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Articles in PresS. Am J Physiol Heart Circ Physiol (June 17, 2004). 10.1152/ajpheart.00103.2004
The contribution of mitral annular excursion and shape dynamics to
total left ventricular volume change
Carlhäll C1,3, Wigström L1,3, Heiberg E1,3, Karlsson M2,3, Bolger A4, Nylander E1,3
Departments of Medicine and Care/Clinical Physiology1 and Biomedical Engineering2 and Center for Medical
Image Science and Visualization3, Linköping University, Sweden
Department of Medicine/Cardiology4, University of California, San Francisco, CA, USA
Running head: Mitral annular dynamics and total LV volume change
Correspondence to:
Carljohan Carlhäll
Department of Medicine and Care, Clinical Physiology,
University Hospital
SE 581 85 Linköping, Sweden
Ph: + 46 13 22 33 77
Fax: + 46 13 14 59 49
E-mail: [email protected]
Copyright © 2004 by the American Physiological Society.
1
Abstract
The mitral annulus (MA) has a complex shape and motion, and its excursion has been
correlated to left ventricular (LV) function. During the cardiac cycle the annulus´ excursion
encompasses a volume that is part of the total LV volume change during both filling and
emptying. Our objective was to evaluate the contribution of MA excursion and shape variation
to total LV volume change. Nine healthy subjects aged 56±11 (mean±SD) years underwent
transesophageal echocardiography (TEE). The MA was outlined in all time frames and a 4D
Fourier series was fitted to the MA coordinates (3D+time) and divided into segments. The
annular excursion volume (AEV) was calculated based on the temporally integrated product of
the segments´ area and their incremental excursion. The 3D LV volumes were calculated by
tracing the endocardial border in 6 coaxial planes. The AEV (10±2 ml) represented 19±3% of
the total LV stroke volume (52±12 ml). The AEV correlated strongly with LV stroke volume
(r = 0.73, p<0.05). Peak MA area occurred during mid-diastole and 91±7% of reduction in
area from peak to minimum occurred before the onset of LV systole. The excursion of the MA
accounts for an important portion of the total LV filling and emptying in humans. These data
suggest an atriogenic influence on MA physiology, and also a sphincter-like action of the MA
that may facilitate ventricular filling and aid competent valve closure. This 4-dimensional TEE
method is the first to allow non-invasive measurement of AEV, and may be used to investigate
the impact of physiological and pathological conditions on this important aspect of LV
performance.
Keywords: annular physiology; ventricular long-axis function; echocardiography; 3dimensional; 4-dimensional
2
INTRODUCTION
The mitral annulus (MA) is a discontinuous fibrous ring and an essential component of the
mitral valve/left atrial/left ventricular complex. It contributes to efficient valve closure as well
as unimpeded left ventricular (LV) filling (14, 19, 26, 29). Many studies support the concept
that the motion of the MA is dynamic throughout the cardiac cycle, yet the timing and extent
of annular motion and shape variation remain incompletely understood (26, 29). Assessment
of the MA physiology has been important to the understanding of disorders of the mitral valve
apparatus and left ventricular dysfunction. The mechanisms of functional valve regurgitation
in the setting of dilated cardiomyopathy and in the design of annuloplasty ring prostheses for
valve repair (15, 24, 28) are two of many areas where MA physiology is a key issue.
Mitral annular excursion is a well established diagnostic tool, which correlates with both
systolic and diastolic function of the left ventricle (2, 8). The translation of the annulus reflects
the contribution of the longitudinally oriented myocardial fibers, which have been shown to be
important in generating the LV stroke volume (8, 11, 22). The annulus´ excursion during the
cardiac cycle encompasses a volume that is part of the total volume change that occurs with
both ventricular filling and emptying. The amount that mitral annular excursion contributes to
the total left ventricular volume change is an important aspect of basic hemodynamics of the
LV, as shown by invasive animal studies using fluoroscopy of radiopaque markers implanted
in the myocardium (23).
