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Journal of Clinical Microbiology logoLink to Journal of Clinical Microbiology
. 1996 Sep;34(9):2163–2169. doi: 10.1128/jcm.34.9.2163-2169.1996

Epidemiological study of an outbreak due to multidrug-resistant Enterobacter aerogenes in a medical intensive care unit.

C Arpin 1, C Coze 1, A M Rogues 1, J P Gachie 1, C Bebear 1, C Quentin 1
PMCID: PMC229210  PMID: 8862578

Abstract

In 1993, 63 isolates of Enterobacter aerogenes were collected from 41 patients in a medical intensive care unit (ICU). During the same period, only 46 isolates from 32 patients were collected in the rest of the hospital. All isolates were analyzed by antibiotic resistance phenotype, and 77 representative isolates were differentiated by plasmid restriction analysis, ribotyping, and arbitrarily primed (AP)-PCR. The extended-spectrum beta-lactamases produced by 22 strains were characterized by determination of their isoelectric points and by hybridization of plasmid DNA with specific probes. The isolates were divided into 25 antibiotic resistance phenotypes, either susceptible (group I) or resistant (group II) to aminoglycosides, and exhibited three phenotypes of resistance to beta-lactams: chromosomally derepressed cephalosporinase alone or associated with either extended-spectrum beta-lactamases (mainly of the SHV-4 type) or imipenem resistance. The results of the tests divided the 77 representative isolates (group I, n = 21; group II, n = 56) into 15 plasmid profiles, 14 ribotypes, and 15 AP-PCR patterns. Although the resistant isolates (group II) exhibited different plasmid profiles, ribotyping and AP-PCR analysis demonstrated an identical chromosomal pattern, indicating an epidemiological relatedness. They were mainly found in the medical ICU and occasionally in other units. The susceptible strains (group I) had various and distinct markers and were mainly isolated in units other than the medical ICU. In conclusion, the presence of a nosocomial outbreak in an ICU and the spread of a multidrug-resistant epidemic strain throughout the hospital was confirmed. Ribotyping and AP-PCR represent discriminatory tools for the investigation of nosocomial outbreaks caused by E. aerogenes.

