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Original Article
Acta Cardiol Sin 2012;28:25-33
Cardiac Imaging
Effect of Preload Reduction by Hemodialysis on
Left Ventricular Mechanical Parameters by
Three-Dimensional Speckle Tracking
Echocardiography
Bao-Tzung Wu,1 Mei-An Tsai-Pai,2 Hung-Yi Hsu,3,5 Pail-Seung Lin,2 Ching-Heng Lin4 and Ying-Tsung Chen1
Background: The effect of acute volume change by hemodialysis on contractile characteristics of the left ventricle
(LV) is not well known and has never been evaluated by 3-dimensional speckle tracking echocardiography
(3D-STE).
Methods: Twenty-three patients on chronic hemodialysis were recruited. 3D-STE was performed immediately
before and after hemodialysis in the dialysis room. The strain, displacement, rotation, torsion, and twist of LV were
calculated by commercial software for different segments of LV.
Results: Hemodialysis produced significant decreases in body weight, systolic and diastolic blood pressure, end-diastolic
and end-systolic volumes, but ejection fraction did not change. The regional torsion increased from 2.1 ± 1.2 to 2.7 ± 1.3
degree/cm (p = 0.012) after dialysis, though the crude global torsion, longitudinal, radial, circumferential, 3D strain, rotation
and twist of LV did not change significantly. The regional torsion correlated with the crude global torsion (r = 0.763,
p < 0.001). The change of ejection fraction after hemodialysis was significantly correlated with changes of circumferential
strain (r = -0.858, p < 0.001), longitudinal strain (r = -0.516, p = 0.012) and LV area (r = -0.883, p < 0.001).
Conclusion: Assessment of LV contractile characteristics by 3D-STE is easy and efficient. The regional torsion,
which could only be evaluated by 3D-STE, is more sensitive to reduction in preload possibly due to deformation
non-uniformity of myocardium in uremic patients.
Key Words:
Echocardiography · Hemodialysis · Speckle tracking · Torsion
INTRODUCTION
About 75% of patients receiving chronic dialysis developed a concentric or eccentric LV geometry and LV
hypertrophy.1,2 These structural changes of LV are associated with impaired LV perfusion and function.3-5
Contraction of helical myocardial fibers of LV produces torsional deformation of LV. This twisting motion
of LV has been shown to be a key factor of normal systolic and diastolic myocardial function in both animals
and humans. Assessment of LV torsion deformation assists in the understanding and quantification of LV function.6-10 LV torsion can be assessed using several techniques such as implanted radiopaque markers, sonomicrometry, magnetic resonance imaging (MRI), and
echocardiography. The radiopaque marker and sono-
Chronic pressure and volume overload can lead to
left ventricular (LV) remodeling in uremic patients.
Received: June 30, 2010
Accepted: December 30, 2010
1
Section of Cardiology; 2Section of Nephrology; 3Section of Neurology,
Department of Internal Medicine; 4Department of Medical Research,
Tungs’ Taichung MetroHarbor Hospital; 5Chung Shan Medical
University, Taichung, Taiwan.
Address correspondence and reprint requests to: Dr. Mei-An Tsai-Pai,
Section of Nephrology, Tung’s Taichung MetroHarbor Hospital,
No. 699, Sec. 1, Chungchi Rd., Wuchi, Taichung 43545. Taiwan.
Tel: 886-4-2658-1919 ext. 73090; Fax: 886-4-2658-2193; E-mail:
[email protected]
25
Acta Cardiol Sin 2012;28:25-33
Bao-Tzung Wu et al.
