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Febrile respiratory illness in the intensive care unit setting: an infection control perspective Matthew P. Mullera and Allison McGeerb Purpose of review We have examined studies published since the severe acute respiratory syndrome outbreak that elucidate the mode of transmission of respiratory pathogens and the optimal means of interrupting their transmission, focusing on transmission in the intensive care unit. Recent findings The severe acute respiratory syndrome may be transmitted by the droplet, contact and occasionally the airborne route. Transmission occurred most frequently when healthcare workers failed to use standard precautions such as hand washing or personal protective equipment designed to limit droplet and contact transmission. Aerosol-generating procedures increased transmission, but incomplete use of personal protective equipment during procedures was common. Recent publications have stressed the benefits of appropriate staffing levels, the use of single occupancy rooms, the immunization of healthcare workers against influenza, and the importance of healthcare workers remaining home when ill in reducing the morbidity and mortality of respiratory infection within the intensive care unit. Summary Most respiratory pathogens can be transmitted by more than one route. Despite this, healthcare worker awareness of clinical syndromes associated with respiratory pathogens that require airborne precautions, combined with the use of standard precautions for all patients, and contact/droplet precautions for patients with undifferentiated febrile respiratory illness should be effective in interrupting the transmission of respiratory pathogens within the intensive care unit. Keywords infection prevention and control, intensive care unit, respiratory tract infection, severe acute respiratory syndrome Curr Opin Crit Care 12:37–42. ß 2006 Lippincott Williams & Wilkins. a Department of Internal Medicine, Infectious Diseases Division, University of Toronto, Mount Sinai Hospital, Toronto, Ontario, Canada M5G 1X5 and b Department of Microbiology, University of Toronto, Mount Sinai Hospital, Toronto, Ontario, Canada M5G 1X5 Correspondence to Matthew P. Muller, MD, FRCPC, Department of Internal Medicine, Infectious Diseases Division, University of Toronto, Mount Sinai Hospital, Toronto, Ontario, Canada M5G 1X5 Tel: +1 416 586 3118; fax: +1 416 586 3140; e-mail: [email protected] Current Opinion in Critical Care 2006, 12:37–42 Abbreviations HCW ICU PAPR PPE SARS VAP healthcare worker intensive care unit powered air-purifying respirator personal protective equipment severe acute respiratory syndrome ventilator-associated pneumonia ß 2006 Lippincott Williams & Wilkins 1070-5295 Introduction Febrile respiratory illness is the most common reason for admission to an intensive care unit (ICU) [1]. In many cases, the illness is caused by infection and the infecting pathogen is transmissible. Infection control strategies designed to interrupt the transmission of respiratory pathogens in the ICU setting were tested during the global outbreak of the severe acute respiratory syndrome (SARS), generating new insights into the mode of transmission of respiratory pathogens and the optimal strategies to interrupt transmission. Although the general principles of infection control are no different in the ICU than in other areas of the hospital, patients with respiratory infection requiring ICU admission provide a number of specific challenges. Such patients are at the severest end of the clinical spectrum. For some infections, such as SARS, patients may be more infectious at the time of their ICU admission than at any other time during their illness [2,3]. ICU patients frequently require potentially aerosol-generating procedures, such as endotracheal intubation, tracheal suction, nebulized medications and bronchoscopy. The transmission of SARS was notably associated with healthcare worker (HCW) involvement in such high-risk procedures [3,4,5,6]. We have examined the recent literature on infection control strategies designed to prevent the transmission of respiratory pathogens in the ICU. Much of this literature focuses on SARS, but still provides important lessons that can be applied to other pathogens. We will not provide a general review of infection control within the ICU or address the prevention of ventilator-associated pneumonia (VAP). Instead, this review focuses on the exogenous transmission of respiratory pathogens within the ICU. VAP results primarily from endogenous infection, although infection control strategies are critical 37 Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited. 38 Respiratory system in preventing VAP and in reducing VAP caused by antibiotic-resistant organisms [7,8]. Rationale for concern about the transmission of respiratory pathogens The majority of patients with febrile respiratory illness admitted to the ICU do not pose a direct risk to HCWs either because the pathogen is not easily transmitted from person to person or because the resultant illness is unlikely to be severe in a healthy individual. Interrupting transmission remains a priority, however, as uncommon but virulent pathogens such as Mycobacterium tuberculosis or invasive group A streptococcus are capable of causing severe illness even in healthy HCWs. Furthermore, viral respiratory pathogens spread rapidly, increase mortality and morbidity in vulnerable ICU patients, and can cause illness among HCWs resulting in significant work shortages. Unfortunately, the etiology of respiratory infection is usually unknown at the time of ICU admission [9]. Therefore, a standard approach is required to protect both ICU HCWs and patients from the most common and dangerous respiratory