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Canadian Journal of Anesthesia 53:122-129 (2006)
© Canadian Anesthesiologists' Society, 2006
General Anesthesia

Intubation of SARS patients: infection and perspectives of healthcare workers

[L’intubation de patients atteints du SRAS: infection et perspectives des travailleurs de la santé]

Karen M. Caputo, BASc*, Robert Byrick, MD*, Martin G. Chapman, MD*, Barbara J. Orser, PhD{dagger} and Beverley A. Orser, MD PhD*

* From the Department of Anesthesia, University of Toronto, Toronto; and the
{dagger} School of Management, University of Ottawa, Ottawa, Ontario, Canada.

Address corresponding to: Dr. Beverley A. Orser, Department of Anesthesia, Room 200-M3, Sunnybrook and Women’s College Health Science Centre, 2075 Bayview Avenue, Toronto, Ontario M4N 3M5, Canada. Phone: 416-978-0574; Fax: 416-978-4940; E-mail: beverley.orser{at}utoronto.ca


   Abstract
TOP
 Abstract
Introduction
 Methods
 Results
 Discussion
 References
 
Purpose: The outbreak of severe acute respiratory syndrome (SARS) in 2003 presented major challenges to the safety of anesthesiologists and other healthcare workers (HCWs). This study determined the incidence of SARS transmission to HCWs who intubated patients and analyzed the concerns of HCWs regarding personal and patient safety.

Methods: Healthcare workers who performed tracheal intubation in 10 Toronto hospitals were identified using the Ontario Public Health database. A questionnaire was used to collect information from the HCWs. To determine if the patterns of personal protection or concerns changed over time, data were analyzed according to whether the intubation occurred during SARS 1 (February 23 to April 21) or SARS 2 (April 22 to July 1).

Results: Thirty-three HCWs who performed 39 intubations on 35 SARS patients were interviewed. Three of 23 HCWs (13%) acquired SARS during SARS 1 whereas none (0/10) acquired SARS during SARS 2. Personal protection increased from SARS 1 to SARS 2 and HCWs’ concerns changed over time. During SARS 1, concerns focused on the need for personal protective equipment whereas during SARS 2, concerns focused on the need for strict training and patient care protocols. HCWs perceived that their experiences were ineffectively integrated into risk management protocols.

Conclusions: Protection guidelines failed to completely prevent the transmission of SARS to HCWs. Nine percent of the interviewed HCWs who intubated patients contracted SARS. A Risk Analysis Framework is presented to facilitate the rapid integration of HCWs’ experiences into practice guidelines.


   Introduction
TOP
 Abstract
 Introduction
Methods
 Results
 Discussion
 References
 
THE management outbreak of severe acute respiratory syndrome (SARS) in 2003 resulted in 438 probable or suspected cases and 43 deaths in the Toronto area. During the epidemic, protocols were developed to reduce the risk of transmission.1–4 These protocols were based on the consensus opinion of infectious disease experts but were initially guided by minimal clinical data. Procedural lists and protocols were frequently revised during the epidemic, sometimes changing several times over the course of a day. Further, not all hospitals had personal protective systems (PPS), such as Stryker suits (Stryker Corporation, Kalamazoo, MI, USA), which were recommended for the protection of HCWs.5

Despite existing safety protocols, 51% of the SARS cases were HCWs of which three died.6 In several cases, the disease was transmitted to family members of HCWs including children. Intubation occurred in 26% of cases and was considered a high-risk procedure for SARS transmission.2 Anesthesiologists and other critical care providers were considered to be at particular risk for infection during endotracheal intubation because the primary mode of transmission was thought to be through contact of mucous membranes with infectious respiratory droplets or fomites.2 Airway management protocols were quickly developed by infection control experts who often lacked expertise in the management of airway problems, and experts in airway management who lacked expertise in infection control. Furthermore, some protocols were proposed by caregivers that had no experience treating SARS patients. Healthcare workers who were directly involved in patient care had limited opportunities to inform policy makers about appropriate protocols and/or refine treatment guidelines.

The purpose of this study was to: 1) determine the incidence of infection in HCWs who intubated SARS patients; 2) identify the self-protection measures used by HCWs during intubation; and 3) solicit recommendations from HCWs who might assist with the management of future pandemics. Based on the responses, a risk management framework was developed to facilitate the rapid integration of HCW experiences into treatment guidelines for the management of future outbreaks of highly infectious diseases.


