 (76.7%) | 19 (90.5%) |
| Erythromycin (ERY) | ||
| Resistant | 41 (15.9%) | 2 (9.5%) |
| Sensitive | 217 (84.1%) | 19 (90.5%) |
| Clindamycin (DA) | ||
| Resistant | 39 (15.1%) | 2 (9.5%) |
| Sensitive | 219 (84.9%) | 19 (90.5%) |
| Quinupristin/Dalfopristin (QDA) | ||
| Resistant | 5 (1.5%) | 0 (0.0%) |
| Sensitive | 253 (98.1%) | 21 (100%) |
| Linezolid (LNZ) | ||
| Resistant | 8 (3.1%) | 1 (4.8%) |
| Sensitive | 250 (96.9%) | 20 (95.2%) |
| Vancomycin (VA) | ||
| Resistant | 18 (7%) | 0 (0.0%) |
| Sensitive | 240 (93%) | 21 (100%) |
| Tetracycline (TET) | ||
| Resistant | 113 (43.8%) | 1 (4.8%) |
| Sensitive | 145 (56.2%) | 20 (95.2%) |
| Tigecycline (TGC) | ||
| Resistant | 4 (1.6%) | 0 (0%) |
| Sensitive | 254 (98.4%) | 21 (100%) |
| Nitrofurantoin (NIT) | ||
| Resistant | 4 (1.6%) | 0 (0.0%) |
| Sensitive | 254 (98.4%) | 21 (100%) |
| Rifampicin (RIF) | ||
| Resistant | 10 (3.9%) | 0 (0.0%) |
| Sensitive | 248 (96.1%) | 21 (100%) |
| Trimethoprim/Sulfamethoxazole (SXT) | ||
| Resistant | 45 (17.4%) | 1 (4.8%) |
| Sensitive | 213 (82.6%) | 20 (95.2%) |
All MRSA isolates (100%) exhibited resistance to benzylpenicillin (BEN), whereas all MSSA isolates remained susceptible. Resistance to oxacillin (OXA) was observed in 35.3% of MRSA isolates, while all MSSA isolates were susceptible. Similarly, cefotaxime (CTX) resistance was noted in 43% of MRSA isolates and 38.1% of MSSA isolates.
Gentamicin (GM) resistance was detected in 20.5% of MRSA isolates, whereas all MSSA isolates were sensitive. Ciprofloxacin (CIP) resistance was identified in 34.1% of MRSA isolates and 23.8% of MSSA isolates. Levofloxacin (LEV) resistance was slightly higher in MRSA isolates (37.2%) compared to MSSA (28.6%). Moxifloxacin (MFX) showed lower resistance rates in MRSA (23.3%) and even lower in MSSA (2.5%).
Erythromycin (ERY) resistance was present in 15.9% of MRSA isolates and 9.5% of MSSA isolates. Clindamycin (DA) showed similar resistance rates, with 15.1% in MRSA and 9.5% in MSSA isolates.
Resistance to quinupristin/dalfopristin (QDA) was rare, observed in only 1.5% of MRSA isolates, with MSSA remaining fully susceptible. Linezolid (LNZ) resistance was found in 3.1% of MRSA isolates and 4.8% of MSSA isolates. Vancomycin (VA) resistance was detected in 7% of MRSA isolates, while all MSSA isolates were susceptible.
Tetracycline (TET) resistance was more frequent in MRSA (43.8%) compared to MSSA (4.8%). Tigecycline (TGC) resistance was rare, found in 1.6% of MRSA isolates, with MSSA remaining fully susceptible.
Nitrofurantoin (NIT) resistance was observed in 1.6% of MRSA isolates, while MSSA remained fully susceptible. Rifampicin (RIF) resistance was low in MRSA (3.9%) and absent in MSSA. Trimethoprim/sulfamethoxazole (SXT) resistance was seen in 17.4% of MRSA isolates and 4.8% of MSSA isolates.
Table 7 presents the prevalence of multidrug resistance among S. aureus, comparing methicillin‐resistant S. aureus (MRSA) and methicillin‐susceptible S. aureus (MSSA). Among the 279 isolates analyzed, 258 (92.47%) were identified as MRSA, while 21 (7.53%) were MSSA.
Table 7.
