Dennis A. Senne
U.S. Department of Agriculture, Animal and Plant Health Inspection Service,
Veterinary Services, National Veterinary Services Laboratories,
Ames, Iowa
U.S.A.
Introduction
Since 2002 there have been reported several outbreaks of highly pathogenic avian influenza (HPAI) throughout the world, caused by H7 subtype and by H5 subtype viruses. Each of the outbreaks were unique, but in terms of size and impact, all pale in comparison to the outbreak of HPAI H5N1 that has been ongoing since 2003 in Asia and more recently in Eastern Europe. The Asian H5N1 outbreak has involved many countries (more than 15) and caused death or destruction of more than 150 million poultry. In addition, the virus has infected more than 150 people, killing at least 80 (9). These events have elevated the public awareness and interest in AI to unprecedented levels, mostly driven by intense media coverage on possible emergence of an influenza pandemic virus. This presentation will provide a general overview of the HPAI H5N1 outbreak in Asia and Eastern Europe and measures taken by the USDA and other governmental agencies to prevent the introduction of the disease into the United States.
In the beginning
Although most of the attention surrounding the outbreak of HPAI H5N1 in Asia has been focused on events that have occurred since late 2003, the origin of the problem can be traced back to 1996 when a HPAI H5N1 virus was first isolated from clinically affected domestic geese in Guangdong Province, China.
The H5 gene from the goose/Guangdong/96 H5N1 virus was later shown to be a component of the precursor virus for the 1997 outbreak of HPAI H5N1 in the Special Administrative Region (SAR) in Hong Kong that infected chicken in three farms and 18 humans; six of the human infections were fatal (1). The human infections were linked to contact with infected poultry in the live poultry markets in Hong Kong. It was the event in Hong Kong in 1997 that spawned the term “bird flu” that now seems to be used frequently, albeit incorrectly, to describe most all AI infections in poultry.
Between 1999 and 2003 several additional events involving HPAI H5N1 in poultry, the live poultry markets (LPMs), wild birds, and humans occurred in Southern China and/or Hong Kong, suggesting that the HPAI virus continued to circulate in the region before the outbreak in 2003. However, only the events in Hong Kong were public knowledge at the time.
The outbreak involving HPAI H5N1 first came to the world’s attention when eight Asian countries (Korea, Vietnam, Japan, Thailand, Cambodia, Laos, Indonesia, and China) reported the presence of the HPAI H5N1 virus in poultry between mid December 2003 and the first week in February 2004. Most of the infections were detected in backyard poultry and domestic ducks. Although relatively few large commercial facilities were infected with the virus, many of the commercial farms in close proximity to the infected backyard flocks were destroyed as a precautionary measure to prevent spread of disease.
In August 2004, the disease was reported in Malaysia. By mid 2005 the disease had spread into Russia (Siberia), Kazakhstan, and Mongolia, and then crossed the Ural Mountains in October into Romania, Turkey and Croatia where infections were primarily limited to backyard poultry and wild birds.
Epidemiology of the disease
The lack of knowledge in the epidemiology of the H5N1 outbreak in Asia was likely a major contributing factor in spread of the disease throughout the region. Early theories on methods of spread focused mainly on migratory birds. Since little could be done to prevent the spread by wild birds, limited actions were taken to enhance biosecurity in backyard flocks during the early stages of the outbreak to prevent spread among backyard poultry flocks. In addition to the wild bird theory, there was also evidence to suggest that the virus may have been disseminated through local and international markets by the movement of poultry and/or poultry products, especially domestic ducks and/or duck meat. Evidence for spread of the virus through movement of poultry meat is supported by the isolation of HPAI H5N1 virus from frozen duck meat exported from China to Korea in 2001 and to Japan in early 2003 (7,8).
The movement of live poultry from backyard flocks to local live poultry markets most certainly contributed to local spread of disease during the early stages of the outbreak and could have been the source of some of the human infections. As the outbreak progressed, it was found that domestic ducks remained asymptomatic even when infected with the HPAI H5N1 virus, and shed large quantities of virus in faeces (10).
China raises about 70% of the world’s domestic ducks, of which the majority are raised out-of-doors in open rice fields. This practice has great potential for H5N1 virus contamination of the environment, thus increasing the chances for further spread of the disease to susceptible backyard poultry, wild birds and humans. Spread of disease could also have been through activities involving game fowl (fighting chickens), an activity deeply engrained in many Asian cultures. The unrestricted movement of these birds would also have great potential to spread the virus over long distances. However, in spite of the evidence incriminating movement of poultry, contaminated meat and/or game fowl in the spread of the disease, there is increasing evidence to support the theory that H5N1 virus, in some situations, was most likely spread by wild migratory birds.
In early April 2005, thousands of wild aquatic birds were found dead in and around Lake Qinghai in Qinghai Province, China. The HPAI H5N1 virus was isolated from several species of birds, but since there was infected poultry in the region, conclusive evidence incriminating wild birds was lacking. In July and August 2005, there were numerous reports of the isolation of HPAI H5N1 from backyard poultry and wild birds in Russia (Siberia), Kazakhstan and Mongolia, where the most likely medium of introduction is suspected to be wild birds. Since August 2005, the disease has spread North and Westward across the Ural Mountains to Romania, Turkey and Croatia. The Ural Mountains provide a natural division between Eastern Europe and Asia. As concerns about the movement of the disease into Eastern Europe and the continued spread of the virus via migratory birds, many countries in the Middle East, Africa and the Indian subcontinent are increasing surveillance for H5N1 in migratory birds and poultry. More detailed summaries of the outbreaks in the various countries are available (3, 4, 5, 6, 7).
