| Peer-Reviewed

Changes in Cortical Thickness Are Associated with Cognitive Impairments in Patients with White Matter Lesions

Received: 8 June 2022    Accepted: 27 June 2022    Published: 5 July 2022
Views:       Downloads:
Abstract

White matter lesions (WMLs) are closely related with cognitive impairment and dementia. It has been hypothesized that cognitive impairment is related to cortical atrophy and cortical thickness network measurements in certain brain regions. We aimed to investigate the characteristics of cortical thickness in patients with WMLs and the relationship that these characteristics have with cognitive function. In this study, 76 WML patients and 37 healthy controls (HC) were enrolled and underwent a T1-weighted 3-D MRI scan using a 3.0-Tesla scanner. According to cognitive assessment results, the WML patients were divided into two subgroups, namely the WMLs with non-dementia vascular cognitive impairment (WML-VCIND) group and the WMLs with vascular dementia (WML-VaD) group. Cortical surface thickness was estimated using FreeSurfer software. The correlation between cognitive function and cortical thickness in WML patients was analyzed. We found that MoCA scores and executive function were significantly decreased in WML-VCIND and WML-VaD patients compared to the HC group (P < 0.0001). Significantly reduced cortical thickness in the left precentral, caudal middle frontal, rostral middle frontal, superior frontal, middle temporal, transverse temporal, insula, bilateral pars opercularis, and superior temporal regions was found in the WML-VaD group compared to the HC group (P < 0.05). The reduced cortical thickness of the above gyrus was positively correlated with executive function in WML patients. These cross-sectional results suggest that decreased cortex thickness in certain gyri in WML patients might lead to cognitive decline. The correlation between cortical thickness changes and cognitive function holds promise for understanding the underlying causes of cognitive impairment in WMLs.

Published in Clinical Neurology and Neuroscience (Volume 6, Issue 2)
DOI 10.11648/j.cnn.20220602.12
Page(s) 29-36
Creative Commons

This is an Open Access article, distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution and reproduction in any medium or format, provided the original work is properly cited.

