Summary and Assessment1

The emergence of a novel human coronavirus in late 2002 alarmed populations across the globe, elicited a massive public health response, gave rise to a multinational research network, gripped the news media, wreaked political havoc in China, and struck a blow to the tourism and travel industries of several countries. By the time this coronavirus, labeled SCoV, apparently receded from human hosts in July 2003, nearly 10 percent of more than 8,000 individuals who fit the probable case definition had died of the disease now known as severe acute respiratory syndrome (SARS) (World Health Organization [WHO], 2003a). Analyses of this epidemic could lead to improvements in the global community’s preparedness for and response to future global outbreaks of infectious disease.2

For these reasons, the Institute of Medicine’s (IOM’s) Forum on Microbial Threats convened the workshop Learning from SARS: Preparing for the Next

1  

The speed with which the SARS epidemic spread last year was matched by a similar swiftness in the rate at which the understanding of the disease and its effects evolved among scientists, public health officials, and other members of the global health community. For this reason, individual papers within this volume are likely to reflect different stages and perspectives from among the many attempts that have been made to assess the course of the epidemic at different times and places. In some cases, analyses of public health responses or variations in empirical data (such as the number of suspected SARS cases or SARS-related deaths) may reflect the fluid nature of these circumstances. For the most current updates on SARS and recommendations for clinicians and public health officials, readers are referred to the relevant websites of the WHO (http://www.who.int/csr/sars/en/) and the CDC (http://www.cdc.gov/ncidod/sars/).

2  

This report entered final production before the January 5, 2004, confirmation of the first SARS case since July 2003—explaining the references throughout the report to the uncertainty about the reemergence of the disease.



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Learning From Sars: Preparing for the Next Disease Outbreak - Workshop Summary Summary and Assessment1 The emergence of a novel human coronavirus in late 2002 alarmed populations across the globe, elicited a massive public health response, gave rise to a multinational research network, gripped the news media, wreaked political havoc in China, and struck a blow to the tourism and travel industries of several countries. By the time this coronavirus, labeled SCoV, apparently receded from human hosts in July 2003, nearly 10 percent of more than 8,000 individuals who fit the probable case definition had died of the disease now known as severe acute respiratory syndrome (SARS) (World Health Organization [WHO], 2003a). Analyses of this epidemic could lead to improvements in the global community’s preparedness for and response to future global outbreaks of infectious disease.2 For these reasons, the Institute of Medicine’s (IOM’s) Forum on Microbial Threats convened the workshop Learning from SARS: Preparing for the Next 1   The speed with which the SARS epidemic spread last year was matched by a similar swiftness in the rate at which the understanding of the disease and its effects evolved among scientists, public health officials, and other members of the global health community. For this reason, individual papers within this volume are likely to reflect different stages and perspectives from among the many attempts that have been made to assess the course of the epidemic at different times and places. In some cases, analyses of public health responses or variations in empirical data (such as the number of suspected SARS cases or SARS-related deaths) may reflect the fluid nature of these circumstances. For the most current updates on SARS and recommendations for clinicians and public health officials, readers are referred to the relevant websites of the WHO (http://www.who.int/csr/sars/en/) and the CDC (http://www.cdc.gov/ncidod/sars/). 2   This report entered final production before the January 5, 2004, confirmation of the first SARS case since July 2003—explaining the references throughout the report to the uncertainty about the reemergence of the disease.

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Learning From Sars: Preparing for the Next Disease Outbreak - Workshop Summary Disease Outbreak on September 30 and October 1, 2003. Participants discussed the emergence, detection, spread, and containment of SARS; political responses to the epidemic; its economic consequences; basic research on coronaviruses; preparations for a possible reemergence of SCoV; and lessons learned from the SARS epidemic that could shape responses to future microbial threats. This workshop summary does not contain consensus recommendations, nor does it represent a consensus opinion of the IOM Forum on Microbial Threats. Rather, it presents the individual perspectives and research of people who made presentations at the IOM workshop on SARS or who participated in workshop discussions. While the workshop attempted to explore a range of issues that emerged from the SARS outbreak, it is important to recognize that neither the discussions nor this report provide an exhaustive survey of the body of knowledge about SARS. Some important issues not addressed through workshop discussions include analyses of modes of transmission in indoor environments, especially airplanes; consideration of major technological breakthroughs or new fields of inquiry that would significantly advance our ability to prevent and treat infectious diseases; and comparative analyses of actions and outcomes related to the public health responses of different countries. It should also be noted that considerable effort was made to engage the participation of more Chinese colleagues in the presentations and discussion of the workshop. The short time during which the workshop was organized made it very difficult for Chinese counterparts to obtain the necessary travel visas. Contributions from Chinese participants were important to the workshop as were additional phone and email consultations to the development of this report. The following text summarizes what transpired during the workshop and assesses how the world’s experience with SARS could potentially guide preparations by the public health community, researchers, and policy makers for future outbreaks of infectious disease. OVERVIEW OF THE SARS EPIDEMIC SARS is unremarkable in certain ways among infectious diseases. For example, the transmission rate of SCoV pales in comparison with those of other known microbial threats, such as influenza, but appears to be similar to that of smallpox. Despite nationwide vaccination campaigns against influenza in the United States, an average of 36,000 U.S. residents die annually from influenza infections—nearly 50 times more people than the number killed by SARS worldwide (Centers for Disease Control and Prevention, 2002). Yet the quality, speed, and effectiveness of the public health response to SARS brilliantly outshone past responses to international outbreaks of infectious disease, validating a decade’s worth of progress in global public health networking. Thus, in several respects, the SARS epidemic reflected fundamental

