Skip to main content
Top
Published in: BMC Neurology 1/2018

Open Access 01-12-2018 | Research article

Evaluation of patients with relapsing-remitting multiple sclerosis using tract-based spatial statistics analysis: diffusion kurtosis imaging

Authors: Hai Qing Li, Bo Yin, Chao Quan, Dao Ying Geng, Hai Yu, Yi Fang Bao, Jun Liu, Yu Xin Li

Published in: BMC Neurology | Issue 1/2018

Login to get access

Abstract

Background

Diffusion kurtosis imaging (DKI) has the potential to provide microstructural insights into myelin and axonal pathology with additional kurtosis parameters. To our knowledge, few studies are available in the current literature using DKI by tract-based spatial statistics (TBSS) analysis in patients with multiple sclerosis (MS). The aim of this study is to assess the performance of commonly used parameters derived from DKI and diffusion tensor imaging (DTI) in detecting microstructural changes and associated pathology in relapsing remitting MS (RRMS).

Methods

Thirty-six patients with RRMS and 49 age and sex matched healthy controls underwent DKI. The brain tissue integrity was assessed by fractional anisotropy (FA), mean diffusivity (MD), axial diffusivity (Da), radial diffusivity (Dr), mean kurtosis (MK), axial kurtosis (Ka) and radial kurtosis (Kr) of DKI and FA, MD, Da and Dr of DTI. Group differences in these parameters were compared using TBSS (P < 0.01, corrected). To compare the sensitivity of these parameters in detecting white matter (WM) damage, the percentage of the abnormal voxels based on TBSS analysis, relative to the whole skeleton voxels for each parameter was calculated.

Results

The sensitivities in detecting WM abnormality in RRMS were MK (78.2%) > Kr (76.7%) > Ka (53.5%) and Dr (78.8%) > MD (76.7%) > FA (74.1%) > Da (28.3%) for DKI, and Dr (79.8%) > MD (79.5%) > FA (68.6%) > Da (40.1%) for DTI. DKI-derived diffusion parameters (FA, MD, and Dr) were sensitive for detecting abnormality in WM regions with coherent fiber arrangement; however, the kurtosis parameters (MK and Kr) were sensitive to discern abnormalities in WM regions with complex fiber arrangement.

