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* From the Department of Pulmonology and Critical Care Medicine (Drs. Herth, Eberhardt, and Becker), Thoraxklinik Heidelberg, Heidelberg, Germany; and Interventional Pulmonology (Dr. Ernst), Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA.
Correspondence to: Armin Ernst, MD, FCCP, Director, Interventional Pulmonology, Beth Israel Deaconess Medical Center, 330 Brookline Ave, Boston, MA 02215; e-mail: aernst{at}bidmc.harvard.edu
Abstract
Study objectives: Transbronchial biopsy (TBBX) for solitary pulmonary nodules (SPNs) is usually performed under fluoroscopic guidance, but the diagnostic yield depends on lesion size and varies widely. Nodules < 3 cm frequently cannot be visualized fluoroscopically. An alternative guidance technique, endobronchial ultrasound (EBUS), also allows visualization of pulmonary nodules. This study assessed the diagnostic yield of EBUS-guided TBBX in fluoroscopically invisible SPNs.
Design: The study was a prospective trial using a crossover design.
Patients and methods: All patients with SPNs and indications for bronchoscopy were included in the study. An EBUS-guided examination was performed in patients with fluoroscopically invisible nodules. The EBUS probe was introduced through a guide catheter into the presumed segment. If a typical ultrasonic picture of solid tissue could be seen, the probe was removed and the catheter left in place. The biopsy forceps were introduced and specimens taken.
Results: One hundred thirty-eight consecutive patients with SPNs were examined. Of those, 54 patients presented with SPNs that could not be visualized with fluoroscopy. The mean diameter of the nodules was 2.2 cm. In 48 patients (89%), the lesion was localized with EBUS, and in 38 patients (70%) the biopsy established the diagnosis. The 16 patients with undiagnosed SPNs were referred for surgical biopsy; 10 of those lesions were malignant and 6 were benign. The diagnosis in nine patients (17%) saved the patients from having to undergo a surgical procedure. The only complication was a pneumothorax in one patient.
Conclusions: EBUS-guided TBBX is a safe and very effective method for SPNs that cannot be visualized by fluoroscopy. The procedure may increase the yield of endoscopic biopsy in patients with these nodules and avert the need for surgical procedures.
Key Words: bronchoscopy • endobronchial ultrasound • lung cancer • solitary pulmonary nodules • transbronchial lung biopsy
Bronchoscopy has been used in evaluating solitary pulmonary nodules (SPNs) and masses for > 30 years. In patients with such nodules, the diagnostic procedure is usually performed as a transbronchial biopsy (TBBX) under fluoroscopic guidance, but the yield varies widely.1 Previous studies23 have shown that the size and location of the abnormalities influence the diagnostic accuracy of TBBX. Nodules that are too small to be visualized by conventional fluoroscopy during the procedure pose a particular problem and usually require additional, often surgical biopsy procedures. Our previous studies45 have shown that endobronchial ultrasound (EBUS) can be used as an alternative to fluoroscopy in providing image guidance for TBBX. We investigated whether EBUS-guided TBBX could be used in patients with fluoroscopically invisible lesions to increase yield and to save patients surgical biopsy procedures.
Materials and Methods
Patients and Methods
In a prospective crossover study from January 2003 to January 2004, all patients with SPNs who were referred for diagnostic bronchoscopy were enrolled. All chest CTs were reviewed, and the size of the lesions was recorded by their longest diameter. The procedures used in the study were in accordance with the recommendations found in the Helsinki Declaration of 1975. The study was approved by the institutional review board, and written informed consent was obtained in all patients, after which the patients underwent bronchoscopy. Procedures were performed under general anesthesia or conscious sedation in standard fashion. A variety of videobronchoscopes (models BF T160; Olympus; Tokyo, Japan) were used.
After complete inspection of the bronchial tree, including the subsegmental bronchi, fluoroscopy was performed using a monoplanar C-arm (Suprer 50 CP; Philipps Company; Amsterdam, the Netherlands). If the lesion was visible fluoroscopically, the procedure was continued with TBBX in the standard manner, and the patient was excluded from the trial. If the lesion could not be visualized by fluoroscopy, the patient was included in the trial and TBBX was performed under EBUS guidance. EBUS was performed with a flexible probe and processor unit (UM-3R, UM-4R, US2020R; Olympus; Tokyo, Japan) as described below. A bronchoscopic diagnosis of fibrosis or inflammation was considered nondiagnostic. All patients with nondiagnostic biopsy results were referred for surgical biopsy procedures.
Endobronchial Ultrasound
The EBUS probe was inserted through a guide sheath into the bronchi leading to the area in which the lesion was suspected. In contrast to the "snowstorm-like" whitish image of air-containing lung tissue, a solid lesion appears darker and more homogeneous. It is usually well-differentiated against the lung tissue by a bright border because of the difference in impedance (Fig 1 ). If a typical ultrasonic picture could be seen, the probe was removed from the sheath and the sheath was left in place. Biopsies were performed with regular disposable biopsy forceps. The forceps were introduced through the guide sheath, and four to six biopsy specimens were obtained.
