Volume 17, Number 2—February 2011
Clonal Spread of Streptococcus pyogenes emm44 among Homeless Persons, Rennes, France
To the Editor: Streptococcus pyogenes, or group A streptococci (GAS), are human pathogens responsible for pharyngitis as well as skin and soft tissue infections. Invasive GAS diseases, including bacteremia, cellulitis, and necrotizing fasciitis, are life-threatening, especially when associated with toxic shock syndrome. Several risk factors for GAS infections are known, such as diabetes, immunosuppression, drug use, and skin lesions (1,2).
In France in 2008, 12% of GAS strains were reported resistant to tetracycline by the national reference center. Unexpected recognition of 8 tetracycline-resistant GAS isolates in January and February 2009 at the 1,950-bed University Hospital of Rennes in western France led to further investigation. We report results of characterization of tetracycline-resistant GAS isolates collected during 2009 from hospitalized and outclinic patients.
Isolates were identified as GAS on the basis of β-hemolysis, Gram staining, negative catalase test result, positive pyrrolidonyl arylamidase test result, and agglutination with Lancefield group A antiserum. Antimicrobial drug susceptibility to penicillin G, amoxicillin, erythromycin, lincomycin, tetracycline, rifampin, streptomycin, kanamycin, gentamicin, and vancomycin was tested by using the disk diffusion method according to the criteria of the French Society for Microbiology (www.sfm.asso.fr). Of 72 nonduplicate GAS isolates collected, 25 (17 from inpatients, 8 from outpatients) were identified as tetracycline resistant; they were further characterized as described (3).
The emm types of these 25 tetracycline-resistant strains were determined by sequencing the variable 5′ end of the emm gene and comparing sequences with the Centers for Disease Control and Prevention database (www.cdc.gov/ncidod/biotech/strep/doc.htm). Twenty-three strains were emm44 type, 1 was emm105, and 1 emm83. Pulsed-field gel electrophoresis (PFGE) patterns obtained after DNA digestion by SmaI restriction enzyme were compared according to Tenover criteria (4). The epidemic clone including 22 strains was characterized by an identical PFGE pattern 44-A1, whereas PFGE pattern 44-A5 of the remaining emm44 strain differed by 4 DNA bands (Figure). Epidemic strains also shared the same biotype 3 obtained on rapid ID 32 Strep strips (bioMérieux, Marcy l’Etoile, France). T types were determined on trypsinated bacteria by slide agglutination with type-specific antisera. Eleven strains were type T11, 4 type T11/12, 1 type T11/3/13/B3264, and 6 non–T-typeable.
All epidemic emm44 strains were susceptible to all antibacterial agents tested except tetracycline. MICs of tetracycline, determined with Etest method (AB Biodisk, Solna, Sweden), were 24–48 mg/L. Screening of strains by PCR for tet(M), tet(O), tet(K), and tet(L) genes showed tetracycline resistance was related to tet(M) gene. A multiplex PCR for detection of speA, speB, speC, smeZ, and ssa toxin genes showed that epidemic strain possessed only speB gene.
Investigation conducted by local health authorities showed that the first 5 patients with emm44 strain were drug users sharing a squat (illegally occupied housing). Although this place was shut down at the end of February after an outbreak of scabies, additional cases of infections caused by emm44 strain occurred. Medical care is difficult to implement for homeless persons, thus, we limited our action to swabbing symptomatic persons to treat them and to limit spread of the epidemic strain. Following recommendations from the Institute for Public Health Surveillance, in mid-April nurses at the 2 main social centers for homeless persons obtained samples from 17 persons. Eleven persons were infected with GAS, of whom 8 had not been swabbed before. All but 1 isolate was emm44.
Among the 22 patients infected with epidemic 44-A1 clone, 4 had several successive isolations of this strain. Most (19) infections were secondary infections of skin injuries; others were abscesses (4), septic arthritis (2), necrotizing fasciitis (1), erysipelas (1), and hygroma (1). Five isolates were from sterile sites (1 surgical sample of necrotizing fasciitis, 1 blood culture, and 3 joint fluids). Most infections had favorable outcomes, with the exception of a 79-year old man who died of erysipelas. Patient median age was 37 years (range 20–79 years); all but 1 were men. Eighty-six percent had risk factors such as alcohol abuse (17, 77%), homelessness (16, 73%), drug use (11, 50%), hepatitis C infection (4, 8%), and HIV infection (1, 4.5%). Two patients had no identified risk factors. Complete characteristics of 50 patients infected with a strain of GAS different from 44-A1 clone were not available. However, this population did differ by its sex ratio (28 men:22 women) and by older median age (47.3 years).
