- Email: [email protected]
Endobronchial Ultrasonography Guidance for Transbronchial Needle Aspiration Using a Double-Channel Bronchoscope
Endobronchial Ultrasonography Guidance for Transbronchial Needle Aspiration Using a Double-Channel Bronchoscope* Koji Kanoh, MD; Teruomi Miyazawa, MD, PhD, FCCP; Noriaki Kurimoto, MD, PhD; Yasuo Iwamoto, MD, PhD; Yuka Miyazu, MD; and Nobuoki Kohno, MD, PhD, FCCP
Study objectives: Endobronchial ultrasonography (EBUS) is used as guidance for transbronchial needle aspiration (TBNA), and real-time imaging of the needle position cannot be confirmed with a single-channel bronchoscope. We assessed the usefulness of EBUS-guided TBNA using a double-channel bronchoscope (EBUS-D), which provides real-time needle position, and compared it with EBUS-guided TBNA using a single-channel bronchoscope (EBUS-S). Design: Randomized, comparative prospective study. Setting: Hiroshima City Hospital, a tertiary-referral teaching hospital. Patients: Between January 2000 and August 2003, 55 patients with intrathoracic lymphadenopathy were included. Patients were randomized to undergo EBUS-D (n ⴝ 30) or EBUS-S (n ⴝ 25). Methods: EBUS-D: The EBUS probe and TBNA catheter were inserted simultaneously through a double-channel bronchoscope. Once the needle placement in the lesion was confirmed by EBUS, TBNA was performed. EBUS-S: The EBUS probe was removed after the determination of the penetration site. Then, the TBNA catheter was inserted and TBNA was performed. Results: All the lymph nodes could be visualized with EBUS in each group of patients. In the EBUS-D group, the TBNA needle was visualized as a hyperechoic point on the real-time EBUS image. The diagnostic accuracy rate of EBUS-D and EBUS-S were statistically significantly different (97% vs 76%, respectively; p ⴝ 0.025). On second attempt of TBNA, the diagnostic rate of the EBUS-D group was superior to that of the EBUS-S group (85.7% vs 33.3%, respectively; p ⴝ 0.036). The mean number of penetrations was 1.24 in the EBUS-D group and 1.36 in the EBUS-S group. No complications were observed in the EBUS-D group, but a self-limiting hemorrhage occurred in a patient in the EBUS-S group. Conclusion: EBUS-D is useful for diagnosing intrathoracic lymphadenopathy, and the obtained specimen with real-time confirmation of the needle is directly proportional to an accurate diagnosis. (CHEST 2005; 128:388 –393) Key words: bronchoscopy; intrathoracic lymphadenopathy; endobronchial ultrasonography; transbronchial needle aspiration Abbreviations: EBUS ⫽ endobronchial ultrasonography; EBUS-D ⫽ endobronchial ultrasonography-guided transbronchial needle aspiration using a double-channel bronchoscope; EBUS-S ⫽ endobronchial ultrasonography-guided transbronchial needle aspiration using a single-channel bronchoscope; TBNA ⫽ transbronchial needle aspiration
use of transbronchial needle aspiration T he(TBNA) in addition to routine bronchoscopy was reported to improve the diagnostic rate for malig-
nancies.1– 4 As target lymph nodes cannot be visualized directly with the conventional TBNA procedure, aspiration efforts are directed by knowledge of
*From the Department of Internal Medicine (Dr. Kanoh), Fukushima Co-op Hospital, Hiroshima; the Department of Pulmonary Medicine (Drs. Miyazawa, Iwamoto, and Miyazu), Hiroshima City Hospital, Hiroshima; the Department of Molecular and Internal Medicine (Dr. Kohno), Graduate School of Biomedical Sciences, Hiroshima University, Hiroshima; and the Department of Surgery (Dr. Kurimoto), Hiroshima National Hospital, Higashi-Hiroshima, Japan. This study was performed at Hiroshima City Hospital, a tertiaryreferral teaching hospital, Hiroshima, Japan.
Manuscript received January 29, 2004; revision accepted June 30, 2004. Reproduction of this article is prohibited without written permission from the American College of Chest Physicians (www.chestjournal. org/misc/reprints.shtml). Correspondence to: Teruomi Miyazawa, MD, PhD, FCCP, Director, Department of Pulmonary Medicine, Hiroshima City Hospital, 7–33 Motomachi, Naka-ku, Hiroshima, Japan; e-mail: [email protected]
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thoracic anatomy and prior CT imaging. Multiple needle passes are required for each target because there is the possibility of error in puncturing the target lesion. Therefore, the diagnostic rate of TBNA seems to be related to the lymph node size and location as well as the operator’s experience. With the development of new technology, endobronchial ultrasonography (EBUS) is reported to be useful in detecting mediastinal and hilar lymphadenopathy in addition to assessing the depth of tracheobronchial tumor invasion.5– 8 Recently, EBUS has also been used for TBNA guidance and has improved the results of N-staging, especially in difficult lymph node levels without any clear endoscopic landmarks.9 –13 However, Shannon et al9 reported that EBUS guidance did not offer a statistically significant advantage when compared with conventional TBNA because the sensitivities of both procedures were extremely high (82.6% vs 90.5%, respectively). However, Herth, et al13 reported that EBUS guidance significantly increased the yield of TBNA in the mediastinal lymph node except for subcarinal lymph node in their randomized trial (84% vs 58%). The main disadvantage of EBUS guidance using a single-channel bronchoscope is that a real-time imaging of the needle position within the target lesion cannot be confirmed because the EBUS probe must be removed during the TBNA procedure. To overcome this problem, a double-channel bronchoscope, through which both a TBNA catheter and an EBUS probe can be inserted simultaneously, was necessary. This study assessed the usefulness of EBUS-guided TBNA using a double-channel bronchoscope (EBUS-D) or EBUS-guided TBNA using a single-channel bronchoscope (EBUS-S). Materials and Methods