Genetic diversity among HPAI H5N1 viruses
By genetic analysis, the Asian H5N1 viruses isolated since 1996 have shown considerable genetic diversity, suggesting evolution of the virus over time, perhaps in different ecosystems. For example, the lineage of HPAI H5N1 virus that first appeared in Hong Kong in early 1997 has not been isolated since the LPMs were depopulated in December of that year.
Most viruses isolated since 2003 fall into one of two major genetic clades, designated clade 1 and clade 2 (11). The majority of human isolates from Thailand, Vietnam and Cambodia are in clade 1. Viruses that comprise clade 2 are the human isolates from Indonesia as well as isolates from poultry and wild birds in China, Russia, Kazakhstan, Mongolia and Eastern Europe. The HPAI H5N1 viruses found in wild bird species in the Qinghai Lake, China are closely related to those from wild birds in Russia, Kazakhstan, Mongolia and Eastern Europe, suggesting wild birds as playing a role in the wide dissemination of the virus. However, it is not yet clear in all cases whether the wild birds or poultry are the original source of the virus in new geographical regions.
Recent spread and concerns
Since November 2005, as cooler temperatures prevail, several Asian countries have reported new outbreaks of HPAI H5N1. China, for example, has reported new outbreaks in 8 of the 30 provinces during November and one in December. Also, China reported the first cases of H5N1 in humans (9 infections, 6 fatalities) in late 2005, and in January 2006, several new outbreaks of disease have been reported in Turkey, both in backyard poultry and in humans. Because of the increase in new cases in poultry and humans, China decided to vaccinate all 14 billion poultry and waterfowl that are produced annually in the country. Vietnam has similarly initiated a countrywide vaccination program for all poultry.
Surveillance for H5N1 is becoming a high priority in countries that share major migratory flyways with Asia and Eastern Europe where infected birds have been found, with the hope of detecting infections early and preventing the spread to domestic poultry. The progressive spread of HPAI H5N1 virus into new regions will require proactive intervention by the countries at risk.
It is important to note that wild birds dying from the infection with the H5N1 virus are most likely are indicators and not the ones responsible for dissemination of the virus, since sick birds (and most certainly dead birds) would not likely migrate. More research is needed to identify the species birds that can serve as carriers capable of spreading the virus over long distances.
What is the threat to the United States?
Since the Asian outbreak of HPAI H5N1 in 2003, the USDA and other Federal Agencies have increased mitigation efforts to prevent the accidental or intentional introduction of the disease into the United States. Such activities include targeted surveillance in domestic and migratory birds, increased boarder protection and vigilance, restriction on trade with affected countries, continued monitoring of imported pet (caged) birds, and outreach and educational programs aimed at being better prepared to detect and respond to outbreaks of disease.
Prospects for the future
The prospects for a quick resolution for the HPAI H5N1 problem in Asia is uncertain because of the number of infections in backyard poultry and especially domestic ducks, were infections can be asymptomatic. However, the international community, including the U.S. and specifically USDA, is reaching out with assistance to countries affected by AI in hopes of controlling the spread of the virus.
References
- Guan, Y., J. S. M. Peiris, L. L. M. Poon, K. C. Dyrting, T. M. Ellis, L. Sims, R. G. Webster and K. F. Shortridge. 2002. Reassortants of H5N1 influenza viruses recently isolated from aquatic poultry in Hong Kong SAR. Avian dis. 47(3):911-913.
- http://www.fao.org/ag/againfo/subjects/documents/ai/AVIbull033.pdf
- Foreign Agriculture Organization of the United Nations. 2005. http://www.fao.org/ag/againfo/subjects/documents/ai/AVIbull034.pdf
- Foreign Agriculture Organization of the United Nations. http://www.fao.org/ag/againfo/subjects/documents/ai/AVIbull035.pdf
- Foreign Agriculture Organization of the United Nations. http://www.fao.org/ag/againfo/subjects/documents/ai/AVIbull036.pdf
- Foreign Agriculture Organization of the United Nations. http://www.fao.org/ag/againfo/subjects/documents/ai/AVIbull037.pdf
- Mase, M., M. Eto, N. Tanimura, K Imai, K. Tsukamoto, T. Horimoto, Y. Kawaoka, and S. Yamaguchi. 2005. Isolation of a genotypically unique H5N1 influenza virus from duck meat imported into Japan from China. Virology 339(1):101-9.
- Tumpey, T. M., D. L. Suarez, L. E. L. Perkins, D. A. Senne, J. Lee, Y. J. Lee, I. P. Mo, H. W. Sung, and D. E. Swayne. 2002. Characterization of a highly pathogenic H5N1 avian influenza A virus isolated from duck meat. J. Virol. 76(12):6344-55.
- World Health Organization. 2005. http://www.who.int/csr/disease/avian_influenza/en/index.html
- World Health Organization. 2004. http://www.who.int/csr/disease/avian_influenza/labstudy_2004_10_29/en/
- World Health Organization Global Influenza Program Surveillance Network. 2005. Evolution of H5N1 avian influenza viruses in Asia. Emerg Infect Dis. Available from http://www.cdc.gov/ncidod/EID/vol11no10/05-0644.htm
From Proceedings of the “Midwest Poultry Federation Convention”, St. Paul, Minnesota, U.S.A.