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Learning From Sars: Preparing for the Next Disease Outbreak - Workshop Summary improvements in how the world responds to an outbreak of infectious disease; and at the same time, highlights the continuing need for investments in a robust response system that is prepared for the next emerging disease—whether naturally occurring or intentionally introduced. The World Health Organization (WHO) deserves credit for initiating and coordinating much of this response through its Global Outbreak Alert and Response Network (GOARN), as do the partner organizations comprising 115 national health services, academic institutions, technical institutions, and individuals. In the future, this public health network—originally developed to manage outbreaks of influenza and other infectious diseases—ideally will encompass more partners and have the capacity to handle outbreaks of greater magnitude than SARS. Nevertheless, it is clear that multinational, collaborative, and coordinated surveillance, research, and containment measures greatly limited the spread of SCoV. Despite the low transmission rate of SCoV and the relatively low number of SARS deaths compared to other infectious diseases, SARS had a remarkably powerful and negative psychological impact on many populations worldwide. The relatively high case fatality rate, the identification of superspreaders, the newness of the disease, the speed of its global spread, and public uncertainty about the ability to control its spread may have contributed to the public’s alarm. This alarm, in turn, may have led to behavior that exacerbated the economic blows to the travel and tourism industries of the countries with the highest number of SARS cases. In addition, the SARS epidemic starkly outlined the benefits and dangers of the impact of globalization on infectious disease. The ease and frequency of international travel facilitated the swift spread of SCoV infections to 5 countries within 24 hours and to more than 30 countries on 6 continents within 6 months (WHO, 2003a). Likewise, the increased migration of workers from rural to urban areas within their home country or into different countries (and continents) has increased the risk that new and previously unrecognized viruses will become established in worldwide human populations. Yet at the same time, worldwide telecommunications networks facilitated collaborative research among 11 geographically distinct laboratories, helping them to identify this new infectious agent in just 1 month. The news media, individuals, and public health organizations disseminated information about SARS almost in real time, influencing behavior that helped limit the spread of the virus. It was also suggested that this information ultimately created heightened awareness and pressure within the Chinese government and public to take action against the SARS and to engage with the global efforts of research, prevention, and containment. A complex set of factors underlies the emergence and spread of microbial threats. The extraordinary capacity of microbes to change and adapt, the disruption of human and microbial environments, and the activities that expose humans

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Learning From Sars: Preparing for the Next Disease Outbreak - Workshop Summary November 2002: First case of SARS occurs in Guangdong Province, China. November January 2002 2004 to new microbes all play a role. The convergence of these and other factors lead to the emergence of infectious diseases, as illustrated in Figure S-1. Emergence of SARS Such a convergence likely occurred during late 2002 in southern China, where merchants and farmers took small wild mammals from their native environments to local markets and sold both slaughtered and live animals for human consumption. Some of these mammals most likely carried a coronavirus resembling SCoV (Guan et al., 2003). The likelihood of human exposure to the virus is quite high when the crowded and relatively unsanitary conditions of these markets are considered. As a result, SARS emerged in the southern Chinese province of Guangdong in late 2002. The index case, retrospectively identified on November 16, occurred in the city of Foshan; by mid-December, SARS had appeared in two additional cities in the province. An expert team from the provincial government and the national Ministry of Health went to the city of Zhongshan to investigate one of these outbreaks. The team concluded on January 21, 2003, that the infection was atypical pneumonia probably caused by a viral agent. The team recommended measures for the prevention and treatment of infection and suggested that a case reporting system be established to monitor the disease. The investigative team’s findings were reported to every hospital in the province. Unfortunately, the reporting of these findings coincided with the Chinese New Year holiday. This compounded the challenge for early intervention against the disease in two ways: the report did not receive significant attention from health officials on leave; and the opportunities for disease spread were greatly enhanced by the travel that often accompanies the celebration of the New Year.3 Additionally, as we discuss later in this chapter, the medical community’s understanding of the true etiology of SARS was delayed significantly by a February announcement from a senior scientist at the Chinese Center for Disease Control that he suspected the infectious agent was Chlamydia—a commonly understood bacterial agent that would not have warranted heightened concern or investigation. 3   Workshop presentation, Yi Guan, University of Hong Kong, September 30, 2003.

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Learning From Sars: Preparing for the Next Disease Outbreak - Workshop Summary January 21, 2003: Guangdong provincial investigators report on “atypical” pneumonia. January 31, 2003: First super-spreading SARS patient. November January 2002 2004 FIGURE S-1 The Convergence Model. This diagram illustrates how four factors that influence the interaction between humans and microbes may converge in such a way that an infectious disease emerges (central box). The interior of the central box is black, representing the unknown influences on emergence, and the lightening to white at the edges of this box represents the known influences. SOURCE: IOM (2003).

