(Chest. 2002;122:1887-1894.)
© 2002
American College of Chest Physicians
Analysis of the Internal Structure of Peripheral Pulmonary Lesions Using Endobronchial Ultrasonography*
Noriaki Kurimoto, MD;
Masaki Murayama, MD;
Shinkichiro Yoshioka, MD and
Takashi Nishisaka, MD
* From the Department of Surgery (Dr. Kurimoto), National Hiroshima Hospital, Higashi-Hiroshima, Japan; the Department of Surgery (Dr. Murayama), Iwakuni Minami Hospital, Iwakuni, Japan; the Second Department of Surgery (Dr. Yoshioka), Hiroshima University School of Medicine, Hiroshima, Japan; and the Department of Pathology (Dr. Nishisaka), Hiroshima PrefecturalHospital, Hiroshima, Japan.
Correspondence to: Noriaki Kurimoto, MD, 513 Jike, Saijyoucyou, Higashi-Hiroshima City, Hiroshima Prefecture, 739-0041 Japan
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Abstract
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Study objective: To correlate the internal structure of peripheral pulmonary lesions, as visualized by endobronchial ultrasonography (EBUS), and the histology of the surgical specimen to develop a classification system for distinguishing benign from malignant lesions by EBUS.
Design: Retrospective review.
Setting: A national hospital.
Patients: One hundred twenty-four patients with peripheral pulmonary lesions who had undergone EBUS in whom a definitive histologic diagnosis was made. In 69 patients, EBUS findings were correlated with the histology of a surgical specimen.
Intervention: EBUS was performed by a miniature probe (20-MHz) introduced up to the lesion through a channel in a bronchoscope.
Results: Three classes and six subclasses of lesions were identified by EBUS based on the internal structure of the lesion, focusing on internal echoes, vascular and bronchial patency, and the morphology of the hyperechoic areas, reflecting air in the alveoli and bronchioles. The classes of lesions are as follows: type I, homogeneous pattern (type Ia, with patent vessels and patent bronchioles; type Ib, without vessels and bronchioles); type II, hyperechoic dots and linear arcs pattern (type IIa, without vessels; type IIb, with patent vessels); and type III, heterogeneous pattern (type IIIa, with hyperechoic dots and short lines; type IIIb, without hyperechoic dots and short lines). Twenty-three of 25 type I lesions (92.0%) were benign, while 98 of 99 type II and III lesions (99.0%) were malignant. Twenty-one of 24 type II lesions (87.5%) were well-differentiated adenocarcinomas, and all type IIIb lesions were malignant, including 18 poorly differentiated adenocarcinomas (81.8%).
Conclusions: EBUS permits the visualization of the internal structure of peripheral pulmonary lesions, and this information suggests the histology of the lesion.
Key Words: endobronchial ultrasonography • internal structure of peripheral pulmonary lesions • miniature probe
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Introduction
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Numerous reports have shown that high-frequency, two-dimensional ultrasonography is a useful technique for evaluating the depth of invasion of gastrointestinal tumors, for detecting lymph node metastasis, and for identifying coronary stenosis and thrombosis.1
2
3
4
5
Since 1994, our facility has worked on the development of endobronchial ultrasonography (EBUS). EBUS uses a miniature probe inserted through the working channel of a flexible bronchoscope to scan the bronchial lumen. The procedure is able to accomplish the following: (1) determine the depth of invasion in cases of tracheobronchial lesions6
7
; (2) check for invasion of the pulmonaryarteries and veins by hilar tumors, and identify lesions and distinguish metastasis to paratracheal and parabronchial lymph nodes8
9
; and (3) localizeperipheral pulmonary lesions during endobronchial brushing and trans-bronchial biopsy (TBB).10
11
The present study was undertaken to examine the internal structure of peripheral pulmonary lesions as visualized by EBUS and to correlate these findings with the histopathology. The goal was to improve the criteria for distinguishing between benign and malignant peripheral pulmonary tumors.
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Materials and Methods
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Subjects
Correlation Between Preoperative EBUS Images and the Histopathology of Peripheral Pulmonary Lesions:
The records of 69 patients who underwent diagnostic preoperative EBUS for a peripheral lesion between January 1996 and December 2000 and whose surgical specimens could be sectioned were reviewed. The histopathologic findings were correlated with the internal structure of the lesions, as visualized by EBUS.
