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Passive Elastography: Shear-Wave

Tomography From Physiological-Noise
Correlation in Soft Tissues

Article in IEEE Transactions on Ultrasonics Ferroelectrics and Frequency Control · July 2011
DOI: 10.1109/TUFFC.2011.1920 · Source: IEEE Xplore

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Passive Elastography: Shear-Wave Tomography from Physiological-Noise Correlation
in Tissues

T. Gallot,1 S. Catheline,1 P. Roux,1 J. Brum,2 N. Benech,2 and C. Negreira2

1 Laboratoire de Géophysique Interne et Tectonophysique,
CNRS-Université J. Fourier, 38041 Grenoble, France
2 Laboratorio de Acústica Ultrasonora, Instituto de Física Facultad de Ciencias,
Universidad de la República Montevideo - Uruguay, 11400 Montevideo - Uruguay
Inspired by seismic-noise correlation and time reversal, a shear-wave tomography of soft tissues
using an ultrasonic scanner is presented here. Free from the need for controlled shear-wave sources,
this passive elastography is based on Green's function retrieval and takes advantage of the permanent
physiological noise of the human body. Results with hydrogels indicate that this tomography tech-
nique is compatible with low frame rates used by conventional echographic and magnetic-resonance
imaging devices. Furthermore, in-vivo experiments on the liver demonstrate the pertinence of ap-
plying tools of seismology in the eld of medical imaging. Passive elastography should now provide
benets for medical applications, whereby determination of local tissue elasticity can support and
improve diagnostic condence.
PACS numbers: pacs number...

Correlation of noise-like signals is a recent method for
the extraction of information from multiply scattered
wave elds [1]. The most important application to date
relates to geophysics and crustal tomography obtained
from seismic-noise correlation [2, 3]. This consists of
extracting a surface-wave velocity map from the low-
amplitude permanent ambient noise in the earth sub-
surface. Passive imaging methods based on noise cor-
relation have also been successfully developed in various
other domains and at various scales, such as in helioseis-
mology [4, 5], oceanography [6, 7], and ultrasonics [8].
Due to muscular activity, there is physiological acous-
tic noise in the body, and this can be used to extract
the mechanical properties of tissues. Recently, Sabra et
al. showed [9] that the natural vibrations of contracting
muscles can provide measurements of their global vis-
coelastic properties. In the present study, passive in-vivo
tomography of soft tissues is proposed, based on the cor-
relation of a physiological noise eld. This natural elastic
eld that is dominated by low-speed shear waves is per-
manently induced by breathing and cardiac activities. It
can be measured at the body surface using ultrasonic
techniques that have been developed in the eld of elas-
tography, which are similar to Doppler methods [10, 11].
At present, an ultrasonic device in the MHz frequency
band can record the motion of the ultrasonic speckle at a
rate of 1,000 frames per second. This ultrafast imaging is
needed to measure shear-wave propagation in the human
body, where the typical frequencies range from 10 Hz to
300 Hz. Using this technology, the active methods that
are dened as transient elastography take advantage of
an external source [12] or a radiation force [13] to clini-
cally characterize the elasticity of soft biological tissues
[14, 15]. Two improvements are proposed in the present
study: rst, the shear-wave source is removed and the
method becomes purely passive, in the sense that it only
relies on the shear noise within the human body. Sec-
ond, we demonstrate that the technique is compatible
with conventional low-frequency imaging devices.
The feasibility of this correlation-based passive tomog-
raphy is rst presented in a tissue-mimicking-phantom of
polyvinyl alcohol (PVA gel; [16]). Contrary to seismol-
ogy, where the seismic noise can only be recorded at or
close to the earcth surface, ultrasound in soft solids al-
lows the measurement of the particle velocity inside the
volume along ultrasonic beams (z -axis in Fig. 1A). A 64-
transducer array connected to a Lecoeur ultrafast scan-
ner was used to measure the ultrasonic echoes from a ho-
mogeneous distribution of scatterers inside the PVA gel,
with a repetition frequency of 1 kHz. Speckle interferom-
etry algorithms allowed the tracking of the echoes and
deduced the scatterer displacement between each shot.
As proof of concept for passive tomography, a 9 s noise-
like elastic eld was created by nger impacts applied
randomly all over the surface (Fig. 1A). To give the
same weight to each frequency, a whitening processing
was applied between 10 Hz and 200 Hz. The displace-
ment ψz (0, t) along the rst transducer at 3 cm inside
the gel is shown in Figure 1B. The zoom of 0.5 s of the
displacement eld along one line parallel to the array (x -
axis) is shown as a color-scale map (Fig. 1C). The n-
ger impacts generated a low-frequency random-like dis-
placement eld that was dominated by shear waves that
clearly showed strong spatial coherence along the x-axis;
e.g., around t = 1.4 s in Figure 1C.
The cross-correlation C (x0 , x; t) processed at two
points x0 and x should naturally highlight the spatio-
temporal coherence of the noise-induced displacement
eld, as in Eq. (1).
C (x0 , x; t) = ψz (x0 , T − t) ⊗ ψz (x, t) (1)
In the case of a spatially homogeneous distribution of

