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Eur J Cardiothorac Surg 2006;29:S145-S149
© 2006 Elsevier Science NL

Review

Cardiac motion and fiber shortening: the whole and its parts

Gerald D. Buckberg a , b , * , Heinz Schelbert c , Aman Mahajan d

a Option on Bioengineering, California Institute of Technology, Pasadena, CA, United States
b Department of Surgery, David Geffen School of Medicine at UCLA, 10833 Le Conte Avenue, 62-258 CHS, Los Angeles, CA 90095, United States
c Department of Molecular and Medical Pharmacology, David Geffen School of Medicine at UCLA, Los Angeles, CA, United States
d Department of Anesthesiology, David Geffen School of Medicine at UCLA, Los Angeles, CA, United States

Received 17 February 2006; accepted 27 February 2006.

* Corresponding author. Address: Department of Surgery, David Geffen School of Medicine at UCLA, 10833 Le Conte Avenue, 62-258 CHS, Los Angeles, CA 90095, USA. Tel.: +1 310 206 1 27; fax: +1 310 8255895. (Email: gbuckberg{at}mednet.ucla.edu).


   Abstract
Top
 Abstract
1. Introduction
 2. Excitation and motion
 3. Comparison of radionuclide...
 4. Isometric systole and...
 5. Radionuclide ventriculography...
 6. Discrepancies and reality
 References
 
Radionuclide ventriculography findings in 24 subjects show that the ventricular blood pool motion goes from base to apex, a finding that contradicts the expectation that an apex to base relationship should exist, because excitation proceeds from apex to base. This discrepancy reflects a difference between motion caused by whole heart transmural action, and regional activity that does not require global movement. Confirmation of the radionuclide ventriculography findings was made from sonomicrometer crystals, echocardiography, and MRI that demonstrated early basal motion. During excitation, only the endocardial muscle is stimulated by the electrical impulse, but transmural motion that is needed for the endocardial motion that is detected by radionuclide ventriculography. Differences between the isometric and ejection phases are described, and there is discussion of how these findings relate to the myocardial band. The reality of twisting and downward motion of the heart observed during ejection only happens following transmural activation, a motion that exists far beyond the QRS electrical signal on the ECG.

Key Words: Radionuclide ventriculography • Echocardiography • Sonomicrometer crystals • MRI • Helical myocardial ventricular band • Excitation–contraction coupling


   1. Introduction
Top
 Abstract
 1. Introduction
2. Excitation and motion
 3. Comparison of radionuclide...
 4. Isometric systole and...
 5. Radionuclide ventriculography...
 6. Discrepancies and reality
 References
 
This review article is written to address the concern that has traditionally arisen after confrontation with the report of Ballester-Rodés et al. [1], whose radionuclide ventriculography data challenges the conventional expectation that the sequence of motion naturally follows the anticipated pathway of excitation–contraction coupling. Ballester-Rodés shows that global motion goes from base to apex, a finding that directly contradicts the anticipated apex to base motion pathway, since the apex and septum are the first to be electrically stimulated, while the base is the last area stimulated [2]. This reproducible motion pathway conformed to sequences predicted from the myocardial band in 24 humans, yet was so unexpected by reviewers of several journals, that 6 years elapsed before the report by Ballester-Rodés could be published. These actions are ascribed to the sequential motion of the helical ventricular myocardial band [1,3].

Motion of the whole heart stems from how its parts alter transmural movement, and this review will try to bring perspective into what the radionuclide ventriculography displays, define its limitations, and identify yardsticks from other imaging methodologies that positively interact with radionuclide ventriculography findings that document a motion sequence that confirms the expected sequential motion pathways of the myocardial band. Emphasis will be placed on the underlying principle that whole heart cardiac motion is linked to interaction of shortening sequences of its individual parts.


