1887

Abstract

Non-typhoidal (NTS) is the second most common cause of foodborne bacterial gastroenteritis in Australia with antimicrobial resistance (AMR) increasing in recent years. Whole-genome sequencing (WGS) provides opportunities for detection of AMR determinants. The objectives of this study were two-fold: (1) establish the utility of WGS analyses for inferring phenotypic resistance in NTS, and (2) explore clinically relevant genotypic AMR profiles to third generation cephalosporins (3GC) in NTS lineages. The concordance of 2490 NTS isolates with matched WGS and phenotypic susceptibility data against 13 clinically relevant antimicrobials was explored. serovar prediction and typing was performed on assembled reads and interrogated for known AMR determinants. The surrounding genomic context, plasmid determinants and co-occurring AMR patterns were further investigated for multidrug resistant serovars harbouring , or . Our data demonstrated a high correlation between WGS and phenotypic susceptibility testing. Phenotypic-genotypic concordance was observed between 2440/2490 (98.0 %) isolates, with overall sensitivity and specificity rates >98 % and positive and negative predictive values >97 %. The most common AMR determinants were , , (A), and . Phenotypic resistance to cefotaxime and azithromycin was low and observed in 6.2 % (151/2486) and 0.9 % (16/1834) of the isolates, respectively. Several multi-drug resistant NTS lineages were resistant to 3GC due to different genetic mechanisms including , or . This study shows WGS can enhance existing AMR surveillance in NTS datasets routinely produced in public health laboratories to identify emerging AMR in NTS. These approaches will be critical for developing capacity to detect emerging public health threats such as resistance to 3GC.

Funding
This study was supported by the:
  • National Health and Medical Research Council (Award GNT1196103)
    • Principle Award Recipient: BenjaminP Howden
  • National Health and Medical Research Council (Award GNT1195210)
    • Principle Award Recipient: DanielleJ Ingle
  • National Health and Medical Research Council (Award GNT1174555)
    • Principle Award Recipient: DeborahA Williamson
  • National Health and Medical Research Council (Award APP1149991)
    • Principle Award Recipient: BenjaminP Howden
  • National Health and Medical Research Council (Award APP1129770)
    • Principle Award Recipient: BenjaminP Howden
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2021-12-15
2022-01-27
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References

  1. Sia C, Baines S, Valcanis M, Lee DYJ, Goncalves De Silva A et al. Figshare 2021 https://doi.org/10.6084/m9.figshare.16556748.v1
    [Google Scholar]
  2. 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]
  3. National Notifiable Diseases Surveillance System Department of Health Canberra Notification for all diseases by State and Territory and Year; 2019 http://www9.health.gov.au/cda/source/rpt_2_sel.cfm
  4. Chen MH, Wang SW, Hwang WZ, Tsai SJ, Hsih YC et al. Contamination of Salmonella Schwarzengrund cells in chicken meat from traditional marketplaces in Taiwan and comparison of their antibiograms with those of the human isolates. Poult Sci 2010; 89:359–365 [View Article] [PubMed]
    [Google Scholar]
  5. Thomas M, Fenske GJ, Antony L, Ghimire S, Welsh R et al. Whole genome sequencing-based detection of antimicrobial resistance and virulence in non-typhoidal Salmonella enterica isolated from wildlife. Gut Pathog 2017; 9:66. [View Article] [PubMed]
