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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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Global Alert and Response, Department of Communicable Disease Surveillance and Response

Severe acute respiratory syndrome (SARS) is the first severe and readily transmissible new disease to emerge in the 21st century. Initially recognized as a global threat in mid-March 2003, SARS was successfully contained in less than 4 months, largely because of an unprecedented level of international collaboration and cooperation. The international response to SARS was coordinated by the World Health Organization (WHO) with the assistance of the Global Outbreak Alert and Response Network (GOARN) and its constituent partners made up of 115 national health services, academic institutions, technical institutions, and individuals. The SARS outbreak has also shown how, in a closely interconnected and interdependent world, a new and poorly understood infectious disease can have an adverse affect not only on public health, but also on economic growth, trade, tourism, business and industrial performance, and political and social stability.

The chronology of the outbreak has been published on the WHO website (WHO, 2003a). The first recorded case occurred in mid-November in the city of Foshan, Guangdong Province, China. The Chinese Ministry of Health officially reported to WHO in mid-February that there had been 300 cases and 5 deaths in an outbreak of “acute respiratory syndrome” in which symptoms were clinically consistent with atypical pneumonia, and that the outbreak was coming under control. To complicate the issue, however, there were also cases of avian influenza, influenza A (H5N1), with three deaths among members of a Hong Kong family who had traveled to Fujian Province. WHO activated its global influenza laboratory network and called for heightened global surveillance on February 19, 2003; GOARN partners were alerted on February 20.

The SARS virus was carried out of southern China on February 21, when a 64-year-old medical doctor who had treated patients in Guangzhou and was himself suffering from respiratory symptoms checked into a room on the ninth floor of the Metropole Hotel in Hong Kong. Through mechanisms that are not yet fully understood, he transmitted the SARS virus to at least 16 other guests, all linked to the ninth floor. Those guests carried the disease to Toronto, Singapore, and Hanoi, or they entered hospitals in Hong Kong. The medical doctor fell severely ill the following day, was hospitalized immediately, and died on March 4. A global outbreak was thus seeded from a single person on a single day on a single floor of a Hong Kong hotel.

A businessman, infected in the Metropole Hotel, traveled to Hanoi, fell ill, and was hospitalized on February 26. He was attended by a WHO official, Dr. Carlo Urbani, following concerns raised by hospital staff. Alarmed at the unusual disease and concerned that it could be an avian influenza, Dr. Urbani contacted the WHO Western Pacific Regional Office (WPRO) on February 28.

On March 10, the Ministry of Health in China asked WHO to provide technical and laboratory support to clarify the cause of the Guangdong outbreak of atypical pneumonia. On March 12, WHO alerted the world to the appearance of a severe respiratory illness of undetermined cause that was rapidly spreading among hospital staff in Vietnam and Hong Kong. Three days later, on March 15, it became clear that the new disease was carried along major airline routes to reach new areas, and WHO issued a further global alert, giving the new disease its name: severe acute respiratory syndrome, or SARS.

The WHO Response

As the outbreak of SARS moved into the spotlight of intense global concern, an unprecedented multifaceted, multilateral, and multidisciplinary response was coordinated jointly by WHO Headquarters, Switzerland, and by WHO WPRO, the Philippines. The management of the global SARS response involved intense daily coordination in the areas of etiology and laboratory diagnosis, surveillance and epidemiology, clinical issues, animal sources, and field operations.

WHO Regional Offices, working through a worldwide network of Country Offices and intercountry networks, were the main channels for support to affected countries. While the six WHO Regional Offices were fully engaged in the global coordination of the SARS response, the Western Pacific Regional Office—covering the area where the vast majority of cases were occurring—bore the brunt of the response, deploying a total of 116 additional experts as short-term consultants during the outbreak. At WHO Headquarters, 75 people worked on the SARS outbreak response, with additional surge capacity provided by partners in the GOARN.

The GOARN is a global technical partnership, coordinated by WHO, to provide rapid multidisciplinary support for outbreak response to affected populations (WHO, 2000; 2001). The GOARN provided critical operational capacity for the initial response to SARS. Responding to requests for assistance from several countries, WHO and its GOARN partners mobilized field teams to support outbreak response in China, Hong Kong, Singapore, Taiwan, and Vietnam. Throughout the outbreak, WHO continued to work with GOARN partners to ensure ongoing support to health authorities, and GOARN teams continued in the field until the chains of transmission were conclusively broken.