   Methods
TOP
 Abstract
 Introduction
 Methods
Results
 Discussion
 References
 
The study protocol was approved by the Public Health Department of Ontario as part of a provincial investigation into the SARS outbreak. The Institutional Ethics Review Board of Sunnybrook and Women’s College Health Sciences Centre approved the questionnaire and research protocol.

Patients who were intubated because of SARS were identified by researchers from the hospital section of the Toronto SARS investigation team using medical records from the Ontario Ministry of Health and Long Term Care, local public health units and hospitals. The HCWs who performed the intubations were identified from the medical records.

Study design and questionnaire
Verbal consent was obtained from respondents with the understanding that they could withdraw from the study at any time. Healthcare workers were interviewed individually and were assured of confidentiality. Each interview was conducted by two investigators and one of the investigators transcribed the information from all interviews.

The interview protocol consisted of three sections (Appendix I, available as Additional Material at www.cja-jca.org), including patient information, HCW information, and HCW recommendations for future outbreaks. The pre-SARS physical status of the patients was classified according to the presence of systemic disease and its impact on daily activity using the American Society of Anesthesiologists’ (ASA) classification of physical status.7 A clinical assessment of the airway anatomy (Mallampati score) was used to predict the view of the larynx during direct larygoscopy.8 The Cormack-Lehane score categorized the actual view of the glottic opening during laryngoscopy.9 The motor activity assessment score (MAAS) was used to estimate the level of patient sedation during the intubation procedure.10

Responses to the questionnaire were recorded throughout the interviews using Microsoft Access database software. The use of semi-structured interviews allowed HCWs to provide detailed information about the procedure. Responses to the opinion and recommendation sections were entered as free text. Subsequently, data were entered into NUD*IST qualitative software program (QSR International, Melbourne, Australia) for coding and analysis. The qualitative data from open-ended questions were iteratively grouped to identify common themes. These themes directed the development of a conceptual model for risk management during an infectious disease outbreak.

Data analysis was undertaken in two phases. The text data were first reviewed in the NUD*IST program and entered into groups pertaining to type of recommendation. Analysis of these groups revealed that most of the HCW comments were observations rather than recommendations. Next, an analysis was undertaken to identify potential changes in the nature and incidence of HCW observations and recommendations during SARS 1 and SARS 2.

Analysis of data
The experiences of HCWs who did and did not develop SARS were compared for intubations performed during SARS 1 (February 23 to April 21, 2003) and SARS 2 (April 22 to July 1, 2003). Differences between the groups were analyzed using a Chi-squared test and a significant difference was considered to exist at P < 0.05.


   Results
TOP
 Abstract
 Introduction
 Methods
 Results
Discussion
 References
 
Patient and caregiver identification
The database identified 59 HCWs who performed at least one intubation of a SARS patient. Ten of the 59 HCWs failed to respond to multiple attempts to contact them, either by telephone or in person. Of the 49 HCWs who were contacted, 33 consented to be interviewed. The most common reason for declining the invitation to participate in the study was involvement in other SARS studies that consumed substantial amounts of time. The interviews were conducted during a six-month interval from August 1, 2003 to January 31, 2004.

The 33 participating HCWs performed 39 intubations of 35 SARS patients. The intubations were performed in ten Toronto hospitals; four were fully affiliated University teaching hospitals and six were community-based hospitals. Approximately 59% (23/39) of the intubations occurred during the SARS 1 and 41% (16/39) during SARS 2.

The 33 HCWs interviewed included 22 anesthesiologists, five respiratory therapists, three specialists in internal medicine, and three physicians from other specialties. Seven HCWs had less than five years of clinical post-graduate experience; five had six to ten years; nine had 11 to 15 years and 12 had greater than 15 years. Three of the 33 HCWs, including two anesthesiologists, acquired SARS. All SARS infections occurred during SARS 1.

The mean age of the 35 patients was 58.4 yr (range 33–86). Nineteen patients were female and 16 were male. Table IGo summarizes the number of infected HCWs in relation to the ASA physical status of the patient prior to SARS and Mallampati and Cormack-Lehane scores. Table IIGo summarizes the transmission during SARS 1 and SARS 2 as it relates to the ASA physical status, Mallampati score and Cormack-Lehane score of the patients.


