Journal Papers

2017

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.
Pier, Danielle, Ali Gholipour, Onur Afacan, Clemente Velasco-Annis, Sean Clancy, Kush Kapur, Judy Estroff, and Simon Warfield. 2016. “3D Super-Resolution Motion-Corrected MRI: Validation of Fetal Posterior Fossa Measurements”. J Neuroimaging 26 (5): 539-44. https://doi.org/10.1111/jon.12342.
PURPOSE: Current diagnosis of fetal posterior fossa anomalies by sonography and conventional MRI is limited by fetal position, motion, and by two-dimensional (2D), rather than three-dimensional (3D), representation. In this study, we aimed to validate the use of a novel magnetic resonance imaging (MRI) technique, 3D super-resolution motion-corrected MRI, to image the fetal posterior fossa. METHODS: From a database of pregnant women who received fetal MRIs at our institution, images of 49 normal fetal brains were reconstructed. Six measurements of the cerebellum, vermis, and pons were obtained for all cases on 2D conventional and 3D reconstructed MRI, and the agreement between the two methods was determined using concordance correlation coefficients. Concordance of axial and coronal measurements of the transcerebellar diameter was also assessed within each method. RESULTS: Between the two methods, the concordance of measurements was high for all six structures (P < .001), and was highest for larger structures such as the transcerebellar diameter. Within each method, agreement of axial and coronal measurements of the transcerebellar diameter was superior in 3D reconstructed MRI compared to 2D conventional MRI (P < .001). CONCLUSIONS: This comparison study validates the use of 3D super-resolution motion-corrected MRI for imaging the fetal posterior fossa, as this technique results in linear measurements that have high concordance with 2D conventional MRI measurements. Lengths of the transcerebellar diameter measured within a 3D reconstruction are more concordant between imaging planes, as they correct for fetal motion and orthogonal slice acquisition. This technique will facilitate further study of fetal abnormalities of the posterior fossa.
Akhondi-Asl, Alireza, Onur Afacan, Mukund Balasubramanian, Robert Mulkern, and Simon Warfield. 2016. “Fast Myelin Water Fraction Estimation Using 2D Multislice CPMG”. Magn Reson Med 76 (4): 1301-13. https://doi.org/10.1002/mrm.26034.
PURPOSE: T2 relaxometry based on multiexponential fitting to a single slice multiecho sequence has been the most common MRI technique for myelin water fraction mapping, where the short T2 is associated with myelin water. However, very long acquisition times and physically unrealistic models for T2 distribution are limitations of this approach. We present a novel framework for myelin imaging which substantially increases the imaging speed and myelin water fraction estimation accuracy. METHOD: We used the 2D multislice Carr-Purcell-Meiboom-Gill sequence to increase the volume coverage. To compensate for nonideal slice profiles, we numerically solved the Bloch equations for a range of T2 and B1 inhomogeneity scales to construct the bases for the estimation of the T2 distribution. We used a finite mixture of continuous parametric distributions to describe the complete T2 spectrum and used the constrained variable projection optimization algorithm to estimate myelin water fraction. To validate our model, synthetic, phantom, and in vivo brain experiments were conducted. RESULTS: Using the Bloch equations, we can model the slice profile and construct the forward model of the T2 curve. Our method estimated myelin water fraction with smaller error than the nonnegative least squares algorithm. CONCLUSIONS: The proposed framework can be used for reliable whole brain myelin imaging with a resolution of 2×2×4  mm3 in ≈17  min. Magn Reson Med 76:1301-1313, 2016. © 2015 Wiley Periodicals, Inc.
Afacan, Onur, Burak Erem, Diona P Roby, Noam Roth, Amir Roth, Sanjay P Prabhu, and Simon K Warfield. (2016) 2016. “Evaluation of Motion and Its Effect on Brain Magnetic Resonance Image Quality in Children.”. Pediatric Radiology 46 (12): 1728-35.

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.