13.1 Historical Perspective

Thus, for Galen, both systole and diastole are active processes brought about by different sets of muscles. Diastole clearly played the superior role because the dilating ventricles “attracted” blood by suction, much like the blacksmith’s bellows or a loadstone, contributing to forward flow of the blood. This view was refuted by Harvey who regarded systole as active and diastole as a purely passive process (cf. Sect. 22.​1).

Resemblance between helical forms and flows in nature and the myocardial structure was also known to the Renaissance anatomists and has been a subject of fascination to researchers ever since. Leonardo da Vinci believed that the heart is a “vessel made of dense muscle” and proposed that closure of the aortic valves results from vortical flow in the sinuses of Valsalva [7]. Leonardo may have been the first to describe the difference between the rotational and irrotational vortex, a key concept of circulation in hydrodynamics [8].¹ Leonardo was also the first to observe shortening of the long axis of the heart during systole [9]. Richard Lower published the first detailed drawings of the separate myocardial muscular layers—overlapping much like rings of an onion—and drew attention to the fact that the endocardium and epicardium meet directly at the apex which is free of muscular elements [10]. In 1728, Senac demonstrated that the myocardial fibers are organized in spiral, three-dimensional arrangement, a finding repeatedly confirmed by investigators over the next 200 years (for review see [11–13]).

Among the numerous available studies of anatomical dissections of the heart, the morphological descriptions and superb illustrations by Scottish anatomist J. Bell Pettigrew stand out and continue to be quoted as a classic in the field [3]. In his monumental work “Design in Nature” published in1908, Pettigrew draw attention to the ubiquitous presence of spiral forms in all kingdoms of nature and suggested that understanding of the common architectural plan of “perplexing” arrangement of myocardial fibers is a “Gordian knot” of anatomy holding the key to its function [14]. Pettigrew maintained that the heart is a transformed blood vessel where the thin-walled atria represent the continuation of the great veins, while the thick-walled ventricles and aortic and pulmonary outflow tracts mark the beginning of the arteries. He further argued that, unlike voluntary muscles, myocardial fibers have neither origin nor insertion, but form continuous spirals (lemniscates) between the apex and the base and, moreover, exhibit spontaneous rhythmical movements of the syncytium.

Using an “innovative” tissue preparation technique (by stuffing sheep hearts with dry oatmeal and boiling them for 4–6 h, a method he called “a truly Scottish procedure”) [15] and laborious dissections, Pettigrew demonstrated that the myocardial wall consists of seven layers which “overlap externally and internally and equilibrate each other according to mathematical law” [3, 14] (Fig. 13.1). The outermost layer runs from left to right obliquely from the base to the apex, while the second and the third layers assume a more obtuse angle as they sink deeper into the wall. Fibers of the fourth layer define the mid-wall and run like a circular band horizontally around the ventricle. Finally, fibers of the three inner layers spiral in the opposite directions, from apex to base. The point of inflection of the inner and outer helical system occurs at the apex forming a characteristic whorl or “vortex cordis” (Fig. 13.2). Pettigrew’s remarkable observations have struck a note with several generations of investigators; here, for example, is a quote by Pasipoularides:

The spiraling and looping pattern of myocardial fibers, including the vortex cordis, is a reflection of intracardiac blood movements. In the heart, form and movement unite in a rhythmical process in space and time: the organ, a form in space, is simultaneously a movement in time…the movement of the cardiac walls is a physical replication of the creative fluid flow movements which they enclose. [16]

