CHEST Original Research

INTERVENTIONAL PULMONOLOGY

The Utility of Sonographic Features

During Endobronchial Ultrasound-Guided
Transbronchial Needle Aspiration for Lymph
Node Staging in Patients With Lung Cancer
A Standard Endobronchial Ultrasound
Image Classification System
Taiki Fujiwara, MD; Kazuhiro Yasufuku, MD, PhD, FCCP; Takahiro Nakajima, MD, PhD;
Masako Chiyo, MD, PhD; Shigetoshi Yoshida, MD, PhD; Makoto Suzuki, MD, PhD;
Kiyoshi Shibuya, MD, PhD; Kenzo Hiroshima, MD, PhD; Yukio Nakatani, MD, PhD;
and Ichiro Yoshino, MD, PhD

Background: Endobronchial ultrasound-guided transbronchial needle aspiration (EBUS-TBNA)

is a minimally invasive procedure with a high yield for lymph node staging of lung cancer. The
aim of this study was to assess the utility of sonographic features of lymph nodes during EBUS-
TBNA for the prediction of metastasis in patients with lung cancer and to establish a standard
endobronchial ultrasound (EBUS) image classification system.
Methods: Digital images of lymph nodes obtained during EBUS-TBNA in patients with lung can-
cer were categorized according to the following characteristics: (1) size (short axis) less or more
than 1 cm, (2) shape (oval or round), (3) margin (indistinct or distinct), (4) echogenicity (homoge-
neous or heterogeneous), (5) presence or absence of central hilar structure, and (6) presence or
absence of coagulation necrosis sign. The sonographic findings were compared with the final
pathologic results.
Results: A total of 1,061 lymph nodes were retrospectively evaluated in 487 patients. The accu-
racy of predicting metastatic property for each category was as high as 63.8% to 86.0%. A multi-
variate analysis revealed that round shape, distinct margin, heterogeneous echogenicity, and
presence of coagulation necrosis sign were independent predictive factors for metastasis. Two
hundred eighty-five of the 664 lymph nodes (42.9%) having at least one metastatic feature of the
four categories were pathologically proven metastatic, and 96.0% of lymph nodes (381/397) were
proven not metastatic when all four categories were determined as benign.
Conclusions: Sonographic features of lymph nodes based on the new EBUS imaging classification
may be helpful in the prediction of metastatic lymph nodes during EBUS-TBNA.
CHEST 2010; 138(3):641–647

Abbreviations: CHS 5 central hilar structure; CP-EBUS 5 convex probe-endobronchial ultrasound CP-EBUS;
EBUS 5 endobronchial ultrasound; EBUS-TBNA 5 endobronchial ultrasound-guided transbronchial needle aspiration;
EUS 5 endoscopic ultrasound; TBNA 5 transbronchial needle aspiration

Lung cancer is the most common cause of cancer-

related death in the Western world. The outcome
1
of the disease depends on staging and therefore proper
staging must be performed to determine the treatment
plan.2 Endobronchial ultrasound-guided transbron-
chial needle aspiration (EBUS-TBNA) is a minimally
invasive procedure performed under local anesthesia
that has been shown to have a high sensitivity and
diagnostic yield for lymph node staging of lung
cancer.2-7 EBUS-TBNA allows cytologic and histologic
examination of mediastinal and hilar lymph nodes.8
It is performed with the convex probe-endobronchial
ultrasound (CP-EBUS), which has a 7.5-MHz ultra-
sound probe on the tip of a bronchovideoscope. The
CP-EBUS is capable of detecting lymph nodes as
small as 2 mm, which are sometimes not visible on

