Abstract
Although disinfection is key to infection control, the colonization patterns and resistomes of hospital-environment microbes remain underexplored. We report the first extensive genomic characterization of microbiomes, pathogens and antibiotic resistance cassettes in a tertiary-care hospital, from repeated sampling (up to 1.5 years apart) of 179 sites associated with 45 beds. Deep shotgun metagenomics unveiled distinct ecological niches of microbes and antibiotic resistance genes characterized by biofilm-forming and human-microbiome-influenced environments with corresponding patterns of spatiotemporal divergence. Quasi-metagenomics with nanopore sequencing provided thousands of high-contiguity genomes, phage and plasmid sequences (>60% novel), enabling characterization of resistome and mobilome diversity and dynamic architectures in hospital environments. Phylogenetics identified multidrug-resistant strains as being widely distributed and stably colonizing across sites. Comparisons with clinical isolates indicated that such microbes can persist in hospitals for extended periods (>8 years), to opportunistically infect patients. These findings highlight the importance of characterizing antibiotic resistance reservoirs in hospitals and establish the feasibility of systematic surveys to target resources for preventing infections.
Highlights
Disinfection is key to infection control, the colonization patterns and resistomes of hospital-environment microbes remain underexplored
A diverse set of sites (n = 7) of concern for infection control[21,22] and different room types distributed around the building (5 single-bed isolation rooms together with 4 multidrug-resistant organisms (MDROs) and 4 standard five-bed wards) were selected for initial sampling at two time points (1 week apart) of a tertiary-care hospital in Singapore (45 beds (4% of total), 179 sites, 358 samples; Fig. 1a and Supplementary Data 1)
While community type A (CTA) sites were more taxonomically diverse (Wilcoxon P value < 10−3; Supplementary Fig. 1) and largely high-touch surfaces with frequent contact from patients and healthcare workers[24], community type B (CTB) represents sites of increasing concern for infection control for their propensity to harbor MDROs10,21,25. Joint analysis of these community types helped to identify key taxonomic features that differentiate them, including several human-microbiome-associated genera and aquatic and terrestrial environment-associated genera in CTA and CTB, respectively, not all genera could be defined in these terms
Summary
Disinfection is key to infection control, the colonization patterns and resistomes of hospital-environment microbes remain underexplored. Comparisons with clinical isolates indicated that such microbes can persist in hospitals for extended periods (>8 years), to opportunistically infect patients These findings highlight the importance of characterizing antibiotic resistance reservoirs in hospitals and establish the feasibility of systematic surveys to target resources for preventing infections. Efforts to survey the hospital environment have focused on culture-based isolation of specific pathogens, with each isolate individually characterized via functional profiling, genotyping and/or whole-genome sequencing[9,10,11]. This is laborious, is prone to isolation bias and precludes insights into overall community structure and how that interacts with the built environment to impact HAIs12
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