1887

Abstract

Infantis is one of the five serovars most frequently causing human salmonellosis in Europe, mainly associated with poultry. A clone harbouring a conjugative plasmid of emerging . Infantis (pESI)-like megaplasmid, carrying multidrug resistant (MDR) and extended-spectrum beta-lactamases (ESBL) genes, has spread in the Italian broiler chicken industry also causing human illness. This work is aimed at elucidating the molecular epidemiology of . Infantis and pESI-like in Europe using whole-genome sequencing and bioinformatics analysis, and to investigate the genetic relatedness of . Infantis clones and pESI-like from animals, meat, feed and humans provided by institutions of nine European countries. Two genotyping approaches were used: chromosome or plasmid SNP-based analysis and the minimum spanning tree (MST) algorithm based on core-genome multilocus sequence typing (cgMLST). The European . Infantis population appeared heterogeneous, with different genetic clusters defined at core-genome level. However, pESI-like variants present in 64.1 % of the isolates were more genetically homogeneous and capable of infecting different clonal lineages in most of the countries. Two different pESI-like with ESBL genes (=82) were observed: -positive in European isolates and -positive in American isolates (study outgroup). Both variants had toxin-antitoxin systems, resistance genes towards tetracyclines, trimethoprim, sulphonamides and aminoglycosides, heavy metals (A) and disinfectants (EΔ). Worryingly, 66 % of the total isolates studied presented different A chromosomal point mutations associated with (fluoro)quinolone resistance (MIC range 0.125–0.5 mg/L), while 18 % displayed transferable macrolide resistance mediated by , and (B) genes. Proper intervention strategies are needed to prevent further dissemination/transmission of MDR . Infantis and pESI-like along the food chain in Europe.

Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000365
2020-04-09
2020-06-04
Loading full text...

Full text loading...

/deliver/fulltext/mgen/6/5/mgen000365.html?itemId=/content/journal/mgen/10.1099/mgen.0.000365&mimeType=html&fmt=ahah

