Human microbiota drives hospital-associated antimicrobial resistance dissemination in the urban environment and mirrors patient case rates

Microbiome

Research

Christopher E. Mason¹  Antonio Galiana²  Fabio Grill²  Mariela Vieytes²  Josefina Puig³  Nadia Riera³  Verónica Antelo³  Cecilia Salazar³  Andrés Parada³  Matias Giménez⁴  Gregorio Iraola⁵  Jimena Risso⁶  Bruno D’Alessandro⁷ 

[1] Department of Physiology and Biophysics, Weill Cornell Medicine, New York, NY, USA;The HRH Prince Alwaleed Bin Talal Bin Abdulaziz Alsaud Institute for Computational Biomedicine, Weill Cornell Medicine, New York, NY, USA;The WorldQuant Initiative for Quantitative Prediction, Weill Cornell Medicine, New York, NY, USA;Hospital Maciel, Montevideo, Uruguay;Microbial Genomics Laboratory, Institut Pasteur de Montevideo, 11400, Montevideo, Uruguay;Microbial Genomics Laboratory, Institut Pasteur de Montevideo, 11400, Montevideo, Uruguay;Molecular Microbiology Laboratory, Instituto de Investigaciones Biológicas Clemente Estable (IIBCE), Montevideo, Uruguay;Microbial Genomics Laboratory, Institut Pasteur de Montevideo, 11400, Montevideo, Uruguay;Wellcome Sanger Institute, Hinxton, UK;Center for Integrative Biology, Universidad Mayor, Santiago de Chile, Chile;Servicio de Evaluación de la Calidad y Control Ambiental, Intendencia de Montevideo, Montevideo, Uruguay;Servicio de Evaluación de la Calidad y Control Ambiental, Intendencia de Montevideo, Montevideo, Uruguay;Instituto de Higiene, Facultad de Medicina, Universidad de la República, Montevideo, Uruguay;

关键词: Antimicrobial resistance;    Urban metagenomics;    Nanopore sequencing;    Carbapenem resistance;    Nosocomial outbreak;    KPC;    Urban wastewater;   

DOI  :  10.1186/s40168-022-01407-8

 received in 2022-07-13, accepted in 2022-10-21,  发布年份 2022

来源: Springer

【 摘 要 】

BackgroundThe microbial community composition of urban environments is primarily determined by human activity. The use of metagenomics to explore how microbial communities are shaped in a city provides a novel input that can improve decisions on public health measures, architectural design, and urban resilience. Of note, the sewage system in a city acts as a complex reservoir of bacteria, pharmaceuticals, and antimicrobial resistant (AMR) genes that can be an important source of epidemiological information. Hospital effluents are rich in patient-derived bacteria and can thus readily become a birthplace and hotspot reservoir for antibiotic resistant pathogens which are eventually incorporated into the environment. Yet, the scope to which nosocomial outbreaks impact the urban environment is still poorly understood.ResultsIn this work, we extensively show that different urban waters from creeks, beaches, sewage spillways and collector pipes enclose discrete microbial communities that are characterized by a differential degree of contamination and admixture with human-derived bacteria. The abundance of human bacteria correlates with the abundance of AMR genes in the environment, with beta-lactamases being the top-contributing class to distinguish low vs. highly-impacted urban environments. Indeed, the abundance of beta-lactamase resistance and carbapenem resistance determinants in the urban environment significantly increased in a 1-year period. This was in line with a pronounced increase of nosocomial carbapenem-resistant infections reported during the same period that was mainly driven by an outbreak-causing, carbapenemase-producing Klebsiella pneumoniae (KPC) ST-11 strain. Genome-resolved metagenomics of urban waters before and after this outbreak, coupled with high-resolution whole-genome sequencing, confirmed the dissemination of the ST-11 strain and a novel KPC megaplasmid from the hospital to the urban environment. City-wide analysis showed that geospatial dissemination of the KPC megaplasmid in the urban environment inversely depended on the sewage system infrastructure.ConclusionsWe show how urban metagenomics and outbreak genomic surveillance can be coupled to generate relevant information for infection control, antibiotic stewardship, and pathogen epidemiology. Our results highlight the need to better characterize and understand how human-derived bacteria and antimicrobial resistance disseminate in the urban environment to incorporate this information in the development of effluent treatment infrastructure and public health policies.2A5ZQFmXmKxDXginhFNeyTVideo Abstract

【 授权许可】

CC BY   
© The Author(s) 2022

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