Skip to main content
Log in

Comparative study of all Salmonella enterica serovar Enteritidis strains isolated from food and food animals in Greece from 2008 to 2010 with clinical isolates

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

Abstract

The aim of the present work was to study the epidemiology of Salmonella enterica serovar Enteritidis (S. Enteritidis) in Greece, comparing all the food and food animal isolates during a 3-year period with clinical isolates. Submission of the generated data to the PulseNet Europe database was carried out in order to study the population structure of this particular serovar and indicate possible connections with European strains. One hundred and sixty-eight (168) S. Enteritidis strains of human, animal, and food origin, isolated during the period 2008–2010 in Greece, were studied. Strains were characterized by phenotypic (antibiotic resistance) and molecular [pulsed-field gel electrophoresis (PFGE) and multilocus sequence typing (MLST)] methods. PFGE revealed 39 XbaI, 48 BlnI, and 80 XbaI–BlnI distinct pulsotypes, suggesting several clones circulating through the food chain and multiple sources of transmission. Submission to the PulseNet Europe database indicated that PFGE profile SENTXB.0001, the most common PFGE profile in Europe, was also predominant in Greece (33.3 %). MLST showed that all the strains studied shared the same sequence type (ST11), representing the most common ST in Europe. High rates of resistance to nalidixic acid were observed among human and poultry isolates (~25 %), indicating the potential fluoroquinolone treatment failure. Our data suggest that strains originating from multiple reservoirs circulated in Greece through the food chain during the study period. Predominant profiles in Greece were common to PulseNet Europe profiles, indicating similarities between the S. Enteritidis populations in Greece and Europe.

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.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Issenhuth-Jeanjean S, Roggentin P, Mikoleit M, Guibourdenche M, de Pinna E, Nair S, Fields PI, Weill FX (2014) Supplement 2008–2010 (no. 48) to the White–Kauffmann–Le Minor scheme. Res Microbiol 165(7):526–530. doi:10.1016/j.resmic.2014.07.004

    Article  PubMed  Google Scholar 

  2. European Food Safety Authority and European Centre for Disease Prevention and Control (2014) The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2012. EFSA J 12(2):3547. doi:10.2903/j.efsa.2014.3547

    Google Scholar 

  3. National School of Public Health and Hellenic Center for Disease Control and Prevention (2015) The Greek system for the surveillance of antimicrobial resistance. Home page at: http://www.mednet.gr/whonet/. Accessed 2 Nov 2015

  4. European Food Safety Authority and European Centre for Disease Prevention and Control (2015) The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2013. EFSA J 13(1):3991. doi:10.2903/j.efsa.2015.3991

    Google Scholar 

  5. Acheson D, Hohmann EL (2001) Nontyphoidal salmonellosis. Clin Infect Dis 32(2):263–269. doi:10.1086/318457

    Article  Google Scholar 

  6. Threlfall EJ, Ward LR, Skinner JA, Graham A (2000) Antimicrobial drug resistance in non-typhoidal salmonellas from humans in England and Wales in 1999: decrease in multiple resistance in Salmonella enterica serotypes Typhimurium, Virchow, and Hadar. Microb Drug Resist 6(4):319–325

    Article  CAS  PubMed  Google Scholar 

  7. Parry CM (2003) Antimicrobial drug resistance in Salmonella enterica. Curr Opin Infect Dis 16(5):467–472

    Article  CAS  PubMed  Google Scholar 

  8. Hyytiä-Trees EK, Cooper K, Ribot EM, Gerner-Smidt P (2007) Recent developments and future prospects in subtyping of foodborne bacterial pathogens. Future Microbiol 2(2):175–185. doi:10.2217/17460913.2.2.175

    Article  PubMed  Google Scholar 

  9. Hopkins KL, Peters TM, de Pinna E, Wain J (2011) Standardisation of multilocus variable-number tandem-repeat analysis (MLVA) for subtyping of Salmonella enterica serovar Enteritidis. Euro Surveill 16(32). pii: 19942

