Most of Birds Korea's thinking on Highly Pathogenic Avian Influenza (HPAI) H5N1 Poultry Flu remains expressed in our simple position statement (posted in mid-August 2005), found at:

• Birds Korea: Poultry Flu Position Statement

Further information and Birdlife International's position statement can be found at:

• http://www.birdlife.org/action/science

With additional (lively!) discussion and opinion at:

• http://www.drmartinwilliams.com/forum

This extended note aims to add some further history and perspective to our own position statement, as well as summarizing some recent information. It is written following:

1. Outbreaks of poultry flu in summer 2005 affecting wild birds, recorded in Qinghai, China; in Novosibirsk, Southern Siberian Russia, and in Mongolia.

2. Other outbreaks that appear to have affected poultry, rather than wild birds or wild birds and poultry;

3. Hugely increased interest in poultry flu in Europe (and to some extent in the US) since late August, provoked largely by media reports of outbreaks “moving west towards Europe carried by migrant birds”, reportedly carrying with them the 'probability' of a massive human flu pandemic;

4. The announcement by authorities in Finland, largely unreported in the same media, that an outbreak there affecting 100 gulls in August was not H5N1 (see: http://www.helsinginsanomat.fi/english/article

It is presented in Birds Korea's belief that (for now at least) poultry flu does NOT present an inevitable and pandemic-scale threat to human health; and in that it is not migratory birds but rather the poultry industry and poultry farms (as well as the cage bird culture) that remain the main source of the problem and its solution.

However, it is apparent from postings on various listservers and website forums, and by many media accounts, that the H5N1 virus is being repeatedly identified with both (1) migratory birds and (2) the next human flu pandemic. This identification in itself raises several potentially significant (long-term) concerns that need to be addressed clearly, logically and honestly by conservation organizations and birdwatchers. Birds Korea believes that:

1. If wild birds are repeatedly blamed as vectors of the disease, even though no/few outbreaks occur that are actually caused by wild birds, then culls of wild birds from affected areas (e.g. “Asia”) could become much more likely. Governments will have little option but to order culls if confronted by influential media, civil society or other agents of the state, with the false argument: “Protect either people or birds.”

2. Popular positive attitudes towards wild birds in many areas could worsen (replaced by fear), and support in such areas for wild bird conservation could diminish;

3. Some/many waterbird-rich wetlands could become closed to the public; wetland reserves could be closed, and even lose their protected status (or have their ecological character altered), especially when close to centres of human population.

4. Wetlands and waterbirds could become increasingly associated with disease;

5. Sites where wild birds and domesticated birds occur together with regularity and for conservation purposes, such as centres run by e.g. the Wildfowl and Wetlands Trust in the UK, could lose significant revenues – long-term damaging their education and research programs, hindering their capacity to add an informed voice to the debate on poultry flu, and weakening existing region-wide conservation strategies;

6. With the focus not falling clearly on the poultry industry and on wild bird markets, the disease will likely be able to persist for longer and more harmfully, to the long-term detriment of both affected bird populations and humans.

With this as background, this Poultry Flu Update is presented in the form of 14 key statements, supported in most cases by detailed examples and references, from published sources; from postings on the Pro-med website; from information contained in AVI Bulletins; and from correspondence with specialists (including members of the Wildlife Conservation Society that investigated the H5N1 outbreak in Mongolia).

It has also benefited greatly from the input of Dr. Martin Williams in Hong Kong (who along with Dr. William Karesh read some sections of the update during the drafting process).

Not all the mass of information recently received/reviewed on poultry flu is reproduced here in full (of course!), due to time and space constraints, and therefore some basic understanding of the disease and the outbreaks is taken as understood. Obviously too, the statements also clearly reflect Birds Korea's own conservation-oriented mandate and beliefs.

As always, we welcome any corrections or additional information; and respectfully urge responsible journalists and decision-makers to seek out additional information from further specialist sources.

NB: All bird species names are as used in the Birds Korea checklist (at: Birds Korea: Checklist).

Birds Korea - Fourteen Key Statements: Poultry Flu is about poultry!

1. While Low Pathogenic Avian Influenza is widespread in some types of wild bird (especially waterbirds, most notably ducks and geese), outbreaks of HPAI are extraordinarily rare in wild birds, with only one case recorded prior to 2005 where infected wild birds were believed to have had no connection with infected poultry - that an outbreak of H5N3 in Common Terns in South Africa back in 1961 (Alexander, 2000).

2. Past outbreaks of HPAI in poultry, however, have a very long history. They were first described back in 1878 as “fowl plague.” Between 1959 and 2000, there were at least 17 primary outbreaks of HPAI in poultry, with 8 such outbreaks between 1990 and 2000 (Alexander, 2000).
   Poultry, here defined as domesticated chickens, ducks, geese and turkey, are simply not meant to be "housed" in the unnatural conditions in which they find themselves (see also: effectmeasure.blogspot.com/2005/02/bird-flu-and-bird-farms).

