Genomic approaches used to investigate an atypical outbreak of Salmonella Adjame Open Access

Abstract

In 2017, an outbreak of gastroenteritis in England attributed to Salmonella Adjame was detected and investigated. With the introduction of whole genome sequencing (WGS) for microbial typing, methods for comparing international outbreak data require evaluation. A case was defined as a person resident in England with a clinical sample from 1 June 2017 to 27 July 2017 from whom S. Adjame was isolated. Cases were interviewed and exposures analysed. Backward tracing of food provenance was undertaken. WGS was performed on isolates from cases and historical isolates and compared using Public Health England’s SnapperDB high-quality SNP pipeline and Enterobase’s Salmonella core genome multi-locus sequence typing (cgMLST) scheme. In total, 14 cases were identified. The majority were vegetarian, probably of South Asian descent, with a median age of 66.5 years with no recent international travel reported. Cases consumed a range of fresh food products including herbs and spices bought from South Asian grocers. Backward tracing did not identify a common source. WGS typing showed sub-clustering and considerable genetic variation across human samples. cgMLST allele-based analysis was comparable to SNP-derived phylogenetic analysis and clusters were defined using each method. Imported herbs or spices were suspected vehicles. The cases were linked in time and place but WGS showed marked heterogeneity, atypical of a point source Salmonella outbreak. The application of incorporating SNP or allelic differences into the case definition may not always be appropriate. With further validation, cgMLST could be used for international outbreak alerts when WGS analysis is being undertaken to facilitate comparison.

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2019-01-16
2024-03-28
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References

