Fast quantitative susceptibility mapping using 3D EPI and total generalized variation

NeuroImage

Volumn 111, Issue , 2015, Pages 622-630

  Langkammer, Christian ^a,b   Bredies, Kristian ^c   Poser, Benedikt A ^d   Barth, Markus ^e   Reishofer, Gernot ^b   Fan, Audrey Peiwen ^f,g   Bilgic, Berkin ^a   Fazekas, Franz ^b   Mainero, Caterina ^a   Ropele, Stefan ^b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MEDICAL UNIVERSITY OF GRAZ   (Austria)

^c UNIVERSITY OF GRAZ   (Austria)

^d MAASTRICHT UNIVERSITY   (Netherlands)

^e UNIVERSITY OF QUEENSLAND   (Australia)

^f Department of Electrical Engineering and Computer Science   (United States)

^g STANFORD UNIVERSITY   (United States)

Author keywords

Dipole inversion; Iron; Myelin; Quantitative susceptibility mapping; Susceptibility tensor imaging; Total generalized variation; Total variation

Indexed keywords

ANATOMY AND HISTOLOGY; BRAIN; ELECTROMAGNETIC FIELD; HUMAN; IMAGE PROCESSING; NUCLEAR MAGNETIC RESONANCE IMAGING; PROCEDURES;

BRAIN; ELECTROMAGNETIC PHENOMENA; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING;

EID: 84939946198     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2015.02.041     Document Type: Article

References (69)

