• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of nihpaAbout Author manuscriptsSubmit a manuscriptNIH Public Access; Author Manuscript; Accepted for publication in peer reviewed journal;
Circ Cardiovasc Imaging. Author manuscript; available in PMC May 1, 2010.
Published in final edited form as:
PMCID: PMC2760045
NIHMSID: NIHMS126604

Diffusion Spectrum MRI Tractography Reveals the Presence of a Complex Network of Residual Myofibers in Infarcted Myocardium

Abstract

Background

Changes in myocardial microstructure are important components of the tissue response to infarction but are difficult to resolve with current imaging techniques. A novel technique, diffusion spectrum MRI tractography (DSI-tractography), was thus used to image myofiber architecture in normal and infarcted myocardium. Unlike diffusion tensor imaging, DSI-tractography resolves multiple myofiber populations per voxel, thus generating accurate 3D tractograms, which we present in the myocardium for the first time.

Methods and Results

DSI-tractography was performed at 4.7 Tesla in excised rat hearts 3 weeks following left coronary artery ligation (n=4), and in 4 age-matched controls. Fiber architecture in the control hearts varied smoothly from endocardium to epicardium, producing a symmetric array of crossing helical structures in which orthogonal myofibers were separated by fibers with intermediate helix angles. Fiber architecture in the infarcted hearts was severely perturbed. The infarct boundary in all cases was highly irregular and punctuated repeatedly by residual myofibers extending from within the infarct to the border zones. In all infarcts longitudinal myofibers extending towards the basal-anterior wall and transversely oriented myofibers extending towards the septum lay in direct contact with each other, forming nodes of orthogonal myofiber intersection or contact.

Conclusions

DSI-tractography resolves 3D myofiber architecture and reveals a complex network of orthogonal myofibers within infarcted myocardium. Mesh-like networks of orthogonal myofibers in infarcted myocardium may resist mechanical remodeling, but likely also increase the risk for lethal re-entrant arrhythmias. DSI-tractography thus provides a new and important readout of tissue injury following myocardial infarction.

Keywords: Myocardial infarction, fiber architecture, MRI, diffusion, myocardium

INTRODUCTION

Methods to determine left ventricular ejection fraction (EF) and the presence of cardiac wall motion abnormalities have become accepted organ-scale indicators of cardiac mechanics and function. However, these measures are limited in their ability to discern the structural basis underlying the development of heart failure and lethal ventricular arrhythmias. There is thus intense interest in the development of non-invasive imaging techniques that provide novel readouts of myocardial structure and function,1 and have the potential to characterize the microstructural response of the myocardium to injury and elucidate potential mechanistic links between molecular and organ scale pathology.1, 2

As demonstrated in pioneering histological studies,3 myofibers in normal myocardium form a series of crossing helical structures, in which the helix angle (angle at which the myofiber spirals around the long axis of the left ventricle) varies smoothly from a left-handed helix (0° to −90°) in the subepicardium to a right-handed helix (0° to 90°) in the subendocardium.3 Alterations in this myofiber pattern following myocardial infarction and in various cardiomyopathies have been detected both histologically and with non-invasive imaging techniques.49 However, current non-invasive imaging techniques are unable to visualize small groups of myofibers as continuous and highly resolved 3-dimensional anatomical entities. Changes in myocardial fiber architecture have thus often been inferred from changes, measured at discrete points in the myocardium, in the average helix angle and the fractional anisotropy of the myofibers in that voxel.49 While this approach has utility,49 the ability to image myofibers as finely resolved 3D tracts would represent a significant advance, and likely provide novel insights into both mechanical and electrical events in the injured myocardium.

