Ting-Yu Su1,2, Siyuan Hu2, Xiaofeng Wang3, Sophie Adler4, Konrad Wagstyl5, Zheng Ding1,2, Joon Yul Choi1, Ken Sakaie6, Ingmar Blümcke1,7, Hiroatsu Murakami1, Stephen Jones6, Imad Najm1, Dan Ma2, and Zhong Irene Wang1
1Epilepsy Center, Neurological Institute, Cleveland Clinic, Cleveland, OH, United States, 2Biomedical Engineering, Case Western Reserve University, Cleveland, OH, United States, 3Quantitative Health Science, Cleveland Clinic, Cleveland, OH, United States, 4University College London Great Ormond Street Institute for Child Health, London, United Kingdom, 5Wellcome Centre for Human Neuroimaging, London, United Kingdom, 6Imaging Institute, Cleveland Clinic, Cleveland, OH, United States, 7Neuropathology, University Hospitals Erlangen, Erlangen, Germany
Synopsis
Keywords: Epilepsy, MR Fingerprinting
Focal cortical
dysplasia (FCD) is a common
pathology in medically intractable focal epilepsy and often difficult to detect
by visual inspection of conventional MRI. We developed a framework for automatic
FCD detection using surface-based processing of conventional MRI and MR
fingerprinting data. Thirty-six patients with FCD and 48 healthy controls were included.
Improved vertex-wise and cluster-wise performance was seen when MRF and FLAIR
features were added to T1w data. A second-stage cluster-wise classifier showed
efficacy to reduce false-positive clusters. Interim results of patient-level sensitivity
of 76% and low false-positive clusters in controls supported potential clinical
applicability of the proposed framework.
Introduction
Focal cortical dysplasia (FCD) is a
common pathology in intractable focal epilepsy. Subtle FCDs can be difficult to
detect by visual inspection of conventional clinical MRI. MR fingerprinting
(MRF) is an advanced quantitative MR technique that allows for the efficient acquisition
of multiparametric tissue maps1. The quantitative nature of
MRF makes it well-suited for reflecting tissue property changes in epileptic lesions. Here, we aimed
to develop a framework for automatic FCD detection using surface-based
morphometric processing of conventional T1-weighted (T1w), fluid-attenuated
inversion recovery (FLAIR), and MRF data.Methods
Patient recruitment: We included 36 patients with medically intractable focal epilepsy and FCD (histologically
confirmed in 29, radiologically confirmed in 7) who underwent pre-surgical evaluation
at the Cleveland Clinic Epilepsy Center. 3D FLAIR images were available in
29 of the 36 patients. Forty-eight healthy controls (HCs) were also included.
MRI data acquisition: High-resolution 3D
whole-brain MRF scans (1 mm3 isotropic voxels) were performed using
a Siemens 3T Prisma scanner2. Dictionary-based
reconstruction of the MRF T1 and T2 maps was performed. T1w images
were synthesized from the MRF T1 maps, which were perfectly aligned with the T1
and T2 maps. A clinical 3D T1w whole-brain magnetization-prepared rapid
acquisition with gradient echo (MPRAGE) scan was acquired with the following
parameters: resolution = 0.5 x 0.5 x 0.9 mm3, repetition time (TR) =
1900 ms, echo time (TE) = 2.57 ms, inversion time (TI) = 1100 ms, 192 slices
and scan time = 3 min 53 sec. 3D FLAIR was acquired with TR of 5000 ms, TE of
393 ms, slice thickness 1mm, and scan time of 7 min 37 sec.
MRI data processing: Freesurfer
“recon-all” was performed on T1w MPRAGE images. The MRF T1 and T2 maps as well
as 3D FLAIR were registered to the T1w images using SyN
in Advanced Normalization Tools (ANTs)3 and sampled at 25%, 50%, and 75% of the cortical
thickness, as well as at the gray-white matter boundary and 0.5 and 1 mm into
the white matter. Lesion ROI was manually created on MRF T1w images and
registered to the same space. We utilized the Multi-center Epilepsy Lesion
Detection (MELD) pipeline4,5 to generate surface-based morphometric (SBM)
features, including thickness, mean curvature, intrinsic curvature, gray-white
contrast, sulcal depth, and asymmetry maps of these features.
Normalization
procedures with intra-subject, intra-hemispheric, and inter-subject z-scoring
using the HCs were performed. Consistent with the MELD pipeline, the neural
network models with 2 hidden layers with 40 and 10 nodes were trained using
patient and HC data. Nested leave-one-out (LOO) cross-validation was used to
assess lesion detection performance on the vertex level (Figure 1). Surfaced-level
clustering was applied to the predicted output with a threshold decided by the
training cohort. True-positive (TP) clusters were defined as the clusters that overlapped
with the lesion label, and false-positive (FP) clusters were defined as the
clusters outside of the lesion label or the existence of any positive clusters in
HCs.
To reduce FP findings, a
second-stage cluster-wise classifier was trained to suppress the FP clusters
and maintain the true-positive clusters based on the Random
Undersampling Boosting (RUSBoost) ensemble algorithm, using the mean, max,
and standard deviation values of features within each cluster as input. LOO
cross-validation was then applied to assess lesion detection performance on the
cluster level (Figure 2).Results
Figure 3 compares features from different feature sets using the uniform manifold approximation
and projection (UMAP) algorithm. The best separation of patients from HCs is
seen from MRF and FLAIR features. Figure 4 shows the area-under-curve (AUC) of receiver
operating characteristic (ROC) plots for vertex-level model performances. A mean AUC of 0.70 was seen based on T1w features. When MRF
features were added to the T1w features, the mean AUC was 0.74. When FLAIR
features were added to the T1w features, the mean AUC was 0.79. The best
performance was shown by using all features including T1w, FLAIR, and MRF, with a mean AUC of 0.8.
Figure 5A shows cluster-wise
performance following the second-stage classifier. Sensitivity was 67% based on
T1w features alone, with 8.33 FP clusters per patient. With MRF features implemented,
the sensitivity was 61%, with a reduced, 4.75 FP clusters per patient. With
FLAIR features added, the sensitivity is 69%, with 4.41
FP clusters per patient. When T1w, MRF, and FLAIR were all implemented, the
highest sensitivity was achieved at 76%, with 6.52 FP clusters per patient. Low
FP clusters in HCs were seen in all feature sets. Figure 5B shows
individual-level lesion detection for two example patients whose lesion
overlapped with prediction output (P1: mMCD; P2: FCD IIb; both histologically
confirmed).Conclusion
Our study attempted for the first time to build a surface-based morphometric
processing platform for automatic FCD detection using MRF data. The results showed
that implementing MRF as well as FLAIR features with T1w features improved vertex-level
prediction performance based on the neural network classifier. The 2nd-stage
cluster-wise classifier showed efficacy to suppress FP clusters. Interim
results of patient-level sensitivity of 76%
and low false-positive clusters in
controls supported the potential clinical applicability
of the proposed framework. Work is ongoing to continue improving sensitivity
and reducing FP clusters on the patient level.Acknowledgements
This study was supported by NIH R01 NS109439 and
R21 EB026764.References
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