High prevalence of hospital-associated methicillin-resistant Staphylococcus aureus in the community in Portugal: evidence for the blurring of community–hospital boundaries

  • A. Tavares
  • M. Miragaia
  • J. Rolo
  • C. Coelho
  • H. de Lencastre
  • CA-MRSA/MSSA working group
Article

Abstract

Methicillin-resistant Staphylococcus aureus (MRSA) is a leading cause of infection in the community (CA-MRSA), but in spite of its relevance, no data exist concerning its epidemiology in Portugal. In this study, we aimed to evaluate the prevalence, population structure, and origin of MRSA in the Portuguese community. A total of 527 isolates, both methicillin-susceptible S. aureus (MSSA) and MRSA, were collected from individuals with no healthcare-related risk factors attending 16 healthcare institutions in Portugal. Isolates were characterized for the presence of mecA, Panton–Valentine leukocidin (PVL), and arginine catabolic mobile element (ACME), and by staphylococcal cassette chromosome mec (SCCmec) typing, pulsed-field gel electrophoresis (PFGE), spa, and multilocus sequence typing (MLST). Susceptibility to a panel of 13 antibiotics was tested. Isolates relatedness was analyzed by goeBURST and BURP. We found a high frequency (21.6 %) of MRSA in the community. However, only 11.4 % of the isolates belonged to typical CA-MRSA epidemic clones (USA300, USA400, USA700, Southwest Pacific, European, and ST398). The remaining isolates, which constituted the great majority (88.6 %), belonged to hospital-associated MRSA (HA-MRSA) epidemic clones, namely, to the EMRSA-15 clone (77.2 %). PVL was rare and carried by 17 isolates only (five MRSA and 12 MSSA). In the whole collection, some MRSA and MSSA were highly related. The high frequency of MRSA in the community in Portugal seems to result mainly from dissemination from the hospital. They might also have emerged from an extant MSSA population, by SCCmec acquisition, or MRSA clonal introduction from abroad.

Notes

Acknowledgments

We are grateful to the healthcare institutions that participated in this project and to all the healthcare workers for their collaboration in the isolation of S. aureus isolates and completion of questionnaires. Moreover, we thank André Velez, Ons Bouchami, and Clara Fonseca for helping with the data introduction in a semantic web database kept at the Laboratory of Molecular Genetics, ITQB. Finally, we thank Stefano Ravaioli for the partial characterization of a subset of 47 isolates and Ons Bouchami for the MLST characterization of ten isolates.

Conflict of interest

The authors declare that they have no conflict of interest.

Financial disclosure

This work was funded by project ref. P-99911 from Fundação Calouste Gulbenkian and, additionally, by Fundação para a Ciência e Tecnologia (FCT) through grant ref. Pest-OE/EQB/LAO004/2011, Portugal. A. Tavares was supported by grant SFRH/BD/44220/2008 from FCT, Portugal; J. Rolo by fellowship 007/BI/2009 from project CONCORD-HEALTH-F3-2008-222718, European Commission, and SFRH/BD/72675/2010 from FCT; and C. Coelho by grant 060/BI-BTI/2011 from TROCAR HEALTH-F3-2008-223031, European Commission.

Author contributions

Conceived and designed the project/surveillance: HdL, MM. Provided isolates and data: CA-MRSA/MSSA working group. Performed experiments: AT, JR, CC. Analyzed the data: AT, MM. Wrote the paper: AT, MM. Manuscript revision: HdL, JR, CC, and CA-MRSA/MSSA working group.

CA-MRSA/MSSA working group:

Author contributions: isolation of S. aureus isolates and filling in of questionnaires; all authors had the opportunity to revise the manuscript before submission.
  1. 1.

    José Melo-Cristino, MD/PhD. Serviço de Patologia Clínica, Hospital de Santa Maria, Centro Hospitalar Lisboa Norte, Avenida Prof. Egas Moniz, 1649-035 Lisboa, Portugal; melo_cristino@fm.ul.pt

     
  2. 2.

    Luís M. Lito, MD. Serviço de Patologia Clínica, Hospital de Santa Maria, Centro Hospitalar Lisboa Norte, Avenida Prof. Egas Moniz, 1649-035 Lisboa, Portugal; lmlito@hsm.min-saude.pt

     
  3. 3.

    José Amorim, MD. Departamento de Análises Clínicas, Sector Microbiologia, Clínica Laboratorial Dr. Edgar Moniz, Rua Sousa Trepa 14, Santo Tirso, 4780-554 Porto, Portugal; coutoamorim14@gmail.com

     
  4. 4.

    Rui Campainha, MSc. Departamento de Análises Clínicas, Sector Microbiologia, Clínica Laboratorial Dr. Edgar Moniz, Rua Sousa Trepa 14, Santo Tirso, 4780-554 Porto, Portugal; ruicampainha@gmail.com

     
  5. 5.

