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Japanese Journal of Applied Physics 56, 07JF04 (2017)https://doi.org/10.7567/JJAP.56.07JF04

Mechanism of synchronized change in ultrasonic integrated backscatter acrosshuman heart wall
Yumi Tobinai1, Hirofumi Taki2,1, and Hiroshi Kanai1,2*
1Graduate School of Engineering, Tohoku University, Sendai 980-8579, Japan
Graduate School of Biomedical Engineering, Tohoku University, Sendai 980-8579, Japan2*E-mail: kanai@ecei.tohoku.ac.jp
Received November 25, 2016; accepted February 15, 2017; published online June 2, 2017
Ultrasonic integrated backscatter (IB) from the heart wall, which has been employed for quantitative tissue characterization of the myocardium, isknown to have cyclic variation-a decrease in systole and an increase in diastole. In the present study, by tracking the measurement position of the
myocardium and compensating for the movement due to the heartbeat, IB and its temporal variation were obtained from the same site with a hightemporal resolution of 1.73 ms. In an in vivo study on a healthy subject, the temporal variation of IB values homogeneously changed across theheart wall, especially during the slow ﬁlling and the atrial systole phases. This new ﬁnding shows that the IB value reﬂects a small movement of the
myocardium of about 5 mm/s. Thus, the proposed measurement has a potential for quantitative and accurate evaluation of the contraction andrelaxation of the myocardium. © 2017 The Japan Society of Applied Physics

1.

Introduction

Ultrasonic diagnosis is non-invasive and inexpensive, andhas thus been widely used in the diagnosis of heart disease. In
patients with a history of myocardial infraction and hypertrophic cardiomyopathy, echogenicity of the diseased heart
wall is increased in ultrasonic B- and M-mode images.1,2)
Therefore, several approaches have been reported that use theultrasound image brightness pattern for the diagnosis of theheart disease. In addition, these approaches have also beenused in the evaluation of the change in thickness of the heartwall,3) blood ﬂow measurement of the cardiac lumen by theultrasonic Doppler method,4) and measurement of the left
ventricular ejection fraction.5) These methods are suitable for
evaluating the structure, blood ﬂow, and movement of theheart. However, it is necessary to improve their accuracy todetect pathological changes in the tissue. Therefore, moreaccurate and quantitative tissue characterization of the
myocardium using ultrasound imaging is desired.
Ultrasonic integrated backscatter (IB) from the heart wall,
which reﬂects myocardial deformation at a wavelength ofabout 500 µm,6,7) is obtained by averaging the ultrasonicscattering power of the returned signal from a region in thetissues. Several research studies have shown that anincrease in IB and ultrasonic attenuation of the myocardium
has a high correlation with the density of the collagenﬁbers.8–10)
Madaras et al. found that IB from the normal myocardium
shows cyclic variation-a decrease in systole and an increasein diastole during one cardiac cycle.11) Wickline et al.
explained the cyclic variation of IB using a Maxwell modelthat consists of three elements: the contractile element insidemyocardial cells, and the elastic elements inside and outside
cells arranged in a series-parallel conﬁguration representing
the physical properties of the myocardium.12) In this model,
by the activated contractile element which stretches a seriesof elastic elements during systole, the elastic modulus andacoustic impedance inside cells are increased. This process
decreases the mismatch in acoustic impedance between thecells and the intercellular substances, resulting in a decreaseof the IB value. During diastole, on the other hand, since only

