Noninvasive Measurement of Shortening in the Fiber and Cross-Fiber Directions in the Normal Human Left Ventricle and in Idiopathic Dilated Cardiomyopathy
Background Studies in anesthetized dogs have shown that myocardial fibers shorten ≈8%. However, in the endocardium, shortening occurs to a much greater extent at 90° to the fiber orientation (“cross-fiber shortening”) than it does along the fiber direction. The purpose of this study was to estimate the extent of fiber and cross-fiber shortening in the normal human left ventricle and in patients with idiopathic dilated cardiomyopathy (IDC).
Methods and Results Ten normal subjects and nine patients with IDC were imaged with magnetic resonance tissue tagging. Finite strain analysis was used to calculate endocardial and epicardial shortening in the fiber and cross-fiber directions using anatomic fiber angles from representative autopsy specimens as references. Anatomic fiber angles were not different between normal subjects and IDC patients. Epicardial fiber strain was −0.14±0.01 in normal subjects and −0.08±0.01 in IDC patients (P<.0001 versus normal subjects). Epicardial cross-fiber strain was −0.08±0.01 in normal subjects and −0.06±0.01 in IDC patients (P=NS). Endocardial fiber strain was −0.16±0.01 in normal subjects and −0.09±0.01 in IDC patients (P<.0001), and endocardial cross-fiber strain was −0.26±0.01 in normal subjects and −0.15±0.01 in IDC patients (P<.0001). Cross-fiber shortening was greater than fiber shortening at the endocardium in both normal subjects (P<.0001) and IDC patients (P<.05).
Conclusions In normal humans, the direction of maximal deformation aligns with the fiber direction in the epicardium but is perpendicular to the fiber direction in the endocardium. When strain in a coordinate system aligned to the fibers is estimated, cross-fiber shortening is found to be the dominant shortening strain at the endocardium. Normal fiber shortening is ≈15%, and this is markedly reduced in IDC. The normal transition in fiber orientation through the wall is not altered in IDC, and cross-fiber shortening is still the dominant strain at the endocardium, suggesting that interactions between myocardial layers persist in these patients.
The fibers of the human left ventricle are arranged in a complex fashion, with epicardial fibers directed in a counterclockwise spiral and endocardial fibers in a clockwise spiral from apex to base. Therefore, there is transition in the orientation of fibers through the wall of the left ventricle, with epicardial fibers oriented obliquely, midwall fibers oriented horizontally, and endocardial fibers oriented obliquely in the opposite direction from epicardial fibers.1
This fiber architecture has important functional consequences. Analysis of canine myocardial shortening with respect to fiber orientation2 3 has shown that at the epicardium, shortening is predominantly aligned in the direction of epicardial fibers. However, at the endocardium, maximal shortening is ≈90° from the endocardial fiber direction.3 4 This “cross-fiber shortening” is thought to be accomplished by the physical rearrangement of fibers or fiber bundles2 induced by contraction of layers with different fiber orientation. LeGrice et al5 suggested that this rearrangement occurs along cleavage planes that separate sheets of myocytes and that it is associated with transverse shearing deformation. These rearrangements and shears allow the endocardium to shorten in two orthogonal directions, producing extensive thickening in a third direction to preserve volume. This would explain the marked systolic endocardial thickening that is essential for normal ejection.3
The extent of fiber and cross-fiber shortening in the left ventricle of normal and abnormal human hearts is unclear. Rademakers et al,3 using MR tagging, and Waldman et al,4 using radiopaque beads, have shown that fiber shortening in anesthetized dogs is ≈8%. In humans, studies that used echocardiography corrected with geometric models have calculated that fiber shortening is 21% in normal subjects and 18% in subjects with left ventricular hypertrophy and normal global function.6 Studies that used MR tagging have suggested that fiber shortening is 30% in normal subjects and 21% in patients with left ventricular hypertrophy.7 Thus, marked differences in the extent of fiber shortening have been observed between human and experimental studies.
