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Published in: BMC Infectious Diseases 1/2016

Open Access 01-12-2016 | Research article

Extended-spectrum beta-lactamase − producing enterobacteriaceae in the intensive care unit: acquisition does not mean cross-transmission

Authors: Mikael Alves, Astrid Lemire, Dominique Decré, Dimitri Margetis, Naïke Bigé, Claire Pichereau, Hafid Ait-Oufella, Jean-Luc Baudel, Georges Offenstadt, Bertrand Guidet, Frédéric Barbut, Eric Maury

Published in: BMC Infectious Diseases | Issue 1/2016

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Abstract

Background

In intensive care unit (ICU), infection and colonization by resistant Gram-negative bacteria increase costs, length of stay and mortality. Extended-spectrum beta-lactamase − producing Enterobacteriaceae (ESBL-E) is a group of pathogens increasingly encountered in ICU setting. Conditions that promote ESBL-E acquisition are not completely understood. The increasing incidence of infections related to ESBL-E and the unsolved issues related to ESBL-E cross-transmission, prompted us to assess the rates of referred and acquired cases of ESBL-E in ICU and to assess patient-to-patient cross-transmission of ESBL-E using a multimodal microbiological analysis.

Methods

During a 5-month period, all patients admitted to a medical ICU were tested for ESBL-E carriage. A rectal swab was performed at admission and then twice a week until discharge or death. ESBL-E strains were analyzed according to antibiotic susceptibility pattern, rep-PCR (repetitive-element Polymerase chain reaction) chromosomal analysis, and plasmid PCR (Polymerase chain reaction) analysis of ESBL genes. Patient-to-patient transmission was deemed likely when 2 identical strains were found in 2 patients hospitalized simultaneously in the ICU.

Results

Among the 309 patients assessed for ESBL-E carriage on admission, 25 were found to carry ESBL-E (importation rate: 8 %). During follow-up, acquisition was observed among 19 of them (acquisition rate: 6.5 %). Using the multimodal microbiological approach, we found only one case of likely patient-to-patient ESBL-E transmission.

