- Email: [email protected]
Species and emm-type distribution of group C and G streptococci from different sites of isolation
Diagnostic Microbiology and Infectious Disease xxx (2016) xxx–xxx
Contents lists available at ScienceDirect
Diagnostic Microbiology and Infectious Disease journal homepage: www.elsevier.com/locate/diagmicrobio
Note
Species and emm-type distribution of group C and G streptococci from different sites of isolation Kristina Trell a, Bo Nilson b,c, Magnus Rasmussen a,⁎ a b c
Division of Infection Medicine, Department of Clinical Sciences, Lund University, Lund, Sweden Department of Laboratory Medicine Lund, Section of Medical Microbiology, Lund University, Lund, Sweden Clinical Microbiology, Labmedicin, Region Skåne, Lund, Sweden
a r t i c l e
i n f o
Article history: Received 28 April 2016 Received in revised form 31 August 2016 Accepted 12 September 2016 Available online xxxx
a b s t r a c t beta-Haemolytic streptococci of groups C (GCS) and G (GGS) from human infections typically belong to Streptococcus dysgalactiae and are important human pathogens. Among GGS (183 isolates), several emm-types were identified without significant differences between different sites of isolation. For GCS (79 isolates), the typedistribution was markedly different and more restricted. © 2016 Elsevier Inc. All rights reserved.
Keywords: Streptococcus dysgalactiae Group G Streptococcus Group C Streptococcus
beta-Haemolytic streptococci of groups C and G (GCS and GGS), the majority of which are Streptococcus dysgalactiae subsp. Equisimilis (SDSE), have become increasingly recognized as causes of severe and invasive human infections (Takahashi et al., 2011; Brandt and Spellerberg, 2009; Rantala, 2014). SDSE cause a disease spectrum similar to that of Streptococcus pyogenes, including erysipelas (Bläckberg et al., 2015), wound infections (Rantala et al., 2009), and pharyngitis (Bramhachari et al., 2010). Species determination of GCS and GGS can be achieved using matrix-assisted laser desorption ionization - time of flight mass spectrometry (MALDI-TOF MS) (Rantala et al., 2010; Cherkaoui et al., 2011) and further typing could be based on the sequence of the emm gene, encoding the M protein (Brandt and Spellerberg, 2009; Jensen and Kilian, 2012). Although subspecies determination is not possible through these methods, previous studies have shown that the vast majority of human isolates of Streptococcus dysgalactiae (SD) are SDSE. Several studies have investigated the distribution of SD emm-types in invasive infections (Takahashi et al., 2011; Rantala et al., 2010; Pinho et al., 2006; Broyles et al., 2009; Loubinoux et al., 2013; Ahmad et al., 2009; Cohen-Poradosu et al., 2004; Tseng et al., 2010; Sunaoshi et al., 2010; Vähäkuopus et al., 2012). Two studies attempted to link certain emm-types to prognosis and found that the most prevalent type, StG6792 (Takahashi et al., 2011), or uncommon types (Rantala et al., 2010) were associated with poor outcome. The distribution of SD emm-types in invasive and non-invasive infections has also been compared indicating StG6, StG480, and StG485 (Jensen and Kilian, 2012), StG10 (Pinho et al., 2006), or StG485 (Sunaoshi et al., 2010) to be ⁎ Corresponding author. Tel.: +46-462220720; fax: +46-46157756. E-mail address: [email protected] (M. Rasmussen).