    [Google Scholar]
  6. Williamson DA, Lane CR, Easton M, Valcanis M, Strachan J et al. Increasing antimicrobial resistance in nontyphoidal Salmonella isolates in Australia from 1979 to 2015. Antimicrob Agents Chemother 2018; 62:e02012-17. [View Article] [PubMed]
    [Google Scholar]
  7. Andino A, Hanning I. . Salmonella enterica: survival, colonization, and virulence differences among serovars. Scientific World Journal 2015; 2015:520179–16 [View Article] [PubMed]
    [Google Scholar]
  8. Magiorakos A-P, Srinivasan A, Carey RB, Carmeli Y, Falagas ME et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 2012; 18:268–281 [View Article] [PubMed]
    [Google Scholar]
  9. Silva C, Calva E, Maloy S, Atlas RM, Maloy S. One Health and Food-Borne Disease: Salmonella Transmission between Humans, Animals, and Plants. Microbiol Spectr 2014; 2:O–2013 [View Article]
    [Google Scholar]
  10. Threlfall EJ, Frost JA, Ward LR, Rowe B. Increasing spectrum of resistance in multiresistant Salmonella Typhimurium. The Lancet 1996; 347:1053–1054 [View Article]
    [Google Scholar]
  11. Ellington MJ, Ekelund O, Aarestrup FM, Canton R, Doumith M et al. The role of whole genome sequencing in antimicrobial susceptibility testing of bacteria: report from the EUCAST Subcommittee. Clin Microbiol Infect 2017; 23:2–22 [View Article] [PubMed]
    [Google Scholar]
  12. Mensah N, Tang Y, Cawthraw S, AbuOun M, Fenner J et al. Determining antimicrobial susceptibility in Salmonella enterica serovar Typhimurium through whole genome sequencing: a comparison against multiple phenotypic susceptibility testing methods. BMC Microbiol 2019; 19:148 [View Article] [PubMed]
    [Google Scholar]
  13. Neuert S, Nair S, Day MR, Doumith M, Ashton PM et al. Prediction of phenotypic antimicrobial resistance profiles from whole genome sequences of non-typhoidal Salmonella enterica. Front Microbiol 2018; 9:592. [View Article] [PubMed]
    [Google Scholar]
  14. McDermott PF, Tyson GH, Kabera C, Chen Y, Li C et al. Whole-genome sequencing for detecting antimicrobial resistance in nontyphoidal Salmonella. Antimicrob Agents Chemother 2016; 60:5515–5520 [View Article] [PubMed]
    [Google Scholar]
  15. Hendriksen RS, Bortolaia V, Tate H, Tyson GH, Aarestrup FM et al. Using genomics to track global antimicrobial resistance. Front Public Health 2019; 7:242 [View Article] [PubMed]
    [Google Scholar]
  16. Zankari E, Hasman H, Kaas RS, Seyfarth AM, Agersø Y et al. Genotyping using whole-genome sequencing is a realistic alternative to surveillance based on phenotypic antimicrobial susceptibility testing. J Antimicrob Chemother 2013; 68:771–777 [View Article] [PubMed]
    [Google Scholar]
  17. Centers for Disease Control and Prevention Antibiotic resistance threats in the United States; 2019 https://www.cdc.gov/drugresistance/pdf/threats-report/2019-ar-threats-report-508.pdf
  18. Antunes P, Coque TM, Peixe L. Emergence of an IncIγ plasmid encoding CMY-2 ß-lactamase associated with the international ST19 OXA-30-producing ß-lactamase Salmonella Typhimurium multidrug-resistant clone. J Antimicrob Chemother 2010; 65:2097–2100 [View Article] [PubMed]
    [Google Scholar]
  19. Tacconelli E, Carrara E, Savoldi A, Harbarth S, Mendelson M et al. Discovery, research, and development of new antibiotics: the WHO priority list of antibiotic-resistant bacteria and tuberculosis. Lancet Infect Dis 2018; 18:318–327 [View Article] [PubMed]
