Journal Papers

2021

Wallace, Tess, Jonathan Polimeni, Jason Stockmann, Scott Hoge, Tobias Kober, Simon Warfield, and Onur Afacan. 2021. “Dynamic Distortion Correction for Functional MRI Using FID Navigators”. Magn Reson Med 85 (3): 1294-1307. https://doi.org/10.1002/mrm.28505.
PURPOSE: To develop a method for slice-wise dynamic distortion correction for EPI using rapid spatiotemporal B0 field measurements from FID navigators (FIDnavs) and to evaluate the efficacy of this new approach relative to an established data-driven technique. METHODS: A low-resolution reference image was used to create a forward model of FIDnav signal changes to enable estimation of spatiotemporal B0 inhomogeneity variations up to second order from measured FIDnavs. Five volunteers were scanned at 3 T using a 64-channel coil with FID-navigated EPI. The accuracy of voxel shift measurements and geometric distortion correction was assessed for experimentally induced magnetic field perturbations. The temporal SNR was evaluated in EPI time-series acquired at rest and with a continuous nose-touching action, before and after image realignment. RESULTS: Field inhomogeneity coefficients and voxel shift maps measured using FIDnavs were in excellent agreement with multi-echo EPI measurements. The FID-navigated distortion correction accurately corrected image geometry in the presence of induced magnetic field perturbations, outperforming the data-driven approach in regions with large field offsets. In functional MRI scans with nose touching, FIDnav-based correction yielded temporal SNR gains of 30% in gray matter. Following image realignment, which accounted for global image shifts, temporal SNR gains of 3% were achieved. CONCLUSIONS: Our proposed application of FIDnavs enables slice-wise dynamic distortion correction with high temporal efficiency. We achieved improved signal stability by leveraging the encoding information from multichannel coils. This approach can be easily adapted to other EPI-based sequences to improve temporal SNR for a variety of clinical and research applications.

2020

Sui, Yao, Onur Afacan, Ali Gholipour, and Simon Warfield. (2020) 2020. “Learning a Gradient Guidance for Spatially Isotropic MRI Super-Resolution Reconstruction”. Med Image Comput Comput Assist Interv 12262: 136-46. https://doi.org/10.1007/978-3-030-59713-9_14.
In MRI practice, it is inevitable to appropriately balance between image resolution, signal-to-noise ratio (SNR), and scan time. It has been shown that super-resolution reconstruction (SRR) is effective to achieve such a balance, and has obtained better results than direct high-resolution (HR) acquisition, for certain contrasts and sequences. The focus of this work was on constructing images with spatial resolution higher than can be practically obtained by direct Fourier encoding. A novel learning approach was developed, which was able to provide an estimate of the spatial gradient prior from the low-resolution (LR) inputs for the HR reconstruction. By incorporating the anisotropic acquisition schemes, the learning model was trained over the LR images themselves only. The learned gradients were integrated as prior knowledge into a gradient-guided SRR model. A closed-form solution to the SRR model was developed to obtain the HR reconstruction. Our approach was assessed on the simulated data as well as the data acquired on a Siemens 3T MRI scanner containing 45 MRI scans from 15 subjects. The experimental results demonstrated that our approach led to superior SRR over state-of-the-art methods, and obtained better images at lower or the same cost in scan time than direct HR acquisition.
Sui, Yao, Onur Afacan, Ali Gholipour, and Simon Warfield. 2020. “SLIMM: Slice Localization Integrated MRI Monitoring”. Neuroimage 223: 117280. https://doi.org/10.1016/j.neuroimage.2020.117280.
