1
|
Jochmann T, Salman F, Dwyer MG, Bergsland N, Zivadinov R, Haueisen J, Schweser F. Quantitative susceptibility mapping in magnetically inhomogeneous tissues. Magn Reson Med 2025. [PMID: 40312865 DOI: 10.1002/mrm.30537] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/04/2024] [Revised: 03/12/2025] [Accepted: 03/30/2025] [Indexed: 05/03/2025]
Abstract
PURPOSE Conventional quantitative susceptibility mapping (QSM) methods rely on simplified physical models that assume isotropic and homogeneous tissue properties, leading to artifacts and inaccuracies in biological tissues. This study aims to develop and evaluate DEEPOLE, a deep learning-based method that incorporates macroscopically nondipolar Larmor frequency shifts into QSM to enhance the quality and accuracy of susceptibility maps. METHODS DEEPOLE integrates the QUASAR model into a deep convolutional neural network to account for frequency contributions neglected by conventional QSM. We trained DEEPOLE using synthesized data reflecting realistic power spectrum distributions. Its performance was evaluated against traditional QSM algorithms-including deep learning QSM, QUASAR (quantitative susceptibility and residual mapping), morphology-enabled dipole inversion (MEDI), fast nonlinear susceptibility inversion (FANSI), and superfast dipole inversion (SDI)-using realistic digital brain models with and without microstructure effects, as well as in vivo human brain data. Quantitative assessments focused on susceptibility estimation accuracy, artifact reduction, and anatomical consistency. RESULTS In digital brain models, DEEPOLE outperformed conventional QSM methods by producing susceptibility maps with fewer artifacts and greater quantitative accuracy, especially in regions affected by microstructure effects. In vivo, DEEPOLE generated more anatomically consistent susceptibility maps and mitigated artifacts such as inhomogeneities and streaking, providing improved susceptibility estimates in deep gray matter and white matter. CONCLUSION Incorporating macroscopically nondipolar Larmor frequency shifts into QSM through DEEPOLE improves the quality and accuracy of susceptibility maps. This methodological advancement enhances the reliability of susceptibility measurements, particularly in studies of neurodegenerative and demyelinating conditions where macroscopically nondipolar contributions are substantial.
Collapse
Affiliation(s)
- Thomas Jochmann
- Institute of Biomedical Engineering and Informatics, Department of Computer Science and Automation, Technische Universität Ilmenau, Ilmenau, Germany
- Buffalo Neuroimaging Analysis Center, Department of Neurology, Jacobs School of Medicine and Biomedical Sciences at the University at Buffalo, The State University of New York, Buffalo, New York, USA
| | - Fahad Salman
- Buffalo Neuroimaging Analysis Center, Department of Neurology, Jacobs School of Medicine and Biomedical Sciences at the University at Buffalo, The State University of New York, Buffalo, New York, USA
- Department of Biomedical Engineering, University at Buffalo, The State University of New York, Buffalo, New York, USA
| | - Michael G Dwyer
- Buffalo Neuroimaging Analysis Center, Department of Neurology, Jacobs School of Medicine and Biomedical Sciences at the University at Buffalo, The State University of New York, Buffalo, New York, USA
- Center for Biomedical Imaging, Clinical and Translational Science Institute, University at Buffalo, The State University of New York, Buffalo, New York, USA
| | - Niels Bergsland
- Buffalo Neuroimaging Analysis Center, Department of Neurology, Jacobs School of Medicine and Biomedical Sciences at the University at Buffalo, The State University of New York, Buffalo, New York, USA
| | - Robert Zivadinov
- Buffalo Neuroimaging Analysis Center, Department of Neurology, Jacobs School of Medicine and Biomedical Sciences at the University at Buffalo, The State University of New York, Buffalo, New York, USA
- Center for Biomedical Imaging, Clinical and Translational Science Institute, University at Buffalo, The State University of New York, Buffalo, New York, USA
| | - Jens Haueisen
- Institute of Biomedical Engineering and Informatics, Department of Computer Science and Automation, Technische Universität Ilmenau, Ilmenau, Germany
- Department of Neurology, Jena University Hospital, Jena, Germany
| | - Ferdinand Schweser
- Buffalo Neuroimaging Analysis Center, Department of Neurology, Jacobs School of Medicine and Biomedical Sciences at the University at Buffalo, The State University of New York, Buffalo, New York, USA
- Center for Biomedical Imaging, Clinical and Translational Science Institute, University at Buffalo, The State University of New York, Buffalo, New York, USA
| |
Collapse
|
2
|
Alushaj E, Kuurstra A, Menon RS, Ganjavi H, Morava A, Sharma M, Kashgari A, Barr J, Reisman W, Khan AR, MacDonald PA. Midbrain and pallidal iron changes identify patients with REM sleep behaviour disorder and Parkinson's disease. NPJ Parkinsons Dis 2025; 11:84. [PMID: 40268921 PMCID: PMC12019255 DOI: 10.1038/s41531-025-00916-1] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/24/2023] [Accepted: 03/15/2025] [Indexed: 04/25/2025] Open
Abstract
Idiopathic REM sleep behaviour disorder (iRBD) is considered a prodromal form of Parkinson's Disease (PD), potentially exhibiting similar patterns of neurodegeneration, such as brain iron changes. We investigated midbrain and pallidal iron using quantitative susceptibility mapping (QSM) in 16 iRBD patients, 30 PD patients, and 38 age-matched healthy controls (HCs) with 3T MRI. QSM revealed elevated substantia nigra pars compacta (SNc) mean susceptibility in both iRBD and PD patient groups compared to HCs, though iRBD and PD QSM measures did not differ. There were no SN pars reticulata group differences. Mean susceptibility was reduced for PD relative to iRBD and HCs in the globus pallidus externa (GPe). Furthermore, mean susceptibility was reduced for PD relative to iRBD in the GP interna (GPi). GPe/GPi mean susceptibility decreased with PD subgroup motor severity. Consistent with this, QSM in left GPi and MDS-UPDRS-III scores correlated negatively in PD patients, as well as in iRBD and PD patients combined. PD patients also evidenced higher mean susceptibility in the right ventral tegmental area (VTA) compared to iRBD and HCs, consistent with later VTA degeneration. RBD symptomatology did not correlate with QSM values. Combining SNc, GPe, GPi, and VTA QSM values, we distinguished iRBD-HCs, PD-HCs, and iRBD-PD patients at single-subject levels (0.84, 0.86, and 0.81 accuracies), using ROC curve analyses with repeated k-folds cross-validation. Using 3T MRI, QSM values in SNc, GPe, GPi, and VTA demonstrate promise as investigational measures and diagnostic/progression biomarkers of prodromal and early PD.
Collapse
Affiliation(s)
- Erind Alushaj
- Department of Neuroscience, Schulich School of Medicine and Dentistry, Western University, London, ON, Canada
- Western Centre for Brain and Mind, Western University, London, ON, Canada
| | - Alan Kuurstra
- Robarts Research Institute, Western University, London, ON, Canada
- Department of Medical Biophysics, Western University, London, ON, Canada
| | - Ravi S Menon
- Robarts Research Institute, Western University, London, ON, Canada
- Department of Medical Biophysics, Western University, London, ON, Canada
| | - Hooman Ganjavi
- Department of Psychiatry, Western University, London, ON, Canada
| | - Anisa Morava
- School of Kinesiology, Faculty of Health Sciences, Western University, London, ON, Canada
| | - Manas Sharma
- Department of Radiology, Western University, London, ON, Canada
- Department of Clinical Neurological Sciences, Western University, London, ON, Canada
| | - Alia Kashgari
- Department of Medicine, Respirology Division, Western University, London, ON, Canada
| | - Jennifer Barr
- Department of Psychiatry, Western University, London, ON, Canada
| | - William Reisman
- Department of Medicine, Respirology Division, Western University, London, ON, Canada
| | - Ali R Khan
- Robarts Research Institute, Western University, London, ON, Canada
- Department of Medical Biophysics, Western University, London, ON, Canada
| | - Penny A MacDonald
- Western Centre for Brain and Mind, Western University, London, ON, Canada.
- Department of Clinical Neurological Sciences, Western University, London, ON, Canada.
| |
Collapse
|
3
|
de Vries E, Hagbohm C, Ouellette R, Granberg T. Clinical 7 Tesla magnetic resonance imaging: Impact and patient value in neurological disorders. J Intern Med 2025; 297:244-261. [PMID: 39775908 PMCID: PMC11846079 DOI: 10.1111/joim.20059] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 01/11/2025]
Abstract
Magnetic resonance imaging (MRI) is a cornerstone of non-invasive diagnostics and treatment monitoring, particularly for diseases of the central nervous system. Although 1.5- and 3 Tesla (T) field strengths remain the clinical standard, the advent of 7 T MRI represents a transformative step forward, offering superior spatial resolution, contrast, and sensitivity for visualizing neuroanatomy, metabolism, and function. Recent innovations, including parallel transmission and deep learning-based reconstruction, have resolved many prior technical challenges of 7 T MRI, enabling its routine clinical use. This review examines the diagnostic impact, patient value, and practical considerations of 7 T MRI, emphasizing its role in facilitating earlier diagnoses and improving care in conditions, such as amyotrophic lateral sclerosis (ALS), epilepsy, multiple sclerosis (MS), dementia, parkinsonism, tumors, and vascular diseases. Based on insights from over 1200 clinical scans with a second-generation 7 T system, the review highlights disease-specific biomarkers such as the motor band sign in ALS and the new diagnostic markers in MS, the central vein sign, and paramagnetic rim lesions. The unparalleled ability of 7 T MRI to study neurological diseases ex vivo at ultra-high resolution is also explored, offering new opportunities to understand pathophysiology and identify novel treatment targets. Additionally, the review provides a clinical perspective on patient handling and safety considerations, addressing challenges and practicalities associated with clinical 7 T MRI. By bridging research and clinical practice, 7 T MRI has the potential to redefine neuroimaging and advance the understanding and management of complex neurological disorders.
Collapse
Affiliation(s)
- Elisabeth de Vries
- Department of NeuroradiologyKarolinska University HospitalStockholmSweden
- Department of Clinical NeuroscienceKarolinska InstitutetStockholmSweden
| | - Caroline Hagbohm
- Department of NeuroradiologyKarolinska University HospitalStockholmSweden
- Department of Clinical NeuroscienceKarolinska InstitutetStockholmSweden
| | - Russell Ouellette
- Department of NeuroradiologyKarolinska University HospitalStockholmSweden
- Department of Clinical NeuroscienceKarolinska InstitutetStockholmSweden
| | - Tobias Granberg
- Department of NeuroradiologyKarolinska University HospitalStockholmSweden
- Department of Clinical NeuroscienceKarolinska InstitutetStockholmSweden
| |
Collapse
|
4
|
Cherukara MT, Shmueli K. Comparing repeatability metrics for quantitative susceptibility mapping in the head and neck. MAGMA (NEW YORK, N.Y.) 2025:10.1007/s10334-025-01229-3. [PMID: 40024974 DOI: 10.1007/s10334-025-01229-3] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Received: 10/25/2024] [Revised: 01/09/2025] [Accepted: 01/21/2025] [Indexed: 03/04/2025]
Abstract
OBJECTIVE Quantitative susceptibility mapping (QSM) is a technique that has been demonstrated to be highly repeatable in the brain. As QSM is applied to other parts of the body, it is necessary to investigate metrics for quantifying repeatability, to enable optimization of repeatable QSM reconstruction pipelines beyond the brain. MATERIALS AND METHODS MRI data were acquired in the head and neck (HN) region in ten healthy volunteers, who underwent six acquisitions across two sessions. QSMs were reconstructed using six representative state-of-the-art techniques. Repeatability of the susceptibility values was compared using voxel-wise metrics (normalized root mean squared error and XSIM) and ROI-based metrics (within-subject and between-subject standard deviation, coefficient of variation (CV), intraclass correlation coefficient (ICC)). RESULTS Both within-subject and between-subject variations were smaller than the variation between QSM dipole inversion methods, in most ROIs. autoNDI produced the most repeatable susceptibility values, with ICC > 0.75 in three of six HN ROIs with an average ICC of 0.66 across all ROIs. Joint consideration of standard deviation and ICC offered the best metric of repeatability for comparisons between QSM methods, given typical distributions of positive and negative QSM values. DISCUSSION Repeatability of QSM in the HN region is highly dependent on the dipole inversion method chosen, but the most repeatable methods (autoNDI, QSMnet, TFI) are only moderately repeatable in most HN ROIs.
