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MR tagging demonstrates quantitative differences in regional ventricular wall motion in mice, rats, and men

¹Cardiovascular MR Laboratories, Cardiovascular Division, Department of Medicine, and ²Department of Biomedical Engineering, Washington University, St. Louis, Missouri

Submitted 23 September 2005 ; accepted in final form 30 May 2006

	ABSTRACT

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Rats and genetically manipulated mouse models have played an important role in the exploration of molecular causes of cardiovascular diseases. However, it has not been fully investigated whether mice or rats and humans manifest similar patterns of ventricular wall motion. Although similarities in anatomy and myofiber architecture suggest that fundamental patterns of ventricular wall motion may be similar, the considerable differences in heart size, heart rate, and sarcomeric protein isoforms may yield quantitative differences in ventricular wall mechanics. To further our understanding of the basic mechanisms of myofiber contractile performance, we quantified regional and global indexes of ventricular wall motion in mice, rats, and men using magnetic resonance (MR) imaging. Both regular cine and tagged MR images at apical, midventricular, and basal levels were acquired from six male volunteers, six Fischer 344 rats, and seven C57BL/6 mice. Morphological parameters and ejection fraction were computed directly from cine images. Myocardial twist (rotation angle), torsion (net twist per unit length), circumferential strain, and normalized radial shortening were calculated by homogeneous strain analysis from tagged images. Our data show that ventricular twist was conserved among the three species, leading to a significantly smaller torsion, measured as net twist per unit length, in men. However, both circumferential strain and normalized radial shortening were the largest in male subjects. Although other parameters, such as circumferential-longitudinal shear strain, need to be evaluated, and the causes of these differences in contractile mechanics remain to be elucidated, the preservation of twist appears fundamental to cardiac function and should be considered in studies that extrapolate data from animals to humans.

ventricular twist; torsion; regional myocardial wall motion

At the microscopic level, the mammalian LV is composed of obliquely running sheets of fibers that course in a helical spiral from apex to base. Armour and Randall (2) reported a similar arrangement of fiber orientations in nine mammalian species ranging in size from ground squirrel to elephant. A similar structure was also identified in humans from in vivo MRI studies (23). Our own observations using diffusion tensor magnetic resonance (MR) imaging also revealed similar myocardial architecture for both rat (6) and mouse (unpublished observations). These similarities in myofiber architecture suggest that the fundamental patterns of wall motion such as torsion, longitudinal and circumferential shortening, and wall thickening may be similar among mammalian species.

However, there are also considerable differences between humans and rodents at both the microscopic and macroscopic levels. Besides the dramatic differences in scale and hemodynamics, sarcomeric protein composition also differs significantly. In human ventricles, -myosin heavy chain (-MHC) is the predominant isoform, comprising >90% of the total myofibrillar myosin. In contrast, -MHC isoform predominates and comprises >95% of the total myofibrillar myosin protein in the ventricles of mice and rats (9, 27). The relative distribution of the -MHC and -MHC isoforms in the myocardium may lead to different phenotypic expression of cardiac diseases, as was demonstrated in two recent studies of transgenic rabbit models of altered sarcomeric proteins (17, 25). It is possible that such different phenotypic expression may arise from the differences in ventricular wall mechanics due to the differences in the distribution of sarcomeric protein isoforms.

Indeed, the comparability of ventricular function between humans and mice has been controversial. It was reported previously that left ventricular torsion, a component of normal systolic function, was equal in mice and humans, suggesting a much smaller twist angle in mice than in humans (2° vs. 10°) (16). However, Zhou et al. (29) reported more recently a twist angle around 8° in mice, which was similar to the twist angle observed in humans (around 10°), indicating much larger torsion in mice. Mathematical modeling suggests that torsion may serve to equalize the transmural distribution of myocardial fiber stress (3, 4). Therefore, accurate quantification of torsion, as well as other regional wall motion parameters, is important in elucidating the difference in disease expression between humans and rodent models.

