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Volume 30, Number 4—April 2024
Research

Emergence of Poultry-Associated Human Salmonella enterica Serovar Abortusovis Infections, New South Wales, Australia

Michael Payne, Sarah Williamson, Qinning Wang, Xiaomei Zhang, Vitali Sintchenko, Anthony Pavic, and Ruiting LanComments to Author 
Author affiliations: University of New South Wales, Sydney, New South Wales, Australia (M. Payne, X. Zhang, R. Lan); Birling Laboratories, Bringelly, New South Wales, Australia (S. Williamson, A. Pavic); Institute of Clinical Pathology and Medical Research–NSW Health Pathology, Westmead Hospital, Westmead, New South Wales, Australia (Q. Wang, V. Sintchenko); University of Sydney, Sydney (V. Sintchenko)

Main Article

Table 4

Sensitivity and specificity of serovar-specific gene markers in a study of the emergence of poultry-associated human Salmonella enterica serovar Abortusovis infections, New South Wales, Australia*

Specific genes No. isolates Length, bp Sensitivity† Specificity†
 Protein function
Identification, n = 2,314 Validation, n = 1,088
Abortusovis-gene1 56 2,367 100 100 100 DUF6430
Abortusovis-gene2 56 330 100 100 100 Hypothetical
Abortusovis-AUS-gene1 51 831 100 100 100 DUF4238
Abortusovis-AUS-gene2 51 810 100 100 100 Hypothetical

*AUS, Australia; FN, false negative; TN, true negative; TP, true positive. †We used sensitivity and specificity as described in previous studies (29,32), where sensitivity is TP/(TP+FN) and specificity is TN/(TN+FP). Per those studies, we defined FN as the genomes from Salmonella Abortusovis lacking any of those same gene markers; FP as the genomes from other serovars containing all those same gene markers; TN as the genomes from other serovars lacking any of those same gene markers; and TP as the genomes from Salmonella Abortusovis containing all specific gene markers for Salmonella Abortusovis.

