Journal Papers

2020

Afacan, Onur, Tess Wallace, and Simon Warfield. 2020. “Retrospective Correction of Head Motion Using Measurements from an Electromagnetic Tracker”. Magn Reson Med 83 (2): 427-37. https://doi.org/10.1002/mrm.27934.
PURPOSE: To investigate the feasibility of using an electromagnetic (EM) tracker to estimate rigid body head motion parameters, and using these measurements to retrospectively reduce motion artifacts. THEORY AND METHODS: A clinically used MPRAGE sequence was modified to measure motion using the EM tracking system once per repetition time. A retrospective k-space based motion correction algorithm that corrects for phase ramps (translation in image domain) and rotation of 3D k-space (rotation in image domain) was developed, using the parameters recorded using an EM tracker. The accuracy of the EM tracker for the purpose of motion measurement and correction was tested in phantoms, volunteers, and pediatric patients. RESULTS: Position localization was accurate to the order of 200 microns compared with registration localization in a phantom study. The quality of reconstructed images was assessed by computing the root mean square error, the structural similarity metric and average edge strength. Image quality improved consistently when motion correction was applied in both volunteer scans with deliberate head motion and in pediatric patient scans. In patients, the average edge strength improved significantly with retrospective motion correction, compared with images with no correction applied. CONCLUSIONS: EM tracking was effective in measuring head motion in the MRI scanner with high accuracy, and enabled retrospective reconstruction to improve image quality by reducing motion artifacts.
Kurugol, Sila, Onur Afacan, Richard S Lee, Catherine M Seager, Michael A Ferguson, Deborah R Stein, Reid C Nichols, et al. (2020) 2020. “Correction To: Prospective Pediatric Study Comparing Glomerular Filtration Rate Estimates Based on Motion-Robust Dynamic Contrast-Enhanced Magnetic Resonance Imaging and Serum Creatinine (eGFR) to 99mTc DTPA.”. Pediatric Radiology 50 (5): 755-56. https://doi.org/10.1007/s00247-020-04654-9.

The originally published version of this article contained a typographical error. In the text under the subheading "Dynamic contrast-enhanced MRI method, post-processing, and MR-GFR calculation" and in Table 1 the intravenous injection rate of gadobutrol was incorrectly listed as 0.2 mL/s.

Kurugol, Sila, Onur Afacan, Richard S Lee, Catherine M Seager, Michael A Ferguson, Deborah R Stein, Reid C Nichols, et al. (2020) 2020. “Prospective Pediatric Study Comparing Glomerular Filtration Rate Estimates Based on Motion-Robust Dynamic Contrast-Enhanced Magnetic Resonance Imaging and Serum Creatinine (eGFR) to 99mTc DTPA.”. Pediatric Radiology 50 (5): 698-705. https://doi.org/10.1007/s00247-020-04617-0.

BACKGROUND: Current methods to estimate glomerular filtration rate (GFR) have shortcomings. Estimates based on serum creatinine are known to be inaccurate in the chronically ill and during acute changes in renal function. Gold standard methods such as inulin and 99mTc diethylenetriamine pentaacetic acid (DTPA) require blood or urine sampling and thus can be difficult to perform in children. Motion-robust radial volumetric interpolated breath-hold examination (VIBE) dynamic contrast-enhanced MRI represents a novel tool for estimating GFR that has not been validated in children.

OBJECTIVE: The purpose of our study was to determine the feasibility and accuracy of GFR measured by motion-robust radial VIBE dynamic contrast-enhanced MRI compared to estimates by serum creatinine (eGFR) and 99mTc DTPA in children.

MATERIALS AND METHODS: We enrolled children, 0-18 years of age, who were undergoing both a contrast-enhanced MRI and nuclear medicine 99mTc DTPA glomerular filtration rate (NM-GFR) within 2 weeks of each other. Enrolled children consented to an additional 6-min dynamic contrast-enhanced MRI scan using the motion-robust high spatiotemporal resolution prototype dynamic radial VIBE sequence (Siemens, Erlangen, Germany) at 3 tesla (T). The images were reconstructed offline with high temporal resolution ( 3 s/volume) using compressed sensing image reconstruction including regularization in temporal dimension to improve image quality and reduce streaking artifacts. Images were then automatically post-processed using in-house-developed software. Post-processing steps included automatic segmentation of kidney parenchyma and aorta using convolutional neural network techniques and tracer kinetic model fitting using the Sourbron two-compartment model to calculate the MR-based GFR (MR-GFR). The NM-GFR was compared to MR-GFR and estimated GFR based on serum creatinine (eGFR) using Pearson correlation coefficient and Bland-Altman analysis.

