(Chest. 2005;128:394-400.)
© 2005
American College of Chest Physicians
A Prospective Study of the Timing and Cost-Effectiveness of Bronchial Washing During Bronchoscopy for Pulmonary Malignant Tumors*
Miep A. van der Drift, MD;
Gert-Jan van der Wilt;
Frederik B.J.M. Thunnissen, MD, PhD and
Julius P. Janssen, MD, PhD, FCCP
* From the Departments of Pulmonary Medicine (Drs. van der Drift and Janssen) and Pathology (Dr. Thunnissen), Canisius-Wilhelmina Hospital, Nijmegen; and the Department of Medical Technology Assessment (Ms. van der Wilt), Radboud University Hospital, Nijmegen, the Netherlands.
Correspondence to: Julius P. Janssen, MD, PhD, FCCP, Canisius-Wilhelmina Hospital, Weg door Jonkerbos 100, 6525 SZ Nijmegen, the Netherlands; e-mail: j.janssen{at}cwz.nl
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Abstract
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Study objectives: The value of obtaining washings during fiberoptic bronchoscopy in the workup of lung cancer is controversial. Moreover, the optimal timing of washing relative to biopsy and brushing is not known. In this study, the diagnostic yields of washings before and after biopsy and brushings were compared. The different diagnostic strategies were assessed in terms of yield and costs.
Design: A prospective study performed from 2001 to 2003 in a secondary care medical center.
Measurements and results: Two hundred twenty-one patients underwent flexible bronchoscopy, and the diagnostic yield of washings before biopsy and brushing (strategy I) and after biopsy and brushing (strategy II) specimens were assessed. Using the known probabilities and costs for various bronchoscopic procedures, the expected utility of a number of diagnostic strategies was estimated. Patients (147 men and 74 women) were included in the study in whom a definite cytologic or histologic diagnosis of pulmonary malignancy had been made. The diagnostic yield of strategy I was 72% for visible tumors and 36% for nonvisible tumors. For strategy II, the diagnostic yield was 74% for visible tumors and in 42% for nonvisible tumors. The comparison of strategies I and II for both visible and nonvisible tumors revealed that 176 cases were concordant (80%); in 19 cases (9%) the cytologic analysis of washings in strategy I was positive for malignancy and negative in strategy II. In 26 cases (12%) washings in strategy II were positive and negative in strategy I (p = 0.37). An analysis of the diagnostic yield of both washings in visible tumors and nonvisible tumors showed no significant difference. In 13 patients, a diagnosis of malignancy was established only by washings (6%). Confining the laboratory investigations of washings or brush samples to those cases in which the initial findings of the biopsies are negative (the two-stage procedure) is more cost-effective than examining all biopsy, brushing, and washing specimens. In patients with visible tumors, brushing or washing in addition to biopsy is equally cost-effective; in patients with nonvisible tumors, biopsy combined with washing is the preferred option.
Conclusions: No difference in the diagnostic yield could be demonstrated for washings before or after biopsies and brushings. Although the additional diagnostic yield of washing and brushing during bronchoscopy is relatively low, it is cost-effective to use these procedures in the diagnostic workup of patients who are clinically suspected of having a pulmonary malignancy.
Key Words: biopsy • bronchoscopy • brushing • cost-effectiveness • endoscopically visible tumor • lung cancer • peripheral nonvisible tumor • washing • yield
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Introduction
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To establish a cytologic or histologic diagnosis in a patient with suspected lung cancer, flexible bronchoscopy is an essential step in the workup. Washings, brushings, and forceps biopsies are often combined to increase the diagnostic yield.12345 The usefulness of obtaining washings is still subject to discussion.6 The diagnostic yield for washings in patients with endoscopically visible (central) tumors varies from 49 to 76% and is similar to the yield for brushings (52 to 77%) but is inferior to the yield of biopsies (71 to 91%).578910 The diagnostic yield of washings in patients with endoscopically nonvisible (peripheral) tumors varies from 35 to 52% and is similar to the yield for brushings (26 to 52%) and for biopsies (36 to 61%).578910
The optimal timing of bronchial washing (ie, whether before or after biopsy and brushing) is not clear. In some studies,8910 washings were obtained before biopsy and brush samples had been taken, whereas in other studies111213 washings were obtained after other specimens were collected. Only two abstracts1415 have been published about the performance of bronchial washing at the time of flexible bronchoscopy, but these have, to our knowledge, never been published as full articles.