Diffusion weighted MRI exploits the preferential diffusion of water along the direction of muscle and nerve fibers.10 Diffusion tensor MRI (DTI) can be used to image the average direction of water diffusion in a voxel, and derive a primary diffusion vector (primary eigenvector) for that voxel.1113 The recent development of diffusion spectrum MRI tractography (DSI-tractography), however, provides a platform to image myocardial fiber architecture with an unheralded level of detail and accuracy.10, 1416 Tractography involves the integration of individual diffusion vectors in a 3-dimensional field to yield continuous individual fibers and has been performed with DTI datasets in the brain, and to a lesser extent in the tongue and heart.1721 Diffusion spectrum MRI (DSI), however, supports the creation of significantly more robust tractograms since it is able to resolve multiple individual diffusion vectors per voxel, rather than only the single composite vector produced by DTI.10, 1416 DSI-tractography in the brain and tongue has resolved complex and converging fiber anatomy with significantly greater accuracy than DTI.10, 1416, 22

In the current study, DSI-tractography resolves, for the first time, 3D myocardial fiber architecture with both high angular and spatial resolution. Moreover, this method provides a platform for the robust visualization of normal myofiber anatomy and the changes in 3D myofiber architecture occurring in infarcted hearts. Using DSI-tractography, we demonstrate a pattern in normal myocardium of crossing helical myofiber tracts, with the helix angle varying smoothly from the endocardium to the epicardium. Following induced myocardial infarction, we observe that the normal architectural pattern is replaced in parts of the infarct by a mesh-like network of orthogonally-oriented residual myofibers, extending from within the infarct to the septal and basal border zones. We propose that this configuration of myofiber anatomy has important implications for both mechanical remodeling and electrical conduction in patients who have suffered a myocardial infarction, and thus has broad clinical and translational relevance.

METHODS

Principles of Diffusion spectrum imaging with tractography (DSI-tractography)

The physical basis of DSI-tractography is described briefly below. The reader interested in a more mathematical description of the technique is referred to the supplementary materials. Diffusion is a physical property, which represents the random translational motion of water molecules in tissue, and is principally affected by the location of diffusional barriers such as membranes or cytoskeletal fibers. In muscular tissue, diffusion is greatest along the direction of individual or populations of muscle fibers due to their elongated and cylindrically symmetric geometry.20, 23 Conversely, diffusion is smallest when normal to the surface of a myofiber.20, 23

DSI acquisitions are assembled by sampling q-space, where q-space is a formalism representing diffusion weighting as a function of the strength and direction of the magnetic field gradient applied during the MRI experiment. Each voxel in physical 3D space has a unique diffusion signature representing the sum of all molecular diffusion events occurring within the indicated tissue. The more a directionally specific diffusion gradient is aligned with the particular fibers in the voxel, the greater the attenuation of the MR signal will be. In contrast to conventional DTI, which involves 6 diffusion encoding gradients, DSI characteristically employs 515 diffusion encoding gradient vectors. Each point in q-space represents the MR signal intensity in the voxel during the application of a particular q-vector. The MR signal is brightest when the q-vector is orthogonal to fiber direction and most attenuated (weakest) when it is applied along the direction of fiber orientation. An inverse Fourier transform of q-space yields a probability density function (PDF) of fiber orientation per voxel and may include multiple local maxima, each denoting a distinct fiber population. By convention, the PDF is converted into an orientation distribution function (ODF) by radially integrating the PDF, producing a probability distribution that is a function of only of fiber angle. The number of directions in which the 3D diffusion function (q-space) is sampled translates into the maximum possible angular resolution of the technique.

Tractography constructs fiber tracts by determining a set of streamlines from the vector directions in the ODF vector field, with intervoxel connectivity determined by a threshold vector angle (< ±17.5° in the current study). The tractography algorithm is constructed such that the tract assumes a path of minimum angular difference. Similarly, if the voxel contains two or more compatible paths, the tract will take that of the least angular difference. Fiber tracts in the myocardium are encoded by the helix or spiral angle they make with the long axis of the left ventricle.