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Learning From Sars: Preparing for the Next Disease Outbreak - Workshop Summary February 11, 2003: Chinese Ministry of health reports to WHO on respiratory disease in Guangdong. November January 2002 2004 On January 31, the first hyperinfective, or superspreading, case of SARS occurred in the city of Guangzhou. The patient was transferred among three hospitals and infected an estimated 200 people, many of them hospital workers. As these events unfolded, the international public health community began to receive news of the outbreak through e-mails, Internet chat rooms, and local media outlets, whose reports were widely disseminated through electronic reporting systems such as the Global Public Health Intelligence Network (GPHIN) and Pro-MED mail (Eysenbach, 2003). Based on this information, WHO queried the Chinese government on February 10 and received a response the following day describing an outbreak of an acute respiratory syndrome involving 305 cases and five deaths in Guangdong Province (WHO, 2003b). Some of the most severe SARS symptoms were suffered by residents of the Amoy Gardens apartment towers in Hong Kong during an outbreak in late March that sickened more than 300 people (WHO, 2003c). Rather than its usual route of transmission by respiratory droplets, the virus is thought to have spread via aerosolized fecal matter through the internal sewer system of the apartment complex (WHO, 2003f). Consequently, on March 31, Hong Kong’s health authorities issued an unprecedented quarantine order to halt the spread of SARS on the island, which required some residents of the housing complex to remain in their apartments until midnight of April 9 (10 days later) (WHO, 2003c). Spread of the SARS Coronavirus Beyond China Epidemiological investigations revealed that the spread of SCoV outside China began on February 21, 2003, when 12 people staying in the Metropole Hotel in Hong Kong contracted SCoV from an infected, symptomatic physician from Zhongshan University (see Figure S-2). These 12 people subsequently carried the infection with them to Singapore, Vietnam, Canada, Ireland, and the United States—initiating chains of infection in all of these countries except for Ireland. According to WHO estimates, most of the more than 8,000 probable cases of SARS worldwide originated with this superspreader (WHO, 2003a). Vietnam Dr. Carlo Urbani, a WHO infectious disease specialist based in Vietnam, reported concerns about a patient in the Hanoi French Hospital with a high

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Learning From Sars: Preparing for the Next Disease Outbreak - Workshop Summary February 18, 2003: Senior microbiologist at Chinese Center for Disease Control announces he suspects the disease is Chlamydia. November January 2002 2004 fever and atypical pneumonia to WHO’s Western Pacific office on February 28 (WHO, 2003c). Responding to Dr. Urbani’s alert and other reports of atypical pneumonia in Vietnam and Hong Kong, WHO sent GOARN teams to Hong Kong and Hanoi to join the investigative and containment efforts already underway. The early detection of SARS in Vietnam, prompt sharing of that information with the international community, and aggressive containment efforts by the Vietnamese government, in partnership with a GOARN team, enabled FIGURE S-2 Portrait of a superspreader: spread of SARS from the Metropole Hotel in Hong Kong as of March 28, 2003.

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Learning From Sars: Preparing for the Next Disease Outbreak - Workshop Summary February 21, 2003: Worldwide epidemic begins at Metropole Hotel, Hong Kong. November January 2002 2004 the Vietnamese to eradicate SARS by the end of April. This was accomplished before SARS was contained in either Canada or Singapore, despite Vietnam’s comparatively limited health care resources and lower education levels among its population. (Tragically, Dr. Urbani himself died of SARS.) It was suggested by workshop participants that containment of the disease in Vietnam was, in fact, aided by the absence of more sophisticated medical devices and facilities—such as mechanical ventilation by intubation, bronchoscopy, aerosolized medications, and large hospital facilities that exposed large numbers of individuals to undiagnosed SARS patients awaiting care—which have been identified as factors that promoted SCoV transmission considerably in Singapore and Toronto (Lee et al., 2003). On March 12, WHO issued a global alert describing outbreaks of the yet-unnamed respiratory disease in Hong Kong and Vietnam and instituted worldwide surveillance (WHO, 2003d). A second alert on March 15 named the condition, listed its symptoms, and advised travelers to have a high level of suspicion of SARS and report to a health worker if they had SARS symptoms and had visited an area where SARS was known to be occurring. Two further alerts provided recommendations for airports to screen passengers and for travelers to avoid areas where SARS had been detected, respectively (WHO, 2003e). Canada Canada’s experience with SARS illustrates the importance of identifying and isolating every infected individual in stemming the spread of the disease. There, the index patient returned to Toronto from Hong Kong on February 23, developed a febrile illness that was diagnosed as pneumonia, then died at home on March 5. Her son, who cared for her, subsequently became ill and on March 7 was admitted to a hospital, where he infected many patients and members of the staff. He died there on March 13, one day after WHO issued its first global alert. In this, the first phase of the Toronto epidemic, unrecognized patients who shared rooms with the son went on to infect scores of other patients, family members, and hospital workers. This scenario was repeated in several area hospitals, as well as others around the globe, even after increased infection control measures were undertaken. Realizing that SARS was not contained within a single hospital, Ontario declared a provincial emergency on March 26 that halted the transfer of patients among hospitals, instituted infection control measures and created SARS units within hospitals, minimized visitor access to hospitals, and established a process