    [Google Scholar]
  20. Clinical Laboratory Standards Institute M100 Performance Standards for Antimicrobial Susceptibility Testing, 28th ed. Wayne, PA: CLSI; 2018
    [Google Scholar]
  21. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article] [PubMed]
    [Google Scholar]
  22. 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]
  23. Hunt M, Mather AE, Sánchez-Busó L, Page AJ, Parkhill J et al. ARIBA: rapid antimicrobial resistance genotyping directly from sequencing reads. Microb Genom 2017; 3:10 [View Article]
    [Google Scholar]
  24. Jia B, Raphenya AR, Alcock B, Waglechner N, Guo P et al. CARD 2017: expansion and model-centric curation of the comprehensive antibiotic resistance database. Nucleic Acids Res 2017; 45:D566–D573 [View Article] [PubMed]
    [Google Scholar]
  25. Heil EL, Johnson JK. Impact of CLSI breakpoint changes on microbiology laboratories and antimicrobial stewardship programs. J Clin Microbiol 2016; 54:840–844 [View Article] [PubMed]
    [Google Scholar]
  26. Achtman M, Wain J, Weill F-X, Nair S, Zhou Z et al. Multilocus sequence typing as a replacement for serotyping in Salmonella enterica. PLoS Pathog 2012; 8:e1002776 [View Article]
    [Google Scholar]
  27. 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]
  28. Gordon NC, Price JR, Cole K, Everitt R, Morgan M et al. Prediction of Staphylococcus aureus antimicrobial resistance by whole-genome sequencing. J Clin Microbiol 2014; 52:1182–1191 [View Article] [PubMed]
    [Google Scholar]
  29. Wickham H. ggplot2: Elegant Graphics for Data Analysis Springer; 2016
    [Google Scholar]
  30. Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: AFast and effective stochastic algorithm for estimating maximumlikelihood phylogenies. Mol Biol Evol 2015; 32:268–274 [View Article] [PubMed]
    [Google Scholar]
  31. Minh BQ, Nguyen MAT, von Haeseler A. Ultrafast approximation for phylogenetic bootstrap. Mol Biol Evol 2013; 30:1188–1195 [View Article] [PubMed]
    [Google Scholar]
  32. Yu G, Smith DK, Zhu H, Guan Y, Lam TT et al. ggtree : an r package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol Evol 2016; 8:28–36 [View Article]
    [Google Scholar]
  33. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
    [Google Scholar]
  34. Carver T, Harris SR, Berriman M, Parkhill J, McQuillan JA. Artemis: an integrated platform for visualization and analysis of high-throughput sequence-based experimental data. Bioinformatics 2012; 28:464–469 [View Article] [PubMed]
    [Google Scholar]
  35. Siguier P, Perochon J, Lestrade L, Mahillon J, Chandler M. ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Research 2006; 34:D32–D36 [View Article]
    [Google Scholar]
  36. 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]
  37. Antipov D, Hartwick N, Shen M, Raiko M, Lapidus A et al. plasmidspades: assembling plasmids from whole genome sequencing data. Bioinformatics 2016btw493 [View Article]
    [Google Scholar]
  38. Wick RR, Schultz MB, Zobel J, Holt KE. Bandage: interactive visualization of de novo genome assemblies. Bioinformatics 2015; 31:3350–3352 [View Article] [PubMed]
    [Google Scholar]
  39. Darling ACE, Mau B, Blattner FR, Perna NT. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 2004; 14:1394–1403 [View Article] [PubMed]
    [Google Scholar]
