Canada Communicable Disease Report
Caring for severe acute respiratory syndrome (SARS) patients in acutecare institutions in the greater Toronto area
LE Nicolle, MD (1), P Perkins, RN (2), D Gravel, BScN, MSc, CIC (2), S Paton, RN, MN (2), M Christian, MD (4), M Ofner, RN, MPH (2), B Henry, MD (3), A McGeer, MD (4), M Vearncombe, MD (5), A Simor, MD (5), C Barry, RN (5), B Mederski, MD (6)
- University of Manitoba, Winnipeg, Manitoba
- Centre for Communicable Diseases and Infection Control, Infectious Disease and Emergency Preparedness Branch, Public Health Agency of Canada, Ottawa, Ontario
- Toronto Public Health, Toronto, Ontario
- Mt. Sinai Hospital, Toronto, Ontario
- Sunnybrook Health Sciences Centre, Toronto, Ontario
- North York General Hospital, North York, Ontario
Greater Toronto Area (GTA) was the only site outside Asia to experience a large outbreak of severe acute respiratory syndrome – coronavirus (SARS-CoV) in the spring of 2003(1). The first GTA case had onset of clinical symptoms 23 February 2003. The initial global alert was announced by the World Health Organization (WHO) on 12 March 2003, but the outbreak was established in the GTA prior to this alert. The GTA outbreak was bi-phasic(2). It originated with the importation of the virus by a woman who had acquired an infection while visiting Hong Kong (3). The second phase followed recrudescence of cases in healthcare workers after de-intensifi cation of control measures as the first phase of the outbreak was considered controlled, but when unrecognized nosocomial transmission continued among patients in one facility(4). During the outbreak, the GTA and adjoining municipalities identified 358 cases, and the case-fatality ratio was 17 %( 5). Amongst the 225 cases in the GTA, 88 (39%) occurred in healthcare workers, 49 (22%) in patients, and 25 (11%) in hospital visitors(5). The onset of symptoms of the last GTA case identified was 12 June 2003.
This large outbreak of acute infectious illness with high mortality caused by a novel virus was unprecedented in Canada in recent times. By the time the outbreak was first identified, several healthcare facilities were already implicated in infection transmission(3,6), and many of the early cases occurred among healthcare workers. The outbreak response was directed and coordinated by the SARS Provincial Operations Centre (POC) of Emergency Measures Ontario. Directives jointly from the chair of this committee and the provincial medical offi cer of health (MOH) mandated the healthcare facility response in addressing the outbreak. GTA acute-care institutions were required to develop capacity, virtually overnight, to provide care for patients with clinical illness ranging from mild to severe. The physical requirements to accommodate these patients were not present in most facilities prior to the outbreak. In addition to providing patient care, extraordinary measures were implemented to prevent further transmission of infection to other hospital patients, employees, and visitors. Persons with prior unprotected exposure also had to be identified and quarantined. All of this occurred before the infectious agent had been identified and characterized, or the mode of transmission was fully understood. This retrospective review was undertaken to explore features related to the provision of care to SARS patients during this unique experience within acute care institutions in the GTA.
The GTA included a large number and variety of acutecare institutions, which provided medical services across a spectrum from small community hospitals to large, tertiary care academic health centres. At the time, healthcare services in the GTA were not regionalized, although some institutions provided services at more than one site. Each institution was governed by a separate board and was funded by a separate budget. There were 20 acute-care hospitals in the GTA designated to provide care for SARS cases during the initial phase of the outbreak, and were required to respond to the provincial directives. Not all hospitals subsequently cared for patients. With the second phase, the directives designated only four acute-care hospitals to admit new SARS patients. However, only two of these hospitals subsequently accepted patients for SARS care, and other hospitals provided care for most non-SARS patients. A convenience sample of 8 acute care GTA hospitals was included in this review (Table 1).
