2 All flu viruses in fact emanate: See, for instance, R. J. Webby and R. G. Webster, “Emergence of Influenza A Viruses,” Philosophical Transactions of the Royal Society of London B: Biological Sciences, 356, no. 1416 (Dec. 29, 2001): 1817-28.
6 a repeat of the Great Influenza: For a definitive account of the 1918 pandemic, see John M. Barry, The Great Influenza: The Epic Story of the Deadliest Plague in History (Viking Penguin: New York, 2004). See also Alfred W. Crosby, America’s Forgotten Pandemic: The Influenza of 1918, 2nd ed. (New York: Cambridge University Press, 2003).
6 at least 50 million lives: N. P. Johnson and J. Mueller, “Updating the Accounts: Global Mortality of the 1918-1920 ‘Spanish’ Influenza Pandemic,” Bulletin of the History of Medicine 76, no. 1 (Spring 2002): 105-15.
7 “accelerated number of near-misses”: Anita Manning, “New, Deadly Flu Pandemic ‘Inevitable,’ Experts Warn,” USA Today, Mar. 2, 2004.
7 theater of conflict that is Asia: Dr. Michael T. Osterholm of the University of Minnesota has called Asia “the genetic roulette table for H5N1 mutations.”
7 first documented global outbreak: C. W. Potter, “A History of Influenza,” Journal of Applied Microbiology 91 (2001): 572-79.
7 since the twelfth century: August Hirsch, Handbook of Geographical and Historical Pathology (London: New Sydenham Society, 1883).
This chapter draws on interviews with disease specialists from the World Health Organization and the U.S. Centers for Disease Control and Prevention, officials from the governments of Indonesia, North Sumatra province, and Karo district, and medical professionals and residents in North Sumatra province, as well as internal documents from WHO and the governments of Indonesia, North Sumatra, and Karo.
13 cruise ships in Alaska: An account of the investigation can be found in Timothy M. Uyeki et al., “Large Summertime Influenza A Outbreak Among Tourists in Alaska and the Yukon Territory,” Clinical Infectious Diseases 36 (2003): 1095-1102.
13 island nation of Madagascar: Accounts of the investigation into the outbreak can be found in “Influenza Outbreak—July-August 2002,” Morbidity and Mortality Weekly Report, 51, no. 45 (Nov. 15, 2002): 1016-18; and Weekly Epidemiological Record 2002, no. 46 (Nov. 15, 2002): 77, 381-88.
18 At Imperial College London: Neil M. Ferguson et al., “Strategies for Containing an Emerging Influenza Epidemic in Southeast Asia,” Nature 437 (Sept. 8, 2005): 209-14.
18 A separate team: Ira M. Longini Jr. et al., “Containing Pandemic Influenza at the Source,” Science 309, no. 5737 (Aug. 12, 2005): 1083-87.
19 “No attempt has ever been made”: “WHO Activities in Avian Influenza and Pandemic Influenza Activities, WHO, Jan.-Dec. 2006, 16. The approach was quickly embodied in WHO planning. See “WHO Pandemic Influenza Draft Protocol for Rapid Response and Containment,” updated draft, WHO, May 30, 2006.
19 WHO’s emergency containment plan: The strategy is described in the finalized WHO protocol. See WHO, “WHO Interim Protocol: Rapid Operations to Contain the Initial Emergence of Pandemic Influenza,” updated Oct. 2007.
20 “It will require excellent surveillance”: WHO, “WHO Activities in Avian Influenza and Pandemic Influenza Activities: January-December 2006,” p. 16.
25 by the time Puji was buried: A local account of the cases and grassroots response is “Report Regarding Bird Flu Disease in Karo Regency, from the Karo Regent Daulat Daniel Sinulingga to the Governor of North Sumatra in Medan, Kabanjahe,” May 31, 2006.
28 According to Batak lore: Interview with Juara Ginting, an anthropologist who grew up in Karo district and studied Batak belief and superstition at North Sumatra University before pursuing a master’s degree at Leiden University in the Netherlands.
29 beheaded a chicken: Margie Mason, “Officials Backtrack Bird Flu Cluster,” Associated Press, May 26, 2005.
29 scores of poultry traders: Jason Gale and Karima Anjani, “Indonesian Bird-Flu Victim Sought Witchdoctor, Shunned Hospital,” Bloomberg, May 26, 2005.
29 “significantly delayed”: WHO, “Avian Influenza Cluster, Karo, North Sumatra, May 2006, WHO Interim Report.”
30 “universally refused”: Ibid.
38 senior Indonesian officials: See, for instance, Health Minister Siti Fadilah Supari, quoted in Tubagus Arie Rukmantara, “Awareness and Prevention Key in Bird Flu Fight,” Jakarta Post, July 28, 2006.
38 “From the lessening of the tension”: Siti Fadilah Supari, It’s Time for the World to Change: In the Spirit of Dignity, Equity, and Transparency, Divine Hand Behind Avian Influenza (Jakarta: Sulaksana Watinsa Indonesia, 2008), 23.
38 Supari would continue: See, for example, “Minister Denies Bird Flu in RI Spreading by Human-to-Human Transmission,” Antara news agency, Sept. 3, 2007.
38 were quickly convinced: Georg Petersen, “Investigative Report of a Cluster of Human Avian Influenza Cases, North Sumatra, May 2006,” WHO.
39 “If he turns out to be positive”: Internal WHO communication from Jakarta, May 21, 2006.
39 “In response to the possibility”: Ibid.
40 tested positive for the virus: The specimens collected by Uyeki and his colleagues later showed that the virus had been aggressively mutating as it moved from son to father. See, for example, Santoso Soroeso, “Epidemiology and Clinical Features of Avian Influenza in Indonesia, Questions and Lessons Learnt,” presented at Australia-Indonesia Symposium in Science and Technology 2006, Sept. 13-14, 2006, Jakarta; and also Declan Butler, “Family Tragedy Spotlights Flu Mutations,” Nature 442 (July 13, 2006): 114-15. Initial analysis of the specimens at Hong Kong University also showed that Dowes’s sample had the same signature mutation as the sample from his son. This seemed to be further evidence that Dowes caught the virus from his son, marking the third generation of transmission. This finding was reported at the time by several media and cited by U.S. Secretary of Health and Human Services Michael O. Leavitt. See, for example, Department of Health and Human Services, Pandemic Planning Update II, a report from Secretary Michael O. Leavitt, June 29, 2006. But researchers familiar with the results later said the initial findings regarding a signature mutation were not as conclusive as at first thought. The case for third-generation spread still rests on the case histories of the Ginting family members and the timing of their illnesses.
42 also onto a third: Politics long prevented researchers from publishing their analysis of human-to-human-to-human spread in the Sumatra cluster. But half a year later, another instance of third-generation transmission was confirmed in Pakistan and later described in a publication. See: “Human Cases of Avian influenza A (H5N1) in North-West Frontier Province, Pakistan, October-November 2007,” Weekly Epidemiological Record, no. 40 (October 3, 2008): 359-64.
This chapter draws on interviews with current and former public health, infectious-disease, and laboratory specialists at the Hong Kong Department of Health and the CDC, as well as animal health researchers in Hong Kong and the United States.
45 a three-year-old boy: The case is described in J. C. de Jong et al., “A Pandemic Warning?” Nature 389, no. 6651 (Oct. 9, 1997): 554; and in Kanta Subbarao et al., “Characterization of an Avian Influenza A (H5N1) Virus Isolated from a Child with a Fatal Respiratory Disease,” Science 279, no. 5349 (Jan. 16, 1998): 393-96.
48 far more than a runny nose and chills: A thorough overview of the clinical spectrum is provided in J. S. Malik Peiris, Menno D. de Jong, and Yi Guan, “Avian Influenza Virus (H5N1): A Threat to Human Health,” Clinical Microbiology Review 20, no. 2 (Apr. 2007): 243-67; and in K. Y. Yuen and S. S. Y. Wong, “Human Infection by Avian Influenza A H5N1,” Hong Kong Medical Journal 11, no. 3 (June 2005): 189-99. WHO has described the symptoms and clinical course of the disease in reports by the agency’s writing committee. See Writing Committee of the Second World Health Organization Consultation on Clinical Aspects of Human Infection with Avian Influenza A (H5N1) Virus, “Update on Avian Influenza A (H5N1) Virus Infection in Humans,” NEJM 358 no. 3 (Jan. 17, 2008): 261-73. The cases in individual countries have also been surveyed and described. See, for example, Hongjie Yu et al., “Clinical Characteristics of 26 Human Cases of Highly Pathogenic Avian Influenza A (H5N1) Virus Infection in China,” PLoS One 3, no. 8 (Aug. 21, 2008): e2985; and Sardikin Giriputro et al., “Clinical and Epidemiological Features of Patients with Confirmed Avian Influenza Presenting to Sulianti Saroso Infectious Diseases Hospital, 2005- 2007,” Annals of the Academy of Medicine (Singapore) 37 (2008): 454-57.
49 a counterattack so furious: This aggressive response has been much discussed. The following is a sampling of the research: M. C. W. Chan et al., “Proinflammatory Cytokine Responses Induced by Influenza A (H5N1) Viruses in Primary Human Alveolar and Bronchial Epithelial Cells,” Respiratory Research 6 (Nov. 11, 2005): 135; C. Y. Cheung et al., “Induction of Proinflammatory Cytokines in Human Macrophages by Influenza A (H5N1) Viruses: A Mechanism for the Unusual Severity of Human Disease?” Lancet 360, no. 9348 (Dec. 7, 2002): 1831-37; Menno D. de Jong et al., “Fatal Outcome of Human Influenza A (H5N1) Is Associated with High Viral Load and Hypercytokinemia,” Nature Medicine 12, no. 10 (Oct. 2006): 1203-07; J. S. Malik Peiris et al., “Re-emergence of Fatal Human Influenza A Subtype H5N1 Disease,” Lancet 363, no. 9409 (Feb. 21, 2004): 617-19; Ka-Fai To et al., “Pathology of Fatal Human Infection Associated with Avian Influenza A H5N1 Virus,” Journal of Medical Virology 63 (2001): 242-46; and Jianfang Zhou et al., “Differential Expression of Chemokines and Their Receptors in Adult and Neonatal Macrophages Infected with Human or Avian Influenza Viruses,” Journal of Infectious Diseases 194 (2006): 61-70.
50 inviting a suicidal counterattack: There has been debate about whether the immune response or the virus itself is more directly responsible for death. See, for instance, Kristy J. Szretter et al., “Role of Host Cytokine Responses in the Pathogenesis of Avian H5N1 Influenza Viruses in Mice,” Journal of Virology 81, no. 6 (Mar. 2007): 2736-44; and Rachelle Salomon, Erich Hoffman, and Robert G. Webster, “Inhibition of the Cytokine Response Does Not Protect Against Lethal H5N1 Influenza Infection,” PNAS 104, no. 30 (July 24, 2007): 12479-81.
50 enters the human body: For an overview of how the microbe operates, see J. S. Malik Peiris, Menno D. de Jong, and Yi Guan, “Avian Influenza Virus (H5N1): A Threat to Human Health,” Clinical Microbiology Review 20, no. 2 (Apr. 2007): 243-67; and R. G. Webster and D. J. Hulse, “Microbial Adaption and Change: Avian Influenza,” Revue Scientifique et Technique, Office International des Épizooties 23, no. 2 (2004): 453-65.
52 receptors in the human respiratory tract: There has also been extensive discussion about the preferences that different strains have for human and avian receptors and the crucial role these play in transmission. The following is a sampling of the research: Susan J. Baigent and John W. McCauley, “Influenza Type A in Humans, Mammals and Birds: Determinants of Virus Virulence, Host-Range and Interspecies Transmission,” BioEssays 25, no. 7 (2003): 657-71; Aarthi Chandrasekaran et al., “Glycan Topology Determines Human Adaptation of Avian H5N1 Virus Hemagglutinin,” Nature Biotechnology 26, no. 1 (Jan. 2008): 107-13; A. Gambaryan et al., “Evolution of the Receptor Binding Phenotype of Influenza A (H5) Viruses,” Virology 344, no. 2 (Jan. 20, 2006): 432-38; Thijs Kuiken et al., “Host Species Barriers to Influenza Virus Infections,” Science 312, no. 5772 (Apr. 21, 2006): 394-97; Masato Hatta et al., “Growth of H5N1 Influenza A Viruses in the Upper Respiratory Tracts of Mice,” PLoS Pathogens 3, no. 10 (Oct. 2007): 1374-79; John M. Nicholls et al., “Sialic Acid Receptor Detection in the Human Respiratory Tract: Evidence for Widespread Distribution of Potential Binding Sites for Human and Avian Influenza Viruses,” Respiratory Research 8 (2007): 73; J. M. Nicholls et al., “Tropism of Avian Influenza A (H5N1) in the Upper and Lower Respiratory Tract,” Nature Medicine 13 (2007): 147-49; Kyoko Shinya et al., “Influenza Virus Receptors in the Human Airway,” Nature 440 (Mar. 23, 2006): 435-36; Debby van Riel et al., “H5N1 Virus Attachment to Lower Respiratory Tract,” Science 312, no. 5772 (Apr. 23, 2006): 399; Terrence M. Tumpey et al., “A Two-Amino Acid Change in the Hemagglutinin of the 1918 Influenza Virus Abolishes Transmission,” Science 315, no. 5812 (Feb. 2, 2007): 655-59; Shinya Yamada et al., “Haemagglutinin Mutations Responsible for the Binding of H5N1 Influenza A Viruses to Human-type Receptors,” Nature 444 (Nov. 16, 2006): 378-82 and Influenza Research at the Human and Animal Interface: Report of a WHO Working Group, WHO, Geneva, Sept. 21-22, 2006.
52 a few other genetic tweaks: For discussion of possible changes in viral proteins that can lead to an avian virus attacking humans and becoming more lethal, see Christopher F. Basler and Patricia V. Aguilar, “Progress in Identifying Virulence Determinants of the 1918 H1N1 and the Southeast Asian H5N1 Influenza A Viruses,” Antiviral Research 79 (2008): 166-78; Andrea Gambotto et al., “Human Infection with Highly Pathogenic H5N1 Influenza Virus,” Lancet 371, no. 9622 (Apr. 26, 2008): 1464-75; and Neal Van Hoeven et al., “Human HA and Polymerase Subunit PB2 Proteins Confer Transmission of an Avian Influenza Virus Through Air,” PNAS, published online before print February 11, 2009, doi: 10.1073/pnas.0813172106.
55 Growing up in Hong Kong: Miriam Shuchman, “Improving Global Health—Margaret Chan at the WHO,” NEJM 356, no. 7 (Feb. 15, 2007): 653-56; and Lawrence K. Altman, “Her Job: Helping Save the World from Bird Flu,” New York Times, Aug. 9, 2005.
56 a baffling plague: On the connection between Hoi-ka’s case with the earlier poultry outbreak, see Eric C. J. Claas et al., “Human Influenza A H5N1 Virus Related to a Highly Pathogenic Avian Influenza Virus,” Lancet 351, no. 9101 (Feb. 14, 1998): 472-77; and David L. Suarez et al., “Comparisons of Highly Virulent H5N1 Influenza A Viruses Isolated from Humans and Chickens from Hong Kong,” Journal of Virology 72, no. 8 (Aug. 1998): 6678-88.
58 The Spanish flu: For a scientific investigation of the 1918 pandemic, see Jeffrey K. Taubenberger and David M. Morens, “1918 Influenza: The Mother of All Pandemics,” Emerging Infectious Diseases 12, no. 1 (Jan. 2006): 15-22.
58 two subsequent pandemics: On flu pandemics of the last century, see Edwin D. Kilbourne, “Influenza Pandemics of the 20th Century,” Emerging Infectious Diseases 12, no. 1 (Jan. 2006): 9-14. WHO estimates that the 1957 pandemic killed two million and the 1968 pandemic one million.
60 If two different flu strains: For a discussion of the compatibility of genes from H5N1 and human viruses, see Li-Mei Chen et al., “Genetic compatibility and Virulence of Reassortants Derived from Contemporary Avian H5N1 and Human H3N2 Influenza A Viruses,” PLoS Pathogens 4, no. 5: e1000072.
60 the recent, seemingly improbable encounter: For early discussions of the H1N1 swine flu virus, see Rebecca J. Garten et al., “Antigenic and Genetic Characteristics of Swine-Origin 2009 A (H1N1) Influenza Viruses Circulating in Humans,” Science, published online before print May 22, 2009, doi: 10.1126/ science.1176225; Novel Swine-Origin Influenza A (H1N1) Virus Investigation Team, “Emergence of a Novel Swine-Origin Influenza A (H1N1) Virus in Humans,” NEJM, published online before print May 7, 2009, doi: 10.1056/ NEJMoa0903810; and Robert B. Belshe, “Implications of the Emergence of a Novel H1 Influenza Virus,” NEJM, published online before print May 7, 2009, doi: 10.1056/NEJMe0903995. On the triple reassortant virus, see Vivek Shinde, et al., “Triple-reassortant swine influenza A (H1) in Humans in the United States, 2005-2009,” NEJM, published online before print May 7, 2009, doi: 10.1056/NEJMoa0903812.
60 even infecting mammals: See, for example, Juthatip Keawcharoen et al., “Avian Influenza H5N1 in Tigers and Leopards,” Emerging Infectious Diseases 10, no. 12 (Dec. 2004): 2189-91; and Guus F. Rimmelzwaan et al., “Influenza A Virus (H5N1) Infection in Cats Causes Systemic Disease with Potential Novel Routes of Virus Spread Within and Between Hosts,” American Journal of Pathology 168, no. 1 (Jan. 2006): 176-83.
60 The dice were being rolled: Alice Croisier et al., “Highly Pathogenic Avian Influenza A (H5N1) and Risks to Human Health,” Background Paper at the Technical Meeting on Highly Pathogenic Avian Influenza and Human H5N1 Infection, June 27-29, 2007, Rome.
60 “appear out of control”: I. Capua and S. Marangon, “Control and Prevention of Avian Influenza in an Evolving Scenario,” Vaccine 25, no. 30 (July 26, 2007): 5645-52.
60 it returns: Antonio Petrini, “Global Situation: HPAI Outbreaks in Poultry—A Synthesis of Country Reports to the OIE,” Background Paper at the Technical Meeting on Highly Pathogenic Avian Influenza and Human H5N1 Infection, June 27-29, 2007, Rome.
