Impact of Subglottic Suctioning on the Incidence of Pneumonia After Cardiac Surgery: A Retrospective Observational Study Jordan K.C. Hudson, MD, MPH, FRCPC,* Bernard J. McDonald, MD, PHD, FRCPC,† John C. MacDonald, MD, FRCPC,† Marc A. Ruel, MD, MPH, FRCSC,‡ and Christopher C.C. Hudson, MD, MPH, FRCPC† Objective: Continuous aspiration of subglottic secretions (CASS) has been found to decrease the incidence of pneumonia in the general intensive care unit (ICU) population, but its benefit in cardiac surgery patients is unclear. The present study aimed to determine whether the routine use of CASS in cardiac surgical patients was associated with decreased pneumonia. Design: A retrospective, single-center observational study. Setting: The study was conducted in a quaternary care cardiac surgery center and university research hospital. Participants: 4,880 patients undergoing cardiac surgery were studied. Interventions: The control group (no CASS) received a standard endotracheal tube and underwent surgery between April 1, 2007 and March 31, 2009. The intervention group (CASS) received a subglottic suctioning endotracheal tube and underwent surgery between June 1, 2009 and May 31, 2011. The primary outcome was the development of pneumonia, and the secondary outcomes were 30-day inhospital mortality, ventilation time, need for tracheostomy, ICU length of stay (LOS), and hospital LOS.
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ENTILATOR-ASSOCIATED PNEUMONIA (VAP) is a serious problem in the intensive care unit (ICU), with a cumulative incidence of 10% to 25% and an attributable risk of 5% to 27%.1–4 The risk of pneumonia is higher with prolonged ventilation, increasing 1% to 3% per day of intubation.5,6 The endotracheal tube is an important mode of transmission for pathogens: respiratory secretions pool between the glottis and the endotracheal tube cuff, promoting growth of pathogens and leaking down around the endotracheal tube cuff into the lungs.3 In an attempt to reduce the incidence of pneumonia, many patient safety advocacy groups are now recommending use of endotracheal tubes designed with a suctioning port situated above the tube cuff, which allow for the removal of respiratory secretions pooling in the subglottic space.5,7 Although meta-analyses of studies in the general ICU population demonstrate a net beneficial effect of subglottic suctioning endotracheal tubes, benefits were concentrated in patients undergoing prolonged mechanical ventilation exceeding 72 hours.8,9 Cardiac surgical patients frequently are ventilated for shorter periods of time than patients in the general ICU population. In the cardiac surgical population, current evidence from 2 randomized control trials (RCTs) does not show a significant benefit of subglottic suctioning (n = 343 and n = 714).10,11 In April 2009, the University of Ottawa Heart Institute (UOHI), an adult quaternary care center specializing in cardiovascular medicine, mandated that all cardiac surgical patients receive an endotracheal tube that allows continuous aspiration of subglottic secretions (CASS) instead of a standard endotracheal tube. The present study tested the hypothesis that CASS is associated with decreased incidence of pneumonia in the postoperative cardiac surgical population.
Measurements and Main Results: The unadjusted incidence of pneumonia was 1.9% in the CASS group and 5.6% in the control group (p o 0.0001). The CASS group also had lower 30-day in-hospital mortality (2.1% v 3.3%; p ¼ 0.007), median ventilation time (8.42 v 7.3 hours; p o 0.0001), and shorter median ICU LOS (1.77 v 1.17 days; p o 0.0004) compared with the control group. Tracheostomy rates and median hospital LOS did not differ between groups. After adjusting using multivariable modeling, CASS remained an independent risk predictor for pneumonia (odds ratio [OR] 0.342, 95% confidence interval [CI] 0.239-0.490) and ICU LOS (OR 0.817, 95% CI 0.7180.931). Conclusions: The universal implementation of CASS in a quaternary care cardiac surgical population was associated with a decreased incidence of pneumonia. & 2014 Elsevier Inc. All rights reserved. KEY WORDS: pneumonia, ventilator-associated pneumonia, subglottic suctioning, cardiac surgery, intensive care, VAP prevention bundle
MATERIALS AND METHODS The study was approved by the Ottawa Hospital Human Research Ethics Board, with a waiver of informed consent, and conducted in accordance with the ethical standards described in the 1964 Declaration of Helsinki and its amendments. Written consent from individual study participants was not required because the study represented a secondary use of nonidentifiable data (TCPS Article 5.5).12 This was a single-center, observational study of all patients undergoing major cardiac surgical procedures at the UOHI from April 1, 2007 to May 31, 2011. Patients undergoing minor procedures without endotracheal intubation, such as pacemaker implantation, were excluded. The UOHI provides all-adult cardiac surgical and postoperative care to a population of approximately 2 million persons. The UOHI perioperative database is a comprehensive, prospectively collected database, documenting more than 400 variables for every surgical patient during the preoperative, intraoperative, and postoperative periods. All information in the database is collected by a dedicated research team and is validated for completeness and
From the *Department of Anesthesiology, University of Ottawa, Ottawa, Ontario, Canada; †Division of Cardiac Anesthesiology and Critical Care Medicine, University of Ottawa Heart Institute, Ottawa, Ontario, Canada; and ‡Division of Cardiac Surgery, University of Ottawa Heart Institute, Ottawa, Ontario, Canada. Supported by the research funds of the Division of Cardiac Anesthesiology and Critical Care Medicine of the University of Ottawa Heart Institute, Ottawa, Ontario, Canada. Address reprint requests to Christopher C. C. Hudson, MD, MPH, FRCPC, Division of Cardiac Anesthesiology and Critical Care Medicine, University of Ottawa Heart Institute, 40 Ruskin Street H2410, Ottawa, Ontario, Canada, K1Y 4W7. E-mail: [email protected] © 2014 Elsevier Inc. All rights reserved. 1053-0770/2601-0001$36.00/0 http://dx.doi.org/10.1053/j.jvca.2014.04.026
