Abstract
Magnetic resonance diffusion tensor imaging (DTI) has greatly facilitated detailed quantifications of myocardial structures. However, structural patterns, such as the distinctive transmural rotation of the fibers, remain incompletely described. To investigate the validity and practicality of pattern-based analysis, 3D DTI was performed on 13 fixed mouse hearts and fiber angles in the left ventricle were transformed and fitted to parametric expressions constructed from elementary functions of the prolate spheroidal spatial variables. It was found that, on average, the myocardial fiber helix angle could be represented to 6.5° accuracy by the equivalence of a product of 10th-order polynomials of the radial and longitudinal variables, and 17th-order Fourier series of the circumferential variable. Similarly, the fiber imbrication angle could be described by 10th-order polynomials and 24th-order Fourier series, to 5.6° accuracy. The representations, while relatively concise, did not adversely affect the information commonly derived from DTI datasets including the whole-ventricle mean fiber helix angle transmural span and atlases constructed for the group. The unique ability of parametric models for predicting the 3D myocardial fiber structure from finite number of 2D slices was also demonstrated. These findings strongly support the principle of parametric modeling for characterizing myocardial structures in the mouse and beyond.
Similar content being viewed by others
References
Abdullah, O. M., S. G. Drakos, N. A. Diakos, O. Wever-Pinzon, A. G. Kfoury, J. Stehlik, C. H. Selzman, B. B. Reid, K. Brunisholz, D. R. Verma, C. Myrick, F. B. Sachse, D. Y. Li, and E. W. Hsu. Characterization of diffuse fibrosis in the failing human heart via diffusion tensor imaging and quantitative histological validation. NMR Biomed. 27(11):1378–1386, 2014.
Alexander, D. C., C. Pierpaoli, P. J. Basser, and J. C. Gee. Spatial transformations of diffusion tensor magnetic resonance images. IEEE Trans. Med. Imaging 20(11):1131–1139, 2001.
Arfken, G. “Prolate Spheroidal Coordinates”, in Mathematical Methods for Physicists (2nd ed.). Orlando: Academic Press, pp. 103–107, 1970.
Arts, T., P. Bovendeerd, T. Delhaas, and F. Prinzen. Modeling the relation between cardiac pump function and myofiber mechanics. J. Biomech. 36(5):731–736, 2003.
Basser, P. J., J. Mattiello, and D. LeBihan. MR diffusion tensor spectroscopy and imaging. Biophys. J. 66(1):259–267, 1994.
Bayer, J. D., R. C. Blake, G. Plank, and N. A. Trayanova. A novel rule-based algorithm for assigning myocardial fiber orientation to computational heart models. Ann. Biomed. Eng. 40(10):2243–2254, 2012.
Borgdorff, M. A. J., B. Bartelds, M. G. Dickinson, P. Steendijk, M. de Vroomen, and R. M. F. Berger. Distinct loading conditions reveal various patterns of right ventricular adaptation. Am. J. Physiol. Heart Circ. Physiol. 305(3):H354–H364, 2013.
Bovendeerd, P. H., T. Arts, J. M. Huyghe, D. H. van Campen, and R. S. Reneman. Dependence of local left ventricular wall mechanics on myocardial fiber orientation: a model study. J. Biomech. 25(10):1129–1140, 1992.
Brook, R. J., and G. C. Arnold. Applied Regression Analysis and Experimental Design. New York: Marcel Dekke, 1985.
Chen, J., S.-K. Song, W. Liu, M. McLean, J. S. Allen, J. Tan, S. A. Wickline, and X. Yu. Remodeling of cardiac fiber structure after infarction in rats quantified with diffusion tensor MRI. Am. J. Physiol. Heart Circ. Physiol. 285(3):946–954, 2003.
Donoho, D. L. Compressed sensing. IEEE Trans. Inf. Theory 52(4):1289–1306, 2006.
Feinberg, D. A., and K. Setsompop. Ultra-fast MRI of the human brain with simultaneous multi-slice imaging. J. Magn. Reson. 229:90–100, 2013.
Gaynor, S. L., H. S. Maniar, J. B. Bloch, P. Steendijk, and M. R. Moon. Right atrial and ventricular adaptation to chronic right ventricular pressure overload. Circulation 112(9 Suppl):I212–I218, 2005.
