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“Synthetic” Comets: A New Look at Lung Sonography
Ultrasound in Med. & Biol., Vol. 37, No. 11, pp. 1762–1770, 2011 Copyright Ó 2011 World Federation for Ultrasound in Medicine & Biology Printed in the USA. All rights reserved 0301-5629/$ - see front matter
doi:10.1016/j.ultrasmedbio.2011.05.024
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Original Contribution ‘‘SYNTHETIC’’ COMETS: A NEW LOOK AT LUNG SONOGRAPHY GINO SOLDATI,* VALERIA GIUNTA,y SARA SHER,z FRANCESCA MELOSI,x and CLAUDIA DINI{ * Emergency Medicine Unit, Valle del Serchio General Hospital, Lucca, Italy; y Pulmonary Medicine Dept IRCCS Foundation, Ca’Granda Hospital, Policlinic, Milan, Italy; z Anesthesia and Critical Care, Niguarda Ca’Granda Hospital, Milan, Italy; x Pediatric Intensive Care Unit, Meyer Hospital, Florence, Italy; and { Biomedical Engineering Faculty, University of Pisa, Pisa, Italy (Received 12 January 2011; revised 19 May 2011; in final form 20 May 2011)
Abstract—Ultrasound interstitial syndrome is an echographic pattern of the lung characterized by the presence of multiple acoustic artifacts called ‘‘comets’’ or B-lines. It correlates to increase in extravascular lung water and to interstitial lung disease. From the physical and genetic point of view, the characteristics and the entity of this correlation have not yet been studied. The purpose of this study was to extrapolate past observations and demonstrate how comets or B-lines are artifactual images whose formation is linked to ultrasound interactions on discretely aerated tissues of variable density. Echographic comets were studied by scanning a wet synthetic, partially aerated polyurethane sponge (phantom). Density of the phantom in different drying phases was measured and correlated to the presence of echographic artifacts. Artifacts (comets) showed a different concentration from a completely white artifactual field to presence of rare comets. Their density correlates with porosity and geometry of the phantom. In our opinion, comets represent superficial, artifactual, density and geometry correlated phenomenon due to the acoustic permeability of a broken (collapsed) specular reflector, normally present when the phantom is dry. (E-mail: [email protected]) Ó 2011 World Federation for Ultrasound in Medicine & Biology. Key Words: Ultrasound, Artifact, Lung, Diagnosis.
furthermore, creates debate regarding the best way to represent them, their quantification and which ultrasound frequency, tissue harmonic and echographic setting should be used for an optimal representation. Exact terminology, especially in relation to their genesis, is also lacking (Feldman et al. 2009) and this may induce the erroneous belief that the echographic interstitial syndrome may represent precise pulmonary landmarks. In view of this, lung interlobular septa have gained a determinant and causal role in the literature (Frassi et al 2007; Lichtenstein et al. 1997) so that in most studies the B-line ended up identifying, although indirectly, a structural component of the lung (the interlobular septum). A recent study documented how artifactual echographic patterns (comet tail) may be reproduced in vitro with elementary systems of bubble layers or foam (Soldati et al. 2009). A similar analysis of these artifacts emerged from studies of intestinal echography in relation to air bubble systems and independent from definite anatomic structures (Wilson et al. 1999). On the basis of this data, we propose that the ‘‘comet-tail’’, whichever its nature, should be described as an acoustic interaction artifact appearing in air substrates of particular geometry and density. The latter characteristics of the insonated
INTRODUCTION Echographic interstitial syndrome identifies that group of ultrasound lung images characterized by the presence of multiple ‘‘comets’’, also known as B-lines, that originate from the pleural line and extend to the inferior margin of the screen (Lichtenstein et al. 1997). A correlation exists between these images and the increase in extravascular lung water (Jambrik et al 2004), interstitial lung disease (Gargani et al. 2008; Reissig and Kroegel 2003; Volpicelli et al. 2006), noncardiogenic lung edema (Copetti et al. 2008), interstitial pneumonia (Volpicelli and Francisco 2009) and lung contusion (Soldati et al. 2006). Because of the clearly detectable difference between the normal lung (Fig. 1A) characterized by multiple reflections and/ or mirror images (A-lines) and lung with interstitial disease (Fig. 1B), clinical interest in lung ultrasonography has exponentially increased in the last few years. From the physical point of view, little is known on the formation of ‘‘comet-tail’’ artifacts (Avruch and Cooperberg 1985; Kremkau and Taylor 1986). Their artifactual nature, Address correspondence to: Gino Soldati, Emergency Medicine Unit, Valle del Serchio General Hospital, Via Nazionale 106, 55036 Pieve Fosciana, Lucca, Italy. E-mail: [email protected] 1762
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Fig. 1. (A) Normal lung. (B) Lung with interstitial disease.
‘‘tissue’’ would, therefore, determine a different concentration of artifacts along the surface. The purpose of this study is to extrapolate past observations (Soldati et al. 2009) by demonstrating how echographic comets are produced by scanning of a partially aerated, synthetic sponge and how their numeric density is thus related with the porosity and geometry of the sponge itself. Terminology The following terms are used in the text: Artifact: A structure not normally present but produced in imaging by an acoustic induced phenomenon. In practical terms, an erroneous interpretation of a signal by the ultrasound machine that does not represent it in anatomic terms. Specular reflector: Acoustically impermeable interface between a relatively transonic medium and a largely
aerated medium, normal or 90 to the direction of the ultrasound beam. The acoustic reflection coefficient is conventionally . 0.7. Comet: Artifactual image originating from an acoustic interface, extending to the inferior edge of the screen with variable depth. The frequencies used in the present study show in its structure a strict overlap of transversal and oblique echoes that characterize its echogeny relative to the background. In this article, it comprehends the terms used in literature as B-line (Lichtenstein et al 1997), comet-tail (Kremkau and Taylor 1986), ringdown (Avruch and Cooperberg 1985) or reverberation (Feldman et al. 2009). Comets may be variably dense or separate but always identifiable. When a homogeneous echogenicity appears in the scanning field as the sum of different comets, the term ‘‘white lung’’ is used. Reflector collapse: A conventional term defining critical acoustic permeabilization (reduction of the
Fig. 2. Polyurethane phantom. Microscopic and macroscopic view.
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acoustic pressure reflection coefficient R , 0.7) of an interface or reflector, demonstrated by the acoustic interaction on the underlying substrate (normally anechogenic or black), which increases its echogenicity producing comets or a white field. MATERIALS AND METHODS Polyurethane are polymers made of organic units linked by urethane molecules. They may be produced as foams or sponges of variable density. We studied a model of porous polyurethane, ‘‘defined as phantom’’, on which we carried out different echographic scans. This material has an interconnected porous geometry, with pore diameter varying from 50 to 150 mm (Fig. 2) and it shows different densities and geometries in time during an experimental controlled wet condition, due to water percolation/evaporation through a relatively fixed mathematical scheme (Yiotis et al. 2004, 2006). The model of fluid transport through a porous material is well known in physical, industrial and geological literature (Dullien 1992). In the present study, we used a commercially available polyurethane sponge (Kendall Copa Plus; Tyco, Mansfield, MA, USA), with a density of 0.12 g/mL. Acoustic conduction velocity of the non-porous polymer is about 1700 m/s and its acoustic impedance is 1.8 Mrayls (Selfridge 1985). Interconnected porosity (%) of the models has been determined by measuring the dimensions and weight of the object:
Fig. 3. Echographic scanning technique of the phantom.
w p 5 12 ,100 r,V where p 5 porosity, w 5 weight, r 5 density of the polymer (1.04 g/mL) and V 5 volume of the model and turns out to be 88%. The polyurethane objects have been modeled to a thickness of 7 mm, comparable weights and a rectangular shape to fit the linear probe used for scans. Weight and volume of each phantom at its dry state was measured and their density derived as mp/V (g/mL). To carry out scans able to simulate both a focal position and one of a superficial, impermeable layer as in the real anatomic situation of the lung, the phantom was then covered by a 150 mm thick chloroprene polymer membrane (Biosynto, Mediflex, Italy) with a density of 1.31 g/mL and
Fig. 4. Drying curves of the 10 phantoms.
