Severe acute respiratory syndrome (SARS) is a new infectious disease which was first recognized in late February 2003, when cases of an atypical pneumonia of unknown cause began appearing among staff at a hospital in Hanoi. Within two weeks, similar outbreaks occurred in various hospitals in Hong Kong, Singapore and Toronto.

On March 15, the World Health Organization (WHO) issued emergency travel recommendations to alert health authorities, physicians and the traveling public to what was perceived to be a worldwide threat to health. The travel recommendations marked a turning point in the early course of the SARS outbreak. Areas with cases detected before the recommendations were issued, namely Vietnam, Hong Kong, Singapore and Toronto, experienced the largest and most severe outbreaks, all characterized by chains of secondary transmission outside the healthcare setting. After the recommendations had been issued, all countries with imported cases, with the exception of provinces in China, were able, through prompt detection of cases and isolation of patients, either to prevent further transmission or to keep the number of additional cases very low (WHO. SARS: Status of the Outbreak).

After the disease had moved out of southern China, Hanoi, Hong Kong, Singapore, and Toronto became the initial "hot zones" of SARS, characterized by rapid increases in the number of cases, especially in healthcare workers and their close contacts. In these areas, SARS first took root in hospital settings, where staff, unaware that a new disease had surfaced, exposed themselves to the infectious agent without barrier protection. All of these initial outbreaks were subsequently characterized by chains of secondary transmission outside the healthcare environment (WHO. SARS: Status of the Outbreak).

Now, at the beginning of July, SARS appears to be under control. It might not be all over, though. Toronto, after having had no new cases for more than 20 days, experienced a second outbreak with cases linked to at least four hospitals, originating probably from a 96 year old man who had a pneumonia that was misinterpreted as a post-operative complication.

It is probably the "unsuspected SARS patients" that will be a major medical challenge if SARS cannot be eradicated. In Singapore, early in the epidemic (MMWR 52: 405-11), and later in Taiwan (MMWR 52: 461-6), the epidemic was driven partly by cases that either had atypical clinical presentations masking their infections, or were otherwise not rapidly identified because of lack of an initial history of direct contact with a known SARS case - despite efforts to implement extensive control measures. These patients became hidden reservoirs, and the subsequent transmission of the SARS virus resulted in substantial morbidity and mortality and the closure of several large healthcare facilities. Health authorities in Singapore subsequently defined an extended case definition that picked up virtually every person with symptoms that might possibly indicate SARS for investigation and monitoring, regardless of whether the person has been in contact with a SARS patient (see Chapter 5: Prevention).

The number of worldwide cases exceeded 4000 on 23 April and then rapidly soared to 5000 on 28 April, 6000 on 2 May, and 7000 on 8 May, when cases were reported from 30 countries. During the peak of the global outbreak, near the start of May, more than 200 new cases were being reported each day.

As of July 3, 2003, severe acute respiratory syndrome (SARS) had been diagnosed in more than 8,000 patients. The first SARS epidemic can be summarized as follows (Oxford):

1. The epidemiological observation that SARS was first detected in the Guangdong province in November 2002 and took three months to spread even to the immediately neighboring Hong Kong, despite easy exchange of family members between the two areas, does suggest, fortunately, a virus with a low infectiousness.
2. Outbreaks to date have been restricted to families, often living in high-density accommodation, and to hotels and hospitals. This limited spread is the hallmark of a virus with low communicability.
3. A truly global respiratory virus like influenza rather quickly emerged to infect millions of persons worldwide. Given the remarkable extent of air travel today, the SARS virus is not spreading rapidly, at least to date.

Two major epidemiological studies have been published on the possible consequences of introduction of the SARS virus into a susceptible population (Lipsitch, Riley). Both calculate that the "basic case reproduction number" - the fundamental epidemiological quantity that determines the potential for disease spread - is of the order of 2 to 4 for the Hong Kong epidemic. They draw the conclusion that the SARS coronavirus, if uncontrolled, would infect the majority of people wherever it was introduced, but that it is not so contagious as to be uncontrollable with good, basic public health measures: improved control measures in hospitals, quarantine of contacts of cases, and voluntary reduction in contacts in the population (Dye).

Riley et al. estimate that in Hong Kong, 2.7 secondary infections were generated on average per case at the start of the epidemic, with a substantial contribution from hospital transmission. Transmission rates fell during the epidemic, primarily due to

• reductions in population contact rates
• improved hospital infection control
• more rapid hospital attendance by symptomatic individuals.

In November 2002, cases of a highly contagious and severe atypical pneumonia were noted in the Guangdong Province of southern China. The condition appeared to be particularly prevalent among healthcare workers and members of their household. Many cases were rapidly fatal. During the first week of February there was growing concern among the public about a mysterious respiratory illness, which apparently had a very high mortality and which caused death within hours (Rosling).

