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Prospective Evaluation of Colonization with Extended-Spectrum β-Lactamase (ESBL)–Producing Enterobacteriaceae Among Patients at Hospital Admission and of Subsequent Colonization with ESBL-Producing Enterobacteriaceae Among Patients During Hospitalization

  • Reuven Friedmann (a1), David Raveh (a2), Esther Zartzer (a1) (a2), Bernard Rudensky (a3), Ellen Broide (a3), Denise Attias (a3) and Amos M. Yinnon (a2)...



To determine the rates of and risk factors for carriage and acquisition of extended-spectrum (β-lactamase (ESBL)-producing Enterobacteriaceae during hospitalization.


Cohort study.


Shaare Zedek Medical Center, a 550-bed teaching hospital.


During a 5-month period (February 1-June 30, 2004), 167 (8%) of 1,985 newly admitted general medical patients were enrolled in our study. Nasal, oropharyngeal, and rectal swab specimens were obtained at admission and every 2-3 days until hospital discharge or death. Enterobacteriaceae isolates were tested for ESBL, and Staphylococcus aureus isolates were tested for methicillin resistance.


Of the 167 patients enrolled in our study, 15 (9%) were identified as nasal carriers of methicillin-resistant S. aureus (MRSA) at admission, and 13 (8%) were rectal carriers of ESBL-producing Enterobacteriaceae at admission. Univariate risk factors for rectal carriage of ESBL-producing Enterobacteriaceae included female sex (odds ratio [OR], 11 [95% confidence interval {CI}, 1.4—238]; P < .05), nursing home residence (OR, 6.9 [95% CI, 1.8-27]; P < .01), recent antibiotic treatment (OR, 9.8 [95% CI, 1.7-74]; P < .05), and concomitant nasal carriage of MRSA and/or ESBL-producing Enterobacteriaceae (OR, 5.8 [95% CI, 1.2-26]; P < .01). Multivariate risk factors were female sex and recent antibiotic treatment. During hospitalization, 35 (21%) of 167 patients had acquired rectal carriage of ESBL-producing Enterobacteriaceae (P = .002, for trend analysis). Of the 12 patients who were still in the hospital 2 weeks after admission, 4 (33%) were carriers of ESBL-producing Enterobacteriaceae. Univariate risk factors for acquisition included an age of older than 65 years (P < .005), nursing home residence (OR 2.6, [95% CI, 0.98-2.6]), impaired cognition (OR, 4.8 [95% CI, 1.9-12]), recent antibiotic treatment (OR, 2.7 [95% CI, 0.9-8.3]), respiratory assistance (OR, 4.2 [95% CI, 1.2-14]), and prolonged hospitalization. Multivariate risk factors were an age of older than 65 years and broad-spectrum antibiotic therapy.


Rectal carriage of ESBL-producing Enterobacteriaceae occurred in 13 (8%) of 167 patients at admission to the medical departments of our hospital and in 4 (33%) of 12 patients still remaining in our hospital after 2 weeks.


Corresponding author

Division of Medicine, Shaare Zedek Medical Center, P.O. Box 3235, Jerusalem 91031, Israel(