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Learning From Sars: Preparing for the Next Disease Outbreak - Workshop Summary February 28, 2003: Atypical pneumonia reported in Hanoi, Vietnam. November January 2002 2004 to screen all persons entering hospitals for symptoms of SARS. Because the spread of SARS in Toronto was largely restricted to the hospital setting, these precautions were effective in controlling the outbreak. When a second phase of SARS occurred in mid-May, after emergency measures were relaxed, it was quickly brought under control with little spread outside the affected hospital (See D. Low in Chapter 1). A similar lapse in infection control in a Taiwan hospital ignited an outbreak in mid-April (WHO, 2003g). Health authorities responded quickly by increasing surveillance, redoubling infection control measures, and launching a mass education campaign credited with reducing the time between symptom onset and patient isolation. Singapore Rapid contact tracing by health authorities in Singapore, where scores of SARS cases had been reported, linked that country’s index case to the Metropole Hotel by April 4. Singaporean authorities imposed strict containment measures, including contact tracing and 10-day quarantine for all contacts of known SARS patients, as well as screening for fever among incoming and outgoing passengers at all airports and seaports. One indication of the effectiveness of these measures is the fact that 80 percent of Singapore’s SARS patients did not infect anyone else (WHO, 2003h; Singapore Government, 2003). On September 8, an isolated case of SARS was reported in Singapore, and subsequently confirmed by the U.S. Centers for Disease Control and Prevention (CDC) (WHO, 2003l). The patient, a 27-year-old microbiology postdoctoral student, had no history of travel to SARS-affected areas or contact with SARS patients. Rather, he apparently become infected through a laboratory accident stemming from the contamination of samples containing West Nile virus, the subject of the patient’s research, with the SCoV, which was also being studied in the same biosafety level 3 facility. THE IMPACT OF THE SARS EPIDEMIC As the SARS coronavirus spread around the globe, so did its political, sociological, and economic repercussions. Workshop participants described the official reaction to the outbreak in China, examined the political and public health implications of how China acknowledged and confronted the full dimensions of the epidemic on national and international levels, and assessed the immediate and long-term economic

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Learning From Sars: Preparing for the Next Disease Outbreak - Workshop Summary March 7, 2003: Son of Toronto index patient enters Scarborough Grace Hospital, initiating outbreak. November January 2002 2004 impact of SARS. Central to these discussions was the recognition of the extreme pressure SARS exerted on both international and local health care systems and the frightening prospect of future outbreaks of greater contagion or virulence. The multinational effort to contain SARS placed unprecedented demands on affected and unaffected countries to accurately identify and report cases in a timely manner, to cooperate with GOARN expert teams of scientists and medical personnel coordinated by WHO, and to sacrifice immediate economic interests (e.g., travel, trade, tourism). Without international legal obligation to report SARS, most countries did so fully. Yet this extraordinary alliance would have failed without the full cooperation of China, the epicenter of the epidemic. Politics, Tradition, and the Chinese Response to SARS Workshop participants asserted that China’s problems in dealing with the SARS epidemic were fundamentally rooted in organizational obstacles. Problems cited during the workshop included impediments to the flow of information through the governmental hierarchy, a lack of coordination among fragmented governmental departments, and a political system in which the value of handling problems internally overrides any recognized value of external assistance. Importantly, workshop participants noted that these systemic failings are not exclusive to China and impede the response to public health and other social problems in a large number of countries around the world. Uniquely, the Chinese tradition of respect for senior scientists in positions of authority may have substantially influenced the behavior of the Chinese Center for Disease Control and of other Chinese scientists who were researching the epidemic (Enserink, 2003). A highly respected Chinese scientist reportedly claimed that Chlamydia infection caused SARS, based on an examination of only two specimens. This may have led the Chinese Center for Disease Control and other Chinese clinicians and scientists to maintain that Chlamydia was the SARS agent, despite other evidence inside China indicating that the agent was viral. Consequently, virologists in a Beijing laboratory refrained from announcing their discovery in early March of the SARS coronavirus, a decision that set back by weeks research on the disease and a more significant public health response in China (Enserink, 2003). The SARS epidemic also exposed weaknesses in China’s public health infrastructure, including inadequate state funding, lack of effective surveillance systems, and severe shortages in facilities and medical staff prepared for an epidemic infec-