1. Acosta-Cabronero J., Williams G.B., Cardenas-Blanco A., Arnold R.J., Lupson V., Nestor P.J. In vivo quantitative susceptibility mapping (QSM) in Alzheimer's disease. PLoS One 2013, 8:e81093. 10.1371/journal.pone.0081093.
2. Andersson J.L.R., Skare S., Ashburner J. How to correct susceptibility distortions in spin-echo echo-planar images: application to diffusion tensor imaging. Neuroimage 2003, 20:870-888. 10.1016/S1053-8119(03)00336-7.
3. Argyridis I., Li W., Johnson G.A., Liu C. Quantitative magnetic susceptibility of the developing mouse brain reveals microstructural changes in the white matter. Neuroimage 2013, 88C:134-142. 10.1016/j.neuroimage.2013.11.026.
4. Balla D.Z., Sanchez-Panchuelo R.M., Wharton S.J., Hagberg G.E., Scheffler K., Francis S.T., Bowtell R. Functional quantitative susceptibility mapping (fQSM). Neuroimage 2014, 100:112-124.
5. Bilgic B., Pfefferbaum A., Rohlfing T., Sullivan E.V., Adalsteinsson E. MRI estimates of brain iron concentration in normal aging using quantitative susceptibility mapping. Neuroimage 2012, 59:2625-2635. 10.1016/j.neuroimage.2011.08.077.
6. Bilgic B., Gagoski B.A., Cauley S.F., Fan A.P., Polimeni J.R., Grant P.E., Wald L.L., Setsompop K. Wave-CAIPI for highly accelerated 3D imaging. Magn. Reson. Med. 2014, 00:1-11. 10.1002/mrm.25347.
7. Blazejewska A.I., Al-Radaideh A.M., Wharton S., Lim S.Y., Bowtell R.W., Constantinescu C.S., Gowland P.A. Increase in the iron content of the substantia nigra and red nucleus in multiple sclerosis and clinically isolated syndrome: a 7Tesla MRI study. J. Magn. Reson. Imaging 2014, 10.1002/jmri.24644.
8. Bredies K. Recovering piecewise smooth multichannel images by minimization of convex functionals with total generalized variation penalty. Efficient Algorithms for Global Optimization Methods in Computer Vision 2014, 44-77. Springer.
9. Bredies K., Kunisch K., Pock T. Total generalized variation. SIAM J. Imaging Sci. 2010, 3:492-526. 10.1137/090769521.
10. Chambolle A., Pock T. A first-order primal-dual algorithm for convex problems with applications to imaging. J. Math. Imaging Vis. 2010, 40:120-145. 10.1007/s10851-010-0251-1.
11. Chang H., Fitzpatrick J.M. A technique for accurate magnetic resonance imaging in the presence of field inhomogeneities. IEEE Trans. Med. Imaging 1992, 11:319-329. 10.1109/42.158935.
12. Chen W., Gauthier S.A., Gupta A., Comunale J., Liu T., Wang S., Pei M., Pitt D., Wang Y. Quantitative susceptibility mapping of multiple sclerosis lesions at various ages. Radiology 2014, 271:183-192. 10.1148/radiol.13130353.
13. De Rochefort L., Liu T., Kressler B., Liu J., Spincemaille P., Lebon V., Wu J., Wang Y. Quantitative susceptibility map reconstruction from MR phase data using Bayesian regularization: validation and application to brain imaging. Magn. Reson. Med. 2010, 63:194-206. 10.1002/mrm.22187.
14. Deistung A., Rauscher A., Sedlacik J., Stadler J., Witoszynskyj S., Reichenbach J.R. Susceptibility weighted imaging at ultra high magnetic field strengths: theoretical considerations and experimental results. Magn. Reson. Med. 2008, 60:1155-1168. 10.1002/mrm.21754.
15. Deistung A., Schäfer A., Schweser F., Biedermann U., Turner R., Reichenbach J.R. Toward in vivo histology: a comparison of quantitative susceptibility mapping (QSM) with magnitude-, phase-, and R2*-imaging at ultra-high magnetic field strength. Neuroimage 2013, 65:299-314. 10.1016/j.neuroimage.2012.09.055.
16. Denk C., Hernandez Torres E., MacKay A., Rauscher A. The influence of white matter fibre orientation on MR signal phase and decay. NMR Biomed. 2011, 24:246-252. 10.1002/nbm.1581.
17. Eskreis-winkler S., Schweitzer A.D., Liu T., Chen W., Kaplitt M.G., Tsiouris A.J., Wang Y. Improved subthalamic nucleus depiction with quantitative susceptibility mapping. Radiology 2013, 269:216-223. 10.1148/radiol.13121991.
