PNAS paper – multiple sublineages of H5N1

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    Martin W

      New paper:
      Establishment of multiple sublineages of H5N1 influenza virus in Asia: Implications for pandemic control
      by several authors inc Robert Webster is causing much discussion.

      Even though main results show movements within poultry industry chiefly responsible for sustaining and spreading H5N1, being taken by some quarters as evidence for wild birds spreading the virus.
      New Scientist (Deborah MacKenzie) among those seizing on this.
      Certainly seems to fit pet notions of Robert Webster, who seems gung-ho re ducks as vectors (just seen paper showing domestic ducks linked to H5N1 outbreaks in Thailand).

      Various questions arise.
      Here’s erudite email from Nial Moores, director of Birds Korea:

      It is increasingly apparent that H5N1 avian influenza has now become one of the most immediate threats to wild birds and their conservation in Eurasia. This is not because wild birds yet threaten human health (apparently there is still no case where a wild bird has even been suggested to infect a human with the disease, and more surprisingly it seems there is still not yet a single case where wild birds have even been proven unambiguously to have infected poultry…?). It is rather because of all of the suspicion and villification of wild birds, and because wild birds can be killed by Highly Pathogenic Avian Influenza H5N1: both directly, and through culls.

      Very recent so-called response strategies to claims that wild birds are spreading HPAI H5N1 include calls for a massive cull of wild birds in parts of Siberia (including the destruction of nesting habitat), and the callous slaughter of some wild birds left exhausted by severe cold in Romania (they were, according to a January 31st Reuters report, beheaded or used as live footballs by a gang of local men). This in addition to the extraordinarily cruel treatment of poultry in many areas, bagged and burnt to protect our health.

      The role of wild birds in the active long-range spread of HPAI H5N1 has been sensationalised and stated as fact ad nauseam for a number of years now it seems, and although the New Scientist article is yet another to suggest such a so-called revelation, it seems appropriate to note its use of the word CAN (rather than the word DO) when suggesting long range spread by wild birds.

      Note too, quote:
      The researchers analysed samples taken from 13,000 migratory birds and
      50,000 market poultry in southeast China between January 2004 and June
      2005, when the Chinese government banned independent sampling. In the
      markets, they found H5N1 in about 2% of apparently healthy ducks and
      geese, and some chickens, in all but two of the months in the sampling
      End of quote

      The 2% level of infection of apparently healthy poultry was found in markets. Only 6 apparently healthy wild birds out of 13 000 were found infected with H5N1 (though even here the details are left very sparse: which species of waterbird, and at what stage of infection they were at). The short New Scientist article then appears to take two huge leaps in logic, the first in assuming that infected wild birds can migrate long distances just because infected captive juvenile mallards (freed from other stresses) can recover and fly, and second in suggesting that just because the genetic make-up of the virus is similar between infected ducks in Poyang, birds at Qinghai and chickens in Turkey, that this somehow proves the method of spread. This seems especially important when the thrust of the research reveals how widespread the virus has become in poultry in China, and even more significantly how many asymptomatic infected poultry can carry and shed the virus.

      Omitted from this and many other similar articles too is a still huge amount of negative data, and numerous unanswered questions, re the spread of HPAI H5N1 by wild birds.

      The listserver group AI Watch (orginally set up by some staff in Birdlife, an excellent initiative for which they are to be warmly congratulated) contains as its members many bird conservationists (including those working in areas with outbreaks), and a range of others with H5N1 relevant expertise. Its members have been trying honestly and openly to look at the available evidence – through researching background information to areas with outbreaks, and through applying existing understanding of wild birds and their migrations to the discussion (something by and large sorely lacking so far: really, which wild bird species have a migration route that takes them from southeast China to Qinghai and then onto Europe?).

