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Microstructural Gray Matter Integrity Deteriorates After an Ischemic Stroke and Is Associated with Processing Speed

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Abstract

Microstructural changes after an ischemic stroke (IS) have mainly been described in white matter. Data evaluating microstructural changes in gray matter (GM) remain scarce. The aim of the present study was to evaluate the integrity of GM on longitudinal data using mean diffusivity (MD), and its influence on post-IS cognitive performances. A prospective study was conducted, including supra-tentorial IS patients without pre-stroke disability. A cognitive assessment was performed at baseline and 1 year, including a Montreal Cognitive Assessment, an Isaacs set test, and a Zazzo cancelation task (ZCT): completion time and number of errors. A 3-T brain MRI was performed at the same two time-points, including diffusion tensor imaging for the assessment of GM MD. GM volume was also computed, and changes in GM volume and GM MD were evaluated, followed by the assessment of the relationship between these structural changes and changes in cognitive performances. One hundred and four patients were included (age 68.5 ± 21.5, 38.5% female). While no GM volume loss was observed, GM MD increased between baseline and 1 year. The increase of GM MD in left fronto-temporal regions (dorsolateral prefrontal cortex, superior and medial temporal gyrus, p < 0.05, Threshold-Free Cluster Enhancement, 5000 permutations) was associated with an increase time to complete ZCT, regardless of demographic confounders, IS volume and location, GM, and white matter hyperintensity volume. GM integrity deterioration was thus associated with processing speed slowdown, and appears to be a biomarker of cognitive frailty. This broadens the knowledge of post-IS cognitive impairment mechanisms.

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Abbreviations

DTI:

Diffusion tensor imaging

DWI:

Diffusion weighted imaging

ET:

Echo time

FLAIR:

Fluid-attenuated inversion recovery

FOV:

Field of view

FSL:

FMRIB software library

FEW:

Family-wise error

GM:

Gray matter

IQCODE:

Informant Questionnaire in Cognitive Decline in the Elderly

IS:

Ischemic stroke

IST:

Isaacs set test

MD:

Mean diffusivity

MNI:

Montreal Neurological Institute

MoCA:

Montreal Cognitive Assessment

NIHSS:

National Institute of Health Stroke Score

RT:

Repetition time

SPM:

Statistical parametric mapping

TFCE:

Threshold-free cluster enhancement

TIV:

Total intracranial volume

WMH:

White matter hyperintensities

ZCT:

Zazzo’s cancelation task

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Funding

The study was supported by public grants (PHRCI-2012 and ANR-10-LABX-57 from the Translational Research and Advanced Imaging Laboratory).

Author information

Authors and Affiliations

  1. UMR-5287, CNRS, Université de Bordeaux, EPHE PSL Research University, Bordeaux, France

    Sharmila Sagnier, Gwenaëlle Catheline, Bixente Dilharreguy & Igor Sibon

  2. Unité Neuro-Vasculaire, CHU de Bordeaux, Bordeaux, France

    Sharmila Sagnier, Mathilde Poli, Sabrina Debruxelles, Pauline Renou, Stéphane Olindo, François Rouanet & Igor Sibon

  3. INCIA Université, Bordeaux 2, 146 rue Léo Saignat Zone Nord, Bâtiment 2A, 2e étage, 33076, Bordeaux, France

    Sharmila Sagnier

  4. Neuroradiologie, CHU de Bordeaux, Bordeaux, France

    Pierre-Antoine Linck, Antoine Bigourdan, Vincent Dousset & Thomas Tourdias

  5. UMR 5800, Univ. Bordeaux, CNRS, INP, LaBRI, 33400, Talence, Bordeaux, France

    Pierrick Coupé

  6. Beth Israel Deaconess Medical Center, Harvard University, Boston, USA

    Fanny Munsch

  7. INSERM-U862, Neurocentre Magendie, Bordeaux, France

    Vincent Dousset & Thomas Tourdias

Authors
  1. Sharmila Sagnier
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  2. Gwenaëlle Catheline
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  3. Bixente Dilharreguy
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  7. Antoine Bigourdan
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  8. Mathilde Poli
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  9. Sabrina Debruxelles
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  10. Pauline Renou
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  11. Stéphane Olindo
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  12. François Rouanet
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  13. Vincent Dousset
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  14. Thomas Tourdias
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  15. Igor Sibon
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Corresponding author

Correspondence to Sharmila Sagnier.

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Ethics Approval

This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the Regional French Human Protection Committee (CPP 2012/19 2012-A00190-43).

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The authors declare no competing interests.

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Sagnier, S., Catheline, G., Dilharreguy, B. et al. Microstructural Gray Matter Integrity Deteriorates After an Ischemic Stroke and Is Associated with Processing Speed. Transl. Stroke Res. 14, 185–192 (2023). https://doi.org/10.1007/s12975-022-01020-9

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  • DOI: https://doi.org/10.1007/s12975-022-01020-9

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