by Alan Sipress
Chapter Eight: Sitting on Fire
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.
22
2 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.
Chapter Nine: The Secret Call
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 confidenti
al 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.
