Received: August 20, 2005
Accepted: November 12, 2005

Fetal Diagn Ther 2006;21:458–465
DOI: 10.1159/000093889

Fetal Myocardial Thickening Measured
by Ultrasonic-Based Technique Called‘Phased-Tracking Method’
Shutaro Kunii a Junichi Sugawara a Yoshitaka Kimura a Noriaki Imai a
Hiroshi Chisaka a Hideyuki Hasegawa c Yoshiro Koiwa b Hiroshi Kanai c
Kunihiro Okamura a
Departments of a Obstetrics and Gynecology, b Cardiovascular Medicine, Tohoku University Graduate School of
Medicine, Sendai, c Department of Electronic Engineering, Graduate School of Engineering, Tohoku University,
Sendai, Japan

Key Words
Fetus  Ultrasonics  Myocardial contraction  Heart
failure  Imaging

Abstract
Objective: To evaluate fetal myocardial movement byusing newly developed ultrasonic technique. Methods:
We analyzed 50 normal fetuses between 25 and 41 weeks’gestation for changes in thickness of fetal myocardium
using the phased-tracking method, a technique with highvertical distance resolution and the potential to evaluatefine ventricular wall movements. We analyzed differences in the rate of change in ventricular wall thickness andin changes in the inner and outer wall layers with advancing gestation. We also analyzed myocardial thickening
period and evaluated the ratio of increasing thickness
period to stroke interval. Results: Mean thickness changing rate was significantly higher in the right (1.18 8
0.34 m/s/m) than in the left ventricular wall (0.86 8
0.31 m/s/m) (p ! 0.001). Mean ratio of increasing thickness period to stroke interval was significantly higher inthe right (0.57 8 0.064) than in the left ventricle (0.46 8
0.075) (p ! 0.001), indicating that myocardial contractionin the fetal right ventricle predominates. The thickness-© 2006 S. Karger AG, Basel
1015–3837/06/0215–0458$23.50/0
Fax +41 61 306 12 34
E-Mail karger@karger.ch
www.karger.com

Accessible online at:www.karger.com/fdt

changing rate of the bilateral ventricular walls was positively and linearly correlated with gestational age. The
myocardial-wall thickness-changing rate was higher inthe outer layer than in the inner layer in late gestation.
Conclusions: We conclude that measurement of the
thickness-changing rate of fetal ventricular walls using
the phased-tracking method might be useful for evaluation of fetal cardiac function.
Copyright © 2006 S. Karger AG, Basel

Introduction

Ultrasonic evaluation of fetal cardiac function is widely used, simple, and non-invasive. The major methods inthe clinical setting are M-mode echocardiography and an
indirect evaluation using the hemodynamic Doppler effect. Because the widths of areas for measurement areconsiderably smaller in fetuses than in adults, measurement errors and interexaminer differences are not negligible [1–3]. Cardiac function originates from myocardial
contractility, and reduction of myocardial movement by
insults such as hypoxia is thought to precede reduction of
output. However, there have been no methods to datethat allow observation of precise myocardial movements

Junichi Sugawara, MD
Division of Maternal Fetal Medicine, Department of Obstetrics and Gynecology
Tohoku University Graduate School of Medicine, 1-1, Seiryomachi, Aobaku
Sendai 980-8574 (Japan)
Tel. +81 22 717 7254, Fax +81 22 717 7258, E-Mail sugawara@mail.tains.tohoku.ac.jp