more common in invasive infections. Other studies could not link certain SD emm-types to whether the site of isolation was sterile or nonsterile (Takahashi et al., 2011; Brandt and Spellerberg, 2009; Rantala, 2014; Loubinoux et al., 2013; Tseng et al., 2010; Lo and Cheng, 2015). Variations in circulating emm-types in different populations could explain these findings. Here we investigate the correlation between site of isolation, SDgroup, and SD emm-type. Isolates from wound and throat swabs were collected prospectively during two 1-month periods in 2008 and 2011 respectively at the department for Clinical Microbiology in Lund. Isolates from blood from 1st of January 2008 to 31st of December 2011 were collected retrospectively through database searches in the same laboratory. The identification of the bacteria had been made by typical appearance on blood agar and latex agglutination (Streptex, Remel, Lenexa, KS, USA) and the bacteria were stored at −80 °C. The bacteria were re-cultured on blood agar in 5% CO2 at 37 °C over night and using the standard direct transfer method samples were subjected to identification with an Ultraflextreme MALDI-TOF MS (Bruker Daltonics, Bremen, Germany), using the MALDI Biotyper version 3.1 with the BDAL5627 Database. A score above 2.0 was required for species determination. Statistical analyses were performed using the Prism 6 software. 262 isolates of GCS and GGS were identified and speciated. The species of the S. equi and S. canis isolates was confirmed by the sequence of the 16S rRNA gene (Cherkaoui et al., 2011; Sonesson et al., 2004). The patients with GCS or GGS bacteremia were significantly older and more likely to be male than patients with the same bacteria isolated from throat or wound. The results are summarized in Table 1. S. equi is a zoonotic pathogen transmitted to humans through animal contacts or through contaminated food (Nicholson et al., 2000; Edwards et al.,
http://dx.doi.org/10.1016/j.diagmicrobio.2016.09.008 0732-8893/© 2016 Elsevier Inc. All rights reserved.
Please cite this article as: Trell K, et al, Species and emm-type distribution of group C and G streptococci from different sites of isolation, Diagn Microbiol Infect Dis (2016), http://dx.doi.org/10.1016/j.diagmicrobio.2016.09.008
2
K. Trell et al. / Diagnostic Microbiology and Infectious Disease xxx (2016) xxx–xxx
Table 1 Site of isolation, group, species of bacteria and demographics of patients Site of isolation
Group
Species
Age (median)
Gender (% female)
Blood
GCS (n = 30) GGS (n = 86) GCS (n = 39) GGS (n = 41) GCS (n = 10) GGS (n = 56)
SD (n = 24), S. equi (n = 6) SD (n = 86) SD (n = 38), S. equi (n = 1) SD (n = 41) SD (n = 10) SD (n = 53), S. canis (n = 3)
61 73 19 23 44 60
27% 31% 56% 54% 38% 39%
Throat Wound
1988; Bordes-Benítez et al., 2006), but we found no temporal clustering of the S. equi isolates, speaking against an outbreak. All isolates were subjected to emm-typing as described (http://www.cdc.gov/streplab) and results are summarized in Fig. 1. From the S. equi, the S. canis and from three SD isolates of GCS from blood, no PCR product was obtained. The emm-type-distribution is different between GCS and GGS (Fig. 1a). Among GCS isolates, StG62647 is dominant and comprises 54% of all isolates while StC36 and StC1400 are also prevalent. Isolates of GGS are more diverse and the four most prevalent types were StG6 (20%), StG643 (20%), StG485 (14%), and StG480 (8%). StG6, StG485, and StG480 have been reported to be common by others (Takahashi et al., 2011; Rantala et al., 2010; Broyles et al., 2009; Loubinoux et al., 2013; Ahmad et al., 2009; Cohen-Poradosu et al., 2004; Tseng et al., 2010), whereas StG643 has only been reported to be prevalent previously in Norway (Oppegaard et al., 2015). A variety of other types were retrieved in lower numbers among GGS isolates (Fig. 1a). The association between certain SD emm-types and the group carbohydrate has usually not been stressed but has been noted previously by Pinho et al. and by Jensen et al. though both these studies were smaller than our present report (Jensen and Kilian, 2012; Pinho et al., 2006). The GCS isolates from blood were more often StG62647 whereas GCS isolates of
emm-types StC36 and StC1400 were common among throat isolates (Fig. 1b). The difference in type distribution between the different isolation sites was statistically significant using the χ 2 test (p = 0.001). For GGS isolates, StG6 was more common in blood than in throat isolates and StG652 was more common in wound isolates as compared to in blood isolates (Fig. 1C). However, the differences were not statistically significant (p = 0.06 with χ 2 test). The type distribution of GGS blood isolates during the time period is shown in Fig. 1D. Most types are represented during all years but the StG6 type dominated in 2010. Differences in emm-type-distribution were thus small and taken together with results from previous studies it is obvious that SD emm-type is not the sole factor that determines which type of infection a given bacterium will cause. The patient medical records were studied (with approval by the Regional ethical committee (no 2013/31)) demonstrating that none of the patients with GCS bacteremia succumbed, whereas 10 (12%) of the patient with GGS bacteremia died within 28 days. We could not find a statistically significant association with a particular SD emm-type and deaths. The mortalities were recorded in three cases infected with StG643, two cases with StG485, and one case each infected with StG6, StG480, StC74a, StG2078, and StG4831.
