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Institute of Medicine (US) Forum on Microbial Threats; Knobler S, Mahmoud A, Lemon S, et al., editors. Learning from SARS: Preparing for the Next Disease Outbreak: Workshop Summary. Washington (DC): National Academies Press (US); 2004.

Cover of Learning from SARS

Learning from SARS: Preparing for the Next Disease Outbreak: Workshop Summary.

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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 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 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.

FIGURE S-1. The Convergence Model.

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 (more...)

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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.

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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).

FIGURE S-2. Portrait of a superspreader: spread of SARS from the Metropole Hotel in Hong Kong as of March 28, 2003.

FIGURE S-2

Portrait of a superspreader: spread of SARS from the Metropole Hotel in Hong Kong as of March 28, 2003.

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 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 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).

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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 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.

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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.

Footnotes

3

Workshop presentation, Yi Guan, University of Hong Kong, September 30, 2003.

Copyright © 2004, National Academy of Sciences.
Bookshelf ID: NBK92478

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