    Alberta Faustino, MD. Serviço de Patologia Clínica, Hospital de Braga, Sete Fontes - S. Victor, Apartado 2056, 4701-901 Braga, Portugal; albertafaustino@gmail.com

     
  6. 6.

    Maria Luísa Gonçalves, MD. Laboratório de Microbiologia, Unidade de Patologia Clínica, Hospital SAMS, Rua Cidade de Gabela, nº 1, 1849-017 Lisboa, Portugal; marialuisa.goncalves@sams.sbsi.pt

     
  7. 7.

    Augusto Machado e Costa, MD. Departamento de Medicina, Hospital SAMS, Rua Cidade de Gabela, nº 1, 1849-017 Lisboa, Portugal; augusto.costa@sams.sbsi.pt

     
  8. 8.

    Filomena Martins, MD. Laboratório de Microbiologia, Hospital de São Francisco Xavier, Centro Hospitalar Lisboa Ocidental, Estrada do Forte do Alto do Duque, 1449-005 Lisboa, Portugal; filomenacmartins@gmail.com

     
  9. 9.

    Elsa Gonçalves, MD. Laboratório de Microbiologia, Hospital de São Francisco Xavier, Centro Hospitalar Lisboa Ocidental, Estrada do Forte do Alto do Duque, 1449-005 Lisboa, Portugal; elsa.a.goncalves@sapo.pt

     
  10. 10.

    Graça Ribeiro, MD. Laboratório de Microbiologia, Serviço de Patologia Clínica, Centro Hospitalar de Coimbra, Quinta dos Vales, São Martinho do Bispo, 3041-801 Coimbra, Portugal; gribeiro@huc.min-saude.pt

     
  11. 11.

    Luísa Boaventura, MD. Laboratório de Microbiologia, Serviço de Patologia Clínica, Centro Hospitalar e Universitário de Coimbra, Praceta Mota Pinto, 3000-075 Coimbra, Portugal; lboaventura@huc.min-saude.pt

     
  12. 12.

    Ana Fonseca, MD. Laboratório de Microbiologia, Serviço de Patologia Clínica, Centro Hospitalar de Cascais, Rua Dr. Francisco Avilez, Apartado 132, 2750-953 Cascais, Portugal; anabruschy@netcabo.pt

     
  13. 13.

    Mafalda Guimarães, MD. Laboratório de Microbiologia, Serviço de Patologia Clínica, Centro Hospitalar de Cascais, Rua Dr. Francisco Avilez, Apartado 132, 2750-953 Cascais, Portugal; guimaraesmafalda@gmail.com

     
  14. 14.

    João Mairos, MD. Serviço de Ginecologia, Hospital da Força Aérea, Complexo da Base do Lumiar, Azinhaga dos Ulmeiros, 1649-020 Lisboa, Portugal; joaomairos@sapo.pt

     
  15. 15.

    Sandra Francisco, MD. Serviço de Patologia Clínica, Hospital da Força Aérea, Complexo da Base do Lumiar, Azinhaga dos Ulmeiros, 1649-020 Lisboa, Portugal; sandrajmfrancisco@gmail.com

     
  16. 16.

    M. Augusta Guimarães, MD. Serviço de Microbiologia, Instituto Português de Oncologia do Porto, Rua Dr. António Bernardino de Almeida, 4200-072 Porto, Portugal; maguimaraes@ipoporto.min-saude.pt

     
  17. 17.

    Catarina Lameiras, MSc/PhD student. Serviço de Microbiologia, Instituto Português de Oncologia do Porto, Rua Dr. António Bernardino de Almeida, 4200-072 Porto, Portugal; lameirascatarina@yahoo.com

     
  18. 18.

    Manuela Ribeiro, MD. Laboratório de Microbiologia, Hospital de São João do Porto, Alameda Prof. Hernâni Monteiro, 4202-451 Porto, Portugal; maria.mribeiro@hsjoao.min-saude.pt

     
  19. 19.

    Lídia Branco, MD. Laboratório de Microbiologia, Hospital de São João do Porto, Alameda Prof. Hernâni Monteiro, 4202-451 Porto, Portugal; lidiabrancolb@gmail.com

     
  20. 20.

    Maria Teresa Azevedo Vaz, MD. Serviço de Patologia Clínica, Centro Hospitalar do Barlavento Algarvio, Sítio do Poço Seco, 8500-338 Portimão, Portugal; teresa.vaz@hbalgarvio.min-saude.pt

     
  21. 21.

    Marília Gião, MD. Serviço de Patologia Clínica, Centro Hospitalar do Barlavento Algarvio, Sítio do Poço Seco, 8500-338 Portimão, Portugal; laboratorio3@hbalgarvio.min-saude.pt

     
  22. 22.

