Transbronchial vs Transesophageal Needle Aspiration Using an Ultrasound Bronchoscope for the Diagnosis of Mediastinal Lesions

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Original Research Pulmonary Procedures

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Transbronchial vs Transesophageal Needle Aspiration Using an Ultrasound Bronchoscope for the Diagnosis of Mediastinal Lesions A Randomized Study Masahide Oki, MD, FCCP; Hideo Saka, MD, FCCP; Masahiko Ando, MD; Rie Tsuboi, MD; Masashi Nakahata, MD; Saori Oka, MD; Yoshihito Kogure, MD; and Chiyoe Kitagawa, MD

BACKGROUND: The purpose of this study was to compare the tolerance, efficacy, and safety of endobronchial ultrasound-guided transbronchial needle aspiration (EBUS-TBNA) with transesophageal endoscopic ultrasound-guided fine-needle aspiration (EUS-FNA) with an endobronchial ultrasound scope for the first pathologic diagnosis of lesions accessible by both procedures.

Patients who had lesions accessible by both EBUS-TBNA and EUS-FNA were enrolled and were randomized to undergo either procedure. Patients quantified tolerance, and operators charted the quality of examination using a 100-mm visual analog scale (VAS).

METHODS:

A specific diagnosis was made in 50 of 55 patients (91%) in the EBUS-TBNA group and in 48 of 55 patients (87%) in the EUS-FNA group (P 5 .76). Compared with EBUS-TBNA, EUS-FNA was associated with a shorter duration of procedure (median, 15.3 min vs 11.3 min; P , .001), lower doses of IV midazolam (mean, 4.4 mg vs 4 mg; P 5 .02) and intraairway lidocaine (mean, 303 mg vs 189 mg; P , .001), less frequent oxygen desaturations (23 of 55 vs two of 55, P , .001), and higher operator satisfaction (P , .001). There was no significant difference in patient tolerance according to the patients’ VAS. Lymph node infection occurred in one patient in the EBUS-TBNA group and in two patients in the EUS-FNA group. RESULTS:

Both EBUS-TBNA and EUS-FNA provide high accuracy with good tolerance, although the occurrence of infectious complications should be monitored carefully. EUS-FNA has the advantage of comparable tolerance with fewer doses of anesthetics and sedatives, a shorter procedure time, and fewer oxygen desaturations during the procedure.

CONCLUSIONS:

TRIAL REGISTRY:

UMIN Clinical Trials Registry; No.: UMIN000005757; URL: http://www.

umin.ac.jp/ctr/

Manuscript received May 28, 2014; revision accepted September 8, 2014; originally published Online First October 2, 2014. ABBREVIATIONS: EBUS 5 endobronchial ultrasound; EBUS-TBNA 5 endobronchial ultrasound-guided transbronchial needle aspiration; EUS 5 endoscopic ultrasound; EUS-FNA 5 endoscopic ultrasoundguided fine-needle aspiration; VAS 5 visual analog scale AFFILIATIONS: From the Department of Respiratory Medicine (Drs Oki, Saka, Tsuboi, Nakahata, Oka, Kogure, and Kitagawa), Nagoya Medical Center; and the Center for Advanced Medicine and Clinical Research (Dr Ando), Nagoya University Hospital, Nagoya, Japan.

CHEST 2015; 147(5):1259-1266

Part of this article was presented in abstract form at CHEST 2013, October 27, 2013, Chicago, IL. FUNDING/SUPPORT: The authors have reported to CHEST that no funding was received for this study. CORRESPONDENCE TO: Masahide Oki, MD, FCCP, Department of Respiratory Medicine, Nagoya Medical Center, 4-1-1 Sannomaru, Naka-ku, Nagoya 460-0001, Japan; e-mail: [email protected] © 2015 AMERICAN COLLEGE OF CHEST PHYSICIANS. Reproduction of this article is prohibited without written permission from the American College of Chest Physicians. See online for more details. DOI: 10.1378/chest.14-1283

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Mediastinal lesions adjoining both the trachea/bronchus and the esophagus can be evaluated by both endobronchial ultrasound-guided transbronchial needle aspiration (EBUS-TBNA) and transesophageal endoscopic ultrasound-guided fine-needle aspiration (EUS-FNA).1 In fact, many investigators have reported the usefulness of EBUS-TBNA or EUS-FNA as the first diagnostic procedure for mediastinal lesions such as lung cancer2,3 and sarcoidosis.4-6 Traditionally, EUS-FNA has been performed with an endoscopic ultrasound (EUS) scope by an endoscopist, but several investigators7-11 have reported that the procedure can be performed using an endo-

bronchial ultrasound (EBUS) scope in place of an EUS scope. Thus, bronchoscopists can select either EBUS-TBNA or EUS-FNA using the same devices for examining lesions adjacent to both the trachea/bronchus and the esophagus.