60 “a distant and unlikely prospect”: Joseph Domenech et al., “Trends of Dynamics of HPAI—Epidemiological and Animal Health Risks,” Background Paper at the Technical Meeting on Highly Pathogenic Avian Influenza and Human H5N1 Infection, June 27-29, 2007, Rome.
60 not the only avian virus menacing humanity: J. S. Malik Peiris, Menno D. de Jong, and Yi Guan, “Avian Influenza Virus (H5N1): A Threat to Human Health,” Clinical Microbiology Review 20, no. 2 (April 2007): 243-67.
60 avian strain called H9N2: K. M. Xu et al., “Evolution and Molecular Epidemiology of H9N2 Influenza A Viruses from Quail in Southern China, 2000 to 2005,” Journal of Virology 81, no. 6 (Mar. 2007): 2635-45; and K. M. Xu et al., “The Genesis and Evolution of H9N2 Influenza Viruses in Poultry from Southern China, 2000 to 2005,” Journal of Virology 81 no. 19 (Oct. 2007): 10389-10401.
61 “The establishment and prevalence”: Hongquan Wan et al., “Replication and Transmission of H9N2 Influenza Viruses in Ferrets: Evaluation of Pandemic Potential,” PLoS One 3, no. 8 (Aug. 2008): e2923.
61 “continued surveillance and study”: Jessica A. Belser et al., “Contemporary North American Influenza H7 Viruses Possess Human Receptor Specificity: Implications for Virus Transmissibility,” PNAS 105 no. 21 (May 27, 2008): 7558-63.
61 Some medical scholars dissent: Dennis Normile, “Avian Influenza: Pandemic Skeptics Warn Against Crying Wolf,” Science 310, no. 5751 (Nov. 18, 2005): 1112-13; and Declan Butler, “Yes, But Will It Jump?” Nature 439, no. 12 (Jan. 2006): 124-25.
62 “Such complacency”: Robert G. Webster et al., “H5N1 Outbreaks and Enzootic Influenza,” Emerging Infectious Diseases 12, no. 1 (Jan. 2006): 3-8.
62 “The virus has evolved”: Remarks in a speech tape for Business Preparedness for Pandemic Influenza, Second Annual Summit, sponsored by the University of Minnesota Center for Infectious Disease Research and Policy, Feb. 5, 2007.
62 “If you put a burglar”: Margaret Chan, “Pandemics: Working Together for an Effective and Equitable Response,” address to the Pacific Health Summit, Seattle, June 13, 2007.
66 “There’s a possibility”: Cindy Sui, “Hospital Staff Ill After Treating Bird Flu Victims,” Hong Kong Standard, Dec. 8, 1997.
66 reached double digits: For a clinical discussion of the Hong Kong cases, see K. Y. Yuen et al., “Clinical Features and Rapid Viral Diagnosis of Human Disease Associated with Avian Influenza A H5N1 Virus,” Lancet 351, no. 9101 (Feb. 14, 1998): 467-71; and Paul K. S. Chan, “Outbreak of Avian Influenza A (H5N1) Virus Infection in Hong Kong in 1997,” Clinical Infectious Diseases 34 (2002): S58-S64.
68 The parallels were eerie: David M. Morens and Anthony S. Fauci, “The 1918 Influenza Pandemic: Insights for the 21st Century,” Journal of Infectious Diseases 195 (2007): 1018-28; Jeffrey K. Taubenberger, “The Origin and Virulence of the 1918 ‘Spanish’ Influenza Virus,” Proceedings of the American Philosophical Society 150, no. 1 (Mar. 2006); Jeffrey K. Taubenberger and David M. Morens, “1918 Influenza: The Mother of All Pandemics,” Emerging Infectious Diseases 12, no. 1 (Jan. 2006): 15-22; and L. Simonsen et al., “Pandemic Versus Epidemic Influenza Mortality: A Pattern of Changing Age Distribution,” Journal of Infectious Diseases 178, no. 1 (July 1998): 53-60.
68 this disquieting pattern: “Epidemiology of WHO-Confirmed Human Cases of Avian Influenza A (H5N1) Infection,” Weekly Epidemiological Record 81, no. 26 (June 30, 2006): 249-57; and “Update: WHO-Confirmed Human Cases of Avian Influenza A (H5N1) Infection, 25 November 2003-24 November 2006,” Weekly Epidemiological Record, 82, no. 6 (Feb. 9, 2007): 41-47.
68 “most important unsolved mystery”: David M. Morens and Anthony S. Fauci, “The 1918 Influenza Pandemic: Insights for the 21st Century,” Journal of Infectious Diseases 195 (2007): 1018-28.
69 tremendous cytokine storms: See, for example, John C. Kash, et al., “Genomic Analysis of Increased Host Immune and Cell Death Responses Induced by 1918 Influenza Virus,” Nature 443 (Oct. 5, 2006): 578-81; Darwyn Kobasa et al., “Enhanced Virulence of Influenza A Viruses with the Hemagglutinin of the 1918 Pandemic Virus,” Nature 431, no. 7009 (Oct. 7, 2004): 703-7; and Darwyn Kobasa et al., “Aberrant Innate Immune Response in Lethal Infection of Ma caques with the 1918 Influenza Virus,” Nature 445 (Jan. 18, 2007): 319-23. A study in 2008 comparing the immune response to H5N1 and the 1918 virus in mice showed “considerable similarities” but found that the H5N1 strain actually elicited significantly higher levels of cytokines and macrophages. See Lucy A. Perrone et al., “H5N1 and 1918 Pandemic Influenza Virus Infection Results in Early and Excessive Infiltration of Macrophages and Neutrophils in the Lungs of Mice,” PLoS Pathogens 4, no. 8 (2008): e1000115.
69 “kissing cousin”: Remarks at Business Preparedness for Pandemic Influenza, Second Annual Summit, University of Minnesota Center for Infectious Disease Research and Policy, Feb. 5, 2007.
69 a wholly avian virus: Jeffrey K. Taubenberger et al., “Characterization of the 1918 Influenza Virus Polymerase Genes,” Nature 437 (Oct. 6, 2005): 889-93; and Terrence M. Tumpey et al., “Characterization of the Reconstructed 1918 Spanish Influenza Pandemic Virus,” Science 310, no. 5745 (Oct. 7, 2005): 77-80.
69 “a number of the same changes”: Jeffrey K. Taubenberger et al., “Characterization of the 1918 Influenza Virus Polymerase Genes,” Nature 437 (Oct. 6, 2005): 889-93.
69 more like the Spanish flu strain: For example, see James Stevens et al., “Structure and Receptor Specificity of the Hemagglutinin from an H5N1 Influenza Virus,” Science 312, no. 5772 (Apr. 21, 2006): 404-10.
69 A series of studies: H. Chen et al., “The Evolution of H5N1 Influenza Viruses in Ducks in Southern China,” PNAS 101, no. 28 (July 13, 2004): 10452-57; Taronna R. Maines et al., “Avian Influenza (H5N1) Viruses Isolated from Humans in Asia in 2004 Exhibit Increased Virulence in Mammals,” Journal of Virology 79, no. 18 (Sept. 2005): 11788-11800; Hui-Ling Yen et al., “Virulence May Determine the Necessary Duration and Dosage of Oseltamivir Treatment for Highly Pathogenic A/Vietnam/1203/04 Influenza Virus in Mice,” Journal of Infectious Diseases 192 (2005): 665-72; and Adrianus C. M. Boon et al., “Role of Terrestrial Wild Birds in Ecology of Influenza A Virus (H5N1),” Emerging Infectious Diseases 13, no. 11 (Nov. 2007): 1720-24.
69 “a process of rapid evolution”: “Mouse Studies of Oseltamivir Show Promise Against H5N1 Influenza Virus,” NIH News, July 18, 2005.
69 already become more ferocious: Carole R. Baskin et al., “Early and Sustained Innate Immune Response Defines Pathology and Death in Nonhuman Primates Infected by Highly Pathogenic Influenza Virus,” PNAS, Published online before print February 13, 2009, doi 10.1073/pnas.0813234106.
70 If the virus continued to develop: J. S. Malik Peiris, “H5N1 Pathogenesis in Humans: An Update,” Power Point presentation to the WHO working group, Sept. 21-22, 2006.
70 though later reported : WHO, “Influenza Research at the Human and Animal Interface: Report of a WHO Working Group,” Geneva, September 21-22, 2006.
70 62 million: Christopher J. L. Murray et al., “Estimation of Potential Global Pandemic Influenza Mortality on the Basis of Vital Registry Data from the 1918- 1920 Pandemic: A Quantitative Analysis,” Lancet 368, no. 9554 (Dec. 23, 2006): 2211-18.
70 $3.13 trillion during the first year: The figures for severe, mild, and moderate pandemics are based on numbers included in Andrew Burns, Dominique van der Mensbrugghe, and Hans Timmer, “Evaluating the Economic Consequences of Avian Influenza,” updated in September 2008. An earlier version of this report, which had calculated the costs using a lower figure for global GDP, put the toll of a severe pandemic at $2.38 trillion. The study was originally published in a slightly different form in the World Bank’s June 2006 edition of Global Development Finance. For further discussion, see Milan Brahmbatt, “Economic Impacts of Avian Influenza Propagation,” speech at the First International Conference on Avian Influenza in Humans, June 29, 2006.
71 “It’s a possibility in this case”: Jane Moir, “Cousins of Child Victim in Flu Alert: Human Transmission Suspected,” South China Morning Post, Dec. 17, 1997.
71 “They live together at Grandma’s”: Edward A. Gargan, “Chicken-Borne Flu Virus Puts Hong Kong on Alert,” New York Times, Dec. 17, 1997.
71 “working at breakneck pace”: Jane Moir, “Cousins of Child Victim in Flu Alert: Human Transmission Suspected,” South China Morning Post, Dec. 17, 1997.
71 barely three hundred square feet: Rhonda Lam Wan, “Bird Flu Cousins’ Flat Behind Pile of Rubbish,” South China Morning Post, Dec. 19, 1997.
71 they were rebuffed: Ibid.
72 a city under siege: See, for example, the following accounts, all from the South China Morning Post: Rhonda Lam Wan and Billy Wong Wai-Yuk, “Doctors Scramble for Special Drug,” Dec. 13, 1997; Andrea Li and Alex Lo, “Fears Force Changes to Menus,” Dec. 16, 1997; Stella Lee, “18 Private Doctors to Join Bird Flu Probe,” Dec. 18, 1997; Rhonda Lam Wan, “Flood of Requests Prompts Promise of A-Strain Testing,” Dec. 20, 1997; and Ng Kang-Chung, “Rush for Bird Flu Tests As Seven More Suspected Victims Found,” Dec. 26, 1997.
73 Fukuda had never before missed: Patricia Guthrie, “Focus on Hong Kong Flu,” Atlanta Journal and Constitution, Dec. 25, 1997.
73 “will stop or spread”: “Hong Kong Tests Show Human-to-Human Transmission of Bird Flu Difficult,” Agence France Presse, Dec. 27, 1997.
73 “measures are sufficient”: Keith B. Richburg, “Hong Kong Killing All Chickens in Fight Against ‘Bird Flu’ Virus,” Washington Post, Dec. 29, 1997.
73 more bad news: For discussion of the poultry outbreaks in late December 1997, see L. D. Sims et al., “Avian Influenza in Hong Kong 1997-2002,” Avian Diseases 47, no. s3 (2003): 832-38; and Kennedy F. Shortridge, “Poultry and the Influenza H5N1 Outbreak in Hong Kong, 1997: Abridged Chronology and Virus Isolation,” Vaccine 17 (1999): s26-s29.
75 would kill every last chicken: For an overview of the 1997 poultry outbreaks and government response, see Kennedy F. Shortridge et al., “Interspecies Transmission of Influenza Viruses: H5N1 Virus and a Hong Kong SAR Perspective,” Veterinary Microbiology 74 (2000): 141-47.
75 The government pressed: Robin Ajello and Catherine Shepherd, “The Flu Fighters,” Asiaweek, Jan. 2008.
75 bloody chaos: Billy Wong Wai-Yuk, “Tears of Anger, Rivers of Blood,” South China Morning Post, Dec. 30, 1997; Stella Lee, “Slaughter Held Up by Inexperience,” South China Morning Post, Dec. 31, 1997; Keith B. Richburg, “Chicken Sightings Frighten Hong Kong, Washington Post, Jan. 3, 1998; and Keith B. Richburg, “Hong Kong Faulted on Handling of ‘Bird Flu’ Crisis, Washington Post, Jan. 4, 1998.
76 On the third day of the slaughter: “Tung Handling of Flu Crisis Attacked,” South China Morning Post, Jan. 1, 1998.
76 In a front-page editorial: “Only Time Will Prove Wisdom of Dramatic Move,” South China Morning Post, Dec. 29, 1997.
76 the “botched” operation: “Taking Charge,” South China Morning Post, Jan. 3, 1998.
76 nearly 350 chickens: Kennedy F. Shortridge, “Poultry and the Influenza H5N1 Outbreak in Hong Kong, 1997: Abridged Chronology and Virus Isolation,” Vaccine 17 (1999): s26-s29.
76 more widespread than expected: Kennedy F. Shortridge et al., “Characterization of Avian H5N1 Influenza Viruses from Poultry in Hong Kong,” Virology 252, no. 2 (Dec. 20, 1998): 331-42.
77 a pandemic had been averted: Kennedy F. Shortridge, J. S. Malik Peiris, and Yi Guan, “The Next Influenza Pandemic: Lessons from Hong Kong,” Journal of Applied Microbiology 94 (2003): 70S-79S.
77 its most successful: Several researchers have held up Hong Kong as the model. See, for example, Robert Webster and Diane Hulse, “Controlling Avian Flu at the Source,” Nature 435 (May 26, 2005): 415-16. Yet the model may be hard to apply elsewhere. See Les Sims, “Achievements, Issues and Options on Strategies for HPAI Control and Prevention,” Background Paper at the Technical Meeting on Highly Pathogenic Avian Influenza and Human H5N1 Infection, June 27-29, 2007, Rome.
78 Their main exposure: Anthony W. Mounts et al., “Case-Control Study of Risk Factors for Avian Influenza A (H5N1) Disease, Hong Kong, 1997,” Journal of Infectious Diseases 180 (1999): 505-8.
78 would resurface in 2001: On this outbreak and Hong Kong’s response, see Yi Guan et al., “Emergence of Multiple Genotypes of H5N1 Avian Influenza Viruses in Hong Kong SAR,” PNAS 99, no. 13 (June 25, 2002): 8950-55; and N. Y. Kung et al., “The Impact of a Monthly Rest Day on Avian Influenza Virus Isolation Rates in Retail Live Poultry Markets in Hong Kong,” Avian Diseases 47 (2003): 1037-41.
78 the virus struck yet again: For an overview of the poultry outbreaks in 2001- 2002, see L. D. Sims et al., “Avian Influenza in Hong Kong 1997-2002,” Avian Diseases 47, no. s3: 832-38; L. D. Sims et al., “An Update on Avian Influenza in Hong Kong 2002,” Avian Diseases 47 (2003): 1083-86; and Kennedy F. Shortridge, J. S. Malik Peiris, and Yi Guan, “The Next Influenza Pandemic: Lessons from Hong Kong,” Journal of Applied Microbiology 94 (2003): 70S-79S.
This chapter draws on interviews with WHO infectious disease specialists and other officials in both Geneva and Asia, public health officials and medical professionals in Thailand, and internal documents from WHO.
81 “Influenza has been an epidemic illness”: Prasert Thongcharoen, Influenza (Bangkok: Mahidol University, 1998).
82 blame the spiraling death toll on the weather: Newin Chidchob, deputy agriculture minister, is quoted in “Thailand Declared Free of Bird Flu,” Nation (Thailand), Jan. 15, 2004. Yukol Limlamthong, director-general of the Livestock Department, is quoted in “Bird Flu: Govt to Sue over ‘False Report,’” Nation (Thailand), Jan. 17, 2004.
85 researchers had confirmed: Arthit Khwankhom and Sirinart Sirisunthorn, “Govt Ignored Chula Warning,” Nation (Thailand), Jan. 30, 2004.
86 “We were fighting”: “What Happened When the H5N1 Virus Visited Thailand,” lecture at the Asia Medical Forum, Lancet 2006, Singapore, May 4, 2006.
87 “Irresponsible media”: Tini Tran, “WHO Says SARS Helped Asia Prepare for Bird Flu; Poultry Culls Continue,” Associated Press, Jan. 16, 2004.
87 “There’s absolutely no evidence”: Alisa Tang, “Thai Cabinet Seeks to Boost Confidence of Chicken-Wary Public,” Associated Press, Jan. 19, 2004.
88 a confidential tip: Internal WHO report, Jan. 20, 2004.
90 broader resurgence of infectious disease: For an excellent exploration of what was optimistically called the Health Transition and subsequent setbacks, see Laurie Garrett, The Coming Plague (Penguin: New York, 1995).
91 Storm clouds were gathering: See, for example, David L. Heymann and Guenael R. Rodier, “Hot Spots in a Wired World: WHO Surveillance of Emerging and Re-emerging Infectious Diseases.”
91 WHO’s rapid response: David L. Heymann and Guenael Rodier, “Global Surveillance, National Surveillance and SARS: Commentary,” Emerging Infectious Diseases 10, No. 2 (Feb. 1, 2004); and David L. Heymann, Mary Kay Kindhauser, and Guenael Rodier, “Coordinating the Global Response,” in SARS: How a Global Epidemic Was Stopped (Manila: WHO Western Pacific Regional Office, 2006).
93 Subsequent study: Kulkanya Chokephaibulkit et al., “A Child with Avian Influenza A (H5N1) Infection,” Pediatric Infectious Disease Journal 24, no. 2 (Feb. 2005): 162-66; and Mongkol Uipprasertkul et al., “Influenza A H5N1 Replication Sites in Humans,” Emerging Infectious Diseases 11, no. 7 (July 2005): 1036-41.
94 followed right behind: For a synopsis of Thailand’s experience with avian flu in 2004, see Thanawat Tiensin, et al., “Highly Pathogenic Avian Influenza H5N1, Thailand, 2004,” Emerging Infectious Diseases 11, no. 11 (Nov. 2005): 1664-72.
95 “It’s not a big deal”: Sutin Wannabovorn, “Thailand Confirms Two Human Cases of Bird Flu as Infection spreads Through Asia,” Associated Press, Jan 23, 2004.
