{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,28]],"date-time":"2026-05-28T00:17:55Z","timestamp":1779927475145,"version":"3.53.1"},"reference-count":37,"publisher":"Springer Science and Business Media LLC","issue":"12","license":[{"start":{"date-parts":[[2020,7,16]],"date-time":"2020-07-16T00:00:00Z","timestamp":1594857600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.springer.com\/tdm"},{"start":{"date-parts":[[2020,7,16]],"date-time":"2020-07-16T00:00:00Z","timestamp":1594857600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/www.springer.com\/tdm"}],"funder":[{"name":"Research Foundation of Capital Institute of Pediatrics","award":["QN-2016-09"],"award-info":[{"award-number":["QN-2016-09"]}]},{"name":"Research Foundation of Capital Institute of Pediatrics","award":["PY-2020-05"],"award-info":[{"award-number":["PY-2020-05"]}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Eur J Clin Microbiol Infect Dis"],"published-print":{"date-parts":[[2020,12]]},"DOI":"10.1007\/s10096-020-03987-5","type":"journal-article","created":{"date-parts":[[2020,7,16]],"date-time":"2020-07-16T20:02:36Z","timestamp":1594929756000},"page":"2361-2371","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":10,"title":["Epidemiological analysis of Group A Streptococcus infections in a hospital in Beijing, China"],"prefix":"10.1007","volume":"39","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-9377-722X","authenticated-orcid":false,"given":"Hongxin","family":"Li","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lin","family":"Zhou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yong","family":"Zhao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lijuan","family":"Ma","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jing","family":"Xu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yan","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qin","family":"Qin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jin","family":"Hu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaoyan","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2020,7,16]]},"reference":[{"issue":"3","key":"3987_CR1","doi-asserted-by":"publisher","first-page":"470","DOI":"10.1128\/CMR.13.3.470","volume":"13","author":"MW Cunningham","year":"2000","unstructured":"Cunningham MW (2000) Pathogenesis of group A streptococcal infections. Clin Microbiol Rev 13(3):470\u2013511","journal-title":"Clin Microbiol Rev"},{"issue":"2","key":"3987_CR2","doi-asserted-by":"publisher","first-page":"264","DOI":"10.1128\/CMR.00101-13","volume":"27","author":"MJ Walker","year":"2014","unstructured":"Walker MJ, Barnett TC, McArthur JD, Cole JN, Gillen CM, Henningham A, Sriprakash KS, Sanderson-Smith ML, Nizet V (2014) Disease manifestations and pathogenic mechanisms of Group A Streptococcus. Clin Microbiol Rev 27(2):264\u2013301","journal-title":"Clin Microbiol Rev"},{"key":"3987_CR3","doi-asserted-by":"publisher","first-page":"1156","DOI":"10.3389\/fmicb.2017.01156","volume":"8","author":"M Chen","year":"2017","unstructured":"Chen M, Wang W, Tu L, Zheng Y, Pan H, Wang G, Chen Y, Zhang X, Zhu L, Chen J (2017) An emm5 Group A streptococcal outbreak among workers in a factory manufacturing telephone accessories. Front Microbiol 8:1156","journal-title":"Front Microbiol"},{"issue":"1","key":"3987_CR4","doi-asserted-by":"publisher","first-page":"452","DOI":"10.1186\/s12879-016-1775-9","volume":"16","author":"S Wu","year":"2016","unstructured":"Wu S, Peng X, Yang Z, Ma C, Zhang D, Wang Q, Yang P (2016) Estimated burden of group A streptococcal pharyngitis among children in Beijing, China. BMC Infect Dis 16(1):452","journal-title":"BMC Infect Dis"},{"issue":"12","key":"3987_CR5","doi-asserted-by":"publisher","first-page":"20749","DOI":"10.2807\/1560-7917.ES2014.19.12.20749","volume":"19","author":"R Guy","year":"2014","unstructured":"Guy