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accuracy. All captured variables were predefined in accordance with commonly used expert consensus definitions and kept up to date. Where possible, preoperative variable definitions or specific postoperative cardiac surgical outcomes, such as “re-opening” are in keeping with definitions used by the CARE score (Cardiac Anesthesia Risk Evaluation score)13 and/or the Society of Thoracic Surgeons database.14 CASS refers to the placement and use of an endotracheal tube that permits the aspiration of secretions above the endotracheal tube cuff. The control group (no CASS) received a standard endotracheal tube and underwent surgery between April 1, 2007 and March 31, 2009. The intervention group (CASS) received a subglottic suctioning endotracheal tube and underwent surgery between June 1, 2009 and May 31, 2011. To allow for adequate time for implementation of the new standard of care, patients seen between April 1 and May 31, 2009 were not included. All patients in this study who received subglottic suctioning had continuous aspiration of secretions via wall suction in accordance with manufacturer’s guidelines, with regular reassessments by respiratory therapists to ensure adequate drainage. All patients in the study also received standard-of-care treatment for VAP prevention, as outlined in the Safer Healthcare Now bundle.15,16 Safer Healthcare Now is a program of the Canadian Patient Safety Institute, similar to the 5 Million Lives Campaign in the United States. The VAP bundle was implemented in June 2005 and includes the use of semirecumbent positioning in all patients who can tolerate head elevation, daily evaluation of readiness for extubation, oral care and decontamination with chlorhexidine, and initiation of safe enteral nutrition within 24 to 48 hours of ICU admission. The addition of CASS to the bundle was made in 2007. The only change in the standard of ventilatory care during the study period was the implementation of CASS. Patients were extubated as soon as the following criteria were met: Normothermia (4361C), neurologically intact and awake, hemodynamic stability, and no physical signs of respiratory distress (per UOHI standard operating procedures for mechanically ventilated patients). The primary outcome of this study was pneumonia, defined as the new onset of pneumonia in a patient who underwent mechanical ventilation. The clinical criteria for the diagnosis of pneumonia are summarized in Table 1. Secondary outcomes for this study included 30-day in-hospital mortality, ventilation time, need for tracheostomy, ICU length of stay (LOS), and hospital LOS. Patients were grouped into three surgical categories: Patients undergoing coronary artery bypass graft (CABG) surgery alone, Table 1. Criteria for the Diagnosis of Pneumonia in Ventilated Patients A. Rales or dullness to percussion on physical examination of chest
and any of the following: 1. new onset of purulent sputum or change in the character of sputum 2. organism isolated from blood culture 3. isolation of pathogen from specimen obtained by transtracheal aspirate, bronchial brushing, or biopsy or B. Chest radiographic examination shows new or progressive
infiltrate, consolidation, cavitation, or pleural effusion and any of the following: 1. one of the additional criteria noted above 2. isolation of virus or detection of viral antigen in respiratory secretion 3. diagnostic single antibody titer (IgM) or fourfold increase in paired serum samples (IgG) for pathogen 4. histopathologic evidence of pneumonia
Table 2. Baseline Demographic, Preoperative, and Intraoperative Clinical Characteristics in Control and CASS Groups
Variable
Control Group
CASS Group
(n ¼ 2,430)
(n ¼ 2,450)
p Value
Age (years) 65.6 ⫾ 11.9 65.0 ⫾ 11.9 NS Height (cm) 170.0 ⫾ 9.85 170.3 ⫾ 9.68 NS Weight (kg) 81.6 ⫾ 17.7 81.6 ⫾ 17.8 NS Surgical category* CABG, n (%) 1293 (53.2%) 1132 (46.2%) o0.0001 Valve, n (%) 396 (16.3%) 470 (19.1%) Complex, n (%) 741 (30.5%) 848 (34.6%) Operative priority† Elective, n (%) 1581 (65.1%) 1560 (63.7%) NS Urgent, n (%) 670 (27.6%) 709 (28.9%) Emergency, n (%) 179 (7.4%) 181 (7.4%) Redo surgery, n (%) 291 (12.0%) 280 (11.4%) NS CARE score, n (%) 1 150 (6.2%) 185 (7.6%) NS 2 967 (39.8%) 914 (37.3%) 3 889 (36.6%) 950 (38.8%) 4 289 (11.9%) 278 (11.4%) 5 135 (5.6%) 123 (5.0%) NYHA angina class, n (%) 0 914 (37.6%) 908 (37.2%) NS 1 137 (5.6%) 139 (5.7%) 2 379 (15.6%) 364 (14.9%) 3 487 (20.0%) 489 (20.0%) 4 513 (21.1%) 542 (22.2%) Previous MI, n (%) 986 (40.6%) 912 (37.2%) 0.0163 NYHA CHF class, n (%) 0 1083 (44.6%) 1092 (44.6%) NS 1 190 (7.8%) 189 (3.9%) 2 444 (18.3%) 475 (19.4%) 3 565 (22.7%) 555 (22.7%) 4 148 (6.1%) 139 (5.7%) Chronic obstructive 326 (13.4%) 295 (12.0%) NS pulmonary disease, n (%) Chronic restrictive 45 (1.8%) 37 (1.51%) NS pulmonary disease, n (%) Other respiratory 83 (3.4%) 65 (2.7%) NS comorbidities, n (%) Previous CVA, n (%) 249 (10.3%) 266 (10.9%) NS Preoperative shock, n (%) 164 (6.8%) 187 (7.6%) NS Cardiopulmonary bypass 104.6 ⫾ 50.7 108.9 ⫾ 63.5 0.0088 time (minutes) Abbreviations: CABG, coronary artery bypass grafting; CARE, cardiac anesthesia risk evaluation; CASS, continuous aspiration of subglottic secretions; CHF, congestive heart failure; CVA, cerebral vascular accident; MI, myocardial infarction; NS, nonsignificant; NYHA, New York Heart Association. *CABG surgery consisted of coronary artery bypass grafting alone; valve surgery consisted of valve repair or replacement alone; complex surgery included CABG with 1 or more valve interventions, aortic surgery, cardiac transplant, left ventricular assist device insertion, pulmonary thromboendarterectomy, or extracorporeal membrane oxygenation. †Elective indicated non-urgent cardiac surgery; urgent indicated surgery within 24 hours of diagnosis; emergency indicated surgery as soon as an operating room is available.
