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120 oracic ultrasound
Pulmonary consolidation
Complex pleural liquid
Figure 17 – Complex non areolar effusion.
FIBRIN
cavity
Figure 18 – Areolar effusion.
HOMOGENEOUSLY ECHOGENIC
Figure 19 – Homogeneously echogenic effusion.
EFFUSION
Pathology of the pleura 121
Homogeneously echogenic collections can be seen typically in case of hemothorax or empyema.
Empyema and neoplastic effusions often appears as complex areolar effusion.
Ultrasound examination also allows an estimate of the volume of the effusion with higher
accuracy than clinical and radiological methods. In practical terms, an ultrasound volumetric
estimate is much more accurate and convenient than a traditional radiological estimation
29,30
Certainly, the highest accuracy is possible with the planimetric determination of the area occupied by the effusion in serial transverse and longitudinal sections, with the mathematical
reconstruction of the volume31.
However, accuracy goes to the detriment of practicality. Some correlations were obtained
between the thickness of the fluid collection at the base, at the apex and in different phases of
respiration and its volume. Goecke and his co-workers32 proposed two simple semiquantitative
methods to estimate the volume of effusions. e first one considers the retroparietal lateral
height of the pleural effusion in centimeters that is multiplied by the empirical value of 90.
e other one considers the maximum subpulmonary height in centimeters, added with the
retroparietal lateral height of the pleural effusion in centimeters. e value obtained is then
multiplied by the constant value of 70, obtaining an estimate of the volume in milliliters.
A more rapid and practical method divides the volume of pleural effusion in classes. e effusion is minimal if it is visible only in the costophrenic sinus (few ml). It is small when it is
fully seen in just one ultrasound convex scan. It is moderate, if two ultrasound convex scans
are needed to see it totally (500-1500 ml). Finally, the effusion is massive if the transonic
space occupies more than two ultrasound scans (> 1500 ml).
We prefer a volumetric division into classes, because, for therapeutic purposes, we believe the
completeness of the patient with his ventilatory dysfunction is more important than a precise
pleural volume, which is anyway always imperfect.
From a functional point of view, an approach taking into account the extension of lobar
compression and the hilar visibility (typical of large or massive effusions), is more important
than a crude estimate of the volume (Table 2).
Table 2 – Grading of pleural effusions
.
Grading Description Landmarks Intercostal spaces
1: Minimum Limited to costophrenic sinus Diaphragmatic dome
partially evident
2: Small Lower lung lobe partially
Involved
3: Small to
medium
4: Medium Lower lung lobe completely
5: Large Upper lung lobe partially
6: Massive Fully collapsed lung Atelectasis of the
Lower lung lobe partially
collapsed
collapsed
involved
Diaphragmatic dome
completely evident
Lower lung lobe
partially atelectatic.
Hilum not visible
Atelectasis of the
lower lung lobe
Hilum visible
Atelectasis of the
lower lung lobe
Upper lung lobe
partially atelectatic
whole lung
Effusion limited to
costophrenic sinus
1 intercostal space
2-3 intercostal spaces
3-4 intercostal spaces
4 or more intercostal
spaces
Hilum completely
visible
122 oracic ultrasound
In the presence of extensive chest opacity detected by radiography (X-ray white hemythorax),
ultrasound plays a key role where the use of X-rays cannot distinguish what is parenchymal
and what really belongs to the pleura (Figs. 20-22-23).
Table 3 lists the most common causes of X-ray white hemithorax.
Table 3 – Causes of white hemithorax by chest X-ray
Pleural effusion
Massive consolidation
Atelectasis
Massive tumor
Fibrothorax
Combinations of these lesions
Pneumonectomy
Pulmonary agenesis
Figure 20 – Chest X-ray: opacity in the right lower field.
PLEURAL EMPYEMA
Figure 21 – The ultrasound examination clarifies the nature of the radiographic finding: pleural
empyema.
Pathology of the pleura 123
PNEUMONIA
AIR BRONCHOGRAMS
Figure 22 – Chest X-ray very similar to the case of Figure 20. In this situation, however, the radiological
opacity is due to a lobar pneumonia.
