You are on page 1of 9

2098 IEEE TRANSACTIONS ON MEDICAL IMAGING, VOL. 35, NO.

9, SEPTEMBER 2016

Probe Oscillation Shear Elastography (PROSE):


A High Frame-Rate Method for Two-Dimensional
Ultrasound Shear Wave Elastography
Daniel C. Mellema, Student Member, IEEE, Pengfei Song, Member, IEEE, Randall R. Kinnick,
Matthew W. Urban, Senior Member, IEEE, James F. Greenleaf, Life Fellow, IEEE,
Armando Manduca, Member, IEEE, and Shigao Chen*, Member, IEEE

Abstract—Ultrasound shear wave elastography (SWE) utilizes Index Terms—Inclusion, mechanical vibration, shear wave, ul-
the propagation of induced shear waves to characterize the shear trasound elastography.
modulus of soft tissue. Many methods rely on an acoustic radia-
tion force (ARF) “push beam” to generate shear waves. However,
specialized hardware is required to generate the push beams, and I. INTRODUCTION
the thermal stress that is placed upon the ultrasound system, trans-
ducer, and tissue by the push beams currently limits the frame-rate
to about 1 Hz. These constraints have limited the implementation
of ARF to high-end clinical systems. This paper presents Probe
Oscillation Shear Elastography (PROSE) as an alternative method
I N MEDICAL practice, physicians have long used manual
palpation of soft tissues as a method to aid medical diag-
nosis. While effective, this is a qualitative process that is limited
to measure tissue elasticity. PROSE generates shear waves using a
harmonic mechanical vibration of an ultrasound transducer, while
to superficial tissues and suffers from inter-rater variability due
simultaneously detecting motion with the same transducer under to the subjective nature of the technique. To address these limita-
pulse-echo mode. Motion of the transducer during detection pro- tions, elasticity imaging has been developed to provide non-in-
duces a “strain-like” compression artifact that is coupled with the vasive and objective quantification of the mechanical proper-
observed shear waves. A novel symmetric sampling scheme is pro- ties of tissue [1]. While many different techniques have been
posed such that pulse-echo detection events are acquired when the
ultrasound transducer returns to the same physical position, al-
developed to quantify these properties [2]–[11], many of these
lowing the shear waves to be decoupled from the compression ar- techniques utilize the propagation of induced shear waves as a
tifact. Full field-of-view (FOV) two-dimensional (2D) shear wave surrogate for, or to quantitatively estimate the shear modulus of
speed images were obtained by applying a local frequency estima- soft tissue. Assuming soft tissues are incompressible, isotropic,
tion (LFE) technique, capable of generating a 2D map from a single linear, and elastic, the shear modulus can be related to shear
frame of shear wave motion. The shear wave imaging frame rate
of PROSE is comparable to the vibration frequency, which can be
wave propagation speed, , by
an order of magnitude higher than ARF based techniques. PROSE
was able to produce smooth and accurate shear wave images from (1)
three homogeneous phantoms with different moduli, with an ef-
fective frame rate of 300 Hz. An inclusion phantom study showed where is density and can be assumed to be for
that increased vibration frequencies improved the accuracy of in- all soft tissues [10]. This relationship allows the shear modulus
clusion imaging, and allowed targets as small as 6.5 mm to be re- to be calculated from the propagation speed of the induced shear
solved with good contrast (contrast-to-noise ratio ) be-
wave.
tween the target and background.
Acoustic radiation force (ARF) based techniques have been
successfully used to generate shear waves within soft tissue.
Manuscript received February 02, 2016; revised March 18, 2016; accepted
This is done by utilizing an ultrasound push beam to displace
March 24, 2016. Date of publication April 04, 2016; date of current version
August 30, 2016. This work was supported by the National Institutes of Health soft tissue and track the propagation of the resulting shear waves
(NIH) grant DK106957. This work was supported by the National Institutes in pulse-echo mode to produce quantitative estimates of tissue
of Health (NIH) grant DK106957. The content is solely the responsibility of
stiffness [2], [3], [5], [6], [8], [9], [11]. While ARF shear wave
the authors and does not necessarily represent the official views of the NIDDK
and NIH. Mayo Clinic and some of the authors have financial interest in the elastography (SWE) methods have proved to be a versatile tool
technology described here. Asterisk indicates corresponding author. for evaluation of the mechanical properties of tissue [12]–[14],
D. C. Mellema is with the Mayo Graduate School and the Department of
this technique suffers from two major drawbacks. The first is
Radiology, Mayo Clinic College of Medicine, Rochester, MN 55905 USA.
P. Song and M. W. Urban are with the Department of Radiology, Mayo Clinic that the high voltage push beam used to generate shear waves re-
College of Medicine, Rochester, MN 55905 USA. quires upgraded hardware, including power supplies and trans-
R. R. Kinnick, J. F. Greenleaf, and A. Manduca are with the Department
mission circuits, which limits the accessibility of ARF SWE
of Physiology and Biomedical Engineering, Mayo Clinic College of Medicine,
Rochester, MN 55905 USA. techniques to dedicated research platforms and high-end clin-
*S. Chen is with the Department of Radiology, Mayo Clinic College of ical systems [2], [15]–[17]. Secondly, the delivered push beams
Medicine, Rochester, MN 55905 USA.
places thermal stress on the hardware, ultrasound transducer,
Color versions of one or more of the figures in this paper are available online
at http://ieeexplore.ieee.org. and tissue, ultimately limiting the typical elastography frame-
Digital Object Identifier 10.1109/TMI.2016.2550007 rate to about 1 Hz [18] to provide hardware cooling time and

0278-0062 © 2016 IEEE. Personal use is permitted, but republication/redistribution requires IEEE permission.
See http://www.ieee.org/publications_standards/publications/rights/index.html for more information.

