{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,30]],"date-time":"2026-10-30T00:29:22Z","timestamp":1793320162189,"version":"4.5.0"},"reference-count":36,"publisher":"Oxford University Press (OUP)","issue":"11","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2021,12,6]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:sec>\n                  <jats:title>Background<\/jats:title>\n                  <jats:p>Treatment of severe group A Streptococcus (GAS) infections requires timely and appropriate antibiotic therapy. We describe the epidemiology of antimicrobial-resistant invasive GAS (iGAS) infections in the United States (US).<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Methods<\/jats:title>\n                  <jats:p>We analyzed population-based iGAS surveillance data at 10 US sites from 2006 through 2017. Cases were defined as infection with GAS isolated from normally sterile sites or wounds in patients with necrotizing fasciitis or streptococcal toxic shock syndrome. GAS isolates were emm typed. Antimicrobial susceptibility was determined using broth microdilution or whole genome sequencing. We compared characteristics among patients infected with erythromycin-nonsusceptible (EryNS) and clindamycin-nonsusceptible (CliNS) strains to those with susceptible infections. We analyzed proportions of EryNS and CliNS among isolates by site, year, risk factors, and emm type.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Results<\/jats:title>\n                  <jats:p>Overall, 17 179 iGAS cases were reported; 14.5% were EryNS. Among isolates tested for both inducible and constitutive CliNS (2011\u20132017), 14.6% were CliNS. Most (99.8%) CliNS isolates were EryNS. Resistance was highest in 2017 (EryNS: 22.8%; CliNS: 22.0%). All isolates were susceptible to \u03b2-lactams. EryNS and CliNS infections were most frequent among persons aged 18\u201334 years and in persons residing in long-term care facilities, experiencing homelessness, incarcerated, or who injected drugs. Patterns varied by site. Patients with nonsusceptible infections were significantly less likely to die. The emm types with &amp;gt;30% EryNS or CliNS included types 77, 58, 11, 83, and 92.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Conclusions<\/jats:title>\n                  <jats:p>Increasing prevalence of EryNS and CliNS iGAS infections in the US is predominantly due to expansion of several emm types. Clinicians should consider local resistance patterns when treating iGAS infections.<\/jats:p>\n               <\/jats:sec>","DOI":"10.1093\/cid\/ciab575","type":"journal-article","created":{"date-parts":[[2021,6,24]],"date-time":"2021-06-24T19:13:26Z","timestamp":1624562006000},"page":"1957-1964","source":"Crossref","is-referenced-by-count":72,"title":["Patterns of Antibiotic Nonsusceptibility Among Invasive Group A <i>Streptococcus<\/i> Infections\u2014United States, 2006\u20132017"],"prefix":"10.1093","volume":"73","author":[{"given":"Katherine","family":"Fay","sequence":"first","affiliation":[{"name":"Respiratory Diseases Branch, Centers for Disease Control and Prevention, Atlanta, Georgia, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jennifer","family":"Onukwube","sequence":"additional","affiliation":[{"name":"Respiratory Diseases Branch, Centers for Disease Control and Prevention, Atlanta, Georgia, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sopio","family":"Chochua","sequence":"additional","affiliation":[{"name":"Respiratory Diseases Branch, Centers for Disease Control and Prevention, Atlanta, Georgia, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"William","family":"Schaffner","sequence":"additional","affiliation":[{"name":"Vanderbilt University School of Medicine, Nashville, Tennessee, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paul","family":"Cieslak","sequence":"additional","affiliation":[{"name":"Public Health Division, Oregon Health Authority, Portland, Oregon, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ruth","family":"Lynfield","sequence":"additional","affiliation":[{"name":"Minnesota Department of Health, St Paul, Minnesota, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alison","family":"Muse","sequence":"additional","affiliation":[{"name":"Emerging Infections Program, New York State Department of Health, Rochester, New York, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chad","family":"Smelser","sequence":"additional","affiliation":[{"name":"New Mexico Department of Health, Santa Fe, New Mexico, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lee