Journal Papers

2022

Koçanaoğullari, Aziz, Cemre Ariyurek, Onur Afacan, and Sila Kurugol. (2022) 2022. “Learning the Regularization in DCE-MR Image Reconstruction for Functional Imaging of Kidneys”. IEEE Access 10: 4102-11. https://doi.org/10.1109/access.2021.3139854.
Kidney DCE-MRI aims at both qualitative assessment of kidney anatomy and quantitative assessment of kidney function by estimating the tracer kinetic (TK) model parameters. Accurate estimation of TK model parameters requires an accurate measurement of the arterial input function (AIF) with high temporal resolution. Accelerated imaging is used to achieve high temporal resolution, which yields under-sampling artifacts in the reconstructed images. Compressed sensing (CS) methods offer a variety of reconstruction options. Most commonly, sparsity of temporal differences is encouraged for regularization to reduce artifacts. Increasing regularization in CS methods removes the ambient artifacts but also over-smooths the signal temporally which reduces the parameter estimation accuracy. In this work, we propose a single image trained deep neural network to reduce MRI under-sampling artifacts without reducing the accuracy of functional imaging markers. Instead of regularizing with a penalty term in optimization, we promote regularization by generating images from a lower dimensional representation. In this manuscript we motivate and explain the lower dimensional input design. We compare our approach to CS reconstructions with multiple regularization weights. Proposed approach results in kidney biomarkers that are highly correlated with the ground truth markers estimated using the CS reconstruction which was optimized for functional analysis. At the same time, the proposed approach reduces the artifacts in the reconstructed images.
Machado-Rivas, Fedel, Camilo Jaimes, Benoit Scherrer, Leslie Benson, Mark Gorman, Simon Warfield, and Onur Afacan. 2022. “Evaluation of White Matter Microstructure in Pediatric Onset Multiple Sclerosis With Diffusion Compartment Imaging”. J Neuroimaging. https://doi.org/10.1111/jon.13038.
BACKGROUND AND PURPOSE: Pediatric-onset multiple sclerosis (POMS) shows earlier axonal involvement and greater axonal loss than in adults. We aim to characterize the white matter (WM) microstructural changes in POMS using a diffusion compartment imaging (DCI) model and compare it to standard diffusion tensor imaging (DTI). METHODS: Eleven patients (2 males, mean age 18.8 ± 3.9 years) with a diagnosis of relapsing and remitting POMS (mean age at disease onset 13.8 ± 2.9 years, mean duration 5.1 ± 1.9 years) and healthy controls (8 males, mean age 26.4 ± 6.5 years) were recruited and imaged at 3 T. A 90-gradient set Cube and Sphere acquisition and a novel DCI model known as DIstribution of Anisotropic MicrOstructural eNvironments with Diffusion-weighted imaging (DIAMOND) were used to calculate a single anisotropic compartment, an isotropic compartment, and a free diffusion compartment. Lesions and contralateral normal-appearing white matter (NAWM) in patients and whole brain WM for controls were labeled. RESULTS: Eleven patients and 11 controls were recruited. When comparing lesions and contralateral NAWM in patients using DCI, compartmental axial diffusivity, radial diffusivity (cRD), and mean diffusivity (cMD) were higher in lesions. Conversely, compartmental fractional anisotropy (cFA) and heterogeneity index were lower in lesions. An analysis of DTI equivalents showed the same trends. In whole-brain NAWM of patients compared to controls, cRD and cMD were higher and cFA was lower in patients. CONCLUSION: Lesions in POMS can be accurately characterized by a DCI model. Incipient changes in NAWM seen in DCI may not be readily observable by DTI.
Ariyurek, Cemre, Tess Wallace, Tobias Kober, Sila Kurugol, and Onur Afacan. 2022. “Prospective Motion Correction in Kidney MRI Using FID Navigators”. Magn Reson Med. https://doi.org/10.1002/mrm.29424.
PURPOSE: Abdominal MRI scans may require breath-holding to prevent image quality degradation, which can be challenging for patients, especially children. In this study, we evaluate whether FID navigators can be used to measure and correct for motion prospectively, in real-time. METHODS: FID navigators were inserted into a 3D radial sequence with stack-of-stars sampling. MRI experiments were conducted on 6 healthy volunteers. A calibration scan was first acquired to create a linear motion model that estimates the kidney displacement due to respiration from the FID navigator signal. This model was then applied to predict and prospectively correct for motion in real time during deep and continuous deep breathing scans. Resultant images acquired with the proposed technique were compared with those acquired without motion correction. Dice scores were calculated between inhale/exhale motion states. Furthermore, images acquired using the proposed technique were compared with images from extra-dimensional golden-angle radial sparse parallel, a retrospective motion state binning technique. RESULTS: Images reconstructed for each motion state show that the kidneys' position could be accurately tracked and corrected with the proposed method. The mean of Dice scores computed between the motion states were improved from 0.93 to 0.96 using the proposed technique. Depiction of the kidneys was improved in the combined images of all motion states. Comparing results of the proposed technique and extra-dimensional golden-angle radial sparse parallel, high-quality images can be reconstructed from a fraction of spokes using the proposed method. CONCLUSION: The proposed technique reduces blurriness and motion artifacts in kidney imaging by prospectively correcting their position both in-plane and through-slice.
