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Staphylococcus aureus nasal carriage among homeless population in Lisbon, Portugal

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Methicillin-resistant Staphylococcus aureus (MRSA) nasal carriage is a major risk factor for infection, namely among populations in the community with inherent prompting factors, such as the homeless. In Portugal, there are no data on S. aureus/MRSA nasal carriage among the homeless community. A total of 84 homeless individuals living in Lisbon (34 with no permanent address and 50 living in shelter) were nasally screened for S. aureus/ MRSA. All isolates were characterized to determine antimicrobial susceptibility and clonal type. A total of 43 (51.2%) S. aureus carriers were identified, including a single individual colonized with MRSA (1.2%). S. aureus carriage rate was higher among individuals with no permanent address (58.8% versus 46%), younger (45.7 ± 12.7 versus 52.5 ± 10.8 years), and with diagnosis of asthma (9% versus 0%). The single MRSA belonged to the EMRSA-15 clone (PFGE D, ST15-SCCmec IVh, and spa type t790). Almost half of the methicillin-susceptible S. aureus (MSSA) isolates (41.9%, n = 18) belonged to two major clones, ST398-t1451 (n = 13) and ST30-t399/t11980/t12808 associated with PFGE I (n = 5). A high proportion of isolates showed non-susceptibility to mupirocin (64%), erythromycin (45%), and fusidic acid (20%) and induced resistance to clindamycin (39%). None of the isolates harboured PVL. Our results suggest that the homeless population of Lisbon does not constitute a reservoir of MRSA in the community, but harbour the highly transmissible ST398-t1451 MSSA lineage.

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  1. Lakhundi S, Zhang K (2018) Methicillin-resistant Staphylococcus aureus: molecular characterization, evolution, and epidemiology. Clin Microbiol Rev 31:e00020–18

  2. David MZ, Daum RS (2010) Community-associated methicillin-resistant Staphylococcus aureus: epidemiology and clinical consequences of an emerging epidemic. Clin Microbiol Rev 23(3):616–687

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. European Union (2018) Social protection committee annual report 2018. Publications Office of the European Union, Brussels

    Google Scholar 

  4. Marrana J, Ferreira P A, Firme J, Gonçalves J, Rosa C, Equipa Intergerações (2015) Do Outro Lado - Programa Intergerações / Intersituações – para o conhecimento das pessoas em situação sem-abrigo em Lisboa. Santa Casa da Misericórdia de Lisboa

  5. Fazel S, Geddes JR, Kushel M (2014) The health of homeless people in high-income countries: descriptive epidemiology, health consequences, and clinical and policy recommendations. Lancet 384(9953):1529–1540

    Article  PubMed  PubMed Central  Google Scholar 

  6. Charlebois ED, Bangsberg DR, Moss NJ, Moore MR, Moss AR, Chambers HF, Perdreau-Remington F (2002) Population-based community prevalence of methicillin-resistant Staphylococcus aureus in the urban poor of San Francisco. Clin Infect Dis 34(4):425–433

    Article  PubMed  Google Scholar 

  7. Gilbert M, MacDonald J, Gregson D, Siushansian J, Zhang K, Elsayed S, Laupland K, Louie T, Hope K, Mulvey M, Gillespie J, Nielsen D, Wheeler V, Louie M, Honish A, Keays G, Conly J (2006) Outbreak in Alberta of community-acquired (USA300) methicillin-resistant Staphylococcus aureus in people with a history of drug use, homelessness or incarceration. CMAJ 175(2):149–154

    Article  PubMed  PubMed Central  Google Scholar 

  8. Farr AM, Aden B, Weiss D, Nash D, Marx MA (2012) Trends in hospitalization for community-associated methicillin-resistant Staphylococcus aureus in New York City, 1997-2006: data from New York State’s Statewide Planning and Research Cooperative System. Infect Control Hosp Epidemiol 33(7):725–731

    Article  PubMed  Google Scholar 

  9. European Centre for Disease Control and Prevention (2018) Antimicrobial resistance surveillance in Europe 2017. Annual Report of the European Antimicrobial Resistance Surveillance Network (EARS-Net). European Centre for Disease Control and Prevention (ECDC), Stockholm: ECDC

  10. Melo-Cristino J, Resina C, Manuel V, Lito L, Ramirez M (2013) First case of infection with vancomycin-resistant Staphylococcus aureus in Europe. Lancet 382(9888):205

    Article  PubMed  Google Scholar 

  11. Tavares A, Miragaia M, Rolo J, Coelho C, de Lencastre H, CA-MRSA/ MSSA working group (2013) 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(10):1269–1283

