A brief history of bird flu

Abstract

In 1918, a strain of influenza A virus caused a human pandemic resulting in the deaths of 50 million people. A century later, with the advent of sequencing technology and corresponding phylogenetic methods, we know much more about the origins, evolution and epidemiology of influenza epidemics. Here we review the history of avian influenza viruses through the lens of their genetic makeup: from their relationship to human pandemic viruses, starting with the 1918 H1N1 strain, through to the highly pathogenic epidemics in birds and zoonoses up to 2018. We describe the genesis of novel influenza A virus strains by reassortment and evolution in wild and domestic bird populations, as well as the role of wild bird migration in their long-range spread. The emergence of highly pathogenic avian influenza viruses, and the zoonotic incursions of avian H5 and H7 viruses into humans over the last couple of decades are also described. The threat of a new avian influenza virus causing a human pandemic is still present today, although control in domestic avian populations can minimize the risk to human health. This article is part of the theme issue 'Modelling infectious disease outbreaks in humans, animals and plants: approaches and important themes'. This issue is linked with the subsequent theme issue 'Modelling infectious disease outbreaks in humans, animals and plants: epidemic forecasting and control'.

Keywords: avian influenza virus; epidemiology; pandemic; phylogenetics; zoonotic.

Figure 1.

PB2 phylogeny of a stratified sample of all influenza subtypes. Tips in the circular neighbour-joining tree are coloured by host: blue, avian; pink, swine; orange, human; green, canine; brown, equine; purple, bat. The rings from inner to outer are: host-type, haemagglutinin subtype (H-type), neuraminidase subtype (N-type) and continent of isolation. The tree shows (clockwise) bats at the root, the avian—Eurasian lineage with many subtypes, human seasonal H1N1, H2N2 and H3N2 spread through all the continents, H1N1, H1N2, H3N2 swine influenza, the H1N1 pandemic swine influenza lineage in humans and swine, and the avian—Americas lineage with many subtypes.

Figure 2.

Cartoon depicting post-translational processing of a linear HA monomer. HA1 and HA2 domains are indicated, as is the linking disulfide bridge. Red boxes indicate hydrophobic regions involved in membrane interactions. Example cleavage sequences from low and high pathogenicity H5 viruses are shown.

Figure 3.

Example of a time-scaled phylogenetic tree with tips coloured by host-type and the discrete trait host model (a); and the same tree mapped into space with continuous spatial coordinates with tips coloured by subtype (b).

Figure 4.

Flyways of migratory water fowl. Flyways run approximately north–south, and also overlap in northern regions, including in Siberia, Greenland, Alaska and across the Bering straits, which allows occasional transmission of influenza viruses between North America and Eurasia. Flyways from http://wpe.wetlands.org/Iwhatfly.

Figure 5.

Time-scaled tree of a stratified subsample of H5 segment 4 (HA). The tree represents the known diversity of LPAI (blue branches) and HPAI (red branches). Tips are represented as circles and coloured by neuraminidase subtype from H5N1 (red) to H5N9 (magenta).