micrometry were only used in animal studies. Cardiac
MRI can be used in humans and represents an assessment “gold standard.” This technique is only used in a
few medical centers in Taiwan. Two-dimensional speckle
tracking imaging echocardiography (2D-STE) has provided a new opportunity for the noninvasive evaluation
of LV torsional deformation.11-16 However, the 2D-STE
could only detect a portion of real 3-dimensional myocardial motion in 2-dimensional section plane of echocardiography. Now, three-dimensional speckle tracking
echocardiography (3D-STE) can evaluate the LV motion
in all directions and can overcome the out-of-plane limitation. The applications of 3D-STE in evaluation of LV
function had only been described in a few reports.17-22
Hemodialysis in uremic patients removes a large
amount of fluid from the body in a few hours. Change in
LV volume during dialysis will alter LV contraction and
strain as described by previous studies.23 The effect of
acute volume change by hemodialysis on LV torsion has
never been evaluated by 3D-STE. The effect of preload
change on LV torsion is controversial. Using different
methods and different subjects (animal or human) will
generate different results. The aim of this study was to
evaluate the LV torsional function in chronic uremic patients, and to compare changes in LV torsional function
immediately before and after dialysis by using 3D-STE .
There are several methods to describe LV torsion.24,25 In
this article, we used crude global torsion and regional
torsion to measure the LV short axis function. In both the
normal and the diseased heart, LV is characterized both
morphologically and functionally by a high degree of
regional non-uniformity. This deformation non-uniformity of myocardium varies from base to apex (regional
torsion). The regional torsion represents the different
rotation angle between two LV short axis planes nearby
and is expressed as “degree/cm”. It is evident from the
literature that the LV deformation is complex and closely
related to the variations in transmural fiber orientation,
irregular shape of the left ventricle, and local differences
in ventricular morphology.
maintenance hemodialysis. All patients were in sinus
rhythm and had received regular hemodialysis three
times a week, according to a standard dialysis program,
for three months or longer. 3D-STE was performed
within 30 minutes before vein puncture for hemodialysis, and after removal of the catheter in all participants.
3D speckle tracking echocardiography
3D-STE was performed from the apical position
with PST-25SX probe (Artida system, Toshiba Medical
Systems, Tokyo, Japan) by the same experienced technician, using a frame rate of 20-30 Hertz. The apical 2
chamber and 4 chamber views, short axis views at different levels of LV from the base to apex, LV endocardial and epicardial boundaries were automatically
reconstructed and tracked in 3D space throughout the
whole cardiac cycle (Figure 1). Subsequently, the endocardial surface was manually adjusted when necessary
in the five planes that best match the actual endocardial
position. The LV was automatically divided into 16
three-dimensional segments, according to American
Society of Echocardiographic recommendation. The
software automatically tracked the contour on the subsequent frame in different vectors simultaneously. The
radial and longitudinal displacement and rotation, torsion, and twist were automatically calculated for each
segment.
Strain, displacement, rotation and torsion
Strain was calculated as: strain = (Lf - Lo)/Lo, where
L f is the final segmental length and L o is the original
segment length at the peak of the R wave of QRS complex. Longitudinal strain (Ls) is defined as the percentage change in regional length in the direction of the longitudinal axis of the endocardium. Circumferential strain
(Cs) is defined as the percentage change in the regional
length in the circumferential direction of the endocardium, and radial strain (Rs) as the percentage change
in wall thickness in the direction of the endocardium. 3D
strain is a true 3D radial strain measurement, defined as
the percentage change in wall thickness in the direction
toward the endocardium in three-dimensional spaces
(Figure 2). Displacement is the displacement of the
endocardial surface (mm) in the direction perpendicular
to the endocardial contour. A positive value indicates
displacement toward the center. Radial displacement is
SUBJECTS AND METHODS
Study population
The study group included 23 uremic patients on
Acta Cardiol Sin 2012;28:25-33
26
Effect of Preload Reduction on 3D Strain and Torsion
C
A
D
B
Figure 1. Three-dimensional speckle tracking echocardiography showed reconstructing imaging respond to the apical 4-chamber (A, upper), the
apical 2-chamber (A, lower), and 3 short-axis views at different levels (B); the plastic bag 3-dimentional and segmental strain images of left ventricular (C); and parametric image of regional circumferential strain-time curves (D).
calculated from the short axis view and longitudinal displacement from the apical view. 3D displacement is
measured in 3D dimensional space. Area tracking is the
rate of change in the area of a regional part of the
endocardial contour. Rotation is the rotary motion of the
myocardium during contraction, while the apex moves
counter-clockwise and the base rotates clockwise.
