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Effect of Age on Phasic Left Atrial Volume
Original Article
Acta Cardiol Sin 2012;28:34-41
Cardiac Imaging
Association between Normal Aging and Phasic
Left Atrial Volume as Assessed by Real-Time
Three-Dimensional Echocardiography
Wei-Wen Lin,1,2 Kuo-Yang Wang,1,3 Chi-Pin Lee,1 Taill-Lih Jou,5 Mei-Chun Chen,1,2
Chih-Tai Ting1,4 and Ying-Tsung Chen1,3,4,5
Background: Left atrial (LA) size is a good predictor of many cardiovascular outcomes, including atrial fibrillation,
stroke and heart failure. Real-time 3D echocardiography (RT3DE) may be a superior index for estimating LA
volume, compared with traditional M-mode and 2D methods. In this study, we used RT3DE to evaluate phasic LA
volumes and functions among different age groups of healthy Taiwanese subjects.
Methods: Sixty-eight healthy volunteers were divided into three groups according to age. Group 1: under 40 years
old (n = 20); group 2: 40-60 years old (n = 24); and group 3: over 60 years old (n = 24). RT3DE of LA volume was
acquired from the apical view. Three phasic LA volumes, including maximal LA volume (LAVmax), minimal LA
volume (LAVmin) and LA volume before atrial contraction (LAVpreA) were measured. These phasic LA volumes
were used to calculate the emptying volume and emptying fraction at different phases of one heart cycle.
Results: There were significantly positive correlations between age and LA volumes (r = 0.639 for LAVmax, r =
0.642 for LAVpreA, r = 0.661 for LAVmin; all p < 0.001). Total LA empty volume (p < 0.001) and active LA empty
volume (p = 0.001) also positively correlated with age. In contrast, total, passive and active LA emptying fractions
were not significantly different among the three age groups.
Conclusion: Aging has a significant effect on phasic LA volumes, but phasic LA empty fractions remain unchanged
in healthy Taiwanese adults.
Key Words:
Aging · Left atrial function · Phasic LA volume · Real-time 3D echocardiography
an important role in overall cardiac performance. 1 But
due to a paucity of proper non-invasive tools to evaluate
LA function within a three-dimensional structure, it has
not been well studied. Increased LA diameter and area
were related to many adverse cardiovascular outcomes,
such as atrial fibrillation (AF), stroke, and heart failure.2-4 Assessment of LA diameter and area by M-mode
and 2D echocardiography provides important physiologic and prognostic information in many different cardiovascular diseases. But LA area has a non-linear relationship to its volume. Morphology of LA may become
less spherical and more elongated during its remodeling.5,6 Measurement of LA area by 2D echocardiography
cannot actually reflect the true volume of LA, whereas
LA volume evaluated by RT3DE may be a superior in-
INTRODUCTION
It is well-known that left atrial (LA) function plays
Received: February 13, 2011
Accepted: June 28, 2011
1
Cardiovascular Center, Taichung Veterans General Hospital;
2
Department of Radiological Technology, Central Taiwan University
of Science and Technology; 3Department of Medicine, Chung-Shan
Medical University, Taichung; 4Cardiovascular Research Center,
National Yang Ming University School of Medicine, Taipei;
5
Department of Internal Medicine, Tungs’ Taichung MetroHarbor
Hospital, Taichung, Taiwan.
Address correspondence and reprint requests to: Dr. Ying-Tsung
Chen, Department of Internal Medicine, Tungs’ Taichung MetroHarbor
Hospital, No. 699, Chungchi Rd., Sec. 1, Wuchi Township, Taichung
County 435, Taiwan. Tel: 886-4-2658-1919; E-mail: ytchen@
livemail.tw
Acta Cardiol Sin 2012;28:34-41
34
Effect of Age on Phasic Left Atrial Volume
dex compared with other traditional methods.7-9 However, there are few studies in the literature on the relationship between changes in LA phasic volumes and cardiovascular outcomes. In this study, we used RT3DE
with speckle tracking to evaluate phasic LA volumes in
different age groups in a healthy Taiwanese population.
