This article appeared in a journal published by Elsevier. The attachedcopy is furnished to the author for internal non-commercial researchand education use, including for instruction at the authors institution
and sharing with colleagues.
Other uses, including reproduction and distribution, or selling or
licensing copies, or posting to personal, institutional or third party
websites are prohibited.
In most cases authors are permitted to post their version of thearticle (e.g. in Word or Tex form) to their personal website or
institutional repository. Authors requiring further information
regarding Elsevier’s archiving and manuscript policies areencouraged to visit:
http://www.elsevier.com/copyrightAuthor's personal copy

Ultrasound in Med. & Biol., Vol. 35, No. 6, pp. 936–948, 2009
Copyright Ó 2009 World Federation for Ultrasound in Medicine & Biology
Printed in the USA. All rights reserved
0301-5629/09/$–see front matterdoi:10.1016/j.ultrasmedbio.2008.12.013

d Original Contribution

PROPAGATION OF VIBRATION CAUSED BY ELECTRICAL EXCITATION IN THE
NORMAL HUMAN HEARTHIROSHI KANAI
Graduate Schools of Engineering and Biomedical Engineering, Tohoku University, Sendai, Japan(Received 12 August 2008, revised 3 December 2008, in final form 16 December 2008)

Abstract—The ability to noninvasively detect regional dynamic myocardial damage related to action potentials
and mechanical properties affected by heart disease is of great clinical importance. Though there are invaluable
clinical tools for diagnosis of a broad range of cardiac conditions, such myocardial properties cannot be evaluated.
We have previously shown that pulsive vibration occurs on the myocardium after electrical stimulation of an isolated heart. In this study, using a novel technique for ultrasonic measurement of the myocardial motion, we
detected pulsive vibrations spontaneously caused by electrical excitation and by valve closure. Using a sparse
sector scan, the vibrations were measured almost simultaneously at about 10,000 points set in the heart wall at
a high temporal resolution. The consecutive spatial distributions of the phase of the vibrations revealed wave propagation along the wall in healthy subjects for the first time in vivo. At around the time of the Q-wave of the electrocardiogram, the propagation started from the interventricular septum and extended to both the base and apicalsides of the heart with a speed of 1 m/s, which corresponds to the propagation of electrical excitation from the Purkinje fiber-myocyte junction in the interventricular septum. Other vibrations then propagated from the base at
several m/s, although some of them had dispersion properties. These are shear waves caused by the mitral-valve
closure, corresponding to the first heart sound. These phenomena have potential for detection of regional myocardial tissue damage related to propagation of the action potentials and regional myocardial viscoelasticity. (E-mail:hkanai@ecei.tohoku.ac.jp) Ó 2009 World Federation for Ultrasound in Medicine & Biology.
Key Words: Echocardiography, Action potentials, Elasticity, Imaging, Shear waves, Electrocardiogram.

tomography (CT) has become possible by placement ofmany electrodes on the surface of the human body (Ramanathan et al. 2004). Though the electrophysiologic activation sequence during activation and repolarization can
be noninvasively reconstructed, the mapping is restricted
to the surface of the heart.
We have previously found that pulsive vibration
occurs in response to electrical stimulation of the extracted
myocardium of a rat (Kanai et al. 2003). The amplitude
was minute, i.e., about 30 mm in displacement and 0.5mm/s in vibration velocity. Though the delay times inboth the generated force and the change in thickness in
response to the electrical stimulation were long at about
100 ms, the delay in the vibration velocity was short at
about 15–30 ms. Therefore, transcutaneous measurementof the minute vibration caused by the electrical excitation
has potential to reveal the propagation of the electricalexcitation in the heart wall in vivo.
Typical imaging tools, namely, magnetic resonant
imaging (MRI), X-ray computed tomography (CT) andconventional echocardiography, enable clinical visualization of cross-sectional images of the human heart. Moreover, the left ventricular (LV) volume, motion and

INTRODUCTION
Though electrocardiography (ECG) has become aninvaluable clinical tool for diagnosis of a broad range of
cardiac conditions, the regional properties of the myocardium can still not be directly measured noninvasively.
Many research reports on the physiologic properties of
the heart conduction system have been published but
almost all of them have concerned animals or isolated
human hearts (Durrer et al. 1970). If the propagation ofelectrical excitation and mechanical vibration in the heart
wall could be directly visualized, regional tissue damage
related to both ion channel gating, which generates theelectrical action potentials and the regional myocardialmechanical properties due to heart diseases could be transthoracically detected. Recently, imaging of epicardial
potentials by a combination of electrocardiographic
imaging and heart-torso geometry obtained by computed

Address correspondence to: Hiroshi Kanai, Ph.D., Graduate
Schools of Engineering and Biomedical Engineering, Tohoku University, 6-6-05 Aramaki-aza-Aoba, Sendai 980-8579, Japan. E-mail:hkanai@ecei.tohoku.ac.jp936