    Article  CAS  PubMed  Google Scholar 

  12. 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(3):e17630

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Martins HFG, Venâncio I, Pinto B, Fernandes RN (2017) Health care of homeless patient in Lisbon: comparison between roofless and houseless people. Revista Sociedade Portuguesa de Medicina Interna (RSPMI). Accessed 30 May 2019

  14. Amore K, Baker M, Howden-Chapman P (2011) The ETHOS definition and classification of homelessness: an analysis. Eur J Homelessness 5(2):19–37

    Google Scholar 

  15. Instituto da Segurança Social Portugal (2009) Estratégia nacional para a integração de pessoas sem-abrigo. Prevenção, intervenção e acompanhamento, 2009–2015

  16. Conceição T, de Lencastre H, Aires-de-Sousa M (2017) Carriage of Staphylococcus aureus among Portuguese nursing students: a longitudinal cohort study over four years of education. PLoS One 12(11):e0188855

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Poulsen AB, Skov R, Pallesen LV (2003) Detection of methicillin resistance in coagulase-negative staphylococci and in staphylococci directly from simulated blood cultures using the EVIGENE MRSA detection kit. J Antimicrob Chemother 51(2):419–421

    Article  CAS  PubMed  Google Scholar 

  18. Aires-de-Sousa M, Boye K, de Lencastre H, Deplano A, Enright MC, Etienne J, Friedrich A, Harmsen D, Holmes A, Huijsdens XW, Kearns AM, Mellmann A, Meugnier H, Rasheed JK, Spalburg E, Strommenger B, Struelens MJ, Tenover FC, Thomas J, Vogel U, Westh H, Xu J, Witte W (2006) High interlaboratory reproducibility of DNA sequence-based typing of bacteria in a multicenter study. J Clin Microbiol 44(2):619–621

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Okuma K, Iwakawa K, Turnidge JD, Grubb WB, Bell JM, O’Brien FG, Coombs GW, Pearman JW, Tenover FC, Kapi M, Tiensasitorn C, Ito T, Hiramatsu K (2002) Dissemination of new methicillin-resistant Staphylococcus aureus clones in the community. J Clin Microbiol 40(11):4289–4294

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Chung M, de Lencastre H, Matthews P, Tomasz A, Adamsson I, Aires de Sousa M, Camou T, Cocuzza C, Corso A, Couto I, Dominguez A, Gniadkowski M, Goering R, Gomes A, Kikuchi K, Marchese A, Mato R, Melter O, Oliveira D, Palacio R, Sá-Leão R, Santos Sanches I, Song JH, Tassios PT, Villari P (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(3):189–198

    Article  CAS  PubMed  Google Scholar 

  21. 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(3):1008–1015

    CAS  PubMed  PubMed Central  Google Scholar 

  22. 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(9):3374–3377

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. 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(1):42–48

    Article  PubMed  CAS  Google Scholar 

  24. Lina G, Piemont Y, Godail-Gamot F, Bes M, Peter MO, Gauduchon V, Vandenesch F, Etienne J (1999) Involvement of Panton-valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clin Infect Dis 29(5):1128–1132

    Article  CAS  PubMed  Google Scholar 

  25. Kluytmans J, van Belkum A, Verbrugh H (1997) Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks. Clin Microbiol Rev 10(3):505–520

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. 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(3):237–245

    Article  PubMed  Google Scholar 

  27. Almeida ST, Nunes S, Paulo AC, Faria NA, de Lencastre H, Sa-Leao R (2015) Prevalence, risk factors, and epidemiology of methicillin-resistant Staphylococcus aureus carried by adults over 60 years of age. Eur J Clin Microbiol Infect Dis 34(3):593–600

    Article  CAS  PubMed  Google Scholar 

  28. Ottomeyer M, Graham CD, Legg AD, Cooper ES, Law CD, Molani M, Matevossian K, Marlin J, Williams C, Newman R, Wasserman JA, Segars LW, Taylor TA (2016) Prevalence of nasal colonization by methicillin-resistant Staphylococcus aureus in persons using a homeless shelter in Kansas City. Front Public Health 4:234

    Article  PubMed  PubMed Central  Google Scholar 

  29. Landers TF, Harris RE, Wittum TE, Stevenson KB (2009) Colonization with Staphylococcus aureus and methicillin-resistant S. aureus among a sample of homeless individuals, Ohio. Infect Control Hosp Epidemiol 30(8):801–803

    Article  PubMed  PubMed Central  Google Scholar 

  30. Leibler JH, Leon C, Cardoso LJP, Morris JC, Miller NS, Nguyen DD, Gaeta JM (2017) Prevalence and risk factors for MRSA nasal colonization among persons experiencing homelessness in Boston, MA. J Med Microbiol 66:1183–1188