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  		TABLE I SARS infection of HCWs, ASA classification (pre-SARS) and airway assessment scores
 

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  		TABLE II SARS infections of HCWs in relation to ASA score and airway assessment scores for patients during SARS 1 and SARS 2
 
Preintubation therapy
A variety of techniques were used prior to the intubation. For HCWs who acquired SARS, two of their patients were treated with bilevel positive airway pressure (Bi-PAPTM; Respironics, Inc., Carlsbad, CA, USA), and the third patient received high-flow oxygen from a facemask. For the HCWs who did not acquire SARS, 29 of their patients received high-flow oxygen and seven were treated with Bi-PAP. During SARS 1, eight of 23 patients were treated with Bi-PAP, whereas only one of 16 patients was treated with Bi-PAP during SARS 2 (P < 0.05).

Drugs administered
Table IIIGo outlines the urgency of intubation and the use of sedative and paralytic drugs. Emergent intubations were more likely to be associated with the transmission of SARS (P < 0.05). Notably, no patient was treated with antisialogue drugs despite recommendations to do so. There was no statistical difference in the urgency of intubation between SARS 1 and SARS 2 or the likelihood that HCWs used sedative or paralyzing agents.


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  		TABLE III Urgency and management of intubation during SARS 1 and SARS 2 and incidence of SARS in HCWs in relation to management strategies
 
Intubation
Table IVGo summarizes the incidence of SARS infection, and techniques used for intubation and the number of attempts. Two of the three intubations that resulted in SARS transmission required two or more attempts. The average number of HCWs present in the patient’s room during intubation was 3.6 (range 2–9). The numbers of HCWs present in the room during the three intubations associated with SARS transmission were three, five and seven. There was a trend towards higher MAAS for patients during SARS 1 compared to SARS 2 (P = 0.05, Table VGo).


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  		TABLE IV SARS infection of HCWs in relation to the techniques and the number of attempts at intubation
 

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  		TABLE V The incidence of SARS infection of HCWs and the MAAS during the intubation
 
Healthcare worker protection
The protective equipment used by HCWs during intubation is summarized in Table VIGo and Figure 1Go. None of the infected HCWs wore PPS or double gloves. Two wore a N95 mask (Tecnol Medical Products, Inc, Fort Worth, TX, USA) and one wore both goggles and a face shield. During SARS 1, HCWs were less likely to wear PPS, double gloves, a N95 mask, and a face shield compared to SARS 2 (P < 0.05). The use of goggles was comparable between the two periods (Figure 1Go).


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  		TABLE VI Incidence of SARS infection of HCWs and personal protective equipment (body substance precautions) and personal protective system (PAPR hood or Stryker suit)
 

Figure 1
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  		FIGURE 1 Healthcare workers personal protection during severe acute respiratory syndrome (SARS) 1 and SARS 2. The use of personal protective equipment, gloves, masks and face shields increased during SARS 2 compared to SARS 1 (P < 0.05).

 
Recommendations and observations
Respondents were asked to provide recommendations for the future management of SARS patients. The responses were categorized as either recommendations or observations (Appendices II and III, available as Additional Material at www.cja-jca.org). Figure 2Go illustrates how HCWs’ recommendations changed over the two periods of the outbreak. During SARS 1, HCWs’ recommendations focused on the need for highly experienced personnel, the need for additional personnel, and the use of personal protective equipment. Recommendations from HCWs during SARS 2 were focused on the need for greater awareness by the medical staff regarding the importance of adhering to strict protocols.


Figure 2
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  		FIGURE 2 The number of recommendations by healthcare workers (HCWs) during severe acute respiratory syndrome (SARS) 1 and SARS 2. During SARS 1, HCWs’ recommendations focused on the need for highly experienced personnel, the need for additional personnel and use of protective equipment. Recommendations by HCWs during SARS 2 were primarily focused on the need for better education for medical staff about the importance of adhering to strict protocols, rather than specific recommendations about the use of protective equipment.

