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American Journal of Respiratory and Critical Care Medicine Vol 165. pp. 1618-1623, (2002)
© 2002 American Thoracic Society

Original Article

Reproducibility of Blind Protected Bronchoalveolar Lavage in Mechanically Ventilated Children

France Gauvin, Jacques Lacroix, Marie-Claude Guertin, François Proulx, Catherine Ann Farrell, Albert Moghrabi, Pierre Lebel and Clément Dassa

Division of Pediatric Intensive Care and Division of Hematology, Department of Pediatrics; Department of Mathematics and Statistics; Department of Microbiology, Sainte-Justine Hospital, Québec; and Department of Social and Preventive Medicine, Faculty of Medicine, Université de Montréal, Québec, Canada

Correspondence and requests for reprints should be addressed to France Gauvin, M.D., Department of Pediatrics, Sainte-Justine Hospital, 3175 Côte Ste-Catherine, Montréal, Québec, Canada H3T 1C5. E-mail: france_gauvin{at}ssss.gouv.qc.ca


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Blind protected bronchoalveolar lavage (BAL) could be an interesting tool in the diagnosis of ventilator-associated pneumonia in intubated children, but its reproducibility has never been evaluated. This study evaluates the reproducibility, feasibility, and safety of blind protected BAL in mechanically ventilated children. Two blind protected BAL were done, at a 2-hour interval, in 30 patients. The reproducibility of microbiologic and cytologic results was studied. A total of 60 BALs was analyzed. Bacterial growth was present in 26 of 60 BAL (43%). Reproducibility for the presence of bacteria on quantitative cultures was excellent (concordance, 93%; kappa [{kappa}], 0.86). Concordance for the type of bacteria isolated was 86% and for the number of bacteria was 79%. Reproducibility for the presence of neutrophils containing bacteria was perfect (concordance, 100%; {kappa}, 1) although only a few BALs had a positive result (8/60). Blind protected BAL was feasible in all patients and all samples were considered adequate for analysis. Complications were mostly benign and transitory except in two cases: one pneumothorax and one significant increase in intracranial pressure. Overall, blind protected BAL is a reproducible test in mechanically ventilated children, is easily feasible, and is usually well tolerated.

Key Words: bronchoalveolar lavage • critical care • pediatric intensive care units • pneumonia • reproducibility of results


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Ventilator-associated pneumonia (VAP) is an important issue in the pediatric intensive care unit (PICU). The incidence of VAP in the PICU is low (1.2%), but the attributable mortality rate is significant (8%) (1). The best way to diagnose VAP is still a matter of debate. Autopsy remains the "gold standard" (2), but is not clinically useful. Clinical criteria alone may not be sufficiently reliable (3, 4). Over the years, new diagnostic techniques such as bronchoscopic bronchoalveolar lavage (BAL) and use of a protected specimen brush have been studied and are now widely used in adults (5–16). The reproducibility of these bronchoscopic methods is reasonable in adults (17–20) and they are now considered to be the best methods to diagnose VAP in this population. In the PICU, these bronchoscopic methods are not easily applicable, mainly because of the small size of the endotracheal tube and because of complications associated with these procedures (21–23). Moreover, experience with these methods in the PICU is still limited and their validity in mechanically ventilated children remains to be determined.

BAL can be done blindly (without bronchoscopy), and can be performed with a catheter that is protected (double-lumen catheter) or not. In adults, the sensitivity and specificity of blind protected BAL range from 70 to 80% and from 65 to 69%, respectively (2, 24). It is easy to perform and safe to use. However, it has been studied only once in mechanically ventilated children (25): sensitivity and specificity were 83 and 75%, respectively, using clinical, radiological, and pathological criteria as reference. It has never been validated by comparison with a gold standard (autopsy) in pediatric patients.

The first step in evaluating the validity of blind protected BAL in the diagnosis of VAP in intubated children would be to estimate its reproducibility. The latter has not been evaluated so far, in a pediatric or adult population.

The primary objective of this study is to evaluate the reproducibility, in mechanically ventilated children, of microbiologic and cytologic analyses of respiratory secretions collected by blind protected BAL. The second objective is to evaluate the safety and feasibility of this technique in the pediatric population.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
A more detailed description about the procedure and reproducibility analysis is available in the online data supplement.

