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

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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) ty**, pulsed-field gel electrophoresis (PFGE), spa, and multilocus sequence ty** (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.

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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 hel** 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

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    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

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    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

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    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

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    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

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    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

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

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

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

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

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

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

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

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    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

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    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

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    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

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    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

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    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

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    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

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Authors and Affiliations

  1. Laboratory of Molecular Genetics, Instituto de Tecnologia Química e Biológica (ITQB), Oeiras, Portugal

    A. Tavares, M. Miragaia, J. Rolo, C. Coelho & H. de Lencastre

  2. Laboratory of Microbiology, The Rockefeller University, 1230 York Ave., New York, NY, 10065, USA

    H. de Lencastre

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  1. A. Tavares
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  2. M. Miragaia
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Correspondence to H. de Lencastre.

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CA-MRSA/MSSA working group: José Melo-Cristino and Luís M. Lito, Serviço de Patologia Clínica, Centro Hospitalar Lisboa Norte, Lisboa, Portugal; José Amorim and Rui Campainha, Departamento de Análises Clínicas, Clínica Lab Dr Edgar Botelho Moniz, Santo Tirso, Portugal; Alberta Faustino, Serviço de Patologia Clínica, Hospital de Braga, Portugal; Maria Luísa Gonçalves and Augusto Machado e Costa, Laboratório de Microbiologia and Departamento de Medicina, Hospital SAMS, Lisboa, Portugal; Filomena Martins and Elsa Gonçalves, Laboratório de Microbiologia, Centro Hospitalar Lisboa Ocidental, Lisboa, Portugal; Graça Ribeiro and Luísa Boaventura, Laboratório de Microbiologia, Centro Hospitalar de Coimbra, Coimbra, Portugal; Ana Fonseca and Mafalda Guimarães, Laboratório de Microbiologia, Centro Hospitalar de Cascais, Cascais, Portugal; João Mairos and Sandra Francisco, Serviço de Ginecologia and Serviço de Patologia Clínica, Hospital da Força Aérea, Lisboa, Portugal; M. Augusta Guimarães and Catarina Lameiras, Serviço de Microbiologia, Instituto Português de Oncologia do Porto, Porto, Portugal; Manuela Ribeiro and Lídia Branco, Laboratório de Microbiologia, Hospital de São João do Porto, Porto, Portugal; Maria Teresa Azevedo Vaz and Marília Gião, Serviço de Patologia Clínica, Centro Hospitalar do Barlavento Algarvio, Portimão, Portugal; Paulo Paixão and Natália Marto, Laboratório de Patologia Clínica, Hospital da Luz, Lisboa, Portugal; Maria Antónia Read, Maria João Soares and Filipa Carneiro, Laboratório de Microbiologia, Hospital Pedro Hispano, Matosinhos, Portugal; Teresa Sardinha, Luisa Sancho, and Germano Sousa, Laboratório de Microbiologia, Hospital Professor Dr Fernando da Fonseca, Amadora, Lisboa, Portugal; Paula Correia, Serviço de Pediatria, Hospital Professor Dr Fernando da Fonseca, Amadora, Lisboa, Portugal; Rosa M. Barros, Margarida Pinto and Isabel Daniel, Laboratório de Microbiologia, Centro Hospitalar de Lisboa Central, Lisboa, Portugal; Maria João Brito, Gonçalo Cordeiro Ferreira and Catarina Gouveia, Unidade de Infecciologia, Centro Hospitalar de Lisboa Central, Lisboa, Portugal; Ana Morais and Idalina Valadares, Laboratório Análises Clínicas, ACES-Centro de Saúde Oeiras e Carnaxide, Oeiras, Portugal.

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Tavares, A., Miragaia, M., Rolo, J. et al. High prevalence of hospital-associated methicillin-resistant Staphylococcus aureus in the community in Portugal: evidence for the blurring of community–hospital boundaries. Eur J Clin Microbiol Infect Dis 32, 1269–1283 (2013). https://doi.org/10.1007/s10096-013-1872-2

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