H","family":"Harrison","sequence":"additional","affiliation":[{"name":"Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Monica","family":"Farley","sequence":"additional","affiliation":[{"name":"Emerging Infections Program, Emory University, Atlanta, Georgia, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Susan","family":"Petit","sequence":"additional","affiliation":[{"name":"Connecticut Department of Public Health, Hartford, Connecticut, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nisha","family":"Alden","sequence":"additional","affiliation":[{"name":"Colorado Department of Public Health and Environment, Denver, Colorado, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mirasol","family":"Apostal","sequence":"additional","affiliation":[{"name":"Emerging Infections Program, Oakland, California, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paula","family":"Snippes Vagnone","sequence":"additional","affiliation":[{"name":"Minnesota Department of Health, St Paul, Minnesota, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Srinivas","family":"Nanduri","sequence":"additional","affiliation":[{"name":"Respiratory Diseases Branch, Centers for Disease Control and Prevention, Atlanta, Georgia, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bernard","family":"Beall","sequence":"additional","affiliation":[{"name":"Respiratory Diseases Branch, Centers for Disease Control and Prevention, Atlanta, Georgia, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chris A","family":"Van Beneden","sequence":"additional","affiliation":[{"name":"Respiratory Diseases Branch, Centers for Disease Control and Prevention, Atlanta, Georgia, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2021,6,25]]},"reference":[{"key":"2021121022485233600_CIT0001","author":"Centers for Disease Control and Prevention"},{"key":"2021121022485233600_CIT0002","doi-asserted-by":"crossref","first-page":"478","DOI":"10.1093\/cid\/ciw248","article-title":"Epidemiology of invasive group A streptococcal infections in the United States, 2005\u20132012","volume":"63","author":"Nelson","year":"2016","journal-title":"Clin Infect Dis"},{"key":"2021121022485233600_CIT0003","doi-asserted-by":"crossref","first-page":"1373","DOI":"10.1086\/497143","article-title":"Practice guidelines for the diagnosis and management of skin and soft-tissue infections","volume":"41","author":"Stevens","year":"2005","journal-title":"Clin Infect Dis"},{"key":"2021121022485233600_CIT0004","article-title":"Mechanisms of antibiotic resistance","volume-title":"Streptococcus pyogenes: basic biology to clinical manifestations","author":"Cattoir","year":"2016"},{"key":"2021121022485233600_CIT0005","doi-asserted-by":"crossref","first-page":"264","DOI":"10.1128\/CMR.00101-13","article-title":"Disease manifestations and pathogenic mechanisms of group A Streptococcus","volume":"27","author":"Walker","year":"2014","journal-title":"Clin Microbiol Rev"},{"key":"2021121022485233600_CIT0006","doi-asserted-by":"crossref","first-page":"1327","DOI":"10.1128\/AAC.01877-13","article-title":"Failure of clindamycin to eradicate infection with beta-hemolytic streptococci inducibly resistant to clindamycin in an animal model and in human infections","volume":"58","author":"Lewis","year":"2014","journal-title":"Antimicrob Agents Chemother"},{"key":"2021121022485233600_CIT0007","doi-asserted-by":"crossref","first-page":"e01422-17","DOI":"10.1128\/mBio.01422-17","article-title":"Population and whole genome sequence based characterization of invasive group A streptococci recovered in the United States during 2015","volume":"8","author":"Chochua","year":"2017","journal-title":"mBio"},{"key":"2021121022485233600_CIT0008","volume-title":"Performance standards for antimicrobial susceptibility testing; 25th informational supplement. CLSI document M100-S25","author":"Clinical and Laboratory Standards Institute","year":"2015"},{"key":"2021121022485233600_CIT0009","doi-asserted-by":"crossref","first-page":"1547","DOI":"10.3389\/fmicb.2020.01547","article-title":"Genomic surveillance of Streptococcus pyogenes strains causing invasive disease, United States, 2016\u20132017","volume":"11","author":"Li","year":"2020","journal-title":"Front Microbiol"},{"key":"2021121022485233600_CIT0010","doi-asserted-by":"crossref","first-page":"2640","DOI":"10.1093\/jac\/dks261","article-title":"Identification of acquired antimicrobial resistance genes","volume":"67","author":"Zankari","year":"2012","journal-title":"J Antimicrob Chemother"},{"key":"2021121022485233600_CIT0011","doi-asserted-by":"crossref","first-page":"60.e9","DOI":"10.1016\/j.cmi.2015.08.027","article-title":"Strain features and distributions