      The following is a personalised summary of a few of the causes so-far suggested by members of the AI watch group as potential/already implicated in the spread of HPAI H5N1 (what a very few of us still stubbornly call Poultry Flu!):

      1) Spread by the legal and illegal caged bird trade. Known examples of diseased captive birds with HPAI H5N1 include the parrot in the UK, Hawk-eagles found in baggage in Belgium, mesias in Taiwan, and a captive Flamingo in Kuwait. The first three were detected in customs, preventing further spread of the disease. The last, like several others, was immediately identified by some media as carried by a migratory wild bird – despite overwhelming evidence to the contrary (the flamingo was in a collection on private property apparently). The recent discovery of infected falcons at a falcon centre in Saudi Arabia is yet one more example of this form of spread.

      2) The related Merit Release: the purposeful release of once-captive birds into the wild in order to gain spiritual merit. Any increase in reports of infected wild birds after such ceremonies?

      3) The movement of poultry and eggs, legal and illegal, and the movement of vehicles and personnel that might also have been contaminated by virus (infected excrement carried on shoes, tires or crates etc). The poultry industry is an enormous industry, legal and illegal, that rears billions of birds annually, moving them both within and beyond national borders: across the width of China, from Thailand to Russia etc. This poultry is of course used for human consumption, and in some cases (as in western China) for control of locust outbreaks, with the potential to infect natural wild bird habitats. Note that this virus can be maintained in the environment for significant periods: apparently for up to two or three weeks in cold water or in droppings.

      H5N1 outbreaks in South Korea and Japan a couple of years back were traced back to infected poultry meat imported from China. The outbreaks in both countries were stamped out quickly by controls on imports and culls of infected poultry. Testing of wild birds in both countries at that time and subsequently revealed none (apart from a few dead ones: see below) were infected with H5N1. How could this have been so if large numbers of healthy yet infected wild birds were carrying the virus around, infecting poultry as they went, as apparently suggested by the New Scientist note below?

      4) Secondary spread to wild birds by infected poultry, including contamination by such poultry of local environments. The HPAI H5N1 virus killed several non-migratory species like Large-billed Crows in Japan and Eurasian Magpie in Korea – species that scavenge around poultry farms (among other places). This, as well as point 5 below, also seems relevant to discoveries of dead H5N1-infected waterbirds like Chinese Pond Heron, Little Egret and Grey Heron, that often feed in polluted fish-rich waterways (e.g as found in many areas near poultry farms, where waterbodies can be enriched by agricultural run-off).

      5) Spread though use of poultry manure as fertiliser in fish-farms. Requiring further investigation, is it not striking that fish-farms using poultry manure enrichment were apparently set up in Qinghai shortly before the massive outbreak there that wiped out several thousand Bar-headed Geese in spring 2005? That species like the Mute Swan, migrating from countries without H5N1 outbreaks, have been found infected at fish-farms in countries with outbreaks?

      6) Spread by infected wild birds. The limited, perhaps inter-connected, outbreaks in wild birds in Mongolia in the summer of 2005 seem to suggest that such medium-range spread by wild birds is possible. Considering the rapid spread of outbreaks of H5N1 in poultry in southern Siberia just before, it seems at least possible that a few ducks infected by sick poultry (or their environs) would be able to fly several hundred kms south to Mongolian wetlands where they could then infect a small number of local nesting waterbirds like Whooper Swans before succumbing to the disease. What is equally or even more important (and too rarely mentioned) is that such outbreaks appear to be extremely rare indeed; that in Mongolia they were very limited in scale; and that they petered out quickly. The virus was not maintained in a highly pathogenic state in wild birds in Mongolia; the outbreaks did not lead to known outbreaks in wild birds in neighboring countries; and they did not involve known infection of poultry or humans by wild birds.

      While considering the above points, the need to review more of the negative data becomes even clearer:

      1) Why have there never been HPAI H5N1 outbreaks in several countries in East Asia that maintain very strict import controls (on poultry and caged birds), even though the same countries receive many wild migrant birds from infected regions annually?