Three-dimensional (3D) echocardiography is an important achievement in cardiac imaging (4,
13, 15). In this study 4-dimensional (4D) transesophageal echocardiography (TEE) with high-
3
resolution acquisition and digitally stored data allows the annular excursion volume (AEV) to
be assessed non-invasively in humans for the first time.
The aims of the present study were to non-invasively evaluate the variation in the shape of the
mitral annulus during the cardiac cycle as well as the contribution of mitral annular excursion
to the total left ventricular volume change, in order to reach a deeper understanding of the
basic physiology of the mitral annulus.
METHODS
Subjects
Transesophageal echocardiography was performed in 10 patients without cardiac disease
undergoing either non-cardiac surgery (n=7), or search for the source of cerebral embolism
(n=3). The criteria for enrollment were: age 20-75 years, no history of current or prior heart
disease or hypertension, absence of cardiac medications, a normal physical examination, a
resting heart rate between 50-100 bpm and a normal electrocardiogram. Nontrivial valve
insufficiency and LV systolic dysfunction were ruled out by echocardiography. The final
study population (table 1) was composed of 9 subjects (4 women/5 men) aged 56±11
(mean±SD) of whom 6 were studied during general anesthesia. One patient was excluded due
to a heart rate > 100 bpm during image acquisition. The local ethical committee approved the
research protocol, and informed consent was obtained from each patient.
Intraoperative Image Acquisition
After induction of general anesthesia and endotracheal intubation in the operative patients
(n=6), or after mild sedation in the ambulatory patients (n=3), a 5 MHz TEE multiplane probe
4
(GE Vingmed Ultrasound) was positioned in the esophagus behind the left atrium, making the
axis of rotation pass near the center of the mitral orifice, and with the 2D sector in a
lateral/septal starting position (0°). By means of a specific 3D acquisition mode (Vivid Five,
GE Vingmed Ultrasound) a trial rotation was initiated to verify that the MA could be
visualized in all rotation angles from 0° to 180°. During temporary cessation of mechanical
ventilation (n=6), or during shallow breathing (n=3), images were automatically acquired with
electrocardiography-triggering during a total of 30 cardiac cycles at 6° increments between
every cycle, and with a frame rate of 36 frames/second. Each scan was performed in less than
30 seconds and 1-3 loops per patient were acquired. Care was taken to ensure that no probe
movement occurred during the scans by holding the probe firmly at the bite guard.
Data Processing and Analysis
The digital image data from the echocardiography scanner were directly transferred to a Unixbased workstation for processing. Quantitative and qualitative analysis of the data-loop with
the best image quality were performed for each subject by means of a custom made software
routine written in Matlab 6.5 (Mathworks, Natick, MA, USA). The MA was defined as the
hinge points where the mitral leaflets met the endocardium on the atrial side; the annulus was
manually outlined in all frames.
In order to obtain a 4D (3D+time) description of the MA, the coordinates (x,y,z and time) for
every marked point along the annulus were extracted from the acquired data. Based on the
coordinates within the image plane and the known rotation angle for the specific image, the
global spatial coordinates (x,y,z) could be calculated. The timing with respect to the cardiac
cycle for each acquired image was estimated by analyzing the electrocardiogram data stored
5
with the image data. Each point was then described based on its rotation angle, ω, and phase in
the cardiac cycle, t. Both the angle and timing are periodic, and hence a Fourier series could be
used to describe each coordinate (x,y and z) based on ω and t. The number of terms used in the
Fourier series controls the spatio-temporal smoothing of the coordinate data. With a small
number of Fourier terms a smoothed representation of the annulus was obtained, while a larger
number permitted a more irregular shape to be generated. The optimal choice of Fourier terms
was therefore dependent on the degree of smoothing desired to compensate for inaccurately
positioned points. We chose the number of Fourier terms to be equal to 5 in the angle
dimension and 7 in the temporal dimension, in order to achieve a physiologically realistic
shape and longitudinal motion of the MA.
Based on the obtained Fourier series, the MA was analyzed at 100 time steps during the cardiac
cycle. In each time frame, the annular shape was divided into 72 triangular segments,
originating from the center of the MA (Fig. 1A).
The annular 3-D area was computed by summing the areas of the different segments.