Functional MRI (fMRI) is extremely challenging to perform in subjects who move because subject motion disrupts blood oxygenation level dependent (BOLD) signal measurement. It has become common to use retrospective framewise motion detection and censoring in fMRI studies to eliminate artifacts arising from motion. Data censoring results in significant loss of data and statistical power unless the data acquisition is extended to acquire more data not corrupted by motion. Acquiring more data than is necessary leads to longer than necessary scan duration, which is more expensive and may lead to additional subject non-compliance. Therefore, it is well established that real-time prospective motion monitoring is crucial to ensure data quality and reduce imaging costs. In addition, real-time monitoring of motion allows for feedback to the operator and the subject during the acquisition, to enable intervention to reduce the subject motion. The most widely used form of motion monitoring for fMRI is based on volume-to-volume registration (VVR), which quantifies motion as the misalignment between subsequent volumes. However, motion is not constrained to occur only at the boundaries of volume acquisition, but instead may occur at any time. Consequently, each slice of an fMRI acquisition may be displaced by motion, and assessment of whole volume to volume motion may be insensitive to both intra-volume and inter-volume motion that is revealed by displacement of the slices. We developed the first slice-by-slice self-navigated motion monitoring system for fMRI by developing a real-time slice-to-volume registration (SVR) algorithm. Our real-time SVR algorithm, which is the core of the system, uses a local image patch-based matching criterion along with a Levenberg-Marquardt optimizer, all accelerated via symmetric multi-processing, with interleaved and simultaneous multi-slice acquisition schemes. Extensive experimental results on real motion data demonstrated that our fast motion monitoring system, named Slice Localization Integrated MRI Monitoring (SLIMM), provides more accurate motion measurements than a VVR based approach. Therefore, SLIMM offers improved online motion monitoring which is particularly important in fMRI for challenging patient populations. Real-time motion monitoring is crucial for online data quality control and assurance, for enabling feedback to the subject and the operator to act to mitigate motion, and in adaptive acquisition strategies that aim to ensure enough data of sufficient quality is acquired without acquiring excess data.
Campanale, Cosimo, Benoit Scherrer, Onur Afacan, Amara Majeed, Simon Warfield, and Stephen Sanders. 2020. “Myofiber Organization in the Failing Systemic Right Ventricle”. J Cardiovasc Magn Reson 22 (1): 49. https://doi.org/10.1186/s12968-020-00637-9.
BACKGROUND: The right ventricle (RV) often fails when functioning as the systemic ventricle, but the cause is not understood. We tested the hypothesis that myofiber organization is abnormal in the failing systemic right ventricle. METHODS: We used diffusion-weighted cardiovascular magnetic resonance imaging to examine 3 failing hearts explanted from young patients with a systemic RV and one structurally normal heart with postnatally acquired RV hypertrophy for comparison. Diffusion compartment imaging was computed to separate the free diffusive component representing free water from an anisotropic component characterizing the orientation and diffusion characteristics of myofibers. The orientation of each anisotropic compartment was displayed in glyph format and used for qualitative description of myofibers and for construction of tractograms. The helix angle was calculated across the ventricular walls in 5 locations and displayed graphically. Scalar parameters (fractional anisotropy and mean diffusivity) were compared among specimens. RESULTS: The hypertrophied systemic RV has an inner layer, comprising about 2/3 of the wall, composed of hypertrophied trabeculae and an epicardial layer of circumferential myofibers. Myofibers within smaller trabeculae are aligned and organized with parallel fibers while larger, composite bundles show marked disarray, largely between component trabeculae. We observed a narrow range of helix angles in the outer, compact part of the wall consistent with aligned, approximately circumferential fibers. However, there was marked variation of helix angle in the inner, trabecular part of the wall consistent with marked variation in fiber orientation. The apical whorl was disrupted or incomplete and we observed myocardial whorls or vortices at other locations. Fractional anisotropy was lower in abnormal hearts while mean diffusivity was more variable, being higher in 2 but lower in 1 heart, compared to the structurally normal heart. CONCLUSIONS: Myofiber organization is abnormal in the failing systemic RV and might be an important substrate for heart failure and arrhythmia. It is unclear if myofiber disorganization is due to hemodynamic factors, developmental problems, or both.
