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Cardiac Mechanics RevisitedThe Relationship of Cardiac Architecture to Ventricular Function
Gerald Buckberg, MD; Julien I.E. Hoffman, MD; Aman Mahajan, MD;Saleh Saleh, MD; Cecil Coghlan, MD
Abstract—The keynote to understanding cardiac function is recognizing the underlying architecture responsible for thecontractile mechanisms that produce the narrowing, shortening, lengthening, widening, and twisting disclosed byechocardiographic and magnetic resonance technology. Despite background knowledge of a spiral clockwise andcounterclockwise arrangement of muscle fibers, issues about the exact architecture, interrelationships, and function ofthe different sets of muscle fibers remain to be resolved. This report (1) details observed patterns of cardiac dynamicdirectional and twisting motions via multiple imaging sources; (2) summarizes the deficiencies of correlations betweenventricular function and known ventricular muscle architecture; (3) correlates known cardiac motions with thefunctional anatomy within the helical ventricular myocardial band; and (4) defines an innovative muscular systolicmechanism that challenges the previously described concept of “isovolumic relaxation.” This new knowledge may opennew doors to treating heart failure due to diastolic dysfunction. (Circulation. 2008;118:2571-2587.)
Congestive heart failure, due usually to both left ventric-ular (LV) and right ventricular failure, is an increasing
problem worldwide. In the United States, �5 million patientssuffer from congestive heart failure, and each year �500 000new patients develop the condition.1 Originally, this syn-drome was believed to be due to failure of the LV to pumpblood efficiently (ie, systolic ventricular failure). More re-cently, emphasis has been placed on diastolic ventricularfailure, in which systolic function appears to be normal butdiastolic ventricular function is impaired.2–4 Diastolic dys-function, in fact, may be the cause of congestive heart failurein up to 50% of these patients.5,6 We have had treatment forsystolic ventricular failure for many years, even if it isimperfect; at present, however, no agreement has beenreached about the best ways of treating diastolic ventricularfailure. To develop better treatments for congestive heartfailure, both systolic and diastolic, we need first to understandthe basic physiology of normal and abnormal ventricularcontraction and relaxation.
The heart is a muscular pump that supplies blood to thebody. This goal is achieved by electric excitation that pro-duces sequential ventricular emptying and filling. Figure 1ademonstrates the physiological sequence of ventricular func-tion: an isovolumic contraction phase to develop preejectiontension, ejection, a postejection isovolumic phase, and thenrapid and slow periods for filling. LV volume decreases
rapidly early in systole and slowly thereafter, correspondingto the rapid early acceleration in the flow curve. The volumethen increases rapidly in early filling and more slowly duringlate filling.
The information shown in Figure 1a is still correct, but it isonly slightly more informative than the concept of WilliamHarvey, who concluded, after dissecting cadaver hearts, thatthe heart squeezed by constriction to eject and dilatedpassively to fill. This accepted view of cardiac function has 3main shortcomings.
1. It implicitly assumes that LV muscle is homogeneous, withall of its fibers contracting or relaxing simultaneously. Thismisconception stems from the ways in which we acquiredinformation about LV function in the past. These were byangiography or echocardiography, which are 2-dimensionaltechniques, and, until recently, all we could see was a globalchange in shape of the cavity and the surrounding muscle.
2. The standard concepts of ventricular function made noattempt to consider the architecture of the LV with itscomplicated array of fiber angles and, in particular, thefunction of the spiral muscle bands that form a partialfigure-8 loop at the apex.
3. The 2-dimensional techniques previously used preventedus from evaluating the twisting phenomena observed dur-ing emptying and filling of the beating heart (Movie I in theonline-only Data Supplement).7 Ventricular twisting can be
From the Departments of Cardiothoracic Surgery (G.B.), Medicine (S.S.), and Anesthesiology (A.M.), David Geffen School of Medicine at UCLA,Los Angeles, Calif; Department of Pediatrics and Cardiovascular Research Institute, University of California at San Francisco, San Francisco (J.I.E.H.);and Division of Cardiovascular Diseases, University of Alabama at Birmingham, Birmingham (C.C.).
The online-only Data Supplement is available with this article at http://circ.ahajournals.org/cgi/content/full/118/24/2571/DC1.Correspondence to Gerald D. Buckberg, MD, Department of Cardiothoracic Surgery, David Geffen School of Medicine at UCLA, 10833 Le Conte Ave,
explained by fibers that form a figure-8 clockwise andcounterclockwise spiral muscle configuration. This muscleconfiguration was previously described by a spectrum ofanatomists8 and is currently supported by tensor magneticresonance imaging (MRI)9 but until recently has not beensubjected to detailed anatomic–physiological correlations.Current interest in the role of the spiral fibers has ledinvestigators to ignore the role of the dominant mass ofcircumferential fibers,10,11 and one of our objectives is toexamine the interactions among these sets of fibers.
All of these deficits are beginning to be resolved by theintroduction of newer imaging techniques such as high-
resolution echocardiography to show regional strains,10,12
magnetic resonance myocardial tagging13 and speckle track-ing by echocardiography to quantify torsion,11 and diffusiontensor MRI9 to photograph natural global motion and dem-onstrate movements that develop from the underlying com-plex LV architecture.
This report relates function to the underlying preciselydescribed functional muscular anatomy that causes the ven-tricular directional motions of narrowing, shortening, length-ening, widening, and twisting (Figures 1b, 1c, and 2), therebyproviding structural explanations for each of these contractilesequences.
Figure 1. a, Currently accepted time frames of systole and diastole, with measurements of intravascular pressure in the aorta, LV, leftatrium (LA), and LV volume, together with their impact on the mitral and aortic valves. Aortic flow occurs between the 2 intervals thatdefine ejection. The physiological phases of cardiac cycle that include isovolumic contraction, ejection, isovolumic “relaxation” (to bequestioned in this report), rapid and slow filling, and atrial contraction are shown. b, Two-dimensional images of the LV in a longitudinalview that shows the normal sequence of narrowing, shortening, lengthening, and widening of the ventricular cavity during a normal car-diac cycle. Images were obtained by epicardial imaging in an open-chest porcine preparation. The phases of the cardiac cycle includeend-diastolic state (bottom right), isometric phase (top left), ejection (top right), and isovolumic phase (bottom left). The broken-linemarkers are within the ventricular cavity and define the transverse (between the mid endocardial walls) and the longitudinal (from apicalendocardium to a line across the mitral annulus) dimensions. Muscle thickness is shown by the dark area adjacent to these intracavitydimensional lines. The pale color is the cavity. The predominant changes exist with muscular thickening that narrows and widens thecavity rather than the external wall dimensional changes. Note progressive muscular thickening (evaluated by wider distance betweenepicardial and endocardial lines as myocardial mass narrows and shortens for ejection), together with maintained thickness as heartlengthens during the rapid filling phase before substantial widening. c, Twist of the heart: clockwise (below baseline) and counterclock-wise (above baseline) motions of the base and apex, respectively, during the cardiac ejection and filling periods are represented inrotational degrees with the use of speckle tracking with marker placed at the LV endocardial surface (Echopac PC V 6, GE Healthcare,Milwaukee, Wis). The relationships between the initial uniform and then reciprocal twisting motions of the base and apex during thepreejection, ejection, and rapid and slow filling periods are explained in the text.