Other, perhaps less phenomenologically oriented, researchers have found it difficult to reproduce Pettigrew’s ingenious dissections and morphological descriptions of discrete muscular layers within the ventricular walls. The preconceived notion that the heart is an organ of blood propulsion has compelled some to emphasize the elements in myocardial architecture which would primarily make it into an efficient pump. (Reviewed by Brecher and Galletti [18].) Carl Ludwig introduced the concept of a muscular cylinder as the principal structure of the left ventricle enveloped by endocardial and epicardial layers crossing at the right angles of its longitudinal axis in the form of an X [19].This model was further refined by von Krehl who named the circular fibers “Triebwerkzeug,” or “propelling tool,” in literal translation from the German [20], technically known as the “actuating fibers.” The concept gained further momentum with the work of MacCallum who stressed the crucial role of the cardiac “fibrous skeleton” [21]. According to MacCallum’s anatomical model, four interconnected fibrous rings at the orifices of the great vessels and the AV orifices serve as attachments of cardiac valves, and also as points of insertion for ventricular muscles, of which several groups had been identified by functional anatomists at the time, such as the “bulbo-spiral” and “sino-spiral” tracts described by Mall [22]. It should be noted parenthetically that during the time, a functional similarity between the skeletal muscle and the myocardium was emphatically supported by Frank [23] and Starling [24, 25] and that seminal experiments were performed on the isolated heart preparations culminating in Starling’s formulation of the “law of the heart” [26] (see Sect. 16.​1). Subsequent work demonstrated that in comparison to the skeletal muscle, the myocardium is capable of developing only a fraction of active tension (2–5 kg/cm² vs. 200 g/cm² of cross section of the muscle) [27]. Frank’s interpretation of myocardial dynamics nevertheless became universally accepted [28, 29].

The pendulum of research into myocardial architecture swung in the other direction when it became apparent, in due course, that beyond general orientation of the myocardial fibers, identification of explicit muscular layers is not possible by histological techniques [30]. Grant maintained that the syncytial nature of the myocardial fibers, with multiple connections and branching, is beyond the laws of plane geometry applied by Lower and his successors who, by means of anatomical preparations, frequently “created the planes they sought” [31]. Streeter and Bassett were unable to find evidence of specific muscle layers, suggested that the myocardium be described as a “continuum” rather than consisting of discrete muscle bundles, and performed the first quantitative measurements of muscle fiber orientation within the heart wall [32]. Researchers from the same group subsequently demonstrated that the overall alignment of myocardial fiber aggregates varies up to 180° (with respect to ventricular equator) within different depths of ventricular wall [33] (Fig. 13.3).

On account of marked uniformity of ventricular wall architecture, Hunter and Smaill introduced the concept of “continuum approach” and proposed that methods of continuum mechanics provide a suitable theoretical framework for the analysis of the complex interaction between mechanical, metabolic, and electrical functions of the heart [35]. Greenbaum and coworkers confirmed major variation of myocardial fiber orientation within the myocardial wall and warned against regarding the ventricle as having a simple geometrical shape or a uniform structure [13]. It is recognized today that every part of ventricular wall possesses a unique architecture, and while it is still possible to identify groups of myocytes contained within perimysial lamellae (secondary structure), it is no longer feasible to distinguish discrete anatomical layers (tertiary arrangement) [34] (Fig. 13.4).

An important contribution to the understanding of the myocardial fiber architecture has been the use of diffusion tensor magnetic resonance imaging (DTMRI), a novel technique which enables visual “tracking” of the aggregated myocyte chains within ventricular walls. While DTMRI studies cannot confirm or exclude the presence of discrete myocardial sheets, they have independently verified previous histological findings. Importantly, they have corroborated the remarkable three-dimensional helical fiber patterns which, according to Smerup et al., “are entirely compatible with the illustrations produced by Pettigrew 150 years ago following careful dissection of the ventricular mass” [36] (Fig. 13.5).

Unlike DTMRI, high-resolution MRI and micro-computed tomography can provide a detailed morphological analysis of cardiac micro-anatomy such as orientation of individual myocytes and of the higher order lamellar units within the myocardial wall [37] (Fig. 13.6). Directional arrangement of the myofibers within the ventricular wall and their contraction sequence within a single cardiac cycle have been further confirmed by tissue Doppler imaging and by sonomicrometry, a method of implanting miniature ultrasound crystals directly on the ventricular wall [38].

13.2 Models of Ventricular Structure and Function

As noted by Lunkenheimer and coworkers [29], Frank’s interest in showing that the heart’s filling and subsequent contraction are determined by venous pressure (preload) and that the forces released during ventricular contraction are solely of constrictive nature was an oversimplification that became generally accepted among clinicians and physiologists, in spite of ample histo-anatomical evidence (as reviewed above) that points to the contrary. Thus, the clinicians working within the “conventional” paradigm of preload, afterload, and contractility essentially view the “ventricular pump” as a homogenous unit generating centripetal forces exclusively during systolic contraction (Fig. 13.7). See Wiggers diagram for the sequence of pressure and volume events during cardiac cycle, Fig. 13.8

To address this deficiency, two additional but contrasting models have evolved over the past several years among the basic scientists and clinicians seeking to explain the movements of ventricular walls in the light of existing research. The first is the ventricular myocardial band (VMB) conceived by Francisco Torrent-Guasp, and the second, the “antagonistic force” model developed by Paul Lunkenheimer (see below).

