Healthcare-Associated Infections Related to Respiratory Therapy
Keith S. Kaye
Dror Marchaim
David J. Weber
William A. Rutala
The most representative data on the incidence of healthcare-associated infections have been provided by the Centers for Disease Control and Prevention (CDC) via the National Healthcare Safety Network (NHSN, formerly NNIS) system. According to the NHSN system data, healthcare-associated pneumonia (HAP) is the third leading cause of device-related healthcare-associated infection (HAI) and second leading cause of HAI overall, accounting for approximately 16% of all HAIs and 24% to 27% of all infections acquired in medical intensive care and coronary care units (1,2, 3 and 4,5). The frequency (episodes per 100 hospitalizations) of HAP is 0.2 to 0.94, the lower rates being reported from small private hospitals and the higher rates from large academic hospitals (2,6). The pooled mean rate of ventilator-related HAP (per 1,000 days ventilated) in intensive care units (ICU) range from 1.3 (medical pediatric ICU) to 5.5 (burn ICU) (7). The frequency of HAP is reportedly higher in selected patient populations, ranging from 0.66 to 1.47 in the elderly (8,9), 1.7 to 7.2 among newborn ICU patients (6,10), and 2.0 to 21.6 among adult ICU residents (11, 12, 13 and 14,15,16). A point prevalence study of ICUs in 17 Western European countries revealed that 20.6% of all patients had an ICU-acquired infection; pneumonia accounted for 46.9% and lower respiratory tract infections other than pneumonia accounted for 17.8% of all ICU-acquired infections (17). A more recent point prevalence study conducted in May 2007 included 14,414 patients in 1,265 ICUs from 75 countries revealed that 51% of patients were infected and that among infected patients 64% had a respiratory tract infection (18).
More than 50% of the antibiotics prescribed in ICUs are for the treatment of HAP, and over 90% of HAPs in ICUs are ventilator-associated pneumonias (VAPs) (5). HAP increases hospital stay by an average of 7 to 9 days per patient and has been reported to produce an excess cost of more than $40,000 per patient (5). The crude mortality rate for HAP may be as high as 30% to 70%, and the HAP-related attributable mortality is estimated to range from 33% to 50% (5,19). It is often difficult to define the exact incidence of HAP and VAP, because there are frequently overlaps with other lower respiratory tract infections, such as tracheobronchitis, especially in mechanically ventilated patients (5).
Multiple risk factors for HAP have been identified by univariate analysis: abdominal or thoracic surgery (14,20,21), advanced age (14,21), altered mental status (8,9,15,21), prior episodes of large-volume aspiration (8,9,12,20,22), H2 blocker therapy (9,22,23), steroid therapy (22), ICU residence (9,20), nasogastric intubation (8,9,14,20), previous antibiotic use (9,20,24,25), rapidly or ultimately fatal disease (12,14), trauma (15,16), neurologic disease (16), underlying chronic lung disease (20), and intubation with mechanical ventilation (9,12,15,20). The risk factors for ICU-acquired pneumonia have been reviewed (26,27). Most (9,12,20,22,28) but not all (14) multivariable analyses have shown that mechanical ventilation is a major risk factor for HAP, with odds ratios ranging from 1.3 to 12.1 (for positive studies). The exact incidence of pneumonia is considered 6- to 20-fold greater than in nonventilated patients (5). Few investigators have included variables related to type of respiratory care procedures in their multivariable risk factor analyses. Joshi et al. (14) found a 2.95-fold increased risk of HAP associated with recent bronchoscopy in ICU patients. Reintubations are additional risk factors for VAP (5).
PATHOGENESIS OF HEALTHCARE-ASSOCIATED PNEUMONIA AND ROLE OF RESPIRATORY CARE EQUIPMENT
HAP may occur by four major routes: (a) aspiration of oropharyngeal flora; (b) inhalation of infectious aerosols; (c) contiguous spread adjacent site; and (d) hematogenous spread from a distant focus of infection. Colonization of the oropharynx and gastrointestinal tract by pathogenic grampositive and gram-negative bacilli, followed by aspiration in the setting of impaired host defenses, is the major cause of HAP. Exposure to invasive respiratory devices and equipment is important in the pathogenesis of HAP and VAP (5).
