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Am J Physiol Heart Circ Physiol 287: H1836-H1841, 2004. First published June 17, 2004; doi:10.1152/ajpheart.00103.2004
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Contribution of mitral annular excursion and shape dynamics to total left ventricular volume change

C. Carlhäll,1,3 L. Wigström,1,3 E. Heiberg,1,3 M. Karlsson,2,3 A. F. Bolger,4 and E. Nylander1,3

Departments of 1Medicine and Care/Clinical Physiology, 2Biomedical Engineering, and 3Center for Medical Image Science and Visualization, Linköping University, Sweden; and 4Department of Medicine/Cardiology, University of California, San Francisco, California 94143

Submitted 5 February 2004 ; accepted in final form 11 June 2004


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 GRANTS
 REFERENCES
 
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 (means ± SD) years underwent transesophageal echocardiography (TEE). The MA was outlined in all time frames, and a four-dimensional (4-D) Fourier series was fitted to the MA coordinates (3-D+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 3-D LV volumes were calculated by tracing the endocardial border in six 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 middiastole, 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-D TEE method is the first to allow noninvasive measurement of AEV and may be used to investigate the impact of physiological and pathological conditions on this important aspect of LV performance.

annular physiology; ventricular long-axis function; echocardiography; three dimension; four dimension

THE MITRAL ANNULUS (MA) is a discontinuous fibrous ring and an essential component of the mitral valve/left atrial/left ventricular (LV) complex. It contributes to efficient valve closure as well as unimpeded LV filling (14, 19, 28, 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 (28, 29). Assessment of the MA physiology has been important to the understanding of disorders of the mitral valve apparatus and LV 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, 27) are two of many areas where MA physiology is a key issue.

MA 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 MA excursion contributes to the total LV 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 (3-D) echocardiography is an important achievement in cardiac imaging (4, 13, 15). In this study 4-dimensional (4-D) transesophageal echocardiography (TEE) with high-resolution acquisition and digitally stored data allows the annular excursion volume (AEV) to be assessed noninvasively in humans.

The goals of the present study were to noninvasively evaluate the variation in the shape of the mitral annulus during the cardiac cycle as well as the contribution of MA excursion to the total LV volume change, to reach a deeper understanding of the basic physiology of the mitral annulus.


   METHODS
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 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
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Subjects. Transesophageal echocardiography was performed in 10 patients without cardiac disease undergoing either noncardiac surgery (n = 7), or search for the source of cerebral embolism (n = 3). The criteria for enrollment were the following: age 20–75 yr, no history of current or prior heart disease or hypertension, absence of cardiac medications, a normal physical examination, a resting heart rate between 50 and 100 beats/min, 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 nine subjects (4 women and 5 men) aged 56 ± 11 yr (means ± SD) of whom six were studied during general anesthesia. One patient was excluded due to a heart rate >100 beats/min during image acquisition. The local ethical committee approved the research protocol, and informed consent was obtained from each patient.


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  		Table 1. Basic demographic and clinical data of study population

 
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 (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 two-dimensional sector in a lateral/septal starting position (0°). By means of a specific 3-D 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/s. Each scan was performed in <30 s, 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 Unix-based workstation for processing. Quantitative and qualitative analyses 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). 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.

To obtain a 4-D (3-D+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. On the basis of 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 with the image data. Each point was then described based on its rotation angle, {omega}, 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 {omega} and t. The number of terms used in the Fourier series controls the spatiotemporal 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 to achieve a physiologically realistic shape and longitudinal motion of the MA.

On the basis of 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.



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  		Fig. 1. Schematic of the mitral annulus (black lines) A: two different time frames during the cardiac cycle and the volume change in one of the 72 segments (gray lines) between these two time frames. B: end diastole and end systole and the total annular excursion volume (shaded gray). Saddlehorn, the annular region closest to the aortic annulus.

 
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. 1, A and B).

The MA shape variation was described by the interpeak (IP) and intervalley (IV) distance ratio. IP distance was measured between the two points, on opposite sides of the MA, that are most elevated toward the atrium. IV distance was defined as the distance between the two most apical points, on opposite sides of the MA (13) (Fig. 2).



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  		Fig. 2. Schematic of the mitral annulus (solid outline) 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.

 
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; Apex, NC). 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 <3%.

The 3-D LV 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. Because of 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 represented 47% of the cardiac cycle (13).

The impact of respiratory motion was minimal in these experimental conditions. Only three subjects were acquired during nonapnea, and these subjects 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. Because 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 means ± 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 three randomly selected subjects. Two-way ANOVA 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
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 METHODS
 RESULTS
DISCUSSION
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MA excursion volume. The magnitude of the MA excursion volume was 10 ± 2 ml, and this represented 19 ± 3% of the total LV volume change (52 ± 12 ml) in our study population (Fig. 3, A–C).