Prevalence of multidrug resistance in Staphylococcus aureus (MDR‐MRSA).
| Resistant drugs, n (%) | MRSA, n = 258 (92.47%) | MSSA, n = 21 (7.53%) | p value |
|---|---|---|---|
| 0‐drug resistant | 0 (0.0%) | 8 (38.1%) | < 0.001 |
| 1‐drug resistant | 53 (20.5%) | 5 (23.8%) | |
| 2‐drug resistant | 63 (24.4%) | 4 (19.0%) | |
| ≥ 3‐drug resistant | 142 (55.0%) | 4 (19.0%) |
Notably, none of the MRSA isolates were susceptible to all tested antibiotics, whereas 8 (38.1%) of the MSSA isolates exhibited no resistance (p < 0.001). Single‐drug resistance was observed in 53 (20.5%) MRSA isolates and 5 (23.8%) MSSA isolates. Dual‐drug resistance was detected in 63 (24.4%) MRSA isolates and 4 (19.0%) MSSA isolates. Alarmingly, multidrug resistance (≥ 3‐drug resistance) was significantly more prevalent in MRSA isolates (55%) compared to MSSA isolates (19.0%).
4. Discussion
Methicillin‐resistant Staphylococcus aureus (MRSA) remains a significant global public health threat, particularly within hospital settings. Epidemiological studies show that MRSA prevalence varies across Indonesia and globally, with significant regional disparities [11, 12, 15, 17]. A systematic review of studies conducted between 2006 and 2020 reported MRSA prevalence rates ranging from 0.3% to 52% among clinical isolates [27], depending on the region and healthcare setting. The highest prevalence was recorded in Jakarta, while multicenter studies in Surabaya and Semarang reported the lowest rates. Notably, MRSA prevalence was particularly high in intensive care units (ICUs), with one study from Dr. Soetomo General Academic Hospital in Surabaya reporting a rate of 50% in ICU settings [27].
Our study found a remarkably high prevalence of methicillin‐resistant S. aureus in Indonesian hospital settings, aligning with previous reports that suggest an increasing trend of MRSA in both clinical and community environments [11, 12, 15, 28, 29]. The reported high prevalence of MRSA in our study may be attributed to several factors: First, hospital‐based sampling bias: Our study was conducted in a healthcare facility where clinical samples were analyzed, which are more likely to yield resistant strains. Second, Patient population characteristics: all samples were derived from hospitalized patients, who are at higher risk of MRSA colonization and infection due to prior antibiotic exposure, prolonged hospital stay, and invasive procedures. Third, specimen selection and laboratory criteria: Only culture‐positive S. aureus isolates from clinically significant specimens were included in the analysis for MRSA, which may have increased the proportion of resistant strains. Moreover, MRSA classification in this study was based exclusively on phenotypic cefoxitin susceptibility testing; molecular confirmation of the mecA or mecC genes was not performed. The reported MRSA prevalence should therefore be interpreted as a phenotypic estimate.
In contrast, methicillin‐susceptible S. aureus (MSSA) was detected in only 7.5% (n = 21) of isolates. This relatively low prevalence is consistent with studies indicating the progressive displacement of MSSA by MRSA strains [16, 30], likely driven by selective pressures from widespread antibiotic use [31]. The high MRSA‐to‐MSSA ratio may be attributed to the extensive use of beta‐lactam antibiotics, which favor the survival and proliferation of MRSA strains over their susceptible counterparts [30, 31]. Reconciling these variations in MRSA prevalence across different locations and time periods is challenging. However, these discrepancies may be explained by differences in circulating clones, infection control practices, and antibiotic prescription trends in various hospital settings.
In this study, males exhibited a slightly higher rate of MRSA infection compared to females. However, the association between gender and S. aureus type was not statistically significant (p > 0.05), suggesting that gender does not play a crucial role in MRSA colonization. This finding aligns with previous research [32], which also reported no significant association between gender and MRSA prevalence. These results indicate that other factors, such as healthcare exposure, antibiotic use, and host immunity, may have a greater influence on MRSA colonization than gender alone.
Regarding age distribution, the majority of MRSA and MSSA isolates were recovered from adults aged 25–64 years (70.5% vs. 71.4%). However, the proportions of MRSA and MSSA were relatively similar across all age groups, with no statistically significant correlation observed (p = 0.82). This finding is consistent with earlier studies [32] that reported no clear age‐related predisposition to MRSA infection. The relatively high prevalence of MRSA and MSSA in the 25–64 age group may be attributed to increased healthcare exposure, occupational risk, or comorbid conditions that heighten susceptibility to S. aureus infections.
