1887

Abstract

Kentucky is commonly found in poultry and rarely associated with human disease. However, a multidrug-resistant (MDR) . Kentucky clone [sequence type (ST)198] has been increasingly reported globally in humans and animals. Our aim here was to assess if the recently reported increase of . Kentucky in poultry in Spain was associated with the ST198 clone and to characterize this MDR clone and its distribution in Spain. Sixty-six isolates retrieved from turkey, laying hen and broiler in 2011–2017 were subjected to whole-genome sequencing to assess their sequence type, genetic relatedness, and presence of antimicrobial resistance genes (ARGs), plasmid replicons and virulence factors. Thirteen strains were further analysed using long-read sequencing technologies to characterize the genetic background associated with ARGs. All isolates belonged to the ST198 clone and were grouped in three clades associated with the presence of a specific point mutation in the gene, their geographical origin and isolation year. All strains carried between one and 16 ARGs whose presence correlated with the resistance phenotype to between two and eight antimicrobials. The ARGs were located in the genomic island (SGI-1) and in some cases ( A1A1, and multiple aminoglycoside-resistance genes) in / plasmids, some of which were consistently detected in different years/farms in certain regions, suggesting they could persist over time. Our results indicate that the MDR . Kentucky ST198 is present in all investigated poultry hosts in Spain, and that certain strains also carry additional plasmid-mediated ARGs, thus increasing its potential public health significance.

Funding
This study was supported by the:
  • Horizon 2020 Framework Programme (Award 77830)
  • This is an open-access article distributed under the terms of the Creative Commons Attribution NonCommercial License.
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2022-03-08
2022-05-18
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References

  1. European Food Safety AuthorityEuropean Centre for Disease Prevention and Control The European Union Summary Report on Antimicrobial Resistance in zoonotic and indicator bacteria from humans, animals and food in 2017/2018. EFSA J 2020; 18:e06007 [View Article]
    [Google Scholar]
  2. Kirk MD, Pires SM, Black RE, Caipo M, Crump JA et al. World Health Organization Estimates of the Global and Regional Disease Burden of 22 Foodborne Bacterial, Protozoal, and Viral Diseases, 2010: A Data Synthesis. PLoS Med 2015; 12:e1001921 [View Article]
    [Google Scholar]
  3. Cassini A, Högberg LD, Plachouras D, Quattrocchi A, Hoxha A et al. Attributable deaths and disability-adjusted life-years caused by infections with antibiotic-resistant bacteria in the EU and the European Economic Area in 2015: a population-level modelling analysis. The Lancet Infectious Diseases 2019; 19:56–66 [View Article] [PubMed]
    [Google Scholar]
  4. Messens W, Vivas-Alegre L, Bashir S, Amore G, Romero-Barrios P et al. Estimating the public health impact of setting targets at the European level for the reduction of zoonotic Salmonella in certain poultry populations. Int J Environ Res Public Health 2013; 10:4836–4850 [View Article]
    [Google Scholar]
  5. Barrow PA, Methner U. Vaccination against Salmonella infections in food animals: rationale, theoretical basis and practical application. In Salmonella in Domestic Animals CABI; 2013 pp 455–475
    [Google Scholar]