Typing the Internal Structure of 124 Lesions Visualized by EBUS:
One hundred sixty-eight patients with peripheral pulmonary lesions underwent EBUS between January 1997 and December 2000, and EBUS was able to visualize the lesion in 143 patients (85.1%). Of these patients, a definitive histopathologic diagnosis was made in 124 (73.8%). The internal structure of these lesions was analyzed, and the lesions were typed based on these findings.
Methods and Equipment
Correlation Between the Preoperative EBUS Images and the Histopathologic Findings:
Bronchoscopy was performed with a flexible bronchoscope under local anesthesia without sedation. The miniature probe was inserted into bronchi that were suspected to lead to the lesions visualized by plain roentgenography or CT scanning. The probe was introduced up to the point at which the operator felt resistance to further advancement of the probe, and scanning was performed while the probe was withdrawn to obtain EBUS images. Surgery specimens were fixed in formalin and cut into 2-mm-thick slices, and the EBUS findings were correlated with the histopathology or hematoxylin-eosin-stained specimens to identify the anatomy that produced the EBUS images.
Typing of 124 Lesions Based on the Internal Structure by EBUS:
Peripheral pulmonary lesions were classified based on their internal structure, focusing on internal echoes and the architecture of blood vessels, bronchi, and hyperechoic patterns.
Images of the peripheral pulmonary lesion also were obtained by high-resolution CT (HRCT) scanning. The HRCT scanning technique uses 2-mm collimation, a sharp algorithm, a 120-kV peak, 250 mA/s, and a 2-s scan. HRCT scanning was started 60 s after the continuous infusion of contrast material (2 mL/s) was initiated. Informed consent was obtained from all the subjects.
Equipment
EBUS was performed using an endoscopic ultrasound system (EU-M30; Olympus; Tokyo, Japan) equipped with a 20-MHz mechanical radial probe with an external diameter of 2.5 mm (UM-3R; Olympus) or 2.0 mm (UM-4R; Olympus) [Fig 1
].
Beyond the level of the subsubsegmental branches, the probe, with the external diameter of 2.5 mm, came in contact with the inner surface of the bronchus circumferentially, making the use of a balloon (which is needed for the central bronchi) unnecessary. The peripheral bronchi were flexible enough to allow the probe to be guided easily into the subpleural regions. In cases in which the lesions were in S1 or S1 + 2, the hard tip of the 2.5-mm probe was too long, making it difficult to insert this probe into right B1 or left B1 + 2, which have sharp bifurcation angles. In these cases, it was easier to advance the 2.0-mm probe.
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Results
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Correlation Between EBUS Images and the Histopathology
The data from the 69 patients in whom preoperative EBUS images could be correlated with the histopathologic findings of surgical specimens were available for analysis (Table 1
).
Of the 18 cases of well-differentiated adenocarcinoma, EBUS showed the preservation of blood vessels within the lesion in 7 (Fig 2
). The lesions in these cases had homogeneous internal echoes overall, but some hyperechoic dots (ie, < 1 mm in size) also were observed, which reflected the presence of residual air in the invaded alveoli. The distribution of the hyperechoic dots was irregular, and the margins of the lesions also were irregular. Blood vessels could be seen coursing through the lesion (Fig 2)
. One of these blood vessels had a diameter of 0.68 mm when measured histopathologically.
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Figure 2.. A representative case of well-differentiated adenocarcinoma. This image, which shows a typical case of well-differentiated adenocarcinoma, has homogeneous internal echoes overall. Blood vessels coursing through the lesion are visible. The blood vessel (arrow) has a diameter of 0.68 mm when measured histopathologically.
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In eight other cases of well-differentiated adenocarcinoma, no blood vessels were visualized. These lesions also presented an irregular distribution of hyperechoic dots or arcs around the probe and had poorly defined borders.
In 25 of the 26 cases of moderately differentiated adenocarcinoma and in 6 of 7 cases of squamous cell carcinoma, the EBUS images showed the obstruction of blood vessels within the lesion, the obstruction of bronchi, heterogeneous internal echoes, and irregular margins (Fig 3
). In one case of moderately differentiated adenocarcinoma, numerous very small hyperechoic echoes were observed within the lesion, the distribution of which was identical to that of the multiple calcifications observed histopathologically. In two cases of squamous cell carcinoma, numerous echo-free areas of various sizes were noted, and their distribution corresponded to areas of necrosis (Fig 4
). In one other case of squamous cell carcinoma, a circular hyperechoic line around the probe corresponded to the bronchial wall, revealing the growth and outward compression of the adventitia of the bronchus. In six cases of poorly differentiated adenocarcinoma, EBUS revealed few patent blood vessels or bronchi, heterogeneous internal echoes, and irregular margins.
