Abstract
In multiple sclerosis studies, lesion volume (or lesion load) derived from conventional T2 imaging correlates modestly with clinical assessment. Determining which specific white matter pathways are impacted by lesions may provide additional insights regarding task-specific clinical impairment. Using diffusion MRI, we introduce a set of tract-based metrics that go beyond traditional lesion load approaches and show how they relate to task performance (i.e., working memory, information processing and verbal fluency) in a cohort of 40 patients with multiple sclerosis.
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Thompson, A.J., Banwell, B.L., Barkhof, F., Carroll, W.M., Coetzee, T., Comi, G., Correale, J., Fazekas, F., Filippi, M., Freedman, M.S., et al.: Diagnosis of multiple sclerosis: 2017 revisions of the McDonald criteria. Lancet Neurol. 17(2), 162–173 (2018)
Vellinga, M., Geurts, J., Rostrup, E., Uitdehaag, B., Polman, C., Barkhof, F., Vrenken, H.: Clinical correlations of brain lesion distribution in multiple sclerosis. J. Mag. Reson. Imaging Official J. Int. Soc. Mag. Reson. Med. 29(4), 768–773 (2009)
Barkhof, F.: The clinico-radiological paradox in multiple sclerosis revisited. Curr. Opin. Neurol. 15(3), 239–245 (2002)
Mollison, D., Sellar, R., Bastin, M., Mollison, D., Chandran, S., Wardlaw, J., Connick, P.: The clinico-radiological paradox of cognitive function and MRI burden of white matter lesions in people with multiple sclerosis: A systematic review and meta-analysis. PloS One 12(5), (2017)
Filippi, M.: Linking structural, metabolic and functional changes in multiple sclerosis. Eur. J. Neurol. 8(4), 291–297 (2001)
Mallik, S., Samson, R.S., Wheeler-Kingshott, C.A., Miller, D.H.: Imaging outcomes for trials of remyelination in multiple sclerosis. J. Neurol. Neurosurg. Psychiatry 85(12), 1396–1404 (2014)
Filippi, M., Preziosa, P., Rocca, M.A.: Microstructural MR imaging techniques in multiple sclerosis. Neuroimaging Clinics 27(2), 313–333 (2017)
Rocca, M.A., Amato, M.P., De Stefano, N., Enzinger, C., Geurts, J.J., Penner, I.K., Rovira, A., Sumowski, J.F., Valsasina, P., Filippi, M., et al.: Clinical and imaging assessment of cognitive dysfunction in multiple sclerosis. Lancet Neurol. 14(3), 302–317 (2015)
Stejskal, E.O., Tanner, J.E.: Spin diffusion measurements: spin echoes in the presence of a time-dependent field gradient. J. Chem. Phys. 42(1), 288–292 (1965)
Basser, P., Mattiello, J., Lebihan, D.: Estimation of the Effective Self-Diffusion Tensor from the NMR Spin Echo (1994)
Conturo, T.E., Lori, N.F., Cull, T.S., Akbudak, E., Snyder, A.Z., Shimony, J.S., McKinstry, R.C., Burton, H., Raichle, M.E.: Tracking neuronal fiber pathways in the living human brain. Proc. Natl. Acad. Sci. 96(18), 10422–10427 (1999)
Rovaris, M., Iannucci, G., Falautano, M., Possa, F., Martinelli, V., Comi, G., Filippi, M.: Cognitive dysfunction in patients with mildly disabling relapsing-remitting multiple sclerosis: an exploratory study with diffusion tensor MR imaging. J. Neurol. Sci. 195(2), 103–109 (2002)
Rovaris, M., Riccitelli, G., Judica, E., Possa, F., Caputo, D., Ghezzi, A., Bertolotto, A., Capra, R., Falautano, M., Mattioli, F., et al.: Cognitive impairment and structural brain damage in benign multiple sclerosis. Neurology 71(19), 1521–1526 (2008)
Akbar, N., Lobaugh, N.J., O’Connor, P., Moradzadeh, L., Scott, C.J., Feinstein, A.: Diffusion tensor imaging abnormalities in cognitively impaired multiple sclerosis patients. Canadian J. Neurol. Sci. 37(5), 608–614 (2010)
