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ABSTRACT |
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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To evaluate the utility of endobronchial ultrasonography (EBUS)
in selecting appropriate candidates with centrally located early-stage lung cancer for photodynamic therapy (PDT) with curative intent, we performed EBUS before PDT in 18 biopsy-proven squamous cell carcinomas (including three carcinoma in situ) that had
been considered to be appropriate candidates for PDT by conventional bronchoscopy and high-resolution computed tomography
(HR-CT). Nine lesions were diagnosed as intracartilaginous by
EBUS and subsequently PDT was performed. Long-term complete
remission has been achieved in these patients with a median follow-up term after PDT of 32 months. The remaining nine lesions
were diagnosed as extracartilaginous by EBUS and were considered
candidates for other therapies such as surgical resection, chemotherapy, and radiotherapy, although two were invisible by HR-CT,
three were superficial, and five were 
1 cm in diameter on observation by bronchoscopy. The depth of tumor invasion estimated by
EBUS was proven to be accurate by histopathologic findings in six
specimens after surgical resection. We conclude that EBUS is a useful technique that might be considered in addition to conventional bronchoscopy and HR-CT to improve the efficacy of PDT in
patients with centrally located early-stage lung cancer.
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INTRODUCTION
METHODS
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DISCUSSION
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Keywords: endobronchial ultrasonography; photodynamic therapy; early-stage lung cancer; high-resolution computed tomography
With a number of recent technical developments and the availability of new instruments, the diagnosis and therapy for early-stage lung cancer have improved considerably (1). Other than surgical resection, photodynamic therapy (PDT) may be one of the best approaches for early-stage lung cancer at this time (2, 3). It has been confirmed that PDT has curative potential in patients with centrally located early-stage lung cancer (4-10). Many criteria in selecting the appropriate candidates for curative intent of PDT have been reported. Bronchoscopic diagnosis is accepted as one of the most important criteria (7, 10), based on statistical data indicating that lesions less than 1.0 cm have a high likelihood of achieving a complete remission (CR) after PDT.
However, local recurrences or subsequent metastases can develop in patients with early-stage lung cancer who achieved a CR with PDT (10, 11), and thus the ability of PDT to produce long-term remission has been reported to be as low as 30% to 50% (6, 11, 12). Because tumors confined to the mucosa and submucosa rarely have lymph node metastases (13, 14), and because laser beams cannot penetrate the exterior wall of the cartilage, it is important for the tumor to be confined within the mucosa and submucosa for successful PDT. Hence, improving the assessment of the depth of the tumor invasion into the bronchial wall will likely improve the quality and efficacy of PDT. We believe that endobronchial ultrasonography (EBUS) may be a useful adjunct for this purpose.
High-frequency ultrasound endoscopy of the gastrointestinal system has been proven to be the best noninvasive method to assess the depth of tumor invasion. In the bronchial system, the normal layered structure of the bronchial wall of the central airway as it appears under EBUS has been reported (15-19), making it possible to evaluate the depth of tumor invasion. We have reported, from a comparison with histopathologic findings, that the accuracy of EBUS in the determination of depth of tumor invasion was 95.8% (17). Thus, the possibility of evaluating the depth of tumor invasion of bronchial wall has come to be realized as feasible. Recently we have reported a clinical trial using autofluorescence bronchoscopy (AFB) and EBUS for centrally located early-stage lung cancer; EBUS facilitated the diagnosis in addition to AFB (19).
In this study, the aim was to select appropriate candidates for PDT with curative intent in patients with centrally located early-stage lung cancer based on an assessment using EBUS, in addition to conventional bronchoscopy and high-resolution computed tomography (HR-CT).
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METHODS |
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
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Selection of Patients
Between September 1997 and August 2001 we carried out a prospective study at Hiroshima City Hospital. We performed conventional white light bronchoscopy (WLB) in 1,779 patients. Of these, 93 patients underwent autofluorescence bronchoscopy (LIFE; laser-induced fluorescence endoscopy system, Xillix Technologies Corporation, Vancouver, Canada) as an adjunct to WLB, because they were felt to have an increased risk of developing lung cancer (e.g., a history of previous treatment for bronchogenic carcinoma or positive findings on sputum cytology and/or hemoptysis).
Twelve of these patients had 18 biopsy-proven squamous cell carcinomas, which satisfied the criteria of a centrally located early-stage
lung cancer (5, 6) and were selected for this study. The criteria were a
negative chest roentgenogram, no nodal enlargement on CT (clinical
stage, Tis or T1, N0M0), an intraluminal tumor size 2 cm, and a visible proximal and distal margin.
