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(Chest. 2001;120:555-561.)
© 2001 American College of Chest Physicians

The Occurrence of Ventilator-Associated Pneumonia in a Community Hospital*

Risk Factors and Clinical Outcomes

Emad H. Ibrahim, MD; Linda Tracy, MRT; Cherie Hill, BS; Victoria J. Fraser, MD and Marin H. Kollef, MD, FCCP

* From the Pulmonary and Critical Care Medicine Division (Drs. Ibrahim and Kollef) and Division of Infectious Diseases (Mss. Tracy and Hill, and Dr. Fraser), Department of Internal Medicine, Washington University School of Medicine, Barnes-Jewish Hospital, Saint Louis, MO.

Correspondence to: Marin H. Kollef, MD, FCCP, Pulmonary and Critical Care Medicine Division, Washington University School of Medicine, Campus Box 8052, 660 South Euclid Ave, St. Louis, MO 63110; e-mail: kollefm{at}msnotes.wustl.edu


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Study objectives: To prospectively identify the occurrence of ventilator-associated pneumonia (VAP) in a community hospital, and to determine the risk factors for VAP and the influence of VAP on patient outcomes in a nonteaching institution.

Design: Prospective cohort study.

Setting: A medical ICU and a surgical ICU in a 500-bed private community nonteaching hospital: Missouri Baptist Hospital.

Patients: Between March 1998 and December 1999, all patients receiving mechanical ventilation who were admitted to the ICU setting were prospectively evaluated.

Intervention: Prospective patient surveillance and data collection.

Results: During a 22-month period, 3,171 patients were admitted to the medical and surgical ICUs. Eight hundred eighty patients (27.8%) received mechanical ventilation. VAP developed in 132 patients (15.0%) receiving mechanical ventilation. Three hundred one patients (34.2%) who received mechanical ventilation died during hospitalization. Logistic regression analysis demonstrated that tracheostomy (adjusted odds ratio [AOR], 6.71; 95% confidence interval [CI], 3.91 to 11.50; p < 0.001), multiple central venous line insertions (AOR, 4.20; 95% CI, 2.72 to 6.48; p < 0.001), reintubation (AOR, 2.88; 95% CI, 1.78 to 4.66; p < 0.001), and the use of antacids (AOR, 2.81; 95% CI, 1.19 to 6.64; p = 0.019) were independently associated with the development of VAP. The hospital mortality of patients with VAP was significantly greater than the mortality of patients without VAP (45.5% vs 32.2%, respectively; p = 0.004). The occurrence of bacteremia, compromised immune system, higher APACHE (acute physiology and chronic health evaluation) II scores, and older age were identified as independent predictors of hospital mortality.

Conclusions: These data suggest that VAP is a common nosocomial infection in the community hospital setting. The risk factors for the development of VAP and risk factors for hospital mortality in a community hospital are similar to those identified from university-affiliated hospitals. These risk factors can potentially be employed to develop local strategies for the prevention of VAP.

Clinical implications: ICU clinicians should be aware of the risk factors associated with the development of VAP and the impact of VAP on clinical outcomes. More importantly, they should cooperate in the development of local multidisciplinary strategies aimed at the prevention of VAP and other nosocomial infections.

Key Words: clinical outcomes • community hospital • critical care • hospital mortality • infection • ICU • nosocomial pneumonia • risk factors


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Pneumonia is the most commonly reported nosocomial infection among ICU patients, occurring predominantly in individuals requiring mechanical ventilation (ie, ventilator-associated pneumonia [VAP]), at a rate of 1 to 3% per day of mechanical ventilation.1 Most investigations of VAP have evaluated patients in large teaching hospitals where the prevalence ranges from 10 to 65%, and the associated case fatality rates are > 20% in these reported studies.1 2 3 4 Additionally, the pathogens responsible for VAP have been shown to vary among hospitals.5 6 Knowledge of the incidence of nosocomial infections and their associated local microbial flora may be important to allow more effective utilization of antimicrobial agents.5 6 However, despite improvements in the diagnosis, treatment, and prevention of VAP, it remains an important cause of hospital morbidity and mortality.7 8 To our knowledge, the occurrence of VAP and its impact on clinical outcomes has not been systematically evaluated in a community hospital setting.