Through GOARN, WHO coordinated development of a number of networks that proved pivotal in developing tools and standards for containment of the epidemic. The networks met regularly by teleconference, usually on a daily basis, to share information and data in real time. They were also assisted by dedicated, secure websites on which network participants were able to share preliminary information. The networks brought frontline workers and international experts together, and demonstrated the international collaboration and cooperation that was characteristic of the response to the SARS outbreak. A virtual network of clinicians was set up to exchange experiences, thoughts, and findings about SARS in an attempt to better understand and treat the disease effectively. The clinical network linked infection control issues closely with every aspect of case management, from clinical diagnosis and investigation to therapy. The discussions also allowed the rapid evaluation of the infection control risks of a number of interventions and helped to indicate potential alternative approaches.

A virtual network of epidemiologists brought together public health institutions, ministries of health, and WHO Country Offices to analyze the spread of SARS and to define appropriate public health measures. Activities of the epidemiology network have included the preparation of a consensus document on the epidemiology of SARS (WHO, 2003b). The laboratory network was established to assist with identifying the etiologic agent of SARS and to develop specific and robust laboratory diagnostic tests for the agent responsible. The network comprised members of the international influenza laboratory network in those countries in which cases of SARS had been reported. Thus a total of 11 expert laboratories in nine countries were included in the network. The success of the laboratory network was quickly demonstrated by the discovery and characterization of the etiological agent, the SARS coronavirus (SCoV), and the rapid development of the first generation of diagnostic tests.

WHO Country Offices: A Critical In-Country Presence

WHO Country Offices work as direct partners with Member States on all issues related to health, including those related to health and poverty, health and macroeconomic reforms, and the Millennium Development Goals. SARS dramatically illustrated the effects of a new disease on the broader health and development agenda.

Traditionally, the Ministry of Health is the primary working partner at the national level; however, in many countries WHO is encouraging a more inclusive definition of the nature of the health sector, leading to greater collaboration with other government institutions, United Nations agencies, nongovernmental organizations (NGOs), and the international donor community—this was particularly important in the SARS outbreak response.

During the SARS outbreak, WHO was widely recognized as a key organization to assist health authorities with national policy formulation and multisectoral coordination of preparedness activities and the SARS outbreak response. WHO provided objective and neutral policy and technical advice to strengthen the capacity of national health administrations to better manage preparedness activities and the SARS outbreak response and to build local capacity. WHO Country Offices—particularly in China and Vietnam—provided extensive technical input on policy development, guidelines and strategies, dissemination of information on key issues, and technical advice for preparedness and response activities. The WHO Country Offices in Beijing and Hanoi, supported considerably by experts from partners in GOARN and WPRO, worked with national authorities to address rapidly developing needs: strengthening disease surveillance and reporting systems; improving the classification and reporting of cases; and advising on field epidemiology, contact tracing, infection control in health care settings, rumor management, and risk communications.

Ultimately, controlling the course of SARS in China and elsewhere was the result of concerted multisectoral preparedness and outbreak response activities by national authorities. WHO’s activities and advice played an important role in catalyzing and coordinating this reponse. These activities are increasingly the routine work of a WHO Country Office anywhere in the world; however, the scale of the SARS outbreak and the attendant political and media interest ensured that the scale of operations was enormous.

In addition to providing direct support through WHO to affected areas, many GOARN partners were also involved in other SARS activities, including providing bilateral assistance to affected areas and supporting other countries in the Western Pacific and Southeast Asia regions. The International Federation of Red Cross and Red Crescent Societies helped to ensure that marginalized sections of society were reached by social mobilization activities. International NGOs and United Nations organizations were also involved in addressing humanitarian aspects of the response and preparedness activities. National surveillance and response institutions provided experts for field teams and, participating in the virtual networks, were also working at their own national levels to enhance preparedness and reporting on SARS cases to WHO. Regional disease surveillance networks provided information on measures and activities to be undertaken to prevent and control outbreaks of SARS.

The initial call for global surveillance was followed by a more detailed description of the surveillance system, which had as its objectives describing the epidemiology of SARS and monitoring the magnitude and spread of the disease in order to provide advice on prevention and control. This description, including revised case definitions and reporting requirements to WHO, was distributed with tools for its implementation through the WHO network to national public health authorities. It was also published on April 4, 2003, in the Weekly Epidemiological Record (Anonymous, 2003). With some minor changes, this global surveillance system remained in place until July 11, 2003, a week after the last chain of human transmission was broken.

Global SARS surveillance was primarily based on the reporting mechanism established through the Daily Country Summary of Cases of SARS. This form requested national public health authorities to report to WHO Geneva (with a copy to the WHO country and regional office) the number of new cases and deaths since the previous report, the cumulative number of probable cases and their geographic distribution, and the areas where local chains of transmission had occurred. Case numbers and information on areas with local transmission were updated daily on the WHO website in accordance with the information received by the national public health authorities. Local transmission was defined as one or more reported probable case(s) of SARS having most likely acquired the infection locally, regardless of the setting in which this may have occurred. An area was removed from the list 20 days after the last reported locally acquired probable case died or was appropriately isolated.