18. Eskreis-Winkler S., Deh K., Gupta A., Liu T., Wisnieff C., Jin M., Gauthier S.a, Wang Y., Spincemaille P. Multiple sclerosis lesion geometry in quantitative susceptibility mapping (QSM) and phase imaging. J. Magn. Reson. Imaging 2014, 00:1-6. 10.1002/jmri.24745.
19. Fan A.P., Bilgic B., Gagnon L., Witzel T., Bhat H., Rosen B.R., Adalsteinsson E. Quantitative oxygenation venography from MRI phase. Magn. Reson. Med. 2013, 00:1-11. 10.1002/mrm.24918.
20. Haacke E.M., Liu S., Buch S., Zheng W., Wu D., Ye Y. Quantitative susceptibility mapping: current status and future directions. Magn. Reson. Imaging 2014, 33:1-25. 10.1016/j.mri.2014.09.004.
21. Jezzard P., Clare S. Sources of distortion in functional MRI data. Hum. Brain Mapp. 1999, 8:80-85.
22. Kaaouana T., de Rochefort L., Samaille T., Thiery N., Dufouil C., Delmaire C., Dormont D., Chupin M. 2D harmonic filtering of MR phase images in multicenter clinical setting: toward a magnetic signature of cerebral microbleeds. Neuroimage 2014, 104:287-300. 10.1016/j.neuroimage.2014.08.024.
23. Khabipova D., Wiaux Y., Gruetter R., Marques J.P. A modulated closed form solution for quantitative susceptibility mapping - a thorough evaluation and comparison to iterative methods based on edge prior knowledge. Neuroimage 2014, 107:163-174. 10.1016/j.neuroimage.2014.11.038.
24. Knoll F., Bredies K., Pock T., Stollberger R. Second order total generalized variation (TGV) for MRI. Magn. Reson. Med. 2011, 65:480-491. 10.1002/mrm.22595.
25. Knoll F., Clason C., Bredies K., Uecker M., Stollberger R. Parallel imaging with nonlinear reconstruction using variational penalties. Magn. Reson. Med. 2012, 67:34-41. 10.1002/mrm.22964.
26. Knoll F., Schultz G., Bredies K., Gallichan D., Zaitsev M., Hennig J., Stollberger R. Reconstruction of undersampled radial PatLoc imaging using total generalized variation. Magn. Reson. Med. 2013, 70:40-52. 10.1002/mrm.24426.
27. Langkammer C., Schweser F., Krebs N., Deistung A., Goessler W., Scheurer E., Sommer K., Reishofer G., Yen K., Fazekas F., Ropele S., Reichenbach J.R. Quantitative susceptibility mapping (QSM) as a means to measure brain iron? A post mortem validation study. Neuroimage 2012, 62:1593-1599. 10.1016/j.neuroimage.2012.05.049.
28. Langkammer C., Liu T., Khalil M., Enzinger C., Jehna M., Fuchs S., Fazekas F., Wang Y., Ropele S. Quantitative susceptibility mapping in multiple sclerosis. Radiology 2013, 267:551-559. 10.1148/radiol.12120707.
29. Langkammer C., Ropele S., Pirpamer L., Fazekas F., Schmidt R. MRI for iron mapping in Alzheimer's disease. Neurodegener. Dis. 2014, 13:189-191. 10.1159/000353756.
30. Li X., van Zijl P.C.M. Mean magnetic susceptibility regularized susceptibility tensor imaging (MMSR-STI) for estimating orientations of white matter fibers in human brain. Magn. Reson. Med. 2014, 72:610-619. 10.1002/mrm.25322.
31. Li W., Wu B., Avram A.V., Liu C. Magnetic susceptibility anisotropy of human brain in vivo and its molecular underpinnings. Neuroimage 2011, 59:2088-2097. 10.1016/j.neuroimage.2011.10.038.
32. Li W., Wu B., Liu C. Quantitative susceptibility mapping of human brain reflects spatial variation in tissue composition. Neuroimage 2011, 55:1645-1656. 10.1016/j.neuroimage.2010.11.088.
33. Li W., Wu B., Batrachenko A., Bancroft-Wu V., Morey R.a, Shashi V., Langkammer C., De Bellis M.D., Ropele S., Song A.W., Liu C. Differential developmental trajectories of magnetic susceptibility in human brain gray and white matter over the lifespan. Hum. Brain Mapp. 2013, 00:2698-2713. 10.1002/hbm.22360.
34. Li W., Avram A.V., Wu B., Xiao X., Liu C. Integrated Laplacian-based phase unwrapping and background phase removal for quantitative susceptibility mapping. NMR Biomed. 2014, 27:219-227. 10.1002/nbm.3056.
35. Liu C. Susceptibility tensor imaging. Magn. Reson. Med. 2010, 63:1471-1477. 10.1002/mrm.22482.