  6. Koutsoumanis K, Allende A, Alvarez-Ordóñez A, Bolton D, Bover-Cid S et al. Salmonella control in poultry flocks and its public health impact. EFSA J 2019; 17:e05596 [View Article] [PubMed]
    [Google Scholar]
  7. Ferrari RG, Rosario DKA, Cunha-Neto A, Mano SB, Figueiredo EES et al. Worldwide Epidemiology of Salmonella Serovars in Animal-Based Foods: a Meta-analysis. Appl Environ Microbiol 2019; 85:e00591-19 [View Article] [PubMed]
    [Google Scholar]
  8. Threlfall EJ. Epidemic Salmonella typhimurium DT 104--a truly international multiresistant clone. J Antimicrob Chemother 2000; 46:7–10 [View Article] [PubMed]
    [Google Scholar]
  9. European Food Safety AuthorityEuropean Centre for Disease Prevention and Control The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2016. EFSA J 2018; 16:e05182 [View Article] [PubMed]
    [Google Scholar]
  10. WHO Critically important antimicrobials for human medicine, 6th revision; 2019 https://www.who.int/publications/i/item/9789241515528
  11. Hawkey J, Le Hello S, Doublet B, Granier SA, Hendriksen RS et al. Global phylogenomics of multidrug-resistant Salmonella enterica serotype Kentucky ST198. Microb Genom 2019; 5: [View Article] [PubMed]
    [Google Scholar]
  12. Le Hello S, Hendriksen RS, Doublet B, Fisher I, Nielsen EM et al. International spread of an epidemic population of Salmonella enterica serotype Kentucky ST198 resistant to ciprofloxacin. J Infect Dis 2011; 204:675–684 [View Article] [PubMed]
    [Google Scholar]
  13. Le Hello S, Weill F-X, Guibert V, Praud K, Cloeckaert A et al. Early strains of multidrug-resistant Salmonella enterica serovar Kentucky sequence type 198 from Southeast Asia harbor Salmonella genomic island 1-J variants with a novel insertion sequence. Antimicrob Agents Chemother 2012; 56:5096–5102 [View Article] [PubMed]
    [Google Scholar]
  14. Joerger RD, Sartori CA, Kniel KE. Comparison of genetic and physiological properties of Salmonella enterica isolates from chickens reveals one major difference between serovar Kentucky and other serovars: response to acid. Foodborne Pathog Dis 2009; 6:503–512 [View Article] [PubMed]
    [Google Scholar]
  15. Johnson TJ, Thorsness JL, Anderson CP, Lynne AM, Foley SL et al. Horizontal gene transfer of a ColV plasmid has resulted in a dominant avian clonal type of Salmonella enterica serovar Kentucky. PLoS One 2010; 5:e15524 [View Article] [PubMed]
    [Google Scholar]
  16. Foley SL, Johnson TJ, Ricke SC, Nayak R, Danzeisen J. Salmonella pathogenicity and host adaptation in chicken-associated serovars. Microbiol Mol Biol Rev 2013; 77:582–607 [View Article] [PubMed]
    [Google Scholar]
  17. Cheng Y, Pedroso AA, Porwollik S, McClelland M, Lee MD et al. rpoS-Regulated core genes involved in the competitive fitness of Salmonella enterica Serovar Kentucky in the intestines of chickens. Appl Environ Microbiol 2015; 81:502–514 [View Article] [PubMed]
    [Google Scholar]
  18. Dhanani AS, Block G, Dewar K, Forgetta V, Topp E et al. Genomic Comparison of Non-Typhoidal Salmonella enterica Serovars Typhimurium, Enteritidis, Heidelberg, Hadar and Kentucky Isolates from Broiler Chickens. PLoS One 2015; 10:e0128773 [View Article] [PubMed]
    [Google Scholar]
  19. Westrell T, Monnet DL, Gossner C, Heuer O, Takkinen J. Drug-resistant Salmonella enterica serotype Kentucky in Europe. Lancet Infect Dis 2014; 14:270–271 [View Article] [PubMed]
    [Google Scholar]
  20. Le Hello S, Bekhit A, Granier SA, Barua H, Beutlich J et al. The global establishment of a highly-fluoroquinolone resistant Salmonella enterica serotype Kentucky ST198 strain. Front Microbiol 2013; 4:395 [View Article] [PubMed]
