Prevalence and Molecular Epidemiology of Gram-negative Bacteria Producing Metallo-β-lactamases (MBLs) in Russia, Belarus and Kazakhstan | CMAC

Prevalence and Molecular Epidemiology of Gram-negative Bacteria Producing Metallo-β-lactamases (MBLs) in Russia, Belarus and Kazakhstan

Clinical Microbiology and Antimicrobial Chemotherapy. 2012; 14(2):132-152

​ Edelstein M.V., Skleenova E.Yu., Shevchenko O.V., Tapalskiy D.V., Azyzov I.S., D’souza J.W., Timokhova A.V., Sukhorukova M.V., Kozyreva V.K., Safronova E.V., Astakhova M.V., Karpov I.A., Shamaeva S.Kh., Abramova N.V., Gordinskaya N.A., Kozlov R.S., METALL study group
Gram-negative P. aeruginosa resistance metallo-beta-lactamase
Section
Antimicrobial Resistance
Type
Journal article
Publication
Clinical Microbiology and Antimicrobial Chemotherapy. 2012; 14(2):132-152

Abstract

The prevalence and molecular epidemiology of MBLproducing Gram-negative bacteria have been studied in Russia (1998–2010), Belarus and Kazakhstan (2005– 2010). Analysis of nosocomial strains isolated as part of several multicentre surveillance studies in Russia revealed rapid increase in prevalence of MBL-positive Pseudomonas aeruginosa isolates (from 4,5% to 20,3% between 2002–2004 and 2006–2007), which was mainly due to epidemic spread of P. aeruginosa clone ST235 VIM-2. Circulation of this clone was noted across Russia as well as in several cities of Belarus and Kazakhstan. ST235 comprised 96,3% of all (n=711) MBL-producing P. aeruginosa, the remaining isolates belonged to unrelated sequence-types: ST234 (3,4%), ST244 (0,1%) and ST270 (0,1%). Most isolates were susceptible only to polymyxins. In P. aeruginosa, five different types of integrons harbouring the genes for MBLs: VIM-2 (99,6%) and IMP-30, a new Glu59/Lys variant of IMP-1, (0,4%) were found. A likely horizontal transfer of the most prevalent Tn5090-associated integron carrying the blaVIM-2 gene cassette from ST235 to ST234 and ST244 was observed in two cases. In addition to P. aeruginosa, production of MBL (VIM-4) was detected in a single isolate of Escherichia coli.

  • 1. Cornaglia G., Rossolini G.M. The emerging threat of acquired carbapenemases in Gram-negative bacteria. Clin Microbiol Infect 2010; 16(2):99-101.
  • 2. Pfeifer Y., Cullik A., Witte W. Resistance to cephalosporins and carbapenems in Gram-negative bacterial pathogens. Int J Med Microbiol 2010; 300(6):371-9.
  • 3. Miriagou V., Cornaglia G., Edelstein M., et al. Acquired carbapenemases in Gram-negative bacterial pathogens: detection and surveillance issues. Clin Microbiol Infect 2010; 16(2):112-22.
  • 4. Walsh T.R. The emergence and implications of metallobeta-lactamases in Gram-negative bacteria. Clin Microbiol Infect 2005; 11 Suppl 6:2-9.
  • 5. Walsh T.R., Toleman M.A., Poirel L., Nordmann P. Metallo-beta-lactamases: the quiet before the storm? Clin Microbiol Rev 2005; 18(2):306-25.
  • 6. Cornaglia G., Giamarellou H., Rossolini G.M. Metallobeta-lactamases: a last frontier for beta-lactams? Lancet Infect Dis 2011; 11(5):381-93.
  • 7. Biondi S., Long S., Panunzio M., Qin W.L. Current trends in beta-lactam based beta-lactamases inhibitors. Curr Med Chem 2011; 18(27):4223-36.
  • 8. Bush K., Fisher J.F. Epidemiological expansion, structural studies, and clinical challenges of new beta-lactamases from gram-negative bacteria. Annu Rev Microbiol 2011; 65:455-78.
  • 9. Rossolini G.M., Condemi M.A., Pantanella F., Docquier J.D., Amicosante G., Thaller M.C. Metallo-beta-lactamase producers in environmental microbiota: new molecular class B enzyme in Janthinobacterium lividum. Antimicrob Agents Chemother 2001; 45(3):837-44.
  • 10. Livermore D.M. beta-Lactamases in laboratory and clinical resistance. Clin Microbiol Rev 1995; 8(4):557-84.
