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 10² TCID₅₀ L⁻¹ (translating to 0.1 TCID₅₀ 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.

KEYWORDS:

• Avian influenza
• transmission
• high pathogenicity
• surface water
• spread
• mallard

Acknowledgments

AKA has been funded by a grant from the German Environment Agency (FKZ 3718 62 236 0). We are grateful to animal keepers at FLI (Doreen Fiedler, Frank Klipp, Harald Manthei, Steffen Kiepert and Christian Lipinski) and thank Aline Maksimov and Diana Parlow for technical support. We would like to thank Annika Graaf and Jana Schulz for her help in preparing the animal experiment application.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Author contributions

Conceptualization, T.C.H., M.B.; methodology, validation A.K.A., T.C.H; formal analysis, A.K.A.; investigation, A.K.A.; resources, H.C.S., T.C.M., M.B.; data curation, T.C.H.; writing—original draft preparation, A.K.A. and T.C.H.; writing—review and editing, A.K.A., H.C.S., T.C.M., M.B. and T.C.H.; visualization, A.K.A.; supervision, T.C.M., M.B., and T.C.H.; project administration, H.C.S.; funding acquisition, T.C.M. All authors have read and agreed to the published version of the manuscript.

Data availability statement

All data pertinent to this study are presented in tables and figures in the main text or in the supplementary materials.

Institutional Review board statement

The animals for the infection experiments were licensed by the animal ethics committee of the Federal State of Mecklenburg-Vorpommerania (LALLF 7221.3-1-023/21, TV „FLI 08/21: Aviäre Influenza in Oberflächenwasser“).

Software

Figure 1 was created with BioRender.com and licensed by the company under agreement number VP23LU0PN1. Other figures were created with GraphPad Prism software version 7 (GraphPad Software, San Diego, CA, USA) or with Inkscape version 1.01.

Additional information

Funding

This research was funded by a grant to A.K.A. from the German Environment Agency (Umweltbundesamt), grant number FKZ 3718 62 236 0.