Eur J Cardiothorac Surg 2005;27:183-190
© 2005 Elsevier Science NL
The architecture of the ventricular mass and its functional implications for organ-preserving surgery
Paul P. Lunkenheimera,*,
Klaus Redmanna,
Robert H. Andersonb
a Experimental Thoraco-, Heart- and Vascular Surgery, University Hospital Muenster, Muenster, Germany
b Cardiac Unit, Institute of Child Health, University College London, London, UK
Received 11 May 2004;
accepted 5 October 2004.
* Corresponding author. Tel.: +49 251 83 56256; fax: +49 251 8356257. (E-mail: redmann{at}uni-muenster.de).
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Abstract
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It has generally been accepted that the myocardial fibres within the ventricular mass are arranged in syncytial fashion, precluding the identification of discrete and isolated muscular pathways. Recently, however, an entire hypothesis for surgical treatment has been proposed on the basis of the existence of a ‘ventricular myocardial band’, suggesting that this arrangement in itself points to detrimental results following partial ventriculectomy. In this review, we re-state the evidence supporting the accepted concept of the ventricular mass being made up of an undefined number of wedge-shaped functional units, each of them exerting its individually programmed contribution to the global activity of the ventricular walls. The wedge-shaped units consist of bundles of individual fibres which are arranged tangentially. An important subset of fibres intrudes into the ventricular wall, thus creating oblique pathways. Their angle of intrusion varies, and can be measured at up to 30°. The steeper the angle of their intrusion, the more efficiently do the fibres counteract the systolic mural thickening. The network of supporting connective tissue, nonetheless, provides the necessary steep angulation towards the endocardium. This fibrous matrix serves as continuous chain for the transmission of forces, including that in the direction from the epicardium towards the endocardium, resulting in a dilating force. We have shown, using needle force probes, that in the hypertrophic heart the dynamic equilibrium of dilating and constricting forces acts at elevated diastolic and systolic levels, because the obliquity of the fibres increases due to the thickening of the wall, and there is a concomitant increase in connective tissue, causing an increase in the forces opposing systolic mural thickening. Then, in a vicious cycle, both populations of myocardial fibres stimulate each other to hypertrophy. Eventually, coronary perfusion becomes critically impaired, with still further deposition of connective tissue. Ultimately, the vector of the dilating force comes to dominate the constricting force, and the ventricle dilates. In this setting, partial left ventriculectomy remains a functionally sound intervention, since it is capable of improving global ventricular function by improving the geometrical state of the remaining anatomic myocardial units.
Key Words: Myocardial syncytium • Dualism • Ventricular mechanics • Organ preservation
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1. Introduction
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Over the years, it has become accepted that the myocardium is arranged in the form of a syncytium. This, of course, is markedly different from the basic arrangement of skeletal muscles, each muscle having its own discrete origin and insertion. As an extension of the syncytial concept for the myocardium, until recently it was accepted that it is not possible to isolate discrete and systematic pathways within the intricate myocardial weave, made up of myocytes within a supporting spatial net of fibrous tissue. Despite this fact, nonetheless, several anatomic investigations revealed recognisable broad patterns of alignment of the bundles of myocardial fibres [1–3]. The specific anatomic arrangement achieves functional significance when attempts are made to explain the complex pattern of motion of the conical walls of the left ventricle. Over the years, this somewhat enigmatic states of affairs concerning myocardial architecture has been variously interpreted by physiologists [4,5], cardiologists [6], and recently, by cardiac surgeons [7,8]. The attention of the cardiac surgeons has largely been focussed by the advent of surgery designed to reduce the left ventricular radius as a potential means of rescuing the failing ventricle [9–11]. This itself is to be welcomed, since it is axiomatic that new progress in anatomy is most likely to occur when its problems include the study of function as well as of structure [12]. Some of the recent interpretations made by non-anatomists [14,15], however, have been based on concepts of structure that are incompatible with the existing morphological knowledge [3,13]. This is exemplified by a recent review published within the Journal [15], in which an entire hypothesis for surgical treatment was founded on the anatomical concept of the ‘ventricular myocardial band’, a concept which, in our opinion, has no foundation in anatomic fact. In this counterbalancing review, therefore, we provide a summary of our own understanding of the functional correlates of the known facts concerning the myocardial architecture of the ventricular mass. We submit that our alternative view of ventricular structure and function is in keeping with most of the known surgical approaches to organ preservation. As we will demonstrate, rather than functioning on the basis of a ‘unique myocardial band’[7,8,14,15], the ventricular mass is able to work harmoniously and efficiently because it is composed of an undefined number of wedge-shaped functional units, each of them exerting its individually programmed contribution to the global activity of the ventricular walls. In this setting, therefore, partial left ventriculectomy functions as a restorative procedure by withdrawing a number of functional myocardial units, albeit without impairing the entity of remaining units, which are then capable of supporting the new ventricle restored in both shape and size.
