荷兰 2009-2023 年带菌和侵袭性化脓性链球菌纵向监测背景下的全国侵袭性疾病激增:一项分子流行病学研究。

IF 6.1 2区 医学 Q1 MICROBIOLOGY
Journal of Clinical Microbiology Pub Date : 2024-10-16 Epub Date: 2024-08-28 DOI:10.1128/jcm.00766-24
Lidewij W Rümke, Matthew A Davies, Stefan M T Vestjens, Boas C L van der Putten, Wendy C M Bril-Keijzers, Marlies A van Houten, Nynke Y Rots, Alienke J Wijmenga-Monsuur, Arie van der Ende, Brechje de Gier, Bart J M Vlaminckx, Nina M van Sorge
{"title":"荷兰 2009-2023 年带菌和侵袭性化脓性链球菌纵向监测背景下的全国侵袭性疾病激增:一项分子流行病学研究。","authors":"Lidewij W Rümke, Matthew A Davies, Stefan M T Vestjens, Boas C L van der Putten, Wendy C M Bril-Keijzers, Marlies A van Houten, Nynke Y Rots, Alienke J Wijmenga-Monsuur, Arie van der Ende, Brechje de Gier, Bart J M Vlaminckx, Nina M van Sorge","doi":"10.1128/jcm.00766-24","DOIUrl":null,"url":null,"abstract":"<p><p>Since 2022, many countries have reported an upsurge in invasive group A streptococcal (iGAS) infections. We explored whether changes in <i>Streptococcus pyogenes</i> carriage rates or emergence of strains with potentially altered virulence, such as <i>emm</i>1 variants M1<sub>UK</sub> and M1<sub>DK</sub>, contributed to the 2022/2023 surge in the Netherlands. We determined <i>emm</i> (sub)type distribution for 2,698 invasive and 351 <i>S</i>. <i>pyogenes</i> carriage isolates collected between January 2009 and March 2023. Genetic evolution of <i>emm</i>1 was analyzed by whole-genome sequencing of 497 <i>emm</i>1 isolates. The nationwide iGAS upsurge coincided with a sharp increase of <i>emm</i>1.0 from 18% (18/100) of invasive isolates in Q1 2022 to 58% (388/670) in Q1 2023 (Fisher's exact test, <i>P</i> < 0.0001). M1<sub>UK</sub> became dominant among invasive <i>emm</i>1 isolates in 2016 and further expanded from 72% in Q1 2022 to 96% in Q1 2023. Phylogenetic comparison revealed evolution and clonal expansion of four new M1<sub>UK</sub> clades in 2022/2023. DNase Spd1 and superantigen SpeC were acquired in 9% (46/497) of <i>emm</i>1 isolates. <i>S. pyogenes</i> carriage rates and <i>emm</i>1 proportions in carriage isolates remained stable during this surge, and the expansion of M1<sub>UK</sub> in iGAS was not reflected in carriage isolates. During the 2022/2023 iGAS surge in the Netherlands, expansion of four new M1<sub>UK</sub> clades was observed among invasive isolates, but not carriage isolates, suggesting increased virulence and fitness of M1<sub>UK</sub> compared to contemporary M1 strains. The emergence of more virulent clades has important implications for public health strategies such as antibiotic prophylaxis for close contacts of iGAS patients.IMPORTANCEThis study describes the molecular epidemiology of invasive group A streptococcal (iGAS) infections in the Netherlands based on >3,000 <i>Streptococcus pyogenes</i> isolates from both asymptomatic carriers and iGAS patients collected before, during, and after the COVID-19 pandemic period (2009-2023) and is the first to assess whether changes in carriage rates or carried <i>emm</i> types contributed to the alarming post-COVID-19 upsurge in iGAS infections. We show that the 2022/2023 iGAS surge coincided with a sharp increase of <i>emm</i>1, particularly the toxicogenic M1<sub>UK</sub> variant, in invasive isolates, but not in carriage isolates. These findings suggest that increased virulence and fitness of M1<sub>UK</sub> likely contributes to an increased dissemination between hosts. The emergence of a more virulent and fit lineage has important implications for iGAS control interventions such as antibiotic prophylaxis for close contacts of iGAS patients and calls for a reappraisal of iGAS control interventions and guidelines.</p>","PeriodicalId":15511,"journal":{"name":"Journal of Clinical Microbiology","volume":null,"pages":null},"PeriodicalIF":6.1000,"publicationDate":"2024-10-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11481533/pdf/","citationCount":"0","resultStr":"{\"title\":\"Nationwide upsurge in invasive disease in the context of longitudinal surveillance of carriage and invasive <i>Streptococcus pyogenes</i> 2009-2023, the Netherlands: a molecular epidemiological study.