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鸭养殖与屠宰肉中 bla 阳性大肠埃希菌的高流行率和传播:对食品安全的日益威胁。

High prevalence and transmission of bla-positive Escherichia coli between farmed ducks and slaughtered meats: An increasing threat to food safety.

机构信息

College of Veterinary Medicine, Qingdao Agricultural University, Qingdao 266109, China.

College of Veterinary Medicine, Qingdao Agricultural University, Qingdao 266109, China.

出版信息

Int J Food Microbiol. 2024 Nov 2;424:110850. doi: 10.1016/j.ijfoodmicro.2024.110850. Epub 2024 Jul 31.

Abstract

The emergence of carbapenem-resistant bacteria especially carbapenem-resistant Escherichia coli (CREC) in food animals poses a serious threat to food safety and public health. Reports about the dissemination of carbapenem-resistant bacteria along the food animal production chain are scattered and mainly focus on swine and chicken. Abuse of antibiotics in duck farms is common especially in China which has the largest duck production industry, however, the CREC transmission between farmed ducks and slaughtered meats remains unclear and the role of slaughterhouse in disseminating CREC among duck meats remains largely unknown. Herein, we collected 251 fecal samples from five typical duck farms along with 125 slaughtered meat samples (25 from each farm) in the corresponding slaughterhouse in Anhui Province, China, in December 2018. All samples were screened for CREC isolates which were analyzed for the presence of carbapenemase genes and colistin resistance gene mcr. The resistance profiles, transferability, pulsed-field gel electrophoresis (PFGE), whole-genome sequencing and phylogenetic analysis of the CREC isolates from both ducks and meats were further characterized. This is the first report presenting the high prevalence of bla-positive CREC isolates in ducks from duck farms (57.8 %) and slaughtered meats (33.6 %) in the corresponding slaughterhouse. Among the 203 bla-positive CREC isolates obtained in this study, 19.2 % harbored mcr-1 and all CREC isolates showed resistance to nearly all currently available antibiotics (except tigecycline). Of note, mcr-1 was found in 17.8 % of the meat-derived CREC carrying bla. Based on the PFGE analysis, clonal spread of bla-positive CREC including some also carrying mcr-1 was found between farmed ducks and slaughtered duck meats even from different farms. Special attention should be paid to the clonal dissemination of meat-derived CREC within the slaughterhouse, which contributed to the high prevalence of bla in slaughtered meats. Additionally, horizontal transmission mainly mediated by transferable bla-bearing IncX3 plasmids, untypable bla-bearing plasmids and mcr-1-bearing IncHI2 plasmids further facilitated the rapid spread of such multidrug-resistant strains. Notably, the bla-bearing plasmids and mcr-1-bearing plasmids in CREC from meats were highly similar to those from animals and humans. More worryingly, the phylogenomic analysis showed that CREC isolates from both ducks and corresponding meats clustered with previously reported human CREC isolates carrying mcr-1 in different geographical areas including China. These findings further prove that the CREC and resistance plasmids in farmed ducks could transmit to meats even from different farms via the slaughterhouse and then trigger infections in humans. The high prevalence and clonal transmission of CREC isolates including those also carrying mcr-1 between ducks and meats are alarming, and urgent control measures are required to reduce the dissemination of such organisms.

摘要

食源性耐碳青霉烯肠杆菌(CRE),尤其是耐碳青霉烯大肠埃希菌(CREC)的出现,对食品安全和公共卫生构成了严重威胁。关于食源性动物中耐碳青霉烯细菌传播的报告较为分散,主要集中在猪和鸡上。中国养鸭场滥用抗生素的现象很普遍,中国是世界上最大的养鸭国,然而,养殖鸭和屠宰鸭肉之间的 CREC 传播仍不清楚,屠宰场在传播鸭肉中的 CREC 方面的作用在很大程度上仍不清楚。在此,我们于 2018 年 12 月在安徽省五个典型的养鸭场收集了 251 份粪便样本,以及来自相应屠宰场的 125 份屠宰肉样本(每个农场 25 份)。所有样本均进行了 CREC 分离株的筛选,分析了碳青霉烯酶基因和粘菌素耐药基因 mcr 的存在情况。对来自鸭和肉的 CREC 分离株的耐药谱、可转移性、脉冲场凝胶电泳(PFGE)、全基因组测序和系统发育分析进行了进一步的特征描述。这是首次报道在相应屠宰场的鸭场(57.8%)和屠宰肉(33.6%)中发现 bla 阳性 CREC 分离株的高流行率。在本研究中获得的 203 株 bla 阳性 CREC 分离株中,19.2%携带 mcr-1,所有 CREC 分离株对目前几乎所有可用的抗生素均表现出耐药性(替加环素除外)。值得注意的是,在携带 bla 的肉源性 CREC 中发现了 17.8%的 mcr-1。基于 PFGE 分析,在养殖场鸭和屠宰鸭之间发现了 bla 阳性 CREC 的克隆传播,包括一些也携带 mcr-1。应特别注意屠宰场内肉源性 CREC 的克隆传播,这导致屠宰肉中 bla 的高流行率。此外,主要由可转移 bla 携带 IncX3 质粒、无法分型的 bla 携带质粒和 mcr-1 携带 IncHI2 质粒介导的水平传播,进一步促进了这些多药耐药株的快速传播。值得注意的是,来自肉类的 bla 携带质粒和 mcr-1 携带质粒与来自动物和人类的 CREC 分离株高度相似。更令人担忧的是,系统发育基因组分析表明,来自鸭和相应肉类的 bla 携带 CREC 分离株与来自不同地理区域的先前报道的携带 mcr-1 的人类 CREC 分离株聚集在一起,包括中国。这些发现进一步证明,养殖场鸭中的 CREC 和耐药质粒可以通过屠宰场传播到肉类,甚至来自不同农场的肉类,然后在人类中引发感染。鸭和肉之间 bla 阳性 CREC 分离株的高流行率和克隆传播,包括携带 mcr-1 的 CREC 分离株,令人震惊,需要采取紧急控制措施来减少这些生物的传播。

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