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acoustic impedance of 1.5 Mrayls (Selfridge 1985). A cylindrical chloroprene water-filled bag, with a diameter of 1 cm, was interposed between the probe and the phantom to create distance. Acoustic gel was used as coupling media between the probe and the water filled bag and between the bag and chloroprene membrane. Finally, a draining pad of polyurethane sponge, with a dimension of 100 3 100 3 7 mm, was placed under the wet models to favor, through capillarity and evaporation, a ‘‘drying’’ time not to exceed 180 min (Fig. 3). Room temperature during the experiment was 22 to 24 and humidity 50% to 60%. After the initial densitometric evaluation and scanning, dry phantoms were soaked in distilled and degassed water for 10 s (5 s per side), then extracted and withheld until dripping stopped. They were then weighed on an electronic precision balance (JAY 1003; Nanjing Oxy Technology & Trading Co., Nanjing, China) with reading accuracy 0.001 g at 4-min intervals thus creating a ‘‘drying curve’’ (Fig. 4). Echographic scans (three consecutive frozen acquisitions in 30 s) were also carried out at 4-min intervals, right after weight acquisition. The relative patterns, stored in the machine’s hard disk, served as material for future phase identification. Images were revised at the end of each procedure on the phantom according to the following criteria.
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‘‘Start’’ was a 4-min standard interval after water dipping: the echographic field has a variable, nonclassifiable echogenity. ‘‘End’’ was the end of the phase 5, with total artifact disappearance. Along the ‘‘drying curve’’, five phases were identified as follows. Phase 1, white: the echographic field is completely and homogenously echogenic. Phase 2, dense comet: echogenic overall aspect with initial dishomogeneity created by no more than 2 hypo/anechogenic vertical bands which are at least 2 mm thick. Phase 3, separate comet: evidence of separate comets which may be counted in a frozen image; there are thin, clear spaces between comets. Phase 4, thinning-out: each comet is clearly separated from the next with at least three intervals larger than 3 mm. Phase 5, exhaustion: five to 10 separate comets extending to the bottom of the field. Concordance among three different operators (GS, VG and CD) on each set of three images defined the various phases. Representative images of each phase are shown in Figure 5, including (A) the sonographic appearance of dry polyurethane. We recorded weight and (corrected) volume of the scaffolds at each echographic scan. For each measure taken, we calculated density corrected for the blowing effect due to dipping. The correction coefficient was determined through an
Fig. 5. Wet and dry polyurethane. (A) Dry polyurethane, a specular reflector. (B) Phase 1, white. (C) Phase 2, dense comet. (D) Phase 3, separate comet. (E) Phase 4, thinning out. (F) Phase 5, exhaustion.
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Table 1. Physical qualities of biologic tissues and synthetic material used in the study Acoustic media
Density (g/mL)
Acoustic impedance (Mrayls)
Porosity (%)
Sound velocity (m/s)
Attenuation at 1MHz (dB/cm)
Distilled water (20 C) Polyurethane polymer Polyurethane foam Chloroprene Muscular tissue Fat tissue Tissue (mean) Inflated lung (TLC) Deflated lung (FRC) Consolidated lung (pneumonia) Atelectatic lung Air (20 C)
0.998 1.04 0.12 1.31 1.07 0.92 1.05 0.15 0.5 0.76 0.84 0.012
1.5 1.8 0.1 1.5 1.7 1.3 1.63 0.1 0.4 0.6 1.4 0.00045
– 0 88 0 0 0 0 85 50 34 16 –
1480 1700 833 1510 1585 1450 1540 500 733 948 1660 343
0.0022 0.46 1.3–3.3 0.63 0.81 50
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TLC 5 total lung capacity; FRC 5 functional residual capacity. (Dunn and Fry 1961; Selfridge 1985; Tong and Fung 2001; Wells 1975, 1977).
estimate of the mean volumetric variation of 10 phantoms, similar in weight and dimensions, undergoing an analogous dipping/percolation treatment. Echographic scans of the dry and wet models were carried out with a commercially available machine (Aplio XV; Toshiba Medical Systems Europe, Rome, Italy), equipped with a 4 cm linear probe (Toshiba PLT 805 AT) operating at a frequency of 6.6 MHz, without tissue harmonics. A relatively low mechanical index of the ultrasound beam (the peak of rarefactional pressure in tissue divided by the square root of the ultrasound frequency) of 0.6 was used. The scan was perpendicular to the surface of the phantom and centered on the median line. We used a mechanic support system for the probe with the least possible compression through the acoustic gel. All images were stored on the machine’s hard disk. Table 1 shows densitometric, porimetric and acoustic characteristics of the polymers used compared with lung and thoracic, normal and pathologic tissue (Wells 1975). Table 2 reports reflection coefficients of the interface between aerated and nonaerated tissues, calculated for a normal acoustic impedance (Tong and Fung 2001; Wells 1975).
The described model theorizes time for appearance and density values of the phantom during the ‘‘drying curves’’ of the phantoms. We considered the beginning of phase 1 as the moment of collapse of the dry specular reflector. Analogously, temporal and densitometric data of phases 2, 3, 4 and 5 represent the values of porosity variation correlated to the expression of countable comets. Finally, the interval beyond the last phase and ‘‘end’’ defined the reconstitution of the specular reflector due to critical reduction in acoustic permeability of the scaffold. The parameters measured were: (1) the presence of a specular reflector in the ‘dry’ model and its eventual collapse caused by geometric/densitometric variations following water dipping; (2) different artifactual representation in relation to a variable geometry; and 3) correlation to substrate density. Numeric data were expressed as absolute values, means and standard deviations. Parametric series were compared through Pearson’s correlation coefficient. Comparisons between means were carried out with analysis of variance (ANOVA) and Bonferroni’s correction using SPSS for Windows version 14 (SPSS, Chicago, IL, USA). Statistic significance was considered when p # 0.05.
Table 2. Reflective properties of acoustic discontinuities in human chest and in polyurethane sponge Interface
Reflection coefficient* R
Water/air Muscle/air Fat/muscle Muscle/inflated lung Muscle/deflated lung Muscle/condensed lung (pneumonia) Muscle/atelectatic lung Spacer/dry polyurethane
20.99y 20.99 0.13 20.88 20.72 20.61 20.01 20.85
* Acoustic pressure reflected back from anatomic interfaces (1 5 maximal reflection, 0 5 maximal acoustic permeability (Dunn and Fry 1961; Selfridge 1985; Tong and Fung 2001; Wells 1975,1977). y The sign of R is negative because the impedance of the second medium is less than water and the lung acts as a pressure relief surface relative to water (Oelze et al. 2003).