  40. Alikhan N-F, Petty NK, Ben Zakour NL, Beatson SA. BLAST ring image generator (BRIG): simple prokaryote genome comparisons. BMC genomics 2011; 12:402 [View Article]
    [Google Scholar]
  41. Csardi G, Nepusz T. The igraph software package for complex network research. InterJournal, Complex Systems; 2006 http://static1.squarespace.com/static/5b68a4e4a2772c2a206180a1/t/5cd1e3cbb208fc26c99de080/1557259212150/c1602a3c126ba822d0bc4293371c.pdf
  42. Ingle DJ, Levine MM, Kotloff KL, Holt KE, Robins-Browne RM. Dynamics of antimicrobial resistance in intestinal Escherichia coli from children in community settings in South Asia and sub-Saharan Africa. Nat Microbiol 2018; 3:1063–1073 [View Article] [PubMed]
    [Google Scholar]
  43. Schultz E, Barraud O, Madec J-Y, Haenni M, Cloeckaert A et al. Multidrug resistance Salmonella genomic Island 1 in a Morganella morganii subsp. morganii human clinical isolate from France. mSphere 2017; 2:1–5 [View Article]
    [Google Scholar]
  44. Monte DFM, Sellera FP, Lopes R, Keelara S, Landgraf M et al. Class 1 integron-borne cassettes harboring blaCARB-2 gene in multidrug-resistant and virulent Salmonella Typhimurium ST19 strains recovered from clinical human stool samples, United States. PLoS One 2020; 15:e0240978 [View Article]
    [Google Scholar]
  45. Zhao S, Li C, Hsu C-H, Tyson GH, Strain E et al. Comparative genomic analysis of 450 strains of Salmonella enterica Isolated from diseased animals. Genes 2020; 11:1025 [View Article]
    [Google Scholar]
  46. 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: [View Article]
    [Google Scholar]
  47. Day MR, Doumith M, Do Nascimento V, Nair S, Ashton PM et al. Comparison of phenotypic and WGS-derived antimicrobial resistance profiles of Salmonella enterica serovars Typhi and Paratyphi. J Antimicrob Chemother 2018; 73:365–372 [View Article] [PubMed]
    [Google Scholar]
  48. Sadouki Z, Day MR, Doumith M, Chattaway MA, Dallman TJ et al. Comparison of phenotypic and WGS-derived antimicrobial resistance profiles of Shigella sonnei isolated from cases of diarrhoeal disease in England and Wales, 2015. J Antimicrob Chemother 2017; 72:2496–2502 [View Article] [PubMed]
    [Google Scholar]
  49. Stoesser N, Batty EM, Eyre DW, Morgan M, Wyllie DH et al. Predicting antimicrobial susceptibilities for Escherichia coli and Klebsiella pneumoniae isolates using whole genomic sequence data. J Antimicrob Chemother 2013; 68:2234–2244 [View Article] [PubMed]
    [Google Scholar]
  50. Tyson GH, McDermott PF, Li C, Chen Y, Tadesse DA et al. WGS accurately predicts antimicrobial resistance in Escherichia coli. J Antimicrob Chemother 2015; 70:2763–2769 [View Article]
    [Google Scholar]
  51. van Vliet AHM, Kusters JG. Use of alignment-free phylogenetics for rapid genome sequence-based typing of Helicobacter pylori virulence markers and antibiotic susceptibility. J Clin Microbiol 2015; 53:2877–2888 [View Article] [PubMed]
    [Google Scholar]
  52. Zhao S, Tyson GH, Chen Y, Li C, Mukherjee S et al. Whole-genome sequencing analysis accurately predicts antimicrobial resistance phenotypes in Campylobacter spp. Appl Environ Microbiol 2016; 82:459–466 [View Article] [PubMed]
    [Google Scholar]
  53. Goldblatt J, Ward A, Yusuf M, Day M, Godbole G et al. Azithromycin susceptibility testing for Salmonella enterica isolates: discordances in results using MIC gradient strips. J Antimicrob Chemother 2020; 75:1820–1823 [View Article] [PubMed]
    [Google Scholar]