R, Williams C, Irvine N, Reynolds A, Coelho J, Saliba V, Thomas D, Doherty L, Chalker V, von Wissmann B, Chand M, Efstratiou A, Ramsay M, Lamagni T (2014) Increase in scarlet fever notifications in the United Kingdom, 2013\/2014. Euro Surveill 19(12):20749","journal-title":"Euro Surveill"},{"issue":"10","key":"3987_CR6","doi-asserted-by":"publisher","first-page":"611","DOI":"10.1016\/S1473-3099(09)70178-1","volume":"9","author":"AC Steer","year":"2009","unstructured":"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(10):611\u2013616","journal-title":"Lancet Infect Dis"},{"issue":"1","key":"3987_CR7","doi-asserted-by":"publisher","first-page":"24","DOI":"10.1016\/S1473-3099(19)30694-2","volume":"20","author":"Y You","year":"2020","unstructured":"You Y, Peng X, Yang P, Wang Q, Zhang J (2020) 8-year M type surveillance of Streptococcus pyogenes in China. Lancet Infect Dis 20(1):24\u201325","journal-title":"Lancet Infect Dis"},{"issue":"17","key":"3987_CR8","doi-asserted-by":"publisher","first-page":"E1768","DOI":"10.1073\/pnas.1403138111","volume":"111","author":"W Nasser","year":"2014","unstructured":"Nasser W, Beres SB, Olsen RJ, Dean MA, Rice KA, Long SW, Kristinsson KG, Gottfredsson M, Vuopio J, Raisanen K, Caugant DA, Steinbakk M, Low DE, McGeer A, Darenberg J, Henriques-Normark B, Van Beneden CA, Hoffmann S, Musser JM (2014) Evolutionary pathway to increased virulence and epidemic group A Streptococcus disease derived from 3,615 genome sequences. Proc Natl Acad Sci U S A 111(17):E1768\u2013E1776","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"1","key":"3987_CR9","doi-asserted-by":"publisher","first-page":"84","DOI":"10.1038\/ng.3147","volume":"47","author":"MR Davies","year":"2015","unstructured":"Davies MR, Holden MT, Coupland P, Chen JH, Venturini C, Barnett TC, Zakour NL, Tse H, Dougan G, Yuen KY, Walker MJ (2015) Emergence of scarlet fever Streptococcus pyogenes emm12 clones in Hong Kong is associated with toxin acquisition and multidrug resistance. Nat Genet 47(1):84\u201387","journal-title":"Nat Genet"},{"issue":"1","key":"3987_CR10","doi-asserted-by":"publisher","first-page":"12","DOI":"10.1016\/j.biocel.2006.08.009","volume":"39","author":"S Sriskandan","year":"2007","unstructured":"Sriskandan S, Faulkner L, Hopkins P (2007) Streptococcus pyogenes: insight into the function of the streptococcal superantigens. Int J Biochem Cell Biol 39(1):12\u201319","journal-title":"Int J Biochem Cell Biol"},{"issue":"5","key":"3987_CR11","doi-asserted-by":"publisher","first-page":"358","DOI":"10.1016\/j.jinf.2019.02.005","volume":"78","author":"M Reglinski","year":"2019","unstructured":"Reglinski M, Sriskandan S, Turner CE (2019) Identification of two new core chromosome-encoded superantigens in Streptococcus pyogenes; speQ and speR. J Infect 78(5):358\u2013363","journal-title":"J Infect"},{"issue":"9","key":"3987_CR12","doi-asserted-by":"publisher","first-page":"668","DOI":"10.1080\/23744235.2019.1638964","volume":"51","author":"R Gergova","year":"2019","unstructured":"Gergova R, Muhtarova A, Mitov I, Setchanova L, Mihova K, Kaneva R, Markovska R (2019) Relation between emm types and virulence gene profiles among Bulgarian Streptococcus pyogenes clinical isolates. Infect Dis (Lond) 51(9):668\u2013675","journal-title":"Infect Dis (Lond)"},{"issue":"1","key":"3987_CR13","doi-asserted-by":"publisher","first-page":"181","DOI":"10.1186\/s12887-019-1536-1","volume":"19","author":"CZ Hua","year":"2019","unstructured":"Hua CZ, Yu H, Xu HM, Yang LH, Lin AW, Lyu Q, Lu HP, Xu ZW, Gao W, Chen XJ, Wang CQ, Jing CM (2019) A multi-center clinical investigation on invasive Streptococcus pyogenes infection in China, 2010\u20132017. BMC Pediatr 19(1):181","journal-title":"BMC Pediatr"},{"issue":"1","key":"3987_CR14","doi-asserted-by":"publisher","first-page":"18051","DOI":"10.1038\/s41598-019-54409-2","volume":"9","author":"A