Therefore, we performed a pilot study with three goals involving a cohort of patients from a community hospital. First, we wanted to determine the magnitude of the problem of VAP among critically ill adult patients in a community nonteaching hospital. Second, we sought to identify the main risk factors for VAP in this patient population. Third, we set out to evaluate the relationship between hospital mortality and VAP. It was our hope that such data would provide useful information for the clinical management of patients at risk for VAP and those developing VAP in the community hospital setting.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Study Location and Patients
The study was conducted at a private community nonteaching hospital: Missouri Baptist Hospital (500 beds) in St. Louis, MO. During a 22-month period (March 1998 to December 1999), all patients admitted to the medical ICU (10 beds) and surgical ICU (10 beds) were potentially eligible for this investigation. Patients in the ICUs were cared for by their attending physicians and by a dedicated group of critical-care specialists providing in-house medical coverage. A locally developed weaning protocol was used to guide weaning from mechanical ventilation. Patients were entered into the study if they were > 16 years old and required mechanical ventilation in the ICU at any point in their hospitalization. This study was approved by the Washington University School of Medicine Human Studies Committee.

Study Design and Data Collection
A dedicated group of infection control nurses collected data prospectively on all patients receiving mechanical ventilation. One of these nurses made daily rounds in the medical and surgical ICUs to identify eligible patients and to record relevant data from patients’ medical records, bedside flow sheets, computerized radiographic reports, and reports of microbiological studies (sputum Gram’s stains, and sputum, blood, and pleural fluid culture results). Study patients were prospectively followed for the occurrence of VAP until they were successfully treated and discharged from the hospital or until death. Patients could not be entered into the study more than once, and only the first episode of VAP was evaluated.

For all study patients, the following characteristics were prospectively recorded at the time of ICU admission: age, gender, concomitant diseases, hospital-admission diagnosis, indication for mechanical ventilation, the ratio of PaO2 to the fraction of inspired oxygen (FIO2), severity of illness based on APACHE (acute physiology and chronic health evaluation) II scores,9 and the patient’s diagnostic category (medical vs surgical). Specific processes of medical care examined throughout the period of ICU admission as potential risk factors for the development of VAP included the administration of antacids, histamine type-2 receptor antagonists, sucralfate, corticosteroids, tracheostomy, dialysis, reintubation, the presence of central venous catheters and their duration, and mechanical ventilation and its duration. For patients with VAP, these risk factors were required to be present at least 48 h prior to the onset of VAP. The main outcome evaluated was the occurrence of VAP. Secondary outcomes evaluated included hospital mortality, the lengths of ICU and hospital stay, and the development of sepsis syndrome.

Respiratory tract culture specimens were obtained from tracheal aspirates using in-line suction catheters and an in-line collection tube (Trach Care; Ballard Medical Products; Draper, UT). Tracheal aspirates were routinely obtained in patients with a clinical suspicion of VAP prior to starting antibiotic treatment unless such a specimen could not be produced by the patient.

Definitions
All definitions were selected prospectively as part of the original study design. APACHE II scores were calculated based on clinical data available from the first 24 h of ICU admission. Sepsis was defined according to the American College of Chest Physicians/Society of Critical Care Medicine Consensus Conference.10 Sepsis was defined as the presence of a clinically identified site of infection (eg, pneumonia, urinary tract) and two or more of the following: temperature > 38°C or < 36°C; heart rate > 90 beats/min; respiratory rate > 20 breaths/min or PaCO2 < 32 mm Hg; and WBC count > 12 x 109/L, < 4.0 x 109/L, or > 0.10 immature forms (ie, bands).

The diagnostic protocol for VAP used in this study was modified from that established by the American College of Chest Physicians.11 VAP was prospectively defined as the occurrence of a new and persistent radiographic infiltrate in conjunction with one of the following: positive pleural/blood culture results for the same organism as that recovered in the tracheal aspirate or sputum; radiographic cavitation; histopathologic evidence of pneumonia; or two of the following: fever, leukocytosis, and purulent tracheal aspirate or sputum. Persistence of an infiltrate was defined as having the infiltrate present radiographically for at least 72 h. Fever was defined as an increase in the core temperature of >= 1°C and a core temperature > 38.3°C. Leukocytosis was defined as a 25% increase in the circulating leukocytes from the baseline and a value > 10 x 109/L. Tracheal aspirates were considered purulent if abundant neutrophils were present per high-power field using Gram’s stain (ie, > 25 neutrophils per high power field). A cut off of 96 h of mechanical ventilation was used to distinguish patients with early-onset VAP from those with late-onset VAP. This threshold has previously been used to determine the influence of late-onset VAP on patient outcomes.2

Hospital mortality was defined as patient deaths occurring during the initial hospital admission during which they were studied. Immunocompromised patients were defined as those receiving corticosteroids, having positive serum test findings for HIV antibody, having received chemotherapy within the past 45 days before hospital admission, having neutropenia (absolute neutrophil count < 0.5 x 109/L), or having had an organ transplant requiring immunosuppressive therapy.

