Skip to main content

Advertisement

Log in

Prevalence, risk factors, and epidemiology of methicillin-resistantStaphylococcus aureus carried by adults over 60 years of age

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

Abstract

The epidemiology of methicillin-resistant Staphylococcus aureus (MRSA) in the community in Portugal is not completely understood. To evaluate S. aureus and MRSA carriage among the elderly, we conducted a large cross-sectional study between April 2010 and December 2012. A total of 3,361 adults over 60 years of age were screened for S. aureus nasopharyngeal and oropharyngeal carriage. MRSA were characterized by staphylococcal cassette chromosome mec (SCCmec) typing, spa typing, multilocus sequence typing (MLST), and tested for the presence of Panton–Valentine leukocidin (PVL). Risk factors for MRSA carriage were identified by multiple logistic regression analysis. The prevalence of S. aureus and MRSA carriage among the elderly was 20.1 % and 1.8 %, respectively. The risk of being an MRSA carrier was higher among the elderly living in retirement homes [odds ratio (OR) = 2.90, 95 % confidence interval (CI): 1.48–5.48] and those that had been hospitalized in the previous year (OR = 2.64, 95 % CI: 1.47–4.58). Among the 62 MRSA isolates, 64.5 % were multidrug-resistant and none carried PVL. Most MRSA (82.3 %) were related to three hospital-associated (HA-MRSA) clones disseminated in Portugal: ST105-II (New York/Japan clone; 43.5 %), ST5-IVc (Pediatric clone; 19.4 %), and ST22-IVh (EMRSA-15 clone; 19.4 %). The New York/Japan and Pediatric clones were significantly associated with carriers living in retirement homes, while the EMRSA-15 clone was associated with carriers that had been hospitalized. We conclude that the elderly population in Portugal is essentially free of MRSA. Given the current European societal challenges for a healthy active aging, these results are of importance to healthcare professionals and public authorities to decide on strategies to promote health in this age group.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Naimi TS, LeDell KH, Como-Sabetti K, Borchardt SM, Boxrud DJ, Etienne J, Johnson SK, Vandenesch F, Fridkin S, O’Boyle C, Danila RN, Lynfield R (2003) Comparison of community- and health care-associated methicillin-resistant Staphylococcus aureus infection. JAMA 290(22):2976–2984

    Article  CAS  PubMed  Google Scholar 

  2. Otter JA, French GL (2010) Molecular epidemiology of community-associated meticillin-resistant Staphylococcus aureus in Europe. Lancet Infect Dis 10(4):227–239

    Article  PubMed  Google Scholar 

  3. Mediavilla JR, Chen L, Mathema B, Kreiswirth BN (2012) Global epidemiology of community-associated methicillin resistant Staphylococcus aureus (CA-MRSA). Curr Opin Microbiol 15(5):588–595

    Article  PubMed  Google Scholar 

  4. Mollaghan AM, Lucey B, Coffey A, Cotter L (2010) Emergence of MRSA clone ST22 in healthy young adults in the community in the absence of risk factors. Epidemiol Infect 138(5):673–676

    Article  CAS  PubMed  Google Scholar 

  5. European Centre for Disease Prevention and Control (ECDC) (2012) Antimicrobial resistance surveillance in Europe 2012. Available online at: http://www.ecdc.europa.eu/en/publications/Publications/antimicrobial-resistance-surveillance-europe-2012.pdf. Accessed 27 May 2014

  6. Faria NA, Miragaia M, de Lencastre H; Multi Laboratory Project Collaborators (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 

  7. 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(9):2912–2917

  8. 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 

  9. 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 10:110

    Article  PubMed Central  PubMed  Google Scholar 

  10. Espadinha D, Faria NA, Miragaia M, Lito LM, Melo-Cristino J, de Lencastre H; Médicos Sentinela Network (2013) Extensive dissemination of methicillin-resistant Staphylococcus aureus (MRSA) between the hospital and the community in a country with a high prevalence of nosocomial MRSA. PLoS One 8(4):e59960

  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. Almeida ST, Nunes S, Santos Paulo AC, Valadares I, Martins S, Breia F, Brito-Avô A, Morais A, de Lencastre H, Sá-Leão R (2014) Low prevalence of pneumococcal carriage and high serotype and genotype diversity among adults over 60 years of age living in Portugal. PLoS One 9(3):e90974

    Article  PubMed Central  PubMed  Google Scholar 

  13. Clinical and Laboratory Standards Institute (CLSI) (2009) Performance standards for antimicrobial disk susceptibility tests; approved standard—tenth edition. M02-A10. CLSI, Wayne

    Google Scholar 

  14. European Committee on Antimicrobial Susceptibility Testing (EUCAST) Clinical breakpoints. Available online at: http://www.eucast.org/clinical_breakpoints/

  15. 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 Central  PubMed  Google Scholar 

  16. Mainous AG 3rd, Hueston WJ, Everett CJ, Diaz VA (2006) Nasal carriage of Staphylococcus aureus and methicillin-resistant S. aureus in the United States, 2001–2002. Ann Fam Med 4(2):132–137

  17. Munckhof WJ, Nimmo GR, Schooneveldt JM, Schlebusch S, Stephens AJ, Williams G, Huygens F, Giffard P (2009) Nasal carriage of Staphylococcus aureus, including community-associated methicillin-resistant strains, in Queensland adults. Clin Microbiol Infect 15(2):149–155

