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Avian Influenza Fact Sheet

Avian Influenza in Humans at CECDP

Synopsis of Avian Influenza
Avian influenza is caused by an Influenza virus. A virus of the family Orthomyxoviridae, which occurs naturally among birds. It was first identified over 100 years ago during an outbreak in Italy. Since then, outbreaks of avian influenza have occurred at irregular intervals all over the world. All birds are thought to be susceptible to infection with avian influenza; however, wild, primarily aquatic, birds serve as the natural host. Infection in host birds is mainly asymptomatic; whereas, infection in domesticated birds, such as chickens, turkeys, and ducks, can range from mild illness to a highly contagious and rapidly fatal disease. Once domestic birds are infected, avian influenza outbreaks can be difficult to control and may have major economic consequences due to the high mortality rates and massive cullings that take place.
  • There are two forms of avian influenza with many strains: A low pathogenicity (LPAI) form that causes mild illness and a highly pathogenicity (HPAI) form that is extremely contagious, causes severe illness, and frequently has high rates of mortality.
  • The strains are identified by two surface proteins designated by the letters H (hemagglutinin) and N (neuraminidase).
  • Outbreaks of LPAI occur frequently worldwide and outbreaks of HPAI (H5 and H7) occur periodically.
  • Infected birds shed the virus in their saliva, nasal secretions, and feces and susceptible birds become infected when they have contact with contaminated excretions or surfaces that are contaminated with excretions.
  • Although avian influenza viruses rarely infect humans, several cases have occurred in Asia since 1997.
  • As a result of these isolated cases, officials are concerned that the virus could mutate to a form that allows human-to-human transmission. If this were to happen, we could possibly be dealing with another major pandemic.
  • Avian influenza can infect humans through poultry-to-human transmission, usually via contact with fecal matter or other live bird excretions.
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Clinical Signs and Symptoms
Birds:
  • Incubation: 3 to 7 days, depending on the isolate, the dose of inoculums, the species, and the age of the bird.
  • Clinical signs and symptoms in carriers (waterfowl):
    • Seroconversion
  • Clinical signs and symptoms in domestic birds:
    • Coughing
    • Sneezing
    • Ruffled feathers
    • Excessive thirst
    • Swollen and cyanotic combs and wattles
    • Congested and swollen conjunctivae with occasional hemorrhage
    • Areas of diffuse hemorrhage between the hocks and feet
    • Edema surrounding the eyes
    • Nervous signs, such as depression
    • Watery green diarrhea that progresses to almost totally white
    • Decreased food consumption
    • Drop in egg production
    • Death can occur within 24 hours of first signs of disease, frequently within 48 hours, or be delayed for as long as a week
  • Postmortem lesions:
    • Severe congestion of the musculature
    • Dehydration
    • Subcutaneous edema of the head and neck area, which is evident as the skin is reflective
    • Fluid may exit the nares and oral cavity
    • Severely congested conjunctivae, occasionally with petechiation
    • Tracheal lumen may contain excessive mucous exudates
    • Hemorrhagic tracheitis
    • Pinpoint petechial hemorrhages on the inside of the keel
    • Pinpoint petechia on the abdominal fat, serosal surfaces, and peritoneum
    • Severely congested kidneys, may be grossly plugged with white urate deposits in the tubules
    • Hemorrhagic or degenerated ovaries with darkened areas of necrosis
    • Peritoneal cavity frequently filled with yolk from ruptured ova (causes severe aircacculitis and peritonitis in birds that survive for 7 to 10 days)
  • HPAI (H5 and H7) prognosis is poor, morbidity and mortality rates may be near 100 percent within 2 to 12 days following the first signs of illness. Birds that survive are usually in poor condition and resume laying eggs only after a period of several weeks.
  • Click on one of the following links for more information on avian influenza in birds:
Pigs:
  • According to the CDC, pigs can be infected with both human and avian influenza viruses.
  • The co-circulation of avian, human, and pig viruses in pigs is of concern because of the potential for genetic exchange, or a "reassortment" of material between these viruses, possibly producing a new, pandemic influenza strain.