patients undergoing valve repair or replacement alone, and all other surgeries (including combined CABG and valve surgery, pulmonary thromboendarterectomy, cardiac transplant, and ascending aortic surgery). Operative priority was defined as elective, urgent (patients
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requiring surgery within 24 hours), and emergency (patients requiring immediate surgery). Assuming a baseline pneumonia rate of 6% in the surgical population, it was estimated that the sample size would have statistical power of 80% to detect an absolute decrease in pneumonia of 1%. Continuous, normally distributed variables were analyzed using twotailed t-tests and are described as mean ⫾ standard deviation, and continuous variables that were not normally distributed were analyzed using Wilcoxon rank sum tests and are described as median ⫾ interquartile range. Categoric variables were analyzed using χ2 tests and are presented as counts (proportions). Potential confounders were identified a priori based on a structured PubMed search using the MESH terms “cardiac surgical procedures,” “coronary artery bypass,” “cardiopulmonary bypass,” “pneumonia,” “ventilator-associated pneumonia,” “prolonged ventilation,” “risk factors,” and “epidemiologic methods.”1,6,9–11,16 For regression analyses, intraoperative and postoperative risk factors were included at baseline if identified through this search strategy in at least two publications from 1995 to 2010. There were no identified risk factors from this literature search that were not available within the institutional database. Univariate analysis was performed for each of these variables with respect to the primary outcome. Multivariable logistic regression models were constructed to adjust for potential confounding variables. All variables meeting a threshold of p o 0.10 on the univariate analysis were selected for evaluation in the multivariable model. The multivariable model was constructed using a stepwise selection algorithm. For adjusted continuous secondary outcomes, clinically significant cutoffs were chosen for ventilation time (r24 hours v 424 hours) and ICU LOS (r2 days v 42 days) to create binary outcome measures. No imputations were performed for missing data, and the sample size was allowed to float with the analysis. All analyses were conducted in SAS v9.2 (SAS Institute, Cary, NC) and GraphPad 5.0 (GraphPad Software Inc, La Jolla, CA). RESULTS
A total of 4,880 patients met the inclusion criteria for this study. Of these, 2,430 patients underwent a major cardiac surgical procedure with a standard endotracheal tube (April 1, 2007 to March 31, 2009), and 2,450 patients underwent a major cardiac surgical procedure with CASS (June 1, 2009 to May 31, 2011). Baseline demographic, preoperative, and intraoperative characteristics are summarized in Table 2. The control and CASS groups differed with respect to type of Table 3. Unadjusted Primary and Secondary Outcomes in Control and CASS Groups Control Group Outcome
Pneumonia 30-day Mortality Tracheostomy Ventilation time, median hours (IQR) ICU length of stay, median days (IQR) Hospital length of stay, median days (IQR)
(n ¼ 2430)
136 81 57 8.42
(5.6%) (3.3%) (2.3%) (5.5-17.3)
CASS Group (n ¼ 2450)
46 51 56 7.3
(1.9%) (2.1%) (2.3%) (4.8-15.0)
1.77 (0.92-3.54)
1.17 (0.92-3.00)
10.0 (7.0-17.0)
10.0 (7.0-16.0)
p Value
o0.0001 0.007 NS o0.0001 0.0004
NS
Abbreviations: CASS, continuous aspiration of subglottic secretions; IQR, interquartile range; NS, nonsignificant.
Table 4. Multivariable Logistic Regression Model of Pneumonia and Secondary Outcomes in CASS Versus Control Groups Outcome
Odds Ratio (95% CI)
Pneumonia 30-day Mortality Ventilation time 424 h ICU length of stay 42 days
0.342 0.700 0.841 0.817
(0.239-0.490) (0.476-1.027) (0.694-1.020) (0.718-0.931)
p Value
o0.0001 0.0685 0.0787 0.0024
CASS, continuous aspiration of subglottic secretions; CI, confidence interval.
surgery, history of previous myocardial infarction, and cardiopulmonary bypass time. The overall incidence of pneumonia in the study population was 3.7%. The unadjusted incidence of pneumonia was 1.9% in the CASS group and 5.6% in the control group (p o 0.0001). The CASS group also had lower 30-day inhospital mortality (2.1% v 3.3%; p ¼ 0.007), median ventilation time (7.3 v 8.4 hours; p o 0.0001), and shorter median ICU LOS (1.17 v 1.77 days; p o 0.0004) compared with the control group (Table 3). Tracheostomy rates and median hospital LOS did not differ between groups. After correcting for the variables that were significant between the 2 groups using multivariable modeling, CASS remained an independent risk predictor for pneumonia (odds ratio [OR] 0.34, 95% confidence interval [CI] 0.24-0.49) and ICU LOS (OR 0.82, 95% CI 0.72-0.93) (Table 4). However, the association between CASS and decreased mortality and ventilation time did not remain after adjusting for confounders. DISCUSSION
This retrospective observational study of patients undergoing cardiac surgery found that the use of CASS was associated with a decreased incidence of pneumonia and decreased ICU LOS. An association between CASS and 30day mortality, need for tracheostomy, or hospital LOS was not found. The CASS group had a 66% lower incidence of pneumonia. The findings were consistent with a recent meta-analysis of RCTs in the ICU population, which found VAP rates were approximately halved by the use of CASS.9 Existing studies vary with respect to how subglottic suctioning was performed. Patients in some trials received intermittent suctioning and drainage, while others received continuous aspiration of subglottic secretions. Intermittent drainage is thought to be less effective for VAP prevention.9,17,18 All patients in this study who received subglottic suctioning had continuous aspiration of secretions with regular reassessments by respiratory therapists to ensure effective drainage. The 2 previous RCTs in the cardiac surgical population did not find a significant benefit.10,11 However, both studies found a trend toward lower VAP rates in patients who received CASS (Relative Risk 0.61 and 0.67). The 1999 study pre-dated current VAP prevention recommendations and had a higher baseline incidence of VAP (8.2%). Their power calculation assumed a baseline incidence of 17.5%, thus their sample size was insufficient to detect the expected 7.5% absolute risk reduction.10 The more recent RCT in
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2008 was powered to detect a 38% relative risk reduction from their baseline risk of VAP of 5.3%, thus their finding of a 32% relative risk reduction with CASS was not statistically significant.11 With larger sample sizes, it is possible that these studies would have found benefit from CASS rather than a trend toward benefit. Previous studies of CASS for VAP prevention found benefit mainly in patients ventilated for periods of time longer than 72 hours.8,9 Given that the median ventilation times in both groups were short (8.4 hours and 7.0 hours in the control and intervention groups, respectively), the findings of the present study suggested that the routine use of CASS may be beneficial even in patients with shorter anticipated ventilation times, including patients undergoing cardiac surgery. It should be noted that subglottic suctioning endotracheal tubes are more expensive than standard endotracheal tubes. The purpose of the study was not to conduct a cost-benefit analysis. However, it is useful to note that, given the difference in endotracheal tube prices of $14.68 (adjusted to 2014 US dollars [USD]), the material cost of using CASS in the intervention group was $35,966 USD. The CASS group had 91 fewer pneumonias than would be expected by the control group results, for a cost reduction of $911,729 USD (based on a conservative estimate of $10,019 as the cost of pneumonia in the ICU).19 The present study was limited by the evolving clinical definitions of pneumonia and ventilator-associated pneumonia. To ensure consistency of diagnostic criteria throughout the study, the UOHI database definition of pneumonia (Table 1) was used for patients receiving postoperative mechanical ventilation, which arose from the Centers for Disease Control and Prevention (CDC) definition.20 It would have been ideal to use the current definition of VAP, but the study pre-dated the release of the new definition.4 The present study also had the inherent limitations of a retrospective analysis of a prospectively collected database. Confounding by unaccounted-for variables may have occurred. Although care was provided according to protocols, the groups were not homogenous, and they represented patients from 2 separate time periods. With the exception of CASS, the VAP prevention bundle and respiratory care pathways implemented at the UOHI did not change during the study period. Nonetheless, it is possible that increased awareness of and compliance with VAP prevention guidelines may have influenced care. Many cardiac surgical patients cannot tolerate head-ofbed elevation due to hemodynamic instability, resulting in greater risk of pneumonia. In addition to a higher pneumonia rate, the control group had a longer median ventilation time (by 1.1 hours) and a
Fig 1. Number of intubated patients (by day) among patients with and without continuous aspiration of subglottic secretions (CASS).