97 teams were running short: Tipawayan Kwankhauw, “Anger and Tears as Thailand’s Farmers Cull Millions of Chickens,” Agence France Presse, Jan. 25, 2004.
100 mixing vessel: See, for instance, S. Scholtissek et al., “The Nucleoprotein as a Possible Major Factor in Determining Host Specificity of Influenza H3N2 Viruses,” Virology 147 (1985) 287-94; H. Kida et al., “Potential for Transmission of Avian Influenza Viruses to Pigs,” Journal of General Virology 75, no. 9 (Sept. 1994): 2183-88; and Ian H. Brown, “The Epidemiology and Evolution of Influenza Viruses in Pigs,” Veterinary Microbiology 74, nos. 1-2 (May 22, 2000): 29-46.
101 “Are the doctor and the media”: “PM Derides Doctor over Pig Comments,” Nation (Thailand), Jan. 28, 2004.
This chapter draws on interviews with current and former infectious-disease specialists, investigators, and other officials at WHO and CDC in the United States, Geneva, and Asia, with Vietnamese, Thai, and Hong Kong disease specialists, and on documents from WHO and CDC and personal notes kept by participants in the events described.
104 When SARS broke out: The results of the outbreak investigation in Vietnam are discussed in Hoang Thu Vu et al., “Clinical Description of a Completed Outbreak of SARS in Vietnam, February-May 2003,” Emerging Infectious Diseases 10, no. 2 (Feb. 2004): 334-38; and Mary G. Reynolds et al., “Factors Associated with Nosocomial SARS-CoV Transmission Among Healthcare Workers in Vietnam, 2003,” BMC Public Health 6 (2006): 207.
109 The flu outbreak that began that fall: For more discussion, see Niranjan Bhat et al., “Influenza-Associated Deaths Among Children in the United States, 2003-2004,” NEJM 353, no. 24 (Dec. 15, 2005): 2559-67; and Laura Jean Podewils et al., “A National Survey of Severe Influenza-Associated Complications Among Children and Adults, 2003-2004,” Clinical Infectious Diseases 40 (June 1, 2005):1693-96.
109 flooded with the infirm: See, for example, Rob Stein, “Shortage of Flu Shots Prompts Rationing,” Washington Post, Dec. 9, 2003; Rob Stein, “24 States Hit Hard by Flu Outbreak,” Washington Post, Dec. 12, 2003; and Anita Manning and Tom Kenworthy, “Flu and Fear Run Rampant,” USA Today, Dec. 10, 2003.
109 give up their beds: “Influenza: Last Bad Flu Season Killed Nearly 65,000; Will This Season Be Worse?” Drug Week, Jan. 2, 2004.
109 made its first recorded appearance: Alfred W. Crosby, America’s Forgotten Pandemic: The Influenza of 1918, 2nd ed. (New York: Cambridge University Press, 2003), 71.
109 sailors transferred days earlier: John M. Barry, The Great Influenza: The Epic Story of the Deadliest Plague in History (Viking Penguin: New York, 2004), 192.
110 Fourth Annual Liberty Loan parade:Philadelphia Inquirer, Sept. 29, 1918.
110 an old photograph:www.history.navy.mil/photos/images/h41000/h41730.jpg.
110 every hospital bed: Barry, Great Influenza, 220.
110 “When they got there”: Selma Epp, transcript of unaired interview for “Influenza 1918,” American Experience, Feb. 28, 1997, quoted in Barry.
110-11 “historic records of the plague”: Ellen C. Potter, letter to Miss M. Carey Thomas, Oct. 3, 1918, M. Carey Thomas Papers, Special Collections Department, Bryn Mawr College.
111 254 deaths in a single day: Barry, Great Influenza, 221.
111 daily toll was 759: Ibid., 329.
111 “none to replace them in the wards”: Francis Edward Tourscher, Work of the Sisters During the Epidemic of Influenza, October, 1918 (Philadelphia: American Catholic Historical Society, 1919), p. 18, accessed through Villanova University Digital Library Browser, reprinted from the Records of the American Catholic Historical Society of Philadelphia 30s, nos. 1-3 (Mar.-Sept. 1919).
111 Almost half the doctors and nurses: Barry, Great Influenza, 226.
111 “had no attention for over 18 hours”: Tourscher, Work of the Sisters, 18.
111 “After gasping for several hours”: Ira Starr, “Influenza in 1918: Recollections of the Epidemic in 1918,” Annals of Internal Medicine 145, no. 2 (July 18, 2006).
111 at the poorhouse: Tourscher, Work of the Sisters, 50.
112 the residence of a wealthy family: Ibid., 62.
112 cars bearing medical insignia: Starr, “Influenza in 1918.”
112 so they could help fill prescriptions: Eileen A. Lynch, “The Flu of 1918: It Started with a Cough in the Summer of 1918,” Pennsylvania Gazette, Nov. 1998.
112 Nearly 500 police officers:Philadelphia Inquirer, Oct. 20, 1918.
112 About 1,800 telephone employees: Barry, Great Influenza, 328.
112 “no other than absolutely necessary calls”:Philadelphia Inquirer, Oct. 18, 1918.
112 one Fishtown home: Tourscher, Work of the Sisters, 74.
112 During the second week: Great Britain Ministry of Health, Report on the Pandemic of Influenza 1918-1919, Reports on Public Health and Medical Subjects no. 4 (London: His Majesty’s Stationery Office, 1920), 319-20, quoted in Crosby, America’s Forgotten Pandemic.
112 abandoned corpses were stacked: “Emergency Service of the Pennsylvania Council of National Defense in the Influenza Crisis,” 35, quoted in Crosby, America’s Forgotten Pandemic.
113 piling up on the porches: Harriet Ferrell, transcript of unaired interview for “Influenza 1918,” American Experience, Feb. 28, 1997, quoted in Barry, Great Influenza.
113 “The smell would just knock you”: Interview by Charles Handy for WHYY-FM program “The Influenza Pandemic of 1918: Philadelphia, 1918.”
113 “They were taking people out”: Ibid.
113 “They had so many died”: Ibid.
113 dispatched a steam shovel: “Emergency Service of the Pennsylvania Council of National Defense in the Influenza Crisis,” 35, quoted in Crosby, America’s Forgotten Pandemic; and the Philadelphia Inquirer, Oct. 12, 1918.
113 people were stealing them: Michael Donohue, transcript of unaired interview for “Influenza 1918,” American Experience, Feb. 28, 1997, quoted in Barry, Great Influenza.
113 under armed guard: Barry, Great Influenza, 327.
113 12,897 Philadelphians: Great Britain Ministry of Health, Report on the Pandemic , 319-320, quoted in Crosby, America’s Forgotten Pandemic.
113 “It was the fear and dread”: Tourscher, Work of the Sisters, 105.
114 tremendous financial pressure: One-third of hospitals were reported to be operating at a deficit. See John G. Bartlett and Luciano Borio, “The Current Status of Planning for Pandemic Influenza and Implications for Health Care Planning in the United States,” Clinical Infectious Diseases 46 (Mar. 15, 2008): 919-25.
114 Hospitals have been closing: Neil A. Halpern, Stephen M. Pastores, and Robert J. Greenstein, “Critical Care Medicine in the United States 1985-2000: An Analysis of Bed Numbers, Use, and Costs,” Critical Care Medicine 32, no. 6 (June 2004): 1254-59. Between 1993 and 2003, the United States saw a net loss of 703 hospitals, or 11 percent, and a decline in inpatient beds of 198,000 or 17 percent. See American Hospital Association figures cited in Institute of Medicine, Hospital-Based Emergency Care: At the Breaking Point (Washington: National Academies Press, 2007), 38. Sixty percent of U.S. hospitals reported in 2001 that they were operating at or over capacity. See the Lewin Group, Emergency Department Overload: A Growing Crisis, the results of the AHA Survey of Emergency Department (ED) and Hospital Capacity.
114 vacant ICU beds were rare: Lewis Rubinson et al., “Augmentation of Hospital Critical Care Capacity After Bioterrorist Attacks or Epidemics: Recommendations of the Working Group on Emergency Mass Critical Care,” Critical Care Medicine 33, no. 10 (2005): 2392-2403. In a severe pandemic, the demand for these ICU beds could outstrip capacity by nearly five times. See Eric Toner et al., “Hospital Preparedness for Pandemic Influenza,” Biosecurity and Bioterrorism 4, no. 2 (2006): 207-14. Even in a moderately severe outbreak, half the states would run out of hospital beds within two weeks. See Trust for America’s Health, Ready or Not? Protecting the Public’s Health from Diseases, Disasters and Bioterrorism, Dec. 2006.
114 a severe nursing shortage: See Elizabeth Daugherty, Richard Branson, and Lewis Rubinson, “Mass Casualty Respiratory Failure,” Current Opinion in Critical Care 13, no. 1 (Feb. 2007): 51-56; Derek C. Angus et al., “Current and Projected Workforce Requirements for Care of the Critically Ill and Patients with Pulmonary Disease,” Journal of the American Medical Association 284, no. 21 (Dec. 6, 2000): 2762-70; Mark A. Kelley et al., “The Critical Care Crisis in the United States: A Report from the Profession,” Chest 125 (2004): 1514-17; Gary W. Ewart et al., “The Critical Care Medicine Crisis: A Call for Federal Action,” white paper from the Critical Care Professional Societies, Chest 125 (2004): 1518-21; and J. K. Stechmiller, “The Nursing Shortage in Acute and Critical Settings,” AACN Clinical Issues 13, no. 4 (Nov. 2002): 577-84. The nationwide shortage of nurses has been estimated at between 100,000 and 291,000. All but ten states had a shortage of registered nurses in 2006. See John G. Bartlett and Luciano Borio, “The Current Status of Planning for Pandemic Influenza and Implications for Health Care Planning in the United States,” Clinical Infectious Diseases 46 (Mar. 15, 2008): 919-25; and Trust for America’s Health, Ready or Not? Protecting the Public’s Health from Diseases, Disasters and Bioterrorism, Dec. 2006.
114 Emergency rooms are being shuttered: Eric W. Nawar, Richard W. Niska, and Jianmin Xu, “National Hospital Ambulatory Medical Care Survey: 2005 Emergency Department Summary,” advance data from Vital and Health Statistics, no. 386, June 29, 2007. For a comprehensive overview of the crisis facing U.S. emergency departments, see Institute of Medicine, Hospital-Based Emergency Care: At the Breaking Point (Washington: National Academies Press, 2007). According to figures from the American Hospital Association cited in the IOM report, the number of hospitals with emergency departments declined by 425 over the decade ending in 2003.
114 departments were routinely overcrowded: “State of Emergency Medicine: Emergency Physician Survey,” American College of Emergency Physicians, October 2003. Sixty-two percent of U.S. hospitals surveyed in 2001 said their emergency departments were operating at or over capacity. For large hospitals and those offering the most advanced trauma care, the percentage increased to about 90 percent. See the Lewin Group, Emergency Department Overload: A Growing Crisis, results of the AHA Survey of Emergency Department (ED) and Hospital Capacity, Apr. 2002. As the IOM writes, “In many cities, hospitals and trauma centers have problems dealing with a multiple-car highway crash, much less the volume of patients likely to result from a large-scale disaster.” Institute of Medicine, Hospital-Based Emergency Care, 265.
114 once every single minute: Catharine W. Burt, Linda F. McCaig, and Roberto H. Valverde, “Analysis of Ambulance Transports and Diversions Among U.S. Emergency Departments,” Annals of Emergency Medicine 47, no. 4 (2006): 317-26. See also Sally Phillips, “Current Status of Surge Research,” Academic Emergency Medicine 13 (2006): 1103-8.
114 hospital executives were too preoccupied: “Emergency Preparedness: States are Planning for Medical Surge, but Could Benefit from Shared Guidance for Allocating Scarce Medical Resources,” U.S. Government Accountability Office, June 2008.
114 decreased 18 percent: Ibid.
114 producers of medical oxygen: Michael D. Christian et al., “Definitive Care for the Critically Ill During a Disaster: Current Capabilities and Limitations,” Chest 133, no. 5 (May 2008): 8S-17S.
114 tremendous shortage of ventilators: Ibid.; and Isaac Weisfuse, “Summary Background on Hospital Pandemic Preparedness in NYC,” in Beth Maldin-Morgenthau et al., “Roundtable Discussion: Corporate Pandemic Preparedness,” Biosecurity and Bioterrorism: Biodefense Strategy, Practice, and Science 5, no. 2 (2007): 171.
115 about 740,000 people would require ventilation: “States are Planning for Medical Surge,” U.S. Government Accountability Office, June 2008.
115 between 53,000 and 105,000: Michael T. Osterholm, “Preparing for the Next Pandemic,” NEJM 352, no. 18 (May 5, 2005): 1839-42; and Elizabeth Daugherty, Richard Branson, and Lewis Rubinson, “Mass Casualty Respiratory Failure,” Current Opinion in Critical Care 13, no. 1 (Feb. 2007): 51-56. A study by New York State found that even in a moderate pandemic, there would be a state-wide shortfall of 1,256 ventilators. In a severe pandemic, the total demand for ventilators in peak weeks would run to 17,844, almost three times the existing capacity. See NYS Working Group on Ventilator Allocation in an Influenza Pandemic, NYS DOH/NYS Task Force on Life and the Law, “Allocation of Ventilators in an Influenza Pandemic: Planning Document,” Mar. 15, 2007.
115 the Spanish flu’s victims: David M. Morens, Jeffrey K. Taubenberger, and Anthony S. Fauci, “Predominant Role of Bacterial Pneumonia as a Cause of Death in Pandemic Influenza: Implications for Pandemic Influenza Preparedness,” Journal of Infectious Diseases 198, no. 7 (Oct. 1, 2008): 962-70; Jonathan A. McCullers, “Planning for an Influenza Pandemic: Thinking Beyond the Virus,” Journal of Infectious Diseases 198, no. 7 (Oct. 1, 2008): 945-47; and John F. Brundage and G. Dennis Shanks, “Deaths from Bacterial Pneumonia During 1918-1919 Influenza Pandemic,” Emerging Infectious Diseases 14, no. 8 (Aug. 2008): 1193-99.
115 80 percent of all prescription drugs: Michael T. Osterholm, “Unprepared for a Pandemic,” Foreign Affairs, Mar.-Apr. 2007.
115 “interconnectedness of the global economy”: Ibid.
116 would run short on everything: Michael T. Osterholm, “Preparing for the Next Pandemic,” Foreign Affairs, July-Aug. 2005.
116 an unpublicized conference call: Personal notes of conference call, Jan. 15, 2004.
116 an article forScience: Richard J. Webby and Robert G. Webster, “Are We Ready for Pandemic Influenza?” Science 302, no. 5650 (Nov. 28, 2003): 1519-22. Webster also raised concerns in 2003 in Robert G. Webster and Elizabeth Jane Walker, “Influenza,” American Scientist 91, no. 2 (Mar.-Apr. 2003): 122.
116 “Klaus was very excited”: Interview with Dick Thompson.
117 “Hitoshi suddenly came alive again”: Interview with Peter Cordingley.
118 The cases continued to come: WHO: “Preliminary Clinical and Epidemiological Description of Influenza A (H5N1) in Vietnam,” Feb. 12, 2004; Tran Tinh Hien et al., “Avian Influenza A (H5N1) in 10 Patients in Vietnam,” NEJM 350, no. 12 (Mar. 18, 2004): 1179-88; and Pham Ngoc Dinh et al., “Risk Factors for Human Infection with Avian Influenza A H5N1, Vietnam 2004,” Emerging Infectious Diseases 12, no. 12 (Dec. 2006): 1841-47.
118 Thailand finally stopped: For an overview of cases in both Thailand and Vietnam, see “Avian Influenza A (H5N1),” Weekly Epidemiological Record 79, no. 7 (Feb. 13, 2004): 65-76. On Thailand specifically, see “Cases of Influenza A (H5N1)—Thailand 2004,” Morbidity and Mortality Weekly Report 53, no. 5 (Feb. 13, 2004): 100-103; Darin Areechokchia et al., “Investigation of Avian Influenza (H5N1) Outbreak in Humans—Thailand, 2004,” Morbidity and Mortality Weekly Report 55, suppl. 1 (Apr. 28, 2006): 3-6; and Anucha Apisarnthanarak et al., “Atypical Avian Influenza (H5N1),” Emerging Infectious Diseases 10, no. 7 (July 2004): 1321-24.
122 release the findings: WHO, “Avian Influenza A (H5N1)—Update 14: Two Additional Human Cases of H5N1 Infection Laboratory Confirmed in Vietnam, Investigation of a Family Cluster,” Feb. 1, 2004.
123 “the ethics of researchers”: “Thaksin Challenges WHO Statement,” Nation (Thailand), Feb. 3, 2004.
123 “temperatures were running high”: Nguyen Tran Hien, Jeremy Farrar, and Peter Horby, “Person-to-Person Transmission of Influenza A (H5N1),” Lancet 371, no. 9622 (Apr. 26, 2008): 1392-94.
125 “think of it like a war”: Notes of WHO teleconference, Feb. 7, 2004.
125 widespread in ducks: Y. Guan et al., “H5N1 Influenza: A Protean Pandemic Threat,” PNAS 101, no. 21 (May 25, 2004): 8156-61.
125 permanent foothold in Asian poultry: K. S. Li et al., “Genesis of a Highly Pathogenic and Potentially Pandemic H5N1 Influenza Virus in Eastern Asia,” Nature 430 (July 8, 2004): 209-13.
126 “no link could be established”: Internal WHO report, undated.
126 “almost certainly H2H transmission”: E-mail, Nov. 6, 2004.
127 more of the story: The cluster is also described in Kumnuan Ungchusak et al., “Probable Person-to-Person Transmission of Influenza A (H5N1),” NEJM 352, no. 4 (Jan. 27, 2005): 333-40; and “Excerpts of the Meeting of the Expert Panel on Avian Influenza,” Bangkok, Sept. 27, 2004.
130 Thailand’s health ministry announced: “Avian Influenza Infection of Patients in Kamphaeng Phet,” press release, Ministry of Health, Thailand, Sept. 28, 2004.
130 WHO released a statement: WHO, “Avian Influenza—Situation in Thailand,” Sept. 28, 2004.
130 But even as they accepted: Likely cases of human transmission have occurred in at least a half-dozen countries, also including Indonesia, Cambodia, Pakistan, and China. On the last, for example, see Hua Wang et al., “Probable Limited Person-to-Person Transmission of Highly Pathogenic Avian Influenza A (H5N1) Virus in China,” Lancet 371, no. 9622 (April 26, 2008): 1427-34.
