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Eur J Cardiothorac Surg 2000;17:570-574
© 2000 Elsevier Science NL

Evaluation of tracheo-bronchial wall invasion using transbronchial ultrasonography (TBUS)

^a Department of Thoracic Surgery, Faculty of Medicine, Kyoto University, Sakyo-ku, Kyoto, 606-8397, Japan
^b Department of Surgery and Surgical Basic Science, Graduate School of Medicine, Kyoto University, Sakyo-ku, Kyoto, 606-8507, Japan
^c Nara-higashi Hospital, Uenoyama 470, Nakano-sho-machi, Tenri City, Nara, 632-0001, Japan
^d Department of Thoracic Surgery, Faculty of Medicine, Kyoto University, Shogoin-kawara-cho 54, Sakyo-ku, Kyoto, 606-8396, Japan

Corresponding author. Tel.:+81-75-751-3835; fax: +81-75-751-4647
e-mail: wadah{at}kuhp.kyoto-u.ac.jp

	Abstract

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion References

 
Background: Whereas accurate evaluation of tumor invasion into the tracheo-bronchial wall is a critical factor in decision-making of therapy for intra-thoracic malignancies, it is sometimes difficult with usual thoracic imaging techniques such as computed tomography. As recent progress in technology of ultrasonography is marked, usefulness of transbronchial ultrasonography (TBUS) in evaluation of tracheo-bronchial wall invasion was assessed. Methods: Following routine fiberoptic bronchoscopy, an ultrasound probe (20 MHz) covered with a balloon sheath was inserted through the bronchoscope. After air present between the ultrasound probe and the tracheo-bronchial wall was eliminated with filling the balloon with distilled water, TBUS imaging was taken. Results: With TBUS, normal tracheo-bronchial wall was represented as a five-layer structure at the cartilagenous portion and a three-layer structure at the membranous portion. Based on this normal TBUS imaging, tumor extent was judged in 35 patients with intra-thoracic malignancies. Among 25 patients with extra-wall tumor including esophageal cancer (n=15) and metastatic lymph nodes (n=7), tracheo-bronchial wall invasion was clearly demonstrated in nine patients, and no invasion was demonstrated in the other 16 patients. Among ten patients with tumor originating from the tracheo-bronchial wall, tumor extent beyond outer border of the wall was demonstrated with TBUS in five patients. These diagnoses were examined pathologically in 15 patients who underwent the operation, and the accuracy was 93.3%. Conclusions: It is suggested TBUS can be a useful diagnostic tool in evaluation of tumor invasion to the tracheo-bronchial wall.

Key Words: Ultrasonography • Ultrasound • Bronchoscopy • Transbronchial ultrasonography • Invasion • Tracheo-bronchial wall

	1. Introduction

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion References

 
The diagnosis of tumor invasion to the tracheo-bronchial wall is a critical factor in decision-making of therapy for malignant tumors originating from the extra-wall tissue such as the esophagus as well as those originating from the tracheo-bronchial wall [1]. The maximal length of the tracheo-bronchial wall that can be resected and reconstructed is limited, and approximately one half of the trachea can be removed and re-approximated [1,2]. Even when the extent of tumor invasion is shorter, operation risk may be higher if tracheal re-approximation is needed. Especially in case of esophageal carcinoma, both thoracotomy and laparotomy are required for the resection, and combined tracheal resection and re-approximation are usually given up because of the higher operation risk [1,3]. Therefore, accurate diagnostic methods of tracheo-bronchial wall invasion should be established. However, routine diagnostic methods such as computed tomograpy (CT), magnetic resonance imaging (MRI), and bronchoscopy could not revealed the exact depth of tumor invasion because they could not revealed detailed structure of the tracheo-bronchial wall.

Endoscopic ultrasonography is an established diagnostic tool of the depth of tumor invasion in field of the digestive system [4]. In field of the respiratory system, endoscopic ultrasonography has not been developed because air present in the tracheo-bronchial lumen and lung parenchyma interferes with penetration of ultrasound. In 1992, Hurter and coworkers reported the first trial of endobronchial ultrasonography (TBUS), and reported that the bronchial wall was represented as a laminal structure with TBUS [5]. Becker also demonstrated the laminal structure, and reported that TBUS was very useful in evaluation of tumor invasion to the tracheo-bronchial wall [6]. However, TBUS has not been widely used as a routine diagnostic tool, because both sophisticated skill and special instruments were required to perform TBUS. Recently, instruments used for TBUS have been improved, and TBUS can be performed more easily. In the present article, therefore, the efficacy of TBUS in evaluation of tumor invasion to the tracheo-bronchial wall is examined.

	2. Patients and methods

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion References

 
2.1. Study design and patients
A prospective preliminary study to check the efficacy and safety of TBUS was conducted after approval by the Institutional Review Board of Kyoto University. All patients who were admitted to our Departments of Kyoto University Hospital for therapy of histologically confirmed intra-thoracic malignancies and in whom whether the tracheo-bronchial wall was involved with the tumor was not clearly judged with routine chest diagnostic modalities such as CT were selected for the candidates.