Wallace, Tess, Tobias Kober, Jason Stockmann, Jonathan Polimeni, Simon Warfield, and Onur Afacan. 2022. “Real-Time Shimming With FID Navigators”. Magn Reson Med. https://doi.org/10.1002/mrm.29421.
PURPOSE: To implement a method for real-time field control using rapid FID navigator (FIDnav) measurements and evaluate the efficacy of the proposed approach for mitigating dynamic field perturbations and improving T 2 * $$ {\mathrm{T}}_2^{\ast } $$ -weighted image quality. METHODS: FIDnavs were embedded in a gradient echo sequence and a subject-specific linear calibration model was generated on the scanner to facilitate rapid shim updates in response to measured FIDnav signals. To confirm the accuracy of FID-navigated field updates, phantom and volunteer scans were performed with online updates of the scanner B0 shim settings. To evaluate improvement in T 2 * $$ {\mathrm{T}}_2^{\ast } $$ -weighted image quality with real-time shimming, 10 volunteers were scanned at 3T while performing deep-breathing and nose-touching tasks designed to modulate the B0 field. Quantitative image quality metrics were compared with and without FID-navigated field control. An additional volunteer was scanned at 7T to evaluate performance at ultra-high field. RESULTS: Applying measured FIDnav shim updates successfully compensated for applied global and linear field offsets in phantoms and across all volunteers. FID-navigated real-time shimming led to a substantial reduction in field fluctuations and a consequent improvement in T 2 * $$ {\mathrm{T}}_2^{\ast } $$ -weighted image quality in volunteers performing deep-breathing and nose-touching tasks, with 7.57% ± 6.01% and 8.21% ± 10.90% improvement in peak SNR and structural similarity, respectively. CONCLUSION: FIDnavs facilitate rapid measurement and application of field coefficients for slice-wise B0 shimming. The proposed approach can successfully counteract spatiotemporal field perturbations and substantially improves T 2 * $$ {\mathrm{T}}_2^{\ast } $$ -weighted image quality, which is important for a variety of clinical and research applications, particularly at ultra-high field.
Machado-Rivas, Fedel, Jasmine Gandhi, Jungwhan John Choi, Clemente Velasco-Annis, Onur Afacan, Simon Warfield, Ali Gholipour, and Camilo Jaimes. 2022. “Normal Growth, Sexual Dimorphism, and Lateral Asymmetries at Fetal Brain MRI”. Radiology 303 (1): 162-70. https://doi.org/10.1148/radiol.211222.
Background Tools in image reconstruction, motion correction, and segmentation have enabled the accurate volumetric characterization of fetal brain growth at MRI. Purpose To evaluate the volumetric growth of intracranial structures in healthy fetuses, accounting for gestational age (GA), sex, and laterality with use of a spatiotemporal MRI atlas of fetal brain development. Materials and Methods T2-weighted 3.0-T half-Fourier acquired single-shot turbo spin-echo sequence MRI was performed in healthy fetuses from prospectively recruited pregnant volunteers from March 2013 to May 2019. A previously validated section-to-volume reconstruction algorithm was used to generate intensity-normalized superresolution three-dimensional volumes that were registered to a fetal brain MRI atlas with 28 anatomic regions of interest. Atlas-based segmentation was performed and manually refined. Labels included the bilateral hippocampus, amygdala, caudate nucleus, lentiform nucleus, thalamus, lateral ventricle, cerebellum, cortical plate, hemispheric white matter, internal capsule, ganglionic eminence, ventricular zone, corpus callosum, brainstem, hippocampal commissure, and extra-axial cerebrospinal fluid. For fetuses younger than 31 weeks of GA, the subplate and intermediate zones were delineated. A linear regression analysis was used to determine weekly age-related change adjusted for sex and laterality. Results The final analytic sample consisted of 122 MRI scans in 98 fetuses (mean GA, 29 weeks ± 5 [range, 20-38 weeks]). All structures had significant volume growth with increasing GA (P < .001). Weekly age-related change for individual structures in the brain parenchyma ranged from 2.0% (95% CI: 0.9, 3.1; P < .001) in the hippocampal commissure to 19.4% (95% CI: 18.7, 20.1; P < .001) in the cerebellum. The largest sex-related differences were 22.1% higher volume in male fetuses for the lateral ventricles (95% CI: 10.9, 34.4; P < .001). There was rightward volumetric asymmetry of 15.6% for the hippocampus (95% CI: 14.2, 17.2; P < .001) and leftward volumetric asymmetry of 8.1% for the lateral ventricles (95% CI: 3.7, 12.2; P < .001). Conclusion With use of a spatiotemporal MRI atlas, volumetric growth of the fetal brain showed complex trajectories dependent on structure, gestational age, sex, and laterality. © RSNA, 2021 Online supplemental material is available for this article. See also the editorial by Rollins in this issue.
Sui, Yao, Onur Afacan, Camilo Jaimes, Ali Gholipour, and Simon Warfield. 2022. “Scan-Specific Generative Neural Network for MRI Super-Resolution Reconstruction”. IEEE Trans Med Imaging 41 (6): 1383-99. https://doi.org/10.1109/TMI.2022.3142610.