Collapse
Affiliation(s)
- Matthew T Cherukara
- Department of Medical Physics and Biomedical Engineering, University College London, London, UK.
| | - Karin Shmueli
- Department of Medical Physics and Biomedical Engineering, University College London, London, UK
| |
Collapse
|
5
|
Zhao H, Ji QH, Jia ZZ, Shen LH. Association between deep gray matter iron deposition and clinical symptoms in Parkinson's disease: a quantitative susceptibility mapping study. Front Neurol 2025; 15:1442903. [PMID: 39835146 PMCID: PMC11743366 DOI: 10.3389/fneur.2024.1442903] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/03/2024] [Accepted: 12/12/2024] [Indexed: 01/22/2025] Open
Abstract
Purpose This study aimed to assess the association between motor and non-motor symptoms of Parkinson's disease (PD) and iron accumulation within the deep gray matter of the brain by Quantitative Susceptibility Mapping (QSM). Methods Fifty-six PD patients and twenty-nine healthy controls were recruited in this study. According to the Hoehn and Yahr (H-Y) stage score, PD patients were divided into early stage (H-Y ≤ 2) and advanced stage (H-Y > 2) groups. Specifically, the Regions of Interest (ROIs) encompassed the substantia nigra (SN), red nucleus (RN), caudate nucleus (CN), globus pallidus (GP) and putamen (PT). Meanwhile, various rating scales were used to assess the clinical symptoms of PD. Results Compared to healthy controls (HCs), PD patients showed a significant increase in magnetic susceptibility values (MSVs) within the SN and GP. Further comparisons indicated that the MSVs of the SN, PT, GP and CN are all higher in advanced stages than in early stages. Significant positive correlations were observed between the MSVs of the SN and scores on the UPDRS-III, HAMA, and HAMD (r = 0.310, p = 0.020; r = 0.273, p = 0.042; r = 0.342, p = 0.010, respectively). Likewise, the MSVs of the GP demonstrated notable correlations with HAMA and HAMD scores (r = 0.275, p = 0.040; r = 0.415, p = 0.001). Additionally, a significant correlation was found between the MSVs of the PT and HAMD scores (r = 0.360, p = 0.006). Furthermore, we identified a significant negative correlation between MMSE scores and the MSVs of both the PT and GP (r = -0.268, p = 0.046; r = -0.305, p = 0.022). Conclusion Our study revealed that QSM possesses the capability to serve as a biomarker for PD. Significant correlations were found between clinical features and the iron deposition in the nigrostriatal system.
Collapse
Affiliation(s)
- Hui Zhao
- Department of Neurology, Affiliated Hospital of Nantong University, Medical School of Nantong University, Nantong, China
- Department of Neurology, Affiliated Rudong Hospital of Xinglin College, Nantong University, Nantong, China
| | - Qiu-Hong Ji
- Department of Neurology, Affiliated Hospital of Nantong University, Medical School of Nantong University, Nantong, China
| | - Zhong-Zheng Jia
- Department of Medical Imaging, Affiliated Hospital of Nantong University, Medical School of Nantong University, Nantong, China
| | - Li-Hua Shen
- Department of Neurology, Affiliated Hospital of Nantong University, Medical School of Nantong University, Nantong, China
| |
Collapse
|
6
|
Mohammadi S, Ghaderi S, Fatehi F. Quantitative Susceptibility Mapping Values Quantification in Deep Gray Matter Structures for Relapsing-Remitting Multiple Sclerosis: A Systematic Review and Meta-Analysis. Brain Behav 2024; 14:e70093. [PMID: 39415615 PMCID: PMC11483550 DOI: 10.1002/brb3.70093] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/11/2024] [Revised: 09/16/2024] [Accepted: 09/20/2024] [Indexed: 10/19/2024] Open
Abstract
BACKGROUND/OBJECTIVES This systematic review and meta-analysis aimed to investigate the role of magnetic susceptibility (χ) in deep gray matter (DGM) structures, including the putamen (PUT), globus pallidus (GP), caudate nucleus (CN), and thalamus, in the most common types of multiple sclerosis (MS) and relapsing-remitting MS (RRMS), using quantitative susceptibility mapping (QSM). METHODS The literature was systematically reviewed up to November 2023, adhering to PRISMA guidelines. This study was conducted using a random-effects model to calculate the standardized mean difference (SMD) in QSM values between patients with RRMS and healthy controls (HCs). Publication bias and risk of bias were also assessed. RESULTS Nine studies involving 1074 RRMS patients with RRMS and 640 HCs were included in the meta-analysis. The results showed significantly higher QSM (χ) values in the PUT (SMD = 0.40, 95% confidence interval [CI] = 0.22-0.59, p = .000), GP (SMD = 0.60, 95% CI = 0.50-0.70, p = .00), and CN (SMD = 0.40, 95% CI = 0.15-0.66, p = .005) of RRMS patients compared to HCs. However, there were no significant differences in the QSM values in the thalamus between patients with RRMS and HCs (SMD = -0.33, 95% CI -0.67-0.01, p = .026). Age- and sex-based subgroup analysis demonstrated that younger patients (< 40 years) in the PUT, GP, and CN groups and larger male populations (> 25%) in the PUT and GP groups had more significant χ. Interestingly, thalamic QSM values were found to decrease in RRMS patients over 40 years of age and in higher male populations. Sex-based subgroup analysis indicated higher iron levels in the PUT and GP of RRMS patients regardless of sex. QSM values were higher in certain brain regions (PUT, GP, and CN) during the early stages (disease duration < 9.6 years) of RRMS, but lower in the thalamus during the later stages (disease duration > 9.6 years) than HCs. DISCUSSION/CONCLUSION QSM may serve as a biomarker for understanding χ value alterations such as iron dysregulation and its contribution to neurodegeneration in RRMS, especially in the basal ganglia nuclei including PUT, GP, and CN.
Collapse
Affiliation(s)
- Sana Mohammadi
- Neuromuscular Research Center, Department of Neurology, Shariati HospitalTehran University of Medical SciencesTehranIran
| | - Sadegh Ghaderi
- Neuromuscular Research Center, Department of Neurology, Shariati HospitalTehran University of Medical SciencesTehranIran
- Department of Neuroscience and Addiction Studies, School of Advanced Technologies in MedicineTehran University of Medical SciencesTehranIran
| | - Farzad Fatehi
- Neuromuscular Research Center, Department of Neurology, Shariati HospitalTehran University of Medical SciencesTehranIran
- Neurology DepartmentUniversity Hospitals of Leicester NHS TrustLeicesterUK
| |
Collapse
|
7
|
Mohammadi S, Ghaderi S, Fatehi F. Iron accumulation/overload and Alzheimer's disease risk factors in the precuneus region: A comprehensive narrative review. Aging Med (Milton) 2024; 7:649-667. [PMID: 39507230 PMCID: PMC11535174 DOI: 10.1002/agm2.12363] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/14/2024] [Accepted: 09/25/2024] [Indexed: 11/08/2024] Open
Abstract
Alzheimer's disease (AD) is a neurodegenerative disease that is characterized by amyloid plaques, neurofibrillary tangles, and neuronal loss. Early cerebral and body iron dysregulation and accumulation interact with AD pathology, particularly in the precuneus, a crucial functional hub in cognitive functions. Quantitative susceptibility mapping (QSM), a novel post-processing approach, provides insights into tissue iron levels and cerebral oxygen metabolism and reveals abnormal iron accumulation early in AD. Increased iron deposition in the precuneus can lead to oxidative stress, neuroinflammation, and accelerated neurodegeneration. Metabolic disorders (diabetes, non-alcoholic fatty liver disease (NAFLD), and obesity), genetic factors, and small vessel pathology contribute to abnormal iron accumulation in the precuneus. Therefore, in line with the growing body of literature in the precuneus region of patients with AD, QSM as a neuroimaging method could serve as a non-invasive biomarker to track disease progression, complement other imaging modalities, and aid in early AD diagnosis and monitoring.
Collapse
Affiliation(s)
- Sana Mohammadi
- Neuromuscular Research Center, Department of Neurology, Shariati HospitalTehran University of Medical SciencesTehranIran
| | - Sadegh Ghaderi
- Neuromuscular Research Center, Department of Neurology, Shariati HospitalTehran University of Medical SciencesTehranIran
- Department of Neuroscience and Addiction Studies, School of Advanced Technologies in MedicineTehran University of Medical SciencesTehranIran
| | - Farzad Fatehi
- Neuromuscular Research Center, Department of Neurology, Shariati HospitalTehran University of Medical SciencesTehranIran
- Neurology DepartmentUniversity Hospitals of Leicester NHS TrustLeicesterUK
| |
Collapse
|
8
|
Sandgaard AD, Shemesh N, Østergaard L, Kiselev VG, Jespersen SN. The Larmor frequency shift of a white matter magnetic microstructure model with multiple sources. NMR IN BIOMEDICINE 2024; 37:e5150. [PMID: 38553824 DOI: 10.1002/nbm.5150] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Received: 11/16/2023] [Revised: 02/15/2024] [Accepted: 02/28/2024] [Indexed: 07/11/2024]
Abstract
Magnetic susceptibility imaging may provide valuable information about chemical composition and microstructural organization of tissue. However, its estimation from the MRI signal phase is particularly difficult as it is sensitive to magnetic tissue properties ranging from the molecular to the macroscopic scale. The MRI Larmor frequency shift measured in white matter (WM) tissue depends on the myelinated axons and other magnetizable sources such as iron-filled ferritin. We have previously derived the Larmor frequency shift arising from a dense medium of cylinders with scalar susceptibility and arbitrary orientation dispersion. Here, we extend our model to include microscopic WM susceptibility anisotropy as well as spherical inclusions with scalar susceptibility to represent subcellular structures, biologically stored iron, and so forth. We validate our analytical results with computer simulations and investigate the feasibility of estimating susceptibility using simple iterative linear least squares without regularization or preconditioning. This is done in a digital brain phantom synthesized from diffusion MRI measurements of an ex vivo mouse brain at ultra-high field.
Collapse
Affiliation(s)
- Anders Dyhr Sandgaard
- Center of Functionally Integrative Neuroscience, Department of Clinical Medicine, Aarhus University, Aarhus, Denmark
| | - Noam Shemesh
- Champalimaud Research, Champalimaud Centre for the Unknown, Lisbon, Portugal
| | - Leif Østergaard
- Center of Functionally Integrative Neuroscience, Department of Clinical Medicine, Aarhus University, Aarhus, Denmark
| | - Valerij G Kiselev
- Division of Medical Physics, Department of Radiology, University Medical Center Freiburg, Freiburg, Germany
| | - Sune Nørhøj Jespersen
- Center of Functionally Integrative Neuroscience, Department of Clinical Medicine, Aarhus University, Aarhus, Denmark
- Department of Physics and Astronomy, Aarhus University, Aarhus, Denmark
| |
Collapse
|
9
|
Schumacher K, Prince MR, Blumenfeld JD, Rennert H, Hu Z, Dev H, Wang Y, Dimov AV. Quantitative susceptibility mapping for detection of kidney stones, hemorrhage differentiation, and cyst classification in ADPKD. Abdom Radiol (NY) 2024; 49:2285-2295. [PMID: 38530430 DOI: 10.1007/s00261-024-04243-6] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/27/2023] [Revised: 02/06/2024] [Accepted: 02/07/2024] [Indexed: 03/28/2024]
Abstract
BACKGROUND AND PURPOSE The objective is to demonstrate feasibility of quantitative susceptibility mapping (QSM) in autosomal dominant polycystic kidney disease (ADPKD) patients and to compare imaging findings with traditional T1/T2w magnetic resonance imaging (MRI). METHODS Thirty-three consecutive patients (11 male, 22 female) diagnosed with ADPKD were initially selected. QSM images were reconstructed from the multiecho gradient echo data and compared to co-registered T2w, T1w, and CT images. Complex cysts were identified and classified into distinct subclasses based on their imaging features. Prevalence of each subclass was estimated. RESULTS QSM visualized two renal calcifications measuring 9 and 10 mm and three pelvic phleboliths measuring 2 mm but missed 24 calcifications measuring 1 mm or less and 1 larger calcification at the edge of the field of view. A total of 121 complex T1 hyperintense/T2 hypointense renal cysts were detected. 52 (43%) Cysts appeared hyperintense on QSM consistent with hemorrhage; 60 (49%) cysts were isointense with respect to simple cysts and normal kidney parenchyma, while the remaining 9 (7%) were hypointense. The presentation of the latter two complex cyst subtypes is likely indicative of proteinaceous composition without hemorrhage. CONCLUSION Our results indicate that QSM of ADPKD kidneys is possible and uniquely suited to detect large renal calculi without ionizing radiation and able to identify properties of complex cysts unattainable with traditional approaches.
