Impact of tissue atrophy on high-pass filtered MRI signal phase-based assessment in large-scale group-comparison studies: A simulation study

Frontiers in Physics

Volumn 1, Issue OCT, 2013, Pages

  Schweser, Ferdinand ^a   Dwyer, Michael G ^b   Deistung, Andreas ^a   Reichenbach, Jürgen R ^a   Zivadinov, Robert ^b  

^a FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^b UNIVERSITY AT BUFFALO   (United States)

Author keywords

Artifacts; Atrophy; Group comparison; High pass filtering; Magnetic susceptibility; Phase imaging; Tissue iron

Indexed keywords

HIGH PASS FILTERS; IRON; MAGNETIC RESONANCE; MAGNETIC RESONANCE IMAGING; MAGNETIC SUSCEPTIBILITY; NEURODEGENERATIVE DISEASES;

ARTIFACT; ATROPHY; GROUP COMPARISON; HIGH-PASS; HIGH-PASS FILTERING; IRON CONCENTRATIONS; LARGE-SCALE GROUP; PHASE IMAGING; SIGNAL PHASE; TISSUE IRON;

TISSUE;

EID: 84928170367     PISSN: None     EISSN: 2296424X     Source Type: Journal    
DOI: 10.3389/fphy.2013.00014     Document Type: Article

References (54)

