Diffusion MRI in the heart

NMR in Biomedicine

Volumn 30, Issue 3, 2017, Pages

  Mekkaoui, Choukri ^a   Reese, Timothy G ^a   Jackowski, Marcel P ^b   Bhat, Himanshu ^c   Sosnovik, David E ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c Siemens HealthCare   (United States)

Author keywords

diffusion; heart; ischemia; MRI; myocardium; myofiber architecture; tensor; tractography

Indexed keywords

CARDIOLOGY; DIAGNOSIS; DIFFUSION; DISEASES; FILTRATION; HEART; IMAGING TECHNIQUES; PRINCIPAL COMPONENT ANALYSIS; TENSORS;

ISCHEMIA; ISCHEMIC HEART DISEASE; MYOCARDIUM; NON-RIGID DEFORMATION; POST-PROCESSING TECHNIQUES; PULSED GRADIENT SPIN ECHOS; TRACTOGRAPHY; TRANSVERSE RELAXATION TIME;

MAGNETIC RESONANCE IMAGING;

ACCELERATION; CARDIAC GATED IMAGING; CARDIAC MUSCLE; CARDIAC MUSCLE CELL; DIFFUSION; DIFFUSION WEIGHTED IMAGING; DUAL GATED STIMULATED ECHO APPROACH; ELECTRON SPIN RESONANCE; EX VIVO STUDY; HEART FAILURE; HEART INFARCTION; HEART VENTRICLE ARRHYTHMIA; HIGH ANGULAR RESOLUTION DIFFUSION IMAGING; HUMAN; HYPERTROPHIC CARDIOMYOPATHY; IN VIVO STUDY; ISCHEMIC HEART DISEASE; MYOCARDIAL STRAIN; NONHUMAN; PRIORITY JOURNAL; PULSED GRADIENT SPIN ECHO; REVIEW; ANIMAL; CARDIAC IMAGING; DIAGNOSTIC IMAGING; EVIDENCE BASED MEDICINE; HEART; HEART MUSCLE ISCHEMIA; IMAGE ENHANCEMENT; PATHOLOGY; PROCEDURES; REPRODUCIBILITY; SENSITIVITY AND SPECIFICITY;

ANIMALS; CARDIAC IMAGING TECHNIQUES; DIFFUSION MAGNETIC RESONANCE IMAGING; EVIDENCE-BASED MEDICINE; HEART; HUMANS; IMAGE ENHANCEMENT; MYOCARDIAL ISCHEMIA; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY;

EID: 84951309918     PISSN: 09523480     EISSN: 10991492     Source Type: Journal    
DOI: 10.1002/nbm.3426     Document Type: Review

References (79)

