Journal Papers

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Kurugol, Sila, Bahram Marami, Onur Afacan, Simon Warfield, and Ali Gholipour. (2017) 2017. “Motion-Robust Spatially Constrained Parameter Estimation in Renal Diffusion-Weighted MRI by 3D Motion Tracking and Correction of Sequential Slices”. Mol Imaging Reconstr Anal Mov Body Organs Stroke Imaging Treat (2017) 10555: 75-85. https://doi.org/10.1007/978-3-319-67564-0_8.
In this work, we introduce a novel motion-robust spatially constrained parameter estimation (MOSCOPE) technique for kidney diffusion-weighted MRI. The proposed motion compensation technique does not require a navigator, trigger, or breath-hold but only uses the intrinsic features of the acquired data to track and compensate for motion to reconstruct precise models of the renal diffusion signal. We have developed a technique for physiological motion tracking based on robust state estimation and sequential registration of diffusion sensitized slices acquired within 200ms. This allows a sampling rate of 5Hz for state estimation in motion tracking that is sufficiently faster than both respiratory and cardiac motion rates in children and adults, which range between 0.8 to 0.2Hz, and 2.5 to 1Hz, respectively. We then apply the estimated motion parameters to data from each slice and use motion-compensated data for 1) robust intra-voxel incoherent motion (IVIM) model estimation in the kidney using a spatially constrained model fitting approach, and 2) robust weighted least squares estimation of the diffusion tensor model. Experimental results, including precision of IVIM model parameters using bootstrap-sampling and in-vivo whole kidney tractography, showed significant improvement in precision and accuracy of these models using the proposed method compared to models based on the original data and volumetric registration.
Marami, Bahram, Benoit Scherrer, Onur Afacan, Simon Warfield, and Ali Gholipour. (2016) 2016. “Motion-Robust Reconstruction Based on Simultaneous Multi-Slice Registration for Diffusion-Weighted MRI of Moving Subjects”. Med Image Comput Comput Assist Interv 9902: 544-52. https://doi.org/10.1007/978-3-319-46726-9_63.
Simultaneous multi-slice (SMS) echo-planar imaging has had a huge impact on the acceleration and routine use of diffusion-weighted MRI (DWI) in neuroimaging studies in particular the human connectome project; but also holds the potential to facilitate DWI of moving subjects, as proposed by the new technique developed in this paper. We present a novel registration-based motion tracking technique that takes advantage of the multi-plane coverage of the anatomy by simultaneously acquired slices to enable robust reconstruction of neural microstructure from SMS DWI of moving subjects. Our technique constitutes three main components: 1) motion tracking and estimation using SMS registration, 2) detection and rejection of intra-slice motion, and 3) robust reconstruction. Quantitative results from 14 volunteer subject experiments and the analysis of motion-corrupted SMS DWI of 6 children indicate robust reconstruction in the presence of continuous motion and the potential to extend the use of SMS DWI in very challenging populations.
Kurugol, Sila, Moti Freiman, Onur Afacan, Liran Domachevsky, Jeannette Perez-Rossello, Michael Callahan, and Simon Warfield. (2017) 2017. “Motion-Robust Parameter Estimation in Abdominal Diffusion-Weighted MRI by Simultaneous Image Registration and Model Estimation”. Med Image Anal 39: 124-32. https://doi.org/10.1016/j.media.2017.04.006.
Quantitative body DW-MRI can detect abdominal abnormalities as well as monitor response-to-therapy for applications including cancer and inflammatory bowel disease with increased accuracy. Parameter estimates are obtained by fitting a forward model of DW-MRI signal decay to the observed data acquired with several b-values. The DW-MRI signal decay models typically used do not account for respiratory, cardiac and peristaltic motion, however, which may deteriorate the accuracy and robustness of parameter estimates. In this work, we introduce a new model of DW-MRI signal decay that explicitly accounts for motion. Specifically, we estimated motion-compensated model parameters by simultaneously solving image registration and model estimation (SIR-ME) problems utilizing the interdependence of acquired volumes along the diffusion-weighting dimension. To accomplish this, we applied the SIR-ME model to the in-vivo DW-MRI data sets of 26 Crohn's disease (CD) patients and achieved improved precision of the estimated parameters by reducing the coefficient of variation by 8%, 24% and 8% for slow diffusion (D), fast diffusion (D*) and fast diffusion fraction (f) parameters respectively, compared to parameters estimated with independent registration in normal-appearing bowel regions. Moreover, the parameters estimated with the SIR-ME model reduced the error rate in classifying normal and abnormal bowel loops to 12% for D and 10% for f parameter with a reduction in error rate by 13% and 11% for D and f parameters, respectively, compared to the error rate in classifying parameter estimates obtained with independent registration. The experiments in DW-MRI of liver in 20 subjects also showed that the SIR-ME model improved the precision of parameter estimation by reducing the coefficient of variation to 7% for D, 23% for D*, and 8% for the f parameter. Using the SIR-ME model, the coefficient of variation was reduced by 4%, 14% and 6% for D, D* and f parameters, respectively, compared to parameters estimated with independent registration. These results demonstrate that the proposed SIR-ME model improves the accuracy and robustness of quantitative body DW-MRI in characterizing tissue microstructure.
