Skip to main content

Advertisement

SpringerLink
Log in

Epidemiological and molecular analysis of Streptococcus pyogenes isolates causing invasive disease in Spain (1998–2009): comparison with non-invasive isolates

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

Abstract

The incidence, clinical manifestations, and circulating clones involved in Streptococcus pyogenes invasive disease was analyzed in two regions of Spain between 1998 and 2009. The annual average incidence of invasive disease was 2 episodes per 100,000 inhabitants (3.1 for children and 1.9 for adults). The most frequent clinical manifestations were cellulitis (41.3%), bacteremia without focus (19.0%), streptococcal toxic shock syndrome (12.6%), and pneumonia (7.7%). Among 247 invasive isolates analyzed, the most prevalent clones were emm1/ST28 (27.9%), emm3/ST15-406 (9.8%), and emm4/ST39 (6.5%). The emm1/ST28 clone was the only clone detected each year throughout the study period and was associated with more than one third of all fatal outcomes. When invasive isolates were compared with 1,189 non-invasive isolates, the emm1/ST28 clone was significantly associated with invasive disease. The speA and ssa genes were more frequent among invasive emm1 and emm4 isolates, respectively. Forty-two (17%) invasive isolates were resistant to erythromycin (21 harbored the mef gene and 21 the ermB or ermA genes). Twenty-two (8.9%) isolates had reduced susceptibility to ciprofloxacin (minimum inhibitory concentration [MIC] 2–8 μg/mL) and 32 (13%) were tetracycline-resistant (tetM or tetO gene). In conclusion, the emm1 type was overrepresented among invasive cases and was associated with high mortality rates.

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

Fig. 1

Similar content being viewed by others

References

  1. Carapetis JR, Steer AC, Mulholland EK, Weber M (2005) The global burden of group A streptococcal diseases. Lancet Infect Dis 5:685–694

    Article  PubMed  Google Scholar 

  2. Darenberg J, Luca-Harari B, Jasir A, Sandgren A, Pettersson H, Schalén C et al (2007) Molecular and clinical characteristics of invasive group A streptococcal infection in Sweden. Clin Infect Dis 45:450–458

    Article  PubMed  CAS  Google Scholar 

  3. Friães A, Ramirez M, Melo-Cristino J (2007) Nonoutbreak surveillance of group A streptococci causing invasive disease in Portugal identified internationally disseminated clones among members of a genetically heterogeneous population. J Clin Microbiol 45:2044–2047

    Article  PubMed  Google Scholar 

  4. Imöhl M, Reinert RR, Ocklenburg C, van der Linden M (2010) Epidemiology of invasive Streptococcus pyogenes disease in Germany during 2003–2007. FEMS Immunol Med Microbiol 58:389–396

    PubMed  Google Scholar 

  5. Luca-Harari B, Ekelund K, van der Linden M, Staum-Kaltoft M, Hammerum AM, Jasir A (2008) Clinical and epidemiological aspects of invasive Streptococcus pyogenes infections in Denmark during 2003 and 2004. J Clin Microbiol 46:79–86

    Article  PubMed  CAS  Google Scholar 

  6. Luca-Harari B, Darenberg J, Neal S, Siljander T, Strakova L, Tanna A et al (2009) Clinical and microbiological characteristics of severe Streptococcus pyogenes disease in Europe. J Clin Microbiol 47:1155–1165

    Article  PubMed  CAS  Google Scholar 

  7. Meisal R, Andreasson IK, Høiby EA, Aaberge IS, Michaelsen TE, Caugant DA (2010) Streptococcus pyogenes isolates causing severe infections in Norway in 2006 to 2007: emm types, multilocus sequence types, and superantigen profiles. J Clin Microbiol 48:842–851

    Article  PubMed  CAS  Google Scholar 

  8. O’Loughlin RE, Roberson A, Cieslak PR, Lynfield R, Gershman K, Craig A et al (2007) The epidemiology of invasive group A streptococcal infection and potential vaccine implications: United States, 2000–2004. Clin Infect Dis 45:853–862

    Article  PubMed  Google Scholar 

  9. Siljander T, Lyytikäinen O, Vähäkuopus S, Snellman M, Jalava J, Vuopio J (2010) Epidemiology, outcome and emm types of invasive group A streptococcal infections in Finland. Eur J Clin Microbiol Infect Dis 29:1229–1235

    Article  PubMed  CAS  Google Scholar 

  10. Lancefield RC (1962) Current knowledge of type-specific M antigens of group A streptococci. J Immunol 89:307–313

    PubMed  CAS  Google Scholar 

  11. Steer AC, Batzloff MR, Mulholland K, Carapetis JR (2009) Group A streptococcal vaccines: facts versus fantasy. Curr Opin Infect Dis 22:544–552