longer median ICU LOS (by 0.6 days). It is possible that longer ventilation time is a confounder of the relationship between CASS and pneumonia; patients ventilated for longer periods of time are more likely to develop pneumonia. However, the incremental risk is estimated to be 1% to 3% per extra day of ventilation5,6, thus the 1.1 hour difference should not account for the 3.7% increased incidence of pneumonia in the control group. It is more likely that both ventilation time and ICU LOS are further down the causal pathway; patients who develop pneumonia are more likely to require prolonged ventilation and a longer ICU stay. In this case, pneumonia would be an intermediate variable between CASS and ventilation time. The vast majority of patients in both groups were extubated by the first postoperative day (Fig 1), and the respiratory care pathway, weaning criteria, and ICU discharge criteria did not change during the study period with the exception of CASS. Ventilator-associated pneumonia is a clinically important complication of mechanical ventilation. With heightened awareness of the severity of pneumonia and the implementation of VAP prevention bundles, the overall incidence of pneumonia is decreasing. The findings of the present study suggest that the use of CASS reduces pneumonia incidence in a cardiac surgical population, even though the median postoperative ventilation time was well under 24 hours. We anticipate more widespread use of subglottic suctioning endotracheal tubes in all surgical patients who are at high risk of requiring postoperative ventilation, even for a brief period of time. In conclusion, universal implementation of CASS in a quaternary care cardiac surgical population was associated with a decreased incidence of pneumonia. Further studies are required to confirm our results. However, it may be prudent to consider the routine use of CASS endotracheal tubes in patients who are expected to require short-term postoperative ventilation.
REFERENCES 1. Collard HR, Saint S, Matthay MA: Prevention of ventilatorassociated pneumonia: An evidence-based systematic review. Ann Intern Med 138:494-501, 2003 2. Craven DE: Preventing ventilator-associated pneumonia in adults: Sowing seeds of change. Chest 130:251-260, 2006 3. Craven DE, Steger KA: Epidemiology of nosocomial pneumonia. New perspectives on an old disease. Chest 108(suppl):1S-16S, 1995 4. Hunter JD: Ventilator associated pneumonia. BMJ 344:e3325, 2012
5. Diaz E, Rodriguez AH, Rello J: Ventilator-associated pneumonia: Issues related to the artificial airway. Respir Care 50:900-906; discussion 906-909, 2005 6. Cook DJ, Walter SD, Cook RJ, et al: Incidence of and risk factors for ventilator-associated pneumonia in critically ill patients. Ann Intern Med 129:433-440, 1998 7. Mahul P, Auboyer C, Jospe R, et al: Prevention of nosocomial pneumonia in intubated patients: Respective role of mechanical
IMPACT OF SUBGLOTTIC SUCTIONING ON THE INCIDENCE OF PNEUMONIA AFTER CARDIAC SURGERY
subglottic secretions drainage and stress ulcer prophylaxis. Intensive Care Med 18:20-25, 1992 8. Dezfulian C, Shojania K, Collard HR, et al: Subglottic secretion drainage for preventing ventilator-associated pneumonia: A metaanalysis. Am J Med 118:11-18, 2005 9. Muscedere J, Rewa O, McKechnie K, et al: Subglottic secretion drainage for the prevention of ventilator-associated pneumonia: A systematic review and meta-analysis. Crit Care Med 39:1985-1991, 2011 10. Kollef MH, Skubas NJ, Sundt TM: A randomized clinical trial of continuous aspiration of subglottic secretions in cardiac surgery patients. Chest 116:1339-1346, 1999 11. Bouza E, Pérez MJ, Muñoz P, et al: Continuous aspiration of subglottic secretions in the prevention of ventilator-associated pneumonia in the postoperative period of major heart surgery. Chest 134:938-946, 2008 12. Canadian Institutes of Health Research, Natural Sciences and Engineering Research Council of Canada, and Social Sciences and Humanities Research Council of Canada: Tri-Council Policy Statement: Ethical Conduct for Research Involving Humans, December 2010. Available online at: http://www.pre.ethics.gc.ca/pdf/eng/tcps2/ TCPS_2_FINAL_Web.pdf 13. Dupuis JY, Wang F, Nathan H, et al: The cardiac anesthesia risk evaluation score: A clinically useful predictor of mortality and morbidity after cardiac surgery. Anesthesiology 94:194-204, 2001
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14. Ferguson TB Jr, Dziuban SW Jr, Edwards FH, et al: The STS National Database: Current changes and challenges for the new millennium. Committee to Establish a National Database in Cardiothoracic Surgery, The Society of Thoracic Surgeons. Ann Thorac Surg 69:680-691, 2000 15. Pruitt B, Jacobs M: Best-practice interventions: How can you prevent ventilator-associated pneumonia? Nursing 36:36-41; quiz 41-32, 2006 16. Muscedere JG, Martin CM, Heyland DK: The impact of ventilator-associated pneumonia on the Canadian health care system. J Crit Care 23:5-10, 2008 17. Dragoumanis CK, Vretzakis GI, Papaioannou VE, et al: Investigating the failure to aspirate subglottic secretions with the Evac endotracheal tube. Anesth Analg 105:1083-1085, 2007 18. O'Neal PV, Munro CL, Grap MJ, et al: Subglottic secretion viscosity and evacuation efficiency. Biol Res Nurs 8:202-209, 2007 19. Safdar N, Dezfulian C, Collard HR, et al: Clinical and economic consequences of ventilator-associated pneumonia: A systematic review. CritCare Med 33:2184-2193, 2005 20. Association for Professionals in Infection Control and Epidemiology, Inc: APIC infection control and applied epidemiology: Principles and practice. St. Louis, Mosby, 1996
