Skip to main content

Advertisement

SpringerLink
Log in

Characterisation of MRSA from Malta and the description of a Maltese epidemic MRSA strain

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

Abstract

Malta has one of the highest prevalence rates of methicillin-resistant Staphylococcus aureus (MRSA) in Europe. However, only limited typing data are currently available. In order to address this situation, 45 MRSA isolates from the Mater Dei Hospital in Msida, Malta, were characterised using DNA microarrays. The most common strain was ST22-MRSA-IV (UK-EMRSA-15, 30 isolates). Sporadic strains included ST36-MRSA-II (UK-EMRSA-16, two isolates), PVL-positive ST80-MRSA-IV (European Clone, one isolate), ST228-MRSA-I (Italian Clone/South German Epidemic Strain, one isolate) and ST239-MRSA-III (Vienna/Hungarian/Brazilian Epidemic Strain, one isolate). Ten MRSA isolates belonged to a clonal complex (CC) 5/ST149, spa type t002 strain. This strain harboured an SCCmec IV element (mecA, delta mecR, ugpQ, dcs, ccrA2 and ccrB2), as well as novel alleles of ccrA/B and the fusidic acid resistance element Q6GD50 (previously described in the sequenced strain MSSA476, BX571857.1:SAS0043). It also carried the gene for enterotoxin A (sea) and the egc enterotoxin locus, as well as (in nine out of ten isolates) genes encoding the toxic shock syndrome toxin (tst1) and enterotoxins C and L (sec, sel). While the presence of the other MRSA strains suggests foreign importation due to travel between Malta and other European countries, the CC5/t002 strain appears, so far, to be restricted to Malta.

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

Similar content being viewed by others

References

  1. Monecke S, Jatzwauk L, Weber S, Slickers P, Ehricht R (2008) DNA microarray-based genotyping of methicillin-resistant Staphylococcus aureus strains from Eastern Saxony. Clin Microbiol Infect 14:534–545

    Article  CAS  PubMed  Google Scholar 

  2. Mato R, Campanile F, Stefani S, Crisóstomo MI, Santagati M, Sanches SI, de Lencastre H (2004) Clonal types and multidrug resistance patterns of methicillin-resistant Staphylococcus aureus (MRSA) recovered in Italy during the 1990s. Microb Drug Resist 10:106–113

    Article  CAS  PubMed  Google Scholar 

  3. Aires de Sousa M, Bartzavali C, Spiliopoulou I, Sanches IS, Crisóstomo MI, de Lencastre H (2003) Two international methicillin-resistant Staphylococcus aureus clones endemic in a university hospital in Patras, Greece. J Clin Microbiol 41:2027–2032

    Article  CAS  PubMed  Google Scholar 

  4. Cuevas O, Cercenado E, Bouza E, Castellares C, Trincado P, Cabrera R, Vindel A (2007) Molecular epidemiology of methicillin-resistant Staphylococcus aureus in Spain: a multicentre prevalence study (2002). Clin Microbiol Infect 13:250–256

    Article  CAS  PubMed  Google Scholar 

  5. Alcoceba E, Mena A, Cruz Pérez M, Ruiz de Gopegui E, Padilla E, Gil J, Ramírez A, Gallegos C, Serra A, Pérez JL, Oliver A (2007) Molecular epidemiology of methicillin-resistant Staphylococcus aureus in Majorcan hospitals: high prevalence of the epidemic clone EMRSA-15. Clin Microbiol Infect 13:599–605

    Article  CAS  PubMed  Google Scholar 

  6. Vourli S, Perimeni D, Makri A, Polemis M, Voyiatzi A, Vatopoulos A (2005) Community acquired MRSA infections in a paediatric population in Greece. Euro Surveill 10:78–79

    CAS  PubMed  Google Scholar 

  7. Chini V, Petinaki E, Foka A, Paratiras S, Dimitracopoulos G, Spiliopoulou I (2006) Spread of Staphylococcus aureus clinical isolates carrying Panton-Valentine leukocidin genes during a 3-year period in Greece. Clin Microbiol Infect 12:29–34

    Article  CAS  PubMed  Google Scholar 

  8. Pérez-Vázquez M, Vindel A, Marcos C, Oteo J, Cuevas O, Trincado P, Bautista V, Grundmann H, Campos J (2009) Spread of invasive Spanish Staphylococcus aureus spa-type t067 associated with a high prevalence of the aminoglycoside-modifying enzyme gene ant(4′)-Ia and the efflux pump genes msrA/msrB. J Antimicrob Chemother 63:21–31

    Article  PubMed  Google Scholar 

  9. Gould SW, Rollason J, Hilton AC, Cuschieri P, McAuliffe L, Easmon SL, Fielder MD (2008) UK epidemic strains of meticillin-resistant Staphylococcus aureus in clinical samples from Malta. J Med Microbiol 57:1394–1398