the contractile element is extended and the stress and strain
applied to the series elastic element become negligible, theacoustic impedance inside the cells is reduced in contrast to
the increase during systole. Thus, the mismatch of acoustic
impedance between cells and intercellular substances isincreased, the IB value is increased, and the cyclic variationof IB reﬂects the change in the dynamics of the tissue and thepathological change.
It has been reported that ischemia decreases the cyclic
variation of IB.13–18) One of the factors that aﬀects the cyclic
variation of IB is the change in the angle of the ultrasonicbeam and the direction of the myocardium ﬁber.19–21) Hallet al. reported that the angle dependence on the backscatterfrom the intercellular substances with the myocardial cells is
equal to that without myocardial cells.22) That work showedthat the large variation in IB indicates the healthiness ofthe myocardium. Another factor involved in the decreasein IB cyclic variation due to ischemia is ﬁbrosis of the
myocardium.23) In severe myocardial ﬁbrosis, the IB value isalways high during one cardiac cycle, decreasing its cyclic
variation. This phenomenon is thought to be caused by anincrease of collagen ﬁber content and a decrease of systolic
function caused by ﬁbrosis of the myocardium. Thus,
various research studies have suggested the possibility thatthe temporal change of IB in the heart wall can be used toassess the myocardial contractile function because it reﬂects
change in the dynamics of tissue, including pathologicalchanges.24–26) However, most such studies have not investigated the temporal variations of IB using a high-frame-rate
measurement.
In the present study, therefore, the position at which the
myocardium was measured was tracked and IB and its
temporal variation were obtained at the same site bycompensating for movement due to the heartbeat. The IB
and its temporal variation had a high temporal resolution of
1.73 ms. Furthermore, the variation of IB during succeeding
frames was calculated in order to observe the temporalchange of IB. As a result, the regional IB values and thevariation of IB during one cardiac cycle for a healthy humanheart were obtained. Based on these ﬁndings, a hypothesis for
its mechanism is proposed in the discussion section.

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Experimental methods

2.1 Tracking of the heart wall using the phased
tracking method

The heart has a translational motion due to the heartbeat, andthe contraction and relaxation of the myocardium change theheart wall thickness. For evaluating the IB in each region ofinterest (ROI) during one cardiac cycle, the measurement
position of the myocardium is tracked by suppressing theeﬀect of the translational motion of the heart wall on themeasurement of the thickness. In this study, the phased
tracking method27,28) was employed to measure IB at thesame site of the heart wall.
Radio frequency (RF) pulses with angular frequency
ω0 = 2πf0 were transmitted at a time interval of ΔT from anultrasonic transducer on the chest surface. The relationshipbetween the instantaneous distance x(t) of a moving object
from the ultrasonic transducer at time t and the instantaneous
period τ(t) required for one-way transmission from theultrasonic transducer to the object is represented byxðtÞ ¼ c0 $ !ðtÞ;

(a)

ð1Þ

where c0 is the acoustic velocity in the human body. The
phase "ðx; tÞ of the received signal from the object is given by
the angular frequency ω0 multiplied by twice the delay time
τ(t) in the one-way propagation as follows:"ðx; tÞ ¼ 2!0 !ðtÞ ¼ 4#f0

xðtÞ
:
c0

ð2Þ

From this equation, the phase diﬀerence !"ðx; tÞ between thereceived signals for the successively transmitted pulses in theinterval ΔT is given by
4#f0!"ðx; tÞ ¼ "ðx; t þ !TÞ & "ðx; tÞ ¼
!xðtÞ:c0c0!"ðx; tÞ:4#f0

Fig. 1. (Color online) IB measurement at the same site of the myocardium
during one cardiac cycle. (a) Setting of the region of interest. (b) Process for
estimation of IBi (n) for the i-th layer.

1IBi ðnÞ ¼ 10 log10!Di ðnÞ

ð3Þ

Therefore, the displacement Δx(t) of the object during theperiod ΔT from a time t is estimated by!xðtÞ ¼(b)

ð4ÞSince this technique enables estimation of the displacement
Δx(t) of the object with a high degree of accuracy, both endsof the ROI set in each beam are accurately tracked. The
position x(t) and the length ΔD(t) of the ROI are followed in
response to translation and thickness change of the heart wall,
respectively, and IB is measured in the tracked region as
described below by Eq. (6). Furthermore, from Δx(t), theaverage velocity of the object during the period ΔT is given by
!
"
!T
!xðtÞ
!"ðx; tÞ
¼ c0 $v^ t þ
:ð5Þ
¼
2!T
4#f0 $ !TThis allows estimation of the myocardial velocity at the samesite.
2.2 High temporal resolution measurement of IB
As shown in Fig. 1(a), at the time of the R-wave in theelectrocardiogram (ECG), measurement layers (ROIs) with athickness of 616 µm were set along each beam, the intervalof the layer centers being 38.5 µm. The displacement of eachlayer was tracked at both ends of each layer during one
cardiac cycle. The IB value of i-th layer (i-th ROI) in the n-thframe, IBi (n), was calculated by29)