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Basic Ventricular Function UpdatedThe observed functional patterns (Figure 2a) include an initialglobal counterclockwise twist (as seen looking toward theheart from the apex) and attendant narrowing or “cocking” in
the isovolumic contraction phase before ejection,14,15 fol-lowed by continuing counterclockwise twisting of the cardiacapex (lower third of the heart) and clockwise twisting of thebase (upper third of the heart as seen by MRI and speckletracking echocardiography) as the ventricle longitudinallyshortens during the ejection phase, and then a vigorous apicaluntwisting in the opposite direction as the ventricle lengthensand slightly widens during an isovolumic phase interval whenno blood enters or leaves the ventricular chamber.12,16–18 Thisapical untwisting motion is associated with a rapid ventricularpressure decay (tau),16 quantifiable rate of untwisting13 andcontinues into the rapid filling interval,7 when suction occurstogether with a recordable intraventricular pressure gradi-ent11,12 until finally a phase of relaxation occurs duringdiastole, when heart widening continues by slower filling,before the atrium contracts prior to the next organized beat.
Cardiac motion begins in the base to narrow and elongatethe ventricular chamber before longitudinal shortening devel-ops,19,20 a sequence that contradicts the presumed apex-to-base contractile pattern inferred from studies on the anatomicpath of the Purkinje system.10 Under these conditions, ven-tricular cavity elongation occurs (ie, mitral valve billow-ing19), yet muscle contraction causes this effect. The observeddifferentiation between initial narrowing and later shorteningopposes the concept of synchronous contraction21,22 with auniform or concomitant strain field across the ventricularwall23,24 because inhomogeneous strain (deformation) devel-ops during contractile wave propagation.25 Until now, eval-uation of regional strain during global ventricular motion waslimited by insufficient spatial and temporal resolution ofimaging technology.
This report will describe mechanics with imaging tools thatamplify dynamic function, portray areas where gaps exist inexplanations from conventional causative concepts, surveymodels of structure and define their advantages and limita-tions, correlate a mechanical structure/function sequence thatis linked to known elements of a double helical cardiacconfiguration that coexists with the circumferential and lon-gitudinal fiber arrangement described in all cardiac anatomicmodels, relate this structure to movement based on multipleimaging modalities, and outline its implications.
Newer Aspects of Ventricular FunctionEarly studies on ventricular torsion with implanted mark-ers23,26 concluded that torsion (angular difference in recipro-cal twisting of apex and base) was required to equalizestresses across the ventricular wall. Newer diagnostic toolsallow noninvasive monitoring of cardiac motion and therebyavoid invasive strategies that can distort cardiac structure andunintentionally vary underlying function.27 Two-dimensionalstrain imaging by the speckle tracking method defines longi-tudinal and radial strain fields on the basis of fiber directionindependent of angle of insonation.28 High spatial and tem-poral resolution echocardiography (Movie II in the online-only Data Supplement) displays global wall movementsrelative to changes in regional myocardial strain, whereregional strain (or deformation) is defined by the Lagrangianformula: [e�(L�Lo)/Lo], where e is strain, Lo is baseline
Figure 2. a, MRI phase contrast velocity mapping (tissue phasemapping) of systolic and diastolic cardiac frames with a tempo-ral resolution of 13.8 ms during free breathing in a in a healthyvolunteer. All motions are described in the text; the arrows showthe clockwise (marker to right) and counterclockwise (marker toleft) directions of transmural twisting motion during the short-axis view and are obtained during isovolumic contraction, midsystole, isovolumic “relaxation” phase, and slower filling in middiastole. b, Differences in mean values for tracing radial, tangen-tial, and longitudinal velocity motion, each 13.8 ms, for 12 vol-unteer subjects in whom basal, mid, and apical segments areanalyzed. Values above zero line indicate contraction, clockwisemotion, and shortening; below the zero line, values defineexpansion, counterclockwise motion, and lengthening. The lineexpansion time is end systole (ES), with an average 320 ms timeframe. Note early radial expansion in basal segment (a), reversalof twisting before end of systole (b), and supplemental latecounterclockwise base motion during systole (c).
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length, and L is the instantaneous length at the time ofmeasurement.
Consequently, positive strain occurs if the segment lengthexceeds its original length, and negative strain exists if thesegment length is shorter than its original length. Strainoccurs in radial (narrowing or compression and widening orexpansion), longitudinal (shortening and lengthening), andcircumferential (tangential) coordinates in the same manneras described by MRI analysis (Figure 2b). Rotation is angularcardiac motion around a vertical axis, and twisting or torsionis the difference between rotation of different segments(usually apex and base) as measured by 2-dimensionalspeckle tracking. Differences likely exist in findings ofechocardiographic and MRI analysis based on the locationand depth of the area evaluated. MRI ventricular analysis istransmural, and echocardiography evaluates transmural mo-tion only if no architectural overlap is found between endo-cardial and epicardial segments that have counterdirectionalmotion. Conversely, when such overlap occurs, echocardiog-raphy predominantly identifies the resultant motion of theendocardial or epicardial segment within the chosen regions.
Function Versus Missing Gaps FromConventional Explanations
The traditional apex to base electric excitation–cardiac mo-tion concept10 is contradicted by early basal motion beforeventricular shortening. MRI studies15,17 support observationsthat initial counterclockwise rotation during isovolumicpreejection cocking that narrows the ventricle14 makes themitral valve billow out,19 rotates the left side of the cardiacbase counterclockwise to the right,17 and produces strain29 tocompress the ventricle and further reduce mitral annulusdimension before ejection.20,30 These observations are con-sistent with the findings of Roy and Adami in 189031 andmore recently Armour and Randall,32 whereby the initialcardiac motion involved the base rather than apex. Recentmultiple gated ventricular acquisitions33 and ultrasonicsonomicrometer crystal measurements34 confirm this motion,but the causative mechanical mechanism is uncertain.
Furthermore, the conical apex and wider base undergotransient bidirectional lengthening during the preejectionphase (Figure 3a) despite sonomicrometer evidence of short-ening of LV wall endocardial fibers.34 Similar narrowing andapical “thrusting” was reported by McDonald in 1970,19 andan apical counterclockwise motion was confirmed by placingan intracoronary wire around the apical tip.35 These observa-tions show a lengthening motion despite a contracting sub-endocardial muscle and simultaneously underscore a discrep-ancy that exists between the MRI that displays transmuralcounterclockwise motion36 of the base and apex during thepreejection isovolumic contraction phase versus speckletracking rotational motions that show that the apex has aclockwise motion.37 Structural reasons for this disparity mustbe defined.
