Skip to main content Accessibility help

Extended-Spectrum β-Lactamase–Producing Escherichia coli and Klebsiella Species: Risk Factors for Colonization and Impact of Antimicrobial Formulary Interventions on Colonization Prevalence

  • Gregory Bisson (a1), Neil O. Fishman (a1), Jean Baldus Patel (a2), Paul H. Edelstein (a2) and Ebbing Lautenbach (a1) (a3)...



The incidence of extended-spectrum β-lactamase (ESβL)–mediated resistance has increased markedly during the past decade. Risk factors for colonization with ESβL-producing Escherichia coli and Klebsiella species (ESβL-EK) remain unclear, as do methods to control their further emergence.


Case–control study.


Two hospitals within a large academic health system: a 725-bed academic tertiary-care medical center and a 344-bed urban community hospital.


Thirteen patients with ESβL-EK fecal colonization were compared with 46 randomly selected noncolonized controls.


Duration of hospitalization was the only independent risk factor for ESβL-EK colonization (odds ratio, 1.11; 95% confidence interval, 1.02 to 1.21). Of note, 8 (62%) of the patients had been admitted from another healthcare facility. In addition, there was evidence for dissemination of a single K. oxytoca clone. Finally, the prevalence of ESβL-EK colonization decreased from 7.9% to 5.7% following restriction of third-generation cephalosporins (P = .51).


ESβL-EK colonization was associated only with duration of hospitalization and there was no significant reduction following antimicrobial formulary interventions. The evidence for nosocomial spread and the high percentage of patients with ESβL-EK admitted from other sites suggest that greater emphasis must be placed on controlling the spread of such organisms within and between institutions.


Corresponding author

University of Pennsylvania School of Medicine, Center for Clinical Epidemiology and Biostatistics, 825 Blockley Hall, 423 Guardian Drive, Philadelphia, PA 19104-6021


