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Ann Thorac Surg 2008;86:1104-1110. doi:10.1016/j.athoracsur.2008.06.042
© 2008 The Society of Thoracic Surgeons
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Original Articles: General Thoracic

Endobronchial Ultrasound-Guided Fine-Needle Aspiration of Mediastinal Lymph Nodes: A Single Institution's Early Learning Curve

Shawn S. Groth, MDa, Bryan A. Whitson, MD, PhDa, Jonathan D'Cunha, MD, PhDa, Michael A. Maddaus, MDa, Mariam Alsharif, MDb, Rafael S. Andrade, MDa,*

a Department of Surgery, Division of Thoracic and Foregut Surgery, University of Minnesota, Minneapolis, Minnesota
b Department of Laboratory Medicine and Pathology, University of Minnesota, Minneapolis, Minnesota

Accepted for publication June 11, 2008.

* Address correspondence to Dr Andrade, Division of Thoracic and Foregut Surgery, MMC 207, 420 Delaware St SE, Minneapolis, MN 55455 (Email: andr0119{at}umn.edu).

Presented at the Forty-fourth Annual Meeting of The Society of Thoracic Surgeons, Fort Lauderdale, FL, Jan 28–30, 2008.


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Discussion
 Acknowledgments
 References
 
Background: The gold standard for mediastinal lymph node evaluation is mediastinoscopy, which is invasive and allows access to only a limited number of mediastinal lymph node (MLN) stations (1, 2, 3, 4, and 7). Endobronchial ultrasound-guided fine-needle aspiration (EBUS-FNA) is emerging as a useful, less invasive technique that offers access to a wider range of MLN stations (2, 3, 4, 7, 10, and 11). We report our initial experience with this procedure.

Methods: Using our prospectively maintained database, we performed a single-institution retrospective chart review. Our study group consisted of all patients at the University of Minnesota who underwent EBUS-FNA for evaluation of mediastinal lymphadenopathy or for thoracic malignancy staging from September 1, 2006, through December 15, 2007. To assess our learning curve, we plotted the cumulative sensitivity (%) and accuracy (%) of our EBUS-FNA results as a function of the number of procedures we performed.

Results: During the study period, 100 patients underwent EBUS, 92 with FNA. Of these, 56 patients (34 women, 22 men; mean age, 60.4 ± 13.7 years) met our inclusion criteria. We found no complications. After our first 10 procedures, the sensitivity of our EBUS-FNA results was 96.2%; accuracy was 97.8% (rates comparable with other large series in the literature).

Conclusions: We conclude that the learning curve for EBUS-FNA for thoracic surgeons is about 10 procedures.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Discussion
 Acknowledgments
 References
 
Evaluation of mediastinal lymphadenopathy and of mediastinal lymph node (MLN) staging for thoracic malignancies often requires a biopsy, as current imaging modalities are insufficiently sensitive, specific, and accurate. Integrated positron emission tomography (PET)–computed tomography (CT) scans are more sensitive (60% to 89%) [1–7] in MLN staging, as compared with either CT alone (43% to 87%) [1, 5–13] or PET alone (67% to 96%) [1–5, 8–11, 14]. Nonetheless, histologic confirmation is often required, particularly if a patient is considered at risk for LN metastases and if treatment would be affected by these findings [15].

Mediastinoscopy is the gold standard for histologic evaluation of mediastinal lymphadenopathy and MLN staging for thoracic malignancies. As demonstrated by large institutional series, the sensitivity of standard cervical mediastinoscopy ranges from 86% to 93% [16–22], diagnostic accuracy ranges from 93% to 96% [16–18, 21, 22], and it is associated with a low morbidity rate (0.6% to 1.1%) and a low mortality rate (0.05% to 0.2%) [18, 19]. However, mediastinoscopy is invasive and allows access to only a limited number of American Thoracic Society MLN stations [23] (1, 2, 3, 4, and 7). Consequently, interest is growing in alternative, less invasive MLN biopsy techniques that provide access to a wider range of MLN stations.