We report clonal spread of an emm44 tetracycline-resistant GAS strain in marginal populations (drug users and homeless persons) in Rennes. This strain, characterized by PFGE pattern 44-A1, represented 22/25 tetracycline resistant GAS isolates and 30% of the 72 GAS isolates identified at the hospital in Pontchaillou in 2009. Locally, emergence of the 44-A1 clone led to the dramatic increase of GAS tetracycline resistance, from 17% in 2008 to 35% in 2009. emm44 GAS strains, which share identical 5′emm sequences with previously designated M/ emm61 strains (5), have mainly been isolated in Asia from throat and skin specimens (6,7). They were rarely reported as responsible for invasive infections in France or other parts of the world (5,8). Polyclonal and emm25 and emm83 monoclonal GAS outbreaks have been recently described among drug users in Switzerland, the United Kingdom, and Spain (9,10) without robust evidence of enhanced virulence of the causative GAS strains. In the outbreak we report, skin infections might be a leading cause of bacterial transmission between people living in poor hygienic conditions and overcrowded spaces.
We thank the local health authorities, the Institute for Public Health Surveillance, and the nurses working in social centers for their helpful collaboration. We also thank Gislène Collobert and Gérald Touak for excellent technical assistance and Lucie Donnio for correcting the English in this manuscript.
- Factor SH, Levine OS, Schwartz B, Harrison LH, Farley MM, McGeer A, Invasive group A streptococcal disease: risk factors for adults. Emerg Infect Dis. 2003;9:970–7.
- Lamagni TL, Darenberg J, Luca-Harari B, Siljander T, Efstratiou A, Henriques-Normark B, Epidemiology of severe Streptococcus pyogenes disease in Europe. J Clin Microbiol. 2008;46:2359–67.
- Mihaila-Amrouche L, Bouvet A, Loubinoux J. Clonal spread of emm type 28 isolates of Streptococcus pyogenes that are multiresistant to antibiotics. J Clin Microbiol. 2004;42:3844–6.
- Tenover FC, Arbeit RD, Goering RV, Mickelsen PA, Murray BE, Persing DH, Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol. 1995;33:2233–9.
- Johnson DR, Kaplan EL, VanGheem A, Facklam RR, Beall B. Characterization of group A streptococci (Streptococcus pyogenes): correlation of M-protein and emm-gene type with T-protein agglutination pattern and serum opacity factor. J Med Microbiol. 2006;55:157–64.
- Koh EH, Kim S, Lee NY. Decrease of erythromycin resistance in group A streptococci by change of emm distribution. Jpn J Infect Dis. 2008;61:261–3.
- Sagar V, Kumar R, Ganguly NK, Chakraborti A. Comparative analysis of emm type pattern of group A streptococcus throat and skin isolates from India and their association with closely related SIC, a streptococcal virulence factor. BMC Microbiol. 2008;8:150.
- Luca-Harari B, Darenberg J, Neal S, Siljander T, Strakova L, Tanna A, Clinical and microbiological characteristics of severe Streptococcus pyogenes disease in Europe. J Clin Microbiol. 2009;47:1155–65.
- Lamagni TL, Neal S, Keshishian C, Hope V, George R, Duckworth G, Epidemic of severe Streptococcus pyogenes infections in injecting drug users in the UK, 2003–2004. Clin Microbiol Infect. 2008;14:1002–9.
- Sierra JM, Sanchez F, Castro P, Salvado M, de la Red G, Libois A, Group A streptococcal infections in injection drug users in Barcelona, Spain: epidemiologic, clinical, and microbiologic analysis of 3 clusters of cases from 2000 to 2003. Medicine (Baltimore). 2006;85:139–46.
FigureCite This Article
1These authors contributed equally to this article.