in fetuses. The methods for evaluation of cardiac function
in fetuses are thus quite limited compared to those available for adults. Development of a method for direct evaluation of myocardial movement in fetuses will be very
useful.
Recently, there have been studies on tissue Doppler
echocardiography using Doppler signals for evaluation of
myocardial movement in fetuses [4–7]. However, changes in myocardial thickness and cardiac movement by pulsation are measured without distinction by tissue Doppler echocardiography and changes in myocardial thickness alone are not recorded, making the method oflimited value for evaluation of myocardial dynamics.
Kanai et al. [8] reported a tracking method by whichmeasurement points of reﬂected ultrasonic pulsatile
waves ﬁxed in myocardium were accurately examined.
They also developed a modiﬁed phased-tracking methodwith which changes in myocardial thickness are continuously measured by integrating the difference in velocity
between two points along an ultrasonic beam. The timeand spatial resolutions of the phased-tracking method arevery high, and changes in the thickness of cardiac muscle
can be measured at a level of several micrometers [9].
Koiwa et al. [10] clinically examined the toxicity of doxorubicin hydrochloride in adult myocardium with use of
the phased-tracking method, and reported that the detection of myocardial microdisorders by this method may
be more sensitive than that by other ultrasonic measurement methods. Impairment of cardiac function may also
be observed in fetuses as changes in myocardial contraction.
In the present study, we evaluated whether changes inthe thickness of fetal myocardium could be measured by
the phased-tracking method, and we also examined differences in the thickness-changing rate between the bilateral ventricular walls and between the inner and outerlayers of the ventricular wall based on weeks of gestation.
Furthermore, we analyzed the myocardial thickening period and evaluated the ratio of myocardial contraction
time (t) to stroke interval (T) ratio of increasing thickness
period to stroke interval (RITS).

Materials and Methods
Subjects
Between January 2003 and December 2003 we examined 50
normal fetuses between 25 and 41 weeks of gestation (mean,
33.5 8 3.9 weeks). In all fetuses, gestational age was calculated
from the ﬁrst day of the last menstrual period and conﬁrmed byultrasound examination between 9 and 11 weeks of gestation. In-

Fetal Myocardial Thickening by
Phased-Tracking Method

clusion criteria for normal fetuses were singleton pregnancy, absence of fetal growth restriction, absence of fetal structural malformations on ultrasound and later at birth, and absence of maternaldisease affecting fetal growth. The mothers’ age range was 19–37
years (mean, 28.5 8 5.2 years). The study design was approved by
the institutional review board, and all women gave informed consent before participating in the study.
Measurement of Myocardial Layer Thickening
Using ultrasonic diagnostic equipment (Toshiba, SSA340A, Tokyo, Japan), the direction of the ultrasonic beam passing throughthe measurement points was selected in the four-chamber view, Bmode cross-sectional image so as to be almost perpendicular to theright ventricular (RV) wall and left ventricular (LV) wall during
measurement. Just after selection, the direction of the ultrasonicbeam was ﬁxed and the quadrature-demodulated signal of the RF
signal was A/D converted during several heartbeats. The principlesof the phased-tracking method, including theoretical and in vivo
evaluations for myocardial layer thickening rate, have been detailed previously [8, 9]. In brief, radiofrequency pulses with an angular frequency of 0 = 2f0 are transmitted at time intervals of Tfrom an ultrasonic transducer on the maternal abdominal wall. The
phase difference, (x;t), between the phase (x;t) of the quadrature-demodulated signal of the received signal, y(x;t), and the phase(x;t + T) of the quadrature-demodulated signal of the subsequently received signal, y(x;t + T), is given by(x;t) = (x;t + T) – (x;t) = –20/c0  x(t)(1)

where x(t) = x(t + T) – x(t) is the movement of the object during
the period T around time t, and c0 is the acoustic velocity in thehuman body. In our examination, the period T was set at 250 s.
Because the maximum value of the acceleration in the interventricular septum (IVS) is about 4 m/s2, the velocity of the adult IVS
changes at most by 0.001 m/s, which is 1/400 of the higher limit of
the measurable velocity (0.4 m/s) for the short period T of 250 s.
Thus, the velocity of the IVS is assumed to be constant during thepulse-repetition interval T. By dividing the movement x by theperiod T, the average velocity v(t + T/2) of the object during theperiod T is given byv(t +T/2) – x(t)/T = c0/20 (x;t)/T(2)