   2. Excitation and motion
Top
 Abstract
 1. Introduction
 2. Excitation and motion
3. Comparison of radionuclide...
 4. Isometric systole and...
 5. Radionuclide ventriculography...
 6. Discrepancies and reality
 References
 
In the normal heart, excitation–contraction coupling is responsible for visible motion of the ventricle on ventriculograms, echocardiogram, and MRI. The radionuclide ventriculography analysis displays how this movement alters ECG gated images of the radiolabeled left ventricular blood pool. This movement reflects a transmural cardiac action that causes a directional movement that reflects the interaction of the overlying ventricular wall muscular layers, whose motion likely proceeds along the major orientation of functional fibers. The linkage between excitation that originates in the cable pathways of the Purkinje system, and motion of the transmural myocytes excited by impulses generated via this nerve plexus, is not yet clarified. For example, the Purkinje fiber network is only connected to the inner part of the endocardial muscle, without macroscopic or microscopic evidence of nerve/muscle attachments within the midmyocardial and epicardial muscle layers.

The wave of electrical excitation is well known from studies by Sodi-Pallares and Calder [2], Scher et al. [4], and Hoffman et al. [5], which demonstrate that a wave front proceeds from endocardium to epicardium. This Purkinje network muscle connection has traditionally been interpreted to mean that the septum and apex, which are stimulated first, should have the first motion. However, the previous paper by Ballester-Rodés et al. [1,3] shows that the motion of the base precedes that of the septal region that gets the earliest stimulation. A major discrepancy with traditional knowledge now arises; this dilemma stems from a noninvasive radionuclide ventriculography test that codifies reproducible results in 24 humans to create findings that unequivocally questions conventional thinking. Does this finding indicate that the radionuclide ventriculography findings are incorrect, or is it possible that the endocardium may become stimulated to shorten earliest, yet fail to cause global or transmural cardiac shortening motion at the time of its activation?


   3. Comparison of radionuclide ventriculography and other measures of motion
Top
 Abstract
 1. Introduction
 2. Excitation and motion
 3. Comparison of radionuclide...
4. Isometric systole and...
 5. Radionuclide ventriculography...
 6. Discrepancies and reality
 References
 
There is a discrepancy between the radionuclide ventriculography findings that addresses how transmural ventricular movement creates changes in the gated intraventricular blood pool, and other tests that concentrate upon the focal events within the overlying muscle responsible for this motion. For example, sonomicrometer crystal tracings display very early endocardial shortening from individual fibers in direct contact with the free wall endocardium (Fig. 1 ) and thereby document that focal shortening of the endocardial region occurs at the same time that the base movement is evident by radionuclide ventriculography tracings. Furthermore, this early observation of endocardial activation is also evidenced by echocardiographic demonstration of early strain in fibers of the base and septum during the isometric phase of systole (Fig. 2 ). A concept must be developed to explain the difference between the capacities of individual fibers covering the endocardial surface to shorten in the absence of global transmural longitudinal shortening motion that exists during ejection.


Figure 1
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  		Fig. 1. Sonomicrometer crystal recording of systolic shortening in the descending (endocardial) and ascending (epicardial) fibers of the apical loop of the myocardial band. Crystals record maximal shortening when placed in this angulation of muscle fibers, and these tracings show shortening of the endocardial muscle during the interval that no motion is observed by radionuclide ventriculography.

 

Figure 2
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  		Fig. 2. Strain imaging of the upper septum adjacent to mitral annulus and lateral base. Arrow shows strain during the isometric contraction period that exists without longitudinal shortening.

 
This discrepancy is not a new problem. An example of this difference between shortening and motion is evident by recognizing that a stimulus can make the skin of an extremity narrow or shrink without having the arm or leg move because transmural fibers beneath the skin may not be stimulated at the same time as the skin is electrically activated. A parallel finding happens in the heart, since the Purkinje fibers show an electrical explosion by the QRS wave, and immediately stimulate the surface of the endocardium during excitation; ultrasonic crystals and echocardiographic strain tracings record such movement, yet the dominant transmural motion of longitudinal shortening during systolic ejection is delayed until global excitation coupling allows the reciprocal twisting seen by MRI [6,7] as the ventricle empties into the aorta.

