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Original Investigations

Assessment of the New Thin Convex Probe Endobronchial Ultrasound Bronchoscope and the Dedicated Aspiration Needle

A Preliminary Study in the Porcine Lung

Wada, Hironobu MD, PhD*,†; Hirohashi, Kentaro MD*; Nakajima, Takahiro MD, PhD*,†; Anayama, Takashi MD, PhD*; Kato, Tatsuya MD, PhD*; Grindlay, Alexandria BSc, CCRP*; McConnell, Judy BSc, CCRP*; Yoshino, Ichiro MD, PhD; Yasufuku, Kazuhiro MD, PhD*

Author Information
Journal of Bronchology & Interventional Pulmonology: January 2015 - Volume 22 - Issue 1 - p 20-27
doi: 10.1097/LBR.0000000000000123
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Abstract

Endobronchial ultrasound-guided transbronchial needle aspiration (EBUS-TBNA) has been demonstrated to be an effective minimally invasive procedure for mediastinal and hilar lymph node staging of lung cancer as well as for biopsy of paratracheal and parabronchial lesions.1–3 EBUS-TBNA was initially recognized as one of the first diagnostic procedures to confirm N2 diseases in accessible lymph node stations, in the second edition of the American College of Chest Physician lung cancer guidelines in 2007.4 Because of the fact that an increasing number of publications have shown the evidence of lymph nodal staging using EBUS-TBNA in lung cancer patients, the recently published third edition of American College of Chest Physician guideline showed an overall median sensitivity of 89% and a median negative predictive value of 91% for mediastinal lymph nodal staging in 2756 cases at multiple institutions.5 In addition, as interlobar lymph nodes (#11) are in the range of the current convex probe EBUS (CP-EBUS), these lymph nodes can be accurately assessed using the CP-EBUS. Yasufuku et al6 have reported preferable results of EBUS-TBNA for 163 patients diagnosed as potentially resectable clinical N0 or N1 non–small cell lung cancer (NSCLC), showing a sensitivity of 76.2%, a specificity of 100%, a diagnostic accuracy of 96.6%, and a negative predictive value of 96.2%, which contributed to differentiating N1 lung cancer from N0 disease. However, because of its size, the current CP-EBUS has limitations in accessing more distal lymph nodes, which include lobar (#12) and segmental lymph (#13) nodes. The current CP-EBUS is able to reach to some, but not all, distal N1 lymph nodes and there is currently no reliable modality to sample entire distal N1 disease. Moreover, noninvasive diagnostic modalities, including computed tomography (CT) and/or positron emission tomography, are far from satisfactory to demonstrate high sensitivity and specificity in identifying N1 nodal metastasis in lung cancer patients.7 Therefore, we sought to develop the new prototype thin CP-EBUS (TCP-EBUS), which is able to assess more distal lymph nodes than the current CP-EBUS. The objective of this study was to assess the new TCP-EBUS in terms of accessibility, operability, and visualization of N1 lymph nodes, and to evaluate the smaller gauge aspiration needle for sampling of lymph nodes in a porcine model.

MATERIALS AND METHODS

TCP-EBUS

All experiments and data analysis were accomplished in University Health Network (UHN). The prototype TCP-EBUS (BF-Y0046, Olympus Medical Systems Corp., Tokyo, Japan) was used in this study. The comparison of the specification between the TCP-EBUS and the current CP-EBUS (BF-UC180F, Olympus Medical Systems Corp.) is shown in Table 1. The TCP-EBUS improves the direction of view (DOV) from 35 to 20 degrees, which is closer to a standard bronchoscope DOV of 0 degrees. This modification facilitates the improvement of endoscopic visibility of the TCP-EBUS. The outer diameter of the tip is 5.9 mm, which is 1 mm smaller than the current CP-EBUS. The length of the rigid part on the probe tip has been shortened by approximately 8 mm (Fig. 1). The upward angulation range has improved from 120 to 170 degrees; however, the downward angulation range has been decreased slightly. The TCP-EBUS is integrated with a convex transducer (7.5 MHz), which scans parallel to the insertion direction of the bronchoscope similar to the current CP-EBUS. The scanning range is also the same, but the TCP-EBUS is made to be used without a balloon. The ultrasound image is processed by a dedicated ultrasound scanner (EU-Y0009, Olympus Medical Systems Corp.) and relayed with the endoscopic images on dual monitors. The TCP-EBUS has integrated a highly flexible passive bending portion slightly proximal to the active bending portion, mimicking a normal bronchoscope. For EBUS-TBNA, a dedicated smaller gauge needle (25 G, Olympus Medical Systems Corp.) with improved flexibility is required.

