Skip to main content
Top
Published in: Annals of Intensive Care 1/2017

Open Access 01-12-2017 | Research

Frequency, associated factors and outcome of multi-drug-resistant intensive care unit-acquired pneumonia among patients colonized with extended-spectrum β-lactamase-producing Enterobacteriaceae

Authors: Keyvan Razazi, Armand Mekontso Dessap, Guillaume Carteaux, Chloé Jansen, Jean-Winoc Decousser, Nicolas de Prost, Christian Brun-Buisson

Published in: Annals of Intensive Care | Issue 1/2017

Login to get access

Abstract

Background

We assessed prevalence, associated factors and prognosis of extended-spectrum beta-lactamase-producing Enterobacteriaceae pneumonia acquired in intensive care unit (ESBL-PE pneumonia) among carriers. Variables associated with nosocomial pneumonia caused by carbapenem-resistant bacteria (CRB) were also assessed.

Methods

A 6-year prospective study (May 2009–March 2015) in the medical ICU of an 850-bed university-affiliated hospital was conducted.

Results

Of the 6303 patients admitted, 843 (13.4%) had ESBL-PE carriage detected. Among carriers, 111 (13%) patients developed ICU-acquired pneumonia of whom 48 (43%) had ESBL-PE pneumonia (6% of carriers). By multivariable analysis, SAPS II at admission >43 [OR 2.81 (1.16–6.79)] and colonization with Enterobacter sp. or K. pneumoniae species [OR 10.96 (2.93–41.0)] were independent predictive factors for ESBL-PE pneumonia in colonized patients, whereas receipt of >2 days of amoxicillin/clavulanic acid during the ICU stay [OR 0.24 (0.08–0.71)] was protective. Patients with ESBL-PE pneumonia had a higher SOFA score (p = 0.037) and more frequent septic shock at pneumonia onset (p = 0.047). However, ESBL-PE pneumonia was not an independent predictor of mortality. Twenty-five patients had pneumonia caused by CRB. Chronic renal insufficiency, administration of third-generation cephalosporin within the past 3 months, acute respiratory distress syndrome before pneumonia and prior therapy with a carbapenem or fluoroquinolones were associated with CRB pneumonia in this selected population.

