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ESBL-colonization at ICU admission: impact on subsequent infection, carbapenem-consumption, and outcome

  • Aurélien Emmanuel Martinez (a1), Andreas Widmer (a1), Reno Frei (a1) (a2), Hans Pargger (a3), Daniel Tuchscherer (a3), Stephan Marsch (a4), Adrian Egli (a2) (a5) and Sarah Tschudin-Sutter (a1) (a6)...



To determine whether colonization with extended-spectrum β-lactamase–producing Enterobacteriaceae (ESBL-PE) predicts the risk for subsequent infection and impacts carbapenem-consumption and outcome in intensive care unit (ICU) patients.


Prospective cohort study.


The 2 ICUs in the University Hospital Basel in Switzerland.


All patients admitted to the 2 ICUs providing mechanical ventilation and an expected ICU stay >48 hours.


Patients were routinely screened for ESBL-PE carriage by rectal swab on admission. Competing risk regression analyses were applied to calculate hazard ratios (HRs) for infection with ESBL-PE and mortality. Length of hospital stay, length of ICU stay, and duration of carbapenem exposure were compared using the Mann-Whitney U test.


Among 302 patients, 24 (8.0%) were colonized with ESBL-PE on ICU admission. Infections with ESBL-PE occurred in 4 patients, of whom 3 (75%) were identified as ESBL-PE colonized on admission. ESBL-PE colonization on admission was associated with subsequent ESBL-PE infection (hazard ratio [HR], 25.52; 95% confidence interval [CI], 2.40–271.41; P = .007) and exposure to carbapenems (HR, 2.42; 95% CI, 1.01–5.79; P = .047), whereas duration of carbapenem exposure did not differ in relation to ESBL-PE colonization (median, 7 days [IQR, 3–8 days] vs median, 6 days [IQR 3–9 days]; P = 0.983). Patients colonized with ESBL-PE were not at increased risk for death overall (HR, 1.00; 95% CI, 0.44–2.30; P = .993) or death attributable to infection (HR, 1.20; 95% CI, 0.28–5.11; P = .808).


Screening strategies for detection of ESBL-PE colonization on ICU admission may allow the identification of patients at highest risk for ESBL-PE infection and the correct allocation of empiric carbapenem treatment.


Corresponding author

Author for correspondence: Sarah Tschudin-Sutter, Email:


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PREVIOUS PRESENTATION: Preliminary results of this study were presented as a poster and as an abstract at the 27th ECCMID European Congress of Clinical Microbiology and Infectious Diseases on April 24, 2017, in Vienna, Austria.