Author's personal copy

Propagation of vibration caused by electrical excitation d H. KANAI

torsional deformation during contraction have been noninvasively measured by CT (Mahoney et al. 1987), twodimensional (2D) echocardiography (Notomi et al.
2005) and tissue tagging MRI (Axel et al. 1989; Buchalter
et al. 1990). However, the temporal resolution in MRI is
inevitably limited by the relaxation time (about 14–25ms) of the tissue in response to the magnetic excitation(Zwanenburg et al. 2004). The time resolution is 13 ms(Wyman et al. 1999a). The in-plane spatial resolution is
1.25 3 3 mm and the slice thickness is 7 mm (Wyman
et al. 1999b). As a characteristic timing parameter ofcardiac contraction, the time to onset of circumferential
shortening was measured with MRI tagging (Wyman
et al. 1999a), in which the time to onset of activation
was determined by the time when the strain due to contraction has a maximum, at least several tenths of a microsecond after the pacing. The tissue Doppler imaging(TDI) technique (Sutherland et al. 1994; Fleming et al.
1994; Heimdal et al. 1998)—modified 2D color flow
mapping—has been developed to accurately measure
myocardial velocity. This technique is still restricted tostatic configurations or large motion (.1 mm) with low
frequency components (,30 Hz) because the detectable
amplitude is greater than the wavelength (about 400 mm
at 3.75 MHz) and the temporal resolution is at most 16
ms. Therefore, it has been considered that there are no
minute vibrations with high frequency components inthe actual human heart walls and none of these conventional clinical imaging methodologies can detect
minute vibrations of the myocardium caused by electricalexcitation and valve closure nor visualize myocardial
dynamic properties with high temporal resolution ofa few milliseconds.
To measure the original wall vibrations of the heartsounds, which are audible by a stethoscope, we havedeveloped a novel ultrasound-based transthoracic method
to measure the minute vibrations in the heart wall as waveforms and to show their spatial distribution (Kanai et al.
1996, 1999a, 1999b). The measurement of the vibration
is simultaneously applied to several thousand points
preset at 51.3-mm intervals along about 10 ultrasonicbeams, which are scanned sparsely in the heart wall tomaintain a high frame rate (Kanai et al. 2001). The spatial
distribution with regard to the waveform or the instantaneous phase of the specific frequency component is shownat every 2 ms, precisely revealing the propagation of thevibration waves on the ultrasonic cross-sectional planeof the heart wall (Kanai 2005).
By applying this novel method to healthy humansubjects, we have previously found that some impulsive
vibrations, which correspond to the second heart sound,are mechanically caused by closure of the heart valves(Kanai et al. 2000) and propagate along the heart wallwith frequency dispersion (Kanai 2005). Their characteris-

937

tics were found to agree with the theoretical characteristicsof the Lamb wave, a kind of the shear plate wave. In healthy
human subjects, we have detected vibrations corresponding
to the response of the myocardium to electrical excitation(Kanai 2007). However, dispersion properties and transmural propagation were not shown. Similar results have beenobtained in an animal study (Pernot et al. 2007; Konofagou2007) in which acquisition at a depth of about 10 mm wasapplied to small animals to realize an equivalently highframe rate (8 kHz) with the ECG gating, that is, its measurement continued during several heartbeats, by referring to
the R-waves, the measured waveform was divided into
several heartbeats and, then, the cross-sectional image ofthe instantaneous displacements was reconstructed in one
cardiac cycle. In a recent article (Wang et al. 2008), thismethod was applied to the left ventricle of a human subject.
However, based on the ECG-gating technique, showing theresults was restricted to the period after the R-wave. Thus,
the wave propagation from the time of the Q-wave to thetime of the R-wave was not shown and the wave propagation could not be analyzed for each frequency component.
In the present study, this novel method was applied tohealthy human hearts to reveal the propagation and dispersion properties of the myocardial vibrations caused byelectrical excitation both in the base-apex and transmural
directions. Furthermore, regarding the mechanical vibrations caused by valve closure, which correspond to the firstheart sound, the present study revealed that there areseveral components which propagate at different speeds.
To understand the following discussion, it may be
helpful to recall that the P-wave of the electrocardiogramis the electrical trigger for mechanical contraction of theatria, while the QRS-complex is the electrical trigger formechanical contraction of the ventricles. The first heartsound follows the QRS-complex and is traditionally
thought to be primarily associated with vibrations resulting from the closure of the tricuspid and mitral values.
The second heart sound usually follows the T-wave andis thought to be primarily associated with vibrations resulting from the closure of the pulmonary and aortic
valves. The techniques and results presented below permit
one to visualize subtle features of specific mechanicalvibrations occurring during the propagation of the electrochemical depolarization wave responsible for the surface
electrocardiogram. Timing points such as TQ, corresponding to the Q-wave of the surface electrocardiogram, and TI
and TII, the time of first and second heart sounds, respectively, are employed in the following discussion.
MATERIALS AND METHODS
According to a novel ultrasonic-based method—thephased tracking method (Kanai et al. 1996, 1999a) —the rapid vibration in the heart wall is measured as

Author's personal copy

938

Ultrasound in Medicine and Biology

a waveform as follows. RF pulses are transmitted from anultrasonic transducer at a pulse repetition interval DT andthe reflected ultrasonic wave is received by the sametransducer and is multiplied by the original RF signal for
quadrature-demodulation. A complex cross-correlation
technique is employed to determine the phase shift Dq(t)between the consecutively obtained resultant signals.
Since Dq(t) corresponds to the displacement Dx(t) during
the short-period DT, the average velocity during the period
is estimated by v(t) 5 Dx(t)/DT. By accumulating the
instantaneous displacement estimate Dx(t), the large
motion x(t) due to the heartbeat is tracked over one heartbeat (Kanai et al. 1997; Yoshiara et al. 2007) and theminute vibration component v(t) superimposed on x(t) issimultaneously obtained as a waveform. Since the highfrequency components contained in the velocity waveformv(t) are suppressed by the integration, the equivalent time
resolution of the resultant displacement wave x(t)decreases. Therefore, the velocity waveform v(t) is ofconcern in the present study. When the maximum measurable depth dmax is 100 mm from the chest surface and thesound speed c0 is 1540 m/s, the repetition pulse interval
DT should be equal to or shorter than 2dmax/c0 y 130
ms. The upper limit jvmaxj of the vibration measurement
is given by
jvmax j5c0p
z0:79 m=s;4pf0 DT(1)

where the frequency f0 of the ultrasound is assumed to be
3.75 MHz. A minute phase change Dq(t) of 0.4 degrees
caused by displacement during DT can be accurately
determined by introducing a constraint, namely, that
their waveforms are identical but their phase values
change (Kanai et al. 1996, 1999a). The achieved lower
limit jvminj in the velocity measurement has been validated as being about 0.1 mm/s, which was confirmed
in phantom experiments (Kanai et al. 1997) and whichcorresponds to 0.13 mm in displacement. The wavelength is about 410 mm for the typical frequency (3.75
MHz) applied to the human heart. Thus, the measurable
displacement on the order of 0.13 mm corresponds toabout 1/3000 of the wavelength. It is difficult to achieve
such minute displacement with the conventional speckle
tracking method when the maximum amplitude of thecross-correlation function of the RF signals is detected.
On the other hand, for the conventional Doppler method,
the large motion is not tracked and thus the displacement
and the velocity of the same point cannot be measured.
Thus, such a minute vibration superimposed on the large
motion cannot be noninvasively measured by any othermethod.
To simultaneously measure the vibrations at many
points in the interventricular septum (IVS), ultrasonicVolume 35, Number 6, 2009

