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(Chest. 2005;128:273-279.)
© 2005 American College of Chest Physicians

Respiratory Microbiology Patterns Within the First 24 h of ARDS Diagnosis*

Influence on Outcome

Torsten T. Bauer, MD; Mauricio Valencia, MD; Joan R. Badia, MD; Santiago Ewig, MD, FCCP; Julià González, MD; Miguel Ferrer, MD and Antoni Torres, MD, FCCP

* From Institut de Pneumologia i Cirugía Toracica (Drs. Bauer, Valencia, Badia, Ewig, Ferrer, and Torres), Servei de Microbiologia (Dr. González), Hospital Clinic, Institut de Investigacions Biomédique August PiISunyer, Universitat de Barcelona, Barcelona, Spain.

Correspondence to: Antoni Torres, MD, FCCP, Hospital Clìnic de Barcelona, Servei de Pneumologia i Cirogía Toracica, Villarroel 170, 08036 Barcelona, Spain; e-mail: atorres{at}medicina.ub.es


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Background: Airway colonization and infection are frequent complications during the course of ARDS. The impact on outcomes of microbiological patterns recovered within the first 24 h after diagnosis has not been evaluated.

Objectives: To describe the incidence and patterns of bronchial colonization and lung infection within the first 24 h of ARDS diagnosis and to evaluate the influence on ICU outcomes.

Methods: Prospective study of ARDS patients evaluated within 24 h of diagnosis. Patients were studied with tracheobronchial aspirate and right and left bronchoscopic protected specimen brush. All samples were cultured quantitatively.

Results: Fifty-five consecutive patients were included. Twelve patients (22%) were clinically suspected of having nosocomial pneumonia (NP), which was confirmed microbiologically in 7 patients, a frequency of 13%. In those patients without suspected pneumonia, we also found potentially pathogenic microorganisms (PPMs) and potentially drug-resistant microorganisms (PDRMs) in 36% and 31%, respectively. Mortality was not significantly higher in those patients with recovery of a PPM (87% vs 73%, p = 0.31), PDRM (89% vs 74%, p = 0.18), or with NP (79% vs 85%, p = 1.0).

Conclusion: There is a strikingly high rate of PPM recovery in early ARDS. However, neither isolation of pathogenic microorganisms nor the confirmation of NP could be associated with an increased mortality.

Key Words: ARDS • colonization • nosocomial pneumonia • pulmonary infiltrates


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Pneumonia and ARDS are closely linked. Pneumonia is a common cause of direct lung injury, causing ARDS in approximately 31% of patients,1 and the course of ARDS is frequently complicated by nosocomial pneumonia (NP). At autopsy, patients who die from ARDS frequently show a pulmonary infection that had not been recognized previously.23 The diagnosis of ventilator-associated pneumonia (VAP) on the course of ARDS is complex because the clinical criteria of VAP (fever, leukocytosis, purulent sputum, or infiltrates) are almost always present in patients with ARDS.4

The impact of NP on the outcome of patients receiving mechanical ventilation also remains controversial.5 It has been demonstrated that infection worsens hypoxemia and can cause sepsis, multiple-organ dysfunction, and death. The impact of VAP or lower respiratory tract colonization on the outcome of ARDS patients has been assessed in several trials,6789 which found that pulmonary infection affects between 34% and > 70% of patients with ARDS. Data on the influence of VAP or lower respiratory tract colonization on mortality and other important clinical outcomes of ARDS patients are also conflictive. Previous studies have some limitations: they have been carried out with different diagnostic methods,10 and ongoing antibiotic treatment is an unavoidable confounding factor.7 No studies have assessed the impact of VAP or isolation of pathogenic microorganisms from lower airways in the first 24 h on the outcomes of ARDS patients. Therefore, we carried out this study to describe the impact of bronchial colonization and lung infection within the first 24 h on the outcome of patients with ARDS.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Study Population
This study was conducted in Hospital Clinic, a 1,000-bed, university, tertiary care hospital. Consecutive patients with ARDS were identified prospectively during 1 year and followed up until death or weaning. The criteria for the diagnosis of ARDS and the inclusion in the study were as follows: (1) meeting the diagnostic criteria according the American-European Consensus Conference,11 (2) a lung injury score according to Murray et al12 ≥ 2.5, and (3) admission to hospital ≥ 48 h prior to the onset of ARDS. Patients with positive serology for HIV and patients with cerebral injury were excluded. The study was approved by the ethical committee and conducted in accordance with its guidelines. In all cases, informed consent was obtained from the next of kin.