Of increasing interest are the costs of several bronchoscopic techniques to obtain a diagnosis in lung cancer. Since the diagnostic yield of washings and brushings is relatively modest, one might consider omitting these procedures altogether. However, the further diagnostic tests used if the results of the above tests are negative are invasive, imposing a burden on the patient and incurring considerable costs. Therefore, even with a relatively low yield, washings and brushings may still be worthwhile. Govert et al16 concluded in their study that the collection of biopsy and either washing or brushing specimens is probably the most cost-effective way to obtain a diagnosis in patients with endoscopically visible tumors. The cost-effectiveness of bronchoscopic procedures in patients with endoscopically nonvisible tumors has, to our knowledge, not been studied.
The aim of this study was to compare the diagnostic yield of washings performed before and after brushings and biopsies during flexible bronchoscopy prospectively in patients with lung cancer. Also, different diagnostic strategies were assessed in terms of diagnostic yield and costs.
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Materials and Methods
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From 2001 to 2003, a prospective study in a secondary care medical center was performed to assess the diagnostic yield of washings before biopsies and brushings (strategy I) and after biopsies and brushings (strategy II). Patients suspected of lung cancer by signs, symptoms, or chest radiograph findings underwent flexible bronchoscopy. An endoscopically visible tumor was defined as an exophytic tumor or mass, mucosal infiltration, or submucosal lesion. An endoscopically nonvisible tumor was defined as a normal bronchial system or bronchial narrowing due to extrinsic compression with normal mucosa. Of these, only patients in whom a definite cytologic or histologic diagnosis of pulmonary malignancy was made were included in the study. If the bronchoscopic techniques did not reveal a diagnosis, other techniques such as transbronchial needle aspiration (TBNA), transthoracic needle aspiration (TTNA), mediastinoscopy, thoracotomy, and biopsies of extrapulmonary lesions were used. Specimens were considered to be adequate if alveolar macrophages and bronchial epithelial cells were present. The number of alveolar macrophages may vary, but in most cases they are also present in the case of a centrally located tumor. Strictly speaking, the presence of alveolar macrophages may not be required, but they are a constant finding in the great majority of the washings.
Bronchoscopies were performed by the specialist pulmonologists or by pulmonary residents (under specialist supervision) of our hospital. Flexible bronchoscopes (model 1T240 [working channel, 2.6 mm] and model 1T30 [working channel, 2.8 mm]; Olympus; Tokyo, Japan) were used. Unless contraindicated, patients were premedicated with diazepam, 5 mg orally, and IM atropine, 0.25 mg, 30 min before undergoing the procedure. Local anesthesia was achieved with 5 mL of 4% lidocaine spray applied to the upper airway including the laryngeal area. This was followed with one to two aliquots of 2.5 mL of 4% lidocaine instilled over the mucosa of the trachea, carina, and bronchial tree during bronchoscopy.
Bronchoscopic Technique
In patients with visible tumors, a first washing (washing I) was performed using 20 mL of saline solution. When the recruitment was low after suctioning due to coughing or if the aliquot was to be separated for microbiological analysis, another 20 mL of saline solution was injected and suctioned. After washing I, biopsy specimens were taken of the suspected area and a brushing was performed. Finally, a second washing (washing II) of the suspected area was done using the same technique as described for the washing I.
In patients with a tumor that was not visible through the bronchoscope, the washings were done in the corresponding segmental bronchus. After the washing I, brushing of the tumor was done under fluoroscopic guidance. If the brush could reach the tumor, biopsies were performed under fluoroscopic guidance. Then, washing II was performed.
The returned aspirates of the washings were fixed in a volume of 20 to 30 mL of fixation fluid (Fixcyt [containing 50% alcohol and 2% carbowax]) and sent for cytologic examination. Biopsy specimens were obtained using biopsy forceps (Olympus). Multiple biopsy specimens (ie, two to eight) were obtained for each patient, unless significant bleeding followed after the first specimen was obtained. The biopsy specimens were sent in neutral buffered formalin for histologic examination. Brushings were obtained with a disposable cytology brush (1.7 mm; Endomed; Phoenix, AZ). The material returned on the brush was spread on a slide, which was immediately fixed in 70% alcohol or by a spray fixative (Cerfix Spray Fixative [containing 2-propanol, polyethylene glycol 300 and acetone]; Zschimmer and Schwartz, Inc; Milledgeville, GA) and the same brush was then agitated in about 20 to 30 mL of fixation fluid and cut off. The slides, rinsing fluid, and brush were combined for the cytologic examination of brushing.