Figure 23 – The causes of white hemythorax on chest X-ray (A), can be quickly identified by
ultrasonographic examination: B, massive pleural effusion; C, massive pulmonary consolidation.
Yu and his co-workers
33,34
showed that, compared with the findings of CT, the diagnostic
sensitivity of ultrasonography is around 95% for pleural disease, 83% for pulmonary consolidations and only 30% for mediastinal lesions.
e traditional chest X-ray is much less accurate. It is estimated that for small effusions
(<200 ml), the sensitivity of chest X-ray does not exceed 30%, while for effusions > 500 ml
sensitivity is up to about 80%, only with an appropriate radiological technique. e weakness of traditional chest radiography is significant for estimating pulmonary compressive
atelectasis, with maximum sensitivity of 13%.
e ultrasound images must nevertheless be interpreted in the clinical context according to
the principles of clinic ultrasound. For example, the presence of an inflammatory picture may
direct towards an inflammatory or septic nature of the effusion. Moreover, the evaluation of
the pleural fluid “echostructure” integrates with the diagnostic hypothesis. We have already
described empyema and neoplastic effusions in terms of areolar effusion35.
Dyspnea associated with sign of pulmonary imbibition (see below) and with transonic pleural
effusion only detectable by ultrasound, suggests heart failure.
124 oracic ultrasound
Dyspnea or hyperpnea without pathologic parenchimal signs or significant pleural images
can suggest a pulmonary embolism. An effusion with a well-defined pulmonary consolidation
suggests a parapneumonic or a neoplastic effusion.
➣ Pleural effusions in critically ill patients
36
Pleural effusions in ICU require a particular attention for a variety of reasons:
• Although they are a rare cause of access to ICU, they complicate the pathological process
of these patients in a significant proportion of cases.
• Pleural diseases are underestimated by clinical examination and chest X-ray in ICU.
• e ultrasound is applied more and more frequently in ICU, because it is very accurate
for pleural diseases.
• An ultrasound of the pleural cavity is performed on patients in the supine position with
many devices and medications on the chest, so the usual technique may not be optimal.
e reasons why a patient in ICU may show pleural effusion are many, primitively pulmonary
or due to systemic or cardiac disease37.
Atelectasis is a common reason for pleural effusion and heart failure is the most frequent cause.
Hydrothorax is detected in 6% of patients with cirrhosis and ascites and effusion is diagnosed in
3-17% of cases of acute pancreatitis. Parapneumonic effusion38 is common and frequently evolves
into empyema, which requires timely drainage. In the case of an apparently primitive pleural
effusion, pulmonary embolism should be the first hypothesis, because an effusion complicates
pulmonary embolism in 30-40% of cases. Finally, unusual and rare causes must be taken into
consideration, such as the esophageal perforation (Boerhaave syndrome), in which early diagnosis
is a key prognostic factor.
From an echographic point of view, these effusions occur with the instrumental signs already
described. e supine position makes it more complicated to estimate the size of a pleural effusion, which tends to align along the dorsal costovertebral areas. erefore coronal scans over
the diaphragm tend to show only major effusions (> 200-300 ml). For optimal viewing of small
effusions and their compression effects on the lung parenchyma, it is necessary to slightly lift
the patient from the side that is explored, and direct the probe as back and upward as possible.
➣ Pleurisy
Pleurisy is frequently caused by viral diseases and is diagnosed on clinical criteria, as it is rarely
accompanied by specific laboratory data or typical imaging. Pleural inflammation produces
a typical pain39 and often fluid collections not detected by X-ray. Small effusions are clearly
visible on ultrasound. Sometimes it is possible to see fibrin branches inside the fluid. In
pleurisy, ultrasound may show an irregular pleural surface, interruptions of the pleural line
(89%) and marked flat or convolutes pleural thickenings (64%).
A pleural thickening is distinguished from an effusion because it participates in “coming
and going” movements associated with breaths (Clip 10). Otherwise a thickening shows
hyperperfusion signals in color or power Doppler.
