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40 oracic ultrasound
Fluid
Consolidated
parenchyma
Only when the pleural fluid interposed
exceeds the size of the axial discrimination
of the exploring frequency, parietal and
visceral pleural interfaces are separated.
is visual gap is produced by impedance
gradients between the wall and the pleural
fluid and between the fluid and the aerated (or non aerated) lung parenchima
(Fig. 11).
➣ Lung cortex
Figure 11 – Small effusion that separates the
visceral from the parietal pleura (arrows). The
subpleural lung parenchyma is consolidated. 10
MHz linear probe.
In the next pages we will use the term
“cortex” to indicate the subpleural lung
that, in the absence of a full consolidation with complete deaeration, produces
artifactual images. “Lung cortex” is the
most peripheral, superficial volume of the organ, with functional capability for gas exchange.
Anatomically the cortex represents a thickness of about 2 cm. It is anatomically identified in
the distal airways beyond the terminal bronchioles, i.e. beyond the 15 bronchial generation
(the so-called transitional bronchioles)1 (Fig. 12).
Trachea
Bronchial tubes
Bronchioles
Terminal
bronchioles
Transitional
bronchioles
Respiratory
bronchioles
Conducting
airways
Acinar
airways
Alveolar
ducts
Alveolar
sacs
Figure 12 – Subdivisions of the human respiratory tree, with their respective levels. Distally, airways
decrease their diameter, but increase in number, until, peripherally, the gas exchanging surface increases
enormously.
Anatomy of chest ultrasound 41
In normal lungs, cortical air spaces are prevailing and interstitium is thin. It can be classified as
interlobular interstitium, with a maximum thickness of 100 microns, intralobular interstitium
and interalveolar septa (with thickness of a few microns). Associated with the alveolar interstitium
is the vascular bed, fed by the centrilobular arteries, whose essential constituent is the capillary
network of the alveolar walls2. e venous and lymphatic vessels are located in the perilobular
interstitium. Anatomically and functionally the cortical respiratory airways (acinar airways)
feed alveolar spaces and are named respiratory bronchioles, alveolar ducts and alveolar sacs3.
To understand the role of ultrasound in pulmonary diseases, it is appropriate to consider the
superficial anatomy of the lung in terms of spatial and physical properties. e spatial properties are the dimensional and connective characteristics of subpleural airspaces and interstice.
ese parameters can simply be represented as linear or planimetric dimensions, and through
the ratio between “full” and “empty” tissue. e physical properties refer to the “roughness” of
the superficial pleural plane able to generate acoustic backscatter but not specular reflection.
Superficial lung parenchyma can be represented as a dynamic foam that periodically inflates
and deflates. At this level, about 30,000 terminal bronchioles nourish the pulmonary acini,
functionally identifying the greater unity of the airways (terminal respiratory unit) (Fig. 13).
Acinus
Terminal
bronchioles
Acinus
Respiratory
bronchioles
Figure 13 – The periphery of the respiratory tree consists of the pulmonary acini (terminal respiratory
unit). 3-24 acini constitute the secondary pulmonary lobule.
From another point of view, the association of 24 acini anatomically identify the morphological superficial unit of the lungs, which is the secondary pulmonary lobule, clearly demarcated
by interlobular septa, and with linear dimensions of about 1-2.5 cm4 on the pleura (Fig. 14).
A pleural/subpleural scan plane interacts with pulmonary acini, grouped (discretized) in
secondary lobules, separated by the thickest peripheral interstitium of the organ (interlobular
septa, about 100 microns).
To identify a prevalent geometry of the normal cortex, it must be considered that airways
have a luminal diameter decreasing as the generations increase toward the periphery5, but the
overall surface of section greatly increases.
42 oracic ultrasound
From the morphometric point of view the terminal bronchioles show an internal diameter
ranging between 1 mm and 300 microns while acini have an average volume of 0.187 ml.
Respiratory bronchioles, alveolar sacs and ducts shows diameters between 500 and 270
microns. Finally alveoli are on average 250 microns and they form a honeycomb structure
almost space filling, with extremely low density (<0.1 g/ml)
6,7
, but with a gas exchanging
surface of about 104 cm2.
Interlobular
septum
Centrilobular
bronchial tube
Centrilobular
artery
Acinus
Pulmonary vein
Interlobular
septum
Figure 14 – Schematic representation of the pulmonary lobule. Pulmonary lobules are separated by
interlobular septa which contain the pulmonary veins. The afferent arteries and bronchi are centrally
located.