Statistical and Cost-Effectiveness Analysis
The level of agreement between both washings was tested with the McNemar test, using a two-sided significance level of 0.05. A decision model was developed to analyze specimen collection strategies of bronchoscopy using appropriate software (DATA, version 4.0; TreeAge Software; Williamstown, MA) [Fig 1
]. The following three approaches were compared: (1) bronchoscopy with biopsy, brushing, and washing; (2) bronchoscopy with biopsy and washing; and (3) bronchoscopy with biopsy and brushing. The data were analyzed separately for patients with visible and nonvisible tumors. It was assumed that, in the case of negative findings, a diagnostic workup was continued by conducting a second bronchoscopy (in the case of a visible tumor) or by using more invasive diagnostic procedures, including thoracotomy, TTNA, mediastinoscopy, TBNA, or biopsies of extrapulmonary lesions (Fig 2
). Using the probabilities and costs of the various procedures, the expected value of a number of diagnostic strategies was estimated. Probability estimates were derived from our study; cost data were derived from the financial department of our hospital (Table 1
). The expected value of an option is the sum of the values of all of the outcomes of that option, with each value being weighed by the probability that the consequence will occur.17 In our model, confirming the diagnosis of lung cancer was used as outcome, while the monetary costs of the applied procedures were used as value inputs.
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Figure 1.. Structure of the decision model comparing three different bronchoscopic strategies in the workup of patients with clinically suspected lung cancer. Positive = malignancy; negative = no malignancy.
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Figure 2.. Probability of using either of the invasive diagnostic procedures following negative biopsy, washing, and brushing results to establish the diagnosis of lung cancer. * = probability in visible tumor/nonvisible tumor.
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In another decision model in the diagnostic workup, biopsy was routinely performed in combination with brushing and washing, but washing or brushing samples were submitted for laboratory investigations only in the case of a negative biopsy finding (two-stage procedure). The structure of this decision model is depicted in Figure 3
.
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Figure 3.. Decision model reflecting the two-stage procedure, as follows: cytology of brushing (or washing) only in the case of negative findings of biopsy and washing (or brushing). See legend of Figure 1 for explanation of terms not used in the text.
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Results
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Two hundred eighty-one patients suspected of lung cancer underwent flexible bronchoscopy; 221 of these patients were proven to have a new pulmonary malignancy. The visible endobronchial abnormalities (137 patients) were exophytic tumors in 76 patients, mucosal infiltration in 37 patients, and submucosal lesions in 24 patients. Eighty-four patients had a nonvisible tumor. The study population had the following characteristics: mean age, 65.6 years; age range, 38 to 88 years; and 147 men and 74 women.
The diagnostic results of visible and nonvisible tumors are presented in Table 2
. A diagnosis was obtained from washing, biopsy, or brushing specimens from visible tumors in 129 of 137 patients (94%). The highest diagnostic yield was obtained by forceps biopsy in mass lesions (92%). The combined diagnostic yield of all three techniques for mass lesions was 97%, for infiltration was 92%, and for submucosal lesions was 88%. A diagnosis was obtained from washing, biopsy, or brushing specimens from nonvisible tumors in 47 of 84 patients (56%). The diagnostic yield of performing washings before biopsies and brushings for specimens of visible tumors was higher than the yield for nonvisible tumors (72% and 36%, respectively). The same is true for the yield for performing washings after biopsies and brushings (74% and 42%, respectively). The yields of washings I and II for submucosal lesions was lower (58% and 54%, respectively) than the yield for exophytic tumor (75% and 84%, respectively) or for mucosal infiltration (76% and 62%, respectively).
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Table 2.. Diagnostic Yield of Bronchoscopically Visible and Nonvisible Tumors Using Different Bronchoscopic Techniques*
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The comparison of washing I and II for both visible and nonvisible tumors revealed that 176 cases were concordant (80%). In 19 cases (9%), cytologic analysis of washing I specimens was positive for malignancy, whereas that of washing II specimens was negative, and in 26 cases (12%) washing II specimens were positive whereas washing I specimens were negative (p = 0.37) [Table 3
]. There were no significant differences in the yields of washings I and II for visible tumors (p = 0.85) or for nonvisible tumors (p = 0.33). A diagnosis of pulmonary malignancy was made exclusively by washing specimens in 13 patients (6%) [Table 4
].
The appearance of washing II specimens was blood-stained in almost every patient (89%), and in the appearance of washing I specimens was blood-stained in 29% of the patients. The analysis of washing II specimens was inconclusive due to poor cellularity in five patients, and the analysis of washing I specimens was inconclusive in one patient.
The amount of saline solution used to obtain both washings was 20 mL for 87% of the patients with visible tumors and 68% of the patients with nonvisible tumors. In the other cases, > 20 mL of saline solution was used because of low recruitment or separation for microbiological analysis. In patients with visible tumors, there were no differences in diagnostic yield for both washings whether 20 mL or > 20 mL of saline solution was used. In patients with nonvisible tumors, the diagnostic yield for washings performed with > 20 mL of saline solution was higher (washing I, 43%; washing II, 52%) than for those performed with only 20 mL of saline solution (30% and 38%, respectively).