sheath was inserted through the 2.8-mm channel. The balloon was subsequently filled with sterile water to eliminate the air between the lesion and the probe. We evaluated the target lesion and determined the penetration site. Then, a 19-gauge TBNA catheter (Wang transbronchial histology needle, MWF-319 or MW-319; Mill-Rose Laboratories; Mentor, OH) was inserted through the 2.0-mm channel after the EBUS probe was retracted to the bronchoscope tip to prevent possible damage by the TBNA needle. Once the needle was introduced through the bronchial wall, the EBUS probe was again advanced to the penetration point along the tracheobronchial wall (Fig 1, 2, top left, A, and bottom left, C). When the TBNA needle was within the lesion, the real-time EBUS image of the needle was a hyperechoic point in the lesion (Fig 2, top right, B, and bottom right, D). If the TBNA needle was not confirmed to be inside the lesion by EBUS on the first attempt, a subsequent penetration was attempted while changing the penetration site. Specimens in the TBNA needle were flushed by air. Histology specimens were fixed in formalin, and cytology specimens were smeared on glass slides and fixed in alcohol before sending to the pathology department. EBUS-S: The EBUS probe was inserted through a singlechannel flexible bronchoscope (BF-1T-30; Olympus). Once the penetration site was determined following the same procedure used for EBUS-D, the EBUS probe was removed through the bronchoscope. Next, the TBNA catheter was inserted through the channel and TBNA was performed. The specimens in the TBNA needle were flushed by air. If a histologic specimen could not be obtained on the first aspiration, a second TBNA was attempted. We did not utilize fluoroscopy or rapid on-site cytopathology evaluation in either study group. Statistical Methods Student t test was used to compare the mean age and size of the lymph node. The 2 test was used to compare the rate of patients with a parenchymal lesion, those with multiple lymphadenopathies, the lymph node locations undergoing TBNA, and the diagnostic rate of EBUS-D and EBUS-S. A statistical software package (SAS, version 8.2; SAS Institute; Cary, NC) for categorical variables was used for all analyses. A p value ⬍ 0.05 was significant difference.
Results The patient characteristics are shown in Table 1. There were no significant differences between the
Patients We enrolled 55 patients with mediastinal and/or hilar lymphadenopathy in this prospective study between January 2000 and August 2003. The indication for TBNA was the diagnosis of an enlarged lymph node. Patients were randomized to undergo EBUS-D (n ⫽ 30) or EBUS-S (n ⫽ 25). This study was approved by the Committee on Human Research of our institution. Written informed consent was obtained from all patients. Procedure EBUS-D: An ultrasonic probe (2.5 mm in diameter, radial mechanical transducer operating at 20 MHz) [UM-BS20 –26R; Olympus; Tokyo, Japan] with a flexible balloon sheath (MAJ643R; Olympus) was connected to an ultrasound unit (EU-M 20; Olympus). A flexible bronchoscope (external diameter, 7.2 mm) [XBF-2T40Y2; Olympus] with two channels (diameters, 2.8 mm and 2.0 mm) was inserted transorally, without an endobronchial tube, under local anesthesia. The EBUS probe with a balloon www.chestjournal.org
Figure 1. TBNA catheter and EBUS probe are inserted simultaneously through a double-channel bronchoscope. The EBUS image by the mechanical radial transducer provides a crosssection (dotted line) of the lymph node with the needle inside. CHEST / 128 / 1 / JULY, 2005
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Figure 2. Top left, A: the left catheter shown is the EBUS probe with a balloon sheath, and the right catheter is the TBNA catheter by which a right hilar lymph node was penetrated. Top right, B: the EBUS image obtained without an inflated balloon shows the needle penetrating the lymph node. The needle tip is recognized as a hyperechoic point (arrow), and the acoustic shadow is revealed in the opposite direction of the EBUS probe (arrow head). Sarcoidosis was diagnosed in this patient. Bottom left, C: the left catheter is the EBUS probe, and the right catheter is the TBNA catheter by which the pretracheal lymph node was penetrated. Bottom right, D: the EBUS image shows a hyperechoic point (arrow) and the acoustic shadow (arrow head) in the lesion. Metastatic adenocarcinoma was diagnosed in this patient.
EBUS-D group and the EBUS-S group in the mean age, percentage of cases of a parenchymal lesions with lymphadenopathy, percentage of cases with multiple lymphadenopathies, mean size of the lesion, and percentage of cases with small nodes ⱕ 20 mm. There was also no significant difference in lymph node locations sampled by EBUS-D and EBUS-S. Table 2 shows the diagnostic yield of TBNA. One patient in the EBUS-D group was excluded from this study because liquid had been aspirated from the lesion leading to a diagnosis of a pericardial cyst after surgical resection. Of 29 patients in the EBUS-D group, 23 histologic diagnoses were established. Of the remaining six patients, cytology diagnoses were 390
established in five. Of 25 patients in the EBUS-S group, 17 histologic diagnoses were established. Of the remaining eight patients, only two diagnoses were made using cytology. The diagnostic rate of EBUS-D was significantly higher than that of EBUS-S (97% vs 76%, respectively; p ⫽ 0.025). Six patients without a specific diagnosis (normal bronchial glands and cartilages in two patients, and four patients without lymphocytes on the specimen) in the EBUS-S group had adenocarcinoma (n ⫽ 5) and sarcoidosis (n ⫽ 1) after surgical resection. A patient without a specific diagnosis in the EBUS-D group was found to have adenocarcinoma after surgical resection. Bronchoscopy
Table 1—Clinical Characteristics of Patients* Characteristics Age, yr Lymphadenopathy with parenchymal lesion Multiple lymphadenopathy Size, mm 10–20 ⬎ 20 Location of the penetrated lymph node Paratracheal Pretracheal Retrotracheal Tracheobronchial Subcarinal Hilar
EBUS-D (n ⫽ 29)
EBUS-S (n ⫽ 25)
p Value
66.5 ⫾ 13.5 19 (65)
63.5 ⫾ 10.2 16 (64)
0.35 0.91
10 (40) 24.6 ⫾ 5.0 11 (38) 18 (62)
12 (48) 24.4 ⫾ 6.7 10 (40) 15 (60)
0.57 0.92 0.56 0.56
5 (17) 14 (48) 0 (0) 2 (8) 2 (8) 6 (21)
4 (16) 10 (40) 1 (4) 1 (4) 3 (12) 6 (24)
0.62
Discussion
*Data are presented as mean ⫾ SE or No. (%).
