1887
Research article Open Access
Like 0

Abstract

Background and aim

Epidemiology of human non-typhoid salmonellosis is characterised by recurrent emergence of new clones of the pathogen over time. Some clonal lines of have shaped epidemiology of the disease at global level, as happened for serotype Enteritidis or, more recently, for 4,[5],12:i:-, a monophasic variant of serotype Typhimurium. The same clonal behaviour is recognisable at sub-serotype level where single outbreaks or more generalised epidemics are attributable to defined clones. The aim of this study was to understand the dynamics of a clone of 4,[5],12:i:- over a 3-year period (2012–15) in a province of Northern Italy where the clone caused a large outbreak in 2013. Furthermore, the role of candidate outbreak sources was investigated and the accuracy of multilocus variable-number tandem repeat analysis (MLVA) was evaluated. we retrospectively investigated the outbreak through whole genome sequencing (WGS) and further monitored the outbreak clone for 2 years after its conclusion. The study showed the transient nature of the clone in the population, possibly as a consequence of its occasional expansion in a food-processing facility. We demonstrated that important weaknesses characterise conventional typing methods applied to clonal pathogens such as 4,[5],12:i:-, namely lack of accuracy for MLVA and inadequate resolution power for PFGE to be reliably used for clone tracking. : The study provided evidence for the remarkable prevention potential of whole genome sequencing used as a routine tool in systems that integrate human, food and animal surveillance.

Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2018.23.13.17-00375
2018-03-29
2018-08-20
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2018.23.13.17-00375
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/23/13/eurosurv-23-13-4.html?itemId=/content/10.2807/1560-7917.ES.2018.23.13.17-00375&mimeType=html&fmt=ahah