Statistical Analysis
Univariate analysis was used to compare variables for the outcome groups of interest. Comparisons were unpaired, and all tests of significance were two tailed. Continuous variables were compared using Student’s t test for normally distributed variables and Wilcoxon’s rank-sum test for nonnormally distributed variables. The {chi}2 statistic or Fisher’s Exact Test was used to compare categorical variables. The primary data analysis compared patients without VAP to patients with VAP, and survivors to nonsurvivors. We confirmed the results of these tests, while controlling for specific patient characteristics and severity of illness (Tables 1 , 2 ) with multiple logistic regression analysis12 using a commercial statistical package.13


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  		Table 1.. Patient Characteristics *

 

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  		Table 2.. Process of Care Variables *

 
Multivariate analysis was performed using models that were judged a priori to be clinically sound. This was necessary to avoid producing spuriously significant results with multiple comparisons.14 A stepwise approach was used for entering new terms into the model with 0.05 as the limit for their acceptance or removal. Model overfitting was examined for by evaluating the ratio of outcome events to the total number of independent variables in the final model and specific testing for interactions between the individual variables was included in our analysis. Results of the logistic regression analyses are reported as adjusted odds ratios (AORs) with their 95% confidence intervals (CIs). All values are expressed as the mean (SD) for continuous variables, or as a percentage of the group they were derived from (categorical variables). All p values of <= 0.05 were considered to indicate statistical significance and were based on univariate analysis.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Patients
During a 22-month period (March 1998 to December 1999), 3,171 consecutive patients admitted to the medical and surgical ICUs were prospectively evaluated. Eight hundred eighty patients (27.8%) received mechanical ventilation and comprised the study cohort (Tables 1 , 2) . The mean (SD) age of patients receiving mechanical ventilation was 69.3 (13.2) years (range, 17 to 98 years); 451 patients (51.2%) were men, and 429 patients (48.8%) were women. The mean APACHE II score of the patients who received mechanical ventilation was 23.8 (SD, 6.8; range, 4 to 45). Three hundred seventy-five patients (42.6%) underwent surgery prior to ICU admission.

VAP
One hundred thirty-two patients (15.0%) who received mechanical ventilation acquired VAP during their ICU stay. Patients with VAP had statistically greater APACHE II scores, were more likely to have bacteremia and congestive heart failure, to receive treatment with corticosteroids, and to have statistically lower PaO2/FIO2 ratios, compared to patients who did not acquire VAP (Table 1) . Patients with VAP were also statistically more likely to require dialysis, reintubation, tracheostomy, multiple central venous lines, and to receive treatment with histamine type-2 receptor antagonists or sucralfate (Table 2) . Similarly, the durations of central vein catheterization and mechanical ventilation were statistically longer among patients with VAP, and patients with VAP were statistically more likely to have required hospitalization prior to ICU admission.

Multivariate analysis demonstrated that tracheostomy (AOR, 6.71; 95% CI, 3.91 to 11.50; p < 0.001), multiple central venous line insertions (AOR, 4.20; 95% CI, 2.72 to 6.48; p < 0.001), reintubation (AOR, 2.88; 95% CI, 1.78 to 4.66; p < 0.001), and the use of antacids (AOR, 2.81; 95% CI, 1.19 to 6.64; p = 0.019) were independent risk factors for the development of VAP. Multiple central venous line insertions (AOR, 4.22; 95% CI, 2.91 to 6.13; p < 0.001) were found to be the only independent predictor of VAP occurring within the first 96 h of mechanical ventilation, while reintubation (AOR, 1.81; 95% CI, 1.40 to 2.35; p = 0.022), antacids (AOR, 4.82; 95% CI, 2.58 to 8.98; p = 0.012), and tracheostomy (AOR, 3.23; 95% CI, 2.43 to 4.29; p < 0.001) were predictors of VAP occurring after 96 h of ventilation. The onset of VAP was most common during the first 2 weeks of mechanical ventilation (Fig 1 ).



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  		Figure 1.. Distribution of onset of VAP for the study cohort. The number of patients who received mechanical ventilation for each time period is provided along with the percent of these patients who did not develop VAP.

 
The Distribution of Pathogens Among Patients With Pneumonia
The pathogens associated with VAP for both survivors and nonsurvivors are shown in Table 3 . Pseudomonas aeruginosa was the most common Gram-negative bacterial pathogen isolated from the respiratory tract among infected patients with VAP for both survivors and nonsurvivors. Staphylococcus aureus was the most common Gram-positive bacterial pathogen associated with VAP. Among the S aureus isolates, 26 isolates (72.2%) were oxacillin resistant. S aureus and Aspergillus spp were significantly more common among patients with VAP who died, compared to patients with VAP who survived. All patients with presumed VAP due to Aspergillus spp were either neutropenic (n = 8) or receiving corticosteroids (n = 1). No significant differences in the distribution of pathogens were found for patients developing VAP within 96 h of the onset of mechanical ventilation and after 96 h.