  • Signs and Symptoms:
    • Fever
    • Cough
    • Shortness of breath
    • Runny nose
Cats:
Humans:
  • H5N1 can replicate in a wide range of cells, resulting in a severe disseminated disease affecting multiple organs and causing high rates of mortality.
  • Public health officials are concerned that H5N1 could mutate or merge with human flu viruses, possibly allowing efficient human-to-human transmission. Because these viruses rarely infect humans, there is little or no immune protection against them in the human population and, therefore, could possible result in an "influenza pandemic."
  • Signs and Symptoms:
    • Fever
    • Cough
    • Shortness of breath
    • Sore throat
    • Muscle aches
    • Eye infections
    • Pneumonia
    • Severe respiratory diseases
    • Chest radiographs at presentation included extensive, usually bilateral infiltration, lobar collapse, focal consolidation, and air bronchograms
    • Gastrointestinal symptoms include diarrhea, vomiting, and abdominal pain (common in children but not adults) - Click here for more information regarding gastrointestinal symptoms and avian influenza published in Emerging Infectious Diseases, 2004.17
    • Symptoms depend on which virus caused the infection
  • Click here for more human-related information on avian influenza posted on the UAB Website for Bioterrorism and Emerging Infectious Education.11
  • Click here for a review of avian influenza published in the Journal of Clinical Virology, 2005.3
  • Click here for more information from Kansas State University Animal Science and Industry Department on Avian Inluenza.
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Diagnosis and Treatment
Diagnostic Samples:
  • Specimens sent to the laboratory should be accompanied by a history of clinical and gross lesions, including any information on recent additions to the flock.
  • Samples include the following:
    • Tracheal or cloacal swabs (swabs from up to five birds can be pooled in the same tube of broth)
    • Feces
    • Internal organs
    • Trachea, lung, spleen, cloaca, and the brain should be sampled
Differential Diagnosis:
  • In animals, the differential diagnoses include Newcastle disease, infectious laryngotracheitis, duck plague, acute poisonings, and fowl cholera.
  • In humans, the differential diagnosis includes naturally occurring forms of human influenza.
Clinical Diagnosis:
  • HPAI is suspected with any flock where sudden deaths follow severe depression, inappetence, and a drastic decline in egg production. Presence of facial edema, swollen and cyanotic combs and wattles, and petechial hemorrhages on internal membrane surfaces increase the likelihood that the disease is HPAI.
  • Diagnosis depends upon the isolation and identification of the virus from isolates using type A influenza antigen-capture enzyme linked immunosorbance.
Laboratory Tests:
  • Serological testing (using commercially available ELISA kits, which detect antibodies) is used as a preliminary screening method for detecting all avian influenza viruses.
  • Viral isolation ("gold standard"):
    • Hemagglutination inhibition assays are used to detect antibodies against human influenza viruses; however, their usefulness for detection of antibodies against avian viruses in mammalian species, including humans, is limited possibly due to poor immunogenicity of some avian viruses and lack of sensitivity to detect low tittered or less avid antibodies induced by avian viruses.
    • Avian viruses can be isolated in embryonated eggs or in cell culture (using permissive cells such as Madin Darby canine kidney, MDCK, cells or rhesus monkey kidney, LLC-MK2).
    • Requires biosafety level 3 laboratory facilities or higher
  • Subtype-specific reverse transcriptase (RT) PCR is used for subtyping of influenza viruses or detection of subtype-specific antibodies.
  • Rapid diagnosis/confirmation:
    • Immunochromatiographic or immunofluorescent for detection of influenza virus antigens (low sensitivity, some kits do not distinguish between influenza types A and B and none of the available kits distinguish between influenza A subtypes)
    • RT-PCR for detection of viral nucleic acids (Results can be generated in a few hours after specimen collection, however, this test is prone to contamination and the consequent risk of false-positive results)
Treatment:
  • In animals:
    • Supportive care
    • Prevention: Avoidance of ducks and other migratory fowl and the pond waters or other waters that they have been in
    • Vaccination:
      • Inactivated oil-emulsion vaccines, although fairly expensive, have been demonstrated to be effective in reducing mortality, preventing disease, or both, in chickens and turkeys.