As shown in Table 3, although there were no statistically significant differences in the diagnostic rate of first passes (75.9% vs 64.0%, respectively; p ⫽ 0.34), the diagnostic rate of second passes in the EBUS-D group was higher than that in the EBUS-S group (87.5% vs 33.3%, respectively; p ⫽ 0.036). In the EBUS-D group, 22 of the initial 29 needle passes (75.9%) were positioned accurately within the target lymph node. Six of an initial 11 passes (54.5%) were confirmed by EBUS in the small lymph node group, and 16 of 18 passes (88.9%) in the large lymph node group. Although all of the subsequent five passes in the small lymph node group were confirmed to be positioned accurately, diagnosis was not obtained in one patient. Two of the subsequent two passes in the large lymph node group were confirmed, and diag-
Table 2—Firm Diagnosis and Diagnostic Rate of TBNA* Variables
EBUS-D (n ⫽ 29)
EBUS-S (n ⫽ 25)
Squamous cell carcinoma Small cell carcinoma Adenocarcinoma Lymphoma Tuberculosis Silicosis Sarcoidosis Inflammation Total‡
3 7 (1)† 12 (4)† 0 1 1 2 2 28 (97)
1 6 9 (1)† 1 1 0 0 1 (1)† 19 (76)§
*Data are presented as No. unless otherwise indicated. The total diagnostic rate for the EBUS-D group was significantly higher than that of the EBUS-S group (p ⫽ 0.025). †Data are presented as No. (No. of cytology diagnoses). ‡Data are presented as No. (%). §p ⫽ 0.025. www.chestjournal.org
nosis was successful. In the EBUS-S group, 12 of an initial 15 TBNAs (80%) in the large lymph node group and 4 of an initial 10 TBNAs (40%) in the small lymph node group yielded an accurate diagnoses. Only two of a subsequent six TBNAs (33.3%) were diagnosed in the small lymph node group and one of a subsequent three TBNAs (33.3%) in the large lymph node group. The number of penetrations required to establish diagnosis was 1.24 in the EBUS-D group and 1.36 in the EBUS-S group. No complications were observed in the EBUS-D group, but a self-limiting hemorrhage ⬍ 30 mL occurred in a patient in the EBUS-S group.
An accurate understanding of the position of the target lesion is essential to improve the diagnostic rate of TBNA, because failure to place the needle within the lesion is the leading cause of a low biopsy yield.14 The advent of new technologies such as EBUS and CT fluoroscopy has led to the concept of integration with TBNA to improve the diagnostic yield.6,9 –11 Although EBUS images show target lesions beyond the airway, needle penetration of the target lesion could not be proved by EBUS using a single-channel bronchoscope. To confirm whether the target lesion was aspirated, rapid on-site cytopathology was needed immediately after aspiration.15–17 In this study, high diagnostic rates were established by EBUS-D without requiring rapid on-site cytopathology because the real-time EBUS image confirmed that the TBNA needle was within the lesion, in which it offered as a hyperechoic point. An advantage of EBUS-D is that if the TBNA needle is not placed correctly on the first penetration, relocation of the penetration site can be easily performed without replacing the TBNA catheter and EBUS probe through the working channel. Factors reported to influence the diagnostic rate of TBNA were the site of the lymphadenopathy sampled,18 use of a histology needle,19,20 bronchoscopic findings at the penetration site such as carinal widening, extrinsic airway compression, submucosal invasion,21 and the increasing numbers of TBNA trials.17,21 In the present study, there were no significant differences for the EBUS-D and EBUS-S groups in the above conditions in each group. As rapid on-site cytopathology also contributes to the improvement of the diagnostic rate of TBNA,15–17 the use of rapid on-site cytopathology in our EBUS-S group might have led to a higher diagnostic rate. Several investigations recommended that the number of aspirations per lesion with a cytology needle should be four to seven,17 or at least three21 for each CHEST / 128 / 1 / JULY, 2005
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Table 3—Diagnostic Rate According to Lymph Node Size and Number of Passes* EBUS-D Variables Small lymph node (10 to 20 mm) Large lymph node (⬎ 20 mm) Total
First (n ⫽ 29) 6/11 (54.4) 16/18 (88.9) 22/29 (75.9)†
EBUS-S Second (n ⫽ 7) 4/5 (80.0) 2/2 (100 ) 6/7 (85.7)‡
First (n ⫽ 25)
Second (n ⫽ 9)
4/10 (40.0) 12/15 (80.0) 16/25 (64.0)
2/6 (33.3) 1/3 (33.3) 3/9 (33.3)
*Data are presented as No./total (%). †p ⫽ 0.34. ‡p ⫽ 0.036.
