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* From the Pulmonary and Critical Care Division (Drs. Iregui and Kollef, and Ms. Ward), and Division of Infectious Disease (Dr. Fraser), Department of Internal Medicine, Washington University School of Medicine; and Department of Nursing (Ms. Sherman), Barnes-Jewish Hospital, St. Louis, MO.
Correspondence to: Marin H. Kollef, MD, FCCP, Washington University School of Medicine, Campus Box 8052, 660 South Euclid Ave, St. Louis, MO 63110; e-mail: kollefm{at}msnotes.wustl.edu
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Abstract |
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Setting: Medical ICU of Barnes-Jewish Hospital, St. Louis, a university-affiliated urban teaching hospital.
Patients: One hundred seven consecutive patients receiving mechanical ventilation and antibiotic treatment for VAP.
Interventions: Prospective patient surveillance and data collection.
Measurements and results: All 107 patients eventually received treatment with an antibiotic regimen that was shown in vitro to be active against the bacterial pathogens isolated from their respiratory secretions. Thirty-three patients (30.8%) received antibiotic treatment that was delayed for 
24 h after initially meeting diagnostic criteria for VAP. These patients were classified as receiving IDAAT. The most common reason for the administration of IDAAT was a delay in writing the antibiotic orders (n = 25; 75.8%). The mean time (± SD) interval from initially meeting the diagnostic criteria for VAP until the administration of antibiotic treatment was 28.6 ± 5.8 h among patients classified as receiving IDAAT, compared to 12.5 ± 4.2 h for all other patients (p < 0.001). Forty-four patients (41.1%) with VAP died during their hospitalization. Increasing APACHE (acute physiology and chronic health evaluation) II scores (adjusted odds ratio, 1.13; 95% confidence interval, 1.09 to 1.18; p < 0.001), presence of malignancy (adjusted odds ratio, 3.20; 95% confidence interval, 1.79 to 5.71; p = 0.044), and the administration of IDAAT (adjusted odds ratio, 7.68; 95% confidence interval, 4.50 to 13.09; p < 0.001) were identified as risk factors independently associated with hospital mortality by logistic regression analysis.
Conclusion: These data suggest that patients classified as receiving IDAAT are at greater risk for hospital mortality. Clinicians should avoid delaying the administration of appropriate antibiotic treatment to patients with VAP in order to minimize their risk of mortality.
Key Words: antibiotics • intensive care • mechanical ventilation • outcomes • pneumonia • resistance
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Introduction |
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Materials and Methods |
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Study Design and Data Collection
A prospective cohort study design was used. The primary outcome examined was hospital mortality. The secondary outcomes included the duration of mechanical ventilation, hospital and ICU lengths of stay, mortality attributed to VAP, and disposition following hospitalization for survivors.
For all study patients, the following characteristics were prospectively recorded by one of the investigators: age; gender; race; indication for mechanical ventilation; health insurance status; premorbid lifestyle scores8 ; severity of illness based on APACHE (acute physiology and chronic health evaluation) II scores9 ; the presence of COPD, congestive heart failure, or underlying malignancy; administration of vasopressors; bacteremia; placement of a tracheostomy; and disposition following hospital discharge. One of the investigators made daily rounds in the ICU to identify eligible patients and to determine the onset of VAP based on the diagnostic criteria described below. As this was strictly an observational study, the investigators did not interact with the ICU treating physicians regarding the diagnosis or management of VAP. Patients entered into the study were prospectively followed up until they were successfully weaned from mechanical ventilation, were discharged from the hospital, died, or were transferred to a long-term care facility.
Definitions
All definitions were selected prospectively as part of the original study design. The premorbid lifestyle score was used as previously defined8
: 1 = patient was independent, fully ambulatory, and not employed with restriction; 2 = patient had restricted activities, could live alone and get out of the house to do basic necessities, or had severely limited exercise ability; 3 = patient was house-bound, could not get out of the house unassisted, could not live alone, or could not do heavy chores; and 4 = patient was bed-bound or chair-bound. We calculated APACHE II scores using clinical data available from the first 24-h period of intensive care.9
Hospital mortality was defined as those patient deaths occurring during the initial hospital admission during which they were studied.
The diagnostic criteria for VAP used in this study were modified from those established by the American College of Chest Physicians.10
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 findings 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 per liter. Tracheal aspirates were considered purulent if abundant neutrophils were present per high power field using Gram stain (ie, > 25 neutrophils per high power field). Tracheal aspirate or BAL cultures were routinely obtained at the time the diagnosis of VAP was being considered.
VAP complicating community-acquired pneumonia was considered to be present if a new infiltrate developed at least 48 h after the start of mechanical ventilation and empiric antibiotic treatment for community-acquired pneumonia. The previous infiltrates, attributed to the community-acquired pneumonia, were also required to be stable or improving in their radiographic appearance for at least 48 h prior to the development of the new infiltrate(s). Lastly, the criteria for VAP noted above also had to be met. All patients were also screened prospectively for possible alternative causes for fever and radiographic chest densities as suggested by other investigators.11 Mortality directly related to VAP was predetermined to be present when a patient died during an episode of VAP and the death could not be directly attributed to any other cause.
