Abstract
Purpose
It is unclear how white matter hyperintensities disrupt surrounding white matter tracts. The aim of this tractography study was to determine the spatial relationship between diffusion characteristics along white matter tracts and the distance from white matter hyperintensities.
Methods
Diffusion tensor 3-T MRI scans were acquired in 29 participants with white matter hyperintensities. In each subject, tractography by the fiber assignment by continuous tracking method was used to segment corticospinal tracts. Mean diffusivity, radial diffusivity, axial diffusivity, and fractional anisotropy were measured along corticospinal tracts in relation to white matter hyperintensities. Diffusion characteristics along tracts were correlated with distance from white matter hyperintensities and were also compared between tracts traversing and not traversing white matter hyperintensities.
Results
In tracts not traversing through white matter hyperintensities, increasing distance from white matter hyperintensities was associated with decreased mean diffusivity (p = 0.002) and increased fractional anisotropy (p = 0.006). In tracts traversing white matter hyperintensities, compared to tracts not traversing white matter hyperintensites, the mean diffusivity was higher at 6–8 voxels, axial diffusivity higher at 4–8 voxels, and radial diffusivity higher at 7 voxels away from white matter hyperintensities (all p < 0.006).
Conclusion
White matter hyperintensities are associated with two patterns of altered diffusion characteristics in the surrounding white matter tract network. Diffusion characteristics along white matter tracts improve further away from white matter hyperintensities suggestive of a local penumbra pattern. Also, altered diffusion extends further along tracts traversing white matter hyperintensities suggestive of a Wallerian-type degenerative pattern.
Similar content being viewed by others
Abbreviations
- WMH:
-
White matter hyperintensities
- NAWM:
-
Normal-appearing white matter
- CST:
-
Corticospinal tract
- WMH tracts:
-
Tracts passing through white matter hyperintensities
- Lesion-free tracts:
-
Tracts not passing through white matter hyperintensities
References
Debette S, Markus HS (2010) The clinical importance of white matter hyperintensities on brain magnetic resonance imaging: systematic review and meta-analysis. BMJ 26:c3666
Gouw AA, Seewann A, van der Flier WM, Barkhof F, Rozemuller AM, Scheltens P, Geurts JJ (2011) Heterogeneity of small vessel disease: a systematic review of MRI and histopathology correlations. J Neurol Neurosurg Psychiatry 82:126–135
Maniega SM, Valdés Hernández MC, Clayden JD, Royle NA, Murray C, Morris Z, Aribisala BS, Gow AJ, Starr JM, Bastin ME, Deary IJ, Wardlaw JM (2015) White matter hyperintensities and normal-appearing white matter integrity in the aging brain. Neurobiol Aging 36:909–918
Schmidt R, Ropele S, Ferro J, Madureira S, Verdelho A, Petrovic K, Gouw A, van der Flier WM, Enzinger C, Pantoni L, Inzitari D, Erkinjuntti T, Scheltens P, Wahlund LO, Waldemar G, Rostrup E, Wallin A, Barkhof F, Fazekas F, LADIS study group (2010) Diffusion-weighted imaging and cognition in the leukoariosis and disability in the elderly study. Stroke 41:e402–e408
Vernooij MW, Ikram MA, Vrooman HA, Wielopolski PA, Krestin GP, Hofman A, Niessen WJ, Van der Lugt A, Breteler MM (2009) White matter microstructural integrity and cognitive function in a general elderly population. Arch Gen Psychiatry 66:545–553
Maillard P, Fletcher E, Harvey D, Carmichael O, Reed B, Mungas D, DeCarli C (2011) White matter hyperintensity penumbra. Stroke 42:1917–1922
Promjunyakul N, Lahna D, Kaye JA, Dodge HH, Erten-Lyons D, Rooney WD, Silbert LC (2015) Characterizing the white matter hyperintensity penumbra with cerebral blood flow measures. Neuroimage Clin 8:224–229
Maillard P, Fletcher E, Lockhart SN, Roach AE, Reed B, Mungas D, DeCarli C (2014) White matter hyperintensities and their penumbra lie along a continuum of injury in the aging brain. Stroke 45:1721–1726
Maillard P, Carmichael O, Harvey D, Fletcher E, Reed B, Mungas D, DeCarli C (2013) FLAIR and diffusion MRI signals are independent predictors of white matter hyperintensities. AJNR Am J Neuroradiol 34:54–61