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References
  1. Jack  E. Salmonella Abortus Ovis—an atypical Salmonella. Vet Rec. 1968;82:558.
  2. Pardon  P, Sanchis  R, Marly  J, Lantier  F, Pépin  M, Popoff  M. [Ovine salmonellosis caused by Salmonella abortus ovis] [in French]. Ann Rech Vet. 1988;19:221–35.PubMedGoogle Scholar
  3. Belloy  L, Decrausaz  L, Boujon  P, Hächler  H, Waldvogel  AS. Diagnosis by culture and PCR of Salmonella abortusovis infection under clinical conditions in aborting sheep in Switzerland. Vet Microbiol. 2009;138:373–7. DOIPubMedGoogle Scholar
  4. Vodas  K, Marinov  MF, Shabanov  M. [Salmonella abortus ovis carrier state in dogs and rats] [in Bulgarian]. Vet Med Nauki. 1985;22:10–5.PubMedGoogle Scholar
  5. Bacciu  D, Falchi  G, Spazziani  A, Bossi  L, Marogna  G, Leori  GS, et al. Transposition of the heat-stable toxin astA gene into a gifsy-2-related prophage of Salmonella enterica serovar Abortusovis. J Bacteriol. 2004;186:4568–74. DOIPubMedGoogle Scholar
  6. Colombo  MM, Leori  G, Rubino  S, Barbato  A, Cappuccinelli  P. Phenotypic features and molecular characterization of plasmids in Salmonella abortusovis. Microbiology. 1992;138:725–31.
  7. Uzzau  S, Gulig  PA, Paglietti  B, Leori  G, Stocker  BA, Rubino  S. Role of the Salmonella abortusovis virulence plasmid in the infection of BALB/c mice. FEMS Microbiol Lett. 2000;188:15–8. DOIPubMedGoogle Scholar
  8. Habrun  B, Listes  E, Spicic  S, Cvetnic  Z, Lukacevic  D, Jemersic  L, et al. An outbreak of Salmonella Abortusovis abortions in sheep in south Croatia. J Vet Med B Infect Dis Vet Public Health. 2006;53:286–90. DOIPubMedGoogle Scholar
  9. Wirz-Dittus  S, Belloy  L, Hüssy  D, Waldvogel  AS, Doherr  MG. Seroprevalence survey for Salmonella Abortusovis infection in Swiss sheep flocks. Prev Vet Med. 2010;97:126–30. DOIPubMedGoogle Scholar
  10. Valdezate  S, Astorga  R, Herrera-León  S, Perea  A, Usera  MA, Huerta  B, et al. Epidemiological tracing of Salmonella enterica serotype Abortusovis from Spanish ovine flocks by PFGE fingerprinting. Epidemiol Infect. 2007;135:695–702. DOIPubMedGoogle Scholar
  11. Dionisi  AM, Carattoli  A, Luzzi  I, Magistrali  C, Pezzotti  G. Molecular genotyping of Salmonella enterica Abortusovis by pulsed field gel electrophoresis. Vet Microbiol. 2006;116:217–23. DOIPubMedGoogle Scholar
  12. Schiaffino  A, Beuzón  CR, Uzzau  S, Leori  G, Cappuccinelli  P, Casadesús  J, et al. Strain typing with IS200 fingerprints in Salmonella abortusovis. Appl Environ Microbiol. 1996;62:2375–80. DOIPubMedGoogle Scholar
  13. Nikbakht  GH, Raffatellu  M, Uzzau  S, Tadjbakhsh  H, Rubino  S. IS200 fingerprinting of Salmonella enterica serotype Abortusovis strains isolated in Iran. Epidemiol Infect. 2002;128:333–6. DOIPubMedGoogle Scholar
  14. Australian Government Department of Agriculture, Fisheries and Forestry. Animal Health Australia 2009. Canberra (ACT), Australia: The Department; 2010.
  15. Heuzenroeder  MW, Ross  IL, Hocking  H, Davos  D, Young  CC, Morgan  G. An integrated typing service for the surveillance of Salmonella in chickens. Barton (ACT): Rural Industries Research and Development Corporation, Australian Government; 2013.
  16. Abraham  S, O’Dea  M, Sahibzada  S, Hewson  K, Pavic  A, Veltman  T, et al. Escherichia coli and Salmonella spp. isolated from Australian meat chickens remain susceptible to critically important antimicrobial agents. PLoS One. 2019;14:e0224281. DOIPubMedGoogle Scholar
  17. Seemann  T. snippy: fast bacterial variant calling from NGS reads, version 3.1 [cited 2020 Apr 19]. https://github.com/tseemann/snippy
