The impact of preload on 3-dimensional deformation parameters: principal strain, twist and torsion
Ahn et al. Cardiovascular Ultrasound
The impact of preload on 3-dimensional deformation parameters: principal strain, twist and torsion
Hyo-Suk Ahn 0
Yong-Kyun Kim 1
Ho Chul Song 1
Euy Jin Choi 1
Gee-Hee Kim 0
Jung Sun Cho 0
Sang-Hyun Ihm 0
Hee-Yeol Kim 0
Chan Seok Park 0
Ho-Joong Youn 0
0 Divisions of Cardiology, College of Medicine, Catholic University of Korea , 222 Banpo-daero, Seocho-gu, Seoul 06591 , Republic of Korea
1 Nephrology, College of Medicine, Catholic University of Korea , Seoul , South Korea
Background: Strain analysis is feasible using three-dimensional (3D) echocardiography. This approach provides various parameters based on speckle tracking analysis from one full-volume image of the left ventricle; however, evidence for its volume independence is still lacking. Methods: Fifty-eight subjects who were examined by transthoracic echocardiography immediately before and after hemodialysis (HD) were enrolled. Real-time full-volume 3D echocardiographic images were acquired and analyzed using dedicated software. Two-dimensional (2D) longitudinal strain (LS) was also measured for comparison with 3D strain values. Results: Longitudinal (pre-HD: −24.57 ± 2.51, post-HD: −21.42 ± 2.15, P < 0.001); circumferential (pre-HD: −33. 35 ± 3.50, post-HD: −30.90 ± 3.22, P < 0.001); and radial strain (pre-HD: 46.47 ± 4.27, post-HD: 42.90 ± 3.61, P < 0. 001) values were significantly decreased after HD. The values of 3D principal strain (PS), a unique parameter of 3D images, were affected by acute preload changes (pre-HD: −38.10 ± 3.71, post-HD: −35.33 ± 3.22, P < 0.001). Twist and torsion values were decreased after HD (pre-HD: 17.69 ± 7.80, post-HD: 13.34 ± 6.92, P < 0.001; and pre-HD: 2.04 ± 0.86, post-HD:1.59 ± 0.80, respectively, P < 0.001). The 2D LS values correlated with the 3D LS and PS values. Conclusion: Various parameters representing left ventricular mechanics were easily acquired from 3D echocardiographic images; however, like conventional parameters, they were affected by acute preload changes. Therefore, strain values from 3D echocardiography should be interpreted with caution while considering the preload conditions of the patients.
Three-dimensional echocardiography; Myocardial strain; Hemodialysis
Two-dimensional (2D) echocardiography is the most
widely used examination method for left ventricular (LV)
dimension and function assessment, and the high frame
rate of 2D speckle tracking echocardiography (STE) allows
for the precise assessment of myocardial function through
the analysis of myocardial deformation. Longitudinal,
circumferential and radial movements, which represent
dynamic LV changes during a cardiac cycle, can be measured
from parasternal and apical echocardiographic windows.
However, assumptions about LV geometry were inevitably
the limitation of this method [
Real-time three-dimensional (3D) echocardiography
is better correlated with cardiac MRI than 2D
echocardiography in the measurement of LV volumes [
It is particularly useful for evaluating cardiac volumes
in patients with cardiomyopathies, whose hearts
possess more complex structures than the normal heart,
and allows for a more accurate measurement of LV
volume even in cases of geometrically asymmetric LV
]. Moreover, 3D echocardiography also
proved to be superior to 2D echocardiography when
evaluating cardiac valves . Studies other than
volume measurements can also be performed; for
example, Yodwut et al. showed the clinical efficacy of
3D echocardiography for the assessment of LV
diastolic function [
Recent studies have shown that 3D strain
measurements of the left ventricle using speckle tracking can
represent LV mechanical function and can be achieved
using several types of vendor-dependent and
independent software. Strain assessed by 3D STE can predict the
prognosis of patients who have suffered acute
myocardial infarction and heart failure [
]. It can be
measured even at frame rates as low as 18 frames/sec ,
and the rotational motion of the left ventricle can also
be reliably measured from 3D echocardiography [
Principal strain (PS) is a newly introduced parameter
in cardiology that can be obtained from 3D
echocardiography. This is accomplished by recognizing the direction
along which strain occurs (the so-called principal
direction) and the entities of actual deformation along the
principal direction. It characterizes 3D strain properties,
including longitudinal and circumferential strain values
as well as torsional shear deformation, and can therefore
represent dynamic 3D movements of the left ventricle
Longitudinal and circumferential strain calculated by
2D STE was demonstrated to be affected by acute
preload changes caused by normal saline infusion [
However, there are little data on the effects of preload
on the various parameters that can be acquired from 3D
STE, such as strain, twist and torsion. Moreover, it is not
known whether the newly introduced echocardiographic
parameter of PS is volume independent. Although twist
can be measured from 2D STE, it is greatly affected by
the position of the parasternal images [
3D STE is anticipated to be a useful tool for a more
accurate analysis of twist and torsion.