The phase difference (x;t) is accurately determined by theconstraint least squares approach based on the complex crosscorrelation between y(x;t) and y(x;t + T) under the condition thatsignal waveforms change only in phase values during the period
T. It is impossible to accurately determine the true lag value fromthe complex correlation function, which is derived from the standard normalized mean squared difference between the quadraturemodulated signals of the successively received signals [11]. However, introduction of the constraint is effective for determinationof the lag between these complex signals. By multiplying the resultant velocity (t + T/2) by the period T, the next depth x(t + T)of the object is estimated byx(t + T) = x(t) +(t + T/2) !T(3)

Using the resultant signal x(t + T), the displacement of theobject (the position of the region of interest) in the heart wall is successfully tracked, and the velocity signal Ax(t) on the large motion
due to the heartbeat is accurately measured.

Fetal Diagn Ther 2006;21:458–465

459

In the current study, a high-speed A/D converter with large-scale
memory was employed to analyze the complex signal resulting fromthe quadrature modulation of the signal received by a sector-typeultrasonic transducer connected to standard ultrasonic diagnostic
equipment. We used an ultrasonic frequency of 3.75 MHz, with apulse repetition interval of 222 s. The resultant real and imaginary
signals of the demodulated Doppler signal were simultaneously A/
D converted with a two-channel 12-bit A/D converter at a sampling
rate of 1 MHz. The initial positions of the multiple sampling points
across the wall were manually set along the ultrasonic beam. The
lower limit of resolution of the change in layer thickness was
0.5 m and the higher limit of measurable velocity was about
0.4 m/s, which was determined by aliasing with the conventional
Doppler system [8]. Measurement was performed in resting fetuses,
taking effects of fetal motions such as respiration-like movementon the cardiovascular system into consideration, and the mean
measurements in three cardiac cycles were analyzed. Measurement
was performed at the site perpendicular to the IVS at the height of
the tricuspid valve tip.
To visualize changes in thickness, the ventricular wall was divided into layers 0.75 mm thick, and thickness changing rate wasexpressed with colors. Blue indicated an increasing thickness of
myocardium, whereas red and yellow indicated thinning. Light
blue and yellow indicated more rapid myocardial changes. We examined whether homogeneous changes in fetal myocardial thickness corresponded with cardiac cycle stages and numerically evaluated observed myocardial thickening changes. The mean time (t)between starts of myocardial thickening and thinning was determined using the thickness-changing rate measured at intervals of
222 s (ﬁg. 1). Analysis of the RV and LV walls was separately performed, covering the entire ventricular wall (width, about 4.5 mm).
The RITS of the RV and LV walls were compared (ﬁg. 1). Furthermore, the relationship between gestational age and RITS was examined. The bilateral ventricular walls were divided into inner andouter layers at the center of the ventricular wall (width, about
2.25 mm), and their thickness-changing rate was separately determined to examine the relationship between thickness-changing rate
and gestational age.
Statistics
All data are expressed as mean value 8 standard deviation(SD). The Mann-Whitney test was used for two-way comparison ofdata. Values were considered signiﬁcantly different at p ! 0.05.
Correlations between age in gestational weeks and measurement
results were analyzed with use of linear regression analysis.

Results

Figure 2 indicates an example of the phased trackingmethod as performed on a normal fetus at 30 weeks gestation. Homogeneous changes in myocardial thickness
corresponding to cardiac cycle stages were observed in all
fetuses.
The mean thickness changing rate in the 50 fetuses was
1.18 8 0.34 m/s/m (mean 8 SD) in the RV wall and
0.86 8 0.31 m/s/m in the LV wall; the higher contraction

