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60 oracic ultrasound
A
C
B
D
Figure 13 – Dense B Lines and white lung may appear in ultrasound scans on lung tissue, with less air content, and not just in lung tissue with anatomical interstitial disease. Rabbit lung (NZ White, 3 kg). A: anatomical image of collapsed areas (arrows). The normal lung (pink) is normally expanded (B). The histology of the collapsed regions (C) shows no abnormalities in interstitium, these are simply less aerated. Ultrasound scans of these regions show a sonographic interstitial syndrome (D).
A
B
C
D
Figure 14 – Correlations between macroscopic, microscopic anatomy and lung ultrasound. Rabbit lung (NZ White, around 3 kg). Macroscopic image of a not fully expanded surface area of the right lung subjected to positive pressure (A, arrow). This area is constituted by a compact region of consolidation (contusion) (B) and by hypoexpanded contiguous regions (D). The ex vivo echographic exploration (C) shows the injury (arrow) as a micro-consolidation inside an area of white lung.
Physics of chest ultrasound 61
Figure 15 shows very schematically, how density variations of the lung, at immediate subpleural level, affect the production of images in lung ultrasound.
air tissue
D: lung density cortical (g/ml)
Figure 15 – Relationships between lung density, lung air content and artifactual (preconsolidation) and real (consolidation) images produced by ultrasound.
Normal S. Interstial White lung Densication Atelectasis
Origin of B Lines and white lung
B Lines are visually similar to ring-down artifacts26. ese images were described in details by Avruch and Cooperberg in 198520 in bubble systems within a liquid. In this experimental setting, when the bubble geometry assumes a tetrahedral arrangement, in the core of the tetrahedron a fluid structure (defined bugle) is isolated. According to the hypothesis of the authors, the “bugle” is able to “resonate” in response to an ultrasonic pulse. e reception by the transducer of the vibrational response was considered at the base of the signal represented on the screen. is hy­pothesis, widely accepted but never seriously verified, distinguishes the ring-down from the comet tail artifact, as the latter, typically elicited in crystal structures27, would be originated by a different mechanism, i.e. reverberation. is distinction appears in almost all textbooks on echography.
e uncertain terminology used to define vertical artifacts (ring down, comet tails, ultrasound lung comets) is already enough to understand that clarity in this area has never been done. In addition, the experiences on humans and animals are quite different from experiments in vitro.
Probably the greatest gap of knowledge in this field stems from the fact that the visual exami­nation of artifacts is a “poor” substitute for a serious analysis of the radio-frequency response of living tissues or materials explored with echography. Usually we do not know the real type and frequency of the wave emitted to explore nor space/time/frequency that the transducers receive. Simply, this analysis does not exist.
In theory, aerated and non specular living tissues can respond to an ultrasonic insonation carried out with frequencies (and machines) commonly used19 through many phenomena. Experiences on fluids and foods demonstrated that a known and tuned ultrasound could analyze a corpuscolated fluid or discriminate the “roughness of a surface”. However in a living tissue this is actually possible only on an experimental setting. e key for interpreting the information received by the transducers lies in the accurate knowledge of some fundamental phenomena as scattering, wave interference, repetitive reflections and so on. is is not pos­sible with the commercial ultrasound instruments.
62 oracic ultrasound
In normal deflated lung, the explanation for the genesis of B Lines and white lung is compat­ible with other observations.
It has been suggested that the shape and the number of opened peripheral air spaces may be modified as a function of lung volume. Mead et al. since 1957 described lung hysteresis relating to lung expansion/deflation with a sequential opening and closing of units. is hypothesis was subsequently confirmed and sustained by other authors.
e concept of alveolar recruitment proposes that during inflation/deflation lungs expand and retract not isotropically, but through a sequential opening and closing of the PAS. In particular during inflation peripheral air space could modify their number by recruitment of alveolar units. On the contrary, during deflation there should be a point in which the opening zone ends and a sequential closing of PAS takes place.
Our hypothesis is in accord with these considerations and in particular with the evidence that the number of air spaces decreases with lung volume decrease (de-rectruitment). Acoustic microholes consists in both closed PAS and unfolded alveolar walls and septa as well as in thickened pathologic interstitium. ese features are well evident in our histological images. (Figure 16).
Figure 16 – Left. Three dimensional surface digital reconstruction of histological 40X field (red = empty) using Thermal LUT option (Image J, NHI, USA). A: enflated lung. B: deflated lung. On the right, related histological thresholded 40X images. A surface of an inflated lung is clearly less porous than the surface of a deflated lung. According to literature, over a range of density between 0.15 and 0.62 g/ml becomes anisotropically more dense and less porous. In B, superficial acoustic holes are significantly larger than in A, permitting the permeation of acoustic waves (in a characteristic range of frequencies hole related), able to generate backscatter rather than specular reflection. (Modified from Soldati G et al, Respiration, 2014;88:458)
the lung
In line with these observation, B Lines and with lung appear thanks to the permeabilization of the reflector in certain points of the pleural surface, which can be pathologically induced and/or related to deflation. ey act as sort of acoustic microholes and have the peculiarity to trap ultrasound pulses in small reverberation rooms, whose dimensions must be related with the wavelength used. e distribution along the pleura of these acoustically active structures,
Physics of chest ultrasound 63
and their volumes, would determine the concentration of B Lines and their confluence for a critical decrease in the density of the substrate. A high and mostly homogeneous (uniform) concentration of these structures could represent the origin of white lung.
