Age-related microstructural differences quantified using myelin water imaging and advanced diffusion MRI

Neurobiology of Aging

Volumn 36, Issue 6, 2015, Pages 2107-2121

  Billiet, Thibo ^a,b,c   Vandenbulcke, Mathieu ^c,d   Mädler, Burkhard ^e,f   Peeters, Ronald ^b,c   Dhollander, Thijs ^b,g   Zhang, Hui ^h   Deprez, Sabine ^a,b,c   Van den Bergh, Bea R H ^d,i   Sunaert, Stefan ^a,b,c   Emsell, Louise ^a,b,c,d  

^a DEPARTMENT OF IMAGING AND PATHOLOGY   (Belgium)

^b UNIVERSITY HOSPITALS LEUVEN   (Belgium)

^c Leuven Research Institute for Neuroscience and Disease O and N4   (Belgium)

^d UNIVERSITY OF LEUVEN   (Belgium)

^e PHILIPS HEALTHCARE   (United States)

^f UNIVERSITY OF BONN   (Germany)

^g FLOREY INSTITUTE OF NEUROSCIENCE AND MENTAL HEALTH   (Australia)

^h UNIVERSITY COLLEGE LONDON   (United Kingdom)

ⁱ TILBURG UNIVERSITY   (Netherlands)

Author keywords

Aging; Diffusion MRI; Healthy; Kurtosis; Myelin water imaging; Relaxometry

Indexed keywords

ADOLESCENT; ADULT; AGE; AGED; AGING; ARTICLE; BRAIN ATROPHY; CONTROLLED STUDY; CORRELATIONAL STUDY; CROSS-SECTIONAL STUDY; DIFFUSION KURTOSIS IMAGING; DIFFUSION TENSOR IMAGING; DIFFUSION WEIGHTED IMAGING; FEMALE; FRACTIONAL ANISOTROPY; HUMAN; HUMAN EXPERIMENT; IMAGE PROCESSING; IMAGING AND DISPLAY; MALE; MULTIEXPONENTIAL T2 RELAXATION; MYELIN WATER IMAGING; NEURITE ORIENTATION DISPERSION AND DENSITY IMAGING; NEUROIMAGING; NORMAL HUMAN; PRIORITY JOURNAL; PROSPECTIVE STUDY; QUANTITATIVE ANALYSIS; WHITE MATTER; ANISOTROPY; BRAIN; MIDDLE AGED; NERVE FIBER; NEURITE; PATHOLOGY; PROCEDURES; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; AGING; ANISOTROPY; AXONS; BRAIN; DIFFUSION TENSOR IMAGING; FEMALE; HUMANS; MALE; MIDDLE AGED; NEURITES; WHITE MATTER; YOUNG ADULT;

EID: 84929296176     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2015.02.029     Document Type: Article

References (64)