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Learning From Sars: Preparing for the Next Disease Outbreak - Workshop Summary March 10, 2003: WHO teams arrive in Hong Kong and Hanoi. March 12, 2003: First WHO global alert issued on yet-unnamed disease. November January 2002 2004 tious disease outbreak. As a forewarning, a workshop participant observed that these same weaknesses are often cited by medical and public health experts when assessing the state of preparedness for infectious disease outbreaks in the United States.4 These statements corresponded with other participants who suggested that, in the case of SARS, the United States was perhaps more lucky than it was prepared. In response to the deficiencies highlighted by SARS, the Chinese government established a case reporting structure, strengthened its emergency response system, dismissed key officials who mismanaged the crisis during its initial months, and provided funding for the prevention and control of SARS. Chinese workshop participants also credited the SARS experience for increasing the recognition and understanding of government officials and the public about the importance of infectious disease control and prevention in general.5 Economic Impact While the most immediate and dramatic economic effects of SARS occurred in Asia, every market in today’s global economy was at some point impacted directly or indirectly by the epidemic. Several agencies and experts have attempted to estimate the cost of SARS based on near-term expenditures and losses in key sectors such as medical expenses, travel and related services, consumer confidence, and investment. One model estimated that the short-term global cost of lost economic activity due to SARS was approximately $80 billion.6 Participants agreed, however, that the true economic consequences of SARS remain to be determined, particularly given the possibility of its return. An economic model presented at the workshop estimated the impact of SARS on several countries—and in aggregate, on the world. It considered two different scenarios: a short-term shock coincident with a one-time epidemic, and long-term effects typical of recurring outbreaks. The model was not intended to 4   See IOM, 2003; General Accounting Office, 2001; National Intelligence Council, 2000. 5   During the development of the this report, a Chinese author commented that the recent commitment by the highest level of Chinese government officials to the prevention and treatment of AIDS, after years of little public recognition of the disease or its victims, might in large part be credited to the new awareness by all Chinese of the threats posed by unchecked infectious diseases. 6   Workshop presentation by Warwick McKibbin, Australia National University, September 30, 2003.

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Learning From Sars: Preparing for the Next Disease Outbreak - Workshop Summary July 5, 2003: SARS contained in Taiwan; WHO declares containment of worldwide epidemic. November January 2002 2004 about the nature of future novel pathogens anticipate the emergence of zoonoses. Thus, workshop participants considered the strategies for containing known zoonoses—in particular, influenza—as potential models for the containment of SARS and unidentified zoonotic diseases of the future. Lessons Learned from Influenza The same trends that ushered SARS into the human population have been apparent during a century of influenza outbreaks. The exponential increase in avian influenza virus infections among humans over the past decade has been associated with a sharp rise in the size and density of chicken and pig farm populations, their proximity to human settlements, and movement of animals through market channels, which in turn parallels the world’s rapidly expanding and mobile population. As with SARS, animal markets provide the breeding ground for recent outbreaks of influenza; laboratory sources also appear to have sparked at least one epidemic. Fortunately, most of the recent influenza outbreaks did not feature the transmission of the virus to humans. However, experts agree that it is only a matter of time until a highly virulent and contagious flu, such as the strain that caused over 20 million and perhaps as many as 40 million deaths during the 1918 influenza epidemic, confronts the world (see Webby and Webster in Chapter 5).13 Vaccines and antiviral therapies play a significant role in containing epidemics of influenza. It is advantageous that the timing of annual outbreaks of influenza and the strain or strains of the virus can, to some extent, be anticipated. However, strategic actions recommended against influenza that could also inform efforts to better prepare for other viral disease outbreaks have yet to be implemented. These strategies include:14 13   Shortly before the publication of this report in January 2004, the highly pathogenic H5N1 avian influenza virus was implicated in a human outbreak of the disease in Vietnam and Thailand. Sixteen of the 20 individuals so far infected have died. Thousands of birds in eight countries, including Vietnam, The Republic of Korea, Thailand, China, and Japan are suspected to be infected with the virus. See http://www.who.int/en/disease outbreaks for more information. 14   Workshop presentation, Robert Webster, St. Jude’s Children’s Research Hospital, October 1, 2003.

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Learning From Sars: Preparing for the Next Disease Outbreak - Workshop Summary September 8, 2003: Isolated case of SARS occurs in Singapore due to laboratory accident. November January 2002 2004 stockpiling of broad-spectrum antiviral drugs, advanced development of pandemic strain vaccines, the establishment of surge capacity for rapid vaccine production, and the development of models to determine the most effective means of delivering therapies during an outbreak. It is evident from the experience of the late 2003 influenza season that our supply and effectiveness of antiviral drugs, capabilities to accurately predict the best viral strain for annual vaccine production, and mechanisms for surge capacity production remain inadequate (Treanor, 2004; WHO, 2003o). Recognition of these vulnerabilities lead numerous workshop participants to call for greater scientific and financial investments to strengthen our defenses against these certain future threats. Quarantine Some emerging infections of the future, like SARS, may be truly novel threats for which the world—including its pharmacopoeia—is inadequately prepared. Lacking other forms of effective interventions, the implementation of quarantine or isolation strategies may prove valuable in such instances. Workshop participants discussed several ways that modeling tools might be used to improve and tailor such measures. Models based on detailed observations from previous epidemics can be used to predict demands on hospital capacity during a hypothetical epidemic and to guide the timing and nature of quarantine measures. Models that can estimate the length and severity of an unfolding epidemic will likely increase public acceptance of quarantine by permitting people to form realistic expectations of their sacrifice and its benefit to the community (see Amirfar et al. in Chapter 5). Evidence indicates that a modern approach to quarantine encompassing a range of options designed to reduce the frequency of social contact can significantly reduce the spread of infectious disease. Such options include short-term, voluntary home curfew; suspension or cancellation of public activities (such as events, mass transit, or access to public buildings); and “snow day” or sheltering-in-place measures. These measures could be employed individually or in concert. In addition to or in place of these strategies, a program of contact surveillance—the monitoring of asymptomatic persons exposed to an infectious disease—could be undertaken. Modern quarantine and contact surveillance preserve individual liberties and require far less labor and other community re-