Collapse
Affiliation(s)
- Karl Schumacher
- Department of Bioengineering, Santa Clara University, Santa Clara, CA, USA
- Department of Radiology, Weill Cornell Medicine, New York, NY, USA
| | - Martin R Prince
- Department of Radiology, Weill Cornell Medicine, New York, NY, USA
| | - Jon D Blumenfeld
- The Rogosin Institute, New York, NY, USA
- Department of Medicine, Weill Cornell Medicine, New York, NY, USA
| | - Hanna Rennert
- Department of Pathology, Weill Cornell Medicine, New York, NY, USA
| | - Zhongxiu Hu
- Department of Radiology, Weill Cornell Medicine, New York, NY, USA
| | - Hreedi Dev
- Department of Radiology, Weill Cornell Medicine, New York, NY, USA
| | - Yi Wang
- Department of Radiology, Weill Cornell Medicine, New York, NY, USA
| | - Alexey V Dimov
- Department of Radiology, Weill Cornell Medicine, New York, NY, USA.
| |
Collapse
|
10
|
Bilgic B, Costagli M, Chan KS, Duyn J, Langkammer C, Lee J, Li X, Liu C, Marques JP, Milovic C, Robinson SD, Schweser F, Shmueli K, Spincemaille P, Straub S, van Zijl P, Wang Y. Recommended implementation of quantitative susceptibility mapping for clinical research in the brain: A consensus of the ISMRM electro-magnetic tissue properties study group. Magn Reson Med 2024; 91:1834-1862. [PMID: 38247051 PMCID: PMC10950544 DOI: 10.1002/mrm.30006] [Citation(s) in RCA: 28] [Impact Index Per Article: 28.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/11/2023] [Revised: 10/31/2023] [Accepted: 12/14/2023] [Indexed: 01/23/2024]
Abstract
This article provides recommendations for implementing QSM for clinical brain research. It is a consensus of the International Society of Magnetic Resonance in Medicine, Electro-Magnetic Tissue Properties Study Group. While QSM technical development continues to advance rapidly, the current QSM methods have been demonstrated to be repeatable and reproducible for generating quantitative tissue magnetic susceptibility maps in the brain. However, the many QSM approaches available have generated a need in the neuroimaging community for guidelines on implementation. This article outlines considerations and implementation recommendations for QSM data acquisition, processing, analysis, and publication. We recommend that data be acquired using a monopolar 3D multi-echo gradient echo (GRE) sequence and that phase images be saved and exported in Digital Imaging and Communications in Medicine (DICOM) format and unwrapped using an exact unwrapping approach. Multi-echo images should be combined before background field removal, and a brain mask created using a brain extraction tool with the incorporation of phase-quality-based masking. Background fields within the brain mask should be removed using a technique based on SHARP or PDF, and the optimization approach to dipole inversion should be employed with a sparsity-based regularization. Susceptibility values should be measured relative to a specified reference, including the common reference region of the whole brain as a region of interest in the analysis. The minimum acquisition and processing details required when reporting QSM results are also provided. These recommendations should facilitate clinical QSM research and promote harmonized data acquisition, analysis, and reporting.
Collapse
Affiliation(s)
- Berkin Bilgic
- Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Charlestown, Massachusetts, USA
| | - Mauro Costagli
- Department of Neuroscience, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Sciences (DINOGMI), University of Genoa, Genoa, Italy
- Laboratory of Medical Physics and Magnetic Resonance, IRCCS Stella Maris, Pisa, Italy
| | - Kwok-Shing Chan
- Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Charlestown, Massachusetts, USA
- Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, The Netherlands
| | - Jeff Duyn
- Advanced MRI Section, NINDS, National Institutes of Health, Bethesda, Maryland, USA
| | | | - Jongho Lee
- Department of Electrical and Computer Engineering, Seoul National University, Seoul, Republic of Korea
| | - Xu Li
- Russell H. Morgan Department of Radiology and Radiological Science, Johns Hopkins University School of Medicine, Baltimore, Maryland, USA
- F.M. Kirby Research Center for Functional Brain Imaging, Kennedy Krieger Institute, Baltimore, Maryland, USA
| | - Chunlei Liu
- Department of Electrical Engineering and Computer Sciences, University of California, Berkeley, California, USA
- Helen Wills Neuroscience Institute, University of California, Berkeley, California, USA
| | - José P Marques
- Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, The Netherlands
| | - Carlos Milovic
- School of Electrical Engineering (EIE), Pontificia Universidad Catolica de Valparaiso, Valparaiso, Chile
| | - Simon Daniel Robinson
- High Field MR Centre, Department of Biomedical Imaging and Image-Guided Therapy, Medical University of Vienna, Vienna, Austria
- Centre of Advanced Imaging, University of Queensland, Brisbane, Australia
| | - Ferdinand Schweser
- Buffalo Neuroimaging Analysis Center, Department of Neurology, Jacobs School of Medicine and Biomedical Sciences at the University at Buffalo, Buffalo, New York, USA
- Center for Biomedical Imaging, Clinical and Translational Science Institute at the University at Buffalo, Buffalo, New York, USA
| | - Karin Shmueli
- Department of Medical Physics and Biomedical Engineering, University College London, London, UK
| | - Pascal Spincemaille
- MRI Research Institute, Department of Radiology, Weill Cornell Medicine, New York, New York, USA
| | - Sina Straub
- Department of Radiology, Mayo Clinic, Jacksonville, Florida, USA
| | - Peter van Zijl
- Russell H. Morgan Department of Radiology and Radiological Science, Johns Hopkins University School of Medicine, Baltimore, Maryland, USA
- F.M. Kirby Research Center for Functional Brain Imaging, Kennedy Krieger Institute, Baltimore, Maryland, USA
| | - Yi Wang
- MRI Research Institute, Departments of Radiology and Biomedical Engineering, Cornell University, New York, New York, USA
| |
Collapse
|
11
|
Mohammadi S, Ghaderi S. Parkinson's disease and Parkinsonism syndromes: Evaluating iron deposition in the putamen using magnetic susceptibility MRI techniques - A systematic review and literature analysis. Heliyon 2024; 10:e27950. [PMID: 38689949 PMCID: PMC11059419 DOI: 10.1016/j.heliyon.2024.e27950] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/10/2023] [Revised: 02/29/2024] [Accepted: 03/08/2024] [Indexed: 05/02/2024] Open
Abstract
Magnetic resonance imaging (MRI) techniques, such as quantitative susceptibility mapping (QSM) and susceptibility-weighted imaging (SWI), can detect iron deposition in the brain. Iron accumulation in the putamen (PUT) can contribute to the pathogenesis of Parkinson's disease (PD) and atypical Parkinsonian disorders. This systematic review aimed to synthesize evidence on iron deposition in the PUT assessed by MRI susceptibility techniques in PD and Parkinsonism syndromes. The PubMed and Scopus databases were searched for relevant studies. Thirty-four studies from January 2007 to October 2023 that used QSM, SWI, or other MRI susceptibility methods to measure putaminal iron in PD, progressive supranuclear palsy (PSP), multiple system atrophy (MSA), and healthy controls (HCs) were included. Most studies have found increased putaminal iron levels in PD patients versus HCs based on higher quantitative susceptibility. Putaminal iron accumulation correlates with worse motor scores and cognitive decline in patients with PD. Evidence regarding differences in susceptibility between PD and atypical Parkinsonism is emerging, with several studies showing greater putaminal iron deposition in PSP and MSA than in PD patients. Alterations in putaminal iron levels help to distinguish these disorders from PD. Increased putaminal iron levels appear to be associated with increased disease severity and progression. Thus, magnetic susceptibility MRI techniques can detect abnormal iron accumulation in the PUT of patients with Parkinsonism. Moreover, quantifying putaminal susceptibility may serve as an MRI biomarker to monitor motor and cognitive changes in PD and aid in the differential diagnosis of Parkinsonian disorders.
Collapse
Affiliation(s)
- Sana Mohammadi
- Department of Medical Sciences, School of Medicine, Iran University of Medical Sciences, Tehran, Iran
| | - Sadegh Ghaderi
- Department of Neuroscience and Addiction Studies, School of Advanced Technologies in Medicine, Tehran University of Medical Sciences, Tehran, Iran
| |
Collapse
|
12
|
Liu M, Zhao S, Chen Z. Interscanner reproducibility of volumetric quantitative susceptibility mapping about cerebral subcortical gray nuclei at different MR vendors with the same magnetic strength. Brain Behav 2024; 14:e3473. [PMID: 38594225 PMCID: PMC11004039 DOI: 10.1002/brb3.3473] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 12/12/2023] [Revised: 03/05/2024] [Accepted: 03/16/2024] [Indexed: 04/11/2024] Open
Abstract
BACKGROUND AND PURPOSE Quantitative susceptibility mapping (QSM) technique was a new quantitative magnetic resonance imaging technique to evaluate the cerebral iron deposition in clinical practice. The current study was aimed to investigate the reproducibility of the volumetric susceptibility value of the subcortical gray nuclei at two different MR vendor with the same magnetic strength. METHODS Cerebral magnitude and phase images of 21 normal subjects were acquired from a 3D multiecho enhanced gradient recalled echo sequence at two different 3.0T MR scanner, and then the magnetic susceptibility images were generated by STI software. The brain structural images were coregistered with magnitude images and generated the normalized parameters, and then generated the normalized susceptibility images. The subcortical gray nuclei template was applied to extract the volumetric susceptibility value of the target nuclei. RESULTS ICC value (95% CI) of the caudate, putamen and GP were 0.847 (0.660-0.935), 0.848 (0.663-0.935) and 0.838 (0.643-0.931), respectively. The ICC value of the thalamus was 0.474 (0.064-0.747). Ninety-five point two percent (20/21) of the difference points of the susceptibility located between the 95% LA for the caudate at the two different 3.0T MR scanner, while the less than 95% of the difference points of the susceptibility value located between the 95% LA for the putamen, globus pallidus and thalamus. CONCLUSION The current study identified that the caudate had the stable reproducibility of the magnetic susceptibility value, and the other basal ganglion nuclei should be cautious for the quantitative evaluation of the magnetic susceptibility value at different 3.0T MR scanner.
Collapse
Affiliation(s)
- Mengqi Liu
- Department of RadiologyHainan Hospital of PLA General HospitalSanyaChina
- Department of RadiologyFirst Medical Center of PLA General HospitalBeijingChina
| | - Shuqiang Zhao
- Department of RadiologyHainan Hospital of PLA General HospitalSanyaChina
| | - Zhiye Chen
- Department of RadiologyHainan Hospital of PLA General HospitalSanyaChina
| |
Collapse
|
13
|
Sandgaard AD, Kiselev VG, Henriques RN, Shemesh N, Jespersen SN. Incorporating the effect of white matter microstructure in the estimation of magnetic susceptibility in ex vivo mouse brain. Magn Reson Med 2024; 91:699-715. [PMID: 37772624 DOI: 10.1002/mrm.29867] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/01/2023] [Revised: 08/07/2023] [Accepted: 08/25/2023] [Indexed: 09/30/2023]
Abstract
PURPOSE To extend quantitative susceptibility mapping to account for microstructure of white matter (WM) and demonstrate its effect on ex vivo mouse brain at 16.4T. THEORY AND METHODS Previous studies have shown that the MRI measured Larmor frequency also depends on local magnetic microstructure at the mesoscopic scale. Here, we include effects from WM microstructure using our previous results for the mesoscopic Larmor frequencyΩ ‾ Meso $$ {\overline{\Omega}}^{\mathrm{Meso}} $$ of cylinders with arbitrary orientations. We scrutinize the validity of our model and QSM in a digital brain phantom includingΩ ‾ Meso $$ {\overline{\Omega}}^{\mathrm{Meso}} $$ from a WM susceptibility tensor and biologically stored iron with scalar susceptibility. We also apply susceptibility tensor imaging to the phantom and investigate how the fitted tensors are biased fromΩ ‾ Meso $$ {\overline{\Omega}}^{\mathrm{Meso}} $$ . Last, we demonstrate how to combine multi-gradient echo and diffusion MRI images of ex vivo mouse brains acquired at 16.4T to estimate an apparent scalar susceptibility without sample rotations. RESULTS Our new model improves susceptibility estimation compared to QSM for the brain phantom. Applying susceptibility tensor imaging to the phantom withΩ ‾ Meso $$ {\overline{\Omega}}^{\mathrm{Meso}} $$ from WM axons with scalar susceptibility produces a highly anisotropic susceptibility tensor that mimics results from previous susceptibility tensor imaging studies. For the ex vivo mouse brain we find theΩ ‾ Meso $$ {\overline{\Omega}}^{\mathrm{Meso}} $$ due to WM microstructure to be substantial, changing susceptibility in WM up to 25% root-mean-squared-difference. CONCLUSION Ω ‾ Meso $$ {\overline{\Omega}}^{\mathrm{Meso}} $$ impacts susceptibility estimates and biases susceptibility tensor imaging fitting substantially. Hence, it should not be neglected when imaging structurally anisotropic tissue such as brain WM.