  • 11. Nordmann P., Naas T., Poirel L. Global spread of Carbapenemase-producing Enterobacteriaceae. Emerg Infect Dis 2011; 17(10):1791-8.
  • 12. El Salabi A., Borra P.S., Toleman M.A., Samuelsen O., Walsh T.R. Genetic and biochemical characterization of a novel metallo-beta-lactamase, TMB-1, from an Achromobacter xylosoxidans strain isolated in Tripoli, Libya. Antimicrob Agents Chemother 2012; 56(5):2241- 5.
  • 13. Nordmann P., Poirel L., Walsh T.R., Livermore D.M. The emerging NDM carbapenemases. Trends Microbiol 2011; 19(12):588-95.
  • 14. Toleman M.A., Spencer J., Jones L., Walsh T.R. blaNDM-1 is a chimera likely constructed in Acinetobacter baumannii. Antimicrob Agents Chemother 2012; 56(5):2773-6.
  • 15. Walsh T.R., Weeks J., Livermore D.M., Toleman M.A. Dissemination of NDM-1 positive bacteria in the New Delhi environment and its implications for human health: an environmental point prevalence study. Lancet Infect Dis 2011; 11(5):355-62.
  • 16. Yong D., Toleman M.A., Giske C.G., et al. Characterization of a new metallo-beta-lactamase gene, bla(NDM-1), and a novel erythromycin esterase gene carried on a unique genetic structure in Klebsiella pneumoniae sequence type 14 from India. Antimicrob Agents Chemother 2009; 53(12):5046-54.
  • 17. Silva F.M., Carmo M.S., Silbert S., Gales A.C. SPM1-producing Pseudomonas aeruginosa: analysis of the ancestor relationship using multilocus sequence typing, pulsed-field gel electrophoresis, and automated ribotyping. Microb Drug Resist 2011; 17(2):215-20.
  • 18. Antoniadou A., Kontopidou F., Poulakou G., et al. Colistin-resistant isolates of Klebsiella pneumoniae emerging in intensive care unit patients: first report of a multiclonal cluster. J Antimicrob Chemother 2007; 59(4):786-90.
  • 19. Livermore D.M., Warner M., Mushtaq S., Doumith M., Zhang J., Woodford N. What remains against carbapenem-resistant Enterobacteriaceae? Evaluation of chloramphenicol, ciprofloxacin, colistin, fosfomycin, minocycline, nitrofurantoin, temocillin and tigecycline. Int J Antimicrob Agents 2011; 37(5):415-9.
  • 20. EUCAST Breakpoint tables for interpretation of MICs and zone diameters. Breakpoint tables for interpretation of MICs and zone diameters. Version 2.0. 2012:1-73.
  • 21. Определение чувствительности микроорганизмов к антибактериальным препаратам (Методические указания МУК 4.2.1890_04). Клин микробиол антимикроб химиотер 2004; 6(4):307-59.
  • 22. EUCAST Breakpoint tables for interpretation of MICs and zone diameters. Breakpoint tables for interpretation of MICs and zone diameters. Version 1.3. 2011:1-73.
  • 23. CLSI Performance standards for antimicrobial susceptibility testing; 21st informational supplement. 2011; (31):165.
  • 24. Шевченко О.В., Эйдельштейн М.В., Степанова М.Н. Металло-β-лактамазы: значение и методы выявления у грамотрицательных неферментирующих бактерий. Клин микробиол антимикроб химиотер 2007; 9(3):211-8.
  • 25. Woodford N., Tierno P.M., Jr., Young K., et al. Outbreak of Klebsiella pneumoniae producing a new carbapenemhydrolyzing class A beta-lactamase, KPC-3, in a New York Medical Center. Antimicrob Agents Chemother 2004; 48(12):4793-9.
  • 26. Tsafnat G., Coiera E., Partridge S.R., Schaeffer J., Iredell J.R. Context-driven discovery of gene cassettes in mobile integrons using a computational grammar. BMC Bioinformatics 2009; 10:281.
  • 27. Partridge S.R., Tsafnat G., Coiera E., Iredell J.R. Gene cassettes and cassette arrays in mobile resistance integrons. FEMS Microbiol Rev 2009; 33(4):757-84.
  • 28. Onteniente L., Brisse S., Tassios P.T., Vergnaud G. Evaluation of the polymorphisms associated with tandem repeats for Pseudomonas aeruginosa strain typing. J Clin Microbiol 2003; 41(11):4991-7.
