Annals of Clinical Microbiology, The official Journal of the Korean Society of Clinical Microbiology

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Original article

A multicenter study on antimicrobial resistance in bloodstream pathogens isolated in Korea: a survey study

1Department of Laboratory Medicine, Soonchunhyang University Seoul Hospital, Seoul, Korea
2Department of Laboratory Medicine, Inje University College of Medicine, Busan, Korea
3Department of Laboratory Medicine, Gyeongsang National University College of Medicine, Jinju, Korea.
4Departments of Laboratory Medicine, Keimyung University School of Medicine, Daegu, Korea
5Department of Laboratory Medicine, Dong-A University College of Medicine, Busan, Korea
6Department of Clinical Pathology, School of Medicine, Kyungpook National University, Daegu, Korea

*These authors contributed equally to this work.

Correspondence to Sunjoo Kim, E-mail: sjkim8239@hanmail.net

Ann Clin Microbiol 2025;28(2):10. https://doi.org/10.5145/ACM.2025.28.2.4
Received on 30 May 2025, Revised on 12 June 2025, Accepted on 12 June 2025, Published on 27 June 2025.
Copyright © Korean Society of Clinical Microbiology.
This is an Open Access article which is freely available under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/).

Abstract

Background: Bacterial antimicrobial resistance (AMR) is a major contributor to the mortality and disease burden associated with bloodstream infections worldwide. The authors investigated the AMR rates of bacterial isolates obtained from blood cultures in 2023 to provide essential baseline data for AMR management and compared these findings with Korea Global Antimicrobial Resistance Surveillance System (Kor-GLASS) (2023) data limited to the first isolate group in our data.

Methods: Through a multicenter survey, we collected AMR data for bacteria causing bloodstream infections in 2023. Sixteen university-affiliated hospitals participated in the survey; nine provided the first isolate data, and seven reported duplicate isolate data. The survey targeted five gram-positive organisms (Staphylococcus aureus, Staphylococcus epidermidis, Streptococcus pneumoniae, Enterococcus faecalis, Enterococcus faecium) and four gram-negative organisms (Escherichia coli, Klebsiella pneumoniae, Acinetobacter baumannii, Pseudomonas aeruginosa).

Results: Resistance to oxacillin was significantly higher for S. epidermidis (76.9%−83.2%) than S. aureus (39.1%−47.4%), while S. pneumoniae showed 38.9%−51.7% resistance to penicillin. Vancomycin resistance was significantly higher in E. faecium (33.6%−37.8%) than E. faecalis (0.3%). E. coli, K. pneumoniae and P. aeruginosa displayed resistance of 1.1%–1.7%, 10.2%24.9%, and 20.2%–27.3%, respectively, to carbapenems. A. baumannii exhibited carbapenem resistance of 66.3%–87.4%.

Conclusion: Resistance rates among the nine pathogens in this survey were similar to those reported by Kor-GLASS, although K. pneumoniae showed a higher carbapenem resistance rate. Continuous monitoring and antimicrobial stewardship are necessary to reduce the AMR of major pathogens causing bloodstream infections.

Keywords

Antibiotic resistance, Microbial sensitivity tests, Bloodstream infection, Multicenter study, South Korea

Introduction

Background

Antibiotic-resistant bacteria pose a global health threat and cause substantial mortality, particularly in low-income countries. A global assessment of antimicrobial resistance (AMR) initiated in 2014 projected up to 10 million AMR-attributable deaths annually by 2050 [1]. Recent estimates indicate that in 2021, 4.7 million deaths will be associated with bacterial AMR worldwide, with 1.1 million directly attributable to resistant pathogens [2]. Resistance patterns vary according to region and socioeconomic status [35], with Asia experiencing the highest mortality from bacterial bloodstream infections [3]. Cumulative AMR-related deaths from 2025 to 2050 are expected to be highest in Asia, reaching 11.8 million [2]. The World Health Organization (WHO) established the Global Antimicrobial Resistance and Use Surveillance System (GLASS) [5], which informs the bacterial priority pathogen list [6]. Many countries have implemented national surveillance systems [7] with South Korea participating via the Korea Global Antimicrobial Resistance Surveillance System (Kor-GLASS), which has published annual reports since 2017 and, currently in its third phase (2023–2025), collected AMR data on 15 major bacterial species from 11 general hospitals nationwide [8].

Objectives

This study investigated the prevalence of antibiotic-resistant bacteria causing bloodstream infections in university-affiliated hospitals in 2023 and compared these resistance rates with Kor-GLASS (2023) data and global studies to provide essential baseline data for AMR management.

Methods

Study design

This is a multicenter survey study.

Setting and participants

Survey data were collected via excel sheet from clinical microbiologists at 16 university-affiliated hospitals in South Korea: Asan Medical Center, Gyeongsang National University Changwon Hospital, Chonnam National University Hospital, Chungnam National University Hospital, Dong-A University Hospital, Kangdong Sacred Heart Hospital, Gyeongsang National University Changwon Hospital, Inje University Haeundae Paik Hospital, Keimyung University Dongsan Hospital, Konkuk University Medical Center, Kyung Hee University Hospital, Kyungpook National University Hospital, Pusan National University Hospital, Samsung Medical Center, Seoul St. Mary’s Hospital, and Soonchunhyang University Seoul Hospital.

Variables

Outcome variables were antimicrobial resistance rats of the tested bloods.

Data sources/measurement

Resistance rates were based on the antimicrobial susceptibility test (AST) results recorded in each hospital’s electronic medical recording system from January 1 to December 31, 2023. The target organisms were five gram-positive species (Staphylococcus aureus, Staphylococcus epidermidis, Streptococcus pneumoniae, Enterococcus faecalis, and Enterococcus faecium) and four gram-negative species (Escherichia coli, Klebsiella pneumoniae, Acinetobacter baumannii, and Pseudomonas aeruginosa). The antibiotics tested for each organism and hospital are listed in Supplementary Table 1.

For each antibiotic, the resistance rates of gram-positive and gram-negative bacteria were calculated as (number of resistant isolates/number of tested isolates) × 100 (%). Data were analyzed separately for hospitals providing the first isolate results (first isolate group: organisms isolated for the first time) and duplicate results (duplicate group: organisms isolated on two or more occasions, with unknown time intervals between isolates).