In contrast with the common sense, the alveolar periphery of the pulmonary acini, rather than
as a geometry similar to “grapes”, is represented with more accuracy as a dry foam, in which
the alveolar faces (extremely thin) are flattened (hexagonal or pentagonal), while the individual
alveoli have a polyhedral shape8.
During a physiological respiratory cycle, this three-dimensional “tessellation” possesses walls
with dimensions, varying according to physiological lung volumes, between few microns and
20-30 microns. is geometry is incorporated in a three-dimensional “tessellation” of a higher
level, represented by secondary pulmonary lobules whose “walls” (interlobular septa) reach 100
microns9. For physical reasons (see below), a foamy tissue with these dimensions, can not be represented by the frequencies of normal use in ultrasound (up to 20 MHz). e healthy lung cortex,
therefore, has no anatomical evidence to the ultrasound and behaves as a near specular reflector.
➣ Geometry/topology of the lung cortex and lung acoustics
Most of the technical considerations expressed in the previous paragraph and in this one are
derived from a series of physical studies that have not had proper attention. Nevertheless it is
useful to discuss about this, in order to understand the physical basis underlying the production
and interpretation of ultrasound images of the normal and pathologic lung.
e lung cortex can be thought as a three-dimensional space (volume), but CT and ultrasound,
for their cross sectional characteristics, explore this space in two-dimensions terms.
Anatomy of chest ultrasound 43
A two-dimensional modeling of the lung cortex can be achieved with various modes and has
already been implemented. We cite for example the method of Voronoi10, applied to the lung
by Burrowes11, the final result of which, relatively to the acinar spaces of the lung, is represented
in Figure 15, since it is very intuitive and explanatory12.
Pulmonary lobule
Pulmonary acinus
Respiratory bronchioles/alveolar ducts
Interlobular septum
Figure 15 – Modelling of the lung cortex according to the method of Voronoi. The peripheral hexagonal
cells represent the alveoli. The system of respiratory bronchioles/alveolar ducts creates an interconnection
through all the distal spaces (acinar units), grouped in the secondary lobules and separated from each
other by interlobular septa (the largest subpleural connective interstitial afferents).
Pulmonary lobule
Pulmonary acinus
If we model this planar representation into a three-dimensional volume, we get a kind of
sponge with full and empty (of air) components. Progressively limiting the volume of the
solid part of the sponge, it tends more and more to resemble a foam, whose boundary is just
a dry foam (Fig. 16).
Respiratory
bronchiole
Alveolar duct
Figure 16 – Scanning microscopic image (190 X) of normal lung parenchyma (pulmonary acinus). The
high porosity of the tissue determines a low specific weight (like a dry foam).
44 oracic ultrasound
A foam and a sponge (with closed spaces) are similar because constituted by an air component distributed in cells and a solid component. rough compressions or distensions, the
aerial part can be variable (in inverse relation to the solid one). is variability explains the
characteristics of the foams, in particular it separates a dry foam (less dense) from a wet foam
(more dense). If a porous tissue is constricted or dilated, without obliterating the empty
spaces, it still remain a sponge (or a foams), but with different density. In simple terms these
are the concepts of geometry and topology to be applied to the normal, deflated or inflated,
or pathological lung.
In lung sonography the interaction of the ultrasound beam faces these characteristics. Within
certain limits related to the frequencies used, when the lung is comparable to a dry foam
(Fig. 16) it behaves in a way, when it is more like a wet foam, in a different way (Fig. 17),
finally, when the cavities are substantially obliterated it behaves differently.
In Figure 15, the thick vertical line represents an interlobular septum located between two
adjacent secondary lobules. e thin vertical line exemplifies the border between two acini,
and is therefore an intralobular septum. If the septa represented, are below a certain size
threshold in relation to the frequencies used, they are irrelevant.
Such a subpleural two-dimensional space, explored by echography, is therefore characterized by its own geometry and topology, which are measureable
13,14
and comparable with the
exploring frequencies.
In the actual lung the behavior is obviously much more complex (Table 3), because the ge-
ometry of the air spaces can vary with breathing. During the physiological respiratory cycle,
the sponge-like configuration (Table 4) remains relatively preserved, as simple continuous
plastic strains, do not alter the topology of an object, in spite of its geometric variations.
However, in cases of marked deflation the lung behaves as an anisotropic sponge, and express
sequential closing of peripheral air spaces (derecruitment). erefore an health but unphysiologically deflated lung behaves as a pathologic lung.