Collapse
Affiliation(s)
- Anders Dyhr Sandgaard
- Center for Functionally Integrative Neuroscience, Department of Clinical Medicine, Aarhus University, Aarhus, Denmark
| | - Valerij G Kiselev
- Division of Medical Physics, Department of Radiology, University Medical Center Freiburg, Freiburg, Germany
| | | | - Noam Shemesh
- Champalimaud Research, Champalimaud Centre for the Unknown, Lisbon, Portugal
| | - Sune Nørhøj Jespersen
- Center for Functionally Integrative Neuroscience, Department of Clinical Medicine, Aarhus University, Aarhus, Denmark
- Department of Physics and Astronomy, Aarhus University, Aarhus, Denmark
| |
Collapse
|
14
|
Krishnan S, George SS, Radhakrishnan V, Raghavan S, Thomas B, Thulaseedharan JV, Puthenveedu DK. Quantitative susceptibility mapping from basal ganglia and related structures: correlation with disease severity in progressive supranuclear palsy. Acta Neurol Belg 2024; 124:151-160. [PMID: 37580639 DOI: 10.1007/s13760-023-02352-5] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/10/2023] [Accepted: 07/31/2023] [Indexed: 08/16/2023]
Abstract
OBJECTIVE We examined whether mean magnetic susceptibility values from deep gray matter structures in patients with progressive supranuclear palsy (PSP) differed from those in patients with Parkinson's disease (PD) and healthy volunteers, and correlated with the PSP rating scale. METHODS Head of caudate nucleus, putamen, globus pallidus, substantia nigra and red nucleus were the regions of interest. Mean susceptibility values from these regions in PSP patients were estimated using quantitative susceptibility mapping. Correlations with clinical severity of disease as measured by the PSP rating scale were examined. The mean susceptibility values were also compared with those from healthy volunteers and age- and disease duration-matched patients with PD. RESULTS Data from 26 healthy volunteers, 26 patients with PD and 27 patients with PSP, were analysed. Patients with PSP had higher mean susceptibility values from all regions of interest when compared to both the other groups. The PSP rating scale scores correlated strongly with mean susceptibility values from the red nucleus and moderately with those from the putamen and substantia nigra. The scores did not correlate with mean susceptibility values from the caudate nucleus or globus pallidus. In patients with PD, the motor deficits correlated moderately with mean susceptibility values from substantia nigra. CONCLUSIONS In patients with PSP, mean susceptibility values indicating the severity of mineralization of basal ganglia and related structures correlate with disease severity, the correlation of red nucleus being the strongest. Further studies are warranted to explore whether mean susceptibility values could serve as biomarkers for PSP.
Collapse
Affiliation(s)
- Syam Krishnan
- Comprehensive Care Centre for Movement Disorders, Sree Chitra Tirunal Institute for Medical Sciences and Technology, Thiruvananthapuram, Kerala, India.
| | - Sneha Susan George
- Comprehensive Care Centre for Movement Disorders, Sree Chitra Tirunal Institute for Medical Sciences and Technology, Thiruvananthapuram, Kerala, India
| | - Vineeth Radhakrishnan
- Comprehensive Care Centre for Movement Disorders, Sree Chitra Tirunal Institute for Medical Sciences and Technology, Thiruvananthapuram, Kerala, India
| | - Sheelakumari Raghavan
- Department of Imaging Sciences and Interventional Radiology, Sree Chitra Tirunal Institute for Medical Sciences and Technology, Thiruvananthapuram, Kerala, India
| | - Bejoy Thomas
- Department of Imaging Sciences and Interventional Radiology, Sree Chitra Tirunal Institute for Medical Sciences and Technology, Thiruvananthapuram, Kerala, India
| | - Jissa Vinoda Thulaseedharan
- Achutha Menon Centre for Health Science Studies, Sree Chitra Tirunal Institute for Medical Sciences and Technology, Thiruvananthapuram, Kerala, India
| | - Divya Kalikavil Puthenveedu
- Comprehensive Care Centre for Movement Disorders, Sree Chitra Tirunal Institute for Medical Sciences and Technology, Thiruvananthapuram, Kerala, India
| |
Collapse
|
15
|
Hage S, Kinkade S, Girard R, Flemming KD, Kim H, Torbey MT, Huang J, Huston J, Shu Y, Selwyn RG, Hart BL, Mabray MC, Feghali J, Sair HI, Narvid J, Lupo JM, Lee J, Stadnik A, Alcazar-Felix RJ, Shenkar R, Hobson N, DeBiasse D, Lane K, McBee NA, Treine K, Ostapkovich N, Wang Y, Thompson RE, Koenig JI, Carroll T, Hanley DF, Awad IA. Trial Readiness of Cavernous Malformations With Symptomatic Hemorrhage, Part II: Biomarkers and Trial Modeling. Stroke 2024; 55:31-39. [PMID: 38134265 PMCID: PMC10752356 DOI: 10.1161/strokeaha.123.044083] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/31/2023] [Revised: 09/26/2023] [Accepted: 10/12/2023] [Indexed: 12/24/2023]
Abstract
BACKGROUND Quantitative susceptibility mapping (QSM) and dynamic contrast-enhanced quantitative perfusion (DCEQP) magnetic resonance imaging sequences assessing iron deposition and vascular permeability were previously correlated with new hemorrhage in cerebral cavernous malformations. We assessed their prospective changes in a multisite trial-readiness project. METHODS Patients with cavernous malformation and symptomatic hemorrhage (SH) in the prior year, without prior or planned lesion resection or irradiation were enrolled. Mean QSM and DCEQP of the SH lesion were acquired at baseline and at 1- and 2-year follow-ups. Sensitivity and specificity of biomarker changes were analyzed in relation to predefined criteria for recurrent SH or asymptomatic change. Sample size calculations for hypothesized therapeutic effects were conducted. RESULTS We logged 143 QSM and 130 DCEQP paired annual assessments. Annual QSM change was greater in cases with SH than in cases without SH (P=0.019). Annual QSM increase by ≥6% occurred in 7 of 7 cases (100%) with recurrent SH and in 7 of 10 cases (70%) with asymptomatic change during the same epoch and 3.82× more frequently than clinical events. DCEQP change had lower sensitivity for SH and asymptomatic change than QSM change and greater variance. A trial with the smallest sample size would detect a 30% difference in QSM annual change during 2 years of follow-up in 34 or 42 subjects (1 and 2 tailed, respectively); power, 0.8, α=0.05. CONCLUSIONS Assessment of QSM change is feasible and sensitive to recurrent bleeding in cavernous malformations. Evaluation of an intervention on QSM percent change may be used as a time-averaged difference between 2 arms using a repeated measures analysis. DCEQP change is associated with lesser sensitivity and higher variability than QSM. These results are the basis of an application for certification by the US Food and Drug Administration of QSM as a biomarker of drug effect on bleeding in cavernous malformations. REGISTRATION URL: https://www.clinicaltrials.gov; Unique identifier: NCT03652181.
Collapse
Affiliation(s)
- Stephanie Hage
- Neurovascular Surgery Program, Department of Neurological Surgery (S.H., S.K., R.G., J.L., A.S., R.J.A.-F., R.S., N.H., D.D., I.A.A.), University of Chicago Medicine and Biological Sciences, IL
| | - Serena Kinkade
- Neurovascular Surgery Program, Department of Neurological Surgery (S.H., S.K., R.G., J.L., A.S., R.J.A.-F., R.S., N.H., D.D., I.A.A.), University of Chicago Medicine and Biological Sciences, IL
| | - Romuald Girard
- Neurovascular Surgery Program, Department of Neurological Surgery (S.H., S.K., R.G., J.L., A.S., R.J.A.-F., R.S., N.H., D.D., I.A.A.), University of Chicago Medicine and Biological Sciences, IL
| | | | - Helen Kim
- Department of Anesthesiology and Perioperative Care, Center for Cerebrovascular Research (H.K.), University of California, San Francisco
| | - Michel T Torbey
- Department of Neurology (M.T.T.), University of New Mexico, Albuquerque
| | | | - John Huston
- Radiology (J. Huston, Y.S.), Mayo Clinic, Rochester, MN
| | - Yunhong Shu
- Radiology (J. Huston, Y.S.), Mayo Clinic, Rochester, MN
| | - Reed G Selwyn
- Department of Diagnostic Radiology (R.G.S., B.L.H.), University of New Mexico, Albuquerque
| | - Blaine L Hart
- Department of Diagnostic Radiology (R.G.S., B.L.H.), University of New Mexico, Albuquerque
| | - Marc C Mabray
- Department of Radiology (M.C.M.), University of New Mexico, Albuquerque
| | | | - Haris I Sair
- The Russell H. Morgan Department of Radiology and Radiological Science, Johns Hopkins School of Medicine, Baltimore, MD (H.I.S.)
| | - Jared Narvid
- Department of Radiology and Biomedical Imaging (J.N., J.M.L.), University of California, San Francisco
| | - Janine M Lupo
- Department of Radiology and Biomedical Imaging (J.N., J.M.L.), University of California, San Francisco
| | - Justine Lee
- Neurovascular Surgery Program, Department of Neurological Surgery (S.H., S.K., R.G., J.L., A.S., R.J.A.-F., R.S., N.H., D.D., I.A.A.), University of Chicago Medicine and Biological Sciences, IL
| | - Agnieszka Stadnik
- Neurovascular Surgery Program, Department of Neurological Surgery (S.H., S.K., R.G., J.L., A.S., R.J.A.-F., R.S., N.H., D.D., I.A.A.), University of Chicago Medicine and Biological Sciences, IL
| | - Roberto J Alcazar-Felix
- Neurovascular Surgery Program, Department of Neurological Surgery (S.H., S.K., R.G., J.L., A.S., R.J.A.-F., R.S., N.H., D.D., I.A.A.), University of Chicago Medicine and Biological Sciences, IL
| | - Robert Shenkar
- Neurovascular Surgery Program, Department of Neurological Surgery (S.H., S.K., R.G., J.L., A.S., R.J.A.-F., R.S., N.H., D.D., I.A.A.), University of Chicago Medicine and Biological Sciences, IL
| | - Nicholas Hobson
- Neurovascular Surgery Program, Department of Neurological Surgery (S.H., S.K., R.G., J.L., A.S., R.J.A.-F., R.S., N.H., D.D., I.A.A.), University of Chicago Medicine and Biological Sciences, IL
| | - Dorothy DeBiasse
- Neurovascular Surgery Program, Department of Neurological Surgery (S.H., S.K., R.G., J.L., A.S., R.J.A.-F., R.S., N.H., D.D., I.A.A.), University of Chicago Medicine and Biological Sciences, IL
| | - Karen Lane
- Brain Injury Outcomes Unit, Department of Neurology (K.L., N.A.M., K.T., N.O., Y.W., R.E.T., D.F.H.), Johns Hopkins University Medical Institutions, Baltimore, MD
| | - Nichole A McBee
- Brain Injury Outcomes Unit, Department of Neurology (K.L., N.A.M., K.T., N.O., Y.W., R.E.T., D.F.H.), Johns Hopkins University Medical Institutions, Baltimore, MD
| | - Kevin Treine
- Brain Injury Outcomes Unit, Department of Neurology (K.L., N.A.M., K.T., N.O., Y.W., R.E.T., D.F.H.), Johns Hopkins University Medical Institutions, Baltimore, MD
| | - Noeleen Ostapkovich
- Brain Injury Outcomes Unit, Department of Neurology (K.L., N.A.M., K.T., N.O., Y.W., R.E.T., D.F.H.), Johns Hopkins University Medical Institutions, Baltimore, MD
| | - Ying Wang
- Brain Injury Outcomes Unit, Department of Neurology (K.L., N.A.M., K.T., N.O., Y.W., R.E.T., D.F.H.), Johns Hopkins University Medical Institutions, Baltimore, MD
| | - Richard E Thompson
- Brain Injury Outcomes Unit, Department of Neurology (K.L., N.A.M., K.T., N.O., Y.W., R.E.T., D.F.H.), Johns Hopkins University Medical Institutions, Baltimore, MD
| | - James I Koenig
- National Institute of Neurological Disorders and Stroke, Bethesda, MD (J.K.)
| | - Timothy Carroll
- Department of Diagnostic Radiology (T.C.), University of Chicago Medicine and Biological Sciences, IL
| | - Daniel F Hanley
- Brain Injury Outcomes Unit, Department of Neurology (K.L., N.A.M., K.T., N.O., Y.W., R.E.T., D.F.H.), Johns Hopkins University Medical Institutions, Baltimore, MD
| | - Issam A Awad
- Neurovascular Surgery Program, Department of Neurological Surgery (S.H., S.K., R.G., J.L., A.S., R.J.A.-F., R.S., N.H., D.D., I.A.A.), University of Chicago Medicine and Biological Sciences, IL
| |
Collapse
|
16
|
Kiersnowski OC, Winston GP, Caciagli L, Biondetti E, Elbadri M, Buck S, Duncan JS, Thornton JS, Shmueli K, Vos SB. Quantitative susceptibility mapping identifies hippocampal and other subcortical grey matter tissue composition changes in temporal lobe epilepsy. Hum Brain Mapp 2023; 44:5047-5064. [PMID: 37493334 PMCID: PMC10502681 DOI: 10.1002/hbm.26432] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/31/2023] [Revised: 07/04/2023] [Accepted: 07/07/2023] [Indexed: 07/27/2023] Open
Abstract
Temporal lobe epilepsy (TLE) is associated with widespread brain alterations. Using quantitative susceptibility mapping (QSM) alongside transverse relaxation rate (R 2 * ), we investigated regional brain susceptibility changes in 36 patients with left-sided (LTLE) or right-sided TLE (RTLE) secondary to hippocampal sclerosis, and 27 healthy controls (HC). We compared three susceptibility calculation methods to ensure image quality. Correlations of susceptibility andR 2 * with age of epilepsy onset, frequency of focal-to-bilateral tonic-clonic seizures (FBTCS), and neuropsychological test scores were examined. Weak-harmonic QSM (WH-QSM) successfully reduced noise and removed residual background field artefacts. Significant susceptibility increases were identified in the left putamen in the RTLE group compared to the LTLE group, the right putamen and right thalamus in the RTLE group compared to HC, and a significant susceptibility decrease in the left hippocampus in LTLE versus HC. LTLE patients who underwent epilepsy surgery showed significantly lower left-versus-right hippocampal susceptibility. SignificantR 2 * changes were found between TLE and HC groups in the amygdala, putamen, thalamus, and in the hippocampus. Specifically, decreased R2 * was found in the left and right hippocampus in LTLE and RTLE, respectively, compared to HC. Susceptibility andR 2 * were significantly correlated with cognitive test scores in the hippocampus, globus pallidus, and thalamus. FBTCS frequency correlated positively with ipsilateral thalamic and contralateral putamen susceptibility and withR 2 * in bilateral globi pallidi. Age of onset was correlated with susceptibility in the hippocampus and putamen, and withR 2 * in the caudate. Susceptibility andR 2 * changes observed in TLE groups suggest selective loss of low-myelinated neurons alongside iron redistribution in the hippocampi, predominantly ipsilaterally, indicating QSM's sensitivity to local pathology. Increased susceptibility andR 2 * in the thalamus and putamen suggest increased iron content and reflect disease severity.