This chapter draws on interviews with dozens of villagers in Suphan Buri Province.
133 another continent in the 1950s: Interview with local historian Samreong Reaungrit.
134 chicken made its debut: For the history of the chicken industry in Thailand, see Christopher L. Delgado, Clare A. Narrod, and Marites M. Tiongco, Policy, Technical, and Environmental Determinants and Implications of the Scaling-Up of Livestock Production in Four Fast-Growing Developing Countries: A Synthesis, Final Research Report of Phase II, International Food Policy Research Institute, June 23, 2003, ch. 2.2; Christopher L. Delgado and Clare A. Narrod, Impact of Changing Market Forces and Policies on Structural Change in the Livestock Industries of Selected Fast-Growing Developing Countries, Final Research Report of Phase I, International Food Policy Research Institute, June 28, 2002, chapter 4.5; and Nipon Poapongsakorn et al., “Annex IV: Livestock Industrialization Project: Phase II—Policy, Technical, and Environmental Determinants and Implications of the Scaling-Up of Swine, Broiler, Layer and Milk Production in Thailand,” July 25, 2003, included in Delgado, Narrod, and Tiongco, Policy, Technical, and Environmental Determinants, 2003.
134 doubled the average amount of chicken: Nipon Poapongsakorn et al., “Annex VIII: Livestock Industrialization, Trade and Social-Health-Environment Issues for the Thai Poultry, Dairy, and Swine Sector,” May 2002, included in Delgado and Narrod, Impact of Changing Market Forces, 2002.
134 an even cheaper source of protein: Ibid.
135 soaring demand for eggs: Thailand’s egg consumption doubled in a decade. Delgado, Narrod, and Tiongco, Policy, Technical, and Environmental Determinants, ch. 2.2.
137 the first to fall sick: Jared Diamond, Guns, Germs, and Steel (New York: W. W. Norton, 1997), 92.
137 afflicting their livestock: Ibid., 196-97.
137 evolved from animal pathogens: Jared Diamond, “Evolution, Consequences and Future of Plant and Animal Domestication,” Nature 418 (Aug. 8, 2002): 700-707.
137 about 60 percent also cause disease in animals: S. Cleaveland, M. K. Laurenson, and L. H. Taylor, “Diseases of Humans and Their Domestic Mammals: Pathogen Characteristics, Host Range and Risk of Emergence,” Philosophical Transactions of the Royal Society of London B: Biological Sciences 356, no. 1411 (July 29, 2001): 991-99.
137 These microbes can hopscotch: Willam B. Karesh and Robert A. Cook, “The Human-Animal Link,” Foreign Affairs, July-Aug. 2005.
137 An even higher proportion: L. H. Taylor, S. M. Latham, and M. E. Wool-house, “Risk Factors for Human Disease Emergence,” Philosophical Transactions of the Royal Society of London B: Biological Sciences 356, no. 1411 (July 29, 2001): 983-89.
137 “Similar to the time”: “Animal Health at the Crossroads: Preventing, Detecting, and Diagnosing Animal Diseases” (Washington: National Academy of Sciences, 2005), 27.
137 a mystery illness erupted: For an account, see Keith B. Richburg, “Malaysia Slow to Act on Virus,” Washington Post, Apr. 29, 1999.
138 opening of trade routes: See, for example, William H. McNeill, Plagues and Peoples (New York: Anchor Books, 1998); Wu Lien-Teh et al., Plague: A Manual for Medical and Public Health Workers (Shanghai: National Quarantine Service, 1936); and John Kelly, The Great Mortality (New York: HarperCollins, 2005).
138 “Pharoah’s rats”: Wu Lien-Teh et al., Plague. I learned of this reference in Kelly, Great Mortality.
138 plague erupted in southern China: For a good account of the Yunnan outbreak and the subsequent spread of the disease, see Carol Benedict, Bubonic Plague in Nineteenth-Century China (Stanford, CA: Stanford University Press, 1996).
139 it ravaged Hong Kong: For accounts, see Benedict, Bubonic Plague; and Edward Marriott, The Plague Race: A Tale of Fear, Science and Heroism (New York: Picador, 2003).
139 “Little wonder, then”: Marriott, Plague Race, 52.
139 reported that patients suffered: James Cantlie, “The First Recorded Appearance of the Modern Influenza Epidemic,” British Medical Journal 2 (1891): 491.
140 “epicenter” of all influenza viruses: Kennedy F. Shortridge and C. H. Stuart-Harris, “An Influenza Epicentre?” Lancet 2 no. 8302 (Oct. 9, 1982): 812-13; and Kennedy F. Shortridge, “Is China an Influenza Epicenter?” Chinese Medical Journal 110 no. 8 (1997): 637-41. More recently, researchers who studied the global spread of seasonal H3N2 flu strains between 2002 and 2007 have also suggested that the region of East and Southeast Asia is the annual source of the world’s seasonal flu viruses. See Colin A. Russell et al., “The Global Circulation of Seasonal Influenza A (H3N2) Viruses,” Science 320, no. 5874 (Apr. 18, 2008): 340-46.
140 aquatic birds: Robert G. Webster et al., “Evolution and Ecology of Influenza A Viruses,” Microbiological Review 56, no. 1 (Mar. 1992): 152-79.
140 actually been isolated earlier: A picture of the Chinese scientist who Shortridge says first isolated the 1957 Asian flu virus is shown in Kennedy F. Shortridge, “Influenza—a Continuing Detective Story,” Lancet 354 (1999): suppl. SIV 29.
141 matter of greater dispute: For a broader examination of competing hypotheses, see Gina Kolata, Flu: The Story of the Great Influenza Pandemic of 1918 and the Search for the Virus that Caused It (New York: Simon & Schuster, 1999), ch. 10.
141 Haskell County, Kansas: John M. Barry, “The Site of the Origin of the 1918 Influenza Pandemic and Its Health Implications,” Journal of Translational Medicine 2 (Jan. 20, 2004): 3. Among the evidence cited by Barry against an Asian or European provenance is Edwin O. Jordan, Epidemic Influenza: A Survey (Chi cago: American Medical Association, 1927). Jordan concluded, “The primary origin of the 1918 pandemic cannot be traced with any degree of plausibility to any one of these localized outbreaks,” referring to India, China, Japan, France, Germany, or the military camps of the United States and Britain. Jordan himself could not pinpoint the origin.
141 British army camp: J. S. Oxford, “The So-called Great Spanish Influenza Pandemic of 1918 May Have Originated in France in 1916,” Philosophical Transactions of the Royal Society of London B: Biological Sciences 356 (2001): 1857-59.
141 a Chinese pedigree: Interviews and e-mail exchanges with Kennedy Shortridge. See also Kennedy F. Shortridge, “The 1918 ‘Spanish’ Flu: Pearls from Swine?” Nature Medicine 5, no. 4 (Apr. 1999): 384-85.
141 medical accounts of an American missionary: W. W. Cadbury, “The 1918 Pandemic of Influenza in Canton,” China Medical Journal 34 (1920): 1-17.
142 the Pearl River delta: Zhao Shidong et al., “Population, Consumption, and Land Use in the Pearl River Delta, Guangdong Province,” in National Academy of Sciences, Growing Populations, Changing Landscapes: Studies from India, China and the United States (Washington: National Academies Press, 2001).
142 “greatest mass urbanization”: This description comes in his tale of another emerging disease to explode out of East Asia: SARS. Karl Taro Greenfeld, China Syndrome: The True Story of the 21st Century’s First Great Epidemic (New York: HarperCollins, 2006), 9.
143 fastest growth on Earth: World Bank, World Development Report 1997 (Washington: International Bank for Reconstruction and Development, 1997), table 1.
143 admiration for Bill Gates: Gates was rated seven times more popular than any sitting member of the Vietnamese Politburo in a survey for Tuoi Tre newspaper. The issue, released in Jan. 2001, was pulled from the newsstands by authorities.
143 “The demand-driven Livestock Revolution”: Christopher Delgado et al., Livestock to 2020: The Next Food Revolution (Washington: International Food Policy Research Institute, 1999), 4. For a discussion of the “livestock revolution,” see also Christopher L. Delgado, Mark W. Rosegrant, and Siet Meijer, “Livestock to 2020: The Revolution Continues,” Jan. 11, 2001, paper presented at the annual meetings of the International Agricultural Trade Research Consortium in Auckland, New Zealand, Jan. 2001.
144 doubled the average amount of meat: Henning Steinfeld and Pius Chilonda, “Old Players, New Players,” in Food and Agriculture Organization, Livestock Report 2006.
144 surpassed that in developed ones: Ibid.
144 China alone has accounted: Ibid.
144 A large majority: Figures on China’s livestock production come from the Food and Agriculture Organization’s database FAOSTAT. For discussion of China’s demand for livestock products, see William P. Roenigk, “Keynote Address: World Poultry Consumption,” Poultry Science 78 (1999): 722-28; and Frank Fuller, Francis Tuan, and Eric Wailes, “Rising Demand for Meat: Who Will Feed China’s Hogs,” in Fred Gale, ed., China’s Food and Agriculture: Issues for the 21st Century, Agricultural Information Bulletin no. AIB-775, Economic Research Service, U.S. Department of Agriculture, Apr. 2002.
144 Southeast Asia’s record: Figures on Southeast Asia’s livestock production come from the Food and Agriculture Organization’s database FAOSTAT.
144 the Indonesian egg: D.K.S. Swastika et al., The Status and Prospect of Feed Crops in Indonesia, UN Centre for Alleviation of Poverty Through Secondary Crops’ Development in Asia and the Pacific, working paper, no. 81, p. 23.
144 as meat prices dropped: “Managing the Livestock Revolution: Policy and Technology to Address the Negative Impacts of a Fast-Growing Sector,” World Bank, June 2005, p. 12.
144 the record is more mixed: On possible negative effects on poverty, equality, food security, and the environment, see Cornelius de Haan et al., “Livestock Development: Implications for Rural Poverty, the Environment and Global Food Security,” World Bank, Nov. 2001; Hartwig de Haen et al., “The World Food Economy in the Twenty-first Century: Challenges for International Cooperation,” Development Policy Review 21, nos. 5-6 (Sept. 2003): 683-96; and Hans Wagner, “Protecting the Eenvironment from the Impact of the Growing Industrialization of Livestock Production in East Asia,” special presentation to UN Animal Production and Health Commission for Asia and the Pacific, 26th session, Sub ang, Malaysia, Aug. 2002. On possible positive effects, see Christopher L. Delgado, Mark Rosegrant, and Nikolas Wada, “Meating and Milking Global Demand: Stakes for Small-Scale Farmers in Developing Countries,” in A. G. Brown, ed., The Livestock Revolution: A Pathway from Poverty? (Canberra: ATSE Crawford Fund, 2003); and Christopher Delgado et al., Livestock to 2020: The Next Food Revolution (Washington: International Food Policy Research Institute, 1999). On equity benefits in Thailand, see Christopher, Narrod, and Tiongco, Policy, Technical, and Environmental Determinants, ch. 3.2.
145 jutting into the fishpond: On the potential pandemic hazards associated with the mixed development of aquaculture and livestock production, see Christoph Scholtissek and Ernest Naylor, “Fish Farming and Influenza Pandemics,” Nature 331 (Jan. 21, 1988): 215.
146 A single gram of bird feces: Christine Power, “The Source and Means of Spread of the Avian Influenza Virus in the Lower Fraser Valley of British Columbia During an Outbreak in the Winter of 2004: An Interim Report,” Canadian Food Inspection Agency, Animal Disease Surveillance Unit, Feb. 15, 1004.
146 how to prevent epidemic contagion: See, for example, V. Martin, A. Forman, and J. Lubroth, Preparing for Highly Pathogenic Avian Influenza (Rome: Food and Agriculture Organization of the United Nations, 2006), ch. 5.
148 There was a time: John Steele Gordon, “The Chicken Story,” American Heritage , Sept. 1996.
148 nearly every four days: “Poultry Slaughter 2006 Annual Summary,” Agricultural Statistics Board, U.S. Department of Agriculture, Feb. 2007.
149 But the watershed: Interview with Carol Cardona, Associate Veterinarian, University of California at Davis School of Veterinary Medicine.
149 safety measures to prevent disease: Interview with Cardona. In fairness, biosecurity remains imperfect. A study in Maryland found most poultry workers are given neither protective clothing nor facilities for on-site decontamination and hygiene. See Lance B. Price et al., “Neurologic Symptoms and Neuropathologic Antibodies in Poultry Workers Exposed to Campylobacter jejuni,” Journal of Occupational and Environmental Medicine 49, no. 7 (July 2007): 748-55.
149 safeguard their investments: Interview with Goosen van den Bosch, head of technical services at Intervet.
149 generous avenue to infection: On the dangers posed by intensive poultry farming, see J. Otte et al., “Industrial Livestock Production and Global Health Risks,” Pro-Poor Livestock Policy Initiative Research Report, UN Food and Agriculture Organization, June 2007.
149 In the unnatural setting: B. Schmit, “Disease Prevention Crucial in Intensive Livestock Production,” Zootecnica International, July 1987, 49-51.
149 Thai commercial farms: J. Otte et al., “Evidence-Based Policy for Controlling HPAI in Poultry: Bio-security Revisited,” Pro-Poor Livestock Policy Initiative Research Report, UN Food and Agriculture Organization, Dec. 20, 2006.
149 lack of genetic diversity: “Managing the Livestock Revolution: Policy and Technology to Address the Negative Impacts of a Fast-Growing Sector,” World Bank, June 2005, p. 9.
149 “Once an influenza virus invades”: R. G. Webster and D. J. Hulse, “Microbial Adaption and Change: Avian Influenza,” Rev. sci. tech. Off. int. Epiz., 2004, 23 (2), 453-65.
150 a country in transition: Jan Slingenbergh et al., “Ecological Sources of Zoonotic Diseases,” Revue scientifique et technique de l’Office International des Epizooties 23, no. 2 (2004): 467-84; Marius Gilbert et al., “Livestock Production Dynamics, Bird Migration Cycles, and the Emergence of Highly Pathogenic Avian Influenza in East and Southeast Asia,” paper presented at a conference of the Food and Agriculture Organization, Rome, May 30-31, 2006.
150 are concentrated around: Pierre Gerber et al., “Geographical Determinants and Environmental Implications of Livestock Production Intensification in Asia,” Bioresource Technology 96 (2005): 263-76; and Pierre Gerber et al., “Geographical Shifts of the Livestock Production: Land Use and Environmental Impact Implications,” paper presented at the conference “Structural Change in the Livestock Sector—Social, Health, and Environmental Implications for Policy Making,” Bangkok, Thailand, Jan. 27-29, 2004.
150 “Agricultural practices have become”: Slingenbergh, “Ecological Sources of Zoonotic Diseases.” On the role of ecological factors in the evolution of zoonotic pathogens, see also Stephanie J. Schrag and Pamela Wiener, “Emerging Infectious Disease: What Are the Relative Roles of Ecology and Evolution?” Trends in Ecology and Evolution 10, no. 8 (Aug. 1995): 319-24.
150 “virtual time bomb”: Les Sims and Claire Narrod, Understanding Avian Influenza (Rome: Food and Agriculture Organization, 2008), 2.
151 showed no symptoms: D. J. Hulse-Post et al., “Role of Domestic Ducks in the Propogation and Biological Evolution of Highly Pathogenic H5N1 Influenza Viruses in Asia,” PNAS 102, no. 30 (July 26, 2005): 10682-87.
151 tested flocks of free-range ducks: Thaweesak Songserm et al., “Domestic Ducks and H5N1 Influenza Epidemic, Thailand,” Emerging Infectious Diseases 12, no. 4 (Apr. 2006): 575-81.
151 Mekong River delta: On the role of ducks in Vietnam’s outbreaks, see Dirk U. Pfeiffer et al., “An Analysis of the Spatial and Temporal Patterns of Highly Pathogenic Avian Influenza Occurrence in Vietnam Using National Surveillance Data,” Veterinary Journal 174, no. 2 (Sept. 2007): 302-9.
151 outbreaks in the chicken population: Marius Gilbert et al., “Free-Grazing Ducks and Highly Pathogenic Avian Influenza, Thailand,” Emerging Infectious Diseases 12, no. 2 (Feb. 2006): 227-34. Further research, broadened to include Vietnam, provided additional confirmation of the link between avian influenza outbreaks on one hand and ducks and intensive rice cultivation on the other. Rice paddies were identified as the best predictor of outbreak locations. See Marius Gilbert et al., “Mapping H5N1 Highly Pathogenic Avian Influenza Risk in Southeast Asia,” PNAS 105, no. 12 (Mar. 25, 2008): 4769-74.
154 Thai government would bar: Thanawat Tiensin et al., “Geographic and Temporal Distribution of Highly Pathogenic Influenza A Virus (H5N1) in Thailand, 2004-2005: An Overview,” Avian Diseases 51 (2007): 182-88.
154 flu outbreaks unexpectedly erupted: See remarks by Dr. Hoang Van Nam, Department of Animal Health, Ministry of Agriculture and Rural Development, Vietnam, at the Technical Meeting on Highly Pathogenic Avian Influenza and Human H5N1 Infection, June 27-29, 2007, Rome; and UN Food and Agriculture Organization, “Ducks May Be Behind Unexpected HPAI Outbreaks,” press release, Avian influenza newsroom, June 7, 2007.
154 the fields of Kanchanaburi province: The episode is discussed in Thaweesak Songserm et al., “Domestic Ducks and H5N1 Influenza Epidemic, Thailand,” Emerging Infectious Diseases 12, no. 4 (Apr. 2006): 575-81.
154 a peasant named Bang-on Benphat: Rungrawee C. Pinyorat, “Thailand Confirms 13th Human Death from Bird Flu,” Associated Press, Oct. 20, 2005; and WHO, Situation in Thailand—Update 35, Oct. 20, 2005.