Experimental Protocol

Excised hearts from 4 normal and 4 infarcted adult Sprague-Dawley rats were studied. Infarction was produced by permanent suture ligation of the left anterior descending coronary artery. Following a 3-week interval, the hearts were perfused-fixed and excised under deep surgical anesthesia with pentobarbital. Perfusion-fixation of the myocardium was achieved by canulating the inferior vena cava and infusing a 4% paraformaldehyde solution, following which the excised hearts were stored in a 1% paraformaldehyde solution. The hearts from the age matched control (non-infarcted) rats were perfused-fixed and excised in an identical manner. All experiments were performed in accordance with regulations for the humane care of laboratory animals at our institution.

Diffusion weighted magnetic resonance imaging of the excised hearts was performed on a 4.7T horizontal bore magnet (Biospec 4.7T, Bruker, Billerica MA) equipped with a 400 mT/m (120 mm internal diameter) gradient. The hearts were immersed in Fomblin and imaged with a tailored solenoid radiofrequency coil. A 3D echoplanar (EPI) sequence was used with an isotropic spatial resolution of 0.4 mm and echo time of 39 ms. Diffusion encoding, following the 90° excitation pulse, was produced by two gradient pulses separated by a 180° refocusing pulse. The maximum b-value (diffusion weighting term proportional to the square of the diffusion gradient multiplied by the diffusion time) was chosen to attenuate the myocardial signal completely and was approximately 104. The repetition time (TR) between adjacent q-vectors was adjusted to produce a signal to noise ratio > 100 in the presence of a b-value of zero and ranged from 1000–1500 ms. This resulted in an imaging time (515 q-vectors, no parallel acquisition, TR 1000–1500 ms) of approximately 12 hours for each heart.

Following imaging, the hearts were sectioned for the histological assessment of overall morphology and myofiber orientation, using hematoxylin and eosin and Masson’s trichrome staining. The hearts were cut longitudinally in the 4-chamber (horizontal long axis) orientation in 5 um thick sections beginning on the anterior free wall surface of the left ventricle. A semi-quantitative correlation score between fiber architecture in the infarct by DSI and by histology was derived by two observers. A fiber was assigned a score of 1 if its location and course on the DSI tractograms replicated its histological form extremely closely. If a good but incomplete correlation was seen between DSI and histology the fiber was assigned a score of 0.5, and if no correlation was seen a score of zero. Post-processing of the DSI datasets, including generation of the ODFs and DSI tractograms, was performed using software (Diffusion Toolkit, TrackVis) developed in our center. The tractograms were generated either as projection images of the entire heart or as tomographic reconstructions, where only fibers passing through a prescribed 2D slice (0.4 mm thick) or a spherical region-of-interest (radius ranging from 1–8 voxels) were displayed. Nodes of orthogonal myofiber intersection or contact (NOMIC) were detected by sweeping a 0.27 mm3 (radius equal to 1 voxel) spherical region-of-interest (ROI) across areas of infracted myocardium. A NOMIC was defined at each point where orthogonal myofibers passed through the same 0.27 mm3 ROI, without the presence of intervening myofibers. A minimum spacing of 1 voxel was placed between successive NOMICs.

RESULTS

As shown in Figure 1, DSI-tractography robustly resolved the transmural variation in myofiber helix angle. In normal hearts myofibers in the mid-myocardium were aligned circumferentially around the long axis of the left ventricle (zero helix angle), subendocardial fibers had a positive or right handed helix angle, while myofibers in the subepicardium had a negative or left handed helix angle. The transition in fiber helix angle from endocardium to epicardium occurred in a smooth and symmetric manner, with little dispersion in the helix angle at a given transmural plane.

Figure 1
Transmural variation in myofiber helix angle: The left ventricle is being viewed (A and C–F) from its lateral wall, and (B) in its short axis. Only those fibers intersecting a spherical region-of-interest are displayed in (D–F). Subendocardial ...

