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Institute of Medicine (US) Forum on Microbial Threats; Knobler SL, Mack A, Mahmoud A, et al., editors. The Threat of Pandemic Influenza: Are We Ready? Workshop Summary. Washington (DC): National Academies Press (US); 2005.

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The Threat of Pandemic Influenza: Are We Ready? Workshop Summary.

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4Strategies for Controlling Avian Influenza in Birds and Mammals


To address the threat that avian influenza (AI) poses to human health, it is necessary to recognize its broader agricultural and economic implications and to integrate this knowledge into disease control strategies. This chapter focuses on the global phenomenon of avian influenza, its impact on the poultry industry, and potential means to control influenza transmission among birds and mammals.

The chapter begins with a review of the activities of the Office International des Épizooties (OIE; also known as the World Organisation for Animal Health), an international and intergovernmental organization at the forefront of animal disease control. The OIE is developing influenza surveillance guidelines that encompass birds, domestic mammals, wildlife, and humans. The OIE recently initiated cooperation between its global network of reference laboratories and that of the World Health Organization (WHO); the partners plan to exchange scientific information on avian influenza, share viral isolates, and may eventually manufacture human vaccines against avian viral strains.

While avian influenza is an uncommon disease of poultry in the United States, the U.S. Department of Agriculture (USDA) recognizes the international importance of the disease and has developed considerable animal health policies to detect, prevent, and control avian influenza. These strategies are presented, along with background information on the biology, ecology, and epidemiology of avian influenza, by David Swayne and David Suarez of the USDA. They review evidence that supports intervention and surveillance focused on the subset of avian influenza viruses that pose significant risk of infecting humans, including certain viruses of low pathogenicity in poultry. The chapter concludes with an example of a low-pathogen avian influenza outbreak in a group of commercial poultry farms and the steps the industry took to contain further spread of the virus, minimize the risk of exposure, and monitor and prevent further infections.


Dewan Sibartie

Scientific and Technical Department

World Organisation for Animal Health (OIE)


Preventing the spread of animal diseases and zoonoses through international trade is one of the primary objectives of the World Organisation for Animal Health (OIE). This is accomplished by establishing international standards that facilitate trade while minimizing the risk of introducing infectious animal diseases and zoonoses. The OIE was founded in 1924, as a result of an outbreak of rinderpest in Belgium. Initially 28 countries united with a mandate to share information on animal disease outbreaks to allow the Member Countries to take the appropriate control measures to protect themselves and to prevent further spread of the disease. A total of 167 countries now form part of the OIE, and providing a mechanism for prompt reporting of disease outbreaks and occurrences is still one of the OIE's primary roles.

Over the years, the OIE has been strongly committed to convincing national policy makers and international donors that the cost of strengthening veterinary services to provide better surveillance, early warning systems, and management of epizootics, including zoonoses, is negligible compared to the economic losses resulting from introduction of infectious animal diseases and zoonoses.

The OIE objectives and activities for the prevention and control of infectious animal diseases and zoonoses are focused on the following areas:

  • Transparency in animal disease status worldwide
    Each Member Country is committed to reporting to the OIE on its health status regarding significant animal diseases and diseases transmissible to humans. The OIE then disseminates the information to all Member Countries to enable them to take appropriate actions to protect themselves.
  • Collection, analysis, and dissemination of veterinary information
    Using its network of internationally recognized scientists, the OIE collects, analyzes, and publishes the latest scientific information on important animal diseases, including those transmissible to humans, especially regarding their prevention and control.
  • Strengthening of international coordination and cooperation in the control of animal diseases
    The OIE provides technical expertise to Member Countries requesting assistance with animal disease control and eradication programs, particularly in developing countries. These activities are performed in coordination with other international organizations responsible for supporting and funding the eradication of infectious animal diseases and zoonoses.
  • Promotion of the safety of world trade in animals and animal products
    The OIE develops standards for application by Member Countries to protect themselves against disease incursions as a result of trade in animals and animal products, while avoiding unjustified sanitary barriers. These standards are developed by experts from Member Countries and from the OIE's network of more than 160 Collaborating Centers and Reference Laboratories.

In 1995 the standards developed by the OIE were formalized as international standards by the Agreement on the Application of Sanitary and Phytosanitary Measures (SPS Agreement) of the World Trade Organization (World Trade Organization, 1995). In order to harmonize SPS measures and remove unjustifiable sanitary or health restrictions on international trade, the Agreement states that governments should follow these international standards, guidelines, and recommendations. The goal of the Agreement is to minimize the risk of disease transmission and remove unjustifiable sanitary or health restrictions on international trade. The Agreement states that it is the sovereign right of a country to provide an appropriate level of animal and public health protection at its borders. However, this sovereign right is not to be misused for protectionist purposes: An importing country can only apply sanitary measures to imports if a similar level of protection is applied to all imports and internally by the importing country. Member Countries can introduce standards providing a higher level of protection than that provided by the OIE standards if there is a scientific justification, but these standards must be based on a science-based risk analysis.

The OIE recognizes highly pathogenic avian influenza (HPAI) as an OIE list A1 disease having the potential for very serious and rapid spread, irrespective of national borders, which can be of serious socioeconomic and public health consequences and which is of major importance to the international trade of poultry and poultry products. Since 1996 it has become clear that avian influenza viruses may be important pathogens capable of infecting humans directly without reassortment. This has been observed during the recent outbreaks of AI in southeast Asia. However, like other organizations also concerned with human health, the OIE is highly concerned about the possibility that the virus can undergo genetic reassortment and become transmissible within humans, resulting in a pandemic capable of claiming millions of lives, as was the case during the so-called Spanish flu of 1918. Firmly convinced that the best way to reduce human exposure to the virus is to eliminate the virus at source—that is, from animals, including wild birds—the OIE strives to assist Member Countries in providing expertise particularly in the following areas: disease surveillance, early detection, early warning and notification, quality and evaluation of veterinary services, diagnosis, surveillance, control strategies, and international trade in poultry and poultry products.

OIE Reference Laboratories and Experts

The OIE is coordinating a worldwide network of some 150 Reference Laboratories and 13 Collaborating Centers and more than 300 experts in various animal diseases. For avian influenza, there are currently six Reference Laboratories and eight experts, but the OIE also benefits from the expertise of other internationally renowned scientists in the field of AI who are called on to assist OIE ad hoc groups or to carry out technical missions on behalf of the OIE in countries affected by the disease. The OIE Reference Laboratories played a particularly significant role during the avian influenza outbreaks in southeast Asia caused by H5NI strain of the AI virus. Not only have the experts of those laboratories provided technical advice, but they have, for example, also provided useful diagnostic material such as H5 antigens to laboratories in affected countries to assist them in their diagnosis. The application of the Differentiating Infected from Vaccinated Animals (DIVA) tests developed by the OIE Reference Laboratory in Italy will be particularly useful for countries that will embark on the use of marker vaccines for the control of AI. The OIE Reference Laboratories also conduct training courses for technical staff in the diagnosis of the disease and characterization of the virus. In addition, the OIE Reference Laboratories are arranging cooperation with the network of the WHO Influenza Reference Laboratories for the exchange of scientific information, sharing of viruses for strain characterizations, and if necessary, the manufacture of human vaccines from poultry strains of the virus.