The interpretation and analysis of Magnetic resonance imaging (MRI) benefit from high spatial resolution. Unfortunately, direct acquisition of high spatial resolution MRI is time-consuming and costly, which increases the potential for motion artifact, and suffers from reduced signal-to-noise ratio (SNR). Super-resolution reconstruction (SRR) is one of the most widely used methods in MRI since it allows for the trade-off between high spatial resolution, high SNR, and reduced scan times. Deep learning has emerged for improved SRR as compared to conventional methods. However, current deep learning-based SRR methods require large-scale training datasets of high-resolution images, which are practically difficult to obtain at a suitable SNR. We sought to develop a methodology that allows for dataset-free deep learning-based SRR, through which to construct images with higher spatial resolution and of higher SNR than can be practically obtained by direct Fourier encoding. We developed a dataset-free learning method that leverages a generative neural network trained for each specific scan or set of scans, which in turn, allows for SRR tailored to the individual patient. With the SRR from three short duration scans, we achieved high quality brain MRI at an isotropic spatial resolution of 0.125 cubic mm with six minutes of imaging time for T2 contrast and an average increase of 7.2 dB (34.2%) in SNR to these short duration scans. Motion compensation was achieved by aligning the three short duration scans together. We assessed our technique on simulated MRI data and clinical data acquired from 15 subjects. Extensive experimental results demonstrate that our approach achieved superior results to state-of-the-art methods, while in parallel, performed at reduced cost as scans delivered with direct high-resolution acquisition.
Askin Incebacak, Ceren, Yao Sui, Laura Gui Levy, Laura Merlini, Joana Sa de Almeida, Sebastien Courvoisier, Tess Wallace, et al. 2022. “Super-Resolution Reconstruction of T2-Weighted Thick-Slice Neonatal Brain MRI Scans”. J Neuroimaging 32 (1): 68-79. https://doi.org/10.1111/jon.12929.
BACKGROUND AND PURPOSE: Super-resolutionreconstruction (SRR) can be used to reconstruct 3-dimensional (3D) high-resolution (HR) volume from several 2-dimensional (2D) low-resolution (LR) stacks of MRI slices. The purpose is to compare lengthy 2D T2-weighted HR image acquisition of neonatal subjects with 3D SRR from several LR stacks in terms of image quality for clinical and morphometric assessments. METHODS: LR brain images were acquired from neonatal subjects to reconstruct isotropic 3D HR volumes by using SRR algorithm. Quality assessments were done by an experienced pediatric radiologist using scoring criteria adapted to newborn anatomical landmarks. The Wilcoxon signed-rank test was used to compare scoring results between HR and SRR images. For quantitative assessments, morphology-based segmentation was performed on both HR and SRR images and Dice coefficients between the results were computed. Additionally, simple linear regression was performed to compare the tissue volumes. RESULTS: No statistical difference was found between HR and SRR structural scores using Wilcoxon signed-rank test (p = .63, Z = .48). Regarding segmentation results, R2 values for the volumes of gray matter, white matter, cerebrospinal fluid, basal ganglia, cerebellum, and total brain volume including brain stem ranged between .95 and .99. Dice coefficients between the segmented regions from HR and SRR ranged between .83 ± .04 and .96 ± .01. CONCLUSION: Qualitative and quantitative assessments showed that 3D SRR of several LR images produces images that are of comparable quality to standard 2D HR image acquisition for healthy neonatal imaging without loss of anatomical details with similar edge definition allowing the detection of fine anatomical structures and permitting comparable morphometric measurement.
Balachandrasekaran, Arvind, Alexander Cohen, Onur Afacan, Simon Warfield, and Ali Gholipour. 2022. “Reducing the Effects of Motion Artifacts in FMRI: A Structured Matrix Completion Approach”. IEEE Trans Med Imaging 41 (1): 172-85. https://doi.org/10.1109/TMI.2021.3107829.
Functional MRI (fMRI) is widely used to study the functional organization of normal and pathological brains. However, the fMRI signal may be contaminated by subject motion artifacts that are only partially mitigated by motion correction strategies. These artifacts lead to distance-dependent biases in the inferred signal correlations. To mitigate these spurious effects, motion-corrupted volumes are censored from fMRI time series. Censoring can result in discontinuities in the fMRI signal, which may lead to substantial alterations in functional connectivity analysis. We propose a new approach to recover the missing entries from censoring based on structured low rank matrix completion. We formulated the artifact-reduction problem as the recovery of a super-resolved matrix from unprocessed fMRI measurements. We enforced a low rank prior on a large structured matrix, formed from the samples of the time series, to recover the missing entries. The recovered time series, in addition to being motion compensated, are also slice-time corrected at a fine temporal resolution. To achieve a fast and memory-efficient solution for our proposed optimization problem, we employed a variable splitting strategy. We validated the algorithm with simulations, data acquired under different motion conditions, and datasets from the ABCD study. Functional connectivity analysis showed that the proposed reconstruction resulted in connectivity matrices with lower errors in pair-wise correlation than non-censored and censored time series based on a standard processing pipeline. In addition, seed-based correlation analyses showed improved delineation of the default mode network. These demonstrate that the method can effectively reduce the adverse effects of motion in fMRI analysis.
Vasylechko, Serge Didenko, Simon K Warfield, Onur Afacan, and Sila Kurugol. (2022) 2022. “Self-Supervised IVIM DWI Parameter Estimation With a Physics Based Forward Model.”. Magnetic Resonance in Medicine 87 (2): 904-14. https://doi.org/10.1002/mrm.28989.

