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(Chest. 2002;121:1618-1623.)
© 2002 American College of Chest Physicians

Incidence and Outcome of Polymicrobial Ventilator-Associated Pneumonia*

Alain Combes, MD; Corinne Figliolini, MD; Jean-Louis Trouillet, MD; Najibi Kassis, MD; Michel Wolff, MD; Claude Gibert, MD and Jean Chastre, MD

* From Service de Réanimation Médicale (Drs. Combes, Trouillet, Gibert, and Chastre), Service de Réanimation Infectieuse (Drs. Figliolini and Wolff), and Service de Microbiologie (Dr. Kassis), Hôpital Bichat, AP-HP, Paris, France.

Correspondence to: Alain Combes, MD, Service de Réanimation Médicale, Institute de Cardìologie, Hopital Pitié-Salpêtrière, 47 Boulevard de l’Hôpital, 75651 Paris Cedex 13, France; e-mail: alain.combes{at}psl.ap-hop-paris.fr


   Abstract
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 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Study objective: To determine the epidemiology and outcome of polymicrobial ventilator-associated pneumonia (VAP).

Setting: Two ICUs (18 and 17 beds) in a university hospital.

Design and patients: We undertook a 16-month study of 124 patients in whom a first episode of VAP had been diagnosed. Patients in whom there was a suspicion of clinical or radiologic VAP underwent bronchoscopy, and VAP was confirmed by the presence of at least two of the following criteria: >= 2% of cells with intracellular bacteria found on direct examination of BAL fluid (BALF); protected-specimen brush sample culture with >= 103 cfu/mL; or BALF culture with >= 104 cfu/mL.

Results: Monomicrobial infections were diagnosed in 65 patients (52%), and polymicrobial infections were diagnosed in 59 patients (48%). Two different bacteria were isolated in 42 patients (34%), three different bacteria were isolated in 10 patients (8%), and four different bacteria were isolated in 7 patients (6%). Patients’ clinical characteristics at ICU admission and on the day of bronchoscopy were similar, particularly the prior duration of mechanical ventilation (MV), the type of ICU admission, disease severity scores, and antibiotic therapy received before VAP was diagnosed. The percentages of nonfermenting, Gram-negative bacilli and methicillin-resistant staphylococci involved in monomicrobial and polymicrobial episodes were similar. Furthermore, no significant difference was detected in outcome parameters, specifically in the mortality rate at 30 days, the ICU mortality rate, the duration of MV, and the rate of infection relapse.

Conclusion: In our study population, the epidemiology and outcomes of patients with monomicrobial and polymicrobial VAP did not differ significantly.

Key Words: artificial respiration • bacterial pneumonia • ICUs


   Introduction
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 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
The incidence of nosocomial ventilator-associated pneumonia (VAP) is high, ranging from 7 to > 40%.1 2 These infections prolong the need for mechanical ventilation (MV) and the length of the hospital stay, contribute to patient mortality and, consequently, are responsible for markedly increased costs.1 2 3 4 5 6 7 The types of causative microorganisms depend mainly on the duration of MV and prior antibiotic use, particularly broad-spectrum antibiotics.8 After prolonged MV and the extensive use of

antibiotics, potentially drug-resistant bacteria become prominent causes of VAP8 and are associated with significantly poorer prognoses.9

In studies by our group5 6 9 and others,3 7 10 more than one microorganism causing VAP was identified in 20 to 60% of the cases. However, to date, no precise data exist regarding the demographics and clinical outcomes of patients developing polymicrobial lung infections. Therefore, to better define and compare the epidemiologic and microbial aspects of monomicrobial and polymicrobial VAP, we conducted a study with consecutive patients receiving MV for >= 48 h, in whom lung parenchyma infection had been documented based on microbiological and clinical findings.


   Materials and Methods
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 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
This study was conducted from January 1997 to June 1998 in two ICUs having 18 and 17 beds. The protocol was designed in accordance with the ethical standards of the Committee for the Protection of Human Subjects of Hôpital Bichat. No informed consent was obtained, given that this epidemiologic study did not modify existing diagnostic or therapeutic strategies.

