...serious incongruities [in infection control] exist between the standards of clinical practice throughout the world.

Despite more than three decades of formal infection control programs in the United States (Haley & Shachtman, 1980) and other industrialized countries (Balcom & Palmer, 1962; Horan-Murphy et al., 1999), serious incongruities exist between the standards of clinical practice throughout the world. Some variability in these standards relates to limitations in available equipment and devices, and the absence of basic infection control infrastructure, such as the presence of sinks to promote handwashing or physical facilities in which to isolate infectious patients. Appropriate and safe use of infection control equipment and resources also varies. This variation is often due more to behavior and attitudes of an individual health care worker rather than the setting in which he or she practices.(Archibald & Reller, 2001; Cardo & Soule, 1999; Kermode et al., 2005; Memish, Cunningham, & Soule, 2005; Soule & Memish, 2001)

This article provides a brief overview of global challenges in infection control and Severe Acute Respiratory Syndrome (SARS). The author, who worked for the World Health Organization (WHO) as a short-term consultant during the SARS outbreak of 2003, reports field observations and describes selected examples of highly innovative, SARS-related infection control practices observed in three affected countries during the height of the outbreak. These examples relate to patient segregation and risk assessment, strategies to limit access to clinical areas, health care worker protection, and efforts to promote public confidence. The conclusion considers lessons learned and potential usefulness of these innovations in the post-2003 SARS era, as imminent threats loom of a global outbreak of influenza and sporadic increase in human infections with avian influenza virus.

Global Challenges in Infection Control

...fundamental infection control cornerstones are often absent in developing countries.

In the United States, Australia, Canada, and the United Kingdom, infection control practice is underpinned by public policy, legislative mandates, and standards developed or endorsed by relevant professional associations (Horan-Murphy et al., 1999; Jackson & Massanari, 2000; Larson, 2003; LeBlanc & Whyman, 1995; Masterton, Teare, & Richards, 2002; Murphy & McLaws, 2000; Whyman, 1994). In these countries, standard infection control education, through recognised tertiary courses and regular scientific meetings, is also available. In contrast, these fundamental infection control cornerstones are often absent in developing countries. As a result, infection control practice in developing countries can be haphazard, with ineffective efforts to minimise disease transmission.

Sudden Acute Respiratory Syndrome

In early 2003, the global infection control community faced perhaps its greatest challenge: sudden acute respiratory syndrome (Peiris, Yuen, Osterhaus, & Stohr, 2003). SARS is a condition that emerged in southern China in November 2002 and spread rapidly throughout the world, despite a global alert issued by the World Health Organization (WHO) on 12 March 2003 (Gerberding, 2003). SARS spread most prolifically throughout the South East Asian countries included in the WHO-defined Western Pacific region (Peiris et al., 2003). The eventual SARS toll was substantial, with 8,098 cases and 774 deaths (Ligappa, McDonald, Simone, & Parashar, 2004).

...health care workers were compelled to adopt unique and innovative strategies to provide protection from SARS transmission.

The rapid spread of SARS, its unique capacity to infect health care workers, and its many unknown features in the early days of the outbreak, meant that health care workers were unsure of the most effective methods of infection control to prevent its transmission (Seow, 2003). As a result, infection control responses varied greatly. Further variation in clinical infection control practices resulted from differences between South East Asian countries in their pre-SARS practices and policies for preventing transmission of health care associated infections (Lee et al., 2004). Inadequate supply of commercially available personal protective apparel in the southern hemisphere during the outbreak, and the author’s observation of lack of familiarity with its use in some South East Asian countries prior to SARS, also contributed to variation in infection controls adopted during the SARS outbreak (Kermode et al., 2005). In these circumstances, health care workers were compelled to adopt unique and innovative strategies to provide protection from SARS transmission. These strategies are discussed and pictured below.

Author Background

From 17 April to 19 May 2003, the author worked as a short-term consultant for the World Health Organization (WHO). Terms of reference for the consultancy included rapid assessments of clinical and isolation facilities and infection control practices in a small sample of health facilities in Singapore, Macau, and the Peoples’ Republic of China (PRC). In each country, the author, as a WHO representative, undertook assessments at the invitation of the national government and in collaboration with senior staff from the local Ministries of Health (MoH). Hospitals to be inspected were selected by the local MoH according to the severity of current or anticipated SARS caseload, their need for expert infection control input, and availability of in-house staff to facilitate and participate in the on-site assessment.

