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Public Health Weekly Report 2024; 17(4): 115-127

Published online November 28, 2023

https://doi.org/10.56786/PHWR.2024.17.4.1

© The Korea Disease Control and Prevention Agency

Characteristics of Carbapenem-resistant Enterobacteriaceae (CRE) in the Republic of Korea, 2022

Jihyeon Lim1, Juyoung Sim2, Hyunju Lee2, Jeonghui Hyun2, Seungjae Lee2, Sookkyung Park2*

1Honam Regional Center for Disease Control and Prevention Jeju Branch Office, Korea Disease Control and Prevention Agency, Jeju, Korea,
2Division of Healthcare Associated Infection Control, Bureau of Healthcare Safety and Immunization, Korea Disease Control and Prevention Agency, Cheongju, Korea

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

Received: November 15, 2023; Revised: November 20, 2023; Accepted: November 20, 2023

This is an open-access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Carbapenem-resistant Enterobacteriaceae (CRE) are species of bacteria in the family Enterobacteriaceae that are resistant to at least one of the carbapenem antibiotics. In 2019, World Health Organization declared antimicrobial resistance as “one of the top ten global public health threats facing humanity,” and with the continually increasing use of antibiotics worldwide, there is a correspondingly growing threat of resistance development among bacteria, thus necessitating more stringent surveillance and management. This report analyzed the 2022 domestic outbreak status of CRE infections with respect to patient age, type of medical institution, carbapenemase genes, and carbapenemase genotype. In 2022, 30,548 cases of CRE infections were reported in 1,257 medical institutions, and the number has been increasing every year since 2017, when the mandatory surveillance system was initiated, increasing by 155.5% compared to 2018 (11,954 cases). The mechanisms of carbapenem antibiotic resistance in CRE infections include carbapenemase-producing Enterobacteriaceae (CP-CRE) and Enterobacteriaceae species that are resistant to carbapenem antibiotics without producing carbapenemase (non-CP-CRE). Of the 30,548 reported cases of CRE infection, 71.0% (21,695 cases) were CPE infections, showing a 46.9% increase compared to 2 021 (14,769 cases). The annual increase in CRE infections is becoming an increasingly concerning social burden, thus emphasizing the need for continuous prevention and management, along with the establishment of a surveillance system for identifying the epidemiological characteristics. The government plans to continue efforts with local governments and medical institutions to prevent the spread of CRE infections, including strengthened CRE management measures in the 2nd Comprehensive Measures for Prevention and Management of Healthcare-Related Infections (2023–2027). In addition, it will strengthen the cooperative management system between medical institutions and the government and continue to implement various management methods such as infection control education.

Key words Carbapenem-resistant Enterobacteriaceae; Carbapenemase-producing Enterobacteriaceae; Antibiotic resistance

Key messages

① What is known previously?

Reports of domestic carbapenem-resistant Enterobacteriaceae (CRE) infections the number has been increasing every year since 2017, when the mandatory surveillance system was initiated.

② What new information is presented?

Of the 30,548 cases of CRE infection reported nationwide in 2022, 71.0% were carbapenemase-producing Enterobacteriaceae (CPE) infections. The highest rates of CPE infection were recorded in Daegu at 80.3% and Incheon at 75.6%, whereas the lowest rates were reported from Sejong at 29.7% and Ulsan at 52.0%. It was also established that there was a significant regional difference in the incidence of infection.

③ What are implications?

A range of measures will be necessary to strengthen the cooperative management system between medical institutions and the government, based on a comprehensive surveillance system. Furthermore, we need to strengthen the implementation of feedback and quarantine guidelines based on relevant reports and case investigation analyses.

Infections caused by carbapenem-resistant Enterobacteriaceae (CRE) are a significant and persistent public health issue worldwide [1], predominantly occurring in healthcare settings. CRE infections involve Enterobacteriaceae species that are resistant to any carbapenem antibiotics, including Ertapenem, Meropenem, Doripenem, and Imipenem. CRE infections are subject to mandatory reporting to local health authorities under a Class 2 comprehensive surveillance system [2].

CRE infections are divided into two groups: carbapenemase-producing Enterobacteriaceae (CPE) and non-CPE infections. The CPE gene is known to significantly contribute to the spread of CRE due to its ability to be easily transmitted among bacteria [3,4]. The infection routes include direct or indirect contact with CRE-infected patients or carriers as well as exposure through contaminated equipment, supplies, and environments. CRE infections can lead to various conditions, including urinary tract infections, gastroenteritis, pneumonia, and sepsis [2]. CRE generally exhibits resistance to multiple antibiotics, which limits the treatment options and increases the financial burden on the healthcare system due to extended hospital stay [5,6].

This study analyzed the CRE infection data from the Republic of Korea (ROK), reported to municipalities and provinces from 2018 to 2022, the latest period after the transition to a comprehensive surveillance system, by age, hospital type, isolated bacteria, and carbapenemase type, comparing the trends across local municipalities and provinces.

To analyze the isolated bacteria and carbapenemase in CRE infections, we used data from the cases with CRE infections reported in 2022 through the Integrated Disease Management System operated by the Korea Disease Control and Prevention Agency (KDCA), the CRE Infection Case Report, and the CPE Infection Reporting (as of June 21, 2023). The analysis of CRE infections from 2018 to 2021 was derived from the KDCA’s Infectious Disease Surveillance Yearbook and previously published epidemiological and management reports [7-10].

1. CRE Infection Reporting Status

Overall, 30,548 cases of CRE infections were reported from 1,257 healthcare facilities in 2022. Since the comprehensive surveillance began in June 2017, both the number of reported cases and the number of reporting healthcare providers have increased year by year (Table 1).

Table 1. Number of CRE designated and medical institutions by year (2018–2022)
20182019202020212022
Reported cases11,95415,36918,11323,31130,548
Number of medical institutions7238319381,0671,257

CRE=carbapenem-resistant Enterobacteriaceae.