    [Google Scholar]
  21. Wasyl D, Kern-Zdanowicz I, Domańska-Blicharz K, Zając M, Hoszowski A. High-level fluoroquinolone resistant Salmonella enterica serovar Kentucky ST198 epidemic clone with IncA/C conjugative plasmid carrying bla(CTX-M-25) gene. Vet Microbiol 2015; 175:85–91 [View Article] [PubMed]
    [Google Scholar]
  22. Wasyl D, Hoszowski A. First isolation of ESBL-producing Salmonella and emergence of multiresistant Salmonella Kentucky in turkey in Poland. Food Research International 2012; 45:958–961 [View Article]
    [Google Scholar]
  23. Légifrance Arrêté du 1er août 2018 relatif à la surveillance et à la lutte contre les infections à Salmonella dans les troupeaux de l’espèce Gallus gallus en filière ponte d’œufs de consommation - Légifrance; 2021 https://www.legifrance.gouv.fr/jorf/id/JORFTEXT000037330841?r=xG21WLRFAo
  24. Alvarez J, Lopez G, Muellner P, de Frutos C, Ahlstrom C et al. Identifying emerging trends in antimicrobial resistance using Salmonella surveillance data in poultry in Spain. Transbound Emerg Dis 2020; 67:250–262 [View Article] [PubMed]
    [Google Scholar]
  25. Antilles N, García-Bocanegra I, Alba-Casals A, López-Soria S, Pérez-Méndez N et al. Occurrence and antimicrobial resistance of zoonotic enteropathogens in gulls from southern Europe. Sci Total Environ 2021; 763:143018 [View Article] [PubMed]
    [Google Scholar]
  26. Anon Comission Regulation 517/2011 implementing Regulation 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 Regula. Official Journal of the European Union, L138, 7; 2021 https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX%3A32011R0517
  27. Anon Commission regulation 200/2012 concerning a Union target for the reduction of Salmonella enteritidis and Salmonella typhimurium in flocks of broilers, as provided for in Regulation 2160/2003 of the European Paliament and of the Council. Official Journal of the European Union, L71, 6; 2012 https://eur-lex.europa.eu/legal-content/EN/ALL/?uri=CELEX%3A32012R0200
  28. Anon Comission Regulation 517/2011 implementing Regulation 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 Regula. Official Journal of the European Union, L349, 6; 2021 https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX%3A32012R1190
  29. Douard G, Praud K, Cloeckaert A, Doublet B. The Salmonella genomic island 1 is specifically mobilized in trans by the IncA/C multidrug resistance plasmid family. PLoS One 2010; 5:e15302 [View Article] [PubMed]
    [Google Scholar]
  30. Doublet B, Praud K, Bertrand S, Collard J-M, Weill F-X et al. Novel insertion sequence- and transposon-mediated genetic rearrangements in genomic island SGI1 of Salmonella enterica serovar Kentucky. Antimicrob Agents Chemother 2008; 52:3745–3754 [View Article] [PubMed]
    [Google Scholar]
  31. Mulvey MR, Boyd DA, Olson AB, Doublet B, Cloeckaert A. The genetics of Salmonella genomic island 1. Microbes Infect 2006; 8:1915–1922 [View Article] [PubMed]
    [Google Scholar]
  32. Hernández M, Iglesias MR, Rodríguez-Lázaro D, Gallardo A, Quijada N et al. Co-occurrence of colistin-resistance genes mcr-1 and mcr-3 among multidrug-resistant Escherichia coli isolated from cattle, Spain, September 2015. Euro Surveill 2017; 22:30586 [View Article] [PubMed]
    [Google Scholar]
  33. Illumina Nextera XT DNA Library Prep Kit Reference Guide For Research Use Only. Not for use in diagnostic procedures; 2018 www.illumina.com/company/legal.html
  34. Quijada NM, Rodríguez-Lázaro D, Eiros JM, Hernández M. TORMES: an automated pipeline for whole bacterial genome analysis. Bioinformatics 2019; 35:4207–4212 [View Article] [PubMed]