Z x2i ðnÞx1i ðnÞ

jzðn; xÞj2 dx;

ð6Þ

where zðn; xÞ is the received RF signal at a depth x of n-thframe, x1i (n) and x2i (n) are the positions of the upper andlower ends of i-th layer in n-th frame, and ΔDi (n) =x2i (n) − x1i (n) is the length of i-th layer (i-th ROI) in thedepth direction, as shown in Fig. 1(b).
Furthermore, the variation of IB among succeeding frames
was evaluated in order to observe the temporal change of
IB. The calculated IB contains many high-frequency components, which may originate from time variance in theamplitude of the reﬂected signal and in the estimation of thelength of the layer in Eq. (6). To suppress the high-frequency
components of the IB waveform, time averaging of the IB
waveform was applied with Hanning window w(n) given by!
"
2#nwðnÞ ¼ 0:5 & 0:5 cosðn ¼ 0; 1; . . . ; N & 1Þ; ð7Þ
N

where N is the length of the Hanning window, that is, the IB
waveform is averaged during N frames. Furthermore, using
the averaged IB, IBi ðnÞ, the variation of IB, ΔIBi (n), wasobtained by!IBi ðnÞ ¼

1' fIBi ðnÞ & IBi ðn & 1Þg:
!T

ð8Þ

2.3

Experimental setting
Using an ultrasonic diagnostic device (Hitachi-Aloka
ProSound F75) with a 3 MHz sector probe (Hitachi-Aloka

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Jpn. J. Appl. Phys. 56, 07JF04 (2017)

Y. Tobinai et al.

Fig. 2. Five ultrasonic beams were set in the parasternal long-axis
ultrasound image of the heart of a 22-year-old healthy male subject. Right
ventricular (RV), interventricular septum (IVS), left ventricular (LV), left
ventricular posterior wall (LVPW), and left atrium (LA).

UST-52105), RF signals were acquired in a parasternal longaxis ultrasonic image of the heart of a 22-year-old healthy
male. Figure 2 shows the B-mode image of the heart of thesubject. Five ultrasonic beams were sparsely set every 10°
and scanned to achieve a high temporal resolution of a 579Hz-frame rate (ΔT = 1.73 ms). The IB value of the i-th layer
in n-th frame, IBi (n), of Eq. (6) was obtained, and by
averaging IBi (n) with a Hanning window of a 71-ms widthof Eq. (7), the averaged IB, IBi ðnÞ, was obtained. Finally, thevariation of IB, ΔIBi (n), of Eq. (8) was estimated at a frameinterval of ΔT = 1.73 ms.
3.

Results and discussion

Figure 3 shows the variation of IBs, {ΔIBi (n)}, along
beam 3 in the IVS and LVPW of Fig. 2 during one cardiac
cycle superimposed on a M-mode image. In the latter halfof diastole, the sign of the variation of IBs, {ΔIBi (n)},changed synchronously across the IVS and LVPW, where
the change cycle was about 60–100 ms. Figure 4 shows theaveraged IBs, fIBi ðnÞg, at three diﬀerent depths in the IVS,
as shown in the striped pattern which appeared in thevariation of IBs, {ΔIBi (n)}, in Fig. 3, that is, in the latter halfof diastole from 0.60 to 1.03 s, and Fig. 5 shows the change
in thickness of the IVS in the corresponding period. The
peaks and dips of averaged IB waveforms, fIBi ðnÞg,appeared almost simultaneously at all depths. Since thethickness change of each measurement layer was smaller than
the wavelength (λ = 500 µm), as shown in Fig. 5, theaveraged IB values, fIBi ðnÞg, in Fig. 4 changed even whena change in thickness in Fig. 5 was suﬃciently small
compared with the wavelength. Thus, the cause of thevariation of IBs, {ΔIBi (n)}, in Fig. 3(a) cannot be explained
only by the change in thickness.
The main scatterers in myocardium are the collagen ﬁbers
that surround the myocardium ﬁbers, as shown in Fig. 6.
The myocardium has a layer structure, each layer of which
consists of three or four myocardium ﬁbers (70–100 µm), andthe layer boundaries (0–50 µm) include an abundance ofcollagen ﬁbers.30) Therefore, the layer interval is about
100 µm, which corresponds to an interval is about λ=5 in thepresent study (λ = 500 µm).
Figure 7 shows a model of the change in IB originating in
the change in thickness. When scatterers of identical size are
distributed regularly at a constant interval of Δx = 100 µm, as

