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Thoracic Cancer ISSN 1759-7706

INVITED REVIEW

Endobronchial ultrasound (EBUS) with tranbronchial needle


aspiration (TBNA) versus mediastinoscopy for mediastinal
staging in non-small cell lung cancer (NSCLC) thoracic cancer
Basil Nasir1, Robert J. Cerfolio1,2 & Ayesha S. Bryant1
1 Division of Cardiothoracic Surgery, University of Alabama at Birmingham, Birmingham, Alabama, USA
2 Section of Thoracic Surgery, JH Estes Endowed Chair for Lung Cancer Research, University of Alabama at Birmingham, Birmingham, Alabama, USA

Keywords Abstract
endobronchial ultrasound; mediastinoscopy;
staging lung cancer. Lung cancer is the leading cause of cancer deaths worldwide and is responsible for
more cancer deaths than the next three most common cancers combined. Despite
Correspondence common use of the best non-invasive tests for assessing clinical stage: computed
Robert J. Cerfolio, Division of Cardiothoracic
tomography (CT) and integrated positron emission tomography/computed tomog-
Surgery, University of Alabama at Birmingham,
703 19thStreet South, Birmingham, AL 35294,
raphy (PET/CT) using 2-deoxy-2-18-fluoro-D-glucose (FDG), the pathologic stage
USA. is often different. The status of mediastinal (N2) lymph nodes is paramount in
Tel: +1 205 934 5937 guiding therapy towards surgery, chemotherapy, radiotherapy or a combination of
Fax: +1 205 975 2815 these modalities. Accurate staging is mandatory for patients prior to commencing
Email: rcerfolio@uab.edu therapy. Invasive tests that afford tissue biopsies of N2 lymph nodes are: esophageal
ultrasound with fine needle aspiration (EUS-FNA), endobronchial ultrasound
Received: 1 December 2011;
(EBUS-TBNA), and mediastinoscopy. This review article compares the two most
accepted 19 December 2011.
commonly used invasive methods to obtain tissue biopsies of mediastinal (N2)
doi: 10.1111/j.1759-7714.2011.00106.x lymph nodes: mediastinoscopy and endobronchial ultrasound (EBUS).

chemotherapy and/or radiotherapy without having tissue


Introduction
biopsies to prove N2 or N3 disease. We see at least one of these
Lung cancer is the leading cause of cancer deaths worldwide patients a week in our clinic. Too often we are requested to
and is responsible for more cancer deaths than the next three offer surgical resection after induction therapy but the
most common cancers combined.1,2 Despite the common patient’s initial stage was never proven. Therefore, the benefit
use of the best non-invasive tests for assessing clinical stage: of surgery compared to the risk is difficult to ascertain.
computed tomography (CT) and integrated positron emis- Patients with lung cancer or a suspicious pulmonary mass
sion tomography/computed tomography (PET/CT) using who have lymphadenopathy by computed tomography (CT)
2-deoxy-2-18-fluoro-D-glucose (FDG), the pathologic stage (greater than 1 cm in size) or suspicious fluoro-D-glucose
often is different.3,4 (FDG) avidity by positron emission tomography PET/CT
The status of mediastinal (N2) lymph nodes is paramount (often defined as a maximum standardized uptake value
in guiding therapy towards surgery, chemotherapy, radio- (maxSUV) greater than 2.5), should undergo tissue sampling
therapy or a combination of these modalities.5 Accurate before undergoing further treatment.6–9 Figure 1 depicts the
staging is mandatory for patients prior to commencing current International Association for the Study of Lung
therapy. Invasive tests that afford tissue biopsies of N2 lymph Cancer lymph node map and the modalities commonly used
nodes are: esophageal ultrasound with fine needle aspiration to sample those nodes.10 This review article compares the two
(EUS-FNA), endobronchial ultrasound (EBUS-TBNA) and most commonly used invasive methods to obtain tissue biop-
mediastinoscopy. Yet too frequently they are not done. sies of mediastinal (N2) lymph nodes: mediastinoscopy and
Too many patients in North America receive induction EBUS.