Lung consolidations
In lung ultrasound a consolidation appears as a tissue, consequently it can be characterized by shape, size, echostructure and echogenicity28 (Fig. 17).
Figure 17 – Right bronchopneumonia. To the left: radiographic image. The ultrasound scans (right and bottom) show quite clearly the irregular alveolar consolidation (top) and the adjacent interstitial syndrome (bottom) due to inflammatory edema.
e physical basis producing images of consolidation are those common to the parenchyma­tous organs. e homogeneity and the relative absence of interfaces critically decrease the shifts in acoustic impedance. Consequently the phenomena of reflection are reduced, and those of scattering increase. e perfect consolidation in lung ultrasound is the obstructive atelectasis, after that internal air has been reabsorbed29 (Fig. 18).
Figure 18 – Lung consolidation (round atelectasis) (arrows). X-ray image and ultrasound equivalent one. The lesion does not contain air.
64 oracic ultrasound
Even pneumonia30 (Fig. 19) may appear relatively homogeneous and have almost no reflec­tions, provided that they contain very little air.
Bronchograms
PNEUMONIA
AIR BRONCHOGRAMS
Figure 19 – Lobar pneumonia. a: left upper lobar consolidation with evident air bronchograms. c: ultrasound image, evident segmental air bronchograms. The peripheral parenchyma is completely hepa­tized. b: x-ray of the same subject after seven days of effective antibiotic therapy. Significant reduction with re-aeration of the lesion. The ultrasound as well (d) shows a clear reduction of the consolidation, only small air bronchiolograms remain.
e air inside the consolidations is reflective and it draws brilliant images depending on its layout. ese images constitute the so-called air bronchograms31. Obviously a pulmonary consolidation is visible only if not covered by aerated lung. To be seen a consolidation must reach the pleural surface.
Other acoustic effects
When ultrasound passes through a highly permeable area the signal is less attenuated. e result is an acoustic reinforcement when the wave encounters a denser deep structure. is effect is the opposite of what is found at the level of attenuating or reflective objects, that produce shadows and/or reverberations. In fluid collections a greater acoustic energy goes behind the permissive area, and this results in hyperechogenicity or reinforcement of the rear wall (an effect clearly seen in cysts).
In lung ultrasound this phenomenon is visible behind pulmonary consolidations32. By virtue of their higher water content, consolidations facilitate the passage of ultrasound in order to make the deep contour of the lesion brilliant (more echogenic). Sometimes lung consolida­tions appears as a “cyst” (Fig. 20).
Physics of chest ultrasound 65
Figure 20 – Lung consolidation. Evidence of faded and artifactual edge. The compact appearance indicates the absence of air inside. The pleural line is clearly broken and a strong posterior enhancement of the lesion is evident.
Finally, pleural and pericardial fluid collections, easily allow the passage of the ultrasound beam and behave similarly to abdominal and articular collections, and to organs and tissues with fluid content (gallbladder, bladder, blood vessels, hematomas, abscesses, seromas) (Fig. 21).
Compressed lung
Figure 21 – Pleural effusion. CT and ultrasound image. The ultrasound examination shows that the pleural liquid is transonic.
A homogeneous non corpuscular liquid creates a transonic area opening therefore good acoustic windows. As the liquid acquires density, corpuscularity or debris, it lacks of transonicity, and it assumes corpuscular, complex, fibrinous, alveolar or pseudo-solid aspects (Fig. 22)
ese characteristics will be considered during the description of pleural effusions. e transonicity of a fluid collection, for the physical reasons discussed above, correlates with
the acoustic reinforcement of the rear wall.
66 oracic ultrasound
Figure 22 – Necrotizing pneumonia and pleural empyema. a: pleural effusion and compressed lung parenchyma (thin arrow) with punctiform (bronchiolar) residual aeration. b: pleural effusion shows echogenic septa that tend to a complex arrangement. c: compact, air-free lung area (thin arrow) with relatively hypoechoic central focus (colliquation). d: best evidence of necrosis (large arrows) and of the complex appearance of the pleural fluid.
Biological damage due to ultrasound
Ultrasound is a form of mechanical energy with biological effects during its diagnostic use. e effects concern the production of heat and non-thermal variations of the media. Non thermal actions are especially cavitation and mechanical effect (bulk acoustic streaming and standing wave radiation forces)33.
e passage of ultrasound in tissues attenuates the acoustic energy and produces heat for en­ergy absorption and scattering. e main harmful effects of induced warming are principally related to the insonation of the embryo and fetus, and then to the obstetric applications of echography34.