Collapse
Affiliation(s)
- Oliver C. Kiersnowski
- Department of Medical Physics and Biomedical EngineeringUniversity College LondonLondonUK
| | - Gavin P. Winston
- Department of Clinical and Experimental EpilepsyUniversity College LondonLondonUK
- Department of Medicine, Division of NeurologyQueen's UniversityKingstonCanada
| | - Lorenzo Caciagli
- Department of Clinical and Experimental EpilepsyUniversity College LondonLondonUK
- Department of BioengineeringUniversity of PennsylvaniaPhiladelphiaPennsylvaniaUSA
| | - Emma Biondetti
- Department of Medical Physics and Biomedical EngineeringUniversity College LondonLondonUK
- Department of Neuroscience, Imaging and Clinical SciencesInstitute for Advanced Biomedical Technologies, “D'Annunzio” University of Chieti‐PescaraChietiItaly
| | - Maha Elbadri
- Department of NeurologyQueen Elizabeth HospitalBirminghamUK
| | - Sarah Buck
- Department of Clinical and Experimental EpilepsyUniversity College LondonLondonUK
| | - John S. Duncan
- Department of Clinical and Experimental EpilepsyUniversity College LondonLondonUK
| | - John S. Thornton
- Neuroradiological Academic UnitUCL Queen Square Institute of Neurology, University College LondonLondonUK
| | - Karin Shmueli
- Department of Medical Physics and Biomedical EngineeringUniversity College LondonLondonUK
| | - Sjoerd B. Vos
- Neuroradiological Academic UnitUCL Queen Square Institute of Neurology, University College LondonLondonUK
- Centre for Microscopy, Characterisation, and AnalysisThe University of Western AustraliaNedlandsAustralia
- Centre for Medical Image Computing, Computer Science departmentUniversity College LondonLondonUK
| |
Collapse
|
17
|
Alushaj E, Hemachandra D, Kuurstra A, Menon RS, Ganjavi H, Sharma M, Kashgari A, Barr J, Reisman W, Khan AR, MacDonald PA. Subregional analysis of striatum iron in Parkinson's disease and rapid eye movement sleep behaviour disorder. Neuroimage Clin 2023; 40:103519. [PMID: 37797434 PMCID: PMC10568416 DOI: 10.1016/j.nicl.2023.103519] [Citation(s) in RCA: 5] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/12/2023] [Revised: 09/24/2023] [Accepted: 09/26/2023] [Indexed: 10/07/2023]
Abstract
The loss of dopamine in the striatum underlies motor symptoms of Parkinson's disease (PD). Rapid eye movement sleep behaviour disorder (RBD) is considered prodromal PD and has shown similar neural changes in the striatum. Alterations in brain iron suggest neurodegeneration; however, the literature on striatal iron has been inconsistent in PD and scant in RBD. Toward clarifying pathophysiological changes in PD and RBD, and uncovering possible biomarkers, we imaged 26 early-stage PD patients, 16 RBD patients, and 39 age-matched healthy controls with 3 T MRI. We compared mean susceptibility using quantitative susceptibility mapping (QSM) in the standard striatum (caudate, putamen, and nucleus accumbens) and tractography-parcellated striatum. Diffusion MRI permitted parcellation of the striatum into seven subregions based on the cortical areas of maximal connectivity from the Tziortzi atlas. No significant differences in mean susceptibility were found in the standard striatum anatomy. For the parcellated striatum, the caudal motor subregion, the most affected region in PD, showed lower iron levels compared to healthy controls. Receiver operating characteristic curves using mean susceptibility in the caudal motor striatum showed a good diagnostic accuracy of 0.80 when classifying early-stage PD from healthy controls. This study highlights that tractography-based parcellation of the striatum could enhance sensitivity to changes in iron levels, which have not been consistent in the PD literature. The decreased caudal motor striatum iron was sufficiently sensitive to PD, but not RBD. QSM in the striatum could contribute to development of a multivariate or multimodal biomarker of early-stage PD, but further work in larger datasets is needed to confirm its utility in prodromal groups.
Collapse
Affiliation(s)
- Erind Alushaj
- Department of Neuroscience, Schulich School of Medicine and Dentistry, Western University, London, Ontario, Canada; Western Institute for Neuroscience, Western University, London, Ontario, Canada
| | - Dimuthu Hemachandra
- Robarts Research Institute, Western University, London, Ontario, Canada; School of Biomedical Engineering, Western University, London, Ontario, Canada
| | - Alan Kuurstra
- Robarts Research Institute, Western University, London, Ontario, Canada; Department of Medical Biophysics, Western University, London, Ontario, Canada
| | - Ravi S Menon
- Robarts Research Institute, Western University, London, Ontario, Canada; Department of Medical Biophysics, Western University, London, Ontario, Canada
| | - Hooman Ganjavi
- Department of Psychiatry, Western University, London, Ontario, Canada
| | - Manas Sharma
- Department of Radiology, Western University, London, Ontario, Canada; Department of Clinical Neurological Sciences, Western University, London, Ontario, Canada
| | - Alia Kashgari
- Department of Medicine, Respirology Division, Western University, London, Ontario, Canada
| | - Jennifer Barr
- Department of Psychiatry, Western University, London, Ontario, Canada
| | - William Reisman
- Department of Medicine, Respirology Division, Western University, London, Ontario, Canada
| | - Ali R Khan
- Robarts Research Institute, Western University, London, Ontario, Canada; Department of Medical Biophysics, Western University, London, Ontario, Canada
| | - Penny A MacDonald
- Western Institute for Neuroscience, Western University, London, Ontario, Canada; Department of Clinical Neurological Sciences, Western University, London, Ontario, Canada.
| |
Collapse
|
18
|
Xie F, Mao T, Tang J, Zhao L, Guo J, Lin H, Wang D, Zhou G. Evaluation of iron deposition in the motor CSTC loop of a Chinese family with paroxysmal kinesigenic dyskinesia using quantitative susceptibility mapping. Front Neurol 2023; 14:1164600. [PMID: 37483438 PMCID: PMC10358764 DOI: 10.3389/fneur.2023.1164600] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/13/2023] [Accepted: 06/12/2023] [Indexed: 07/25/2023] Open
Abstract
Introduction Previous studies have revealed structural, functional, and metabolic changes in brain regions inside the cortico-striatal-thalamo-cortical (CSTC) loop in patients with paroxysmal kinesigenic dyskinesia (PKD), whereas no quantitative susceptibility mapping (QSM)-related studies have explored brain iron deposition in these areas. Methods A total of eight familial PKD patients and 10 of their healthy family members (normal controls) were recruited and underwent QSM on a 3T magnetic resonance imaging system. Magnetic susceptibility maps were reconstructed using a multi-scale dipole inversion algorithm. Thereafter, we specifically analyzed changes in local mean susceptibility values in cortical regions and subcortical nuclei inside the motor CSTC loop. Results Compared with normal controls, PKD patients had altered brain iron levels. In the cortical gray matter area involved with the motor CSTC loop, susceptibility values were generally elevated, especially in the bilateral M1 and PMv regions. In the subcortical nuclei regions involved with the motor CSTC loop, susceptibility values were generally lower, especially in the bilateral substantia nigra regions. Conclusion Our results provide new evidence for the neuropathogenesis of PKD and suggest that an imbalance in brain iron levels may play a role in PKD.
Collapse
Affiliation(s)
- Fangfang Xie
- Department of Radiology, Xiangya Hospital, Central South University, Changsha, China
| | - Ting Mao
- Department of Radiology, Xiangya Hospital, Central South University, Changsha, China
| | - Jingyi Tang
- Department of Radiology, Xiangya Hospital, Central South University, Changsha, China
| | - Linmei Zhao
- Department of Radiology, Xiangya Hospital, Central South University, Changsha, China
| | - Jiuqing Guo
- Department of Radiology, Xiangya Hospital, Central South University, Changsha, China
| | - Huashan Lin
- Department of Pharmaceutical Diagnosis, GE Healthcare, Changsha, China
| | - Dongcui Wang
- Department of Radiology, Xiangya Hospital, Central South University, Changsha, China
- National Clinical Research Center for Geriatric Disorders, Xiangya Hospital, Central South University, Changsha, China
| | - Gaofeng Zhou
- Department of Radiology, Xiangya Hospital, Central South University, Changsha, China
- National Clinical Research Center for Geriatric Disorders, Xiangya Hospital, Central South University, Changsha, China
| |
Collapse
|
19
|
Wang Y, He N, Zhang C, Zhang Y, Wang C, Huang P, Jin Z, Li Y, Cheng Z, Liu Y, Wang X, Chen C, Cheng J, Liu F, Haacke EM, Chen S, Yang G, Yan F. An automatic interpretable deep learning pipeline for accurate Parkinson's disease diagnosis using quantitative susceptibility mapping and T1-weighted images. Hum Brain Mapp 2023. [PMID: 37335041 PMCID: PMC10365226 DOI: 10.1002/hbm.26399] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/27/2022] [Revised: 05/11/2023] [Accepted: 06/02/2023] [Indexed: 06/21/2023] Open
Abstract
Parkinson's disease (PD) diagnosis based on magnetic resonance imaging (MRI) is still challenging clinically. Quantitative susceptibility maps (QSM) can potentially provide underlying pathophysiological information by detecting the iron distribution in deep gray matter (DGM) nuclei. We hypothesized that deep learning (DL) could be used to automatically segment all DGM nuclei and use relevant features for a better differentiation between PD and healthy controls (HC). In this study, we proposed a DL-based pipeline for automatic PD diagnosis based on QSM and T1-weighted (T1W) images. This consists of (1) a convolutional neural network model integrated with multiple attention mechanisms which simultaneously segments caudate nucleus, globus pallidus, putamen, red nucleus, and substantia nigra from QSM and T1W images, and (2) an SE-ResNeXt50 model with an anatomical attention mechanism, which uses QSM data and the segmented nuclei to distinguish PD from HC. The mean dice values for segmentation of the five DGM nuclei are all >0.83 in the internal testing cohort, suggesting that the model could segment brain nuclei accurately. The proposed PD diagnosis model achieved area under the the receiver operating characteristic curve (AUCs) of 0.901 and 0.845 on independent internal and external testing cohorts, respectively. Gradient-weighted class activation mapping (Grad-CAM) heatmaps were used to identify contributing nuclei for PD diagnosis on patient level. In conclusion, the proposed approach can potentially be used as an automatic, explainable pipeline for PD diagnosis in a clinical setting.