Table 1. Selected characteristics of the hospitals enrolled in this review
|Cared for SARS patients||+||+||+||+||+||+||+||+|
|Staff diagnosed with SARS||+||+||+||+||-||+||-||+|
|Sars care sites||+||+||+||+||-||+||+||+|
|– SARS unit|
|– Critical care||+||+||+||+||+||+||+||+|
|Airborne isolation rooms||-||+||+||+||+||+||+||+|
|Patients admitted to SARS
|* Small: <200 bed; medium 200 – 600 beds; large >600 beds † Variable numerators among hospitals – some report confi rmed and suspected SARS patients, others all patients who were cared for using SARS precautions. ‡ Day/month in 2003 § One site only|
Interviews requested by the GTA MOH were conducted from July 2003 through June 2004 as part of an investigation of the SARS experience. For seven of the hospitals, a spectrum of relevant employees were interviewed, including individuals from administration, infection control directors and practitioners, occupational health, human resources, housekeeping, engineering, unit managers, quality assurance and risk management, supply chain and support services, clinical educators, nutrition services and infectious disease physicians. For the remaining hospitals, all information was provided through the Director of Information Management.
Standard questions and a uniform electronic data collection were used. Specific questions addressed the provision of care, including characteristics of SARS units, Staffing, training, signage, supplies, use of personal protective equipment (PPE), housekeeping practices, visitor guidelines, organizational structure, and infection control capacity. A final open-ended question invited individuals interviewed to comment on personal concerns and positive or negative experiences during the outbreak period.
The analysis was primarily a descriptive summary of the hospital experience. This included variability in response across hospitals, unique practices relevant to the care of SARS patients, and the development and function of the SARS units. Information collected was often incomplete, refl ecting data not being provided or available and the collection of different information across the hospitals. Responses to the open-ended question describing personal observations were evaluated qualitatively to identify major themes and summarized within these themes.
Creation of units: The March directive specifi ed a requirement to create a SARS unit and the size of the unit: 30 beds for hospitals with > 500 beds, 20 beds for 400 to 500 beds, and 15 for fewer than 400 beds. Seven hospitals created SARS units, including two with units at two different sites. The initial units opened from 23 March 2003 to 3 April 2003, 3 to 18 days elapsing between receiving the directive and opening a functional unit. The size varied from 4 to 25 beds (Table 2). Two hospitals replaced the initial unit with a second unit developed to address defi ciencies in bed numbers or ventilation requirements in the prior unit. Four hospitals closed their SARS units after the first phase, when the outbreak was declared over. Three of these re-opened to accommodate patients for the second phase, but only two subsequently admitted patients.
Physical plan: Each hospital designated a space for the unit considering variables including size, safety, security, and engineering requirements. There was no consistency in the physical plan of units (Table 2). Most rooms on SARS units did not have anterooms, but did have separate bathrooms. A single patient in each room was usual, although one hospital had two patients in a room if these were members of the same family. Most units had a dedicated elevator and restricted entrances, usually a single entrance monitored by security. The location of the nursing station and staff lounges and whether they were within a negative pressure area, were variable (Table 2).
Ventilation characteristics: All units had ventilation provided as 100% fresh outside air, exhausted 100% to the outside (Table 2). To create negative pressure, three hospitals had a portable HEPA unit in each room, two had centrally-supplied air exhausted to the outside, and two used areas with existing negative pressure. At some hospitals, portable HEPA units were also used to create negative pressure in critical care areas and emergency rooms. Air exchanges varied from 9 to 18 per hour; the directives had required a minimum of six air exchanges per hour. The 24 April 2003 directives required twice weekly monitoring, but five of seven hospitals monitored daily, one twice daily and one weekly. Monitoring was achieved through pre-existing electronic monitors or smoke or tissue tests if these were not available.
