Skip to main content

Advertisement

Log in

Characterization of the emerging clinically-relevant multidrug-resistant Salmonella enterica serotype 4,[5],12:i:- (monophasic variant of S. Typhimurium) clones

  • Article
  • Published:
European Journal of Clinical Microbiology & Infectious Diseases Aims and scope Submit manuscript

Abstract

To better understand the recent success/emergence of Salmonella enterica serotype 4,[5],12:i:- we characterized the population diversity, fljAB deletion patterns, antibiotic resistance features and associated genetic elements of a comprehensive collection obtained in the last decade from Portugal (2002–2010). One hundred thirty-one isolates from human clinical specimens, food, environment and piggeries, verified by PCR as S. 4,[5],12:i:-, were studied for clonality (Pulsed-Field Gel Electrophoresis and Multilocus Sequence Typing), antibiotic resistance by phenotypic (disk diffusion and/or agar dilution) and genotypic (PCR/Restriction Fragment Length Polymorphism and sequencing, genomic location) methods and fljAB-deletions (PCR). Plasmid analysis included determination of size, content and characterization of the incompatibility group (PCR-Based Replicon Typing and I-CeuI/S1-hybridization). Results showed three multidrug-resistant (MDR) clones circulating and causing infections, associated with particular phenotypic and genotypic features. Most of the isolates belonged to the widespread European (ASSuT phenotype, RR1-RR2 resistance regions, ST34) and Spanish (carrying a sul3-type III integron within IncA/C plasmids, ST19) clones circulating in Europe. A third clone, here designated Southern European clone (carrying a sul3-type I integron within IncR plasmids, ST19), presents a fljAB region different from the previous clones and similar to the US strains, despite differences in the MDR mobile genetic platforms. The success of S. 4,[5],12:i:- might be related to the selective advantage offered by MDR profiles associated with stable genetic elements, also carrying virulence features, along with well adapted clones to the animal food production and causing human infections.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. European Food Safety Authority (2014) The European union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2012. EFSA J 12(2):35–47

    Google Scholar 

  2. Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O'Brien SJ, Jones TF, Fazil A, Hoekstra RM (2010) The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis 50(6):882–889

    Article  PubMed  Google Scholar 

  3. European Food Safety Authority (2010) EFSA panel on biological hazards (BIOHAZ): Scientific opinion on monitoring and assessment of the public health risk of “Salmonella Typhimurium-like” strains. EFSA J 8(10):1826

    Google Scholar 

  4. Hopkins KL, Kirchner M, Guerra B, Granier SA, Lucarelli C, Porrero MC, Jakubczak A, Threlfall EJ, Mevius DJ (2010) Multiresistant Salmonella enterica serovar 4,[5],12:i:- in Europe: a new pandemic strain? Euro Surveill 15(22):19580

    CAS  PubMed  Google Scholar 

  5. Switt AI, Soyer Y, Warnick LD, Wiedmann M (2009) Emergence, distribution, and molecular and phenotypic characteristics of Salmonella enterica serotype 4,5,12:i:-. Foodborne Pathog Dis 6(4):407–415

    Article  PubMed  PubMed Central  Google Scholar 

  6. Gossner CM, van Cauteren D, Le Hello S, Weill FX, Terrien E, Tessier S, Janin C, Brisabois A, Dusch V, Vaillant V, Jourdan-da Silva N (2012) Nationwide outbreak of Salmonella enterica serotype 4,[5],12:i:- infection associated with consumption of dried pork sausage, France, November to December 2011. Euro Surveill 17(5)

  7. Raguenaud ME, Le Hello S, Salah S, Weill FX, Brisabois A, Delmas G, Germonneau P (2012) Epidemiological and microbiological investigation of a large outbreak of monophasic Salmonella Typhimurium 4,5,12:i:- in schools associated with imported beef in Poitiers, France, October 2010. Euro Surveill 17(40):20289

    CAS  PubMed  Google Scholar 

  8. Antunes P, Mourão J, Pestana N, Peixe L (2011) Leakage of emerging clinically relevant multidrug-resistant Salmonella clones from pig farms. J Antimicrob Chemother 66(9):2028–2032

