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SARS: Emergence, Detection, and Response

OVERVIEW

The story of the emergence, spread, and control of severe acute respiratory syndrome (SARS) is the latest, most vivid episode of a microbial threat in our highly connected world. The SARS epidemic of 2002–2003 not only demonstrated the ease with which a local outbreak can rapidly transform into a worldwide epidemic, but also how news of such a threat can travel faster than a microbe. Notably, the experience demonstrated how effectively the global public health community can collaborate to contain a novel microbial threat.

SARS emerged in November 2002 in the southern Chinese province of Guangdong and has been linked with the handling and preparing of exotic mammals for human consumption. The virus ultimately spread to 30 countries and administrative regions within 6 months. Key points in the chronology of the epidemic are included in the Summary and Assessment.

This chapter begins with a description of the World Health Organization’s (WHO) coordination of a massive and multinational public health response to SARS. While the authors emphasize that the actions of individual nations ultimately contained the epidemic, they describe the many ways that WHO supported governments through its Global Outbreak Alert and Response Network (GOARN) and its country offices. These efforts served to highlight the important brokering role that can be played by the WHO in catalyzing and galvanizing the capacity of its member states in response to global public health challenges. This is followed by a discussion of the contributions made by the U.S. Centers for Disease Control and Prevention (CDC) in responding to and helping contain the SARS outbreak in the U.S. and overseas. In both of these papers, the authors describe not just the actions taken by the WHO and the CDC during the recent



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Learning From Sars: Preparing for the Next Disease Outbreak - Workshop Summary 1 SARS: Emergence, Detection, and Response OVERVIEW The story of the emergence, spread, and control of severe acute respiratory syndrome (SARS) is the latest, most vivid episode of a microbial threat in our highly connected world. The SARS epidemic of 2002–2003 not only demonstrated the ease with which a local outbreak can rapidly transform into a worldwide epidemic, but also how news of such a threat can travel faster than a microbe. Notably, the experience demonstrated how effectively the global public health community can collaborate to contain a novel microbial threat. SARS emerged in November 2002 in the southern Chinese province of Guangdong and has been linked with the handling and preparing of exotic mammals for human consumption. The virus ultimately spread to 30 countries and administrative regions within 6 months. Key points in the chronology of the epidemic are included in the Summary and Assessment. This chapter begins with a description of the World Health Organization’s (WHO) coordination of a massive and multinational public health response to SARS. While the authors emphasize that the actions of individual nations ultimately contained the epidemic, they describe the many ways that WHO supported governments through its Global Outbreak Alert and Response Network (GOARN) and its country offices. These efforts served to highlight the important brokering role that can be played by the WHO in catalyzing and galvanizing the capacity of its member states in response to global public health challenges. This is followed by a discussion of the contributions made by the U.S. Centers for Disease Control and Prevention (CDC) in responding to and helping contain the SARS outbreak in the U.S. and overseas. In both of these papers, the authors describe not just the actions taken by the WHO and the CDC during the recent

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Learning From Sars: Preparing for the Next Disease Outbreak - Workshop Summary epidemic but also the lessons that were learned and the preparations being made to handle any future challenges that may arise from SARS or other emerging diseases. The chapter continues with a broad overview of what is known and hypothesized about the emergence of SCoV, the natural history of the epidemic, the evolution of the virus, and the clinical profile of SARS. The authors suggest studies to answer some of the many remaining questions about this new disease. Given the likelihood of an animal reservoir for the virus in China that could reinfect the human population, continued vigilance for SARS is warranted. This chapter explores the value of modern quarantine in curtailing the spread of infectious disease in general and SARS in particular. Risks for the reintroduction of SARS include the possibility of initial low-level transmission that eludes surveillance and a laboratory-acquired infection, as occurred in Singapore in September 2003 and in Taiwan in December 2003. During the epidemic, hospitals in Hong Kong, Singapore, Vietnam, and Canada struggled to contain SARS within their walls. For example, in the first phase of the Toronto epidemic, which began on February 23, unrecognized SARS patients infected scores of other patients, family members, and hospital workers. Even after increased infection control measures were undertaken, this scenario was replayed in several area hospitals, as well as others around the globe. A sobering analysis of mistakes made in the communication and practice of hospital and community hygiene during the epidemic concludes the chapter. THE WHO RESPONSE TO SARS AND PREPARATIONS FOR THE FUTURE J.S. Mackenzie, P. Drury, A. Ellis,1 T. Grein, K.C. Leitmeyer, S. Mardel, A. Merianos, B. Olowokure, C. Roth, R. Slattery, G. Thomson, D. Werker, and M. Ryan 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 1   Strategy for Development and Monitoring Zoonoses, Foodborne Diseases and Kinetoplastidae, Department of Communicable Diseases Control, Prevention and Eradication, World Health Organization, Geneva, Switzerland.