Authorized licensed use limited to: Universidad Autonoma de Baja California. Downloaded on September 19,2020 at 21:15:53 UTC from IEEE Xplore. Restrictions apply.
MELLEMA et al.: PROSE: A HIGH FRAME-RATE METHOD FOR TWO-DIMENSIONAL ULTRASOUND SHEAR WAVE ELASTOGRAPHY 2099

prevent tissue damage. While the low frame-rate is not pro-


hibitive for imaging static soft tissues, it currently is not suit-
able to image dynamic soft tissues or for the real-time survey of
large three-dimensional regions.
There are many alternatives to generate shear waves without
the use of an ARF-based push beam. Twenty five years ago,
Yamakoshi utilized a continuous sinusoidal vibration of a plate
placed adjacent to an ultrasound transducer to generate shear
waves, and used a phase based estimation technique to recover
the shear wave speed [10]. More recently Kevin Parker's group Fig. 1. A diagram depicting the equipment used to drive the transducer (Tx) vi-
has developed a method that utilizes multiple external vibra- bration system. A sinusoidal signal is output from a function generator and then
amplified to drive the voice-coil actuator. The voice-coil was mechanically se-
tion shear wave sources to produce a “crawling wave” field that cured to the leaf spring and the Tx was secured to the rest of the system through
can be used to compute the shear modulus [19], [20]. How- a custom fixture, allowing the entire system to vibrate. Shear waves are gener-
ever, both of these techniques require separate devices for the ated by the motion of the transducer in contact with the object's surface. Shear
waves were observed using standard pulse-echo detection.
generation and the detection of shear waves, which increases
the footprint of the measurement probe, and can cause diffi-
culty when investigating certain tissues due to physiological and the shear wave speed image was reconstructed using the
constraints (e.g., liver due to rib shadowing). Transient Elas- Local Frequency Estimation (LFE) processing method [24]. The
tography (TE), commercialized as Fibroscan (Echosens, Paris, efficacy of PROSE was evaluated through homogeneous and in-
France), has addressed this issue by using a small single ele- clusion phantom studies.
ment transducer to deliver a mechanical impulse to generate
a single longitudinally polarized transient shear wave into the II. METHODS
body that can be detected by the same ultrasound transducer
[8]. TE has the added advantage that the use of transient ex- A. Vibration System
citation avoids standing wave and other potential artifacts. As To generate shear wave motion, a custom vibration system
described by Sandrin [21], these longitudinally polarized shear was created, co-axially mounting a linear voice coil actuator
waves arise as result of the diffraction from a source of finite (BEI Kimco Magnetics, Vista, CA) to an L11–4v linear array
size as the summed contributions of transversely polarized shear ultrasound transducer (Verasonics Inc., Kirkland, WA) for use
waves coming from subsources give rise to a globally, longitu- with a Verasonics Vantage Ultrasound system (Verasonics Inc.,
dinally polarized shear wave on the axis of the vibrator. In a Kirkland, WA). A function generator (Agilent 33250A, Agilent
recent paper, Catheline and Benech demonstrate from the elas- Technologies, Inc., Santa Clara, CA, USA) was used to gen-
todynamic Green's function that there are longitudinal shear erate a sinusoidal driving signal for shear wave generation. This
waves that can be detected in both the near and far field [22]. output was connected to an amplifier (Crown D150A, Crown
TE has been widely applied in studying liver fibrosis; however, Audio, Inc., Elkhart, IN, USA; voltage gain: 26 dB) before being
FibroScan does not provide two-dimensional (2D) imaging and delivered to the voice-coil vibration system. To generate shear
is not suited for detection of local changes in tissue elasticity. It waves, the vibration system was manually held with a single
is feasible to extend TE to 2D [23], however these methods are hand such that the transducer was in continuous contact with
not capable of high frame-rate imaging as they require the gen- the tested object. The vibration system is depicted in Fig. 1.
erated shear wave to travel through the entire target and dissi-
pate, before a second image can be acquired. Therefore, there is B. Symmetric Detection
still a need for the development of a mechanically coupled shear The generated motion can be observed using a standard pulse-
wave device capable of producing high frame-rate 2D elastog- echo detection. However, the detected motion is comprised of
raphy images. three separate components: 1) the compressional wave gener-
In this paper we propose Probe Oscillation Shear Wave Elas- ated by the harmonic vibration of the transducer, 2) the shear
tography (PROSE) as a new method, which utilizes continuous waves generated in the same fashion, and 3) a compression ar-
mechanical vibration of the ultrasound transducer to produce tifact caused by transducer motion relative to the imaged tissue.
harmonic longitudinally polarized shear waves, similar to the This compression artifact arises from transducer compression
waves generated using TE, for 2D quantitative elastography from the surface producing deformations within the object sim-
while simultaneously acquiring the resulting shear wave motion ilar to deformation in quasi-static compression elastography.
using the same transducer under pulse-echo detection mode. To Fig. 2 illustrates how this effect arises when the transducer is
accomplish this, a standard ultrasound transducer was mounted moved by between two consecutive detection events. In a
co-axially with a custom made voice-coil actuator system, al- non-moving reference system, the relative displacement of a
lowing the transducer to vibrate in the axial direction. When the single scatterer (represented by grid intersections) is greatest at
system is placed in contact with an object, the motion at the face the surface whereas a scatterer at the bottom will not be dis-
of the transducer produces longitudinally polarized shear waves placed. This leads to a depth dependent displacement profile
to propagate within the contacted medium, which can be ob- that nonlinearly decreases with depth. If the transducer's frame
served using standard pulse-echo detection. Single frame shear of reference is used, as would be the case during pulse-echo
wave motion was obtained using a symmetric sampling scheme detection, the compression profile is small at the surface since

Authorized licensed use limited to: Universidad Autonoma de Baja California. Downloaded on September 19,2020 at 21:15:53 UTC from IEEE Xplore. Restrictions apply.
2100 IEEE TRANSACTIONS ON MEDICAL IMAGING, VOL. 35, NO. 9, SEPTEMBER 2016

adjusted such that the detection events occurred symmetrically


around the maximum and minimum transducer displacement,
with the time between two sequential detection events em-
pirically set as of the vibration period.