References

  1. Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O’Brien SJ, et al. The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis. 2010;50(6):882-9.  https://doi.org/10.1086/650733  PMID: 20158401 
  2. European Food Safety Authority (EFSA) / European Centre for Disease Prevention and Control (ECDC). The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2013. EFSA J. 2015;13(1):3991.  https://doi.org/10.2903/j.efsa.2015.3991 
  3. O’Brien SJ. The ‘decline and fall’ of nontyphoidal salmonella in the United Kingdom. Clin Infect Dis. 2013;56(5):705-10.  https://doi.org/10.1093/cid/cis967  PMID: 23166188 
  4. Ward LR, Threlfall J, Smith HR, O’Brien SJ. Salmonella enteritidis epidemic. Science. 2000;287(5459):1753-4, author reply 1755-6.  https://doi.org/10.1126/science.287.5459.1753c  PMID: 10755925 
  5. European Food Safety Authority (EFSA) / European Centre for Disease Prevention and Control (ECDC). The European Union Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents and Food-borne Outbreaks in 2012. EFSA J. 2014;12(2):3547.  https://doi.org/10.2903/j.efsa.2014.3547 
  6. European Food Safety Authority (EFSA), European Centre for Disease Prevention and Control (ECDC). The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2014. EFSA J. 2015;13(12):4329.  https://doi.org/10.2903/j.efsa.2015.4329 
  7. Cito F, Baldinelli F, Calistri P, Di Giannatale E, Scavia G, Orsini M, et al. Outbreak of unusual Salmonella enterica serovar Typhimurium monophasic variant 1,4 [5],12:i:-, Italy, June 2013 to September 2014. Euro Surveill. 2016;21(15):30194.  https://doi.org/10.2807/1560-7917.ES.2016.21.15.30194  PMID: 27105170 
  8. Barco L, Ramon E, Cortini E, Longo A, Dalla Pozza MC, Lettini AA, et al. Molecular characterization of Salmonella enterica serovar 4,[5],12:i:- DT193 ASSuT strains from two outbreaks in Italy. Foodborne Pathog Dis. 2014;11(2):138-44.  https://doi.org/10.1089/fpd.2013.1626  PMID: 24328499 
  9. Olson AB, Andrysiak AK, Tracz DM, Guard-Bouldin J, Demczuk W, Ng LK, et al. Limited genetic diversity in Salmonella enterica serovar Enteritidis PT13. BMC Microbiol. 2007;7(1):87.  https://doi.org/10.1186/1471-2180-7-87  PMID: 17908316 
  10. Allard MW, Luo Y, Strain E, Pettengill J, Timme R, Wang C, et al. On the evolutionary history, population genetics and diversity among isolates of Salmonella Enteritidis PFGE pattern JEGX01.0004. PLoS One. 2013;8(1):e55254.  https://doi.org/10.1371/journal.pone.0055254  PMID: 23383127 
  11. García P, Malorny B, Rodicio MR, Stephan R, Hächler H, Guerra B, et al. Horizontal Acquisition of a Multidrug-Resistance Module (R-type ASSuT) Is Responsible for the Monophasic Phenotype in a Widespread Clone of Salmonella Serovar 4,[5],12:i. Front Microbiol. 2016;7:680.  https://doi.org/10.3389/fmicb.2016.00680  PMID: 27242707 
  12. Hopkins KL, Kirchner M, Guerra B, Granier SA, Lucarelli C, Porrero MC, et al. Multiresistant Salmonella enterica serovar 4,[5],12:i:- in Europe: a new pandemic strain? Euro Surveill. 2010;15(22):19580. PMID: 20546690 
  13. Hauser E, Tietze E, Helmuth R, Junker E, Blank K, Prager R, et al. Pork contaminated with Salmonella enterica serovar 4,[5],12:i:-, an emerging health risk for humans. Appl Environ Microbiol. 2010;76(14):4601-10.  https://doi.org/10.1128/AEM.02991-09  PMID: 20472721 
  14. Gallati C, Stephan R, Hächler H, Malorny B, Schroeter A, Nüesch-Inderbinen M. Characterization of Salmonella enterica subsp. enterica serovar 4,[5],12:i:- clones isolated from human and other sources in Switzerland between 2007 and 2011. Foodborne Pathog Dis. 2013;10(6):549-54.  https://doi.org/10.1089/fpd.2012.1407  PMID: 23614800 
  15. Italian National Institute of Statistics (Istat). Resident population on 1st January. Rome: Istat. [Accessed 27 Sep 2017]. Available from: http://dati.istat.it/Index.aspx?lang=en&SubSessionId=0579ebed-fa5c-4c91-bc67-1ec73751e213&themetreeid=21
  16. Frisén M, Andersson E, Pettersson K. Semiparametric estimation of outbreak regression. Statistics. 2010;44(2):107-17.  https://doi.org/10.1080/02331880903021484 
  17. Tauxe RV. Molecular subtyping and the transformation of public health. Foodborne Pathog Dis. 2006;3(1):4-8.  https://doi.org/10.1089/fpd.2006.3.4  PMID: 16602974 
  18. Höhle M, Meyer S, Paul M. Surveillance: Temporal and Spatio-Temporal Modelling and Monitoring of Epidemic Phenomena. 2015; R package version 1.9-1. [Accessed 9 Jun 2017]. Available from: http://CRAN.R-project.org/package=surveillance
  19. European Food Safety Authority (EFSA). Manual for reporting on food-borne outbreaks in accordance with Directive 2003/99/EC for information derived from the year 2012. Parma: EFSA; 2012. Available from: http://onlinelibrary.wiley.com/doi/10.2903/sp.efsa.2012.EN-265/epdf
  20. European Commission. Regulation (EC) n. 2073/2005 on Microbiological criteria for foodstuffs. Luxembourg: Publications Office of the European Union. 22.12.2005:L 338/1. Available from: http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2005:338:0001:0026:EN:PDF
  21. International Organization for Standardization (ISO). Detection of Salmonella spp. in animal faeces and in environmental samples from the primary production stage. ISO 6579:2002/Amd 1:2007. Geneva: ISO; July 2007. Available from: https://www.iso.org/standard/42109.html
  22. Barco L, Lettini AA, Ramon E, Longo A, Saccardin C, Pozza MC, et al. A rapid and sensitive method to identify and differentiate Salmonella enterica serotype Typhimurium and Salmonella enterica serotype 4,[5],12:i:- by combining traditional serotyping and multiplex polymerase chain reaction. Foodborne Pathog Dis. 2011;8(6):741-3.  https://doi.org/10.1089/fpd.2010.0776  PMID: 21247297 
