Matteo Mancini1,2, Sjoerd Vos1,2,3, Vejay Vakharia2,4, Rachel Sparks1,2, Karin Trimmel4, Gavin P. Winston3,4,5, John Duncan2,3,4, and Sebastian Ourselin1,2,4,6
1Translational Imaging Group, University College London, London, United Kingdom, 2Wellcome EPSRC Centre for Interventional and Surgical Sciences (WEISS), University College London, London, United Kingdom, 3Epilepsy Society MRI Unit, Chalfont St Peter, United Kingdom, 4Department of Clinical and Experimental Epilepsy, University College London, London, United Kingdom, 5Neuroimaging of Epilepsy Laboratory, Montreal Neurological Institute, McGill University, Montreal, Canada, 6Dementia Research Centre, University College London, London, United Kingdom
Synopsis
Diffusion MRI and tractography hold great
potential for surgery planning, but fiber tract reconstruction requires an
expert rater. In this work, we set up an automated reconstruction pipeline
based on anatomical criteria that does not require manual intervention and we
validated it on epilepsy patients with specific focus on language-related
bundles. We first compared the results with the ones obtained from human raters
and then further validated them using task fMRI. The fiber tracts reconstructed
from the pipeline were in line with the agreement between different human
raters and showed good overlap with function.
Introduction
The use of diffusion-weighted
imaging (DWI) and tractography in surgery planning is still limited, despite
their potential to inform the surgeons on function-related white matter bundles
to avoid during resections1. Although several semi-automated
approaches have been proposed in the last years2,3, they all require
expert manual segmentation of the tracts. Additionally, validation of such
methods has been mostly on healthy subjects with scarce attention to function-related
aspects. Here we propose an automated parcellation-based approach that relies
on anatomically constrained tractography (ACT) and validate its application on reconstructing
language-related tracts of temporal lobe epilepsy (TLE) patients.Methods
The dataset consists
of thirty TLE patients (mean age(SD): 36.87(11.41); m/f: 12/18; affected lobe:
14 left/16 right). These patients were scheduled for resection and underwent
the MRI protocol as part of the clinical procedures, that included: T1-weighted
sequence (MPRAGE) and multi-shell DWI (2mm isotropic resolution, gradient
directions: 11, 8, 32, and 64 at b-values: 0, 300, 700, and 2500 s/mm2, single
b=0-image with reverse phase-encoding). The patients also underwent task-based
fMRI (gradient-echo planar T2*-weighted images with TE/TR = 22/2500 ms, 50
contiguous 2.4mm slices (0.1mm gap) with a 24 cm field of view, 64×64 matrix,
in-plane pixel size of 3.75×3.75 mm). Three tasks were employed: auditory
naming (AN), picture naming (PN) and verbal fluency (VF)4,5. The
acquired data were processed using a tailored pipeline assembled with NiPype
(fig.1). Briefly, T1-weighted data were processed using geodesic-information
flow (GIF) for tissue segmentation and parcellation6. Then,
segmentation and parcellation data were rigidly co-registered in the diffusion
space. DWI data were corrected for signal drift, geometric distortions and
eddy-current induced distortions. An orientation distribution function was
estimated using multi-tissue constrained spherical deconvolution7.