Contaminated respiratory care equipment may lead to HAP by two routes. First, respiratory care equipment may serve as a reservoir for microorganisms, especially
gram-negative bacilli. Fluid-containing devices such as nebulizers and humidifiers may become heavily contaminated by bacteria capable of multiplying in water. Pathogens may then be spread to the patient by hospital personnel or by aerosolization into room air. Second, contaminated equipment may lead to direct airway inoculation of microorganisms if it is directly linked to a ventilatory system or if contaminated medications are instilled by aerosolization. The role of inhalation and respiratory care equipment in HAP has been reviewed several times in the era of medical/surgical intensive care (15,26,27,29,32, 33, 34 and 35,36,37, 38, 39, 40, 41, 42, 43 and 44,45, 46 and 47). Multiple reports exist in the scientific literature regarding outbreaks associated with the use of equipment introduced into the respiratory system, ranging from tongue depressors to bronchoscopes (48).
gram-negative bacilli. Fluid-containing devices such as nebulizers and humidifiers may become heavily contaminated by bacteria capable of multiplying in water. Pathogens may then be spread to the patient by hospital personnel or by aerosolization into room air. Second, contaminated equipment may lead to direct airway inoculation of microorganisms if it is directly linked to a ventilatory system or if contaminated medications are instilled by aerosolization. The role of inhalation and respiratory care equipment in HAP has been reviewed several times in the era of medical/surgical intensive care (15,26,27,29,32, 33, 34 and 35,36,37, 38, 39, 40, 41, 42, 43 and 44,45, 46 and 47). Multiple reports exist in the scientific literature regarding outbreaks associated with the use of equipment introduced into the respiratory system, ranging from tongue depressors to bronchoscopes (48).
Fluid-containing respiratory devices are the major environment-associated reservoirs for HAP; however, most or all phases of respiratory support have been linked to healthcare-associated respiratory infections or suggested as potential environmental reservoirs. These include mechanical ventilation bags (MVBs), ventilators, aerosolized medications, bronchoscopy, suction catheters, suction regulators devices, and respiratory support personnel. Evidence suggests that alterations in infection control practices during the 1960s decreased the number of cases of HAP from environmental sources (49).
INFECTIONS ASSOCIATED WITH INTUBATION AND MECHANICAL VENTILATION
Pathophysiology of Infection
Intubation for respiratory support increases the patient’s risk of HAP. Nasotracheal or orotracheal intubation predisposes patients to bacterial colonization and HAP by the following pathophysiologic alterations (5,50, 51 and 52): (a) it causes sinusitis and trauma to the nasopharynx (nasotracheal tube); (b) it impairs swallowing of secretions; (c) it acts as a reservoir for bacterial proliferation; (d) it increases bacterial adherence and colonization of airways; (e) it requires the presence of a foreign body that traumatizes the oropharyngeal epithelium; (f) it causes ischemia secondary to cuff pressure; (g) it impairs ciliary clearance and cough; (h) it can cause leakage of secretions around the cuff; and (i) it requires suctioning to remove secretions. Mechanical ventilation also exposes the patient to fluid-filled devices, such as in-line nebulizers and humidifiers, which are used to provide humidification or medications.
Incidence of Respiratory Infections
Multiple studies have demonstrated that mechanical ventilation is a major predisposing factor for HAP (5,22,26,28,53, 54, 55, 56, 57, 58, 59, 60 and 61). Direct comparisons of the various studies require caution because of important differences in study design, including patient population, period of study, criteria for entry into the study, and diagnostic criteria for pneumonia. However, the following generalizations can be made: between 15% and 40% of patients who undergo mechanical ventilation for more than 48 hours develop HAP, and the case-fatality rate is exceedingly high.