Fig. 1. In A, the type-distribution of GGS (black bars) and GCS (gray bars) expressed as proportion of total isolates (n = 183 for GGS and n = 73 for GCS) is shown. B shows the type distribution of GCS isolates from blood (black bars), skin (light gray bars), and throat (dark gray bars). In C, the type-distribution of GGS isolated from blood (black bars), skin (light gray bars), and throat (dark gray bars) is given. D depicts the number of GGS blood isolates per year of types StG6 (③), StG643 (⓿), StG480 (⑤), StG485 (⑩), StC74a (➊), and other types (④).
Please cite this article as: Trell K, et al, Species and emm-type distribution of group C and G streptococci from different sites of isolation, Diagn Microbiol Infect Dis (2016), http://dx.doi.org/10.1016/j.diagmicrobio.2016.09.008
K. Trell et al. / Diagnostic Microbiology and Infectious Disease xxx (2016) xxx–xxx
Conflicting Interests The authors have no conflicting interests to declare.
Acknowledgements This work was supported by the Swedish Government Fund for Clinical Research (ALF), the Royal Physiographic Society in Lund, and the foundations of Marianne and Marcus Wallenberg, Crafoord, and Österlund. The excellent technical assistance by Mrs. Gisela Hovold and the important advice by Dr. Malin Inghammar is acknowledged.
References Ahmad Y, Gertz RE, Li Z, Sakota V, Broyles LN, Van Beneden C, et al. Genetic relationships deduced from emm and multilocus sequence typing of invasive Streptococcus dysgalactiae subsp. equisimilis and S. canis recovered from isolates collected in the United States. J Clin Microbiol 2009;47:2046–54. Bläckberg A, Trell K, Rasmussen M. Erysipelas, a large retrospective study of aetiology and clinical presentation. BMC Infect Dis 2015;15:402. Bordes-Benítez A, Sánchez-Oñoro M, Suárez-Bordón P, García-Rojas AJ, Saéz-Nieto JA, González-García A, et al. Outbreak of Streptococcus equi subsp. zooepidemicus infections on the island of Gran Canaria associated with the consumption of inadequately pasteurized cheese. Eur J Clin Microbiol Infect Dis 2006;25:242–6. Bramhachari PV, Kaul SY, McMillan DJ, Shaila MS, Karmarkar MG, Sriprakash KS. Disease burden due to Streptococcus dysgalactiae subsp. equisimilis (group G and C streptococcus) is higher than that due to Streptococcus pyogenes among Mumbai school children. J Med Microbiol 2010;59:220–3. Brandt CM, Spellerberg B. Human infections due to Streptococcus dysgalactiae subspecies equisimilis. Clin Infect Dis 2009;49:766–72. Broyles LN, Van Beneden C, Beall B, Facklam R, Shewmaker PL, Malpiedi P, et al. Population-based study of invasive disease due to beta-hemolytic streptococci of groups other than A and B. Clin Infect Dis 2009;48:706–12. Cherkaoui A, Emonet S, Fernandez J, Schorderet D, Schrenzel J. Evaluation of matrixassisted laser desorption ionization-time of flight mass spectrometry for rapid identification of Beta-hemolytic streptococci. J Clin Microbiol 2011;49:3004–5. Cohen-Poradosu R, Jaffe J, Lavi D, Grisariu-Greenzaid S, Nir-Paz R, Valinsky L, et al. Group G streptococcal bacteremia in Jerusalem. Emerg Infect Dis 2004;10:1455–60. Edwards AT, Roulson M, Ironside MJ. A milk-borne outbreak of serious infection due to Streptococcus zooepidemicus (Lancefield Group C). Epidemiol Infect 1988;101:43–51.