1. Ashburner J. Afast diffeomorphic image registration algorithm. Neuroimage 2007, 38:95-113.
2. Avants B.B., Epstein C.L., Grossman M., Gee J.C. Symmetric diffeomorphic image registration with cross-correlation: evaluating automated labeling of elderly and neurodegenerative brain. Med. Image Anal. 2008, 12:26-41.
3. Bartzokis G., Lu P.H., Heydari P., Couvrette A., Lee G.J., Kalashyan G., Freeman F., Grinstead J.W., Villablanca P., Finn J.P., Mintz J., Alger J.R., Altshuler L.L. Multimodal magnetic resonance imaging assessment of white matter aging trajectories over the lifespan of healthy individuals. Biol. Psychiatry 2012, 72:1026-1034.
4. Basser P.J., Mattiello J., LeBihan D. Estimation of the effective self-diffusion tensor from the NMR spin echo. J.Magn. Reson. B 1994, 103:247-254.
5. Beaulieu C. The basis of anisotropic water diffusion in the nervous system-a technical review. NMR Biomed. 2002, 15:435-455.
6. Beaulieu C., Allen P.S. Determinants of anisotropic water diffusion in nerves. Magn. Reson. Med. 1994, 31:394-400.
7. Billiet T., Madler B., D'Arco F., Peeters R., Deprez S., Plasschaert E., Leemans A., Zhang H., den Bergh B.V., Vandenbulcke M., Legius E., Sunaert S., Emsell L. Characterizing the microstructural basis of "unidentified bright objects" in neurofibromatosis type 1: a combined invivo multicomponent T2 relaxation and multi-shell diffusion MRI analysis. Neuroimage Clin. 2014, 4:649-658.
8. Brickman A.M., Meier I.B., Korgaonkar M.S., Provenzano F.A., Grieve S.M., Siedlecki K.L., Wasserman B.T., Williams L.M., Zimmerman M.E. Testing the white matter retrogenesis hypothesis of cognitive aging. Neurobiol. Aging 2012, 33:1699-1715.
9. Callaghan M.F., Freund P., Draganski B., Anderson E., Cappelletti M., Chowdhury R., Diedrichsen J., Fitzgerald T.H., Smittenaar P., Helms G., Lutti A., Weiskopf N. Widespread age-related differences in the human brain microstructure revealed by quantitative magnetic resonance imaging. Neurobiol. Aging 2014, 35:1862-1872.
10. Coutu J.P., Chen J.J., Rosas H.D., Salat D.H. Non-Gaussian water diffusion in aging white matter. Neurobiol. Aging 2014, 35:1412-1421.
11. Davis S.W., Dennis N.A., Buchler N.G., White L.E., Madden D.J., Cabeza R. Assessing the effects of age on long white matter tracts using diffusion tensor tractography. Neuroimage 2009, 46:530-541.
12. De Santis S., Drakesmith M., Bells S., Assaf Y., Jones D.K. Why diffusion tensor MRI does well only some of the time: variance and covariance of white matter tissue microstructure attributes in the living human brain. Neuroimage 2014, 89:35-44.
13. Deoni S.C., Dean D.C., O'Muircheartaigh J., Dirks H., Jerskey B.A. Investigating white matter development in infancy and early childhood using myelin water faction and relaxation time mapping. Neuroimage 2012, 63:1038-1053.
14. Draganski B., Ashburner J., Hutton C., Kherif F., Frackowiak R.S., Helms G., Weiskopf N. Regional specificity of MRI contrast parameter changes in normal ageing revealed by voxel-based quantification (VBQ). Neuroimage 2011, 55:1423-1434.
15. Falangola M.F., Jensen J.H., Babb J.S., Hu C., Castellanos F.X., Di Martino A., Ferris S.H., Helpern J.A. Age-related non-Gaussian diffusion patterns in the prefrontal brain. J.Magn. Reson. Imaging 2008, 28:1345-1350.
16. Fjell A.M., Westlye L.T., Amlien I., Espeseth T., Reinvang I., Raz N., Agartz I., Salat D.H., Greve D.N., Fischl B., Dale A.M., Walhovd K.B. High consistency of regional cortical thinning in aging across multiple samples. Cereb. Cortex 2009, 19:2001-2012.
17. Flynn S.W., Lang D.J., Mackay A.L., Goghari V., Vavasour I.M., Whittall K.P., Smith G.N., Arango V., Mann J.J., Dwork A.J., Falkai P., Honer W.G. Abnormalities of myelination in schizophrenia detected invivo with MRI, and post-mortem with analysis of oligodendrocyte proteins. Mol. Psychiatry 2003, 8:811-820.
18. Frazier J.A., Chiu S., Breeze J.L., Makris N., Lange N., Kennedy D.N., Herbert M.R., Bent E.K., Koneru V.K., Dieterich M.E., Hodge S.M., Rauch S.L., Grant P.E., Cohen B.M., Seidman L.J., Caviness V.S., Biederman J. Structural brain magnetic resonance imaging of limbic and thalamic volumes in pediatric bipolar disorder. Am. J. Psychiatry 2005, 162:1256-1265.
19. Gong N.J., Wong C.S., Chan C.C., Leung L.M., Chu Y.C. Aging in deep gray matter and white matter revealed by diffusional kurtosis imaging. Neurobiol. Aging 2014, 35:2203-2216.