RESULTS A total of 10 polyurethane phantoms 7 mm thick, mean volume 7.55 6 0.54 mL, range 6.8 to 8.3 mL, mean weight 0.909 6 0.065 g, range 0.817–0.997 g were studied. Water dipping increased mean weight to 2.541 6 0.186 g, range 2.197–2.880 g and decreased the porosity to around 71%. Following water dipping phantom volumes increased along a timeline including three phases: (1) instantaneous volume increase by 19%; (2) slow increase for 40 min (further increase 13.7%, global increase 35.6%); and (3) plateau up to 120 min with global volume increase of 44.5%. The time/volume curve of dimensional increase of wet phantoms furnished
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correction coefficients for density calculations in time and, thus, the ratio of weight to corrected volume. For each scaffold, a ‘‘dewetting’’ curve was created by calculating weight at 4-min intervals. Variation of weight-intime curves are represented in Figure 4. Curves show a time (21) characterized by the initial dry weight and a final time identifying the end of evaluation. The latter values varied with a mean value of 128 6 28.47 min, range 104–176 min. A correlation existed between wet weight and time to dry (R 5 0.73, p , 0.05) but not between these times and dry scaffold weight. Figure 6 shows the mean and confidence interval (95%) of the starting time of each echographic phase through the drying period. Calculation of density in time for each scaffold showed a trend in reduction with a reciprocal increase in porosity toward a value around 83% at 120 min. Density of the ‘‘wet’’ scaffolds was in average 0.287 6 0.0304 g/mL; mean density at the beginning of the ‘‘white phase’’ was 0.258 6 0.0249 g/mL; mean density at the end of the experiment was 0.1438 6 0.0097 g/mL. Figure 7 shows mean values and confidence intervals of density for each model through all experimental phases. Table 3 lists mean densities, range and standard deviation of the phantoms at each characteristic phase. In each experimental case, echographic scans showed an organized progression from the white phase, through the dense comet phase, to thinning out of comets and finally to the reconstitution of the specular reflector, across decreasing values of density and reciprocal increasing values of porosity (from 71% to around 83%). Specifically, the phantom behaved as a specular reflector for values of density lower than 0.13 g/mL. In this case, the whole field under the acoustically imperme-
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Fig. 7. Phantom density values (g/mL, mean and confidence interval – 95%) in the five (1–5) different experimental phases. ‘‘Start’’ is 4-min standard interval after water dipping, ‘‘end’’ represents total artifact disappearance.
able surface was practically anechogenic so that even a metallic object, as 20 to 16 Gauge needles, placed inside the scaffold became invisible. Artifacts started appearing, in a constant progression, for values of density going from 0.132 g/mL to 0.34 g/mL. The ‘‘white phase’’ was preceded by a period no longer than 4 min, in which the scaffold was hypoechogenic or with variable echogenicity, for values of mean density of 0.287 to 0.258 g/mL (Start). Throughout this period the scaffold was characterized by an elevated acoustic permeability, in that an 18 G needle inserted in the phantom was easily identifiable. The ‘‘white phase’’ was characterized by diffuse hyperechogeny. Mean density values of the phantom in this phase (0.258– 0.205 g/mL) were statistically different (p , 0.05) from those relative to the ‘‘separate comet’’ phase (mean density 0.188–0.172 g/mL). The same statistically significant difference characterized the difference in density from the ‘‘dense comet’’ phase to the ‘‘thinning-out’’ phase and between ‘‘separate comet’’ phase and Table 3. Mean densities, range and standard deviation of the phantoms at each characteristic phase Phases N Mean density Standard deviation Minimum Maximum
Fig. 6. Starting time (in minutes, mean and confidence interval – 95%) of the experimental phases characterized by artifacts of variable density. (1: White; 2: Dense comet; 3: Separate comet; 4: Thinning-out; 5: Exhaustion.).
Start 1 2 3 4 5 End Total
10 10 10 10 10 10 10 70
0.2879 0.2581 0.2052 0.1882 0.1723 0.1576 0.1438 0.2018
0.0304 0.0249 0.0218 0.0186 0.0158 0.0107 0.0097 0.0531
0.256 0.230 0.175 0.153 0.146 0.142 0.132 0.132
0.340 0.319 0.250 0.219 0.198 0.175 0.160 0.340
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‘‘exhaustion’’ phase. Densitometric comparisons for contiguous phases 1 through 5 did not result statistically significant. DISCUSSION The three main presuppositions of this study were that: (1) Normal lung behaves, at the pleural level, as a specular reflector with an in vivo reflection coefficient of 0.88 (Wells 1977). Absence of artifacts indicates massive, homogeneous reflection, which, in fact, produces horizontal repetitive reflections (A-lines), as transducer reverberations (Dunn and Fry 1961). (2) Artefactual phenomenons in the pathologic lung, as hyperechogeny (white lung), lung comets (B-lines), micro and macro consolidations, appear in realtime sonography as signals of ‘‘acoustic permeabilization’’ of the pleural plane, with consequent physical interactions (probably multiple variable reflections) of the ultrasound beam with the more or less aerated subpleural tissue. (3) General biophysical evidence, as well as dedicated studies, has indicated how lung acoustic permeability is a density correlated phenomenon, so that acoustic interaction between the ultrasound beam and the pulmonary parenchyma increases as lung density approaches that of water (Dunn 1974; Oelze et al. 2008). The use of a phantom with acoustic characteristics comparable to those of lung tissue (in its air and solid compartments) and with a porosity or density that varied in time, allowed us to confirm these presuppositions through two main important aspects that will be synthetically and qualitatively explained: (1) the drying curve (Yiotis et al. 2004) of porous materials and its transition points (as large scale superficial phenomenons in the phantom); and (2) the theoretic concept of ‘‘percolation’’ or ‘‘geometrical phase transition’’ (Dullien 1992; Yiotis et al. 2004) in a three-dimensional (3-D), finite, latex structure (for small scale phenomenons of the superficial interface of the phantom). In a microporous interconnected and wet material, phenomenons of capillarity prevail. A completely soaked phantom with all its air spaces filled with water (occupation probability of 1, represents a liquid cluster with total vertical hydraulic (and obviously acoustic) connectivity (Oelze et al. 2008; Szabo 2004). Acoustic permeability in such a case is close to that of water (Yiotis 2007). From the clinical/practical point of view this situation is represented by scanning of a lung consolidation (as air deprived pneumonia or atelectasis) (Bouhemad et al. 2010). Passive water soaking in a sponge is only partial for physical reasons. That obtained in this experiment (with a resultant phantom’s porosity of 71%) was characterized
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by an initial transitory phase of capillarity driven redistribution of about 4 min before appearance of the ‘‘white’’ phase. This first phase produces a large number of superficial acoustic interactions own to a high superficial connection (Yiotis et al. 2006). The subsequent phases identified, through the presence of objectively identifiable artifactual phenomenons, a progressively declining superficial acoustic permeability. Such permeability resulted density or porosity dependent. Through these phases our drying curves showed a behavior comparable to a drying constant rate period (DCRP) which, in line with Yiotis (2004 and 2006), is characterized by water excess on the model’s porous surface. During the DCRP, capillarity controls water flow from inside the pore space to the surface of the phantom, where water evaporates. Liquid flows through either completely or partially wet pores and pore walls are either covered with water or have water in the corners and the central part dry. This way the air/water interface takes the shape of a meniscus reflecting the need of creating a particular contact angle with the solid and the tendency of minimizing interfacial area within the pore. It is therefore allowed to state that, in a partially soaked capillary system, the formation of many air clusters with a curvilinear delimitation is possible. The drying curves terminated with the exhaustion of comets and the reconstitution of the phantom’s acoustically impermeable surface notwithstanding residual hydration and thus greater density. Further dehydration would have followed faster kinetics as the falling rate period (FRP) in which drying is controlled by mass transfer through the dry pore space. In our model this phase was without comets and the phantom’s surface behaved as a specular reflector inside the DCRP, probably for the presence of a complete superficial gaseous cluster. In our study, acoustic artifacts appeared solely in the dewetting DCRP phase, characterized by relatively reproducible values of mean density and especially by characteristic geometry of aqueous clusters. In line with the literature (Dullien 1992; Yiotis et al. 2004; Yiotis et al. 2006), DCRP corresponds to the phase in which the main liquid cluster (MLC) is formed and predominates. From the geometrical point of view, this means that certain gas percolations exist in the model but during the drying period most liquid pores belong to the sample-spanning liquid cluster (main liquid cluster, MLC) and only a percentage of liquid pores belong to isolated liquid clusters (disconnected clusters, DC). The MLC maintains a superficial connectivity and induces an acoustic permeability that is function of the probability of pore filling. This principle is defined, on large scale, by the mean porosity value of the scaffold but from the geometrical point of view and on small (very superficial) scale, superficial connectivity of the MLC will become
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Fig. 8. Effect of the geometric variation of a porous, permeable structure, with variable water occupation probability p, on its acoustic permeability. (X-Y: two-dimensional (2-D) latex, Z: third dimension, not shown). Black: full, White: empty. At the right and left side of the graphical scheme the corresponding echographic representation on polyurethane phantom. (A) p 5 0, completely aerated substrate (i.e., normal lung). (B) p 5 1, completely full substrate (i.e., lung condensation), complete permeabilization (arrows). (C) p 5 0.96, total superficial connection, the empty cell generates the central reflective spot. (D) p 5 0.96, superficial disconnection focus, the empty cell is analogous to a small air bubble in a liquid medium (focal reflective spot). (E) p 5 0.78, aerous spanning cluster, coexistence of two main liquid clusters (MLC); combination and amplification of (C) and (D). (F) p5 0.87, superficial disconnection of an MLC able to capture ultrasound. (G) p 5 0.75, similar superficial disconnection with different configuration. (H) p 5 0.43, complete superficial disconnection, reconstitution of the specular reflector. Only (F) and (G) geometries produce comet-tail artifacts in the spots indicated by the arrows which can actually repeat themselves on the surface. (A) and (H) are acoustically and sonographically equivalent.