The administration of IDAAT was arbitrarily defined as a time period of 24 h between the point at which the diagnostic criteria for VAP were first documented, including the first identification of a new radiographic infiltrate, and the subsequent administration of appropriate antibiotic treatment. This was based on several studies2
3
suggesting that short delays in the administration of effective antibiotic treatment could increase mortality for patients with VAP. The timing of antibiotic administration was determined from the bedside computerized nursing records. Appropriate antibiotic therapy included the administration of at least one antibiotic with in vitro activity against the bacterial pathogens isolated from the patient’s respiratory secretions, as well as from blood and pleural fluid when applicable.
Antibiotic Treatment for VAP
Antibiotic therapy for VAP was based on our prior experience identifying the most common bacterial pathogens associated with VAP in the medical ICU.1
6
12
All patients with suspected VAP had cultures obtained (blood, tracheal aspirate, or BAL) before antibiotic administration. Antibiotic administration included initial treatment for methicillin-resistant Staphylococcus aureus with vancomycin and Pseudomonas aeruginosa with at least one of the following antibiotics: ciprofloxacin, imipenem, cefepime, or pipercillin-tazobactam. Initial combination antibiotic treatment for P aeruginosa and the total duration of antibiotic administration were left to the discretion of the patients’ treating physicians. The presence of VAP due to antibiotic-resistant bacteria was prospectively defined as Gram-negative bacteria resistant to the prescribed antibiotic(s) for this class of bacteria and VAP due to Gram-positive bacteria resistant to vancomycin.
Statistical Analysis
All comparisons were unpaired, and all tests of significance were two tailed. Continuous variables were compared using the Student’s t test for normally distributed variables and the Wilcoxon rank-sum test for nonnormally distributed variables. The 
2 test was used to compare categorical variables. The primary data analysis compared patients receiving IDAAT to all other patients in the cohort. A second data analysis compared patients who died during their hospitalization to those who survived. A logistic regression model was used to control for the effects of confounding variables in order to determine the relationship between hospital mortality (dependent variable) and IDAAT (independent variable).13
14
A stepwise approach was used to enter new terms into the logistic regression model, where 0.05 was set as the limit for the acceptance or removal of new terms. Variables entered into the logistic regression model were required a priori to have a plausible biological relationship to the dependent outcome variable in order to avoid spurious associations.15
Model overfitting was examined 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 independent variables was included in our analyses.14
15
Results of the logistic regression analysis are reported as adjusted odds ratios with 95% confidence intervals. Values are expressed as the mean ± SD (continuous variables), or as a percentage of the group from which they were derived (categorical variables). All p values were two tailed, and p 
0.05 indicated statistical significance.
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Results |
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Antibiotic Treatment of VAP
All patients were eventually treated with an appropriate antibiotic regimen that was active against the bacteria isolated from their respiratory secretions. Cultures of respiratory secretions identified at least one bacterial pathogen in all patients. Sixty-four patients (59.8%) had tracheal aspirate specimens alone, and 43 patients (40.2%) underwent bronchoscopically guided BAL to obtain cultures. The bacterial pathogens isolated from respiratory secretions included P aeruginosa (n = 39), methicillin-resistant S aureus (n = 24), methicillin-sensitive S aureus (n = 11), Acinetobacter species (n = 9), Enterobacter species (n = 6), and other Gram-negative bacterial species (n = 24). Six patients (5.6%) had two bacterial species isolated from their respiratory secretions. Twelve patients (11.2%) received new antibiotics within 72 h of meeting criteria for the diagnosis of VAP.
Thirty-three patients (30.8%) received antibiotic treatment that was delayed for 24 h after first meeting the diagnostic criteria for VAP and were classified as receiving IDAAT. The reasons accounting for the delays in the administration of appropriate antibiotic treatment included the presence of a bacterial species resistant to the initially prescribed antibiotic regimen (n = 6), delays in writing antibiotic orders (n = 25), and delays in the administration of antibiotics after the initial order was written (n = 2). The bacteria resistant to the initially prescribed antibiotic regimen included P aeruginosa (n = 3), Acinetobacter species (n = 2), and Enterobacter species (n = 1). The mean duration of time from when patients initially met the diagnostic criteria for VAP until the administration of antibiotics was 28.6 ± 5.8 h among patients classified as receiving IDAAT, compared to 12.5 ± 4.2 h for all other patients (p < 0.001; Fig 1
). IDAAT attributed to the isolation of a bacterial species resistant to the initially prescribed antibiotic regimen was associated with a significantly longer duration of delay compared to the other two reasons for classification as IDAAT (37.2 ± 7.7 h vs 26.7 ± 3.2 h; p = 0.019). Patients receiving IDAAT had a statistically shorter stay in the hospital prior to the development of VAP compared to patients not receiving IDAAT (Table 1
).