   This has led Birds Korea to coin the term “Poultry Flu” as a popular name to describe (at this time especially) “Highly Pathogenic Avian Influenza Type A H5N1”, to focus greater attention on the poultry industry and poultry farmers in the evolution, spread and prevention of this disease (see also: medicalnewstoday.com/medicalnews).

   As noted by science author Wendy Orent (in lit., September, 2005):

   • “we should distinguish between ordinary avian and poultry flu! Poultry flu, to me, is flu that's adapted to spread among - and often kill - chickens and other domestic birds. It's been subjected to unique selection pressures that have to do with how the chickens are raised. It has no more in common with avian flu than a white leghorn has with a red jungle fowl!”

3. The first known case of H5N1 was in a chicken in the UK back in 1959 (Alexander 2000). The present H5N1 outbreaks can be traced back to a "domesticated" goose in China, in 1996 (Melville and Shortridge, 2004).

4. The present strains and sub-forms of H5N1 poultry flu in Asia are all traceable back to 1996/1997: poultry flu has therefore been maintained in the vast poultry industry/trade of the region for 9 years now, often concealed.

   Such concealment is not necessarily government-driven, nor is it necessarily organized. Huge numbers of people depend economically on poultry and poultry products; and some domesticated birds have been proven to remain asymptomatic even when infected.

   A mailing to Pro-med by Joe Dudley (posted September 7th 2005, archive number 20050907.2648) states: “The data provided in the Office International des Epizooties (OIE) report of 30 Aug 2005 submitted by Thailand cited in ProMED-mail posting 20050903.2603 seem to suggest the existence -- or appearance -- of possible resistance to H5N1 in one or more native Thai chicken breeds. The OIE report indicates that in one reported outbreak none of the 10 infected chickens died, and in another only 5 of 15 infected chickens died. oie.int/eng/info/hebdo/aIS_55.htm#Sec3. If the phenomenon is widespread, it seems that this could indicate that native chicken flocks as well as domestic ducks are serving as reservoirs for H5N1 virus in SE Asia.”

   All of the above appears to complicate guidelines governing the resumption in trade of poultry from “previously affected” areas outlined in a Pro-med posting in March 2004 (at: ProMed: promedmail.org/pls/2400:1001):

   • “According to Article 2.1.14.2. of OIE's International Animal Health Code, ‘A country may be considered free from highly pathogenic avian influenza (HPAI) when it has been shown that HPAI has not been present for at least the past 3 years. This period shall be 6 months after the slaughter of the last affected animal for countries in which a stamping-out policy is practised with or without vaccination against HPAI.' However, countries may also declare certain zones within their boundaries to be free from HPAI. According to Article 2.1.14.3. of the Code, ‘an infected zone may become free if at least 21 days have elapsed after the confirmation of the last case and the completion of a stamping-out policy and disinfection procedures, or 6 months have elapsed after the clinical recovery or death of the last affected animal if a stamping-out policy was not practiced.' Zones declared free from HPAI after complying with the described requirements may be eligible for export of susceptible animals and/or their products, under conditions agreed upon between the exporting and importing countries.”

5. There are no known cases of transmission of poultry flu from wild birds to people, and cases of transmission from poultry to people remain very rare.

   There are 70 billion chickens alone reared annually in Asia (this according to Wendy Orent in her October 2004 piece for the LA Times, entertainingly entitled, “Be Afraid [If You're a Chicken]”); probably smaller but still huge numbers of ducks and geese for human use. However, in 9 years there have been only ca 63 recorded fatalities, in a vast region of huge human population, where in many local areas people live in very close contact with poultry.

   (Also see Wendy Orent's excellent “Chicken Little” account in September 2005, in The New Republic magazine [subscription required] at: www.tnr.com/doc.mhtml)

6. There is still no hard evidence that wild migratory birds are capable of carrying the virus long distances (though the outbreak in Mongolia suggests such a possibility), and in addition there is no evidence that wild birds are capable of spreading it to domestic poultry, let alone people. ("Craig Pringle, viral diseases moderator for ProMed Mail cautions that although the virus has been found in migratory birds, it is a leap to assume they can spread it to domestic poultry. He told New Scientist that it is possible the virus could have reached Russia and Kazakhstan through general trade routes”: New Scientist online article, August 11, 2005, at: newscientist.com/article.ns?id=dn7834).

   There is abundant evidence, however, that wild birds (and other animals) have been infected by direct or indirect contact with sick poultry.

   Approaching the outbreaks logically, it would be reasonable to assume that if wild waterbirds were the main vectors of poultry flu that:

   • Outbreaks would be very widespread and frequent, and could only be controlled through culling of infected waterbird flocks (this has not been the case up to now);

   • Outbreaks would predominantly be in areas with significant concentrations of waterbirds, even in remote areas lacking much human influence (this has not been the case up to now);

   • Testing of large numbers of apparently healthy birds would at least occasionally reveal individuals with H5N1, even away from areas with outbreaks (proving the existence of a reservoir of HPAI in wild migrant birds). It has not, up to now.

