Reshaping the battlefield: A decade of clonal wars among Staphylococcus aureus in China

IF 15.8 1区医学 Q1 PHARMACOLOGY & PHARMACY Drug Resistance Updates Pub Date : 2025-01-01 DOI:10.1016/j.drup.2024.101178

Wangxiao Zhou , Ye Jin , Pan Chen , Qi Ge , Xu Dong , Yunbo Chen , Minghua Jiang , Yonghong Xiao

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Abstract

Background

Long-term comprehensive studies on the genomic epidemiology of both methicillin-resistant Staphylococcus aureus (MRSA) and methicillin-susceptible S. aureus (MSSA) isolates are limited in China. Here, we aimed to assess the genomic epidemiological characteristics and population dynamics of S. aureus in China.

Methods

We performed whole-genome sequencing and resistance phenotyping on 3848 S. aureus isolates from bloodstream infections across 72 hospitals in 22 provinces, from 2011 to 2020 in China. We explored the dynamic trends in the resistance/virulence genes and mobile genetic element profiles across lineages, and conducted time-scaled phylogenetic investigation for prevalent lineages.

Findings

The results revealed 315 different sequence types (STs) among all strains, 205 of which were novel. Significant shifts in MRSA population structure were observed, with ST59 replacing ST239 as the dominant lineage, exhibiting widespread inter-hospital transmission and increasing lineage diversity. In contrast, the composition of predominant MSSA lineages, ST188 (11.21 %), ST7 (9.79 %), ST22 (9.10 %), ST5 (8.56 %) and ST398 (7.91 %), remained relatively stable over time, with the diversity among MSSA strains consistently preserved at the population level. Phylogenetic reconstruction showed that ST59, ST398, ST22 and ST188 MSSA could evolve into corresponding MRSA lineages through the acquisition of staphylococcal cassette chromosome mec (SCCmec) elements. Moreover, the distribution patterns of resistance and virulence genes closely correlated with different lineages, where the proportion of PVL⁺ isolates in MRSA is rising. Concurrently, changes in the MRSA population structure led to an overall decrease in the number of resistance and virulence genes, significantly increased antimicrobial sensitivity.

Interpretation

The shifting genomic landscape of S. aureus in China underscores the need for tailored antimicrobial stewardship and enhances understanding of its epidemiological trends over the past decade.

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重塑战场：中国金黄色葡萄球菌之间的十年克隆战争。

背景：国内对耐甲氧西林金黄色葡萄球菌（MRSA）和耐甲氧西林金黄色葡萄球菌（MSSA）基因组流行病学的长期综合研究有限。在此，我们旨在评估金黄色葡萄球菌在中国的基因组流行病学特征和种群动态。方法：我们对2011年至2020年中国22个省72家医院血液感染的3848株金黄色葡萄球菌进行了全基因组测序和耐药表型分析。我们探索了抗性/毒力基因和可移动遗传元件在不同谱系中的动态变化趋势，并对流行谱系进行了时间尺度的系统发育研究。结果：在所有菌株中发现315个不同的序列类型（STs），其中205个为新序列类型。MRSA群体结构发生了显著变化，ST59取代ST239成为优势谱系，表现出广泛的医院间传播和谱系多样性的增加。相比之下，MSSA优势系ST188（11.21 %）、ST7（9.79 %）、ST22（9.10 %）、ST5（8.56 %）和ST398（7.91 %）的组成随时间的推移保持相对稳定，菌株间的多样性在种群水平上保持一致。系统发育重建显示，ST59、ST398、ST22和ST188 MSSA均可通过获取葡萄球菌盒式染色体mec （SCCmec）元件进化为相应的MRSA谱系。此外，耐药和毒力基因的分布模式与不同谱系密切相关，其中PVL+分离株在MRSA中的比例呈上升趋势。同时，MRSA种群结构的变化导致耐药和毒力基因数量总体减少，抗菌敏感性显著提高。解读：中国金黄色葡萄球菌基因组格局的变化强调了量身定制抗菌药物管理的必要性，并加强了对过去十年其流行病学趋势的了解。

本文章由计算机程序翻译，如有差异，请以英文原文为准。

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来源期刊

Drug Resistance Updates 医学-药学

CiteScore

26.20

自引率

11.90%

发文量

审稿时长

29 days

期刊介绍： Drug Resistance Updates serves as a platform for publishing original research, commentary, and expert reviews on significant advancements in drug resistance related to infectious diseases and cancer. It encompasses diverse disciplines such as molecular biology, biochemistry, cell biology, pharmacology, microbiology, preclinical therapeutics, oncology, and clinical medicine. The journal addresses both basic research and clinical aspects of drug resistance, providing insights into novel drugs and strategies to overcome resistance. Original research articles are welcomed, and review articles are authored by leaders in the field by invitation. Articles are written by leaders in the field, in response to an invitation from the Editors, and are peer-reviewed prior to publication. Articles are clear, readable, and up-to-date, suitable for a multidisciplinary readership and include schematic diagrams and other illustrations conveying the major points of the article. The goal is to highlight recent areas of growth and put them in perspective. *Expert reviews in clinical and basic drug resistance research in oncology and infectious disease *Describes emerging technologies and therapies, particularly those that overcome drug resistance *Emphasises common themes in microbial and cancer research