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 CT imaging. Lymph nodes as small as 3 mm in the
short axis can be punctured under real-time ultrasound
guidance. Well-trained bronchoscopists encounter
mediastinal and hilar lymph nodes of various sizes
and features.
It has been reported that sonographic features are
useful imaging tools in the evaluation of cervical lymph
node metastasis in head and neck cancers, breast can-
cers, and thoracic malignancies.9,10 Furthermore, sono-
graphic features during endoscopic ultrasound (EUS)
have been shown to be useful for the prediction of
malignant lymph nodes in the mediastinum and the
hilum.11,12 To date, there are no reports on the classifi-
cation of sonographic features during EBUS-TBNA
and the usefulness of these features in the prediction
of metastasis in mediastinal and hilar lymph nodes.
The aim of this study was to assess the utility of the
morphologic features of lymph nodes obtained by
endobronchial ultrasound (EBUS) for the prediction
of presence or absence of metastasis in mediastinal
and/or hilar lymph nodes in patients with lung cancer.
Materials and Methods
Patients
A retrospective chart review was performed in patients who
underwent EBUS-TBNA for mediastinal staging of lung cancer at
the Department of Thoracic Surgery, Chiba University Hospital,
from January 2003 to August 2007. EBUS-TBNA was performed
in patients with lung cancer or suspected lung cancer without pre-
vious treatment, with radiologically defined mediastinal and/or
hilar lymph nodes with a short axis of ⱖ 5 mm on enhanced
CT imaging or positive on PET scan (defined as standardized
uptake value . 2.5). Chest CT imaging was performed with a
single-injection contrast on a multidetector-row CT scan. Lymph
node stations and numbers were determined according to the
international TNM staging system reported by Mountain and
Dresler.13
EBUS-TBNA
EBUS-TBNA was performed on an outpatient basis in patients
under conscious sedation (midazolam) with local anesthesia. The
Manuscript received August 24, 2009; revision accepted March 20,
2010.
Affiliations: From the Department of Thoracic Surgery
(Drs Fujiwara, Yasufuku, Nakajima, Chiyo, Yoshida, Suzuki, Shibuya,
and Yoshino) and Diagnostic Pathology (Drs Hiroshima and
Nakatani), Graduate School of Medicine, Chiba University, Chiba,
Japan; and the Division of Thoracic Surgery (Dr Yasufuku),
Toronto General Hospital, University Health Network, Toronto,
ON, Canada.
Corresponding author: Kazuhiro Yasufuku, MD, PhD, Division
of Thoracic Surgery, Toronto General Hospital, University Health
Network, 200 Elizabeth S, 9N-957, Toronto, ON, M5G2C4,
Canada; e-mail: kazuhiro.yasufuku@uhn.on.ca
© 2010 American College of Chest Physicians. Reproduction
of this article is prohibited without written permission from the
American College of Chest Physicians (http://www.chestpubs.org/
site/misc/reprints.xhtml).
DOI: 10.1378/chest.09-2006
642
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CP-EBUS (BF-UC260F-OL8; Olympus; Tokyo, Japan) was used
for the examination of the mediastinal and hilar lymph nodes. The
CP-EBUS is integrated with a convex transducer (7.5 MHz) that
scans parallel to the insertion direction of the bronchoscope. Images
can be obtained by contacting the probe directly or by attaching
a balloon to the tip. The ultrasound features are processed in
a dedicated ultrasound scanner (EU-C2000/EU-C60; Olympus).
A dedicated 22-gauge needle was used to perform transbronchial
needle aspiration (TBNA) (NA-201SX-4022; Olympus) for lymph
node sampling. The needle is equipped with an internal stylet that
is withdrawn after passing through the bronchial wall and can be
visualized through the optic device and on the ultrasound fea-
tures. After the initial puncture, the internal stylet is used to clean
out the internal lumen, which becomes clogged with bronchial
membrane. The internal stylet is then removed and negative pres-
sure is applied with a syringe. After the needle is moved back and
forth inside the lymph node, the needle is retrieved and the inter-
nal sheath is used once again to push out the histologic core.3-5
With this method, histologic cores, as well as cytologic specimens,
can be obtained.
The aspirated material was smeared onto glass slides, air dried,
and immediately stained with Diff-Quik (Sysmex Corporation;
Kobe, Japan) for immediate interpretation by an on-site cyto-
pathologist to confirm adequate cell material. Furthermore,
Papanicolaou and Giemsa staining and light microscopy were
performed by an independent cytopathologist who was blinded
to the details of the EBUS image characteristics. Histologic
cores were fixed with formalin and stained with hematoxylin and
eosin. Immunohistochemistry was also performed in some patients.
In patients with malignant lymph nodes, the determination was
based on malignant cytologic and/or histologic results at EBUS-
TBNA or surgical-pathologic confirmation. In patients with benign
lymph nodes, this determination was based on surgical-pathologic
confirmation of EBUS-TBNA-targeted nodes by lymph node dis-
section of the lymph node station of interest, or on results of clinical
follow-up for at least 6 months demonstrating a lack of clinical or
radiologic disease progression. We determined the lymph node
location based on the standard lymph node map reported in 1997
by Mountain and Dresler.13 The lymph nodes were systematically
visualized, starting with N1 lymph nodes, followed by N2 nodes,
and finally N3 nodes. EBUS-TBNA was then performed first from
N3 nodes, followed by N2 nodes, and, if necessary, N1 nodes. If
N3 nodes were found to be positive for malignancy on rapid
on-site cytologic evaluation, we terminated the procedure. All
EBUS-TBNA were performed by three individuals (T. F., T. N.,
K. Y.) or under their supervision.
EBUS Image Characteristics of Lymph Nodes
JPEG images and digital video images of all the lymph nodes
obtained by CP-EBUS were reviewed by three different individuals
(T. F., T. N., K. Y.) blinded to the results of EBUS-TBNA. We
avoided the use of special imaging software, which may have
affected the evaluation of image characteristics. The lymph nodes
were characterized based on EBUS images as follows (Fig 1):
(1) short-axis size less or more than 1 cm, (2) shape (oval or round),
(3) margin (indistinct or distinct), (4) echogenicity (homogeneous
or heterogeneous), (5) presence or absence of central hilar struc-
ture (CHS), and (6) presence or absence of coagulation necrosis
sign. We measured both the long and the short axis of all lymph
nodes. When the ratio of the short to long axis of lymph nodes was
, 1.5, we defined the lymph nodes as round. On the other hand,
if the ratio was . 1.5, we defined it as oval. The short and long
axes were measured as a distance of two perpendicular directions
for triangular-shaped lymph nodes. When we observed lymph
nodes by CP-EBUS, there existed echogenic differences between
the lymph node and the surrounding connective tissue structure.
Original Research
 Figure 1. Different endobronchial ultrasound (EBUS) image characteristics used for the classification
of lymph nodes. Size; less or more than 1 cm; shape: oval or round; margin: indistinct or distinct; echo-
genicity: homogeneous or heterogeneous; central hilar structure (CHS): present or absent; coagulation
necrosis sign: present or absent.