It is not known how fiber and cross-fiber shortening are affected in idiopathic dilated cardiomyopathy (IDC). Myocardial fiber shortening might be reduced, directly reflecting reduced contractility. Alternatively, dilation of the left ventricle might have effects on fiber orientation, resulting in a more circumferential fiber arrangement. As the variation in fiber orientation through the left ventricular wall diminishes, cross-fiber shortening might be reduced. Finally, because integration of epicardial and endocardial strains may be mediated via connective tissue,8 cross-fiber shortening might be reduced due to alterations in this matrix.9
The aims of the present study were to use MR tissue tagging, a noninvasive method of marking specific segments of myocardial tissue,10 11 to estimate fiber shortening in the normal in vivo human myocardium and to determine if marked cross-fiber shortening occurs at the endocardium. We also sought to determine the extent of fiber shortening and cross-fiber shortening in IDC.
Ten normal volunteers who had no history of cardiac disease or hypertension and nine patients with compensated heart failure (NYHA class II or III) due to IDC were studied (Table 1⇓). IDC was diagnosed by clinical evidence of heart failure, echocardiographic evidence of chamber dilation, and normal coronary arteries on selective angiography. All patients had ejection fractions <35%, were in sinus rhythm, had no history of hypertension, and were treated with digoxin, ACE inhibition, and diuretics. Informed consent was obtained from all participants. Approval for this study was obtained from the institutional review board.
Images were acquired with a Resonex RX4000, 0.38-T resistive magnet using a spin-echo pulse sequence with time to echo of 30 ms and time to repeat of every two RR cycles. Three short-axis images were acquired, aligned so that the plane of the images was parallel to the AV groove and spaced 1.5 to 3.0 cm apart to cover the left ventricle from base to apex. Tags were created by radiofrequency saturation of thin planes orthogonal to the short axis at end diastole.10 On each short-axis slice, three radially spaced tags (transecting the myocardium at six locations), intersecting at the center of the left ventricle, were placed at 120° apart (Fig 1⇓). When long-axis images were being acquired, the imaging and tagging planes used in the short-axis images were interchanged so that three long-axis images were obtained 120° apart, each with three transverse tags in the planes previously used to obtain short-axis images (Fig 2⇓). Images were acquired at end diastole (defined by the QRS complex) and at end systole (timed by a Doppler echocardiogram immediately before the scan).
The tag intersection points at the endocardium and epicardium were digitized, yielding a set of six endocardial and six epicardial points per short- and long-axis slice, as described by Rademakers et al.12 The endocardial and epicardial tag intersection points from the short- and long-axis images were combined to yield three-dimensional coordinates using an algorithm as described by Moore et al13 and Azhari et al11 (Fig 3⇓). Thus, from the combined short- and long-axis images, six tag points at the epicardium and six tag points from the endocardium across three slices yielded a set of data with 36 points per time point. The 36 data points were grouped to yield 12 cuboids (see Fig 3⇓) for each time point.
Finite Strain Analysis
Finite strain analysis, as originally described by Waldman et al2 and adapted to MR tagged data by Azhari et al,11 was applied to the endocardial and epicardial faces of the cuboids. Each face was divided into four triangles and transformed into a regional coordinate system. Strain analysis was applied to each triangle to calculate the circumferential and longitudinal strains (Fig 3⇑). Subsequently, the principal strain was calculated, defined as the magnitude and direction of maximal shortening. The direction of the principal strain was expressed as an angle with respect to the circumferential direction. A negative sign for strain values indicates shortening.
Estimation of Fiber and Cross-Fiber Shortening
Representative anatomic fiber angles were obtained from autopsy specimens from nine patients who died of noncardiac causes with normal hearts and nine patients with IDC confirmed at autopsy. All hearts were fixed overnight in a distended state by introducing formalin into the cavities at 30 to 40 cm H2O while the entire heart was immersed in formalin.3 The age at death for the autopsied cardiomyopathy patients was 45±7 years, and the weight of the hearts was 705±156 g. The hearts were sliced along three equally spaced transverse sections aligned so that the plane of the sections was parallel to the AV groove,3 in a similar fashion to the method used for the selection of the short-axis MR images. Two layers were therefore obtained that measured 1.5 to 2.5 cm in the long-axis direction, depending on the size of the ventricle. These two layers were each divided into 6 cuboids by three equally spaced radial dissection planes that intersected at the center of the left ventricle, in a similar fashion to the method used to define the long-axis imaging planes. The first cuboid was defined by the radial cut from the mid interventricular septum to the anterior wall, and cuboids 2 to 6 were defined in a clockwise direction around the short axis of the left ventricle when viewed from apex to base. Cuboids 7 to 12 were arranged in the same format, though in the second, more apical short-axis slice. These anatomic cuboids, each corresponding to an imaged cuboid, were sectioned parallel to the epicardium. After the outermost 0.5 mm was discarded, the orientation of the fibers with respect to the short-axis plane was identified with the use of a ×7 magnifier containing a protractor graticule. Similarly, fiber orientation was obtained 1 mm inward from the endocardial surface. Fiber angles were expressed as an angle with respect to the short-axis direction.