The normal global cardiac motions of longitudinal shortening during twisting to eject and reciprocal twisting for longitudinal lengthening during suction occur during evolution of the T wave of repolarization on the electrocardiogram. Consequently, these global transmural shortening and lengthening movements exist far beyond the QRS of the EKG, a measurement that only conveys the action potential for initiation of electrical stimulation. In fact, the echocardiogram shows that longitudinal motion of the septum, which is immediately activated during the isometric phase, is to slightly lengthen, rather than shorten and move upward (Fig. 3 ). This is a surprising finding, since shortening would be expected if the endocardium is contracting, yet the opposite motion occurs. This initial motion implies that the focally, but not globally, contracting septum is pushed upward by its compression by the surrounding base of the heart, and simultaneously indicates there is no transmural septal contraction. This disparity addresses the contrast between shortening of individual fibers and visible movement of the transmural muscle mass that is observed by the previously listed imaging modalities. Longitudinal septal shortening occurs during the next phase of ejection caused by global or transmural contraction.


Figure 3
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  		Fig. 3. Esophageal four-chamber view with m-mode through upper septum (adjacent to mitral annulus). Arrows show slight upward septal displacement during the isovolumetric contraction period.

 

   4. Isometric systole and global motion
Top
 Abstract
 1. Introduction
 2. Excitation and motion
 3. Comparison of radionuclide...
 4. Isometric systole and...
5. Radionuclide ventriculography...
 6. Discrepancies and reality
 References
 
Documentation of the early endocardial shortening capacity that exists without global shortening motion is shown in Figs. 1 and 2 that demonstrate sonomicrometry and echocardiographic evidence of focal shortening and strain during the isometric phase. Of equal importance, there is no longitudinal septal or lateral wall shortening motion during the early systolic phase of isometric tension evident by ventriculogram, MRI, echocardiogram, or MRI recordings. However, basal motion is evident by the observations of Ballester-Rodés et al. [3] and shown in Fig. 4 that describes a motion that proceeds from the right to the left side of the radionuclide ventricular image.


Figure 4
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  		Fig. 4. Radionuclide venticulography showing motion (colored areas) of the base of the ventricular pool during isometric contraction, without evidence of motion of endocardium (central red area) on the ventricular pool in the center where septal motion is needed to show movement. Note the sequential activation from right to left sides of the ventricular pool.

 
This sequential activation or the base appears as a counterclockwise ‘cocking’ on MRI [6,7] and by regional implant measurements by Ingels et al. [8]. Of equal importance, there is a narrowing motion of the base of the heart during this isometric phase, as a 26% constriction of the mitral annulus is observed by echocardiography [9]. In this early isometric period, this movement exists in the base or basal loop, following a sequence that begins in the right segment, then goes to the left segment to define a wraparound compression of the central septum which fails to show the downward movement that occurs during systolic ejection. The radionuclide ventriculogram confirms this motion.

A discrepancy therefore exists between the presence of focal shortening by sonomicrometer endocardial crystals and early strain by noninvasive echocardiogram, and absence of global apical or septal shortening motion on radionuclide ventriculography scan recorded at the same time. An explanation of this dilemma must shed light on this difference, and this clarification is especially important because the radionuclide ventriculography and echocardiogram are noninvasive studies that provide valid readings. Furthermore, the crystal recordings, which are invasive, demonstrate a shortening between pairs of endocardial crystals when there is a complete absence of shortening motion within a septum that is surrounded by the compressive motion of the right and left segments of the basal loop.

That this sequential ‘cocking’ causes a right to left motion, is completely supported by the crystal recording on the right and left basal loop segments. Recent studies demonstrate that shortening initiates in the right segment and starts 0.10 ms later in the left segment [10].

These observations correspond to the movement sequences defined by Ballester-Rodés in his report. The counterclockwise motion during the isometric phase shown by MRI [6] suggests the earlier shortening right side pulls the later shortening left side to cause this motion.


   5. Radionuclide ventriculography analysis and limitations
Top
 Abstract
 1. Introduction
 2. Excitation and motion
 3. Comparison of radionuclide...
 4. Isometric systole and...
 5. Radionuclide ventriculography...
6. Discrepancies and reality
 References
 
Insight into this discrepancy between radionuclide ventriculography records and conventional thinking is drawn from understanding the information provided by radionuclide ventriculography analysis, its limitations, and surveying why differences between regional shortening and global motion do not invalidate the radionuclide ventriculography recordings.

