Skip to main content

Advertisement

SpringerLink
Log in

Epidemiology of the Staphylococcus aureus CA-MRSA USA300 in Belgium

  • Original Article
  • Published:
European Journal of Clinical Microbiology & Infectious Diseases Aims and scope Submit manuscript

Abstract

The methicillin-resistant Staphylococcus aureus (MRSA) sequence type (ST) 8 Panton-Valentine toxin (PVL)-positive USA300 clone has a worldwide distribution. The USA300 North American (NA) variant, harbouring the arginine catabolic mobile element (ACME), is predominant in the USA while the Latin American (LV) variant is predominant in Northern South America. Both variants have failed to become endemic in Europe. We examined here the epidemiology of the USA300 clone in Belgium from 2006 to 2019. A total of 399 clonal complex 8 PVL-positive MRSA isolates received between 2006 and 2019 by the Belgian National Reference Laboratory for S. aureus were investigated for the presence of ACME. Selected ACME-positive (n=102) and ACME-negative (n=16) isolates were sequenced, characterized for the presence of several resistance and virulence molecular markers and subjected to phylogenetic analysis. A total of 300 isolates were USA300-NA (ACME-positive), while only 99 were ACME-negative. Most USA300-NA interspersed in the phylogeny analysis with isolates from other countries, suggesting multiple introductions. However, two big clades were maintained and spread over a decade, peaking between 2010 and 2017 to finally decrease. Few ACME-negative isolates, mainly related to trips to South America, were identified as USA300-LV. The remaining ACME-negative isolates were ST8 SCCmec IVb or ST923 SCCmec IVa (COL923). Two clades of the USA300-NA clone have successfully spread in Belgium, but seem to currently decrease. Related South American variants have been detected for the first time in Belgium, including the emerging COL923 clone.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Junie LM, Jeican II, Matros L, Pandrea SL (2018) Molecular epidemiology of the community-associated methicillin-resistant Staphylococcus aureus clones: a synthetic review. Clujul Med 91(1):7–11

  2. Planet PJ (2017) Life after USA300: the rise and fall of a superbug. J Infect Dis 215(suppl_1):S71–SS7

    Article  CAS  Google Scholar 

  3. Liu C, Graber CJ, Karr M et al (2008) A population-based study of the incidence and molecular epidemiology of methicillin-resistant Staphylococcus aureus disease in San Francisco, 2004-2005. Clin Infect Dis 46(11):1637–1646

    Article  CAS  Google Scholar 

  4. Boyle-Vavra S, Li X, Alam MT et al (2015) USA300 and USA500 clonal lineages of Staphylococcus aureus do not produce a capsular polysaccharide due to conserved mutations in the cap5 locus. mBio 6(2):e02585–e02514

    Article  Google Scholar 

  5. Planet PJ, Diaz L, Kolokotronis SO et al (2015) Parallel Epidemics of community-associated methicillin-resistant Staphylococcus aureus USA300 infection in North and South America. J Infect Dis 212(12):1874–1882

    Article  CAS  Google Scholar 

  6. Uhlemann AC, Dordel J, Knox JR et al (2014) Molecular tracing of the emergence, diversification, and transmission of S. aureus sequence type 8 in a New York community. Proc Natl Acad Sci U S A 111(18):6738–6743

    Article  CAS  Google Scholar 

  7. Glaser P, Martins-Simões P, Villain A et al (2016) Demography and intercontinental spread of the USA300 community-acquired methicillin-resistant Staphylococcus aureus lineage. mBio 7(1):e02183–e02115

    Article  CAS  Google Scholar 

  8. Strauss L, Stegger M, Akpaka PE et al (2017) Origin, evolution, and global transmission of community-acquired Staphylococcus aureus ST8. Proc Natl Acad Sci U S A 114(49):E10596–E1E604