    Article  PubMed  CAS  Google Scholar 

  12. McNeil SA, Halperin SA, Langley JM, Smith B, Warren A, Sharratt GP et al (2005) Safety and immunogenicity of 26-valent group a streptococcus vaccine in healthy adult volunteers. Clin Infect Dis 41:1114–1122

    Article  PubMed  CAS  Google Scholar 

  13. Steer AC, Law I, Matatolu L, Beall BW, Carapetis JR (2009) Global emm type distribution of group A streptococci: systematic review and implications for vaccine development. Lancet Infect Dis 9:611–616

    Article  PubMed  Google Scholar 

  14. Le Hello S, Doloy A, Baumann F, Roques N, Coudene P, Rouchon B et al (2010) Clinical and microbial characteristics of invasive Streptococcus pyogenes disease in New Caledonia, a region in Oceania with a high incidence of acute rheumatic fever. J Clin Microbiol 48:526–530

    Article  PubMed  Google Scholar 

  15. Richardson LJ, Towers RJ, Cheng AC, Currie BJ, Carapetis JR, Giffard PM et al (2010) Diversity of emm sequence types in group A beta-haemolytic streptococci in two remote Northern Territory Indigenous communities: implications for vaccine development. Vaccine 28:5301–5305

    Article  PubMed  CAS  Google Scholar 

  16. Pérez-Trallero E, Montes M, Orden B, Tamayo E, García-Arenzana JM, Marimón JM (2007) Phenotypic and genotypic characterization of Streptococcus pyogenes isolates displaying the MLSB phenotype of macrolide resistance in Spain, 1999 to 2005. Antimicrob Agents Chemother 51:1228–1233

    Article  PubMed  Google Scholar 

  17. Clinical and Laboratory Standards Institute (CLSI) (2009) Performance standards for antimicrobial susceptibility testing; 19th informational supplement. CLSI documents M100-S19. CLSI, Wayne, PA

  18. Pérez-Trallero E, Marimón JM, Montes M, Orden B, De Pablos M (1999) Clonal differences among erythromycin-resistant Streptococcus pyogenes in Spain. Emerg Infect Dis 5:235–240

    Article  PubMed  Google Scholar 

  19. Schmitz FJ, Beyer A, Charpentier E, Normark BH, Schade M, Fluit AC et al (2003) Toxin-gene profile heterogeneity among endemic invasive European group A streptococcal isolates. J Infect Dis 188:1578–1586

    Article  PubMed  CAS  Google Scholar 

  20. Powis J, McGeer A, Duncan C, Goren R, De Azavedo JC, Bast DJ et al (2005) Prevalence and characterization of invasive isolates of Streptococcus pyogenes with reduced susceptibility to fluoroquinolones. Antimicrob Agents Chemother 49:2130–2132

    Article  PubMed  CAS  Google Scholar 

  21. Lamagni TL, Neal S, Keshishian C, Powell D, Potz N, Pebody R et al (2009) Predictors of death after severe Streptococcus pyogenes infection. Emerg Infect Dis 15:1304–1307

    Article  PubMed  Google Scholar 

  22. Ardanuy C, Domenech A, Rolo D, Calatayud L, Tubau F, Ayats J et al (2010) Molecular characterization of macrolide- and multidrug-resistant Streptococcus pyogenes isolated from adult patients in Barcelona, Spain (1993–2008). J Antimicrob Chemother 65:634–643

    Article  PubMed  CAS  Google Scholar 

  23. Ikebe T, Hirasawa K, Suzuki R, Isobe J, Tanaka D, Katsukawa C et al (2005) Antimicrobial susceptibility survey of Streptococcus pyogenes isolated in Japan from patients with severe invasive group A streptococcal infections. Antimicrob Agents Chemother 49:788–790

    Article  PubMed  CAS  Google Scholar 

  24. Thigpen MC, Richards CL Jr, Lynfield R, Barrett NL, Harrison LH, Arnold KE et al (2007) Invasive group A streptococcal infection in older adults in long-term care facilities and the community, United States, 1998–2003. Emerg Infect Dis 13:1852–1859

    PubMed  Google Scholar 

  25. Montes M, Orden B, Tamayo E, Alos JI, Pérez-Trallero E (2006) Characterisation of the main clones of Streptococcus pyogenes carrying the ermA (subclass TR) gene in Spain. Int J Antimicrob Agents 28:408–412

    Article  PubMed  Google Scholar 

  26. Rivera A, Rebollo M, Miró E, Mateo M, Navarro F, Gurguí M et al (2006) Superantigen gene profile, emm type and antibiotic resistance genes among group A streptococcal isolates from Barcelona, Spain. J Med Microbiol 55:1115–1123