We hypothesized that various kinds of strain values
from 3D STE, including PS, twist and torsion, may be
influenced by acute volume change. We attempted to
test this in a group of patients with end-stage renal
disease (ESRD) who underwent periodic hemodialysis (HD)
and experienced a subsequent preload reduction.
Patients who were regularly undergoing HD at Bucheon
St. Mary’s Hospital in Bucheon, South Korea, were
recruited. All subjects were enrolled on a prospective
basis. Among the 98 patients who were regularly
undergoing HD on a periodic basis for at least 1 month prior
to enrollment in the institute, 63 patients volunteered.
An experienced echocardiographer who was blinded to
the study design performed screening echocardiography
on all volunteer subjects. Before and after the screening
echocardiography, the exclusion criteria were as follows:
(i) current acute coronary syndrome; (ii) previous
cardiac surgery or device implantation; (iii) current
presence or previous history of significant arrhythmia, such
as atrial fibrillation; (iv) LV ejection fraction less than
50%; (v) evidence of major valvular heart disease (i.e.,
any degree of mitral or aortic stenosis; more than a mild
degree of mitral, aortic, or tricuspid regurgitation; and
the presence of a prosthetic valve); and (vi) a poor
echocardiographic window that was not appropriate for
Five patients were excluded after the screening
echocardiography due to significant valve dysfunction
(n = 2), arrhythmia detected during echocardiographic
examination (n = 1), LV regional wall motion
abnormalities (n = 1) and a poor echocardiographic window
(n= 1); therefore, 58 subjects were finally enrolled in this
Transthoracic 2D and real-time 3D examinations were
carried out by an experienced echocardiographer who
was blinded to the study design while the patients were
in the left lateral decubitus position.
A commercially available ultrasound machine (Vivid
E9; General Electric Health Care, Milwaukee, WI)
equipped with phased array transducers (M5S-D and
4 V–D) was applied for echocardiographic examination.
Echocardiograms were performed immediately before
and less than 30 min after a single dialysis session.
From the M-mode measurements, LV dimension and
diastolic LV septal and posterior thickness were
determined in the parasternal long-axis view. The 2D data
were acquired from the parasternal long-axis and
shortaxis views and the three standard apical views. For each
view, three consecutive cardiac cycles were recorded
during quiet respiration. LV mass was determined using
the area–length method and was corrected for body
surface area. LV volume, ejection fraction and left atrial
volume were determined using the modified Simpson’s
method from apical 4- and 2-chamber views. Pulsed
Doppler echocardiography of transmitral velocities was
used to determine the peak E velocity, peak A velocity
and the ratio between peak E and A velocities (E/A
ratio). LV early diastolic e’ velocity and late diastolic a’
velocity were determined at the septal and lateral portion
of the mitral annulus by Doppler tissue imaging and
then averaged for evaluation. These measurements were
obtained by setting the sample volume at the septal and
lateral annulus and then recording at a sweep of
100 mm/s. All examinations were performed according
to the recommendations of the American Society of
Echocardiography and the European Association of
Cardiovascular Imaging [
During 3D imaging, to achieve a high frame rate and
the highest spatial resolution, the pyramidal scan volume
was focused on the LV volume and the data sets were
acquired during a single breath hold, taking care to
include the whole left ventricle.