      • Viable vaccines prepared using naturally avirulent or attenuated strains (reassortment could result when a single host bird is simultaneously infected with both the vaccine and another AI virus, resulting in a new virus)
      • There is no cross-protection among the 15 known HA subtypes, so either a multivalent vaccine will be needed or vaccination postponed until the prevalent disease-causing subtype in the area is identified.
  • In humans:
    • Supportive care
    • Antiviral medications:
      • Amantadine (inhibits ion channel activity of the M2 membrane proteins)
        • Disadvantages include neurotoxicity and rapid development of drug resistance (single nucleotide substitution resulting in amino acid substitutions at positions 26, 27, 30, 31, or 34 of the M2 Protein)
      • Rimantadine (inhibits ion channel activity of the M2 membrane proteins)
        • Disadvantages: neurotoxicity is less pronounced than amantadine, however, rimantadine is not available in most parts of the world
      • Oseltamivir (inhibits neuraminidase)
        • Proven efficacy if started early during the course of illness or if used as a seasonal or post exposure prophylaxis
        • Proven efficacy if started early during the course of illness or if used as a seasonal or post exposure prophylaxis
      • Zanamivir (inhibits neuraminidase)
        • Proven efficacy if started early during the course of illness or if used as a seasonal or post exposure prophylaxis
        • Poor oral availability and is therefore administered by inhalation (limited use in the elderly)
        • Development of drug resistance has been reported (mutations in the active site of neuraminidase or in the hemaglutinin)
      • H5N1 virus (currently infecting birds and some humans in Asia) appears to be resistant to amantadine and rimantadine, two of the commonly used medications for treating influenza.
    • There currently is no vaccine to protect humans against the H5N1 virus; however, vaccine development efforts began in April 2005.
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Econcomic Consequences and Disease Eradication
Economic Consequences:
  • Loss of flocks:
    • In the mid-Atlantic region, Delaware, Maryland, Virginia, and Pennsylvania account for about 10% of U.S. broiler production.
    • Texas accounts for about 7% of broiler production.
    • The affected states are not among the major poultry producing states in the U.S. and, therefore, overall supply of poultry to the U.S. market did not decrease noticeably. Furthermore, non-infected flocks from the infected areas will eventually be marketed once officials determine that it is safe to transport the birds.
    • In terms of domestic consumption, avian influenza is not expected to reduce consumer confidence in poultry, given the steady demand for beef even after the discovery of BSE in the U.S. in December 2003.
  • Costs associated with eradication efforts:
    • Indemnification programs for LPAI are generally managed by the individual states.
    • Indemnification programs for HPAI are generally managed by the USDA.
    • The standard rate of indemnification offered by the USDA is 50% of fair market value for losses associated with depopulation; however, in the case of depopulation due to HPAI, the standard allowable rate of indemnification is 100%.
  • International trade embargoes:
    • In terms of U.S. exports, the U.S. exports about 16% of its poultry production and, as a result of the outbreaks below, 50 foreign countries have imposed restrictions on importing U.S. poultry and poultry products, affecting over 10% of such exports.
  • Federal appropriations to control avian influenza in poultry:
    • Congress appropriated APHIS $994,000 for avian influenza in FY2004, primarily for the control in live birds.
    • The USDA released $13.7 million of Commodity Credit Corporation funds for the purpose of instituting a larger, national LPAI program and to assist Texas with the HPAI outbreak.
    • For FY2005, APHIS requested a significant increase to expand its avian influenza program from $1 million to $12.7 million, more than half of which is expected to be used for indemnities when flocks are destroyed.
  • Increased costs to consumers
Disease Prevention and Eradication:
  • Immediate notification of state and federal health officials if AI signs are observed, especially if they are accompanied by a drop in feed consumption and/or a significant drop in egg production.
  • Quarantine and destruction of infected or potentially exposed poultry flocks are standard control measures aimed at preventing spread to other farms and establishment of the virus in the local poultry population.
  • USDA importation of birds:
    • All birds must be quarantined and tested for avian influenza virus prior to entering the U.S.