Local health officials reported 305 cases of the unknown disease to the WHO (WER 7/2003), as well as 5 resulting deaths.

SARS was carried out of the Guangdong Province on February 21, 2003, when an infected medical doctor spent a single night on the 9th floor of a Hong Kong hotel when he visited his family (Hotel M). He had become unwell a few days earlier and was now seriously ill. He was admitted to a hospital on February 22 and died ten days later (Tsang).

Before the end of February, guests and visitors to the hotel's ninth floor had seeded outbreaks of cases in the hospital systems of Hong Kong, Vietnam, and Singapore. Simultaneously, the disease began spreading around the world along international air travel routes as guests at the hotel flew home to Toronto and other cities around the world (WHO. SARS: Status of the Outbreak).

SARS, the first severe infectious disease to emerge in the twenty-first century, has taken advantage of opportunities for rapid international spread made possible by the unprecedented volume and speed of air travel. SARS has also shown how, in a closely interconnected and interdependent world, a new and poorly understood infectious disease can adversely affect economic growth, trade, tourism, business and industrial performance, and social stability as well as public health.

The Hong Kong index patient (the physician from Guangdong) infected 12 other persons who had been staying at the same hotel (MMWR 2003;52:241-248). Two of these individuals were subsequently responsible for outbreaks in two local hospitals.

The Hong Kong health authorities immediately implemented enhanced infection-control procedures in all hospitals in Hong Kong, including stringent barrier and respiratory protection for healthcare workers, daily environmental disinfection of affected wards, and cohorting of SARS patients.

Towards the end of March 2003, a further SARS outbreak occurred among residents of Amoy Gardens, Hong Kong, with a total of 320 SARS cases in less than three weeks. The probable index patient was a patient suffering from chronic renal failure; in addition to person-to-person spread and to the use of communal facilities such as lifts and staircases, the SARS virus may have been spread through the sewage systems of the buildings (for details, see Government of Hong Kong Special Administrative Region).

 Figure 1. Epidemic curve, Hong Kong; June 16 (from Yeoh).

After the initial phase of exponential growth, the rate of confirmed SARS cases fell to less than 20 per day by April 28. The Hong Kong epidemic seems to have been under control even earlier, by early April 2003, in the sense that each case had, already by then, failed to replace itself (Riley). The main reason for this would have been the reduction in the contact rate between infectious individuals and the rest of the population.

At the beginning of June, public hospitals attempted to resume normal service, grappling with a backlog of an estimated 16 000 postponed operations because of the suspension of 30% of the medical services during the SARS crisis (Parry).

By June 16, 1755 cases of SARS had been diagnosed in Hong Kong. 295 patients (16.8%) had died. 1386 patients (79.0%) had recovered. Around 30% of cases occurred in healthcare workers. Among these, nurses were the most exposed category, accounting for about 55% of all infected healthcare workers. 15% were doctors, 27% support staff. Eight medical workers had died by June 2.

The outbreak in Vietnam began on February 26, when a 48-year-old Chinese-American businessman was admitted to the French hospital in Hanoi with a 3-day history of high fever, dry cough, myalgia and a mild sore throat. He had previously been in Hong Kong, where he visited an acquaintance staying on the 9th floor of the hotel where the Guangdong physician was a guest.

By March 5, secondary probable SARS cases were identified among health care workers in Hanoi, and subsequently 63 people were infected.

On April 28, the WHO removed Vietnam from the list of affected areas, making it the first country to successfully contain its SARS outbreak. The absence of any new cases for a continuous 20-day period (the duration of two incubation periods) was an encouraging indicator that appropriate detection and protection measures, as recommended by the WHO, were able to contain outbreaks and prevent their further spread (WHO, WER 18/2003):

• prompt identification of persons with SARS, their movements and contacts;
• effective isolation of SARS patients in hospitals;
• appropriate protection of medical staff treating these patients;
• comprehensive identification and isolation of suspected SARS cases;
• exit screening of international travelers;
• timely and accurate reporting and sharing of information with other authorities and/or governments.

SARS was introduced to Toronto by a woman of Hong Kong descent who had traveled home to visit relatives from February 13 to February 23, 2003. Whilst visiting their son in Hong Kong, she and her husband stayed at Hotel M from February 18 until February 21, at the same time and on the same floor as the Guangdong physician from whom the international outbreak originated. The woman and her husband only stayed in the hotel at night, and spent the days visiting their son. They returned to their apartment in Toronto, which they shared with two other sons, a daughter-in-law, and a five-month-old grandson on February 23, 2003. Two days later, the woman developed fever, anorexia, myalgia, a sore throat, and a mild non-productive cough. She died nine days after the onset of the illness. On March 8 and 9, five out of the six adult family members presented with symptoms of SARS (Poutanen).

