How to detect carbapenemase producers? A literature review of phenotypic and molecular methods

Journal of Microbiological Methods

Volumn 107, Issue , 2014, Pages 106-118

  Hammoudi, D ^a,b   Ayoub Moubareck, C ^a,b,c   Karam Sarkis, D ^a,b  

^a SAINT JOSEPH UNIVERSITY   (Lebanon)

^b Rodolph Merieux Laboratory   (Lebanon)

^c ZAYED UNIVERSITY   (United Arab Emirates)

Author keywords

Carbapenemases; Detection; Molecular methods; Phenotypic methods; Screening

Indexed keywords

1,10 PHENANTHROLINE; 2 MERCAPTOPROPIONIC ACID; BETA LACTAM ANTIBIOTIC; BORONIC ACID DERIVATIVE; CARBAPENEM; CARBAPENEMASE; CEFOTAXIME; CEFTAZIDIME; CEFTRIAXONE; CEPHALOSPORIN DERIVATIVE; CLAVULANIC ACID; CLOXACILLIN; DIPICOLINIC ACID; DORIPENEM; EDETIC ACID; ERTAPENEM; IMIPENEM; MEROPENEM; PENICILLIN DERIVATIVE; PROPIONIC ACID DERIVATIVE; SODIUM MERCAPTOACETIC ACID; SULBACTAM; TAZOBACTAM; THIOGLYCOLIC ACID; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; BETA LACTAMASE;

AGAR MEDIUM; ANALYTIC METHOD; ANTIBIOTIC SENSITIVITY; BIOCHEMISTRY; CARBA NP TEST; CARBAPENEMASE PRODUCING ENTEROBACTERIACEAE; COMBINED DISC TEST; CULTURE MEDIUM; CULTURE TECHNIQUE; DOUBLE DISC SYNERGY TEST; ENZYME ANALYSIS; ENZYME INHIBITION ASSAY; EPSILOMETER TEST; GENE IDENTIFICATION; GENE SEQUENCE; IMMUNOAFFINITY CHROMATOGRAPHY; ISOELECTRIC FOCUSING; MASS SPECTROMETRY; MODIFIED HODGE TEST; MOLECULAR CLONING; MOLECULAR GENETICS; MULTILOCUS SEQUENCE TYPING; NONHUMAN; PHENOTYPE; POLYMERASE CHAIN REACTION; REVIEW; ULTRAVIOLET SPECTROPHOTOMETRY; ANTIBIOTIC RESISTANCE; CHEMICAL ANALYSIS; DRUG SCREENING; GENETICS; HUMAN; META ANALYSIS; MICROBIAL SENSITIVITY TEST; MOLECULAR TYPING; PROCEDURES;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BETA-LACTAM RESISTANCE; BETA-LACTAMASES; CHEMISTRY TECHNIQUES, ANALYTICAL; DRUG EVALUATION, PRECLINICAL; HUMANS; MICROBIAL SENSITIVITY TESTS; MOLECULAR TYPING;

EID: 84908620706     PISSN: 01677012     EISSN: 18728359     Source Type: Journal    
DOI: 10.1016/j.mimet.2014.09.009     Document Type: Review

References (123)