Table 2. Physical characteristics of SARS units developed in seven acute-care hospitals
|1||2||3||4 (1)*||4 (2)*||6||7||7 (1)*(a)†||7 (1)*(b)†||7 (2)*||8 (a)+||8 (b)+|
|Portable HEPA||all rooms||-||10 rooms||-||-||+||+||all rooms||-||in ER|
|Forced central air||+||+||+||+||+||+||+||?||+||+||+|
|Existing negative pressure||10 rooms||1||0||4 rooms||one site||4||7|
|Air exchanges per hour||8||9||12||9||9||9||9||NS||9||9||9-12||16|
|- Method||smoke &
|mechanical; smoke tests|
|- Location||Central||Central||Central||Central||Central||Central||Central||Outside||Central||Centre front|
|- Negative pressure||no||yes||no||NP relative
|- Negative pressure||no||yes||no||no||no||yes|
|Abbreviations: NP, negative pressure; NS, not stated * Hospitals with SARS units at more than one site; designated by (1) and (2) † An initial unit (a) was subsequently replaced by a second unit (b)|
Personnel: Nurses, housekeeping, unit clerk and transporters were usually dedicated to the SARS unit. Other staff attended as needed and included infection control personnel, physiotherapists, occupational therapists, respiratory therapists, chaplaincy, mental health, educators, public health, social work, dietitians, and technologists. Students were not allowed to work on the units, although post-graduate infectious disease trainees provided care on one unit. There was variability in nurse to patient Staffing ratios and shifts (Table 3). A small cadre of physicians provided care to SARS patients at most sites, with availability 24 hours a day and seven days a week. Physician fatigue was a signifi cant issue. With the exception of patients admitted to the ICU, medical care was usually provided by infectious disease physicians, who were often dedicated to the unit. Other participating physicians included internists on three units, respirologists at two hospitals, orthopedic and plastic surgery attendings at a hospital with a cluster of cases on surgical wards, and a psychiatrist.
Stress management: Seven hospitals described interventions to address fatigue and stress for staff working with SARS patients. These included frequent breaks, provision of free food and refreshments, and a buddy system, access to mental health professionals and stress counseling, and using only staff who had volunteered for assignment to the unit. Four of the hospitals described additional perks such as provision of free tickets to museums, entertainment, food, and hotel rooms. Three hospitals provided extra time off for staff working on the unit, and one hospital reported that staff working with SARS patients received double pay. Provision of additional remuneration was subsequently prevented by the nursing union(7).
Staff Outcomes: Six hospitals reported a total of 73 staff members diagnosed with SARS (range 1 to 48); two facilities had no infected staff members identified. The majority of staff members were infected following nonprotected exposure to patients prior to the patient being identified as a risk for SARS. Some episodes with staff members becoming infected after institution of precautions have been previously reported(8-10). The number of staff members on home or work quarantine also varied greatly - from two to an estimated 4,000.
Equipment and Supplies
Patient rooms: All hospitals restricted equipment and supplies in the SARS patient room, as required by the POC directive. Equipment in the room included furniture (bed, table, chair, laundry hamper and garbage container) and direct patient care equipment as necessary (IV poles and pumps, blood pressure, stethoscope, oxymeter, thermometer, glucometer and oxygen). Some hospitals also allowed televisions, computers, and a telephone. Linen, supplies for laboratory specimens, and personal protective equipment were outside the room.
Eye protection: In the first phase, goggles were usually used for eye protection, with occasional use of safety glasses, face shields, and masks with attached face shields. The goggles were uniformly reprocessed by the staff member between patients, usually using accelerated hydrogen peroxide. In the second phase, following POC directives, disposable face shields became the consistent equipment for eye protection. One facility used face shields over the goggles.
N95 mask fit testing: None of the hospitals had fit testing programs in place prior to the outbreak. The seven hospitals that provided patient care during the second phase of the outbreak all introduced fit testing programs after the POC directive. Most hospitals started fit testing at the beginning of May 2003, with dates of 1, 5, 6, 25, and 29 May 2003 (two hospitals). Initial failure rates with fit testing reported by five hospitals, were 6% to 8%, “few”, “large initially”, 18% with first mask, to as high as 30%. The hospital with high initial failure rates addressed the problem by changes in testing procedure and increased selection of mask types. This high initial failure rate compromised the ability to continue providing care for SARS patients in some hospitals, and heightened staff concerns about personal safety.
