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Volume 28, Number 1—January 2022
Research

New Sequence Types and Antimicrobial Drug–Resistant Strains of Streptococcus suis in Diseased Pigs, Italy, 2017–2019

Lucilla Cucco, Marta Paniccià, Francesca Romana Massacci, Alessandra Morelli, Massimo Ancora, Iolanda Mangone, Adriano Di Pasquale, Andrea Luppi, Denis Vio, Cesare Cammà, and Chiara Francesca MagistraliComments to Author 
Author affiliations: Istituto Zooprofilattico Sperimentale dell’Umbria e delle Marche ‘Togo Rosati,’ Perugia, Italy (L. Cucco, M. Paniccià, F.R. Massacci, A. Morelli, C.F. Magistrali); Istituto Zooprofilattico Sperimentale di Abruzzo e Molise ‘Giuseppe Caporale,’ Teramo, Italy (M. Ancora, I. Mangone, A. Di Pasquale, C. Cammà); Istituto Zooprofilattico Sperimentale della Lombardia e della Emilia-Romagna ‘Bruno Ubertini,’ Brescia, Italy (A. Luppi); Istituto Zooprofilattico Sperimentale delle Venezie, Padova, Italy (D. Vio)

Main Article

Table 1

Combination of putative virulence genes among sequence types and minimum core genome groups of Streptococcus suis from diseased pigs, Italy, 2017–2019*

Sequence type MCG group Serotype Virulence profile No. isolates/total no. isolates for each sequence type (%)
ST1 1 2 mrpEU/sly/epf 3/17 (17.6)
ST1 1 1/2 mrpEU/sly/epf 14/17 (82.4)
ST7 1 1/2 mrpEU /sly/epf 6/9 (66.6)
ST7 1 2 mrpEU /sly/epf 3/9 (33.3)
ST11 N 1 mrp/sly/epf 2/2 (100)
ST16 1 9 mrp*/sly 3/3 (100)
ST28 4 2 mrpNA1/sly 1/1 (100)
ST29 4 7 mrp* 3/6 (50)
mrpNA1 3/6 (50)
ST94 3 4 mrpNA1/sly 2/3 (66.7)
9 mrpNA1/sly 1/3 (33.3)
ST108 3 23 mrpNA1/sly 1/1 (100)
ST123 3 9 mrpNA1/sly 17/17 (100)
ST1540 N 9 - 3/3 (100)
ST1541 1 9 - 1/1 (100)
ST1542 N 3 - 1/1 (100)
ST1543 3 4 mrpNA1/sly 1/1 (100)
ST1544 3 4 mrpNA1/sly 1/2 (50)
5 mrpNA1/sly 1/2 (50)
ST1545 1 8 mrp* 1/1 (100)
ST1546 1 8 mrp/sly 1/1 (100)
ST1547 1 10 - 7/7 (100)
ST1548 N 15 sly 1/1 (100)
ST1549 N 19 - 1/1 (100)

*Dashes indicate absence of putative virulence genes according to PCR. mrp* is the mrp variant (22). MCG, minimum core genome; N, not groupable; ST, sequence type.