Data Collection
All data were retrieved on the day of diagnosis of ARDS. Demographic characteristics (age, gender, history) were recorded, and clinical data (vital signs and laboratory results) were used to calculate clinical evaluation scores (APACHE [acute physiology and chronic health evaluation] II, multiple system organ failure score).1314 Pulmonary physiologic data (arterial blood gases, ventilator settings, compliance, and pulmonary artery wedge pressure) and antimicrobial treatment were also recorded. Antimicrobial therapy was considered to be adequate if the recovered potentially pathogenic microorganism (PPM) was susceptible to the drug administered empirically.

Sampling Procedure
All studies were performed within 24 h after inclusion in the study. First, a tracheobronchial aspirate (TBAS) was collected without prior administration of saline solution in a standard sputum trap (Proclinics; Barcelona, Spain). Thereafter, a fiberoptic bronchoscopic examination was performed (Pentax FB18; Asahi Optical Ltd; Japan). Patients were premedicated with IV propofol or midazolam. An endotracheal tube adapter was used in order to allow mechanical ventilation. Fraction of inspired oxygen (FIO2) was increased to 100% prior to the procedure, and ventilator support was adjusted in order to maintain minute ventilation. No local anesthetics were administered, and suction was carefully avoided throughout the procedure. Protected specimen brush (PSB) [Microbiology brush; Mill-Rose Inc.; Mentor, OH] samples were retrieved bilaterally as described by Wimberley et al15 in the most prominently affected areas on chest radiography or in one segment of the lower lobes in cases with diffuse infiltrates.

Microbiological Investigations
All samples were processed within 30 min. Samples were quantitatively plated on blood, chocolate, Wilkins-Chalgren, and Sabouraud agar media in serial dilutions of 1:10, 1:100, and 1:1,000. If results were negative, the plates were discharged after 3 days of testing for aerobic bacteria, and after 4 weeks of testing for fungi. If positive, results were expressed as colony-forming units per milliliter. Identification as well as susceptibility testing was performed using standard methods.16 For purposes of analysis, only PPMs were taken into account. The following microorganisms were considered as non-PPMs and excluded: Streptococci spp. except Streptococcus pneumoniae, coagulase-negative Staphylococci, Neisseriae spp., Corynebacteriae spp. and Candida spp. For purposes of analysis, Pseudomonas aeruginosa, Acinetobacter spp, Enterobacter spp, Stenotrophomonas maltophilia and methicillin-resistant Staphylococcus aureus were grouped as potentially drug-resistant microorganisms (PDRMs).17

Definition of Pneumonia
Clinical Suspicion of NP:
Since the presence of pulmonary infiltrates is misleading in patients with ARDS, clinical suspicion of NP was defined by a clinical pulmonary infection score (CPIS) > 6.18

Microbiologically Confirmed NP:
This is defined as the clinical suspicion of NP and bacterial growth of a PPM in quantitative cultures above the defined threshold in at least one of the samples of lower respiratory secretions (TBAS: ≥ 105 cfu/mL; PSB: ≥ 103 cfu/mL).

Frequency of NP in Patients With ARDS:
This is defined as the number of patients with microbiologically confirmed NP over all included patients.

Statistical Analysis
Data are reported as No. or mean ± SD. Frequencies were compared with {chi}2 test or Fisher Exact Test (expected cell frequency < 5) and means by unpaired Student t test. {kappa} statistics were employed for this comparison in order to correct agreements made by chance ({kappa} = {kappa} coefficient, and p values are reported). All data were processed using software (SPSS 10.0 for Windows; SPSS; Chicago, IL). The level of significance was set at 5% (all two-tailed).


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Patients
The study included 55 patients. The clinical and demographic characteristics of this population are shown in Table 1 . The primary diagnoses for ICU admission were respiratory failure (n = 16), shock (n = 12), after abdominal surgery (n = 11), after cardiac surgery (n = 5), after thoracic surgery (n = 3), coma (n = 5), and other reasons (n = 3). All patients with pneumonia and 77% of the patients without pneumonia had received ventilation for > 48 h prior to the diagnosis of ARDS. There was a significant lower pH at entry in the study between the groups (7.30 in the pneumonia group vs 7.35 in the no-pneumonia group, p = 0.01). The parameters of respiratory mechanics and oxygenation did not show any differences.


