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Food Safety Research Information Office: A Focus on Avian Influenza (Bird Flu)
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Avian influenza

  A Focus on Avian Influenza (Bird Flu)
Internal temperature of baked chicken must reach 165F

The highly pathogenic Avian Influenza H5N1 virus has killed millions of poultry in a growing number of countries throughout Asia, Europe and Africa. Although Avian Influenza viruses are essentially animal diseases, the highly pathogenic H5N1 is able to infect and kill humans. Health experts are concerned that the co-existence of human flu viruses and avian flu viruses (especially H5N1) will provide an opportunity for genetic material to be exchanged between species-specific viruses, possibly creating a new virulent influenza strain that is easily transmissible and lethal to humans.

In addition to human health concerns, if H5N1 is introduced into the United States (U.S.) by migratory birds or other means, it could have a very significant impact on the North American poultry industry and the safety and stability of the food supply. In an effort to protect our commercial flocks and prevent infected birds from reaching the farm-to-table continuum, scientists, epidemiologists, and animal health experts from industry, government, and academia are developing avian influenza control measures in the areas of: biosecurity, surveillance, intervention and inspection. If, however, H5N1 infected birds should enter the U.S. food supply, commercial food processing interventions currently used to reduce microbial pathogens (i.e. Salmonella) would further help to eliminate the virus.

Type A influenza Viruses and Avian Influenza
Geese flying

Avian Influenza (AI) or “Bird Flu” is a type A influenza virus. Type A influenza viruses are also found in mammals including humans, pigs, horses, and marine mammals.14 Waterfowl and seabirds provide a natural reservoir for all known influenza A viruses and scientific evidence suggests that mammalian influenza viruses could have evolved from avian influenza viruses even though a significant species barrier exists making avian-to-mammalian transmission inefficient and limited.17 In May of 1997, when the first influenza A H5N1 subtype was isolated from a child in Hong Kong, it became clearer that in spite of a host-range restriction, AI can cause zoonotic disease and should be closely monitored.14, 19

Influenza A viruses are categorized into subtypes on the basis of two glycoproteins or surface antigens: hemagglutinin (HA) and neuraminidase (NA). Hemagglutinin attaches the virion to the host cell receptor for cell entry and neuraminidase facilitates the spread of the progeny virus. There are 16 different HA subtypes, H1 to H16, and 9 different NA subtypes, N1 to N9, allowing for many different combinations of HA and NA proteins. These subtypes are further classified into strains.16, 18

There are genetic differences between the influenza A subtypes that infect birds and the subtypes that infect both people and birds. There are three HA subtypes (H1-H3) of influenza A viruses that are known to only infect humans, such as influenza A virus H1N1 which caused the Spanish Flu Epidemic in 1918.16 The three HA subtypes of the avian influenza A viruses that are known to infect both birds and humans are: H5, H7, and H9.2, 16 The H5 and H7 subtypes cause a highly pathogenic form of AI such as H7N7, H7N3, and H5N1 viruses.16

Type A influenza viruses are very unstable and dynamic, evolving through either of two processes: antigenic drift or antigenic shift.

  • Antigenic drift happens frequently through point mutations in the two genes that produce the surface antigens HA and NA, causing minor gradual changes in these glycoproteins.
  • Antigenic shift is not frequent and represents an abrupt, large change resulting in a new influenza A subtype that has never circulated among humans. Antigenic shift can occur during direct animal-to-human transmission or through genetic reassortment, a process that occurs when human and animal influenza A virus genes exchange genetic material in a host co-infected with both strains.16 This process can result in a novel human influenza A virus that is lethal and highly transmissible between persons. Some experts suggest that genetic reassortment could have preceded the influenza pandemics of 1918, 1957, and 1968.14, 15

The Avian Influenza A (H5N1) virus, currently being spread by migratory birds across Asia, Europe and Africa, causing poultry outbreaks and mortality in both poultry and humans is an example of the instability of the Type A viruses. According to some scientists, “several lines of evidence indicate that the currently circulating influenza A (H5N1) viruses have in fact evolved to more virulent forms since 1997, with a higher mortality among human cases, different antigenic properties, a different internal gene constellation, and an expanded host range.” 15