Promjunyakul NO, Lahna DL, Kaye JA, Dodge HH, Erten-Lyons D, Rooney WD, Silbert LC (2016) Comparison of cerebral blood flow and structural penumbras in relation to white matter hyperintensities: a multi-modal magnetic resonance imaging study. J Cereb Blood Flow Metab 36:1528–1536
Reginold W, Itorralba J, Luedke AC, Fernandez-Ruiz J, Reginold J, Islam O, Garcia A (2016) Tractography at 3T MRI of corpus callosum tracts crossing white matter hyperintensities. AJNR Am J Neuroradiol 37:1617–1622
Ryberg C, Rostrup E, Sjöstrand K, Paulson OB, Barkhof F, Scheltens P, van Straaten EC, Fazekas F, Schmidt R, Erkinjuntti T, Wahlund LO, Basile AM, Pantoni L, Inzitari D, Waldemar G, LADIS study group (2008) White matter changes contribute to corpus callosum atrophy in the elderly: the LADIS study. AJNR Am J Neuroradiol 29:1498–1504
Jones DK, Travis AR, Eden G, Pierpaoli C, Basser PJ (2005) PASTA: pointwise assessment of streamline tractography attributes. Magn Reson Med 53:1462–1467
Goodlett CB, Fletcher PT, Gilmore JH, Gerig G (2009) Group analysis of DTI fiber tract statistics with application to neurodevelopment. Neuroimage 45:S133–S142
O’Donnell LJ, Westin CF, Golby AJ (2009) Tract-based morphometry for white matter group analysis. Neuroimage 45:832–844
Zhu H, Kong L, Li R, Styner M, Gerig G, Lin W, Gilmore JH (2011) FADTTS: functional analysis of diffusion tensor tract statistics. Neuroimage 56:1412–1425
Yeatman JD, Dougherty RF, Myall NJ, Wandell BA, Feldman HM (2012) Tract profiles of white matter properties: automating fiber-tract quantification. PLoS One 7:e49790
Chen Z, Zhang H, Yushkevich PA, Liu M, Beaulieu C (2016) Maturation along white matter tracts in human brain using a diffusion tensor surface model tract-specific analysis. Front Neuroanat 10:9
Johnson RT, Yeatman JD, Wandell BA, Buonocore MH, Amaral DG, Nordahl CW (2014) Diffusion properties of major white matter tracts in young, typically developing children. Neuroimage 88:143–154
Wardlaw JM, Smith EE, Biessels GJ, Cordonnier C, Fazekas F, Frayne R, Lindley RI, O’Brien JT, Barkhof F, Benavente OR, Black SE, Brayne C, Breteler M, Chabriat H, Decarli C, de Leeuw FE, Doubal F, Duering M, Fox NC, Greenberg S, Hachinski V, Kilimann I, Mok V, Rv O, Pantoni L, Speck O, Stephan BC, Teipel S, Viswanathan A, Werring D, Chen C, Smith C, van Buchem M, Norrving B, Gorelick PB, Dichgans M (2013) STandards for ReportIng Vascular changes on nEuroimaging. Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration. Lancet Neurol 12:822–838
Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TE, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, Niazy RK, Saunders J, Vickers J, Zhang Y, De Stefano N, Brady JM, Matthews PM (2010) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23:S208–S219
Wiegell MR, Larsson HB, Wedeen VJ (2000) Fiber crossing in human brain depicted with diffusion tensor MR imaging. Radiology 217:897–903
Simões R, Mönninghoff C, Dlugaj M, Weimar C, Wanke I, van Cappellen van Walsum AM, Slump C (2013) Automatic segmentation of cerebral white matter hyperintensities using only 3D FLAIR images. Magn Reson Imaging 31:1182–1189
Cox RW (1996) AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 29:162–173
Reginold W, Luedke AC, Tam A, Itorralba J, Fernandez-Ruiz J, Reginold J, Islam O, Garcia A (2015) Cognitive function and 3-Tesla magnetic resonance imaging tractography of white matter hyperintensities in elderly persons. Dement Geriatr Cogn Dis Extra 21:387–394
Song SK, Sun SW, Ju WK, Lin SJ, Cross AH, Neufeld AH (2003) Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. Neuroimage 20:1714–1722
Schwartz ED, Cooper ET, Fan Y, Jawad AF, Chin CL, Nissanov J, Hackney DB (2005) MRI diffusion coefficients in spinal cord correlate with axon morphometry. Neuroreport 16:73–76
Song SK, Sun SW, Ramsbottom MJ, Chang C, Russell J, Cross AH (2002) Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage 17:1429–1436
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Funding
No funding was received for this study.
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
Informed consent
Informed consent was obtained from all individual participants included in the study.
Rights and permissions
About this article
Cite this article
Reginold, W., Sam, K., Poublanc, J. et al. Impact of white matter hyperintensities on surrounding white matter tracts. Neuroradiology 60, 933–944 (2018). https://doi.org/10.1007/s00234-018-2053-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00234-018-2053-x