Counter-clockwise is defined as plus direction. Twist is
the difference in myocardial rotation at any given short
axis level relative to the corresponding point at the left
ventricular base (Figure 2).
A
D
B
Crude global torsion and regional torsion
Torsion is a measurement of the degree of a point
on the LV short axis segment rotated around the long
axis, subtracting the rotation of a reference point on
the basal short axis plane, and dividing the distance
between these two points. Counter-clockwise rotation
is expressed in a positive value and clockwise rotation
in a negative value. Crude global torsion (so-called
basal torsion by the manufacturer), is calculated by net
LV rotation angles obtained from basal (clockwise)
and apical (counter-clockwise) short axis planes at the
C
E
Figure 2. Calculation of strain, rotation and twist Strain is calculated
as (Lf - Lo)/Lo ´ 100% in longitudinal (A), circumferential (B) and circumferential (C) directions as well as in dimension. (D) In each
short-axis plane, rotation (degree) is calculated as the rotatory motion
about the center of the left ventricle. Counterclockwise rotation is expressed with positive values. (E) Twists (degrees) calculation: difference
in rotation angle between each short axis and basal short axis. ED,
end-diastole; ES, end-systole; Lf, final segmental length in each subsequent frame; Lo, original segmental length in starting frame.
27
Acta Cardiol Sin 2012;28:25-33
Bao-Tzung Wu et al.
same time point dividing by the long axis length of LV
between both planes. Regional torsion is a summation
of torsional movement of different segments of LV.
The LV is divided into six to seven short-axis planes
with a pre-set thickness about 1 cm. The torsion of
each segment is calculated by the degree of a point on
the LV wall rotating around the long axis relative to a
nearby point, and dividing by the distance between
these two points. Although every LV long axis distance is different, the values are consistent even
though the distances between different points are not
the same (Figure 3).
Intraobserver and interobserver variability
Intraobserver variability was determined by having
an experienced sonographer repeat the measurement of
LV torsion in 10 randomly selected subjects. Interobserver variability was determined by having an echocardiography specialist repeat the measuring of these
variables after the first sonographer. Intraobserver and
interobserver variabilities were calculated as the absolute difference between the corresponding repeated measurements as a percentage of their mean.
Figure 3. Rb: basal rotation angle, Rn: regional rotation angle at different short-axis planes, Ra: apical rotation angle (degree), L0: distance
between basal and apical short axis plane, Ln: distance between different regional short axis plane, Crude global torsion: (Rb-Ra)/Lo (degree/cm), Regional torsion: summation of (Rn-1 - Rn)/Ln (degree/cm).
Hemodialysis did not produce significant changes in
longitudinal, radial, circumferential, or 3D strain of LV.
The regional LV torsion increased from 2.1 ± 1.2 to 2.7
± 1.3 degree/cm (p = 0.012) after dialysis. Crude global
torsion, rotation, twist and endocardial displacement in
all three directions did not change after hemodialysis.