Thoracic Cancer 3 (2012) 131–138 © 2011 Tianjin Lung Cancer Institute and Blackwell Publishing Asia Pty. Ltd 131
NSCLC Staging: EBUS vs. mediastinoscopy B. Nasir et al.

Figure 1 This figure depicts the N2 lymph nodes stations and which ones are accessibly by which staging modality.

132 Thoracic Cancer 3 (2012) 131–138 © 2011 Tianjin Lung Cancer Institute and Blackwell Publishing Asia Pty. Ltd
B. Nasir et al. NSCLC Staging: EBUS vs. mediastinoscopy

Table 1 Indication for mediastinoscopy and/or endobronchial ultra- copy. Classic cervical mediastinoscopy can be used to assess
sound (EBUS) the upper paratracheal (2R and 2L), lower paratracheal (4R
1) Tumor is central and 4L) and superior portion of the subcarinal (7) lymph
2) Tumor is greater than 4 cm node stations. The lower cervical (1R and 1L) and hilar (10R
3) Integrated PET/CT and/or CT scan suggest the presence of hilar (N1) and 10L) lymph node stations are occasionally obtainable as
disease
well.
4) Tumor has a maxSUV of greater than 10
5) The ratio of the maxSUV of the mediastinal lymph node to the
primary tumor is greater than 0.5 Extended mediastinoscopy
6) Patient has lung nodules bilaterally
7) Pneumonectomy is required There are several different types of mediastinoscopy and it is
CT, computed tomography; PET, positron emission tomography;
important that the terms are carefully defined when perform-
maxSUV, maximum standardized uptake value. ing a comparative analysis. One such modification first
described by Ginsberg in 1996 is called extended mediasti-
noscopy.13 It affords the surgeon the ability to biopsy lymph
nodes stations (#5 aorta-pulmonary and #6 para-aortic) to be
Radiologic staging
sampled.14 However since it was first described few surgeons
In our practice, patients who have non-small cell lung cancer have adopted it. Our preference has been to use thoracoscopy
or a lung nodule that is suspicious for cancer undergo both an for level 5 and 6 lymph nodes if that is the only site of medias-
integrated PET/CT test and a CT scan. The CT scan is per- tinal disease, and now, lately, a robotic approach.15
formed with intravenous contrast, and includes 5 mm colli- More recently, transcervical extended mediastinal lym-
mated cuts from the neck down to the mid-abdomen so as to phadenectomy (TEMLA)16 allows the mediastinoscope to be
image the liver and adrenal gland. Suspicious lymph nodes placed in the posterior and inferior mediastinum and biop-
include those that are greater than 1 cm in length in the short- sies can be obtained from lymph node stations 8 and even 9.
axis measurement. Integrated PET/CT is used routinely and However, this too has not been well embraced by most tho-
we have written extensively on the definition of what consti- racic surgeons, mainly because EUS, which safely allows for
tutes a suspicious N2 lymph node on integrated PET/CT.11 minimally invasive biopsy of these posterior inferior lymph
MRI of the brain and/or bone scans are used selectively to nodes stations, is increasing in availability. Although a few
further evaluate sites suspicious for metastatic disease. Once centers have shown outstanding results, it is not commonly
the presence of metastatic disease is eliminated after clinical practiced in the United States.
staging, then biopsies of N2 lymph nodes is warranted in Recently, video mediastinoscopy has been introduced and
selected patients as shown in Table 1. The most commonly has been quickly adopted by many surgeons throughout the
modalities used are: cervical mediastinoscopy, esophageal world. Recent reports have shown its superiority over stan-
ultrasound with fine needle aspiration (EUS-FNA), EBUS, dard mediastinoscopy.17 Although outcome data is still
and navigational bronchoscopy. lacking it offers some obvious and immediately noticeable
advantages over standard mediastinoscopy in our opinion.
These include better visualization of several structures
Mediastinoscopy
(azygous vein, the pulmonary artery, the left recurrent
Cervical mediastinoscopy is an operation that was first laryngeal nerve) making the procedure safer. In addition,
described in 1959 by Carlens from Sweden. Pearson further this enhanced view of the operative field affords bigger,
popularized it in the early 1960’s. Approximately 10 000 better and safer biopsies of lymph nodes. Finally, as it is a
mediastinoscopy procedures are performed annually in the video procedure, the entire operation is shown on a
United States.12 It is performed through a small 4 cm collar monitor. This enhances teaching, engages the entire opera-
incision in the neck approximately one to two fingerbreadths tive and anesthetic team’s involvement and it can be used as
above the sternal notch. Dissection is carried further down to documentation of a medical record for medical-legal
the level of the strap muscles. The sternohyoid and sternothy- reasons. All future comparisons to EBUS should be made
roid muscles are separated in the midline exposing the using the most up to date EBUS technology and video-
trachea with the overlying pretracheal fascia. The fascia is mediastinoscopy available.
incised and elevated. A pretracheal plane is developed bluntly A series by Cho et al. (2011) showed that the complication
with the surgeon’s finger and the finger is placed in a blood- rate was lower in the video mediastinoscopy group (3.6% in
less plane under the innominate artery. The mediastinoscope the conventional group vs. 1.6% in the video-assisted group,
is placed through this space and several different stations of P = 0.03).17 They also demonstrated a small, but statistically
lymph nodes are identified and biopsied. Figure 1 depicts the significant, increase in the number of lymph nodes examined
stations that are reliably seen during standard mediastinos- and sampled in the video mediastinoscopy group.

