This Article
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Morris, D.
Right arrow Articles by Doran, G.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Morris, D.
Right arrow Articles by Doran, G.

 Previous Article  |  Next Article 

Antimicrobial Agents and Chemotherapy, April 2006, p. 1608-1609, Vol. 50, No. 4
0066-4804/06/$08.00+0     doi:10.1128/AAC.50.4.1608-1609.2006
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

LETTER TO THE EDITOR

First Report of Extended-Spectrum-ß-Lactamase-Producing Salmonella enterica Isolates in Ireland


arrow
LETTER
 
Production of extended-spectrum-ß-lactamases (ESBLs) is predominantly associated with the Enterobacteriaceae, particularly Escherichia coli and Klebsiella pneumoniae. ESBL production in Salmonella spp. was first identified in 1988 (11) and is increasing in prevalence worldwide (3, 18). A survey of ESBL prevalence in Enterobacteriaceae in Ireland was previously conducted, but this did not include Salmonella spp. (13). We have examined a large collection of human and animal isolates of salmonella for ESBL production.

Antimicrobial susceptibility data for 4,466 isolates received between January 2001 and April 2005 was reviewed for suspected ESBL production using Clinical Laboratory Standards Institute (CLSI) ESBL screen criteria (7). This represents the complete collection of isolates received from human and animal sources by the National Salmonella Reference Laboratory of Ireland during this time period. ESBL production was confirmed by the CLSI combination disk method using cefpodoxime and cefpodoxime plus clavulanate and by the ESBL Etest method using ceftazidime/ ceftazidime plus clavulanate, cefotaxime/cefotaxime plus clavulanate, and cefepime/cefepime plus clavulanate strips (AB Biodisk). Confirmed ESBL producers were screened for blaTEM and blaSHV by PCR using specific primers and protocols as reported previously (8). The blaCTX-M gene was detected by PCR using universal CTX-M primers (16). The gene was characterized by PCR and sequencing as previously described for group 1 and group 9 genes (3) and using primers CTX-M-group-2F (5'-ATGATGACTCAG AGCATTC) and CTX-M-group-2R (5'-TCAGAAACCGTGGGTTAC) for group 2 genes (4) or primers CTX-M-group 8/25F (5'-ATGATGAGAAAAAGC GTAAG) and CTX-M-group 8/25R (5'-TTAATAACCGTCGGTGAC), designed from the nucleotide sequence alignment of blaCTX-M-8 (5), blaCTX-M-25 (15), and blaCTX-M-26 (6), for group 8 and group 25 genes.

Seven ESBL-producing isolates were detected (Table 1). Five were from humans, and four of these were associated with travel outside of Ireland. Six of the seven ESBL producers were coresistant to other classes of antimicrobial agents (Table 1). The Salmonella enterica serovar Worthington isolate was from a 6-month-old child of Indian origin. Previous reports of serovar Worthington infection are predominantly from India, and resistance to cefotaxime and ceftriaxone has been noted (10); however, this is the first confirmation of ESBL production in serovar Worthington. The S. enterica serovar Concord isolate was from a patient originally from Ethiopia. CTX-M production in serovar Concord has not previously been reported. CTX-M production in S. enterica serovar Typhimurium is well described (9). The majority of enzymes reported in this serovar belong to CTX-M group 2; however, CTX-M-15 and CTX-M-3 (both CTX-M group 1) have also recently been reported (1, 14). Serovar Typhimurium 695/04 reported here represents the first description of blaCTX-M-14 in this serovar. Serovar Typhimurium 227/05 was associated with travel to Andorra. The isolate repeatedly was confirmed as ESBL positive, with a cefotaxime MIC of 4 µg/ml, falling to 0.094 µg/ml in the presence of clavulanic acid, and a cefepime MIC of 16 µg/ml, falling to 0.25 µg/ml with clavulanic acid, while the ceftazidime MIC was 0.5 µg/ml. PCR assays for blaCTX-M, blaSHV, and blaTEM were consistently negative for this isolate, and DNA was shown to be amplifiable by the 16S/23S rRNA intergenic spacer region PCR (2) (Table 1). The most common cefotaximases encountered are the CTX-M family of ß-lactamases, and several members of this group have been associated with high levels of resistance to cefepime (12, 19). Hyperproduction of SHV-5 has also been associated with elevated MICs for cefepime (17). High-level resistance to cefepime in previous studies was associated with high level resistance (>32 µg/ml) to cefotaxime, which was not observed in isolate number 227/05 (12, 17). This suggests that this isolate may harbor another type of ESBL, e.g., PER-1, PER-2, VEB-1, BEL-1, or GES-1.