    Article  CAS  Google Scholar 

  9. Toleman MS, Reuter S, Jamrozy D et al (2019) Prospective genomic surveillance of methicillin-resistant Staphylococcus aureus (MRSA) associated with bloodstream infection, England, 1 October 2012 to 30 September 2013. Euro Surveill 24(4):1800215

    Article  Google Scholar 

  10. Planet PJ, Diaz L, Rios R, Arias CA (2016) Global spread of the community-associated methicillin-resistant Staphylococcus aureus USA300 Latin American variant. J Infect Dis 214(10):1609–1610

    Article  Google Scholar 

  11. Von Dach E, Diene SM, Fankhauser C, Schrenzel J, Harbarth S, Francois P (2016) Comparative genomics of community-associated methicillin-resistant Staphylococcus aureus shows the emergence of clone ST8-USA300 in Geneva, Switzerland. J Infect Dis 213(9):1370–1379

    Article  Google Scholar 

  12. Brauner J, Hallin M, Deplano A et al (2013) Community-acquired methicillin-resistant Staphylococcus aureus clones circulating in Belgium from 2005 to 2009: changing epidemiology. Eur J Clin Microbiol Infect Dis 32(5):613–620

    Article  CAS  Google Scholar 

  13. Kairet K, Ho E, Van Kerkhoven D et al (2017) USA300, a strain of community-associated methicillin-resistant Staphylococcus aureus, crossing Belgium’s borders: outbreak of skin and soft tissue infections in a hospital in Belgium. Eur J Clin Microbiol Infect Dis 36(5):905–909

  14. Ridom SeqSphere+. https://www.ridom.de/seqsphere/

  15. EUCAST. Breakpoint tables for interpretation of MICs and zone diameters. Version 9.0. 2019: http://www.eucast.org

  16. Bankevich A, Nurk S, Antipov D et al (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19(5):455–477

    Article  CAS  Google Scholar 

  17. Heinrichs A, Argudin MA, De Mendonca R et al (2019) An outpatient clinic as a potential site of transmission for an outbreak of New Delhi metallo-beta-lactamase-producing Klebsiella pneumoniae sequence type 716: a study using whole-genome sequencing. Clin Infect Dis 68(6):993–1000

    Article  Google Scholar 

  18. Strauss L, Ruffing U, Abdulla S et al (2016) Detecting Staphylococcus aureus virulence and resistance genes: a comparison of whole-genome sequencing and DNA microarray technology. J Clin Microbiol 54(4):1008–1016

    Article  CAS  Google Scholar 

  19. Guardabassi L, Moodley A, Williams A et al (2019) High prevalence of USA300 among clinical isolates of methicillin-resistant Staphylococcus aureus on St. Kitts and Nevis, West Indies. Front Microbiol 10:1123

    Article  Google Scholar 

  20. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59(3):307–321

    Article  CAS  Google Scholar 

  21. Lefort V, Longueville JE, Gascuel O (2017) SMS: smart model selection in PhyML. Mol Biol Evol 34(9):2422–2424

    Article  CAS  Google Scholar 

  22. Letunic I, Bork P (2019) Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res 47(W1):W256–W2W9

    Article  CAS  Google Scholar 

  23. Goyal M, Javerliat F, Palmieri M et al (2019) Genomic evolution of Staphylococcus aureus during artificial and natural colonization of the human nose. Front Microbiol 10:1525

    Article  Google Scholar 

  24. Center for Genomic Epidemiology. Available at: http://www.genomicepidemiology.org/. Accessed October 2019.

  25. Larsen MV, Cosentino S, Rasmussen S et al (2012) Multilocus sequence typing of total-genome-sequenced bacteria. J Clin Microbiol 50(4):1355–1361

    Article  CAS  Google Scholar 

  26. Zankari E, Hasman H, Cosentino S et al (2012) Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother 67:2640–2644

    Article  CAS  Google Scholar 

  27. Kaya H, Hasman H, Larsen J et al (2018) SCCmecFinder, a web-based tool for typing of staphylococcal cassette chromosome mec in Staphylococcus aureus using whole-genome sequence data. mSphere 3(1):e00612–e00617

    Article  Google Scholar 

  28. Carattoli A, Hasman H (2020) PlasmidFinder and in silico pMLST: identification and typing of plasmid replicons in whole-genome sequencing (WGS). Methods Mol Biol 2075:285–294

    Article  CAS  Google Scholar 

  29. BacMet: Antibacterial biocide and metal resistance genes database. Available at: http://bacmet.biomedicine.gu.se/. Accessed October 2019.

