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Transthoracic ultrasound (US) has become an important diagnostic tool in modern chest
medicine. The range of thoracic lesions for which transthoracic US may yield useful diag-
nostic information has expanded to include not only chest wall and pleural lesions, but
also peripheral lung nodules, pulmonary consolidations, necrotizing pneumonias and
lung abscesses, tumors with obstructive pneumonitis, mediastinal masses, and peri-
diaphragmatic lesions. A variety of ultrasound features and signs of chest diseases have
been well characterized and widely applied in clinical practice. US guidance increases the
diagnostic success rate and decreases the complications associated with interventional
procedures such as thoracentesis, closed tube drainage for pleural effusion, and needle
biopsy of the pleura. Transthoracic needle aspiration or biopsy, under real-time US guidance,
is a relatively safe and easy procedure, and may provide adequate tissue sampling of
lesions for cytologic, histologic or microbiologic analysis. This article presents the general
techniques and wide applications of transthoracic US and US-guided invasive procedures
in the diagnosis and management of various chest diseases.
©Elsevier & CTSUM. All rights reserved. J Med Ultrasound 2008 • Vol 16 • No 1 7
T.H. Tsai, J.S. Jerng, P.C. Yang
the diagnosis and management of various chest transthoracic US examination: (1) chest wall lesions;
diseases with clinical examples, and describes (2) pleural lesions such as pleural effusion, pleural
patient selection and indications, general imaging thickening or pleural tumors; (3) peridiaphragmatic
techniques, US images of normal chest, ultrasonog- lesions; (4) peripheral pulmonary lesions which abut
raphic characteristics of various chest diseases, and the pleura; (5) pulmonary lesions with an accessible
US-guided interventional procedures. US window; and (6) mediastinal tumors in contact
with the chest wall [1,3,4,7]. In general, indica-
tions for US-guided interventional procedures in-
Techniques for Transthoracic US clude: (1) identifying pleural effusion and guiding
Examination and Normal US Images thoracentesis and drainage for effusion, especially
of the Chest when the effusion is minimal or loculated; (2)
localizing pleural thickening or tumors for pleural
Patient selection and indications biopsy; (3) identifying peripheral pulmonary nod-
Evaluation of thoracic lesions using transthoracic US ules and guiding TNB to determine etiology of
is inherently hindered for two reasons. Firstly, the the lesion, particularly when cancer or infection is
lungs are well concealed by the bony ribs, scapulae, suspected; (4) evaluating the nature of pulmonary
and spine. Secondly, the air-containing lung consolidation of unknown etiology; (5) needle
parenchyma is a poor US transmitter and reflects aspiration of the cavity of a necrotizing pneumonia
most of the US beam. Structures located deep or lung abscess for microbiologic diagnosis; (6)
within a normally aerated lung are not visualized identifying the central tumor producing obstruc-
with transthoracic US. Therefore, the application of tive pneumonitis and guiding TNB of the tumor
transthoracic US is restricted to those with an avail- for histologic diagnosis, especially when fiberoptic
able “US window”, which allows the US beam to bronchoscopy is not feasible; (7) evaluating a
penetrate, allowing visualization of the target lesion mediastinal tumor and guiding TNB for histologic
[1,3,4]. The US window used most often is chest diagnosis; (8) identifying the nature of a chest wall
wall, atelectatic or consolidated lung, or pleural lesion and guiding needle sampling; and (9) assist-
fluid interposed between the lesion and chest wall ing in the assessment of cervical lymphadenopathy
(Fig. 1). The following lesions are thus suited to in patients with lung cancer [1,3–7].
A B
Fig. 1. Pleural effusion as an ultrasound (US) window for approach of a lung tumor. (A) Computed tomography scan shows a lung
tumor and right pleural effusion in an 81-year-old man. (B) The pleural effusion interposed between the tumor and chest wall
creates a US window, allowing visualization of the lung tumor with transthoracic US. The histologic diagnosis of lung cancer was
obtained by transthoracic needle biopsy under US guidance. E = effusion; T = tumor.
General techniques for transthoracic US are seen as two thin and bright echogenic lines.
examination Normally, the two pleural lines are smooth and less
The equipment suitable for transthoracic US imag- than 2 mm in thickness [9]. Because of the move-
ing are those equipped with 3.5-, 5-, 7.5-, or 10-MHz ments of the pleurae during lung excursion, the
convex, linear and sector transducers. Most series two pleural lines glide with each other during res-
also provide both color Doppler US and amplitude piration on real-time US. This is termed “lung slid-
US angiography software which can be used to ing” or “gliding sign” of the pleurae [10]. Small
detect blood flow signals. A higher frequency (i.e. uneven irregularities of the visceral pleura may
7.5- or 10-MHz) transducer provides better resolu- produce vertical reverberations known as “comet-
tion of near structures, such as the chest wall and tail artifacts” [9,11] (Fig. 2). However, with a 3.5-
pleura. Otherwise, a 3.5-MHz transducer is more MHz transducer, it is not always possible to
suitable for visualization of deeper lesions. A linear visualize the two pleural lines and the pleural space
or convex transducer usually has a broad view of between them. Instead, a highly echogenic line
the field and is better than a sector scanner for representing the pleurae and the pleuropulmonary
screening. For lesions with a small US window or a surface is seen with reverberation echo artifacts
very narrow intercostal space, a sector transducer just beneath it. Back-and-forth movements of this
is generally preferred [1,3,7]. echogenic pleural line during respiration can still
During transthoracic US examination, the patient be observed on real-time US.