  • 29. Shevchenko O., Edelstein M. Application of fluorescent MLVA for molecular typing of MBL-producing Pseudomonas aeruginosa strains. 8th International Meeting on Microbial Epidemiological Markers; 2008 May; Zakopane, Poland.
  • 30. DeWoody J.A., Schupp J., Kenefic L., Busch J., Murfitt L., Keim P. Universal method for producing ROXlabeled size standards suitable for automated genotyping. Biotechniques 2004; 37(3):348, 50, 52.
  • 31. Curran B., Jonas D., Grundmann H., Pitt T., Dowson C.G. Development of a multilocus sequence typing scheme for the opportunistic pathogen Pseudomonas aeruginosa. J Clin Microbiol 2004; 42(12):5644-9.
  • 32. Galleni M., Lamotte-Brasseur J., Rossolini G.M., Spencer J., Dideberg O., Frere J.M. Standard numbering scheme for class B beta-lactamases. Antimicrob Agents Chemother 2001; 45(3):660-3.
  • 33. Lolans K., Queenan A.M., Bush K., Sahud A., Quinn J.P. First nosocomial outbreak of Pseudomonas aeruginosa producing an integron-borne metallo-beta-lactamase (VIM-2) in the United States. Antimicrob Agents Chemother 2005; 49(8):3538-40.
  • 34. Tseng S.P., Tsai J.C., Teng L.J., Hsueh P.R. Dissemination of transposon Tn6001 in carbapenem-non-susceptible and extensively drug-resistant Pseudomonas aeruginosa in Taiwan. J Antimicrob Chemother 2009; 64(6):1170-4.
  • 35. Samuelsen O., Buaro L., Toleman M.A., et al. The first metallo-beta-lactamase identified in norway is associated with a TniC-like transposon in a Pseudomonas aeruginosa isolate of sequence type 233 imported from Ghana. Antimicrob Agents Chemother 2009; 53(1):331-2.
  • 36. Perez F., Hujer A.M., Hujer K.M., Decker B.K., Rather P.N., Bonomo R.A. Global challenge of multidrugresistant Acinetobacter baumannii. Antimicrob Agents Chemother 2007; 51(10):3471-84.
  • 37. Cagnacci S., Gualco L., Roveta S., et al. Bloodstream infections caused by multidrug-resistant Klebsiella pneumoniae producing the carbapenem-hydrolysing VIM-1 metallo-beta-lactamase: first Italian outbreak. J Antimicrob Chemother 2008; 61(2):296-300.
  • 38. Canton R., Akova M., Carmeli Y., et al. Rapid evolution and spread of carbapenemases among Enterobacteriaceae in Europe. Clin Microbiol Infect 2012; 18(5):413-31.
  • 39. Rossolini G.M., Luzzaro F., Migliavacca R., et al. First countrywide survey of acquired metallo-beta-lactamases in gram-negative pathogens in Italy. Antimicrob Agents Chemother 2008; 52(11):4023-9.
  • 40. Tato M., Coque T.M., Ruiz-Garbajosa P., et al. Complex clonal and plasmid epidemiology in the first outbreak of Enterobacteriaceae infection involving VIM-1 metallobeta-lactamase in Spain: toward endemicity? Clin Infect Dis 2007; 45(9):1171-8.
  • 41. Vatopoulos A. High rates of metallo-beta-lactamaseproducing Klebsiella pneumoniae in Greece – a review of the current evidence. Euro Surveill 2008; 13(4).
  • 42. Psichogiou M., Tassios P.T., Avlamis A., et al. Ongoing epidemic of blaVIM-1-positive Klebsiella pneumoniae in Athens, Greece: a prospective survey. J Antimicrob Chemother 2008; 61(1):59-63.
  • 43. Giske C.G., Froding I., Hasan C.M., et al. Diverse Sequence Types of Klebsiella pneumoniae Contribute to the Dissemination of blaNDM-1 in India, Sweden, and the United Kingdom. Antimicrob Agents Chemother 2012; 56(5):2735-8.
  • 44. Rolain J.M., Parola P., Cornaglia G. New Delhi metallobeta-lactamase (NDM-1): towards a new pandemia? Clin Microbiol Infect 2010; 16(12):1699-701.
  • 45. Walsh T.R., Toleman M.A. The new medical challenge: why NDM-1? Why Indian? Expert Rev Anti Infect Ther 2011; 9(2):137-41.