Regarding the specimen type, there was predominance of pus samples, reflecting higher sample submission from specific clinical departments such as surgical or burn units. This distribution is largely influenced by the hospital's case load and the higher frequency of wound‐related infections requiring microbiological investigation. The present investigation depicted that the prevalence of MRSA and MSSA isolated from pus was the highest in comparison to other clinical samples, despite the fact that there was no statistical correlation between the isolation rates of MRSA and MSSA with any of the analyzed clinical samples. Pus was the primary source of S. aureus, accounting for 77.8% of isolates. Among these, 77.9% were MRSA, while 76.2% were MSSA, indicating a comparable distribution between the two groups. Other specimen types, including blood, body fluids, sputum, and urine, contributed minimally to the overall distribution. The absence of significant variation in MRSA and MSSA proportions across different specimen types (p > 0.05) suggests that S. aureus colonization and infection are not strongly influenced by the site of isolation. The predominance of pus as the primary source of isolates aligns with previous studies [33, 34, 35], which have highlighted skin and soft tissue infections as the most frequent clinical manifestations of MRSA and MSSA. The elevated isolation rates of S. aureus and MRSA in pus observed in our study may be partly attributed to the fact that wound samples were primarily sourced from the burn unit and surgical wards. MRSA is becoming more prevalent in surgical wards, especially among critically ill patients who have spent extended periods in intensive care units [36, 37].
Antimicrobial susceptibility testing (AST) of 279 S. aureus isolates against 17 commonly tested antibiotics revealed high resistance rates to β‐lactam antibiotics, particularly benzylpenicillin (92.5%), oxacillin (33%), and cefotaxime (42.7%), indicating significant β‐lactamase production and methicillin resistance. The high resistance to β‐lactams (92.5%) aligns with previous studies, including those by Shrestha et al. (91.94%) [38], Ansari et al. (94.7%) [39], and Belbase et al. (97.4%) [40]. Similarly, Kumari et al. [41] reported 100% resistance in a tertiary care hospital in eastern Nepal, a finding corroborated by studies elsewhere [42]. Additionally, a study in East Java found 100% penicillin resistance among S. aureus isolates from raw milk samples, with 80% also resistant to tetracycline [43].
Among the aminoglycosides and fluoroquinolones analyzed, resistance to gentamicin was observed in 19% of the isolates. In contrast, the fluoroquinolones ciprofloxacin, levofloxacin, and moxifloxacin exhibited resistance rates of 33.4%, 36.6%, and 22.3%, respectively. These findings are consistent with the earlier studies, which reported higher ciprofloxacin resistance rates in other regions of the country [38, 39]. The widespread use of fluoroquinolones is likely driven by their indiscriminate and empirical administration. These drugs are relatively inexpensive and readily available as over‐the‐counter medications in Indonesia, contributing to their excessive use. As a resource‐limited nation where a significant portion of the population lives below the poverty line, economic constraints, inadequate healthcare infrastructure, and a general lack of awareness regarding antimicrobial resistance further exacerbate the unregulated consumption of these antibiotics. Consequently, quinolones are frequently administered without prior antibiotic susceptibility testing, accelerating the emergence of drug‐resistant strains.
Antimicrobial resistance remains a significant concern in clinical microbiology, particularly in relation to macrolides and lincosamides. In a recent study, the resistance rates for erythromycin and clindamycin were found to be relatively low, observed in 15.4% and 14.7% of bacterial isolates, respectively. These findings indicate that a substantial proportion of isolates remain susceptible to these agents, though resistance is still present at a notable level. In contrast, the streptogramin combination quinupristin/dalfopristin exhibited the highest susceptibility rate among the tested antimicrobial agents, with 98.2% of isolates remaining susceptible. This suggests that quinupristin/dalfopristin may serve as an effective therapeutic option against infections caused by resistant strains. The high susceptibility rate underscores its potential role in clinical settings where macrolide and lincosamide resistance poses a challenge. Continued surveillance of antimicrobial resistance patterns is essential for optimizing treatment strategies and mitigating the spread of resistant bacterial strains. Further research into the mechanisms underlying resistance to macrolides, lincosamides, and streptogramins will be critical for developing novel antimicrobial agents and preserving the efficacy of existing therapies.
Notably, resistance to vancomycin, linezolid, and rifampicin remained relatively low, observed at 6.5%, 3.2%, and 3.6%, respectively. These findings suggest that these agents continue to be viable treatment options for bacterial infections, particularly in cases where multidrug resistance poses a therapeutic challenge.