...risk assessment, patient segregation, limitation of access, health care worker safety, and promotion of public confidence...are critical elements of standard outbreak management.

The author assessed SARS preparedness and compliance with relevant sections of the WHO Infection Control Guidelines during hospital visits. Assessment and information gathering also involved interviews with members of the infection control and clinical staff. During these interviews the consultant asked open-ended questions, in English, to elicit information. The questions concerned SARS-related infection control policy, education, quality assurance activities, the greatest challenges faced in the outbreak, and the most important information about SARS-related infection control that staff wished to convey to the broader infection control community. Onsite inspection included, at a minimum, assessment of infection control capacity and underlying policy context review of triage procedures; emergency departments or fever clinics; isolation capacity; intensive care units (where they existed); available personal protection; high-risk procedures; staff health monitoring; screening and limitation of visitors; and inter and intra-hospital patient transfer policies.

The author reviewed 14 hospitals, 4 fever clinics, a traditional Chinese medical center, and a public health laboratory in Singapore, Macau, and PRC during the mission. The five selected examples, described and pictured in this article, are field observations from this experience. The examples relate to risk assessment, patient segregation, limitation of access, health care worker safety, and promotion of public confidence. These items are critical elements of standard outbreak management.

Field Observations

Observed Methods of Risk Assessment and Patient Segregation

One innovation employed in Singapore [to segregate and eliminate unnecessary exposure] was the use of screening triage areas outside of the Emergency Department.

Risk Assessment. Patients were assessed and classified according to World Health Organisation case definitions of SARS (World Health Organisation, 2003a). Probable and suspect cases were admitted into isolation in a specified clinical area of Singapore’s designated SARS hospital. Where possible, all non-SARS patients were discharged or transferred from the SARS hospital in an effort to reduce transmission risk to hospital visitors, inpatients, and staff.

Patient Segregation. Quarantine and/or isolation have been used for several decades to limit contact between at-risk and infectious patients (Jackson & Lynch, 1985). Typically, patients are isolated based on a presumptive or known diagnosis of their infectious status. Isolation generally involves placement of the patient in a cohort with similarly infected patients or isolation in a single room within a ward. Access to the patient is limited and signage is often employed to ensure that all health care workers are aware of the patient’s segregation. A major flaw in this system is delay in implementation of isolation until a patient is admitted to the hospital. As such, staff in receiving areas (e.g., the Emergency Department) can experience inadvertent exposure during the time when a patient receives initial health care and assessment (Li, Cheng, & Gu, 2003). The nature of care delivered in Emergency Departments, including the frequent clinical assessment of patients, makes isolation impractical and difficult.

Colored beach umbrellas were placed equidistant [and] patients were instructed to remain within the shaded part of the umbrella...

During the 2003 SARS outbreak, governments, health administrators, and clinicians identified the increasing incidence of disease among the community. As a result, a variety of screening measures were adopted to expedite patient segregation and eliminate unnecessary exposure among health care workers and other patients. One innovation employed in Singapore to meet these goals was the use of screening triage areas outside of the Emergency Department. The triage areas were tent-like in their structure. They included a designated route for patient flow according to preliminary assessment, which included measurement of temperature, blood pressure, oxygenation, and respiratory rate. Patients were positioned at least one metre (approximately three feet) from each other in designated seats to limit the opportunity for patient-to-patient spread. All staff working in the area wore comprehensive personal protective equipment, including N95 masks and protective eyewear (Seow, 2003).

In Chinese hospitals, possible SARS cases were routinely assessed in Fever Clinics that posed a real risk of outpatient transmission due to close proximity to other patients (Li et al., 2003; Pang et al., 2003). In one hospital, health care workers adopted a unique system to maintain distance between patients waiting to be assessed. Colored beach umbrellas (Picture 1) were placed equidistant (approximately two metres from each other) in a straight line. Patients were instructed to remain within the shaded part of the umbrella as this would provide protection from the heat of the sun and ensure distance from other potentially infectious patients. The colored umbrellas also provided brightness in an otherwise stark and distressing environment.

Picture 1. Patient Segregation with use of Beach Umbrellas
(Murphy, C. personal collection).

Observed Strategies to Limit Access to Clinical Areas

...nurses were stationed at hospital entry points and they provided information, warnings, and temperature checks to all entrants.

