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Public Health Weekly Report 2025; 18(2): 75-89

Published online December 11, 2024

https://doi.org/10.56786/PHWR.2025.18.2.2

© The Korea Disease Control and Prevention Agency

Characteristics of Notified Carbapenem-resistant Enterobacterales Cases in the Republic of Korea, 2023

Hyunju Lee , Seungjae Lee , Yeon Hwa Jung , Jihyun Choi , Sook-kyung Park *

Division of Healthcare Associated Infection Control, Department of Healthcare Safety and Immunization, Korea Disease Control and Prevention Agency, Cheongju, Korea

*Corresponding author: Sook-kyung Park, Tel: +82-43-719-7580, E-mail: monica23@korea.kr

Received: October 31, 2024; Revised: December 9, 2024; Accepted: December 10, 2024

This is an Open Access aritcle distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) which permits unrestricted distribution, and reproduction in any medium, provided the original work is properly cited.

Carbapenem-resistant Enterobacterales (CRE) infections are increasing worldwide and have become a major public health threat. The Centers for Disease Control and Prevention reported that “the coronavirus disease-19 (COVID-19) pandemic has led to a surge in CRE infections as healthcare facilities have prioritized COVID-19 infection control, making routine infection prevention and control more difficult.” and the World Health Organization estimated 4.95 million people deaths worldwide in 2019 due to antibiotic-resistant bacteria. The annual number of CRE infection cases has been increasing by about 20–30%. In 2023, an analysis of CRE infection reports revealed a total of 38,405 cases, with 55.4% of patients being male. Most cases (65.2%) occurred in individuals aged 70 years and older. Among healthcare facilities, general hospitals had the highest reporting rate at 43.3%. In particular, the number of CRE infection reports in long-term care hospitals and the proportion of total reports increased every year, from 1,077 cases (7.0%) in 2019 to 5,815 cases (15.1%) in 2023. The primary bacteria identified were Klebsiella pneumoniae (72.4%) and Escherichia coli (14.1%). Among CRE infections, carbapenemase-producing Enterobacterales (CP-CRE) infections accounted for 73.7% of all reported cases in 2023, with the proportion of CP-CRE infections steadily increasing every year. Therefore, this study analyzed CRE infection data reported through the Korea Disease Control and Prevention Agency system from 2019 to 2023, thereby providing important insights for the development of effective infection prevention and management strategies.

Key words Carbapenem-resistant Enterobacterales; Carbapenemase-producing Enterobacterales; Drug resistance, microbial

Key messages

① What is known previously?

Domestic carbapenem-resistant Enterobacterales (CRE) infection case have increased by 20–30% every year since 2019. Recently, carbapenemase-producing Enterobacterales (CP-CRE) infections accounted for more than 70% of the reported cases, and this proportion is gradually increasing.

② What new information is presented?

Among the CRE (38,405 cases) reported in 2023, the proportion of general hospitals was the highest at 43.3% and the reporting rate of CRE infections in long-term care hospitals increased from 7.0% in 2019 to 15.1% in 2023. The CP-CRE infection rate was 73.7% (28,318 cases), and the number of reporting healthcare facilities increased by 27.4% compared with the previous year (1,117 healthcare facilities).

③ What are implications?

This report provides data for formulating effective strategies for infection prevention and control, while also highlighting that surveillance and infection control are necessary to control the spread of CRE.

The prevalence of carbapenem-resistant Enterobacterales (CRE) infections has significantly increased in recent years, posing a major public health threat [1-3]. The coronavirus disease 2019 (COVID-19) pandemic has exacerbated this trend due to factors such as insufficient healthcare resources, inadequate infection control practices, and increased antibiotic use [4].

CRE infections are caused by Enterobacterales that exhibit resistance to carbapenems. Transmission primarily occurs through direct or indirect contact with infected individuals or contaminated environments. The likelihood of occurrence is greater in long-term inpatients, those taking immunosuppressive medications, and those with a history of CRE infections [5]. Of particular concern are carbapenemase-producing Enterobacterales (CP-CRE), which have emerged as a significant threat in outbreaks due to their ability to transfer resistance genes to other bacteria via plasmids or other mechanisms, enabling rapid transmission [6]. Recent data on CRE infections in the Republic of Korea (ROK) reveal a steady increase in the prevalence of CP-CRE among CRE, highlighting the urgent need for proactive measures to control outbreaks in healthcare settings [7,8].

This report presents a comparative and analytical overview of the incidence and epidemiological characteristics of CRE infections over the past 5 years (2019–2023), aiming to shed light on the evolving patterns of these infections.

A comprehensive analysis of demographic (sex and age) and epidemiological characteristics (e.g., region, type of healthcare facility, infectious disease patient classification, isolate, carbapenemase type) was conducted. Data were collected from three primary sources: (1) CRE infection case reports, (2) CRE infection investigation reports, and (3) CP-CRE infection case reports. These reports were obtained from the Korea Disease Control and Prevention Agency’s Integrated Disease and Health Management System and span the period from 2019 to 2023. The analysis was based on the reporting dates of infectious disease in healthcare facilities. Results from 2019 to 2022 were drawn from the Annual Report on the Notified Infectious Diseases in Korea and the CRE Infectious Disease Analysis Report [7,8].

1. Carbapenem-resistant Enterobacterales Infection Report Status

CRE infection, classified as Class 2 infectious disease, is monitored through a mandatory surveillance system. Since its implementation in June 2017, the number of reported cases has increased by 20–30% annually. In 2023, a total of 38,405 cases were reported from 1,467 healthcare facilities (Table 1).

