1887

Abstract

Extended-spectrum cephalosporins and fluoroquinolones are essential antimicrobials for treating invasive salmonellosis, although emerging resistance to these antimicrobials is of growing concern, especially in India. Therefore, a study was conducted to characterize the antimicrobial susceptibility phenotypes, types of extended-spectrum -lactamase (ESBL) gene plasmids and serological relationships of 21 non-typhoidal isolates from patients who attended three different hospitals in India from 2006 to 2008. The isolates were cultured from stool, blood and cerebrospinal fluid samples obtained from patients presenting with diarrhoea and accompanying systemic manifestations such as fever, vomiting and meningism. Non-typhoidal isolates were investigated using serotyping and antimicrobial susceptibility testing. PCR screening was also performed to detect the -lactamase, and genes and class 1 integrons. Sequencing for quinolone resistance mutations and plasmid replicon typing were also performed. An antimicrobial resistance microarray was used for preliminary screening and identification of and genes, and phenotypic testing for the presence of efflux pumps was also performed. Ten out of 21 isolates (48 %) possessed the extended-spectrum cephalosporin resistance phenotype, with PCR amplification and sequencing revealing that isolates possessed TEM-1, SHV-12, DHA-1, OXA-1-like and CTX-M-15 ESBL genes. FII plasmid replicons were detected in seven isolates (33 %). The involvement of efflux pumps was detected in four isolates (19 %) resistant to ciprofloxacin. It was concluded that SHV-12-carrying serotype Agona may play an important role in ESBL-mediated resistance in non-typhoidal salmonellae in India. The very high percentage (48 %) of ESBL-producing non-typhoidal salmonellae isolated from these patients represents a real and immediate challenge to the effective antimicrobial therapy of infections associated with systemic manifestations. Continued surveillance for the presence of ESBL-producing (non-typhoidal) salmonellae in India is essential.

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2010-12-01
2019-08-21
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References

  1. Asensi, M. D., Solari, C. A. & Hofer, E. ( 1994; ). A Salmonella Agona outbreak in a pediatric hospital in the city of Rio de Janeiro, Brazil. Mem Inst Oswaldo Cruz 89, 1–4.[CrossRef]
    [Google Scholar]
  2. Carattoli, A., Bertini, A., Villaa, L., Falbo, V., Hopkins, K. L. & Threlfall, E. J. ( 2005; ). Identification of plasmids by PCR-based replicon typing. J Microbiol Methods 63, 219–228.[CrossRef]
    [Google Scholar]
  3. Eckert, C., Gautier, V., Saladin-Allard, M., Hidri, N., Verdet, C., Ould-Hocine, Z., Barnaud, G., Delisle, F., Rossier, A. & other authors ( 2004; ). Dissemination of CTX-M-type β-lactamases among clinical isolates of Enterobacteriaceae in Paris, France. Antimicrob Agents Chemother 48, 1249–1255.[CrossRef]
    [Google Scholar]
  4. Giraud, E., Brisabois, A., Martel, J. L. & Chaslus-Dancla, E. ( 1999; ). Comparative studies of mutations in animal isolates and experimental in vitro- and in vivo-selected mutants of Salmonella spp. suggest a counterselection of highly fluoroquinolone-resistant strains in the field. Antimicrob Agents Chemother 43, 2131–2137.
    [Google Scholar]
  5. Gniadkowski, M. ( 2001; ). Evolution and epidemiology of extended-spectrum β-lactamases (ESBLs) and ESBL-producing microorganisms. Clin Microbiol Infect 7, 597–608.[CrossRef]
    [Google Scholar]
  6. Grimm, V., Ezaki, S., Susa, M., Cornelius, K., Schmid, R. D. & Bachmann, T. T. ( 2004; ). Use of DNA microarrays for rapid genotyping of TEM β-lactamases that confer resistance. J Clin Microbiol 42, 3766–3774.[CrossRef]
    [Google Scholar]
  7. Guerra, B., Soto, S., Helmuth, R. & Mendoza, M. C. ( 2002; ). Characterization of a self-transferable plasmid from Salmonella enterica serotype Typhimurium clinical isolates carrying two integron-borne gene cassettes together with virulence and drug resistance genes. Antimicrob Agents Chemother 46, 2977–2981.[CrossRef]
    [Google Scholar]
  8. Guinée, P. A., Kampelmacher, E. H. & Willems, H. M. ( 1961; ). Six new Salmonella types, isolated in Ghana (S. volta, S. agona, S. wa, S. techimani, S. mampong and S. tafo). Antonie van Leeuwenhoek 27, 469–472.[CrossRef]
    [Google Scholar]
  9. Hammami, A., Arlet, G., Redjeb, S. B., Grimont, F., Hassen, A. B., Rekik, A. & Philippon, A. ( 1991; ). Nosocomial outbreak of acute gastroenteritis in a neonatal intensive care unit in Tunisia caused by multiply drug resistant Salmonella Wien producing SHV-2 β-lactamase. Eur J Clin Microbiol Infect Dis 10, 641–646.[CrossRef]
    [Google Scholar]
  10. Jesudason, M., Kurian, T., Periera, S. M., Jayasheela, M. & Koshi, G. ( 1988; ). Isolation of Salmonella Agona (4, 12:f, g, s:) for the first time in India. Indian J Pathol Microbiol 31, 303–305.