    [Google Scholar]
  35. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article] [PubMed]
    [Google Scholar]
  36. Wood DE, Salzberg SL. Kraken: ultrafast metagenomic sequence classification using exact alignments. Genome Biol 2014; 15:R46 [View Article] [PubMed]
    [Google Scholar]
  37. 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]
    [Google Scholar]
  38. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 2013; 29:1072–1075 [View Article]
    [Google Scholar]
  39. 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 [View Article]
    [Google Scholar]
  40. Bortolaia V, Kaas RS, Ruppe E, Roberts MC, Schwarz S et al. ResFinder 4.0 for predictions of phenotypes from genotypes. J Antimicrob Chemother 2020; 75:3491–3500 [View Article]
    [Google Scholar]
  41. Chen L, Yang J, Yu J, Yao Z, Sun L et al. VFDB: a reference database for bacterial virulence factors. Nucleic Acids Res 2005; 33:D325–8 [View Article] [PubMed]
    [Google Scholar]
  42. 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 [View Article] [PubMed]
    [Google Scholar]
  43. Zankari E, Allesøe R, Joensen KG, Cavaco LM, Lund O et al. PointFinder: a novel web tool for WGS-based detection of antimicrobial resistance associated with chromosomal point mutations in bacterial pathogens. J Antimicrob Chemother 2017; 72:2764–2768 [View Article] [PubMed]
    [Google Scholar]
  44. 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 [View Article] [PubMed]
    [Google Scholar]
  45. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009; 25:1754–1760 [View Article] [PubMed]
    [Google Scholar]
  46. 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]
  47. Zhou Y, Liang Y, Lynch KH, Dennis JJ, Wishart DS. PHAST: a fast phage search tool. Nucleic Acids Res 2011; 39:W347–52 [View Article] [PubMed]
    [Google Scholar]
  48. Katoh K, Rozewicki J, Yamada KD. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 2019; 20:1160–1166 [View Article] [PubMed]
    [Google Scholar]
  49. Croucher NJ, Page AJ, Connor TR, Delaney AJ, Keane JA et al. Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res 2015; 43:e15 [View Article] [PubMed]
    [Google Scholar]
  50. 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]
  51. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res 2019; 47:W256–W259 [View Article] [PubMed]
    [Google Scholar]
  52. Tonkin-Hill G, Lees JA, Bentley SD, Frost SDW, Corander J. RhierBAPS: An R implementation of the population clustering algorithm hierBAPS. Version 1. Wellcome Open Res 2018; 3:93 [View Article] [PubMed]
    [Google Scholar]
  53. Assefa S, Keane TM, Otto TD, Newbold C, Berriman M. ABACAS: algorithm-based automatic contiguation of assembled sequences. Bioinformatics 2009; 25:1968–1969 [View Article] [PubMed]
    [Google Scholar]
  54. Carver TJ, Rutherford KM, Berriman M, Rajandream M-A, Barrell BG et al. ACT: the Artemis Comparison Tool. Bioinformatics 2005; 21:3422–3423 [View Article] [PubMed]
    [Google Scholar]
  55. R Core Team R: a language and environment for statistical computing; 2021
  56. De Coster W, D’Hert S, Schultz DT, Cruts M, Van Broeckhoven C. NanoPack: visualizing and processing long-read sequencing data. Bioinformatics 2018; 34:2666–2669 [View Article] [PubMed]
    [Google Scholar]
  57. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: Resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 2017; 13:1–22 [View Article] [PubMed]
    [Google Scholar]