2D and 3D speckle tracking analysis
2D and 3D images were kept in a proprietary format
(GE Healthcare, Milwaukee, WI) with Digital Imaging
and Communications in Medicine Wrapper. Images
were downloaded into a software package (EchoPAC
version 12.0; GE Healthcare, Milwaukee, WI) and then
exported into ImageArena Software (TomTec Imaging
Systems; Unterschleissheim, Germany) for analysis,
including 2D and 3D strain analyses. The 2D strain data
were used to validate the 3D strain data. For this
purpose, three apical B-mode sequences (2-, 3- and
Pre-HD (n = 58)
chamber views) were recorded at an optimal frame rate
(>30 frames/sec, also ensuring >30 frames/heartbeat)
and optimal resolution for myocardium while focusing
the image on the entire left ventricle; the images were
kept in the DICOM format for post-processing. LS was
assessed using the speckle tracking method at the
endocardial level with Cardiac Performance Analysis software
(Version 1.2, TomTec Imaging Systems;
Unterschleissheim, Germany). Global values were then calculated as
averages from the segments in each view.
Three-dimensional images were analyzed using
commercially available vendor-independent software (4D LV
analysis version 3.1; TomTec Imaging Systems;
Unterschleissheim, Germany). First, the LV long axis was
designated in the three apical views (four, three and two
chamber) by the operator. The software distinguished
the LV endocardial border and tracked it for an entire
cardiac cycle. Last, the curves of PS strain were
determined using the standard 16-segment model.
The reliability of the 3D measurements was estimated
by comparing the 3D global longitudinal strain (LS)
parameters with the corresponding parameter measured by
2D analysis from the relevant subjects. Correlations
between 3D global PS and 2D global LS were also
investigated. We also compared the differences in the 3D data
analyzed by vendor-independent (4D LV analysis version
3.1; TomTec Imaging Systems, Unterschleissheim,
Germany) and vendor-dependent (Echo PAC version
12.0; General Electric Health Care, Milwaukee, WI)
software. Area strain (AS; i.e., area change ratio) could not
be determined by vendor-independent software, and PS
could not be calculated by vendor-dependent software.
We directly compared only the values of 3D global
longitudinal, circumferential, and radial strain that were
acquired from the same 3D echocardiographic images
using two different 3D image analysis systems. We also
investigated the correlation between PS and AS.
To evaluate intra-observer variability in the offline
analysis, 20 patients were randomly selected and analyzed
by the same operator with at least a 1-week interval
between the two analyses. To assess the effect of
interobserver variability, the same 20 subjects were analyzed
in a random order at different times using the same
software by a second investigator who was blinded to the
results from the first investigator.
All data analyses were performed using the statistical
analysis software package R version 3.4.1 [
continuous variables were shown as the mean ± standard
deviation (SD). Differences in continuous variables
between the pre- and post-HD states were estimated using
the paired t-test. The x2 and Fisher’s exact tests were
applied to assess differences between categorical
variables. The correlations between 3D PS, 3D LS and 2D
LS were evaluated by Pearson’s correlation coefficient.
Linear regression analysis between the values of 2D and
3D strain was performed. The correlation between 3D
PA and AS was also evaluated by Pearson’s correlation
coefficient and linear regression analysis [
Reliability was evaluated using the intra-class
correlation coefficient (ICC) to determine both intra- and
inter-observer variability using an R package for the ICC
]. The inter-software variability was determined by
the ICC. The clinical significance of the ICC was
interpreted as follows: excellent, ICC ≥ 0.80; good,
0.60 ≤ ICC < 0.80; moderate, 0.40 ≤ ICC < 0.60; and
poor, ICC < 0.40. Bland-Altman analyses were also
performed. The R package BlandAltmanLeh was used
for this purpose [
]. P-values <0.05 were considered
3D STE analysis successfully performed in all 58
patients, but the measurement of LS from 2D STE could
not be performed due to poor image quality in one
patient pre-HD and two patients post-HD.