  18. Minh  BQ, Schmidt  HA, Chernomor  O, Schrempf  D, Woodhams  MD, von Haeseler  A, et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol. 2020;37:1530–4. DOIPubMedGoogle Scholar
  19. 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(W1):W242-5. DOIPubMedGoogle Scholar
  20. Bouckaert  R, Vaughan  TG, Barido-Sottani  J, Duchêne  S, Fourment  M, Gavryushkina  A, et al. BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLOS Comput Biol. 2019;15:e1006650. DOIPubMedGoogle Scholar
  21. Page  AJ, Cummins  CA, Hunt  M, Wong  VK, Reuter  S, Holden  MT, et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics. 2015;31:3691–3. DOIPubMedGoogle Scholar
  22. Brynildsrud  O, Bohlin  J, Scheffer  L, Eldholm  V. Rapid scoring of genes in microbial pan-genome-wide association studies with Scoary. Genome Biol. 2016;17:238. DOIPubMedGoogle Scholar
  23. Clausen  PTLC, Aarestrup  FM, Lund  O. Rapid and precise alignment of raw reads against redundant databases with KMA. BMC Bioinformatics. 2018;19:307. DOIPubMedGoogle Scholar
  24. Syberg-Olsen  MJ, Garber  AI, Keeling  PJ, McCutcheon  JP, Husnik  F. Pseudofinder: detection of pseudogenes in prokaryotic genomes. Mol Biol Evol. 2022;39:msac153.
  25. Liu  B, Zheng  D, Jin  Q, Chen  L, Yang  J. VFDB 2019: a comparative pathogenomic platform with an interactive web interface. Nucleic Acids Res. 2019;47(D1):D687–92. DOIPubMedGoogle Scholar
  26. Carattoli  A, Hasman  H. PlasmidFinder and in silico pMLST: identification and typing of plasmid replicons in whole-genome sequencing (WGS). Methods Mol Biol. 2020;2075:285–94. DOIPubMedGoogle Scholar
  27. Seemann  T. ABRicate, mass screening of contigs for antimicrobial resistance or virulence genes. 1.0.1 [cited 2020 Apr 19]. https://github.com/tseemann/abricate
  28. Wishart  DS, Han  S, Saha  S, Oler  E, Peters  H, Grant  JR, et al. PHASTEST: faster than PHASTER, better than PHAST. Nucleic Acids Res. 2023;51(W1):W443–50. DOIPubMedGoogle Scholar
  29. Zhang  X, Payne  M, Lan  R. In silico identification of serovar-specific genes for Salmonella serotyping. Front Microbiol. 2019;10:835. DOIPubMedGoogle Scholar
  30. Alikhan  NF, Zhou  Z, Sergeant  MJ, Achtman  M. A genomic overview of the population structure of Salmonella. PLoS Genet. 2018;14:e1007261. DOIPubMedGoogle Scholar
  31. Allison  GE, Angeles  D, Tran-Dinh  N, Verma  NK. Complete genomic sequence of SfV, a serotype-converting temperate bacteriophage of Shigella flexneri. J Bacteriol. 2002;184:1974–87. DOIPubMedGoogle Scholar
  32. Zhang  X, Payne  M, Nguyen  T, Kaur  S, Lan  R. Cluster-specific gene markers enhance Shigella and enteroinvasive Escherichia coli in silico serotyping. Microb Genom. 2021;7:000704. DOIPubMedGoogle Scholar
  33. Clune  T, Beetson  S, Besier  S, Knowles  G, Paskin  R, Rawlin  G, et al. Ovine abortion and stillbirth investigations in Australia. Aust Vet J. 2020;1:22.PubMedGoogle Scholar
  34. Price  SL, Vadyvaloo  V, DeMarco  JK, Brady  A, Gray  PA, Kehl-Fie  TE, et al. Yersiniabactin contributes to overcoming zinc restriction during Yersinia pestis infection of mammalian and insect hosts. Proc Natl Acad Sci U S A. 2021;118:e2104073118. DOIPubMedGoogle Scholar
  35. Wellawa  DH, Allan  B, White  AP, Köster  W. Iron-uptake systems of chicken-associated Salmonella serovars and their role in colonizing the avian host. Microorganisms. 2020;8:1203. DOIPubMedGoogle Scholar
  36. Schubert  S, Picard  B, Gouriou  S, Heesemann  J, Denamur  E. Yersinia high-pathogenicity island contributes to virulence in Escherichia coli causing extraintestinal infections. Infect Immun. 2002;70:5335–7. DOIPubMedGoogle Scholar
