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Eur J Cardiothorac Surg 2006;29:S139-S144
© 2006 Elsevier Science NL

The sequence of regional ventricular motion

Manel Ballester-Rodés a , * , Albert Flotats b , Francisco Torrent-Guasp c , Ignasi Carrió-Gasset a , Manel Ballester-Alomar d , Francesc Carreras e , Ana Ferreira f , Jagat Narula g

a Department of Medicine, Faculty of Medicine, University of Lleida, Spain
b Service of Nuclear Medicine, Hospital de la Santa Creu i Sant Pau, Barcelona, Spain
c Consultant Cardiologist, Faculty of Medicine, University of Lleida, Spain
d Hospital de Mataró, Barcelona, Spain
e Cardiac Diagnostic Imaging Unit, Department of Cardiology, Hospital de la Santa Creu i Sant Pau, Barcelona, Spain
f Hospital Royo Villanova, Zaragoza, Spain
g Division of Cardiology, University of California, Irvine College of Medicine, CA, USA

Received 17 February 2006; accepted 27 February 2006.

* Corresponding author. Address: Catalunya 1, esc. A, 3-2, 08390 Montgat, Barcelona, Spain. Tel.: +34 639354201. (Email: mballesterr{at}comll.es).


   Abstract
Top
 Abstract
1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
 5. Implications
 6. Limitations of the...
 References
 
Objective: The chronology of electrical events that mechanically activate the myocardium has been described as initiating at the level of the septum, spreading to the apex, then to the bodies of both ventricles and eventually to the base of the heart (apex-to base activation). It has recently been suggested that the myocardium is a single muscular band that conforms a double-loop helicoid. Contraction of the myocardium would follow the trajectory of the muscular fibers that originate at the pulmonary artery towards the body of the left ventricle and to the aorta (base-to apex contraction). This would explain the movements of the base of the heart and the twisting motion of the ventricles seen at magnetic resonance studies. Methods: Temporal Fourier analysis of equilibrium radionucleide angiocardiography, by studying the topography of the regional myocardial mechanical displacement corresponding to the wave front of electro-mechanical activation, provides information on the sequence of regional ventricular contraction was used in 29 normal individuals to observe the sequence of myocardial motion. Results: Analysis disclosed that the base of the heart first moves (right then left ventricle) and mechanical movement later descends to involve the apex and the septum. These findings are in concordance with the proposed activation of the helical myocardium and open the way to more complex studies. Conclusions: Although electrical activation of the myocardium (QRS complex) follows a septum–apex–body–base of the left ventricle sequence, mechanical activation follows a base-to-apex sequence. This is likely to be related to anisotropic propagation of the electromechanical stimulus throughout the myocardial band once the electrical stimulus has been delivered at the base of the heart.

Key Words: Radionucleide angiocardiography • Helical ventricular myocardial band • Excitation contraction coupling • Regional ventricular motion sequence


   1. Introduction
Top
 Abstract
 1. Introduction
2. Patients and methods
 3. Results
 4. Discussion
 5. Implications
 6. Limitations of the...
 References
 
Recent studies have shown that the ventricular myocardium can be dissected as a single muscular band, which fibers can be seen to extend from the pulmonary artery to the aorta, and spatially configures a double-loop helicoid (Figs. 1 and 2 ) [1–5]. The functional implications of this anatomy have been a recent focus of interest. It has been suggested that the downward/upward movements of the base of the heart and the twisting motion of the ventricles seen at magnetic resonance studies could be explained by the sequential mechanical motion of the ventricular band from the pulmonary artery to the aorta preferentially following the muscular fibers (anisotropic conduction) [4,6]. This would provide a link between ventricular form and function [7].


Figure 1
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  		Fig. 1. (A) Successive phases of unrolling of the ventricular myocardium into a single muscular myocardial band. The band extends from the pulmonary artery to the aorta and in its middle portion suffers a 180° twist. (B) Unrolling of the band. When extended several segments can be identified: the right (RVS) and left (LVS) ventricular segments conform the basal loop. The descendent segment (DS) and ascendent segment (AS) constitute the apical loop. (C) Schematic presentation of the double-loop helical orientation of the myocardial band. Abbreviations: Ao, aorta; AS, ascendent segment; DS, descendent segment; LVS, left ventricular segment; PA, pulmonary artery; RVS, right ventricular segment.