  • 46. Livermore D.M., Walsh T.R., Toleman M., Woodford N. Balkan NDM-1: escape or transplant? Lancet Infect Dis 2011; 11(3):164.
  • 47. Martinovich A., Shevchenko O., Edelstein M., Kozlov R. Assessment of carbapenem resistance and presence of acquired carbapenemases in Russian nosocomial isolates of Acinetobacter spp. 18th European Congress of Clinical Microbiology and Infectious Diseases; 2008 April; Barcelona, Spain.
  • 48. Martinovich A., Edelstein M., Kozlov R. Multilocus sequence typing of Acinetobacter strains from Russia and Belarus that produce acquired OXA carbapenemases. 49th Interscience Conference on Antimicrobial Agents and Chemotherapy; 2009 September; San Francisco, CA, USA.
  • 49. Colinon C., Miriagou V., Carattoli A., Luzzaro F., Rossolini G.M. Characterization of the IncA/C plasmid pCC416 encoding VIM-4 and CMY-4 beta-lactamases. J Antimicrob Chemother 2007; 60(2):258-62.
  • 50. Drieux L., Bourgeois-Nicolaos N., Cremniter J., et al. Accumulation of carbapenemase-producing Gramnegative bacteria in a single patient linked to the acquisition of multiple carbapenemase producers and to the in vivo transfer of a plasmid encoding VIM-1. Int J Antimicrob Agents 2011; 38(2):179-80.
  • 51. Kassis-Chikhani N., Decre D., Gautier V., et al. First outbreak of multidrug-resistant Klebsiella pneumoniae carrying blaVIM-1 and blaSHV-5 in a French university hospital. J Antimicrob Chemother 2006; 57(1):142-5.
  • 52. Ktari S., Arlet G., Mnif B., et al. Emergence of multidrugresistant Klebsiella pneumoniae isolates producing VIM-4 metallo-beta-lactamase, CTX-M-15 extended-spectrum beta-lactamase, and CMY-4 AmpC beta-lactamase in a Tunisian university hospital. Antimicrob Agents Chemother 2006; 50(12):4198-201.
  • 53. Loli A., Tzouvelekis L.S., Tzelepi E., et al. Sources of diversity of carbapenem resistance levels in Klebsiella pneumoniae carrying blaVIM-1. J Antimicrob Chemother 2006; 58(3):669-72.
  • 54. Miriagou V., Carattoli A., Tzelepi E., Villa L., Tzouvelekis L.S. IS26-associated In4-type integrons forming multiresistance loci in enterobacterial plasmids. Antimicrob Agents Chemother 2005; 49(8):3541-3.
  • 55. Miriagou V., Papagiannitsis C.C., Kotsakis S.D., et al. Sequence of pNL194, a 79.3-kilobase IncN plasmid carrying the blaVIM-1 metallo-beta-lactamase gene in Klebsiella pneumoniae. Antimicrob Agents Chemother 2010; 54(10):4497-502.
  • 56. Samuelsen O., Toleman M.A., Hasseltvedt V., et al. Molecular characterization of VIM-producing Klebsiella pneumoniae from Scandinavia reveals genetic relatedness with international clonal complexes encoding transferable multidrug resistance. Clin Microbiol Infect 2011; 17(12):1811-6.
  • 57. Ikonomidis A., Spanakis N., Poulou A., Pournaras S., Markou F., Tsakris A. Emergence of carbapenemresistant Enterobacter cloacae carrying VIM-4 metallobeta-lactamase and SHV-2a extended-spectrum betalactamase in a conjugative plasmid. Microb Drug Resist 2007; 13(4):221-6.
  • 58. Shevchenko O.V., Mudrak D.Y., Skleenova E.Y., et al. First detection of VIM-4 metallo-beta-lactamaseproducing Escherichia coli in Russia. Clin Microbiol Infect 2012.
  • 59. Stratchounski L., Kretchikov V., Edelshtein I., Kozlova I., Edelshtein M. First report of metallo-betalactamase production in P. aeruginosa strains isolated in different regions of Russia. 6th European Congress of Chemotherapy and Infection/24th Interdisciplinary Meeting of Anti-Infection Chemotherapy; 2004 December; Paris, France.
  • 60. Gutierrez O., Juan C., Cercenado E., et al. Molecular epidemiology and mechanisms of carbapenem resistance in Pseudomonas aeruginosa isolates from Spanish hospitals. Antimicrob Agents Chemother 2007; 51(12):4329-35.