OIE Standards

One of the major activities of the OIE is to develop standards, guidelines, and recommendations for the diagnosis and control of important animal diseases, including zoonoses. OIE standards are science-based and are developed by experts and approved by the OIE International Committee, which has representatives from the 167 Member Countries. The World Trade Organization Agreement on Sanitary and Phyto-Sanitary (WTO-SPS) measures recognizes the OIE as the only international organization for setting standards on animal diseases and zoonoses. Standards concerning terrestrial (nonaquatic) animals are contained in the Terrestrial Animal Health Code (the Terrestrial Code) (World Organisation for Animal Health, 2003) and the OIE Manual of Diagnostic Tests and Vaccines, or Terrestrial Manual (World Organisation for Animal Health, 2004a). The Terrestrial Code provides the governments and the Chief Veterinary Officers of OIE Member Countries with recommendations for establishing national health measures or rules applicable to the importation of animals and animal products with respect to OIE listed animal diseases in order to avoid importation of pathogens while avoiding unjustified sanitary barriers. The Terrestrial Manual describes the diagnostic methods that are to be used and the methods for the production and control of biological products, including vaccines.

The Terrestrial Code

Definition of avian influenza infection. Chapter 2.1.14 of the Terrestrial Code provides standards for highly pathogenic avian influenza (HPAI). However, in view of the latest scientific advances, especially regarding the potential risks posed by low-pathogenic strains and the ability of the virus to infect humans, a new Chapter (World Organisation for Animal Health, 2004b) has been proposed by an OIE ad hoc group of experts and is being studied by OIE Member Countries. A new definition of notifiable avian influenza has been proposed as follows:

For the purposes of this Terrestrial Code, notifiable avian influenza (NAI) is defined as an infection of poultry caused by any influenza A virus of the H5 or H7 subtypes or by any AI virus with an intravenous pathogenicity index (IVPI) greater than 1.2 (or as an alternative at least 75 percent mortality) as described below. NAI viruses can be divided into highly pathogenic notifiable avian influenza (HPNAI) and low-pathogenicity notifiable avian influenza (LPNAI):

  1. HPNAI viruses have an IVPI in 6-week-old chickens greater than 1.2 or, as an alternative, cause at least 75 percent mortality in 4- to 8-week-old chickens infected intravenously. H5 and H7 viruses, which do not have an IVPI of greater than 1.2 or cause less than 75 percent mortality in an intravenous lethality test, should be sequenced to determine whether multiple basic amino acids are present at the cleavage site of the hemagglutinin molecule (HA); if the amino acid motif is similar to that observed for other HPNAI isolates, the isolate being tested should be considered as HPNAI.
  2. LPNAI are all influenza A viruses of H5 and H7 subtypes that are not HPNAI viruses.

Disease notification. The current Terrestrial Code provides for countries to report HPAI within 24 hours. If the proposed Chapter is approved, countries would start notifying all NAI as defined above. Countries also need to report a provisional diagnosis of HPAI if this represents important new information of epidemiological significance to other countries. The OIE in turn forwards this information to other countries in order for countries at risk to take appropriate precautions. Following outbreaks of AI in southeast Asia, the OIE collaborated with other international organizations to provide expertise to countries in the region to improve their disease reporting systems. Thanks to the “rumours tracking system,” the OIE has been able to query some countries about rumours of the possible occurrence of AI in those countries. This system proved effective in that at least two countries that had not reported the disease to the OIE then confirmed the presence of the disease. In view of the zoonotic importance of the disease, the OIE is working in close collaboration with WHO on the notification of all important zoonoses. As a result there is constant and instant sharing of information between the two organizations about the occurrence of AI in animals and humans.

Evaluation of veterinary services. The Terrestrial Code provides guidelines for the quality and the evaluation of veterinary services (which include public and private components) in Member Countries. This is important to assert the credibility of the services because it enhances the international acceptance of the certification of exports and facilitates the risk analysis process of an importing country. The results of this evaluation can help provide the importing country the assurance that information on sanitary/ zoosanitary situations provided by the veterinary services of an exporting country is objective, meaningful, and correct. Evaluation of veterinary services has gained further importance since the ban on imports of poultry and poultry products from several southeast Asian countries following the avian influenza crisis. For countries to resume their trade, especially with Europe, the veterinary services must demonstrate efficiency in terms of diagnosis, surveillance, and certification for exports. The Terrestrial Code spells out the procedures for an independent and reliable certification free from political or other commercial considerations.

International trade of poultry and poultry products. As mentioned earlier, the OIE provides standards, guidelines and recommendations to assure the sanitary safety of international trade in animals and animal products to avoid the transfer of agents pathogenic for animals or humans while avoiding unjustified sanitary barriers. In this context, the OIE is fully aware of the constraints faced by countries wishing, for example, to export fresh poultry meat. These constraints relate mainly to vaccination, surveillance, and zoning/compartmentalization. The new proposed Chapter attempts to solve some of these constraints, especially in the light of the outbreaks in southeast Asia, Europe, and North America. During a meeting of AI experts jointly organized by the Food and Agriculture Organization of the United Nations (FAO), the OIE, and WHO, held in February 2004 in Bangkok, Thailand, the three organizations agreed that due to ethical, social, economic, and environmental reasons, the stamping-out policy may not be appropriate for some countries in the region. Thus they recommended that vaccination, which has proved to reduce morbidity, mortality, and virus shedding, can provide an additional useful tool in those countries provided that the vaccines used comply with the standards of the OIE Terrestrial Manual and that vaccines are administered under the supervision of the official veterinary services. The veterinary services should have the necessary expertise and resources to ensure that appropiate and adequate surveillance is carried out to avoid possible problems caused by vaccination, the main one being the difficulty in differentiating infected from vaccinated animals by serology.

The proposed Code Chapter allows the export of live birds from countries, zones, or compartments that have been vaccinated provided details of the vaccines and the vaccination programs are stated. In order to assist well-managed enterprises with a high level of biosecurity to export, the Chapter proposes that the concept of compartmentalization be adopted. The Code defines “compartmentalization” as “one or more establishments under a common biosecurity management system containing an animal subpopulation with a distinct health status with respect to a specific disease for which required surveillance, control, and biosecurity measures have been applied for the purpose of international trade.” This concept will enable countries having integrated and well-managed poultry enterprises to export under certain conditions even if the rest of the country is infected.

The new Chapter also proposes that a country or zone/compartment may be considered free from NAI when it has been shown that NAI infection has not been present for the past 12 months. If infected poultry are slaughtered, this period shall be 3 months (instead of 6) after the slaughter of the last infected poultry and disinfection of all affected premises. This would encourage countries wishing to resume exports to carry out stamping-out whenever feasible and apply strict biosecurity measures.

The OIE has already put at the disposal of Member Countries relevant expertise to help them improve the production and quality control of vaccines. Such help is also available for the establishment of OIE Reference Laboratories on AI.

