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Avian influenza is not a new disease, but the emergence of high pathogenicity avian influenza (HPAI) viruses of the A/Goose/Guangdong/1/96 lineage (Gs/GD) has necessitated fundamental changes to prevention and control strategies for this disease. No longer just an avian disease, avian influenza is capable of causing severe disease in humans and is considered a potential human pandemic threat requiring One Health approaches. In addition, Gs/GD HPAI viruses have developed the capacity to be carried across and between continents by migratory birds. Given the persistence of the current A(H5N1) clade 2.3.4.4b viruses in wild birds, enhanced measures to prevent and control infection will be needed. In most countries, infection in poultry can be eliminated, although questions will remain about the sustainability of repeated stamping out. Systematic preventive vaccination should be seriously considered as a method for reducing the number of outbreaks. HPAI will not be eliminated from countries where Gs/GD viruses remain enzootic until major changes are made to the way that poultry are reared and sold, vaccination is improved and other factors that inhibit reporting and response are overcome. Currently, focus lies on Gs/GD HPAI, yet control of low pathogenicity avian influenza viruses also requires attention, including the development of vaccines that are appropriately matched to circulating strains of virus.

H5Nx A/Goose/Guangdong/1/96 Eurasian lineage high pathogenicity avian influenza (HPAI) viruses have been the main HPAI strains detected globally since 2005. These have spread around the world, causing a panzootic that has spanned six continents, with continual threat to not only wild and captive birds and poultry, but also wild, captive and domestic mammals and humans. The viruses' ecology and epidemiology - especially the 2.3.4.4b clade - have changed, with over 489 species of birds infected and spreading the virus over migratory routes. This results in the death of many birds, including endangered species, and serves as a source of transmission to poultry and mammals. Improved surveillance and sharing of HPAI virus sequences, metadata and viruses across the veterinary, public health, wildlife and environment sectors are needed to elucidate the population dynamics of the infections, which is crucial to addressing this complex One Health issue. The development of appropriate mitigation strategies or changes in husbandry, production and selling practices can reduce the risk of viruses being introduced into farms, as well as their amplification and viral evolution, and any spill-back to wild birds. Approaches to prevention and control of HPAI in countries where these 2.3.4.4b viruses remain entrenched in poultry, or places at risk of virus introduction via wild bird populations, involve measures to reduce the effects of the disease in poultry (including enhanced farm bio-security, vaccination, zoning and compartmentalisation). Their uptake reflects the difficulties encountered in relying solely on biosecurity for disease prevention and on stamping out alone for virus control and elimination. The World Organisation for Animal Health's Terrestrial Animal Health Code allows use of vaccination of poultry under specific conditions and without negatively impacting HPAI-free status if appropriate surveillance is conducted, thus supporting safe trade in poultry and poultry products. Nevertheless, concerns regarding loss of valuable export markets still interfere with greater utilisation of vaccination.

This literature review provides an overview of use of environmental samples (ES) such as faeces, water, air, mud and swabs of surfaces in avian influenza (AI) surveillance programs, focussing on effectiveness, advantages and gaps in knowledge. ES have been used effectively for AI surveillance since the 1970s. Results from ES have enhanced understanding of the biology of AI viruses in wild birds and in markets, of links between human and avian influenza, provided early warning of viral incursions, allowed assessment of effectiveness of control and preventive measures, and assisted epidemiological studies in outbreaks, both avian and human. Variation exists in the methods and protocols used, and no internationally recognized guidelines exist on the use of ES and data management. Few studies have performed direct comparisons of ES versus live bird samples (LBS). Results reported so far demonstrate reliance on ES will not be sufficient to detect virus in all cases when it is present, especially when the prevalence of infection/contamination is low. Multiple sample types should be collected. In live bird markets, ES from processing/selling areas are more likely to test positive than samples from bird holding areas. When compared to LBS, ES is considered a cost-effective, simple, rapid, flexible, convenient and acceptable way of achieving surveillance objectives. As a non-invasive technique, it can minimize effects on animal welfare and trade in markets and reduce impacts on wild bird communities. Some limitations of environmental sampling methods have been identified, such as the loss of species-specific or information on the source of virus, and taxonomic-level analyses, unless additional methods are applied. Some studies employing ES have not provided detailed methods. In others, where ES and LBS are collected from the same site, positive results have not been assigned to specific sample types. These gaps should be remedied in future studies., (© 2020 Food and Agriculture Organization of the United Nations. Transboundary and Emerging Diseases published by Blackwell Verlag GmbH.)