V
ENTILATOR-ASSOCIATED PNEUMONIA (VAP) is a serious problem in the intensive care unit (ICU), with a cumulative incidence of 10% to 25% and an attributable risk of 5% to 27%.1–4 The risk of pneumonia is higher with prolonged ventilation, increasing 1% to 3% per day of intubation.5,6 The endotracheal tube is an important mode of transmission for pathogens: respiratory secretions pool between the glottis and the endotracheal tube cuff, promoting growth of pathogens and leaking down around the endotracheal tube cuff into the lungs.3 In an attempt to reduce the incidence of pneumonia, many patient safety advocacy groups are now recommending use of endotracheal tubes designed with a suctioning port situated above the tube cuff, which allow for the removal of respiratory secretions pooling in the subglottic space.5,7 Although meta-analyses of studies in the general ICU population demonstrate a net beneficial effect of subglottic suctioning endotracheal tubes, benefits were concentrated in patients undergoing prolonged mechanical ventilation exceeding 72 hours.8,9 Cardiac surgical patients frequently are ventilated for shorter periods of time than patients in the general ICU population. In the cardiac surgical population, current evidence from 2 randomized control trials (RCTs) does not show a significant benefit of subglottic suctioning (n = 343 and n = 714).10,11 In April 2009, the University of Ottawa Heart Institute (UOHI), an adult quaternary care center specializing in cardiovascular medicine, mandated that all cardiac surgical patients receive an endotracheal tube that allows continuous aspiration of subglottic secretions (CASS) instead of a standard endotracheal tube. The present study tested the hypothesis that CASS is associated with decreased incidence of pneumonia in the postoperative cardiac surgical population.
Measurements and Main Results: The unadjusted incidence of pneumonia was 1.9% in the CASS group and 5.6% in the control group (p o 0.0001). The CASS group also had lower 30-day in-hospital mortality (2.1% v 3.3%; p ¼ 0.007), median ventilation time (8.42 v 7.3 hours; p o 0.0001), and shorter median ICU LOS (1.77 v 1.17 days; p o 0.0004) compared with the control group. Tracheostomy rates and median hospital LOS did not differ between groups. After adjusting using multivariable modeling, CASS remained an independent risk predictor for pneumonia (odds ratio [OR] 0.342, 95% confidence interval [CI] 0.239-0.490) and ICU LOS (OR 0.817, 95% CI 0.7180.931). Conclusions: The universal implementation of CASS in a quaternary care cardiac surgical population was associated with a decreased incidence of pneumonia. & 2014 Elsevier Inc. All rights reserved. KEY WORDS: pneumonia, ventilator-associated pneumonia, subglottic suctioning, cardiac surgery, intensive care, VAP prevention bundle
MATERIALS AND METHODS The study was approved by the Ottawa Hospital Human Research Ethics Board, with a waiver of informed consent, and conducted in accordance with the ethical standards described in the 1964 Declaration of Helsinki and its amendments. Written consent from individual study participants was not required because the study represented a secondary use of nonidentifiable data (TCPS Article 5.5).12 This was a single-center, observational study of all patients undergoing major cardiac surgical procedures at the UOHI from April 1, 2007 to May 31, 2011. Patients undergoing minor procedures without endotracheal intubation, such as pacemaker implantation, were excluded. The UOHI provides all-adult cardiac surgical and postoperative care to a population of approximately 2 million persons. The UOHI perioperative database is a comprehensive, prospectively collected database, documenting more than 400 variables for every surgical patient during the preoperative, intraoperative, and postoperative periods. All information in the database is collected by a dedicated research team and is validated for completeness and
From the *Department of Anesthesiology, University of Ottawa, Ottawa, Ontario, Canada; †Division of Cardiac Anesthesiology and Critical Care Medicine, University of Ottawa Heart Institute, Ottawa, Ontario, Canada; and ‡Division of Cardiac Surgery, University of Ottawa Heart Institute, Ottawa, Ontario, Canada. Supported by the research funds of the Division of Cardiac Anesthesiology and Critical Care Medicine of the University of Ottawa Heart Institute, Ottawa, Ontario, Canada. Address reprint requests to Christopher C. C. Hudson, MD, MPH, FRCPC, Division of Cardiac Anesthesiology and Critical Care Medicine, University of Ottawa Heart Institute, 40 Ruskin Street H2410, Ottawa, Ontario, Canada, K1Y 4W7. E-mail: [email protected] © 2014 Elsevier Inc. All rights reserved. 1053-0770/2601-0001$36.00/0 http://dx.doi.org/10.1053/j.jvca.2014.04.026