  37. Liu  D, Yang  Y, Gu  J, Tuo  H, Li  P, Xie  X, et al. The Yersinia high-pathogenicity island (HPI) carried by a new integrative and conjugative element (ICE) in a multidrug-resistant and hypervirulent Klebsiella pneumoniae strain SCsl1. Vet Microbiol. 2019;239:108481. DOIPubMedGoogle Scholar
  38. Miller  RA, Wiedmann  M. The cytolethal distending toxin produced by nontyphoidal Salmonella serotypes Javiana, Montevideo, Oranienburg, and Mississippi induces DNA damage in a manner similar to that of serotype Typhi. MBio. 2016;7:e02109–16. DOIPubMedGoogle Scholar
  39. Joerger  RD, Choi  S. Contribution of the hdeB-like gene (SEN1493) to survival of Salmonella enterica enteritidis Nal(R) at pH 2. Foodborne Pathog Dis. 2015;12:353–9. DOIPubMedGoogle Scholar
  40. Deckers  D, Vanlint  D, Callewaert  L, Aertsen  A, Michiels  CW. Role of the lysozyme inhibitor Ivy in growth or survival of Escherichia coli and Pseudomonas aeruginosa bacteria in hen egg white and in human saliva and breast milk. Appl Environ Microbiol. 2008;74:4434–9. DOIPubMedGoogle Scholar
  41. Thiennimitr  P, Winter  SE, Winter  MG, Xavier  MN, Tolstikov  V, Huseby  DL, et al. Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota. Proc Natl Acad Sci U S A. 2011;108:17480–5. DOIPubMedGoogle Scholar
  42. Anderson  CJ, Clark  DE, Adli  M, Kendall  MM. Ethanolamine signaling promotes Salmonella niche recognition and adaptation during infection. PLoS Pathog. 2015;11:e1005278. DOIPubMedGoogle Scholar
  43. Harris  JB, Baresch-Bernal  A, Rollins  SM, Alam  A, LaRocque  RC, Bikowski  M, et al. Identification of in vivo-induced bacterial protein antigens during human infection with Salmonella enterica serovar Typhi. Infect Immun. 2006;74:5161–8. DOIPubMedGoogle Scholar
  44. Harvey  PC, Watson  M, Hulme  S, Jones  MA, Lovell  M, Berchieri  A Jr, et al. Salmonella enterica serovar typhimurium colonizing the lumen of the chicken intestine grows slowly and upregulates a unique set of virulence and metabolism genes. Infect Immun. 2011;79:4105–21. DOIPubMedGoogle Scholar
  45. Hoelzer  K, Moreno Switt  AI, Wiedmann  M. Animal contact as a source of human non-typhoidal salmonellosis. Vet Res (Faisalabad). 2011;42:34. DOIPubMedGoogle Scholar
  46. Sabbagh  SC, Lepage  C, McClelland  M, Daigle  F. Selection of Salmonella enterica serovar Typhi genes involved during interaction with human macrophages by screening of a transposon mutant library. PLoS One. 2012;7:e36643. DOIPubMedGoogle Scholar
  47. Sana  TG, Flaugnatti  N, Lugo  KA, Lam  LH, Jacobson  A, Baylot  V, et al. Salmonella Typhimurium utilizes a T6SS-mediated antibacterial weapon to establish in the host gut. Proc Natl Acad Sci U S A. 2016;113:E5044–51. DOIPubMedGoogle Scholar
  48. Langridge  GC, Fookes  M, Connor  TR, Feltwell  T, Feasey  N, Parsons  BN, et al. Patterns of genome evolution that have accompanied host adaptation in Salmonella. Proc Natl Acad Sci U S A. 2015;112:863–8. DOIPubMedGoogle Scholar
  49. AbuOun  M, Jones  H, Stubberfield  E, Gilson  D, Shaw  LP, Hubbard  ATM, et al.; On Behalf Of The Rehab Consortium. A genomic epidemiological study shows that prevalence of antimicrobial resistance in Enterobacterales is associated with the livestock host, as well as antimicrobial usage. Microb Genom. 2021;7:10–2. DOIPubMedGoogle Scholar
  50. McLure  A, Shadbolt  C, Desmarchelier  PM, Kirk  MD, Glass  K. Source attribution of salmonellosis by time and geography in New South Wales, Australia. BMC Infect Dis. 2022;22:14. DOIPubMedGoogle Scholar

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