Among the tested antibiotics, tigecycline and nitrofurantoin demonstrated the highest susceptibility rates, with 98.6% of isolates remaining sensitive to these agents. This indicates their strong potential as effective treatment choices, especially in infections where alternative antibiotics may be compromised by resistance. Additionally, trimethoprim/sulfamethoxazole maintained a susceptibility rate of 83.5%, further highlighting its continued utility in antimicrobial therapy despite the presence of some resistant strains.
The prevalence of MRSA strains resistant to vancomycin varies considerably across different study locations. Previous investigations have reported no vancomycin resistance (0.0%) in certain regions of Nepal [38, 44], while resistance rates have been documented at 33%–41% in India [11], 29.4% in Ethiopia [32], and as high as 62.5% in southwest Nigeria [45]. In the present study, vancomycin resistance was detected in 7% of MRSA isolates, whereas all methicillin‐susceptible S. aureus (MSSA) isolates remained susceptible. These findings highlight the urgent need for continuous surveillance, judicious antibiotic use, and stringent infection control measures to curb the spread of vancomycin‐resistant S. aureus and prevent further escalation of antimicrobial resistance, especially in the hospital setting.
The increasing resistance of MRSA to existing antibiotics is a significant public health concern. In the present study, all MRSA isolates exhibited complete resistance (100%) to benzylpenicillin. This finding aligns with broader trends observed in Indonesia, where MRSA strains have demonstrated resistance to multiple antibiotics. In Yogyakarta, both human‐ and animal‐derived MRSA isolates showed high resistance rates, including 100% resistance to oxacillin and penicillin, 99.27% to ampicillin, and 87.77% to erythromycin [20]. Similar patterns of penicillin resistance have been reported among MRSA strains in various study settings worldwide [33, 40].
The ability of MRSA to acquire and maintain multidrug resistance (MDR) poses significant challenges in clinical settings. Since staphylococci can spread through direct or indirect contact, the rising prevalence of MDR‐MRSA is becoming a critical concern in modern healthcare. Notably, MRSA exhibits a higher level of resistance to various antibiotics compared to MSSA, and its prevalence varies geographically, clinical setting, and site of infection [40, 41, 46]. For instance, Adhikari et al. from Nepal reported a significantly higher prevalence of MDR‐MRSA (94.05%) compared to methicillin‐sensitive S. aureus (52.12%) [16]. In India, various studies have documented MDR rates in MRSA as high as 33%–41% [11]. In a tertiary care hospital in Nepal, Belbase et al. found that 68.6% of MRSA isolates from pus and wound swab samples exhibited MDR [40]. Additionally, in the United States, MDR‐MRSA was observed in the lower respiratory tract in 67.8% of inpatients and 65% of outpatients [46]. Alarmingly, findings from the present study indicate that multidrug resistance (≥ 3‐drug resistance) was significantly more prevalent in MRSA isolates (55%) compared to MSSA isolates (19.0%). These findings underscore the higher burden of antimicrobial resistance among MRSA isolates, highlighting the critical need for stringent antibiotic stewardship and effective infection control measures to mitigate the spread of multidrug‐resistant S. aureus.
In our study, we observed that MSSA isolates demonstrated 100% susceptibility to benzylpenicillin. All MSSA isolates (21/21) were classified as benzylpenicillin‐susceptible by VITEK2 MIC‐based interpretation. This finding should be interpreted with caution, as our workflow did not include a supplemental beta‐lactamase induction test (e.g., nitrocefin or clover‐leaf test), which CLSI recommends for definitive detection of low‐level or inducible beta‐lactamase‐producing strains that may not be reliably identified by routine MIC/disk testing alone. It is therefore possible that some beta‐lactamase‐producing isolates were not detected as resistant using our testing platform; confirmatory beta‐lactamase testing is recommended in future studies.
5. Limitations
This study was accomplished with some limitations that should be addressed in further studies in a similar setting.
-
i.
While this study provides important insights into the prevalence and antimicrobial resistance profile of MDR‐MRSA in Indonesian hospitals, there are several limitations that should be considered. The cross‐sectional nature of the study does not allow for the determination of causal relationships between risk factors and resistance patterns.
-
ii.
The study was limited to clinical isolates, and community‐acquired MDR‐MRSA strains may differ in their resistance profiles. Future research should include larger, multicenter studies with longitudinal data to assess the evolving trends of MDR‐MRSA and its association with clinical outcomes. Moreover, molecular epidemiological studies would help to further elucidate the genetic mechanisms underlying multidrug resistance and the potential for strain transmission across different settings.