In 2022, male patients outnumbered female patients with regard to the incidence of CRE infections, accounting for 55.8% (17,036 cases) vs. 44.2% (13,512 cases), respectively. By age group, those aged 70 years and above represented 63.5% (19,399 cases), followed by the age group of 60–69 years, at 19.2% (5,864 cases), and the group of 50–59 years, at 9.5% (2,914 cases). The incidence of CRE infections among those over 70 years of age has been increasing, from 57.0% (6,819 cases) in 2018 to 63.5% (19,399 cases) in 2022. By the type of healthcare facilities, general hospitals reported 43.5% of cases (13,298 cases), followed by tertiary hospitals (38.4%; 11,737 cases), nursing hospitals (12.3%; 3,760 cases), and primary care clinics (5.0%; 1,515 cases). Particularly, reports from nursing hospitals have steadily increased, from 7.0% (n=1,077) in 2019, 8.2% (n=1,485) in 2020, 10.2% (n=2,383) in 2021, to 12.3% (n=3,760) in 2022 (Table 2).

Table 2. Characteristics of Carbapenem-resistant Enterobacteriaceae (2018–2022)
Category20182019202020212022
Total11,95415,36918,11323,31130,548
Sex
Male6,759 (56.5)8,727 (56.8)10,210 (56.4)13,362 (57.3)17,036 (55.8)
Female5,195 (43.5)6,642 (43.2)7,903 (43.6)9,949 (42.7)13,512 (44.2)
Age group
0–19 yr420 (3.5)333 (2.2)311 (1.7)336 (1.4)341 (1.1)
20–39 yr429 (3.6)513 (3.3)502 (2.8)667 (2.9)784 (2.6)
40–49 yr618 (5.2)760 (4.9)774 (4.3)1,042 (4.5)1,246 (4.1)
50–59 yr1,403 (11.7)1,789 (11.6)2,035 (11.2)2,372 (10.2)2,914 (9.5)
60–69 yr2,265 (18.9)2,943 (19.1)3,405 (18.8)4,587 (19.7)5,864 (19.2)
≥70 yr6,819 (57.0)9,031 (58.8)11,086 (61.2)14,307 (61.4)19,399 (63.5)
Medical institution type
Advanced general hospital5,298 (44.3)6,266 (40.8)7,099 (39.2)9,442 (40.5)11,737 (38.4)
General hospital5,226 (43.7)6,803 (44.3)8,013 (44.2)9,786 (42.0)13,298 (43.5)
Hospital843 (7.1)1,093 (7.1)1,380 (7.6)1,512 (6.5)1,515 (5.0)
Long-term care hospital517 (4.3)1,077 (7.0)1,485 (8.2)2,383 (10.2)3,760 (12.3)
Othersa)70 (0.6)130 (0.8)136 (0.8)188 (0.8)238 (0.8)

Unit: n (%). a)Others: clinic, public health center, medical center.



Notably, analysis of the 2022 CRE Infection Case Report revealed that among the 30,808 isolated strains, K. pneumonia accounted for 70.9% of cases (n=21,845), E. coli for 14.0% of cases (n=4,313), Enterobacter spp. for 7.0% of cases (n=2,152), C. freundii for 2.5% of cases (n=767), and K. oxytoca for 1.1% of cases (n=353). These top 5 strains have remained the same over the past 5 years (2018–2022). The prevalence of K. pneumonia has been increasing annually since 2019, from 62.0% in 2018, 60.4% in 2019, 62.6% in 2020, 68.6% in 2021, to 70.9% in 2022. In contrast, E. coli has been showing a decreasing trend since 2019, from 17.8% in 2018, 19.2% in 2019, 18.0% in 2020, 14.3% in 2021, to 14.0% in 2022 (Table 3).

Table 3. Distribution of Carbapenem-resistant Enterobacteriaceae (CRE) by species (2018–2022)
Speciesa)20182019202020212022
Total10,15015,64019,63522,92530,808
Klebsiella pneumoniae6,289 (62.0)9,452 (60.4)12,296 (62.6)15,723 (68.6)21,845 (70.9)
Escherichia coli1,805 (17.8)3,010 (19.2)3,541 (18.0)3,280 (14.3)4,313 (14.0)
Enterobacter spp.1,199 (11.8)1,853 (11.8)1,869 (9.5)1,930 (8.4)2,152 (7.0)
Citrobacter freundii260 (2.6)403 (2.6)501 (2.6)586 (2.6)767 (2.5)
Klebsiella oxytoca167 (1.6)234 (1.5)315 (1.6)290 (1.3)353 (1.1)
Serratia marcescens66 (0.7)136 (0.9)278 (1.4)268 (1.2)288 (0.9)
Citrobacter koseri41 (0.4)118 (0.8)113 (0.6)219 (1.0)306 (1.0)
Raoultella ornithinolytica14 (0.1)30 (0.2)49 (0.2)45 (0.2)52 (0.2)
Providencia rettgeri76 (0.7)118 (0.8)137 (0.7)105 (0.5)102 (0.3)
K. pneumoniae, K. oxytoca excluding Klebsiella spp.43 (0.4)127 (0.8)220 (1.1)208 (0.9)310 (1.0)
R. ornithinolytica excluding Raoultella spp.21 (0.2)12 (0.1)15 (0.1)20 (0.1)23 (0.1)
C. freundii, C. koseri excluding Citrobacter spp.38 (0.4)4 (0.0)138 (0.7)98 (0.4)93 (0.3)
Proteus spp.124 (1.2)57 (0.4)40 (0.2)51 (0.2)62 (0.2)
Morganella morganii0 (0.0)23 (0.1)21 (0.1)20 (0.1)24 (0.1)
P. rettgeri excluding Providencia spp.2 (0.0)21 (0.1)24 (0.1)29 (0.1)22 (0.1)
Othersb)5 (0.0)42 (0.3)78 (0.4)53 (0.2)96 (0.3)

Unit: n (%). a)Multiple isolates can be selected when filling out a CRE infection case investigation form. b)Others: Kluyvera spp. 28 cases, Hafnia alvei 12 cases, Pantoea spp. 6 cases, Lelliottia spp. 4 cases, S. marcescens and Serratia spp. 3 cases, etc.



