PDF(Pubmed)
Abstract：
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 Campylobacter spp. and Salmonella 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 Campylobacter jejuni and 19 Salmonella spp. isolates, DNA was extracted for WGS using Oxford Nanopore Technologies MinION platform. We found that the dominant serotypes of C. jejuni and Salmonella enterica 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 C. jejuni from the same sites between 2021 and 2022. Most of the positive Salmonella spp. samples were multidrug-resistant (MDR) S. enterica serovar Muenchen carrying the plasmid of emerging S. infantis (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 C. jejuni and S. enterica 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 Salmonella spp. samples are MDR S. enterica serovar Muenchen isolates carrying the pESI megaplasmid. The results demonstrate a close relationship between the S. enterica serovar Muenchen isolates found in our sample collection and those responsible for 40% of all clinical Salmonella spp. isolates in Israel as previously reported, with a sequence identity of over 99.9%. These findings suggest the transboundary spread of MDR S. enterica 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.
摘要：
抗菌素耐药性(AMR)是由过度使用导致的一个关键的全球问题，误用，和/或对人类使用抗生素不足，动物\'农业，以及受污染的环境。这项研究是中东地区首次进行的一项健康调查，该调查结合了全基因组测序（WGS）来检查AMR在弯曲杆菌属中的传播。和沙门氏菌。进行这项横断面研究是为了检查AMR在人-动物-环境界面的作用，并在西岸中部的拉马拉/比雷赫省和耶路撒冷省进行，巴勒斯坦。在2021年和2022年，共收集和分析了592个样本。共有65种空肠弯曲杆菌和19种沙门氏菌。隔离物,使用牛津纳米孔技术MinION平台提取用于WGS的DNA。我们发现鸡粪中存在空肠弯曲菌和肠沙门氏菌的优势血清型，市场上出售的鸡肉，和无症状的农场工人的粪便，无论来源如何，分离株之间的遗传相似性都很高。此外,我们的结果显示，在2021年至2022年间，来自相同地点的空肠弯曲菌的菌株快速周转。大多数阳性沙门氏菌。样品是多药耐药（MDR）肠球菌血清型Muenchen，携带新生婴儿链球菌（pESI）大质粒的质粒，赋予多种抗生素耐药性。我们的发现强调了MDR食源性病原体通过食物链从动物传播到人类，强调“一个健康”方法的重要性，该方法考虑了人与人之间的相互联系，动物,和环境健康。重要性在这项研究之前，在中东国家，几乎没有关于沙门氏菌病和弯曲杆菌病以及相关AMR的人-动物-环境综合研究。现有的少数研究缺乏强大的流行病学研究设计，适用于一种健康方法，并且没有使用WGS来确定循环血清型及其AMR谱。由于公共卫生和粮食安全服务的崩溃，中东国家的内乱和战争推动了AMR。这项研究同时对人类进行采样，动物,和环境，利用WGS对巴勒斯坦肉鸡生产链中的食源性致病菌进行全面调查。我们表明，在养鸡场的样本中可以发现相同的空肠弯曲杆菌和肠球菌血清型。市场上出售的鸡肉，和无症状肉鸡生产工人。最显着的特征是在同一采样位置检测到的物种的遗传谱变化迅速。大多数阳性沙门氏菌。样品是携带pESI大质粒的MDR肠溶菌分离株。结果表明，在我们的样本中发现的肠沙门氏菌分离株与占所有临床沙门氏菌40％的分离株之间存在密切的关系。如前所述，在以色列的分离株，序列同一性超过99.9%。这些发现表明MDRS.enterica血清型Muenchen菌株通过食物链从动物到人类的跨界传播。该研究强调了将OneHealth综合研究与WGS相结合的重要性，以检测无法检测到的食源性病原体的环境-动物-人类传播。这项研究展示了环境-动物-人类综合采样和WGS监测AMR的好处。环境样本,在受冲突蹂躏的地方，监测系统有限，法规薄弱，可以提供有效的AMR监控解决方案。细菌分离物的WGS提供了细菌血清型和AMR在复杂的社会生态系统中的分布和传播的因果推断。因此,我们的研究结果指出，通过公共和动物卫生和食品安全当局的更紧密合作，实施“一个健康”方法的预期好处。