\",\"authors\":\"Lidewij W Rümke, Matthew A Davies, Stefan M T Vestjens, Boas C L van der Putten, Wendy C M Bril-Keijzers, Marlies A van Houten, Nynke Y Rots, Alienke J Wijmenga-Monsuur, Arie van der Ende, Brechje de Gier, Bart J M Vlaminckx, Nina M van Sorge\",\"doi\":\"10.1128/jcm.00766-24\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>Since 2022, many countries have reported an upsurge in invasive group A streptococcal (iGAS) infections. We explored whether changes in <i>Streptococcus pyogenes</i> carriage rates or emergence of strains with potentially altered virulence, such as <i>emm</i>1 variants M1<sub>UK</sub> and M1<sub>DK</sub>, contributed to the 2022/2023 surge in the Netherlands. We determined <i>emm</i> (sub)type distribution for 2,698 invasive and 351 <i>S</i>. <i>pyogenes</i> carriage isolates collected between January 2009 and March 2023. Genetic evolution of <i>emm</i>1 was analyzed by whole-genome sequencing of 497 <i>emm</i>1 isolates. The nationwide iGAS upsurge coincided with a sharp increase of <i>emm</i>1.0 from 18% (18/100) of invasive isolates in Q1 2022 to 58% (388/670) in Q1 2023 (Fisher's exact test, <i>P</i> < 0.0001). M1<sub>UK</sub> became dominant among invasive <i>emm</i>1 isolates in 2016 and further expanded from 72% in Q1 2022 to 96% in Q1 2023. Phylogenetic comparison revealed evolution and clonal expansion of four new M1<sub>UK</sub> clades in 2022/2023. DNase Spd1 and superantigen SpeC were acquired in 9% (46/497) of <i>emm</i>1 isolates. <i>S. pyogenes</i> carriage rates and <i>emm</i>1 proportions in carriage isolates remained stable during this surge, and the expansion of M1<sub>UK</sub> in iGAS was not reflected in carriage isolates. During the 2022/2023 iGAS surge in the Netherlands, expansion of four new M1<sub>UK</sub> clades was observed among invasive isolates, but not carriage isolates, suggesting increased virulence and fitness of M1<sub>UK</sub> compared to contemporary M1 strains. The emergence of more virulent clades has important implications for public health strategies such as antibiotic prophylaxis for close contacts of iGAS patients.IMPORTANCEThis study describes the molecular epidemiology of invasive group A streptococcal (iGAS) infections in the Netherlands based on >3,000 <i>Streptococcus pyogenes</i> isolates from both asymptomatic carriers and iGAS patients collected before, during, and after the COVID-19 pandemic period (2009-2023) and is the first to assess whether changes in carriage rates or carried <i>emm</i> types contributed to the alarming post-COVID-19 upsurge in iGAS infections. We show that the 2022/2023 iGAS surge coincided with a sharp increase of <i>emm</i>1, particularly the toxicogenic M1<sub>UK</sub> variant, in invasive isolates, but not in carriage isolates. These findings suggest that increased virulence and fitness of M1<sub>UK</sub> likely contributes to an increased dissemination between hosts. The emergence of a more virulent and fit lineage has important implications for iGAS control interventions such as antibiotic prophylaxis for close contacts of iGAS patients and calls for a reappraisal of iGAS control interventions and guidelines.</p>\",\"PeriodicalId\":15511,\"journal\":{\"name\":\"Journal of Clinical Microbiology\",\"volume\":null,\"pages\":null},\"PeriodicalIF\":6.1000,\"publicationDate\":\"2024-10-16\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11481533/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Journal of Clinical Microbiology\",\"FirstCategoryId\":\"3\",\"ListUrlMain\":\"https://doi.org/10.1128/jcm.00766-24\",\"RegionNum\":2,\"RegionCategory\":\"医学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"2024/8/28 0:00:00\",\"PubModel\":\"Epub\",\"JCR\":\"Q1\",\"JCRName\":\"MICROBIOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of Clinical Microbiology","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1128/jcm.00766-24","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/8/28 0:00:00","PubModel":"Epub","JCR":"Q1","JCRName":"MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0