Surveillance and monitoring of animal health. The Terrestrial Code has a generic chapter outlining the general requirements for a country to carry out surveillance and monitoring of animal health. The fundamental principles described in that Chapter also apply to avian influenza. However, an OIE ad hoc group of experts will soon be working on a specific Chapter on surveillance guidelines for avian influenza, taking on board the latest scientific knowledge on AI. In the meantime the new proposed Chapter on AI spells out certain general ideas on serological surveillance in flocks, especially in the presence of vaccination. The DIVA tests developed by an OIE Reference Laboratory will prove helpful to countries using marker vaccines. The principle of this test is accepted by the OIE, and further work on its applicability to other animal diseases is in progress in some OIE Reference Laboratories.

Information provided by the exporting country's surveillance and monitoring program is considered to be a key component of the risk analysis conducted by an importing country. OIE has provided and will continue to provide expert assistance to southeast Asian countries to improve surveillance and monitoring systems to control the disease. The OIE advises that countries establish programs to monitor high-risk avian populations, such as live bird markets, fighting cocks, and other markets selling wild birds. This should decrease the risk of AI transmission through trade.

The Terrestrial Code also provides detailed procedures for conducting a risk analysis that also applies to AI. Member Countries are allowed under the WTO-SPS Agreement to apply a higher level of SPS measures provided there is a scientific justification and it is supported by a risk analysis.

The Terrestrial Manual

The Terrestrial Manual is a companion volume to the Terrestrial Code and provides a uniform approach to the diagnosis of HPAI. Its purpose is also to facilitate international trade in animals and animal products by describing internationally agreed-on laboratory methods for avian influenza diagnosis and requirements for the production and quality control of AI vaccines. The methods described also form the basis for effective avian influenza surveillance and monitoring. The serological techniques described include the hemagglutination-inhibition and agar gel immunodiffusion tests. The immunodiffusion test is a group-specific test that can detect all strains of avian influenza virus and is appropriate for a monitoring program. The Chapter also mentions the use of commercial Enzyme Linked Immunosorbent Assay (ELISA) kits that detect antibody against the nucleocapsid protein. Such tests have usually been evaluated and validated by the manufacturer, and it is essential that the manufacturer's instructions be followed. Although not specifically mentioned in the Chapter on HPAI, the importance of marker vaccines and the DIVA test are well recognized by the OIE. Virus isolation techniques and virus characterization techniques for the confirmation of HPAI are also described in detail.

Stamping-Out and Carcass Disposal

The OIE continues to rely on the principle that stamping-out remains the method of choice for the rapid elimination of the virus and thus its spread to humans, but is fully aware that this method is not applicable to certain countries for reasons stated earlier. For this reason, the OIE has an ad hoc group that has formulated recommendations for the mass slaughter of animals during an emergency and the safe disposal of carcasses. These methods vary depending on the available resources, equipment, and infrastructure. Work is progressing by an OIE ad hoc group on carcass disposal, and the OIE will finalize details of the methods applicable in different situations.

Food Safety

In pursuance with one of its missions to ensure safety of food of animal origin, OIE experts have conducted research on the possible contamination of humans through the consumption of poultry meat or products. This has been particularly important during the recent influenza outbreaks in southeast Asia, when consumption of these commodities fell drastically, threatening millions of farmers who depend almost entirely on subsistence animal farming for their livelihoods. Therefore it was important to restore consumer confidence in poultry products. OIE experts have concluded that humans can only be infected while in contact with infected birds and that the main mode of transmission in humans in the context of this Asian epizootic is by the respiratory route. In addition, they have demonstrated that when poultry products are cooked to an internal temperature of at least 70°C, the virus is destroyed.

The Role of Wildlife

The role of wildlife in the transmission and spread of AI has been widely discussed by the international scientific community. In a February 2004 meeting, the OIE experts in the Working Group on Wildlife Diseases reviewed the available literature and other relevant documentation and made the following salient observations:

  • Virtually all H and N combinations have been isolated from birds.
  • Wild birds, particularly those associated with aquatic environments, are the reservoirs of viruses of low virulence for poultry.
  • Viruses may become virulent following transmission and cycling in commercial poultry.
  • There is current concern about the lack of knowledge on the prevalence of viruses of H5 and H7 subtypes in bird populations.
  • Outbreaks of disease in commercial poultry have been linked to a close association between commercial poultry and waterfowl on many occasions.
  • Isolation of virus from other wild birds is completely overshadowed by the number, variety, and distribution of influenza viruses isolated from waterfowl. The highest rate of detection of influenza virus is from ducks.
  • The concentration of ducks, their potential to excrete high levels of virus and its ability to remain viable in an aquatic environment means that “large” areas of the environment will be contaminated.
  • Different virus subtypes can be identified simultaneously within a single bird.
  • The predominant subtype isolated from domestic ducks varies from year to year.
  • Natural protection of ducks does not provide cross-protection between influenza A subtypes.
  • Influenza viruses can sweep through bird populations without having any signs of disease present.
  • Studies indicate that the viruses identified in Eurasia and Australia are genetically distinct from those in North America. This most likely reflects the distinct flyways of each hemisphere.
  • There is an “avian influenza season” (at least in temperate countries) in the fall/winter.
  • Surveillance programs of wild birds when outbreaks of poultry influenza have occurred often find little or no signs of infection.

Therefore, they recommend that as far as practically possible, wild birds should be separated from commercial poultry. Surveillance programs should also be conducted in wild birds, placing more emphasis on ducks and using sentinel birds to detect presence of the disease; in temperate zones, surveying should be concentrated in young birds in the fall/winter. They also emphasized that surveillance is of global interest because this type of information in one country is important for other countries to know.

However, the Working Group is of the unanimous opinion that the role of wild birds in occurrences of virulent influenza A in poultry and in humans is widely misunderstood. Virulent strains of these viruses seldom have been found in wild birds, even in association with outbreaks in poultry. The Working Group does not contest the possibility that the co-cycling of more than one influenza strain within a so-called “mixing vessel” host such as the pig may result in genetic exchanges and genetic shift. Such events could result in the evolution of highly pathogenic viral strains with rapid passaging and spread, especially within and between intensively farmed poultry houses, and with high risk of “cross-over” infection to humans. Control programs for virulent strains of avian influenza viruses therefore should be focused on biosecurity of poultry populations and protection of humans exposed to poultry.

Continual OIE Involvement

The OIE continues to monitor the worldwide AI situation closely, paying particular attention to southeast Asia, where the disease has far more economic and possibly more public health impact. Relevant information is posted continuously on the OIE website ( to update Member Countries on the prevailing situation. On March 19, 2004, the OIE again alerted countries on the unjustified optimism being displayed by certain countries on the perception that the epidemic is over. The OIE has appealed to Member Countries to maintain vigilance because the virus is still circulating and eradication is a long way ahead. This has been proven to be true as outbreaks of highly pathogenic avian influenza have again been recently recorded in some countries of southeast Asia that thought they had successfully overcome the outbreaks.