One such technique is transbronchial needle aspiration. It is less invasive than mediastinoscopy and allows access to a wider range of MLN stations (2, 3, 4, 7, 10, and 11) [24, 25], but conventional transbronchial needle aspiration is performed blindly (without precise knowledge of the location of the MLN being biopsied), resulting in wide variability in diagnostic yield.

Recently, endobronchial ultrasound (EBUS) [26–30] has generated considerable interest as a simple and precise method to improve the diagnostic yield of transbronchial needle aspiration. As demonstrated in a randomized trial, EBUS-guided fine-needle aspiration (EBUS-FNA) affords significantly (p < 0.05) greater diagnostic yield (80%) as compared with conventional transbronchial needle aspiration (71%) [27]. Moreover, the development of a linear scanning probe now allows real-time procedure guidance [31–37], resulting in excellent sensitivity (89% to 99%) and diagnostic yield (85% to 99%) [31, 33, 34, 37].

We undertook this study to examine our learning curve with EBUS-FNA to obtain biopsies of MLNs in patients with benign and malignant disease.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Discussion
 Acknowledgments
 References
 
Patients
The Institutional Review Board of the University of Minnesota approved this retrospective review of our prospectively maintained database and waived the need to obtain informed consent for each patient. We studied the charts of all consecutive patients who underwent EBUS-FNA at our institution for evaluation of mediastinal lymphadenopathy or staging of thoracic malignancy from September 1, 2006 (when we first performed EBUS-FNA), through December 15, 2007. We included patients in our analysis if (1) their malignancy diagnosis was based on immediate EBUS-FNA cytology or if (2) they underwent a confirmatory procedure (ie, mediastinoscopy or thoracoscopy) that sampled the same MLN stations biopsied by EBUS-FNA to verify normal, benign, or nondiagnostic EBUS-FNA findings.

We excluded patients with a benign or nondiagnostic biopsy result by EBUS-FNA who underwent a confirmatory procedure that sampled different MLN stations than those sampled by EBUS-FNA, because we would not be able to verify our EBUS-FNA findings in these patients. We also excluded patients who underwent EBUS-FNA of peribronchial masses. For our analysis, we looked at patient characteristics, preoperative treatment factors (eg, chemotherapy and radiation therapy), indications for EBUS, and results of immediate and permanent cytology and histology testing.

Endobronchial Ultrasound–Guided Fine-Needle Aspiration
Our EBUS-FNA procedures were performed principally by one board-certified thoracic surgeon (R.S.A.). Before beginning an EBUS-FNA practice at our institution, the surgeon enrolled in a 2-day certified EBUS-FNA training course and spent 3 days being proctored by a physician with extensive experience with EBUS-FNA.

Patients were under general anesthesia (endotracheal tube size ≥ 8.5 mm). We used an ultrasonographic bronchofibervideoscope (Olympus Exera; Olympus Imaging American, Center Valley, Pennsylvania), with real-time ultrasonographic guidance provided by integrated color Doppler. Thus, we were able to easily identify vascular structures and to obtain accurate access to MLNs (Fig 1). Using a 22G aspiration needle (Vizishot; Olympus Medical Systems, Tokyo, Japan), we obtained MLN samples from stations 2, 3, 4, 7, 10, or 11 (Fig 2); for lung cancer staging, each of these MLN stations is routinely sampled for all patients, regardless of PET/CT findings or ultrasonographic appearance. With 10 to 15 needle passes, we accessed each target MLN 1 to 3 times. If adequate MLN tissue was not obtained after 3 attempts, an alternative MLN biopsy technique (ie, mediastinoscopy thoracoscopy, or thoracotomy) was performed. On each MLN sample, we performed immediate and permanent cytology testing. As determined by the cytologist (M.A.), the adequacy of cytology specimens was defined by the presence of lymphocytes. All patients without a histologic diagnosis of cancer per immediate cytology testing from our EBUS-FNA procedure (ie, normal LN tissue, benign pathology, or nondiagnostic specimens) underwent confirmatory MLN biopsies with an alternative procedure (ie, mediastinoscopy or thoracoscopy), to minimize the risk of failing to diagnose a malignancy. Permanent histologic specimens were fixed in formalin.