460

Fetal Diagn Ther 2006;21:458–465

rate of the RV wall was signiﬁcant compared with that of
the LV wall (p = 0.0001, ﬁg. 3). Correlations between
thickness changing rate of the bilateral ventricular walls
and gestational age were positive and linear (RV wall,y = 0.027x + 0.316, R2 = 0.112, p = 0.018; LV wall, y =0.024x + 0.094, R2 = 0.102, p = 0.023) (ﬁgs. 4, 5). The
mean RITS was signiﬁcantly higher in the RV (0.57 8
0.064) than in the LV (0.46 8 0.075) (p ! 0.0001, ﬁg. 6),
showing that myocardial thickening was more rapid andlonger in the RV wall than in the LV wall. There were
no correlations between RITS and gestational age (RV,
p = 0.17; LV, p = 0.11) (data not shown).
Figures 7 and 8 show the relationship between ratio of
thickness-changing rate of the outer layer to that of theinner layer for the RV and LV walls and gestational age,respectively. The ratio was signiﬁcantly correlated withgestational age in weeks (RV wall, y = 0.11x -2.65, R2 =0.403, p ! 0.0001, ﬁg. 7; LV wall, y = 0.146x-3.534, R2 =0.323, p ! 0.0001, ﬁg. 8).

Discussion

In this study, we measured microchanges in the thickness of local myocardium in normal human fetuses by thephased tracking method and found that thickening changes were more rapid and longer in the RV wall than in the
LV wall. Furthermore, the thickness changing rate of theouter layer of the myocardium increased as gestation advanced.
Since M-mode echocardiography was applied to fetuses in 1970 [12], direct measurement and evaluation ofchanges in fetal myocardial thickness using ultrasoundhave been attempted. There have been a number of studies on the increasing rate of wall thickness ([wall thickness
in systole – wall thickness in diastole]/wall thickness indiastole n 100) determined by measuring myocardial
thickness at the end of diastole and systole by M-mode
echocardiography. Sutton et al. [13] reported that there
were no differences in the increasing rate of wall thicknessof the RV wall and IVS between 20 and 40 weeks of gestation, but that the rate for the LV wall was signiﬁcantly
lower at 20 weeks than at 40 weeks of gestation; they suggested that the dominance of the LV is reduced with fetal
maturity . Kamoi et al. [14] reported that there were nodifferences in the increasing rate of wall thickness of thebilateral ventricular walls and IVS between gestational
trimesters but the rate was higher in the LV wall than in
the RV wall over the entire course of gestation; the author
suggested that the LV myocardium is dominant to that ofKunii /Sugawara /Kimura /Imai /Chisaka /Hasegawa /Koiwa /Kanai /Okamura

Stroke interval = T
Decreasing thickness

Diastole
Time

Velocity of
myocardial
thickness

Systolet
Increasing thickness

Fig. 1. Principle of average myocardial

thickness velocity (v) and RITS. t: Timeinterval of measuring myocardial thickness
velocity (222 s). v: Velocity of myocardial
thickness. Calculated average of V duringsystolic interval. RITS: (Increasing thickness interval:t)/(stroke interval:T).

Time interval = t

Minimum

Maximum

Minimum

V

Myocardial
thickness

Thickening velocity
Thinning

Thickening+3 m/s/m–3 m/s/m

40

RV wall

Distance (mm)30

Right ventricle

IVS

20

Left ventricle10

LV wall
0

0

0.5

1.0

1.5

2.0

2.5

Time (sec)Fig. 2. Results of the phased tracking method. The ventricular wall is divided into layers 0.75 mm thick, andthickness changing rate is color coded: blue, increasing thickness; red and yellow, thinning; light blue and yellow,
faster change. From top to bottom, these waves indicate the RV wall, IVS, and LV wall.

Fetal Myocardial Thickening by
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Fetal Diagn Ther 2006;21:458–465

461

p < 0.0001
Velocity of myocardial thickness (m/s/m)

2.0

Velocity of myocardial thickness (m/s/m)

1.6
1.4
1.2
1.0
0.8
0.6
0.4
0.2

y = 0.024 x + 0.094

R2 = 0.102 p = 0.023

1.8
1.6
1.4
1.2
1.0
0.8
0.6
0.4
0.2
0
24

26

28

30

0

32

34

36

38

40

42

Gestation (week)
RV wall

LV wallFig. 3. Comparison of RV wall and LV wall myocardial thickness

Fig. 5. Correlation between velocity of myocardial thickness in LV

velocity. In these normal fetuses (n = 50), mean contraction rate
was 1.18 8 0.34 m/s/m (mean 8 SD) in the RV wall and 0.86 8
0.31 m/s/m in the LV wall, a signiﬁcant difference (p ! 0.0001).