Table 1. Number of CREㆍCP-CRE designated and healthcare facilities by year (2019–2023)
Category20192020202120222023
CRE infectionNo. of cases15,36918,11323,31130,54838,405
No. of healthcare facilities (place)8319381,0671,2571,467
CP-CRE infectionNo. of cases8,88711,21814,76921,69528,318
No. of CP-CRE healthcare facilities (place)*6226707178771,117
CP-CRE/CRE ratio (%)57.861.963.471.073.7

CRE=carbapenem-resistant Enterobacterales; CP-CRE=carbapenemase-producing Enterobacterales. *Number of healthcare facilities where at least one case of CP-CRE occurred in the year.



The demographic characteristics of CRE infections reported in 2023 showed that 55.4% (21,293 cases) were male and 65.2% (25,057 cases) were aged ≥70 years. Other age groups included 18.5% (7,112 cases) aged 60–69 years and 8.9% (3,416 cases) aged 50–59 years. Those aged ≥70 years accounted for 58.8% (9,031 cases) of all reports in 2019 and 65.2% (25,057 cases) in 2023, with the proportion increasing annually. Regarding healthcare facility type, 43.3% (16,648 cases) were from general hospitals, 35.0% (13,443 cases) from advanced general hospitals, 15.1% (5,815 cases) from long-term care hospitals, and 5.5% (2,105 cases) from hospitals. In particular, the number and percentage of long-term care hospital reports increased from 7.0% (1,077 cases) in 2019, 8.2% (1,485 cases) in 2020, and 10.2% (2,383 cases) in 2021, 12.3% (3,760 cases) in 2022, and 15.1% (5,815 cases) in 2023.

Furthermore, an analysis of the 2023 notification data according to the CRE infectious disease classification criteria revealed that 5.4% (2,067 cases) of “patients” had CRE detected in blood and 94.6% (36,338 cases) of “pathogen carriers” had CRE detected in clinical specimens other than blood (Table 2).

Table 2. Characteristics of carbapenem-resistant Enterobacterales (2019–2023)
Category20192020202120222023
Total15,36918,11323,31130,54838,405
Sex
Male8,727 (56.8)10,210 (56.4)13,362 (57.3)17,036 (55.8)21,293 (55.4)
Female6,642 (43.2)7,903 (43.6)9,949 (42.7)13,512 (44.2)17,112 (44.6)
Age group
0–19333 (2.2)311 (1.7)336 (1.4)341 (1.1)456 (1.2)
20–39513 (3.3)502 (2.8)667 (2.9)784 (2.6)895 (2.3)
40–49760 (4.9)774 (4.3)1,042 (4.5)1,246 (4.1)1,469 (3.8)
50–591,789 (11.6)2,035 (11.2)2,372 (10.2)2,914 (9.5)3,416 (8.9)
60–692,943 (19.1)3,405 (18.8)4,587 (19.7)5,864 (19.2)7,112 (18.5)
≥709,031 (58.8)11,086 (61.2)14,307 (61.4)19,399 (63.5)25,057 (65.2)
Healthcare facility type
Advanced general hospital6,266 (40.8)7,099 (39.2)9,442 (40.5)11,737 (38.4)13,443 (35.0)
General hospital6,803 (44.3)8,013 (44.2)9,786 (42.0)13,298 (43.5)16,648 (43.3)
Hospital1,093 (7.1)1,380 (7.6)1,512 (6.5)1,515 (5.0)2,105 (5.5)
Long-term care hospital1,077 (7.0)1,485 (8.2)2,383 (10.2)3,760 (12.3)5,815 (15.1)
Others*130 (0.8)136 (0.8)188 (0.8)238 (0.8)394 (1.0)
Case classification
Patient of an infectious disease774 (5.0)972 (5.4)1,312 (5.6)1,897 (6.2)2,067 (5.4)
Pathogen carrier14,595 (95.0)17,141 (94.6)21,999 (94.4)28,651 (93.8)36,338 (94.6)

Values are presented as number (%). *Others=clinic level, dentistryㆍKorea’s traditional medicine hospitals.



Of the 38,405 reports of CRE infections in 2023, a total of 36,680 (95.5%) were registered in individual investigation reports, with Klebsiella pneumoniae accounting for 72.4% (26,553 cases), Escherichi coli 14.1% (5,155 cases), Enterobacter spp. 6.0% (2,215 cases), Citrobacter freundii 1.9% (681 cases), and Citrobacter koseri 1.3% (466 cases) of the isolates. The five most common isolates over the past 5 years have largely maintained their rankings as a percentage of the total from 2019 to 2023. Notably , the prevalence of K. pneumoniae has steadily increased since 2019: 60.4% in 2019, 62.6% in 2020, 68.6% in 2021, 70.9% in 2022, and 72.4% in 2023 (Supplementary Table 1; available online).

2. Carbapenemase-producing Enterobacterales Infection Report Status

Of the 38,405 CRE infections reported in 2023, the proportion of CP-CRE infections was 73.7%, with a total of 28,318 cases confirmed in 1,117 healthcare facilities. The proportion of CP-CRE infections increased annually throughout the study period, with 57.8% (8,887 cases) in 2019, 61.9% (11,218 cases) in 2020, 63.4% (14,769 cases) in 2021, 71.0% (21,695 cases) in 2022, and 73.7% (28,318 cases) in 2023 (Table 1).