Aging is often associated with myocardial fibrosis, stiffness and ventricular diastolic dysfunction.10 Impaired
relaxation depresses the early diastolic mitral inflow
volume, and the LA active emptying volume increases to
maintain cardiac output.11 The compensatory changes of
LA mechanical function secondary to aging LV are not
well understood. The purpose of this study is to evaluate
phasic LA function in different age groups of a healthy
Taiwanese population. A better understanding of the different phases of LA volume in a cardiac cycle, and their
contribution to cardiac output in healthy and disease
hearts, may be of value in the development of future
therapeutic and diagnostic modalities.
for off-line speckle tracking analysis. Care was taken to
ensure that the entire LA was visualized, without any
dropout of the LA wall. In the parasternal long axis or
short axis view, M-mode of the LA and LV chamber
were measured for diameter and wall thickness. In the
apical 4-chamber view, mitral inflow was recorded at the
tip of the mitral leaflet. The peak velocities of early and
late diastolic filling waves (E-wave, A-wave) and the
E/A velocity ratio were measured. RT3DE datasets were
analyzed using the 3D wall motion tracking software
(Toshiba Medical Systems). In apical views (4-chamber
and 2-chamber), LA endocardial boundaries were manually measured at the end diastolic phase. Then, the 3D
endocardial surface was reconstructed and automatically
tracked throughout the cardiac cycle. (Figure 1).
Eight-one consecutive healthy volunteers without
any history of cardiovascular disease were recruited in
this study (including hospital employee and adult from
health examination center). Thirteen volunteers were excluded due to poor imaging quality of the LA after
RT3DE, and subjects with diabetes, hypertension or arrhythmia were also excluded. Subjects were divided into
three groups according to their age, as follows: group 1:
under 40 years old (n = 20); group 2: 40-60 years old (n
= 24); and group 3: over 60 years old (n = 24). The study
protocol was approved by the institutional review board
of the hospital, and written informed consent was obtained from all subjects prior to the study.
LA phasic volume measurement
Three basic volumes were measured 9 (Figure 1,
right): (a) maximal LA volume (LAVmax), at left ventricular (LV) end-systolic phase, just before mitral valve
opening; (b) pre-atrial contraction volume (LAVpreA),
before the P-wave on surface ECG; and (c) minimal LA
volume (LAVmin), at LV end-diastolic phase, just before
mitral valve closure. The LA volumes above were used
to estimate the emptying volume and emptying fraction:
LA empty volume (LAEV): LAVmax - LAVmin; LA
emptying fraction (LAEF): (LAEV/LAVmax) ´ 100%.
Four LA emptying parameters were derived: (a) LA passive empty volume: LAVmax - LAVpreA; (b) LA passive emptying fraction: (LAVmax - LAVpreA)/LAVmax
´ 100%; (c) LA active emptying volume: LAVpreA LAVmin; and (d) LA active emptying fraction: (LAVpreA
- LAVmin)/LAVpreA ´ 100%. LA expansion index was
calculated using the equation total LAEV/LAVmin ´
100%. All the LA volume data were corrected for body
surface area.
Echocardiographic studies
All patients were imaged in a left lateral decubitus
position using Artida ultrasound system equipment (Toshiba Medical Systems Co., Tochigi, Japan) with a 3
MHz/PST-25SX probe. RT3DE with speckle tracking
imaging was performed from the apical position by an
experienced technician. The average frame rate for analysis was 25-30 frames/s. Three consecutive cardiac
cycles during a single breath-hold were stored digitally
Intraobserver and interobserver variability
Intraobserver variability was determined by having
an observer repeat the LA volume (LAVmax, LAVmin,
and LAVpreA) measurements in 20 randomly selected
subjects. Interobserver variability was determined by
having an echocardiography specialist repeatedly measure these randomly selected subjects. Intraobserver and
interobserver variabilities were presented by BlandAltman plot.
METHODS
35
Acta Cardiol Sin 2012;28:34-41
Wei-Wen Lin et al.
A
B
C
D
E
Figure 1. (A) apical four-chamber strain and (B) two-chamber images via real-time 3D speckle tracking echocardiography. (C,D) Left atrium (LA)
3D reconstruction image in systolic and diastolic phase. (E) Left atrial volume (dash line, right y-axis) and displacement distance (solid line, left
y-axis). Maximum LA volume (LAVmax), pre atrial contraction volume (LAVpreA) and minimal LA volume (LAVmin) (white arrows).
Statistical analysis
Continuous data were expressed as median (minimum, maximum).