wall and gestational age (weeks).

y = 0.027 x + 0.316

p < 0.0001

R2 = 0.111 p = 0.018
0.7

1.75
0.6

1.50
1.25

0.5

1.00

0.4
RITS

Velocity of myocardial thickness (m/s/m)

2.00

0.75

0.3

0.50
0.2
0.25
0.1

0
24

26

28

30

32

34

36

38

40

42

Gestation (week)

0
RV wall

LV wallFig. 4. Correlation between velocity of myocardial thickness in RV
wall and gestational age (weeks).

Fig. 6. RITS in the RV and LV walls. Mean RITS was signiﬁcantly higher in the RV wall (0.57 8 0.064) than in the LV wall (0.46
8 0.075) (n = 50) (p ! 0.0001).

the RV during fetal development as a pre-stage of LV
functional dominance after birth.
Although these studies used almost the same method,
the results differed. This may be because measurement ofchanges in the thickness of fetal cardiac muscle (considered to be about 1–2 mm wide) was difﬁcult at the distance resolution of conventional ultrasound diagnostic
instruments, taking into consideration the vertical dis-462

Fetal Diagn Ther 2006;21:458–465

Kunii /Sugawara /Kimura /Imai /Chisaka /Hasegawa /Koiwa /Kanai /Okamuray = 0.112 x – 2.651

R2 = 0.403 p < 0.0001

y = 0.145 x – 3.534

3.0

2.50

R2 = 0.323 p < 0.0001

Ratio of outer to inner velocity

Ratio of outer to inner velocity

2.25
2.00
1.75
1.50
1.25
1.00
0.75
0.50

2.5

2.0
1.5

1.0

0.5

0.25
0

0
24

26

28

30

32

34

36

38

40

42

Gestation (week)

Fig. 7. Ratio of thickness changing rate of the outer layer to the in-

24

26

28

30

32

34

36

38

40

42

Gestation (week)

ner layer of the RV wall (n = 50) with gestational age (weeks).

Fig. 8. Ratio of thickness-changing rate of the outer layer to the inner layer of the LV wall (n = 50) with gestational age (weeks).

tance resolution of about 1 mm in currently used ultrasound diagnostic instruments. The thickness-changing
rate of the IVS wall was signiﬁcantly lower than that of
the RV and LV walls, suggesting that the septum was not
positively involved in ejection from the ventricles. A
study by Vosters [15], in which M-mode echocardiography was used, also reported that the wall thickening rateof the IVS during systole was signiﬁcantly low.
Because ejection time has been reported as reduced in
adult patients with heart failure [16], measurement of thesystolic time interval by electrocardiography and Doppler echocardiography has been widely used for clinicalevaluation of cardiac function. To evaluate cardiac function in fetuses, a method using the difference in blood
ﬂow time around the valve, called the Tei index, and theratio was reported [17]. The Tei index in fetuses with intrauterine growth restriction and fetuses with gestation
complicated by diabetes differs from those seen in normal
fetuses, suggesting that this index can be used for screening of cardiac function abnormality in fetuses with highsensitivity [17]. It has also been reported that there is asigniﬁcant difference in the Tei index between hydropic
and normal fetuses, with the index correlated with theseverity of heart failure [18]. However, because the Tei
index returns to normal in severe heart failure, and simultaneous measurement of two or more blood ﬂows in asingle cardiac cycle is impossible when measuring the ratio of blood ﬂow time around the valve, there are prob-