The distribution of carbapenemases was 77.4% (21,907 cases) for Klebsiella pneumoniae carbapenemase (KPC), 15.9% (4,487 cases) for New Delhi metallo-β-lactamase (NDM), and 6.2% (1,766 cases) for oxacillinase (OXA). The three genotypes that have consistently dominated from 2019 to 2023, in their proportional rankings over time. Notably, since 2019, the proportion of KPCs among all carbapenemases has continued to increase, whereas the proportion of NDMs has decreased (Supplementary Table 2; available online).

A regional analysis of carbapenemases showed that the prevalence of KPC was 27.3% (5,991 cases) in Seoul, 24.6% (5,388 cases) in Gyeonggi-do, and 8.0% (1,743 cases) in Gyeongsangnam-do. The prevalence of NDM was 32.0% (1,436 cases) in Seoul, 22.0% (988 cases) in Gyeonggi-do, and 14.5% (652 cases) in Incheon. The prevalence of OXA was 34.1% (603 cases) in Seoul, 20.5% (362 cases) in Gyeonggi-do, and 11.2% (197 cases) in Incheon (Figure 1, Table 3).

Figure 1. Geographical distribtuion map of CP-CRE Infection by carbapenemase genotype in region 2023
CP-CRE=carbapenemase-producing Enterobacterales; KPC=Klebsiella pneumoniae carbapenemase; NDM=New Delhi metallo-β-lactamase; OXA=oxacillinase; Etc.=Verona integron-encoded metallo-β-lactamase, Imipenemase, Guiana extended spectrum β-lactamase.

Table 3. Distribtuion of carbapenemase-producing Enterobacterales by carbapenemase genotype in region 2023
RegionTotalKPCNDMOXAEtc.*
Total28,31821,9074,4871,766158
Seoul8,065 (28.5)5,991 (27.3)1,436 (32.0)603 (34.1)35 (22.2)
Busan2,121 (7.5)1,738 (7.9)304 (6.8)74 (4.2)5 (3.2)
Daegu1,488 (5.3)1,264 (5.8)173 (3.9)40 (2.3)11 (7.0)
Incheon2,425 (8.6)1,559 (7.1)652 (14.5)197 (11.2)17 (10.8)
Gwangju706 (2.5)450 (2.1)79 (1.8)176 (10.0)1 (0.6)
Daejeon693 (2.4)506 (2.3)154 (3.4)30 (1.7)3 (1.9)
Ulsan268 (0.9)225 (1.0)34 (0.8)8 (0.5)1 (0.6)
Sejong28 (0.1)23 (0.1)5 (0.1)0 (0.0)0 (0.0)
Gyeonggi6,780 (23.9)5,388 (24.6)988 (22.0)362 (20.5)42 (26.6)
Gangwon539 (1.9)448 (2.0)41 (0.9)48 (2.7)2 (1.3)
Chungbuk298 (1.1)229 (1.0)41 (0.9)26 (1.5)2 (1.3)
Chungnam588 (2.1)501 (2.3)71 (1.6)16 (0.9)0 (0.0)
Jeonbuk960 (3.4)759 (3.5)84 (1.9)111 (6.3)6 (3.8)
Jeonnam410 (1.4)273 (1.2)78 (1.7)45 (2.5)14 (8.9)
Gyeongbuk771 (2.7)662 (3.0)98 (2.2)3 (0.2)8 (5.1)
Gyengnam2,007 (7.1)1,743 (8.0)232 (5.2)21 (1.2)11 (7.0)
Jeju171 (0.6)148 (0.7)17 (0.4)6 (0.3)0 (0.0)

Values are presented as number (%). KPC=Klebsiella pneumoniae carbapenemase; NDM=New Delhi metallo-β-lactamase; OXA=oxacillinase; *Etc.=Verona integron-encoded metallo-β-lactamase, Imipenemase, Guiana extended spectrum β-lactamase.


The prevalence of CRE infections is increasing both domestically and globally. The Centers for Disease Control and Prevention reported a 35.0% increase in healthcare-associated CRE infections in 2020, coinciding with the COVID-19 pandemic, compared with that in the previous year, as noted in the 「COVID-19: U.S. impact on antimicrobial resistance, special report 2022」 report. This surge peaked in 2021 and persisted above pre-pandemic levels in 2022 [4].

In the ROK, since mandatory CRE infection surveillance began in June 2017, the number of reported cases and reporting healthcare facilities continues to increased. In particular, reports from long-term care hospitals (the number of reporting healthcare facilities) increased markedly from 1,458 cases (322 facilities) in 2020 to 5,815 cases (566 facilities) in 2023. This represents a 4.0-fold increase in cases and a 1.8-fold increase in the number of reporting healthcare facilities. As indicated by the testing status, the proportion of fecal specimens among all positive specimens in long-term care hospitals increased from 2,441 cases (69.2%) in 2020 to 8,558 cases (73.6%) in 2023. This suggests that preemptive and contact testing are being actively implemented to manage CRE patients.

Long-term care hospitals, which primarily admit elderly and rehabilitation patients with chronic diseases, pose unique challenges [9]. The average length of stay in all healthcare facilities is 16.1 days, with an average length of stay of 134.4 days in long-term care hospitals [10,11]. The risk of CRE infection may be increased due to the multi-bedded structure of long-term care hospitals and the lack of infection control staff and resources.

To address these challenges, the ROK is implementing measures to prevent the spread of CRE infections. These measures include facility and environmental management improvements, including long-term care hospitals, expansion of infection control systems, and reorganization of healthcare-related infection response frameworks. Efforts are also underway to strengthen infection control personnel capabilities through administrative and financial assistance, including reimbursement systems.