Since January 27, 2004, the OIE has been alerting international donors about the pressing need to provide assistance to countries in southeast Asia affected by the disease. Assistance also should be provided to strengthen veterinary services and to improve surveillance and early response to diseases. There cannot be any delay in this assistance not only because of economic reasons, but because no opportunity should be given to that virus to undergo genetic reassortment in human beings and thus create a new human influenza pandemic.


David E. Swayne and David L. Suarez

U.S. Department of Agriculture, Agriculture Research Service, Southeast Poultry Research Laboratory, Athens, Georgia


Strategies to control avian influenza virus are developed to prevent, manage, or eradicate the virus from a country, region, state, county, or farm. These strategies are developed using various aspects of five components: (1) biosecurity, (2) diagnostics and surveillance, (3) eliminating poultry infected with AI virus, (4) decreasing host susceptibility to the virus, and (5) education. Avian influenza in U.S. commercial poultry is uncommon. Prevention of AI is the preferred strategy and is practiced primarily by reducing the risk of introduction or exposure. The primary risks for introduction into commercial poultry include: (1) direct access to wild birds infected with AI viruses, (2) the drinking water source being untreated surface water contaminated with AI viruses, (3) location in the same geographic region as pigs infected with endemic swine influenza virus (turkey breeder hens only), and (4) epidemiologic links to a live poultry marketing system. Vaccines are uncommon and used only in areas of high risk. The USDA licenses all AI vaccines. However, both the USDA and state veterinarian determine when licensed vaccines can be used in the field.

Background on Avian Influenza

Avian influenza is a disease of birds caused by type A orthomyxovirus (Swayne and Halvorson, 2003). Avian influenza viruses are pleomorphic and have eight segments of single-stranded, negative-sense RNA that code for 10 proteins. These proteins include two surface glycoproteins, the hemagglutinin (HA) and neuraminidase (NA), and internal proteins such as the matrix (M) and nucleoproteins (NP). Serologic reaction in the agar gel immunodiffusion (AGID) test to the M and NP is the basis for speciation or classification of all AI viruses as type A influenza viruses (influenza A viruses). Furthermore, serologic reaction to the HA and NA are the basis for subtyping into 15 HA (H1-15) and 9 NA (N1-9) subtypes, respectively.

Avian influenza viruses are grouped into two broad pathotypes based on virulence in chickens: (1) viruses of low virulence, that is, low-pathogenicity AI (LPAI); and (2) viruses of high virulence, that is, high-pathogenicity AI (HPAI) (Swayne and Halvorson, 2003; Swayne and Suarez, 2000). The LPAI viruses can be any of the hemagglutinin (H1-15) and neuraminidase (N1-9) subtypes. The LPAI viruses cause various clinical problems ranging from clinically in apparent infections to drops in egg production and mild respiratory disease with low mortality rates. However, more severe respiratory disease and higher mortality rates may be seen when such infections are accompanied by secondary viral or bacterial pathogens. By contrast, HPAI viruses have all been of the H5 or H7 hemagglutinin subtypes and produces severe, often fatal, systemic disease affecting multiple internal organ systems. In birds raised on the ground, the infection spreads rapidly, but in poultry houses where birds are caged, the infection may spread more slowly. Infections with HPAI may present with depression, decreased feed consumption, and possibly neurological signs. Lesions seen may include edema-to-necrosis of comb and wattles, edema of the head and legs, subcutaneous hemorrhages of feet, petechial hemorrhages on surface of viscera, and pulmonary edema, congestion, and hemorrhage. For regulatory purposes, AI viruses are classified as high pathogenicity (HP) when they cause 75 percent or greater mortality in intravenously inoculated chickens (all HA subtypes) or have a deduced amino acid sequence at the hemagglutinin proteolytic cleavage site compatible with HPAI virus (H5 or H7 only).

Type A influenza viruses are continually changing either through random mutation in the genome (drift) or through rearrangement of gene segments between two different influenza viruses (shift). The latter results in hybrid or reassortant viruses.

Several detailed reviews have been published in the general area of AI (Swayne and Halvorson, 2003) and HPAI (Swayne and Suarez, 2000), ecology and epidemiology of AI (Swayne, 2000; Webster et al., 1992), AI vaccines (Swayne, 2003), AI control in the United States (Swayne and Akey, 2004), and immunology of avian influenza (Suarez and Schultz, 2000).

Ecology and Epidemiology

Avian influenza viruses exist in five discrete ecosystems (Swayne, 2000). The reservoir for genes of all type A influenza viruses circulate in wild bird populations, principally waterfowl (Order: Anseriformes) and shorebirds (Order: Charadriiformes), but to a lesser frequency in other wild birds, especially in aquatic habitats (Kawaoka et al., 1988; Slemons et al., 1974). The virus appears to be well adapted to these species, causing only an asymptomatic enteric infection with large amounts of virus being shed into the environment. For ducks, such as mallard or pintail ducks, the highest incidence of infection is usually in the fall, when large numbers of young naïve ducks congregate before flying south for the winter. The incidence of infection typically drops to low levels in the winter months, but virus can often be isolated all year long. The wild bird population therefore remains a reservoir source of virus that cannot be practically controlled (Stallknecht and Shane, 1988). Most AI viruses isolated from wild birds are low pathogenicity (LP), but a few have been HP, especially when isolated from wild birds trapped on poultry farms affected with HPAI.

Common poultry species, including chickens and turkeys, are not natural hosts for avian influenza viruses (Hopkins et al., 1990; Suarez, 2000). If chickens are experimentally infected with wild duck isolates, typically the viruses will replicate at low levels, not be transmitted efficiently from bird to bird, and cause little to no disease (Lee et al., 2004). In this situation, the virus will typically fail to maintain itself in the poultry population with or without human intervention. However, through captivation and domestication, humans have altered the natural ecosystems and created four new and different ecosystems where AI viruses may exist and cause avian infections: (1) backyard (village) and recreational poultry (fighting cocks), (2) live poultry market system, (3) outdoor-reared semi-commercial to industrial poultry (ducks and geese, meat turkeys, and “organic” chickens), and (4) indoor-reared industrial poultry (broilers [meat chickens], meat turkeys, egg-laying chickens, breeders, and ducks). However, the risk for AI virus introduction and maintenance varies with each ecosystem. The ecosystems with the highest risk for AI virus infections are 1, 2, and 3 because they may have direct or indirect exposure to wild birds that carry AI viruses. Mixing of poultry species on a farm increases the opportunity for crossing species and adaptation.

Species Adaptation and Transmission

Influenza viruses adapt and have optimal replication in a single animal species with common and easy intraspecies transmission. However, interspecies transmission within the same class is occasionally reported, such as pig to human or wild mallard to domestic turkey. Most rarely, transmission has occurred interspecies and interclass, such as bird to human and bird to pig. Such interspecies transmission is usually inefficient and produces self-limiting infections. However, the influenza A viruses can adapt to the new host species through circulation as low-level infections within a population and, through random mutations in the viral genome, gradually adapt to the new species with increased efficiency of replication and transmission. Alternatively, an existing influenza A virus can reassort with another influenza A virus, producing a hybrid influenza A virus with the resulting eight gene segments being a combination of those from the two viruses. This type of change produced the human pandemic viruses of 1957 and 1968, and the H3N2 swine influenza viruses reported recently in the past 20 years around the world.