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Learning From Sars: Preparing for the Next Disease Outbreak - Workshop Summary 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.

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Learning From Sars: Preparing for the Next Disease Outbreak - Workshop Summary 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

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Learning From Sars: Preparing for the Next Disease Outbreak - Workshop Summary 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

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Learning From Sars: Preparing for the Next Disease Outbreak - Workshop Summary 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

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Learning From Sars: Preparing for the Next Disease Outbreak - Workshop Summary 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 Reemergence 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

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Learning From Sars: Preparing for the Next Disease Outbreak - Workshop Summary 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 interepidemic period; the development of a panel of positive control sera; and the formulation of strong recommendations about laboratory safety. Indeed, biosafety

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Learning From Sars: Preparing for the Next Disease Outbreak - Workshop Summary 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, in-

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Learning From Sars: Preparing for the Next Disease Outbreak - Workshop Summary cluding 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 framework (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. THE CENTERS FOR DISEASE CONTROL AND PREVENTION’S ROLE IN INTERNATIONAL COORDINATION AND COLLABORATION IN RESPONSE TO THE SARS OUTBREAK James W. LeDuc and Anne Pflieger National Center for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia The global outbreak of an acute respiratory illness that became known as severe acute respiratory syndrome (SARS) was the first major international out-

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Learning From Sars: Preparing for the Next Disease Outbreak - Workshop Summary break of the 21st century and clearly had a dramatic, worldwide effect far exceeding the morbidity and mortality that directly resulted from infection with the novel coronavirus that causes SARS. In addition to the infection and hospitalization of several thousand individuals and the nearly 900 deaths that occurred in the countries with SARS cases, the entire global economy was affected by SARS, leading to serious losses of revenue, collapse of regional tourist and travel industries, and significant decreases in the gross national product among the nations affected (Lee and McKibbin, 2003). Despite several introductions of the virus from returning infected travelers, the United States was spared from the worst of SARS, given that there was no significant secondary spread, no large hospital-based outbreaks as seen in several countries, and no fatalities. The fact that the United States had relatively few cases belies the enormous effort put forth by public health officials in responding to the outbreak. The Centers for Disease Control and Prevention (CDC) worked closely with state and local governments, the health care delivery industry, and other federal agencies to actively alert the traveling public about the risks of SARS, to prepare the health care delivery system to recognize and treat suspected SARS patients, and to assure the public that appropriate interventions to protect them from infection were being taken. These efforts were undertaken in close collaboration with international partners in the World Health Organization (WHO) and in the countries most affected by SARS. The collaborative international response can be considered in five parts: coordination of response, collaborations in science, communications at home and abroad, capacity building and response preparedness, and challenges and lessons learned. Coordination of Response More than 800 CDC staff members were organized into 13 domestic teams, with core members serving throughout most of the 7-month response period. Domestic teams each focused on one critical aspect of the response, including clinical care and infection control, epidemiology of the outbreak, diagnostics and laboratory studies, quarantine issues, information management, occupational health issues (included staff from the National Institute for Occupational Safety and Health), communications, environmental issues, and community outreach programs focused on the challenges of providing accurate information to special groups such as immigrants and the Asian community. In addition, two teams were organized to review and offer constructive criticism of the response as it unfolded and to plan for possible pandemic transmission of SARS, and two other teams engaged in international efforts to respond to the outbreak and conduct subsequent scientific studies. Each group worked closely with experts from throughout the CDC Centers and often included members from other federal agencies (e.g., Department of Defense, Department of State, and National Institutes of Health, Food and Drug Administration [FDA], and others from the Department

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Learning From Sars: Preparing for the Next Disease Outbreak - Workshop Summary FIGURE 1-5 Range of available responses to SARS at the national, state, and community levels. to restrict movement during an epidemic, community officials would consider factors such as: the number of suspected, probable, and confirmed cases; whether cases have well-defined exposure risks; how many potential new exposures each case has been in contact with; what type of transmission is predominant (e.g., airborne, droplet, fomite); how many generations of transmission have occurred; and the morbidity and case-fatality rate of the epidemic. Decision makers would also need to consider the baseline amount of movement in the community, the impact of curtailing movement on critical infrastructure, the resources available to support containment, and the public’s reaction to the epidemic. Planning for Community Containment In some circumstances, containment of SARS or other microbial threats at the community level could be accomplished without restricting movement, with the focus instead on educating the public through such means as press releases