Thoracic Cancer 3 (2012) 131–138 © 2011 Tianjin Lung Cancer Institute and Blackwell Publishing Asia Pty. Ltd 133
NSCLC Staging: EBUS vs. mediastinoscopy B. Nasir et al.

Table 2 List of studies that report efficacy of standard mediastinoscopy

Negative
Study Number Sensitivity predictive value Mortality Morbidity Notes

Studies including clinical stage I-III


Lemaire et al. 200618 1459 86 94.5 0.05 1.07
Hammoud et al. 199925 1369 85.2 92 0.2 0.6
Coughlin et al. 198526 1259 92 97 0 0.002
Luke et al. 198627 1000 85 91 0 2.3
De Leyn et al. 199628 500 76 87 – –
Ebner et al. 199929 224 87 87 – – 7% after neoadjuvant therapy
Lardinois et al. 200330 187 87 92 0 3.7
Jolly et al. 199131 136 91 91 – –
Ratto et al. 199032 123 88 94 – –
Gdeedo et al. 199733 100 89 96 – –
Total 6357 86.3 92.9
Studies including clinical stage II-III
Dillemans et al. 199434 331 72 84 – – 8% underwent anterior mediastinotomy
Venissac et al. 200335 174 97.3 98.7 0 0.83
Yasufuku et al. 201136 153 79 90 0 2.6
Cerfolio et al. 201019 146 88 93 – –
Kimura et al. 200337 125 84.4 91.9 – –
Annema et al. 201024 118 79 86 0 7 Randomized trial mediastinoscopy vs. EBUS
Total 1047 81.7 89.7
Studies including clinical stage I
Choi et al. 200338 291 44 91.8 – –
Total 7695 84.1 92.4

EBUS, endobronchial ultrasound.