13.2.1 Ventricular Myocardial Band

The concept of VMB introduced by Torrent-Guasp presents a significant deviation from the classical model presented above and a notable attempt to portray the heart not only as a propulsion, but as a “pressure-suction pump” [11, 40]. According to its adherents, the model optimally explains the mechanics of sequential myocardial contraction, including torsion and untwisting, and presents a “unifying approach to causative architectural mechanisms affecting the heart” [41]. It arose on the premise that the limited shortening capacity of myocardial sarcomeres (in the range of 10–20%) is inadequate to account for ventricular ejection fraction of up to 60%. Similarly, the thickening of left ventricular wall of up to 30% can only be explained with additional systolic “augmentation” [11]. Finally, rapid ventricular filling at the end of diastole, frequently accompanied by negative pressure (i.e. suction) cannot be explained solely by elastic diastolic recoil of the ventricle. To affect these changes, according to Torrent-Guasp and collaborators, participation of an additional contractile force is needed. This is as afforded by the VMB.

The topology of the model is based on a unique dissection method by which the heart is unfolded into a single muscular band extending between aorta and pulmonary artery (Fig. 13.9). Accordingly, the architectural plan of the ventricles is formed by a pair of counter-directional (apical and basal) loops, each consisting of two segments. Fibers of the basal loop, forming the free wall of the right ventricle and the basal portion of the left ventricle, course predominantly in circumferential fashion. On the contrary, the two segments of the apical loop (descending and ascending) run mainly in the vertical direction (parallel to long axis of the left ventricle) and cross at about 90° [11]. Functionally, the apical portion of the VMB is the principal force-generator acting in the manner of twisting and untwisting of the ventricular cone (e.g., wringing of a wet towel), without any net movement of the apex. Contraction of the descending fibers brings about systolic ejection through simultaneous descent of the ventricular base, counter-clockwise rotation, and LV cavity reduction. Ventricular filling, on the other hand, is brought about by the contraction of the ascending fibers of the ventricular loop, with clockwise rotation, ascent, and cavity augmentation (Fig 13.9b). Diastolic chamber elongation, affected by contraction of the ascending segment, is a unique, but controversial element of the Torrent-Guasp model [42–44]. It results in ventricular elongation, clockwise rotation, and an increase in size of the AV valve orifices which supposedly augments venous return by the generation of (active) ventricular diastolic suction, referred to as vis á fronte by physicians of antiquity (see Sect. 15.​2). Let us mention parenthetically that Galen’s concept of “force from the front,” pulling the blood toward the heart, was still referred to until the 1960s, before the almost universal acceptance of Guyton’s venous return model [45, 46] (see Sect. 14.​3). This is confirmed by magnetic resonance velocity mapping of the ventricular base which demonstrates that the valve plane ascends (in the direction opposite to the apex) 26–64 ms before the onset of flow through the mitral valve [47]. The issue is far from resolved, and as mentioned, several researchers have noted that rapid ventricular filling cannot be explained solely by passive elastic recoil of the expanding ventricle (see [11, 48]). Rushmer et al. proposed, for example, that ventricular ejection is brought about by the transverse constrictor muscle (Krehl’s actuating fibers, referred to above) and that simultaneous contraction of the helical inner and outer muscular layers oppose each other, only to generate “stored potential energy” which, in turn, is responsible for diastolic recoil (cf. Fig. 13.2b) [49]. Thus, the concept of VMB provides an anatomical and physiological basis for active ventricular systolic and diastolic myocardial cycling which, according to the authors, can be represented by workings of an internal combustion engine, where the blood represents the stationary component (i.e., the piston) and the ventricle, the cylinder. During the isovolumic phase of the ventricular contraction, the blood serves as a fulcrum, e.g., a “hemoskeleton”, for the apical elongation of the ventricle (cylinder) [11].

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