155 “Even insects can’t get in”: Even modern, all-enclosed poultry houses have been found to be vulnerable to disease. See, for example, J. Otte et al., “Industrial Livestock Production and Global Health Risks,” Pro-Poor Livestock Policy Initiative Research Report, UN Food and Agriculture Organization, Agriculture and Consumer Protection Department, Animal Production and Health Division, June 2007. All-enclosed houses are even vulnerable to insects that spread infection. See Kyoko Sawabe et al., “Detection and Isolation of Highly Pathogenic Avian Influenza A Viruses from Blow Flies Collected in the Vicinity of an Infected Poultry Farm in Kyoto, Japan, 2004,” American Journal of Tropical Medicine and Hygiene 75, no. 2 (2006): 327-32; and Birthe Hald et al., “Flies and Campylobacter Infection of Broiler Flocks,” Emerging Infectious Diseases 10, no. 8 (Aug. 2004): 1490-92. In some cases, the fans used for ventilating enclosed houses expel contaminated particles into the outside air, where they can infect other poultry houses and farms. See Christine Power, “The Source and Means of Spread of the Avian Influenza Virus in the Lower Fraser Valley of British Columbia During an Outbreak in the Winter of 2004: An Interim Report,” Canadian Food Inspection Agency, Animal Disease Surveillance Unit, Feb. 15, 2004; and T. A. Jones, C. A. Donnelly, and M. Stamp Dawkins, “Environmental and Management Factors Affecting the Welfare of Chickens on Commercial Farms in the United Kingdom and Demark Stocked at Five Densities,” Poultry Science 84 (2005): 1155-65.
This chapter draws on interviews with public health officials and other disease specialists in Hong Kong and Guangdong.
158 “strange contagious disease”:SARS: How a Global Epidemic Was Stopped (Manila: WHO Western Pacific Regional Office, 2006), 5.
158 detected in a Hong Kong family: The case is described in J. S. Malik Peiris et al., “Re-emergence of Fatal Human Influenza A Subtype H5N1 Disease,” Lancet 363, no. 9409 (Feb. 21, 2004): 617-19; and Bernice Wuethrich, “An Avian Flu Jumps to People,” Science 299, no. 5612 (Mar. 7, 2003): 1504.
161 a medical conference in Beijing: Ceci Connolly, “Four Months of Clues to Diagnosis,” Washington Post, June 23, 2003; and Donald J. McNeil Jr. with Lawrence K. Altman, “As SARS Outbreak Took Shape, Health Agency Took Fast Action,” New York Times, May 4, 2003.
161 “He talked about deaths”:Disclosure, Canadian Broadcasting Corp., Nov. 18, 2003, cited in “Documentary Says WHO Missed Chances to Contain SARS in China,” Canadian Press, Nov. 18, 2003.
161 “put two and two together”: Michael Specter, “Nature’s Bioterrorist: Is There Any Way to Prevent a Deadly Avian-Flu Pandemic?” New Yorker, Feb. 28, 2005.
163 precisely what it was: For a description of the Guangdong outbreak and analysis of the samples collected in Guangdong, see N. S. Zhong et al., “Epidemiology and Cause of Severe Acute Respiratory Syndrome (SARS) in Guangdong, People’s Republic of China, in February, 2003,” Lancet 362, no. 9393 (Oct. 25, 2003): 1353-58.
163 With the vials stashed in his satchel: A riveting account of this episode can be found in Karl Taro Greenfeld, China Syndrome (New York: HarperCollins, 2006), ch. 20.
165 “We tried to do our best”: Cheung Chi-fai, “Margaret Chan Breaks Down Twice at Hearing,” South China Morning Post, Jan. 14, 2004.
165 “Usually, with other infectious diseases”: Mary Ann Benitez, “Health Chief Told Outbreak a State Secret,” South China Morning Post, Jan. 13, 2004.
165 She was faulted: Report of the Select Committee to Inquire into the Handling of the Severe Acute Respiratory Syndrome Outbreak by the Government and the Hospital Authority, Hong Kong Legislative Council, July 2004, ch. 3, www.legco.gov.hk/yr03-04/english/sc/sc_sars/reports/sars_rpt.htm (accessed Feb. 16, 2009).
165 a forty-four-year-old seafood seller:SARS: How a Global Epidemic Was Stopped (Manila: WHO Western Pacific Regional Office, 2006), ch. 13.
166 ninth floor of the Metropole: For an excellent account of the Metropole episode, see Ellen Nakashima, “SARS Signals Missed in Hong Kong,” Washington Post, May 20, 2003. See also SARS: How a Global Epidemic Was Stopped, ch. 14.
168 Air China flight 112:SARS: How a Global Epidemic Was Stopped, ch. 15; Brad Evenson, “‘Viral Bullets’: SARS ‘Super Spreader’ Seemed to Infect All Those Around Him on Air China Flight 112,” National Post, Mar. 29, 2003; Joseph Kahn with Elisabeth Rosenthal, “Even in Remote China, SARS Arrives in Force,” New York Times, Apr. 22, 2003; and Indira A. R. Lakshmanan, “Health Experts Express Alarm at Nature of SARS Spread on Air China Flight,” Boston Globe, May 18, 2003.
168 more than 4,000: Ellen Nakashima, “SARS Signals Missed in Hong Kong,” Washington Post, May 20, 2003.
169 islanders of the Pacific: Alfred W. Crosby, America’s Forgotten Pandemic: The Influenza of 1918, 2nd ed. (New York: Cambridge University Press, 2003), ch. 12.
169 Eskimo villages of Alaska: John M. Barry, The Great Influenza: The Epic Story of the Deadliest Plague in History (New York: Viking Penguin, 2004), ch. 30; Gina Kolata, Flu: The Story of the Great Influenza Pandemic of 1918 and the Search for the Virus That Caused It (New York: Simon & Schuster, 1999), ch. 4; and Crosby, America’s Forgotten Pandemic, ch. 12.
170 threat of infectious disease: For a discussion of the positive and negative implications of globalization for infectious disease, see Karen J. Monaghan, “SARS: Down But Still a Threat,” National Intelligence Council, 2003, reprinted in Stacey Knobler et al., eds., Learning from SARS: Preparing for the Next Disease Outbreak—Workshop Summary (Washington: National Academies Press, 2004).
170 speed of jet aircraft: John T. Bowen Jr. and Christian Laroe, “Airline Networks and the International Diffusion of Severe Acute Respiratory Disease, SARS,” Geographical Journal 172, no. 2 (June 2006): 130-44.
170 “real potential for rapid dissemination”: Statement of Mark A. Gendreau before the Committee on House Transportation and Infrastructure Subcommittee on Aviation, Apr. 6, 2005, Congressional Quarterly: Congressional Testimony, Apr. 6, 2005.
170 “a wake-up call”: WHO news release, International Health Regulations Enter into Force, June 14, 2006.
170 The Black Death: David Herlihy, The Black Death and the Transformation of the West (Cambridge, MA: Harvard University Press, 1997).
170 The last of three cholera epidemics: G. F. Pyle, “The Diffusion of Cholera in the United States in the Nineteenth Century,” Geographical Analysis 1 (1969): 59-75.
170-71 Using data on the volume of travelers: Rebecca F. Grais, Hugh Ellis, and Gregory E. Glass, “Assessing the Impact of Airline Travel on the Geographic Spread of Pandemic Influenza,” European Journal of Epidemiology 18 (2003): 1065-72.
171 a different statistical approach: Ben S. Cooper et al., “Delaying the International Spread of Pandemic Influenza,” PLoS Medicine 3, no. 6 (June 2006): e212.
171 isolated a pathogen: J. S. Malik Peiris et al., “Coronavirus as a Possible Cause of Severe Acute Respiratory Syndrome,” Lancet 361, no. 9366 (Apr. 19, 2003): 1319-25.
172 an unprecedented coup: For a fuller discussion of WHO’s success, see J. S. Mackenzie et al., “The WHO Response to SARS and Preparations for the Future,” in Stacey Knobler et al., eds., Learning from SARS: Preparing for the Next Disease Outbreak—Workshop Summary (Washington: National Academies Press, 2004); David L. Heymann and Guenael Rodier, “SARS: Lessons from a New Disease,” in Knobler, Learning from SARS; and SARS: How a Global Epidemic Was Stopped (Manila: WHO Western Pacific Regional Office, 2006), ch. 2.
172 “The quality, speed and effectiveness”: Knobler, Learning from SARS, 2.
174 approached the traders: For a dramatic account, see Karl Taro Greenfeld, China Syndrome (New York: HarperCollins, 2006), ch. 69.
175 found the evidence: Yi Guan et al., “Isolation and Characterization of Viruses Related to the SARS Coronavirus from Animals in Southern China,” Science 302, no. 5643 (Oct. 10, 2003): 276-78. For a discussion of Guan’s investigation, see Dennis Normile and Martin Enserink, “Tracking the Roots of a Killer,” Science 301, no. 5631 (July 18, 2003): 297-99.
176 “first emerging disease”:SARS: How a Global Epidemic Was Stopped, overview.
177 its reproductive number was lower: Marc Lipsitch et al., “Transmission Dynamics and Control of Severe Acute Respiratory Syndrome,” Science 300, no. 5627 (June 20, 2003): 1966-70.
177 three times greater or more: Christophe Fraser et al., “Factors That Make an Infectious Disease Outbreak Controllable,” PNAS 101, no. 16 (Apr. 20, 2004): 6146-51.
177 virus in their nose and throat: J. S. Malik Peiris et al., “Clinical Progression and Viral Load in a Community Outbreak of Coronavirus-Associated SARS Pneumonia: A Progressive Study,” Lancet 361, no. 9371 (May 24, 2003): 1767-72.
177 rarely contagious in the first few days: Roy M. Anderson et al., “Epidemiology, Transmission Dynamics and Control of SARS: The 2002-2003 Epidemic,” Philosophical Transactions of the Royal Society of London B: Biological Sciences 359 (2004): 1091-1105; and Lipsitch, “Transmission Dynamics.”
177 “very lucky this time”: Anderson, “Epidemiology, Transmission Dynamics and Control of SARS.”
177 between 30 and 50 percent: Fraser, “Factors That Make an Infectious Disease Outbreak Controllable.”
177 “Once adapted to human-to-human transmission”: J. S. Malik Peiris and Yi Guan, “Confronting SARS: A View from Hong Kong,” Philosophical Transactions of the Royal Society of London B: Biological Sciences 359 (2004): 1075-79.
188 about 7,500 years: Barbara West and Ben-Xiong Zhou, “Did Chickens Go North? New Evidence for Domestication,” Journal of Archaeological Science 15 (1988): 515-33.
188 most likely in Thailand itself: Akishinonomiya Fumihito et al., “One Subspecies of the Red Junglefowl (Gallus gallus gallus) Suffices as the Matriarchic Ancestor of All Domestic Breeds,” PNAS 91 (Dec. 1994), 12505-9.
188 red jungle fowl: Ibid.
189 “fight for kingdoms”: “Commemoration of King Naresuan: The Nation’s Great King 400 Years Ago,” Welcome to Chiangmai and Chiangrai, n.d., www.chiangmai-chiangrai.com/king_n.html (accessed Feb. 16, 2009).
190 Yuenyong included the song: Charles Piller, “Squawking at Bird Flu Warning,” Los Angeles Times, Sept. 1, 2005.
196 clear their throats: For the various details of this case, see Vijay Joshi, “Thai Man Dies of Bird Flu, Asian Toll Rises to 28,” Associated Press, Sept. 9, 2004; “Bird Flu Kills 18-Year-Old Man in Thailand,” Kyodo News Service, Sept. 9, 2004; and “Thai Man Dies of Bird Flu: Health Ministry,” Agence France Presse, Sept. 9, 2004.
197 had died in previous weeks: “Breeder Dies from Bird Flu,” Nation (Thailand), Sept. 10, 2004.
197 “The victim failed to report”: Anusak Konglang, “Thailand Reports First Bird Flu Death in Over Seven Months,” Agence France Presse, July 26, 2006.
197 villagers had declined to notify officials: “Thailand Tries to Improve Bird Flu Monitoring,” Reuters, June 27, 2006.
198 The state’s chief minister: “Repent, Nik Aziz Tells Cockfighting Buffs,” Bernama, Sept. 23, 2004.
198 Thailand shipped nearly six thousand: Kasikorn Research Center, Feb. 10, 2004, cited in “Raising Domestic Chicken Breeds: Interesting,” Thai Press Reports, Feb. 11, 2004.
198 illegal cockfighting tours: “Cock-fighting Birds Likely Culprit in Mukdahan H5N1 Outbreak,” Nation (Thailand), Mar. 21, 2007.
200 30 million households: “Govt Defends Its Bird Flu Measures,” Jakarta Post, Aug. 10, 2006.
200 “greatest single challenge”: Comments from the U.S. Agency for International Development in appendix 2 of Influenza Pandemic: Efforts to Forestall Onset Are Underway; Identifying Countries at Greatest Risk Entails Challenges, Government Accountability Office, June 2007, GAO-07-604.
201 force poultry farming underground: Juan Lubroth at an FAO press conference in Bangkok, quoted in FAO news release, “New Bird Flu Outbreaks Require Strong Vigilance,” Jan. 23, 2007.
202 continue to take risks: Sowath Ly et al., “Interaction Between Humans and Poultry, Rural Cambodia,” Emerging Infectious Diseases 13, no. 1 (Jan. 2007): 130-32; and H. M. Barennes et al., “Avian Influenza Risk Perceptions, Laos,” Emerging Infectious Diseases 13, no. 7 (July 2007): 1126-28.
203 thirteen thousand live poultry markets: Joseph Domenech et al., “Trends and Dynamics of HPAI—Epidemiological and Animal Health Risks,” Background Paper at the Technical Meeting on Highly Pathogenic Avian Influenza and Human H5N1 Infection, Rome, June 27-29, 2007.
203 a perilous nexus: Robert G. Webster, “Wet Markets—a Continuing Source of Severe Acute Respiratory Syndrome and Influenza?” Lancet 363, no. 9404 (Jan. 17, 2004): 234-36. See also Writing Committee of the Second World Health Organization Consultation on Clinical Aspects of Human Infection with Avian Influenza A (H5N1) Virus, “Update on Avian Influenza A (H5N1) Virus Infection in Humans,” NEJM 358, no. 3 (Jan. 17, 2008): 261-73; and L. D. Sims, “Lessons Learned from Asian H5N1 Outbreak Control,” Avian Diseases 51 (2007): 182-88 (2007).
203 “missing link”: D. A. Senne, J. E. Pearson, and B. Panigrahy, “Live Poultry Markets: A Missing Link in the Epidemiology of Avian Influenza,” in B. C. East erday, ed., Proceedings of the Third Annual Symposium on Avian Influenza, Madison, Wisconsin (Richmond, VA: U.S. Animal Health Association, 1992).
203 1997 human outbreak in Hong Kong: J. C. de Jong et al., “A Pandemic Warning?” Nature 389, no. 6651 (Oct. 9, 1997): 554; Eric C. J. Claas et al., “Human Influenza A H5N1 Virus Related to a Highly Pathogenic Avian Influenza Virus,” Lancet 351, no. 9101 (Feb. 14, 1998): 472-77; and Anthony W. Mounts et al., “Case-Control Study of Risk Factors for Avian Influenza A (H5N1) Disease, Hong Kong, 1997,” Journal of Infectious Diseases 180 (1999): 505-8.
203 returned to Hong Kong’s markets: L. D. Sims et al., “Avian Influenza in Hong Kong 1997-2002,” Avian Diseases 47 (2003), no. s3: 832-38.
203 On the mainland: Ming Liu et al., “The Influenza Virus Gene Pool in a Poultry Market in South Central China,” Virology 305, no. 2 (Jan. 20, 2003): 267-75.
203 six city dwellers: Hongjie Yu et al., “Human Influenza A (H5N1) Cases, Urban Areas of the People’s Republic of China, 2005-2006,” Emerging Infectious Diseases 13, no. 7 (July 2007): 1061-64.
207 a rapid-response unit: Interview with Nick Marx, WildAid.
207 imported by the tens of thousands: Hong Kong government press release, Jan. 6, 2007.
207 principal threat of reinfection: Mary Ann Benitez, “Ban Wild Bird Imports, Experts Say,” South China Morning Post, Jan. 20, 2007.
213 related to the Guangdong goose isolate: Xiyan Xu et al., “Genetic Characterization of the Pathogenic Influenza A/Goose/Guangdong/1/96 (H5N1) Virus: Similarity of Its Hemagglutinin Gene to Those of H5N1 Viruses from the 1997 Outbreaks in Hong Kong,” Virology 261, no. 1 (Aug. 15, 1999): 15-19.
213 At least three other academic papers: H. Chen K. Yu, and Z. Bu, “Molecular Analysis of Hemagglutinin Gene of Goose Origin Highly Pathogenic Avian Influenza Virus,” Agricultural Sciences in China 32 (1999): 87-92; X. Tang et al., “Isolation and Characterization of Prevalent Strains of Avian Influenza Viruses in China,” Chinese Journal of Animal and Poultry Infectious Diseases 20 (1998): 1-5; and Y. Guo, X. Xu, and X. Wen, “Genetic Characterization of an Avian Influenza A (H5N1) Virus Isolated from a Sick Goose in China,” Chinese Journal of Experimental and Clinical Virology 12, no. 4 (Dec. 1998): 322-25.
213 continued to deny publicly: See, for example, “Authorities Deny Claim on Disease,” Chinadaily.com, Mar. 7, 2007.
213 spawned the wider epidemic: On Guangdong as the continuing source of H5N1 virus strains that spread internationally, see, for example, Robert G. Wal lace et al., “A Statistical Phylogeography of Influenza A H5N1,” PNAS 104, no. 11 (Mar. 13, 2007): 4473-78. For a discussion of the precursor flu viruses that gave birth to H5N1, see, for example, L. Duan et al., “Characterization of Low-Pathogenic H5 Subtype Influenza Viruses from Eurasia: Implications for the Origin of Highly Pathogenic H5N1 Viruses,” Journal of Virology 81, no. 14 (July 2007): 7529-39; and Zi-Ming Zhao et al., “Genotypic Diversity of H5N1 Highly Pathogenic Avian Influenza Viruses,” Journal of General Virology 89 (2008): 2182-93.
213 just months before the Hong Kong cases: See, for example, Rone Tempest, “Hong Kong to Extend Poultry Ban to Ensure Avian Virus Is Eradicated,” Los Angeles Times, Dec. 31, 1997. Chinese authorities may also have covered up poultry outbreaks in Guangdong in Oct. 2003. See Dennis Chong, “Guangdong Hid Deaths,” Standard (Hong Kong), Feb. 4, 2004.