1. Edelman RR, Gaa J, Wedeen VJ, Loh E, Hare JM, Prasad P, Li W. In vivo measurement of water diffusion in the human heart. Magn. Reson. Med. 1994; 32(3): 423–428.
2. Reese TG, Wedeen VJ, Weisskoff RM. Measuring diffusion in the presence of material strain. J. Magn. Reson. B 1996; 112(3): 253–258.
3. 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(6): 786–791.
4. 2-mapping of the heart. JACC Cardiovasc. Imaging 2012; 5(12): 1231–1239.
5. 2 mapping. Magn. Reson. Med. 2015; 73(4): 1549–1554.
6. 2 mapping at 3 T. Magn. Reson. Med. 2015; 74(3): 803–816.
7. Lu H, Nagae-Poetscher LM, Golay X, Lin D, Pomper M, van Zijl PC. Routine clinical brain MRI sequences for use at 3.0 Tesla. J. Magn. Reson. Imaging 2005; 22(1): 13–22.
8. Sundgren PC, Dong Q, Gomez-Hassan D, Mukherji SK, Maly P, Welsh R. Diffusion tensor imaging of the brain: review of clinical applications. Neuroradiology 2004; 46(5): 339–350.
9. Sosnovik DE, Mekkaoui C, Huang S, Chen HH, Dai G, Stoeck CT, Ngoy S, Guan J, Wang R, Kostis WJ, Jackowski MP, Wedeen VJ, Kozerke S, Liao R. Microstructural impact of ischemia and bone marrow-derived cell therapy revealed with diffusion tensor magnetic resonance imaging tractography of the heart in vivo. Circulation 2014; 129(17): 1731–1741.
10. Wu MT, Su MY, Huang YL, Chiou KR, Yang P, Pan HB, Reese TG, Wedeen VJ, Tseng WY. Sequential changes of myocardial microstructure in patients postmyocardial infarction by diffusion-tensor cardiac MR: correlation with left ventricular structure and function. Circ. Cardiovasc. Imaging 2009; 2: 32–40.
11. 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(10): 1036–1045.
12. Nguyen C, Fan Z, Xie Y, Dawkins J, Tseliou E, Bi X, Sharif B, Dharmakumar R, Marban E, Li D. In vivo contrast free chronic myocardial infarction characterization using diffusion-weighted cardiovascular magnetic resonance. J. Cardiovasc. Magn. Reson. 2014; 16(1): 68.
13. Sosnovik DE, Wang R, Dai G, Reese TG, Wedeen VJ. Diffusion MR tractography of the heart. J. Cardiovasc. Magn. Reson. 2009; 11: 47.
14. Basser PJ. Inferring microstructural features and the physiological state of tissues from diffusion-weighted images. NMR Biomed. 1995; 8(7/8): 333–344.
15. 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): S205–223.
16. Le Bihan D, Johansen-Berg H. Diffusion MRI at 25: exploring brain tissue structure and function. Neuroimage 2012; 61(2): 324–341.
17. Pierpaoli C, Basser PJ. Toward a quantitative assessment of diffusion anisotropy. Magn. Reson. Med. 1996; 36(6): 893–906.
18. Jones DK. The effect of gradient sampling schemes on measures derived from diffusion tensor MRI: a Monte Carlo study. Magn. Reson. Med. 2004; 51(4): 807–815.
19. 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(3): 339–347.
20. 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(6 Pt 2): H2308–2318.
21. Mekkaoui C, Huang S, Chen HH, Dai G, Reese TG, Kostis WJ, Thiagalingam A, Maurovich-Horvat P, Ruskin JN, Hoffmann U, Jackowski MP, Sosnovik DE. Fiber architecture in remodeled myocardium revealed with a quantitative diffusion CMR tractography framework and histological validation. J. Cardiovasc. Magn. Reson. 2012; 14: 70.
22. Sosnovik DE, Wang R, Dai G, Wang T, Aikawa E, Novikov M, Rosenzweig A, Gilbert RJ, Wedeen VJ. Diffusion spectrum MRI tractography reveals the presence of a complex network of residual myofibers in infarcted myocardium. Circ. Cardiovasc. Imaging 2009; 2(3): 206–212.
23. 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(2 Pt 2): H571–582.