TABLE 1
TABLE 1:
The Comparison of the Thin Convex Probe-Endobronchial Ultrasound (CP-EBUS) and the Current CP-EBUS
FIGURE 1
FIGURE 1:
The appearance of both the thin (top) and current convex probe endobronchial ultrasound (CP-EBUS) (bottom). The thin CP-EBUS (TCP-EBUS) has a 1 mm smaller outer diameter and a shortened rigid part on the tip. It is made for use without a balloon.

Animals

This study was approved by the Animal Care Committees at the UHN. All animals were provided with humane care in accordance with the policies formulated by the UHN Animal Care Committee, the Animal for Research Act of the Province of Ontario, and the Canadian Council on Animal Care. Male adult Yorkshire pigs (Caughell Farms, Fingal, ON) were used for this study. After introduction of general anesthesia with 5% isoflurane inhalation, an endotracheal tube with a diameter of 8.0 mm or more was inserted to keep the airway open for adequate ventilation by oral or a tracheotomy port. The bronchoscope was inserted through the endotracheal tube and all assessments were performed under fluoroscopy assistance.

Assessment of the TCP-EBUS

Using 6 live pigs (the averaged body weight was 32.4±1.3 kg) the following endpoints were evaluated; accessibility, operability, and TBNA capability of the TCP-EBUS. With regard to the accessibility assessment, maximum reach was measured to determine the insertion capability from a standard point, which was set at 1 ring proximal from the tracheobronchial angle. Endoscopic visibility range, which indicates how far the scope can sustain endoscopic imaging, was also measured in the same manner and compared between the 2 CP-EBUSs. For the accessibility assessment the left upper lobe (LUL) bronchus, tracheobronchus on the right, and the right lower lobe (RLL) bronchus were selected for the evaluation in 3 pigs. Operability was assessed in terms of the maneuverability and ultrasound visibility of the scopes during the procedures in 6 pigs. TBNA capability was evaluated at not only N1 lymph nodes but also at mediastinal lymph nodes using the dedicated 25 G aspiration needle in 3 pigs. The Doppler mode facilitated distinguishing pulmonary vessels from lymph nodes. The obtained aspirates in the needle were air blown on to a glass slide and smeared for cytologic evaluation. Diff-quick staining was immediately performed to evaluate the TBNA adequacy.

RESULTS

Accessibility and Operability Assessment

In all evaluated bronchi (n=9), the TCP-EBUS showed a greater reach with improved operability compared with the current CP-EBUS. On average, the TCP-EBUS had a 14.7 mm greater endoscopic visibility range and a 16.0 mm greater maximum reach (Table 2) than the current CP-EBUS. The TCP-EBUS also consistently visualized 1 to 3 distal bifurcations further than the current CP-EBUS (Table 3). The current CP-EBUS was able to visualize the LUL bronchial orifice or the LUL upper division bronchial orifice, but was unable to visualize further airways beyond that point. In all 3 cases, the TCP-EBUS was able to visualize as far as the current CP-EBUS and was even able to visualize a further distal bifurcation in the LUL lower division bronchus. The current CP-EBUS was able to be inserted only into the LUL lower division bronchus; however, the TCP-EBUS was easily inserted into both the upper and lower division bronchi in the LUL selectively. The highly flexible passive bending portion slightly proximal to the active bending portion of the TCP-EBUS was helpful in allowing insertion into the distal airway in the upper division bronchus. Both the thin and current CP-EBUS were able to be inserted into the tracheobronchus on the right side. The current CP-EBUS lost the endoscopic image immediately after the insertion into the tracheobronchus; however, the TCP-EBUS was able to visualize 1 bifurcation deeper than the current CP-EBUS after insertion. In the RLL bronchus, both the endoscopic visibility range and the maximum reach were superior in the TCP-EBUS. In addition, the TCP-EBUS was able to visualize the liver across the diaphragm. Measurements were larger at both the LUL bronchus and the RLL bronchus when compared with the tracheobronchus as the LUL lower division bronchus and RLL bronchus were relatively straight in the porcine model and allowed for easy bronchoscope insertion.

