The Veterinary Quarterly | 2019
Role for migratory domestic poultry and/or wild birds in the global spread of avian influenza?
Abstract
Recently, the Dutch bird migration atlas has been launched (https://vogeltrekatlas.nl) based on more than 13 million ring recovery data obtained during the previous 100 years. As such it is a very valuable source on information regarding bird migration. Within veterinary medicine bird migration is nowadays frequently associated with avian influenza (AI). However, AI virus strains have been circulating and diversifying in wild bird populations for at least the last 100 years (Lycett et al. 2019). AI viruses in particular highly pathogenic avian influenza (HPAI) [or previously called ‘fowl plague’] viruses form a continuous threat to the poultry industry, public health, and to some wild bird species (van den Brand et al. 2018). For instance, it has been estimated that up to 11–39% of the wintering population of peregrine falcons (Falco peregrinus) in the Netherlands might have died due to HPAI A/H5N8 virus strains during autumn–winter 2016–2017 (Kleyheeg et al. 2017). Sporadic infections of humans with a limited number of avian virus subtypes (H5, H6, H7, H9, H10) have been known to occur directly from avian sources, but without as yet leading to sustained human to human transmission (Yuen et al. 1998, Koopmans et al. 2004, Fouchier et al. 2004, Shi et al. 2013, Parry 2013, Chen et al. 2014, Bui et al. 2017, Lycett et al. 2019). Typically, these infections are severe in humans, often causing death (Lycett et al. 2019) including the regrettable death of a veterinarian from pneumonia after infection with AI A/H7N7 virus. The 57-year-old veterinarian became ill within days of visiting a poultry farm hit by an AI outbreak (Sheldon 2003). It has been stated that direct transmission of the virus from wild birds to humans appears to be very rare (or non-existent), presumably due to the low frequency of contact between the two populations. However, transmission from domestic avian species to humans does occur, especially in live bird markets in Asia (Lycett et al. 2019). Of course, it is important not to confuse the threat posed by HPAI with that of a human flu pandemic (Sheldon 2005). In 1918, a H1N1 strain of influenza A virus, the ‘Spanish flu’, caused a human pandemic resulting in the deaths of 50 million people. Since then, three other human influenza A virus pandemics have occurred: H2N2 in 1957 (‘Asian flu’), H3N2 in 1968 (‘Hong Kong flu’), and H1N1 again in 2009 (‘swine flu’)(Lycett et al. 2019). It has been suggested that the human H2N2 and H3N2 pandemic viruses might have had an avian origin on the basis of antigenic crossreactivity (Pereira et al. 1967). However, the subsequent two human pandemics (H2N2 in 1957 and H3N2 in 1968) were not caused by completely avian-origin viruses, but were rather reassortant viruses with avianorigin HA, PB1 polymerase and (for the 1957 pandemic) NA segments (Kawaoka et al. 1989, Bean et al. 1992, Sch€afer et al. 1993, Joseph et al. 2015, Lycett et al. 2019). The 2009 H1N1 ‘swine flu’ pandemic was a result of reassortment between different strains of influenza A virus that had been circulating in swine for at least 10 years (Smith et al. 2009, Lycett et al. 2019). Since the emergence of the HPAI A/H5N1 virus in poultry in China in 1996, H5 HPAI viruses that share a common ancestral virus strain (A/goose/Guangdong/ 1/96 [GsGd]) have continued to cause outbreaks in poultry (Duan et al. 2008). The hemagglutinin (H) gene of the HPAI A/H5N1 virus diversified into multiple genetic lineages (“clades”). More recently, reassortment between the HPAI A/H5N1 virus and the low pathogenic avian influenza (LPAI) viruses resulted in HPAI viruses with neuraminidase (N) genes (N1, N2, N5, N6, and N8) and other genes of LPAI virus origin (Zhao et al. 2012, Liu et al. 2013, Zhao et al. 2013, Wong et al. 2015). From China, H5 GsGd virus has been introduced to other Asian countries, the Middle East, Africa, and Europe. Within Europe, HPAI A/H5N1 GsGd virus has been detected in multiple countries in 2004 (clade 1), 2005/2006/2007 (clades 2.2 and 2.2.1), and 2008/2009/ 2010 (clade 2.3.2)(Cattoli et al. 2009, Reid et al. 2011). In November and December of 2014, the HPAI A/H5N8 GsGd virus (clade 2.3.4.4, group A, Buan-like)(Jeong et al. 2014) was detected in various countries of Asia, Europe, and for the first time North America (van den Brand et al. 2018). HPAI A/H5N6 virus as a novel reassortant of the H5N8 clade 2.3.4.4 group B viruses (Beerens et al. 2018) was first detected at the Russia Mongolia border in May 2016 (Beerens et al. 2019). Remarkably, the first detection of HPAI A/H5N6 virus in the Netherlands as well as in Europe (Beerens et al. 2018) was on a commercial farm notably keeping meat ducks no sooner than on December 7, 2017 (Beerens et al. 2019). HPAI is essentially a poultry disease (van den Brand et al. 2018). The intranasal inoculation with A/chicken/ Hong Kong/220/97 (A/H5N1) influenza virus in chicken