Conclusions

In unselected ICU patients, we found rather low rates of ESBL-E referred and acquired cases. Only 5 % of acquisitions appeared to be related to patient-to-patient transmission. These data highlight the importance of jointly analyzing phenotypic profile and molecular data to discriminate strains of ESBL-E.
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Literature
1.
go back to reference Tansarli GS, Karageorgopoulos DE, Kapaskelis A, Falagas ME. Impact of antimicrobial multidrug resistance on inpatient care cost: an evaluation of the evidence. Expert Review of Anti-Infective Therapy. 2013;11(3):321–31.CrossRefPubMed Tansarli GS, Karageorgopoulos DE, Kapaskelis A, Falagas ME. Impact of antimicrobial multidrug resistance on inpatient care cost: an evaluation of the evidence. Expert Review of Anti-Infective Therapy. 2013;11(3):321–31.CrossRefPubMed
2.
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
3.
go back to reference Conterno LO, Shymanski J, Ramotar K, Toye B, Zvonar R, Roth V. Impact and cost of infection control measures to reduce nosocomial transmission of extended-spectrum beta-lactamase-producing organisms in a non-outbreak setting. J Hosp Infect. 2007;65(4):354–60.CrossRefPubMed Conterno LO, Shymanski J, Ramotar K, Toye B, Zvonar R, Roth V. Impact and cost of infection control measures to reduce nosocomial transmission of extended-spectrum beta-lactamase-producing organisms in a non-outbreak setting. J Hosp Infect. 2007;65(4):354–60.CrossRefPubMed
4.
go back to reference Bradford PA. Extended-spectrum beta-lactamases in the 21st century: characterization, epidemiology, and detection of this important resistance threat. Clin Microbiol Rev. 2001;14(4):933–51.CrossRefPubMedPubMedCentral Bradford PA. Extended-spectrum beta-lactamases in the 21st century: characterization, epidemiology, and detection of this important resistance threat. Clin Microbiol Rev. 2001;14(4):933–51.CrossRefPubMedPubMedCentral
5.
go back to reference Brun-Buisson C, Legrand P, Philippon A, Montravers F, Ansquer M, Duval J. Transferable enzymatic resistance to third-generation cephalosporins during nosocomial outbreak of multiresistant Klebsiella pneumoniae. Lancet. 1987;2(8554):302–6.CrossRefPubMed Brun-Buisson C, Legrand P, Philippon A, Montravers F, Ansquer M, Duval J. Transferable enzymatic resistance to third-generation cephalosporins during nosocomial outbreak of multiresistant Klebsiella pneumoniae. Lancet. 1987;2(8554):302–6.CrossRefPubMed
6.
go back to reference Coque TM, Baquero F, Canton R. Increasing prevalence of ESBL-producing Enterobacteriaceae in Europe. Euro Surveill 2008 13(47):1-11. Coque TM, Baquero F, Canton R. Increasing prevalence of ESBL-producing Enterobacteriaceae in Europe. Euro Surveill 2008 13(47):1-11.
7.
go back to reference Woerther PL, Angebault C, Lescat M, Ruppe E, Skurnik D, Mniai AE, Clermont O, Jacquier H, Costa AD, Renard M et al. Emergence and dissemination of extended-spectrum beta-lactamase-producing Escherichia coli in the community: lessons from the study of a remote and controlled population. J Infect Dis. 2010;202(4):515–23.CrossRefPubMed Woerther PL, Angebault C, Lescat M, Ruppe E, Skurnik D, Mniai AE, Clermont O, Jacquier H, Costa AD, Renard M et al. Emergence and dissemination of extended-spectrum beta-lactamase-producing Escherichia coli in the community: lessons from the study of a remote and controlled population. J Infect Dis. 2010;202(4):515–23.CrossRefPubMed
8.
go back to reference Herindrainy P, Randrianirina F, Ratovoson R, Ratsima Hariniana E, Buisson Y, Genel N, Decre D, Arlet G, Talarmin A, Richard V. Rectal carriage of extended-spectrum beta-lactamase-producing gram-negative bacilli in community settings in Madagascar. PLoS One 2011 6(7): e1122738. Herindrainy P, Randrianirina F, Ratovoson R, Ratsima Hariniana E, Buisson Y, Genel N, Decre D, Arlet G, Talarmin A, Richard V. Rectal carriage of extended-spectrum beta-lactamase-producing gram-negative bacilli in community settings in Madagascar. PLoS One 2011 6(7): e1122738.
9.