Risk Factors for Introduction of Influenza Virus A into Poultry

There are several recognized risk factors for the introduction of influenza A viruses into domestic poultry. The first is direct access of poultry to wild birds infected with AI viruses, especially wild ducks. A good example of this is turkeys in Minnesota that were raised outdoors (“on range”) in the 1980s and early 1990s (Halvorson et al., 1985). Outbreaks of multiple subtypes of avian influenza occurred routinely in the fall, when infected ducks had the opportunity to commingle with turkeys. Once the virus was introduced onto a turkey farm, the virus could become adapted to turkeys and spread to other turkey farms by the movement of infected birds and contaminated materials. In the late 1990s, the practice of range-rearing turkeys was greatly diminished in favor of confinement rearing. This management change reduced the exposure of turkeys to wild ducks, and the incidence of avian influenza outbreaks was greatly reduced.

A second risk factor has been infection through AI virus-contaminated drinking water. For some poultry operations, the birds' drinking water comes from surface sources, such as a lake, where wild birds often have free access. If the drinking water is not properly purified, avian influenza virus could be introduced by this source. The use of raw drinking water was suggested to be the source of AI outbreaks in the United States, Australia, and Chile (Sivanandan et al., 1991; Suarez et al., 2004).

A third risk factor has been exposure of turkeys to pigs infected with the swine influenza virus. Turkeys are susceptible to swine influenza viruses, and having a turkey farm and swine farm in close proximity is a risk factor for the introduction of swine influenza to turkeys. Infections with both classical H1N1 swine influenza and the more recent reassortant H1N2 and H3N2 swine influenza viruses have been reported (Suarez et al., 2002; Wright et al., 1992).

A fourth risk factor for the introduction of AI viruses into commercial poultry is the live bird marketing system, which is found in many countries around the world, including the United States. Live bird markets offer a variety of birds that can be slaughtered and used for human food consumption. Historically, this system was used as a way to maintain the freshness of the product before refrigeration was available. However, in the United States today, the live poultry markets cater to consumers who enjoy the variety of birds, including several types of chickens, quail, pheasant, ducks, geese, and other birds, and the freshness offered by the markets. These markets are extremely popular with certain ethnic populations, and the consumer pays a premium price for the live bird compared to purchase of a chilled or frozen bird from a supermarket. However, this system provides an ideal environment to introduce and maintain avian influenza viruses into the U.S. poultry population. Domestic waterfowl, primarily ducks, are often raised on ponds where exposure to wild birds, including ducks, is common. This provides a high risk for domestic ducks to be infected with avian influenza. These infected ducks are often sold in the live bird marketing system, where there is close contact with chickens, quail, and other gallinaceous birds. These birds can become infected and will typically stay in the markets for a few days before being slaughtered and sold, providing an opportunity for the virus to infect the naïve birds that are being introduced into the market periodically. Many live bird markets are never free of birds, and a continuous cycle of infection can be maintained, with the virus continuing to become better adapted to chickens. The virus in the live bird market system, although generally believed to be separate from our commercial poultry system, has been a nidus of infection for spread to our commercial poultry sector. One example is the H7N2 AI virus that has been circulating in the northeast United States since 1994 and has been associated with at least five different outbreaks in industrialized poultry in seven states (Spackman et al., 2003). Another example is the H5N1 HPAI in Hong Kong, where the associated risk of domestic waterfowl introducing avian influenza to chickens and other gallinaceous birds has prompted the Hong Kong government to segregate gallinaceous birds, and ducks and geese from being sold together. Additionally, the Hong Kong government instituted periodic market closures to try to break the cycle of infection within the market. These changes have appeared effective in reducing the incidence of infected birds in the markets.

Basic Strategies for Avian Influenza Control

AI control strategies are designed to achieve one of three goals or outcomes (Swayne and Akey, 2004): (1) prevention—preventing introduction of AI, (2) management—reducing losses by minimizing negative economic impact through management practices, or (3) eradication—total elimination of AI. These goals are achieved through specific control strategies developed through incorporation and use of five universal components: (1) biosecurity (exclusion and inclusion), including quarantine, (2) diagnostics and surveillance, (3) elimination of AI virus-infected poultry, (4) decreasing host susceptibility to the virus (vaccines and host genetics), and (5) education of all personnel on infectious diseases and their control. Various combinations of these five components will determine whether the outcome of a control program will be prevention, management or eradication.

With HPAI, the U.S. Department of Agriculture has legal jurisdiction over the outbreak and can declare an animal health emergency. This sets into motion a cooperative state and federal eradication program as established in the Avian Influenza Emergency Disease Guidelines (U.S. Department of Agriculture, 1994) and supplemental documents. By contrast, LPAI is a less severe disease of poultry and is under the control of the animal health authority in each state, but some H5 and H7 LPAI viruses have exhibited the ability to mutate from LP to HP after circulation in domestic poultry. The USDA is developing a control program that will make all H5 and H7 AI viruses eradicable in the United States. Internationally, the OIE establishes the animal health standards for trade in poultry and poultry products, and HPAI is a legitimate non-tariff trade barrier. However, control of H5 and H7 LPAI has become an international issue and the OIE is developing new AI standards that will include control of H5 and H7 LPAI.

Surveillance for Avian Influenza in Poultry

Surveillance can be active or passive. Active surveillance is based on statistical sampling of a population to determine the presence or absence of AI infection and typically has utilized detection of AI-specific antibody. However, during an AI outbreak within an infected zone, surveillance for the AI virus in poultry is necessary. By contrast, passive surveillance, usually in the form of diagnostic investigations of respiratory, reproductive, or high-mortality diseases, is based on clinical submissions and looks for the etiological cause of the disease either by isolating the agent or by detecting specific nucleic acids or proteins, in this case, for AI virus. Passive surveillance is used to detect the first HPAI cases in an AI-free area and for identifying additional cases within an infected zone. Passive surveillance—that is, lack of clinical cases—cannot be used as the criteria to demonstrate eradication of HPAI or freedom from AI infections. Active and passive surveillance for antibodies or AI virus is conducted in individual state veterinary diagnostic laboratories and the National Veterinary Services Laboratories (Ames, Iowa). A national active surveillance program for H5 and H7 AI is under development for meat chickens and turkeys with sampling at all slaughter plants and for all egg-laying chickens on the farm. Poultry products from this new program will be certified H5 and H7 AI free.

In the United States, AI is an uncommon disease of commercial poultry and AI virus infections are equally uncommon. In a nationwide survey of commercial poultry through the National Poultry Improvement Plan in 1997 (Personal communication, Andy Rorer, National Poultry Improvement Plan, U.S. Department of Agriculture, April 28, 2001), no AI virus infections were identified in meat chicken (broilers) or meat turkey flocks (Table 4-1). Antibodies to AI virus were detected in turkey breeders of North Carolina, but these antibodies were the result of vaccination with H1N1 vaccine and not from AI virus infections (Table 4-1). Infections to AI viruses were detected in chickens on ten and two egg-type chicken farms in Pennsylvania and Virginia, respectively. The 10 affected farms represented 3 percent of the total egg-layer farms in Pennsylvania and the virus was an H7N2 LPAI virus that spread from the live poultry market system. The two affected farms represented 4 percent of the total egg-layer farms in Virginia and the virus was an H1N1 LP swine influenza virus.