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accuracy. All captured variables were predefined in accordance with commonly used expert consensus definitions and kept up to date. Where possible, preoperative variable definitions or specific postoperative cardiac surgical outcomes, such as “re-opening” are in keeping with definitions used by the CARE score (Cardiac Anesthesia Risk Evaluation score)13 and/or the Society of Thoracic Surgeons database.14 CASS refers to the placement and use of an endotracheal tube that permits the aspiration of secretions above the endotracheal tube cuff. The control group (no CASS) received a standard endotracheal tube and underwent surgery between April 1, 2007 and March 31, 2009. The intervention group (CASS) received a subglottic suctioning endotracheal tube and underwent surgery between June 1, 2009 and May 31, 2011. To allow for adequate time for implementation of the new standard of care, patients seen between April 1 and May 31, 2009 were not included. All patients in this study who received subglottic suctioning had continuous aspiration of secretions via wall suction in accordance with manufacturer’s guidelines, with regular reassessments by respiratory therapists to ensure adequate drainage. All patients in the study also received standard-of-care treatment for VAP prevention, as outlined in the Safer Healthcare Now bundle.15,16 Safer Healthcare Now is a program of the Canadian Patient Safety Institute, similar to the 5 Million Lives Campaign in the United States. The VAP bundle was implemented in June 2005 and includes the use of semirecumbent positioning in all patients who can tolerate head elevation, daily evaluation of readiness for extubation, oral care and decontamination with chlorhexidine, and initiation of safe enteral nutrition within 24 to 48 hours of ICU admission. The addition of CASS to the bundle was made in 2007. The only change in the standard of ventilatory care during the study period was the implementation of CASS. Patients were extubated as soon as the following criteria were met: Normothermia (4361C), neurologically intact and awake, hemodynamic stability, and no physical signs of respiratory distress (per UOHI standard operating procedures for mechanically ventilated patients). The primary outcome of this study was pneumonia, defined as the new onset of pneumonia in a patient who underwent mechanical ventilation. The clinical criteria for the diagnosis of pneumonia are summarized in Table 1. Secondary outcomes for this study included 30-day in-hospital mortality, ventilation time, need for tracheostomy, ICU length of stay (LOS), and hospital LOS. Patients were grouped into three surgical categories: Patients undergoing coronary artery bypass graft (CABG) surgery alone, Table 1. Criteria for the Diagnosis of Pneumonia in Ventilated Patients A. Rales or dullness to percussion on physical examination of chest
and any of the following: 1. new onset of purulent sputum or change in the character of sputum 2. organism isolated from blood culture 3. isolation of pathogen from specimen obtained by transtracheal aspirate, bronchial brushing, or biopsy or B. Chest radiographic examination shows new or progressive
infiltrate, consolidation, cavitation, or pleural effusion and any of the following: 1. one of the additional criteria noted above 2. isolation of virus or detection of viral antigen in respiratory secretion 3. diagnostic single antibody titer (IgM) or fourfold increase in paired serum samples (IgG) for pathogen 4. histopathologic evidence of pneumonia
Table 2. Baseline Demographic, Preoperative, and Intraoperative Clinical Characteristics in Control and CASS Groups
Variable
Control Group
CASS Group
(n ¼ 2,430)
(n ¼ 2,450)
p Value
Age (years) 65.6 ⫾ 11.9 65.0 ⫾ 11.9 NS Height (cm) 170.0 ⫾ 9.85 170.3 ⫾ 9.68 NS Weight (kg) 81.6 ⫾ 17.7 81.6 ⫾ 17.8 NS Surgical category* CABG, n (%) 1293 (53.2%) 1132 (46.2%) o0.0001 Valve, n (%) 396 (16.3%) 470 (19.1%) Complex, n (%) 741 (30.5%) 848 (34.6%) Operative priority† Elective, n (%) 1581 (65.1%) 1560 (63.7%) NS Urgent, n (%) 670 (27.6%) 709 (28.9%) Emergency, n (%) 179 (7.4%) 181 (7.4%) Redo surgery, n (%) 291 (12.0%) 280 (11.4%) NS CARE score, n (%) 1 150 (6.2%) 185 (7.6%) NS 2 967 (39.8%) 914 (37.3%) 3 889 (36.6%) 950 (38.8%) 4 289 (11.9%) 278 (11.4%) 5 135 (5.6%) 123 (5.0%) NYHA angina class, n (%) 0 914 (37.6%) 908 (37.2%) NS 1 137 (5.6%) 139 (5.7%) 2 379 (15.6%) 364 (14.9%) 3 487 (20.0%) 489 (20.0%) 4 513 (21.1%) 542 (22.2%) Previous MI, n (%) 986 (40.6%) 912 (37.2%) 0.0163 NYHA CHF class, n (%) 0 1083 (44.6%) 1092 (44.6%) NS 1 190 (7.8%) 189 (3.9%) 2 444 (18.3%) 475 (19.4%) 3 565 (22.7%) 555 (22.7%) 4 148 (6.1%) 139 (5.7%) Chronic obstructive 326 (13.4%) 295 (12.0%) NS pulmonary disease, n (%) Chronic restrictive 45 (1.8%) 37 (1.51%) NS pulmonary disease, n (%) Other respiratory 83 (3.4%) 65 (2.7%) NS comorbidities, n (%) Previous CVA, n (%) 249 (10.3%) 266 (10.9%) NS Preoperative shock, n (%) 164 (6.8%) 187 (7.6%) NS Cardiopulmonary bypass 104.6 ⫾ 50.7 108.9 ⫾ 63.5 0.0088 time (minutes) Abbreviations: CABG, coronary artery bypass grafting; CARE, cardiac anesthesia risk evaluation; CASS, continuous aspiration of subglottic secretions; CHF, congestive heart failure; CVA, cerebral vascular accident; MI, myocardial infarction; NS, nonsignificant; NYHA, New York Heart Association. *CABG surgery consisted of coronary artery bypass grafting alone; valve surgery consisted of valve repair or replacement alone; complex surgery included CABG with 1 or more valve interventions, aortic surgery, cardiac transplant, left ventricular assist device insertion, pulmonary thromboendarterectomy, or extracorporeal membrane oxygenation. †Elective indicated non-urgent cardiac surgery; urgent indicated surgery within 24 hours of diagnosis; emergency indicated surgery as soon as an operating room is available.