Inpatient access was limited by the imposition of isolation. However, the potential remained for other hospital visitors and staff to inadvertently come into contact with the patient’s immediate environment. To reduce this risk of exposure, hospitals employed a range of innovative measures. For example, in most hospitals, nurses were stationed at hospital entry points and they provided information, warnings, and temperature checks to all entrants (Picture 2). In some facilities security staff were employed at the entrances, in addition to the nurses, to assist with maintaining order. The major Singaporean SARS hospital closed all but one elevator from service so that movement throughout the hospital could be monitored and limited. Comprehensive screening was performed on all persons seeking to enter clinical areas that housed SARS patients. These measures were also used to limit media personnel from seeking exclusive images and insights into the SARS clinical setting and patients.

Picture 2. Limitation of Access - Nurses Stationed at Hospital Entry
(Murphy, C. personal collection).

Protection of Health Care Workers

An important component of WHO intervention was to ensure that all health care workers were aware of appropriate precautions and competent in use of personal protective equipment.

At the peak of the 2003 outbreak, SARS affected an unprecedented number of health care workers, some of whom succumbed to it. Such occupational risk was unprecedented and challenges faced by clinical staff working in these conditions have been well described elsewhere. An important component of WHO intervention was to ensure that all health care workers were aware of appropriate precautions and competent in use of personal protective equipment (PPE). Recommended personal protective equipment and apparel included a face mask, single pair of gloves, eye protection, disposable apron, and footwear able to withstand decontamination. Where available, N95 or P100 masks were preferred as they provide a high level of protection (99% filtering efficiency) (Loeb et al., 2004; Seto et al., 2003; World Health Organisation, 2003b).

Availability and types of PPE used throughout Asia varied greatly. However, in all facilities visited by the author, clinicians paid great attention to compliance with the locally approved system in use. The level of compliance with recommendations was striking, especially in view of well documented breaches in standard infection controls during non-SARS times.

Picture 3. Typical Personal Protective Equipment
(Murphy, C. personal collection).

[Use of a mirror] was an uncomplicated intervention that ensured the highest possible level of protection...

During observational visits, the author was struck by two simple measures that had been designed and introduced by health care workers independent of WHO or CDC recommendations. The first involved the use of a pocket or small mirror to assess the fit of a face mask and to ensure that there were no visible gaps that could potentially lead to health care worker exposure (Picture 4). This was an uncomplicated, inexpensive intervention that ensured the highest possible level of protection using the limited available resources.

The second innovative measure was the use of an isolation-buddy. The isolation buddy was an external observer whose key role was to remain outside of the patient room and to closely observe the health care worker who was providing direct clinical care. In the event of an inadvertent breach of PPE, such as touching of the face, the isolation buddy would immediately draw the caregiver’s attention to the breach and ensure their rapid removal from the immediate clinical setting until appropriate remedial measures could be employed. In view of the long hours worked, the high stress nature of the care provided, and the general discomfort of wearing full PPE apparel in extreme humidity, clinical caregivers were often unable to function at their previous levels of clinical competence (Maunder et al., 2003). The presence of a reliable “buddy” provided needed support and contributed to a safer working environment.

 
Picture 4. Use of Mirror to Check Mask Fit.
(Murphy, C. personal collection).

Government and Media Efforts to Promote Public Confidence

Variability in public perceptions regarding infectious diseases and misinterpretation of infection controls is well documented. However, the unprecedented nature of SARS, and limited knowledge about it in both the public and clinical communities in the earliest days of the epidemic, resulted in significant levels of community concern (Arguin, Navin, Steele, Weld, & Kozarsky, 2004; Person, Sy, Holton, Govert, & Liang, 2004). For already stressed health care systems to cope with the unprecedented demands common in the 2003 outbreak, public education and cooperation were critical.

A key goal of all governments was to instill a sense of public confidence in the local health system.

A key goal of all governments was to instill a sense of public confidence in the local health system (Arguin et al., 2004). A variety of measures were used to achieve this goal, ranging from regular media releases; the introduction of designated call centres to handle community concerns; and provision of updated statistics of SARS cases and areas of local transmission. Despite these measures, in some countries the public held serious concerns. In an extreme example in Singapore, nurses using public transport were discriminated against as members of the public accused them of spreading SARS within the community.