C. Motion Detection
Coherent compounding plane wave imaging [28], [29] was
used to detect the resulting motion (detection pulse center fre-
quency 6.25 MHz). As previously established, a three angle
Fig. 2. a). Compression of the transducer introduces deformation within the compounding method (steering angles of , 0 , and 2 )
medium, leading to a strain-like compression profile (c, black dashed line) that was utilized to increase the signal-to-noise-ratio (SNR) of the
contaminates the shear wave motion (c, black solid line). b) The proposed sym- shear wave signal without substantially reducing the effective
metric sampling scheme allows the transducer to return to the same physical
location between consecutive pulse-echo detection events, suppressing the com- frame rate [30]. Because the probe is continuously moving, each
pression artifact (c, grey line). steering angle will capture a slightly different image, resulting in
blurring of the final compounded images. However, it has been
previously established that as long as the transmission sequence
the scatterers' displacement is similar to that of the transducer, is identical, causing identical blurring patterns in each of the
whereas the scatters at the bottom will show a displacement compounded images, the underlying motion can still be success-
closer to the total amount the transducer was displaced (dashed fully recovered using standard motion calculation methods [31].
line in Fig. 2(c)). The resulting shear wave motion observed The spatial pixel resolution of the image was one ultrasound
by the transducer is contaminated by the compression profile wavelength (0.246 mm), and resulting field-of-view (FOV) of
(black line in Fig. 2(c)). It should be noted that with sinusoidal the investigated medium was . Particle ve-
probe motion the magnitude of the strain profile is not static, but locity was computed from the in-phase/quadrature (IQ) data of
will oscillate as the relative displacement of individual scatters consecutive frames utilizing a one-dimensional autocorrelation
changes as the probe moves through its cycle. method [32]. A three pixel spatial window was used for aver-
The effects of the compressional wave can be suppressed aging in the autocorrelation process, and a spatial
through spatial high-pass filtering [25], because the large dif- median filter was used to remove spurious noise from the re-
ferences in propagation speed of the compressional and shear sulting shear wave motion signal.
waves allows for clear separation of the wavelengths of the
two waves. However the compression artifact is more difficult D. Filtering Process
to decouple from the shear waves, and may cause complica- Once the shear wave motion was acquired using the sym-
tions when calculating the shear wave speed using time-of-flight metric detection scheme and particle velocity data was obtained
(TOF) or phase gradient methods if not properly suppressed using the autocorrelation process. A sixth order Butterworth
[26], [27]. Temporal filtering is unable to decouple the two ef- band-pass filter was applied to each frame to remove spatial
fects as they both oscillate with the same frequency; and spa- wavelengths representing shear wave speeds outside a prede-
tial filtering is ineffective as the spatial frequency content of the termined physiological range (cutoffs corresponding to 0.5–10
compression profile often overlaps with the spatial frequencies m/s). Because the shear wave propagation is primarily in the
of the shear waves. While it may be possible to estimate the axial direction, motion propagating in the lateral direction was
compression through a fitting-and-subtraction process, it is not removed by filtering the corresponding spatial Fourier domain
guaranteed to be accurate in the presence of tissue heterogeneity (k-space) components through the use of a rolled-off wedge
that would arise with inclusions. filter [33], [34].
Alternatively, because the transducer's motion is sinusoidal,
a sampling scheme can be implemented such that the two con- E. Local Shear Wave Speed Estimation
secutive pulse-echo events for motion detections are symmet- Sampling twice per period does not have the temporal reso-
rically spaced in time around the peak transducer displacement lution required to robustly estimate the shear wave speed using
position so the transducer is at the same physical location for standard TOF methods. However, since the shear waves were
the two pulse-echo events. Because pulse-echo motion detection harmonic in nature, LFE can be used to obtain a 2D shear wave
only detects relative motion between two pulse-echo events, speed image from a single frame of 2D shear wave data [24],
the compression profile is automatically suppressed and only [35], [36]. Because the LFE requires the Fourier Transform,
shear waves are “seen” by this symmetric detection scheme. wave motion was mirrored in the two spatial dimensions to
Fig. 2 shows the symmetric detection events at and and reduce the rippling effects in k-space due to discontinuous
the resulting shear wave motion detected without the compres- edges in the spatial domain. The resulting images were pro-
sion artifact (grey line, Fig. 2(c)). Thus, it is possible to acquire cessed using LFE to estimate the spatial wavelength at each
two symmetrically sampled shear wave images per cycle, one at pixel. The LFE utilized 10 frequency bands with half-octave
the maximum and one at the minimum of the transducer posi- scaling of the center frequency for each band, spanning the
tion. To accomplish the desired detection timing, a miniature ac- wavelengths corresponding to shear wave speeds of 0.5–10 m/s
celerometer (ADXL335, Analog Devices, Norwood, MA) was [24]. An additional weighting term was added to the estimation
mounted on the transducer. Ultrasound detection timing was method to compensate for changes in shear wave amplitude

Authorized licensed use limited to: Universidad Autonoma de Baja California. Downloaded on September 19,2020 at 21:15:53 UTC from IEEE Xplore. Restrictions apply.
MELLEMA et al.: PROSE: A HIGH FRAME-RATE METHOD FOR TWO-DIMENSIONAL ULTRASOUND SHEAR WAVE ELASTOGRAPHY 2101

Fig. 3. Results from evaluating the homogeneous phantoms with PROSE at 300 Hz. (a) A representative shear wave motion frame from the 25 kPa phantom.
(b) The reconstructed shear wave speed image from the 10 kPa phantom, (c) the 25 kPa phantom and (d) the 45 kPa phantom.