Fiber architecture in normal rat myocardium is shown in more detail in Figure 2. Fiber tracts in both the subendocardium (2A, 2B) and subepicardium (2D, 2E) of the lateral wall form convex half-turns of a spiral. However, the fibers in the subendocardium of the lateral wall are aligned from the posterior-base to antero-apex (2F, 2G) forming a positive right-handed helix, and those in the subepicardium (2I, 2J) from the antero-base to the postero-apex forming a negative or left-handed helix. The circumferential fiber tracts in the mid-myocardium formed a single complete turn around the minor axis of the left ventricle on the DSI-tractograms (2C, 2H). The helix angle at identical transmural locations in the septum was equal to that in the lateral wall. However, right-handed fibers in the septum coursed from the antero-base to the postero-apex, and left handed fibers from the postero-base to the antero-apex, completing a loop of their respective helices.

Figure 2
Fiber architecture in a normal rat heart viewed (A–E) from the LV apex and (F–J) from the lateral wall. Fiber tracts in both the subendocardium (A, B) and subepicardium (D, E) form a half-turn of a spiral. However, in the lateral wall, ...

Changes in myofiber architecture in the infarcted hearts were best visualized in an orientation looking down onto the anterior and lateral walls of the left ventricle (Figure 3). In the control hearts a regular network of myofiber sheets, consisting predominantly of subepicardial (yellow-green) and mid-myocardial (blue) fibers, was visualized in this orientation (Figure 3). A profound loss of myofibers was seen in the infarcted myocardium, and myofiber tract length in the entire heart was reduced from 10.5 +/− 0.7 mm in the normal hearts (mean +/− SEM) to 6.9 +/− 0.8 mm in the infarcted hearts (P < 0.05). The infarct boundary in all cases was highly irregular and punctuated at frequent intervals by strands of residual myofibers extending from within the infarct to the basal and septal border zones (Figure 3). Far fewer and significantly smaller strands of residual myofibers extended from the infarct into the border zones at the anterolateral apex (Figure 3). A high degree of correlation (correlation score = 0.79 +/− 0.08) was seen between the myofiber patterns on the DSI-tractograms and the corresponding histological sections through the left ventricles of the infarcted hearts (Figure 3).

Figure 3
Projection DSI-tractograms looking down onto the anterior and anterolateral walls of (A) a normal and (B) an infarcted rat heart. (A) The visualized fibers in the control heart have helix angles consistent with subepicardial (green-yellow) and mid-myocardial ...

In normal myocardium subendocardial fibers and orthogonally oriented mid-subepicardial fibers coursed through completely different transmural planes (separated by myofibers with intermediate helix angles), and thus did not intersect (Figure 4). In all 4 infarcted hearts, however, longitudinally oriented myofibers (pink) extended from within the infarct to the border zones in the basal anterior and lateral walls, and formed a complex network of orthogonal myofibers with transversely oriented mid-myocardial (blue) and subepicardial (green) fibers coursing from within the infarct to the septum (Figure 3, Figure 4). The normal transmural evolution of myofiber helix angle was lost in infarcted myocardium, and replaced by a single composite layer of tissue containing myofiber strands with highly disperse helix angles. The longitudinally oriented myofibers extending from the within the infarcts to the base were characterized by strongly positive helix angles, consistent with residual subendocardial or subendocardial-like myofibers. Moreover, these residual subendocardial-like myofibers were not separated by intervening myofibers from the orthogonal mid-subepicardial myofibers, which coursed from the infarct to the septum. Each infarct was thus characterized by an area where orthogonally-oriented residual myofibers lay in direct contact with each other (Figure 4), forming nodes of orthogonal myofiber intersection or contact (NOMIC). The portion of the infarct zone with myofiber architecture supporting the formation of NOMICs averaged (mean +/− SEM) 33.8 +/− 3.4 % , and was found in the more basal and septal portions of the infarcts, as shown in the infarcted heart in Figure 5. Within this area, an average of 7 +/− 0.7 (mean +/− SEM) NOMICs were present in each of the infarcted hearts.

