Departament of Biology & CESAM, University of Aveiro, Campus de Santiago, 3810-193, Aveiro, Portugal.
Centre for Ecology, Evolution and Environmental Changes (cE3c), Faculdade de Ciências, Universidade de Lisboa, 1749-016, Lisbon, Portugal; Biosystems & Integrative Sciences Institute (BioISI), Faculdade de Ciências, Universidade de Lisboa, 1749-016, Lisbon, Portugal.
Environ Pollut. 2022 Aug 1;306:119367. doi: 10.1016/j.envpol.2022.119367. Epub 2022 Apr 28.
Extended-spectrum β-lactamases (ESBL)-producing Enterobacterales have been classified as critical priority pathogens by the World Health Organization (WHO). ESBL are universally distributed and, in 2006, were firstly reported on a wild animal. Understanding the relative contributions of wild animals to ESBL circulation in the environment is urgently needed. In this work, we have conducted a nationwide study in Portugal to investigate the occurrence of bacteria carrying clinically significant antimicrobial resistance genes (ARG), using widely distributed wild ungulates as model species. A total of 151 antimicrobial resistant-Enterobacterales isolates were detected from 181 wild ungulates: 50% (44/88) of isolates from wild boar (Sus scrofa), 40.3% (25/62) from red deer (Cervus elaphus), 41.4% (12/29) from fallow deer (Dama dama) and 100% (2/2) from mouflon (Ovis aries subsp. musimon). Selected isolates showed a diversified resistance profile, with particularly high values corresponding to ampicillin (71.5%) and tetracycline (63.6%). Enterobacterales strains carried bla, tetA, tetB, sul2, sul1 or dfrA1 ARG genes. They also carried bla-type genes, which are prevalent in human infections, namely CTX-M-14, CTX-M-15 and CTX-M-98. Strikingly, this is the first report of CTX-M-98 in wildlife. Almost 40% (n = 59) of Enterobacterales were multi-drug resistant. The diversity of plasmids carried by ESBL isolates was remarkable, including IncF, K and P. This study highlights the potential role of wild ungulates as environmental reservoirs of CTX-M ESBL-producing E. coli and in the spill-over of AMR bacteria and their determinants. Our findings suggest that wild ungulates are useful as strategic sentinel species of AMR in terrestrial environments, especially in response to potential sources of anthropogenic pollution, providing early warning of potential risks to human, animal and environmental health.
产超广谱β-内酰胺酶（ESBL）肠杆菌科已被世界卫生组织（WHO）列为危急优先病原体。ESBL 广泛分布，并且于 2006 年首次在野生动物中报道。了解野生动物对环境中 ESBL 传播的相对贡献是迫切需要的。在这项工作中，我们在葡萄牙进行了一项全国性研究，以调查携带临床上重要的抗菌药物耐药基因（ARG）的细菌的发生情况，使用广泛分布的野生有蹄类动物作为模型物种。从 181 只野生有蹄类动物中检测到 151 株耐抗菌药物的肠杆菌科分离株：50%（44/88）来自野猪（Sus scrofa），40.3%（25/62）来自马鹿（Cervus elaphus），41.4%（12/29）来自黇鹿（Dama dama）和 100%（2/2）来自摩弗伦羊（Ovis aries subsp. musimon）。选定的分离株表现出多样化的耐药谱，其中氨苄青霉素（71.5%）和四环素（63.6%）的耐药率特别高。肠杆菌科菌株携带 bla、tetA、tetB、sul2、sul1 或 dfrA1 ARG 基因。它们还携带 bla 型基因，这些基因在人类感染中很常见，即 CTX-M-14、CTX-M-15 和 CTX-M-98。值得注意的是，这是首次在野生动物中报道 CTX-M-98。近 40%（n=59）的肠杆菌科对多种药物耐药。ESBL 分离株携带的质粒多样性显著，包括 IncF、K 和 P。这项研究强调了野生有蹄类动物作为 CTX-M 产 ESBL 大肠杆菌的环境储库以及 AMR 细菌及其决定因素溢出的潜在作用。我们的研究结果表明，野生有蹄类动物是陆地环境中 AMR 的有用战略哨点物种，尤其是在应对潜在的人为污染来源时，可以对人类、动物和环境健康的潜在风险发出预警。