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Learning From Sars: Preparing for the Next Disease Outbreak - Workshop Summary December 5, 2003: Taiwanese researcher contracts SARS during experiment. November January 2002 2004 sources than would be required to enforce a mandatory quarantine. Voluntary and other forms of scalable quarantine nevertheless reduce productivity and may result in public perceptions that stigmatize groups of individuals and promote irrational behavior. For example, there is evidence that consumers began to avoid Asian restaurants in the United States and other nonaffected countries during the SARS epidemic even though neither quarantine nor public health messages suggested such action. For any quarantine to be effective, workshop participants noted, a number of needs must be met, including: education to build public trust in health authorities, compensation and job security for quarantined workers, and incentives to health care workers to maintain their morale in the face of increased risk and to pay greater attention to infection control practices. In the more difficult case of mandatory quarantine, enforcement requires careful planning and a clear understanding of public health law; this is particularly true in the United States, where quarantine is likely to necessitate the coordination of federal, state, and local jurisdictions and legal authorities. For example, if an infectious disease has the potential to spread across state boundaries but has not yet done so, an action by CDC to limit transmission would require the cooperation of appropriate state and local authorities. The presidential executive order adding SARS to a list of other diseases subject to federal quarantine actions eliminated such jurisdictional uncertainties (Executive Order 13295: Revised List of Quarantinable Communicable Diseases, 2003). Additional legal considerations include planning for due process—proper notice, legal representation, court-reviewed decisions, and remote communications to permit a quarantined person to be heard in court—and for practical contingencies, such as the need for law enforcement officials to serve notice of quarantine (see Matthews in Chapter 5). Workshop participants also discussed the need to develop strategies by which hospitals—and entire communities, in the event of quarantine—can determine when precautions against infection can be scaled back. Some experts have argued that containment measures should be swiftly imposed in response to a perceived infectious disease threat (as occurred when SARS appeared in Vietnam) and reduced only after surveillance determines the absence of a threat. Clearly, the consequences of false alarms in this case must be weighed against the risks of

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Learning From Sars: Preparing for the Next Disease Outbreak - Workshop Summary December 7-10, 2003: Infected researcher attends conference in Singapore. November January 2002 2004 inaction in the early stages of an epidemic, as demonstrated by China’s experience with SARS. Informing the Public Although no presentations exclusively addressed the subject of public communication, this topic was identified as important and was widely discussed by workshop participants. Social cohesion and compliance with quarantine in Toronto were attributed in part to a combination of clear communication and practical guidance by public health authorities. The media’s sustained and intensive focus on the epidemic, heavy traffic on informational SARS websites operated by WHO and CDC, and a great volume of calls to CDC’s SARS hotline reflect the public’s hunger for news and information during the public health emergency. Official travel and health advisories, though deemed necessary, were also linked to consumer avoidance of international travel, international events, and even Asian restaurants. It was suggested that such adverse effects could be mediated in the future by accompanying advisories with educational messages designed to help the public develop a realistic perception of the risks for infection and appropriate responses. Research designed to identify why societies respond dramatically and irrationally to certain types of public health threats might help communicators to develop messages that positively influence the public’s behavior during medical emergencies. The media’s powerful role in the response to SARS was characterized in both positive and negative terms: as a cause of stigma and discrimination due to sensationalized reporting on the epidemic; as a demystifier of quarantine and other public health measures through exhaustive coverage; and, as a persuasive contributor to China’s decision to cooperate with international efforts to control SARS. The Internet, recognized as a key source of early leads to the outbreak of SARS, was also viewed with concern for its potential to propagate false rumors. It is important to guard against such threats in the event of public health emergencies. Likewise, it will be critical to make use of the media to inform and educate the public on how best to protect themselves and their communities in the event of future outbreaks

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Learning From Sars: Preparing for the Next Disease Outbreak - Workshop Summary December 17, 2003: Singapore authorities quarantine 70 individuals. November January 2002 2004 Surge Capacity Health Care Personnel Workshop participants remarked that the strained capacity of the U.S. and global public health infrastructure—attributed to insufficient funding, labor shortages, and a lack of facilities—impedes preparations for SARS and other threats to public health. As described earlier, even some of the highly developed health care systems of Toronto struggled to cope with inadequate numbers of health care personnel (particularly because of the inevitable toll that moderately to highly contagious diseases take on health care personnel) and were ultimately unable to sustain normal levels of care for both SARS and non-SARS patients. In moving forward, workshop participants suggested that up-to-date information and skills needed for containing epidemic-prone diseases must be better integrated into the training of all health care professionals, not only those specializing in infectious diseases or infection control. In citing Toronto’s call to health care personnel in other regions and countries, a participant recommended the expansion and establishment of formal networks to rapidly identify, transport, and enlist experienced health care personnel in the event of future outbreaks. Such contingencies would be designed for local, regional, national, and international responses and, in particular, would facilitate the mobilization of human and technical resources that are known to have previously tackled certain disease outbreaks. The question was asked, if SARS is to reemerge how will we harness the skills and new knowledge of the thousands of individuals involved with finally containing the disease? While some participants lauded the efforts of GOARN and the CDC in this regard, they questioned if that was enough. Health Care Facilities The inability to effectively establish isolation areas and procedures within hospitals and other health care facilities contributed to the spread of SARS in several countries. Inadequate facilities not only promoted the spread of the disease, but also forced the suspension of other vital health care procedures. As previously described, one workshop participant suspected that more patients died during the SARS outbreak in Toronto as a result of the inability to access appropriate care for conditions other than SARS rather than from SARS itself.