Geerts, L., P. Bovendeerd, K. Nicolay, and T. Arts. Characterization of the normal cardiac myofiber field in goat measured with MR-diffusion tensor imaging. Am. J. Physiol. Heart Circ. Physiol. 283(1):H139–H145, 2002.
Giannakidis, A., D. Rohmer, A. I. Veress, and G. T. Gulberg. Diffusion. Diffusion tensor magnetic resonance imaging-derived myocardial fiber disarray in hypertensive left ventricular hypertrophy: visualization, quantification and the effect on mechanical function to cite this version, 2012.
Golub, G. H., and C. Reinsch. Singular value decomposition and least squares solutions. Numer. Math. 14(5):403–420, 1970.
Healy, L. J., Y. Jiang, and E. W. Hsu. Quantitative comparison of myocardial fiber structure between mice, rabbit, and sheep using diffusion tensor cardiovascular magnetic resonance. J. Cardiovasc. Magn. Reson. 13(1):74, 2011.
Helm, P. A., L. Younes, M. F. Beg, D. B. Ennis, C. Leclercq, O. P. Faris, E. McVeigh, D. Kass, M. I. Miller, and R. L. Winslow. Evidence of structural remodeling in the dyssynchronous failing heart. Circ. Res. 98(1):125–132, 2006.
Holmes, A., D. F. Scollan, and R. L. Winslow. Direct histological validation of diffusion tensor MRI in formaldehyde-fixed myocardium. Magn. Reson. Med. 44(1):157–161, 2000.
Hsu, E. W., and S. Mori. Analytical expressions for the NMR apparent diffusion coefficients in an anisotropic system and a simplified method for determining fiber orientation. Magn. Reson. Med. 34(2):194–200, 1995.
Hsu, E. W., A. L. Muzikant, S. A. Matulevicius, R. C. Penland, and C. S. Henriquez. Magnetic resonance myocardial fiber-orientation mapping with direct histological correlation. Am. J. Physiol. Heart Circ. Physiol. 274(5 Pt 2):H1627–H1634, 1998.
Jiang, Y., K. Pandya, O. Smithies, and E. W. Hsu. Three-dimensional diffusion tensor microscopy of fixed mouse hearts. Magn. Reson. Med. 52(3):453–460, 2004.
Kanai, A., and G. Salama. Optical mapping reveals that repolarization spreads anisotropically and is guided by fiber orientation in guinea pig hearts. Circ. Res. 77(4):784–802, 1995.
Koay, C. G., L.-C. Chang, J. D. Carew, C. Pierpaoli, and P. J. Basser. A unifying theoretical and algorithmic framework for least squares methods of estimation in diffusion tensor imaging. J. Magn. Reson. 182(1):115–125, 2006.
Kung, G. L., O. M. Ajijola, R. Tung, M. Vaseghi, J. K. Gahm, W. Zhou, A. Mahajan, A. Garfinkel, K. Shivkumar, and D. B. Ennis. Microstructural remodeling in the porcine infarct border zone measured by diffusion tensor and late gadolinium enhancement MRI. Circulation 126(21 Supplement):A14246, 2012.
Larkman, D. J., J. V. Hajnal, A. H. Herlihy, G. A. Coutts, I. R. Young, and G. Ehnholm. Use of multicoil arrays for separation of signal from multiple slices simultaneously excited. J. Magn. Reson. Imaging 13(2):313–317, 2001.
Lombaert, H., J.-M. Peyrat, P. Croisille, S. Rapacchi, L. Fanton, F. Cheriet, P. Clarysse, I. Magnin, H. Delingette, and N. Ayache. Human atlas of the cardiac fiber architecture: study on a healthy population. IEEE Trans. Med. Imaging 31(7):1436–1447, 2012.
Lustig, M., D. Donoho, and J. M. Pauly. Sparse MRI: the application of compressed sensing for rapid MR imaging. Magn. Reson. Med. 58(6):1182–1195, 2007.
Mori, S., K. Oishi, and A. V. Faria. White matter atlases based on diffusion tensor imaging. Curr. Opin. Neurol. 22(4):362–369, 2009.
Peyrat, J.-M., M. Sermesant, X. Pennec, H. Delingette, C. Xu, E. McVeigh, and N. Ayache. Towards a statistical atlas of cardiac fiber structure. Med. Image Comput. Comput. Assist. Interv. 9(Pt 1):297–304, 2006.