Patients
This prospective descriptive study was performed over 27 months, with patients 18 years old or younger admitted to the PICU of Sainte-Justine Hospital (Québec, Canada). A sample size of 30 patients was considered appropriate (ß = 80%; {alpha} = 0.05; {rho} > 0.8) (26). All consecutive mechanically ventilated patients with recognized risk factors for VAP (27), who were in the PICU for more than 48 hours, and with two of the following criteria, were included: (1) rectal temperature > 38°C or < 36.3°C and two respiratory signs: tachypnea, dyspnea, bradypnea, ronchi/wheezing; (2) purulent aspect or increased amount of endotracheal secretions; (3) positive culture of endotracheal secretions; (4) positive blood culture; and (5) new radiological infiltrate or pleural effusion. Exclusion criteria were as follows: pregnancy, brain death, contraindication to perform a BAL (severe bronchospasm, pulmonary hypertension, cardiopulmonary instability, severe hypoxemia), refusal from attending physician or parent to participate, loss of specimen, and impossibility to complete BAL. Informed consent was obtained from the parents. This study was approved by the Research Ethics Committee of Sainte-Justine Hospital.

Bronchoalveolar Lavage
All BALs were done by the same operator (F. G.), using a protected double-lumen catheter (Combicath; Plastimed, Saint Leu la Forêt, France). BAL was performed twice, with a 2-hour interval, in each patient. All complications during or 24 hours after the procedure were reported.

Specimen Evaluation
Microbiology.
For quantitative cultures, a conventional dilution technique was used to obtain a precise positivity threshold. Aerobic and anaerobic cultures, as well as Gram staining, were done. All growth >= 102 colony-forming units per milliliter (CFU/ml) was reported.

Cytology.
Cell counts with differential and May-Grünwald-Giemsa coloration were done. Samples showing >= 1% of neutrophils containing bacteria were reported.

All samples were analyzed by the same microbiologist (P. L.) and the same hematologist (A. M.), who were blinded as to the origin of the samples. Samples were not paired when sent to the laboratory.

Reproducibility Analysis
Results of the two BALs done in each patient (quantitative bacterial cultures and cytologic tests) were analyzed for reproducibility.

Concordance percentage was used for reproducibility of presence of bacteria, number of bacteria, and type (species) of bacteria between the two BALs.

The kappa ({kappa}) score was used to estimate reproducibility of the presence of bacteria on quantitative culture and on Gram stain, as well as the presence of neutrophils containing bacteria. It was also used to evaluate agreement for different bacterial thresholds.

An intraclass correlation coefficient (ICC) was calculated to compare both bacterial index (BI) and predominant species index (PSI) between paired BALs.

Stratification between patients with or without prior antibiotic treatment was also done.

Descriptive data are expressed as means ± SD; median (range). Continuous data were compared by the Student paired t test or Wilcoxon signed-rank test. Categorical data were compared by {chi}2 analysis. Absence of systematic difference (bias) between paired BALs was evaluated by the McNemar test. Statistical significance was established at p < 0.05.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Demographic Data
Thirty-three patients were included in the study. Three patients were excluded: two patients because of contraindication to perform the second BAL (cardiopulmonary instability; elevated intracranial pressure) and one because of loss of the second specimen. Demographic data for the remaining 30 patients are presented in Table 1. Significant severity of illness was present in these patients, who suffered from various underlying disease processes. Primary diagnosis was mainly trauma (n = 6), acute respiratory distress syndrome (ARDS; n = 5), and severe burns (n = 4). Ten patients (33%) had multiple organ dysfunction syndrome (MODS) on the day of entry in the study. Twenty-one patients (70%) received antibiotic therapy for 4 ± 5 days before BAL was performed. Length of stay in the PICU was 47 ± 75 days. One death occurred during the study and was unrelated to the BAL.


