JAC Advance Access originally published online on May 20, 2008
Journal of Antimicrobial Chemotherapy 2008 62(3):632-634; doi:10.1093/jac/dkn211
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Research letters |
Plasmid-mediated quinolone resistance due to qnrB5 and qnrS1 genes in Salmonella enterica serovars Newport, Hadar and Saintpaul isolated from turkey meat in Denmark
1 National Food Institute, Technical University of Denmark, Bülowsvej 27, DK-1790 Copenhagen V, Denmark 2 Department of Veterinary Pathobiology, LIFE—Faculty of Life Sciences, University of Copenhagen, Stigbøjlen 4, DK-1870 Frederiksberg C, Denmark
* Correspondence address. National Food Institute, Technical University of Denmark, Bülowsvej 27, room B25, DK-1790 København, Denmark. Tel: +45-72-34-62-69; Fax: +45-72-34-63-41; E-mail: licav{at}food.dtu.dk
Keywords: qnr , poultry , aac(6')Ib-cr , antimicrobial resistance , fluoroquinolones , PFGE
Sir,
Recently, new transferable mechanisms conferring low-level quinolone resistance have been described. The first gene found was qnrA, followed by other qnr genes (B and S), and a large number of variants of these genes have been found to date.1 qnr genes encode proteins that protect topoisomerases and reduce susceptibility to fluoroquinolones. At first, these genes were found very rarely, but now they seem to have spread more rapidly than expected and have been found in the USA, Africa, Asia and also in Europe. Furthermore, other genes encoding transferable quinolone resistance have been described: aac(6')Ib-cr encodes an aminoglycoside-modifying enzyme able to modify ciprofloxacin.1
In this study, we report the finding of Salmonella isolates carrying qnr genes, isolated from turkey meat imported from Germany and Poland, which were found among samples of meat for retail in Denmark. As part of a case-by-case surveillance programme, meat batches were sampled and 12 samples of each batch of fresh or frozen meat were cultured for isolation of Salmonella enterica.2 The Salmonella isolates obtained were serotyped and MICs determined for a panel, including 17 antimicrobials, by the broth microdilution method according to the CLSI guidelines, and CLSI breakpoints were used for the interpretation of the results, except for ciprofloxacin where the breakpoint used for determination of resistance was MIC > 0.06 mg/L, according to EUCAST (http://www.eucast.org). In 2007, 1536 batches of meat were analysed in this programme, including meat from chicken (n = 581), turkey (n = 209), beef (n = 290) and pork (n = 456). In total, 10.5% of the batches were positive for Salmonella. Ciprofloxacin resistance was observed in 2.6% of the total batches analysed.
We observed that turkey meat accounted for 52.5% of the ciprofloxacin-resistant batches and 64.1% of the ciprofloxacin-resistant isolates. In total, 209 batches of turkey meat were analysed and 39 (18.7%) of these were found positive for Salmonella. A total of 175 Salmonella isolates were obtained from turkey meat for further characterization. One hundred and sixteen isolates (66.3% of the turkey meat isolates) belonging to 21 batches of turkey meat (53.8% of the turkey meat Salmonella-positive batches) were found to be resistant to ciprofloxacin, whereas only 108 isolates (61.7%) from 19 batches (46.3%) were found to be resistant to nalidixic acid. Eight ciprofloxacin-resistant Salmonella isolates (6.9%) belonging to three turkey meat batches showed reduced susceptibility to ciprofloxacin (MIC 0.5–1 mg/L) but were susceptible or intermediate to nalidixic acid (MIC 8–16 mg/L), whereas no other isolates from other meat sources showed the same phenotype. These strains belonged to the following serovars: Saintpaul (n = 1), Newport (n = 3) and Hadar (n = 4). One of the positive batches contained both the four Hadar isolates and a Saintpaul isolate. Additionally, three isolates of Salmonella Saintpaul obtained from two batches of turkey meat, also imported from Germany and Poland, collected in January–February 2008 showed the same resistance phenotype regarding quinolones. Thus, these 11 isolates were submitted to a screening for qnrA, qnrB, qnrS and aac(6')Ib-cr by PCR amplification as described previously.3 All PCR amplicons were sent for sequencing (Macrogen, Korea) to determine the gene variants present.