   • Patterns of outbreaks would match the distribution or migration patterns of key suspected carrier species (They do not: see statement 7 below).

   The initial outbreaks of poultry flu in Hong Kong in 1997 were eradicated by increased controls on the conditions in which various caged species were imported and held, and by the slaughter of poultry (e.g. Shortridge et al., 2000), not by the culling of wild birds.

   Following the slaughter, the H5N1/97 virus was not isolated in poultry or people in Hong Kong until a further outbreak in poultry farms in winter 2002/2003, that was again controlled through a combination of culling, quarantine and in addition vaccination of poultry (OIE, World Animal Health, Report, July 2003). The outbreaks were confined to urban areas and no live infected wild birds were found in natural habitats, even at wetlands supporting many thousands of migratory waterbirds at that time (e.g. at Mai Po).

   The very few individuals of species that contracted the virus and died, such as Grey Heron, are known on rare occasions to scavenge dead animals (at least in Korea, based on personal observations), and in Hong Kong likely inhabited waterways infected by contaminated poultry (Martin Williams, in lit., 2005).

   The virus was instead tested for and detected in poultry being imported from South-east China into Hong Kong between 1999-2002; and also in duck meat imported into South Korea (Melville, Shortridge 2004). More recent outbreaks in other areas away from Hong Kong have also been controlled, superficially at least, by poultry culls and by greater restriction of movement of poultry and caged birds.

   Furthermore, in several instances, HPAI outbreaks (including poultry flu) have been confined to poultry farms and/or have been linked back directly to bird markets (e.g. in 1986, a virus appeared in poultry in five north-east states of the USA. In each state the index cases were linked to live bird markets in New York City: Alexander, 2000). As noted by Melville and Shortridge (2004) and others,

   • “There are no reservoirs of HPAI in natural populations, suggesting high levels of pathogenicity in wild birds, in which case their role in the movement of virus would be severely limited.”

   In several cases (as in Hong Kong in 1997 and Japan in 2004) it is much more probable therefore that scavenging wild birds came into contact with infected domestic birds (or their faeces) and were infected – rather than themselves being the primary source of infection.

   In Japan in 2004, after outbreaks in a poultry farm in the south-west of Honshu, and then among bantams kept as pets in Kyushu, a large-scale outbreak at one poultry farm in yet another region of Honshu went unreported for a week, during which time it also spread to a neighboring farm (see Pro-Med mailing: ProMed: promedmail.org/pls/askus). These scattered outbreaks were not matched by outbreaks in wild birds, and again do not match the movements of any known wild bird species within Japan, instead rather better indicating the import and dispersal of infected poultry/poultry products.

   Following the outbreaks (all information per Manami Ikeda, JAWAN, in lit. August 2005) a total of nine dead infected crows were found within a 30 km radius of poultry-flu infected poultry farms in Kyoto and Osaka. As a result, the Ministry of Environment and the Ministry of Agriculture, Fisheries and Forestry ordered a nationwide virus check on crows and doves between March 16 and April 16, 2004. In total, about 18,000 dead individuals were collected and tested, but none tested positive for the virus.

   The death of these nine Large-billed Crows in Japan therefore seems most likely due to contact with contaminated poultry. Large-billed Crows are non-migratory, can be considered an “aberrant host” (e.g. Suaze, 2000), and are known to scavenge round farms and often feed on animal carcasses if available.

   In addition, no live wild birds in Japan, including Large-billed Crows, since that time have been proven to carry H5N1, despite intensive testing efforts.

   A posting to the Pro-med website by Dr. George Arzey, Senior Veterinary Officer (Avian Health), New South Wales Department of Primary Industries on September 5th 2005, also highlights the “enigma” of poultry flu being widespread in South-east Asia in areas used by migrant waterbirds, some of which then migrate on to Australia and New Zealand, while there have been no outbreaks of H5N1 in either country. Additionally, as reported by researchers there, no wild birds in either country have tested positive for H5N1 poultry flu.

   The same enigma, by extension, can be said of nations on all continents outside of Asia. All are linked by overlaps in the migration routes of a number of species. For example, Greater White-fronted Geese migrating from affected areas of South-east China, breed in northern Siberia, where they would likely come into contact with Lesser Snow Geese migrating into North America, and other geese and shorebird species migrating westward towards Europe. Despite 9 years of infection of poultry in China, H5N1 poultry flu has yet to be recorded in e.g. Western Europe (since infected turkeys in England back in 1991: Alexander 2000), or in the US.

   In addition, there is no evidence that the outbreaks themselves originated in wild birds, but rather a “practically identical” strain of poultry flu to that isolated in Hong Kong in 1997 was the one implicated at both Qinghai and Novosibirsk in 2005.

   • “According to the sequence data, the cleavage site structure is practically identical to that of the highly pathogenic strain of subtype H5N1 isolated in Hong Kong in 1997”: August 5th, 2005 from Dr Evgueny A. Nepoklonov, Head of the Main Veterinary Department, Ministry of Agriculture and Food, Moscow, posted to ProMED.

