Influenza in Migratory Birds and Evidence of Limited Intercontinental Virus Exchange

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Abstract
Migratory waterfowl of the world are the natural reservoirs of influenza viruses of all known subtypes. However, it is unknown whether these waterfowl perpetuate highly pathogenic (HP) H5 and H7 avian influenza viruses. Here we report influenza virus surveillance from 2001 to 2006 in wild ducks in Alberta, Canada, and in shorebirds and gulls at Delaware Bay (New Jersey), United States, and examine the frequency of exchange of influenza viruses between the Eurasian and American virus clades, or superfamilies. Influenza viruses belonging to each of the subtypes H1 through H13 and N1 through N9 were detected in these waterfowl, but H14 and H15 were not found. Viruses of the HP Asian H5N1 subtypes were not detected, and serologic studies in adult mallard ducks provided no evidence of their circulation. The recently described H16 subtype of influenza viruses was detected in American shorebirds and gulls but not in ducks. We also found an unusual cluster of H7N3 influenza viruses in shorebirds and gulls that was able to replicate well in chickens and kill chicken embryos. Genetic analysis of 6,767 avian influenza gene segments and 248 complete avian influenza viruses supported the notion that the exchange of entire influenza viruses between the Eurasian and American clades does not occur frequently. Overall, the available evidence does not support the perpetuation of HP H5N1 influenza in migratory birds and suggests that the introduction of HP Asian H5N1 to the Americas by migratory birds is likely to be a rare event. Influenza surveillance in wild migratory birds has been done at two sites in North America: 1) in Alberta, Canada, for the past 31 years, and 2) along Delaware Bay, United States, for the past 22 years. These studies support the concept that wild migratory birds are the reservoirs of all influenza A viruses and that the influenza viruses in the world can be divided into two distinct superfamilies, one in Eurasia and the other in the Americas. From time to time these viruses spread to domestic poultry and to humans and cause pandemics of disease. Many investigators have expanded these studies particularly in Europe, Asia, and the Americas. The emergence of highly pathogenic H5N1 in Asia a decade ago and the continuing evolution and spread of these H5N1 viruses to the whole of Eurasia is a continuing problem for veterinary and human public health. The available evidence from Eurasia is that migratory birds can be infected and may be involved in local spread of the highly pathogenic H5N1 virus. The question addressed in the present study is why the highly pathogenic H5N1 influenza virus has not yet reached the Americas despite the overlap in migratory bird pathways, particularly in Alaska. Genomic analysis of influenza viruses from our repository failed to provide evidence of influenza viruses with their whole genome originating from Eurasia. However, we found occasional influenza viruses from North America with single or multiple genes that originated in Eurasia. Our interpretation is that while influenza viruses do exchange between the two hemispheres, this is a rare occurrence. Regardless, enhanced surveillance should be continued in the Americas in case this rare event occurs.