target lymph node in the conventional TBNA. Shannon et al9 reported that EBUS-guided TBNA exhibited a similarly high diagnostic rate to conventional TBNA, and decreased the number of aspirations for paratracheal lymph node sampling (mean [⫾SD], 2.00 ⫾ 0.20 aspirations vs 2.91 ⫾ 0.34 aspirations, respectively; p ⫽ 0.03). In the present study, the mean number of aspirations to establish diagnosis was 1.24 in the EBUS-D group. This means that EBUS guidance is useful in decreasing the number of aspirations when rapid on-cite cytopathology is not available, and that EBUS guidance spares patients from risks such as hemorrhage from unnecessary additional TBNA puncture. Another adjunctive imaging technique to visualize the TBNA needle within the lesion, CT fluoroscopy guidance, has been reported.22–24 The diagnostic rate of CT fluoroscopy-guided TBNA (74.1% as reported by White et al,22 and 68.7% as reported by Garpestad et al23) was lower than that of EBUS-guided TBNA reported by Shannon et al (82.6%),9 Herth et al (86%),11 and also our EBUS-D results. Moreover, the three to four penetrations per lesion that were required with CT fluoroscopy-guided TBNA and CT fluoroscopy has the disadvantage of radiation exposure to the patients and the operators. According to Goldberg et al,24 CT fluoroscopy confirmed that only 6 of the initial 18 needle passes (33%) were positioned properly within the target lesion. With CT fluoroscopy guidance, the rate of subsequent successful passes increased to 62%. In contrast, needle confirmation in the initial trial of EBUS-D was higher (75.9%), and 100% confirmation of needle placement within the lesion was achieved in a subsequent trial (data were shown). Additionally, although six penetrations (5.2%) punctured great vessels with CT fluoroscopy guidance,24 there was no accidental puncture in the EBUS-D group. EBUS guidance using the double-channel bronchoscope also has its limitations. The double-channel bronchoscope (7.2 mm in diameter) may not be well tolerated by all patients. However, in our experience, transoral insertion encountered no serious problems, even though Japanese people are usually of slighter 392
stature than many Westerners. No endotracheal tube was used, and this scope is used exclusively for EBUS-guided TBNA. Furthermore, since our transducer was of the radial type, we could not see the entire course of the needle within the lesion. We are currently performing TBNA using a convex type ultrasonic bronchoscope, which shows the image of the needle course within the lesion.25,26 Its outer diameter is 6.9 mm, and it has a small curved array transducer located in front of a 30° oblique forward viewing optic lens and a biopsy channel of 2 mm. It was reported to be useful in the diagnosis of thoracic diseases.25,26 It may be easier to penetrate the target lymph node using the ultrasonic bronchoscope than with the EBUS-D because the entire puncture procedure of the target lesion is performed under direct ultrasound guidance. However, it is difficult to obtain a histologic diagnosis with the convex type ultrasonic bronchoscope because only a 22-gauge needle can be used for sampling. The 22-gauge needle has been reported to be inferior to the 19-gauge needle in the diagnostic rate.19 Therefore, in cases requiring cytology such as staging of lung cancer and diagnosis for suspected malignancy, the ultrasound bronchoscope will be useful. Otherwise, EBUS-guided TBNA in this study could easily enable histologic diagnosis with the 19-gauge histology needle, and is able to establish the diagnosis of benign diseases such as sarcoidosis, silicosis, and tuberculosis. Transesophageal lymph node sampling under endoscopic ultrasound guidance fine-needle aspiration 27–29 can also generate the image of course of the needle. Endoscopic ultrasound through the esophagus gives access to the subcarinal, aortopulmonary, and posterior mediastinum lymph nodes. However, the images of paratracheal and anterior mediastinal lesions are limited by distortion caused by the intratracheal airspace, and the hilar lymph nodes cannot be accessed from the esophagus. In contrast, EBUS guidance allows access to such limited locations with under endoscopic ultrasound guidance fine-needle aspiration. Furthermore, the target lymph node can Bronchoscopy
be detected more readily through the tracheobronchial tree because it has many points of orientation. The weak point of our study was that the locations of the penetrated lymph nodes were not exactly equalized. If many patients with lymphadenopathy in the left paratracheal/aortopulmonary window had been included in this study, the diagnostic rate might be decreased because TBNA in this location is more difficult than in any other site. By visualizing TBNA needle placement, operators will have more confidence in attempting biopsies as well as less fear of puncturing major vessels, and the specimen obtained by use of the TBNA needle placement with real-time confirmation will yield an accurate diagnosis with a decreasing number of penetrations. ACKNOWLEDGMENT: The authors thank Professor J. Patrick Barron of the International Medical Communication Center of Tokyo Medical University for his review of this article.
References 1 Harrow EM, Abi-Saleh W, Blum J, et al. The utility of transbronchial needle aspiration in the staging of bronchogenic carcinoma. Am J Respir Crit Care Med 2000; 161:601– 607 2 Gasparini S, Ferretti M, Secchi EB, et al. Integration of transbronchial and percutaneous approach in the diagnosis of peripheral pulmonary nodules or masses. Chest 1995; 108: 131–137 3 Dasgupta A, Jain P, Minai OA, et al. Utility of transbronchial needle aspiration in the diagnosis of endobronchial lesions. Chest 1999; 115:1237–1241 4 Shure D, Fedullo PF. Transbronchial needle aspiration in the diagnosis of submucosal and peribronchial bronchogenic carcinoma. Chest 1985; 88:1:49 –51 5 Becker HD, Herth F. Endobronchial ultrasound of the airways and mediastinum. In: Bolliger CT, Mathur PN, eds. Interventional bronchoscopy (vol 30). Basel, Switzerland: Karger, 2000; 80 –93 6 Goldberg BB, Steiner RM, Liu JB, et al. US-assisted bronchoscopy with use of miniature transducer-containing catheters. Radiology 1994; 190:233–237 7 Kurimoto N, Murayama M, Yoshioka S, et al. Assessment of usefulness of endobronchial ultrasonography in determination of depth of tracheobronchial tumor invasion. Chest 1999; 115:1500 –1506 8 Miyazu Y, Miyazawa T, Kurimoto N, et al. Endobronchial ultrasonography in the assessment of centrally located earlystage lung cancer before photodynamic therapy. Am J Respir Crit Care Med 2002; 165:832– 837 9 Shannon JJ, Bude RO, Orens JB, et al. Endobronchial ultrasound-guided needle aspiration of mediastinal adenopathy. Am J Respir Crit Care Med 1996; 153:1424 –1430 10 Kanoh K, Kurimoto N, Miyazawa T, et al. A case of real-time endobronchial ultrasonography-guided bronchial needle aspi-