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Learning From Sars: Preparing for the Next Disease Outbreak - Workshop Summary January 5, 2004: China and WHO confirm SARS case in Guangdong Province. November January 2002 2004 As such, participants called for preparedness planning that established procedures for rapid identification and use of facilities designated not only for treatment of suspected and confirmed cases of an epidemic disease, but also facilities that could be isolated for the conduct of other critical procedures such as emergency surgeries, trauma care, and organ transplantation. In this regard, several participants credited the rapid construction of “SARS hospitals” in China as a key element in ultimately containing the disease. Supporting the Research Response Years of investment in basic research on coronaviruses, largely in the veterinary research fields, helped the scientific community to identify the SARS coronavirus within months of its emergence. Consequently, numerous participants noted that the potential for future outbreaks not only justifies presentday investments in basic research on viruses and microbes, but also argues for greater attention to and investment in research efforts that integrate the direct contributions of zoonotic infectious disease research with biomedical research efforts. As noted earlier (see Box S-1), a number of basic scientific questions about the biology and epidemiology of SARS need to be answered in order to develop diagnostics and therapeutics for the disease, as well as to construct and implement targeted surveillance strategies. Apart from research that is specific to the SARS coronavirus, however, workshop participants discussed a number of broader areas of basic research that might be pursued in order to counter the threat that would arise from either a recurrence of SARS or the emergence of other new infections. First, now that the more urgent pace of responding to an ongoing epidemic has subsided, researchers should be encouraged to thoroughly and methodically take stock of data that was accumulated over the course of fighting this epidemic. Workshop participants suggested that the public health community should not be complacent about the eventual success that was had in containing last year’s SARS outbreak; there remains a need to understand exactly what strategies were most effective, what strategies were less successful or even counterproductive, and what steps would be most essential for combating the emergence of a new and possibly more virulent or more infectious pathogen. As part of this retrospective evaluation, for example, extant patient and hospital records should be assembled, compared, and analyzed in order to provide as exact an assessment as possible of the effectiveness of each of the many control

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Learning From Sars: Preparing for the Next Disease Outbreak - Workshop Summary measures that were adopted, as well as the points of greatest weakness that allowed the virus to spread. Some of the lessons to be learned will be specific to the profile of SARS, but many of them will also be readily applicable to other new infections in the crucial early stages of an epidemic when less is known about the biology of the disease than about its manner and rate of spread. On the next occasion when scientists and public health officials are confronted by a novel threat, it is important that they have a battery of well-researched studies to fall back on concerning measures that have previously been shown to be effective and feasible in controlling even a disease entity that has not yet been well characterized. Secondly, this evaluative process should expand beyond those areas encompassed by clinical medicine and emergency care. The SARS epidemic illustrated how rapidly the impacts of a new disease can reverberate through the political and economic structures of successive countries and regions, and the decisions that were made in response to the epidemic ultimately reached into the highest levels of government and international bodies. Just as with the measures that were taken within individual hospitals and clinical settings, the comparative effectiveness of the broader quarantine measures, travel advisories, communications with the general public, and other legal and public health directives that were issued should be gauged relative to their costs and difficulties. Any possible improvements in the measures that were adopted in the case of SARS—or recommendations for flexible options or combinations of options that might be applied in the face of different types of pathogens—may need to be examined within a broad and multidisciplinary discussion framework. Finally, basic research needs to be conducted into not only the measures that were most effective in containing the last epidemic but also those steps that would best facilitate research on understanding the next one. The uncertainty and confusion that are likely to be present in an epidemic’s early stages may at least be ameliorated if scientists, public health officials, and governmental bodies understand and are well prepared to collect the types of data that have been shown to be most crucial in assessing the nature and magnitude of a novel threat. A number of workshop participants commented on the need to look into better standards for data capture and coordination during the course of an epidemic, as well as the need to have better models on hand for evaluating the effects of possible intervention strategies as early as possible. Likewise, while carefully controlled therapeutic trials are often impractical (or at best extremely difficult) during the first stages of a disease outbreak, some workshop participants lamented the fact that relatively little progress was made toward developing a standard treatment algorithm for SARS patients during last year’s epidemic, and there remains significant controversy over the effectiveness of certain treatments that were applied. It was suggested that in the case of any future epidemics, better pooling of data from scattered clinical treatment

