Antimicrobial susceptibility of travel-related Salmonella enterica serovar Typhi isolates detected in Switzerland (2002–2013) and molecular characterization of quinolone resistant isolates

BMC Infectious Diseases

Roger Stephan¹  Nicole Cernela¹  Grethe Sägesser¹  Helga Abgottspon¹  Magdalena Nüesch-Inderbinen¹ 

[1] Institute for Food Safety and Hygiene, National Centre for Enteropathogenic Bacteria and Listeria, Vetsuisse Faculty University of Zurich, Winterthurerstr 272, Zurich, CH-8057, Switzerland

关键词: PMQR;    ParC;    GyrA;    Ciprofloxacin;    Nalidixic acid;    MDR;    Typhoid fever;   

Others  :  1229545
DOI  :  10.1186/s12879-015-0948-2

 received in 2014-08-26, accepted in 2015-05-07,  发布年份 2015

【 摘 要 】

Background

Typhoid fever is an acute, invasive, and potentially fatal systemic infection caused by Salmonella enterica subspecies enterica serotype Typhi (S. Typhi). Drug resistance to antimicrobials such as ciprofloxacin is emerging in developing countries, threatening the efficacy of treatment of patients in endemic regions as well as of travellers returning from these countries.

Methods

We compared the antimicrobial resistance profiles of 192 S. Typhi isolated from patients over a time span of twelve years. Susceptibility testing was done by the disk diffusion method. A representative selection of isolates (n = 41) was screened by PCR for mutations in the quinolone resistance-determining regions (QRDRs) of the gyrA and parC genes and all 192 isolates were screened for plasmid-mediated quinolone resistance (PMQR) genes. Multilocus sequence typing (MLST) was used to investigate the sequence type of isolates from patients with a known history of international travel.

Results

Resistance rates for nalidixic acid increased from 20 % to 66.7 % between 2002 and 2013. Resistance to ciprofloxacin was detected in 55.6 % of the isolates by 2013. Ciprofloxacin resistance was predominantly associated with the triple substitutions Ser83 → Phe and Asp87 → Asn in GyrA and Ser80 → Ile in ParC. The plasmid-mediated resistance gene qnrS1 was detected in two isolates. Sequence type ST1 was associated with the Indian subcontinent, while ST2 was distributed internationally. Multidrug resistance was noted for 11.5 % of the isolates.

Conclusions

Fluoroquinolone resistant S. Typhi constitute a serious public health concern in endemic areas as well as in industrialized countries. Increased surveillance of global patterns of antimicrobial resistance is necessary and the control of resistant strains is of the utmost importance to maintain treatment options.