摘要

自 2022 年以来,许多国家都报告了侵袭性 A 群链球菌(iGAS)感染的激增。我们探讨了化脓性链球菌携带率的变化或emm1变种M1UK和M1DK等毒力可能改变的菌株的出现是否导致了荷兰2022/2023年的感染激增。我们确定了 2009 年 1 月至 2023 年 3 月间收集的 2,698 株侵入性和 351 株化脓性链球菌携带分离物的 emm(亚)型分布。通过对 497 例 emm1 分离物进行全基因组测序,分析了 emm1 的基因演变。在全国范围内iGAS激增的同时,emm1.0也从2022年第一季度占入侵分离株的18%(18/100)急剧增加到2023年第一季度的58%(388/670)(费雪精确检验,P < 0.0001)。2016 年,M1UK 在侵袭性 emm1 分离物中占主导地位,并从 2022 年第一季度的 72% 进一步扩大到 2023 年第一季度的 96%。系统发生学比较显示,2022/2023年有四个新的M1UK支系进化和克隆扩增。9%(46/497)的emm1分离株获得了DN酶Spd1和超抗原SpeC。在这一激增期间,化脓性链球菌的带菌率和带菌分离物中emm1的比例保持稳定,iGAS中M1UK的扩展并未反映在带菌分离物中。在荷兰 2022/2023 年 iGAS 激增期间,在侵入性分离物中观察到四个新的 M1UK 支系扩展,但在携带性分离物中没有观察到,这表明与当代 M1 菌株相比,M1UK 的毒力和适应性有所增强。毒性更强的支系的出现对公共卫生策略具有重要影响,如对 iGAS 患者的密切接触者进行抗生素预防。重要意义本研究描述了荷兰侵袭性 A 组链球菌(iGAS)感染的分子流行病学,其依据是 COVID-19 大流行期间(2009-2023 年)之前、期间和之后从无症状带菌者和 iGAS 患者中收集的超过 3000 份化脓性链球菌分离物。我们发现,2022/2023 年 iGAS 感染激增与侵袭性分离株中的 emm1(尤其是致毒的 M1UK 变体)急剧增加同时发生,但与携带分离株中的情况不同。这些研究结果表明,M1UK 的毒力和适应性增强很可能导致其在宿主之间的传播增加。毒性和适应性更强的品系的出现对iGAS控制干预措施(如对iGAS患者的密切接触者进行抗生素预防)具有重要影响,并要求对iGAS控制干预措施和指南进行重新评估。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
Nationwide upsurge in invasive disease in the context of longitudinal surveillance of carriage and invasive Streptococcus pyogenes 2009-2023, the Netherlands: a molecular epidemiological study.

Since 2022, many countries have reported an upsurge in invasive group A streptococcal (iGAS) infections. We explored whether changes in Streptococcus pyogenes carriage rates or emergence of strains with potentially altered virulence, such as emm1 variants M1UK and M1DK, contributed to the 2022/2023 surge in the Netherlands. We determined emm (sub)type distribution for 2,698 invasive and 351 S. pyogenes carriage isolates collected between January 2009 and March 2023. Genetic evolution of emm1 was analyzed by whole-genome sequencing of 497 emm1 isolates. The nationwide iGAS upsurge coincided with a sharp increase of emm1.0 from 18% (18/100) of invasive isolates in Q1 2022 to 58% (388/670) in Q1 2023 (Fisher's exact test, P < 0.0001). M1UK became dominant among invasive emm1 isolates in 2016 and further expanded from 72% in Q1 2022 to 96% in Q1 2023. Phylogenetic comparison revealed evolution and clonal expansion of four new M1UK clades in 2022/2023. DNase Spd1 and superantigen SpeC were acquired in 9% (46/497) of emm1 isolates. S. pyogenes carriage rates and emm1 proportions in carriage isolates remained stable during this surge, and the expansion of M1UK in iGAS was not reflected in carriage isolates. During the 2022/2023 iGAS surge in the Netherlands, expansion of four new M1UK clades was observed among invasive isolates, but not carriage isolates, suggesting increased virulence and fitness of M1UK compared to contemporary M1 strains. The emergence of more virulent clades has important implications for public health strategies such as antibiotic prophylaxis for close contacts of iGAS patients.IMPORTANCEThis study describes the molecular epidemiology of invasive group A streptococcal (iGAS) infections in the Netherlands based on >3,000 Streptococcus pyogenes isolates from both asymptomatic carriers and iGAS patients collected before, during, and after the COVID-19 pandemic period (2009-2023) and is the first to assess whether changes in carriage rates or carried emm types contributed to the alarming post-COVID-19 upsurge in iGAS infections. We show that the 2022/2023 iGAS surge coincided with a sharp increase of emm1, particularly the toxicogenic M1UK variant, in invasive isolates, but not in carriage isolates. These findings suggest that increased virulence and fitness of M1UK likely contributes to an increased dissemination between hosts. The emergence of a more virulent and fit lineage has important implications for iGAS control interventions such as antibiotic prophylaxis for close contacts of iGAS patients and calls for a reappraisal of iGAS control interventions and guidelines.

求助全文
通过发布文献求助,成功后即可免费获取论文全文。 去求助
来源期刊
Journal of Clinical Microbiology
Journal of Clinical Microbiology 医学-微生物学
CiteScore
17.10
自引率
4.30%
发文量
347
审稿时长
3 months
期刊介绍: The Journal of Clinical Microbiology® disseminates the latest research concerning the laboratory diagnosis of human and animal infections, along with the laboratory's role in epidemiology and the management of infectious diseases.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信