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Extended-spectrum β-lactamase-producing Shigella strains in Israel, 2000–2004

  • V. VasilevEmail author
  • R. Japheth
  • R. Yishai
  • N. Andorn
  • L. Valinsky
  • S. Navon-Venezia
  • I. Chmelnitsky
  • Y. Carmeli
  • D. Cohen
Article

Abstract

Routine susceptibility testing of 5,616 Shigella isolates at the National Shigella Reference Centre in Israel over a 5-year period (2000–2004) revealed resistance to ceftriaxone in one strain of Shigella boydii 2 and in two strains each of Shigella flexneri 2a, S. flexneri 6, and Shigella sonnei. All seven isolates were confirmed as producers of extended-spectrum β-lactamase (ESBL) by the combination disk method, the Vitek 1 system, and a modification of the double-disk synergy test, which is based on the inhibitory properties of clavulanic acid, tazobactam, and sulbactam. Tazobactam had the strongest effect in all seven strains. Molecular characterization of the ESBLs identified CTX-M-type enzymes, consisting of the CTX-M-9 group (n = 3), CTX-M-3 (n = 2), CTX-M-39 (n = 1), and CTX-M-2 group (n = 1). Three of the strains also carried bla-OXA genes and a bla-TEM gene. Although the prevalence of ESBLs in this study was low, further research is needed on the spread and transfer of resistance genes, both in hospitals and in the community.

Keywords

Clavulanic Acid Cefpodoxime Shigellosis Tazobactam Shigella Flexneri 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

The authors are grateful to C. Block, J.M. Shehadeh, E. Cohen, G. Rahav, and B. Reuveni for their assistance.