 

Figure 2
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  		Fig. 2. Proposed role of sequential contraction of the ascendent and descendent segments of the ventricular band in the ejection and suction of blood [3–5,8,29]. (a) The basal loop has been removed to expose the apical loop (b) formed by the descendent (DS) and ascendent (AS) segments; (c) during systole, the base of the heart is pulled downwards, towards the apex, due to the contraction of the descendent segment (thick bundles). This results in shortening of the left ventricular cavity and result in ventricular ejection. Such a movement of the DS forces the ascendent segment to adopt a curvilinear configuration. Subsequent contraction (thick bundles) (d) uncoils and undoes the configurational change and allows sudden upward movement of the base of the heart, resulting in expansion of ventricular cavity and ventricular filling. The torsion and untorsion motion of the ventricles extensively described in magnetic resonance studies [11–22] can be explained by the angled spatial distribution of the descendent and ascendent and fibers.

 
In this model, the proposed sequence of myocardial contraction starts from right ventricle to involve the entire base of the heart before descending to the apex and septum (base-to-apex contraction) [3,4,6].

In order to study the topography of the regional myocardial mechanical displacement, corresponding to the wave front of electro-mechanical activation, and to correlate it with the proposed anatomy of the myocardial band, Fourier analysis of equilibrium radionucleide angiocardiography was employed in a series of 29 normal individuals.


   2. Patients and methods
Top
 Abstract
 1. Introduction
 2. Patients and methods
3. Results
 4. Discussion
 5. Implications
 6. Limitations of the...
 References
 
Planar equilibrium radionucleide angiocardiography (RNA) studies were performed in 29 patients without heart disease admitted prior to receiving doxorubicin treatment for cancer. They all had a clinically normal cardiovascular examination and a normal electrocardiogram. Radio labeling of the red blood cells was accomplished by an in vitro method following OSHA guidelines for safe handling of human blood products [8]. Nine hundred and twenty-five MBq of technetium-99m-labeled autologous red blood cells were intravenously administered [9]. RNA images are acquired 10 min later by a gamma camera (Siemens Orbiter) interfaced to a dedicated computer (Elscint Apex SPX) using a low energy high resolution parallel hole collimator, with an appropriate ECG gating device linked to the image acquisition computer. A beat length window of 15% was selected, and 32 frames per R-R interval were acquired in a 64 x 64 matrix at a spatial resolution of 4.4 mm, for a total of 7 million. Supine imaging was performed in the anterior, best septal with 10° caudal tilt and left lateral views [10].

To assess the technical adequacy of acquisition, visual assessment of the LAO view in a cine loop mode was performed and the number of cycles and collected counts checked. Spatial and temporal smoothening was applied to compensate for changes due to noise of random variation and decay of radioactivity [9]. Amplitude and phase parametric images at the fundamental frequency (the heart rate) were generated by calculation of amplitude and phase parameters of the first harmonic for each elementary curve, on a pixel-by-pixel basis.

The time–activity curve of each pixel was fitted with a single cosine whose period equated an R-R interval. A phase histogram was obtained plotting the different values of the phase on the abscissa in degrees with the number of elements in the same phase on the ordinate. A dynamic display mode was used to demonstrate the sequence of mechanical activity that involved the ventricles during contraction (Elscint Apex SPX Contraction Onset Display function). The phase data were presented in a sequential display of 32 myocardial contraction images, in which pixels within the phase image are added based on their phase value. The color-coded sequential display of myocardial contraction images can be viewed both cinematically, as continuous-loop movie or frame-by-frame, for improved perception of the overall sequence of contraction.


   3. Results
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
4. Discussion
 5. Implications
 6. Limitations of the...
 References
 
Fig. 3 displays sequential ventricular motion in four different normal individuals. At the beginning of the sequence, a signal invariably appeared in the most basal portion of the right ventricle, at the level of the pulmonary infundibulum, in the form of a dot or a line. This signal gradually spread to involve the entire right ventricular wall. After the right ventricular mechanical motion had started, but no yet completed, the activity appeared in the basal portion of the left ventricle and fully extended to the entire base of both ventricles. At this stage, no activity was detected in the apical or septal regions of the ventricle. Finally, the mechanical activity extended to involve the apical and septal regions. This sequence of mechanical motion was invariably observed in the 29 normal individuals studied.


Figure 3
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  		Fig. 3. Sequential Fourier analysis of equilibrium radionuclide angiocardiography in four normal individuals. These studies provide information on the wave front (indicated in yellow) of ventricular contraction [30–32]. Invariably, the earliest activation occurs in the base of the right ventricle near the pulmonary infundibulum, extending to the basal portion of the left ventricle. The apex and septum, at the time of mechanical activation of the base of the heart, seem to be spared, leaving an ‘island of inactivity’ (white arrows) which is filled in subsequent images.

