The Modern Ecology of Avian Influenza

Many emerging infectious diseases in human populations originated among animals. Attention has often focused on wild animal reservoirs, but most zoono-tic pathogens (ones which can be passed between animals and humans) of recent concern to human health either originate in, or are transferred through domesticated animals raised for human consumption. A case in point in Highly Pathogenic Avian Influenza (HPAI) which has resulted in massive poul-try-house culls in recent years.

Intensive food animal production systems and their associated value chains dominate in developed countries and are increasingly important in developing countries. These systems are characterized by large numbers of animals being raised in confinement with high throughput and rapid turnover. Although not typically recognized as such, industrial food animal production generates unique ecosystems—environments that may facilitate the evolution of new patho-gens and their transmission to human populations.

It is often assumed that confined food animal production reduces risks of emerging diseases. Evidence suggests, however, that these industrial systems may increase animal and public health risks. Moreover, the economic drivers and constraints faced by the industry and its participants must be fully understood in order to develop effective preventive policy.

The high-profile emergence of human diseases from animal populations, such as Nipah virus infection in 1999 in Malaysia and Singapore, SARS in 2002 in China, and HPAI from 1997 to the present around the world, have heightened public awareness of linkages between animal populations and human health.

Yet the environments of domesticated food animals—systems that are driven by unique ecological, social, and economic factors—are not usually recognized as ecosystems in and of themselves, with intense interactions between animals, humans, and pathogens. But the industrial food animal ecosystem is exactly that—a distinct entity consisting of organisms (including humans, domesticated and wild animals, and microorganisms) interacting with each other and an anthropomorphically designed environment designed to maximize profit rather than biological sustainability.

Avian flu exemplifies how ecological conditions of animal husbandry and the food production supply chain can influence health risks for human populations worldwide. In the industrial farm, pathogens can move by unregulated and unrecognized pathways, such as on airborne dust, via nuisance insects, in animal wastes utilized in agriculture and aquaculture, in contaminated water, and by wild animals. While individual countries have taken steps to contain outbreaks at the farm level and to reduce local dissemination of the flu, the globalized nature of the food animal production industry and supply chain must be recognized for its role in augmenting rapid transmission of pathogens across long distances.

Modern Industrial Production in Poultry-Houses

In industrial poultry production thousands of birds of similar genotypes are raised for one purpose with rapid population turnover at one site under highly controlled conditions, often in confined housing. Such industrial-scale production is expanding rapidly in Asia, Africa, Latin America, North Africa, and the Near East, and is led by both national and multinational corporations seeking expanding markets of increasingly urban consumer populations within these countries. Concerns have been raised over the risk of raising large numbers of birds this way, given the relatively weak veterinary and public health infrastructure in some of these countries.

In the industrialized countries, the vast majority of chickens and turkeys are now produced in houses in which thousands of birds are confined throughout their lifespan. Increasingly, pigs and cattle are also raised under similar conditions of confinement and high density.

For poultry (and pigs), industrial production is organized in stages with separate primary breeders, multipliers, and producers (often contract growers). A small number of globally operating companies form the apex of the breeding pyramid. The feeds supplied to animals in industrial operations are highly formulated and substantially different from the foraged feeds traditionally available to these same species. This sector is also dominated by a small number of commercial entities.

The consolidation of poultry and pig production was undertaken for reasons of competitive advantage and has greatly affected the geography of food ani-mal populations. In the USA, poultry production is highly concentrated in the southeastern states, with more than 40% of total production occurring in Georgia, Arkansas, and Alabama. Reasons for locating in the south include less restrictive environmental and public health regulation as well as access to farmland for disposal of manure and a lessened need for heating in winter when ventilation fans bring in cold air. Similar trends have occurred world-wide.

The geographic concentration of pig and poultry production has also increased regional and global movement of animals and their products. In the indus-trial model, different production stages are often undertaken at different sites, requiring a significant amount of live animal transfers, some of which cross national borders.

These transfers provide significant opportunities for interactions between large populations of confined animals, which may contribute to the evolution and transmission of infectious pathogens. This may be of particular relevance to the evolution of human-to-human transmissible avian influenza, as oc-curred in the 1918 pandemic.

Furthermore, animals held in confinement produce large volumes of waste. Much of this waste, which contains many pathogens, is disposed of on land without any requirements for pretreatment, posing an opportunity for human contact and transmission to wild animals, both avian and mammalian.