20. Haroutunian V., Katsel P., Roussos P., Davis K.L., Altshuler L.L., Bartzokis G. Myelination, oligodendrocytes, and serious mental illness. Glia 2014, 62:1856-1877.
21. Hennig J. Multiecho imaging sequences with low refocusing flip angles. J.Magn. Reson. 1988, 78:397-407.
22. Hui E.S., Cheung M.M., Qi L., Wu E.X. Towards better MR characterization of neural tissues using directional diffusion kurtosis analysis. Neuroimage 2008, 42:122-134.
23. Inano S., Takao H., Hayashi N., Abe O., Ohtomo K. Effects of age and gender on white matter integrity. AJNR Am. J. Neuroradiol. 2011, 32:2103-2109.
24. Irfanoglu M.O., Walker L., Sarlls J., Marenco S., Pierpaoli C. Effects of image distortions originating from susceptibility variations and concomitant fields on diffusion MRI tractography results. Neuroimage 2012, 61:275-288.
25. Jelescu I.O., Veraart J., Adisetiyo V., Milla S.S., Novikov D.S., Fieremans E. One diffusion acquisition and different white matter models: how does microstructure change in human early development based on WMTI and NODDI?. Neuroimage 2015, 107:242-256.
26. Jensen J.H., Helpern J.A. MRI quantification of non-Gaussian water diffusion by kurtosis analysis. NMR Biomed. 2010, 23:698-710.
27. Jensen J.H., Helpern J.A., Ramani A., Lu H., Kaczynski K. Diffusional kurtosis imaging: the quantification of non-Gaussian water diffusion by means of magnetic resonance imaging. Magn. Reson. Med. 2005, 53:1432-1440.
28. Jones D.K., Cercignani M. Twenty-five pitfalls in the analysis of diffusion MRI data. NMR Biomed. 2010, 23:803-820.
29. Kempton M.J., Underwood T.S., Brunton S., Stylios F., Schmechtig A., Ettinger U., Smith M.S., Lovestone S., Crum W.R., Frangou S., Williams S.C., Simmons A. Acomprehensive testing protocol for MRI neuroanatomical segmentation techniques: evaluation of a novel lateral ventricle segmentation method. Neuroimage 2011, 58:1051-1059.
30. Kumar R., Chavez A.S., Macey P.M., Woo M.A., Harper R.M. Brain axial and radial diffusivity changes with age and gender in healthy adults. Brain Res. 2013, 1512:22-36.
31. Kunz N., Zhang H., Vasung L., O'Brien K.R., Assaf Y., Lazeyras F., Alexander D.C., Huppi P.S. Assessing white matter microstructure of the newborn with multi-shell diffusion MRI and biophysical compartment models. Neuroimage 2014, 96:288-299.
32. Lally P., Zhang H., Pauliah S., Price D., Bainbridge A., Balraj G., Cady E., Shankaran S., Thayyil S. 8.9 microstructural changes in neonatal encephalopathy revealed with the neurite orientation dispersion and density imaging (NODDI) model. Arch. Dis. Child Fetal Neonatal. Ed. 2014, 99(Suppl 1):A14.
33. Latt J., Nilsson M., Wirestam R., Stahlberg F., Karlsson N., Johansson M., Sundgren P.C., van Westen D. Regional values of diffusional kurtosis estimates in the healthy brain. J.Magn. Reson. Imaging 2013, 37:610-618.
34. Laule C., Vavasour I.M., Kolind S.H., Traboulsee A.L., Moore G.R., Li D.K., Mackay A.L. Long T2 water in multiple sclerosis: what else can we learn from multi-echo T2 relaxation?. J.Neurol. 2007, 254:1579-1587.
35. Laule C., Vavasour I.M., Madler B., Kolind S.H., Sirrs S.M., Brief E.E., Traboulsee A.L., Moore G.R., Li D.K., MacKay A.L. MR evidence of long T2 water in pathological white matter. J.Magn. Reson. Imaging 2007, 26:1117-1121.
36. Lebel C., Gee M., Camicioli R., Wieler M., Martin W., Beaulieu C. Diffusion tensor imaging of white matter tract evolution over the lifespan. Neuroimage 2012, 60:340-352.
37. Leemans, A. 2009. ExploreDTI: A Graphical Toolbox for Processing, Analyzing, and Visualizing Diffusion MR Data. 17th Annual Meeting of Intl Soc Mag Reson Med, Hawaii, USA, pp.3537.
38. Leemans A., Jones D.K. The B-matrix must be rotated when correcting for subject motion in DTI data. Magnet Reson. Med. 2009, 61:1336-1349.
39. Madden D.J., Whiting W.L., Huettel S.A., White L.E., MacFall J.R., Provenzale J.M. Diffusion tensor imaging of adult age differences in cerebral white matter: relation to response time. Neuroimage 2004, 21:1174-1181.
40. Madler B., Drabycz S.A., Kolind S.H., Whittall K.P., MacKay A.L. Is diffusion anisotropy an accurate monitor of myelination? Correlation of multicomponent T2 relaxation and diffusion tensor anisotropy in human brain. Magn. Reson. Imaging 2008, 26:874-888.