Friaes","year":"2019","unstructured":"Friaes A, Melo-Cristino J, Ramirez M (2019) Changes in emm types and superantigen gene content of Streptococcus pyogenes causing invasive infections in Portugal. Sci Rep 9(1):18051","journal-title":"Sci Rep"},{"key":"3987_CR15","first-page":"CD011571","volume":"3","author":"G Dupire","year":"2019","unstructured":"Dupire G, Droitcourt C, Hughes C, Le Cleach L (2019) Antistreptococcal interventions for guttate and chronic plaque psoriasis. Cochrane Database Syst Rev 3:CD011571","journal-title":"Cochrane Database Syst Rev"},{"issue":"8","key":"3987_CR16","doi-asserted-by":"publisher","first-page":"441","DOI":"10.1007\/s00403-008-0866-x","volume":"300","author":"L Nahary","year":"2008","unstructured":"Nahary L, Tamarkin A, Kayam N, Sela S, Fry L, Baker B, Powles A, Rogers S, Benhar I (2008) An investigation of antistreptococcal antibody responses in guttate psoriasis. Arch Dermatol Res 300(8):441\u2013449","journal-title":"Arch Dermatol Res"},{"key":"3987_CR17","doi-asserted-by":"publisher","first-page":"727","DOI":"10.1186\/s12879-014-0727-5","volume":"14","author":"AC Bowen","year":"2014","unstructured":"Bowen AC, Tong SY, Chatfield MD, Carapetis JR (2014) The microbiology of impetigo in indigenous children: associations between Streptococcus pyogenes, Staphylococcus aureus, scabies, and nasal carriage. BMC Infect Dis 14:727","journal-title":"BMC Infect Dis"},{"issue":"3","key":"3987_CR18","doi-asserted-by":"publisher","first-page":"295","DOI":"10.1097\/QCO.0000000000000262","volume":"29","author":"DE Bessen","year":"2016","unstructured":"Bessen DE (2016) Tissue tropisms in group A Streptococcus: what virulence factors distinguish pharyngitis from impetigo strains? Curr Opin Infect Dis 29(3):295\u2013303","journal-title":"Curr Opin Infect Dis"},{"issue":"1","key":"3987_CR19","doi-asserted-by":"publisher","first-page":"81","DOI":"10.4103\/ijmr.IJMR_1517_16","volume":"147","author":"N Bhardwaj","year":"2018","unstructured":"Bhardwaj N, Mathur P, Behera B, Mathur K, Kapil A, Misra MC (2018) Antimicrobial resistance in beta-haemolytic streptococci in India: a four-year study. Indian J Med Res 147(1):81\u201387","journal-title":"Indian J Med Res"},{"key":"3987_CR20","unstructured":"CLSI (2018) Performance standards for antimicrobial susceptibility testing. Clinical and Laboratory Standards Institute (CLSI), M100, 28th edition"},{"issue":"5","key":"3987_CR21","doi-asserted-by":"publisher","first-page":"402","DOI":"10.4161\/viru.2.5.16342","volume":"2","author":"D Metzgar","year":"2011","unstructured":"Metzgar D, Zampolli A (2011) The M protein of group A Streptococcus is a key virulence factor and a clinically relevant strain identification marker. Virulence 2(5):402\u2013412","journal-title":"Virulence"},{"issue":"7","key":"3987_CR22","doi-asserted-by":"publisher","first-page":"e0180757","DOI":"10.1371\/journal.pone.0180757","volume":"12","author":"M Imohl","year":"2017","unstructured":"Imohl M, Fitzner C, Perniciaro S, van der Linden M (2017) Epidemiology and distribution of 10 superantigens among invasive Streptococcus pyogenes disease in Germany from 2009 to 2014. PLoS One 12(7):e0180757","journal-title":"PLoS One"},{"key":"3987_CR23","doi-asserted-by":"publisher","first-page":"59","DOI":"10.3389\/fpubh.2018.00059","volume":"6","author":"G Gherardi","year":"2018","unstructured":"Gherardi G, Vitali LA, Creti R (2018) Prevalent emm types among invasive GAS in Europe and North America since year 2000. Front Public Health 6:59","journal-title":"Front Public Health"},{"key":"3987_CR24","doi-asserted-by":"publisher","unstructured":"Okabe T, Norose Y, Hida M, Takeda S, Takase M, Suzuki Y, Ohkuni H (2020) Changes over an 8-year period in Streptococcus pyogenes emm types in pharyngeal isolates from non-invasive infection patients at a pediatric facility[published online ahead of print, 2020 Jan 31]. J Nippon Med Sch.