Figure 1: A) Experimental set-up for the in-vitro correlation-
based tomography. A complex shear-wave eld was created
by nger impacts applied to the surface of a tissue-mimicking
phantom (PVA gel). Displacements were measured inside the
volume using an ultrafast ultrasonic scanner and elastography
algorithms. B) The z -component of the particle velocity at x
= 0, z = 3 cm, the rst point of the red line. C) The zoom
of 0.5 s of the particle velocity along the red line shows the
wave propagation around 1.4 s.
white noise sources [17], the noise-correlation function
C (x0 , x; t) can be shown to be related to the Green's
function G(x0 , x; t) between xo and x, according to Eq.
(2):
d ods were compared to measure the local shear velocity,
C(x0 , x; t) = G(x0 , x; −t) − G(x0 , x; t) (2)
dt
The analogy with time-reversal (TR) physics [18] follows
directly from Eq. (2), as the sum of the causal and
acausal Green's function is exactly what would be ob-
served on x in a perfect TR eld with a source at x0
sending a pulse at t = 0 s [19]. In this interpretation, the
correlation function consists of using each noise source
excited by the nger impacts as part of a TR mirror that
refocuses on x0 [20]. This noise-correlation-based refo-
cusing is similar to the TR eld of elastic waves that were
recently observed in a soft solid cavity [21]. The noise-
correlation function C(x0 , x; t) is shown for six refocusing
spots x0 (Fig. 2). For each position, the amplitude was
maximal at x = x0 and t = 0, as predicted by Eq. (2).
The classical cross-shape of a focused eld was seen along
the x-axis, showing the converging wave for t < 0, the
refocusing at t = 0, and the diverging wave for t > 0.
The TR eld emerges on each spot without the need for
any extra spatial averaging. Compared to the equivalent
TR experiment using a unique point-like source in soft
solids [21], a signicant improvement in signal-to-noise-
ratio is obtained in this correlation-based experiment,
where many nger impacts can create a quasi-random
noise-like eld. Indeed, to provide the local speed esti-
2
Figure 2: Correlation maps measured at six refocusing spots
x0 in a homogeneous hydrogel. The converging and diverging
waves are responsible for this typical cross-like shape of the
TR eld in this spatio-temporal representation. The group
velocity of these waves can be estimated from the delay δt of
the maximum of the eld along δx (bottom right). Another
approach estimates the -6 dB focal spot width close to the
half wavelength λ/2(top right).
mation of the shear waves at each position,correlation-
based techniques take advantage of: 1) the spatial diver-
sity of the noise sources; and 2) the long duration of the
noise recording. In the following, two independent meth-
which in soft solids is directly related to the elasticity
properties.
Two PVA phantoms were prepared with dierent scat-
terer concentrations. The stiness was independent of
the scatterer concentrations [16], although it created an
apparent interface on a sonogram (Fig. 3A). The sti-
ness of this hydrogel was controlled by the number of
freeze-thaw cycles: one cycle for the soft gel on the top
(0 < z < 15 e 20 mm), and ve cycles for the sti gel
below. Transient elastography [10] was used for the stan-
dard measurement of the shear velocities, as 4.3 m/s and
1.2 m/s respectively.
In the rst method, the speed of the converging and
diverging shear waves were measured. According to elas-
ticity theory, the speed is the key parameter, as the shear-
wave speed cs is related to the shear elasticity µ and also
µ 3E
to the Young's modulus E , according to : c2s = ≈ .
ρ ρ
The whole frequency spectrum of the refocusing was used
to estimate the local group velocity. Spatial ltering was
applied to the correlation eld to select only one direc-
tion of propagation (e.g., along the x-positive direction).
The group velocity at frequencies ranging from 10 Hz to
100 Hz were deduced from the delays δt between two con-
secutive local eld maxima separated by δx = 0.8 mm.