Collapse
Affiliation(s)
- Yida Wang
- Shanghai Key Laboratory of Magnetic Resonance, East China Normal University, Shanghai, China
| | - Naying He
- Department of Radiology, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China
| | - Chunyan Zhang
- Department of MRI, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan, China
| | - Youmin Zhang
- Department of Radiology, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China
| | - Chenglong Wang
- Shanghai Key Laboratory of Magnetic Resonance, East China Normal University, Shanghai, China
| | - Pei Huang
- Department of Neurology, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China
| | - Zhijia Jin
- Department of Radiology, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China
| | - Yan Li
- Department of Radiology, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China
| | - Zenghui Cheng
- Department of Radiology, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China
| | - Yu Liu
- Department of Radiology, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China
| | - Xinhui Wang
- Department of Radiology, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China
| | - Chen Chen
- Department of MRI, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan, China
| | - Jingliang Cheng
- Department of MRI, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan, China
| | - Fangtao Liu
- Department of Radiology, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China
| | - Ewart Mark Haacke
- Department of Radiology, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China
- Department of Biomedical Engineering, Wayne State University, Detroit, Michigan, USA
| | - Shengdi Chen
- Department of Neurology, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China
| | - Guang Yang
- Shanghai Key Laboratory of Magnetic Resonance, East China Normal University, Shanghai, China
- Institute of Brain and Education Innovation, East China Normal University, Shanghai, China
- Shanghai Center for Brain Science and Brain-Inspired Technology, Shanghai, China
| | - Fuhua Yan
- Department of Radiology, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China
| |
Collapse
|
20
|
Hage S, Kinkade S, Girard R, Flemming KD, Kim H, Torbey MT, Huang J, Huston J, Shu Y, Selwyn RG, Hart BL, Mabray MC, Feghali J, Sair HI, Narvid J, Lupo JM, Lee J, Stadnik A, Alcazar R, Shenkar R, Hobson N, DeBiasse D, Lane K, McBee N, Treine K, Ostapkovich N, Wang Y, Thompson RE, Mendoza-Puccini C, Koenig J, Carroll T, Hanley DF, Awad IA. Cavernous Angioma Symptomatic Hemorrhage (CASH) Trial Readiness II: Imaging Biomarkers and Trial Modeling. MEDRXIV : THE PREPRINT SERVER FOR HEALTH SCIENCES 2023:2023.06.01.23290854. [PMID: 37333396 PMCID: PMC10275015 DOI: 10.1101/2023.06.01.23290854] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 06/20/2023]
Abstract
Background Quantitative susceptibility mapping (QSM) and dynamic contrast enhanced quantitative perfusion (DCEQP) MRI sequences assessing iron deposition and vascular permeability were previously correlated with new hemorrhage in cavernous angiomas. We assessed their prospective changes in cavernous angiomas with symptomatic hemorrhage (CASH) in a multisite trial readiness project ( clinicaltrials.gov NCT03652181 ). Methods Patients with CASH in the prior year, without prior or planned lesion resection or irradiation were enrolled. Mean QSM and DCEQP of CASH lesion were acquired at baseline, and at 1- and 2-year follow-ups. Sensitivity and specificity of biomarker changes were analyzed in relation to predefined lesional symptomatic hemorrhage (SH) or asymptomatic change (AC). Sample size calculations for hypothesized therapeutic effects were conducted. Results We logged 143 QSM and 130 DCEQP paired annual assessments. Annual QSM change was greater in cases with SH than in cases without SH (p= 0.019). Annual QSM increase by ≥ 6% occurred in 7 of 7 cases (100%) with recurrent SH and in 7 of 10 cases (70%) with AC during the same epoch, and 3.82 times more frequently than clinical events. DCEQP change had lower sensitivity for SH and AC than QSM change, and greater variance. A trial with smallest sample size would detect a 30% difference in QSM annual change in 34 or 42 subjects (one and two-tailed, respectively), power 0.8, alpha 0.05. Conclusions Assessment of QSM change is feasible and sensitive to recurrent bleeding in CASH. Evaluation of an intervention on QSM percent change may be used as a time-averaged difference between 2 arms using a repeated measures analysis. DCEQP change is associated with lesser sensitivity and higher variability than QSM. These results are the basis of an application for certification by the U.S. F.D.A. of QSM as a biomarker of drug effect in CASH.
Collapse
|
21
|
Dimov AV, Li J, Nguyen TD, Roberts AG, Spincemaille P, Straub S, Zun Z, Prince MR, Wang Y. QSM Throughout the Body. J Magn Reson Imaging 2023; 57:1621-1640. [PMID: 36748806 PMCID: PMC10192074 DOI: 10.1002/jmri.28624] [Citation(s) in RCA: 8] [Impact Index Per Article: 4.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/15/2022] [Revised: 01/19/2023] [Accepted: 01/20/2023] [Indexed: 02/08/2023] Open
Abstract
Magnetic materials in tissue, such as iron, calcium, or collagen, can be studied using quantitative susceptibility mapping (QSM). To date, QSM has been overwhelmingly applied in the brain, but is increasingly utilized outside the brain. QSM relies on the effect of tissue magnetic susceptibility sources on the MR signal phase obtained with gradient echo sequence. However, in the body, the chemical shift of fat present within the region of interest contributes to the MR signal phase as well. Therefore, correcting for the chemical shift effect by means of water-fat separation is essential for body QSM. By employing techniques to compensate for cardiac and respiratory motion artifacts, body QSM has been applied to study liver iron and fibrosis, heart chamber blood and placenta oxygenation, myocardial hemorrhage, atherosclerotic plaque, cartilage, bone, prostate, breast calcification, and kidney stone.
Collapse
Affiliation(s)
- Alexey V. Dimov
- Department of Radiology, Weill Cornell Medicine, New York, NY, United States
| | - Jiahao Li
- Department of Radiology, Weill Cornell Medicine, New York, NY, United States
| | - Thanh D. Nguyen
- Department of Radiology, Weill Cornell Medicine, New York, NY, United States
| | | | - Pascal Spincemaille
- Department of Radiology, Weill Cornell Medicine, New York, NY, United States
| | - Sina Straub
- Department of Radiology, Mayo Clinic, Jacksonville, FL, United States
| | - Zungho Zun
- Department of Radiology, Weill Cornell Medicine, New York, NY, United States
| | - Martin R. Prince
- Department of Radiology, Weill Cornell Medicine, New York, NY, United States
| | - Yi Wang
- Department of Radiology, Weill Cornell Medicine, New York, NY, United States
| |
Collapse
|
22
|
Kiersnowski OC, Karsa A, Wastling SJ, Thornton JS, Shmueli K. Investigating the effect of oblique image acquisition on the accuracy of QSM and a robust tilt correction method. Magn Reson Med 2023; 89:1791-1808. [PMID: 36480002 PMCID: PMC10953050 DOI: 10.1002/mrm.29550] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/23/2022] [Revised: 10/28/2022] [Accepted: 11/16/2022] [Indexed: 12/13/2022]
Abstract
PURPOSE Quantitative susceptibility mapping (QSM) is used increasingly for clinical research where oblique image acquisition is commonplace, but its effects on QSM accuracy are not well understood. THEORY AND METHODS The QSM processing pipeline involves defining the unit magnetic dipole kernel, which requires knowledge of the direction of the main magnetic fieldB ^ 0 $$ {\hat{\boldsymbol{B}}}_{\mathbf{0}} $$ with respect to the acquired image volume axes. The direction ofB ^ 0 $$ {\hat{\boldsymbol{B}}}_{\mathbf{0}} $$ is dependent on the axis and angle of rotation in oblique acquisition. Using both a numerical brain phantom and in vivo acquisitions in 5 healthy volunteers, we analyzed the effects of oblique acquisition on magnetic susceptibility maps. We compared three tilt-correction schemes at each step in the QSM pipeline: phase unwrapping, background field removal and susceptibility calculation, using the RMS error and QSM-tuned structural similarity index. RESULTS Rotation of wrapped phase images gave severe artifacts. Background field removal with projection onto dipole fields gave the most accurate susceptibilities when the field map was first rotated into alignment withB ^ 0 $$ {\hat{\boldsymbol{B}}}_{\mathbf{0}} $$ . Laplacian boundary value and variable-kernel sophisticated harmonic artifact reduction for phase data background field removal methods gave accurate results without tilt correction. For susceptibility calculation, thresholded k-space division, iterative Tikhonov regularization, and weighted linear total variation regularization, all performed most accurately when local field maps were rotated into alignment withB ^ 0 $$ {\hat{\boldsymbol{B}}}_{\mathbf{0}} $$ before susceptibility calculation. CONCLUSION For accurate QSM, oblique acquisition must be taken into account. Rotation of images into alignment withB ^ 0 $$ {\hat{\boldsymbol{B}}}_{\mathbf{0}} $$ should be carried out after phase unwrapping and before background-field removal. We provide open-source tilt-correction code to incorporate easily into existing pipelines: https://github.com/o-snow/QSM_TiltCorrection.git.
Collapse
Affiliation(s)
- Oliver C. Kiersnowski
- Department of Medical Physics and Biomedical EngineeringUniversity College LondonLondonUnited Kingdom
| | - Anita Karsa
- Department of Medical Physics and Biomedical EngineeringUniversity College LondonLondonUnited Kingdom
| | - Stephen J. Wastling
- Neuroradiological Academic UnitUCL Queen Square Institute of NeurologyLondonUnited Kingdom
- Lysholm Department of NeuroradiologyNational Hospital for Neurology and NeurosurgeryLondonUnited Kingdom
| | - John S. Thornton
- Neuroradiological Academic UnitUCL Queen Square Institute of NeurologyLondonUnited Kingdom
- Lysholm Department of NeuroradiologyNational Hospital for Neurology and NeurosurgeryLondonUnited Kingdom
| | - Karin Shmueli
- Department of Medical Physics and Biomedical EngineeringUniversity College LondonLondonUnited Kingdom
| |
Collapse
|
23
|
Perosa V, Rotta J, Yakupov R, Kuijf HJ, Schreiber F, Oltmer JT, Mattern H, Heinze HJ, Düzel E, Schreiber S. Implications of quantitative susceptibility mapping at 7 Tesla MRI for microbleeds detection in cerebral small vessel disease. Front Neurol 2023; 14:1112312. [PMID: 37006483 PMCID: PMC10050564 DOI: 10.3389/fneur.2023.1112312] [Citation(s) in RCA: 3] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/30/2022] [Accepted: 02/20/2023] [Indexed: 03/17/2023] Open
Abstract
BackgroundCerebral microbleeds (MBs) are a hallmark of cerebral small vessel disease (CSVD) and can be found on T2*-weighted sequences on MRI. Quantitative susceptibility mapping (QSM) is a postprocessing method that also enables MBs identification and furthermore allows to differentiate them from calcifications.AimsWe explored the implications of using QSM at submillimeter resolution for MBs detection in CSVD.MethodsBoth 3 and 7 Tesla (T) MRI were performed in elderly participants without MBs and patients with CSVD. MBs were quantified on T2*-weighted imaging and QSM. Differences in the number of MBs were assessed, and subjects were classified in CSVD subgroups or controls both on 3T T2*-weighted imaging and 7T QSM.Results48 participants [mean age (SD) 70.9 (8.8) years, 48% females] were included: 31 were healthy controls, 6 probable cerebral amyloid angiopathy (CAA), 9 mixed CSVD, and 2 were hypertensive arteriopathy [HA] patients. After accounting for the higher number of MBs detected at 7T QSM (Median = Mdn; Mdn7T−QSM = 2.5; Mdn3T−T2 = 0; z = 4.90; p < 0.001) and false positive MBs (6.1% calcifications), most healthy controls (80.6%) demonstrated at least one MB and more MBs were discovered in the CSVD group.ConclusionsOur observations suggest that QSM at submillimeter resolution improves the detection of MBs in the elderly human brain. A higher prevalence of MBs than so far known in healthy elderly was revealed.