studies with a more selective approach, in which only clinical


Efficacy of mediastinoscopy
stages II and III underwent mediastinoscopy, a sensitivity of
All studies on any modality that report efficacy have to be 82% and a false negative rate of 13% were demonstrated. This
taken in proper context. The efficacy of any test is directly shows that the accuracy of mediastinoscopy is favorable inde-
related to the incidence of the disease in the population pendent of clinical stage. In a publication from our institu-
studied and the experience of the operator. This concept tion, we analyzed the accuracy of mediastinoscopy by lymph
cannot be overstated when considering mediastinoscopy and node station.19 For lymph node stations 2, 4 and 7, the sensi-
EBUS. tivity of mediastinoscopy was 87%, 89% and 87% respec-
There have been multiple studies documenting the accu- tively and the negative predictive value was 98%, 94% and
racy of mediastinoscopy in assessing mediastinal lymph 98% respectively. Our false negative rate was 6%. This shows
nodes and these are summarized in Table 2. Thus the sensitiv- that mediastinoscopy functions well independent of the
ity of mediastinoscopy ranges from 44% to 97.3% and the lymph node station assessed.
false negative rate ranges from 3% to 13%. The majority of
the false negative results in these studies were in lymph node
Morbidity and mortality of mediastinoscopy
stations not assessed by mediastinoscopy. When taking into
account false results in the paratracheal (4R, 4L) and subcari- The average morbidity and mortality for cervical media-
nal (7) stations, the rate of false negatives drops by half.18 One stinoscopy are 2% to 3% and 0.3% to 0.08% respectively.
limitation shared amongst all these studies is that there are Hemorrhage is the most feared complication during
few, if any, false positives. This is because if EBUS or medias- mediastinoscopy due to the vascular structures at risk.
tinoscopy is deemed positive by pathology or cytology, most Reported rates of hemorrhage vary due to variability in defi-
patients are precluded from undergoing thoracotomy, thora- nition (eg defined as bleeding greater than 500 mL, bleeding
coscopic, or robotic resection with thoracic lymph node sam- requiring blood transfusion or bleeding requiring explora-
pling. Thus, it is not possible to determine specificity. tion). One of the larger series to evaluate the safety of medias-
Table 2 shows a compilation of studies that employed tinoscopy comes from Duke University.8 The most common
mediastinoscopy for clinical stages I to III. The cumulative complications from their series included vocal cord dysfunc-
sensitivity was 83% and the false negative rate was 10%. In tion (0.55%), hemorrhage (0.32%), pneumothorax (0.09%)

134 Thoracic Cancer 3 (2012) 131–138 © 2011 Tianjin Lung Cancer Institute and Blackwell Publishing Asia Pty. Ltd
B. Nasir et al. NSCLC Staging: EBUS vs. mediastinoscopy

Table 3 List of studies that report efficacy of standard endobronchial ultrasound (EBUS) with fine needle aspiration of N2 lymph nodes

Negative
Study Number Sensitivity predictive value Mortality Morbidity Notes

Studies including clinical stage II-III


Herth et al. 200622 502 86 11 – –
Yasufuku et al. 201136 153 81 91 – –
Annema at al. 201024 123 94 93 0 6 Randomized trial mediastinoscopy vs. EBUS
Rintoul et al. 200939 109 91 60 0 0
Yasufuku et al. 200523 108 94.6 89.5
Wallace et al. 200840 97 69 88 Sensitivity 93% and NPV 97% when combined
with EUS
Cerfolio et al. 201019 72 57 79 0 0
Yasufuku et al. 200441 70 95 90 – –
Vilmann et al. 200542 31 85 72 – – Accuracy 100% when combined with EUS
Total 1265 84.9 55.2
Studies including clinical stage I-III
Szlubowski et al. 200943 226 89 83.5 0 0
Studies including clinical stage I
Herth et al. 200844 100 89 98.9 – –
Total 1591 85.7 62.0

EBUS, endobronchial ultrasound; EUS, esophageal ultrasound; NPV, negative predictive value.

and one death (0.05%). In the Duke series, seven patients suf- cytologist at the time to communicate with the endosonogra-
fered a vascular injury and required operative intervention pher as to the presence of atypical cells or normal lymphoid
via sternotomy, thoracotomy or a cervical approach. The tissue and thus can help steer more biopsies in a certain
injured vessels in this series were the azygos vein in three station. This is a critical aspect of EBUS and directly affects
patients, pulmonary artery in two patients, and superior vena the efficacy.
cava and innominate artery in one patient each. The death EBUS can be used to assess the upper paratracheal (2R and
occurred in a patient with a pulmonary artery injury. Another 2L), retrotracheal (3p), lower paratracheal (4R and 4L), sub-
larger series by Park from Memorial Sloan Kettering Cancer carinal (7), and hilar (10R and 10L) lymph node stations. In
Center in 2003 showed a 0.4% rate of major hemorrhage in a experienced hands, prevascular (3a) and subaortic (5) lymph
12-year period of 3391 mediastinoscopy procedures.20 We nodes can be sampled as well. Like mediastinoscopy, EBUS
have performed 1695 mediastinoscopy procedures over the does not assess the posterior mediastinal lymph nodes reli-
past 13 years and have had no mortality and only one patient ably. These include the paraesophageal (8) and inferior pul-
(<1%) required further operative intervention for bleeding monary ligament (9) lymph node stations.
(transfusion was not required).