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2. Historical background
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In an attempt to elucidate the mechanism of the diastolic unfolding of the myocardium, Brachet, in 1816, introduced the concept of biphasic contraction [4]. He argued that a population of myocardial fibres running parallel to the endocardial and epicardial surfaces of the ventricles would contract during systole. He then opined that a second population of fibres, aligned radially, and intruding amongst the fibres extending parallel to the surface, or tangential fibres, would serve to cancel the systolic mural thickening, these fibres being activated during diastole so as to permit ventricular refilling. Despite the brilliance and simplicity of this biomechanical concept, as yet there has been no structural, nor functional, evidence forthcoming to support the concept.
Rather, at the turn of the twentieth century, Frank established the basis of modern cardiodynamics [5]. He postulated it was the performance of the left ventricle as a haemodynamic pump, in terms of pressure and stroke volume, which defined the mechanical work undertaken by the myocardium. When making this assumption, he commented: "So little is known about the orientation of the myocardial fibres that any determination of tension in individual fibres seems to be impossible ... The longitudinal direction of the myocardial fibres must generally be tangential with respect to the ventricular surface. If these fibres were in a normal direction to the wall surface, their shortening would induce ventricular dilation rather than a reduction in ventricular volume". Thus, Frank emphasised the contribution of the tangential fibres, but significantly, he did not himself reach the conclusion that all the myocardial fibres within the ventricular walls needed to be aligned in strictly tangential fashion. Rather, in accordance with the Laplacian approach to ventricular function [16], he emphasised the prevalence of a structure that acts in centripetal direction. His statement, however, has subsequently been interpreted to presume he meant that, during contraction, there were no other forces than those supporting ventricular ejection. This notion, carefully cherished during the late 20th century, reached its inexorable conclusion in the unfortunate concept of contractility [6]. This implicitly presumed the exclusive prevalence of a constrictive action of the myocardium in producing systolic emptying of the ventricle. It further presumed, in clandestine fashion, that the ventricular myocardium behaves in unitary fashion, contracting synchronously so that each region contributes to the intercavitary pressure to the same extent, and in essentially coincident time course. The innovative morphological findings of Streeter [12] were seized upon as providing the necessary structural background to underpin the physiological concept. Streeter had shown that, in selected areas from the left ventricle, the myocardial fibres were indeed aligned parallel to the epicardium, with only a minor proportion of the fibres extending transmurally. Streeter also claimed that the described arrangement was uniform throughout the various regions of the ventricular wall.
More recent data produced by Jouk and colleagues [13], derived from examination and reconstruction of the entirety of the ventricular mass without first introducing artefactual cuts or dissection, questions the validity of these assertions. The particular advantage of their method is that, by using polarized light, they have been able to compile data on the alignment of the myocardial fibres within cross sections of both ventricles. They were then able to reconstruct the overall arrangement by superimposing the data from sequential slices, also reducing the shrinkage artefact to a minimum.
Prior to the work of Jouk and colleagues, however, a fundamentally different concept had been advanced to account for the structure of the ventricular mass. Although never reproduced by independent investigators, and never, to the best of our knowledge passing the acid test of peer review, this concept now seems to be gaining increased recognition, judging from its acceptance by distinguished surgical commentators [7,8,17].