  • 61. Giakkoupi P., Petrikkos G., Tzouvelekis L.S., Tsonas S., Legakis N.J., Vatopoulos A.C. Spread of integronassociated VIM-type metallo-beta-lactamase genes among imipenem-nonsusceptible Pseudomonas aeruginosa strains in Greek hospitals. J Clin Microbiol 2003; 41(2):822-5.
  • 62. Kimura S., Alba J., Shiroto K., et al. Clonal diversity of metallo-beta-lactamase-possessing Pseudomonas aeruginosa in geographically diverse regions of Japan. J Clin Microbiol 2005; 43(1):458-61.
  • 63. Lee K., Lim C.H., Cho J.H., et al. High prevalence of ceftazidime-resistant Klebsiella pneumoniae and increase of imipenem-resistant Pseudomonas aeruginosa and Acinetobacter spp. in Korea: a KONSAR program in 2004. Yonsei Med J 2006; 47(5):634-45.
  • 64. Lee K., Park A.J., Kim M.Y., et al. Metallo-beta-lactamaseproducing Pseudomonas spp. in Korea: high prevalence of isolates with VIM-2 type and emergence of isolates with IMP-1 type. Yonsei Med J 2009; 50(3):335-9.
  • 65. Castanheira M., Bell J.M., Turnidge J.D., Mathai D., Jones R.N. Carbapenem resistance among Pseudomonas aeruginosa strains from India: evidence for nationwide endemicity of multiple metallo-beta-lactamase clones (VIM-2, -5, -6, and -11 and the newly characterized VIM18). Antimicrob Agents Chemother 2009; 53(3):1225-7.
  • 66. Черкашин Е.А., Федорчук В.В., Иванов Д.В., Сидоренко С.В., Тишков В.И. Исследование распространенности метало-бета-лактамаз в Российской Федерации. Вестн Моск Унив (Химия) 2006; 47(3):83-6.
  • 67. Кузнецова М.В., Карпунина Т.И., Егорова Д.О., Плотникова Е.Г., Демаков В.А. Карбапенемоустойчивые штаммы Pseudomonas aeruginosa в стационарах города Пермь. Клин микробиол антимикроб химиотер 2010; 12(3):246-52.
  • 68. Giske C.G., Libisch B., Colinon C., et al. Establishing clonal relationships between VIM-1-like metallo-betalactamase-producing Pseudomonas aeruginosa strains from four European countries by multilocus sequence typing. J Clin Microbiol 2006; 44(12):4309-15.
  • 69. Maatallah M., Cheriaa J., Backhrouf A., et al. Population structure of Pseudomonas aeruginosa from five Mediterranean countries: evidence for frequent recombination and epidemic occurrence of CC235. PLoS One 2011; 6(10):e25617.
  • 70. Nemec A., Krizova L., Maixnerova M., Musilek M. Multidrug-resistant epidemic clones among bloodstream isolates of Pseudomonas aeruginosa in the Czech Republic. Res Microbiol 2010; 161(3):234-42.
  • 71. Woodford N., Turton J.F., Livermore D.M. Multiresistant Gram-negative bacteria: the role of high-risk clones in the dissemination of antibiotic resistance. FEMS Microbiol Rev 2011; 35(5):736-55.
  • 72. Lauretti L., Riccio M.L., Mazzariol A., et al. Cloning and characterization of blaVIM, a new integron-borne metallobeta-lactamase gene from a Pseudomonas aeruginosa clinical isolate. Antimicrob Agents Chemother 1999; 43(7):1584-90.
  • 73. Samuelsen O., Toleman M.A., Sundsfjord A., et al. Molecular epidemiology of metallo-beta-lactamaseproducing Pseudomonas aeruginosa isolates from Norway and Sweden shows import of international clones and local clonal expansion. Antimicrob Agents Chemother 2010; 54(1):346-52.
  • 74. Libisch B., Watine J., Balogh B., et al. Molecular typing indicates an important role for two international clonal complexes in dissemination of VIM-producing Pseudomonas aeruginosa clinical isolates in Hungary. Res Microbiol 2008; 159(3):162-8.
  • 75. Lepsanovic Z., Libisch B., Tomanovic B., Nonkovici Z., Balogh B., Fuzi M. Characterisation of the first VIM metallo-beta-lactamase-producing Pseudomonas aeruginosa clinical isolate in Serbia. Acta Microbiol Immunol Hung 2008; 55(4):447-54.