 

Table 1. Baseline characteristics of the 16 university-affiliated hospitals participating in the survey

Categories No. (%)
No. of beds ≥ 1,000 6 (37.5)
700–999 9 (56.3)
500–699 1 (6.3)
Location Seoul 7 (43.8)
Other citiesa) 9 (56.3)
Isolate count First isolate 9 (56.3)
Duplicate 7 (43.8)
Total 16 (100.0)

a) Busan (3 hospitals), Daegu (2), Daejeon (1), Gwangju (1), Changwon (1), and Jinju (1).

Bias

The number of isolates refers to those that underwent AST rather than the total number identified at each hospital. Selection and measurement biases may be present in duplicate isolates, and sampling bias may occur when AST for specific antibiotics is performed in a limited number of hospitals (Supplementary Table 1).

Study size

Sample size estimation was not done since data were collected from the respondents’ hospital data of antimicrobial susceptibility tests.

Statistical methods

Results were summarized using descriptive statistics.

Results

Sixteen university-affiliated hospitals participated in the survey (Table 1), of which 37.5% had 1,000 or more beds, 43.8% ranged between 700 and 999 beds, 6.3% contained 500 to 699 beds; 43.8% were located in Seoul, and 56.3% were in other cities. Between January 1 and December 31, 2023, 56.3% (268,074 isolates) were categorized into the first isolate group (excluding duplicate results), while 43.8% (174,575 isolates) belonged to the duplicate group (including duplicates). Antibiotic susceptibility testing results were recruited (Table 2). Gram-negative bacteria were 2–3 times more common than gram-positive bacteria (2.7-fold in the first isolate group and 2.0-fold in the duplicate group). Overall, E. coli (first isolate, 43.1%; duplicate, 36.9%) and K. pneumoniae (first isolate, 21.1%; duplicate, 23.1%) were the most common, whereas A. baumannii (first isolate, 2.3%; duplicate, 4.4%) and S. pneumoniae (first isolate, 0.4%; duplicate, 0.2%) were the least frequent.

Table 2. Species distribution of bacterial isolates tested for antimicrobial susceptibility in 16 university-affiliated hospitals in 2023

OrganismsNo. of isolates% of isolates
First isolateDuplicateFirst isolateDuplicate
Gram-positive bacteria72,97258,83027.233.7
Staphylococcus aureus23,69222,8928.813.1
Staphylococcus epidermidis19,33921,9747.212.6
Enterococcus faecalis14,6944,4055.52.5
Enterococcus faecium14,1889,2645.35.3
Streptococcus pneumoniae1,0592950.40.2
Gram-negative bacteria195,102115,74572.866.3
Escherichia coli115,55764,38843.136.9
Klebsiella pneumoniae56,47140,39821.123.1
Pseudomonas aeruginosa16,8953,3016.31.9
Acinetobacter baumannii6,1797,6582.34.4
Total268,074174,575100.0100.0

Resistance rates for gram-positive and gram-negative bacteria comparing the first isolate and duplicate groups and the investigated antibiotics are summarized in Tables 3 and 4, respectively. The total resistance rates, without distinguishing between the first and duplicate groups, are presented in Supplementary Table 2.

Gram-positive bacteria

S. aureus exhibited high resistance to penicillin (85.1%–86.0%), oxacillin (39.1%–47.4%), and cefoxitin (60.0%). Cefoxitin was not assessed in any hospital in the first isolate group, whereas it was detected in only one hospital in the duplicate group, indicating a potential bias. Resistance to macrolides ranged from 13.5% to 33.0% and to minocycline from 1.2% to 3.4%. Resistance to vancomycin (0.0%), daptomycin (0.0%), and linezolid (0.0%–0.3%) was rare, and resistance to trimethoprim-sulfamethoxazole ranged from 0.7% to 2.0%. S. epidermidis showed very high resistance to penicillin (93.0%–94.2%) and oxacillin (76.9%–83.2%). Resistance rates for macrolides and trimethoprim-sulfamethoxazole were 34.0%–67.6% and 37.9%–45.2%, respectively. Rare resistance was observed for vancomycin (0.0%), daptomycin (0.0%), and linezolid (0.0%–0.2%). S. pneumoniae demonstrated resistance to penicillin (38.9%–51.7%), third-generation cephalosporins (14.8%–33.3%), and meropenem (62.5%). Resistance to macrolide and tetracycline exceeded 71.2% and 75.6%, respectively, whereas that of trimethoprim-sulfamethoxazole ranged from 28.6% to 41.0%. Vancomycin resistance was not observed. E. faecium showed resistance rate exceeding 89.6% to penicillin and ampicillin and 33.6%–37.8% to vancomycin. Daptomycin resistance was 2.9% in the first isolate group (744 isolates) and 100% in the duplicate group (16 isolates, one hospital), whereas linezolid resistance was 0.1%–0.9%. E. faecalis exhibited penicillin resistance of 6.5% (first isolate) and 23.7% (duplicate) and vancomycin and daptomycin resistance of 0.3% and 0.0%–0.4%, respectively. High-level gentamicin and streptomycin resistance was observed 37.7%–48.2% and 11.6%–15.8%, respectively (Table 3).

Table 3. Prevalence of antimicrobial resistance of five gram-positive bacteria

 

Antibiotics

Organisms

 

SAUSEPSPNEFMEFA
FirstDupFirstDupFirstDupFirstDupFirstDup
PenicillinsPenicillin85.186.093.094.238.951.789.991.36.523.7
Ampicillin      89.691.30.31.9
Oxacillin39.147.476.983.2      
CephalosporinsCefoxitin (2nd GC)NAa)60.0b)        
Cefotaxime (3rd GC)    33.322.2    
Ceftriaxone (3rd GC)    16.714.8    
Ceftaroline (5th GC)11.1b)4.7b)        
CarbapenemsMeropenem    62.5NAa)    
GlycopeptidesVancomycin0.00.00.00.00.00.033.637.80.30.3
LipopeptidesDaptomycin0.00.0b)    29.3100.0b)0.40.0b)
MacrolidesAzithromycin30.933.0b)59.534.0      
Erythromycin30.130.358.567.687.888.6    
Clindamycin13.528.334.849.271.284.8    
TetracyclinesTetracycline12.112.819.519.775.685.0    
Minocycline1.23.4b)0.01.1      
AminoglycosidesGentamicin (High-level)      28.036.437.748.2
Streptomycin (High-level)        11.615.8
FluoroquinolonesLevofloxacin    9.12.9    
Moxifloxacin    14.33.8    
Folate pathway inhibitorsTrimethoprim-sulfamethoxazole0.72.037.945.241.028.6    
OxazolidinonesLinezolid0.00.30.00.2  0.10.90.31.3
RifamycinsRifampin1.26.111.714.8      
Total No. of isolates23,69222,89219,33921,9741,05929514,1889,26414,6944,405

The numbers shown in the colored cells indicate the antimicrobial resistance rates. Color-coded as follows: red (76.0–100%), orange (51.0–75.9%), yellow (26.0–50.9%), sky blue (1.0–25.9%), and blue (0.0–0.9%).
a)None of the hospitals performed the test; b)Only one hospital contributed data.
Abbreviations: SAU, Staphylococcus aureus; SEP, Staphylococcus epidermidis; SPN, Streptococcus pneumoniae; EFM, Enterococcus faecium; EFA, Enterococcus faecalis; First, first isolate group; Dup, duplicate group; GC, generation cephalosporins; NA, not available.