A comparison of international isolate distributions with European Centre for Disease Prevention and Control surveillance data for only certain bacteria such as K. pneumoniae and E. coli reveals discrepancies between the datasets. These discrepancies make absolute comparisons difficult. However, it is notable that the percentages of carbapenem resistance in K. pneumoniae increased from 8.5% in 2018 to 10.9% in 2022. These findings suggest that CRE infections are increasing globally [12]. The World Health Organization (WHO) has classified CRE as a “critical pathogen with the highest priority for research, development, and public health action to prevent and control antimicrobial resistance” in its “WHO bacterial priority pathogens list, 2024” report. The WHO also emphasized the need for international efforts to address antimicrobial resistance, including the implementation of robust infection prevention and control measures, the surveillance of emerging trends, the advancement of drug development, and the creation of diagnostic and prevention tools [2].

Global strategies to reduce CRE infections include healthcare providers identifying and mitigating risk factors, emphasizing hand hygiene, personal protective equipment use, and proper environmental disinfection for infection control, and prescribing antibiotics judiciously and conducting preemptive testing for “asymptomatic carriers” [13]. In the ROK, the government is developing a response system to prevent the spread of CRE infections. This system will be a feasible, on-site one in healthcare facilities to evaluate CRE prevalence and to design and pilot a reduction strategy, establishing a foundation for systematic surveillance, prevention, and management of CRE infections.

The occurrence and distribution of infectious diseases were analyzed using basic statistical methods based on CRE case and investigation reports. This report highlights the growing burden of CRE infections in Korean healthcare facilities, necessitating active surveillance and reinforced infection prevention and control measures. Collaborative efforts among the government, local authorities, and healthcare facilities will be essential to curbing the spread of this significant public health threat.

Ethics Statement: Not applicable.

Funding Source: None.

Acknowledgments: None.

Conflict of Interest: The authors have no conflicts of interest to declare.

Author Contributions: Conceptualization: HJL. Data curation: HJL. Formal analysis: HJL. Investigation: HJL, JHC Methodology: HJL, SJL. Project administration: SJL, HJL. Software: HJL. Supervision: SKP, SJL, HJL. Validation: HJL. Visualization: HJL. Writing – original draft: HJL. Writing – review & editing: SKP, SJL, YHJ, JHC.

Supplementary data are available online.

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    Available from: https://www.who.int/publications/i/item/9789290620112
  4. Centers for Disease Control and Prevention (CDC). COVID-19: U.S. impact on antimicrobial resistance, special report 2022 [Internet]. CDC; 2022 [cited 2024 Oct 30].
    Available from: https://www.cdc.gov/antimicrobial-resistance/data-research/threats/COVID-19.html
  5. Pérez-Galera S, Bravo-Ferrer JM, Paniagua M, et al; COMBACTE-CARE-EURECA Team. Risk factors for infections caused by carbapenem-resistant Enterobacterales: an international matched case-control-control study (EURECA). EClinicalMedicine 2023;57:101871.
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    Available from: https://www.mohw.go.kr/board.es?mid=a10411010200&bid=0019&act=view&list_no=372195
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Surveillance Reports

Public Health Weekly Report 2025; 18(2): 75-89

Published online January 9, 2025 https://doi.org/10.56786/PHWR.2025.18.2.2

Copyright © The Korea Disease Control and Prevention Agency.

Characteristics of Notified Carbapenem-resistant Enterobacterales Cases in the Republic of Korea, 2023

Hyunju Lee , Seungjae Lee , Yeon Hwa Jung , Jihyun Choi , Sook-kyung Park *

Division of Healthcare Associated Infection Control, Department of Healthcare Safety and Immunization, Korea Disease Control and Prevention Agency, Cheongju, Korea

Correspondence to:*Corresponding author: Sook-kyung Park, Tel: +82-43-719-7580, E-mail: monica23@korea.kr

Received: October 31, 2024; Revised: December 9, 2024; Accepted: December 10, 2024

This is an Open Access aritcle distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) which permits unrestricted distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Carbapenem-resistant Enterobacterales (CRE) infections are increasing worldwide and have become a major public health threat. The Centers for Disease Control and Prevention reported that “the coronavirus disease-19 (COVID-19) pandemic has led to a surge in CRE infections as healthcare facilities have prioritized COVID-19 infection control, making routine infection prevention and control more difficult.” and the World Health Organization estimated 4.95 million people deaths worldwide in 2019 due to antibiotic-resistant bacteria. The annual number of CRE infection cases has been increasing by about 20–30%. In 2023, an analysis of CRE infection reports revealed a total of 38,405 cases, with 55.4% of patients being male. Most cases (65.2%) occurred in individuals aged 70 years and older. Among healthcare facilities, general hospitals had the highest reporting rate at 43.3%. In particular, the number of CRE infection reports in long-term care hospitals and the proportion of total reports increased every year, from 1,077 cases (7.0%) in 2019 to 5,815 cases (15.1%) in 2023. The primary bacteria identified were Klebsiella pneumoniae (72.4%) and Escherichia coli (14.1%). Among CRE infections, carbapenemase-producing Enterobacterales (CP-CRE) infections accounted for 73.7% of all reported cases in 2023, with the proportion of CP-CRE infections steadily increasing every year. Therefore, this study analyzed CRE infection data reported through the Korea Disease Control and Prevention Agency system from 2019 to 2023, thereby providing important insights for the development of effective infection prevention and management strategies.

Keywords: Carbapenem-resistant Enterobacterales, Carbapenemase-producing Enterobacterales, Drug resistance, microbial

Body

Key messages

① What is known previously?