when transitioning from materials with different stiffness [37]. A single rectangular region-of-interest (ROI) was used to
Because the vibration frequency used to generate the shear calculate the mean and standard deviation of the shear wave
waves is known, the spatial wavelength maps were converted speed images. For comparison five shear wave speed images
to shear wave speed images using velocity of a shear wave in were acquired with a General Electric LOGIQ E9 scanner
the medium, (LE9; GE Healthcare, Wauwatosa, WI) equipped with an ARF
SWE method [15]. The mean and standard deviation from
(2) the LE9 (9L, Breast settings, 1 cm diameter circular ROIs)
measurements were used as a reference to compare with results
where is the known vibration frequency and is the measured of PROSE.
wavelength.
G. Inclusion Phantom Study
F. Homogeneous Phantom Study
To test the resolution capabilities of PROSE, a standard
Three tissue-mimicking homogeneous cylindrical phantoms stepped cylinder inclusion phantom (Model 049A, CIRS Inc.,
(Model 039, CIRS Inc., diameter 11.6 cm, height 14 cm; sound Norfolk, VA) was imaged. The nominal shear wave speed of
speed of 1540 m/s, ultrasound attenuation of 0.5 dB/cm/MHz) the Type IV inclusion is 5.2 m/s and provides good contrast to
with nominal Young's moduli (E) of 10, 25, and 45 kPa were im- the softer background material's shear wave speed of 2.9 m/s.
aged using the PROSE technique. It has been previously shown Since it is known that the resolution of the LFE is linked to
that for a perfectly elastic material the shear wave speeds can be the wavelength of the shear waves [40], the 10.4 mm Type IV
related to Young's modulus by, inclusion was imaged at 300 Hz, 350 Hz and 400 Hz vibration
frequency. A real-time B-mode imaging sequence was added
(3) to guide transducer placement and a reference B-mode image
was saved just prior to the initiation of PROSE acquisitions. To
resulting in nominal shear wave speeds of 1.83, 2.89, and 3.87
evaluate the ability of PROSE to resolve inclusions of various
m/s for the three phantoms [2]. Because it was previously shown
sizes, the 6.5, 10.4, and 16.7 mm inclusions were also imaged
that pre-compression of materials can change stiffness measure-
using a 400 Hz vibration frequency. For both of the inclusion
ments [38], [39], the transducer vibration system was manually
studies, circular ROIs containing the inclusions were selected
handheld on the surface of the phantom with care taken to min-
based on the reference B-mode image, whereas the ROI for
imize manual compression of the phantom. The motion of the
the background was a rectangle placed above the inclusion.
probe is on the order of millimeters, therefore, it is not expected
Five reference measurements were acquired using the LE9
that the vibration will substantially increase the shear modulus
(9L, Breast settings) for each of the three inclusions, using
of the phantom through the vibration cycle. Utilizing a trigger
circular ROI drawn with from the B-mode image, as well as
from the Verasonics system, a 300 Hz sinusoidal signal was ap-
the background (1 cm diameter circular ROI). The LE9 results
plied to the probe vibration system. Since the vibration system
were used as a reference to compare with PROSE results.
started from rest, a 150 ms warm-up period was added to ensure
that the system reached steady state. Immediately following the
warm-up period, the symmetric sampling scheme was initiated, III. RESULTS
allowing for continuous acquisition with a maximum effective Fig. 3 shows a frame of the shear wave motion signal and the
frame-rate of twice the vibration frequency. After motion de- shear wave speed images obtained with PROSE from the homo-
modulation, the two resulting motion frames were processed geneous phantoms. The measured shear wave speed estimates
using spatial wedge and band-pass filters, and shear wave speed were , , and
images were generated using LFE. A final estimate of the shear for the 10 kPa, 25 kPa and 45 kPa phantoms, respectively, com-
wave speed was obtained by averaging the two images obtained pared to , , and ,
at the maximum and minimum displacement. respectively, using the LE9 (Fig. 4).

Authorized licensed use limited to: Universidad Autonoma de Baja California. Downloaded on September 19,2020 at 21:15:53 UTC from IEEE Xplore. Restrictions apply.
2102 IEEE TRANSACTIONS ON MEDICAL IMAGING, VOL. 35, NO. 9, SEPTEMBER 2016

IV. DISCUSSION

In this study we presented a new technique, PROSE, which


is capable of simultaneously generating and detecting longi-
tudinally polarized harmonic shear waves for 2D shear wave
elastography. Shear waves were introduced through the con-
tinuous harmonic vibration of a standard transducer using a
voice-coil actuator system. As opposed to ARF-based methods
for generating shear waves, it was possible to use the transducer
in “detect-only” mode, thus eliminating the stress imposed on
the ultrasound system, transducer, and tissue by the high in-
tensity push beams. A novel symmetric detection scheme was
used to suppress the interference of compression strain and the
shear wave signal detected by pulse-echo ultrasound. A single
frame LFE processing technique was used to evaluate the de-
Fig. 4. Shear wave speed measurements of the three homogeneous phantoms tected motion, and allowed for a substantial increase in the shear
for PROSE at 300 Hz compared with those obtained with the LOGIQ E9. Error wave imaging frame-rate compared to traditional full FOV ARF
bars represent one standard deviation.
techniques.
Experiments in homogeneous phantoms and inclusion
phantoms demonstrated that PROSE was able to produce 2D
Fig. 5 shows the resulting shear wave speed images of the shear wave images with values similar to those obtained with
10.4 mm inclusion with varying frequencies. Two ROIs were a high-end GE LOGIQ E9 scanner. All of the homogenous
manually selected to evaluate the performance of PROSE. One phantom results showed smooth shear wave speed images with
ROI was selected using the B-mode image to determine the in- relatively small standard deviations.
clusion boundaries. A second ROI, used to measure the back- The key principle behind PROSE is that symmetric sampling,
ground, was placed above the 10.4 mm inclusion and 5 mm across peaks or nulls of probe compression, is able to acquire
from the edges. The measured shear wave speeds within the in- two images where the compression of the material is identical
clusions were , , and but the shear wave phase differs, allowing for isolation of the
for the 300 Hz, 350 Hz, and 400 Hz acquisitions, re- shear wave signal from probe compression artifact. To ensure
spectively, compared to using the LE9. The sampling when the compressional effects were identical, this
measured shear wave speeds in the background were study relied on a three-axis accelerometer to provide informa-
, , and for the 300 tion of the probes trajectory. A small timing error may result in
Hz, 350 Hz, and 400 Hz acquisitions, respectively, compared to incomplete suppression of the compressional effects, which has
, using the LE9. These results and comparisons low spatial frequency (i.e., large spatial wavelength) and thus
to the nominal values were reported in Table I. The contrast to may lead to overestimation of shear wave speed. In principle,
noise ratio (CNR) was calculated to quantify the ability to de- a higher vibration frequency will require more precise timing
tect the stiff inclusions, for symmetric sampling. As an additional precaution, all shear
wave fields were processed using a spatial band-pass filter de-
(4) signed to suppress large spatial frequencies due to incomplete
removal of the compressional effects by the symmetric sam-
where , and are the mean shear wave speed of the inclu- pling scheme [25]. Cut points of the band-pass filter were se-
sion and background, respectively; is the standard deviation lected based on the expected biological range of shear wave
of the shear wave speed of the background. The measured CNR speed (0.5–10 m/s) and the vibration frequency of PROSE. In
values were converted to decibels using and are this study the time between symmetrically sampled frames
included in Table I. was empirically set at 1/10th the vibration period. This sets an
Fig. 6 shows the shear wave speed images that were obtained upper limit of the imaging depth due to echo time-of-flight con-
from the stepped cylinder phantom with three different inclu- siderations as it is necessary to receive all echoes within the
sion sizes. ROIs were established similarly to the previous in- window. For the highest vibration frequency used in this
clusion study. The measured shear wave speeds at 400 Hz within study (400 Hz), the used is 250 microseconds. Considering
the inclusions were , , and 3 angle plane wave compounding, the pulse-echo time for each
for the 16.7 mm, 10.4 mm, and 6.5 mm inclusions, re- plane wave image is 83.3 microseconds, which corresponds to
spectively, compared to , , and a maximal imaging depth of over 60 mm. If the motion is small
, respectively, using the LE9. The measured enough that aliasing will not occur in the shear wave motion cal-
shear wave speeds in the background were , culation step, increasing will allow an increase in imaging
, and for the 16.7 mm, 10.4 depth without needing to change the number of steering angles
mm and 6.5 mm inclusions, respectively, compared to or the vibration frequency. Conversely, if the motion was large
, using LE9. These results were summarized and com- enough for aliasing to occur, it would be necessary to reduce
pared in Fig. 7 and Table I. to facilitate correct motion calculation. In this study the maximal