36. Liu T., Spincemaille P., De Rochefort L., Kressler B., Wang Y. Calculation of susceptibility through multiple orientation sampling (COSMOS): a method for conditioning the inverse problem from measured magnetic field map to susceptibility source image in MRI. Magn. Reson. Med. 2009, 61:196-204. 10.1002/mrm.21828.
37. Liu T., Liu J., de Rochefort L., Spincemaille P., Khalidov I., Ledoux J.R., Wang Y. Morphology enabled dipole inversion (MEDI) from a single-angle acquisition: comparison with COSMOS in human brain imaging. Magn. Reson. Med. 2011, 66:777-783. 10.1002/mrm.22816.
38. Liu T., Surapaneni K., Lou M., Cheng L., Spincemaille P., Wang Y. Cerebral microbleeds: burden assessment by using quantitative susceptibility mapping. Radiology 2011, 262:269-278. 10.1148/radiol.11110251.
39. Lotfipour A.K., Wharton S., Schwarz S.T., Gontu V., Schäfer A., Peters A.M., Bowtell R.W., Auer D.P., Gowland P.A., Bajaj N.P.S. High resolution magnetic susceptibility mapping of the substantia nigra in Parkinson's disease. J. Magn. Reson. Imaging 2012, 35. 10.1002/jmri.22752.
40. Lutti A., Thomas D.L., Hutton C., Weiskopf N. High-resolution functional MRI at 3T: 3D/2D echo-planar imaging with optimized physiological noise correction. Magn. Reson. Med. 2013, 69:1657-1664. 10.1002/mrm.24398.
41. Marques J.P., Bowtell R. Application of a Fourier-based method for rapid calculation of field inhomogeneity due to spatial variation of magnetic susceptibility. Concepts Magn. Reson. Part B: Magn. Reson. Eng. 2005, 25B:65-78. 10.1002/cmr.b.20034.
42. Patenaude B., Smith S.M., Kennedy D.N., Jenkinson M. A Bayesian model of shape and appearance for subcortical brain segmentation. Neuroimage 2011, 56:907-922.
43. Poser B.a, Koopmans P.J., Witzel T., Wald L.L., Barth M. Three dimensional echo-planar imaging at 7Tesla. Neuroimage 2010, 51:261-266. 10.1016/j.neuroimage.2010.01.108.
44. Raven E.P., Lu P.H., Tishler T.A., Heydari P., Bartzokis G. Increased iron levels and decreased tissue integrity in hippocampus of Alzheimer's disease detected in vivo with magnetic resonance imaging. J. Alzheimers Dis. 2013, 37:127-136. 10.3233/JAD-130209.
45. Rudko D.A., Solovey I., Gati J.S., Kremenchutzky M., Menon R.S. Multiple sclerosis: improved identification of disease-relevant changes in gray and white matter by using susceptibility-based MR imaging. Radiology 2014, 272:851-864. 10.1148/radiol.14132475.
46. Sati P., George I.C., Shea C.D., Gaitán M.I., Reich D.S. FLAIR*: a combined MR contrast technique for visualizing white matter lesions and parenchymal veins. Radiology 2012, 265:926-932. 10.1148/radiol.12120208.
47. Sati P., Thomasson D., Li N., Pham D., Biassou N., Reich D., Butman J. Rapid, high-resolution, whole-brain, susceptibility-based MRI of multiple sclerosis. Mult. Scler. 2014, 1-7. 10.1177/1352458514525868.
48. Schäfer A., Forstmann B.U., Neumann J., Wharton S., Mietke A., Bowtell R., Turner R. Direct visualization of the subthalamic nucleus and its iron distribution using high-resolution susceptibility mapping. Hum. Brain Mapp. 2012, 33:2831-2842. 10.1002/hbm.21404.
49. Schofield M.A., Zhu Y. Fast phase unwrapping algorithm for interferometric applications. Opt. Lett. 2003, 28:1194-1196. 10.1364/OL.28.001194.
50. Schweser F., Deistung A., Lehr B.W., Reichenbach J.R. Differentiation between diamagnetic and paramagnetic cerebral lesions based on magnetic susceptibility mapping. Med. Phys. 2010, 37:5165-5178.
51. Schweser F., Deistung A., Lehr B.W., Reichenbach J.R. Quantitative imaging of intrinsic magnetic tissue properties using MRI signal phase: an approach to in vivo brain iron metabolism?. Neuroimage 2010, 54:2789-2807. 10.1016/j.neuroimage.2010.10.070.
52. Schweser F., Sommer K., Deistung A., Reichenbach J.R. Quantitative susceptibility mapping for investigating subtle susceptibility variations in the human brain. Neuroimage 2012, 62:2083-2100. 10.1016/j.neuroimage.2012.05.067.