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  		Table 1. Initial Characteristics of the Study Patients (n = 55)*

 
Diagnostic Tools
TBAS samples were obtained in 84% of the patients. Six patients could not tolerate a fiberoptic investigation; samples of right PSB were available in 49 of 55 patients (89%). Thirty-three patients also tolerated a left PSB (33 of 55 patients, 60%). A total of 58% of patients were investigated with all three techniques. There was a significant higher recovery of PPMs above the threshold with TBAS when compared to right, left, and bilateral PSB (37%, 16%, 25%, and 25%, respectively; p < 0.01). However, the recovery of PDRMs above the threshold was almost equal between the three techniques (19%, 12%, 12%, and 22%, respectively; p > 0.1). The quantitative concordance of TBAS with unilateral and bilateral PSB was only moderate ({kappa} = 0.43 to 0.46). Quantitative concordance of unilateral with bilateral PSB was good ({kappa} = 0.72 to 0.82). However, when right was compared to left PSB, the quantitative concordance was again only moderate ({kappa} = 0.46).

Bacteriologic Patterns
Initial results of microbiological investigations are summarized in Table 2 . P aeruginosa was the most frequent isolate in tracheobronchial aspirate and left PSB, and the second most frequent in the right PSB. Other frequent microorganisms were Escherichia coli, methicillin-resistant S aureus and Staphylococcus epidermidis. Candida spp was frequently isolated but mostly below cut-off (Table 2). Overall, 44% of patients had at least one PPM in at least one of the samples taken, and 29% of patients had a PPM above the threshold. TBAS yielded PPMs above the threshold in 24%, right PSB in 18%, and left PSB in 15% of patients.


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  		Table 2. Initial Bacteriology Within 24 h of Onset of ARDS*

 
At least one PDRM was found in 38% of patients. PDRMs above the defined threshold were recovered in 27% of patients with all techniques: 17% with TBAS, 12% with right PSB, and 12% with left PSB. Polybacterial growth (two or more PPMs) was found in 27% of patients. Significant differences were found in the mean duration of respiratory support prior to the diagnosis of ARDS between those patients with and without recovery of PPMs (8.9 ± 10.2 days vs 3.8 ± 3.9 days, p = 0.02) and PDRMs (10 ± 10.7 days vs 3.7 ± 3.7 days, p = 0.02) [Table 3 ].


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  		Table 3. Duration of Mechanical Ventilation Prior to the Onset of ARDS and Recovery of PPMs and PDRMs

 
Frequency of Clinically Suspected and Microbiologically Confirmed NP
Overall, 12 patients (22%) were clinically suspected of having NP on the first day after diagnosis of ARDS. Infection could be microbiologically confirmed in seven of them (58%). Thus, the microbiologically confirmed pneumonia rate in the first 24 h diagnosis of ARDS was 13%. All seven patients with microbiologically confirmed NP had been admitted to the hospital at least 6 days before (range, 6 to 43 days) and had received mechanical ventilation for > 48 h. All these patients had at least one isolated PPM or PDRM (E coli [n = 1], P aeruginosa [n = 4], and Stenotrophomonas spp [n = 2], Enterobacter spp [n = 1], and K pneumoniae [n = 1]), and had received prior antibiotic treatment for at least 3 days (range, 3 to 15 days). Suspected pneumonia or microbiologically confirmed pneumonia was not associated with ventilation for ≥ 48 h prior to ARDS onset.

As expected, patients with microbiologically confirmed NP had significantly higher isolation of PPMs and PDRMs than in patients without it. Conversely, among patients who were not clinically suspected of having pneumonia on the day of diagnosis of ARDS, recovery of PPMs or PDRMs was strikingly frequent.

Antimicrobial Treatment
The modification of antibiotic treatment before sampling had a strong influence on the number of positive culture findings. Antimicrobial treatment was modified within 72 h before sampling in 32 of 55 patients (58%). There was a significantly higher recovery rate of PPMs (p = 0.024) and PDRMs (p = 0.05) in patients without antibiotic changes in the previous 8 days to microbiologic sampling, compared to those without antibiotic change.

Outcome
The outcome data are shown in Table 4 . Overall mortality was 44 of 55 patients (80%), with a mean survival time of 16 ± 15 days. The mean length of ICU stay (22 ± 16 days vs 20 ± 14 days, p = 0.70), the APACHE II score on the day of ICU admission (18.3 ± 9.4 vs 22.6 ± 6.3, p = 0.08), and the multi-system organ failure score (1.0 ± 1.2 vs 0.97 ± 0.9, p = 0.95) did not show significant differences between survivors and nonsurvivors, respectively. Equally, neither the PaO2/FIO2 ratio nor the Murray score on inclusion to the study were different between survivors and nonsurvivors (p = 0.44 and 0.29, respectively).