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  		Table 3.. Pathogens Associated With VAP Infection *

 
Hospital Mortality
Three hundred one patients (34.2%) receiving mechanical ventilation died during their hospitalization. The mortality rate of patients developing VAP (45.5%) was significantly greater than the mortality rate of patients without VAP (32.2%; p = 0.004). Patients who died during their hospitalization were statistically older, had greater APACHE II scores, lower PaO2/FIO2 ratios, were more likely to have bacteremia, be immunocompromised, develop acute renal failure, have congestive heart failure, and be white, compared to patients who survived their hospitalization (Table 1) . The patients who died more frequently underwent dialysis, required multiple central venous lines, and received treatment less frequently with histamine type-2 receptor antagonists and antacids. Similarly, the duration of mechanical ventilation was significantly longer among hospital nonsurvivors (Table 2) . Multivariate analysis demonstrated that the occurrence of bacteremia (AOR, 3.56; 95% CI, 1.98 to 6.40; p < 0.001), an immunocompromised state (AOR, 1.56; 95% CI, 0.96 to 2.51; p = 0.070), higher APACHE II scores (1-point increments) [AOR, 1.08; 95% CI, 1.05 to 1.11; p < 0.001], and older age (1-year increments) [AOR, 1.03; 95% CI, 1.02 to 1.05; p < 0.001] were independently associated with hospital mortality.

Secondary Clinical Outcomes
Patients developing VAP had significantly longer lengths of stay in the ICU (23.9 [19.8] days vs 5.9 [5.7] days; p < 0.001) and in the hospital (38.6 [25.8] days vs 15.2 [13.0] days; p < 0.001), compared to patients without VAP. Sepsis syndrome occurred significantly more often among patients with VAP, compared to patients without VAP (34.1% vs 10.4%; p < 0.001).


   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
This study demonstrated that VAP is an important nosocomial infection among patients receiving mechanical ventilation in a community hospital. The development of VAP was associated with greater hospital mortality rates and longer lengths of stay in the ICU and hospital, compared to patients without VAP. However, VAP was not independently associated with hospital mortality using multivariate analysis. We also identified independent risk factors associated with VAP, including tracheostomy, reintubation, the presence of multiple central venous catheters, and the use of antacids. These risk factors could assist in identifying patients at higher risk for VAP as well as management issues requiring potential intervention (eg, avoiding the use of antacids and minimizing the occurrence of reintubation). Additionally, we found that P aeruginosa and S aureus were the most common etiologic pathogens associated with VAP using tracheal aspirate cultures. Finally, it appears that the occurrence of VAP, its associated risk factors, and the influence of VAP on clinical outcomes at a community hospital are similar to those reported from academic medical centers.2 15

The importance of these findings are that they demonstrate that clinically diagnosed VAP is a common problem among patients receiving mechanical ventilation in a community hospital. Additionally, these data have potential implications for the antimicrobial management of VAP. Our findings suggest that antipseudomonal antibiotics and antibiotics directed against S aureus may be initially indicated in many patients with suspected VAP in this specific community hospital. The microbiological flora accounting for VAP in this study are remarkably similar to the pathogens associated with VAP in a large teaching hospital located in the same city, as well as those reported from the Centers for Disease Control and Prevention.6 15 Local knowledge of the microbiological etiologies of VAP appears to be important due to variations in the occurrence of bacterial pathogens between ICUs.5

Interestingly, most of the episodes of VAP in this study were associated with potentially antibiotic-resistant bacteria (eg, P aeruginosa, oxacillin-resistant S aureus, Stenotrophomonas maltophilia, Enterobacter spp). Previous studies16 17 18 have demonstrated the importance of prior antibiotic exposure as a risk factor for VAP due to antibiotic-resistant bacteria. Unfortunately, we did not capture antibiotic utilization data in this study. Nevertheless, we found that patients with VAP were more likely to have hospitalization prior to their ICU admission, compared to patients without VAP. This has been observed by other investigators5 19 suggesting that time of exposure in the hospital, in addition to prior antibiotic therapy, may predispose to infection with antibiotic-resistant bacteria. Finally, a number of other investigations20 21 have demonstrated that community hospitals can be associated with nosocomial infections, including VAP, due to antibiotic-resistant bacteria.