pathogens. Transmission of respiratory pathogens Understanding the transmission of respiratory pathogens is the key step in developing a rational strategy to prevent infection. Fortunately, although there are many respiratory pathogens, there are only three routes of transmission within the ICU: airborne, droplet, or contact transmission (Table 1). Most respiratory pathogens are believed to be transmitted primarily or exclusively by the droplet route. Airborne transmission is considered to occur only with a select group of organisms: M. tuberculosis, measles, smallpox, and varicella-zoster virus (e.g. chicken pox or disseminated zoster). Contact transmission is recognized as a potential cause of transmission for many pathogens, but is generally considered less significant than droplet spread. Accumulating evidence suggests that the distinction between droplet and airborne transmission may not be as clear-cut as previously thought, and that the role of contact transmission may have been underestimated. SARS provides an example of the complexity of respiratory virus transmission. Initial reports suggested that SARS was transmitted by the droplet route [10,11]. However, in the Amoy Gardens outbreak, SARS cases appeared rapidly in several different apartment buildings in a manner atypical of contact or droplet transmission [12]. The airflow dynamics within and around the buildings corresponded to the distribution of illness, suggesting airborne transmission. The current hypothesis is that a bathroom exhaust fan aerosolized contaminated feces into an airshaft, with subsequent airborne transmission [12]. Reports in which HCWs developed SARS despite the appropriate use of personal protective equipment (PPE) effective for droplet transmission and instances of transmission over distances greater than 1 m are also suggestive of airborne transmission [5,13,14]. Aerosol-generating procedures may generate finer droplets than those produced spontaneously by coughing, resulting in transmission beyond 1 m and in ‘extended droplet’ transmission [15]. Others have suggested that the strict definition of airborne transmission should be modified to include obligate (i.e. only transmitted by the airborne route), preferential (i.e. most commonly transmitted by the airborne route), or opportunistic (i.e. transmitted by the airborne route under specific circumstances) airborne transmission [15,16]. Influenza is another example of a virus considered to be transmitted primarily by the droplet route. Both animal models and observational studies of human outbreaks, however, suggest that airborne transmission can occur with influenza [17–21]. In one outbreak a single ill passenger on an airplane with an inactivated ventilation system transmitted influenza to 91% of the passengers and crew, a finding highly suggestive of airborne transmission [17]. Contact transmission is important for a number of viral respiratory tract infections, including respiratory syncytial virus, parainfluenza virus and adenovirus [8]. Hand washing or hand disinfection has been associated with a reduction in the incidence of viral respiratory tract infections in several contexts [22,23,24]. Although droplet transmission was considered the primary mode of transmission for SARS, hand hygiene was consistently Table 1 Routes of transmission of respiratory pathogens in the intensive care unit Route Description Airborne Small droplets (< 5 mm) expelled from the respiratory tract of an infected individual dry and shrink while airborne, forming droplet nuclei capable of remaining airborne for prolonged periods and traveling large distances before being inhaled into the distal airways of a susceptible individual Large (> 10 mm) droplets are expelled from the respiratory tract of an infected individual and come into contact with the oral, nasal or conjunctival mucosa of a susceptible individual. The large size of the droplet ensures that they fall rapidly and prevents transmission over distances > 1 m Results from physical contact with an infected or colonized individual or through physical contact with a contaminated object Droplet Contact Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited. Febrile respiratory illness in the intensive care unit Muller and McGeer 39 identified as an effective means of reducing SARS transmission [8,25,26,27]. Direct contact with respiratory secretions was also an independent predictor of SARS risk, providing further evidence of the importance of contact transmission in SARS [26]. Given the uncertainty about the routes of transmission for many respiratory pathogens, including SARS and influenza, infection control strategies designed to reduce the transmission of infection from patients with undifferentiated febrile respiratory illness should not be strictly focused on the prevention of droplet transmission. For most patients with febrile respiratory illness, it should be assumed that droplet or contact transmission may occur, and that airborne transmission may also be important when there is a risk of aerosolization. This cautious approach is particularly important for virulent organisms such as the SARS coronavirus or pandemic influenza [28 –30]. Strategies to interrupt the transmission of respiratory pathogens The transmission of respiratory pathogens can be interrupted by limiting the number of susceptible or infected individuals in the ICU or by protecting the susceptible from the infected individuals. Removing susceptible and infected individuals from the intensive care unit Susceptible individuals can be ‘removed’ from the ICU by changing their immunological status from susceptible to immune through immunization. Although immunization is not available for most respiratory pathogens, influenza is an important exception. It has been repeatedly