Figure 1
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  		Fig 1. Endobronchial ultrasonography image, with color Doppler of an artery and vein.

 

Figure 2
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  		Fig 2. Real-time ultrasonography image of a fine-needle aspiration of a mediastinal lymph node (MLN).

 
Statistical Analysis
For overall diagnosis (based on immediate cytology testing), we defined a true positive result by the presence of any abnormal MLN pathology, whether benign (eg, granuloma or hyperplasia) or malignant. We defined a true negative result if the sample was normal (and adequate). If the sample was nondiagnostic or if it was deemed normal after completion of EBUS-FNA but then abnormal after a confirmatory procedure, we defined the result as a false negative. If the sample was deemed abnormal after completion of EBUS-FNA but then normal after a confirmatory procedure, we defined the result as a false positive.

For cancer diagnosis (based on immediate cytology testing), we defined a true positive by the presence of malignant MLN pathology; true negative, by a normal or benign (and adequate) sample. If the sample was nondiagnostic, or if it was deemed normal after completion of EBUS-FNA but then malignant after a confirmatory procedure, we defined the result as a false negative. If the sample was deemed malignant after completion of EBUS but then normal after a confirmatory procedure, we defined the result as a false positive.

We used the standard definitions of sensitivity (true positive/[true positive + false negative]), specificity (true negative/[true negative + false positive]), positive predictive value (true positive/[true positive + false positive]), negative predictive value (true negative/[true negative + false negative]), and accuracy ([true positive + true negative]/[true positive + true negative + false positive + false negative]). To examine our learning curve, we plotted cumulative sensitivity (%) of our EBUS-FNA results over time.

To analyze our data, we used SAS version 9.1 (SAS Institute, Cary, North Carolina). We herein report results, where appropriate, as mean ± SD. To examine any potential confounding effects on our false negative rate and accuracy, we stratified patients by chemotherapy or radiation therapy before EBUS-FNA. To compare between strata, we used either a {chi}2 test or a Fisher's exact test, depending on the number of expected counts. For all statistical testing, we used a two-sided significance level of 0.05.


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Discussion
 Acknowledgments
 References
 
During the study period, 100 patients underwent EBUS at our institution; 92 underwent EBUS-FNA. Of these, 56 patients (34 women, 22 men; mean age, 60.4 ± 13.7 years) met our inclusion criteria (Fig 3). The most common indication for EBUS-FNA was assessment of mediastinal lymphadenopathy in the absence of a known malignancy (69.6%). A total of 8 patients completed preoperative chemotherapy; 5 completed preoperative radiation therapy (Table 1). To confirm benign or nondiagnostic EBUS-FNA findings, we performed 26 mediastinoscopies, 5 thoracoscopic MLN biopsies, and 2 thoracotomies with MLN biopsies.


Figure 3
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  		Fig 3. Study group algorithm. (EBUS = endobronchial ultrasonography; FNA = fine-needle aspiration; MLN = mediastinal lymph node.)

 

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  		Table 1 Patient Characteristics
 
Using EBUS-FNA, we diagnosed a variety of benign and malignant diseases (Table 2), including 2 cases of lymphoma (confirmed by identical flow cytometry results from tissue obtained by EBUS-FNA and mediastinoscopy). We found no perioperative complications.