Thus, Torrent Guasp and his colleagues [14,15] have argued that, contrary to the large corpus of existing anatomical knowledge [1–3,18–21], the myocardium is arranged on the basis of a unique myocardial band. Like skeletal muscles, this band is held to have a discrete origin, at the aortic outflow, and an insertion at the subpulmonary infundibulum. Over the last 50 years, Torrent Guasp, by means of manual cleavage of hearts prepared by boiling and other techniques, has claimed to be able to unravel the ventricular myocardial mass in reproducible fashion, thus demonstrating the purported band-like continuum. The result is presented in appealing fashion, such that cardiac surgeons, searching for better understanding of the arrangement of the ventricular musculature in the organ on which they operate, now base large bodies of impending research on the new anatomic premise. In our opinion, the alleged ventricular myocardial band is produced artefactually. Furthermore, Torrent-Guasp and his supporters [14,15,17]signally fail to discuss the wealth of pre-existing anatomic evidence that militates against their concept, nor do they consider more recent evidence supporting the earlier anatomic studies [22].
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3. The basic arrangement of the myocardium
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Overall, the individual myocardial cells are orientated parallel to one another, having numerous lateral branches which pass out of a single group of cells at very acute angles [23,24]. On account of the numerous large clefts between the groups of cells, these spaces accommodating blood vessels and nerves, as well as strands of connective tissue, the groups of cells themselves are aggregated into larger fascicles, the orientation of these bundles being clearly recognizable to the naked eye once the epicardium is stripped from the ventricular surface (Fig. 1). These are the so-called fiber bundles, which intermingle constantly with adjacent bundles of myocardium within the overall fibrous matrix. No bundle is therefore single, but rather is part of a continuous network, which is a repetition on a larger scale of the arrangement of the individual myocytes seen under the microscope. The ‘stripping method’, long used by morphologists to study the architectural make-up [1–3,18–21], reveals the arrangement of these groups of fibres, considered to represent a fascicle, with a number of such fascicles joined side-by-side sufficient to be pulled off together as a sheet. It is generally agreed that the so-called fascicles and sheets are never fully separated from their neighbours. The orientation of the fascicles simply marks the major orientation of the myocytes. The overall longitudinal orientation is then presumed to represent the direction in which the muscle shortens during its contraction. Indeed, throughout the ventricular mass, muscular fascicles emerging from the one strand cross over to mingle with neighbouring, and then with remote, strands while changing progressively the major orientation of their long axis. When considered in the totality of the ventricular mass, therefore, these classical studies militate against any simple scheme arguing for uniformity of the global ventricular walls [8,15]. The classical studies also show that the direction of the fibres is constantly shifting as they penetrate the heart wall. Ultimately, the longitudinal orientation of the fibres on the epicardial surface of the heart can be at right angles to those that are immediately sub-endocardial. In stripping off the fibres, it can also be shown that successive bundles pass one under the other, so that they overlap much as do the shingles of a roof (Fig. 2). In this respect, it should be remembered that the intermingling of the populations of fibres is very much in support of Brachet's original concept of tangential and radial fibres [1], albeit that the intruding fibres are never directly radial.
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Fig. 1. This dissection of the inferior, diaphragmatic, aspect of a human heart was made simply by removing the epicardium. The yellow dotted line marks the inferior interventricular groove. The arrows show the broad tangential orientation of the bundles of myocardial fibres that form the epicardial surface of the ventricular mass.
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Fig. 2. In this preparation, the left ventricle of a human heart was dissected in step-wise fashion. This reveals the differing orientation of the bundles of myocardial fibres, shown by the arrows, that overlap as do the shingles of a roof as they intrude from the epicardial towards the endocardial layers of the wall. This arrangement is incompatible with the concept of a unique ventricular myocardial band.
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Although most morphologists have, of necessity, adopted a method of ‘stripping’ to display the orientation of the complicated meshwork of myocardial fibres, some have argued against its validity, since the technique is unequivocally, to greater or lesser extent, artefactual [18,19]. The consensus, nonetheless, favours the presence of an almost infinite number of individual planes of cleavage, comparable to collapsed, non-communicating hollow spaces in an artificial sponge, thus supporting the overall concept of a syncytium of muscle within a network of fibrous tissue [3,21]. Indeed, the very arrangement of the supporting fibrous matrix denies the existence of a continuous myocardial band. Were the ventricular mass arranged in the form described by Torrent-Guasp and his colleagues [14], then the supporting fibrous tissue would need to be arranged so as to divide the myocardium in a fashion comparable to the fascial sheaths that delimit the skeletal musculature within the limbs. Such fibrous sheaths supporting the ‘ventricular myocardial band’ have, to the best of our knowledge, never been described. This is hardly surprising, since they do not exist. Instead, the myocytes are set within a fibrous matrix, or epimysium, with complex struts and weaves. The known overall arrangement of collagenous epimysial support lends support neither to the concept of the ‘ventricular myocardial band’[14], nor to the concept of radial fibrous partitions as proposed by LeGrice and colleagues [25].