Patients
All consecutive patients meeting the following criteria were entered into the study: requirement of MV for >= 48 h; a new and persistent (ie, for > 24 h) infiltrate was observed on a chest radiograph; presence of macroscopically purulent tracheal aspirates; clinical status permitting fiberoptic bronchoscopy; and presence of a case of VAP that had been documented by the microbiological processing of samples from a protected-specimen brush (PSB) and BAL fluid (BALF).11 In addition, only the first episode of VAP was considered in the analysis. Finally, for the selection of the initial empiric antibiotic therapy, we used an algorithm that was based on the duration of MV (ie, > 7 days or < 7 days), and the presence or absence of prior antibiotic therapy,8 and we also took into account the results of the direct examination of BALF.

Specimen Collection and Microbiological Processing
Patients suspected of having VAP underwent fiberoptic bronchoscopy,5 and the microbiological specimens were processed as previously described.11 Both Gram and Wright stains were used for cytocentrifuge preparations. Patients were considered to have VAP when at least two of the following criteria were present: >= 2% of the cells in the cytocentrifuge preparations from BALF contained intracellular bacteria; or at least one bacterial species grew at a significant concentration from the PSB sample (ie, >= 103 cfu/mL) or from the BALF sample (ie, >= 104 cfu/mL).11

Data Collection and Outcome Measures
Each patient’s hospital chart was constituted prospectively, and the following data were recorded: age; sex; severity of underlying medical condition, stratified according to the criteria of McCabe and Jackson12 ; primary ICU admission diagnostic category; simplified acute physiology score (SAPS) II13 ; Glasgow coma scale score; presence or absence of infection; presence or absence of organ dysfunction (ie, ODIN score)14 ; presence or absence of sepsis, severe sepsis, or septic shock15 ; and sepsis-related organ failure assessment score.16 All these parameters were recorded within the 24 h following the patient’s admission to the ICU, with the worst value for each variable being retained.

In addition, the following parameters were recorded on the day of bronchoscopy (day 0): days receiving MV; temperature; WBC count; PaO2/fraction of inspired oxygen (FIO2) ratio; radiologic score17 ; and the presence or absence of any antimicrobial agents for > 24 h during the 15 days preceding the episode. Furthermore, the administration of any the following classes of antibiotics during the 15 days preceding the event was recorded: imipenem; third-generation cephalosporins; aminoglycoside; fluoroquinolone; and/or other antibiotics (as defined by exclusion). Broad-spectrum antibiotics (eg, imipenem, third-generation cephalosporins, and fluoroquinolone) were regrouped to constitute a new parameter.

Outcome measures included the following: 30-day and ICU mortality rates; duration of MV; MV-free days counted 30 days after the VAP onset; duration of ICU stay; percentage of patients who relapsed; the evolution of clinical parameters; and composite scores from the day of ICU admission to days 0, 1, 3, 7, and 14.

Statistical Analysis
Clinical and laboratory data were statistically analyzed with the Student’s t test for the comparison of continuous variables, or by the {chi}2 test or Fisher’s Exact Test for the comparison of percentages. We did not use the correction for multiple comparisons. Time-to-event variables were estimated according to the Kaplan-Meier method and were compared by means of the log-rank test. Statistical significance was defined as p < 0.05.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Study Population
Among the 124 patients for whom a diagnosis of VAP had been documented, 65 (52%) had monomicrobial infections and 59 (48%) had at least two bacteria isolated at significant concentrations from pulmonary specimens. Of the latter patients, 42 (34%) had two bacteria present, 10 (8%) had three bacteria present, and 7 (6%) had four bacteria present. The clinical characteristics of patients at ICU admission and on the day of bronchoscopy are listed in Tables 1 and 2 , respectively. A high percentage of patients had the following signs of severe illness at ICU admission: > 50% of patients had a preexisting, rapidly fatal, or ultimately fatal disease; about 40% of patients had severe sepsis or septic shock; and patients had an average of three failing organs. As indicated, no statistical differences between the two groups were noted for baseline values, particularly etiologic factors of VAP. Similarly, the prescription of antibiotics (ie, imipenem, third-generation cephalosporins, fluoroquinolones, aminoglycosides, and vancomycin) prior to acquiring VAP did not differ significantly between the two groups of patients. Finally, there was no statistical difference in the frequency of infection type according to the time of occurrence (18 patients [28%] had early-onset [ie, at <= 5 days] monomicrobial infections and 18 patients [31%] had early-onset polymicrobial infections).