Conclusions

Although few ESBL-PE carriers developed ESBL-PE pneumonia overall, a high proportion of pneumonia were caused by ESBL-PE in carriers developing ICUAP. ESBL-PE pneumonia was not an independent predictor of mortality. As pneumonia caused by CRB is increasing, knowledge of factors associated with ESBL-PE or CRB pneumonia may help empiric therapy of pneumonia among ESBL-PE carriers.
Appendix
Available only for authorised users
Literature
2.
go back to reference Lee SY, Kotapati S, Kuti JL, Nightingale CH, Nicolau DP. Impact of extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella species on clinical outcomes and hospital costs: a matched cohort study. Infect Control Hosp Epidemiol. 2006;27(11):1226–32.CrossRefPubMed Lee SY, Kotapati S, Kuti JL, Nightingale CH, Nicolau DP. Impact of extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella species on clinical outcomes and hospital costs: a matched cohort study. Infect Control Hosp Epidemiol. 2006;27(11):1226–32.CrossRefPubMed
3.
go back to reference Tumbarello M, Spanu T, Sanguinetti M, Citton R, Montuori E, Leone F, et al. Bloodstream infections caused by extended-spectrum-beta-lactamase-producing Klebsiella pneumoniae: risk factors, molecular epidemiology, and clinical outcome. Antimicrob Agents Chemother. 2006;50(2):498–504.CrossRefPubMedPubMedCentral Tumbarello M, Spanu T, Sanguinetti M, Citton R, Montuori E, Leone F, et al. Bloodstream infections caused by extended-spectrum-beta-lactamase-producing Klebsiella pneumoniae: risk factors, molecular epidemiology, and clinical outcome. Antimicrob Agents Chemother. 2006;50(2):498–504.CrossRefPubMedPubMedCentral
4.
go back to reference Damas P, Layios N, Seidel L, Nys M, Melin P, Ledoux D. Severity of ICU-acquired pneumonia according to infectious microorganisms. Intensive Care Med. 2011;37(7):1128–35.CrossRefPubMed Damas P, Layios N, Seidel L, Nys M, Melin P, Ledoux D. Severity of ICU-acquired pneumonia according to infectious microorganisms. Intensive Care Med. 2011;37(7):1128–35.CrossRefPubMed
5.
go back to reference Rottier WC, Ammerlaan HSM, Bonten MJM. Effects of confounders and intermediates on the association of bacteraemia caused by extended-spectrum β-lactamase-producing Enterobacteriaceae and patient outcome: a meta-analysis. J Antimicrob Chemother. 2012;67(6):1311–20.CrossRefPubMed Rottier WC, Ammerlaan HSM, Bonten MJM. Effects of confounders and intermediates on the association of bacteraemia caused by extended-spectrum β-lactamase-producing Enterobacteriaceae and patient outcome: a meta-analysis. J Antimicrob Chemother. 2012;67(6):1311–20.CrossRefPubMed
6.
go back to reference Cantón R, Akóva M, Carmeli Y, Giske CG, Glupczynski Y, Gniadkowski M, et al. Rapid evolution and spread of carbapenemases among Enterobacteriaceae in Europe. Clin Microbiol Infect. 2012;18(5):413–31.CrossRefPubMed Cantón R, Akóva M, Carmeli Y, Giske CG, Glupczynski Y, Gniadkowski M, et al. Rapid evolution and spread of carbapenemases among Enterobacteriaceae in Europe. Clin Microbiol Infect. 2012;18(5):413–31.CrossRefPubMed
7.
go back to reference Trouillet JL, Vuagnat A, Combes A, Kassis N, Chastre J, Gibert C. Pseudomonas aeruginosa ventilator-associated pneumonia: comparison of episodes due to piperacillin-resistant versus piperacillin-susceptible organisms. Clin Infect Dis. 2002;34(8):1047–54.CrossRefPubMed Trouillet JL, Vuagnat A, Combes A, Kassis N, Chastre J, Gibert C. Pseudomonas aeruginosa ventilator-associated pneumonia: comparison of episodes due to piperacillin-resistant versus piperacillin-susceptible organisms. Clin Infect Dis. 2002;34(8):1047–54.CrossRefPubMed
8.