Evaluation of Tumor Before PDT
All patients had a HR-CT scan (Hi-Speed Advantage, General Electric Medical Systems, Milwaukee, WI). The images were evaluated by two experienced radiologists, and the depth of tumor invasion by HR-CT was divided into three categories using the methods of Sutedja and coworkers (20, 21): IV, invisible; IL, strictly intraluminal; EL, signs of extraluminal tumor.
Bronchoscopy was performed and the tumors were assessed in terms of location and size. The bronchoscopic appearance of each tumor was classified as being S, superficial type; N, nodular type; or P, polypoid type.
EBUS was performed under local anesthesia. For the endobronchial ultrasonography (EU-M 20; Olympus, Tokyo, Japan), a 2.5-mm-diameter, 20-MHz frequency radial mechanical transducer type ultrasonic probe (UM-BS20-26R; Olympus) and a flexible balloon sheath that was equipped with a balloon at the tip (MAJ-643R; Olympus) were utilized. We introduced them through the 2.8-mm-diameter channel of a flexible bronchoscope (BF-1T20; Olympus). The image by EBUS revealed the layered structure of the tracheobronchial wall. The depth of tumor invasion into the bronchial wall was determined by observation of the cartilage layer and was divided into two categories: intracartilaginous or extracartilaginous (Figure 1). If the tumor was intracartilaginous, indicating that the tumor was contained within the mucosa and/or submucosa, the lesion was considered suitable for PDT. On the other hand, if the depth of tumor invasion was extracartilaginous, indicating that the tumor extended beyond the cartilage, alternative therapies, such as surgical resection, chemotherapy, and radiotherapy, were employed.
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Comparison of the Depth of Tumor Invasion by EBUS with Histopathologic Findings
We compared previously in vivo EBUS imaged sections with postoperative extra vivo sections also imaged by EBUS, and contrasted the histopathologic findings after surgery. In the cases that received PDT there was obviously no specimen for histopathologic examination. This procedure involved only surgical candidates.
Photodynamic Therapy and Follow-up
All tumors judged to be suitable for PDT were treated by PDT according to the method described by Hayata and coworkers (9). After achieving complete remission by PDT, both HR-CT and bronchoscopy, which involved endoscopes, and cytologic and histologic studies were repeated at three-month intervals during the first year after treatment, at six-month intervals in the second year, and once a year thereafter.
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RESULTS |
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Table 1 shows the characteristics of these 12 patients and the reasons for the discovery of their tumors. The broncoscopy, HR-CT, and EBUS results of all 18 tumors including three carcinoma in situ (CIS) are given in Table 2. All 18 lesions were considered to be candidates for PDT according to bronchoscopy and HR-CT. Two CIS and one squamous cell carcinoma were seen using only AFB and were missed with conventional WLB. According to the evaluation by EBUS, 9 of these 18 lesions including three CIS were diagnosed as intracartilaginous, because the cartilage was not involved by the tumor. Therefore these tumors were considered candidates for PDT and were subsequently treated by PDT. In this subgroup, the CR rate of PDT was 100%. Long-term complete remission has been achieved in all patients with a median follow-up term after PDT of 32.0 ± 14.0 months.
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The remaining nine lesions were diagnosed as extracartilaginous based on the assessment by EBUS, because the cartilage was invaded by the tumor and were considered candidates for alternative therapies. Six of nine patients were considered candidates for surgery and underwent surgical resection. Resected tissue specimens revealed that the depth of tumor invasion estimated by EBUS and the histopathologic findings were identical in six patients. None of these patients has developed a recurrence (median follow-up: 22.3 ± 13.8 months). Because the remaining three patients were considered to be a high surgical risk, they were treated with PDT plus chemotherapy (one patient), PDT plus radiotherapy (one patient), or PDT plus chemotherapy and radiotherapy (one patient). All achieved CR and remain disease free (median follow-up: 24.0 ± 18.4 months).
The depth of tumor invasion estimated by HR-CT indicated that 11 lesions were invisible, three lesions were strictly intraluminal, and four lesions had slight changes indicating extraluminal spread. Two of the 11 lesions, although they were invisible on HR-CT, invaded beyond the cartilage as shown by EBUS.
The relationship between the bronchoscopic appearance and the depth of tumor invasion estimated by EBUS is shown in Table 3. Ten lesions were bronchoscopically superficial types, three were nodular types, and five were polypoid types. In spite of the superficial lesions on bronchoscopy, three tumors invaded beyond the cartilage as shown by EBUS. In these cases, bronchial surface was edematous with irregular thickening, but the precise tumor margin was difficult to assess bronchoscopically.
