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(Chest. 2005;128:1650-1656.)
© 2005 American College of Chest Physicians

Impact of Ventilator-Associated Pneumonia on Outcome in Patients With COPD*

Saad Nseir, MD; Christophe Di Pompeo, PhD; Stéphane Soubrier, MD; Béatrice Cavestri, MD; Elsa Jozefowicz, MD; Fabienne Saulnier, MD and Alain Durocher, MD

* From the Intensive Care Unit (Drs. Nseir, Soubrier, Cavestri, Jozefowicz, Saulnier, and Durocher), Calmette Hospital, Regional University Centre; and Medical Assessment Laboratory (Dr. Di Pompeo), EA 3614, Lille II University, Lille, France.

Correspondence to: Saad Nseir, MD, Réanimation Médicale, Hôpital Calmette, CHRU, boulevard du Pr Leclercq, 59037 Lille cedex, France; e-mail s-nseir{at}chru-lille.fr


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Purpose: The aim of this study was to determine the impact of ventilator-associated pneumonia (VAP) on outcome in patients with COPD.

Methods: Prospective, observational, case-control study conducted in a 30-bed ICU during a 5-year period. All COPD patients who required intubation and mechanical ventilation (MV) for > 48 h were eligible. VAP diagnosis was based on clinical, radiographic, and quantitative microbiologic criteria. Patients with unconfirmed VAP were excluded, as well as patients with ventilator-associated tracheobronchitis without subsequent VAP. Matching (1:1) criteria included MV duration before VAP occurrence, age ± 5 years, simplified acute physiology score II on ICU admission ± 5, and ICU admission category. Variables associated with ICU mortality were determined using univariate and multivariate analyses.

Results: A total of 1,241 patients were eligible; 181 patients (14%) were excluded, including 133 patients for VAT and 48 patients for unconfirmed VAP. VAP developed in 77 patients (6%), and all were successfully matched. Pseudomonas aeruginosa was the most frequently isolated bacteria (31%). ICU mortality rate (64% vs 28%), duration of MV (24 ± 15 d vs 13 ± 11 d [± SD]), and ICU stay (26 ± 17 d vs 15 ± 13 d) were significantly (< 0.001) higher in case patients than in control patients. VAP was the only variable independently associated with ICU mortality (odds ratio [OR], 7.7; 95% confidence interval [CI], 3.2 to 18.6; p < 0.001). In VAP patients who received corticosteroids during their ICU stay compared with those who did not receive corticosteroids, mortality rate (50% vs 82%; OR, 1.8; 95% CI, 1.2 to 2.7; p = 0.002), duration of MV (21 ± 14 d vs 27 ± 16 d, p = 0.043), and ICU stay (22 ± 16 d vs 31 ± 18 d, p = 0.006) were significantly lower.

Conclusion: VAP is associated with increased mortality rates and longer duration of MV and ICU stay in COPD patients.

Key Words: clinical outcome • COPD • corticosteroid treatment • critical care • mechanical ventilation • nosocomial pneumonia • ventilator-associated pneumonia


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Ventilator-associated pneumonia (VAP) is the second-most-frequent nosocomial infection among ICU patients. This infection is associated with high mortality and morbidity rates.1 However, mortality attributable to VAP is controversial. The largest case-control study,2 conducted in the United States on 842 VAP patients, found no significant difference in mortality rates between VAP patients and matched control subjects, suggesting that severely ill patients died with VAP and not of VAP. However, other well-conducted case-control studies345 concluded that VAP is associated with an attributable mortality rate (range, 27 to 50%). These conflicting results could be explained by differences in patient characteristics, adequacy of initial antimicrobial treatment, microorganisms responsible for VAP, severity of illness, comorbid factors, and host response factors.6

COPD is a risk factor for nosocomial lower respiratory tract infections.78 Rello et al9 demonstrated that COPD was associated with higher mortality rates in VAP patients. However, after adjustment for confounding factors, COPD was not independently associated with mortality in VAP patients. To our knowledge, no study has evaluated the impact of VAP on mortality and morbidity in COPD patients. However, bronchopulmonary infection could result in increased mortality and morbidity rates when structural lung disease is present. Therefore, we performed a prospective case-control study to determine the impact of VAP on mortality and duration of mechanical ventilation (MV) and ICU stay in COPD patients.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
This prospective, observational, case-control study was conducted in a 30-bed ICU from January 1996 to January 2001. Because it was observational, Institutional Review Board approval was not required in accordance with Institutional Review Board Regulation.