    Paulo Paixão, MD/PhD. Laboratório de Patologia Clínica, Hospital da Luz, Avenida Lusíada, 100, 1500-650 Lisboa, Portugal; pjpaixao@hospitaldaluz.pt

     
  23. 23.

    Natália Marto, MD. Laboratório de Patologia Clínica, Hospital da Luz, Avenida Lusíada, 100, 1500-650 Lisboa, Portugal; nfmarto@hospitaldaluz.pt

     
  24. 24.

    Maria Antónia Read, MSc. Laboratório de Microbiologia, Hospital Pedro Hispano, Rua Dr. Eduardo Torres, 4450-114 Matosinhos, Portugal; Antonia.Read@ulsm.min-saude.pt

     
  25. 25.

    Maria João Soares, MD. Laboratório de Microbiologia, Hospital Pedro Hispano, Rua Dr. Eduardo Torres, 4450-114 Matosinhos, Portugal; Maria.Soares@ulsm.min-saude.pt

     
  26. 26.

    Filipa Carneiro, MSc. Laboratório de Microbiologia, Hospital Pedro Hispano, Rua Dr. Eduardo Torres, 4450-114 Matosinhos, Portugal; Filipa.Carneiro@ulsm.min-saude.pt

     
  27. 27.

    Teresa Sardinha, MSc. Laboratório de Microbiologia, Hospital Professor Doutor Fernando da Fonseca, IC 19 Venteira – Amadora, 2720-276 Amadora, Portugal; tmsardinha@sapo.pt

     
  28. 28.

    Luisa Sancho, MD. Laboratório de Microbiologia, Hospital Professor Doutor Fernando da Fonseca, IC 19 Venteira – Amadora, 2720-276 Amadora, Portugal; luisasancho6@gmail.com

     
  29. 29.

    Germano Sousa, MD. Laboratório de Microbiologia, Hospital Professor Doutor Fernando da Fonseca, IC 19 Venteira – Amadora, 2720-276 Amadora, Portugal; germanosousa@cm-lab.com

     
  30. 30.

    Paula Correia, MD. Serviço de Pediatria, Hospital Professor Doutor Fernando da Fonseca, IC 19 Venteira – Amadora, 2720-276 Amadora, Portugal; tirado.paula@gmail.com

     
  31. 31.

    Rosa M. Barros, MD. Laboratório de Microbiologia, Hospital D. Estefânia, Centro Hospitalar de Lisboa Central, Rua José A Serrano, 1140-199 Lisboa, Portugal; barros.rosamachado@gmail.com

     
  32. 32.

    Margarida Pinto, MD. Laboratório de Microbiologia, Hospital D. Estefânia, Centro Hospitalar de Lisboa Central, Rua José A Serrano, 1140-199 Lisboa, Portugal; margaridafeijopinto@gmail.com

     
  33. 33.

    Isabel Daniel, MD. Laboratório de Microbiologia, Hospital D. Estefânia, Centro Hospitalar de Lisboa Central, Rua José A Serrano, 1140-199 Lisboa, Portugal; isabeldani@gmail.com

     
  34. 34.

    Maria João Brito, MD. Unidade de Infecciologia - Área de Pediatria Médica. Hospital D. Estefânia, Centro Hospitalar de Lisboa Central, EPE Rua Jacinta Marto, 116-045 Lisboa, Portugal; joao.rochabrito@netcabo.pt

     
  35. 35.

    Gonçalo Cordeiro Ferreira, MD. Unidade de Infecciologia - Área de Pediatria Médica. Hospital D. Estefânia, Centro Hospitalar de Lisboa Central, EPE Rua Jacinta Marto, 116-045 Lisboa, Portugal; goncalo.cf@chlc.min-saude.pt

     
  36. 36.

    Catarina Gouveia, MD. Unidade de Infecciologia - Área de Pediatria Médica. Hospital D. Estefânia, Centro Hospitalar de Lisboa Central, EPE Rua Jacinta Marto, 116-045 Lisboa, Portugal; cmfgouveia@gmail.com

     
  37. 37.

    Ana Morais, MD. Laboratório de Microbiologia, ACES Oeiras - Centros de Saúde de Oeiras e Carnaxide, Avenida Salvador Allende, 2780-163 Oeiras, Portugal; ana.morais@csoeiras.min-saude.pt

     
  38. 38.