The second phase of ventricular shortening and narrowingoccurs during the reciprocal twisting of the apex and baseduring ejection (Movies I and II in the online-only DataSupplement), and these observations validate Borelli’s 1669concept that blood is wrung out from the heart, just like
wringing out a wet towel. This ballet-like progression patternof muscular torsion involves thickening, circumferential andlongitudinal shortening, and shearing, but the spiral muscularcomponents responsible actions for these actions are de-scribed incompletely.11,34,38,39 Such force generation and tor-sion make use of a 60-degree angulation of ventricular wallfibers oriented together with spatially disposed counterwovenhelices that act as “opposing force couples”38; this angulationis identical to the angle determined by Sallin40 for optimalejection in mathematical modeling.
The third phase is the isovolumic interval that precedesrapid filling, whereby the apical clockwise twist accompaniesthe 2 movements of lengthening and basal widening(Figures 2b and 3b). Rapid deceleration of LV pressurewave follows this sequential deformation pattern (Figure1a), associated with a time constant of LV pressure decay(tau)12 untwisting rate,13 as apical untwisting occurs to allowsubsequent suction12 of atrial contents into the ventricleduring the fourth rapid filling phase that includes similarlengthening, widening, and twisting motions.
In the past, lengthening during the isovolumic and rapidfilling phases was thought to reflect restoring forces fromrecoil of muscular potential energy stored during systole41,42
and from release of the compressed titin coil.43 However,sonomicrometer crystal measurements record continuing sub-epicardial muscle shortening of the LV free wall (despitecessation of shortening on both sides of the cardiac base andsubendocardial region) as shown in Figure 4,44 echocardiog-raphy documents ongoing strain during this muscular con-traction (Figure I in the online-only Data Supplement), andpostsystolic contraction exists during this interval.45 Thisobservation implies that ongoing contraction via an activemuscular mechanism contributes to this motion, and theresponsible muscle must be identified. Moreover, slightwidening of the base and apex occurs during the isovolumicinterval (Figures 2b and 3b) to cause a stretch that cannotresult from the contracting muscle responsible for rapidlengthening.
Structural Mechanisms UnderlyingVentricular Function
The heart requires an architectural design that allows thecontractile apparatus to empty and fill with optimal mechan-ical efficiency, determined by integration of vectors of forcegenerated by sarcomeres that can only shorten by activecontraction. Ventricular thickening increases �50% for only�13% myocyte shortening,46 so that myocyte deformationfrom strain relative to fiber orientation influences thesefindings. The extracellular collagen matrix of the myocardi-um is an important scaffold in maintaining muscle fiberalignment, ventricular shape, and size. It forms a spiralfibrillar structure of endomysial collagen47 to support aspatial distribution of myocytes and myofibers that en-sheathes48 the adjacent 3-dimensional reciprocal spiral ar-rangement pattern of muscle structure.
Many anatomic dissections of the musculature of theconical heart ventricles over the past 500 years8 confirm thatthe clockwise oblique fibers of the surface epicardial layerand counterclockwise oblique subendocardial layer fibers
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meet at the apical vortex and that a transverse layer surroundsthe LV base.49 Histological studies50 document this arrange-ment, but controversy exists about the architectural formcreating this 3-dimensional configuration and about how thisdual helical configuration influences function.
Robb and Robb in 19428 described an arrangement of 4distinct muscle bundles of superficial and deep bulbospiraland sinospiral fibers that resembled those previously definedby Mall and MacCallum,51 and they believed that each fiberbundle attached to the cardiac fibrous skeleton (Figure 5A).The deep circular bulbospiral fibers were traditionallythought to cause the dominant constriction motion duringejection, a movement that differs from the predominanttwisting during the shortening motion during ejection andrapid filling. They did not consider how a myocardialsyncytium without an obvious beginning or end could coor-dinate sequential motion,21,52 and the reproducibility of thesetracts is questioned.52,53
Rushmer et al, in 1953,41 looked at the whole ventricularmass, conceptually distinguished 3 layers of fibers (Figure5B), postulated that these fibers twisted into a vortex at theapex, and implied an intimate connection of individualmuscle layers that they believed was impossible to demon-strate by dissection of a real heart. Moreover, the transverseconstrictor muscle was considered responsible for ejection bycircumferential compression. Rushmer et al implied thatsimultaneous contraction of the oblique inner and outermuscles canceled each other out, suggested that tensiondeveloped between them generated stored potential energythat putatively establishes diastolic recoil that is currentlythought to restore form during the rapid filling phase,42 anddid not consider how transverse constrictor muscle influencedthe recoil process.
In 1979, Streeter50 modeled the LV, using the work ofKrehl49 and Torrent-Guasp,54 and described fibers that runlike geodesics (shortest path on a curved form) on toroidal
Figure 3. a, Two-dimensional imagingshowing the change in length of the LVcavity and width of the mitral annulusduring the diastole (*after atrial contrac-tion), preejection isovolumic contraction,and systolic ejection phases in open-chest pig. The length (L) and width (W)line dimensions are measured andexpressed numerically, and the percent-age change related to dimensions is rec-orded at the end of the diastolic fillingphase. Note that the LV cavity lengthensduring the preejection isovolumic contrac-tion phase and then shortens and nar-rows after ejection ensues. b, Two-dimensional imaging showing changes inventricular length and width between endsystole (with mitral valve closed) and thepostejection isovolumic interval. Note thatthe ventricular cavity lengthens and car-diac base widens as the mitral annulusincreases diameter, and mitral valveopening begins despite no change inventricular blood volume. The length andwidth line dimensions are measured andexpressed numerically, and the percent-age change is related to dimensions mea-sured in end systole, as observed in themarker on the ECG.
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surfaces, superimposed like doughnuts as in a set of super-imposed Russian dolls or a set of nested warped pretzels(Figure 5C). Each doughnut conformed to a ventricularcavity, with a tunnel at the center of each donut correspond-ing to the cavity chamber. Echocardiographic and MRI strainpattern recordings of narrowing before sequential twistingdiffer from the synchronous contraction developing from thisarchitectural backdrop. Streeter’s work established the �60°helical angular orientations of myocytes around the ventric-ular equator recently confirmed by diffusion tensor MRIrecordings.55 However, his ventricular histology sectionsfrom the LV base displayed a more transverse central fiberorientation, whereas apical sections displayed only obliquefiber orientation, and either the left- or right-handed helix canform the endocardial component. These anatomic studies didnot define the physiological implications of this architectureon LV mechanics.
The underlying structural concept of Streeter56 was en-dorsed by Greenbaum et al in 1981,57 but they disagreed withthe symmetrical organization proposed by Rushmer et al,41
invoking the principle that the dissection method might havedisrupted muscle fascicles, making it difficult to define theorigin of the fibrous cardiac skeleton. This anatomic obser-vation may be correct, but the functional objective is to showhow the principal vector forces within the 3-dimensionalcardiac structure influence cohesive integrated sequentialfiber contraction to cause the observed motions during eachbeat.