Fig. 3. (Color online) Variation of IB, {ΔIBi (n)}, during one cardiac
cycle in the IVS and LVPW. (a) Variation of IB, {ΔIBi(n)}, along beam 3
superimposed on an M-mode image. (b) ECG. (c) Phonocardiogram (PCG).
(d) Velocity waveform vi(t) of each point in the IVS. (e) Velocity waveformvi(t) of each point in the LVPW.

(a)

(b)

(c)

Fig. 4. (Color online) Averaged IB signal in the IVS. (a) RV side,(b) middle, and (c) LV side.

Fig. 5. (Color online) Change in thickness during the latter half ofdiastole in the IVS.

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Y. Tobinai et al.

Fig. 6. (Color online) An illustration of layered structure of the
myocardium.

(a)

(a)

(b)
Fig. 8. (Color online) Displacement Δx(t) of Eq. (4) during one cardiac
cycle at ﬁve diﬀerent depths in the IVS of the same human subject.
(a) Positions of ﬁve diﬀerent depths in the B-mode image with space scan.
(b) Displacement waveform Δxi(t).

(b)
Fig. 7. (Color online) A model showing dependence of the relationshipbetween change in the interference state of the scattered waves and the IBvalue on change in thickness in the myocardium when scattering intensitiesof the scatterers are uniform (a) and non-uniform (b).

shown in Fig. 7(a), the scattered echoes cancel each other out
regardless of the contraction (Δx = 125 µm) and relaxation(Δx = 83 µm) of the myocardium, resulting in a low IB value
at almost all times. In contrast, when scatterers of diﬀerent
size are distributed at diﬀerent intervals, as shown in
Fig. 7(b), a slight change in the tissue thickness varies theinterference state of the echoes from scatterers, resulting ina large change in IB. Since the change in thickness during
the latter part of diastole in Fig. 3(a) is suﬃciently smaller
than λ=2, as shown in Fig. 5, the change of IB values may becaused by the process shown in Fig. 7(b).
According to the above model, it can be explained that thesynchronized variation of IBs, {ΔIBi(n)}, across the heart
wall in Fig. 3(a) occurs by the synchronized contraction andrelaxation across the heart wall. Figure 8(b) shows thedisplacements {Δxi (n)} in the myocardium of the myocardial
layers during one cardiac cycle at ﬁve diﬀerent depths set in
the IVS, as shown in Fig. 8(a). The diﬀerence among thedisplacements {Δxi (n)} of ﬁve layers became relatively small
after 0.6 s in the slow ﬁlling and the atrial systole phases. It
can be said that all the myocardial ﬁber layers across theheart wall showed similar motion. In these phases, the left
ventricular volume greatly increased and then the left
ventricular pressure slightly increased. Since the sarcomere
length is constant in these phases,31) the averaged IBs,
fIBi ðnÞg, in these phases observed in Fig. 4 may originate
from the minute thinning of the myocardium across the heart
wall caused by the increase of the ventricular volume.
This assumption was conﬁrmed by the following experiment using a bovine heart. As shown in Fig. 9, the IVS ofa bovine heart with a length of 90 mm and a thickness of
35 mm was extracted and ﬁxed in a water tank withphysiological saline solution of 0.9% concentration at
23 °C. Similar to the parasternal long-axis image of thehuman heart, the IVS was ﬁxed so that the right ventricularside was set at the upper side and the left ventricular side wasset at the lower side. Since the left ventricular volume
increases about 1.5 times in the slow ﬁlling phase andffiffiffiffiffi
pffitheatrial systole phase, the IVS lengthens by about 1:14 ¼ 3 1:5
times. Thus, the extracted IVS of the bovine should be
stretched at least by 13 mm, which corresponds to 14% of the
90 mm length of the IVS. In the actual experiment, it was
stretched by 20 mm. By setting both ends of the IVS to thearms of a stage controller using forceps, one side of the IVS
was stretched by 20 mm for 4 s at a constant speed, resulting