Gram-negative bacteria

E. coli demonstrated high resistance to ampicillins (70.2%–71.1%) and moderate to most of beta-lactams (13.0%–45.6%), except for piperacillin-tazobactam (5.2%–6.3%), cefoxitin (8.5%–10.8%), and ceftazidimeavibactam (0.9%). Carbapenem resistance remained low (1.1%–1.7%). Fluoroquinolone resistance ranged from 46.9% to 53.1%, with levofloxacin reaching 100% in the duplicate group (1,042 isolates, two hospitals) compared with 46.9% in the first isolate group (6,925 isolates). Trimethoprim-sulfamethoxazole resistance was 37.0%–37.6%. K. pneumoniae exhibited very high resistance to ampicillin (96.9%–99.8%) and 18.8%–49.6% to other beta-lactams. Carbapenem resistance ranged from 10.2% to 24.9%. Fluoroquinolone resistance was 34.1%–44.6%, with 100% resistance to levofloxacin in the duplicate group (727 isolates, two hospitals) and 34.1% in the first isolate group (3,294 isolates). Trimethoprim-sulfamethoxazole resistance was 35.2%–40.0%. A. baumannii displayed resistance exceeding 49.1% to most antibiotics, except minocycline (1.2%–9.9%). Carbapenem resistance was particularly high (66.3%–87.4%). P. aeruginosa showed 14.3%–30.2% resistance to most of beta-lactams and carbapenem resistance was 20.2%–27.3%. Tobramycin and fluoroquinolones resistance was 8.1%–11.2% and 28.3%–30.2%, respectively (Table 4).

Table 4. Prevalence of antimicrobial resistance of four gram-negative bacteria

 

Antibiotics

Organisms

 

ECOKPNABMPAE
FirstDupFirstDupFirstDupFirstDup
PenicillinsPenicillin        
Ampicillin70.271.196.999.8    
Penicillin/beta-lactamase
inhibitor combinations
Amoxicillin-clavulanate13.028.318.827.1    
Ampicillin-sulbactam27.522.144.145.3b)55.973.7  
Piperacillin-tazobactam5.26.327.134.963.987.521.230.2
CephalosporinsCefazolin (1st GC)45.644.432.344.4    
Cefuroxime (2nd GC)38.744.048.849.6    
Cefoxitin (2nd GC)8.510.824.025.5    
Cefotaxime (3rd GC)32.844.138.445.6    
Ceftriaxone (3rd GC)26.430.4b)45.546.8b)67.388.7  
Ceftazidime (3rd GC)    76.785.120.427.6
Cefepime (4th GC)37.442.837.639.665.376.015.219.9
Ceftazidime-avibactam0.9NAa)4.6NAa)  14.3NAa)
Ceftolozane-tazobactam      80.0b)20.0b)
CarbapenemsImipenem1.31.216.119.367.987.223.927.3
Meropenem1.41.317.124.966.387.420.225.0
Ertapenem1.11.710.220.5    
TetracyclinesTetracycline41.545.0b)36.451.7b)    
Minocycline    1.29.9  
AminoglycosidesGentamicin25.023.614.423.958.976.9  
Tobramycin25.56.027.219.757.289.811.28.1
Amikacin1.10.41.02.153.949.1  
FluoroquinolonesCiprofloxacin49.453.140.944.6  29.028.3
Levofloxacin46.9100.034.1100.064.085.228.630.2
Folate pathway inhibitorsTrimethoprim-sulfamethoxazole37.637.040.035.261.183.3  
Total No. of isolates115,55764,38856,47140,3986,1797,65816,8953,301

The numbers shown in the colored cells indicate the antimicrobial resistance rates. Color-coded as follows: red (76.0–100%), orange (51.0–75.9%), yellow (26.0–50.9%), sky blue (1.0–25.9%), and blue (0.0–0.9%).
a)None of the hospitals performed the test; b)Only one hospital contributed data.
Abbreviations: ECO, Escherichia coli; KPN, Klebsiella pneumoniae; ABM, Acinetobacter baumannii; PAE, Pseudomonas aeruginosa; First, first isolate group; Dup, duplicate group; GC, generation cephalosporins; NA, not available.

Discussion

Interpretation/comparison with previous studies

This study analyzed the resistance rates of major pathogens isolated from bloodstream infections in Korea in 2023 using AST data from 16 university-affiliated hospitals and compared the findings with the 2023 Kor-GLASS annual report [8]. As Kor-GLASS excluded duplicate results, comparisons were made only with the first isolate group (nine hospitals). Our dataset includes a higher number of isolates, whereas KorGLASS covers a broader geographic range. For S. aureus, S. pneumoniae, E. faecalis, and E. faecium, KorGLASS collected only 832, 27, 287, and 543 isolates, respectively, compared to 23,692, 1,059, 14,694, and 14,188 isolates, respectively, in our dataset. For E. coli, K. pneumoniae, A. baumannii, and P. aeruginosa, KorGLASS collected 2,844, 1,244, 269, and 269 isolates, respectively, compared to 115,557, 56,471, 6,179, and 16,895 isolates, respectively in our study. Kor-GLASS included 11 general hospitals from each of the 10 regions, providing a more balanced regional distribution than that in our study, comprising five hospitals in Seoul, one in Gyeongbuk, two in Gyeongnam, and one in Busan.

For S. aureus, the methicillin-resistant S. aureus (MRSA) rate in Kor-GLASS was 45.2%, similar to previous years, whereas our data showed a rate of 39.1%, which is 6.1% lower than that of Kor-GLASS. The multidrug-resistant (MDR) S. aureus rate was 47.6% in Kor-GLASS and 84.6% (22/26) in long-term care hospitals, with SCCmec type IV, the most prevalent genotype (30.5%) [8,9], characterized by high transmissibility and rapid growth and is now increasingly observed among MRSA strains worldwide [1012].