In 1957, Torrent-Guasp discovered a helical heart structureby simple hand dissection.58 First, he unraveled the heart to
identify an underlying midventricular spiral fold that changesthe transverse fibers to an oblique configuration and thatallows the unfolded heart to become a simple flattenedlongitudinal ropelike model extending from the pulmonaryartery to aorta (Figure 5D; Movie III in the online-only DataSupplement). Refolding the heart into its natural biologicalconfiguration allows definition of 2 loops, termed the trans-verse basal and oblique apical loops (Figure 6aand 6b). Thebasal loop is circumferential and wraps around both the LVand right ventricle but does not involve the septum, a findingsupported by recent diffusion tensor MRI analysis,59 but thisobservation needs further investigation. The apical loop iscomposed of a descending and ascending segment thatconforms to the right- and left-handed helical arrangementdescribed by anatomists over many years. Torrent-Guasp’sdissection introduces a “principal or dominant pathway”without defining individual fiber tracts and gives a road mapto its configuration. The resultant surrounding external basalloop buttress (or transverse shell embracing the LV and rightventricle) covers the internal oblique helical or conical apicalloop comprising reciprocally oblique fibers termed the de-scending and ascending segments with a figure-8 configura-tion that form a vortex at the cardiac apex. These architecturalfindings mirror the anatomic suggestions in Rushmer’s car-toon41 (Figure 5b) and concur with Grant’s ropelike model,52
but the physiological impact is questioned,60 together withrecurrent concerns about reproducibility and importance oftracts disrupted during manual dissection.21,52,53,61
Torrent-Guasp’s exposure of the midventricular fold anduncovering of dominant muscular pathways introduces spa-
Figure 4. Top left shows a diagram of the heart with the positions of the sonomicrometer crystals, one of which is deep in endocar-dium in open-chest pig. Bottom left shows that lengthening of the right-handed helix or descending (Desc.) anterior fibers is beginningwhile the left-handed helix or ascending (Asc.) anterior fibers are still shortening; the LV pressure and dP/dt tracings indicate the timing.The solid line shows the beginning and ending of the right-handed helix shortening, and the hatched lines show the left-handed helix orascending segment. Top right panel shows the section examined by the ultrasound probe, with the region of interest at the left andright parts of the septum. The bottom right panel shows the septum at higher magnification, and the timing lines parallel those in thefree wall in the sonomicrometer tracings. Strain in the right (red) and left (blue) sides of the septum is shown. M-mode shows displace-ment of the left and right sides of the septum toward their respective ventricular chambers. Note delay of initiation of ascending seg-ment and right septal motion, lengthening of descending segment during isovolumic phase after ejection, and continuing displacementof the right side of the septum toward the right ventricular cavity, despite beginning of LV cavity expansion. This displacement corre-sponds to the sonomicrometer tracings that display widening of the right-handed helix or descending segment while the left-handedhelix or ascending segment continues to shorten.
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tial macroscopic correlations between his dissections and thehistological models of Streeter et al.56 Although the data ofStreeter have been interpreted as showing a continuum offiber angles across the wall,62 his images of the LV base(Figure 7a) also suggest 3 groups of fibers: inner and outerfibers that tend to run obliquely to the equatorial plane and amiddle set that runs more horizontally. This explanation issupported strongly by diffusion tensor MRI that shows thesame 3 sets of fibers in the intact heart59 (Figure 7b).Moreover, Streeter’s lower images of the LV free wall nearthe apex demonstrate the reciprocal oblique fibers of theascending and descending segments of the helical apical loopthat are also evident with diffusion tensor MRI63 (Figure 7athrough 7c).
Many differences of opinion have been expressed aboutventricular architecture. The notion of a continuum of fiberangles is at odds with the notion of discrete bands, particu-larly because histological boundaries of discrete bands havenot been demonstrated. On the other hand, diffusion tensorMRI as well as studies with polarized light demonstrates 3layers of the LV free wall, compatible with layers that areeither discontinuous or separated by a narrow zone in whichfiber angles change markedly over very short distances. The
syncytial nature of cardiac muscle also argues against discretebands, except that we know that connective tissue septa existthroughout the wall and that during severe dilatation of theventricle these septa allow bundles of myocytes to slip pasteach other. The fact remains that different sets of ventricularmuscle fibers exist that do not contract synchronously and arelikely to play specific roles in contraction and relaxation.
Structure/Function Correlation and ProposedMechanical Sequence
The common features of a circumferential muscle mass withpredominantly transverse fibers and the oblique helical fiberarrangement of the inner and outer wall are documented by allanatomic descriptions and must be integrated to define afunctional model that can explain how the heart fills andempties. Previously, investigators had concentrated on one orthe other set of fibers, with little regard for their interaction.The improved newer imaging methods add a unique way tofocus on regional natural motions, and an attempt will bemade to functionally explain these movements with theinteractions among these oblique and circumferential fi-bers. Although the details of the planes of fiber structurecausing these natural motions are uncertain,60 the macro-
Figure 5. Myocardial fiber organization. a, Mall and MacCallum’s suggestion of 4 myocardial bundles, with deep (circular) and superfi-cial oblique bulbospiral tracts. Aorta (A), mitral (M), tricuspid (T), right ventricle (RV), left ventricle (LV), and papillary muscles (pp) areshown. b, Rushmer’s conceptual model showing how spiral superficial and deep clockwise and counterclockwise layers twist at theapex and sandwich the central transverse constrictor muscle. c, Streeter’s LV model in which inner and outer fibers run like geodesics(shortest path on curved surface) on toroidal surfaces (resembling doughnuts), and superimposed layers decrease in size like Russiandolls. d, Torrent-Guasp’s model of predominant fiber trajectory follows a pathway that contains an upper left base or circumferentialmuscle that embraces an internal helical loop. The upper right image displays intact heart muscular components containing an uppertransverse circumferential muscle (or basal loop) surrounding the oblique right- and left-handed helical apical loop. The unfolded coiledarrangement resembles a flattened rope model beginning at the pulmonary artery and ending at the aorta (Ao), with circumferential fiber(or basal loop) right (RS) and left segments (LS) attached to the double helical apical loop right-handed helix or descending segment(DS) and left-handed helix or ascending segment (AS).
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scopic motions are clear, and the subsequent role of theanatomist is to explain the 3-dimensional microstructurethat causes these movements. Images that display cardiacmotion are best understood in context of the dominantforce created as a result of interactions among the simul-taneously contracting wrapped circumferential fibers andoblique helical fibers. For example, within this architec-ture, the right-handed helix can move one way, theleft-handed helix can move the other way, and the outcomeis in concert with which movement dominates, unless thecircumferential wrap is more powerful.
