Antimicrobial resistance in hospital wastewater in Scotland: a cross-sectional metagenomics study

Abstract

BackgroundAntimicrobial resistance (AMR) is a global health crisis. It is well established that hospital wastewater can contain organisms that are on the WHO priority list of antibiotic-resistant organisms. We aimed to use metagenomics to study whether the abundances of resistance genes in hospital wastewater reflects clinical activity within the hospital. MethodsHospital wastewater was collected over a 24-h period in June, 2017 from multiple collection points representing different specialties within a tertiary hospital site in Scotland, UK and simultaneously from community sewage works. High throughput shotgun sequencing was done using Illumina HiSeq4000. Sequence reads were assigned taxonomically and to the AMR genes in the ResFinder database. The measured AMR gene abundances were correlated to hospital antimicrobial usage in defined daily doses per 100 occupied bed-days, mean patient length of stay in hospital, mean patient age per hospital collection point, and resistance levels in clinical isolates. Findings1047 bacterial genera and 174 different AMR genes were detected across all samples. Microbiota composition and AMR gene abundance and diversity varied between each collection point and AMR gene abundance was higher in hospital wastewater than in community influent. The composition of AMR genes correlated with microbiota composition (Procrustes analysis, p=0·002). Increased antimicrobial consumption at a class level was associated with higher AMR gene abundance within that class in hospital wastewater (incidence rate ratio 2·80, 95% CI 1·2–6·5, p=0·016). Prolonged mean patient length of stay was associated with higher total AMR gene abundance in hospital wastewater (2·05, 1·39–3·01, p=0·0003). No overall association was found between resistance in clinical isolates at an antimicrobial class level and AMR gene abundance in hospital wastewater. InterpretationAntimicrobial usage is a major driver of AMR gene outflow from hospitals into the sewage environment. The positive relationship between length of stay and AMR gene abundance is consistent with prolonged admission being a risk factor for carriage and infection with resistant microorganisms. Our findings show that hospital wastewater does reflect inpatient activity. With further evaluation this method might represent a useful surveillance tool to monitor hospital AMR gene outflow and guide environmental policy on AMR. FundingAcademy of Medical Sciences.