If the majority of the margin (. 50%) was clearly visualized with
a high echoic border, we determined the lymph nodes to be dis-
tinct, and if the margin was unclear, we determined them to be
indistinct. CHS seen in cervical lymph nodes9 is defined as a linear,
flat, hyperechoic area in the center of the lymph node. The coagu-
lation necrosis sign is a hypoechoic area within the lymph node
without blood flow. It is also seen in cervical lymph node features
and in mediastinal lymph node features during EUS.9,14 We
defined the intralymphatic lesion, which showed low echoic area
with absence of blood flow on Doppler. This sign often correlates
with an existence of necrosis within the lymph node. Typical coag-
ulation necrosis signs are found as one low echoic area within the
lymph node and they sometimes occupy the majority of the lymph
node. Multiple low echoic spots within the lymph node were
categorized in some cases as heterogeneous echo features instead
of coagulation necrosis signs. The final characteristics of the sono-
graphic findings for each lymph node were based on an agree-
ment of at least two reviewers.
Data Analysis
All six sonographic characteristics of the lymph nodes were
compared with the final pathologic result of the lymph node. The
sensitivity, specificity, positive predictive value, negative predictive
value, and diagnostic accuracy rate were calculated by standard
definitions. We used StatView for Windows, version 5 (SAS Institute;
Cary, NC) for statistics analysis. This study was a retrospective
chart review and therefore the institutional review board of Chiba
University approved the study without the need to obtain informed
consent.
Results
Patients
The characteristics of the 487 patients who were
enrolled and evaluated in this study are summarized
in Table 1. There were 372 men and 115 women, and
the average age was 68.0 years. The histologic types
of lung cancers were adenocarcinoma in 244,
squamous cell carcinoma in 144, small cell carcinoma
in 32, large cell carcinoma in 19, and other cancers in
48. A total of 1,061 lymph nodes were analyzed, and
the proportion of each station is summarized in
Table 2. Radiologically suspected nodes were fre-
quently observed in the station 4R and station
7 lymph nodes (623 in number and 59% in proportion)
Table 2—Lymph Node Stations Included in the Study

Table 1—Patient Characteristics Lymph Node Station No.