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ration using a double-channel flexible bronchoscope. J Bronchiol 2002; 9:112–114 Herth FJ, Becker HD, Ernst A. Ultrasound-guided transbronchial needle aspiration: an experience in 242 patients. Chest 2003; 123:604 – 607 Falcone F, Fois F, Grosso D. Endobronchial ultrasound. Respiration 2003; 70:179 –194 Herth FJ, Becker HD, Ernst A. Conventional vs endobronchial ultrasound-guided transbronchial needle aspiration: a randomized trial. Chest 2004; 125:322–325 Wang KP. Continued efforts to improve the sensitivity of transbronchial needle aspiration. Chest 1998; 114:4 –5 Davenport RD. Rapid on-site evaluation of transbronchial aspirates. Chest 1990; 98:59 – 61 Diette GB, White P Jr, Terry P, et al. Utility of on-site cytopathology assessment for bronchoscopic evaluation of lung masses and adenopathy. Chest 2000; 117:1186 –1190 Chin Jr R, McCain TW, Lucia MA, et al. Transbronchial needle aspiration in diagnosing and staging lung cancer: how many aspirates are needed? Am J Respir Crit Care Med 2002; 166:377–381 Haponik EF, Cappellari JO, Chin R, et al. Education and experience improve transbronchial needle aspiration performance. Am J Respir Crit Care Med 1995; 151:1998 –2002 Schenk DA, Chambers SL, Derdak S, et al. Comparison of the Wang 19-gauge and 22-gauge needles in the mediastinal staging lung cancer. Am Rev Respir Dis 1993; 147: 1251–1258 Mehta AC, Kavuru MS, Meeker DP, et al. Transbronchial needle aspiration for histology specimens. Chest 1989; 96: 1228 –1232 Shure D. Transbronchial biopsy and needle aspiration. Chest 1989; 95:1130 –1138 White CS, Weiner EA, Patel P, et al. Transbronchial needle aspiration: guidance with CT fluoroscopy. Chest 2000; 118: 1630 –1638 Garpestad E, Goldberg SN, Herth F, et al. CT fluoroscopy guidance for transbronchial needle aspiration: an experience in 35 patients. Chest 2001; 119:329 –332 Goldberg SN, Raptopoulos V, Boiselle PM, et al. Mediastinal lymphadenopathy: diagnostic yield of transbronchial mediastinal lymph node biopsy with CT fluoroscopic guidance-initial experience. Radiology 2000; 216:764 –767 Krasnik M, Vilmann P, Larsen SS, et al. Preliminary experience with a new method of endoscopic transbronchial real time ultrasound guided biopsy for diagnosis of mediastinal and hilar lesions. Thorax 2003; 58:1083–1086 Ono R, Suemasu K, Matsunaka T. Bronchoscopic ultrasonography in the diagnosis of lung cancer. Jpn J Clin Oncol 1993; 23:34 – 40 Roberts SA. Obtaining tissue from the mediastinum: endoscopic ultrasound guided transesophageal biopsy. Thorax 2000; 55:983–985 Wallance MB, Silvestri GA, Sahai AV, et al. Endoscopic ultrasound-guided fine needle aspiration for staging patients with carcinoma of the lung. Ann Thorac Surg 2001; 72:1861– 1867 Fritscher-Ravens A, Soehendra N, Schirrow L, et al. Role of transesophageal endosonography-guided fine-needle aspiration in the diagnosis of lung cancer. Chest 2000; 117:339 –345
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Study objectives: Endobronchial ultrasonography (EBUS) is used as guidance for transbronchial needle aspiration (TBNA), and real-time imaging of the needle position cannot be confirmed with a single-channel bronchoscope. We assessed the usefulness of EBUS-guided TBNA using a double-channel bronchoscope (EBUS-D), which provides real-time needle position, and compared it with EBUS-guided TBNA using a single-channel bronchoscope (EBUS-S). Design: Randomized, comparative prospective study. Setting: Hiroshima City Hospital, a tertiary-referral teaching hospital. Patients: Between January 2000 and August 2003, 55 patients with intrathoracic lymphadenopathy were included. Patients were randomized to undergo EBUS-D (n ⴝ 30) or EBUS-S (n ⴝ 25). Methods: EBUS-D: The EBUS probe and TBNA catheter were inserted simultaneously through a double-channel bronchoscope. Once the needle placement in the lesion was confirmed by EBUS, TBNA was performed. EBUS-S: The EBUS probe was removed after the determination of the penetration site. Then, the TBNA catheter was inserted and TBNA was performed. Results: All the lymph nodes could be visualized with EBUS in each group of patients. In the EBUS-D group, the TBNA needle was visualized as a hyperechoic point on the real-time EBUS image. The diagnostic accuracy rate of EBUS-D and EBUS-S were statistically significantly different (97% vs 76%, respectively; p ⴝ 0.025). On second attempt of TBNA, the diagnostic rate of the EBUS-D group was superior to that of the EBUS-S group (85.7% vs 33.3%, respectively; p ⴝ 0.036). The mean number of penetrations was 1.24 in the EBUS-D group and 1.36 in the EBUS-S group. No complications were observed in the EBUS-D group, but a self-limiting hemorrhage occurred in a patient in the EBUS-S group. Conclusion: EBUS-D is useful for diagnosing intrathoracic lymphadenopathy, and the obtained specimen with real-time confirmation of the needle is directly proportional to an accurate diagnosis. (CHEST 2005; 128:388 –393) Key words: bronchoscopy; intrathoracic lymphadenopathy; endobronchial ultrasonography; transbronchial needle aspiration Abbreviations: EBUS ⫽ endobronchial ultrasonography; EBUS-D ⫽ endobronchial ultrasonography-guided transbronchial needle aspiration using a double-channel bronchoscope; EBUS-S ⫽ endobronchial ultrasonography-guided transbronchial needle aspiration using a single-channel bronchoscope; TBNA ⫽ transbronchial needle aspiration
use of transbronchial needle aspiration T he(TBNA) in addition to routine bronchoscopy was reported to improve the diagnostic rate for malig-
nancies.1– 4 As target lymph nodes cannot be visualized directly with the conventional TBNA procedure, aspiration efforts are directed by knowledge of
*From the Department of Internal Medicine (Dr. Kanoh), Fukushima Co-op Hospital, Hiroshima; the Department of Pulmonary Medicine (Drs. Miyazawa, Iwamoto, and Miyazu), Hiroshima City Hospital, Hiroshima; the Department of Molecular and Internal Medicine (Dr. Kohno), Graduate School of Biomedical Sciences, Hiroshima University, Hiroshima; and the Department of Surgery (Dr. Kurimoto), Hiroshima National Hospital, Higashi-Hiroshima, Japan. This study was performed at Hiroshima City Hospital, a tertiaryreferral teaching hospital, Hiroshima, Japan.