  10. Peters TM, Berghold C, Brown D, Coia J, Dionisi AM, Echeita A, Fisher IST, Gatto AJ, Gill N, Green J, Gerner-Smidt P, Heck M, Lederer I, Lukinmaa S, Luzzi I, Maguire C, Prager R, Usera M, Siitonen A, Threlfall EJ, Torpdahl M, Tschäpe H, Wannet W, van der Zwaluw WK (2007) Relationship of pulsed-field profiles with key phage types of Salmonella enterica serotype Enteritidis in Europe: results of an international multi-centre study. Epidemiol Infect 135(8):1274–1281. doi:10.1017/S0950268807008102

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Barrett TJ, Gerner-Smidt P, Swaminathan B (2006) Interpretation of pulsed-field gel electrophoresis patterns in foodborne disease investigations and surveillance. Foodborne Pathog Dis 3(1):20–31

    Article  CAS  PubMed  Google Scholar 

  12. Achtman M, Wain J, Weill FX, Nair S, Zhou Z, Sangal V, Krauland MG, Hale JL, Harbottle H, Uesbeck A, Dougan G, Harrison LH, Brisse S; S. Enterica MLST Study Group (2012) Multilocus sequence typing as a replacement for serotyping in Salmonella enterica. PLoS Pathog 8(6):e1002776

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Guibourdenche M, Roggentin P, Mikoleit M, Fields PI, Bockemühl J, Grimont PAD, Weill F-X (2010) Supplement 2003–2007 (No. 47) to the White-Kauffmann-Le Minor scheme. Res Microbiol 161(1):26–29. doi:10.1016/j.resmic.2009.10.002

    Article  PubMed  Google Scholar 

  14. Grimont PAD, Weill F (2007) Antigenic formulae of the Salmonella serovars. World Health Organization Collaborating Center for Reference and Research on Salmonella (ed). Institut Pasteur, Paris

  15. Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, Harbarth S, Hindler JF, Kahlmeter G, Olsson-Liljequist B, Paterson DL, Rice LB, Stelling J, Struelens MJ, Vatopoulos A, Weber JT, Monnet DL (2012) Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 18(3):268–281. doi:10.1111/j.1469-0691.2011.03570.x

    Article  CAS  PubMed  Google Scholar 

  16. Papadopoulos T, Petridou E, Zdragas A, Nair S, Peters T, de Pinna E, Mandilara G, Passiotou M, Vatopoulos A (2015) Phenotypic and molecular characterization of multidrug-resistant Salmonella enterica serovar Hadar in Greece, from 2007 to 2010. Clin Microbiol Infect 21(2):149.e1–149.e4

    Article  CAS  Google Scholar 

  17. Medalla F, Hoekstra RM, Whichard JM, Barzilay EJ, Chiller TM, Joyce K, Rickert R, Krueger A, Stuart A, Griffin PM (2013) Increase in resistance to ceftriaxone and nonsusceptibility to ciprofloxacin and decrease in multidrug resistance among Salmonella strains, United States, 1996–2009. Foodborne Pathog Dis 10(4):302–309. doi:10.1089/fpd.2012.1336

    Article  CAS  PubMed  Google Scholar 

  18. European Food Safety Authority and European Centre for Disease Prevention and Control (2014) The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2012. EFSA J 12(3):3590. doi:10.2903/j.efsa.2014.3590

    Google Scholar 

  19. Aarestrup FM, Wiuff C, Mølbak K, Threlfall EJ (2003) Is it time to change fluoroquinolone breakpoints for Salmonella spp.? Antimicrob Agents Chemother 47(2):827–829. doi:10.1128/aac.47.2.827-829.2003

    Article  CAS  PubMed  Google Scholar 

  20. European Committee on Antimicrobial Susceptibility Testing (EUCAST) (2014) European Society of Clinical Microbiology and Infectious Diseases (ESCMID). Home page at: http://www.eucast.org/

  21. European Centre for Disease Prevention and Control (ECDC) (2014) Surveillance of antimicrobial consumption in Europe 2012. ECDC, Stockholm

    Google Scholar 

  22. Allard MW, Luo Y, Strain E, Pettengill J, Timme R, Wang C, Li C, Keys CE, Zheng J, Stones R, Wilson MR, Musser SM, Brown EW (2013) On the evolutionary history, population genetics and diversity among isolates of Salmonella Enteritidis PFGE pattern JEGX01.0004. PLoS One 8(1):e55254. doi:10.1371/journal.pone.0055254