patients undergoing valve repair or replacement alone, and all other surgeries (including combined CABG and valve surgery, pulmonary thromboendarterectomy, cardiac transplant, and ascending aortic surgery). Operative priority was defined as elective, urgent (patients
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IMPACT OF SUBGLOTTIC SUCTIONING ON THE INCIDENCE OF PNEUMONIA AFTER CARDIAC SURGERY
requiring surgery within 24 hours), and emergency (patients requiring immediate surgery). Assuming a baseline pneumonia rate of 6% in the surgical population, it was estimated that the sample size would have statistical power of 80% to detect an absolute decrease in pneumonia of 1%. Continuous, normally distributed variables were analyzed using twotailed t-tests and are described as mean ⫾ standard deviation, and continuous variables that were not normally distributed were analyzed using Wilcoxon rank sum tests and are described as median ⫾ interquartile range. Categoric variables were analyzed using χ2 tests and are presented as counts (proportions). Potential confounders were identified a priori based on a structured PubMed search using the MESH terms “cardiac surgical procedures,” “coronary artery bypass,” “cardiopulmonary bypass,” “pneumonia,” “ventilator-associated pneumonia,” “prolonged ventilation,” “risk factors,” and “epidemiologic methods.”1,6,9–11,16 For regression analyses, intraoperative and postoperative risk factors were included at baseline if identified through this search strategy in at least two publications from 1995 to 2010. There were no identified risk factors from this literature search that were not available within the institutional database. Univariate analysis was performed for each of these variables with respect to the primary outcome. Multivariable logistic regression models were constructed to adjust for potential confounding variables. All variables meeting a threshold of p o 0.10 on the univariate analysis were selected for evaluation in the multivariable model. The multivariable model was constructed using a stepwise selection algorithm. For adjusted continuous secondary outcomes, clinically significant cutoffs were chosen for ventilation time (r24 hours v 424 hours) and ICU LOS (r2 days v 42 days) to create binary outcome measures. No imputations were performed for missing data, and the sample size was allowed to float with the analysis. All analyses were conducted in SAS v9.2 (SAS Institute, Cary, NC) and GraphPad 5.0 (GraphPad Software Inc, La Jolla, CA). RESULTS
A total of 4,880 patients met the inclusion criteria for this study. Of these, 2,430 patients underwent a major cardiac surgical procedure with a standard endotracheal tube (April 1, 2007 to March 31, 2009), and 2,450 patients underwent a major cardiac surgical procedure with CASS (June 1, 2009 to May 31, 2011). Baseline demographic, preoperative, and intraoperative characteristics are summarized in Table 2. The control and CASS groups differed with respect to type of Table 3. Unadjusted Primary and Secondary Outcomes in Control and CASS Groups Control Group Outcome
Pneumonia 30-day Mortality Tracheostomy Ventilation time, median hours (IQR) ICU length of stay, median days (IQR) Hospital length of stay, median days (IQR)
(n ¼ 2430)
136 81 57 8.42
(5.6%) (3.3%) (2.3%) (5.5-17.3)
CASS Group (n ¼ 2450)
46 51 56 7.3
(1.9%) (2.1%) (2.3%) (4.8-15.0)
1.77 (0.92-3.54)
1.17 (0.92-3.00)
10.0 (7.0-17.0)
10.0 (7.0-16.0)
p Value
o0.0001 0.007 NS o0.0001 0.0004
NS
Abbreviations: CASS, continuous aspiration of subglottic secretions; IQR, interquartile range; NS, nonsignificant.
Table 4. Multivariable Logistic Regression Model of Pneumonia and Secondary Outcomes in CASS Versus Control Groups Outcome
Odds Ratio (95% CI)
Pneumonia 30-day Mortality Ventilation time 424 h ICU length of stay 42 days
0.342 0.700 0.841 0.817
(0.239-0.490) (0.476-1.027) (0.694-1.020) (0.718-0.931)
p Value
o0.0001 0.0685 0.0787 0.0024
CASS, continuous aspiration of subglottic secretions; CI, confidence interval.
surgery, history of previous myocardial infarction, and cardiopulmonary bypass time. The overall incidence of pneumonia in the study population was 3.7%. The unadjusted incidence of pneumonia was 1.9% in the CASS group and 5.6% in the control group (p o 0.0001). The CASS group also had lower 30-day inhospital mortality (2.1% v 3.3%; p ¼ 0.007), median ventilation time (7.3 v 8.4 hours; p o 0.0001), and shorter median ICU LOS (1.17 v 1.77 days; p o 0.0004) compared with the control group (Table 3). Tracheostomy rates and median hospital LOS did not differ between groups. After correcting for the variables that were significant between the 2 groups using multivariable modeling, CASS remained an independent risk predictor for pneumonia (odds ratio [OR] 0.34, 95% confidence interval [CI] 0.24-0.49) and ICU LOS (OR 0.82, 95% CI 0.72-0.93) (Table 4). However, the association between CASS and decreased mortality and ventilation time did not remain after adjusting for confounders. DISCUSSION
This retrospective observational study of patients undergoing cardiac surgery found that the use of CASS was associated with a decreased incidence of pneumonia and decreased ICU LOS. An association between CASS and 30day mortality, need for tracheostomy, or hospital LOS was not found. The CASS group had a 66% lower incidence of pneumonia. The findings were consistent with a recent meta-analysis of RCTs in the ICU population, which found VAP rates were approximately halved by the use of CASS.9 Existing studies vary with respect to how subglottic suctioning was performed. Patients in some trials received intermittent suctioning and drainage, while others received continuous aspiration of subglottic secretions. Intermittent drainage is thought to be less effective for VAP prevention.9,17,18 All patients in this study who received subglottic suctioning had continuous aspiration of secretions with regular reassessments by respiratory therapists to ensure effective drainage. The 2 previous RCTs in the cardiac surgical population did not find a significant benefit.10,11 However, both studies found a trend toward lower VAP rates in patients who received CASS (Relative Risk 0.61 and 0.67). The 1999 study pre-dated current VAP prevention recommendations and had a higher baseline incidence of VAP (8.2%). Their power calculation assumed a baseline incidence of 17.5%, thus their sample size was insufficient to detect the expected 7.5% absolute risk reduction.10 The more recent RCT in
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2008 was powered to detect a 38% relative risk reduction from their baseline risk of VAP of 5.3%, thus their finding of a 32% relative risk reduction with CASS was not statistically significant.11 With larger sample sizes, it is possible that these studies would have found benefit from CASS rather than a trend toward benefit. Previous studies of CASS for VAP prevention found benefit mainly in patients ventilated for periods of time longer than 72 hours.8,9 Given that the median ventilation times in both groups were short (8.4 hours and 7.0 hours in the control and intervention groups, respectively), the findings of the present study suggested that the routine use of CASS may be beneficial even in patients with shorter anticipated ventilation times, including patients undergoing cardiac surgery. It should be noted that subglottic suctioning endotracheal tubes are more expensive than standard endotracheal tubes. The purpose of the study was not to conduct a cost-benefit analysis. However, it is useful to note that, given the difference in endotracheal tube prices of $14.68 (adjusted to 2014 US dollars [USD]), the material cost of using CASS in the intervention group was $35,966 USD. The CASS group had 91 fewer pneumonias than would be expected by the control group results, for a cost reduction of $911,729 USD (based on a conservative estimate of $10,019 as the cost of pneumonia in the ICU).19 The present study was limited by the evolving clinical definitions of pneumonia and ventilator-associated pneumonia. To ensure consistency of diagnostic criteria throughout the study, the UOHI database definition of pneumonia (Table 1) was used for patients receiving postoperative mechanical ventilation, which arose from the Centers for Disease Control and Prevention (CDC) definition.20 It would have been ideal to use the current definition of VAP, but the study pre-dated the release of the new definition.4 The present study also had the inherent limitations of a retrospective analysis of a prospectively collected database. Confounding by unaccounted-for variables may have occurred. Although care was provided according to protocols, the groups were not homogenous, and they represented patients from 2 separate time periods. With the exception of CASS, the VAP prevention bundle and respiratory care pathways implemented at the UOHI did not change during the study period. Nonetheless, it is possible that increased awareness of and compliance with VAP prevention guidelines may have influenced care. Many cardiac surgical patients cannot tolerate head-ofbed elevation due to hemodynamic instability, resulting in greater risk of pneumonia. In addition to a higher pneumonia rate, the control group had a longer median ventilation time (by 1.1 hours) and a
Fig 1. Number of intubated patients (by day) among patients with and without continuous aspiration of subglottic secretions (CASS).