Domestic carbapenem-resistant Enterobacterales (CRE) infection case have increased by 20–30% every year since 2019. Recently, carbapenemase-producing Enterobacterales (CP-CRE) infections accounted for more than 70% of the reported cases, and this proportion is gradually increasing.

② What new information is presented?

Among the CRE (38,405 cases) reported in 2023, the proportion of general hospitals was the highest at 43.3% and the reporting rate of CRE infections in long-term care hospitals increased from 7.0% in 2019 to 15.1% in 2023. The CP-CRE infection rate was 73.7% (28,318 cases), and the number of reporting healthcare facilities increased by 27.4% compared with the previous year (1,117 healthcare facilities).

③ What are implications?

This report provides data for formulating effective strategies for infection prevention and control, while also highlighting that surveillance and infection control are necessary to control the spread of CRE.

Introduction

The prevalence of carbapenem-resistant Enterobacterales (CRE) infections has significantly increased in recent years, posing a major public health threat [1,-3]. The coronavirus disease 2019 (COVID-19) pandemic has exacerbated this trend due to factors such as insufficient healthcare resources, inadequate infection control practices, and increased antibiotic use [4].

CRE infections are caused by Enterobacterales that exhibit resistance to carbapenems. Transmission primarily occurs through direct or indirect contact with infected individuals or contaminated environments. The likelihood of occurrence is greater in long-term inpatients, those taking immunosuppressive medications, and those with a history of CRE infections [5]. Of particular concern are carbapenemase-producing Enterobacterales (CP-CRE), which have emerged as a significant threat in outbreaks due to their ability to transfer resistance genes to other bacteria via plasmids or other mechanisms, enabling rapid transmission [6]. Recent data on CRE infections in the Republic of Korea (ROK) reveal a steady increase in the prevalence of CP-CRE among CRE, highlighting the urgent need for proactive measures to control outbreaks in healthcare settings [7,8].

This report presents a comparative and analytical overview of the incidence and epidemiological characteristics of CRE infections over the past 5 years (2019–2023), aiming to shed light on the evolving patterns of these infections.

Methods

A comprehensive analysis of demographic (sex and age) and epidemiological characteristics (e.g., region, type of healthcare facility, infectious disease patient classification, isolate, carbapenemase type) was conducted. Data were collected from three primary sources: (1) CRE infection case reports, (2) CRE infection investigation reports, and (3) CP-CRE infection case reports. These reports were obtained from the Korea Disease Control and Prevention Agency’s Integrated Disease and Health Management System and span the period from 2019 to 2023. The analysis was based on the reporting dates of infectious disease in healthcare facilities. Results from 2019 to 2022 were drawn from the Annual Report on the Notified Infectious Diseases in Korea and the CRE Infectious Disease Analysis Report [7,8].

Results

1. Carbapenem-resistant Enterobacterales Infection Report Status

CRE infection, classified as Class 2 infectious disease, is monitored through a mandatory surveillance system. Since its implementation in June 2017, the number of reported cases has increased by 20–30% annually. In 2023, a total of 38,405 cases were reported from 1,467 healthcare facilities (Table 1).

Number of CREㆍCP-CRE designated and healthcare facilities by year (2019–2023)
Category20192020202120222023
CRE infectionNo. of cases15,36918,11323,31130,54838,405
No. of healthcare facilities (place)8319381,0671,2571,467
CP-CRE infectionNo. of cases8,88711,21814,76921,69528,318
No. of CP-CRE healthcare facilities (place)*6226707178771,117
CP-CRE/CRE ratio (%)57.861.963.471.073.7

CRE=carbapenem-resistant Enterobacterales; CP-CRE=carbapenemase-producing Enterobacterales. *Number of healthcare facilities where at least one case of CP-CRE occurred in the year..



The demographic characteristics of CRE infections reported in 2023 showed that 55.4% (21,293 cases) were male and 65.2% (25,057 cases) were aged ≥70 years. Other age groups included 18.5% (7,112 cases) aged 60–69 years and 8.9% (3,416 cases) aged 50–59 years. Those aged ≥70 years accounted for 58.8% (9,031 cases) of all reports in 2019 and 65.2% (25,057 cases) in 2023, with the proportion increasing annually. Regarding healthcare facility type, 43.3% (16,648 cases) were from general hospitals, 35.0% (13,443 cases) from advanced general hospitals, 15.1% (5,815 cases) from long-term care hospitals, and 5.5% (2,105 cases) from hospitals. In particular, the number and percentage of long-term care hospital reports increased from 7.0% (1,077 cases) in 2019, 8.2% (1,485 cases) in 2020, and 10.2% (2,383 cases) in 2021, 12.3% (3,760 cases) in 2022, and 15.1% (5,815 cases) in 2023.

Furthermore, an analysis of the 2023 notification data according to the CRE infectious disease classification criteria revealed that 5.4% (2,067 cases) of “patients” had CRE detected in blood and 94.6% (36,338 cases) of “pathogen carriers” had CRE detected in clinical specimens other than blood (Table 2).