   This is supported by research published online by Nature on July 6th, 2005, which concluded that detailed analysis indicated that “the virus causing the outbreak at Qinghai was a single introduction, most probably from poultry in southern China” (Chen et al, 2005).

   It perhaps needs to be noted in this respect that the Bar-headed Goose is a species suspected by some of introducing the virus to Qinghai Lake, as it was the first species to exhibit symptoms of the disease, and as 90% of wild birds killed by poultry flu there were of this species (Chen et al, 2005). However, Bar-headed Geese that are found in China in winter (where they potentially might have picked up the virus from poultry) are considered to be largely sedentary, i.e. they do not migrate to Qinghai (Wurdinger, 2005). In addition, very few Bar-headed Geese winter in the south of China.

   It might be rather more appropriate to consider the following from Lancet: “It is reported for example that chickens transported 1500 km from Lanzhou, Gansu Province, China, apparently introduced H5N1 to Lhasa, Tibet, in January 2004.” (Melville and Shortridge, 2004).

   All of the above reveals that:

   1. Healthy-looking waterbirds and other wild birds are not known to carry H5N1.

   2. The virus has persisted in poultry populations in the region since at least 1996/1997, with some infected birds appearing asymptomatic;

   3. Stricter controls of the management of poultry in Hong Kong was able to prevent re-emergence of the disease in a given area;

   4. The virus responsible for the recent outbreaks was transported in several known cases to areas free of the virus (e.g. Hong Kong and South Korea) through human activity, not through wild bird movements.

7. Outbreaks of the disease have never and still do not match the patterns of natural bird migration: migrations which have evolved over time and which are predictable.

   As also noted by Dr. Azery to ProMed (September 5th, 2005):

   • “When the spread of the current epidemic in SE Asia occurred, migratory waterfowl were almost instantaneously blamed as the source, although the timing and distribution of several new outbreaks did not fit any known migratory pattern for any species including terrestrial birds (Melville DS & KF Shortridge. Reflection and reaction. Lancet Infect Dis. 2004; 4: May). The presence of H5N1 in live bird markets as early as 1999 (Hong Kong in geese) and 2001 in Vietnam in geese imported from China (Nguyen, et al. Isolation and characterisation of Avian Influenza viruses, including HP H5N1 from poultry in live bird markets in Hanoi, Vietnam in 2001. J Virology 2005; 79(7): 4201-12), provided a credible alternative explanation for H5N1 outbreaks in domestic poultry. The paper by Nguyen et al (2005) identified the domestic duck as being the major reservoir of the AIV pool in nature and the live bird markets in Asian countries as a suitable environment for reassortment and transmission.”

   It easy for those that do not know much about birds or their migration and who do not know much about the geography of Asia to suggest that the spread of the disease is linked to the migration of waterbirds. It is a situation somewhat analogous to a birdwatcher with very limited knowledge of medicine diagnosing a human case of poultry flu – just because the person concerned starting coughing after eating a portion of chicken.

   owever, it is apparent to those that do understand birds and their migrations that the pattern of outbreaks has not and still does not match the movement of wild migratory birds – in any of the outbreaks since 1997. As noted by Melville and Shortridge (2004) in Lancet: “the timing and the distribution of the reported spread of H5N1 from South Korea (Dec 17, 2003) to Viet Nam (Jan 8, 2004) to Indonesia (Feb 6, 2004) does not fit any known migratory pattern for any species”.

   Moreover, it does not even match the migration pattern or distribution of any species group.

   Considering the recent focus on Anseriformes (swans, geese and ducks) as potential carriers of poultry flu, it is worth examining our own data and published data on the movements and distribution of such species – from Korea southward.

   Most Anseriformes start to arrive in South Korea in September, reaching a peak in October, with southward migration effectively over by late November. According to survey data published by the South Korean Ministry of Environment (anon 1999 and anon 2000), based on counts conducted in January, approximately one million ducks, geese and swans typically over-winter, including in recent years ca 500 000 Baikal Teal. However, despite the poultry flu outbreak in South Korea in December 2003, there have been no cases of H5N1 detected in wild waterbirds (not even Baikal Teal, a species that congregates in a huge, dense flock of up to or more than 400 000 individuals).

   The majority of migrant individuals (e.g. Northern Pintail and Greater White-fronted Goose) are believed to leave Korea in November to winter in China, with return migration through Korea in March and April.

   The outbreak of poultry flu in Korea in mid-December occurred therefore during a period of limited movement of waterbirds.

   If waterbirds had infected poultry in South Korea, then some wild birds in affected areas would likely also have tested positive for poultry flu: as noted above, they did not. In addition, considering their migration from Korea to China, then further outbreaks should have been reported in waterbird flocks in China in December or January. They were not, even though many waterbirds in China would have either migrated through Korea or mixed with other waterbirds which had.