2. CPE Infection Reporting Status

In 2022, out of 30,548 reported cases of CRE infections, 71.0% of cases (n=21,695) were confirmed as CPE infections in 877 healthcare facilities. The proportion of CPE infections has increased year by year, standing at 49.9% of cases (n=5,962) in 2018, 57.8% (n=8,887) in 2019, 61.9% (n=11,218) in 2020, and 63.4% (n=14,769) in 2021. The number of positive CPE cases in 2022 showed a significant increase of 263.9% compared to that in 2018 (Table 4).

Table 4. Number of Carbapenemase-producing Enterobacteriaceae (CPE) designated and medical institutions by year (2018–2022)
Category20182019202020212022
CRE infection11,95415,36918,11323,31130,548
CPE infection5,962 (49.9)8,887 (57.8)11,218 (61.9)14,769 (63.4)21,695 (71.0)
Number of CPE medical institutiona)-622670717877

Unit: n (%). CRE=carbapenem-resistant Enterobacteriaceae. a)Number of medical institutions where at least one case of CPE occurred in the year.



The regional distribution of CPE infections reported in 2022 showed the highest incidence in Daegu, with 80.3% of cases (n=1,445), followed by that in Incheon, with 75.6% of cases (n=2,026), that in Daejeon, with 74.6% of cases (n=530), that in Gyeongbuk, with 74.4% of cases (n=585), and that in Gyeongnam, with 74.1% of cases (n=1,372) (Table 5).

Table 5. Reporting status of CPE infection by province/city in 2022
Province/cityCPE infectionCPE infection (CPE/CRE)
Total30,54821,695 (71.0)
Seoul9,1536,419 (70.1)
Busan2,5011,670 (66.8)
Daegu1,7991,445 (80.3)
Incheon2,6792,026 (75.6)
Gwangju490298 (60.8)
Daejeon710530 (74.6)
Ulsan344179 (52.0)
Sejong3711 (29.7)
Gyonggi6,6004,774 (72.3)
Gangwon706458 (64.9)
Chungbuk302198 (65.6)
Chungnam803531 (66.1)
Jeonbuk1,213879 (72.5)
Jeonnam425234 (55.1)
Gyeongbuk786585 (74.4)
Gyeongnam1,8521,372 (74.1)
Jeju14886 (58.1)

Unit: n (%). CRE=carbapenem-resistant Enterobacteriaceae; CPE=carbapenemase-producing Enterobacteriaceae.



Among the 22,048 carbapenemases reported in the 2022 CPE Infection Reporting Form, Klebsiella pneumoniae carbapenemase (KPC) accounted for 77.1% (n=17,000); New Delhi metallo-β-lactamase (NDM), for 16.8% (n=3,705); and oxacillinases (OXA), for 5.2% (n=1,141). These top 3 carbapenemase types have remained the same each year from 2019 to 2022, with KPC continuously increasing and NDM decreasing. Notably, OXA decreased to 5.8% (n=533) in 2019, 4.3% (n=522) in 2020, and 2.9% (n=419) in 2021, but slightly increased to 5.2% (n=1,141) in 2022 (Table 6).

Table 6. Distribution of Carbapenemase-producing Enterobacteriaceae (CPE) by carbapenemase genotype (2018–2022)
Carbapenemase genotypea)20182019202020212022
Total5,8009,20912,13614,32022,048
KPC4,132 (71.2)6,309 (68.5)8,958 (73.8)10,914 (76.2)17,000 (77.1)
NDM1,432 (24.7)2,240 (24.3)2,516 (20.7)2,822 (19.7)3,705 (16.8)
OXA116 (2.0)533 (5.8)522 (4.3)419 (2.9)1,141 (5.2)
VIM69 (1.2)59 (0.6)60 (0.5)78 (0.5)84 (0.4)
IMP43 (0.7)53 (0.6)67 (0.6)68 (0.5)92 (0.4)
GES8 (0.1)15 (0.2)13 (0.1)19 (0.1)26 (0.1)

Unit: n (%). KPC=Klebsiella pneumoniae carbapenemase; NDM=New Delhi metallo-β-lactamase; OXA=Oxacillinase; VIM=Verona integron-encoded metallo-β-lactamase; IMP=Imipenemase; GES=Guiana extended spectrum β-lactamase. a)Multiple carbapenemase genotypes can be selected when filling out the CPE report.


This report examined the CRE infection cases (n=30,548) reported to the KDCA’s Integrated Disease Management System from healthcare facilities in 2022 to identify the CRE infection status in the ROK by the type of healthcare facility, age, and isolated bacteria, and analyzed the related carbapenemases and the CPE infection status by region using the CPE Infection Reporting data.

In the ROK, the incidence of CRE infections has been increasing annually since 2017. This increasing trend has also been observed on the global scale. Although a direct international comparison is difficult due to the surveillance standards varying from country to country, with the United States (US) reporting CPE (plus CPO from 2023), the United Kingdom reporting CPE and gram-negative bacteria producing carbapenemase, and Japan reporting based on the clinical symptoms and laboratory diagnostic criteria, the surveillance data indicate an increase in carbapenem-resistant bacteria [11,12].

For efficient CRE infection management, the US Centers for Disease Control and Prevention recommends strategies that include the identification of patients in the initial phase of the spread stage, rapidly implementing appropriate measures, such as isolation and contact tracing to prevent further spread, recognizing transmission within and between healthcare facilities, and providing guidance for additional response measures. These measures include the management of patients by identifying novel pathogens and characterizing their mechanisms, as well as the adaptation of ongoing infection prevention activities to address the emerging challenges [13].