 
The frequency of common observations is summarized in Figure 3Go. During SARS 1, respondents frequently identified human error, such as a doctor leaving the room wearing a surgical cap or a failure to wash hands. During SARS 2, the observations related to both equipment and personnel factors such as the failure of a battery on a Stryker hood during disrobing, concerns that Stryker suits suck in room air, and the improper use of surgical masks by nurses and physicians.


Figure 3
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  		FIGURE 3 The frequency and type of observations reported by healthcare workers during severe acute respiratory syndrome (SARS) 1 and SARS 2. During SARS 1, observations focused on human actions including a doctor leaving the room with surgical cap still on, failure to wash, lack of negative ventilation rooms. During SARS 2, most observations related to both equipment and personnel factors such as battery failure on Stryker hood during disrobing, concern that Stryker suits suck in room air, and improper use of masks by nurses and physicians. Fewer observations about policy and guidelines were observed during SARS 2.

 
Development of a risk management framework
A data-derived risk management tool was then developed to facilitate the development of guidelines based on HCWs’ responses. The framework consisted of three broad categories or "breakpoints" in the system which potentially increased the risk of infection. These potential areas of weakness or vulnerability were categorized as: 1) process breakpoints; 2) people break-points; and 3) technology/infrastructure breakpoints. Table VIIGo outlines the framework and experience-based recommendations from which the framework was derived.


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  		TABLE VII
 

   Discussion
TOP
 Abstract
 Introduction
 Methods
 Results
 Discussion
References
 
Existing safety protocols and practice guidelines failed to protect all HCWs from SARS transmission during the 2003 outbreak.11–13 Anesthesiologists were at particular risk as 9% of the interviewed HCWs who performed an intubation contracted SARS. All SARS infections occurred during SARS 1 and the pattern of self-protection changed over time as the use of personal protective equipment increased during SARS 2. Since 26% of SARS patients required intubation, clearly the number of HCWs would rapidly decline if a similar trend occurred during a future outbreak.2 This unique dataset provides compelling evidence that aggressive measures are required to protect HCWs from viral transmission.

This report was subject to the considerable limitations of a questionnaire-based study and possible bias of the HCWs who agreed to participate. The sample size was small and possibly, not all HCWs who performed an intubation were identified in the initial chart review. Confounding factors and recall bias do not permit firm conclusions to be drawn regarding a causal link between increased personal protection strategies and the reduced number of infections during SARS 2. Nevertheless, it was apparent that HCWs developed their own self-protection strategies which were often stricter and sometimes inconsistent with policies out-lined by the Ontario Ministry of Health or hospitals.

The first provincial guidelines for intubation were published one month after the onset of SARS 1.14–16 These guidelines focused on both the intubation procedures ("intubate while the patient is sedated and paralyzed if medical condition permits") and personnel requirements ("the most experienced staff member should perform the intubation with a maximum of two to three persons present"). The time course suggests a lag in gathering local knowledge and providing feedback to practitioners. Responses from the HCWs suggest that the process underlying the development of guidelines was suboptimal as it did not incorporate the experiences of front-line staff, and guidelines were inconsistently implemented.

The challenges of developing effective guidelines in an acute situation cannot be underestimated. Discussions between the authors and experts that developed the guidelines highlighted several difficulties. The guidelines took weeks to develop from the time risk was identified due to: a) the absence of data; b) the high stress environment; c) an inability to hold face to face meetings in healthcare settings; d) difficulty in guaranteeing a supply of protective equipment after it was recommended; e) difficulty in coping with the competing risks of HCWs and patients; and f) an understandable lack of consensus on what the important issues were and how to deal with them.

In an editorial by Nicolle, the "chaotic" process of developing and distributing guidelines was eloquently described.17 Proposed solutions include the need to develop a mechanism for rapid development, communication and implementation of guidelines for infection control measures. A risk management strategy must be developed to rapidly translate the experience of frontline HCWs into treatment protocols for high risk situations. Responses from the HCWs in this study identified three key breakpoints or potential areas of vulnerability that must be addressed when developing such guidelines: 1) process; 2) people; and 3) technology/infrastructure.

In summary, consensus-based guidelines failed to prevent the transmission of SARS during SARS 1. Healthcare workers perceived that their experiences and advice were ineffectively integrated into risk management protocols. The data-derived risk analysis framework presented in this report may be useful to facilitate the integration of HCWs’ experiences into treatment guidelines during future epidemics.