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Jensen A, Kilian M. Delineation of Streptococcus dysgalactiae, its subspecies, and its clinical and phylogenetic relationship to Streptococcus pyogenes. J Clin Microbiol 2012;50: 113–26. Lo H-H, Cheng W-S. Distribution of virulence factors and association with emm polymorphism or isolation site among beta-hemolytic group G Streptococcus dysgalactiae subspecies equisimilis. APMIS 2015;123:45–52. Loubinoux J, Plainvert C, Collobert G, Touak G, Bouvet A, Poyart C, et al. Adult invasive and noninvasive infections due to Streptococcus dysgalactiae subsp. equisimilis in France from 2006 to 2010. J Clin Microbiol 2013;51:2724–7. Nicholson ML, Ferdinand L, Sampson JS, Benin A, Balter S, Pinto SW, et al. Analysis of immunoreactivity to a Streptococcus equi subsp. zooepidemicus M-like protein To confirm an outbreak of poststreptococcal glomerulonephritis, and sequences of M-like proteins from isolates obtained from different host species. J Clin Microbiol 2000;38: 4126–30. Oppegaard O, Mylvaganam H, Kittang BR. Beta-haemolytic group A, C and G streptococcal infections in Western Norway: a 15-year retrospective survey. Clin Microbiol Infect 2015;21:171–8. Pinho MD, Melo-Cristino J, Ramirez M. Clonal relationships between invasive and noninvasive Lancefield group C and G streptococci and emm-specific differences in invasiveness. J Clin Microbiol 2006;44:841–6. Rantala S. Streptococcus dysgalactiae subsp. equisimilis bacteremia: an emerging infection. Eur J Clin Microbiol Infect Dis 2014;33:1303–10. Rantala S, Vuopio-Varkila J, Vuento R, Huhtala H, Syrjänen J. Clinical presentations and epidemiology of beta-haemolytic streptococcal bacteraemia: a population-based study. Clin Microbiol Infect 2009;15:286–8. Rantala S, Vahakuopus S, Vuopio-Varkila J, Vuento R, Syrjanen J. Streptococcus dysgalactiae subsp. equisimilis Bacteremia, Finland, 1995-2004. Emerg Infect Dis 2010;16:843–6. Sonesson A, Oqvist B, Hagstam P, Björkman-Burtscher IM, Miörner H, Petersson AC. An immunosuppressed patient with systemic vasculitis suffering from cerebral abscesses due to Nocardia farcinica identified by 16S rRNA gene universal PCR. Nephrol Dial Transplant 2004;19:2896–900. Sunaoshi K, Murayama SY, Adachi K, Yagoshi M, Okuzumi K, Chiba N, et al. Molecular emm genotyping and antibiotic susceptibility of Streptococcus dysgalactiae subsp. equisimilis isolated from invasive and non-invasive infections. J Med Microbiol 2010;59:82–8. Takahashi T, Ubukata K, Watanabe H. Invasive infection caused by Streptococcus dysgalactiae subsp. equisimilis: characteristics of strains and clinical features. J Infect Chemother 2011;17:1–10. Tseng S-P, Lin Y-Y, Tsai J-C, Hsueh P-R, Chen H-J, Hung W-C, et al. Distribution of emm types and genetic characterization of the mgc locus in group G Streptococcus dysgalactiae subsp. equisimilis from a hospital in northern Taiwan. J Clin Microbiol 2010;48:2975–7. Vähäkuopus S, Vuento R, Siljander T, Syrjänen J, Vuopio J. Distribution of emm types in invasive and non-invasive group A and G streptococci. Eur J Clin Microbiol Infect Dis 2012;31:1251–6.
