Journal Papers

2021

Asaturyan, Hykoush, Barbara Villarini, Karen Sarao, Jeanne Chow, Onur Afacan, and Sila Kurugol. 2021. “Improving Automatic Renal Segmentation in Clinically Normal and Abnormal Paediatric DCE-MRI via Contrast Maximisation and Convolutional Networks for Computing Markers of Kidney Function”. Sensors (Basel) 21 (23). https://doi.org/10.3390/s21237942.
There is a growing demand for fast, accurate computation of clinical markers to improve renal function and anatomy assessment with a single study. However, conventional techniques have limitations leading to overestimations of kidney function or failure to provide sufficient spatial resolution to target the disease location. In contrast, the computer-aided analysis of dynamic contrast-enhanced (DCE) magnetic resonance imaging (MRI) could generate significant markers, including the glomerular filtration rate (GFR) and time-intensity curves of the cortex and medulla for determining obstruction in the urinary tract. This paper presents a dual-stage fully modular framework for automatic renal compartment segmentation in 4D DCE-MRI volumes. (1) Memory-efficient 3D deep learning is integrated to localise each kidney by harnessing residual convolutional neural networks for improved convergence; segmentation is performed by efficiently learning spatial-temporal information coupled with boundary-preserving fully convolutional dense nets. (2) Renal contextual information is enhanced via non-linear transformation to segment the cortex and medulla. The proposed framework is evaluated on a paediatric dataset containing 60 4D DCE-MRI volumes exhibiting varying conditions affecting kidney function. Our technique outperforms a state-of-the-art approach based on a GrabCut and support vector machine classifier in mean dice similarity (DSC) by 3.8% and demonstrates higher statistical stability with lower standard deviation by 12.4% and 15.7% for cortex and medulla segmentation, respectively.
Sui, Yao, Onur Afacan, Ali Gholipour, and Simon Warfield. 2021. “MRI Super-Resolution Through Generative Degradation Learning”. Med Image Comput Comput Assist Interv 12906: 430-40. https://doi.org/10.1007/978-3-030-87231-1_42.
Spatial resolution plays a critically important role in MRI for the precise delineation of the imaged tissues. Unfortunately, acquisitions with high spatial resolution require increased imaging time, which increases the potential of subject motion, and suffers from reduced signal-to-noise ratio (SNR). Super-resolution reconstruction (SRR) has recently emerged as a technique that allows for a trade-off between high spatial resolution, high SNR, and short scan duration. Deconvolution-based SRR has recently received significant interest due to the convenience of using the image space. The most critical factor to succeed in deconvolution is the accuracy of the estimated blur kernels that characterize how the image was degraded in the acquisition process. Current methods use handcrafted filters, such as Gaussian filters, to approximate the blur kernels, and have achieved promising SRR results. As the image degradation is complex and varies with different sequences and scanners, handcrafted filters, unfortunately, do not necessarily ensure the success of the deconvolution. We sought to develop a technique that enables accurately estimating blur kernels from the image data itself. We designed a deep architecture that utilizes an adversarial scheme with a generative neural network against its degradation counterparts. This design allows for the SRR tailored to an individual subject, as the training requires the scan-specific data only, i.e., it does not require auxiliary datasets of high-quality images, which are practically challenging to obtain. With this technique, we achieved high-quality brain MRI at an isotropic resolution of 0.125 cubic mm with six minutes of imaging time. Extensive experiments on both simulated low-resolution data and clinical data acquired from ten pediatric patients demonstrated that our approach achieved superior SRR results as compared to state-of-the-art deconvolution-based methods, while in parallel, at substantially reduced imaging time in comparison to direct high-resolution acquisitions.
Sui, Yao, Onur Afacan, Camilo Jaimes, Ali Gholipour, and Simon Warfield. (2021) 2021. “Gradient-Guided Isotropic MRI Reconstruction from Anisotropic Acquisitions”. IEEE Trans Comput Imaging 7: 1240-53. https://doi.org/10.1109/tci.2021.3128745.