The clinical characteristics of the subjects are
summarized in Table 1. The mean ultrafiltration rate was
11.5 ± 4.6 mL/kg/h. The mean age of the subjects was
59 ± 12 years, and 50% of the participants were male
(n = 29). The most common cause of ESRD was diabetes
mellitus (n = 36, 62%), the second was hypertension
(n = 17, 29%), and the third was chronic
glomerulonephritis (n = 3, 5%) (Table 1).
Table 2 presents the changes in blood pressure and
heart rate after acute preload reduction caused by HD.
Systolic, diastolic and mean blood pressure were
significantly lowered after HD. The differences in heart rate
based on HD status were statistically insignificant.
Conventional echocardiographic parameters are
summarized in Table 3. Many echocardiographic parameters
that depict LV systolic and diastolic function were
changed after HD. The end-diastolic, end-systolic and stroke
volumes of the left ventricle were decreased after HD.
LV ejection fraction was also altered by preload
reduction. Diastolic parameters were evaluated by
pulsedwave Doppler, including the peak E wave velocity, E/A
ratio, E wave deceleration time and isovolumetric
relaxation time, which showed significantly different values
based on HD status. Left atrial volume index, peak early
diastolic tissue velocity (e’) and the ratio between peak
early diastolic mitral inflow velocity and peak early
diastolic tissue velocity (E/ e’) were also affected (Table 3).
Table 4 summarizes the LV volumes, strain, twist and
torsion measured by 3D STE. The frame rates were not
significantly different between pre- and post-HD
patients. All parameters were easily obtained from one 3D
LV full-volume image, and they were all affected by
acute preload reduction. The novel parameter 3D PS
was also changed after HD (pre-HD: −38.10 ± 3.71,
post-HD: −35.33 ± 3.22, P < 0.001). The values of twist
and torsion were decreased according to the preload
change caused by HD (pre-HD: 17.69 ± 7.80
postHD:13.34 ± 6.92, p < 0.001; pre-HD: 2.04 ± 0.86
postHD: 1.59 ± 0.80, respectively, P < 0.001) (Table 4, Figs. 1
Table 5 compares the volumetric parameters measured
by 2D and 3D echocardiography. End-diastolic and
endsystolic volumes calculated by 3D echocardiography
were significantly larger than those measured by 2D
echocardiography. Linear analyses showed that values of
2D global LS were correlated with those of 3D global PS
and LS (Fig. 3).
Table 6 shows that global LV strains in all directions
are significantly different when analyzed by different
analysis software although the same analyzer performed
the analysis using the same images, and the correlations
were weak or moderate. The correlation between PS and
AS was weak in the pre-HD group, but a better
correlation was observed in the post-HD group (Fig. 4).
Table 7 summarizes the ICCs of 3D STE strain for
intra- and inter-observer measurements. All
measurements were in excellent or good agreement, although
some inter-observer variations were present, with
relatively weak power. Bland-Altman plots for pre- and
post-HD PS are presented in Fig. 5.
