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Antimicrobial Agents and Chemotherapy, September 2009, p. 3832-3836, Vol. 53, No. 9
0066-4804/09/$08.00+0     doi:10.1128/AAC.00121-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

Mechanisms of Resistance in Nontyphoidal Salmonella enterica Strains Exhibiting a Nonclassical Quinolone Resistance Phenotype{triangledown}

Marianne Gunell,1* Mark A. Webber,2 Pirkko Kotilainen,1,3 Andrew J. Lilly,2 Jonathan M. Caddick,2 Jari Jalava,1 Pentti Huovinen,1 Anja Siitonen,4 Antti J. Hakanen,1,3 and Laura J. V. Piddock2

Antimicrobial Resistance Unit,1 Gastrointestinal Infection Unit, National Institute for Health and Welfare, Turku and Helsinki, Finland,4 Antimicrobial Agents Research Group, School of Immunity and Infection, University of Birmingham, Birmingham B15 2TT, United Kingdom,2 Department of Medicine, Turku University Hospital and University of Turku, Turku, Finland3

Received 28 January 2009/ Returned for modification 21 March 2009/ Accepted 4 July 2009

Nontyphoidal Salmonella enterica strains with a nonclassical quinolone resistance phenotype were isolated from patients returning from Thailand or Malaysia to Finland. A total of 10 isolates of seven serovars were studied in detail, all of which had reduced susceptibility (MIC ≥ 0.125 µg/ml) to ciprofloxacin but were either susceptible or showed only low-level resistance (MIC ≤ 32 µg/ml) to nalidixic acid. Phenotypic characterization included susceptibility testing by the agar dilution method and investigation of efflux activity. Genotypic characterization included the screening of mutations in the quinolone resistance-determining regions (QRDR) of gyrA, gyrB, parC, and parE by PCR and denaturing high-pressure liquid chromatography and the amplification of plasmid-mediated quinolone resistance (PMQR) genes qnrA, qnrB, qnrS, qnrD, aac(6')-Ib-cr, and qepA by PCR. PMQR was confirmed by plasmid analysis, Southern hybridization, and plasmid transfer. No mutations in the QRDRs of gyrA, gyrB, parC, or parE were detected with the exception of a Thr57-Ser substitution within ParC seen in all but the S. enterica serovar Typhimurium strains. The qnrA and qnrS genes were the only PMQR determinants detected. Plasmids carrying qnr alleles were transferable in vitro, and the resistance phenotype was reproducible in Escherichia coli DH5{alpha} transformants. These data demonstrate the emergence of a highly mobile qnr genotype that, in the absence of mutation within topoisomerase genes, confers the nontypical quinolone resistance phenotype in S. enterica isolates. The qnr resistance mechanism enables bacteria to survive elevated quinolone concentrations, and therefore, strains carrying qnr alleles may be able to expand during fluoroquinolone treatment. This is of concern since nonclassical quinolone resistance is plasmid mediated and therefore mobilizable.

* Corresponding author. Mailing address: Antimicrobial Resistance Unit, National Institute for Health and Welfare (THL), Kiinamyllynkatu 13, 20520 Turku, Finland. Phone: 358 20 610 6000. Fax: 358 20 610 6699. E-mail: mamali{at}utu.fi

{triangledown} Published ahead of print on 13 July 2009.

Antimicrobial Agents and Chemotherapy, September 2009, p. 3832-3836, Vol. 53, No. 9
0066-4804/09/$08.00+0     doi:10.1128/AAC.00121-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.





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