Skip to main content Accessibility help
×
Home

Gastrointestinal Tract Colonization With Fluoroquinolone-Resistant Escherichia coli in Hospitalized Patients: Changes Over Time in Risk Factors for Resistance

  • Ebbing Lautenbach (a1) (a2) (a3) (a4), Joshua P. Metlay (a5) (a2) (a3) (a4) (a6), Mark G. Weiner (a5) (a4), Warren B. Bilker (a2) (a3) (a4), Pam Tolomeo (a3), Xiangqun Mao (a7), Irving Nachamkin (a7) (a4) and Neil O. Fishman (a1) (a4)...

Abstract

Objective.

The prevalence of fluoroquinolone (FQ) resistance in Escherichia coli has increased markedly in recent years. Despite the important role of gastrointestinal tract colonization with FQ-resistant E. coli (FQREC), the prevalence of and risk factors for FQREC colonization among the general hospitalized patient population have not been described, to our knowledge. The objective of this study was to identify the prevalence of and risk factors for FQREC colonization among hospitalized patients.

Design.

Three-year case-control study. Case patients (ie, all subjects with FQREC colonization) were compared with control patients (ie, all subjects without FQREC colonization).

Setting.

Two large medical centers within an academic health system.

Participants.

All patients hospitalized at the 2 study hospitals.

Main Outcome Measure.

Three annual fecal surveillance surveys were conducted. All patients colonized with FQREC (levofloxacin minimum inhibitory concentration, ≥ 8 μg/mL) were identified.

Results.

Of the 774 subjects, 89 (11.5%) were colonized with FQREC. Although there was a significant association between prior FQ use and FQREC colonization on bivariable analysis (odds ratio [OR], 2.02 [95% confidence interval {CI}, 1.14–3.46]; P = .01), there was statistically significant effect modification by year of study (P = .005). In multivariable analyses, after controlling for the hospital and for the duration of hospitalization prior to sampling, the association between FQ use and FQREC colonization was as follows: adjusted OR (aOR), 0.97 (95% CI, 0.29–3.23) in 2002; aOR, 1.41 (95% CI, 0.57–3.50) in 2003; and aOR, 9.87 (95% CI, 3.67–26.55) in 2004.

Conclusions.

The association between prior FQ use and FQREC colonization varied significantly by study year, suggesting that the clinical epidemiology of resistant organisms may change over time. Furthermore, in the context of recent work showing significant changes in FQREC prevalence as well as changes in FQ resistance mechanisms (specifically, efflux overexpression) over the same time period, these results suggest a previously unrecognized complexity in the relationship between the clinical and molecular epidemiology of FQ resistance.

Copyright

Corresponding author

University of Pennsylvania School of Medicine, Center for Clinical Epidemiology and Biostatistics, 825 Blockley Hall, 423 Guardian Drive, Philadelphia, PA 19104-6021 (ebbing@mail.med.upenn.edu)