diagnostic equipment (SSD6500; Aloka Co. Ltd., Tokyo,
Japan) was modified so that N scan lines with different
directions from a sector scanner could be arbitrarily
selected in real time (Kanai 2005; Kanai et al. 2000).
The number, N, of directions should be increased asmuch as possible so as to increase the spatial resolution.
However, the actual maximum velocity jvactj of the vibration at the points in the IVS of the human heart is about
0.07 m/s (Kanai et al. 1996, 1999a) in a typical case,which is about 1/10.7 of jvmaxj. That is, the maximum
number Nmax of the beam directions is given by dividing
jvmaxj of eqn 1 by jvactj,
jvmax jz10:
Nmax 5jvact j(2)Thus, about 10 appropriate directions (N 5 10) aresparsely selected from the 240 directions addressable in
the phased-array ultrasonic probe as illustrated by thenarrow fan-shaped area at the center of Fig. 1a. Alongeach scan line, the RF signal is acquired at a sampling
frequency fs of 15 MHz and, thus, many points at intervalsof c0/fs 5 51.3 mm are set from the apical side to the baseside in the IVS. The spatial resolution along the ultrasonicbeam depends mainly on the length of the transmitted
ultrasonic pulse, which is a few times the wavelength(about 410 mm) of the employed frequency of 3.75
MHz. By applying the above procedure to each j-th point
preset along the k-th scan line, the vibrations at several
thousand points, {vj,k(t)} (j 5 1,2,.; k 5 1,2,.,N), aresimultaneously measured.
If the propagation speed of the detected pulsive wave
is 7 m/s for a 50 Hz component, its wavelength is 14 cm,
which is comparable to the size of the whole heart and,thus, its propagation phenomenon along the heart wallcannot be easily visualized by showing the amplitude of
the pulsive wave. Instead, the phase value of the pulsive
wave, which varies from 0 to 360 degrees within one
wavelength, is effective for such visualization. The phasevalue uj,k(t; f1) of the measured wave vj,k(t) for a frequency
f1 is obtained by applying a short-time Fourier transformwith a Gaussian window. From the results obtained at
multiple frequencies {f1}, the dispersion property of the
propagation of the detected vibration is shown. Fora frequency less than 20 Hz, however, the length of theGaussian window would have to be long, precluding
detection of change in the propagation phenomena. For
the frequency components higher than 60 Hz, the signalto-noise ratio was rather poor. Thus, the frequencies {f1}at 40 Hz and 40 6 16 Hz were selected. In the actual
experiments, instead, 21 Hz, 41 Hz and 55 Hz were
replaced by the respective values closest to the discrete
frequencies determined by the window length. The total

Author's personal copy

Propagation of vibration caused by electrical excitation d H. KANAI

939

Since the amplitude at 6 8.2 ms decreased to 50% ofthat at the window center using this setting, the equivalent
time resolution of Fourier analysis was about 16 ms. The
underlying hypothesis for the frequency analysis is thatthe spectrum does not change during the equivalent
period.
The phase value uj,k(t; f1) is color-coded based on theupper-right circular illustration in Fig. 1b for imaging of
2D spatial distribution {uj,k(t; f1)} (j 5 1,2,.) (Kanai
2005; Kanai et al. 2000). An example of this is shownin Fig. 1b. The detected phase value uj,k(t; f1) corresponds
to the delay time of the specific frequency component
from the center of the short time window. By shifting
the time t of the window by about 2 ms, the same analysis
is consecutively applied. By this procedure, minute vibrations {vj,k(t)} are simultaneously detected at many points
in the heart wall and the spatial distribution of their phasecomponents, {uj,k(t; f1)}, are consecutively obtained withhigh time resolution, which is sufficient to visualize thepropagation of the wave caused by electrical excitationand that of mechanical vibration in the heart wall. In thepresent study, this method was applied to three normal
young male volunteers. The study was approved by thereview committee of the Graduate School of Engineering,Tohoku University and the healthy subjects gave
informed consent.

RESULTSFig 1. (a) Illustration showing a typical cross-sectional image ofthe heart in the apical view acquired by a conventional ultrasound diagnostic system. The fan-shaped region corresponds
to the sparse scanning range of the ultrasonic beams in thepresent measurements. The conduction system from the sinoatrial (SA) node through the atrio-ventricular (AV) node andHis bundle to the Purkinje network, shown by green lines, transmits the cardiac impulse almost simultaneously to the entire rightand left ventricular endocardia. (b) Example of the spatial distributions of color-coded phase values of the 42 Hz component in
the waveforms of Fig. 2. The region surrounded by the uprightthin black rectangle for each time was cut out and set in an array
to show consecutive spatial distributions of color-coded phasevalues of the waveforms along the center of the IVS aroundTR, as shown in the upper panel of each of Figs. 4, 6 and 7.
The region surrounded by the horizontal black rectangle wascut out, rotated by -90 degrees, and set in an array to show thetransmural distributions from the LV side to the RV side aroundTR as shown in the lower panel of each of Fig. 4a through c.

length of the Gaussian window was 6 72 ms, but its
amplitude parameter was set so that the amplitude at 636 ms decreased to 3.5% of that at the window center.

Figure 2 shows a typical example of the vibration
waveforms, vA(t), vB(t) and vC(t), for a subject at threepoints—(A) apical side, (B) middle and (C) base side—
set on an ultrasonic beam passing through the IVS
between the left ventricle (LV) and the right ventricle(RV), as illustrated in Fig. 1. Though four consecutive
heartbeats were overlaid, there was high reproducibility
in succeeding cardiac cycles. Around the radiation time(TI) of the first heart sound and the radiation time (TII)
of the second heart sound, some discriminative steep
pulses can be observed in these waveforms. Steep pulses
at TII were the mechanical vibrations caused by closureof the semilunar valves (the aortic and pulmonary valves)(Kanai 2007). The pulsive vibrations at TI were mechanically caused vibrations due to closure of the atrioventricular valves (the mitral and tricuspid valves). These
components at TI and TII correspond to the original vibrations of the two major heart sounds (the first heart soundand the second heart sound), which are audible using
a stethoscope (Luisada and Portaluppi 1982). Especiallyduring atrial systole, middle systole and the period of rapid
inflow, there are small noisy components, which show theinteraction between the rapid blood flow (inflow or
outflow) and the heart wall.

