Avian influenza virus risk assessment in falconry

Human infections with avian influenza viruses have been reported for the subtypes H5, H7, and H9 [1]. Siembieda et al. [2] determined an eight-time higher risk for waterfowl hunters to come into contact with AIV compared to non-hunters. Dishman et al. [3] found that duck hunters were engaged in several practices that could expose them to AIV infected wildlife. Gill et al. [4] detected antibodies against AIV subtype H11 in 1 out of 39 tested waterfowl hunters. Falconers might even be at higher risk, since hunting with falconry birds represents a selective hunting style, meaning sick, easy to catch birds are caught at a higher frequency [5]. Potentially, such birds could suffer from an AIV infection [6]. Besides natural infections of free ranging birds of prey with highly pathogenic (HP) H5N1 virus [7], the first case of HP H5N1 infection in a captive falconry bird occurred in a Saker falcon in Saudi Arabia [8], followed by the culling of 37 falconry birds after confirmation of H5N1 infections in 5 falcons [9]. In 2007, H5N1 was transmitted to 10 falconry birds with direct hunting contact to infected Houbara bustards [10]. The close contact of falconers to falconry birds and their prey could pose an enhanced risk of infection with AIV to the falconer. Moreover, because falconers also come into contact with human influenza virus strains, they might contribute to the development of new pandemic virus strains should there be a co-infection with human influenza viruses. To investigate the risk of AIV transmission from falconry birds and their prey to falconers and to assess falconers in Germany as a risk group, we conducted a field study to evaluate the prevalence of AIV in falconry birds and their captured prey as well as the occurrence of antibodies against several AIV subtypes in falconers. Membership figures of the largest German falconry association, "Deutscher Falkenorden" indicate approximately 1500 falconers in Germany. This figure correspond to generally all falconers, but the number of falconers who actually go hunting with raptors, and therefore might fall into a risk group, is much smaller and ranges about 500 to 600 falconers. Of these about only 100 - 200 are actively hunting avian prey whereas most of them are hunting small mammals like rabbits and hares. For our study, 43 active falconers provided one serum sample and took tracheal and cloacal swabs from 1080 prey birds during 2 hunting seasons (September through March 2006/2007 and 2007/2008). The geographical range covered by the falconers comprised 11 out of 16 federal German states with a focus on north-west Germany, namely the federal states Lowers Saxony and North Rhine Westphalia (51.2% of falconers). The falconers captured the prey birds with 54 falconry birds in 14 out of 16 federal states in Germany, again with a focus on Lowers Saxony and North Rhine Westphalia (80.5% of prey samples). Sampled prey species comprised 759 raven crows (Corvus corone corone, 70.3%), 89 common pheasants (Phasianus colchicus, 8.2%), 74 gulls (Laridae, 6.9%), 59 grey partridges (Perdix perdix, 5.5%), 53 ducks (Anatidae, 4.9%), 31 black-billed magpies (Pica pica, 2.9%), 7 common wood pigeons (Columba palumbus, 0.6%), 6 common coots (Fulica atra, 0.6%) and 2 Egyptian geese (Alopochen aegyptiacus, 0.2%). The falconers were instructed to take dry swab samples immediately after their falconry bird killed the prey and to keep the samples chilled during transport. Samples were sent within a period of seven days to our institute, meanwhile stored refrigerated. At our institute, the samples were stored at -80°C until processed. Swabs were investigated by virus isolation in SPF embryonated chicken eggs as described by OIE [11] and by molecular methods: RNA was firstly screened for the presence of Influenza A virus RNA as described by Spackman et al. [12], using primers modified by Hoffman. In case of a positive result, samples were further characterized by real time RT-PCR for subtypes H5, H6 and H9 and nested RT-PCR for H7 as described by others [13–15]. Further subtyping was carried out at the Friedrich Loeffler Institute (Insel Riems, Germany) using microarray analysis [16].

In conclusion, we were able to show that the AIV prevalence of prey birds from falconry is generally low, both in randomly selected sampled birds from the wild bird monitoring program, and also in actually hunted prey birds. We were also able to show that falconry birds that come into contact with AIV through their prey do not necessarily become infected. A reason for this could be that in most cases falconry birds are not allowed to eat the whole prey after the hunt, but after a short time are offered an alternative prey, such as dead chicken or mice, so that the falconer can take the catch. This short duration might not be long enough for infection. Concerning free ranging raptors the risk of infection would be higher, since these usually feed on the whole prey animal and infections of carnivores feeding on H5N1 infected animals have been reported in literature [10, 19]. We were unable to investigate 3 falconry birds, because of accidents or non-return to the falconer during the study period. According to the falconers, these birds did not show any signs of disease until the point when they resigned from the study. Thus, infection with HPAIV H5N1 for these birds seems unlikely since Lierz et al. [20] showed that falcons are highly susceptible to HPAIV H5N1. All serum samples from the falconers showed positive results using the competitive multi-species Influenza A-ELISA. Since this method detects antibodies against all influenza A viruses regardless if of avian or human origin, this result is most likely due to previous contact to human influenza A viruses of the subtypes H1 and H3 through infection or vaccination. The following investigation using microneutralization assay to detect antibodies against subtypes H5 and H7 as well as the screening of the sera for antibodies against subtypes H9 and H13 using HI gave negative results. Currently falconers do not seem to carry a higher risk for getting infected with AIV through the handling of falconry birds and their prey.