Annular excursion volume was calculated by temporally integrating the sum of the volume
change of all the 72 segments. The volume change for one segment was calculated as the
product of the segment’s area and its incremental excursion at the periphery between
consecutive time frames (Fig. 1A,B).
The MA shape variation was described by the interpeak and intervalley distance ratio.
Interpeak (IP) distance was measured between the 2 points, on opposite sides of the MA, that
are most elevated toward the atrium. Intervalley (IV) distance was defined as the distance
between the 2 most apical points, on opposite sides of the MA (13) (Fig. 2).
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The annular excursion was determined as the distance between the annulus and the epicardial
apex. The total excursion amplitude was measured as the difference between the two most
extreme annular positions over the cardiac cycle (nearest and farthest away from the apex).
This excursion was measured at the four standard sites along the MA (lateral, anterior, septal
and posterior) (10).
The agreement between the Fourier-term description of the MA and the individually marked
points was verified by exporting the coordinates to a visualization software (Ensight 7.4, CEI
Inc., Apex, NC, USA). The accuracy of the measurements was also validated in vitro by
imaging a phantom immersed in a water bath and comparing its measured size with its true
dimensions. This demonstrated a mean error in size of less than 3%.
The 3-dimensional left ventricular volumes were calculated by tracing the endocardial border
in 6 coaxial long axis planes at 10 different time frames, 3 in systole and 7 in diastole.
(Echopac-3D, GE Vingmed Ultrasound) (21).
The onset of systole was assigned to the first frame in which mitral valve closure could be
seen and the onset of diastole was noted to be the time frame coinciding with mitral valve
opening (5). With this definition, systole represented 53±6% of the cardiac cycle length in the
studied population. Due to differing individual heart rates, cycle lengths were normalized by
linear interpolation into 100 parts. Systole and diastole were then normalized separately for
each individual data set, so that systole always represented 53%, and diastole 47% of the
cardiac cycle (13).
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The impact of respiratory motion was minimal in these experimental conditions. Only three
subjects were acquired during non-apnea, and these were sedated and thus had shallow
breathing. By means of a respiratory-gated function in the analysis software, extreme
respiratory positions could be included or excluded. Since shallow breathing was confirmed in
all cases, no time-frames had to be excluded from the acquired image sequences.
Statistical Analysis
Data are presented as mean±SD unless otherwise stated. One-way analysis of variance was
used to assess differences in annular excursion. Paired student´s T-test was used to assess
differences in MA shape during the cardiac cycle. Pearson´s correlation coefficient was used
to assess linear correlations between different variables. Inter- and intraobserver variabilities
in tracing the MA were assessed for annular excursion amplitude (12 observations) and area
(12 observations) in 3 randomly selected subjects. Two-way analysis of variance showed no
significant difference between observations for annular excursion amplitude (p>0.05 for both
inter and intravariability) or area (p>0.05 for both inter and intravariability). Statistical
significance was set at p<0.05.
RESULTS
Mitral Annular Excursion Volume
The magnitude of the mitral annular excursion volume was 10±2 ml and this represented
19±3% of the total left ventricular volume change (52±12 ml) in our study population (Fig.
3A-C).
The timing of the annular excursion volume and the left ventricular volume changes during
the cardiac cycle, both demonstrated similar contributions from early (E) and late (A) diastolic
8
mitral valve inflows (Fig. 3A-C).
The annular excursion volume correlated strongly with left ventricular stroke volume (p<0.05)
and body size (p<0.05 ) but not with left ventricular ejection fraction (n.s.) or heart rate (n.s.)
(Table 2).
Mitral Annular Shape Variation
The MA area increased from mitral valve opening to a peak value of 9.9±1.8 cm2 at the time
of onset of atrial contraction. The area then decreased to its minimum value of 9.0±1.5 cm2
which was reached shortly after mitral valve closure. The area increased again during early
systole (Fig. 4). 91±7% of the reduction from maximal to minimum area occurred before LV
systole (Fig. 4).
