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Mechanisms of Resistance

Molecular Epidemiology and Mechanisms of Carbapenem Resistance in Pseudomonas aeruginosa Isolates from Spanish Hospitals

O. Gutiérrez, C. Juan, E. Cercenado, F. Navarro, E. Bouza, P. Coll, J. L. Pérez, A. Oliver
O. Gutiérrez
1Servicio de Microbiología and Unidad de Investigación, Hospital Son Dureta, Instituto Universitario de Investigación en Ciencias de la Salud (IUNICS), Palma de Mallorca
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C. Juan
1Servicio de Microbiología and Unidad de Investigación, Hospital Son Dureta, Instituto Universitario de Investigación en Ciencias de la Salud (IUNICS), Palma de Mallorca
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E. Cercenado
2Servicio de Microbiología, Hospital General Universitario Gregorio Marañón, Madrid
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F. Navarro
3Servicio de Microbiología, Hospital de la Santa Creu i Sant Pau, and Departament de Genètica i Microbiologia, Universidad Autònoma de Barcelona, Barcelona, Spain
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E. Bouza
2Servicio de Microbiología, Hospital General Universitario Gregorio Marañón, Madrid
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P. Coll
3Servicio de Microbiología, Hospital de la Santa Creu i Sant Pau, and Departament de Genètica i Microbiologia, Universidad Autònoma de Barcelona, Barcelona, Spain
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J. L. Pérez
1Servicio de Microbiología and Unidad de Investigación, Hospital Son Dureta, Instituto Universitario de Investigación en Ciencias de la Salud (IUNICS), Palma de Mallorca
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A. Oliver
1Servicio de Microbiología and Unidad de Investigación, Hospital Son Dureta, Instituto Universitario de Investigación en Ciencias de la Salud (IUNICS), Palma de Mallorca
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  • For correspondence: aoliver@hsd.es
DOI: 10.1128/AAC.00810-07
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    FIG. 1.

    Structure of the blaVIM-2 integron from plasmid pV2GY3 of P. aeruginosa strain GY3. The locations of the primers used for PCR amplification are also shown. IR, inverted repeat; approx., approximately.

  • FIG. 2.
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    FIG. 2.

    Clustal W (version 1.83) multiple-sequence alignment of AAC(6′)-32, AAC(6′)-31 (26), and AAC(6′)-Ib′ (16). Dashes represent amino acid residues that are lacking in the indicated sequence relative to the sequence of AAC(6′)-32; asterisks indicate identical residues, colons indicate conserved substitutions, and dots indicate semiconserved substitutions.

Tables

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  • TABLE 1.

    Primers used in this work

    PrimerSequence (5′ to 3′)PCR product size (bp)Use
    VIM1-F GTTAAAAGTTATTAGTAGTTTATTG 799Amplification and sequencing of blaVIM-1 and related genes
    VIM1-R CTACTCGGCGACTGAGC
    VIM2-F ATGTTCAAACTTTTGAGTAAG 801Amplification and sequencing of blaVIM-2 and related genes
    VIM2-R CTACTCAACGACTGAGCG
    VIM-F AGTGGTGAGTATCCGACAG Sequencing of blaVIM
    VIM-R ATGAAAGTGCGTGGAGAC
    IMP1-F ATGAGCAAGTTATCTGTATTC 741Amplification and sequencing of blaIMP-1 and related genes
    IMP1-R TTAGTTGCTTGGTTTTGATGG
    IMP2-F ATGAAGAAATTATTTGTTTTATG 741Amplification and sequencing of blaIMP-2 and related genes
    IMP2-R TTAGTTACTTGGCTGTGATG
    INT-F CTCTCACTAGTGAGGGGC 1,010Amplification and sequencing of intI
    INT-R ATGAAAACCGCCACTGCG
    INT-R-I CGCAGTGGCGGTTTTCAT VariableAmplification and sequencing of gene(s) between intI and blaVIM-2
    VIM2-F-I CTTACTCAAAAGTTTGAACAT
    qacE-F GAAAGGCTGGCTTTTTCTTG 210Amplification of qacEΔ1
    qacE-R ATTATGACGACGCCGAGTC
    qacE-F-I CAAGAAAAAGCCAGCCTTTC VariableAmplification and sequencing of gene(s) between blaVIM and qacEΔ1
    VIM-2-R-I CGCTCAGTCGTTGAGTAG
    PSE-1F ATGCTTTTATATAAAATGTGTG 914Amplification and sequencing of blaPSE-1 and related genes
    PSE-1R TCAGCGCGACTGTGATGTA
    OprDF CGCCGACAAGAAGAACTAGC 1,412Amplification and sequencing of oprD
    OprDR GTCGATTACAGGATCGACAG
    OprDF2 GCCGACCACCGTCAAATCG Sequencing of oprD
  • TABLE 2.