go back to reference Armand-Lefèvre L, Angebault C, Barbier F, Hamelet E, Defrance G, Ruppé E, et al. Emergence of imipenem-resistant gram-negative bacilli in intestinal flora of intensive care patients. Antimicrob Agents Chemother. 2013;57(3):1488–95.CrossRefPubMedPubMedCentral Armand-Lefèvre L, Angebault C, Barbier F, Hamelet E, Defrance G, Ruppé E, et al. Emergence of imipenem-resistant gram-negative bacilli in intestinal flora of intensive care patients. Antimicrob Agents Chemother. 2013;57(3):1488–95.CrossRefPubMedPubMedCentral
9.
go back to reference Boucher HW, Talbot GH, Bradley JS, Edwards JE, Gilbert D, Rice LB, et al. Bad bugs, no drugs: no ESKAPE! An update from the Infectious Diseases Society of America. Clin Infect Dis. 2009;48(1):1–12.CrossRefPubMed Boucher HW, Talbot GH, Bradley JS, Edwards JE, Gilbert D, Rice LB, et al. Bad bugs, no drugs: no ESKAPE! An update from the Infectious Diseases Society of America. Clin Infect Dis. 2009;48(1):1–12.CrossRefPubMed
10.
go back to reference Depuydt P, Benoit D, Vogelaers D, Decruyenaere J, Vandijck D, Claeys G, et al. Systematic surveillance cultures as a tool to predict involvement of multidrug antibiotic resistant bacteria in ventilator-associated pneumonia. Intensive Care Med. 2008;34(4):675–82.CrossRefPubMed Depuydt P, Benoit D, Vogelaers D, Decruyenaere J, Vandijck D, Claeys G, et al. Systematic surveillance cultures as a tool to predict involvement of multidrug antibiotic resistant bacteria in ventilator-associated pneumonia. Intensive Care Med. 2008;34(4):675–82.CrossRefPubMed
11.
go back to reference Derde LPG, Cooper BS, Goossens H, Malhotra-Kumar S, Willems RJL, Gniadkowski M, et al. Interventions to reduce colonisation and transmission of antimicrobial-resistant bacteria in intensive care units: an interrupted time series study and cluster randomised trial. Lancet Infect Dis. 2014;14(1):31–9.CrossRefPubMedPubMedCentral Derde LPG, Cooper BS, Goossens H, Malhotra-Kumar S, Willems RJL, Gniadkowski M, et al. Interventions to reduce colonisation and transmission of antimicrobial-resistant bacteria in intensive care units: an interrupted time series study and cluster randomised trial. Lancet Infect Dis. 2014;14(1):31–9.CrossRefPubMedPubMedCentral
12.
go back to reference Le Gall JR, Lemeshow S, Saulnier F. A new simplified acute physiology score (SAPS II) based on a European/North American multicenter study. JAMA. 1993;270(24):2957–63.CrossRefPubMed Le Gall JR, Lemeshow S, Saulnier F. A new simplified acute physiology score (SAPS II) based on a European/North American multicenter study. JAMA. 1993;270(24):2957–63.CrossRefPubMed
13.
go back to reference Charlson ME, Pompei P, Ales KL, MacKenzie CR. A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis. 1987;40(5):373–83.CrossRefPubMed Charlson ME, Pompei P, Ales KL, MacKenzie CR. A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis. 1987;40(5):373–83.CrossRefPubMed
14.
go back to reference American Thoracic Society, Infectious Diseases Society of America. Guidelines for the management of adults with hospital-acquired, ventilator-associated, and healthcare-associated pneumonia. Am J Respir Crit Care Med. 2005;171(4):388–416.CrossRef American Thoracic Society, Infectious Diseases Society of America. Guidelines for the management of adults with hospital-acquired, ventilator-associated, and healthcare-associated pneumonia. Am J Respir Crit Care Med. 2005;171(4):388–416.CrossRef
15.
go back to reference Barbier F, Pommier C, Essaied W, Garrouste-Orgeas M, Schwebel C, Ruckly S, et al. Colonization and infection with extended-spectrum β-lactamase-producing Enterobacteriaceae in ICU patients: what impact on outcomes and carbapenem exposure? J Antimicrob Chemother. 2016;71(4):1088–97.CrossRefPubMed Barbier F, Pommier C, Essaied W, Garrouste-Orgeas M, Schwebel C, Ruckly S, et al. Colonization and infection with extended-spectrum β-lactamase-producing Enterobacteriaceae in ICU patients: what impact on outcomes and carbapenem exposure? J Antimicrob Chemother. 2016;71(4):1088–97.CrossRefPubMed
