At the onset of the global outbreak, patients infected with SARS coronavirus (SARS-CoV) sought care at emergency departments for symptoms of what appeared to be common respiratory infections. During such encounters, minimal infection control measures were implemented since most known infections did not warrant them. However, in some circumstances, conditions were favorable for efficient transmission of SARS. Many exposed healthcare workers, patients, and visitors became infected and subsequently transmitted infection to others in their healthcare facilities. Nosocomial transmission was the primary accelerator of SARS infections, accounting for 72% of cases in Toronto (3) and 55% of probable cases in Taiwan (Table) (4).

Figure 1

Figure 1. Number of probable cases of severe acute respiratory syndrome, by location and date of illness onset—Toronto and Taiwan, February 23–June 15, 2003.

In Toronto, the outbreak unfolded in two phases, both attributable to nosocomial transmission (Figure 1). The first phase resulted from a case of unrecognized SARS in an infected contact of a recent traveler to Hong Kong (5). The second phase resulted from unknown transmission of SARS among hospitalized patients during a period when healthcare workers were being instructed to wear personal protective equipment, including gowns, gloves, and masks (6). In Taiwan, the outbreak had two phases (Figure 1). The first phase consisted of sporadic SARS cases in travelers without nosocomial transmission (7). In the second phase, transmission at one municipal hospital ignited a number of subsequent nosocomial outbreaks when SARS patients were transferred to other facilities (4).

A number of factors may make nosocomial transmission a common mode of infection. Unlike many other viral respiratory diseases in which the concentration of virus is greatest on disease onset, the concentration of SARS-CoV in secretions appears to peak approximately 10 days after symptom onset (8) when a patient’s symptoms are often worsening and may require medical attention. Thus, patients may be most capable of transmitting the virus at the point when they encounter healthcare workers. In addition, transmission appears to be primarily through exposure to respiratory droplets and direct contact with patients and their contaminated environment (5,9). Healthcare workers and others in contact with SARS patients may be more likely to become infected, especially if exposed during aerosol-generating procedures (i.e., intubation, nebulizing medications). Finally, even after recognition of SARS, lapses in infection control measures may be responsible for infection in healthcare workers.

Whether SARS will occur again, and if so, whether the epidemiology will be similar to the outbreak in the spring of 2003 are not known. However, given the severity of illness seen in SARS patients and their eventual need for medical attention, healthcare workers and others in healthcare facilities are likely to remain at high risk if SARS reemerges.

Over the course of the SARS outbreak, certain persons and settings were found to be more efficient at transmitting SARS-CoV infection than others. In Taiwan, after an initial period of apparent control of SARS by public health officials (7), exposures to an apparent “super-spreader” with SARS contributed to an explosion of infections at a municipal hospital in Taipei (4). An infected hospital laundry attendant continued working despite worsening symptoms of diarrhea and pneumonia. Between the onset of his illness and eventual recognition of SARS, exposures to the worker and to the hospital led to at least 137 probable cases, including 45 in healthcare workers. Similarly, a small number of persons also generated a large number of cases during the first phase of the Toronto outbreak when a cluster of healthcare workers were infected with SARS after the intubation of a severely ill SARS patient (10). Comparable transmission from one person to many was seen in Singapore as well (11).

In contrast, experiences with SARS in the United States and several other countries have not shown similar superspreading patients or events despite opportunities for transmission (12). The reasons for such variable communicability are uncertain but may be due to innate characteristics of infected patients (13), high virus concentrations in secretions during peak illness (8), or exposures to aerosol-generating procedures such as intubation or positive-pressure ventilation (10). Because these procedures are considered high risks for SARS transmission, the Centers for Disease Control and Prevention (CDC) has developed guidelines that emphasize use of PPE and, if needed, furlough for healthcare workers with unprotected exposure to these procedures (14).

On February 23, 2003, a 78-year-old Canadian woman returned from a visit to Hong Kong. While there, she had unknowingly been infected with SARS-CoV during her stay at a hotel in Kowloon (5). After returning to Toronto, the patient’s condition worsened, and she died at home. SARS developed in her son, and he was hospitalized with respiratory distress on March 7. Before his death on March 13, he infected two other patients and one healthcare worker, all of whom subsequently exposed others to the infection before SARS was eventually recognized. Infected visitors also contributed to transmission in the hospital. Ultimately, 128 cases were associated with this hospital outbreak, including 47 (37%) hospital staff and 36 (28%) patients and visitors (5). Many of these cases occurred early in the global outbreak and before SARS transmission was recognized in Canada. Once the disease was recognized, appropriate infection control practices were initiated so that by May 14, the World Health Organization advised that Toronto was no longer an “affected area” with the last locally acquired (recognized case having occurred on April 20, 2003.

