JAC Advance Access originally published online on March 6, 2007
Journal of Antimicrobial Chemotherapy 2007 59(4):814-815; doi:10.1093/jac/dkm010
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Correspondence |
Less frequent Salmonella serovars as a reservoir of antimicrobial resistance
Statens Serum Institut, Artillerivej 5, DK-2300 Copenhagen S, Denmark
* Corresponding author. Tel: +45-32683191; Fax: +45-32683887; E-mail: lbs{at}ssi.dk
Keywords: ciprofloxacin , multidrug-resistant , MICs
Salmonella enterica serovars Enteritidis and Typhimurium are the most frequent Salmonella serovars isolated from humans. However, a significant proportion of human Salmonella isolates belong to other serovars, for which antimicrobial susceptibility patterns are rarely reported. In Denmark, the frequency of isolation of these less frequent Salmonella serovars from human clinical samples has increased in recent years. They represented 
30% of all human Salmonella isolates, which corresponded to an incidence of 10.5 per 100 000 inhabitants in 2005.1 From 2003 to 2005, 530 isolates belonging to these Salmonella serovars were tested for their antimicrobial susceptibility by broth microdilution (Sensititre; Trek Diagnostic Systems Ltd, East Grinstead, UK) at the Statens Serum Institut. These included 106 Salmonella Virchow, 95 Salmonella Newport, 91 Salmonella Stanley, 80 Salmonella Dublin, 53 Salmonella Hadar, 38 Salmonella Saintpaul, 32 Salmonella Derby, 20 Salmonella Uganda and 15 Salmonella Anatum obtained from sporadic clinical infections, isolated at the 16 clinical microbiology laboratories in Denmark. The MICs for these 530 human clinical Salmonella isolates were determined for ampicillin (1–32 mg/L), cefalotin (4–32 mg/L), chloramphenicol (2–64 mg/L), ciprofloxacin (0.03–4 mg/L), gentamicin (1–32 mg/L), nalidixic acid (8–64 mg/L), sulfamethoxazole (64–1024 mg/L), streptomycin (4–64 mg/L), tetracycline (2–32 mg/L) and trimethoprim (4–32 mg/L). The CLSI (formerly NCCLS) breakpoints were used.2 For ciprofloxacin, a breakpoint of 
0.125 mg/L was also used,3,4 and for streptomycin, a breakpoint of 32 mg/L was used.5 Escherichia coli ATCC 25922 was used for quality control.
The number of tested isolates and the percentages of resistance are reported in Table 1. Isolates belonging to some serovars, e.g. Salmonella Dublin, Salmonella Saintpaul and Salmonella Derby, were susceptible to most antimicrobials tested, whereas isolates belonging to other serovars showed much higher frequencies of resistance, e.g. Salmonella Virchow, Salmonella Newport and Salmonella Stanley. A high prevalence of multidrug resistance (resistance to four or more antimicrobial agents) was observed among isolates belonging to the following serovars: Salmonella Hadar (30%), Salmonella Virchow (25%), Salmonella Stanley (22%) and Salmonella Newport (19%). Resistance to ampicillin, chloramphenicol, streptomycin, sulfamethoxazole and tetracycline was present in Salmonella Newport (15%), Salmonella Stanley (8%) and Salmonella Virchow (1%). Resistance to these five antimicrobials could indicate the presence of the multidrug-resistant region Salmonella genomic island 1 (SGI1). This region is well described and common in Salmonella Typhimurium phage type DT104. It has also been found in other Salmonella serovars, e.g. Salmonella Newport.6
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Of the tested Salmonella Hadar and Salmonella Virchow isolates, 87% and 80%, respectively, were resistant to nalidixic acid. However, these isolates were not resistant to ciprofloxacin when the CLSI breakpoint (4 mg/L) was used. When using the EUCAST breakpoint for ciprofloxacin (0.125 mg/L), a good consistency was observed between nalidixic acid and ciprofloxacin resistance frequencies, even though minor differences were seen for Salmonella Hadar and Salmonella Stanley. For these two serovars, a higher resistance to ciprofloxacin than to nalidixic acid was observed (Table 1). This might indicate that nalidixic acid is a more precise indicator for low fluoroquinolone resistance than ciprofloxacin.
A Danish study has shown failures of treatment with ciprofloxacin for infection with Salmonella Typhimurium DT104, with an MIC value below the CLSI breakpoint.7 Similar failures of treatment might be observed for Salmonella Hadar and Salmonella Virchow if the CLSI breakpoint for ciprofloxacin is used. This is of great concern, since ciprofloxacin is often the drug of choice when treating invasive Salmonella infections.
Twelve Salmonella Hadar and one Salmonella Newport isolate were resistant to cefalotin (Table 1). When tested phenotypically for extended-spectrum ß-lactamase (ESBL) activity using the Etest (cefotaxime and ceftazidime with and without clavulanic acid), all isolates were ESBL negative.8
Prevalence of antimicrobial resistance varies greatly among less frequent Salmonella serovars isolated in Denmark, and some serovars show a higher level of resistance than others.
None to declare.
Footnotes
Present address. Novozymes, Krogshøjvej 36, DK-2880 Bagsværd, Denmark 
Acknowledgements
Part of this study was presented at the Forty-sixth Interscience Conference on Antimicrobial Agents and Chemotherapy, San Francisco, CA, USA, 2006. Ingrid B. Jensen is thanked for technical assistance. This work was a part of The Danish Integrated Antimicrobial Resistance Monitoring and Research Programme (DANMAP) and was funded by the Danish Ministry of the Interior and Health.
References
1 Anon. (2006) Annual Report on Zoonoses in Denmark 2005 , Copenhagen, Denmark Ministry of Family and Consumer Affairs.
2 Clinical and Laboratory Standards Institute. (2005) Performance Standards for Antimicrobial Susceptibility Testing: Fifteenth Informational Supplement M100-S15(CLSI, Wayne, PA, USA).
3
Aarestrup FM, Wiuff C, Mølbak K, et al. (2003) Is it time to change fluoroquinolone breakpoints for Salmonella spp.? Antimicrob Agents Chemother 47:827–9.
4 European Committee on Antimicrobial Susceptibility Testing. Fluoroquinolones — EUCAST Clinical MIC Breakpoints 2006-06-20 (v 2.2) http://www.srga.org/eucastwt/MICTAB/MICquinolones.htm (1 January 2007, date last accessed).
5 DANMAP. (2005) Use of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Bacteria from Food Animals, Foods and Humans in Denmark http://www.danmap.org/pdfFiles/Danmap_2005.pdf (3 January 2007, date last accessed).
6 Mulvey MR, Boyd DA, Olson AB, et al. (2006) The genetics of Salmonella genomic island 1. Microbes Infect 8:1915–22.[CrossRef][Web of Science][Medline]
7
Kristiansen MA, Sandvang D, Rasmussen TB. (2003) In vivo development of quinolone resistance in Salmonella enterica serotype Typhimurium DT104. J Clin Microbiol 41:4462–4.
8 Etest Technical Guide 3B. Etest for MIC Determination (AB Biodisk, Solna, Sweden) http://www.abbiodisk.com/pdf/etg/M0000003.pdf (7 February 2007, date last accessed).
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