Non-planarity of the MA was present throughout the cardiac cycle. There was a consistent
pattern of elevation (peak) of the anteroseptal and posterolateral segments of the annulus
toward the atrium and of a complementary depression (valley) of the posteroseptal and
anterolateral segments toward the LV (Fig. 2).
Concordant increases in both the interpeak (IP) and intervalley (IV) distances were observed
starting after mitral valve opening, reaching a peak value of 3.3±0.2 and 3.5±0.5 cm,
respectively, with the onset of atrial contraction. Both subsequently began to decrease. In early
systole interpeak distance increased, while in contrast the intervalley decreased (Fig. 5A).
The shape of the MA was relatively constant during most of diastole. It began to change shape
with the onset of atrial contraction, and reached its most elliptical state shortly after mitral
valve closure. During this “presystolic” period, the IP/IV ratio fell from 0.94±0.15 to
0.89±0.16 (p<0.05 ). This was followed by an opposite shape change, resulting in the MA
reaching its most circular configuration during mid-systole (Fig. 5B).
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The total annular excursion showed no significant differences in amplitude between the 4
standard points around MA (Table 3).
DISCUSSION
Mitral Annular Excursion Volume
The current study demonstrates for the first time that the mitral annular excursion volume in
humans accounts for an important portion of the total left ventricular volume change. The
timing of these volume changes during the cardiac cycle seems to be synchronous and
demonstrates similar contributions from E and A mitral valve inflows. These findings
emphasize that the annular excursion is an important component of the LV filling and
emptying. They are concordant with previous estimates from invasive animal studies;
Tibayan, et al., demonstrated that the annular excursion volume accounted for one fourth of
the total left ventricular filling in ovine hearts (23).
It is well known that the longitudinally oriented myocardial fibers make important
contributions to the normal LV stroke volume and ejection fraction (8, 11, 22). Without the
longitudinal component, normal sarcomere shortening would lead to a shortening fraction of
approximately 12 % and an EF of < 30% (8, 11). Longitudinal shortening also contributes to
radial shortening because myocardial tissue volume is non-compressible and therefore
constant during contraction, and therefore as the outer diameter is almost unchanged, the
radial inner diameter must decrease (9, 22).
The contribution of the ventricular long-axis motion to the total LV volume change was 19%
in the present study, but this can be anticipated to be an underestimation of the true functional
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contribution during the cardiac cycle. This is because the calculation of the annular excursion
volume does not consider the contribution from the radial inner diameter reduction of the LV,
nor the fact that the area of the LV base is slightly larger than the MA area during the systolic
descent toward the apex.
The AEV change and its relation to the LV volume change may serve as a tool for
investigating the impact of different physiological and pathological conditions on LV function.
It has been postulated that abnormal ventricular long-axis dynamics may be due to
subendocardial ischemia, which would mainly affect the longitudinal oriented myocardial
fibers (3, 11, 12, 20, 31). In that case both the magnitude of the AEV/LVSV ratio and the
relative time courses of these two parameters would be affected. Furthermore, in both normal
aging and LV hypertrophy there is decreased long axis motion, increased short axis motion
and unchanged ejection fraction (32, 33). The relationship between AEV/LVSV would be
expected to be affected in these conditions as well.
The correlation between the annular excursion volume and LV stroke volume was strong
whereas AEV and LV ejection fraction had a weak relation (2, 33).
Mitral Annular Shape Variation
The diastolic increase in mitral annular area is consistent with earlier results in both human
and animal studies (6, 7, 29), which also demonstrated that the maximal area occurring in mid
to late diastole. The 91±7% decrease in MA area during atrial contraction that was measured
in this study is also in agreement with earlier findings (16, 28, 29, 30). Glasson et al. found a
presystolic MA area reduction of 89±3% in their ovine model, with the minimal area
11
occurring immediately after mitral valve closure (7).
The shape changes of the MA have been investigated previously with different and more
invasive methods. The increase in interpeak distance during diastole followed by a reduction
during atrial contraction is similar with recent findings from an animal study (28). Glasson et
al., showed that the ratio of the septal-lateral dimension and the intercommissural dimension
in sheep fell from 0.73±0.02 to 0.69±0.01 during this presystolic period (7). While the
intercommissural distance are not strictly identical to the points used in this study, they can be
generally compared to the timing and extent of the fall in IP/IV ratio in the current study, in
both cases indicating a more elliptic shape at end-diastole.