All 1,061
Patient Characteristics No.
2R 41
Patients 487 2L 19
Male (female) sex 372 (115) 4R 335
Age, y, mean (range) 68.0 (28-87) 4L 86
Histology 7 288
Adenocarcinoma 244 10 44
Squamous cell carcinoma 144 11L 75
Large cell carcinoma 19 11R 166
Small cell carcinoma 32 12 5
Other 48 13 1

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 and were subjected to the analysis. No patients had
any complications related to EBUS-TBNA.

Morphologic Findings of EBUS

Representative morphologic findings of EBUS are
shown in Figure 2. The size of evaluated lymph nodes
ranged from 2 mm to 33.4 mm, and the number of
nodes with a short axis , 1 cm and that of nodes with
a short axis of . 1 cm were 642 (60.5%) and 419
(39.5%), respectively. For shape, 612 (57.7%) lymph
nodes were characterized as oval and 449 (42.3%) as
round. For margin, 430 (40.5%) nodes exhibited
indistinct margins and 631 (59.5%) had distinct margins.
For echogenicity, 726 (68.4%) nodes were character-
ized as homogeneous and 335 (31.6%) nodes as het-
erogeneous. CHS was observed in 334 (31.5%) nodes
and the presence of the coagulation necrosis sign
in 265 (25.0%) nodes. The presence or absence of
metastasis based on each feature is shown in Figure 3.
When lymph nodes had the following features: short
axis of more than 1 cm, round shape, distinct margin,
heterogeneous echogenicity, absence of CHS, or
presence of coagulation necrosis sign, they tended to
suggest metastatic lymph nodes. Diagnostic yields for
each feature are summarized in Table 3. The accuracy
of predicting metastatic property was 76.4% for size,
79.3% for shape, 65.7% for margin, 89.9% for echo-
genicity, 63.8% for CHS, and 86.0% for coagulation
necrosis sign. In all the morphologic categories, nega-
tive predictive values were higher (88.4% to 96.0%)
in comparison with corresponding positive predictive
values (43.3% to 78.9%). Logistic regression analysis
revealed that shape, margin, echogenicity, and coag-
ulation necrosis sign were independent predictive
factors, with respective hazard ratios of 3.1, 3.1, 2.0,
and 5.6 (Table 4). Two hundred eighty-five of the 664
lymph nodes (42.9%) having a metastatic feature in at
Figure 2. Representative morphologic findings of EBUS charac-
least one of the four categories were pathologically teristics. Size ⱕ 1 cm (A) or more than 1 cm (B); shape: oval (C) or
proven metastatic, and 96.0% of lymph nodes round ( D); margin: indistinct (E ) or distinct (F); echogenicity:
(381/397) were pathologically proven not metastatic homogeneous (G) or heterogeneous (H); central hilar structure:
present or absent (I); coagulation necrosis sign: present or absent
when all four categories were determined as not (J). See Figure 1 legend for expansion of the abbreviation.
metastatic.

Discussion ultrasound guidance.2-7 Although we use preopera-

Since our first successful EBUS-TBNA in 2002, we
have performed . 1,000 EBUS-TBNA procedures
without any complications at our department. For
mediastinal staging in lung cancer, all the mediastinal
lymph nodes and hilar lymph nodes accessible by
CP-EBUS are visualized in a systematic way and eval-
uated. As reported previously, CP-EBUS is capable of
detecting even small-sized lymph nodes not visible
on CT imaging and lymph nodes as small as 3 mm
in the short axis can be punctured under real-time
tive imaging by CT scan and/or PET scan as a reference
prior to EBUS-TBNA, we do inspect all lymph nodes
based on the site of the primary tumor and on the
lobar lymphatic drainage pattern. There are often
important lymph nodes that need to be sampled even
when preoperative imaging by CT scan and/or PET
scan is negative for malignancy. During the process,
we have realized that there are some EBUS sono-
graphic features that are suggestive of benign lymph
nodes. The aim of the current study was to classify
the different sonographic features of mediastinal

