The Fatal Strain (55 page)

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.

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.