After the first phase of SARS in Toronto, healthcare workers continued to use extensive personal protective equipment (e.g., routine contact precautions with an N95 or equivalent respirator). However, after a period with no apparent SARS transmission, public health officials relaxed the requirement for extensive PPE. Subsequently, a cluster of SARS cases occurred among healthcare workers, followed by the second phase of SARS transmission in Toronto (6). In retrospect, investigators determined that SARS-CoV transmission had continued undetected among patients. These unrecognized cases occurred later in the global outbreak and after recognition of SARS transmission in Canada.

The experiences from Taiwan and from both outbreak phases in Toronto underscore the difficulty in detecting SARS cases and the cascade of infections that can occur from even one unrecognized case among persons in the hospital. Symptoms of SARS are nonspecific and may represent infection due to a number of respiratory pathogens. Without rapid diagnostic tests, clinicians must rely for diagnosis on a patient’s history of travel, exposure to healthcare facilities, or contact with patients with suspicious cases of pneumonia. To prevent SARS transmission, all healthcare workers and visitors entering hospitals in Toronto and Taiwan were screened for symptoms or epidemiologic links to settings where transmission was known or suspected. Epidemiologic links are important discriminators for considering a diagnosis of SARS; however, before any global SARS activity and during periods of notable local transmission, these epidemiologic links may lose their discriminating ability. Ultimately, vigilant and intuitive clinicians may be the best means of recognizing cases of SARS.

Minimizing Transmission through Early Detection and Intervention

Hospital emergency departments were important sites for SARS transmission during the early part of the outbreak in Toronto (5). In Taiwan, transmission in the emergency department occurred through unrecognized case-patients and during a period when infection control measures were weakened due to the rapid influx of SARS patients seeking evaluation. A number of administrative, engineering, and other controls were eventually implemented to minimize transmission of SARS in emergency departments in both Toronto and Taiwan. One important activity was “triage screening.” For this, a questionnaire was administered to entrants to identify SARS symptoms and exposures. Screening was accompanied by a temperature check, mandatory hand hygiene by the patient, and often by providing a surgical mask before admission to the hospital. These precautions were taken when the patient was first encountered by hospital staff.

Figure 2

Figure 2. A, evaluation center for severe acute respiratory syndrome (SARS) in Toronto, demonstrating spatial separation of chairs in waiting area intended to reduce patient-to-patient transmission. B, evaluation center for SARS in Taiwan,...

At the peak of the outbreaks in Toronto and Taiwan, healthcare providers and public health officials were faced with the possibility that any person coming to an emergency department with a febrile respiratory illness might have SARS and might transmit infection to other patients. In response, officials either constructed or retrofitted existing facilities to create SARS evaluation centers (i.e., “Fever Clinics”) (13). These units were designed to safely assess large numbers of people while minimizing the risk for SARS transmission, and in fact in both Toronto and Taiwan, no transmission was reported in these facilities. Staff and patients were grouped into cohorts, and a space of >l m was allocated between patients to make direct contact and droplet transmission less likely. Dedicated entrances and exits and clearly marked patient pathways were provided to segregate patients under evaluation. Provisions were made to ensure adequate ventilation and air exhaust to reduce the risk for droplet or airborne transmission. In Taiwan, temporary structures with high efficiency filtration were built (Figure 2). In Toronto, both tents and existing facilities were used.

Many infection control activities in Toronto and Taiwan were resource intensive and difficult to maintain for an extended period. To prevent unnecessary use of staff and materials, some measures were implemented only when transmission in the surrounding community or within the hospital reached a particular level. For example, using surgical masks throughout a hospital to contain infection in a healthcare worker or other person with symptoms was only implemented when transmission in the community was ongoing or recent transmission had occurred in the facility. Other functions, such as limiting access, restricting transfers, and performing surveillance for new-onset illness among healthcare workers, were initiated at different times in hospitals on the basis of hospital transmission or community transmission.

Closing an emergency department or hospital ward also was linked to the level of transmission within a hospital. Closings were necessary to prevent additional cases in a hospital where the risk for transmission was high or the source of transmission was unknown. However, given the substantial negative effect on hospital finances and healthcare access in a community, the decision to close a hospital to new admissions was made only in consultation with public health authorities.

On July 5, 2003, the World Health Organization declared the world free of ongoing SARS transmission (16). However, the factors that led to the emergence of SARS are likely still in place, permitting the possibility that SARS will reemerge. If this happens, nosocomial transmission and cases among healthcare workers may also occur. Taking the experiences from Toronto and Taiwan and applying them to preparedness and prevention efforts likely will minimize SARS transmission in healthcare facilities.