INFECTIONS ASSOCIATED WITH COMPONENTS OF MECHANICAL VENTILATION
Ventilators
The internal machinery of mechanical ventilators is not considered an important source of bacterial contamination of inhaled air (62). In the 1960s, the use of a high-efficiency bacterial filter interposed between the machinery and the main breathing circuit was advocated to eliminate contaminants from the driving gas and to prevent retrograde contamination of the machine by patients (63). The filters were shown, however, to alter the function of the ventilators by impeding high gas flows. Later studies have not shown that a filter placed between the inspiratory phase circuit and the patient prevents infection (64,65).
Placement of a filter or condensate trap on the expiratory limb of the mechanical-ventilator circuit may help prevent cross-contamination of the ventilated patient’s immediate environment (66), but the importance of such filters in preventing HAP has not been demonstrated (29,67).
Periodic sterilization or high-level disinfection of the internal ventilator machinery is unnecessary; however, ventilator circuits should be sterilized or subjected to high-level disinfection between patient uses (68). Failure to properly clean and sterilize ventilator circuits between patients has led to outbreaks with Pseudomonas aeruginosa (69), Bacillus cereus (70), and Acinetobacter species (71). The failure to properly disinfect ventilator temperature probes between patients has led to outbreaks of Burkholderia cepacia pneumonia (72).
Nebulizer Equipment
Nebulizers have been a significant source of HAP. Nebulizers with large-volume (>500 mL) reservoirs, including those used in intermittent positive-pressure breathing (IPPB) machines and ultrasonic or spinning-disk roomair “humidifiers,” pose the greatest risk of pneumonia to patients, probably because of the total amount of aerosol they generate (73). Other types of nebulizers include smallvolume nebulizers for administration of medications, most commonly bronchodilators. Such small-volume nebulizers may be placed in the inspiratory circuit of mechanical ventilators or handheld.
Nebulizers used in association with mechanical ventilators may be inserted into the inspiratory phase tubing of the mechanical ventilator circuit for the administration of medications or used to provide humidification of air. In-line medication nebulizers may become contaminated by reflux of tubing condensate (74) or use of contaminated solutions (75). Contaminated nebulizers may then lead to HAP via direct instillation of pathogenic bacteria into the lung (76,77). Botman and de Krieger (78) demonstrated that small-volume nebulizers frequently become colonized with pathogenic bacteria, and that nebulizers are associated with an increased risk of respiratory colonization of patients. The risk of pneumonia is related to the production of contaminated bacterial droplets <4 µm in diameter (50). Particles larger than 10 µm are trapped in the nasopharynx or trachea, whereas particles smaller
than 4 µm may be delivered into the patient’s terminal bronchioles and alveoli. Craven et al. (50) emphasized that the risk of pneumonia is related to the size and number of the aerosol particles, the concentration of pathogenic bacteria, and whether aerosol particles are delivered directly into the endotracheal tube or into the oropharynx. The temperature of the reservoir fluid is also critically important, because most healthcare-associated pathogens cannot survive for long periods in distilled water or saline at temperatures above 50°C. Decreases in the frequency of nebulizer contamination were shown to relate to decreases in the occurrence of necrotizing pneumonia (49).
than 4 µm may be delivered into the patient’s terminal bronchioles and alveoli. Craven et al. (50) emphasized that the risk of pneumonia is related to the size and number of the aerosol particles, the concentration of pathogenic bacteria, and whether aerosol particles are delivered directly into the endotracheal tube or into the oropharynx. The temperature of the reservoir fluid is also critically important, because most healthcare-associated pathogens cannot survive for long periods in distilled water or saline at temperatures above 50°C. Decreases in the frequency of nebulizer contamination were shown to relate to decreases in the occurrence of necrotizing pneumonia (49).
In addition to the previously mentioned mechanisms of contamination, in-line, fine-particle nebulizers used to humidify air mixed with oxygen from a wall oxygen outlet may become contaminated when ambient air contains bacteria (79).
Contaminated nebulizers have been responsible for several outbreaks. Four cases of Legionella pneumophila pneumonia resulted when contaminated tap water was used in jet nebulizers to humidify oxygen administered by face mask (80). Failure to disinfect nebulizers between patients led to an outbreak of Serratia marcescens pneumonia (75). Use of contaminated ultrasonic nebulizers in IPPB machines has led to infections with S. marcescens (81,82) and P. aeruginosa (83). Use of contaminated inhaled budesonide with sulbutamol through nebulizers led to seven cases of B. cepacia bacteremia in a pediatric ICU (77). In 2005, six pediatric cases of Ralstonia spp. infections were related to the use of a particular brand of oxygen delivery device (84).