Table 3 – Normal pulmonary geometry
Tree with 23 dichotomous generations
The conducting portion includes generations 0-16
The respiratory portion is divided into 30,000 acini, including 3 x 108 alveoli
The diameter of the branches decreases progressively with the generations
The total area of the section increases progressively with the subdivision generations
The length / diameter ratio is > 3 in the totality of generations
Average size of the subpleural air spaces 250 microns
Thickness interalveolar septa 8-20 microns
Thickness interlobular septa 50-100 microns
Modified from: Mauroy B, Filoche M, Andrade JS, Sapoval B. Interplay between geometry and flow
distribution in an airway tree.
Phys Rev Lett
2003; 90.
e passage of the lung cortex from normal to pathological, is characterized by different
aspects depending on whether one considers the interstitial lung disease rather than alveolar
syndomes, or destructive patterns (emphysema).
Anatomy of chest ultrasound 45
In interstitial pathologies, the cortical geometry always changes and this is expressed by
variations of weight/volume relationships. e organ’s density complaints the dimensional
changes of the septa (enlarged) and air spaces (collapsed).
In pure interstitial diseases, from a physical point of view, the lung resembles a strongly
deflated organ where numerous derecruited peripheral air spaces are present. If the lung is
a foam, in interstitial disease the foam is wet or, in other words, the lung is a more dense
sponge (Figs. 17 and 18).
In consolidating pathologies emerging on the pleura, the ultrasound interact with permissive
holes along a more or less specular plane. e effect is related to the size of consolidations in
relationship with the insonanting wavelenght. If the consolidation is very large compared to
the wavelenght, it is represented as a solid tissue. erefore a consolidation is a real picture.
In conclusion, lung ultrasound interprets changes of the physical properties of the pleural
reflector in terms of variable compositions of full and empty spaces (Fig. 19).
Respiratory
bronchiole
Alveolar duct
Figure 17 – Structurally the peripheral lung is a spongy tissue (A: anatomical image of lung 190X), that
in the modeling, can be assimilated to a variously contiguous set of air bubbles (a more or less hydrated
foam) (B). The white arrows indicate the “interstitium” of a wet foam.
Figure 18 – A layer of air microbubbles in a fluid assuming a wet configuration (left) is physically and
topologically similar to a lung with interstitial disease (diffuse alveolar damage, right), and as such it
loses its ability of specular reflection producing vertical artifacts.
46 oracic ultrasound
Figure 19 – Schematic representation of the ultrasonic interactions on two-dimensionally modeled
patterns as full (black) and empty (white). A: normal lung pattern and massive reflection. B: total
consolidation and massive permeability. F and G: full/empty geometries capable of producing B Lines.
The arrows indicate acoustic microholes. Pattern H is physically equivalent to A (Modified from Soldati
G
et al. UMB
2011).
Table 4 – Pulmonary topology
The modeling of the lung cortex can be assimilated to a foam-like space (wet or dry).
The sectional (tomographic) feature of ultrasound on subpleural space allows a twodimensional modeling.
However carried out, modeling can be studied in terms of full/empty.
The distribution on a (two-dimensional) plane of full and empties affects the production of
ultrasound images.
Artifactual images (B Lines and white lung) are relevant to a topological homeomorphism with
normal lung, i.e. the foam-like pattern, even if dimensionally (geometrically) varied, must be
present.
“Tissue” images are produced by structural (not homeomorphic) changes and lost (obliteration)
of empties.
The frequency used probably defines the “scale” of visibility of acoustic phenomena.
Anatomy of chest ultrasound 47
➤ Recommended readings
Block B. Colour atlas of ultrasound anatomy. ieme, Stuttgart-New York, 2004.
Crystal RG, West JB, Weibel ER, Barnes PJ. e lung: scientific foundations. Lippincott-Raven, Philadelphia,
1997.
Hartwig WC. Fundamental anatomy. Lippincott Wlliam & Wilkins, Philadelphia, 2008.
Hutzler S, Weaire D. Physics of foams. Oxford University Press, Oxford, 1999.
Sapoval B, Filoche M, Weibel ER. In: Branching in nature (Fleury V, Gouyet JF, Leonetti M, eds.). ED
Science, Paris, 2001.
Weibel ER. Morphometry of the human lung. Academic Press, New York, 1963.
Weibel ER. e pathway for oxygen. Harvard Univ. Press, Cambridge, 1984.
➤ Bibliography
1. Berend N, Rynell AC, Ward HE. Structure of a human pulmonary acinus. orax 1991; 46: 117-121.
2. Tawhai M, Burrowes KS, Hoffman EA. Computational models of structure function relationship in the
pulmonary circulation and their validation. Exp Physiol 2006; 91: 285-293.