Clip 10 – Tiny circumscribed pleural effusion (longitudinal extension about
1 cm). The visceral pleura flows below the anechoic area that remains fixed.
This finding excludes pleural thickening.
Pathology of the pleura 125
Many times in pleurisy, millimeter-sized subpleural consolidations are evident, scanning the
pleural surface with small parts probe.
Gehmacher and co-workers40 reported that ultrasound abnormalities can be detected in
91% of cases of pleurisy, in patients whose chest X-rays had not shown significant images
(Figs. 24-26).
Figure 24 – Thickening of the parietal pleura (arrows). Pleural plaques differ from effusions because they
maintain the same morphology during respiration, while the pleura (if not adherent) is flowing below.
Figure 25 – Patient with right parasternal pleuritic pain. Not significant X-ray (a). Ultrasound
examination (b, c, d) shows focal interstitial syndrome immediately above the diaphragm in the right
parasternal position. Irregular and fragmented pleura. The remaining lung fields are normal (e). Viral
pleurisy. No pleural effusion is observed.
126 oracic ultrasound
It is important to remember that about 20% of hypo-anechoic pleural lesions do not contain
free liquid, but represent pleural thickening. Marks and his co-workers41 have shown that if
hypoechoic or anechoic pleural lesions vary in size or shape, or if they contain mobile debris, it
is likely that they contain fluid that can be suctioned. In fact, on ultrasound a localized liquid
lesion may appear as a solid. ese doubtful aspects can be better specified with the use of
ultrasound contrast agents, which of course do not lead to enhancement in fluid collections.
Figure 26 – To the left, CT imaging of small parietal pleural thickening. To the right, ultrasound image.
In uncertain cases, Color Doppler imaging may also be useful. In pleural thickening there is no
evidence of the so-called fluid color sign, which is always present in the fluid collections and is
generated by the movement of the fluid in relation to the respiratory activity42 (Clips 11-12).
Clips 11, 12 – Color Doppler detects the movements of pleural fluid during
the respiratory phases (fluid color sign). This sign is useful to distinguish
effusions from pleural thickening.
➣ Fibrosis and pleural thickening
43
Pleural fibrosis has multiple etiologies. It is the result of primitive pleural diseases and/or the
complication of lung or pleural inflammations. In most cases, fibrosis is patchy or localized,
less frequently it is spread out. e most common cause of localized pleural fibrosis is fibrinous or purulent pleurisy. e localization of this disease is mainly basal.
Edema, and the subsequent collagenization of the pleura, may be seen on ultrasound, especially
if associated with effusion. It appears as a diffuse, circumscribed, band, convoluted, nodular,
irregular, hypoechoic or structured serous thickening. e costophrenic sinus is typically occluded, and consequently the lung curtain and the detachment of the diaphragmatic zone of
apposition are missing. Pleural thickening can be traced along the lateral and posterior chest
walls up to variable height. It is not possible, only with morphological findings, to establish
the etiology of a pleural thickening. e evolution of the disease may be indicative. In cases
Pathology of the pleura 127
of reversible inflammatory etiology, these issues are resolved with therapy. is does not occur,
or occurs slowly or partly, in the case of fibrotic or productive lesions.
Pleural plaques are circumscribed foci of dense fibrous tissue affecting the parietal pleura.
Frequently, their etiology is linked to the inhalation of asbestos44 and their seat is usually
bilateral in the axillary region (VII or VIII rib). Not calcified plaques resemble post-infection
fibrosis. ey appear as immobile hypoechoic smooth or convoluted thickening, and do
not implicate apices and costophrenic angles. e plaques from asbestosis are calcified in a
percentage between 20% and 50% and appear as echogenic lesions with posterior acoustic
shadow, in some cases affecting completely the lower pleural regions (Fig. 27).
Figure 27 – Irregular solid plaque adherent to the surface of the right hemidiaphragm, with a calcified
focus (arrow). To the left, CT image, to the right, ultrasound image. Concomitant pleural effusion.
