Lee Soomin, An Jae-Uk, Woo JungHa, Song Hyokeun, Yi Saehah, Kim Woo-Hyun, Lee Ju-Hoon, Ryu Sangryeol, Cho Seongbeom
College of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National University, Seoul, South Korea.
Department of Food and Animal Biotechnology, Seoul National University, Seoul, South Korea.
Front Microbiol. 2022 May 6;13:873856. doi: 10.3389/fmicb.2022.873856. eCollection 2022.
Global spread of strains carrying the mobilized colistin resistance gene (MCR1-EC) poses serious threats to public health. Colistin has been generally prescribed for swine colibacillosis, having made swine farms as major reservoirs of MCR1-EC. The present study aimed to understand characteristic differences of MCR1-EC, including prevalence, antimicrobial resistance, and virulence, according to swine production stages. In addition, genetic relatedness was evaluated between MCR1-EC isolated from this study as well as pig-, human-, and chicken-derived strains published in the National Center for Biotechnology Information (NCBI), based on the multi-locus sequence types (MLSTs) and whole-genome sequences (WGS). Individual fecal samples ( = 331) were collected from asymptomatic weaning-piglets, growers, finishers, and sows from 10 farrow-to-finishing farms in South Korea between 2017 and 2019. The weighted prevalence of MCR1-EC was 11.6% (95% CI: 8.9%-15.0%, 55/331), with the highest prevalence at weaning stage. The 96.2% of MCR1-EC showed multi-drug resistance. Notably, weaning stage-derived MCR1-EC showed higher resistance rates (e.g., against extended-spectrum β-lactams or quinolones) than those from other stages. MCR1-EC with virulence advantages (e.g., intestinal/extraintestinal pathogenic or robust biofilm formation) were identified from all pig stages, accounting for nearly half of the total strains. WGS-based in-depth characterization showed that intestinal pathogenic MCR1-EC harbored multi-drug resistance and multiple virulence factors, which were highly shared between strains isolated from pigs of different stages. The clonal distribution of MCR1-EC was shared within swine farms but rarely across farms. The major clonal type of MCR1-EC from swine farms and NCBI database was ST10-A. Core genomes of MCR1-EC isolated from individuals within closed environments (same farms or human hospitals) were highly shared (genetic distance < 0.01), suggesting a high probability of clonal expansion of MCR1-EC within closed environments such as livestock husbandry. To the best of our knowledge, this is the first study to analyze the differences in the characteristics and clonal distribution of MCR1-EC according to production stages in swine farms, an important reservoir of MCR1-EC. Our results highlight the need to establish MCR1-EC control plans in swine farms based on an in-depth understanding of MCR1-EC characteristics according to swine production stages, focusing especially on the weaning stages.
携带可移动黏菌素耐药基因(MCR1-EC)的菌株在全球范围内传播,对公众健康构成严重威胁。黏菌素通常被用于治疗猪大肠杆菌病,这使得养猪场成为MCR1-EC的主要储存库。本研究旨在了解MCR1-EC在猪不同生产阶段的特征差异,包括流行率、抗菌药物耐药性和毒力。此外,基于多位点序列类型(MLST)和全基因组序列(WGS),对本研究分离的MCR1-EC以及美国国立生物技术信息中心(NCBI)公布的猪源、人源和鸡源菌株之间的遗传相关性进行了评估。2017年至2019年期间,从韩国10个从产仔到育肥农场的无症状断奶仔猪、生长猪、育肥猪和母猪中采集了个体粪便样本(n = 331)。MCR1-EC的加权流行率为11.6%(95%CI:8.9%-15.0%,55/331),在断奶阶段流行率最高。96.2%的MCR1-EC表现出多重耐药性。值得注意的是,断奶阶段来源的MCR1-EC比其他阶段的MCR1-EC表现出更高的耐药率(如对超广谱β-内酰胺类或喹诺酮类药物)。在所有猪阶段均鉴定出具有毒力优势(如肠道/肠外致病性或强大的生物膜形成能力)的MCR1-EC,占总菌株的近一半。基于WGS的深入特征分析表明,肠道致病性MCR1-EC具有多重耐药性和多种毒力因子,这些在不同阶段猪分离的菌株之间高度共享。MCR1-EC的克隆分布在养猪场内是共享的,但很少在不同猪场之间共享。养猪场和NCBI数据库中MCR1-EC的主要克隆类型是ST10-A。在封闭环境(同一猪场或人类医院)中个体分离的MCR1-EC的核心基因组高度共享(遗传距离<0.01),这表明MCR1-EC在畜牧养殖等封闭环境中克隆扩增的可能性很高。据我们所知,这是第一项分析MCR1-EC在养猪场(MCR1-EC的重要储存库)不同生产阶段的特征和克隆分布差异的研究。我们的结果强调,需要在深入了解MCR1-EC根据猪生产阶段的特征的基础上,在养猪场制定MCR1-EC控制计划,尤其要关注断奶阶段。