By mid-May, the Toronto epidemic was thought to be over after the initial outbreak had mostly come under control. However, an undiagnosed case at North York General Hospital led to a second outbreak among other patients, family members and healthcare workers.

The new outbreak spread from the SARS ward on the eighth floor of North York General Hospital, where a 96 year old man undergoing surgery for a fractured pelvis on 19 April is believed to have contracted the disease. The man developed pneumonia-like symptoms after his surgery but was not suspected of having SARS. He died on 1 May (Spurgeon).

A woman from the hospital's orthopedic ward, who was transferred to St John's Rehabilitation Hospital on 28 April, was later recognized as having a mild case of SARS, and five other SARS cases then appeared at St John's Hospital (Spurgeon).

The second Toronto outbreak (and the Taiwan outbreak, see below) demonstrate that spread among health care workers can occur despite knowledge about the epidemiology and transmission of SARS (see also Chapter 3: Transmission). SARS patients with chronic illnesses occurring concurrently with fever and/or pneumonia with a plausible diagnosis are extremely challenging to the public health and healthcare systems (MMWR 52: 405-11).

On July 2, the WHO removed Toronto from its list of areas with recent local transmission (WHO Update 93).

To date, 251 cases of SARS have been diagnosed in Canada, most of them in the Toronto area. 43 patients have died.

The index case of SARS in Singapore was a previously healthy 23-year-old woman of Chinese ethnicity who had been staying on the 9th floor of Hotel M during a vacation to Hong Kong from February 20-25, 2003 (Hsu). She developed fever and a headache on February 25 and a dry cough on February 28. She was admitted to a hospital in Singapore on March 1. At that time, SARS had not yet been recognized as a new disease easily spread in hospitals. As a result, hospital staff were unaware of the need to isolate patients and protect themselves. Over a period of several days, the index patient infected at least 20 other people. No further transmission from this patient was observed after strict infection control measures were implemented (Hsu).

The virus initially spread rapidly among hospital staff, patients, visitors, and their close family contacts. Later on, spread of infection between hospitals occurred when patients with underlying disease - which masked the symptoms of SARS - were transferred to other hospitals, placed in rooms with other patients, and managed without adequate protective equipment (WHO Update 70).

The outbreak in Singapore was amplified by several so-called "superspreaders" (see also chapter 3: Transmission). 144 of Singapore's 206 probable cases have been linked to contact with only 5 individuals (WHO Update 70; Figure 2).

Figure 2. Probable cases of severe acute respiratory syndrome, by reported source of infection - Singapore, February 25-April 30, 2003 (from MMWR 52: 405-11)

On April 20, after the identification of a cluster of illness among employees at a crowded wholesale market, the market was closed for 15 days and more than 400 persons were placed in home quarantine. The spread of infection was limited to only 15 other persons.

In Singapore, 76% of infections were acquired in a healthcare facility; the remainder either had household, multiple, or unknown exposures. Due to rigorous contact tracing and isolation procedures, 81% of probable SARS cases had no evidence of transmission to other persons with a clinically identifiable illness (MMWR 2003; 52: 405-11).

Of the 84 (42%) healthcare workers with probable SARS, 49 were nurses; 13, physicians; and 22, persons with other occupations (attendants, radiographers, housekeepers, a porter, and a cleaning supervisor); no SARS cases have been reported among laboratory workers or pathologists (MMWR 2003; 52: 405-11).

238 cases of SARS were diagnosed in Singapore; 33 patients died.

On May 31, Singapore was removed from the list of areas with recent local transmission (WHO Update 70).

Up until mid-April, the Chinese authorities underestimated the magnitude of the epidemic in Beijing, with only 37 cases having been reported by April 19. In the following two days, the Chinese authorities announced more than 400 (WHO Update 35) new SARS cases. Additional reports (WHO Update 36) indicated that SARS had spread to other provinces, including western Guangxi, northern Gansu, and Inner Mongolia.

On April 23, the WHO extended its SARS-related travel advice (WHO Update 37) to Beijing and the Shanxi Province of China, recommending that persons planning to travel to these destinations consider postponing all but essential travel. Four days later, the Chinese Authorities closed theaters, Internet cafes, discos and other recreational activities and suspended the approval of marriages in an effort to prevent gatherings where SARS could be spread.

To date, the epidemic in China seems to be under control. 5,327 cases of SARS have been diagnosed, 349 patients have died.

On June 24, Beijing was removed from the list of areas with recent local transmission (WHO Update 87).