Non-parametric Spearman’s correlation test showed
that both end-diastolic volume and end-systolic volume
were correlated with systolic BP (r = 0.507, p < 0.001
and r = 0.536, p < 0.001, respectively), diastolic BP (r =
0.435, p < 0.003; r = 0.462, p = 0.001), ejection fraction
(r = -0.553, p < 0.001; r = -0.711, p < 0.001), circumferential strain (r = 0.451, p = 0.002; r = 0.600, p < 0.001),
longitudinal strain (r = 0.309, p = 0.037; r = 0.427, p =
0.003), radial strain (r = -0.368, p = 0.008; r = -0.359, p
= 0.014), and LV area (r = 0.416, p = 0.004; r = 0.582, p
< 0.001). LV ejection fraction was significantly correlated with systolic BP (r = -0.442, p = 0.020), diastolic
BP (r = -0.350, p = 0.017), circumferential strain (r =
-0.822, p < 0.001), longitudinal strain (r = -0.589, p <
0.001), and LV area (r = -0.862, p < 0.001). Circumferential strain was correlated with longitudinal strain (r =
0.525, p < 0.001) and radial strain (r = -0.334, p =
Statistical methods
Data were expressed as mean ± SD for continuous
variables. Values of different groups of patients were
compared using the Student t test. Univariate correlation
was assessed by Pearson’s correlation coefficients. A p
value < .05 was considered statistically significant.
RESULTS
A total of 23 patients were enrolled in this study.
The mean patient age was 64 years (range 41 to 81
years). Ten patients were men, thirteen patients had hypertension, and twelve patients had diabetes. Table 1
summarizes clinical and echocardiographic characteristics in the 23 patients.
The body weight, systolic blood pressure (BP) and
diastolic BP were significantly decreased after hemodialysis (p < 0.001, p = 0.007 and p = 0.003, respectively). Hemodialysis produced significant decreases in
end-diastolic volume and end-systolic volume, though
LV ejection fraction did not change after hemodialysis.
Acta Cardiol Sin 2012;28:25-33
28
Effect of Preload Reduction on 3D Strain and Torsion
Table 1. Comparison of contractile properties of left ventricle before and after hemodialysis
Age (y/o)
Male/Female
Height (cm)
Systolic BP (mmHg)
Diastolic BP (mmHg)
Body weight (kg)
Heart rate (beat /min)
Circumferential strain (%)
Longitudinal strain (%)
Radial strain (%)
Rotation (deg)
Twist (deg)
Regional torsion (deg/cm)
Crude global torsion (deg/cm)
3-dimentional strain (%)
Radial displacement (mm)
Longitudinal displacement (mm)
3-dimentional displacement (mm)
Area (%)
End-diastolic volume
End-systolic volume
Ejection fraction (%)
Before dialysis
After dialysis
p
61.7 ± 9.113/10
155.5 ± 8.900
137.4 ± 18.40
82.8 ± 13.1
56.1 ± 10.3
84.2 ± 17.2
-24.0 ± 7.50-13.6 ± 4.7-0
22.9 ± 12.3
2.6 ± 1.8
3.5 ± 3.1
2.1 ± 1.2
1.2 ± 1.1
26.2 ± 12.3
5.0 ± 1.5
3.6 ± 1.2
7.3 ± 1.1
-34.9 ± 10.589.7 ± 35.9
44.1 ± 25.7
53.1 ± 9.00
126.2 ± 22.70
74.0 ± 11.9
53.9 ± 10.2
83.6 ± 15.8
-23.8 ± 8.20-13.9 ± 4.3019.8 ± 13.1
2.2 ± 2.0
4.3 ± 3.0
2.7 ± 1.3
1.4 ± 1.1
23.6 ± 12.8
4.8 ± 1.5
3.5 ± 1.2
7.3 ± 1.2
-35.1 ± 10.979.3 ± 27.5
38.0 ± 20.7
54.1 ± 9.50
0.007
0.003
< 0.001 <
0.426
0.976
0.411
0.260
0.121
0.339
0.012
0.858
0.287
0.191
0.773
0.726
0.858
0.036
0.016
0.394
DISCUSSION
0.019). Longitudinal strain was correlated with radial
strain (r = -0.501, p < 0.001). Among circumferential,
longitudinal and radial strain, only circumferential strain
was correlated with LV twist (r = -0.360, p = 0.014),
regional torsion (r = -0.320, p = 0.016) and crude global
torsion (r = -0.329, p = 0.025). The regional torsion significantly correlated with the crude global torsion (r =
0.763, p < 0.001). However, regional and crude global
torsion were not correlated with LV volumes or LV ejection fraction.