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Figure 3.. A representative case of moderately differentiated adenocarcinoma. This EBUS image revealed the obstruction of blood vessels within the lesion, the obstruction of bronchi, heterogeneous internal echoes, and irregular margins.
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Figure 4.. A representative case of squamous cell carcinoma. This EBUS image revealed numerous echo-free areas of various sizes within the lesion, and their distribution corresponded histopathologically to areas of necrosis within the tumor.
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In three of four cases of small cell carcinoma, the tumors had directly invaded the pulmonary artery adjacent to the affected bronchus, resulting in stenosis of the pulmonary artery within the lesion (Fig 5
). In three cases, carcinoid tumors had grown out of the bronchial lumen across the bronchial wall, resulting in a characteristic snowman-like form, with the neck located at the cartilaginous part of the bronchus. Bleeding within the carcinoid tumor appeared as mottled hyperechoic areas on the EBUS images (Fig 6
).
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Figure 5.. A representative case of small cell carcinoma. This small cell carcinoma had directly invaded the pulmonary artery (arrow) coursing along the affected bronchus, resulting in stenosis of the pulmonary artery within the lesion.
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Figure 6.. A representative case of carcinoid tumor. This carcinoid tumor had grown out of the bronchial lumen across the bronchial wall, resulting in a characteristic snowman-like form, with the neck located at the cartilaginous part of the bronchus. Bleeding within the carcinoid tumor was visible as mottled hyperechoic areas in the EBUS images.
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Internal echoes were homogeneous in cases of primary malignant lymphoma of the lung, and the appearance was similar to that of pneumonia. Large blood vessels remained patent within the lesions, suggesting that the lesions were soft. Echo-free areas with star-shaped margins were visible within the lesion in one case of inflammatory pseudotumor, corresponding to the lumen of the dilated bronchus.
Tumor Typing Based on the Internal Structure Visualized by EBUS
Histopathology was available for 124 lesions visualized by EBUS. The lesions were typed based on the internal echoes (whether homogenous or heterogenous), vascular patency, and the morphology of the hyperechoic areas (reflecting the presence of air and the state of the bronchi) [Table 2
].
Type I: Homogeneous Pattern
Type Ia, Homogeneous Pattern With Patent Vessels and Patent Bronchioles:
Seventeen lesions (13.7%) were classified as type Ia (Fig 7
). The majority of these lesions (15) were pneumonia, characterized by exudate-filled alveoli. EBUS images of this type revealed normal blood vessels and normal bronchi, free of compression and stenosis, within the lesion. The internal echoes were homogeneous. Thus, the ultrasound attenuation was small, and even tissue 15 to 20 mm from the probe could be seen clearly. Because the lesions extended from one lobule to another, the margins were often linear in some parts. The type Ia group also included one case of organizing pneumonia and one case of metastasis from pancreatic cancer in addition to the 15 cases of pneumonia.
Type Ib, Homogeneous Pattern Without Vessels and Bronchioles:
Eight lesions (6.5%) were classified as type Ib (Fig 8
). No blood vessels were seen within the lesion by EBUS. Mottled or linear hyperechoic areas were scant. The internal echoes were homogeneous. Similar to the situation with type Ia lesions, ultrasound attenuation was small, and even tissue 15 to 20 mm from the probe could be visualized clearly. The type Ib group of lesions included one case of moderately differentiated squamous cell carcinoma, four cases of organizing pneumonia, and three cases of tuberculoma.
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Figure 8.. EBUS images of a type Ib lesion. No blood vessels were seen within the lesion. Mottled or linear hyperechoic areas were scarcely visible. The internal echoes were hypoechoic and homogeneous.
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Type II: Hyperechoic Dots and Linear Arcs Pattern
Type IIa, Hyperechoic Dots and Linear Arcs Without Vessels:
Thirteen lesions (10.5%) were classified as type IIa (Fig 9
). All 13 lesions were well-differentiated adenocarcinomas that had replaced the alveolar epithelium. No blood vessels could be visualized within the lesions by EBUS. Hyperechoic dots or hyperechoic linear arcs (primarily around the probe) were distributed irregularly within the lesions. The presence of residual air in the alveoli is characteristic of well-differentiated adenocarcinomas, which grow to replace the alveolar epithelium. The air remaining in the alveoli hampered the visualization of blood vessels within the lesions and obscured the margins of the lesions.