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The relationship between the bronchoscopic diameter of the tumor and the depth of tumor invasion estimated by EBUS is given in Table 4. Although 14 lesions were < 1 cm in diameter as determined by bronchoscopy, five lesions protruded beyond the cartilage when imaged by EBUS.
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Three typical cases are shown in Figures 2-5. Each was an early-stage, biopsy-proven squamous cell carcinoma. Information obtained by broncoscopy and HR-CT was compared with EBUS.
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Figure 2 shows a case of CIS. Bronchoscopy revealed irregular thickness at the spur between the superior and lingual bronchi of the left upper lobe (Figure 2A). The lesion was invisible on HR-CT and EBUS (Figures 2B and 2C). This patient was considered to be a suitable candidate for PDT and was treated by PDT.
Figure 3 depicts a squamous cell carcinoma at the spur between the B1 + 2 and B3 bronchi of the left upper lobe. By bronchoscopy, this area was slightly raised (Figure 3A) but the tumor was not visible on HR-CT (Figure 3B). The tumor was confined within the submucosal tissue by EBUS and therefore was diagnosed as intracartilaginous (Figure 3C). This patient was also considered to be a suitable candidate for PDT and was treated by PDT.
Figure 4 shows a case of squamous cell carcinoma at the orifice of the right B6. Under bronchoscopy, the tumor appeared superficial and slightly reddish, although it was initially missed by WLB and first detected by AFB (Figure 4A). HR-CT showed an obscure lesion at the site, and because of little contrast between the lesion and the surrounding mediastinal connective tissue, we diagnosed it as invisible (Figure 4B). The cartilage layer was involved and interrupted by the tumor when observed by EBUS, and this tumor was diagnosed as extracartilaginous (Figure 4C). Although the size of the tumor was < 1 cm by bronchoscopy, it had invaded beyond the cartilage when imaged by EBUS. Thus, this patient was considered to be a candidate for surgical resection and a lower lobectomy was performed. Because the histologic findings in the resected specimens showed that the tumor invasion was beyond the cartilage, it was proven that the evaluation of depth of tumor invasion by EBUS was correct. The histologic findings showed that the shape of tumor and depth of tumor invasion were revealed to be exactly as indicated in the EBUS image (Figure 5). The EBUS diagnosis of the depth of tumor invasion was proven accurate based on the results of histopathologic findings in the other resected specimens.
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DISCUSSION |
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
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The use of EBUS for the evaluation of depth of tumor invasion in patients with centrally located early-stage lung cancer may improve the efficacy of PDT. In this study, all selected lesions had been diagnosed as suitable candidates for PDT by bronchoscopy and HR-CT, but a number of them proved to be not appropriate for PDT. The tumors diagnosed as intracartilaginous by EBUS were successfully treated with PDT. EBUS provides more accurate information about the depth of tumor invasion than conventional bronchoscopy and HR-CT. Whether PDT will achieve complete remission in a patient greatly depends on accurate patient selection based on an exact assessment of a tumor's dimensions (11, 12, 19, 22). The depth of tumor invasion is an important factor for the success of PDT as well as tumor location, size, and lack of nodal involvement.
Tumors < 2.0 cm are reported to have less than a 10% chance of having lymph node metastasis based on surgical specimens (13, 14). In addition, it has been reported that for bronchoscopically superficial tumors with a surface diameter < 1.0 cm or nodular tumors with a surface diameter < 0.5 cm, complete remission can be achieved with PDT (7, 10). Therefore, bronchoscopic evaluation has been recognized as vital in the successful application of PDT. In the present study, the depth of tumor invasion as estimated by surface diameter was not always accurate when histopathologic specimens were examined. We have found five tumors < 1.0 cm that have shown extracartilaginous invasion by EBUS image that was later confirmed histopathologically. Also three tumors appeared bronchoscopically superficial but were shown to be extracartilaginous by EBUS. Tumors with extracartilaginous invasion have been reported to have intrapulmonary lymph node and hilar lymph node metastases in 6.4% of cases (13). On the other hand, if there is no extracartilaginous invasion, there is little likelihood of a metastasis (13). This indicates that it is important to treat tumors by PDT with curative intent only if they remain intracartilaginous, that is, limited within the mucosa and submucosa.