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  		Table 1. ICU Admission Clinical Characteristics of 124 Patients Who Were Prospectively Studied for Development of VAP*

 

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  		Table 2. Clinical Characteristics of Patients on the Day of Bronchoscopy*

 
Microbiological Findings
A total of 207 bacteria were grown in cultures at significant concentrations from PSB and/or BALF samples for the 124 VAP episodes (Table 3 ). The microorganisms most frequently isolated from patients with monomicrobial VAP were nonfermenting, Gram-negative bacilli (NF-GNB) [ie, Pseudomonas, Acinetobacter, and Stenotrophomonas maltophilia] (44.6%), followed by methicillin-resistant Staphylococcus aureus (MRSA) [15.4%] and Streptococcus species (6.2%). In patients with polymicrobial pneumonia, streptococci (28.9%) were the microorganisms found most frequently, followed by NF-GNB (24.6%) and MRSA (12.7%). Anaerobic pathogens rarely were recovered from either population (Table 3) .


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  		Table 3. Microbiological Findings in Monomicrobial and Polymicrobial Episodes

 
Furthermore, looking at the bacteria involved in VAP episodes, NF-GNB and MRSA were isolated from 30 patients with polymicrobial VAP (50.8%) and 18 patients with polymicrobial VAP (30.5%), respectively, compared to 29 with monomicrobial VAP (44.6%) and 10 with monomicrobial VAP (15.4%), respectively (p = 0.49 and p = 0.06, respectively) [Fig 1 ]. In addition, at least one strain of antibiotic-resistant nosocomial bacteria (ie, MRSA or NF-GNB) was involved in 39 monomicrobial episodes (60%) and 39 polymicrobial episodes (66%; p = 0.48). Polymicrobial VAP was caused exclusively by cocci in 14 cases (23%), Gram-negative bacilli in 11 cases (19%), or a mixture of cocci and Gram-negative bacilli in 34 cases (58%). Streptococci, Neisseria, and/or Haemophilus species were frequently associated with antibiotic-resistant bacteria in polymicrobial episodes, and this association was only slightly higher in patients with early-onset vs late-onset polymicrobial VAP (72% vs 51%, respectively; p = 0.13).



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  		Figure 1. Distribution of microorganisms in 124 patients who developed VAP. The numbers 1 to 4 represent the number of different bacterial species recovered per patient from microbiological sample cultures GNB = Gram-negative bacilli; MSSA = methicillin-sensitive S aureus.

 
Clinical Outcomes
The day 30 and ICU mortality rates did not differ significantly between the two groups (deaths from monomicrobial infections: day 30, 23 [35%] vs ICU, 35 [54%]; deaths from polymicrobial infections: day 30, 15 [25%] vs ICU, 27 [46%]) [Table 4 ]. In addition, there were no statistically significant differences between groups for the duration of MV, MV-free days at day 30, length of post-VAP ICU and hospital stays, and the frequency of and time to relapse (Table 4) . Furthermore, no statistical difference was noted for the probability of survival or of continuing to require MV between day 0 and day 30.


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  		Table 4. Outcome Parameters of Monomicrobial and Polymicrobial VAP Episodes*

 
Finally, the evolution of temperature, PaO2/FIO2 ratio, WBC count, pH, and radiologic, lung injury, and disease severity scores from days 1 to 14 did not differ for the two groups among those patients who were still alive at each time point.