can be scanned in the sitting or supine position. The underlying air-filled lung is a highly reflec-
Bedridden patients can be examined in the lateral tive interface that may block transmission of US
decubitis or oblique position. After applying US into the lung parenchyma. US images of the lung
transmission gel, the probe is moved in transverse parenchyma thus display a pattern of repeated
or longitudinal directions along the intercostal horizontal echoes caused by an acoustic reverbera-
spaces to avoid interference by the bony ribs. The tion artifact [11] (Fig. 2). These echoes may be
lesion is first localized using grayscale, real-time US bright but formless, and diminish rapidly in inten-
imaging, and normal areas are also scanned for sity with increasing distance from the transducer.
control comparisons. The location, sonographic Both hemidiaphragms can be visualized just above
appearance and echogenicity, and vascularity of the liver and spleen, and the respiratory move-
the lesion are characterized, with the latter charac- ments of both hemidiaphragms can be observed
teristic determined by color Doppler US [8]. The on real-time US. During inspiration, the reverbera-
liver and fasted gallbladder can be used as tissue- tion echoes of the lower lung descend progressively
texture references for solid and fluid-containing with lung excursion and appear like a curtain. By
regions. Hence, the echogenicity of a lesion is com- defining the position of the hemidiaphragm, dif-
pared with that of the liver and defined as hypo- ferentiation can be made between the thoracic
echoic, isoechoic or hyperechoic accordingly. and abdominal compartments.
A B C
Fig. 2. Normal ultrasound images of the chest. (A) Transverse image through the intercostal space using a 10-MHz scanner.
The chest wall is visualized as multiple layers of echogenicity representing muscles and fasciae. The visceral and parietal pleurae
appear as echogenic bright lines that glide during respiration (gliding sign). Reverberation echo artifacts beneath the pleural lines
imply an underlying air-filled lung. (B) Longitudinal image across the ribs. Normal ribs are seen as hyperechoic chambered surfaces
(arrowheads) with prominent acoustic shadows beneath the ribs. (C) Ultrasound image displaying comet-tail artifacts (arrows).
Pp = parietal pleura; Pv = visceral pleura.
and intrathoracic lesions that extend peripherally vessel [13]. In patients with palpable cervical
into the chest wall. On US, chest wall tumors lesions of unknown nature, US can differentiate
usually appear as well-defined, hypoechoic masses lymph nodes from ligaments, thrombosed veins,
within the soft tissue layers of the chest wall. scar tissue, nodular goiter, or fat pads. The cytol-
Inflammatory lesions may show an irregular mar- ogic features of affected lymph nodes can be clari-
gin and heterogeneous internal echo texture. When fied with the aid of aspiration cytology [14].
the chest wall lesion invades the ribs, areas of
destructive bone may be seen as eccentric, hyper- Pleural effusion
echoic plate-like shadows inside the lesion. Oste- US is very helpful in determining the nature of
olytic bone lesions caused by metastatic tumors pleural lesions and is extremely sensitive in detect-
generally appear as round or ring shadows within ing pleural effusion. On US, pleural effusion is
the center of a hypoechoic tumor (Fig. 3). US- characterized by an echo-free or hypoechoic space
guided percutaneous aspiration or biopsy of chest between the visceral and parietal pleurae that can
wall lesions has been reported to have a very high change shape with respiration (Fig. 4A). The effu-
diagnostic yield [12]. sion can be free or encapsulated. Compressive
US is also useful for the evaluation of cervical atelectasis of the lung in a large effusion may be
and supraclavicular lymph nodes in patients with seen as a tongue-like structure within the effusion.
malignancy. Lymph nodes on US appear as round According to the internal echogenicity, effusion
or ovoid, discrete hypoechoic nodules, or multiple can be classified as anechoic, complex nonsep-
confluent and lobulated masses within the soft tis- tated, complex septated, and homogeneously
sue layers. Color Doppler US can be employed to echogenic [15]. The effusion is defined as anechoic
differentiate the cross section of a vessel from a if a totally echo-free space is present between the
lymph node by detecting blood flow signals in the visceral and parietal pleurae, complex nonseptated
A B
Fig. 3. A 68-year-old man with metastatic lung cancer to the chest wall. (A) Computed tomography scan shows a soft tissue tumor
with rib destruction (arrowheads). (B) Ultrasound reveals a well-defined, hypoechoic mass within the chest wall. The hyperechoic
rings inside the hypoechoic tumor represent osteolytic ribs (arrows). T = tumor.
A B C
D E
Fig. 4. (A) Ultrasound image of minimal subpulmonary effusion seen as an echo-free space between the visceral pleura, parietal
pleura, and diaphragm. This echo-free space may change shape with respiration. (B–E) The effusion can be subclassified as
(B) anechoic, (C) complex nonseptated, (D) complex septated, and (E) homogenously echogenic. Note the movable echogenic
densities within the complex nonseptated effusion, and the floating strands and septa within the complex septated effusion
(arrows). D = diaphragm; L = collapsed lung; PE = pleural effusion.
if echogenic materials are present inside the effu- space is demonstrated (Figs. 4B–4E). The echogenic
sion, complex septated if floating strands or septa densities within a complex effusion probably reflect
are present inside the effusion, and homogeneously the presence of tissue debris, protein-rich particles,
echogenic if a homogeneously echogenic pleural fibrins, or blood in the pleural fluid. Sonographic
characteristics of effusion are informative for differ- within a two-probe range; and (4) large or massive,
entiating transudate from exudate. In a study of if the space is bigger than a two-probe range [7].