1. Abbott I., Cerqueira G.M., et al. Carbapenem resistance in Acinetobacter baumannii: laboratory challenges, mechanistic insights and therapeutic strategies. Expert Rev. Anti-Infect. Ther. 2013, 11(4):395-409.
2. Adler A., Navon-Venezia S., et al. Laboratory and clinical evaluation of screening agar plates for detection of carbapenem-resistant Enterobacteriaceae from surveillance rectal swabs. J. Clin. Microbiol. 2011, 49(6):2239-2242.
3. Alvarez-Buylla A., Picazo J.J., et al. Optimized method for Acinetobacter species carbapenemase detection and identification by matrix-assisted laser desorption ionization-time of flight mass spectrometry. J. Clin. Microbiol. 2013, 51(5):1589-1592.
4. Ambretti S., Gaibani P., Berlingeri A., Cordovana M., Tamburini M.V., Bau G., Landini M.P., Sambri V. Evaluation of phenotypic and genotypic approaches for the detection of class A and class B carbapenemasescin Enterobacteriaceae. Microb. Drug Resist. 2013, 19(3):212-215.
5. Anderson K.F., Lonsway D.R., et al. Evaluation of methods to identify the Klebsiella pneumoniae carbapenemase in Enterobacteriaceae. J. Clin. Microbiol. 2007, 45(8):2723-2725.
6. Avlami A., Bekris S., et al. Detection of metallo-beta-lactamase genes in clinical specimens by a commercial multiplex PCR system. J. Microbiol. Methods 2010, 83(2):185-187.
7. Bernabeu S., Poirel L., et al. Spectrophotometry-based detection of carbapenemase producers among Enterobacteriaceae. Diagn. Microbiol. Infect. Dis. 2012, 74(1):88-90.
8. Bogaerts P., Bebrone C., et al. Detection and characterization of VIM-31, a new variant of VIM-2 with Tyr224His and His252Arg mutations, in a clinical isolate of Enterobacter cloacae. Antimicrob. Agents Chemother. 2012, 56(6):3283-3287.
9. Bracco S., Migliavacca R., et al. Evaluation of brilliance CRE agar for the detection of carbapenem-resistant Gram-negative bacteria. New Microbiol. 2013, 36(2):181-186.
10. Bratu S., Landman D., et al. Detection of KPC carbapenem-hydrolyzing enzymes in Enterobacter spp. from Brooklyn, New York. Antimicrob. Agents Chemother. 2005, 49(2):776-778.
11. Bratu S., Mooty M., et al. Emergence of KPC-possessing Klebsiella pneumoniae in Brooklyn, New York: epidemiology and recommendations for detection. Antimicrob. Agents Chemother. 2005, 49(7):3018-3020.
12. Carrer A., Fortineau N., et al. Use of ChromID extended-spectrum beta-lactamase medium for detecting carbapenemase-producing Enterobacteriaceae. J. Clin. Microbiol. 2010, 48(5):1913-1914.
13. Chen C.M., Cui S.J. Detection of porcine parvovirus by loop-mediated isothermal amplification. J. Virol. Methods 2009, 155(2):122-125.
14. Chu Y.W., Cheung T.K., et al. EDTA susceptibility leading to false detection of metallo-beta-lactamase in Pseudomonas aeruginosa by Etest and an imipenem-EDTA disk method. Int. J. Antimicrob. Agents 2005, 26(4):340-341.
15. CLSI Performance Standards for Antimicrobial Suceptibility Testing: Twenty-first Informational Supplement 2014, (Wayne, PA, USA).
16. Cohen Stuart J., Leverstein-Van Hall M.A. Guideline for phenotypic screening and confirmation of carbapenemases in Enterobacteriaceae. Int. J. Antimicrob. Agents 2010, 36(3):205-210.
17. Cohen Stuart J., Voets G., Rottier W., Voskuil S., Scharringa J., Van Dijk K., Fluit A.C., Leverstein-Van Hall M. Evaluation of the Oxoid Brillance™ CRE agar for the detection of carbapenemase-producing Enterobacteriaceae. Eur. J. Clin. Microbiol. Infect. Dis. 2013, 32(11):1445-1449.
18. Cunningham S.A., Noorie T., et al. Rapid and simultaneous detection of genes encoding Klebsiella pneumoniae carbapenemase (blaKPC) and New Delhi metallo-beta-lactamase (blaNDM) in Gram-negative bacilli. J. Clin. Microbiol. 2013, 51(4):1269-1271.
19. Dahmen S., Mansour W., et al. Imipenem resistance in Klebsiella pneumoniae is associated to the combination of plasmid-mediated CMY-4 AmpC beta-lactamase and loss of an outer membrane protein. Microb. Drug Resist. 2012, 18(5):479-483.