Marami, Bahram, Benoit Scherrer, Onur Afacan, Burak Erem, Simon Warfield, and Ali Gholipour. 2016. “Motion-Robust Diffusion-Weighted Brain MRI Reconstruction Through Slice-Level Registration-Based Motion Tracking”. IEEE Trans Med Imaging 35 (10): 2258-69. https://doi.org/10.1109/TMI.2016.2555244.
This work proposes a novel approach for motion-robust diffusion-weighted (DW) brain MRI reconstruction through tracking temporal head motion using slice-to-volume registration. The slice-level motion is estimated through a filtering approach that allows tracking the head motion during the scan and correcting for out-of-plane inconsistency in the acquired images. Diffusion-sensitized image slices are registered to a base volume sequentially over time in the acquisition order where an outlier-robust Kalman filter, coupled with slice-to-volume registration, estimates head motion parameters. Diffusion gradient directions are corrected for the aligned DWI slices based on the computed rotation parameters and the diffusion tensors are directly estimated from the corrected data at each voxel using weighted linear least squares. The method was evaluated in DWI scans of adult volunteers who deliberately moved during scans as well as clinical DWI of 28 neonates and children with different types of motion. Experimental results showed marked improvements in DWI reconstruction using the proposed method compared to the state-of-the-art DWI analysis based on volume-to-volume registration. This approach can be readily used to retrieve information from motion-corrupted DW imaging data.
Marami, Bahram, Benoit Scherrer, Shadab Khan, Onur Afacan, Sanjay Prabhu, Mustafa Sahin, Simon Warfield, and Ali Gholipour. 2019. “Motion-Robust Diffusion Compartment Imaging Using Simultaneous Multi-Slice Acquisition”. Magn Reson Med 81 (5): 3314-29. https://doi.org/10.1002/mrm.27613.
PURPOSE: To achieve motion-robust diffusion compartment imaging (DCI) in near continuously moving subjects based on simultaneous multi-slice, diffusion-weighted brain MRI. METHODS: Simultaneous multi-slice (SMS) acquisition enables fast and dense sampling of k- and q-space. We propose to achieve motion-robust DCI via slice-level motion correction by exploiting the rigid coupling between simultaneously acquired slices. This coupling provides 3D coverage of the anatomy that substantially constraints the slice-to-volume alignment problem. This is incorporated into an explicit model of motion dynamics that handles continuous and large subject motion in robust DCI reconstruction. RESULTS: We applied the proposed technique, called Motion Tracking based on Simultanous Multislice Registration (MT-SMR) to multi b-value SMS diffusion-weighted brain MRI of healthy volunteers and motion-corrupted scans of 20 pediatric subjects. Quantitative and qualitative evaluation based on fractional anisotropy in unidirectional fiber regions, and DCI in crossing-fiber regions show robust reconstruction in the presence of motion. CONCLUSION: The proposed approach has the potential to extend routine use of SMS DCI in very challenging populations, such as young children, newborns, and non-cooperative patients.
Kurugol, Sila, Moti Freiman, Onur Afacan, Liran Domachevsky, Jeannette Perez-Rossello, Michael Callahan, and Simon Warfield. (2015) 2015. “Motion Compensated Abdominal Diffusion Weighted MRI by Simultaneous Image Registration and Model Estimation (SIR-ME)”. Med Image Comput Comput Assist Interv 9351: 501-9. https://doi.org/10.1007/978-3-319-24574-4_60.
Non-invasive characterization of water molecule's mobility variations by quantitative analysis of diffusion-weighted MRI (DW-MRI) signal decay in the abdomen has the potential to serve as a biomarker in gastrointestinal and oncological applications. Accurate and reproducible estimation of the signal decay model parameters is challenging due to the presence of respiratory, cardiac, and peristalsis motion. Independent registration of each b-value image to the b-value=0 s/mm(2) image prior to parameter estimation might be sub-optimal because of the low SNR and contrast difference between images of varying b-value. In this work, we introduce a motion-compensated parameter estimation framework that simultaneously solves image registration and model estimation (SIR-ME) problems by utilizing the interdependence of acquired volumes along the diffusion weighting dimension. We evaluated the improvement in model parameters estimation accuracy using 16 in-vivo DW-MRI data sets of Crohn's disease patients by comparing parameter estimates obtained using the SIR-ME model to the parameter estimates obtained by fitting the signal decay model to the acquired DW-MRI images. The proposed SIR-ME model reduced the average root-mean-square error between the observed signal and the fitted model by more than 50%. Moreover, the SIR-ME model estimates discriminate between normal and abnormal bowel loops better than the standard parameter estimates.
Coll-Font, Jaume, Onur Afacan, Jeanne Chow, Richard Lee, Simon Warfield, and Sila Kurugol. 2021. “Modeling Dynamic Radial Contrast Enhanced MRI With Linear Time Invariant Systems for Motion Correction in Quantitative Assessment of Kidney Function”. Med Image Anal 67: 101880. https://doi.org/10.1016/j.media.2020.101880.
Early identification of kidney function deterioration is essential to determine which newborn patients with congenital kidney disease should be considered for surgical intervention as opposed to observation. Kidney function can be measured by fitting a tracer kinetic (TK) model onto a series of Dynamic Contrast Enhanced (DCE) MR images and estimating the filtration rate parameter from the model. Unfortunately, breathing and large bulk motion events due to patient movement in the scanner create outliers and misalignments that introduce large errors in the TK model parameter estimates even when using a motion-robust dynamic radial VIBE sequence for DCE-MR imaging. The misalignments between the series of volumes are difficult to correct using standard registration due to 1) the large differences in geometry and contrast between volumes of the dynamic sequence and 2) the requirement of fast dynamic imaging to achieve high temporal resolution and motion deteriorates image quality. These difficulties reduce the accuracy and stability of registration over the dynamic sequence. An alternative registration approach is to generate noise and motion free templates of the original data from the TK model and use them to register each volume to its contrast-matched template. However, the TK models used to characterize DCE-MRI are tissue specific, non-linear and sensitive to the same motion and sampling artifacts that hinder registration in the first place. Hence, these can only be applied to register accurately pre-segmented regions of interest, such as kidneys, and might converge to local minima under the presence of large artifacts. Here we introduce a novel linear time invariant (LTI) model to characterize DCE-MR data for different tissue types within a volume. We approximate the LTI model as a sparse sum of first order LTI functions to introduce robustness to motion and sampling artifacts. Hence, this model is well suited for registration of the entire field of view of DCE-MR data with artifacts and outliers. We incorporate this LTI model into a registration framework and evaluate it on both synthetic data and data from 20 children. For each subject, we reconstructed the sequence of DCE-MR images, detected corrupted volumes acquired during motion, aligned the sequence of volumes and recovered the corrupted volumes using the LTI model. The results show that our approach correctly aligned the volumes, provided the most stable registration in time and improved the tracer kinetic model fit.
Guler, Seyhmus, Alexander Cohen, Onur Afacan, and Simon Warfield. 2021. “Matched Neurofeedback During FMRI Differentially Activates Reward-Related Circuits in Active and Sham Groups”. J Neuroimaging 31 (5): 947-55. https://doi.org/10.1111/jon.12899.
BACKGROUND AND PURPOSE: Functional MRI neurofeedback (fMRI-nf) leverages the brain's ability to self-regulate its own activity. However, self-regulation processes engaged during fMRI-nf are incompletely understood. Here, we used matched feedback in an fMRI-nf experimental protocol to investigate whether brain processes recognize true neurofeedback signals. METHODS: We implemented an existing fMRI-nf protocol to train lateralized motor activity using a finger-tap task in conjunction with real-time feedback. Twelve healthy, right-handed, adult participants were assigned into age- and sex-matched active and sham study groups. Matched participant pairs received the same visual feedback, based on brain activity of the participant from the active group. We compared group-averaged activation maps before, during, and after neurofeedback, and analyzed changes in lateralized motor activity due to neurofeedback. RESULTS: Active and sham groups demonstrated different brain activation to the same feedback during neurofeedback. In particular, there was higher activation in visual cortex, secondary somatosensory cortex, and right inferior frontal gyrus in the active group compared to the sham group. Conversely, sham participants demonstrated higher activation in anterior cingulate cortex, left frontal pole, and posterior superior temporal gyrus. Despite differing brain activations during neurofeedback, neither group demonstrated significant improvement in lateralized motor activity from pre to postfeedback scan in the same session. We also observed no significant difference between pre and postfeedback activation maps, suggesting that no significant finger-tap related functional reorganization had occurred. CONCLUSIONS: These findings suggest that fMRI neurofeedback paradigms that monitor or incorporate activity from regions reported here would provide enhanced efficacy for research investigation and clinical intervention.
Schmaranzer, Florian, Onur Afacan, Till Lerch, Young-Jo Kim, Klaus Siebenrock, Michael Ith, Jennifer Cullmann, et al. 2021. “Magnetization-Prepared 2 Rapid Gradient-Echo MRI for B Insensitive 3D T1 Mapping of Hip Cartilage: An Experimental and Clinical Validation”. Radiology 299 (1): 150-58. https://doi.org/10.1148/radiol.2021200085.
Background Often used for T1 mapping of hip cartilage, three-dimensional (3D) dual-flip-angle (DFA) techniques are highly sensitive to flip angle variations related to B1 inhomogeneities. The authors hypothesized that 3D magnetization-prepared 2 rapid gradient-echo (MP2RAGE) MRI would help provide more accurate T1 mapping of hip cartilage at 3.0 T than would 3D DFA techniques. Purpose To compare 3D MP2RAGE MRI with 3D DFA techniques using two-dimensional (2D) inversion recovery T1 mapping as a standard of reference for hip cartilage T1 mapping in phantoms, healthy volunteers, and participants with hip pain. Materials and Methods T1 mapping at 3.0 T was performed in phantoms and in healthy volunteers using 3D MP2RAGE MRI and 3D DFA techniques with B1 field mapping for flip angle correction. Participants with hip pain prospectively (July 2019-January 2020) underwent indirect MR arthrography (with intravenous administration of 0.2 mmol/kg of gadoterate meglumine), including 3D MP2RAGE MRI. A 2D inversion recovery-based sequence served as a T1 reference in phantoms and in participants with hip pain. In healthy volunteers, cartilage T1 was compared between 3D MP2RAGE MRI and 3D DFA techniques. Paired t tests and Bland-Altman analysis were performed. Results Eleven phantoms, 10 healthy volunteers (median age, 27 years; range, 26-30 years; five men), and 20 participants with hip pain (mean age, 34 years ± 10 [standard deviation]; 17 women) were evaluated. In phantoms, T1 bias from 2D inversion recovery was lower for 3D MP2RAGE MRI than for 3D DFA techniques (mean, 3 msec ± 11 vs 253 msec ± 85; P < .001), and, unlike 3D DFA techniques, the deviation found with MP2RAGE MRI did not correlate with increasing B1 deviation. In healthy volunteers, regional cartilage T1 difference (109 msec ± 163; P = .008) was observed only for the 3D DFA technique. In participants with hip pain, the mean T1 bias of 3D MP2RAGE MRI from 2D inversion recovery was -23 msec ± 31 (P < .001). Conclusion Compared with three-dimensional (3D) dual-flip-angle techniques, 3D magnetization-prepared 2 rapid gradient-echo MRI enabled more accurate T1 mapping of hip cartilage, was less affected by B1 inhomogeneities, and showed high accuracy against a T1 reference in participants with hip pain. © RSNA, 2021.
Afacan, Onur, Edward Yang, Alexander Lin, Eduardo Coello, Melissa DiBacco, Phillip L. Pearl, Simon Warfield, and Ssadh Deficiency Investigators Consortium. 2021. “Magnetic Resonance Imaging (MRI) and Spectroscopy in Succinic Semialdehyde Dehydrogenase Deficiency”. J Child Neurol 36 (13-14): 1162-68. https://doi.org/10.1177/0883073821991295.
Succinic semialdehyde dehydrogenase (SSADH) deficiency is an autosomal recessive disorder of γ-aminobutyric acid (GABA) degradation, resulting in elevations of brain GABA and γ-hydroxybutyric acid (GHB). Previous magnetic resonance (MR) spectroscopy studies have shown increased levels of Glx in SSADH deficiency patients. Here in this work, we measure brain GABA in a large cohort of SSADH deficiency patients using advanced MR spectroscopy techniques that allow separation of GABA from overlapping metabolite peaks. We observed significant increases in GABA concentrations in SSADH deficiency patients for all 3 brain regions that were evaluated. Although GABA levels were higher in all 3 regions, each region had different patterns in terms of GABA changes with respect to age. We also report results from structural magnetic resonance imaging (MRI) of the same cohort compared with age-matched controls. We consistently observed signal hyperintensities in globus pallidus and cerebellar dentate nucleus.