References

Hide All
1.Hooper, DC. New uses for new and old quinolones and the challenge of resistance. Clin Infect Dis 2000;30:243254.
2.Lee, YL, Cesario, T, McCauley, V, Flionis, L, Pax, A, Thrupp, L. Low-level colonization and infection with ciprofloxacin-resistant gram-negative bacilli in a skilled nursing facility. Am J Infect Control 1998;26:552557.
3.Linder, JA, Huang, ES, Steinman, MA, Gonzales, R, Stafford, RS. Fluoroquinolone prescribing in the United States: 1995 to 2002. Am J Med 2005;118:259268.
4.Lautenbach, E, Strom, BL, Nachamkin, I, et al. Longitudinal trends in fluoroquinolone resistance among Enterobacteriaceae isolates from inpatients and outpatients (1989-2000): differences in the emergence and epidemiology of resistance across organisms. Clin Infect Dis 2004;38:655662.
5.Neuhauser, MM, Weinstein, RA, Rydman, R, Danziger, LH, Karam, G, Quinn, JP. Antibiotic resistance among gram-negative bacilli in US intensive care units. JAMA 2003;289:885888.
6.Lautenbach, E, Metlay, JP, Bilker, WB, Edelstein, PH, Fishman, NO. Association between fluoroquinolone resistance and mortality in Escherichia coli and Klebsiella pneumoniae infections: role of inadequate empiric antimicrobial therapy. Clin Infect Dis 2005;41:923929.
7.Lautenbach, E, Strom, BL, Bilker, WB, Patel, JB, Edelstein, PH, Fishman, NO. Epidemiological investigation of fluoroquinolone resistance in infections due to extended-spectrum β-lactamase-producing Escherichia coli and Klebsiella pneumoniae. Clin Infect Dis 2001;33:12881294.
8.Paterson, DL, Mulazimoglu, L, Casellas, JM, et al. Epidemiology of ciprofloxacin resistance and its relationship to extended-spectrum β-lactamase production in Klebsiella pneumoniae isolates causing bacteremia. Clin Infect Dis 2000;30:473478.
9.Bettelheim, KA. The genus Escherichia. In: Balows, A, Truper, HG, Dworkin, M, Harder, W, Schleifer, KH, eds. The Prokaryotes: a handbook on the biology of bacteria: ecophysiology, isolates, identification, applications. New York: Springer-Verlag; 1991.
10.Janda, JM, Abbott, SL. The Enterobacteria. Philadelphia: Lippincott-Raven;1998.
11.Arbeit, RD, Arthur, M, Dunn, R, Kim, C, Selander, RK, Goldstein, R. Resolution of recent evolutionary divergence among Escherichia coli from related lineages: the application of pulsed field electrophoresis to molecular epidemiology. J Infect Dis 1990;161:230235.
12.Brumfitt, W. Progress in understanding urinary infections. J Antimicrob Chemother 1991;27:922.
13.Oethinger, M, Jellen-Ritter, AS, Conrad, S, Marre, R, Kern, WV. Colonization and infection with fluoroquinolone-resistant Escherichia coli among cancer patients: clonal analysis. Infection 1998;26:379384.
14.Lautenbach, E, Fishman, NO, Metlay, JP, et al. Phenotypic and genotypic characterization of fecal Escherichia coli isolates with decreased susceptibility to fluoroquinolones: results from a large hospital-based surveillance initiative. J Infect Dis 2006;194:7985.
15.Maslow, JN, Lee, B, Lautenbach, E. Fluoroquinolone-resistant Escherichia coli carriage in long-term care facility. Emerg Infect Dis 2005;11:889894.
16.Baum, HV, Franz, U, Geiss, HK. Prevalence of ciprofloxacin-resistant Escherichia coli in hematologic-oncologic patients. Infection 2000;28:278281.
17.Richard, P, Delangle, MH, Raffi, F, Espaze, E, Richet, H. Impact of fluoroquinolone administration on the emergence of fluoroquinolone-resistant gram-negative bacilli from gastrointestinal flora. Clin Infect Dis 2001;32:162166.
18.Aparicio, JR, Such, J, Pascual, S, et al. Development of quinolone-resistant strains of Escherichia coli in stools of patients with cirrhosis undergoing norfloxacin prophylaxis: clinical consequences. J Hepatol 1999;31:277283.
19.Zaidi, MB, Zamora, E, Diaz, P, Tollefson, L, Fedorka-Cray, PJ, Headrick, ML. Risk factors for fecal quinolone-resistant Escherichia coli in Mexican children. Antimicrob Agents Chemother 2003;47:19992001.