Figure 4
Presence of a network of orthogonal myofibers in infarcted myocardium. (A, B) Normal heart viewed from (A) its lateral wall and (B) its apex. Subendocardial (pink) and midmyocardial (blue) fibers cross over each other in completely separate transmural ...
Figure 5
(A) Tomographic display showing the basal and septal portions of an infarcted rat heart and the adjacent border zones. Residual myofibers are most frequent in the septal and basal portions of the infarct, and nodes of orthogonal myofiber intersection ...

DISCUSSION

Despite significant advances in delineating the molecular basis of myocardial injury the translation of this knowledge into novel therapies has been slow. A compelling need thus exists to develop novel non-invasive imaging techniques, capable of resolving myocardial pathology at the microstructural and molecular levels, in order to accelerate the translation of this knowledge into the clinical setting.1, 2 We present in this study, the first application of diffusion spectrum MRI (DSI) tractography in the myocardium and show that the technique is able to resolve myocardial fiber architecture in the intact heart with an exceptional level of detail and accuracy. We show, moreover, using DSI that a complex network of residual myofibers is present in infarcted myocardium, and that these fibers form nodes of orthogonal myofiber intersection or contact (NOMIC) within the infarct.

MRI is uniquely able to image muscle and nerve tracts due to its sensitivity to the diffusion of water.10 During diffusion tensor imaging (DTI), 6 diffusion-encoding gradients are applied to determine the direction of preferred diffusion (primary eigenvector), which corresponds to the long axis of myofibers.1113 The mean helix angle in a voxel, derived from a composite primary eigenvector, can be used to approximate the average myofiber orientation in that voxel.49, 11 DTI has been used to demonstrate a loss of right-handed (subendocardial) fibers and a decrease in fiber anisotropy in infarcted myocardium.4, 5, 7 Multivoxel tracts have been constructed in the brain, and to a lesser extent in the tongue and myocardium using DTI.1721 However, DTI is significantly limited in its angular and spatial resolution and cannot fully resolve converging, crossing or complex fiber geometries.10, 1416 DSI, however, is able to resolve multiple distinct fiber populations per voxel and has demonstrated the capacity to visualize complex and intersecting fiber tracts in the tongue and the brain.10, 1416 The ability of DSI-tractography to detect multiple fiber tracts in a single voxel allowed the presence of residual orthogonal myofibers and NOMICs in the infarcted myocardium to be detected in volumes as small as 0.27 mm3 in this study (Figure 4, Figure 5).

The presence of a network of orthogonally-oriented residual myofibers within the infarct is likely to provide tensile strength and resist infarct expansion and remodeling. Far fewer residual myofibers were seen in the apical portions of the infarcts (Figure 5), which may explain the propensity for aneurysm formation in this location. The presence of a network of residual myofibers within an infarct, however, could also constitute a substrate that is highly susceptible to electrical re-entry and ventricular tachycardia.24 The formation of a mesh-like myofiber network within the infarct is thus likely to provide mechanical advantage at the cost of significant electrophysiological risk.

DSI-tractography is a 3D imaging technique in which fiber tracts can be visualized from any orientation and can follow curved trajectories in 3D space. Histological sections, however, are inherently two-dimensional. Moreover, the DSI-tractograms in this study were visualized either as projection images or as 0.4 mm thick tomographic reconstructions, whereas the histological sections were only 5 um thick. A histological section tangential to the myocardium is thus less likely than a DSI-tractogram to visualize both subendocardial and subepicadial fibers. Despite these differences the residual myofibers seen with DSI-tractography in the infarcted hearts were well observed in the corresponding histological sections, with a high degree of correlation between the two techniques (Figure 3, Figure 5).