TABLE 4-1. Results of the 1997 U.S. National Survey for Avian Influenza Virus (AIV) Infections by Antibody Detection .


Results of the 1997 U.S. National Survey for Avian Influenza Virus (AIV) Infections by Antibody Detection .

By contrast, the live poultry market system has had LPAI viruses isolated from birds beginning in 1986, with the current H7N2 LPAI virus appearing in 1994 (Mullaney, 2003). The infection rate of the 123 retail markets in the northeast United States has been as high as 60 percent, but control programs have reduced the rate to between 0 and 5 percent. The live poultry market system continues to be a major source of AI viruses and risk for introduction to the commercial poultry operations.

Avian Influenza Vaccines

The AI vaccines provide protection from clinical signs and death, but protection is hemagglutinin subtype specific such that H5 AI vaccines only protect against the H5 subtype, and so on. In addition, AI vaccines can be helpful in decreasing the number of AI virus-infected birds, reducing environmental contamination with the AI virus, preventing spread of AI viruses between farms, and minimizing economic losses. With HPAI, vaccination may help bring an uncontrolled outbreak into a manageable situation, but eradication can only be accomplished if vaccination is accompanied by enhanced biosecurity, active and passive surveillance, education, and elimination of infected poultry as additional components within the control strategy.

In U.S. commercial poultry production, AI is not an endemic disease and vaccination is uncommon. The principal preventive strategy is avoidance of infection by minimizing the risk for AI virus exposure. However, in some areas of the country with high risk of LPAI exposure, limited amounts of vaccine have been used. In 2001, 2,797,000 doses of H1N1 or H1N2 inactivated AI vaccine was used in turkey breeders to prevent infection by swine influenza viruses (Table 4-2) (Swayne, 2001). In layers, 677,000 doses of inactivated H6N2 AI vaccine were used on one egg-laying chicken farm in California (Table 4-2). Vaccine was only used when necessary to prevent an economic animal health issue and was funded by the farmer or production company. Inactivated AI vaccine averages 5 to 7 cents per dose plus 5 to 7 cents to administer each dose.

TABLE 4-2. Avian Influenza Vaccine Usage in United States from July 1, 2000, to June 30, 2001 .


Avian Influenza Vaccine Usage in United States from July 1, 2000, to June 30, 2001 .

In the United States, AI vaccines must be licensed by the USDA's Center for Veterinary Biologics, under one of three authorities, before they can be used. Three types of licenses are issued: autogenous, conditional, and full licensure. Full license has been granted for recombinant fowlpox with H5 AI gene insert (1998) and inactivated H5 (1999) vaccine, but they have not been used in United States. Conditional or autogenous licenses have been granted for various hemagglutinin subtypes, including H6 and H7. Vaccines for H5 and H7 require approval from the USDA and the state veterinarian before use, while all other subtypes only require approval by the state veterinarian for use. Worldwide, Mexico, Guatemala, and El Salvador have used more than 1.3 billion doses of inactivated H5N2 AI vaccine since 1995 and 850 million doses of recombinant fowlpox since 1997. In addition, Pakistan has used inactivated H7N3 AI virus vaccine since 1995. Throughout the Middle East, H9N2 LPAI is endemic, and vaccination with inactivated H9N2 vaccine is commonly practiced.

Public Health Risk for Avian Influenza

AI viruses have rarely produced infections in humans, and these infections rarely result in human-to-human transmission. In addition, not all AI viruses have the same ability to cross the species barrier and infect humans, and AI viruses that are HP for chickens does not predict their ability to infect humans and cause severe disease. In a previous mouse model study using seven H5 HPAI viruses, only the H5N1 HPAI viruses from Hong Kong during 1997 caused high mortality and significant weight loss in BALB/c mice (Table 4-3) (Dybing et al., 2000). One other H5 HPAI virus caused weight loss, but not high mortality (Table 4-3). By comparison, examination of two H7N2 LPAI viruses from the United States in the BALB/c mouse model (Mx-1 influenza-susceptible mice) showed no lethality and more limited infection of the respiratory infection as compared to the highly lethal Hong Kong H5N1 HPAI virus (Table 4-4) (Henzler et al., 2003). Furthermore, in the CAST/Ei mice (Mx+1 influenza-resistant mice), infection with H7N2 LPAI virus was not detected, but H5N1 was still highly lethal for the mice. These studies suggest that some, but not all, AI viruses have the ability to infect mammalian model systems, and intervention strategies should be focused on reducing the risk for those AI viruses with significant risk of infecting humans.

TABLE 4-3. Differences in Virulence of Seven HPAI Viruses for a BALB/c Mouse Used to Predict Human Infection and Disease (Dybing et al., 2000) .


Differences in Virulence of Seven HPAI Viruses for a BALB/c Mouse Used to Predict Human Infection and Disease (Dybing et al., 2000) .

TABLE 4-4. Data on Virus Replication and Mortality in BALB/c and CAST/Ei Mice Following Intranasal Inoculation with Two Low- and One High-Pathogenicity AI Viruses .


Data on Virus Replication and Mortality in BALB/c and CAST/Ei Mice Following Intranasal Inoculation with Two Low- and One High-Pathogenicity AI Viruses .

Finally, the H5N1 HPAI viruses of Asia have been the primary focus as the next potential pandemic influenza viruses. However, we must remember that the previous three pandemics (1918, 1957, and 1968) resulted from reassortment of LPAI with human influenza A viruses and not from HPAI viruses. From that viewpoint, the next pandemic virus could be an H9N2, H6N2, H2N2, or any of a number of hemagglutinin and neuraminidase subtypes. Active surveillance in poultry is a critical issue, and significant veterinary diagnostic and regulatory infrastructure improvements are needed in the developing world to accomplish this goal. These aspects in a global control strategy are lacking in most developing countries, especially Asia. This inability to detect and eliminate AI infections prior to human infections and reassortment are the real threats that may lead to the next world pandemic.


Carol Cardona, DVM, PhD, dipl. ACPV

University of California, Davis

Outbreak of H6N2 Avian Influenza in California

California has experienced a number of outbreaks of avian influenza in commercial poultry over the years. Most of these outbreaks have been in turkeys and have previously been reported (Ghazikhanian et al., 1981; McCapes et al., 1986). Beginning in 2000, an outbreak of H6N2 avian influenza began in commercial egg-laying chickens in southern California (Webby et al., 2003; Woolcock et al., 2003). Initially, the infecting virus caused no disease or clinical signs; however, by 2001, the virus seemed to be more adapted to growth in chickens in that it seemed to spread more easily, and was associated with decreased egg production and decreased egg quality in infected flocks (Kinde et al., 2003). The outbreak expanded to new areas of the state and to new types of poultry over a period of 2 years. Because the strain of this virus was not H5 and not H7, there were no regulations or plans in place to control this virus. Eventually, the poultry industry of California was able to control this outbreak with a voluntary plan they developed, but it was not before a great deal of damage had been done.