  • Prevention and control measures:
    • Protect domestic poultry by preventing contact with free-flying birds or their feces
    • Avoid live markets and educate employees about the dangers posed by these markets
    • Prevent contact between newly infected and susceptible birds
    • Control the traffic between infected and uninfected birds
    • Remove all organic material and completely clean and disinfect all surfaces of houses, equipment and area
    • Vaccines are generally not practical to prevent infections since they are not cross-protective for the 15 virus subtypes that infect poultry and since there is no way to predict which type will infect a flock
  • Click on one of the following links for more information on biosecurity and containment procedures:6, 14, 20, 25, 37
  • Click on one of the following links for more information on depopulation and composting:7
  • Viability:
    • Avian influenza virus may remain infectious in soil, water, or contaminated equipment for weeks to months depending on the temperature and humidity (i.e., longer in colder climates).
    • Viruses can survive indefinitely in frozen material.
  • Viral inactivation:
    • Heat and drying
    • Most disinfectants and detergents; in order to ensure that the cleaning and disinfecting process is thorough, the area to be disinfected must be clear of organic materials
  • Click here for more information on pathogen surveillance in animals published in Science, 2005.30
Avian Influenza and Bioterrorism:
  • The prospect of intentionally generating novel viral strains with pandemic potential is a real concern. There is some evidence that research directed toward engineering of bioweapons with improved lethality was conducted in the past, demonstrating that the threat is not simply hypothetical.
  • Bioweapon potential:
    • Highly contagious among birds
    • Morbidity and mortality is high
    • Virus in infected birds is shed in high concentrations
    • Airborne transmission has been demonstrated when birds are in close proximity with appropriate air movement
    • Historically, it was considered very unusual for avian influenza to directly infect humans. However, recent reports [Hong Kong (H5N1), 1997; Hong Kong/China (H9N2), 1999; Netherlands (H7N7), 2003; Asia (H5N1), 2003-present] indicate that at least some people who have had contact with domestic poultry have become directly infected with virulent avian influenza virus. Click here for more information on ecological and immunological determinants of influenza evolution published in Nature, 2003.24
  • For more information on avian influenza and response to a natural or intentional-induced pandemic, click on one of the following links:
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Outbreaks
Avian Influenza Outbreak Information: Animal cases in the United States
  • 2004: Several flocks of chickens (~ 80,000 chickens) in Delaware tested positive for H7N2 (LPAI). The flocks were destroyed and composted. Delaware also imposed a temporary ban on live poultry sales and expanded the quarantine to about 80 farms in a six-mile radius. Click here for more information on this outbreak published by Delmarva Poultry Industry, Inc.36
  • 2004: H7N2 (LPAI) was also discovered in four live bird markets in New Jersey and in a commercial flock of about 330,000 chickens in Maryland.
  • 2004: A flock tested positive for H2N2 (LPAI) in Pennsylvania.
  • 2004: A flock of about 7,000 chickens and two live bird markets tested positive for an H5N2 (HPAI) in Texas. The birds were depopulated and quarantine was imposed. Click here for more information on this outbreak published in the Journal of Virology, 2004.31
  • 2003: Two commercial operations managed by the same enterprise in Connecticut tested positive for H7N2 (LPAI).
  • 1983-1984: 17 million birds had to be destroyed in Pennsylvania as a result of HPAI (H5N1) at a cost of about $65 million.
  • Source: World Health Organization Website. Available at http://www.who.int/csr/disease/avian_influenza/country/cases_table_2005_11_17/....
  • Note: WHO reports only laboratory-confirmed cases.
Avian Influenza Update (February 2006): Animal cases (H5N1)
Number of Avian Influenza Outbreaks (H5N1) by Country According to the FAO Agriculture Department.
Source: FAO Agriculture Department. Available at http://www.fao.org/ag/againfo/home/en/who.html.