The effect of tissue fixation on diffusion MRI has been extensively studied.13, 25, 26 Tissue fixation reduces the overall diffusion scalar but does not change the relative magnitudes or directions of the diffusion vectors.25, 26 Although stronger b-values (diffusion gradients) are required following fixation, DTI of fixed tissue has been shown to produce identical fiber orientations and tractograms to those obtained in live and fresh unfixed tissue.25, 26 It has also been suggested that in the myocardium DTI of fixed tissue may produce more accurate data than that obtained in fresh perfused tissue due to the absence of flow artifacts and the ability to obtain data with higher signal to noise.13

The ability of DSI-tractography to resolve complex changes in myofiber architecture in infracted myocardium has been demonstrated in this study. Further study will be needed to determine whether these changes are replicated in large animals and humans, and to fully characterize their electrophysiological impact. Diffusion MRI of the human myocardium has been performed in vivo,4, 27, 28 and a clear pathway to clinical translation of DSI-tractography in the myocardium exists: Scan times in humans will be reduced by the shorter T1 (longitudinal relaxation time) of the myocardium at clinical field strengths and the consequent ability to shorten the repetition time (TR), adjustment of the DSI-algorithm will be performed to achieve adequate spatial and angular resolution with significantly fewer than 515 diffusion-encoding gradients, and highly accelerated parallel acquisitions with 32 and 128 channel cardiac arrays will be used.29

In conclusion, we have applied DSI-tractography ex vivo to image myocardial fiber architecture with an unheralded level of precision. Moreover, the potential of a mesh-like network of orthogonal myofibers to persist in portions of infarcted myocardium has been identified. Our study demonstrates that DSI-tractography has the capacity to robustly identify microstructural changes in myofiber anatomy and provide readouts relevant to both mechanical remodeling and electrical conduction in the diseased ventricle. While further study will be required, DSI-tractography has the potential to become a highly valuable imaging technology in cardiovascular medicine.

Acknowledgements

We thank Yoshiko Iwamoto for assistance with the histological studies.

Funding: This study was supported in part by the following grant from the National Institutes of Health: DES (R01 HL093038 and K08 HL079984), RJG (RO1 DC05604), VJW (RO1 MH64044), and (NCRR P41RR14075) to the Martinos Center for Biomedical Imaging, as well as by the Leducq Foundation (EA, AR).

Footnotes

Muscle fibers in the myocardium spiral around the left ventricle with a helix angle that is determined by their transmural location. This myofiber architecture influences both the mechanical and electrical properties of the left ventricle and is perturbed in injured myocardium. The impact of altered myofiber architecture, however, remains poorly understood in large part because of the difficulty in assessing this in vivo. In the current paper we describe a technique known as Diffusion Spectrum MRI Tractography (DSI-tractography) to image 3D myofiber architecture in vivo. The technique is based on the preferential diffusion of water along myofibers, which creates a detectable change in the MR signal when an appropriate magnetic gradient is applied. DSI-tractography represents a significant advance over previously developed techniques in that multiple fiber populations can be resolved in a single voxel, supporting the construction of robust myofiber tractograms. DSI-tractography was used to image normal and infarcted rat myocardium in this study. We show that a complex network of residual myofibers persists within portions of the infarcted myocardium, linking the infarct zone to the border zone. We show, moreover, that these residual myofibers can form abnormal connections with each other. The use of DSI-tractography could thus provide valuable insights into both electrical and mechanical events in infarcted myocardium. The translation of the technique to humans will require some modifications but is feasible. DSI-tractography thus has the potential to become a highly valuable tool in the cardiovascular imaging armamentarium.

