Wastewater monitoring of human and avian influenza A viruses in Northern Ireland: a genomic surveillance study.


Journal

The Lancet. Microbe
ISSN: 2666-5247
Titre abrégé: Lancet Microbe
Pays: England
ID NLM: 101769019

Informations de publication

Date de publication:
09 Oct 2024
Historique:
received: 01 09 2023
revised: 29 04 2024
accepted: 17 06 2024
medline: 13 10 2024
pubmed: 13 10 2024
entrez: 12 10 2024
Statut: aheadofprint

Résumé

Influenza A viruses (IAVs) are significant pathogens of humans and other animals. Although endemic in humans and birds, novel IAV strains can emerge, jump species, and cause epidemics, like the latest variant of H5N1. Wastewater-based epidemiology (WBE) has been shown capable of detecting human IAVs. We aimed to assess whether whole-genome sequencing (WGS) of IAVs from wastewater is possible and can be used to discriminate between circulating strains of human and any non-human IAVs, such as those of avian origin. Using a pan-IAV RT-quantitative PCR assay, six wastewater treatment works (WWTWs) across Northern Ireland were screened from Aug 1 to Dec 5, 2022. A nanopore WGS approach was used to sequence RT-qPCR-positive samples. Phylogenetic analysis of sequences relative to currently circulating human and non-human IAVs was performed. For comparative purposes, clinical data (PCR test results) were supplied by The Regional Virus Laboratory, Belfast Health and Social Care Trust (Belfast, Northern Ireland, UK). We detected a dynamic IAV signal in wastewater from Sept 5, 2022, onwards across Northern Ireland, which did not show a clear positive relationship with the clinical data obtained for the region. Meta (mixed strain) whole-genome sequences were generated from wastewater samples displaying homology to only human and avian IAV strains. The relative proportion of IAV reads of human versus avian origin differed across time and sample site. A diversity in subtypes and lineages was detected (eg, H1N1, H3N2, and several avian). Avian segment 8 related to those found in recent H5N1 clade 2.3.4.4b was identified. WBE affords a means to monitor circulating human and avian IAV strains and provide crucial genetic information. As such, WBE can provide rapid, cost-effective, year-round One Health surveillance to help control IAV epidemic and pandemic-related threats. However, optimisation of WBE protocols are necessary to ensure observed wastewater signals not only correlate with clinical case data, but yield information on the wider environmental pan-influenz-ome. Department of Health for Northern Ireland.

Sections du résumé

BACKGROUND BACKGROUND
Influenza A viruses (IAVs) are significant pathogens of humans and other animals. Although endemic in humans and birds, novel IAV strains can emerge, jump species, and cause epidemics, like the latest variant of H5N1. Wastewater-based epidemiology (WBE) has been shown capable of detecting human IAVs. We aimed to assess whether whole-genome sequencing (WGS) of IAVs from wastewater is possible and can be used to discriminate between circulating strains of human and any non-human IAVs, such as those of avian origin.
METHODS METHODS
Using a pan-IAV RT-quantitative PCR assay, six wastewater treatment works (WWTWs) across Northern Ireland were screened from Aug 1 to Dec 5, 2022. A nanopore WGS approach was used to sequence RT-qPCR-positive samples. Phylogenetic analysis of sequences relative to currently circulating human and non-human IAVs was performed. For comparative purposes, clinical data (PCR test results) were supplied by The Regional Virus Laboratory, Belfast Health and Social Care Trust (Belfast, Northern Ireland, UK).
FINDINGS RESULTS
We detected a dynamic IAV signal in wastewater from Sept 5, 2022, onwards across Northern Ireland, which did not show a clear positive relationship with the clinical data obtained for the region. Meta (mixed strain) whole-genome sequences were generated from wastewater samples displaying homology to only human and avian IAV strains. The relative proportion of IAV reads of human versus avian origin differed across time and sample site. A diversity in subtypes and lineages was detected (eg, H1N1, H3N2, and several avian). Avian segment 8 related to those found in recent H5N1 clade 2.3.4.4b was identified.
INTERPRETATION CONCLUSIONS
WBE affords a means to monitor circulating human and avian IAV strains and provide crucial genetic information. As such, WBE can provide rapid, cost-effective, year-round One Health surveillance to help control IAV epidemic and pandemic-related threats. However, optimisation of WBE protocols are necessary to ensure observed wastewater signals not only correlate with clinical case data, but yield information on the wider environmental pan-influenz-ome.
FUNDING BACKGROUND
Department of Health for Northern Ireland.