Likewise, the ROK is about to develop and implement intervention programs as part of the Second Comprehensive Plan for Healthcare-Associated Infections. These programs include tasks for establishing strategies to strengthen CRE infection management. This involves assessment of the current state of infection control aimed at reducing CRE infections, analysis of the barriers to effective infection control, and building and pilot-testing of an enhanced infection control intervention model specifically for CRE reduction. Additionally, the plan includes bolstering the CRE surveillance system to establish a cooperative framework between healthcare facilities and the government. This effort will focus on improving reporting and case analysis feedback, enhancing compliance with isolation guidelines, providing customized education for healthcare workers, and supporting active surveillance. These varied and intensive efforts are crucial for strengthening the prevention and management of CRE infections [14].

Ethics Statement: Not applicable.

Funding Source: None.

Acknowledgments: None.

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

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

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  4. Kim MK, Joo S, Shin E, Kim J, Yoo J, assignee. Antimicrobial resistance and molecular characteristics of carbapenem-resistant Enterobacteriaceae isolated in the Republic of Korea, 2021. Public Health Wkly Rep 2023;16:541-59.
  5. Yun SJ, Kwon SM, Hur ES, et al, assignee. Outbreaks of carbapenem resistant Enterobacterales (CRE) according to the type of hospitals. Korean J healthc assoc Infect Control Prev 2022;27:162-7.
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  6. Centers for Disease Control and Prevention (CDC), assignee. Carbapenem-resistant Enterobacterales (CRE) [Internet]. CDC; 2019 [cited 2023 Sep 1].
    Available from: https://www.cdc.gov/hai/organisms/cre/index.html
  7. Korea Disease Control and Prevention Agency (KDCA), assignee. Annual report on the notified infectious diseases in Korea, 2022. KDCA; 2023.
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  10. Jeong H, Hyun J, Lee Y, assignee. Characteristics of carbapenem-resistant Enterobacteriaceae (CRE) in the Republic of Korea, 2021. Public Health Wkly Rep 2022;15:2354-63.
  11. Centers for Disease Control and Prevention, assignee (2023). National Notifiable Diseases Surveillance System, Weekly Tables of Infectious Disease Data [Internet].
    Available from: https://wonder.cdc.gov/nndss/static/2023/04/2023-04-table355.html. (cited 2023 Sep 1)
  12. Quarterly laboratory surveillance of acquired carbapenemase-producing Gram-negative bacteria in England: October 2020 to September 2022, assignee. Health Prot Rep 2023;17:1-29. Health Prot Rep 2023;17:1-29.
  13. Centers for Disease Control and Prevention (CDC), assignee. Interim guidance for a public health response to contain novel or targeted multidrug-resistant organisms (MDROs). CDC; 2022.
  14. Korea Disease Control and Prevention Agency Press Release [cited 2023 Apr 12]
    Available from: https://www.kdca.go.kr/board/board.es?mid=a20501010000&bid=0015&list_no=722274&cg_code=&act=view&nPage=3

Surveillance Reports

Public Health Weekly Report 2024; 17(4): 115-127

Published online January 25, 2024 https://doi.org/10.56786/PHWR.2024.17.4.1

Copyright © The Korea Disease Control and Prevention Agency.

Characteristics of Carbapenem-resistant Enterobacteriaceae (CRE) in the Republic of Korea, 2022

Jihyeon Lim1, Juyoung Sim2, Hyunju Lee2, Jeonghui Hyun2, Seungjae Lee2, Sookkyung Park2*

1Honam Regional Center for Disease Control and Prevention Jeju Branch Office, Korea Disease Control and Prevention Agency, Jeju, Korea,
2Division of Healthcare Associated Infection Control, Bureau of Healthcare Safety and Immunization, Korea Disease Control and Prevention Agency, Cheongju, Korea

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

Received: November 15, 2023; Revised: November 20, 2023; Accepted: November 20, 2023

This is an open-access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Carbapenem-resistant Enterobacteriaceae (CRE) are species of bacteria in the family Enterobacteriaceae that are resistant to at least one of the carbapenem antibiotics. In 2019, World Health Organization declared antimicrobial resistance as “one of the top ten global public health threats facing humanity,” and with the continually increasing use of antibiotics worldwide, there is a correspondingly growing threat of resistance development among bacteria, thus necessitating more stringent surveillance and management. This report analyzed the 2022 domestic outbreak status of CRE infections with respect to patient age, type of medical institution, carbapenemase genes, and carbapenemase genotype. In 2022, 30,548 cases of CRE infections were reported in 1,257 medical institutions, and the number has been increasing every year since 2017, when the mandatory surveillance system was initiated, increasing by 155.5% compared to 2018 (11,954 cases). The mechanisms of carbapenem antibiotic resistance in CRE infections include carbapenemase-producing Enterobacteriaceae (CP-CRE) and Enterobacteriaceae species that are resistant to carbapenem antibiotics without producing carbapenemase (non-CP-CRE). Of the 30,548 reported cases of CRE infection, 71.0% (21,695 cases) were CPE infections, showing a 46.9% increase compared to 2 021 (14,769 cases). The annual increase in CRE infections is becoming an increasingly concerning social burden, thus emphasizing the need for continuous prevention and management, along with the establishment of a surveillance system for identifying the epidemiological characteristics. The government plans to continue efforts with local governments and medical institutions to prevent the spread of CRE infections, including strengthened CRE management measures in the 2nd Comprehensive Measures for Prevention and Management of Healthcare-Related Infections (2023–2027). In addition, it will strengthen the cooperative management system between medical institutions and the government and continue to implement various management methods such as infection control education.