Authorized licensed use limited to: Universidad Autonoma de Baja California. Downloaded on September 19,2020 at 21:15:53 UTC from IEEE Xplore. Restrictions apply.
MELLEMA et al.: PROSE: A HIGH FRAME-RATE METHOD FOR TWO-DIMENSIONAL ULTRASOUND SHEAR WAVE ELASTOGRAPHY 2103

Fig. 5. Shear wave speed images from the inclusion phantom, 10.4 mm target, for PROSE performed at a) 300 Hz, b) 350 Hz and c) 400 Hz. ROIs were drawn
from B-mode images. d.) Comparison of the inclusion and background shear wave speed of PROSE with the LE9. Error bars represent one standard deviation.

TABLE I
SHEAR WAVE SPEED BIAS AND CNR OF INCLUSION AND BACKGROUND

Fig. 6. Results from evaluating the inclusion phantom with PROSE at 400 Hz. (a) A representative shear wave motion frame from the 16.7 mm inclusion. (b)
The shear wave speed image from the 6.5 mm inclusion, (c) the 10.4 mm inclusion and (d) the 16.7 mm inclusion.

probe motion was below 0.1 mm for all experiments and thus ally requires one or more wavelengths to accurately estimate
sufficiently small to prevent aliasing. the shear wave speed of inclusions [36]. The inclusions in this
PROSE has the capacity for imaging inclusions. However, study have a shear wave speed of about 4.5 m/s. This corre-
there are three sources of errors that must be considered. First, sponds to a wavelength of about 15 mm at 300 Hz and 11 mm
the propagation speed of shear waves within the inclusion may at 400 Hz. At 300 Hz, the inclusion (diameter 10.4 mm) con-
be physically modified by the boundary effects imposed by the tains less than one shear wavelength, and therefore are biased
background material. Therefore, the shear wave speed within low. At 400 Hz, the inclusion has about one wavelength and
the inclusion may no longer be solely determined by the in- the results are much closer to that obtained by the LOGIQ E9.
clusion's material property. Secondly, the LFE algorithm ide- Finally, the LFE algorithm assumes local homogeneity, which

Authorized licensed use limited to: Universidad Autonoma de Baja California. Downloaded on September 19,2020 at 21:15:53 UTC from IEEE Xplore. Restrictions apply.
2104 IEEE TRANSACTIONS ON MEDICAL IMAGING, VOL. 35, NO. 9, SEPTEMBER 2016