Conclusions

The diffusion and kurtosis parameters could provide complementary information for revealing brain microstructural damage in RRMS. Dr and DKI_Kr may be regarded as useful surrogate markers for reflecting pathological changes in RRMS.
Literature
1.
go back to reference Frohman EM, Racke MK, Raine CS. Multiple sclerosis--the plaque and its pathogenesis. N Engl J Med. 2006;354(9):942–55.CrossRefPubMed Frohman EM, Racke MK, Raine CS. Multiple sclerosis--the plaque and its pathogenesis. N Engl J Med. 2006;354(9):942–55.CrossRefPubMed
2.
go back to reference Basser PJ, Jones DK. Diffusion-tensor MRI: theory, experimental design and data analysis - a technical review. NMR Biomed. 2002;15(7–8):456–67.CrossRefPubMed Basser PJ, Jones DK. Diffusion-tensor MRI: theory, experimental design and data analysis - a technical review. NMR Biomed. 2002;15(7–8):456–67.CrossRefPubMed
3.
go back to reference Tuch DS, Reese TG, Wiegell MR, Wedeen VJ. Diffusion MRI of complex neural architecture. Neuron. 2003;40(5):885–95.CrossRefPubMed Tuch DS, Reese TG, Wiegell MR, Wedeen VJ. Diffusion MRI of complex neural architecture. Neuron. 2003;40(5):885–95.CrossRefPubMed
4.
go back to reference Abdallah CG, Tang CY, Mathew SJ, Martinez J, Hof PR, Perera TD, Shungu DC, Gorman JM, Coplan JD. Diffusion tensor imaging in studying white matter complexity: a gap junction hypothesis. Neurosci Lett. 2010;475(3):161–4.CrossRefPubMedPubMedCentral Abdallah CG, Tang CY, Mathew SJ, Martinez J, Hof PR, Perera TD, Shungu DC, Gorman JM, Coplan JD. Diffusion tensor imaging in studying white matter complexity: a gap junction hypothesis. Neurosci Lett. 2010;475(3):161–4.CrossRefPubMedPubMedCentral
5.
go back to reference Hui ES, Cheung MM, Qi L, Wu EX. Towards better MR characterization of neural tissues using directional diffusion kurtosis analysis. NeuroImage. 2008;42(1):122–34.CrossRefPubMed Hui ES, Cheung MM, Qi L, Wu EX. Towards better MR characterization of neural tissues using directional diffusion kurtosis analysis. NeuroImage. 2008;42(1):122–34.CrossRefPubMed
7.
go back to reference Jensen JH, Helpern JA, 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(6):1432–40.CrossRefPubMed Jensen JH, Helpern JA, 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(6):1432–40.CrossRefPubMed
8.
go back to reference Falangola MF, Jensen JH, Babb JS, Hu C, Castellanos FX, Di Martino A, Ferris SH, Helpern JA. Age-related non-Gaussian diffusion patterns in the prefrontal brain. Journal of magnetic resonance imaging: JMRI. 2008;28(6):1345–50.CrossRefPubMed Falangola MF, Jensen JH, Babb JS, Hu C, Castellanos FX, Di Martino A, Ferris SH, Helpern JA. Age-related non-Gaussian diffusion patterns in the prefrontal brain. Journal of magnetic resonance imaging: JMRI. 2008;28(6):1345–50.CrossRefPubMed
9.
go back to reference Zhuo J, Xu S, Proctor JL, Mullins RJ, Simon JZ, Fiskum G, Gullapalli RP. Diffusion kurtosis as an in vivo imaging marker for reactive astrogliosis in traumatic brain injury. NeuroImage. 2012;59(1):467–77.CrossRefPubMed Zhuo J, Xu S, Proctor JL, Mullins RJ, Simon JZ, Fiskum G, Gullapalli RP. Diffusion kurtosis as an in vivo imaging marker for reactive astrogliosis in traumatic brain injury. NeuroImage. 2012;59(1):467–77.CrossRefPubMed
10.
go back to reference Guglielmetti C, Veraart J, Roelant E, Mai Z, Daans J, Van Audekerke J, Naeyaert M, Vanhoutte G, Delgado YPR, Praet J, Fieremans E, Ponsaerts P, Sijbers J, Van der Linden A, Verhoye M. Diffusion kurtosis imaging probes cortical alterations and white matter pathology following cuprizone induced demyelination and spontaneous remyelination. NeuroImage. 2016;125:363–77.CrossRefPubMed Guglielmetti C, Veraart J, Roelant E, Mai Z, Daans J, Van Audekerke J, Naeyaert M, Vanhoutte G, Delgado YPR, Praet J, Fieremans E, Ponsaerts P, Sijbers J, Van der Linden A, Verhoye M. Diffusion kurtosis imaging probes cortical alterations and white matter pathology following cuprizone induced demyelination and spontaneous remyelination. NeuroImage. 2016;125:363–77.CrossRefPubMed
11.
go back to reference Raz E, Bester M, Sigmund EE, Tabesh A, Babb JS, Jaggi H, Helpern J, Mitnick RJ, Inglese M. A better characterization of spinal cord damage in multiple sclerosis: a diffusional kurtosis imaging study. AJNR Am J Neuroradiol. 2013;34(9):1846–52.CrossRefPubMed Raz E, Bester M, Sigmund EE, Tabesh A, Babb JS, Jaggi H, Helpern J, Mitnick RJ, Inglese M. A better characterization of spinal cord damage in multiple sclerosis: a diffusional kurtosis imaging study. AJNR Am J Neuroradiol. 2013;34(9):1846–52.CrossRefPubMed
