Rozanna Meijboom1,2, Susana Muñoz Maniega1,2, Maria Valdés Hernández1,2, Nathalie Royle1, Zoe Morris1, John Starr3, Mark Bastin1,2, Ian Deary4, and Joanna Wardlaw1,2
1Centre for Clinical Brain Sciences, University of Edinburgh, Edinburgh, United Kingdom, 2UK Dementia Research Institute, University of Edinburgh, Edinburgh, United Kingdom, 3Alzheimer Scotland Dementia Research Centre, University of Edinburgh, Edinburgh, United Kingdom, 4Department of Psychology, University of Edinburgh, Edinburgh, United Kingdom
Synopsis
White matter hyperintensities (WMH) are common in older brains.
We analyzed how WMH affect white matter (WM) tracts and particularly their
normal-appearing WM (NAWM). We used MRI of 52 participants (72.2±0.7y) to quantify diffusion parameters of WMH-affected tracts.
The intersections of tracts with WMH were identified and volumes
quantified. Diffusion parameters
were measured for tract-WMH, tract-NAWM, and for tract-NAWM at different
distances from the tract-WMH edge, and from the edge of nearby—non-intersecting—WMH.
Tract-NAWM showed a gradient of diffusion abnormalities away from tract-WMH,
and nearby-WMH. Tract-WMH diffusion, and either tract-WMH volume or whole-brain
WMH load, predicted tract-NAWM diffusion.
Introduction
White matter hyperintensities (WMH) are common
in older brains and may contribute to age-related cognitive decline. The presence
of WMH within white matter (WM) tracts indicate underlying microstructural
changes that could ultimately lead to cortical disconnection. Whole-brain
studies of WMH also observed tissue damage in nearby normal-appearing-white-matter
(NAWM)1,2, but no study has looked at the spread of damage specifically
within tracts. Also, it is not established whether NAWM is affected only by the
WMH intersecting the tracts (tract-WMH), or also by nearby WMH (nearby-WMH)
that do not intersect. Here, we use a subsample of the Lothian Birth Cohort
19363 (LBC1936) to investigate microstructural
changes of WMH-affected tracts by measuring diffusion parameters in tract-WMH, tract-NAWM,
and tract-NAWM at several distances from the WMH (Fig. 1). Methods
Fifty-two participants (27 male; age 72.2±0.7 years) were selected from the
LBC1936 study3 to represent all levels of WMH burden (Fazekas). All
patients received T1, T2, T2*-weighted imaging, FLAIR and diffusion MRI (64
directions; b= 1000 s/mm2) scans at 1.5T (GE). WMH and NAWM were
segmented4 and registered to diffusion space. Fractional anisotropy (FA)
and mean diffusivity (MD) maps were calculated from diffusion data (FSL v4.1). Eighteen
WM tracts were reconstructed using automated tractography (Tracula5,
Freesurfer v5.3) and intersected with WMH and NAWM to establish tract-WMH and
tract-NAWM. We calculated volumes and weighted-mean FA and MD for each. Additionally,
FA and MD were measured for tract-NAWM spatial contours at 2mm, 4mm, 6mm, 8mm
and 10mm around the tract-WMH and nearby-WMH (Fig.2). For each tract and for
all tracts combined (averaged for each participant), FA and MD were compared between
tract-WMH and tract-NAWM; between tract-WMH and tract-NAWM at 2mm, between 2mm
and 4mm, etc (SPSS21.0).
We also compared the parameters from tract-WMH spatial contours with the contours established for nearby-WMH.
Additionally, we investigated predictive effects of tract-WMH % volume, Fazekas
and tract-WMH diffusion on tract-NAWM diffusion.Results
The tracts affected by WMH to a larger extent were the
forceps major, superior longitudinal fasciculi and the anterior thalamic
radiations, while the lowest % overlap with WMH were in the dorsal cingula and
the forceps minor. The expected patterns of decreased FA and increased MD were
generally observed in tract-WMH in comparison with tract-NAWM (in 89% of
individual tracts for FA and 94% for MD). Additionally, combining all tracts,
tract-NAWM FA was predicted by tract-WMH FA (Bstd= 0.337, t(49)=3.396, p<0.002)
and tract-WMH % volume (Bstd=-0.580, t(49)=-5.842, p<0.001) with no
significant effect of Fazekas, age or gender. Tract-NAMW MD was predicted by
tract-WMH MD (Bstd=.472, t(49)= 4.148, p<0.006) and Fazekas (Bstd=0.327,
t(49)=2.875, p<0.001), with no significant effect of tract-WMH % volume, age
or gender. We found
that diffusion abnormalities decreased with distance from the tract-WMH, with
lower FA and higher MD in tract-WMH compared with tract-NAWM at 2mm, in 2mm
tract-NAWM compared with 4mm, and for MD only in 4mm tract-NAWM compared with
6mm (Fig.3). This was similarly observed in 61% of individual tracts for FA and
83% for MD. A similar distance pattern was observed for nearby-WMH contours,
with generally slightly more abnormal diffusion values than in tract-WMH
contours.
Discussion
Tract-WMH showed microstructural changes
suggestive of tissue damage. These were, to a lesser extent, also observed in
tract-NAWM which became less pronounced along the tract and further away from
the WMH. FA was predicted by %WMH overlap with the tract, while MD was predicted
by whole-brain WMH burden. This suggests that tract-NAWM changes in water
content and mobility, reflected by MD, are related to diffuse WM damage
typically seen in the ageing brain, whereas tract-NAWM changes in myelin and
axonal packing, reflected by FA, are more related to tract-specific WM damage. The changes in tract-NAWM
diffusion with distance displayed similar patterns for both tract-WMH and
nearby-WMH, with a comparable generally gradual decrease of abnormalities as
distance increased. This may suggest that age-related WM damage does not
propagate predominantly along tract axons, as expected from ischemic damage,
but also propagates via different mechanisms.Conclusion
Overall, these results suggest that tract-NAWM is
also affected by the pathological process underlying WMH. The changes in
tract-NAWM may predate lesion progression, and may play an important role in
cognitive ageing. Our future
efforts are aimed at elucidating lesion progression, and the relationship between
microstructural changes of tract-WMH and tract-NAWM, and cognitive functioning,
at older ages. Acknowledgements
No acknowledgement found.References
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