go back to reference Valverde A, Coque TM, Sanchez-Moreno MP, Rollan A, Baquero F, Canton R. Dramatic increase in prevalence of fecal carriage of extended-spectrum beta-lactamase-producing Enterobacteriaceae during nonoutbreak situations in Spain. J Clin Microbiol. 2004;42(10):4769–75.CrossRefPubMedPubMedCentral Valverde A, Coque TM, Sanchez-Moreno MP, Rollan A, Baquero F, Canton R. Dramatic increase in prevalence of fecal carriage of extended-spectrum beta-lactamase-producing Enterobacteriaceae during nonoutbreak situations in Spain. J Clin Microbiol. 2004;42(10):4769–75.CrossRefPubMedPubMedCentral
10.
go back to reference Leflon-Guibout V, Blanco J, Amaqdouf K, Mora A, Guize L, Nicolas-Chanoine MH. Absence of CTX-M enzymes but high prevalence of clones, including clone ST131, among fecal Escherichia coli isolates from healthy subjects living in the area of Paris, France. J Clin Microbiol. 2008;46(12):3900–5.CrossRefPubMedPubMedCentral Leflon-Guibout V, Blanco J, Amaqdouf K, Mora A, Guize L, Nicolas-Chanoine MH. Absence of CTX-M enzymes but high prevalence of clones, including clone ST131, among fecal Escherichia coli isolates from healthy subjects living in the area of Paris, France. J Clin Microbiol. 2008;46(12):3900–5.CrossRefPubMedPubMedCentral
11.
go back to reference Ruppe E, Pitsch A, Tubach F, de Lastours V, Chau F, Pasquet B, et al. Clinical predictive values of extended-spectrum beta-lactamase carriage in patients admitted to medical wards. Eur J Clin Microbiol Infect Dis. 2012;31(3):319-25. Ruppe E, Pitsch A, Tubach F, de Lastours V, Chau F, Pasquet B, et al. Clinical predictive values of extended-spectrum beta-lactamase carriage in patients admitted to medical wards. Eur J Clin Microbiol Infect Dis. 2012;31(3):319-25.
12.
go back to reference Derde LP, Cooper BS, Goossens H, Malhotra-Kumar S, Willems RJ, Gniadkowski M, Hryniewicz W, Empel J, Dautzenberg MJ, Annane D 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 LP, Cooper BS, Goossens H, Malhotra-Kumar S, Willems RJ, Gniadkowski M, Hryniewicz W, Empel J, Dautzenberg MJ, Annane D 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
13.
go back to reference Jarlier V, Trystram D, Brun-Buisson C, Fournier S, Carbonne A, Marty L, Andremont A, Arlet G, Buu-Hoi A, Carlet J et al. Curbing methicillin-resistant Staphylococcus aureus in 38 French hospitals through a 15-year institutional control program. Arch Intern Med. 2010;170(6):552–9.CrossRefPubMed Jarlier V, Trystram D, Brun-Buisson C, Fournier S, Carbonne A, Marty L, Andremont A, Arlet G, Buu-Hoi A, Carlet J et al. Curbing methicillin-resistant Staphylococcus aureus in 38 French hospitals through a 15-year institutional control program. Arch Intern Med. 2010;170(6):552–9.CrossRefPubMed
14.
go back to reference Cooper BS, Stone SP, Kibbler CC, Cookson BD, Roberts JA, Medley GF, Duckworth G, Lai R, Ebrahim S. Isolation measures in the hospital management of methicillin resistant Staphylococcus aureus (MRSA): systematic review of the literature. BMJ. 2004;329(7465):533.CrossRefPubMedPubMedCentral Cooper BS, Stone SP, Kibbler CC, Cookson BD, Roberts JA, Medley GF, Duckworth G, Lai R, Ebrahim S. Isolation measures in the hospital management of methicillin resistant Staphylococcus aureus (MRSA): systematic review of the literature. BMJ. 2004;329(7465):533.CrossRefPubMedPubMedCentral
15.
go back to reference Lucet JC, Paoletti X, Lolom I, Paugam-Burtz C, Trouillet JL, Timsit JF, Deblangy C, Andremont A, Regnier B. Successful long-term program for controlling methicillin-resistant Staphylococcus aureus in intensive care units. Intensive Care Med. 2005;31(8):1051–7.CrossRefPubMed Lucet JC, Paoletti X, Lolom I, Paugam-Burtz C, Trouillet JL, Timsit JF, Deblangy C, Andremont A, Regnier B. Successful long-term program for controlling methicillin-resistant Staphylococcus aureus in intensive care units. Intensive Care Med. 2005;31(8):1051–7.CrossRefPubMed
16.
go back to reference Harris AD, Kotetishvili M, Shurland S, Johnson JA, Morris JG, Nemoy LL, Johnson JK. How important is patient-to-patient transmission in extended-spectrum beta-lactamase Escherichia coli acquisition. Am J Infect Control. 2007;35(2):97–101.CrossRefPubMed Harris AD, Kotetishvili M, Shurland S, Johnson JA, Morris JG, Nemoy LL, Johnson JK. How important is patient-to-patient transmission in extended-spectrum beta-lactamase Escherichia coli acquisition. Am J Infect Control. 2007;35(2):97–101.CrossRefPubMed