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4. The revisionist accounts of myocardial architecture
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Despite the existing anatomic evidence, Torrent-Guasp and his colleagues [14] have drawn the analogy between the hypothetical unique band and a pulley block. As a main feature of that purported setting, the rope in the pulley block is one strictly longitudinal entity, with a maximum of freedom of motion between the windings packed side-by-side or one above the other. The authors claim, therefore, that the presumed planes of cleavage that are purportedly followed when demonstrating the band by dissection, but surprisingly never demonstrated by histology, are preformed within the ventricular wall. They then argue that, in the beating heart, these planes of cleavage serve as the substrate for sliding. If true, then sliding along those planes should be so unimpeded that, in the dilated heart, constricting the right ventricular leg of the band by plication should produce shrinkage of the left ventricular cavity. In reality, Batista and his colleagues have shown, with right ventricular plication performed on hundreds of patients [9], that this inference, despite its appeal, is fundamentally wrong. More significantly, despite the existence of a considerable body of evidence supporting the notion of a syncytium, the supporters of the concept of the ventricular myocardial band have used it to argue against the concept of partial left ventriculectomy [8], ignoring the evidence from hundreds of patients who have been improved subsequent to surgery designed to reduce ventricular radius [9–11]. In addition, these supporters have designed allegedly complementary concepts of embryological development [26]. These equally revisionary concepts ignore totally the huge advances made in this field over the last decade [27,28]. The same authors, again seduced by the apparent attractiveness of the concept, have also sought to explain diastolic filling on the basis of perpetual motion [7,14], thus revealing their fundamental misunderstanding of the basic mechanisms of myocardial contraction.
At this point, we must consider also the recent suggestion that the tangentially arranged myocardial fibres are themselves sequestrated into a series of blocks, the blocks then being arranged in radial fashion. In this respect, Le Grice and colleagues [25] have suggested that discrete strands of fibrous tissue are interposed between the layers of myocardium, extending as sheaths from the epicardial to the endocardial surfaces of the ventricular wall. Although more in keeping with conventional knowledge concerning myocardial structure, this concept is again deficient in detail when set against the known variability in the overall alignment of the fascicles of myocardial fibres. This notion is also incompatible with the evidence concerning global ventricular mural structure, since we are unaware of any study that has demonstrated radial septation of the ventricular wall by connective tissue. We recognize that this concept might be essential for the development of a mathematical model [29]. Such models, nonetheless, if they are to be valid, must take into account all the available evidence. There is ample data from evaluations of regional ventricular function using various imaging methods [30–32], from the existing anatomic investigations [1–3,18–21], and from developmental studies [13], to show that the ventricular wall is far from a homogeneous entity simply divided by radial sheets of connective tissue.
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5. Structure conditions function of the ventricular myocardium
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For us, in accordance with the view of Grant [19], the ventricular musculature is truly an interwoven network of myocardial cells set in a matrix of supporting fibrous tissue. Rather than being formed on the basis of a skeletal muscle, the heart is a modified blood vessel, with each discrete myocardial cell attached to its neighbours in fashions of varying complexity. As we have illustrated, the bundles of individual fibres are themselves arranged in such a way that it is possible to discern a prevailing alignment that is parallel to the surfaces of the chambers. This array looks basically tangential, although almost all of those fibres oscillate in angulation against the strict tangential alignment with variance of about 12°. An important subset of fibres within the myocardial mass, however, is aligned in such a way that their longitudinal axis deviates from the tangential pattern. These fibres intrude into the ventricular wall to create oblique pathways (Fig. 3). This angle of intrusion also varies, and can be measured at up to 30° [22,23]. This population of intruding myocardial fibres has a measurable impact on ventricular dynamics. The steeper the angle of their intrusion, the more efficient those fibres counteract systolic thickening of the ventricular wall.
