Comparison of diffusion tensor imaging by cardiovascular magnetic resonance and gadolinium enhanced 3D image intensity approaches to investigation of structural anisotropy in explanted rat hearts

Journal of Cardiovascular Magnetic Resonance

Volumn 17, Issue 1, 2015, Pages

  Bernus, Olivier ^a   Radjenovic, Aleksandra ^b   Trew, Mark L ^c   Legrice, Ian J ^c,d   Sands, Gregory B ^c   Magee, Derek R ^e   Smaill, Bruce H ^c,d   Gilbert, Stephen H ^f  

^a UNIVERSITÉ DE BORDEAUX   (France)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

^c UNIVERSITY OF AUCKLAND   (New Zealand)

^d UNIVERSITY OF AUCKLAND   (New Zealand)

^e UNIVERSITY OF LEEDS   (United Kingdom)

^f MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

Cardiovascular magnetic resonance; Diffusion tensor imaging; Myocardium; Myolaminar

Indexed keywords

GADOLINIUM PENTETATE; CONTRAST MEDIUM;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANISOTROPY; ARTICLE; CARDIOVASCULAR MAGNETIC RESONANCE; COMPARATIVE STUDY; DIFFUSION TENSOR IMAGING; EXPLANT; HEART LEFT VENTRICLE; HEART MUSCLE CELL; IMAGE ANALYSIS; IMAGE PROCESSING; MALE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SCANNER; PRIORITY JOURNAL; RAT; SENSITIVITY ANALYSIS; STRUCTURE ANALYSIS; THREE DIMENSIONAL IMAGING; ANIMAL; CARDIAC MUSCLE CELL; COMPUTER ASSISTED DIAGNOSIS; CYTOLOGY; HEART CONTRACTION; HEART LEFT VENTRICLE FUNCTION; ISOLATED HEART; NUCLEAR MAGNETIC RESONANCE IMAGING; PREDICTIVE VALUE; PROCEDURES; WISTAR RAT;

ANIMALS; CONTRAST MEDIA; DIFFUSION TENSOR IMAGING; GADOLINIUM DTPA; IMAGE INTERPRETATION, COMPUTER-ASSISTED; IMAGING, THREE-DIMENSIONAL; ISOLATED HEART PREPARATION; MAGNETIC RESONANCE IMAGING; MALE; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; PREDICTIVE VALUE OF TESTS; RATS, WISTAR; VENTRICULAR FUNCTION, LEFT;

EID: 84928579331     PISSN: 10976647     EISSN: 1532429X     Source Type: Journal    
DOI: 10.1186/s12968-015-0129-x     Document Type: Article

References (65)