Copyright

Copyright © The Author(s), 2022. Published by Science Publishing Group

Keywords

White Matter Lesions, Cognition, Cortical Thickness, Magnetic Resonance Imaging

References
[1] Wardlaw, J. M.; Smith, E. E.; Biessels, G. J.; Cordonnier, C.; Fazekas, F.; Frayne, R.; Lindley, R. I.; O'Brien, J. T.; Barkhof, F.; Benavente, O. R.; Black, S. E.; Brayne, C.; Breteler, M.; Chabriat, H.; Decarli, C.; de Leeuw, F. E.; Doubal, F.; Duering, M.; Fox, N. C.; Greenberg, S.; Hachinski, V.; Kilimann, I.; Mok, V.; Oostenbrugge, R.; Pantoni, L.; Speck, O.; Stephan, B. C.; Teipel, S.; Viswanathan, A.; Werring, D.; Chen, C.; Smith, C.; van Buchem, M.; Norrving, B.; Gorelick, P. B.; Dichgans, M.; nEuroimaging, S. T. f. R. V. c. o., Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration. Lancet Neurol, 2013, 12 (8), 822-38.
[2] Biesbroek, J. M.; Lam, B. Y. K.; Zhao, L.; Tang, Y.; Wang, Z.; Abrigo, J.; Chu, W. W. C.; Wong, A.; Shi, L.; Kuijf, H. J.; Biessels, G. J.; Mok, V. C. T., High white matter hyperintensity burden in strategic white matter tracts relates to worse global cognitive performance in community-dwelling individuals. J Neurol Sci, 2020, 414, 116835.
[3] Hase, Y.; Horsburgh, K.; Ihara, M.; Kalaria, R. N., White matter degeneration in vascular and other ageing-related dementias. J Neurochem, 2018, 144 (5), 617-633.
[4] Sudo, F. K.; Alves, C. E.; Alves, G. S.; Ericeira-Valente, L.; Tiel, C.; Moreira, D. M.; Laks, J.; Engelhardt, E., White matter hyperintensities, executive function and global cognitive performance in vascular mild cognitive impairment. Arq Neuropsiquiatr, 2013, 71 (7), 431-6.
[5] Prins, N. D.; van Dijk, E. J.; den Heijer, T.; Vermeer, S. E.; Jolles, J.; Koudstaal, P. J.; Hofman, A.; Breteler, M. M., Cerebral small-vessel disease and decline in information processing speed, executive function and memory. Brain, 2005, 128 (Pt 9), 2034-41.
[6] Zhuang, Y.; Zeng, X.; Wang, B.; Huang, M.; Gong, H.; Zhou, F., Cortical Surface Thickness in the Middle-Aged Brain with White Matter Hyperintense Lesions. Front Aging Neurosci, 2017, 9, 225.
[7] Goto, M.; Hagiwara, A.; Fujita, S.; Hori, M.; Kamagata, K.; Aoki, S.; Abe, O.; Sakamoto, H.; Sakano, Y.; Kyogoku, S.; Daida, H., Influence of Mild White Matter Lesions on Voxel-based Morphometry. Magn Reson Med Sci, 2021, 20 (1), 40-46.
[8] Li, C.; Du, H.; Zheng, J.; Wang, J., A voxel-based morphometric analysis of cerebral gray matter in subcortical ischemic vascular dementia patients and normal aged controls. Int J Med Sci, 2011, 8 (6), 482-6.
[9] Liu, H.; Wang, L.; Geng, Z.; Zhu, Q.; Song, Z.; Chang, R.; Lv, H., A voxel-based morphometric study of age- and sex-related changes in white matter volume in the normal aging brain. Neuropsychiatr Dis Treat, 2016, 12, 453-65.
[10] Fischl, B., FreeSurfer. Neuroimage, 2012, 62 (2), 774-81.
[11] Wen, H. B.; Zhang, Z. X.; Niu, F. S.; Li, L., [The application of Montreal cognitive assessment in urban Chinese residents of Beijing]. Zhonghua Nei Ke Za Zhi, 2008, 47 (1), 36-9.
[12] Morris, J. C., The Clinical Dementia Rating (CDR): current version and scoring rules. Neurology, 1993, 43 (11), 2412-4.
[13] The, L. S. G.; Poggesi, A.; Pantoni, L.; Inzitari, D.; Fazekas, F.; Ferro, J.; O'Brien, J.; Hennerici, M.; Scheltens, P.; Erkinjuntti, T.; Visser, M.; Langhorne, P.; Chabriat, H.; Waldemar, G.; Wallin, A.; Wahlund, A., 2001-2011: A Decade of the LADIS (Leukoaraiosis And DISability) Study: What Have We Learned about White Matter Changes and Small-Vessel Disease? Cerebrovasc Dis, 2011, 32 (6), 577-588.
[14] Fleischman, D. A.; Leurgans, S.; Arfanakis, K.; Arvanitakis, Z.; Barnes, L. L.; Boyle, P. A.; Han, S. D.; Bennett, D. A., Gray-matter macrostructure in cognitively healthy older persons: associations with age and cognition. Brain Struct Funct, 2014, 219 (6), 2029-49.
[15] Alber J, Alladi S, Bae HJ, Barton DA, Beckett LA, Bell JM, Berman SE, Biessels GJ, Black SE, Bos I, Bowman GL, Brai E, Brickman AM, Callahan BL, Corriveau RA, Fossati S, Gottesman RF, Gustafson DR, Hachinski V, Hayden KM, Helman AM, Hughes TM, Isaacs JD, Jefferson AL, Johnson SC, Kapasi A, Kern S, Kwon JC, Kukolja J, Lee A, Lockhart SN, Murray A, Osborn KE, Power MC, Price BR, Rhodius-Meester HFM, Rondeau JA, Rosen AC, Rosene DL, Schneider JA, Scholtzova H, Shaaban CE, Silva NCBS, Snyder HM, Swardfager W, Troen AM, van Veluw SJ, Vemuri P, Wallin A, Wellington C, Wilcock DM, Xie SX, Hainsworth AH. White matter hyperintensities in vascular contributions to cognitive impairment and dementia (VCID): Knowledge gaps and opportunities. Alzheimers Dement (N Y). 2019 Apr 9; 5: 107-117.