Materials and Methods

them necessary. Additional 2% lidocaine into the airway or IV midazolam was administered properly during the procedure if the operator deemed it necessary. If oxygen saturation decreased to , 90% for more than 20 s during the procedure, oxygen supplementation was provided to maintain oxygen saturation at . 90%. The lesion location examined; the number of the punctures; the duration of the procedure, which was measured from insertion to removal of the EBUS scope through the vocal cord; the dose of intraairway lidocaine and IV midazolam administered; and supplemental oxygen administration were recorded.

Patients A prospective study that was approved by the institutional review board of Nagoya Medical Center (identifier: 2011-403) and registered with the UMIN-Clinical Trials Registry (identifier: UMIN000005757) was carried out. Between May 2011 and January 2013, patients with hilar/mediastinal lymph nodes or tumors that were accessible with both EBUS-TBNA and EUS-FNA, who needed to have a definitive diagnosis, were enrolled. Patients who had been given a definitive pathologic diagnosis prior to bronchoscopy (eg, patients with proven lung cancer for only mediastinal staging purposes) were excluded. Patients who needed to undergo other bronchoscopic procedures such as transbronchial biopsy, brushing, and BAL were also excluded. Patients who had lesions for which either EBUS-TBNA or EUS-FNA was obviously more suitable than the other (eg, EBUS-TBNA preferred: lymph node stations 2R, 4R, and hilar lymph nodes; EUS-FNA preferred: lymph node stations 8, 9, and occasionally 5) were also excluded. Thus, the locations of the main target lesion we expected were nodal stations 2L, 3p, 4L, 7, and lung mass adjacent to the mediastinum, but some lesions in other locations accessible by both procedures (eg, large extended lesions) were also included. Randomization for EBUS-TBNA or EUS-FNA was performed by minimization with stratification factors including lymph node location (subcarinal lymph node vs others), lymph node size (ⱖ 20 mm vs , 20 mm), number of target lymph nodes (one vs two or more lesions), operator experience (staff pulmonologists vs pulmonary residents ⱕ 5 years after receiving their MD degree), and the use of rapid on-site cytologic evaluation. Written informed consent was obtained from all patients. Procedures For EBUS-TBNA and EUS-FNA, a convex probe EBUS scope (BF-UC260FOL8 or BF-UC260FW; Olympus Corporation) and 22-gauge needles (NA-201SX-4022; Olympus Corporation) were used. The endoscopic procedures were performed by staff pulmonologists or supervised pulmonary residents. Before the procedure, the upper airway was anesthetized with 4% lidocaine through a nebulizer, and bolus IV midazolam was administered for both procedures. The doses of lidocaine and midazolam were not defined in the study protocol. In patients assigned to the EBUS-TBNA group, the procedure was performed in a manner similar to that described previously.12 After the insertion of an EBUS scope into the trachea, 2% lidocaine was administered into the trachea and bronchus through the working channel using a spray catheter, and then needle aspirations for the target lesion were performed. The use of rapid on-site cytologic evaluation depended on the operator. Three punctures for each lesion were made regardless of the result of rapid on-site cytologic evaluation, but additional punctures were permitted if the operator considered

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FOR EDITORIAL COMMENT SEE PAGE 1201

However, it is unknown which procedure should be selected for examining such lesions. The purpose of this study was to compare the tolerance, efficacy, and safety of EBUS-TBNA vs EUS-FNA with an EBUS scope for the diagnosis of accessible lesions by both techniques.