   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
To ascertain the epidemiologic and microbial etiologic aspects of polymicrobial VAP, we undertook a study of patients who required MV for >= 48 h and for whom strict bronchoscopic criteria were applied to diagnose pneumonia. Of the 124 consecutive VAP episodes studied, only one bacterial strain was isolated from the microbiological samples of 65 patients, compared to the two, three, and four different strains isolated from 42, 10, and 7 patients, respectively. Our results indicate that the patients’ clinical characteristics at ICU admission and on the day of bronchoscopy were not statistically different, particularly the duration of MV, the type of ICU admission, disease severity scores, and the antibiotic therapy received before acquiring VAP. The percentages of NF-GNB (particularly Pseudomonas aeruginosa) or MRSA involved in monomicrobial and polymicrobial episodes were not statistically different. Finally, no significant differences could be established for outcome parameters, specifically 30-day and ICU mortality rates, the duration of MV, and the percentage of patients who relapsed.

To the best of our knowledge, this is the first study to date to prospectively evaluate the characteristics and outcomes of patients with polymicrobial VAP. The frequency of such infections varies widely. Among 684 patients undergoing heart surgery, 45 (6.5%) developed VAP, with 6 patients (13.3%) having polymicrobial VAP.18 However, most patients in that study had received MV for < 48 h and developed VAP only when MV was prolonged. The 48% infection rate reported herein is in agreement with previous data from medical and surgical ICU patients, 40 to 62% of whom developed polymicrobial infections.3 5 6 8 10 14

The presence of the bacteria responsible for a case of pneumonia in patients receiving MV depends on the time of infection occurrence. The aspiration of oropharyngeal flora results in early infection soon after endotracheal intubation. Cases of VAP are often polymicrobial, and streptococci, Neisseria, and Haemophilus species are commonly isolated in high titers.3 After more prolonged durations of MV, the frequency of polymicrobial infection is thought to be much lower, and staphylococci and enteric Gram-negative rods usually are isolated from lung samples.6 7 19 However, in this study, we did not detect any statistically significant difference between the rates of polymicrobial infection according to the time of occurrence. Indeed, the duration of MV and the length of the hospital stay prior to acquiring VAP were longer for patients with polymicrobial VAP, although this was not statistically significant. Furthermore, microorganisms, such as streptococci, Neisseria, and Haemophilus species, that were found in patients with early-onset infections were also frequently involved in late-onset infections and were associated with antibiotic-resistant bacteria in this setting.

To the best of our knowledge, few data are available in the literature regarding outcome parameters for patients with nosocomial polymicrobial VAP. In a study of bacteremic nosocomial pneumonia, Bryan and Reynolds20 did not detect any difference in mortality rate between monomicrobial and polymicrobial episodes (57% vs 68%, respectively). We also did not find any significant between-group differences for the main outcome parameters that were evaluated. The 30-day mortality rate was 35% for patients with monomicrobial episodes and 25% for patients with polymicrobial episodes, which are values that are within the ranges previously observed by our group5 21 and by others3 7 18 with similar case mixes.

One factor that is potentially associated with a more severe outcome for patients with polymicrobial infections would be the inappropriateness of initial antibiotic therapy, with some bacterial species escaping the spectrum of initial empiric therapy. But, despite a lower percentage of appropriateness for the initial antibiotic therapy in the polymicrobial group (75% vs 92%, respectively), the mortality rate was not statistically different for the two groups that we analyzed. However, drug-resistant bacteria, such as MRSA or NF-GNB, are clearly associated with poorer prognoses2 9 and higher frequencies of relapse, and these bacteria were frequently isolated from patients in both groups (in approximately two thirds of the episodes). Thus, one of the most valuable prognostic factors in this setting is probably the type of bacterium rather than the number of pathogens isolated in a particular episode.