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Fig. 3. By use of a cylindrical twin-knife, the curve of which more or less follows the layered rotation of the fibres upon a radial axis, we succeeded in cutting the long axis of the oblique transmural fibres strictly parallel to the plane of section that intrude between the tangential fibres at the base of the left ventricular superior wall. By exposing them longitudinally, we can then demonstrate their exact alignment and continuous coupling. Towards the inner zones of the wall, the fibres are more inclined towards the endocardium than in the directly subepicardial zones, where they run almost tangentially. The end-result is a continuous myocardial strand coupling the epicardium to the endocardium. Such segmental variation in the orientation of the fibres is incompatible with the concept of a unique ventricular myocardial band. Note also that there is no angle of inclination reaching or exceeding 45°. Any deviation of transmission of contractile force close to radial is achieved only in consequence of the interference of the connective tissue, which is firmly interwoven between the myocytes.
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An overt dilating force, however, can only be generated when the erection of the fibres exceeds an angle of 45°, which up to now we have been unable to measure. The network of supporting connective tissue, nonetheless, which is firmly coupled to the myocardial syncytium, provides the necessary steep angulation towards the endocardium. Arranged in a quasi-rectangular net, with tangential, obliquely intruding, and radial components, the fibrous matrix serves as continuous chain for the transmission of forces, including that in the direction from the epicardium towards the endocardium.
Taking the components of myocardium and fibrous matrix as working in harmony, the presence of two opposite structural components provides a dualistic system that interacts during systolic thickening of the ventricular wall. And mural thickening is the driving principle of ventricular emptying. We have shown by direct measurements using needle force probes that the systolic forces produced by the fibres aligned in tangential fashion produce an unloading type of force [23]. This means that the force decreases continuously during ejection while the ventricle shrinks. The population of fibres intruding in oblique fashion, in contrast, produces an auxotonic type of force signal [23]. This force increases in power during thickening of the ventricular wall while the ventricle ejects (Fig. 4).
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Fig. 4. (Upper): Two types of force tracings are recorded in the left ventricular wall. When the force probe is coupled to fibres running parallel to the epicardium, an unloading type of signal (left) is recorded, whereas those fibres aligned more or less steeply inclined towards the endocardium engender an auxotonic type of signal (right). (Lower): Cardiodynamics during an acute loss in blood volume. The unloading type of force drops faster than does left ventricular pressure (LVP), yet parallels left ventricular shrinkage. In contrast, the auxotonic type of signal heralds a marked increase in force in the array of oblique transmural fibres.
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It is self-evident that the extent of shortening of the individual fibres is limited by their resistance to shorten [5,33]. Of particular importance is that the duration of contractile activity, is a function of the extent of shortening [34,35]. The less the freedom of a single fibre to shorten, the longer is its period of contractile activity. When considered in the context of the ventricular wall, the denser the interweave of tangential and obliquely intruding pathways, and the steeper the angle of intrusion, the more any wedge-shaped segment of the ventricular wall will be hindered in thickening, but the longer will be its contractile activity. Our measurements have revealed a negligible delay in onset of systolic mechanical activation. This is compatible with established knowledge in the propagation of excitation throughout the left ventricular wall. But we have also shown markedly disparate durations of segmental activity. By using magnetic resonance, we have documented segmental gradients in velocity and amplitude of thickening of the left ventricular walls associated with variations in the time course of contractile activity, thus providing direct evidence of the interference of the basic mechanism for contraction as described above [34–36] (Fig. 5). When assessed towards the base of the left ventricle, we found the amount of mural thickening to be greatest in the posterior and superior walls, slightly less in the inferior wall, and minimal in the basal septum. This pattern is so accentuated that it must be of some significance for the functioning of the ventricular pump. Presumably, it favours flow of blood from the ventricular inlet towards the subaortic outflow tract. The inward motion occurs in step-fashion, rather than at a constant speed. The wall moves very slowly at first, faster in the second phase, but more slowly again towards the end of ventricular ejection. This modulation in the velocity of mural thickening itself varies in timing and in amount between adjacent regions. The resulting possibilities to adjust the shape of the left ventricular cavity may well serve to minimize intracavitary resistance to flow, particularly in the small hypovolemic heart. In contrast, in the diseased heart characterised by a dilated cavity and a thinned wall, and therefore with a flattened oblique transmural netting, we have shown that intersegmental variations in mural motion are far less pronounced. From a functional standpoint, this is also understandable, since resistance to flow through the ventricular cavity is minimal in the dilated heart, and needs neither modulation nor control. It is worthy of note that this potential of the ventricular musculature to adjust its optimal mural motion is independent of any external regulatory mechanism, and is retained, therefore, when the organ is transplanted.