    Article  CAS  PubMed  Google Scholar 

  10. Monecke S, Slickers P, Ehricht R (2008) Assignment of Staphylococcus aureus isolates to clonal complexes based on microarray analysis and pattern recognition. FEMS Immunol Med Microbiol 53:237–251

    Article  CAS  PubMed  Google Scholar 

  11. Monecke S, Slickers P, Hotzel H, Richter-Huhn G, Pohle M, Weber S, Witte W, Ehricht R (2006) Microarray-based characterisation of a Panton-Valentine leukocidin-positive community-acquired strain of methicillin-resistant Staphylococcus aureus. Clin Microbiol Infect 12:718–728

    CAS  PubMed  Google Scholar 

  12. Monecke S, Ehricht R, Slickers P, Wiese N, Jonas D (2009) Intra-strain variability of methicillin-resistant Staphylococcus aureus strains ST228-MRSA-I and ST5-MRSA-II. Eur J Clin Microbiol Infect Dis (in press)

  13. Monecke S, Berger-Bächi B, Coombs G, Holmes A, Kay I, Kearns A, Linde HJ, O’Brien F, Slickers P, Ehricht R (2007) Comparative genomics and DNA array-based genotyping of pandemic Staphylococcus aureus strains encoding Panton-Valentine leukocidin. Clin Microbiol Infect 13:236–249

    Article  CAS  PubMed  Google Scholar 

  14. Kondo Y, Ito T, Ma XX, Watanabe S, Kreiswirth BN, Etienne J, Hiramatsu K (2007) Combination of multiplex PCRs for staphylococcal cassette chromosome mec type assignment: rapid identification system for mec, ccr, and major differences in junkyard regions. Antimicrob Agents Chemother 51:264–274

    Article  CAS  PubMed  Google Scholar 

  15. Oliveira DC, de Lencastre H (2002) Multiplex PCR strategy for rapid identification of structural types and variants of the mec element in methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 46:2155–2161

    Article  CAS  PubMed  Google Scholar 

  16. Milheiriço C, Oliveira DC, de Lencastre H (2007) Multiplex PCR strategy for subtyping the staphylococcal cassette chromosome mec type IV in methicillin-resistant Staphylococcus aureus: ‘SCCmec IV multiplex’. J Antimicrob Chemother 60:42–48

    Article  PubMed  Google Scholar 

  17. Shore AC, Rossney AS, O’Connell B, Herra CM, Sullivan DJ, Humphreys H, Coleman DC (2008) Detection of staphylococcal cassette chromosome mec-associated DNA segments in multiresistant methicillin-susceptible Staphylococcus aureus (MSSA) and identification of Staphylococcus epidermidis ccrAB4 in both methicillin-resistant S. aureus and MSSA. Antimicrob Agents Chemother 52:4407–4419

    Article  CAS  PubMed  Google Scholar 

  18. Ma XX, Ito T, Tiensasitorn C, Jamklang M, Chongtrakool P, Boyle-Vavra S, Daum RS, Hiramatsu K (2002) Novel type of staphylococcal cassette chromosome mec identified in community-acquired methicillin-resistant Staphylococcus aureus strains. Antimicrob Agents Chemother 46:1147–1152

    Article  CAS  PubMed  Google Scholar 

  19. Ma XX, Ito T, Chongtrakool P, Hiramatsu K (2006) Predominance of clones carrying Panton-Valentine leukocidin genes among methicillin-resistant Staphylococcus aureus strains isolated in Japanese hospitals from 1979 to 1985. J Clin Microbiol 44:4515–4527

    Article  CAS  PubMed  Google Scholar 

  20. Enright MC, Day NPJ, Davies CE, Peacock SJ, Spratt BG (2000) Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J Clin Microbiol 38:1008–1015

    CAS  PubMed  Google Scholar 

  21. Witte W, Enright M, Schmitz FJ, Cuny C, Braulke C, Heuck D (2001) Characteristics of a new epidemic MRSA in Germany ancestral to United Kingdom EMRSA 15. Int J Med Microbiol 290:677–682

    CAS  PubMed  Google Scholar 

  22. Holden MTG, Feil EJ, Lindsay JA, Peacock SJ, Day NPJ, Enright MC, Foster TJ, Moore CE, Hurst L, Atkin R, Barron A, Bason N, Bentley SD, Chillingworth C, Chillingworth T, Churcher C, Clark L, Corton C, Cronin A, Doggett J, Dowd L, Feltwell T, Hance Z, Harris B, Hauser H, Holroyd S, Jagels K, James KD, Lennard N, Line A, Mayes R, Moule S, Mungall K, Ormond D, Quail MA, Rabbinowitsch E, Rutherford K, Sanders M, Sharp S, Simmonds M, Stevens K, Whitehead S, Barrell BG, Spratt BG, Parkhill J (2004) Complete genomes of two clinical Staphylococcus aureus strains: evidence for the rapid evolution of virulence and drug resistance. Proc Natl Acad Sci USA 101:9786–9791