[16] Prins, N. D.; Scheltens, P., White matter hyperintensities, cognitive impairment and dementia: an update. Nat Rev Neurol, 2015, 11 (3), 157-65.
[17] Pendlebury, S. T.; Cuthbertson, F. C.; Welch, S. J.; Mehta, Z.; Rothwell, P. M., Underestimation of cognitive impairment by Mini-Mental State Examination versus the Montreal Cognitive Assessment in patients with transient ischemic attack and stroke: a population-based study. Stroke, 2010, 41 (6), 1290-3.
[18] Rossi Espagnet, M. C.; Romano, A.; Carducci, F.; Calabria, L. F.; Fiorillo, M.; Orzi, F.; Bozzao, A., Grey matter volume alterations in CADASIL: a voxel-based morphometry study. J Headache Pain, 2012, 13 (3), 231-8.
[19] Jouvent, E.; Mangin, J. F.; Duchesnay, E.; Porcher, R.; During, M.; Mewald, Y.; Guichard, J. P.; Herve, D.; Reyes, S.; Zieren, N.; Dichgans, M.; Chabriat, H., Longitudinal changes of cortical morphology in CADASIL. Neurobiol Aging, 2012, 33 (5), 1002 e29-36.
[20] Godin, O.; Maillard, P.; Crivello, F.; Alperovitch, A.; Mazoyer, B.; Tzourio, C.; Dufouil, C., Association of white-matter lesions with brain atrophy markers: the three-city Dijon MRI study. Cerebrovasc Dis, 2009, 28 (2), 177-84.
[21] Righart, R.; Duering, M.; Gonik, M.; Jouvent, E.; Reyes, S.; Herve, D.; Chabriat, H.; Dichgans, M., Impact of regional cortical and subcortical changes on processing speed in cerebral small vessel disease. Neuroimage Clin, 2013, 2, 854-61.
[22] Fan, J.; Zhong, M.; Gan, J.; Liu, W.; Niu, C.; Liao, H.; Zhang, H.; Tan, C.; Yi, J.; Zhu, X., Spontaneous neural activity in the right superior temporal gyrus and left middle temporal gyrus is associated with insight level in obsessive-compulsive disorder. J Affect Disord, 2017, 207, 203-211.
[23] Wang, S.; Yuan, J.; Guo, X.; Teng, L.; Jiang, H.; Gu, H.; Hu, W.; Jiang, T., Correlation between prefrontal-striatal pathway impairment and cognitive impairment in patients with leukoaraiosis. Medicine (Baltimore), 2017, 96 (17), e6703.
[24] Kim, H. J.; Ye, B. S.; Yoon, C. W.; Noh, Y.; Kim, G. H.; Cho, H.; Jeon, S.; Lee, J. M.; Kim, J. H.; Seong, J. K.; Kim, C. H.; Choe, Y. S.; Lee, K. H.; Kim, S. T.; Kim, J. S.; Park, S. E.; Kim, J. H.; Chin, J.; Cho, J.; Kim, C.; Lee, J. H.; Weiner, M. W.; Na, D. L.; Seo, S. W., Cortical thickness and hippocampal shape in pure vascular mild cognitive impairment and dementia of subcortical type. Eur J Neurol, 2014, 21 (5), 744-51.
[25] Seo, H. S.; Kim, J. H.; Lee, D. H.; Lee, Y. H.; Suh, S. I.; Kim, S. Y.; Na, D. G., Nonenhancing intramedullary astrocytomas and other MR imaging features: a retrospective study and systematic review. AJNR Am J Neuroradiol, 2010, 31 (3), 498-503.
[26] Mok, V.; Wong, K. K.; Xiong, Y.; Wong, A.; Schmidt, R.; Chu, W.; Hu, X.; Leung, E. Y.; Chen, S.; Chen, Y.; Tang, W. K.; Chen, X.; Ho, C. L.; Wong, K. S.; Wong, S. T., Cortical and frontal atrophy are associated with cognitive impairment in age-related confluent white-matter lesion. J Neurol Neurosurg Psychiatry, 2011, 82 (1), 52-7.
[27] Kloppenborg, R. P.; Nederkoorn, P. J.; Geerlings, M. I.; van den Berg, E., Presence and progression of white matter hyperintensities and cognition: a meta-analysis. Neurology, 2014, 82 (23), 2127-38.
[28] Smith, E. E.; Egorova, S.; Blacker, D.; Killiany, R. J.; Muzikansky, A.; Dickerson, B. C.; Tanzi, R. E.; Albert, M. S.; Greenberg, S. M.; Guttmann, C. R., Magnetic resonance imaging white matter hyperintensities and brain volume in the prediction of mild cognitive impairment and dementia. Arch Neurol, 2008, 65 (1), 94-100.
[29] Arvanitakis, Z.; Fleischman, D. A.; Arfanakis, K.; Leurgans, S. E.; Barnes, L. L.; Bennett, D. A., Association of white matter hyperintensities and gray matter volume with cognition in older individuals without cognitive impairment. Brain Struct Funct, 2016, 221 (4), 2135-46.
[30] Debette, S.; Markus, H. S., The clinical importance of white matter hyperintensities on brain magnetic resonance imaging: systematic review and meta-analysis. BMJ, 2010, 341, c3666.
Cite This Article
  • APA Style