Author's personal copy

940

Ultrasound in Medicine and Biology

Volume 35, Number 6, 2009

Fig 2. Vibration waveforms on the heart wall accurately measured at points A, B and C set in the interventricular septum(IVS) along an ultrasonic beam in Fig. 1a for a young healthy subject. The waveforms for four consecutive cardiac cycles
are overlaid. Times TQ, TR, TI and TII, respectively, show the Q-wave and R-wave of the ECG, the beginning of the firstheart sound and the beginning of the second heart sound.

Figures 2 through 4 show data for the abovementioned subject. The ultrasonic beams were transmitted
at every 2.25 degrees in eight directions (N 5 8) and thepulse repetition interval DT 5 1786 ms, that is, the pulse
repetition frequency (PRF) was 560 Hz and the temporal
resolution in the measurement was about 2 ms. Figure 3
shows the consecutive instantaneous velocity distribution,{vj,k(t)} (j 5 1,2,.; k 5 4), along the fourth ultrasonicbeam which passes through the center of the IVS in
Fig. 1a for a period of about 6100 ms around the time(TR) of the R-wave of the ECG. The horizontal red andblue bars show the upward velocity (vj,k(t) . 0) and downward velocity (vj,k(t) , 0), respectively.
For the same subject in Fig. 3, the consecutively
obtained phase distributions are shown in the upper panelof each of Fig. 4a through c, in which the scales along thetime and the depth axes exactly coincide with those in
Fig. 3. In each of Fig. 4a through c, the upper panel shows
the consecutive instantaneous phase distributions {uj,k(t; f1)} (j 5 1,2,.; k 5 4; jt-TRj # 100 ms) for the f1 5
21 Hz, 41 Hz and 55 Hz components involved in the vibrations {vj,k(t)}, simultaneously detected at several thousand
points in the upright thin rectangular region of the heart
wall of Fig. 1b. That is, the region surrounded by the
upright thin black rectangle for each time was cut out
and set in an array to show consecutive spatial distributions of color-coded phase values {uj,k(t; f1)} of the

waveforms along the center of the IVS around TR, as
shown in Fig. 4. The dashed straight lines, which correspond to the wave propagations in Fig. 3, are overlaid inFig. 4. Since the low frequency component is dominant
in the measured vibrations {vj,k(t)}, the phase distribution{uj,k (t; f1)} in Fig. 4a corresponds to the velocity distribution {vj,k(t)} in Fig. 3. When a higher frequency of f1 isemployed in the Fourier transform, however, the wavelength of the sinusoidal wave component detected by
the Fourier transform with f1 becomes shorter and then
the temporal resolution in the phase distributions{uj,k(t;f1)} increases; these phase distributions {uj,k(t;f1)}
for higher frequency components (f1 5 41 Hz and 55 Hz)
are different from that (f1 5 21 Hz) in Fig. 4a and thevelocity distribution {vj,k(t)} in Fig. 3.
On the other hand, the region surrounded by the horizontal black rectangle in Fig. 1b was cut out, rotated by-90 degrees and set in an array to show the consecutive
instantaneous phase distributions {uj,k(t; f1)} (j: fixed; k:varied; jt-TRj # 100 ms) around TR in the lower panelof each of Fig. 4a through c. Employing these panels, it
is possible to show the propagation of the vibration in
the transmural direction from the LV side to the RV sidein the center of the IVS. For the propagation component
which starts at the time of the Q-wave (TQ) of the ECG,
the propagation speed is 0.9 m/s, which corresponds tothe conduction speed in the myocardium. On the otherAuthor's personal copy

Propagation of vibration caused by electrical excitation d H. KANAI

941

Fig 3. Consecutive velocity distribution along an ultrasonic beam which passes through the center of the IVS in Fig. 1a forthe period of about 6100 ms around TR of the same subject as in Fig. 2. The horizontal lengths of the red and blue bars show
the upward velocity and downward velocity, respectively.

hand, for the components around TI, there is no time delay
between the LV and RV sides of the IVS.
The results obtained by applying the same procedures as those in Figs. 3 and 4 to two other healthy
subjects are shown in Figs. 5, 6 and 7. Similar phenomena
were observed for all three subjects. Since the duration of
the first heart sound of the second subject (Figs. 5 and 6)
was shorter than that of the first subject (Figs. 3 and 4), thenumber of wave propagations was less than that of the firstsubject. In Fig. 6b and c, at 130 ms and at 30 ms before TQ,
waves propagated twice from the base side of the IVS tothe apical side with a propagation speed of 4 m/s, whichcorresponds to the conduction speed in the Purkinje fibers.
A wave then propagated from each of a few points in the
IVS to both apical and base sides of the IVS with a propagation speed of 0.9 m/s, which corresponds to the conduction speed in the myocardium. For the third subject in
Fig. 7, however, these propagations started at about 200
ms and 100 ms before TQ, the propagation phenomenaof the wave which started at 100 ms before TQ in Fig. 7
being similar to Figs 6b and c, and Fig. 4b and c.
DISCUSSION
The source of myocardial contraction is electricalstimulation. As shown in the vibration waveforms vA(t),vB(t) and vC(t) of Fig. 2, from the end of the first heartsound, these points move upward to the apical side andthere are differences in amplitudes among these waveforms, which correspond to the speed of change in length.
By integrating the difference between the waveforms, thechanges in length between these points are obtained,
which shows the contraction of the myocardium in the