more and more irregular in time. This progressive disconnection of the MLC, which preludes the formation of a minimum superficial air content for which the structure will no longer be superficially permeable to ultrasound, may be studied through latex percolation. From the practical point of view, this means that in our model during the ‘‘dewetting’’ comet producing phase, there is an irregularly interconnected, superficial MLC (whose superficial pores are randomly either full or empty), with progressively declining interconnection in relation to structure density and porosity (Fig. 8). Superficial connections may be surrounded by air gaining the role of acoustic traps (or acoustic holes) with variable concentration. At this level, the specular reflector loses its integrity producing multiple focal reflection points with
reverberating potential and casually modulated by either constructive or destructive interference. As the number of acoustic holes grows denser, geometry will evermore resemble a comet producing bilayer bubble system in a liquid medium (Soldati et al. 2009). Finally, the specular reflector will be reconstructed once the MLC and the DC are no longer superficially connected.
CONCLUSIONS This study validates the following hypothesis: (1) No matter what the physical nature or genesis of the radio-frequency (RF) signal, comets created in the phantom represent superficial, artifactual, density
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(3)
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correlated phenomenons due to a physical modification of the specular reflector in a dry model. Acoustic permeability of a microporous tissue is density dependent (O’Brien et al. 2002; Oelze et al. 2003; Dunn 1986): lower porosity induces greater acoustic permeability and greater acoustic interactions with the aerated superficial structures. Dominant ‘‘anatomic’’ structures are not necessarily involved in the genesis of comets. It is a random phenomenon. Comet concentration and ‘‘white’’ are correlated on the large scale and for dimensions of the vertical substrate within 7 mm, with substrate mean density. On the small scale and superficial level, with geometry of discrete air spaces as described in the percolation theory (Yiotis et al. 2006). The most efficient air space geometry for the production of artifacts is that of a bubble millimetric bilayer that typically, in an elementary gel model, produces comets (Soldati et al. 2009).
We believe that further validation of the above points would contribute to ameliorate the diagnostic power of chest sonography. A clear correlation between artifactual subpleural components and nonconsolidating density/ tissue geometry would allow quantification of interstitial pathology at the cortical level. This could furthermore contribute to perfectionating lung ultrasonographic exploration systems in terms of acoustic spectrography. This study has certain limits. A systematic RF analysis of the signals relative to artifacts has not been carried out so that their dependence on the frequency used is not known. Artifacts are in fact comparable to those observed in pathologic lung only upon an inspective (visual) examination. Geometric behavior of phantom air spaces during the ‘‘dewetting’’ phase was deduced from studies relative to different, although structurally similar, materials. The vertical density gradient of the phantom through the ‘‘dewetting’’ phases was assumed to be null (gravity stabilized) so that a positive gravity-dependent gradient (however, present) was ignored and this is actually a simplification of the model. Finally, for the estimate of artifact formation, a standard, commercially available real-time diagnostic system with fixed frequencies was used and its purpose is certainly not that of quantifying artifacts. REFERENCES Avruch L, Cooperberg PL. The ring down artifact. J Ultrasound Med 1985;4:21–28. Bouhemad B, Liu ZH, Arbelot C, Zhang M, Ferrari F, Le-Guen M, Girard M, Lu Q, Rouby JJ. Ultrasound assessment of antibioticinduced pulmonary reareation in ventilator associated pneumonia. Crit Care Med 2010;38:84–92. Copetti R, Soldati G, Copetti P. Chest sonography: A useful tool to differentiate acute cardiogenic pulmonary edema from acute respiratory distress syndrome. Cardiovasc Ultrasound 2008;6:16.