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Selected References

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  1. Birnboim H. C., Doly J. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 1979 Nov 24;7(6):1513–1523. doi: 10.1093/nar/7.6.1513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Brosius J., Ullrich A., Raker M. A., Gray A., Dull T. J., Gutell R. R., Noller H. F. Construction and fine mapping of recombinant plasmids containing the rrnB ribosomal RNA operon of E. coli. Plasmid. 1981 Jul;6(1):112–118. doi: 10.1016/0147-619x(81)90058-5. [DOI] [PubMed] [Google Scholar]
  3. Chabbert Y. A., El Solh N., Le Pors M. J., Roussel A., Witchitz J. L. Plasmid epidemics. Prog Clin Biol Res. 1979;35:27–32. [PubMed] [Google Scholar]
  4. Chanal C. M., Sirot D. L., Petit A., Labia R., Morand A., Sirot J. L., Cluzel R. A. Multiplicity of TEM-derived beta-lactamases from Klebsiella pneumoniae strains isolated at the same hospital and relationships between the responsible plasmids. Antimicrob Agents Chemother. 1989 Nov;33(11):1915–1920. doi: 10.1128/aac.33.11.1915. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chow J. W., Shlaes D. M. Imipenem resistance associated with the loss of a 40 kDa outer membrane protein in Enterobacter aerogenes. J Antimicrob Chemother. 1991 Oct;28(4):499–504. doi: 10.1093/jac/28.4.499. [DOI] [PubMed] [Google Scholar]
  6. Davin-Regli A., Saux P., Bollet C., Gouin F., De Micco P. Investigation of outbreaks of Enterobacter aerogenes colonisation and infection in intensive care units by random amplification of polymorphic DNA. J Med Microbiol. 1996 Feb;44(2):89–98. doi: 10.1099/00222615-44-2-89. [DOI] [PubMed] [Google Scholar]
  7. Flynn D. M., Weinstein R. A., Nathan C., Gaston M. A., Kabins S. A. Patients' endogenous flora as the source of "nosocomial" Enterobacter in cardiac surgery. J Infect Dis. 1987 Aug;156(2):363–368. doi: 10.1093/infdis/156.2.363. [DOI] [PubMed] [Google Scholar]
  8. Gaston M. A. Enterobacter: an emerging nosocomial pathogen. J Hosp Infect. 1988 Apr;11(3):197–208. doi: 10.1016/0195-6701(88)90098-9. [DOI] [PubMed] [Google Scholar]
  9. Gaston M. A., Strickland M. A., Ayling-Smith B. A., Pitt T. L. Epidemiological typing of Enterobacter aerogenes. J Clin Microbiol. 1989 Mar;27(3):564–565. doi: 10.1128/jcm.27.3.564-565.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Georghiou P. R., Hamill R. J., Wright C. E., Versalovic J., Koeuth T., Watson D. A., Lupski J. R. Molecular epidemiology of infections due to Enterobacter aerogenes: identification of hospital outbreak-associated strains by molecular techniques. Clin Infect Dis. 1995 Jan;20(1):84–94. doi: 10.1093/clinids/20.1.84. [DOI] [PubMed] [Google Scholar]
  11. Grattard F., Pozzetto B., Berthelot P., Rayet I., Ros A., Lauras B., Gaudin O. G. Arbitrarily primed PCR, ribotyping, and plasmid pattern analysis applied to investigation of a nosocomial outbreak due to Enterobacter cloacae in a neonatal intensive care unit. J Clin Microbiol. 1994 Mar;32(3):596–602. doi: 10.1128/jcm.32.3.596-602.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Grattard F., Pozzetto B., Tabard L., Petit M., Ros A., Gaudin O. G. Characterization of nosocomial strains of Enterobacter aerogenes by arbitrarily primed-PCR analysis and ribotyping. Infect Control Hosp Epidemiol. 1995 Apr;16(4):224–230. doi: 10.1086/647094. [DOI] [PubMed] [Google Scholar]
  13. Grimont F., Grimont P. A. Ribosomal ribonucleic acid gene restriction patterns as potential taxonomic tools. Ann Inst Pasteur Microbiol. 1986 Sep-Oct;137B(2):165–175. doi: 10.1016/s0769-2609(86)80105-3. [DOI] [PubMed] [Google Scholar]
  14. Haertl R., Bandlow G. Epidemiological fingerprinting of Enterobacter cloacae by small-fragment restriction endonuclease analysis and pulsed-field gel electrophoresis of genomic restriction fragments. J Clin Microbiol. 1993 Jan;31(1):128–133. doi: 10.1128/jcm.31.1.128-133.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hopkins J. M., Towner K. J. Enhanced resistance to cefotaxime and imipenem associated with outer membrane protein alterations in Enterobacter aerogenes. J Antimicrob Chemother. 1990 Jan;25(1):49–55. doi: 10.1093/jac/25.1.49. [DOI] [PubMed] [Google Scholar]
  16. Huber T. W., Thomas J. S. Detection of resistance due to inducible beta-lactamase in Enterobacter aerogenes and Enterobacter cloacae. J Clin Microbiol. 1994 Oct;32(10):2481–2486. doi: 10.1128/jcm.32.10.2481-2486.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. John J. F., Jr, Twitty J. A. Plasmids as epidemiologic markers in nosocomial gram-negative bacilli: experience at a university and review of the literature. Rev Infect Dis. 1986 Sep-Oct;8(5):693–704. doi: 10.1093/clinids/8.5.693. [DOI] [PubMed] [Google Scholar]
