Could climate change spread avian influenza and create a global pandemic

Influenza A viruses have been isolated from many species including humans, pigs, horses, mink, felids, marine mammals and a wide range of domestic birds, but wild birds belonging to the orders Anseriformes (particularly ducks, geese, and swans) and Charadriiformes (particularly gulls, terns, and waders) are thought to form the virus reservoir in nature (Olsen et al., 2006). Climate change and alterations in the environment or animal breeding processes could be responsible for the mutations undergone by the virus and the jumps from one species to another. Ducks and other aquatic birds tend to congregate into flocks in the late fall and winter, creating dense populations that are optimal for efficient influenza transmission. Because of their likely avian origin in ducks and other shorebird, the winter seasonal nature of influenza in humans may be a relic of avian influenza in bird species.

H5N1 avian influenza spread rapidly across Asia from east to west. The pathways by which the virus has and will spread between countries have been debated extensively, but have yet to be analyzed comprehensively and quantitatively. Despite intensive research, the means by which this spread was accomplished have remained extraordinarily controversial. Evidence is beginning to suggest that a combination of factors have all contributed to the persistence and spread of H5N1: movements by infected wild birds, transportation of infected domestic birds, and uncontrolled interactions between wild and domestic birds. To minimize the adverse effects of avian influenza, it is critical to detect its presence in a potential host population - whether wild bird or domestic poultry - early enough to mount an appropriate and effective response. Understanding the role of migratory birds in the spread of avian influenza viruses, the epidemiology of the avian influenza virus and its subtypes, and the exposure rates of various wild species are essential to future management of this disease.

The H5N1 virus has become established in bird populations of Southeast Asia and it has probably already reached the Arctic through migratory water birds. Avian flu virus can last indefinitely at a temperature dozens of degrees below freezing, as it is found in the northern most areas that migratory birds frequent. Influenza A viruses can survive over 30 days at 0°C (over 1 month at freezing temperature). Recently Scott Rogers from Bowling Green State University in Ohio and his colleagues found the influenza A virus genes in ice and water from high-latitude lakes that are visited by large numbers of migratory birds (Rogers et al., 2006). It shows that there is potential for a human virus to survive the freezing process. Imagine if older, more vicious strains, such as the virus responsible for the Spanish flu pandemic, which killed somewhere between 20 and 40 million people in 1918-1919, were to re-emerge. So if these viruses have been huddled in the ice for thousands of years, how did they get there in the first place? According to Rogers et al. one very effective way for viruses to travel the world is to hitch a ride in the guts of migrating birds. As the birds visit lakes along their paths they shed viruses into the lakes and onto the ice (when present) and drink water containing viruses discharged by other birds or released from the ice by thawing. Therefore, these lakes become abiotic mixing pools for the viruses, while the birds are the biotic vessels where mixing occurs (including replication and recombination). Since there are susceptible hosts along their migration path, they may pass the viruses to other birds as well as to swine, humans, or other animals.

Mixing and recombination of American and Eurasian influenza strains occurs in regions such as Alaska where these species mix and breed (Pederson et al., 2004). When birds migrate south they carry and disseminate these viruses along their migratory pathways.

Until recently, bird flu outbreaks mainly occurred in Indonesia, Vietnam, Thailand, Laos, Cambodia, and China. But in July, 2005, Russia and Kazakhstan confirmed H5N1 outbreaks in poultry and wild birds. Birds flying from Siberia have carried the virus to the Greece, Turkey, and eastern Europe. Many scientists believe migrating wild fowl are responsible for carrying the virus from Asia and Siberia to Romania and Turkey. The scientists found that viruses from the most recently affected countries, all of which lie along migratory routes, were almost identical to viruses recovered from dead migratory birds at Qinghai Lake in China. The viruses from Turkey's first human cases were also virtually identical to the Qinghai Lake strain. In Romania, the outbreak was first detected in and around the remote Danube Delta, Europe's largest wetlands which also happen to lie on a major migratory route for wild birds.

Although some argue there is not enough evidence yet for firm conclusions, the theory is gaining ground. Kilpatrick et al. (2006) integrated data on phy-logenetic relationships of virus isolates, migratory bird movements, and trade in poultry and wild birds to determine the pathway for 52 individual introduction events into countries and predict future spread. They showed that 9 of 21 of H5N1 introductions to countries in Asia were most likely through poultry, and 3 of 21 were most likely through migrating birds. In contrast, spread to most (20/23) countries in Europe were most likely through migratory birds. Spread in Africa was likely partly by poultry (2/8 introductions) and partly by migrating birds (3/8). Theirs analyses predict that H5N1 is more likely to be introduced into the Western Hemisphere through infected poultry and into the mainland United States by subsequent movement of migrating birds from neighboring countries, rather than from eastern Siberia. These results highlight the potential synergism between trade and wild animal movement in the emergence and pandemic spread of pathogens and demonstrate the value of predictive models for disease control (Kilpatrick et al., 2006).

