Quinolone-resistant Escherichia coli at the interface between humans, poultry and their shared environment- a potential public health risk.

Mabel Kamweli Aworh, Jacob K P Kwaga, Rene S Hendriksen, Emmanuel C Okolocha, Erin Harrell, Siddhartha Thakur
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Abstract

Background: Commensal Escherichia coli residing in the guts of humans and animals are reservoirs of multidrug resistance (MDR) genes, including quinolone resistance genes, in humans and poultry. This study aimed to characterize quinolones resistance in E. coli recovered from poultry workers, chickens, and poultry farm/market environments in Abuja, Nigeria.

Methods: This was a cross-sectional study conducted between December 2018 and April 2019 comprising poultry workers, chickens and their poultry farm/market environments. This study characterized E. coli isolates from stool, faecal and environmental samples using antimicrobial susceptibility testing and whole-genome sequencing methods. Core-genome multilocus sequences-based phylogeny was used to determine the relatedness between quinolone-resistant E. coli isolates. Data were analyzed using descriptive statistics.

Results: Of 110 E. coli isolates, quinolone-resistant phenotypes were observed in 68.2% (n = 75) isolates. Whole-genome sequencing detected plasmid-mediated quinolone resistance (PMQR) genes in 63.6% (n = 70) isolates. The most prevalent PMQR gene detected in 56 of these 70 E. coli isolates was qnrS1, followed by qnrB19 in 14 isolates and aac(6')-lb-cr in two isolates. Fifteen ciprofloxacin and 19 nalidixic acid-resistant isolates respectively showed double mutations in the quinolone-resistance determining regions (QRDRs) of gyrA, with single or double mutations in parC, and a single mutation in parE. The most prevalent amino-acid substitutions observed were S83L + D87N in gyrA (46.5%, n = 20), S80I in parC (51.2%, n = 22) and S458A in parE (14%, n = 6). About 2.9% (2/70) of PMQR isolates were extended-spectrum beta-lactamase (ESBL) producers while 2.9% (2/70) had plasmid-mediated colistin resistance (PMCR) genes.

Conclusions: PMQR genes were prevalent in E. coli isolates recovered from healthy humans, chickens and poultry farm/market environments. PMCR genes (mcr-1.1) occurred in PMQR-positive isolates recovered from manure and drinking water originating from poultry farm/market environments. It was found that the gene encoding ESBL coexisted with qnrS-positive isolates of human and avian origin. Horizontal transfer of PMQR genes among E. coli isolates in the human-poultry-environment interface has public health implications for the spread of antimicrobial resistance. Relevant government agencies should enforce regulations to restrict the use of critically important antimicrobials in poultry production.

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人类、家禽及其共同环境界面上的耐奎诺酮大肠杆菌--潜在的公共卫生风险。
背景:居住在人类和动物肠道中的共生大肠杆菌是人类和家禽耐多药(MDR)基因(包括喹诺酮类药物耐药基因)的储存库。本研究旨在分析从尼日利亚阿布贾的家禽工人、鸡和家禽养殖场/市场环境中回收的大肠杆菌对喹诺酮类药物的耐药性:这是一项在 2018 年 12 月至 2019 年 4 月期间进行的横断面研究,研究对象包括家禽工人、鸡及其家禽养殖场/市场环境。本研究采用抗菌药敏感性测试和全基因组测序方法对粪便、粪便和环境样本中分离出的大肠杆菌进行了鉴定。采用基于核心基因组多焦点序列的系统进化来确定耐喹诺酮大肠杆菌分离物之间的亲缘关系。数据采用描述性统计方法进行分析:结果:在 110 个大肠杆菌分离株中,68.2%(n = 75)的分离株出现了耐喹诺酮表型。全基因组测序在 63.6%(n = 70)的分离物中检测到质粒介导的喹诺酮耐药性(PMQR)基因。在这 70 个大肠杆菌分离物中,56 个分离物中检测到的最普遍的 PMQR 基因是 qnrS1,其次是 14 个分离物中的 qnrB19 和 2 个分离物中的 aac(6')-lb-cr。分别有 15 个耐环丙沙星和 19 个耐萘啶酸的分离物在 gyrA 的喹诺酮抗性决定区(QRDRs)中出现双突变,在 parC 中出现单突变或双突变,在 parE 中出现单突变。观察到的最普遍的氨基酸替换是gyrA中的S83L + D87N(46.5%,n = 20)、parC中的S80I(51.2%,n = 22)和parE中的S458A(14%,n = 6)。约2.9%(2/70)的PMQR分离株是广谱β-内酰胺酶(ESBL)产生者,而2.9%(2/70)的分离株具有质粒介导的可乐定耐药(PMCR)基因:结论:从健康人、鸡和家禽养殖场/市场环境中分离出的大肠杆菌普遍存在 PMQR 基因。从家禽养殖场/市场环境的粪便和饮用水中分离出的 PMQR 阳性分离物含有 PMCR 基因(mcr-1.1)。研究发现,编码 ESBL 的基因与 qnrS 阳性的人源和禽源分离物共存。在人类-家禽-环境界面中,大肠杆菌分离物之间的 PMQR 基因水平转移对抗菌药耐药性的传播具有公共卫生影响。相关政府机构应执行法规,限制在家禽生产中使用至关重要的抗菌药物。
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