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

Meghan Perry*, Bram van Bunnik, Luke McNally, Bryan Wee, Patrick Munk, Amanda Warr, Barbara Moore, Pota Kalima, Carol Philip, Ana Maria de Roda Husman, Frank Møller Aarestrup, Mark Woolhouse

*Corresponding author for this work

Research output: Contribution to journalConference abstract in journalResearchpeer-review

Abstract

Background : Antimicrobial 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. Methods : Hospital 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. Findings : 1047 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. Interpretation : Antimicrobial 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. Funding : Academy of Medical Sciences.
Original languageEnglish
JournalLancet
Volume394
Pages (from-to)S1
ISSN0140-6736
DOIs
Publication statusPublished - 2019

Cite this

Perry, Meghan ; van Bunnik, Bram ; McNally, Luke ; Wee, Bryan ; Munk, Patrick ; Warr, Amanda ; Moore, Barbara ; Kalima, Pota ; Philip, Carol ; de Roda Husman, Ana Maria ; Aarestrup, Frank Møller ; Woolhouse, Mark. / Antimicrobial resistance in hospital wastewater in Scotland: a cross-sectional metagenomics study. In: Lancet. 2019 ; Vol. 394. pp. S1.
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title = "Antimicrobial resistance in hospital wastewater in Scotland: a cross-sectional metagenomics study",
abstract = "Background : Antimicrobial 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. Methods : Hospital 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. Findings : 1047 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. Interpretation : Antimicrobial 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. Funding : Academy of Medical Sciences.",
author = "Meghan Perry and {van Bunnik}, Bram and Luke McNally and Bryan Wee and Patrick Munk and Amanda Warr and Barbara Moore and Pota Kalima and Carol Philip and {de Roda Husman}, {Ana Maria} and Aarestrup, {Frank M{\o}ller} and Mark Woolhouse",
year = "2019",
doi = "10.1016/s0140-6736(19)32798-9",
language = "English",
volume = "394",
pages = "S1",
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issn = "0140-6736",
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Perry, M, van Bunnik, B, McNally, L, Wee, B, Munk, P, Warr, A, Moore, B, Kalima, P, Philip, C, de Roda Husman, AM, Aarestrup, FM & Woolhouse, M 2019, 'Antimicrobial resistance in hospital wastewater in Scotland: a cross-sectional metagenomics study', Lancet, vol. 394, pp. S1. https://doi.org/10.1016/s0140-6736(19)32798-9

Antimicrobial resistance in hospital wastewater in Scotland: a cross-sectional metagenomics study. / Perry, Meghan; van Bunnik, Bram; McNally, Luke; Wee, Bryan; Munk, Patrick; Warr, Amanda; Moore, Barbara; Kalima, Pota; Philip, Carol; de Roda Husman, Ana Maria; Aarestrup, Frank Møller; Woolhouse, Mark.

In: Lancet, Vol. 394, 2019, p. S1.

Research output: Contribution to journalConference abstract in journalResearchpeer-review

TY - ABST

T1 - Antimicrobial resistance in hospital wastewater in Scotland: a cross-sectional metagenomics study

AU - Perry, Meghan

AU - van Bunnik, Bram

AU - McNally, Luke

AU - Wee, Bryan

AU - Munk, Patrick

AU - Warr, Amanda

AU - Moore, Barbara

AU - Kalima, Pota

AU - Philip, Carol

AU - de Roda Husman, Ana Maria

AU - Aarestrup, Frank Møller

AU - Woolhouse, Mark

PY - 2019

Y1 - 2019

N2 - Background : Antimicrobial 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. Methods : Hospital 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. Findings : 1047 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. Interpretation : Antimicrobial 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. Funding : Academy of Medical Sciences.

AB - Background : Antimicrobial 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. Methods : Hospital 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. Findings : 1047 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. Interpretation : Antimicrobial 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. Funding : Academy of Medical Sciences.

U2 - 10.1016/s0140-6736(19)32798-9

DO - 10.1016/s0140-6736(19)32798-9

M3 - Conference abstract in journal

VL - 394

SP - S1

JO - Lancet

JF - Lancet

SN - 0140-6736

ER -