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  		Table 2 Diagnoses by Endobronchial Ultrasound-Guided Fine-Needle Aspiration
 
By plotting the cumulative sensitivity (%) of our EBUS-FNA results over time, we noted a significant improvement in both sensitivity and diagnostic accuracy for both overall diagnosis and cancer diagnosis after our first 10 procedures (Table 3). Excluding the results from our first 10 patients (because 10 was the number of procedures we needed to perform to overcome our learning curve), EBUS-FNA had a sensitivity of 93.3% and an accuracy of 96.7% for patients undergoing EBUS-FNA for assessment of mediastinal lymphadenopathy in the absence of a known malignancy. The smallest MLN that we obtained diagnostic tissue from was 4.5 mm. Neither chemotherapy nor radiation therapy had a significant (p > 0.2) adverse effect on the sensitivity or accuracy of EBUS-FNA (data not shown). However, the number of these patients is too small to draw valid conclusions.


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  		Table 3 Diagnostic Ability of Endobronchial Ultrasound-Guided Fine-Needle Aspiration as Function of Surgeon Experience
 
In 23 of our 56 patients, a cancer diagnosis was achieved with EBUS-FNA, so a more invasive diagnostic procedure (ie, mediastinoscopy, thoracoscopy, or thoracotomy) was avoided. For patients who required an additional diagnostic procedure, there were no complications.

Excluding the results from our first 10 patients (because 10 was the number of procedures we needed to perform to overcome our learning curve), we correctly established the diagnosis in 14 (87.5%) of 16 patients who underwent EBUS-FNA of stations 10 and 11—stations not accessible by mediastinoscopy.


   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Discussion
 Acknowledgments
 References
 
We demonstrated that, after a relatively small number of EBUS-FNA cases (about 10), thoracic surgeons can achieve excellent sensitivity (96.4%) and diagnostic accuracy (97.8%) in the assessment of MLNs. Our EBUS-FNA results were substantiated by confirmatory procedures, such as mediastinoscopy or thoracoscopy. Our findings are in concordance with the findings from other large series of EBUS-FNA cases. Herth and coworkers [31], in a study of 502 patients with mediastinal or hilar lymphadenopathy, demonstrated a sensitivity of 94% and an overall diagnostic accuracy of 94%. Similarly, Yasufuku and associates [35] achieved a sensitivity of 92.3% and a diagnostic accuracy of 98% in a series of 108 patients with suspected or proven lung cancer. Vincent and coworkers [34] reported a sensitivity of 99.1% and a diagnostic accuracy of 98.7% in 152 patients. The sensitivity and accuracy of EBUS-FNA appears to be comparable with that of mediastinoscopy [16–22], but a formal comparison is still required.

Although not available at all institutions, we believe that rapid on-site cytology plays a critical role in MLN assessment since it facilitates rapid clinical decision making. If the cytology specimen is inadequate or nondiagnostic, it allows the surgeon to determine (in the same anesthesia setting) if additional MLN tissue using EBUS-FNA (or an alternative MLN biopsy technique) is required. Currently, we proceed with a lobectomy in the same anesthesia setting as EBUS-FNA if we can biopsy all relevant LN stations and obtain a satisfactory negative sample. For patients with a cytologic confirmation of advanced disease, an intravenous subcutaneous port or a stent may be placed in the same anesthesia setting.

We believe thoracic surgeons are ideally suited for EBUS-FNA for three reasons: (1) they are intimately involved in the diagnosis, staging, and treatment of thoracic malignancies; (2) they are capable of performing additional diagnostic procedures if necessary (eg, mediastinoscopy, thoracoscopy); and (3) they have the option of offering a therapeutic intervention at the same time as EBUS-FNA (eg, resection, stenting). The ability to achieve as many diagnostic and therapeutic goals in one setting is crucial for the expeditious workup and well-being of patients.

Endobronchial ultrasound-guided FNA has several distinct advantages over mediastinoscopy. First, it allows access to more MLN stations than mediastinoscopy, as evidenced by our diagnostic yield of 87.5% for stations 10 and 11. Although histologic assessment of N1 MLNs does not currently impact surgical decision-making, accurate preoperative identification of patients with N1 disease could facilitate enrollment in potential future clinical trials and translational research studies.

