J Korean Med Sci.  2020 Sep;35(36):e303. 10.3346/jkms.2020.35.e303.

Positivity of Carbapenemase-producing Enterobacteriaceae in Patients Following Exposure within Long-term Care Facilities in Seoul, Korea

• Park JJ
• Seo YB
• Lee J
• Eom JS
• Song W
• Choi YK
• Kim SR
• Son HJ
• Cho NH

• KMID: 2506543
• DOI: http://doi.org/10.3346/jkms.2020.35.e303

Abstract

Background
Carbapenemase-producing Enterobacteriaceae (CPE) are emerging as a worldwide threat. Long-term care facilities (LTCFs) are considered a reservoir for CPE and play a central role in transmission to acute care hospitals. We investigated the CPE positivity in patients exposed to CPE in LTCFs. Furthermore, we analyzed the CPE positivity rates in the environment exposed to CPE.
Methods
We collected rectal swab specimens from patients residing in LTCFs who were exposed to CPE. Environmental sampling was performed by infection control practitioners from sites classified as patient private space, common space in the patient room, common space other than patient rooms, and nursing station. Each sample was cultured on a Chrom KlebsiellaF pneumoniae carbapenemase (KPC) agar for CPE screening. The positive isolates were subjected to a polymerase chain reaction to identify the presence of bla _KPC , bla _VIM , bla _IMP , bla _OXA-48 , and bla _NDM and determine CPE genotype.
Results
From 65 index cases, a total of 24 hospitals and 481 patients were enrolled; 414 patients who had resided in the same patient room as a patient with confirmed CPE and 67 patients who were newly admitted to that patient room. A total of 117 (24.3%) patients were positive for CPE among which 93 (22.5%, 93/414) were already admitted patients and 24 (35.8%, 24/67) were newly admitted patients. A total of 163 CPEs were detected and K. pneumoniae (n = 104, 63.8%) was the most common bacteria followed by Escherichia coli (n = 43, 26.4%) and Citrobacter koseri (n = 11, 6.7%). Environmental sampling was performed in 24 hospitals and 604 sites. A total of 12 sites (2.0%) were positive for CPE and sink in the nursing station (n = 6, 4.2%) was the most contaminated space.
Conclusion
CPE colonization rates in patients exposed to CPE in LTCFs were higher than those found in acute care hospitals. Proper infection control measures for detecting and reducing CPE colonization in patients residing in LTCFs are required. Newly admitted patients could also be carriers; therefore, infection control for newly admitted patients also needs to be thorough.

Keyword

Carbapenemase-producing Enterobacteriaceae; Long-term Care Facility; Infection Control

Reference

1. Nordmann P, Cuzon G, Naas T. The real threat of Klebsiella pneumoniae carbapenemase-producing bacteria. Lancet Infect Dis. 2009; 9(4):228–236. PMID: 19324295.

2. Nordmann P, Naas T, Poirel L. Global spread of carbapenemase-producing Enterobacteriaceae . Emerg Infect Dis. 2011; 17(10):1791–1798. PMID: 22000347.

3. Tumbarello M, Trecarichi EM, De Rosa FG, Giannella M, Giacobbe DR, Bassetti M, et al. Infections caused by KPC-producing Klebsiella pneumoniae: differences in therapy and mortality in a multicentre study. J Antimicrob Chemother. 2015; 70(7):2133–2143. PMID: 25900159.

4. Centers for Disease Control and Prevention. Antibiotic resistance threats in the United States. Updated 2019. Accessed January 20, 2020. https://www.cdc.gov/drugresistance/pdf/threats-report/2019-ar-threats-report-508.pdf.

5. Årdal CO, Findlay D, Savic M, Carmeli Y, Gyssens I, Laxminarayan R, et al. Revitalizing the antibiotic pipeline: stimulating innovation while driving sustainable use and global access. Updated 2018. Accessed January 20, 2020. http://drive-ab.eu/wp-content/uploads/2018/01/DRIVE-AB-Final-Report-Jan2018.pdf.

6. Korea Centers for Disease Control and Prevention. Infectious Disease Portal. Updated 2020. Accessed January 20, 2020. http://www.cdc.go.kr/npt/biz/npp/ist/simple/simplePdStatsMain.do.

7. Brolund A, Lagerqvist N, Byfors S, Struelens MJ, Monnet DL, Albiger B, et al. Worsening epidemiological situation of carbapenemase-producing Enterobacteriaceae in Europe, assessment by national experts from 37 countries, July 2018. Euro Surveill. 2019; 24(9):1900123.

8. Chotiprasitsakul D, Srichatrapimuk S, Kirdlarp S, Pyden AD, Santanirand P. Epidemiology of carbapenem-resistant Enterobacteriaceae: a 5-year experience at a tertiary care hospital. Infect Drug Resist. 2019; 12:461–468. PMID: 30863128.

9. Tran DM, Larsson M, Olson L, Hoang NTB, Le NK, Khu DTK, et al. High prevalence of colonisation with carbapenem-resistant Enterobacteriaceae among patients admitted to Vietnamese hospitals: risk factors and burden of disease. J Infect. 2019; 79(2):115–122. PMID: 31125639.

10. Won SY, Munoz-Price LS, Lolans K, Hota B, Weinstein RA, Hayden MK, et al. Emergence and rapid regional spread of Klebsiella pneumoniae carbapenemase-producing Enterobacteriaceae . Clin Infect Dis. 2011; 53(6):532–540. PMID: 21865189.