   The next reported outbreak was in Viet Nam, in January. According to Cu, Trai and Phillipps (2000) although some species of duck are shared by Korea and Viet Nam, no species of swan and only two species of goose had been recorded in Viet Nam by 2000: the Bar-headed Goose (described as a rare migrant), and the Greylag Goose (described as an uncommon winter visitor). There is only one record of Bar-headed Goose in South Korea; and fewer than 10 records of Greylag Goose (e.g. Park, 2002). If a species of Anseriform was responsible for spreading the disease from Korea to Viet Nam, it therefore would very likely have to be a duck species.

   But what about continuing the spread, from Viet Nam to Indonesia? Only one species of northern duck found in both Korea and Viet Nam also occurs in Indonesia (the next country to report an outbreak of poultry flu) with any regularity: the Garganey.

   The Garganey is a scarce migrant species in Korea, with typical latest dates in autumn coming in late September/early October – two months before the outbreak in South Korea and a full four months before the outbreak in Indonesia.
   The Garganey is also a scarce species in Indonesia. A review of data gathered in Indonesia during the Asian Waterbird Census between 1999 and 2001 (in Li and Mundkur, 2004) confirms that no species of swan, goose or “northern” duck – including Garganey - were recorded in a survey of 67 wetlands there during that period.

   There is therefore clearly no obvious link between migrant waterbirds and poultry flu outbreaks in 2003/2004. The fact that almost all northern Anseriformes are very scarce as far south as Indonesia also greatly undermines suggestions that one species of waterbird infected another, which in turn infected another, allowing the outbreaks to spread beyond the range of one or more species (as has been recently alleged).

   What such outbreaks do reveal, however, is how widespread the disease had/has become in poultry of the region.

   In 2005, the apparent northwest progression of disease outbreaks, first in China at Qinghai, then in Xinjiang, then in Novosibirsk (and Kazakhstan), also provided, some suggested, the strongest evidence yet that migratory waterbirds, moving back northward, were again spreading the disease as they went.

   A chronology of outbreaks according to AVI Bull. 032 on July 31st 2005 (to the background of HPAI outbreaks in 21 out of 30 Indonesian Provinces...) included:

   1. Qinghai, Central China, April 30th-June 28th;
   2. Xinjiang, China: first on June 20th;
   3. Novosibirsk, Southern Russia: July 15th-

   And subsequently (reported elsewhere):

   4. Eastern Kazakhstan: July 22nd-
   5. Mongolia, late July

   Although superficially suggesting a bird's migration route, first along a broadly SE-NW axis, this kind of pattern would be an extremely odd and wasteful behavior for any species.

   It would need to entail a steady and continuous northwestward migration between April and July, followed by dispersion east and west. It is not a (known) migration pattern shown by any species of wild bird.

   Generally, most bird species that breed in the northern hemisphere do so in months between March and August/September. The further north they nest, the later such migrants will arrive on their breeding territory, which they will then occupy for a number of weeks or months. In the far north, most summer visitors for example will lay eggs and fledge young between May and the first half of July.

   In some cases, such as in some shorebird species, failed breeders (after migrating all the way to northern breeding areas, arriving there in mid-late May), will then start to migrate south again soon after, with increasing numbers of such adults arriving back at key staging areas (often coastal) as early as mid to late July (e.g. as far south as Korea).

   In a few other species, individuals will not complete their northward migration in spring and will therefore not go as far as the full adults, summering at a site well south of their breeding grounds.

   For the majority of all species, they simply (and logically) occupy breeding areas for several weeks/ months (between for example May and July), after which many species undertake some form of moult before southward migration.

   In the case of many Anseriformes, most individuals are effectively flightless or have restricted powers of flight in mid-summer. All parts of this biological cycle are fairly regular and predictable, evolved to meet given environmental conditions.

   Of especial interest in this regard is the Bar-headed Goose, which as suggested above has been proposed as a likely vector (being the species most affected by the outbreak in Qinghai).

   According to Wurninger's account of Bar-headed Goose (2005): the species'

   • "Spring migration starts in March in India and Pakistan; arrives at Kok Nor Mar-Apr; and northern Gobi and Pamir mid-May."; Egg-laying takes place in "early to mid-May in Tianshan; incubation 27-30 days...breeding pairs with goslings start wing moult 24-28 days after young hatch; both adults lose all primaries and secondaries within 24 hr. Able to fly 32-25 days later with young; by then, primaries 80% of normal length, and within 40-45 days, wings fully grown"; Autumn migration starts in northern breeding areas in late Aug, in Pamir end Sept".

   This gives approximate spring/summer dates thus:

   1. Arrival of Bar-headed Goose at e.g. Qinghai in late April/early May (more or less coinciding with the first outbreaks there);

   2. Egg-laying and incubation;

   3. Early June-mid-June hatching of goslings (when the outbreak was starting in Xinjiang);

   4. Early July-late July wing moult of adults starts, when these geese are flightless.

   This is the period when the disease “reached” Novosibirisk and Kazakhstan.

   5. End of August, Bar-headed Goose capable of longer flights

   6. "Autumn migration starts in northern breeding areas in late Aug, in Pamir end Sept".