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  		TABLE 1. Demographic data of the patients

 
BAL Data
Thirty pairs of BALs were analyzed. All specimens were considered satisfactory (< 1% squamous epithelial cells [2, 28]). The amount of fluid injected was similar between the two BALs (BAL 1: 20.2 ± 13.6 ml; BAL 2: 18.8 ± 12.0; p = 0.49), as well as the amount of aspirated fluid (BAL 1: 6.0 ± 3.6 ml; BAL 2: 5.4 ± 2.7; p = 0.42). The ratio of fluid aspirated to fluid injected was appropriate and similar for both BALs (BAL 1: 32 ± 11%; BAL 2: 34 ± 20%; p = 0.91). Cellularity of the samples was analyzed and there was no difference between the two BALs [BAL 1: 3,145 (± 6,878) x 106/L; BAL 2: 2,237 (± 4,737) x 106/L; p = 0.11]. Differential count showed no difference in the percentage of neutrophils between the two BALs [BAL 1: 65.3 (± 23.9) x 106/L; BAL 2: 64.2 (± 25.6) x 106/L; p = 0.31].

Bacteriologic Data
Microbiologic results are shown in Table E1 (see online data supplement). There was bacterial growth (>= 102 CFU/ml) in 26 of 60 BALs (43%). Thirteen different bacterial species were found (see Table E2 in the online data supplement). There was more than one bacterial species in 17 BALs.

There was concordance between the two BALs for the presence of bacteria in 28 of 30 patients (12 positive/positive; 16 negative/negative). Results were discordant in two patients (two negative/positive). These results indicate excellent reproducibility (concordance percentage, 93%; {kappa}, 0.86). No systematic bias was detected between the two BAL groups (p = 0.16).

Among the 14 patients with at least one positive culture, we assessed concordance for the number and type of bacteria isolated. For the number of bacteria, two BALs were considered concordant if the result of quantitative culture (predominant species) showed a difference in log10 CFU/ml <= 1 (e.g., 102/ 103). For the type of bacteria, there was concordance between the two BALs if the predominant bacteria found in both BALs were from the same species (e.g., Staphylococcus aureus/Staphylococcus aureus). For the number of bacteria, we found a concordance percentage of 79%. For the type of bacteria, the concordance percentage was 86%; discordant results are those from the two patients with one positive BAL and one negative BAL.

The BI (which represents the sum of the log of all species obtained by the BAL [29]) was calculated for each BAL (see Table E1 in the online data supplement). There was no significant difference between the BI of BAL 1 and BAL 2 (Wilcoxon; p = 0.21). The ICC for the BI was calculated at 0.82, which demonstrates good reproducibility. The PSI (which refers to the log of the species in highest concentration only [5, 30]) was also evaluated for each BAL (see Table E1 in the online data supplement). Comparison between the PSI of BAL 1 and BAL 2 for all patients showed no significant difference (Wilcoxon; p = 0.06). The ICC for the PSI was calculated at 0.82, which also represents good reproducibility.

Cytologic Data
Cytologic results are shown in Table E1 (see online data supplement). Neutrophils containing bacteria were reported in eight BALs. There was perfect agreement (concordance percentage, 100%; {kappa}, 1) between paired BALs in all patients (26 negative/negative and 4 positive/positive). Cytologic results were evaluated twice by the same observer; intraobserver repeatability was assessed and agreement was excellent (98%). Afterward, samples were analyzed by another blinded observer; interobserver repeatability was also evaluated and was excellent (100%).

Gram stain was also evaluated for each BAL and was positive for the presence of bacteria in 14 BALs (Table E1 in the online data supplement). Results were concordant in 25 of 29 BALs (5 positive/positive and 20 negative/negative), which indicates substantial agreement (concordance percentage, 83%; {kappa}, 0.62). In the five patients with positive Gram stain in both BALs, the type of bacteria reported was the same.

Bacterial Threshold
Using the BI and the PSI, different thresholds for quantitative cultures were evaluated (102 to 105 CFU/ml). For each threshold, the {kappa} score indicated substantial agreement (> 0.6) and the McNemar test showed no systematic bias (p > 0.05). Reproducibility was best at a threshold of 102 or 103 CFU/ml for both index (Figure 1) .



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  		Figure 1. Diagram showing reproducibility for different thresholds of quantitative cultures using the bacterial index (A) and the predominant species index (B). Thresholds are expressed on the x axis with the log 10 in CFU/ml (ex: 103 = 3 on the log scale). Reproducibility is evaluated by the kappa score on the y axis.