    Article  CAS  PubMed  Google Scholar 

  9. Hauser E, Tietze E, Helmuth R, Junker E, Blank K, Prager R, Rabsch W, Appel B, Fruth A, Malorny B (2010) Pork contaminated with Salmonella enterica serovar 4,[5],12:i:-, an emerging health risk for humans. Appl Environ Microbiol 76(14):4601–4610

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Garcia P, Guerra B, Bances M, Mendoza MC, Rodicio MR (2011) IncA/C plasmids mediate antimicrobial resistance linked to virulence genes in the Spanish clone of the emerging Salmonella enterica serotype 4,[5],12:i:-. J Antimicrob Chemother 66(3):543–549

    Article  CAS  PubMed  Google Scholar 

  11. Lucarelli C, Dionisi AM, Filetici E, Owczarek S, Luzzi I, Villa L (2012) Nucleotide sequence of the chromosomal region conferring multidrug resistance (R-type ASSuT) in Salmonella Typhimurium and monophasic Salmonella Typhimurium strains. J Antimicrob Chemother 67(1):111–114

    Article  CAS  PubMed  Google Scholar 

  12. Garcia P, Hopkins KL, Garcia V, Beutlich J, Mendoza MC, Threlfall J, Mevius D, Helmuth R, Rodicio MR, Guerra B, Med-Vet-Net WPPG (2014) Diversity of plasmids encoding virulence and resistance functions in Salmonella enterica subsp. enterica Serovar Typhimurium monophasic variant 4,[5],12:i:- Strains circulating in Europe. PLoS One 9(2):e89635

    Article  PubMed  PubMed Central  Google Scholar 

  13. Soyer Y, Moreno Switt A, Davis MA, Maurer J, McDonough PL, Schoonmaker-Bopp DJ, Dumas NB, Root T, Warnick LD, Grohn YT, Wiedmann M (2009) Salmonella enterica serotype 4,5,12:i:-, an emerging Salmonella serotype that represents multiple distinct clones. J Clin Microbiol 47(11):3546–3556

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Council Regulation (EC) No. 517/2011 of 25 May 2011 implementing Regulation (EC) No 2160/2003 of the European Parliament and of the Council as regards a Union target for the reduction of the prevalence of certain Salmonella serotypes in laying hens of Gallus gallus and amending Regulation (EC) No 2160/2003 and Commission Regulation (EU) No 200/2010. Official Journal of the European Communities L138/45

  15. Tennant SM, Diallo S, Levy H, Livio S, Sow SO, Tapia M, Fields PI, Mikoleit M, Tamboura B, Kotloff KL, Nataro JP, Galen JE, Levine MM (2010) Identification by PCR of non-typhoidal Salmonella enterica serovars associated with invasive infections among febrile patients in Mali. PLoS Negl Trop Dis 4(3):e621

    Article  PubMed  PubMed Central  Google Scholar 

  16. Pritchett LC, Konkel ME, Gay JM, Besser TE (2000) Identification of DT104 and U302 phage types among Salmonella enterica serotype typhimurium isolates by PCR. J Clin Microbiol 38(9):3484–3488

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Clinical and Laboratory Standards Institute (CLSI) (2013) Performance standards for antimicrobial susceptibility testing: twenty-first informational supplement M100-S23. CLSI, Wayne, IN, USA

    Google Scholar 

  18. Antunes P, Machado J, Peixe L (2006) Characterization of antimicrobial resistance and class 1 and 2 integrons in Salmonella enterica isolates from different sources in Portugal. J Antimicrob Chemother 58(2):297–304

    Article  CAS  PubMed  Google Scholar 

  19. Antunes P, Machado J, Peixe L (2007) Dissemination of sul3-containing elements linked to class 1 integrons with an unusual 3′ conserved sequence region among Salmonella isolates. Antimicrob Agents Chemother 51(4):1545–1548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Carattoli A, Bertini A, Villa L, Falbo V, Hopkins KL, Threlfall EJ (2005) Identification of plasmids by PCR-based replicon typing. J Microbiol Methods 63(3):219–228

    Article  CAS  PubMed  Google Scholar 

  21. Garcia-Fernandez A, Fortini D, Veldman K, Mevius D, Carattoli A (2009) Characterization of plasmids harbouring qnrS1, qnrB2 and qnrB19 genes in Salmonella. J Antimicrob Chemother 63(2):274–281