213 continuing to circulate: Angela N. Cauthen et al., “Continued Circulation in China of Highly Pathogenic Avian Influenza Viruses Encoding the Hemagglutinin Gene Associated with the 1997 H5N1 Outbreak in Poultry and Humans,” Journal of Virology 74, no. 14 (July 2000): 6592-99; and Robert G. Webster et al., “Characterization of H5N1 Influenza Viruses That Continue to Circulate in Geese in Southeastern China,” Journal of Virology 76, no. 1 (Jan. 2002): 118-26.
213 geese and ducks exported from Guangdong: Yi Guan et al., “H5N1 Influenza Viruses Isolated from Geese in Southeastern China: Evidence for Genetic Reassortment and Interspecies Transmission to Ducks,” Virology 292, no. 1 (Jan. 5, 2002): 16-23.
213 duck meat exported from Shanghai: Terrence M. Tumpey et al., “Characterization of Highly Pathogenic H5N1 Avian Influenza A Virus Isolated from Duck Meat,” Journal of Virology 76, no. 12 (June 2002): 6344-55; and X. H. Lu et al., “Pathogenesis of and Immunity to a New Influenza A (H5N1) Virus Isolated from Duck Meat,” Avian Diseases 47 (2003): 1135-40.
213 had repeatedly come back positive: H. Chen et al., “The Evolution of H5N1 Influenza Viruses in Ducks in Southern China,” PNAS 101, no. 28 (July 13, 2004): 10452-57. For more discussion of the virus in Chinese ducks, see L. D. Sims et al., “Origin and Evolution of Highly Pathogenic H5N1 Avian Influenza in Asia,” Veterinary Record 157, no. 6 (Aug. 6, 2005): 159-64.
213 China as the wellspring: H. Chen et al., “Establishment of Multiple Sublineages of H5N1 Influenza Virus in Asia: Implications for Pandemic Control,” PNAS 103, no. 8 (Feb. 21, 2006): 2845-50. China’s health ministry dismissed this study, saying it jumped to conclusions. See Mary Ann Benitez and Joseph Ma, “H5N1 Kills 8th Person on Mainland,” South China Morning Post, Feb. 11, 2006.
214 vaccinating their flocks against it: Debora MacKenzie, “Bird Flu Outbreak Started a Year Ago,” New Scientist, Jan. 31, 2004.
214 an even riskier strategy: The account of amantadine use in Chinese poultry flocks is based on extensive interviews with animal-health experts and executives of pharmaceutical companies.
214 had become resistant to the drug: On amantadine resistance among some H5N1 variants, see K. S. Li et al., “Genesis of Highly Pathogenic and Potentially Pandemic H5N1 Influenza Virus in Eastern Asia,” Nature 430 (July 8, 2004): 209-13; T. T. Hien et al., “Avian Influenza A (H5N1) in 10 Patients in Vietnam,” NEJM 350 (2004): 1179-88; Natalia A. Ilyushina, Elena A. Govorkova, and Robert G. Webster, “Detection of Amantadine Resistant Variants Among Avian Influenza Viruses Isolated in North America and Asia,” Virology 341, no. 1 (Oct. 10, 2005), 102-6; and Chung-Lam Cheung et al., “Distribution of Amantadine-Resistant H5N1 Avian Influenza Variants in Asia,” Journal of Infectious Diseases 193 (June 15, 2006): 1626-29.
215 used the drug in poultry: Fu Jing, “Misuse of Antiviral on Poultry Must Stop,” China Daily, June 21, 2005.
216 in a pair of Hanoi markets: Doan C. Nguyen et al., “Isolation and Characterization of Avian Influenza Viruses, Including Highly Pathogenic H5N1, from Poultry in Live Bird Markets in Hanoi, Vietnam, in 2001,” Journal of Virology 79, no. 7 (Apr. 2005): 4201-14.
216 a new variant of the H5N1 virus: J. Wang et al., “Identification of the Progenitors of Indonesian and Vietnamese Avian Influenza A (H5N1) Viruses from Southern China,” Journal of Virology 82, no. 7 (Apr. 2008): 3405-14.
216 how it decimated poultry: Interviews with animal health officials in Ha Tay and Vinh Phuc provinces.
216 Japfa’s annual corporate filings: PT Japfa Comfeed Indonesia Tbk, Annual Report 2003; PT Multibreeder Adirama Indonesia Tbk, Annual Report 2003; and PT Japfa Comfeed Indonesia Tbk, Annual Report 2004.
216 hushed up their findings: Karl Taro Greenfeld, “On High Alert,” Time Asia, Jan. 26, 2005.
217 “the first signs of an epidemic”: Ibid.
217 first outbreak eventually confirmed: T. Delquigny et al., “Evolution and Impact of Avian Influenza Epidemic and Description of the Avian Production in Vietnam,” final report for FAO’s TCP/RAS/3010, Emergency Regional Support for Post Avian Influenza Rehabilitation (Rome: UN Food and Agriculture Organization, 2004).
218 at least three separate occasions: H. Chen et al., “Establishment of Multiple Sublineages of H5N1 Influenza Virus in Asia: Implications for Pandemic Control,” PNAS 103, no. 8 (Feb. 21, 2006): 2845-50.
218 the government had not responded: Ben Rowse, “Hospitalized Woman in Vietnam Tests Positive for Bird Flu,” Agence France Presse, Aug. 16, 2004.
218 were going unanswered: E-mail, Aug. 13, 2004.
218 “So basically, bugger all”: E-mail, Aug. 17, 2004.
218 “grave concerns”: Avian influenza update, WHO, Report from Hanoi office, Mar. 16, 2005.
218 they were flying blind: E-mail exchange between senior WHO officials in Geneva, Mar. 13, 2005.
220 widely praised by UN agencies: See, for example, FAO news release, “Once Hard Hit by Bird Flu, Vietnam Consolidates Progress,” Dec. 6, 2006; and WHO, “Successful Strategies in Controlling Avian Influenza,” INFOSAN Information Note no. 4/2006, Aug. 14, 2006.
220 called its performance “remarkable”: Comments from the U.S. Agency for International Development in appendix 2 of Influenza Pandemic: Efforts to Forestall Onset Are Underway; Identifying Countries at Greatest Risk Entails Challenges, Government Accountability Office, June 2007, GAO-07-604. The term remarkable was applied to both Vietnam and Thailand.
220 “The situation is alarming”: “Vietnam Battles Three Bird Flu Outbreaks,” DPA (German Press Agency) article published in the Bangkok Post, Dec. 22, 2006.
222 Their revelations hit the streets: Duc Trung and Hoai Nam, “Chances of Bird Flu to Break Out, Quarantine Papers Are Sold like Vegetables,” Thanh Nieh, Aug. 16, 2005.
222 spread to nearly one-third of Indonesia’s provinces: Remarks of Agriculture Minister Bungaran Saragih in Material of Consultative Meeting Between Minister of Agriculture and Commission III DPR on Avian Influenza, Jan. 29, 2004.
222 provenance of the Indonesian strain: J. Wang et al., “Identification of the Progenitors of Indonesian and Vietnamese Avian Influenza A (H5N1) Viruses from Southern China,” Journal of Virology 82, no. 7 (Apr. 2008): 3405-14.
223 separate findings of a pathologist: Walujo Budi Priyono of the Disease Investigation Centre in Yogyakarta, quoted in FAO news release, “Virus Detective Work in Indonesia: The Case of the Mysterious Livestock Disease,” 2005.
223 “As of now, there are no findings”: Sofyan Sudrajat in Republika, Jan. 25, 2004.
224 10 million chickens: “Death of 10 Million Laying Hens in Indonesia from Bird Flu,” Kompas, Jan. 25, 2004.
224 trade in poultry and poultry products: G. J. D. Smith et al., “Evolution and Adaptation of H5N1 Influenza Virus in Avian and Human Hosts in Indonesia and Vietnam,” Virology 350 (2006): 258-68.
224 “Indonesia is a time-bomb”: “Indonesia Is a Bird-Flu Time-Bomb, Animal Health Chief,” Agence France Presse, Apr. 14, 2006.
225 She repeated her allegations: Agnes Aristiarini, “Fighting Against Bird Flu,” Kompas, Sept. 20, 2005.
225 because of party politics: “Avian Flu Expert Speaks Out,” Van Zorge Report, Apr. 12, 2006.
226 “the lack of a national strategy”: Katia Dolmadjian, “Animal Health Experts Discuss Merits of Vaccination Against Bird Flu,” Agence France Presse, Mar. 22, 2007. On how the poultry epidemic in Indonesia continued to pose a threat to human health, see Endang R. Sedyaningsih et al., “Epidemiology of Cases of H5N1 Virus Infection in Indonesia, July 2005-July 2006,” Journal of Infectious Diseases 196 (Aug. 15, 2007): 522-27.
226 the commission formally acknowledged: The commission wrote, “Indonesia reported its first case of H5N1 infection in poultry in Pekalongan and [the Jakarta suburb of] Tangerang Regencies in August 2003.” Media release, “Indonesia after 2 years, 99 cases,” KOMNAS FBPI, June 6, 2007.
226 “I will remember the support”: Josephine Ma and Mary Ann Benitez, “Beijing Agrees to Share Bird Flu Samples Sooner,” South China Morning Post, Dec. 2, 2006.
227 “my nationality on my sleeve”: Mary Ann Benitez, “A Giant Responsibility,” South China Morning Post, Nov. 12, 2006.
228 “We will have to look”: Ma and Benitez, “Beijing Agrees.”
228 “No nation has the right”: “Health Diplomacy in the 21st Century,” address to Directorate for Health and Social Affairs, Norway, Oslo, Feb. 13, 2007.
228 a cause for concern: Doubts about China’s openness in dealing with bird flu escalated in June 2006, when Chinese researchers disclosed that mainland China had had its first human case in November 2003, two years earlier than authorities had previously reported. See Qing-Yu Zhu et al., “Fatal Infection with Influenza A (H5N1) Virus in China,” NEJM 354, no. 25 (June 22, 2006): 2731-32.
228 “What on earth is going on?”: E-mail, Apr. 19, 2006.
228 a related outbreak in poultry: WHO’s chief representative in China, Hank Bekedam, expressed public frustration, saying, “That is not a good record.” Audra Ang, “WHO: Bird Flu Continues to Be Public Health Threat in China as New Case Reported in Military,” Associated Press, May 28, 2007.
228 without fully disarming the virus: A general warning about the difficulty of monitoring for bird flu in areas where poultry immunization is widely but imperfectly practiced can be found in Influenza Team, European Centre for Disease Surveillance and Control, “World Avian Influenza Update,” Eurosurveillance 11, no. 6 (2006): 060622.
228 exposure to this second strain, H9N2: For a fuller discussion of the dangers posed by cocirculation of H9N2 and H5N1, see Alexey Khalenkov et al., “Modulation of the Severity of Highly Pathogenic H5N1 Influenza in Chickens Previously Inoculated with Israeli H9N2 Influenza Viruses,” Virology 383 (2009): 32-38.
229 the politics of China’s public health system: Huang’s exploration of infectious-disease policy in China can be found in his writings, including “China’s Response to Avian Flu,” paper delivered at SAIS China Forum, Mar. 18, 2006, Washington; “The Political Challenges of Health Crises in China,” speech at the Conference on Asia and the Science and Politics of Pandemics, CNA Corp., Feb. 3, 2005; and “The Politics of China’s SARS Crisis,” Harvard Asia Quarterly, Fall 2003.
229 transformed the country’s health sector: See also Nan-Shan Zhong and Guang-Qiao Zeng, “Pandemic Planning in China: Applying Lessons from Severe Acute Respiratory Syndrome,” Respirology 13, suppl. 1 (2008): S33-S35.
229 did not extend to the agriculture ministry: See, for example, “Sanitising the Record; Infectious Diseases in China,” Economist, July 1, 2006.
229 the central government wasn’t sure: Notes of WHO meeting with Hui Liangyu in e-mail, Feb. 6, 2004. Two years later, the Chinese health ministry was still complaining that local authorities were failing to report possible cases of bird flu in a timely fashion. See, for example, Nicholas Zamiska, “China Bird-Flu Data in Doubt,” Wall Street Journal, Apr. 27, 2006.
229 that changed his life: For good accounts of Qiao Songju’s ordeal, see “Whistle-Blower Awaits Blackmail Verdict,” Chinadaily.com, Apr. 29, 2006; Xu Xiang, “China Plagued by Bird-Flu Cover-ups,” Asia Times Online, June 8, 2006; and Jane Cai, “Bird Flu Whistle-Blower Gets Jail Term for Graft,” South China Morning Post, July 10, 2006.
230 “Qiao Songju is a sinner”: Xu Xiang, “China Plagued by Bird-Flu Cover-ups.”
231 “block information from us”: Notes of telephone briefing for WHO headquarters, July 20, 2005.
232 “from poultry in southern China”: H. Chen et al., “H5N1 Virus Outbreak in Migratory Waterfowl,” Nature 436 (July 14, 2005): 191-92. A separate study of the Qinghai Lake outbreak published at about the same time, is Jinhua Liu et al., “Highly Pathogenic H5N1 Influenza Virus Infection in Migratory Birds,” Science 309, no. 5738 (Aug. 19, 2005): 1206.
232 No bird flu has broken out: “Chinese Official Questions Credibility of Nature ’s Article on Bird Flu,” Xinhua, July 8, 2005.
232 could have been contaminated: Nicholas Zamiska and Matt Pottinger, “Two Experts in China Dispute Bird-Flu Risks,” Wall Street Journal, July 19, 2005.
232 shuttered immediately: “Highly Pathogenic Microbe Labs Must Operate Under Government Supervision: Ministry,” Xinhua, Dec. 15, 2005.
233 a new wave of disease: G. J. D. Smith et al., “Emergence and Predominance of an H5N1 Influenza Variant in China,” PNAS 103, no. 45 (November 7, 2006): 16936-41.
233 “not based on science”: Lindsay Beck, “China Shares Bird Flu Samples, Denies New Strain Report,” Reuters, Nov. 10, 2006. This time, the research faced a wider barrage from Chinese officials, including the directors of the National Influenza Centre and the National Avian Influenza Reference Laboratory. See “Experts Refute New Bird Flu Strain Claim,” Chinadaily.com, Nov. 6, 2006; and “New US Bird Flu Report Lacks Evidence Base,” Chinadaily.com, Nov. 10, 2006.
This chapter draws on interviews with current and former infectious-disease and laboratory specialists and other public health officials at WHO and the agency’s consultants in Asia, North America, Europe, and Australia. The chapter also draws on interviews with infectious-disease and laboratory specialists, public health officials, and doctors and nurses in Vietnam at the national level and at the provincial and local levels in Hanoi and Thai Binh, as well as with victims and their families. In addition, material for this chapter is drawn from internal documents from WHO and personal notes kept by several participants in the events described.
241 genetic signature of the pathogen: Q. Mai Le et al., “Isolation of Drug-Resistant H5N1 Virus,” Nature 437 (Oct. 20, 2005): 1108.
245 shifting patterns of infection: WHO Inter-country Consultation: Influenza A/H5N1 in Humans in Asia, Manila, May 6-7, 2005. On the genetic changes detected, see also WHO Global Influenza Program Surveillance Network, “Evolution of H5N1 Avian Influenza Viruses in Asia,” Emerging Infectious Diseases 11, no. 10 (Oct. 2005): 1515-21.
246 drafted a confidential report: “Reassessment of the Current Situation of Influenza A (H5N1) in Vietnam,” internal WHO report, June 2005.
248 “We’ll never have perfect data”: Personal notes of meeting.
249 “If the results are correct”: Vietnam Pandemic Assessment, internal WHO memo, June 9, 2005.
249 the conference call: The account of the conference call is based on interviews with ten of the participants, personal notes of the call kept by several participants, and WHO documents describing it.
253 diagnosing the virus: See, for example, Pui Hong Chung et. al., the Global Influenza Program, “Expert Consultation on Diagnosis of H5N1 Avian Influenza Infections in Humans,” Influenza and Other Respiratory Viruses 1, no. 4 (July 2007): 131-38; Writing Committee of the Second World Health Organization Consultation on Clinical Aspects of Human Infection with Avian Influenza A (H5N1) Virus, “Update on Avian Influenza A (H5N1) Virus Infection in Humans,” NEJM 358, no. 3 (Jan. 17, 2008): 261-73; and WHO, “Influenza Research at the Human and Animal Interface,” Report of WHO Working Group, Sept. 21-22, 2006.
253 mountains of eastern Turkey: Ahmet Faik Oner et al., “Avian Influenza A (H5N1) Infection in Eastern Turkey in 2006,” NEJM 355, no. 21 (Nov. 23, 2006): 2179-85.
254 Researchers in Indonesia: I. Nyoman Kandun et al., “Three Indonesian Clusters of H5N1 Virus Infection in 2005,” NEJM 355, no. 21 (Nov. 23, 2006): 2186-94.
254 doctors in Thailand: “H5N1 Virus Now Harder to Detect in Humans,” Nation (Thailand), Aug. 18, 2006; and Writing Committee of the World Health Organization Consultation on Human Influenza A/H5, “Avian Influenza A (H5N1) Virus Infection in Humans,” NEJM 353, no. 13 (Sept. 29, 2005): 1374-85.
254 WHO says they are not sensitive enough: WHO, “WHO Recommendations on the Use of Rapid Testing for Influenza Diagnosis”; and WHO, “Clinical Management of Human Infection with Avian Influenza A (H5N1) Virus,” updated Aug. 15, 2007.
255 “does not encourage immediate openness”: Angus Nicoll, “Human H5N1 Infections: So Many Cases—Why So Little Knowledge?” Eurosurveillance 11, nos. 4-6 (Apr.-June 2006): 74-75.
255 fewer than a dozen victims: One of the few autopsies was performed on Captan Boonmanut, the Thai boy whose admission to Siriraj Hospital in Bangkok helped alert Dr. Prasert Thongcharoen to the spreading virus. See Mongkol Uip rasertkul et al., “Influenza A H5N1 Replication Sites in Humans,” Emerging Infectious Diseases 11, no. 7 (July 2005): 1036-41.
256 Rini Dina: Her case is discussed in: I. Nyoman Kandun et al., “Three Indonesian Clusters of H5N1 Virus Infection in 2005,” NEJM 355, no. 21 (Nov. 23, 2006): 2186-94.
258 on the afternoon of Tuesday, June 14: The account of this meeting is based primarily on an internal WHO account, “Notes of Avian Influenza Meeting, Tuesday, June 14, 2005.”
260 when Troedsson reported back: Personal notes of call, June 14, 2005.
260 Stohr and his colleagues in Geneva: Personal notes of discussion, June 14, 2005.
260 sent an e-mail: E-mail from Yan Li, June 13, 2005.