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Learning From Sars: Preparing for the Next Disease Outbreak - Workshop Summary and travel alerts and advisories (as was done in the United States in 2003). In other situations, targeted restrictions, including quarantine of close contacts and restriction of some group gatherings, would be appropriate. A more restrictive option would include general voluntary movement restrictions, including measures such as fever screening at entrances of public places, “snow-day” or “shelter-in-place” quarantines, closing public places, canceling public gatherings, and restricting mass transit. Rarely, in the most extreme circumstances, compulsory movement restrictions, including the closing of airports and borders, would be warranted. Advance planning is necessary to enable officials to assess risk, make decisions, and implement necessary measures as effectively as possible in the event of a disease outbreak. Jurisdictions should establish an emergency operations center structure and a legal preparedness plan, and forge connections among essential partners such as law enforcement officials, first responders, health-care facilities, educators, the media, and the legal community. Provisions must be made to monitor and assess factors such as those above to determine response level for both implementing and scaling back interventions and movement restrictions. Educational message strategies should be developed to disseminate information to government decision makers, health-care providers and first responders, and the public; it will be especially important to address the possibility that some people may experience stigmatization as a result of containment. A draft of the CDC SARS Preparedness Plan entitled, “Public Health Guidance for Community-Level Preparedness and Response to Severe Acute Respiratory Syndrome (SARS) is posted at http://www.cdc.gov/ncidod/sars/updatedguidance.htm. Appendices D and E specifically address Community Containment and Border Strategies, respectively. A SARS preparedness checklist (available at http://www.astho.org) also provides guidance for public health officials in developing such plans. To plan for case and contact management, jurisdictions should secure necessary protocols for clinical evaluation and monitoring, contact tracing and monitoring, and reporting of disease. Standards, tools, and supplies must be established for home and nonhospital isolation facilities. A telecommunications plan should be developed to provide for case and contact monitoring and fever triage, as well as to provide information to decision makers, health-care workers, and the public. Provisions must be made to ensure that all isolated and quarantined individuals receive food, medicine, and mental health and other supporting services, including transportation to medical facilities. Jurisdictions should also identify and develop assessment procedures for appropriate nonhospital residential facilities. These sites could be used for quarantining contacts or persons for whom “home isolation” is indicated, but who do not have an appropriate “home” environment. To prepare for the implementation of community containment measures, jurisdictions must establish legal authorities and procedures to implement all levels

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Learning From Sars: Preparing for the Next Disease Outbreak - Workshop Summary FIGURE 1-6 Range of available responses to SARS at borders. of movement restrictions. Essential personnel for the implementation of quarantine and other movement restrictions will include law enforcement officials, first responders and other deployable government services workers, and key personnel from the transportation, business, and education sectors. Training programs and deployment drills should be developed for these partners, as well as for public health personnel. Preparing to Respond and Secure National Borders Similar criteria to those used to determine community-level containment policy must be considered when determining appropriate responses to SARS at national borders (see Figure 1-6). In addition to considering circumstances in their area, officials contemplating movement across national borders must also monitor events in adjacent areas and, given the frequency of global travel, throughout the world. A limited border response could resemble that mounted by the United States in 2003 (i.e., issuing travel advisories and alerts; meeting flights from SARS areas to triage arriving ill passengers; and monitoring contacts for symptoms of illness). More intensive arrival screening could include questionnaires on symptoms and exposure to SARS, temperature screening, or even requiring health certification or registration with the local health department. In some circumstances, predeparture screening also would be appropriate. A further step would be to quarantine arriving passengers from affected areas, and under the most extreme circumstances, restriction of inbound and outbound travel may be necessary.