    Article  CAS  PubMed  Google Scholar 

  22. Silveira L, Marques A, Machado J (2013) Infecções por Salmonella enterica no período entre 2000–2012. Boletim Epidemiológico do Instituto Nacional de Saúde Dr Ricardo Jorge 2013. http://repositorio.insa.pt//. Accessed 08 April 2014

  23. European Medicines Agency, European Surveillance of Veterinary Antimicrobial Consumption (2013) Sales of veterinary antimicrobial agents in 25 EU/EEA countries in 2011. EMA/236501/2013

  24. DANMAP (2012) Use of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Bacteria from Food Animals, Foods and Humans in Denmark. http://www.danmap.org/. Accessed 08 April 2014

  25. Lucarelli C, Dionisi AM, Torpdahl M, Villa L, Graziani C, Hopkins K, Threlfall J, Caprioli A, Luzzi I (2010) Evidence for a second genomic island conferring multidrug resistance in a clonal group of strains of Salmonella enterica serovar Typhimurium and its monophasic variant circulating in Italy, Denmark, and the United Kingdom. J Clin Microbiol 48(6):2103–2109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Mandilara G, Lambiri M, Polemis M, Passiotou M, Vatopoulos A (2013) Phenotypic and molecular characterisation of multiresistant monophasic Salmonella Typhimurium (1,4,[5],12:i:-) in Greece, 2006 to 2011. Euro Surveill 18(22)

  27. Mulvey MR, Finley R, Allen V, Ang L, Bekal S, El Bailey S, Haldane D, Hoang L, Horsman G, Louie M, Robberts L, Wylie J, McCracken M, Langner S, Ahmed R, Tabor H, Gilmour M (2013) Emergence of multidrug-resistant Salmonella enterica serotype 4,[5],12:i:- involving human cases in Canada: results from the Canadian integrated program on antimicrobial resistance surveillance (CIPARS), 2003–10. J Antimicrob Chemother 68(9):1982–1986

    Article  CAS  PubMed  Google Scholar 

  28. European Food Safety Authority (2011) Scientific report of EFSA: analysis of the baseline survey of Salmonella in holdings with breeding pigs, in the EU, 2008; Part B: analysis of factors potentially associated with Salmonella pen positivity. EFSA J 9(7):2329

  29. Garcia P, Malorny B, Hauser E, Mendoza MC, Rodicio MR (2013) Genetic types, gene repertoire, and evolution of isolates of the Salmonella enterica serovar 4,5,12:i:- Spanish clone assigned to different phage types. J Clin Microbiol 51(3):973–978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Carattoli A (2009) Resistance plasmid families in Enterobacteriaceae. Antimicrob Agents Chemother 53(6):2227–2238

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Novais A, Rodrigues C, Branquinho R, Antunes P, Grosso F, Boaventura L, Ribeiro G, Peixe L (2012) Spread of an OmpK36-modified ST15 Klebsiella pneumoniae variant during an outbreak involving multiple carbapenem-resistant Enterobacteriaceae species and clones. Eur J Clin Microbiol Infect Dis 31(11):3057–3063

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors wish to thank Claudia Lucarelli for kindly providing the XbaI PFGE profiles designated according to PulseNet for comparison and to Laura Dias, Liliana Ferreira and Tatiana Alves for technical assistance. This study was funded by research grants from the Fundação para a Ciência e a Tecnologia (PEst-C/EQB/LA0006/2013) and Investigação Jovem da Universidade do Porto/Santander Totta (PP_IJUP2010-17). Joana Mourão was supported by a Ph.D. fellowship from Fundação para a Ciência e a Tecnologia (grant number SFRH/BD/77518/2011; POPH-QREN).

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to P. Antunes.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 457 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mourão, J., Machado, J., Novais, C. et al. Characterization of the emerging clinically-relevant multidrug-resistant Salmonella enterica serotype 4,[5],12:i:- (monophasic variant of S. Typhimurium) clones. Eur J Clin Microbiol Infect Dis 33, 2249–2257 (2014). https://doi.org/10.1007/s10096-014-2180-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10096-014-2180-1

Keywords

Navigation