 

   4. Discussion
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
5. Implications
 6. Limitations of the...
 References
 
The precise ventricular mechanics have been recently unveiled in magnetic resonance tagging studies [11–22]. Using this technique, a complex motion of the ventricular myocardial fibers throughout the cardiac cycle is observed: (a) a systolic downward displacement of the base of the ventricles towards a motionless apex; (b) an initial systolic clockwise motion of base and apex, and a change to an anticlockwise motion of the base while the apex continues to move clockwise; (c) undoing of the previous movements in diastole; and (d) rapid untwisting of the apex lasting less then 75 ms preceding the filling phase of the ventricles [17]. The precise explanation for these movements is lacking.

4.1 Myocardial mechanics and anisotropic conduction
Recent reports have disclosed that the myocardium is formed by a single muscular band that expands from the pulmonary artery to the aorta and spatially adopts a double-loop helicoid (Figs. 1 and 2). The muscle fibers originating from the pulmonary artery and right ventricle can be visually followed to the basal portion of the left ventricle, at which point they descend to the apex in a spiral way and finally ascend to the base of the heart and eventually reach the aorta. Microscopically, studies have shown that the myocardial architecture is laminar and formed by sheets of myocytes separated by layers of perimysial connective tissue [23]. When the myocardium contracts, sliding between the myocardial laminae and apposition occurs, which results in local wall thickening [24–26].

Progression of ventricular motion preferentially follows the longitudinal axis of the myofibers, in what has been named as anisotropic conduction. Thus, it seems coherent that having identified the trajectory of the myocardial fibers along the ventricular band, propagation would take place along the described helicoid [7]. According to this model, the first two segments to contract would be the right ventricle and the basal portion of the left ventricle (basal loop), a phenomenon previously described by Armour and Randall [27] as a stiff outer shell. At that point, contraction of the descendent segment, which spirals down to the apex occupying the left ventricular endocardium, would bring the contracted basal loop close to the apex, rotate the base of the heart anticlockwise, and reduce left ventricular volume, which, along with ventricular wall thickening, would generate ejection of the blood from the ventricles. Subsequent contraction of the ascendant segment would cause a brisk upwards motion of the ventricular base and an elongation of the ventricular chamber with the mitral and aortic valve closed, and the generation of a negative pressure which would open the atrioventricular valves [17] to initiate the rapid filling and a clockwise untwisting of the base of the ventricles. It has recently been proposed that the descendent and ascendant segments act as an agonist–antagonist muscular unit [28], and systolic ventricular filling is due to muscular contraction of the ascendant segment [29].

In the present study, temporal Fourier analysis of the phase image of equilibrium radionucleide angiocardiography (RNA), which offers information about the timing of regional ventricular contraction by identification of changes in regional mechanics [30–33], was used to analyze the progression of myocardial motion. In the early 1980s, Fourier analysis of the phase image was employed to evaluate various cardiovascular conditions characterized by asynchronous ventricular contraction, such as myocardial infarction, disorders of conduction, or pre-excitation syndromes. Links et al. [30,32] described cinematic display of the phase data as a ‘wave of emptying,’ in which pixels within a static image of the heart blacked out at a time based on their phase value. This display constitutes a morphologic representation of the phase histogram wherein the zones are displayed sequentially as they reach their minimal volume (or phase). Validation of the method was reported when catheter stimulation at different ventricular sites precisely corresponded to the site detected by phase analysis [32].

Therefore, this method was deemed adequate to discern between the two modes of ventricular mechanical motion (base-to-apex, apex-to-base) in 29 normal individuals. The findings reported indicate that myocardial motion is initiated at the basal portion of the right ventricle, extends to the basal portion of the left ventricle and later proceeds to involve the apex and septum. These observations are in accordance to the sequential mechanical motion proposed to occur in the helicoid ventricle, which first involves the base of the heart later to involve the septum and apex [3,4,6].

4.2 Initial two-site basal ventricular motion
Close observation of basal ventricular motion reveals that initiation of the stimulus begins in the upper portion of the right ventricle and gradually expands to the free wall of the right ventricle (see Fig. 3), but much before the entire right ventricle is activated, the basal portion of the left begins its mechanical motion. This would not be expected if motion of the myocardium band would follow, in a strict sequence, the right and then the left ventricle through the band (see Fig. 4A). In fact, there seems to be two different sites that almost simultaneously activate the base of the heart (Fig. 4B), motion of the right ventricular base preceding the left basal portion. This is in agreement with recent studies showing temporal evolution of the three dimensional strain maps derived from magnetic resonance imaging, which allow mapping the electromechanical motion of the ventricles (Fig. 5 ) [34]. These maps illustrate that the onset of motion is observed at the level of the base of the heart in two distinct sites. In the mentioned study, pacing of the right or left ventricle revealed isochronic waves of mechanical activity spreading across the myocardium at a velocity that doubled the ventricular activation via the normal conduction, whereas stimulation of the atria was followed by a simultaneous motion of the base of the heart at two different opposing sites: right ventricle and the base of the left ventricle. Therefore, these observations are in accordance with the Fourier studies herein described, and could reflect the role of the specific electrical conduction tissue in synchronizing and/or accelerating electromechanical motion through the ventricular myocardium (Fig. 4C).