The H6N2 low-pathogenicity strain of avian influenza virus, which infected commercial poultry in California, is not a strain regulated by either the California Department of Food and Agriculture (CDFA) or the USDA. Most American trading partners and, therefore, regulatory agencies, focus on H5 and H7 viruses. This is completely understandable because these are the viruses that may mutate to become highly pathogenic strains (Easterday et al., 1997). After our experience in California, we believe that low-pathogenicity strains of all types can cause significant losses for commercial poultry producers. And the same connections between farms that would spread an H5 or an H7 strain would also result in the spread of a virus of any H or N type. Although state and federal regulatory agencies have focused on specific viruses for a very good reason, this is a rather arbitrary decision and one that has limited the study of the AI viruses that are the most prevalent among avian species.

The Spread of AIV Among Commercial Poultry Farms

Commercial poultry companies are first and foremost businesses. They are streamlined to reduce production and processing costs, while maximizing profit margins. Many of the practices involved in the modern production of poultry also support the spread and amplification of disease agents such as AI virus.

In California's experience with avian influenza, one such practice was the movement of eggs from the farm to the processing plant. Eggs are collected from the flocks that produced them, then brought to processing plants, where they are cleaned and packed for stores. This proved to be an important way in which avian influenza was transmitted from farm to farm. Eggs are packed on reusable flats in the chicken house. Those flats are then placed onto pallets or racks, which go to the processing plant. Most eggs that are packed are clean, but some may be contaminated by fecal material. That fecal material is often transferred to the reusable plastic flats, where it becomes mixed with other organic material such as broken eggs. The reusable flats are emptied at the plant, washed (less than perfectly), returned to pallets or racks, and then returned either to the farm they came from or to another unrelated farm. When flats and racks are sent to different farms, they carry infectious material from their farm of origin, resulting in the spread of disease. We suspect that AI virus spread among many egg-laying farms by this means. Other practices that probably played a part in the spread of AI virus in California include moving live birds to slaughter; moving manure off infected farms; rendering pickups of dead birds; sharing equipment; and using common transporters and service crews. These practices alone are not unsafe and would not be suspect if farms were distant from each other, but they were not.

Poultry farms, like many other types of animal agriculture, are frequently located near each other to take advantage of shared resources. These resources include feed mills, rendering plants, slaughter facilities, and markets. The result has been that in parts of California, Georgia, Arkansas, Iowa, North Carolina, and other states with large poultry industries, there are local regions with dense populations of poultry. These dense populations, if infected with AI virus, can serve to exponentially expand the virus in a relatively small region, resulting in the infection of both commercial and noncommercial poultry.

Concentrations of commercial poultry support the growth of population sectors, which in turn support animal agriculture. The large numbers of low-paying, low-skill positions in animal agriculture often attract new immigrants as workers. These new immigrants are frequently also engaged in activities that involve live birds, such as cockfighting and the purchase of birds for food at live bird markets. The former has been implicated in the spread of the exotic Newcastle disease virus in California and the latter has been implicated in the spread and maintenance of H7N2 avian influenza virus in the northeastern United States (Bulaga et al., 2003). Both of these populations, the game fowl and the birds produced for live bird markets, have the potential to become reservoirs of virus for commercial poultry populations. Unfortunately, in California and in other parts of the country, neither of these populations is surveyed regularly for disease, and few markets utilize veterinary services.

The Control of Low-Pathogenicity Avian Influenza in California

Once the commercial companies involved in the California outbreak realized they could not economically live with this virus, they developed a voluntary control plan that required surveillance and biosecurity, and placed limits on the movements of infected flocks. The first part of the plan required participants to minimize the risk of exposure with the following biosecurity practices:

Transportation of birds

  1. Minimize the movement of birds
    1. Use on-site composting or cremation if possible to dispose of carcasses after euthanasia
  2. Move birds safely, if they must be moved
    1. Avoid driving near other poultry facilities
    2. Test flocks 2 weeks prior to movement
    3. Birds with clinical disease should never be moved
    4. Clean, disinfected trucks should be used
    5. Principles of biosecurity should be closely followed
  3. Move infected birds only to slaughter
    1. Actively shedding birds should not be moved to another facility
    2. Previously infected birds are strongly discouraged from movement except to slaughter

Movement of manure

  1. Manure trucks must be tarped before they leave any facility
    1. They must follow routes that avoid contact with other poultry traffic
  2. Multiple pickups from different farms on the same day are not allowed
  3. Manure should be pushed to the edge of the property for pickup
    1. Traffic patterns should be established that avoid interaction between manure trucks and other farm traffic
    2. Scheduling should be done to avoid clean traffic
  4. Manure should not be spread or stored close to any other poultry

Marketing of eggs

  1. Dedicated racks and flats will be used for each ranch
  2. Racks and flats from different ranches will not be commingled
  3. Flats will be washed and disinfected at the processing plant
  4. Rack washing at the processing plant is strongly encouraged

Feed mills and feed delivery

  1. Feed trucks should be cleaned and disinfected at the feed mill
    1. They should be kept away from “clean” areas of the production facility
    2. They should be cleaned and disinfected again when they enter a facility
  2. Drivers should be either kept away from “clean” areas or provided with protective clothing
  3. All trucks and equipment leaving a facility should be cleaned and disinfected before exiting the facility if suspect or positive flocks are present

Movement of crews

  1. A representative of the poultry company will monitor all work performed by crews to ensure that the following rules are observed:
    1. Protective clothing and footwear provided by the ranch must be worn
    2. Hand washing is required before handling birds
    3. Crew vehicles should be cleaned and disinfected before they enter a facility or, preferably, they should be left off site

Mortality disposal

  1. Onsite cremation or composting are the preferred methods of mortality disposal
  2. Use renderers safely, if they must be used
    1. Tarp trucks
    2. Put mortality pickup at the edge of the property
    3. Coordinate the routing of the truck to avoid “clean” farm traffic

Shared employees

  1. Employees should not be shared by poultry companies
  2. Employees are required to wear clean clothes to work
  3. Employees are required to disinfect their footwear before entering production facilities
  4. Clean rooms for changing and clean clothes should be provided for employees
  5. Shower facilities are optimal, but are not required

Shared equipment

  1. Equipment should not be shared between poultry facilities
  2. If it is shared, it should be cleaned and disinfected at both ends

Physical proximity

  1. Communicate with neighbors to avoid behaviors that endanger each other's flocks
  2. Control vectors (rodents and insects) as much as possible
  3. Communication of disease status between neighbors is required

Common vendors (propane, utility, supplies, etc.)