644 Original Research

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 Figure 3. The actual results of comparison between EBUS image classification and final pathology.
When lymph nodes had small sizes, round shapes, indistinct margins, homogeneous echogenicities, and
the presence of CHS, they tended to be benign. On the other hand, when lymph nodes had the presence
of CNS, they tended to be malignant. CHS 5 central hilar structure; CNS 5 coagulation necrosis sign.
See Figure 1 for expansion of other abbreviation.

lymph nodes and to apply this EBUS image classifica-
tion to the prediction of lymph node metastasis. Our
results show that sonographic EBUS features of lymph
nodes during EBUS-TBNA are helpful for the predic-
tion of benign lymph nodes in lung cancer patients.
Ahuja and Ying9 reported that sonography is a useful
imaging tool in the evaluation of cervical lymph nodes
in patients with malignancies of the head, neck, and
thorax. As for the evaluation of mediastinal and hilar
lymph nodes, EUS was first accepted as a diagnostic
modality in the 1990s.11,12 In both cervical ultrasonog-
raphy and EUS, the morphologic characters of lymph
nodes are analyzed, and size . 10 mm, round shape,
distinct margin, heterogeneous echogenicity, absence
of central echogenic hilum, and coagulation necrosis
are considered signs of lymph node metastasis.9,11,12,14,15
From our experience, we defined six different mor-
phologic characteristics of mediastinal and hilar
lymph nodes during EBUS-TBNA in patients with
lung cancer, similar to the features examined in
cervix ultrasonography and EUS. Calcification was
not included as a significant echo feature in these
reports and because the incidence of calcification was
rare in our initial experience with EBUS, we did not
include it as a criterion. More than 1,000 lymph nodes
were investigated morphologically and pathologically
by three different individuals (T. F., T. N., K. Y.).
When multiple lymph nodes were detected in the
same lymph node station, we sampled the largest
lymph node by EBUS-TBNA, whereas the pathology
of the smaller lymph nodes within the same lymph
node station was confirmed by surgery. In this study,
we demonstrated the diagnostic accuracies for meta-
static property of the four independent predictive
characters of EBUS, including shape, margin, echo-
genicity, and the absence of central necrosis sign. The
diagnostic accuracy of predicting metastatic nodes
from our new classification system was very high.
If we can predict metastatic lymph nodes from
EBUS morphology, should we consider just looking

Table 3—Diagnostic Yield of Each Endobronchial Ultrasound Image Category for Metastatic Lymph Node

Positive Predictive Negative Predictive

Morphologic Category Sensitivity Specificity Value Value Diagnosis Accuracy

Size: . 10 mm 77.9 75.8 55.9 89.7 76.4

Shape: round 88.0 75.8 59.0 94.1 79.3
Margin: distinct 94.4 54.3 45.5 96.0 65.7
Echogenicity: heterogeneous 77.3 86.6 69.5 90.6 83.9
Central hilar structure: absence 89.7 53.5 43.3 92.9 63.8
Coagulation necrosis sign: presence 69.4 92.6 78.9 88.4 86.0