PURPOSE: To assess the robustness and repeatability of intravoxel incoherent motion model (IVIM) parameter estimation for the diffusion-weighted MRI in the abdominal organs under the constraints of noisy diffusion signal using a novel neural network method.

METHODS: Clinically acquired abdominal scans of Crohn's disease patients were retrospectively analyzed with regions segmented in the kidney cortex, spleen, liver, and bowel. A novel IVIM parameter fitting method based on the principle of a physics guided self-supervised convolutional neural network that does not require reference parameter estimates for training was compared to a conventional non-linear least squares (NNLS) algorithm, and a voxelwise trained artificial neural network (ANN).

RESULTS: Results showed substantial increase in parameter robustness to the noise corrupted signal. In an intra-session repeatability experiment, the proposed method showed reduced coefficient of variation (CoV) over multiple acquisitions in comparison to conventional NLLS method and comparable performance to ANN. The use of D and f estimates from the proposed method led to the smallest misclassification error in linear discriminant analysis for characterization between normal and abnormal Crohn's disease bowel tissue. The fitting of D∗ parameter remains to be challenging.

CONCLUSION: The proposed method yields robust estimates of D and f IVIM parameters under the constraints of noisy diffusion signal. This indicates a potential for the use of the proposed method in conjunction with accelerated DW-MRI acquisition strategies, which would typically result in lower signal to noise ratio.

2021

Villarini, Barbara, Hykoush Asaturyan, Sila Kurugol, Onur Afacan, Jimmy Bell, and Louise Thomas. (2021) 2021. “3D Deep Learning for Anatomical Structure Segmentation in Multiple Imaging Modalities”. Proc IEEE Int Symp Comput Based Med Syst 2021: 166-71. https://doi.org/10.1109/cbms52027.2021.00066.
Accurate, quantitative segmentation of anatomical structures in radiological scans, such as Magnetic Resonance Imaging (MRI) and Computer Tomography (CT), can produce significant biomarkers and can be integrated into computer-aided assisted diagnosis (CADx) systems to support the interpretation of medical images from multi-protocol scanners. However, there are serious challenges towards developing robust automated segmentation techniques, including high variations in anatomical structure and size, the presence of edge-based artefacts, and heavy un-controlled breathing that can produce blurred motion-based artefacts. This paper presents a novel computing approach for automatic organ and muscle segmentation in medical images from multiple modalities by harnessing the advantages of deep learning techniques in a two-part process. (1) a 3D encoder-decoder, Rb-UNet, builds a localisation model and a 3D Tiramisu network generates a boundary-preserving segmentation model for each target structure; (2) the fully trained Rb-UNet predicts a 3D bounding box encapsulating the target structure of interest, after which the fully trained Tiramisu model performs segmentation to reveal detailed organ or muscle boundaries. The proposed approach is evaluated on six different datasets, including MRI, Dynamic Contrast Enhanced (DCE) MRI and CT scans targeting the pancreas, liver, kidneys and psoas-muscle and achieves quantitative measures of mean Dice similarity coefficient (DSC) that surpass or are comparable with the state-of-the-art. A qualitative evaluation performed by two independent radiologists verified the preservation of detailed organ and muscle boundaries.