Characteristics of carbapenem-resistant Enterobacterales (2019–2023)
Category20192020202120222023
Total15,36918,11323,31130,54838,405
Sex
Male8,727 (56.8)10,210 (56.4)13,362 (57.3)17,036 (55.8)21,293 (55.4)
Female6,642 (43.2)7,903 (43.6)9,949 (42.7)13,512 (44.2)17,112 (44.6)
Age group
0–19333 (2.2)311 (1.7)336 (1.4)341 (1.1)456 (1.2)
20–39513 (3.3)502 (2.8)667 (2.9)784 (2.6)895 (2.3)
40–49760 (4.9)774 (4.3)1,042 (4.5)1,246 (4.1)1,469 (3.8)
50–591,789 (11.6)2,035 (11.2)2,372 (10.2)2,914 (9.5)3,416 (8.9)
60–692,943 (19.1)3,405 (18.8)4,587 (19.7)5,864 (19.2)7,112 (18.5)
≥709,031 (58.8)11,086 (61.2)14,307 (61.4)19,399 (63.5)25,057 (65.2)
Healthcare facility type
Advanced general hospital6,266 (40.8)7,099 (39.2)9,442 (40.5)11,737 (38.4)13,443 (35.0)
General hospital6,803 (44.3)8,013 (44.2)9,786 (42.0)13,298 (43.5)16,648 (43.3)
Hospital1,093 (7.1)1,380 (7.6)1,512 (6.5)1,515 (5.0)2,105 (5.5)
Long-term care hospital1,077 (7.0)1,485 (8.2)2,383 (10.2)3,760 (12.3)5,815 (15.1)
Others*130 (0.8)136 (0.8)188 (0.8)238 (0.8)394 (1.0)
Case classification
Patient of an infectious disease774 (5.0)972 (5.4)1,312 (5.6)1,897 (6.2)2,067 (5.4)
Pathogen carrier14,595 (95.0)17,141 (94.6)21,999 (94.4)28,651 (93.8)36,338 (94.6)

Values are presented as number (%). *Others=clinic level, dentistryㆍKorea’s traditional medicine hospitals..



Of the 38,405 reports of CRE infections in 2023, a total of 36,680 (95.5%) were registered in individual investigation reports, with Klebsiella pneumoniae accounting for 72.4% (26,553 cases), Escherichi coli 14.1% (5,155 cases), Enterobacter spp. 6.0% (2,215 cases), Citrobacter freundii 1.9% (681 cases), and Citrobacter koseri 1.3% (466 cases) of the isolates. The five most common isolates over the past 5 years have largely maintained their rankings as a percentage of the total from 2019 to 2023. Notably , the prevalence of K. pneumoniae has steadily increased since 2019: 60.4% in 2019, 62.6% in 2020, 68.6% in 2021, 70.9% in 2022, and 72.4% in 2023 (Supplementary Table 1; available online).

2. Carbapenemase-producing Enterobacterales Infection Report Status

Of the 38,405 CRE infections reported in 2023, the proportion of CP-CRE infections was 73.7%, with a total of 28,318 cases confirmed in 1,117 healthcare facilities. The proportion of CP-CRE infections increased annually throughout the study period, with 57.8% (8,887 cases) in 2019, 61.9% (11,218 cases) in 2020, 63.4% (14,769 cases) in 2021, 71.0% (21,695 cases) in 2022, and 73.7% (28,318 cases) in 2023 (Table 1).

The distribution of carbapenemases was 77.4% (21,907 cases) for Klebsiella pneumoniae carbapenemase (KPC), 15.9% (4,487 cases) for New Delhi metallo-β-lactamase (NDM), and 6.2% (1,766 cases) for oxacillinase (OXA). The three genotypes that have consistently dominated from 2019 to 2023, in their proportional rankings over time. Notably, since 2019, the proportion of KPCs among all carbapenemases has continued to increase, whereas the proportion of NDMs has decreased (Supplementary Table 2; available online).

A regional analysis of carbapenemases showed that the prevalence of KPC was 27.3% (5,991 cases) in Seoul, 24.6% (5,388 cases) in Gyeonggi-do, and 8.0% (1,743 cases) in Gyeongsangnam-do. The prevalence of NDM was 32.0% (1,436 cases) in Seoul, 22.0% (988 cases) in Gyeonggi-do, and 14.5% (652 cases) in Incheon. The prevalence of OXA was 34.1% (603 cases) in Seoul, 20.5% (362 cases) in Gyeonggi-do, and 11.2% (197 cases) in Incheon (Figure 1, Table 3).

Figure 1. Geographical distribtuion map of CP-CRE Infection by carbapenemase genotype in region 2023
CP-CRE=carbapenemase-producing Enterobacterales; KPC=Klebsiella pneumoniae carbapenemase; NDM=New Delhi metallo-β-lactamase; OXA=oxacillinase; Etc.=Verona integron-encoded metallo-β-lactamase, Imipenemase, Guiana extended spectrum β-lactamase.