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1.Livermore, DM. Bacterial resistance: origins, epidemiology, and impact. Clin Infect Dis 2003;36(Suppl 1):S11S23.
2.Paterson, DL, Bonomo, RA. Extended-spectrum β-lactamases: a clinical update. Clin Microbiol Rev 2005;18:657686.
3.Livermore, DM. Defining an extended-spectrum β-lactamase. Clin Microbiol Infect 2008;14 (Suppl 1):310.
4.Cohen, MJ, Anshilevitz, O, Raveh, D, Broide, E, Rudensky, B, Yinnon, AM. Colonization and acquisition of multi-drug resistant organisms among hospital patient neighboring the critically ill. Infect Control Hosp Epidemiol 2006;27:675681.
5.Tallis, E, Rudensky, B, Attias, D, Raveh, D, Schlesinger, Y, Yinnon, AM. Invitto activity of cefepime and other broad-spectrum antimicrobials against several groups of gram—negative bacilli and Staphylococcus aureus. Diagn Microbiol Infect Dis 1999;35:121126.
6.Nicolas-Chanoine, MH, Jarlier, V; La Collégiale de Bactériologie-Virologie-Hygiène Hospitalière de l’Assistance Publique, Hôpitaux de Paris, France. Extended-spectrum β-lactamases in long-term-care facilities. Clin Microbiol Infect 2008;14 (Suppl 1):111116.
7.Pitout, JDD, Laupland, KB. Extended-spectrum β-lactamase-producing Enterobacteriaceae: an emerging public-health concern. Lancet Infect Dis 2008;8:159166.
8.Rodríguez-Baño, J, Navarro, MD. Extended-spectrum β-lactamases in ambulatory care: a clinical perspective. Clin Microbiol Infect 2008;14 (Suppl 1):104110.
9.Moor, CT, Roberts, SA, Simmons, G, et al.Extended-spectrum β-lactamase (ESBL)-producing Enterobacteria: factors associated with infection in the community setting, Auckland, New Zealand. J Hosp Infect 2008;68:355362.
10.Adler, A, Raveh, D, Rudensky, B, Yinnon, AM, Benenson, S. Enteric gram-negative bacteremia at the emergency department: risk factors for extended-spectrum β-lactamase and outcome. Infect Dis Clin Pract 2008;16:109112.
11.Doi, Y, Adams, J, O'Keefe, A, Quereshi, Z, Ewan, L, Paterson, DL. Community-acquired extended-spectrum β-lactamase producers, United States. Emerg Infect Dis 2007;13:1121.
12.Colodner, R, Rock, W, Chazan, B, et al.Risk factors for the development of extended-spectrum β-lactamase-producing bacteria in non-hospitalised patients. Eur J Clin Microbiol Infect Dis 2004;23:163167.
13.Borer, A, Gilad, J, Mensahe, G, Peled, N, Riesenberg, K, Schlaeffer, F. Extended-spectrum β-lactamase-producing Enterobacteriaceae strains in community-acquired bacteremia in southern Israel. Med Sci Monit 2002;8:CR4447.
14.Raveh, D, Gratch, L, Yinnon, AM, Sonnenblick, M. Demographic and clinical characteristics of patients admitted to medical departments. J Eval Clin Pract 2005;11:3344.
15.Sonnenblick, M, Raveh, D, Gratch, L, Yinnon, AM. Clinical and demographic characteristics of elderly patients hospitalised in an internal medicine department in Israel. Int J Clin Pract 2007;61:247254.
16.Benenson, S, Yinnon, AM, Schlesinger, Y, Rudensky, B, Raveh, D. Optimization of empirical antibiotic selection for suspected Gram-negative bacteraemia in the emergency department. Int J Antimicrob Agents 2005;25:398403.
17.Raveh, D, Rudensky, D, Schlesinger, Y, Attias, D, Yinnon, AM. Trends in bacteremias: analysis of 7544 patient-specific bacteremic episodes spanning 11 years (1990-2000). J Hosp Infect 2003;55:196203.
18.Raveh, D, Rudensky, B, Huerta, M, Aviv, Y, Yinnon, AM. An improved, evidence-based method for empirical treatment of urinary tract infection. Eur J Clin Microbiol Infect Dis 2003;22:158164.
19.Jerassy, Z, Yinnon, AM, Mazouz-Cohen, S, et al.Prospective hospital-wide studies of 505 patients with nosocomial bacteraemia in 1997 and 2002. J Hosp Infect 2006;62:230236.
20.Friedmann, R, Hamburger, R, Shulman, C, Yinnon, AM, Raveh, D. Antimicrobial susceptibilities of urinary pathogens in a multidisciplinary long-term care facility. Diagn Microbiol Infect Dis 2003;46:217222.
21.Henshke, R, Yinnon, AM, Rudensky, B, Attias, D, Raveh, D. Assessment of the clinical significance of production of extended-spectrum-β-lac-tamase (ESBL) by Enterobacteriaceae. Infection 2006;34:6674.
22.Raveh, D, Muallem-Zilca, E, Greenberg, A, Wiener-Well, Y, Yinnon, AM. Two-phase drug utilization evaluation of cefepime, piperacillin-tazobactam and meropenem. QJM 2006;99:397406.