Piuze, E., H. Lombaert, J. Sporring, G. J. Strijkers, A. J. Bakermans, and K. Siddiqi. Atlases of cardiac fiber differential geometry. Lecture Notes in Computer Science (including subseries Lecture Notes in Artificial Intelligence and Lecture Notes in Bioinformatics), LNCS, vol. 7945, pp. 442–449, 2013.
Reese, T. G., R. M. Weisskoff, R. N. Smith, B. R. Rosen, R. E. Dinsmore, and V. J. Wedeen. Imaging myocardial fiber architecture in vivo with magnetic resonance. Magn. Reson. Med. 34(6):786–791, 1995.
Ripplinger, C. M., W. Li, J. Hadley, J. Chen, F. Rothenberg, R. Lombardi, S. A. Wickline, A. J. Marian, and I. R. Efimov. Enhanced transmural fiber rotation and connexin 43 heterogeneity are associated with an increased upper limit of vulnerability in a transgenic rabbit model of human hypertrophic cardiomyopathy. Circ. Res. 101(10):1049–1057, 2007.
Rohmer, D., A. Sitek, and G. T. Gullberg. Reconstruction and visualization of fiber and laminar structure in the normal human heart from ex vivo diffusion tensor magnetic resonance imaging. Investig. Radiol. 42(11):777–789, 2007.
Schmitt, B., K. Fedarava, J. Falkenberg, K. Rothaus, N. K. Bodhey, C. Reischauer, S. Kozerke, B. Schnackenburg, D. Westermann, P. P. Lunkenheimer, R. H. Anderson, F. Berger, and T. Kuehne. Three-dimensional alignment of the aggregated myocytes in the normal and hypertrophic murine heart. J. Appl. Physiol. 107(3):921–927, 2009.
Scollan, D. F., A. Holmes, R. Winslow, J. Forder, S. H. Gilbert, D. Benoist, A. P. Benson, E. White, S. F. Tanner, A. V. Holden, H. Dobrzynski, O. Bernus, A. Radjenovic, A. J. Physiol, H. Circ, E. K. Englund, C. P. Elder, Q. Xu, Z. Ding, B. M. Damon, R. Integr, C. Physiol, B. Schmitt, K. Fedarava, J. Falkenberg, K. Rothaus, N. K. Bodhey, S. Kozerke, B. Schnackenburg, D. Westermann, P. Paul, R. H. Anderson, F. Berger, and T. Kuehne. Histological validation of myocardial microstructure obtained from diffusion tensor magnetic resonance imaging. Am. J. Physiol. Heart Circ. Physiol. 275:H2308–H2318, 1998.
Streeter, D. D., H. M. Spotnitz, D. P. Patel, J. Ross, and E. H. Sonnenblick. Fiber orientation in the canine left ventricle during diastole and systole. Circ. Res. 24(3):339–347, 1969.
Toussaint, N., C. T. Stoeck, T. Schaeffter, S. Kozerke, M. Sermesant, and P. G. Batchelor. In vivo human cardiac fibre architecture estimation using shape-based diffusion tensor processing. Med. Image Anal. 17(8):1243–1255, 2013.
Vercauteren, T., X. Pennec, A. Perchant, and N. Ayache. Symmetric log-domain diffeomorphic registration: a demons-based approach. Med. Image Comput. Comput. Assist. Interv. 11(Pt 1):754–761, 2008.
Welsh, C. L., E. V. R. Dibella, G. Adluru, and E. W. Hsu. Model-based reconstruction of undersampled diffusion tensor k-space data. Magn. Reson. Med. 70(2):429–440, 2013.
Wu, M. T., M. Y. Su, Y. L. Huang, K. R. Chiou, P. Yang, H. B. Pan, T. G. Reese, V. J. Wedeen, and W. I. Tseng. Sequential changes of myocardial microstructure in patients postmyocardial infarction by diffusion-tensor cardiac MR: correlation with left ventricular structure and function. Circ. Cardiovasc. Imaging 2(1):32–40, 2009.
Wu, E. X., Y. Wu, J. M. Nicholls, J. Wang, S. Liao, S. Zhu, C.-P. P. Lau, and H.-F. F. Tse. MR diffusion tensor imaging study of postinfarct myocardium structural remodeling in a porcine model. Magn. Reson. Med. 58(4):687–695, 2007.
