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* From the Department of Pulmonary Diseases (Drs. Yoshikawa, Sukoh, Fukumoto, Harada, and Isobe), National Hospital Organization Hokkaido Cancer Center, Sapporo, Japan; the First Department of Medicine (Drs. Yamazaki, Kikuchi, and Nishimura), Hokkaido University School of Medicine, Sapporo, Japan; and the Department of Pulmonary Medicine (Drs. Kanazawa and Munakata), Fukushima Medical University School of Medicine, Fukushima, Japan.
Correspondence to: Noriaki Sukoh, MD, PhD, Department of Pulmonary Diseases, National Hospital Organization Hokkaido Cancer Center, Kikusui-4–2, Shiroishiku, Sapporo 060-8638, Japan; e-mail: sukou{at}sap-cc.go.jp
Abstract
Study objectives: We evaluated the feasibility and efficacy of transbronchial biopsy (TBB) and bronchial brushing by endobronchial ultrasonography (EBUS) with a guide sheath (GS) as a guide for diagnosing peripheral pulmonary lesions (PPLs) without radiographic fluoroscopy.
Patients: One hundred twenty-one patients with 123 PPLs (mean diameter, 31.0 mm) whose bronchoscopic findings were normal.
Methods: An EBUS-GS was inserted and advanced to the PPL without fluoroscopy. Once we obtained the EBUS image, the probe was withdrawn and the GS was left in place. TBB and/or bronchial brushing were performed via the GS. When an EBUS image could not be obtained, we changed to the bronchoscopic examination under fluoroscopy.
Results: Seventy-six of 123 PPLs (61.8%) were diagnosed by EBUS-GS guidance without fluoroscopy. The diagnostic yield for PPLs > 20 mm in diameter (75.6%) was significantly higher than that for those 
20 mm in diameter (29.7%; p < 0.01). The PPLs located in the middle lobe and the lingular segment had significantly higher diagnostic yields (p < 0.05). When the bronchus leading to the PPL was identified on the CT scan, the yield was 79.2%. Moreover, the solid lesions had a higher diagnostic yield (67.0%) compared with nonsolid lesions (35.0%; p < 0.05). Multivariate analysis revealed that the diameter and the location of the PPL were independent predictors of diagnostic sensitivity by EBUS-GS-guided bronchoscopy (p < 0.05).
Conclusions: EBUS-GS–guided bronchoscopy without the use of radiographic fluoroscopy is effective for diagnosing PPLs. The diameter, location, and CT scan appearance of the PPLs, and the identification of the bronchus leading to the PPLs were valuable as factors related to a higher diagnostic sensitivity with this procedure.
Key Words: bronchoscopy • endobronchial ultrasonography with guide sheath • fluoroscopy • lung cancer • peripheral pulmonary lesion
Since the 1970s, a transbronchial approach using a flexible bronchoscope has been one of the most generally accepted methods for diagnosing peripheral pulmonary lesions (PPLs) under fluoroscopy.12345678 The diagnostic accuracy was reported to be 48 to 80% for malignant PPLs,12345678 and 35 to 50% for benign PPLs,13 including central PPLs. Smaller PPLs have been detected due to the advances in and the widespread use of CT scanning.910 However, the yield is not satisfactory for these smaller PPLs as it detects only 14 to 54% of PPLs that are 20 mm in diameter.136
The transbronchial procedure has been performed with the usage of fluoroscopy, but it has the disadvantages of excessive radiation exposure for patients and medical workers.11 Therefore, it is desirable to improve the accuracy of the diagnosis of PPLs safely and to reduce the radiation exposure during the examination.
Endobronchial ultrasonography (EBUS) has been investigated for its application in the diagnosis of central airway lesions from the early 1990s1213 and has also been applied to the assessment of PPLs.1415161718 To date, several reports12131415161718192021 have shown the usefulness of EBUS for visualizing the parabronchial structure, confirming the precise location of PPLs, and diagnosing them. Furthermore, the combination of the EBUS technique with a guide sheath (GS) to diagnose PPLs was introduced by Kurimoto et al.19 The advantages of the EBUS-GS technique are that it provides access to bronchial lesions for repeated sampling and protects against bleeding from the biopsy site by wedging the GS into the bronchial lumen. These points show the value of using the EBUS-GS technique compared to the use of EBUS alone. By using an EBUS-GS with radiographic fluoroscopy, investigators have reported1920 high sensitivity for the diagnosis of PPLs. However, we speculated that the application of EBUS-GS guidance might make it possible to omit radiographic fluoroscopic guidance and reduce the radiation exposure. Thus, in the present study, we evaluated the feasibility, efficacy, and safety of the EBUS-GS technique as a guide for transbronchial biopsy (TBB) for the diagnosis of PPLs in the absence of radiographic fluoroscopy. And this is the first report to clarify the characteristics of the PPLs diagnosed under EBUS-GS guidance alone.