20. Dallenne C., Da Costa A., et al. Development of a set of multiplex PCR assays for the detection of genes encoding important beta-lactamases in Enterobacteriaceae. J. Antimicrob. Chemother. 2010, 65(3):490-495.
21. Deshpande L.M., Jones R.N., et al. Occurrence and characterization of carbapenemase-producing Enterobacteriaceae: report from the SENTRY Antimicrobial Surveillance Program (2000-2004). Microb. Drug Resist. 2006, 12(4):223-230.
22. Dortet L., Poirel L., et al. Rapid detection of carbapenemase-producing Pseudomonas spp. J. Clin. Microbiol. 2012, 50(11):3773-3776.
23. Dortet L., Poirel L., et al. CarbAcineto NP Test for rapid detection of carbapenemase-producing Acinetobacter spp. J. Clin. Microbiol. 2014, 52(7):2359-2364.
24. El-Herte R.I., Kanj S.S., et al. The threat of carbapenem-resistant Enterobacteriaceae in Lebanon: an update on the regional and local epidemiology. J. Infect. Public Health 2012, 5(3):233-243.
25. Empel J., Filczak K., et al. 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):2829-2834.
26. EUCAST, E.c.o.a.s.t. Breakpoint Tables for Interpretation of MICs and Zone Diameters 2014.
27. Falagas M.E., Karageorgopoulos D.E., et al. Therapeutic options for infections with Enterobacteriaceae producing carbapenem-hydrolyzing enzymes. Future Microbiol 2011, 6(6):653-666.
28. Ferreira A.E., Marchetti D.P., et al. Molecular characterization of clinical multiresistant isolates of Acinetobacter sp. from hospitals in Porto Alegre, State of Rio Grande do Sul, Brazil. Rev. Soc. Bras. Med. Trop. 2011, 44(6):725-730.
29. Gazin M., Paasch F., et al. Current trends in culture-based and molecular detection of extended-spectrum-beta-lactamase-harboring and carbapenem-resistant Enterobacteriaceae. J. Clin. Microbiol. 2012, 50(4):1140-1146.
30. Giakkoupi P., Tzouvelekis L.S., et al. Discrepancies and interpretation problems in susceptibility testing of VIM-1-producing Klebsiella pneumoniae isolates. J. Clin. Microbiol. 2005, 43(1):494-496.
31. 2+ facilitates detection of VIM-2-producing Pseudomonas aeruginosa. J. Clin. Microbiol. 2008, 46(4):1568-1569.
32. Giakkoupi P., Pappa O., et al. Emerging Klebsiella pneumoniae isolates coproducing KPC-2 and VIM-1 carbapenemases. Antimicrob. Agents Chemother. 2009, 53(9):4048-4050.
33. Girlich D., Naas T., et al. Biochemical-genetic characterization and regulation of expression of an ACC-1-like chromosome-borne cephalosporinase from Hafnia alvei. Antimicrob. Agents Chemother. 2000, 44(6):1470-1478.
34. Girlich D., Poirel L., et al. Value of the modified Hodge test for detection of emerging carbapenemases in Enterobacteriaceae. J. Clin. Microbiol. 2012, 50(2):477-479.
35. Girlich D., Poirel L., et al. Comparison of the SUPERCARBA, CHROMagar KPC, and Brilliance CRE screening media for detection of Enterobacteriaceae with reduced susceptibility to carbapenems. Diagn. Microbiol. Infect. Dis. 2013, 75(2):214-217.
36. Giske C.G., Gezelius L., et al. A sensitive and specific phenotypic assay for detection of metallo-beta-lactamases and KPC in Klebsiella pneumoniae with the use of meropenem disks supplemented with aminophenylboronic acid, dipicolinic acid and cloxacillin. Clin. Microbiol. Infect. 2011, 17(4):552-556.
37. Gordon N.C., Wareham D.W. Evaluation of CHROMagar Acinetobacter for detection of enteric carriage of multidrug-resistant Acinetobacter baumannii in samples from critically ill patients. J. Clin. Microbiol. 2009, 47(7):2249-2251.
38. Gutierrez O., Juan C., et al. Molecular epidemiology and mechanisms of carbapenem resistance in Pseudomonas aeruginosa isolates from Spanish hospitals. Antimicrob. Agents Chemother. 2007, 51(12):4329-4335.
39. Hawkey P.M., Livermore D.M. Carbapenem antibiotics for serious infections. BMJ 2012, 344:e3236.
