Subtype Diversity of Influenza A Virus in North American Waterfowl: a Multidecade Study

Abstract

The discovery in 1976 of waterfowl as the primary reservoir of influenza A viruses (IAVs) has since spurred decades of waterfowl surveillance efforts by researchers dedicated to understanding the ecology of IAV and its subsequent threat to human and animal health. Here, we employed a multidecade, continental-scale approach of surveillance data to understand trends of seasonal IAV subtype diversity. Between 1976 and 2015, IAVs were detected in 8,427 (10.8%) of 77,969 samples from migratory waterfowl throughout the Central and Mississippi Migratory Flyways in the United States and Canada. A total of 96 hemagglutinin (HA)/neuraminidase (NA) subtype combinations were isolated, which included most HA (H1 to H14) and all 9 NA subtypes. We observed an annual trend of high influenza prevalence, involving a few dominant subtypes, on northern breeding grounds during summer with progressively lowered influenza prevalence, comprised of a highly diverse profile of subtypes, as waterfowl migrate toward southern wintering grounds. Isolates recovered during winter had the highest proportion of mixed and rare HA/NA combinations, indicating increased opportunity for reassortment of IAVs. In addition, 70% of H5 and 49% of H7 IAV isolates were recovered from samples collected during fall and spring, respectively; these are subtypes that can have significant implications for public health and agriculture sectors. Annual cyclical dominance of subtypes on northern breeding grounds is revealed through the longitudinal nature of this study. Our novel findings exhibit the unrealized potential for discovery using existing IAV surveillance data. IMPORTANCE Wild aquatic birds are the primary natural reservoir of influenza A viruses (IAVs) and are therefore responsible for the dispersal and maintenance of IAVs representing a broad range of antigenic and genetic diversity. The aims of IAV surveillance in waterfowl not only relate to understanding the risk of spillover risk to humans, but also to improving our understanding of basic questions related to IAV evolution and ecology. By evaluating several decades of surveillance data from wild aquatic birds sampled along North American migratory flyways, we discovered an annual trend of increasing subtype diversity during southbound migration, peaking on southern wintering grounds. Winter sampling revealed the highest proportion of mixed and rare infections that suggest higher opportunity for spillover. These findings allow improvements to surveillance efforts to robustly capture IAV diversity that will be used for vaccine development and cultivate a more thorough understanding of IAV evolution and persistence mechanisms.

Avian Influenza Viruses Detected in Birds in Sub-Saharan Africa: A Systematic Review

“…The HA subtype diversity in our study has similarities and differences to that found in studies in China [ 107 ], Netherlands [ 108 ], North America [ 109 , 110 ], Germany [ 111 ] and Northern Europe [ 112 ] though a number of these studies were done in wild aquatic birds. For example, our study was comparable to the study in China [ 107 ] and that in the Netherlands [ 108 ], which did not detect H8, H12–H16.…”

“…For example, our study was comparable to the study in China [ 107 ] and that in the Netherlands [ 108 ], which did not detect H8, H12–H16. Furthermore, our study only detected six NA subtypes and 19 HA/NA combinations, while studies in Germany [ 111 ], Northern Europe [ 112 ] and North America [ 109 , 110 ] detected 40 or more subtype combinations. This higher subtype diversity in these studies could be because the surveillance was focused on wild waterfowl, which are expected to harbor a large pool of various AIV subtypes, which could also be true for Southern Africa, which had the highest subtype diversity in sub-Saharan Africa.…”

Influenza A Viruses in Whistling Ducks (Subfamily Dendrocygninae)

“…Results from efforts reported here indicate that BBWD are exposed to (seroprevalence range 3.3%–18.9%) and can be infected by (isolation of H10N7) avian IAV; the observed prevalence of IAV infection as determined by virus isolation (0.6%) was found to be low but consistent with prevalence estimates for other wintering duck species elsewhere in the Americas [ 7 , 33 , 34 , 35 ]. However, the NP antibody prevalence described in this study was substantially lower than that observed in mallard and teal species collected at sites in Louisiana at the same time of year (average 65%, 2018–2019; unpublished data).…”

“…Low apparent seroprevalence in these resident WD may represent limited lifetime exposure to IAV due to this species’ limited geographic range within waterfowl wintering habitats in North America; this is supported by the low overall seroprevalence in adult (AHY) BBWD in this study (12.5%, average). Unlike mallard and teal species, WD are not present on traditional waterfowl breeding and staging areas during fall migration where IAV prevalence is consistently at its highest [ 34 ]. Disparate behavior and foraging strategies, largely localized movement, single species flocks, and differential susceptibility to IAV may also limit IAV exposure and play a role in the limited detection of antibodies we report in this resident species.…”

Genomic Evidence for Sequestration of Influenza A Virus Lineages in Sea Duck Host Species

“…Due to the implications of avian-origin IAV, wild bird populations, especially waterfowl, have historically been a focus for influenza surveillance efforts. However, waterfowl species are surveilled at different intensities [ 11 ]. Because some subtypes are recovered more frequently from certain species of wild bird [ 12 ], it can create a bias that makes certain subtypes appear rarer than others.…”