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Figure 9.. EBUS images of type IIa lesions. No blood vessels could be visualized within the lesions. Hyperechoic dots (< 1 mm in diameter) or hyperechoic linear arcs (primarily around the probe) were distributed irregularly within the lesions.
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Type IIb, Hyperechoic Dots and Linear Arcs With Patent Vessels:
Eleven lesions (8.9%) were classified as type IIb (Fig 10
). The majority of lesions (eight) were well-differentiated adenocarcinomas that had proliferated and replaced the alveolar epithelium while preserving the blood vessels within the lesion. In the EBUS images, the blood vessels showed little or no compression or stenosis within the lesion, and the internal echoes were relatively homogeneous. Hyperechoic dots, distributed irregularly within the lesions, corresponded to residual air in the alveoli, which is a characteristic of well-differentiated adenocarcinoma. The density of cancer cells was higher, and the volume of air remaining in the alveoli was smaller in type IIb lesions than in type IIa lesions (ie, well-differentiated adenocarcinoma). The margins were irregular because the lesions grew without any relationship to existing structures. The type IIb group included one case of moderately differentiated adenocarcinoma and two cases of malignant lymphoma, in addition to the eight cases of well-differentiated adenocarcinoma.
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Figure 10.. EBUS images of a type IIb lesion. Blood vessels (arrow), almost free of compression or stenosis, were visible within the lesions, and the internal echoes were relatively homogeneous. Hyperechoic dots (< 1 mm in diameter) were distributed irregularly within the lesions, corresponding to the presence of residual air in the alveoli.
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Type III: Heterogeneous Pattern
Type IIIa, Heterogeneous Pattern With Hyperechoic Dots and Short Lines:
Fifty-three lesions (42.7%) were classified as type IIIa (Fig 3) . The majority of cases (30) were moderately differentiated adenocarcinomas that had grown with a relatively high cell density and had formed a mass. No blood vessels were seen within the lesion by EBUS. Areas of mottling and linear hyperechoic areas were irregularly distributed within the lesion, corresponding to compressed or stenotic bronchi or alveolar air. The internal echoes were heterogeneous, markedly attenuated sound-wave transmissions, so only areas about 6 to 8 mm from the probe could be visualized clearly. Because the lesions spread in a random manner, without extension along lung structures, the margins of the lesions often were rounded. The type IIIa group included three cases of well-differentiated adenocarcinoma, four cases of poorly differentiated adenocarcinoma, nine cases of moderately differentiated squamous cell carcinoma, six cases of poorly differentiated squamous cell carcinoma, and one case of organizing pneumonia, in addition to the 30 cases of moderately differentiated adenocarcinoma. Moderately differentiated squamous cell carcinomas presented numerous echo-free areas that corresponded to areas of necrosis within the tumor, which is characteristic of squamous cell carcinoma.
Type IIIb, Heterogeneous Pattern Without Hyperechoic Dots and Short Lines:
Twenty-two lesions (17.7%) were classified as type IIIb (Fig 11 ). The majority of lesions (18) were poorly differentiated adenocarcinoma, which had a high cell density and had formed a mass. The lesions were avascular and showed scant mottled or linear hyperechoic areas. The internal echoes were heterogeneous. Since the lesions extend outward, their margins tend to be roundish. This group included one case of moderately differentiated adenocarcinoma and three cases of poorly differentiated squamous cell carcinoma, in addition to the 18 cases of poorly differentiated adenocarcinoma.
Thus, of the 17 type Ia lesions, 15 were pneumonia and 1 was organizing pneumonia. Of the eight type Ib lesions, four were organizing pneumonia and three were tuberculomas. So, 23 of 25 type I lesions (92.0%) were benign disease, while 98 of 99 type II and III lesions (99.0%) were malignant (Table 2)
.
Twenty-one of 24 type II lesions (87.5%) were well-differentiated adenocarcinomas. All 22 type IIIb lesions were malignant, including 18 cases (81.8%) of poorly differentiated adenocarcinoma.
