Histological validation of myocardial microstructure obtained from diffusion tensor magnetic resonance imaging.

Diffusion tensor magnetic resonance imaging (MRI) is a possible new means of elucidating the anatomic structure of the myocardium. It enjoys several advantages over traditional histological approaches, including the ability to rapidly measure fiber organization in isolated, perfused, arrested hearts, thereby avoiding fixation and sectioning of artifacts. However, quantitative validation of this MRI method has been lacking. Here, fiber orientations estimated in the same locations in the same heart using both diffusion tensor MRI and histology are compared in a total of two perfused rabbit hearts. Fiber orientations were statistically similar for both methods and differed on average by 12 degrees at any single location. This is similar to the 10 degrees uncertainty in fiber orientation achieved with histology. In addition, imaging studies performed in a total of seven hearts support a level of organization beyond the myofiber, the recently described laminar organization of the ventricular myocardium.

[1]  P R Ershler,et al.  Anatomical architecture and electrical activity of the heart. , 1997, Acta cardiologica.

[2]  K K Kwong,et al.  Anisotropy of water diffusion in the myocardium of the rat. , 1994, Circulation research.

[3]  P. Hunter,et al.  Mathematical model of geometry and fibrous structure of the heart. , 1991, The American journal of physiology.

[4]  E. G. J. Olsen,et al.  The Normal Heart , 1987 .

[5]  F. P. Mall,et al.  On the muscular architecture of the ventricles of the human heart , 1911 .

[6]  P S Chen,et al.  Effects of myocardial fiber orientation on the electrical induction of ventricular fibrillation. , 1993, The American journal of physiology.

[7]  I W Hunter,et al.  An anatomical heart model with applications to myocardial activation and ventricular mechanics. , 1992, Critical reviews in biomedical engineering.

[8]  G M Hutchins,et al.  The architecture of the human ventricular myocardium. , 1972, The Johns Hopkins medical journal.

[9]  P. Hunter,et al.  Laminar structure of the heart: ventricular myocyte arrangement and connective tissue architecture in the dog. , 1995, The American journal of physiology.

[10]  E. Hsu,et al.  Analytical expressions for the NMR apparent diffusion coefficients in an anisotropic system and a simplified method for determining fiber orientation , 1995, Magnetic resonance in medicine.

[11]  Dd. Streeter,et al.  Gross morphology and fiber geometry of the heart , 1979 .

[12]  J W Covell,et al.  Transverse shear along myocardial cleavage planes provides a mechanism for normal systolic wall thickening. , 1995, Circulation research.

[13]  D. D. Streeter,et al.  Engineering Mechanics for Successive States in Canine Left Ventricular Myocardium: II. Fiber Angle and Sarcomere Length , 1973, Circulation research.

[14]  A V Panfilov,et al.  Generation of Reentry in Anisotropic Myocardium , 1993, Journal of cardiovascular electrophysiology.

[15]  P. Basser,et al.  Estimation of the effective self-diffusion tensor from the NMR spin echo. , 1994, Journal of magnetic resonance. Series B.

[16]  Maarten R. Drost,et al.  Determination of muscle fibre orientation using Diffusion-Weighted MRI. , 1996 .

[17]  C. Henriquez,et al.  Magnetic resonance myocardial fiber-orientation mapping with direct histological correlation. , 1998, American journal of physiology. Heart and circulatory physiology.

[18]  Hitoshi Matsuzawa,et al.  Three-dimensional anisotropy contrast magnetic resonance imaging of the rat nervous system: MR axonography , 1995, Neuroscience Research.

[19]  J. G. Miller,et al.  Structural Remodeling of Human Myocardial Tissue After Infarction: Quantification With Ultrasonic Backscatter , 1992, Circulation.

[20]  D. Hearse,et al.  Calcium and cardioplegia. The optimal calcium content for the St. Thomas' Hospital cardioplegic solution. , 1984, The Journal of thoracic and cardiovascular surgery.

[21]  R Luypaert,et al.  A method for myelin fiber orientation mapping using diffusion-weighted MR images. , 1994, Magnetic resonance imaging.

[22]  W. Roberts,et al.  Pathologic anatomy of the cardiomyopathies. Idiopathic dilated and hypertrophic types, infiltrative types, and endomyocardial disease with and without eosinophilia. , 1975, Human pathology.