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  		Table 4. Outcomes of Patients With vs Without Pneumonia and With vs Without Isolate of PPMs*

 
The mean ICU length of stay was not significantly different among patients with PPM and PDRM recovery. Additionally, neither the ICU length of stay nor the hospital length of stay were influenced by the diagnosis of pneumonia.

There were no differences on mean duration of mechanical ventilation between those patients with microbiologically confirmed pneumonia and those without. Similarly, the recovery of PPMs or PDRMs did not appear to influence the mean duration of mechanical ventilation for ARDS diagnosis at all.

Regarding mortality, there were no differences between patients with recovery of PPMs (87% vs 73%, p = 0.31) and PDRMs (89% vs 74%, p = 0.18). The mortality of patients with microbiologically confirmed NP was higher than patients without pneumonia; however, this comparison did not reach statistical significance (85% vs 79%, p = 1.0). Finally, the mortality in the group of patients with PPM recovery and no suspected pneumonia (nine patients) was 88%.


   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
The most important findings of the study were as follows: (1) NP in the first 24 h of ARDS was microbiologically confirmed in 13%, (2) PPMs and PDRMs were frequently isolated, and (3) an association between NP or recovery of bacterial isolation in early ARDS and a worse outcome could not be established. In this study, a combination of clinical and microbiological criteria yielded a 13% frequency of pneumonia on the day of the diagnosis of ARDS. Our data suggest that lower respiratory tract colonization or infection is probably related to the fact that patients were hospitalized for a long time and had received prior antibiotic treatment. Although there is a previous study19 that associated ARDS with defective defense mechanisms in the lung, this issue is still not fully clarified. The design of our study does not allow us to raise any conclusion in this point.

The combined approach of clinical judgment (CPIS ≥ 6) and quantitative culture results used in our study is an accepted strategy for the diagnosis of microbiologically confirmed NP, with high sensitivity and an acceptable specificity.18 Accordingly, we found PPMs in 81% and a PPM above the infectious threshold in 58% of the patients who were clinically suspected of having pneumonia (CPIS ≥ 6). Possibly, prior antimicrobial treatment has influenced these results. The majority of patients in our study received antimicrobial treatment on the day of onset of ARDS; of those, this treatment had been modified within the preceding 72 h in 58%. It has been claimed that in order to maintain a satisfactory diagnostic yield in patients receiving antimicrobial treatment, it is crucial not to introduce new antimicrobial agents within the last 24 h or 72 h.2021 In our study, when antibiotic therapy was modified in the last 8 days prior to sampling, all the diagnostic tests had significantly fewer bacterial recoveries.

Among patients without clinical suspicion of pneumonia, we found PPMs in 41% and even PDRMs in 33% of the cases. Although these figures dropped when the defined thresholds for infection were taken into account, these data are concordant with a previous study22 that shows a high colonization rate in patients with ARDS. These findings may fit with those from an immediate postmortem study from our group, where a high rate of microbiologically positive lung cultures was observed without histologic signs of pneumonia.23 It has also been demonstrated that the appearance of VAP in ARDS patients can be preceded by colonization in approximately two thirds of episodes.22

Our data on the respiratory microbiology patterns of ARDS patients raise concerns about the validity of incidence data of NP in these patients. Sutherland et al7 reported an incidence of 4% of VAP during the course of ARDS when defined by clinical and microbiological criteria, and of 15% when only microbiological criteria were used. However, other authors89 have reported a much higher incidence of pneumonia. This marked variability in results is directly attributable to differences in sampling methods, populations, and timing of sampling with respect to duration of antibiotic therapy. In our study, TBAS consistently recovered more and different microorganisms than PSB. The quantitative concordance was only moderate for all comparisons except for unilateral vs bilateral PSB. This unsatisfactory result may be partially explained by the variability inherent to all diagnostic techniques. Marquette et al24 could show that when PSB was performed repeatedly, there was a 100% qualitative concordance and a high variability in quantification leading to variations in the number of cases with pneumonia. All these findings strongly support that NP in ARDS also is a multifocal process in both lungs with the presence of several different microorganisms and/or bacterial burdens involved. This also corroborates with previous findings in a postmortem study24 of a general population with VAP. Diagnostic methods that are restricted to one unilateral lung site or to a very small sampling area (eg, PSB) may therefore recover lesser different microorganisms or lesser different quantities of microorganisms in patients with ARDS. TBAS has a high sensitivity, as it samples a larger bronchial area. Thus, it is not surprising that we obtained a better diagnostic yield with this method.