320 patients, it was found that a transudate was Although transthoracic US is very powerful in
invariably anechoic, whereas an anechoic effusion the evaluation of pleural effusion, differentiation of
can be either a transudate or an exudate. Pleural minimal effusion from organized effusion or pleural
effusions with complex nonseptated, complex thickening may sometimes be difficult. Both lesions
septated and homogeneously echogenic patterns can appear anechoic on grayscale US, and thus,
are always exudative. Homogeneously echogenic “free of echoes” is not a reliable sign for fluid collec-
effusion is typically seen in hemorrhagic effusion tion. It has been reported that nearly 20% of echo-
and empyema [15]. free pleural lesions do not yield free fluid, whereas a
Other associated sonographic findings some- significant percentage of complex-appearing lesions
times help to assess the nature of pleural effusion do [20]. Therefore, accurately predicting whether
[7]. For example, effusion with adjacent thickened an echo-free or complex-appearing lesion is ame-
pleura is usually indicative of an exudate. The pres- nable to thoracentesis is not always possible with
ence of a pulmonary consolidation may suggest grayscale US. Marks et al suggested that if a pleural
an exudate of infectious origin. Pleural nodules may lesion changes its shape with respiratory excursion
be seen in patients with malignant effusion [16]. In and if it contains movable strands or echo densities,
cases of acute thoracic empyema, it was reported the lesion contains fluid and can be aspirated [21].
that sonographic septation is a useful sign in pre- However, these criteria still have limitations, as some
dicting the need for subsequent intrapleural fibri- loculated or small effusions do not change shape
nolytic therapy or surgical intervention [17]. with respiration or have movable septa or echo den-
Methods for measuring the volume of pleural sities, but are still amenable to aspiration. Another
effusion by means of US have been reported in sev- useful sign to distinguish effusion from a solid pleu-
eral studies [18,19]. The volume of effusion can also ral lesion is the so-called “fluid color sign” of pleural
be arbitrarily classified as: (1) minimal, if the echo- effusion [22,23]. It was observed that true fluid,
free space is seen within the costophrenic angle; even in cases of loculated or small effusions, may
(2) small, if the space is over the costophrenic angle generate a color flow pattern during the respiratory
but still within a one-probe range; (3) moderate, if or cardiac cycle and thus display a turbulent color
the space is greater than a one-probe range but signal with color Doppler imaging (Fig. 5). In a study
A B
Fig. 5. Fluid color sign to differentiate minimal effusion from a solid pleural lesion. (A) True fluid generates a color flow pattern
during respiratory or cardiac cycles on color Doppler ultrasound. (B) Organized pleural thickening or pleural tumor appears as
a colorless pleural lesion on color Doppler ultrasound.
comprising 76 patients, relatively high sensitivity (Fig. 7). Sometimes, differentiation between pleu-
(89.2%) and specificity (100%) of the fluid color ral fibrosis and pleural tumors is difficult, while US-
sign in recognizing minimal fluid collection have guided needle biopsy is helpful for pathologic
been demonstrated [23]. diagnosis [26].
A B
Fig. 6. Putrid pleuritis resulting in pleural thickening in an 82-year-old man with acute thoracic empyema. (A) On admission,
ultrasound showed massive pleural effusion with sonographic septation. Closed tube drainage and intrapleural fibrinolytic therapy
were performed for the empyema. PE = pleural effusion; (B) One month later, obvious thickening and adhesion of the pleura were
revealed on ultrasound, with highly echogenic shadows indicative of calcification. P = pleura.
A B C
Fig. 7. Various ultrasound images of metastatic pleural tumors. (A) Pleural nodule. (B) Polypoid pleural tumors. (C) Sheet-like
pleural thickening (arrows). L = collapsed lung; PE = pleural effusion; T = pleural tumor.
Peridiaphragmatic lesions
Radiographic elevation of a hemidiaphragm and
peridiaphragmatic lesions usually pose a diagnostic
problem for physicians. Using liver and spleen as
Fig. 8. Ultrasound image of hydropneumothorax. Note the air– a US window, US is very useful in the simultaneous
fluid level (arrow). Loss of gliding sign is demonstrated above the evaluation of abnormalities in supradiaphragmatic,
air–fluid level on real-time ultrasound, which implies pneu- diaphragmatic and infradiaphragmatic compart-
mothorax. During inspiration, the reverberation echoes of the ments. Transthoracic US can identify basal pulmo-
pneumothorax progressively descend and present the lowering
nary tumors, subphrenic abscesses, and hepatic or
of a “curtain” that gradually masks the effusion (curtain sign).
splenic masses located in peridiaphragmatic areas.
E = effusion; L = collapsed lung; PNEUMO = pneumothorax.
By defining the position of the hemidiaphragm,
differentiation of subpulmonary effusion and sub-
generates the so-called “curtain sign”, which allows phrenic fluid collection is relatively easy (Fig. 9).
the confident diagnosis of hydropneumothorax Also, the real-time visualization of diaphragm
[27] (Fig. 8). motion during respiration allows discrimination
It is recommended that the US findings sugges- between diaphragm palsy and eventration [28].
tive of pneumothorax be compared with those of
the healthy side of the chest. It should be noted Peripheral lung tumors
that the gliding sign of the pleurae on real-time US On US, peripheral lung tumors appear as well-
comes from the movements of the pleurae during defined, homogeneous, hypoechoic or echogenic
respiratory excursion. Certain conditions, such as nodules with posterior acoustic enhancement. The
bullae or emphysema, may result in impaired echogenicity of the tumor increases with tumor
lung expansion, and subsequently, the absence or size. Central necrosis can be detected in some
A B
Fig. 9. A 46-year-old man with subphrenic abscess complicated after a radical nephrectomy for left renal cell carcinoma. Chest
radiograph shows elevation of left hemidiaphragm with costophrenic angle blunting (not shown). (A) Computed tomography scan
reveals subphrenic abscess and left pleural effusion. (B) Ultrasound can simultaneously show pleural effusion, subphrenic abscess
fluid collection, and outline of the diaphragm. A = subphrenic abscess; PE = pleural effusion; D = diaphragm.
cases of large cavitary tumor. If the tumor extends on US are indicators of pleural and chest wall
to the pleura, the pleural line may be interrupted involvement [29,30].