Second, EBUS-FNA is less invasive than mediastinoscopy. Although the complication rate for mediastinoscopy is very low (less than 1%) [18, 19], the potential complications can be severe (eg, significant hemorrhage). Complications from EBUS-FNA, however, are exceedingly rare. Real-time ultrasound guidance with integrated color Doppler allows easy identification of vascular structures and minimizes the risk for significant bleeding. More than 1,000 EBUS-FNA procedures have now been reported in the literature, all without significant complications [31, 33, 34, 37, 38].

Third, reevaluation of the mediastinum after a previous mediastinoscopy, MLN dissection, or neoadjuvant therapy is likely safer with EBUS-FNA than with mediastinoscopy. However, our experience in such settings is limited. No studies have specifically addressed the accuracy and safety of EBUS-FNA under such circumstances.

Fourth, a potential advantage of EBUS-FNA is the ability to sample MLNs without general anesthesia; the diagnostic accuracy of EBUS-FNA with or without general anesthesia is similar [31]. In our experience, the vast majority of patients who are candidates for evaluation and treatment of thoracic malignancies can undergo general anesthesia. Doing so is usually more comfortable for patients and may allow for more thorough staging of MLNs that are of normal size and appearance on ultrasonography. Sampling of small paratracheal MLNs is challenging and can be facilitated with the use of intermittent apnea. Additionally, endoscopic ultrasound-guided fine-needle aspiration may also be performed in the same setting, without repositioning the patient or further topical anesthetic maneuvers. The combination of EBUS-FNA and endoscopic ultrasound-guided fine-needle aspiration allows near-complete mediastinal staging without a skin incision.

We recognize several limitations to our study. One is that our learning curve may have been slightly more than 10 patients. Our exclusion criteria were designed to allow us to achieve the most accurate representation of the sensitivity and accuracy of EBUS-FNA for sampling MLNs—all noncancer EBUS-FNA findings were corroborated by a confirmatory procedure to ensure the absence of sampling error. Consequently, patients without a cancer diagnosis per immediate EBUS-FNA cytology and patients who did not undergo a confirmatory procedure that sampled the same MLN station biopsied by EBUS-FNA were excluded from our analysis. Only 2 such patients were excluded before we overcame our learning curve (10 patients). The goal of our study, however, was not to strictly define a number of procedures needed to overcome the learning curve for EBUS-FNA. Rather, the goal was to demonstrate that thoracic surgeons can achieve excellent results after a relatively short learning curve. Another limitation is that our study is reflective of a single thoracic surgeon's experience. Nonetheless, we believe that most thoracic surgeons can achieve excellent results after a relatively short learning curve because of their experience with bronchoscopy and intimate understanding of mediastinal anatomy.

Several unanswered questions regarding EBUS-FNA remain: How accurate is EBUS-FNA in patients with a previously treated mediastinum? How cost effective is EBUS-FNA, as compared with mediastinoscopy? Will EBUS-guided techniques provide an opportunity for the delivery of novel forms of treatment (eg, brachytherapy, intratumoral agents)?

In conclusion, we demonstrated that EBUS-FNA is a safe, minimally invasive technique that allows access to more MLNs than mediastinoscopy does. After a relatively short learning curve, diagnostic results similar to those of mediastinoscopy can be achieved. We urge thoracic surgeons to become familiar with this technique, thoracic surgery residency programs to incorporate this procedure into their curricula, and thoracic surgical societies to become involved in certifying EBUS-FNA credentials.


   Discussion
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
Acknowledgments
 References
 
DR ROBERT J. CERFOLIO (Birmingham, AL): Excellent presentation. I think your last slide about the teaching and the certification of EBUS is critical. We've gone through this at UAB and the politics of how to institute EBUS in an academic institution should not be underestimated—the pulmonologists want to be able to do it so they can attract their fellows, the surgeons, we want to be able to do it for our fellows, our gastrointestinal expert wants to do it because he does the endoscopic ultrasound-guided fine needle aspiration and it is best for the patient to be able to do the two together. So how have you worked it out and how can you help educate the rest of us to put this in your hospital and make everybody happy, your GI guy, your pulmonologists, and the surgeons who should be learning how to do it?