The first two suspected SARS cases were diagnosed in a couple on March 14. The man had a history of travel in February to the Guangdong Province and to Hong Kong. On March 26, a Taiwanese resident of Hong Kong's Amoy Gardens flew to Taiwan and took a train to Taichung to celebrate the traditional festival, Qing Ming. The man's brother became Taiwan's first SARS fatality, and a fellow passenger on the train was also infected.

Suddenly, in the last 10 days of April, the number of cases began to increase steadily, which would have made Taiwan's epidemic the third-worst in the world after China and Hong Kong. The origin of the outbreak was a laundry worker aged 42 years with diabetes mellitus and peripheral vascular disease who was employed at hospital A. On April 12, 14, and 15, he had a fever and diarrhea and was evaluated in the emergency department. The patient remained on duty and interacted frequently with patients, staff, and visitors. The patient had sleeping quarters in the hospital's basement and spent off-duty time socializing in the emergency department. On April 16, because of worsening symptoms, the patient was admitted to the hospital with a diagnosis of infectious enteritis (MMWR 52;461-6). On April 18, the patient became short of breath. A chest radiograph showed bilateral infiltrates, and the patient was transferred to an isolation room in the intensive care unit with suspected SARS (MMWR 52;461-6).

Because the index patient had been symptomatic for 6 days before SARS was diagnosed, the number of potentially exposed persons was estimated at 10,000 patients and visitors and 930 staff. On April 24, hospital A was contained, and all patients, visitors, and staff were quarantined within the building (MMWR 52;461-6).

Healthcare worker clusters at eight additional hospitals in Taiwan have been linked to the initial outbreak at hospital A. Preliminary data suggest that many of these clusters occurred when pre-symptomatic patients or patients with SARS symptoms attributed to other causes were discharged or transferred to other healthcare facilities. SARS later extended to multiple cities and regions of Taiwan, including several university and private hospitals. Four of these hospitals, including a 2,300-bed facility in southern Taiwan, discontinued emergency and routine services. Sporadic community cases also were reported in Taipei and southern Taiwan (MMWR 52;461-6).

The April outbreak in Taiwan may serve as an example of the far-reaching consequences of one single unrecognized SARS case.

On July 5, Taiwan was removed from the list of areas with recent local transmission (WHO Update 96).

The number of probable SARS cases reported from other countries over the time period November 1, 2002 to July 31, 2003, is shown in the following table.

Notes:

The cumulative number of cases includes the number of deaths. Updated data are available at http://www.who.int/csr/sars/en/

As the number of new cases continues to dwindle, one of the most important questions for the future is whether SARS can be eliminated or eradicated from its new human host. Experience with many other infectious diseases, including smallpox and poliomyelitis, has demonstrated that complete eradication of an infectious disease is possible only when three precise requirements can be met (WHO Update 84):

1. An effective intervention capable of interrupting transmission - ideally, a vaccine - must be available.
2. Easy-to-use diagnostic tools are needed, with sufficient sensitivity and specificity to detect levels of infection that can lead to transmission of the disease.
3. Finally, infection of humans must be essential to the life-cycle of the causative agent - if the chain of human-to-human transmission is broken, the agent cannot survive. Existence of an animal reservoir greatly complicates eradication, but does not preclude it, provided that interventions exist to break the chain of transmission in the animal species as well.

To achieve eradication at the global level, the control intervention must be safe, simple, and affordable. Current control measures for SARS, including case detection and isolation, tracing and follow-up of contacts, and quarantine, are effective but extremely time-intensive, costly, and socially disruptive. Few, if any, countries can sustain such efforts over time (WHO Update 84).

During the first epidemic of SARS, most countries had to deal with a small number of imported cases. When these cases were promptly detected, isolated, and managed according to strict procedures of infection control, further spread to hospital staff and family members either did not occur at all or resulted in a very small number of secondary infections (Chan-Yeung).

In countries with significant transmission of the SARS virus, the local outbreaks of Spring 2003 have been controlled; however, second outbreaks, such as those in Taiwan and Toronto, teach that complacency must be avoided.

Many lessons have been learned:

• Only one individual is required for an outbreak. One single infected individual is sufficient to test the flexibility of modern healthcare systems to the limit;
• The SARS virus is sufficiently transmissible to cause a very large epidemic if unchecked, but not so contagious as to be uncontrollable with good, basic public health measures (Dye);
• The unsuspected SARS patients will be the greatest challenge in medicine if SARS cannot be eradicated

Many questions remain unsolved:

• Will SARS maintain itself, with new foci appearing here and there?
• Will SARS establish itself as an endemic illness, perhaps with seasonal patterns? (Holmes)
• Will SARS remain confined to the areas where it is currently located, or will it spread around the world?
• What would the virus do in the developing countries?
• Would the transmission patterns be different if the virus was introduced into populations with a high prevalence of immunocompromised patients, i.e., people living with HIV?

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