1. LeGrice IJ, Pope AJ, Sands GB, Whalley G, Doughty RN, Smaill BH. Progression of myocardial remodeling and mechanical dysfunction in the spontaneously hypertensive rat. Am J Physiol Heart Circ Physiol. 2012;303:H1353-65.
2. 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:e103-12.
3. Sands GB, Gerneke DA, Hooks DA, Green CR, Smaill BH, Legrice IJ. Automated imaging of extended tissue volumes using confocal microscopy. Microsc Res Tech. 2005;67:227-39.
4. Trew ML, Caldwell BJ, Sands GB, Hooks DA, Tai DC, Austin TM, et al. Cardiac electrophysiology and tissue structure: bridging the scale gap with a joint measurement and modelling paradigm. Exp Physiol. 2006;91:355-70. Epub 2006 Jan 2023.
5. Caldwell BJ, Trew ML, Sands GB, Hooks DA, LeGrice IJ, Smaill BH. Three distinct directions of intramural activation reveal nonuniform side-to-side electrical coupling of ventricular myocytes. Circ Arrhythm Electrophysiol. 2009;2:433-40. Epub 2009 Jun 2018.
6. Pope AJ, Sands GB, Smaill BH, LeGrice IJ. Three-dimensional transmural organization of perimysial collagen in the heart. Am J Physiol Heart Circ Physiol. 2008;295:H1243-H1252. Epub 2008 Jul 1218.
7. Hales PW, Schneider JE, Burton RA, Wright BJ, Bollensdorff C, Kohl P. Histo-anatomical structure of the living isolated rat heart in two contraction states assessed by diffusion tensor MRI. Prog Biophys Mol Biol. 2012;110:319-30.
8. Gilbert SH, Benson AP, Li P, Holden AV. Regional localisation of left ventricular sheet structure: integration with current models of cardiac fibre, sheet and band structure. Eur J Cardiothorac Surg. 2007;32:231-49.
9. Costa KD, Takayama Y, McCulloch AD, Covell JW. Laminar fiber architecture and three-dimensional systolic mechanics in canine ventricular myocardium. Am J Physiol. 1999;276:H595-607.
10. Dokos S, Smaill BH, Young AA, LeGrice IJ. Shear properties of passive ventricular myocardium. Am J Physiol Heart Circ Physiol. 2002;283:H2650-9.
11. Gilbert SH, Benoist D, Benson AP, White E, Tanner SF, Holden AV, et al. Visualization and quantification of whole rat heart laminar structure using high-spatial resolution contrast-enhanced MRI. Am J Physiol Heart Circ Physiol. 2012;302:H287-98.
12. LeGrice IJ, Smaill BH, Chai LZ, Edgar SG, Gavin JB, Hunter PJ. Laminar structure of the heart: ventricular myocyte arrangement and connective tissue architecture in the dog. Am J Physiol. 1995;269:H571-82.
13. Streeter DD. Vol. I. The heart. Section 2: The cardiovascular system: Gross morphology and fiber geometry of the heart. In: M. BR, editor. Handbook of Physiology Volume 1, Am. Physiol. Soc. Bethesda, MD. 1979. p. 61-112.
14. Colli Franzone P, Guerri L, Taccardi B. Potential distributions generated by point stimulation in a myocardial volume: simulation studies in a model of anisotropic ventricular muscle. J Cardiovasc Electrophysiol. 1993;4:438-58.
15. Trayanova NA. Whole-heart modeling: applications to cardiac electrophysiology and electromechanics. Circ Res. 2011;108:113-28.
16. Wang VY, Lam HI, Ennis DB, Cowan BR, Young AA, Nash MP. Modelling passive diastolic mechanics with quantitative MRI of cardiac structure and function. Med Image Anal. 2009;13:773-84.
17. Eriksson TS, Prassl AJ, Plank G, Holzapfel GA. Modeling the dispersion in electromechanically coupled myocardium. In: International journal for numerical methods in biomedical engineering. 2013.
18. 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:H1627-34.
19. Gilbert SH, Benson AP, Li P, Holden AV. Visualisation of dog myocardial structure from diffusion tensor magnetic resonance imaging: The paradox of uniformity and variability. In: Sachse FBSG, editor. Functional Imaging and Modeling of the Heart, Proceedings. Volume 4466. 2007. p. 403-12. Lecture Notes in Computer Science].
20. Scollan DF, Holmes A, Zhang J, Winslow RL. Reconstruction of cardiac ventricular geometry and fiber orientation using magnetic resonance imaging. Ann Biomed Eng. 2000;28:934-44.
21. 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.