TABLE 2
TABLE 2:
The Comparison of Endoscopic Visibility Range and Maximum Reach Between the CP-EBUS
TABLE 3
TABLE 3:
The Comparison of Number of Bifurcations Visible on Endoscope

TBNA Capability Assessment

The TCP-EBUS visualized not only hilar but also mediastinal lymph nodes by contacting the probe directly onto bronchial walls without a balloon. The evaluated lymph nodes were clearly visualized and then punctured by the dedicated 25 G aspiration needle. The direct contact method successfully functioned to visualize mediastinal lymph nodes due to the smaller-sized probe and smooth inner surface of the porcine trachea. The needle was smoothly inserted into the targeted lymph nodes without any resistance and sufficient lymphoid sampling was achieved (Fig. 2). The samples appeared to have less blood contamination. Even after the needle was loaded, the tip of the bronchoscope was flexible thus it contributed to improvement of operability, allowing easy insertion into the LUL upper division bronchus.

FIGURE 2
FIGURE 2:
The thin convex probe endobronchial ultrasound (TCP-EBUS) demonstrates the adequate lymphoid sampling in the left lower division bronchus of the left upper lobe. A, Endobronchial ultrasound visualized a segmental lymph node, and endobronchial ultrasound transbronchial needle aspiration was successfully performed using the TCP-EBUS and the dedicated aspiration needle. B, Fluoroscopy shows the tip of the scope located in the lower division bronchus. C, Diff-quick staining revealed adequate lymphoid tissue sampling. The scale bar shows 5 mm (A) and 50 μm (C).

DISCUSSION

The newly developed prototype TCP-EBUS demonstrated an improved accessibility to the distal airways with excellent operability and TBNA capability for lobar and segmental lymph nodes in the porcine lung. The TCP-EBUS was easily inserted into both the upper and lower division bronchus of LUL, which has similar divergence as the human lung, and the segmental lymph nodes were visualized and sufficient lymphoid sampling was obtained. The results shown in this study is promising, as adult human lungs are usually larger than the porcine lungs used in this study, indicating that the TCP-EBUS will likely be able to reach and obtain samples from segmental lymph nodes in human lung. Several improvements have been made to the TCP-EBUS. These improvements include: smaller probe size, shortened rigid part on the tip, larger upward angulation range, and decreased angle of the direction of the endoscopic view, which, when combined, allow better access to the peripheral airway with a sustained endoscopic view. The shortened rigid part on the tip and flexible needle makes the EBUS-TBNA procedure easier with the TCP-EBUS. Better ultrasound visualization of the lymph nodes especially after the needle has been loaded facilitates the precise puncture of the lymph nodes. The smaller gauge aspiration needle enables adequate lymphoid sampling from not only N1 lymph nodes but also mediastinal lymph nodes.