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Learning From Sars: Preparing for the Next Disease Outbreak - Workshop Summary centers could at least initiate the process of assessing the efficacy of different treatment strategies and provide groundwork for more reliable clinical advisories until the time and means are available for more thorough studies. Engaging the Private Sector Several presentations and considerable discussion concentrated on mechanisms that could potentially engage the private sector—specifically, pharmaceutical and biotechnology companies—in the research and development of products targeted at the greatest threats to public health, including infectious diseases. For pharmaceutical researchers, streamlining the development process is crucial to productive engagement in strategic research. Means of streamlining this process include the clear identification of patient and physician needs, access to detailed biological studies of the pathogen of interest, and technologies such as computational and combinatorial chemistry that speed target selection and lead generation. Workshop presenters described the need for technology to improve predictions of the safety of drug candidates so unsafe compounds could be weeded out at an early and less expensive stage of the development process. Promotion of International Cooperation and Collaboration If SARS never returns, the 2003 epidemic will nonetheless be remembered as a watershed event in the history of public health because of the degree of multinational cooperation to contain the disease. As the world becomes more conscious of microbial threats to health, countries are increasingly compelled to report infectious outbreaks and join international efforts to contain them. Recognizing that such transparency often comes at a price to a nation’s economy, particularly in developing countries, workshop participants attempted to identify incentives to encourage nations and individuals to act for the common good. Some participants offered specific ideas for incentives, including cooperative grants to support disease-monitoring efforts by academic researchers in developing countries and high-profile awards from bodies such as the Institute of Medicine or World Health Organization to countries or individuals who make important sacrifices for the health of world. Networking can also play a vital role in local and regional preparedness for infectious disease threats. Tabletop exercises, in which detailed outbreak scenarios are presented to officials who develop a response based on the tools and resources at their disposal, encourage preparedness and provide a forum for building collaborations among the many individuals and sectors essential to an effective, coordinated response. From such exercises, the real-time compilation of epidemiological, clinical, and laboratory data that could be made available to the international community through WHO could also stimulate cooperation and collaboration. When implemented via the Internet or other communication net-

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Learning From Sars: Preparing for the Next Disease Outbreak - Workshop Summary works, these exercises can be used to develop systems of communication, as well as working relationships, in advance of an outbreak or other emergency. Some countries are increasingly cognizant of the fact that the health of the global public affects the individual security of all nations, especially those that are most enmeshed in global networks of trade, tourism, and investment. Nevertheless, many governments continue to allocate inadequate resources to their health care systems and lack the political will to improve the quality of their public health systems and the integration of those systems nationally and internationally. This observation highlights an additional lesson offered by SARS, one that echoes what we have learned from HIV/AIDS, influenza, Ebola, malaria, and a host of other infectious diseases: the desperate state of public health infrastructure in much of the world, and especially in those countries where microbial threats are likeliest to emerge and take hold. If such lessons are to be heeded, global strategies to enhance the prevention and control capabilities of all nations will be important as the world prepares for future outbreaks of infectious disease. Adel A.F. Mahmoud, M.D., Ph.D. Chair, Forum on Microbial Threats Stanley M. Lemon, M.D. Vice-Chair, Forum on Microbial Threats REFERENCES Center for Disease Control Taiwan. A report on the laboratory-acquired SARS in Taiwan. [Online] Available: http://www.cdc.gov.tw/sarsen/ [accessed January 19, 2004]. Centers for Disease Control and Prevention. Public health and aging: influenza vaccination coverage among adults aged >50 years and pneumococcal vaccination coverage among adults aged >65 years—United States, 2002. MMWR 52(41):987-92. Enserink M. 2003. SARS in China. China’s missed chance. Science 301(5631):294-6. Eysenbach G. 2003. SARS and population health technology. Journal of Medical Internet Research 5(2):e14. General Accounting Office. 2001. Challenges in Improving Infectious Disease Surveillance Systems. GAO-01-722. Washington, DC: GAO. Guan Y, Zheng BJ, He YQ, Liu XL, Zhuang ZX, Cheung CLLSW, Li PH, Zhang LJ, Guan YJ, Butt KM, Wong KLCKW, Lim W, Shortridge KF, et al. 2003. Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China. Science 302(5643):276-8. Hogg C. 2003. Test for early detection of SARS. BBC News. Holmes KV. 2003. SARS coronavirus: a new challenge for prevention and therapy. Journal of Clinical Investigation 111(11):1605-9. Institute of Medicine. 2003. Microbial Threats to Health: Emergence, Detection, and Response. Washington, DC: The National Academies Press. Lee N, Hui D, Wu A, Chan P, Cameron P, Joynt GM, Ahuja A, Yung MY, Leung CB, To KF, Lui SF, Szeto CC, Chung S, Sung JJ. 2003. A major outbreak of severe acute respiratory syndrome in Hong Kong. New England Journal of Medicine 348(20):1986-94. National Intelligence Council. 2000. National Intelligence Estimate: The Global Infectious Disease Threat and Its Implications for the United States. NIE 99–17D. Washington, DC: NIC. Seto WH, Tsang D, Yung RW, Ching TY, Ng TK, Ho M, Ho LM, Peiris JS. 2003. Effectiveness of precautions against droplets and contact in prevention of nosocomial transmission of severe acute respiratory syndrome (SARS). Lancet 361(9368):1519-20.

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