22. Hsu EW, Buckley DL, Bui JD, Blackband SJ, Forder JR. Two-component diffusion tensor MRI of isolated perfused hearts. Magn Reson Med. 2001;45:1039-45.
23. Forder JR, Bui JD, Buckley DL, Blackband SJ. MR imaging measurement of compartmental water diffusion in perfused heart slices. Am J Physiol Heart Circ Physiol. 2001;281:H1280-5.
24. Kohler S, Hiller KH, Waller C, Jakob PM, Bauer WR, Haase A. Visualization of myocardial microstructure using high-resolution T 2 imaging at high magnetic field. Magn Reson Med. 2003;49:371-5.
25. Jähne B. Digital image processing. The Netherlands: Springer-Verlag; 2005.
26. Farid H, Simoncelli EP. Differentiation of Discrete Multidimensional Signals. IEEE Trans Image Process. 2004;13:496-508.
27. Gilbert SH, Sands GB, LeGrice IJ, Smaill BH, Bernus O, Trew ML. A framework for myoarchitecture analysis of high resolution cardiac MRI and comparison with diffusion Tensor MRI. Conference Proceedings. 2012;2012:4063-6.
28. Gilbert SH, Trew ML, Smaill BH, Radjenovic A, Bernus O. Measurement of Myocardial Structure: 3D Structure Tensor Analysis of High Resolution MRI Quantitatively Compared to DT-MRI. Statistical Atlases and Computational Models of the Heart 2012. In in Lect Notes Comput Sc. 2012;7746:207-14.
29. Papadakis NG, Xing D, Huang CL, Hall LD, Carpenter TA. A comparative study of acquisition schemes for diffusion tensor imaging using MRI. J Magn Reson. 1999;137:67-82.
30. Benson AP, Gilbert SH, Li P, Newton SM, Holden AV. Reconstruction and Quantification of Diffusion Tensor Imaging-Derived Cardiac Fibre and Sheet Structure in Ventricular Regions used in Studies of Excitation Propagation. Mathematical Modelling Nat Phenomena. 2008;3:101-30.
31. Marchand P, Marmet L. Binomial smoothing filter: A way to avoid some pitfalls of least-squares polynomial smoothing. Rev Sci Instrum. 1983;54:1034-41.
32. Helm PA, Tseng HJ, Younes L, McVeigh ER, Winslow RL. Ex vivo 3D diffusion tensor imaging and quantification of cardiac laminar structure. Magn Reson Med. 2005;54:850-9.
33. Yoo TS, Ackerman MJ, Lorensen WE, Schroeder W, Chalana V, Aylward S, et al. Engineering and algorithm design for an image processing Api: a technical report on ITK-the Insight Toolkit. Stud Health Technol Inform. 2002;85:586-92.
34. Hsu EW. Myocardial Fiber Orientation Mapping via MR Diffusion Tensor Imaging. In: Joint EMBS-BMES conference; Oct. Houston, TX: IEEE; 2002. p. 1169-70.
35. Chen J, Liu W, Zhang H, Lacy L, Yang X, Song SK, et al. Regional ventricular wall thickening reflects changes in cardiac fiber and sheet structure during contraction: quantification with diffusion tensor MRI. Am J Physiol Heart Circ Physiol. 2005;289:H1898-907.
36. Fisher R. Dispersion on a Sphere. Proc R Soc Lond A Math Phys Sci. 1953;217:295-305.
37. Scheer P, Sverakova V, Doubek J, Janeckova K, Uhrikova I, Svoboda P. Basic values of M-mode echocardiographic parameters of the left ventricle in outbreed Wistar rats. Vet Med. 2012;57:42-52.
38. Helm PA, Younes L, Beg MF, Ennis DB, Leclercq C, Faris OP, et al. Evidence of structural remodeling in the dyssynchronous failing heart. Circ Res. 2006;98:125-32. Epub 2005 Dec 2008.
39. Chen J, Song SK, Liu W, McLean M, Allen JS, Tan J, et al. Remodeling of cardiac fiber structure after infarction in rats quantified with diffusion tensor MRI. Am J Physiol Heart Circ Physiol. 2003;285:H946-954. Epub 2003 May 2022.
40. Kung GL, Nguyen TC, Itoh A, Skare S, Ingels Jr NB, Miller DC, et al. The presence of two local myocardial sheet populations confirmed by diffusion tensor MRI and histological validation. J Magn Reson Imaging. 2011;34:1080-91.
41. Hsu EW, Xue R, Holmes A, Forder JR. Delayed reduction of tissue water diffusion after myocardial ischemia. Am J Physiol. 1998;275:H697-702.
42. Bassingthwaighte JB, Yipintsoi T, Harvey RB. Microvasculature of the dog left ventricular myocardium. Microvasc Res. 1974;7:229-49.
43. Le Bihan D, Breton E, Lallemand D, Grenier P, Cabanis E, Laval-Jeantet M. MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. Radiology. 1986;161:401-7.
