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DTI-derived indexes of brain WM correlate with cognitive performance in vascular MCI and small-vessel disease. A TBSS study

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Abstract

Indexes derived from diffusion tensor imaging (DTI) are sensitive to changes of both T2-hyperintense and normal-appearing brain white matter (WM) in elderly subjects with variable cognitive status. We investigated correlations between global cognitive performance and DTI-derived indexes along the WM tracts in the brain of patients with vascular mild cognitive impairment (MCI) and small vessel disease (SVD). Seventy-six patients with vascular MCI and SVD were assessed through Montreal Cognitive Assessment (MoCA) and Mini Mental State Examination (MMSE) test and underwent DTI examination on a 1.5 T MR scanner. We used Tract Based Spatial Statistics (TBSS) to assess voxel-wise in the entire brain the spatial distribution of the correlation between values of fractional anisotropy, mean, axial/radial diffusivity and global cognitive performance as assessed with MoCA and MMSE tests. All correlations were statistically tested with a significant p-value <0.05 using a family-wise error correction for multiple comparisons. The MoCA score significantly correlated with fractional anisotropy (positive correlation) and mean, axial and radial diffusivity (negative correlations) in WM tracts of cerebral hemispheres and corpus callosum, as well as in the intra-thalamic WM tracts and the superior cerebellar peduncle decussation in the midbrain. No significant correlations were observed for MMSE score. Global cognitive performance, as measured by the MoCA score, in patients with vascular MCI and SVD is associated with microstructural changes in WM tracts underlying intra- and inter-hemispheric cerebral, thalamo-cortical and cerebello-thalamic connections.

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Funding

The VMCI-Tuscany was funded by Tuscany Region Health Programme in the framework of the “Bando Regione Salute 2009”.

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Authors and Affiliations

  1. Quantitative and Functional Neuroradiology Research Unit, Meyer Children and Careggi Hospitals, Florence, Italy

    Mario Mascalchi & Francesca Lorenzini

  2. “Mario Serio” Department of Clinical and Experimental Biomedical Sciences, University of Florence, Florence, Italy

    Mario Mascalchi & Stefano Ciulli

  3. Neuroscience section, NEUROFARBA Department, University of Florence, Florence, Italy

    Emilia Salvadori, Anna Poggesi, Marco Pasi & Domenico Inzitari

  4. Medical Physics Section, Department of Biomedicine and Prevention, University of Rome “Tor Vergata”, Rome, Italy

    Nicola Toschi & Stefano Ciulli

  5. Department of Radiology, Athinoula A. Martinos Center for Biomedical Imaging, Boston, MA, USA

    Nicola Toschi

  6. Harvard Medical School, Boston, MA, USA

    Nicola Toschi

  7. Unit of Medical Physics, Pisa University Hospital “Azienda Ospedaliero-Universitaria Pisana”, Pisa, Italy

    Marco Giannelli

  8. Department of Electrical, Electronic, and Information Engineering “Guglielmo Marconi”, University of Bologna, Via Venezia 52, 47521, Cesena, Italy

    Stefano Orsolini & Stefano Diciotti

  9. School of Computer Science and Electronic Engineering, University of Essex, Colchester, UK

    Stefano Ciulli

  10. Neuroradiology Unit, Careggi General Hospital, Florence, Italy

    Andrea Ginestroni

  11. Department of Medicine, Surgery and Neuroscience, University of Siena, Siena, Italy

    Antonio Giorgio & Nicola De Stefano

  12. ‘L. Sacco’ Department of Biomedical and Clinical Sciences, University of Milan, Milan, Italy

    Leonardo Pantoni

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  1. Mario Mascalchi
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Correspondence to Stefano Diciotti.

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The Authors declare that they have no conflict of interest.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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Informed consent was obtained from all individual participants included in the study.