The mean fiber angles at the epicardial and endocardial faces for each of the 12 cuboids for the normal and IDC hearts were then used to calculate estimated fiber and cross-fiber direction shortening using a method similar to that described by Waldman et al4 and adapted for MR tagged data by Rademakers et al3 (Fig 3⇑).
Thickening was calculated by use of a three-dimensional volume-element method as described and validated by Beyar et al14 and Lima et al.15 The thickness of a cuboid at a given time point was defined as the volume of the cuboid divided by the average surface area of the epicardium and endocardium.
Because angular rotation (torsion angle) is directly proportional to radius and is also affected by long-axis shortening, it is necessary to take these into account when groups with different left ventricular cavity sizes are compared. Angular circumferential-longitudinal shear (shear CL), which is derived from the torsion angle, takes into account both of these factors. This is defined as the difference between the systolic position of an apical tag point and the equivalent tag point on the basal slice as expressed as an angle of which the vertex is the tag point on the basal slice (Fig 4⇓); it is calculated according to the formula used by Buchalter et al16 : shearCL=tan−1[2rsin(t/2)/h], where r is the radius, t is the torsion angle, and h is the distance between the basal and apical slices.
Left Ventricular Mass
Images were acquired for quantification of left ventricular mass during the same session that tagged images were acquired. Five to six short-axis slices spanning the entire left ventricle were acquired, and left ventricular mass was calculated as described by Shapiro et al.17
Statistical analysis compared the differences in strains between the normal control subjects and the patients with IDC, expressed as a mean (±SEM, unless otherwise stated) of the regional endocardial and epicardial strain values. Repeated measures ANCOVA was used to compare the two groups, accounting for each individual’s age, sex, and body surface area. ANOVA was used to compare strains within groups.
Anatomic Fiber Angles
No significant differences in fiber angles between normal hearts and hearts with IDC were found at either the epicardium or endocardium (Figs 5⇓ and 6⇓). There were significant regional differences in fiber angles among the various segments for the normal hearts (epicardium: P=.01; endocardium: P<.05) and only at the epicardium for the IDC hearts (epicardium: P<.05; endocardium: P=NS).
To demonstrate the validity of estimating fiber and cross-fiber shortening with anatomic samples from subjects other than those undergoing the imaging studies, the variability of fiber angle measurements as determined by the mean±SD for each individual cuboid is presented in Table 1⇑. In normal subjects, the variability in measurements is low, with the SD averaging only 5.8° and measuring <10° for all cuboids. In IDC, the variability is slightly higher but still averages only 9°. This low variability among individuals indicates that a reliable mean fiber angle for a strain reference can be obtained and that it is possible to estimate fiber shortening and cross-fiber shortening using as an anatomic reference a group of hearts from subjects other than those being imaged.
Finite Strain Analysis
In normal subjects, the principal strain was −0.18±0.03 and the principal strain angle was 75±12° at the epicardium. In IDC patients, the principal strain at the epicardium was −0.14±0.03 (P<.005; probability values are for normal subjects versus IDC patients unless otherwise stated) and the principal strain angle was 54±13° (P<.01). Thus, in normal subjects, maximal shortening at the epicardium aligns very closely with the anatomic fiber direction. In IDC, the magnitude of maximal shortening at the epicardium is reduced and the direction is more oblique than in normal subjects but still within 20° of the anatomic fiber orientation (Fig 5⇑).