Pre-existing infection control resources and expertise were variable (Table 3). Hospitals with limited infection control resources prior to the outbreak usually committed additional resources during the outbreak. Hospital 1 added an occupational health nurse and second infection control nurse for fever surveillance, and Hospital 6 added two clinical educators and one additional nurse, and by the end of the outbreak had a 50% ID physician and 2.6 new ICP’s. Hospital 7 hired an additional practitioner and added secretarial support. All but one hospital reported that all other infection control activities were suspended for the duration of the SARS outbreak. Members of the infection control team were fully occupied in addressing specifi c needs for SARS, including training, continuing education, and policy development and, in some cases, providing expertise to assist other hospitals.
Table 3. Staffing of SARS units and infection control resources at facilities at the beginning of the SARS outbreak
|Intensive care unit (ICU)||1:1||1:1||1.4:1||1:2||1:2||1:1||1:3||2:1|
|Nurse shift (hr.)||8||12||12||8 or 12||12||8 or 12||12||12|
number of working days
|Infection control personnel|
| – Infection Control
|– Years ICP experience
|– Other personnel|
|Surgical site infection (SSI)
surveillance pre SARS
|* CIC: certified in infection control
† 8 hour shifts
‡ 12 hour shifts
Qualitative Review of Personnel Experience
The major themes expressed by individuals at the end of the interviews in these comments were consistent across the hospitals (Table 4). These included concerns about resource limitation, restrictions in patient care, inconsistent directives, inadequate communication both within and outside the hospital, defi cits in emergency preparedness and interaction between acute-care institutions and regions, limitations in staff knowledge and training, and excessive staff stress. These comments are evidence of the frustration and intense stress experienced as the institutions and individuals responded to unprecedented demands in an environment of limitation in knowledge and equipment, shifting priorities, and rapidly changing interagency and interfacility relationships.
One observation apparent from this review is that the SARS response was not static, but dynamic. POC directives and the institutions’ response evolved continually throughout the SARS outbreak, with new and updated directives daily and occasionally multiple directives per day, requiring ongoing review and implementation at the facility level. As the outbreak progressed, policies and practices continually changed. The hospital response required continued modifi cations throughout the outbreak on virtually a daily basis, to respond to limitations in the institution’s capacity as well as outside directives and evolving knowledge.
Institutional characteristics and capabilities varied greatly prior to the outbreak. Uniform directives from a central authority required implementation within each facility, irrespective of pre-existing infrastructure or resources. At the onset of the SARS outbreak, there was no regional standardization of resources or equipment, procedures for patient care, or infection control resources or practice. Thus, centralized, uniform directives, mandating a consistent facility response to SARS, were overlaid on a collection of institutions with diverse administrations, physical capacity, policies, information systems, and resources. It is not surprising, then, that a consistent theme is the wide inter-hospital variability in response to directives, including specifi c practices, Staffing, design of SARS units or cleaning procedures.
Table 4. Observations from individuals interviewed describing personal perceptions of the SARS experience
|Restrictions in care||
Another general theme is limitation - in expertise, personnel, supplies, and outside assistance. Hospitals were required to implement POC directives as they were issued, but fi nancial resources and support for implementation were not provided. This is understandable, as the provincial government was overwhelmed by requirements for personnel and resources to address the epidemic. Hospitals were directed to “do what was needed”, with the understanding that reimbursement for expenditures attributable to the outbreak response would be reconciled after the crisis had resolved. Resources in the entire GTA were not suffi cient to respond within the required timeframe for some directives, such as universal mask fit-testing. There were insufficient quantities of many supplies, particularly face shields and masks. Most hospitals did not have plans allowing access to suffi cient quantities of necessary equipment on short notice or agreements in place with suppliers for surge capacity. A list of potential suppliers was not even available in some cases. These limitations required hospitals to interpret directives within the context of resource availability and contributed to variability in implementation and practice. This GTA experience with limitation has been analyzed with respect to priority setting during the outbreak(11).