24. LeGrice IJ, Takayama Y, Covell JW. Transverse shear along myocardial cleavage planes provides a mechanism for normal systolic wall thickening. Circ. Res. 1995; 77(1): 182–193.
25. Dou J, Tseng WY, Reese TG, Wedeen VJ. Combined diffusion and strain MRI reveals structure and function of human myocardial laminar sheets in vivo. Magn. Reson. Med. 2003; 50(1): 107–113.
26. 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(1): 31–42.
27. 2 and left-ventricular histo-architecture in the fixed and embedded rat heart. NMR Biomed. 2011; 24(7): 836–843.
28. 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(2/3): 319–330.
29. Bernstein MA, Zhou XJ, Polzin JA, King KF, Ganin A, Pelc NJ, Glover GH. Concomitant gradient terms in phase contrast MR: analysis and correction. Magn. Reson. Med. 1998; 39(2): 300–308.
30. Jezzard P, Barnett AS, Pierpaoli C. Characterization of and correction for eddy current artifacts in echo planar diffusion imaging. Magn. Reson. Med. 1998; 39(5): 801–812.
31. Reese TG, Heid O, Weisskoff RM, Wedeen VJ. Reduction of eddy-current-induced distortion in diffusion MRI using a twice-refocused spin echo. Magn. Reson. Med. 2003; 49(1): 177–182.
32. 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(2): 331–337.
33. Nguyen C, Fan Z, Sharif B, He Y, Dharmakumar R, Berman DS, Li D. In vivo three-dimensional high resolution cardiac diffusion-weighted MRI: a motion compensated diffusion-prepared balanced steady-state free precession approach. Magn. Reson. Med. 2014; 72(5): 1257–1267.
34. Delattre BM, Viallon M, Wei H, Zhu YM, Feiweier T, Pai VM, Wen H, Croisille P. In vivo cardiac diffusion-weighted magnetic resonance imaging: quantification of normal perfusion and diffusion coefficients with intravoxel incoherent motion imaging. Invest. Radiol. 2012; 47(11): 662–670.
35. Dabir D, Child N, Kalra A, Rogers T, Gebker R, Jabbour A, Plein S, Yu CY, Otton J, Kidambi A, McDiarmid A, Broadbent D, Higgins DM, Schnackenburg B, Foote L, Cummins C, Nagel E, Puntmann VO. Reference values for healthy human myocardium using a T1 mapping methodology: results from the International T1 Multicenter cardiovascular magnetic resonance study. J. Cardiovasc. Magn. Reson. 2014; 16: 69.
36. Kawel-Boehm N, Maceira A, Valsangiacomo-Buechel ER, Vogel-Claussen J, Turkbey EB, Williams R, Plein S, Tee M, Eng J, Bluemke DA. Normal values for cardiovascular magnetic resonance in adults and children. J. Cardiovasc. Magn. Reson. 2015; 17: 29.
37. Nielles-Vallespin S, Mekkaoui C, Gatehouse P, Reese TG, Keegan J, Ferreira PF, Collins S, Speier P, Feiweier T, de Silva R, Jackowski MP, Pennell DJ, Sosnovik DE, Firmin D. In vivo diffusion tensor MRI of the human heart: reproducibility of breath-hold and navigator-based approaches. Magn. Reson. Med. 2013; 70(2): 454–465.
38. Stoeck CT, Kalinowska A, von Deuster C, Harmer J, Chan RW, Niemann M, Manka R, Atkinson D, Sosnovik DE, Mekkaoui C, Kozerke S. Dual-phase cardiac diffusion tensor imaging with strain correction. PLoS One 2014; 9(9): e107159.
39. Tunnicliffe EM, Scott AD, Ferreira P, Ariga R, McGill LA, Nielles-Vallespin S, Neubauer S, Pennell DJ, Robson MD, Firmin DN. Intercentre reproducibility of cardiac apparent diffusion coefficient and fractional anisotropy in healthy volunteers. J. Cardiovasc. Magn. Reson. 2014; 16: 31.
40. Froeling M, Strijkers GJ, Nederveen AJ, Luijten PR. Whole heart DTI using asymmetric bipolar diffusion gradients. J. Cardiovasc. Magn. Reson. 2015; 17(Suppl. 1): P15.