View this table:
[in this window]
[in a new window]
 
TABLE 1. Extended antibiogram, PCR, and sequence analysis results for isolates confirmed as ESBL producers by phenotypic methods


arrow
REFERENCES
 
    1
  1. Baraniak, A., E. Sadowy, W. Hryniewicz, and M. Gniadkowski. 2002. Two different extended-spectrum beta-lactamases (ESBLs) in one of the first ESBL-producing salmonella isolates in Poland. J. Clin. Microbiol. 40:1095-1097.[Abstract/Free Full Text]
  2. 2
  3. Barry, T., G. Colleran, M. Glennon, L. K. Dunican, and F. Gannon. 1991. The 16S-23S ribosomal spacer region as a target for DNA probes to identify eubacteria. PCR Methods Appl. 1:51-56.[Medline]
  4. 3
  5. Batchelor, M., K. Hopkins, E. J. Threlfall, F. A. Clifton-Hadley, A. D. Stallwood, R. H. Davies, and E. Liebana. 2005. blaCTX-M genes in clinical Salmonella isolates recovered from humans in England and Wales from 1992 to 2003. Antimicrob. Agents Chemother. 49:1319-1322.[Abstract/Free Full Text]
  6. 4
  7. Bauernfeind, A., I. Stemplinger, R. Jungwirth, S. Ernst, and J. M. Casellas. 1996. Sequences of beta-lactamase genes encoding CTX-M-1 (MEN-1) and CTX-M-2 and relationship of their amino acid sequences with those of other beta-lactamases. Antimicrob. Agents Chemother. 40:509-513.[Abstract]
  8. 5
  9. Bonnet, R., J. L. Sampaio, R. Labia, C. De Champs, D. Sirot, C. Chanal, and J. Sirot. 2000. A novel CTX-M beta-lactamase (CTX-M-8) in cefotaxime-resistant Enterobacteriaceae isolated in Brazil. Antimicrob. Agents Chemother. 44:1936-1942.[Abstract/Free Full Text]
  10. 6
  11. Brenwald, N. P., G. Jevons, J. M. Andrews, J. H. Xiong, P. M. Hawkey, and R. Wise. 2003. An outbreak of a CTX-M-type beta-lactamase-producing Klebsiella pneumoniae: the importance of using cefpodoxime to detect extended-spectrum beta-lactamases. J. Antimicrob. Chemother. 51:195-196.[Free Full Text]
  12. 7
  13. Clinical and Laboratory Standards Institute. 2005. Performance standards for antimicrobial disk susceptibility tests, approved standard, 8th ed. (M2-A8). Clinical and Laboratory Standards Institute, Wayne, Pa.
  14. 8
  15. Essack, S. Y., L. M. Hall, D. G. Pillay, M. L. McFadyen, and D. M. Livermore. 2001. Complexity and diversity of Klebsiella pneumoniae strains with extended-spectrum beta-lactamases isolated in 1994 and 1996 at a teaching hospital in Durban, South Africa. Antimicrob. Agents Chemother. 45:88-95.[Abstract/Free Full Text]
  16. 9
  17. Gazouli, M., E. Tzelepi, A. Markogiannakis, N. J. Legakis, and L. S. Tzouvelekis. 1998. Two novel plasmid-mediated cefotaxime-hydrolyzing beta-lactamases (CTX-M-5 and CTX-M-6) from Salmonella typhimurium. FEMS Microbiol. Lett. 165:289-293.[Medline]
  18. 10
  19. Ghadage, D., and A. Bal. 2003. Outbreak of neonatal meningitis caused by Salmonella enterica serotype Worthington. Indian J. Pathol. Microbiol. 46:268-270.[Medline]
  20. 11
  21. Hammami, A., G. Arlet, S. Ben Redjeb, F. Grimont, A. Ben Hassen, A. Rekik, and A. Philippon. 1991. Nosocomial outbreak of acute gastroenteritis in a neonatal intensive care unit in Tunisia caused by multiply drug resistant Salmonella wien producing SHV-2 beta-lactamase. Eur. J. Clin. Microbiol. Infect. Dis. 10:614-616.
  22. 12
  23. Jeong, S. H., I. K. Bae, S. B. Kwon, J. H. Lee, J. S. Song, H. I. Jung, K. H. Sung, S. J. Jang, and S. H. Lee. 2005. Dissemination of transferable CTX-M-type extended-spectrum beta-lactamase-producing Escherichia coli in Korea. J. Appl. Microbiol. 98:921-927.[CrossRef][Medline]
  24. 13
  25. Morris, D., C. O'Hare, M. Glennon, M. Maher, G. Corbett-Feeney, and M. Cormican. 2003. Extended-spectrum ß-lactamases in Ireland, including a novel enzyme, TEM-102. Antimicrob. Agents Chemother. 47:2572-2578.[Abstract/Free Full Text]
  26. 14
  27. Moubareck, C., F. Doucet-Populaire, M. Hamze, Z. Daoud, and F. X. Weill. 2005. First extended-spectrum-beta-lactamase (CTX-M-15)-producing Salmonella enterica serotype Typhimurium isolate identified in Lebanon. Antimicrob. Agents Chemother. 49:864-865.[Free Full Text]
  28. 15
  29. Munday, C. J., D. A. Boyd, N. Brenwald, M. Miller, J. M. Andrews, R. Wise, M. R. Mulvey, and P. M. Hawkey. 2004. Molecular and kinetic comparison of the novel extended-spectrum beta-lactamases CTX-M-25 and CTX-M-26. Antimicrob. Agents Chemother. 48:4829-4834.[Abstract/Free Full Text]
  30. 16
  31. Munday, C. J., G. M. Whitehead, N. J. Todd, M. Campbell, and P. M. Hawkey. 2004. Predominance and genetic diversity of community- and hospital-acquired CTX-M extended-spectrum beta-lactamases in York, UK. J. Antimicrob. Chemother. 54:628-633.[Abstract/Free Full Text]
  32. 17
  33. Tzouvelekis, L. S., E. Tzelepi, E. Prinarakis, M. Gazouli, A. Katrahoura, P. Giakkoupi, O. Paniara, and N. J. Legakis. 1998. Sporadic emergence of Klebsiella pneumoniae strains resistant to cefepime and cefpirome in Greek hospitals. J. Clin. Microbiol. 36:266-268.[Abstract/Free Full Text]
  34. 18
  35. Weill, F. X., J. D. Perrier-Gros-Claude, M. Demartin, S. Coignard, and P. A. Grimont. 2004. Characterization of extended-spectrum-beta-lactamase (CTX-M-15)-producing strains of Salmonella enterica isolated in France and Senegal. FEMS Microbiol. Lett. 238:353-358.[Medline]
  36. 19
  37. Yu, W. L., M. A. Pfaller, P. L. Winokur, and R. N. Jones. 2002. Cefepime MIC as a predictor of the extended-spectrum beta-lactamase type in Klebsiella pneumoniae, Taiwan. Emerg. Infect. Dis. 8:522-524.[Medline]
Dearbhaile Morris*
Mary Whelan
Geraldine Corbett-Feeney
Martin Cormican