   Acknowledgments
 
We thank the HCWs who consented to participate in this study, Ms. A. Shigayeva for administrative assistance, Drs. A. McGeer and K. Rose for their helpful comments on the manuscript, and Dr. K. Vicente for his invaluable contributions to the design of the study.


   Footnotes
 
This study was funded by grant support from the Departments of Anesthesia and Critical Care at Sunnybrook and Women’s College Health Science Centre, the E. W. R. Steacie Memorial Fellowship and the Ministry of Health and Long Term Care. B.A. Orser is supported by a Canada Research Chair in Anesthesia and the Canadian Institutes of Health Research.

Accepted for publication May 20, 2005. Revision accepted July 9, 2005.


   References
TOP
 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 
1 Peng PW, Wong DT, Bevan D, Gardam M. Infection control and anesthesia: lessons learned from the Toronto SARS outbreak. Can J Anesth 2003; 50: 989–97.[Abstract/Free Full Text]

2 Fowler RA, Guest CB, Lapinsky SE, et al. Transmission of severe acute respiratory syndrome during intubation and mechanical ventilation. Am J Resp Crit Care Med 2004; 169: 1198–202.[Abstract/Free Full Text]

3 Tsang KW, Ho PL, Ooi GC, et al. A cluster of cases of severe acute respiratory syndrome in Hong Kong. N Engl J Med 2003; 348: 1977–85.[Abstract/Free Full Text]

4 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.[Abstract/Free Full Text]

5 US Centers for Disease Control. Infection control pre-cautions for aerosol-generating procedures on patients who have suspected severe acute respiratory syndrome (SARS). March 20, 2003. Available from URL; http://www.cdc.gov/ncidod/sars/aerosolinfection-control.htm (accessed March 29, 2003).

6 Booth CM, Matukas LM, Tomlinson GA, et al. Clinical features and short-term outcomes of 144 patients with SARS in the greater Toronto area. [erratum appears in JAMA 2003; 290: 334]. JAMA 2003; 289: 2801–9.[Abstract/Free Full Text]

7 American Society of Anesthesiologists. ASA Physical Status Classification System. Available from URL; http://www.asahq.org/clinical/physicalstatus.htm.

8 Mallampati SR, Gatt SP, Gugino LD, et al. A clinical sign to predict difficult tracheal intubation: a prospective study. Can Anesth Soc J 1985; 32: 429–34.[Medline]

9 Cormack RS, Lehane J. Difficult tracheal intubation in obstetrics. Anaesthesia 1984; 39: 1105–11.[Medline]

10 Devlin JW, Boleski G, Mlynarek M, et al. Motor Activity Assessment Scale: a valid and reliable sedation scale for use with mechanically ventilated patients in an adult surgical intensive care unit. Crit Care Med 1999; 27: 1271–5.[Medline]

11 Scales DC, Green K, Chan AK, et al. Illness in intensive care staff after brief exposure to severe acute respiratory syndrome. Emerg Infect Dis 2003; 9: 1205–10.[Medline]

12 Lee N, Hui D, Wu A, et al. A major outbreak of severe acute respiratory syndrome in Hong Kong. N Engl J Med 2003; 348: 1986–94.[Abstract/Free Full Text]

13 Seto WH, Tsang D, Yung RW, 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.[Medline]

14 Kamming D, Gardam M, Chung F. I. Anaesthesia and SARS (Editorial). Br J Anaesth 2003; 90: 715–8.[Free Full Text]

15 Health Canada. Infection Control Guidance if there is a SARS Outbreak Anywhere in the World, When an Individual Presents to a Health Care Institution With a Respiratory Infection. 17 Dec 2003. Available from URL; http://www.phac-aspc.gc.ca/sars-sras/pdf/sars-icg-outbreakworld_e.pdf

16 SARS Provincial Operations Centre OMOHaL-TC. Directives to all Ontario acute care hospitals for high-risk procedures in critical care areas during a SARS outbreak. Directive 03-06 (R). May 1 2003, revised May 13 2003. Available from URL; http://www.health.gov.on.ca/english/providers/program/emu/sars/sars_obc/directives/dir_high_risk_procedures.pdf.

17 Nicolle L. SARS safety and science (Editorial). Can J Anesth 2003; 50: 983–8.[Free Full Text]




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This Article
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