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 Table 4—Logistic Regression Analysis of Endobronchial Ultrasound Image Categories for Prediction
of Metastatic Lymph Nodes
Morphologic Category
Size (. 10 mm/, 10 mm)
Shape (round/oval)
Margin (distinct/indistinct)
Echogenicity (heterogeneous/homogeneous)
Central hilar structure (absence/presence)
Coagulation necrosis sign (presence/absence)
at the morphology without doing a biopsy if we find
such lymph nodes? The answer is no. Studies com-
paring EUS morphology to EUS-fine-needle aspiration
have shown that EUS-fine-needle aspiration is supe-
rior to imaging by EUS alone.16-18 We should always
try to get tissue diagnosis from suspicious lymph
nodes; thus, EBUS-TBNA should always be per-
formed on lymph nodes that are suspicious for metas-
tasis on EBUS images. On the other hand, one of the
potential benefits of this study is the negative predic-
tive value. If an operator performs EBUS-TBNA on
a lymph node in a patient with suspected lung cancer
and the cytologic specimen reveals only benign lym-
phocytes, then this is the instance in which the lack of
lymph node EBUS malignant features can be more
reassuring in confirming the true negativity of that
lymph node. This would also be useful during the
EBUS-TBNA procedure to avoid unnecessary passes
where rapid on-site cytology reveals only benign lym-
phocytes in lymph nodes with benign ultrasound
features. The purpose of this study was to highlight
the efficiency and highly precise examination of
EBUS-TBNA with the use of echo features. Further
prospective studies are recommended to confirm the
utility of sonographic features during EBUS-TBNA.
The limitation of our study is that we did not
include the sonographic features of noncancerous
adenopathy. Mediastinal lymphadenopathy can also
be observed in patients with noncancerous disease
such as sarcoidosis and TB, and autoimmune dis-
eases such as Sjogren syndrome and systemic lupus
erythmatosus.9,19 The echo features are quite differ-
ent from the metastatic findings detected in the pres-
ent study. There is definitely a role for evaluating the
lymph nodes of noncancerous lymphadenopathy.
However, we chose not to include this patient popu-
lation because the findings may have confused the
interpretation of lymph nodes in patients with lung
cancer.
Conclusions
In conclusion, by careful examination of the sono-
graphic features of lymph nodes during EBUS-TBNA,
we may speculate on the presence of metastatic lymph
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Hazard Ratio 95% CI P Value
1.34 0.882-2.03 .171
3.1 1.79-5.36 , .0001
3.05 1.61-5.75 .0006
1.96 1.12-3.40 .0176
1.34 0.793-2.25 .278
5.64 3.40-9.38 , .0001
nodes even in patients with lung cancer. The four sono-
graphically obtained morphologic features, including
round shape, distinct margin, heterogeneous echoge-
nicity, and presence of coagulation necrosis sign, are
independent predictive factors for nodal metastasis.
When at least one such feature is observed during the
EBUS procedure, subsequent needle aspiration must
be performed. Conversely, when all four categories are
sonographically determined not metastatic, we may be
able to avoid unnecessary biopsies in such lymph
nodes. Our findings and the EBUS image classification
system will need to be validated in a prospective study
before we can make clinical decisions based on imag-
ing alone during the procedure.
Acknowledgments
Author contributions: Dr Fujiwara: contributed to the evalua-
tion of the EBUS images, performance of the EBUS-TBNA, and
evaluation of the lymph nodes by surgery.
Dr Yasufuku: contributed to the evaluation of the EBUS images,
performance of the EBUS-TBNA, and evaluation of the lymph
nodes by surgery.
Dr Nakajima: contributed to the evaluation of the EBUS images,
performance of the EBUS-TBNA, and evaluation of the lymph
nodes by surgery.
Dr Chiyo: contributed to the performance of the EBUS-TBNA and
evaluation of the lymph nodes by surgery.
Dr Yoshida: contributed to the evaluation of the lymph nodes
by surgery.
Dr Suzuki: contributed to the evaluation of the lymph nodes
by surgery.
Dr Shibuya: contributed to the evaluation of the lymph nodes
by surgery.