40. Hodge W., Ciak J., et al. Simple method for detection of penicillinase-producing Neisseria gonorrhoeae. J. Clin. Microbiol. 1978, 7(1):102-103.
41. Hornstein M., Sautjeau-Rostoker C., et al. Oxacillin-hydrolyzing beta-lactamase involved in resistance to imipenem in Acinetobacter baumannii. FEMS Microbiol. Lett. 1997, 153(2):333-339.
42. Hrabak J., Walkova R., et al. Carbapenemase activity detection by matrix-assisted laser desorption ionization-time of flight mass spectrometry. J. Clin. Microbiol. 2011, 49(9):3222-3227.
43. Hrabak J., Chudackova E., et al. Matrix-assisted laser desorption ionization-time of flight (MALDI-TOF) mass spectrometry for detection of antibiotic resistance mechanisms: from research to routine diagnosis. Clin. Microbiol. Rev. 2013, 26(1):103-114.
44. Ikonomidis A., Ntokou E., et al. Hidden VIM-1 metallo-beta-lactamase phenotypes among Acinetobacter baumannii clinical isolates. J. Clin. Microbiol. 2008, 46(1):346-349.
45. Ito H., Arakawa Y., et al. Plasmid-mediated dissemination of the metallo-beta-lactamase gene blaIMP among clinically isolated strains of Serratia marcescens. Antimicrob. Agents Chemother. 1995, 39(4):824-829.
46. Jacoby G.A. AmpC beta-lactamases. Clin. Microbiol. Rev. 2009, 22(1):161-182. (Table of Contents).
47. Kanj S.S., Kanafani Z.A. Current concepts in antimicrobial therapy against resistant Gram-negative organisms: extended-spectrum beta-lactamase-producing Enterobacteriaceae, carbapenem-resistant Enterobacteriaceae, and multidrug-resistant Pseudomonas aeruginosa. Mayo Clin. Proc. 2011, 86(3):250-259.
48. Karah N., Giske C.G., et al. A diversity of OXA-carbapenemases and class 1 integrons among carbapenem-resistant Acinetobacter baumannii clinical isolates from Sweden belonging to different international clonal lineages. Microb. Drug Resist. 2011, 17(4):545-549.
49. Kitao T., Miyoshi-Akiyama T., et al. Development of an immunochromatographic assay for diagnosing the production of IMP-type metallo-beta-lactamases that mediate carbapenem resistance in Pseudomonas. J. Microbiol. Methods 2011, 87(3):330-337.
50. Koivunen M.E., Krogsrud R.L. Principles of immunochemical techniques used in clinical laboratories. Lab. Med. 2006, 37(8):8.
51. Kulkarni M.V., Zurita A.N., et al. Use of Imipenem to detect KPC, NDM, OXA, IMP, and VIM carbapenemase activity from Gram-negative rods in 75 minutes using liquid chromatography-tandem mass spectrometry. J. Clin. Microbiol. 2014, 52(7):2500-2505.
52. Lee K., Chong Y., et al. Modified Hodge and EDTA-disk synergy tests to screen metallo-beta-lactamase-producing strains of Pseudomonas and Acinetobacter species. Clin. Microbiol. Infect. 2001, 7(2):88-91.
53. Lee K., Lim J.B., et al. bla(VIM-2) cassette-containing novel integrons in metallo-beta-lactamase-producing Pseudomonas aeruginosa and Pseudomonas putida isolates disseminated in a Korean hospital. Antimicrob. Agents Chemother. 2002, 46(4):1053-1058.
54. Lee K., Lim Y.S., et al. Evaluation of the Hodge test and the imipenem-EDTA double-disk synergy test for differentiating metallo-beta-lactamase-producing isolates of Pseudomonas spp. and Acinetobacter spp. J. Clin. Microbiol. 2003, 41(10):4623-4629.
55. Lee K., Kim C.K., et al. Improved performance of the modified Hodge test with MacConkey agar for screening carbapenemase-producing Gram-negative bacilli. J. Microbiol. Methods 2010, 83(2):149-152.
56. Libisch B., Watine J., 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):162-168.
57. Livermore D.M., Woodford N. The beta-lactamase threat in Enterobacteriaceae, Pseudomonas and Acinetobacter. Trends Microbiol. 2006, 14(9):413-420.
58. Loli A., Tzouvelekis L.S., et al. Outbreak of Acinetobacter baumannii with chromosomally encoded VIM-1 undetectable by imipenem-EDTA synergy tests. Antimicrob. Agents Chemother. 2008, 52(5):1894-1896.