For the sake of clarity, δx was set at 18 mm for Figure
2 (bottom right panel). This technique was applied to
construct the shear-wave-speed tomography of the two-
layered hydrogel. The velocity along the x-axis was es-
timated for 83 lines at successive depths, resulting in a
49×49 mm² stiness map. The shear velocity is shown as
a color-scale map (Fig. 3B). The averaged shear velocity
in the two media, at 4.8 m/s and 1.7 m/s, were close to
the measurements made by standard transient elastog-
raphy [10]. Furthermore, the interface between the two
media that was seen from the ultrasonic echoes in Figure
3a closely matched the shear-velocity map (Fig. 3B).
Figure 3: A) Sonogram of the bilayer hydrogel, where the
two layers with dierent scatterer concentrations are clearly
apparent. B) Shear-wave-speed tomography estimated
from local group-speed estimation. C) Shear-wavelength
tomography estimated from the refocusing width. D) Slow
shear-wavelength tomography estimated from a displace-
ment eld sampled at 50 Hz. The interface between the two
layers is in the same position in the four images, and good
quantitative agreement was found for the shear-speed values.
In a second method, the shear-wave speed was de-
duced from estimation of both the wavelength and the
frequency, through the relationship v = λ f . In a TR
eld, the Rayleigh criteria stipulate that the focal spot
width is close to the half wavelength [22]. Consequently,
the -6 dB width measured for each position → −
r0 of Fig-
ure 2 (top right panel), gives the wavelength estimation
directly. This is known as the spatial auto-correlation
method in seismology [23], and it is based on the correla-
tion function C (→−
r0 , →
−
r ; 0) at the refocusing time (t = 0)
between seismic stations, or in the present study, between
the refocusing point → −
r0 and the 64 × 83 acquisition points
3
→
−
r , as in Eq. (3):
ˆ T
C (→
−
r0 , →
−
r ; 0) = ψz (→
−
r0 , τ ) .ψz (→
−
r , τ ) dτ (3)
0
To benet from the self-averaging properties of the TR
process [24], the refocusing was computed using a large
frequency bandwidth. In this bandwidth, the frequency
associated with the estimated wavelength was the up-
per frequency fmax [25]. Consequently, for an easier
comparison, the wavelength tomography was translated
into speed tomography (Fig. 3B), using the relationship
v =λf .
Basically, the wavelength tomography of this second
method was independent of the speed tomography of the
rst method. However, opportunely, they coincided (Fig.
3B and C). In both of the layers, the average wave speed
was 4.1 m/s and 1.7 m/s for the sti and the soft gels,
respectively, which was in good agreement with the classi-
cal active-transient elastography measurements (4.3 m/s
and 1.2 m/s). The wavelength approach, however, was
more robust with regard to the signal-to-noise ratio [25],
as the wavelength was estimated when the intensity was
maximal.
A second advantage of this wavelength tomography is
its compatibility with slow imaging devices that cannot
reach the typical 1 kHz sampling frequency of an ultrafast
scanner. Under the Shannon frequency (< 400 Hz), the
temporal coherence of the experimental elastic eld was
progressively lost, as the maximum observed frequency
was around 200 Hz. However, in the worst case, despite
a total loss of time coherence, the spatial coherence was
conserved and the refocusing map can still be used for
wavelength estimation. Mathematically, this loss of time
coherence can be written according to Eq. (4), by adding
a random phase φ to the time argument of the displace-
ment ψz :
ˆ
T
Cφ (→
−
r0 , →
−
r ; 0) = ψz (→
−
r0 , φ (τ )) .ψz (→
−
r , φ (τ )) dτ (4)
0
Due to the time integration, this phase does not mod-
ify the correlation map at t = 0, C (→ −
r0 , →
−
r ; 0) =
→
− →
−
Cφ ( r0 , r ; 0). This means that the estimation of wave-
length tomography is feasible, despite the slow imaging
frequency. However, the loss in the frequency information
prevents estimation of the maximum frequency, and the
shear speed cannot be deduced directly. Thus, only the
shear wavelength was used to construct the tomography
shown in Figure 3D. In this experimental demonstration,
a 50-Hz sampling frequency was used. The interface was
clearly apparent, with the contrast between the two lay-
ers similar to that seen for Figure 3B and C. To relate
the measured wavelength to the shear speed, the maxi-
mum frequency was estimated from the raw displacement
eld sampled at 1 kHz. On a conventional ultrasonic de-
vice, this estimation can be performed in a limited region