    Article  CAS  PubMed  Google Scholar 

  23. Coleman DC, Sullivan DJ, Russell RJ, Arbuthnott JP, Carey BF, Pomeroy HM (1989) Staphylococcus aureus bacteriophages mediating the simultaneous lysogenic conversion of beta-lysin, staphylokinase and enterotoxin A: molecular mechanism of triple conversion. J Gen Microbiol 135:1679–1697

    CAS  PubMed  Google Scholar 

  24. van Wamel WJB, Rooijakkers SHM, Ruyken M, van Kessel KPM, van Strijp JAG (2006) The innate immune modulators staphylococcal complement inhibitor and chemotaxis inhibitory protein of Staphylococcus aureus are located on beta-hemolysin-converting bacteriophages. J Bacteriol 188:1310–1315

    Article  PubMed  Google Scholar 

  25. Robinson DA, Enright MC (2004) Evolution of Staphylococcus aureus by large chromosomal replacements. J Bacteriol 186:1060–1064

    Article  CAS  PubMed  Google Scholar 

  26. Kuroda M, Ohta T, Uchiyama I, Baba T, Yuzawa H, Kobayashi I, Cui L, Oguchi A, Aoki K, Nagai Y, Lian J, Ito T, Kanamori M, Matsumaru H, Maruyama A, Murakami H, Hosoyama A, Mizutani-Ui Y, Takahashi NK, Sawano T, Inoue R, Kaito C, Sekimizu K, Hirakawa H, Kuhara S, Goto S, Yabuzaki J, Kanehisa M, Yamashita A, Oshima K, Furuya K, Yoshino C, Shiba T, Hattori M, Ogasawara N, Hayashi H, Hiramatsu K (2001) Whole genome sequencing of meticillin-resistant Staphylococcus aureus. Lancet 357:1225–1240

    Article  CAS  PubMed  Google Scholar 

  27. Pi B, Yu M, Chen Y, Yu Y, Li L (2009) Distribution of the ACME-arcA gene among meticillin-resistant Staphylococcus haemolyticus and identification of a novel ccr allotype in ACME-arcA-positive isolates. J Med Microbiol 58:731–736

    Article  CAS  PubMed  Google Scholar 

  28. Grinberg A, Kingsbury DD, Gibson IR, Kirby BM, Mack HJ, Morrison D (2008) Clinically overt infections with methicillin-resistant Staphylococcus aureus in animals in New Zealand: a pilot study. N Z Vet J 56:237–242

    CAS  PubMed  Google Scholar 

  29. Walther B, Monecke S, Ruscher C, Friedrich AW, Ehricht R, Slickers P, Soba A, Wleklinski CG, Wieler LH, Lübke-Becker A (2009) Comparative molecular analysis substantiates zoonotic potential of equine methicillin-resistant Staphylococcus aureus. J Clin Microbiol 47:704–710

    Article  PubMed  Google Scholar 

  30. Walther B, Wieler LH, Friedrich AW, Hanssen AM, Kohn B, Brunnberg L, Lübke-Becker A (2008) Methicillin-resistant Staphylococcus aureus (MRSA) isolated from small and exotic animals at a university hospital during routine microbiological examinations. Vet Microbiol 127:171–178

    Article  CAS  PubMed  Google Scholar 

  31. Johnson AP, Aucken HM, Cavendish S, Ganner M, Wale MC, Warner M, Livermore DM, Cookson BD (2001) Dominance of EMRSA-15 and -16 among MRSA causing nosocomial bacteraemia in the UK: analysis of isolates from the European Antimicrobial Resistance Surveillance System (EARSS). J Antimicrob Chemother 48:143–144

    Article  CAS  PubMed  Google Scholar 

  32. [No authors listed] (1993) EMRSA-16: a new epidemic strain of Staphylococcus aureus. Commun Dis Rep CDR Wkly 3:25

    Google Scholar 

  33. Larsen AR, Böcher S, Stegger M, Goering R, Pallesen LV, Skov R (2008) Epidemiology of European community-associated methicillin-resistant Staphylococcus aureus clonal complex 80 type IV strains isolated in Denmark from 1993 to 2004. J Clin Microbiol 46:62–68

    Article  CAS  PubMed  Google Scholar 

  34. Maier J, Melzl H, Reischl U, Drubel I, Witte W, Lehn N, Linde H (2005) Panton-Valentine leukocidin-positive methicillin-resistant Staphylococcus aureus in Germany associated with travel or foreign family origin. Eur J Clin Microbiol Infect Dis 24:637–639