  30. Pal C, Bengtsson-Palme J, Rensing C, Kristiansson E, Larsson DG (2014) BacMet: antibacterial biocide and metal resistance genes database. Nucleic Acids Res 42(Database issue):D737–D743

    Article  CAS  Google Scholar 

  31. Heatmapper. Available at www.heatmapper.ca. Accessed January 2021.

  32. Denis O, Deplano A, De Beenhouwer H et al (2005) Polyclonal emergence and importation of community-acquired methicillin-resistant Staphylococcus aureus strains harbouring Panton-Valentine leucocidin genes in Belgium. J Antimicrob Chemother 56(6):1103–1106

    Article  CAS  Google Scholar 

  33. Enstrom J, Froding I, Giske CG et al (2018) USA300 methicillin-resistant Staphylococcus aureus in Stockholm, Sweden, from 2008 to 2016. PLoS One 13(11):e0205761

    Article  Google Scholar 

  34. Kennedy AD, Porcella SF, Martens C et al (2010) Complete nucleotide sequence analysis of plasmids in strains of Staphylococcus aureus clone USA300 reveals a high level of identity among isolates with closely related core genome sequences. J Clin Microbiol 48(12):4504–4511

    Article  CAS  Google Scholar 

  35. Senn L, Clerc O, Zanetti G et al (2016) The stealthy superbug: the role of asymptomatic enteric carriage in maintaining a long-term hospital outbreak of ST228 methicillin-resistant Staphylococcus aureus. mBio 7(1):e02039–e02015

    Article  CAS  Google Scholar 

  36. Worby CJ, Chang HH, Hanage WP, Lipsitch M (2014) The distribution of pairwise genetic distances: a tool for investigating disease transmission. Genetics 198(4):1395–1404

    Article  Google Scholar 

  37. Popovich KJ, Snitkin E, Green SJ et al (2016) Genomic epidemiology of USA300 methicillin-resistant Staphylococcus aureus in an urban community. Clin Infect Dis 62(1):37–44

    Article  CAS  Google Scholar 

  38. Read TD, Petit RA 3rd, Yin Z, Montgomery T, McNulty MC, David MZ (2018) USA300 Staphylococcus aureus persists on multiple body sites following an infection. BMC Microbiol 18(1):206

    Article  CAS  Google Scholar 

  39. Challagundla L, Luo X, Tickler IA et al (2018) Range expansion and the origin of USA300 North American epidemic methicillin-resistant Staphylococcus aureus. MBio 9(1):e02016–e02017

    Article  Google Scholar 

  40. Wu K, Conly J, McClure JA, Kurwa HA, Zhang K (2020) Arginine catabolic mobile element in evolution and pathogenicity of the community-associated methicillin-resistant Staphylococcus aureus strain USA300. Microorganisms 8(2):275

    Article  CAS  Google Scholar 

  41. Arias CA, Rincon S, Chowdhury S et al (2008) MRSA USA300 clone and VREF--a U.S.-Colombian connection? N Engl J Med 359(20):2177–2179

    Article  CAS  Google Scholar 

  42. Escobar-Perez J, Reyes N, Marquez-Ortiz RA et al (2017) Emergence and spread of a new community-genotype methicillin-resistant Staphylococcus aureus clone in Colombia. BMC Infect Dis 17(1):108

    Article  Google Scholar 

  43. Reyes J, Rincon S, Diaz L et al (2009) Dissemination of methicillin-resistant Staphylococcus aureus USA300 sequence type 8 lineage in Latin America. Clin Infect Dis 49(12):1861–1867