Preejection PhaseUltrasonic crystal data show that, at the initiation of systole,the predominantly transverse circumferential muscle shortensalmost simultaneously with the right-handed helix or de-scending segment (Figure II in the online-only Data Supple-ment) to compress the central left- and right-handed heliceslike a stiff outer shell and to cause the temporary longitudinallengthening of the apex and base during the preejectioninterval (Figure 3a and Figure III in the online-only DataSupplement). This circumferential muscle is consistent withthe horizontal fiber orientation displayed in the histologyanalysis of Streeter et al,56 and diffusion tensor MRI analy-sis59 and its motion corroborate the constriction functiondescribed by Ingels et al.39 The action of this establishedcircumferential muscle mass has not been considered incurrent echocardiographic descriptions of muscular causesfor motion.10,11 Although the inner shell is stimulated at theearliest interval by the direct Purkinje-myocyte fiber connec-tion,64 transmural stimulation of the right-handed helix isinsufficient to cause longitudinal shortening at this time.Figure III in the online-only Data Supplement displays a briefshortening, followed immediately by apical stretching due tothe narrowing during the presystolic isovolumic contractionphase that is caused by the dominant motion of the circum-ferential fibers. The simultaneous consequence is rotating theentire heart in a counterclockwise direction on MRI record-ings viewed from the apex and thereby explaining thecocking motion observed during the isovolumic preejectioninterval (Figures 2a and 8c). This radial shortening due tocircumferential fiber contraction occurs in humans19 to com-press the as-yet not fully contracted inner helix to account forthe bidirectional cavity lengthening during this isovolumic
Figure 6. a, Unscrolling of Torrent-Guasp’s myocardial bandmodel, whereby his unwrapped heart (e) contains an obliquecenterfold that separates the basal and apical loops. Note (1)the transverse basal loop fiber orientation (b through e), repre-senting circumferential fibers, and (2) the right- and left-handedapical loop helix with predominantly oblique fibers and recipro-cal spiral (c) representing the right- and left-handed helix config-uration, which (3) twists at basal and apical loop junction. Themyocardial band extends between the pulmonary artery (PA)and the aorta (Ao). Note (a) the intact heart and (b) detachmentof the right ventricle free wall with circumferential transverse ori-entation of right basal segment (RS). A genu adjacent to theseptum separates the right and left ventricles, with (c) thedetached rotated apical loop showing the left basal loop seg-ment (LS) surrounding the inner helix configuration containingoblique right- and left-handed helical or descending andascending segments. Note (d) unwrapping of the helix to showunfolding of the descending segment (DS) and (e) the complete
transverse myocardial band, with the central myocardial musclefold to separate the basal and apical loops. The left segment isthe transverse circumferential or basal loop, containing left andright segments, and the right segment is the unwrapped right-and left-handed helices of the apical loop containing a descend-ing and ascending segment (AS). b, Architectural arrangementof the fiber orientation of the detached circumferential fibers(basal loop) that has predominantly horizontal fibers comparedwith the conical apical loop that contains right- and left-handedoblique fibers in a helical design, with these segments superim-posed (top image); when the segments are separated (below),the right-handed helix or descending segment (lower left) isconnected to the myocardial fold, and its oblique fibers aimtoward the apex, whereas the overlying left-handed helix orascending segment (lower right) is longer, and its oblique fiberscourse toward the fiber connection with the aorta.
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contraction phase. The elongation of the double helix causedby cocking is also evident by ventriculography during thepresystolic interval,19 confirmed by echocardiography (Fig-ure 3a), MRI analysis (Figure 2b), and velocity vectors of
directional motion (Figure IV in the online-only Data Sup-plement). This preejection stretch of the helix may “load” themuscles to produce a Starling effect via the titin mechanism65
Analysis of timing of the electric impulse shows that earlyactivation of the right and left parts of the base and septum ofthe heart occurs through the moderator band (right ventri-cle)64 and from the left posterior fascicle66 (LV). Humanendocardial mapping studies at this time interval show thatthe upper septum becomes activated 15 to 20 ms before theapical region.67,68 A clockwise motion is implied becausemultiple gated ventriculography analysis33 and ultrasoniccrystals34 show that the sequence of initiation of contractileactivation to produce strain29 and compression (Figure 2b)proceeds from right to left to constrict the base of the heart.However, the mechanical rotation sequence is counterclock-wise (Figures 2a and 8c), a finding that may reflect how thelarger muscle mass of the left part of the circumferential musclebecomes dominant to govern global rotation (Figure 8a).
The endocardial contraction does not exert sufficient forceto cause the consistent longitudinal shortening movement thatexists during ejection, as evident from radionuclide ventricu-lography recordings29 and speckle tracking imaging record-ings showing evidence of that brief shortening that is subse-quently overcome by lengthening during this interval (FigureIV in the online-only Data Supplement).10 The failure toshorten the chamber during the isometric phase implies thatthe counterclockwise rotation of the apex is due to circum-ferential muscle movement because the epicardial segment ofthe helix is not contracting during the preejection period, asshown in Figure 4.
The apex is composed of the right- and left-handed helicalfibers, and its motion is determined by how it is affected byboth the helical fibers and their interconnection with thesurrounding base of the heart. For example, the contrast
between the MRI that displays counterclockwise motion ofthe transmural wall and the clockwise motion shown byspeckle tracking that samples predominantly the endocardiummay relate to the imaging evaluation tool because the super-imposed epicardial segment is not contracting. Movie II in theonline-only Data Supplement shows a transmural imageand demonstrates how high-definition echocardiographycan provide visual insight into counterdirectional forces ofthe right- and left-handed helical segments that are usuallytermed endocardium versus epicardium or descendingversus ascending regions. The counterclockwise motiondisplayed by MRI recordings (Figure 2a and 2b) showsthat the dominant rotational direction is governed by themore powerful circumferential muscle component. How-ever, the capacity of speckle tracking imaging to recognizepreejection endocardial clockwise rotation introduces amechanical reason for mitral valve closure before LVpressure generation because presystolic blood flow veloc-ity is directed from the apex toward the base during earlyendocardial rotation37 to thereby establish a flow-relatedexplanation. Conversely, initiation of left-handed helixcontraction is delayed until ejection (Figure 4) when it isresponsible for the ongoing counterclockwise twisting ofthe apex, as described in the next section.
EjectionDuring ejection, the circumferential fibers continue to shortentogether with the oblique fibers in the right- and left-handedhelices (or descending and ascending apical segments) thatco-contract to shorten and thicken to empty the heart. Thecircumferential fibers produce a horizontal counterforce that
Figure 8. Preejection phase. a, Cranial view of the model of the helical ventricular myocardial band showing how the conical right- andleft-handed helix or apical loop is surrounded or embraced by the circumferential fibers or basal loop. Note that circumferential fibermuscle thickness is thin in the right component or segment and thicker in the left component or segment. b, Velocity vectors duringthe preejection phase in open-chest pig preparation (Siemens Acuson System) that define the directional motion in the image plane.Vector length is proportional to the strength of the velocity forces and is in the downward axis (toward apex) that correlates with elon-gation observed by other imaging modalities (speckle tracking imaging, MRI, left ventriculography, surface myocardial crystals). Themitral valve is closed, and the increased long axis is expected in a closed system that becomes narrower as preejection vectors movefrom base to apex. c, MRI visualization of myocardial velocities of rotation (tangential vectors) recorded on the short axis in humans attemporal resolution of 13.8 ms during presystolic isovolumic contraction showing counterclockwise rotation (arrows pointed to the leftside) of the apex and base at this interval.