3. Haefeli Bleuer B, Weibel ER. Morphometry of the human pulmonary acinus. Anat Rec 1988; 220: 401-414.
4. Hansen JE, Ampaya EP. Human air space shape, sizes, areas and volumes. J Appl Physiol 1975; 38: 990-995.
5. Tawhai M, Burrowes KS. Developing integrative computational models of pulmonary structure. Anat Rec
(Part B: New Anat) 2003; 275B: 207-218.
6. Kitaoka H, Tamura S, Takaki R. A three dimensional model of the human pulmonary acinus. J Appl
Physiol 2000; 88: 2260-2268.
7. Weibel ER. How to make an alveolus. Eur Respir J 2008; 31: 483-485.
8. Grebenkow DS, Guillot G, Sapoval B. Restricted diffusion in a model acinar labyrinth by NMR: eoretical
and numerical results. J Magnetic Res 2006; 184: 143-156.
9. Leeming A, Schroter R. A model morphology of the pulmonary acinus. Proc Inst Mech Eng 2008; 222:
429-437.
10. Voronoi G. Nouvelles applications des paramètres continus à la théorie des formes quadratiques. Journal
für die Reine und Angewandte Mathematik 1908; 133: 97-178.
11. Burrowes KS, Tawhai MH, Hunter PJ. Modeling RBC and neutrophil distribution through an anatomically based pulmonary capillary network. Ann Biomed Eng 2004; 32, 585-595.
12. Denny E, Schroter RC. A mathematical model for the morphology of the pulmonary acinus. J Biomech
Eng 1996; 118: 210-215.
13. Michielsen K, De Raedt H. Integral geometry morphological image analysis. Physics Reports 2001; 347:
461-538.
14. Quilliet C, Ataei Talebi S, Rabaud D et al. Topological and geometric disorders correlate robustly in two
dimensional foams. Philos Mag Lett 2008; 88: 651-660.
3
Physics of chest ultrasound
➣ Introduction
In this discussion, we will not explore the physics of ultrasound present in dedicated textbooks
and already treated. Moreover, those who use chest ultrasound probably know at least the
basics of general sonography and its physics. In this chapter we will highlight some concepts
related to the ultrasound interaction with tissues containing variable air volume, important
for the study of lungs.
Many planes interact with ultrasound during a chest scan. ese structures are impedant
interfaces with variable dimensions acting as reflectors (more or less specular) or scatterers.
eir effects can be simply summarized in reflections, reverberations (defined as multiple
repetitive reflections within a critical volume), backscattering, wave interferences and acoustic
shadowing/enhancement. eir importance lies in the fact that they are at the base of the
artifactual component of the lung1.
When speaking about “artifacts”, it is important to understand some concepts. In ultrasound
imaging terminology, an artifact is an error of perception or representation of an acoustic
information, introduced by the equipment and induced by interaction phenomena between
energy and tissue2. In practical terms, it is the interpretation of a signal from the ultrasound
machine, not represented in terms of real anatomy. Consequently, the common sense would
indicate lung artifactual images as electronic wrong acquisitions.
However, it is necessary to recognize that in physical sense and according to the information
processing of the machine, lung artifacts (A Lines, B Lines and white lung) are real radiofrequency signals, which identify real interactions and/or interference between acoustic waves
and tissue structures explored. erefore, the visual representation of lung artifacts is only
a surrogate of a real message coming back from the geometry of a frothy substrate. For an
optimal lung sonography this message must be decrypted.
With this background in mind, we recognize normal (or physiological) artifactual component
in the subpleural plane, represented by the repetitive horizontal images, called transducer
reverberations or A lines (Fig. 1). In certain pathologies the normal pattern changes, and an
artifactual component, consisting of vertical images appears. ese B Lines are arranged with
a variable density (number/cm) along the pleural plane until their coalescence. Otherwise,
the subpleural field changes from horizontal reverberations (A Lines) to a diffuse echogenicity
erasing A Lines (white lung)
When the ultrasound passes through different contiguous “tissues”, with a “stiffness” or a
significant resistance to molecular motion (tissue density), characteristically bright interfaces
(echoic)6 are observed.
An intercostal scan is a superposition of layers of tissue (subcutaneous tissue, muscle, pleural
plane) separated by echogenic surfaces, represented by the interfaces of the fascial planes and
3-5
(Figs. 2, 3).
49
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