Precise N1 lymph node staging allows detailed assessment of patients with lung cancer. This may help to determine the optimal strategy and prognosis. Even though lobectomy with systematic lymph node dissection is the standard of care for lung cancer, limited resection, especially segmental resection, has shown excellent results in select patients with tumors that are <20 mm.8,9 Furthermore, 2 randomized phase III clinical trials are currently ongoing in North America (Cancer and Leukemia Group B, CALGB 140503)10 and Japan (Japan Clinical Oncology Group, JCOG 0802/West Japan Oncology Group, WJOG 4607L).11 The goal of these trials is to compare sublobar resection to lobectomy for NSCLC of a <20 mm tumor, which may demonstrate additional evidence for sublobar resection in early-stage lung cancer patients. Because of the prevalence of CT screening and the recent trend toward minimally invasive surgery, early-stage lung cancer is increasingly assessed and segmental resection will potentially be applied to such lesions in the near future. Precise N1 lymph node diagnosis is mandatory to ensure the success of segmental resection; therefore, we contend that the TCP-EBUS will be a beneficial tool for a complete systematic evaluation of N1 lymph nodes for appropriate selection of segmental resection.

Stereotactic body radiotherapy (SBRT) is a therapeutic option for clinical stage I lung cancer patients who are unfit for surgery.12 Some clinical studies have shown excellent rates of local control (83% to 95% in 3 y) and overall survival (47% to 72% in 3 y) after SBRT for surgically fit or unfit patients with clinical stage I NSCLC.13–16 Some retrospective or prospective comparison studies have also demonstrated a similar local tumor control rate between SBRT and surgery for patients with clinical stage I NSCLC.13,16,17 However, a randomized phase III clinical trial designed to compare surgery and SBRT for high-risk operable patients with NSCLC (American College of Surgeons Oncology Group, ACOSOG Z4099/Radiation Therapy Oncology Group, RTOG 1021)18 was unfortunately closed due to low accrual16 and there have been no completed prospective randomized clinical trials comparing those disparate treatments. A recent large-scale retrospective propensity-matched study has demonstrated that the 3-year overall survival after SBRT and surgery (56 matched patients) was 52% versus 68% (P=0.05), disease-free survival was 47% versus 65% (P=0.01), and local recurrence-free survival rate at 3 years was 90% versus 92% (P=0.07), respectively, concluding that surgical resection seems to result in better outcomes than SBRT.16 One of the advantages of surgery over SBRT is that it enables accurate pathologic staging that will aid management of patients after surgery. Staging for SBRT is currently determined by radiologic modalities (CT and positron emission tomography); however, these modalities have shown a less accurate diagnostic yield than EBUS-TBNA,7,19 and this may cause understaging for occult regional disease that is not suitable for SBRT.12 We believe that the TCP-EBUS will contribute to a proper selection of good candidates for SBRT, and will also be useful for decision making of appropriate adjuvant treatment in patients treated with SBRT owing to the accurate N1 lymph node staging.

Some randomized clinical trials have shown preferable overall survival rate in NSCLC patients after neoadjuvant chemotherapy followed by surgery, when compared with surgery alone,20–23 even though most of these studies had a small number of patients, and the difference was not statistically significant.24 Precise pathologic diagnosis of mediastinal lymph nodes by mediastinoscopy drove the development of randomized clinical trials to determine the survival benefit in patients with N2 disease undergoing neoadjuvant chemotherapy. In contrast, the benefit of neoadjuvant chemotherapy for N1 disease remains unclear due to the lack of a reliable modality for preoperative sampling from N1 lymph nodes. The TCP-EBUS has great potential to clarify the efficacy of neoadjuvant chemotherapy for patients with biopsy-proven N1 disease.

The current CP-EBUS has demonstrated the efficacy for the diagnosis of intrapulmonary lesions located adjacent to the central airway.25,26 Likewise, the TCP-EBUS could facilitate assessment of intrapulmonary lesions located adjacent to a segmental or a more distal bronchus. The visualization of the liver by the TCP-EBUS in the porcine lung encourages the bronchial investigation by the TCP-EBUS for more distal lesions in the human lung. Electromagnetic navigational bronchoscopy (ENB) is an emerging technology for accurate diagnosis of peripheral lung nodules showing the improved diagnostic yield up to the range of 59% to 85%.27–30 This technology may work for the diagnosis of those intrapulmonary lesions; however, the diagnostic yield of ENB largely depends on the quality of the preprocedure CT scan because motion artifacts and insufficient inspiratory effort result in inaccurate pathway development. In addition, the cost of ENB is high and its use is still limited to specialized facilities.27 Radial probe EBUS (RP-EBUS) is an alternative approach for visualization of the intrapulmonary lesions. A meta-analysis and systematic review of RP-EBUS has shown an overall sensitivity of 0.73 (95% confidence interval, 0.70-0.76) for detection of peripheral lung cancer.30 However, the target lesions were mainly located in the peripheral lung and the diagnostic yield for the relatively centrally located pulmonary nodules remains unresolved. Furthermore, both the RP-EBUS and the ENB are unable to provide real-time guided aspiration of the targets and this may cause a lower accuracy rate than the TCP-EBUS.