As a matter of fact, researchers at the United States Department of Agriculture’s (USDA) Agricultural Research Service (ARS) have compared the relationships between H5N1 viruses from multiple countries over several years. The study found that most of the H5N1 isolates from humans were antigenically homogeneous and distinct from viruses circulating before the end of 2003, and some of the 2005 isolates showed evidence of antigenic drift.26

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Veterinarian David Swayne

Pathogenicity
AI viruses are categorized into one of two main pathotypes: low pathogenicity avian influenza (LPAI) or high pathogenicity avian influenza (HPAI). This classification is based on virulence or the virus’s ability to cause severe disease and death in chickens.11, 12 Most strains are low pathogenic and cause only mild symptoms (such as a drop in egg production) and may even go undetected. The highly pathogenic strains such as H5N1 often spread more rapidly through poultry flocks and can sometimes have a mortality rate that reaches 90-100 percent within 2 or 3 days if the virus speads to multiple internal organs. It is possible for LPAI viruses to evolve into HPAI viruses or for both pathotypes to evolve into a more virulent form.12

Transmission
Avian species differ in their susceptibility to the type A influenza virus, but domestic chickens and turkeys are most susceptible, and large outbreaks have previously been initiated by direct or indirect contact with waterfowl.8 Generally, wild waterfowl are both natural and silent reservoirs of avian influenza viruses since they carry and transmit the virus to domestic birds and are asymptomatic because the virus is often nonpathogenic to them. However, since late 2002, H5N1 outbreaks in Asia have resulted in severe, systemic disease and mortality among waterfowl, especially young ducks.12

Natural carriers (waterfowl, seabirds) shed the AI virus in their feces, nasal secretions, and saliva transmitting it to domestic flocks of chickens and turkeys. Once the virus has infected one domestic bird in a flock, it quickly spreads because:

  • infected birds shed the virus in their oral secretions and feces for up to 10 days;2
  • the virus can live for long periods of time (several weeks) in the feces shed from sick birds; and
  • poultry are kept in close quarters facilitating further spread of the virus.

According to the World Health Organization (WHO), “susceptible birds become infected when they have contact with contaminated secretions or excretions or with surfaces that are contaminated with secretions or excretions from infected birds. Domesticated birds may become infected with avian influenza virus through direct contact with infected waterfowl or other infected poultry, or through contact with surfaces (such as dirt or cages) or materials (such as water or feed) that have been contaminated with the virus.” 8

Food Safety and Highly Pathogenic (mainly H5N1) Avian Influenza Viruses
Eggs in carton

Researchers are evaluating the risk of highly pathogenic avian influenza viruses being transmitted to humans via poultry products in the food chain. The transmission of highly pathogenic avian influenza viruses to humans, mainly H5N1, is not clearly understood and exploring all possible sources of infection and routes of transmission will help determine the public health risk. “The exact entry route(s) of the virus in humans is (are) not known but it is generally accepted that respiratory and/or oropharyngeal tissues are the entry sites.” 4

Current evidence suggests that humans can become infected with H5N1 avian influenza virus following direct contact with live or dead infected birds, and the greatest risk of exposure is for those individuals who handle and slaughter infected birds. It is possible that handling or ingesting “uncooked” or “improperly cooked” poultry products, such as raw chicken meat and eggs, could be a possible transmission route.3

Handling and Consumption of Poultry Products

Virus quantities present in infected food of avian origin is quite variable and depends on several factors: virus strain; avian species; type of organ; stage of infection at which the food product was collected; the degree of viraemia; physical or chemical treatments on the food (heating; cooking; freezing); and pH changes in meat after slaughter.4 Refrigeration and freezing can actually help the virus to survive on fresh contaminated poultry meat, therefore it can be spread during food marketing, distribution, and preparation making good hygiene practices essential to avoid cross contamination.2