At the endocardium in normal subjects, the principal strain was −0.31±0.03 and the principal strain angle was 6±9°. In IDC patients, the principal strain at the endocardium was −0.24±0.03 (P<.005) and the principal strain angle was 16±10° (P=.08). Thus, the direction of maximal shortening at the endocardium is 76° and 86° from the endocardial fiber angle in normal subjects and IDC patients, respectively, indicating that maximal shortening is oriented at nearly right angles to the anatomic fiber angles in both these groups (Fig 6⇑).
Estimated Fiber and Cross-Fiber Shortening
Epicardial fiber shortening was −0.14±0.01 and −0.08±0.01 in normal subjects and IDC patients, respectively (P<.0001). Endocardial fiber shortening was −0.16±0.01 and −0.09±0.01 in normal subjects and IDC patients, respectively (P<.0001). Thus, fiber shortening was ≈15% in normal subjects and was markedly reduced in IDC. There was a small but significant difference in fiber shortening between the epicardium and endocardium in normal subjects (P<.05) and a similar trend but no significant difference in the IDC patients.
Epicardial cross-fiber shortening was significantly less than epicardial fiber shortening in the normal subjects (P<.0001), although there was no significant difference in the IDC patients (P=NS). Epicardial cross-fiber shortening was −0.08±0.01 in normal subjects and was not significantly different in IDC patients (−0.06±0.01; P=NS). Endocardial cross-fiber shortening was significantly greater than endocardial fiber shortening for both the normal (P<.0001) and IDC groups (P<.05). Endocardial cross-fiber shortening was −0.26±0.01 in normal subjects and −0.15±0.01 in IDC patients (P<.0001).
All strain values, including circumferential shortening, longitudinal shortening, fiber cross-fiber shear strain, and shear CL are presented in Tables 2⇓ and 3⇓. Transmural wall thickening, end-diastolic wall thickness, and left ventricular mass are presented in Table 4⇓.
This study has demonstrated that in normal humans, the direction of maximal deformation aligns with the fiber direction in the epicardium but is perpendicular to the fiber direction in the endocardium. When strain in a coordinate system aligned to the fibers is estimated, cross-fiber shortening is found to be the dominant shortening strain at the endocardium. Fiber shortening in the normal human myocardium is ≈15%, and this is markedly reduced in IDC. The normal transition in fiber orientation through the left ventricular wall is not significantly altered in IDC. Consequently, the anatomic substrate for endocardial cross-fiber shortening is preserved so that although cross-fiber shortening is also reduced in IDC, this is still a dominant endocardial strain.
Shortening of a layer of myocardium in its cross-fiber direction is thought to occur by the rearrangement of those fibers in three-dimensional space.3 4 Because a fiber can generate force only in the direction of its sarcomere orientation, cross-fiber shortening must be driven by contraction of other layers in which fibers are oriented differently. Epicardial fiber shortening, at a mechanical advantage due to its greater radius and with lateral tethering by collagen cross bridges between fiber groups, may be able to force the endocardium to shorten in a direction perpendicular to its anatomic fibers.3 4 Indeed, an association between the extent of epicardial fiber shortening and endocardial cross-fiber shortening has been demonstrated previously.3 Endocardial fibers also shorten in the fiber direction, though to a lesser extent than in the cross-fiber direction. The significance of shortening in two directions is that bundles of fibers must thicken extensively in the third direction to preserve volume. This has been postulated as a mechanism producing marked endocardial thickening, essential for normal ejection.3 Cleavage planes within the myocardium may provide the anatomic substrate for this fiber rearrangement, which results in longitudinal-radial shear.5 Another possible explanation for endocardial cross-fiber shortening is that it merely represents the coming together of endocardial trabeculae. However, at the epicardium, where trabeculae are absent, cross-fiber shortening is still evident both in the canine heart3 4 and in the human heart, as demonstrated here. This suggests that endocardial cross-fiber shortening is the result of rearrangement within the internal structure of the wall.
The present study has shown that the anatomic fiber angles in IDC are not significantly different from those in normal human hearts. Although this has not been demonstrated previously, it is consistent with a previous report18 of human hypertensive cardiomyopathy in which no difference in fiber angles was shown. Thus, the essential anatomic factor necessary for cross-fiber shortening, that is, the transmural transition in fiber orientation, is preserved in these stable patients with IDC. Consequently, endocardial cross-fiber shortening remains a dominant endocardial strain. Whether anatomic fiber angles and endocardial cross-fiber shortening are preserved in all forms of cardiomyopathy, including acute myocarditis, or in patients with a more rapidly progressive course remains to be determined.