CountryWinter 2003Spring 2004Summer 2004Autumn 2004Winter 2004Spring 2005Summer 2005Autumn 2005Total
Cambodia92112
China50111313794
Croatia33
Indonesia627645129
Japan77
Kazakstan11
Korea9211
Kuwait11
Laos1919
Malaysia55
Mongolia213
Romania2929
Russian Federation221032
Thailand183793582122318411049
Turkey55
Ukraine1717
Vietnam84104320695912971771
Total Outbreaks367114414596116052444413188
Avian Influenza Outbreak Information: Human Cases
  • The first recorded case of poultry-to-human transmission of avian influenza occurred in Hong Kong in 1997. Officials determined that close contact with live infected poultry was the source of this infection and genetic studies determined that the virus had jumped directly from birds to humans. Since that time, there have been several recorded cases of human infection as a result of avian influenza virus and, as of late June 2005, health officials throughout Asia have reported a total of 108 confirmed human cases of AI (H5N1), with 54 of these infections resulting in mortality. Human cases have also been reported in the Netherlands in 2003 (89 confirmed cases and 1 death associated with H7N7). While evidence of human-to-human transmission is limited, one case of probable human-to-human transmission was reported in Thailand and two possible cases have been reported in Vietnam. Humans co-infected with avian influenza and another influenza strain could theoretically serve as a host for genetic reassortment events of the two strains. The world has not experienced an influenza pandemic since 1968.
Date of onsetIndonesiaVietnamThailandCambodiaChinaTotal
casesdeathscasesdeathscasesdeathscasesdeathscasesdeathscasesdeaths
12/03- 03/0400231612800003524
07/04-10/04004454000098
12/04- present11765224144218635
Total11792422113442113067
  • Future Pandemic: The most severe flu pandemic occurred in 1918 and resulted in the death of more than 20 million people worldwide; 550,00 people died in the U.S. and 28 percent were sickened by the illness. The CDC projects that a modern pandemic would likely result in 2 to 7.4 million deaths worldwide and affect as many as over 300 million people.
  • Visit the World Organization for Animal Health Website for additional information about these outbreaks.
  • Click on one of the following links for more information on avian influenza infection in humans, 1 (Wildlife Conservation Society), 2 (N Engl J Med, 2005), 3 (J Infect Dis, 2005), 4 (Emerg Infect Dis, 2004).13, 19, 27, 28
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Sources and Related Articles
Sources:
  1. Animal and Plant Health Inspection Service, USDA, April 2002. Fact Sheet: Low Pathogenic Avian Influenza Virus. Available at http://www.aphis.usda.gov/lpa/pubs/fsheet_faq_notice/fs_ahlpai.pdf.
  2. Centers for Disease Control and Prevention, October 25, 2005. Key Facts: Information about Avian Influenza (Bird Flu) and Avian Influenza A (H5N1) Virus. Available at http://www.cdc.gov/flu/avian/gen-info/pdf/avianflufacts.pdf.
  3. Center for Infectious Disease Research and Policy at the University of Minnesota, 2005. Avian Influenza. Available at http://www.cidrap.umn.edu/cidrap/content/influenza/avianflu/index.html.←
  4. De Jong, M. D. and T. T. Hien, October 4, 2005. Avian Influenza A (H5N1). J Clin Virol. [Epub ahead of print]. Available at http://www.sciencedirect.com/science.
  5. FAO Animal Production and Health Division, January-June 2004. Avian Influenza. EMPRES Transboundary Animal Diseases Bulletin. No. 25 - 2005. Available at http://www.fao.org/ag/againfo/subjects/en/health/diseases-cards/cd/documents/y5537e00.pdf.
  6. Humanitarian Early Warning Service, 2005. Avian Influenza Monitoring Page. A service of the Inter-Agency Standing Committee on Preparedness and Contingency Planning. Available at http://www.hewsweb.org/avian_flu/.←
  7. Maryland Cooperative Extension Service. Biosecurity Safeguards adapted from the DPI Emergency Poultry Disease Manual←.
    1. Biosecurity Procedures for Technical Service Personnel. Available at http://www.agnr.umd.edu/HotTopics/AvianInfluenza/BP1.pdf.
    2. Biosecurity Procedures for Commercial Poultry Farms. Available at http://www.agnr.umd.edu/HotTopics/AvianInfluenza/BP2.pdf.
    3. Biosecurity Procedures for Operators of : Feed Delivery and Pickup Trucks, Chick Delivery Buses, Egg Pickup Vehicles, and Feed Ingredient (Including Grain) Delivery Equipment. Available at http://www.agnr.umd.edu/HotTopics/AvianInfluenza/BP3.pdf.
    4. Biosecurity Procedures for Live-Haul Crews. Available at http://www.agnr.umd.edu/HotTopics/AvianInfluenza/BP4.pdf.
    5. Biosecurity Procedures for Live-Haul Crews, part 2. Available at http://www.agnr.umd.edu/HotTopics/AvianInfluenza/BP5.pdf.