    Article  CAS  Google Scholar 

  44. Escobar JA, Marquez-Ortiz RA, Alvarez-Olmos MI et al (2013) Detection of a new community genotype methicillin-resistant Staphylococcus aureus clone that is unrelated to the USA300 clone and that causes pediatric infections in Colombia. J Clin Microbiol 51(2):661–664

    Article  Google Scholar 

Download references

Acknowledgements

We thank Raf De Ryck, Pascal Buidin, Geneviève Hay, Nathalie Legros and Christine Thiroux for technical assistance. We thank our microbiologist colleagues for sending their staphylococcal strains to the NRC and the technicians of the service Transversal activities in Applied Genomics at Sciensano for performing the WGS.

Funding

This work was supported by the LHUB-ULB (no. project 485951501).

Author information

Authors and Affiliations

  1. Department of Microbiology, Laboratoire Hospitalier Universitaire de Bruxelles (LHUB-ULB), CNR Staphylocoques, Route de Lennik 808, 1070, Brussels, Belgium

    Maria A. Argudín, Ariane Deplano, Claire Nonhoff, Nicolas Yin, Charlotte Michel, Delphine Martiny & Marie Hallin

  2. Current address: Molecular Biology Laboratory, Tour R. Franklin, Cliniques Universitaires Saint Luc UCL, Brussels, Belgium

    Maria A. Argudín

  3. Transversal activities in Applied Genomics, Sciensano, Brussels, Belgium

    Sigrid C. J. De Keersmaecker

Authors
  1. Maria A. Argudín
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ariane Deplano
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Claire Nonhoff
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nicolas Yin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Charlotte Michel
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Delphine Martiny
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sigrid C. J. De Keersmaecker
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Marie Hallin
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MAA conceived the idea and analyzed the epidemiological and NGS data. MAA, AD, CN, NY, CM, DM and MH work(ed) at the Belgian National Reference Centre of Staphylococci and therefore contributed in the generation and validation of the epidemiological data. SCJDK obtained the NGS data. MAA wrote the manuscript in consultation with MH with input from the remaining authors.

Corresponding author

Correspondence to Maria A. Argudín.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Table S1-S4.

PCR, antimicrobial resistance and CGE results of the CC8 PVL-positive isolates recovered at the NRLS. Table S2. PCR, antimicrobial resistance and CGE results of the Belgian CC8 PVL-negative isolates used as outgroup. Table S3. Global ST8 collection used in the wgSNPs analysis. Table S4. Genes and regions investigated by using MyDbFinder (CGE). (XLSX 141 kb)

Figure S1.

Minimum spanning tree of CC8 Belgian isolates (n=138) based on 4546 wgSNPs. The genome of the USA300-NA TCH1516 (accession number: NC_010079) strain (in red) was used as reference genome. (PPTX 167 kb)

Figure S2.

Heatmap [clustering method: complete linkage, distance measurement method: Pearson correlation coefficient (between 0 and 1)] of presence/absence of genes by isolate. Genes and region used in the classification of isolates (SCCmec, ACME, COMER), as well as genes present in all isolates investigated by WGS were omitted. Black colour indicates presence of gene(s). FQR-NA, fluoroquinolone resistant USA300-NA isolates; FQS-NA; fluoroquinolone susceptible USA300-NA isolates; NA-AN, USA300-NA ACME-negative; LV, USA300-LV isolates; ST8-IVb, ST8 SCCmec IVb isolates; ST923, ST923 SCCmec IVa isolates. (PPTX 396 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Argudín, M.A., Deplano, A., Nonhoff, C. et al. Epidemiology of the Staphylococcus aureus CA-MRSA USA300 in Belgium. Eur J Clin Microbiol Infect Dis 40, 2335–2347 (2021). https://doi.org/10.1007/s10096-021-04286-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10096-021-04286-3

Keywords

Search

Navigation