    [Google Scholar]
  11. Karisik, E., Ellington, M. J., Pike, R., Warren, R. E., Livermore, D. M. & Woodford, N. ( 2006; ). Molecular characterization of plasmids encoding CTX-M-15 β-lactamase from Escherichia coli strains in the United Kingdom. J Antimicrob Chemother 58, 665–668.[CrossRef]
    [Google Scholar]
  12. Komp Lindgren, P., Karlsson, A. & Hughes, D. ( 2003; ). Mutation rate and evolution of fluoroquinolone resistance in Escherichia coli isolates from patients with urinary tract infections. Antimicrob Agents Chemother 47, 3222–3232.[CrossRef]
    [Google Scholar]
  13. Kumar, Y., Sharma, A., Sehgal, R. & Kumar, S. ( 2009; ). Distribution trends of Salmonella serovars in India (2001–2005). Trans R Soc Trop Med Hyg 103, 390–394.[CrossRef]
    [Google Scholar]
  14. Lévesque, C., Piché, L., Larose, C. & Roy, P. H. ( 1995; ). PCR mapping of integrons reveals several novel combinations of resistance genes. Antimicrob Agents Chemother 39, 185–191.[CrossRef]
    [Google Scholar]
  15. Miriagou, V., Tassios, P. T., Legakis, N. J. & Tzouvelekis, L. S. ( 2004; ). Expanded spectrum-cephalosporin resistance in non-typhoidal Salmonella. Int J Antimicrob Agents 23, 547–555.[CrossRef]
    [Google Scholar]
  16. Nath, G., Tikoo, A., Manocha, H., Tripathi, A. K. & Gulati, A. K. ( 2000; ). Drug resistance in Salmonella typhi in North India with special reference to ciprofloxacin. J Antimicrob Chemother 46, 149–150.[CrossRef]
    [Google Scholar]
  17. NCCLS ( 2000; ). Performance Standards for Antimicrobial Disk Susceptibility Tests; Approved Standard, 7th edn, M2-A7. Wayne, PA: National Committee for Clinical Laboratory Standards.
  18. Novais, A., Cantón, R., Valverde, A., Machado, E., Galán, J. C., Peixe, L., Carattoli, A., Baquero, F. & Coque, T. M. ( 2006; ). Dissemination and persistence of bla CTX-M-9 are linked to class 1 integrons containing CR1 associated with defective transposon derivatives from Tn402 located in early antibiotic resistance plasmids of IncH12, IncP1-α, and IncFI groups. Antimicrob Agents Chemother 50, 2741–2750.[CrossRef]
    [Google Scholar]
  19. Park, S. H., Seo, Y. H., Ahn, J. Y., Park, P. H., Kim, K. H., Song, Y. H. & Kim, J. E. ( 2010; ). Characteristics of CTX-M type extended spectrum β-lactamase producing non-typhoidal Salmonella isolates. Infect Chemother 42, 35–38.
    [Google Scholar]
  20. Paterson, D. L., Rice, L. B. & Bonomo, R. A. ( 2001; ). Rapid method of extraction and analysis of extended spectrum β-lactamases from clinical strains of Klebsiella pneumoniae. Clin Microbiol Infect 7, 709–711.[CrossRef]
    [Google Scholar]
  21. Pérez-Pérez, F. J. & Hanson, N. D. ( 2002; ). Detection of plasmid-mediated AmpC β-lactamase genes in clinical isolates by using multiplex PCR. J Clin Microbiol 40, 2153–2162.[CrossRef]
    [Google Scholar]
  22. Piddock, L. J. V., Whale, K. & Wise, R. ( 1990; ). Quinolone resistance in Salmonella: clinical experience. Lancet 335, 1459.