References

  1. EFSA (European Food Safety Authority) and ECDC (European Centre for Disease Prevention and Control), 2018 The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2017. EFSA Journal 2018; 16:5500
    [Google Scholar]
  2. EFSA (European Food Safety Authority) and ECDC (European Centre for Disease Prevention and Control), 2017 The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2016. EFSA Journal 2017; 15:5077–5228
    [Google Scholar]
  3. EFSA (European Food Safety Authority) and ECDC (European Centre for Disease Prevention and Control), 2018 The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2016. EFSA Journal 2018; 6:5182
    [Google Scholar]
  4. Franco A, Leekitcharoenphon P, Feltrin F, Alba P, Cordaro G et al. Emergence of a clonal lineage of multidrug-resistant ESBL-producing Salmonella Infantis transmitted from broilers and broiler meat to humans in Italy between 2011 and 2014. PLoS One 2015; 10:e0144802 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  5. Aviv G, Tsyba K, Steck N, Salmon-Divon M, Cornelius A et al. A unique megaplasmid contributes to stress tolerance and pathogenicity of an emergent Salmonella enterica serovar Infantis strain. Environ Microbiol 2014; 16:977–994 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  6. Hindermann D, Gopinath G, Chase H, Negrete F, Althaus D et al. Salmonella enterica serovar Infantis from food and human infections, Switzerland, 2010-2015: poultry-related multidrug resistant clones and an emerging ESBL-producing clonal lineage. Front Microbiol 2017; 8:1322 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  7. Tate H, Folster JP, Hsu C-H, Chen J, Hoffmann M et al. Comparative analysis of extended-spectrum-β-lactamase CTX-M-65-producing Salmonella enterica serovar Infantis isolates from humans, food animals, and retail chickens in the United States. Antimicrob Agents Chemother 2017; 61:e00488-17 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  8. Carfora V, Alba P, Leekitcharoenphon P, Ballarò D, Cordaro G et al. Colistin resistance mediated by mcr-1 in ESBL-producing, multidrug resistant Salmonella Infantis in broiler chicken industry, Italy (2016-2017). Front Microbiol 2018; 9:1880 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  9. MacLean RC, San Millan A. Microbial evolution: towards resolving the plasmid paradox. Curr Biol 2015; 25:R764–R767 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  10. Janowicz A, De Massis F, Ancora M, Cammà C, Patavino C et al. Core genome multilocus sequence typing and single nucleotide polymorphism analysis in the epidemiology of Brucella melitensis infections. J Clin Microbiol 2018; 56:pii: e00517-18 [CrossRef]
    [Google Scholar]
  11. Pearce ME, Alikhan N-F, Dallman TJ, Zhou Z, Grant K et al. Comparative analysis of core genome MLST and SNP typing within a European Salmonella serovar enteritidis outbreak. Int J Food Microbiol 2018; 274:1–11 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  12. Hendriksen RS, Pedersen SK, Leekitcharoenphon P, Malorny B, Borowiak M et al. Final report of engage ‐ establishing next generation sequencing ability for genomic analysis in Europe. EFS3 2018; 15: [CrossRef]
    [Google Scholar]
  13. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  14. Nurk S, Bankevich A, Antipov D, Gurevich AA, Korobeynikov A et al. Assembling single-cell genomes and mini-metagenomes from chimeric MDA products. J Comput Biol 2013; 20:714–737 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  15. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 2013; 29:1072–1075 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  16. Yoshida CE, Kruczkiewicz P, Laing CR, Lingohr EJ, Gannon VPJ et al. The Salmonella in silico typing resource (SISTR): an open Web-Accessible tool for rapidly typing and subtyping draft Salmonella genome assemblies. PLoS One 2016; 11:e0147101 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  17. Kaas RS, Leekitcharoenphon P, Aarestrup FM, Lund O. Solving the problem of comparing whole bacterial genomes across different sequencing platforms. PLoS One 2014; 9:e104984 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  18. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009; 25:1754–1760 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  19. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 2010; 26:841–842 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  20. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J et al. 1000 genome project data processing subgroup. The sequence Alignment/Map format and SAMtools. Bioinformatics 2009; 25:2078–2079
    [Google Scholar]
  21. Price MN, Dehal PS, Arkin AP. FastTree 2--approximately maximum-likelihood trees for large alignments. PLoS One 2010; 5:e9490 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  22. Letunic I, Bork P. Interactive tree of life (iTOL) V3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res 2016; 44:W242–W245 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  23. Revell LJ. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 2012; 3:217–223 [CrossRef]
    [Google Scholar]
  24. Alikhan N-F, Zhou Z, Sergeant MJ, Achtman M. A genomic overview of the population structure of Salmonella. PLoS Genet 2018; 14:e1007261 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  25. 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
    [Google Scholar]