Ahtam, Banu, Susan Waisbren, Vera Anastasoaie, Gerard Berry, Matthew Brown, Stephanie Petrides, Onur Afacan, et al. 2020. “Identification of Neuronal Structures and Pathways Corresponding to Clinical Functioning in Galactosemia”. J Inherit Metab Dis 43 (6): 1205-18. https://doi.org/10.1002/jimd.12279.
Classic galactosemia (OMIM# 230400) is an autosomal recessive disorder due to galactose-1-phosphate uridyltransferase deficiency. Newborn screening and prompt treatment with a galactose-free diet prevent the severe consequences of galactosemia, but clinical outcomes remain suboptimal. Five men and five women with classic galactosemia (mean age = 27.2 ± 5.47 years) received comprehensive neurological and neuropsychological evaluations, electroencephalogram (EEG) and magnetic resonance imaging (MRI). MRI data from nine healthy controls (mean age = 30.22 ± 3.52 years) were used for comparison measures. Galactosemia subjects experienced impaired memory, language processing, visual-motor skills, and increased anxiety. Neurological examinations revealed tremor and dysarthria in six subjects. In addition, there was ataxia in three subjects and six subjects had abnormal gait. Mean full scale IQ was 80.4 ± 17.3. EEG evaluations revealed right-sided abnormalities in five subjects and bilateral abnormalities in one subject. Compared to age- and gender-matched controls, subjects with galactosemia had reduced volume in left cerebellum white matter, bilateral putamen, and left superior temporal sulcus. Galactosemia patients also had lower fractional anisotropy and higher radial diffusivity values in the dorsal and ventral language networks compared to the controls. Furthermore, there were significant correlations between neuropsychological test results and the T1 volume and diffusivity scalars. Our findings help to identify anatomic correlates to motor control, learning and memory, and language in subjects with galactosemia. The results from this preliminary assessment may provide insights into the pathophysiology of this inborn error of metabolism.
Afacan, Onur, Scott Hoge, Tess Wallace, Ali Gholipour, Sila Kurugol, and Simon Warfield. 2020. “Simultaneous Motion and Distortion Correction Using Dual-Echo Diffusion-Weighted MRI”. J Neuroimaging 30 (3): 276-85. https://doi.org/10.1111/jon.12708.
BACKGROUND AND PURPOSE: Geometric distortions resulting from large pose changes reduce the accuracy of motion measurements and interfere with the ability to generate artifact-free information. Our goal is to develop an algorithm and pulse sequence to enable motion-compensated, geometric distortion compensated diffusion-weighted MRI, and to evaluate its efficacy in correcting for the field inhomogeneity and position changes, induced by large and frequent head motions. METHODS: Dual echo planar imaging (EPI) with a blip-reversed phase encoding distortion correction technique was evaluated in five volunteers in two separate experiments and compared with static field map distortion correction. In the first experiment, dual-echo EPI images were acquired in two head positions designed to induce a large field inhomogeneity change. A field map and a distortion-free structural image were acquired at each position to assess the ability of dual-echo EPI to generate reliable field maps and enable geometric distortion correction in both positions. In the second experiment, volunteers were asked to move to multiple random positions during a diffusion scan. Images were reconstructed using the dual-echo correction and a slice-to-volume registration (SVR) registration algorithm. The accuracy of SVR motion estimates was compared to externally measured ground truth motion parameters. RESULTS: Our results show that dual-echo EPI can produce slice-level field maps with comparable quality to field maps generated by the reference gold standard method. We also show that slice-level distortion correction improves the accuracy of SVR algorithms as slices acquired at different orientations have different levels of distortion, which can create errors in the registration process. CONCLUSIONS: Dual-echo acquisitions with blip-reversed phase encoding can be used to generate slice-level distortion-free images, which is critical for motion-robust slice to volume registration. The distortion corrected images not only result in better motion estimates, but they also enable a more accurate final diffusion image reconstruction.