In patients assigned to the EUS-FNA group, the procedure was performed at the left lateral position as described previously.9 Handling of sampled specimens, the puncture number, and the recorded items were the same as with the EBUS-TBNA procedures. Questionnaire Before randomization, patients charted their anxiety on a 100-mm visual analog scale (VAS) (0 5 no anxiety, 100 5 extreme anxiety). Two hours after the procedure, patients assessed the following items with VAS: discomfort (0 5 no discomfort, 100 5 not tolerable), satisfaction (0 5 not satisfactory, 100 5 fully satisfactory), cough (0 5 nonexistent, 100 5 unbearable), vomiting (0 5 nonexistent, 100 5 unbearable), pain (0 5 nonexistent, 100 5 unbearable), and dyspnea (0 5 nonexistent, 100 5 unbearable). Operators also assessed their satisfaction and the patient’s cough with VAS after the procedure. Study End Points The primary end point was to compare the patient-reported discomfort assessed with VAS during EBUS-TBNA and EUS-FNA. The secondary end points were to compare patient-reported satisfaction, sensations, operator-reported satisfaction and patient’s cough, diagnostic yield, procedure durations, doses of sedatives and anesthetics, and complications between the two procedures. Statistical Analysis In our previous study,13 the mean VAS score on the patient’s discomfort during bronchoscopy including EBUS-TBNA was 41.6 ⫾ 31.9 mm. Because the minimal clinically important difference with the VAS score has not been established, we simply calculated a sample size to compare the mean VAS scores between EBUS-TBNA and EUS-FNA. We estimated that with 110 patients, the study would have 90% power to detect a significant difference in the VAS score at the level of .05 with an effect size of 0.65 SD between the two diagnostic procedures. Continuous variables were analyzed using the Mann-Whitney U test, and dichotomous variables were analyzed using the Fisher exact test. The results were considered statistically significant when the two-tailed P value ⱕ .05. Statistical analyses were performed using a statistical software program (PASW Statistics 18; IBM).

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Results

Diagnostic Yields

Patients

The final diagnosis and needle aspiration results are shown in Table 2. The diagnostic yield of EBUS-TBNA and EUS-FNA was 91% (50 of 55; 83% [25 of 30] in benign disease, 100% [25 of 25] in malignant disease) and 87% (48 of 55; 88% [23 of 26] in benign disease, 86% [25 of 29] in malignant disease), respectively (P 5 .76).

Three hundred twenty consecutive patients who had an indication for EBUS-TBNA, EUS-FNA, or both were assessed for eligibility. In the study period, all EUS-FNA procedures for intrathoracic lesions were performed using an EBUS scope but not an EUS scope. Sixty-seven patients for staging purposes, 107 patients with EBUS-TBNA preferred lesions (right-sided hilar/ mediastinal lymph nodes or lung tumors in 105, leftsided hilar lymph node or lung tumor in two), eight patients with EUS-FNA preferred lesions (station 5 in three, station 8 in three, right upper-lobe tumor in one, posterior mediastinal tumor in one), two patients requiring both procedures (stations 4R and 8 in one, stations 4R and thoracic vertebral tumor in one), 10 patients requiring other bronchoscopic procedures in the same settings, two patients with known malignancy, one patient without lymphadenopathy, and 13 patients with ineligibility assessed by attending physicians were excluded. Thus, a total of 110 patients with lesions accessible to both EBUS-TBNA and EUS-FNA were enrolled. Fifty-five patients were assigned to the EBUS-TBNA group and 55 patients to the EUS-FNA group (Fig 1). Table 1 shows the baseline characteristics of patients and lesions. Seventy-seven lesions with a median of 16.3 mm in the shortest diameter on CT scan were examined in the EBUS-TBNA group, and 78 lesions with a median of 16.4 mm in the EUS-FNA group were examined. Stations 7 and 4L were the frequently examined lesions. There was no statistical difference in the baseline characteristics between the groups.

Outcome Parameters

The results of patient and operator reports are shown in Table 3. The baseline anxiety of patients before procedures was similar in both groups. According to the patients’ reports, there was no statistically significant difference in their discomfort, satisfaction, cough, vomiting, pain, and dyspnea. On the other hand, compared with EBUS-TBNA, EUS-FNA was associated with lower scores of cough (P , .001) and higher operator satisfaction according to the operator VAS (P , .001). Oxygen desaturations occurred more frequently during EBUS-TBNA procedures (23 of 55 patients [42%] in the EBUS-TBNA group and two of 55 patients [4%] in the EUS-FNA group, P , .001). The dosages of sedatives and anesthetics used are shown in Table 4. There was no statistical difference in the preprocedural dose of lidocaine for upper airway and IV midazolam between both groups; however, total doses of intraairway lidocaine and IV midazolam administered were significantly lower in the EUS- FNA group than in the EBUS-TBNA group (P 5 .02). As shown in Table 5, EUS-FNA was associated with shorter duration of the procedure (median, 15.3 min vs 11.3 min, P , .001).