Collapse
Affiliation(s)
- Valentina Perosa
- J. Philip Kistler Stroke Research Center, Massachusetts General Hospital, Boston, MA, United States
- *Correspondence: Valentina Perosa
| | - Johanna Rotta
- Department of Neurology, Otto-von-Guericke University, Magdeburg, Germany
| | - Renat Yakupov
- Institute of Cognitive Neurology and Dementia Research (IKND), Magdeburg, Germany
- German Center for Neurodegenerative Diseases (DZNE), Magdeburg, Germany
| | - Hugo J. Kuijf
- Image Sciences Institute, University Medical Center Utrecht, Utrecht, Netherlands
| | - Frank Schreiber
- Department of Neurology, Otto-von-Guericke University, Magdeburg, Germany
- German Center for Neurodegenerative Diseases (DZNE), Magdeburg, Germany
| | - Jan T. Oltmer
- Athinoula A. Martinos Center, Massachusetts General Hospital, Department of Radiology, Boston, MA, United States
| | - Hendrik Mattern
- German Center for Neurodegenerative Diseases (DZNE), Magdeburg, Germany
- Institute of Physics, Otto-von-Guericke University, Magdeburg, Germany
| | - Hans-Jochen Heinze
- Department of Neurology, Otto-von-Guericke University, Magdeburg, Germany
- Institute of Cognitive Neurology and Dementia Research (IKND), Magdeburg, Germany
- German Center for Neurodegenerative Diseases (DZNE), Magdeburg, Germany
- Center for Behavioral Brain Sciences, Magdeburg, Germany
| | - Emrah Düzel
- Institute of Cognitive Neurology and Dementia Research (IKND), Magdeburg, Germany
- German Center for Neurodegenerative Diseases (DZNE), Magdeburg, Germany
- Center for Behavioral Brain Sciences, Magdeburg, Germany
- Institute of Cognitive Neuroscience, University College London, London, United Kingdom
| | - Stefanie Schreiber
- Department of Neurology, Otto-von-Guericke University, Magdeburg, Germany
- German Center for Neurodegenerative Diseases (DZNE), Magdeburg, Germany
- Center for Behavioral Brain Sciences, Magdeburg, Germany
| |
Collapse
|
24
|
Zhang Q, Luo X, Zhou L, Nguyen TD, Prince MR, Spincemaille P, Wang Y. Fluid Mechanics Approach to Perfusion Quantification: Vasculature Computational Fluid Dynamics Simulation, Quantitative Transport Mapping (QTM) Analysis of Dynamics Contrast Enhanced MRI, and Application in Nonalcoholic Fatty Liver Disease Classification. IEEE Trans Biomed Eng 2023; 70:980-990. [PMID: 36107908 DOI: 10.1109/tbme.2022.3207057] [Citation(s) in RCA: 5] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/08/2022]
Abstract
OBJECTIVE We quantify liver perfusion using quantitative transport mapping (QTM) method that is free of arterial input function (AIF). QTM method is validated in a vasculature computational fluid dynamics (CFD) simulation and is applied for processing dynamic contrast enhanced (DCE) MRI images in differentiating liver with nonalcoholic fatty liver disease (NAFLD) from healthy controls using pathology reference in a preclinical rabbit model. METHODS QTM method was validated on a liver perfusion simulation based on fluid dynamics using a rat liver vasculature model and the mass transport equation. In the NAFLD grading task, DCE MRI images of 7 adult rabbits with methionine choline-deficient diet-induced nonalcoholic steatohepatitis (NASH), 8 adult rabbits with simple steatosis (SS) were acquired and processed using QTM method and dual-input two compartment Kety's method respectively. Statistical analysis was performed on six perfusion parameters: velocity magnitude | u | derived from QTM, liver arterial blood flow LBFa, liver venous blood flow LBFv, permeability Ktrans, blood volume Vp and extravascular space volume Ve averaged in liver ROI. RESULTS In the simulation, QTM method successfully reconstructed blood flow, reduced error by 48% compared to Kety's method. In the preclinical study, only QTM |u| showed significant difference between high grade NAFLD group and low grade NAFLD group. CONCLUSION QTM postprocesses DCE-MRI automatically through deconvolution in space and time to solve the inverse problem of the transport equation. Comparing with Kety's method, QTM method showed higher accuracy and better differentiation in NAFLD classification task. SIGNIFICANCE We propose to apply QTM method in liver DCE MRI perfusion quantification.
Collapse
|
25
|
Lee K, Ellison B, Selim M, Long NH, Filippidis A, Thomas AJ, Spincemaille P, Wang Y, Soman S. Quantitative susceptibility mapping improves cerebral microbleed detection relative to susceptibility-weighted images. J Neuroimaging 2023; 33:138-146. [PMID: 36168880 DOI: 10.1111/jon.13054] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/13/2022] [Revised: 09/10/2022] [Accepted: 09/12/2022] [Indexed: 02/01/2023] Open
Abstract
BACKGROUND AND PURPOSE Cerebral microbleed (CMB) detection impacts disease diagnosis and management. Susceptibility-weighted imaging (SWI) MRI depictions of CMBs are used with phase images (SWIP) to distinguish blood from calcification, via qualitative intensity evaluation (bright/dark). However, the intensities depicted for a single lesion can vary within and across consecutive SWIP image planes, impairing the classification of findings as a CMB. We hypothesize that quantitative susceptibility mapping (QSM) MRI, which maps tissue susceptibility, demonstrates less in- and through-plane intensity variation, improving the clinician's ability to categorize a finding as a CMB. METHODS Forty-eight patients with acute intracranial hemorrhage who received multi-echo gradient echo MRI used to generate both SWI/SWIP and morphology-enabled dipole inversion QSM images were enrolled. Five hundred and sixty lesions were visually classified as having homogeneous or heterogeneous in-plane and through-plane intensity by a neuroradiologist and two diagnostic radiology residents using published rating criteria. When available, brain CT scans were analyzed for calcification or acute hemorrhage. Relative risk (RR) ratios and confidence intervals (CIs) were calculated using a generalized linear model with log link and binary error. RESULTS QSM showed unambiguous lesion signal intensity three times more frequently than SWIP (RR = 0.3235, 95% CI 0.2386-0.4386, p<.0001). The probability of QSM depicting homogeneous lesion intensity was three times greater than SWIP for small (RR = 0.3172, 95% CI 0.2382-0.4225, p<.0001), large (RR = 0.3431, 95% CI 0.2045-0.5758, p<.0001), lobar (RR = 0.3215, 95% CI 0.2151-0.4805, p<.0001), cerebellar (RR = 0.3215, 95% CI 0.2151-0.4805, p<.0001), brainstem (RR = 0.3100, 95% CI 0.1192-0.8061, p = .0163), and basal ganglia (RR = 0.3380, 95% CI 0.1980-0.5769, p<.0001) lesions. CONCLUSIONS QSM more consistently demonstrates interpretable lesion intensity compared to SWIP as used for distinguishing CMBs from calcification.
Collapse
Affiliation(s)
- Kyuwon Lee
- Department of Radiology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts, USA
| | - Brian Ellison
- Department of Radiology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts, USA
| | - Magdy Selim
- Department of Neurology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts, USA
| | - Ngo H Long
- Department of General Medicine/Primary Care, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts, USA
| | - Aristotelis Filippidis
- Department of Neurosurgery, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts, USA
| | - Ajith J Thomas
- Department of Neurological Surgery, Cooper University Health Care, Cooper Medical School of Rowan University, Camden, New Jersey, USA
| | | | - Yi Wang
- Department of Radiology, Weill Cornell Medicine, New York, New York, USA
| | - Salil Soman
- Department of Radiology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts, USA
| |
Collapse
|
26
|
Sharma B, Beaudin AE, Cox E, Saad F, Nelles K, Gee M, Frayne R, Gobbi DG, Camicioli R, Smith EE, McCreary CR. Brain iron content in cerebral amyloid angiopathy using quantitative susceptibility mapping. Front Neurosci 2023; 17:1139988. [PMID: 37139529 PMCID: PMC10149796 DOI: 10.3389/fnins.2023.1139988] [Citation(s) in RCA: 6] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/08/2023] [Accepted: 03/22/2023] [Indexed: 05/05/2023] Open
Abstract
Introduction Cerebral amyloid angiopathy (CAA) is a small vessel disease that causes covert and symptomatic brain hemorrhaging. We hypothesized that persons with CAA would have increased brain iron content detectable by quantitative susceptibility mapping (QSM) on magnetic resonance imaging (MRI), and that higher iron content would be associated with worse cognition. Methods Participants with CAA (n = 21), mild Alzheimer's disease with dementia (AD-dementia; n = 14), and normal controls (NC; n = 83) underwent 3T MRI. Post-processing QSM techniques were applied to obtain susceptibility values for regions of the frontal and occipital lobe, thalamus, caudate, putamen, pallidum, and hippocampus. Linear regression was used to examine differences between groups, and associations with global cognition, controlling for multiple comparisons using the false discovery rate method. Results No differences were found between regions of interest in CAA compared to NC. In AD, the calcarine sulcus had greater iron than NC (β = 0.99 [95% CI: 0.44, 1.53], q < 0.01). However, calcarine sulcus iron content was not associated with global cognition, measured by the Montreal Cognitive Assessment (p > 0.05 for all participants, NC, CAA, and AD). Discussion After correcting for multiple comparisons, brain iron content, measured via QSM, was not elevated in CAA compared to NC in this exploratory study.
Collapse
Affiliation(s)
- Breni Sharma
- Cumming School of Medicine, University of Calgary, Calgary, AB, Canada
- Department of Clinical Neurosciences, University of Calgary, Calgary, AB, Canada
- Hotchkiss Brain Institute, University of Calgary, Calgary, AB, Canada
| | - Andrew E. Beaudin
- Cumming School of Medicine, University of Calgary, Calgary, AB, Canada
- Department of Clinical Neurosciences, University of Calgary, Calgary, AB, Canada
- Hotchkiss Brain Institute, University of Calgary, Calgary, AB, Canada
| | - Emily Cox
- Cumming School of Medicine, University of Calgary, Calgary, AB, Canada
- Department of Clinical Neurosciences, University of Calgary, Calgary, AB, Canada
- Hotchkiss Brain Institute, University of Calgary, Calgary, AB, Canada
| | - Feryal Saad
- Cumming School of Medicine, University of Calgary, Calgary, AB, Canada
- Department of Clinical Neurosciences, University of Calgary, Calgary, AB, Canada
- Hotchkiss Brain Institute, University of Calgary, Calgary, AB, Canada
- Seaman Family MR Research Centre, University of Calgary, Calgary, AB, Canada
| | - Krista Nelles
- Department of Medicine (Neurology), University of Alberta, Edmonton, AB, Canada
| | - Myrlene Gee
- Department of Medicine (Neurology), University of Alberta, Edmonton, AB, Canada
| | - Richard Frayne
- Cumming School of Medicine, University of Calgary, Calgary, AB, Canada
- Department of Clinical Neurosciences, University of Calgary, Calgary, AB, Canada
- Hotchkiss Brain Institute, University of Calgary, Calgary, AB, Canada
- Seaman Family MR Research Centre, University of Calgary, Calgary, AB, Canada
- Department of Radiology, University of Calgary, Calgary, AB, Canada
- Calgary Image Processing and Analysis Centre, University of Calgary, Calgary, AB, Canada
| | - David G. Gobbi
- Cumming School of Medicine, University of Calgary, Calgary, AB, Canada
- Department of Clinical Neurosciences, University of Calgary, Calgary, AB, Canada
- Hotchkiss Brain Institute, University of Calgary, Calgary, AB, Canada
- Department of Radiology, University of Calgary, Calgary, AB, Canada
- Calgary Image Processing and Analysis Centre, University of Calgary, Calgary, AB, Canada
| | - Richard Camicioli
- Department of Medicine (Neurology), University of Alberta, Edmonton, AB, Canada
- Neuroscience and Mental Health Institute, University of Alberta, Edmonton, AB, Canada
| | - Eric E. Smith
- Cumming School of Medicine, University of Calgary, Calgary, AB, Canada
- Department of Clinical Neurosciences, University of Calgary, Calgary, AB, Canada
- Hotchkiss Brain Institute, University of Calgary, Calgary, AB, Canada
- Seaman Family MR Research Centre, University of Calgary, Calgary, AB, Canada
- *Correspondence: Eric E. Smith,
| | - Cheryl R. McCreary
- Cumming School of Medicine, University of Calgary, Calgary, AB, Canada
- Department of Clinical Neurosciences, University of Calgary, Calgary, AB, Canada
- Hotchkiss Brain Institute, University of Calgary, Calgary, AB, Canada
- Seaman Family MR Research Centre, University of Calgary, Calgary, AB, Canada
- Department of Radiology, University of Calgary, Calgary, AB, Canada
| |
Collapse
|
27
|
Reduced basal ganglia tissue-iron concentration in school-age children with attention-deficit/hyperactivity disorder is localized to limbic circuitry. Exp Brain Res 2022; 240:3271-3288. [PMID: 36301336 DOI: 10.1007/s00221-022-06484-7] [Citation(s) in RCA: 7] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/31/2022] [Accepted: 10/10/2022] [Indexed: 11/04/2022]
Abstract
Dopamine-related abnormalities in the basal ganglia have been implicated in attention-deficit/hyperactivity disorder (ADHD). Iron plays a critical role in supporting dopaminergic function, and reduced brain iron and serum ferritin levels have been linked to ADHD symptom severity in children. Furthermore, the basal ganglia is a central brain region implicated in ADHD psychopathology and involved in motor and reward functions as well as emotional responding. The present study repurposed diffusion tensor imaging (DTI) to examine effects of an ADHD diagnosis and sex on iron deposition within the basal ganglia in children ages 8-12 years. We further explored associations between brain iron levels and ADHD symptom severity and affective symptoms. We observed reduced iron levels in children with ADHD in the bilateral limbic region of the striatum, as well as reduced levels of iron-deposition in males in the sensorimotor striatal subregion, regardless of diagnosis. Across the whole sample, iron-deposition increased with age in all regions. Brain-behavior analyses revealed that, across diagnostic groups, lower tissue-iron levels in bilateral limbic striatum correlated with greater ADHD symptom severity, whereas lower tissue-iron levels in the left limbic striatum only correlated with anxious, depressive and affective symptom severity. This study sheds light on the neurobiological underpinnings of ADHD, specifically highlighting the localization of tissue-iron deficiency in limbic regions, and providing support for repurposing DTI for brain iron analyses. Our findings highlight the need for further investigation of iron as a biomarker in the diagnosis and treatment of ADHD and sex differences.