  54. Khan S, Kurup P, Vinod V, Biswas R, Pillai GK et al. Reconsidering azithromycin disc diffusion interpretive criteria for Salmonellae in view of azithromycin MIC creep among typhoidal and nontyphoidal Salmonella. J Lab Physicians 2019; 11:39–44 [View Article] [PubMed]
    [Google Scholar]
  55. Katiyar A, Sharma P, Dahiya S, Singh H, Kapil A et al. Genomic profiling of antimicrobial resistance genes in clinical isolates of Salmonella Typhi from patients infected with Typhoid fever in India. Sci Rep 2020; 10:8299. [View Article] [PubMed]
    [Google Scholar]
  56. Doyle RM, O’Sullivan DM, Aller SD, Bruchmann S, Clark T et al. Discordant bioinformatic predictions of antimicrobial resistance from whole-genome sequencing data of bacterial isolates: an inter-laboratory study. Microb Genom 2020; 6: [View Article] [PubMed]
    [Google Scholar]
  57. Frye JG, Jackson CR. Genetic mechanisms of antimicrobial resistance identified in Salmonella enterica, Escherichia coli, and Enteroccocus spp. isolated from U.S. food animals. Front Microbiol 2013; 4:135. [View Article] [PubMed]
    [Google Scholar]
  58. Sunde M, Norström M. The genetic background for streptomycin resistance in Escherichia coli influences the distribution of MICs. J Antimicrob Chemother 2005; 56:87–90 [View Article] [PubMed]
    [Google Scholar]
  59. Doumith M, Ellington MJ, Livermore DM, Woodford N. Molecular mechanisms disrupting porin expression in ertapenem-resistant Klebsiella and Enterobacter spp. clinical isolates from the UK. J Antimicrob Chemother 2009; 63:659–667 [View Article] [PubMed]
    [Google Scholar]
  60. Ye Y, Xu L, Han Y, Chen Z, Liu C et al. Mechanism for carbapenem resistance of clinical Enterobacteriaceae isolates. Exp Ther Med 2018; 15:1143–1149 [View Article] [PubMed]
    [Google Scholar]
  61. Hicks AL, Kissler SM, Lipsitch M, Grad YH, Holt KE. Surveillance to maintain the sensitivity of genotype-based antibiotic resistance diagnostics. PLoS Biol 2019; 17:e3000547 [View Article]
    [Google Scholar]
  62. Hawkey J, Le Hello S, Doublet B, Granier SA, Hendriksen RS et al. Global phylogenomics of multidrug-resistant Salmonella enterica serotype Kentucky ST198. Microbial Genomics 2019; 5: [View Article]
    [Google Scholar]
  63. Park AK, Shin E, Kim S, Park J, Jeong HJ et al. Traveller-associated high-level ciprofloxacin-resistant Salmonella enterica Serovar Kentucky in the Republic of Korea. J Glob Antimicrob Resist 2020; 22:190–194 [View Article] [PubMed]
    [Google Scholar]
  64. Harvey RR, Friedman CR, Crim SM, Judd M, Barrett KA et al. Epidemiology of Salmonella enterica serotype Dublin infections among humans, United States, 1968–2013. Emerg Infect Dis 2017; 23:1493–1501 [View Article]
    [Google Scholar]
  65. Mangat CS, Bekal S, Avery BP, Côté G, Daignault D et al. Genomic Investigation of the Emergence of Invasive Multidrug-Resistant Salmonella enterica Serovar Dublin in Humans and Animals in Canada. Antimicrob Agents Chemother 2019; 63: [View Article]
    [Google Scholar]
  66. Plumb ID, Schwensohn CA, Gieraltowski L, Tecle S, Schneider ZD et al. Outbreak of Salmonella newport infections with decreased susceptibility to azithromycin linked to beef obtained in the United States and soft cheese obtained in Mexico - United States, 2018-2019. MMWR Morb Mortal Wkly Rep 2019; 68:713–717 [View Article] [PubMed]
    [Google Scholar]
  67. Sidjabat HE, Seah KY, Coleman L, Sartor A, Derrington P et al. Expansive spread of IncI1 plasmids carrying blaCMY-2 amongst Escherichia coli. Int J Antimicrob Agents 2014; 44:203–208 [View Article] [PubMed]