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Fig. 5. The figure reveals the half-cycle motion of the left ventricular base of a heart of a young healthy student, imaged by magnetic resonance tomography from end-diastole to the end of ejection. It shows minor inward motion of the epicardium, and pronounced centripetal motion of the endocardium. The ejection period was recorded in ten slices at constant time intervals. Note the marked differences in amount of wall thickening between adjacent segments. Even more significantly, note that the centripetal displacement of the endocardium is discontinuous, slow at the beginning, then rapid, and slow again towards the end of ejection. The variations in velocity also vary between the ventricular segments.
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6. The dualistic structure and function of the ventricular wall
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At first glance, the concept of dualism in terms of myocardial function seems to be counterproductive. To date, we have considered the concept only in relation to systole, or ventricular emptying. The faster, and the more complete, the degree of emptying, the more efficient the function of the ventricle seems to be. In reality, most bodily functions are based on some kind of dualism. The function of skeletal muscle, for example, is organized on a strictly dualistic, or antagonistic, basis. Here, the dualistic principle serves to restore the position of a joint, once it has been bent, and serves to stabilize the joint at any preferred angle of flexion, permitting the pattern of motion of the limb to be modulated both in time and in the amplitude of its excursion. This is achieved by the presence of discrete muscles that act against one another. Furthermore, measurement of the tension generated in the antagonizing pair of muscles can deliver information concerning the instantaneous position of the joint they operate.
Is there such an arrangement working within the ventricular mass? We believe that there is. Under conditions of rest, which is during ventricular diastole, the dualism in the normal myocardium can be considered to be in a state of equilibrium between the dilating and constricting forces. With the onset of contractile activity, the equilibrium is destabilized, and the constricting forces override the dilatory forces. At the end of ejection, a new equilibrium is established between opposing forces. Ejection ultimately terminates when the dilating forces reach the same level as the constricting forces. In a first attempt, the heart cycle seems to be conceptualised as the myocardium oscillating between the low-level diastolic state of equilibrium of forces at rest, and the high-level state of equilibrium of forces at the termination of ejection. In reality, we have found that, in the normal heart, the contractile force in the oblique intruding myocardial pathways consistently persists beyond the end-systolic drop in ventricular pressure (Fig. 4). This overhang in auxotonic force [34,35] might serve to give the first impetus to dilation. Further investigation is now needed to assess the quantitative impact of the oblique myocardial fibres. Interesting, from measurements on patients suffering from ischaemic heart disease, all being in advanced states of heart failure as assessed in the classification of the New York Heart Association, we know that the level of forces measured during systole in both the tangential and oblique intruding fibres is three times that we find in the canine and the porcine heart. Furthermore, the incidence of curves generated by auxotonic forces is at least doubled in those patients as compared to that found in healthy animals. This observation confirms the pivotal role of connective tissue, which accumulates in the ischaemic heart, and which is prone to enhance the deviation of tangential forces to the radial direction. The generation of myocardial force, nonetheless, was not impaired. Rather, with the increase in generation of auxotonic force, the intrinsic dualism was likely to be shifted towards a drop in hemodynamic efficiency.
We have also shown, nonetheless, by using needle force probes, that this dynamic equilibrium of forces acts at elevated diastolic and systolic levels in the setting of the hypertrophied compared to the normal heart [37]. This represents a harmonic shift of the equilibrium to a higher level of expenditure of energy. This is because the obliquity of the fibres running transmurally rather than tangentially increases due to the thickening of the wall, and there is a concomitant increase in connective tissue. Consequently, there is an increase in the forces opposing systolic mural thickening. Then, in a vicious cycle, both populations of myocardial fibres stimulate each other to hypertrophy. In this respect, ventricular hypertrophy in response to arterial hypertension, or aortic valvar stenosis, is classically understood as a compensatory mechanism designed to reduce the tension in single myocardial fibres by increasing their cross-sectional area. It has been inferred that the process of mural thickening continues until the tension in the individual fibres has returned to ‘control’ level [38,39]. In contrast to this inference, our direct measurements, made in fibres aligned both tangentially and transmurally, reveal that the hypertrophic heart continues to function with an elevated level of force in the individual myocardial fibres. Eventually, as hypertrophy continues, coronary perfusion becomes critically impaired, and consequently, there is continuing deposition of connective tissue. Once this situation has been reached, the vector of the dilating force comes to dominate the constricting force. On account of the resulting imbalance of the dynamic equilibrium, the initially constrictive hypertrophy turns into a dilated variant.
