Abstract

Dabbling and diving ducks partly occupy shared habitats but have been reported to play different roles in wildlife infectious disease dynamics. Influenza A virus (IAV) epidemiology in wild birds has been based primarily on surveillance programs focused on dabbling duck species, particularly mallard (Anas platyrhynchos). Surveillance in Eurasia has shown that in mallards, some subtypes are commonly (H1 to H7 and H10), intermediately (H8, H9, H11, and H12), or rarely (H13 to H16) detected, contributing to discussions on virus host range and reservoir competence. An alternative to surveillance in determining IAV host range is to study virus attachment as a determinant for infection. Here, we investigated the attachment patterns of all avian IAV subtypes (H1 to H16) to the respiratory and intestinal tracts of four dabbling duck species (Mareca and Anas spp.), two diving duck species (Aythya spp.), and chicken, as well as to a panel of 65 synthetic glycan structures. We found that IAV subtypes generally showed abundant attachment to colon of the Anas duck species, mallard, and Eurasian teal (Anas crecca), supporting the fecal-oral transmission route in these species. The reported glycan attachment profile did not explain the virus attachment patterns to tissues but showed significant attachment of duck-originated viruses to fucosylated glycan structures and H7 virus tropism for Neu5Gc-LN. Our results suggest that Anas ducks play an important role in the ecology and epidemiology of IAV. Further knowledge on virus tissue attachment, receptor distribution, and receptor binding specificity is necessary to understand the mechanisms underlying host range and epidemiology of IAV.IMPORTANCE Influenza A viruses (IAVs) circulate in wild birds worldwide. From wild birds, the viruses can cause outbreaks in poultry and sporadically and indirectly infect humans. A high IAV diversity has been found in mallards (Anas platyrhynchos), which are most often sampled as part of surveillance programs; meanwhile, little is known about the role of other duck species in IAV ecology and epidemiology. In this study, we investigated the attachment of all avian IAV hemagglutinin (HA) subtypes (H1 to H16) to tissues of six different duck species and chicken as an indicator of virus host range. We demonstrated that the observed virus attachment patterns partially explained reported field prevalence. This study demonstrates that dabbling ducks of the Anas genus are potential hosts for most IAV subtypes, including those infecting poultry. This knowledge is useful to target the sampling of wild birds in nature and to further study the interaction between IAVs and birds.

Highlights

  • Dabbling and diving ducks partly occupy shared habitats but have been reported to play different roles in wildlife infectious disease dynamics

  • The host range of Influenza A virus (IAV) is partially determined by the HA subtype, as most clearly demonstrated for H13 and H16 subtypes, which have evolved into gull-adapted lineages [9,10,11] and resulted in host range restriction between species belonging to the Laridae family and Anseriformes order

  • For the epidemiology of most IAV subtypes, a major role is played by ducks—in particular, dabbling ducks such as mallard (Anas platyrhynchos)—in which epidemics of low pathogenic avian influenza A viruses (LPAIVs) occur each fall in the Northern Hemisphere [2, 6]

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Summary

Introduction

Dabbling and diving ducks partly occupy shared habitats but have been reported to play different roles in wildlife infectious disease dynamics. Influenza A virus (IAV) epidemiology in wild birds has been based primarily on surveillance programs focused on dabbling duck species, mallard (Anas platyrhynchos). Subtypes detected in a minimum of 5 and a maximum of 14 of 20 years of surveillance (25% to 75%) were considered “intermediate” subtypes (i.e., H8, H9, H11, and H12) (Tables 1 and 2) This leads to the question of whether mallards are the primary reservoir of the so-called intermediate and rare subtypes or if persistence of these subtypes is driven by infections in other host species, in particular other dabbling (e.g., Anas and Mareca) or diving (e.g., Aythya) duck species, which are insufficiently covered in surveillance studies [15]. Attachment patterns of some HA subtypes (i.e., H3, H4, H6, H12, and H16) of LPAIVs to cells and tissues of birds have been described using virus histochemistry and have been suggested to Journal of Virology jvi.asm.org 2

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