    Article  PubMed  PubMed Central  Google Scholar 

  31. Dall’Antonia M, Coen PG, Wilks M, Whiley A, Millar M (2005) Competition between methicillin-sensitive and -resistant Staphylococcus aureus in the anterior nares. J Hosp Infect 61(1):62–67

    Article  PubMed  Google Scholar 

  32. Shrestha NK, Fraser TG, Gordon SM (2019) Methicillin resistance in Staphylococcus aureus infections among patients colonized with methicillin-susceptible Staphylococcus aureus. Clin Microbiol Infect 25(1):71–75

    Article  CAS  PubMed  Google Scholar 

  33. Liu C, Bayer A, Cosgrove SE, Daum RS, Fridkin SK, Gorwitz RJ, Kaplan SL, Karchmer AW, Levine DP, Murray BE, M JR, Talan DA, Chambers HF, Infectious Diseases Society of A (2011) Clinical practice guidelines by the infectious diseases society of america for the treatment of methicillin-resistant Staphylococcus aureus infections in adults and children. Clin Infect Dis 52(3):e18–e55

    Article  PubMed  Google Scholar 

  34. Khan A, Wilson B, Gould IM (2018) Current and future treatment options for community-associated MRSA infection. Expert Opin Pharmacother 19(5):457–470

    Article  CAS  PubMed  Google Scholar 

  35. Raoult D, Foucault C, Brouqui P (2001) Infections in the homeless. Lancet Infect Dis 1(2):77–84

    Article  CAS  PubMed  Google Scholar 

  36. Monteiro M, Read A, Carneiro F, Soares MJ, Soares V (2016) Letter to the editor concerning the evaluation of mupirocin resistance in methicillin-resistant Staphylococcus aureus strains. Acta Medica Port 29(9):578

    Article  Google Scholar 

  37. Conceição T, Diamantino F, Coelho C, de Lencastre H, Aires-de-Sousa M (2013) Contamination of public buses with MRSA in Lisbon, Portugal: a possible transmission route of major MRSA clones within the community. PLoS One 8(11):e77812

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Ballhausen B, Kriegeskorte A, van Alen S, Jung P, Kock R, Peters G, Bischoff M, Becker K (2017) The pathogenicity and host adaptation of livestock-associated MRSA CC398. Vet Microbiol 200:39–45

    Article  PubMed  Google Scholar 

  39. Conceição T, de Lencastre H, Aires-de-Sousa M (2017) Frequent isolation of methicillin resistant Staphylococcus aureus (MRSA) ST398 among healthy pigs in Portugal. PLoS One 12(4):e0175340

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. Uhlemann AC, Porcella SF, Trivedi S, Sullivan SB, Hafer C, Kennedy AD, Barbian KD, McCarthy AJ, Street C, Hirschberg DL, Lipkin WI, Lindsay JA, DeLeo FR, Lowy FD (2012) Identification of a highly transmissible animal-independent Staphylococcus aureus ST398 clone with distinct genomic and cell adhesion properties. mBio 3:e00027–12

  41. Valentin-Domelier AS, Girard M, Bertrand X, Violette J, Francois P, Donnio PY, Talon D, Quentin R, Schrenzel J, van der Mee-Marquet N, Bloodstream Infection Study Group of the Reseau des Hygienistes du C (2011) Methicillin-susceptible ST398 Staphylococcus aureus responsible for bloodstream infections: an emerging human-adapted subclone? PLoS One 6(12):e28369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. David MZ, Siegel J, Lowy FD, Zychowski D, Taylor A, Lee CJ, Boyle-Vavra S, Daum RS (2013) Asymptomatic carriage of sequence type 398, spa type t571 methicillin-susceptible Staphylococcus aureus in an urban jail: a newly emerging, transmissible pathogenic strain. J Clin Microbiol 51(7):2443–2447

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Rasigade JP, Laurent F, Hubert P, Vandenesch F, Etienne J (2010) Lethal necrotizing pneumonia caused by an ST398 Staphylococcus aureus strain. Emerg Infect Dis 16(8):1330

    Article  PubMed  PubMed Central  Google Scholar 

  44. van Belkum A, Melles DC, Peeters JK, van Leeuwen WB, van Duijkeren E, Huijsdens XW, Spalburg E, de Neeling AJ, Verbrugh HA, Dutch Working Party on S, Research of M-S (2008) Methicillin-resistant and -susceptible sequence type 398 in pigs and humans. Emerg Infect Dis 14(3):479–483