Manuscript received January 29, 2004; revision accepted June 30, 2004. Reproduction of this article is prohibited without written permission from the American College of Chest Physicians (www.chestjournal. org/misc/reprints.shtml). Correspondence to: Teruomi Miyazawa, MD, PhD, FCCP, Director, Department of Pulmonary Medicine, Hiroshima City Hospital, 7–33 Motomachi, Naka-ku, Hiroshima, Japan; e-mail: [email protected]
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thoracic anatomy and prior CT imaging. Multiple needle passes are required for each target because there is the possibility of error in puncturing the target lesion. Therefore, the diagnostic rate of TBNA seems to be related to the lymph node size and location as well as the operator’s experience. With the development of new technology, endobronchial ultrasonography (EBUS) is reported to be useful in detecting mediastinal and hilar lymphadenopathy in addition to assessing the depth of tracheobronchial tumor invasion.5– 8 Recently, EBUS has also been used for TBNA guidance and has improved the results of N-staging, especially in difficult lymph node levels without any clear endoscopic landmarks.9 –13 However, Shannon et al9 reported that EBUS guidance did not offer a statistically significant advantage when compared with conventional TBNA because the sensitivities of both procedures were extremely high (82.6% vs 90.5%, respectively). However, Herth, et al13 reported that EBUS guidance significantly increased the yield of TBNA in the mediastinal lymph node except for subcarinal lymph node in their randomized trial (84% vs 58%). The main disadvantage of EBUS guidance using a single-channel bronchoscope is that a real-time imaging of the needle position within the target lesion cannot be confirmed because the EBUS probe must be removed during the TBNA procedure. To overcome this problem, a double-channel bronchoscope, through which both a TBNA catheter and an EBUS probe can be inserted simultaneously, was necessary. This study assessed the usefulness of EBUS-guided TBNA using a double-channel bronchoscope (EBUS-D) or EBUS-guided TBNA using a single-channel bronchoscope (EBUS-S). Materials and Methods
sheath was inserted through the 2.8-mm channel. The balloon was subsequently filled with sterile water to eliminate the air between the lesion and the probe. We evaluated the target lesion and determined the penetration site. Then, a 19-gauge TBNA catheter (Wang transbronchial histology needle, MWF-319 or MW-319; Mill-Rose Laboratories; Mentor, OH) was inserted through the 2.0-mm channel after the EBUS probe was retracted to the bronchoscope tip to prevent possible damage by the TBNA needle. Once the needle was introduced through the bronchial wall, the EBUS probe was again advanced to the penetration point along the tracheobronchial wall (Fig 1, 2, top left, A, and bottom left, C). When the TBNA needle was within the lesion, the real-time EBUS image of the needle was a hyperechoic point in the lesion (Fig 2, top right, B, and bottom right, D). If the TBNA needle was not confirmed to be inside the lesion by EBUS on the first attempt, a subsequent penetration was attempted while changing the penetration site. Specimens in the TBNA needle were flushed by air. Histology specimens were fixed in formalin, and cytology specimens were smeared on glass slides and fixed in alcohol before sending to the pathology department. EBUS-S: The EBUS probe was inserted through a singlechannel flexible bronchoscope (BF-1T-30; Olympus). Once the penetration site was determined following the same procedure used for EBUS-D, the EBUS probe was removed through the bronchoscope. Next, the TBNA catheter was inserted through the channel and TBNA was performed. The specimens in the TBNA needle were flushed by air. If a histologic specimen could not be obtained on the first aspiration, a second TBNA was attempted. We did not utilize fluoroscopy or rapid on-site cytopathology evaluation in either study group. Statistical Methods Student t test was used to compare the mean age and size of the lymph node. The 2 test was used to compare the rate of patients with a parenchymal lesion, those with multiple lymphadenopathies, the lymph node locations undergoing TBNA, and the diagnostic rate of EBUS-D and EBUS-S. A statistical software package (SAS, version 8.2; SAS Institute; Cary, NC) for categorical variables was used for all analyses. A p value ⬍ 0.05 was significant difference.
Results The patient characteristics are shown in Table 1. There were no significant differences between the
Patients We enrolled 55 patients with mediastinal and/or hilar lymphadenopathy in this prospective study between January 2000 and August 2003. The indication for TBNA was the diagnosis of an enlarged lymph node. Patients were randomized to undergo EBUS-D (n ⫽ 30) or EBUS-S (n ⫽ 25). This study was approved by the Committee on Human Research of our institution. Written informed consent was obtained from all patients. Procedure EBUS-D: An ultrasonic probe (2.5 mm in diameter, radial mechanical transducer operating at 20 MHz) [UM-BS20 –26R; Olympus; Tokyo, Japan] with a flexible balloon sheath (MAJ643R; Olympus) was connected to an ultrasound unit (EU-M 20; Olympus). A flexible bronchoscope (external diameter, 7.2 mm) [XBF-2T40Y2; Olympus] with two channels (diameters, 2.8 mm and 2.0 mm) was inserted transorally, without an endobronchial tube, under local anesthesia. The EBUS probe with a balloon www.chestjournal.org
Figure 1. TBNA catheter and EBUS probe are inserted simultaneously through a double-channel bronchoscope. The EBUS image by the mechanical radial transducer provides a crosssection (dotted line) of the lymph node with the needle inside. CHEST / 128 / 1 / JULY, 2005
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Figure 2. Top left, A: the left catheter shown is the EBUS probe with a balloon sheath, and the right catheter is the TBNA catheter by which a right hilar lymph node was penetrated. Top right, B: the EBUS image obtained without an inflated balloon shows the needle penetrating the lymph node. The needle tip is recognized as a hyperechoic point (arrow), and the acoustic shadow is revealed in the opposite direction of the EBUS probe (arrow head). Sarcoidosis was diagnosed in this patient. Bottom left, C: the left catheter is the EBUS probe, and the right catheter is the TBNA catheter by which the pretracheal lymph node was penetrated. Bottom right, D: the EBUS image shows a hyperechoic point (arrow) and the acoustic shadow (arrow head) in the lesion. Metastatic adenocarcinoma was diagnosed in this patient.