2D speckle tracking is a useful method for cardiac
evaluation. It has been applied in cases of subclinical cardiac
dysfunction and for predicting prognosis. 2D
echocardiographic images at higher frame rates enable the
calculation of strain rate, and thus, it is possible to determine
subtle changes in cardiac performance using this
technique. However, at least six images should be obtained to
measure the global strain and twist values from 2D
echocardiography, and one type of strain cannot represent the
dynamic cardiac motion. 2D speckle tracking also has
limitations in measuring twist because its values are greatly
affected by the position of image planes [
Real-time 3D echocardiography was first introduced in
]. It has advantages for the measurement of LV
volume, with a better correlation with cardiac MRI and
fewer geometric assumption requirements. Consequently,
3D echocardiography has been suggested as a better
option to measure LV volumes in cases of cardiomyopathy
or aneurysmal changes that distort the geometry of the left
Recent advances in cardiovascular imaging techniques
have made it possible to measure values of various types
of strains from 3D echocardiographic images using the
speckle tracking method, which is already widely used
and has proven to have clinical importance in 2D
]. LV 3D strain was reported as a valuable
predictor for LV function improvement after myocardial
] and can be an effective noninvasive
method for assessing the twist motion of the left
ventricle, as it is less dependent on the position of the
image plane [
]. A trial to determine normal reference
values for real-time 3-dimensional STE has already been
ESRD patients who are regularly undergoing HD have
been used as a model for acute preload change in several
previous studies. These studies showed that LV and atrial
strain values were significantly decreased following
preload reduction by HD [
]. 3D echocardiography
was also applied on ESRD patients for the evaluation of
dynamic LV volume changes during HD , and it
showed feasibility for clinical application in this group of
PS analysis is a method for describing
multidimensional deformations. It identifies the directions along
which strain develops and the entity of actual
contractions, and therefore, it is particularly well suited for
biologic tissues with an underlying structure of muscular
fibers along which the stress is generated, such as the
]. In this study, we used vendor-independent
software that was previously applied by several
9, 26, 27
]. This software was designed to track the
CI confidence interval, 3D three-dimensional, STE speckle tracking
echocardiography, HD hemodialysis, GPS global principal strain, GLS global longitudinal
strain, GCS global circumferential strain, GRS global radial strain
real-time 3D and 4D endocardial motion of the left
ventricle. It provides the 3D PS value, which is unavailable
from 2D images, as well as the traditional longitudinal,
circumferential and radial strains.
Three-dimensional PS has proven to be effective in
detecting subclinical cardiac abnormalities [
]. AS is
also a novel parameter for 3D echocardiographic images,
but it only considers the longitudinal and
circumferential movement of the left ventricle and does not
represent the dynamic 3D motion of the left ventricle or have
a correlation with myocardial muscle direction . PS
can represent more complex movements of the left
ventricle because it considers not only longitudinal and
circumferential movement but also twist movement during
systole and diastole. It was also shown to correlate with
cardiac muscle fiber arrangements. Therefore, it is a
useful and novel parameter that can represent complex LV
movements during the cardiac cycle.
In this study, twist and torsion calculated using 3D
STE were also affected by acute preload changes. LV
rotation plays an important role in LV contraction and
relaxation. From 2D STE, the difference in the systolic
rotation of the myocardium in the apical and basal
short-axis planes is referred to as twist and reported in
degrees. Data normalized to the distance between the
respective image planes are referred to as torsion and
reported in degrees/cm [
]. Weiner et al. reported
that the rotational movement of the left ventricle
measured by 2D STE was affected by preload changes
caused by normal saline infusion [
]. However, the
measurement of twist using 2D STE requires two
apical and basal slices in two different cardiac cycles,
and the dependence on the position of two image
planes results in a less accurate analysis. The 3D STE
used in this study will be a promising tool for further
investigations of the rotational movement of the left
This study has several strong points compared to
other studies investigating changes in the
echocardiographic parameters based on preload changes [
First, we used newly developed novel strain values for
the evaluation of preload reduction. Other strain values,
which can be obtained from 2D STE, were also easily and
simultaneously calculated during the same cardiac cycle.
This benefit made it possible to measure various
parameters representing cardiac mechanics more accurately.
Second, the software used was newly introduced
vendor-independent software for 3D echocardiographic
image analysis. There are several types of software for
3D strain evaluation on the market, but they yield
different values in the measurement of 3D strain, even
within the same patients [
]. Our results also showed
significant vendor dependency even when the same 3D
images were analyzed. In the clinic, various types of
echocardiographic machines are used for patient care,
and 3D echocardiography is already recommended in
several guidelines for the evaluation of cardiac function,
such as during cancer therapy [
]. This limitation can
hamper the application of this technique in the clinical
setting. The software that we used in this study was
previously used by several investigators and has proven
efficacy in 3D echocardiographic image analyses among
various types of patients.
Third, 3D strain values could have been acquired
from all subjects even though we could not calculate
the LS value in 3 subjects due to poor
echocardiographic windows. For measurements of acceptable
strain values, good-quality real-time 3D
echocardiographic images are essential. In addition, a significant
learning curve is required even for experienced
physicians or echocardiographers.
