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Current Medical Imaging

Editor-in-Chief

ISSN (Print): 1573-4056
ISSN (Online): 1875-6603

Research Article

Secondary Degeneration of White Matter Tract following Basal Ganglia Infarction: A Longitudinal Diffusion Tensor Imaging Study

Author(s): Shasha Zheng, Qixiang Lin, Miao Zhang, Hesheng Liu, Yong He and Jie Lu*

Volume 20, 2024

Published on: 29 November, 2023

Article ID: e15734056247080 Pages: 10

DOI: 10.2174/0115734056247080231116111402

Price: $65

Abstract

Introduction: We explored the relationship between secondary degeneration of white matter (WM) tracts and motor outcomes after left basal ganglia infarction and investigated alterations in the diffusion indices of WM tracts in distal areas.

Methods: Clinical neurological evaluations were accomplished using the Fugl–Meyer scale (FMS). Then, the fractional anisotropy (FA) of the bilateral superior corona radiata (SCR), cerebral peduncle (CP), corticospinal tracts (CST), and corpus callosum (CC) were measured in all patients and control subjects.

Results: Regional-based analysis revealed decreased FA values in the ipsilesional SCR, CP, and CST of the patients, compared to the control subjects at 5- time points. The relative FA (rFA) values of the SCR, CP, and CST decreased progressively with time, the lowest values recorded at 90 days before increasing slightly at 180 days after stroke. Compared to the contralateral areas, the FA values of the ipsilesional SCR and CST areas were significantly decreased (P=0.023), while those of the CP decreased at 180 days (P=0.008). Compared with the values at 7 days, the rFA values of the ipsilesional SCR and CP areas were significantly reduced at 14, 30, and 90 days, while those in the CST area were significantly reduced at 14, 90, and 180 days. The CP rFA value at 7 days correlated positively with the FM scores at 180 days (r=0.469, P=0.037).

Conclusion: This study provides an objective, comprehensive, and automated protocol for detecting secondary degeneration of WM, which is important in understanding rehabilitation mechanisms after stroke.