Comparisons among the three age groups were analyzed using the Kruskal-Wallis test. All 68 subjects
were put together as a group, and a simple linear regression test was used to evaluate the correlation between
phasic LA volume, stroke volume and age. A p value <
0.05 was considered statistically significant.
< 0.001). However, there were no significant differences
among the three age groups in the LV internal dimension
at end-diastolic and end-systolic (LVIDd, LVIDs) phases
and ejection fractions (EF). The mitral E/A ratios were
lower in groups 2 and 3 than in group 1 (p < 0.001), suggesting greater diastolic dysfunction with increased age.
Phasic LA volumes changes and correlations
among age groups
The three phasic LA volumes and calculated phasic
LA emptying fractions are shown in Table 2 and Figure
2. LAVmax, LAVpreA and LAVmin were increased significantly in groups 2 and 3 as compared with group 1 (p
< 0.05). Total and active LA empty volumes were
greater in group 3 than in groups 1 and 2 (p < 0.05). In
contrast to the increases in phasic LA volumes and
empty volumes with age, total, passive and active LA
emptying fractions were not significantly different among
the age groups.
Table 3 showed the correlations between age and
phasic LA volumes and functions. There were direct
RESULTS
Demographic and M-mode, 2D echocardiography
measurements
The demographic and routine echocardiography
measurement data are listed in Table 1. Aorta and LA
diameters were significantly higher in groups 2 and 3
compared with group 1 (p < 0.001). LV chamber thickness (including ventricular septum and posterior wall)
increased in groups 2 and 3 as compared with group 1 (p
Acta Cardiol Sin 2012;28:34-41
36
Effect of Age on Phasic Left Atrial Volume
Table 1. Basic demographic data
Age (y/o)
Sex (M/F)
SBP (mmHg)
DBP (mmHg)
HR (beat/min)
BSA (M2)
AO (mm)
LA (mm)
IVSd (mm)
LVIDd (mm)
PWd (mm)
LVIDs (mm)
PA (mm)
peak E (cm/sec)
peak A (cm/sec)
E/A ratio
EF (%)
Mean ± SD
d
p < 0.05 vs. 20-40 y/o
k
Kruskal-Wallis Test
20-40 y/o (n = 20)
40-60 y/o (n = 24)
> 60 y/o (n = 24)
p-value k
29.83 ± 7.010
12/8
.119 ± 11.4
71.2 ± 12.6
73.4 ± 14.5
1.51 ± 0.23
30.25 ± 2.950
31.71 ± 4.110
9.33 ± 1.52
45.88 ± 5.890
9.04 ± 1.30
29.25 ± 6.210
21.92 ± 3.540
80.17 ± 9.400
58.04 ± 13.20
1.47 ± 0.46
63.67 ± 3.800
49.21 ± 6.470
14/10
.120 ± 12.2
72.6 ± 10.8
71.3 ± 12.0
1.48 ± 0.32
d
34.04 ± 5.10d0
d
37.13 ± 5.33d0
d
12.13 ± 2.11d0
44.50 ± 5.540
d
11.42 ± 2.26d0
27.00 ± 4.670
d
24.25 ± 4.13d0
d
63.71 ± 14.73d
d
76.46 ± 12.42d
d
0.85 ± 0.21d
61.75 ± 4.200
68.15 ± 4.530
13/11
122.3 ± 17.60
76.4 ± 17.9
070.6 ± 14.33
1.55 ± 0.22
d
34.85 ± 4.02d0
d
37.55 ± 6.04d0
d
12.50 ± 1.57d0
45.70 ± 5.250
d
12.25 ± 1.68d0
25.15 ± 4.650
d
25.55 ± 4.55d0
d
63.60 ± 9.38d0
d
0 80.00 ± 16.27d0
0d0.83 ± 0.21d0
62.35 ± 4.120
NS
NS
NS
NS
< 0.0001
< 0.0001
< 0.0001
NS
< 0.0001
NS
< 0.0150
< 0.0001
< 0.0001
< 0.0001
NS
Values are means ± SD, *p < 0.05 was considered significant. AO, aorta; LA, left atrium; IVSd, interventricular septum in diastole;
LVIDd, left ventricular internal diameter in diastole; PWd, posterior wall in diastole; LVIDs, left ventricular internal diameter in
systole; PA, pulmonary artery; LVEF, left ventricular ejection fraction; BSA, body surface area.