    Coresistance of carbapenem-resistant isolates to β-lactam and non-β-lactam antibiotics

    Antibiotic or resistance phenotype% of resistant isolates among:Statistical significance (P)
    Carbapenem-susceptible isolates (n = 1,014)cCarbapenem-resistant isolates (n = 236)c
    Ticarcillin1134<0.001
    Piperacillin928<0.001
    Piperacillin-tazobactam624<0.001
    Ceftazidime1146<0.001
    Cefepime1452<0.001
    Aztreonam1953<0.001
    Gentamicin2659<0.001
    Amikacin919<0.001
    Tobramycin944<0.001
    Ciprofloxacin2553<0.001
    Ofloxacin3268<0.001
    Imipenem95d
    Meropenem68
    MDRa46
    Panresistantb4
    • ↵ a MDR isolates are resistant to at least three of the following four antibiotics: ceftazidime, imipenem, tobramycin, and ciprofloxacin (27).

    • ↵ b Panresistant, resistant to all antibiotics tested.

    • ↵ c The percentages of resistant isolates shown include isolates in the intermediate and resistant CLSI categories (5).

    • ↵ d The remaining 5% of strains were imipenem susceptible, and the MIC of meropenem for these strains was 8 μg/ml (CLSI intermediate category).

  • TABLE 3.

    MICs for the VIM-2-producing P. aeruginosa GY3 clinical strain, the corresponding PAO1 transformant harboring plasmid pV2GY3 with blaVIM-2 and aac(6′)-32, and the E. coli XL1-Blue strain harboring plasmid pGTAAC-32 with the cloned aac(6′)-32

    StrainMIC (μg/ml) ofa:
    PIPPIP-TZTICAZTCAZFEPMERIMPCIPTOBGENAMK
    P. aeruginosa
        GY3168>2562161616>32>32>2563264
        PAO1(pV2GY3)1616>2562241616>320.125641648
        PAO121.51221.51.50.3820.1250.7523
    E. coli
        XL1-Blue0.380.190.75
        XL1-Blue(pGTAAC-32)60.51.5
    • ↵ a MICs of piperacillin (PIP), piperacillin-tazobactam (PIP-TZ), ticarcillin (TIC), aztreonam (AZT), ceftazidime (CAZ), cefepime (FEP), meropenem (MER), imipenem (IMP), ciprofloxacin (CIP), tobramycin (TOB), gentamicin (GEN), and amikacin (AMK) were determined by Etest.

  • TABLE 4.

    Inactivating mutations in oprD in imipenem-resistant clones

    Type of inactivating mutationCloneDescription of mutation(s)a
    Frameshift mutation produced by 1-bp insertion or deletionLP2Deletion of 1 bp (G) at GGGGG repeat (nt 631-635)
    CAS2Deletion of 1 bp (C) at CC repeat (nt 475 and 476)
    VDS3Insertion of 1 bp (G) at GGGG repeat (nt 413-416)
    Premature stop codonSCA1aTGG→TGA at nt 831
    ALB1TGG→TGA at nt 195
    DRP2TAT→TAA at nt 219
    Partial deletion of the coding sequenceLC413-bp deletion beginning at nt 891
    RYC125-bp deletion beginning at nt 552
    Interruption of the coding sequence by ISDEF11,337-bp IS at nt 1048; encodes a 361-aa putative IS4 type transposase
    NoneUNC1Several nonunique polymorphisms in OprD: T103S, K115T, F170L, E185Q, P186G, V189T, R310E, A315G, and G425A
    • ↵ a Nucleotide (nt) and amino acid (aa) numbers are according to the published oprD sequence of PAO1. Boldface indicates mutated nucleotides.

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Molecular Epidemiology and Mechanisms of Carbapenem Resistance in Pseudomonas aeruginosa Isolates from Spanish Hospitals
O. Gutiérrez, C. Juan, E. Cercenado, F. Navarro, E. Bouza, P. Coll, J. L. Pérez, A. Oliver
Antimicrobial Agents and Chemotherapy Nov 2007, 51 (12) 4329-4335; DOI: 10.1128/AAC.00810-07

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Molecular Epidemiology and Mechanisms of Carbapenem Resistance in Pseudomonas aeruginosa Isolates from Spanish Hospitals
O. Gutiérrez, C. Juan, E. Cercenado, F. Navarro, E. Bouza, P. Coll, J. L. Pérez, A. Oliver
Antimicrobial Agents and Chemotherapy Nov 2007, 51 (12) 4329-4335; DOI: 10.1128/AAC.00810-07
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KEYWORDS

carbapenems
Pseudomonas aeruginosa
beta-lactam resistance

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