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Learning From Sars: Preparing for the Next Disease Outbreak - Workshop Summary Conclusion Modern quarantine represents a wide range of scalable interventions to separate or restrict movement (e.g. detain, isolate, or conditionally release) of individuals or populations infected by or exposed to highly dangerous contagions. These strategies can be an important part of the public health toolbox for suppressing transmission and stopping epidemics such as SARS. However, the ethical implementation of modern quarantine can be resource and labor intensive. Quarantine is most effective when it is tailored to specific circumstances and used in conjunction with other containment measures; people affected by quarantine must be ensured appropriate support services. The effectiveness of quarantine is further improved by comprehensive preparedness planning. Effective communication and public trust are quintessential components; consequently, the public must receive clear messages about the role and importance of quarantine as a means of containing certain infectious disease in advance of, as well as during, the epidemic. If a future epidemic affects the United States as SARS did other countries in 2003, it may be necessary to recommend quarantine, among other containment measures, in this country. Thus, it is essential that planning for the effective implementation of quarantine and other containment measures be undertaken at every level of government, and well in advance of the need. Strategic and operative plans should be exercised at all levels to expose and rectify gaps and pitfalls in nonurgent settings to ensure our readiness in an emergency. Acknowledgments The authors thank Alison Mack, Katherine Oberholtzer, Alexandra Levitt, and Ava Navin for technical assistance in the preparation and review of the manuscript. IMPACTS OF SARS ON HEALTH CARE SYSTEMS AND STRATEGIES FOR COMBATING FUTURE OUTBREAKS OF EMERGING INFECTIOUS DISEASES Abu Saleh M. Abdullah,9 Brian Tomlinson,10 G. Neil Thomas,9 and Clive S. Cockram10 Severe acute respiratory syndrome (SARS), resulting from a novel coronavirus, originated in November 2002 in, Guangdong Province, China. By February 2003 it had spread to Hong Kong and subsequently to 32 countries or regions on most continents, infecting about 8,098 patients and resulting in 774 deaths 9   Department of Community Medicine, The University of Hong Kong. 10   Department of Medicine and Therapeutics, Chinese University of Hong Kong, Hong Kong.

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Learning From Sars: Preparing for the Next Disease Outbreak - Workshop Summary (WHO, 2003k). The overall case fatality ratio is approximately 15 percent (WHO, 2003b). The nonspecific disease presentation, coupled with a long incubation period and the initial absence of a reliable diagnostic test, limited the understanding of the magnitude of the outbreak. The outbreak has identified a number of deficiencies in hospital and community infection control systems in Hong Kong. The lessons learned should be applied on a worldwide basis to help prevent the spread of other new infections that may emerge (Abdullah et al., 2003). In this chapter we outline our experience with medical and public health issues that have arisen in dealing with the outbreak of SARS in Hong Kong and suggest appropriate strategies for combating future infections. The SARS Epidemic in Hong Kong The first case of SARS to be identified in Hong Kong was a physician, who had been treating patients in Guangzhou. He traveled to Hong Kong on February 21, 2003. He rapidly became ill and was hospitalized, and he died soon after. This doctor apparently was able to warn his medical attendants of the highly infectious nature of his illness based on his own experience. Precautions were taken to prevent the spread of infection, so there were few cases of transmission within the hospital from this case (Tsang et al., 2003). In contrast, the index case at the Prince of Wales Hospital who was the source of the first large hospital-based outbreak was not known to be highly infectious (Lee et al., 2003; Tomlinson and Cockram, 2003). This patient was admitted before the discovery of the SARS coronavirus and any international recognition of the disease. The clinical picture was that of “typical” community-acquired pneumonia with no suspicious circumstances. This patient was thus treated using standard protocols established for previous cases in Hong Kong—in an eight-bed cubicle of an open general medical ward. Heightened infection control precautions were not instituted. During the epidemic, cases who were admitted to hospitals who did not show symptoms suggestive of SARS may not have been treated with strict isolation precautions, and this resulted in larger hospital outbreaks in areas such as Hong Kong and Toronto (Simmerman et al., 2003). In Hong Kong, this first received attention when 11 health care workers from the same ward of a hospital went on sick leave simultaneously in early March 2003. At that point different hypotheses were tested and different control measures were instituted to combat the disease. However, the prolonged epidemic affected a total of 1,755 individuals over a period of 3 months in Hong Kong. The last case was confirmed on June 11, 2003. Learning from the Experience A few important lessons were learned over the course of the SARS outbreak. Cardiopulmonary resuscitation and endotracheal intubation were identified as