41. Maedler B., MacKay A. Towards Whole Brain Myelin Imaging. International Society for Magnetic Resonance in Medicine 2007, Berlin, Germany, pp. 1723.
42. Melbourne A., Eaton-Rosen Z., Bainbridge A., Kendall G.S., Cardoso M.J., Robertson N.J., Marlow N., Ourselin S. Measurement of myelin in the preterm brain: multi-compartment diffusion imaging and multi-component T2 relaxometry. Med. Image Comput. Comput Assist. Interv. 2013, 16(Pt 2):336-344.
43. Mori S., Wakana S., Nagae-Poetscher L.M., van Zijl P.C.M. MRI Atlas of Human White Matter 2005, Amsterdam, The Netherlands, Elsevier.
44. Pannese E. Morphological changes in nerve cells during normal aging. Brain Struct. Funct. 2011, 216:85-89.
45. Pfefferbaum A., Sullivan E.V., Hedehus M., Lim K.O., Adalsteinsson E., Moseley M. Age-related decline in brain white matter anisotropy measured with spatially corrected echo-planar diffusion tensor imaging. Magn. Reson. Med. 2000, 44:259-268.
46. Poot D.H., den Dekker A.J., Achten E., Verhoye M., Sijbers J. Optimal experimental design for diffusion kurtosis imaging. IEEE Trans. Med. Imaging 2010, 29:819-829.
47. Prasloski T., Madler B., Xiang Q.S., Mackay A., Jones C. Applications of stimulated echo correction to multicomponent T(2) analysis. Magn. Reson. Med. 2012, 67:1803-1814.
48. Prasloski T., Rauscher A., MacKay A.L., Hodgson M., Vavasour I.M., Laule C., Madler B. Rapid whole cerebrum myelin water imaging using a 3D GRASE sequence. Neuroimage 2012, 63:533-539.
49. Raz N., Gunning F.M., Head D., Dupuis J.H., McQuain J., Briggs S.D., Loken W.J., Thornton A.E., Acker J.D. Selective aging of the human cerebral cortex observed invivo: differential vulnerability of the prefrontal gray matter. Cereb. Cortex 1997, 7:268-282.
50. Salat D.H., Lee S.Y., van der Kouwe A.J., Greve D.N., Fischl B., Rosas H.D. Age-associated alterations in cortical gray and white matter signal intensity and gray to white matter contrast. Neuroimage 2009, 48:21-28.
51. Salat D.H., Tuch D.S., Greve D.N., van der Kouwe A.J., Hevelone N.D., Zaleta A.K., Rosen B.R., Fischl B., Corkin S., Rosas H.D., Dale A.M. Age-related alterations in white matter microstructure measured by diffusion tensor imaging. Neurobiol. Aging 2005, 26:1215-1227.
52. Song S.K., Yoshino J., Le T.Q., Lin S.J., Sun S.W., Cross A.H., Armstrong R.C. Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neuroimage 2005, 26:132-140.
53. Stanisz G.J., Webb S., Munro C.A., Pun T., Midha R. MR properties of excised neural tissue following experimentally induced inflammation. Magn. Reson. Med. 2004, 51:473-479.
54. Sullivan E.V., Pfefferbaum A. Diffusion tensor imaging and aging. Neurosci. Biobehav R. 2006, 30:749-761.
55. Tournier J.D., Mori S., Leemans A. Diffusion tensor imaging and beyond. Magn. Reson. Med. 2011, 65:1532-1556.
56. Van Hecke W., Leemans A., D'Agostino E., De Backer S., Vandervliet E., Parizel P.M., Sijbers J. Nonrigid coregistration of diffusion tensor images using a viscous fluid model and mutual information. IEEE Trans. Med. Imaging 2007, 26:1598-1612.
57. Van Hecke W., Leemans A., Sage C.A., Emsell L., Veraart J., Sijbers J., Sunaert S., Parizel P.M. The effect of template selection on diffusion tensor voxel-based analysis results. Neuroimage 2011, 55:566-573.
58. Vavasour I.M., Laule C., Li D.K., Traboulsee A.L., MacKay A.L. Is the magnetization transfer ratio a marker for myelin in multiple sclerosis?. J.Magn. Reson. Imaging 2011, 33:713-718.
59. Vos S.B., Jones D.K., Viergever M.A., Leemans A. Partial volume effect as a hidden covariate in DTI analyses. Neuroimage 2011, 55:1566-1576.
60. Wheeler-Kingshott C.A., Cercignani M. About "axial" and "radial" diffusivities. Magn. Reson. Med. 2009, 61:1255-1260.
61. Whitaker K.J., Kolind S.H., MacKay A.L., Clark C.M. Quantifying development: investigating highly myelinated voxels in preadolescent corpus callosum. Neuroimage 2008, 43:731-735.
62. Whittall K.P., Mackay A.L. Quantitative interpretation of NMR relaxation data. J.Magn. Reson. 1989, 84:134-152.
63. Winston G.P., Micallef C., Symms M.R., Alexander D.C., Duncan J.S., Zhang H. Advanced diffusion imaging sequences could aid assessing patients with focal cortical dysplasia and epilepsy. Epilepsy Res. 2014, 108:336-339.
64. Zhang H., Schneider T., Wheeler-Kingshott C.A., Alexander D.C. NODDI: practical invivo neurite orientation dispersion and density imaging of the human brain. Neuroimage 2012, 61:1000-1016.