IVS. However, contraction is obtained by integration
along the time axis and, thus, the time resolution
decreases. In Figs. 3 through 7, the displayed period is
until the end of the first heart sound and, in this shortperiod, no contraction is distinguishable.
As shown in Fig. 2, around TQ, there were small
inflection points in vA(t), vB(t) and vC(t). Around TQ,
mechanically caused vibration is not possible because
the atrioventricular valves are still open. Physiologically,
the depolarized action potentials, cyclically generated at
the sino-atrial (SA) node, propagate through the atrioventricular (AV) node and His bundle to the Purkinje
fibers. The Purkinje fibers form interweaving networks
on the endocardial surface of both ventricles and transmit
the cardiac impulse almost simultaneously to the right andleft ventricular endocardia at a speed of 2–4 m/s (Zipes
and Braunwald 2005; Katz 2001). Around TQ, based oncell-to-cell connections, the action potential starts to propagate with a speed of 0.3–1 m/s (Katz 2001) to the entire
heart wall from the Purkinje fiber-myocyte junctions on
the surface of the IVS, where the Purkinje fibers are incontact with the myocardium. For the papillary muscle
of a rat, the response of the myocardium to electrical stimulation can be detected as vibration velocity of the
myocardium (Kanai et al. 2003). Thus, the vibration
with inflection points around TQ in Fig. 2 would correspond to the response of the myocardium in the IVS tothe electrical stimulation.
As shown in Fig. 3, before TQ, the downward (blue)
components were dominant due to the ventricular dilatation during the atrial contraction. However, from TQ, theregion of the downward component was graduallyreplaced by the upward (red) component from the center

Author's personal copy

942

Ultrasound in Medicine and Biology

Volume 35, Number 6, 2009

Fig. 4. Consecutive spatial distributions of color-coded phase values for the 22-Hz (a), 42-Hz (b) and 55-Hz (c) components of the measured waveforms for the subject in Figs. 2 and 3. The upper panel of each figure shows the consecutive
distribution along the center of the IVS from the apex to the base. The lower panel of each figure shows the consecutive
distribution in the transmural direction from the LV side to the RV side. At least the same dotted straight lines corresponding to the propagation in Fig. 3 are overlaid in Fig. 4a.

Author's personal copy

Propagation of vibration caused by electrical excitation d H. KANAI

943

Fig. 5. Consecutive velocity distribution of the second healthy young subject for the period of about 6100 ms around TR
along an ultrasonic beam, which passes through the center of the IVS as in Fig. 1a. The horizontal lengths of red and blue
bars show the upward velocity and downward velocity, respectively.

part of the IVS to both the base and apical sides. Since its
propagation speed was slow at about 0.8 m/s, which corresponds to the conduction speed in the myocardium, thisphenomenon would correspond to the muscle contraction
caused by the depolarization of the heart muscle. At theradiation time (TI) of the first heart sound, the velocity
distribution became complex due to propagation ofseveral vibrations corresponding to the heart sound.
Then, 70 ms after TR, the upward (red) component became
dominant, reflecting the contraction of the ventricle insystole. The propagation speeds of the vibrations corresponding to the first heart sound were 3–15 m/s. Since
the vibration was measured in the axial direction of theultrasound and its direction was the same as the wave
propagation along the IVS, the measurement was inconsistent with the definition of a shear wave. By separate
in vivo experiments, from the parasternal longitudinal
axis view of the IVS, there were some wave propagations
from the time of the R-wave and the propagation speed ofeach component was on the order of several m/s. Though
the IVS is narrow, there is possibility that the wavefront
inclined by several degrees from the axis passing throughthe IVS and from the axial direction of the measured ultrasound. Due to these factors, these vibrations correspond to
the shear wave (Kanai 2005; Kundo 2003; Sarvazyan et al1995). It was found for the first time in the present study
that two or three pulses propagate with different speeds
along the IVS.
In the upper panel of Fig. 4a, phenomena similar to
those of Fig. 3 were observed because the low frequency
components were dominant in the detected vibrations.
Before TQ, blue or green components, which show the
downward components according to the upper-rightcircular illustration in Fig. 1b, were dominant. From TQ
in the upper panel of Fig. 4a, a wave (violet: 270-degrees
component of a sinusoidal wave) began to propagate fromthe center of the IVS to both sides. The dotted straightlines in Fig. 4a coincide with those in Fig. 3. Anotherpropagation is shown in Fig. 4a, which started 100 ms
before the R-wave and propagated at a speed of 4 m/s.
In Fig. 4b and c, a similar propagation was found. For
this subject, the peak time TP of the P-wave of the ECG
was 130 ms before the R-wave. Thus, after the time of
the P-wave, a pulse propagated from the base side to theapical side at a speed of 4 m/s, corresponding to that of
the conduction speed in the Purkinje fibers.
By increasing the temporal resolution using higher
frequency analysis in the upper panel of Fig. 4b and c,
at 50 ms after the propagation, there were three waves,which started at points a, b and c in the upper panel ofFig. 4b and c. Their propagation speed was about 4 m/s.
These phenomena are very complex and are considered
to show the response of the myocardium to the excitation
due to the propagation of the electrical conduction wave.
Though there are a few propagations, which correspond to
the propagation of the electrical conduction wave from theviewpoint of propagation speed, direction and time, thesedifferences and causes could not be clarified in the present
study.
Then, from 12 ms after TR, the upward (red) component clearly propagated from the base of the IVS to theapical side. Its speed was about 7 m/s and did not vary
for the frequencies of 21 Hz, 41 Hz and 55 Hz. This would
be the shear wave mechanically caused by closure of theatrioventricular valves. The reason why the propagation
speed was unchanged at different frequencies for a shear

Author's personal copy

944

Ultrasound in Medicine and Biology

Volume 35, Number 6, 2009

Fig. 6. Consecutive spatial distributions of the color-coded phase values of the waveforms along the center of the IVS
around TR for the 22-Hz (a), 42-Hz (b) and 55-Hz (c) components for the second subject in Fig. 5.

wave is described in the next paragraph. At TI (about 30
ms after TR), the two components (yellow and green
components) started to propagate in the same direction.
The yellow component is clearly shown in Fig. 4 andthe propagation speed is 7.0 m/s. For the green component, however, there was large dispersion since its speed
was about 3.0 m/s for 21 Hz, 5.8 m/s for 41 Hz and 7.0
m/s for 55 Hz. Thus, this would be the Lamb wave, a shear

Author's personal copy

Propagation of vibration caused by electrical excitation d H. KANAI

945

Fig. 7. Consecutive spatial distributions of the color-coded phase values of the waveforms along the center of the IVS
around TR for the 42-Hz component for the third healthy young subject.