  1. Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M et al. The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis 2010; 50:882–889 [View Article][PubMed]
    [Google Scholar]
  2. Le Minor L, Orio J, Lerat MT. [3 new Salmonella serotypes isolated in Ivory Coast: S. ebrie=35:g,m,t:-; S. cocody=(8), 20:r,i:e,n,z15; S. adjame=13,23:r:1,6]. Ann Inst Pasteur 1967; 112:661–663
    [Google Scholar]
  3. Dallman T, Ashton P, Schafer U, Jironkin A, Painset A et al. SnapperDB: a database solution for routine sequencing analysis of bacterial isolates. Bioinformatics 2018; 34:3028–3029 [View Article][PubMed]
    [Google Scholar]
  4. Kanagarajah S, Waldram A, Dolan G, Jenkins C, Ashton PM et al. Whole genome sequencing reveals an outbreak of Salmonella Enteritidis associated with reptile feeder mice in the United Kingdom, 2012-2015. Food Microbiol 2018; 71:32–38 [View Article][PubMed]
    [Google Scholar]
  5. Dallman T, Inns T, Jombart T, Ashton P, Loman N et al. Phylogenetic structure of European Salmonella Enteritidis outbreak correlates with national and international egg distribution network. Microb Genom 2016; 2:e000070 [View Article][PubMed]
    [Google Scholar]
  6. Ashton PM, Nair S, Peters TM, Bale JA, Powell DG et al. Identification of Salmonella for public health surveillance using whole genome sequencing. PeerJ 2016; 4:e1752 [View Article][PubMed]
    [Google Scholar]
  7. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article][PubMed]
    [Google Scholar]
  8. Tewolde R, Dallman T, Schaefer U, Sheppard CL, Ashton P et al. MOST: a modified MLST typing tool based on short read sequencing. PeerJ 2016; 4:e2308 [View Article][PubMed]
    [Google Scholar]
  9. Achtman M, Wain J, Weill FX, Nair S, Zhou Z et al. Multilocus sequence typing as a replacement for serotyping in Salmonella enterica. PLoS Pathog 2012; 8:e1002776 [View Article][PubMed]
    [Google Scholar]
  10. Issenhuth-Jeanjean S, Roggentin P, Mikoleit M, Guibourdenche M, de Pinna E et al. Supplement 2008-2010 (no. 48) to the White-Kauffmann-Le Minor scheme. Res Microbiol 2014; 165:526–530 [View Article][PubMed]
    [Google Scholar]
  11. Guibourdenche M, Roggentin P, Mikoleit M, Fields PI, Bockemühl J et al. Supplement 2003-2007 (No. 47) to the White-Kauffmann-Le Minor scheme. Res Microbiol 2010; 161:26–29 [View Article][PubMed]
    [Google Scholar]
  12. Grimont P, Weil F-X. Antigentic Formulae of the Salmonella Serovars, 9th ed. Institut Pasteur: WHO Collaborating Centre for Reference and Research on Salmonella; 2008
    [Google Scholar]
  13. Zhou Z, Lundstrøm I, Tran-Dien A, Duchêne S, Alikhan N-F et al. Millennia of genomic stability within the invasive Para C Lineage of Salmonella enterica. bioRxiv 2017
    [Google Scholar]
  14. Zhou Z, Alikhan NF, Sergeant MJ, Luhmann N, Vaz C et al. GrapeTree: visualization of core genomic relationships among 100,000 bacterial pathogens. Genome Res 2018; 28:1395–1404 [View Article][PubMed]
    [Google Scholar]
  15. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article][PubMed]
    [Google Scholar]
  16. Li H, Durbin R. Fast and accurate short read alignment with burrows-wheeler transform. Bioinformatics 2009; 25:1754–1760 [View Article][PubMed]
    [Google Scholar]
  17. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J et al. The sequence alignment/map format and SAMtools. Bioinformatics 2009; 25:2078–2079 [View Article][PubMed]
    [Google Scholar]
  18. Mckenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K et al. The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 2010; 20:1297–1303 [View Article][PubMed]
    [Google Scholar]
  19. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313 [View Article][PubMed]
    [Google Scholar]
  20. van Doren JM, Kleinmeier D, Hammack TS, Westerman A. Prevalence, serotype diversity, and antimicrobial resistance of Salmonella in imported shipments of spice offered for entry to the United States, FY2007-FY2009. Food Microbiol 2013; 34:239–251 [View Article][PubMed]
    [Google Scholar]
  21. Lehmacher A, Bockemühl J, Aleksic S. Nationwide outbreak of human salmonellosis in Germany due to contaminated paprika and paprika-powdered potato chips. Epidemiol Infect 1995; 115:501–511 [View Article][PubMed]
    [Google Scholar]
  22. Podolak R, Enache E, Stone W, Black DG, Elliott PH. Sources and risk factors for contamination, survival, persistence, and heat resistance of Salmonella in low-moisture foods. J Food Prot 2010; 73:1919–1936 [View Article][PubMed]
    [Google Scholar]
  23. US Food and Drug Administration 2013; United States Food and Drug Administration (US FDA) Risk Profile: Pathogen and Filth in Spices 2013. https://www.fda.gov/food/foodscienceresearch/risksafetyassessment/ucm367339.htm [accessed 14 December 2017]
  24. European Commission Rapid Alert System for Food and Feed 2017; European Commission Rapid Alert System for Food and Feed Portal. https://webgate.ec.europa.eu/rasff-window/portal/ [accessed 14 December 2017]
  25. Inns T, Ashton PM, Herrera-Leon S, Lighthill J, Foulkes S et al. Prospective use of whole genome sequencing (WGS) detected a multi-country outbreak of Salmonella enteritidis. Epidemiol Infect 2017; 145:289–298 [View Article][PubMed]
    [Google Scholar]
  26. EFSA (European Food Safety Authority) and ECDC (European Centre for Disease Prevention and Control) Multi-Country Outbreak of Salmonella Enteritidis Infections Linked to Polish Eggs 2017
    [Google Scholar]
  27. Allard MW, Strain E, Melka D, Bunning K, Musser SM et al. Practical value of food pathogen traceability through building a whole-genome sequencing network and database. J Clin Microbiol 2016; 54:1975–1983 [View Article][PubMed]
    [Google Scholar]
  28. Nadon C, Van Walle I, Gerner-Smidt P, Campos J, Chinen I et al. PulseNet International: Vision for the implementation of whole genome sequencing (WGS) for global food-borne disease surveillance. Euro Surveill 2017; 22:30544 [View Article][PubMed]
    [Google Scholar]
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