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Discussion |
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This investigation confirms the results of previous VAP studies demonstrating an association between the administration of appropriate antibiotic treatment and clinical outcome. Alvarez-Lerma3 showed that among 490 episodes of pneumonia acquired in the ICU setting, 214 episodes (43.7%) required modification of the initial antibiotic regimen due to either isolation of a resistant microorganism (62.1%) or lack of clinical response to therapy (36.0%). Attributable mortality from VAP was significantly lower among patients receiving initial appropriate antibiotic treatment compared to patients receiving inappropriate treatment (16.2% vs 24.7%; p = 0.034). Similarly, other investigators2 4 5 6 7 have demonstrated increased hospital mortality among patients with VAP not receiving initial appropriate antibiotic treatment. Delays in the administration of appropriate antibiotic treatment for community-acquired pneumonia have also been associated with increased hospital mortality.16 17 Our investigation is unique in identifying a potentially important temporal threshold for the administration of appropriate antibiotic therapy to patients with VAP. Delays in the administration of appropriate antibiotic treatment beyond 24 h appeared to significantly increase the risk of hospital mortality.
The most common pathogens associated with the administration of inappropriate antimicrobial treatment among patients with VAP include potentially antibiotic-resistant Gram-negative bacteria (P aeruginosa, Acinetobacter species, Klebsiella pneumoniae, and Enterobacter species) and S aureus, especially strains with methicillin resistance.2 3 6 12 This differs from hospital-acquired bloodstream infections in which antibiotic-resistant Gram-positive bacteria (methicillin-resistant S aureus, vancomycin-resistant enterococci, and coagulase-negative staphylococci), Candida species, and less commonly antibiotic-resistant Gram-negative bacteria account for most cases of inappropriate antibiotic treatment.18 However, it is important to recognize that the predominant pathogens associated with hospital-acquired infections may vary between hospitals as well as among specialized units within individual hospitals.19 20 Therefore, updated hospital-specific or unit-specific antibiograms should be very helpful in determining the combination of antibiotics most likely to provide initial appropriate treatment of VAP and other hospital-acquired infections.21
Our study has several limitations. First, it was performed within a single medical ICU and the results may not be generalizable to other treatment settings. However, these findings are consistent with those observed by other investigators,2 3 4 suggesting that they may be applicable to other populations. Second, the study examined a relatively small sample size, limiting our ability to detect all possible differences among the study groups of interest. We only identified six patients in whom bacterial isolates were resistant to the initially prescribed antibiotic regimens. Therefore, we cannot determine the impact of antibiotic resistance on clinical outcomes in this study. Third, we employed clinical criteria to establish the diagnosis of VAP. This was purposefully done to study a cohort of patients that more closely reflects the population of patients with VAP in the "real world" setting. Previous studies5 22 have demonstrated that clinically diagnosed VAP is a good predictor of clinical outcomes compared to VAP diagnosed using bronchoscopically obtained quantitative cultures.
Another important limitation of this study was that we did not attempt to determine the factors influencing physician delays in writing orders for antibiotic therapy once patients met the diagnostic criteria for VAP. Potential explanations for such delays include failure of treating physicians to recognize the presence of VAP, forgetting to write orders for antibiotics, awaiting the results of diagnostic tests such as cultures, and attributing the patient’s clinical findings to a noninfectious process. Our results highlight the need for a heightened awareness of VAP among ICU clinicians. This study was an observational study not designed to prove causality between a clinical risk factor (eg, administration of IDAAT) and a specific outcome of interest (eg, hospital mortality). To validate the relationship between IDAAT and increased hospital mortality, a prospective trial randomly assigning patients to IDAAT vs appropriate antibiotic treatment administered without delay would have to be performed. Due to ethical and patient safety concerns, it is unlikely that such a study will ever be carried out. Additional large studies are also required that match patients for severity of illness to determine the attributable mortality of IDAAT, given the conflicting results of another recent smaller study.23
In summary, our study suggests that patients receiving IDAAT are at greater risk for hospital mortality compared to patients receiving appropriate antibiotic treatment within 24 h of meeting diagnostic criteria for VAP. Given the increasing rates of nosocomial infections due to antibiotic-resistant bacteria, clinicians should consider the following recommendations for the antibiotic treatment of hospital-acquired infections. Risk stratification should be employed to identify those patients at greater risk for infection due to antibiotic-resistant bacteria. These risk factors include prior antibiotic treatment, prolonged lengths of stay in the hospital, and the presence of invasive devices (eg, central venous catheters, endotracheal tubes, urinary catheters).21 24 Patients at increased risk for infection with antibiotic-resistant bacteria should be treated initially with a combination of antibiotics providing coverage for the most likely pathogens to be encountered in that specific clinical setting (Fig 2 ). Initial antibiotic treatment should also be modified once the agent of infection is identified, or antibiotic therapy should be discontinued altogether if the diagnosis of infection becomes unlikely (ie, de-escalation of antibiotic therapy).25 26 Such an approach to antibiotic therapy for VAP can be viewed as a strategy to balance the need to provide appropriate initial antibiotic treatment to high risk patients while avoiding unnecessary empiric antibiotic utilization which can further promote antibiotic resistance among potentially pathogenic bacteria.
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Footnotes |
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This work was supported in part by the Barnes-Jewish Hospital Foundation.
Received for publication October 16, 2001. Accepted for publication January 17, 2002.
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