44. Kingsley PB, Monahan WG. Selection of the optimum b factor for diffusion-weighted magnetic resonance imaging assessment of ischemic stroke. Magn Reson Med. 2004;51:996-1001.
45. Scott AD, Ferreira PF, Nielles-Vallespin S, Gatehouse P, McGill LA, Kilner P, et al. Optimal diffusion weighting for in vivo cardiac diffusion tensor imaging. Magn Reson Med 2014, In Press.
46. Thickman DI, Kundel HL, Wolf G. Nuclear magnetic resonance characteristics of fresh and fixed tissue: the effect of elapsed time. Radiology. 1983;148:183-5.
47. Holmes AA, Scollan DF, Winslow RL. Direct histological validation of diffusion tensor MRI in formaldehyde-fixed myocardium. Magn Reson Med. 2000;44:157-61.
48. Wu Y, Tepper HL, Voth GA. Flexible simple point-charge water model with improved liquid-state properties. J Chem Phys. 2006;124:024503.
49. Ferreira PF, Kilner PJ, McGill LA, Nielles-Vallespin S, Scott AD, Ho SY, et al. In vivo cardiovascular magnetic resonance diffusion tensor imaging shows evidence of abnormal myocardial laminar orientations and mobility in hypertrophic cardiomyopathy. J Cardiovasc Magn Reson. 2014;16:87.
50. Kim S, Chi-Fishman G, Barnett AS, Pierpaoli C. Dependence on diffusion time of apparent diffusion tensor of ex vivo calf tongue and heart. Magn Reson Med. 2005;54:1387-96.
51. Jiang Y, Pandya K, Smithies O, Hsu EW. Three-dimensional diffusion tensor microscopy of fixed mouse hearts. Magn Reson Med. 2004;52:453-60.
52. Bishop MJ, Plank G. The role of fine-scale anatomical structure in the dynamics of reentry in computational models of the rabbit ventricles. J Physiol. 2012;590:4515-35.
53. Young AA, Legrice IJ, Young MA, Smaill BH. Extended confocal microscopy of myocardial laminae and collagen network. J Microsc. 1998;192:139-50.
54. Smith RM, Matiukas A, Zemlin CW, Pertsov AM. Nondestructive optical determination of fiber organization in intact myocardial wall. Microsc Res Tech. 2008;71:510-6.
55. Haibo N, Castro SJ, Stephenson RS, Jarvis JC, Lowe T, Hart G, et al. Extracting myofibre orientation from micro-CT images: An optimisation study. In: Computing in Cardiology Conference (CinC). 2013. 22-25 Sept. 2013. 2013: 823-826.
56. Varray F, Wang L, Fanton L, Zhu Y-M, Magnin I. High Resolution Extraction of Local Human Cardiac Fibre Orientations. In: Ourselin S, Rueckert D, Smith N, editors. Functional Imaging and Modeling of the Heart. Volume 7945. Springer Berlin Heidelberg: Lecture Notes in Computer Science; 2013. p. 150-7.
57. Lunkenheimer P, Niederer P, Sanchez-Quintana D, Murillo M, Smerup M. Models of Ventricular Structure and Function Reviewed for Clinical Cardiologists. J Cardiovasc Trans Res. 2013;6:176-86.
58. 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.
59. Beg MF, Helm PA, McVeigh E, Miller MI, Winslow RL. Computational cardiac anatomy using MRI. Magn Reson Med. 2004;52:1167-74.
60. Hsu EW, Henriquez CS. Myocardial Fiber Orientation Mapping Using Reduced Encoding Diffusion Tensor Imaging. J Cardiovasc Magn Reson. 2001;3:339-48.
61. Lee SC, Kim K, Kim J, Lee S, Han Yi J, Kim SW, et al. One micrometer resolution NMR microscopy. J Magn Reson. 2001;150:207-13.
62. Geerts L, Bovendeerd P, Nicolay K, Arts T. Characterization of the normal cardiac myofiber field in goat measured with MR-diffusion tensor imaging. Am J Physiol Heart Circ Physiol. 2002;283:H139-45.
63. Dierckx H, Benson AP, Gilbert SH, Ries ME, Holden AV, Verschelde H, et al. Intravoxel Fibre Structure of the Left Ventricular Free Wall and Posterior Left-Right Ventricular Insertion Site in Canine Myocardium Using Q-Ball Imaging. Functional Imaging and Modeling of the Heart, Proceedings. In Lect Notes Comput Sc. 2009;5528:495-504.
64. Scollan DF, Holmes A, Winslow R, Forder J. Histological validation of myocardial microstructure obtained from diffusion tensor magnetic resonance imaging. Am J Physiol. 1998;275:H2308-18.
65. Holmes AA, Scollan DF, Winslow RL. Direct histological validation of diffusion tensor MRI in formaldehyde-fixed myocardium. Magn Reson Med. 2000;44:157-61.