      2) IF wild birds are responsible for spreading the virus from Qinghai to Russia and eastern Europe, why have the same species been unable even to reinfect poultry or wild birds in South Korea and Japan (we have well over a million waterbirds coming from Siberia and China to Korea in winter, yet no outbreaks of HPAI H5N1 here for a couple of years)?

      3) Why have many species of geese and other waterbird species that breed in genuinely remote areas of northern Siberia etc to winter in infected regions (where they mix with species like Mallard and Pochard, both implicated by some as H5N1 carriers), not yet been infected?

      4) Why has the disease not yet spread though Siberian-nesting waterbirds from Asia into the Americas or into Australia or New Zealand (it has now had 10 years in which to do so, while it apparently managed to move from China or SE Asia to western Asia and eastern Europe in only the past 8 months)?

      5) Why no outbreaks in India this winter (it was after all infected Bar-headed Geese, that winter in India, that were for a while blamed for spreading the disease north from Qinghai last summer)?

      6) Why too do the infected wild bird species seem to keep falling into the same several categories, namely: (a) scavengers around human habitations and poultry farms (crows etc), (b) species popular in capivity (from falcons, to laughing thrushes and Oriental Magpie Robins), and (c) waterbirds that need to use human-modified wetlands?

      The pattern of outbreaks, to me at least, seems to vary little. Typically, it involves sick poultry and quick accusations that wild birds infected them; it includes calls for controls on wildlife reservoirs by either media, decision-makers or the general public; and each time it includes papers, notes or skewed media articles revealing that finally there is now overwhelming evidence that wild birds and not people and their poultry are really to blame.

      It would be really wonderful if more such questions were asked repeatedly to media and certain leading organisations (like FAO) that have been always been so quick to blame wild birds for outbreaks of the disease.

      Contrary to widespread reports, it is not bird conservationists that are burying their heads in the sand…

      Many questions (and sadly still far too few people asking them).


        In the previous post mention was made of “Merit Release.” I understand what this is, and see a possible co-repondence to recent holidays in China.

        We have just recently passed through the recent Lunar New Year.

        Seemingly con-incidentally we have seen a sudden resurgence in H5N1 in Hong kong. As I recall, these recent outbreaks were all identified in the last two weeks.

        How much does this seem to fit a possible relational pattern?



        Martin W

          Seemed possible to me for at least one case, a mynah near major temple. Also, high poultry demand here and nearby Guangdong over cny. Thread re wild birds in HK with H5N1

          Martin W

            I emailed Drs Robert Webster and Guan Yi, re the PNAS paper. Various questions. Dr (Prof) Guan promptly sent email with some brief answers:

            Re species carrying virus between Poyang and Qinghai: "As we point out in our paper, it is migratory duck." – I’ve replied, saying this isn’t detailed enough. He and his team rightly want detail re virology. But detail needed too re wild birds. Especially where no migration routes (so far as I’ve seen) known to link Poyang and Qinghai – and places Poyang birds known to migrate to did not suffer major die-offs.

            Qn: What information do you have on H5N1 in poultry and wild birds elsewhere in central and northern China, especially between Poyang and Qinghai? "As far as I know, no any other groups would like working as hard as our group to do surveillance study for long-term. So, H5N1 information between Poyang and Qinghai is not clear. If you can provide some information to fill the gap, it would be very useful." – well, wish I could supply or find such info. But with a vacuum of data for north China, saying there is certainly a direct link between Poyang and Qinghai is surely impossible (well, not if good science anyway).

            Qn: Did you consider transport within the poultry trade, even smuggling – perhaps of those apparently healthy chickens? "There is no limitation for poultry movement, but it would not make any sense if poultry were transported that far away." – directly from Poyang to Qinghai would indeed seem silly. But transportation networks in n China? Remembering, too, an outbreak at goose farm in nw Xinjiang. Point: A previous outbreak in poultry in Tibet was traced to a source in Lanzhou – not a great distance from Qinghai, so trade/smuggling would seem plausible. "Do you have convince data to prove this link? How closely related between the virus from Tibet and Lanzhou? Please think question in molecular virology point of view as well." – sent the info, which from an FAO report; nothing on virology tho.