Efficacy of EBUS
Endobronchial ultrasound
The efficacy of EBUS has been summarized in Table 3; the
Hurter first introduced EBUS in 1992.21 Since then it has also combined sensitivity of EBUS with TBNA is approximately
undergone refinement and development. It has been quickly 85%, but it ranges from 57% to 95% depending on the series.
adopted by many centers. EBUS can be performed under Even more variable is the negative predictive value, which
general anesthesia with endotracheal intubation, but most averaged 62%, but ranged from 11% to 98.9%. This variabil-
centers perform this with conscious sedation without any ity in test performance is due to a number of factors: the inci-
purported compromise in accuracy.22,23 The procedure and dence of the disease in the population, the operators’
type of equipment used have previously been described.19 experience, as well as the pathologists’ experience. As can be
Briefly, the procedure is performed using a flexible broncho- seen, centers with high experience with EBUS consistently
scope equipped with a linear ultrasound. The bronchoscope report accuracy greater than 90%. This is in contrast to medi-
includes a working port through which a 22-gauge biopsy astinoscopy, which has been performed for many years and
needle can be inserted and real-time ultrasound-guided most centers have a large experience with the procedure, with
transbronchial fine needle aspiration can be performed. satisfactory results in all the series examined. One series by
Rapid on site evaluation (ROSE) is used by many centers but Herth in 2006 documented an extremely high false negative
not by all. It affords increased efficacy because it allows the rate of 89%.22 This has been explained by a very high preva-

Thoracic Cancer 3 (2012) 131–138 © 2011 Tianjin Lung Cancer Institute and Blackwell Publishing Asia Pty. Ltd 135
NSCLC Staging: EBUS vs. mediastinoscopy B. Nasir et al.

Table 4 Comparison of mediastinoscopy and endobronchial ultrasound (EBUS)

Mediastinoscopy EBUS

N2 lymph node 1, 2R, 2L, 4R, 4L, superior aspect of 7 2R, 2L, 3p, 4R, 4L, 7,
stations accessible
Advantages Affords larger amount of tissue for genetic and proteomic No incisions needed
analysis
Better at diagnosis of some conditions (e.g. non-Hodgkin’s Can be done via intravenous sedation
lymphoma, sarcoid)
Faster than EBUS, checks multiple N2 stations easier and Very low morbidity
quicker
Uses pathology not just cytology Can be repeated in patients both before and after induction
chemotherapy and/or radiotherapy
Helps dissect out vessels for subsequent lobectomy Can be done after a mediastinoscopy
Lower false negative rate than EBUS Can be performed in patients with permanent tracheostomy
Excellent initial test for N2
Useful for patients who are too ill for mediastinoscopy and prior to
undergoing stereotactic radiosurgery for lung cancer to stage
their mediastinum
Disadvantages Costs more money Usually only provides cytological analysis
Requires general anesthesia Often ROSE is not available at all hospital at all times
Difficult to repeat Provides only small quantity of tissue
Risk of serious bleeding High false negative rate
Difficult to teach standard mediastinoscopy (video Highly user dependent (more so then mediastinoscopy)
mediastinoscopy may be easier)

EBUS, endobronchial ultrasound; ROSE, rapid on site evaluation.