The TCP-EBUS potentially benefits patients with not only lung cancer but also benign lung diseases including pulmonary sarcoidosis. Bilateral hilar adenopathy is the most common feature of sarcoidosis, and those lymph nodes can be targets to obtain the cytopathologic diagnosis. The CP-EBUS has proved the efficacy for the diagnosis of stage I and II pulmonary sarcoidosis in clinically and radiologically suspicious patients, showing an 83.3% to 94.4% diagnostic yield, which is significantly superior to a traditional transbronchial lung biopsy.31–34 As the TCP-EBUS has greater accessibility to distal N1 nodes than the CP-EBUS, it may contribute to the augmentation of the diagnostic yield in sarcoidosis patients.

There are several limitations in the current study. First, all lymph nodes evaluated in this study were normal without calcification. Also, the tracheal rings of the pig are softer than the human trachea; therefore, the pig lymph nodes are more easily punctured than human lymph nodes especially mediastinal lymph nodes. In addition, insertion may be more difficult through the human airway wall as the 25 G needle is thinner and less rigid than the current needles. Thus, the feasibility of the TCP-EBUS for the evaluation of lymph nodes, especially mediastinal lymph nodes, remains unclear for human cases. Second, the size and the divergence of the bronchial tree are different between pigs and humans. Even though the accessibility assessment has shown a farther reach in the 3 respective bronchi in the porcine lung, the exact assessable range of the TCP-EBUS in the human lung is unknown.

Lastly, other EBUS bronchoscopes are described. Currently, 2 different EBUS scopes are commercially available for clinical use. Pentax Medical (Montvale, NJ) has produced an EBUS bronchoscope (EB-1970UK) that integrates charge coupled device chips on its tip, allowing for excellent endoscopic imaging. It has a 2.0 mm working channel diameter and its angulation ranges from 120 degrees upward and 90 degrees downward. However, because of the location of the charge coupled device chips, the rigid distal end outer diameter and the forward oblique angle of DOV are as large as 7.4 mm and 45 degrees, respectively. A Fuji scope (EB-530 US; Fujifilm, Tokyo, Japan) has a smaller outer diameter of 6.7 mm with a 2.0 mm working channel. The upward and downward angulations are 130 and 90 degrees, respectively. This scope decreases its DOV up to 10 degrees forward oblique, which allows for easy manipulation of the scope and constant visualization by endoscopic imaging during EBUS-TBNA.35

In conclusion, the TCP-EBUS has improved accessibility to peripheral bronchi with excellent operability, and it is capable of sampling N1 lymph nodes (lobar and segmental) as well as mediastinal lymph nodes using the dedicated aspiration needle. We believe that the TCP-EBUS will allow a more precise assessment of the N1 lymph nodes during nodal staging for lung cancer, which will provide potential improvement and development of multiple treatments for lung lesions.