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1.Paterson, DL, Bonomo, RA. Extended-spectrum β-lactamases: a clinical update. Clin Microbiol Rev 2005;18:657686.
2.Bradford, PA. Extended-spectrum β-lactamases in the 21st century: characterization, epidemiology, and detection of this important resistance threat. Clin Microbiol Rev 2001;14:933951.
3.Candevir Ulu, A, Kurtaran, B, Inal, AS, et al. Risk factors of carbapenem-resistant Klebsiella pneumoniae infection: a serious threat in ICUs. Med Sci Monit 2015;21:219224.
4.Chelazzi, C, Pettini, E, Villa, G, De Gaudio, AR. Epidemiology, associated factors and outcomes of ICU-acquired infections caused by gram-negative bacteria in critically ill patients: an observational, retrospective study. BMC Anesthesiol 2015;15:125.
5.Vincent, JL, Bihari, DJ, Suter, PM, et al. The prevalence of nosocomial infection in intensive care units in Europe. Results of the European Prevalence of Infection in Intensive Care (EPIC) Study. JAMA 1995;274:639644.
6.Richards, MJ, Edwards, JR, Culver, DH, Gaynes, RP. Nosocomial infections in combined medical-surgical intensive care units in the United States. Infect Control Hosp Epidemiol 2000;21:510515.
7.Johnson, MT, Reichley, R, Hoppe-Bauer, J, Dunne, WM, Micek, S, Kollef, M. Impact of previous antibiotic therapy on outcome of gram-negative severe sepsis. Crit Care Med 2011;39:18591865.
8.Pakyz, AL, Oinonen, M, Polk, RE. Relationship of carbapenem restriction in 22 university teaching hospitals to carbapenem use and carbapenem-resistant Pseudomonas aeruginosa. Antimicrob Agents Chemother 2009;53:19831986.
9.Kritsotakis, EI, Tsioutis, C, Roumbelaki, M, Christidou, A, Gikas, A. Antibiotic use and the risk of carbapenem-resistant extended-spectrum-beta-lactamase-producing Klebsiella pneumoniae infection in hospitalized patients: results of a double case-control study. J Antimicrob Chemother 2011;66:13831391.
10.Biehl, LM, Schmidt-Hieber, M, Liss, B, Cornely, OA, Vehreschild, MJGT. Colonization and infection with extended spectrum beta-lactamase producing Enterobacteriaceae in high-risk patients—review of the literature from a clinical perspective. Crit Rev Microbiol 2016;42:116.
11.Cornejo-Juárez, P, Suárez-Cuenca, JA, Volkow-Fernández, P, et al. Fecal ESBL Escherichia coli carriage as a risk factor for bacteremia in patients with hematological malignancies. Support Care Cancer 2016;24:253259.
12.Vehreschild, MJGT, Hamprecht, A, Peterson, L, et al. A multicentre cohort study on colonization and infection with ESBL-producing Enterobacteriaceae in high-risk patients with haematological malignancies. J Antimicrob Chemother 2014;69:33873392.
13.Ebrahimi, F, Mózes, J, Monostori, J, et al. Comparison of the faecal colonization rates with extended-spectrum beta-lactamase producing enterobacteria among patients in different wards, outpatients and screened medical students. Microbiol Immunol 2016;60:285294.
14.Bassetti, M, De Waele, JJ, Eggimann, P, et al. Preventive and therapeutic strategies in critically ill patients with highly resistant bacteria. Intens Care Med 2015;41:776795.
15.Hinic, V, Ziegler, J, Straub, C, Goldenberger, D, Frei, R. Extended-spectrum beta-lactamase (ESBL) detection directly from urine samples with the rapid isothermal amplification-based eazyplex(R) SuperBug CRE assay: proof of concept. J Microbiol Methods 2015;119:203205.
16.Magiorakos, AP, Srinivasan, A, Carey, RB, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 2012;18:268281.
17.National Healthcare Safety Network (NHSN) Patient Safety Component Manual. Centers for Disease Control and Prevention website. Published 2018. Accessed January 15, 2019.
18.Fine, JP, Gray, RJ. A proportional hazards model for the subdistribution of a competing risk. J Am Stat Assoc 1999;94:496509.
19.Coviello, V, Boggess, M. Cumulative incidence estimation in the presence of competing risks. Stata J 2004;4:103112.
20.Pires, J, Kuenzli, E, Hauser, C, et al. Intestinal colonisation with extended-spectrum cephalosporin-resistant Enterobacteriaceae in different populations in Switzerland: prevalence, risk factors and molecular features. J Glob Antimicrob Resist 2017;12:1719.