Changes of ejection fraction after hemodialysis were
significantly correlated with changes of circumferential
strain (r = -0.858, p < 0.001), longitudinal strain (r =
-0.516, p = 0.012) and LV area (r = -0.883, p < 0.001),
but not with those of radial strain, systolic BP, diastolic
BP, end-diastolic volume, or end-systolic volume (Figure 4). Change in ejection fraction was not correlated
with rotation, torsion or twist of LV.
The intraobserver variability for the LV torsion
measurement were 10 ± 6%, and the interobserver variability were 12 ± 8%.
Main findings
In this study, we evaluated the effect of acute preload reduction in uremic patients by newly developed
3D-STE. Hemodialysis produces acute change in intravascular volume status, and gives a good opportunity to
examine the changes of cardiac contractile characteristics in relation to acute volume loss. However, few reports demonstrated the changes of contractile parameters
of left ventricle in chronic dialysis patients.23,26 The significant decreases in end-diastolic volume and end systolic volume after dialysis were clearly demonstrated by
using 3D-STE in our study. The application of 3D-STE
in clinical practice is still developing. Our study demonstrated the benefits of 3D-STE in the evaluation and
quantification of the cardiac contractile function. Our
results could be a basis for future studies.
LV ejection fraction was significantly correlated
with systolic BP, diastolic BP, end-diastolic volume,
end-systolic volume, circumferential strain, longitudinal
29
Acta Cardiol Sin 2012;28:25-33
Bao-Tzung Wu et al.
A
B
C
D
Figure 4. The change in ejection fraction after dialysis was significantly correlated with changes in area of LV (A), circumferential strain (B), and
longitudinal strain (C), but not with change in radial strain (D).
to evaluate individual responses to hemodialysis and to
tailor appropriate dialysis therapy, especially in vulnerable patients suffering hypotension and fainting episodes.
Our results were consistent with Murata et a1’s report that peak systolic strain and ejection were not
changed before and after hemodialysis. 29 But the LV
functions in the horizontal plane, not only the radial
dyssynchrony but also the regional torsion, improved after dialysis.29 Weiner et al. revealed that the LV rotation
and torsion increased after normal saline infusion in normal subjects.30 We further demonstrated that in volume
overload uremic patients, decreased preload also increased LV torsion. The changes in LV torsion after
hemodialysis were substantial as evaluated by regional
torsion, but not by crude global torsion. The regional
torsion could be a better parameter to assess changes in
LV contractile property, because of the deformation
non-uniformity of myocardium.
strain, and LV area. In contrast, the changes in ejection
fraction after hemodialysis were correlated with the
changes in circumferential strain, longitudinal strain and
LV area, but not with systolic BP, diastolic BP, enddiastolic volume or end-systolic volume. Although
hemodialysis consistently produces acute reduction in
intravascular volume, the changes in ejection fraction,
strain and torsion of LV after dialysis were quite variable. The hemodialysis which induced changes in ejection fraction, systolic BP and diastolic BP among different patients were not only a result of intravascular
volume reduction, but might be affected by the co-existence of myocardial damage, intravascular volume status, and a function of the autonomic nervous system.