Fibrothorax (diffuse pleural thickening) has infectious etiology (especially tuberculosis),
but may be the result of a hemothorax, or it may be associated with collagen diseases and
asbestosis. In these cases there is a pleural rind, typically less than 1 cm thick, well evident
in ultrasound. Unilaterality supports the infectious or traumatic hypothesis (hemothorax),
bilaterality the asbestosis hypothesis. Extensive calcifications are more typical for pleural
empyema, tuberculous disease and hemothorax.
Sometimes focal lesions with various echogenicity, thicker than 3 mm, with or without irregular
margins, are detected incidentally. ey are due to pleurisy, empyema, tumors, hemothorax
or iatrogenic pleurodesis. Hypoechoic foci, as in pleurisy with rich exudate, often acquire
echogenicity becoming, in some cases, calcified.
From the practical point of view, it is important to differentiate hypoechoic thickening of the
pleura from small fluid collections and lung atelectasis, as these are drainable with thoracentesis. In the case of solid pleural lesions, ultrasonography can adequately address the biopsy. In
doubtful cases, the pleural lesions can be evaluated with contrast agents (contrast enhanced
sonography, CEUS), which enhance their microcirculation after about 18-20 seconds45.
➣ Pleural tumors
A brief discussion of the sonographic appearance of pleural tumors is important, because these
lesions may occur with not well defined radiographic opacity. Undoubtedly, this problem is
solved in most cases with a simple ultrasound examination46.
128 oracic ultrasound
In addition, the ultrasound visibility of a nodularity, a thickening or a pleural mass, especially
with effusion, makes an estimation easy in terms of size, echostrucure and vascularization,
including the enhancement patterns with CEUS.
We distinguish benign and malignant primary tumors, and metastatic pleural tumors.
Pleural metastases generally originate from breast or bronchial neoplasms. ey are frequently
multiple, located at the level of the costal pleura, the costophrenic sinus and on the diaphragmatic surface. ey have a low echogenicity and variable dimensions. Variable is their
tendency to invade adjacent structures (lung or chest wall).
eir shape is usually nodular or polypoid. More rarely it appears plaque-like and it is easily
defined by the coexistence of pleural effusion47 (Clip 13). e metastatic symphysis between
the visceral and parietal pleura abolishes the pleural sliding.
Clip 13 – Pleural metastases from breast cancer. The polypoid lesion is
adherent to the diaphragmatic pleura. Coexisting pleural effusion.
Benign tumors of the pleura are rare (lipomas, schwannomas, chondromas), representing
only 5% of pleural tumors. ey are moderately echogenic well demarcated lesions, and
are obviously not infiltrative. e presence of calcified foci and adipose echostructure may
indicate benignity. e vascular pattern, unlike malignant lesions, is scarce and/or ordered,
with prolonged ultrasound contrast uptake and absence of washout48.
e most frequent malignant tumor of the pleura is mesothelioma49. Although relatively rare,
its frequency is increasing. Many of these cancers are related to asbestos exposure.
Mesothelioma appears as a plaque-like (28%) or lobulated (72%) thickening that involves a
portion or even the entire lung, showing an infiltrative tendency towards the fissures and the
chest wall. From the radiological point of view, it produces a unilateral pleural thickening
with a plaque-like or lobulated tendency50.
Differently from benign pleural plaques, usually smooth, the appearance of mesothelioma
is irregular, with angular and infiltrating edges. e echogenicity of the lesions is low and
sometimes has to be differentiated from concomitant effusions. e growth on the parietal
pleura, in the absence of pleural fluid, is documented by the underlying lung that slides on the
lesion. is sliding is abolished when the tumor invades the visceral pleura. e visualization
of neoplastic, hypoechoic tissue with spiculated or token-like shape, confirms the invasion
in the parietal planes of the chest.
e effusion appearing with the mesothelioma can be relatively transonic, fibrinous, or corpuscular in the case of the presence of blood.
e diagnostic accuracy of ultrasonography for malignant tumors of the pleura is similar to
that of CT. Ultrasound allows easy real time transparietal biopsies of pleural lesions.
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