1887
Research article Open Access
Like 0

Abstract

Background

Remarkably high carriage prevalence of a community-associated meticillin-resistant (MRSA) strain of sequence type (ST) 22 in the Gaza strip was reported in 2012. This strain is linked to the pandemic hospital-associated EMRSA-15. The origin and evolutionary history of ST22 in Gaza communities and the genomic elements contributing to its widespread predominance are unknown. We generated high-quality draft genomes of 61 ST22 isolates from Gaza communities and, along with 175 ST22 genomes from global sources, reconstructed the ST22 phylogeny and examined genotypes unique to the Gaza isolates. The Gaza isolates do not exhibit a close relationship with hospital-associated ST22 isolates, but rather with a basal population from which EMRSA-15 emerged. There were two separate resistance acquisitions by the same MSSA lineage, followed by diversification of other genetic determinants. Nearly all isolates in the two distinct clades, one characterised by staphylococcal cassette chromosome (SCC IVa and the other by SCC V and MSSA isolates, contain the toxic shock syndrome toxin-1 gene. The genomic diversity of Gaza ST22 isolates is not consistent with recent emergence in the region. The results indicate that two divergent Gaza clones evolved separately from susceptible isolates. Researchers should not assume that isolates identified as ST22 in the community are examples of EMRSA-15 that have escaped their healthcare roots. Future surveillance of MRSA is essential to the understanding of ST22 evolutionary dynamics and to aid efforts to slow the further spread of this lineage.

Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2018.23.34.1700592
2018-08-23
2019-06-20
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2018.23.34.1700592
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/23/34/eurosurv-23-34-2.html?itemId=/content/10.2807/1560-7917.ES.2018.23.34.1700592&mimeType=html&fmt=ahah