After written informed consent was taken, a total of 35 patients from January 1997 to August 1999, were entered into the study. There were 29 males and six females, and the average age was 55.5 years (range: 19–79). Among 35 patients, 25 patients had tumor originating from the extra tracheo-bronchial wall including esophageal carcinoma (n=15), lymph node metastases of bronchogenic carcinoma (n=7), malignant lymphoma (n=2), and thyroid carcinoma (n=1). The other ten patients had tumor originating from the tracheo-bronchial wall including bronchogenic carcinoma (n=9) and adenoid cystic carcinoma of the trachea (n=1). In all patients, chest CT and routine fiberoptic bronchoscopy (FBS) were performed. In all patients with esophageal carcinoma, both esophagoscopy and esophageal ultrasonography (EUS) were performed, which could not revealed whether or not the tracheo-bronchial wall was involved with the tumor.

After all the TBUS findings were informed to patients, the operation was performed to examine the accuracy of the TBUS findings concerning the tracheo-bronchial invasion. In 20 patients among all 35 patients who underwent TBUS, the operation could not be performed because of failure to take informed consent, tumor progression, or poor performance status.

2.2. Procedure of TBUS scanning
Following routine FBS, TBUS scanning was performed. A 20 MHz radial-mechanical type ultrasound probe combined with a balloon (UM-BS20-26R, Olympus Optical Co. Ltd., Tokyo, Japan) was inserted through a fiberoptic bronchoscope. Air present between the ultrasound probe and the bronchial wall was eliminated by filling the balloon with distilled water (Fig. 1), and TBUS imaging was taken using ultrasound units (MH-240 and EU-M30, Olympus Optical Co. Ltd.). During TBUS scanning, the bronchial lumen was obstructed with the dilated balloon. Although TBUS scanning distal to the carina could be performed safely under local anesthesia in all cases, general anesthesia with controlled ventilation was essential in TBUS scanning at the trachea. When TBUS scanning at the trachea is performed, another 20 MHz ultrasound probe (UM-3R, Olympus Optical Co. Ltd.) covered with a bigger balloon sheath (MH-246R, Olympus Optical Co. Ltd.) should be used, because the balloon with UM-BS20-26R was too small to obstruct the trachea. A thicker fiberoptic bronchoscope (BF-ST30 or BF-ST40, Olympus Optical Co. Ltd.) with a bigger channel was also needed to use the UM-3R probe covered with the MH-246R balloon sheath. The arterial oxygen saturation was continuously monitored during entire bronchoscopy including TBUS scanning.

View larger version (99K): [in this window] [in a new window]   Fig. 1. A 20 MHz radial-mechanical type ultrasound probe combined with a balloon (UM-BS20-26R, Olympus Optical Co. Ltd., Tokyo, Japan). The ultrasound probe was inserted through a fiberoptic bronchoscope. Air present between the ultrasound probe and the bronchial wall was eliminated by filling the balloon with distilled water, and TBUS imaging was taken using ultrasound units (MH-240 and EU-M30, Olympus Optical Co. Ltd.).

	3. Results

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion References

View larger version (44K): [in this window] [in a new window]   Fig. 2. (A) A case of esophageal carcinoma. (B) With TBUS, the tracheo-bronchial wall was represented as a five-layer at the cartilagenous portion (1) the first hyperechoic layer at the luminal side corresponding to the marginal echo including the mucous epithelium; (2) the second hypoechoic layer corresponding to the submucosal tissue; (3) the third hyperechoic layer corresponding to the marginal echo on the inner border of the cartilage; (4) the fourth hypoechoic layer corresponding to the cartilage; (5) the fifth hyperechoic layer corresponding to the marginal echo on the outer border), and a 3-layer structure at the membranous portion (1) the first hyperechoic layer demonstrated at the luminal side corresponding to the marginal echo including the mucous epithelium; (2) the second hypoechoic layer corresponding to the submucosal tissue including smooth muscle; (3) the third hyperechoic layer at the outer side corresponding to the outer marginal echo). No tumor invasion was clearly demonstrated with TBUS (*), which was confirmed pathologically. (C) Schema of the TBUS imaging shown in (B).

3.3. Accuracy of TBUS evaluation of tumor invasion
Results of the TBUS findings were shown in the Table 2. With TBUS, tumor invasion to the tracheo-bronchial wall was demonstrated in 21 patients, and not in the other 14 patients. In 15 patients, the operation was performed and pathological examination was performed. In 14 patients among the 15 patients who underwent the operation, the accuracy of the diagnosis taken with TBUS was confirmed pathologically. In 12 patients with negative tumor invasion with TBUS, tumor invasion proved to be negative pathologically. In two patients in whom the membranous portion of the tracheal-bronchial wall was involved with the esophageal carcinoma, the findings were confirmed pathologically.

Therefore, the accuracy of TBUS calculated from the group of patients with histological confirmation was 93.3% (14/15). The sensitivity and the specificity of TBUS were 66.7 and 100.0%, respectively.