1. Bartzokis G, Aravagiri M, Oldendorf WH, Mintz J, Marder SR. Field dependent transverse relaxation rate increase may be a specific measure of tissue iron stores. Magn Reson Med. (1993) 29:459-64. doi: 10.1002/mrm.1910290406
2. Chen X, Zeng C, Luo T, Ouyang Y, Lv F, Rumzan R, et al. Iron deposition of the deep grey matter in patients with multiple sclerosis and neuromyelitis optica: a control quantitative study by 3D-enhanced susceptibility-weighted angiography (ESWAN). Eur J Radiol. (2012) 81:e633-9. doi: 10.1016/j.ejrad.2012.01.003
3. Cherubini A, Péran P, Caltagirone C, Sabatini U, Spalletta G. Aging of subcortical nuclei: microstructural, mineralization and atrophy modifications measured in vivo using MRI. Neuroimage (2009) 48:29-36. doi: 10.1016/j.neuroimage.2009.06.035
4. Deistung A, Schäfer A, Schweser F, Biedermann U, Turner R, Reichenbach JR. 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. doi: 10.1016/j.neuroimage.2012.09.055
5. Drayer BP, Burger P, Hurwitz B, Dawson D, Cain J. Reduced signal intensity on MR images of thalamus and putamen in multiple sclerosis: increased iron content? Am J Roentgenol. (1987) 149:357-63. doi: 10.2214/ajr.149.2.357
6. Drayer BP., Burger P, Hurwitz B, Dawson D, Cain J, Leong J, et al. Magnetic resonance imaging in multiple sclerosis: decreased signal in thalamus and putamen. Ann Neurol. (1987) 22:546-50. doi: 10.1002/ana.410220418
7. Faul F, Erdfelder E, Lang AG, Buchner A. G*Power 3, a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods (2009) 39:175-91. doi: 10.3758/BF03193146
8. Faul F, Erdfelder E, Buchner A, Lang AG. Statistical power analyses using G*Power 3.1, tests for correlation and regression analyses. Behav Res Methods (2007) 41:1149-60. doi: 10.3758/BRM.41.4.1149
9. Grabner G, Trattnig S, Barth M. Filtered deconvolution of a simulated and an in vivo phase model of the human brain. J Magn Reson Imaging (2010) 32:289-97. doi: 10.1002/jmri.22246
10. Griffiths PD, Dobson BR, Jones GR, Clarke DT. Iron in the basal ganglia in Parkinson's disease. An in vitro study using extended X-ray absorption fine structure and cryo-electron microscopy. Brain (1999) 122:667-73. doi: 10.1093/brain/122.4.667
11. Haacke EM, Ayaz M, Khan A, Manova ES, Krishnamurthy B, Gollapalli L, et al. Establishing a baseline phase behavior in magnetic resonance imaging to determine normal vs. abnormal iron content in the brain. J Magn Reson Imaging (2007) 26:256-64. doi: 10.1002/jmri.22987
12. Haacke EM, Cheng NYC, House MJ, Liu Q, Neelavalli J, Ogg RJ, et al. Imaging iron stores in the brain using magnetic resonance imaging. Magn Reson Imaging (2005) 23:1-5. doi: 10.1016/j.mri.2004.10.001
13. Haacke EM, Tang J, Neelavalli J. Susceptibility mapping as a means to visualize veins and quantify oxygen saturation. J Magn Reson Imaging (2010) 676:663-76. doi: 10.1002/jmri.22276
14. Hagemeier J, Dwyer MG, Bergsland N, Schweser F, Magnano CR, Heininen-Brown M, et al. Effect of age on mri phase behavior in the subcortical deep gray matter of healthy individuals. Am J Neuroradiol. (2013). doi: 10.3174/ajnr.A3569. [Epub ahead of print]
15. Hagemeier J, Geurts JJG, Zivadinov R. Brain iron accumulation in aging and neurodegenerative disorders. Expert Rev Neurother. (2012) 12:1467-80. doi: 10.1586/ern.12.128
16. Hagemeier J, Weinstock-Guttman B, Bergsland N, Heininen-Brown M, Carl E, Kennedy C, et al. Iron deposition on SWI-filtered phase in the subcortical deep gray matter of patients with clinically isolated syndrome may precede structure-specific atrophy. Am J Neuroradiol. (2012) 33:1596-601. doi: 10.3174/ajnr.A3030
17. Hagemeier J, Weinstock-Guttman B, Heininen-Brown M, Poloni GU, Bergsland N, Schirda C, et al. Gray matter SWI-filtered phase and atrophy are linked to disability in MS. Front Biosci. (2013) 5:525-32. doi: 10.2741/E634
18. Hagemeier J, Yeh EA, Brown MH, Bergsland N, Dwyer MG, Carl E, et al. Iron content of the pulvinar nucleus of the thalamus is increased in adolescent multiple sclerosis. Mult Scler. (2012). 19:567-576. doi: 10.1177/1352458512459289
