SEEN - SE European Bird Migration Network
Migratory birds and influenza virus

Zdeněk Hubálek

Medical Zoology Laboratory, Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, Czech Republic

Influenza A virus (family Orthomyxoviridae) has often been isolated from wild birds (at least 88 species, 12 orders) worldwide, mainly from ducks, gulls, terns, shearwaters, shorebirds, less often from passerines. Wild aquatic birds are the primordial source and reservoir of all influenza viruses for other vertebrates. The gene pool of influenza A viruses in aquatic birds provides all the genetic diversity required for the emergence of pandemic influenza viruses for humans, other mammals and birds. All known antigenic subtypes of influenza A virus (H1 to H14, and N1 to N9) have namely been found to perpetuate in aquatic birds, particularly in waterfowl. The predominant subtypes of viruses isolated from gulls and shorebirds (e.g., H9, H11, H13, N9) differ from those in wild ducks, and are largely nonpathogenic; however, ducks, shorebirds and gulls jointly serve as a reservoir for H4 and N6 subtypes. Southern China is regarded as a region where influenza viruses co-circulate in urban and rural conditions among people, domestic pigs and ducks, thus providing the opportunity for interspecies transmission and genetic exchange among the viruses. In wild ducks, influenza viruses replicate in the cells of the intestinal tract and are excreted in high concentrations in the faeces; the virus shedding can continue for 2–4 weeks. Moreover, the viruses are quite stable in the water environment – they persist in ponds for 4 days at 22ºC, and for 30 days at 0ºC, but some strains could remain infective in water for 207 days at 17ºC and up to 102 days at 28ºC. Most viral isolates are from asymptomatic birds, and avian morbidity or mortality have rarely been observed. However, also highly pathogenic avian influenza A (HPAI) strains (e.g., H7N1, H5N1) occur that kill birds. An extensive HPAI H5N1 epornitic in poultry started in south-east Asia in 1997 and has raised special concern because of its rapid expansion across Eurasia in 2005. The history of the HPAI H5N1 virus dispersal over Eurasia in 2005 indicates that migrating birds have been involved; additional, less important mechanisms in the dispersal might have been legal and illegal bird trade although this has been controlled by stringent veterinary measures in most Eurasian countries in 2005. The virus is believed to have been transmitted to domestic poultry from wild migratory waterfowl after contact at open reservoirs in certain localities, e.g. in some Russian regions (Novosibirsk, Chelyabinsk), Turkey and Romania. The Romanian and Croatian H5N1 isolates from migratory swans in autumn of 2005 present additional indirect evidence of the virus spread by migratory birds.
Although HPAI is largely a paramount veterinary (and economic) problem, bird-to-human transmissions have also been sporadically reported; about 140 laboratory-confirmed human cases in SE. Asia have been reported to WHO as of December 2005, 70 of them fatal. Obviously, humans can become infected with HPAI only when they inhale or ingest a massive virus dose from faeces or feathers of infected birds resulting from a very close contact. This event is improbable to occur under normal circumstances, and only some professional groups (keepers of caught birds and poultry) are at risk. Fortunately, HPAI H5N1 virus has been quite exceptionally (if at all) passed from human to human up to now. However, the risk for generating a reassortant pandemic human strain of influenza A has to be considered.


Mid April to June: >6,000 migratory birds died on Qinghai Hu Lake, Qinghai province, northern China: the H5N1 virus isolated, e.g., from a bar-headed goose (Anser indicus).
Mid May: dying of migratory birds in the neighbouring Xinjiang province, China.
18 July: outbreaks in poultry and wild waterfowl in Novosibirsk region (at least 15 villages), Asian Russia (the isolates identical to 3 strains from migratory birds on Qinghai Hu).
22 July to August: outbreaks in poultry in 5 areas, northern Kazakhstan.
2 Aug.: migratory waterfowl (Anas penelope, Tadorna ferruginea, Anser indicus, Cygnus cygnus) infected in northern Mongolia: 80 dead birds on Erhel Lake, Huvsgel province; 9 dead birds on Khunt Lake, Bulgan province.
August: outbreaks in poultry in the Altai (at least 14 areas), Kurgan (at least 6 villages), Omsk (at least 6 areas) and Tyumen (at least 6 villages) regions, Asian Russia.
13 Aug.: outbreaks in Chelyabinsk region (at a lake that borders Kazakhstan, and another area), southern Ural Territory, Russia.
1 Oct.: death of 1,700 young domestic turkeys at a free-range farm at the Manyas Lake (Kuşcenneti National Park), Bal?kesir province, western Asian Turkey.
Early October: an HPAI epornitic in poultry started in Crimea, South Ukraine (although reported only in late November).
Early October: 40 mute swans (Cygnus olor) found dead at Maliuc and a wild duck near Ceamurlia de Jos village (Tulcea county, the Danube Delta, Romania) were positive for H5N1. An outbreak among domestic hens and ducks followed in Ceamurlia de Jos.
10 Oct.: 2 migratory wild geese and a mute swan found dead at River Danube near Vadu-Oii village (the Danube Delta, Romania), 10 km from the border with Ukraine.
17 Oct.: an outbreak in chickens, geese and ducks in a village, Tula region, European Russia.
19-27 Oct.: >35 wild mute swans dead in several localities in Croatia (Zdenci Natural Park and surroundings, Našice, Baranjsko Petrovo Selo, Slavonski Brod); H5N1 diagnosed in several swans, including one individual ringed in Hungary.
21 Oct.: a dead grey heron in Vaslui county (Romania) on the Prut River shore, 100 km north of the Danube Delta, at the border with Moldova; the H5N1 isolate was identical to the strains isolated in Novosibirsk, Qinghai, Turkey and Romania previously.
21-26 Oct.: outbreaks in chickens in 3 villages in Tambov region, European Russia (c. 400 km southeast of Moscow).
11 Nov.: a migratory flamingo (Phoenicopterus ruber) found dead on a shore in Kuwait was infected with H5N1 (the first case in the Persian Gulf region).

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