Forty-five patients had a nondiagnostic bronchoscopy result, of whom 37 patients had a nonvisible tumor. In these patients, a diagnosis of pulmonary malignancy was established by a second bronchoscopy (2 patients), by TBNA of mediastinal lymphadenopathy (6 patients), by TTNA (21 patients), by mediastinoscopy (2 patients), by thoracotomy (6 patients), and by biopsies of extrapulmonary lesions (eg, liver and adrenal gland) [8 patients].
The pathologic diagnoses of the pulmonary malignancies were squamous cell carcinoma (76 patients), adenocarcinoma (49 patients), undifferentiated large cell carcinoma (38 patients), small cell carcinoma (41 patients), carcinoid tumor (2 patients), bronchioloalveolar carcinoma,1 and metastases from other organs (eg, breast carcinoma, renal cell carcinoma, and other carcinomas) [14 patients]. There were no false-positive results for the washings. Tumor cell type diagnoses were confirmed by resection samples in 28 patients who underwent thoracotomy.
Costs of Various Strategies in Relation to the Diagnostic Yield
The diagnostic yield in patients with visible tumors was 0.94, 0.88, and 0.88, respectively, for biopsy, washing, and brushing; for biopsy and washing; and for biopsy and brushing. The probability of using an invasive diagnostic procedure after a negative first bronchoscopy result is summarized in Figure 2, reflecting the frequency of these procedures in our series. It is assumed that either of these procedures establishes the diagnosis of lung cancer. The expected values of the various approaches were $1,247, $1,223, and $1,223, respectively, favoring the performance of bronchoscopy with biopsy and either washing or brushing. In the two-stage procedure, the estimated probability of establishing the diagnosis of lung cancer at the initial stage of the diagnostic workup remained unchanged (0.94, 0.88, and 0.88 respectively). If no malignancy was found, the diagnosis of lung cancer was established by examining either brushing or washing samples. The estimated probability of establishing the diagnosis after cytology of the brushing or the washing was in both cases 0.50. In the absence of a diagnosis after the first bronchoscopy, the same more invasive diagnostic options and associated probabilities were modeled. The expected value of these approaches was $1,247, $1,156, and $1,156 respectively, favoring the two-stage procedure, irrespective of whether brushing or washing was used in combination with biopsies.
In patients with nonvisible tumors, the diagnostic yields for the three approaches were 0.56, 0.46, and 0.49, respectively. The probability of using an invasive diagnostic procedure after a negative first bronchoscopy result is summarized in Figure 2, again reflecting the frequency of these procedures in our series. The expected value of the various strategies was $2,084, $2,243, and $2,178, respectively, hence favoring the approach employing bronchoscopy with biopsy in combination with washing and brushing. In the two-stage procedure, the estimated probabilities of establishing the diagnosis of lung cancer at the initial stage of the diagnostic workup remained unchanged (0.56, 0.46, and 0.49 respectively). The estimated probabilities of establishing the diagnosis after cytology of the washing samples (in the case of a negative test result after brushing) or cytology of the brushing samples (in the case of a negative test result after washing) were 0.12 and 0.18 respectively. In the absence of a diagnosis after the first bronchoscopy was performed, the same more invasive diagnostic options and associated probabilities were modeled. The expected values of these approaches were $2,084, $2,043, and $2,051, respectively, favoring the approach employing bronchoscopy in combination with washing, followed by cytology of the brushing in case of an initially negative test result.
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Discussion
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The aim of this study was to assess the diagnostic importance of the timing of washings at bronchoscopy in the investigation of patients who were suspected of having a pulmonary malignancy. The diagnostic yields in patients with visible tumors was 72% after washing I and 74% after washing II, which corresponds to values from other studies.578910 The extent of visible tumors influences the diagnostic yield. The yields of washings I and II for submucosal lesions were lower (58% and 54%, respectively) than those for exophytic tumors (75% and 84%, respectively) or for mucosal infiltration (76% and 62%, respectively). Other studies1819 have given similar results, although the definition of visible tumor varied between studies. The diagnostic yield for washings in patients with nonvisible tumors was lower than was expected (washing I, 36%; washing II, 42%). In other studies, it varies from 35 to 52%.578910
When comparing washings before and after biopsies and brushings, no significant differences in the diagnostic yield could be demonstrated for both visible and nonvisible tumors in our study. In the literature, no comparable study has been found. Raymond et al14 described in an abstract no difference in diagnostic yield relative to the timing of washings for central tumors. In peripheral nonvisible tumors, however, the yield for bronchial washing after biopsy and brushing was significantly higher than the yield for washing before biopsy and brushing (45% and 25%, respectively). In another abstract regarding visible tumors, Scriven et al15 showed a higher yield for washings after biopsy and brushing.