  23. Centre for Disease Prevention and Control (CDC). Standard Operating Procedure for PulseNet PFGE of Escherichia coli O157:H7, Escherichia coli non-O157 (STEC), Salmonella serotypes, Shigella sonnei and Shigella flexneri; Atlanta: CDC; 2013. Available from: http://www.cdc.gov/pulsenet/pdf/ecoli-shigella-salmonella-pfge-protocol-508c.pdf
  24. Lindstedt BA, Vardund T, Aas L, Kapperud G. Multiple-locus variable-number tandem-repeats analysis of Salmonella enterica subsp. enterica serovar Typhimurium using PCR multiplexing and multicolor capillary electrophoresis. J Microbiol Methods. 2004;59(2):163-72.  https://doi.org/10.1016/j.mimet.2004.06.014  PMID: 15369852 
  25. Larsson JT, Torpdahl M, Petersen RF, Sorensen G, Lindstedt BA, Nielsen EM. Development of a new nomenclature for Salmonella typhimurium multilocus variable number of tandem repeats analysis (MLVA). Euro Surveill. 2009;14(15):14. PMID: 19371515 
  26. Chevreux B, Wetter T, Suhai S. Genome Sequence Assembly Using Trace Signals and Additional Sequence Information. Computer science and biology: Proceedings of German conference on bioinformatics (GCB); 1999.
  27. Pettengill JB, Luo Y, Davis S, Chen Y, Gonzalez-Escalona N, Ottesen A, et al. An evaluation of alternative methods for constructing phylogenies from whole genome sequence data: a case study with Salmonella. PeerJ. 2014;2:e620.  https://doi.org/10.7717/peerj.620  PMID: 25332847 
  28. Huelsenbeck JP, Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 2001;17(8):754-5.  https://doi.org/10.1093/bioinformatics/17.8.754  PMID: 11524383 
  29. Bauer AW, Kirby WM, Sherris JC, Turck M. Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol. 1966;45(4):493-6.  https://doi.org/10.1093/ajcp/45.4_ts.493  PMID: 5325707 
  30. Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S, Lund O, et al. Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother. 2012;67(11):2640-4.  https://doi.org/10.1093/jac/dks261  PMID: 22782487 
  31. Hopkins KL, Davies RH, Threlfall EJ. Mechanisms of quinolone resistance in Escherichia coli and Salmonella: recent developments. Int J Antimicrob Agents. 2005;25(5):358-73.  https://doi.org/10.1016/j.ijantimicag.2005.02.006  PMID: 15848289 
  32. Boland C, Bertrand S, Mattheus W, Dierick K, Jasson V, Rosseel T, et al. Extensive genetic variability linked to IS26 insertions in the fljB promoter region of atypical monophasic variants of Salmonella enterica serovar Typhimurium. Appl Environ Microbiol. 2015;81(9):3169-75.  https://doi.org/10.1128/AEM.00270-15  PMID: 25724958 
  33. Lucarelli C, Dionisi AM, Filetici E, Owczarek S, Luzzi I, Villa L. Nucleotide sequence of the chromosomal region conferring multidrug resistance (R-type ASSuT) in Salmonella Typhimurium and monophasic Salmonella Typhimurium strains. J Antimicrob Chemother. 2012;67(1):111-4.  https://doi.org/10.1093/jac/dkr391  PMID: 21990047 
  34. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014;30(14):2068-9.  https://doi.org/10.1093/bioinformatics/btu153  PMID: 24642063 
  35. Tennant SM, Diallo S, Levy H, Livio S, Sow SO, Tapia M, et al. Identification by PCR of non-typhoidal Salmonella enterica serovars associated with invasive infections among febrile patients in Mali. PLoS Negl Trop Dis. 2010;4(3):e621.  https://doi.org/10.1371/journal.pntd.0000621  PMID: 20231882 
  36. Scaltriti E, Sassera D, Comandatore F, Morganti M, Mandalari C, Gaiarsa S, et al. Differential single nucleotide polymorphism-based analysis of an outbreak caused by Salmonella enterica serovar Manhattan reveals epidemiological details missed by standard pulsed-field gel electrophoresis. J Clin Microbiol. 2015;53(4):1227-38.  https://doi.org/10.1128/JCM.02930-14  PMID: 25653407 
  37. Dimovski K, Cao H, Wijburg OL, Strugnell RA, Mantena RK, Whipp M, et al. Analysis of Salmonella enterica serovar Typhimurium variable-number tandem-repeat data for public health investigation based on measured mutation rates and whole-genome sequence comparisons. J Bacteriol. 2014;196(16):3036-44.  https://doi.org/10.1128/JB.01820-14  PMID: 24957617 
  38. Petersen RF, Litrup E, Larsson JT, Torpdahl M, Sørensen G, Müller L, et al. Molecular characterization of Salmonella Typhimurium highly successful outbreak strains. Foodborne Pathog Dis. 2011;8(6):655-61.  https://doi.org/10.1089/fpd.2010.0683  PMID: 21381921 
  39. Wuyts V, Mattheus W, De Laminne de Bex G, Wildemauwe C, Roosens NH, Marchal K, et al. MLVA as a tool for public health surveillance of human Salmonella Typhimurium: prospective study in Belgium and evaluation of MLVA loci stability. PLoS One. 2013;8(12):e84055.  https://doi.org/10.1371/journal.pone.0084055  PMID: 24391880 
  40. Lienau EK, Strain E, Wang C, Zheng J, Ottesen AR, Keys CE, et al. Identification of a salmonellosis outbreak by means of molecular sequencing. N Engl J Med. 2011;364(10):981-2.  https://doi.org/10.1056/NEJMc1100443  PMID: 21345093 
  41. Octavia S, Wang Q, Tanaka MM, Kaur S, Sintchenko V, Lan R. Delineating community outbreaks of Salmonella enterica serovar Typhimurium by use of whole-genome sequencing: insights into genomic variability within an outbreak. J Clin Microbiol. 2015;53(4):1063-71.  https://doi.org/10.1128/JCM.03235-14  PMID: 25609719 
  42. Wuyts V, Denayer S, Roosens NH, Mattheus W, Bertrand S, Marchal K, et al. Whole Genome Sequence Analysis of Salmonella Enteritidis PT4 Outbreaks from a National Reference Laboratory’s Viewpoint. PLoS Curr. 2015;7:10. PMID: 26468422 
/content/10.2807/1560-7917.ES.2018.23.13.17-00375
Loading

Data & Media loading...

Comment has been disabled for this content
Submit comment
Close
Comment moderation successfully completed
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error