   It is also important to note, that according to Wurdinger (2005) at least, the Bar-headed Goose does not occur as far north as Novosibirsk, nor does it occur in the affected part of Kazakhstan.

   The outbreak in Mongolia, at Lake Erkhel, is rather more puzzling.

   According to Wildlife Conservation Society specialists this seems most likely to have been caused by wild waterbirds, even though it does not seem to match migration patterns (either linking it to outbreaks further west, or by date). Considering the typically rather higher density of LPAI infection in juvenile ducks (reported by Hinshaw [1980], in Alexander 2000), it seems possible that either dispersing waterbirds from affected areas in Russia moved to the lake (for a post-breeding moult?) carrying the virus with them; or that other factors, such as gulls scavenging on infected items (poultry products consumed further north, or even locally, e.g. at the tourist camp located at one end of Erkhel Lake) might have been involved.

8. Wild birds, for whatever reason (energetics, lack of resistance?) appear to be highly susceptible to HIAP when exposed: many birds die, and quickly.

   In Qinghai, up to 200 birds a day died at the peak of the outbreak between May 18th and 5th June, resulting in a total of ca 6 000 fatalities (AVI Bulletin, 032, July 2005). This revealed clearly that poultry flu can be fatal to wild migrant birds, even to those species groups (such as Anseriformes) suspected by some as being the most likely vectors for the disease (and thus considered most likely to have developed some resistance to it). Colonial-nesting species such as Bar-headed Goose and Great Black-headed or Pallas's Gull were the most affected, followed by Great Cormorant (also a colonial nester) and Ruddy Shelduck (AVI Bulletin 032).

9. As far as is known to Birds Korea, no wild bird has been tested that appeared healthy and that carries H5N1 (unlike some domesticated poultry in Viet Nam): this despite tens of thousands of birds being tested in a large number of countries that receive migrant birds from affected regions; and despite testing of wild birds in affected areas - even from infected/affected sites, e.g. in Mongolia.

   As reported by W. Karesh DVM, Director, Field Veterinary Program, Wildlife Conservation Society (in lit., September 2005):

   “We visited 9 sites to sample live birds and also found dead birds at two sites (Erkhel and a small lake about 60 km southeast of Erkhel Lake). At Erkhel, there was a mix of species that died and probably all of them were NOT due to avian influenza.

   But, H5N1 avian influenza was found in 3 dead Whooper Swans and 1 Bar-headed Goose. We counted over 6500 live birds of at least 55 species on Erkhel Lake at the time.

   The estimate of 100 dead birds came from a period of about 2 weeks around the time of the live bird counts. About half of the dead birds were Whooper Swans. The other 50 or so we identified were Bar-headed Geese, Ruddy Shelduck, immature Herring [Mongolian] Gulls, and then some Common Pochards, Common Goldeneye and a number of other species.

   Once again, it is important to realize that many things can kill birds, especially young ones and during the breeding and nesting season. Of the close to 900 live birds we sampled, including hundreds of Ruddy Shelduck, Bar-headed Geese, and Black-headed Gulls, Herring Gulls, and Whooper Swans, they all tested negative, meaning that they were not shedding the virus”.

10. Recent outbreaks have often been misreported or misrepresented. The outbreaks in China (at Qinghai), in Mongolia (at Lake Erkhel), and in the Novosibirsk region of southern Siberian Russia between May and July 2005 have all been blamed on wild birds (as were earlier outbreaks), in a “slam-dunk” way. All three areas have been incorrectly characterised by some media as remote, and with wild birds that had no contact with poultry, simply and frighteningly dropping dead.

    Although it is difficult to get access to good information:

    1. In addition to the findings on virus type reported in Nature (see Statement 6 above), news reports at Qinghai allow that 20 000 poultry in the area were slaughtered as a result of the outbreak and that the lake is actually a major tourist destination with a Buddhist lamasery within a mile of the water's edge (See: www.guardian.co.uk/international/story). Considering the prevalence of cage birds in the region, considering the presence of poultry in the region, considering Buddhist ceremonies in some areas 'releasing' caged wild birds back into the wild, it is not too hard to suggest human influence in the outbreak.

    2. In Mongolia, the affected area is also described by Mongolian reporters as a tourist destination with its local population in the high hundreds/ low thousands, allowing the outbreak in wild birds to be first observed (see: ubpost.mongolnews.mn).
       According to personal comments made in emails to us by Dr. William Karesh, “The method of spread can not be determined, we did not see any chickens around the lakes, they are not common in Mongolia and they have not found the disease in chickens. So, there could have been some species of bird that brought it to the lake (either before it died, or a species that is not killed by the virus). Within Mongolia, it would be possible for the virus to move from place to place either by a wild bird, or on vehicles.”