The trade-off between image resolution, signal-to-noise ratio (SNR), and scan time in any magnetic resonance imaging (MRI) protocol is inevitable and unavoidable. Super-resolution reconstruction (SRR) has been shown effective in mitigating these factors, and thus, has become an important approach in addressing the current limitations of MRI. In this work, we developed a novel, image-based MRI SRR approach based on anisotropic acquisition schemes, which utilizes a new gradient guidance regularization method that guides the high-resolution (HR) reconstruction via a spatial gradient estimate. Further, we designed an analytical solution to propagate the spatial gradient fields from the low-resolution (LR) images to the HR image space and exploited these gradient fields over multiple scales with a dynamic update scheme for more accurate edge localization in the reconstruction. We also established a forward model of image formation and inverted it along with the proposed gradient guidance. The proposed SRR method allows subject motion between volumes and is able to incorporate various acquisition schemes where the LR images are acquired with arbitrary orientations and displacements, such as orthogonal and through-plane origin-shifted scans. We assessed our proposed approach on simulated data as well as on the data acquired on a Siemens 3T MRI scanner containing 45 MRI scans from 14 subjects. Our experimental results demonstrate that our approach achieved superior reconstructions compared to state-of-the-art methods, both in terms of local spatial smoothness and edge preservation, while, in parallel, at reduced, or at the same cost as scans delivered with direct HR acquisition.
Machado-Rivas, Fedel, Onur Afacan, Shadab Khan, Bahram Marami, Clemente Velasco-Annis, Hart Lidov, Simon Warfield, Ali Gholipour, and Camilo Jaimes. 2021. “Spatiotemporal Changes in Diffusivity and Anisotropy in Fetal Brain Tractography”. Hum Brain Mapp 42 (17): 5771-84. https://doi.org/10.1002/hbm.25653.
Population averaged diffusion atlases can be utilized to characterize complex microstructural changes with less bias than data from individual subjects. In this study, a fetal diffusion tensor imaging (DTI) atlas was used to investigate tract-based changes in anisotropy and diffusivity in vivo from 23 to 38 weeks of gestational age (GA). Healthy pregnant volunteers with typically developing fetuses were imaged at 3 T. Acquisition included structural images processed with a super-resolution algorithm and DTI images processed with a motion-tracked slice-to-volume registration algorithm. The DTI from individual subjects were used to generate 16 templates, each specific to a week of GA; this was accomplished by means of a tensor-to-tensor diffeomorphic deformable registration method integrated with kernel regression in age. Deterministic tractography was performed to outline the forceps major, forceps minor, bilateral corticospinal tracts (CST), bilateral inferior fronto-occipital fasciculus (IFOF), bilateral inferior longitudinal fasciculus (ILF), and bilateral uncinate fasciculus (UF). The mean fractional anisotropy (FA) and mean diffusivity (MD) was recorded for all tracts. For a subset of tracts (forceps major, CST, and IFOF) we manually divided the tractograms into anatomy conforming segments to evaluate within-tract changes. We found tract-specific, nonlinear, age related changes in FA and MD. Early in gestation, these trends appear to be dominated by cytoarchitectonic changes in the transient white matter fetal zones while later in gestation, trends conforming to the progression of myelination were observed. We also observed significant (local) heterogeneity in within-tract developmental trajectories for the CST, IFOF, and forceps major.
Sui, Yao, Onur Afacan, Ali Gholipour, and Simon Warfield. (2021) 2021. “Fast and High-Resolution Neonatal Brain MRI Through Super-Resolution Reconstruction From Acquisitions With Variable Slice Selection Direction”. Front Neurosci 15: 636268. https://doi.org/10.3389/fnins.2021.636268.