 
Use of Antibiotics before BAL
There was prior antibiotic treatment in 21 of 30 patients (70%). BAL cultures were more frequently positive among patients without prior antibiotic treatment than among patients with prior antibiotic treatment (83 versus 26%; p < 0.001). However, the presence of antibiotics did not modify reproducibility. The concordance percentage for the presence of bacteria was 95% in the group with antibiotics versus 89% in the group without antibiotics. There was no significant difference between the {kappa} score of the two groups (0.88 versus 0.61; p = 0.46). Concordance percentages for the number of bacteria isolated (83 versus 75%) and the type of bacteria isolated (83 versus 87%) were also similar in both groups.

Other factors, such as the length of the catheter used, the amount of fluid retrieved, and the type of bacteria found, were also evaluated and did not have an effect on reproducibility of the method.

Complications
Adverse events during the procedure are detailed in Table 2. Most adverse events were benign, transient, and did not require any treatment: lowest oxygen saturation noted was 80% and lasted for less than 2 minutes; average increase in intracranial pressure was 10 mm Hg and returned to baseline within 5 minutes without additional therapy; bradycardia and a drop in blood pressure occurred in one patient but resolved spontaneously within seconds. In two patients, significant complications were observed: one patient (1 month old) with ARDS developed during the second BAL a pneumothorax that required chest tube insertion for drainage. Another patient (9 years old) with head injury developed increased intracranial hypertension during the first BAL and was excluded from the study because he remained too unstable. No significant complications occurred in any patients in the 24 hours after the BAL. There were significantly more adverse events during the first BAL compared with the second BAL (83 versus 47%; p < 0.05).


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  		TABLE 2. Complications during bronchoalveolar lavage

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Blind Protected BAL
In adults, bronchoscopic BAL is considered one of the most reliable diagnostic tests for VAP and is used to obtain quantitative cultures, calculate the BI, and obtain cytologic results (5, 7, 11–16, 28, 31–36). Nonbronchoscopic BAL has also been used in the past 10 years with good results (9, 37). The advantages of doing a blind (nonbronchoscopic) BAL include ease of performance at the bedside, feasibility through small endotracheal tubes (< 4.0 mm), less discomfort for the patient, and low cost. The disadvantage is that, without bronchoscopy, it is difficult to predict in which part of the lung the sample will be taken. Some authors consider that a bronchial aspirate is reliable only if directed toward the affected lung region (38, 39). Others consider that when a nosocomial pneumonia is present, bacteria can be found in all parts of the lungs; therefore a blind method should not weaken the validity of a BAL (40–42). Moreover, the accrual of information obtained by bronchoscopic BAL compared with blind BAL is probably small (sensitivity of blind BAL: 76 to 100% versus bronchoscopic BAL: 43 to 100% [37, 43, 44]; specificity of blind BAL: 75 to 100% versus bronchoscopic BAL: 50 to 100% [5, 6, 8, 12]). In our study, even though we did not assess the position of the catheter during blind BAL, the method was reproducible.

BAL can be done with or without a protected catheter. The use of a protected catheter generates a sample without contamination from upper airway flora. Such a protected method could be more reliable for the precise diagnostic of VAP and does not require more manipulations than the nonprotected method.

Therefore, the combination of a blind (nonbronchoscopic) and a protected method seems ideal for the pediatric population, regarding reproducibility, safety and costs; however, its validity as a diagnostic marker of VAP in critically ill children still remains to be estimated with autopsy as the reference standard.

Bacterial Threshold
In the literature, the most frequently used threshold for BAL is 104 CFU/ml (11, 13, 28). This threshold is used mainly for bronchoscopic nonprotected BAL. In our study, the objective was not to find the best threshold to diagnose VAP but to evaluate the reproducibility of blind protected BAL. Therefore, we analyzed the data with a sensitive threshold (102 CFU/ml) to include all significant bacterial growth in the analysis. We also considered it appropriate to look at a low threshold because most contaminants should be excluded with a protected catheter.

We evaluated the reproducibility of blind protected BAL at different thresholds of bacterial growth (102 to 105 CFU/ml). Our results show better reproducibility at a lower threshold, showing that the method is better when all bacteria (even those present in small amounts) are taken into account. Using a more sensitive threshold is then probably appropriate for this type of instrument.