References

  1. 1.
    Ahamed J, Kundu M (1999) Molecular characterization of the SHV-11 β-lactamase of Shigella dysenteriae. Antimicrob Agents Chemother 43:2081–2083PubMedGoogle Scholar
  2. 2.
    Jeong YS, Lee JC, Kang HY, Yu HS, Lee EY, Choi CH, Tae SH, Lee YC, Cho DT, Seol SY (2003) Epidemiology of nalidixic acid resistance and TEM-1- and TEM-52-mediated ampicillin resistance of Shigella sonnei isolates obtained in Korea between 1980 and 2000. Antimicrob Agents Chemother 47:3719–3723PubMedCrossRefGoogle Scholar
  3. 3.
    Schumacher H, Nir M, Mansa B, Grassy A (1992) β-Lactamases in Shigella. APMIS 100:954–956PubMedCrossRefGoogle Scholar
  4. 4.
    Livermore DM (1995) β-Lactamases in laboratory and clinical resistance. Clin Microbiol Rev 8:557–584PubMedGoogle Scholar
  5. 5.
    Walter-Rasmussen J, Høiby N (2004) Cefotaximases (CTX-M-ases), an expanding family of extended-spectrum β-lactamases. Can J Microbiol 50:137–165CrossRefGoogle Scholar
  6. 6.
    Bonnet R (2004) Growing group of extended-spectrum β-lactamases: the CTX-M enzymes. Antimicrob Agents Chemother 48:1–14PubMedCrossRefGoogle Scholar
  7. 7.
    Woodford N, Ward ME, Kaufmann ME, Turton J, Fagan EJ, James D, Johnson AP, Pike R, Warner M, Cheasty T, Pearson A, Harry S, Leach JB, Loughrey A, Lowes JA, Warren RE, Livermore D (2004) Community and hospital spread of Escherichia coli producing CTX-M extended-spectrum β-lactamases in the UK. J Antimicrob Chemother 54:735–743PubMedCrossRefGoogle Scholar
  8. 8.
    Pitout JDD, Hanson ND, Church DL, Laupland KB (2004) Population-based laboratory surveillance for Escherichia coli-producing extended-spectrum β-lactamases: importance of community isolates with bla CTX-M genes. Clin Infect Dis 38:1736–1741PubMedCrossRefGoogle Scholar
  9. 9.
    Pallecci L, Malossi M, Mantella A, Gotuzzo E, Trigoso C, Bartoloni A, Paradisi F, Kronvall G, Rossolini GM (2004) Detection of CTX-M-type β-lactamase gene in fecal Escherichia coli isolates from healthy children in Bolivia and Peru. Antimicrob Agents Chemother 48:4556–4561CrossRefGoogle Scholar
  10. 10.
    Bou G, Cartelle M, Tomas M, Canle D, Molina F, Moure R, Eiros JM, Guerrero A (2002) Identification and broad dissemination of CTX-M-14 β-lactamase in different Escherichia coli strains in the northwest area of Spain. J Clin Microbiol 40:4030–4036PubMedCrossRefGoogle Scholar
  11. 11.
    Ben-Ami R, Schwaber MJ, Navon-Venezia S, Schwartz D, Giladi M, Chmelnitsky I, Leavitt A, Carmeli Y (2006) Influx of extended-spectrum β-lactamase-producing Enterobacteriaceae into the hospital. Clin Infect Dis 42:925–934PubMedCrossRefGoogle Scholar
  12. 12.
    Borer A, Gilad J, Menashe G, Peled N, Reisenberg K, Schlaeffer F (2002) Extended-spectrum beta-lactamase producing Enterobacteriaceae strains in southern Israel. Med Sci Monit 8:CR44-CR47PubMedGoogle Scholar
  13. 13.
    Navon-Venezia S, Hammer-Munz O, Schwartz D, Turner D, Kuzmenko B, Carmeli Y (2003) Occurrence and phenotypic characteristics of extended-spectrum β-lactamases among members of the family Enterobacteriaceae at the Tel-Aviv Medical Center (Israel) and evaluation of diagnostic tests. J Clin Microbiol 41:155–158PubMedCrossRefGoogle Scholar
  14. 14.
    Colodner R, Raz R, Chazan B, Sakran W (2004) Susceptibility pattern of extended spectrum β-lactamase producing bacteria isolated from inpatients to five antimicrobial drugs in a community hospital in Northern Israel. Int J Antimicrob Agents 24:409–410PubMedCrossRefGoogle Scholar
  15. 15.
    Mendelson G, Hait V, Ben-Israel J, Gronich D, Granot E, Raz R (2005) Prevalence and risk factors of extended-spectrum-producing Escherichia coli and Klebsiella pneumoniae in an Israeli long-term care facility. Eur J Microbiol Infect Dis 24:17–22CrossRefGoogle Scholar
  16. 16.
    Vasilev V, Japheth R, Yishai R, Andorn N (2004) Antimicrobial resistance of Shigella flexneri serotypes in Israel during a period of three years: 2000–2002. Epidemiol Infect 132:1049–1054PubMedCrossRefGoogle Scholar