    Idalina Valadares, BSc. Laboratório de Microbiologia, ACES Oeiras - Centros de Saúde de Oeiras e Carnaxide, Avenida Salvador Allende, 2780-163 Oeiras, Portugal; maria.valadares@csoeiras.min-saude.pt

     

Supplementary material

10096_2013_1872_MOESM1_ESM.docx (78 kb)
ESM 1(DOCX 77 kb)

References

  1. 1.
    David MZ, Daum RS (2010) Community-associated methicillin-resistant Staphylococcus aureus: epidemiology and clinical consequences of an emerging epidemic. Clin Microbiol Rev 23:616–687PubMedCrossRefGoogle Scholar
  2. 2.
    Burlak C, Hammer CH, Robinson MA, Whitney AR, McGavin MJ, Kreiswirth BN et al (2007) Global analysis of community-associated methicillin-resistant Staphylococcus aureus exoproteins reveals molecules produced in vitro and during infection. Cell Microbiol 9:1172–1190PubMedCrossRefGoogle Scholar
  3. 3.
    Montgomery CP, Boyle-Vavra S, Adem PV, Lee JC, Husain AN, Clasen J et al (2008) Comparison of virulence in community-associated methicillin-resistant Staphylococcus aureus pulsotypes USA300 and USA400 in a rat model of pneumonia. J Infect Dis 198:561–570PubMedCrossRefGoogle Scholar
  4. 4.
    Wang R, Braughton KR, Kretschmer D, Bach TH, Queck SY, Li M et al (2007) Identification of novel cytolytic peptides as key virulence determinants for community-associated MRSA. Nat Med 13:1510–1514PubMedCrossRefGoogle Scholar
  5. 5.
    Watkins RR, David MZ, Salata RA (2012) Current concepts on the virulence mechanisms of meticillin-resistant Staphylococcus aureus. J Med Microbiol 61:1179–1193PubMedCrossRefGoogle Scholar
  6. 6.
    Udo EE, Pearman JW, Grubb WB (1993) Genetic analysis of community isolates of methicillin-resistant Staphylococcus aureus in Western Australia. J Hosp Infect 25:97–108PubMedCrossRefGoogle Scholar
  7. 7.
    Coombs GW, Nimmo GR, Bell JM, Huygens F, O’Brien FG, Malkowski MJ et al (2004) Genetic diversity among community methicillin-resistant Staphylococcus aureus strains causing outpatient infections in Australia. J Clin Microbiol 42:4735–4743PubMedCrossRefGoogle Scholar
  8. 8.
    Centers for Disease Control and Prevention (CDC) (1999) Four pediatric deaths from community-acquired methicillin-resistant Staphylococcus aureus—Minnesota and North Dakota, 1997–1999. JAMA 282:1123–1125CrossRefGoogle Scholar
  9. 9.
    Klevens RM, Morrison MA, Nadle J, Petit S, Gershman K, Ray S et al (2007) Invasive methicillin-resistant Staphylococcus aureus infections in the United States. JAMA 298:1763–1771PubMedCrossRefGoogle Scholar
  10. 10.
    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 41:2027–2032PubMedCrossRefGoogle Scholar
  11. 11.
    Armand-Lefevre L, Ruimy R, Andremont A (2005) Clonal comparison of Staphylococcus aureus isolates from healthy pig farmers, human controls, and pigs. Emerg Infect Dis 11:711–714PubMedCrossRefGoogle Scholar
  12. 12.
    van Cleef BA, Monnet DL, Voss A, Krziwanek K, Allerberger F, Struelens M et al (2011) Livestock-associated methicillin-resistant Staphylococcus aureus in humans, Europe. Emerg Infect Dis 17:502–505PubMedCrossRefGoogle Scholar
  13. 13.
    Fan J, Shu M, Zhang G, Zhou W, Jiang Y, Zhu Y et al (2009) Biogeography and virulence of Staphylococcus aureus. PLoS One 4:e6216PubMedCrossRefGoogle Scholar
  14. 14.
    Khanna T, Friendship R, Dewey C, Weese JS (2008) Methicillin resistant Staphylococcus aureus colonization in pigs and pig farmers. Vet Microbiol 128:298–303PubMedCrossRefGoogle Scholar
  15. 15.
    Mediavilla JR, Chen L, Mathema B, Kreiswirth BN (2012) Global epidemiology of community-associated methicillin resistant Staphylococcus aureus (CA-MRSA). Curr Opin Microbiol 15:588–595PubMedCrossRefGoogle Scholar
  16. 16.
    Nimmo GR (2012) USA300 abroad: global spread of a virulent strain of community-associated methicillin-resistant Staphylococcus aureus. Clin Microbiol Infect 18:725–734PubMedCrossRefGoogle Scholar
  17. 17.
    Rolo J, Miragaia M, Turlej-Rogacka A, Empel J, Bouchami O, Faria NA et al (2012) High genetic diversity among community-associated Staphylococcus aureus in Europe: results from a multicenter study. PLoS One 7:e34768PubMedCrossRefGoogle Scholar
  18. 18.