170 ms (2.90 GHz, Intel i5 processor, 8.00 GB RAM). However,


it is expected that an optimized implementation in
with a GPU will reduce the processing time by over an order of
magnitude. As such, it is expected that PROSE will be able to
achieve a real-time frame-rate greater than 10 Hz, and this will
increase as computational technology improves. Such a frame
rate will be helpful for elasticity imaging of lesions that are diffi-
cult to visualize in B-mode imaging (such as myofascial trigger
points), where real-time B-mode imaging cannot be easily used
to locate the lesion for elasticity imaging.
The second benefit is the method's flexibility. PROSE relies
on generating a shear wave field that originates from the sur-
face and propagates into the target, thus, both diffraction ef-
fects as well as attenuation will need to be considered. Because
the diffraction pattern is determined by probe contact and un-
derlying material, altering the contact area may improve wave
Fig. 7. Shear wave speeds for individual inclusions and the background (BG) propagation. Additionally, in situations where the material is
of the inclusion phantom for PROSE at 400 Hz and the LE9. Error bars represent
one standard deviation. viscoelastic, attenuation will be a factor in limiting the depth
of observable shear waves. There is a frequency-penetration
tradeoff, because higher vibration frequencies have better spa-
is violated near boundaries between regions with different stiff- tial resolution but attenuate faster leading to shallower imaging
ness. This causes the shear wave speed reported by the LFE to depths. Fundamentally, PROSE can be performed using a wide
gradually transition between regions [35], leading to elevated range of vibration frequencies, allowing a user switching from a
shear wave speeds in the background and reduced shear wave shallow imaging mode with good spatial resolution at high fre-
speeds inside the inclusion near the boundary. As the vibration quency to a deep tissue imaging mode by changing the driving
frequency is increased, the shear wave wavelength decreases, signal. It is expected that PROSE could allow the user to change
leading to a reduced transition region and a reduction of under- the vibration frequency on-the-fly, allowing for target specific
estimation bias for the inclusion. Fig. 5(d) illustrates that these imaging that can be rapidly adapted for each patient.
effects were observed experimentally. While the PROSE method has shown promising results, the
The choice of vibration frequency has effects on PROSE technique is still limited by wave propagation effects common
imaging. Ideally, high vibration frequency is preferred because to all mechanical shear wave methods. As the wave field prop-
the shorter wavelength of shear waves at higher vibration fre- agates away from the transducer, the waves can reflect or es-
quencies is beneficial for resolving small inclusions. However, tablish standing wave patterns, giving rise to more complex
shear waves at higher frequencies typically undergo higher wave fields. While the LFE method is robust in handling wave
attenuation and therefore have less penetration. In this study, fields with multiple propagation directions within the imaging
the vibration frequency of 300–400 Hz was chosen to image plane [27], [41], [42], no 2D imaging method can account for
the 6.5 mm inclusion for the phantom study. It is expected that out-of-plane wave propagation, which may bias the results [25].
in practice, the vibration frequency can be easily adjusted and Volumetric (3D) imaging of shear waves may be the funda-
optimized for a given imaging task, thanks to the high frame mental solution to this issue [42]. It is expected that this problem
rate potential of PROSE. of out-of-plane wave propagation should be alleviated when
PROSE provides two key benefits over other ultrasound elas- we increase the shear wave frequency, because shear waves
tography techniques. The first is the increased frame-rate. Due attenuate more quickly at higher frequency, thus reducing the
to the symmetric sampling scheme, PROSE's frame-rate is fun- chance of strong reflections. Additionally, for in vivo applica-
damentally linked to the vibration frequency. Given a vibration tions, higher attenuation of shear wave and irregular boundary
frequency of 300 Hz and PROSE's ability to acquire and process conditions are expected to reduce the contribution of shear wave
two images every period, a maximum frame-rate of 600 Hz was motion from reflected and out-of-plane shear waves, further mit-
achieved. However, to increase the robustness of the measure- igating the effect and allowing a wider range of vibration fre-
ments, two sequential shear wave speed maps were averaged, quencies to be used.
reducing the effective PRF to the vibration frequency. Thus, the It is expected that transitioning to in vivo imaging will bring
PRT for this study was 3.3, 2.9 and 1.7 ms for vibrations fre- additional challenges. For example, the effective coupling of
quencies of 300, 350, and 400 Hz, respectively. This upper limit shear wave energy through different tissue layers to the target
of frame rate may be higher than what is clinically necessary. region may need further investigation. We expect that this would
This high frame rate capacity can be used to improve image not be a significant problem because FibroScan can effectively
signal-to-noise ratio by multi-frame averaging. Currently, the deliver shear waves into deep liver regions through the muscle
LFE processing is the limiting factor for real-time display. The and fat layers. Tissues are viscoelastic, which will impose higher
current MATLAB (MathWorks Inc., Natick, MA) implementa- attenuation of shear waves and thus may reduce the penetra-
tion of the LFE was able to process a single frame in less than tion of PROSE for in vivo applications. The shear wave speed

Authorized licensed use limited to: Universidad Autonoma de Baja California. Downloaded on September 19,2020 at 21:15:53 UTC from IEEE Xplore. Restrictions apply.
MELLEMA et al.: PROSE: A HIGH FRAME-RATE METHOD FOR TWO-DIMENSIONAL ULTRASOUND SHEAR WAVE ELASTOGRAPHY 2105