For S. pneumoniae, the small number of isolates analyzed in Kor-GLASS (27 isolates) limits the generalizability; the resistance rates for penicillin, cefotaxime, ceftriaxone, and meropenem were 11.1%, 7.4%, 7.4%, and 51.9%, respectively, all of which were significantly lower than those observed in our study (38.9%, 33.3%, 16.7%, and 62.5%, respectively). Resistance to erythromycin was also high in both KorGLASS (81.5%) and our study (87.8%). Jung et al. [13] reported 7.7% penicillin and cefotaxime and 92.3% erythromycin resistance among S. pneumoniae isolates from invasive infections in a children’s hospital (2014–2018) in South Korea, showing especially high erythromycin resistance. As data on macrolide resistance in S. pneumoniae from bloodstream infections in our country are limited, Kor-GLASS is needed to monitor resistance rates separately by age, particularly for pediatric patients.

For E. faecium, the resistance rates to ampicillin (89.0% in Kor-GLASS, 89.6% in our data) and vancomycin (34.6% and 33.6%) were high or moderate, respectively, whereas linezolid resistance was very low (0.0% and 0.1%, respectively). Daptomycin resistance differed markedly (0.7% vs. 29.3%), likely because of a bias of 90.9% (676/744) in the isolates originating from a single hospital. The prevalence of MDR E. faecium steadily increased, reaching 65.7% in Kor-GLASS. Although vanB-positive vancomycinresistant enterococci (VRE) remains rare (0.5%) [8], its increasing prevalence in regions such as Europe and Australia, and its potential to spread resistance genes [14,15], particularly in anaerobic bacteria, underscores the need for ongoing surveillance. For E. faecalis, the ampicillin and vancomycin resistance rates were very low in both Kor-GLASS (0.7% each) and our data (0.3% each). Two vancomycin-resistant E. faecalis isolates from Kor-GLASS carried vanA. The high gentamicin and streptomycin resistance rates in Kor-GLASS were 42.2% and 5.9 %, respectively, which are similar to our data (37.7% and 11.6%, respectively). High-level gentamicin resistance in E. faecalis is clinically significant owing to its association with combination therapy failure, and its rate has declined steadily in Kor-GLASS over the past 3 years. A metaanalysis [16] reported a high-level gentamicin resistance of 44.3%, which is consistent with data from South Korea. The proportion of MDR isolates in Kor-GLASS was 3.8% for E. faecalis, which was substantially lower than the 65.7% observed for E. faecium.

For E. coli, the resistance rates were 38.9% for cefotaxime and 12.0% for ceftazidime in Kor-GLASS, whereas our data showed rates of 32.8% and 26.4%, respectively. The predominance of CTX-M likely explains the higher cefotaxime resistance among 3rd generation cephalosporins [17]. Carbapenem resistance rates were very low in Kor-GLASS (imipenem, 0.2%; meropenem, 0.2%; and ertapenem, 0.7%) and slightly higher in our study (1.3%, 1.4%, and 1.1%, respectively). Kor-GLASS identified seven carbapenem-resistant (CR) E. coli isolates. KPC is now the most common type in South Korea [8,18], whereas NDM-1 and OXA48 have been more frequently reported [19].

For K. pneumoniae, Kor-GLASS reported resistance rates of 42.6% for cefotaxime and 30.3% for ceftazidime, whereas our data showed rates of 45.6% and 46.8%, respectively. Carbapenem resistance was lower, probably due to the small number of isolates, but increased in Kor-GLASS (5.9%–7.2% among 1,244 isolates) and higher in our data (10.2%–17.1% among 4,199–6,950 isolates), while a single-center study in South Korea also reported a 10% prevalence in 2020 [20]. In South Korea, carbapenemase-producing Enterobacterales (CPE) account for 63.4% of carbapenem-resistant Enterobacterals infections [21], with K. pneumoniae accounting for 58.9% [22]. Recently, KPC-2, NDM-1, and OXA-48 have become the most common carbapenemase-producing (CP)-K. pneumoniae strains [18,22], and KPC is the most prevalent strain globally [23]. The use of ceftazidime-avibactam for KPC producers has led to resistant KPC variants and increased ceftazidime-avibactam-resistance [24] and NDM-producing K. pneumoniae, with resistance rates of 5.5% in Kor-GLASS and 4.6% in our data. However, continued surveillance is needed considering the rapid global spread of CPE [6].

CR-A. baumannii remains a major global issue, with Kor-GLASS reporting very high resistance rates (85.3%–85.6%) compared to our data showing 66.3%–67.9% based on relatively few isolates (269 in KorGLASS, 588 in our data), while WHO/European Centre for Disease Prevention and Control (2020–2022) [4] reported prevalence exceeding 50% in 35 countries and 96.3% in the Asia-Pacific region [25]. OXA-23 is the predominant carbapenemase globally as well as in South Korea (99.3% in Kor-GLASS). In Kor-GLASS, resistance rates for ampicillin-sulbactam, minocycline, tigecycline, and colistin used for OXA-23-producing A. baumannii were 77.4%, 7.6%, 2.3%, and 1.1%, respectively, along with Asia-Pacific data (over 80%, 7.2%, 6.7%, and 1.7%, respectively) [25], whereas our data showed lower rates for ampicillin-sulbactam (55.9%) and minocycline (1.2%).

For P. aeruginosa, piperacillin-tazobactam resistance was 20.4%–24.9% in Kor-GLASS and 21.2% in our study. The carbapenem resistance rates for imipenem and meropenem were 30.5% and 27.1% in KorGLASS (269 isolates), 35.4% and 34.4% in Choi et al. [26] (212 isolates), and 23.9% and 20.2% in our data (2,147 isolates), respectively, likely due to differences in the number of isolates. In Kor-GLASS, CP-P. aeruginosa was 45.1% of the CR isolates, mainly NDM-1 and GES genotypes; however, Choi et al. [26] found IMP-6 and NDM-1 most frequently, indicating genotype heterogeneity. Globally, VIM and IMP are the most common, with IMP prevalent in the Asia-Pacific region and NDM increasing in Europe and Asia [27].