The PCR and sequencing results show that all four serotype Saintpaul isolates carried qnrS1 and that the remaining isolates harboured qnrB5 (Figure 1). None of the isolates tested were positive for either qnrA or aac(6')Ib-cr, and none showed mutations inside the QRDR of gyrA and parC genes, although a mutation leading to an amino acid substitution outside the QRDR of parC (T57S) was detected in all strains carrying the qnrB5 gene. PFGE restricted with XbaI revealed that three of the Salmonella Saintpaul isolates were indistinguishable, although they originated from two batches of meat from Germany and Poland, and the remaining one showed high similarity to the previous one. The qnrB5-positive Newport isolates were indistinguishable, although they were originated from two batches of meat. Similarly, the Hadar isolates were found to be indistinguishable as they might represent isolates of the same strain present in one batch of meat from Germany, which also contained one of the Salmonella Saintpaul isolates positive for qnrS1. Furthermore, the antimicrobial susceptibility profiles showed similarities within serovars (Figure 1).
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32 mg/L) was defined based on research performed at our Institute.The findings indicate that turkey meat might be a possible source of Salmonella harbouring transferable quinolone-resistant determinants. These resistance determinants are emerging and qnr genes had previously been described in S. enterica from several countries: qnrA in serovar Concord, qnrB2 and qnrB5 in Salmonella Berta, qnrS1 in Salmonella Typhimurium, Infantis, Corvallis, Stanley, Saintpaul, Typhimurium, Virchow and Virginia and qnrS2 in serovar Anatum.4–11
A high prevalence of quinolone-resistant Salmonella was found in turkey meat (66.3% of the isolates and 53.8% of the positive batches from turkey meat) and three of these batches contained isolates with qnr genes (6.9%). To identify sources and selective factors such as quinolone usage in farms, it would be important to be able to trace back to the origin of these Salmonella isolates; however, in this study, the information obtained was limited to the slaughter location.
This is, to our knowledge, the first report of qnr genes detected in S. enterica serovar Hadar and Newport and the first report of plasmid-mediated quinolone resistance from turkey meat, although qnrS1 in Salmonella from poultry origin had been previously detected in Germany in a Salmonella Infantis isolate, and then in the UK, Turkey and Thailand.6,8–10
The presence of qnr genes in human pathogens isolated from meat products is of concern as Salmonella carrying qnr genes may cause outbreaks in humans as has been previously described in the UK with Salmonella Virchow.8 Furthermore, for human salmonellosis, treatment with fluoroquinolones might be attempted, and although the possible clinical implications of transferable quinolone resistance are still unknown, treatment failure could be a possible outcome.
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L. M. C. was supported by a grant from the EU Marie Curie Programme TRAINAU (MEST-CT-2004-007819).
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None to declare.
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References |
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2 Anonymous. Intensified control of Campylobacter and Salmonella in fresh meat—a case-by-case risk assessment. In: Annual Report on Zoonoses in Denmark 2006 (2006) Technical University of Denmark. 10.
3 Cavaco LM, Frimodt-Moller N, Hasman H, et al. Prevalence of quinolone resistance mechanisms and associations to minimum inhibitory concentrations in quinolone-resistant Escherichia coli isolated from humans and swine in Denmark. Microb Drug Resist (2008) in press.
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Hopkins KL, Wootton L, Day MR, et al. Plasmid-mediated quinolone resistance determinant qnrS1 found in Salmonella enterica strains isolated in the UK. J Antimicrob Chemother (2007) 59:1071–5.
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Kehrenberg C, Friederichs S, de Jong A, et al. Identification of the plasmid-borne quinolone resistance gene qnrS in Salmonella enterica serovar Infantis. J Antimicrob Chemother (2006) 58:18–22.
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Kehrenberg C, Hopkins KL, Threlfall EJ, et al. Complete nucleotide sequence of a small qnrS1-carrying plasmid from Salmonella enterica subsp. enterica Typhimurium DT193. J Antimicrob Chemother (2007) 60:903–5.
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Veldman K, van Pelt W, Mevius D. First report of qnr genes in Salmonella in The Netherlands. J Antimicrob Chemother (2008) 61:452–3.
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