Eur J Cardiothorac Surg 2006;29:S56-S60
© 2006 Elsevier Science NL
Left ventricular muscle band (VMB): thoughts on its physiologic and clinical implications
John P. Boineau
*
Division of Cardiothoracic Surgery, Washington University School of Medicine, 660 S. Euclid Ave., Box 8234, St. Louis, MO 63110, USA
Received 17 February 2006;
accepted 28 February 2006.
* Corresponding author. Tel.: +1 314 362 8311; fax: +1 314 361 8706. (Email: schuesslerd{at}wustl.edu).
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Abstract
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Although the ventricular muscle band (VMB) is formed by one continuous band of myocardium and there is some evidence to suggest that it may contract sequentially along its course from the right ventricle, through the septum, then along its basoapical left ventricular spiral, the structure is not activated in this sequence. Activation as programmed by the fully developed Purkinje system proceeds broadly and directly from endocardium to epicardium and from apex to base. Although not activated sequentially along its course, the band may still contract and relax sequentially if there is a progressive lengthening of the contraction duration in association with a nonuniform lengthening of the cardiac fiber action potential (repolarization) duration. Also, the systolic and diastolic functions of the band should be considered as part of a complex, integrated electromechanical system in which the activation is programmed to ensure optimal function.
Key Words: Ventricular myocardial band • Ventricular activation and repolarization • Specialized ventricular conduction (Purkinje) system • Excitation–contraction coupling
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1. Introduction
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Anatomic data demonstrates that the heart can be unwrapped, forming a continuous myocardial strap or band, proceeding from the lateral RV and its outflow to the LV and its outflow. This band is separated by a plane of connective tissue which can be separated as demonstrated by Torrent-Guasp et al. [1]. The tissue of the unwrapped band appears to be relatively isotropic (all fibers running approximately parallel). In the LV, the band proceeds first around the base and then loops in a figure of eight spiral around the apex and back to the LV base. Investigators have postulated that this structural architecture has important hemodynamic consequences which could determine the sequence of contraction and relaxation of the ventricles. They also conclude that disruption of the structure could have a significant effect on mechanics and should be considered with surgical remodeling of the LV [2]. In addition to overcoming outflow impedance and pressure and ensuring flow, it would appear that the ventricular muscle band's (VMB's) other systolic function is to ‘wind-up’ (wringing out the blood mass) and at the same time compress the elastic helical spring, which when released recoils in diastole creating the conditions for LV suction. Thus, anatomy mechanics, and motion of the ventricles and VMB must be tightly integrated. This would require a special kind of electrical activation to program this degree of mechanical complexity.
There is some MRI data which suggests that the cardiac contraction phase sequentially follows the band from right to left. Since the band fibers are approximately isotropic or parallel, and if the band loops were electrophysiologically perfectly insulated by the connective tissue plane, then focal stimulation of the lateral RV should be followed by sequential activation and contraction following the various convolutions of the band.
This helical looping of the LV myocardial architecture has long been known [3]. In the 1960s, Kienle first described the changing distribution of currents corresponding to the locations of wavefronts as activation moved through the LV walls from endocardium to epicardium [4]. He concluded that the intramural location and distribution of wavefronts could be deduced from the orientation of the current fields since they parallel the major axes of the cardiac fibers. Over the QRS interval, the orientation changed from horizontal to oblique, occasionally became vertical, then took a different oblique axis or horizontal again. This data is also available from potential distribution maps obtained from either the body surface or the epicardium, since the current fields are perpendicular to the potential fields.
Cardiac ultrasound images demonstrate myocardial planes and long-axis views. Some adjacent parallel segments often appear to be moving discordantly—particularly in the septum. Although part of this discordance may be due to the projection of a three-dimensional event onto a two-dimensional echo plane, the images suggest that there could be some discordance of adjacent fiber bundles in the same plane.
At the macroscopic level, studies by LeGrice et al. [5,6] have emphasized the laminar structure of ventricular myocardial organization and changes in its direction at different LV transmural depths. Long-axis sections through the LV support a radial or endo- to epiorientation of individual muscle fiber bundles separated by connective tissue planes. This radial orientation is more consistent for the midmyocardium and contrasts with a more tangential arrangement of myofibers closer to the epi- and endocardial surfaces. Most of these studies are based on analyses of individual LV cross-sections taken from different focal LV sites. This data provides the basis for several current mathematical solutions used to model the spread of activation and the development of wall tension (stress and strain) [7]. However, these methods limit a comprehensive three-dimensional analysis which would be important if the myocardium is organized predominantly as a continuous isotropic band arranged in a three-dimensional figure of eight or helical configuration as suggested by the unrolled LV band.