Volume 37, Number 11, 2011 Dullien FAL. Porous media. Fluid transport and pore structure. San Diego: Academic Press; 1992. Dunn F, Fry WJ. Ultrasonic absorption and reflection by lung tissue. Phys Med Biol 1961;5:401–410. Dunn F. Attenuation and speed of ultrasound in lung. J Acoust Soc Am 1974;56:1638–1639. Dunn F. Attenuation and speed of ultrasound in lung: Dependence upon frequency and inflation. J Acoust Soc Am 1986;80:1248–1250. Feldman MK, Katyal S, Blackwood MS. US artifacts. Radiographics 2009;29:1179–1189. Frassi F, Gargani L, Gligorova S, Ciampi Q, Mottola G, Picano E. Clinical and echocardiographic determinants of Ultrasound Lung Comets. Eur J Echocardiogr 2007;8:474–479. Gargani L, Frassi F, Soldati G, Tesorio P, Gheorghiade M, Picano E. Ultrasound lung comets for differential diagnosis of acute cardiogenic dyspnea: A comparison with natriuretic peptides. Eur J Heart Fail 2008;10:70–77. Jambrik Z, Monti S, Coppola V, Agricola E, Mottola G, Miniati M, Picano E. Usefulness of ultrasound lung comets as non radiologic sign of extravascular lung water. Am J Cardiol 2004;93:1265–1270. Kremkau FW, Taylor KJW. Artifacts in ultrasound imaging. J Ultrasound Med 1986;5:227–237. Lichtenstein D, Meziere G, Biderman P, Gepner A, Barre O. The comettail artifact: An ultrasound sign of alveolar-interstitial syndrome. Am J Respir Crit Care Med 1997;156:1640–1646. O’Brien WD, Kramer JM, Waldrop TG, Frizzel LA, Miller RJ, Blue JP, Zachary JF. Ultrasound induced lung hemorrhage: Role of acoustic boundary conditions at the pleural surface. J Acoust Soc Am 2002; 111:1102–1109. Oelze ML, Miller RJ, Blue JP, Zachary JF, O’Brien WD. Impedance measurement of ex vivo rat lung at different volumes of inflation. J Acoust Soc Am 2003;114:3384–3393. Oelze ML, Miller RJ, Blue JP, Zachary JF, O’Brien WD. Estimation of the acoustic impedance of lung versus level of inflation for different species and ages of animals. J Acoust Soc Am 2008;124:2340–2352. Reissig A, Kroegel C. Transthoracic sonography of diffuse parenchymal lung disease. J Ultrasound Med 2003;22:173–180. Selfridge AR. Approximate material properties in isotropic materials. IEEE Trans Sonics Ultrason 1985;32:381–394. Soldati G, Testa A, Silva FR, Carbone L, Portale G, Silveri NG. Chest ultrasonography in lung contusion. Chest 2006;130:533–538. Soldati G, Copetti R, Sher S. Sonographic interstitial syndrome: The sound of lung water. J Ultrasound Med 2009;28:163–174. Szabo TL. Diagnostic ultrasound imaging. Amsterdam: Elsevier Academic Press; 2004. Tong P, Fung YC. Biomechanics of Injury and healing. In: Fung YC, Chien S, (eds). Introduction to bioengineering, advanced series in biomechanics, Vol 2. London: World Scientific Publishing; 2001. Volpicelli G, Mussa A, Garofalo G, Cardinale L, Casoli G, Perotto F, Fava C, Frascisco M. Bedside lung ultrasound in the assessment of alveolar interstitial syndrome. Am J Emerg Med 2006;24: 689–696. Volpicelli G, Frascisco MF. Sonographic detection of radio occult interstitial lung involvement in measles pneumonitis. Am J Emerg Med 2009;128:1–3. Wells NT. Absorption and dispersion of ultrasound in biological tissue. Ultrasound Med Biol 1975;4:369–376. Wells PNT. Velocity, absorption and attenuation in biological materials. In: Wells PNT, (ed). Biomedical ultrasonics. London: Academic Press; 1977. p. 98–126. Wilson SR, Burns PN, Wilkinson LM, Simpson DH, Muradali D. Gas at abdominal US: Appearance, relevance, and analysis of artifacts. Radiology 1999;210:113–123. Yiotis AG, Boudouvis AG, Stubos AK, Tsimpanogiannis IN, Yortsos YC. Effect of liquid films on the drying of porous media. AIChE J 2004;50:2721–2737. Yoitis AG, Tsimpanogiannis IN, Stubos AK, Yortsos YC. Pore network study of the characteristic period in the drying of porous material. J Colloid Interface Sci 2006;297:738–748. Yiotis AG, Tsimpanogiannis IN, Stubos AK, Yortsos YC. Coupling between external and internal mass transfer during drying of a porous medium. Water Resour Res 2007;43:1–12.
doi:10.1016/j.ultrasmedbio.2011.05.024
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Original Contribution ‘‘SYNTHETIC’’ COMETS: A NEW LOOK AT LUNG SONOGRAPHY GINO SOLDATI,* VALERIA GIUNTA,y SARA SHER,z FRANCESCA MELOSI,x and CLAUDIA DINI{ * Emergency Medicine Unit, Valle del Serchio General Hospital, Lucca, Italy; y Pulmonary Medicine Dept IRCCS Foundation, Ca’Granda Hospital, Policlinic, Milan, Italy; z Anesthesia and Critical Care, Niguarda Ca’Granda Hospital, Milan, Italy; x Pediatric Intensive Care Unit, Meyer Hospital, Florence, Italy; and { Biomedical Engineering Faculty, University of Pisa, Pisa, Italy (Received 12 January 2011; revised 19 May 2011; in final form 20 May 2011)
Abstract—Ultrasound interstitial syndrome is an echographic pattern of the lung characterized by the presence of multiple acoustic artifacts called ‘‘comets’’ or B-lines. It correlates to increase in extravascular lung water and to interstitial lung disease. From the physical and genetic point of view, the characteristics and the entity of this correlation have not yet been studied. The purpose of this study was to extrapolate past observations and demonstrate how comets or B-lines are artifactual images whose formation is linked to ultrasound interactions on discretely aerated tissues of variable density. Echographic comets were studied by scanning a wet synthetic, partially aerated polyurethane sponge (phantom). Density of the phantom in different drying phases was measured and correlated to the presence of echographic artifacts. Artifacts (comets) showed a different concentration from a completely white artifactual field to presence of rare comets. Their density correlates with porosity and geometry of the phantom. In our opinion, comets represent superficial, artifactual, density and geometry correlated phenomenon due to the acoustic permeability of a broken (collapsed) specular reflector, normally present when the phantom is dry. (E-mail: [email protected]) Ó 2011 World Federation for Ultrasound in Medicine & Biology. Key Words: Ultrasound, Artifact, Lung, Diagnosis.
furthermore, creates debate regarding the best way to represent them, their quantification and which ultrasound frequency, tissue harmonic and echographic setting should be used for an optimal representation. Exact terminology, especially in relation to their genesis, is also lacking (Feldman et al. 2009) and this may induce the erroneous belief that the echographic interstitial syndrome may represent precise pulmonary landmarks. In view of this, lung interlobular septa have gained a determinant and causal role in the literature (Frassi et al 2007; Lichtenstein et al. 1997) so that in most studies the B-line ended up identifying, although indirectly, a structural component of the lung (the interlobular septum). A recent study documented how artifactual echographic patterns (comet tail) may be reproduced in vitro with elementary systems of bubble layers or foam (Soldati et al. 2009). A similar analysis of these artifacts emerged from studies of intestinal echography in relation to air bubble systems and independent from definite anatomic structures (Wilson et al. 1999). On the basis of this data, we propose that the ‘‘comet-tail’’, whichever its nature, should be described as an acoustic interaction artifact appearing in air substrates of particular geometry and density. The latter characteristics of the insonated
INTRODUCTION Echographic interstitial syndrome identifies that group of ultrasound lung images characterized by the presence of multiple ‘‘comets’’, also known as B-lines, that originate from the pleural line and extend to the inferior margin of the screen (Lichtenstein et al. 1997). A correlation exists between these images and the increase in extravascular lung water (Jambrik et al 2004), interstitial lung disease (Gargani et al. 2008; Reissig and Kroegel 2003; Volpicelli et al. 2006), noncardiogenic lung edema (Copetti et al. 2008), interstitial pneumonia (Volpicelli and Francisco 2009) and lung contusion (Soldati et al. 2006). Because of the clearly detectable difference between the normal lung (Fig. 1A) characterized by multiple reflections and/ or mirror images (A-lines) and lung with interstitial disease (Fig. 1B), clinical interest in lung ultrasonography has exponentially increased in the last few years. From the physical point of view, little is known on the formation of ‘‘comet-tail’’ artifacts (Avruch and Cooperberg 1985; Kremkau and Taylor 1986). Their artifactual nature, Address correspondence to: Gino Soldati, Emergency Medicine Unit, Valle del Serchio General Hospital, Via Nazionale 106, 55036 Pieve Fosciana, Lucca, Italy. E-mail: [email protected] 1762
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Fig. 1. (A) Normal lung. (B) Lung with interstitial disease.
