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70 oracic ultrasound
31. Soldati G, Testa A. Anatomia ecografica del torace. In: Manuale di ecografia clinica in urgenza (Testa A,
ed.). Verduci, Roma, 2008, pp. 81-89.
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Respir Dis 1992; 146: 756-762.
33. Miller DL. A review of the ultrasonic bioeffects of microsonation, gas body activation and related cavitation like phenomena. Ultrasound Med Biol 1987; 13: 443-470.
34. Sheiner E, Freeman J, Abramowicz JS. Acoustic output as measured by mechanical and thermal indices
during routine obstetric ultrasonic examnation. J Ultrasuond Med 2005; 24: 1665-1670.
35. Child SZ, Hartman CL, Carstensen EL. Lung damage from exposure to pulsed ultrasound. Ultrasound
Med Biol 1991; 17: 179-188.
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37. Church CC, O’Brien WD. Evaluation of the threshold for lung hemarrhage by diagnostic ultrasound
and a proposed new safety index. Ultrasound Med Biol 2007; 33: 810-818.
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➤ Updated Bibliography
Mead J., Whittenberger JL., Radford EP. Jr. Surface tension as a factor in pulmonary volume-pressure hysteresis. J App Physiol 1957; 10: 191-196.
Escolar JD., Escolar A. Lung hysteresis: a morphological view. Histol Histopathol 2004; 19:159-166.
Escolar JD., Escolar MA., Guzman J., Roques M. Pressure volume curve and alveolar recruitment. A mor-
phometric model of the respiratory cycle. Histol. Histopathol 2002; 17:383-392.
Smaldone GC, Mitzner W, Itoh H. Role of alveolar recruitment in lung inflation: influence on pressure-
volume hysteresis. J Appl Physiol: Repirat Environ Exercise Physiol 1983;55:1321-1332.
ese articles furnish a complete view of the morphometric variations of peripheral air spaces during inflation/
deflation of the lungs. Recruitment and derecruitment of alveolar units could be responsible for the formation of
“acoustic holes” on the lung surface.
Scarpelli EM. e alveolar surface network: a new anatomy and its physiological significance. Anat Rec.
1998;251:491-527.
e description of a bubble model for surfactant distribution inside terminal air spaces.
Woitczak JA, Wood RW. High frequency ultrasound in ex vivo animal lung in pulmonary edema. Journal
of Anesthesiology and Clinical Science 2013;2:21.
Soldati G, Inchingolo R, Smargiassi A, Sher S, Nenna R, Inchingolo CD, Valente S. Ex vivo lung sonography:
morphologic-ultrasound relationship. Ultrasound Med Biol. 2012;38:1169-79.
Contribute to a better knowledge of artifactual production independent from anatomic entities and from deflated
healthy lungs.
4
Semiotics of chest ultrasound
Chest ultrasound is the study of the chest wall with its anatomical planes
made of soft and bone tissue. Moreover, it is a pleural dynamic reflection (a strong acoustic discontinuity). Finally, it is an interpretation of
subpleural artifactual components (the shape of the air). We talk about
lung ultrasound, only in the case of pulmonary consolidations.
➣ Anatomical basis of subpleural ultrasound
Introducing the echographic findings of the chest, we need to specify that “lung ultrasound”,
except for consolidations, is just the study of acoustic interactions of the first 2-3 mm of subpleural lung tissue. erefore, the physician needs to deeply know the lung cortex, as described
above. In this chapter we will briefly resume, from a clinical and practical point of view, the
topics already outlined above in physical and anatomical terms.
Lungs are basically composed of porous functional units, suitable for gas exchange, and of
interstitium. is sort of scaffold has a central (peribronchial and perivascular) component
and a cortical or peripheral (centrilobular) component. e central interstitium upholsters
bronchi and vessels to the hilum and expands peripherally. e cortical interstitium, which has
the greatest interest in thoracic ultrasound, is located immediately beneath the pleura (where
its thickness is about 0.1 mm), extending vertically in the lung parenchyma and constituting
the interlobular septa.
On the surface of the lung, these connective structures, also about 0.1 mm thick, isolate the
smaller functional units that are the secondary pulmonary lobules, with diameter ranging between 1 and 2.5 cm. e pulmonary lobules, represented everywhere in the mantle, are most
visible on the surface of the upper lobes, on the side of the middle lobe and lingula, and on the
diaphragmatic surface of the lower lobes.