Since the H5N1 virus is present in the meat and eggs of infected poultry, some experts are concerned about advising the public that it is safe to eat poultry meat and eggs.6 These experts have raised the issue that although thorough cooking can kill the virus, people don’t always follow the guidelines for safe handling of food. In addition, although evidence doesn’t prove that the human intestinal tract is a portal of entry for infection or that the virus replicates in the gut, evidence also doesn’t prove against it.6 Some mammals (felines, ferrets, mice) have already become infected by eating raw infected bird meat. 6, 7, 13

The WHO clearly states that the key to preventing avian influenza in food consumption is to properly cook the meat product(s). “To date, no epidemiological data suggests that the disease can be transmitted to humans through properly cooked food (even if contaminated with the virus prior to cooking). However, in a few instances, cases have been linked to consumption of dishes made of raw contaminated poultry blood.” 1, 2

The Food Standards Agency (FSA) of the United Kingdom (UK) is also advising its consumers that avian flu does not pose a food safety risk and is emphasizing the importance of proper food handling during poultry preparation. Following recent risk assessment advice from its independent expert scientific body, the Advisory Committee on Microbiological Safety of Food (ACMSF), the FSA has suggested that even if the AI virus is present after cooking, several other factors exist in humans that will prevent or limit infection following ingestion. They human factors include: saliva, gastric acid, and the lack of appropriate receptors in the gut needed for the virus to enter the body. 31

The European Food Safety Authority (EFSA)’s published scientific risk assessment report released in February 2006 titled, “Food as a Possible Source of Infection with Highly Pathogenic Avian Influenza Viruses for Humans and other Mammals”, also agrees that no direct evidence implicates poultry products in the transmission of H5N1 avian influenza virus to humans. The report reviews the science regarding the fate of highly pathogenic Avian Influenza viruses in avian species, and the food chain as a potential vehicle of transmission. It states that no evidence currently exists to prove that the human intestinal tract is a portal of entry or a target organ for the H5N1 virus, but that the existence of an undisclosed virus entry site in the intestinal tract can not be ruled out at this time.4 The report recommended that experimental inoculation studies be conducted on animal models (i.e. pigs, cats, ferrets) to examine different inoculation routes and virus replication in different tissues along the course of infection.4

EFSA’s current position statement is, “on present evidence, humans who have acquired the infection have been in direct contact with infected live or dead birds. There is no epidemiological evidence to date that avian influenza can be transmitted to humans through consumption of food, notably poultry and eggs. EFSA and other organizations such as the WHO generally support longstanding food safety advice that chicken and eggs be properly cooked in order to protect consumers from possible risks of food poisoning. Thoroughly cooking poultry meat and eggs also eliminates viruses, thereby providing further safety assurance in the unlikely event that H5N1 virus maybe present in raw poultry products entering the food
chain.” 32

Cooking poultry products (chicken, duck, goose, turkey, and guinea fowl) thoroughly and to the proper temperature (at or above 70C in all parts of the product) is essential to kill the H5N1 virus and prevent transmission from food.2, 10

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Avian Influenza (H5N1) and Humans 3
Hens in a cage at a market

Since the first Avian Influenza outbreak occurred in 1997, there has been an increasing number of HPAI H5N1 bird-to-human transmissions leading to clinically severe and fatal human infections. However, because there is a significant species barrier that exists between birds and humans, the virus does not easily cross over to humans, and currently there is no evidence that human to human transmission is occurring. Although millions of birds have become infected with the virus since its discovery, 206 humans have died from the H5N1 in twelve countries according to WHO data as of November 2007. For more information:

More research is necessary to understand the pathogenesis and epidemiology of the H5N1 virus in humans. Exposure routes and other disease transmission characteristics such as genetic and immunological factors, that may increase the likelihood of infection, are not clearly understood. To date, the majority of humans infected with the H5N1 lived or worked in small family farms with backyard flocks, and/or are poultry workers that handled or butchered infected birds in wet markets or live animal markets.