‘‘tissue’’ would, therefore, determine a different concentration of artifacts along the surface. The purpose of this study is to extrapolate past observations (Soldati et al. 2009) by demonstrating how echographic comets are produced by scanning of a partially aerated, synthetic sponge and how their numeric density is thus related with the porosity and geometry of the sponge itself. Terminology The following terms are used in the text: Artifact: A structure not normally present but produced in imaging by an acoustic induced phenomenon. In practical terms, an erroneous interpretation of a signal by the ultrasound machine that does not represent it in anatomic terms. Specular reflector: Acoustically impermeable interface between a relatively transonic medium and a largely
aerated medium, normal or 90 to the direction of the ultrasound beam. The acoustic reflection coefficient is conventionally . 0.7. Comet: Artifactual image originating from an acoustic interface, extending to the inferior edge of the screen with variable depth. The frequencies used in the present study show in its structure a strict overlap of transversal and oblique echoes that characterize its echogeny relative to the background. In this article, it comprehends the terms used in literature as B-line (Lichtenstein et al 1997), comet-tail (Kremkau and Taylor 1986), ringdown (Avruch and Cooperberg 1985) or reverberation (Feldman et al. 2009). Comets may be variably dense or separate but always identifiable. When a homogeneous echogenicity appears in the scanning field as the sum of different comets, the term ‘‘white lung’’ is used. Reflector collapse: A conventional term defining critical acoustic permeabilization (reduction of the
Fig. 2. Polyurethane phantom. Microscopic and macroscopic view.
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acoustic pressure reflection coefficient R , 0.7) of an interface or reflector, demonstrated by the acoustic interaction on the underlying substrate (normally anechogenic or black), which increases its echogenicity producing comets or a white field. MATERIALS AND METHODS Polyurethane are polymers made of organic units linked by urethane molecules. They may be produced as foams or sponges of variable density. We studied a model of porous polyurethane, ‘‘defined as phantom’’, on which we carried out different echographic scans. This material has an interconnected porous geometry, with pore diameter varying from 50 to 150 mm (Fig. 2) and it shows different densities and geometries in time during an experimental controlled wet condition, due to water percolation/evaporation through a relatively fixed mathematical scheme (Yiotis et al. 2004, 2006). The model of fluid transport through a porous material is well known in physical, industrial and geological literature (Dullien 1992). In the present study, we used a commercially available polyurethane sponge (Kendall Copa Plus; Tyco, Mansfield, MA, USA), with a density of 0.12 g/mL. Acoustic conduction velocity of the non-porous polymer is about 1700 m/s and its acoustic impedance is 1.8 Mrayls (Selfridge 1985). Interconnected porosity (%) of the models has been determined by measuring the dimensions and weight of the object:
Fig. 3. Echographic scanning technique of the phantom.
w p 5 12 ,100 r,V where p 5 porosity, w 5 weight, r 5 density of the polymer (1.04 g/mL) and V 5 volume of the model and turns out to be 88%. The polyurethane objects have been modeled to a thickness of 7 mm, comparable weights and a rectangular shape to fit the linear probe used for scans. Weight and volume of each phantom at its dry state was measured and their density derived as mp/V (g/mL). To carry out scans able to simulate both a focal position and one of a superficial, impermeable layer as in the real anatomic situation of the lung, the phantom was then covered by a 150 mm thick chloroprene polymer membrane (Biosynto, Mediflex, Italy) with a density of 1.31 g/mL and
Fig. 4. Drying curves of the 10 phantoms.
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acoustic impedance of 1.5 Mrayls (Selfridge 1985). A cylindrical chloroprene water-filled bag, with a diameter of 1 cm, was interposed between the probe and the phantom to create distance. Acoustic gel was used as coupling media between the probe and the water filled bag and between the bag and chloroprene membrane. Finally, a draining pad of polyurethane sponge, with a dimension of 100 3 100 3 7 mm, was placed under the wet models to favor, through capillarity and evaporation, a ‘‘drying’’ time not to exceed 180 min (Fig. 3). Room temperature during the experiment was 22 to 24 and humidity 50% to 60%. After the initial densitometric evaluation and scanning, dry phantoms were soaked in distilled and degassed water for 10 s (5 s per side), then extracted and withheld until dripping stopped. They were then weighed on an electronic precision balance (JAY 1003; Nanjing Oxy Technology & Trading Co., Nanjing, China) with reading accuracy 0.001 g at 4-min intervals thus creating a ‘‘drying curve’’ (Fig. 4). Echographic scans (three consecutive frozen acquisitions in 30 s) were also carried out at 4-min intervals, right after weight acquisition. The relative patterns, stored in the machine’s hard disk, served as material for future phase identification. Images were revised at the end of each procedure on the phantom according to the following criteria.
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‘‘Start’’ was a 4-min standard interval after water dipping: the echographic field has a variable, nonclassifiable echogenity. ‘‘End’’ was the end of the phase 5, with total artifact disappearance. Along the ‘‘drying curve’’, five phases were identified as follows. Phase 1, white: the echographic field is completely and homogenously echogenic. Phase 2, dense comet: echogenic overall aspect with initial dishomogeneity created by no more than 2 hypo/anechogenic vertical bands which are at least 2 mm thick. Phase 3, separate comet: evidence of separate comets which may be counted in a frozen image; there are thin, clear spaces between comets. Phase 4, thinning-out: each comet is clearly separated from the next with at least three intervals larger than 3 mm. Phase 5, exhaustion: five to 10 separate comets extending to the bottom of the field. Concordance among three different operators (GS, VG and CD) on each set of three images defined the various phases. Representative images of each phase are shown in Figure 5, including (A) the sonographic appearance of dry polyurethane. We recorded weight and (corrected) volume of the scaffolds at each echographic scan. For each measure taken, we calculated density corrected for the blowing effect due to dipping. The correction coefficient was determined through an
Fig. 5. Wet and dry polyurethane. (A) Dry polyurethane, a specular reflector. (B) Phase 1, white. (C) Phase 2, dense comet. (D) Phase 3, separate comet. (E) Phase 4, thinning out. (F) Phase 5, exhaustion.
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Table 1. Physical qualities of biologic tissues and synthetic material used in the study Acoustic media
Density (g/mL)
Acoustic impedance (Mrayls)
Porosity (%)
Sound velocity (m/s)
Attenuation at 1MHz (dB/cm)
Distilled water (20 C) Polyurethane polymer Polyurethane foam Chloroprene Muscular tissue Fat tissue Tissue (mean) Inflated lung (TLC) Deflated lung (FRC) Consolidated lung (pneumonia) Atelectatic lung Air (20 C)
0.998 1.04 0.12 1.31 1.07 0.92 1.05 0.15 0.5 0.76 0.84 0.012
1.5 1.8 0.1 1.5 1.7 1.3 1.63 0.1 0.4 0.6 1.4 0.00045
– 0 88 0 0 0 0 85 50 34 16 –
1480 1700 833 1510 1585 1450 1540 500 733 948 1660 343
0.0022 0.46 1.3–3.3 0.63 0.81 50
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TLC 5 total lung capacity; FRC 5 functional residual capacity. (Dunn and Fry 1961; Selfridge 1985; Tong and Fung 2001; Wells 1975, 1977).
estimate of the mean volumetric variation of 10 phantoms, similar in weight and dimensions, undergoing an analogous dipping/percolation treatment. Echographic scans of the dry and wet models were carried out with a commercially available machine (Aplio XV; Toshiba Medical Systems Europe, Rome, Italy), equipped with a 4 cm linear probe (Toshiba PLT 805 AT) operating at a frequency of 6.6 MHz, without tissue harmonics. A relatively low mechanical index of the ultrasound beam (the peak of rarefactional pressure in tissue divided by the square root of the ultrasound frequency) of 0.6 was used. The scan was perpendicular to the surface of the phantom and centered on the median line. We used a mechanic support system for the probe with the least possible compression through the acoustic gel. All images were stored on the machine’s hard disk. Table 1 shows densitometric, porimetric and acoustic characteristics of the polymers used compared with lung and thoracic, normal and pathologic tissue (Wells 1975). Table 2 reports reflection coefficients of the interface between aerated and nonaerated tissues, calculated for a normal acoustic impedance (Tong and Fung 2001; Wells 1975).