All COPD patients who required intubation and MV for > 48 h were eligible. Patients without COPD, trauma patients, patients who did not receive MV or received MV for < 48 h, patients who only received noninvasive ventilation (NIV), patients with solid or hematology malignancy, and patients with tracheotomy at ICU admission were not eligible. Patients with ventilator-associated tracheobronchitis (VAT)7 without subsequent VAP were excluded, as well as patients with clinically suspected VAP without microbiologic confirmation.

All data were prospectively collected. VAP episodes were identified by prospective surveillance of nosocomial infections. Only first episodes of VAP occurring > 48 h after the initiation of MV were included.

Study Population
Patients were intubated either via the oral or nasal routes according to the clinical status and the habits of the physician in charge. The oropharyngeal cavity was cleaned qid with chlorhexidine solution. Continuous subglottic suctioning was not utilized. The ventilator circuit was not changed routinely. In all patients, a heat and moisture exchanger was positioned between the Y piece and the patient; the heat and moisture exchangers were changed every 48 h or more frequently if visibly soiled. Patients were kept in semirecumbent position during most of their period of MV. There was no systematic stress ulcer prophylaxis and no selective digestive decontamination. Infection control policy included isolation techniques in patients with multidrug-resistant bacteria (MRB), written antibiotic treatment protocol, and continuous surveillance of nosocomial infections. Corticosteroid treatment (methylprednisolone, 0.5 to 1 mg/kg/d) was at the physicians’ discretion. This treatment was administered for acute exacerbation of COPD or bronchospasm. In the absence of contraindications, NIV was used in all COPD patients with acute hypercapnic respiratory failure. Intubation was performed in patients with NIV failure or contraindications for NIV.

Definitions
COPD was defined according to American Thoracic Society criteria.10 VAP was defined by the presence of two of the following criteria: temperature > 38.5°C or < 36.5°C, leukocyte count > 10,000/µL or < 1,500/µL, purulent tracheal aspirate, associated with new or progressive radiographic infiltrate and a positive (≥ 106 cfu/mL) tracheal aspirate culture result. VAP episodes occurring < 5 d after starting MV were considered to be early onset. Late-onset VAP was defined as VAP diagnosed ≥ 5 d after starting MV. Prior antibiotic use was defined as any antibiotic treatment during the 2 weeks preceding ICU admission. Antimicrobial therapy was deemed adequate when at least one antibiotic active in vitro on all organisms causing VAP was administrated in appropriate dosage within the first 24 h of VAP occurrence. MRB were defined as follows: methicillin-resistant Staphylococcus aureus, ceftazidime or imipenem-resistant Pseudomonas aeruginosa, Acinetobacter baumannii, extended-spectrum ß-lactamase-producing Gram-negative bacilli, and Stenotrophomonas maltophilia. Long-term oral corticosteroid use was defined as administration of corticosteroids (≥ 20 mg/d) during at least 1 month over the last 3 months. Corticosteroid treatment during ICU stay was defined as any corticosteroid treatment for > 2 days. Outcomes evaluated included ICU mortality, duration of MV, and ICU stay.

Matching Criteria
Each case patient was matched to one control patient according to the following criteria: (1) duration of MV before VAP occurrence; a control patient had to have at least the same duration of MV before VAP occurrence as a case patient; (2) age ± 5 years; (3) simplified acute physiology score (SAPS) II on ICU admission ± 5 points; (4) category of ICU admission (medical/surgical); and (5) date of ICU admission when more than one potential control patient was well matched to a case patient.

Statistical Analysis
Statistical software (SPSS version 9; SPSS; Chicago, IL) was used for data analysis. Case patients were compared with control subjects using {chi}2 test or Fisher Exact Test when appropriate for qualitative variables, and Mann-Whitney U test for quantitative variables. Results are presented as frequency (%) for qualitative variables or mean ± SD for quantitative variables.