  17. 17.
    Bauer AW, Kirby WM, Sherris JC, Turk N (1966) Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol 36:493–496Google Scholar
  18. 18.
    National Committee for Clinical Laboratory Standards (1999) Performance standards for antimicrobial susceptibility testing. Approved standard M100–S9. NCCLS, Wayne, PAGoogle Scholar
  19. 19.
    National Committee for Clinical Laboratory Standards (2003) Performance standards for antimicrobial susceptibility testing. 13th informational supplement. Document M100–S13 (M2), for use with M2-A8-Disk Diffusion. NCCLS, Wayne, PAGoogle Scholar
  20. 20.
    National Committee for Clinical Laboratory Standards (2003) Performance standards for antimicrobial disk susceptibility tests. Approved standard M2–A8. NCCLS, Wayne, PAGoogle Scholar
  21. 21.
    European Antimicrobial Resistance Surveillance System (2004) Protocol for ESBL reporting. EARSS manual. National Institute of Public Health and Environmental Hygiene (RIVM), Bilthoven, the Netherlands, pp 26–27Google Scholar
  22. 22.
    Thomson K, Molland E (2004) Newer β-lactamases: clinical and laboratory implications (in-house manual). Center for Research in Antiinfectives and Biotechnology. Department of Medical Microbiology and Immunology, Creighton University School of Medicine. Omaha, Nebraska, pp 5–6Google Scholar
  23. 23.
    Bush K, Macalintal C, Rasmussen BA, Lee VJ, Yang Y (1993) Kinetic interactions of tazobactam with β-lactamases from all major structural classes. Antimicrob Agents Chemother 37:851–858PubMedGoogle Scholar
  24. 24.
    Tzouvelekis LS, Tzelepi E, Tassios PT, Legakis NJ (2000) CTX-M- type β-lactamases: an emerging group of extended-spectrum enzymes. Int J Antimicrob Agents 14:137–142PubMedCrossRefGoogle Scholar
  25. 25.
    Poirel P, Gniadkowski M, Nordman P (2002) Biochemical analysis of the ceftazidime-hydrolising extended-spectrum β-lactamase CTX-M-15 and of its structurally related β-lactamase CTX-M-3. J Antimicrob Chemother 50:1031–1034PubMedCrossRefGoogle Scholar
  26. 26.
    Stürenburg E, Mack D (2003) Extended-spectrum β-lactamases: implications for the clinical microbiological laboratory, therapy and infection control. J Infect 47:273–295PubMedCrossRefGoogle Scholar
  27. 27.
    Schlesinger Y, Navon-Venezia S, Chmelnitsky I, Hammer-Münz O, Leavitt A, Gold HS, Schwaber MJ, Carmeli Y (2005) Characterization of extended-spectrum beta-lactamases (ESBLs) among Enterobacter isolates in Tel-Aviv. Antimicrob Agents Chemother 49:1150–1156PubMedCrossRefGoogle Scholar
  28. 28.
    Nordmann P, Naas T (1994) Sequence analysis of PER-1 extended-spectrum beta-lactamase from Pseudomonas aeruginosa and comparison with class-A beta-lactamases. Antimicrob Agents Chemother 38:104–114PubMedGoogle Scholar
  29. 29.
    Bauerfeind A, Stemplinger I, Jungwirth R, Ernst S, Casellas JM (1996) Sequences of β-lactamase genes encoding CTX-M-1 (MEN-1) and CTX-M-2 and relationship of their amino acid sequences with those of other β-lactamases. Antimicrob Agents Chemother 40:509–513Google Scholar
  30. 30.
    Steward CD, Rasheed JK, Hubert SK, Biddle JW, Raney PM, Anderson GJ, William PP, Brittain KL, Oliver A, McGowan JE, Tenover FC (2001) Characterization of clinical isolates of Klebsiella pneumoniae from 19 laboratories using the National Committee for Clinical Laboratory Standards extended-spectrum beta-lactamase detection methods. J Clin Microbiol 39:2864–2872PubMedCrossRefGoogle Scholar
  31. 31.
    Chmelnitsky I, Carmeli Y, Leavitt A, Schwaber MJ, Navon-Venezia S (2005) CTX-M-2 and a new CTX-M-39 enzyme are the major extended-spectrum beta-lactamases in multiple Escherichia coli clones from Tel-Aviv. Antimicrob Agents Chemother 49:4745–4750PubMedCrossRefGoogle Scholar
  32. 32.