Mesaros, S., Rocca, M., Kacar, K., Kostic, J., Copetti, M., Stosic-Opincal, T., Preziosa, P., Sala, S., Riccitelli, G., Horsfield, M., et al.: Diffusion tensor mri tractography and cognitive impairment in multiple sclerosis. Neurology 78(13), 969–975 (2012)
Ciccarelli, O., Catani, M., Johansen-Berg, H., Clark, C., Thompson, A.: Diffusion-based tractography in neurological disorders: concepts, applications, and future developments. Lancet Neurol. 7(8), 715–727 (2008)
Lipp, I., Parker, G.D., Tallantyre, E.C., Goodall, A., Grama, S., Patitucci, E., Heveron, P., Tomassini, V., Jones, D.K.: Tractography in the presence of multiple sclerosis lesions. NeuroImage 209, (2020)
Jeurissen, B., Tournier, J.D., Dhollander, T., Connelly, A., Sijbers, J.: Multi-tissue constrained spherical deconvolution for improved analysis of multi-shell diffusion MRI data. NeuroImage 103, 411–426 (2014)
Smith, R.E., Tournier, J.D., Calamante, F., Connelly, A.: Anatomically-constrained tractography: improved diffusion mri streamlines tractography through effective use of anatomical information. NeuroImage 62(3), 1924–1938 (2012)
Girard, G., Whittingstall, K., Deriche, R., Descoteaux, M.: Towards quantitative connectivity analysis: reducing tractography biases. NeuroImage 98, 266–278 (2014)
Gajamange, S., Raffelt, D., Dhollander, T., Lui, E., van der Walt, A., Kilpatrick, T., Fielding, J., Connelly, A., Kolbe, S.: Fibre-specific white matter changes in multiple sclerosis patients with optic neuritis. NeuroImage: Clinical 17 (2018) 60–68
Mito, R., Raffelt, D., Dhollander, T., Vaughan, D.N., Tournier, J.D., Salvado, O., Brodtmann, A., Rowe, C.C., Villemagne, V.L., Connelly, A.: Fibre-specific white matter reductions in alzheimer’s disease and mild cognitive impairment. Brain 141(3), 888–902 (2018)
Tur, C., Grussu, F., Prados, F., Charalambous, T., Collorone, S., Kanber, B., Cawley, N., Altmann, D.R., Ourselin, S., Barkhof, F., et al.: A multi-shell multi-tissue diffusion study of brain connectivity in early multiple sclerosis. Multi. Sclerosis J. 1352458519845105 (2019)
Charalambous, T., Tur, C., Prados, F., Kanber, B., Chard, D.T., Ourselin, S., Clayden, J.D., Wheeler-Kingshott, C.A.G., Thompson, A.J., Toosy, A.T.: Structural network disruption markers explain disability in multiple sclerosis. J. Neurol. Neurosurg. Psychiatry 90(2), 219–226 (2019)
Dumont, M., Roy, M., Jodoin, P.M., Morency, F.C., Houde, J.C., Xie, Z., Bauer, C., Samad, T.A., Van Dijk, K.R., Goodman, J., et al.: Free water in white matter differentiates mci and ad from control subjects. Frontiers Aging Neurosci. 11, 270 (2019)
Beaudoin, A.M., Rheault, F., Theaud, G., Whittingstall, K., Lamontagne, A., Descoteaux, M.: White matter tractometry correlates with fatigue severity in young adults with multiple sclerosis (1322). Neurology 94(15 Supplement) (2020)
Storelli, L., Pagani, E., Preziosa, P., Filippi, M., Rocca, M.A.: Measurement of white matter fiber-bundle cross-section in multiple sclerosis using diffusion-weighted imaging. Multi. Sclerosis J. 1352458520938999 (2020)
Maier-Hein, K.H., Neher, P.F., Houde, J.C., Côté, M.A., Garyfallidis, E., Zhong, J., Chamberland, M., Yeh, F.C., Lin, Y.C., Ji, Q.: Others: The challenge of mapping the human connectome based on diffusion tractography. Nat. Commun. 8, 1349 (2017)
Jones, D.K., Knösche, T.R., Turner, R.: White matter integrity, fiber count, and other fallacies: The do’s and don’ts of diffusion MRI. NeuroImage 73, 239–254 (2013)
Schilling, K.G., Nath, V., Hansen, C., Parvathaneni, P., Blaber, J., Gao, Y., Neher, P., Aydogan, D.B., Shi, Y., Ocampo-Pineda, M., et al.: Limits to anatomical accuracy of diffusion tractography using modern approaches. NeuroImage 185, 1–11 (2019)