16.
go back to reference Guet-Revillet H, Le Monnier A, Breton N, Descamps P, Lecuyer H, Alaabouche I, et al. Environmental contamination with extended-spectrum β-lactamases: is there any difference between Escherichia coli and Klebsiella spp? Am J Infect Control. 2012;40(9):845–8.CrossRefPubMed Guet-Revillet H, Le Monnier A, Breton N, Descamps P, Lecuyer H, Alaabouche I, et al. Environmental contamination with extended-spectrum β-lactamases: is there any difference between Escherichia coli and Klebsiella spp? Am J Infect Control. 2012;40(9):845–8.CrossRefPubMed
17.
go back to reference Sakellariou C, Gürntke S, Steinmetz I, Kohler C, Pfeifer Y, Gastmeier P, et al. Sepsis caused by extended-spectrum beta-lactamase (ESBL)-positive K. pneumoniae and E. coli: comparison of severity of sepsis, delay of anti-infective therapy and ESBL genotype. PLoS ONE. 2016;11(7):e0158039.CrossRefPubMedPubMedCentral Sakellariou C, Gürntke S, Steinmetz I, Kohler C, Pfeifer Y, Gastmeier P, et al. Sepsis caused by extended-spectrum beta-lactamase (ESBL)-positive K. pneumoniae and E. coli: comparison of severity of sepsis, delay of anti-infective therapy and ESBL genotype. PLoS ONE. 2016;11(7):e0158039.CrossRefPubMedPubMedCentral
18.
go back to reference Leistner R, Gürntke S, Sakellariou C, Denkel LA, Bloch A, Gastmeier P, et al. Bloodstream infection due to extended-spectrum beta-lactamase (ESBL)-positive K. pneumoniae and E. coli: an analysis of the disease burden in a large cohort. Infection. 2014;42(6):991–7.CrossRefPubMed Leistner R, Gürntke S, Sakellariou C, Denkel LA, Bloch A, Gastmeier P, et al. Bloodstream infection due to extended-spectrum beta-lactamase (ESBL)-positive K. pneumoniae and E. coli: an analysis of the disease burden in a large cohort. Infection. 2014;42(6):991–7.CrossRefPubMed
19.
go back to reference Bruyère R, Vigneron C, Bador J, Aho S, Toitot A, Quenot J-P, et al. Significance of prior digestive colonization with extended-spectrum β-lactamase-producing Enterobacteriaceae in patients with ventilator-associated pneumonia. Crit Care Med. 2016;44(4):699–706.PubMed Bruyère R, Vigneron C, Bador J, Aho S, Toitot A, Quenot J-P, et al. Significance of prior digestive colonization with extended-spectrum β-lactamase-producing Enterobacteriaceae in patients with ventilator-associated pneumonia. Crit Care Med. 2016;44(4):699–706.PubMed
20.
go back to reference Carbonne H, Le Dorze M, Bourrel A-S, Poupet H, Poyart C, Cambau E, et al. Relation between presence of extended-spectrum β-lactamase-producing Enterobacteriaceae in systematic rectal swabs and respiratory tract specimens in ICU patients. Ann Intensive Care. 2017;7(1):13.CrossRefPubMedPubMedCentral Carbonne H, Le Dorze M, Bourrel A-S, Poupet H, Poyart C, Cambau E, et al. Relation between presence of extended-spectrum β-lactamase-producing Enterobacteriaceae in systematic rectal swabs and respiratory tract specimens in ICU patients. Ann Intensive Care. 2017;7(1):13.CrossRefPubMedPubMedCentral
21.
go back to reference Boyer A, Doussau A, Thiébault R, Venier AG, Tran V, Boulestreau H, et al. Pseudomonas aeruginosa acquisition on an intensive care unit: relationship between antibiotic selective pressure and patients’ environment. Crit Care Lond Engl. 2011;15(1):R55.CrossRef Boyer A, Doussau A, Thiébault R, Venier AG, Tran V, Boulestreau H, et al. Pseudomonas aeruginosa acquisition on an intensive care unit: relationship between antibiotic selective pressure and patients’ environment. Crit Care Lond Engl. 2011;15(1):R55.CrossRef
22.