The described model theorizes time for appearance and density values of the phantom during the ‘‘drying curves’’ of the phantoms. We considered the beginning of phase 1 as the moment of collapse of the dry specular reflector. Analogously, temporal and densitometric data of phases 2, 3, 4 and 5 represent the values of porosity variation correlated to the expression of countable comets. Finally, the interval beyond the last phase and ‘‘end’’ defined the reconstitution of the specular reflector due to critical reduction in acoustic permeability of the scaffold. The parameters measured were: (1) the presence of a specular reflector in the ‘dry’ model and its eventual collapse caused by geometric/densitometric variations following water dipping; (2) different artifactual representation in relation to a variable geometry; and 3) correlation to substrate density. Numeric data were expressed as absolute values, means and standard deviations. Parametric series were compared through Pearson’s correlation coefficient. Comparisons between means were carried out with analysis of variance (ANOVA) and Bonferroni’s correction using SPSS for Windows version 14 (SPSS, Chicago, IL, USA). Statistic significance was considered when p # 0.05.
Table 2. Reflective properties of acoustic discontinuities in human chest and in polyurethane sponge Interface
Reflection coefficient* R
Water/air Muscle/air Fat/muscle Muscle/inflated lung Muscle/deflated lung Muscle/condensed lung (pneumonia) Muscle/atelectatic lung Spacer/dry polyurethane
20.99y 20.99 0.13 20.88 20.72 20.61 20.01 20.85
* Acoustic pressure reflected back from anatomic interfaces (1 5 maximal reflection, 0 5 maximal acoustic permeability (Dunn and Fry 1961; Selfridge 1985; Tong and Fung 2001; Wells 1975,1977). y The sign of R is negative because the impedance of the second medium is less than water and the lung acts as a pressure relief surface relative to water (Oelze et al. 2003).
RESULTS A total of 10 polyurethane phantoms 7 mm thick, mean volume 7.55 6 0.54 mL, range 6.8 to 8.3 mL, mean weight 0.909 6 0.065 g, range 0.817–0.997 g were studied. Water dipping increased mean weight to 2.541 6 0.186 g, range 2.197–2.880 g and decreased the porosity to around 71%. Following water dipping phantom volumes increased along a timeline including three phases: (1) instantaneous volume increase by 19%; (2) slow increase for 40 min (further increase 13.7%, global increase 35.6%); and (3) plateau up to 120 min with global volume increase of 44.5%. The time/volume curve of dimensional increase of wet phantoms furnished
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correction coefficients for density calculations in time and, thus, the ratio of weight to corrected volume. For each scaffold, a ‘‘dewetting’’ curve was created by calculating weight at 4-min intervals. Variation of weight-intime curves are represented in Figure 4. Curves show a time (21) characterized by the initial dry weight and a final time identifying the end of evaluation. The latter values varied with a mean value of 128 6 28.47 min, range 104–176 min. A correlation existed between wet weight and time to dry (R 5 0.73, p , 0.05) but not between these times and dry scaffold weight. Figure 6 shows the mean and confidence interval (95%) of the starting time of each echographic phase through the drying period. Calculation of density in time for each scaffold showed a trend in reduction with a reciprocal increase in porosity toward a value around 83% at 120 min. Density of the ‘‘wet’’ scaffolds was in average 0.287 6 0.0304 g/mL; mean density at the beginning of the ‘‘white phase’’ was 0.258 6 0.0249 g/mL; mean density at the end of the experiment was 0.1438 6 0.0097 g/mL. Figure 7 shows mean values and confidence intervals of density for each model through all experimental phases. Table 3 lists mean densities, range and standard deviation of the phantoms at each characteristic phase. In each experimental case, echographic scans showed an organized progression from the white phase, through the dense comet phase, to thinning out of comets and finally to the reconstitution of the specular reflector, across decreasing values of density and reciprocal increasing values of porosity (from 71% to around 83%). Specifically, the phantom behaved as a specular reflector for values of density lower than 0.13 g/mL. In this case, the whole field under the acoustically imperme-
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Fig. 7. Phantom density values (g/mL, mean and confidence interval – 95%) in the five (1–5) different experimental phases. ‘‘Start’’ is 4-min standard interval after water dipping, ‘‘end’’ represents total artifact disappearance.
able surface was practically anechogenic so that even a metallic object, as 20 to 16 Gauge needles, placed inside the scaffold became invisible. Artifacts started appearing, in a constant progression, for values of density going from 0.132 g/mL to 0.34 g/mL. The ‘‘white phase’’ was preceded by a period no longer than 4 min, in which the scaffold was hypoechogenic or with variable echogenicity, for values of mean density of 0.287 to 0.258 g/mL (Start). Throughout this period the scaffold was characterized by an elevated acoustic permeability, in that an 18 G needle inserted in the phantom was easily identifiable. The ‘‘white phase’’ was characterized by diffuse hyperechogeny. Mean density values of the phantom in this phase (0.258– 0.205 g/mL) were statistically different (p , 0.05) from those relative to the ‘‘separate comet’’ phase (mean density 0.188–0.172 g/mL). The same statistically significant difference characterized the difference in density from the ‘‘dense comet’’ phase to the ‘‘thinning-out’’ phase and between ‘‘separate comet’’ phase and Table 3. Mean densities, range and standard deviation of the phantoms at each characteristic phase Phases N Mean density Standard deviation Minimum Maximum
Fig. 6. Starting time (in minutes, mean and confidence interval – 95%) of the experimental phases characterized by artifacts of variable density. (1: White; 2: Dense comet; 3: Separate comet; 4: Thinning-out; 5: Exhaustion.).