Other possible exposure routes are direct contact with poultry feces or swimming in water contaminated with carcasses or feces of infected birds. In a few cases, children were thought to become sick because they had contact with contaminated feces of free-ranging chickens while playing. In some cases, no exposure route was identified suggesting unknown environmental factors may act as disease vectors.

Clinical Signs and Symptoms in Humans5

According to the WHO, the highly pathogenic H5N1 virus has an aggressive course with rapid clinical deterioration and high fatality rates. Current data for H5N1 infection in humans suggests it may be longer than the seasonal influenza (2-3 days) with an incubation period anywhere from two to eight days or as long as 17 days.

Initial symptoms included below have been reported in some, not all, infected H5N1 patients. The spectrum of clinical symptoms may be broader than those mentioned.*

  • high fever, usually with a temperature higher than 38C and influenza-like symptoms
  • influenza-like symptoms
  • diarrhea, vomiting, abdominal pain, chest pain, and bleeding from the nose and gums
  • watery diarrhea without blood appears
  • respiratory symptoms
  • development of manifestations in the lower respiratory tract

Other clinical features 3 or more days post symptom onset:*

  • Difficulty breathing, respiratory distress, a hoarse voice, and a crackling sound when inhaling are commonly seen
  • Sputum production is variable and sometimes bloody
  • Blood-tinted respiratory secretions
  • Pneumonia (primary viral pneumonia)
  • Multi-organ dysfunction.
  • Common laboratory abnormalities: leukopenia (mainly lymphopenia), mild-to-moderate thrombocytopenia, elevated aminotransferases, and with some instances of disseminated intravascular coagulation.

These clinical features could change given the tendency of this virus to evolve quickly and unpredictably.

*Symptoms described were taken almost verbatim from resource cited to ensure accuracy due to the variability of symptoms in patients.

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Avian Influenza (H5N1) in Mammals
Avian influenza viruses can also be transmitted to mammals. Some examples of mammals that have become infected with the highly pathogenic influenza type H5N1 are cats and ferrets. In January of 2004 in a Thailand zoo, 140 tigers died or were euthanized after being fed H5N1 infected chicken and there was also reasonable evidence of tiger to tiger transmission.7

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Avian Influenza Research at the USDA Agricultural Research Service
Veterinary Medical Officer David Suarez works to eradicate avian influenza

The pathogenesis of avian influenza viruses in humans is not clearly understood. Disease surveillance programs and molecular epidemiological studies will help scientists understand how and why these viruses infect humans and what pandemic risks they pose.

The United States Department of Agriculture (USDA) Agricultural Research Service (ARS) is working to develop new vaccines and diagnostic tools to help control this disease in poultry.9, 22, 25 Research projects have investigated the risk of LPAI and HPAI viruses being transmitted to humans through food. ARS researchers have already determined the effectiveness of pasteurization and cooking to inactivate the virus in egg products and poultry meat. This heat inactivation information helped the USDA’s Animal and Plant Health Inspection Service (APHIS) with trade negotiations of poultry and poultry products from the U.S. to other countries, including Japan.27

The Southeast Poultry Research Laboratory (SEPRL) of the USDA/ARS conducts basic and applied research to study national and international exotic and emerging poultry disease problems that impact poultry and human health. Since 1997, SEPRL has focused on avian influenza H5N1 research such as: assessing food safety risk; developing diagnostic tests and vaccines; identifying risk factors that impact international trade; and evaluating virulence factors of AI.11

SEPRL has four major objectives of avian influenza research: 11

  1. Determine how AI virus causes disease in poultry and why some strains are more virulent than others.
  2. Evaluate the genetics of the virus for epidemiological studies that will trace the origin of viruses during outbreaks. This research can be related to their other work involving the surveillance of wild birds in North America.
  3. Develop control measures for AI viruses including vaccine development and improvement of vaccine strategies.
  4. Develop diagnostic and detection tests for AIV.

