Paul G. Allen School for Global Health, Washington State University, Pullman, Washington, USA.
Laboratory of Data Discovery for Health Ltd, Hong Kong Science and Technology Park, Tai Po, Hong Kong, China.
Microbiol Spectr. 2024 Jun 4;12(6):e0395623. doi: 10.1128/spectrum.03956-23. Epub 2024 May 3.
Antimicrobial resistance (AMR) poses a significant threat to global health and sustainable development goals, especially in low- and middle-income countries (LMICs). This study aimed to understand the transmission of AMR between poultry, humans, and the environment in Bangladesh using a One Health approach. We analyzed the whole genome sequences (WGS) of 117 extended-spectrum β-lactamase-producing (ESBL-Ec) isolates, with 46 being carbapenem resistant. These isolates were obtained from human ( = 20) and poultry feces ( = 12), as well as proximal environments (wastewater) ( = 85) of three different study sites, including rural households ( = 48), rural poultry farms ( = 20), and urban wet markets ( = 49). The WGS of ESBL-Ec isolates were compared with 58 clinical isolates from global databases. No significant differences in antibiotic resistance genes (ARGs) were observed in ESBL-Ec isolated from humans with and without exposure to poultry. Environmental isolates showed higher ARG diversity than human and poultry isolates. No clonal transmission between poultry and human isolates was found, but wastewater was a reservoir for ESBL-Ec for both. Except for one human isolate, all ESBL-Ec isolates were distinct from clinical isolates. Most isolates (77.8%) carried at least one plasmid replicon type, with IncFII being the most prevalent. IncFIA was predominant in human isolates, while IncFII, Col(MG828), and p0111 were common in poultry. We observed putative sharing of ARG-carrying plasmids among isolates, mainly from wastewater. However, in most cases, bacterial isolates sharing plasmids were also clonally related, suggesting clonal spread was more probable than just plasmid transfer.
Our study underscores that wastewater discharged from households and wet markets carries antibiotic-resistant organisms from both human and animal sources. Thus, direct disposal of wastewater into the environment not only threatens human health but also endangers food safety by facilitating the spread of antimicrobial resistance (AMR) to surface water, crops, vegetables, and subsequently to food-producing animals. In regions with intensive poultry production heavily reliant on the prophylactic use of antibiotics, compounded by inadequate waste management systems, such as Bangladesh, the ramifications are particularly pronounced. Wastewater serves as a pivotal juncture for the dissemination of antibiotic-resistant organisms and functions as a pathway through which strains of human and animal origin can infiltrate the environment and potentially colonize new hosts. Further research is needed to thoroughly characterize wastewater isolates/populations and understand their potential impact on interconnected environments, communities, and wildlife.
抗生素耐药性(AMR)对全球健康和可持续发展目标构成重大威胁,特别是在低收入和中等收入国家(LMICs)。本研究旨在采用一种大健康方法了解孟加拉国家禽、人类和环境之间 AMR 的传播。我们分析了 117 株产extended-spectrum β-lactamase(ESBL-Ec)的全基因组序列(WGS),其中 46 株对碳青霉烯类耐药。这些分离株来自三个不同研究地点的人类(=20)和家禽粪便(=12)以及近环境(废水)(=85),包括农村家庭(=48)、农村家禽养殖场(=20)和城市湿市场(=49)。将 ESBL-Ec 分离株的 WGS 与来自全球数据库的 58 株临床分离株进行比较。在有和没有接触家禽的人类中,ESBL-Ec 分离株的抗生素耐药基因(ARGs)没有显著差异。环境分离株的 ARG 多样性高于人类和家禽分离株。未发现家禽和人类分离株之间存在克隆传播,但废水是两者的 ESBL-Ec 储库。除了一个人类分离株外,所有 ESBL-Ec 分离株都与临床分离株不同。大多数分离株(77.8%)携带至少一种质粒复制子类型,IncFII 是最常见的。IncFIA 主要存在于人类分离株中,而 IncFII、Col(MG828)和 p0111 在家禽中常见。我们观察到 ARG 携带质粒在分离株之间的潜在共享,主要来自废水。然而,在大多数情况下,共享质粒的细菌分离株也具有克隆关系,这表明克隆传播比仅仅质粒转移更有可能。
我们的研究强调,来自家庭和湿市场的废水不仅携带来自人类和动物来源的抗生素耐药生物,而且还通过将抗生素耐药性(AMR)传播到地表水、作物、蔬菜,随后传播到生产动物,从而直接威胁到人类健康,还危及食品安全。在严重依赖抗生素预防性使用且废物管理系统不充分的集约化家禽生产地区,例如孟加拉国,其影响尤其明显。废水是抗生素耐药生物传播的关键节点,也是人类和动物来源的菌株渗透环境并可能定植新宿主的途径。需要进一步研究以充分描述废水分离株/种群并了解它们对相互关联的环境、社区和野生动物的潜在影响。