Keywords: Carbapenem-resistant Enterobacteriaceae, Carbapenemase-producing Enterobacteriaceae, Antibiotic resistance

Body

Key messages

① What is known previously?

Reports of domestic carbapenem-resistant Enterobacteriaceae (CRE) infections the number has been increasing every year since 2017, when the mandatory surveillance system was initiated.

② What new information is presented?

Of the 30,548 cases of CRE infection reported nationwide in 2022, 71.0% were carbapenemase-producing Enterobacteriaceae (CPE) infections. The highest rates of CPE infection were recorded in Daegu at 80.3% and Incheon at 75.6%, whereas the lowest rates were reported from Sejong at 29.7% and Ulsan at 52.0%. It was also established that there was a significant regional difference in the incidence of infection.

③ What are implications?

A range of measures will be necessary to strengthen the cooperative management system between medical institutions and the government, based on a comprehensive surveillance system. Furthermore, we need to strengthen the implementation of feedback and quarantine guidelines based on relevant reports and case investigation analyses.

Introduction

Infections caused by carbapenem-resistant Enterobacteriaceae (CRE) are a significant and persistent public health issue worldwide [1], predominantly occurring in healthcare settings. CRE infections involve Enterobacteriaceae species that are resistant to any carbapenem antibiotics, including Ertapenem, Meropenem, Doripenem, and Imipenem. CRE infections are subject to mandatory reporting to local health authorities under a Class 2 comprehensive surveillance system [2].

CRE infections are divided into two groups: carbapenemase-producing Enterobacteriaceae (CPE) and non-CPE infections. The CPE gene is known to significantly contribute to the spread of CRE due to its ability to be easily transmitted among bacteria [3,4]. The infection routes include direct or indirect contact with CRE-infected patients or carriers as well as exposure through contaminated equipment, supplies, and environments. CRE infections can lead to various conditions, including urinary tract infections, gastroenteritis, pneumonia, and sepsis [2]. CRE generally exhibits resistance to multiple antibiotics, which limits the treatment options and increases the financial burden on the healthcare system due to extended hospital stay [5,6].

This study analyzed the CRE infection data from the Republic of Korea (ROK), reported to municipalities and provinces from 2018 to 2022, the latest period after the transition to a comprehensive surveillance system, by age, hospital type, isolated bacteria, and carbapenemase type, comparing the trends across local municipalities and provinces.

Methods

To analyze the isolated bacteria and carbapenemase in CRE infections, we used data from the cases with CRE infections reported in 2022 through the Integrated Disease Management System operated by the Korea Disease Control and Prevention Agency (KDCA), the CRE Infection Case Report, and the CPE Infection Reporting (as of June 21, 2023). The analysis of CRE infections from 2018 to 2021 was derived from the KDCA’s Infectious Disease Surveillance Yearbook and previously published epidemiological and management reports [7,,-10].

Results

1. CRE Infection Reporting Status

Overall, 30,548 cases of CRE infections were reported from 1,257 healthcare facilities in 2022. Since the comprehensive surveillance began in June 2017, both the number of reported cases and the number of reporting healthcare providers have increased year by year (Table 1).

Number of CRE designated and medical institutions by year (2018–2022)
20182019202020212022
Reported cases11,95415,36918,11323,31130,548
Number of medical institutions7238319381,0671,257

CRE=carbapenem-resistant Enterobacteriaceae..



In 2022, male patients outnumbered female patients with regard to the incidence of CRE infections, accounting for 55.8% (17,036 cases) vs. 44.2% (13,512 cases), respectively. By age group, those aged 70 years and above represented 63.5% (19,399 cases), followed by the age group of 60–69 years, at 19.2% (5,864 cases), and the group of 50–59 years, at 9.5% (2,914 cases). The incidence of CRE infections among those over 70 years of age has been increasing, from 57.0% (6,819 cases) in 2018 to 63.5% (19,399 cases) in 2022. By the type of healthcare facilities, general hospitals reported 43.5% of cases (13,298 cases), followed by tertiary hospitals (38.4%; 11,737 cases), nursing hospitals (12.3%; 3,760 cases), and primary care clinics (5.0%; 1,515 cases). Particularly, reports from nursing hospitals have steadily increased, from 7.0% (n=1,077) in 2019, 8.2% (n=1,485) in 2020, 10.2% (n=2,383) in 2021, to 12.3% (n=3,760) in 2022 (Table 2).

Characteristics of Carbapenem-resistant Enterobacteriaceae (2018–2022)
Category20182019202020212022
Total11,95415,36918,11323,31130,548
Sex
Male6,759 (56.5)8,727 (56.8)10,210 (56.4)13,362 (57.3)17,036 (55.8)
Female5,195 (43.5)6,642 (43.2)7,903 (43.6)9,949 (42.7)13,512 (44.2)
Age group
0–19 yr420 (3.5)333 (2.2)311 (1.7)336 (1.4)341 (1.1)
20–39 yr429 (3.6)513 (3.3)502 (2.8)667 (2.9)784 (2.6)
40–49 yr618 (5.2)760 (4.9)774 (4.3)1,042 (4.5)1,246 (4.1)
50–59 yr1,403 (11.7)1,789 (11.6)2,035 (11.2)2,372 (10.2)2,914 (9.5)
60–69 yr2,265 (18.9)2,943 (19.1)3,405 (18.8)4,587 (19.7)5,864 (19.2)
≥70 yr6,819 (57.0)9,031 (58.8)11,086 (61.2)14,307 (61.4)19,399 (63.5)
Medical institution type
Advanced general hospital5,298 (44.3)6,266 (40.8)7,099 (39.2)9,442 (40.5)11,737 (38.4)
General hospital5,226 (43.7)6,803 (44.3)8,013 (44.2)9,786 (42.0)13,298 (43.5)
Hospital843 (7.1)1,093 (7.1)1,380 (7.6)1,512 (6.5)1,515 (5.0)
Long-term care hospital517 (4.3)1,077 (7.0)1,485 (8.2)2,383 (10.2)3,760 (12.3)
Othersa)70 (0.6)130 (0.8)136 (0.8)188 (0.8)238 (0.8)

Unit: n (%). a)Others: clinic, public health center, medical center..