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accentuates narrowing throughout ejection. Furthermore,these contracting transverse circumferential fibers provide a“buttress” to counteract the outward forces generated by thetwisting and shortening oblique muscle of the inner right- andleft-handed helical segments and thereby prevent an outwardexplosion at the cardiac base during ejection. The twistingsegments move in clockwise and counterclockwise direc-tions, as shown by recent echocardiographic observations18 aswell as by tangential vectors by MRI (Figure 2a) and visuallyin Movie II in the online-only Data Supplement, whichsimultaneously allows comparison to underlying architectureto convey structural reasons for directional motions in areaswith and without overlap of helical fibers (Figure 9a).
Strain is greatest in the right-handed helix (or subendocar-dium),11 accounting for its capacity to cause shortening andclockwise twisting of the cardiac basal region, but thesimultaneous counterclockwise apical twist is due to thetorque of the co-contracting left-handed helix (or epicardium)with a larger radius of curvature39; their interaction is respon-sible for systolic torsion. The subendocardial muscle isformed by both the right- and left-handed helices (or descend-ing or ascending segments) (Figure 9b), depending on their
sampling site within the helical architecture. This structuralarrangement explains why MRI (Figure 2a and 2b) andspeckle tracking imaging69 display clockwise and counter-clockwise shortening during ejection. Conversely, speckletracking imaging displays transmural motion in regions with-out helical fiber overlap in areas of lateral and inferior wallsand septum just below the aortic valve. As a result, nocounterforces act on the endocardium of the left-handed helix(or ascending segment) in these areas (Figure 9b).
Sonomicrometer crystal tracings demonstrate sequentialshortening of the descending, posterior, and ascending seg-ments (Figures V and VI in the online-only Data Supplement)of the Torrent-Guasp model.34 However, a network of con-nected fibers exists within the deeper intermingled transverseand oblique fibers,21 so that transverse fiber interconnectionsmay induce shearing by creating transmural torque, whereasoblique fibers exert directional shortening. The global rota-tional and directional forces are displayed by MRI in Figure2a and 2b, which conveys how these co-contracting clock-wise and counterclockwise forces create the radial velocitiesthat define systolic compression of the LV. As the right-handed helix (or descending segment) contraction dominates
Figure 9. a, Ejection. Apical view (a) of myocardialarchitecture of the ventricular myocardial bandshowing the relationships of the oblique fibers inthe right-handed helix or descending (deep) andleft-handed helix or ascending (surface) segmentsthat (1) overlap in the anterior lateral LV free walland septum and (2) do not overlap in the most lat-eral region. Short-axis view (b) of Movie II in theonline-only Data Supplement during ejectionshowing similar overlap of endocardial and epicar-dial muscle fibers in anterior lateral ( LV) free walland septum and showing no overlap in most lat-eral region, as shown in views of apical myocardialarchitecture. Vector imaging (c) performed at theapex during ejection in the open-chest pig demon-strating that endocardial vectors in each region ofthe septum (formed by the descending segment)point radially inward in a clockwise direction,whereas endocardial vectors on the anterior andlateral wall point radially inward in a counterclock-wise direction and correspond to the apical viewarchitecture. b, Topographical view of myocardialarchitecture showing left- and right-handed orascending and descending segments of the helicalventricle, surrounded by the circumferential muscleof the basal loop. Note (1) how the central ventric-ular cavity is composed of overlapping left- andright-handed helices or ascending and descendingsegment fibers in the septum region, (2) how theleft-handed helix wraps around and overlaps theright-handed helix in this region, and (3) absenceof overlap in the lateral wall, which is composed ofthe left-handed helix or ascending segment. Thelack of overlap in the left-handed helix or ascend-ing segment also occurs in the septum, below theaortic valve, as displayed in Figure 10, comparingfunction to architecture with different views of theunwrapped heart.
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to shorten the ventricular chamber, it simultaneously pullsdown the co-contracting left-handed helix (or ascendingsegment), whose fibers now become more horizontally ori-ented. Consequently, such helical co-contraction joins thecircumferential contraction to accentuate chamber narrow-ing40 during the ejection phase to aid ventricular propulsionof blood.
Deformation is greatest toward the apex to achieve maxi-mal reduction in chamber volume25 and may be explained bythe fact that the right- and left-handed helical segmentsconverge toward the apex to form the vortex of the doublehelical loop.25 The oblique right-handed helix initiates short-ening and is joined 80 ms later by co-contraction of theleft-handed helix that comprises the ascending segment of theapical loop (Figure 4, Figures VI and VII in the online-onlyData Supplement). This shortening also thickens and twiststhe LV apex and exerts a torque in an opposite (counterclock-wise) direction, as shown in Movie II in the online-only DataSupplement, by MRI in Figure 2a, and by velocity vectordirectional motion (Figure VIIIa in the online-only DataSupplement). This regional left-handed helical directionalmotion is evident by velocity vector analysis in whichleft-handed helical components in the lateral wall and upperseptum have no helical overlap (Figure 10). However, theleft-handed helical mechanical mechanism underlying coun-terclockwise apical motion during ejection differs from thepreejection phase apical rotation, which represents domi-nance of the circumferential fibers when contraction of theleft-handed helix (or ascending segment) is absent.
Each spiral arm of the helix globally twists itself inopposite directions; the right-handed helix is dominant, di-rected downward, and its twist causes the observed clockwiserotation of the cardiac base. Conversely, the left-handed helixtwists counterclockwise to produce apical reciprocal rotation.Although its longitudinal motion is directed upward, it movesdownward during ejection because it is dominated by theright-handed helix, as shown by velocity vector analysis(Figure VIIIb in the online-only Data Supplement). Evidencefor the simultaneous elevation and straightening of theleft-handed helix (ascending segment) muscle is delayed untilthe isovolumic interval, when its ongoing contraction nowexists without right-handed helix (descending segment) con-
traction, resulting in upwardly directed velocity vector, asdiscussed in the next section (Figure VIIIc in the online-onlyData Supplement).
These observations contradict prior suggestions that theepicardial muscle exerts the downward force during ejec-tion,39 as well as recent suggestions that the epicardium(left-handed helix) twists within itself, so that its apex goes inone direction (counterclockwise) and its base in the oppositedirection (clockwise), together with the suggestion that theendocardium (right-handed helix) has the reverse action.11 Alimitation of this analysis is the absence of recognition thatthe endocardium can be formed by either the left- or right-handed helix, depending on their overlap. The left- andright-handed helices connect at the apical vortex that be-comes the turning point for their reciprocal motion. Thereby,the helical arrangement of fibers shows that the entireright-handed helix component twists clockwise to shorten thechamber. Such early clockwise motion was evident byspeckle tracking imaging during the preejection interval(Figure 1c),37 when transient shortening occurs (Figure III inthe online-only Data Supplement), and from the continuedclockwise motion of the cardiac base during ejection, asevident by MRI tangential motion (Figure 2a and 2b) andspeckle tracking imaging.18 Furthermore, velocity vectorimaging shows clockwise rotation of the endocardial segment(forming the LV septum endocardium) at all levels (apex, midwall, and base) during ejection (Figure IX in the online-onlyData Supplement).