The POC directives for the second phase of the outbreak designated a limited number of acute-care institutions – the four “SARS alliance hospitals” - as the admission and treatment centres for new SARS patients. However, restriction of SARS activity to a limited number of hospitals, with a goal of preserving non-SARS care at other hospitals, was not effective. Some designated hospitals did not admit SARS patients in the second phase of the outbreak, while non-alliance hospitals evaluated and cared for most patients. There was no authority in the region to compel the designated hospitals to accept patients. This again highlights the lack of a pre-existing co-operative, regionalized response plan for the provision of health care.
The POC directives themselves were consistently identified as problematic, including the process for development, dissemination, and specifi c content. Directives were uniformly described as being too frequent, inconsistent, and not scientifically based. This contributed to what one individual described as the impression of a “chaotic, uncontrolled, panic response”. The information fl ow was essentially unidirectional, down from the operations centre, with little opportunity for feedback or clarifi cation with respect to interpretation or effectiveness. Directives occasionally had clear errors identified, but there was no process for feedback to address such errors. Some facilities, in frustration, created their own practices based on national and international guidelines. There was, in fact, considerable variation in practice from one hospital to another, despite the uniform directives.
An important question to address is what specifi c interventions were actually necessary to limit transmission of SARS in the healthcare setting. As evidence suggests, the majority of SARS transmission in healthcare institutions is droplet spread (12) ; negative pressure ventilation to control transmission may not be necessary for routine patient care. Ventilation requirements are still likely appropriate for aerosolizing procedures. Analyses of the effectiveness of personal protective equipment (PPE) for healthcare workers have been reported worldwide (13-19). These reports suggest that masks, gowning and gloving, are benefi cial. The evidence does not suggest a clear benefit for N95 masks beyond surgical masks(13,16). The directive between outbreak phases which required intensifi cation of personal protective precautions was repeatedly identified as a concern. These intensifi ed recommendations for PPE were not based on characteristics of disease transmission or practical experience. Double gloving, gowning on the unit and again for the patient room, scrub suits, or any additional level of PPE beyond masks, gowns, gloves and eye protection were excessive relative to practices in other global SARS outbreaks, which were also controlled. Importantly, the intensifi cation of PPE increased the complexity of donning and removing equipment, so the potential for contamination may have been increased.
The focus of PPE use was the protection of healthcare workers. Many healthcare workers failed to appreciate the dual goal of patient protection, and lapses in practice, such as going from one patient to another without changing PPE, were observed. Part of this likely refl ected the previouslydiscussed complexity of removing and donning PPE. The failure to consider patient as well as worker safety likely resulted in the sustained chain of patient-to-patient transmission at one hospital that precipitated the second phase of the outbreak(4). It also may explain the observation in the GTA(20), and elsewhere(21,22) that MRSA transmission paradoxically increased, despite uniform barrier precautions for all patient care.
Another mandated practice consistently identified as problematic was the directive for fit testing in the second phase of the epidemic. The goals of fit testing and the necessity for it for healthcare workers in the prevention of infectious diseases remain controversial(23) . There is no body of evidence to support the effi cacy of N95 masks or fit-testing in preventing healthcare-acquired infections, but occupational health legislation requires fit-testing in settings where an N95 mask is required. There was no active fit-testing program in any GTA acute-care institution prior to the May directive. This was consistent with Canadian guidelines which specify an “N95 mask or equivalent” so fit-testing was not necessarily required. The evaluation of the cluster of cases following an intubation episode at one hospital focused on lack of fittesting, to the exclusion of multiple other likely contributing factors(8). There were insufficient resources in individual hospitals or the region to provide, virtually overnight, an appropriate fit- testing program. The initial high failure rates caused by defi ciencies in testing procedures and a limited variety of masks aggravated staff concerns about safety. This issue remains a problem in the aftermath of SARS and continues to affect some working relationships.