    6. Biosecurity Procedures for Vaccination Crews, Beak Trimming Crews, Pullet/Cockerel Movers, Crews Moving Hens to Slaughter. Available at http://www.agnr.umd.edu/HotTopics/AvianInfluenza/BP6.pdf.
    7. Biosecurity Procedures for Poultry Industry Support Companies (Electric and Gas Company Field Personnel, Etc.). Available at http://www.agnr.umd.edu/HotTopics/AvianInfluenza/BP7.pdf.
    8. Biosecurity Procedures for Suppliers of Goods (Poultry Litter and/or Vaccines/Drugs and Chemicals). Available at http://www.agnr.umd.edu/HotTopics/AvianInfluenza/BP8.pdf.
    9. Biosecurity Procedures for Live Bird Suppliers and Haulers. Available at http://www.agnr.umd.edu/HotTopics/AvianInfluenza/BP9.pdf.
  8. Maryland Cooperative Extension Service. Fact Sheets.
  9. National Center for Foreign Animal and Zoonotic Disease Defense, U.S. Department of Homeland Security. Avian Influenza. Available at http://fazd.tamu.edu/factsheets/aifactsheet.
  10. Office International des Epizooties - World Organisation for Animal Health, 2005. Disease Information Published During the Past 18 Months. Available at http://www.oie.int/eng/info/hebdo/A_DSUM.htm.
  11. USGS National Wildlife Health Center, August 2005. The Avian Influenza H5N1 Threat: Current Facts and Future Concerns About Highly Pathogenic Avian Influenza H5N1. Available at http://www.nwhc.usgs.gov/research/avian_influenza/HPAI082005.pdf. ←
  12. UAB: Bioterrorism and Emerging Infections Education. Avian Influenza Summary. Available at http://bioterrorism.uab.edu/EI/Avian/summary.asp.
    13. Related Articles:
  13. Anonymous. How Can We Protect Human, Livestock and Wildlife Health From Avian Influenza? Published by the Wildlife Conservation Society. Available at http://www.wcs.org/media/file/avian-influenzamigratorybirdsaug2005factsheetupdatev2.pdf.←
  14. Anonymous, December 13, 2004. Avian Influenza: Protecting Poultry Workers at Risk. Published by the U.S. Department of Labor, Occupation Safety and Health Administration. Available at http://www.osha.gov/dts/shib/shib121304.pdf.←
  15. Anonymous, 2005. Responding to the Avian Influenza Pandemic Threat: Recommended Strategic Actions. Published by the World Health Organization. Available at http://www.who.int/csr/resources/publications/influenza/WHO_CDS_CSR_GIP_05_8-EN.pdf.←
  16. Anonymous, January 2005. Avian Influenza: Assessing the Pandemic Threat. Published by the World Health Organization. Available at http://www.who.int/csr/disease/influenza/H5N1-9reduit.pdf.←
  17. Apisarnthanarak, A., R. Kitphati, K. Thongphubeth, P. Patoomanunt, P. Anthanont, et. al., July 2004. Atypical Avian Influenza (H5N1). Emerging Infectious Diseases. 10(7):1321-1324. Available at http://www.cdc.gov/ncidod/EID/vol10no7/pdfs/04-0415.pdf.←
  18. Beard, C. W., 1998. Avian Influenza (Fowl Plague). The Gray Book: Foreign Animal Diseases (1998 Edition). Pat Campbell & Associates and Carter Printing Company, Richmond. Available at http://www.vet.uga.edu/vpp/gray_book/FAD/AVI.htm.
  19. Beigel, J. H., J. Farrar, A. M. Han, F. G. Hayden, R. Hyer, et. al., September 29, 2005. Avian Influenza A (H5N1) Infection in Humans. N Engl J Med. 353(13):1374-1385. Available at http://content.nejm.org/cgi/reprint/353/13/1374.pdf.←
  20. Beyer, R. S., March 1996. Avian Influenza Prevention in Gamebird and Ratite Facilities. Published by the Kansas State University Cooperative Extension Service. Available at http://www.oznet.ksu.edu/library/LVSTK2/Mf2114.pdf.←
  21. Chen, H., G. J. D. Smith, S. Y. Zhang, K. Qin, J. Wang, et. al., July 14, 2005. Avian Flu: H5N1 Virus Outbreak in Migratory Waterfowl. Nature. 436:191-192. Available at http://www.nature.com/nature/journal/v436/n7048/pdf/nature03974.pdf.