go back to reference Thuong M, Arvaniti K, Ruimy R, de la Salmonière P, Scanvic-Hameg A, Lucet JC, et al. Epidemiology of Pseudomonas aeruginosa and risk factors for carriage acquisition in an intensive care unit. J Hosp Infect. 2003;53(4):274–82.CrossRefPubMed Thuong M, Arvaniti K, Ruimy R, de la Salmonière P, Scanvic-Hameg A, Lucet JC, et al. Epidemiology of Pseudomonas aeruginosa and risk factors for carriage acquisition in an intensive care unit. J Hosp Infect. 2003;53(4):274–82.CrossRefPubMed
23.
go back to reference Luyt C-E, Aubry A, Lu Q, Micaelo M, Bréchot N, Brossier F, et al. Imipenem, meropenem, or doripenem to treat patients with Pseudomonas aeruginosa ventilator-associated pneumonia. Antimicrob Agents Chemother. 2014;58(3):1372–80.CrossRefPubMedPubMedCentral Luyt C-E, Aubry A, Lu Q, Micaelo M, Bréchot N, Brossier F, et al. Imipenem, meropenem, or doripenem to treat patients with Pseudomonas aeruginosa ventilator-associated pneumonia. Antimicrob Agents Chemother. 2014;58(3):1372–80.CrossRefPubMedPubMedCentral
24.
go back to reference Vodovar D, Marcadé G, Rousseau H, Raskine L, Vicaut E, Deye N, et al. Predictive factors for extended-spectrum beta-lactamase producing Enterobacteriaceae causing infection among intensive care unit patients with prior colonization. Infection. 2014;42(4):743–8.CrossRefPubMed Vodovar D, Marcadé G, Rousseau H, Raskine L, Vicaut E, Deye N, et al. Predictive factors for extended-spectrum beta-lactamase producing Enterobacteriaceae causing infection among intensive care unit patients with prior colonization. Infection. 2014;42(4):743–8.CrossRefPubMed
25.
go back to reference Shorr AF. Review of studies of the impact on Gram-negative bacterial resistance on outcomes in the intensive care unit. Crit Care Med. 2009;37(4):1463–9.CrossRefPubMed Shorr AF. Review of studies of the impact on Gram-negative bacterial resistance on outcomes in the intensive care unit. Crit Care Med. 2009;37(4):1463–9.CrossRefPubMed
26.
go back to reference Lambert M-L, Suetens C, Savey A, Palomar M, Hiesmayr M, Morales I, et al. Clinical outcomes of health-care-associated infections and antimicrobial resistance in patients admitted to European intensive-care units: a cohort study. Lancet Infect Dis. 2011;11(1):30–8.CrossRefPubMed Lambert M-L, Suetens C, Savey A, Palomar M, Hiesmayr M, Morales I, et al. Clinical outcomes of health-care-associated infections and antimicrobial resistance in patients admitted to European intensive-care units: a cohort study. Lancet Infect Dis. 2011;11(1):30–8.CrossRefPubMed
27.
go back to reference Nguile-Makao M, Zahar J-R, Français A, Tabah A, Garrouste-Orgeas M, Allaouchiche B, et al. Attributable mortality of ventilator-associated pneumonia: respective impact of main characteristics at ICU admission and VAP onset using conditional logistic regression and multi-state models. Intensive Care Med. 2010;36(5):781–9.CrossRefPubMed Nguile-Makao M, Zahar J-R, Français A, Tabah A, Garrouste-Orgeas M, Allaouchiche B, et al. Attributable mortality of ventilator-associated pneumonia: respective impact of main characteristics at ICU admission and VAP onset using conditional logistic regression and multi-state models. Intensive Care Med. 2010;36(5):781–9.CrossRefPubMed
Metadata
Title
Frequency, associated factors and outcome of multi-drug-resistant intensive care unit-acquired pneumonia among patients colonized with extended-spectrum β-lactamase-producing Enterobacteriaceae
Authors
Keyvan Razazi
Armand Mekontso Dessap
Guillaume Carteaux
Chloé Jansen
Jean-Winoc Decousser
Nicolas de Prost
Christian Brun-Buisson
Publication date
01-12-2017
Publisher
Springer International Publishing
Published in
Annals of Intensive Care / Issue 1/2017
Electronic ISSN: 2110-5820
DOI
https://doi.org/10.1186/s13613-017-0283-4

Other articles of this Issue 1/2017

Annals of Intensive Care 1/2017 Go to the issue