[1,3,4]. In patients with lung cancer, detection of Pulmonary arteriovenous malformations are fre-
tumor extension to the pleura and chest wall is quently located in the periphery of lungs and may,
important and may influence the subsequent treat- therefore, be detected with transthoracic US. Pul-
ment plan. High-resolution real-time US, particu- monary arteriovenous malformations on US appear
larly with higher frequency (i.e. 7.5- or 10-MHz) as well-defined hypoechoic nodules, with turbulent
scanning probes, has the advantage of clear dis- blood flow through the lesion on color Doppler
crimination of the various soft tissue layers within imaging. Flow signals into and out of the lesion, as
the chest wall, and thus can be very valuable for well as their anatomic continuity, can be clearly
determining the extent of pleural and chest wall demonstrated. The characteristic of low-impedance
invasion in patients with lung cancer [29]. Sugama flow can be shown by spectral wave analysis
et al [30] have defined the US criteria for the extent (Fig. 11). US can also reveal a decrease or disap-
of tumor invasion. Ultrasound pattern (UP)1 indi- pearance of flow in these lesions after effective
cates that the tumor is in contact with the visceral arterial embolization [31].
pleura, while UP2 means that the tumor has
extended beyond the visceral pleura and is in con- Pulmonary consolidation, lung abscess, and
tact with the parietal pleura, and UP3 means that obstructive pneumonitis
the tumor has extended to the chest wall through The consolidated lung on US may appear as a
both visceral and parietal pleurae. On US, the vis- wedge-shaped hypoechoic lesion that can move
ceral pleura line is intact in UP1, but is invaded or with respiration. The margin is typically irregular or
interrupted in UP2 and UP3. Direct visualization of serrated. The air bronchogram within the consoli-
chest wall extension by the tumor can be observed dation may present as bifurcating hyperechoic lines
in UP3. The movement of the tumor with respira- arising from the hilar region. These hyperechoic air
tion is unaltered in UP1, disturbed in UP2, and is densities can move with respiration on real-time
not present in UP3 [30] (Fig. 10). In summary, dis- US (Fig. 12A). Microabscesses in necrotizing pneu-
ruption of the pleura, extension through the chest monia can be detected as scattered hypoechoic
wall, and fixation of the tumor during breathing to anechoic spaces within the irregular-shaped
A B
C D
Fig. 10. Ultrasound patterns (UP) of tumor invasion to the pleura and chest wall. (A) UP1 indicates that the tumor is in contact
with the visceral pleura. The visceral and parietal pleurae lines are intact, and smooth respiratory movement of the tumor is visible
on real-time ultrasound. (B) UP2 indicates the tumor extends beyond the visceral pleura, and is in contact with the parietal pleura.
The visceral pleura line is thus interrupted, and the respiratory movement of the tumor is disturbed on real-time ultrasound.
(C) UP3 indicates the tumor extends to the chest wall through the visceral and parietal pleurae. There is no respiratory movement
of the tumor. Note that the invaded ribs are seen as hyperechoic plate-like shadows inside the lesion (arrows). (D) Computed
tomography scan from the same patient as in Figure (C). PAE = posterior acoustic enhancement; Pp = parietal pleura; Pv = visceral
pleura; T = tumor.
consolidation. Some of the microabscesses may an irregular wall width, a blurred outer margin, an
have hyperechoic speckled densities which repre- oval or round shape, an acute chest wall angle,
sent air echoes inside the cavity [32]. In the case and a negative pleural separation [34].
of a lung abscess, the air within the cavity may ”Fluid bronchogram” is a very useful sign indica-
appear as a hyperechoic area with a posterior tive of bronchial obstruction, and the presence of
acoustic shadow (Fig. 12B). The air–fluid level of this sign in an appropriate clinical context should
the cavity can be demonstrated if the patient is raise suspicion of obstructive pneumonitis. On US,
scanned in the sitting position. The hyperechoic fluid bronchogram is identified as branching hyper-
air portion is depicted in the upper part of the echoic tubular structures with an anechoic interior
lesion, whereas the dependent fluid portion is lumen, representing the dilated fluid-filled airways
inhomogeneous and echogenic [33] (Fig. 12C). within the consolidation (Fig. 13). Fluid bron-
Transthoracic US can be useful in differentiating chogram usually parallels the pulmonary vessels,
between a lung abscess and empyema. The ultraso- but shows no blood flow signals on color Doppler
nographic characteristics of a lung abscess include US [35,36]. In cases of tumor causing obstructive
A B
C D
Fig. 11. Pulmonary arteriovenous malformation. (A) Computed tomography scan shows a well-defined, enhanced mass in the left
upper lung. (B) On grayscale ultrasound (US), the lesion appears as a well-defined, homogenous and hypoechoic mass with posterior
acoustic enhancement. (C, D) Color Doppler US and amplitude US angiography indicate a tangled vascular structure with clear
vessel outline and anatomic continuity. Also note the low impedance flow characteristics on spectral wave analysis. M = mass.
A B C
Fig. 12. (A) Ultrasound (US) image of pulmonary consolidation as a wedge-shaped hypoechoic lesion with bifurcating hyperechoic
lines arising from the hilum. The hyperechoic lines are air densities within the airways of the consolidated lung (air bronchogram).
These hyperechoic lines can move with respiration on real-time US. Localized pleural effusion is also noted. (B) US image of lung
abscess. The air portion is depicted as a hyperechoic area casting a characteristic acoustic shadow below the lesion (arrowheads).
(C) US image of infected bullae in a 41-year-old man. US clearly shows the air–fluid level (arrow) while the patient is scanned in
the sitting position. The air portion is depicted in the upper part of the lesion, whereas the dependent fluid portion is inhomogeneous,
with echogenic densities within the abscess fluid. PE = pleural effusion; A = air portion; F = abscess fluid.