Mechanical Ventilation with Humidification
Humidification of inspiratory air is an important aspect of ventilator management. Humidification may be achieved by bubble-through humidifiers, which produce minimal aerosols, or wick humidifiers, which produce no aerosols (85). Bubble-through humidifiers are usually heated to temperatures that reduce or eliminate bacterial pathogens (86). For these reasons, current humidification practices are not believed to pose a significant risk of pneumonia to ventilated patients (73). However, one study that purposely used contaminated water found that although colony counts in bubble-through humidifiers decreased with time, viable microorganisms remained throughout the study (86). Further, when bubble-through humidifiers were heated, both condensate and effluent gas rapidly became contaminated. Additional studies are required of actual ventilators in use to assess the importance of humidification as a risk factor for HAP (87). It is currently recommended that sterile water be used to fill these humidifiers (29) because tap or distilled water may harbor relatively heat-resistant pathogens (80,85,88, 89, 90 and 91).
A potential risk factor for pneumonia in patients using mechanical ventilation with humidification is the condensate that forms in the inspiratory-phase tubing of the ventilator circuit. This condensate forms as a result of the difference in the temperatures of the inspiratory-phase gas and ambient air. Condensate formation is increased if the tubing is unheated compared to the use of heated bubble-through humidifiers. Both the ventilator tubing and condensate rapidly become colonized by gram-negative and gram-positive bacteria during use. The colonizing pathogens originate from the patient, and thus, the highest levels of bacteria are closest to the endotracheal tube, with lower levels near the humidifier reservoir. Craven et al. (88) demonstrated that 33% of inspiratory circuits became colonized by oropharyngeal flora from the patient within 2 hours of use, and 80% were colonized within 24 hours of use. They hypothesized that spillage of this contaminated fluid into the patient’s respiratory tract, as might occur during procedures such as patient suctioning or transportation for clinical studies, might lead to HAP. Contaminated condensate can also serve as a reservoir for respiratory pathogens, which can be transmitted person to person via the hands of medical personnel if staff members fail to wash their hands following ventilator manipulation.
The frequency of ventilator tubing changes and its relationship to the incidence of HAP has been investigated by several research groups (Table 66-1). In a landmark study, Craven et al. (99) reported that ventilator tubing could be safely changed every 48 hours as opposed to the then-recommended 24-hour changes. After many years and multiple investigations (Table 66-1), current data indicate that breathing circuits, including all its variable components, should not be changed on a routine basis, and individual components should be replaced only when they malfunction or become visibly contaminated (68,100).
Filling the in-line humidifier with contaminated water has led to an outbreak of Pseudomonas fluorescens infections (101). The reuse of inadequately disinfected ventilator circuits has led to outbreaks with Acinetobacter species (71,102) and Pseudomonas species (103). Reusable ventilator tubing should be thoroughly cleaned and dried after patient use and then sterilized with ethylene oxide gas, subjected to high-level disinfection with a Food and Drug Administration (FDA)-cleared chemical sterilant, or pasteurized (see Chapters 80 and 81). Only sterile water should be used in humidifiers and nebulizers.