41. McNab JA, Edlow BL, Witzel T, Huang SY, Bhat H, Heberlein K, Feiweier T, Liu K, Keil B, Cohen-Adad J, Tisdall MD, Folkerth RD, Kinney HC, Wald LL. The Human Connectome Project and beyond: initial applications of 300 mT/m gradients. Neuroimage 2013; 80: 234–245.
42. Tseng WY, Reese TG, Weisskoff RM, Wedeen VJ. Cardiac diffusion tensor MRI in vivo without strain correction. Magn. Reson. Med. 1999; 42(2): 393–403.
43. Stoeck CT, von Deuster C, Genet M, Atkinson D, Kozerke S. Second-order motion-compensated spin echo diffusion tensor imaging of the human heart. Magn. Reson. Med. 2015; 17(Suppl 1): P81.
44. Welsh C, Di Bella E, Hsu E. Higher-order motion-compensation for in vivo cardiac diffusion tensor imaging in rats. IEEE Trans. Med. Imaging 2015; 34(9): 1843–1853.
45. Jeong EK, Kim SE, Parker DL. High-resolution diffusion-weighted 3D MRI, using diffusion-weighted driven-equilibrium (DW-DE) and multishot segmented 3D-SSFP without navigator echoes. Magn. Reson. Med. 2003; 50(4): 821–829.
46. Wei H, Viallon M, Delattre BM, Moulin K, Yang F, Croisille P, Zhu Y. Free-breathing diffusion tensor imaging and tractography of the human heart in healthy volunteers using wavelet-based image fusion. IEEE Trans. Med. Imaging 2015; 34(1): 306–316.
47. Scott AD, Ferreira PF, Nielles-Vallespin S, Gatehouse P, McGill LA, Kilner P, Pennell DJ, Firmin DN. Optimal diffusion weighting for in vivo cardiac diffusion tensor imaging. Magn. Reson. Med. 2015; 74(2): 420–430.
48. Shemesh N, Ozarslan E, Komlosh ME, Basser PJ, Cohen Y. From single-pulsed field gradient to double-pulsed field gradient MR: gleaning new microstructural information and developing new forms of contrast in MRI. NMR Biomed. 2010; 23(7): 757–780.
49. Axel L, Wedeen VJ, Ennis DB. Probing dynamic myocardial microstructure with cardiac magnetic resonance diffusion tensor imaging. J. Cardiovasc. Magn. Reson. 2014; 16: 89.
50. Reese TG, Benner T, Wang R, Feinberg DA, Wedeen VJ. Halving imaging time of whole brain diffusion spectrum imaging and diffusion tractography using simultaneous image refocusing in EPI. J. Magn. Reson. Imaging 2009; 29(3): 517–522.
51. Setsompop K, Cohen-Adad J, Gagoski BA, Raij T, Yendiki A, Keil B, Wedeen VJ, Wald LL. Improving diffusion MRI using simultaneous multi-slice echo planar imaging. Neuroimage 2012; 63(1): 569–580.
52. Setsompop K, Gagoski BA, Polimeni JR, Witzel T, Wedeen VJ, Wald LL. Blipped-controlled aliasing in parallel imaging for simultaneous multislice echo planar imaging with reduced g-factor penalty. Magn. Reson. Med. 2012; 67(5): 1210–1224.
53. Lau AZ, Tunnicliffe EM, Frost R, Koopmans PJ, Tyler DJ, Robson MD. Accelerated human cardiac diffusion tensor imaging using simultaneous multislice imaging. Magn. Reson. Med. 2015; 73(3): 995–1004.
54. 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(6): 1377–1386.
55. Descoteaux M, Deriche R. High angular resolution diffusion MRI segmentation using region-based statistical surface evolution. J Math Imaging Vis 2009; 33: 239–252.
56. Kung GL, Nguyen TC, Itoh A, Skare S, Ingels NB, Jr, Miller DC, Ennis DB. The presence of two local myocardial sheet populations confirmed by diffusion tensor MRI and histological validation. J. Magn. Reson. Imaging 2011; 34(5): 1080–1091.
57. Cheng YJ, Lang D, Caruthers SD, Efimov IR, Chen J, Wickline SA. Focal but reversible diastolic sheet dysfunction reflects regional calcium mishandling in dystrophic mdx mouse hearts. Am. J. Physiol. Heart Circ. Physiol. 2012; 303(5): H559–568.
58. Strijkers GJ, Bouts A, Blankesteijn WM, Peeters TH, Vilanova A, van Prooijen MC, Sanders HM, Heijman E, Nicolay K. Diffusion tensor imaging of left ventricular remodeling in response to myocardial infarction in the mouse. NMR Biomed. 2009; 22(2): 182–190.