53. Schweser F., Deistung A., Sommer K., Reichenbach J.R. Toward online reconstruction of quantitative susceptibility maps: superfast dipole inversion. Magn. Reson. Med. 2013, 69:1582-1594. 10.1002/mrm.24405.
54. Shmueli K., de Zwart J.A., van Gelderen P., Li T.-Q.Q., Dodd S.J., Duyn J.H. Magnetic susceptibility mapping of brain tissue in vivo using MRI phase data. Magn. Reson. Med. 2009, 62:1510-1522. 10.1002/mrm.22135.
55. Smith S., Jenkinson M., Woolrich M., Beckmann C., Behrens T., Johansen-Berg H., Bannister P., De Luca M., Drobnjak I., Flitney D., Niazy R., Saunders J., Vickers J., Zhang Y., De Stefano N., Brady J., Matthews P. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 2004, 23:208-219.
56. Stüber C., Morawski M., Schäfer A., Labadie C., Wähnert M., Leuze C., Streicher M., Barapatre N., Reimann K., Geyer S., Spemann D., Turner R. Myelin and iron concentration in the human brain: a quantitative study of MRI contrast. Neuroimage 2014, 10.1016/j.neuroimage.2014.02.026.
57. Sun H., Wilman A.H. Quantitative susceptibility mapping using single-shot echo-planar imaging. Magn. Reson. Med. 2014, 00. (n/a-n/a). 10.1002/mrm.25316.
58. Sun H., Walsh A.J., Lebel R.M., Blevins G., Catz I., Lu J.-Q., Johnson E.S., Emery D.J., Warren K.G., Wilman A.H. Validation of quantitative susceptibility mapping with Perls' iron staining for subcortical gray matter. Neuroimage 2014, 105:486-492. 10.1016/j.neuroimage.2014.11.010.
59. Valkonen T., Bredies K., Knoll F. Total generalized variation in diffusion tensor imaging. SIAM J. Imaging Sci. 2013, 6:487-525. 10.1137/120867172.
60. Wang Y., Liu T. Quantitative susceptibility mapping (QSM): decoding MRI data for a tissue magnetic biomarker. Magn. Reson. Med. 2014, 00. (n/a-n/a). 10.1002/mrm.25358.
61. Wen J., Cross A.H., Yablonskiy D.a On the role of physiological fluctuations in quantitative gradient echo MRI: implications for GEPCI, QSM, and SWI. Magn. Reson. Med. 2014, 00:1-9. 10.1002/mrm.25114.
62. Wharton S., Bowtell R. Effects of white matter microstructure on phase and susceptibility maps. Magn. Reson. Med. 2014, 00:1-12. 10.1002/mrm.25189.
63. Wiggermann V., Hernández Torres E., Vavasour I.M., Moore G.R.W., Laule C., MacKay A.L., Li D.K.B., Traboulsee A., Rauscher A. Magnetic resonance frequency shifts during acute MS lesion formation. Neurology 2013, 81:211-218. 10.1212/WNL.0b013e31829bfd63.
64. Wisnieff C., Liu T., Spincemaille P., Wang S., Zhou D., Wang Y. Magnetic susceptibility anisotropy: cylindrical symmetry from macroscopically ordered anisotropic molecules and accuracy of MRI measurements using few orientations. Neuroimage 2013, 70:363-376. 10.1016/j.neuroimage.2012.12.050.
65. Wisnieff C., Ramanan S., Olesik J., Gauthier S., Wang Y., Pitt D. Quantitative susceptibility mapping (QSM) of white matter multiple sclerosis lesions: interpreting positive susceptibility and the presence of iron. Magn. Reson. Med. 2014, 00:1-7. 10.1002/mrm.25420.
66. Xu Y., Haacke E.M. An iterative reconstruction technique for geometric distortion-corrected segmented echo-planar imaging. Magn. Reson. Imaging 2008, 26:1406-1414. 10.1016/j.mri.2008.04.008.
67. Yanez F., Fan A., Bilgic B., Milovic C., Adalsteinsson E., Irarrazaval P. Quantitative susceptibility map reconstruction via a total generalized variation regularization. 2013 International Workshop on Pattern Recognition in Neuroimaging. IEEE 2013, 203-206. 10.1109/PRNI.2013.59.
68. Zhou D., Liu T., Spincemaille P., Wang Y. Background field removal by solving the Laplacian boundary value problem. NMR Biomed. 2014, 10.1002/nbm.3064.
69. Zwanenburg J.J.M., Versluis M.J., Luijten P.R., Petridou N. Fast high resolution whole brain T2* weighted imaging using echo planar imaging at 7T. Neuroimage 2011, 56:1902-1907. 10.1016/j.neuroimage.2011.03.046.