19. Hikita T, Abe K, Sakoda S, Tanaka H, Murase K, Fujita N. Determination of transverse relaxation rate for estimating iron deposits in central nervous system. Neurosci Res. (2005) 51:67-71. doi: 10.1016/j.neures.2004.09.006
20. Holt RW, Diaz PJ, Duerk JL, Bellon EM. MR susceptometry: an external-phantom method for measuring bulk susceptibility from field-echo phase reconstruction maps. J Magn Reson Imaging (1994) 4:809-18. doi: 10.1002/jmri.1880040612
21. Hopp KM, Popescu BFG, McCrea RPE, Harder SL., Robinson CA, Haacke EM, et al. Brain iron detected by SWI high pass filtered phase calibrated with synchrotron X-ray fluorescence. J Magn Reson Imaging (2010) 31:1346-54. doi: 10.1002/jmri.22201
22. Koch KM, Papademetris X, Rothman DL, de Graaf RA. Rapid calculations of susceptibility-induced magnetostatic field perturbations for in vivo magnetic resonance. Phys Med Biol. (2006) 51:6381-402. doi: 10.1088/0031-9155/51/24/007
23. Langkammer C, Schweser F, Krebs N, Deistung A, Goessler W, Scheurer E, et al. Quantitative susceptibility mapping (QSM) as a means to measure brain iron? A post mortem validation study. Neuroimage (2012) 62:1593-99. doi: 10.1016/j.neuroimage.2012.05.049
24. LeVine SM. Iron deposits in multiple sclerosis and Alzheimer's disease brains. Brain Res. (1997) 760:298-303. doi: 10.1016/S0006-8993(97)00470-8
25. Li W, Wu B, Liu C. Quantitative susceptibility mapping of human brain reflects spatial variation in tissue composition. Neuroimage (2011) 55:1645-56. doi: 10.1016/j.neuroimage.2010.11.088
26. Liem MK, Lesnik Oberstein SA, Versluis MJ, Maat-Schieman MLC, Haan J, Webb AG, et al. 7T MRI reveals diffuse iron deposition in putamen and caudate nucleus in CADASI L. J Neurol Neurosurg Psychiatry (2012) 83:1180-5. doi: 10.1136/jnnp-2012-302545
27. Liu T, Khalidov I, de Rochefort L, Spincemaille P, Liu J, Tsiouris AJ, et al. A novel background field removal method for MRI using projection onto dipole fields (PDF). NMR Biomed. (2011) 24:1129-36. doi: 10.1002/nbm.1670
28. 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. doi: 10.1002/mrm.21828
29. Liu T, Wisnieff C, Lou M, Chen W, Spincemaille P, Wang Y. Nonlinear formulation of the magnetic field to source relationship for robust quantitative susceptibility mapping. Magn Reson Med. (2013) 69:467-76. doi: 10.1002/mrm.24272
30. Marques JP, Bowtell RW. Application of a Fourier-based method for rapid calculation of field inhomogeneity due to spatial variation of magnetic susceptibility. Concepts Magn Reson B Magn Reson Eng. (2005) 25B:65-78. doi: 10.1002/cmr.b.20034
31. Minagar A, Barnett MH, Benedict RHB, Pelletier D, Pirko I, Sahraian MA, et al. The thalamus and multiple sclerosis: modern views on pathologic, imaging, and clinical aspects. Neurology (2013) 80:210-9. doi: 10.1212/WNL.0b013e31827b910b
32. Noll DC, Nishimura DG, Makovski A. Homodyne detection in magnetic resonance imaging. IEEE Trans Med Imaging (1991) 10:154-63. doi: 10.1109/42.79473
33. Péran P, Hagberg GE, Luccichenti G, Cherubini A, Brainovich V, Celsis P, et al. Voxel-based analysis of R2* maps in the healthy human brain. J Magn Reson Imaging (2007) 26:1413-20. doi: 10.1002/jmri.21204
34. Rauscher A, Sedlacik J, Barth M, Mentzel HJ, Reichenbach, JR. Magnetic susceptibility-weighted MR phase imaging of the human brain. Am J Neuroradiol. (2005) 26:736-42
35. Reichenbach JR, Barth M, Haacke EM, Klarhöfer M, Kaiser WA, Moser E. High-resolution MR venography at 3.0 Tesla. J Comp Assist Tomogr. (2000) 24:949-57. doi: 10.1097/00004728-200011000-00023
36. Reichenbach JR, Venkatesan R, Schillinger D, Kido DK, Haacke EM. Small vessels in the human brain: MR-venography with deoxyhemoglobin as an intrinsic contrast agent. Radiology (1997) 204:272-77