In 45 patients, the diagnostic yield of washing I was different from that of washing II. The question remains how the difference in yield between both washings can be explained. Arroliga and Matthay1 suggested that washings should be obtained after forceps and brush biopsies were performed to increase the diagnostic yield by referring to a study performed by Chaudhary et al.12 Chaudhary et al12 argued that more tumor cells would be freed after manipulation techniques were performed. However, Chaudhary et al12 did not compare washings before and after biopsies and brushes in their study. The hypothesis of obtaining more tumor cells by manipulation was not confirmed in our study. Another explanation for the different results of washing I and washing II might be patient-related factors in bronchoscopy (eg, cooperation of the patient or coughing). Although washing II specimens were blood-stained in almost every patient, this did not complicate the cytologic examination by the pathologist. It is not clear whether the amount of saline solution that was used to perform a washing influences the diagnostic yield. In our study, in patients with nonvisible tumors there was a trend for a higher diagnostic yield in washings performed with larger amounts of saline solution (ie, > 20 mL). Pirozynski20 showed that performing a BAL using 200 mL of NaCl was a valuable diagnostic tool in detecting peripheral pulmonary malignant neoplasms, especially in patients with adenocarcinomas, bronchioloalveolar carcinomas, and tumors exceeding 3 cm. Others have suggested6 that only small volumes (ie, < 20 mL) are required for a bronchial washing.
In 13 patients (6%), biopsies and brushings showed no malignancy, and the diagnosis of malignancy was established only by washings. Some studies have reported that adding bronchial washings to biopsies and brushings increases the diagnostic yield,891112132122 whereas others have reported7192324 no additional value of washings. The additional value of a washing as the only test providing a diagnosis varied from 1.5 to 5% in patients with visible tumors, and from 7.4 to 9.5% in those with nonvisible tumors. In our study, the variation was 2.9% (washing II) to 4.4% (washing I) in patients with visible tumors, and 4.8% for both washings in patients with nonvisible tumors.
In one study16 on the cost-effectiveness of adding a cytologic specimen, a modest increase in the sensitivity of fiberoptic bronchoscopy was found. Although the diagnostic yield of washing and brushing during bronchoscopy is relatively low, it is still cost-effective to use these procedures in the diagnostic workup of patients who are clinically suspected of having a pulmonary malignancy. Clearly, this is due to the relatively high costs associated with the more invasive procedures that are used in cases with negative biopsy, brushing, and washing results. The two-stage procedure in which laboratory investigations of washing or brushing specimens are confined to those cases in which the initial findings are negative could be a more cost-effective option. This is due to the saving of the costs of laboratory investigations, while at the same time fully exploiting the potential of these minimally invasive procedures at the expense of a delay in the analysis of the cytologic specimens of about a day. The extra costs of administration for storing brushing and washing samples were minimal ($3.5) and were therefore neglected. In the two-stage procedure, biopsy combined with brushing or washing was equally cost-effective in patients with visible tumors; in patients with nonvisible tumors, biopsy combined with washing was the preferred option.
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Conclusion
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The timing of washings during bronchoscopy in the diagnosis of lung cancer (before or after biopsy and brushing) does not influence the diagnostic yield. Although the diagnostic yield of washing and brushing during bronchoscopy is relatively low, it is cost-effective to use these procedures in the diagnostic workup of patients who are clinically suspected of having a pulmonary malignancy. Confining laboratory investigations of washing or brushing to those cases in which the initial findings of the biopsies are negative (the two-stage procedure) is more cost-effective than examining all biopsy, brushing, and washing specimens. In patients with visible tumors, biopsy combined with brushing or washing is equally cost-effective. In patients with nonvisible tumors, biopsy combined with washing is the preferred option.
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Acknowledgements
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We thank T.M. de Boo, MSC, Department of Epidemiology and Biostatistics University Medical Centre Nijmegen, the Netherlands, for statistical assistance, and Dr D. Whitehouse, pulmonologist, Chichester, UK, for language correction.
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Footnotes
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Abbreviations: TBNA = transbronchial needle aspiration; TTNA = transthoracic needle aspiration
Received for publication December 29, 2003.
Accepted for publication January 31, 2005.
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References
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Abstract
Introduction
