Ann Clin Microbiol.  2018 Jun;21(2):28-35. 10.5145/ACM.2018.21.2.28.

The Usefulness of Active Surveillance Culture of Extended-Spectrum β-Lactamase-Producing Escherichia coli in ICU Settings without Outbreak in the Situation of Wide Spread of Sequence Type 131 ESBL-Producing E. coli in Community

• Kim YA
• Park YS
• Kim H
• Seo YH
• Lee K

• KMID: 2414136
• DOI: http://doi.org/10.5145/ACM.2018.21.2.28

Abstract

BACKGROUND
In the present study, the prevalence and risk factors for acquisition of extended-spectrum β-lactamase (ESBL)-producing Escherichia coli in intensive care unit (ICU) settings without outbreak in the situation of widespread sequence type (ST) 131 ESBL-producing E. coli in a Korean community was investigated.
METHODS
Consecutive and prospective screening of ESBL-producing E. coli colonization was performed in all patients admitted to surgical or medical ICUs within 48 hours for two months. ESBL genotype was determined based on PCR and sequencing. PCR for O16-ST131/O25-ST131 was performed for all ESBL producers. Clinical information was obtained from a review of electronic medical record to determine the risk factors for ESBL-producing E. coli colonization.
RESULTS
The colonization rate of ESBL-producing E. coli at ICU admission was 14.9% (42/281). CTX-M-15 (N=15), CTX-M-14 (N=12), and CTX-M-27 (N=10) were commonly detected using PCR of ESBL genes. Approximately half (45.2%, 19/42) of ESBL producers were ST131 clone with 14 ST131-O25 and 5 ST131-O16. In univariate analysis, independent risk factor for acquisition of ESBL-producing E. coli compared with controls was ICU type (odds ratio, 2.05; P < 0.032); however, site of acquisition, previous antibiotic use, and hospital stay were not significant risk factors.
CONCLUSION
In this study, the colonization of ESBL-producing E. coli at ICU admission without outbreak was frequent and it could be an infection source, regardless of acquisition site. We recommend routine use of ASC to control endemic ESBL-producing E. coli considering the wide distribution of ST131-ESBL-producing E. coli in the Korean community.

Keyword

Escherichia coli; Extended-spectrum β-lactamase; Prevalence; Sequence type 131

MeSH Terms

Clone Cells
Colon
Electronic Health Records
Escherichia coli*
Escherichia*
Genotype
Humans
Intensive Care Units
Length of Stay
Mass Screening
Polymerase Chain Reaction
Prevalence
Prospective Studies
Risk Factors

Figure

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  Fig. 1. (A) Pulsed-field gel electrophoresis. SM, Lambda Ladders (Preomega, Wisconsin). (B) Dendrogram of XbaI-restricted DNA of colonizing ESBL-producing E. coli isolated from ICU-admitted patients (N=38).* *Five ESBL-producing E. coli isolates were excluded due to repeated failure of re-culture. Abbreviations: ST131, sequence type131; O25, serogroup O25; O16, serogroup O16; ESBL, extended-spectrum beta-lactamase.

Reference

References

1. Muto CA, Jernigan JA, Ostrowsky BE, Richet HM, Jarvis WR, Boyce JM, et al. SHEA guideline for preventing nosocomial transmission of multidrug-resistant strains of Staphylococcus aureus and enterococcus. Infect Control Hosp Epidemiol. 2003; 24:362–86.

2. Troché G, Joly LM, Guibert M, Zazzo JF. Detection and treatment of antibiotic-resistant bacterial carriage in a surgical intensive care unit: a 6-year prospective survey. Infect Control Hosp Epidemiol. 2005; 26:161–5.

3. Thouverez M, Talon D, Bertrand X. Control of Enterobacteriaceae producing extended-spectrum beta-lactamase in intensive care units: rectal screening may not be needed in non-epidemic situations. Infect Control Hosp Epidemiol. 2004; 25:838–41.