SEPRLs Research Accomplishments: 11

  1. Developed a real-time polymerase chain reaction (RT-PCR) diagnostic test for avian influenza that is rapid, sensitive, and specific.
  2. Developed new vaccines and strategies for vaccine application.
  3. Evaluated different vaccine types and formulations and determined which vaccine virus strains provide the best protection.
  4. Demonstrated that during improper vaccine use, genetic changes in AI virus can occur and decrease vaccine protection, similar to what happens with human influenza vaccine.
  5. Determined the risk of exposure to AI virus through the food supply is negligible or minimal and that AI virus is rapidly inactivated by normal cooking and in the case of egg products, pasteurization.
  6. Maintained surveillance of free-flying wild birds throughout the United States (including Alaska) for AI viruses.
  7. Characterized AI virus strains for numerous outbreaks in the United States and around the world.

Individual research projects that are currently being conducted at the Exotic and Emerging Avian Viral Diseases Research Unit to meet the SEPRL objectives and accomplishments listed above include:

Mucosal Immunization to Protect Poultry against Avian Influenza

Project Objectives:23

  1. Develop vaccines that induce a strong mucosal immune response against avian influenza
  2. Develop diagnostic tests to evaluate vaccine effectiveness
  3. Develop sensitive serological tests for AI detection.
  4. Develop sensitive serological tests to differentiate vaccinated from AI virus infected chickens.
  5. Develop, evaluate, and validate on-farm diagnostic tests to establish disease transmission patterns and routes.
  6. Establish on-farm biosecurity practices for AI disease prevention

Evaluation of Avian Influenza Isolates for Suitability as Vaccines

Project Objectives:21

  1. Evaluate the antigenic drift in H5 subtype AI virus vaccines from Mexico.
  2. Determine specific amino acid changes important for immunity and vaccine efficacy.

Development of Cooking Standards for Inactivation of Avian Influenza and Newcastle Disease Viruses in Poultry Meat

Project Objectives:30

  1. Develop cooking standards to kill HPAI viruses in poultry meat by determining Dt and Z values for heat inactivation at commercial cooking temperatures and processes.

Laboratory Assessment of Avian Influenza Transmission to Agricultural Animals and Humans through Meat Infected with …Avian Influenza Virus

Project Objectives: 20

  1. Determine the transmission potential and infective dose needed for transmission of H5N1 virus to chickens and other agricultural animals through infected chicken meat.
  2. Assess the suitability of laboratory mammals (i.e. ferrets) to be used as animal models to study human transmission of H5N1 via consumption of infected chicken meat.
  3. Determine transmission potential and infective dose needed for transmission of H5N1 virus to an animal model for human infection through infected chicken meat.
  4. Determine if four additional HPAI viruses can be transmitted through infected chicken meat to chickens, ducks and an animal model for human infection.

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Scientist injecting flu antigen into eggs

Application of Molecular Biological Techniques to the Diagnosis & Control of Avian Influenza/vaccines & Anti-Virals to Protect Food Animals

Project Objectives: 28

  1. Define the role of individual genes in virulence of influenza and characterize how the host’s response affects infection and disease.
  2. Develop a comprehensive influenza sequence database.
  3. Develop new poultry vaccines against AI.
  4. Improve existing AI diagnostic tests to be more rapid and accurate.
  5. Evaluate the efficacy of existing AI vaccines.
  6. Develop AI vaccines that allow mass immunization through water, feed, or aerosol sprayers, elimination need for individual injection.
  7. Develop vaccines and companion serological diagnostic tests that distinguish vaccinated birds from field infected birds.
  8. Develop AI vaccines that cross protect against different subtypes.
  9. Develop automated ELISA based serological tests that can predict flock immunity from AI vaccines.
  10. Develop vaccine challenge models that will predict efficacy of new vaccines against both LPAI and HPAI viruses.
  11. Improve sensitivity of RT-PCR procedures for detection of AI infections in poultry and differentiate HA and NA subtype in less than 8 hours.
  12. Develop a rapid “pen side” screening test for simultaneous detection of AI virus and identification of HA and NA subtypes.
  13. Develop improved models to predict which LPAI viruses can evolve into HPAI viruses.
  14. Fund international efforts to collect and sequence AI viruses with specialized bioinformatics technologies.
  15. Develop a global AI molecular epidemiological map based on wild bird and poultry AI viruses.