With a large number of patients requiring unique management, the creation of designated units provides effi ciencies in patient care, Staffing, and training, in addition to the separation of infectious patients. At least one hospital included in this review provided care to SARS patients without creating a unit, continuing to use pre-existing negative pressure rooms throughout the hospital. There did not appear to be unique outcomes for patients or staff in this hospital, although the number of SARS patients cared for was small. As reported in Taiwan(24) the availability of dedicated units did not completely prevent transmission of infection(8,9). The GTA experience does, however, show the capacity of the system and individual institutions to rapidly adapt patientcare areas for specialized engineering requirements. Adequate care for SARS patients and protection of staff members appear to have been achieved irrespective of physical characteristics of the units, such as access, or location of nursing unit or lounge.
The 2003 SARS outbreak was an extraordinary experience globally as well as locally for healthcare institutions and individuals participating in the GTA outbreak. Observations from this experience, which are described in this review, are limited by incomplete information and variable reporting among facilities. While the experience of only eight hospitals is described, these hospitals are likely representative of the experience throughout the GTA as these hospitals admitted the majority of the SARS patients. The experience of each hospital was unique, but the consistent stresses and problems in addressing the outbreak were remarkably consistent across this diverse group. The comments of individuals are evidence for the stress experienced and consistency in issues of concern for participating individuals. Other reports have addressed some aspects of the intensive stress experienced(12,25,26). In an environment characterized by many unknowns, with high personal and institutional stress, facilities and their staff were, however, key contributors to the ultimate control of SARS in the GTA.
The experience in the GTA and other urban areas with large SARS outbreaks described is exceptional. Infection control personnel should all be hopeful they will not fi nd themselves in a similar situation. Beyond this, reviewing the experience allows an exploration of what aspects of the experience could be improved through improved understanding and preparedness(27,28) . Among these is an appreciation that healthcare delivery is a fully integrated system, and no facilities can function in isolation. Second, the commitment to infection control practices, based on knowledge, must be a focus of any outbreak response to promote practices which are rational and feasible. Standardized, continuing, training of healthcare workers in infection control must remain a priority.
The authors acknowledge the contribution of the following individuals for whom the project would not be possible: Katie Cassidy, John Koch, Stephanie Leduc, Louise Marasco, Melinda Piecki, and the staff at each participating hospital.
- WHO Consensus document on the epidemiology of severe acute respiratory syndrome (SARS). Available from: http://www.who.int/csr/sars/en/WHOconsensus.pdf
- Low DE, McGeer A. SARS – One year later. New Engl J Med 2003;349:2381-82
- Varia M, Wilson S, Sarwal S et al. for the Hospital Outbreak Investigation Team. Investigation of a nosocomial outbreak of severe acute respiratory syndrome in Toronto. Can Med Assoc J 2003;169(4):285-92.
- Wong T, Wallington T, McDonald LC et al. Late recognition of SARS in nosocomial outbreak, Toronto. Emerg Infect Dis 2005;11(2):322-25.
- Svoboda T, Henry B, Shulman L et al. Public health measures to control the spread of the severe acute respiratory syndrome during the outbreak in Toronto. N Engl J Med 2004;350:2352-61.
- Poutanen SM, Low DE, Henry B et al. Identifi cation of severe acute respiratory syndrome in Canada. N Engl J Med 2003;348:1995-2005.
- Lim S, Closson T, Howard G et al. Collateral damage: the unforeseen effects of emergency outbreak policies. Lancet Infect Dis 2004;4(11):697-703.
- Ofner M, Lem M, Sarwa S et al. SARS Investigative Team. Cluster of severe acute respiratory syndrome cases among protected healthcare workers – Toronto, April 2003. CCDR 2003;29(11):93-97.
- Christian MD, Loutfy M, McDonald LC et al. Possible SARS coronavirus transmission during cardiopulmonary resuscitation. Emerg Infect Dis 2004;10(2):287-93.