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  		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: LV volume change variability; C: annular excursion volume change variability. MC, mitral valve closure; MO, mitral valve opening.

 
The timing of the annular excursion volume and the LV volume changes during the cardiac cycle both demonstrated similar contributions from early (E) and late (A) diastolic mitral valve inflows (Fig. 3, A–C).

The annular excursion volume correlated strongly with LV stroke volume (P < 0.05) and body size (P < 0.05) but not with LV ejection fraction (NS, not significant) or heart rate (NS) (Table 2).


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  		Table 2. Linear correlation analysis between annular excursion volume and different demographic and clinical parameters

 
MA 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).



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  		Fig. 4. MA area change during two cardiac cycles. Data are mean values for all subjects (n = 9).

 
Nonplanarity 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 IP and 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, IP distance increased, whereas in contrast, the IV decreased (Fig. 5A).



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  		Fig. 5. A: MA IP and IV distances during two cardiac cycles. B: ratio of IP to IV distances during 2 cardiac cycles. Data are mean values for all subjects (n = 9).

 
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-to-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 midsystole (Fig. 5B).

The total annular excursion showed no significant differences in amplitude among the four standard points around MA (Table 3).


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  		Table 3. Total mitral annular excursion from four different sites around annulus

 

   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
GRANTS
 REFERENCES
 
MA excursion volume. In the current study the mitral annular excursion volume was assessed noninvasively using high-resolution 4-D imaging technique. This study demonstrates for the first time without considerable geometric assumptions, that the mitral annular excursion volume in humans accounts for an important portion of the total LV volume change. Earlier, Toumanidis et al. (29a) approximated from 2-D echocardiography the excursion volume of the mitral annulus as the volume of a truncated cone. Although their method was based on assumptions about 3-D volumes, obtaining a large excursion volume, it was a first attempt to study the annular excursion volume in humans. In the present study, the timing of the volume changes during the cardiac cycle seems to be synchronous and demonstrates similar contributions from E and A mitral valve inflows. All of 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. (23) demonstrated that the annular excursion volume accounted for one-fourth of the total LV filling in ovine hearts.

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 ~12% and an ejection fraction of <30% (8, 11). Longitudinal shortening also contributes to radial shortening because myocardial tissue volume is noncompressible 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 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 longitudinally oriented myocardial fibers (3, 11, 12, 20, 31). In that case both the magnitude of the AEV-to-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).

MA shape variation. The diastolic increase in MA 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% of the total decrease in MA area that occurred during atrial contraction in this study is also in agreement with earlier findings (16, 27, 28, 30). Glasson et al. (7) found that 89 ± 3% of MA area reduction occurred before LV systole in their ovine model, with the minimal area observed immediately after mitral valve closure.

The shape changes of the MA have been investigated previously with different and more invasive methods. The increase in IP distance during diastole followed by a reduction during atrial contraction is similar with recent findings from an animal study (27). Glasson et al. (7) 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. While the intercommissural distance are not strictly identical to the points used in this study, they can be generally compared with the timing and extent of the fall in IP-to-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 middiastole 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, 26, 28). 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 (27) 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 septal-lateral diameter dilatation, and they proposed that this perhaps was due in part to a decrease in presystolic annular reduction (27). It has also been suggested that under normal conditions, MA septal-lateral diameter reduction before systole acts to "preposition" the leaflets for closure before the rise in LV pressure in early systole (27). In an ovine model of tachycardia-induced cardiomyopathy, a 25% increase in end-diastolic septal-lateral diameter was proposed to be the underlying mechanism of mitral regurgitation (25).

The present study shows an IP increase and IV decrease during systole, which is consistent with some prior studies (7, 13, 27), 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 with 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 with other methods. The anatomic 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 (29). 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 noninvasive methods have been based on a Fourier series fitted to three spatial coordinates for each time frame (18). The method used in this study fit the Fourier series to the complete data set with three 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 LV 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 present analysis requires time-consuming postprocessing. 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-D TEE method presented here allows these mechanisms to be studied noninvasively 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.


   GRANTS
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 ABSTRACT
 METHODS
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 DISCUSSION
 GRANTS
REFERENCES
 
The study was supported in part by the Swedish Heart and Lung Foundation and the Swedish Medical Research Council (Grant 9481).


   ACKNOWLEDGMENTS
 
We gratefully acknowledge the technical assistance given by Dr. Lisha Na.


   FOOTNOTES
 

Address for reprint requests and other correspondence: C. Carlhäll, Dept. of Medicine and Care, Clinical Physiology, Univ. Hospital, SE 581 85 Linköping, Sweden (E-mail: carca{at}imv.liu.se)

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.


   REFERENCES
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