A B
C
Sternum
Lung
AsA
Tumor
US-guided thoracentesis and closed tube to identify the diaphragm and upper abdominal
drainage for pleural effusion organs before puncture, to ensure that the target
For pleural effusion of unknown etiology, it is usually pleural lesion is indeed above the diaphragm [45].
necessary to obtain the fluid for cytologic, biochem-
ical or microbiologic examination. Transthoracic US-guided needle biopsy of the pleura
US is superior to chest radiography in identifying There are some advantages in using transthoracic
fluid collection and choosing the optimal site for US in guiding needle biopsy of pleural lesions. One
diagnostic thoracentesis [4,42]. The largest and advantage of US-guided pleural biopsy is related to
most accessible area of fluid accumulation can be possible focal pleural involvement in various dis-
identified, and the depth for needle penetration eases. Because focal pleural thickening or pleural
can be measured by US. US-guided thoracentesis tumors can be clearly identified with US, biopsy
is particularly useful when the effusion is minimal can be aimed at the local area with sonographic
or loculated, when tedious radiographic study is not abnormalities. The chances of obtaining pleural tis-
possible, or when safe thoracentesis is mandatory sues with significant pathologic findings will thus
in a critically ill patient [2,43]. With real-time US, increase. Another advantage of real-time US is that
direct visualization of the effusion during thoracen- the advance of the needle can be monitored, and
tesis is even applicable. These US-guided measures over-penetration of the needle into the underlying
help to improve the success rate of thoracentesis lung parenchyma can be prevented. This is partic-
and avoid complications such as pneumothorax [4]. ularly true for patients with minimal pleural effusion
By differentiating minimal or loculated effusion from or even without pleural effusion [4,26].
pleural thickening using the US criteria described
earlier, US helps to predict the presence of fluid in US-guided TNB for histologic diagnosis of
the pleural space and to decide whether it is ame- thoracic lesions
nable to thoracentesis. In brief, a pleural space, Transthoracic US can be used to guide TNB of the
which changes shape with respiration or contains chest wall, peripheral pulmonary lesions or medi-
movable stands or echo densities on grayscale US, astinal lesions, for either fine-needle aspiration for
or displays a fluid color sign on color Doppler US, cytologic and microbiologic analyses or large-bore
indicates the presence of fluid accumulation and needle biopsy for histologic diagnosis [1,3–5,46–48].
is amenable to thoracentesis [21–23]. The choice of fine-needle aspiration or large-bore
There are several clinical situations in which biopsy depends greatly on local pathologic exper-
closed tube drainage for effusion is needed. These tise and is too complex to discuss in detail in this
include huge effusions compromising the respiratory article. In general, fine-needle aspiration for cytol-
condition, complicated parapneumonic effusion and ogic examination may be sufficient for clinical man-
empyema, hemothorax, and malignant effusion agement in cases of primary lung cancer. However,
preparing for pleurodesis. Complications related to concerns arise regarding the reliability of nonspe-
these drainage procedures, such as laceration of the cific, benign or negative results. Although multiple
lung, diaphragm, liver and spleen, could be disas- passes may improve the diagnostic yield for malig-
trous. Malposition of the tube can result in failure of nant lesions, a negative result for fine-needle aspi-
drainage, particularly in loculated effusion. As with ration does not confidently exclude malignancy.
diagnostic thoracentesis, it is clear that transthoracic It should be noted that an adequate histologic
US can decrease the risk of malposition and other specimen is generally required for benign lesions,
complications by identifying a suitable site for the mediastinal masses, and some malignancies, such
procedure [44]. On a few occasions, the liver or as lymphomas and sarcomas [46–48]. In a com-
spleen has been mistaken for a fluid collection on US. parative study, it was demonstrated that transtho-
Thus, it would be wise for inexperienced operators racic large-bore Tru-Cut biopsy under US guidance
A B
Collapsed
lung
Heart
Fig. 15. Ultrasound (US) guidance improves diagnostic yield of TNB for malignant tumors with necrosis. (A) Computed tomogra-
phy scan shows a large lung mass with extensive central necrosis and left pleural effusion in a 60-year-old woman. (B) US clearly
reveals the necrotic center (*) and solid portion of the tumor (arrows). The histologic diagnosis of spindle cell sarcoma was made by
transthoracic needle biopsy of the mural portion of tumor under US guidance.
can be as safe as US-guided fine-needle aspiration, route and depth (usually assisted with a precise
and that the diagnostic accuracy is significantly puncture transducer), to avoid penetrating the aer-
higher than that of fine-needle aspiration [47]. ated lung, great vessels or major bronchi. During
In our institution, we almost routinely perform TNB, the tip of the needle and, occasionally, the
fine-needle aspiration first with a 20–22-gauge needle shaft can be seen as an echogenic focus on
needle containing an outer sheath and inner the real-time US monitor, thus allowing advance of
stylet. The aspiration materials placed onto glass the needle to the target lesion with precision.
slides are divided into two groups: one group is Small peripheral lung nodules may move con-
air-dried and the other is fixed in 95% alcohol. siderably with respiration and are often obscured
Papanicolaou stain is used on the alcohol-fixed by overlying ribs. These factors may make TNB dif-
slides, while Liu stain and Gram stain are used on ficult. However, with real-time US monitoring,
the air-dried slides. Liu stain, which is completed in TNB can be performed in a specific phase of respi-
only 3 minutes, can be performed at the bedside ration that renders the nodule most accessible and
and used for immediate microscopic examination evident. Successful localization and biopsy of tumors
to assess the adequacy of the specimens. If the as small as 1 cm have been possible using this
specimens are judged inadequate or inconclusive, approach [49,50]. TNB for large lung masses is
or if histologic specimens are required, large-core generally not difficult. However, large lung masses
cutting biopsies are then performed with a 16-, frequently have extensive areas of central necrosis,
18- or 20-gauge Tru-Cut needle for conventional so that only a small part of the tumor remains viable.