horizontal wave of the guided wave in a thin wall (theseptum), which was mechanically caused by closure of
the atrioventricular valves. The propagation of thismechanically caused vibration was also observed at theradiation time of the second heart sound in a previous
study (Kanai 2005), in which the pulse propagated fromthe root of the aortic valve to both the base side and theapical side at the time of the aortic value closure. The
dispersion property for the Lamb wave is determined by
the geometric dispersion and the viscous dispersion. As
shown in the upper panel of Fig. 4b and c, from 50 ms afterTR, the second component of the first heart sound propagated in the same direction. The propagation speed wasabout 7 m/s and there was no clear dispersion. In
Fig. 4a, the propagation of the second component cannot
be clearly detected since the temporal resolution is not sohigh for the low frequency component.
For the shear wave, its propagation speed at theangular frequency u depends on the complex viscoelastic
modulus G*(u), which is composed of the storage
modulus GR(u) and the loss modulus GI(u), the latterbeing given by the viscosity m2(u) multiplied by u. There
have been few data on the human myocardium, which
could be used to determine the frequency dependence ofsuch mechanical properties. Alternatively, according to
the measured data for the thoracic arterial walls of humansubjects (Learoyd et al. 1966), for the frequency range of 2
to 10 Hz, the storage modulus GR(u) and loss modulus
GI(u) are almost unchanged, which means that theviscosity m2(u) 5 GI(u)/u gradually decreased as thefrequency increased. However, the rate of decrease was
not given in the cited paper. Nasseri et al. 2002 quantitatively determined the frequency dependency of theviscosity m2(u) of pig kidney to be 2362.6 3 u (0.278-1)
5 626.7 3 f -0.722 [Pa$s], where this relationship welldescribes the frequency dependence of the above viscosity
m2(u) for the human thoracic artery (Learoyd et al. 1966).
Thus, it can be assumed that the loss modulus GI(u) 5 u
3 m2(u) of the human heart is in proportion to u 3 u -0.722
5 u0.278. When the stiffness ratio GI(u)/GR(u) is assumed
to be about 0.8, which was measured for the canine left
ventricle in case of 120 mmHg by pressure perturbation
at 22 Hz (Templeton and Nardizzi 1974), the change inthe magnitude of the elastic modulus jG*(u)j 5 jGR(u)1 jGI(u)j can be roughly estimated to be jG*(55 Hz)j/jG*(21 Hz)j y 1.13. That is, in the frequency range of
21 Hz to 55 Hz measured in the present study, jG*(u)jis almost unchanged and thus the pro u pagation speedof the shear wave appears to be unchanged. For the present
procedure, it is difficult to accurately measure the propagation speed to differentiate these small changes. For theLamb wave, on the other hand, its propagation speed
depends on the viscous dispersion determined by elastic
modulus G*(u) and geometric dispersion.
The wave propagations in the lower panel in each of
Fig. 4a through c correspond to those found in the upper
panel of each of the figures. However, there was a timedelay for the component at TQ, which means that thecomponent propagates from the LV side to the RV side
at a speed of about 1 m/s, which corresponds to the
conduction speed in the myocardium. For the two vibration components corresponding to the first heart sound,
there was no clear time delay. Thus, the wavefront ofeach of the latter components is perpendicular to theaxis of the apex-base along the IVS. In the upper panelof each of Fig. 4a through c, the green component whichstarts at a time TI has a large dispersion property, which
would be the Lamb wave. On the other hand, in the lower
panels of Fig. 4a through c, there are corresponding green
components. However, as the thickness of the IVS isAuthor's personal copy

946

Ultrasound in Medicine and Biology

about 10 mm, it is difficult to detect the incline angle of the
wave front from the axis passing through the septum andfrom the axial direction of the measured ultrasound.
The bundles of His have two branches, on the left
ventricular side and right ventricular side, respectively,
and on both sides there are Purkinje fibers. Thus, fromthe physiologic point of view, it is normally consideredthat the electrical conduction wave propagates from bothsides to the middle of the IVS. However, the in vivo experimental results obtained in the present study do not correspond to these physiologic facts. This should be clarified
in future studies.
At 20 ms before TQ in Fig. 6 and at 90 ms before TQ
in Fig. 7, a wave propagated from the base side of the IVS
to the apical side with a propagation speed of about 4 m/s,
which corresponds to the conduction speed in the Purkinje
fibers. Then, from each of the several points in the IVS,
a wave propagated to both the apical and base sides of
the IVS with a propagation speed of about 0.9 m/s, whichcorresponds to the conduction speed in the myocardium.
These results show the possibility that the detectedphenomena correspond to the response of the myocardium
to the excitation due to the propagation of an electricalconduction wave. Since it is known that simple bifurcation of the Purkinje fibers into the anterior and posteriorfascicles is uncommon (Katz 2001) and highly depends
on the subjects, such differences among the three subjects
regarding the propagation around TQ will occur. According to the rough sketch by Netter 1969, the electricalconduction wave arrives at the IVS at about the sametime as the Q-wave of the ECG. Thus, for the subjects
in Figs. 4 and 6, the above results correspond to the physiologic phenomenon. However, for the subject in Fig. 7,
the arrival time of the electrical conduction wave wasmuch earlier than that of the Q-wave, which is also oneof the problems unresolved in the present study.
Since the propagation time of these components isvery short, i.e., about 10 ms from the base to the apex, it
has been difficult to measure and analyze these phenomena.
For noninvasive electrocardiographic imaging for cardiac
electrophysiology and arrhythmia (Ramanathan et al2004), the estimation of the potential is restricted to thesurface of the heart wall (epicardium) and, thus, the potential inside the IVS cannot be estimated. Even with the excellent MRI-tagging method (Wyman et al. 1999a, 1999b;
Zwanenburg et al. 2004), the spatial and time resolutions
are still not sufficient. These phenomena are very complex
and it is still difficult to completely explain the relationshipbetween these vibrations and either the ECG or the heartsound, which was detected as a longitudinal wave bya microphone attached to the chest wall.
In Figs. 3 through 7, the analyzed period, i.e., fromthe P-wave of the ECG to the S-wave of the ECG, is about
200 ms around the time (TR) of the R-wave. During thisVolume 35, Number 6, 2009short period in end diastole, the wall moves slowly andthe displacement is very small. The displacement component along the ultrasonic beam can be tracked by measurement. The displacement component normal to theultrasound beam in the apical view can be estimatedfrom the displacement along the ultrasonic beam in theparasternal longitudinal view as shown in Fig. 1b of Kanai
2005. For example, for the period just before the R-waveof the ECG, there is a small downward pulse in the parasternal longitudinal view. For this pulse, the maximum
amplitude is about 50 mm/s at the middle septum but
the duration time is about 50 ms. By approximating thevelocity waveform of this pulse with a downward isosceles triangle, the displacement accumulated during theperiod can be estimated to be about (50 mm/s) 3 (50ms)/2 y 1.3 mm, which is comparable to the size (about
1.5 mm) of the focal area. Thus, it can be assumed that theeach myocardium does not move so much as the focal areaof the ultrasonic beam during this short period. In Figs. 3
through 7, moreover, since the analyzed period for eachpropagation is at most 50 ms, it can be assumed that theeach propagation phenomenon is shown for the same
myocardium. These assumptions should be further clarified by simultaneous measurements of various components in the displacement.
The accuracy has been evaluated for the velocity
measurement (Kanai et al. 1997) and for minute change
in thickness (Kanai et al. 1999b). When the signalto-noise ratio (SNR) is low such as in obese subjects,
a decrease in the accuracy is inevitable. However, the relationship among the SNR in an acquired RF signal, theaccuracy in the velocity measurement and the accuracy
in the phase estimate of the velocity waveform have notbeen evaluated. The decrease in the SNR for the suboptimal images in actual clinical measurements has notbeen evaluated either. These evaluations should be established in the near future for actual clinical application.
The velocity of each wave propagation shown in
Figs. 3 through 7 was determined by dividing the distance(vertical axis) by the propagation time. The dashed line
was drawn manually by considering the wave front visible
in Fig. 2. The emphasis of this study is not on the accurate
determination of the wave velocity but on the fact that
there are several wave propagations in the septum ataround the R-wave of the ECG. Thus, the velocity values
were expressed as two digits in this study. It is necessary
for clinical applications to develop a method to determine
the propagation velocity of each wave in the results as inFigs. 3 through 7.
Infarcted muscle, resulting from an occluded coronary artery, is already dead and so polarization of the cells
is not possible. Between the infarcted area and thesurrounding normal muscle, there is injured cardiac
muscle, which has cell membranes that are never fullyAuthor's personal copy