will be frequency dependent due to tissue viscosity. Therefore, REFERENCES


care needs be taken when interpreting these measurements at a
[1] J. F. Greenleaf, M. Fatemi, and M. Insana, “Selected methods for
single frequency. Viscoelasticity, hysteresis, and nonlinear ef- imaging elastic properties of biological tissues,” Annu. Rev. Biomed.
fects of tissue may cause imperfect removal of the compression Eng., vol. 5, pp. 57–78, 2003.
artifact, even if the probe were at the exact location during sym- [2] J. Bercoff, M. Tanter, and M. Fink, “Supersonic shear imaging: A new
technique for soft tissue elasticity mapping,” IEEE Trans. Ultrason.,
metric sampling. It is expected that in practice these high order Ferroelectr., Freq. Control, vol. 51, no. 4, pp. 396–409, Apr. 2004.
effects will not be prominent because the vibration amplitude [3] S. Chen et al., “Shearwave dispersion ultrasound vibrometry (SDUV)
of the probe is small. In addition, the band-pass filter used in for measuring tissue elasticity and viscosity,” IEEE Trans. Ultrason.,
Ferroelectr., Freq. Control, vol. 56, no. 1, pp. 55–62, Jan. 2009.
this study should be able to further suppress any residual com- [4] D. J. Lomas, P. J. Rossman, J. F. Greenleaf, A. Manuca, and R. L.
pression artifacts. Future studies are needed to further inves- Ehman, “Magnetic resonance elastography by direct visualization of
tigate the impact of these higher order effects for in vivo tis- propagating acoustic strain waves,” Sci., vol. 269, pp. 1854–1855,
1995.
sues. Another consideration for in vivo applications is the ef- [5] S. A. McAleavey, M. Menon, and J. Orszulak, “Shear-modulus estima-
fects of physiological motion on image acquisition. Most other tion by application of spatially-modulated impulsive acoustic radiation
force,” Ultrason. Imag., vol. 29, pp. 87–104, Apr. 2007.
methods utilize time-of-flight or phase-based reconstructions, [6] K. Nightingale, S. McAleavey, and G. Trahey, “Shear-wave generation
which makes them vulnerable to motion artifacts as it's nec- using acoustic radiation force: In vivo and ex vivo results,” Ultrasound
essary to track motion through multiple frames. In contrast, Med. Biol., vol. 29, pp. 1715–1723, Dec. 2003.
[7] J. Ophir, I. Cespedes, H. Ponnekanti, Y. Yazdi, and X. Li, “Elastog-
PROSE utilizes a single frame of shear wave motion for LFE re- raphy: A quantitative method for imaging the elasticity of biological
construction, allowing for full FOV estimations to be acquired tissues,” Ultrason. Imag., vol. 13, pp. 111–134, Apr. 1991.
in a very short duration (0.25–0.33 ms), thus substantially re- [8] L. Sandrin et al., “Transient elastography: A new noninvasive method
for assessment of hepatic fibrosis,” Ultrasound Med. Biol., vol. 29, pp.
ducing the window for motion artifacts. 1705–1713, Dec. 2003.
In future work, the actuation system will be miniaturized, by [9] P. Song et al., “Comb-push ultrasound shear elastography (CUSE): A
replacing the signal generator and amplifier with integrated cir- novel method for two-dimensional shear elasticity imaging of soft tis-
sues,” IEEE Trans. Med. Imag., vol. 31, no. 9, pp. 1821–1832, Sep.
cuit counterparts. The actuator and probe adaptor should be im- 2012.
proved to be smaller and easily attachable to a wide range of [10] Y. Yamakoshi, J. Sato, and T. Sato, “Ultrasonic imaging of internal
vibration of soft tissue under forced vibration,” IEEE Trans. Ultrason.,
ultrasound transducers. One should be able to eliminate the mo-
Ferroelectr., Freq. Control, vol. 37, no. 2, pp. 45–53, Mar. 1990.
tion sensor used to guide the timing of symmetric pulse-echo [11] A. P. Sarvazyan, O. V. Rudenko, S. D. Swanson, J. B. Fowlkes, and
detection and use the sinusoidal driving signal to trigger pulse- S. Y. Emelianov, “Shear wave elasticity imaging: A new ultrasonic
technology of medical diagnostics,” Ultrasound Med. Biol., vol. 24,
echo detection, once the fixed phase delay between the driving pp. 1419–1435, Nov. 1998.
signal and the actual transducer displacement is evaluated. Ad- [12] A. Athanasiou et al., “Breast lesions: Quantitative elastography with
ditionally, methods for increasing the vibration amplitude will supersonic shear imaging-preliminary results,” Radiol., vol. 256, pp.
297–303, Jul. 2010.
also be explored as this may allow for increased wave pene- [13] S. F. Eby et al., “Shear wave elastography of passive skeletal muscle
tration at higher frequencies. Finally, the current implementa- stiffness: Influences of sex and age throughout adulthood,” Clin.
tion only utilized a single pair of frames for the symmetric mo- Biomech., vol. 30, pp. 22–27, Jan. 2015.
[14] M. Muller, J. L. Gennisson, T. Deffieux, M. Tanter, and M. Fink,
tion detection spaced by a constant set at the vibra- “Quantitative viscoelasticity mapping of human liver using supersonic
tion frequency. The effect of varying was not explored. Fu- shear imaging: Preliminary in vivo feasibility study,” Ultrasound Med.
ture experiments will be conducted to optimize the selection of Biol., vol. 35, pp. 219–229, Feb. 2009.
[15] P. Song et al., “Two-dimensional shear-wave elastography on con-
with respect to the tissue motion, as well as exploring the ventional ultrasound scanners with time-aligned sequential tracking
use of multiple pairs of frames evenly distributed around the (TAST) and comb-push ultrasound shear elastography (CUSE),”
IEEE Trans. Ultrason., Ferroelectr., Freq. Control, vol. 62, no. 2, pp.
maximum or minimum displacement can be obtained, and re- 290–302, Feb. 2015.
sults (2D map of shear wave motion or final elastography im- [16] LOGIQ E9 Shear Wave Elastography GE Healthcare. Wauwatosa,
ages) averaged to improve the signal-to-noise ratio. As such, WI, 2014 [Online]. Available: http://www3.gehealthcare.com/
~/media/documents/us-global/products/ultrasound/white%20pa-
it is expected that these improvements will position PROSE as pers/logiq/gehealthcare-whitepaper_logiq-e9%20shear-wave.pdf
an attractive low-cost, high frame-rate ultrasound elastography [17] J. Bercoff, ShearWave Elastography. Supersonic Imagine. Aix en
method. Provence, France, 2008 [Online]. Available: file:///C:/Users/m079848/
Downloads/27v1+-+WP+ShearWave+Elastography.pdf
V. CONCLUSIONS [18] J. Bamber, “EFSUMB guidelines and recommendations on the clin-
ical use of ultrasound elastography. Part 1: Basic principles and tech-
This paper introduces PROSE as a novel high frame-rate nology,” Ultraschall in Der Medizin, vol. 34, pp. 169–184, Apr. 2013.
[19] K. Hoyt, B. Castaneda, and K. J. Parker, “Two-dimensional sonoelas-
shear wave elasticity imaging technique capable of generating tographic shear velocity imaging,” Ultrasound Med. Biol., vol. 34, pp.
2D shear wave speed images. This was accomplished by 276–288, Feb. 2008.
[20] Z. Wu, L. S. Taylor, D. J. Rubens, and K. J. Parker, “Sonoelastographic
generating shear waves through mechanical vibration of the imaging of interference patterns for estimation of the shear velocity of
ultrasound transducer with simultaneous motion detection. homogeneous biomaterials,” Phys. Med. Biol., vol. 49, pp. 911–922,
PROSE demonstrated good reconstructions of 2-D shear wave Mar. 2004.
[21] L. Sandrin, M. Tanter, J. L. Gennisson, S. Catheline, and M. Fink,
speed images in both homogeneous and inclusion phantoms “Shear elasticity probe for soft tissues with 1-D transient elastography,”
compared to results obtained by the GE LE9 scanner. With IEEE Trans. Ultrason., Ferroelectr., Freq. Control, vol. 49, no. 4, pp.
further refinement of vibration hardware, PROSE may be a 436–446, Apr. 2002.
[22] S. Catheline and N. Benech, “Longitudinal shear wave and transverse
promising technology for real-time shear wave imaging for dilatational wave in solids,” J. Acoust. Soc. Am., vol. 137, pp. EL200–5,
mid- to low-end ultrasound systems. Feb. 2015.