  • 76. Juan C., Zamorano L., Mena A., Alberti S., Perez J.L., Oliver A. Metallo-beta-lactamase-producing Pseudomonas putida as a reservoir of multidrug resistance elements that can be transferred to successful Pseudomonas aeruginosa clones. J Antimicrob Chemother 2010; 65(3):474-8.
  • 77. Kitao T., Tada T., Tanaka M., et al. Emergence of a novel multidrug-resistant Pseudomonas aeruginosa strain producing IMP-type metallo-beta-lactamases and AAC(6’)-Iae in Japan. Int J Antimicrob Agents 2012; 39(6):518-21.
  • 78. Kouda S., Ohara M., Onodera M., et al. Increased prevalence and clonal dissemination of multidrugresistant Pseudomonas aeruginosa with the blaIMP-1 gene cassette in Hiroshima. J Antimicrob Chemother 2009; 64(1):46-51.
  • 79. Glupczynski Y., Bogaerts P., Deplano A., et al. Detection and characterization of class A extended-spectrum-betalactamase-producing Pseudomonas aeruginosa isolates in Belgian hospitals. J Antimicrob Chemother 2010; 65(5):866-71.
  • 80. Koh T.H., Khoo C.T., Tan T.T., et al. Multilocus sequence types of carbapenem-resistant Pseudomonas aeruginosa in Singapore carrying metallo-beta-lactamase genes, including the novel bla(IMP-26) gene. J Clin Microbiol 2010; 48(7):2563-4.
  • 81. Seok Y., Bae I.K., Jeong S.H., Kim S.H., Lee H., Lee K. Dissemination of IMP-6 metallo-beta-lactamaseproducing Pseudomonas aeruginosa sequence type 235 in Korea. J Antimicrob Chemother 2011; 66(12):2791-6.
  • 82. Sardelic S., Bedenic B., Colinon-Dupuich C., et al. Infrequent Finding of Metallo-beta-Lactamase VIM-2 in Carbapenem-Resistant Pseudomonas aeruginosa Strains from Croatia. Antimicrob Agents Chemother 2012; 56(5):2746-9.
  • 83. Cholley P., Thouverez M., Hocquet D., van der MeeMarquet N., Talon D., Bertrand X. Most multidrugresistant Pseudomonas aeruginosa isolates from hospitals in eastern France belong to a few clonal types. J Clin Microbiol 2011; 49(7):2578-83.
  • 84. Danel F., Hall L.M., Duke B., Gur D., Livermore D.M. OXA-17, a further extended-spectrum variant of OXA10 beta-lactamase, isolated from Pseudomonas aeruginosa. Antimicrob Agents Chemother 1999; 43(6):1362-6.
  • 85. Danel F., Hall L.M., Gur D., Akalin H.E., Livermore D.M. Transferable production of PER-1 beta-lactamase in Pseudomonas aeruginosa. J Antimicrob Chemother 1995; 35(2):281-94.
  • 86. Empel J., Filczak K., Mrowka A., Hryniewicz W., Livermore D.M., Gniadkowski M. Outbreak of Pseudomonas aeruginosa infections with PER-1 extended-spectrum beta-lactamase in Warsaw, Poland: further evidence for an international clonal complex. J Clin Microbiol 2007; 45(9):2829-34.
  • 87. Libisch B., Poirel L., Lepsanovic Z., et al. Identification of PER-1 extended-spectrum beta-lactamase producing Pseudomonas aeruginosa clinical isolates of the international clonal complex CC11 from Hungary and Serbia. FEMS Immunol Med Microbiol 2008; 54(3):330- 8.
  • 88. Viedma E., Juan C., Acosta J., et al. Nosocomial spread of colistin-only-sensitive sequence type 235 Pseudomonas aeruginosa isolates producing the extended-spectrum beta-lactamases GES-1 and GES-5 in Spain. Antimicrob Agents Chemother 2009; 53(11):4930-3.
  • 89. Toleman M.A., Vinodh H., Sekar U., Kamat V., Walsh T.R. blaVIM-2-harboring integrons isolated in India, Russia, and the United States arise from an ancestral class 1 integron predating the formation of the 3’ conserved sequence. Antimicrob Agents Chemother 2007; 51(7):2636-8.
  • 90. Lee J.Y., Song J.H., Ko K.S. Identification of nonclonal Pseudomonas aeruginosa isolates with reduced colistin susceptibility in Korea. Microb Drug Resist 2011; 17(2):299-304.
Views
0 Abstract
0 PDF
0 Crossref citations
Shared