To fully understand the basic wall motion mechanics in mammalian hearts in vivo, we quantified regional and global indexes of ventricular wall motion in mice, rats, and men. MR tagging has been shown to yield accurate and reliable quantification of the regional cardiac function in humans (1, 12, 20, 26). With the advance in MR imaging technology and small animal monitoring, it is feasible now to assess the regional wall motion in small animals (8, 11, 16, 19, 29). Accordingly, we used MR tagging to quantify regional and global myocardial wall motion, as well as other morphological features that may alter the motion patterns.

	MATERIALS AND METHODS

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MR imaging of mice and rats. C57BL/6 mice (male, 1.8 ± 0.3 mo; n = 7) and Fischer 344 rats (male, 23.5 ± 1.2 mo; n = 6) underwent MR imaging on a 4.7-T Varian INOVA system (Varian Associates, Palo Alto, CA) equipped with a gradient insert (60 G/cm, 10 cm inner diameter). Surface coils of 2.5 and 5 cm were fabricated for the imaging of mice and rats, respectively. Animals were anesthetized with 0.7–1% isoflurane by a nose cone and placed into the coil in prone position. Electrodes were attached to front paws and right leg for ECG gating and monitoring of vital signs. The animals were kept warm by blowing hot air into the magnet using a blow dryer. The heat flow and the anesthesia level were manually adjusted to maintain the heart rate close to that under conscious conditions. The animal protocol was approved by the Animal Studies Committee of the Washington University Medical Center.

A horizontal long-axis view was acquired perpendicular to the interventricular septum. Three short-axis (SA) slices, parallel to the tricuspid and mitral valve plane, were imaged at basal, midventricular, and apical levels. The midventricular slice was chosen at 50% of the distance between the atrioventricular valve plane and the apex. Basal and apical slices were chosen 2 and 3 mm above and below the midventricular slice in mice and rats, respectively.

Myocardial tagging was performed with two sets of SPAMM1331 sequences, with a total duration of 7 ms, executed sequentially after the detection of R wave to generate stripe tags in two orthogonal directions in one acquisition series. Tagged cine images were acquired with ECG-gated gradient-echo sequence using the following parameters: flip angle, 30°; echo time, 3 ms; data matrix, 256 x 256. The field of view was 4 cm x 4 cm for mice and 6.5 cm x 6.5 cm for rats. The slice thickness was 1 mm for mice and 1.5 mm for rats. Repetition time was adjusted according to the R-R interval of the heart. Fifteen frames were acquired during one cardiac cycle, yielding a temporal resolution of 8 ms in mice and 14 ms in rats. The temporal resolution enabled the coverage of systole with seven or eight frames in rats and six or seven frames in mice. The tag resolution was 0.6 mm for mice and 0.9 mm for rats, allowing three or four tag lines to be placed across the ventricular wall of rats (Fig. 1, A and D) and two or three tag lines for mice (Fig. 1, B and E). The tagged images were zero filled into a 512 x 512 data matrix.

View larger version (116K): [in this window] [in a new window]   Fig. 1. Representative tagged short-axis images from rat (A and D), mouse (B and E), and male patient (C and F) at end diastole (A–C) and end systole (D–F).

MR imaging of men. Healthy male volunteers (11.6 ± 2.7 years; n = 6) recruited from a pediatric clinic at Washington University Medical Center were scanned on a 1.5-T Intera whole body MR system (Philips Medical Systems, Best, The Netherlands). Written informed consent was obtained from each subject’s parent or legal guardian before the study, which was approved by the Institutional Review Board of the Washington University Medical Center. To ensure that data were comparable between subjects, the same imaging protocol used for animals was followed with acquisition parameters scaled for human hearts. Cine images of contiguous SA planes from the mitral valve plane to the apex were obtained with an ECG-gated gradient-echo sequence. Normal cardiac structure and wall motion were confirmed with the standard cine images before tagging. SPAMM sequence was used for tag generation. The tagged images were acquired with the following parameters: flip angle, 50°; echo time, 3–4 ms; field of view, 33 cm x 33 cm; matrix size, 128 x 128; tag resolution, 6 mm; slice thickness 7–8 mm. Repetition time was also adjusted according to the R-R interval such that 20 frames were acquired during one cardiac cycle, yielding a temporal resolution of 37 ms. The tag resolution resulted in two or three tag lines across the ventricular wall (Fig. 1, C and F), and the temporal resolution enabled the coverage of systole with eight or nine frames.