Although new agents such as lefamulin, tedizolid, sulbactam-durlobactam, imipenem-relebactam, meropenem-vaborbactam, plazomicin, and cefiderocol have been developed to address the increasing antibiotic resistance, none were used in the hospitals surveyed. Meta-analyses have identified resistance to imipenem-relebactam (14.6% among gram-negative bacilli, higher in intensive care units [ICUs] and developing countries) [28] and cefiderocol (3.0% in A. baumannii, 1.4% in P. aeruginosa) [29], emphasizing the need for ongoing monitoring. Because resistance inevitably increases over time, antimicrobial stewardship programs (ASP) are crucial for prevention. Alawi et al. [30] achieved a 40% reduction in intravenous antibiotic use, leading to an 80.9% decrease in the incidence of MDR organisms in ICUs and a 62.0% decrease in long-term care facilities over 5 years. Sumathi et al. [31] reduced the duration of antibiotic use from 12 to 8 days and lowered the MRSA rates from 45% to 30% in India. In addition, ASPs have shown substantial economic impacts: Timbrook et al. [32] reported a 16.4% decrease in daily antibiotic use and savings of 1,892,895 USD in the US; Banan et al. [33] observed a 55.5% (5,669.2 USD) reduction in expenses for colistin, meropenem, and tigecycline in Palestine.

Limitations

A major limitation of this study was its focus on university-affiliated hospitals, excluding smaller hospitals and long-term care facilities where AMR may be more prevalent. From 2020 to 2022, the average antibiotic use in South Korean clinics and long-term care hospitals was 17.7% and 7.2% higher, respectively, than that in general hospitals [8], and 34.9% of long-term care physicians acknowledged unnecessary or inappropriate antibiotic prescriptions [34]. The predominance of institutions in Seoul and other metropolitan areas further limits regional generalizability. We included both the first isolate and duplicate data, which might have affected the resistance rate if AMR strains were isolated more frequently. The AMR data for the duplicate group showed similar or slightly higher resistance rates. Finally, although the AST methods and equipment were not standardized among the participating hospitals, they may have affected the AMR data.

Conclusion

This study analyzed AMR rates of the bloodstream isolates of major gram-positive and gram-negative bacteria in university-affiliated hospitals, showing trends largely consistent with Kor-GLASS (2023), except for higher CR-K. pneumoniae. Moreover, this study demonstrated that a retrospective multicenter analysis can provide valuable insights into the AMR rates of blood culture isolates. Broader surveillance across diverse hospital types and regions and monitoring of resistance to new antibiotics are needed for the effective management of major pathogens causing bloodstream infections.

Ethics statement

This study was approved by the Institutional Review Board of Gyeongsang National University Changwon Hospital (IRB No. 2024-09-011).

Conflicts of interest

No potential conflicts of interest relevant to this article were reported.

Funding

This study was funded by a grant from the Korean Society of Clinical Microbiology and the Ministry of Trade, Industry, and Energy of Korea (RS-2024- 00403563). The funders had no role in the study design, data collection and interpretation, or the decision to submit the manuscript for publication.

Data availability

The datasets generated during the current study are available from the corresponding author upon request.

Acknowledgments

The authors thank all participants who shared the AMR data of each hospital.

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5. World Health Organization. Global antimicrobial resistance and use surveillance system (GLASS) report. Antibiotic use data for 2022. Geneva; World Health Organization, 2025.

6. World Health Organization. WHO bacterial priority pathogens list, 2024: bacterial pathogens of public health importance to guide research, development and strategies to prevent and control antimicrobial resistance. Geneva; World Health Organization, 2024.

7. Sabbatucci M, Ashiru-Oredope D, Barbier L, Bohin E, Bou-Antoun S, Brown C, et al. Tracking progress on antimicrobial resistance by the quadripartite country self-assessment survey (TrACSS) in G7 countries, 2017-2023: opportunities and gaps. Pharmacol Res 2024;204:107188.

8. Korea Disease Control and Prevention Agency. National Antimicrobial Resistance Surveillance Report 2023. Cheongju; Korea Disease Control and Prevention Agency, 2023.

9. Hwang YJ. Comparing the phylogenetic distribution of multilocus sequence typing, staphylococcal protein A, and staphylococcal cassette chromosome mec types in methicillin-resistant Staphylococcus aureus (MRSA) in Korea from 1994 to 2020. Antibiotics 2023;12:1397.

10. Yamaguchi T, Nakamura I, Sato T, Ono D, Sato A, Sonoda S, et al. Changes in the genotypic characteristics of community-acquired methicillin-resistant Staphylococcus aureus collected in 244 medical facilities in Japan between 2010 and 2018: a nationwide surveillance. Microbiol Spectr 2022;10:e0227221.

11. Sadeghi Moghaddam T, Namaei MH, Afshar D, Yousefi M. High frequency of SCCmec type IV and multidrug-resistant SCCmec type I among hospital acquired methicillin-resistant Staphylococcus aureus isolates in Birjand Imam Reza Hospital, Iran. Iran J Microbiol 2022;14:67-75.

12. Naimi HM, Tristan A, Bes M, Vandenesch F, Nazari QA, Laurent F, et al. Molecular characterization and antimicrobial resistance of nasal Staphylococcus aureus in the community of Kabul. J Glob Antimicrob Resist 2023;34:18-22.

13. Jung J, Yoo RN, Sung H, Kim M, Lee J. Antibiotics susceptability of Streptococcus pneumoniae isolated from single tertiary childrens’ hospital since 2014 and choice of appropriate empirical antibiotics. Pediatr Infect Vaccine 2019;26:1-10.

14. Piezzi V, Wassilew N, Atkinson A, D’Incau S, Kaspar T, Seth-Smith HM, et al. Nosocomial outbreak of vancomycin-resistant Enterococcus faecium (VRE) ST796, Switzerland, 2017 to 2020. Euro Surveill 2022;27:2200285.

15. Werner G, Neumann B, Weber RE, Kresken M, Wendt C, Bender JK, et al. Thirty years of VRE in Germany – “expect the unexpected”: the view from the National Reference Centre for Staphylococci and Enterococci. Drug Resist Updat 2020;53:100732.

16. Shahini Shams Abadi M, Taji A, Salehi F, Kazemian H, Heidari H. High-level gentamicin resistance among clinical isolates of enterococci in Iran: a systematic review and meta-analysis. Folia Med 2021;63:15-23.

17. Harbaoui S, Ferjani S, Abbassi MS, Saidani M, Gargueh T, Ferjani M, et al. Genetic heterogeneity and predominance of blaCTX-M-15 in cefotaxime-resistant Enterobacteriaceae isolates colonizing hospitalized children in Tunisia. Lett Appl Microbiol 2022;75:1460-74.

