Genomic epidemiology and longitudinal sampling of ward wastewater environments and patients reveals complexity of the transmission dynamics of bla KPC-carbapenemase-producing Enterobacterales in a hospital setting.

IF 3.7 Q2 INFECTIOUS DISEASES JAC-Antimicrobial Resistance Pub Date : 2024-09-03 eCollection Date: 2024-10-01 DOI:10.1093/jacamr/dlae140
N Stoesser, R George, Z Aiken, H T T Phan, S Lipworth, T P Quan, A J Mathers, N De Maio, A C Seale, D W Eyre, A Vaughan, J Swann, T E A Peto, D W Crook, J Cawthorne, A Dodgson, A S Walker
{"title":"Genomic epidemiology and longitudinal sampling of ward wastewater environments and patients reveals complexity of the transmission dynamics of <i>bla</i> <sub>KPC</sub>-carbapenemase-producing Enterobacterales in a hospital setting.","authors":"N Stoesser, R George, Z Aiken, H T T Phan, S Lipworth, T P Quan, A J Mathers, N De Maio, A C Seale, D W Eyre, A Vaughan, J Swann, T E A Peto, D W Crook, J Cawthorne, A Dodgson, A S Walker","doi":"10.1093/jacamr/dlae140","DOIUrl":null,"url":null,"abstract":"<p><strong>Background: </strong>Healthcare-associated wastewater and asymptomatic patient reservoirs colonized by carbapenemase-producing Enterobacterales (CPE) contribute to nosocomial CPE dissemination, but the characteristics and dynamics of this remain unclear.</p><p><strong>Methods: </strong>We systematically sampled wastewater sites (<i>n</i> = 4488 samples; 349 sites) and patients (<i>n</i> = 1247) across six wards over 6-12 months to understand bla<sub>KPC</sub>-associated CPE (KPC-E) diversity within these reservoirs and transmission in a healthcare setting. Up to five KPC-E-positive isolates per sample were sequenced (Illumina). Recombination-adjusted phylogenies were used to define genetically related strains; assembly and mapping-based approaches were used to characterize antimicrobial resistance genes, insertion sequences (ISs) and Tn<i>4401</i> types/target site sequences. The accessory genome was evaluated in some of the largest clusters, and those crossing reservoirs.</p><p><strong>Results: </strong>Wastewater site KPC-E-positivity was substantial [101/349 sites (28.9%); 228/5601 (4.1%) patients cultured]. Thirteen KPC-E species and 109 strains were identified using genomics, and 24% of wastewater and 26% of patient KPC-E-positive samples harboured one or more strains. Most diversity was explained by the individual niche, suggesting localized factors are important in selection and spread. Tn<i>4401</i> + flanking target site sequence diversity was greater in wastewater sites (<i>P</i> < 0.001), which might favour Tn<i>4401</i>-associated transposition/evolution. Shower/bath- and sluice/mop-associated sites were more likely to be KPC-E-positive (adjusted OR = 2.69; 95% CI: 1.44-5.01; <i>P</i> = 0.0019; and adjusted OR = 2.60; 95% CI: 1.04-6.52; <i>P</i> = 0.0410, respectively). Different strains had different bla<sub>KPC</sub> dissemination dynamics.</p><p><strong>Conclusions: </strong>We identified substantial and diverse KPC-E colonization of wastewater sites and patients in this hospital setting. Reservoir and niche-specific factors (e.g. microbial interactions, selection pressures), and different strains and mobile genetic elements likely affect transmission dynamics. This should be considered in surveillance and control strategies.</p>","PeriodicalId":14594,"journal":{"name":"JAC-Antimicrobial Resistance","volume":"6 5","pages":"dlae140"},"PeriodicalIF":3.7000,"publicationDate":"2024-09-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11369815/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"JAC-Antimicrobial Resistance","FirstCategoryId":"1085","ListUrlMain":"https://doi.org/10.1093/jacamr/dlae140","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/10/1 0:00:00","PubModel":"eCollection","JCR":"Q2","JCRName":"INFECTIOUS DISEASES","Score":null,"Total":0}
引用次数: 0

Abstract

Background: Healthcare-associated wastewater and asymptomatic patient reservoirs colonized by carbapenemase-producing Enterobacterales (CPE) contribute to nosocomial CPE dissemination, but the characteristics and dynamics of this remain unclear.

Methods: We systematically sampled wastewater sites (n = 4488 samples; 349 sites) and patients (n = 1247) across six wards over 6-12 months to understand blaKPC-associated CPE (KPC-E) diversity within these reservoirs and transmission in a healthcare setting. Up to five KPC-E-positive isolates per sample were sequenced (Illumina). Recombination-adjusted phylogenies were used to define genetically related strains; assembly and mapping-based approaches were used to characterize antimicrobial resistance genes, insertion sequences (ISs) and Tn4401 types/target site sequences. The accessory genome was evaluated in some of the largest clusters, and those crossing reservoirs.