One of several possible explanations of this dilemma relates to a possible signal to noise difference between the background activity within the recorder and amount of early endocardial muscle stimulation that exists when the Purkinje fibers directly touch the endocardial muscle in a nerve myocyte connection. No motion signal would appear if there is equality of background activity and the new activity exists only in this thin endocardial segment. This mismatch was previously encountered when radioactive microspheres were used to measure regional blood flow [11]. Appearance analysis showed that a minimum of 400 microspheres must be present to accurately record the flow measurement. Failure to deliver at least this quantity of microspheres resulted in a major incompatibility between background noise and available signal, so that no accurate flow recordings could be achieved if <400 microspheres were present in regional tissue.

Background noise diminishes the fidelity of tracking ventricular wall motion and its temporal sequence from the gated radionuclide ventriculograms. Effects of background noise in the Ballester-Rodés study would seem to be relatively small in view of the high counts statistics of the radionuclide ventriculograms. More important for resolving differences between Ballester-Rodés’ findings and previous observations on the activation sequence of the left ventricular myocardium is that phase analysis of equilibrium radionuclide ventriculograms only tracks motion. The narrowing of the mitral annulus during the isometric phase [9] shows that there is motion on the ventricular blood pool to support basal motion during this cardiac cycle phase.

Spatial differences may also exist, so that the endocardial excitation that renders regional shortening by sonomicrometer crystals may not be associated with transmural cardiac movement to shorten; this activity requires the entire septal movement observed during ejection. A zone of no activity of intraventricular blood adjacent to the septum was observed by Ballester-Rodés’ report in this isometric phase, implying that this region was not exerting transmural motion. This finding is supported by the echo record of no downward septal motion in the isometric interval.

Wall motion analysis by radionuclide ventriculography entails the acquisition of ECG gated images of the radiolabeled left ventricular blood pool and formatting of the sequential gated image frames recorded over the length of an average cardiac cycle, into a 64 x 64 digital image matrix. Changes in counts, and thus in radioactivity in each image element or pixel during the cardiac cycle reflect proportionate changes in regional blood volume. Decreases in counts following excitation in pixels located at the border as well as at the center of the ventricular blood pool image correspond to regional decreases in ventricular blood volume and, therefore reflect regional systolic wall motion. During isometric contraction, these regional changes result in cardiac motion since narrowing of the mitral valve occurs during this interval [9]. Conversely, there was no activity observed in the ventricular pool adjacent to the septum (Fig. 4) indicating no regional transmural wall motion. This observation is confirmed by echocardiogram, which thereby supports the radionuclide ventriculography observations. Thus, if the septum has focal motion but no movement, there is no visible effect on the blood pool image and thus on phase analysis recordings.

Regional septal systolic wall motion is expected during ejection, and longitudinal shortening would occur during contraction of the endocardium, together with the entire ventricular wall. The radionuclide ventriculogram tracing in Fig. 5 shows motion in the region occupied by the septum as its endocardium touches the ventricular pool during this ejection interval, thereby confirming accurate recording of such septal movement.


Figure 5
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  		Fig. 5. Radionuclide ventriculography during ejection showing movement in the central (colored) region of the ventricular pool, with loss of motion in the basal (lateral blue) areas that were active during the isometric phase.

 

   6. Discrepancies and reality
Top
 Abstract
 1. Introduction
 2. Excitation and motion
 3. Comparison of radionuclide...
 4. Isometric systole and...
 5. Radionuclide ventriculography...
 6. Discrepancies and reality
References
 
Differences between what is expected and shown do not mean there are errors in prior concepts, but rather reflect the importance of coordination of information from several sources to find reality. The radionuclide ventriculography scan described by Ballester-Rodés defines a sequential motion of the base of the heart on the underlying pool of blood in the ventricular cavity during the isometric phase of systole. This motion is consistent with sonomicrometer tracings of the right and left segments of the basal loop of the myocardial band, corresponds to the narrowing of the mitral valve during this interval by echocardiogram, as well as echocardiographic measurement of early strain in this upper region of the base of the heart. Consequently, other imaging modalities show compression of the intraventricular blood pool during isometric systole, and confirm that the base has motion before the apex. The limitation of the radionuclide ventriculography recordings is recognition that this test tracks cardiac motion, an activity that requires transmural movement.