Several groups have examined the muscular architecture of the ventricles at both the microscopic and macroscopic levels. At the microscopic level, the data has emphasized the geometric anisotropy of fiber orientation and its relationship to propagation of activation. Spach et al. [8,9] have shown that activation is considerably faster in the direction of the fiber orientation compared to cross-fiber activation. Furthermore, they have demonstrated that even though cross-fiber activation is slower than axial depolarization, it has a greater safety factor for conduction than depolarization in the long axis of the fibers. Saffitz et al. [10] have demonstrated the importance of the arrangement of myocardial connexons of low electrical resistance and the relatively synchronous spread of activation in the ventricles. In addition to the myocardial fiber anisotropy, the greater spacing of connexons bridging connective tissue planes between parallel fiber bundles results in a somewhat circuitous spread of the impulses across the fiber axes. However, these microscopic discontinuities are minimized by the broad wavefront of electrical generators encountering the fiber long axes as a result of the rapid endocardial dispersion by the Purkinje system.
When one considers the actual activation sequence of the ventricle, there is an apparent mismatch between the EP and the band anatomy. Activation does not follow the band but occurs relatively synchronously directly and radially from endo- to epicardium, crossing any anatomic ‘discontinuity’ created by the connective tissue planes of the band [11,12] (see Fig. 1
). The activation begins in both the right and left ventricular endocardium and spreads radially (transventricular) along all axes concurrently, thus initiating the activation sequence within a very small time window (<15 ms), and total activation lasts for only 80–90 ms in most normal adult humans. If the band were activated unidirectionally along its continuous course, then the total activation time would be much longer and determined by the normal myocardial conduction velocity (0.2–0.6 m/s) [13] times the length of the unrolled strap. However, the normal sequence of ventricular activation results in a greater synchrony, albeit less unidirectional than that which would occur if the band activated and contracted along its course.
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Fig. 1. Transmural activation of the anterolateral LV in a dog. Note the uniform spread of wavefronts from subendocardium to subepicardium in the LV wall and also oppositely in the papillary muscle (PM). This synchronizes contraction of the PM with the LV.
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The basis of synchronous activation is due to the following factors: (1) a specialized ventricular conduction system (SVCS) which consists of two central impulse distribution points insulated from the smooth upper endocardium, the common left, and right bundle branches. Thereafter the SVCS branches geometrically into increasingly greater numbers of fascicles of finer geometry, finally becoming noninsulated only at the most distal of thousands of terminations in LV and RV. (2) A richly trabeculated endocardium in which the endocardial invaginations carry the Purkinje tissue partway into the LV endocardium, further increasing the speed and area of early ventricular activation. (3) A very rapid conduction velocity of the SVCS (approximately 1.5–2.5 m/s) [13,14] which is five times faster than ordinary radial myocardial spread across the walls. (4) A predominantly radial (in contrast to tangential) component of the transmural fiber axis. However, this does not nullify other major axial components of an obliquely oriented muscle band.
In addition to the effect of the Purkinje system, myocardial activation is anisotropic, progressing faster in the axial than radial direction if artificially stimulated near the center of the LV wall. As a result of the Purkinje programming, the highly trabeculated nature of the apical and midwalls, and because the LV apex is thinner than the base, the activation viewed from the epicardial surface travels from apex to base (Fig. 2
). Thus, the thought that activation travels unidirectionally along the ventricular myocardial band from right ventricle through the septum and through the LV hilex from base to apex then back to base, thereby determining a convoluted sequential contraction, is untenable. However, activation resulting from an artificial, focal stimulation (pacing) propagates faster in the fibers’ long axis than transversely. Therefore, myocardial propagation in the direction of the band could be greater than across the band, at least for certain distances, but then connexons, which cross the connective tissue planes electrically connect and pass on the radial or transverse activation. However, the band still may have an effect due to the mechanical differences in the durations of contraction and relaxation phases.
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Fig. 2. Canine epicardial activation. Note the early ‘breakthrough’ of activation in the midanterior RV and later breakthrough at the LV apex. Subsequently, activation progresses centrifugally in the RV and from apex to base in the LV. Human activation has much the same sequence.