2005 Annual Report: Application of Molecular Biological Techniques to the Diagnosis & Control of Avian Influenza/vaccines & Anti-Virals to Protect Food Animals

Accomplishments: 27

  1. Used reverse genetic techniques to predict virulence of avian influenza viruses.
  2. Evaluated several outbreaks to understand the molecular epidemiology of AI viruses. These outbreaks included: H5 in Texas; H3N2 in turkeys from several states; and H4 and H6 viruses from wild birds.
  3. Vaccine development including the use of DNA vaccines.
  4. Improved an existing diagnostic test to prevent false negative tests.

2005: Annual Report: Mucosal Immunization to Protect Poultry Against Avian Influenza

Accomplishments: 24

  1. Developed and evaluated two new recombinant avian influenza vaccines.
  2. Developed an ELISA test to detect antibodies against the non-structural (NS) protein of influenza virus that can be used as a DIVA (differentiate infected from vaccinated animals) test. 29
  3. Examined human pandemic H5 and H7 influenza vaccine strains and found them to be low risk to agricultural systems should they escape during the manufacturing process.
  4. Improved the use of DNA vaccines for use in the production of reference diagnostic reagents with the addition of the cytokine adjuvants, IL-2 and interferon.

Prevention and Control of Avian Influenza in the U.S. (AICAP)

AICAP is a research and education project established by the USDA in 2005 to help prevent and control avian influenza. The project is led by the University of Maryland, College Park, and includes a multidisciplinary team of researchers and extension specialists from 17 states.

For additional information:

References

1. World Health Organization. (2006). Avian influenza: food safety issues. Retrieved April 6. 2006, from http://www.who.int/foodsafety/micro/avian/en/.

2. World Health Organization. (2006). Highly pathogenic H5N1 avian influenza outbreaks in poultry and in humans: Food safety implications. Retrieved April 6, 2006, from
http://www.who.int/entity/foodsafety/fs_management/No_07_AI_Nov05_en.pdf.

3. World Health Organization. (2006). Avian influenza (" bird flu") – The Disease in Humans. Retrieved April 6, 2006, from http://www.who.int/mediacentre/factsheets/avian_influenza/en/#humans.

4. (2006). Scientific Report of the Scientific Panel on Biological Hazards on “Food as a possible source of infection with highly pathogenic avian influenza viruses for humans and other mammals”. The EFSA Journal, 74, 1-29. Retrieved April 12, 2006, from
http://www.efsa.eu.int/science/biohaz/biohaz_documents/catindex_en.html.

5. World Health Organization. (2006). Avian influenza (" bird flu"): Clinical Features. Retrieved April 6, 2006, from http://www.who.int/mediacentre/factsheets/avian_influenza/en/#clinical.

6. Butler, D. (13 April 2006). Bird-Flu Experts Question Advice on Eating Poultry. Nature 440, 850-851. Retrieved April 13, 2006, from http://www.nature.com/nature/journal/v440/n7086/full/440850a.html.

7. Thanawongnuwech R., Amonsin A., Tantilertcharoen R., Damrongwatanapokin S., Theamboonlers A., Payungporn S., et al. (2005) Probable tiger-to-tiger transmission of avian influenza H5N1. Emerging Infectious Diseases. Retrieved April 13, 2006, from
http://www.cdc.gov/ncidod/EID/vol11no05/05-0007.htm.

8. Centers for Disease Control. (2006). Key Facts about Avian Influenza (Bird Flu) and Avian Influenza A (H5N1) Virus. Retrieved April 20, 2006, from
http://www.cdc.gov/flu/avian/gen-info/facts.htm.