Table 2. Phasic LA volume data
Max LA volume (ml)
Minimal LA volume (ml)
Per A volume (ml)
Max LA volume (ml/M2)
Minimal LA volume (ml/M2)
Per A volume (ml/M2)
Total LA SV (MaxV-MinV) (ml/M2)
Passive LA SV (MaxV- preA) (ml/M2)
Active LA SV (preA-Min A) (ml/M2)
Total LA EF (LASV/MaxV) ´ 100%
Active LA EF (active LASV/preA V) ´ 100%
Passive LA EF (passive LA SV/MaxV) ´ 100%
LA expansion index (total LA SV/MinV) ´ 100%
k
Kruskal-Wallis Test
d
p < 0.05 vs. < 40 y/o
y
p < 0.05 vs. 40-60 y/o
< 40 y/o (n = 20)
40-60 y/o (n = 24)
> 60 y/o (n = 24)
p-value k
36.71 ± 9.62
15.10 ± 4.32
23.82 ± 7.49
23.96 ± 5.51
10.00 ± 2.61
15.76 ± 4.52
13.96 ± 3.43
08.20 ± 2.79
05.76 ± 2.62
00.58 ± 0.06
00.36 ± 0.10
00.35 ± 0.09
01.44 ± 0.36
041.53 ± 10.00
18.21 ± 4.24
28.55 ± 7.09
d
28.67 ± 7.59d
d
12.55 ± 3.12d
d
19.70 ± 5.30d
16.12 ± 4.88
08.97 ± 3.95
07.14 ± 2.99
00.56 ± 0.04
00.36 ± 0.08
00.31 ± 0.09
01.29 ± 0.23
052.01 ± 12.58
23.31 ± 5.52
36.47 ± 8.55
dy
33.85 ± 8.56dy
dy
15.14 ± 3.65dy
dy
23.71 ± 5.72dy
d
18.71 ± 5.46d
10.14 ± 4.49
0d8.56 ± 3.18d
00.55 ± 0.05
00.35 ± 0.10
00.29 ± 0.10
01.24 ± 0.26
< 0.0001
< 0.0001
< 0.0001
< 0.0001
< 0.0001
< 0.0001
< 0.0060
< 0.1390
< 0.0030
< 0.0960
< 0.9920
< 0.1960
< 0.0960
Values are means ± SD, *p < 0.05 was considered significant. LA, left atrium; SV, stroke volume; EF, ejection fraction.
37
Acta Cardiol Sin 2012;28:34-41
Wei-Wen Lin et al.
A
B
C
D
Figure 2. Phasic left atrial volume and stroke volume in different age groups. LAVmax: LA volume maximum; LAVpreA: LA volume pre atrial
contraction; LAVmin: LA volume minimum; LASV: LA stroke volume.
sive LA empty volumes (correlation coefficient = 0.384,
p = 0.006).
Table 3. Correlations of age with phasic left atrial volume and
stroke volume
age
LA diameter (mm)
LAVmax (ml/M2)
LAVmin (ml/M2)
LAVpreA (ml/M2)
Total LAEV (ml/M2)
Passive LAEV (ml/M2)
Active LAEV (ml/M2)
Correlation coefficient
p-value
Correlation coefficient
p-value
Correlation coefficient
p-value
Correlation coefficient
p-value
Correlation coefficient
p-value
Correlation coefficient
p-value
Correlation coefficient
p-value
Observer variabilities
Intra- and inter-observer variability was present by
Bland-Altman analysis (Table 4).
0.532
< 0.001 <
0.639
< 0.001 <
0.661
< 0.001 <
0.642
< 0.001 <
0.559
< 0.001 <
0.327
0.006
0.452
< 0.001 <
DISCUSSION
In people without cardiovascular disease, LA diameter
and area continue to increase from childhood to old age.2,3
However, to the best of the authors’ knowledge, there are
no data on the effect of age on phasic LA volume among
healthy Taiwanese. Our study demonstrates that phasic
LA volumes, including LAVmax, LAVpreA and LAVmin,
increased with age in a clear linear fashion, and showed
good correlations (Tables 2 and 3). Total and active LA
empty volumes were also age-dependently higher in the
older age groups, but the passive LA empty volumes did
not correlate with age. Furthermore, LA total, active and
passive emptying fraction were not significantly different
among the three age groups. The results indicate that
LAV, left atrial volume; LAEV, left atrial empty volume.