Results: Wastewater site KPC-E-positivity was substantial [101/349 sites (28.9%); 228/5601 (4.1%) patients cultured]. Thirteen KPC-E species and 109 strains were identified using genomics, and 24% of wastewater and 26% of patient KPC-E-positive samples harboured one or more strains. Most diversity was explained by the individual niche, suggesting localized factors are important in selection and spread. Tn4401 + flanking target site sequence diversity was greater in wastewater sites (P < 0.001), which might favour Tn4401-associated transposition/evolution. Shower/bath- and sluice/mop-associated sites were more likely to be KPC-E-positive (adjusted OR = 2.69; 95% CI: 1.44-5.01; P = 0.0019; and adjusted OR = 2.60; 95% CI: 1.04-6.52; P = 0.0410, respectively). Different strains had different blaKPC dissemination dynamics.

Conclusions: We identified substantial and diverse KPC-E colonization of wastewater sites and patients in this hospital setting. Reservoir and niche-specific factors (e.g. microbial interactions, selection pressures), and different strains and mobile genetic elements likely affect transmission dynamics. This should be considered in surveillance and control strategies.

查看原文
分享 分享
微信好友 朋友圈 QQ好友 复制链接
本刊更多论文
通过对病房废水环境和患者进行基因组流行病学和纵向采样,揭示了医院环境中产蓝 KPC-碳青霉烯酶肠杆菌传播动态的复杂性。
背景:产碳青霉烯酶肠杆菌(CPE)定植的医疗相关废水和无症状患者蓄水池导致了院内 CPE 的传播,但其特征和动态仍不清楚:我们在 6-12 个月内对 6 个病房的废水处理场所(349 个场所,4488 份样本)和患者(1247 人)进行了系统采样,以了解这些蓄水池中 blaKPC 相关 CPE(KPC-E)的多样性以及在医疗环境中的传播情况。每个样本最多可测序 5 个 KPC-E 阳性分离株(Illumina)。重组调整后的系统发生被用来定义基因相关的菌株;基于组装和映射的方法被用来描述抗菌药耐药性基因、插入序列 (IS) 和 Tn4401 类型/靶点序列。在一些最大的集群和跨越水库的集群中对附属基因组进行了评估:结果:污水点的 KPC-E 阳性率很高[101/349 个点(28.9%);228/5601(4.1%)名培养出的患者]。利用基因组学方法确定了 13 个 KPC-E 物种和 109 个菌株,24% 的废水和 26% 的患者 KPC-E 阳性样本中含有一个或多个菌株。大多数多样性是由个体生态位解释的,这表明局部因素在选择和传播中非常重要。Tn4401 + 侧翼目标位点序列多样性在废水位点中更为显著(与 P 4401 相关的转座/进化。淋浴/洗澡和水槽/拖把相关位点更有可能出现 KPC-E 阳性(调整 OR = 2.69;95% CI:1.44-5.01;P = 0.0019;调整 OR = 2.60;95% CI:1.04-6.52;P = 0.0410)。不同的菌株具有不同的 blaKPC 传播动态:我们发现在医院环境中,KPC-E 在废水处理场所和患者中的定植数量巨大且种类繁多。蓄水池和生态位特异性因素(如微生物相互作用、选择压力)以及不同菌株和移动遗传因子可能会影响传播动态。监测和控制策略应考虑到这一点。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 去求助
来源期刊
CiteScore
5.30
自引率
0.00%
发文量
0
审稿时长
16 weeks
期刊最新文献
Nursing home nurses' opinion profiles on the potential evolution of their role in antimicrobial stewardship and associated factors: a national cross-sectional study in France. Clinical pharmacist-led antifungal drug utilization reviews in cancer care hospital: a prospective audit and feedback. State of the art of real-life concentration monitoring of rifampicin and its implementation contextualized in resource-limited settings: the Tanzanian case. Capturing the complexity of veterinarians' antibiotic prescribing practices in the livestock sector: a meta-ethnography across contexts: Veterinarians' antibiotic prescribing in different contexts. Development of a PCR assay for rapid and accurate detection of an emerging vanB Enterococcus faecium clone in the Capital Region of Denmark.
×
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
现在去查看 取消
×
提示
确定
0
微信
客服QQ
Book学术公众号 扫码关注我们
反馈
×
意见反馈
请填写您的意见或建议
请填写您的手机或邮箱
已复制链接
已复制链接
快去分享给好友吧!
我知道了
×
扫码分享
扫码分享
Book学术官方微信
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术
文献互助 智能选刊 最新文献 互助须知 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 Book学术 All rights reserved.
ghs 京公网安备 11010802042870号 京ICP备2023020795号-1