Even without a difference in epicardial fiber angle between groups, there was a difference in the angle of epicardial principal strain. The more oblique angle of maximal shortening in ICD patients appears to be due to the preservation of epicardial cross-fiber shortening, which was not significantly reduced despite a 40% reduction in fiber shortening. The reasons for this relative sparing of epicardial cross-fiber shortening are uncertain. As is the case with endocardial cross-fiber shortening, epicardial cross-fiber shortening must be due to shortening at another myocardial layer, presumably the clockwise fibers of the endocardium. We speculate that the preservation of this strain in cardiomyopathy might occur because of a relative increase in endocardial mechanical influence over the epicardium. This increased influence could result from ventricular dilatation, which augments both epicardial and endocardial radii by similar amounts and thereby reduces the ratio of epicardial to endocardial radius. That is, the epicardial and endocardial radii become more similar, and there is a reduction in the usual extent of epicardial dominance. The influence of one layer on the other may thus become more bidirectional.
Fiber shortening in the human left ventricle was found in this study to be ≈15%. Although fiber shortening in the epicardium and the endocardium could not be evaluated in normal subjects before the development of the methods used here, several previous imaging studies have evaluated midwall shortening in normal humans. Because midwall fibers are oriented circumferentially, values of midwall circumferential shortening may approximate fiber shortening. These studies have produced different results. Palmon et al,7 using MRI with spatial modulation of magnetization (SPAMM), a tagging method, reported values of midwall circumferential shortening of 30%, although a more recent study using the same methods found lesser values ranging from 15% to 28%.19 This wide range in normal subjects may relate to differences in global function within the normal range, which also might explain some of the differences among these studies, which used relatively small sample sizes. Aurigemma et al6 used echocardiography to track midwall shortening, with a geometric correction used for different epicardial versus endocardial thickening, and found values of 21%. However, unlike the present work, neither method used data from three dimensions in the calculation of circumferential shortening. Therefore, these studies could not take into account both the effect of differential epicardial versus endocardial thickening and the effect of the considerable shortening that occurs along the long axis in the human left ventricle20 (Fig 2⇑) on circumferential shortening. Through-plane motion due to long-axis shortening results in alteration of the mass of any short-axis slice as myocardium that was not present in diastole moves into the imaging plane in systole.20 The advantages of using a three-dimensional approach have been clearly demonstrated.15
Those limitations are not present in studies of transplanted hearts containing radiopaque beads. Ingels et al21 measured midwall shortening along cords in the circumferential direction in that model and found cord shortening of 14%, in agreement with the current study. Finite strain analysis was used to determine fiber shortening in epicardial and endocardial locations in canine models by Waldman et al4 using bead placement and by Rademakers et al3 using MRI tagging, and values of ≈8% were found. The discrepancy between human data and these canine studies may be related to the administration of anesthesia in the canine model; in studies of conscious pigs, similar strain values to those of normal humans in the present study have been documented.22
The major abnormality in IDC demonstrated in the present study is the marked reduction in fiber shortening at both the epicardium and the endocardium. We demonstrated a small but significant difference in fiber shortening across the left ventricular wall in normal subjects (epicardium −0.14±0.01 versus endocardium −0.16±0.01; P<.05) and a trend in the same direction in IDC patients. Arts et al23 24 suggested that equal fiber shortening at the epicardium and endocardium as a consequence of torsion of the left ventricle results in uniform distribution of muscle fiber stress, fiber shortening, and contractile work across the left ventricular wall.25 In that model of left ventricular mechanics, when torsion is allowed, the transmural differences in sarcomere shortening and end-systolic fiber stress are <16% and 18%, respectively. When torsion is prevented, the transmural differences increase to 32% and 42%. In both normal subjects and IDC patients, the transmural difference in fiber shortening was ≈12% in the present study. Although this difference is significant in the normal subjects, its magnitude is small, and these results are therefore consistent with the hypothesis that there is only minor variation in fiber shortening across the ventricular wall. An essential component of the model of Arts et al23 is the transmural transition in fiber orientations, which produces torsion, which in turn results in uniform fiber shortening. Because fiber orientations are not altered in IDC, this probably explains the maintenance of a relatively uniform transmural fiber shortening in this group.