in pneumococci from children with invasive disease before and after 13-valent conjugate vaccine implementation in the USA","volume":"22","author":"Metcalf","year":"2016","journal-title":"Clin Microbiol Infect"},{"key":"2021121022485233600_CIT0012","doi-asserted-by":"crossref","first-page":"574.e7","DOI":"10.1016\/j.cmi.2017.02.021","article-title":"Short-read whole genome sequencing for determination of antimicrobial resistance mechanisms and capsular serotypes of current invasive Streptococcus agalactiae recovered in the USA","volume":"23","author":"Metcalf","year":"2017","journal-title":"Clin Microbiol Infect"},{"key":"2021121022485233600_CIT0013","doi-asserted-by":"crossref","first-page":"e00756","DOI":"10.1128\/mBio.00756-16","article-title":"Penicillin-binding protein transpeptidase signatures for tracking and predicting beta-lactam resistance levels in Streptococcus pneumoniae","volume":"7","author":"Li","year":"2016","journal-title":"mBio"},{"key":"2021121022485233600_CIT0014","doi-asserted-by":"crossref","first-page":"342","DOI":"10.1097\/INF.0000000000001442","article-title":"Macrolide and clindamycin resistance in group A streptococci isolated from children with pharyngitis","volume":"36","author":"DeMuri","year":"2017","journal-title":"Pediatr Infect Dis J"},{"key":"2021121022485233600_CIT0015","doi-asserted-by":"crossref","first-page":"599","DOI":"10.1086\/432473","article-title":"Macrolide-resistant Streptococcus pyogenes in the United States, 2002\u20132003","volume":"41","author":"Richter","year":"2005","journal-title":"Clin Infect Dis"},{"key":"2021121022485233600_CIT0016","doi-asserted-by":"crossref","first-page":"1794","DOI":"10.1086\/426025","article-title":"Community-based surveillance in the United States of macrolide-resistant pediatric pharyngeal group A streptococci during 3 respiratory disease seasons","volume":"39","author":"Tanz","year":"2004","journal-title":"Clin Infect Dis"},{"key":"2021121022485233600_CIT0017","doi-asserted-by":"crossref","first-page":"1240","DOI":"10.1093\/jac\/dkl101","article-title":"Multicentre surveillance of the prevalence and molecular epidemiology of macrolide resistance among pharyngeal isolates of group A streptococci in the USA","volume":"57","author":"Green","year":"2006","journal-title":"J Antimicrob Chemother"},{"key":"2021121022485233600_CIT0018","doi-asserted-by":"crossref","first-page":"e0137313","DOI":"10.1371\/journal.pone.0137313","article-title":"Antimicrobial susceptibility of invasive Streptococcus pyogenes isolates in Germany during 2003\u20132013","volume":"10","author":"Im\u00f6hl","year":"2015","journal-title":"PLoS One"},{"key":"2021121022485233600_CIT0019","doi-asserted-by":"crossref","first-page":"842","DOI":"10.1128\/JCM.01312-09","article-title":"Streptococcus pyogenes isolates causing severe infections in Norway in 2006 to 2007: emm types, multilocus sequence types, and superantigen profiles","volume":"48","author":"Meisal","year":"2010","journal-title":"J Clin Microbiol"},{"key":"2021121022485233600_CIT0020","doi-asserted-by":"crossref","first-page":"1229","DOI":"10.1007\/s10096-010-0989-9","article-title":"Epidemiology, outcome and emm types of invasive group A streptococcal infections in Finland","volume":"29","author":"Siljander","year":"2010","journal-title":"Eur J Clin Microbiol Infect Dis"},{"key":"2021121022485233600_CIT0021","doi-asserted-by":"crossref","first-page":"3975","DOI":"10.1128\/JCM.01163-06","article-title":"Group A streptococci from invasive-disease episodes in Poland are remarkably divergent at the molecular level","volume":"44","author":"Szczypa","year":"2006","journal-title":"J Clin Microbiol"},{"key":"2021121022485233600_CIT0022","doi-asserted-by":"crossref","first-page":"702","DOI":"10.1111\/j.1469-0691.2011.03624.x","article-title":"Invasive group A streptococcal infections in adults, France (2006\u20132010)","volume":"18","author":"Plainvert","year":"2012","journal-title":"Clin Microbiol Infect"},{"key":"2021121022485233600_CIT0023","doi-asserted-by":"crossref","first-page":"707","DOI":"10.1007\/s10096-011-1362-3","article-title":"Significant decline in the erythromycin resistance of group A Streptococcus isolates at a German paediatric tertiary care centre","volume":"31","author":"Farmand","year":"2012","journal-title":"Eur J Clin Microbiol Infect Dis"},{"key":"2021121022485233600_CIT0024","doi-asserted-by":"crossref","first-page":"1515","DOI":"10.3201\/eid1809.120049","article-title":"Antimicrobial drug use and macrolide-resistant Streptococcus pyogenes, Belgium","volume":"18","author":"Van Heirstraeten","year":"2012","journal-title":"Emerg Infect