The occurrence of avian influenza A(H5N1) in Hong Kong in 1997 led to the development of a "One-Health" approach to deal with emerging infectious diseases that has been applied to other emergent diseases such as SARS and the pandemic H1N1 2009. Evaluation of poultry marketing and production systems and investigations at the animal-human interface, led to defining the routes of human exposure to avian influenza and factors that allowed virus to multiply and persist. Active and systematic surveillance of apparently healthy as well as diseased poultry and wild birds provided evidence of ongoing virus evolution in the wider region. Epidemiological studies, supplemented with molecular epidemiology, helped to elucidate the role of the poultry marketing system and live poultry markets in the persistence of avian influenza viruses and provided evidence for the impact of interventions designed to interrupt virus transmission. Enhanced bio-security, active surveillance together with targeted and evidence-based interventions in the poultry production, and marketing system together with poultry vaccination has prevented further human H5N1 disease and minimized outbreaks of poultry disease in Hong Kong. Similar strategies have led to the understanding of the emergence of SARS and provided options for preventing the re-emergence of this disease. Surveillance of influenza in swine has provided insights into the emergence of the 2009 pandemic, to the reverse zoonosis of the pandemic virus from humans to swine and to the emergence of novel reassortant viruses within swine. "One Health" strategies are not "cost-free" and require sensitive implementation to optimize food-safety and food security, while safeguarding the economics of animal husbandry and the environment and remaining sensitive to cultural practices.

Three broad factors, occurring concurrently, prevent elimination of highly pathogenic avian influenza caused by viruses of the H5N1 subtype (H5N1 HPAI) in countries and subregions where infection has remained endemic. These factors are the nature of the poultry sector, the quality of veterinary and animal production services (both public and private) serving the poultry industry, and the extent and level of commitment at all levels to virus elimination. Most of these countries have developed and adopted programs for progressive control of H5N1 HPAI, focused on the local factors hindering elimination of the viruses. Based on the rate of implementation of these measures over the last 5 to 7 yr (during which time there has been unprecedented financial and technical support from the international donor community), it is not expected that global eradication of H5N1 HPAI viruses can be achieved within the next 10 yr. If the "classical" approach to control, based around early case detection and culling, were adopted in a zone containing millions of free-running ducks, the work load required to complete even the first round of testing would exceed existing capacity. There would be no guarantees of sustained success locally, especially if the viruses are not eradicated regionally.

Vaccination has been used extensively for the control and prevention of highly pathogenic avian influenza (HPAI) caused by viruses of the H5N1 subtype in endemically infected countries. The Food and Agriculture Organization views vaccination as a legitimate aid in the control and prevention of infection and disease caused by HPAI viruses but does not see it as a panacea. Vaccination should be used as just one in a number of measures used together to reduce the effect and risk of infection. It will be required for a considerable time in endemically infected countries. The methods used in Vietnam in implementing blanket vaccination against H5N1 HPAI viruses demonstrate the steps that should be considered when introducing vaccination. So far, it has not been possible to determine the precise effect of vaccination in endemically infected countries because it has been used in combination with other measures. Well managed vaccination campaigns will reduce the incidence of infection in poultry and therefore reduce the risk to humans from these viruses. Vaccination was implemented to protect both poultry and humans, with a major goal being to reduce the risk of emergence of a human influenza pandemic virus. Economic analysis of vaccination should focus on cost-effectiveness of proposed strategies. Ex-ante and ex-post evaluation of vaccination campaigns should take into account the benefits generated in the poultry sector and for human health.

Numerous lessons have been learned so far in controlling H5N1 avian influenza in Asia. Early detection of incursions of virus prevented establishment of the disease in several countries, notably Japan, South Korea, and Malaysia. In countries where detection of early cases was delayed, infection is endemic and has been for three or more years. Control measures implemented in these countries need to reflect this finding. Vaccination will continue to be one of the key measures used in these endemically infected countries. Used alone, vaccination will not result in elimination of H5N1 viruses from a country, but, if used correctly, it will markedly reduce the prevalence of and susceptibility to infection. Vaccination has already played a valuable role in reducing the adverse effects of H5N1 viruses. Mass culling also reduces the level of infection in infected areas. However, the long-term benefits are limited in endemically infected countries owing to the high probability of reinfection on restocking unless other measures are used in parallel. Full epidemiological studies have not been conducted in many infected countries. Nevertheless, it is recognized that the number of clinical cases does not truly reflect the levels of infection. Domestic ducks and large live poultry markets have played a key role in the persistence of infection, because they can be infected silently. In tackling this disease, countries should adopt integrated control programs using the combination of measures best suited to the local environment. All surveillance data should be shared, both positive and negative, and should include information on cases of infection and disease. Socioeconomic and ecological implications of all control measures should be assessed before implementation, especially the impact on the rural poor.

