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H5N1 HPAI in Different Species

3.5 Wild Birds and H5N1 HPAI

Wild aquatic birds have been incriminated in a number of outbreaks of HPAI as the source of LPAI viruses that subsequently converted to highly pathogenic strains in poultry (see Table 2.1 and Swayne and Suarez, 2000). However until the emergence of Asian-lineage H5N1 HPAI viruses, wild birds were not regarded as a primary source of HPAI viruses.

Until 2002, only a few individual dead wild birds infected with HPAI viruses had been detected and only one outbreak of HPAI (H5N3) involving multiple wild common terns (Sterna hirundo) in South Africa in 1961 had been reported [Becker, 1961]). H5N1 HPAI has changed the way we view wild birds and HPAI – not only have numerous wild birds been killed by H5N1 HPAI viruses, but the evidence presented in Chapter 2 strongly suggests that they have played a role in the long-distance spread of these viruses.

As discussed in Chapter 2, cases in dead wild birds have been identified for which no association with poultry has been found, including a range of species in Europe and wild water birds in Mongolia. Although the source of these viruses is not known and they may have been derived originally from poultry, it has been possible through a process of elimination to rule out poultry or items related to poultry as the direct route of introduction.

Infected dead ‘wild’ birds have also been found in Hong Kong SAR where domestic poultry in commercial farms have remained free from infection since 2003 (AFCD, 2006; AFCD, 2007). Some of these infected wild birds could have been part of shipments of captured birds imported largely for religious functions. The current evidence for this is circumstantial, based on the species affected and the locations where the dead birds were found (Young, 2007). Viruses isolated from dead free-flying birds in Hong Kong SAR in 2006 and 2007 differ genetically from those detected in poultry in 2002-03 (OIE, 2006b) indicating that these were not derived from earlier outbreaks in poultry. It is also extremely unlikely that these were derived from the few remaining small flocks of backyard poultry given the very low number of such birds in Hong Kong SAR.

Ornithologists have pointed out that the timing and pattern of disease outbreaks in poultry do not always coincide with known migratory patterns (Bird Life International, 2006). Although this is true, it does not reflect the fact that bird movements are not as precise as existing maps suggest (EFSA, 2006). This was demonstrated by the apparently aberrant movement of water birds in the northern winter of 2005-06, associated with freezing conditions around the Black Sea. Many birds are nomadic, moving in accordance with availability of feed and water, rather than long-distance migrants following strict patterns of movement (see for example Tracey et al, 2004; EFSA, 2006). This could possibly explain some of the movement of virus that has occurred but which does not fit with accepted ‘normal’ migratory patterns.

In addition, coincidence of infections in poultry with times of migration is not essential because amplification of virus in resident wild birds or domestic ducks could occur before virus spreads to domestic chickens and infection becomes apparent. Delays between introduction of infection by wild birds and infection in poultry has been demonstrated with LPAI viruses in farmed turkeys in Minnesota, United States, in the early 1980s where there was an apparent lag between introduction of the viruses by wild ducks and subsequent infection of the turkeys (Halvorson et al, 1985).

Despite intensive surveillance of wild birds, only a few 'healthy' wild birds have been found to be infected with H5N1 viruses – most have been found sick or dead. The infected live birds include at least one grebe from Siberia in 2005 (Lvov et al, 2006), healthy swans from Poland in 2006 (Minta et al, 2006) and a total of six out of 4 300 wild ducks found in Poyang Lake, China, in early 2005 (Chen et al, 2006c). It is worth noting that had the viruses from the Poyang Lake ducks (species not identified) reassorted they could have produced a virus similar to that found in dead and dying birds in Qinghai, China, in May 2005 (Chen et al, 2006c). In addition, healthy tree sparrows (Passer montanus) were found to be infected with a novel genotype of HPAI H5N1 virus in China in 2004 (Kou et al, 2005).

The difficulty in detecting virus-positive live birds could relate to the very low prevalence of healthy carriers. Based on experimental information involving a limited range of species, most birds infected with H5N1 HPAI viruses do not excrete virus for more than a few days, although some ducks will excrete virus for several weeks. It may also reflect sampling inadequacies given that current HPAI viruses are excreted at lower levels by the cloacal route than the respiratory route in experimentally-infected mallards, although in at least one duck in this study, cloacal excretion extended over a longer period (Hulse-Post et al, 2005).

It is also evident that wild birds can be infected by poultry, as was seen in large-billed crows (Corvus macrorhynchos) in Japan (2004) possibly scavenging on chickens that died from H5N1 infection (Nishiguchi et al, 2005) and most likely with hooded vultures (Necrosyrtes monachus) in Burkina Faso in 2006 (Ducatez et al, 2007). The infected crows in Japan were found for up to 30 days after the farm cases ceased. Most of these were probably infected after scavenging dead poultry but the possibility of a short-term independent cycle of infection in the crows cannot be ruled out.

Much remains unknown about the survival of H5N1 HPAI viruses in wild bird populations, including the important question of whether infection is sustained in these without replenishment from other sources, especially infected domestic poultry. Since 2005, only H5N1 viruses of subclade 2.2 have been detected in wild birds and poultry to the north and west of China, and in Japan and the Republic of Korea, despite the detection of a range of other clades and subclades in poultry in China and other parts of eastern Asia.

H5N1 HPAI viruses have been detected in many parts of the Palaearctic, so the persistence of virus in water over the northern winter in colder areas remains a possibility. This has been proposed as one of the methods of survival of other avian influenza viruses from year to year (Stallknecht, 1997), with the alternative being that viruses continue to circulate year round at low levels in wild bird (duck) populations. If the former occurs, healthy migratory birds returning to infected locations could pick up residual viruses that have survived over the cold months. Either of these infection pathways would hinder attempts at global eradication of Asian-lineage H5N1 HPAI viruses.

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