Notably, analysis of the 2022 CRE Infection Case Report revealed that among the 30,808 isolated strains, K. pneumonia accounted for 70.9% of cases (n=21,845), E. coli for 14.0% of cases (n=4,313), Enterobacter spp. for 7.0% of cases (n=2,152), C. freundii for 2.5% of cases (n=767), and K. oxytoca for 1.1% of cases (n=353). These top 5 strains have remained the same over the past 5 years (2018–2022). The prevalence of K. pneumonia has been increasing annually since 2019, from 62.0% in 2018, 60.4% in 2019, 62.6% in 2020, 68.6% in 2021, to 70.9% in 2022. In contrast, E. coli has been showing a decreasing trend since 2019, from 17.8% in 2018, 19.2% in 2019, 18.0% in 2020, 14.3% in 2021, to 14.0% in 2022 (Table 3).

Distribution of Carbapenem-resistant Enterobacteriaceae (CRE) by species (2018–2022)
Speciesa)20182019202020212022
Total10,15015,64019,63522,92530,808
Klebsiella pneumoniae6,289 (62.0)9,452 (60.4)12,296 (62.6)15,723 (68.6)21,845 (70.9)
Escherichia coli1,805 (17.8)3,010 (19.2)3,541 (18.0)3,280 (14.3)4,313 (14.0)
Enterobacter spp.1,199 (11.8)1,853 (11.8)1,869 (9.5)1,930 (8.4)2,152 (7.0)
Citrobacter freundii260 (2.6)403 (2.6)501 (2.6)586 (2.6)767 (2.5)
Klebsiella oxytoca167 (1.6)234 (1.5)315 (1.6)290 (1.3)353 (1.1)
Serratia marcescens66 (0.7)136 (0.9)278 (1.4)268 (1.2)288 (0.9)
Citrobacter koseri41 (0.4)118 (0.8)113 (0.6)219 (1.0)306 (1.0)
Raoultella ornithinolytica14 (0.1)30 (0.2)49 (0.2)45 (0.2)52 (0.2)
Providencia rettgeri76 (0.7)118 (0.8)137 (0.7)105 (0.5)102 (0.3)
K. pneumoniae, K. oxytoca excluding Klebsiella spp.43 (0.4)127 (0.8)220 (1.1)208 (0.9)310 (1.0)
R. ornithinolytica excluding Raoultella spp.21 (0.2)12 (0.1)15 (0.1)20 (0.1)23 (0.1)
C. freundii, C. koseri excluding Citrobacter spp.38 (0.4)4 (0.0)138 (0.7)98 (0.4)93 (0.3)
Proteus spp.124 (1.2)57 (0.4)40 (0.2)51 (0.2)62 (0.2)
Morganella morganii0 (0.0)23 (0.1)21 (0.1)20 (0.1)24 (0.1)
P. rettgeri excluding Providencia spp.2 (0.0)21 (0.1)24 (0.1)29 (0.1)22 (0.1)
Othersb)5 (0.0)42 (0.3)78 (0.4)53 (0.2)96 (0.3)

Unit: n (%). a)Multiple isolates can be selected when filling out a CRE infection case investigation form. b)Others: Kluyvera spp. 28 cases, Hafnia alvei 12 cases, Pantoea spp. 6 cases, Lelliottia spp. 4 cases, S. marcescens and Serratia spp. 3 cases, etc..



2. CPE Infection Reporting Status

In 2022, out of 30,548 reported cases of CRE infections, 71.0% of cases (n=21,695) were confirmed as CPE infections in 877 healthcare facilities. The proportion of CPE infections has increased year by year, standing at 49.9% of cases (n=5,962) in 2018, 57.8% (n=8,887) in 2019, 61.9% (n=11,218) in 2020, and 63.4% (n=14,769) in 2021. The number of positive CPE cases in 2022 showed a significant increase of 263.9% compared to that in 2018 (Table 4).

Number of Carbapenemase-producing Enterobacteriaceae (CPE) designated and medical institutions by year (2018–2022)
Category20182019202020212022
CRE infection11,95415,36918,11323,31130,548
CPE infection5,962 (49.9)8,887 (57.8)11,218 (61.9)14,769 (63.4)21,695 (71.0)
Number of CPE medical institutiona)-622670717877

Unit: n (%). CRE=carbapenem-resistant Enterobacteriaceae. a)Number of medical institutions where at least one case of CPE occurred in the year..



The regional distribution of CPE infections reported in 2022 showed the highest incidence in Daegu, with 80.3% of cases (n=1,445), followed by that in Incheon, with 75.6% of cases (n=2,026), that in Daejeon, with 74.6% of cases (n=530), that in Gyeongbuk, with 74.4% of cases (n=585), and that in Gyeongnam, with 74.1% of cases (n=1,372) (Table 5).

Reporting status of CPE infection by province/city in 2022
Province/cityCPE infectionCPE infection (CPE/CRE)
Total30,54821,695 (71.0)
Seoul9,1536,419 (70.1)
Busan2,5011,670 (66.8)
Daegu1,7991,445 (80.3)
Incheon2,6792,026 (75.6)
Gwangju490298 (60.8)
Daejeon710530 (74.6)
Ulsan344179 (52.0)
Sejong3711 (29.7)
Gyonggi6,6004,774 (72.3)
Gangwon706458 (64.9)
Chungbuk302198 (65.6)
Chungnam803531 (66.1)
Jeonbuk1,213879 (72.5)
Jeonnam425234 (55.1)
Gyeongbuk786585 (74.4)
Gyeongnam1,8521,372 (74.1)
Jeju14886 (58.1)

Unit: n (%). CRE=carbapenem-resistant Enterobacteriaceae; CPE=carbapenemase-producing Enterobacteriaceae..