    Monecke S, Coombs G, Shore AC, Coleman DC, Akpaka P, Borg M et al (2011) A field guide to pandemic, epidemic and sporadic clones of methicillin-resistant Staphylococcus aureus. PLoS One 6:e17936PubMedCrossRefGoogle Scholar
  19. 19.
    Chua K, Laurent F, Coombs G, Grayson ML, Howden BP (2011) Antimicrobial resistance: not community-associated methicillin-resistant Staphylococcus aureus (CA-MRSA)! A clinician’s guide to community MRSA—its evolving antimicrobial resistance and implications for therapy. Clin Infect Dis 52:99–114PubMedCrossRefGoogle Scholar
  20. 20.
    Köck R, Becker K, Cookson B, van Gemert-Pijnen JE, Harbarth S, Kluytmans J et al (2010) Methicillin-resistant Staphylococcus aureus (MRSA): burden of disease and control challenges in Europe. Euro Surveill 15:19688PubMedGoogle Scholar
  21. 21.
    Moran GJ, Krishnadasan A, Gorwitz RJ, Fosheim GE, McDougal LK, Carey RB et al (2006) Methicillin-resistant S. aureus infections among patients in the emergency department. N Engl J Med 355:666–674PubMedCrossRefGoogle Scholar
  22. 22.
    Manzur A, Dominguez AM, Pujol M, González MP, Limon E, Hornero A et al (2008) Community-acquired methicillin-resistant Staphylococcus aureus infections: an emerging threat in Spain. Clin Microbiol Infect 14:377–380PubMedCrossRefGoogle Scholar
  23. 23.
    Larsen AR, Stegger M, Böcher S, Sørum M, Monnet DL, Skov RL (2009) Emergence and characterization of community-associated methicillin-resistant Staphyloccocus aureus infections in Denmark, 1999 to 2006. J Clin Microbiol 47:73–78PubMedCrossRefGoogle Scholar
  24. 24.
    Witte W, Strommenger B, Cuny C, Heuck D, Nuebel U (2007) Methicillin-resistant Staphylococcus aureus containing the Panton–Valentine leucocidin gene in Germany in 2005 and 2006. J Antimicrob Chemother 60:1258–1263PubMedCrossRefGoogle Scholar
  25. 25.
    Marchese A, Gualco L, Maioli E, Debbia E (2009) 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 34:424–428PubMedCrossRefGoogle Scholar
  26. 26.
    Aires-de-Sousa M, Correia B, de Lencastre H; Multilaboratory Project Collaborators (2008) Changing patterns in frequency of recovery of five methicillin-resistant Staphylococcus aureus clones in portuguese hospitals: surveillance over a 16-year period. J Clin Microbiol 46:2912–2917PubMedCrossRefGoogle Scholar
  27. 27.
    Tavares DA, Sá-Leão R, Miragaia M, de Lencastre H (2010) Large screening of CA-MRSA among Staphylococcus aureus colonizing healthy young children living in two areas (urban and rural) of Portugal. BMC Infect Dis 10:110PubMedCrossRefGoogle Scholar
  28. 28.
    Sá-Leão R, Sanches IS, Couto I, Alves CR, de Lencastre H (2001) Low prevalence of methicillin-resistant strains among Staphylococcus aureus colonizing young and healthy members of the community in Portugal. Microb Drug Resist 7:237–245PubMedCrossRefGoogle Scholar
  29. 29.
    Conceição T, Aires-de-Sousa M, Pona N, Brito MJ, Barradas C, Coelho R et al (2011) High prevalence of ST121 in community-associated methicillin-susceptible Staphylococcus aureus lineages responsible for skin and soft tissue infections in Portuguese children. Eur J Clin Microbiol Infect Dis 30:293–297PubMedCrossRefGoogle Scholar
  30. 30.
    Nazareth R, Gonçalves-Pereira J, Tavares A, Miragaia M, de Lencastre H, Silvestre J et al (2012) Community-associated methicillin-resistant Staphylococcus aureus infection in Portugal. Rev Port Pneumol 18:34–38PubMedCrossRefGoogle Scholar
  31. 31.
    Pomba C, Hasman H, Cavaco LM, da Fonseca JD, Aarestrup FM (2009) First description of meticillin-resistant Staphylococcus aureus (MRSA) CC30 and CC398 from swine in Portugal. Int J Antimicrob Agents 34:193–194PubMedCrossRefGoogle Scholar
  32. 32.
    The European Parliament and the Council of the European Union (1998) Decision No 2119/98/EC of the European Parliament and of the Council of 24 September 1998: setting up a network for the epidemiological surveillance and control of communicable diseases in the Community. Official J Eur Communities L 268/1. Available online at: http://eurlex.europa.eu/LexUriServ/LexUriServ.do?uri=CELEX:31998D2119:EN:HTML
  33. 33.