EBUS-D group and the EBUS-S group in the mean age, percentage of cases of a parenchymal lesions with lymphadenopathy, percentage of cases with multiple lymphadenopathies, mean size of the lesion, and percentage of cases with small nodes ⱕ 20 mm. There was also no significant difference in lymph node locations sampled by EBUS-D and EBUS-S. Table 2 shows the diagnostic yield of TBNA. One patient in the EBUS-D group was excluded from this study because liquid had been aspirated from the lesion leading to a diagnosis of a pericardial cyst after surgical resection. Of 29 patients in the EBUS-D group, 23 histologic diagnoses were established. Of the remaining six patients, cytology diagnoses were 390
established in five. Of 25 patients in the EBUS-S group, 17 histologic diagnoses were established. Of the remaining eight patients, only two diagnoses were made using cytology. The diagnostic rate of EBUS-D was significantly higher than that of EBUS-S (97% vs 76%, respectively; p ⫽ 0.025). Six patients without a specific diagnosis (normal bronchial glands and cartilages in two patients, and four patients without lymphocytes on the specimen) in the EBUS-S group had adenocarcinoma (n ⫽ 5) and sarcoidosis (n ⫽ 1) after surgical resection. A patient without a specific diagnosis in the EBUS-D group was found to have adenocarcinoma after surgical resection. Bronchoscopy
Table 1—Clinical Characteristics of Patients* Characteristics Age, yr Lymphadenopathy with parenchymal lesion Multiple lymphadenopathy Size, mm 10–20 ⬎ 20 Location of the penetrated lymph node Paratracheal Pretracheal Retrotracheal Tracheobronchial Subcarinal Hilar
EBUS-D (n ⫽ 29)
EBUS-S (n ⫽ 25)
p Value
66.5 ⫾ 13.5 19 (65)
63.5 ⫾ 10.2 16 (64)
0.35 0.91
10 (40) 24.6 ⫾ 5.0 11 (38) 18 (62)
12 (48) 24.4 ⫾ 6.7 10 (40) 15 (60)
0.57 0.92 0.56 0.56
5 (17) 14 (48) 0 (0) 2 (8) 2 (8) 6 (21)
4 (16) 10 (40) 1 (4) 1 (4) 3 (12) 6 (24)
0.62
Discussion
*Data are presented as mean ⫾ SE or No. (%).
As shown in Table 3, although there were no statistically significant differences in the diagnostic rate of first passes (75.9% vs 64.0%, respectively; p ⫽ 0.34), the diagnostic rate of second passes in the EBUS-D group was higher than that in the EBUS-S group (87.5% vs 33.3%, respectively; p ⫽ 0.036). In the EBUS-D group, 22 of the initial 29 needle passes (75.9%) were positioned accurately within the target lymph node. Six of an initial 11 passes (54.5%) were confirmed by EBUS in the small lymph node group, and 16 of 18 passes (88.9%) in the large lymph node group. Although all of the subsequent five passes in the small lymph node group were confirmed to be positioned accurately, diagnosis was not obtained in one patient. Two of the subsequent two passes in the large lymph node group were confirmed, and diag-
Table 2—Firm Diagnosis and Diagnostic Rate of TBNA* Variables
EBUS-D (n ⫽ 29)
EBUS-S (n ⫽ 25)
Squamous cell carcinoma Small cell carcinoma Adenocarcinoma Lymphoma Tuberculosis Silicosis Sarcoidosis Inflammation Total‡
3 7 (1)† 12 (4)† 0 1 1 2 2 28 (97)
1 6 9 (1)† 1 1 0 0 1 (1)† 19 (76)§
*Data are presented as No. unless otherwise indicated. The total diagnostic rate for the EBUS-D group was significantly higher than that of the EBUS-S group (p ⫽ 0.025). †Data are presented as No. (No. of cytology diagnoses). ‡Data are presented as No. (%). §p ⫽ 0.025. www.chestjournal.org
nosis was successful. In the EBUS-S group, 12 of an initial 15 TBNAs (80%) in the large lymph node group and 4 of an initial 10 TBNAs (40%) in the small lymph node group yielded an accurate diagnoses. Only two of a subsequent six TBNAs (33.3%) were diagnosed in the small lymph node group and one of a subsequent three TBNAs (33.3%) in the large lymph node group. The number of penetrations required to establish diagnosis was 1.24 in the EBUS-D group and 1.36 in the EBUS-S group. No complications were observed in the EBUS-D group, but a self-limiting hemorrhage ⬍ 30 mL occurred in a patient in the EBUS-S group.