17.
go back to reference Harris AD, Perencevich EN, Johnson JK, Paterson DL, Morris JG, Strauss SM, Johnson JA. Patient-to-patient transmission is important in extended-spectrum beta-lactamase-producing Klebsiella pneumoniae acquisition. Clin Infect Dis. 2007;45(10):1347–50.CrossRefPubMed Harris AD, Perencevich EN, Johnson JK, Paterson DL, Morris JG, Strauss SM, Johnson JA. Patient-to-patient transmission is important in extended-spectrum beta-lactamase-producing Klebsiella pneumoniae acquisition. Clin Infect Dis. 2007;45(10):1347–50.CrossRefPubMed
18.
go back to reference Lee SO, Kim YS, Kim BN, Kim MN, Woo JH, Ryu J. Impact of previous use of antibiotics on development of resistance to extended-spectrum cephalosporins in patients with enterobacter bacteremia. Eur J Clin Microbiol Infect Dis. 2002;21(8):577–81.CrossRefPubMed Lee SO, Kim YS, Kim BN, Kim MN, Woo JH, Ryu J. Impact of previous use of antibiotics on development of resistance to extended-spectrum cephalosporins in patients with enterobacter bacteremia. Eur J Clin Microbiol Infect Dis. 2002;21(8):577–81.CrossRefPubMed
19.
go back to reference Overdevest I, Willemsen I, Rijnsburger M, Eustace A, Xu L, Hawkey P, Heck M, Savelkoul P, Vandenbroucke-Grauls C, van der Zwaluw K et al. Extended-spectrum beta-lactamase genes of Escherichia coli in chicken meat and humans, The Netherlands. Emerging Infectious Diseases. 2011;17(7):1216–22.CrossRefPubMedPubMedCentral Overdevest I, Willemsen I, Rijnsburger M, Eustace A, Xu L, Hawkey P, Heck M, Savelkoul P, Vandenbroucke-Grauls C, van der Zwaluw K et al. Extended-spectrum beta-lactamase genes of Escherichia coli in chicken meat and humans, The Netherlands. Emerging Infectious Diseases. 2011;17(7):1216–22.CrossRefPubMedPubMedCentral
20.
go back to reference Huang SS, Datta R, Platt R. Risk of acquiring antibiotic-resistant bacteria from prior room occupants. Arch Intern Med. 2006;166(18):1945–51.CrossRefPubMed Huang SS, Datta R, Platt R. Risk of acquiring antibiotic-resistant bacteria from prior room occupants. Arch Intern Med. 2006;166(18):1945–51.CrossRefPubMed
21.
go back to reference Kramer A, Schwebke I, Kampf G. How long do nosocomial pathogens persist on inanimate surfaces? A systematic review. BMC infectious diseases. 2006;6:130.CrossRefPubMedPubMedCentral Kramer A, Schwebke I, Kampf G. How long do nosocomial pathogens persist on inanimate surfaces? A systematic review. BMC infectious diseases. 2006;6:130.CrossRefPubMedPubMedCentral
22.
go back to reference Datta R, Platt R, Yokoe DS, Huang SS. Environmental cleaning intervention and risk of acquiring multidrug-resistant organisms from prior room occupants. Arch Intern Med. 2011;171(6):491–4.CrossRefPubMed Datta R, Platt R, Yokoe DS, Huang SS. Environmental cleaning intervention and risk of acquiring multidrug-resistant organisms from prior room occupants. Arch Intern Med. 2011;171(6):491–4.CrossRefPubMed
23.
go back to reference Harris AD, McGregor JC, Furuno JP. What infection control interventions should be undertaken to control multidrug-resistant gram-negative bacteria? Clin Infect Dis. 2006;43 Suppl 2:S57–61.CrossRefPubMed Harris AD, McGregor JC, Furuno JP. What infection control interventions should be undertaken to control multidrug-resistant gram-negative bacteria? Clin Infect Dis. 2006;43 Suppl 2:S57–61.CrossRefPubMed
24.
go back to reference Abad C, Fearday A, Safdar N. Adverse effects of isolation in hospitalised patients: a systematic review. J Hosp Infect. 2010;76(2):97–102.CrossRefPubMed Abad C, Fearday A, Safdar N. Adverse effects of isolation in hospitalised patients: a systematic review. J Hosp Infect. 2010;76(2):97–102.CrossRefPubMed
25.
go back to reference Jarlier V, Nicolas MH, Fournier G, Philippon A. Extended broad-spectrum beta-lactamases conferring transferable resistance to newer beta-lactam agents in Enterobacteriaceae: hospital prevalence and susceptibility patterns. Rev Infect Dis. 1988;10(4):867–78.CrossRefPubMed Jarlier V, Nicolas MH, Fournier G, Philippon A. Extended broad-spectrum beta-lactamases conferring transferable resistance to newer beta-lactam agents in Enterobacteriaceae: hospital prevalence and susceptibility patterns. Rev Infect Dis. 1988;10(4):867–78.CrossRefPubMed