On a lighter note, a source of inspiration to a small hospital in Manila was advertising, at the entrance to their Emergency Department, the number of days they had been "SARS Free." The author assumed that publication of this information was made in an effort to instill public confidence in the perceived low level of community risk for SARS in Manila at the time.

Lessons Learned and Current Challenges

The rapid spread of SARS was unprecedented in modern infectious diseases...and provided a rich opportunity for clinicians to test the practicalities of new approaches to infection control and to identify deficiencies...

A unique feature of SARS was its ability to spread within health care settings with 1725 health care worker infections accounting for 20% of total reported global cases ("Protecting against SARS during equipment maintenance," 2003). The rapid spread of SARS was unprecedented in modern infectious diseases and as such, resulted in urgent, intensive efforts to disseminate information (Gerberding, 2003), improve infection control (Seto et al., 2003), and carefully prepare in unaffected countries (Cameron, Rainer, & De Villiers Smit, 2003). By necessity, these efforts and preparedness preceded identification of the causative agent, a novel coronavirus (Guan et al., 2003), in early April 2003 and detailed conclusive information about the specific routes of SARS transmission.

Challenging conditions, as previously noted, made designing appropriate, effective, and standard infection control responses difficult. Variation in pre-SARS infection control capacity between nations and regions of the world, the absence of universally accepted and applicable generic infection control guidelines, and differences in routinely available personal protective apparel during the outbreak limited the extent to which a standardized minimum global level of infection control could be guaranteed. In that environment, innovation was necessary and the examples cited in this article most likely represent a small proportion of unique local responses to the unprecedented infection control requirements of the 2003 SARS outbreak.

The most efficient method of minimizing exposure and disease transmission appears to be rigourous, consistent use of personal protective apparel.

In 2006, public health experts simultaneously grapple with increased reports of human infection with avian influenza virus and the prediction that the world will again be faced with a separate, global outbreak of human influenza (Perdue & Swayne, 2005; Schultsz et al., 2005; Yuen & Wong, 2005). The 2003 SARS outbreak provided a rich opportunity for clinicians to test the practicalities of new approaches to infection control and to identify deficiencies with existing controls (Seto et al., 2003). Subsequent to the SARS outbreak, researchers have further investigated and reported on the most efficient strategies for reducing patient and health care worker transmission of respiratory viruses. The most efficient method of minimizing exposure and disease transmission appears to be rigourous, consistent use of personal protective apparel (Chow, 2004). Elsewhere researchers have described particular clinical scenarios which appear to have been associated with increased risk of exposure to SARS (Lau et al., 2004; Loeb et al., 2004). Their identification is useful as a prompt to all health care workers to remain routinely vigilant when performing "high-risk" activities, including cardiopulmonary resuscitation, intubation, suctioning, or oxygen mask manipulation (Christian et al., 2004; Loeb et al., 2004).

Challenges for...experts and policymakers are to work toward a minimum standard of practice and to consider the potential value...of the unique contributions developed.

Vigilance is especially important in the event of a global influenza or Avian influenza pandemic.

Challenges for local, national, and global experts and policy makers are: 1) to work toward a minimum standard of infection control practice and 2) to consider the potential value, or otherwise, that incorporation of the unique contributions to routine practice developed during the SARS outbreak could make toward improved global levels of infection control and increased patient safety (World Health Organisation, 2003c). As well, several routine infection controls, including use of isolation buddies and mask efficiency, remain untested, incompletely evaluated, or subject to debate. Clarification of the proven efficacy of each item of personal protective apparel and all components of isolation against respiratory virus transmission is needed and could potentially reduce the high degree of global infection control inconsistency observed during the 2003 SARS outbreak.

Author

Cathryn Murphy RN, MPH, CIC, PhD
E-mail: cmurp@bigpond.net.au

Associate Professor Cathryn Murphy is an epidemiologist and holds an academic appointment in the Faculty of Health Sciences and Medicine at Bond University in Queensland, Australia. Cathryn has been active within the infection control community since 1989. Career highlights include a position as a guest researcher in the Division of Healthcare Quality and Infection Prevention at the Centers for Disease Control and Prevention, Atlanta, Georgia in 2000; and a short-term mission throughout South East Asia with the World Health Organisation during the height of the 2003 SARS Outbreak. She is currently a Managing Director of Infection Control Plus, an independent, global infection control consulting company.

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