Reproducibility
Before evaluating the validity of a diagnostic test, a study to assess its reproducibility needs to be done. The only study of the reproducibility of BAL in the literature was done in adults by Gerbeaux and coworkers with bronchoscopic nonprotected BAL (30). In that study, reproducibility was evaluated in 44 ventilated adults with suspected VAP. The two BALs were performed in the same lung area with a 30-minute interval. The qualitative repeatability for bacteria (presence or absence) was excellent (concordance, 96%; {kappa}, 0.72). The quantitative repeatability (same log10 for both BALs) was poorer (27%). They used a threshold of 104 CFU/ml and reported only the predominant species for each BAL. Our study is different because it was done with pediatric patients instead of adults and with blind protected BAL instead of bronchoscopic nonprotected BAL. In our study, the reproducibility of blind protected BAL was excellent for the presence of bacteria on quantitative culture (93%). It was also very good for the type of bacteria isolated (85%) and for the number of bacteria isolated (78%). The BI and the PSI were also highly reproducible.

The presence of neutrophils containing bacteria has been validated in adults as a diagnostic tool to assess rapidly the possibility of pneumonia in mechanically ventilated patients (5, 7, 9, 32, 33, 45–47). A study done in intubated pediatric patients with blind protected BAL has shown a sensitivity and specificity of 55 and 89%, using a threshold of 1% (25). The reproducibility of neutrophils containing bacteria has not been evaluated so far. In our study, concordance between the two BALs was perfect. However, only a few patients demonstrated a positive result and we did not study the diagnostic value of this test. A subsequent study to evaluate its validity in the diagnosis of VAP in children is required before using this test routinely in the PICU.

In the literature, some data showed that the administration of antibiotics before BAL can modulate the results of bacterial cultures (24, 48–51). In our study, the fact that some patients were treated with antibiotics before BAL did not seem to influence the reproducibility, even though the proportion of positive BALs was higher in the group without antibiotics.

Complications
Complications of BAL were frequent, but most were transitory and benign. There were more complications during the first BAL compared with the second one. This suggests a better knowledge of the patients and adaptation on the part of the operator during the second BAL. Even though blind protected BAL is considered fairly safe, two significant complications were observed. Blind protected BAL is less invasive and probably safer than bronchoscopic BAL, but it should be done by a qualified operator and the patient should be monitored carefully during and after the procedure. Complications could probably be avoided with better sedation and use of paralyzing agents in unstable patients.

Limitations and Strengths of the Study
Our study shows that the reproducibility of quantitative cultures, even if very good, was not perfect. In two cases, only the second BAL was positive. The reason for these variations is difficult to explain. We do not believe that a washout effect of the first BAL on the second one was an important factor because there was a 2-hour interval between the two procedures. A contamination of the second sample by the prior BAL is unlikely because the technique was done blindly and the chance that the catheter tip arrived exactly at the same site both times is small. A variation due to a different dilution of the two samples is also unlikely because the amount of fluid injected and aspirated, as well as the cellularity of fluid aspirated, were similar in both samples from all patients. The possibility that the concentration of bacteria is different in certain lung segments could explain these variations. Variations of results can exist even if two samples are taken from the same segment, by the same operator (19). The fact that the samples are taken blindly or directed bronchoscopically does not seem to eliminate the variations between the results. Such variations could be impossible to avoid.

This study has a number of strengths. By assessing all consecutive patients prospectively and by using strict inclusion and exclusion criteria, the possibility of selection bias is low and generalizability of the results to all mechanically ventilated children must be good. All BALs were done by the same operator to avoid interobserver variability. All analyses were done by the same technicians and all results were evaluated by the same experts (one hematologist and one microbiologist) to exclude the possibility of variability due to the technique or interpretation of the results. Intrasubject variability was also excluded because the two BALs were done in the same patient, with a 2-hour interval.

Conclusion
Results of quantitative and qualitative cultures of lower respiratory tract secretions collected by blind protected BAL are reproducible in mechanically ventilated children. This procedure is easily accomplished at the bedside, yields adequate samples of bronchoalveolar secretions, and is usually safe. Further studies are required to estimate the validity of blind protected BAL as a diagnostic marker of VAP in critically ill children, using autopsy as the reference standard.


   Acknowledgments
 
Supported by the Fondation de l'Hôpital Sainte-Justine.


   FOOTNOTES
 
This article has an online data supplement, which is accessible from this issue's table of contents online at www.atsjournals.org

Received in original form April 26, 2001; accepted in final form January 22, 2002


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
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