demonstrated that yearly influenza vaccination of HCWs in long-term care hospitals reduces all-cause mortality among the patients in their care by 30–40% [31,32]. Vaccination of ICU staff would be expected to confer similar benefits, particularly for elderly or immunocompromised patients, and would reduce illness and time off work among HCWs. Although infected patients cannot easily be removed from the ICU, infected HCWs can and should be. HCWs with symptoms of acute respiratory tract infection (e.g. fever and cough) should not report to work or be involved in the care of ICU patients, as this puts patients at risk of severe complications and will result in illness among other HCWs [8,33]. Finally, although infected patients cannot be completely removed from the ICU, caring for such patients in a single room limits the potential exposure of other patients and staff. The SARS outbreak also demonstrated the importance of having negative pressure, single-occupancy ICU rooms available. Two recent reports advocated that future ICUs consist exclusively of single-occupancy rooms, largely as a result of the recognition that single rooms are associated with a reduced risk of transmission of infectious pathogens and provide maximum flexibility during outbreaks of potentially airborne pathogens [34,35–38]. Interrupting transmission from infected to susceptible individuals within the intensive care unit Guidelines have described the infection control precautions that should be used for all patient contacts (e.g. routine practices or standard precautions) and for patient contacts when specific infectious pathogens are suspected (e.g. additional precautions) [39,40]. Routine practices/standard precautions include hand washing or hand disinfection before and after all patient contacts and the use of appropriate PPE when there is the potential for contact with blood or bodily fluids [39,40]. PPE may include the use of gloves, gowns, surgical masks and eye protection. For example, routine venipuncture requires the use of gloves. When performing endotracheal intubation or a nasopharyngeal swab that may induce coughing or sneezing, the use of gloves, gowns, masks and eye protection is required. Additional precautions require that HCWs are aware of the clinical syndromes associated with organisms that require additional precautions (e.g. fever, cough and an upper lobe infiltrate are suggestive of tuberculosis and require airborne precautions) [39]. Studies of SARS transmission among HCWs implicated failures in the appropriate use of PPE as a cause of transmission [3,4,25,41,42]. These were not only failures of SARS-specific (i.e. additional) precautions, but also failures of routine practices and standard precautions, such as the failure to perform hand hygiene, lack of eye protection during procedures likely to cause splashes, or the failure to wear gloves for contact with mucous membranes and respiratory secretions [4]. In some cases, failures may have resulted from a lack of appropriate infection control training or a lack of access to appropriate equipment [41]. The failure of HCWs to use accepted infection control precautions is a commonly described phenomenon. Studies consistently show that HCW compliance with hand hygiene recommendations is less than 50%, and that compliance is lowest when it is most important: in the ICU, for invasive procedures and for emergency procedures [43–45]. Studies of adherence to airborne precautions during the care of patients with drugresistant tuberculosis have also shown an inconsistent use of precautions [46]. Although studies of SARS have suggested that inadequate education and understanding of the need for and Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited. 40 Respiratory system application of PPE is one reason for reduced adherence to hand hygiene and the use of PPE, poor compliance, particularly in the ICU, has also been correlated with increased workload [43,47]. Recent studies have also demonstrated that a low nurse-to-patient ratio is associated with an increased risk of bloodstream infection in patients, presumably because of a breakdown in appropriate infection prevention practice [48–50]. The bottom line is that current infection prevention recommendations, if applied consistently and correctly, are capable of preventing virtually all transmission of respiratory pathogens in the ICU. Improving adherence among HCWs is the biggest challenge, and a multifaceted approach is required. Important measures include the provision of clear infection control guidelines, infection control education, feedback on rates of adherence and infection, adequate and accessible supplies, adequate staffing levels, positive role models among HCW leadership, a positive safety climate, and administrative support for infection control [43,51,52]. Controversies over the selection and use of personal protective equipment Although obtaining adequate adherence to existing guidelines is probably more important than improving or revising these guidelines, it is obvious that such guidelines should be based on the best evidence available. The simplest and most effective measures should be recommended. Several areas of controversy in the appropriate selection and use of PPE for ICU patients with febrile respiratory illness will now be discussed. N95 versus surgical masks During the SARS outbreak, N95 masks were recommended for HCWs caring for SARS patients. Several studies suggested that both surgical and N95 masks were protective, although in one of the studies cases related to an index patient receiving nebulized therapy were excluded from the analysis [25,42]. The authors concluded that droplet and contact precautions were sufficient provided that ‘no aerosolizations are expected’ [25]. In a Vietnamese outbreak