            Qn: I’m curious: why were you able to obtain so many specimens from birds at Poyang? "I have big group in mainland working for me."

            Qn: Further, were there indications of H5N1 killing wild birds at Poyang? "Some of them, Yes. Died birds were observed during some seasons." [would be good if had info on poultry farming around and fish farming at Poyang. inc whether any domestic duck farms – this is the kind of place where wild birds might mingle with domestic] Nothing yet to my follow-up email.

            Nothing, too, from Robert Webster (inc no answer to whether he is fully objective!) [third time, I think, I’ve tried emailing Robert W; wonder if should really be hopeful] Article on Webster, inc re his belief birds are pivotal with flu, and dangerous pandemic may loom: Profile: Robert Webster

            "Perhaps his most valued contribution is the idea that wild birds are a reservoir of influenza viruses" – now, seemingly aiming to show wild birds can also carry dangerous Poultry Flu. And not too fussed about fiddly things like details re wild bird species, migration routes and timings.


              The PNAS paper is an interesting one.

              It seems to indicate that though H5N1 may be asymptomaitcally caried in wild duck populations, that the virus only cquires sufficient pathogenicity after having been in terrestrial poultry for some period.

              That would explain some of the virus qualities seen in the current situation.

              H5N1 may have started as an aquatic bird virus, but it’s pathogenic contemporary is derived more from domestic chickens than wild ducks, hence the new propensity for it to kill many species of wild waterfowl (including the geese and swans.)

              Although Guan Yi doesn’t draw this conclusion, it seems his work could support the hypothesis.


                All H5N1 viruses isolated in Eurasia since 1996, whether from ducks geese or chickens are already highly pathogenic for chickens. They do not need passage in chickens to change to a highly pathogenic form.


                Les Sims


                  Les Sims wrote:

                  All H5N1 viruses isolated in Eurasia since 1996, whether from ducks geese or chickens are already highly pathogenic for chickens. They do not need passage in chickens to change to a highly pathogenic form.


                  Les Sims

                  Yes, I understand that point, yet the virus had not been particularly pathogenic for other species (not many others) until it became such an issue for Chickens. Those chickens that are asymptomatic/immune may well be adding some mystery point mutation necessary to be virulent to more of the wild bird species.

                  Otherwise, with (an) H5N1 (variant) in chickens for so many years, wouldn’t we have seen a lot more die off in wild birds as we are seeing now?

                  Slightly less fatal disease in chickens allows more transport of asymptomatic, or less ill chickens(chicks??). Slightly more fatal virus shows up as higher epidemic exposure in wild populations. Vaccination with sub-optimal vaccine may amplify the carrier-syndrome in domestic poultry.

                  (Maybe I’m stretching it a bit here, but sci-fi speculation is a hobby of mine.)

                  Martin W

                    First major die-off in wild/ornamental birds with H5N1 of Guangdong goose 96 lineage was in 2002, in Hong Kong.
                    Were more deaths in 2003/04.
                    But, didn’t cause so much fuss as those now – and Qinghai Lake incident remarkable.
                    So, seems H5N1 has always been deadly to wild birds. Some variations in ducks (rather more guff in another thread or two here:Trojan ducks, PNAS paper).

                    Martin W

                      Just found map showing eastern flyway for Siberian crane.
                      As vast majority of the Sibes winter at Poyang, this is also useful as map of flyway for Poyang winter birds; though other species follow broader/somewhat different routes (eg, white-naped crane might follow fairly tight routes, but most not along coast; swan goose also mainly migrating inland – but not heading off way to west [unless you believe – as certain virologists just might – that they change species en route, becoming bar-headed geese]).


                      Sent URL to Robert Webster, suggesting this is rather different route to his Tooth Fairy Bird.

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