The dynamic changes in MA shape suggest that the annulus has a sphincter-like action. These
temporal changes may facilitate ventricular filling by annular expansion during early and mid
diastole, and aid competent mitral valve closure during the marked decrease in MA area in late
diastole and early systole.
Alterations in the timing of atrial contraction in sheep have been shown to affect MA
dynamics, suggesting an “atriogenic” influence on annular physiology (7, 25, 29). An
anatomic basis for this relationship can be found in the atrial myocardial fibers that have been
shown to insert into the MA, especially in the lateral region of the annulus which is relatively
more dynamic (1).
Timek and co-workers demonstrated that increased atrial size and diminished atrial
contraction were accompanied by increased end-diastolic MA size and decreased presystolic
MA area reduction. Delayed valve closure was also accompanied by MA area and septallateral diameter dilatation and they proposed that this perhaps was due in part to a decrease in
presystolic annular reduction (28). It has also been suggested that under normal conditions,
12
MA septal-lateral diameter reduction before systole acts to “pre-position” the leaflets for
closure before the rise in LV pressure in early systole (28). In an ovine model of tachycardiainduced cardiomyopathy, a 25% increase in end-diastolic septal-lateral diameter was proposed
to be the underlying mechanism of mitral regurgitation (27).
The present study shows an IP increase and IV decrease during systole which is consistent
with some prior studies (7, 13, 28), although a decrease in the IP diameter was described in
earlier estimates (6). The anteroseptal segment of MA is firmly attached to the rigid structures
of the aortic annular complex. During mechanical systole the LV longitudinal fibers that insert
into the annular ring are exerting a pulling force toward the apex. This force may elicit more
descent at the more flexible lateral portion of the MA compared to the anteroseptal part, thus
increasing the IP distance. During early systole the increase in LV pressure exerts a force
backwards on the mitral valve apparatus, and this may partially explain the MA dilatation seen
during this period.
Comparison to Other Methods
The anatomical definition of the MA with echocardiography is more subjective than in
imaging based on visually identifiable structures such as implanted myocardial markers or
piezoelectric crystals (26). Nevertheless, the tracing of the annulus from noninvasively
acquired images in the present study was performed in a consistent manner, with good
reproducibility demonstrated by the absence of significant inter- or intraobserver variation.
Earlier studies of the MA using invasive methods have been based on a Fourier series fitted to
3 spatial coordinates for each time frame (18). The method used in this study fit the Fourier
13
series to the complete data set, with 3 spatial coordinates and time t, for the first time. This
resulted in a more stable description of annulus and allows a higher number of the Fourier
terms to be fitted to the data. This development offers definite advantage when describing
physiological parameters in a reliable manner.
Study Limitations
Six of the experimental subjects were under general anesthesia during data acquisition, and
this might have contributed to the small circulatory volumes measured in those cases (17).
Age-related differences in left ventricular filling pattern could have influenced our findings to
some extent. While this was not studied in the present investigation, there was no obvious
difference between subjects at the upper and lower ends of the age spectrum of our subjects.
In the present study the calculation of the AEV change was performed with a higher temporal
resolution than the LV volume change, and this should be considered when comparing the
relative time courses of these two parameters.
The current analysis requires time-consuming post processing. Automatic segmentation
methods would make this approach more clinically applicable.
In conclusion, the excursion of the mitral annulus accounts for an important portion of the
total LV filling and emptying in humans. The amount of volume change attributed to the
annular excursion is concordant with previous estimates from invasive animal studies. These
data also support atrial influence on annular physiology, and suggest a sphincter-like action of
the annulus that may facilitate ventricular filling during diastole and aid competent valve
closure. The novel 4-dimensional TEE method presented here allows these mechanisms to be
14
studied non-invasively for the first time, and may serve as a tool for investigating the impact
of physiological and pathological conditions on LV and mitral valve performance.