in which N95 masks were not available for 3 weeks, no transmission occurred, suggesting that surgical masks are sufficient to protect from SARS [53]. A fourth study confirmed that both N95 and surgical masks confer protection but found a 50% reduction in risk with N95 compared with surgical masks [42]. This finding was not statistically significant, however. Taken together, these results suggest that in most cases combined droplet/contact precautions that include the use of a surgical mask are sufficient to prevent SARS transmission. Limited data suggest that the use of an N95 mask may confer additional protection. The use of an N95 mask may be particularly important when HCWs are involved in potential aerosol-generating procedures, although this was not directly addressed in these studies. Current Canadian guidelines no longer recommend N95 masks for the routine care of patients with undifferentiated febrile respiratory illness, but it may still be reasonable to consider the use of an N95 mask in combination with droplet/contact precautions if there is a suspicion that a highly virulent and transmissible pathogen may be present (e.g. avian influenza, SARS) [28,33]. Fit testing PPE must be used properly to be optimally effective. Fit testing involves testing HCWs to determine whether they can taste or smell chemical agents released while they wear the N95 mask. Fit checking is the process of ensuring that a seal has been obtained after putting on the mask. Fit checking should be performed every time an N95 mask is used. HCWs who have not been trained in the use of the N95 mask frequently fail fit testing [46,54]. Mandatory fit testing provides an opportunity to educate HCWs on the correct use of the N95 and the importance of fit checking, and also allows formal testing of the mask’s fit. Volunteers who do not receive fit testing have higher mucosal exposure to droplets than those who have fit testing [15,55]. When education was compared with education and fit testing, there was no difference in the proportion of HCWs who could subsequently pass a fit test [56]. The selection of good quality masks by the institution, and the provision of sufficient education to permit HCWs to select the best fitting mask and perform a fit check each time they use it, is probably more important than fit testing in ensuring that HCWs are using N95 masks correctly [15,56]. Powered air-purifying respirators During the SARS outbreak, an apparent failure of PPE led to recommendations for the use of powered airpurifying respirators (PAPRs) during aerosol-generating procedures [6]. PAPRs have been recommended for use when caring for patients with active tuberculosis, but these recommendations were challenged because of concerns about cost, the psychological impact on patients, and reduced vision, hearing, and ability to communicate [57]. The use of PAPRs was more acceptable to HCWs for SARS than it had been for tuberculosis, presumably because of a higher perceived risk [58]. No evidence is available on the effectiveness of PAPRs compared with the use of N95 masks, eye protection, gowns and gloves. Although the performance of aerosolgenerating procedures was associated with SARS transmission in several studies, failure to use the appropriate Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited. Febrile respiratory illness in the intensive care unit Muller and McGeer 41 PPE or to use PPE correctly were frequently described and may have been the primary cause of infection [3,4,5,6]. In two studies that adjusted for incorrect or incomplete PPE use [41,59], participation in a high-risk procedure was not associated with SARS transmission. In addition, concern has been raised that difficulties in the removal of PAPRs without selfcontamination may actually put HCWs at risk [59]. Clearly, if PAPRs are to be used, HCWs should be carefully trained in their use, removal and maintenance. There is currently no evidence to suggest that PAPRs should be used for ICU patients with undifferentiated febrile respiratory illness, either for routine care or during aerosol-generating procedures. The value of PAPRs during the care of ICU patients known to have SARS or other highly virulent organisms remains uncertain. It is important to recognize that any benefits of PAPRs accrue to HCWs, whereas their disadvantages pose risks primarily for patients, a situation that complicates the assessment of their use. Conclusion Patients with undifferentiated febrile respiratory illness, when admitted to the ICU, are a potential risk to both HCWs and other patients. Although the nature of infectious disease transmission is complex, a recognition of syndromes associated with airborne pathogens, and the consistent use of hand hygiene and droplet/contact precautions for patients with febrile respiratory illness, will be sufficient to interrupt transmission in the vast majority of cases. The biggest current challenge lies in identifying and implementing effective strategies designed to improve HCW adherence to these basic infection control priniciples. References and recommended reading Papers of particular interest, published within the annual period of review, have been highlighted as: of special interest of outstanding interest Additional references related to this topic can also be found in the Current World Literature section in this issue (pp. 68–69). Harrison DA, Brady AR, Rowan K. 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This editorial considers evidence on the transmission of SARS within ICUs and the association with aerosol-generating procedures and concludes that adherence to simple, established measures such as hand disinfection offers the best protection again SARS transmission within the ICU. Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.