  18. Leying H., Cullmann W., Dick W. Carbapenem resistance in Enterobacter aerogenes is due to lipopolysaccharide alterations. Chemotherapy. 1991;37(2):106–113. doi: 10.1159/000238841. [DOI] [PubMed] [Google Scholar]
  19. Lupski J. R. Molecular mechanisms for transposition of drug-resistance genes and other movable genetic elements. Rev Infect Dis. 1987 Mar-Apr;9(2):357–368. doi: 10.1093/clinids/9.2.357. [DOI] [PubMed] [Google Scholar]
  20. Markowitz S. M., Smith S. M., Williams D. S. Retrospective analysis of plasmid patterns in a study of burn unit outbreaks of infection due to Enterobacter cloacae. J Infect Dis. 1983 Jul;148(1):18–23. doi: 10.1093/infdis/148.1.18. [DOI] [PubMed] [Google Scholar]
  21. Mathew A., Harris A. M., Marshall M. J., Ross G. W. The use of analytical isoelectric focusing for detection and identification of beta-lactamases. J Gen Microbiol. 1975 May;88(1):169–178. doi: 10.1099/00221287-88-1-169. [DOI] [PubMed] [Google Scholar]
  22. Mellencamp M. A., Roccaforte J. S., Preheim L. C., Sanders C. C., Anene C. A., Bittner M. J. Isolation of Enterobacter aerogenes susceptible to beta-lactam antibiotics despite high level beta-lactamase production. Eur J Clin Microbiol Infect Dis. 1990 Nov;9(11):827–830. doi: 10.1007/BF01967384. [DOI] [PubMed] [Google Scholar]
  23. Meyers H. B., Fontanilla E., Mascola L. Risk factors for development of sepsis in a hospital outbreak of Enterobacter aerogenes. Am J Infect Control. 1988 Jun;16(3):118–122. doi: 10.1016/0196-6553(88)90050-8. [DOI] [PubMed] [Google Scholar]
  24. Nicolas M. H., Jarlier V., Honore N., Philippon A., Cole S. T. Molecular characterization of the gene encoding SHV-3 beta-lactamase responsible for transferable cefotaxime resistance in clinical isolates of Klebsiella pneumoniae. Antimicrob Agents Chemother. 1989 Dec;33(12):2096–2100. doi: 10.1128/aac.33.12.2096. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Philippon A., Labia R., Jacoby G. Extended-spectrum beta-lactamases. Antimicrob Agents Chemother. 1989 Aug;33(8):1131–1136. doi: 10.1128/aac.33.8.1131. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Poilane I., Cruaud P., Lachassinne E., Grimont F., Grimont P. A., Collin M., Gaudelus J., Torlotin J. C., Collignon A. Enterobacter cloacae cross-colonization in neonates demonstrated by ribotyping. Eur J Clin Microbiol Infect Dis. 1993 Nov;12(11):820–826. doi: 10.1007/BF02000401. [DOI] [PubMed] [Google Scholar]
  27. Ross G. W., Boulton M. G. Improvement of the specificity of an antiserum to -lactamase by absorption with a mutant which does not produce the enzyme. J Bacteriol. 1972 Dec;112(3):1435–1437. doi: 10.1128/jb.112.3.1435-1437.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Ross G. W., Boulton M. G. Purification of beta-lactamases on QAE-sephadex. Biochim Biophys Acta. 1973 Jun 6;309(2):430–439. doi: 10.1016/0005-2744(73)90041-7. [DOI] [PubMed] [Google Scholar]
  29. Rubens C. E., Farrar W. E., Jr, McGee Z. A., Schaffner W. Evolution of a plasmid mediating resistance to multiple antimicrobial agents during a prolonged epidemic of nosocomial infections. J Infect Dis. 1981 Feb;143(2):170–181. doi: 10.1093/infdis/143.2.170. [DOI] [PubMed] [Google Scholar]
  30. Sirot D., Sirot J., Labia R., Morand A., Courvalin P., Darfeuille-Michaud A., Perroux R., Cluzel R. Transferable resistance to third-generation cephalosporins in clinical isolates of Klebsiella pneumoniae: identification of CTX-1, a novel beta-lactamase. J Antimicrob Chemother. 1987 Sep;20(3):323–334. doi: 10.1093/jac/20.3.323. [DOI] [PubMed] [Google Scholar]
  31. Tzouvelekis L. S., Tzelepi E., Mentis A. F., Vatopoulos A. C., Tsakris A. Imipenem resistance in Enterobacter aerogenes is associated with derepression of chromosomal cephalosporinases and impaired permeability. FEMS Microbiol Lett. 1992 Aug 15;74(2-3):195–199. doi: 10.1016/0378-1097(92)90428-q. [DOI] [PubMed] [Google Scholar]
  32. de Champs C., Guelon D., Joyon D., Sirot D., Chanal M., Sirot J. Treatment of a meningitis due to an Enterobacter aerogenes producing a derepressed cephalosporinase and a Klebsiella pneumoniae producing an extended-spectrum beta-lactamase. Infection. 1991 May-Jun;19(3):181–183. doi: 10.1007/BF01643247. [DOI] [PubMed] [Google Scholar]
  33. de Champs C., Henquell C., Guelon D., Sirot D., Gazuy N., Sirot J. Clinical and bacteriological study of nosocomial infections due to Enterobacter aerogenes resistant to imipenem. J Clin Microbiol. 1993 Jan;31(1):123–127. doi: 10.1128/jcm.31.1.123-127.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. de Champs C., Sirot D., Chanal C., Poupart M. C., Dumas M. P., Sirot J. Concomitant dissemination of three extended-spectrum beta-lactamases among different Enterobacteriaceae isolated in a French hospital. J Antimicrob Chemother. 1991 Apr;27(4):441–457. doi: 10.1093/jac/27.4.441. [DOI] [PubMed] [Google Scholar]

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