longer median ICU LOS (by 0.6 days). It is possible that longer ventilation time is a confounder of the relationship between CASS and pneumonia; patients ventilated for longer periods of time are more likely to develop pneumonia. However, the incremental risk is estimated to be 1% to 3% per extra day of ventilation5,6, thus the 1.1 hour difference should not account for the 3.7% increased incidence of pneumonia in the control group. It is more likely that both ventilation time and ICU LOS are further down the causal pathway; patients who develop pneumonia are more likely to require prolonged ventilation and a longer ICU stay. In this case, pneumonia would be an intermediate variable between CASS and ventilation time. The vast majority of patients in both groups were extubated by the first postoperative day (Fig 1), and the respiratory care pathway, weaning criteria, and ICU discharge criteria did not change during the study period with the exception of CASS. Ventilator-associated pneumonia is a clinically important complication of mechanical ventilation. With heightened awareness of the severity of pneumonia and the implementation of VAP prevention bundles, the overall incidence of pneumonia is decreasing. The findings of the present study suggest that the use of CASS reduces pneumonia incidence in a cardiac surgical population, even though the median postoperative ventilation time was well under 24 hours. We anticipate more widespread use of subglottic suctioning endotracheal tubes in all surgical patients who are at high risk of requiring postoperative ventilation, even for a brief period of time. In conclusion, universal implementation of CASS in a quaternary care cardiac surgical population was associated with a decreased incidence of pneumonia. Further studies are required to confirm our results. However, it may be prudent to consider the routine use of CASS endotracheal tubes in patients who are expected to require short-term postoperative ventilation.
REFERENCES 1. Collard HR, Saint S, Matthay MA: Prevention of ventilatorassociated pneumonia: An evidence-based systematic review. Ann Intern Med 138:494-501, 2003 2. Craven DE: Preventing ventilator-associated pneumonia in adults: Sowing seeds of change. Chest 130:251-260, 2006 3. Craven DE, Steger KA: Epidemiology of nosocomial pneumonia. New perspectives on an old disease. Chest 108(suppl):1S-16S, 1995 4. Hunter JD: Ventilator associated pneumonia. BMJ 344:e3325, 2012
5. Diaz E, Rodriguez AH, Rello J: Ventilator-associated pneumonia: Issues related to the artificial airway. Respir Care 50:900-906; discussion 906-909, 2005 6. Cook DJ, Walter SD, Cook RJ, et al: Incidence of and risk factors for ventilator-associated pneumonia in critically ill patients. Ann Intern Med 129:433-440, 1998 7. Mahul P, Auboyer C, Jospe R, et al: Prevention of nosocomial pneumonia in intubated patients: Respective role of mechanical
IMPACT OF SUBGLOTTIC SUCTIONING ON THE INCIDENCE OF PNEUMONIA AFTER CARDIAC SURGERY
subglottic secretions drainage and stress ulcer prophylaxis. Intensive Care Med 18:20-25, 1992 8. Dezfulian C, Shojania K, Collard HR, et al: Subglottic secretion drainage for preventing ventilator-associated pneumonia: A metaanalysis. Am J Med 118:11-18, 2005 9. Muscedere J, Rewa O, McKechnie K, et al: Subglottic secretion drainage for the prevention of ventilator-associated pneumonia: A systematic review and meta-analysis. Crit Care Med 39:1985-1991, 2011 10. Kollef MH, Skubas NJ, Sundt TM: A randomized clinical trial of continuous aspiration of subglottic secretions in cardiac surgery patients. Chest 116:1339-1346, 1999 11. Bouza E, Pérez MJ, Muñoz P, et al: Continuous aspiration of subglottic secretions in the prevention of ventilator-associated pneumonia in the postoperative period of major heart surgery. Chest 134:938-946, 2008 12. Canadian Institutes of Health Research, Natural Sciences and Engineering Research Council of Canada, and Social Sciences and Humanities Research Council of Canada: Tri-Council Policy Statement: Ethical Conduct for Research Involving Humans, December 2010. Available online at: http://www.pre.ethics.gc.ca/pdf/eng/tcps2/ TCPS_2_FINAL_Web.pdf 13. Dupuis JY, Wang F, Nathan H, et al: The cardiac anesthesia risk evaluation score: A clinically useful predictor of mortality and morbidity after cardiac surgery. Anesthesiology 94:194-204, 2001
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14. Ferguson TB Jr, Dziuban SW Jr, Edwards FH, et al: The STS National Database: Current changes and challenges for the new millennium. Committee to Establish a National Database in Cardiothoracic Surgery, The Society of Thoracic Surgeons. Ann Thorac Surg 69:680-691, 2000 15. Pruitt B, Jacobs M: Best-practice interventions: How can you prevent ventilator-associated pneumonia? Nursing 36:36-41; quiz 41-32, 2006 16. Muscedere JG, Martin CM, Heyland DK: The impact of ventilator-associated pneumonia on the Canadian health care system. J Crit Care 23:5-10, 2008 17. Dragoumanis CK, Vretzakis GI, Papaioannou VE, et al: Investigating the failure to aspirate subglottic secretions with the Evac endotracheal tube. Anesth Analg 105:1083-1085, 2007 18. O'Neal PV, Munro CL, Grap MJ, et al: Subglottic secretion viscosity and evacuation efficiency. Biol Res Nurs 8:202-209, 2007 19. Safdar N, Dezfulian C, Collard HR, et al: Clinical and economic consequences of ventilator-associated pneumonia: A systematic review. CritCare Med 33:2184-2193, 2005 20. Association for Professionals in Infection Control and Epidemiology, Inc: APIC infection control and applied epidemiology: Principles and practice. St. Louis, Mosby, 1996