    3. In the affected region of Siberian Russia, according to Alexander Solokha of WWF Russia, some local people raise ducks and geese for slaughter as well as eggs, which they supplement annually by catching duck chicks at local lakes with nets (along with eggs for further incubation), rearing these together with domestic poultry. Some also keep turkeys (an early report on Niman's website apparently revealed that a turkey, a non-native domestic species in the region, had contracted H5N1: how could a turkey ‘naturally' catch it from a wild duck?).

    Note also, posting 20050824.2492 to Pro-Med on August 24 by Hon S. Ip, of the United States Geological Survey, National Wildlife Health Center, Diagnostic Virology Laboratory:

    • “in some of the limited information available on the nature of the Novosibirsk HPAI H5N1 virus, as provided by Russia to OIE [see 20050813.2369 and www.oie.int/downld/AVIAN%20INFLUENZA/Russia%20HPAI.pdf], the 4 isolates of H5N1 from domestic poultry in 2 regions of Novosibirsk are similar, but one sample, which is from a wild duck, clearly has a different PCR electrophoreogram pattern (Figure 1 in the OIE report). While other data not included in the report may show that the virus in wild birds is related to those isolated from affected poultry in the Novosibirsk region, the available data suggest that such is not the case, and certainly no data that shows the wild birds were the vector of transmission has been madeavailable at the present time.”

    Also from H. Niman's website, a mechanical translation of information on the region's poultry: “Let us note, in the suburb of Tyumen' are located two large poultry-breeding complexes - Bohr poultry processing facility and ‘Tyumen' broiler'. Volume of the production of Bohr poultry processing facility: 2 million eggs per day, 3 800 tons of fresh meat - yearly. Now in the enterprise more than 3.3 million poultry, including 2.3 million hens for egg production. The poultry processing facility meets the demand of West and East Siberia, and also part of the Urals and central Russia…The ‘Tyumen broiler' supplies its production into the northern part of the region….”

    An additional and related element is the contemporaneous spread of foot and mouth disease within the same region, now affecting China, Mongolia and parts of Russia. As noted on Pro-med (Archive Number 20050906.2643): there is “clear circumstantial evidence (in the absence of official reports) that China's territory must be widely contaminated with Foot and Mouth Asia-1 [serotype]. The disease seems to have spread therefrom (sic) to several neighboring countries since early 2005 (see FAO statement, 24 June 2005, in 20050624.1774 as well as other postings). – Mod. AS”. If so, this is equally clear circumstantial evidence that diseased domesticated animals are still crossing national borders within this region – by human transport.

    Concerning the outbreaks in southern Siberian Russia, several factors are best considered in combination:

    1. Some domesticated ducks appear to be able to have the virus without showing symptoms;

    2. The Novosibirsk region borders China, and Kazakhstan;

    3. There is extensive trade between China and Russia (and other regions that have experienced outbreaks), including the import of poultry and “poultry products.” It has been suggested, for example, that Russia still imports almost 50% of its poultry/poultry products.

    4. The virus has been circulating in poultry flocks in some parts of neighboring China for at least 9 years;

    5. An extensive poultry vaccination program has been conducted in several parts of China, meaning potentially that an increased number of individual poultry could be infected yet (largely) asymptomatic.

    6. Poultry in the affected region is a major industry as well as a staple of local households.

    7. That other diseases, such as foot-and-mouth, have also been spreading within the same region at the same time: indicating that controls on the movement of diseased domesticated (non-flying!) animals have not been successful.

    It is therefore not difficult to imagine how the trade and transport of chickens, ducks or geese, or turkeys, or even just their droppings on a truck, a cage or even someone's shoes, could have infected local poultry, which in turn (being largely asymptomatic) could have spread the disease to newly caught wild birds - sickening and dying when infected, and attracting attention.

    • (Note: “the influenza Virus can survive in poultry droppings for up to 2 weeks [Lu et al., 2003. Avian Dis 47:1015-1021], movement of people and contaminated farm equipment can rapidly spread the virus from one locale to another.” Hon S. Ip, of the United States Geological Survey, Pro-med mailing 20050824.2492).

    As stated above, the affected area has both abundant local, household-level poultry rearing and a huge poultry industry, apparently supplying eggs and poultry west to the Urals and east, to some degree matching the rapid spread of the disease in the region.

11. Recent reports indicate that “the infections reported so far do coincide geographically with major rail, trade and travel links through the region” (New Scientist online article: www.newscientist.com/article.ns?id=dn7905)

12. Media reports that incite fear by comparing wild birds to "intercontinental ballistic missiles" (apparently first posted on the online version of Wall Street Journal, August 8th, 2005), conjuring up images of North Korean missile tests and planes slamming into the World Trade Centre, or state like Niman has that one or more Asian countries are not testing for the disease properly, are simply and maliciously playing on subconscious fears.

    At their best, such reports can be considered melodramatic, ill-informed and poorly written; at their worst, they appear to be both racist and negative about (and fearful of) wildlife and "other" species.

13. The outbreaks of poultry flu should lead to a profound rethinking of the poultry industry, a profound rethinking of peoples abuse of other (and our own) species.