histologic examinations. Aspiration or biopsy of the central necrotic portion
Patients referred for US-guided TNB should be of a malignant tumor may yield a false negative
carefully assessed for the location, sonographic result. US guidance can improve the diagnostic
pattern, and blood flow information of the lesion yield of TNB in such cases by delineating the solid
by grayscale and color Doppler US. Attention portion of the tumor and directing sampling of
should be focused on the lesion that is most likely these mural regions [51] (Fig. 15). For patients with
to be accessible using a percutaneous approach. Pancoast or superior sulcus tumors, although US
Once it has been determined that a lesion is ame- evaluation is often handicapped by interference from
nable to TNB, care is taken to ensure the puncture the scapulae and ribs, satisfactory demonstration
of the lesion is often achieved by the supraclavic- accidental puncture of great vessels and vital struc-
ular approach. US is helpful in assessing the local tures in the mediastinum [40,41]. Because the
extent of tumor involvement and guiding the nee- diagnostic accuracy using fine-needle aspiration is
dle directly to the apical lung tumor for histologic lower in lymphoma, thymic tumors, and benign
diagnosis. Because great vessels may be present in lesions, large-bore needle biopsy is generally rec-
the surrounding area in such cases, color Doppler ommended for mediastinal lesions [40,48].
US can be used to provide detailed vascular infor-
mation prior to TNB [52]. US-guided fine-needle aspiration for
A lung tumor lacking pleural contact but with microbiologic diagnosis of pulmonary
an accessible US window can also be sampled infections
under US guidance. For patients with lung tumors Transthoracic US can be useful in evaluating focal
associated with obstructive pneumonitis, fiberop- pulmonary infiltrates and guiding fine-needle aspi-
tic bronchoscopy is usually the standard diagnos- ration for microbiologic diagnosis of pulmonary
tic approach. However, if the obstructing lesion is infections [1,3,4,32]. Use of this invasive technique
extraluminal, fiberoptic bronchoscopy may reveal may enable accurate microbiologic diagnosis of
only external compression and satisfactory diag- unusual pulmonary infections, which is especially
nostic material cannot be obtained with either helpful in immunocompromised patients [53]. In
bronchoscopic biopsy or transbronchial needle pulmonary consolidations, the fluid-containing air
aspiration. These patients may be subjected to US- spaces become a good US window, and lesions
guided TNB to establish the histologic diagnosis of deep-seated in the consolidated lung can be visual-
the obstructing tumor [35,36]. Using the consoli- ized with transthoracic US. Parapneumonic effusion,
dated lung as a US window, US can clearly delineate abscess formation or tumor with obstructive pneu-
the central tumor and adjacent consolidated lung. monitis can be clearly demonstrated. Thoracentesis
Although some obstructing tumors are deep-seated of empyema or parapneumonic effusion can be per-
and located near the hilum, it is usually possible to formed safely under the guidance of US, even if the
obtain sufficient specimens for cytologic or histol- fluid collection is localized and minimal. Transtho-
ogic diagnosis. The route of the puncture needle racic fine-needle aspiration under US guidance pro-
can be selected to avoid major bronchi and pul- vides reliable and non-contaminated specimens for
monary vessels of the consolidated lung under microbiologic stain and culture. In patients with
real-time US guidance, and thus, the complication necrotizing pneumonia, US can be used as a guide
of major bleeding can be minimized. in the needle aspiration of microabscesses [4,32]. For
Accurate histologic diagnosis of a mediastinal lung abscesses in the lung periphery, high-resolution
mass is a cornerstone for planning appropriate treat- real-time US can identify the areas where the vis-
ment. Surgery is curative for thymoma, teratoma, ceral pleura adheres to the parietal pleura (lesion-
and neurogenic tumor, but is not indicative for pleura symphysis), thus preventing pneumothorax
lymphoma, and should not be performed for and spillage of abscess material into the pleural
metastatic lesions from pulmonary or extrapul- cavity during needle aspiration. US can also pro-
monary sites. Transthoracic US evaluation of medi- vide precise guidance of the needle tip to the fluid
astinal masses followed by a US-guided biopsy is a portion of the abscess and ensure aspiration of an
rapid and safe method of obtaining specimens for adequate amount of fluid for bacterial culture. The
histologic examinations. Transthoracic US has the results of cultures obtained from US-guided abscess
advantage of good discrimination between great aspiration have been found to be superior to those
vessels and the target mass, particularly in conjunc- obtained from sputum, blood, and bronchoalveolar
tion with color Doppler US. The biopsy of medi- lavage fluid [33]. A similar technique can be applied
astinal tumors under real-time US guidance avoids for drainage of abscess fluid if it is clinically indicated.
Pulmonary cryptococcosis is not a rare disease in window, transthoracic US is a very reliable and
both immunocompetent and immunocompromised informative imaging modality for evaluating lesions
hosts, and possesses the potential for dissemination. of the chest wall, pleural cavity, perdiaphragmatic
A definite diagnosis of pulmonary cryptococcosis area, mediastinum, and peripheral lung. The range
requires a specific histopathologic examination and of chest diseases for which transthoracic US may
a positive culture. Serum cryptococcal antigen is yield diagnostic information has greatly expanded.
often negative in such cases. Therefore, a timely and Color Doppler US further increases the diagnostic
correct diagnosis of pulmonary cryptococcosis is potential and safety of invasive procedures. US
often difficult. Because the lesions of pulmonary guidance increases the success rate while decreasing
cryptococcosis tend to be subpleural in location, the complications of many interventional proce-
specimens can usually be obtained with US-guided dures such as thoracentesis, closed tube drainage for
needle aspiration for fungal isolation. Cryptococci pleural effusion, and needle biopsy of the pleura.
can also be directly detected after the lung aspirates With real-time US monitoring and precise puncture-
have been stained with Liu or Papanicolaou stain or guiding devices, US can be used effectively to guide
with India ink [54]. In addition, direct determina- TNB and other invasive procedures in the thorax.