18. Park JJ, Seo YB, Lee J, Eom JS, Song W, Choi YK, et al. Positivity of carbapenemase-producing Enterobacteriaceae in patients following exposure within long-term care gfacilities in Seoul, Korea. J Korean Med Sci 2020;35:e303.

19. Hong JS, Park BY, Kim D, Kim K, Lee KH, Cho NH, et al. Epidemiological study of an outbreak of KPC-2-producing Klebsiella pneumoniae in a tertiary hospital in Korea. Ann Clin Microbiol 2020;23:81-92.

20. Chong YP. Changing epidemiology of multidrug-resistant pathogens: a new battle against carbapenem-resistant Enterobacterales. Korean J healthc assoc Infect Control Prev 2023;28:243-4.

21. Kim SY, Shin J, Shin SY, Ko KS. Characteristics of carbapenem-resistant Enterobacteriaceae isolates from Korea. Diagn Microbiol Infect Dis 2013;76:486-90.

22. Park SH, Park SH, Kim JS, Yu JK, Kim JK, Suh HS, et al. Genetic distribution of carbapenem-resistant Enterobacteriaceae in Seoul Korea, 2018-2020. J Bacteriol Virol 2022;52:28-38.

23. van Duin D, Arias CA, Komarow L, Chen L, Hanson BM, Weston G, et al. Molecular and clinical epidemiology of carbapenem-resistant Enterobacterales in the USA (CRACKLE-2): a prospective cohort study. Lancet Infect Dis 2020;20:731-41.

24. Qiao S, Xin S, Zhu Y, Zhao F, Wu H, Zhang J, et al. A large-scale surveillance revealed that KPC variants mediated ceftazidime-avibactam resistance in clinically isolated Klebsiella pneumoniae. Microbiol Spectr 2024;12:e0025824.

25. Lee YL, Ko WC, Hsueh PR. Geographic patterns of Acinetobacter baumannii and carbapenem resistance in the Asia-Pacific Region: results from the Antimicrobial Testing Leadership and Surveillance (ATLAS) program, 2012-2019. Int J Infect Dis 2023;127:48-55.

26. Choi YJ, Kim YA, Junglim K, Jeong SH, Shin JH, Shin KS, et al. Emergence of NDM1-producing Pseudomonas aeruginosa sequence type 773 clone: shift of carbapenemase molecular epidemiology and spread of 16S rRNA methylase genes in Korea. Ann Lab Med 2023;43:196-9.

27. Wang MG, Liu ZY, Liao XP, Sun RY, Li RB, Liu Y, et al. Retrospective data insight into the global distribution of carbapenemase-producing Pseudomonas aeruginosa. Antibiotics 2021;10:548.

28. Abniki R, Tashakor A, Masoudi M, Mansury D. Global resistance of imipenem/relebactam against gram-negative bacilli: systematic review and meta-analysis. Curr Ther Res Clin Exp 2024;100:100723.

29. Karakonstantis S, Rousaki M, Vassilopoulou L, Kritsotakis EI. Global prevalence of cefiderocol non-susceptibility in Enterobacterales, Pseudomonas aeruginosa, Acinetobacter baumannii, and Stenotrophomonas maltophilia: a systematic review and meta-analysis. Clin Microbiol Infect 2024;30:178-88.

30. Alawi MM, Tashkandi WA, Basheikh MA, Warshan FM, Ghobara HA, Ramos RB, et al. Effectiveness of antimicrobial stewardship program in long-term care: a five-year prospective single-center study. Interdiscip Perspect Infect Dis 2022;2022:8140429.

31. Sumathi S, Venkateswarlu K. The impact of antimicrobial stewardship programs on antimicrobial resistance patterns in a tertiary care hospital: an observational study. J Adv Med Pharm Sci 2023;6:300-4.

32. Timbrook TT, Hurst JM, Bosso JA. Impact of an antimicrobial stewardship program on antimicrobial utilization, bacterial susceptibilities, and financial expenditures at an academic medical center. Hosp Pharm 2016;51:703-11.

33. Banan MA, Nazzal MA, Abdelhaq AI, Abutaha SA, Zyoud SH, Sabateen A. Impact of an antibiotic stewardship program on antibiotic utilization, bacterial susceptibilities, and cost of antibiotics. Sci Rep 2023;13:5040.

34. Lee S, Kim Y, Kim D, Seo S, Kim S, Shin N. Analysis of antimicrobial use in Korean longterm care hospitals, 2020-2022. Public Health Wkly Rep 2025;18:225-43.

Supplementary material

Supplementary Table 1. Distribution of hospitals responding to the survey on the prevalence of antimicrobial resistance

Antibiotics

Organisms

Gram-positive organismsGram-negative organisms
SAUSEPSPNEFMEFAECOKPNABMPAE
FirstDupFirstDupFirstDupFirstDupFirstDupFirstDupFirstDupFirstDupFirstDup
PenicillinsPenicillin9777768787        
Ampicillin      97979797    
Oxacillin7797              

Penicillin/

beta-lactamase inhibitor combinations

Amoxicillin-clavulanate          4647    
Ampicillin-sulbactam          7271    
Piperacillin-tazobactam          96956797
Sulbactam-durlobactam              00  
Cephalo-sporinsCefazolin (1st GC)          7777    
Cefuroxime (2nd GC)          4252    
Cefoxitin (2nd GC)0100      8785    
Cefotetan (2nd GC)          0000    
Cefotaxime (3rd GC)    85    7777    
Ceftriaxone (3rd GC)    75    4141    
Ceftazidime (3rd GC)              8797
Cefepime (4th GC)          97979797
Ceftaroline (5th GC)1100              
Cefiderocol          00000000
Ceftazidime-avibactam          2030  20
Ceftolozane-tazobactam                11
CarbapenemsImipenem          97979796
Meropenem    40    73739797
Ertapenem          8787    
Imipenem-relebactam          0000  00
Meropenem- vaborbactam          0000    
GlycopeptidesVancomycin9742979797        
LipopeptidesDaptomycin4197  3131        
MacrolidesAzithromycin4142              
Clarithromycin0000              
Erythromycin979794            
LincosamidesClindamycin979796            
TetracyclinesTetracycline979797    4131    
Doxycycline000000            
Minocycline3131          67  
Amino-glycosidesGentamicin          979796  
Gentamicin (High-level)      8787        
Tobramycin          43537464
Amikacin          878775  
Streptomycin (High-level)      8687        
Plazomicin          0000    
Fluoro-quinolonesCiprofloxacin          97979797
Levofloxacin    45    72629696
Moxifloxacin    97            
Folate pathway inhibitorsTrimethoprim-sulfamethoxazole979796    969796  
Oxa-zolidinonesLinezolid8787  8787        
Tedizolid0000  0000        
RifamycinsRifampin9696              
Pleuro-mutilinsLefamulin0000              

The numbers in cells indicate the number of responding hospitals.
Abbreviations: SAU, Staphylococcus aureus; SEP, Staphylococcus epidermidis; SPN, Streptococcus pneumoniae; EFM, Enterococcus faecium; EFA, Enterococcus faecalis; ECO, Escherichia coli; KPN, Klebsiella pneumoniae; ABM, Acinetobacter baumannii; PAE, Pseudomonas aeruginosa; First, first isolate group; Dup, duplicate group; GC, generation cephalosporins.