positive correlations between LA diameter, phasic LA
volumes (including LAVmax, LAVpreA and LAVmin)
and age (p < 0.001). Moreover, age correlated well with
total and active LA empty volumes (p < 0.001), though
only a weak correlation was found between age and pasActa Cardiol Sin 2012;28:34-41
38
Effect of Age on Phasic Left Atrial Volume
Table 4. Bland-Altman analysis for intra-observer and inter-observer variability
Mean difference
Max LA volume (ml)
Minimal LA volume (ml)
Pre A volume (ml)
intra-observer
inter-observer
intra-observer
inter-observer
intra-observer
inter-observer
1.36
2.35
0.69
-0.181.28
0.34
95% C.I. of the Difference
0.55
1.26
0.12
-0.930.65
-0.51-
2.16
3.43
1.26
0.57
1.91
1.18
p
0.002
0.000
0.019
0.622
0.000
0.417
although LA volume increases as age increases, LA systolic function may remain unchanged in healthy adults.
which suggest that both LA diameter and phasic LA
volumes increase with age (Table 3, Figure 2).
Effect of age on phasic LA volume and
mechanical function
LA volume may be considered as a barometer of LV
diastolic pressure. 12 Age increases ventricular myocardium fibrosis and stiffness, which leads to an increase
in LV filling pressure.10 In the early LV diastolic phase,
LA is exposed to the pressure of left ventricle just after
the mitral valve opens, and the maximal or reserved LA
volume may be related to the early LV filling pressure.
As age increases, the increased LV filling pressure leads
to greater reserved and pre-atrial contraction LA volumes. Consequently, the minimal LA volume may be related to the elevated end-diastolic pressure.13
In this study, age was significantly correlated with
increased phasic LA volumes (Tables 2 and 3). The total
and active LA empty volumes increase to provide adequate LV filling volume (Table 2). The passive LA
empty volume (at conduit phase) is influenced by LV
myocardium diastolic velocity and compliance, and is
less influenced by the atrial function itself. But the
dilated LA still functions as described by the FrankStarling mechanism12,13 and there is a normal emptying
fraction (Table 2).
Thomas et al.14 reported that LA diameter, LAVmax
and LAVmin volume were not changed in normal age
subjects. LA size increase is a pre-clinical pathology
condition, but is not a part of normal aging. The results
were in conflict with previous studies that atrial size increased with aging.2-4,15 The authors suggested that this
difference may be attributed to the fact that they estimated LA volumes by using biplane methods of discs
and 3D reconstruction from 2D images, without using
M-mode methods. By using RT3DE, our observations
were consistent with most of the recent studies,15,23-25
Phasic LA volumes and function in different
cardiovascular diseases
Associations between changes in phasic LA volumes
and function with different cardiovascular diseases have
been demonstrated in a recent report by Stefanadis et
al. 16 In patients with hypertrophic cardiomyopathy, 17
LAVmax, LAVmin and LAVpreA were increased, but
total, active and passive LA ejection were decreased.
Changes in LA function may be secondary to LV myocardial fibrosis and diastolic dysfunction in these patients. In patients who suffered myocardial infarction
with non-ST elevation, there were progressive increases
in LAVmax and LAVmin, with decreased active and passive LA empty volumes.18
Phasic LA volume assessed by RT3DE and its
clinical implication
For years, M-mode and 2D echocardiography have
been used to measure LA size, with good clinical implications in many diseases, including atrial fibrillation and
heart failure. 19,20 They generally remain the standard
procedure in daily practice. RT3DE is a relatively new
ultrasound technique, with little information to prove its
incremental clinical implications at the present time.
However, by using more sophisticated echocardiographic tools in the future, such as the 3D measurement
of strain, strain rate and torsion, the use of RT3DE may
provide more substantial information about phasic LA
volumes, and thus increase its value as a clinical instrument to practitioners.
Study limitations
There were some limitations of this study. First, in
our study, LV wall thickness increased in the old age
39
Acta Cardiol Sin 2012;28:34-41
Wei-Wen Lin et al.
4. Gardin JM, McClelland R, Kitzman D, et al. M-mode echocardiographic predictors of six- to seven-year incidence of coronary heart disease, stroke, congestive heart failure, and mortality
in an elderly cohort (the cardiovascular health study). Am J
Cardiol 2001;87:1051-7.