4. Gardam MA, Burrows LL, Kus JV, Brunton J, Low DE, Conly JM, et al. Is surveillance for multidrug-resistant Enterobacteriaceae an effective infection control strategy in the absence of an outbreak? J Infect Dis. 2002; 186:1754–60.

5. Paterson DL and Bonomo RA. Extended-spectrum beta-lactamases: a clinical update. Clin Microbiol Rev. 2005; 18:657–86.

6. Colpan A, Johnston B, Porter S, Clabots C, Anway R, Thao L, et al. Escherichia coli sequence type 131 (ST131) subclone H30 as an emergent multidrug-resistant pathogen among US veterans. Clin Infect Dis. 2013; 57:1256–65.

7. Johnson JR, Urban C, Weissman SJ, Jorgensen JH, Lewis JS 2nd, Hansen G, et al. Molecular epidemiological analysis of Escherichia coli sequence type ST131 (O25: H4) and bla _CTX-M-15 among extended-spectrum-β-lactamase-producing E. coli from the United States, 2000 to 2009. Antimicrob Agents Chemother. 2012; 56:2364–70.

8. Kim SY, Park YJ, Johnson JR, Yu JK, Kim YK, Kim YS. Prevalence and characteristics of Escherichia coli sequence type 131 and its H30 and H30Rx subclones: a multicenter study from Korea. Diagn Microbiol Infect Dis. 2016; 84:97–101.

9. Lee Y, Kim YA, Song W, Lee H, Lee HS, Jang SJ, et al. Recent trends in antimicrobial resistance in intensive care units in Korea. Korean J Nosocomial Infect Control. 2014; 19:29–36.

10. Kim YA, Kim JJ, Kim H, Lee K. Community-onset extended-spectrum-β-lactamase-producing Escherichia coli sequence type 131 at two Korean community hospitals: the spread of multidrug-resistant E. coli to the community via healthcare facilities. Int J Infect Dis. 2017; 54:39–42.

11. Park YS, Bae IK, Kim J, Jeong SH, Hwang SS, Seo YH, et al. Risk factors and molecular epidemiology of community-onset extended-spectrum β-lactamase-producing Escherichia coli bacteremia. Yonsei Med J. 2014; 55:467–75.

12. Benenson S, Levin PD, Block C, Adler A, Ergaz Z, Peleg O, et al. Continuous surveillance to reduce extended-spectrum β-lactamase Klebsiella pneumoniae colonization in the neonatal intensive care unit. Neonatology. 2013; 103:155–60.

13. Ko YJ, Moon HW, Hur M, Park CM, Cho SE, Yun YM. Fecal carriage of extended-spectrum β-lactamase-producing Enterobacteriaceae in Korean community and hospital settings. Infection. 2013; 41:9–13.

14. 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; 34:20–5.

15. CLSI. Performance standards for antimicrobial susceptibility testing: 26th informational supplement. CLSI document M100S. Wayne, PA: Clinical and Laboratory Standards Institute;2016.

16. Ryoo NH, Kim EC, Hong SG, Park YJ, Lee K, Bae IK, et al. Dissemination of SHV-12 and CTX-M-type extended-spectrum beta-lactamases among clinical isolates of Escherichia coli and Klebsiella pneumoniae and emergence of GES-3 in Korea. J Antimicrob Chemother. 2005; 56:698–702.

17. Park Y, Kang HK, Bae IK, Kim J, Kim JS, Uh Y, et al. Prevalence of the extended-spectrum beta-lactamase and qnr genes in clinical isolates of Escherichia coli. Korean J Lab Med. 2009; 29:218–23.

18. Johnson JR, Clermont O, Johnston B, Clabots C, Tchesnokova V, Sokurenko E, et al. Rapid and specific detection, molecular epidemiology, and experimental virulence of the O16 subgroup within Escherichia coli sequence type 131. J Clin Microbiol. 2014; 52:1358–65.

19. Montecalvo MA, Jarvis WR, Uman J, Shay DK, Petrullo C, Rodney K, et al. Infection-control measures reduce transmission of vancomycin-resistant enterococci in an endemic setting. Ann Intern Med. 1999; 131:269–72.