  58. Robertson J, Nash JHE. MOB-suite: software tools for clustering, reconstruction and typing of plasmids from draft assemblies. Microb Genom 2018; 4: [View Article] [PubMed]
    [Google Scholar]
  59. Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 2015; 31:3691–3693 [View Article] [PubMed]
    [Google Scholar]
  60. Alikhan NF, Petty NK, Ben Zakour NL, Beatson SA. BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genomics 2011; 12:1–10 [View Article] [PubMed]
    [Google Scholar]
  61. Shah DH, Paul NC, Guard J. Complete Genome Sequence of a Ciprofloxacin-Resistant Salmonella enterica subsp. enterica Serovar Kentucky Sequence Type 198 Strain, PU131, Isolated from a Human Patient in Washington State. Genome Announc 2018; 6:e00125-18 [View Article] [PubMed]
    [Google Scholar]
  62. Elnekave E, Hong SL, Lim S, Johnson TJ, Perez A et al. Comparing serotyping with whole-genome sequencing for subtyping of non-typhoidal Salmonella enterica: a large-scale analysis of 37 serotypes with a public health impact in the USA. Microb Genom 2020; 6:1–13 [View Article] [PubMed]
    [Google Scholar]
  63. Chen H, Song J, Zeng X, Chen D, Chen R et al. National prevalence of Salmonella enterica serotype Kentucky ST198 with high-level resistance to ciprofloxacin and extended-spectrum cephalosporins in China, 2013 to 2017. mSystems 2021; 6:e00935-20 [View Article] [PubMed]
    [Google Scholar]
  64. Coipan CE, Westrell T, Hoek A, Alm E, Kotila S et al. Genomic epidemiology of emerging ESBL-producing Salmonella Kentucky bla CTX-M-14b in Europe. Emerg Microbes Infect 2020; 9:2124–2135
    [Google Scholar]
  65. Partridge SR, Tsafnat G, Coiera E, Iredell JR. Gene cassettes and cassette arrays in mobile resistance integrons. FEMS Microbiol Rev 2009; 33:757–784 [View Article] [PubMed]
    [Google Scholar]
  66. Escudero JA, Loot C, Nivina A, Mazel D. The Integron: Adaptation On Demand. In Mobile DNA III American Society for Microbiology; 2014 pp 139–161
    [Google Scholar]
  67. Souque C, Escudero JA, MacLean RC. Integron activity accelerates the evolution of antibiotic resistance. Elife 2021; 10:1–47 [View Article] [PubMed]
    [Google Scholar]
  68. Naas T, Aubert D, Lambert T, Nordmann P. Complex genetic structures with repeated elements, a sul-type class 1 integron, and the blaVEB extended-spectrum beta-lactamase gene. Antimicrob Agents Chemother 2006; 50:1745–1752 [View Article] [PubMed]
    [Google Scholar]
  69. Cowley LA, Dallman TJ, Fitzgerald S, Irvine N, Rooney PJ et al. Short-term evolution of Shiga toxin-producing Escherichia coli O157:H7 between two food-borne outbreaks. Microb Genom 2016; 2:e000084 [View Article] [PubMed]
    [Google Scholar]
  70. Zurfluh K, Klumpp J, Nüesch-Inderbinen M, Stephan R. Full-length nucleotide sequences of mcr-1-harboring plasmids isolated from extended-spectrum-β-lactamase-producing Escherichia coli isolates of different origins. Antimicrob Agents Chemother 2016; 60:5589–5591 [View Article] [PubMed]
    [Google Scholar]
  71. García Fernández A, Cloeckaert A, Bertini A, Praud K, Doublet B et al. Comparative analysis of IncHI2 plasmids carrying blaCTX-M-2 or blaCTX-M-9 from Escherichia coli and Salmonella enterica strains isolated from poultry and humans. Antimicrob Agents Chemother 2007; 51:4177–4180 [View Article] [PubMed]
    [Google Scholar]
  72. Ktari S, Le Hello S, Ksibi B, Courdavault L, Mnif B et al. Carbapenemase-producing Salmonella enterica serotype Kentucky ST198, North Africa. J Antimicrob Chemother 2015; 70:3405–3407 [View Article] [PubMed]
    [Google Scholar]