A comprehensive approach to highly pathogenic avian influenza (HPAI) is crucial for identifying all the factors that contribute to its emergence, spread and persistence. Epidemiological understanding makes it possible to predict the evolution of the virus and to prevent and control the socioeconomic, environmental, institutional and policy consequences. At FAO, risk assessment and intelligence with regard to HPAI are based on lessons learnt from assisting countries to design strategies and on implementation of technical assistance programmes, which reveal important elements, such as the roles of ducks, live-bird markets and trade. Wild birds were found to contribute, by transporting the H5N1 virus over long distances. The contributions of different poultry farming systems and market chains in the epidemiology of HPAI are well recognized; however, the respective roles of smallholder systems and commercial farms are unclear. FAO considers that smallholders will continue to be an important factor and should be taken into account in control and prevention programmes. Changes in poultry farming are essentially driven by the private sector and market forces and could have negative consequences on the livelihoods of smallholders and on ecologically balanced production systems and agricultural biodiversity. Biosecurity can, however, be improved at the level of farms and markets. Institutional factors, such as the capacity of animal health systems to deliver control programmes, are also important, requiring strengthening and innovation in risk analysis and management.

Highly pathogenic H5N1 avian influenza viruses have been circulating in Asia for over ten years, providing considerable experience on which to base appropriate long-term strategies for their control. Experience in Hong Kong SAR demonstrates that existing production and marketing practices should be changed and a range of parallel measures used. It also shows the extent of surveillance required to ensure continuing freedom from infection. Certain high-risk practices should be changed or otherwise overcome in order to control and prevent disease, including intensive rearing of large numbers of poultry in premises without biosecurity commensurate with the level of risk for exposure; complex market chains involving many smallholders selling poultry through large numbers of transporters and middlemen in poorly regulated live poultry markets; and rearing of large numbers of ducks outdoors. These high-risk practices are compounded by weak veterinary services and poor reporting systems. In many parts of Asia, these methods of rearing and marketing are an integral way of life, support the poorest members of the community or cannot be changed quickly without severe socioeconomic consequences. The gains made so far will be ephemeral unless there is a shift from an emergency focus to one of consolidation in which these high-risk practices are identified and sustainable measures implemented to minimize the risks they pose, taking account of the socioeconomic effects of interventions. Vaccination will play a key role, as it currently does in China and Viet Nam.

Highly pathogenic avian influenza (HPAI) has been recognized as a serious viral disease of poultry since 1878. The number of outbreaks of this disease globally has increased in the past 10 years culminating in 2004 with the unprecedented outbreak of H5N1 HPAI involving nine countries in East and South East Asia. Apart from the geographical extent of this outbreak and apparent rapid spread, this epidemic has a number of unique features, among which is the carriage of highly pathogenic AI viruses by asymptomatic domestic waterfowl. When this disease first emerged it was recognized almost simultaneously in a number of countries for the first time. This created considerable concern among both veterinary and public health authorities especially as the virus was also shown to cause fatal disease in humans. This article brings together a range of information on H5N1 HPAI viruses in Asia that were collected by FAO during the past year through field projects and explores possible reasons for the emergence of the disease in late 2003 and early 2004. Key epidemiological features of the disease in different Asian countries are described in an attempt to look for, and where possible, explain similarities and differences. This includes assessment of factors that could have contributed to the spread of the disease. Molecular aspects of the viruses are examined to assess relationships between isolates from different locations and times so as to gain insights into the origins of viruses in various countries. It is apparent that the coincidence and grouping of the reports declaring the outbreaks of HPAI did not truly reflect the time course of disease emergence, which was widespread well before the outbreak. The factors that could have led to a change from infection to emergence of widespread disease in 2003-2004 are discussed. There are still some questions that remain unanswered regarding the origins of the 2004 outbreak. This article does not provide answers to all of these, but brings together what is currently known about these outbreaks and the viruses that have caused them.

