Molecular Epidemiology of Group A Streptococcus Isolated from Children in Beijing during 2011 to 2019

Abstract

Objective This study aimed to examine the characteristics of Group A Streptococcus (GAS) infection and identify the emm genotypes and the superantigen gene of GAS strains isolated from children from 2011 to 2019 in Tongzhou District, Beijing.

Methods Pharyngeal swab samples from children with scarlet fever or pharyngeal infection were collected and tested for GAS. In GAS isolates, emm genotypes and superantigen genes were identified. Logistic regression models were used to explore the correlations between demographic characteristics, clinical manifestations, and GAS infection.

Results In total, 172/1,214 (14.2%) GAS were isolated. The GAS infection rate in children with scarlet fever was 47.5%, higher than 8.5% in children with pharyngeal infection (p < 0.001). The risk of GAS infection was associated with oral mucosal congestion in children with scarlet fever, and older age, tonsillitis, and rash in children with pharyngeal infection. Seven emm genotypes were detected in 164 GAS isolated strains, of which emm12 and emm1 accounted for 47.0 and 46.3%, respectively. Among 112 GAS isolates, the top 5 detection rates of superantigen genes were speF 100.0%, speG 100.0%, speB 98.2%, speC 94.6%, and smeZ 82.1%. Higher proportions of speA, speJ, and speK were detected in emm1 isolates, while speH and speI were more common in emm12 isolates (p < 0.001).

Conclusion The changing predominant type expanded the knowledge of the circulating emm types, which should be considered in future vaccine development.

Keywords

Group A Streptococcus - genotype - superantigen - scarlet fever - pharyngeal disease

Data Availability

The original dataset presented in this study is included in the supplementary material, further inquiries can be directed to the corresponding authors.

Ethical Approval

The Peking University Institutional Review Board Office granted Ethical approval to carry out the study within its facilities (IRB00001052-19005). Written informed consent from the participants' legal guardian was not required and oral informed consent was given to participate in this study in accordance with the national legislation and the institutional requirements.

Authors' Contributions

Q-B.L. and F.C. conceived and designed the experiments, reviewed drafts of the paper, and approved the final draft. H-J.L. and T-T.W. collected and analyzed the data, prepared figures and tables, authored drafts of the paper, and approved the final draft. H-M.S., Y.C., M-L.T., L.Z., L.X., J.D., and G-F.Z. collected the data and performed the investigations. All authors have approved the final draft and agreed to the published version of the manuscript.

^* These authors contributed equally to this work and share the first authorship.