  73. Le Hello S, Harrois D, Bouchrif B, Sontag L, Elhani D et al. Highly drug-resistant Salmonella enterica serotype Kentucky ST198-X1: a microbiological study. Lancet Infect Dis 2013; 13:672–679 [View Article] [PubMed]
    [Google Scholar]
  74. Lei C-W, Zhang Y, Wang X-C, Gao Y-F, Wang H-N. Draft genome sequence of a multidrug-resistant Salmonella enterica serotype Kentucky ST198 with chromosomal integration of blaCTX-M-14b isolated from a poultry slaughterhouse in China. J Glob Antimicrob Resist 2020; 20:145–146 [View Article] [PubMed]
    [Google Scholar]
  75. European Food Safety AuthorityEuropean Centre for Disease Prevention and Control The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2017. EFSA J 2019; 17:e05598 [View Article] [PubMed]
    [Google Scholar]
  76. Alonso CA, Michael GB, Li J, Somalo S, Simón C et al. Analysis of blaSHV-12-carrying Escherichia coli clones and plasmids from human, animal and food sources. J Antimicrob Chemother 2017; 72:1589–1596 [View Article] [PubMed]
    [Google Scholar]
  77. Lambrecht E, Van Meervenne E, Boon N, Van de Wiele T, Wattiau P et al. Characterization of cefotaxime- and ciprofloxacin-resistant commensal Escherichia coli originating from Belgian farm animals indicates high antibiotic resistance transfer rates. Microb Drug Resist 2018; 24:707–717 [View Article] [PubMed]
    [Google Scholar]
  78. Lambrecht E, Coillie EV, Boon N, Heyndrickx M, Wiele TV de. Transfer of antibiotic resistance plasmid from commensal E. coli towards human intestinal microbiota in the M-SHIME: effect of E. coli dosis, human individual and antibiotic use. Life (Basel) 2021; 11:192 [View Article] [PubMed]
    [Google Scholar]
  79. Carroll LM, Gaballa A, Guldimann C, Sullivan G, Henderson LO et al. Identification of novel mobilized colistin resistance gene mcr-9 in a multidrug-resistant, colistin-susceptible Salmonella enterica serotype typhimurium isolate. mBio 2019; 10:e00853-19 [View Article]
    [Google Scholar]
  80. Osei Sekyere J, Maningi NE, Modipane L, Mbelle NM. Emergence of mcr-9.1 in extended-spectrum-β-lactamase-producing clinical Enterobacteriaceae in Pretoria, South Africa: global evolutionary phylogenomics, resistome, and mobilome. mSystems 2020; 5:e00148-20 [View Article] [PubMed]
    [Google Scholar]
  81. Hayer SS, Lim S, Hong S, Elnekave E, Johnson T et al. Genetic determinants of resistance to extended-spectrum cephalosporin and fluoroquinolone in Escherichia coli isolated from diseased pigs in the United States. mSphere 2020; 5:e00990-20 [View Article] [PubMed]
    [Google Scholar]
  82. de Curraize C, Siebor E, Varin V, Neuwirth C, Hall RM. Two New SGI1-LK Variants Found in Proteus mirabilis and Evolution of the SGI1-HKL Group of Salmonella Genomic Islands. mSphere 2020; 5:e00875-19 [View Article] [PubMed]
    [Google Scholar]
  83. Cohen E, Davidovich M, Rokney A, Valinsky L, Rahav G et al. Emergence of new variants of antibiotic resistance genomic islands among multidrug-resistant Salmonella enterica in poultry. Environ Microbiol 2020; 22:413–432 [View Article] [PubMed]
    [Google Scholar]
  84. Deng W, Marshall NC, Rowland JL, McCoy JM, Worrall LJ et al. Assembly, structure, function and regulation of type III secretion systems. Nat Rev Microbiol 2017; 15:323–337 [View Article] [PubMed]
    [Google Scholar]
  85. El Hage R, Losasso C, Longo A, Petrin S, Ricci A et al. Whole-genome characterisation of TEM-1 and CMY-2 β-lactamase-producing Salmonella Kentucky ST198 in Lebanese broiler chain. J Glob Antimicrob Resist 2020; 23:408–416 [View Article] [PubMed]
    [Google Scholar]
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