It is increasingly acknowledged that migratory birds, notably waterfowl, play a critical role in the maintenance and spread of influenza A viruses. In order to elucidate the epidemiology of influenza A viruses in their natural hosts, a better understanding of the pathological effects in these hosts is required.

Wild birds were thought not to suffer from mild forms of avian influenza. But new data suggest that so-called 'low-pathogenic' avian influenza viruses do affect the lives of birds. According to scientist Jan van Gils from Netherlands Institute of Ecology, infected swans clearly suffer from their 'mild' disease. The late departure from the wintering grounds could lead to late arrival in the breeding grounds, and thus to a lost breeding season. All in all, these low-pathogenic viruses have a much greater impact than previously thought. Because of their slower migration, ill birds get in touch with many more healthy birds passing by them on migration. In this way the virus can spread itself more rapidly than previously thought (Van Gils et al., 2007).

Acquiring more knowledge about mild but illness-causing avian influenza viruses is very important. Van Gils suggests that these mild virus types always formed the origin of massive pandemics such as the Spanish Flu and that only such viruses that are non-lethal to birds can be spread easily by (wild or captive) birds, simply because the birds stay alive. Only after mixing with human flu can such a low-pathogenic avian flu cause the nightmare of a deadly pandemic among humans. High-pathogenic avian flu that causes death among birds seems to originate from intensive poultry farms.

Biologists reported on the feeding and migratory performance of wild migratory Bewick's swans (Cygnus columbianus bewickii Yarrell) naturally infected with low-pathogenic avian influenza (LPAI) A viruses of subtypes H6N2 and H6N8. Using information on geolocation data collected from Global Positioning Systems fitted to neck-collars, they showed that infected swans experienced delayed migration, leaving their wintering site more than a month after uninfected animals. This was correlated with infected birds traveling shorter distances and fueling and feeding at reduced rates. The data suggest that LPAI virus infections in wild migratory birds may have higher clinical and ecological impacts than previously recognized (Van Gils et al., 2007). This contrasts previous ideas that mild forms of bird flu do not cause illness among wild birds. Moreover, these patterns can affect the rate of spread of avian influenza. Warming climate may be a factor in the population increase and expansion in distribution. Biologists believe that climate change is affecting living things worldwide, and the latest evidence suggests that warmer winters may mean fewer migratory birds. New research shows that as winter temperatures have risen in central Europe, the number of migratory birds has dropped. Ultimately, this may also decrease the number of migratory bird species there (Society for Conservation Biology, 2003).

new highly pathogenic human strain

Fig. 45.1 Reassortment of viral RNA genome segments (genetic mixing or recombination) creating a new viral strain.

Wild aquatic water birds are the primary reservoir of influenza A viruses and bird influenza viruses serve as a genetic reservoir for other animal influenza strains including those that infect humans (Widjaja et al., 2004; Webster et al., 2002). The past influenza pandemics of the twentieth century are all of avian origin (Horimoto et al., 2005), including the 1918 influenza pandemic (Taubenberger et al., 2005). According to Taubenberger, the Spanish flu virus that killed up to 50

million people in 1918-1919 was "...avian like virus that adapted to humans". The researchers believe the two other major flu pandemics of the twentieth century - in 1957 and 1968 - were caused by human flu viruses which acquired two or three key genes from bird flu virus strains. The greatest concern is that the H5N1 virus will recombine with a human virus that will give the new strain the capacity to become readily transmitted from person to person (Fig. 45.1). In places with high concentrations of domestic pigs and chickens, pigs may serve as a "mixing vessel" for the virus because of their genetic similarity to humans.

In 1997, the new avian influenza virus (H5N1 avian flu) emerged in Hong Kong killing six people. This was the first time that an avian influenza virus was shown to be transmitted directly from birds to humans. The virus persisted in the region, and has since spread to a number of 60 countries in Asia, Europe, and Africa (Fig. 45.2). Twenty-six countries have experienced outbreaks in 2007. Except for a few outbreaks in wild birds, most of the confirmed outbreaks have been in domestic poultry, including chickens, turkeys, geese, ducks, and quails.

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Fig. 45.2 Areas reporting confirmed occurrence of H5N1 avian influenza in poultry and wild birds since 2003.

The World Health Organization says there have been 329 cases of human avian influenza, including 206 deaths, with the highest number of cases reported in Indonesia and Vietnam. The avian H5N1 strain is highly virulent to people with a mortality rate of over 60% (Marshall et al., 2005). The case distribution upon age groups is different in avian influenza as compared to seasonal flu. For the latter, the casualties are usually the very young and the very old, as exemplified by a V-shaped graph. For the pandemic flu, it is inverse with the youth with being the victims (Fig. 45.3). As of February 2008, the median age of patients influenza A (H5N1) virus infection is approximately 18 years. The overall case fatality proportion is 61%. The primary pathologic process that causes death is fulminant viral pneumonia (WHO, 2008). Handling of sick or dead poultry during the week before the onset of illness is the most commonly recognized risk factor. Although the A (H5N1) virus is at present poorly adapted to humans, limited human-to-human transmission continues to occur.

Fig. 45.3 Human avian influenza A (H5N1) cases by age group and country.

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