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March 12, 2013; 80 (11) Article

Cognitive impairment in MS

Impact of white matter integrity, gray matter volume, and lesions

Hanneke E. Hulst, Martijn D. Steenwijk, Adriaan Versteeg, Petra J.W. Pouwels, Hugo Vrenken, Bernard M.J. Uitdehaag, Chris H. Polman, Jeroen J.G. Geurts, Frederik Barkhof
First published March 6, 2013, DOI: https://doi.org/10.1212/WNL.0b013e31828726cc
Hanneke E. Hulst
From the Departments of Radiology (H.E.H., M.D.S., A.V., H.V., F.B.), Anatomy and Neurosciences (H.E.H., J.J.G.G.), Physics and Medical Technology (P.J.W.P.), Neurology (B.M.J.U., C.H.P.), and Epidemiology and Biostatistics (B.M.J.U.), VU University Medical Center, Amsterdam, the Netherlands.
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Martijn D. Steenwijk
From the Departments of Radiology (H.E.H., M.D.S., A.V., H.V., F.B.), Anatomy and Neurosciences (H.E.H., J.J.G.G.), Physics and Medical Technology (P.J.W.P.), Neurology (B.M.J.U., C.H.P.), and Epidemiology and Biostatistics (B.M.J.U.), VU University Medical Center, Amsterdam, the Netherlands.
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Adriaan Versteeg
From the Departments of Radiology (H.E.H., M.D.S., A.V., H.V., F.B.), Anatomy and Neurosciences (H.E.H., J.J.G.G.), Physics and Medical Technology (P.J.W.P.), Neurology (B.M.J.U., C.H.P.), and Epidemiology and Biostatistics (B.M.J.U.), VU University Medical Center, Amsterdam, the Netherlands.
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Petra J.W. Pouwels
From the Departments of Radiology (H.E.H., M.D.S., A.V., H.V., F.B.), Anatomy and Neurosciences (H.E.H., J.J.G.G.), Physics and Medical Technology (P.J.W.P.), Neurology (B.M.J.U., C.H.P.), and Epidemiology and Biostatistics (B.M.J.U.), VU University Medical Center, Amsterdam, the Netherlands.
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Hugo Vrenken
From the Departments of Radiology (H.E.H., M.D.S., A.V., H.V., F.B.), Anatomy and Neurosciences (H.E.H., J.J.G.G.), Physics and Medical Technology (P.J.W.P.), Neurology (B.M.J.U., C.H.P.), and Epidemiology and Biostatistics (B.M.J.U.), VU University Medical Center, Amsterdam, the Netherlands.
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Bernard M.J. Uitdehaag
From the Departments of Radiology (H.E.H., M.D.S., A.V., H.V., F.B.), Anatomy and Neurosciences (H.E.H., J.J.G.G.), Physics and Medical Technology (P.J.W.P.), Neurology (B.M.J.U., C.H.P.), and Epidemiology and Biostatistics (B.M.J.U.), VU University Medical Center, Amsterdam, the Netherlands.
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Chris H. Polman
From the Departments of Radiology (H.E.H., M.D.S., A.V., H.V., F.B.), Anatomy and Neurosciences (H.E.H., J.J.G.G.), Physics and Medical Technology (P.J.W.P.), Neurology (B.M.J.U., C.H.P.), and Epidemiology and Biostatistics (B.M.J.U.), VU University Medical Center, Amsterdam, the Netherlands.
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Jeroen J.G. Geurts
From the Departments of Radiology (H.E.H., M.D.S., A.V., H.V., F.B.), Anatomy and Neurosciences (H.E.H., J.J.G.G.), Physics and Medical Technology (P.J.W.P.), Neurology (B.M.J.U., C.H.P.), and Epidemiology and Biostatistics (B.M.J.U.), VU University Medical Center, Amsterdam, the Netherlands.
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Frederik Barkhof
From the Departments of Radiology (H.E.H., M.D.S., A.V., H.V., F.B.), Anatomy and Neurosciences (H.E.H., J.J.G.G.), Physics and Medical Technology (P.J.W.P.), Neurology (B.M.J.U., C.H.P.), and Epidemiology and Biostatistics (B.M.J.U.), VU University Medical Center, Amsterdam, the Netherlands.
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Citation
Cognitive impairment in MS
Impact of white matter integrity, gray matter volume, and lesions
Hanneke E. Hulst, Martijn D. Steenwijk, Adriaan Versteeg, Petra J.W. Pouwels, Hugo Vrenken, Bernard M.J. Uitdehaag, Chris H. Polman, Jeroen J.G. Geurts, Frederik Barkhof
Neurology Mar 2013, 80 (11) 1025-1032; DOI: 10.1212/WNL.0b013e31828726cc

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Abstract

Objective: To investigate whether extent and severity of white matter (WM) damage, as measured with diffusion tensor imaging (DTI), can distinguish cognitively preserved (CP) from cognitively impaired (CI) multiple sclerosis (MS) patients.

Methods: Conventional MRI and DTI data were acquired from 55 MS patients (35 CP, 20 CI) and 30 healthy controls (HC). Voxelwise analyses were used to investigate fractional anisotropy (FA), mean diffusivity, radial diffusivity, and axial diffusivity of a WM skeleton. Regional gray matter volume was quantified and lesion probability maps were generated.

Results: Compared to HCs, decreased FA was found in 49% of the investigated WM skeleton in CP patients and in 76% of the investigated WM in CI patients. Several brain areas that showed reduced FA in both patient groups were significantly worse in CI patients, i.e, corpus callosum, superior and inferior longitudinal fasciculus, corticospinal tracts, forceps major, cingulum, and fornices. In CI patients, WM integrity damage was additionally seen in cortical brain areas, thalamus, uncinate fasciculus, brainstem, and cerebellum. These findings were independent of lesion location and regional gray matter volume, since no differences were found between the groups.

Conclusion: CI patients diverged from CP patients only on DTI metrics. WM integrity changes were found in areas that are highly relevant for cognition in the CI patients but not in the CP patients. These WM changes are therefore thought to be related to the cognitive deficits and suggest that DTI might be a powerful tool when monitoring cognitive impairment in MS.

GLOSSARY

AD=
axial diffusivity;
CI=
cognitively impaired;
CL=
cortical lesion;
CP=
cognitively preserved;
DIR=
double inversion recovery;
DTI=
diffusion tensor imaging;
EDSS=
Expanded Disability Status Scale;
FA=
fractional anisotropy;
GLM=
general linear model;
GM=
gray matter;
HC=
healthy control;
LPM=
lesion probability map;
MD=
mean diffusivity;
MPRAGE=
magnetization-prepared rapid acquisition gradient-echo;
MS=
multiple sclerosis;
NBV=
normalized brain volume;
NGMV=
normalized gray matter volume;
NWMV=
normalized white matter volume;
RD=
radial diffusivity;
TBSS=
tract-based spatial statistics;
TE=
echo time;
TI=
inversion time;
TR=
repetition time;
VBM=
voxel-based morphometry;
WM=
white matter

Footnotes

  • Go to Neurology.org for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • Supplemental data at www.neurology.org

  • Received June 26, 2012.
  • Accepted November 26, 2012.
  • © 2013 American Academy of Neurology
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