The brain of neonates is small in comparison to adults. Imaging at typical resolutions such as one cubic mm incurs more partial voluming artifacts in a neonate than in an adult. The interpretation and analysis of MRI of the neonatal brain benefit from a reduction in partial volume averaging that can be achieved with high spatial resolution. Unfortunately, direct acquisition of high spatial resolution MRI is slow, which increases the potential for motion artifact, and suffers from reduced signal-to-noise ratio. The purpose of this study is thus that using super-resolution reconstruction in conjunction with fast imaging protocols to construct neonatal brain MRI images at a suitable signal-to-noise ratio and with higher spatial resolution than can be practically obtained by direct Fourier encoding. We achieved high quality brain MRI at a spatial resolution of isotropic 0.4 mm with 6 min of imaging time, using super-resolution reconstruction from three short duration scans with variable directions of slice selection. Motion compensation was achieved by aligning the three short duration scans together. We applied this technique to 20 newborns and assessed the quality of the images we reconstructed. Experiments show that our approach to super-resolution reconstruction achieved considerable improvement in spatial resolution and signal-to-noise ratio, while, in parallel, substantially reduced scan times, as compared to direct high-resolution acquisitions. The experimental results demonstrate that our approach allowed for fast and high-quality neonatal brain MRI for both scientific research and clinical studies.
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.
Coll-Font, Jaume, Onur Afacan, Scott Hoge, Harsha Garg, Kumar Shashi, Bahram Marami, Ali Gholipour, Jeanne Chow, Simon Warfield, and Sila Kurugol. 2021. “Retrospective Distortion and Motion Correction for Free-Breathing DW-MRI of the Kidneys Using Dual-Echo EPI and Slice-to-Volume Registration”. J Magn Reson Imaging 53 (5): 1432-43. https://doi.org/10.1002/jmri.27473.
BACKGROUND: Diffusion-weighted MRI (DW-MRI) of the kidneys is a technique that provides information about the microstructure of renal tissue without requiring exogenous contrasts such as gadolinium, and it can be used for diagnosis in cases of renal disease and assessing response-to-therapy. However, physiological motion and large geometric distortions due to main B0 field inhomogeneities degrade the image quality, reduce the accuracy of quantitative imaging markers, and impede their subsequent clinical applicability. PURPOSE: To retrospectively correct for geometric distortion for free-breathing DW-MRI of the kidneys at 3T, in the presence of a nonstatic distortion field due to breathing and bulk motion. STUDY TYPE: Prospective. SUBJECTS: Ten healthy volunteers (ages 29-38, four females). FIELD STRENGTH/SEQUENCE: 3T; DW-MR dual-echo echo-planar imaging (EPI) sequence (10 b-values and 17 directions) and a T2 volume. ASSESSMENT: The distortion correction was evaluated subjectively (Likert scale 0-5) and numerically with cross-correlation between the DW images at b = 0 s/mm2 and a T2 volume. The intravoxel incoherent motion (IVIM) and diffusion tensor (DTI) model-fitting performance was evaluated using the root-mean-squared error (nRMSE) and the coefficient of variation (CV%) of their parameters. STATISTICAL TESTS: Statistical comparisons were done using Wilcoxon tests. RESULTS: The proposed method improved the Likert scores by 1.1 ± 0.8 (P < 0.05), the cross-correlation with the T2 reference image by 0.13 ± 0.05 (P < 0.05), and reduced the nRMSE by 0.13 ± 0.03 (P < 0.05) and 0.23 ± 0.06 (P < 0.05) for IVIM and DTI, respectively. The CV% of the IVIM parameters (slow and fast diffusion, and diffusion fraction for IVIM and mean diffusivity, and fractional anisotropy for DTI) was reduced by 2.26 ± 3.98% (P = 6.971 × 10-2 ), 11.24 ± 26.26% (P = 6.971 × 10-2 ), 4.12 ± 12.91% (P = 0.101), 3.22 ± 0.55% (P < 0.05), and 2.42 ± 1.15% (P < 0.05). DATA CONCLUSION: The results indicate that the proposed Di + MoCo method can effectively correct for time-varying geometric distortions and for misalignments due to breathing motion. Consequently, the image quality and precision of the DW-MRI model parameters improved. LEVEL OF EVIDENCE: 2 TECHNICAL EFFICACY STAGE: 1.
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.