Supplementary Table 2. Prevalence (%) of total antimicrobial resistance in five gram-positive and four gram-negative bacteria

Organisms

Antibiotics

Gram-positive organismsGram-negative organisms
SAUSEPSPNEFMEFAECOKPNABMPAE
PenicillinsPenicillin85.693.746.890.510.9    
Ampicillin   90.30.770.698.2  
Oxacillin43.380.3       
Penicillin/beta-lactamase inhibitor combinationsAmoxicillin-clavulanate     24.625.3  
Ampicillin-sulbactam     26.744.3  
Piperacillin-tazobactam     5.630.180.222.9
Sulbactam-durlobactam       0.0 
CephalosporinsCefazolin (1st GC)     45.137.8  
Cefuroxime (2nd GC)     39.548.9  
Cefoxitin (2nd GC)60.0    9.424.6  
Cefotetan (2nd GC)         
Cefotaxime (3rd GC)  27.1  38.842.7  
Ceftriaxone (3rd GC)  15.6  38.645.9  
Ceftazidime (3rd GC)       83.221.8
Cefepime (4th GC)     27.938.571.016.0
Ceftaroline (5th GC)5.7        
Cefiderocol         
Ceftazidime-avibactam     0.94.6 14.3
Ceftolozane-tazobactam        40.0
CarbapenemsImipenem     1.217.578.524.5
Meropenem  62.5  1.418.777.921.1
Ertapenem     1.415.2  
Imipenem-relebactam         
Meropenem- vaborbactam         
GlycopeptidesVancomycin0.00.00.035.40.3    
LipopeptidesDaptomycin0.00.0 30.80.4    
MacrolidesAzithromycin31.453.5       
Clarithromycin         
Erythromycin30.263.487.9      
LincosamidesClindamycin21.142.873.5      
TetracyclinesTetracycline12.519.676.6  41.536.8  
Doxycycline         
Minocycline2.70.4     8.2 
AminoglycosidesGentamicin     24.418.668.3 
Gentamicin (High-level)   31.440.3    
Tobramycin     19.324.569.510.9
Amikacin     0.81.552.1 
Streptomycin (High-level)   9.912.6    
Plazomicin         
FluoroquinolonesCiprofloxacin     50.942.579.028.8
Levofloxacin  8.0  53.846.071.528.7
Moxifloxacin  6.1      
Folate pathway inhibitorsTrimethoprim-sulfamethoxazole1.441.939.2  37.437.965.1 
OxazolidinonesLinezolid0.20.0 0.50.6    
Tedizolid         
RifamycinsRifampin3.613.3       
PleuromutilinsLefamulin         
Total No. of isolates46,58441,3131,35423,45219,099179,94596,86913,83720,196

The numbers in the cells indicate the antibiotic resistance rate of all investigated isolates, without distinguishing between the first isolate group and the duplicate group.
Abbreviations: SAU, Staphylococcus aureus; SEP, Staphylococcus epidermidis; SPN, Streptococcus pneumoniae; EFM, Enterococcus faecium; EFA, Enterococcus faecalis; ECO, Escherichia coli; KPN, Klebsiella pneumoniae; ABM, Acinetobacter baumannii; PAE, Pseudomonas aeruginosa.

Table 1
Table 2
Table 3
Table 4

1. O’Neill J. Tackling drug-resistant infections globally: final report and recommendations. London; Wellcome Trust, 2016: 84.

2. GBD 2021 Antimicrobial Resistance Collaborators. Global burden of bacterial antimicrobial resistance 1990-2021: a systematic analysis with forecasts to 2050. Lancet 2024;404:1199-226.

3. Rudd KE, Johnson SC, Agesa KM, Shackelford KA, Tsoi D, Kievlan DR, et al. Global, regional, and national sepsis incidence and mortality, 1990-2017: analysis for the Global Burden of Disease Study. Lancet 2020;395:200-11.

4. European Centre for Disease Prevention and Control, World Health Organization. Antimicrobial resistance surveillance in Europe 2023-2021 data. WHO Web site on infectious diseases. https://www.who.int/europe/publications/i/item/9789289058537 [Online] (last visited on 16 June 2025).

5. World Health Organization. Global antimicrobial resistance and use surveillance system (GLASS) report. Antibiotic use data for 2022. Geneva; World Health Organization, 2025.

6. World Health Organization. WHO bacterial priority pathogens list, 2024: bacterial pathogens of public health importance to guide research, development and strategies to prevent and control antimicrobial resistance. Geneva; World Health Organization, 2024.

7. Sabbatucci M, Ashiru-Oredope D, Barbier L, Bohin E, Bou-Antoun S, Brown C, et al. Tracking progress on antimicrobial resistance by the quadripartite country self-assessment survey (TrACSS) in G7 countries, 2017-2023: opportunities and gaps. Pharmacol Res 2024;204:107188.

8. Korea Disease Control and Prevention Agency. National Antimicrobial Resistance Surveillance Report 2023. Cheongju; Korea Disease Control and Prevention Agency, 2023.

9. Hwang YJ. Comparing the phylogenetic distribution of multilocus sequence typing, staphylococcal protein A, and staphylococcal cassette chromosome mec types in methicillin-resistant Staphylococcus aureus (MRSA) in Korea from 1994 to 2020. Antibiotics 2023;12:1397.

10. Yamaguchi T, Nakamura I, Sato T, Ono D, Sato A, Sonoda S, et al. Changes in the genotypic characteristics of community-acquired methicillin-resistant Staphylococcus aureus collected in 244 medical facilities in Japan between 2010 and 2018: a nationwide surveillance. Microbiol Spectr 2022;10:e0227221.