    Na Wei, Yufei Wei, Yuexiu Li, Decai Tian, Hongyan Chen, et al. (2022). Changes in Cortical Thickness Are Associated with Cognitive Impairments in Patients with White Matter Lesions. Clinical Neurology and Neuroscience, 6(2), 29-36. https://doi.org/10.11648/j.cnn.20220602.12

    Copy | Download

    ACS Style

    Na Wei; Yufei Wei; Yuexiu Li; Decai Tian; Hongyan Chen, et al. Changes in Cortical Thickness Are Associated with Cognitive Impairments in Patients with White Matter Lesions. Clin. Neurol. Neurosci. 2022, 6(2), 29-36. doi: 10.11648/j.cnn.20220602.12

    Copy | Download

    AMA Style

    Na Wei, Yufei Wei, Yuexiu Li, Decai Tian, Hongyan Chen, et al. Changes in Cortical Thickness Are Associated with Cognitive Impairments in Patients with White Matter Lesions. Clin Neurol Neurosci. 2022;6(2):29-36. doi: 10.11648/j.cnn.20220602.12

    Copy | Download

  • @article{10.11648/j.cnn.20220602.12,
      author = {Na Wei and Yufei Wei and Yuexiu Li and Decai Tian and Hongyan Chen and Yumei Zhang},
      title = {Changes in Cortical Thickness Are Associated with Cognitive Impairments in Patients with White Matter Lesions},
      journal = {Clinical Neurology and Neuroscience},
      volume = {6},
      number = {2},
      pages = {29-36},
      doi = {10.11648/j.cnn.20220602.12},
      url = {https://doi.org/10.11648/j.cnn.20220602.12},
      eprint = {https://article.sciencepublishinggroup.com/pdf/10.11648.j.cnn.20220602.12},
      abstract = {White matter lesions (WMLs) are closely related with cognitive impairment and dementia. It has been hypothesized that cognitive impairment is related to cortical atrophy and cortical thickness network measurements in certain brain regions. We aimed to investigate the characteristics of cortical thickness in patients with WMLs and the relationship that these characteristics have with cognitive function. In this study, 76 WML patients and 37 healthy controls (HC) were enrolled and underwent a T1-weighted 3-D MRI scan using a 3.0-Tesla scanner. According to cognitive assessment results, the WML patients were divided into two subgroups, namely the WMLs with non-dementia vascular cognitive impairment (WML-VCIND) group and the WMLs with vascular dementia (WML-VaD) group. Cortical surface thickness was estimated using FreeSurfer software. The correlation between cognitive function and cortical thickness in WML patients was analyzed. We found that MoCA scores and executive function were significantly decreased in WML-VCIND and WML-VaD patients compared to the HC group (P < 0.0001). Significantly reduced cortical thickness in the left precentral, caudal middle frontal, rostral middle frontal, superior frontal, middle temporal, transverse temporal, insula, bilateral pars opercularis, and superior temporal regions was found in the WML-VaD group compared to the HC group (P < 0.05). The reduced cortical thickness of the above gyrus was positively correlated with executive function in WML patients. These cross-sectional results suggest that decreased cortex thickness in certain gyri in WML patients might lead to cognitive decline. The correlation between cortical thickness changes and cognitive function holds promise for understanding the underlying causes of cognitive impairment in WMLs.},
     year = {2022}
    }
    