Jaimes, Camilo, Fedel Machado-Rivas, Onur Afacan, Shadab Khan, Bahram Marami, Cynthia Ortinau, Caitlin Rollins, Clemente Velasco-Annis, Simon Warfield, and Ali Gholipour. 2020. “In Vivo Characterization of Emerging White Matter Microstructure in the Fetal Brain in the Third Trimester”. Hum Brain Mapp 41 (12): 3177-85. https://doi.org/10.1002/hbm.25006.
The third trimester of pregnancy is a period of rapid development of fiber bundles in the fetal white matter. Using a recently developed motion-tracked slice-to-volume registration (MT-SVR) method, we aimed to quantify tract-specific developmental changes in apparent diffusion coefficient (ADC), fractional anisotropy (FA), and volume in third trimester healthy fetuses. To this end, we reconstructed diffusion tensor images from motion corrected fetal diffusion magnetic resonance imaging data. With an approved protocol, fetal MRI exams were performed on healthy pregnant women at 3 Tesla and included multiple (2-8) diffusion scans of the fetal head (1-2 b = 0 s/mm2 images and 12 diffusion-sensitized images at b = 500 s/mm2 ). Diffusion data from 32 fetuses (13 females) with median gestational age (GA) of 33 weeks 4 days were processed with MT-SVR and deterministic tractography seeded by regions of interest corresponding to 12 major fiber tracts. Multivariable regression analysis was used to evaluate the association of GA with volume, FA, and ADC for each tract. For all tracts, the volume and FA increased, and the ADC decreased with GA. Associations reached statistical significance for: FA and ADC of the forceps major; volume and ADC for the forceps minor; FA, ADC, and volume for the cingulum; ADC, FA, and volume for the uncinate fasciculi; ADC of the inferior fronto-occipital fasciculi, ADC of the inferior longitudinal fasciculi; and FA and ADC for the corticospinal tracts. These quantitative results demonstrate the complex pattern and rates of tract-specific, GA-related microstructural changes of the developing white matter in human fetal brain.
Kurugol, Sila, Catherine Seager, Hatim Thaker, Jaume Coll-Font, Onur Afacan, Reid Nichols, Simon Warfield, Richard Lee, and Jeanne Chow. (2020) 2020. “Feed and Wrap Magnetic Resonance Urography Provides Anatomic and Functional Imaging in Infants Without Anesthesia”. J Pediatr Urol 16 (1): 116-20. https://doi.org/10.1016/j.jpurol.2019.11.002.
OBJECTIVE: To describe a technique for performing magnetic resonance urogram (MRU) in infants without sedation or anesthesia. METHODS: Eighteen infants underwent MRU in the absence of sedating medications using a 'feed and wrap' technique (FW-MRU). Dynamic contrast enhanced images were obtained. Dynamic radial VIBE and compressed sensing image reconstruction were used to correct for motion artifact. RESULTS: Seventeen of the 18 patients had successful FW-MRU. Feed and wrap' magnetic resonance urogram provided high-quality anatomic and functional renal data. CONCLUSION: Initial experience with FW-MRU demonstrates it to be a promising anesthesia-free modality for obtaining anatomic and functional imaging of the urinary tract in infants.
Coll-Font, Jaume, Onur Afacan, Jeanne Chow, Richard Lee, Alto Stemmer, Simon Warfield, and Sila Kurugol. 2020. “Bulk Motion-Compensated DCE-MRI for Functional Imaging of Kidneys in Newborns”. J Magn Reson Imaging 52 (1): 207-16. https://doi.org/10.1002/jmri.27021.