of interest, as for the Doppler mode. The maximum fre-
quency was around fmax '50 Hz, which implied averaged
shear-wave speeds of 3.7 m/s and 1.9 m/s in the hard and
soft gels, respectively, which were close to the expected
values.
In these phantom experiments, the noise-like elastic
eld was created by nger impacts. For the in-vivo exper-
iment, the physiologic noise that is permanently present
in the body creates a natural complex shear-wave eld.
Thus the liver was imaged at a 750-Hz repetition fre-
quency, by placing the transducer array under the ribs
of the subject (Fig. 4A). In Figure 4B, the particle dis-
placements in the low-frequency bandwidth from 5 Hz to
70 Hz are mainly due to cardiac activity. The displace-
ment eld in the liver shows a cardiac pulse each 0.5 s,
followed by reverberation and scattering. This complex
eld was used to compute the correlation function (Fig.
4C).
Figure 4: A) Experimental set-up for the in-vivo correlation-
based tomography: an ultrafast scanner was used to measure
the natural displacement eld in the liver region. B) The par-
ticle velocity along an acquisition line at 4 cm, and parallel to
the array, shows the physiological elastic eld. C) In the cor-
relation map C(x0 , x; t) with x0 = 14 mm, only one direction
of propagation emerged from the refocusing eld.
Compared to the refocusing eld in Figure 2, only one
branch of the cross-shape was recovered, which can be
explained by the strong directivity of the eld. In other
words, using a TR analogy, we were not dealing here with
a perfect TR cavity, where the converging wave was com-
ing from all directions of a closed surface, but rather with
a TR mirror that was located around the heart region and
that was re-emitting waves in the direction of the liver.
In addition to this problem of directivity, it should be
noted that the particle velocity amplitudes were weak,
at only 7.5 mm/s, which was quite close to the sensi-
tivity limit of the elastography, at around 1 mm/s. For
these two reasons, only the more robust technique, i.e.,
the wavelength approach, was used for in-vivo passive
tomography.
In the sonogram data (Fig. 5A), two zones were visi-
ble. Above z ' 12 mm, the bright region corresponded
4
to the abdominal muscles, whereas the dark region was
the liver. Good correspondence was seen with the shear-
wave-speed tomography (Fig. 5B), where the interface
between these two regions was seen around z ' 12mm. In
muscle and liver, the averaged shear-wave speeds were in
quantitative agreement with other studies [26, 27]. The
variability of the reconstructed tomographies shown in
Figures 3 and 5 are believed to be related to the direc-
tivity variance of the shear-wave eld. Indeed, it is well
established in seismology that the ux resulting from a
diuse eld [28, 29] can be responsible for bias in the to-
mography. Special eorts need to be made to compensate
for this eect.
Figure 5: A) Sonogram of the liver region. The interface
between the abdominal muscles and the liver is visible around
z = 12 mm. B) The passive shear-wave-speed tomography
from the correlation width clearly shows the two regions. The
averaged shear-speed estimations are in agreement with values
in the literature.
In summary, while other stiness-tomography tech-
niques actually suer from the physiological noise in
the human body, the proposed method takes advantage
of this permanent elastic eld as passive elastography,
in the sense that no articial shear-wave sources were
needed. Future studies will focus on the heart, where
elastography with active methods is only achievable with
diculty. Passive elastography is also compatible with
low-frequency acquisition systems, such as standard two-
dimensional and three-dimensional ultrasound and mag-
netic resonance.
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