lems to be solved such as errors caused by the effect ofchanges in heart beat. Furthermore, because this method
is an indirect evaluation of cardiac function using theblood ﬂow interval, effects of pre- and post-load may not
be avoided, suggesting that it is unclear whether evaluation of cardiac function with this method is accurate.
Because myocardial movement can be directly observed with high accuracy by the phased tracking method,
myocardial contraction time can be accurately measured.
Further, because simultaneous measurement of the RV
and LV walls is possible with this method, changes inheartbeat may not affect measurement. Finally, because
myocardial contraction time and thickness changing rate
can be simultaneously measured, a more accurate anddirect evaluation of cardiac function is possible.
In this study, we measured changes in myocardial
thickness in normal fetuses by the phased tracking method, and we found more rapid and longer movements in
the RV wall than in the LV wall. The RV is generally
dominant in fetuses due to the direction of blood ﬂow andoutput from the heart [19]. The results of our study indicate that fetal myocardial activity itself was also dominant in the RV.
In our preliminary experiment, we examined thickness changing rate of myocardium in sheep fetuses withacidemia caused by umbilical cord compression with useof the phased tracking method; the thickness changing
rate and RITS in the RV were markedly reduced by ag-

Fetal Myocardial Thickening by
Phased-Tracking Method

Fetal Diagn Ther 2006;21:458–465

463

gravation of blood gas conditions compared with those in
the LV. Kamitomo et al. [20] reported that the output
from the LV was not signiﬁcantly lower in hypoxic sheep
fetuses than in the control group, but RV output was signiﬁcantly lower in the former group than in the latter. If
reduction of contraction rate of the RV myocardium occurs prior to reduction of output, measurement of the
myocardial thickening rate by the phased tracking method may be used for earlier diagnosis of hypoxia-induced
functional RV insufﬁciency in fetuses. In fetuses with intrauterine growth restriction and in fetuses whose gestations are complicated by maternal diabetes, the relationship of thickness changing rate between the RV and LV
were reversed (data not shown), suggesting that the normal dominance of the RV had almost failed.
With regard to evaluation of changes in the thicknessof the local ventricular wall, there was a study in which
the ventricular wall of an adult dog was divided into twoor three layers using thread passing through the myocardium as the marker, and the wall thickening rate of thelayers was measured using an ultrasonic diagnostic apparatus. The wall thickening rate of the inner layer was
reported to be higher than that of the outer layer in adults[11, 21, 22]. In the present study, measurement of the
thickness changing rate of local myocardium in fetuses by
the phased tracking method indicated that the rate of theouter layer was higher than that of the inner layer duringlate gestation. Fisher et al. [23] examined the distributionof blood ﬂow in the myocardium of sheep fetuses, newborn lambs, and adult sheep and reported that the distri-bution of local blood ﬂow outside the myocardium wassigniﬁcantly higher in sheep fetuses in late gestation thanin the newborn lambs and adult sheep [4]. Because the
distribution of blood ﬂow in local myocardium is considered to be related to oxygen consumption, contraction of
the outer layer of myocardium may be more active in lategestation than after birth. Hay and Low [24] reported thatthe construction of denser and more regular ﬁlaments andtheir arrangement in a more ﬁxed direction were observedin myoﬁbrils in non-dividing myocardial cells as gestation proceeded and that these changes were more marked
in the outer myocardial layer. The higher thickness changing rate of the outer layer of myocardium in late gestation
may be caused by the high distribution of blood ﬂow inthe outer layer as well as physiological changes such as
more rapid maturity of the myocardial microstructure.
The evaluation of local myocardium by the phased
tracking method has just started, and its importance will
be clariﬁed by studying measurement of the ventricular
walls in fetuses with disorders and in neonates.
In this study, we measured changes in the thickness of
fetal myocardium by the phased tracking method andconﬁrmed that the thickening changes were more rapid
and longer in the RV wall than in the LV wall. Secondly,
the thickness changing rate of the outer layer of myocardium increased with progression of gestation. This study
suggests that measurement of changes in the thickness of
fetal myocardium might be a good diagnostic tool for theevaluation of fetal cardiac function.

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