Swans the silent sentinels for bird flu

Swans are highly susceptible to contracting H5N1 HPAI and generally die quickly from the virus.

Wild ducks are silent spreaders of potentially pandemic avian influenza viruses and wild swans are silent sentinels. Wild ducks are generally tolerant of H5N1 HPAI (highly pathogenic avian influenza), carrying the virus without symptomatic disease and excreting virus wherever they may roam. Swans, on the other hand, are highly susceptible and generally die soon after the contracting the infection.

From Japan in the Far East to the United Kingdom (UK) at the western tip of Europe, wild swans have been found infected (and mostly dead) with the potentially pandemic H5N1 HPAI virus. One of the most recent reports of wild swans with an avian influenza virus was in the United States near Providence, in the tiny north eastern state of Rhode Island. This time the culprit was one of the H7 subtypes (H7N3), increasingly regarded by experts as alternative candidates to H5 subtypes as a template for an influenza pandemic with avian origins.

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Widespread reports of H5N1 in wild swans right across Europe began in late 2005 and 2006 after rapid spread of the virus across central/western Asia and into Europe from Lake Qinghai (western China) where the virus was recorded in many different wild birds, notably bar-headed geese, in May 2005.

From late 2005 into 2006, the World Organisation for Animal Health (OIE) published reports of H5N1 infected swans in Western Asia (Azerbaijan and Iran) and Europe. Thirteen European Union member states confirmed outbreaks of H5N1 HPAI in wild birds during 2006. They were Germany, Austria, Denmark, Italy, Greece, UK, the Czech Republic, Poland, Slovakia, Slovenia, Sweden, France and Hungary, and almost entirely in swans.

Widespread outbreaks 

The largest outbreaks in wild swans and subsequently responsible for first H5N1 outbreaks in European poultry occurred in Germany and France. In January 2006, large numbers of dead swans were found on the Baltic Sea island of Ruegen, which is owned by Germany but delineated by a triangle from the north coast of Germany, the southern coast of Sweden, and the east coast of Denmark.

Fifteen infected wild swans were recorded during January 2006 in the south east Ain Département of France where the virus subsequently wiped out 11,000 turkeys on a single farm. This was Western Europe’s very first outbreak of H5N1 in commercial poultry. At the same time, Turkey was in the midst a huge and fast moving outbreak in poultry during one of the coldest winters on record around the Black Sea where Turkey is located. Ornithologists said these infected swans, normally resident in the Black Sea region, had been forced westwards in to Europe by especially severe winter conditions.

The UK subsequently had its own scare when a dead swan, found on a beach in Eastern Scotland, tested positive for H5N1. After initial confusion (because the carcass was in an advanced state of decomposition), the swan was finally confirmed (by DNA testing) as a whooper swan, a migratory species that comes to the UK as a winter visitor from continental Europe. Experts subsequently decided the bird was infected in continental Europe and died in flight over the North Sea, only to be washed up on the Scottish coast.

Until then, almost all reports of H5N1 infected (dead) swans related to mute swans, a largely sedentary species tending to stay in one location unless forced out by extreme weather conditions. This pattern was maintained through 2007 with more than 300 infected wild birds found in Germany and a much lower number in neighbouring countries. Those in France and the Czech Republic were all swans. German data reported to OIE does not specify which wild bird species were involved although other reports suggest most were wild swans.

The single biggest and strangest outbreak in wild swans occurred at the end of 2007 in the County of Dorset, western England. A large (800-1000) herd of mute swans, behaving and managed more like a flock of free range geese than wild birds, became infected with H5N1 HPAI. About a dozen dead birds from the herd, maintained as a tourist attraction, were confirmed with H5N1 HPAI.

Genetic sequences support movement 

Given the high susceptibility of swans and especially mute swans to H5N1 HPAI, experts expected the virus disease to scythe through the herd, but this did not happen. The manager of the reserve claimed he was told by government officials that the birds had most likely developed resistance to the disease. It is not clear whether any subsequent tests were conducted to see whether these apparently healthy swans were carrying H5N1 antibodies and possibly still shedding the virus.

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Focus then switched to the Far East where H5N1 was identified in four whooper swans in Japan’s Akita prefecture. Subsequent genetic sequencing showed the virus to be virtually identical to the H5N1 virus that caused South Korea’s worst outbreak in poultry, kicking off around the same time in April 2008. The South Korea National Veterinary Research and Quarantine Service said the genetic makeup of the H5N1 bird flu sampled from chickens in Gimje, South Jeolla Province was 99.7 percent identical to a sample from wild swans found in Japan's Akita prefecture and that it was of clade 2.3.2.

More detailed genetic sequencing reported by Recombionics said the swan isolates from Japan were reassortants having clade 2.3.2-like HA (Haemagglutinin), but clade 2.3.4 for the remaining genes. Recombionics went on to say how more recent media reports out of South Korea noted similarities between isolates in South Korea and human sequences in Vietnam. The reassorted genes in the isolates from Japan signal dual infections most easily explained by recombination, the report said.

These sequences, they say, support movement of H5N1 along the East Asian migratory flyway which feeds into Alaska in North America.  The sequences, as well as the location of these isolates in northern Japan, raise concerns that H5N1 is migrating toward North America.  This avenue of migration is also supported by the timing of the outbreaks in Japan and South Korea (April 2008).  Clade 2.3 had not been reported previously in South Korea or Japan, and the record size of the poultry outbreak in South Korea (April 2008) provides new opportunities for H5N1 to evolve as birds migrate out of those countries and into Siberia and Alaska, Recombionics claimed.

Experts warn against complacency 

Latest reports (August 2008) of wild swans infected with avian influenza virus come from North America though not with H5N1. H7N3 was detected in a small number of mute swans collected from the Seekonk River (Rhode Island State) during routine surveillance performed by the Department of Environmental Management's Division of Fish & Wildlife. The swans were caught near the Swan Point Cemetery in Providence and subsequently tested by the USDA. Four of the 11 birds were found to be infected with the H7N3 strain of the avian influenza virus. CIDRAP NEWS said it was a low pathogenic virus, but there was no indication as to whether the swans showed clinical symptoms of avian influenza.

Recombionics says reports of H7 outbreaks in the US have become more common.  The most recent was in poultry in Arkansas.  Initially only antibodies were detected, but low pathogenic H7N3 was subsequently isolated. In addition, H7N3 sequences from Delaware and Maryland have been deposited at Genbank but have not yet been released, Recombionics said in its August 21, 2008, release.  Previous outbreaks of H7N3 bird flu in poultry include USA (Texas, 2004), Canada (British Colombia 2004; Saskatchewan 2007), and UK (Norfolk 2007).

Experts have consistently warned that H7 avian influenza subtypes are showing increasing evidence of adaptation for human infection and the ability to transmit between humans.  H7 outbreaks are frequently linked to human infections although so far most cases have been mild.  More aggressive human cases have been reported for H7N2 (New York, 2002, and United Kingdom, 2007) and H7N7 (Netherlands, 2004). Most human H7N3 cases, where occurring (e.g. Canada and UK), are linked to eye infections. More information on the pathogenicity of these isolates would be useful, says Recombionics.

Some of the most telling comments were made by the local press in Providence, Rhode Island, USA, and similar to those made by the UK press following a recent outbreak of H7N7 in poultry in the County of Oxfordshire. Both compared their respective H7 subtypes “favourably” with H5N1 and claimed they were of little or no risk to humans.  It is this is kind of complacency that virologists and influenza experts on both sides of the Atlantic are warning against.

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