Distribtuion of carbapenemase-producing Enterobacterales by carbapenemase genotype in region 2023
RegionTotalKPCNDMOXAEtc.*
Total28,31821,9074,4871,766158
Seoul8,065 (28.5)5,991 (27.3)1,436 (32.0)603 (34.1)35 (22.2)
Busan2,121 (7.5)1,738 (7.9)304 (6.8)74 (4.2)5 (3.2)
Daegu1,488 (5.3)1,264 (5.8)173 (3.9)40 (2.3)11 (7.0)
Incheon2,425 (8.6)1,559 (7.1)652 (14.5)197 (11.2)17 (10.8)
Gwangju706 (2.5)450 (2.1)79 (1.8)176 (10.0)1 (0.6)
Daejeon693 (2.4)506 (2.3)154 (3.4)30 (1.7)3 (1.9)
Ulsan268 (0.9)225 (1.0)34 (0.8)8 (0.5)1 (0.6)
Sejong28 (0.1)23 (0.1)5 (0.1)0 (0.0)0 (0.0)
Gyeonggi6,780 (23.9)5,388 (24.6)988 (22.0)362 (20.5)42 (26.6)
Gangwon539 (1.9)448 (2.0)41 (0.9)48 (2.7)2 (1.3)
Chungbuk298 (1.1)229 (1.0)41 (0.9)26 (1.5)2 (1.3)
Chungnam588 (2.1)501 (2.3)71 (1.6)16 (0.9)0 (0.0)
Jeonbuk960 (3.4)759 (3.5)84 (1.9)111 (6.3)6 (3.8)
Jeonnam410 (1.4)273 (1.2)78 (1.7)45 (2.5)14 (8.9)
Gyeongbuk771 (2.7)662 (3.0)98 (2.2)3 (0.2)8 (5.1)
Gyengnam2,007 (7.1)1,743 (8.0)232 (5.2)21 (1.2)11 (7.0)
Jeju171 (0.6)148 (0.7)17 (0.4)6 (0.3)0 (0.0)

Values are presented as number (%). KPC=Klebsiella pneumoniae carbapenemase; NDM=New Delhi metallo-β-lactamase; OXA=oxacillinase; *Etc.=Verona integron-encoded metallo-β-lactamase, Imipenemase, Guiana extended spectrum β-lactamase..


Discussion

The prevalence of CRE infections is increasing both domestically and globally. The Centers for Disease Control and Prevention reported a 35.0% increase in healthcare-associated CRE infections in 2020, coinciding with the COVID-19 pandemic, compared with that in the previous year, as noted in the 「COVID-19: U.S. impact on antimicrobial resistance, special report 2022」 report. This surge peaked in 2021 and persisted above pre-pandemic levels in 2022 [4].

In the ROK, since mandatory CRE infection surveillance began in June 2017, the number of reported cases and reporting healthcare facilities continues to increased. In particular, reports from long-term care hospitals (the number of reporting healthcare facilities) increased markedly from 1,458 cases (322 facilities) in 2020 to 5,815 cases (566 facilities) in 2023. This represents a 4.0-fold increase in cases and a 1.8-fold increase in the number of reporting healthcare facilities. As indicated by the testing status, the proportion of fecal specimens among all positive specimens in long-term care hospitals increased from 2,441 cases (69.2%) in 2020 to 8,558 cases (73.6%) in 2023. This suggests that preemptive and contact testing are being actively implemented to manage CRE patients.

Long-term care hospitals, which primarily admit elderly and rehabilitation patients with chronic diseases, pose unique challenges [9]. The average length of stay in all healthcare facilities is 16.1 days, with an average length of stay of 134.4 days in long-term care hospitals [10,11]. The risk of CRE infection may be increased due to the multi-bedded structure of long-term care hospitals and the lack of infection control staff and resources.

To address these challenges, the ROK is implementing measures to prevent the spread of CRE infections. These measures include facility and environmental management improvements, including long-term care hospitals, expansion of infection control systems, and reorganization of healthcare-related infection response frameworks. Efforts are also underway to strengthen infection control personnel capabilities through administrative and financial assistance, including reimbursement systems.

A comparison of international isolate distributions with European Centre for Disease Prevention and Control surveillance data for only certain bacteria such as K. pneumoniae and E. coli reveals discrepancies between the datasets. These discrepancies make absolute comparisons difficult. However, it is notable that the percentages of carbapenem resistance in K. pneumoniae increased from 8.5% in 2018 to 10.9% in 2022. These findings suggest that CRE infections are increasing globally [12]. The World Health Organization (WHO) has classified CRE as a “critical pathogen with the highest priority for research, development, and public health action to prevent and control antimicrobial resistance” in its “WHO bacterial priority pathogens list, 2024” report. The WHO also emphasized the need for international efforts to address antimicrobial resistance, including the implementation of robust infection prevention and control measures, the surveillance of emerging trends, the advancement of drug development, and the creation of diagnostic and prevention tools [2].

Global strategies to reduce CRE infections include healthcare providers identifying and mitigating risk factors, emphasizing hand hygiene, personal protective equipment use, and proper environmental disinfection for infection control, and prescribing antibiotics judiciously and conducting preemptive testing for “asymptomatic carriers” [13]. In the ROK, the government is developing a response system to prevent the spread of CRE infections. This system will be a feasible, on-site one in healthcare facilities to evaluate CRE prevalence and to design and pilot a reduction strategy, establishing a foundation for systematic surveillance, prevention, and management of CRE infections.

The occurrence and distribution of infectious diseases were analyzed using basic statistical methods based on CRE case and investigation reports. This report highlights the growing burden of CRE infections in Korean healthcare facilities, necessitating active surveillance and reinforced infection prevention and control measures. Collaborative efforts among the government, local authorities, and healthcare facilities will be essential to curbing the spread of this significant public health threat.

Declarations

Ethics Statement: Not applicable.

Funding Source: None.

Acknowledgments: None.

Conflict of Interest: The authors have no conflicts of interest to declare.

Author Contributions: Conceptualization: HJL. Data curation: HJL. Formal analysis: HJL. Investigation: HJL, JHC Methodology: HJL, SJL. Project administration: SJL, HJL. Software: HJL. Supervision: SKP, SJL, HJL. Validation: HJL. Visualization: HJL. Writing – original draft: HJL. Writing – review & editing: SKP, SJL, YHJ, JHC.

Supplementary Materials

Supplementary data are available online.

Fig 1.

