Improving risk assessment of the emergence of novel influenza A viruses by incorporating environmental surveillance

Abstract

Reassortment is an evolutionary mechanism by which influenza A viruses (IAV) generate genetic novelty. Reassortment is an important driver of host jumps and is widespread according to retrospective surveillance studies. However, predicting the epidemiological risk of reassortant emergence in novel hosts from surveillance data remains challenging. IAV strains persist and co-occur in the environment, promoting co-infection during environmental transmission. These conditions offer opportunity to understand reassortant emergence in reservoir and spillover hosts. Specifically, environmental RNA could provide rich information for understanding the evolutionary ecology of segmented viruses, and transform our ability to quantify epidemiological risk to spillover hosts. However, significant challenges with recovering and interpreting genomic RNA from the environment have impeded progress towards predicting reassortant emergence from environmental surveillance data. We discuss how the fields of genomics, experimental ecology and epidemiological modelling are well positioned to address these challenges. Coupling quantitative disease models and natural transmission studies with new molecular technologies, such as deep-mutational scanning and single-virus sequencing of environmental samples, should dramatically improve our understanding of viral co-occurrence and reassortment. We define observable risk metrics for emerging molecular technologies and propose a conceptual research framework for improving accuracy and efficiency of risk prediction. This article is part of the theme issue ‘Dynamic and integrative approaches to understanding pathogen spillover’.

Highly Pathogenic Avian Influenza Viruses at the Wild–Domestic Bird Interface in Europe: Future Directions for Research and Surveillance

“…Additionally, carcasses of dead birds can contaminate waters used by migratory birds. The chances of HPAI H5 virus detection are low, but with improving virus detection and characterization techniques—such as third generation sequencing—the integration of environmental sampling in routine surveillance programs becomes more feasible [ 192 ]. For this, the extraction and detection methods for environmental sampling should be prioritized, further optimised and standardized [ 3 , 193 ].…”

Mammalian pathogenicity and transmissibility of low pathogenic avian influenza H7N1 and H7N3 viruses isolated from North America in 2018

“…As risk assessment activities of influenza viruses capable of jumping species barriers include virus, host, and ecological considerations [ 37 , 38 ], it is prudent to employ multi-disciplinary One Health approaches to reduce the incidence and burden of disease in both zoonotic and human hosts [ 39 ]. Swift identification of and response to avian influenza outbreaks in poultry prevents the spread of virus to other susceptible animals, reduces the likelihood of human exposure to the virus, and limits the opportunity for virus adaptation in novel hosts [ 40 , 41 ]. Concurrent characterization of avian influenza viruses associated with outbreaks in gallinaceous birds represents a critical component of these activities, to facilitate a better understanding of these emerging viruses to cause disease in and transmit among mammalian hosts.…”

Experimental virus evolution in cancer cell monolayers, spheroids, and tissue explants

“…Experimental virus evolution has been used for investigating basic evolutionary processes under controlled laboratory conditions, as well as for clinical applications. These applications include the production of live attenuated vaccines ( Martín and Minor 2002 ), analysis of vaccine reversion to virulent phenotypes ( Stern et al 2017 ), modeling viral emergence in the laboratory ( Elena, Fraile, and García-Arenal 2014 ; Morley, Mendiola, and Turner 2015 ; Pepin et al 2019 ), predicting the appearance of drug resistances ( Dickinson et al 2014 ), and optimization of therapeutic viruses ( Sanjuán and Grdzelishvili 2015 ; Zainutdinov et al 2019 ). For experimental virus evolution to provide useful results, though, laboratory conditions should reproduce relevant selective pressures found in nature ( Geoghegan and Holmes 2018 : 40).…”