Dis"},{"key":"2021121022485233600_CIT0025","doi-asserted-by":"crossref","first-page":"615","DOI":"10.1586\/14787210.2015.1023292","article-title":"Macrolide-resistant Streptococcus pyogenes: prevalence and treatment strategies","volume":"13","author":"Silva-Costa","year":"2015","journal-title":"Expert Rev Anti Infect Ther"},{"key":"2021121022485233600_CIT0026","author":"Centers for Disease Control and Prevention"},{"key":"2021121022485233600_CIT0027","doi-asserted-by":"crossref","first-page":"909","DOI":"10.3201\/eid1906.121020","article-title":"Characteristics of group A Streptococcus strains circulating during scarlet fever epidemic, Beijing, China, 2011","volume":"19","author":"Yang","year":"2013","journal-title":"Emerg Infect Dis"},{"key":"2021121022485233600_CIT0028","doi-asserted-by":"crossref","first-page":"2131","DOI":"10.1007\/s10096-015-2462-2","article-title":"Epidemiology and emm types of invasive group A streptococcal infections in Finland, 2008-2013","volume":"34","author":"Smit","year":"2015","journal-title":"Eur J Clin Microbiol Infect Dis"},{"key":"2021121022485233600_CIT0029","first-page":"e000316","article-title":"Unexpected relationships between frequency of antimicrobial resistance, disease phenotype and emm type in group A Streptococcus","volume":"5","author":"Sanson","year":"2019","journal-title":"Microb Genom"},{"key":"2021121022485233600_CIT0030","doi-asserted-by":"crossref","first-page":"1325","DOI":"10.1093\/infdis\/jiu260","article-title":"A systematic and functional classification of Streptococcus pyogenes that serves as a new tool for molecular typing and vaccine development","volume":"210","author":"Sanderson-Smith","year":"2014","journal-title":"J Infect Dis"},{"key":"2021121022485233600_CIT0031","doi-asserted-by":"crossref","first-page":"694","DOI":"10.1093\/cid\/ciw807","article-title":"Seasonal, geographic, and temporal trends of emm clusters associated with invasive group A streptococcal infections in US multistate surveillance","volume":"64","author":"Smeesters","year":"2017","journal-title":"Clin Infect Dis"},{"key":"2021121022485233600_CIT0032","doi-asserted-by":"crossref","first-page":"1140","DOI":"10.1128\/AAC.01352-07","article-title":"Plasmid-borne erm(T) from invasive, macrolide-resistant Streptococcus pyogenes strains","volume":"52","author":"Woodbury","year":"2008","journal-title":"Antimicrob Agents Chemother"},{"key":"2021121022485233600_CIT0033","article-title":"Invasive group A streptococcal infections among people who inject drugs and people experiencing homelessness in the United States, 2010\u20132017 [manuscript published online ahead of print 17 June 2020]","author":"Valenciano","year":"2020","journal-title":"Clin Infect Dis"},{"key":"2021121022485233600_CIT0034","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1007\/s11606-008-0859-7","article-title":"Patterns and determinants of inappropriate antibiotic use in injection drug users","volume":"24","author":"Starrels","year":"2009","journal-title":"J Gen Intern Med"},{"key":"2021121022485233600_CIT0035","doi-asserted-by":"crossref","first-page":"997","DOI":"10.1007\/s11524-011-9589-y","article-title":"Prescription medication borrowing among adult patients at an urban medical center","volume":"88","author":"Ward","year":"2011","journal-title":"J Urban Health"},{"key":"2021121022485233600_CIT0036","first-page":"269","article-title":"Clindamycin affects group A Streptococcus virulence factors and improves clinical outcome","volume":"215","author":"Andreoni","year":"2017","journal-title":"J Infect Dis"}],"container-title":["Clinical Infectious Diseases"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/cid\/advance-article-pdf\/doi\/10.1093\/cid\/ciab575\/39541819\/ciab575.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/cid\/article-pdf\/73\/11\/1957\/41608061\/ciab575.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/cid\/article-pdf\/73\/11\/1957\/41608061\/ciab575.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,12,10]],"date-time":"2021-12-10T22:51:49Z","timestamp":1639176709000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/cid\/article\/73\/11\/1957\/6309497"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,6,25]]},"references-count":36,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2021,6,25]]},"published-print":{"date-parts":[[2021,12,6]]}},"URL":"https:\/\/doi.org\/10.1093\/cid\/ciab575","relation":{},"ISSN":["1058-4838","1537-6591"],"issn-type":[{"value":"1058-4838","type":"print"},{"value":"1537-6591","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2021,12,1]]},"published":{"date-parts":[[2021,6,25]]}}}