26.
go back to reference Healy M, Huong J, Bittner T, Lising M, Frye S, Raza S, Schrock R, Manry J, Renwick A, Nieto R et al. Microbial DNA typing by automated repetitive-sequence-based PCR. J Clin Microbiol. 2005;43(1):199–207.CrossRefPubMedPubMedCentral Healy M, Huong J, Bittner T, Lising M, Frye S, Raza S, Schrock R, Manry J, Renwick A, Nieto R et al. Microbial DNA typing by automated repetitive-sequence-based PCR. J Clin Microbiol. 2005;43(1):199–207.CrossRefPubMedPubMedCentral
27.
go back to reference Pitout JD, Campbell L, Church DL, Wang PW, Guttman DS, Gregson DB. Using a commercial DiversiLab semiautomated repetitive sequence-based PCR typing technique for identification of Escherichia coli clone ST131 producing CTX-M-15. J Clin Microbiol. 2009;47(4):1212–5.CrossRefPubMedPubMedCentral Pitout JD, Campbell L, Church DL, Wang PW, Guttman DS, Gregson DB. Using a commercial DiversiLab semiautomated repetitive sequence-based PCR typing technique for identification of Escherichia coli clone ST131 producing CTX-M-15. J Clin Microbiol. 2009;47(4):1212–5.CrossRefPubMedPubMedCentral
28.
go back to reference Nemoy LL, Kotetishvili M, Tigno J, Keefer-Norris A, Harris AD, Perencevich EN, Johnson JA, Torpey D, Sulakvelidze A, Morris JG, Jr. et al. Multilocus sequence typing versus pulsed-field gel electrophoresis for characterization of extended-spectrum beta-lactamase-producing Escherichia coli isolates. J Clin Microbiol. 2005;43(4):1776–81.CrossRefPubMedPubMedCentral Nemoy LL, Kotetishvili M, Tigno J, Keefer-Norris A, Harris AD, Perencevich EN, Johnson JA, Torpey D, Sulakvelidze A, Morris JG, Jr. et al. Multilocus sequence typing versus pulsed-field gel electrophoresis for characterization of extended-spectrum beta-lactamase-producing Escherichia coli isolates. J Clin Microbiol. 2005;43(4):1776–81.CrossRefPubMedPubMedCentral
29.
go back to reference Dallenne C, Da Costa A, Decre D, Favier C, Arlet G. Development of a set of multiplex PCR assays for the detection of genes encoding important beta-lactamases in Enterobacteriaceae. The Journal of Antimicrobial Chemotherapy. 2010;65(3):490–5.CrossRefPubMed Dallenne C, Da Costa A, Decre D, Favier C, Arlet G. Development of a set of multiplex PCR assays for the detection of genes encoding important beta-lactamases in Enterobacteriaceae. The Journal of Antimicrobial Chemotherapy. 2010;65(3):490–5.CrossRefPubMed
30.
go back to reference Decre D, Gachot B, Lucet JC, Arlet G, Bergogne-Berezin E, Regnier B. Clinical and bacteriologic epidemiology of extended-spectrum beta-lactamase-producing strains of Klebsiella pneumoniae in a medical intensive care unit. Clin Infect Dis. 1998;27(4):834–44.CrossRefPubMed Decre D, Gachot B, Lucet JC, Arlet G, Bergogne-Berezin E, Regnier B. Clinical and bacteriologic epidemiology of extended-spectrum beta-lactamase-producing strains of Klebsiella pneumoniae in a medical intensive care unit. Clin Infect Dis. 1998;27(4):834–44.CrossRefPubMed
31.
go back to reference Buke C, Armand-Lefevre L, Lolom I, Guerinot W, Deblangy C, Ruimy R, Andremont A, Lucet JC. Epidemiology of multidrug-resistant bacteria in patients with long hospital stays. Infect Control Hosp Epidemiol. 2007;28(11):1255–60.CrossRefPubMed Buke C, Armand-Lefevre L, Lolom I, Guerinot W, Deblangy C, Ruimy R, Andremont A, Lucet JC. Epidemiology of multidrug-resistant bacteria in patients with long hospital stays. Infect Control Hosp Epidemiol. 2007;28(11):1255–60.CrossRefPubMed
32.
go back to reference Paniagua R, Valverde A, Coque TM, Baquero F, Canton R. Assessment of prevalence and changing epidemiology of extended-spectrum beta-lactamase-producing Enterobacteriaceae fecal carriers using a chromogenic medium. Diagn Microbiol Infect Dis. 2010;67(4):376–9.CrossRefPubMed Paniagua R, Valverde A, Coque TM, Baquero F, Canton R. Assessment of prevalence and changing epidemiology of extended-spectrum beta-lactamase-producing Enterobacteriaceae fecal carriers using a chromogenic medium. Diagn Microbiol Infect Dis. 2010;67(4):376–9.CrossRefPubMed
33.