Rollins, Caitlin, Cynthia Ortinau, Christian Stopp, Kevin Friedman, Wayne Tworetzky, Borjan Gagoski, Clemente Velasco-Annis, et al. 2021. “Regional Brain Growth Trajectories in Fetuses With Congenital Heart Disease”. Ann Neurol 89 (1): 143-57. https://doi.org/10.1002/ana.25940.
OBJECTIVE: Congenital heart disease (CHD) is associated with abnormal brain development in utero. We applied innovative fetal magnetic resonance imaging (MRI) techniques to determine whether reduced fetal cerebral substrate delivery impacts the brain globally, or in a region-specific pattern. Our novel design included two control groups, one with and the other without a family history of CHD, to explore the contribution of shared genes and/or fetal environment to brain development. METHODS: From 2014 to 2018, we enrolled 179 pregnant women into 4 groups: "HLHS/TGA" fetuses with hypoplastic left heart syndrome (HLHS) or transposition of the great arteries (TGA), diagnoses with lowest fetal cerebral substrate delivery; "CHD-other," with other CHD diagnoses; "CHD-related," healthy with a CHD family history; and "optimal control," healthy without a family history. Two MRIs were obtained between 18 and 40 weeks gestation. Random effect regression models assessed group differences in brain volumes and relationships to hemodynamic variables. RESULTS: HLHS/TGA (n = 24), CHD-other (50), and CHD-related (34) groups each had generally smaller brain volumes than the optimal controls (71). Compared with CHD-related, the HLHS/TGA group had smaller subplate (-13.3% [standard error = 4.3%], p < 0.01) and intermediate (-13.7% [4.3%], p < 0.01) zones, with a similar trend in ventricular zone (-7.1% [1.9%], p = 0.07). These volumetric reductions were associated with lower cerebral substrate delivery. INTERPRETATION: Fetuses with CHD, especially those with lowest cerebral substrate delivery, show a region-specific pattern of small brain volumes and impaired brain growth before 32 weeks gestation. The brains of fetuses with CHD were more similar to those of CHD-related than optimal controls, suggesting genetic or environmental factors also contribute. ANN NEUROL 2021;89:143-157.
Wallace, Tess, Onur Afacan, Camilo Jaimes, Joanne Rispoli, Kristina Pelkola, Monet Dugan, Tobias Kober, and Simon Warfield. 2021. “Free Induction Decay Navigator Motion Metrics for Prediction of Diagnostic Image Quality in Pediatric MRI”. Magn Reson Med 85 (6): 3169-81. https://doi.org/10.1002/mrm.28649.
PURPOSE: To investigate the ability of free induction decay navigator (FIDnav)-based motion monitoring to predict diagnostic utility and reduce the time and cost associated with acquiring diagnostically useful images in a pediatric patient cohort. METHODS: A study was carried out in 102 pediatric patients (aged 0-18 years) at 3T using a 32-channel head coil array. Subjects were scanned with an FID-navigated MPRAGE sequence and images were graded by two radiologists using a five-point scale to evaluate the impact of motion artifacts on diagnostic image quality. The correlation between image quality and four integrated FIDnav motion metrics was investigated, as well as the sensitivity and specificity of each FIDnav-based metric to detect different levels of motion corruption in the images. Potential time and cost savings were also assessed by retrospectively applying an optimal detection threshold to FIDnav motion scores. RESULTS: A total of 12% of images were rated as non-diagnostic, while a further 12% had compromised diagnostic value due to motion artifacts. FID-navigated metrics exhibited a moderately strong correlation with image grade (Spearman's rho ≥ 0.56). Integrating the cross-correlation between FIDnav signal vectors achieved the highest sensitivity and specificity for detecting non-diagnostic images, yielding total time savings of 7% across all scans. This corresponded to a financial benefit of $2080 in this study. CONCLUSIONS: Our results indicate that integrated motion metrics from FIDnavs embedded in structural MRI are a useful predictor of diagnostic image quality, which translates to substantial time and cost savings when applied to pediatric MRI examinations.