RESULTS: Twenty-one children (7 female, 14 male) were enrolled between February 2017 and May 2018. Data from six of these children were not further analyzed because of deviations from the MRI protocol. Fifteen patients were analyzed (5 female, 10 male; average age 5.9 years); the method was technically feasible in all children. The results showed that the MR-GFR correlated with NM-GFR with a Pearson correlation coefficient (r-value) of 0.98. Bland-Altman analysis (i.e. difference of MR-GFR and NM-GFR versus mean of NM-GFR and MR-GFR) showed a mean difference of -0.32 and reproducibility coefficient of 18 with 95% confidence interval, and the coefficient of variation of 6.7% with values between -19 (-1.96 standard deviation) and 18 (+1.96 standard deviation). In contrast, serum creatinine compared with NM-GFR yielded an r-value of 0.73. Bland-Altman analysis (i.e. difference of eGFR and NM-GFR versus mean of NM-GFR and eGFR) showed a mean difference of 2.9 and reproducibility coefficient of 70 with 95% confidence interval, and the coefficient of variation of 25% with values between -67 (-1.96 standard deviation) and 73 (+1.96 standard deviation).

CONCLUSION: MR-GFR is a technically feasible and reliable method of measuring GFR when compared to the reference standard, NM-GFR by serum 99mTc DTPA, and MR-GFR is more reliable than estimates based on serum creatinine.

Afacan, Onur, Scott Hoge, Tess E Wallace, Ali Gholipour, Sila Kurugol, and Simon K Warfield. (2020) 2020. “Simultaneous Motion and Distortion Correction Using Dual-Echo Diffusion-Weighted MRI.”. Journal of Neuroimaging : Official Journal of the American Society of 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.

Sui, Yao, Onur Afacan, Ali Gholipour, and Simon K Warfield. (2020) 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.