Propagation of vibration caused by electrical excitation d H. KANAI

polarized due to the deficiency of ion channel gating(Netter 1969). In such injured myocardium, the conduction speed decreases. Moreover, during the remodelingfrom the onset of acute myocardial infarction to thechronic stage, myocardial mechanical properties (acoustic
velocity and attenuation) change (Saijo et al. 1997). Since
each of these propagations depends on the regional
myocardial characteristics, that is, the physiologic properties of the action potential and the mechanical propertiesof the viscoelasticity, both of which cannot be noninvasively estimated in general, new insights on these spontaneous phenomena detected in human subjects in this study
show potential for noninvasive assessment of myocardial
tissue damage due to heart failure and its spatial range.
The method also has potential as a noninvasive tool forassessing de-synchronization of myocardial function in
cardiac fibrillation as in Witkowski et al. 1998 and Rohret al. 1997.
CONCLUSION
To conclude, by observing rapid, minute vibration
components simultaneously at several thousand points
in the human heart wall to visualize the wave propagation
along the heart wall, we found for the first time that there
are several types of vibration propagation which start at TQ
and TI. By considering the time, the propagation direction
and the dispersion properties of each vibration, the vibration at TQ was seen to correspond to the response of the
myocardium to electrical stimulation, which propagatesfrom the Purkinje fiber-myocyte junctions to the wholeheart and the vibrations at TI correspond to the propagation of the waves mechanically excited by closure of theatrioventricular valves. These phenomena have potential
for detection of regional myocardial tissue damage related
to propagation of the action potentials and regional
myocardial viscoelasticity.
Acknowledgments—The author is grateful to Prof. Yoshifumi Saijo of
Tohoku University for his helpful and valuable advice. The author isalso grateful to Prof. Emeritus Motonao Tanaka of Tohoku University,
Prof. Floyd Dunn of the Bioacoustics Research Laboratory of the University of Illinois and Dr. Jens E. Wilhjelm of the Technical University ofDenmark for useful discussions. The author also acknowledges theexperimental contributions of Assoc. Prof. Dr. Hideyuki Hasegawa in
our laboratory.—This study was partly supported by a grant-in-aid forscientific research from the Ministry of Education, Culture, Sports,
Science and Technology of Japan (2005-2007, No. 17206043).

REFERENCES
Axel L, Dougherty L. MR imaging of motion with spatial modulation ofmagnetization. Radiology 1989;171:841–845.
Buchalter MB, Weiss JL, Rogers WJ, Zerhouni EA, Weisfeldt ML,
Beyar R, Shapiro EP. Noninvasive quantification of left ventricularrotational deformation in normal humans using magnetic resonanceimaging myocardial tagging. Circulation 1990;81:1236–1244.