(Centrilobular) arteries and bronchi, with a diameter of about 1 mm, are placed at the center of
the lobules, at 5-10 mm from the pleural surface, while pulmonary veins run in the interlobular
septa, at the periphery of secondary lobules.
Each lobule is composed of about 3-24 pulmonary acini, which have afferent (acinar and intralobular) arteries of 0.3-0.5 mm. e acinus, which the terminal bronchiole is connected to,
is formed by 60-120 alveoli.
e internal structures of the lobule are supported by a fine network of connective tissue, called intralobular interstitium, which is anchored on the interlobular septa and on the centrilobular peduncle.
e subpleural lung, which is studied in echography, is a porous tissue (a kind of “dry” foam) at low
density (0.12 g/ml, in the inspiratory phase), characterized by a fine and homogeneous air dispersion in elementary rates, with a mean diameter of 0.25 mm and micrometric walls (the alveoli).
1-4
71
72 oracic ultrasound
➣ Elements of practical ultrasound anatomy
Chest ultrasound reproduces on each hemithorax a succession of layers. Starting from the
surface: the skin, the subcutaneous tissue, the breasts, the superficial fascia, the extraparietal
muscle planes and the intercostal muscles. e chest wall also includes acoustically impermeable structures such as the ribs, which are partially transonic in their cartilaginous part (Fig.
1), the sternum, the shoulder blades, and the vertebrae. Sternum and vertebrae preclude
diagnostic access of ultrasound toward the mediastinum.
RIB
MIRROR EFFECT
Figure 1 – Longitudinal scan of the cartilaginous part of a rib. The rib, which generates the acoustic
shadow, and the mirror effect which consists in the reproduction of the artifactual costal image below the
pleural line, are observed. The cartilaginous portion of the rib does not mask the pleural line.
PLEURAL LINE
Some parietal planes, such as fasciae, are discretely impedant; others, such as bone planes and
the visceral pleura, are strongly reflective.
Among the hypoechoic muscular structures, fascial planes are reflective according to the classic
scheme already studied on the wall of the abdomen5.
e echogenic pleuro-parenchymal line (pleural line)6 is placed down the parietal plane and
the ribs. It marks the peripheral mantle limit of the lung (or pulmonary cortex, constituted
by the secondary pulmonary lobules) (Fig. 2).
SKIN
SUBCUTANEOUS
TISSUE
MUSCLE
ZONE
RIB
PLEURAL LINE
Figure 2 – Echographic representation of anatomical planes of the chest wall.
Semiotics of chest ultrasound 73
As mentioned above, the pulmonary lobules are separated by interlobular septa. e normal
thickness of subpleural interlobular septa is about 100 microns. erefore the so called pleural
line, the pleural mesothelium and the subpleural visceral connection (about 100 microns)
with its septal connections do not normally have such dimensions as to be able to interact,
in an anatomical sense, with the frequencies normally used (between 3 and 15 MHz).
e pleural line, which in echography is not usually resolved into its two parietal and visceral
components, is normally regular. Between the parietal and visceral pleural lines there is the
virtual pleural space, which measures only 0.3-0.4 mm and contains a micrometric plate of
pleural fluid. A chance to see this space is conditioned by the use of very high frequencies
(above 15 MHz)7.
e visceral pleura physiologically slides on the parietal one with a movement called “pleural
sliding” (sliding sign)8 (Clips 1, 2, 3). e pleural movement is synchronous with the expansion of the lung, and thus with the ventilation. In normal subjects it roughly indicates the
volumes of ventilation.
e underlying lung parenchyma, usually filled with air, is replaced by an amorphous image,
with horizontal reflections that are regularly repeated in depth, evenly spaced, as multiplications of the pleural plane, defined A Lines9. As the subpleural level is an artifactual image, it
does not show any anatomical structure. Its background, which emerges between A Lines,
is an artifact due to the machine, and it appears as a faint echogenicity. Especially in young
subjects and subjects with thin walls, fictitious images appear on the lung fields, that represent
the most superficial structures in a “mirror effect”. Alternatively, in the same way, a widespread
background hypoechogenicity may be produced: it must be recognized and judged as non
pathological (Fig. 3).
Pleura
Mirror eect
Figure 3 – Sometimes, depending on the frequency used and the characteristics of the superficial
planes, the lung fields are hypoechoic or they present false structures because of the mirror effect.
Clip 1 – Transverse scan with linear probe. The characteristic movement of
the pleural line, corresponding to the breaths (pleural sliding), and A Lines
are observed.