20.Lautenbach, E, Harris, AD, Perencevich, EN, Nachamkin, I, Tolomeo, P, Metlay, JP. Test characteristics of perirectal and rectal swab compared to stool sample for detection of fluoroquinolone-resistant Escherichia coli in the gastrointestinal tract. Antimicrob Agents Chemother 2005;49:798800.
21.Clinical and Laboratory Standards Institute (CLSI). Performance Standards for Antimicrobial Susceptibility Testing: 16th informational supplement. Wayne, PA: CLSI; 2006:M100-S16.
22.Barton, TD, Fishman, NO, Weiner, MG, LaRosa, LA, Lautenbach, E. High rate of coadministration of di- or tri-valent cation-containing compounds with oral fluoroquinolones: risk factors and potential implications. Infect Control Hosp Epidemiol 2005;26:9399.
23.Quain, RD, Barton, TD, Fishman, NO, Weiner, MG, Lautenbach, E. Coadministration of oral levofloxacin with agents that impair its absorption: potential impact on emergence of resistance. Int J Antimicrob Agents 2005;26:327330.
24.Gasink, LB, Fishman, NO, Weiner, MG, Nachamkin, I, Bilker, WB, Lautenbach, E. Fluoroquinolone-resistant Pseudomonas aeruginosa: assessment of risk factors and clinical impact. Am J Med 2006;199:526.e19-25.
25.MacAdam, H, Zaoutis, TE, Gasink, LB, Bilker, WB, Lautenbach, E. Investigating the association between antibiotic use and antibiotic resistance: impact of different methods of categorizing prior antibiotic use. Int J Antimicrob Agents 2006;28:325332.
26.Deyo, RA, Cherkin, DC, Ciol, MA. Adapting a clinical comorbidity index for use with ICD-9-CM administrative databases. J Clin Epidemiol 1992;45:613619.
27.Kleinbaum, DG, Kupper, LL, Morgenstern, H. Epidemiologic research: principles and quantitative methods. New York: Van Nostrand Reinhold; 1982.
28.Mantel, N, Haenszel, W. Statistical aspects of the analysis of data from retrospective studies of disease. J Natl Cancer Inst 1959;22:719748.
29.Hosmer, DO, Lemeshow, SL. Applied logistic regression. New York: Wiley and Sons; 1989.
30.Sun, GW, Shook, TL, Kay, GL. Inappropriate use of bivariable analysis to screen risk factors for use in multivariable analysis. J Clin Epidemiol 1996;49:907916.
31.Mickey, RM, Greenland, S. The impact of confounder selection criteria on effect estimation. Am J Epidemiol 1989;129:125137.
32.Jacoby, GA. Mechanisms of resistance to quinolones. Clin Infect Dis 2005;41(Suppl 2):S120S126.
33.Hooper, DC. Emerging mechanisms of fluoroquinolone resistance. Emerg Infect Dis 2001;7:337341.
34.Wang, H, Dzink-Fox, JL, Chen, M, Levy, SB. Genetic characterization of highly fluoroquinolone-resistant clinical Escherichia coli strains from China: role of acrR mutations. Antimicrob Agents Chemother 2001;45:15151521.
35.White, DG, Goldman, JD, Demple, B, Levy, SB. Role of the acrAB locus in organic solvent tolerance mediated by expression of marA, soxS, or robA in Escherichia coli. J Bacteriol 1997;179:61226126.
36.Lautenbach, E, Fishman, NO, Bilker, WB, et al. Risk factors for fluoroquinolone resistance in nosocomial Escherichia coli and Klebsiella pneumoniae infections. Arch Intern Med 2002;162:24692477.
37.Lautenbach, E, Larosa, LA, Kasbekar, N, Peng, HP, Maniglia, RJ, Fishman, NO. Fluoroquinolone utilization in the emergency departments of academic medical centers: prevalence of, and risk factors for, inappropriate use. Arch Intern Med 2003;163:601605.
38.Poole, K. Efflux-mediated resistance to fluoroquinolones in gram-negative bacteria. Antimicrob Agents Chemother 2000;44:22332241.
39.Paterson, DL. Looking for risk factors for the acquisition of antibiotic resistance: a 21st century approach. Clin Infect Dis 2002;34:15641567.
40.Baquero, F. Low-level antibacterial resistance: a gateway to clinical resistance. Drug Resistance Updates 2001;4:93105.
41.Courvalin, P, Trieu-Cuot, P. Minimizing potential resistance: the molecular view. Clin Infect Dis 2001;33(Suppl 3):S138S146.

Metrics

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