Univariate and multivariate analyses were performed to determine variables associated with ICU mortality. The following variables were included in the univariate analysis: age, gender, SAPS II on ICU admission, surgery, transfer from other wards, diabetes mellitus, prior antibiotic use, long-term oral corticosteroid use, organ failures, primary diagnosis, corticosteroid treatment during ICU stay, VAP, VAP related to MRB, and adequacy of initial antimicrobial treatment for VAP. Only significant (p < 0.05) variables were included in the stepwise logistic regression model.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
During the study period, 1,241 patients were eligible; 181 patients (14%) were excluded, including 133 patients (10%) for VAT without subsequent VAP, and 48 patients (3%) for clinically suspected VAP without bacteriologic confirmation. VAP developed in 77 patients (6%), and were all successfully matched (Fig 1 ). The rate of prior antibiotic use was higher in case patients than in control patients. During ICU stay, the duration of antibiotic treatment was longer in case patients than in control patients. Other patient characteristics were similar in case patients and control patients (Table 1 ). The mean time between starting MV and VAP occurrence was 12 ± 9 d (± SD). VAP was late in onset in 55 patients (71%). Initial antimicrobial treatment was adequate in 58 patients (75%) with VAP. The rate of inadequate initial antibiotic treatment was higher in patients with VAP related to MRB than in patients with VAP related to other bacteria (18 of 32 patients [56%] vs 1 of 45 patients [2%]; odds ratio [OR], 2.3; 95% confidence interval [CI], 1.5 to 3.6; p < 0.001). The mean dose of corticosteroids received by VAP patients during ICU stay was 0.6 ± 0.2 mg/kg/d (equivalent to 180 ± 60 mg/d of hydrocortisone in a 60-kg patient); mean duration of corticosteroid treatment was 19 ± 14 days.



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  		Figure 1.. Study profile.

 

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  		Table 1.. Patient Characteristics*

 
Microbiologic Results
One hundred one bacteria were associated (≥ 106 cfu/mL) with the 77 first VAP episodes. P aeruginosa (31%), A baumannii (19%), and S aureus (14%) were the most frequently isolated microorganisms (Table 2 ). VAP was polymicrobial in 23 patients (29%). VAP was related to MRB in 32 patients (41%). Tracheal aspirate culture findings were positive at 104 to 105 cfu/mL in 7 of 48 patients (14%) with unconfirmed VAP.


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  		Table 2.. Bacteria Associated With 77 Episodes of VAP

 
Outcome of Case Patients and Control Patients
Mortality rate, duration of MV, and length of ICU stay were significantly higher in case patients than in control patients (Table 3 ). No significant relationship was found between outcome of VAP patients and adequacy of initial antimicrobial treatment, MRB, or surgery (Table 4 ). However, mortality rate, duration of MV, and ICU stay were significantly lower in VAP patients who received corticosteroids during their ICU stay compared with those who did not receive corticosteroids (Table 4). Among the 42 VAP patients who received corticosteroids in the ICU, 34 patients received long-term corticosteroid treatment, and 8 patients received only short-term corticosteroid treatment. In VAP patients with long-term and short-term corticosteroid treatment compared with VAP patients who did not receive corticosteroids, the mortality rate was significantly lower (21 of 34 patients [61%] vs 29 of 35 patients [82%]; p = 0.045), and durations of MV (23 ± 16 d vs 27 ± 16 d, p = 0.182) and ICU stay (25 ± 18 d vs 31 ± 18 d, p = 0.109) were similar. In VAP patients with only short-term corticosteroid treatment compared with VAP patients who did not receive corticosteroids, the mortality rate (0 of 8 patients [0%] vs 29 of 35 patients [82%], p = <0.001) and duration of MV (14 ± 11 d vs 27 ± 16 d, p = 0.039) and ICU stay (15 ± 11 d vs 31 ± 18 d, p = 0.006) were significantly lower. In VAP patients with only short-term corticosteroid treatment compared with VAP patients receiving long-term and short-term corticosteroids, respectively, the mortality rate (0 of 8 patients [0%] vs 21 of 34 patients [61%], p = 0,002) and duration of MV (14 ± 11 d vs 23 ± 16 d, p = 0.008) and ICU stay (15 ± 11 d vs 25 ± 18 d, p = 0.001) were significantly lower. No significant difference was found between VAP patients who received corticosteroids during their ICU stay compared with those who did not receive corticosteroids with regard to adequacy of initial antibiotic treatment (31 of 42 patients [73%] vs 27 of 35 patients [77%], p = 0.473) and MRB rates (19 of 42 patients [42%] vs 13 of 35 patients [37%], p = 0.314).