Publikationsverlauf

Eingereicht: 20. Oktober 2023

Angenommen: 22. April 2024

Artikel online veröffentlicht:
29. Mai 2024

• References

• 1 Ahmed MI, Saunders RV, Bandi S. Group A streptococcal infections in children. Curr Pediatr Rev 2021; 17 (01) 70-73
• 2 Ralph AP, Carapetis JR. Group A streptococcal diseases and their global burden. Curr Top Microbiol Immunol 2013; 368: 1-27
• 3 Carapetis JR, Steer AC, Mulholland EK, Weber M. The global burden of Group A streptococcal diseases. Lancet Infect Dis 2005; 5 (11) 685-694
• 4 Yang P, Peng X, Zhang D. et al. Characteristics of Group A Streptococcus strains circulating during scarlet fever epidemic, Beijing, China, 2011. Emerg Infect Dis 2013; 19 (06) 909-915
• 5 Peng X, Yang P, Wu S. et al [emm types of mutation in scarlet-fever-related group A streptococcal, among children in Beijing, 2011–2014]. Zhonghua Liu Xing Bing Xue Za Zhi 2015; 36 (12) 1397-1400
• 6 Smeesters PR, McMillan DJ, Sriprakash KS. The streptococcal M protein: a highly versatile molecule. Trends Microbiol 2010; 18 (06) 275-282
• 7 You Y, Peng X, Yang P, Wang Q, Zhang J. 8-year M type surveillance of Streptococcus pyogenes in China. Lancet Infect Dis 2020; 20 (01) 24-25
• 8 Emgård J, Bergsten H, McCormick JK. et al. MAIT cells are major contributors to the cytokine response in Group A streptococcal toxic shock syndrome. Proc Natl Acad Sci U S A 2019; 116 (51) 25923-25931
• 9 Tongzhou District People's Government of Beijing Municipality. Statistical Communiqué of Tongzhou on the National Economic and Social Development. Accessed December 2023 at: https://www.bjtzh.gov.cn/bjtz/xxfb/tjsj/tjsh.shtml
• 10 Chinese Ministry of Health. Diagnostic criteria for scarlet fever (WS282-2008). Accessed February 28, 2008 at http://www.nhc.gov.cn/wjw/s9491/200802/38805.shtml
• 11 Wu S, Peng X, Yang Z. et al. Estimated burden of Group A streptococcal pharyngitis among children in Beijing, China. BMC Infect Dis 2016; 16 (01) 452
• 12 Mei-juan Z, Ying K, Jie Y, Hong-bo J, Ying L. Pathogenic surveillance of scarlet fever in Shunyi District, Beijing from 2012 to 2019. J Med Inf 2022; 35 (04) 146-149
• 13 Li H, Zhou L, Zhao Y. et al. Epidemiological analysis of Group A Streptococcus infections in a hospital in Beijing, China. Eur J Clin Microbiol Infect Dis 2020; 39 (12) 2361-2371
• 14 Nelson GE, Pondo T, Toews KA. et al. Epidemiology of invasive Group A streptococcal infections in the United States, 2005–2012. Clin Infect Dis 2016; 63 (04) 478-486
• 15 Lambertsen LM, Ingels H, Schønheyder HC, Hoffmann S. Danish Streptococcal Surveillance Collaboration Group 2011. Nationwide laboratory-based surveillance of invasive beta-haemolytic streptococci in Denmark from 2005 to 2011. Clin Microbiol Infect 2014; 20 (04) O216-O223
• 16 Darenberg J, Luca-Harari B, Jasir A. et al. Molecular and clinical characteristics of invasive Group A streptococcal infection in Sweden. Clin Infect Dis 2007; 45 (04) 450-458
• 17 Chalker V, Jironkin A, Coelho J. et al. Scarlet Fever Incident Management Team. Genome analysis following a national increase in scarlet fever in England 2014. BMC Genomics 2017; 18 (01) 224
• 18 Brouwer S, Rivera-Hernandez T, Curren BF. et al. Pathogenesis, epidemiology and control of Group A Streptococcus infection. Nat Rev Microbiol 2023; 21 (07) 431-447
• 19 Commons RJ, Smeesters PR, Proft T, Fraser JD, Robins-Browne R, Curtis N. Streptococcal superantigens: categorization and clinical associations. Trends Mol Med 2014; 20 (01) 48-62
• 20 Reglinski M, Sriskandan S, Turner CE. Identification of two new core chromosome-encoded superantigens in Streptococcus pyogenes; speQ and speR. J Infect 2019; 78 (05) 358-363
• 21 Ma CN, Peng XM, Wu SS. et al. [Study on the super-antigen genes of Group A Streptococcus pyogenes strains isolated from patients with scarlet fever and pharyngeal infection, in Beijing, 2015–2017]. Zhonghua Liu Xing Bing Xue Za Zhi 2018; 39 (10) 1375-1380
• 22 Li H, Zhou L, Zhao Y, Ma L, Liu X, Hu J. Molecular epidemiology and antimicrobial resistance of Group A Streptococcus recovered from patients in Beijing, China. BMC Infect Dis 2020; 20 (01) 507
• 23 Proft T, Webb PD, Handley V, Fraser JD. Two novel superantigens found in both Group A and Group C Streptococcus . Infect Immun 2003; 71 (03) 1361-1369
• 24 Castro SA, Dorfmueller HC. A brief review on Group A Streptococcus pathogenesis and vaccine development. R Soc Open Sci 2021; 8 (03) 201991
• 25 Friães A, Pinto FR, Silva-Costa C, Ramirez M, Melo-Cristino J. Superantigen gene complement of Streptococcus pyogenes–relationship with other typing methods and short-term stability. Eur J Clin Microbiol Infect Dis 2013; 32 (01) 115-125
• 26 Berman HF, Tartof SY, Reis JN, Reis MG, Riley LW. Distribution of superantigens in Group A streptococcal isolates from Salvador, Brazil. BMC Infect Dis 2014; 14: 294