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H5N1 HPAI in Different Species

3.4 Other Poultry and H5N1 HPAI

A wide range of other poultry is produced and sold in Asia and elsewhere. This includes quail, pheasants, guinea fowl, partridges, pigeons, muscovy ducks and turkeys. The precise role of these species in the evolution, persistence and transmission of Asian-lineage H5N1 HPAI viruses remains poorly understood because little research has been carried out. Many of these birds are raised in small numbers together with chickens, ducks and geese in smallholder and village flocks, and are also sold together with other poultry in live-poultry markets, providing opportunities for cross-species infection.

Quail (Coturnix spp.) have attracted considerable attention because the internal genes of the H5N1 HPAI viruses from Hong Kong in 1997 were similar to those found in an H9N2 virus in quail (Guan et al, 1999). This suggested a possible role for this species in the evolution of the Hong Kong/97 genotype HPAI virus. Quail were also among the first avian species in which it was recognised that greater quantities of influenza virus could be excreted via the respiratory tract than in faeces, in contrast to earlier findings with avian influenza viruses in aquatic avian species (Liu et al, 2003). Outbreaks of H5N1 HPAI have been reported in quail in several countries, including Indonesia and Viet Nam. Experimentally, quail are highly susceptible to infection with H5N1 HPAI viruses (Perkins and Swayne, 2001).

It is no longer allowed to sell quail in live-poultry markets in Hong Kong SAR due to concerns about their role as a potential source of other influenza viruses that could reassort with H5N1 viruses. Quail are also known to be able to support growth of swine influenza viruses (Makarova et al, 2003).

Experimentally infected domestic pheasants (Phasianus colchinus) have the capacity to excrete some low pathogenicity avian influenza viruses for an extended period of time (>45 days) even in the face of antibodies to the virus. This has been associated with selection of antigenic variants during the infection process (Humberd et al, 2007), but it is unlikely that this also applies to H5N1 HPAI viruses (experimental inoculation of pheasants with a Hong Kong/97 H5N1 HPAI virus strain resulted in the death of all inoculated birds in 2.5-4 days [Perkins and Swayne, 2001]).

Little information is available on Asian-lineage H5N1 HPAI viruses in domestic guinea fowl (Numida meleagris) and partridges (Alectoris spp.). Guinea fowl experimentally inoculated with a Hong Kong/97 HPAI virus all died within five days (range 2-5 days, mean 2.5 days) (Perkins and Swayne, 2001). Some dead partridges naturally infected with H5N1 HPAI viruses were detected in Hong Kong SAR in 1997 (Sims, unpublished). In one experimental study using a Hong Kong SAR H5N1 HPAI virus from 1997, not all inoculated partridges died and those that died lived longer (4-6.5 days, 70 percent mortality) than other gallinaceous species inoculated with the same strain of virus. No virus was detected in the surviving birds 14 days after inoculation suggesting that they were not long-term virus shedders (Perkins and Swayne, 2001).

Domestic pigeons (Columba spp.) were largely resistant to infection with an H5N1 HPAI virus isolated from Hong Kong in 1997 (Perkins and Swayne, 2002) but infection and disease have been recorded in these birds with more recent H5N1 HPAI viruses both naturally and experimentally. Nevertheless, pigeons appear to be more resistant to infection than many other avian species (Boon et al, 2007; Werner et al, 2007) with high experimental challenge only resulting in development of neurological signs in some 20 percent of experimentally infected birds in one study (Klopfeisch et al, 2006). One recent study in China concluded that pigeons were resistant to infection using five different H5N1 HPAI isolates (Liu et al, 2007).

Clinically- and subclinically-infected muscovy ducks (Cairina moschata) have been detected in a number of countries including Viet Nam.  Experimental infection of young muscovy ducks led to the development of neurological signs (Steensels et al, 2007).Virus shedding was detected up to 19 days after infection. Because these birds are often used as surrogate hens for hatching eggs in village flocks, they could, if subclinically infected, pass virus onto chicks when they hatch.

Turkeys (Meleagris gallopavo) appear to be inordinately susceptible to infection with avian influenza viruses based on the apparent disproportionate number of cases of avian influenza (including H5N1 HPAI) in Europe involving turkey farms (see for example Capua et al,2003), They do not survive for more than a few days after experimental infection (Perkins and Swayne, 2001). As with other poultry species, turkeys incubating H5N1 HPAI virus may not show clinical signs. In the early stages of an outbreak, this could potentially lead to the inadvertent dispatch to slaughter of poultry containing infected birds. This is supported by the detection in early 2007 of presumably recently infected asymptomatic poultry in barns adjacent to a clinically affected flock on a turkey farm in the United Kingdom (Defra, 2007). Turkeys are a minor species of poultry in Asia, and therefore probably played little or no role in the initial evolution and emergence of Asian-lineage H5N1 viruses.

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