Disclosures: None

REFERENCES

1. Buckberg GD, Weisfeldt ML, Ballester M, Beyar R, Burkhoff D, Coghlan HC, Doyle M, Epstein ND, Gharib M, Ideker RE, Ingels NB, LeWinter MM, McCulloch AD, Pohost GM, Reinlib LJ, Sahn DJ, Sopko G, Spinale FG, Spotnitz HM, Torrent-Guasp F, Shapiro EP. Left ventricular form and function: scientific priorities and strategic planning for development of new views of disease. Circulation. 2004;110:e333–e336. [PubMed]
2. Sosnovik DE, Nahrendorf M, Weissleder R. Molecular magnetic resonance imaging in cardiovascular medicine. Circulation. 2007;115:2076–2086. [PubMed]
3. Streeter DD, Jr, Spotnitz HM, Patel DP, Ross J, Jr, Sonnenblick EH. Fiber orientation in the canine left ventricle during diastole and systole. Circ Res. 1969;24:339–347. [PubMed]
4. Wu MT, Tseng WY, Su MY, Liu CP, Chiou KR, Wedeen VJ, Reese TG, Yang CF. Diffusion tensor magnetic resonance imaging mapping the fiber architecture remodeling in human myocardium after infarction: correlation with viability and wall motion. Circulation. 2006;114:1036–1045. [PubMed]
5. Wu EX, Wu Y, Nicholls JM, Wang J, Liao S, Zhu S, Lau CP, Tse HF. MR diffusion tensor imaging study of postinfarct myocardium structural remodeling in a porcine model. Magn Reson Med. 2007;58:687–695. [PubMed]
6. Helm PA, Younes L, Beg MF, Ennis DB, Leclercq C, Faris OP, McVeigh E, Kass D, Miller MI, Winslow RL. Evidence of structural remodeling in the dyssynchronous failing heart. Circ Res. 2006;98:125–132. [PubMed]
7. Chen J, Song SK, Liu W, McLean M, Allen JS, Tan J, Wickline SA, Yu X. Remodeling of cardiac fiber structure after infarction in rats quantified with diffusion tensor MRI. Am J Physiol Heart Circ Physiol. 2003;285:H946–H954. [PubMed]
8. Tseng WY, Dou J, Reese TG, Wedeen VJ. Imaging myocardial fiber disarray and intramural strain hypokinesis in hypertrophic cardiomyopathy with MRI. J Magn Reson Imaging. 2006;23:1–8. [PubMed]
9. Ripplinger CM, Li W, Hadley J, Chen J, Rothenberg F, Lombardi R, Wickline SA, Marian AJ, Efimov IR. 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. 2007;101:1049–1057. [PMC free article] [PubMed]
10. Hagmann P, Jonasson L, Maeder P, Thiran JP, Wedeen VJ, Meuli R. Understanding diffusion MR imaging techniques: from scalar diffusion-weighted imaging to diffusion tensor imaging and beyond. Radiographics. 2006;26 Suppl 1:S205–S223. [PubMed]
11. Reese TG, Weisskoff RM, Smith RN, Rosen BR, Dinsmore RE, Wedeen VJ. Imaging myocardial fiber architecture in vivo with magnetic resonance. Magn Reson Med. 1995;34:786–791. [PubMed]
12. Hsu EW, Muzikant AL, Matulevicius SA, Penland RC, Henriquez CS. Magnetic resonance myocardial fiber-orientation mapping with direct histological correlation. Am J Physiol. 1998;274:H1627–H1634. [PubMed]
13. Holmes AA, Scollan DF, Winslow RL. Direct histological validation of diffusion tensor MRI in formaldehyde-fixed myocardium. Magn Reson Med. 2000;44:157–161. [PubMed]
14. Wedeen VJ, Hagmann P, Tseng WY, Reese TG, Weisskoff RM. Mapping complex tissue architecture with diffusion spectrum magnetic resonance imaging. Magn Reson Med. 2005;54:1377–1386. [PubMed]
15. Gilbert RJ, Magnusson LH, Napadow VJ, Benner T, Wang R, Wedeen VJ. Mapping complex myoarchitecture in the bovine tongue with diffusion-spectrum magnetic resonance imaging. Biophys J. 2006;91:1014–1022. [PMC free article] [PubMed]