59. Mammeri H., Eb F., et al. Molecular characterization of AmpC-producing Escherichia coli clinical isolates recovered in a French hospital. J. Antimicrob. Chemother. 2008, 61(3):498-503.
60. Mathew A., Harris A.M., et al. The use of analytical isoelectric focusing for detection and identification of beta-lactamases. J. Gen. Microbiol. 1975, 88(1):169-178.
61. Meric M., Kasap M., et al. Emergence and spread of carbapenem-resistant Acinetobacter baumannii in a tertiary care hospital in Turkey. FEMS Microbiol. Lett. 2008, 282(2):214-218.
62. Merlino J., Siarakas S., et al. Evaluation of CHROMagar Orientation for differentiation and presumptive identification of Gram-negative bacilli and Enterococcus species. J. Clin. Microbiol. 1996, 34(7):1788-1793.
63. Miriagou V., Cornaglia G., et al. Acquired carbapenemases in Gram-negative bacterial pathogens: detection and surveillance issues. Clin. Microbiol. Infect. 2010, 16(2):112-122.
64. Moran Gilad J., Carmeli Y., et al. Laboratory evaluation of the CHROMagar KPC medium for identification of carbapenem-nonsusceptible Enterobacteriaceae. Diagn. Microbiol. Infect. Dis. 2011, 70(4):565-567.
65. Moubareck C., Bremont S., et al. GES-11, a novel integron-associated GES variant in Acinetobacter baumannii. Antimicrob. Agents Chemother. 2009, 53(8):3579-3581.
66. Mugnier P., Poirel L., et al. Carbapenem-resistant and OXA-23-producing Acinetobacter baumannii isolates in the United Arab Emirates. Clin. Microbiol. Infect. 2008, 14(9):879-882.
67. Naas T., Nordmann P. Analysis of a carbapenem-hydrolyzing class A beta-lactamase from Enterobacter cloacae and of its LysR-type regulatory protein. Proc. Natl. Acad. Sci. U. S. A. 1994, 91(16):7693-7697.
68. Nakano R., Okamoto R., et al. CFE-1, a novel plasmid-encoded AmpC beta-lactamase with an ampR gene originating from Citrobacter freundii. Antimicrob. Agents Chemother. 2004, 48(4):1151-1158.
69. Nordmann P. Résistance aux carbapénèmes chez les bacilles à Gram négatif. Med./Sci. 2010, 26:950-959.
70. Nordmann P., Poirel L. Strategies for identification of carbapenemase-producing Enterobacteriaceae. J. Antimicrob. Chemother. 2013, 68(3):487-489.
71. Nordmann P., Naas T., et al. Global spread of Carbapenemase-producing Enterobacteriaceae. Emerg. Infect. Dis. 2011, 17(10):1791-1798.
72. Nordmann P., Poirel L., et al. How to detect NDM-1 producers. J. Clin. Microbiol. 2011, 49(2):718-721.
73. Nordmann P., Dortet L., et al. Carbapenem resistance in Enterobacteriaceae: here is the storm!. Trends Mol. Med. 2012, 18(5):263-272.
74. Nordmann P., Girlich D., et al. Detection of carbapenemase producers in Enterobacteriaceae by use of a novel screening medium. J. Clin. Microbiol. 2012, 50(8):2761-2766.
75. Nordmann P., Gniadkowski M., et al. Identification and screening of carbapenemase-producing Enterobacteriaceae. Clin. Microbiol. Infect. 2012, 18(5):432-438.
76. Nordmann P., Poirel L., et al. Rapid detection of carbapenemase-producing Enterobacteriaceae. Emerg. Infect. Dis. 2012, 18(9):1503-1507.
77. Notake S., Matsuda M., et al. Detection of IMP metallo-beta-lactamase in carbapenem-nonsusceptible Enterobacteriaceae and non-glucose-fermenting Gram-negative rods by immunochromatography assay. J. Clin. Microbiol. 2013, 51(6):1762-1768.
78. Notomi T., Okayama H., et al. Loop-mediated isothermal amplification of DNA. Nucleic Acids Res. 2000, 28(12):E63.
79. Park Y.K., Choi J.Y., et al. Two distinct clones of carbapenem-resistant Acinetobacter baumannii isolates from Korean hospitals. Diagn. Microbiol. Infect. Dis. 2009, 64(4):389-395.
80. Pasteran F., Mendez T., et al. Sensitive screening tests for suspected class A carbapenemase production in species of Enterobacteriaceae. J. Clin. Microbiol. 2009, 47(6):1631-1639.
81. Patel G., Bonomo R.A. "Stormy waters ahead": global emergence of carbapenemases. Front. Microbiol. 2013, 4:48.