go back to reference Laurent C, Rodriguez-Villalobos H, Rost F, Strale H, Vincent JL, Deplano A, Struelens MJ, Byl B. Intensive care unit outbreak of extended-spectrum beta-lactamase-producing Klebsiella pneumoniae controlled by cohorting patients and reinforcing infection control measures. Infect Control Hosp Epidemiol. 2008;29(6):517–24.CrossRefPubMed Laurent C, Rodriguez-Villalobos H, Rost F, Strale H, Vincent JL, Deplano A, Struelens MJ, Byl B. Intensive care unit outbreak of extended-spectrum beta-lactamase-producing Klebsiella pneumoniae controlled by cohorting patients and reinforcing infection control measures. Infect Control Hosp Epidemiol. 2008;29(6):517–24.CrossRefPubMed
34.
go back to reference Gardam MA, Burrows LL, Kus JV, Brunton J, Low DE, Conly JM, Humar A. Is surveillance for multidrug-resistant enterobacteriaceae an effective infection control strategy in the absence of an outbreak? J Infect Dis. 2002;186(12):1754–60.CrossRefPubMed Gardam MA, Burrows LL, Kus JV, Brunton J, Low DE, Conly JM, Humar A. Is surveillance for multidrug-resistant enterobacteriaceae an effective infection control strategy in the absence of an outbreak? J Infect Dis. 2002;186(12):1754–60.CrossRefPubMed
35.
go back to reference Lucet JC, Regnier B. [Enterobacteria producing extended spectrum beta-lactamases]. Pathol Biol (Paris). 1998;46(4):235–43. Lucet JC, Regnier B. [Enterobacteria producing extended spectrum beta-lactamases]. Pathol Biol (Paris). 1998;46(4):235–43.
36.
go back to reference D’Agata EM, Gautam S, Green WK, Tang YW. High rate of false-negative results of the rectal swab culture method in detection of gastrointestinal colonization with vancomycin-resistant enterococci. Clin Infect Dis. 2002;34(2):167–72.CrossRefPubMed D’Agata EM, Gautam S, Green WK, Tang YW. High rate of false-negative results of the rectal swab culture method in detection of gastrointestinal colonization with vancomycin-resistant enterococci. Clin Infect Dis. 2002;34(2):167–72.CrossRefPubMed
37.
go back to reference Harris AD, Nemoy L, Johnson JA, Martin-Carnahan A, Smith DL, Standiford H, Perencevich EN. Co-carriage rates of vancomycin-resistant Enterococcus and extended-spectrum beta-lactamase-producing bacteria among a cohort of intensive care unit patients: implications for an active surveillance program. Infect Control Hosp Epidemiol. 2004;25(2):105–8.CrossRefPubMed Harris AD, Nemoy L, Johnson JA, Martin-Carnahan A, Smith DL, Standiford H, Perencevich EN. Co-carriage rates of vancomycin-resistant Enterococcus and extended-spectrum beta-lactamase-producing bacteria among a cohort of intensive care unit patients: implications for an active surveillance program. Infect Control Hosp Epidemiol. 2004;25(2):105–8.CrossRefPubMed
38.
go back to reference Bird J, Browning R, Hobson RP, MacKenzie FM, Brand J, Gould IM. Multiply-resistant Klebsiella pneumoniae: failure of spread in community-based elderly care facilities. J Hosp Infect. 1998;40(3):243–7.CrossRefPubMed Bird J, Browning R, Hobson RP, MacKenzie FM, Brand J, Gould IM. Multiply-resistant Klebsiella pneumoniae: failure of spread in community-based elderly care facilities. J Hosp Infect. 1998;40(3):243–7.CrossRefPubMed
39.
go back to reference Haverkate MR, Derde LP, Brun-Buisson C, Bonten MJ, Bootsma MC. Duration of colonization with antimicrobial-resistant bacteria after ICU discharge. Intensive Care Med. 2014;40(4):564–71.CrossRefPubMedPubMedCentral Haverkate MR, Derde LP, Brun-Buisson C, Bonten MJ, Bootsma MC. Duration of colonization with antimicrobial-resistant bacteria after ICU discharge. Intensive Care Med. 2014;40(4):564–71.CrossRefPubMedPubMedCentral
Metadata
Title
Extended-spectrum beta-lactamase − producing enterobacteriaceae in the intensive care unit: acquisition does not mean cross-transmission
Authors
Mikael Alves
Astrid Lemire
Dominique Decré
Dimitri Margetis
Naïke Bigé
Claire Pichereau
Hafid Ait-Oufella
Jean-Luc Baudel
Georges Offenstadt
Bertrand Guidet
Frédéric Barbut
Eric Maury
Publication date
01-12-2016
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2016
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-016-1489-z

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