Department of Bacteriology
National University of Ireland
Galway, Ireland,1

Peter Hawkey
Xu Li

Division of Immunity and Infection
University of Birmingham
Birmingham B15 2TT, United Kingdom,2

Geraldine Doran
National Salmonella Reference Laboratory of Ireland
University College Hospital
Galway, Ireland,3

* Phone: 35391544652, Fax: 35391495514, E-mail: dearbhaile.morris{at}nuigalway.ie


Antimicrobial Agents and Chemotherapy, April 2006, p. 1608-1609, Vol. 50, No. 4
0066-4804/06/$08.00+0     doi:10.1128/AAC.50.4.1608-1609.2006
Copyright © 2006, American Society for Microbiology. All Rights Reserved.




This article has been cited by other articles:

  • Fabre, L., Delaune, A., Espie, E., Nygard, K., Pardos, M., Polomack, L., Guesnier, F., Galimand, M., Lassen, J., Weill, F.-X. (2009). Chromosomal Integration of the Extended-Spectrum {beta}-Lactamase Gene blaCTX-M-15 in Salmonella enterica Serotype Concord Isolates from Internationally Adopted Children. Antimicrob. Agents Chemother. 53: 1808-1816 [Abstract] [Full Text]  
  • Rotimi, V. O., Jamal, W., Pal, T., Sovenned, A., Albert, M. J. (2008). Emergence of CTX-M-15 type extended-spectrum {beta}-lactamase-producing Salmonella spp. in Kuwait and the United Arab Emirates. J Med Microbiol 57: 881-886 [Abstract] [Full Text]  

This Article
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Morris, D.
Right arrow Articles by Doran, G.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Morris, D.
Right arrow Articles by Doran, G.