21.Harris, AD, McGregor, JC, Johnson, JA, et al. Risk factors for colonization with extended-spectrum beta-lactamase-producing bacteria and intensive care unit admission. Emerg Infect Dis 2007;13:11441149.
22.Mulki, SS, Ramamurthy, K, Bhat, S. Fecal carriage of extended-spectrum beta-lactamase-producing Enterobacteriaceae in intensive care unit patients. Indian J Crit Care Med 2017;21:525527.
23.Pilmis, B, Cattoir, V, Lecointe, D, et al. Carriage of ESBL-producing Enterobacteriaceae in French hospitals: the PORTABLSE study. J Hosp Infect 2018;98:247252.
24.Repesse, X, Artiguenave, M, Paktoris-Papine, S, et al. Epidemiology of extended-spectrum beta-lactamase-producing Enterobacteriaceae in an intensive care unit with no single rooms. Ann Intensive Care 2017;7:73.
25.Osthoff, M, McGuinness, SL, Wagen, AZ, Eisen, DP. Urinary tract infections due to extended-spectrum beta-lactamase-producing gram-negative bacteria: identification of risk factors and outcome predictors in an Australian tertiary referral hospital. Int J Infect Dis 2015;34:7983.
26.Maslikowska, JA, Walker, SA, Elligsen, M, et al. Impact of infection with extended-spectrum beta-lactamase-producing Escherichia coli or Klebsiella species on outcome and hospitalization costs. J Hosp Infect 2016;92:3341.
27.Rodriguez-Bano, J, Picon, E, Gijon, P, et al. Community-onset bacteremia due to extended-spectrum beta-lactamase-producing Escherichia coli: risk factors and prognosis. Clin Infect Dis 2010;50:4048.
28.Barbier, F, Pommier, C, Essaied, W, et al. Colonization and infection with extended-spectrum beta-lactamase-producing Enterobacteriaceae in ICU patients: what impact on outcomes and carbapenem exposure? J Antimicrob Chemother 2016;71:10881097.
29.Leistner, R, Bloch, A, Sakellariou, C, Gastmeier, P, Schwab, F. Costs and length of stay associated with extended-spectrum beta-lactamase production in cases of Escherichia coli bloodstream infection. J Glob Antimicrob Resist 2014;2:107109.
30.Tumbarello, M, Spanu, T, Di Bidino, R, et al. Costs of bloodstream infections caused by Escherichia coli and influence of extended-spectrum-beta-lactamase production and inadequate initial antibiotic therapy. Antimicrob Agents Chemother 2010;54:40854091.
31.Harris, PN, Yin, M, Jureen, R, et al. Comparable outcomes for beta-lactam/beta-lactamase inhibitor combinations and carbapenems in definitive treatment of bloodstream infections caused by cefotaxime-resistant Escherichia coli or Klebsiella pneumoniae. Antimicrob Resist Infect Control 2015;4:14.
32.Ng, TM, Khong, WX, Harris, PN, et al. Empiric piperacillin-tazobactam versus carbapenems in the treatment of bacteraemia due to extended-spectrum beta-lactamase-producing Enterobacteriaceae. PLoS One 2016;11:e0153696.
33.Liss, BJ, Vehreschild, JJ, Cornely, OA, et al. Intestinal colonisation and blood stream infections due to vancomycin-resistant enterococci (VRE) and extended-spectrum beta-lactamase-producing Enterobacteriaceae (ESBLE) in patients with haematological and oncological malignancies. Infection 2012;40:613619.
34.Cheikh, A, Belefquih, B, Chajai, Y, Cheikhaoui, Y, El Hassani, A, Benouda, A. Enterobacteriaceae producing extended-spectrum beta-lactamases (ESBLs) colonization as a risk factor for developing ESBL infections in pediatric cardiac surgery patients: “retrospective cohort study”. BMC Infect Dis 2017;17:237.
35.Cornejo-Juarez, P, Suarez-Cuenca, JA, Volkow-Fernandez, P, et al. Fecal ESBL Escherichia coli carriage as a risk factor for bacteremia in patients with hematological malignancies. Support Care Cancer 2016;24:253259.
36.Grohs, P, Podglajen, I, Guerot, E, et al. Assessment of five screening strategies for optimal detection of carriers of third-generation cephalosporin-resistant Enterobacteriaceae in intensive care units using daily sampling. Clin Microbiol Infect 2014;20:O879O886.
37.van Prehn, J, Kaiser, AM, van der Werff, SD, van Mansfeld, R, Vandenbroucke-Grauls, C. Colonization sites in carriers of ESBL-producing gram-negative bacteria. Antimicrob Resist Infect Control 2018;7:52.


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