[23]  J. Pekar,et al.  MR color mapping of myelin fiber orientation. , 1991, Journal of computer assisted tomography.

[24]  T. Mareci,et al.  Diffusion anisotropy in excised normal rat spinal cord measured by NMR microscopy. , 1997, Magnetic resonance imaging.

[25]  L Tung,et al.  Spatial distribution of cardiac transmembrane potentials around an extracellular electrode: dependence on fiber orientation. , 1995, Biophysical journal.

[26]  E C Wong,et al.  In vivo determination of the anisotropic diffusion of water and the T1 and T2 times in the rabbit lens by high-resolution magnetic resonance imaging. , 1993, Investigative ophthalmology & visual science.

[27]  Rong Xue,et al.  Delayed reduction of tissue water diffusion after myocardial ischemia. , 1998, American journal of physiology. Heart and circulatory physiology.

[28]  P. Basser,et al.  Diffusion tensor MR imaging of the human brain. , 1996, Radiology.

[29]  AnthonyKanai,et al.  Optical Mapping Reveals That Repolarization Spreads Anisotropically and Is Guided by Fiber Orientation in Guinea Pig Hearts , 1995 .

[30]  G. Hutchins,et al.  Arterial-venous relationships in the human left ventricular myocardium: anatomic basis for countercurrent regulation of blood flow. , 1986, Circulation.

[31]  A. M. Scher,et al.  Influence of Cardiac Fiber Orientation on Wavefront Voltage, Conduction Velocity, and Tissue Resistivity in the Dog , 1979, Circulation research.

[32]  F W Prinzen,et al.  Regional fibre stress : fibre strain area as an estimate of regional blood flow and oxygen demand in the canine heart , 2005 .

[33]  G Olivetti,et al.  Side-to-side slippage of myocytes participates in ventricular wall remodeling acutely after myocardial infarction in rats. , 1990, Circulation research.

[34]  R. Lux,et al.  Effect of Myocardial Fiber Direction on Epicardial Potentials , 1994, Circulation.

[35]  V. P. Chacko,et al.  Oxygenation in the rabbit myocardium: assessment with susceptibility-dependent MR imaging. , 1993, Radiology.

[36]  J. Covell,et al.  Relation Between Transmural Deformation and Local Myofiber Direction in Canine Left Ventricle , 1988, Circulation research.

[37]  A. Grimm,et al.  Fiber bundle direction in the mammalian heart. An extension of the "nested shells" model. , 1976, Basic research in cardiology.

[38]  F. Tezuka Muscle fiber orientation in normal and hypertrophied hearts. , 1975, The Tohoku journal of experimental medicine.

[39]  G A Johnson,et al.  Diffusion‐weighted MR microscopy with fast spin‐echo , 1993, Magnetic resonance in medicine.

[40]  C F Hazlewood,et al.  Nuclear magnetic resonance measurement of skeletal muscle: anisotrophy of the diffusion coefficient of the intracellular water. , 1976, Biophysical journal.

[41]  J. E. Tanner,et al.  Spin diffusion measurements : spin echoes in the presence of a time-dependent field gradient , 1965 .

[42]  J. Ross,et al.  Fiber Orientation in the Canine Left Ventricle during Diastole and Systole , 1969, Circulation research.

[43]  M. Lev,et al.  Architecture of the human ventricular myocardium; technic for study using a modification of the Mall-MacCallum method. , 1956, Laboratory investigation; a journal of technical methods and pathology.

[44]  F W Prinzen,et al.  Adaptation of cardiac structure by mechanical feedback in the environment of the cell: a model study. , 1994, Biophysical journal.

[45]  C W Balke,et al.  Interaction of fiber orientation and direction of impulse propagation with anatomic barriers in anisotropic canine myocardium. , 1988, Circulation.

[46]  T. Koide,et al.  Hypertrophic cardiomyopathy without asymmetric hypertrophy. , 1982, British heart journal.

[47]  R. Dinsmore,et al.  Imaging myocardial fiber architecture in vivo with magnetic resonance , 1995, Magnetic resonance in medicine.

[48]  A D McCulloch,et al.  Transmural distribution of three-dimensional strain in the isolated arrested canine left ventricle. , 1991, The American journal of physiology.