Wu, D., J. Xu, M. T. McMahon, P. C. M. van Zijl, S. Mori, F. J. Northington, and J. Zhang. In vivo high-resolution diffusion tensor imaging of the mouse brain. Neuroimage 83:18–26, 2013.
Zhang, L., J. Allen, L. Hu, S. D. Caruthers, S. A. Wickline, and J. Chen. Cardiomyocyte architectural plasticity in fetal, neonatal, and adult pig hearts delineated with diffusion tensor MRI.”. Am. J. Physiol. Heart Circ. Physiol. 304(2):H246–H252, 2013.
Acknowledgements
The authors would like to thank Brian Watson for laboratory assistance, and Osama Abdullah and Dr. S. Joshi for their technical discussion. This work was supported by National Institutes of Health (NIH) Grants R01 HL092055 and S10 RR023017.
Author information
Authors and Affiliations
Corresponding author
Additional information
Associate Editor Joel D. Stitzel oversaw the review of this article.
Appendix
Appendix
Representations of the Standardized Prolate Spheroidal LV Geometry
Based on the general equation of an upright prolate spheroidal surface with longitudinal radius a and transverse radius b in Cartesian coordinates,
as depicted in Fig. 5, the geometry of the LV was approximated by a constant-thickness volume consisting of concentric prolate spheroidal shells specified by,
where τ ∈ [0, 1] was the transmural distance variable, a 1 and b 1 were the outer longitudinal and transverse radii, a 2 and b 2 were the inner radii, and \(w = a_{1} - a_{2} = b_{1} - b_{2}\) was the wall thickness of the volume.
The Cartesian coordinates of a prolate spheroid could be alternatively represented using the spherical radial μ, circumferential ψ and azimuthal ν coordinate variables and focal distance ρ according to :3
Using trigonometric manipulation, the above 3 equations were combined and reduced to
By comparing Eq. (13) to Eq. (9), the spherical coordinates of all points in the above prolate spheroidal LV volume were found by first determining \(\mu\) and ρ according to
followed by ψ and ν through
In the spherical coordinate system, the local tangential basis vectors, \(\hat{c}\), \(\hat{l}\) and \(\hat{n}\) in the circumferential, longitudinal and normal (or radial) directions, respectively, were then computed according to
Mapping of the Standardized Geometry to Specimen-Specific Anatomy
The standardized prolate spheroidal volume was mapped to the specimen-specific anatomy by first determining the size-related parameters in Eq. (9). As also shown in Fig. 5, since the entire transverse axis radii lay in the equatorial plane, b 1 and b 2 were respectively estimated from the areas A 1 of the LV (with filled cavity) and A 2 of its cavity in the mid-ventricular cardiac short-axis slice, according to,
The wall thickness w was computed from \(w = b_{1} - b_{2}\). The distance from the equatorial slice to the cardiac apex was taken to be the outer longitudinal axis length a 1.
Since the prolate spheroidal shape was only an approximation of the actual LV anatomy, a one-to-one and invertible mapping between the two was obtained by registering the former to the latter via diffeomorphic demons.39 For computing the local myocardial fiber orientation quantities (e.g., the helix angle) while ensuring orthogonality of the reference axes, the rotational component of the diffeomorphic transformation was used to map2 the tangential basis vectors, \(\hat{c}\), \(\hat{l}\) and \(\hat{n}\), for each point in the prolate spheroidal volume onto the anatomical space.
Finally, to account for size variability among hearts and facilitate numerical modeling as polynomials, the radial coordinate variable (μ, originally spanning [\(\tanh^{ - 1} \left( {b_{1} /a_{1} } \right)\),\(\tanh^{ - 1} \left( {b_{2} /a_{2} } \right)\)]) and azimuthal variable (ν, spanning [0, π]) were both normalized via linear transformation to span the interval [−1, 1].
Rights and permissions
About this article
Cite this article
Merchant, S.S., Gomez, A.D., Morgan, J.L. et al. Parametric Modeling of the Mouse Left Ventricular Myocardial Fiber Structure. Ann Biomed Eng 44, 2661–2673 (2016). https://doi.org/10.1007/s10439-016-1574-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10439-016-1574-x