Figure 1.Geographical distribtuion map of CP-CRE Infection by carbapenemase genotype in region 2023
CP-CRE=carbapenemase-producing Enterobacterales; KPC=Klebsiella pneumoniae carbapenemase; NDM=New Delhi metallo-β-lactamase; OXA=oxacillinase; Etc.=Verona integron-encoded metallo-β-lactamase, Imipenemase, Guiana extended spectrum β-lactamase.
Public Health Weekly Report 2025; 18: 75-89https://doi.org/10.56786/PHWR.2025.18.2.2
Number of CREㆍCP-CRE designated and healthcare facilities by year (2019–2023)
Category20192020202120222023
CRE infectionNo. of cases15,36918,11323,31130,54838,405
No. of healthcare facilities (place)8319381,0671,2571,467
CP-CRE infectionNo. of cases8,88711,21814,76921,69528,318
No. of CP-CRE healthcare facilities (place)*6226707178771,117
CP-CRE/CRE ratio (%)57.861.963.471.073.7

CRE=carbapenem-resistant Enterobacterales; CP-CRE=carbapenemase-producing Enterobacterales. *Number of healthcare facilities where at least one case of CP-CRE occurred in the year..


Characteristics of carbapenem-resistant Enterobacterales (2019–2023)
Category20192020202120222023
Total15,36918,11323,31130,54838,405
Sex
Male8,727 (56.8)10,210 (56.4)13,362 (57.3)17,036 (55.8)21,293 (55.4)
Female6,642 (43.2)7,903 (43.6)9,949 (42.7)13,512 (44.2)17,112 (44.6)
Age group
0–19333 (2.2)311 (1.7)336 (1.4)341 (1.1)456 (1.2)
20–39513 (3.3)502 (2.8)667 (2.9)784 (2.6)895 (2.3)
40–49760 (4.9)774 (4.3)1,042 (4.5)1,246 (4.1)1,469 (3.8)
50–591,789 (11.6)2,035 (11.2)2,372 (10.2)2,914 (9.5)3,416 (8.9)
60–692,943 (19.1)3,405 (18.8)4,587 (19.7)5,864 (19.2)7,112 (18.5)
≥709,031 (58.8)11,086 (61.2)14,307 (61.4)19,399 (63.5)25,057 (65.2)
Healthcare facility type
Advanced general hospital6,266 (40.8)7,099 (39.2)9,442 (40.5)11,737 (38.4)13,443 (35.0)
General hospital6,803 (44.3)8,013 (44.2)9,786 (42.0)13,298 (43.5)16,648 (43.3)
Hospital1,093 (7.1)1,380 (7.6)1,512 (6.5)1,515 (5.0)2,105 (5.5)
Long-term care hospital1,077 (7.0)1,485 (8.2)2,383 (10.2)3,760 (12.3)5,815 (15.1)
Others*130 (0.8)136 (0.8)188 (0.8)238 (0.8)394 (1.0)
Case classification
Patient of an infectious disease774 (5.0)972 (5.4)1,312 (5.6)1,897 (6.2)2,067 (5.4)
Pathogen carrier14,595 (95.0)17,141 (94.6)21,999 (94.4)28,651 (93.8)36,338 (94.6)

Values are presented as number (%). *Others=clinic level, dentistryㆍKorea’s traditional medicine hospitals..


Distribtuion of carbapenemase-producing Enterobacterales by carbapenemase genotype in region 2023
RegionTotalKPCNDMOXAEtc.*
Total28,31821,9074,4871,766158
Seoul8,065 (28.5)5,991 (27.3)1,436 (32.0)603 (34.1)35 (22.2)
Busan2,121 (7.5)1,738 (7.9)304 (6.8)74 (4.2)5 (3.2)
Daegu1,488 (5.3)1,264 (5.8)173 (3.9)40 (2.3)11 (7.0)
Incheon2,425 (8.6)1,559 (7.1)652 (14.5)197 (11.2)17 (10.8)
Gwangju706 (2.5)450 (2.1)79 (1.8)176 (10.0)1 (0.6)
Daejeon693 (2.4)506 (2.3)154 (3.4)30 (1.7)3 (1.9)
Ulsan268 (0.9)225 (1.0)34 (0.8)8 (0.5)1 (0.6)
Sejong28 (0.1)23 (0.1)5 (0.1)0 (0.0)0 (0.0)
Gyeonggi6,780 (23.9)5,388 (24.6)988 (22.0)362 (20.5)42 (26.6)
Gangwon539 (1.9)448 (2.0)41 (0.9)48 (2.7)2 (1.3)
Chungbuk298 (1.1)229 (1.0)41 (0.9)26 (1.5)2 (1.3)
Chungnam588 (2.1)501 (2.3)71 (1.6)16 (0.9)0 (0.0)
Jeonbuk960 (3.4)759 (3.5)84 (1.9)111 (6.3)6 (3.8)
Jeonnam410 (1.4)273 (1.2)78 (1.7)45 (2.5)14 (8.9)
Gyeongbuk771 (2.7)662 (3.0)98 (2.2)3 (0.2)8 (5.1)
Gyengnam2,007 (7.1)1,743 (8.0)232 (5.2)21 (1.2)11 (7.0)
Jeju171 (0.6)148 (0.7)17 (0.4)6 (0.3)0 (0.0)

Values are presented as number (%). KPC=Klebsiella pneumoniae carbapenemase; NDM=New Delhi metallo-β-lactamase; OXA=oxacillinase; *Etc.=Verona integron-encoded metallo-β-lactamase, Imipenemase, Guiana extended spectrum β-lactamase..


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