Materials and Methods
Patients
From June 2004 to July 2005, 121 consecutive patients with 123 PPLs who were referred to the Hokkaido Cancer Center for diagnostic bronchoscopy were prospectively enrolled in the study. PPLs were defined as those lesions that were surrounded by pulmonary parenchyma and were bronchoscopically invisible (ie, no evidence of endobronchial change). CT scanning was performed using a multidetector CT scanner with 7.5-mm slices; images of the PPLs were obtained with slices of 1.25 to 2.5 mm as well. All chest CT scans were reviewed, and the longest diameter, location, characteristics, and the bronchi leading to the lesion were recorded. This study was approved by the ethics committee of our institution. Written informed consent was obtained from all the patients prior to performing the procedure.
EBUS-GS–Guided TBB and Bronchial Brushing
Each patient was premedicated using 7.5 to 15 mg of pentazocine hydrochloride and 0.25 to 0.5 mg of atropine sulfate. Local anesthesia of the upper respiratory tract was achieved using 4% lidocaine. EBUS was performed using an endoscope ultrasound system (EU-M30S; Olympus; Tokyo, Japan), which was equipped with a 20-MHz mechanical radial-type probe (XUM-S20–17R; Olympus) with an external diameter of 1.4 mm and a GS (XBO1–836-12; Olympus). Videobronchoscopes with a working channel diameter of 2.0 mm were used (BF-260 and BF-P240; Olympus). The EBUS probe was inserted into the GS beforehand, and the GS-covered probe was introduced via the working channel of the bronchoscope and advanced to the PPL to obtain an EBUS image. The probe and GS were confirmed to reach the lesion by EBUS images. Once a typical EBUS image could be seen, the probe was withdrawn from the sheath and the GS was left in place. A biopsy forceps or a bronchial brush was introduced through the GS to obtain pathologic specimens.19 These procedures were performed without fluoroscopy. When an EBUS image could not be obtained, we made the shift to examination under fluoroscopy. We attempted to advance the EBUS-GS to the lesion using an angulated curette. A double-hinged curette was inserted into the GS, and the appropriate bronchus was selected by manipulating the curette under fluoroscopy. Once the target bronchus was determined, the curette was removed and the GS was left in place. The probe was inserted again through the GS to confirm the EBUS image. Once the location of the lesion was identified, TBB and/or bronchial brushing were performed. Otherwise, we removed the EBUS-GS and subsequently performed TBB, bronchial brushing, and/or curetting in reference to fluoroscopy. The biopsy was repeated until adequate specimens were collected.
Statistical Analysis
The data are presented as the mean ± SD. To clarify the characteristics of the PPLs diagnosed under EBUS-GS guidance without fluoroscopy, a comparison of the diagnostic yields was done using the 
2 test with an 
of 0.05. We report the 95% confidence intervals, and all tests were two-sided. Logistic regression analysis was applied for the multivariate analysis of factors related with diagnostic sensitivity; p < 0.05 was regarded as being significant.
Results
A total of 121 patients (72 male and 49 female) with 123 PPLs were examined. The mean age was 66.2 years (range, 38 to 82 years). The mean (± SD) diameter of the PPLs was 31.0 ± 15.9 mm (range, 11.0 to 98.0 mm). The PPLs were localized in the right upper lobe in 37 lesions (30.1%), the right middle lobe in 10 lesions (8.1%), the right lower lobe in 31 lesions (25.2%), the left upper division in 22 lesions (17.9%), the left lingular segment in 5 lesions (4.1%), and the left lower lobe in 18 lesions (14.6%). The CT scan appearance of the PPLs showed 103 solid lesions (83.7%), 14 mixed ground-glass opacity (GGO) lesions (11.4%), 4 pure GGO lesions (3.3%), and 2 cavity lesions (1.6%).
Table 1 shows the final diagnoses for the 123 PPLs. The diagnoses in the biopsy finding-negative patients were established by video-assisted thoracoscopic surgery, thoracotomy, percutaneous guided needle aspiration, and follow-up. One hundred three of the 123 PPLs were primary lung cancer. Ninety-three of the 123 PPLs (75.6%) were visualized by EBUS. Typical findings that were observed are shown in Figure 1 . All patients whose PPLs were visible on EBUS images subsequently underwent EBUS-GS-guided TBB and/or bronchial brushing. The diagnostic yield was 61.8% by EBUS-GS–guided TBB and bronchial brushing without fluoroscopy, and 86.2% by all bronchoscopic procedures. The ratio of the lesions diagnosed by EBUS-GS guidance alone was 71.7% among the lesions diagnosed by all bronchoscopic procedures. The diagnostic sensitivities of the EBUS-GS–guided procedure without fluoroscopy for malignant and benign lesions were 60.7% (65 of 107 lesions) and 68.8% (11 of 16 lesions), respectively. For malignant lesions, the diagnostic yield of cytology and biopsy specimens were 90.8% (59 of 65 lesions) and 47.7% (31 of 65 lesions), respectively.
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20 mm, 20 to 30 mm, and > 30 mm were 29.7%, 57.9%, and 89.6%, respectively. The diagnostic yield for lesions > 20 mm in the longest diameter (75.6%) was significantly higher than that for lesions 20 mm (29.7%; p < 0.01).