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  		Table 3.. Outcomes of Study Patients and Excluded Patients*

 

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  		Table 4.. Outcomes of Subgroups of Patients With VAP*

 
Factors Associated With ICU Mortality
Renal, cardiac, and neurologic failures on ICU admission, VAP, and VAP related to MRB were associated with ICU mortality in univariate analysis (Table 5 ). Only VAP was independently associated with ICU mortality (OR, 7.76; 95% CI, 3.2 to 18.6; p < 0.001).


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  		Table 5.. Risk Factors for ICU Mortality in Patients With and Without VAP

 
Characteristics and Outcome of Excluded Patients
Patients excluded for unconfirmed VAP were significantly younger than case patients and control patients, as well as patients excluded for VAT compared with case patients and control patients. SAPS II was significantly lower in VAT patients compared with control patients. The rate of prior antibiotic use was significantly higher in patients with unconfirmed VAP compared with control patients, and in VAT patients compared with control patients. Neurologic failure was more frequent in patients with unconfirmed VAP compared with case patients and control patients. The duration of antibiotic treatment during ICU stay was longer in patients with unconfirmed VAP compared with control patients, and in VAT patients compared with control patients. Other patient characteristics were similar in excluded patients compared with case patients and control patients (Table 1).

No significant difference in outcome was found between patients excluded for unconfirmed VAP and case patients. Mortality rate, duration of MV, and ICU stay were significantly higher in patients excluded for unconfirmed VAP compared with control patients (Table 3). In patients with unconfirmed VAP who had positive tracheal aspirate culture findings (104 to 105 cfu/mL) compared with those who had negative culture findings, mortality rates (4 of 7 patients [57%] vs 26 of 41 patients [63%], p = 0.531), duration of MV (23 ± 13 d vs 22 ± 12 d, p = 0.491), and duration of ICU stay (25 ± 14 d vs 24 ± 16 d, p = 0.489) were similar. In patients with unconfirmed VAP who had positive tracheal aspirate culture findings (104 to 105 cfu/mL) compared with VAP patients, respectively, mortality rates (4 of 7 patients [57%] vs 50 of 77 patients [64%], p = 0.389), duration of MV (23 ± 13 d vs 24 ± 15 d, p = 0.461), and length of ICU stay (25 ± 14 d vs 26 ± 17 d, p = 0.459) were similar.

Although the duration of MV and ICU stay were similar in VAT patients compared with case patients, the mortality rate was significantly lower in patients with VAT compared with case patients. Mortality rate, duration of MV, and ICU stay were significantly higher in VAT patients compared with control patients (Table 3).


   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Our results demonstrate that VAP is associated with higher mortality rates and longer duration of MV and ICU stay in COPD patients. In addition, VAP is independently associated with ICU mortality. Our results also suggest that low doses of corticosteroids are associated with a lower mortality rate and shorter duration of MV and ICU stay in COPD patients with VAP.

To our knowledge, this case-control study is the first to evaluate the impact of VAP on mortality and morbidity in COPD patients. Previous studies8111213 conducted in heterogeneous ICU populations, including some patients with COPD, highlighted the link between VAP and increased mortality and morbidity. However, VAP may increase mortality in severely ill patients but may be more likely to develop in sicker patients, with inherently higher mortality rates.14 Several studies2345121315161718192021222324252627 have investigated the complex relationship between VAP and mortality using different diagnostic criteria and different statistical methods in different populations. Multivariate analyses, case-control studies, and randomized controlled studies of an effective prevention of VAP were used to determine the impact of VAP on mortality and morbidity.

VAP has been identified as an independent risk factor for mortality by numerous studies.131516 However, other studies1217 failed to identify VAP as an independent risk factor for mortality. The selection and exclusion of potential risk factors, and the different patient characteristics may explain these conflicting results. Three of eight case-control studies345 concluded that VAP was associated with significantly increased mortality. However, the mortality rates did not differ significantly between patients with VAP and matched control subjects in the five other case-control studies.218192021 In the largest study2 on VAP conducted in the United States, 842 patients with VAP were matched with 2,243 patients without VAP according to duration of MV, severity of illness on hospital admission, type of hospital admission, and age. The mortality rates were similar in case patients and control patients. However, patients with VAP occurring > 24 h after intubation were included. In addition, the mean interval between intubation and the identification of VAP was 3.3 days. Moreover, rates of COPD patients included in that study could not be determined. Randomized studies2223242526 showed a reduction in VAP rates using continuous aspiration of subglottic secretions, selective digestive decontamination, semirecumbent position, and chest physiotherapy. A reduction in VAP rates in these studies was not associated with reduction in mortality rates, suggesting the absence of mortality attributable to VAP. However, a randomized trial27 assessed the efficacy of NIV in patients with weaning failure, and found a significant reduction in nosocomial pneumonia and mortality rates in patients with NIV compared with the conventional weaning group. These results suggest that invasive ventilation withdraw is associated with a reduction in VAP incidence, resulting in lower mortality rate.