    They likely will not. Already huge numbers of poultry have been slaughtered as a result (a slightly earlier slaughter than if they had been slaughtered for consumption in the usual way...); and in some areas culls of wild birds have been encouraged.

14. In the short-term, biosecurity needs to be improved, wild birds and poultry kept separate, and arguments and bad reporting need to be confronted with logic and science.

    Longer term, people will need to deconstruct numerous myths, limit and ultimately dismantle the cage bird trade (see: e.g. news.bbc.co.uk/1/hi/health/4219592.stm) and the poultry industry, and change the relationship between people and other species. We will all need to take increasing responsibility for our own choices, and simultaneously make better collective choices for our own species.

Summary

• Poultry Flu is the popular name coined by Birds Korea to describe HPAI H5N1, as it is disease primarily of poultry, and a product of the unhygienic and inhumane conditions found in the poultry industry.

• In the summer of 2005 there have been a series of outbreaks of poultry flu, some of which have also killed large numbers of wild birds, revealing that the disease has again spread from China and South-east Asia, this time to reach Kazakhstan, southern Siberian Russia and Mongolia.

• Although these recent outbreaks are all traceable back to original outbreaks in 1996/1997, recent media reports have in many cases stated (without evidence) that wild migrant birds are responsible for the spread of the disease, and have greatly increased concerns that migrant birds will therefore soon spread poultry flu into Europe and the US. This line of argument has become almost as influential as it is ill-informed, fuelled by the often-discussed potential for poultry flu to mutate into a disease that can kill non-avian species, including people - leading potentially to a massive human pandemic. Indeed, poultry flu has already claimed the lives of over 60 people since 1997 (admittedly in a region of huge human and poultry population, and taking almost 9 years to do so).

• Such fears, understandable as they are (if based in facts) can create an obviously negative climate for bird conservation, with several potentially long-term implications.

• Fortunately, much of the line-of-thinking does not seem to be supported by available evidence – especially with regards to wild birds.

  1. Poultry flu outbreaks have not yet and still do not match wild bird migration patterns, in either time or location;

  2. there have been no cases (yet) of poultry flu virus transmission from a wild bird to a human;

  3. and no healthy wild birds tested for poultry flu have (yet) been identified, despite very extensive testing in a large number of countries.

• Instead, it is increasingly recognized that poultry within the region can and are acting as reservoirs for poultry flu; and that the pattern of outbreaks (past and present) better matches transport systems and the outbreaks of other domesticated animal disease (such as foot and mouth) than it does spread through natural bird migration.

• As a result, it seems appropriate to focus most of the effort on controlling poultry flu on the poultry industry and on household poultry units, rather than on wild birds.

• Although most of the outbreaks can be clearly traced to poultry, the death of waterbirds in Mongolia from poultry flu seem, however, to have taken place without such an obvious source of infection, suggesting the possibility that at least some birds infected with the virus are able to migrate significant distances.

  This is possibly only the second case where such a Highly Pathogenic Avian Influenza outbreak in wild birds occurred without such an influence (the first being H5N3 in Common Terns in South Africa in 1961).

• As such, even though the disease was not transmitted to people and seemed to “fizzle out” without culling, testing for the virus in wild birds should be continued, and birdwatchers should, as recommended in some countries, act as look-outs for disease outbreaks in new and already affected areas.

• As control of poultry has proved to be a fairly effective mechanism for controlling some poultry flu outbreaks in the past, Birds Korea believes that in the short term biosecurity needs to be greatly improved (keeping wild birds and domesticated poultry separate, and preventing possibly infected poultry from contaminating wild bird habitats), while long-term much stricter controls will need to be imposed and enforced on both the caged bird and the poultry industries. Ultimately, we as people will need to reconsider our relationship to other species.

Acknowledgements

Many thanks to Dr. Martin Williams in Hong Kong (drmartinwilliams.com), Wendy Orent in the US, and Dr. Taej Mundkur of Wetlands International for providing extensive materials and great insight;
David Melville in New Zealand for permitting use of his 2004 Lancet publication
Ikeda Minami of JAWAN in Japan;
Ed Keeble in the UK and Axel Braunlich in Mongolia;
Dr. Billy Karesh, Colin Poole and Dr. Martin Gilbert of the Wildlife Conservation Society (for first-hand information from Mongolia and permission to use WCS materials);
and Alexander Solokha of WWF Russia/Wetlands International Russia Program for insight into the outbreaks in Russia.

References

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• Anon. (1999) & Anon (2000). Winter Bird National Census Results (in Korean). Published by the Korean National Ministry of Environment.
• Li, D. & T. Mundkur. (2004). Numbers and distribution of waterbirds and wetlands in the Asia-Pacific region. Results of the Asian Waterbird Census: 1997-2001. Wetlands International, Kuala Lumpur, Malaysia.
• Chen H., Smith G., Zhang S., Qin K., Wang J., Li K., Webster R., Peiris J. & Y. Guan.(2005) H5N1 Outbreak in Migratory Waterfowl. Brief Communications. Nature. Online edition (July 6, 2005).
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