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Thus, how does the activation of the developed heart relate to the ventricular myocardial band? During cardiac development, activation and contraction proceed unidirectionally from the venous pacemaker and from proximal to distal in the cardiac tube. This causes a peristaltic-like contraction in the direction of blood flow. This unidirectional peristalsis continues into the early stages of looping of the cardiac tube. Between 5 and 8 weeks with the evolution of septation and wall thickening, endocardial trabeculation begins and with it the development of the specialized ventricular conduction system. Thus, at about 7–8 weeks, there is a functioning Purkinje system with rapid depolarization which reorders the myocardial activation [15]. Therefore, in the developed heart, the activation no longer proceeds unidirectionally from proximal to distal or along the convoluted ventricular muscle band. Then how might mechanical function proceed sequentially along its helical course if not activated unidirectionally? First, it is unlikely that this structure has no functional consequences. Whether function follows form, or vice versa (or both), there are very few biologic entities that do not subserve some function or have some functional consequences. Second, although excitation and contraction are rapidly and sequentially initiated by depolarization, if contraction lasted significantly longer in some of the components of the band than in others, then the band could still have an important mechanical effect on pumping and relaxation sequences. There are several seemingly unrelated bits of data that may have some bearing on this.
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2. Electromechanical coupling—background
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It has long been known that subendocardial fibers have longer action potential durations than subepicardial fibers [16]. Also, more recent studies by Antzelevitch et al. [17] have shown that the midmyocardial fibers (M cells) have very long action potentials, longer than even the subendocardial fibers. In isolated preparations, these action potentials are capable of extreme durations. In vivo, however, the electrotonic interactions with all of the other cells with shorter action potentials ‘steals’ currents and reduces the extreme durations of individual cells. These M cells also appear to be different in their molecular, biochemical, and ion channel characteristics from other cells. These longer action potentials implicate a much longer midmyocardial contraction phase than either the inner or outer LV layers. Thus, even though programmed for rapid synchronous radial activation by the SVCS, perhaps certain deeper fibers although activated early could still contract longer. If those endo and midwall fibers were arranged along the band, then this might contribute to the base to apex and vortical motions during contraction and relaxation.
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3. Hypothesis
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If longer action potential durations implicate a longer phase of contraction, then subendocardial and midmyocardial fibers, although activated earlier than subepicardial fibers, could contract longer (Fig. 3
). Since these fibers are arranged unidirectionally along the ventricular myocardial band, even though activated earlier, they might still contract longer, resulting in some directional mechanical force along the band.
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Fig. 3. Action potential duration correlates with the length of contraction. There is nonuniform action potential duration of the different transmyocardial regions. Thus, even though activated early some VMB regions might sustain tension for longer periods than others.
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Is it possible that the Purkinje system, with its intrinsic developmental link to the trabeculated endocardium, by synchronizing and minimizing the activation, actually functions to permit optimal contraction of the ventricular myocardial band rather than an impediment to its operation? Although speculation, it suggests possible avenues of investigation of the relation between cardiac cellular, molecular, biochemical, and macroscopic electrophysiology and anatomy.
Although it is traditional to think of form determining function, the two are inextricably linked and in the developing heart function plays a major role in determining form. It is likely that with increasing flow demands together with increasing ventricular mass and rapid filling that diastolic turbulence and shedding of fluid vortices have an effect on the evolution of the complex endocardial trabeculations. Also, trabeculation and evolution of the Purkinje system are closely linked temporally and possibly both are affected by the hemodynamics. These functional effects probably extend to the development of the VMB. From this perspective one begins to see the VMB in a larger context as part of an integrated, interdependent system in which evolving function has a major shaping influence on the final anatomic conformation. It implicates an interaction between the molding forces and the responding tissue which contains all of the necessary molecular machinery to differentiate and adapt resulting in its final anatomic and functional form as expressed in the developed heart.
Of particular interest would be computational models which integrate the macroscopic band geometry, and the microscopic two- and three-dimensional reconstructions with the cellular and molecular studies of different myocardial fiber types (Fig. 4
).
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Fig. 4. Proposed concept of the relationships among developmental factors which determine the adult ventricular architecture and its mechanics.
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These models should consist not only of geometric and electrophysiologic parameters but also the mechanical effects of diastolic ventricular filling and systolic loading, since many of the anatomic, mechanical, and electrophysiologic functions may be interdependent. Most of the technology to perform this task is currently available. This would require the collaboration between several different groups and institutions and necessitate a significant level of research support and funding.
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Footnotes
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This article was originally presented on May 28, 2005, at The New Concepts of Cardiac Anatomy and Physiology, Liverpool, UK.
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References
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Abstract
1. Introduction