74 oracic ultrasound
Clip 2 – Longitudinal scan with linear probe. Below the costal plane the
pleural line with its characteristic movement (sliding sign) Is observed.
Clip 3 – Sliding sign at the apex of the lung, where the movements of the
pleural line are less extensive than the basis.
Mirror effects are reflection phenomena, influenced by the angle of insonation. For perfectly
orthogonal insonations, where superficial attenuation is minimal and pleural mirroring is very
high (reflection coefficient > 0.85), the presence of closely overlapping A Lines is frequent.
eir evidence is detected on emphysematous subpleural bubbles and, in general terms, it
could indicate a hyperexpansion of the lung, because of the increase of pleural reflectivity
(called hypermirror) (Fig. 4).
A LINES
Figure 4 – Between A Lines multiple horizontal reverberations are evident (hypermirror phenomenon).
Reverberation echoes decrease in intensity as the distance from the transducer increases,
in relation to the frequency used, so after a few inches an acoustic vacuum appears on the
screen (Fig. 5).
ATTENUATION OF
THE ULTRASOUND BEAM,
AS DEPTH INCREASES
Figure 5 – Attenuation of the ultrasound beam, as depth increases.
Semiotics of chest ultrasound 75
At basal level, intercostal scans do not normally allow the definition of diaphragm, because
of the blocking artifacts of the beam from the aerated lung. What is allowed is the movement
of supradiaphragmatic lung segments, that during inhalation descend in the recesses of the
pleural cavity. is effect is similar to a curtain that obscures the diaphragmatic limit and the
hypochondriacs organs (curtain sign) (Clips 4-5). Full visibility of the diaphragm through the
ribs is then indicative of a supradiaphragmatic acoustic window, which can be an effusion,
an atelectasis or a consolidation (Fig. 6).
PLEURAL EFFUSION
LIVER
DIAPHRAGM
Figure 6 – The presence of a pleural effusion allows excellent visualization of the diaphragm.
Clip 4 – Longitudinal scan at the base of the right lung. It shows the movement
of the lower lung lobe in costophrenic sinus with intermittent partial masking
of the liver (curtain).
Clip 5 – Curtain at the base of left lung.
e transthoracic image of the diaphragmatic region is therefore very different from the
transabdominal view, when liver and spleen act as acoustic windows and allow to identify
curvilinear echoes of the diaphragm with the overlying lung tissue (Fig. 7).
e analysis of the supradiaphragmatic region is very important for thoracic ultrasound,
because when the patient is seated or half seated, it is an area which collects pleural effusions
that at this level eliminate pulmonary artifacts. In this case a view from the top of the diaphragmatic domes and the lung bases detached from the wall is obtained (Fig. 6).
e lung in the pleural fluid can be viewed as an artifact or as a parenchymatous structure
with dispersed air, depending on how much the effusion compresses the parenchyma.
In addition, the pulmonary “curtain” movement allows to determine the perviousness of the
costophrenic sinus and the mobility of the diaphragm.
76 oracic ultrasound
LIVER
DIAPHRAGM
DIAPHRAGM
Figure 7 – A: longitudinal scan at the level of the right last ribs: the diaphragm is evident thanks to
the acoustic window provided by the liver. B: subcostal transverse scan in right hypochondrium: the
diaphragm is evident behind the liver.
In fully cooperative patient, deep inhalations and other maneuvers facilitate the investigation.
For example, the patient can place his ipsilateral upper limb above his head thereby enlarging
the intercostal spaces, or lay his ipsilateral hand on his contralateral shoulder thus raising
the lateral margin of the scapula in order to partially uncover the “blind” retroscapular area.
Finally, the axillary and supraclavicular regions are studied respectively by raising the limb
above the head and turning the head in contralateral direction, using small well-fitting probes.
Cardiac imaging is obtained through classical cardiac parasternal scans, apical scans, subxiphoid and jugular scans. e description of these echographic windows will be addressed in
a separate chapter.