tion of crytoptococcal antigen in lung aspirates Although US-guided TNB requires certain expertise,
has been shown to be a rapid and useful method for the technique is relatively easy to master and can
diagnosis of pulmonary cryptococcosis, and can be be performed in many situations where computed
more reliable than isolation of this organism [55]. tomography-guided aspiration or biopsy would
US-guided transthoracic fine-needle aspiration previously have been used. Our experience with
through the consolidated lung is relatively safe. US transthoracic US suggests that it considerably en-
helps to select an area where the consolidation is hances the diagnostic and therapeutic capabilities of
complete and where there is no air-containing tissue chest physicians, improves patient care, is efficient
interposed between the lesion and pleura. The major and cost-effective, and has become an indispensable
bronchi and vessels within the consolidation can be imaging tool in modern chest medicine.
clearly identified by high-resolution US in conjuga-
tion with color Doppler US. The route for needle
aspiration can be selected to avoid these vital struc- References
tures, and thus, the complications of major bleed-
ing and pneumothorax can be minimized [4,32]. 1. Yang PC. Ultrasound-guided transthoracic biopsy
It should be noted that the etiology of pulmonary of the chest. Radiol Clin North Am 2000;38:323–43.
consolidation is diverse. Although infectious pneu- 2. Yu CJ, Yang PC, Chang DB, et al. Diagnostic and
monia is the most common, noninfectious diseases therapeutic use of chest sonography: value in critically
ill patients. AJR Am J Roentgenol 1992;159:695–701.
such as lymphoma and bronchioloalveolar cell car-
3. Yang PC. Ultrasound-guided transthoracic biopsy of
cinoma may also present as pulmonary consolida-
peripheral lung, pleural, and chest wall lesions. J Thorac
tions. US-guided large-bore biopsy has been proved Imaging 1997;12:272–84.
useful and relatively safe for histologic diagnosis of 4. Yang PC, Kuo SH, Luh KT. Ultrasonography and
pulmonary consolidation of unknown etiology [32]. ultrasound-guided needle biopsy of chest diseases:
indications, techniques, diagnostic yields and com-
plications. J Med Ultrasound 1993;2:53–63.
5. Beckh S, Bolcskei PL, Lessnau KD. Real-time chest
Conclusion
ultrasonography: a comprehensive review for the pul-
monologist. Chest 2002;122:1759–73.
Advances in transducer design, signal processing, 6. Koh DM, Burke S, Davies N, et al. Transthoracic US of
and Doppler technology have greatly improved the the chest: clinical uses and applications. Radiographics
imaging quality of US. By scanning through the US 2002;22:e1.
7. Tsai TH, Yang PC. Ultrasound in the diagnosis and 23. Wu RG, Yang PC, Kuo SH, et al. Fluid color sign: a use-
management of pleural disease. Curr Opin Pulm Med ful indicator for discrimination between pleural thick-
2003;9:282–90. ening and pleural effusion. J Ultrasound Med 1995;
8. Yang PC. Applications of colour Doppler ultrasound 14:767–9.
in the diagnosis of chest diseases. Respirology 1997; 24. Gorg C, Gorg K, Schwerk WB, et al. Sonography of
2:231–8. the diaphragmatic pleura in tumor patients. Ultraschall
9. Mathis G. Thoraxsonography—Part I: chest wall and Med 1988;9:274–8. [In German]
pleura. Ultrasound Med Biol 1997;23:1131–9. 25. Heilo A, Stenwig AE, Solheim OP. Malignant pleural
10. Lichtenstein DA, Menu Y. A bedside ultrasound sign mesothelioma: US-guided histologic core-needle bi-
ruling out pneumothorax in the critically ill. Lung slid- opsy. Radiology 1999;211:657–9.
ing. Chest 1995;108:1345–8. 26. Chang DB, Yang PC, Luh KT, et al. Ultrasound-
11. Lichtenstein D, Meziere G, Biderman P, et al. The guided pleural biopsy with Tru-Cut needle. Chest 1991;
comet-tail artifact: an ultrasound sign ruling out pneu- 100:1328–33.
mothorax. Intensive Care Med 1999;25:383–8. 27. Targhetta R, Bourgeois JM, Chavagneux R, et al.
12. Yang GG, Wu HD, Yang PC, et al. Sonographic pat- Ultrasonographic approach to diagnosing hydro-
terns of ribs with tumor involvement. J Formosan Med pneumothorax. Chest 1992;101:931–4.
Assoc 1991;90:141–5. 28. Ko JC, Yang PC, Chang DB, et al. Ultrasonog-
13. Chang DB, Yang PC, Luh KT, et al. Ultrasonic evalua- raphic evaluation of peridiaphragmatic lesions:
tion of cervical lymphadenopathy. J Formosan Med Assoc a prospective study. J Med Ultrasound 1994;2:
1990;89:286–92. 84–92.
14. Chang DB, Yang PC, Yu CJ, et al. Ultrasonography 29. Suzuki N, Saitoh T, Kitamura S. Tumor invasion of
and ultrasonographically guided fine-needle aspira- the chest wall in lung cancer: diagnosis with US.
tion biopsy of impalpable cervical lymph nodes in Radiology 1993;187:39–42.
patients with non-small cell lung cancer. Cancer 1992; 30. Sugama Y, Tamaki S, Kitamura S, et al. Ultrasonog-
70:1111–4. raphic evaluation of pleural and chest wall invasion
15. Yang PC, Luh KT, Chang DB, et al. Value of sonography of lung cancer. Chest 1988;93:275–9.
in determining the nature of pleural effusion: analysis 31. Wang HC, Kuo PH, Liaw YS, et al. Diagnosis of pul-
of 320 cases. AJR Am J Roentgenol 1992;159:29–33. monary arteriovenous malformations by colour Dopp-
16. Gorg C, Restrepo I, Schwerk WB. Sonography of ler ultrasound and amplitude ultrasound angiography.
malignant pleural effusion. Eur Radiol 1997;7:1195–8. Thorax 1998;53:372–6.