82. Perez-Perez F.J., Hanson N.D. Detection of plasmid-mediated AmpC beta-lactamase genes in clinical isolates by using multiplex PCR. J. Clin. Microbiol. 2002, 40(6):2153-2162.
83. Poirel L., Nordmann P. Carbapenem resistance in Acinetobacter baumannii: mechanisms and epidemiology. Clin. Microbiol. Infect. 2006, 12(9):826-836.
84. Poirel L., Heritier C., et al. Emergence of oxacillinase-mediated resistance to imipenem in Klebsiella pneumoniae. Antimicrob. Agents Chemother. 2004, 48(1):15-22.
85. Poirel L., Marque S., et al. OXA-58, a novel class D {beta}-lactamase involved in resistance to carbapenems in Acinetobacter baumannii. Antimicrob. Agents Chemother. 2005, 49(1):202-208.
86. Poirel L., Naas T., et al. Diversity, epidemiology, and genetics of class D beta-lactamases. Antimicrob. Agents Chemother. 2010, 54(1):24-38.
87. Poirel L., Schrenzel J., et al. Molecular analysis of NDM-1-producing enterobacterial isolates from Geneva, Switzerland. J. Antimicrob. Chemother. 2011, 66(8):1730-1733.
88. Poirel L., Walsh T.R., et al. Multiplex PCR for detection of acquired carbapenemase genes. Diagn. Microbiol. Infect. Dis. 2011, 70(1):119-123.
89. Poirel L., Potron A., et al. OXA-48-like carbapenemases: the phantom menace. J. Antimicrob. Chemother. 2012, 67(7):1597-1606.
90. Pournaras S., Poulou A., et al. Inhibitor-based methods for the detection of KPC carbapenemase-producing Enterobacteriaceae in clinical practice by using boronic acid compounds. J. Antimicrob. Chemother. 2010, 65(7):1319-1321.
91. Qi J., Du Y., et al. A loop-mediated isothermal amplification method for rapid detection of NDM-1 gene. Microb. Drug Resist. 2012, 18(4):359-363.
92. Queenan A.M., Bush K. Carbapenemases: the versatile beta-lactamases. Clin. Microbiol. Rev. 2007, 20(3):440-458. (table of contents).
93. Ratkai C., Quinteira S., et al. Controlling for false positives: interpreting MBL Etest and MBL combined disc test for the detection of metallo-beta-lactamases. J. Antimicrob. Chemother. 2009, 64(3):657-658.
94. Ruppe E., Bidet P., et al. First detection of the Ambler class C 1 Amp. beta-lactamase in Citrobacter freundii by a new, simple double-disk synergy test. J. Clin. Microbiol. 2006, 44(11):4204-4207.
95. Samra Z., Bahar J., et al. Evaluation of CHROMagar KPC for rapid detection of carbapenem-resistant Enterobacteriaceae. J. Clin. Microbiol. 2008, 46(9):3110-3111.
96. Samuelsen O., Buaro L., et al. Evaluation of phenotypic tests for the detection of metallo-beta-lactamase-producing Pseudomonas aeruginosa in a low prevalence country. J. Antimicrob. Chemother. 2008, 61(4):827-830.
97. Schneider I., Queenan A.M., et al. Novel carbapenem-hydrolyzing oxacillinase OXA-62 from Pandoraea pnomenusa. Antimicrob. Agents Chemother. 2006, 50(4):1330-1335.
98. Segal H., Elisha B.G. Use of Etest MBL strips for the detection of carbapenemases in Acinetobacter baumannii. J. Antimicrob. Chemother. 2005, 56(3):598.
99. Shahcheraghi F., Abbasalipour M., et al. Isolation and genetic characterization of metallo-beta-lactamase and carbapenamase producing strains of Acinetobacter baumannii from patients at Tehran hospitals. Iran. J. Microbiol. 2011, 3(2):68-74.
100. Stuart J.C., Voets G., et al. Detection of carbapenemase-producing Enterobacteriaceae with a commercial DNA microarray. J. Med. Microbiol. 2012, 61(Pt 6):809-812.
101. Tenover F.C., Arbeit R.D., et al. Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J. Clin. Microbiol. 1995, 33(9):2233-2239.
102. Tenover F.C., Kalsi R.K., et al. Carbapenem resistance in Klebsiella pneumoniae not detected by automated susceptibility testing. Emerg. Infect. Dis. 2006, 12(8):1209-1213.
103. Thomson K.S. Extended-spectrum-beta-lactamase, AmpC, and Carbapenemase issues. J. Clin. Microbiol. 2010, 48(4):1019-1025.