\u00a0https:\/\/doi.org\/10.1272\/jnms.JNMS.2020_87-502","DOI":"10.1272\/jnms.JNMS.2020_87-502"},{"key":"3987_CR25","doi-asserted-by":"publisher","first-page":"1052","DOI":"10.3389\/fmicb.2017.01052","volume":"8","author":"B Lu","year":"2017","unstructured":"Lu B, Fang Y, Fan Y, Chen X, Wang J, Zeng J, Li Y, Zhang Z, Huang L, Li H, Li D, Zhu F, Cui Y, Wang D (2017) High prevalence of macrolide-resistance and molecular characterization of Streptococcus pyogenes isolates circulating in China from 2009 to 2016. Front Microbiol 8:1052","journal-title":"Front Microbiol"},{"issue":"10","key":"3987_CR26","doi-asserted-by":"publisher","first-page":"1414","DOI":"10.1017\/S0950268809002118","volume":"137","author":"Y Ma","year":"2009","unstructured":"Ma Y, Yang Y, Huang M, Wang Y, Chen Y, Deng L, Yu S, Deng Q, Zhang H, Wang C, Liu L, Shen X (2009) Characterization of emm types and superantigens of Streptococcus pyogenes isolates from children during two sampling periods. Epidemiol Infect 137(10):1414\u20131419","journal-title":"Epidemiol Infect"},{"issue":"10","key":"3987_CR27","doi-asserted-by":"publisher","first-page":"1229","DOI":"10.1099\/jmm.0.000335","volume":"65","author":"DSJ Lindsay","year":"2016","unstructured":"Lindsay DSJ, Brown AW, Scott KJ, Denham B, Thom L, Rundell G, Ure R, Jones B, Smith AJ (2016) Circulating emm types of Streptococcus pyogenes in Scotland: 2011\u20132015. J Med Microbiol 65(10):1229\u20131231","journal-title":"J Med Microbiol"},{"key":"3987_CR28","doi-asserted-by":"crossref","unstructured":"Gonzalez-Abad MJ, Alonso Sanz M (2019) Invasive Streptococcus pyogenes infections (2011\u20132018): EMM-type and clinical presentation. An Pediatr (Barc) 92(6):351\u2013358","DOI":"10.1016\/j.anpede.2019.10.006"},{"issue":"6","key":"3987_CR29","doi-asserted-by":"publisher","first-page":"557","DOI":"10.1097\/INF.0000000000000677","volume":"34","author":"C d'Humieres","year":"2015","unstructured":"d'Humieres C, Bidet P, Levy C, Bechet S, Bonacorsi S, Bingen E, Cohen R (2015) Comparative epidemiology of Streptococcus pyogenes emm-types causing invasive and noninvasive infections in French children by use of high-resolution melting-polymerase chain reaction. Pediatr Infect Dis J 34(6):557\u2013561","journal-title":"Pediatr Infect Dis J"},{"issue":"5","key":"3987_CR30","doi-asserted-by":"publisher","first-page":"2880","DOI":"10.1128\/IAI.68.5.2880-2887.2000","volume":"68","author":"DA Scaramuzzino","year":"2000","unstructured":"Scaramuzzino DA, McNiff JM, Bessen DE (2000) Humanized in vivo model for streptococcal impetigo. Infect Immun 68(5):2880\u20132887","journal-title":"Infect Immun"},{"issue":"Suppl","key":"3987_CR31","doi-asserted-by":"publisher","first-page":"S13","DOI":"10.1016\/j.ijantimicag.2013.04.005","volume":"42","author":"A Norrby-Teglund","year":"2013","unstructured":"Norrby-Teglund A, Johansson L (2013) Beyond the traditional immune response: bacterial interaction with phagocytic cells. Int J Antimicrob Agents 42(Suppl):S13\u2013S16","journal-title":"Int J Antimicrob Agents"},{"issue":"5","key":"3987_CR32","doi-asserted-by":"publisher","first-page":"e1004155","DOI":"10.1371\/journal.ppat.1004155","volume":"10","author":"KJ Kasper","year":"2014","unstructured":"Kasper KJ, Zeppa JJ, Wakabayashi AT, Xu SX, Mazzuca DM, Welch I, Baroja ML, Kotb M, Cairns E, Cleary PP, Haeryfar SM, McCormick JK (2014) Bacterial superantigens promote acute nasopharyngeal infection by Streptococcus pyogenes in a human MHC Class II-dependent manner. PLoS Pathog 10(5):e1004155","journal-title":"PLoS Pathog"},{"issue":"3","key":"3987_CR33","doi-asserted-by":"publisher","first-page":"306","DOI":"10.1097\/INF.0000000000000088","volume":"33","author":"C Silva-Costa","year":"2014","unstructured":"Silva-Costa C, Carrico JA, Ramirez M, Melo-Cristino J (2014) Scarlet fever