12.
go back to reference Yoshida M, Hori M, Yokoyama K, Fukunaga I, Suzuki M, Kamagata K, Shimoji K, Nakanishi A, Hattori N, Masutani Y, et al. Diffusional kurtosis imaging of normal-appearing white matter in multiple sclerosis: preliminary clinical experience. Jpn J Radiol. 2013;31(1):50–5.CrossRefPubMed Yoshida M, Hori M, Yokoyama K, Fukunaga I, Suzuki M, Kamagata K, Shimoji K, Nakanishi A, Hattori N, Masutani Y, et al. Diffusional kurtosis imaging of normal-appearing white matter in multiple sclerosis: preliminary clinical experience. Jpn J Radiol. 2013;31(1):50–5.CrossRefPubMed
13.
go back to reference Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE, Mackay CE, Watkins KE, Ciccarelli O, Cader MZ, Matthews PM, et al. Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. NeuroImage. 2006;31(4):1487–505.CrossRefPubMed Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE, Mackay CE, Watkins KE, Ciccarelli O, Cader MZ, Matthews PM, et al. Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. NeuroImage. 2006;31(4):1487–505.CrossRefPubMed
14.
go back to reference Polman CH, Reingold SC, Banwell B, Clanet M, Cohen JA, Filippi M, Fujihara K, Havrdova E, Hutchinson M, Kappos L, et al. Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria. Ann Neurol. 2011;69(2):292–302.CrossRefPubMedPubMedCentral Polman CH, Reingold SC, Banwell B, Clanet M, Cohen JA, Filippi M, Fujihara K, Havrdova E, Hutchinson M, Kappos L, et al. Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria. Ann Neurol. 2011;69(2):292–302.CrossRefPubMedPubMedCentral
15.
go back to reference Zhu J, Zhuo C, Qin W, Wang D, Ma X, Zhou Y, Yu C. Performances of diffusion kurtosis imaging and diffusion tensor imaging in detecting white matter abnormality in schizophrenia. NeuroImage Clinical. 2015;7:170–6.CrossRefPubMed Zhu J, Zhuo C, Qin W, Wang D, Ma X, Zhou Y, Yu C. Performances of diffusion kurtosis imaging and diffusion tensor imaging in detecting white matter abnormality in schizophrenia. NeuroImage Clinical. 2015;7:170–6.CrossRefPubMed
16.
go back to reference Vrenken H, Geurts JJ, Knol DL, van Dijk LN, Dattola V, Jasperse B, van Schijndel RA, Polman CH, Castelijns JA, Barkhof F, et al. Whole-brain T1 mapping in multiple sclerosis: global changes of normal-appearing gray and white matter. Radiology. 2006;240(3):811–20.CrossRefPubMed Vrenken H, Geurts JJ, Knol DL, van Dijk LN, Dattola V, Jasperse B, van Schijndel RA, Polman CH, Castelijns JA, Barkhof F, et al. Whole-brain T1 mapping in multiple sclerosis: global changes of normal-appearing gray and white matter. Radiology. 2006;240(3):811–20.CrossRefPubMed
17.
go back to reference Roosendaal SD, Geurts JJ, Vrenken H, Hulst HE, Cover KS, Castelijns JA, Pouwels PJ, Barkhof F. Regional DTI differences in multiple sclerosis patients. NeuroImage. 2009;44(4):1397–403.CrossRefPubMed Roosendaal SD, Geurts JJ, Vrenken H, Hulst HE, Cover KS, Castelijns JA, Pouwels PJ, Barkhof F. Regional DTI differences in multiple sclerosis patients. NeuroImage. 2009;44(4):1397–403.CrossRefPubMed
18.
go back to reference Bester M, Jensen JH, Babb JS, Tabesh A, Miles L, Herbert J, Grossman RI, Inglese M. Non-Gaussian diffusion MRI of gray matter is associated with cognitive impairment in multiple sclerosis. Mult Scler. 2015;21(7):935–44.CrossRefPubMed Bester M, Jensen JH, Babb JS, Tabesh A, Miles L, Herbert J, Grossman RI, Inglese M. Non-Gaussian diffusion MRI of gray matter is associated with cognitive impairment in multiple sclerosis. Mult Scler. 2015;21(7):935–44.CrossRefPubMed
19.
go back to reference de Kouchkovsky I, Fieremans E, Fleysher L, Herbert J, Grossman RI, Inglese M. Quantification of normal-appearing white matter tract integrity in multiple sclerosis: a diffusion kurtosis imaging study. J Neurol. 2016;263(6):1146–55.CrossRefPubMedPubMedCentral de Kouchkovsky I, Fieremans E, Fleysher L, Herbert J, Grossman RI, Inglese M. Quantification of normal-appearing white matter tract integrity in multiple sclerosis: a diffusion kurtosis imaging study. J Neurol. 2016;263(6):1146–55.CrossRefPubMedPubMedCentral
20.