	4. Discussion

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion References

 
It has been already reported that ultrasonography is superior to CT or MRI in demonstrating detailed structures of the wall of various tubular organs and in evaluation of the depth of tumor invasion to the wall [4]. In field of digestive system, it has been demonstrated that the wall is represented as a laminal structure with EUS, and the anatomical structures corresponding to each echo layer have been also confirmed. However, anatomical structures corresponding to each layer with TBUS had not been determined. Becker reported that the tracheo-bronchial wall was represented as a 7-layer structure using the same ultrasound probe (20 MHz) as used in the present study. He suggested the corresponding anatomical structures, but no histological evidence was demonstrated [6]. On the other hand, Kurimoto and coworkers have demonstrated the histologically confirmed anatomical structures corresponding to each layer demonstrated with the same 20 MHz ultrasound probe (Table 1) [7].

In only 15 patients among all 35 patients studied, the operation was performed and the TBUS findings were examined histologically. The accuracy, sensitivity, and the specificity of TBUS calculated from the group of 15 patients with histological confirmation were 93.3, 66.7 and 100.0%, respectively. The sensitivity taken in the study was as low as 66.7%, partly because only two patients out of 14 patients in whom tracheo-bronchial wall invasion was judged to be positive with TBUS underwent the operation. Histological confirmation is essential to establish the efficacy of TBUS, which could not be fully examined in the small number of patients who underwent the operation in the present study.

The efficacy of EUS has been already established as a diagnostic tool for determination of depth of tumor invasion and regional lymph node status of esophageal carcinoma, because EUS can clearly visualize the esophageal wall and regional lymph nodes [3,8]. Tio and coworkers compared the efficacy of EUS in evaluation of progression of the esophageal carcinoma with that of CT, and reported the superiority of EUS. The accuracy of evaluation of the tumor extent (T-factor) with EUS was 89%, whereas that with CT was only 59%. The accuracy of evaluation of the regional nodal involvement (N-factor) with EUS was 80%, whereas that with CT was only 50% [9]. Moreover, Chak and coworkers reported that EUS was significantly more accurate than CT scanning in identifying extra-wall invasion of the esophageal carcinoma (87.5 vs. 43.8%, respectively, P=0.0002) [10]. However, EUS was not accurate in diagnosing the tumor invasion to the tracheo-bronchial wall or to the aorta, due to the limited depth of penetration of ultrasound [11,12]. Chest CT and MRI were not accurate in the diagnosis, because they could not visualize the detailed wall structure of the tracheo-bronchus or the aorta. As demonstrated in the present study, TBUS might be most accurate in evaluation of tumor invasion to the tracheo-bronchial wall because TBUS clearly demonstrated the detailed wall structures. Therefore, when tracheo-bronchial wall invasion of esophageal carcinoma is suspected with routine CT, MRI, or bronchoscopy, TBUS may be essential in decision-making of the therapy. At the same time, to confirm the efficacy of TBUS in evaluation of the tracheo-bronchial wall invasion of the esophageal carcinoma, a prospective study with pathological evidence should be conducted.

In one patient who underwent TBUS following preoperative chemo-radiotherapy, it was revealed intraoperatively that scar tissue, post-therapeutic change of cancer tissue, was tightly adhesive to the tracheal wall. Preoperative TBUS demonstrated no tumor in the fourth hypoechoic layer although it demonstrated partial disappearance of the fifth hyperechoic layer. With these findings taken with TBUS, tumor invasion to the tracheal wall was judged to be negative (false negative). Evaluation of tumor invasion to surrounding tissues could be more difficult, when chemotherapy and/or radiotherapy were performed. In such cases, more accurate evaluation of tumor invasion could be done if more detailed structures of the tracheal wall was demonstrated with TBUS. In order to reveal more detailed structures of the tracheo-bronchial wall with TBUS, an ultrasound probe with a higher frequency is needed. Recently, a 30 MHz ultrasound probe (UM-S30-25R) has been just delivered from Olympus Optical Co. Ltd. Using the 30 MHz probe, more detailed structures of the tracheo-bronchial wall can be demonstrated, although the length of penetration of ultrasound is shorter. In further study, normal structure of the tracheo-bronchial wall and evaluation of tumor invasion to the wall will be examined using the 30 MHz ultrasound probe. In conclusion, TBUS can be performed safely, and the efficacy in evaluation of the depth of tumor invasion into tracheo-bronchial wall should be established in further study with sufficient comparison between the TBUS findings and the histological findings.

	Acknowledgments

 
We thank Mr Kenji Hirooka and Mr Kenichi Nishina (Development Group, Ultrasound Products Department, Endoscopic Division, Olympus Optical Co. Ltd., Hachioji, Tokyo, Japan) for helpful discussions. This work was supported in part by a Grant-in-Aid from the JFE (The Japanese Foundation for Research and Promotion of Endoscopy) to an author (F.T).

	Footnotes

 
Presented at the 13th Annual Meeting for the European Association for Cardio-thoracic Surgery, Glasgow, Scotland, UK, September 5–8, 1999.

	References

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion References

 

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