    Article  CAS  PubMed  Google Scholar 

  18. Scerri J, Monecke S, Borg MA (2013) Prevalence and characteristics of community carriage of methicillin-resistant Staphylococcus aureus in Malta. J Epidemiol Glob Health 3(3):165–173

  19. Pan A, Lee A, Cooper B, Chalfine A, Daikos GL, Garilli S, Goossens H, Malhotra-Kumar S, Martínez JA, Patroni A, Harbarth S; SURF study group (MRSA colonisation on admission to surgical wards in Europe: identification of risk factors), in collaboration with the MOSAR-04 Study Team (2013) Risk factors for previously unknown meticillin-resistant Staphylococcus aureus carriage on admission to 13 surgical wards in Europe. J Hosp Infect 83(2):107–113

  20. Lewis HC, Mølbak K, Reese C, Aarestrup FM, Selchau M, Sørum M, Skov RL (2008) Pigs as source of methicillin-resistant Staphylococcus aureus CC398 infections in humans, Denmark. Emerg Infect Dis 14(9):1383–1389

  21. 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 Central  PubMed  Google Scholar 

  22. 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(3):212–218

  23. Maugat S, de Rougemont A, Aubry-Damon H, Reverdy ME, Georges S, Vandenesch F, Etienne J, Coignard B (2009) Methicillin-resistant Staphylococcus aureus among a network of French private-sector community-based-medical laboratories. Med Mal Infect 39(5):311–318

  24. Lasseter G, Charlett A, Lewis D, Donald I, Howell-Jones R, McNulty CA (2010) Staphylococcus aureus carriage in care homes: identification of risk factors, including the role of dementia. Epidemiol Infect 138(5):686–696

    Article  CAS  PubMed  Google Scholar 

  25. Olsen K, Falch BM, Danielsen K, Johannessen M, Ericson Sollid JU, Thune I, Grimnes G, Jorde R, Simonsen GS, Furberg AS (2012) Staphylococcus aureus nasal carriage is associated with serum 25-hydroxyvitamin D levels, gender and smoking status. The Tromsø Staph and Skin Study. Eur J Clin Microbiol Infect Dis 31(4):465–473

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  26. Sdougkos G, Chini V, Papanastasiou DA, Christodoulou G, Stamatakis E, Vris A, Christodoulidi I, Protopapadakis G, Spiliopoulou I (2008) Community-associated Staphylococcus aureus infections and nasal carriage among children: molecular microbial data and clinical characteristics. Clin Microbiol Infect 14(11):995–1001

  27. Cursino MA, Garcia CP, Lobo RD, Salomão MC, Gobara S, Raymundo GF, Kespers T, Soares RE, Mollaco CH, Keil KG, Malieno PB, Krebs VL, Gibelli MA, Kondo MM, Zugaib M, Costa SF, Levin AS (2012) Performance of surveillance cultures at different body sites to identify asymptomatic Staphylococcus aureus carriers. Diagn Microbiol Infect Dis 74(4):343–348

    Article  PubMed  Google Scholar 

  28. Miller LG, Eells SJ, Taylor AR, David MZ, Ortiz N, Zychowski D, Kumar N, Cruz D, Boyle-Vavra S, Daum RS (2012) Staphylococcus aureus colonization among household contacts of patients with skin infections: risk factors, strain discordance, and complex ecology. Clin Infect Dis 54(11):1523–1535

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  29. Lee CJ, Sankaran S, Mukherjee DV, Apa ZL, Hafer CA, Wright L, Larson EL, Lowy FD (2011) Staphylococcus aureus oropharyngeal carriage in a prison population. Clin Infect Dis 52(6):775–778

    Article  PubMed Central  PubMed  Google Scholar 

  30. Hamdan-Partida A, Sainz-Espuñes T, Bustos-Martínez J (2010) Characterization and persistence of Staphylococcus aureus strains isolated from the anterior nares and throats of healthy carriers in a Mexican community. J Clin Microbiol 48(5):1701–1705

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

The authors are grateful to the participants that collaborated in the study. We thank Ana Paula Ribeiro from Câmara Municipal de Montemor-o-Novo for her extraordinary support in the implementation of fieldwork in Montemor-o-Novo. We thank the excellent skills of nurses Anabela Gonçalves and Pedro Fonseca.

Conflict of interest

The authors declare that they have no conflict of interest.

Financial disclosure

This work was partially supported by grants PTDC/BIA-BEC/098289/2008 (to RS-L) and PEst-OE/EQB/LA0004/2011 (to the Oeiras Associated Laboratory) from Fundação para a Ciência e a Tecnologia (FCT), Portugal. NAF was supported by post-doctoral grant SFRH/BPD/66514/2009 from FCT.

Authorship/contribution

Conceived and designed the experiments: RS-L, HdL. Acquired data and performed experiments: STA, SN, RS-L. Analyzed the data: STA, SN, ACSP, NAF, RS-L. Contributed reagents/materials/analysis tools: RS-L, HdL. Wrote the paper: STA, RS-L. Critically revised the manuscript and approved the final version: all authors.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to R. Sá-Leão.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Table S1

(DOCX 39 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Almeida, S.T., Nunes, S., Paulo, A.C.S. et al. Prevalence, risk factors, and epidemiology of methicillin-resistantStaphylococcus aureus carried by adults over 60 years of age. Eur J Clin Microbiol Infect Dis 34, 593–600 (2015). https://doi.org/10.1007/s10096-014-2267-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10096-014-2267-8

Keywords

Navigation