DR GROTH: That's a great question. We believe that the care of the patient is a global process and that a multidisciplinary approach is crucial. Potential conflicts with pulmonologists and gastroenterologists can be worked out at the institutional level. The EBUS program at our institution was initiated by thoracic surgeons and was met positively by our pulmonologists. Performing as many therapeutic and diagnostic interventions safely in one setting is in the patient's best interest. This can be accomplished by a thoracic surgeon who is proficient at EBUS, EUS, and all other methods of mediastinal staging.

DR CAROLYN E. REED (Charleston, SC): I really enjoyed your paper. We have embraced EBUS for a long time. I have a couple of points. One, I assume that you did your study in the operating room because of this comparison. To be cost effective, it's critical that EBUS be done in an outpatient setting.

DR GROTH: Yes.

DR REED: And it's very easy to do, so I assume you're doing that now. That's number one. Number two, I agree with everything you've listed regarding thoracic surgeons. The other thing is, it has become clear to me in working with interventional pulmonologists who do this procedure that they really don't have as firm a grasp of anatomy as we do, and one of the common things that they will say is, "Well, we just didn't see a level 4 lymph node." You and I know that there is always a level 4 lymph node there, and yet they say, "Well, it wasn't there."

The third thing that I would say is that there are a number of people now who are actually using EBUS also in the esophagus, so that at one setting, with one instrument, you can get almost a total medical mediastinoscopy. Thank you.

DR GROTH: Thank you, Dr Reed. To answer your first question, we prefer to do EBUS under general anesthesia, it is more comfortable for patients and allows access to small lymph nodes in difficult locations where intermittent apnea may be required.

Second, I agree with you that there are always lymph nodes in all stations. On rare occasions we may not be able to see them and consequently cannot biopsy them. Under those circumstances it is critical to perform a mediastinoscopy or some other procedure to accomplish accurate staging.

We currently perform EUS for mediastinal staging as well and will also pass the EBUS scope down the esophagus if necessary. It is important to be trained and credentialed in EUS to do this.

DR FRANK C. DETTERBECK (New Haven, CT): I have one comment and one question. The comment is that with any new technology, we see that the early results are always much better than they are years later with more refined technology. It's true for CT. It was true for PET. It's true for everything. So we have to be a little bit careful. So EBUS is newer. It looks better than mediastinoscopy. But 5 years from now, it may not be as different.

My question, though, is about the size of lymph nodes. My impression is that the needle-based techniques, like EBUS or EUS, are more dependent on the size of the lymph node you're aiming for as opposed to mediastinoscopy. Do you have any comments about that from your study?

DR GROTH: Thank you, Dr Detterbeck. We have been able to achieve diagnostic tissue from lymph nodes as small as 4.5 mm. We biopsy lymph nodes regardless of their size or ultrasonographic appearance.

DR AKIF TURNA (Istanbul, Turkey): Could you explain the lymph node dissection methods applied during this study? When you use less invasive lymph node dissection during the surgery, it is very possible to get higher sensitivity and specificity rates, and it's especially tricky about the 4L station.

DR GROTH: We thoroughly look at all lymph node stations, again, 2, 3, 4, 7, 10, and 11, and any relevant masses that are accessible by EBUS. We are very meticulous in our mediastinal lymph node dissections and make sure we resect lymph nodes from all stations, regardless of the approach.

DR TURNA: Did you resect 4L lymph nodes in all left-sided patients?

DR GROTH: No, not generally on left-sided procedures.


   Acknowledgments
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
 Acknowledgments
References
 
We would like to thank Mary Knatterud, PhD, for her invaluable editorial assistance.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
 Acknowledgments
 References
 

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