【 授权许可】

   
2015 Nüesch-Inderbinen et al.; licensee BioMed Central.

【 参考文献 】

• [1]Kaur J, Jain SK. Role of antigens and virulence factors of Salmonella enterica serovar Typhi in its pathogenesis. Microbiol Res. 2012; 167:199-210.
• [2]Kothari A, Pruthi A, Chugh TD. The burden of enteric fever. J Infect Dev Ctries. 2008; 2:253-9.
• [3]Hassing RJ, Goessens WH, Mevius DJ, van Pelt W, Mouton JW, Verbon A et al.. Decreased ciprofloxacin susceptibility in Salmonella Typhi and Paratyphi infections in ill-returned travellers: the impact on clinical outcome and future treatment options. Eur J Clin Microbiol Infect Dis. 2013; 32:1295-301.
• [4]Keller A, Frey M, Schmid H, Steffen R, Walker T, Schlagenhauf P. Imported typhoid fever in Switzerland, 1993 to 2004. J Travel Med. 2008; 15:248-51.
• [5]Background document: the diagnosis, treatment, and prevention of typhoid fever. WHO, Geneva, Switzerland; 2003.
• [6]Parry CM, Hien TT, Dougan G, White NJ, Farrar JJ. Typhoid fever. N Engl J Med. 2002; 347:1770-82.
• [7]Strahilevitz J, Jacoby GA, Hooper DC, Robicsek A. Plasmid-mediated quinolone resistance: a multifaceted threat. Clin Microbiol Rev. 2009; 22:664-89.
• [8]Martínez-Martínez L, Pascual A, Jacoby GA. Quinolone resistance from a transferable plasmid. Lancet. 1998; 351:797-9.
• [9]Jacoby GA, Walsh KE, Mills DM, Walker VJ, Oh H, Robicsek A et al.. qnrB, another plasmid-mediated gene for quinolone resistance. Antimicrob Agents Chemother. 2006; 50:1178-82.
• [10]Hata M, Suzuki M, Matsumoto M, Takahashi M, Sato K, Ibe S et al.. Cloning of a novel gene for quinolone resistance from a transferable plasmid in Shigella flexneri 2b. Antimicrob Agents Chemother. 2005; 49:801-3.
• [11]Parry CM, Thuy CT, Dongol S, Karkey A, Vinh H, Chinh NT et al.. Suitable disk antimicrobial susceptibility breakpoints defining Salmonella enterica serovar Typhi isolates with reduced susceptibility to fluoroquinolones. Antimicrob Agents Chemother. 2010; 54:5201-8.
• [12]Hakanen A, Kotilainen P, Jalava J, Siitonen A, Huovinen P. Detection of decreased fluoroquinolone susceptibility in Salmonellas and validation of nalidixic acid screening test. J Clin Microbiol. 1999; 37:3572-7.
• [13]Lynch MF, Blanton EM, Bulens S, Polyak C, Vojdani J, Stevenson J et al.. Typhoid fever in the United States, 1999–2006. JAMA. 2009; 302:859-65.
• [14]Cooke FJ, Wain J. The emergence of antibiotic resistance in typhoid fever. Travel Med Infect Dis. 2004; 2:67-74.
• [15]Crump JA, Barrett TJ, Nelson JT, Angulo FJ. Reevaluating fluoroquinolone breakpoints for Salmonella enterica serotype Typhi and for non-Typhi salmonellae. Clin Infect Dis. 2003; 37:75-81.
• [16]Wayne P, editor. Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Third Informational Supplement. CLSI document M100-S23. 2013.
• [17]Karczmarczyk M, Martins M, McCusker M, Mattar S, Amaral L, Leonard N et al.. Characterization of antimicrobial resistance in Salmonella enterica food and animal isolates from Colombia: identification of a qnrB19-mediated quinolone resistance marker in two novel serovars. FEMS Microbiol Lett. 2010; 313:10-9.
• [18]Robicsek A, Strahilevitz J, Sahm DF, Jacoby GA, Hooper DC. qnr prevalence in ceftazidime-resistant Enterobacteriaceae isolates from the United States. Antimicrob Agents Chemother. 2006; 50:2872-4.
• [19]Kim HB, Park CH, Kim CJ, Kim E-C, Jacoby GA, Hooper DC. Prevalence of plasmid-mediated quinolone resistance determinants over a 9-year period. Antimicrob Agents Chemother. 2009; 53:639-45.
• [20]Wang M, Guo Q, Xu X, Wang X, Ye X, Wu S et al.. New plasmid-mediated quinolone resistance gene, qnrC, found in a clinical isolate of Proteus mirabilis. Antimicrob Agents Chemother. 2009; 53:1892-7.
• [21]Cavaco LM, Hasman H, Xia S, Aarestrup FM. qnrD, a novel gene conferring transferable quinolone resistance in Salmonella enterica serovar Kentucky and Bovismorbificans strains of human origin. Antimicrob Agents Chemother. 2009; 53:603-8.
• [22]Kidgell C, Reichard U, Wain J, Linz B, Torpdahl M, Dougan G et al.. Salmonella Typhi, the causative agent of typhoid fever, is approximately 50,000 years old. Infect Genet Evol. 2002; 2:39-45.
• [23]Dimitrov T, Dashti AA, Albaksami O, Udo EE, Jadaon MM, Albert MJ. Ciprofloxacin-resistant Salmonella enterica serovar typhi from Kuwait with novel mutations in gyrA and parC genes. J Clin Microbiol. 2009; 47:208-11.
• [24]Baker S, Duy PT, Nga TV, Dung TT, Phat VV, Chau TT et al.. Fitness benefits in fluoroquinolone-resistant Salmonella Typhi in the absence of antimicrobial pressure. Elife. 2013; 2:e01229.
• [25]Holt KE, Dolecek C, Chau TT, Duy PT, La TT, Hoang NV et al.. Temporal fluctuation of multidrug resistant Salmonella typhi haplotypes in the Mekong river delta region of Vietnam. PLoS Negl Trop Dis. 2011; 5:e929.
• [26]Giraud E, Baucheron S, Cloeckaert A. Resistance to fluoroquinolones in Salmonella: emerging mechanisms and resistance prevention strategies. Microbes Infect. 2006; 8:1937-44.
• [27]Baucheron S, Monchaux I, Le Hello S, Weill FX, Cloeckaert A. Lack of efflux mediated quinolone resistance in Salmonella enterica serovars Typhi and Paratyphi A. Front Microbiol. 2014; 5:12.
• [28]Lunguya O, Lejon V, Phoba MF, Bertrand S, Vanhoof R, Verhaegen J et al.. Salmonella typhi in the Democratic Republic of the Congo: fluoroquinolone decreased susceptibility on the rise. PLoS Negl Trop Dis. 2012; 6:e1921.
• [29]Geetha VK, Yugendran T, Srinivasan R, Harish BN. Plasmid-mediated quinolone resistance in typhoidal Salmonellae: a preliminary report from South India. Indian J Med Microbiol. 2014; 32:31-4.
• [30]Dahiya S, Kapil A, Kumar R, Das BK, Sood S, Chaudhry R et al.. Multiple locus sequence typing of Salmonella Typhi, isolated in North India - a preliminary study. Indian J Med Res. 2013; 137:957-62.