16. Wedeen VJ, Wang RP, Schmahmann JD, Benner T, Tseng WY, Dai G, Pandya DN, Hagmann P, D'Arceuil H, de Crespigny AJ. Diffusion spectrum magnetic resonance imaging (DSI) tractography of crossing fibers. Neuroimage. 2008;41:1267–1277. [PubMed]
17. Hagmann P, Thiran JP, Jonasson L, Vandergheynst P, Clarke S, Maeder P, Meuli R. DTI mapping of human brain connectivity: statistical fibre tracking and virtual dissection. Neuroimage. 2003;19:545–554. [PubMed]
18. Helm P, Beg MF, Miller MI, Winslow RL. Measuring and mapping cardiac fiber and laminar architecture using diffusion tensor MR imaging. Ann N Y Acad Sci. 2005;1047:296–307. [PubMed]
19. Wu EX, Wu Y, Tang H, Wang J, Yang J, Ng MC, Yang ES, Chan CW, Zhu S, Lau CP, Tse HF. Study of myocardial fiber pathway using magnetic resonance diffusion tensor imaging. Magn Reson Imaging. 2007;25:1048–1057. [PubMed]
20. Peyrat JM, Sermesant M, Pennec X, Delingette H, Xu C, McVeigh ER, Ayache N. A computational framework for the statistical analysis of cardiac diffusion tensors: application to a small database of canine hearts. IEEE Trans Med Imaging. 2007;26:1500–1514. [PubMed]
21. Rohmer D, Sitek A, Gullberg GT. Reconstruction and visualization of fiber and laminar structure in the normal human heart from ex vivo diffusion tensor magnetic resonance imaging (DTMRI) data. Invest Radiol. 2007;42:777–789. [PubMed]
22. Gilbert RJ, Wedeen VJ, Magnusson LH, Benner T, Wang R, Dai G, Napadow VJ, Roche KK. Three-dimensional myoarchitecture of the bovine tongue demonstrated by diffusion spectrum magnetic resonance imaging with tractography. Anat Rec A Discov Mol Cell Evol Biol. 2006;288:1173–1182. [PubMed]
23. Tseng WY, Wedeen VJ, Reese TG, Smith RN, Halpern EF. Diffusion tensor MRI of myocardial fibers and sheets: correspondence with visible cut-face texture. J Magn Reson Imaging. 2003;17:31–42. [PubMed]
24. Hooks DA, Trew ML, Caldwell BJ, Sands GB, LeGrice IJ, Smaill BH. Laminar arrangement of ventricular myocytes influences electrical behavior of the heart. Circ Res. 2007;101:e103–e112. [PubMed]
25. Sun SW, Neil JJ, Song SK. Relative indices of water diffusion anisotropy are equivalent in live and formalin-fixed mouse brains. Magn Reson Med. 2003;50:743–748. [PubMed]
26. D'Arceuil HE, Westmoreland S, de Crespigny AJ. An approach to high resolution diffusion tensor imaging in fixed primate brain. Neuroimage. 2007;35:553–565. [PubMed]
27. Dou J, Reese TG, Tseng WY, Wedeen VJ. Cardiac diffusion MRI without motion effects. Magn Reson Med. 2002;48:105–114. [PubMed]
28. Gamper U, Boesiger P, Kozerke S. Diffusion imaging of the in vivo heart using spin echoes--considerations on bulk motion sensitivity. Magn Reson Med. 2007;57:331–337. [PubMed]
29. Schmitt M, Potthast A, Sosnovik DE, Polimeni JR, Wiggins GC, Triantafyllou C, Wald LL. A 128-channel receive-only cardiac coil for highly accelerated cardiac MRI at 3 Tesla. Magn Reson Med. 2008;59:1431–1439. [PMC free article] [PubMed]

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

  • PubMed
    PubMed
    PubMed citations for these articles

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...