    The Commission of the European Communities (2000) Commission decision of 22 December 1999 on the communicable diseases to be progressively covered by the Community network under decision number 2119/98/EC of the European Parliament and of the Council. Official J Eur Communities L 28/50. Available online at: http://eurlex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2000:028:0050:0053:EN:PDF
  34. 34.
    Clinical and Laboratory Standards Institute (CLSI) (2009) Performance standards for antimicrobial susceptibility testing; Nineteenth informational supplement. CLSI document M100-S19. CLSI, Wayne, PAGoogle Scholar
  35. 35.
    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 46:2155–2161PubMedCrossRefGoogle Scholar
  36. 36.
    Lina G, Piémont Y, Godail-Gamot F, Bes M, Peter MO, Gauduchon V et al (1999) Involvement of Panton–Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clin Infect Dis 29:1128–1132PubMedCrossRefGoogle Scholar
  37. 37.
    Milheiriço C, Oliveira DC, de Lencastre H (2007) Update to the multiplex PCR strategy for assignment of mec element types in Staphylococcus aureus. Antimicrob Agents Chemother 51:3374–3377PubMedCrossRefGoogle Scholar
  38. 38.
    Okuma K, Iwakawa K, Turnidge JD, Grubb WB, Bell JM, O’Brien FG et al (2002) Dissemination of new methicillin-resistant Staphylococcus aureus clones in the community. J Clin Microbiol 40:4289–4294PubMedCrossRefGoogle Scholar
  39. 39.
    Oliveira DC, Milheiriço C, Vinga S, de Lencastre H (2006) Assessment of allelic variation in the ccrAB locus in methicillin-resistant Staphylococcus aureus clones. J Antimicrob Chemother 58:23–30PubMedCrossRefGoogle Scholar
  40. 40.
    Ito T, Ma XX, Takeuchi F, Okuma K, Yuzawa H, Hiramatsu K (2004) Novel type V staphylococcal cassette chromosome mec driven by a novel cassette chromosome recombinase, ccrC. Antimicrob Agents Chemother 48:2637–2651PubMedCrossRefGoogle Scholar
  41. 41.
    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 60:42–48PubMedCrossRefGoogle Scholar
  42. 42.
    Chung M, de Lencastre H, Matthews P, Tomasz A, Adamsson I, Aires de Sousa M et al (2000) Molecular typing of methicillin-resistant Staphylococcus aureus by pulsed-field gel electrophoresis: comparison of results obtained in a multilaboratory effort using identical protocols and MRSA strains. Microb Drug Resist 6:189–198PubMedCrossRefGoogle Scholar
  43. 43.
    Faria NA, Carrico JA, Oliveira DC, Ramirez M, de Lencastre H (2008) Analysis of typing methods for epidemiological surveillance of both methicillin-resistant and methicillin-susceptible Staphylococcus aureus strains. J Clin Microbiol 46:136–144PubMedCrossRefGoogle Scholar
  44. 44.
    Bens CC, Voss A, Klaassen CH (2006) Presence of a novel DNA methylation enzyme in methicillin-resistant Staphylococcus aureus isolates associated with pig farming leads to uninterpretable results in standard pulsed-field gel electrophoresis analysis. J Clin Microbiol 44:1875–1876PubMedCrossRefGoogle Scholar
  45. 45.
    Shopsin B, Gomez M, Montgomery SO, Smith DH, Waddington M, Dodge DE et al (1999) Evaluation of protein A gene polymorphic region DNA sequencing for typing of Staphylococcus aureus strains. J Clin Microbiol 37:3556–3563PubMedGoogle Scholar
  46. 46.
    Mellmann A, Weniger T, Berssenbrügge C, Rothgänger J, Sammeth M, Stoye J et al (2007) Based Upon Repeat Pattern (BURP): an algorithm to characterize the long-term evolution of Staphylococcus aureus populations based on spa polymorphisms. BMC Microbiol 7:98PubMedCrossRefGoogle Scholar
  47. 47.
    Enright MC, Day NP, 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 38:1008–1015PubMedGoogle Scholar
  48. 48.
    Diep BA, Stone GG, Basuino L, Graber CJ, Miller A, des Etages SA et al (2008) The arginine catabolic mobile element and staphylococcal chromosomal cassette mec linkage: convergence of virulence and resistance in the USA300 clone of methicillin-resistant Staphylococcus aureus. J Infect Dis 197:1523–1530PubMedCrossRefGoogle Scholar
  49. 49.
    Diep BA, Gill SR, Chang RF, Phan TH, Chen JH, Davidson MG et al (2006) Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus. Lancet 367:731–739PubMedCrossRefGoogle Scholar
  50. 50.