    Article  CAS  PubMed  Google Scholar 

  35. Francois P, Harbarth S, Huyghe A, Renzi G, Bento M, Gervaix A, Pittet D, Schrenzel J (2008) Methicillin-resistant Staphylococcus aureus, Geneva, Switzerland, 1993–2005. Emerg Infect Dis 14:304–307

    Article  PubMed  Google Scholar 

  36. Dauwalder O, Lina G, Durand G, Bes M, Meugnier H, Jarlier V, Coignard B, Vandenesch F, Etienne J, Laurent F (2008) Epidemiology of invasive methicillin-resistant Staphylococcus aureus clones collected in France in 2006 and 2007. J Clin Microbiol 46:3454–3458

    Article  PubMed  Google Scholar 

  37. Durand G, Bes M, Meugnier H, Enright MC, Forey F, Liassine N, Wenger A, Kikuchi K, Lina G, Vandenesch F, Etienne J (2006) Detection of new methicillin-resistant Staphylococcus aureus clones containing the toxic shock syndrome toxin 1 gene responsible for hospital- and community-acquired infections in France. J Clin Microbiol 44:847–853

    Article  CAS  PubMed  Google Scholar 

  38. Shore A, Rossney AS, Keane CT, Enright MC, Coleman DC (2005) Seven novel variants of the staphylococcal chromosomal cassette mec in methicillin-resistant Staphylococcus aureus isolates from Ireland. Antimicrob Agents Chemother 49:2070–2083

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors want to thank Antje Ruppelt, Hanna Kanig (TU Dresden), Elke Müller, Ines Engelmann and Jana Sachtschal (CLONDIAG) for their excellent technical assistance, as well as Dr. Wolfram Rudolph for the sequencing. We acknowledge the staff of the Bacteriology Laboratory of Mater Dei Hospital and the Infection Control Unit of Mater Dei Hospital for providing the isolates. Staphylococcus aureus control isolates for SCCmec typing were kindly provided by Prof. Teruyo Ito, Juntendo University, Japan, Prof. Herminia de Lencastre, Rockefeller University, New York, USA, and Prof. Robert Daum, University of Chicago, USA. We acknowledge Prof. E. Jacobs for his support.

Ralf Ehricht and Peter Slickers are employees of CLONDIAG. The authors declare no other conflicting interests.

Author information

Authors and Affiliations

  1. Infection Control Unit, Mater Dei Hospital, Msida, Malta

    E. A. Scicluna & M. A. Borg

  2. Microbiology Research Unit, Dublin Dental School & Hospital, University of Dublin, Trinity College Dublin, Dublin, Ireland

    A. C. Shore & D. C. Coleman

  3. Institute for Medical Microbiology and Hygiene, Faculty of Medicine “Carl Gustav Carus”, Technical University of Dresden, Fetscherstrasse 74, 01307, Dresden, Germany

    A. Thürmer & S. Monecke

  4. CLONDIAG GmbH, Loebstedter Strasse 103–105, 07749, Jena, Germany

    R. Ehricht & P. Slickers

Authors
  1. E. A. Scicluna
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. C. Shore
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. Thürmer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. R. Ehricht
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. P. Slickers
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. M. A. Borg
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. D. C. Coleman
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. S. Monecke
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to S. Monecke.

Electronic supplementary material

Suppmentary 1

Patient data, results of susceptibility tests and hybridisation data for all isolates (PDF 152 kb)

Suppmentary 2

Alignment for the following sequences: EU934095.1, S. haemolyticus H9, ccrA/BSHP (1-3017); AM904731.1, S. pseudintermedius KM241, SCCmec (4627-7625); AB037671.1, S. aureus 85/2082, SCCmec III (5430-8425); ccrA/B MLT, the sequence described herein, consensus sequence of two isolates of the Maltese epidemic CC5-MRSA strain; hybridisation probe ccrA3_1 and labelling primer ccrA3_1; hybridisation probe ccrB3_1 and labelling primer ccrB3_1; PCR primers ccrA3F and ccrA3R; PCR primers ccrB3F and ccrB3R; and PCR primers fw_ccrA3 cons and rv_ccrB5_5p (reverse complement shown for labelling and reverse PCR primers) (PDF 20 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Scicluna, E.A., Shore, A.C., Thürmer, A. et al. Characterisation of MRSA from Malta and the description of a Maltese epidemic MRSA strain. Eur J Clin Microbiol Infect Dis 29, 163–170 (2010). https://doi.org/10.1007/s10096-009-0834-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10096-009-0834-1

Keywords

Search

Navigation