Image analysis. MR images were transferred to a personal computer for data analysis. A MATLAB-based cardiovascular MR image analysis tool package was developed for image analysis (19). Epicardial and endocardial borders were traced interactively in each temporal frame from regular cine images (Fig. 2A). The traced contours from SA slices were used to calculate LV diameter, wall thickness, and the ratio of wall thickness to LV radius. These contours were also stacked to compute LV volume and ejection fraction. End-diastolic frame was defined as the frame immediately after the detection of R wave, i.e., the first frame in the acquisition series. End-systolic frame was defined as the frame that had the minimal LV volume. LV length was measured directly from horizontal long-axis cine images (Fig. 2B). Longitudinal shortening was calculated as the percent change in LV length at end systole compared with that at end diastole.

View larger version (65K): [in this window] [in a new window]   Fig. 2. A: short-axis image of a rat heart overlaid with endocardial and epicardial contours. Red dots are the control points used in B-spline contour tracing. LV, left ventricle. B: horizontal long-axis view of a rat heart. C: short-axis tagged image overlaid with semiautomatically tracked tagging mesh. D: triangulation of the myocardium in homogeneous strain analysis. E: visualization of myocardial wall motion from end diastole to end systole by following the motion of the centroid of each triangular element. F: quantification of myocardial wall motion by quantifying the displacement of the triangular center and the deformation of the triangle. P1 and Pn, vectors from the centroid of the cavity to the centroid of a triangle at phase 1 and n, respectively; , twist angle.

Myocardial twist and radial shortening were computed relative to the center of ventricular cavity with the use of the method outlined in Fogel et al. (12). As shown in Fig. 2F, radial shortening, a measure of the displacement of the centroid of each triangle, was calculated as , where P₁ and P_n are vectors from the centroid of the cavity to the centroid of a triangle at phase 1 and n, respectively. Positive shortening values represented net inward wall motion of each triangle’s centroid toward the ventricular cavity relative to the end-diastolic distance. To account for the differences in heart size among different species, radial shortening was normalized by the LV radius to yield normalized radial shortening (5). Twist angle was defined as the rotation of the centroid of the triangles from end diastole to end systole. Positive twist represented clockwise rotation viewed from base. Net twist angle was defined as the difference between the ventricular twist at apical and basal slices. Torsion was calculated as the net twist angle normalized by the slice separation. Lagrangian strain tensor was computed in each triangle by use of homogeneous strain analysis. This approach assumes that deformations within each triangle are locally homogeneous. Lagrangian strain tensor was further projected onto the circumferential direction to yield circumferential strain.

Statistical analysis. We used unpaired Student’s t-tests for comparisons between two groups. Differences among the three species (men, rats, and mice) were analyzed by ANOVA. All measurements are presented as means ± SD. P values <0.05 were considered statistically significant.

	RESULTS

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Physiological characteristics and LV morphology. Average body weight was 41.2 ± 10.7 kg for men, 429 ± 40 g for rats, and 26 ± 1 g for mice. The body surface area of the male volunteers was in the normal range (1.28 ± 0.21 m²). Smaller species showed increased heart rate: 78 ± 8 beats/min for men, 278 ± 21 beats/min for rats, and 436 ± 63 beats/min for mice. Morphological data and ejection fraction are presented in Table 1. Besides the obvious differences in heart sizes, wall thickness-to-LV radius ratio was significantly smaller in men than in rats and mice (P < 0.001). However, the LV radius-to-length ratio was the same in men and mice, whereas it was significantly larger in rats (P < 0.001), suggesting that rats have a more spherical LV. Despite large variations in body weights and heart sizes, the ejection fraction was similar in mice, rats, and men (P = not significant).