By July 11, 2003, 29 countries had reported a total of 8,437 probable cases, including 813 deaths (crude case fatality ratio 8.6 percent) from November 1, 2002. Ninety-two percent (n = 7,754) of the reports were received from China (including Hong Kong, Macao, and Taiwan). In the final compilation of reports received from public health authorities, there were 18 areas in 6 countries that experienced local transmission of SARS, with the first reported chain transmission starting on November 16, 2002, in Guangdong Province, China (WHO, 2003c).

The Origin of the Etiological Agent

As the SARS outbreak spread, and before the etiological agent was identified, questions were being raised as to where this new infection had originated. Early discussions between members of the first WHO Mission in China and colleagues from the Chinese Centers for Disease Control (CDC and Guangdong CDC implicated food preparers possibly connected with preparation of animals for food as being a particular risk group. As a result, on April 10 WHO formed an internal working group to address the potential that SARS could be a zoonotic disease. With the collaboration of the Food and Agriculture Organization (FAO) and the Office of International des Epizooties (OIE), an international working group on the animal reservoir of SARS was established. Animal susceptibility studies were carried out in various laboratories around the world. Subsequently, findings from Guan et al. (2003) from the University of Hong Kong indicated that masked palm civets and raccoon dogs sampled in a Shenzen market carried a virus very similar to SCoV.

In mid-July, WHO received permission to organize a mission to China to review animal studies conducted by Chinese scientists and recommend further research on the role of animals in the transmission of SCoV. The mission was carried out as a joint endeavor among the government of China, FAO, and WHO from August 10 to 22, 2003. A comprehensive report of the mission and recommendations were provided to the government of China for review. Important collaborations were established between members of the mission and Chinese scientists. Collaborative projects are ongoing and focus on developing a screening test for animals, animal susceptibility studies, and further testing of animals from markets. As part of enhanced SARS surveillance in China, wild animal handlers are considered a high-risk group. Protocols have been developed to prompt an appropriate epidemiological investigation should this group begin presenting at hospitals with symptoms of SARS.

Preparations for the Future


Will SARS return? This is difficult to answer without recourse to a crystal ball. If SARS is to return, it has to reemerge from one of three sources: (1) from undetected transmission cycles in areas with little or no health care facilities; (2) from an animal source; or (3) from a laboratory accident. With respect to the first possible source, it is difficult to believe that there have been continued, undetected transmission cycles. However, as SCoV is believed to have spread into the human population from a wild animal source, this has to remain a possibility, but whether it will occur this year or sometime in the future remains unknown. Preliminary results would indicate that SCoV, or a related virus, occurs in a number of wildlife species. However, the ability of the virus to cross the species barrier to cause disease in humans, and then to become adapted to transmit between humans, may be a relatively rare event. Of greater immediate concern is the threat posed by stocks of SCoV and clinical specimens potentially containing SCoV, which are kept in many laboratories globally, as well as the paucity of safer biosafety level 3 (BSL3) facilities in many parts of south and eastern Asia.

Surveillance and Laboratory Safety

WHO has been very active in preparing for the possible return of SARS. Of particular importance has been the preparation of an epidemiological and surveillance document, Alert, Verification and Public Health Management of SARS in the Post-Outbreak Period, which was posted on the WHO website on August 14 (WHO, 2003d); a workshop concerned with laboratory preparedness and planning to ensure rapid, sensitive, and specific early diagnosis of SCoV infections, and aspects of biosafety in the laboratory (WHO, 2003e); clinical trial preparedness; a meeting to determine SARS research priorities; training courses on SARS diagnosis and epidemiology; a meeting to discuss the development of SCoV vaccines (WHO, 2003f); and a series of capacity-building developments and assistance to countries within the Western Pacific Region as well as a continuing dialogue with and assistance to China.

Health authorities in nodal areas, where cases had occurred previously, and in areas of potential re-emergence (WHO, 2003d) have maintained heightened SARS surveillance established during the outbreak period, and continue doing so for the foreseeable future. WHO will also continue to identify and verify rumors about SARS through its usual, well-established mechanisms.