23.Drori-Zeides, T, Raveh, D, Schlesinger, Y, Yinnon, AM. Practical guidelines for vancomycin usage, with prospective drug utilization evaluation. Infect Control Hosp Epidemiol 2000;21:4547.
24.Raveh, D, Levy, Y, Schlesinger, Y, Greenberg, A, Rudensky, B, Yinnon, AM. Longitudinal surveillance of antibiotic use in the hospital. QJM 2001;94:141152.
25.CLSI (formerly NCCLS). Performance standards for antimicrobial susceptibility testing: 16th informational supplement. CLSI document. Wayne, PA: CLSI, 2006.
26.Carter, MW, Oakton, KJ, Warner, M, Livermore, DM. Detection of extended-spectrum β-lactamases in klebsiellae with the Oxoid combination disc method. J Clin Microbiol 2000;38:42284232.
27.Wertheim, HF, Melles, DC, Vos, MC, et al.The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis 2005;5:751762.
28.Schlesinger, Y, Yahalom, S, Raveh, D, et al.Methicillin-resistant Staphylococcus aureus nasal colonization in children in Jerusalem: community vs. chronic care institutions. Isr Med Assoc J 2003;5:847851.
29.Valverde, A, Coque, TM, Sánchez-Moreno, MP, Rollan, A, Baquero, F, Canton, R. Dramatic increase in prevalence of fecal carriage of extended-spectrum β-lactamase-producing Enterobacteriaceae during non-outbreak situations in Spain. J Clin Microbiol 2004;42:47694775.
30.Buke, C, Armand-Lefevre, L, Lolom, I, et al.Epidemiology of multidrug-resistant bacteria in patients with long hospital stay. Infect Control Hosp Epidemiol 2007;28:12551260.
31.Martins, IS, Pessoa-Silva, CL, Nouer, SA, et al.Endemie extended-spectrum β-lactamase-producing Klebsiella pneumoniae at an intensive care unit: risk factors for colonization and infection. Microb Drug Resist 2006;12:5058.
32.Troché, F, Joly, LM, Guibert, M, Zazzo, JF. Detection and treatment of antibiotic-resistant bacterial carriage in a surgical intensive care unit: a 6-year prospective study. Infect Control Hosp Epidemiol 2005;26:161165.
33.Esposito, S, Capuano, A, Noviello, S, et al.Modification of patients' endogenous bacterial flora during hospitalization in a large teaching hospital in Naples. J Chemother 2003;15:568573.
34.Peña, C, Pujol, M, Ricart, A, et al.Risk factors for faecal carriage of Klebsiella pneumoniae producing extended spectrum β-lactamase (ESBL-KP) in the intensive care unit. J Hosp Infect 1997;35:916.
35.Tumbarello, M, Sanguinetti, M, Montuori, E, et al.Predictors of mortality in blood stream infections caused by extended-spectrum β-lactamase-producing Enterobacteriaceae: importance of inadequate antimicrobial treatment. Antimicrob Agents Chemother 2007;51:19871994.
36.Lautenbach, E, Patel, JB, Bilker, WB, Edelstein, PH, Fishman, NO. Extended-spectrum β-lactamase-producing Escherichia coli and Klebsiella pneumoniae, risk factors for infection and impact of resistance on outcomes. Clin Infect Dis 2001;32:11621171.
37.Paterson, DL, Ko, WC, Gottberg, AV, et al.Outcome of cephalosporin treatment for serious infections due to apparently susceptible organisms producing extended-spectrum β-lactamases: implications for the clinical microbiology laboratory. J Clin Microbiol 2001;39:22062212.
38.Menashe, G, Borer, A, Yagupsky, P, et al.Clinical significance and impact on mortality of extended-spectrum β lactamase-producing Enterobacteriaceae isolates in nosocomial bacteremia. Scand J Infect Dis 2001;33:188193.
39.Warren, RE, Harvey, G, Carr, R, Ward, D, Doroshenko, A. Control of infections due to extended-spectrum β-lactamase-producing organisms in hospitals and the community. Clin Microbiol Infect 2008;14(Suppl 1): 124133.
40.Reddy, P, Malczynski, M, Obias, A, et al.Screening for extended-spectrum β-lactamase-producing Enterobacteriaceae among high-risk patients and rates of subsequent bacteremia. Clin Infect Dis 2007;45:846852.

Prospective Evaluation of Colonization with Extended-Spectrum β-Lactamase (ESBL)–Producing Enterobacteriaceae Among Patients at Hospital Admission and of Subsequent Colonization with ESBL-Producing Enterobacteriaceae Among Patients During Hospitalization

  • Reuven Friedmann (a1), David Raveh (a2), Esther Zartzer (a1) (a2), Bernard Rudensky (a3), Ellen Broide (a3), Denise Attias (a3) and Amos M. Yinnon (a2)...


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