Avian influenza: An unfinished story

Avian influenza — often referred to in the media as “bird flu” — has become one of the most publicized emerging infectious diseases since late 2003.

This followed the detection of highly pathogenic avian influenza (HPAI) caused by viruses of the H5N1 subtype in many countries in Asia. These Asian-lineage HPAI viruses produced fatal disease in poultry, wild birds, humans and other mammals, with subsequent spread of disease to at least 52 countries across three continents.

According to data from the World Organisation for Animal Health (OIE), the virus has caused 6,700 outbreaks in domestic fowl holdings in 52 countries from the end of 2003 to March 30, 2010. The disease was reported in 30 countries in Asia, 12 countries in Europe and 10 countries in Africa.

With the help of the international donor community, affected countries have mobilized hundreds of millions of dollars to assist in disease control efforts. Concerns about the potential of these viruses to unleash a global pandemic of human influenza have prompted comprehensive action.

Though the infectivity of the virus in humans seems to be limited, WHO data indicate that the recorded fatality rate for the disease was alarming — it killed 291 out of the 492 registered, laboratory-confirmed human patients in 15 countries from 2003 to March 30, 2010.

It appears as though ’swine flu,’ which has been officially designated by WHO as “pandemic (H1N1) 2009” has overshadowed the continuous circulation and threat of avian influenza, at least in the public perception and in media coverage. Since the emergence of swine flu in April 2009, the disease has been reported in 213 countries.

Spread of H1N1 has declined since early 2010. As of March 30, 2010, WHO statistics indicate that it has caused “only” 16,931 deaths. The fear that this virus will perpetrate a pandemic reminiscent of the historical Spanish flu has enabled avian influenza to return to the frontline, though at a lower profile than what was observed in previous years.

Avian influenza recurrence

The recurrence of avian influenza in European domestic fowl — namely in the Romanian Danube delta — after being absent from domestic poultry in Europe since the end of 2007 is indicative of the continuous circulation of this zoonotic virus.

Since the beginning of 2010, the continuous or recurrent circulation of H5N1 has been reported to the OIE from 13 countries.

In nine of these countries, the reports were related to domestic fowl kept in commercial or backyard holdings: Vietnam (29 outbreaks), Bangladesh (17), Nepal (7), Bhutan and India (5 each), Myanmar (3), Romania (2), Cambodia and Israel (1 each). In four countries — Bulgaria, China (mainland), China (Hong Kong) and Russia — the 2010 cases were diagnosed in wild birds, found dead and forwarded to the laboratory for investigation.

Prior to the outbreak on Jan. 24, 2010, the last outbreak in Israel was in January 2008. That outbreak occurred at a large commercial farm with an advanced biosecurity system. It was eradicated by a total culling of the affected flock of birds.

A significant period had also passed since the last outbreak in Bulgaria.

Before consecutive outbreaks in the Tulcea region of the Danube Delta area of Romania on March 16 and 17, 2010, H5N1 was previously detected in Romania via a single backyard fowl holding in Tulcea on Nov. 27, 2007.

In October 2005, Romania was the first country in mainland Europe to detect the H5N1 virus in poultry. That outbreak was also in the Danube delta, which is Europe’s largest wetlands. This area lies near the Black Sea and is a major flyway of migratory birds.

For obvious reasons, experts suspect that wild birds introduced the virus into this region. However, the subject has caused an ongoing heated debate between two groups of investigators, which have emerged since the start of the panzootic era in 2003. The question at hand is this: Are migratory birds responsible for the maintenance of H5N1 and its distribution, or is the virus maintained and spread by human activities, intensive poultry industry systems and (legal and illegal) animal transportation?!

The detection of an H5N1-infected common buzzard (a hawk) in Bulgaria, some 200 km south of Tulcea and similarly on the coast of the Black Sea, has added fuel to the debate. It is the spring migration period of these birds from eastern Africa to their habitat in Europe. In the absence of a smoking gun in infected premises, only circumstantial evidence could be applied in most cases. However, several experimental infection trials in wild species, such as mute swans, have produced some incriminating evidence that some birds can become subclinical carriers of this highly pathogenic virus. The debate is continuing.

In this respect, readers may find the following outcome of the epidemiological investigation, carried out by the Israeli Veterinary Service concerning the January 2010 outbreak, of interest:

“The epidemiologic investigation revealed that no birds were introduced into the farm since the chicks were placed and that no birds were moved out of the farm. The two workers on the farm had no contact with other birds since the chicks were placed. Movements of the vaccinating crew and the treating veterinarian have been investigated and three contact farms were identified. These three farms are located with the surveillance zone and therefore are under the surveillance procedures. Feed was delivered to the poultry houses from outside the fence by underground feed pipes.

The epidemiological report did not reveal any specific reason concerning the introduction of the virus into the affected poultry house. One possible scenario is the introduction of the virus into the single infected house by stepping on infected droppings in the area between the sanitary facilities (where clothes and shoe-changing and showering take place) and the entrance to the poultry house. No foot baths were used at the entrance to the houses. Within several km of the farm there are fish ponds and sewage treatment ponds that attract a high number of wild birds in general and water fowls specifically.

During the investigation, wild ducks, cormorants and aigrettes were seen flying over the farm.”

Similarly, in the January 2008 incident in Israel, no alternative explanation to the introduction of the virus could be found.

Several recent papers provided contradictory views and debatable experimental results on this issue. Molecular virology, epidemiology and ornithology experts have become intensively involved and may enhance plausible explanations for the continued circulation of the virus and its repeated introduction to some sites after periods of apparent absence.

Despite all of this, one point remains unabated, avian influenza, or rather HPAI H5N1, has become one of the panzootic zoonoses with the longest lifespan and widest distribution. It will probably keep epidemiologists, public-health and animal-health experts, physicians, veterinarians, ecologists, ornithologists and researchers busy for an extended period. This virus’ potential for becoming a pandemic is also still under investigation. Undoubtedly, the infection is a formidable subject for the exercising of One Health.

Arnon Shimshony, DVM, is Associate Professor at the Koret School of Veterinary Medicine Hebrew University of Jerusalem, Rehovot, and is the ProMED-mail Animal Diseases Zoonoses Moderator. Dr. Shimshony was Chief Veterinary Officer, State of Israel, from 1974 to 1999.