947

Durrer D, van Dam RT, Freud GE, Janse MJ, Meijler FL,
Arzbaecher RC. Total excitation of the isolated human heart. Circulation 1970;41:899–912.
Fleming AD, Xia X, McDicken WN, Sutherland GR, Fenn L. Assessment of colour Doppler tissue imaging using test-phantoms. Ultrasound Med Biol 1994;20:937–951.
Heimdal A, Støylen A, Torp H, Skjærpe T. Real-time strain rate imagingof the left ventricle by ultrasound. J Am Soc Echocardiogr 1998;11:
1013–1019.
Kanai H, Sato M, Koiwa Y, Chubachi N. Transcutaneous measurement
and spectrum analysis of heart wall vibrations. IEEE Trans Ultrason
Ferroelectr Freq Control 1996;43:791–810.
Kanai H, Hasegawa H, Chubachi N, Koiwa Y, Tanaka M. Noninvasive
evaluation of local myocardial thickening and its color-coded
imaging. IEEE Trans Ultrason Ferroelectr Freq Control 1997;44:752–768.
Kanai H, Koiwa Y, Zhang J. Real-time measurements of local myocardium motion and arterial wall thickening. IEEE Trans Ultrason Ferroelectr Freq Control 1999a;46:1229–1242.
Kanai H, Sugimura K, Koiwa Y, Tsukahara Y. Accuracy evaluation in
ultrasonic-based measurement of microscopic change in thickness.
Electron Lett 1999b;35:949–950.
Kanai H, Yonechi S, Susukida I, Koiwa Y, Kamada H, Tanaka M. Onsetof pulsatile waves in the heart walls at end-systole. Ultrasonics 2000;
38:405–411.
Kanai H, Koiwa Y. Myocardial rapid velocity distribution. Ultrasound
Med Biol 2001;27:481–498.
Kanai H, Katsumata S, Honda H, Koiwa Y. Measurement and analysis ofvibration in the myocardium telescopic motion for novel echographic diagnosis. Acoust Sci Technol 2003;24:17–22.
Kanai H. Propagation of spontaneously actuated pulsive vibration inhuman heart wall and in vivo viscoelasticity estimation. IEEE TransUltrason Ferroelectr Freq Control 2005;52:1931–1942.
Kanai H. Ultrasonic imaging of propagation of electric excitation in heartwall. IEEE Ultrason Symp 2007;753–756.
Katz AM. Physiology of the Heart. Philadelphia: Lippincott Williams &Wilkins; 2001.
Konofagou E, Luo J, Saluja D, Fujikura K, Cervantes D, Coromilas J.
Noninvasive electromechanical wave imaging and conduction
velocity estimation in vivo. IEEE Ultrason Symp 2007;969–972.
Kundo T. Ultrasonic nondestructive evaluation. New York: CRC Press;
2003.
Learoyd BM, Taylor MG. Alterations with age in the viscoelastic properties of human arterial walls. Circ Res 1966;18:278–292.
Luisada AA, Portaluppi F. The heart sounds: New facts and their clinicalImplications. New York: Praeger Scientific; 1982.
Mahoney LT, Smith W, Noel MP, Florentine M, Skorton DJ,
Collins SM. Measurement of right ventricular volume using cinecomputed tomography. Invest Radiol 1987;22:451–455.
Nasseri S, Bilston LE, Phan-Thien N. Viscoelastic properties of pig
kidney in shear, experimental results and modelling. Rheologica
Acta 2002;41:180–192.
Netter FH. A compilation of paintings on the normal and pathologic
anatomy and physiology, embryology, and diseases of the heart.
Summit, NJ: Ciba Pharmaceutical; 1969.
Notomi Y, Setser RM, Shiota T, Martin-Miklovic MG, Weaver JA,
Popovic ZB, Yamada H, Greenberg NL, White RD, Thomas JD.
Assessment of left ventricular torsional deformation by Doppler
tissue imaging: Validation study with tagged magnetic resonanceimaging. Circulation 2005;111:1141–1147.
Pernot M, Fujikura K, Fung-Kee-Fung SD, Konofagou E. ECG-gated,mechanical and electromechanical wave imaging of cardiovascular
tissues in vivo. Ultrasound Med Biol 2007;33:1075–1085.
Ramanathan C, Ghanem RN, Jia P, Ryu K, Zudy Y. Noninvasive electrocardiographic imaging for cardiac electrophysiology andarrhythmia. Nat Med 2004;10:422–428.
Rohr S, Kucera JP, Fast VG, Kléber AG. Paradoxical improvement of
impulse conduction in cardiac tissue by partial cellular uncoupling.
Science 1997;275:841–844.
Saijo Y, Tanaka M, Okawai H, Sasaki H, Nitta S, Dunn F. Ultrasonictissue characterization of infarcted myocardium by scanning acoustic
microscopy. Ultrasound Med Biol 1997;23:77–85.

Author's personal copy

948

Ultrasound in Medicine and Biology

Sarvazyan AP, Skovoroda AR, Emelianov SY, Fowlkes JB, Pipe JG,
Adler RS, Buxton RB, Carson PL. Biophysical bases of elasticity
imaging. Acoust Imaging 1995;21:223–240.
Sutherland GR, Stewart MJ, Groundstroem KW, Moran CM, Fleming A,
Guell-Peris FJ, Riemersma RA, Fenn LN, Fox KA, McDicken WN.
Color Doppler myocardial imaging: A new technique for the assessment of myocardial function. J Am Soc Echocardiogr 1994;7:
441–458.
Templeton GH, Nardizzi LR. Elastic and viscous stiffness of the canine
left ventricle. J Appl Physiol 1974;36:123–127.
Wang S, Lee WN, Provost J, Luo J, Konofagou EE. A composite highframe-rate system for clinical cardiovascular imaging. IEEE TransUltrason Ferroelectr Freq Control 2008;55:2221–2233.
Witkowski FX, Leon LJ, Penkoske PA, Giles WR, Spanok MR,
Ditto WL, Winfree AT. Spatiotemporal evolution of ventricularfibrillation. Nature 1998;39:78–82.

Volume 35, Number 6, 2009
Wyman BT, Hunter WC, Prinzen FW, McVeigh ER. Mapping propagation of mechanical activation in the paced heart with MRI tagging.
Am J Physiol Heart Circ Physiol 1999a;276:881–891.
Wyman BT, Hunter WC, Prinzen FW, Faris OP, McVeigh ER. Effects ofsingle- and biventricular pacing on temporal and spatial dynamics ofventricular contraction. Am J Physiol Heart Circ Physiol 1999b;282:
H372–H379.
Yoshiara H, Hasegawa H, Kanai H, Tanaka M. Ultrasonic imaging of
propagation of contraction and relaxation in the heart walls at hightemporal resolution. Jpn J Appl Phys 2007;46:4889–4896.
Zipes DP, Braunwald E. Braunwald’s Heart disease: A textbook of
cardiovascular medicine. Philadelphia: Elsevier; 2005.
Zwanenburg JJM, Götte MJM, Kuijer JPA, Hofman MBM, Knaapen P,
Heethaar RW, van Rossum AC, Marcus JT. Reduction in postsystolic
wall thickening during late preconditioning. Am J Physiol Heart Circ
Physiol 2004;288:787–794.