lence of N2 disease, which makes their false negative rate Therefore, it is difficult to attribute a complication rate to
unreliable due to mathematical reasons. If this study is EBUS based on this data. Nonetheless, the complications
excluded, the pooled false negative rate is approximately 25%. were minor and included: hoarseness in four patients, a pneu-
We reported our initial experience with EBUS at our insti- mothorax and mediastinitis in one patient each. The last
tution at The University of Alabama at Birmingham. We patient also underwent a mediastinoscopy and presented
found the efficacy of EBUS was dependent on the lymph node with fever and chills within 24 hours of mediastinoscopy. The
station assessed.19 The overall patient sensitivity for N2 patient was treated with antibiotics.
disease for EBUS was 57%, the overall patient negative pre-
dictive value (NPV) was 79%, and the overall patient accu-
racy was 83%. The most common location for a false negative
Discussion
was the 4R lymph node station. The sensitivity of EBUS was Too many physicians view EBUS and mediastinoscopy as
62% for level 4 lymph nodes, 38% for level 5 lymph nodes and competing procedures. However we believe they are best
64% for level 7 lymph nodes. The NPV were 76% for level 4 viewed as complementary staging modalities. Each patient
lymph nodes, 82% for level 5 lymph nodes, and 88% for level presents a unique situation. The physician must choose
7 lymph nodes. An interesting finding in the study was that which procedure is best. Although there are obvious institu-
there was still a significant false negative rate when the lymph tional biases, the truth is most academic and large private
node examined was greater than 2 cm, but the false negative practice centers in North America have both procedures
rate was zero when the ratio of maxSUV of N2 lymph node to available. Table 4 outlines some of the distinct advantages and
the primary tumor was greater than 1. disadvantages to both mediastinoscopy and EBUS.
EBUS has not, and will not in the near future, replace medi-
astinoscopy. However, as physicians receive training for EBUS
Morbidity and mortality for EBUS
earlier in their career, as endoscopes get smaller, ultrasound
Few studies have reported the morbidity and mortality attrib- guided needles become more accurate and as smaller
uted to EBUS. There have been no reports of any mortality amounts of tissue are required to perform genetic and
associated with this procedure. Furthermore, the complica- molecular testing, EBUS may one day supplant mediastinos-
tion rate is extremely low in series that do report morbidity. copy. However, false negative rates must fall significantly and
One series reported a morbidity of 6%, but all patients with a consistently amongst many centers before EBUS makes medi-
negative result by EBUS underwent a mediastinoscopy.24 astinoscopy a historical note.

136 Thoracic Cancer 3 (2012) 131–138 © 2011 Tianjin Lung Cancer Institute and Blackwell Publishing Asia Pty. Ltd
B. Nasir et al. NSCLC Staging: EBUS vs. mediastinoscopy

A common clinical scenario illustrates the complementary 8 Detterbeck FC, DeCamp MM Jr, Kohman LJ, Silvestri GA.
nature of these two tests. A young patient with a resectable Invasive staging: the guidelines. Chest 2003; 123 (Suppl.):
right upper lobe mass with an obvious metastatic lymph node 167S–175S.
in the 4R station can be considered. EBUS should be chosen as 9 Schipper P, Schoolfield M. Minimally invasive staging of N2
the initial staging test and all stations should be biopsied. disease: endobronchial ultrasound/ transesophageal
Genetic testing should be performed on the nodal tissue or endoscopic ultrasound, mediastinoscopy and thoracoscopy.
the mass itself to guide adjuvant therapy. The presence of N3 Thorac Surg Clin 2008; 18: 363–79.
disease must be ruled out by EBUS. After the completion of 10 Rusch VW, Asamura H, Watanabe H, Giroux DJ, Rami-Porta
R, Goldstraw P. The IASLC Lung Cancer Staging Project; A
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proposal for a new international lymph node map in the
ensure that the N2 disease has been downstaged, and resec-
forthcoming seventh edition of the TNM classification for
tion can be performed.
lung cancer. J Thorac Oncol 2009; 4: 568–77.
11 Cerfolio RJ, Bryant AS. Ratio of the maximum standardized
Conclusion uptake value on FDG-PET of the mediastinal (N2) lymph
nodes to the primary tumor mat be a universal predictor of
EBUS and mediastinoscopy are complementary staging pro- nodal malignancy in patients with nonsmall-cell lung cancer.
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