  26. Zhang Z, Schwartz S, Wagner L, Miller W. A greedy algorithm for aligning DNA sequences. J Comput Biol 2000; 7:203–214 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  27. Carattoli A, Zankari E, García-Fernández A, Voldby Larsen M, Lund O et al. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother 2014; 58:3895–3903 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  28. Larsen MV, Cosentino S, Rasmussen S, Friis C, Hasman H et al. Multilocus sequence typing of total-genome-sequenced bacteria. J Clin Microbiol 2012; 50:1355–1361 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  29. Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S et al. Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother 2012; 67:2640–2644 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  30. Paulsen IT, Littlejohn TG, Rådström P, Sundström L, Sköld O et al. The 3' conserved segment of integrons contains a gene associated with multidrug resistance to antiseptics and disinfectants. Antimicrob Agents Chemother 1993; 37:761–768 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  31. Koutsoumanis K, Allende A, Alvarez‐Ordóñez A, Bolton D et al.EFSA Panel on Biological Hazards (EFSA BIOHAZ Panel) Salmonella control in poultry flocks and its public health impact. EFSA Journal 2019; 17:e05596
    [Google Scholar]
  32. Pate M, Mičunovič J, Golob M, Vestby LK, Ocepek M. Salmonella Infantis in broiler flocks in slovenia: the prevalence of multidrug resistant strains with high genetic homogeneity and low biofilm-forming Ability. Biomed Res Int 2019; 2019:4981463–13 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  33. Ammar AM, Abdeen EE, Abo-Shama UH, Fekry E, Kotb Elmahallawy E. Molecular characterization of virulence and antibiotic resistance genes among Salmonella serovars isolated from broilers in Egypt. Lett Appl Microbiol 2019; 68:188–195 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  34. Ranjbar R, Rahmati H, Shokoohizadeh L. Detection of common clones of Salmonella enterica serotype Infantis from human sources in Tehran hospitals. Gastroenterol Hepatol Bed Bench 2018; 11:54–59[PubMed][PubMed]
    [Google Scholar]
  35. Vinueza-Burgos C, Baquero M, Medina J, De Zutter L, Occurrence DZL. Occurrence, genotypes and antimicrobial susceptibility of Salmonella collected from the broiler production chain within an integrated poultry company. Int J Food Microbiol 2019; 299:1–7 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  36. Szmolka A, Szabó M, Kiss J, Pászti J, Adrián E et al. Molecular epidemiology of the endemic multiresistance plasmid pSI54/04 of Salmonella infantis in broiler and human population in Hungary. Food Microbiol 2018; 71:25–31 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  37. Kücken D, Feucht H, Kaulfers P. Association of qacE and qacEDelta1 with multiple resistance to antibiotics and antiseptics in clinical isolates of Gram-negative bacteria. FEMS Microbiol Lett 2000; 183:95–98 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  38. Guerra B, Soto S, Cal S, Mendoza MC. Antimicrobial resistance and spread of class 1 integrons among Salmonella serotypes. Antimicrob Agents Chemother 2000; 44:2166–2169 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  39. Borowiak M, Szabo I, Baumann B, Junker E, Hammerl JA et al. Vim-1-Producing Salmonella Infantis isolated from swine and minced pork meat in Germany. J Antimicrob Chemother 2017; 72:2131–2133 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  40. EMA (European Medicines Agency) 2018 Reflection paper on off-label use of antimicrobials in veterinary medicine in the European Union. https://www.ema.europa.eu/en/documents/scientific-guideline/reflection-paper-label-use-antimicrobials-veterinary-medicine-european-union-first-version_en.pdf
  41. Gymoese P, Kiil K, Torpdahl M, Østerlund MT, Sørensen G et al. WGS based study of the population structure of Salmonella enterica serovar Infantis. BMC Genomics 2019; 20:870 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  42. Yokoyama E, Murakami K, Shiwa Y, Ishige T, Ando N et al. Phylogenetic and population genetic analysis of Salmonella enterica subsp. enterica serovar Infantis strains isolated in Japan using whole genome sequence data. Infect Genet Evol 2014; 27:62–68 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  43. Goeders N, Van Melderen L. Toxin-Antitoxin systems as multilevel interaction systems. Toxins 2014; 6:304–324 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  44. Anonymous Salmonella in livestock production 2018 data – AphA 2019 – to be published on line OCT 2019; 2019
  45. Dierikx CM, van der Goot JA, Smith HE, Kant A, Mevius DJ. Presence of ESBL/AmpC-producing Escherichia coli in the broiler production pyramid: a descriptive study. PLoS One 2013; 8:e79005. [CrossRef][PubMed][PubMed]
    [Google Scholar]
  46. Aviv G, Rahav G, Gal-Mor O. Horizontal transfer of the Salmonella enterica serovar Infantis resistance and virulence plasmid pESI to the gut microbiota of Warm-Blooded hosts. mBio 2016; 7:e01395–16 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  47. Iranzo J, Puigbò P, Lobkovsky AE, Wolf YI, Koonin EV. Inevitability of genetic parasites. Genome Biol Evol 2016; 8:2856–2869 [CrossRef][PubMed][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000365
Loading
/content/journal/mgen/10.1099/mgen.0.000365
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

EXCEL

Most cited this month Most Cited RSS feed

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