Chronic dialysis patients may have prominent myocardial interstitial fibrosis.27,28 Marked cardiac fibrosis may
alter myocardial contractile characteristics, and influence the results of speckle tracking analysis. Therefore,
our study did not show consistent changes in most echocardiographic parameters. The changes in cardiac performance after hemodialysis were difficult to judge by simple clinical rule in different patients. 3D-STE could help
Acta Cardiol Sin 2012;28:25-33
Previous studies by other imaging techniques
The regional LV torsion increased significantly after
hemodialysis in our patients. The increase in LV torsion
30
Effect of Preload Reduction on 3D Strain and Torsion
could result from decreases in afterload (blood pressure)
and preload (end-diastolic volume). The results of
changing afterload and preload on LV torsion were controversial in previous animal and human studies, which
used cine, MRI, microsonometry and 2D-STE testing
techniques.31-34 In a human cardiac allografts study, the
author used LV mid-wall metallic markers to measure
the rotation of LV. After volume loading with normal
saline (2000 cc), torsion angles between middle and
apex of LV wall did not increase significantly. But in an
animal study evaluated by cardiac MRI, LV torsion increased after volume loading. MacGowan et al. studied
the canine heart using MRI tagging, and LV torsion was
concluded to be afterload and preload dependent. 33
Hansen showed that pressure and volume loading do not
affect LV systolic twist or torsion in transplant patients
by using cine with titanium marker at the middle wall of
the heart.32
nique, we can calculate the strain directly related to fiber
orientation. The regional non-uniformity of myocardium, such as regional torsion in this study, could be
evaluated easily by 3D-STE, but not 2D echocardiography. In addition, circumferential rotation also contributes 3D wall deformation and affects tracking accuracy. The 3D-STE had the benefit of being less time
consuming, with fewer out of plane artifacts and limitations of the Doppler insonnation angle, compared with
2D-STE and 2D tissue Doppler.22 Discordant results between 3D-STE and 2D-STE in previous reports may be
explained by the fact that 3D-STE assesses the real motion of the myocardium in the certain three-dimensional
volume space, and current 2D-STE ignored the movement out of the ultrasound section plane.
The advantages of 3D-STE
3D echocardiography (3D-STE) has been applied to
assess traditional echocardiographic parameters such as
volume, mass, global and regional wall motion of LV.
The myocardial architecture of LV includes layers of
helical fibers running in different directions. 35,36 Left
ventricular motion is a complex process consisting of
rotation, contraction and shortening. Estimation of components of LV strain and strain rate by using 3D-STE
correlated well with those estimated by sonomicrometry
and cardiac magnetic resonance, and provided further
information about the kinetics of LV. 37,38 This study
used the newly developed 3D speckle tracking technique
to trace the speckle spatial motion of myocardium. By
calculation and reconstruction of the motion and deformation of the myocardial tissue, the 3D-STE could
achieve accurate qualitative and quantitative estimation
of motion velocity, strain, strain rate, displacement, and
twist and torsion. 21,22 Torsional motion has been measured by 2D ultrasound speckle tracking image both in
animals and humans.11,14,39 In the conventional 2D echocardiography, only the echo speckles in LV short axis
view was calculated for LV short axis strain or twist. The
longitudinal heart motion during cardiac cycle inevitably
causes out of plane error in 2D short axis imaging. But
in the real world, the muscle fibers were contractile in an
upright or downward oblique way. Using 3D strain tech-
There were some limitations of this study. Threedimensional echocardiography spatial resolution full
volume LV data set for 3D-STE comprised 6 sectors, so
the artifact occurring around the border between sectors
may affect speckle tracking quality. After hemodialysis,
LV volume may still be in fluctuation in these patients,
therefore, it is necessary to perform echocardiography at
the patients’ dry weight, preferably the day after dialysis
due to substantial variability over time in measurement
of LV volume and strain. Our study population was
small, and there were substantial differences in demographic characteristics among recruited patients.
LIMITATIONS
CONCLUSION
Assessment of LV contractile characteristics by
3D-STE is less laborious, and more time-saving than
2D-STE. The regional torsion is more sensitive to change,
as preload changed, than other parameters such as crude
global torsion, longitudinal, circumference and radial
strain. This could be due to unevenly distributed interstitial fibrosis in regional myocardium in uremic patients. The changes of 3D-STE parameters in chronic
dialysis patients might help the medical community to
better understand the physiological and biomechanical
alterations of cardiac contraction caused by hemodialysis.
31
Acta Cardiol Sin 2012;28:25-33
Bao-Tzung Wu et al.
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