Among the 22,048 carbapenemases reported in the 2022 CPE Infection Reporting Form, Klebsiella pneumoniae carbapenemase (KPC) accounted for 77.1% (n=17,000); New Delhi metallo-β-lactamase (NDM), for 16.8% (n=3,705); and oxacillinases (OXA), for 5.2% (n=1,141). These top 3 carbapenemase types have remained the same each year from 2019 to 2022, with KPC continuously increasing and NDM decreasing. Notably, OXA decreased to 5.8% (n=533) in 2019, 4.3% (n=522) in 2020, and 2.9% (n=419) in 2021, but slightly increased to 5.2% (n=1,141) in 2022 (Table 6).

Distribution of Carbapenemase-producing Enterobacteriaceae (CPE) by carbapenemase genotype (2018–2022)
Carbapenemase genotypea)20182019202020212022
Total5,8009,20912,13614,32022,048
KPC4,132 (71.2)6,309 (68.5)8,958 (73.8)10,914 (76.2)17,000 (77.1)
NDM1,432 (24.7)2,240 (24.3)2,516 (20.7)2,822 (19.7)3,705 (16.8)
OXA116 (2.0)533 (5.8)522 (4.3)419 (2.9)1,141 (5.2)
VIM69 (1.2)59 (0.6)60 (0.5)78 (0.5)84 (0.4)
IMP43 (0.7)53 (0.6)67 (0.6)68 (0.5)92 (0.4)
GES8 (0.1)15 (0.2)13 (0.1)19 (0.1)26 (0.1)

Unit: n (%). KPC=Klebsiella pneumoniae carbapenemase; NDM=New Delhi metallo-β-lactamase; OXA=Oxacillinase; VIM=Verona integron-encoded metallo-β-lactamase; IMP=Imipenemase; GES=Guiana extended spectrum β-lactamase. a)Multiple carbapenemase genotypes can be selected when filling out the CPE report..


Discussion

This report examined the CRE infection cases (n=30,548) reported to the KDCA’s Integrated Disease Management System from healthcare facilities in 2022 to identify the CRE infection status in the ROK by the type of healthcare facility, age, and isolated bacteria, and analyzed the related carbapenemases and the CPE infection status by region using the CPE Infection Reporting data.

In the ROK, the incidence of CRE infections has been increasing annually since 2017. This increasing trend has also been observed on the global scale. Although a direct international comparison is difficult due to the surveillance standards varying from country to country, with the United States (US) reporting CPE (plus CPO from 2023), the United Kingdom reporting CPE and gram-negative bacteria producing carbapenemase, and Japan reporting based on the clinical symptoms and laboratory diagnostic criteria, the surveillance data indicate an increase in carbapenem-resistant bacteria [11,12].

For efficient CRE infection management, the US Centers for Disease Control and Prevention recommends strategies that include the identification of patients in the initial phase of the spread stage, rapidly implementing appropriate measures, such as isolation and contact tracing to prevent further spread, recognizing transmission within and between healthcare facilities, and providing guidance for additional response measures. These measures include the management of patients by identifying novel pathogens and characterizing their mechanisms, as well as the adaptation of ongoing infection prevention activities to address the emerging challenges [13].

Likewise, the ROK is about to develop and implement intervention programs as part of the Second Comprehensive Plan for Healthcare-Associated Infections. These programs include tasks for establishing strategies to strengthen CRE infection management. This involves assessment of the current state of infection control aimed at reducing CRE infections, analysis of the barriers to effective infection control, and building and pilot-testing of an enhanced infection control intervention model specifically for CRE reduction. Additionally, the plan includes bolstering the CRE surveillance system to establish a cooperative framework between healthcare facilities and the government. This effort will focus on improving reporting and case analysis feedback, enhancing compliance with isolation guidelines, providing customized education for healthcare workers, and supporting active surveillance. These varied and intensive efforts are crucial for strengthening the prevention and management of CRE infections [14].

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: JHL. Data curation: JHL, HJL. Formal analysis: JHL. Investigation: JHL. Methodology: JHL, SJL. Project administration: SJL, JHL. Software: JHL. Supervision: SKP, SJL, JHL. Validation: JHL. Visualization: JHL. Writing – original draft: JHL. Writing – review & editing: SKP, SJL, JHH, HJL, JYS, JHL.

Number of CRE designated and medical institutions by year (2018–2022)
20182019202020212022
Reported cases11,95415,36918,11323,31130,548
Number of medical institutions7238319381,0671,257

CRE=carbapenem-resistant Enterobacteriaceae..


Characteristics of Carbapenem-resistant Enterobacteriaceae (2018–2022)
Category20182019202020212022
Total11,95415,36918,11323,31130,548
Sex
Male6,759 (56.5)8,727 (56.8)10,210 (56.4)13,362 (57.3)17,036 (55.8)
Female5,195 (43.5)6,642 (43.2)7,903 (43.6)9,949 (42.7)13,512 (44.2)
Age group
0–19 yr420 (3.5)333 (2.2)311 (1.7)336 (1.4)341 (1.1)
20–39 yr429 (3.6)513 (3.3)502 (2.8)667 (2.9)784 (2.6)
40–49 yr618 (5.2)760 (4.9)774 (4.3)1,042 (4.5)1,246 (4.1)
50–59 yr1,403 (11.7)1,789 (11.6)2,035 (11.2)2,372 (10.2)2,914 (9.5)
60–69 yr2,265 (18.9)2,943 (19.1)3,405 (18.8)4,587 (19.7)5,864 (19.2)
≥70 yr6,819 (57.0)9,031 (58.8)11,086 (61.2)14,307 (61.4)19,399 (63.5)
Medical institution type
Advanced general hospital5,298 (44.3)6,266 (40.8)7,099 (39.2)9,442 (40.5)11,737 (38.4)
General hospital5,226 (43.7)6,803 (44.3)8,013 (44.2)9,786 (42.0)13,298 (43.5)
Hospital843 (7.1)1,093 (7.1)1,380 (7.6)1,512 (6.5)1,515 (5.0)
Long-term care hospital517 (4.3)1,077 (7.0)1,485 (8.2)2,383 (10.2)3,760 (12.3)
Othersa)70 (0.6)130 (0.8)136 (0.8)188 (0.8)238 (0.8)

Unit: n (%). a)Others: clinic, public health center, medical center..