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Learning From Sars: Preparing for the Next Disease Outbreak - Workshop Summary procedures causing very high risk to medical personnel. During some resuscitation procedures and difficult intubations, cases were reported of health care workers becoming infected despite the use of what was believed to be appropriate protective equipment. The use of nebulizers received particular attention in relation to the index patient at the Prince of Wales Hospital in Hong Kong (Lee et al., 2003). Other procedures such as nasopharyngeal aspiration, bronchoscopy, airway suction, and noninvasive ventilation procedures such as Bi-level Positive Airway Procedure (BiPAP) were also suspected to increase the dissemination of infection. It soon became apparent that respiratory secretions were not the only source of transmission of infection. Feces and urine were recognized to be major hazards. Cleaning the patient and the bedding after fecal incontinence, often performed by health care workers less trained in infection control procedures, proved to be a high-risk duty. Another problem found with the hospital management of SARS patients was that even after implementation of usual infection precautions for staff with gloves, gowns, and face masks, new infections in health care workers continued to occur (Lee and Sung, 2003). These may have been partly related to lapses in following standard procedures and partly because of initial lack of awareness of the mode of spread of the virus. Although it was concluded at an early stage that the infection was spread by droplets, it was not immediately recognized that the virus was so tenacious that it could survive outside the body on surfaces for long periods of time. The estimates of the time that the virus could survive on various surfaces grew longer and longer—from hours to days over the period of the outbreak—as understanding of the virus increased. Another contributing factor to the spread of infection within hospitals in Hong Kong was probably the relative inexperience of most hospital staff with respiratory pathogens with such a degree of infectivity. In recent years the only common infective respiratory conditions encountered in Hong Kong hospitals have been tuberculosis and influenza, and these generally have been contained quite easily within hospitals without specialized isolation facilities. Lack of experience in dealing with such a novel agent as the SARS coronavirus must have contributed to the high rate of infection within hospitals. This must be addressed by appropriate training, with repeated reinforcement and checking of infection control techniques so that hospital staff are ready for the next emerging infection. It is also likely that over the years a degree of complacency has developed, and that procedures that should be considered routine, such as washing hands between examining different patients, are no longer strictly implemented. Furthermore, the use of face masks in Hong Kong hospitals was previously a rarity except in operating rooms and designated high-risk areas. Guidelines need to be developed that are based on the best available evidence. In hospital settings in Hong Kong, such guidelines were established at a relatively early stage of the outbreak (Ho, 2003), but in the general community, it was more difficult to provide clear guidelines apart from applying the principles

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Learning From Sars: Preparing for the Next Disease Outbreak - Workshop Summary of common hygiene. The use of face masks outside of the hospital environment was adopted by a large percentage of the population, but guidelines for the use of this and other preventive measures were often vague and inconsistent. In the community setting, contact tracing and quarantining of people who had been in close contact with cases who developed SARS was rapidly introduced and was of vital importance in curtailing the spread of the disease and bringing the epidemic to an end (Riley et al., 2003). Again much experience was gained during the course of the outbreak, particularly regarding communication between different sectors of the health services, and mechanisms have been introduced to improve such communications. The initial case of the Guangzhou doctor was reported to the Hong Kong Department of Health, but contact tracing was not initially conducted at the Metropole Hotel where he stayed because there were no other reports of atypical pneumonia related to that hotel and little was understood about the nature of the condition. In retrospect such contact tracing clearly should have been attempted, although it is unlikely that it could have prevented the spread of disease to other countries. The other people who were infected at the hotel would have left Hong Kong soon afterward, at a time when they were still asymptomatic. International travel provides a means to disseminate an infection like SARS throughout the world. Fortunately few cases seem to have actually acquired the infection during air travel. Although measures were instituted to stop people with fever from traveling by air, those who were incubating the disease and were still asymptomatic would not be identified, so perhaps stricter measures are needed to effectively reduce the risk of spread of such diseases to other countries. The ease and frequency of international travel demand effective channels be established for rapid international communication of information about infectious diseases. Rapid alerting to potential threats will help ensure that appropriate measures can be instituted and official public information can be disseminated to mitigate public alarm. Conclusion Based on our current understanding about its pathogenicity and transmissibility, SARS needs to be regarded as a serious disease. Health care workers and service providers should use SARS as an example to prepare themselves with potential measures to combat any future outbreak of infectious disease. The SARS outbreak provides a timely reminder of the importance of the reorganization of health care systems with an international focus to ensure adequate surveillance mechanisms, rapid response to epidemics, effective prevention and control strategies, and maintenance of optimal infrastructure nationally and internationally (Lee and Abdullah, 2003). In advance of future disease outbreaks, countries where no SARS cases have been reported should be prepared with clear national and provincial contingency plans and mechanisms for integrating such plans into an international response (Lee and Abdullah, 2003).

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