The entire left-handed helix (epicardium) twists counter-clockwise; this motion prevails at the apex and appears as aleftward direction of upper septum motion by velocity vectoranalysis (Figure 10) that correlates movement with theanatomic wraparound configuration. Simultaneously, the left-handed helix thickens during co-contraction to compress thecavity, but its effort to elevate the ventricle is offset by theprevailing dominance of the right-handed helix (descendingsegment) contraction, as demonstrated by downward velocityvectors during ejection (Figure 10, Figure VIIIb in theonline-only Data Supplement). The contraction-related eleva-tion of the left-handed helix only becomes apparent duringthe isovolumic phase, when right-handed helix contractionstops (Figures 2b and 3b; Figure VIIIc in the online-only Data
Figure 10. Ejection. Comparison of the leftwardvelocity vector changes in motion (Siemens Acu-son System) observed in the lateral wall and upperseptum during later ejection (left) with the muscu-lar architecture of the left- and right-handed heli-ces of the ascending and descending segments ofthe apical loop (right). Note (1) that the septum isformed by overlap of these helical segments,except for the upper wall, which is beneath theaorta formed by only the left-handed helix orascending segment; (2) that the lateral wall is com-posed of the wrap of only the left-handed helix orascending segment because no overlap exists inthis region (as shown in Movie II in the online-onlyData Supplement); (3) the relationship of this left-handed helix or ascending segment architecture tothe leftward rotation in lateral wall and septum;and (4) downward motion of entire LV wall duringejection (as shown by echocardiography and MRI).
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Supplement). From a mechanical standpoint, the shorteningmotion during ejection reflects the dominant force of theright-handed helix rather than the constrictive motion of thecircumferential fibers that predominantly causescompression.
Isovolumic PhaseAfter ejection, the right-handed helix (or descending seg-ment) stops contracting but maintains stiffness and tension17
and thus may act as a fulcrum for left-handed helix (ascend-ing segment) straightening because this segment continues tocontract in an unopposed fashion for an additional �90 ms(Figure 6). When a helix is compressed, its 2 ends approacheach other, and the internal coils (or springs) become morehorizontal, and when it is stretched, the 2 ends move apart,the coils become more vertical, and the helix becomesstraighter. These changes represent rearrangement of the coilsas a whole and can be separated from changes of length ofindividual segments (myocytes) of the coil. For example, inthe postsystolic isovolumic period, the left-handed helix (orascending segment), which was compressed and more hori-zontal, continues to contract and straighten because it is nolonger opposed by contraction of the right-handed helicalspiral.
The contraction of the left-handed helix is the only forcefor the abrupt change to an upward velocity vector direction(Figure VIIIc in the online-only Data Supplement) during thisphase. Cavity widening also occurs without blood inflow(Figures 2b and 3b; Figure VIIIc in the online-only DataSupplement) and is likely related to recoil of circumferentialmuscle that has stopped contracting. The discrepancy be-tween a fixed volume and increases in width and length is
probably due to the use of a 2- rather than 3-dimensionalmeasurement. The oblique right- and left-handed helicesdemonstrate a spatial and temporal relationship during theinitiation and completion of their shortening that interactswith the predominantly transverse circumferential muscle.
The predominant motion is rapid clockwise untwisting ofthe apex and mid wall, together with accentuation of theclockwise motion of the base (Figure 2b). These movementsoccur before the end of systole and exist only while theleft-handed helix is still contracting (Figures 2b and 4;Figures I and VI in the online-only Data Supplement).Moreover, the widening of the cardiac base shown byechocardiography in Figure 3b, MRI (Figure 2b), sonomi-crometer crystals (Figure II in the online-only Data Supple-ment), and velocity vector analysis (Figure VIIIc in theonline-only Data Supplement) is associated with a lengthen-ing of the basal area (Figure 2b).
The untwisting motion during elongation creates a negativepressure and potential vacuum70 that continues into the phaseof rapid cavity filling after the decelerating ventricularpressure falls below atrial pressure. Its origin is likely fromtitin-related recoil43 of the noncontracting circumferentialfibers that exerted a counterclockwise motion during preejec-tion. The right-handed helix straightens as the left-handedhelix maintains strain, continues to shorten (Figures 4 and 11;Figures I and VI in the online-only Data Supplement), andelevates, so that the left-handed helix (ascending segment)cannot be the cause of untwisting. This observation contra-dicts a recent report’s comment that untwisting is due to theepicardium because this reversal of twisting is not possible ina region that is still contracting.12 Moreover, the ongoing
Figure 11. Isovolumic phase. a, Frontal view of apical view of myocardial architecture of the ventricular myocardial band showing therelationships of the oblique fibers in the right-handed helix or descending (deep) and left-handed helix or ascending (surface) segmentson the septum, where the left-handed helix is the only segment contracting during the isovolumic phase, as shown in testing bysonomicrometer crystals and persistence of strain by speckle track imaging. b, Velocity vectors in the open-chest pig (Siemens AcusonSystem) taken in the first 20 ms of the isovolumic interval and showing vector length and velocity forces in the upward axis (away fromapex) that correlate with elongation observed by other imaging modalities (MRI, sonomicrometer crystals, echo analysis). Note that thelateral forces are outward (expansion) and are in region of surrounding left segment of circumferential muscle or basal loop that is notcontracting (sonomicrometer crystals). c, Two-dimensional speckle strain of the LV in the short-axis view showing strain in anterior andlateral LV walls demonstrating (1) that peak strain is different in different segments (with lateral wall exceeding anterior wall) (mean valueis shown by white dots) and (2) persistence of strain during the isovolumic interval (outlined by red dots) that follows the T wave shownon the underlying ECG.
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left-handed helix shortening and strain now provide a mus-cular explanation for the origin of postsystolic contraction.45
Most likely, the clockwise rotation of the apex is governedby recoil of the circumferential fibers (or basal loop), whichalso stop contracting, and is the opposite movement from itspreejection counterclockwise motion (Figure II in the online-only Data Supplement). Although the apex continues itscounterclockwise motion because of the left-handed helix, itsradial velocity forces are markedly diminished (Figure 2b) sothat the observed net clockwise motion reflects untwisting ofthe apex from recoil of the circumferential fibers (or basalloop). Additionally, this decreased force of contraction is apotential reason for the later lengthening during the isovolu-mic interval recently reported by Notomi et al.12,16 An addedmechanical factor is that the prominent untwisting shown inFigure 2b may also imply an unwinding of the taut right-handed helix (or descending segment), which now returns toits original helical starting point (Figure 6b, lower left).