In order to demonstrate harmful effects, experimental studies have employed animal models and energies four times higher than those usually used in diagnostics. It is likely that stand­ard diagnostic tests do not have any action in this regard, particularly on lungs, unless high energies and Doppler techniques (such as pulsed Doppler) are employed. e major damage is espected on the fetus, where potentially critical temperatures can be reached, especially close to the bones35.
Physics of chest ultrasound 67
e non-thermal effects (which are theoretically sensitized by increased local temperature) are produced by mechanical energy. is kind of damage occurs in particular when the acoustic field interacts with gas36.
is may be represented by physiologic gas (as in the lung or in the gut), by microbubbles deliberately introduced (contrasts) or by bubbles created during the rarefactional phase of the acoustic pressure cycle (acoustic cavitation).
Of particular relevance is the exposure of lung tissue to the acoustic energy of ultrasound. Pulmonary haemorrhages (mainly capillary) were produced after prolonged exposure to ultra­sound in the lungs of rodents, pigs and monkeys, and although these findings have not been reproduced on neonatal or adult human lungs, their biological consequences are not clear37. Studies on humans have shown no correlation between the diagnostic use of ultrasound and adverse effects, and the overall picture suggests that, with usual Mechanical Index*, there are no risks related to the use of ultrasound.
Some observations, however, are congruous with the applications of chest ultrasound. e lung is an aerated organ with a variable physiological (during respiration) and pathological aeration. It is likely that in a physiologically expanded lung, the penetration of acoustic en­ergy is low because of the pleural mirror effect. is protective action may be weakened for intermediate degrees of collapse or increases in lung density38.
Widespread use of echocardiography in adults, in pediatrics and neonatology and the use of breast ultrasound have not ever produced clinical lung injuries. However, according to the “as low as reasonably achievable” precepts, we believe that during pleuropulmonary exploration, especially in children and in newborn, the output of the machine (Mechanical Index) should be kept to a minimum39. It is interesting to note that all artifactual subpleural, physiological and pathological components, can be identified with such evidence, even when using very low mechanical index (0.4-0.6).
Lung ultrasound of the future
In this chapter some concepts are expressed. ey may predict a lung ultrasound of the future. As a diagnostic role is recognized to lung ar­tifacts, we believe that is necessary their in-depth knowledge. Knowing the genetic basis of what is seen, in the evidence that what is seen is not anatomy, means that the complexity needed to produce real-time image is probably missing and misleading. It is also evident that the ultrasound equipment and probes, as they are built today, are not made to amplify or classify artifacts.
On the contrary, the “cosmetics” needed to produce clear images, increas­ingly seeks to elide artifacts, which are becoming less noticeable with advanced ultrasound techniques.
(continued)
* e mechanical index is the (dimensionless) ratio between the peak of negative pressure of ultrasound and the square root of its frequency.
68 oracic ultrasound
(continued)
With this in mind, it is relatively easy to theorize that an exploring ultra­sound, with a well-defined frequency, probes the specularity of a strongly impedant surface and indicates when this surface becomes increasingly permeable to insonation, as the density immediately below varies.
And it is also relatively easy to assume that an image is not necessary for this exploration. A sort of “reflection acoustic spectroscopy” would replace the current cumbersome ultrasound machines, revealing how the porosity and the forms of subpleural space of a pathological lung vary.
Beyond future scenarios we think that ultrasound scans of a pathological lung largely represent a very particular ultrasound of an acoustic interface. Lung ultrasound detects the “shape of the air”.
Recommended readings
Adam A, Dixon AK. Grainger & Allison’s Diagnostic Radiology. Elsevier Churchill Livingstone, Philadelphia, 2008. Bankman IN. Handbook of medical imaging, processing and analysis. Academic Press, San Diego, 2000. Fehrenbach H, Ochs M. Studying lung ultrastructure. In: Methods in pulmonary research (Uhlig S, Taylor AE,
eds.). Birkha, Basel, 1998, pp. 429-454. Glaser R. Biophysics. Springer, Berlin, 2001. Hill CR, Bamber JC, Haar GR. Physical principles of medical ultrasound. John Wiley & Sons, Chichester, 2004. Hobbie RK, Roth BJ. Intermediate Physics for Medicine and Biology. Springer, New Yok, 2007. Lichtenstein D. Whole body ultrasonography in the critically ill. Springer-Verlag, Berlin-Heidelberg, 2010. Mathis G. Chest sonography. Springer-Verlag, Berlin-Heidelberg, 2008. Szabo TL. Diagnostic ultrasound imaging. Elsevier Academic Press, Amsterdam, 2004.
Tong P, Fung YC. Biomechanics of Injury and healing. In: Introduction to Bioingineering, Advanced Series in
Biomechanics, vol 2. (Fung YC, Chien S, eds.). World Scientific Publishing London, 2001.
Weibel ER. e pathway for oxygen. Harvard University Press, Cambridge, 1984. Weibel ER. Stereological methods, vol. 1, Practical methods for biological morphometry. Academic Press,
London, 1979. Wells PNT. Biomedical Ultrasonics. Academic Press, London, 1977. West JB. Respiratory physiology. Lippincott William & Wilkins, Philadelphia, 2008.
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