    Copy | Download

  • TY  - JOUR
    T1  - Changes in Cortical Thickness Are Associated with Cognitive Impairments in Patients with White Matter Lesions
    AU  - Na Wei
    AU  - Yufei Wei
    AU  - Yuexiu Li
    AU  - Decai Tian
    AU  - Hongyan Chen
    AU  - Yumei Zhang
    Y1  - 2022/07/05
    PY  - 2022
    N1  - https://doi.org/10.11648/j.cnn.20220602.12
    DO  - 10.11648/j.cnn.20220602.12
    T2  - Clinical Neurology and Neuroscience
    JF  - Clinical Neurology and Neuroscience
    JO  - Clinical Neurology and Neuroscience
    SP  - 29
    EP  - 36
    PB  - Science Publishing Group
    SN  - 2578-8930
    UR  - https://doi.org/10.11648/j.cnn.20220602.12
    AB  - White matter lesions (WMLs) are closely related with cognitive impairment and dementia. It has been hypothesized that cognitive impairment is related to cortical atrophy and cortical thickness network measurements in certain brain regions. We aimed to investigate the characteristics of cortical thickness in patients with WMLs and the relationship that these characteristics have with cognitive function. In this study, 76 WML patients and 37 healthy controls (HC) were enrolled and underwent a T1-weighted 3-D MRI scan using a 3.0-Tesla scanner. According to cognitive assessment results, the WML patients were divided into two subgroups, namely the WMLs with non-dementia vascular cognitive impairment (WML-VCIND) group and the WMLs with vascular dementia (WML-VaD) group. Cortical surface thickness was estimated using FreeSurfer software. The correlation between cognitive function and cortical thickness in WML patients was analyzed. We found that MoCA scores and executive function were significantly decreased in WML-VCIND and WML-VaD patients compared to the HC group (P < 0.0001). Significantly reduced cortical thickness in the left precentral, caudal middle frontal, rostral middle frontal, superior frontal, middle temporal, transverse temporal, insula, bilateral pars opercularis, and superior temporal regions was found in the WML-VaD group compared to the HC group (P < 0.05). The reduced cortical thickness of the above gyrus was positively correlated with executive function in WML patients. These cross-sectional results suggest that decreased cortex thickness in certain gyri in WML patients might lead to cognitive decline. The correlation between cortical thickness changes and cognitive function holds promise for understanding the underlying causes of cognitive impairment in WMLs.
    VL  - 6
    IS  - 2
    ER  - 

    Copy | Download

Author Information
  • Department of Neurology, Beijing Tiantan Hospital, Capital Medical University, Beijing, China

  • Department of Neurology, Beijing Tiantan Hospital, Capital Medical University, Beijing, China

  • Department of Rehabilitation, Beijing Tiantan Hospital, Capital Medical University, Beijing, China

  • Department of Neurology, Beijing Tiantan Hospital, Capital Medical University, Beijing, China

  • Department of Radiology, Beijing Tiantan Hospital, Capital Medical University, Beijing, China

  • Department of Rehabilitation, Beijing Tiantan Hospital, Capital Medical University, Beijing, China

  • Sections