261 Kinsmen Place Lodge: The details in this account are drawn from extensive press coverage of the episode in August and September 2003, including multiple articles written by Helen Branswell of Canadian Press; Pamela Fayerman, Kim Pemberton, and Nicholas Read of the Vancouver Sun; Mark Hume of the Toronto Globe and Mail; and Lawrence K. Altman of the New York Times. See also Wayne Kondro, “Canadian Officials Watch SARS-like Mystery Bug,” Lancet 362, no. 9385 (Aug. 30, 2003): 714.
262 without his permission: Nicholas Zamiska, “Avian Flu Puts WHO in a Bind,” Wall Street Journal Asia, Oct. 18, 2005.
263 Khai signaled his government’s good intentions: For Ellen Nakashima’s full interview with Khai, see “Transcript: Interview with Phan Van Khai,” washingtonpost.com, June 16, 2005.
264 “They should be from different backgrounds”: Personal notes of discussion.
264 say as little as necessary: Personal notes of call.
264 without actually lying to them: For WHO’s vaguely worded, four-paragraph press release about the mission, see “International Team of Avian Influenza Experts Visits Viet Nam,” June 24, 2005.
266 rogue bits of genetic material: Several members of the WHO mission, including Tashiro, told me that the Canadian primers were at fault. Plummer later told me that he did not dispute the findings that the tests conducted with the Canadian-supplied primers had yielded false positives. But he added, “Given that both our lab and the CDC have concluded that our primers are effective, we remain confident that they were not the cause of the false positives.”
266 French press agency reported: “Top Scientists Downgrade Risk of Imminent Bird Flu Pandemic,” Agence France Presse, June 29, 2005.
269 more people had died: On the stream of Indonesian cases in late 2005 and early 2006, see Endang R. Sedyaningsih et al., “Epidemiology of Cases of H5N1 Virus Infection in Indonesia, July 2005-June 2006,” Journal of Infectious Diseases 196, no. 4 (Aug. 15, 2007): 522-27.
269 keeping her identity confidential: Though I continue to honor this request, the victim’s name was disclosed in Indonesian press reports.
273 humming with questions: On the key steps and objectives of an avian flu investigation, see “WHO Guidelines for Investigation of Human Cases of Avian Influenza A (H5N1),” WHO, Jan. 2007.
274 A study of Indonesia’s first 127 confirmed cases: I. Nyoman Kandun et al., “Factors Associated with Case Fatality of Human H5N1 Infections in Indonesia: A Case Series,” Lancet 372, no. 9640 (Aug. 30, 2008): 744-49.
277 deadliest outbreak of Marburg hemorrhagic fever: Accounts of the Angola outbreak can be found in John Donnelly, “Deadly Virus, Anger Take Hold in Angola,” Boston Globe, Apr. 12, 2005; Sharon LaFraniere and Denise Grady, “Stalking a Deadly Virus, Battling a Town’s Fears,” New York Times, Apr. 17, 2005; and M. A. J. McKenna, “CDC Team Sees Small Advances Against Disease,” Atlanta Journal-Constitution, May 25, 2005.
277 a flare-up in southern Sudan: A good account is David Brown, “U.N. Team Studies Sudan Outbreak,” Washington Post, Oct. 21, 1998.
278 the mountains of Afghanistan: For details, see WHO press release, “‘Influenza-like’ Acute Respiratory Infection Behind Deadly Afghan Outbreak,” Mar. 2, 1999.
280 suddenly erupted in Azerbaijan: Some of the details in this account come from internal WHO situation updates, field reports, and notes of conference calls in March 2006. The outbreak is described in “Human Avian Influenza in Azerbaijan, February-March 2006,” Weekly Epidemiological Record, no. 18, May 5, 2006, 183-88; A. Gilsdorf et al., “Two Clusters of Human Infection with Influenza A/H5N1 Virus in the Republic of Azerbaijan, February-March 2006,” Eurosurveillance 11, nos. 4-6, Apr.-June 2006, 122-26; and Caroline Brown, “First H5N1 Outbreak in Humans Associated with Dead Wild Birds: Azerbaijan, February-April 2006,” paper presented at FAO/OIE International Scientific Conference on Avian Influenza and Wild Birds, Rome, May 30-31, 2006.
282 rumors and emerging reports: See Gina Samaan et al., “Rumor Surveillance and Avian Influenza H5N1,” Emerging Infectious Diseases 11, no. 3 (Mar. 2005): 463-66.
285 Five South Koreans: “Five More in S. Korea Infected by Bird Flu,” Agence France Presse, Sept. 15, 2006.
285 Hong Kong’s mass slaughter: C. B. Bridges et al., “Risk of Influenza A (H5N1) Infection Among Poultry Workers, Hong Kong, 1997-1998,” Journal of Infectious Diseases 185, no. 8 (Apr. 15, 2002): 1005-10. This article also reports that 10 percent of 1,525 poultry workers tested in Hong Kong were positive for H5N1 antibodies.
285 In one telling study: Sirenda Vong et al., “Low Frequency of Poultry-to-Human H5N1 Virus Transmission, Southern Cambodia, 2005,” Emerging Infectious Diseases 12, no. 10 (Oct. 2006): 1542-47. A pair of studies that looked at Nigerian poultry workers with widespread exposure to likely infected poultry and Chinese workers in live poultry markets at the time of a human infection possibly contracted in a market also showed minimal evidence of antibodies to H5N1. See J. R. Ortiz et al., “Lack of Evidence of Avian-to-Human Transmission of Avian Influenza A (H5N1) Virus Among Poultry Workers, Kano, Nigeria, 2006,” Journal of Infectious Diseases 196, no. 11 (Dec. 1, 2007), 1685-91; and Ming Wang et al., “Food Markets with Live Birds at Source of Avian Influenza,” Emerging Infectious Diseases 12, no. 11 (Nov. 2006): 1773-75.
285 A subsequent study: Sirenda Vong et al., “Risk Factors Associated with Sub-clinical Human Infection with Avian Influenza A (H5N1) Virus—Cambodia, 2006,” Journal of Infectious Diseases 199, no. 12 (June 15, 2009): 1744-52.
285 enigma of the cullers: There’s a similar puzzle for health-care workers. Studies of health-care staff in Vietnam who treated avian-flu patients also found no evidence of exposure to the virus. This is in marked contrast to the experience with SARS, which took a heavy toll on health-care workers. See Nguyen Thanh Liem, World Health Organization Avian Influenza Investigation Team Vietnam, and Wilina Lim, “Lack of H5N1 Avian Influenza Transmission to Hospital Employees, Hanoi, 2004,” Emerging Infectious Diseases 11, no. 2 (Feb. 2005): 210-15; and Constance Schultsz et al., “Avian Influenza H5N1 and Healthcare Workers,” Emerging Infectious Diseases 11, no. 7 (July 2005): 1158-59.
286 unable to identify a possible source: Endang R. Sedyaningsih et al., “Epidemiology of Cases of H5N1 Virus Infection in Indonesia, July 2005-June 2006,” Journal of Infectious Diseases 196, no. 4 (Aug. 15, 2007): 522-27.
286 were ruled inconclusive: Bayu Krisnamurti, head of Indonesia’s National Avian Influenza Committee, quoted in “Indonesia Investigating Suspicious Bird Flu cases: Official,” Agence France Presse, Dec. 18, 2007.
286 behavior of the virus in Indonesia “mysterious”: “Mysterious Bird Flu Baffles Indonesian Scientists,” Agence France Presse, Feb. 6, 2008.
286 the country’s first human case: It is described in I. Nyoman Kandun et al., “Three Indonesian Clusters of H5N1 Virus Infection in 2005,” NEJM 355, no. 21 (Nov. 23, 2006): 2186-94.
287 a quarter of all confirmed cases: Writing Committee of the Second World Health Organization Consultation on Clinical Aspects of Human Infection with Avian Influenza A (H5N1) Virus, “Update on Avian Influenza A (H5N1) Virus Infection in Humans,” NEJM 358, no. 3 (Jan. 17, 2008): 261-73. On case clusters, see also Sonja J. Olsen et al., “Family Clustering of Avian A (H5N1),” Emerging Infectious Diseases 11, no. 11 (Nov. 2005): 1799-1801. On Indonesian clusters specifically, see discussion in Endang R. Sedyaningsih et al., “Epidemiology of Cases of H5N1 Virus Infection in Indonesia, July 2005-June 2006,” Journal of Infectious Diseases 196, no. 4 (Aug. 15, 2007): 522-27.
289 made some people susceptible: See, for example, WHO, Report of WHO Working Group, “Influenza Research at the Human and Animal Interface,” Sept. 21-22, 2006.
289 statistical chance alone: V. E. Pitzer et al., “Little Evidence for Genetic Susceptibility to Influenza A (H5N1) from Family Clustering Data,” Emerging Infectious Diseases 13, no. 7 (July 2007): 1074-76.
294 despite some projections: Hitoshi Oshitani, Taro Kamigaki, and Akira Suzuki, “Major Issues and Challenges of Influenza Pandemic Preparedness in Developing Countries,” Emerging Infectious Diseases 14, no.6 (June 2008): 875-80.
295 “He just knows everybody”: Interview with Dr. Megge Miller.
296 The health workers at the two local clinics: Interviews with Ly Lai and Dr. Ou Sary, Kampot province.
297 it went a long way: Interviews with current and former WHO officials in Cambodia, including Drs. Michael O’Leary, Isabel Bergeri, and Megge Miller. See Richard Stone, “Combating the Bird Flu Menace, Down on the Farm,” Science 311, no. 5763 (Feb. 17, 2006): 944-46.
298 a surprising item: William Prochnau and Laura Parker, “The Waiting Plague,” Vanity Fair, Nov. 2005.
298 had pledged $2.3 billion: UN System Influenza Coordinator (SIC) and World Bank, “Responses to Avian Influenza and State of Pandemic Readiness, Third Global Progress Report,” Dec. 2007 (1st printing, released Nov. 29, 2007). The total figure increased modestly to $2.7 billion in 2008. See UN SIC and World Bank, “Responses to Avian Influenza and State of Pandemic Readiness, Fourth Global Progress Report,” Oct. 2008.
299 ninety-one-page progress report: UN SIC and World Bank, “Responses… Third Global Progress Report,” Dec. 2007 (1st printing).
299 a new version of the report: UN SIC and World Bank, “Responses… Third Global Progress Report,” Dec. 2007 (2nd printing, released Dec. 18, 2007), 8-9.
299 would decline even further in 2008: UN SIC and World Bank, “Responses… Fourth Global Progress Report,” Oct. 2008. The report warned, “There is a risk that this decline in resources pledged, especially for countries with the greatest remaining needs, could undermine the sustainability of the investments made to date.”
299 warned of growing “flu fatigue”: Paula Dobriansky, undersecretary of state for democracy and global affairs, “Remarks at the International Partnership on Avian and Pandemic Influenza Ministerial, Sharm El Sheikh, Egypt,” Federal News Service, Oct. 25, 2008.
299 the World Bank had helped estimate: World Bank, “Avian and Human Influenza: Update on Financing Needs and Framework,” Nov. 30, 2006. The original estimates were in World Bank, “Avian and Human Influenza: Financing Needs and Gaps,” Jan. 12, 2006.
299 sector after sector: UN SIC and World Bank, “Responses… Third Global Progress Report,” Dec. 2007 (1st printing).
300 “Adequate financial support”: Ibid.
301 Yet the obstacles are many: An excellent examination of the challenges facing the development of a pandemic vaccine is the seven-part series “The Pandemic Vaccine Puzzle,” written by Maryn McKenna for the Center for Infectious Disease Research and Policy and posted online beginning October 25, 2007. The articles are available at www.cidrap.umn.edu. Another fine overview is Joost H. C. M. Kreijtz, Albert D. M. E. Osterhaus, and Guus F. Rimmelzwaan, “Vaccination Strategies and Vaccine Formulations for Epidemic and Pandemic Influenza Control,” Human Vaccines 5 (Mar. 2009): 3. See also WHO, “Global Pandemic Influenza Action Plan to Increase Vaccine Supply,” Oct. 23, 2006; and National Institute of Allergy and Infectious Diseases, “Report of the Blue Ribbon Panel on Influenza Research,” Sept. 11-12, 2006.
301 research into any kind of flu vaccine: See, for example, a pair of studies by the Institute of Medicine. Kathleen R. Stratton, Jane S. Durch, and Robert S. Lawrence, eds., Vaccines for the 21st Century: A Tool for Decisionmaking (Washington; National Academies Press, 2000); and Institute of Medicine staff, New Vaccine Development: Establishing Priorities (Washington: National Academies Press, 1985).
301 An analysis in 2007: Aeby Thomas, Niels Guldager, and Klaus Hermansen, “Pandemic Flu Preparedness: A Manufacturing Perspective,” BioPharm International, Aug. 2, 2007. For further discussion of the delays inherent in developing a pandemic vaccine, see Jesse L. Goodman, “How Fast Can a New Vaccine for an Emerging Respiratory Virus Be Developed and Available for Use?” Presentation at the International Conference on Emerging Infectious Diseases, Atlanta, GA, Mar. 22, 2006.
301 confound efforts to develop a single vaccine: See, for example, WHO, Report of WHO Working Group, “Influenza Research at the Human and Animal Interface,” Sept. 21-22, 2006; Steven Riley, Joseph T. Wu, and Gabriel M. Leung, “Optimizing the Dose of Pre-Pandemic Influenza Vaccines to Reduce the Infection Rate,” PLoS Medicine 4, no. 6 (June 2007): e218; and G. J. D. Smith et al., “Emergence and Predominance of an H5N1 Influenza Variant in China,” PNAS 103, no. 45 (Nov. 7, 2006): 16936-41.
301 unusually resistant to experimental vaccines: See, for example, Karl G. Nich olson et al., “Safety and Antigenicity of Non-adjuvanted and MF59-adjuvanted Influenza A/Duck/Singapore/97 (H5N3) Vaccine: A Randomized Trial of Two Potential Vaccines Against H5N1 Influenza,” Lancet 357, no. 9272 (June 16, 2001): 1937-43; Jean-Louis Bresson et al., “Safety and Immunogenicity of an Inactivated Split-Virion Influenza A/Vietnam/1194/2004 (H5N1) Vaccine: Phase I Randomised Trial,” Lancet 367, no. 9253 (May 20, 2006): 1657-64; Isabel Leroux-Roels et al., “Antigen Sparing and Cross-Reactive Immunity with an Adjuvanted rH5N1 Prototype Pandemic Influenza Vaccine: A Randomised Controlled Trial,” Lancet 370, no. 9587 (Aug. 18, 2007): 580-89; and Nega Ali Gogi et al., “Immune Responses of Healthy Subjects to a Single Dose of Intramuscular Inactivated Influenza A/ Vietnam/1203/2004 (H5N1) Vaccine After Priming with an Antigenic Variant,” paper presented at Third WHO Meeting on Evaluation of Pandemic Influenza Prototype Vaccines in Clinical Trials, Geneva, Feb. 15-16, 2007.
302 This could cut the production time: Peter F. Wright, “Vaccine Preparedness—Are We Ready for the Next Influenza Pandemic?” NEJM 358, no. 24 (June 12, 2008): 2540-43.
302 Initial clinical trials: Hartmut J. Ehrlich et al., “A Clinical Trial of a Whole-Virus H5N1 Vaccine Derived from Cell Culture,” NEJM 358, no. 24 (June 12, 2008): 2573-84.
302 than even seasonal flu shots: David Brown, “Bird Flu Vaccine Shows Promise,” Washington Post, July 27, 2006; Leroux-Roels, “Antigen Sparing”; and Suryaprakash Sambhara and Gregory A. Poland, “Breaking the Immunogenicity Barrier of Bird Flu Vaccines,” Lancet 370, no. 9587 (Aug. 18, 2007): 544.
302 could radically increase: WHO, “Projected Supply of Pandemic Influenza Vaccine Increases Sharply,” press release, Oct. 23, 2007.
302 “can’t provide vaccines to the world free”: Wayne Pisano, quoted in a Council on Foreign Relations letter from Laurie Garrett, senior fellow for global health, June 20, 2007.
302 a local vaccine against hepatitis B: Tini Tran, “Vietnam Struggles to Rein In Hepatitis B,” Associated Press, July 17, 2000.
302 a new generation of vaccines: “Health: Vietnam Successfully Produces Second Generation Hepatitis Vaccines,” Vietnam News Briefs, Apr. 11, 2002.
303 “future availability to Vietnam is doubtful”: “Report of WHO Mission to Support Influenza A/H5N1 Vaccine Development in Vietnam,” 2005.
303 “serious ethical reservations”: Ibid.
304 “the volunteer ‘spirit’ may not be universally shared”: Internal WHO document, 2005.
304 monkey kidney cells: “Vietnam-made Bird Flu Vaccine Proves Effective,” Vietnamese News Agency, Aug. 22, 2008.
304 on researchers at the institute: “Volunteers for H5N1 Vaccines Get Second Injection,” Vietnamese News Agency, May 17, 2008.
304 student volunteers: Ibid.
304 “Good results”: Tranh Dinh Lam, “Vietnam: Bird Flu Vaccine for Humans May Be Available by 2009,” Interpress Service, June 4, 2008.
304 mass production by late 2009: “Vietnam-made Bird Flu Vaccine Proves Effective,” Vietnamese News Agency, Aug. 22, 2008.
304 30,000 Vietnamese dong: Ibid.
304 Siti Fadilah Supari was far less patient: The accounts of Supari’s political rise, her battle over the sharing of viruses, and the wider international dispute over samples and benefits are drawn from interviews with Supari, current and former officials of the Indonesian health ministry, and other Indonesian public health officials and political figures. It also draws on interviews with WHO officials and public health and diplomatic officials from the United States, Australia, and other countries, as well as documents from the Indonesian health ministry, WHO, and the U.S. Department of Health and Human Services.
305 Her scheduled flight: Details of Supari’s trip to Geneva are drawn from Siti Fadilah Supari, It’s Time for the World to Change: In the Spirit of Dignity, Equity, and Transparency, Divine Hand Behind Avian Influenza (Jakarta: Sulaksana Watinsa Indonesia, 2008), 112ff.
306 “We do not really know”: Statement by the Minister of Health of the Republic of Indonesia H. E. Dr. Siti Fadilah Supari at the Inter-Governmental Meeting for Pandemic Influenza Preparedness, Geneva, Nov. 20, 2007.