The relationship between VAP and mortality is influenced by several factors: adequacy of initial antimicrobial treatment, microorganisms responsible for VAP, severity of illness, comorbid factors, and host response factors. In our study, the mortality rate attributable to VAP was 34%. This high rate could be explained by the following: (1) advanced age, (2) high rates of VAP related to MRB and inadequate initial antibiotic treatment, (3) high rate of late-onset VAP, and (4) antecedent of COPD. Advanced age, VAP related to MRB, inadequate initial antibiotic treatment, and late-onset VAP have previously been reported to be associated with higher mortality rates in ICU patients.3282930 COPD is associated with increased mortality rates in VAP patients.9 In patients with structural lung disease, nosocomial bronchopulmonary infection may result in increased mortality and morbidity. However, in patients with community-acquired pneumonia, structural lung disease was not associated with increased mortality.31

In this study, VAP was associated with longer duration of MV and ICU stay. These results are consistent with those of other case-control studies.23518192021 In order to reduce mortality and morbidity in COPD patients with VAP, prompt and adequate initial antibiotic treatment should be used.6 In addition, prevention measures should be applied in intubated COPD patients to reduce VAP incidence.32

In COPD patients with VAP, corticosteroid use during ICU stay, especially short-term use in patients without long-term corticosteroid use, was associated with lower mortality rate and shorter duration of MV and ICU stay. These results are plausible given that increased inflammatory response is the main predictor of nonresponse and mortality in patients with VAP.33 In addition, a recent randomized controlled study34 conducted in patients with severe community-acquired pneumonia found a significant reduction in mortality rate in patients who received low doses of hydrocortisone compared with those who received placebo. However, corticosteroid use is the major independent risk factor for ICU-acquired paresis.35 Furthermore, corticosteroid use could be harmful in patients with immunoparalysis and uncontrolled sources of infection. The beneficial effect of corticosteroids found in our study was a secondary outcome, and further randomized trials are necessary to determine the effect of corticosteroids on outcome of COPD patients with VAP.

Our study has several limitations. First, this was a single-center study. Therefore, our results may not be generalizable to patients in other ICUs. Second, some of the trends observed in VAP subgroup analyses could have reached statistical significance if the number of included patients had been larger. Third, invasive procedures were not used to diagnose VAP. However, quantitative tracheal aspirate was performed in all patients with a threshold of 106 cfu/mL. Postmortem studies36 demonstrated an acceptable overall diagnostic accuracy of quantitative tracheal aspirate as compared with BAL or protected specimen brush. Fourth, information on severity of COPD was not available. Finally, exclusion of patients with unconfirmed VAP and patients with VAT may be debatable. Because clinical and radiographic signs of VAP are not specific, we used clinical, radiographic, and quantitative microbiologic criteria to define VAP. A high rate of prior antibiotic use (70%) may have resulted in negative culture findings of tracheal aspirate in some patients with unconfirmed VAP. However, the characteristics and outcomes of all excluded patients were carefully evaluated.

We conclude that VAP is associated with increased mortality and longer duration of MV and ICU stay in COPD patients. Efforts should be made to reduce VAP incidence in these patients and to initiate prompt and adequate antibiotic treatment when VAP is suspected.


   Footnotes
 
Abbreviations: CI = confidence interval; MRB = multidrug-resistant bacteria; MV = mechanical ventilation; NIV = noninvasive ventilation; OR = odds ratio; SAPS = simplified acute physiology score; VAP = ventilator-associated pneumonia; VAT = ventilator-associated tracheobronchitis

Presented in part at the 101st American Thoracic Society Conference, May 20–25, 2005, San Diego, CA.

Received for publication December 15, 2004. Accepted for publication February 14, 2005.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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