Figure 4
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  		Fig. 4. Hypothesis of anisotropic conduction through the helicoid myocardial band. A fully extended myocardial band is shown: (A) expected electrical activation, which starts at the level of the infundibulum of the pulmonary artery and spreads through the free wall of the right ventricle and proceeds to the left basal portion of the left (activation of the descendent and ascendent segments not shown); (B) interpretation of the findings: activation of the right ventricle (right segment of the band) takes place, but much before spread of activation to the entire right ventricle has been completed, the base of the left ventricle (left segment of the band) is activated (the two-site activation shown in arrows); (C) a possible interpretation takes into account the cardiac conduction system; the right bundle branch first activates the ventricular mass, and after a short interval, much before the entire right ventricle has been involved, the left bundle branch activates the left ventricular base. Thus, a two-site basal ventricular band activation seems to be occurring.

 

Figure 5
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  		Fig. 5. Temporal evolution of the three dimensional mechanical activation maps derived from magnetic resonance imaging of paced canine hearts and mapped into a bull's eye plot of the ventricle (see schematic representation on top of the illustration) Modified from Wyman et al. [34]. The thick black line delineates the interior edge of the right ventricle. The thin lines represent isochrones of activation times. The white ‘X’ indicates the pacing site. The left map corresponding to pacing of the most lower part of the right ventricle, near the septum, shows that the mechanical activity which appears near the right ventricle (blue) uniformly spreads from this ventricle to involve the left. On the contrary, the map in the middle of the illustration represents pacing of the coronary sinus, where the basal portion of the left ventricle is first activated (blue) and the front wave uniformly spreads in the direction of the right ventricle; finally, the bull's eye map on the right of the figure, obtained when pacing is from the right atrium (thus reproducing the physiologic ventricular activation), discloses two opposing initial sites at the ventricular base, in a way similar to the findings revealed at Fourier studies (Fig. 3).

 

   5. Implications
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
 5. Implications
6. Limitations of the...
 References
 
The implications of the findings herein reported are several: (a) the role of the electrical conduction system in the activation of the helicoid heart should be evaluated; (b) surgical therapies aimed at reducing the left ventricular volume to treat heart failure must take into account the functional implications of excising/sparing certain segments of the band in order to optimize surgical results [6,35]; (c) biventricular pacing has become a form of treatment of patients with heart failure and intraventricular conduction defects. Intriguingly, only about one-half of the patients favorably respond to the device insertion [36], and a sound explanation for the success observed in these patients or failure to improve in others is not forthcoming.

Knowledge of the natural sequence of electromechanical ventricular motion should open the way to study the effects of selective stimulation of the segments of the band on ventricular function, and provide a rationale for ventricular pacing protocols. In fact, several aspects of ventricular function should be rethought in the light of the helicoid ventricular anatomy proposed. New techniques, such as heart surface optimal mapping of transmembrane potentials, where three-dimensional spatio-temporal events can be analyzed [37], or diffusion magnetic resonance imaging [38], which may display in vivo myofiber orientation and therefore image myocardial angles of the descendent and ascendant segments during the cardiac cycle, could provide some of the tools needed to clarify the complexity of ventricular function in health and disease.

In summary, although electrical ventricular activation (QRS complex) follows a septum–apex–body–base sequence, mechanical motion follows a base-to-apex sequence. This is likely to be related to anisotropic propagation of the electromechanical stimulus throughout the myocardial band once the electrical stimulus has been delivered at the base of the heart.


   6. Limitations of the study
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
 5. Implications
 6. Limitations of the...
References
 
The present study does not attempt to precisely describe the sequence and topography of electromechanical motion, but to explore the sequence and direction of ventricular contraction. The method used is useful but, admittedly, not optimal: (a) indeed, the precise topography of the wave front of myocardial contraction cannot be inferred from planar images. In this respect, SPECT studies would provide a better spatial resolution but at expense of reducing temporal resolution; (b) the only phase of the cycle analyzed is the systolic phase, to where reduction of ventricular volume was minimal. Therefore, no analysis of the filling phase could be obtained. Despite these limitations, data herein included open a discussion to the precise sequence of myocardial contraction in humans.


   References
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
 5. Implications
 6. Limitations of the...
 References
 

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