➣ Diaphragm in chest ultrasound
e diaphragm requires a particular description. Not so much for its specific pathology, which
is not discussed here, but for its physiological and pathophysiological correlations with the
ventilatory function, lung volumes and respiratory work. Diaphragmatic abnormalities are
pathophysiologically decisive in many neuromuscular diseases such as amyotrophic lateral
sclerosis, muscular dystrophy, myasthenia gravis and Guillain-Barré syndrome. e determination of the abnormal movement of the diaphragm may also be useful in the definition
of respiratory distress, or of the paradoxical movements that may occur in pathological
conditions characterized by decreased lung compliance or bronchial obstructive disease. e
study of diaphragmatic dynamics is also important to determine the timing for weaning the
patient from the ventilator.
e echographic definition of these situations can avoid, where necessary, the use of fluoroscopy or other radiologic evaluations.
e diaphragm expands the lungs by increasing the volume of the chest cavity through its
inspiratory descent. It is the largest respiratory muscle, contributing to 75% of the ventilation
at rest, when other muscles are not involved. e diaphragmatic “piston-like” movement causes
the lowering of the lung bases and then its activity is responsible of the echographic curtain10.
e techniques traditionally used to diagnose hypomobility of the hemidiaphragms are invasive
or involve ionizing radiations. Other methods produce indirect data or are uncomfortable for
the patient (plethysmography, measurement of transdiaphragmatic pressure, dynamic MRI).
Semiotics of chest ultrasound 77
e lowering of the diaphragm is visible through ascending subcostal, transverse or coronal
ultrasound scans, thanks to the acoustic windows of the liver and spleen, that make it more
easily detectable on the right side11 (Fig. 8).
Figure 8 – Right ascending subcostal scan. The M-mode tracing shows the respiratory movements of
the diaphragm.
e display of hemidiaphragms is often not complete because of the air artifacts in the lungs
and it is better visible on the backside.
Diaphragmatic excursion in normal breathing is 1-2 cm, but it reaches 7-11 cm during forced
respiration12 (Figs. 9 and 10).
Liver
Diaphragm
Figure 9 – Movement of the diaphragm during normal breathing in a healthy subject, explored by
a coronal scan through the liver. The contraction and relaxation of the muscle are made evident by
M-Mode scan and the excursion is 28 mm.
78 oracic ultrasound
Figure 10 – Same scan in the same subject during maximum inhalation and exhalation. The excursion
is 53 mm. At the peak of inhalation artifacts appear, that are related to the interposition of the lung
margin descending into the costophrenic sinus.
Employing a hemicoronal acoustic window with display of diaphragmatic dome and using
M-Mode associated with traditional ultrasound, Kantarci13 showed that the maximum inspiratory lowering here is an average of 49 mm to the right and 50 mm to the left. Females
showed a lowering of about 2-3 mm less. is movement was directly correlated to the body
mass. In this work an underestimation of excursion values (2-6 cm) is clear, compared to
what was previously reported. is may be due to a non perfectly perpendicular impact of
the M-Mode line, which is inevitable in the ultrasound technique used.
In order to avoid this error and standardize the assessment, a method to estimate the movements of the right hemidiaphragm has been recently proposed. is method employs a B-Mode
and subcostal transverse M-Mode scan through the liver, while maintaining the image of the
inferior vena cava to the right and the gallbladder in the center of the screen14. In this scan
the right hemidiaphragm appears as an echogenic curve line with upward concavity and it is
easily samplable with the M-Mode line.
With this method, the diaphragmatic excursions at rest and during forced breaths are respectively 18.4 +/- 7.6 and 78.8 +/- 13.3 mm, without any correlation with demographic and
anthropometric parameters.
Because of the acoustic window, exploration of the left hemidiaphragm is much less feasible.
For this reason, according to this technique, the study of diaphragmatic movements is more
useful in cases of neuromuscular diseases with bilateral engagement.
Procedures for ultrasound exploration of the hemi-diaphragms have also been proposed
according to different principles. A fairly standardized method involves the measurement
of the diaphragmatic thickness, evaluated in a fixed position, at level of the eighth or ninth
intercostal space along the midaxillary line15.
is is the region where the diaphragm touches the rib cage in parallel, in the so-called “zone
of apposition”. Its echographic evidence is clear with appropriate frequency linear probes
(7.5-10 MHz) and this allows accurate measurements of thickness, estimated to an average
of about 2.8 mm during normal breathing (Fig. 11).
During maximum inhalation, thickness increases beyond 4 mm and this increase is correlated
with the shortening of the diaphragm and, significantly, with lung volumes from residual
volume to total lung capacity (Figs. 12 and 13)16.
Semiotics of chest ultrasound 79
Diaphragmatic
apposition
Figure 11 – Coronal scan to visualize the area of diaphragmatic apposition.
Diaphragm
Figure 12 – Thickening of diaphragm in the right zone of apposition. A: normal breathing.
B: maximum inhalation. The increase of muscle thickness from 2.5 to 4.4 mm is evident.
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