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Y. Tobinai et al.

(a)
(b)

(a)

(c)

(d)

(b)
Fig. 9. (Color online) IB measurement of the IVS of the bovine heart.
(a) Experimental system. (b) State of measurement.

Fig. 11. (Color online) Averaged IB signal in the IVS of the bovine heart
in Fig. 9 at three diﬀerent typical layers. (a) Positions of three diﬀerent depth
layers. Averaged IB signals, fIBi ðnÞg, for (b) RV side, (c) middle, and(d) LV side.

Fig. 12. (Color online) Change in thickness in the IVS of the bovine heart
in Fig. 9.
Fig. 10. (Color online) Variation of IB, {ΔIBi(n)}, in the IVS of thebovine heart in Fig. 9.

in a decrease in thickness of 2.7 mm. Using the same
ultrasonic diagnostic device and method as applied to thehuman heart in Fig. 3, the averaged IB values, fIBi ðnÞg, andthe variation of IBs, {ΔIBi(n)}, were obtained, as shown in
Figs. 10 and 11, respectively.
Figure 10 shows the variation of IBs, {ΔIBi(n)}, in the
IVS for 4 s superimposed on the M-mode image. A striped
pattern was clearly observed and the variation of IBs,
{ΔIBi(n)}, changed synchronistically across the bovine heartwall, similar to what occurred in the in vivo measurement in
Fig. 3(a). Figures 11(b)–11(d) show averaged IB waveforms,
fIBi ðnÞg, for three diﬀerent depth layers set along theultrasonic beam in the bovine IVS, as shown in Fig. 11(a),and Fig. 12 shows the change in thickness of the IVS. As
shown in Fig. 12, the thickness decreased almost linearly.

Though the thickness change of each measurement layer wasmuch smaller than the wavelength, the peaks and dips of
averaged IB waveforms, fIBi ðnÞg, appeared almost simultaneously across the heart wall. These results are consistent
with the in vivo measurement shown in Figs. 3(a) and5(b)–5(d). Since this experiment using a bovine heart
simulated the thinning of the human IVS in the slow ﬁlling
and atrial systole phases, the change in the averaged IB
values, fIBi ðnÞg, in slow ﬁlling and the atrial systole phasesof the human IVS can be explained as being due to thechange in the positions of non-uniform scatterers associatedwith the thickness change smaller than the wavelength.
4.

Conclusions

In this study, the measurement position of the myocardium
was tracked and IB and its temporal variation were obtained
from the same site by compensating for the movement due tothe heartbeat. The IB and its temporal variation have a high

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Jpn. J. Appl. Phys. 56, 07JF04 (2017)

Y. Tobinai et al.

temporal resolution of 1.73 ms. The peaks and dips of IB
waveforms appeared almost simultaneously across all depths
during the slow ﬁlling and atrial systole phases. Also, thethickness change of each measurement layer was muchsmaller than the wavelength. Therefore, by modeling thechange in interference state of the echoes from scatterers andIB values originating from the thickness of the myocardium,
non-uniformity of the scattering intensity of the scatter was
shown. Furthermore, the reason for the occurrence of thesynchronized variation of IB across the heart wall duringcontraction and relaxation was found by an experiment using
the bovine heart. These new ﬁndings show that the IB value
reﬂects a small movement of the myocardium of about
5 mm=s, showing the potential of using IB measurement toevaluate contraction and relaxation of the myocardium
quantitatively and accurately.

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