    [Google Scholar]
  23. Renuka, K., Kapil, A., Kabra, S. K., Wig, N., Das, B. K., Prasad, V. V., Chaudhry, R. & Seth, P. ( 2004; ). Reduced susceptibility to ciprofloxacin and gyrA gene mutation in North Indian strains of Salmonella enterica serotype Typhi and serotype Paratyphi A. Microb Drug Resist 10, 146–153.[CrossRef]
    [Google Scholar]
  24. Robicsek, A., Strahilevitz, J., Jacoby, G. A., Macielag, M., Abbanat, D., Park, C. H., Bush, K. & Hooper, D. C. ( 2006; ). Fluoroquinolone-modifying enzyme: a new adaptation of a common aminoglycoside acetyltransferase. Nat Med 12, 83–88.[CrossRef]
    [Google Scholar]
  25. Rotimi, V. O., Jamal, W., Pal, T., Sovenned, A. & Albert, M. J. ( 2008; ). Emergence of CTX-M-15 type extended-spectrum β-lactamase-producing Salmonella spp. in Kuwait and the United Arab Emirates. J Med Microbiol 57, 881–886.[CrossRef]
    [Google Scholar]
  26. Schumacher, A., Steinke, P., Bohnert, J. A., Akova, M., Jonas, D. & Kern, W. V. ( 2006; ). Effect of 1-(1-naphthylmethyl)-piperazine, a novel putative efflux pump inhibitor, on antimicrobial drug susceptibility in clinical isolates of Enterobacteriaceae other than Escherichia coli. J Antimicrob Chemother 57, 344–348.[CrossRef]
    [Google Scholar]
  27. Singhal, S., Mathur, T., Khan, S., Upadhyay, D. J., Chugh, S., Gaind, R. & Rattan, A. ( 2005; ). Evaluation of methods for AmpC β-lactamase in Gram negative clinical isolates from tertiary care hospitals. Indian J Med Microbiol 23, 120–124.[CrossRef]
    [Google Scholar]
  28. Taşli, H. & Bahar, I. H. ( 2005; ). Molecular characterisation of TEM- and SHV-derived extended spectrum β-lactamases in hospital-based Enterobacteriaceae in Turkey. Jpn J Infect Dis 58, 162–167.
    [Google Scholar]
  29. Tavechio, A. T., Ghilardi, A. C. R., Peresi, J. T. M., Fuzihara, T. O., Yonamine, E. K., Jakabi, M. & Fernandes, S. A. ( 2002; ). Salmonella serotypes isolated from nonhuman sources in Sao Paulo, Brazil, from 1996 through 2000. J Food Prot 65, 1041–1044.
    [Google Scholar]
  30. Threlfall, E. J. ( 2002; ). Antimicrobial drug resistance in Salmonella: problems and perspectives in food- and water-borne infections. FEMS Microbiol Rev 26, 141–148.[CrossRef]
    [Google Scholar]
  31. Verdet, C., Benzerara, Y., Gautier, V., Adam, O., Ould-Hocine, Z. & Arlet, G. ( 2006; ). Emergence of DHA-1-producing Klebsiella spp. in the Parisian region: genetic organization of the ampC and ampR genes originating from Morganella morganii. Antimicrob Agents Chemother 50, 607–617.[CrossRef]
    [Google Scholar]
  32. Wang, M., Sahm, D. F., Jacoby, G. A. & Hooper, D. C. ( 2004; ). Emerging plasmid-mediated quinolone resistance associated with the qnr gene in Klebsiella pneumoniae clinical isolates in the United States. Antimicrob Agents Chemother 48, 1295–1299.[CrossRef]
    [Google Scholar]
  33. Weill, F. X., Demartin, M., Tande, D., Espie, E., Rakotoarivony, I. & Grimont, P. A. ( 2004; ). SHV-12-like extended spectrum β-lactamase-producing strains of Salmonella enterica serotypes Babelsberg and Enteritidis isolated in France among infants adopted from Mali. J Clin Microbiol 42, 2432–2437.[CrossRef]
    [Google Scholar]
  34. Whichard, J. M., Gay, K. & Stevenson, J. E. ( 2007; ). Human Salmonella and concurrent decreased susceptibility to quinolones and extended-spectrum cephalosporins. Emerg Infect Dis 13, 1681–1688.[CrossRef]
    [Google Scholar]
  35. Woodford, N., Fagan, E. J. & Ellington, M. J. ( 2006; ). Multiplex PCR for rapid detection of genes encoding CTX-M extended-spectrum β-lactamases. J Antimicrob Chemother 57, 154–155.
    [Google Scholar]
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