9. Respiratory Diseases Committee of the American Association of Avian Pathologists -- USDA, Agricultural Research Service used with permission. (2005). Asian Bird Flu. Retrieved April 11, 2006, from http://ars.usda.gov/Research/docs.htm?docid=11425.

10. World Health Organization. (2006). Prevention of Foodborne Disease: Five Keys to Safer Food. Retrieved April 3, 2006, from http://www.who.int/foodsafety/consumer/5keys/en/.

11. USDA, Agricultural Research Service. (2005). Avian Influenza Virus. Retrieved April 11, 2006, from http://www.ars.usda.gov/Research/docs.htm?docid=11421.

12. USDA, Agricultural Research Service. (2006). Pathogenicity of Avian Influenza Viruses in Poultry. Retrieved April 11, 2006, from
http://www.ars.usda.gov/research/publications/publications.htm?seq_no_115=180717.

13. Influenza team, European Centre of Disease Prevention and Control, Stockholm, Sweden (2006, April 13). H5N1 infections in cats – public health implications. Euro Surveillance 11(4), Article E060413.4. Retrieved April 25, 2006, from http://www.eurosurveillance.org/ew/2006/060413.asp#4.

14. Yuen K., Chan, P., Peiris, M., Tsang, D., Que, T., Shortridge, K., Cheung, P., To, W., Ho, E., & Sung, R. (1998). Clinical features and rapid viral diagnosis of human disease associated with avian influenza A H5N1 virus. The Lancet, 351, 467-471. Retrieved April 13, 2006, from http://tinyurl.com/fdvla.

15. Ungchusak K., Auewarakul P., Dowell S.F., Kitphati R., Auwanit W., Puthavathana P., Uiprasertkul M., Boonnak K., Pittayawonganon C., Cox N.J., Zaki S.R., Thawatsupha P., Chittaganpitch M., Khontong R., Simmerman J.M., & Chunsutthiwat S. (2005). Probable Person-to-Person Transmission of Avian Influenza A (H5N1). New England Journal of Medicine, 352(4), 333-340. Retrieved April 7, 2006, from http://content.nejm.org/cgi/content/abstract/352/4/333.

16. Centers for Disease Control. (2005). Influenza Viruses. Retrieved April 25, 2006, from http://www.cdc.gov/flu/avian/gen-info/flu-viruses.htm.

17. Karasin A.I., Brown I.H., Carman S., Olsen C.W. (2000). Isolation and Characterization of H4N6 Avian Influenza Viruses from Pigs with Pneumonia in Canada. Journal of Virology, 74(19), 9322-9327. Retrieved April 24, 2006, from http://jvi.asm.org/cgi/content/full/74/19/9322.

18. Canadian Food Inspection Agency. (2005). Avian Influenza - Virus Subtypes. Retrieved April 20, 2006, from http://www.inspection.gc.ca/english/anima/heasan/disemala/avflu/bacdoc/avflutypese.shtml.

19. de Jong J.C., Claas E.C., Osterhaus A.D., Webster R.G., & Lim W.L. (1997). A Pandemic Warning. Nature, 389, 554 -555. Retrieved April 9, 2006, from http://www.nature.com/nature/journal/v389/n6651/pdf/389554a0.pdf.

20. USDA, Agricultural Research Service. (2006). Laboratory Assessment of Avian Influenza Transmission to Agricultural Animals and Humans through Meat Infected with ...avian Influenza Virus. Retrieved April 11, 2006, from
http://www.ars.usda.gov/research/projects/projects.htm?ACCN_NO=409883.

21. USDA, Agricultural Research Service. (2006). Evaluation of Avian Influenza Isolates for Suitability as Vaccines. Retrieved April 11, 2006, from
http://www.ars.usda.gov/research/projects/projects.htm?ACCN_NO=409360.

22. USDA, Agricultural Research Service. (2006). Avian Influenza Virus: Prospects for Prevention and Control by Vaccination. Retrieved April 11, 2006, from
http://www.ars.usda.gov/research/publications/publications.htm?seq_no_115=172748.