    Simpson EH (1949) Measurement of diversity. Nature 163:688CrossRefGoogle Scholar
  51. 51.
    Amorim ML, Vasconcelos C, Oliveira DC, Azevedo A, Calado E, Faria NA et al (2009) Epidemiology of methicillin-resistant Staphylococcus aureus (MRSA) nasal colonization among patients and healthcare workers in a Portuguese hospital: a pre-intervention study toward the control of MRSA. Microb Drug Resist 15:19–26PubMedCrossRefGoogle Scholar
  52. 52.
    Vourli S, Vagiakou H, Ganteris G, Orfanidou M, Polemis M, Vatopoulos A et al (2009) High rates of community-acquired, Panton–Valentine leukocidin (PVL)- positive methicillin-resistant S. aureus (MRSA) infections in adult outpatients in Greece. Euro Surveill 14. pii: 19089Google Scholar
  53. 53.
    Thibaut S, Caillon J, Huart C, Grandjean G, Lombrail P, Potel G et al (2010) Susceptibility to the main antibiotics of Escherichia coli and Staphylococcus aureus strains identified in community acquired infections in France (MedQual, 2004–2007). Med Mal Infect 40:74–80PubMedCrossRefGoogle Scholar
  54. 54.
    Daskalaki M, Rojo P, Marin-Ferrer M, Barrios M, Otero JR, Chaves F (2010) Panton–Valentine leukocidin-positive Staphylococcus aureus skin and soft tissue infections among children in an emergency department in Madrid, Spain. Clin Microbiol Infect 16:74–77PubMedCrossRefGoogle Scholar
  55. 55.
    Maugat S, de Rougemont A, Aubry-Damon H, Reverdy ME, Georges S, Vandenesch F et al (2009) Methicillin-resistant Staphylococcus aureus among a network of French private-sector community-based-medical laboratories. Med Mal Infect 39:311–318PubMedCrossRefGoogle Scholar
  56. 56.
    González-Domínguez M, Seral C, Sáenz Y, Salvo S, Gude MJ, Porres-Osante N et al (2012) Epidemiological features, resistance genes, and clones among community-onset methicillin-resistant Staphylococcus aureus (CO-MRSA) isolates detected in northern Spain. Int J Med Microbiol 302:320–326PubMedCrossRefGoogle Scholar
  57. 57.
    Horner C, Parnell P, Hall D, Kearns A, Heritage J, Wilcox M (2013) Meticillin-resistant Staphylococcus aureus in elderly residents of care homes: colonization rates and molecular epidemiology. J Hosp Infect 83:212–218PubMedCrossRefGoogle Scholar
  58. 58.
    Shore AC, Rossney AS, Brennan OM, Kinnevey PM, Humphreys H, Sullivan DJ et al (2011) Characterization of a novel arginine catabolic mobile element (ACME) and staphylococcal chromosomal cassette mec composite island with significant homology to Staphylococcus epidermidis ACME type II in methicillin-resistant Staphylococcus aureus genotype ST22-MRSA-IV. Antimicrob Agents Chemother 55:1896–1905PubMedCrossRefGoogle Scholar
  59. 59.
    Richardson JF, Reith S (1993) Characterization of a strain of methicillin-resistant Staphylococcus aureus (EMRSA-15) by conventional and molecular methods. J Hosp Infect 25:45–52PubMedCrossRefGoogle Scholar
  60. 60.
    Johnson AP, Pearson A, Duckworth G (2005) Surveillance and epidemiology of MRSA bacteraemia in the UK. J Antimicrob Chemother 56:455–462PubMedCrossRefGoogle Scholar
  61. 61.
    Johnson AP, Aucken HM, Cavendish S, Ganner M, Wale MC, Warner M et al (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 48:143–144PubMedCrossRefGoogle Scholar
  62. 62.
    Pearman JW, Coombs GW, Grubb WB, O’Brien F (2001) A British epidemic strain of methicillin-resistant Staphylococcus aureus (UK EMRSA-15) in Western Australia. Med J Aust 174:662PubMedGoogle Scholar
  63. 63.
    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 290:677–682PubMedCrossRefGoogle Scholar
  64. 64.
    Hsu LY, Koh TH, Singh K, Kang ML, Kurup A, Tan BH (2005) Dissemination of multisusceptible methicillin-resistant Staphylococcus aureus in Singapore. J Clin Microbiol 43:2923–2925PubMedCrossRefGoogle Scholar
  65. 65.
    Melter O, Urbásková P, Jakubů V, Macková B, Zemlicková H; Czech participants in EARSS (2006) Emergence of EMRSA-15 clone in hospitals throughout the Czech Republic. Euro Surveill 11:E060803.6PubMedGoogle Scholar
  66. 66.
    Amorim ML, Faria NA, Oliveira DC, Vasconcelos C, Cabeda JC, Mendes AC et al (2007) Changes in the clonal nature and antibiotic resistance profiles of methicillin-resistant Staphylococcus aureus isolates associated with spread of the EMRSA-15 clone in a tertiary care Portuguese hospital. J Clin Microbiol 45:2881–2888PubMedCrossRefGoogle Scholar