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References
  1. Princivalli  MS, Palmieri  C, Magi  G, Vignaroli  C, Manzin  A, Camporese  A, et al. Genetic diversity of Streptococcus suis clinical isolates from pigs and humans in Italy (2003-2007). Euro Surveill. 2009;14:19310. DOIPubMedGoogle Scholar
  2. Segura  M, Fittipaldi  N, Calzas  C, Gottschalk  M. Critical Streptococcus suis virulence factors: are they all really critical? Trends Microbiol. 2017;25:585–99. DOIPubMedGoogle Scholar
  3. Willemse  N, Howell  KJ, Weinert  LA, Heuvelink  A, Pannekoek  Y, Wagenaar  JA, et al. An emerging zoonotic clone in the Netherlands provides clues to virulence and zoonotic potential of Streptococcus suis. Sci Rep. 2016;6:28984. DOIPubMedGoogle Scholar
  4. Palmieri  C, Varaldo  PE, Facinelli  B. Streptococcus suis, an emerging drug-resistant animal and human pathogen. Front Microbiol. 2011;2:235. DOIPubMedGoogle Scholar
  5. Dong  W, Zhu  Y, Ma  Y, Ma  J, Zhang  Y, Yuan  L, et al. Multilocus sequence typing and virulence genotyping of Streptococcus suis serotype 9 isolates revealed high genetic and virulence diversity. FEMS Microbiol Lett. 2017;364:1–8. DOIPubMedGoogle Scholar
  6. Estrada  AA, Gottschalk  M, Rossow  S, Rendahl  A, Gebhart  C, Marthaler  DG. Serotype and genotype (multilocus sequence type) of Streptococcus suis isolates from the United States serve as predictors of pathotype. J Clin Microbiol. 2019;57:e00377–19. DOIPubMedGoogle Scholar
  7. Prüfer  TL, Rohde  J, Verspohl  J, Rohde  M, de Greeff  A, Willenborg  J, et al. Molecular typing of Streptococcus suis strains isolated from diseased and healthy pigs between 1996-2016. PLoS One. 2019;14:e0210801. DOIPubMedGoogle Scholar
  8. Goyette-Desjardins  G, Auger  JP, Xu  J, Segura  M, Gottschalk  M. Streptococcus suis, an important pig pathogen and emerging zoonotic agent-an update on the worldwide distribution based on serotyping and sequence typing. Emerg Microbes Infect. 2014;3:e45. DOIPubMedGoogle Scholar
  9. Blume  V, Luque  I, Vela  AI, Borge  C, Maldonado  A, Domínguez  L, et al. Genetic and virulence-phenotype characterization of serotypes 2 and 9 of Streptococcus suis swine isolates. Int Microbiol. 2009;12:161–6.PubMedGoogle Scholar
  10. Zheng  H, Du  P, Qiu  X, Kerdsin  A, Roy  D, Bai  X, et al. Genomic comparisons of Streptococcus suis serotype 9 strains recovered from diseased pigs in Spain and Canada. Vet Res (Faisalabad). 2018;49:1–13. DOIPubMedGoogle Scholar
  11. Estrada  AA, Gottschalk  M, Rossow  S, Rendahl  A, Gebhart  C, Marthaler  DG. Serotype and genotype (multilocus sequence type) of Streptococcus suis isolates from the United States serve as predictors of pathotype. J Clin Microbiol. 2019;57:1–16. DOIPubMedGoogle Scholar
  12. Ye  C, Bai  X, Zhang  J, Jing  H, Zheng  H, Du  H, et al. Spread of Streptococcus suis sequence type 7, China. Emerg Infect Dis. 2008;14:787–91. DOIPubMedGoogle Scholar
  13. Kerdsin  A, Hatrongjit  R, Gottschalk  M, Takeuchi  D, Hamada  S, Akeda  Y, et al. Emergence of Streptococcus suis serotype 9 infection in humans. J Microbiol Immunol Infect. 2017;50:545–6. DOIPubMedGoogle Scholar
  14. Willemse  N, van der Ark  KCH, Stockhofe-Zurwieden  N, Smith  H, Picavet  DI, van Solt-Smits  C, et al. Clonal expansion of a virulent Streptococcus suis serotype 9 lineage distinguishable from carriage subpopulations. Sci Rep. 2019;9:15429. DOIPubMedGoogle Scholar
  15. Werinder  A, Aspán  A, Backhans  A, Sjölund  M, Guss  B, Jacobson  M. Streptococcus suis in Swedish grower pigs: occurrence, serotypes, and antimicrobial susceptibility. Acta Vet Scand. 2020;62:36. DOIPubMedGoogle Scholar
  16. Rieckmann  K, Pendzialek  SM, Vahlenkamp  T, Baums  CG. A critical review speculating on the protective efficacies of autogenous Streptococcus suis bacterins as used in Europe. Porcine Health Manag. 2020;6:12. DOIPubMedGoogle Scholar