However, there are also several weak points in this
study. The major limitation of this study is that it was
performed in a single center with a relatively small
number of patients, although the number of individuals
enrolled in this study was larger than that in other studies
13, 23, 24, 28
Second, this study only tracked the endocardium and
not the entire myocardium. Compared with the
epicardium, endocardial shape change is known to be more
associated with global shape change; epicardial,
endocardial or global volume; and global rotation and
global twist parameters [
Third, although the heart rate and frame rate were not
significantly different between the pre- and post-HD
phases, the relatively higher heart rate post-HD due to
acute volume reduction might have affected the frame
rate of the 3D echocardiographic images and ultimately
led to a greater decrease in all LV mechanical
parameters. The frame rates of both groups were greater than
25 frames/s in this study. Yodwut et al. previously
demonstrated that frame rates greater than 18 frames/s did
not affect the strain values [
]. The lower resolution of
the 3D echocardiogram may also influence the quality of
the strain analysis and principal strain analysis (PSA)
results. We attempted to mitigate this limitation by
performing multiple 3D tracking assessments and by
validating our data to 2D LS results. Although a previous
study reported significant differences in 2D and 3D
strain values [
], in this study the values of LS
measured by 3D STE were relatively well correlated with
both PS and 2D LS. Additionally, 2D STE measurements
were not possible in three patients whose 3D STE
measurements were available for 3D strain evaluation.
Fourth, HD is not a simple process that leads to only
acute volume reduction. During HD, activation of the
sympathetic nervous system occurs for the invitation
and maintenance of compensatory mechanisms to
maintain blood pressure, especially mechanisms involving
heart rate and peripheral vasoconstriction [
heart rate was not significantly different after HD, but
HD affected blood pressure in this study. The effects of
a decrease in blood pressure on the echocardiographic
parameters could not be excluded.
Fifth, a study that aimed to determine normal reference
values of 3D echocardiographic strain showed that there
were differences in normal values between different
segments, walls and levels of the left ventricle. There is still
no accepted reference value of 3D strain, and there are
significant inter-vendor differences in the measured values
]. We used vendor-independent software in this study
and compared only global strain values before and after
acute preload reduction in the same subjects; therefore,
this limitation could be overcome in this study.
This study showed that deformation parameters
measured from 3D echocardiographic images using the
speckle tracking method are affected by acute preload
changes. 3D echocardiography can be used to calculate
strain, twist and torsion, which can represent complex
LV mechanics, from a single image. However, all
parameters representing LV systolic function, including the
novel parameter of PS, were affected by acute preload
changes. Therefore, the values of strain, twist and
torsion acquired from 3D STE should be interpreted with
caution and with consideration of the preload status of
the patient. The findings of this study are important for
patients in critical settings, such as acute heart failure
and shock patients, who are experiencing significant
volume shifts due to the disease and the treatment. More
studies are needed to explore the prognostic value of PS,
a novel parameter that reflects actual deformation along
the principal direction, especially in ESRD patients who
are very susceptible to cardiovascular complications.
Availability of data and materials
All authors have full control of all primary data, and they agree to allow the
journal to review their data if requested. The datasets used and/or analyzed
during the current study are available from the corresponding author upon
HSA, MD: Data analysis, data interpretation and concept/design. YKK, MD,
PhD, HCS, MD, PhD, EJC, MD. PhD: Data collection. GHK, MD. PhD, JSC, MD.
PhD: Drafting of the article. SHI, MD, PhD, HYK, MD, PhD: Approval of the
article. CSP, MD. PhD: Concept/design, data collection, approval of the article
and statistical analysis. HJY, MD. PhD: Drafting of the article and approval of
the article. All authors read and approved the final manuscript.
Ethics approval and consent to participate
This study was approved by the Institutional Review Board of Bucheon St.
Mary’s Hospital and was in compliance with the Declaration of Helsinki.
Written consent was obtained from the subjects before performing the
Consent for publication
The authors declare that they have no competing interests.
Springer Nature remains neutral with regard to jurisdictional claims in
published maps and institutional affiliations.
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