The fact that poultry production has been transformed from smallscale methods to industrial-scale operations has important consequences. There is substantial evidence of pathogen movement between and among these industrial facilities, release to the external environment, and exposure to farm workers. This challenges the assumption that modern poultry production is more biosecure and biocontained than backyard or smallholder operations in preventing introduction and release of pathogens.

History of the Emergence of Novel Influenza A Viruses

Avian influenza (AI) is an infectious viral disease of birds (especially wild water fowl such as ducks and geese), often causing no apparent signs of illness. AI viruses can sometimes spread to domestic poultry and cause large-scale outbreaks of serious disease. Some of these AI viruses have also been report-ed to cross the species barrier and cause disease or subclinical infections in humans and other mammals.
AI viruses are divided into 2 groups based on their ability to cause disease in poultry. Highly pathogenic viruses result in high death rates (up to 100% mortality within 48 hours) in some poultry species. Low pathogenicity viruses also cause outbreaks in poultry but are not generally associated with se-vere disease.

Wild aquatic birds are believed to be the primary reservoir of influenza A viruses, and all influenza A viruses in mammals likely have ancestral links to avian lineages. An important feature of influenza A viruses is their capacity to undergo molecular transformation through recombination and reassort-ment, which facilitates adaptation to new host populations and thereby the potential to cause major disease outbreaks in humans and other species. Influ-enza A viruses are classified on the basis of their HA (hemagglutinin) and NA (neuraminidase) antigens and their pathogenicity to chickens. Strains that cause severe disease and high levels of mortality are classified as highly pathogenic avian influenza while viruses causing milder disease in domesticated poultry are classified as low pathogenic avian influenza (LPAI).

The transition from LPAI to HPAI can result from a single mutation affecting a surface protein. The probability of such a mutation is amplified in the set-ting of industrial poultry production due to the rapid viral replication that occurs in an environment of thousands of confined, susceptible animals.

Pigs may potentially assume a separate important role in the emergence of novel influenza A viruses, as they can be infected by both avian and human viruses. Note the proximity of concentrated poultry and swine operations as a source of disease risk from influenza A viruses, although to date there have only been reports of avian influenza viruses in pigs, not swine influenza in poultry.

The A(H5N1) virus subtype, a highly pathogenic AI virus, first infected humans in 1997 during a poultry outbreak in Hong Kong. Since its widespread re-emergence in 2003 and 2004, this avian virus has spread from Asia to Europe and Africa and has become entrenched in poultry in some countries, resulting in millions of poultry infections, several hundred human cases, and many human deaths.

Food Animal Production Workers at Risk

A number of recent studies demonstrate that influenza A viruses from animals can move across the animal:human interface in the context of food animal production and processing.

While fewer people are now engaged in animal husbandry at fewer sites, the high throughput and confinement of highly concentrated animal populations increases the intensity of microbial exposures for farmers, their families, farm workers, veterinarians, and others in contact with these operations.

The conditions of work provide many opportunities for both worker infection and transfer to others in the community. There has been minimal atten-tion to animal-human interactions associated with the operation and management of broiler poultry houses. Many workers are provided little or no protective clothing or opportunities for personal hygiene or decontamination on-site. Studies of poultry house workers in Maryland indicate that work-ers take their clothes home for washing.

Environmental Contamination Pathways

In addition, the design and operational requirements of large-scale swine and broiler poultry houses result in other compromises of biosecurity. Through multiple pathways, pathogens move in and out of these facilities and are then available for exchange among wild avians, domestic avians, swine, and other animals as well as humans.

The rapid spread of avian influenza among poultry flocks can be partly attributed to air exchanges between confinement facilities located within several hundred meters of one another. Tunnel ventilation systems, which are increasingly used in the U.S. industry, consist of eight 1-meter-diameter fans posi-tioned at one end of the building. These fans generate large quantities of aerosolized dust and emissions of small particles from broiler houses.

Other points of release and interspecies transfer include methods of handling animal house wastes, the use of poultry house wastes in aquaculture, and open-truck transport of food animals from farms to processing plants. Pathogen contamination of shipping containers and trucks, which are not enclosed, is known to occur, and animal stress during transport increases pathogen shedding.

Food Animal Wastes and Biosecurity

In addition to the production of animals for human consumption, industrial farms also produce large amounts of animal waste, or biosolids. Animal bio-solids contain a range of pathogens that may include influenza viruses, which can persist for extended periods of time in the absence of specific treatment. Apart from some use in animal feeds and aquaculture, poultry and swine wastes are almost entirely managed by land disposal. Contamination of both surface and ground water can result from these practices. Moreover, both holding and land disposal of poultry wastes can attract wild avians because spilled feed is present in these wastes.