The predominance of PDRMs in patients with VAP and ARDS has been reported previously.1721 In our study, many samples showed significant growth of PDRMs. In addition, PDRMs were identified as causative agents in all but one patient with microbiologically confirmed NP. Although, these microorganisms correspond to the spectrum of late-onset VAP, only 38% of our patients received ventilation for > 5 days. This can be explained by the antimicrobial use prior to the diagnosis.

An important question arises as to whether colonization or pneumonia has a significant influence on outcomes in ARDS patients. In our study, mortality was not associated with the presence of PPMs, PDRMs, or NP during the early course of ARDS. These results in early ARDS agree with those previously published. Surprisingly, no study has been able to demonstrate an increase in mortality due to NP in patients with ARDS.78922 Delclaux et al8 showed that the occurrence of VAP did not appear to influence overall survival in a population of ARDS patients: 78% patients acquiring VAP died, compared with 92% patients without VAP. Chastre et al9 and Markowicz et al22 have published similar results; both groups studied a significant number of ARDS patients and found comparable mortality rates in patients with and without pneumonia. The patients included in our series bear a high mortality (80%). This must be underlined as an important limitation, as these figures possibly prevent identifying differences in mortality or other outcome measures among patients with and without infection. It must be pointed out that our protocol included a population of extremely sick ARDS patients, with lung injury scores > 2.5 (mean, 2.9 ± 0.3), which can account to some extent for the high mortality encountered. However, this study was not designed or powered to assess risk factors for mortality. Possibly, the high mortality in all series of ARDS is, in fact, a major limitation to finding significant differences in outcomes attributable to infection. In this setting the most frequent cause of death is multiple organ failure. Sutherland et al7 presented a series with the lowest overall mortality (44%). Even in this situation, they did not find any differences in mortality among patients with ARDS alone (40 of 89 patients, 45%) and those with ARDS and pneumonia (6 of 16 patients, 38%). In this study, there was a trend to longer duration of mechanical ventilation in patients with PPMs and PDRMs above the threshold, but it did not reach statistical significance. A previous trial22 reported a longer duration of mechanical ventilation in patients with ARDS who acquired pneumonia; however, study diagnosis criteria of pneumonia were less specific, as they only required one of three clinical criteria. In the present study, the likelihood of pneumonia was established by a high punctuation in the CPIS score. This approach is more specific and may possibly account for the differences between both studies. However, the early high mortality rate in our study may be a bias factor. The low number of survivors precludes further interpretation. Future multicentric case control studies that focus on the assessment of the attributable mortality of NP in patients with ARDS are warranted.

In conclusion, the isolation of pathogenic microorganisms and potentially drug-resistant microorganisms in the first 24 h after ARDS diagnosis was strikingly high. The frequency of microbiologically confirmed NP in early ARDS was 13%. Given the discordance in microbiological results between the diagnostic methods, an initial microbiological evaluation of NP in patients with ARDS should include TBAS and bilateral PSB, or other diagnostic techniques assessing the bacterial burden of both lungs. A significant impact of early lower airway colonization or infection on outcomes from ARDS could not be demonstrated.


   Footnotes
 
Abbreviations: APACHE = acute physiology and chronic health evaluation; CPIS = clinical pulmonary infection score; FIO2 = fraction of inspired oxygen; NP = nosocomial pneumonia; PDRM = potentially drug-resistant microorganism; PPM = potentially pathogenic microorganism; PSB = protected specimen brush; TBAS = tracheobronchial aspirate; VAP = ventilator-associated pneumonia

Dr. Torsten Bauer was a research fellow from the Medizinische Klinik, Abteilung für Pneumologie, Allergologie und Schlafmedizin, Bergmannsheil–Universitätsklinik, Bochum, Germany. Dr. Mauricio Valencia was a 2002 European Respiratory Society research fellow from the Universidad Pontificia Bolivariana, Medellín, Colombia. Dr. Santiago Ewig was a research fellow from the Medizinische Universitätsklinik and Poliklinik Bonn, Bonn, Germany.

Supported by Red Gira G03/063, FIS 02/0632, and Red Respira RTIC03/11.

Received for publication July 21, 2004. Accepted for publication December 9, 2004.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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