Host Range of Influenza A Virus H1 to H16 in Eurasian Ducks Based on Tissue and Receptor Binding Studies

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.

Keywords: avian influenza; chicken; glycan; hemagglutinin; sialic acid receptor; virus attachment; wild birds.

FIG 1

Attachment of low pathogenic avian influenza viruses of subtypes H1 to H16 to colon of six Eurasian duck species and chicken. The mean abundance of cells to which virus attached was scored as follows: 1, negative (no attachment); 2, scarce (<10% cells positive); 3, moderate (10 to 50% cells positive); 4, abundant (>50% cells positive).

FIG 2

Attachment of low pathogenic avian influenza viruses of subtypes H1 to H16 to trachea of six Eurasian duck species and chicken. The mean abundance of cells to which virus attached was scored as follows: 1, negative (no attachment); 2, scarce (<10% cells positive); 3, moderate (10 to 50% cells positive); 4, abundant (>50% cells positive).

FIG 3

Attachment of low pathogenic avian influenza viruses of subtypes H1 to H16 to the glycan array. Each column represents one virus, and each row represents one glycan structure (Table 7). The colors indicate high (yellow) to low (dark blue) attachment based on the median signal from nine replicates for each virus and glycan structure combination, internally normalized toward the highest measured signal for each virus. The row annotation shows glycan type as shown in Table 7. Row numbers indicate glycan structures as shown in Table 7. The dendrogram was built based on Canberra distance and complete unweighted pair group method using average linkages (UPGMA) clustering of the attachment intensities. Column annotations show avian host species of virus isolation, HA clade, and HA group adopted from reference .