59. 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(3): H946–954.
60. Holmes AA, Scollan DF, Winslow RL. Direct histological validation of diffusion tensor MRI in formaldehyde-fixed myocardium. Magn. Reson. Med. 2000; 44(1): 157–161.
61. 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(10): 1049–1057.
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(1): H139–145.
63. 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(1): 125–132.
64. Smerup M, Nielsen E, Agger P, Frandsen J, Vestergaard-Poulsen P, Andersen J, Nyengaard J, Pedersen M, Ringgaard S, Hjortdal V, Lunkenheimer PP, Anderson RH. The three-dimensional arrangement of the myocytes aggregated together within the mammalian ventricular myocardium. Anat. Rec. 2009; 292(1): 1–11.
65. 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(4): 687–695.
66. 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(7): 1048–1057.
67. 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(5 Pt 2): H1627–1634.
68. Mekkaoui C, Porayette P, Jackowski MP, Kostis WJ, Dai G, Sanders S, Sosnovik DE. Diffusion MRI tractography of the developing human fetal heart. PLoS One 2013; 8(8): e72795.
69. Zhang L, Allen J, Hu L, Caruthers SD, Wickline SA, Chen J. Cardiomyocyte architectural plasticity in fetal, neonatal, and adult pig hearts delineated with diffusion tensor MRI. Am. J. Physiol. Heart Circ. Physiol. 2013; 304(2): H246–252.
70. Ennis DB, Kindlman G, Rodriguez I, Helm PA, McVeigh ER. Visualization of tensor fields using superquadric glyphs. Magn. Reson. Med. 2005; 53(1): 169–176.
71. Schultz T, Kindlmann GL. Superquadric glyphs for symmetric second-order tensors. IEEE Trans. Vis. Comput. Graph. 2010; 16(6): 1595–1604.
72. Huang S, Chen HH, Yuan H, Dai G, Schuhle DT, Mekkaoui C, Ngoy S, Liao R, Caravan P, Josephson L, Sosnovik DE. Molecular MRI of acute necrosis with a novel DNA-binding gadolinium chelate: kinetics of cell death and clearance in infarcted myocardium. Circ. Cardiovasc. Imaging 2011; 4(6): 729–737.
73. Simari RD, Pepine CJ, Traverse JH, Henry TD, Bolli R, Spoon DB, Yeh E, Hare JM, Schulman IH, Anderson RD, Lambert C, Sayre SL, Taylor DA, Ebert RF, Moye LA. Bone marrow mononuclear cell therapy for acute myocardial infarction: a perspective from the cardiovascular cell therapy research network. Circ. Res. 2014; 114(10): 1564–1568.
74. Naumova AV, Modo M, Moore A, Murry CE, Frank JA. Clinical imaging in regenerative medicine. Nat. Biotechnol. 2014; 32(8): 804–818.
75. McGill LA, Ismail TF, Nielles-Vallespin S, Ferreira P, Scott AD, Roughton M, Kilner PJ, Ho SY, McCarthy KP, Gatehouse PD, de Silva R, Speier P, Feiweier T, Mekkaoui C, Sosnovik DE, Prasad SK, Firmin DN, Pennell DJ. Reproducibility of in-vivo diffusion tensor cardiovascular magnetic resonance in hypertrophic cardiomyopathy. J. Cardiovasc. Magn. Reson. 2012; 14: 86.
76. 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): 1–8.
77. Trayanova NA. Whole-heart modeling: applications to cardiac electrophysiology and electromechanics. Circ. Res. 2011; 108(1): 113–128.
78. Froeling M, Strijkers GJ, Nederveen AJ, Chamuleau SA, Luijten PR. Feasibility of in vivo whole heart DTI and IVIM with a 15 minute acquisition protocol. J. Cardiovasc. Magn. Reson. 2014; 16(Suppl. 1): O15.
79. Mekkaoui C, Reese TG, Jackowski MP, Bhat H, Kostis WJ, Sosnovik DE. In vivo fiber tractography of the right and left ventricles using diffusion tensor MRI of the entire human heart. J. Cardiovasc. Magn. Reson. 2014; 16(Suppl. 1): 17.