View larger version (14K): [in this window] [in a new window]   Fig. 3. Ventricular twist and torsion in men, rats, and mice. A: LV twist angles at base, midventricle, and apex were similar in all 3 species. B: net twist angles were conserved across the 3 species. C: torsion was significantly smaller in men.

View larger version (21K): [in this window] [in a new window]   Fig. 4. Circumferential strain (A) and normalized radial shortening (B) in men, rats, and mice. *P < 0.05; P < 0.01.

	DISCUSSION

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Our observations of similar twist angles but large torsion in small species are consistent to those reported by Zhou et al. (29). More recently, Gilson et al. (15) quantified twist and torsion in mice with a novel technique called displacement-encoded imaging using stimulated echoes. They also estimated a net twist value of 11° for the entire mouse heart (15). However, Henson et al. (16) reported similar torsion between mice and humans in an earlier study. This discrepancy may stem from the specific methods used to measure ventricular twist. First, end-systolic twist angle was measured in our study, whereas that reported by Henson et al. was the twist angle at 80% of the systole. Also, a higher tagging resolution of 0.6 mm was achieved in mice in our study compared with the 1.2-mm tagging resolution in the study reported by Henson et al. More importantly, although Henson et al. used a DANTE train with 32 pulses for their tagging studies of mice, the present study used a SPAMM1331 tagging sequence that was similar to that used by Zhou et al. (29), resulting in significantly shorter time for the implementation of the tagging sequence. Because the duration of the QRS complex is very short for mice and rats (<20 ms), longer tagging time may delay the subsequent image acquisition such that the first frame is acquired when the heart is already in the contracting state. Accordingly, the acquired reference frame for strain and twist calculation may not be from end diastole.

Although the net twist in mice observed in the present study was similar to that reported in previous studies (15, 29), the calculated torsion was larger because of the differences in torsion calculation. Although both Zhou et al. and Gilson et al. used net twist normalized by LV length as a measure of torsion, we calculated torsion as net twist normalized by the distance between the basal and apical slices. In addition, the distance between apical and basal slices in the study of Gilson et al. was only 3 mm apart, whereas it was 4 mm apart in the present study. Despite these differences, all three studies demonstrated that torsion of the mouse heart is much larger than the torsion in the human heart.

The underlying mechanisms for the observed differences in myocardial wall motion between humans and small animals remain to be elucidated. The ratio of wall thickness to radius was significantly smaller in humans. Because ventricular torsion is due to the contraction of obliquely oriented fibers in competing orientations at the endocardium and epicardium, the epicardium has a mechanical advantage because of a larger moment arm. Therefore, changes in the ratio of wall thickness to radius alone may alter ventricular torsion (28). The smaller wall thickness-to-radius ratio in humans may lead to a relatively smaller mechanical advantage of the epicardial fibers in torsion. On the other hand, torsion is also considered a major mechanism for the ejection of blood. Despite the differences in their body weights and heart sizes, the ejection fraction was similar in mice, rats, and men. The observed enhancement in normal strains in humans seems to have compensated for the reduced torsion in larger species.

Twist per unit length was used as a measure of torsion in the present study to compare our data with previous studies. Such measure is not scale invariant. Because torsion reflects the underlying shearing motion of the myocardium, the CL shear strain can serve as a scale-invariant measure of ventricular torsion. However, such quantification is only available through three-dimensional analysis. Alternatively, to account for the difference in ventricular size, we also evaluated radius x torsion as a unitless measure of torsion; it was largest in rats. Further investigation through mathematical modeling is needed to fully understand the quantitative relationship between torsion and other modes of myocardial deformation. Also, it is not known whether the observed quantitative differences in myocardial deformation may result in different stress distribution. Such difference may play a role in the observed differences in disease progression of different animal models (18, 24).

