Swiss Tropical and Public Health Institute , Allschwil, Switzerland.
University of Basel , Basel, Switzerland.
Appl Environ Microbiol. 2023 Sep 28;89(9):e0065823. doi: 10.1128/aem.00658-23. Epub 2023 Sep 1.
Antimicrobial resistance (AMR) is a critical global concern driven by the overuse, misuse, and/or usage of inadequate antibiotics on humans, animals' agriculture, and as a result of contaminated environments. This study is the first One Health survey in the Middle East that incorporated whole-genome sequencing (WGS) to examine the spread of AMR in spp. and spp. This cross-sectional study was conducted to examine the role of AMR at the human-animal-environmental interface and was performed in Ramallah/Al-Bireh and Jerusalem governorates of the central West Bank, Palestine. In 2021 and 2022, a total of 592 samples were collected and analyzed. From a total of 65 and 19 spp. isolates, DNA was extracted for WGS using Oxford Nanopore Technologies MinION platform. We found that the dominant serotypes of and were present in chicken manure, chicken meat sold in markets, and feces of asymptomatic farm workers, with high genetic similarities between the isolates regardless of origin. Additionally, our results showed rapid strain turnover in from the same sites between 2021 and 2022. Most of the positive spp. samples were multidrug-resistant (MDR) serovar Muenchen carrying the plasmid of emerging (pESI) megaplasmid, conferring resistance to multiple antibiotics. Our findings highlight the spread of MDR foodborne pathogens from animals to humans through the food chain, emphasizing the importance of a One Health approach that considers the interconnections between human, animal, and environmental health. IMPORTANCE Prior to this study, there existed hardly an integrated human-animal-environmental study of Salmonellosis and Campylobacteriosis and related AMR in Middle Eastern countries. The few existing studies lack robust epidemiological study designs, adequate for a One Health approach, and did not use WGS to determine the circulating serotypes and their AMR profiles. Civil unrest and war in Middle Eastern countries drive AMR because of the breakdown of public health and food security services. This study samples simultaneously humans, animals, and the environment to comprehensively investigate foodborne pathogens in the broiler chicken production chain in Palestine using WGS. We show that identical serotypes of and can be found in samples from chicken farms, chicken meat sold in markets, and asymptomatic broiler chicken production workers. The most striking feature is the rapid dynamic of change in the genetic profile of the detected species in the same sampling locations. The majority of positive spp. samples are MDR serovar Muenchen isolates carrying the pESI megaplasmid. The results demonstrate a close relationship between the serovar Muenchen isolates found in our sample collection and those responsible for 40% of all clinical spp. isolates in Israel as previously reported, with a sequence identity of over 99.9%. These findings suggest the transboundary spread of MDR serovar Muenchen strains from animals to humans through the food chain. The study underscores the importance of combining integrated One Health studies with WGS for detecting environmental-animal-human transmission of foodborne pathogens that could not be detected otherwise. This study showcases the benefits of integrated environmental-animal-human sampling and WGS for monitoring AMR. Environmental samples, which may be more accessible in conflict-torn places where monitoring systems are limited and regulations are weak, can provide an effective AMR surveillance solution. WGS of bacterial isolates provides causal inference of the distribution and spread of bacterial serotypes and AMR in complex social-ecological systems. Consequently, our results point toward the expected benefits of operationalizing a One Health approach through closer cooperation of public and animal health and food safety authorities.
抗微生物药物耐药性(AMR)是一个全球性的重大问题,主要是由于人类、动物农业和受污染环境中过度、不当使用或使用不足的抗生素造成的。本研究是中东地区首次采用全基因组测序(WGS)进行的一项“One Health”调查,旨在研究 spp. 和 spp. 中 AMR 的传播情况。这项横断面研究旨在检验人-动物-环境界面的 AMR 作用,并在巴勒斯坦西岸中部的拉马拉/伯利恒和耶路撒冷省进行。2021 年和 2022 年,共采集了 592 份样本并进行了分析。在总共 65 株 和 19 株 spp. 分离株中,使用牛津纳米孔技术 MinION 平台提取 DNA 进行 WGS。我们发现, 和 的主要血清型存在于鸡粪、市场上销售的鸡肉和无症状农场工人的粪便中,无论来源如何,分离株之间具有高度的遗传相似性。此外,我们的结果表明,2021 年至 2022 年间,来自同一地点的 分离株发生了快速的菌株更替。大多数阳性 spp. 样本是携带新兴 (pESI) 大型质粒的多药耐药(MDR)血清型 Muenchen 的 ,对多种抗生素具有耐药性。我们的研究结果强调了食源性病原体从动物传播到人类的途径,突出了采用“One Health”方法的重要性,该方法考虑了人类、动物和环境卫生之间的相互联系。
在此之前,中东国家几乎没有对沙门氏菌病和弯曲菌病及其相关 AMR 进行综合的人-动物-环境研究。少数现有的研究缺乏稳健的流行病学研究设计,不足以采用“One Health”方法,并且没有使用 WGS 来确定循环血清型及其 AMR 谱。中东国家的内乱和战争破坏了公共卫生和食品安全服务,推动了 AMR 的发展。本研究采用 WGS 同时对人类、动物和环境进行采样,全面调查巴勒斯坦肉鸡生产链中的食源性病原体。我们发现,来自鸡场、市场上销售的鸡肉和无症状肉鸡生产工人的样本中可以发现相同的血清型 和 。最引人注目的特征是在同一采样地点检测到的物种的遗传特征的快速动态变化。大多数阳性 spp. 样本是携带 pESI 大型质粒的 MDR 血清型 Muenchen 分离株。结果表明,我们样本中发现的 血清型 Muenchen 分离株与之前报道的以色列 40%的临床 spp. 分离株密切相关,其序列同一性超过 99.9%。这些发现表明,MDR 血清型 Muenchen 菌株通过食物链从动物传播到人类。该研究强调了将综合的“One Health”研究与 WGS 相结合,用于检测食源性病原体在环境-动物-人类之间的传播的重要性,这些传播途径是其他方法无法检测到的。本研究展示了综合环境-动物-人类采样和 WGS 用于监测 AMR 的益处。环境样本可能更容易获得,因为在监测系统有限且法规薄弱的冲突地区,环境样本可能更容易获得,这些地区可能更容易获得。环境样本可能更容易获得,因为在监测系统有限且法规薄弱的冲突地区,环境样本可能更容易获得。环境样本可能更容易获得,因为在监测系统有限且法规薄弱的冲突地区,环境样本可能更容易获得。WGS 可以对细菌血清型和 AMR 在复杂的社会-生态系统中的分布和传播提供因果推断。因此,我们的研究结果表明,通过加强公共卫生和动物卫生以及食品安全当局之间的合作,实施“One Health”方法将预期带来益处。