Understanding the animal-human interface is a critical element in evaluating and predicting risks of emergent zoonoses, as well as in designing evidence-based programs for prevention and early detection of emerging infectious diseases, such as avian influenza. This has been well documented in terms of zoonoses arising from wild animal species77
and in regard to food safety,78
but it remains underrecognized in terms of workers involved in the production of domesticated animals.
There have been major changes in many aspects of domestic food animal production in the U.S. and other countries during the 20th century, resulting in industrial-scale operations involving high densities of confined animal populations, which is how most of the world's animal protein sources are now derived. These changes in organization, intensity, housing, and waste generation may influence the emergence and transfers of avian influenza virus among wild and domestic species, and from avians to human populations. If this is the case, then inferences based upon the last global and national experience with pandemic avian influenza in 1914–1918 may need reconsideration.
Most importantly, the modern methods of both poultry (particularly broiler chickens) and swine production have changed. These operations result in high numbers of poultry and swine housed under confined conditions at great density and geographic concentration. These operations have also changed the management and autonomy of animal husbandry: individual farmers are increasingly supplanted by large producers that contract with growers to raise animals. This has implications for public health surveillance and interventions, as the farmer no longer makes decisions in relation to feeding, housing, or operations. Access to animal facilities is also increasingly controlled by producers rather than farmers. These changes in some cases may have beneficial impacts in terms of early detection and veterinary oversight.
These new methods of food animal production generate many routes of pathogen transfer among wild and domesticated species and from animals to humans through occupational, peri-occupational, and environmental pathways. At the animal-human interface in these operations, there is inadequate protection of workers and their communities, and, more generally, there is incomplete biocontainment to prevent transfers from the animal house to the general environment. Indeed, the main emphasis of disease prevention with increasing production intensity is typically on enhancing biosecurity, whereas biocontainment is considered less of a priority. Evidence would suggest that once a pathogen has been introduced into such a production facility, it can rapidly multiply; for some pathogens, enormous quantities of infectious organisms can be released and expose other production units. For example, it has not been recognized that the necessity for high ventilation of densely confined animals greatly impairs attempts at biocontainment. Moreover, little attention has been given to the generation and lack of management of the millions of tons of animal wastes generated annually. Food animal wastes are largely disposed on land, and this creates an unrecognized magnet for wild avians because of the presence of undigested feed in the waste. There is some use of poultry wastes as bedding for fish ponds, which creates an additional opportunity for wild avian contact. Studies of bacterial pathogens provide strong evidence for the bidirectional transfers of pathogens among poultry grown in these confined operations, wild birds, and human populations.
Our analysis of the Thai HPAI outbreak and surveillance data suggests that commercial poultry production, an ostensibly more “biosecure” system of production, is not associated with a reduction in risk of HPAI infection at the farm or flock level, as compared with that experienced by subsistence backyard producers. Although the majority of reported HPAI outbreaks in Thailand in 2004 occurred in the latter, this increased cumulative risk of HPAI in the backyard sector is primarily due to their relatively greater numbers rather than more risky production practices.
Some of the measures being considered to make backyard poultry production safer, including the forced housing or confinement of poultry, are not likely to result in a major reduction of HPAI 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 HPAI outbreaks as a consequence of the loss of household production flocks, but not as a result of enhanced biosecurity and biocontainment.
Additionally, the geographic concentration and housing density of commercial poultry production can greatly augment the spread of HPAI in an infected area. A study of an outbreak in The Netherlands found that the transmission rate of the virus was not necessarily affected by improved biosecurity and biocontainment measures but by depletion of susceptible flocks due to complete depopulation of infected areas.79
The authors suggested that reducing flock density in commercial flocks might reduce the probability of a major epidemic in which large numbers of poultry flocks must be culled. Following the aforementioned HPAI outbreak in Canada, restriction permits for the development of new operations were proposed as a method to control the density of commercial operations when deemed too close to existing farms.36
This analysis suggests that renewed attention to the animal-human interface should focus on high-risk populations, especially farm workers. A similar conclusion was reached by Saenz et al.18,80
in an analysis of the risks of influenza outbreaks and transmission to human populations in the context of large-scale commercial poultry and swine production. Monitoring this population may improve detection of early events in emergence of avian influenza. In addition, careful evaluation of operations at all poultry facilities—large and small—should be undertaken to reduce opportunities for the transmission of disease among avian and other species. Moreover, if appropriate protections such as vaccination are identified, the agricultural workforce constitutes a high-risk population for whom protection from zoonotic disease is important not only for their health but for the health of their communities and the population at large. Finally, improved oversight and management of animal wastes—including transport and sale as well as use in aquaculture—should be included in strategies to reduce risks of pandemic HPAI.