Figure 1 – The flow of patients screened and enrolled in the study. EBUS-TBNA 5 endobronchial ultrasound-guided transbronchial needle aspiration; EUS-FNA 5 endoscopic ultrasound-guided fine-needle aspiration.

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Complications

One lymph node infection (2%) occurred in the EBUS-TBNA group and two (4%) in the EUS-FNA group. Two patients (one in the EBUS-TBNA group, and one in the EUS-FNA group) recovered and were discharged from our hospital after antibiotic treatment. Infectious symptoms of the remaining patient in the EUS-FNA group were also relieved after antibiotic treatment, but the patient with stage IV squamous cell lung cancer with poor performance status died because of the progression of lung cancer 54 days after the procedure.

Discussion To our knowledge, this is the first randomized study to compare both EBUS-TBNA and EUS-FNA directly as a TABLE 1

first diagnostic procedure in patients with accessible lesions. We demonstrated that both EBUS-TBNA and EUS-FNA provided a high diagnostic yield of approximately 90%, with good tolerance in the diagnosis of accessible lesions. EUS-FNA has the advantage of comparable tolerance with fewer doses of anesthetics and sedatives, shorter procedure time, and fewer oxygen desaturations during the procedure. EBUS-TBNA and EUS-FNA have been reported to be comparably accurate and safe procedures for the diagnosis of mediastinal lesions.2-5 The accessibility of EBUS-TBNA to the mediastinum is greater than that of EUS-FNA,8 but some regions can be accessed by both procedures. Although EUS-FNA, even using an EUS

] Characteristics of Patients and Lesions

Characteristics No. patients

EBUS-TBNA

P Value

EUS-FNA

55

55

Male (female)

36 (19)

39 (16)

.68

…

Age, median (range), y

64 (25-83)

65 (28-83)

.50

Body weight, median (range), kg

62 (38-86)

60 (37-88)

.55

77

78

…

33 (22)

32 (23)

No. lesions examined Total number 1 lesion (2 lesions)

1.00

Lesion size Median (range), mm , 20 mm (ⱖ 20 mm)

16.3 (9.0-62.0)

16.4 (8.6-62.0)

.72

53 (24)

54 (24)

1.00

0

1

…

2L

1

0

…

3p

3

3

…

4L

16

24

…

7

43

44

.54

10R

1

0

…

10L

7

3

…

11L

1

0

…

Right upper lobe

3

3

…

Left upper lobe

1

0

…

Right lower lobe

1

0

…

14 (41)

14 (41)

1.00

30 (25)

26 (29)

.57

45 (10)

45 (10)

1.00

Location of lesion examined 2R

Use of ROSE With ROSE (without ROSE) Primary disease Benign (malignant) Bronchoscopy Initial bronchoscopy (previous nondiagnostic bronchoscopy)

EBUS-TBNA 5 endobronchial ultrasound-guided transbronchial needle aspiration; EUS-FNA 5 endoscopic ultrasound-guided fine-needle aspiration; ROSE 5 rapid on-site cytologic evaluation.

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TABLE 2

] Final Diagnosis and Needle Aspiration Results No. Patients (Final Diagnosis)

Pathologic Findings

EBUS-TBNA

EUS-FNA

Diagnostic Malignant Primary lung cancer Adenocarcinoma

11

13

Squamous cell carcinoma

5

8

Large cell carcinoma Non-small cell carcinoma Small cell carcinoma Metastatic adenocarcinoma

…

…

5

2

1 (gastric cancer)

Metastatic squamous cell carcinoma Diffuse large B-cell lymphoma

1

1

…

…

1 (esophageal cancer)

2

…

Benign Epithelioid cell granuloma with/without necrosis

25 (25 sarcoidosis)

23 (22 sarcoidosis, 1 TB)