Condensate formation can be eliminated by the use of a heat-moisture exchanger (HME) or a hygroscopic condenser humidifier (also known as an “artificial nose”) (104,105). The HME eliminates the need for a humidifier by recycling heat and moisture exhaled by the patient. Because a humidifier is not used, no condensate forms in the inspiratory tubing of the ventilator circuit. Thus, bacterial colonization of the tubing is avoided. Some authorities still advocate to routinely change the HME every 5 to 7 days or as clinically indicated (100). Potential problems with HMEs include increased dead space and resistance to breathing, and leakage around the endotracheal tube with drying of sputum and blockage of the tracheobronchial tree (106). Several investigators have reported on the use of an HME (107, 108, 109, 110, 111, 112, 113, 114, 115, 116, 117 and 118). Prospective studies demonstrate that changing HMEs every 48 to 72 hours rather than every 24 hours did not affect their efficacy or the incidence of HAP (115,119, 120 and 121). In addition, randomized studies found no difference in the infection rates of patients assigned to a hydrophobic HME or a hygroscopic HME (113,118,119,122,123). Multiple randomized trials have compared the rates of VAP in patients in whom an in-line HME was used compared to patients managed with a conventional heated-wire humidifier
(109,112, 113 and 114,116,117,124). The rates of pneumonia were lower with use of the HME (range of relative risks (RRs), 0.35-0.85); one study reached statistical significance (117). Use of the HME was speculated to be cost-effective and reduces the rate of late-onset, ventilator-related HAP (117,125), but recent guidelines state that despite the fact that HME reduces colonization, the role of HME in VAP prevention is not clear and remains questionable (5,100,126).
(109,112, 113 and 114,116,117,124). The rates of pneumonia were lower with use of the HME (range of relative risks (RRs), 0.35-0.85); one study reached statistical significance (117). Use of the HME was speculated to be cost-effective and reduces the rate of late-onset, ventilator-related HAP (117,125), but recent guidelines state that despite the fact that HME reduces colonization, the role of HME in VAP prevention is not clear and remains questionable (5,100,126).
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Manual Ventilation Bags
Manual ventilation bags are used for urgent ventilation, during routine suctioning of the intubated patient, during transport of the intubated patient, and to ventilate patients during chest physiotherapy. The exterior surface and connecting port of manual ventilation bags are routinely contaminated during use. Secretions left in the bag may be aerosolized and/or sprayed into the lower respiratory tract of patients. Further, the exterior surface may serve as a reservoir for pathogens transmitted person to person on the hands of healthcare personnel. Contaminated manual ventilation bags have been linked to epidemics of HAP and VAP related to specific microorganisms (102,127, 128 and 129). Thompson et al. (130) demonstrated that, in patients with gram-negative bacteria in their sputum, 71% of the manual ventilation bag valves and 29% of the air samples taken from the exhalation valve assemblies were culture positive for the same microorganisms. Weber et al. (131) cultured the interior and exterior surfaces of manual ventilation bags used on 14 ICU patients whose respiratory tracts were colonized or infected. Overall, 51 simultaneous cultures of manual ventilation bag components resulted in the following findings: (a) the manual ventilation bag exterior surface was culture positive 100% of the time; (b) the manual ventilation bag exhalation port was culture positive 96% of the time; and (c) the manual ventilation bag interior surfaces were culture positive only 12% of the time. In three instances (6%), the manual ventilation bag port became colonized with a pathogen prior to its appearance in the patient’s respiratory tract, suggesting that the manual ventilation bag was the source for the colonizing pathogen.
Contaminated manual ventilation bags may serve as a source for healthcare-associated infection by colonizing the hands of medical personnel who then may cross-transmit such pathogens directly to other patients or to respiratory or other medical equipment, and by introducing pathogens into patients. The following guidelines have been suggested
for the prevention of healthcare-associated respiratory tract infections associated with manual ventilation bags (131). First, all medical personnel should wash their hands before and immediately after any contact with patients or potentially contaminated equipment such as manual ventilation bags. Second, manual ventilation bags should be sterilized or subjected to high-level disinfection between patients (68). Third, the manual ventilation bag should be cleaned of visible secretions daily and then disinfected with alcohol (68). Both the exterior surface and the manual ventilation bag exhalation valve should be disinfected. The interior surface does not need to be disinfected during routine use. When reprocessed in an appropriate area of the ICU or in central processing, if tenacious sputum cannot be removed from the exhalation port, the port should be disassembled, cleaned, and sterilized or subjected to high-level disinfection.
for the prevention of healthcare-associated respiratory tract infections associated with manual ventilation bags (131). First, all medical personnel should wash their hands before and immediately after any contact with patients or potentially contaminated equipment such as manual ventilation bags. Second, manual ventilation bags should be sterilized or subjected to high-level disinfection between patients (68). Third, the manual ventilation bag should be cleaned of visible secretions daily and then disinfected with alcohol (68). Both the exterior surface and the manual ventilation bag exhalation valve should be disinfected. The interior surface does not need to be disinfected during routine use. When reprocessed in an appropriate area of the ICU or in central processing, if tenacious sputum cannot be removed from the exhalation port, the port should be disassembled, cleaned, and sterilized or subjected to high-level disinfection.