37. Rumzan R, Wang JJ, Zeng C, Chen X, Li Y, Luo T, et al. Iron deposition in the precentral grey matter in patients with multiple sclerosis: a quantitative study using susceptibility-weighted imaging. Eur J Radiol. (2013) 82:e95-9. doi: 10.1016/j.ejrad.2012.09.006
38. Salomir R, de Senneville BD, Moonen CTW. A fast calculation method for magnetic field inhomogeneity due to an arbitrary distribution of bulk susceptibility. Concepts Magn Reson B Magn Reson Eng. (2003) 19B:26-34. doi: 10.1002/cmr.b.10083
39. Schäfer A, Wharton SJ, Gowland P, Bowtell RW. Using magnetic field simulation to study susceptibility-related phase contrast in gradient echo MRI. Neuroimage (2009) 48:126-37. doi: 10.1016/j.neuroimage.2009.05.093
40. Schoonheim MM, Popescu V, Rueda Lopes FC, Wiebenga OT, Vrenken H, Douw L, et al. Subcortical atrophy and cognition: sex effects in multiple sclerosis. Neurology (2012) 79:1754-61. doi: 10.1212/WNL.0b013e3182703f46
41. Schweser F, Deistung A, Lehr BW, Reichenbach JR. Differentiation between diamagnetic and paramagnetic cerebral lesions based on magnetic susceptibility mapping. Med Phys. (2010) 37:5165-78. doi: 10.1118/1.3481505
42. Schweser F, Deistung A, Lehr BW, Reichenbach JR. Quantitative imaging of intrinsic magnetic tissue properties using MRI signal phase: an approach to in vivo brain iron metabolism? Neuroimage (2011) 54:2789-807. doi: 10.1016/j.neuroimage.2010.10.070
43. Schweser F, Deistung A, Sommer K, Reichenbach JR. Toward online reconstruction of quantitative susceptibility maps: superfast dipole inversion. Magn Reson Med. (2013) 69:1581-93. doi: 10.1002/mrm.24405
44. Schweser F, Sommer K, Deistung A, Reichenbach JR. Quantitative susceptibility mapping for investigating subtle susceptibility variations in the human brain. Neuroimage (2012) 62:2083-2100. doi: 10.1016/j.neuroimage.2012.05.067
45. Shmueli K, de Zwart JA, van Gelderen P, Li TQ, Dodd SJ, Duyn JH. Magnetic susceptibility mapping of brain tissue in vivo using MRI phase data. Magn Reson Med. (2009) 62:1510-22. doi: 10.1002/mrm.22135
46. Walsh AJ, Wilman AH. Susceptibility phase imaging with comparison to R2 mapping of iron-rich deep grey matter. Neuroimage (2011) 57:452-61. doi: 10.1016/j.neuroimage.2011.04.017
47. Wang D, Li WB, Wei XE, Li, YH, Dai YM. An investigation of age-related iron deposition using susceptibility weighted imaging. PLoS ONE (2012) 7:e50706. doi: 10.1371/journal.pone.0050706
48. Wang Y, Butros SR, Shuai X, Dai Y, Chen C, Liu M, et al. Different iron-deposition patterns of multiple system atrophy with predominant parkinsonism and idiopathetic Parkinson diseases demonstrated by phase-corrected susceptibility-weighted imaging. Am J Neuroradiol. (2012) 33:266-73. doi: 10.3174/ajnr.A2765
49. Wharton SJ, Schäfer A, Bowtell RW. Susceptibility mapping in the human brain using threshold-based k-space division. Magn Reson Med. (2010) 63:1292-304. doi: 10.1002/mrm.22334
50. Wu B, Li W, Guidon A, Liu C. Whole brain susceptibility mapping using compressed sensing. Magn Reson Med. (2011) 24:1129-36. doi: 10.1002/mrm.23000
51. Xu X, Wang Q, Zhang M. Age, gender, and hemispheric differences in iron deposition in the human brain: an in vivo MRI study. Neuroimage (2008) 40:35-42. doi: 10.1016/j.neuroimage.2007.11.017
52. Yan SQ, Sun JZ, Yan YQ, Wang H, Lou M. Evaluation of brain iron content based on magnetic resonance imaging (MRI): comparison among phase value, R2* and magnitude signal intensity. PLoS ONE (2012) 7:e31748. doi: 10.1371/journal.pone.0031748
53. Yao B, Li TQ, Gelderen PV, Shmueli K, de Zwart JA, Duyn JH. Susceptibility contrast in high field MRI of human brain as a function of tissue iron content. Neuroimage (2009) 44:1259-66. doi: 10.1016/j.neuroimage.2008.10.029
54. Zivadinov R, Heininen-Brown M, Schirda CV, Poloni GU, Bergsland N, Magnano CR, et al. Abnormal subcortical deep-gray matter susceptibility-weighted imaging filtered phase measurements in patients with multiple sclerosis: a case-control study. Neuroimage (2012) 59:331-9. doi: 10.1016/j.neuroimage.2011.07.045