    [Google Scholar]
  68. Nadimpalli M, Fabre L, Yith V, Sem N, Gouali M et al. CTX-M-55-type ESBL-producing Salmonella enterica are emerging among retail meats in Phnom Penh, Cambodia. J Antimicrob Chemother 2019; 74:342–348 [View Article] [PubMed]
    [Google Scholar]
  69. Hamamoto K, Ueda S, Toyosato T, Yamamoto Y, Hirai I. High prevalence of cPrevalence of Chromosomal blaCTX-M-14 in Escherichia coli isolates possessing blaCTX-M-14. Antimicrob Agents Chemother 2016; 60:2582–2584 [View Article] [PubMed]
    [Google Scholar]
  70. Sparham SJ, Kwong JC, Valcanis M, Easton M, Trott DJ et al. Emergence of multidrug resistance in locally-acquired human infections with Salmonella Typhimurium in Australia owing to a new clade harbouring blaCTX-M-9. Int J Antimicrob Agents 2017; 50:101–105 [View Article] [PubMed]
    [Google Scholar]
  71. Xu G, An W, Wang H, Zhang X. Prevalence and characteristics of extended-spectrum β-lactamase genes in Escherichia coli isolated from piglets with post-weaning diarrhea in Heilongjiang province, China. Front Microbiol 2015; 6:1103. [View Article] [PubMed]
    [Google Scholar]
  72. Chiu C-H, Lee J-J, Wang M-H, Chu C. Genetic analysis and plasmid-mediated blaCMY-2 in Salmonella and Shigella and the Ceftriaxone Susceptibility regulated by the ISEcp-1 tnpA-blaCMY-2-blc-sugE. Journal of Microbiology, Immunology and Infection 2021; 54:649–657 [View Article]
    [Google Scholar]
  73. Zhang C-Z, Ding X-M, Lin X-L, Sun R-Y, Lu Y-W et al. The emergence of chromosomally located blaCTX-M-55 in Salmonella from foodborne animals in China. Front Microbiol 2019; 10: [View Article]
    [Google Scholar]
  74. Lee W, Bloomfield S, Mather A, Edwards A, Chattaway M et al. Analysis of β-lactam, azithromycin and fosfomycin resistance in non-typhoidal Salmonella: Characterisation of an S. Infantis plasmid. Access Microbiology 2020; 2:7A [View Article]
    [Google Scholar]
  75. Brown AC, Chen JC, Watkins LKF, Campbell D, Folster JP et al. CTX-M-65 extended-spectrum β-lactamase-producing Salmonella enterica serotype Infantis, United States1. Emerg Infect Dis 2018; 24:2284–2291 [View Article] [PubMed]
    [Google Scholar]
  76. Karczmarczyk M, Wang J, Leonard N, Fanning S. Complete nucleotide sequence of a conjugative IncF plasmid from an Escherichia coli isolate of equine origin containing blaCMY-2 within a novel genetic context. FEMS Microbiol Lett 2014; 352:123–127 [View Article] [PubMed]
    [Google Scholar]
  77. Tagg KA, Iredell JR, Partridge SR. Complete sequencing of IncI1 sequence type 2 plasmid pJIE512b indicates mobilization of blaCMY-2 from an IncA/C plasmid. Antimicrob Agents Chemother 2014; 58:4949–4952 [View Article]
    [Google Scholar]
  78. Yassine H, Bientz L, Cros J, Goret J, Bébéar C et al. Experimental evidence for IS1294b-mediated transposition of the blaCMY-2 cephalosporinase gene in Enterobacteriaceae. J Antimicrob Chemother 2015; 70:697–700 [View Article] [PubMed]
    [Google Scholar]
  79. Yasugi M, Hatoya S, Motooka D, Matsumoto Y, Shimamura S et al. Whole-genome analyses of extended-spectrum or AmpC β-lactamase-producing Escherichia coli isolates from companion dogs in Japan. PloS one 2021; 16:e0246482 [View Article] [PubMed]
    [Google Scholar]
  80. Timme RE, Sanchez Leon M, Allard MW. Utilizing the public genometrakr database for foodborne pathogen traceback. Foodborne bacterial pathogens. In Methods in Molecular Biology. 1918 New York, NY: Springer New York; 2018 pp 201–212