It is difficult to detect early-stage superficial cancers by conventional WLB because these lesions are only a few mucosal layers thick and a few millimeters in surface diameter. AFB has been used for detecting and localizing early-stage lung cancer and for categorizing the extent of endobronchial spread of lung cancer (19, 23-25). However, the view by AFB is limited to the lumen and the internal surface of the airways (16, 19).
HR-CT has been reported to provide more accurate information about tumor extension than conventional CT scan in patients with early-stage lung cancer who were referred for bronchoscopic treatment (20, 21). Strictly intraluminal tumors on HR-CT could be achieved with a high rate of complete response after bronchoscopic treatment (20-22). Therefore, HR-CT might help to estimate the depth of tumor invasion in patients with early-stage lung cancer. However, in this study, we could clearly indicate that EBUS offered more accurate information regarding the depth of tumor invasion than did bronchoscopy or HR-CT. To date, we believe that the most promising way to estimate the depth of tumor invasion is EBUS, which is impossible with other diagnostic imaging methods.
Moreover, EBUS is useful not only in evaluating the depth of tumor invasion but also in localizing the tumor margin as accurately as AFB. Even in cases showing intact mucosa, we can sometimes detect submucosal tumor spread. In tumors that have signs of extraluminal spread, it can be difficult to distinguish accurately the tumor from the bronchial wall, peribronchial tissue, or atelectasis by HR-CT (21). On the other hand, EBUS can delineate the tumor margin much more easily. AFB is useful for delineating the endobronchial spread of the tumor, and EBUS is useful for delineating the perpendicular extension of the tumor into the bronchial wall. EBUS is a new modality that should be seriously considered when deciding to treat a tumor with PDT.
In the image depicted by EBUS, a layered structure of the tracheobronchial wall can be observed (15-19). Starting on the luminal side of the tracheobronchial wall, the first layer is seen as a hyperechoic layer, the second layer is isoechoic, the third layer is hyperechoic, the fourth layer is hypoechoic, and the fifth layer is hyperechoic (15-19). From our experimental analysis by needle puncture (17), the third, fourth, and fifth layers in the EBUS image are produced by the presence of the cartilage. The third layer is the marginal echo on the inner surface of the cartilage, the fourth layer is cartilage, and the fifth layer is the marginal echo started at the outer side of the cartilage and contains the adventitia. Although all layers cannot always be observed, the cartilage layer can be observed relatively easily. We believe that it is feasible to evaluate the depth of tumor invasion into the bronchial wall by following this cartilaginous layer, and we divided the depth of tumor invasion into two levels, based on whether the tumor was intracartilaginous or extracartilaginous (19). If the tumor is intracartilaginous, it can be successfully treated with PDT.
There are currently some problems with depth evaluation by EBUS. First, visualization of lesions at bronchial spurs is difficult. Second, CIS lesions are difficult to image. Third, it can be technically difficult for inexperienced users to handle and orient the device.
From experimental analysis, the epithelium is 0.05-mm thick on average, whereas the thickness of the first marginal echo is 0.68 mm (17, 18). Thus, the first marginal echo is more than 10 times thicker than the epithelium. Therefore, in cases of CIS, tumors would not be visible on EBUS, because the tumor was wholly contained within the first marginal echo. If a tumor was not visible on either EBUS or HR-CT, we decided that the tumor would be suitable for PDT with curative intent. Recently, a 30-MHz frequency radial mechanical transducer type ultrasonic probe (UM-S30-25R; Olympus) has been developed. Using this new instrument, the first marginal echo would be shallower; therefore, in our ongoing study, CIS lesions may be depicted. Also, a three-dimensional ultrasonography system (EU-IP 2; Olympus) currently under development may depict CIS or early lung cancers more clearly even if they are at the spur. In the near future, improvements in EBUS will provide the bronchoscopist with an excellent tool for centrally located early tumor detection and better tumor assessment.
The study of depth evaluation of early-stage lung cancer by EBUS is still at a developmental stage. The best way to ascertain the diagnostic accuracy of EBUS is the histopathologic proof of tumors in resected specimens, as we showed in the present study, but this is not possible in patients treated with PDT. Therefore, according to the experimental (17) and clinical (18, 19) data that we believed to be reliable, we used EBUS findings to select appropriate candidates for PDT. The second best check on the accuracy of EBUS is to compare the clinical outcome in patients treated, based on EBUS and independent of EBUS findings. In the present study, all PDT patients selected by EBUS were in long-term complete remission. Additional studies and longer follow-up periods are required to investigate the real clinical significance of EBUS in assessing early lung cancer, and to determine whether the depth of tumor invasion as revealed by EBUS is useful for selecting patients whose tumors can be treated with PDT. To date, EBUS is a safe and feasible technique and may be used in addition to conventional bronchoscopy and HR-CT to improve the success rate of PDT.