    Article  PubMed  PubMed Central  Google Scholar 

  45. Valour F, Tasse J, Trouillet-Assant S, Rasigade JP, Lamy B, Chanard E, Verhoeven P, Decousser JW, Marchandin H, Bes M, Chidiac C, Vandenesch F, Ferry T, Laurent F, Lyon B, Joint Infection study g (2014) Methicillin-susceptible Staphylococcus aureus clonal complex 398: high prevalence and geographical heterogeneity in bone and joint infection and nasal carriage. Clin Microbiol Infect 20(10):O772–O775

    Article  CAS  PubMed  Google Scholar 

  46. Uhlemann AC, McAdam PR, Sullivan SB, Knox JR, Khiabanian H, Rabadan R, Davies PR, Fitzgerald JR, Lowy FD (2017) Evolutionary dynamics of pandemic methicillin-sensitive Staphylococcus aureus ST398 and its international spread via routes of human migration. mBio 8:e01375–16

  47. Mediavilla JR, Chen L, Uhlemann AC, Hanson BM, Rosenthal M, Stanak K, Koll B, Fries BC, Armellino D, Schilling ME, Weiss D, Smith TC, Lowy FD, Kreiswirth BN (2012) Methicillin-susceptible Staphylococcus aureus ST398, New York and New Jersey, USA. Emerg Infect Dis 18(4):700–702

    Article  PubMed  PubMed Central  Google Scholar 

  48. Argudin MA, Deplano A, Vandendriessche S, Dodemont M, Nonhoff C, Denis O, Roisin S (2018) CC398 Staphylococcus aureus subpopulations in Belgian patients. Eur J Clin Microbiol Infect Dis 37(5):911–916

    Article  CAS  PubMed  Google Scholar 

  49. Lozano C, Aspiroz C, Charlez L, Gomez-Sanz E, Toledo M, Zarazaga M, Torres C (2011) Skin lesion by methicillin-resistant Staphylococcus aureus ST398-t1451 in a Spanish pig farmer: possible transmission from animals to humans. Vector Borne Zoonotic Dis 11(6):605–607

    Article  PubMed  Google Scholar 

  50. Lozano C, Rezusta A, Gomez P, Gomez-Sanz E, Baez N, Martin-Saco G, Zarazaga M, Torres C (2012) High prevalence of spa types associated with the clonal lineage CC398 among tetracycline-resistant methicillin-resistant Staphylococcus aureus strains in a Spanish hospital. J Antimicrob Chemother 67(2):330–334

    Article  CAS  PubMed  Google Scholar 

  51. Tavares A, Faria NA, de Lencastre H, Miragaia M (2013) Population structure of methicillin-susceptible Staphylococcus aureus (MSSA) in Portugal over a 19-year period (1992-2011). Eur J Clin Microbiol Infect Dis 33(3):423–432

    Article  PubMed  CAS  Google Scholar 

  52. Faria NA, Miragaia M, de Lencastre H, Multi Laboratory Project C (2013) Massive dissemination of methicillin resistant Staphylococcus aureus in bloodstream infections in a high MRSA prevalence country: establishment and diversification of EMRSA-15. Microb Drug Resist 19(6):483–490

    Article  CAS  PubMed  Google Scholar 

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The authors are grateful to the medical doctors and nurses of the VOXLisboa association for the given assistance during the nasal screenings.


This work was partly supported by project PTDC/DTP-EPI/0842/2014 from Fundação para a Ciência e a Tecnologia (FCT), Portugal, by Project LISBOA-01-0145-FEDER-007660 (Microbiologia Molecular, Estrutural e Celular) funded by FEDER funds through COMPETE2020-Programa Operacional Competitividade e Internacionalização (POCI) and by national funds through FCT, and by ONEIDA project LISBOA-01-0145-FEDER-016417 co-funded by FEEI-“Fundos Europeus Estruturais e de Investimento” from “Programa Operacional Regional Lisboa 2020” and by national funds from FCT. Teresa Conceição and Suzilaine Rodrigues were supported by grants SFRH/BPD/72422/2010 and 02/BI/2017 respectively, from FCT, Portugal.

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Correspondence to Teresa Conceição.

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The protocol was approved by the Ethics Committee of Escola Superior de Saúde da Cruz Vermelha Portuguesa and a written informed consent was obtained from all participants.

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Conceição, T., Martins, H., Rodrigues, S. et al. Staphylococcus aureus nasal carriage among homeless population in Lisbon, Portugal. Eur J Clin Microbiol Infect Dis 38, 2037–2044 (2019).

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