References

  1. Chambers HF, Deleo FR. Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat Rev Microbiol. 2009;7(9):629-41.  https://doi.org/10.1038/nrmicro2200  PMID: 19680247 
  2. Centers for Disease Control and Prevention (CDC). Four pediatric deaths from community-acquired methicillin-resistant Staphylococcus aureus — Minnesota and North Dakota, 1997-1999. MMWR Morb Mortal Wkly Rep. 1999;48(32):707-10. PMID: 21033181 
  3. Biber A, Abuelaish I, Rahav G, Raz M, Cohen L, Valinsky L, et al. PICR Study Group. A typical hospital-acquired methicillin-resistant Staphylococcus aureus clone is widespread in the community in the Gaza strip. PLoS One. 2012;7(8):e42864.  https://doi.org/10.1371/journal.pone.0042864  PMID: 22916171 
  4. Salgado CD, Farr BM, Calfee DP. Community-acquired methicillin-resistant Staphylococcus aureus: a meta-analysis of prevalence and risk factors. Clin Infect Dis. 2003;36(2):131-9.  https://doi.org/10.1086/345436  PMID: 12522744 
  5. Regev-Yochay G, Carmeli Y, Raz M, Pinco E, Etienne J, Leavitt A, et al. Prevalence and genetic relatedness of community-acquired methicillin-resistant Staphylococcus aureus in Israel. Eur J Clin Microbiol Infect Dis. 2006;25(11):719-22.  https://doi.org/10.1007/s10096-006-0210-3  PMID: 17043835 
  6. Holden MTG, Hsu L-Y, Kurt K, Weinert LA, Mather AE, Harris SR, et al. A genomic portrait of the emergence, evolution, and global spread of a methicillin-resistant Staphylococcus aureus pandemic. Genome Res. 2013;23(4):653-64.  https://doi.org/10.1101/gr.147710.112  PMID: 23299977 
  7. Inouye M, Dashnow H, Raven L-A, Schultz MB, Pope BJ, Tomita T, et al. SRST2: Rapid genomic surveillance for public health and hospital microbiology labs. Genome Med. 2014;6(11):90.  https://doi.org/10.1186/s13073-014-0090-6  PMID: 25422674 
  8. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014;30(14):2068-9.  https://doi.org/10.1093/bioinformatics/btu153  PMID: 24642063 
  9. 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(22):3691-3.  https://doi.org/10.1093/bioinformatics/btv421  PMID: 26198102 
  10. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. 1000 Genome Project Data Processing Subgroup. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25(16):2078-9.  https://doi.org/10.1093/bioinformatics/btp352  PMID: 19505943 
  11. Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, et al. 1000 Genomes Project Analysis Group. The variant call format and VCFtools. Bioinformatics. 2011;27(15):2156-8.  https://doi.org/10.1093/bioinformatics/btr330  PMID: 21653522 
  12. Croucher NJ, Page AJ, Connor TR, Delaney AJ, Keane JA, Bentley SD, et al. Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res. 2015;43(3):e15.  https://doi.org/10.1093/nar/gku1196  PMID: 25414349 
  13. 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(1):212-20.  https://doi.org/10.1128/AAC.01310-13  PMID: 24145532 
  14. Chen L, Xiong Z, Sun L, Yang J, Jin Q. VFDB 2012 update: toward the genetic diversity and molecular evolution of bacterial virulence factors. Nucleic Acids Res. 2012;40(Database issue)D641-645.  https://doi.org/10.1093/nar/gkr989  PMID: 22067448 
  15. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30(9):1312-3.  https://doi.org/10.1093/bioinformatics/btu033  PMID: 24451623 
  16. Rambaut A, Lam TT, Max Carvalho L, Pybus OG. Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen). Virus Evol. 2016;2(1):vew007.  https://doi.org/10.1093/ve/vew007  PMID: 27774300 
  17. Drummond AJ, Suchard MA, Xie D, Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol. 2012;29(8):1969-73.  https://doi.org/10.1093/molbev/mss075  PMID: 22367748 
  18. Drummond AJ, Suchard MA, Xie D, Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol. 2012;29(8):1969-73.  https://doi.org/10.1093/molbev/mss075  PMID: 22367748 
  19. Sako T, Tsuchida N. Nucleotide sequence of the staphylokinase gene from Staphylococcus aureus. Nucleic Acids Res. 1983;11(22):7679-93.  https://doi.org/10.1093/nar/11.22.7679  PMID: 6359061 
  20. van Wamel WJB, Rooijakkers SHM, Ruyken M, van Kessel KPM, van Strijp JAG. The innate immune modulators staphylococcal complement inhibitor and chemotaxis inhibitory protein of Staphylococcus aureus are located on beta-hemolysin-converting bacteriophages. J Bacteriol. 2006;188(4):1310-5.  https://doi.org/10.1128/JB.188.4.1310-1315.2006  PMID: 16452413 
  21. Novick RP. Mobile genetic elements and bacterial toxinoses: the superantigen-encoding pathogenicity islands of Staphylococcus aureus. Plasmid. 2003;49(2):93-105.  https://doi.org/10.1016/S0147-619X(02)00157-9  PMID: 12726763 
  22. Marchese A, Gualco L, Maioli E, Debbia E. Molecular analysis and susceptibility patterns of meticillin-resistant Staphylococcus aureus (MRSA) strains circulating in the community in the Ligurian area, a northern region of Italy: emergence of USA300 and EMRSA-15 clones. Int J Antimicrob Agents. 2009;34(5):424-8.  https://doi.org/10.1016/j.ijantimicag.2009.06.016  PMID: 19651493 
  23. Conceição T, Diamantino F, Coelho C, de Lencastre H, Aires-de-Sousa M. Contamination of public buses with MRSA in Lisbon, Portugal: a possible transmission route of major MRSA clones within the community. PLoS One. 2013;8(11):e77812.  https://doi.org/10.1371/journal.pone.0077812  PMID: 24223124 
  24. Fridkin SK, Hageman JC, Morrison M, Sanza LT, Como-Sabetti K, Jernigan JA, et al. Active Bacterial Core Surveillance Program of the Emerging Infections Program Network. Methicillin-resistant Staphylococcus aureus disease in three communities. N Engl J Med. 2005;352(14):1436-44.  https://doi.org/10.1056/NEJMoa043252  PMID: 15814879 
  25. Roche FM, Downer R, Keane F, Speziale P, Park PW, Foster TJ. The N-terminal A domain of fibronectin-binding proteins A and B promotes adhesion of Staphylococcus aureus to elastin. J Biol Chem. 2004;279(37):38433-40.  https://doi.org/10.1074/jbc.M402122200  PMID: 15234962 
  26. Johnson AP. Methicillin-resistant Staphylococcus aureus: the European landscape. J Antimicrob Chemother. 2011;66(Suppl 4):iv43-8.  https://doi.org/10.1093/jac/dkr076  PMID: 21521706 
  27. Monecke S, Coombs G, Shore AC, Coleman DC, Akpaka P, Borg M, et al. A field guide to pandemic, epidemic and sporadic clones of methicillin-resistant Staphylococcus aureus. PLoS One. 2011;6(4):e17936.  https://doi.org/10.1371/journal.pone.0017936  PMID: 21494333 
  28. Geraci DM, Bonura C, Giuffrè M, Aleo A, Saporito L, Graziano G, et al. tst1-positive ST22-MRSA-IVa in healthy Italian preschool children. Infection. 2014;42(3):535-8.  https://doi.org/10.1007/s15010-013-0583-z  PMID: 24448875 
  29. Udo EE, Boswihi SS, Al-Sweih N. High prevalence of toxic shock syndrome toxin-producing epidemic methicillin-resistant Staphylococcus aureus 15 (EMRSA-15) strains in Kuwait hospitals. New Microbes New Infect. 2016;12:24-30.  https://doi.org/10.1016/j.nmni.2016.03.008  PMID: 27222714 
  30. Abou Shady HM, Bakr AEA, Hashad ME, Alzohairy MA. Staphylococcus aureus nasal carriage among outpatients attending primary health care centers: a comparative study of two cities in Saudi Arabia and Egypt. Braz J Infect Dis. 2015;19(1):68-76.  https://doi.org/10.1016/j.bjid.2014.09.005  PMID: 25523075 
  31. Al-Bakri AG, Al-Hadithi H, Kasabri V, Othman G, Kriegeskorte A, Becker K. The epidemiology and molecular characterization of methicillin-resistant staphylococci sampled from a healthy Jordanian population. Epidemiol Infect. 2013;141(11):2384-91.  https://doi.org/10.1017/S0950268813000010  PMID: 23340022 
  32. Al Laham N, Mediavilla JR, Chen L, Abdelateef N, Elamreen FA, Ginocchio CC, et al. MRSA clonal complex 22 strains harboring toxic shock syndrome toxin (TSST-1) are endemic in the primary hospital in Gaza, Palestine. PLoS One. 2015;10(3):e0120008. https://doi.org/10.1371/journal.pone.0120008  PMID: 25781188 
  33. Köser CU, Holden MTG, Ellington MJ, Cartwright EJP, Brown NM, Ogilvy-Stuart AL, et al. Rapid whole-genome sequencing for investigation of a neonatal MRSA outbreak. N Engl J Med. 2012;366(24):2267-75.  https://doi.org/10.1056/NEJMoa1109910  PMID: 22693998 
/content/10.2807/1560-7917.ES.2018.23.34.1700592
Loading

Data & Media loading...

Comment has been disabled for this content
Submit comment
Close
Comment moderation successfully completed
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error