Laboratory preparedness has been a major concern as the northern hemisphere has approached the winter season with the prospects of increased influenza activity and other respiratory diseases, potentially leading to a significant increase in requests for diagnostic tests for SCoV. This could lead to an unsustainable surge in the work of clinical diagnostic laboratories, and the strong possibility of false-positive test results. Thus a number of recommendations were made at a SARS laboratory workshop held in Geneva in October 2003, all of which have been introduced or are in the process of being introduced (WHO, 2003e). The major outcomes have been the establishment of an International SARS Reference and Verification Laboratory Network to provide a diagnostic service to those countries and areas that do not have the necessary diagnostic facilities and to verify any laboratory-diagnosed case of SCoV infection reported in the inter-epidemic period; the development of a panel of positive control sera; and the formulation of strong recommendations about laboratory safety. Indeed, biosafety has become a major issue since the occurrence of the laboratory-acquired cases in Singapore and Taiwan (WHO, 2003f), and a major biosafety document is nearing completion with respect to the containment level and conditions under which work is undertaken with live SCoV. This document will support and extend the earlier document posted on the WHO website (WHO, 2003g). Finally, the workshop attendees considered the algorithms under which laboratory diagnosis should be undertaken, and these have been incorporated into the algorithms developed in the epidemiological document Alert, Verification and Public Health Management of SARS in the Post-Outbreak Period.

Diagnostics and Therapeutic Countermeasures

Insufficient evidence is available to evaluate the effectiveness of specific treatment measures, including antivirals, steroids, traditional Chinese medicine, and the appropriate type of mechanical ventilation. Therefore, generic protocols urgently need to be developed for SARS and other future disease outbreaks. The WHO SARS Clinical team hosted a workshop to plan future clinical trials for SARS with the following objectives: (1) to review treatment experiences in different countries during the last outbreak; (2) to share existing plans for future clinical trials and identify candidate therapies; (3) to agree on basic trial design, including a hierarchy of outcome parameters and agreed standards of care; and (4) to assist in preparedness for clinical trials at relatively short notice.

A SARS Research Advisory Committee was established to determine the major gaps in our knowledge of the origin, ecology, epidemiology, clinical diagnosis and treatment, and social and economic impacts of SARS, and to discuss research needs required to fill these gaps for effective public health management of SARS, including preparedness and response to future outbreaks. The committee was asked to prioritize the research issues with the aim that the prioritized list of issues could be widely circulated to international and national funding bodies as a consensus blueprint of international research objectives aimed at achieving a better understanding of the virus, its origins, and pathogenesis, so that public health management could be improved if SCoV returns. A report on the meeting is available on the WHO website (WHO, 2003h), and the full recommendations will be placed on the website in early 2004.

Training courses on laboratory diagnosis of SCoV were held in the fall in collaboration with WHO Regional Offices in Europe and Africa, and a further “train-the-trainer” course is being planned in association with the WHO Regional Office for the Americas (AMRO/PAHO) in 2004.

WHO has also held a meeting to discuss possible SCoV vaccines, and a number of recommendations were made to facilitate and accelerate SARS vaccine development and evaluation (WHO, 2003i).

In the Western Pacific Region, a number of activities have been started that are aimed at improving preparedness for the possible reemergence of SCoV, including updating existing guidelines for surveillance and response activities in the interoutbreak period, updating an assessment protocol for national preparedness, and developing a WPRO SARS risk assessment and preparedness frame-work (WHO Western Pacific Regional Office, 2003). Other priorities have been to strengthen infection control and establish a regional laboratory network. The objectives of the latter are to ensure proper laboratory diagnosis by providing coordination, technical support, and communication among country and regional reference laboratories.

Concluding Comments

WHO’s vision for global health security is a world on alert and ready to respond rapidly—both locally and globally—to epidemic-prone and emerging disease threats, whether they are natural or intentional in origin, minimizing their impact on the health and economy of the world’s populations.

Defense against the threat posed by epidemics such as SARS requires a collaborative, multifaceted response. National and international public health systems represent a major pillar of action for rapid and effective containment.

Through unprecedented collaboration the world community has demonstrated that it is possible to contain a serious infectious threat to the world population. Pivotal to addressing future threats is the need for a global coordinating mechanism that allows the worldwide community to be alerted and to respond to health events of international concern as rapidly, appropriately, and effectively as possible. The World Health Assembly recognized the role played by WHO, its staff, and GOARN partners during the 56th Assembly in passing a resolution, WHA56.29, in which it strongly supported the GOARN partnership and WHO’s global role in surveillance and response to infectious disease threats.

Harnessing the undoubted global capacities for detection, characterization, and containment of epidemic threats will require sustained strategic investment in initiatives like GOARN. However, at the end of the day these threats can only truly be faced with the courage and personal sacrifice as made by the thousands of individuals who came together to put a genie back in the bottle.


Strategy for Development and Monitoring Zoonoses, Foodborne Diseases and Kinetoplastidae, Department of Communicable Diseases Control, Prevention and Eradication, World Health Organization, Geneva, Switzerland.

Copyright © 2004, National Academy of Sciences.
Bookshelf ID: NBK92476


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