[1]
Zhang M, Lin Q, Lu J, et al. Pontine infarction: Diffusion-tensor imaging of motor pathways-a longitudinal study. Radiology 2015; 274(3): 841-50.
[http://dx.doi.org/10.1148/radiol.14140373] [PMID: 25356962]
[2]
Puig J, Blasco G, Schlaug G, et al. Diffusion tensor imaging as a prognostic biomarker for motor recovery and rehabilitation after stroke. Neuroradiology 2017; 59(4): 343-51.
[http://dx.doi.org/10.1007/s00234-017-1816-0] [PMID: 28293701]
[3]
Nagarajan A, Ravichandar R. Glioblastoma multiforme of spinal cord - Case series in a tertiary cancer centre. J Clin Transl Res 2021; 7(6): 792-6.
[PMID: 34988331]
[4]
Yu Q, Jiao Y, Huo R, et al. Application of the concept of neural networks surgery in cerebrovascular disease treatment. Brain & Heart 2022; 1(1): 223-3.
[http://dx.doi.org/10.36922/bh.v1i1.223]
[5]
Zhang L, Lei S, Hu Y, et al. Distinctive clinicopathological features and differential gene expression of cerebral venous thrombosis mimicking brain tumors. Brain & Heart 2023; 1(1): 188-8.
[http://dx.doi.org/10.36922/bh.v1i1.188]
[6]
Gandhi K, Gillihan L, Wozniak MA, Zhuo J, Raghavan P. Progressive Wallerian Degeneration of the Corpus Callosal Splenium in a Patient with Alexia without Agraphia: Advanced MR Findings. Neuroradiol J 2014; 27(6): 653-6.
[http://dx.doi.org/10.15274/NRJ-2014-10097] [PMID: 25489886]
[7]
Fukui K, Iguchi I, Kito A, Watanabe Y, Sugita K. Extent of pontine pyramidal tract Wallerian degeneration and outcome after supratentorial hemorrhagic stroke. Stroke 1994; 25(6): 1207-10.
[http://dx.doi.org/10.1161/01.STR.25.6.1207] [PMID: 8202981]
[8]
Zhang L, Xue H, Chen T, et al. Investigation of quantitative susceptibility mapping in diagnosis of tuberous sclerosis complex and assessment of associated brain injuries at 1.5 Tesla. J Clin Transl Res 2020; 5(3): 102-8.
[PMID: 32617425]
[9]
Mazumdar A, Mukherjee P, Miller JH, Malde H, McKinstry RC. Diffusion-weighted imaging of acute corticospinal tract injury preceding Wallerian degeneration in the maturing human brain. AJNR Am J Neuroradiol 2003; 24(6): 1057-66.
[PMID: 12812927]
[10]
Watanabe H, Tashiro K. Brunnstrom stages and Wallerian degenerations: A study using MRI. Tohoku J Exp Med 1992; 166(4): 471-3.
[http://dx.doi.org/10.1620/tjem.166.471] [PMID: 1502693]
[11]
Kuhn MJ, Johnson KA, Davis KR. Wallerian degeneration: Evaluation with MR imaging. Radiology 1988; 168(1): 199-202.
[http://dx.doi.org/10.1148/radiology.168.1.3380957] [PMID: 3380957]
[12]
Kuhn MJ, Mikulis DJ, Ayoub DM, Kosofsky BE, Davis KR, Taveras JM. Wallerian degeneration after cerebral infarction: Evaluation with sequential MR imaging. Radiology 1989; 172(1): 179-82.
[http://dx.doi.org/10.1148/radiology.172.1.2740501] [PMID: 2740501]
[13]
Liu X, Tian W, Qiu X, et al. Correlation analysis of quantitative diffusion parameters in ipsilateral cerebral peduncle during Wallerian degeneration with motor function outcome after cerebral ischemic stroke. J Neuroimaging 2012; 22(3): 255-60.
[http://dx.doi.org/10.1111/j.1552-6569.2011.00617.x] [PMID: 21699612]
[14]
Schaechter JD, Perdue KL, Wang R. Structural damage to the corticospinal tract correlates with bilateral sensorimotor cortex reorganization in stroke patients. Neuroimage 2008; 39(3): 1370-82.
[http://dx.doi.org/10.1016/j.neuroimage.2007.09.071] [PMID: 18024157]
[15]
Schaechter JD, Fricker ZP, Perdue KL, et al. Microstructural status of ipsilesional and contralesional corticospinal tract correlates with motor skill in chronic stroke patients. Hum Brain Mapp 2009; 30(11): 3461-74.
[http://dx.doi.org/10.1002/hbm.20770] [PMID: 19370766]
[16]
Ward NS, Newton JM, Swayne OBC, et al. Motor system activation after subcortical stroke depends on corticospinal system integrity. Brain 2006; 129(3): 809-19.
[http://dx.doi.org/10.1093/brain/awl002] [PMID: 16421171]
[17]
Lindenberg R, Renga V, Zhu LL, Betzler F, Alsop D, Schlaug G. Structural integrity of corticospinal motor fibers predicts motor impairment in chronic stroke. Neurology 2010; 74(4): 280-7.