20. Ostrowsky BE, Trick WE, Sohn AH, Quirk SB, Holt S, Carson LA, et al. Control of vancomycin-resistant enterococcus in health care facilities in a region. N Engl J Med. 2001; 344:1427–33.

21. Rupp ME, Marion N, Fey PD, Bolam DL, Iwen PC, Overfelt CM, et al. Outbreak of vancomycin-resistant Enterococcus faecium in a neonatal intensive care unit. Infect Control Hosp Epidemiol. 2001; 22:301–3.

22. Nijssen S, Bonten MJ, Weinstein RA. Are active microbiological surveillance and subsequent isolation needed to prevent the spread of methicillin-resistant Staphylococcus aureus? Clin Infect Dis. 2005; 40:405–9.

23. Shitrit P, Gottesman BS, Katzir M, Kilman A, Ben-Nissan Y, Chowers M. Active surveillance for methicillin-resistant Staphylococcus aureus (MRSA) decreases the incidence of MRSA bacteremia. Infect Control Hosp Epidemiol. 2006; 27:1004–8.

24. Kurup A, Chlebicka N, Tan KY, Chen EX, Oon L, Ling TA, et al. Active surveillance testing and decontamination strategies in intensive care units to reduce methicillin-resistant Staphylococcus aureus infections. Am J Infect Control. 2010; 38:361–7.

25. Holzmann-Pazgal G, Monney C, Davis K, Wanger A, Strobel N, Zhong F. Active surveillance culturing impacts methicillin-resistant Staphylococcus aureus acquisition in a pediatric intensive care unit. Pediatr Crit Care Med. 2011; 12:e171–5.

26. Ohkushi D, Uehara Y, Iwamoto A, Misawa S, Kondo S, Shimizu K, et al. An effective active surveillance method for controlling nosocomial MRSA transmission in a Japanese hospital. J Infect Chemother. 2013; 19:871–5.

27. Popoola VO, Budd A, Wittig SM, Ross T, Aucott SW, Perl TM, et al. Methicillin-resistant Staphylococcus aureus transmission and infections in a neonatal intensive care unit despite active surveillance cultures and decolonization: challenges for infection prevention. Infect Control Hosp Epidemiol. 2014; 35:412–8.

28. Popoola VO, Colantuoni E, Suwantarat N, Pierce R, Carroll KC, Aucott SW, et al. Active surveillance cultures and decolonization to reduce Staphylococcus aureus infections in the neonatal intensive care unit. Infect Control Hosp Epidemiol. 2016; 37:381–7.

29. Pierce R, Lessler J, Popoola VO, Milstone AM. Meticillin-resistant Staphylococcus aureus (MRSA) acquisition risk in an endemic neonatal intensive care unit with an active surveillance culture and decolonization programme. J Hosp Infect. 2017; 95:91–7.

30. Niumsup PR, Tansawai U, Na-Udom A, Jantapalaboon D, Assawatheptawee K, Kiddee A, et al. Prevalence and risk factors for intestinal carriage of CTX-M-type ESBLs in Enterobacteriaceae from a Thai community. Eur J Clin Microbiol Infect Dis. 2018; 37:69–75.

31. Woerther PL, Burdet C, Chachaty E, Andremont A. Trends in human fecal carriage of extended-spectrum β-lactamases in the community: toward the globalization of CTX-M. Clin Microbiol Rev. 2013; 26:744–58.

32. Kim JS, Kim MJ, Kim SJ, Shin E, Oh KH, Kim SG, et al. First description of CTX-M-3 extended-spectrum β-lactamase in an outbreak strain of Shiga toxin-producing Escherichia coli O103: H2. Int J Antimicrob Agents. 2016; 47:244–5.

33. Ko YJ, Moon HW, Hur M, Yun YM. Risk factors of fecal carriage with extended-spectrum β-lactamase-producing Enterobacteriaceae in hospitalized patients. Am J Infect Control. 2013; 41:1241–3.