An accurate understanding of the position of the target lesion is essential to improve the diagnostic rate of TBNA, because failure to place the needle within the lesion is the leading cause of a low biopsy yield.14 The advent of new technologies such as EBUS and CT fluoroscopy has led to the concept of integration with TBNA to improve the diagnostic yield.6,9 –11 Although EBUS images show target lesions beyond the airway, needle penetration of the target lesion could not be proved by EBUS using a single-channel bronchoscope. To confirm whether the target lesion was aspirated, rapid on-site cytopathology was needed immediately after aspiration.15–17 In this study, high diagnostic rates were established by EBUS-D without requiring rapid on-site cytopathology because the real-time EBUS image confirmed that the TBNA needle was within the lesion, in which it offered as a hyperechoic point. An advantage of EBUS-D is that if the TBNA needle is not placed correctly on the first penetration, relocation of the penetration site can be easily performed without replacing the TBNA catheter and EBUS probe through the working channel. Factors reported to influence the diagnostic rate of TBNA were the site of the lymphadenopathy sampled,18 use of a histology needle,19,20 bronchoscopic findings at the penetration site such as carinal widening, extrinsic airway compression, submucosal invasion,21 and the increasing numbers of TBNA trials.17,21 In the present study, there were no significant differences for the EBUS-D and EBUS-S groups in the above conditions in each group. As rapid on-site cytopathology also contributes to the improvement of the diagnostic rate of TBNA,15–17 the use of rapid on-site cytopathology in our EBUS-S group might have led to a higher diagnostic rate. Several investigations recommended that the number of aspirations per lesion with a cytology needle should be four to seven,17 or at least three21 for each CHEST / 128 / 1 / JULY, 2005
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Table 3—Diagnostic Rate According to Lymph Node Size and Number of Passes* EBUS-D Variables Small lymph node (10 to 20 mm) Large lymph node (⬎ 20 mm) Total
First (n ⫽ 29) 6/11 (54.4) 16/18 (88.9) 22/29 (75.9)†
EBUS-S Second (n ⫽ 7) 4/5 (80.0) 2/2 (100 ) 6/7 (85.7)‡
First (n ⫽ 25)
Second (n ⫽ 9)
4/10 (40.0) 12/15 (80.0) 16/25 (64.0)
2/6 (33.3) 1/3 (33.3) 3/9 (33.3)
*Data are presented as No./total (%). †p ⫽ 0.34. ‡p ⫽ 0.036.
target lymph node in the conventional TBNA. Shannon et al9 reported that EBUS-guided TBNA exhibited a similarly high diagnostic rate to conventional TBNA, and decreased the number of aspirations for paratracheal lymph node sampling (mean [⫾SD], 2.00 ⫾ 0.20 aspirations vs 2.91 ⫾ 0.34 aspirations, respectively; p ⫽ 0.03). In the present study, the mean number of aspirations to establish diagnosis was 1.24 in the EBUS-D group. This means that EBUS guidance is useful in decreasing the number of aspirations when rapid on-cite cytopathology is not available, and that EBUS guidance spares patients from risks such as hemorrhage from unnecessary additional TBNA puncture. Another adjunctive imaging technique to visualize the TBNA needle within the lesion, CT fluoroscopy guidance, has been reported.22–24 The diagnostic rate of CT fluoroscopy-guided TBNA (74.1% as reported by White et al,22 and 68.7% as reported by Garpestad et al23) was lower than that of EBUS-guided TBNA reported by Shannon et al (82.6%),9 Herth et al (86%),11 and also our EBUS-D results. Moreover, the three to four penetrations per lesion that were required with CT fluoroscopy-guided TBNA and CT fluoroscopy has the disadvantage of radiation exposure to the patients and the operators. According to Goldberg et al,24 CT fluoroscopy confirmed that only 6 of the initial 18 needle passes (33%) were positioned properly within the target lesion. With CT fluoroscopy guidance, the rate of subsequent successful passes increased to 62%. In contrast, needle confirmation in the initial trial of EBUS-D was higher (75.9%), and 100% confirmation of needle placement within the lesion was achieved in a subsequent trial (data were shown). Additionally, although six penetrations (5.2%) punctured great vessels with CT fluoroscopy guidance,24 there was no accidental puncture in the EBUS-D group. EBUS guidance using the double-channel bronchoscope also has its limitations. The double-channel bronchoscope (7.2 mm in diameter) may not be well tolerated by all patients. However, in our experience, transoral insertion encountered no serious problems, even though Japanese people are usually of slighter 392
stature than many Westerners. No endotracheal tube was used, and this scope is used exclusively for EBUS-guided TBNA. Furthermore, since our transducer was of the radial type, we could not see the entire course of the needle within the lesion. We are currently performing TBNA using a convex type ultrasonic bronchoscope, which shows the image of the needle course within the lesion.25,26 Its outer diameter is 6.9 mm, and it has a small curved array transducer located in front of a 30° oblique forward viewing optic lens and a biopsy channel of 2 mm. It was reported to be useful in the diagnosis of thoracic diseases.25,26 It may be easier to penetrate the target lymph node using the ultrasonic bronchoscope than with the EBUS-D because the entire puncture procedure of the target lesion is performed under direct ultrasound guidance. However, it is difficult to obtain a histologic diagnosis with the convex type ultrasonic bronchoscope because only a 22-gauge needle can be used for sampling. The 22-gauge needle has been reported to be inferior to the 19-gauge needle in the diagnostic rate.19 Therefore, in cases requiring cytology such as staging of lung cancer and diagnosis for suspected malignancy, the ultrasound bronchoscope will be useful. Otherwise, EBUS-guided TBNA in this study could easily enable histologic diagnosis with the 19-gauge histology needle, and is able to establish the diagnosis of benign diseases such as sarcoidosis, silicosis, and tuberculosis. Transesophageal lymph node sampling under endoscopic ultrasound guidance fine-needle aspiration 27–29 can also generate the image of course of the needle. Endoscopic ultrasound through the esophagus gives access to the subcarinal, aortopulmonary, and posterior mediastinum lymph nodes. However, the images of paratracheal and anterior mediastinal lesions are limited by distortion caused by the intratracheal airspace, and the hilar lymph nodes cannot be accessed from the esophagus. In contrast, EBUS guidance allows access to such limited locations with under endoscopic ultrasound guidance fine-needle aspiration. Furthermore, the target lymph node can Bronchoscopy
be detected more readily through the tracheobronchial tree because it has many points of orientation. The weak point of our study was that the locations of the penetrated lymph nodes were not exactly equalized. If many patients with lymphadenopathy in the left paratracheal/aortopulmonary window had been included in this study, the diagnostic rate might be decreased because TBNA in this location is more difficult than in any other site. By visualizing TBNA needle placement, operators will have more confidence in attempting biopsies as well as less fear of puncturing major vessels, and the specimen obtained by use of the TBNA needle placement with real-time confirmation will yield an accurate diagnosis with a decreasing number of penetrations. ACKNOWLEDGMENT: The authors thank Professor J. Patrick Barron of the International Medical Communication Center of Tokyo Medical University for his review of this article.
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