[http://dx.doi.org/10.1212/WNL.0b013e3181ccc6d9] [PMID: 20101033]
[18]
Schiemanck SK, Kwakkel G, Post MWM, Kappelle LJ, Prevo AJH. Predicting long-term independency in activities of daily living after middle cerebral artery stroke: Does information from MRI have added predictive value compared with clinical information? Stroke 2006; 37(4): 1050-4.
[http://dx.doi.org/10.1161/01.STR.0000206462.09410.6f] [PMID: 16497980]
[19]
Smith SM, Jenkinson M, Johansen-Berg H, et al. Tract-based spatial statistics: Voxelwise analysis of multi-subject diffusion data. Neuroimage 2006; 31(4): 1487-505.
[http://dx.doi.org/10.1016/j.neuroimage.2006.02.024] [PMID: 16624579]
[20]
Mori S, Oishi K, Jiang H, et al. Stereotaxic white matter atlas based on diffusion tensor imaging in an ICBM template. Neuroimage 2008; 40(2): 570-82.
[http://dx.doi.org/10.1016/j.neuroimage.2007.12.035] [PMID: 18255316]
[21]
Yu C, Zhu C, Zhang Y, et al. A longitudinal diffusion tensor imaging study on Wallerian degeneration of corticospinal tract after motor pathway stroke. Neuroimage 2009; 47(2): 451-8.
[http://dx.doi.org/10.1016/j.neuroimage.2009.04.066] [PMID: 19409500]
[22]
Qiu M, Darling WG, Morecraft RJ, Ni CC, Rajendra J, Butler AJ. White matter integrity is a stronger predictor of motor function than BOLD response in patients with stroke. Neurorehabil Neural Repair 2011; 25(3): 275-84.
[http://dx.doi.org/10.1177/1545968310389183] [PMID: 21357529]
[23]
Puig J, Pedraza S, Blasco G. Wallerian degeneration in the corticospinal tract evaluated by diffusion tensor imaging correlates with motor deficit 30 days after middle cerebral artery ischemic stroke. AJNR Am J Neuroradiol 2010; 31(7): 1324-30.
[http://dx.doi.org/10.3174/ajnr.A2038]
[24]
Cai J, Ji Q, Xin R, et al. Contralesional Cortical Structural Reorganization Contributes to Motor Recovery after Sub-Cortical Stroke: A Longitudinal Voxel-Based Morphometry Study. Front Hum Neurosci 2016; 10: 393.
[http://dx.doi.org/10.3389/fnhum.2016.00393] [PMID: 27536229]
[25]
Thomalla G, Glauche V, Koch MA, Beaulieu C, Weiller C, Röther J. Diffusion tensor imaging detects early Wallerian degeneration of the pyramidal tract after ischemic stroke. Neuroimage 2004; 22(4): 1767-74.
[http://dx.doi.org/10.1016/j.neuroimage.2004.03.041] [PMID: 15275932]
[26]
Liang Z, Zeng J, Zhang C, et al. Longitudinal investigations on the anterograde and retrograde degeneration in the pyramidal tract following pontine infarction with diffusion tensor imaging. Cerebrovasc Dis 2008; 25(3): 209-16.
[http://dx.doi.org/10.1159/000113858] [PMID: 18216462]
[27]
Martin A, Stillman J, Miguez MJ, et al. The effect of dietary supplementation on brain-derived neurotrophic factor and cognitive functioning in Alzheimer’s dementia. J Clin Transl Res 2017; 3(3): 337-43.
[http://dx.doi.org/10.18053/jctres.03.201703.006] [PMID: 30895275]
[28]
Liang Z, Zeng J, Liu S, et al. A prospective study of secondary degeneration following subcortical infarction using diffusion tensor imaging. J Neurol Neurosurg Psychiatry 2007; 78(6): 581-6.
[http://dx.doi.org/10.1136/jnnp.2006.099077] [PMID: 17237143]
[29]
Yin D, Yan X, Fan M. Secondary degeneration detected by combining voxel-based morphometry and tract-based spatial statistics in subcortical strokes with different outcomes in hand function. AJNR Am J Neuroradiol 2013; 34(7): 1341-7.
[http://dx.doi.org/10.3174/ajnr.A3410]
[30]
Muhammad Atif M, Afzal F. The effects of a task-oriented walking intervention on improving balance self-efficacy in post-stroke patients. Adv Neurol 2023; 2(2): 388.
[http://dx.doi.org/10.36922/an.388]
[31]
Koyama T, Marumoto K, Miyake H, Domen K. Relationship between diffusion tensor fractional anisotropy and long-term motor outcome in patients with hemiparesis after middle cerebral artery infarction. J Stroke Cerebrovasc Dis 2014; 23(9): 2397-404.
[http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2014.05.017] [PMID: 25169825]
[32]
