Exploring surface water as a transmission medium of avian influenza viruses – systematic infection studies in mallards

Abstract

Mallards ( Anas platyrhynchos ) are an abundant anseriform migratory wild bird species worldwide and an important reservoir for the maintenance of low pathogenicity (LP) avian influenza viruses (AIV). They have also been implicated in the spread of high pathogenicity (HP) AIV after spill-over events from HPAIV-infected poultry. The spread of HPAIV within wild water bird populations may lead to viral contamination of natural habitats. The role of small shallow water bodies as a transmission medium of AIV among mallards is investigated here in three experimental settings. (i) Delayed onset but rapid progression of infection seeded by two mallards inoculated with either LP or HP AIV to each eight sentinel mallards was observed in groups with access to a small 100 L water pool. In contrast, groups with a bell drinker as the sole source of drinking water showed a rapid onset but lengthened course of infection. (ii) HPAIV infection also set off when virus was dispersed in the water pool; titres as low as 10 2 TCID 50 L −1 (translating to 0.1 TCID 50 mL −1 ) proved to be sufficient. (iii) Substantial loads of viral RNA (and infectivity) were also found on the surface of the birds’ breast plumage. “Unloading” of virus infectivity from contaminated plumage into water bodies may be an efficient mechanism of virus spread by infected mallards. However, transposure of HPAIV via the plumage of an uninfected mallard failed. We conclude, surface water in small shallow water bodies may play an important role as a mediator of AIV infection of aquatic wild birds.

Clade 2.3.4.4b H5N1 high pathogenicity avian influenza virus (HPAIV) from the 2021/22 epizootic is highly duck adapted and poorly adapted to chickens

“…It must be emphasised that the pond and drinking waters were replaced and refreshed daily, hence the levels of H5N1-21 vRNA detection represented accumulation during the preceding 24 hours. It has also been demonstrated that deliberate experimental contamination of water with clade 2.3.4.4 H5N8-2016 isolates from the UK and The Netherlands can result in successful infection of naïve chickens [55], with similar observations having been made for mallards [56].…”

“…It must be emphasised that the pond and drinking waters were replaced and refreshed daily, hence the levels of H5N1-21 vRNA detection represented accumulation during the preceding 24 hours. It has also been demonstrated that deliberate experimental contamination of water with clade 2.3.4.4 H5N8-2016 isolates from the UK and The Netherlands can result in successful infection of naïve chickens [55], with similar observations having been made for mallards [56]. By specifically identifying how environmental contamination features in the mechanism of H5Nx clade 2.3.4.4 HPAIV transmission, this study along with others has confirmed the importance of biosecurity to prevent water contamination at poultry premises from becoming a source of infection and onward spread [53, 57].…”

Investigating Environmental Matrices for Use in Avian Influenza Virus Surveillance—Surface Water, Sediments, and Avian Fecal Samples

“…Yet, the tenacity of AIV in surface water and in sediments is remarkably high for a virion whose infectivity depends on an intact lipid envelope ( 11 – 15 ). In addition, very few viral particles resuspended in surface water can be sufficient to start an infection, as recently shown by experimental infection studies in mallards ( Anas platyrhynchos ) ( 10 ). This highlights the putative importance of surface water as a transmission medium of AIV.…”

“…If infected birds congregate in such water bodies, AIVs could then be excreted in surface water through fecal contamination. This may turn such waters into a highly efficient source of infection ( 10 ). Once present in water, AIV can drift with currents, sink into sediments, or may otherwise be diluted and inactivated by various abiotic and biotic factors.…”

The Changing Dynamics of Highly Pathogenic Avian Influenza H5N1: Next Steps for Management & Science in North America

“…Waterfowl and other aquatic species have commonly been asymptomatic carriers of LPAIV, presenting with mild enteric infections, which circulate among wild birds. Transmission of LPAIVs primarily occurs via an indirect fecal-oral route involving an environmental exposure, which provides opportunity for spread via shared waterbodies along migratory routes or wintering areas of congregation (Fouchier & Munster 2009;Ramey et al 2020;Ahrens et al 2022). The Gs/GD H5Nx viruses, however, have also evolved to replicate within the respiratory tract and can thus transmit directly through a respiratory route (i.e., respiratory droplets).…”