Dr Hiroshima: contributed to the pathologic evaluation of the
lymph nodes.
Dr Nakatani: contributed to the pathologic evaluation of the
lymph nodes.
Dr Yoshino: contributed to the evaluation of the lymph nodes by sur-
gery.
Financial/nonfinancial disclosures: The authors have reported
to CHEST the following conflicts of interest: Dr Yasufuku has
received unrestricted grants from Olympus Medical Systems for
continuing medical education. Drs Fujiwara, Nakajima, Chiyo,
Yoshida, Suzuki, Shibuya, Hiroshima, Nakatani, and Yoshino have
reported that no potential conflicts of interest exist with any com-
panies/organizations whose products or services may be discussed
in this article.
References
1. Jemal A, Siegel R, Ward E, et al. Cancer statistics, 2003.
CA Cancer J Clin. 2003;53:5-26.
Original Research
 2. Yasufuku K, Fujisawa T. Staging and diagnosis of non-small
cell lung cancer: invasive modalities. Respirology. 2007;12(2):
173-183.
3. Yasufuku K, Chiyo M, Sekine Y, et al. Real-time endobron-
chial ultrasound-guided transbronchial needle aspiration
of mediastinal and hilar lymph nodes. Chest. 2004;126(1):
122-128.
4. Yasufuku K, Chiyo M, Koh E, et al. Endobronchial ultra-
sound guided transbronchial needle aspiration for staging of
lung cancer. Lung Cancer. 2005;50(3):347-354.
5. 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(3):710-718.
6. Herth FJ, Ernst A, Eberhardt R, Vilmann P, Dienemann H,
Krasnik M. Endobronchial ultrasound-guided transbronchial
needle aspiration of lymph nodes in the radiologically normal
mediastinum. Eur Respir J. 2006;28(5):910-914.
7. Vincent BD, El-Bayoumi E, Hoffman B, et al. Real-time
endobronchial ultrasound-guided transbronchial lymph node
aspiration. Ann Thorac Surg. 2008;85(1):224-230.
8. Nakajima T, Yasufuku K, Iyoda A, et al. The evaluation of
lymph node metastasis by endobronchial ultrasound-guided
transbronchial needle aspiration: crucial for selection of
surgical candidates with metastatic lung tumors. J Thorac
Cardiovasc Surg. 2007;134(6):1485-1490.
9. Ahuja AT, Ying M. Sonographic evaluation of cervical
lymph nodes. AJR Am J Roentgenol. 2005;184(5):1691-1699.
10. Kim TH, Kang DK, Kim SY, Lee EJ, Jung YS, Yim H. Sono-
graphic differentiation of benign and malignant papillary
lesions of the breast. J Ultrasound Med. 2008;27(1):75-82.
www.chestpubs.org
Downloaded From: http://journal.publications.chestnet.org/ by a Universidade of Sao Paulo User on 05/22/2015
11. Lee N, Inoue K, Yamamoto R, Kinoshita H. Patterns of
internal echoes in lymph nodes in the diagnosis of lung cancer
metastasis. World J Surg. 1992;16(5):986-994.
12. Bhutani MS, Hawes RH, Hoffman BJ. A comparison of the
accuracy of echo features during endoscopic ultrasound
(EUS) and EUS-guided fine-needle aspiration for diagnosis
of malignant lymph node invasion. Gastrointest Endosc.
1997;45(6):474-479.
13. Mountain CF, Dresler CM. Regional lymph node classifica-
tion for lung cancer staging. Chest. 1997;111(6):1718-1723.
14. Roberts SA, Mahon BS, Evans R. Coagulation necrosis in
malignant mediastinal nodes on endoscopic ultrasound: a new
endosonographic sign. Clin Radiol. 2005;60(5):587-591.
15. Catalano MF, Alcocer E, Chak A, et al. Evaluation of metastatic
celiac axis lymph nodes in patients with esophageal carcinoma:
accuracy of EUS. Gastrointest Endosc. 1999;50(3):352-356.
16. Chen VK, Eloubeidi MA. Endoscopic ultrasound-guided fine
needle aspiration is superior to lymph node echofeatures:
a prospective evaluation of mediastinal and peri-intestinal
lymphadenopathy. Am J Gastroenterol. 2004;99(4):628-633.
17. Schmulewitz N, Wildi SM, Varadarajulu S, et al. Accuracy
of EUS criteria and primary tumor site for identification of
mediastinal lymph node metastasis from non-small-cell lung
cancer. Gastrointest Endosc. 2004;59(2):205-212.
18. Kramer H, Sanders J, Post WJ, Groen HJ, Suurmeijer AJ.
Analysis of cytological specimens from mediastinal lesions
obtained by endoscopic ultrasound-guided fine-needle aspira-
tion. Cancer. 2006;108(4):206-211.
19. Ying M, Ahuja AT, Yuen HY. Grey-scale and power Doppler
sonography of unusual cervical lymphadenopathy. Ultrasound
Med Biol. 2004;30(4):449-454.
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