5. Tsang T, Barnes M, Gersh B, et al. Left atrial volume as a
morphophysiologic expression of left ventricular diastolic dysfunction and relation to cardiovascular risk burden. Am J Cardiol
2002;90:1284-9.
6. Tsang T, Abhayaratna W, Barnes M, et al. Prediction of cardiovascular outcomes with left atrial size: is volume superior to area
or diameter? J Am Coll Cardiol 2006;47:1018-23.
7. Shin MS, Fukuda S, Song JM, et al. Relationship between left
atrial and left ventricular function in hypertrophic cardiomyopathy: a real-time 3-dimensional echocardiographic study. J Am
Soc Echocardiogr 2006;19:796-801.
8. Gottdiener JS, Kitzman DW, Aurigemma GP, et al. Left atrial
volume, geometry, and function in systolic and diastolic heart
failure of persons over 65 years of age (the cardiovascular health
study). Am J Cardiol 2006;97:83-9.
9. Anwar AM, Soliman OI, Geleijnse ML, et al. Assessment of left
atrial volume and function by real-time three-dimensional echocardiography. Int J Cardiol 2008;123:155-61.
10. Terman A, Brunk UT. The aging myocardium: roles of mitochondrial damage and lysosomal degradation. Heart Lung Circ
2005;14:107-14.
11. Daneshvar D, Wei J, Tolstrup K, et al. Diastolic dysfunction: improved understanding using emerging imaging techniques. Am
Heart J 2010;160:394-404.
12. Stefanadis C, Dernellis J, Stratos C, et al. Assessment of left atrial
pressure-area relation in humans by means of retrograde left atrial
catheterization and echocardiographic automatic boundary detection: effects of dobutamine. J Am Coll Cardiol 1998;31:426-36.
13. Anwar AM, Geleijnse ML, Soliman OI, et al. Left atrial FrankStarling law assessed by real-time, three-dimensional echocardiographic left atrial volume changes. Heart 2007;93:1393-7.
14. Thomas L, Levett K, Boyd A, et al. Compensatory changes in
atrial volumes with normal aging: is atrial enlargement inevitable? J Am Coll Cardiol 2002;40:1630-5.
15. Pan NH, Tsao HM, Chang NC, et al. Aging dilates atrium and
pulmonary veins: implications for the genesis of atrial fibrillation. Chest 2008;133:190-6.
16. Stefanadis C, Dernellis J, Toutouzas P. A clinical appraisal of left
atrial function. Eur Heart J 2001;22:22-36.
17. Eshoo S, Semsarian C, Ross DL, et al. Left atrial phasic volumes
are modulated by the type rather than the extent of left ventricular
hypertrophy. J Am Soc Echocardiogr 2010;23:538-44.
18. Boyd AC, Ng AC, Tran da T, et al. Left atrial enlargement and
phasic function in patients following non-ST elevation myocardial infarction. J Am Soc Echocardiogr 2010;23:1251-8.
19. Psaty BM, Manolio TA, Kuller LH, et al. Incidence of and risk
factors for atrial fibrillation in older adults. Circulation 1997;
96:2455-61.
group. In the previous studies by others, LV mass increased as age increased.21,22 We cannot separate the effects of LV mass on LA size. Second, we did not evaluate backward flow in pulmonary veins, due to poor temporal and spatial resolution in RT3DE. LV diastolic
function has been shown to be impaired as age increases.
The active LAEV increase in our study may not totally
increase during LV preload, and the pulmonary veins
backward flow may also increase during atrial contraction. Third, due to a low frame rate (20-30 frames/s),
some LA volume measurement were not entirely in the
images before the p wave on the electrocardiogram. In
some patients, we manually identified and measured the
LA volumes closest to the pre-A point.
CONCLUSION
Phasic LA volumes were significantly and dosedependently associated with increased age in healthy
Taiwanese adults, but phasic LA emptying fractions did
not differ among the three age groups. These results
carry important clinical and prognostic implications.
Monitoring phasic LA volumes by real-time 3D echocardiography in healthy subjects, and for evaluation of
different cardiovascular diseases in Taiwan, may be of
considerable value in clinical practice and have an important public health impact.
ACKNOWLEDGMENT
This work was supported by the research grant
TCVGH-993103B from the Taichung Veterans General
Hospital, Taiwan, Republic of China.
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