2019

Sui, Yao, Onur Afacan, Ali Gholipour, and Simon Warfield. (2019) 2019. “Isotropic MRI Super-Resolution Reconstruction With Multi-Scale Gradient Field Prior”. Med Image Comput Comput Assist Interv 11766: 3-11. https://doi.org/10.1007/978-3-030-32248-9_1.
In this work, we proposed a novel image-based MRI super-resolution reconstruction (SRR) approach based on anisotropic acquisition schemes. We achieved superior reconstruction to state-of-the-art work by introducing a new multi-scale gradient field prior that guides the reconstruction of the high-resolution (HR) image. The prior improves both spatial smoothness and edge preservation. The inverse of the forward model of image formation is used to propagate the gradient guidance from the low-resolution (LR) images to the HR image space. The gradient fields over multiple scales were exploited for more accurate edge localization in the reconstruction. The proposed SRR allows inter-volume motion during the MRI scans and can incorporate with the LR images with arbitrary orientations and displacements in the frequency space, such as orthogonal and origin-shifted scans. The proposed approach was evaluated on the synthetic data as well as the data acquired on a Siemens 3T MRI scanner containing 45 MRI scans from 14 subjects. The evaluation results demonstrate that our proposed prior leads to improved SRR as compared to state-of-the-art priors, and that the proposed SRR obtains better results at lower or the same cost in scan time than direct HR acquisition. In particular, the anatomical structures of hippocampus can be clearly shown in our reconstructed images. This is a significant improvement for the in vivo studies of the hippocampus.
Coll-Font, Jaume, Onur Afacan, Jeanne Chow, and Sila Kurugol. (2019) 2019. “Linear Time Invariant Model Based Motion Correction (LiMo-MoCo) of Dynamic Radial Contrast Enhanced MRI”. Med Image Comput Comput Assist Interv 11765: 430-37. https://doi.org/10.1007/978-3-030-32245-8_48.
Early identification of kidney function deterioration is essential to determine which newborn patients with dilation of the renal pelvis (hydronephrosis) should undergo surgery. Kidney function can be measured by fitting a tracer kinetic (TK) model onto a series of Dynamic Contrast Enhanced (DCE) MR images and deriving the glomerular filtration rate (GFR) from the TK model. Unfortunately, heavy breathing and large bulk motion events create outliers and misalignments that introduce large errors in the TK estimates. Moreover, aligning the series of DCE images is not trivial due to the contrast differences between them and the undersampling artifacts due to fast imaging. We present a bulk motion detection and a linear time invariant (LTI) model-based motion correction approach for DCE-MRI alignment that leverages the temporal dynamics of the DCE data at each voxel. We evaluate our approach on 10 newborn patients that underwent DCE imaging without sedation. For each patient, we reconstructed the sequence of DCE images, detected and removed the volumes corrupted by motion using a self navigation approach, aligned the sequence using our approach and fitted the TK model to compute GFR. The results show that our approach correctly aligned all volumes and improved the TK model fit and, on average, reducing the normalized root-mean-squared error by 0.17.
Afacan, Onur, Judy Estroff, Edward Yang, Carol Barnewolt, Susan Connolly, Richard Parad, Robert Mulkern, Simon Warfield, and Ali Gholipour. (2019) 2019. “Fetal Echoplanar Imaging: Promises and Challenges”. Top Magn Reson Imaging 28 (5): 245-54. https://doi.org/10.1097/RMR.0000000000000219.
Fetal magnetic resonance imaging (MRI) has been gaining increasing interest in both clinical radiology and research. Echoplanar imaging (EPI) offers a unique potential, as it can be used to acquire images very fast. It can be used to freeze motion, or to get multiple images with various contrast mechanisms that allow studying the microstructure and function of the fetal brain and body organs. In this article, we discuss the current clinical and research applications of fetal EPI. This includes T2*-weighted imaging to better identify blood products and vessels, using diffusion-weighted MRI to investigate connections of the developing brain and using functional MRI (fMRI) to identify the functional networks of the developing brain. EPI can also be used as an alternative structural sequence when banding or standing wave artifacts adversely affect the mainstream sequences used routinely in structural fetal MRI. We also discuss the challenges with EPI acquisitions, and potential solutions. As EPI acquisitions are inherently sensitive to susceptibility artifacts, geometric distortions limit the use of high-resolution EPI acquisitions. Also, interslice motion and transmit and receive field inhomogeneities may create significant artifacts in fetal EPI. We conclude by discussing promising research directions to overcome these challenges to improve the use of EPI in clinical and research applications.
Peters, Jurriaan, Robbert Struyven, Anna Prohl, Lana Vasung, Andrija Stajduhar, Maxime Taquet, John Bushman, et al. 2019. “White Matter Mean Diffusivity Correlates With Myelination in Tuberous Sclerosis Complex”. Ann Clin Transl Neurol 6 (7): 1178-90. https://doi.org/10.1002/acn3.793.
OBJECTIVE: Diffusion tensor imaging (DTI) of the white matter is a biomarker for neurological disease burden in tuberous sclerosis complex (TSC). To clarify the basis of abnormal diffusion in TSC, we correlated ex vivo high-resolution diffusion imaging with histopathology in four tissue types: cortex, tuber, perituber, and white matter. METHODS: Surgical specimens of three children with TSC were scanned in a 3T or 7T MRI with a structural image isotropic resolution of 137-300 micron, and diffusion image isotropic resolution of 270-1,000 micron. We stained for myelin (luxol fast blue, LFB), gliosis (glial fibrillary acidic protein, GFAP), and neurons (NeuN) and registered the digitized histopathology slides (0.686 micron resolution) to MRI for visual comparison. We then performed colocalization analysis in four tissue types in each specimen. Finally, we applied a linear mixed model (LMM) for pooled analysis across the three specimens. RESULTS: In white matter and perituber regions, LFB optical density measures correlated with fractional anisotropy (FA) and inversely with mean diffusivity (MD). In white matter only, GFAP correlated with MD, and inversely with FA. In tubers and in the cortex, there was little variation in mean LFB and GFAP signal intensity, and no correlation with MRI metrics. Neuronal density correlated with MD. In the analysis of the combined specimens, the most robust correlation was between white matter MD and LFB metrics. INTERPRETATION: In TSC, diffusion imaging abnormalities in microscopic tissue types correspond to specific histopathological markers. Across all specimens, white matter diffusivity correlates with myelination.
Cole, Alexis, Dorothy Perry, Ali Raza, Arthur Nedder, Elizabeth Pollack, William Regan, Sarah Bosch, et al. (2019) 2019. “Perioperatively Inhaled Hydrogen Gas Diminishes Neurologic Injury Following Experimental Circulatory Arrest in Swine”. JACC Basic Transl Sci 4 (2): 176-87. https://doi.org/10.1016/j.jacbts.2018.11.006.
This study used a swine model of mildly hypothermic prolonged circulatory arrest and found that the addition of 2.4% inhaled hydrogen gas to inspiratory gases during and after the ischemic insult significantly decreased neurologic and renal injury compared with controls. With proper precautions, inhalational hydrogen may be administered safely through conventional ventilators and may represent a complementary therapy that can be easily incorporated into current workflows. In the future, inhaled hydrogen may diminish the sequelae of ischemia that occurs in congenital heart surgery, cardiac arrest, extracorporeal life-support events, acute myocardial infarction, stroke, and organ transplantation.