Prevention of Healthcare-Associated Pneumonia
Several authors have summarized measures that may reduce the incidence of VAP (5,29,30,31,45,73,100,132, 133, 134 and 135,136,137, 138 and 139,140,141, 142, 143, 144, 145, 146, 147, 148, 149 and 150,151,152). These measures include (a) preference to the orotracheal (as opposed to nasotracheal) route when intubation is necessary; (b) use of aseptic technique for respiratory tract manipulation; (c) use of mouth washes with oral antiseptics for intubated patients (e.g., chlorhexidine); (d) proper disinfection and maintenance of respiratory equipment; (e) use of a new ventilator circuit each time a new patient is placed on a ventilator, but no routine change of circuits for a single patient unless visibly soiled or mechanically malfunctioning; (f) new HME for each patient, and change of HME as clinically indicated (some still recommend routine changes every 5 to 7 days (100)); (g) hand hygiene before and after contact with mucous membranes or contaminated equipment, whether or not gloves are worn; (h) elevation of the head of the bed to 45 degrees (when it is not possible to elevate this high, then attempts should be made to raise the head of the bed as much as possible (100)); (i) continuous subglottic suctioning, particularly in patients expected to be mechanically ventilated for >72 hours (100); and (j) noninvasive ventilation to avoid risks associated with endotracheal intubation and mechanical ventilation (153). Additional measures include (a) identification and elimination of environmental reservoirs for pathogens; (b) use of barrier precautions for colonized and infected patients; (c) extubation and removal of nasogastric tubes as soon as clinically possible; (d) avoidance of oversedation and paralytics; (e) use of proper endotracheal suctioning techniques; (f) maintaining adequate endotracheal cuff pressures; and (g) control of antibiotic use. Table 66-2 summarizes the current and the past CDC guidelines relevant to this chapter for the prevention of HAP.
More recent guidelines, from various professional societies, (100,151,152) address issues and data related to VAP prevention that were not fully covered in the 2004 CDC guidelines (29). These are as follows: (a) subglottic drainage of secretions. Although this was mentioned in CDC’s 2004 guidelines as being helpful in preventing VAP (154), more recent guidelines have more strongly supported the use of subglottic suctioning (5,100,151,152). (b) Silver-coated endotracheal tubes. In a large prospective study, involving 54 institutions and 2003 patients, the use of silver-coated endotracheal tubes reduced the incidence of VAP by 36%, though no differences in mortality, length of ICU stay, and duration of mechanical ventilation were noted (140). (c) Polyurethane cuffed endotracheal tubes. So far, this device, which is designed to prevent leakage and aspiration of subglottic secretions around the endotracheal cuff, has only been tested in a pilot study design and only in postoperative cardiac surgery patients (155). (d) Selective oral decontamination (SOD) and selective digestive decontamination (SDD). One randomized trial (156) demonstrated a favorable impact of SOD and SDD on mortality of mechanically ventilated patients; and one meta-analysis (157) reported a reduction in VAP rates associated with SOD and SDD, but reported conflicting results regarding reduction in overall mortality. Emergence of antimicrobial resistance is a concern pertaining to this practice. (e) Oral care with chlorhexidine. Most guidelines recommend routine care with antiseptics (most commonly chlorhexidine), despite publication of few negative trials (158, 159 and 160). (f) Daily assessment of readiness to wean and following weaning protocols reduces VAP prevalence and improves patient outcomes (151,161). (g) Stress ulcer prophylaxis. The bulk of recent data (although mostly retrospective) suggest that avoiding use of antacids, when possible, might reduce risk for VAP (151,162,163). (h) Implementing VAP prevention bundles are cost-effective and are associated with reduced incidence of VAP (133,151,164, 165 and 166).
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