The concept of dualism has further implications. In hypovolemia, or in patients suffering from orthostatic disregulation, unlimited constrictive activity of the pump would prove disastrous, the wedge-shaped segments squeezing one another to an extent that the resulting forced remodeling of the myocardium would damage the interwoven microvascular pathways. This mechanism has been reported in terminal situations, when hypovolemia had erroneously been treated with pharmacological sympatho-adrenergic stimulation. In this setting, extensive subendocardial and intramural haemorrhages have been described at autopsy [40]. In those who survive such an emergency, arrhythmias may develop, caused by the persisting damage to the subendocardial tissues. Under normal circumstances, the heart is protected against such orthostatic challenges, typically associated with confined venous return when ventricular filling proves to be inadequate. By measuring forces in the two populations of fibres during experimental hypovolemia in pigs, we found, in compliance with Laplace's Law, a dramatic drop in the force recorded in the tangential population of fibres, but no drop, or more often an increase, in the force measured in the intruding transmural pathways (Fig. 4). This is still further evidence that the transmural fibres function under normal conditions so as to prevent undue systolic mural thickening, and thereby defend the ventricles against critical ventricular constriction. Hence, to a certain extent they might also be able to prevent mutual friction, as is seen in the emergency situation.
The concept of controlling mural thickness by the force of an oblique transmural population of myocardial fibres is applicable throughout the entirety of the cardiac cycle. Retaining the stability of segmental mural thickness is as important for the global shape of the heart as it is essential for ensuring that the mean equatorial diameter, and ventricular length, remain constant. It is hardly credible that global ventricular size and shape could remain constant if the biventricular myocardial mass was built exclusively of tangentially aligned muscle fibres like a ball of wool. It is equally incredible that the ventricular mass could be arranged in the form of a solitary band extending from the aorta to the pulmonary trunk. Rather, the shape of any individual heart, and its identically repeated motion perpetuated for considerably long periods of life, is preserved by a spatial contractile netting that functions by means of populations of oblique transmural fibres preventing the major population of those arrayed in tangential fashion from losing their appropriate alignment.
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7. Conclusions
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In our opinion, all the reproducible anatomic evidence currently available continues to support the concept of the myocardium being arranged in the form of a syncytial mesh. The evidence also indicates, however, that within this mesh there is a significant population of myocardial fibres orientated obliquely that intrude within the wall, rather than running exclusively tangential to the ventricular wall [13,22]. We have cited evidence to suggest that the function of the oblique transmural pathways, working in harmony with their supporting connective tissue, is partially to counteract the prevailing tangential component of the myocardial weave. We speculate that the inherent dualism thus produced serves to control segmental systolic mural thickening. A particular feature of the dualistic principle is that it is specific for the arrangement found in any given region of the ventricular wall. As the precise degree of the oblique transmural intrusion varies within the ventricular wall, so does the efficiency of control of regional mural thickening. It is our opinion, therefore, that the ventricular wall is composed of functional wedge-shaped transmural units, albeit not sequestrated by fibrous sheaths, but each contributing to ventricular ejection to an individually defined extent, and along an individually defined time scale within the cardiac cycle. This functional division of the ventricular wall into self-controlled functional units, which is readily explained by the known regional variations in the alignment of the myocardial fibres, guarantees that the typical pattern of motion of the individual heart is preserved subsequent to transplantation. More importantly, an extensive ventriculotomy, and even partial ventriculectomy, are well tolerated [10], provided that the remaining functional units have been shifted by the intervention into a geometric location that favours improved working conditions.
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Acknowledgments
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Our work is supported by the Deutsch Forschungsgemeinschaft, Karl und Lore Klein Stiftung, Ernst und Berta Grimmke Stiftung, Bundesministerium für Bildung und Forschung, and the British Heart Foundation.
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Top
Abstract
1. Introduction
