Challenging the conceptual framework of maintenance hosts for influenza A viruses in wild birds

Abstract

The conceptual framework considering Anseriformes and Charadriiformes as the main maintenance hosts for influenza A viruses (IAV) in wild birds has shaped IAV research and surveillance over the last decades. We challenge this framework by reviewing the world-wide surveillance data on non-Anseriformes and non-Charadriiformes (NANC) species, generally considered as playing little role in IAV maintenance, available in literature and online data bases (close to 200 sources). Globally, we found an IAV infection rate of 1·51% (95% CI, 1·44–1·59%) for c. 101 000 birds tested from NANC species. If Anseriformes have, as expected, a higher infection rate than any other bird orders, eight bird orders have an infection rate higher or close to the Charadriiformes infection rate, challenging the status of Charadriiformes. We interpret the attention paid in favour of Charadriiformes by an extrapolation bias from data collected in hotspots of IAV infection in Charadriiformes (e.g. Delaware Bay, USA). The growing data on IAV in wild birds world-wide, summarised here, support two non-exclusive hypotheses: (i) the quality of the diagnostic tools and techniques used explain the patterns observed; (ii) IAV maintenance is determined by complex multi-host systems composed of multiple bird species, dependent on the ecosystem and its bird diversity and composition. Synthesis and applications. Our results have two main implications. First, new research and surveillance should be designed in order to understand influenza A viruses ecology in wild birds across the world, along with appropriate diagnostic tools and new hypotheses and dedicated protocols. This should be done in line with our new conceptual framework that conveys less a priori than its predecessor. Second, our results call for more bridging between biological and epidemiological sciences in order to tackle disease ecology in multi-host systems. (Résumé d'auteur

The roles of migratory and resident birds in local avian influenza infection dynamics

“…In spite of AIV infection dynamics being arguably one of the best studied avian‐wildlife host–pathogen systems, our study highlights that we typically lack crucial information allowing identifying and quantifying the major mechanisms that lead to high prevalence levels in cases where migrants are involved; that is, data on the number and turnover of migrants in a bird population. Thus, besides maintaining efforts in virus sampling and growing our understanding of virus diversity and evolution, their temporal occurrence and host range (Caron et al., ; Munster et al., ; Olsen et al., ) we additionally need increased efforts in recording of host demography. Given the here revealed importance of migration, and notably the timing and strategy of migration, it appears crucial to extend the wildlife disease surveillance database with demographic features such as the timing of birth and density, as well as turnover.…”

“…The poultry industry and trade is an important part of this problem, with some highly pathogenic AIV strains being endemic in poultry in several countries in Africa and Asia, where also low pathogenic AIV is sometimes more readily circulating among domestic than wild birds (Hassan, Hoque, Debnath, Yamage, & Klaassen, 2017). Irrespectively, wild birds and notably birds of the order Anseriformes (ducks and geese) are the ancestral reservoir host for AIV (Caron, Capelle, & Gaidet, 2017) and remain of key importance for global AIV diversity (Alexander, 2007), notably in the face of readily reassorting high pathogenic AIV virus such as H5 clade 2.3.4.4 (Lee, Bertran, Kwon, & Swayne, 2017). Anseriformes also play a major role in the dispersal of AIV (Alexander, 2007), including dispersal of highly pathogenic strains (e.g.…”

“…Thus, besides maintaining efforts in virus sampling and growing our understanding of virus diversity and evolution, their temporal occurrence and host range (Caron et al, 2017;Munster et al, 2007;Olsen et al, 2006) we additionally need increased efforts in recording of host demography. Given the here revealed importance of migration, and notably the timing and strategy of migration, it appears crucial to extend the wildlife disease surveillance database with demographic features such as the timing of birth and density, as well as turnover.…”

Avian influenza viruses at the wild–domestic bird interface in Egypt

“…On the offshore islands; gulls, terns and herons breed in large colonies. Gulls and terns may conduct longer foraging trips inland during the breeding season that may affect AIV epidemiology locally [35][36][37][38][39]. The wetlands are most important for AIV epidemiology due to aggregation of waterfowl, gulls and shorebirds [40] (Figure 1).…”

Highly Pathogenic Avian Influenza H5N1 (HPAI/H5N1) Virus Search from Wild Birds in Ghana

“…Globally, wild birds play an important role in the ecosystem such as, forest regeneration through plant pollination and seed dispersal and provide ecotourism [15]. Wild birds are natural reservoirs for avian influenza (AI) viruses and play a major role in the evolution, maintenance, and spread of AI viruses [2,14]. They host a wide diversity of subtypes, and provide a dynamic population for viral evolution and transmission to domestic flocks and mammals (12).…”