Please cite this article as: Trell K, et al, Species and emm-type distribution of group C and G streptococci from different sites of isolation, Diagn Microbiol Infect Dis (2016), http://dx.doi.org/10.1016/j.diagmicrobio.2016.09.008
Contents lists available at ScienceDirect
Diagnostic Microbiology and Infectious Disease journal homepage: www.elsevier.com/locate/diagmicrobio
Note
Species and emm-type distribution of group C and G streptococci from different sites of isolation Kristina Trell a, Bo Nilson b,c, Magnus Rasmussen a,⁎ a b c
Division of Infection Medicine, Department of Clinical Sciences, Lund University, Lund, Sweden Department of Laboratory Medicine Lund, Section of Medical Microbiology, Lund University, Lund, Sweden Clinical Microbiology, Labmedicin, Region Skåne, Lund, Sweden
a r t i c l e
i n f o
Article history: Received 28 April 2016 Received in revised form 31 August 2016 Accepted 12 September 2016 Available online xxxx
a b s t r a c t beta-Haemolytic streptococci of groups C (GCS) and G (GGS) from human infections typically belong to Streptococcus dysgalactiae and are important human pathogens. Among GGS (183 isolates), several emm-types were identified without significant differences between different sites of isolation. For GCS (79 isolates), the typedistribution was markedly different and more restricted. © 2016 Elsevier Inc. All rights reserved.
Keywords: Streptococcus dysgalactiae Group G Streptococcus Group C Streptococcus
beta-Haemolytic streptococci of groups C and G (GCS and GGS), the majority of which are Streptococcus dysgalactiae subsp. Equisimilis (SDSE), have become increasingly recognized as causes of severe and invasive human infections (Takahashi et al., 2011; Brandt and Spellerberg, 2009; Rantala, 2014). SDSE cause a disease spectrum similar to that of Streptococcus pyogenes, including erysipelas (Bläckberg et al., 2015), wound infections (Rantala et al., 2009), and pharyngitis (Bramhachari et al., 2010). Species determination of GCS and GGS can be achieved using matrix-assisted laser desorption ionization - time of flight mass spectrometry (MALDI-TOF MS) (Rantala et al., 2010; Cherkaoui et al., 2011) and further typing could be based on the sequence of the emm gene, encoding the M protein (Brandt and Spellerberg, 2009; Jensen and Kilian, 2012). Although subspecies determination is not possible through these methods, previous studies have shown that the vast majority of human isolates of Streptococcus dysgalactiae (SD) are SDSE. Several studies have investigated the distribution of SD emm-types in invasive infections (Takahashi et al., 2011; Rantala et al., 2010; Pinho et al., 2006; Broyles et al., 2009; Loubinoux et al., 2013; Ahmad et al., 2009; Cohen-Poradosu et al., 2004; Tseng et al., 2010; Sunaoshi et al., 2010; Vähäkuopus et al., 2012). Two studies attempted to link certain emm-types to prognosis and found that the most prevalent type, StG6792 (Takahashi et al., 2011), or uncommon types (Rantala et al., 2010) were associated with poor outcome. The distribution of SD emm-types in invasive and non-invasive infections has also been compared indicating StG6, StG480, and StG485 (Jensen and Kilian, 2012), StG10 (Pinho et al., 2006), or StG485 (Sunaoshi et al., 2010) to be ⁎ Corresponding author. Tel.: +46-462220720; fax: +46-46157756. E-mail address: [email protected] (M. Rasmussen).
more common in invasive infections. Other studies could not link certain SD emm-types to whether the site of isolation was sterile or nonsterile (Takahashi et al., 2011; Brandt and Spellerberg, 2009; Rantala, 2014; Loubinoux et al., 2013; Tseng et al., 2010; Lo and Cheng, 2015). Variations in circulating emm-types in different populations could explain these findings. Here we investigate the correlation between site of isolation, SDgroup, and SD emm-type. Isolates from wound and throat swabs were collected prospectively during two 1-month periods in 2008 and 2011 respectively at the department for Clinical Microbiology in Lund. Isolates from blood from 1st of January 2008 to 31st of December 2011 were collected retrospectively through database searches in the same laboratory. The identification of the bacteria had been made by typical appearance on blood agar and latex agglutination (Streptex, Remel, Lenexa, KS, USA) and the bacteria were stored at −80 °C. The bacteria were re-cultured on blood agar in 5% CO2 at 37 °C over night and using the standard direct transfer method samples were subjected to identification with an Ultraflextreme MALDI-TOF MS (Bruker Daltonics, Bremen, Germany), using the MALDI Biotyper version 3.1 with the BDAL5627 Database. A score above 2.0 was required for species determination. Statistical analyses were performed using the Prism 6 software. 262 isolates of GCS and GGS were identified and speciated. The species of the S. equi and S. canis isolates was confirmed by the sequence of the 16S rRNA gene (Cherkaoui et al., 2011; Sonesson et al., 2004). The patients with GCS or GGS bacteremia were significantly older and more likely to be male than patients with the same bacteria isolated from throat or wound. The results are summarized in Table 1. S. equi is a zoonotic pathogen transmitted to humans through animal contacts or through contaminated food (Nicholson et al., 2000; Edwards et al.,
http://dx.doi.org/10.1016/j.diagmicrobio.2016.09.008 0732-8893/© 2016 Elsevier Inc. All rights reserved.