Our findings are consistent with those reported from other studies2 15 17 of university-affiliated teaching hospitals. Heyland and colleagues22 found that patients with VAP had longer lengths of stay in the ICU and greater risk of hospital mortality, compared to patients without VAP. One potential explanation for these findings, as suggested by our current investigation, is that patients with VAP in a community hospital ICU have high rates of infection with antibiotic-resistant pathogens (eg, P aeruginosa, Acinetobacter spp, oxacillin-resistant S aureus). These pathogens are associated with higher rates of attributable hospital mortality.23 24 Therefore, knowledge of the local microbiology associated with VAP may allow for greater administration of adequate initial antimicrobial therapy that has been associated with reduced hospital mortality.25 26 27 28

The risk factors for patients with VAP developing in this community hospital appear to be markers for colonization of the aerodigestive tract with pathogenic bacteria and aspiration, respectively. Tracheostomy and reintubation were identified as important risk factors for the development of VAP. This suggests that aspiration during reintubation and in the presence of tracheostomy may have contributed to the development of VAP in some patients.29 30 The use of antacids in patients with VAP suggests that colonization of the stomach with pathogenic bacteria may have contributed to the occurrence of VAP.31 Sucralfate use was also associated with VAP (Table 2) . This is most likely due to the greater severity of illness among patients receiving sucralfate, compared to those not getting this agent: mean (SD) APACHE II scores, 25.0 (7.4) vs 23.6 (6.7); p = 0.030. Interestingly, multiple venous catheter insertions were also found to be an independent risk factor for VAP in this cohort. This may be a surrogate marker for either severity of illness or prolonged length of stay in the ICU predisposing to VAP.19

Our study has several limitations. First, our patient population may not be similar to those at other community hospitals. Therefore, our results may not be applicable to ICUs with lower rates of VAP due to P aeruginosa and S aureus. However, P aeruginosa and S aureus are reported by the Centers for Disease Control and Prevention to be the most common pathogens associated with VAP among hospitals in the United States.6 Variability in the pathogens associated with VAP among different hospitals has also been demonstrated to occur.5 This suggests that hospitals need to identify the bacterial pathogens associated with hospital-acquired infections locally in order to optimize antibiotic utilization. Second, we used a clinical diagnosis of VAP that could be established at the bedside without requiring invasive diagnostic procedures. Although some authors11 have warned that the incidence of VAP may be overestimated when clinical criteria alone are used, the observed incidence of VAP in our study was similar to that reported by other investigators32 employing bronchoscopic methods for the diagnosis of VAP. Ruiz and coworkers33 have also demonstrated that the outcome of VAP does not appear to be influenced by the technique used for microbial investigation. However, these investigators used quantitative cultures of tracheobronchial aspirates to define VAP that we did not employ.

It appears that the adequacy of the initial antimicrobial treatment for VAP may be the most important determinant of clinical outcomes.25 26 27 28 Therefore, the effectiveness of antibiotic treatment for VAP should be examined in future studies evaluating the influence of hospital-acquired pneumonia on mortality. We did not examine antibiotic use patterns in this study and cannot assess the role of antibiotic therapy on clinical outcomes or prior antibiotic administration as a risk factor for VAP. Additionally, we did not examine severity of illness throughout the duration of mechanical ventilation as a potential risk factor for VAP. Finally, our subgroup analyses may not have the power to identify all important risk factors for VAP in this patient population.

Despite the above-noted limitations, our data suggest that the risk factors for VAP and mortality in a community hospital are similar to those identified from university-affiliated hospitals. These risk factors can be employed to develop local strategies for the prevention of VAP in the community hospital setting. Our findings also highlight the importance of assessing the magnitude of the occurrence of nosocomial infections at a given institution. Combined with the knowledge of the causative pathogens, more effective strategies can be potentially developed for the prevention and treatment of VAP. Additionally, other studies describing the medical practices within community hospitals, especially compared to academic medical centers, are needed. This is especially true in our current medical-care environment where market forces, consolidation of hospitals and medical practices, and the incorporation of many hospitals into profit-based systems may influence medical practices more so than their academic affiliation.


   Acknowledgements
 
The authors thank the members of the infection control team at Missouri Baptist Hospital for their assistance in collecting the data for this investigation.


   Footnotes
 
Abbreviations: AOR = adjusted odds ratio; APACHE = acute physiology and chronic health evaluation; CI = confidence interval; FIO2 = fraction of inspired oxygen; VAP = ventilator-associated pneumonia

This investigation was supported in part by grants from the Centers for Disease Control and Prevention (UR8/CCU715087).

Received for publication June 27, 2000. Accepted for publication January 10, 2001.


   References
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 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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