Failure to detect ongoing early motion of the endocardium, demonstrated by sonomicrometer tracings and echocardiographic strain pattern, simply reflects an absence of transmural downward motion of the free lateral wall and septum during the isometric phase of systole. The individual parts of the endocardium are developing shortening and strain by sonomicrometer and echo tracings, but there is the delayed twisting motion of the septum to convey longitudinal shortening during systole; this movement requires transmural activation of the entire ventricular wall, a finding that is not part of the motion action displayed by radionuclide ventriculography recordings, because it did not occur during the isometric phase.

The discrepancy is to expect early endocardial electrical activation to become translated into transmural motion. This action of the free wall and septum requires transmural motion rather than only shortening of endocardial fibers that have direct contact with the Purkinje system. The reality of twisting and downward motion of the heart observed during ejection happens when such transmural activation occurs, an event that exists far beyond the QRS of the electrical signal of the ECG.


   References
Top
 Abstract
 1. Introduction
 2. Excitation and motion
 3. Comparison of radionuclide...
 4. Isometric systole and...
 5. Radionuclide ventriculography...
 6. Discrepancies and reality
 References
 

  1. Ballester-Rodés M, Flotats A, Torrent-Guasp F, Carrio-Gasset I, Ballester-Alomar M, Carreras F, Ferreira A, Narula J. The sequence of regional ventricular motion. Eur J Cardiothorac Surg 2006;29S:S139-S144.[Abstract/Free Full Text]
  2. Sodi-Pallares D, Calder RM. New bases of electrocardiography. St. Louis: CV Mosby Co.; 1956.
  3. Ballester-Rodés M, Flotats A, Torrent-Guasp F, Ballester-Alomar M, Carreras F, Ferreira A, Narula J. Base-to-apex ventricular activation: Fourier studies in 29 normal individuals. Eur J Nucl Med Mol Imaging 2005;32(12):1481-1483.[Medline]
  4. Scher AM, Rodriguez MI, Liikane J, Young AC. The mechanism of atrioventricular conduction. Circ Res 1959;7(1):54-61.[Abstract/Free Full Text]
  5. Hoffman BF, Cranefield PF, Stuckey JH, Amer NS, Cappelletti R, Domingo RT. Direct measurement of conduction velocity in in situ specialized conducting system of mammalian heart. Proc Soc Exp Biol Med 1959;102:55-57.[CrossRef][Medline]
  6. Lorenz CH, Pastorek JS, Bundy JM. Delineation of normal human left ventricular twist throughout systole by tagged cine. J Cardiovasc Magn Reson 2000;2(2):97-108.[Medline]
  7. Jung B, Markl M, Foll D, Buckberg GD, Hennig J. Investigating myocardial motion by MRI using tissue phase mapping. Eur J Cardiothorac Surg 2006;29S:S150-S157.[Abstract/Free Full Text]
  8. Ingels NB, Hansen D, Daughters II GT, Stinson EB, Alderman E, Miller DC. Relation between longitudinal, circumferential, and oblique shortening and torsional deformation in the left ventricle of the transplanted human heart. Cir Res 1989;64:915-927.[Abstract/Free Full Text]
  9. Ormiston JA, Shah PM, Tei C, Wong M. Size and motion of the mitral valve annulus in man. I. A two-dimentional echocardiographic method and findings in normal subjects. Circulation 1981;64(4):113-120.[Abstract/Free Full Text]
  10. Castella M, Buckberg GD, Saleh S, Gharib M. Structure function interface with sequential shortening of basal and apical components of the myocardial band. Eur J Cardiothorac Surg 2005;27(6):980-987.[Abstract/Free Full Text]
  11. Buckberg GD, Luck JC, Payne DB, Hoffman JIE, Archie JP, Fixler DE. Some sources of error in measuring regional blood flow with radioactive microspheres. J Appl Physiol 1971;31:598-615.[Free Full Text]



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