Start 1 2 3 4 5 End Total
10 10 10 10 10 10 10 70
0.2879 0.2581 0.2052 0.1882 0.1723 0.1576 0.1438 0.2018
0.0304 0.0249 0.0218 0.0186 0.0158 0.0107 0.0097 0.0531
0.256 0.230 0.175 0.153 0.146 0.142 0.132 0.132
0.340 0.319 0.250 0.219 0.198 0.175 0.160 0.340
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‘‘exhaustion’’ phase. Densitometric comparisons for contiguous phases 1 through 5 did not result statistically significant. DISCUSSION The three main presuppositions of this study were that: (1) Normal lung behaves, at the pleural level, as a specular reflector with an in vivo reflection coefficient of 0.88 (Wells 1977). Absence of artifacts indicates massive, homogeneous reflection, which, in fact, produces horizontal repetitive reflections (A-lines), as transducer reverberations (Dunn and Fry 1961). (2) Artefactual phenomenons in the pathologic lung, as hyperechogeny (white lung), lung comets (B-lines), micro and macro consolidations, appear in realtime sonography as signals of ‘‘acoustic permeabilization’’ of the pleural plane, with consequent physical interactions (probably multiple variable reflections) of the ultrasound beam with the more or less aerated subpleural tissue. (3) General biophysical evidence, as well as dedicated studies, has indicated how lung acoustic permeability is a density correlated phenomenon, so that acoustic interaction between the ultrasound beam and the pulmonary parenchyma increases as lung density approaches that of water (Dunn 1974; Oelze et al. 2008). The use of a phantom with acoustic characteristics comparable to those of lung tissue (in its air and solid compartments) and with a porosity or density that varied in time, allowed us to confirm these presuppositions through two main important aspects that will be synthetically and qualitatively explained: (1) the drying curve (Yiotis et al. 2004) of porous materials and its transition points (as large scale superficial phenomenons in the phantom); and (2) the theoretic concept of ‘‘percolation’’ or ‘‘geometrical phase transition’’ (Dullien 1992; Yiotis et al. 2004) in a three-dimensional (3-D), finite, latex structure (for small scale phenomenons of the superficial interface of the phantom). In a microporous interconnected and wet material, phenomenons of capillarity prevail. A completely soaked phantom with all its air spaces filled with water (occupation probability of 1, represents a liquid cluster with total vertical hydraulic (and obviously acoustic) connectivity (Oelze et al. 2008; Szabo 2004). Acoustic permeability in such a case is close to that of water (Yiotis 2007). From the clinical/practical point of view this situation is represented by scanning of a lung consolidation (as air deprived pneumonia or atelectasis) (Bouhemad et al. 2010). Passive water soaking in a sponge is only partial for physical reasons. That obtained in this experiment (with a resultant phantom’s porosity of 71%) was characterized
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by an initial transitory phase of capillarity driven redistribution of about 4 min before appearance of the ‘‘white’’ phase. This first phase produces a large number of superficial acoustic interactions own to a high superficial connection (Yiotis et al. 2006). The subsequent phases identified, through the presence of objectively identifiable artifactual phenomenons, a progressively declining superficial acoustic permeability. Such permeability resulted density or porosity dependent. Through these phases our drying curves showed a behavior comparable to a drying constant rate period (DCRP) which, in line with Yiotis (2004 and 2006), is characterized by water excess on the model’s porous surface. During the DCRP, capillarity controls water flow from inside the pore space to the surface of the phantom, where water evaporates. Liquid flows through either completely or partially wet pores and pore walls are either covered with water or have water in the corners and the central part dry. This way the air/water interface takes the shape of a meniscus reflecting the need of creating a particular contact angle with the solid and the tendency of minimizing interfacial area within the pore. It is therefore allowed to state that, in a partially soaked capillary system, the formation of many air clusters with a curvilinear delimitation is possible. The drying curves terminated with the exhaustion of comets and the reconstitution of the phantom’s acoustically impermeable surface notwithstanding residual hydration and thus greater density. Further dehydration would have followed faster kinetics as the falling rate period (FRP) in which drying is controlled by mass transfer through the dry pore space. In our model this phase was without comets and the phantom’s surface behaved as a specular reflector inside the DCRP, probably for the presence of a complete superficial gaseous cluster. In our study, acoustic artifacts appeared solely in the dewetting DCRP phase, characterized by relatively reproducible values of mean density and especially by characteristic geometry of aqueous clusters. In line with the literature (Dullien 1992; Yiotis et al. 2004; Yiotis et al. 2006), DCRP corresponds to the phase in which the main liquid cluster (MLC) is formed and predominates. From the geometrical point of view, this means that certain gas percolations exist in the model but during the drying period most liquid pores belong to the sample-spanning liquid cluster (main liquid cluster, MLC) and only a percentage of liquid pores belong to isolated liquid clusters (disconnected clusters, DC). The MLC maintains a superficial connectivity and induces an acoustic permeability that is function of the probability of pore filling. This principle is defined, on large scale, by the mean porosity value of the scaffold but from the geometrical point of view and on small (very superficial) scale, superficial connectivity of the MLC will become
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Fig. 8. Effect of the geometric variation of a porous, permeable structure, with variable water occupation probability p, on its acoustic permeability. (X-Y: two-dimensional (2-D) latex, Z: third dimension, not shown). Black: full, White: empty. At the right and left side of the graphical scheme the corresponding echographic representation on polyurethane phantom. (A) p 5 0, completely aerated substrate (i.e., normal lung). (B) p 5 1, completely full substrate (i.e., lung condensation), complete permeabilization (arrows). (C) p 5 0.96, total superficial connection, the empty cell generates the central reflective spot. (D) p 5 0.96, superficial disconnection focus, the empty cell is analogous to a small air bubble in a liquid medium (focal reflective spot). (E) p 5 0.78, aerous spanning cluster, coexistence of two main liquid clusters (MLC); combination and amplification of (C) and (D). (F) p5 0.87, superficial disconnection of an MLC able to capture ultrasound. (G) p 5 0.75, similar superficial disconnection with different configuration. (H) p 5 0.43, complete superficial disconnection, reconstitution of the specular reflector. Only (F) and (G) geometries produce comet-tail artifacts in the spots indicated by the arrows which can actually repeat themselves on the surface. (A) and (H) are acoustically and sonographically equivalent.
more and more irregular in time. This progressive disconnection of the MLC, which preludes the formation of a minimum superficial air content for which the structure will no longer be superficially permeable to ultrasound, may be studied through latex percolation. From the practical point of view, this means that in our model during the ‘‘dewetting’’ comet producing phase, there is an irregularly interconnected, superficial MLC (whose superficial pores are randomly either full or empty), with progressively declining interconnection in relation to structure density and porosity (Fig. 8). Superficial connections may be surrounded by air gaining the role of acoustic traps (or acoustic holes) with variable concentration. At this level, the specular reflector loses its integrity producing multiple focal reflection points with
reverberating potential and casually modulated by either constructive or destructive interference. As the number of acoustic holes grows denser, geometry will evermore resemble a comet producing bilayer bubble system in a liquid medium (Soldati et al. 2009). Finally, the specular reflector will be reconstructed once the MLC and the DC are no longer superficially connected.
CONCLUSIONS This study validates the following hypothesis: (1) No matter what the physical nature or genesis of the radio-frequency (RF) signal, comets created in the phantom represent superficial, artifactual, density
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(3)
(4)
(5)
Ultrasound in Medicine and Biology
correlated phenomenons due to a physical modification of the specular reflector in a dry model. Acoustic permeability of a microporous tissue is density dependent (O’Brien et al. 2002; Oelze et al. 2003; Dunn 1986): lower porosity induces greater acoustic permeability and greater acoustic interactions with the aerated superficial structures. Dominant ‘‘anatomic’’ structures are not necessarily involved in the genesis of comets. It is a random phenomenon. Comet concentration and ‘‘white’’ are correlated on the large scale and for dimensions of the vertical substrate within 7 mm, with substrate mean density. On the small scale and superficial level, with geometry of discrete air spaces as described in the percolation theory (Yiotis et al. 2006). The most efficient air space geometry for the production of artifacts is that of a bubble millimetric bilayer that typically, in an elementary gel model, produces comets (Soldati et al. 2009).
We believe that further validation of the above points would contribute to ameliorate the diagnostic power of chest sonography. A clear correlation between artifactual subpleural components and nonconsolidating density/ tissue geometry would allow quantification of interstitial pathology at the cortical level. This could furthermore contribute to perfectionating lung ultrasonographic exploration systems in terms of acoustic spectrography. This study has certain limits. A systematic RF analysis of the signals relative to artifacts has not been carried out so that their dependence on the frequency used is not known. Artifacts are in fact comparable to those observed in pathologic lung only upon an inspective (visual) examination. Geometric behavior of phantom air spaces during the ‘‘dewetting’’ phase was deduced from studies relative to different, although structurally similar, materials. The vertical density gradient of the phantom through the ‘‘dewetting’’ phases was assumed to be null (gravity stabilized) so that a positive gravity-dependent gradient (however, present) was ignored and this is actually a simplification of the model. Finally, for the estimate of artifact formation, a standard, commercially available real-time diagnostic system with fixed frequencies was used and its purpose is certainly not that of quantifying artifacts. REFERENCES Avruch L, Cooperberg PL. The ring down artifact. J Ultrasound Med 1985;4:21–28. Bouhemad B, Liu ZH, Arbelot C, Zhang M, Ferrari F, Le-Guen M, Girard M, Lu Q, Rouby JJ. Ultrasound assessment of antibioticinduced pulmonary reareation in ventilator associated pneumonia. Crit Care Med 2010;38:84–92. Copetti R, Soldati G, Copetti P. Chest sonography: A useful tool to differentiate acute cardiogenic pulmonary edema from acute respiratory distress syndrome. Cardiovasc Ultrasound 2008;6:16.
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