JAC Advance Access originally published online on July 16, 2007
Journal of Antimicrobial Chemotherapy 2007 60(3):704-706; doi:10.1093/jac/dkm261
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Correspondence |
Plasmid-mediated quinolone resistance determinant qnrS1 detected in Salmonella enterica serovar Corvallis strains isolated in Denmark and Thailand
1 National Food Institute, Technical University of Denmark, Bülowsvej 27, DK-1790 Copenhagen V, Denmark 2 Department for Veterinary Pathobiology, LIFE—Faculty of Life Sciences, University of Copenhagen, Stigbojlen 4, DK-1870 Frederiksberg C, Denmark
* Corresponding author. Tel: +45-72-34-62-69; Fax: +45-72-34-63-41; E-mail: lcaxx{at}food.dtu.dk
Keywords: imported meat , qnr , QRDR
Until recently, chromosomal mutations in the topoisomerase genes involved in DNA transcription and replication were considered the main mechanisms of quinolone resistance in Enterobacteriaceae. A new and transferable mechanism was described in 1998 in a Klebsiella pneumoniae isolate obtained from a patient in 1994 in Alabama, USA. Other qnr genes (A, B and S) and several variants encoding plasmid-mediated quinolone resistance have recently been described.1 These encode Qnr proteins that are members of the pentapeptide family and are able to protect topoisomerases, and thus reduce their susceptibility to fluoroquinolones.1 Plasmid-mediated quinolone resistance, which was originally found very rarely, seems to have spread more rapidly than expected and is now found in the US, Africa, Asia and also in Europe.1 The genes are often located on transferable plasmids and co-transmitted with other important resistance genes, especially genes encoding resistance to cephalosporins.1
We have recently described the characterization of a collection of 59 S. Corvallis isolates from Denmark, Bulgaria and Thailand.2 A total of 23 isolates in this collection showed reduced susceptibility to ciprofloxacin (MIC > 0.06 mg/L) but were found to be susceptible or intermediate to nalidixic acid (MIC 8–16 mg/L). All isolates showing this type of resistance profile were examined for the presence of qnrA, qnrB, qnrS and aac(6')Ib by PCR amplification and sequencing of the gyrA and parC genes. Briefly, qnrA and qnrS were amplified using primers based on published sequences and qnrB using primers described before as FQ1 and FQ2.3 As positive control strains, we used E. coli J53 pMG252 positive for qnrA, E. coli J53 pMG298 positive for qnrB (both strains kindly provided by Dr George Jacoby) and for qnrS E. coli MT102 pBC-H2.6, obtained by electroporating the plasmid pBC-H2.6 (obtained from Dr M. Hata, through the Rikken DNA Bank) into E. coli MT102. For aac(6')Ib, PCR was performed as described by Park et al.4 As positive control, we used the strain Salmonella enterica S74 (GenBank accession number: DQ278189).5
Of the 23 isolates, 7 were obtained from humans in Denmark and the remaining 16 were isolated in Thailand from: humans (n = 6), chicken (n = 5), pork (n = 3) and beef (n = 2). All 23 isolates carried the qnrS gene and sequencing revealed that it was the qnrS1 variant. None of the isolates tested was positive either for qnrA, qnrB or aac(6')Ib genes and none showed mutations in the quinolone resistance determining regions (QRDR) sequenced. PFGE revealed seven different types although all were related (Figure 1) and some of the types could be observed in both countries in humans and foodstuffs. Some of the isolates were susceptible to all antimicrobials tested except ciprofloxacin, others were in addition resistant to streptomycin, sulfamethoxazole and tetracycline (n = 16). In none of these isolates was resistance observed towards penicillins or cephalosporins and therefore we did not investigate the presence of ESBL genes in these isolates, although they are usually found in association with qnr genes.1
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This is the first report of qnr genes detected in 23 S. enterica Corvallis isolates and also the first report of qnr in Salmonella isolates from Denmark and Thailand.
The epidemiology of Salmonella infections in Denmark is complicated. It is interesting that isolates of the same serovar, with the same newly emerged resistance mechanisms and the same PFGE type were found in patients in Thailand, patients in Denmark and imported food products. Denmark has been importing an increasing amount of chicken meat, and much of the imported chicken originates from Thailand. These data support the possibility that some patients in Denmark acquired S. Corvallis from imported chicken meat from Thailand. We have recently indicated a similar phenomenon of infections with multidrug-resistant S. Schwarzengrund.6
Regarding the detection of quinolone resistance, the presence of the qnr genes alone does not necessarily mediate full resistance to nalidixic acid and thus makes the use of nalidixic acid for screening for fluoroquinolone resistance unreliable. This is in contrast to the mutation-mediated resistance, where one mutation encodes low-level resistance to fluoroquinolones and full resistance to nalidixic acid. Low-level fluoroquinolone resistance is difficult to detect in routine diagnostic laboratories and these isolates might easily be considered susceptible especially when using diffusion testing. Further studies are needed on optimization of detection in clinical laboratories of low-level resistance.
None to declare.
Acknowledgements
L. M. C. was supported by a grant from the EU Marie Curie Programme TRAINAU (MEST-CT-2004-007819). Thanks to Dr George Jacoby for kindly providing QnrA and B positive control strains and primer sequences, to Dr Mami Hata for providing qnrS gene DNA through Rikken DNA Bank. Thanks to Lisbeth Andersen and Berith Kummerfeldt for technical assistance.
References
1 Robicsek A, Jacoby GA, Hooper DC. The worldwide emergence of plasmid-mediated quinolone resistance. Lancet Infect Dis (2006) 6:629–40.[CrossRef][ISI][Medline]
2 Archambault M, Petrov P, Hendriksen RS, et al. Molecular characterization and occurrence of extended-spectrum beta-lactamase resistance genes among Salmonella enterica serovar Corvallis from Thailand, Bulgaria, and Denmark. Microb Drug Resist (2006) 12:192–8.[CrossRef][ISI][Medline]
3
Jacoby GA, Walsh KE, Mills DM, et al. qnrB, another plasmid-mediated gene for quinolone resistance. Antimicrob Agents Chemother (2006) 50:1178–82.
4
Park CH, Robicsek A, Jacoby GA, et al. Prevalence in the United States of aac(6’)Ib-cr encoding a ciprofloxacin-modifying enzyme. Antimicrob Agents Chemother (2006) 50:3953–5.
5
Peirano G, Agerso Y, Aarestrup FM, et al. Occurrence of integrons and antimicrobial resistance genes among Salmonella enterica from Brazil. J Antimicrob Chemother (2006) 58:305–9.
6 Aarestrup FM. International spread of multidrug-resistant Salmonella Schwarzengrund in food products. Emerg Infect Dis (2007) 13:726–31.[ISI][Medline]
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