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

Andrew J Lee; Stephen Carson; Marina I Reyne; Andrew Marshall; Daniel Moody; Danielle M Allen; Pearce Allingham; Ashley Levickas; Arthur Fitzgerald; Stephen H Bell; Jonathan Lock; Jonathon D Coey; Cormac McSparron; Behnam F Nejad; Evan P Troendle; David A Simpson; David G Courtney; Gisli G Einarsson; James P McKenna; Derek J Fairley; Tanya Curran; Jennifer M McKinley; Deirdre F Gilpin; Ken Lemon; John W McGrath; Connor G G Bamford

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

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

Lancet Microbe. 2024 Oct 9:100933. doi: 10.1016/S2666-5247(24)00175-7. Online ahead of print.

Authors

Andrew J Lee¹, Stephen Carson², Marina I Reyne², Andrew Marshall², Daniel Moody², Danielle M Allen², Pearce Allingham², Ashley Levickas², Arthur Fitzgerald³, Stephen H Bell², Jonathan Lock², Jonathon D Coey², Cormac McSparron⁴, Behnam F Nejad⁴, Evan P Troendle³, David A Simpson³, David G Courtney³, Gisli G Einarsson⁵, James P McKenna⁶, Derek J Fairley⁶, Tanya Curran⁶, Jennifer M McKinley⁴, Deirdre F Gilpin⁵, Ken Lemon⁷, John W McGrath⁸, Connor G G Bamford⁸

Affiliations

¹ School of Biological Sciences, Queen's University Belfast, Belfast, Northern Ireland, UK. Electronic address: [email protected].
² School of Biological Sciences, Queen's University Belfast, Belfast, Northern Ireland, UK.
³ Wellcome-Wolfson Institute for Experimental Medicine, School of Medicine, Dentistry and Biomedical Sciences, Queen's University Belfast, Belfast, Northern Ireland, UK.
⁴ Geography, School of Natural and Built Environment, Queen's University Belfast, Belfast, Northern Ireland, UK.
⁵ School of Pharmacy, Queen's University Belfast, Belfast, Northern Ireland, UK.
⁶ Regional Virology Laboratory, Belfast Health and Social Care Trust, Royal Victoria Hospital, Belfast, Northern Ireland, UK.
⁷ Veterinary Sciences Division, Agri-Food and Biosciences Institute, Stormont, Belfast, Northern Ireland, UK.
⁸ 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.

PMID: 39395428
DOI: 10.1016/S2666-5247(24)00175-7

Abstract

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: 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: 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: 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: Department of Health for Northern Ireland.