4
Strategies for Controlling Avian Influenza in Birds and Mammals

OVERVIEW

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



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The Threat of Pandemic Influenza: Are We Ready? - Workshop Summary 4 Strategies for Controlling Avian Influenza in Birds and Mammals OVERVIEW 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

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The Threat of Pandemic Influenza: Are We Ready? - Workshop Summary 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. STANDARDS AND ACTIVITIES OF THE OIE RELATED TO AVIAN INFLUENZA Dewan Sibartie Scientific and Technical Department World Organisation for Animal Health (OIE) Introduction 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 informa-

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

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The Threat of Pandemic Influenza: Are We Ready? - Workshop Summary 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 Laborato- 1   Diseases to be urgently notified by Member Countries.

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

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

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

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

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

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

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The Threat of Pandemic Influenza: Are We Ready? - Workshop Summary 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 (http://www.oie.int) 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.

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The Threat of Pandemic Influenza: Are We Ready? - Workshop Summary cant 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. LOW-PATHOGENICITY AVIAN INFLUENZA OUTBREAKS IN COMMERCIAL POULTRY IN CALIFORNIA 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

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

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The Threat of Pandemic Influenza: Are We Ready? - Workshop Summary 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 Minimize the movement of birds Use on-site composting or cremation if possible to dispose of carcasses after euthanasia Move birds safely, if they must be moved Avoid driving near other poultry facilities Test flocks 2 weeks prior to movement Birds with clinical disease should never be moved Clean, disinfected trucks should be used Principles of biosecurity should be closely followed Move infected birds only to slaughter Actively shedding birds should not be moved to another facility Previously infected birds are strongly discouraged from movement except to slaughter Movement of manure Manure trucks must be tarped before they leave any facility They must follow routes that avoid contact with other poultry traffic

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The Threat of Pandemic Influenza: Are We Ready? - Workshop Summary Multiple pickups from different farms on the same day are not allowed Manure should be pushed to the edge of the property for pickup Traffic patterns should be established that avoid interaction between manure trucks and other farm traffic Scheduling should be done to avoid clean traffic Manure should not be spread or stored close to any other poultry Marketing of eggs Dedicated racks and flats will be used for each ranch Racks and flats from different ranches will not be commingled Flats will be washed and disinfected at the processing plant Rack washing at the processing plant is strongly encouraged Feed mills and feed delivery Feed trucks should be cleaned and disinfected at the feed mill They should be kept away from “clean” areas of the production facility They should be cleaned and disinfected again when they enter a facility Drivers should be either kept away from “clean” areas or provided with protective clothing 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 A representative of the poultry company will monitor all work performed by crews to ensure that the following rules are observed: Protective clothing and footwear provided by the ranch must be worn Hand washing is required before handling birds Crew vehicles should be cleaned and disinfected before they enter a facility or, preferably, they should be left off site Mortality disposal Onsite cremation or composting are the preferred methods of mortality disposal Use renderers safely, if they must be used Tarp trucks Put mortality pickup at the edge of the property Coordinate the routing of the truck to avoid “clean” farm traffic

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The Threat of Pandemic Influenza: Are We Ready? - Workshop Summary Shared employees Employees should not be shared by poultry companies Employees are required to wear clean clothes to work Employees are required to disinfect their footwear before entering production facilities Clean rooms for changing and clean clothes should be provided for employees Shower facilities are optimal, but are not required Shared equipment Equipment should not be shared between poultry facilities If it is shared, it should be cleaned and disinfected at both ends Physical proximity Communicate with neighbors to avoid behaviors that endanger each other’s flocks Control vectors (rodents and insects) as much as possible Communication of disease status between neighbors is required Common vendors (propane, utility, supplies, etc.) Keep unnecessary visitors off the farm Visitors should wear protective clothing to enter the facility A consistent visitor policy should be established for all premises 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: When there is little risk of infection, flocks will be tested at slaughter During times when there is a risk of infection: 20 birds will be tested for AI by AGID monthly Flocks must be checked daily for: Decreases in egg production Increased mortality 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

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The Threat of Pandemic Influenza: Are We Ready? - Workshop Summary et al., 1986). The California plan required the following to Control the virus—making a responsible response to AI virus infection: Negative flocks (never infected with avian influenza virus) have no restrictions on movement Virus-negative flocks (previously positive but no longer shedding virus): Move to slaughter Pullets (young hens) may be moved to a positive lay ranch Suspect flocks Get a diagnosis as soon as possible Contact your veterinarian, and/or Submit birds to the diagnostic laboratory Notify your neighbors Self-quarantine Positive flocks (currently infected and shedding avian influenza virus) Notify neighboring poultry farms Self-quarantine Do not move birds until the flock is no longer shedding virus Coordinate movement of the flock to minimize risk Document route and time of travel and let other producers know or Euthanize and dispose of the flock on site (composting or cremation) 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. Clean and disinfect the farm Leave sufficient downtime before repopulation (at least 2 weeks)

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The Threat of Pandemic Influenza: Are We Ready? - Workshop Summary Use of vaccine in flocks at risk of infection 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

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

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The Threat of Pandemic Influenza: Are We Ready? - Workshop Summary 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. REFERENCES Bulaga LL, Garber L, Senne D, Myers TJ, Good R, Wainwright S, Trock S, Suarez DL. 2003. Epidemiologic and surveillance studies on avian influenza in live-bird markets in New York and New Jersey, 2001. Avian Diseases 47(Suppl):996–1001. Chin PS, Hoffmann E, Webby R, Webster RG, Guan Y, Peiris M, Shortridge KF. 2002. Molecular evolution of H6 influenza viruses from poultry in Southeastern China: Prevalence of H6N1 influenza viruses possessing seven A/Hong Kong/156/97 (H5N1)-like genes in poultry. J Virol 76:507–516. Dybing JK, Schultz Cherry S, Swayne DE, Suarez DL, Perdue ML. 2000. Distinct pathogenesis of Hong Kong-origin H5N1 viruses in mice as compared to other highly pathogenic H5 avian influenza viruses. J Virol 74:1443–1450. Easterday BC, Hinshaw VS, Halvorson DA. 1997. Influenza. In: Calnek BW, Barnes HJ, Beard CW, McDougald LR, Saif YM, eds. Diseases of Poultry. 10th ed. Ames, IA: Iowa State University Press. Pp. 583–605. Ghazikhanian GY, Kelly BJ, Dungan WM, Bankowski RA, Reynolds B, Wichman RW. 1981 (April 22–24). Avian Influenza Outbreaks in Turkey Breeder Flocks from 1979 to 1981. Presented at the First International Symposium on Avian Influenza, Beltsville, MD. Halvorson DA, Kelleher CJ, Senne DA. 1985. Epizootiology of avian influenza: Effect of season on incidence in sentinel ducks and domestic turkeys in Minnesota. Applied Environ Microbiol 49:914–919. Halvorson DA, Karunakaran D, Abraham AS, Newman JA, Sivanandan V. 1986. Efficacy of vaccine in the control of avian influenza. In: Proceedings of the Second International Symposium on Avian Influenza. Athens, GA: United States Animal Health Association. Pp. 264–270. Henzler DJ, Kradel DC, Davison S, Ziegler AF, Singletary D, DeBok P, Castro AE, Lu H, Eckroade R, Swayne D, Lagoda W, Schmucker B, Nesselrodt A. 2003. Epidemiology, production losses, and control measures associated with an outbreak of avian influenza subtype H7N2 in Pennsylvania (1996–98). Avian Diseases 47:1022–1036.

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