  17. O’Dea  MA, Laird  T, Abraham  R, Jordan  D, Lugsomya  K, Fitt  L, et al. Examination of Australian Streptococcus suis isolates from clinically affected pigs in a global context and the genomic characterisation of ST1 as a predictor of virulence. Vet Microbiol. 2018;226:31–40. DOIPubMedGoogle Scholar
  18. Rieckmann  K, Seydel  A, Szewczyk  K, Klimke  K, Rungelrath  V, Baums  CG. Streptococcus suis cps7: an emerging virulent sequence type (ST29) shows a distinct, IgM-determined pattern of bacterial survival in blood of piglets during the early adaptive immune response after weaning. Vet Res (Faisalabad). 2018;49:48. DOIPubMedGoogle Scholar
  19. Du  F, Lv  X, Duan  D, Wang  L, Huang  J. Characterization of a linezolid- and vancomycin-resistant Streptococcus suis isolate that harbors optrA and vanG operons. Front Microbiol. 2019;10:2026. DOIPubMedGoogle Scholar
  20. Okwumabua  O, O’Connor  M, Shull  E. A polymerase chain reaction (PCR) assay specific for Streptococcus suis based on the gene encoding the glutamate dehydrogenase. FEMS Microbiol Lett. 2003;218:79–84. DOIPubMedGoogle Scholar
  21. Smith  HE, Reek  FH, Vecht  U, Gielkens  ALJ, Smits  MA. Repeats in an extracellular protein of weakly pathogenic strains of Streptococcus suis type 2 are absent in pathogenic strains. Infect Immun. 1993;61:3318–26. DOIPubMedGoogle Scholar
  22. Silva  LMG, Baums  CG, Rehm  T, Wisselink  HJ, Goethe  R, Valentin-Weigand  P. Virulence-associated gene profiling of Streptococcus suis isolates by PCR. Vet Microbiol. 2006;115:117–27. DOIPubMedGoogle Scholar
  23. Fittipaldi  N, Fuller  TE, Teel  JF, Wilson  TL, Wolfram  TJ, Lowery  DE, et al. Serotype distribution and production of muramidase-released protein, extracellular factor and suilysin by field strains of Streptococcus suis isolated in the United States. Vet Microbiol. 2009;139:310–7. DOIPubMedGoogle Scholar
  24. Clinical and Laboratory Standards Institute. VET08 performance standards for antimicrobial disk. 4th ed. Wayne (PA): The Institute; 2018.
  25. Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing (M100). Wayne (PA): The Institute; 2017. p. 27–39
  26. Bolger  AM, Lohse  M, Usadel  B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–20. DOIPubMedGoogle Scholar
  27. Bankevich  A, Nurk  S, Antipov  D, Gurevich  AA, Dvorkin  M, Kulikov  AS, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19:455–77. DOIPubMedGoogle Scholar
  28. Wileman  TM, Weinert  LA, Howell  KJ, Wang  J, Peters  SE, Williamson  SM, et al. Pathotyping the zoonotic pathogen Streptococcus suis: novel genetic markers to differentiate invasive disease-associated isolates from non-disease-associated isolates from England and Wales. J Clin Microbiol. 2019;57:1–15. DOIPubMedGoogle Scholar
  29. Price  MN, Dehal  PS, Arkin  AP. FastTree 2—approximately maximum-likelihood trees for large alignments. PLoS One. 2010;5:e9490. DOIPubMedGoogle Scholar
  30. 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
  31. Feldgarden  M, Brover  V, Haft  DH, Prasad  AB, Slotta  DJ, Tolstoy  I, et al. Validating the AMRFINder tool and resistance gene database by using antimicrobial resistance genotype-phenotype correlations in a collection of isolates. Antimicrob Agents Chemother. 2019;63:1–20. DOIPubMedGoogle Scholar
  32. Jia  B, Raphenya  AR, Alcock  B, Waglechner  N, Guo  P, Tsang  KK, et al. CARD 2017: expansion and model-centric curation of the comprehensive antibiotic resistance database. Nucleic Acids Res. 2017;45(D1):D566–73. DOIPubMedGoogle Scholar
  33. Zankari  E, Hasman  H, Cosentino  S, Vestergaard  M, Rasmussen  S, Lund  O, et al. Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother. 2012;67:2640–4. DOIPubMedGoogle Scholar
  34. Gupta  SK, Padmanabhan  BR, Diene  SM, Lopez-Rojas  R, Kempf  M, Landraud  L, et al. ARG-ANNOT, a new bioinformatic tool to discover antibiotic resistance genes in bacterial genomes. Antimicrob Agents Chemother. 2014;58:212–20. DOIPubMedGoogle Scholar