    [Google Scholar]
  81. Li X-Z, Plésiat P, Nikaido H. The challenge of efflux-mediated antibiotic resistance in gram-negative bacteria. Clin Microbiol Rev 2015; 28:337–418 [View Article] [PubMed]
    [Google Scholar]
  82. Abraham S, Groves MD, Trott DJ, Chapman TA, Turner B et al.. Salmonella enterica isolated from infections in Australian livestock remain susceptible to critical antimicrobials. Int J Antimicrob Agents 2014; 43:126–130 [View Article]
    [Google Scholar]
  83. Arnott A, Wang Q, Bachmann N, Sadsad R, Biswas C et al. Multidrug-resistant Salmonella enterica 4,[5],12:i:- Sequence Type 34, New South Wales, Australia, 2016-2017. Emerg Infect Dis 2018; 24:751–753 [View Article] [PubMed]
    [Google Scholar]
  84. Cain AK, Liu X, Djordjevic SP, Hall RM. Transposons related to Tn1696 in IncHI2 plasmids in multiply antibiotic resistant Salmonella enterica serovar Typhimurium from Australian animals. Microb Drug Resist 2010; 16:197–202 [View Article] [PubMed]
    [Google Scholar]
  85. Graham RMA, Hiley L, Rathnayake IU, Jennison AV. Comparative genomics identifies distinct lineages of S. Enteritidis from Queensland, Australia. PLoS One 2018; 13:e0191042 [View Article]
    [Google Scholar]
  86. Miko A, Pries K, Schroeter A, Helmuth R. Molecular mechanisms of resistance in multidrug-resistant serovars of Salmonella enterica isolated from foods in Germany. J Antimicrob Chemother 2005; 56:1025–1033 [View Article] [PubMed]
    [Google Scholar]
  87. Pornsukarom S, Thakur S, Schaffner DW. Horizontal dissemination of antimicrobial resistance determinants in multiple Salmonella serotypes following isolation from the commercial swine operation environment after manure application. Appl Environ Microbiol 2017; 83:20 [View Article]
    [Google Scholar]
  88. Trongjit S, Angkititrakul S, Tuttle RE, Poungseree J, Padungtod P et al. Prevalence and antimicrobial resistance in Salmonella enterica isolated from broiler chickens, pigs and meat products in Thailand-Cambodia border provinces. Microbiol Immunol 2017; 61:23–33 [View Article] [PubMed]
    [Google Scholar]
  89. Yau S, Liu X, Djordjevic SP, Hall RM. RSF1010-like plasmids in Australian Salmonella enterica serovar Typhimurium and origin of their sul2-strA-strB antibiotic resistance gene cluster. Microb Drug Resist 2010; 16:249–252 [View Article] [PubMed]
    [Google Scholar]
  90. Ambrose SJ, Harmer CJ, Hall RM. Evolution and typing of IncC plasmids contributing to antibiotic resistance in Gram-negative bacteria. Plasmid 2018; 99:40–55 [View Article] [PubMed]
    [Google Scholar]
  91. Reid CJ, Roy Chowdhury P, Djordjevic SP. Tn6026 and Tn6029 are found in complex resistance regions mobilised by diverse plasmids and chromosomal islands in multiple antibiotic resistant Enterobacteriaceae. Plasmid 2015; 80:127–137 [View Article] [PubMed]
    [Google Scholar]
  92. Petrovska L, Mather AE, AbuOun M, Branchu P, Harris SR et al. Microevolution of monophasic Salmonella Typhimurium during epidemic, United Kingdom, 2005–2010. Emerg Infect Dis 2016; 22:617–624 [View Article]
    [Google Scholar]
  93. Ingle DJ, Ambrose RL, Baines SL, Duchene S, Gonçalves da Silva A et al. Evolutionary dynamics of multidrug resistant Salmonella enterica serovar 4,[5],12:i:- in Australia. Nat Commun 2021; 12:4786 [View Article]
    [Google Scholar]
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