23. USDA, Agricultural Research Service. (2006). Mucosal Immunization to Protect Poultry Against Avian Influenza. Retrieved April 11, 2006, from
http://www.ars.usda.gov/research/projects/projects.htm?ACCN_NO=405500.

24. USDA, Agricultural Research Service. (2006). Annual Report 2005: Mucosal Immunization to Protect Poultry Against Avian Influenza. Retrieved April 11, 2006, from http://www.ars.usda.gov/research/projects/projects.htm?
ACCN_NO=405500&showpars=true&fy=2005
.

25. USDA, Agricultural Research Service. (2006). Avian Influenza Vaccination in North America: Strategies and Difficulties. Retrieved April 11, 2006, from
http://www.ars.usda.gov/research/publications/publications.htm?seq_no_115=181470.

26. USDA, Agricultural Research Service. (2006). Evolution of H5n1 Avian Influenza Viruses in Asia: Antigenicity, Antiviral Drug Sensitivity and Vaccine Development. Retrieved April 11, 2006, from
http://www.ars.usda.gov/research/publications/publications.htm?seq_no_115=184356.

27. USDA, Agricultural Research Service. (2006). Annual 2005 Report: Application of Molecular Biological Techniques to the Diagnosis & Control of Avian Influenza/vaccines & Anti-Virals to Protect Food Animals. Retrieved April 12, 2006, from http://www.ars.usda.gov/research/projects/projects.htm?
ACCN_NO=404887&showpars=true&fy=2005
.

28. USDA, Agricultural Research Service. (2006). Application of Molecular Biological Techniques to the Diagnosis & Control of Avian Influenza/vaccines & Anti-Virals to Protect Food Animals. Retrieved April 12, 2006, from
http://www.ars.usda.gov/research/projects/projects.htm?ACCN_NO=404887.

29. USDA, Agricultural Research Service. (2006). Overview of Avian Influenza Diva Test Strategies. Retrieved April 12, 2006, from
http://www.ars.usda.gov/research/publications/publications.htm?seq_no_115=181471.

30. USDA, Agricultural Research Service. (2006). Development of Cooking Standards for Inactivation of Avian Influenza and Newcastle Disease Viruses in Poultry Meat. Retrieved April 11, 2006, from
http://www.ars.usda.gov/research/projects/projects.htm?ACCN_NO=409769.

31. Food Standards Agency. (2008). Bird flu update 16 February 2007. Retrieved March 12, 2008, from
http://www.foodstandards.gov.uk/news/newsarchive/2005/dec/avianflu.

32. European Food Safety Authority. (March 2006). EFSA publishes scientific report on avian influenza and food safety. Retrieved April 12, 2006, from
http://www.efsa.eu.int/press_room/press_statements/1413_en.html.

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Additional Resources

Avian Influenza (Bird Flu) Resource List
USDA. NAL. Food Safety Research Information Office.

Avian Influenza News Feed
USDA. NAL. Food Safety Research Information Office.

Books and Journals from AGRICOLA
USDA. National Agricultural Library.

Isolation and Characterization of Avian Influenza Viruses, Including Highly Pathogenic H5n1 Viruses, from Poultry in Live Bird Markets in Hanoi, Vietnam – 2001
USDA. Agricultural Research Service.

Characterization of Highly Pathogenic H5n1 Avian Influenza a Viruses Isolated from Korean Poultry
USDA. Agricultural Research Service.

Occupational and Consumer Risks from Avian Influenza Viruses
USDA. Agricultural Research Service.

Situation Updates – Avian Influenza
World Health Organization.

Control of Zoonotic Avian Viruses
USDA. Agricultural Research Service.

Avian Influenza
USDA. Agricultural Research Service.


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  1. This document was created by Tara Smith.
    Users are encouraged to provide feedback and comments.
  2. This document was created in May 2006; Updated in Mar 2008

 
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