is caused by a limited number of Streptococcus pyogenes lineages and is associated with the exotoxin genes ssa, speA and speC. Pediatr Infect Dis J 33(3):306\u2013310","journal-title":"Pediatr Infect Dis J"},{"issue":"5","key":"3987_CR34","doi-asserted-by":"publisher","first-page":"859","DOI":"10.1007\/s10096-011-1385-9","volume":"31","author":"S Rantala","year":"2012","unstructured":"Rantala S, Vahakuopus S, Siljander T, Vuopio J, Huhtala H, Vuento R, Syrjanen J (2012) Streptococcus pyogenes bacteraemia, emm types and superantigen profiles. Eur J Clin Microbiol Infect Dis 31(5):859\u2013865","journal-title":"Eur J Clin Microbiol Infect Dis"},{"issue":"1","key":"3987_CR35","doi-asserted-by":"publisher","first-page":"256","DOI":"10.1128\/AAC.50.1.256-261.2006","volume":"50","author":"IN Grivea","year":"2006","unstructured":"Grivea IN, Al-Lahham A, Katopodis GD, Syrogiannopoulos GA, Reinert RR (2006) Resistance to erythromycin and telithromycin in Streptococcus pyogenes isolates obtained between 1999 and 2002 from Greek children with tonsillopharyngitis: phenotypic and genotypic analysis. Antimicrob Agents Chemother 50(1):256\u2013261","journal-title":"Antimicrob Agents Chemother"},{"issue":"2","key":"3987_CR36","doi-asserted-by":"publisher","first-page":"160","DOI":"10.1016\/j.jmii.2013.08.015","volume":"48","author":"PK Chuang","year":"2015","unstructured":"Chuang PK, Wang SM, Lin HC, Cho YH, Ma YJ, Ho TS, Shen CF, Liu CC (2015) The trend of macrolide resistance and emm types of group A streptococci from children at a medical center in southern Taiwan. J Microbiol Immunol Infect 48(2):160\u2013167","journal-title":"J Microbiol Immunol Infect"},{"key":"3987_CR37","doi-asserted-by":"crossref","unstructured":"Muhtarova A, Mihova K, Markovska R, Mitov I, Kaneva R, Gergova R (2019) Molecular emm typing of Bulgarian macrolide-resistant Streptococcus pyogenes isolates. Acta Microbiol Immunol Hung\u00a067(1): 14\u201317","DOI":"10.1556\/030.66.2019.033"}],"container-title":["European Journal of Clinical Microbiology &amp; Infectious Diseases"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s10096-020-03987-5.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s10096-020-03987-5\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s10096-020-03987-5.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,7,15]],"date-time":"2021-07-15T23:12:29Z","timestamp":1626390749000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s10096-020-03987-5"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,7,16]]},"references-count":37,"journal-issue":{"issue":"12","published-print":{"date-parts":[[2020,12]]}},"alternative-id":["3987"],"URL":"https:\/\/doi.org\/10.1007\/s10096-020-03987-5","relation":{},"ISSN":["0934-9723","1435-4373"],"issn-type":[{"value":"0934-9723","type":"print"},{"value":"1435-4373","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,7,16]]},"assertion":[{"value":"6 April 2020","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"6 July 2020","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"16 July 2020","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Compliance with ethical standards"}},{"value":"The authors declare that they have no conflicts of interest.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflicts of interest"}},{"value":"This study was approved by the ethics committee of the Capital Institute of Pediatrics. Written consent forms were obtained from the participants\u2019 guardians before collecting the pharyngeal swab samples, and anonymity of the participants was guaranteed.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicableDisclaimerThe study sponsors had no role in study design; collection, analysis, and interpretation of data; writing the report; or the decision to submit the report for publication.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}}]}}