17. Chen KY, Liaw YS, Wang HC, et al. Sonographic sep- 32. Yang PC, Luh KT, Chang DB, et al. Ultrasonographic
tation: a useful prognostic indicator of acute tho- evaluation of pulmonary consolidation. Am Rev Respir
racic empyema. J Ultrasound Med 2000;19:837–43. Dis 1992;146:757–62.
18. Eibenberger KL, Dock WI, Ammann ME, et al. 33. Yang PC, Luh KT, Lee YC, et al. Lung abscesses: US
Quantification of pleural effusions: sonography ver- examination and US-guided transthoracic aspira-
sus radiography. Radiology 1994;191:681–4. tion. Radiology 1991;180:171–5.
19. Lorenz J, Borner N, Nikolaus HP. Sonographic vol- 34. Wu HD, Yang PC, Lee LN. Differentiation of lung
umetry of pleural effusions. Ultraschall Med 1988;9: abscess and empyema by ultrasonography. J Formos
212–5. [In German] Med Assoc 1991;90:749–54.
20. Laing FC, Filly RA. Problems in the application of 35. Yang PC, Luh KT, Wu HD, et al. Lung tumors associ-
ultrasonography for the evaluation of pleural opaci- ated with obstructive pneumonitis: US studies.
ties. Radiology 1978;126:211–4. Radiology 1990;174:717–20.
21. Marks WM, Filly RA, Callen PW. Real-time evaluation 36. Liaw YS, Yang PC, Wu ZG, et al. The bacteriology
of pleural lesions: new observations regarding the of obstructive pneumonitis. A prospective study
probability of obtaining free fluid. Radiology 1982; using ultrasound-guided transthoracic needle aspira-
142:163–4. tion. Am J Respir Crit Care Med 1994;149:1648–53.
22. Wu RG, Yuan A, Liaw YS, et al. Image comparison 37. Yang PC. Color Doppler ultrasound of pulmonary
of real-time gray-scale ultrasound and color Doppler consolidation. Eur J Ultrasound 1996;3:169–78.
ultrasound for use in diagnosis of minimal pleural 38. Yuan A, Yang PC, Chang DB. Pulmonary infarction:
effusion. Am J Respir Crit Care Med 1994;150:510–4. use of color Doppler sonography for diagnosis and
assessment of reperfusion of the lung. AJR Am J large-bore cutting biopsy with fine-needle aspiration.
Roentgenol 1993;160:419–20. Cancer 1992;69:2553–60.
39. Yuan A, Yang PC, Chang DB, et al. Lung sequestra- 48. Middleton WD, Teefey SA, Dahiya N. Ultrasound-
tion. Diagnosis with ultrasound and triplex Doppler guided chest biopsies. Ultrasound Q 2006;22:241–52.
technique in an adult. Chest 1992;102:1880–2. 49. Yuan A, Yang PC, Chang DB, et al. Ultrasound-
40. Yu CJ, Yang PC, Chang DB, et al. Evaluation of guided aspiration biopsy of small peripheral pul-
ultrasonically guided biopsies of mediastinal masses. monary nodules. Chest 1992;101:926–30.
Chest 1991;100:399–405. 50. Liao WY, Chen MZ, Chang YL, et al. US-guided
41. Yang PC, Chang DB, Lee YC, et al. Mediastinal transthoracic cutting biopsy for peripheral thoracic
malignancy: ultrasound guided biopsy through the lesions less than 3 cm in diameter. Radiology 2000;
supraclavicular approach. Thorax 1992;47:377–80. 217:685–91.
42. Diacon AH, Brutsche MH, Soler M. Accuracy of pleural 51. Pan JF, Yang PC, Chang DB, et al. Needle aspiration
puncture sites: a prospective comparison of clinical biopsy of malignant lung masses with necrotic cen-
examination with ultrasound. Chest 2003;123:436–41. ters. Improved sensitivity with ultrasonic guidance.
43. Mayo PH, Goltz HR, Tafreshi M, et al. Safety of Chest 1993;103:1452–6.
ultrasound-guided thoracentesis in patients receiving 52. Yang PC, Lee LN, Luh KT, et al. Ultrasonography of
mechanical ventilation. Chest 2004;125:1059–62. Pancoast tumor. Chest 1988;94:124–8.
44. O’Moore PV, Mueller PR, Simeone JF, et al. Sonog- 53. Hung CC, Chen MY, Kuo PH, et al. Ultrasound-
raphic guidance in diagnostic and therapeutic inter- guided percutaneous transthoracic needle aspiration
ventions in the pleural space. AJR Am J Roentgenol biopsy for diagnosis of pulmonary lesions in
1987;149:1–5. advanced HIV infection. J Formos Med Assoc 1999;98:
45. Diacon AH, Theron J, Bolliger CT. Transthoracic 195–200.
ultrasound for the pulmonologist. Curr Opin Pulm 54. Lee LN, Yang PC, Kuo SH, et al. Diagnosis of pul-
Med 2005;11:307–12. monary cryptococcosis by ultrasound guided percu-
46. Yang PC, Chang DB, Yu CJ, et al. Ultrasound-guided taneous aspiration. Thorax 1993;48:75–8.
core biopsy of thoracic tumors. Am Rev Respir Dis 55. Liaw YS, Yang PC, Yu CJ, et al. Direct determination
1992;146:763–7. of cryptococcal antigen in transthoracic needle aspi-
47. Yang PC, Lee YC, Yu CJ, et al. Ultrasonographically rate for diagnosis of pulmonary cryptococcosis. J Clin
guided biopsy of thoracic tumors. A comparison of Microbiol 1995;33:1588–91.