The results obtained in this study may be tempered by several limitations. First, our study was conducted in two ICUs in a large university hospital (ie, > 1,200 beds). Very frequently, patients who are treated in our institution come from another ICU, are receiving MV at ICU admission, and have already been treated with antibiotics, thereby increasing the likelihood of VAP due to highly resistant nosocomial bacteria. The use of broad-spectrum initial empiric antibiotic therapy that covers most microorganisms in these patients may partly explain the lack of difference observed in the outcome parameters. Furthermore, at ICU admission, approximately 60% of the patients had an underlying disease (McCabe score, >= 2), 40% of the patients presented with signs of severe sepsis or septic shock, and patients had an average of three dysfunctional organs that were failing (ODIN score). Thus, our results may not be applicable to patients hospitalized in a non-tertiary-care hospital.

Second, it can be argued on the basis of animal studies that most cases of VAP are in fact polymicrobial. In baboons who were mechanically ventilated for 7 to 10 days, Johanson and coworkers22 demonstrated that polymicrobial VAP developed in 100% of the cases. However, the absence of prior antibiotic therapy could account for the results obtained in their study. In addition, Marquette and coworkers23 showed that, after 4 days of MV, 94% of healthy, ventilated piglets had VAP. However, when animals had received ceftriaxone prophylaxis, VAP was diagnosed histologically in only 44%. Among these infections, 94% in the control group and 25% in the antibiotic group were polymicrobial. Therefore, antibiotic therapy prior to VAP onset seems to be associated with dramatically fewer polymicrobial infections. Actually, Rouby and coworkers10 showed that, in critically ill patients who died after receiving prolonged MV and had frequently been treated with antibiotic drugs, only 43% of cases of bronchopneumonia were histologically polymicrobial. Indeed, our observations are in keeping with that finding.

Third, we may have missed a certain percentage of infections using bronchoscopic techniques for the diagnosis of VAP. However, in this study, we applied a strict diagnostic protocol, combining the microbiological results obtained with PSB and BALF samples obtained by bronchoscopy, which we previously had shown was able to correctly identify lung segments yielding >= 104 organisms per gram in 91% of the cases, and histopathologic findings.11

It may also be argued that bacteria originating from the skin or oropharynx, such as streptococci, Neisseria, Enterobacteriaceae, and coagulase-negative Staphylococcus have low pathogenicity and are sometimes contaminants. That we11 and others10 have recovered these types of pathogens from the lung biopsy specimens of patients receiving MV decreases the likelihood that the tissues had been contaminated. In addition, if these bacteria are excluded from the analysis, epidemiologic characteristics (ie, age, disease severity scores, duration of prior MV, rate of early-onset VAP, and types of antibiotics prescribed) and outcome parameters (ie, day 30 and ICU mortality rates, and VAP relapse rate) remain similar for the monomicrobial and polymicrobial groups (data not shown).

Finally, we cannot exclude the possibility of a type II error in accepting the null hypothesis. Some trends observed in this study (for example, a slightly higher mortality rate in the monomicrobial group, differences between groups in the duration of MV or the antibiotics administered in the 24 h prior to VAP onset) could have reached statistical significance if the study sample size had been larger.

In conclusion, the findings of this study indicate that microbiological cultures of bronchoscopic PSB or BALF samples yield more than one bacteria for approximately 50% of patients receiving MV for > 48 h. For the population studied, the patient demographics and clinical parameters at ICU admission and at VAP onset did not differ significantly for the two groups. When the distribution pattern of the microorganisms isolated was examined, we noted a relatively high percentage of antibiotic-resistant bacteria (ie, MRSA or NF-GNB) involved in monomicrobial and polymicrobial infections. Finally, we demonstrated that the main outcome parameters (ie, ICU and hospital mortality rates, duration of MV, and the percentage of relapses) did not differ significantly for patients with monomicrobial and polymicrobial VAP.


   Footnotes
 
Abbreviations: BALF = BAL fluid; FIO2 = fraction of inspired oxygen; MRSA = methicillin-resistant Staphylococcus aureus; MV = mechanical ventilation; NF-GNB = nonfermenting Gram-negative bacilli; ODIN = organ dysfunctions and/or infection; PSB = protected-specimen brush; SAPS = simplified acute physiology score; VAP = ventilator-associated pneumonia

Received for publication May 1, 2001. Accepted for publication October 30, 2001.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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