REFERENCES

1. Yasufuku K, Chiyo M, Sekine Y, et al.. Real-time endobronchial ultrasound-guided transbronchial needle aspiration of mediastinal and hilar lymph nodes. Chest. 2004;126:122–128.
2. Yasufuku K, Pierre A, Darling G, et al.. A prospective controlled trial of endobronchial ultrasound-guided transbronchial needle aspiration compared with mediastinoscopy for mediastinal lymph node staging of lung cancer. J Thorac Cardiovasc Surg. 2011;142:1393–1400.
3. Yasufuku K. Current clinical applications of endobronchial ultrasound. Expert Rev Respir Med. 2010;4:491–498.
4. Detterbeck FC, Jantz MA, Wallace M, et al.. Invasive mediastinal staging of lung cancer: ACCP evidence-based clinical practice guidelines (2nd edition). Chest. 2007;132:202S–220S.
5. Silvestri Ga, Gonzalez AV, Jantz MA, et al.. Methods for staging non-small cell lung cancer: diagnosis and management of lung cancer, 3rd ed: American College of Chest Physicians evidence-based clinical practice guidelines. Chest. 2013;143:e211S–e2150.
6. Yasufuku K, Nakajima T, Waddell T, et al.. Endobronchial ultrasound-guided transbronchial needle aspiration for differentiating n0 versus n1 lung cancer. Ann Thorac Surg. 2013;96:1756–1760.
7. Carrillo SA, Daniel VC, Hall N, et al.. Fusion positron emission/computed tomography underestimates the presence of hilar nodal metastases in patients with resected non-small cell lung cancer. Ann Thorac Surg. 2012;93:1621–1624.
8. Tsutani Y, Miyata Y, Nakayama H, et al.. Oncologic outcomes of segmentectomy compared with lobectomy for clinical stage IA lung adenocarcinoma: propensity score-matched analysis in a multicenter study. J Thorac Cardiovasc Surg. 2013;146:358–364.
9. Bao F, Ye P, Yang Y, et al.. Segmentectomy or lobectomy for early stage lung cancer: a meta-analysis. Eur J Cardiothorac Surg. 2014;46:1–7.
10. Clinical Trials (PDQ®), National Cancer Institute, http://www.cancer.gov/clinicaltrials/search/view?cdrid=555324&version=HealthProfessional. Assessed on May 31, 2014.
11. Nakamura K, Saji H, Nakajima R, et al.. A phase III randomized trial of lobectomy versus limited resection for small-sized peripheral non-small cell lung cancer (JCOG0802/WJOG4607L). Jpn J Clin Oncol. 2010;40:271–274.
12. Howington JA, Blum MG, Chang AC, et al.. Treatment of stage I and II non-small cell lung cancer: diagnosis and management of lung cancer, 3rd ed: American College of Chest Physicians evidence-based clinical practice guidelines. Chest. 2013;143:e278S–e313.
13. Grills IS, Mangona VS, Welsh R, et al.. Outcomes after stereotactic lung radiotherapy or wedge resection for stage I non-small-cell lung cancer. J Clin Oncol. 2010;28:928–935.
14. Timmerman R, Paulus R, Galvin J, et al.. Stereotactic body radiation therapy for inoperable early stage lung cancer. JAMA. 2010;303:1070–1076.
15. Shibamoto Y, Hashizume C, Baba F, et al.. Stereotactic body radiotherapy using a radiobiology-based regimen for stage I nonsmall cell lung cancer: a multicenter study. Cancer. 2012;118:2078–2084.
16. Crabtree TD, Puri V, Robinson C, et al.. Analysis of first recurrence and survival in patients with stage I non-small cell lung cancer treated with surgical resection or stereotactic radiation therapy. J Thorac Cardiovasc Surg. 2014;147:1183–1191.
17. Onishi H, Shirato H, Nagata Y, et al.. Hypofractionated stereotactic radiotherapy (HypoFXSRT) for stage I non-small cell lung cancer: updated results of 257 patients in a Japanese multi-institutional study. J Thorac Oncol. 2007;2:S94–S100.
18. Fernando HC, Timmerman R. American College of Surgeons Oncology Group Z4099/Radiation Therapy Oncology Group 1021: a randomized study of sublobar resection compared with stereotactic body radiotherapy for high-risk stage I non-small cell lung cancer. J Thorac Cardiovasc Surg. 2012;144:S35–S38.