- Wallington T, Berger L, Henry B et al. Health Canada Update: Severe acute respiratory syndrome – Toronto, 2003. CCDR 2003;29(13):113-17.
- Bell JAH, Hyland S, DePellegrin T et al. SARS and hospital priority setting: A qualitative case study and evaluation. BMC Health Serv Res 2004;4:36. Available from: http//www.biomedcentral.com/1472-6963/4/36.
- Christian MD, Poutanen SM, Loutfy MR et al. Severe acute respiratory syndrome. Clin Infect Dis 2004;38(10):1420-27.
- Seto WH, Tsang D, Yung RWH et al. Effectiveness of precautions against droplets and contact in prevention of nosocomial transmission of severe acute respiratory syndrome (SARS). Lancet 2003;361:1519-20.
- Ho AS, Sung JJY, Chan-Yeung M. An outbreak of severe acute respiratory syndrome among hospital workers in a community hospital in Hong Kong. Ann Intern Med 2003;139(7):564-67.
- Lau JTF, Fung KS, Wong TW et al. SARS transmission among hospital workers in Hong Kong. Emerg Infect Dis 2004;10(2):280-86.
- Loeb M, McGeer A, Henry B et al. SARS among critical care nurses, Toronto. Emerg Infect Dis 2004;10(2):251-55.
- Wong TW, Lee CK, Tam W et al. Cluster of SARS among medical students exposed to single patient, Hong Kong. Emerg Infect Dis 2004;10(2):269-76.
- Le DH, Bloom SA, Nguyen QH et al. Lack of SARS transmission among public hospital workers, Viet Nam. Emerg Infect Dis 2004;10(2):265-68.
- Park BJ, Peck AJ, Kuehnert MJ et al. Lack of SARS transmission among healthcare workers, United States. Emerg Infect Dis 2004;10(2):244-48.
- Poutanen SM, Vearncombe M, McGeer AJ et al. Nosocomial acquisition of methicillin-resistant Staphylococcus aureus during an outbreak of severe acute respiratory syndrome. Infect Control Hosp Epidemiol 2005;26(2):134-37.
- Yap FHY, Gomersall CD, Fung KSC et al. Increase in methicillin-resistant Staphylococcus aureus acquisition rate and change in pathogen pattern associated with an outbreak of severe acute respiratory syndrome. Clin Infect Dis 2004;39(4):511-16.
- Chai LYA, Ng TM, Habib AG et al. Paradoxical increase in methicillin-resistant Staphylococcus aureus acquisition rates despite barrier precautions and increased handwashing compliance during an outbreak of severe acute respiratory syndrome. Clin Infect Dis 2005;40(4):632-33.
- Tokars, JI, et al., Use and efficacy of tuberculosis infection control practices at hospitals with previous outbreaks of multidrug-resistant tuberculosis. Infect Control Hosp Epidemiol 2001;22(7):449-55.
- Fung C-P, Hsieh T-L, Tan K-H et al. Rapid creation of a temporary isolation ward for patients with severe acute respiratory syndrome in Taiwan. Infect Control Hosp Epidemiol 2004;25(12):1026-32.
- Maunder R. The experience of the 2003 SARS outbreak as a traumatic stress among frontline healthcare workers in Toronto: Lessons learned. Philos Trans R Soc Lond B Biol Sci 2004;359(1447):1117-25.
- Robertson E, Hershenfi eld K, Grace SL et al. The psychosocial effects of being quarantined following exposure to SARS: A qualitative study of Toronto healthcare workers. Can J Psychiatry 2004;49(6):403-07.
- Loeb MB. Severe acute respiratory syndrome: Preparedness, management, and impact. Infect Control Hosp Epidemiol 2004;25(12):1017-19.
- Srinivasan A, McDonald LC, Jernigan D et al. Foundations of the severe acute respiratory syndrome preparedness and response plan for healthcare facilities. Infect Control Hosp Epidemiol 2004;25(12):1020-25.
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