go back to reference Liu Y, Duan Y, He Y, Yu C, Wang J, Huang J, Ye J, Parizel PM, Li K, Shu N. Whole brain white matter changes revealed by multiple diffusion metrics in multiple sclerosis: a TBSS study. Eur J Radiol. 2012;81(10):2826–32.CrossRefPubMed Liu Y, Duan Y, He Y, Yu C, Wang J, Huang J, Ye J, Parizel PM, Li K, Shu N. Whole brain white matter changes revealed by multiple diffusion metrics in multiple sclerosis: a TBSS study. Eur J Radiol. 2012;81(10):2826–32.CrossRefPubMed
21.
go back to reference Yu HJ, Christodoulou C, Bhise V, Greenblatt D, Patel Y, Serafin D, Maletic-Savatic M, Krupp LB, Wagshul ME. Multiple white matter tract abnormalities underlie cognitive impairment in RRMS. NeuroImage. 2012;59(4):3713–22.CrossRefPubMed Yu HJ, Christodoulou C, Bhise V, Greenblatt D, Patel Y, Serafin D, Maletic-Savatic M, Krupp LB, Wagshul ME. Multiple white matter tract abnormalities underlie cognitive impairment in RRMS. NeuroImage. 2012;59(4):3713–22.CrossRefPubMed
22.
go back to reference Douaud G, Jbabdi S, Behrens TE, Menke RA, Gass A, Monsch AU, Rao A, Whitcher B, Kindlmann G, Matthews PM, et al. DTI measures in crossing-fibre areas: increased diffusion anisotropy reveals early white matter alteration in MCI and mild Alzheimer's disease. NeuroImage. 2011;55(3):880–90.CrossRefPubMed Douaud G, Jbabdi S, Behrens TE, Menke RA, Gass A, Monsch AU, Rao A, Whitcher B, Kindlmann G, Matthews PM, et al. DTI measures in crossing-fibre areas: increased diffusion anisotropy reveals early white matter alteration in MCI and mild Alzheimer's disease. NeuroImage. 2011;55(3):880–90.CrossRefPubMed
23.
go back to reference Vos SB, Jones DK, Jeurissen B, Viergever MA, Leemans A. The influence of complex white matter architecture on the mean diffusivity in diffusion tensor MRI of the human brain. NeuroImage. 2012;59(3):2208–16.CrossRefPubMed Vos SB, Jones DK, Jeurissen B, Viergever MA, Leemans A. The influence of complex white matter architecture on the mean diffusivity in diffusion tensor MRI of the human brain. NeuroImage. 2012;59(3):2208–16.CrossRefPubMed
24.
go back to reference Wu EX, Cheung MM. MR diffusion kurtosis imaging for neural tissue characterization. NMR Biomed. 2010;23(7):836–48.CrossRefPubMed Wu EX, Cheung MM. MR diffusion kurtosis imaging for neural tissue characterization. NMR Biomed. 2010;23(7):836–48.CrossRefPubMed
25.
go back to reference Sun SW, Liang HF, Le TQ, Armstrong RC, Cross AH, Song SK. Differential sensitivity of in vivo and ex vivo diffusion tensor imaging to evolving optic nerve injury in mice with retinal ischemia. NeuroImage. 2006;32(3):1195–204.CrossRefPubMed Sun SW, Liang HF, Le TQ, Armstrong RC, Cross AH, Song SK. Differential sensitivity of in vivo and ex vivo diffusion tensor imaging to evolving optic nerve injury in mice with retinal ischemia. NeuroImage. 2006;32(3):1195–204.CrossRefPubMed
26.
go back to reference Song SK, Sun SW, Ju WK, Lin SJ, Cross AH, Neufeld AH. Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. NeuroImage. 2003;20(3):1714–22.CrossRefPubMed Song SK, Sun SW, Ju WK, Lin SJ, Cross AH, Neufeld AH. Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. NeuroImage. 2003;20(3):1714–22.CrossRefPubMed
27.
go back to reference Lin F, Yu C, Jiang T, Li K, Chan P. Diffusion tensor tractography-based group mapping of the pyramidal tract in relapsing-remitting multiple sclerosis patients. AJNR Am J Neuroradiol. 2007;28(2):278–82.PubMed Lin F, Yu C, Jiang T, Li K, Chan P. Diffusion tensor tractography-based group mapping of the pyramidal tract in relapsing-remitting multiple sclerosis patients. AJNR Am J Neuroradiol. 2007;28(2):278–82.PubMed
28.
go back to reference Henry RG, Oh J, Nelson SJ, Pelletier D. Directional diffusion in relapsing-remitting multiple sclerosis: a possible in vivo signature of Wallerian degeneration. Journal of magnetic resonance imaging : JMRI. 2003;18(4):420–6.CrossRefPubMed Henry RG, Oh J, Nelson SJ, Pelletier D. Directional diffusion in relapsing-remitting multiple sclerosis: a possible in vivo signature of Wallerian degeneration. Journal of magnetic resonance imaging : JMRI. 2003;18(4):420–6.CrossRefPubMed
Metadata
Title
Evaluation of patients with relapsing-remitting multiple sclerosis using tract-based spatial statistics analysis: diffusion kurtosis imaging
Authors
Hai Qing Li
Bo Yin
Chao Quan
Dao Ying Geng
Hai Yu
Yi Fang Bao
Jun Liu
Yu Xin Li
Publication date
01-12-2018
Publisher
BioMed Central
Published in
BMC Neurology / Issue 1/2018
Electronic ISSN: 1471-2377
DOI
https://doi.org/10.1186/s12883-018-1108-2

Other articles of this Issue 1/2018

BMC Neurology 1/2018 Go to the issue