Wasserthal, J., Neher, P., Maier-Hein, K.H.: TractSeg—fast and accurate white matter tract segmentation. NeuroImage 183, 239–253 (2018)
Tallantyre, E.C., Major, P.C., Atherton, M.J., Davies, W.A., Joseph, F., Tomassini, V., Pickersgill, T.P., Harding, K.E., Willis, M.D., Winter, M., et al.: How common is truly benign ms in a uk population? J. Neurol. Neurosurg. Psychiatry 90(5), 522–528 (2019)
Fischer, J., Rudick, R., Cutter, G., Reingold, S., Force, N.M.S.C.O.A.T.: The multiple sclerosis functional composite measure (MSFC): an integrated approach to ms clinical outcome assessment. Multi. Sclerosis J. 5(4) 244–250 (1999)
Weiss, L.G., Saklofske, D.H., Coalson, D., Raiford, S.E.: WAIS-IV Clinical Use and Interpretation: Scientist-Practitioner Perspectives. Academic (2010)
Coughlan, A., Oddy, M., Crawford, J.: Birt Memory and Information Processing Battery (bmipb). Brain Injury Rehabilitation Trust, London (2007)
Delis, D.C., Kaplan, E., Kramer, J.H.: Delis-Kaplan Executive Function System (2001)
Veraart, J., Novikov, D.S., Christiaens, D., Ades-Aron, B., Sijbers, J., Fieremans, E.: Denoising of diffusion MRI using random matrix theory. NeuroImage 142, 394–406 (2016)
Andersson, J.L.R., Sotiropoulos, S.N.: An integrated approach to correction for off-resonance effects and subject movement in diffusion MR imaging. NeuroImage 125, 1063–1078 (2016)
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 20(2), 870–888 (2003)
Chamberland, M., Whittingstall, K., Fortin, D., Mathieu, D., Descoteaux, M.: Real-time multi-peak tractography for instantaneous connectivity display. Frontiers Neuroinf. 8, 59 (2014)
Filippi, M., Brück, W., Chard, D., Fazekas, F., Geurts, J.J., Enzinger, C., Hametner, S., Kuhlmann, T., Preziosa, P., Rovira, À., et al.: Association between pathological and mri findings in multiple sclerosis. Lancet Neurol. 18(2), 198–210 (2019)
Holland, C.M., Charil, A., Csapo, I., Liptak, Z., Ichise, M., Khoury, S.J., Bakshi, R., Weiner, H.L., Guttmann, C.R.: The relationship between normal cerebral perfusion patterns and white matter lesion distribution in 1,249 patients with multiple sclerosis. J. Neuroimaging 22(2), 129–136 (2012)
Filippi, M., Rocca, M.A., Martino, G., Horsfield, M.A., Comi, G.: Magnetization transfer changes in the normal appering white matter precede the appearance of enhancing lesions in patients with multiple sclerosis. Ann. Neurol. 43(6), 809–814 (1998)
Thiebaut de Schotten, M., Dell’Acqua, F., Ratiu, P., Leslie, A., Howells, H., Cabanis, E., Iba-Zizen, M., Plaisant, O., Simmons, A., Dronkers, N., et al.: From phineas gage and monsieur leborgne to hm: revisiting disconnection syndromes. Cerebral Cortex 25(12), 4812–4827 (2015)
Foulon, C., Cerliani, L., Kinkingnehun, S., Levy, R., Rosso, C., Urbanski, M., Volle, E., Thiebaut de Schotten, M.: Advanced lesion symptom mapping analyses and implementation as bcbtoolkit. Gigascience 7(3), giy004 (2018)
Fox, M.D.: Mapping symptoms to brain networks with the human connectome. New England J. Med. 379(23), 2237–2245 (2018)
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Chamberland, M., Winter, M., Brice, T.A.W., Jones, D.K., Tallantyre, E.C. (2021). Beyond Lesion-Load: Tractometry-Based Metrics for Characterizing White Matter Lesions within Fibre Pathways. In: Gyori, N., Hutter, J., Nath, V., Palombo, M., Pizzolato, M., Zhang, F. (eds) Computational Diffusion MRI. Mathematics and Visualization. Springer, Cham. https://doi.org/10.1007/978-3-030-73018-5_18
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