Highly (H5N1) and Low (H7N2) Pathogenic Avian Influenza Virus Infection in Falcons Via Nasochoanal Route and Ingestion of Experimentally Infected Prey

Kateri Bertran,Jorge García De La Fuente,Taiana Costa,David Solanes,Natàlia Majó,Núria Busquets,Iván Cordón,Roser Dolz,Francesc Xavier Abad,Todd Davis

doi:10.1371/journal.pone.0032107

Kateri Bertran, Jorge García De La Fuente + Show 8 more

Open Access

https://doi.org/10.1371/journal.pone.0032107

Copy DOI

Abstract

An experimental infection with highly pathogenic avian influenza (HPAI) and low pathogenic avian influenza (LPAI) viruses was carried out on falcons in order to examine the effects of these viruses in terms of pathogenesis, viral distribution in tissues and viral shedding. The distribution pattern of influenza virus receptors was also assessed. Captive-reared gyr-saker (Falco rusticolus x Falco cherrug) hybrid falcons were challenged with a HPAI H5N1 virus (A/Great crested grebe/Basque Country/06.03249/2006) or a LPAI H7N2 virus (A/Anas plathyrhynchos/Spain/1877/2009), both via the nasochoanal route and by ingestion of previously infected specific pathogen free chicks. Infected falcons exhibited similar infection dynamics despite the different routes of exposure, demonstrating the effectiveness of in vivo feeding route. H5N1 infected falcons died, or were euthanized, between 5–7 days post-infection (dpi) after showing acute severe neurological signs. Presence of viral antigen in several tissues was confirmed by immunohistochemistry and real time RT-PCR (RRT-PCR), which were generally associated with significant microscopical lesions, mostly in the brain. Neither clinical signs, nor histopathological findings were observed in any of the H7N2 LPAI infected falcons, although all of them had seroconverted by 11 dpi. Avian receptors were strongly present in the upper respiratory tract of the falcons, in accordance with the consistent oral viral shedding detected by RRT-PCR in both H5N1 HPAI and H7N2 LPAI infected falcons. The present study demonstrates that gyr-saker hybrid falcons are highly susceptible to H5N1 HPAI virus infection, as previously observed, and that they may play a major role in the spreading of both HPAI and LPAI viruses. For the first time in raptors, natural infection by feeding on infected prey was successfully reproduced. The use of avian prey species in falconry husbandry and wildlife rehabilitation facilities could put valuable birds of prey and humans at risk and, therefore, this practice should be closely monitored.

Highlights

Avian influenza (AI) is one of the most important biological threats, for poultry and for other avian species and humans [1,2]
AI typically courses as an asymptomatic infection in wild birds, recent highly pathogenic avian influenza (HPAI) epidemics resulted in unprecedented high mortality rates for certain wild bird species
It is worth highlighting that Hong Kong had a series of cases of natural infection of peregrine falcons (Falco peregrinus) with H5N1 in 2004, 2006 and 2008 [9,10,11], other countries subsequently reported HPAI cases in different prey species, such as in Hodgson’s hawk eagles (Spizaetus nipalensis) in Belgium [12], saker falcons (Falco cherrug) in Saudi Arabia [13] and, more recently in Saudi Arabia, houbara bustards (Chlamydotis undulate macqueenii),which interestingly infected falcons that came into contact with them [14]

Summary

Introduction

Avian influenza (AI) is one of the most important biological threats, for poultry and for other avian species and humans [1,2]. Susceptibility to AI viruses varies greatly among wild bird and poultry species, as well as their possible role as vectors or reservoirs [3,4]. Gallinaceous poultry are considered to be highly susceptible, whereas waterfowl have long been recognized as natural reservoirs, they may show variable morbidity depending on the infective viral strain [5,6]. AI typically courses as an asymptomatic infection in wild birds, recent highly pathogenic avian influenza (HPAI) epidemics resulted in unprecedented high mortality rates for certain wild bird species. It is worth highlighting that Hong Kong had a series of cases of natural infection of peregrine falcons (Falco peregrinus) with H5N1 in 2004, 2006 and 2008 [9,10,11], other countries subsequently reported HPAI cases in different prey species, such as in Hodgson’s hawk eagles (Spizaetus nipalensis) in Belgium [12], saker falcons (Falco cherrug) in Saudi Arabia [13] and, more recently in Saudi Arabia, houbara bustards (Chlamydotis undulate macqueenii),which interestingly infected falcons that came into contact with them [14]

Methods

Results

Conclusion