The day after we received the HPAIV (H5N1)–containing common buzzard carcass, officials in Romania notified the OIE of an outbreak of an HPAIV (H5N1) in Letea Village (Danube Delta); 47 backyard chickens were found dead. These reports are considered to be the introduction of HPAIV (H5N1) clade 2.3.2.1 into Europe. Furthermore, the European Reference Laboratory on Avian Influenza and Newcastle Disease (Weybridge, UK) found that the HA gene sequence of the Bulgarian isolate is 99.9% similar to that of the Romanian isolates from Letea Village (34), confirming that both viruses are derived from a common source, which is most likely wild birds.

St. Konstantin and Helena Black Sea Resort, where the common buzzard carcass was found, is located on the border of Batova (43°21′11′′N, 27°57′33′′E), which is a complex of habitats typical for woodland bird species, waterfowl, and poultry. This area is defined as a bottleneck migration site of global importance because 3 flows of migratory birds meet over the Batova River Valley (35). Each spring (March–April), migratory waterfowl from Africa, Bosphorus, and the Dardanelle Straits stop at the lakes along the coast of the Black Sea in Bulgaria on their way north (36). Their next resting spot is the Danube Delta, where the Romanian outbreak occurred and <250 km from where the Bulgarian buzzard carcass was found. Thus, if we are correct in our hypothesis that birds from Via Pontica are the hosts that carried the HPAIV (H5N1) to Bulgaria and Romania, the virus most likely came from Tyva and Mongolia, where its ancestral viruses had been isolated, to Via Pontica by using >2 other overlapping flyways. Although this is the most likely scenario, it is still unconfirmed. To confirm this hypothesis, the pathogenicity of A/common buzzard/Bulgaria/38WB/2010 in ducks and its possible transmission among them must be defined, which will require additional biologic studies.

To trace the possible routes of introduction of HPAIVs (H5N1) into Bulgaria, the veterinary authorities and ornithologists from the Bulgarian Society for the Protection of Birds organized continuous monitoring of the bird areas along the Black Sea coast, near the Danube River and around the Ogosta Dam and Lom River. From January 1, 2010, through April 30, 2010, a total of 812 cloacal, fecal, and tissue samples from wild birds collected from these areas were tested for avian influenza virus; 269 samples were collected after March 15, 2010. All samples tested were negative for HPAIV (H5N1). Five carcasses of common buzzards found in different areas were submitted to the Regional Diagnostic Lab on Avian Influenza after March 15, 2010; only 1 was carrying HPAIV (H5N1).

Common buzzards are considered territorial birds that usually do not migrate long distances. A 3-year study conducted in southern England showed that local radio-tagged common buzzards forage within 1 km of their nests during their first winter; most of the birds that do not disperse make only brief excursions before they opt for a stay-at-home strategy, and most of those that disperse return to their natal area during the following breeding season (37). Long-term ornithologic studies conducted during 1979–2005 in Bulgaria, however, showed unambiguously that extensive autumn and spring migrations of common buzzards (as many as 42,100 birds) occur on the western Black Sea Via Pontica flyway (35,38). Kostadinova et al. reported ≈6 pairs of common buzzards breeding in the Batova habitat, but during autumn and spring migrations, ornithologists counted as many as 19,712 individuals of the species in the area (35). In most cases, common buzzards migrate singly or in loose flocks with other raptors, lesser spotted eagles, white pelicans, or black storks (38).

Migration of common buzzards in different parts of Europe appears to depend on the local climate; buzzards from northern Europe fly to the western Black Sea area during the winter season, whereas buzzards from Bulgaria fly south. Tracking bands belonging to common buzzards from Finland, Romania, and Israel have been found in Bulgaria (39). The buzzard infected with HPAIV (H5N1) in Bulgaria was not banded; however, even if it had been a migrant, the habitat nearest to St. Konstantin and Helena Black Sea Resort that provides different food sources is Batova, with an area of 38,132.8 ha (35). The migration of the common buzzards suggests that these birds are capable of spreading pathogens over long distances.

Our results show that chickens are highly susceptible to influenza virus A/common buzzard/Bulgaria/38WB/2010 (H5N1) and that the virus is highly pathogenic in them. Mammals appear not to be susceptible. Although buzzards can serve as intermediate hosts of HPAIV (H5N1) between migratory birds and poultry, the lack of gross pathologic findings in the buzzard carcass we examined indicates that the bird died shortly after infection. Thus, in this case, the buzzard could not have served as a reservoir of infection to spread the virus over a long distance. Additionally, the lack of poultry farms within 10 km of the area where the buzzard carcass was found may partially explain why no outbreak occurred. As part of a regular avian influenza surveillance plan, we tested 1,709 cloacal and fecal samples from mule ducks that were collected monthly during January 1, 2010–April 30, 2010, from 64 farms in 5 regions of Bulgaria (Plovdiv, Pazardjik, Stara Zagora, Haskovo, and Dobrich). No notifiable avian influenza viruses were isolated from any sample.

Since clade 2.3.2 was first isolated from a dead Chinese pond heron in Hong Kong in 2004, it has spread geographically and evolved genetically. A new fourth-order clade, 2.3.2.1, was recently identified, and A/common buzzard/Bulgaria/38WB/2010 was classified in this clade (8). The question that arises now that clade 2.3.2.1 has spread from Asia to Europe is whether it can cause a scenario similar to that caused by clade 2.2 from 2005–2006, when HPAIV (H5N1) killed millions of birds in Asia, Europe, and Africa. Although no new HPAIV (H5N1)–related events have been reported in Europe since March 2010, some of the aspects of the 2.3.2.1 clade make it difficult to predict the consequences of the clade’s arrival on the continent. For example, this clade is already widely distributed in Asia and is being perpetuated in many wild bird species, which is a prerequisite for long-distance distribution through migration. Wild bird species infected with HPAIV (H5N1) from clade 2.3.2.1 include gray herons, peregrine falcons, and great egrets in Hong Kong; whooper swans, ruby shelducks, and bar-headed geese in Mongolia; and grebes and black-headed gulls in Tyva (8).

The potential of clade 2.3.2.1 HPAIV (H5N1) to cause an outbreak is heightened because vaccines currently in use do not efficiently protect poultry flocks from a strain of this clade that was recently identified in Vietnam (40). Now that clade 2.3.2.1 has spread to Europe, implementing active surveillance plans in all high-risk areas and monitoring the wild birds in the region will play key roles in early detection of incidences of HPAIV (H5N1) infection and in prevention of outbreaks. The expansion of the geographic distribution of HPAIV (H5N1) in wild birds and poultry and the virus’s repeated interspecies transmission to humans make this virus a substantial pandemic threat.