Identifiants

pubmed: 39395428
pii: S2666-5247(24)00175-7
doi: 10.1016/S2666-5247(24)00175-7
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

100933

Informations de copyright

Copyright © 2024 The Author(s). Published by Elsevier Ltd.. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests DFG and JWM report grants from the Northern Ireland Department of Health and Public Health Agency. All other authors declare no competing interests.

Auteurs

Andrew J Lee (AJ)

School of Biological Sciences, Queen's University Belfast, Belfast, Northern Ireland, UK. Electronic address: a.j.lee@qub.ac.uk.

Stephen Carson (S)

School of Biological Sciences, Queen's University Belfast, Belfast, Northern Ireland, UK.

Marina I Reyne (MI)

School of Biological Sciences, Queen's University Belfast, Belfast, Northern Ireland, UK.

Andrew Marshall (A)

School of Biological Sciences, Queen's University Belfast, Belfast, Northern Ireland, UK.

Daniel Moody (D)

School of Biological Sciences, Queen's University Belfast, Belfast, Northern Ireland, UK.

Danielle M Allen (DM)

School of Biological Sciences, Queen's University Belfast, Belfast, Northern Ireland, UK.

Pearce Allingham (P)

School of Biological Sciences, Queen's University Belfast, Belfast, Northern Ireland, UK.

Ashley Levickas (A)

School of Biological Sciences, Queen's University Belfast, Belfast, Northern Ireland, UK.

Arthur Fitzgerald (A)

Wellcome-Wolfson Institute for Experimental Medicine, School of Medicine, Dentistry and Biomedical Sciences, Queen's University Belfast, Belfast, Northern Ireland, UK.

Stephen H Bell (SH)

School of Biological Sciences, Queen's University Belfast, Belfast, Northern Ireland, UK.

Jonathan Lock (J)

School of Biological Sciences, Queen's University Belfast, Belfast, Northern Ireland, UK.

Jonathon D Coey (JD)

School of Biological Sciences, Queen's University Belfast, Belfast, Northern Ireland, UK.

Cormac McSparron (C)

Geography, School of Natural and Built Environment, Queen's University Belfast, Belfast, Northern Ireland, UK.

Behnam F Nejad (BF)

Geography, School of Natural and Built Environment, Queen's University Belfast, Belfast, Northern Ireland, UK.

Evan P Troendle (EP)

Wellcome-Wolfson Institute for Experimental Medicine, School of Medicine, Dentistry and Biomedical Sciences, Queen's University Belfast, Belfast, Northern Ireland, UK.

David A Simpson (DA)

Wellcome-Wolfson Institute for Experimental Medicine, School of Medicine, Dentistry and Biomedical Sciences, Queen's University Belfast, Belfast, Northern Ireland, UK.

David G Courtney (DG)

Wellcome-Wolfson Institute for Experimental Medicine, School of Medicine, Dentistry and Biomedical Sciences, Queen's University Belfast, Belfast, Northern Ireland, UK.

Gisli G Einarsson (GG)

School of Pharmacy, Queen's University Belfast, Belfast, Northern Ireland, UK.

James P McKenna (JP)

Regional Virology Laboratory, Belfast Health and Social Care Trust, Royal Victoria Hospital, Belfast, Northern Ireland, UK.

Derek J Fairley (DJ)

Regional Virology Laboratory, Belfast Health and Social Care Trust, Royal Victoria Hospital, Belfast, Northern Ireland, UK.

Tanya Curran (T)

Regional Virology Laboratory, Belfast Health and Social Care Trust, Royal Victoria Hospital, Belfast, Northern Ireland, UK.

Jennifer M McKinley (JM)

Geography, School of Natural and Built Environment, Queen's University Belfast, Belfast, Northern Ireland, UK.

Deirdre F Gilpin (DF)

School of Pharmacy, Queen's University Belfast, Belfast, Northern Ireland, UK.

Ken Lemon (K)

Veterinary Sciences Division, Agri-Food and Biosciences Institute, Stormont, Belfast, Northern Ireland, UK.

John W McGrath (JW)

School of Biological Sciences, Queen's University Belfast, Belfast, Northern Ireland, UK; Institute for Global Food Security, Queen's University Belfast, Belfast, Northern Ireland, UK.

Connor G G Bamford (CGG)

School of Biological Sciences, Queen's University Belfast, Belfast, Northern Ireland, UK; Institute for Global Food Security, Queen's University Belfast, Belfast, Northern Ireland, UK.

Classifications MeSH