  1. Keep unnecessary visitors off the farm
  2. Visitors should wear protective clothing to enter the facility
  3. A consistent visitor policy should be established for all premises
  4. Keep a logbook of visitors

The producer participants in the plan were also required to Monitor for new infections with the following surveillance of their flocks:

  1. When there is little risk of infection, flocks will be tested at slaughter
  2. During times when there is a risk of infection:
    1. 20 birds will be tested for AI by AGID monthly
    2. Flocks must be checked daily for:
      1. Decreases in egg production
      2. Increased mortality
      3. Clinical signs of disease

The next critical step is to determine what should happen with a positive flock. Because there was no money for the indemnification of their losses, depopulation of the flocks was not considered an option. However, the producers selected another strategy, controlled marketing, which has been highly successful in controlling AI in turkeys in Minnesota (Halvorson et al., 1986). The California plan required the following to Control the virus—making a responsible response to AI virus infection:

  1. Negative flocks (never infected with avian influenza virus) have no restrictions on movement
  2. Virus-negative flocks (previously positive but no longer shedding virus):
    1. Move to slaughter
    2. Pullets (young hens) may be moved to a positive lay ranch
  3. Suspect flocks
    1. Get a diagnosis as soon as possible
      1. Contact your veterinarian, and/or
      2. Submit birds to the diagnostic laboratory
    2. Notify your neighbors
    3. Self-quarantine
  1. Positive flocks (currently infected and shedding avian influenza virus)
    1. Notify neighboring poultry farms
    2. Self-quarantine
      1. Do not move birds until the flock is no longer shedding virus
      2. Coordinate movement of the flock to minimize risk
        1. Document route and time of travel and let other producers know
      3. or
        Euthanize and dispose of the flock on site (composting or cremation)
        1. Limit exposure of carcasses to predators and other mechanical vectors

The final step in the California control plan is how to Prevent infection in future flocks. In this step, the California producers relied heavily on the use of a killed autogenous vaccine. The use of vaccine allowed them to stop the cycle of infection in multi-age farms, which have a continuous flow of new birds entering the infected farm. Vaccination was highly successful for most farms, but only when implemented in conjunction with biosecurity practices.

  1. Clean and disinfect the farm
    1. Leave sufficient downtime before repopulation (at least 2 weeks)
  2. Use of vaccine in flocks at risk of infection
    1. Fulfill all CDFA/USDA requirements for biosecurity and flock plans

Using this voluntary plan, California controlled and eradicated H6N2 AI virus from commercial poultry flocks. The producers in the state soon learned that not telling each other about AI virus infections resulted in the spread of the outbreak. The outbreak was stopped when more communication began among all types of producers. This seems like a simple lesson to have learned, but the poultry producers and processors in California are no different from other small business owners in that they do not usually share confidential information with their competitors. To achieve the level of communication that resulted in the eradication of AI virus in California, all participants had to agree not to use infection status to gain a competitive advantage.

Exposure of Humans to Poultry in the United States

The U.S. commercial poultry industry protects public health by focusing its efforts on preventing poultry infections with AI viruses. This goal of prevention is both economically rewarding for the poultry business and a sound public health practice. However, because natural AI virus reservoirs are widely dispersed, this strategy does not always work, as was the case in California. When AI virus infections occur, it is important to understand where and how the general public interacts with poultry in order to assess and minimize risk of spread.

Many people envision poultry production as it was 100 years ago, as a dozen chickens on the family farm. However, today, poultry production occurs on large farms that house dense populations of chickens or turkeys. The industrialization of food production has meant that the general public is not exposed to the processes by which they are fed. The work force that produces all the food we need to survive is small and in the case of poultry, includes workers in poultry facilities and slaughterhouses, bird haulers, vaccination crews, manure haulers, renderers, and veterinarians. These workers are the most likely to be exposed to poultry pathogens infecting commercial poultry flocks.

In many parts of the world, poultry for consumption are purchased live, allowing the consumer to assess the bird's health and fitness. Live bird markets also exist in the United States, on the east coast, in the midwest, and in the major immigrant centers on the west coast (Los Angeles and San Francisco). Live bird markets all over the world are an important part of daily commerce and represent both a mixing pot of avian and mammalian disease agents and a steady stream of human traffic. The transmission of avian influenza to humans in Hong Kong in 1997 (Mounts et al., 1999; Shortridge et al., 2000; Subbarao et al., 1998) and in other parts of Asia (Webster, 2004) has raised the profile of live bird markets. Although surveillance has been increased, disease control measures have been established in only a few locations (Mullaney, 2003), primarily because they have been difficult to conceive and implement. Today, in the United States and all over the world, these markets remain a key location where the public is in direct contact with poultry that are sometimes actively shedding AI virus.

Perhaps the most intensive contact between poultry and people in the United States occurs among those individuals who own poultry for hobby purposes or keep them as a continuing source of eggs or fresh meat. These individuals come from a wide variety of cultural backgrounds and socioeconomic strata. However, these individuals—including cockfighters, 4H participants, poultry fanciers, and backyard flock owners—have one thing in common: few of them take their birds to veterinarians. This is partially due to a lack of interest in poultry on the part of most practicing veterinarians and partly because these owners do not want to spend money for veterinary care. Because they rarely see veterinarians, AI virus infections in these types of flocks usually go undetected and unreported. This lack of care combined with the level of contact between flock owners and hobby or backyard chickens make these human and poultry interactions some of the most important to public health.

So, while the general public is largely limited in its exposure to poultry by intensive farming and biosecurity practices, there are a number of exceptions through which humans may be intensively exposed to poultry. These scenarios are where disease prevention in poultry flocks is limited by a lack of contact with veterinarians and a lack of poultry husbandry knowledge that public health may be critically at risk. Unfortunately, many of the people most intensively exposed to these small populations of poultry are also underserved by human health professionals.

In California, the outbreak of H6N2 avian influenza in densely populated poultry regions resulted in the exposure of many small flocks to AI virus. How many were infected or their types are not known. However, we suspect that some of these noncommercial flocks are now persistently infected manmade reservoirs for the virus. These types of reservoirs have been implicated in the spread of disease to commercial flocks, but their roles in public health have been largely invisible.


The fact that California's low-pathogenicity strain of avian influenza virus was of the H6N2 type did not prevent it from spreading to many commercial poultry flocks or from causing disease and production losses in infected chickens and turkeys. In addition, the fact that this virus was not of the H5 or H7 types does not limit its potential to donate genetic material to potential pandemic strains. The interaction of animal agriculture and the public is complex and dynamic, and we do not fully understand the risks associated with the various types of contacts between humans and birds. We do not know where or how the next pandemic influenza virus will arise, but that lack of knowledge should not limit the surveillance we conduct in birds or in the public.

Low-pathogenicity strains of AI virus are the most prevalent strains among all species of birds, including commercial poultry. Non-H5 and -H7 low-pathogenicity AI viruses have contributed genetic material to the highly pathogenic viruses currently circulating in Asia (Chin et al., 2002), and one has infected humans (Lin et al., 2000). Our knowledge of where the next pandemic virus will arise is too premature to eliminate as irrelevant the non-H5 or -H7 avian influenza strains.


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Diseases to be urgently notified by Member Countries.

Copyright © 2005, National Academy of Sciences.
Bookshelf ID: NBK22152


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