In addition, there is growing use of poultry and duck house wastes for use as feed in land-based aquaculture operations. This mode of pathogen transfer is wholly unregulated. Open impoundments for aquaculture are essentially small wetlands, and they are frequently visited by wild avians, setting up an-other setting for bidirectional pathogen transfers. It should be noted that the fecal-water-oral route is considered a highly probable mode of transmission of avian influenza virus between birds.

There is a paucity of research on transfers of viruses from industrial farms; however, there is extensive literature on the exchange of bacteria among con-fined food animals, wild animals, humans, and the environment. This literature supports concerns about the efficacy of biocontainment at industrial food animal production operations.

Outbreaks

Further evidence of the limits of current bioexclusion measures in large-scale industrial poultry operations is provided by recent HPAI H5N1 outbreaks reported in large-scale industrial poultry units with supposedly high biosecurity standards in South Korea (a 300,000 bird unit), in Russia (two 200,000 bird units), and in Nigeria (a 50,000 bird unit), and in the UK (a 160,000 turkey unit).

Large industrial flocks appear to be overrepresented in the list of HPAI H5N1 outbreaks reported compared to outbreaks in backyard/village flocks, in relation to their respective shares of total national flocks.

Given that a gram of infected feces can contain as many as 10 billion infectious virus particles, a small amount of contaminated fecal material or litter ad-hering to boots, clothing, or equipment may be sufficient to transmit virus from an infected to a susceptible flock.

Increased Risks in Confined Poultry Flocks

The hypothesis that confined poultry operations may present increased risks of HPAI has been tested through an analysis of data on the 2004 HPAI epi-demic in Thailand, which also includes a separate dataset from the nationwide active surveillance program undertaken by the Thai government to detect HPAI infections in poultry. These data are unique and highly relevant to addressing questions on biosecurity and biocontainment risks associated with different modes of poultry production.

An analysis of that Thai data (taken from approximately 230,000 flocks in more than 50,000 villages) indicates that the odds of H5N1 outbreaks and in-fections are significantly higher in large-scale commercial poultry operations as compared with backyard flocks. This data suggests that successful strategies to prevent or mitigate the emergence of pandemic avian influenza must consider risk factors specific to modern industrialized food animal production.

Similarly, data from Canada, although incomplete, have also indicated that in contrast to backyard flocks, large commercial operations were dispropor-tionately affected by a 2004 HPAI outbreak.

Economics

As it can be more profitable to raise animals in areas where feed is abundant, e.g., close to feed mills, areas of high poultry density have emerged in a number of regions worldwide. Semi-vertical integration of production processes, where a large company supplies young birds and feed, while farmers provide housing and labor, has often not been accompanied by systematic spatial planning of the units in the system. Although spatial concentration is convenient from an organizational point of view, it has serious drawbacks for the control of epidemic diseases.

Poultry production is also inherently an economic activity, driven by financial incentives and profit motives. These economic forces exist in parallel with the biological pressures that moderate pathogen evolution and spread. Improving the sustainability of current poultry production methods relies on a clear understanding of these economic incentives and their relationship to biological drivers of avian influenza emergence.

Conclusions

There have been major changes in many aspects of domestic poultry production in the U.S. and other countries during the 20th century, resulting in in-dustrial-scale operations involving high densities of confined avian populations, which is how most of the world’s animal protein sources are now derived. To date there has been little consideration of industrial poultry production as an ecosystem, in its own right, for understanding emerging infectious dis-ease. These changes in organization, intensity, housing, and waste generation, however, seriously influence the emergence and transfer of diseases among wild and domestic species, and from animals to human populations.

Some of the measures being considered to make the raising of backyard flocks safer, including the forced housing or confinement of poultry, are not likely to result in a major reduction of disease risks. In contrast, the costs will likely be significant and will be imposed upon a marginal group of entrepreneurs and household producers. This may result in an overall reduction of outbreaks as a consequence of the loss of household production flocks, but not as a result of enhanced biosecurity and biocontainment.

This articles is based on a World Health Organization fact sheet on avian influenza, a Public Health Reports article “The Animal-Human Interface and Industrial Food Animal Production: Rethinking Biosecurity and Biocontainment”, and an EcoHealth article “Industrial Food Animal Production and Global Health Risks: Exploring the Ecosystems and Economics of Avian Influenza”