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Zheng J, Keys CE, Zhao S, Ahmed R, Meng J, Brown EW (2011) Simultaneous analysis of multiple enzymes increases accuracy of pulsed-field gel electrophoresis in assigning genetic relationships among homogeneous Salmonella strains. J Clin Microbiol 49(1):85–94. doi:10.1128/jcm.00120-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Ribot EM, Fair MA, Gautom R, Cameron DN, Hunter SB, Swaminathan B, Barrett TJ (2006) Standardization of pulsed-field gel electrophoresis protocols for the subtyping of Escherichia coli O157:H7, Salmonella, and Shigella for PulseNet. Foodborne Pathog Dis 3(1):59–67

    Article  CAS  PubMed  Google Scholar 

  25. Murase T, Nakamura A, Matsushima A, Yamai S (1996) An epidemiological study of Salmonella enteritidis by pulsed-field gel electrophoresis (PFGE): several PFGE patterns observed in isolates from a food poisoning outbreak. Microbiol Immunol 40(11):873–875

    Article  CAS  PubMed  Google Scholar 

  26. Noda T, Murakami K, Asai T, Etoh Y, Ishihara T, Kuroki T, Horikawa K, Fujimoto S (2011) Multi-locus sequence typing of Salmonella enterica subsp. enterica serovar Enteritidis strains in Japan between 1973 and 2004. Acta Vet Scand 53(1):38

    Article  PubMed  PubMed Central  Google Scholar 

  27. Köser CU, Ellington MJ, Cartwright EJP, Gillespie SH, Brown NM, Farrington M, Holden MTG, Dougan G, Bentley SD, Parkhill J, Peacock SJ (2012) Routine use of microbial whole genome sequencing in diagnostic and public health microbiology. PLoS Pathog 8(8), e1002824. doi:10.1371/journal.ppat.1002824

    Article  PubMed  PubMed Central  Google Scholar 

  28. den Bakker HC, Allard MW, Bopp D, Brown EW, Fontana J, Iqbal Z, Kinney A, Limberger R, Musser KA, Shudt M, Strain E, Wiedmann M, Wolfgang WJ (2014) Rapid whole-genome sequencing for surveillance of Salmonella enterica serovar enteritidis. Emerg Infect Dis J 20(8):1306–1314. doi:10.3201/eid2008.131399

    Article  Google Scholar 

  29. Ashton P, Nair S, Peters T, Tewolde R, Day M, Doumith M, Green J, Jenkins C, Underwood A, Arnold C, de Pinna E, Dallman T, Grant K (2015) Revolutionising public health reference microbiology using whole genome sequencing: Salmonella as an exemplar. bioRxiv. doi:10.1101/033225

    Google Scholar 

  30. Quick J, Ashton P, Calus S, Chatt C, Gossain S, Hawker J, Nair S, Neal K, Nye K, Peters T, De Pinna E, Robinson E, Struthers K, Webber M, Catto A, Dallman TJ, Hawkey P, Loman NJ (2015) Rapid draft sequencing and real-time nanopore sequencing in a hospital outbreak of Salmonella. Genome Biol 16(1):114. doi:10.1186/s13059-015-0677-2

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

The authors gratefully acknowledge the personnel of the National Veterinary Reference Centre for Salmonella in Chalkis, Greece, and also the personnel of the National Reference Centre for Salmonella in Vari, Greece, for providing and serotyping all the veterinary and human isolates, respectively. We also thank the administration and personnel of the Veterinary Research Institute (VRI-NAGREF, Thessaloniki) for their for laboratory assistance in the PFGE typing. Acknowledgments are also extended to the Salmonella Reference Service in Colindale, London, UK, for all the laboratory assistance during MLST and for submission to the PulseNet Europe database.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to T. Papadopoulos.

Ethics declarations

Funding

No specific funding was used for this research.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This research did not involve human participants and/or animals.

Informed consent

Not applicable.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Papadopoulos, T., Petridou, E., Zdragas, A. et al. Comparative study of all Salmonella enterica serovar Enteritidis strains isolated from food and food animals in Greece from 2008 to 2010 with clinical isolates. Eur J Clin Microbiol Infect Dis 35, 741–746 (2016). https://doi.org/10.1007/s10096-016-2591-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10096-016-2591-2

Keywords

Navigation