104. Tijet N., Boyd D., et al. Evaluation of the Carba NP test for rapid detection of carbapenemase-producing Enterobacteriaceae and Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 2013, 57(9):4578-4580.
105. Tsakris A., Kristo I., et al. First occurrence of KPC-2-possessing Klebsiella pneumoniae in a Greek hospital and recommendation for detection with boronic acid disc tests. J. Antimicrob. Chemother. 2008, 62(6):1257-1260.
106. Tsakris A., Kristo I., et al. Evaluation of boronic acid disk tests for differentiating KPC-possessing Klebsiella pneumoniae isolates in the clinical laboratory. J. Clin. Microbiol. 2009, 47(2):362-367.
107. Upadhyay S., Sen M.R., et al. Diagnostic utility of combination of inducer and inhibitor based assay in detection of Pseudomonas aeruginosa producing AmpC beta-lactamase. J. Microbiol. Methods 2011, 87(1):116-118.
108. Versalovic J., Koeuth T., et al. Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting of bacterial genomes. Nucleic Acids Res. 1991, 19(24):6823-6831.
109. Vourli S., Giakkoupi P., et al. Novel GES/IBC extended-spectrum beta-lactamase variants with carbapenemase activity in clinical enterobacteria. FEMS Microbiol. Lett. 2004, 234(2):209-213.
110. Vrioni G., Daniil I., et al. Comparative evaluation of a prototype chromogenic medium (ChromID CARBA) for detecting carbapenemase-producing Enterobacteriaceae in surveillance rectal swabs. J. Clin. Microbiol. 2012, 50(6):1841-1846.
111. Walsh T.R., Toleman M.A., et al. Metallo-beta-lactamases: the quiet before the storm?. Clin. Microbiol. Rev. 2005, 18(2):306-325.
112. Wang L., Gu H., et al. Rapid low-cost detection of Klebsiella pneumoniae carbapenemase genes by internally controlled real-time PCR. J. Microbiol. Methods 2012, 91(3):361-363.
113. Wareham D.W., Gordon N.C. Modifications to CHROMagar Acinetobacter for improved selective growth of multi-drug resistant Acinetobacter baumannii. J. Clin. Pathol. 2011, 64(2):164-167.
114. Wieser A., Schneider L., et al. MALDI-TOF MS in microbiological diagnostics-identification of microorganisms and beyond (mini review). Appl. Microbiol. Biotechnol. 2012, 93(3):965-974.
115. Wolter D.J., Kurpiel P.M., et al. Phenotypic and enzymatic comparative analysis of the novel KPC variant KPC-5 and its evolutionary variants, KPC-2 and KPC-4. Antimicrob. Agents Chemother. 2009, 53(2):557-562.
116. Won S.Y., Munoz-Price L.S., et al. Emergence and rapid regional spread of Klebsiella pneumoniae carbapenemase-producing Enterobacteriaceae. Clin. Infect. Dis. 2011, 53(6):532-540.
117. Woodford N., Warner M., et al. Evaluation of a commercial microarray to detect carbapenemase-producing Enterobacteriaceae. J. Antimicrob. Chemother. 2011, 66(12):2887-2888.
118. Yagi T., Wachino J., et al. Practical methods using boronic acid compounds for identification of class C beta-lactamase-producing Klebsiella pneumoniae and Escherichia coli. J. Clin. Microbiol. 2005, 43(6):2551-2558.
119. Yan J.J., Wu J.J., et al. Comparison of the double-disk, combined disk, and Etest methods for detecting metallo-beta-lactamases in Gram-negative bacilli. Diagn. Microbiol. Infect. Dis. 2004, 49(1):5-11.
120. Yang Y., Bush K. Biochemical characterization of the carbapenem-hydrolyzing beta-lactamase AsbM1 from Aeromonas sobria AER 14M: a member of a novel subgroup of metallo-beta-lactamases. FEMS Microbiol. Lett. 1996, 137(2-3):193-200.
121. Yigit H., Queenan A.M., et al. Novel carbapenem-hydrolyzing beta-lactamase, KPC-1, from a carbapenem-resistant strain of Klebsiella pneumoniae. Antimicrob. Agents Chemother. 2001, 45(4):1151-1161.
122. Yong D., Lee K., et al. Imipenem-EDTA disk method for differentiation of metallo-beta-lactamase-producing clinical isolates of Pseudomonas spp. and Acinetobacter spp. J. Clin. Microbiol. 2002, 40(10):3798-3801.
123. Zhanel G.G., Wiebe R., et al. Comparative review of the carbapenems. Drugs 2007, 67(7):1027-1052.