As in most animal studies, rats and mice were anesthetized during the entire course of MRI scan. The heart rate was lower than those reported in conscious rats and mice, which may lead to depressed contractile behavior of the heart. However, the ejection fraction was similar in mice, rats, and humans in the present study. In addition, our data suggest that not every parameter of myocardial wall motion, e.g., twist and torsion, was reduced in anesthetized mice and rats. Hence, it is unlikely that the observed decrease in circumferential strain and normalized radial shortening in rats and mice is attributable solely to the effects of anesthesia. Also, rats in this study were of an older age group, whereas humans and mice were at about the same maturation stage. Although ventricular morphology and function may change slightly with age, wall thickness-to-radius ratio was similar between mice and rats. In a recent study, Oxenham et al. (22) reported unaltered myocardial strains but slightly increased apical rotation with aging. Net twist in rats was slightly higher than that in mice and humans in the present study (Fig. 3B). However, no statistical significance was detected.

One limitation of the present study is that only two-dimensional tagging analysis was performed. Hence, errors due to the through-plane motion cannot be corrected. In addition, the CL shear, the scale-invariant measure of ventricular torsion, cannot be quantified from two-dimensional tagging. Instead, we used twist per unit length as a measure of torsion for the purpose of interlaboratory comparison. Because torsion is essentially a shear motion in the CL direction, further investigation is needed to examine whether the scale-invariant CL shear is conserved across species. Also, radial strain was not presented in the present study. Compared with circumferential strain, radial strain calculated from strain tensor is more prone to noise because of the limited number of triangular elements in the radial directions. As a result, many investigators focused on circumferential strain only (10, 11, 14). Alternatively, Fogel et al. (12, 13) used radial shortening, i.e., myocardial motion in the radial direction, as a measure of radial wall motion. In this study, we used the scale invariant radial shortening, i.e., radial shortening normalized by LV radius, for interspecies comparison.

In conclusion, we found that ventricular twist, but not torsion, was conserved in mice, rats, and humans. Accordingly, ventricular twist may provide the most direct correlation of contractile parameters in different species. The smaller torsion in larger species may have been compensated by the greater normal strains to generate similar ejection fraction. Although the causes and implications of these differences in contractile behavior remain to be elucidated, the preservation of twist appears fundamental to cardiac function and should be considered in studies that extrapolate observations from rodent to human.

	GRANTS

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The authors acknowledge the support of the Washington University Small Animal Imaging Resource, funded in part through National Cancer Institute Small Animal Imaging Research Program Grant R24 CA-83060. This work was supported by National Heart, Lung, and Blood Institute Grants R01 HL-73315 (X. Yu) and R01 HL-42950 (S. A. Wickline). W. Liu was supported by a predoctoral fellowship from the Heartland Affiliate of the American Heart Association (0215174Z).

	ACKNOWLEDGMENTS

 
The authors thank Dr. Joseph J. H. Ackerman, Director of the Biomedical MR Laboratory (BMRL) at Washington University, for the advice and MR resources. The authors are indebted to Dr. Sheng-Kwei Song who provided invaluable technical assistance.

	FOOTNOTES

 

Address for reprint requests and other correspondence: X. Yu, Dept. of Biomedical Engineering, Case Western Reserve Univ., Wickenden 427, 10900 Euclid Ave., Cleveland, OH 44106 (e-mail: Xin.Yu{at}case.edu)

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

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This Article Abstract Full Text (PDF) All Versions of this Article: 291/5/H2515    most recent 01016.2005v1 Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Web of Science (10) Citing Articles via Google Scholar Google Scholar Articles by Liu, W. Articles by Yu, X. Search for Related Content PubMed PubMed Citation Articles by Liu, W. Articles by Yu, X.