Quantifying Fiber Angles From Autopsy Specimens
To estimate fiber and cross-fiber shortening, we used anatomic data from autopsy specimens. The extremely low variation in fiber angles among individuals indicates that it is possible to use a reference fiber angle from an autopsied population to estimate fiber and cross-fiber shortening in an individual subject, as we did here. Error could potentially result from incorrect matching of imaged and autopsied regions. However, the regional variation in the anatomic fiber angles is low, so mismatches are unlikely to have affected the estimates of fiber and cross-fiber shortening values significantly. For example, even the unlikely error of mismatching functional data by one whole cuboid (1/6 of the circumference) would result in a maximal possible error of only 7° in normal subjects and 8° in IDC patients. A mismatch between basal and apical halves of the LV would have even less of an effect.
The autopsied cardiomyopathy patients likely had more severe heart failure than our imaged cardiomyopathy population. However, because the fiber angles are the same in normal subjects and those dying of IDC, it is unlikely that our patient population with less severe heart failure has significantly different fiber angles from those measured.
In this study, fiber angles were not modified for any changes that might occur between end systole and end diastole. However, it is known that changes in fiber angles during the cardiac cycle are small,26 so that the error in applying fiber angles measured in diastolic- or systolic-arrested hearts to live hearts is likely to be small. In addition, the postmortem hearts were likely to have arrested in a state somewhere between end diastole and end systole, so the fiber angles measured probably represent an intermediate value.
Finite strain analysis assumes regional homogeneity of deformation and was therefore applied only to deformation of the epicardial and endocardial faces, in which fibers course in a generally uniform direction. Analysis of deformation within the short-axis plane, ie, wall thickening, which occurs in a direction along which fiber orientation and therefore material properties are known to vary, was performed by use of simple geometric methods14 15 rather than finite strain analysis. However, even within the epicardial and endocardial faces, small inhomogeneities might occur, and this represents a potential source of error. The average end-diastolic segment lengths of the endocardial arc, epicardial arc, and long-axis edge of the cuboids were 2.6, 3.0, and 1.8 cm for the normal subjects and 3.0, 3.6, and 2.2 cm for the cardiomyopathy patients. These are greater than in our previous canine studies of deformation using MRI3 11 because imaging additional planes adds imaging time, which is constrained in patients. However, note that beads2 4 21 or other devices27 28 29 implanted for strain analysis in previous invasive canine studies have usually been separated by at least 1 to 2 cm, and in previous human studies, circumferential bead separation was ≈4.75 cm.21 Errors introduced by regional inhomogeneities in the present study are therefore similar to those of prior invasive canine studies and less than those of prior invasive human studies. The noninvasive nature of the method and the ability to analyze data from multiple regions throughout the left ventricle are important advantages of the present study. Marked improvements in both tag density and imaging time are now possible30 and will result in a greater homogeneity and spatial resolution in future work.
Fiber shortening in the normal human myocardium is ≈15% and is similar in the epicardium and endocardium. However, cross-fiber shortening is the dominant strain in the normal human endocardium and exceeds 25%. In stable patients with IDC, fiber shortening is markedly reduced. Also, the transmural transition in anatomic fiber orientations are not significantly altered in these patients, and as a consequence, although cross-fiber shortening is reduced, this is still the dominant endocardial strain. This supports the concept that significant interactions between layers of the human left ventricle occur during systole in both normal subjects and patients with IDC. MR tagging is a promising technique with which regional strains, including fiber shortening and cross-fiber shortening, can be studied noninvasively in humans.
This study was supported by NHLBI grants RO1-HL-46223 (Dr Shapiro) and RO1-HL-43722 (Dr Weiss).
Presented in part at the 66th Scientific Sessions of the American Heart Association, Atlanta, Ga, November 8-11, 1993, and previously published in abstract form (Circulation. 1993;88[pt 2]:I-346).
- Received July 29, 1996.
- Revision received January 28, 1997.
- Accepted February 3, 1997.
- Copyright © 1997 by American Heart Association
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