Acknowledgements
The study was supported in part by the Swedish Heart and Lung Foundation and the Swedish Medical
Research Council (Grant 9481). The technical assistance given by Lisha Na, MD, is also gratefully
acknowledged.
15
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FIGURE LEGENDS
Fig. 1. Schematic of reconstructed mitral annulus (black lines) A: in two different time frames
during the cardiac cycle and the volume change in one of the 72 segments (grey lines) between
these two time frames. B: in end-diastole and end-systole, and the total annular excursion
volume (shaded grey). Saddlehorn, the annular region closest to the aortic annulus
Fig. 2. Schematic of reconstructed mitral annulus with interpeak (IP) and intervalley (IV)
distances and reference points around annulus. Lat, lateral; ant, anterior, sept, septal; post,
posterior. Saddlehorn, the annular region closest to the aortic annulus
Fig. 3. A: left ventricular (LV) volume and mitral annular excursion volume (AEV) changes
during the cardiac cycle. Data are mean values for all subjects (n=9). B: left ventricular
volume change variability; c annular excursion volume change variability. MC, mitral valve
closure; MO, mitral valve opening.
Fig. 4. Mitral annular area change during 2 cardiac cycles. Data are mean values for all
subjects (n=9). MC, mitral valve closure; MO, mitral valve opening.
Fig. 5. A: mitral annular interpeak (IP)- and intervalley (IV) distances during 2 cardiac cycles.
B: ratio of IP- and IV distances during 2 cardiac cycles. Data are mean values for all subjects
(n=9). MC, mitral valve closure; MO, mitral valve opening.
Table1. Basic demographic and clinical data of the study
population
Normal subjects
n=9
Age, years
56±11 (45-75)
Gender f/m
4/5
Height, cm
170±12
Weight, kg
77±11
Body mass index, kg/m2
23±2
Heart rate, beats/min
68±8
Systolic blood pressure, mmHg
126±26
Diastolic blood pressure, mmHg
79±13
Left ventricular end-diastolic volume, ml
96±22
Left ventricular end-systolic volume, ml
45±17
Left ventricular stroke volume, ml
52±12
Left ventricular ejection fraction, %
54±9
Values are means ± SD, (range).
Table 2. Linear correlation analysis between annular excursion volume and different
demographic and clinical parameters
Variable
AEV
SEE
Level of
significance
Weight, kg
0.82
1.1
p<0.01
Height, cm
0.74
1.3
p<0.05
Left ventricular stroke volume, ml
0.73
1.3
p<0.05
Age, years
-0.50
1.6
n.s.
Systolic blood pressure, mmHg
0.40
1.7
n.s.
Diastolic blood pressure, mmHg
0.39
1.7
n.s.
Heart rate, beats/min
-0.08
1.9
n.s.
Left ventricular ejection fraction, %
0.01
1.9
n.s.
AEV, annular excursion volume; SEE, standard error of the estimate.
Table 3. Total mitral annular excursion from 4 different sites around annulus
Annular excursion (mm)
Lateral
Anterior
Septal
Posterior
11±1.8
10±2.0
10±1.3
11±1.6
Values are means ± SD for all subjects (n=9).
Fig.1.A,B
d
Sa
n
or
h
dle
Base
A
d
Sa
n
or
h
dle
Apex
Base
Enddiastole
B
Endsystole
Apex
Fig.2
rn
o
h 150°
e
l
dd
a
S
Sept
180°
120°
210°
IP
240°
270°
Ant
300°
IV
90°
330°
0°
60°
30°
Lat
Post
Fig.3.A-C
50
LV volume
10
AEV
8
40
6
30
4
20
2
10
0
0
Time
MC
B
LV volume change (ml)
80
60
40
20
0
Time
MC
C
AEV change (ml)
14
12
10
8
6
4
2
0
MC
Time
MO
AEV change (ml)
LV volume change (ml)
A
Fig.4
Area (cm2)
10
9,5
9
Time
MO
MC
Fig.5.A,B
A
Distance (cm)
3,6
Intervalley
Interpeak
3,3
3
Time
B
0,95
IP/IV
more
circular
0,9
more
elliptical
0,85
Time
MO
MC