Authorized licensed use limited to: Universidad Autonoma de Baja California. Downloaded on September 19,2020 at 21:15:53 UTC from IEEE Xplore. Restrictions apply.
2106 IEEE TRANSACTIONS ON MEDICAL IMAGING, VOL. 35, NO. 9, SEPTEMBER 2016

[23] L. Sandrin, M. Tanter, S. Catheline, and M. Fink, “Shear modulus [33] R. H. Bamberger and M. J. T. Smith, “A filter bank for the directional
imaging with 2-D transient elastography,” EEE Trans. Ultrason., Fer- decomposition of images: Theory and design,” IEEE Trans. Signal
roelectr., Freq. Control, vol. 49, no. 4, pp. 426–435, Apr. 2002. Process., vol. 40, no. 4, pp. 882–893, Apr. 1992.
[24] H. Knutsson, C. F. Westin, and G. H. Granlund, “Local multiscale fre- [34] Y. M. Lu and M. N. Do, “Multidimensional directional filter banks and
quency and bandwidth estimation,” in Proc. IEEE Int. Conf. Image surfacelets,” IEEE Trans. Image Process., vol. 16, no. 4, pp. 918–931,
Process., 1994, vol. I, pp. 36–40. Apr. 2007.
[25] H. Zhao et al., “External vibration multi-directional ultrasound [35] A. Manduca, R. Muthupillai, P. J. Rossman, J. F. Greenlead, and R. L.
shearwave elastography (EVMUSE): Application in liver fibrosis Ehman, “Image processing for magnetic resonance elastography,” in
staging,” IEEE Trans. Med. Imag., vol. 33, no. 11, pp. 2140–2148, Proc. SPIE, 1996, vol. 2710, pp. 616–623.
Nov. 2014. [36] A. Manduca et al., “Magnetic resonance elastography: Non-invasive
[26] S. Catheline, F. Wu, and M. Fink, “A solution to diffraction biases in mapping of tissue elasticity,” Med. Image Anal., vol. 5, pp. 237–254,
sonoelasticity: The acoustic impulse technique,” J. Acoust. Soc. Am., Dec. 2001.
vol. 105, pp. 2941–2950, May 1999. [37] I. Sack, J. Rump, T. Elgeti, A. Samani, and J. Braun, “MR elastography
[27] M. L. Palmeri, M. H. Wang, J. J. Dahl, K. D. Frinkley, and K. of the human heart: Noninvasive assessment of myocardial elasticity
R. Nightingale, “Quantifying hepatic shear modulus in vivo using changes by shear wave amplitude variations,” Magn. Reson. Med., vol.
acoustic radiation force,” Ultrasound Med. Biol., vol. 34, pp. 546–558, 61, pp. 668–677, Mar. 2009.
Apr. 2008. [38] R. G. Barr and Z. Zhang, “Effects of precompression on elasticity
[28] M. Tanter, J. Bercoff, N. Benech, and M. Fink, “Coherent plane-wave imaging of the breast: Development of a clinically useful semiquan-
compounding for very high frame rate ultrasonography and transient titative method of precompression assessment,” J. Ultrasound Med.,
elastography,” IEEE Trans. Ultrason., Ferroelectr., Freq. Control, vol. vol. 31, pp. 895–902, Jun. 2012.
56, no. 3, pp. 489–506, Mar. 2009. [39] H. Latorre-Ossa, J. L. Gennisson, E. De Brosses, and M. Tanter, “Quan-
[29] M. Tanter, J. Bercoff, L. Sandrin, and M. Fink, “Ultrafast compound titative imaging of nonlinear shear modulus by combining static elas-
imaging for 2-D motion vector estimation: Application to transient tography and shear wave elastography,” IEEE Trans. Ultrason., Ferro-
elastography,” IEEE Trans. Ultrason., Ferroelectr., Freq. Control, vol. electr., Freq. Control, vol. 59, no. 4, pp. 833–839, Apr. 2012.
49, no. 10, pp. 1363–1674, Oct. 2002. [40] A. Manduca, R. Muthupillai, P. J. Rossman, J. F. Greenleaf, and R. L.
[30] G. Montaldo, M. Tanter, J. Bercoff, N. Benech, and M. Fink, “Co- Ehman, “Local wavelength estimation for magnetic resonance elastog-
herent plane-wave compounding for very high frame rate ultrasonog- raphy,” in Proc. IEEE Int. Conf. Image Process., 1996, pp. 527–530.
raphy and transient elastography,” IEEE Trans. Ultrason., Ferroelectr., [41] Y. K. Mariappan, P. J. Rossman, K. J. Glaser, A. Manduca, and R.
Freq. Control, vol. 56, no. 3, pp. 489–506, Mar. 2009. L. Ehman, “Magnetic resonance elastography with a phased-array
[31] J. A. Jensen and S. I. Nikolov, “Directional synthetic aperture flow acoustic driver system,” Magn. Reson. Med., vol. 61, pp. 678–685,
imaging,” IEEE Trans. Ultrason., Ferroelectr., Freq. Control, vol. 51, Mar. 2009.
no. 9, pp. 1107–1118, Sep. 2004. [42] M. Wang, B. Byram, M. Palmeri, N. Rouze, and K. Nightingale,
[32] C. Kasai, K. Namekawa, A. Koyano, and R. Omoto, “Real-time “Imaging transverse isotropic properties of muscle by monitoring
two-dimensional blood flow imaging using an autocorrelation tech- acoustic radiation force induced shear waves using a 2-D matrix ultra-
nique,” IEEE Trans. Sonics Ultrason., vol. 32, no. 3, pp. 458–463, sound array,” IEEE Trans. Med. Imag., vol. 32, no. 9, pp. 1671–1684,
May 1985. Sep. 2013.

Authorized licensed use limited to: Universidad Autonoma de Baja California. Downloaded on September 19,2020 at 21:15:53 UTC from IEEE Xplore. Restrictions apply.

You might also like