  35. Camacho  C, Coulouris  G, Avagyan  V, Ma  N, Papadopoulos  J, Bealer  K, et al. BLAST+: architecture and applications. BMC Bioinformatics. 2009;10:421. DOIPubMedGoogle Scholar
  36. TeamCore. R: A language and environment for statistical computing [cited 2021 Dec 20]. https://www.R-project.org
  37. Wisselink  HJ, Smith  HE, Stockhofe-Zurwieden  N, Peperkamp  K, Vecht  U. Distribution of capsular types and production of muramidase-released protein (MRP) and extracellular factor (EF) of Streptococcus suis strains isolated from diseased pigs in seven European countries. Vet Microbiol. 2000;74:237–48. DOIPubMedGoogle Scholar
  38. Lacouture  S, Okura  M, Takamatsu  D, Corsaut  L, Gottschalk  M. Development of a mismatch amplification mutation assay to correctly serotype isolates of Streptococcus suis serotypes 1, 2, 1/2, and 14. J Vet Diagn Invest. 2020;32:490–4. DOIPubMedGoogle Scholar
  39. Mancini  F, Adamo  F, Creti  R, Monaco  M, Alfarone  G, Pantosti  A, et al. A fatal case of streptococcal toxic shock syndrome caused by Streptococcus suis carrying tet (40) and tet (O/W/32/O), Italy. J Infect Chemother. 2016;22:774–6. DOIPubMedGoogle Scholar
  40. Fittipaldi  N, Xu  J, Lacouture  S, Tharavichitkul  P, Osaki  M, Sekizaki  T, et al. Lineage and virulence of Streptococcus suis serotype 2 isolates from North America. Emerg Infect Dis. 2011;17:2239–44. DOIPubMedGoogle Scholar
  41. Chen  C, Zhang  W, Zheng  H, Lan  R, Wang  H, Du  P, et al. Minimum core genome sequence typing of bacterial pathogens: a unified approach for clinical and public health microbiology. J Clin Microbiol. 2013;51:2582–91. DOIPubMedGoogle Scholar
  42. Guo  G, Du  D, Yu  Y, Zhang  Y, Qian  Y, Zhang  W. Pan-genome analysis of Streptococcus suis serotype 2 revealed genomic diversity among strains of different virulence. Transbound Emerg Dis. 2021;68:637–47. DOIPubMedGoogle Scholar
  43. Dong  X, Chao  Y, Zhou  Y, Zhou  R, Zhang  W, Fischetti  VA, et al. The global emergence of a novel Streptococcus suis clade associated with human infections. EMBO Mol Med. 2021;13:e13810. DOIPubMedGoogle Scholar
  44. Dong  W, Ma  J, Zhu  Y, Zhu  J, Yuan  L, Wang  Y, et al. Virulence genotyping and population analysis of Streptococcus suis serotype 2 isolates from China. Infect Genet Evol. 2015;36:483–9. DOIPubMedGoogle Scholar
  45. Zhang  C, Zhang  P, Wang  Y, Fu  L, Liu  L, Xu  D, et al. Capsular serotypes, antimicrobial susceptibility, and the presence of transferable oxazolidinone resistance genes in Streptococcus suis isolated from healthy pigs in China. Vet Microbiol. 2020;247:108750. DOIPubMedGoogle Scholar
  46. Hong  B, Ba  Y, Niu  L, Lou  F, Zhang  Z, Liu  H, et al. A comprehensive research on antibiotic resistance genes in microbiota of aquatic animals. Front Microbiol. 2018;9:1617. DOIPubMedGoogle Scholar
  47. Fioriti  S, Morroni  G, Coccitto  SN, Brenciani  A, Antonelli  A, Di Pilato  V, et al. Detection of oxazolidinone resistance genes and characterization of genetic environments in enterococci of Swine origin, Italy. Microorganisms. 2020;8:2021. DOIPubMedGoogle Scholar
  48. European Centre for Disease Prevention and Control (ECDC)European Food Safety Authority (EFSA). European Medicines Agency (EMA). ECDC/EFSA/EMA second joint report on the integrated analysis of the consumption of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from humans and food-producing animals: Joint Interagency Antimicrobial Consumption and Resistance Analysis (JIACRA). Report. EFSA J. 2017;15:e04872.PubMedGoogle Scholar
  49. van Hout  J, Heuvelink  A, Gonggrijp  M. Monitoring of antimicrobial susceptibility of Streptococcus suis in the Netherlands, 2013-2015. Vet Microbiol. 2016;194:5–10. DOIPubMedGoogle Scholar

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Page updated: December 20, 2021
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