Hide All
1.Jacoby, GA. Extended-spectrum β-lactamases and other enzymes providing resistance to oxyimino-β-lactams. Infect Dis Clin North Am 1997;11:875887.
2.Jacobson, KL, Cohen, SH, Inciardi, JF, et al. The relationship between antecedent antibiotic use and resistance to extended-spectrum cephalosporins in group I B-lactamase-producing organisms. Clin Infect Dis 1995;21:11071113.
3.Rice, LB, Eckstein, EC, DeVente, J, et al. Ceftazidime-resistant Klebsiella pneumoniae isolates recovered at the Cleveland Department of Veterans Affairs Medical Center. Clin Infect Dis 1996;23:118124.
4.Schiappa, DA, Hayden, MK, Matushek, MG, et al. Ceftazidime-resistant Klebsiella pneumoniae and Escherichia coli bloodstream infection: a case-control and molecular epidemiologic investigation. J Infect Dis 1996;174:529536.
5.Knothe, H, Shah, P, Kremery, V, et al. Transferable resistance to cefotaxime, cefoxitin, cefamandole and cefuroxime in clinical isolates of Klebsiella pneumoniae and Serratia marcescens. Infection 1983;11:315317.
6.Sirot, D, Sirot, J, Labia, R, et al. Transferable resistance to third-generation cephalosporins in clinical isolates of Klebsiella pneumoniae: identification of CTX-1, a novel B-lactamase. J Antimicrob Chemother 1987;20:323334.
7.Brun-Buisson, C, Legrand, P, Phillippon, A, et al. Transferable enzymatic resistance to third-generation cephalosporins during nosocomial outbreak of multiresistant Klebsiella pneumoniae. Lancet 1987;2:302306.
8.Rice, LB, Willey, SH, Papanicolaou, GA, et al. Outbreak of ceftazidime resistance caused by extended-spectrum B-lactamases at a Massachusetts chronic-care facility. Antimicrob Agents Chemother 1990;34:22002209.
9.Meyer, KS, Urban, C, Eagen, JA, et al. Nosocomial outbreak of Klebsiella infection resistant to late-generation cephalosporins. Ann Intern Med 1993;119:353358.
10.Itokazu, GS, Quinn, JP, Bell-Dixon, C, et al. Antimicrobial resistance rates among aerobic gram-negative bacilli recovered from patients in intensive care units: evaluation of a national postmarketing surveillance program. Clin Infect Dis 1996;23:779784.
11.Lautenbach, E, Patel, JB, Bilker, WB, et al. Extended-spectrum B-lactamase-producing Escherichia coli and Klebsiella pneumoniae: risk factors for infection and impact of resistance on outcomes. Clin Infect Dis 2001;15:11621171.
12.Paterson, DL, Ko, WC, Mohapatra, S, et al. Klebsiella pneumoniae bacteremia: impact of extended-spectrum B-lactamase (ESBL) production in a global study of 216 patients. Presented at the annual meeting of the Interscience Conference on Antimicrobial Agents and Chemotherapy; September 28-October 1, 1997; Toronto, Ontario, Canada.
13.Wiener, J, Quinn, JP, Bradford, PA, et al. Multiple antibiotic-resistant Klebsiella and Escherichia coli in nursing homes. JAMA 1999;281:517523.
14.Lucet, JC, Chevret, S, Decre, D, et al. Outbreak of multiply resistant enterobacteriaceae in an intensive care unit: epidemiology and risk factors for acquisition. Clin Infect Dis 1996;22:430436.
15.Knaus, WA, Drapier, EA, Wagner, DP, et al. APACHE II: a severity of disease classification system. Crit Care Med 1985;13:818829.
16.National Committee for Clinical Laboratory Standards (NCCLS). Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically, 5th ed. Approved standard. M7-A5. Wayne, PA: National Committee for Clinical Laboratory Standards; 2000.
17.Thomson, KS, Sanders, CC. Detection of extended-spectrum beta-lacta-mases in members of the family enterobacteriaceae: comparison of the double-disk and three-dimensional tests. J Clin Microbiol 1992;36:18771882.
18.Livermore, DM, Williams, JD. B-lactams: mode of action and mechanisms of bacterial resistance. In: Lorian, V, ed. Antibiotics in Laboratory Medicine, 4th ed. Baltimore, MD: Williams and Wilkins; 1996.
19.Gautom, RK. Rapid pulsed-field gel electrophoresis protocol for typing of Escherichia coli 0157:H7 and other gram-negative organisms in 1 day. J Clin Microbiol 1997;35:29772980.
20.Kleinbaum, DG, Kupper, LL, Morgenstern, H. Epidemiologic Research: Principles and Quantitative Methods. New York: Van Nostrand Reinhold; 1982.
21.Mantel, N, Haenszel, W. Statistical aspects of the analysis of data from retrospective studies of disease. J Natl Cancer Inst 1959;22:719748.
22.Hosmer, DW, Lemeshow, S. Applied Logistic Regression. New York: John Wiley & Sons; 1989.
23.Piroth, L, Aube, H, Doise, JM, et al. Spread of extended-spectrum β-lactamase-producing Klebsiella pneumoniae: are β-lactamase inhibitors of therapeutic value? Clin Infect Dis 1998;27:7680.
24.Pena, C, Pujol, M, Ardanuy, C, et al. Epidemiology and successful control of a large outbreak due to Klebsiella pneumoniae producing extended-spectrum β-lactamases. Antimicrob Agents Chemother 1998;42:5358.
25.DeChamps, C, Sauvant, MP, Chanal, C, et al. Prospective survey of colonization of infection caused by expanded-spectrum B-lactamase-producing members of the family enterobacteriaceae in an intensive care unit. J Clin Microbiol 1989;27:28872890.
26.Pena, 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.
27.Deere, D, Gachot, B, Lucet, JC, et al. Clinical and bactériologie epidemiology of extended-spectrum B-lactamase-producing strains of Klebsiella pneumoniae in a medical intensive care unit. Clin Infect Dis 1998;27:834844.
28.Casewell, M, Philipps, I. Hands as route of transmission for Klebsiella species. Br Med J 1977;2:13151317.
29.D'Agata, E, Venkataraman, L, DeGirolami, P, et al. The molecular and clinical epidemiology of enterobacteriaceae producing extended-spectrum β-lactamase in a tertiary care hospital. J Hosp Infect 1998;36:279285.
30.Lucet, JC, Fichelle, A, Decre, D, et al. Control of a prolonged outbreak of extended-spectrum B-lactamase-producing Enterobacteriaceae in a university hospital. Presented at the American Society for Microbiology 36th Annual Interscience Conference on Antimicrobial Agents and Chemotherapy; September 15-18, 1996; New Orleans, LA. Abstract no. J108.

Related content

Powered by UNSILO

Extended-Spectrum β-Lactamase–Producing Escherichia coli and Klebsiella Species: Risk Factors for Colonization and Impact of Antimicrobial Formulary Interventions on Colonization Prevalence

  • Gregory Bisson (a1), Neil O. Fishman (a1), Jean Baldus Patel (a2), Paul H. Edelstein (a2) and Ebbing Lautenbach (a1) (a3)...


Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed.