Journal Papers

2017

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.
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, Seyed Sadegh Mohseni Salehi, Onur Afacan, Benoit Scherrer, Caitlin Rollins, Edward Yang, Judy Estroff, Simon Warfield, and Ali Gholipour. 2017. “Temporal Slice Registration and Robust Diffusion-Tensor Reconstruction for Improved Fetal Brain Structural Connectivity Analysis”. Neuroimage 156: 475-88. https://doi.org/10.1016/j.neuroimage.2017.04.033.
Diffusion weighted magnetic resonance imaging, or DWI, is one of the most promising tools for the analysis of neural microstructure and the structural connectome of the human brain. The application of DWI to map early development of the human connectome in-utero, however, is challenged by intermittent fetal and maternal motion that disrupts the spatial correspondence of data acquired in the relatively long DWI acquisitions. Fetuses move continuously during DWI scans. Reliable and accurate analysis of the fetal brain structural connectome requires careful compensation of motion effects and robust reconstruction to avoid introducing bias based on the degree of fetal motion. In this paper we introduce a novel robust algorithm to reconstruct in-vivo diffusion-tensor MRI (DTI) of the moving fetal brain and show its effect on structural connectivity analysis. The proposed algorithm involves multiple steps of image registration incorporating a dynamic registration-based motion tracking algorithm to restore the spatial correspondence of DWI data at the slice level and reconstruct DTI of the fetal brain in the standard (atlas) coordinate space. A weighted linear least squares approach is adapted to remove the effect of intra-slice motion and reconstruct DTI from motion-corrected data. The proposed algorithm was tested on data obtained from 21 healthy fetuses scanned in-utero at 22-38 weeks gestation. Significantly higher fractional anisotropy values in fiber-rich regions, and the analysis of whole-brain tractography and group structural connectivity, showed the efficacy of the proposed method compared to the analyses based on original data and previously proposed methods. The results of this study show that slice-level motion correction and robust reconstruction is necessary for reliable in-vivo structural connectivity analysis of the fetal brain. Connectivity analysis based on graph theoretic measures show high degree of modularity and clustering, and short average characteristic path lengths indicative of small-worldness property of the fetal brain network. These findings comply with previous findings in newborns and a recent study on fetuses. The proposed algorithm can provide valuable information from DWI of the fetal brain not available in the assessment of the original 2D slices and may be used to more reliably study the developing fetal brain connectome.
Gholipour, Ali, Caitlin Rollins, Clemente Velasco-Annis, Abdelhakim Ouaalam, Alireza Akhondi-Asl, Onur Afacan, Cynthia Ortinau, et al. 2017. “A Normative Spatiotemporal MRI Atlas of the Fetal Brain for Automatic Segmentation and Analysis of Early Brain Growth”. Sci Rep 7 (1): 476. https://doi.org/10.1038/s41598-017-00525-w.
Longitudinal characterization of early brain growth in-utero has been limited by a number of challenges in fetal imaging, the rapid change in size, shape and volume of the developing brain, and the consequent lack of suitable algorithms for fetal brain image analysis. There is a need for an improved digital brain atlas of the spatiotemporal maturation of the fetal brain extending over the key developmental periods. We have developed an algorithm for construction of an unbiased four-dimensional atlas of the developing fetal brain by integrating symmetric diffeomorphic deformable registration in space with kernel regression in age. We applied this new algorithm to construct a spatiotemporal atlas from MRI of 81 normal fetuses scanned between 19 and 39 weeks of gestation and labeled the structures of the developing brain. We evaluated the use of this atlas and additional individual fetal brain MRI atlases for completely automatic multi-atlas segmentation of fetal brain MRI. The atlas is available online as a reference for anatomy and for registration and segmentation, to aid in connectivity analysis, and for groupwise and longitudinal analysis of early brain growth.
Hesper, Tobias, Evgeny Bulat, Sarah Bixby, Alireza Akhondi-Asl, Onur Afacan, Patricia Miller, Garrett Bowen, Simon Warfield, and Young-Jo Kim. (2017) 2017. “Both 3-T DGEMRIC and Acetabular-Femoral T2 Difference May Detect Cartilage Damage at the Chondrolabral Junction”. Clin Orthop Relat Res 475 (4): 1058-65. https://doi.org/10.1007/s11999-016-5136-1.
BACKGROUND: In addition to case reports of gadolinium-related toxicities, there are increasing theoretical concerns about the use of gadolinium for MR imaging. As a result, there is increasing interest in noncontrast imaging techniques for biochemical cartilage assessment. Among them, T2 mapping holds promise because of its simplicity, but its biophysical interpretation has been controversial. QUESTIONS/PURPOSES: We sought to determine whether (1) 3-T delayed gadolinium-enhanced MRI of cartilage (dGEMRIC) and T2 mapping are both capable of detecting cartilage damage at the chondrolabral junction in patients with femoroacetabular impingement (FAI); and (2) whether there is a correlation between these two techniques for acetabular and femoral head cartilage assessment. METHODS: Thirty-one patients with hip-related symptoms resulting from FAI underwent a preoperative 3-T MRI of their hip that included dGEMRIC and T2 mapping (symptomatic group, 16 women, 15 men; mean age, 27 ± 8 years). Ten volunteers with no symptoms according to the WOMAC served as a control (asymptomatic group, seven women, three men; mean age, 28 ± 3 years). After morphologic cartilage assessment, acetabular and femoral head cartilages were graded according to the modified Outerbridge grading criteria. In the midsagittal plane, single-observer analyses of precontrast T1 values (volunteers), the dGEMRIC index (T1Gd, patients), and T2 mapping values (everyone) were compared in acetabular and corresponding femoral head cartilage at the chondrolabral junction of each hip by region-of-interest analysis. RESULTS: In the symptomatic group, T1Gd and T2 values were lower in the acetabular cartilage compared with corresponding femoral head cartilage (T1Gd: 515 ± 165 ms versus 650 ± 191 ms, p < 0.001; T2: 39 ± 8 ms versus 46 ± 10 ms, p < 0.001). In contrast, the asymptomatic group demonstrated no differences in T1 and T2 values for the acetabular and femoral cartilages with the numbers available (T1: 861 ± 130 ms versus 860 ± 182 ms, p = 0.98; T2: 43 ± 7 ms versus 42 ± 6 ms, p = 0.73). No correlation with the numbers available was noted between the modified Outerbridge grade and T1, T1Gd, or T2 as well as between T2 and either T1 or T1Gd. CONCLUSIONS: Without the need for contrast media application, T2 mapping may be a viable alternative to dGEMRIC when assessing hip cartilage at the chondrolabral junction. However, acquisition-related phenomena as well as regional variations in the microstructure of hip cartilage necessitate an internal femoral head cartilage control when interpreting these results. LEVEL OF EVIDENCE: Level IV, diagnostic study.

2016

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.
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.
Afacan, Onur, Burak Erem, Diona Roby, Noam Roth, Amir Roth, Sanjay Prabhu, and Simon Warfield. (2016) 2016. “Evaluation of Motion and Its Effect on Brain Magnetic Resonance Image Quality in Children”. Pediatr Radiol 46 (12): 1728-35. https://doi.org/10.1007/s00247-016-3677-9.
BACKGROUND: Motion artifacts pose significant problems for the acquisition of MR images in pediatric populations. OBJECTIVE: To evaluate temporal motion metrics in MRI scanners and their effect on image quality in pediatric populations in neuroimaging studies. MATERIALS AND METHODS: We report results from a large pediatric brain imaging study that shows the effect of motion on MRI quality. We measured motion metrics in 82 pediatric patients, mean age 13.4 years, in a T1-weighted brain MRI scan. As a result of technical difficulties, 5 scans were not included in the subsequent analyses. A radiologist graded the images using a 4-point scale ranging from clinically non-diagnostic because of motion artifacts to no motion artifacts. We used these grades to correlate motion parameters such as maximum motion, mean displacement from a reference point, and motion-free time with image quality. RESULTS: Our results show that both motion-free time (as a ratio of total scan time) and average displacement from a position at a fixed time (when the center of k-space was acquired) were highly correlated with image quality, whereas maximum displacement was not as good a predictor. Among the 77 patients whose motion was measured successfully, 17 had average displacements of greater than 0.5 mm, and 11 of those (14.3%) resulted in non-diagnostic images. Similarly, 14 patients (18.2%) had less than 90% motion-free time, which also resulted in non-diagnostic images. CONCLUSION: We report results from a large pediatric study to show how children and young adults move in the MRI scanner and the effect that this motion has on image quality. The results will help the motion-correction community in better understanding motion patterns in pediatric populations and how these patterns affect MR image quality.
Afacan, Onur, Ali Gholipour, Robert Mulkern, Carol Barnewolt, Judy Estroff, Susan Connolly, Richard Parad, Sigrid Bairdain, and Simon Warfield. 2016. “Fetal Lung Apparent Diffusion Coefficient Measurement Using Diffusion-Weighted MRI at 3 Tesla: Correlation With Gestational Age”. J Magn Reson Imaging 44 (6): 1650-55. https://doi.org/10.1002/jmri.25294.
PURPOSE: To evaluate the feasibility of using diffusion-weighted magnetic resonance imaging (DW-MRI) to assess the fetal lung apparent diffusion coefficient (ADC) at 3 Tesla (T). MATERIALS AND METHODS: Seventy-one pregnant women (32 second trimester, 39 third trimester) were scanned with a twice-refocused Echo-planar diffusion-weighted imaging sequence with 6 different b-values in 3 orthogonal diffusion orientations at 3T. After each scan, a region-of-interest (ROI) mask was drawn to select a region in the fetal lung and an automated robust maximum likelihood estimation algorithm was used to compute the ADC parameter. The amount of motion in each scan was visually rated. RESULTS: When scans with unacceptable levels of motion were eliminated, the lung ADC values showed a strong association with gestational age (P < 0.01), increasing dramatically between 16 and 27 weeks and then achieving a plateau around 27 weeks. CONCLUSION: We show that to get reliable estimates of ADC values of fetal lungs, a multiple b-value acquisition, where motion is either corrected or considered, can be performed. J. Magn. Reson. Imaging 2016;44:1650-1655.
Kurugol, Sila, Moti Freiman, Onur Afacan, Jeannette Perez-Rossello, Michael Callahan, and Simon Warfield. 2016. “Spatially-Constrained Probability Distribution Model of Incoherent Motion (SPIM) for Abdominal Diffusion-Weighted MRI”. Med Image Anal 32: 173-83. https://doi.org/10.1016/j.media.2016.03.009.
Quantitative diffusion-weighted MR imaging (DW-MRI) of the body enables characterization of the tissue microenvironment by measuring variations in the mobility of water molecules. The diffusion signal decay model parameters are increasingly used to evaluate various diseases of abdominal organs such as the liver and spleen. However, previous signal decay models (i.e., mono-exponential, bi-exponential intra-voxel incoherent motion (IVIM) and stretched exponential models) only provide insight into the average of the distribution of the signal decay rather than explicitly describe the entire range of diffusion scales. In this work, we propose a probability distribution model of incoherent motion that uses a mixture of Gamma distributions to fully characterize the multi-scale nature of diffusion within a voxel. Further, we improve the robustness of the distribution parameter estimates by integrating spatial homogeneity prior into the probability distribution model of incoherent motion (SPIM) and by using the fusion bootstrap solver (FBM) to estimate the model parameters. We evaluated the improvement in quantitative DW-MRI analysis achieved with the SPIM model in terms of accuracy, precision and reproducibility of parameter estimation in both simulated data and in 68 abdominal in-vivo DW-MRIs. Our results show that the SPIM model not only substantially reduced parameter estimation errors by up to 26%; it also significantly improved the robustness of the parameter estimates (paired Student's t-test, p < 0.0001) by reducing the coefficient of variation (CV) of estimated parameters compared to those produced by previous models. In addition, the SPIM model improves the parameter estimates reproducibility for both intra- (up to 47%) and inter-session (up to 30%) estimates compared to those generated by previous models. Thus, the SPIM model has the potential to improve accuracy, precision and robustness of quantitative abdominal DW-MRI analysis for clinical applications.