    Sabate M, Tarrago R, Navarro F, Miro E, Verges C, Barbe J, Prats G (2000) Cloning and sequence of the gene encoding a novel cefotaxime-hydrolyzing beta-lactamase (CTX-M-9) from Escherichia coli in Spain. Antimicrob Agents Chemother 44:1970–1973PubMedCrossRefGoogle Scholar
  33. 33.
    Quellette M, Bissonnette L, Roy PH (1997) Precise insertion of antibiotic resistance determinants into Tn21-like transposons: nucleotide sequence of the OXA-1 β-lactamase gene. Proc Natl Acad Sci USA 84:7378–7387Google Scholar
  34. 34.
    Eckert C, Gautier V, Saladin-Allard M, Hidri N, Verdet C, Ould-Hocine Z, Barnaud G, Delisle F, Rossier A, Lambert T, Phillipon A, Arlet G (2004) Dissemination of CTX-M-type β-lactamases among clinical isolates of Enterobacteriaceae in Paris, France. Antimicrob Agents Chemother 48:1249–1255PubMedCrossRefGoogle Scholar
  35. 35.
    Kim S, Kim J, Kang Y, Park Y, Lee B (2004) Occurrence of extended-spectrum beta-lactamases in members of the genus Shigella in the Republic of Korea. J Clin Microbiol 42:5264–5269PubMedCrossRefGoogle Scholar
  36. 36.
    Acikgoz ZC, Gulay Z, Bicmen M, Gocer S, Gamberzade S (2003) CTX-M-3 extended-spectrum β-lactamase in a Shigella sonnei clinical isolate: first report from Turkey. Scand J Infect Dis 35:503–505PubMedCrossRefGoogle Scholar
  37. 37.
    Pai H, Choi EC, Lee HJ, Hong JY, Jacoby GA (2001) Identification of CTX-M-14 extended-spectrum β-lactamase in clinical isolates of Shigella sonnei, Escherichia coli and Klebsiella pneumoniae in Korea. J Clin Microbiol 39:3747–3749PubMedCrossRefGoogle Scholar
  38. 38.
    Radice M, Gonzales C, Power MC, Vidal P, Gutkind G (2001) Third-generation cephalosporin resistance in Shigella sonnei, Argentina. Emerg Infect Dis 7:442–443PubMedGoogle Scholar
  39. 39.
    Navia MM, Capitano L, Ruiz J, Vargas M, Urassa H, Schellemberg D, Gascon J, Vila J (1999) Typing and characterization of mechanisms of resistance of Shigella spp. isolated from feces of children under 5 years of age from Ifakara, Tanzania. J Clin Microbiol 37:3113–3117PubMedGoogle Scholar
  40. 40.
    Siu LK, Lo JYC, Yuen PY, Chau MHNG, Ho PL (2000) β-Lactamases in Shigella flexneri isolated from Hong Kong and Shanghai and a novel OXA-1-like β-lactamase, OXA-30. Antimicrob Agents Chemother 44:2034–2038PubMedCrossRefGoogle Scholar
  41. 41.
    Sirot D, Chanal C, Bennet R, Champs CD, Sirot J (2001) Inhibitor-resistant TEM-33 β-lactamase in a Shigella sonnei isolate. Antimicrob Agents Chemother 45:2179–2180PubMedCrossRefGoogle Scholar
  42. 42.
    Peirano G, Agersø Y, Aarestrup FM, Rodrigues DP (2005) Occurrence of integrons and resistance genes among sulphonamide-resistant Shigella spp. from Brazil. J Antimicrob Chemother 55:301–305PubMedCrossRefGoogle Scholar
  43. 43.
    Leverstein-van Hall MA, Fluit AC, Paauw A, Box ATA, Brisse S, Verhoef J (2002) Evaluation of the E test ESBL and BD Phoenix, VITEK 1, and VITEK 2 automated instruments for detection of extended-spectrum beta-lactamases in multiresistant Escherichia coli and Klebsiella spp. J Clin Microbiol 40:3703–3711PubMedCrossRefGoogle Scholar
  44. 44.
    Lartigue M, Poirel L, Decousser J, Nordman P (2005) Multidrug-resistant Shigella sonnei and Salmonella enterica serotype typhimurium isolates producing CTX-M β-lactamases as causes of community-acquired infection in France. Clin Infect Dis 40:1069–1070PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • V. Vasilev
    • 1
    Email author
  • R. Japheth
    • 1
  • R. Yishai
    • 1
  • N. Andorn
    • 1
  • L. Valinsky
    • 1
  • S. Navon-Venezia
    • 2
  • I. Chmelnitsky
    • 2
  • Y. Carmeli
    • 2
  • D. Cohen
    • 3
  1. 1.Central Laboratories of the Ministry of HealthGivat Shaul, JerusalemIsrael
  2. 2.Division of EpidemiologyTel Aviv Sourasky Medical CenterTel AvivIsrael
  3. 3.Department of Epidemiology and Preventive Medicine, Sackler Faculty of MedicineTel Aviv UniversityTel AvivIsrael

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