BACKGROUND: Evaluation of kidney function in newborns with hydronephrosis is important for clinical decisions. Dynamic contrast-enhanced (DCE) MRI can provide the necessary anatomical and functional information. Golden angle dynamic radial acquisition and compressed sensing reconstruction provides sufficient spatiotemporal resolution to achieve accurate parameter estimation for functional imaging of kidneys. However, bulk motion during imaging (rigid or nonrigid movement of the subject resulting in signal dropout) remains an unresolved challenge. PURPOSE: To evaluate a motion-compensated (MoCo) DCE-MRI technique for robust evaluation of kidney function in newborns. Our method includes: 1) motion detection, 2) motion-robust image reconstruction, 3) joint realignment of the volumes, and 4) tracer-kinetic (TK) model fitting to evaluate kidney function parameters. STUDY TYPE: Retrospective. SUBJECTS: Eleven newborn patients (ages <6 months, 6 female). FIELD STRENGTH/SEQUENCE: 3T; dynamic "stack-of-stars" 3D fast low-angle shot (FLASH) sequence using a multichannel body-matrix coil. ASSESSMENT: We evaluated the proposed technique in terms of the signal-to-noise ratio (SNR) of the reconstructed images, the presence of discontinuities in the contrast agent concentration time curves due to motion with a total variation (TV) metric and the goodness of fit of the TK model, and the standard variation of its parameters. STATISTICAL TESTS: We used a paired t-test to compare the MoCo and no-MoCo results. RESULTS: The proposed MoCo method successfully detected motion and improved the SNR by 3.3 (P = 0.012) and decreased TV by 0.374 (P = 0.017) across all subjects. Moreover, it decreased nRMSE of the TK model fit for the subjects with less than five isolated bulk motion events in 6 minutes (mean 1.53, P = 0.043), but not for the subjects with more frequent events or no motion (P = 0.745 and P = 0.683). DATA CONCLUSION: Our results indicate that the proposed MoCo technique improves the image quality and accuracy of the TK model fit for subjects who present isolated bulk motion events. LEVEL OF EVIDENCE: 3 Technical Efficacy Stage: 1 J. Magn. Reson. Imaging 2020;52:207-216.
Wallace, Tess, Onur Afacan, Tobias Kober, and Simon Warfield. 2020. “Rapid Measurement and Correction of Spatiotemporal B Field Changes Using FID Navigators and a Multi-Channel Reference Image”. Magn Reson Med 83 (2): 575-89. https://doi.org/10.1002/mrm.27957.
PURPOSE: To measure spatiotemporal B0 field changes in real time using FID navigators (FIDnavs) and to demonstrate the efficacy of retrospectively correcting high-resolution T 2 * -weighted images using a novel FIDnav framework. METHODS: A forward model of the complex FIDnav signals was generated by simulating the effect of changes in the underlying B0 inhomogeneity coefficients, with spatial encoding provided by a multi-channel reference image. Experiments were performed at 3T to assess the accuracy of B0 field estimates from FIDnavs acquired from a 64-channel head coil under different shim settings and in 5 volunteers performing deep-breathing and nose-touching tasks designed to modulate the B0 field. Second-order, in-plane spherical harmonic (SH) inhomogeneity coefficients estimated from FIDnavs were incorporated into an iterative reconstruction to retrospectively correct 2D gradient-echo images acquired in both axial and sagittal planes. RESULTS: Spatiotemporal B0 field changes measured from rapidly acquired FIDnavs were in good agreement with the results of second-order SH fitting to the measured field maps. FIDnav field estimates accounted for a significant proportion of the ΔB0 variance induced by deep breathing (64 ± 21%) and nose touching (67 ± 34%) across all volunteers. Ghosting, blurring, and intensity modulation artifacts in T 2 * -weighted images, induced by spatiotemporal field changes, were visibly reduced following retrospective correction with FIDnav inhomogeneity coefficients. CONCLUSIONS: Spatially resolved B0 inhomogeneity changes up to second order can be characterized in real time using the proposed approach. Retrospective FIDnav correction substantially improves T 2 * -weighted image quality in the presence of strong B0 field modulations, with potential for real-time shimming.