Conversely, an opposite action exists for the circumferen-tial muscle in preparation for ventricular filling, as untwistingand widening develop a potential intraventricular vacuum forsubsequent suction during unopposed straightening of theleft-handed helix or ascending segment. MRI studies showthat the cardiac base widens and the chamber cavity lengthens(Figures 2b, 3b, and 11) and remains thick,71 so that thecounterforce of the stiff outer rim circumferential muscleprevents potential implosion of the base during lengthening.The circumferential muscle thereby exerts the balancingaction of preventing explosion during ejection and avoidingimplosion before and during rapid filling and has the predom-inant action of governing narrowing and widening motions.In contrast, the oblique fiber orientation of the right- andleft-handed helices governs the shortening and lengtheningmotions.
Observations that document the muscular role of theleft-handed helix during this interval include sonomicrometercrystal evidence of ongoing contraction (Figure 4), continu-ing strain (Figure 11, Figure I in the online-only DataSupplement), MRI evidence of radial velocity showing con-traction (Figure 2b) and thickening,71 and an abrupt change inthe velocity vector toward elongation as the isovolumic phasebegins (Figure VIIIc in the online-only Data Supplement).The elevation component from ongoing contraction of theleft-handed helix mirrors the spatial alteration that existswhen a cobra elevates as its muscles continue to contract inthe interval before striking. For the heart, this cardiac cham-ber elevation motion is due to the now unopposed contractingmuscular force of the left-handed helix that becomes morevertical and is not “recoil from stored potential energy”because shortening (negative strain) and thickening existduring this phase of cardiac motion. Moreover, this activemuscular effort is the reason that the ventricle returns to theprevious “neutral” longitudinal position during the isovolu-mic phase, a motion that contradicts the conventional conceptof recoil, which occurs at the ventricular base for wideningand untwisting. The presence of active contraction during theperiod previously considered to be “isovolumic relaxation”suggests that this term is ambiguous and should be avoidedunless qualified by accurate muscular descriptions.
The physiological untwisting action is caused by a geo-metric dynamic change in shape and has been characterizedby a series of hemodynamic changes that include measuringthe rate of untwisting,13 as well as tau (change in time relatedto change in deceleration in LV pressure),72,73 and also bymeasuring the intraventricular pressure gradient that is max-imal just after the mitral valve opens,12 which is considered inthe next section.
Rapid Filling and SuctionThe suction phase for rapid filling occurs after the ventricularpressure falls below atrial pressure and is associated with afurther rapid accentuation of untwisting of the apex in aclockwise direction (Figure 2b); Dong et al13 showed that40% of untwisting occurred before the rapid filling phase.Continued untwisting is caused by elastic recoil of com-pressed titin coils within the left-handed helix fibers, in amanner similar to circumferential muscle (basal loop) wid-ening and recoil for clockwise rotation during the isovolumicphase. Although the recoil mechanism is responsible for rapidfilling, the vital role of active and unopposed left-handedhelix contraction to cause straightening during the isovolumicphase is an important component because suction is impededor avoided if this motion is opposed by prolonged descendingcontraction, as discussed in the next section.74,75 As thecontractile phase dissipates and all the muscle segmentsbecome relaxed, the rapid titin-related “unwinding” of theapex to its original position creates the suction required tocause rapid ventricular filling, which occurs as the ventricularpressure drops below the atrial pressure. Further wideningand lengthening develop from the hydraulic effects resultingfrom rapid and then passive filling after the apical reciprocaltwisting action has stopped.
The contributions of different segments of the helicalventricular myocardial band toward these 4 phases of phys-iological motion response are identified by placing sonomi-crometer crystals into the right and left segments of the basalloop, as well as into the descending and ascending segmentsof the apical loop of the LV free wall.34 During the preejec-tion isovolumic contraction phase, shortening occurs in 3regions of the right and left basal segments and the LVendocardium. With ejection, co-contraction exists in thedescending and ascending segments, together with ongoingshortening of the both basal loop segments, so that all 4 areasare shortening. Conversely, during the isovolumic intervals,active shortening occurs in only the 1 ascending segmentbecause contraction has stopped in both segments of the basalloop and in the descending segment. Recoil after completionof contraction in the ascending segment produces the apexclockwise motion responsible for early rapid filling, an actionthat requires the isovolumic phase to display a temporalhiatus between descending and ascending apical loop seg-ment contraction.
ImplicationsExcitation/contraction events during the preejection sequencemay have clinical utility to understand cardiac resynchroni-zation therapy. During preejection, the circumferential basalloop rather than the left- and right-handed helical apical loop
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is responsible for causing ventricular lengthening becauseright-handed helical or descending segment contraction doesnot cause transmural shortening of the free wall and septum,and the left-handed helical (or ascending) segment has not yetcontracted. Biventricular pacing initiates a dynamic transmu-ral septal contraction and thereby offsets the septum bulgeduring dyssynchrony by placing the septum in a midlineposition.76 This architectural alteration changes the geometricposition of the posterior papillary muscle to limit its tetheringof the mitral leaflet by the bulging septum and thus improvesleaflet coaptation to reduce mitral regurgitation, but withoutrestoring the twisting motion of the septum.
The interaction of timing of contraction of left- andright-handed helices (or ascending and descending segmentsof the apical loop) governs the efficiency of apical untwistingthat determines suction, thereby introducing a paradigm shiftin conventional thinking. The traditional concept of elasticrecoil and passive dilatation as the cause of changing ven-tricular volume before filling becomes changed to include anactive contractile process77 that simply disappears or becomeslimited when descending segment contraction is prolonged.78
The impact of prolonged systolic forces during ejection wasobserved by Stuber et al,74 employing tagging MRI studies inpatients with aortic stenosis (Figure 12) and also in patientswith dilated cardiomyopathy.79
Systolic contraction extended into the isovolumic phase(previously termed early diastole), and a similar pattern wasobserved after transient ischemia78 to produce diastolic dys-function (Figures Xa, Xb, Xc, and XI in the online-only DataSupplement). Sonomicrometer crystal studies demonstratedthat extended descending segment contraction limits thenormal hiatus (�80 ms interval) between cessation of de-scending and ascending segment shortening to generate anabnormal pattern that is remedied by sodium-hydrogen ex-change inhibitors.78 Recognition of this active process maylead to selection of new drugs that can modify a contractilemechanism for cardiac dynamics during the phase of rapidfilling44 and therefore remedy the diastolic dysfunctional
component of congestive heart failure that affects �50% ofpatients.6
ConclusionsKeith, in 1918, presented a currently unfulfilled challenge bystating, “We cannot claim to have mastered the mechanism ofthe human heart until we have a fundamental explanation ofits architecture.” We conclude that comparison of functionalimages against several structural models showed that thehelical ventricular muscular band model of Torrent-Guaspprovides a functional anatomic model that explains theobserved directional and twisting sequential motions. Furthertesting of these spatial anatomic concepts is needed becausethe architectural coordination of structure and function, ifproperly confirmed, may adhere to Keith’s challenge andallow accurate understanding of the mechanisms of cardiacdynamics.
DisclosuresDr Buckberg consults with Helical Heart Company LLC (www.helicalheart.com), which makes a spatial heart model of helicalventricular myocardial band anatomic configuration. The otherauthors report no conflicts.
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