11. Hong SK, Yong D, Kim K, Hong SS, Hong SG, Khosbayar T, et al. First outbreak of KPC-2-producing Klebsiella pneumoniae sequence type 258 in a hospital in South Korea. J Clin Microbiol. 2013; 51(11):3877–3879. PMID: 24006005.

12. Go E, Ju SJ, Park S, Yoo J, Hwang KJ. Distributions of carbapenem-resistant Enterobacteriaceae (CRE) in Korea, 2018. Public Health Wkly Rep. 2019; 12(45):1977–1983.

13. Bhargava A, Hayakawa K, Silverman E, Haider S, Alluri KC, Datla S, et al. Risk factors for colonization due to carbapenem-resistant Enterobacteriaceae among patients exposed to long-term acute care and acute care facilities. Infect Control Hosp Epidemiol. 2014; 35(4):398–405. PMID: 24602945.

14. Lee HJ, Choi JK, Cho SY, Kim SH, Park SH, Choi SM, et al. Carbapenem-resistant Enterobacteriaceae: prevalence and risk factors in a single community-based hospital in Korea. Infect Chemother. 2016; 48(3):166–173. PMID: 27659436.

15. Mills JP, Talati NJ, Alby K, Han JH. The epidemiology of carbapenem-resistant Klebsiella pneumoniae colonization and infection among long-term acute care hospital residents. Infect Control Hosp Epidemiol. 2016; 37(1):55–60. PMID: 26455382.

16. Munoz-Price LS. Long-term acute care hospitals. Clin Infect Dis. 2009; 49(3):438–443. PMID: 19548836.

17. Lin MY, Lyles-Banks RD, Lolans K, Hines DW, Spear JB, Petrak R, et al. The importance of long-term acute care hospitals in the regional epidemiology of Klebsiella pneumoniae carbapenemase-producing Enterobacteriaceae . Clin Infect Dis. 2013; 57(9):1246–1252. PMID: 23946222.

18. Ben-David D, Masarwa S, Fallach N, Temkin E, Solter E, Carmeli Y, et al. Success of a national intervention in controlling carbapenem-resistant Enterobacteriaceae in Israel's long-term care facilities. Clin Infect Dis. 2019; 68(6):964–971. PMID: 29986007.

19. Hayden MK, Lin MY, Lolans K, Weiner S, Blom D, Moore NM, et al. Prevention of colonization and infection by Klebsiella pneumoniae carbapenemase-producing Enterobacteriaceae in long-term acute-care hospitals. Clin Infect Dis. 2015; 60(8):1153–1161. PMID: 25537877.

20. Kim BM, Jeon EJ, Jang JY, Chung JW, Park J, Choi JC, et al. Four year trend of carbapenem-resistance in newly opened ICUs of a university-affiliated hospital of south Korea. Tuberc Respir Dis (Seoul). 2012; 72(4):360–366. PMID: 23227077.

21. Huh K, Kim J, Cho SY, Ha YE, Joo EJ, Kang CI, et al. Continuous increase of the antimicrobial resistance among gram-negative pathogens causing bacteremia: a nationwide surveillance study by the Korean Network for Study on Infectious Diseases (KONSID). Diagn Microbiol Infect Dis. 2013; 76(4):477–482. PMID: 23721721.

22. Kim DK, Kim HS, Pinto N, Jeon J, D'Souza R, Kim MS, et al. Xpert CARBA-R assay for the detection of carbapenemase-producing organisms in intensive care unit patients of a Korean tertiary care hospital. Ann Lab Med. 2016; 36(2):162–165. PMID: 26709264.

23. Guideline for specimen collection and management for infectious diseases diagnosis. Updated 2018. Accessed December 12, 2018. http://www.prism.go.kr/homepage/lately/retrieveLatelyDetail.do;jsessionid=F32046F3D71BBB1E7E30E4DDF0AAB003.node02?research_id=1351000-201800220.

24. Kim J, Lee JY, Kim SI, Song W, Kim JS, Jung S, et al. Rates of fecal transmission of extended-spectrum β-lactamase-producing and carbapenem-resistant Enterobacteriaceae among patients in intensive care units in Korea. Ann Lab Med. 2014; 34(1):20–25. PMID: 24422191.

25. Kang JS, Yi J, Ko MK, Lee SO, Lee JE, Kim KH. Prevalence and risk factors of carbapenem-resistant Enterobacteriaceae acquisition in an emergency intensive care unit in a tertiary hospital in Korea: a case-control study. J Korean Med Sci. 2019; 34(18):e140. PMID: 31074254.

26. Park JW, Kwak SH, Jung J, Lee JY, Lim YJ, Choi HS, et al. The rate of acquisition of carbapenemase-producing Enterobacteriaceae among close contact patients depending on carbapenemase enzymes. Infect Chemother. 2020; 52(1):39–47. PMID: 32114721.

27. Hwang JH, Park JS, Lee E, Bae JY, Song KH, Choe PG, et al. Active surveillance for carbapenem-resistant Enterobacteriaceae, vancomycin-resistant enterococci and toxigenic Clostridium difficile among patients transferred from long-term care facilities in Korea. J Hosp Infect. 2018; 99(4):487–491. PMID: 29476883.

28. Blanco N, O'Hara LM, Harris AD. Transmission pathways of multidrug-resistant organisms in the hospital setting: a scoping review. Infect Control Hosp Epidemiol. 2019; 40(4):447–456. PMID: 30837029.