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was set at 0.05, and statistical software was used for all analyses (SPSS version 11.5; SPSS; Chicago, IL). Results
One hundred thirty-eight consecutive patients with SPNs were examined. Of those, 54 patients (18 women and 36 men; mean age, 46.3 years; range, 35 to 78 years) presented with fluoroscopically invisible SPNs and were included in the trial population. The mean ± SD diameter of the lesion was 2.2 ± 0.7 cm (range, 1.4 to 3.3 cm). The nodules were located in the right middle lobe in 8 patients (15%), the left upper lobe in 10 patients (18%), the right upper lobe in 14 patients (26%), the left lower lobe in 14 patients (26%), and the right lower lobe in 8 patients (15%). The lesion was localized in 48 patients with EBUS-guided TBBX (89%).
A diagnosis was established in 38 of these patients (70%). In the 10 other patients, the lesion was localized but the pathologist was unable to establish a definitive diagnosis. The lesion could not be localized in six patients (11%); four of those lesions were located in the right upper lobe and two were in the left upper lobe, always in the apical segment. The mean examination time (including the biopsies) was 12.3 min (range, 6 to 18 min). The mean number of specimens obtained was 4.5 (range, 4 to 6). The 16 patients with undiagnosed SPNs were referred for surgical biopsy; surgical findings showed malignant lesions in 10 patients and benign lesions in 6 patients.
Tables 1 and 2 show the yield of TBBX by location of the lesions and the final diagnosis. Lesions were distributed fairly evenly throughout the lung. In 15 patients (28%), histologic findings showed benign lesions; in 39 patients (72%), the specimens were malignant. The diagnosis obtained by EBUS-guided TBBX in nine patients (17%) saved a surgical procedure (sarcoidosis, n = 2; tuberculosis, n = 3; metastatic disease, n = 2; small cell lung cancer, n = 2). Self-limited bleeding was observed in three patients, but severe bleeding was not observed in this study. One patient (2%) had a pneumothorax that was treated by tube thoracostomy. No deaths occurred with the diagnostic procedure.
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The need to workup and manage pulmonary nodules and masses is encountered with increasing frequency in chest medicine. A commonly performed procedure, endoscopic transbronchial biopsy, is associated with many problems. The yield greatly depends on the size and location of the abnormality2367 and generally on the ability to visualize the lesion fluoroscopically. The frequently small abnormalities that cannot be visualized with fluoroscopy present a particular problem because transbronchial biopsy, if performed, becomes a "blind, best-guess" biopsy. We showed previously that EBUS can provide an alternative to fluoroscopy for image guidance in biopsies for peripheral lesions.4 In that study, a trend toward superior results with EBUS was particularly strong in lesions < 3 cm in diameter. Our data were confirmed by Shirakawa et al.5
The current study assessed whether EBUS can help localize small, fluoroscopically invisible lesions. We postulated that EBUS could be added easily to TBBX and could help the bronchoscopist avoid aborting the procedure for lack of image guidance.
Our results indicate that EBUS guidance is very effective in TBBX. Lesions were detected in 89% of patients, and diagnostic biopsy tissue was obtained in 70%. Furthermore, the biopsy results averted the need for more surgery in 17% of patients.
EBUS is easily learned and adds little time to the TBBX procedure. Previous studies have proved its value for other indications, such as transbronchial needle aspiration guidance,8 decision support in invasive procedures,910 and detailed assessment of the airway wall.1112 This study confirms that image guidance for endoscopic transbronchial biopsies can be added to this growing list of indications for EBUS.
Footnotes
Abbreviations: EBUS = endobronchial ultrasound; SPN = solitary pulmonary nodule; TBBX = transbronchial biopsy
The endobronchial ultrasound probe was loaned to the authors by Olympus Ltd., Tokyo, Japan, for the duration of this study.
Received for publication March 10, 2005. Accepted for publication June 18, 2005.
References
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  M. Y. Dolina, D. C. Cornish, S. A. Merritt, L. Rai, R. Mahraj, W. E. Higgins, and R. Bascom Interbronchoscopist Variability in Endobronchial Path Selection: A Simulation Study Chest, April 1, 2008; 133(4): 897 - 905. [Abstract] [Full Text] [PDF]
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F. D. Sheski and P. N. Mathur Endobronchial Ultrasound Chest, January 1, 2008; 133(1): 264 - 270. [Abstract] [Full Text] [PDF]
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 T. R. Gildea, P. J. Mazzone, D. Karnak, M. Meziane, and A. C. Mehta Electromagnetic Navigation Diagnostic Bronchoscopy: A Prospective Study Am. J. Respir. Crit. Care Med., November 1, 2006; 174(9): 982 - 989. [Abstract] [Full Text] [PDF]
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K.-P. Wang, A. Ernst, F. Herth, R. Eberhard, and H. Becker Is endobronchial ultrasound necessary for transbronchial lung biopsy in solitary pulmonary nodule? Chest, October 1, 2006; 130(4): 1277 - 1278. [Full Text] [PDF]
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