307 her cell phone rang: Yanto Soegiarto, “Diving into the Deep End,” Globe Asia, Oct. 2007.
309 a running dispute with foreign scientists: The account of the NAMRU dispute is based on interviews with Andrew Jeremijenko, other NAMRU staff, and Indonesian health ministry officials.
309 “difficult to get the damn virus”: Interview with Jeremijenko.
310 cease all activities: “Circular Regarding the Status of NAMRU-2,” Oct. 25, 2005, signed by Secretary Titie Kabul Adimidjaja, acting head of Badan Litbangkes.
312 “I never gave permission”: Wahya Dhyatmika and Pramono, “WHO’s Virus?” Tempo, Feb. 20, 2007.
312 unless they met Supari’s demands: The Indonesian position is best detailed in Endang R. Sedyaningsih et al., “Toward Mutual Trust, Transparency and Equity in Virus Sharing Mechanism: The Avian Influenza Case of Indonesia,” Annals of the Academy of Medicine (Singapore) 37, no. 6 (June 2008): 482-88. Supari was one of the authors on this paper written by Indonesian health ministry officials. The position prevailing in many developing countries, in particular the United States, is well articulated in Richard Holbrooke and Laurie Garrett, “‘Sovereignty’ That Risks Global Health,” Washington Post, Aug. 10, 2008. An Indonesian response to the column by Holbrooke and Garrett is Makarim Wibisono, “The Responsible Virus and Sharing Benefits,” Jakarta Post, Aug. 27, 2008. Wibisono was the Indonesian ambassador to the United Nations in New York and in Geneva.
313 Her attack was unprecedented: For a discussion of the global health issues raised by Indonesia’s decision to withhold virus samples, see Chan Chee Khoon and Gilles de Wildt, “Developing Countries, Donor Leverage, and Access to Bird Flu Vaccines,” DESA Working Paper no. 41, UN Department of Economic and Social Affairs, June 2007.
313 viruses were biological resources: On two rival interpretations of international law governing virus samples, see David P. Fidler, “Influenza Virus Samples, International Law, and Global Health Diplomacy,” Emerging Infectious Diseases 14, no. 1 (Jan. 2008): 88-94.
313 “WHO has become a target”: Personal notes of conversation.
314 “Indonesia’s leadership alerted”: “RI ‘Will Not Share’ Flu Samples,” Jakarta Post, Feb. 7, 2007. The joint statement issued after the meetings between Supari and Heymann is “Sharing of Avian Influenza Viruses and Pandemic Vaccine Production,” Joint Statement from the Ministry of Health of Indonesia and the World Health Organization, Feb. 16, 2007.
314 “the answer is still no, no, no”: Wahya Dhyatmika and Pramono, “WHO’s Virus?” Tempo, Feb. 20, 2007.
314 The Indonesian leader stressed: “RI Stresses Need for Production of Affordable Bird Flu Vaccines,” Antara news agency, Apr. 4, 2007.
314 “We will resume the sending of virus samples”: “Indonesia Confirms Readiness to Send Bird Flu Virus to WHO,” Xinhua, April 4, 2007.
314 “I believe the developing countries are right”: Margaret Chan, Opening remarks at the Meeting on Options for Increasing the Access of Developing Countries to H5N1 and other Potential Pandemic Vaccines, Geneva, April 25, 2007.
315 “I will fail you”: Laura MacInnis, “WHO’s Chan Pledges Fair Access to Bird Flu Vaccines,” Reuters, May 17, 2007.
315 suggested the UN Security Council: Laurie Garrett and David P. Fidler, “Sharing H5N1 Viruses to Stop a Global Influenza Pandemic,” PLoS Medicine 4, no. 11 (Nov. 2007): e330, 1712-14.
315 “I was exhausted”: Siti Fadilah Supari, It’s Time for the World to Change: In the Spirit of Dignity, Equity, and Transparency, Divine Hand Behind Avian Influenza (Jakarta: Sulaksana Watinsa Indonesia, 2008), 129.
315 their private encounter: Accounts of the meeting were provided by several Indonesian and WHO officials. Supari’s comments are drawn from Supari, It’s Time for the World to Change, 129-31.
317 weapons of mass destruction: Supari, It’s Time for the World to Change, 19.
317 “the nuttiest idea I ever heard”: “Remarks by Defense Secretary Robert Gates to the Indonesian Council on World Affairs, Jakarta, Indonesia,” Federal News Service, Feb. 25, 2008.
317 a rapturous reception: See, for example, “Alarm as Indonesia Thumbs Nose at West over Bird Flu,” Agence France Presse, Sept. 7, 2008.
317 “of no use to us”: “RI Seeking Equality in Cooperation with NAMRU-2: Minister,” Antara news agency, June 26, 2008.
317 One lawmaker called for a probe: “News Focus: Call for Closure of NAMRU- 2 in Indonesia Increasing,” Antara news agency, June 27, 2008.
321 a quarter of all the illegally trafficked chickens: “Illegal Chickens in Northern Area Test Positive for Bird Flu,” Viet Nam News, Mar. 22, 2008.
321 uncovered lab evidence: H. Chen et al., “Establishment of Multiple Sublineages of H5N1 Influenza Virus in Asia: Implications for Pandemic Control,” PNAS 103, no. 8 (Feb. 21, 2006): 2845-50.
321 on “multiple occasions”: Tien Dung Nguyen et al., “Multiple Sublineages of Influenza A Virus (H5N1), Vietnam, 2005-2007,” Emerging Infectious Diseases 14, no. 4 (Apr. 2008): 632-36.
322 The strain made its debut: For more discussion, see Carl Suetens et al., “Eagles Testing Positive for H5N1 Imported Illegally into Europe from Thailand,” Eurosurveillance 8, no. 44 (Oct. 28, 2004); and Debora MacKenzie, “Europe Has Close Call with Deadly Bird Flu,” New Scientist, Oct. 26, 2004.
322 “very, very lucky”: MacKenzie, “Europe Has Close Call.”
322 exploded out of East Asia: See overviews in “Epidemiology of WHO-Confirmed Human Cases of Avian Influenza A(H5N1) Infection,” Weekly Epidemiological Record 81, No. 26 (June 30, 2006): 249-57; and “Update: WHO-Confirmed Human Cases of Avian Influenza A(H5N1) Infection,” Weekly Epidemiological Record 82, No. 6 (Feb. 9, 2007): 41-47.
322 each time researchers checked: See, for example, B. Pattnaik et al., “Phylogenetic Analysis Revealed Genetic Similarity of the H5N1 Avian Influenza Viruses Isolated from HPAI Outbreaks in Chickens in Maharashtra, India, with Those Isolated from Swan in Italy and Iran in 2006,” Current Science 91, no. 1 (July 10, 2006): 77-81; M. F. Ducatez et al., “Multiple Introductions of H5N1 in Nigeria,” Nature 442 (July 6, 2006): 37; and Siegfried Weber et al., “Molecular Analysis of Highly Pathogenic Avian Influenza Virus of Subtype H5N1 Isolated from Wild Birds and Mammals in Northern Germany,” Journal of General Virology 88 (2007): 554-58.
323 fallen sick in Turkey: For details, see Ahmet Faik Oner et al., “Avian Influenza A (H5N1) Infection in Eastern Turkey in 2006,” NEJM 355, no. 21 (Nov. 23, 2006): 2179-85.
323 the famed bird market: Elaine Sciolino, “In the Land of Coq au Vin, Soul Searching over Bird Flu,” New York Times, Feb. 24, 2006.
323 the ravens at the Tower of London: Mary Jordan, “Bird Flu Fears Coop Up London’s Famous Ravens,” Washington Post, Feb. 22, 2006.
323 dumped in the Nile River: Daniel Williams, “Spooked by Bird Flu, Egyptians Horde [sic] Water,” Washington Post, Feb. 26, 2006.
323 “While it was originally suspected”: “Nigeria; Bird Flu: FG Links Source to Illegal Importation of Chicks,” Africa News, Mar. 3, 2006.
323 introduced to the country three separate times: M. F. Ducatez et al., “Multiple Introductions of H5N1 in Nigeria,” Nature 442 (July 6, 2006): 37.
323 most likely along internal trade routes: “FAO Urges Nigeria to Increase Bird Flu Control Measures,” FAO news release, Feb. 20, 2007. In most of the affected Nigerian states, the flu strains continued to evolve into new forms. See Isabella Monne et al., “Reassortant Avian Influenza Virus (H5N1) in Poultry, Nigeria, 2007,” Emerging Infectious Diseases 14, No. 4 (Apr. 2008): 637-40.
324 Are wild birds the culprit: The evidence implicating wild birds has been mounting. The following is a sampling: H. Chen et al., “H5N1 Virus Outbreak in Migratory Waterfowl,” Nature 436 (July 14, 2005): 191-92; Dennis Normile, “Are Wild Birds to Blame?” Science 310, no. 5747 (Oct. 21, 2005): 426-28; Robert G. Webster et al., “H5N1 Outbreaks and Enzootic Influenza,” Emerging Infectious Diseases 12, no. 1 (Jan. 2006): 3-8; H. Chen et al., “Establishment of Multiple Sublineages of H5N1 Influenza Virus in Asia: Implications for Pandemic Control,” PNAS 103, no. 8 (Feb. 21, 2006): 2845-50; Dennis Normile, “Evidence Points to Migratory Birds in H5N1 Spread,” Science 311, no. 5765 (Mar. 3, 2006): 1225; Bjorn Olsen et al., “Global Patterns of Influenza A Virus in Wild Birds,” Science 312, no. 5772 (Apr. 21, 2006): 384-88; Marius Gilbert et al., “Anatidae Migration in the Western Palearctic and the Spread of Highly Pathogenic Avian Influenza Virus H5N1 Virus,” Emerging Infectious Diseases 12, no. 11 (Nov. 2006): 1650-56; Raja Sengupta et al., “Ecoregional Dominance in Spatial Distribution of Avian Influenza (H5N1) Outbreaks,” Emerging Infectious Diseases 13, no. 8 (Aug. 2007): 1269-70; Juthatip Kwawcharoen et al., “Wild Ducks as Long-Distance Vectors of Highly Pathogenic Avian Influenza Virus (H5N1),” Emerging Infectious Diseases 14, no. 4 (Apr. 2008): 600-606; Donata Kalthoff et al., “Pathogenicity of Highly Pathogenic Avian Influenza Virus (H5N1) in Adult Mute Swans,” Emerging Infectious Diseases 14, no. 8 (Aug. 2008): 1267-70; and A. Townsend Peterson et al., “Influenza A Virus Infections in Land Birds, People’s Republic of China,” Emerging Infectious Diseases 14, no. 10 (Oct. 2008): 1644-46.
324 Or is it trade in poultry: There is also a body of evidence indicating that the role of wild birds in spreading the virus is less significant than that of commerce. See, for example, D. S. Melville and Kennedy F. Shortridge, “Influenza: Time to Come to Grips with the Avian Dimension,” Lancet Infectious Diseases 4, no. 5 (May 2004): 261-62; Chris J. Feare, “The Role of Wild Birds in the Spread of HPAI H5N1,” Avian Diseases 51, no. S1 (2007): 440-47; M. Gauthier-Clerc, C. Lebarbenchon, and F. Thomas, “Recent Expansion of Highly Pathogenic Avian Influenza H5N1: A Critical Review,” Ibis 149 (2007): 202-14; Thomas P. Weber and Nikolaos I. Stilianakis, “Ecological Immunology of Avian Influenza (H5N1) in Migratory Birds,” Emerging Infectious Diseases 13, no. 8 (Aug. 2007): 1139-43; and “Don’t Blame Wild Birds for H5N1 Spread—Expert,” Reuters, Jan. 23, 2008.
324 both these opportunities: See, for example, Joseph Domenech et al., “Trends and Dynamics of HPAI—Epidemiological and Animal Health Risks,” Background Paper at the Technical Meeting on Highly Pathogenic Avian Influenza and Human H5N1 Infection, Rome, June 27-29, 2007; and A. Marm Kilpatrick et al., “Predicting the Global Spread of H5N1 Avian Influenza,” PNAS 103, no. 51 (Dec. 19, 2006): 19368-73. For a wide-ranging examination of the role wild birds play in the spread of the virus, see the presentations at the FAO-OIE International Scientific Conference on Avian Influenza and Wild Birds, Rome, May 30-31, 2006.
324 “far from over”: “New Avian Influenza Flare-ups,” FAO news release, Jan. 24, 2008.
324 “finally cause a human influenza pandemic”: “Bird Flu Situation in Indonesia Critical,” FAO news release, Mar. 18, 2008.
325 actively undergoing genetic changes: On the endemicity and continuing evolution of the virus in Indonesia, see Tommy Tsan-Yuk Lam et al., “Evolutionary and Transmission Dynamics of Reassortant H5N1 Influenza Virus in Indonesia,” PLoS Pathogens 4, no. 8 (Aug. 2008): e1000130.
325 only a few localities were completely capable: Minister of Agriculture and Rural Development Cao Duc Phat, quoted in “Vietnam Preventive Measures Are Not Enough,” Thai Press Reports, Mar. 24, 2008.
325 poultry vaccination program was flagging: Deputy Minister of Agriculture and Rural Development Bui Ba Bong, quoted in “Half-Done Vaccination Poses High Bird-Flu Risk,” Saigon Times Daily, Mar. 13, 2008.
325 would be unable to keep paying: See, for example, Jan Slingenbergh, senior officer of the FAO’s Animal Production and Health Service in “H5N1 HPAI Pathogenicity Rising, but Situation in Check,” FAOAIDE news, Situation Update 55, July 25, 2008.
325 were both becoming more lethal: Mary Pantin-Jackwood of the U.S. Department of Agriculture and colleagues from the Viet Nam National Centre for Veterinary Diagnosis in “H5N1 HPAI Pathogenicity Rising.” FAOAIDE news, Situation Update 55, July 25, 2008.
325 “We still have a very serious situation”: “China Needs Better Bird Flu Surveillance Experts,” Reuters, Feb. 18, 2009.
326 the Thai government launched: Supamit Chunsuttiwat, “Response to Avian Influenza and Preparedness for Pandemic Influenza: Thailand’s Experience,” Respirology 13, suppl. 1 (2008): S36-S40; and Kumnuan Ungchusak, “What Happened When the H5N1 Virus Visited Thailand,” lecture at the Asia Medical Forum, Lancet 2006, in Singapore, May 4, 2006.
326 continued to detect the virus: Alongkorn Amonsin et al., “Influenza Virus (H5N1) in Live Bird Markets and Food Markets, Thailand,” Emerging Infectious Diseases 14, no. 11 (Nov. 2008): 1739-42.
326 “Some commercial producers”: E-mail from Juan Lubroth, Aug. 11, 2006, citing information from the U.S. Agency for International Development.
326 a baffling transplant: “New Bird Flu Strain Detected in Nigeria,” FAO news release, Aug. 11, 2008. For more discussion see Alice Fusaro et al., “Introduction into Nigeria of a Distinct Genotype,” Emerging Infectious Diseases, 15, no. 3 (March 2009): 445-47.
326 “Somewhat surprising”: “Bird Flu Returns to Germany,” Deutsche Welle, Oct. 9, 2008.
326 “particularly worrying”: “New Avian Influenza Flare-ups,” FAO news release, Jan. 24, 2008.
326 “a new chapter in the evolution”: “Bird Flu Virus in Europe—a Hidden Danger,” FAO news release, Oct. 25, 2007.
327 “We must never forget”: “Concern Over Flu Pandemic Justified,” Address to the Sixty-second World Health Assembly, Geneva, Switzerland, May 18, 2009.
327 “Do not drop the ball”: “World Is Better Prepared for Influenza Pandemic,” Address to the ASEAN+3 Health Ministers’ Special Meeting on Influenza A (H1N1), Bangkok, Thailand, via teleconference, May 8, 2009.
327 For each one of those fatalities: Juan Lubroth, a senior FAO official, estimated in June 2008 that 240 million birds had died or been slaughtered. Julia Zappei, “Health Experts: Global Fight Against Bird Flu Remains Weak, Can Worsen Global Food Crisis,” Associated Press, June 20, 2008.
327 reducing the circulation of these viruses in animals: The likelihood of altogether eliminating the H5N1 virus is at best slim. Animal-health expert Les Sims, who first confronted this strain in Hong Kong in 1997 and has followed it since, writes, “The prospects of global eradication of H5N1 HPAI viruses circulating in Asia, Africa and Europe within the next 10 to 20 years is poor. Unless the viruses change or there are major shifts in the way poultry are reared, arising from accelerated rural development, they may never be eradicated.” Les D. Sims, “Lessons Learned from Asian H5N1 Outbreak Control,” Avian Diseases 51, no. S1 (2007): 174-81.
328 relations were strained: See, for example, the discussion over sample sharing between the agencies in Declan Butler, “‘Refusal to Share’ Leaves Agency Struggling to Monitor Bird Flu,” Nature 435 (May 12, 2005): 131.
328 cash-strapped veterinary counterparts: Senior officials at the World Organization for Animal Health, known by its French initials OIE, offered a similar critique: “Although financial resources have been targeted to the human health rather than the animal health field under the pressure of a possible human pandemic, the main message… remains that the viral load in the environment and therewith the risk of a pandemic should be diminished by eradication of the virus at its animal source.” Christianne Bruschke, Alex Thiermann, and Bernard Vallat, “Implementing Appropriate OIE/FAO Prevention Measures in Different Country Contexts,” Background Paper at the Technical Meeting on Highly Pathogenic Avian Influenza and Human H5N1 Infection, Rome, June 27-29, 2007.
330 “The present situation is unique”: “Sharing of Influenza Viruses and Access to Vaccines and Other Benefits,” Opening Remarks at the Intergovernmental Meeting on Pandemic Influenza Preparedness, Geneva, Nov. 20, 2007.
330 Researchers initially concluded: Christophe Fraser et al., “Pandemic Potential of a Strain of Influenza A (H1N1): Early Findings,” Science, published online before print May 11, 2009, doi: 10.1126/science.1176062.
330 no greater than that for ordinary flu bugs: Dr. Daniel Jernigan, deputy director of the CDC Influenza Division, at a CDC telebriefing on the investigation of human cases of H1N1 flu, May 20, 2009.
330 planning for hospitals and public health systems remains wanting: See, for example, Christopher Lee, “U.S. flu Outbreak Plan Criticized,” Washington Post, Feb. 2, 2008.