Pierpaoli C, Barnett A, Pajevic S, et al. Water diffusion changes in Wallerian degeneration and their dependence on white matter architecture. Neuroimage 2001; 13(6): 1174-85.
[http://dx.doi.org/10.1006/nimg.2001.0765] [PMID: 11352623]
[33]
Doron K, Gazzaniga M. Neuroimaging techniques offer new perspectives on callosal transfer and interhemispheric communication. Cortex 2008; 44(8): 1023-9.
[http://dx.doi.org/10.1016/j.cortex.2008.03.007] [PMID: 18672233]
[34]
Gazzaniga MS. Cerebral specialization and interhemispheric communication: Does the corpus callosum enable the human condition? Brain 2000; 123(7): 1293-326.
[http://dx.doi.org/10.1093/brain/123.7.1293] [PMID: 10869045]
[35]
Bonzano L, Tacchino A, Roccatagliata L, Abbruzzese G, Mancardi GL, Bove M. Callosal contributions to simultaneous bimanual finger movements. J Neurosci 2008; 28(12): 3227-33.
[http://dx.doi.org/10.1523/JNEUROSCI.4076-07.2008] [PMID: 18354026]
[36]
Johansen-Berg H, Della-Maggiore V, Behrens TEJ, Smith SM, Paus T. Integrity of white matter in the corpus callosum correlates with bimanual co-ordination skills. Neuroimage 2007; 36(Suppl 2) (Suppl. 2): T16-21.
[http://dx.doi.org/10.1016/j.neuroimage.2007.03.041] [PMID: 17499163]
[37]
Lenzi D, Conte A, Mainero C, et al. Effect of corpus callosum damage on ipsilateral motor activation in patients with multiple sclerosis: A functional and anatomical study. Hum Brain Mapp 2007; 28(7): 636-44.
[http://dx.doi.org/10.1002/hbm.20305] [PMID: 17080438]
[38]
Putnam MC, Wig GS, Grafton ST, Kelley WM, Gazzaniga MS. Structural organization of the corpus callosum predicts the extent and impact of cortical activity in the nondominant hemisphere. J Neurosci 2008; 28(11): 2912-8.
[http://dx.doi.org/10.1523/JNEUROSCI.2295-07.2008] [PMID: 18337422]
[39]
Wang LE, Tittgemeyer M, Imperati D, et al. Degeneration of corpus callosum and recovery of motor function after stroke: A multimodal magnetic resonance imaging study. Hum Brain Mapp 2012; 33(12): 2941-56.
[http://dx.doi.org/10.1002/hbm.21417] [PMID: 22020952]
[40]
Oudeman J, Nederveen AJ, Strijkers GJ, Maas M, Luijten PR, Froeling M. Techniques and applications of skeletal muscle diffusion tensor imaging: A review. J Magn Reson Imaging 2016; 43(4): 773-88.
[http://dx.doi.org/10.1002/jmri.25016] [PMID: 26221741]
[41]
Haque ME, Gabr RE, Hasan KM, et al. Ongoing Secondary Degeneration of the Limbic System in Patients With Ischemic Stroke: A Longitudinal MRI Study. Front Neurol 2019; 10: 154.
[http://dx.doi.org/10.3389/fneur.2019.00154] [PMID: 30890995]
[42]
Li J, Rong DD, Shan Y, Zhang M, Zhao C, Lu J. Brain Abnormalities in Pontine Infarction: A Longitudinal Diffusion Tensor Imaging and Functional Magnetic Resonance Imaging study. J Stroke Cerebrovasc Dis 2022; 31(2): 106205.
[http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2021.106205] [PMID: 34879300]
[43]
Simpkins AN, Dias C, Norato G, Kim E, Leigh R. Early Change in Stroke Size Performs Best in Predicting Response to Therapy. Cerebrovasc Dis 2017; 44(3-4): 141-9.
[http://dx.doi.org/10.1159/000477945] [PMID: 28683442]
[44]
Huhn K, Engelhorn T, Linker RA, Nagel AM. Potential of Sodium MRI as a Biomarker for Neurodegeneration and Neuroinflammation in Multiple Sclerosis. Front Neurol 2019; 10: 84.
[http://dx.doi.org/10.3389/fneur.2019.00084] [PMID: 30804885]
[45]
Crowe MJ, Bresnahan JC, Shuman SL, Masters JN, Beattie MS. Apoptosis and delayed degeneration after spinal cord injury in rats and monkeys. Nat Med 1997; 3(1): 73-6.
[http://dx.doi.org/10.1038/nm0197-73] [PMID: 8986744]
[46]
Marin MA, Carmichael ST. Mechanisms of demyelination and remyelination in the young and aged brain following white matter stroke. Neurobiol Dis 2019; 126: 5-12.
[http://dx.doi.org/10.1016/j.nbd.2018.07.023] [PMID: 30031782]
[47]
Kim B, Winstein C. Can Neurological Biomarkers of Brain Impairment Be Used to Predict Poststroke Motor Recovery? A Systematic Review. Neurorehabil Neural Repair 2017; 31(1): 3-24.
[http://dx.doi.org/10.1177/1545968316662708] [PMID: 27503908]

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