Please cite this article as: Trell K, et al, Species and emm-type distribution of group C and G streptococci from different sites of isolation, Diagn Microbiol Infect Dis (2016), http://dx.doi.org/10.1016/j.diagmicrobio.2016.09.008
2
K. Trell et al. / Diagnostic Microbiology and Infectious Disease xxx (2016) xxx–xxx
Table 1 Site of isolation, group, species of bacteria and demographics of patients Site of isolation
Group
Species
Age (median)
Gender (% female)
Blood
GCS (n = 30) GGS (n = 86) GCS (n = 39) GGS (n = 41) GCS (n = 10) GGS (n = 56)
SD (n = 24), S. equi (n = 6) SD (n = 86) SD (n = 38), S. equi (n = 1) SD (n = 41) SD (n = 10) SD (n = 53), S. canis (n = 3)
61 73 19 23 44 60
27% 31% 56% 54% 38% 39%
Throat Wound
1988; Bordes-Benítez et al., 2006), but we found no temporal clustering of the S. equi isolates, speaking against an outbreak. All isolates were subjected to emm-typing as described (http://www.cdc.gov/streplab) and results are summarized in Fig. 1. From the S. equi, the S. canis and from three SD isolates of GCS from blood, no PCR product was obtained. The emm-type-distribution is different between GCS and GGS (Fig. 1a). Among GCS isolates, StG62647 is dominant and comprises 54% of all isolates while StC36 and StC1400 are also prevalent. Isolates of GGS are more diverse and the four most prevalent types were StG6 (20%), StG643 (20%), StG485 (14%), and StG480 (8%). StG6, StG485, and StG480 have been reported to be common by others (Takahashi et al., 2011; Rantala et al., 2010; Broyles et al., 2009; Loubinoux et al., 2013; Ahmad et al., 2009; Cohen-Poradosu et al., 2004; Tseng et al., 2010), whereas StG643 has only been reported to be prevalent previously in Norway (Oppegaard et al., 2015). A variety of other types were retrieved in lower numbers among GGS isolates (Fig. 1a). The association between certain SD emm-types and the group carbohydrate has usually not been stressed but has been noted previously by Pinho et al. and by Jensen et al. though both these studies were smaller than our present report (Jensen and Kilian, 2012; Pinho et al., 2006). The GCS isolates from blood were more often StG62647 whereas GCS isolates of
emm-types StC36 and StC1400 were common among throat isolates (Fig. 1b). The difference in type distribution between the different isolation sites was statistically significant using the χ 2 test (p = 0.001). For GGS isolates, StG6 was more common in blood than in throat isolates and StG652 was more common in wound isolates as compared to in blood isolates (Fig. 1C). However, the differences were not statistically significant (p = 0.06 with χ 2 test). The type distribution of GGS blood isolates during the time period is shown in Fig. 1D. Most types are represented during all years but the StG6 type dominated in 2010. Differences in emm-type-distribution were thus small and taken together with results from previous studies it is obvious that SD emm-type is not the sole factor that determines which type of infection a given bacterium will cause. The patient medical records were studied (with approval by the Regional ethical committee (no 2013/31)) demonstrating that none of the patients with GCS bacteremia succumbed, whereas 10 (12%) of the patient with GGS bacteremia died within 28 days. We could not find a statistically significant association with a particular SD emm-type and deaths. The mortalities were recorded in three cases infected with StG643, two cases with StG485, and one case each infected with StG6, StG480, StC74a, StG2078, and StG4831.