Suspicious findings of epithelioid cell granuloma

2 (2 sarcoidosis)

1 (1 sarcoidosis)

Nonrepresentative samples

3 (3 suspected benign lesion with unchanged size)

6 (1 adenocarcinoma, 1 malignant mesothelioma. 2 suspected benign lesion with unchanged size, 2 suspected malignant lesion with increased size)

Nondiagnostic

See Table 1 for expansion of abbreviations.

scope, has been considered to have better tolerability than EBUS-TBNA,14,15 there is no consensus as to which procedure should be performed for each case. As shown in Table 3, all items on procedure tolerance reported by patients after including discomfort, satisfaction, cough, vomiting, pain, and dyspnea were superior in the EUS-FNA TABLE 3

group, but the difference was not statistically significant. Actually, as shown by the operator’s report, cough was significantly more frequent during EBUS-TBNA than during EUS-FNA. A similar tolerance during both procedures should be achieved by an adequate amount of sedatives and anesthetics. The advantage of EUS-FNA is

] Outcome Parameters

Variables Oxygen desaturations, with (without)

EBUS-TBNA (n 5 55) 23 (32)

EUS-FNA (n 5 55) 2 (53)

P Value , .001

Patient reports Anxiety before procedure, VAS, mm

52.0 ⫾ 27.3

55.2 ⫾ 26.6

.50

Discomfort, VAS, mm

16.7 ⫾ 24.2

10.0 ⫾ 17.8

.40

Satisfaction, VAS, mm

85.2 ⫾ 21.0

90.1 ⫾ 16.0

.47

Cough, VAS, mm

12.4 ⫾ 22.7

4.9 ⫾ 12.6

.41

Vomiting, VAS, mm

4.9 ⫾ 10.8

2.8 ⫾ 7.0

.87

Pain, VAS, mm

7.4 ⫾ 19.6

1.3 ⫾ 3.8

.57

Dyspnea, VAS, mm

8.1 ⫾ 19.4

1.8 ⫾ 5.0

.27

Operator reports Satisfaction, VAS, mm

66.3 ⫾ 23.5

80.6 ⫾ 21.0

, .001

Cough, VAS, mm

45.4 ⫾ 24.5

7.0 ⫾ 11.5

, .001

Data are presented as mean ⫾ SD unless indicated otherwise. VAS 5 visual analog scale. See Table 1 for expansion of other abbreviations.

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TABLE 4

] Dose of Sedatives and Anesthetics

Variables

EBUS-TBNA (n 5 55)

EUS-FNA (n 5 55)

P Value

191.3 ⫾ 67.0

188.7 ⫾ 84.8

.87

Intraairway lidocaine dose Before procedure, mg During procedure, mg

111.3 ⫾ 47.4

0

, .001

Total, mg

302.5 ⫾ 78.1

188.7 ⫾ 84.8

, .001

Before procedure, mg

4.00 ⫾ 0.84

3.93 ⫾ 0.60

.34

During procedure, mg

0.35 ⫾ 0.75

0.04 ⫾ 0.29

.003

Total, mg

4.35 ⫾ 1.21

3.96 ⫾ 0.72

.02

IV midazolam dose

Data are presented as mean ⫾ SD. See Table 1 for expansion of abbreviations.

that the comparable tolerance can be achieved with fewer doses of anesthetics and sedatives. Another advantage of EUS-FNA is the shorter procedure time. This is because local anesthesia is not needed during the procedure and because of the ease of puncturing the esophageal wall. On the other hand, local anesthesia with lidocaine is necessary during EBUS-TBNA, and because the tracheobronchial cartilage prevents penetration during EBUS-TBNA, we should often reposition the puncture site. Moreover, EUS-FNA has the advantage of fewer oxygen desaturations. Because of these advantages, we prefer EUS-FNA to EBUS-TBNA. In fact, the operator’s satisfaction was significantly higher in EUS-FNA than in EBUS-TBNA. Put another way, we can perform EBUS-TBNA with similar tolerance to EUS-FNA when we use a sufficient amount of anesthetics, sedatives, and supplemental oxygen. It is undoubtable that we have to continue efforts to increase patient tolerance and satisfaction,16 but the most important thing we have to do is to provide a successful diagnostic result for the patient.17 There is a learning curve to achieve satisfactory results with these procedures,18,19 and most bronchoscopists may be more familiar with EBUS-TBNA than EUS-FNA. The choice of procedure depends on the operator’s experience and skill.