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Discussion
We evaluated the feasibility, efficacy, and safety of TBB and bronchial brushing using the EBUS-GS technique without radiographic fluoroscopy for the diagnosis of PPLs. The diagnostic yield for PPLs was 61.8% for EBUS-GS guidance alone without fluoroscopy. Most of the PPLs (75.6%) were visualized clearly by EBUS imaging. For > 70% of the PPLs diagnosed by bronchoscopy, definitive diagnoses could be achieved efficiently by EBUS-GS guidance alone without radiologic equipment and the accompanying radiation exposure. Herth and associates15 studied 50 patients and failed to demonstrate a difference between EBUS-guided (without the GS technique) and fluoroscopy-guided TBB for the diagnosis of PPLs. However, there has been no report on use of the EBUS-GS technique alone without fluoroscopy as a bronchial guide for the diagnosis of the PPLs.
Several groups have reported1235 that the combination of bronchial brushing and biopsy gave the optimum overall accuracy. In this study, the combining bronchial brushing and biopsy improved diagnostic accuracy.
In the present study, the diagnostic yield for PPLs > 20 mm in diameter was significantly higher than that for PPLs 20 mm in diameter by EBUS-GS guidance alone (p < 0.01). This was mainly due to technical problems in that the probe with a GS could not be introduced into a PPL properly. We could obtain the EBUS image for only 16 of 37 PPLs 20 mm (43.2%). Kikuchi and associates20 and Paone and associates18 reported high diagnostic rates (53% and 71%, respectively) for PPLs < 20 mm in diameter using EBUS with fluoroscopy. A better diagnostic rate was achieved with fluoroscopy than without fluoroscopy for the following reasons: (1) confirmation of the location of the PPLs with the three-dimensional perspective achieved by the combined EBUS-GS technique; (2) selection of a more appropriate bronchus by manipulation of the angulated curette; and (3) recognition of the movement of the PPLs during deep respiration. Hence, EBUS-GS–guided TBB without fluoroscopy appeared to have a limitation in diagnosing smaller PPLs, but its application was beneficial in diagnosing PPLs > 20 mm in diameter.
Regarding location, the diagnostic yields of the PPLs located in the right middle lobe and the left lingular segment were significantly higher. It might be easier to identify a bronchus that leads to a PPL in these areas on the CT scan. On the other hand, the diagnostic yields of the PPLs located in the right upper and lower lobes were obviously lower. Previously, Herth and associates15 and Shirakawa and associates16 also pointed out the low diagnostic yield of PPLs in the right upper lobe. This might be due to the relatively long and stiff tip of the EBUS catheter, which interferes with maneuverability in tortuous airways and sharp bends. As for the PPLs in the right lower lobe, the GS seemed to move and slip off more easily from the lesion with deep respiration.
For the PPLs to which an accessible bronchus was identified or presumed from the CT scan images, the diagnostic accuracy was significantly higher. For the PPLs to which we could identify an appropriate bronchi, the yield was around 80%. Hence, to improve the diagnostic yield, it is critical to examine the proper route to the lesions by thin slice CT scanning. Moreover, the widespread use of virtual bronchoscopic navigation that shows the proper route to the lesion precisely is awaited.22
The characteristics of the PPLs seen on CT scans affected the yield as well. Solid lesions had a significantly higher diagnostic yield than those with other patterns. The reasons for the lower yields of nonsolid lesions are as follows: (1) difficulty in obtaining an EBUS image for GGOs; and (2) the fact that GGOs might not penetrate the bronchus. Thus, it was necessary to obtain enough specimens. Reichenberger and associates23 reported that the use of transbronchial needle aspiration increased the diagnostic yield from 35 to 51% without additional risk. For the lesions that may not have penetrated the bronchus such as pure or mixed GGOs, the addition of transbronchial needle aspiration might increase the diagnostic yield.
In summary, we demonstrated the feasibility and the value of the EBUS-GS–guided transbronchial procedure without the use of radiographic fluoroscopy. The adaptation of the EBUS-GS technique without fluoroscopy for the diagnosis of PPLs was clarified. The preferable characteristics of PPLs for the use of this technique are as follows: (1) PPLs in which the longest diameter is > 20 mm; (2) the bronchus leading to the PPL has been identified or can be presumed from CT scan findings; and (3) the CT scan appearance is of a solid lesion. This study suggests that the EBUS-GS technique should be the first procedure used for diagnosing such lesions. In cases in which EBUS images cannot be obtained, we should make the shift to the usual bronchoscopic examination performed under fluoroscopy. We are convinced that EBUS-GS guidance without the use of radiographic fluoroscopy will be of increasing importance in the future.
Footnotes
Abbreviations: EBUS = endobronchial ultrasonography; GGO = ground-glass opacity; GS = guide sheath; PPL = peripheral pulmonary lesion; TBB = transbronchial biopsy
The authors have reported to the ACCP that no significant conflicts of interest exist with any companies/organizations whose products or services may be discussed in this article.
Received for publication October 13, 2006. Accepted for publication March 1, 2007.
References
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