-
iii.
Vancomycin susceptibility was determined using the VITEK2 AST‐GP card, which derives an MIC‐based categorical result per CLSI breakpoints. Individual MIC values were not retained in the dataset extracted for this retrospective study, and no confirmatory reference‐standard method (e.g., broth microdilution or E‐test) was performed on isolates classified as vancomycin‐resistant. Automated systems can have reduced accuracy for vancomycin MIC determination near the resistance breakpoint; therefore, the reported vancomycin resistance rate (7.0% among MRSA isolates) should be interpreted with caution, and confirmatory phenotypic and molecular testing (e.g., van gene detection) is recommended in future studies before this finding is used to guide clinical or public‐health decision‐making.
-
iv.
The molecular confirmation of MRSA, such as the detection of mecA or mecC genes, was not performed in this study, which may limit the accuracy of MRSA confirmation. However, identification of MRSA was based on standard phenotypic methods in accordance with established guidelines.
-
v.
In our study, we observed 100% susceptibility of MSSA isolates to benzylpenicillin may reflect limitations in susceptibility testing and interpretation.
-
vi.
Ward‐level data (e.g., ICU, surgical, or burn unit origin) were not consistently available in the retrospective laboratory database and could therefore not be analyzed; this is acknowledged as a limitation. However, the predominance of pus/wound specimens (77.8% of isolates) is consistent with a case mix weighted toward surgical and wound‐care services, settings repeatedly associated with elevated MRSA recovery rates, and may partly explain the high prevalence observed.
6. Conclusion
Our study demonstrated the overwhelming predominance of MRSA over MSSA, with its prevalence varying significantly across different clinical sample types. Hospital pus samples were identified as the primary reservoir for MRSA. The prevalence of MRSA strains was notably higher than in studies from other countries. Moreover, multidrug resistance (MDR) was more pronounced in MRSA than in MSSA, with Quinupristin/Dalfopristin, Linezolid, Vancomycin, Tigecycline, Nitrofurantoin, and Rifampicin identified as effective treatment options. Molecular confirmation of the mecA or mecC genes was not performed. The reported MRSA prevalence should therefore be interpreted as a phenotypic estimate, and results should be interpreted with appropriate caution until confirmed by molecular methods in future studies.
Given the widespread burden of MRSA and the risk of increasing resistance to commonly used antibiotics, urgent measures are needed in hospital settings. These include the development and enforcement of infection control strategies, mandatory antibiotic susceptibility testing before prescription, regular surveillance and reporting systems, and the prudent use of antimicrobial agents.
Additionally, genotypic studies are strongly recommended to monitor the spread of resistant S. aureus strains. Future research should prioritize longitudinal studies to track resistance trends over time and explore novel therapeutic approaches to combat MRSA infections effectively.
Author Contributions
Muhammad Evy Prastiyanto: conceptualization, investigation, methodology, writing – review and editing, resources, data curation, writing – original draft, software, formal analysis. Afifah Khairunnisa: investigation, methodology, resources, supervision, data curation, writing – review and editing. Shiv Kumar Sah: investigation, methodology, software, formal analysis, writing – review and editing, data curation.
Funding
The authors have nothing to report.
Conflicts of Interest
The authors declare no conflicts of interest.
Transparency Statement
Mr. Shiv Kumar Sah, the corresponding author, affirms that this manuscript is an honest, accurate, and transparent account of the study being reported; that no important aspects of the study have been omitted; and that any discrepancies from the study as planned have been explained.
Acknowledgments
We sincerely appreciate all the patients whose clinical samples contributed to this study, recognizing their invaluable role in advancing medical research. Our heartfelt gratitude also goes to the Hospital management for granting access to clinical samples and laboratory resources, which were essential for conducting this research. Additionally, we extend our deep appreciation to the microbiology and clinical laboratory staff for their dedicated support in sample collection, processing, and antimicrobial susceptibility testing. Their expertise and commitment significantly contributed to the success of this study. We also acknowledge the use of Grammarly software, which was employed solely for language polishing and grammatical correction. All authors have read and approved the final version of the manuscript. The corresponding author, Mr. Shiv Kumar Sah, had full access to all of the data in this study and takes complete responsibility for the integrity of the data and the accuracy of the data analysis.
Data Availability Statement
The data that support the findings of this study are available from the corresponding author upon reasonable request.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The data that support the findings of this study are available from the corresponding author upon reasonable request.