Outbreaks of H5N1 highly pathogenic avian influenza (HPAI) that occurred in Hong Kong up until February/March 2002 were controlled by stamping out. With endemic presence of the virus in the region and large daily importation of poultry to Hong Kong, the Administration considered that further risk management measures, in addition to improved biosecurity and enhanced surveillance, were necessary to prevent outbreaks. Vaccination using a killed H5N2 vaccine was evaluated over a 12-month period in the district with the last HPAI cases in the early 2002 outbreak. The vaccination trial showed that farmer-administered killed H5N2 vaccine produced suitable flock antibody responses; vaccinated birds were protected against H5N1 HPAI virus challenge and excreted significantly less H5N1 virus; and vaccination was able to control virus excretion in flocks during field outbreaks. Universal vaccination of local chicken farms was introduced in June 2003 and by the end of 2003 all chickens entering the live poultry markets in Hong Kong were vaccinated by killed H5N2 vaccine. In addition to vaccination, an enhanced biosecurity programme on farms and in live poultry markets and a comprehensive surveillance programme in poultry, wild birds, recreation park birds and pet birds were in place. Vaccination use and performance is closely monitored. This programme was successful in protecting local farms and live poultry markets from H5N1 outbreaks during the regional H5N1 outbreaks in 2004.

Highly pathogenic avian influenza (HPAI) has been recognised as a serious viral disease of poultry since 1878. The number of recorded outbreaks of HPAI has increased globally in the past 10 years culminating in 2004 with the unprecedented outbreaks of H5N1 HPAI involving at least nine countries in East and South-East Asia. Apart from the geographical extent of these outbreaks and apparent rapid spread, this epidemic has a number of unique features, among which is the role that asymptomatic domestic waterfowl and more particularly free-ranging ducks play in the transmission of highly pathogenic H5N1. Field epidemiological studies have been conducted by the Food and Agriculture Organization and several collaborative centres to explore the factors that could have led to a change from infection to the emergence of widespread disease in 2003-2004 and 2005. Domestic waterfowl, specific farming practices and agro-ecological environments have been identified to play a key role in the occurrence, maintenance and spread of HPAI. Although there are some questions that remain unanswered regarding the origins of the 2004 outbreaks, the current understanding of the ecology and epidemiology of the disease should now lead to the development of adapted targeted surveillance studies and control strategies.

Outbreaks of highly pathogenic avian influenza caused by H5N1 viruses were reported almost simultaneously in eight neighbouring Asian countries between December 2003 and January 2004, with a ninth reporting in August 2004, suggesting that the viruses had spread recently and rapidly. However, they had been detected widely in the region in domestic waterfowl and terrestrial poultry for several years before this, and the absence of widespread disease in the region before 2003, apart from localised outbreaks in the Hong Kong Special Autonomous Region (SAR), is perplexing. Possible explanations include limited virus excretion by domestic waterfowl infected with H5N1, the confusion of avian influenza with other serious endemic diseases, the unsanctioned use of vaccines, and the under-reporting of disease as a result of limited surveillance. There is some evidence that the excretion of the viruses by domestic ducks had increased by early 2004, and there is circumstantial evidence that they can be transmitted by wild birds. The migratory birds from which viruses have been isolated were usually sick or dead, suggesting that they would have had limited potential for carrying the viruses over long distances unless subclinical infections were prevalent. However, there is strong circumstantial evidence that wild birds can become infected from domestic poultry and potentially can exchange viruses when they share the same environment. Nevertheless, there is little reason to believe that wild birds have played a more significant role in spreading disease than trade through live bird markets and movement of domestic waterfowl. Asian H5N1 viruses were first detected in domestic geese in southern China in 1996. By 2000, their host range had extended to domestic ducks, which played a key role in the genesis of the 2003/04 outbreaks. The epidemic was not due to the introduction and spread of a single virus but was caused by multiple viruses which were genotypically linked to the Goose/GD/96 lineage via the haemagglutinin gene. The H5N1 viruses isolated from China, including the Hong Kong SAR, between 1999 and 2004 had a range of genotypes and considerable variability within genotypes. The rising incidence and widespread reporting of disease in 2003/04 can probably be attributed to the increasing spread of the viruses from existing reservoirs of infection in domestic waterfowl and live bird markets leading to greater environmental contamination. When countries in the region started to report disease in December 2003, others were alerted to the risk and disease surveillance and reporting improved. The H5N1 viruses have reportedly been eliminated from three of the nine countries that reported disease in 2003/04, but they could be extremely difficult to eradicate from the remaining countries, owing to the existence of populations and, possibly, production and marketing sectors, in which apparently normal birds harbour the viruses.