Electronic supplementary material

Supplementary Fig. 1

Between-group TBSS analysis at different anatomic levels (z coordinates in Montreal Neurological Institute standard space) identifies in yellow WM tracts showing a significant (p-value <0.05 corrected, threshold-free cluster enhancement) increase of MD in patients with vascular MCI and SVD as compared to healthy controls. They include WM tracts in the cerebral hemispheres, corpus callosum, thalami, midbrain, pons, middle cerebellar peduncles and left cerebellar hemisphere. The red-yellow overlay shows the group FLAIR-lesion map. See text for abbreviations (GIF 213 kb)

High resolution image (TIFF 4985 kb)

Supplementary Fig. 2

Between-group TBSS analysis at different anatomic levels (z coordinates in Montreal Neurological Institute space) identifies in red WM tracts showing a significant (p value <0.05 corrected, threshold-free cluster enhancement) decrease of FA in patients with vascular MCI and SVD as compared to healthy controls. They include WM tracts in the cerebral hemispheres, corpus callosum, thalami, midbrain, pons, superior and middle cerebellar peduncles and cerebellar hemispheres. The red-yellow overlay shows the group FLAIR-lesion map. See text for abbreviations (GIF 218 kb)

High resolution image (TIFF 5086 kb)

Supplementary Fig. 3

Between-group TBSS analysis at different anatomic levels (z coordinates in Montreal Neurological Institute space) identifies in green WM tracts showing a significant (p value <0.05 corrected, threshold-free cluster enhancement) increase of RD in patients with vascular MCI and SVD as compared to healthy controls. They include WM tracts in the cerebral hemispheres, corpus callosum, thalami, midbrain, pons, superior and middle cerebellar peduncles and left cerebellar hemisphere. The red-yellow overlay shows the group FLAIR-lesion map. See text for abbreviations (GIF 213 kb)

High resolution image (TIFF 5346 kb)

Supplementary Fig. 4

Between group TBSS analysis at different anatomic levels (z coordinates in Montreal Neurological Institute space) identifies in blu/light-blu WM tracts showing a significant (p value <0.05 corrected, threshold-free cluster enhancement) increase of AD in patients with vascular MCI and SVD as compared to healthy controls. They include WM tracts in the cerebral hemispheres, corpus callosum and thalami. The red-yellow overlay shows the group FLAIR-lesion map. See text for abbreviations (GIF 206 kb)

High resolution image (TIFF 4894 kb)

Supplementary Fig. 5

Within-group regression TBSS analysis at different anatomic levels (z coordinates in Montreal Neurological Institute space) in patients with vascular MCI and SVD. Red identifies WM tracts showing a significant (p value <0.05 corrected, threshold-free cluster enhancement) positive correlation of FA with MoCA scores. They include WM tracts in the cerebral hemispheres, corpus callosum, and thalami. The spatial distribution of these WM tracts is bilateral but not symmetrical. The red-yellow overlay shows the group FLAIR-lesion map. See text for abbreviations (GIF 159 kb)

High resolution image (TIFF 3538 kb)

Supplementary Fig. 6

Within-group regression TBSS analysis at different anatomic levels (z coordinates in Montreal Neurological Institute space) in patients with vascular MCI and SVD. Blue identifies the WM tracts showing a significant (p value <0.05 corrected, threshold-free cluster enhancement) negative correlation of axial diffusivity with MoCA scores. They include WM tracts in the cerebral hemispheres, corpus callosum, and left thalamus. The spatial distribution of these WM tracts is bilateral but not symmetrical. The red-yellow overlay shows the group FLAIR-lesion map. See text for abbreviations (GIF 150 kb)

High resolution image (TIFF 3988 kb)

Supplementary Fig. 7

Within-group regression TBSS analysis at different anatomic levels (z coordinates in Montreal Neurological Institute space) in patients with vascular MCI and SVD. Green identifies the WM tracts showing a significant (p value <0.05 corrected, threshold-free cluster enhancement) negative correlation of RD with MoCA scores. They include WM tracts in the cerebral hemispheres, corpus callosum, thalami and decussation of superior cerebellar peduncles in the midbrain. The spatial distribution of these WM tracts is bilateral but not symmetrical. The red-yellow overlay shows the group FLAIR-lesion map. See text for abbreviations (GIF 157 kb)

High resolution image (TIFF 3823 kb)

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Mascalchi, M., Salvadori, E., Toschi, N. et al. DTI-derived indexes of brain WM correlate with cognitive performance in vascular MCI and small-vessel disease. A TBSS study. Brain Imaging and Behavior 13, 594–602 (2019). https://doi.org/10.1007/s11682-018-9873-5

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