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Footnotes |
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Correspondence and requests for reprints should be addressed to Teruomi Miyazawa, M.D., Ph.D., Director, Department of Pulmonary Medicine, Hiroshima City Hospital, 7-33 Motomachi, Naka-ku, Hiroshima 730-0011, Japan. E-mail: ikyoku{at}city-hosp.naka.hiroshima.jp
(Received in original form August 22, 2001 and accepted in revised form December 10, 2001).
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 A. Pasic, H. A. Brokx, E. F. Comans, G. J. Herder, E. K. Risse, O. S. Hoekstra, P. E. Postmus, and T. G. Sutedja Detection and Staging of Preinvasive Lesions and Occult Lung Cancer in the Central Airways with 18F-Fluorodeoxyglucose Positron Emission Tomography: A Pilot Study Clin. Cancer Res., September 1, 2005; 11(17): 6186 - 6189. [Abstract] [Full Text] [PDF]
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K. Kanoh, T. Miyazawa, N. Kurimoto, Y. Iwamoto, Y. Miyazu, and N. Kohno Endobronchial Ultrasonography Guidance for Transbronchial Needle Aspiration Using a Double-Channel Bronchoscope Chest, July 1, 2005; 128(1): 388 - 393. [Abstract] [Full Text] [PDF]
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 J. K. LeBlanc, B. M. Devereaux, T. F. Imperiale, K. Kesler, J. M. DeWitt, O. Cummings, D. Ciaccia, S. Sherman, P. Mathur, D. Conces, et al. Endoscopic Ultrasound in Non-Small Cell Lung Cancer and Negative Mediastinum on Computed Tomography Am. J. Respir. Crit. Care Med., January 15, 2005; 171(2): 177 - 182. [Abstract] [Full Text] [PDF]
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Y. Iwamoto, T. Miyazawa, N. Kurimoto, Y. Miyazu, A. Ishida, K. Matsuo, and Y. Watanabe Interventional Bronchoscopy in the Management of Airway Stenosis Due to Tracheobronchial Tuberculosis Chest, October 1, 2004; 126(4): 1344 - 1352. [Abstract] [Full Text] [PDF]
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Y. Nakamura, C. Endo, M. Sato, A. Sakurada, S.-i. Watanabe, R. Sakata, and T. Kondo A New Technique for Endobronchial Ultrasonography and Comparison of Two Ultrasonic Probes: Analysis With a Plot Profile of the Image Analysis Software NIH Image Chest, July 1, 2004; 126(1): 192 - 197. [Abstract] [Full Text] [PDF]
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A. Ernst, D. Feller-Kopman, H. D. Becker, and A. C. Mehta Central Airway Obstruction Am. J. Respir. Crit. Care Med., June 15, 2004; 169(12): 1278 - 1297. [Abstract] [Full Text] [PDF]
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Y. Miyazu, T. Miyazawa, N. Kurimoto, Y. Iwamoto, A. Ishida, K. Kanoh, and N. Kohno Endobronchial Ultrasonography in the Diagnosis and Treatment of Relapsing Polychondritis With Tracheobronchial Malacia Chest, December 1, 2003; 124(6): 2393 - 2395. [Abstract] [Full Text] [PDF]
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M. J. Tobin Chronic Obstructive Pulmonary Disease, Pollution, Pulmonary Vascular Disease, Transplantation, Pleural Disease, and Lung Cancer in AJRCCM 2002 Am. J. Respir. Crit. Care Med., February 1, 2003; 167(3): 356 - 370. [Full Text] [PDF]
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G. Sutedja New techniques for early detection of lung cancer Eur. Respir. J., January 1, 2003; 21(39_suppl): 57S - 66s. [Abstract] [Full Text] [PDF]
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S. G. Spiro and J. C. Porter Lung Cancer--Where Are We Today?: Current Advances in Staging and Nonsurgical Treatment Am. J. Respir. Crit. Care Med., November 1, 2002; 166(9): 1166 - 1196. [Abstract] [Full Text] [PDF]
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T. Miyazawa, Y. Miyazu, Y. Iwamoto, A. Ishida, K. Kanoh, H. Sumiyoshi, M. Doi, and N. Kurimoto Stenting at the Flow-limiting Segment in Tracheobronchial Stenosis due to Lung Cancer Am. J. Respir. Crit. Care Med., May 15, 2004; 169(10): 1096 - 1102. [Abstract] [Full Text] [PDF]
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