11. Sadeghi Moghaddam T, Namaei MH, Afshar D, Yousefi M. High frequency of SCCmec type IV and multidrug-resistant SCCmec type I among hospital acquired methicillin-resistant Staphylococcus aureus isolates in Birjand Imam Reza Hospital, Iran. Iran J Microbiol 2022;14:67-75.

12. Naimi HM, Tristan A, Bes M, Vandenesch F, Nazari QA, Laurent F, et al. Molecular characterization and antimicrobial resistance of nasal Staphylococcus aureus in the community of Kabul. J Glob Antimicrob Resist 2023;34:18-22.

13. Jung J, Yoo RN, Sung H, Kim M, Lee J. Antibiotics susceptability of Streptococcus pneumoniae isolated from single tertiary childrens’ hospital since 2014 and choice of appropriate empirical antibiotics. Pediatr Infect Vaccine 2019;26:1-10.

14. Piezzi V, Wassilew N, Atkinson A, D’Incau S, Kaspar T, Seth-Smith HM, et al. Nosocomial outbreak of vancomycin-resistant Enterococcus faecium (VRE) ST796, Switzerland, 2017 to 2020. Euro Surveill 2022;27:2200285.

15. Werner G, Neumann B, Weber RE, Kresken M, Wendt C, Bender JK, et al. Thirty years of VRE in Germany – “expect the unexpected”: the view from the National Reference Centre for Staphylococci and Enterococci. Drug Resist Updat 2020;53:100732.

16. Shahini Shams Abadi M, Taji A, Salehi F, Kazemian H, Heidari H. High-level gentamicin resistance among clinical isolates of enterococci in Iran: a systematic review and meta-analysis. Folia Med 2021;63:15-23.

17. Harbaoui S, Ferjani S, Abbassi MS, Saidani M, Gargueh T, Ferjani M, et al. Genetic heterogeneity and predominance of blaCTX-M-15 in cefotaxime-resistant Enterobacteriaceae isolates colonizing hospitalized children in Tunisia. Lett Appl Microbiol 2022;75:1460-74.

18. Park JJ, Seo YB, Lee J, Eom JS, Song W, Choi YK, et al. Positivity of carbapenemase-producing Enterobacteriaceae in patients following exposure within long-term care gfacilities in Seoul, Korea. J Korean Med Sci 2020;35:e303.

19. Hong JS, Park BY, Kim D, Kim K, Lee KH, Cho NH, et al. Epidemiological study of an outbreak of KPC-2-producing Klebsiella pneumoniae in a tertiary hospital in Korea. Ann Clin Microbiol 2020;23:81-92.

20. Chong YP. Changing epidemiology of multidrug-resistant pathogens: a new battle against carbapenem-resistant Enterobacterales. Korean J healthc assoc Infect Control Prev 2023;28:243-4.

21. Kim SY, Shin J, Shin SY, Ko KS. Characteristics of carbapenem-resistant Enterobacteriaceae isolates from Korea. Diagn Microbiol Infect Dis 2013;76:486-90.

22. Park SH, Park SH, Kim JS, Yu JK, Kim JK, Suh HS, et al. Genetic distribution of carbapenem-resistant Enterobacteriaceae in Seoul Korea, 2018-2020. J Bacteriol Virol 2022;52:28-38.

23. van Duin D, Arias CA, Komarow L, Chen L, Hanson BM, Weston G, et al. Molecular and clinical epidemiology of carbapenem-resistant Enterobacterales in the USA (CRACKLE-2): a prospective cohort study. Lancet Infect Dis 2020;20:731-41.

24. Qiao S, Xin S, Zhu Y, Zhao F, Wu H, Zhang J, et al. A large-scale surveillance revealed that KPC variants mediated ceftazidime-avibactam resistance in clinically isolated Klebsiella pneumoniae. Microbiol Spectr 2024;12:e0025824.

25. Lee YL, Ko WC, Hsueh PR. Geographic patterns of Acinetobacter baumannii and carbapenem resistance in the Asia-Pacific Region: results from the Antimicrobial Testing Leadership and Surveillance (ATLAS) program, 2012-2019. Int J Infect Dis 2023;127:48-55.

26. Choi YJ, Kim YA, Junglim K, Jeong SH, Shin JH, Shin KS, et al. Emergence of NDM1-producing Pseudomonas aeruginosa sequence type 773 clone: shift of carbapenemase molecular epidemiology and spread of 16S rRNA methylase genes in Korea. Ann Lab Med 2023;43:196-9.

27. Wang MG, Liu ZY, Liao XP, Sun RY, Li RB, Liu Y, et al. Retrospective data insight into the global distribution of carbapenemase-producing Pseudomonas aeruginosa. Antibiotics 2021;10:548.

28. Abniki R, Tashakor A, Masoudi M, Mansury D. Global resistance of imipenem/relebactam against gram-negative bacilli: systematic review and meta-analysis. Curr Ther Res Clin Exp 2024;100:100723.

29. Karakonstantis S, Rousaki M, Vassilopoulou L, Kritsotakis EI. Global prevalence of cefiderocol non-susceptibility in Enterobacterales, Pseudomonas aeruginosa, Acinetobacter baumannii, and Stenotrophomonas maltophilia: a systematic review and meta-analysis. Clin Microbiol Infect 2024;30:178-88.

30. Alawi MM, Tashkandi WA, Basheikh MA, Warshan FM, Ghobara HA, Ramos RB, et al. Effectiveness of antimicrobial stewardship program in long-term care: a five-year prospective single-center study. Interdiscip Perspect Infect Dis 2022;2022:8140429.

31. Sumathi S, Venkateswarlu K. The impact of antimicrobial stewardship programs on antimicrobial resistance patterns in a tertiary care hospital: an observational study. J Adv Med Pharm Sci 2023;6:300-4.

32. Timbrook TT, Hurst JM, Bosso JA. Impact of an antimicrobial stewardship program on antimicrobial utilization, bacterial susceptibilities, and financial expenditures at an academic medical center. Hosp Pharm 2016;51:703-11.

33. Banan MA, Nazzal MA, Abdelhaq AI, Abutaha SA, Zyoud SH, Sabateen A. Impact of an antibiotic stewardship program on antibiotic utilization, bacterial susceptibilities, and cost of antibiotics. Sci Rep 2023;13:5040.

34. Lee S, Kim Y, Kim D, Seo S, Kim S, Shin N. Analysis of antimicrobial use in Korean longterm care hospitals, 2020-2022. Public Health Wkly Rep 2025;18:225-43.