  67. 67.
    Faria NA, Oliveira DC, Westh H, Monnet DL, Larsen AR, Skov R et al (2005) Epidemiology of emerging methicillin-resistant Staphylococcus aureus (MRSA) in Denmark: a nationwide study in a country with low prevalence of MRSA infection. J Clin Microbiol 43:1836–1842PubMedCrossRefGoogle Scholar
  68. 68.
    Gosbell IB, Barbagiannakos T, Neville SA, Mercer JL, Vickery AM, O’Brien FG et al (2006) Non-multiresistant methicillin-resistant Staphylococcus aureus bacteraemia in Sydney, Australia: emergence of EMRSA-15, Oceania, Queensland and Western Australian MRSA strains. Pathology 38:239–244PubMedCrossRefGoogle Scholar
  69. 69.
    Pérez-Roth E, Lorenzo-Díaz F, Batista N, Moreno A, Méndez-Alvarez S (2004) Tracking methicillin-resistant Staphylococcus aureus clones during a 5-year period (1998 to 2002) in a Spanish hospital. J Clin Microbiol 42:4649–4656PubMedCrossRefGoogle Scholar
  70. 70.
    Coelho C, Torres C, Radhouani H, Pinto L, Lozano C, Gómez-Sanz E et al (2011) Molecular detection and characterization of methicillin-resistant Staphylococcus aureus (MRSA) isolates from dogs in Portugal. Microb Drug Resist 17:333–337PubMedCrossRefGoogle Scholar
  71. 71.
    Simões RR, Aires-de-Sousa M, Conceição T, Antunes F, da Costa PM, de Lencastre H (2011) High prevalence of EMRSA-15 in Portuguese public buses: a worrisome finding. PLoS One 6:e17630PubMedCrossRefGoogle Scholar
  72. 72.
    Holden MT, Hsu LY, Kurt K, Weinert LA, Mather AE, Harris SR et al (2013) A genomic portrait of the emergence, evolution, and global spread of a methicillin-resistant Staphylococcus aureus pandemic. Genome Res. [Epub ahead of print]Google Scholar
  73. 73.
    Horváth A, Dobay O, Kardos S, Ghidán Á, Tóth Á, Pászti J et al (2012) Varying fitness cost associated with resistance to fluoroquinolones governs clonal dynamic of methicillin-resistant Staphylococcus aureus. Eur J Clin Microbiol Infect Dis 31:2029–2036PubMedCrossRefGoogle Scholar
  74. 74.
    European Surveillance of Antimicrobial Consumption (ESAC) (2010) ESAC Yearbook 2008—ESAC document prepared by the ESAC Management Team, the ESAC Scientific Advisory Board and the ESAC National Networks. University of Antwerp. Home page at: http://www.esac.ua.ac.be
  75. 75.
    Relatório Inquérito de Prevalência de Infeção (2010) Programa Nacional de Prevenção e Controlo da Infeção Associada aos Cuidados de Saúde. Departamento da Qualidade na Saúde. Direcção Geral da Saúde. Home page at: http://www.dgs.pt/
  76. 76.
    Parienti JJ, Cattoir V, Thibon P, Lebouvier G, Verdon R, Daubin C et al (2011) Hospital-wide modification of fluoroquinolone policy and meticillin-resistant Staphylococcus aureus rates: a 10-year interrupted time-series analysis. J Hosp Infect 78:118–122PubMedCrossRefGoogle Scholar
  77. 77.
    Lafaurie M, Porcher R, Donay JL, Touratier S, Molina JM (2012) Reduction of fluoroquinolone use is associated with a decrease in methicillin-resistant Staphylococcus aureus and fluoroquinolone-resistant Pseudomonas aeruginosa isolation rates: a 10 year study. J Antimicrob Chemother 67:1010–1015PubMedCrossRefGoogle Scholar
  78. 78.
    Ito T, Katayama Y, Hiramatsu K (1999) Cloning and nucleotide sequence determination of the entire mec DNA of pre-methicillin-resistant Staphylococcus aureus N315. Antimicrob Agents Chemother 43:1449–1458PubMedGoogle Scholar
  79. 79.
    Hedlund L, Hellmark B, Söderquist B (2013) Presence of arginine catabolic mobile element among community-acquired meticillin-resistant Staphylococcus aureus is linked to a specific genetic background. APMIS 121:221–225PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • A. Tavares
    • 1
  • M. Miragaia
    • 1
  • J. Rolo
    • 1
  • C. Coelho
    • 1
  • H. de Lencastre
    • 1
    • 2
  • CA-MRSA/MSSA working group
  1. 1.Laboratory of Molecular GeneticsInstituto de Tecnologia Química e Biológica (ITQB)OeirasPortugal
  2. 2.Laboratory of MicrobiologyThe Rockefeller UniversityNew YorkUSA

Personalised recommendations