An outbreak of highly pathogenic avian influenza caused by multiple genotypes of H5N1 virus occurred in Hong Kong, commencing in January 2002. Infection in local chicken farms was preceded by the detection of virus in multiple retail markets and the main poultry wholesale market. The first case of this disease on a local farm was detected on February 1, 2002. By February 9, 2002, 15 farms were infected, and by late March a total of 22 infected farms had been identified. Three main clusters of infected farms were seen, suggesting multiple incursions of virus, and subsequent limited lateral spread to neighboring firms. Control of this disease has been effected through a combination of quarantine, tightening of biosecurity measures, and depopulation of infected and contact farms. About 950,000 birds have been destroyed. Vaccination using a killed H5 vaccine was introduced in April 2002 to farms in one zone where infection has persisted. None of the viruses isolated contained the internal genes found in the 1997 H5N1 virus.

In 1997, a high-pathogenicity H5N1 avian influenza virus caused serious disease in both man and poultry in Hong Kong, China. Eighteen human cases of disease were recorded, six of which were fatal. This unique virus was eliminated through total depopulation of all poultry markets and chicken farms in December 1997. Other outbreaks of high-pathogenicity avian influenza (HPAI) caused by H5N1 viruses occurred in poultry in 2001 and 2002. These H5N1 viruses isolated had different internal gene constellations to those isolated in 1997. No new cases of infection or disease in man due to these or other H5N1 viruses have been reported. This paper provides an overview and chronology of the events in Hong Kong relating to avian influenza, covering the period from March 1997 to March 2002.

Retail live poultry markets (LPMs) may act as a reservoir of avian influenza viruses (AIV). In this study we test the hypothesis that a rest day in the LPMs where the stalls are completely emptied of poultry, cleansed, and restocked will reduce the isolation rates of avian influenza viruses. The isolation rate of H9N2 subtype viruses from chicken was significantly lower after the rest day than prior to it, indicating its impact in reducing transmission. In contrast, Newcastle disease virus (NDV) isolation rates appear unaffected by this intervention, possibly reflecting differences in herd immunity or virus transmission dynamics.

The transmission of avian H5N1 influenza viruses to 18 humans in Hong Kong in 1997 with six deaths established that avian influenza viruses can transmit to and cause lethal infection in humans. This report characterizes the antigenic and biological properties of the H5N1 influenza viruses isolated from chickens, ducks, and geese from farms and poultry markets in Hong Kong during 1997 and compares them with those of virus isolated from the index human case. Each of the H5N1 viruses from Hong Kong poultry markets that were tested were lethal in chickens, possessed polybasic amino acids at the carboxy-terminus of HA1, and by definition were highly pathogenic in poultry. The available nonpathogenic H5 influenza viruses and the pathogenic H5N1 virus from Hong Kong were analyzed with monoclonal antibodies prepared to A/chicken/Pennsylvania/1370/83 (H5N2). The analysis revealed limited antigenic drift in 15 years and established that monoclonal antibodies are useful reagents for identification and antigenic analysis of avian strains that may transmit to humans in the future. One of the monoclonal antibodies permitted separation of the H5N1 influenza viruses from poultry into two groups that correlated with the presence or absence of a carbohydrate at residue 158 adjacent to the receptor binding site on HA. The H5N1 viruses examined replicated in geese, pigs, rats, and mice, but to only a very limited extent in ducks. It is noteworthy that all infected geese shed virus and that the H5N1 viruses caused disease signs and death in a portion (3 of 16) of the geese, with evidence of systemic spread to the brain. The tropism for geese is unusual and may provide insight into the origin of these viruses. In mice, the H5N1 virus caused lethal pneumonia and spread systemically to the brain. Mice would thus provide an ideal model system for studying immune responses and pathogenesis. Transmission experiments in chickens revealed that the H5N1 viruses are spread by fecal-oral transmission rather than by aerosol, and that the viruses are inactivated by drying of feces at ambient temperature. However, infectivity is maintained for at least 4 days in wet feces at 25 degreesC. There were differences in the morphology of the H5N1 viruses isolated from birds and humans. The perpetuation of H5N1 influenza viruses in the poultry markets in Hong Kong and the transmission of these viruses to humans emphasize the importance of these markets in the epidemiology of influenza. The poultry markets are of critical importance in the perpetuation and transmission of influenza viruses to other avian species and to mammals, including humans., (Copyright 1998 Academic Press.)