Fiber tracts were reconstructed probabilistically with MRTrix3 using iFOD2 and ACT:
focusing on the bundles related to language, we reconstructed the arcuate
fasciculus (AF), inferior fronto-occipital fasciculus (IFOF), inferior
longitudinal fasciculus (ILF), and uncinate fasciculus (UF) bilaterally. Using
GIF parcellation, the seeding regions as well as the inclusion and exclusion
areas were defined based on anatomical criteria8. 5000 streamlines
were estimated randomly placing the seeds at the white matter/grey matter
interface. To exclude spurious streamlines, a cluster-based approach based on QuickBundles
was used9, discarding streamlines with either direction, distance or
position of the centre of gravity out of the main clusters. We adopted a
two-fold validation approach: as a first validation, for ten of the thirty
subjects (5 RTLE/5 LTLE) the fiber tracts of the left hemisphere were manually
segmented by two experts, following established criteria10. Using
the Cohen’s kappa and the Jaccard index10,2, we quantified agreement
and overlap between the automated procedure and the manual ones and compared it
to the inter-rater agreement. As a further validation, we used the maximal
activation points in the language-dominant hemisphere obtained from the fMRI
tasks as seeds for probabilistic tractography for all the subjects. Using the
mentioned scores, we quantified the overlap between the language-related fiber
tracts and the ones obtained using fMRI seeding.Results
Figure 2 shows the tracts for a sample subject on the left hemisphere,
while figure 3 shows the left AF for the same subject as reconstructed from the
automated procedure and the human raters. The kappa showed in general moderate
agreement between the automated reconstructed tracts and the expert ones, with
AF getting substantial agreement with one rater (fig.4). It must be noticed
that in all the comparisons the agreement was greater or comparable to the
inter-rater agreement. The Jaccard index showed similar results. The overlap
between fMRI seeded and automated reconstructed tracts highlighted mainly good overlap
between AF and all the tasks and scarce overlap with UF (fig.5).Discussion
The automated procedure reconstructed good
quality tracts with few spurious streamlines. Compared to the human experts,
the agreement differed between the raters, but showed higher values than the
inter-rater comparison, indicating it finds a good middle ground between different human raters.
When compared to previous work2, the overlap in terms of Jaccard
index showed comparable or higher values than the ones reported in Garyfallidis
and colleagues2. In terms of functional overlap, the VF task
activated the inferior and middle frontal gyrus5, and we
consistently observed a predominant overlap with AF. PN and AN tasks
respectively activated superior and middle temporal gyri4, and as a
consequence the related tracts overlap in different ways with IFOF, ILF and AF.
The UF was not involved in the tasks and accordingly it scarcely overlaps.Conclusions
We proposed an anatomy-constrained method for reconstructing fiber tracts
that does not require an expert eye. We observed results comparable to human
ones and functionally meaningful.Acknowledgements
We are grateful to the Wolfson Foundation and Epilepsy Society for supporting the Epilepsy Society MRI
scanner. This work was supported by the Wellcome/EPSRC (203145Z/16/Z), NIHR BRC UCLH/UCL High Impact
Initiative, MRC (MR/M00841X/1), and Health Innovation Challenge Fund (WT106882).
KT was supported by a 1-year fellowship each by the European Academy of Neurology and the Austrian Society of Neurology.
References
1. Essayed WI, Zhang F, Unadkat P, et al. White matter tractography for neurosurgical planning: A topography-based review of the current state of the art. NeuroImage Clinical. 2017;15:659-72.
2. Garyfallidis E, Cote MA, Rheault F, et al. Recognition of white matter bundles using local and global streamline-based registration and clustering. NeuroImage. 2017.
3. Wassermann D, Makris N, Rathi Y, et al. The white matter query language: a novel approach for describing human white matter anatomy. Brain structure & function. 2016;221(9):4705-21.
4. Gonzalvez GG, Trimmel K, Haag A, et al. Activations in temporal areas using visual and auditory naming stimuli: A language fMRI study in temporal lobe epilepsy. Epilepsy research. 2016;128:102-12.
5. Bonelli SB, Powell R, Thompson PJ, et al. Hippocampal activation correlates with visual confrontation naming: fMRI findings in controls and patients with temporal lobe epilepsy. Epilepsy research. 2011;95(3):246-54.
6. Cardoso MJ, Modat M, Wolz R, et al. Geodesic Information Flows: Spatially-Variant Graphs and Their Application to Segmentation and Fusion. IEEE transactions on medical imaging. 2015;34(9):1976-88.
7. Jeurissen B, Tournier JD, Dhollander T, et al. Multi-tissue constrained spherical deconvolution for improved analysis of multi-shell diffusion MRI data. NeuroImage. 2014;103:411-26.
8. Catani M, Thiebaut de Schotten M. A diffusion tensor imaging tractography atlas for virtual in vivo dissections. Cortex; a journal devoted to the study of the nervous system and behavior. 2008;44(8):1105-32.
9. Garyfallidis E, Brett M, Correia MM, et al. QuickBundles, a Method for Tractography Simplification. Frontiers in neuroscience. 2012;6:175.
10. Wakana S, Caprihan A, Panzenboeck MM, et al. Reproducibility of quantitative tractography methods applied to cerebral white matter. NeuroImage. 2007;36(3):630-44.