19. Yasufuku K, Nakajima T, Motoori K, et al.. Comparison of endobronchial ultrasound, positron emission tomography, and CT for lymph node staging of lung cancer. Chest. 2006;130:710–718.
20. Gilligan D, Nicolson M, Smith I, et al.. Preoperative chemotherapy in patients with resectable non-small cell lung cancer: results of the MRC LU22/NVALT 2/EORTC 08012 multicentre randomised trial and update of systematic review. Lancet. 2007;369:1929–1937.
21. Depierre A, Milleron B, Moro-Sibilot D, et al.. Pre-operative chemotherapy followed by surgery compared with primary surgery in resectable stage I (except T1N0), II and IIIA non-small cell lung cancer. J Clin Oncol. 2002;20:247–253.
22. Pisters KM, Vallières E, Crowley JJ, et al.. Surgery with or without preoperative paclitaxel and carboplatin in early-stage non-small-cell lung cancer: Southwest Oncology Group Trial S9900, an intergroup, randomized, phase III trial. J Thorac Oncol. 2010;28:1843–1849.
23. Burdett S, Stewart L, Rydzewska L. Chemotherapy and surgery versus surgery alone in non-small cell lung cancer. Cochrane Database Syst Rev. 2007;18:CD006157.
24. Ramnath N, Dilling TJ, Harris LJ, et al.. Treatment of stage III non-small cell lung cancer: diagnosis and management of lung cancer, 3rd ed: American College of Chest Physicians evidence-based clinical practice guidelines. Chest. 2013;143:e314S–e3140.
25. Nakajima T, Yasufuku K, Fujiwara T, et al.. Endobronchial ultrasound-guided transbronchial needle aspiration for the diagnosis of intrapulmonary lesions. J Thorac Oncol. 2008;3:985–988.
26. Tournoy KG, Rintoul RC, van Meerbeeck JP, et al.. EBUS-TBNA for the diagnosis of central parenchymal lung lesions not visible at routine bronchoscopy. Lung Cancer. 2009;63:45–49.
27. Leong S, Ju H, Marshall H, et al.. Electromagnetic navigation bronchoscopy: a descriptive analysis. J Thorac Dis. 2012;4:173–185.
28. Lamprecht B, Porsch P, Wegleitner B, et al.. Electromagnetic navigation bronchoscopy (ENB): increasing diagnostic yield. Respir Med. 2012;106:710–715.
29. Pearlstein DP, Quinn CC, Burtis CC, et al.. Electromagnetic navigation bronchoscopy performed by thoracic surgeons: one center’s early success. Ann Thorac Surg. 2012;93:944–949.
30. Steinfort DP, Khor YH, Manser RL, et al.. Radial probe endobronchial ultrasound for the diagnosis of peripheral lung cancer: systematic review and meta-analysis. Eur Respir J. 2011;37:902–910.
31. Wong M, Yasufuku K, Nakajima T, et al.. Endobronchial ultrasound: new insight for the diagnosis of sarcoidosis. Eur Respir J. 2007;29:1182–1186.
32. Tremblay A, Stather DR, Maceachern P, et al.. A randomized controlled trial of standard vs endobronchial ultrasonography-guided transbronchial needle aspiration in patients with suspected sarcoidosis. Chest. 2009;136:340–346.
33. Nakajima T, Yasufuku K, Kurosu K, et al.. The role of EBUS-TBNA for the diagnosis of sarcoidosis—comparisons with other bronchoscopic diagnostic modalities. Respir Med. 2009;103:1796–1800.
34. Oki M, Saka H, Kitagawa C, et al.. Prospective study of endobronchial ultrasound-guided transbronchial needle aspiration of lymph nodes versus transbronchial lung biopsy of lung tissue for diagnosis of sarcoidosis. J Thorac Cardiovasc Surg. 2012;143:1324–1329.
35. Xiang Y, Zhang F, Akulian J, et al.. EBUS-TBNA by a new Fuji EBUS scope (with video). J Thorac Dis. 2013;5:36–39.
Keywords:

convex probe endobronchial ultrasound; endobronchial ultrasound-guided transbronchial needle aspiration; N1 lymph nodes

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