  22. Cyranoski, D., May 26, 2005. Bird Flu Spreads Among Java's Pigs. Nature. 435(7041):390. Available at http://www.nature.com/nature/journal/v435/n7041/pdf/435390a.pdf.
  23. Fauci, A. S., May 26, 2005. Race Against Time. Nature. 435:423-424. Available at http://www.nature.com/nature/journal/v435/n7041/pdf/435423a.pdf.
  24. Ferguson, N. M., A. P. Galvani, and R. M. Bush, March 27, 2003. Ecological and Immunological Determinants of Influenza Evolution. Nature. 422:428-433. Available at http://www.nature.com/nature/journal/v422/n6930/pdf/nature01509.pdf.←
  25. Ferguson, N. M., D. A. T. Cumminghs, S. Cauchemez, C. Fraser, S. Riley, et. al., September 8, 2005. Strategies for Containing an Emerging Influenza Pandemic in Southeast Asia. Nature. 437:209-214. Available at http://www.nature.com/nature/journal/v437/n7056/pdf/nature04017.pdf.←
  26. Hamburg, M. A., S. A. Hearne, J. Levi, K. Elliot, L. M. Segal, M. J. Earls, June 2005. A Killer Flu? Published by the Trust for America's Health. Available at http://healthyamericans.org/reports/flu/Flu2005.pdf.←
  27. Hayden, F. and A. Croisier, October 15, 2005. Transmission of Avian Influenza Virus to and Between Humans. J Infect Dis. 192(8):1311-1314. Available at http://www.journals.uchicago.edu/JID/journal/issues/v192n8/35079/....←
  28. Hirst, M., C. R. Astell, M. Griffith, S. M. Coughlin, M. Moksa, et. al., December 2004. Novel Avian Influenza H7N3 Strain Outbreak, British Columbia. Emerging Infectious Diseases. 10(12):2192-2195. Available at http://www.cdc.gov/ncidod/EID/vol10no12/pdfs/04-0743.pdf.←
  29. King, P. B., February 2004. What Small Flock Owners Should Know About "Bird Flu" (or Avian Influenza). Published by the Maryland Cooperative Extension Service in Emergency Management and AgroSecurity. Available at http://www.agnr.umd.edu/HotTopics/AvianInfluenza/TP1.pdf.←
  30. Kuiken, T., F. A. Leighton, R. A. M. Fouchier, J. W. LeDuc, J. S. M. Peiris, et. al., September 9, 2005. Pathogen Surveillance in Animals. Science. 309(5741):1680-1681. Available at http://www.sciencemag.org/cgi/reprint/309/5741/1680.pdf.←
  31. Lee, C. W., D. E. Swayne, J. A. Linares, D. A. Senne, and D. L. Suarez, July-August 2005. H5N2 Avian Influenza Outbreak in Texas in 2004: The First Highly Pathogenic Strain in the United States in 20 Years? J Virol. 79(17):11412-11421. Available at http://jvi.asm.org/cgi/reprint/79/17/11412.←
  32. Li, K. S., Y. Guan, J. Wang, G. J. D. Smith, K. M. Xu, et. al., July 2004. Genesis of a Highly Pathogenic and Potentially Pandemic H5N1 Influenza Virus in Eastern Asia. Nature. 430:209-213. Available at http://www.nature.com/nature/journal/v430/n6996/pdf/nature02746.pdf.
  33. Monke, J., May 14, 2004. Avian Influenza: Multiple Strains Cause Different Effects Worldwide. CRS Report for Congress, Order Code RS21747. Available at http://usinfo.state.gov/gi/img/assets/5096/crs_bird_flu_may_2004.pdf.
  34. Normile, D., October 21, 2005. Are Wild Birds to Blame? Science. 310(5747):426-428. Available at http://www.sciencemag.org/cgi/reprint/310/5747/426.pdf.←
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