Distribution of Carbapenem-resistant Enterobacteriaceae (CRE) by species (2018–2022)
Speciesa)20182019202020212022
Total10,15015,64019,63522,92530,808
Klebsiella pneumoniae6,289 (62.0)9,452 (60.4)12,296 (62.6)15,723 (68.6)21,845 (70.9)
Escherichia coli1,805 (17.8)3,010 (19.2)3,541 (18.0)3,280 (14.3)4,313 (14.0)
Enterobacter spp.1,199 (11.8)1,853 (11.8)1,869 (9.5)1,930 (8.4)2,152 (7.0)
Citrobacter freundii260 (2.6)403 (2.6)501 (2.6)586 (2.6)767 (2.5)
Klebsiella oxytoca167 (1.6)234 (1.5)315 (1.6)290 (1.3)353 (1.1)
Serratia marcescens66 (0.7)136 (0.9)278 (1.4)268 (1.2)288 (0.9)
Citrobacter koseri41 (0.4)118 (0.8)113 (0.6)219 (1.0)306 (1.0)
Raoultella ornithinolytica14 (0.1)30 (0.2)49 (0.2)45 (0.2)52 (0.2)
Providencia rettgeri76 (0.7)118 (0.8)137 (0.7)105 (0.5)102 (0.3)
K. pneumoniae, K. oxytoca excluding Klebsiella spp.43 (0.4)127 (0.8)220 (1.1)208 (0.9)310 (1.0)
R. ornithinolytica excluding Raoultella spp.21 (0.2)12 (0.1)15 (0.1)20 (0.1)23 (0.1)
C. freundii, C. koseri excluding Citrobacter spp.38 (0.4)4 (0.0)138 (0.7)98 (0.4)93 (0.3)
Proteus spp.124 (1.2)57 (0.4)40 (0.2)51 (0.2)62 (0.2)
Morganella morganii0 (0.0)23 (0.1)21 (0.1)20 (0.1)24 (0.1)
P. rettgeri excluding Providencia spp.2 (0.0)21 (0.1)24 (0.1)29 (0.1)22 (0.1)
Othersb)5 (0.0)42 (0.3)78 (0.4)53 (0.2)96 (0.3)

Unit: n (%). a)Multiple isolates can be selected when filling out a CRE infection case investigation form. b)Others: Kluyvera spp. 28 cases, Hafnia alvei 12 cases, Pantoea spp. 6 cases, Lelliottia spp. 4 cases, S. marcescens and Serratia spp. 3 cases, etc..


Number of Carbapenemase-producing Enterobacteriaceae (CPE) designated and medical institutions by year (2018–2022)
Category20182019202020212022
CRE infection11,95415,36918,11323,31130,548
CPE infection5,962 (49.9)8,887 (57.8)11,218 (61.9)14,769 (63.4)21,695 (71.0)
Number of CPE medical institutiona)-622670717877

Unit: n (%). CRE=carbapenem-resistant Enterobacteriaceae. a)Number of medical institutions where at least one case of CPE occurred in the year..


Reporting status of CPE infection by province/city in 2022
Province/cityCPE infectionCPE infection (CPE/CRE)
Total30,54821,695 (71.0)
Seoul9,1536,419 (70.1)
Busan2,5011,670 (66.8)
Daegu1,7991,445 (80.3)
Incheon2,6792,026 (75.6)
Gwangju490298 (60.8)
Daejeon710530 (74.6)
Ulsan344179 (52.0)
Sejong3711 (29.7)
Gyonggi6,6004,774 (72.3)
Gangwon706458 (64.9)
Chungbuk302198 (65.6)
Chungnam803531 (66.1)
Jeonbuk1,213879 (72.5)
Jeonnam425234 (55.1)
Gyeongbuk786585 (74.4)
Gyeongnam1,8521,372 (74.1)
Jeju14886 (58.1)

Unit: n (%). CRE=carbapenem-resistant Enterobacteriaceae; CPE=carbapenemase-producing Enterobacteriaceae..


Distribution of Carbapenemase-producing Enterobacteriaceae (CPE) by carbapenemase genotype (2018–2022)
Carbapenemase genotypea)20182019202020212022
Total5,8009,20912,13614,32022,048
KPC4,132 (71.2)6,309 (68.5)8,958 (73.8)10,914 (76.2)17,000 (77.1)
NDM1,432 (24.7)2,240 (24.3)2,516 (20.7)2,822 (19.7)3,705 (16.8)
OXA116 (2.0)533 (5.8)522 (4.3)419 (2.9)1,141 (5.2)
VIM69 (1.2)59 (0.6)60 (0.5)78 (0.5)84 (0.4)
IMP43 (0.7)53 (0.6)67 (0.6)68 (0.5)92 (0.4)
GES8 (0.1)15 (0.2)13 (0.1)19 (0.1)26 (0.1)

Unit: n (%). KPC=Klebsiella pneumoniae carbapenemase; NDM=New Delhi metallo-β-lactamase; OXA=Oxacillinase; VIM=Verona integron-encoded metallo-β-lactamase; IMP=Imipenemase; GES=Guiana extended spectrum β-lactamase. a)Multiple carbapenemase genotypes can be selected when filling out the CPE report..


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