    Article  PubMed  CAS  Google Scholar 

  27. Aziz RK, Kotb M (2008) Rise and persistence of global M1T1 clone of Streptococcus pyogenes. Emerg Infect Dis 14:1511–1517

    Article  PubMed  CAS  Google Scholar 

  28. Rogers S, Commons R, Danchin MH, Selvaraj G, Kelpie L, Curtis N et al (2007) Strain prevalence, rather than innate virulence potential, is the major factor responsible for an increase in serious group A streptococcus infections. J Infect Dis 195:1625–1633

    Article  PubMed  CAS  Google Scholar 

  29. Haukness HA, Tanz RR, Thomson RB Jr, Pierry DK, Kaplan EL, Beall B et al (2002) The heterogeneity of endemic community pediatric group a streptococcal pharyngeal isolates and their relationship to invasive isolates. J Infect Dis 185:915–920

    Article  PubMed  Google Scholar 

  30. Tamayo E, Montes M, García-Medina G, García-Arenzana JM, Pérez-Trallero E (2010) Spread of a highly mucoid Streptococcus pyogenes emm3/ST15 clone. BMC Infect Dis 10:233

    Article  PubMed  Google Scholar 

  31. Montes M, Tamayo E, Orden B, Larruskain J, Pérez-Trallero E (2010) Prevalence and clonal characterization of Streptococcus pyogenes clinical isolates with reduced fluoroquinolone susceptibility in Spain. Antimicrob Agents Chemother 54:93–97

    Article  PubMed  CAS  Google Scholar 

  32. Pires R, Ardanuy C, Rolo D, Morais A, Brito-Avô A, Gonçalo-Marques J et al (2010) Emergence of ciprofloxacin-nonsusceptible Streptococcus pyogenes isolates from healthy children and pediatric patients in Portugal. Antimicrob Agents Chemother 54:2677–2680

    Article  PubMed  CAS  Google Scholar 

  33. Böhlen LM, Mühlemann K, Dubuis O, Aebi C, Täuber MG (2000) Outbreak among drug users caused by a clonal strain of group A streptococcus. Emerg Infect Dis 6:175–179

    Article  PubMed  Google Scholar 

  34. Curtis SJ, Tanna A, Russell HH, Efstratiou A, Paul J, Cubbon M et al (2007) Invasive group A streptococcal infection in injecting drug users and non-drug users in a single UK city. J Infect 54:422–426

    Article  PubMed  CAS  Google Scholar 

  35. Tyrrell GJ, Lovgren M, St Jean T, Hoang L, Patrick DM, Horsman G et al (2010) Epidemic of group A Streptococcus M/emm59 causing invasive disease in Canada. Clin Infect Dis 51:1290–1297

    Article  PubMed  Google Scholar 

  36. Aguero J, Ortega-Mendi M, Eliecer Cano M, Gonzalez de Aledo A, Calvo J, Viloria L et al (2008) Outbreak of invasive group A streptococcal disease among children attending a day-care center. Pediatr Infect Dis J 27:602–604

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the grants PI 080808 from the Ministerio de Ciencia e Innovación, Spain, and GIU09-59 from the University of the Basque Country, UPV/EHU, Spain, and by CIBER de Enfermedades Respiratorias (CIBERES—CB06/06/0037), an initiative of the ISCIII (Instituto de Salud Carlos III), Madrid, Spain.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Microbiology Service, Hospital Donostia—Instituto Biodonostia, San Sebastián, Gipuzkoa, Spain

    M. Montes & E. Pérez-Trallero

  2. Biomedical Research Centre Network for Respiratory Diseases (CIBERES), Madrid, Spain

    M. Montes, C. Ardanuy, E. Tamayo, J. Liñares & E. Pérez-Trallero

  3. Microbiology Service, Hospital Universitari de Bellvitge—University of Barcelona—IDIBELL, Barcelona, Spain

    C. Ardanuy, A. Domènech & J. Liñares

  4. Department of Preventive Medicine and Public Health, Faculty of Medicine, Basque Country University, San Sebastian, Spain

    E. Pérez-Trallero

  5. Servicio de Microbiología, Hospital Donostia, Paseo Dr. Beguiristain s/n, 20014, San Sebastián, Gipuzkoa, Spain

    E. Pérez-Trallero

Authors
  1. M. Montes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. C. Ardanuy
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. E. Tamayo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. Domènech
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. J. Liñares
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. E. Pérez-Trallero
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E. Pérez-Trallero.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Montes, M., Ardanuy, C., Tamayo, E. et al. Epidemiological and molecular analysis of Streptococcus pyogenes isolates causing invasive disease in Spain (1998–2009): comparison with non-invasive isolates. Eur J Clin Microbiol Infect Dis 30, 1295–1302 (2011). https://doi.org/10.1007/s10096-011-1226-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10096-011-1226-x

Keywords

Search

Navigation