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Discussion
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EBUS uses high-frequency ultrasound (20 MHz) to create detailed images of the internal structures of lesions, although it cannot image tissue that is external to the lesion. Endoscopic ultrasonography has been used to examine the internal structure of pancreatic lesions, and the results have been correlated with histopathology in cases of cystic tumors, calcifications, and pancreatic stones.10
11
Some investigators have reported that dynamic MRI provides information on enhanced patterns of peripheral pulmonary lesions.12
13
Awaya et al14
has reported that the bronchi and vessels can be seen as they cross peripheral lesions. The advantage of MRI is that it is less invasive than EBUS, but the images are of poorer quality because the beating heart and breathing introduce motion artifacts.13
The use of miniature ultrasound probes for diagnosing peripheral pulmonary lesions has been reported previously. Hürter and Hanarath15
reported the successful visualization of peripheral lung lesions in 19 of 26 cases, and Goldberg et al16
reported that EBUS provided unique information that complement other diagnostic modalities in 18 of 25 cases (including 6 peripheral lesions and 19 hilar tumors). This is the first report to focus on the internal structure of peripheral pulmonary lesions and to correlate these findings with the histopathology of the surgical specimen.
We also evaluated the spatial resolution of EBUS using the 20-MHz probe. Spatial resolution, which refers to resolution in the direction of the propagated wave front, and is theoretically defined as follows: spatial resolution (
x) = n
/2 (where is the wavelength and n is an empirically derived coefficient that is 4 to 5). At a frequency of 20 MHz, the speed of sound transmission through soft tissue in vivo is 1,540 m/s, and the spatial resolution (x) is approximately 0.38 mm. In one case of well-differentiated adenocarcinoma, the tumor vessel was visualized by EBUS that had a diameter of 0.68 mm on histopathologic examination. This indicates that blood vessels of this caliber can be visualized using the 20-MHz probe.
We developed our classification system with the aim of distinguishing between benign and malignant diseases, identifying the type of lung cancer, and determining the degree of differentiation.
Two patients with type Ia lesions had a disease other than pneumonia. One of these patients had pulmonary metastasis from pancreatic cancer, and the other had moderately differentiated adenocarcinoma. In both cases, blood vessels and bronchi within the lesion were preserved. However, blood vessels and bronchi could not be visualized in some areas of the lesions. Because of such heterogeneity, we think that it may be necessary to further divide type Ia into subtypes depending on whether the preserved blood vessels and bronchi are distributed homogeneously or heterogeneously. Type IIIa lesions included a variety of different types of lung cancer. Three lesions contained multiple cysts, and the tumors were moderately differentiated squamous cell carcinomas in all three cases. Thus, the presence of multiple cysts is suggestive of squamous cell carcinoma.
The average time that required to complete EBUS in 168 patients with peripheral pulmonary lesions was 8.38 min. Fluoroscopy was not able to confirm whether or not the forceps had reached the favorable point for endobronchial brushing and TBB. EBUS cannot create images of healthy air-filled lungs, but it can image peripheral pulmonary lesions because only small amounts of air come into contact with the probe. The exploration of some bronchi with the miniature probe allowed us to determine, more definitively than with fluoroscopy, which bronchus should be selected for endobronchial brushing and TBB. EBUS is also useful for examining lesions that are difficult to visualize by fluoroscopy (eg, lesions behind the mediastinum or diaphragm, ill-defined shadows, small lesions, and lesions behind another shadow). EBUS clearly identifies which bronchus is most closely related to the lesion and which bronchus should be subjected to biopsy. On fluoroscopy, the probe appeared at a slight distance even when the probe was at the site of the lesion, as demonstrated by the definitive diagnosis of adenocarcinoma by endobronchial brushing at the site of EBUS. This suggests that the area at the margins of the lesions contain more air, so the margins may appear normal on fluoroscopy, and the size of the lesion is underestimated.
If EBUS is unable to reach a lesion, what procedure should be tried? The usefulness of a technique using a curette loaded into the guide sheath is now under investigation for visualizing lesions that are not accessible with a probe. In a modification of the technique, the curette, capped by a guide sheath, is introduced into the lesion. Then, the curette is withdrawn, leaving the guide sheath in situ. The miniature probe then is introduced through the guide sheath to the lesion and then pulled back for scanning to acquire EBUS images. The probe then is removed with the guide sheath left in situ in the lesion. A biopsy forceps or bronchial brush then is introduced into the sheath, and brushings and/or biopsy specimens are collected.
EBUS provides a new way to visualize the internal structures of peripheral pulmonary lesions. Classification of the ultrasonograms suggests the pathology and histology of the lesions.
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Footnotes
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Abbreviations: EBUS = endobronchial ultrasonography; HRCT = high-resolution CT; TBB = transbronchial biopsy
Received for publication November 13, 2001.
Accepted for publication June 4, 2002.
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TOP
Abstract
Introduction