Fig. 1. In A, the type-distribution of GGS (black bars) and GCS (gray bars) expressed as proportion of total isolates (n = 183 for GGS and n = 73 for GCS) is shown. B shows the type distribution of GCS isolates from blood (black bars), skin (light gray bars), and throat (dark gray bars). In C, the type-distribution of GGS isolated from blood (black bars), skin (light gray bars), and throat (dark gray bars) is given. D depicts the number of GGS blood isolates per year of types StG6 (③), StG643 (⓿), StG480 (⑤), StG485 (⑩), StC74a (➊), and other types (④).
Please cite this article as: Trell K, et al, Species and emm-type distribution of group C and G streptococci from different sites of isolation, Diagn Microbiol Infect Dis (2016), http://dx.doi.org/10.1016/j.diagmicrobio.2016.09.008
K. Trell et al. / Diagnostic Microbiology and Infectious Disease xxx (2016) xxx–xxx
Conflicting Interests The authors have no conflicting interests to declare.
Acknowledgements This work was supported by the Swedish Government Fund for Clinical Research (ALF), the Royal Physiographic Society in Lund, and the foundations of Marianne and Marcus Wallenberg, Crafoord, and Österlund. The excellent technical assistance by Mrs. Gisela Hovold and the important advice by Dr. Malin Inghammar is acknowledged.
References Ahmad Y, Gertz RE, Li Z, Sakota V, Broyles LN, Van Beneden C, et al. Genetic relationships deduced from emm and multilocus sequence typing of invasive Streptococcus dysgalactiae subsp. equisimilis and S. canis recovered from isolates collected in the United States. J Clin Microbiol 2009;47:2046–54. Bläckberg A, Trell K, Rasmussen M. Erysipelas, a large retrospective study of aetiology and clinical presentation. BMC Infect Dis 2015;15:402. Bordes-Benítez A, Sánchez-Oñoro M, Suárez-Bordón P, García-Rojas AJ, Saéz-Nieto JA, González-García A, et al. Outbreak of Streptococcus equi subsp. zooepidemicus infections on the island of Gran Canaria associated with the consumption of inadequately pasteurized cheese. Eur J Clin Microbiol Infect Dis 2006;25:242–6. Bramhachari PV, Kaul SY, McMillan DJ, Shaila MS, Karmarkar MG, Sriprakash KS. Disease burden due to Streptococcus dysgalactiae subsp. equisimilis (group G and C streptococcus) is higher than that due to Streptococcus pyogenes among Mumbai school children. J Med Microbiol 2010;59:220–3. Brandt CM, Spellerberg B. Human infections due to Streptococcus dysgalactiae subspecies equisimilis. Clin Infect Dis 2009;49:766–72. Broyles LN, Van Beneden C, Beall B, Facklam R, Shewmaker PL, Malpiedi P, et al. Population-based study of invasive disease due to beta-hemolytic streptococci of groups other than A and B. Clin Infect Dis 2009;48:706–12. Cherkaoui A, Emonet S, Fernandez J, Schorderet D, Schrenzel J. Evaluation of matrixassisted laser desorption ionization-time of flight mass spectrometry for rapid identification of Beta-hemolytic streptococci. J Clin Microbiol 2011;49:3004–5. Cohen-Poradosu R, Jaffe J, Lavi D, Grisariu-Greenzaid S, Nir-Paz R, Valinsky L, et al. Group G streptococcal bacteremia in Jerusalem. Emerg Infect Dis 2004;10:1455–60. Edwards AT, Roulson M, Ironside MJ. A milk-borne outbreak of serious infection due to Streptococcus zooepidemicus (Lancefield Group C). Epidemiol Infect 1988;101:43–51.
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Please cite this article as: Trell K, et al, Species and emm-type distribution of group C and G streptococci from different sites of isolation, Diagn Microbiol Infect Dis (2016), http://dx.doi.org/10.1016/j.diagmicrobio.2016.09.008