Cortical Microstructural Involvement in Cerebral Small Vessel Disease

Overview

Journal Cereb Circ Cogn Behav

Date 2024 Mar 21

PMID 38510580

Authors

Annemarie Reilander

Marlene Engel

Ulrike Noth

Ralf Deichmann

Manoj Shrestha

Marlies Wagner

Rene-Maxime Gracien

Alexander Seiler

Affiliations

Soon will be listed here.

Abstract

Background: In cerebral small vessel disease (CSVD), cortical atrophy occurs at a later stage compared to microstructural abnormalities and therefore cannot be used for monitoring short-term disease progression. We aimed to investigate whether cortical diffusion tensor imaging (DTI) and quantitative (q) magnetic resonance imaging (MRI) are able to detect early microstructural involvement of the cerebral cortex in CSVD.

Materials And Methods: 33 CSVD patients without significant cortical or whole-brain atrophy and 16 healthy control subjects were included and underwent structural MRI, DTI and high-resolution qMRI with T, T* and T mapping at 3 T as well as comprehensive cognitive assessment. After tissue segmentation and reconstruction of the cortical boundaries with the Freesurfer software, DTI and qMRI parameters were saved as surface datasets and averaged across all vertices.

Results: Cortical diffusivity and quantitative T values were significantly increased in patients compared to controls ( < 0.05). T values correlated significantly positively with white matter hyperintensity (WMH) volume ( < 0.01). Both cortical diffusivity and T showed significant negative associations with axonal damage to the white matter fiber tracts ( < 0.05).

Conclusions: Cortical diffusivity and quantitative T mapping are suitable to detect microstructural involvement of the cerebral cortex in CSVD and represent promising imaging biomarkers for monitoring disease progression and effects of therapeutical interventions in clinical studies.

References

Heinen R, Groeneveld O, Barkhof F, de Bresser J, Exalto L, Kuijf H . Small vessel disease lesion type and brain atrophy: The role of co-occurring amyloid. Alzheimers Dement (Amst). 2020; 12(1):e12060. PMC: 7364862. DOI: 10.1002/dad2.12060. View

Mestre H, Kostrikov S, Mehta R, Nedergaard M . Perivascular spaces, glymphatic dysfunction, and small vessel disease. Clin Sci (Lond). 2017; 131(17):2257-2274. PMC: 5567781. DOI: 10.1042/CS20160381. View

Song S, Sun S, Ju W, Lin S, Cross A, Neufeld A . Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. Neuroimage. 2003; 20(3):1714-22. DOI: 10.1016/j.neuroimage.2003.07.005. View

Morris J, Mohs R, Rogers H, Fillenbaum G, HEYMAN A . Consortium to establish a registry for Alzheimer's disease (CERAD) clinical and neuropsychological assessment of Alzheimer's disease. Psychopharmacol Bull. 1988; 24(4):641-52. View

Smith S . Fast robust automated brain extraction. Hum Brain Mapp. 2002; 17(3):143-55. PMC: 6871816. DOI: 10.1002/hbm.10062. View

Behrens T, Berg H, Jbabdi S, Rushworth M, Woolrich M . Probabilistic diffusion tractography with multiple fibre orientations: What can we gain?. Neuroimage. 2006; 34(1):144-55. PMC: 7116582. DOI: 10.1016/j.neuroimage.2006.09.018. View

Nitkunan A, Lanfranconi S, Charlton R, Barrick T, Markus H . Brain atrophy and cerebral small vessel disease: a prospective follow-up study. Stroke. 2010; 42(1):133-8. DOI: 10.1161/STROKEAHA.110.594267. View

Fukunaga M, Li T, van Gelderen P, de Zwart J, Shmueli K, Yao B . Layer-specific variation of iron content in cerebral cortex as a source of MRI contrast. Proc Natl Acad Sci U S A. 2010; 107(8):3834-9. PMC: 2840419. DOI: 10.1073/pnas.0911177107. View

Zhang C, Wong S, van de Haar H, Staals J, Jansen J, Jeukens C . Blood-brain barrier leakage is more widespread in patients with cerebral small vessel disease. Neurology. 2016; 88(5):426-432. DOI: 10.1212/WNL.0000000000003556. View

10.

Carey D, Caprini F, Allen M, Lutti A, Weiskopf N, Rees G . Quantitative MRI provides markers of intra-, inter-regional, and age-related differences in young adult cortical microstructure. Neuroimage. 2017; 182:429-440. PMC: 6189523. DOI: 10.1016/j.neuroimage.2017.11.066. View

11.

Haacke E, Cheng N, House M, Liu Q, Neelavalli J, Ogg R . Imaging iron stores in the brain using magnetic resonance imaging. Magn Reson Imaging. 2005; 23(1):1-25. DOI: 10.1016/j.mri.2004.10.001. View

12.

Fischl B, Salat D, van der Kouwe A, Makris N, Segonne F, Quinn B . Sequence-independent segmentation of magnetic resonance images. Neuroimage. 2004; 23 Suppl 1:S69-84. DOI: 10.1016/j.neuroimage.2004.07.016. View

13.

De Guio F, Duering M, Fazekas F, de Leeuw F, Greenberg S, Pantoni L . Brain atrophy in cerebral small vessel diseases: Extent, consequences, technical limitations and perspectives: The HARNESS initiative. J Cereb Blood Flow Metab. 2019; 40(2):231-245. PMC: 7370623. DOI: 10.1177/0271678X19888967. View

14.

Song S, Sun S, Ramsbottom M, Chang C, Russell J, Cross A . Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage. 2002; 17(3):1429-36. DOI: 10.1006/nimg.2002.1267. View

15.

Wardlaw J, Smith E, Biessels G, Cordonnier C, Fazekas F, Frayne R . Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration. Lancet Neurol. 2013; 12(8):822-38. PMC: 3714437. DOI: 10.1016/S1474-4422(13)70124-8. View

16.

Edwards L, Kirilina E, Mohammadi S, Weiskopf N . Microstructural imaging of human neocortex in vivo. Neuroimage. 2018; 182:184-206. DOI: 10.1016/j.neuroimage.2018.02.055. View

17.

Jokinen H, Lipsanen J, Schmidt R, Fazekas F, Gouw A, van der Flier W . Brain atrophy accelerates cognitive decline in cerebral small vessel disease: the LADIS study. Neurology. 2012; 78(22):1785-92. DOI: 10.1212/WNL.0b013e3182583070. View

18.

Noth U, Volz S, Hattingen E, Deichmann R . An improved method for retrospective motion correction in quantitative T2* mapping. Neuroimage. 2014; 92:106-19. DOI: 10.1016/j.neuroimage.2014.01.050. View

19.

Stock B, Shrestha M, Seiler A, Foerch C, Hattingen E, Steinmetz H . Distribution of Cortical Diffusion Tensor Imaging Changes in Multiple Sclerosis. Front Physiol. 2020; 11:116. PMC: 7083109. DOI: 10.3389/fphys.2020.00116. View

20.

Liu T, Sachdev P, Lipnicki D, Jiang J, Geng G, Zhu W . Limited relationships between two-year changes in sulcal morphology and other common neuroimaging indices in the elderly. Neuroimage. 2013; 83:12-7. DOI: 10.1016/j.neuroimage.2013.06.058. View