TABLE 5

Bronchoscopy training, including didactic training and hands-on training with animal models, plastic airway models, or virtual-reality simulators, has been reported to be associated with better outcomes in comparison with no training.20 In the survey of training for EBUS among US pulmonary fellowships,21 EBUS was reported to have rapidly disseminated into fellowship training programs. The goal of training in EBUS-TBNA is independent successful performance, and some objective assessment tools for competency have been proposed.22 On the other hand, because EUS-FNA with an EBUS scope is a relatively new and underused technique, the best way to train is still unknown. In our study, one experienced expert, who had been trained by an expert gastroenterologist, supervised with verbal instructions during all procedures. Before starting the EUS-FNA procedure, pulmonologists should obtain training from an expert gastroenterologist and obtain privileges from respected institutions, and local guidelines should be followed to perform this procedure safely and accurately. The occurrence of severe complications associated with EBUS-TBNA and EUS-FNA has been reported to be very rare.23,24 However, as the procedures have become popular, reports on severe complications, especially infectious complications, have increased. In a Japanese survey on the complications associated with EBUS-TBNA,25 the

] Durations of Procedures EBUS-TBNA

No. Lesions Aspirated

Patients, No. (%)

Procedure Duration, Median (Range), min

EUS-FNA Patients, No. (%)

Procedure Duration, Median (Range), min

P Value

1

33 (60)

12.0 (7.8-28.0)

32 (58)

8.0 (5.8-22.8)

, .001

2

22 (40)

18.3 (15.3-55.5)

23 (42)

14.5 (9.5-25.0)

, .001

Total

55 (100)

15.3 (7.8-55.5)

55 (100)

11.3 (5.8-25.0)

, .001

See Table 1 for expansion of abbreviations.

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occurrence of infectious complications was reported to be 14 among all 7,345 cases (0.19%; mediastinitis in seven, pneumonia in four, pericarditis in one, cyst infection in one, and sepsis in one). The authors described the possibility of recall bias in the retrospective questionnaire survey as a limitation, and so the reported frequency may be the minimum. Oguri et al26 reported three cases with infectious complications among the lesions examined by EBUS-TBNA. The complications occurred in their institution among a total of 48 consecutive cases who had undergone EBUS-TBNA during 9 months. They suggested that a large mass with necrosis is associated with the occurrence of infectious complications. In our study, two patients with infectious complications in the EUS-FNA group had a necrotic lymph node, which may be associated with the occurrence of infectious complications. In the needle aspiration procedures for necrotic lesions, reducing the puncture number (eg, with the use of rapid on-site cytologic evaluation12) may decrease the complications. Another possible reason is inadequate punctures. In our study, the operators had difficulty puncturing the lymph node in one patient in each group.

Acknowledgments Author contributions: M. O. was the principal author and had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. M. O., H. S., M. A., R. T., M. N., S. O., Y. K., and C. K. contributed to the study design and approval of the final manuscript; M. O., H. S., R. T., M. N., S. O., and Y. K. contributed to the performance of procedures; M. O. and H. S. contributed to the data collection; and M. O., H. S., and M. A. contributed to the data analysis and interpretation and preparation of the manuscript. Financial/nonfinancial disclosures: The authors have reported to CHEST that no potential conflicts of interest exist with any companies/organizations whose products or services may be discussed in this article.

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They were finally able to obtain three to five specimens, but several further punctures were attempted and failed during the procedures. Actually, the procedure time in the two patients was much longer than the median. To ensure a safer procedure, a certain level of experience and skills may be necessary. The limitation of our study is that it was carried out at a single institution. Although the operators had a variety of skills, our team may have had relatively more extensive experience in performing needle aspiration procedures. Naturally, the evidence level of the single-center study is lower than that of larger multicenter studies.

Conclusions In conclusion, both EBUS-TBNA and EUS-FNA provide high accuracy with good tolerance, although the occurrence of infectious complications should be monitored carefully. EUS-FNA has the advantages of comparable tolerance with a lower dose of anesthetics and sedatives, a shorter procedure time, and fewer oxygen desaturations during the procedure.

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