Collapse
|
28
|
Uchida Y, Kan H, Sakurai K, Oishi K, Matsukawa N. Quantitative susceptibility mapping as an imaging biomarker for Alzheimer’s disease: The expectations and limitations. Front Neurosci 2022; 16:938092. [PMID: 35992906 PMCID: PMC9389285 DOI: 10.3389/fnins.2022.938092] [Citation(s) in RCA: 29] [Impact Index Per Article: 9.7] [Reference Citation Analysis] [Abstract] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/06/2022] [Accepted: 07/14/2022] [Indexed: 11/25/2022] Open
Abstract
Alzheimer’s disease (AD) is the most common type of dementia and a distressing diagnosis for individuals and caregivers. Researchers and clinical trials have mainly focused on β-amyloid plaques, which are hypothesized to be one of the most important factors for neurodegeneration in AD. Meanwhile, recent clinicopathological and radiological studies have shown closer associations of tau pathology rather than β-amyloid pathology with the onset and progression of Alzheimer’s symptoms. Toward a biological definition of biomarker-based research framework for AD, the 2018 National Institute on Aging–Alzheimer’s Association working group has updated the ATN classification system for stratifying disease status in accordance with relevant pathological biomarker profiles, such as cerebral β-amyloid deposition, hyperphosphorylated tau, and neurodegeneration. In addition, altered iron metabolism has been considered to interact with abnormal proteins related to AD pathology thorough generating oxidative stress, as some prior histochemical and histopathological studies supported this iron-mediated pathomechanism. Quantitative susceptibility mapping (QSM) has recently become more popular as a non-invasive magnetic resonance technique to quantify local tissue susceptibility with high spatial resolution, which is sensitive to the presence of iron. The association of cerebral susceptibility values with other pathological biomarkers for AD has been investigated using various QSM techniques; however, direct evidence of these associations remains elusive. In this review, we first briefly describe the principles of QSM. Second, we focus on a large variety of QSM applications, ranging from common applications, such as cerebral iron deposition, to more recent applications, such as the assessment of impaired myelination, quantification of venous oxygen saturation, and measurement of blood– brain barrier function in clinical settings for AD. Third, we mention the relationships among QSM, established biomarkers, and cognitive performance in AD. Finally, we discuss the role of QSM as an imaging biomarker as well as the expectations and limitations of clinically useful diagnostic and therapeutic implications for AD.
Collapse
Affiliation(s)
- Yuto Uchida
- Department of Neurology, Nagoya City University Graduate School of Medical Sciences, Nagoya, Japan
- The Russell H. Morgan Department of Radiology and Radiological Science, Johns Hopkins University School of Medicine, Baltimore, MD, United States
- *Correspondence: Yuto Uchida,
| | - Hirohito Kan
- Department of Integrated Health Sciences, Nagoya University Graduate School of Medicine, Nagoya, Japan
| | - Keita Sakurai
- Department of Radiology, National Center for Geriatrics and Gerontology, Ōbu, Japan
| | - Kenichi Oishi
- The Russell H. Morgan Department of Radiology and Radiological Science, Johns Hopkins University School of Medicine, Baltimore, MD, United States
| | - Noriyuki Matsukawa
- Department of Neurology, Nagoya City University Graduate School of Medical Sciences, Nagoya, Japan
- Noriyuki Matsukawa,
| |
Collapse
|
29
|
Kim J, Nguyen TD, Zhang J, Gauthier SA, Marcille M, Zhang H, Cho J, Spincemaille P, Wang Y. Subsecond accurate myelin water fraction reconstruction from FAST-T 2 data with 3D UNET. Magn Reson Med 2022; 87:2979-2988. [PMID: 35092094 DOI: 10.1002/mrm.29176] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/28/2021] [Revised: 12/31/2021] [Accepted: 01/08/2022] [Indexed: 11/10/2022]
Abstract
PURPOSE To develop a 3D UNET convolutional neural network for rapid extraction of myelin water fraction (MWF) maps from six-echo fast acquisition with spiral trajectory and T2 -prep data and to evaluate its accuracy in comparison with multilayer perceptron (MLP) network. METHODS The MWF maps were extracted from 138 patients with multiple sclerosis using an iterative three-pool nonlinear least-squares algorithm (NLLS) without and with spatial regularization (srNLLS), which were used as ground-truth labels to train, validate, and test UNET and MLP networks as a means to accelerate data fitting. Network testing was performed in 63 patients with multiple sclerosis and a numerically simulated brain phantom at SNR of 200, 100 and 50. RESULTS Simulations showed that UNET reduced the MWF mean absolute error by 30.1% to 56.4% and 16.8% to 53.6% over the whole brain and by 41.2% to 54.4% and 21.4% to 49.4% over the lesions for predicting srNLLS and NLLS MWF, respectively, compared to MLP, with better performance at lower SNRs. UNET also outperformed MLP for predicting srNLLS MWF in the in vivo multiple-sclerosis brain data, reducing mean absolute error over the whole brain by 61.9% and over the lesions by 67.5%. However, MLP yielded 41.1% and 51.7% lower mean absolute error for predicting in vivo NLLS MWF over the whole brain and the lesions, respectively, compared with UNET. The whole-brain MWF processing time using a GPU was 0.64 seconds for UNET and 0.74 seconds for MLP. CONCLUSION Subsecond whole-brain MWF extraction from fast acquisition with spiral trajectory and T2 -prep data using UNET is feasible and provides better accuracy than MLP for predicting MWF output of srNLLS algorithm.
Collapse
Affiliation(s)
- Jeremy Kim
- Department of Computer Science, Stanford University, Stanford, California, USA
| | - Thanh D Nguyen
- Department of Radiology, Weill Cornell Medicine, New York, New York, USA
| | - Jinwei Zhang
- Department of Radiology, Weill Cornell Medicine, New York, New York, USA
- Meinig School of Biomedical Engineering, Cornell University, Ithaca, New York, USA
| | - Susan A Gauthier
- Department of Neurology, Weill Cornell Medicine, New York, New York, USA
| | - Melanie Marcille
- Department of Neurology, Weill Cornell Medicine, New York, New York, USA
| | - Hang Zhang
- Meinig School of Biomedical Engineering, Cornell University, Ithaca, New York, USA
| | - Junghun Cho
- Department of Radiology, Weill Cornell Medicine, New York, New York, USA
| | | | - Yi Wang
- Department of Radiology, Weill Cornell Medicine, New York, New York, USA
- Meinig School of Biomedical Engineering, Cornell University, Ithaca, New York, USA
| |
Collapse
|
30
|
Nikparast F, Ganji Z, Danesh Doust M, Faraji R, Zare H. Brain pathological changes during neurodegenerative diseases and their identification methods: How does QSM perform in detecting this process? Insights Imaging 2022; 13:74. [PMID: 35416533 PMCID: PMC9008086 DOI: 10.1186/s13244-022-01207-6] [Citation(s) in RCA: 12] [Impact Index Per Article: 4.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/16/2021] [Accepted: 03/13/2022] [Indexed: 12/14/2022] Open
Abstract
The presence of iron is essential for many biological processes in the body. But sometimes, for various reasons, the amount of iron deposition in different areas of the brain increases, which leads to problems related to the nervous system. Quantitative susceptibility mapping (QSM) is one of the newest magnetic resonance imaging (MRI)-based methods for assessing iron accumulation in target areas. This Narrative Review article aims to evaluate the performance of QSM compared to other methods of assessing iron deposition in the clinical field. Based on the results, we introduced related basic definitions, some neurodegenerative diseases, methods of examining iron deposition in these diseases, and their advantages and disadvantages. This article states that the QSM method can be introduced as a new, reliable, and non-invasive technique for clinical evaluations.
Collapse
Affiliation(s)
- Farzaneh Nikparast
- Medical Physics Research Center, Mashhad University of Medical Sciences, Mashhad, Iran
| | - Zohreh Ganji
- Medical Physics Research Center, Mashhad University of Medical Sciences, Mashhad, Iran
| | - Mohammad Danesh Doust
- Medical Physics Research Center, Mashhad University of Medical Sciences, Mashhad, Iran
| | - Reyhane Faraji
- Medical Physics Research Center, Mashhad University of Medical Sciences, Mashhad, Iran
| | - Hoda Zare
- Medical Physics Research Center, Mashhad University of Medical Sciences, Mashhad, Iran. .,Department of Medical Physics, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran.
| |
Collapse
|
31
|
Longitudinal Observation of Asymmetric Iron Deposition in an Intracerebral Hemorrhage Model Using Quantitative Susceptibility Mapping. Symmetry (Basel) 2022. [DOI: 10.3390/sym14020350] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 02/01/2023] Open
Abstract
Quantitative susceptibility mapping (QSM) is used to obtain quantitative magnetic susceptibility maps of materials from magnitude and phase images acquired by three-dimensional gradient-echo using inverse problem-solving. Few preclinical studies have evaluated the intracerebral hemorrhage (ICH) model and asymmetric iron deposition. We created a rat model of ICH and compared QSM and conventional magnetic resonance imaging (MRI) during the longitudinal evaluation of ICH. Collagenase was injected in the right striatum of 12-week-old Wistar rats. QSM and conventional MRI were performed on days 0, 1, 7, and 28 after surgery using 7-Tesla MRI. Susceptibility, normalized signal value, and area of the hemorrhage site were statistically compared during image analysis. Susceptibility decreased monotonically up to day 7 but increased on day 28. Other imaging methods showed a significant increase in signal from day 0 to day 1 but a decreasing trend after day 1. During the area evaluation, conventional MRI methods showed an increase from day 0 to day 1; however, decreases were observed thereafter. QSM showed a significant increase from day 0 to day 1. The temporal evaluation of ICH by QSM suggested the possibility of detecting of asymmetric iron deposition for normal brain site.
Collapse
|
32
|
Cho J, Nguyen TD, Huang W, Sweeney EM, Luo X, Kovanlikaya I, Zhang S, Gillen KM, Spincemaille P, Gupta A, Gauthier SA, Wang Y. Brain oxygen extraction fraction mapping in patients with multiple sclerosis. J Cereb Blood Flow Metab 2022; 42:338-348. [PMID: 34558996 PMCID: PMC9122515 DOI: 10.1177/0271678x211048031] [Citation(s) in RCA: 16] [Impact Index Per Article: 5.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 01/11/2023]
Abstract
We aimed to demonstrate the feasibility of whole brain oxygen extraction fraction (OEF) mapping for measuring lesion specific and regional OEF abnormalities in multiple sclerosis (MS) patients. In 22 MS patients and 11 healthy controls (HC), OEF and neural tissue susceptibility (χn) maps were computed from MRI multi-echo gradient echo data. In MS patients, 80 chronic active lesions with hyperintense rim on quantitative susceptibility mapping were identified, and the mean OEF and χn within the rim and core were compared using linear mixed-effect model analysis. The rim showed higher OEF and χn than the core: relative to their adjacent normal appearing white matter, OEF contrast = -6.6 ± 7.0% vs. -9.8 ± 7.8% (p < 0.001) and χn contrast = 33.9 ± 20.3 ppb vs. 25.7 ± 20.5 ppb (p = 0.017). Between MS and HC, OEF and χn were compared using a linear regression model in subject-based regions of interest. In the whole brain, compared to HC, MS had lower OEF, 30.4 ± 3.3% vs. 21.4 ± 4.4% (p < 0.001), and higher χn, -23.7 ± 7.0 ppb vs. -11.3 ± 7.7 ppb (p = 0.018). Our feasibility study suggests that OEF may serve as a useful quantitative marker of tissue oxygen utilization in MS.
Collapse
Affiliation(s)
- Junghun Cho
- Department of Radiology, Weill Cornell Medicine, New York, NY, USA
| | - Thanh D Nguyen
- Department of Radiology, Weill Cornell Medicine, New York, NY, USA
| | - Weiyuan Huang
- Department of Radiology, Weill Cornell Medicine, New York, NY, USA
| | - Elizabeth M Sweeney
- Department of Population Health Sciences, Weill Cornell Medicine, New York, NY, USA
| | - Xianfu Luo
- Department of Radiology, Weill Cornell Medicine, New York, NY, USA
| | | | - Shun Zhang
- Department of Radiology, Weill Cornell Medicine, New York, NY, USA
| | - Kelly M Gillen
- Department of Radiology, Weill Cornell Medicine, New York, NY, USA
| | | | - Ajay Gupta
- Department of Radiology, Weill Cornell Medicine, New York, NY, USA
| | - Susan A Gauthier
- Department of Radiology, Weill Cornell Medicine, New York, NY, USA.,Department of Neurology, Weill Cornell Medicine, New York, NY, USA
| | - Yi Wang
- Department of Radiology, Weill Cornell Medicine, New York, NY, USA.,Department of Biomedical Engineering, Cornell University, Ithaca, NY, USA
| |
Collapse
|
33
|
Xie H, Zhuang H, Guo Y, Sharma RD, Zhang Q, Li J, Lu S, Xu L, Chan Q, Yoneda T, Spincemaille P, Zhang H, Guo H, Prince MR, Yu C, Wang Y. The appearance of magnetic susceptibility objects in SWI phase depends on object size: Comparison with QSM and CT. Clin Imaging 2022; 82:67-72. [PMID: 34798560 DOI: 10.1016/j.clinimag.2021.11.005] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/14/2021] [Revised: 10/14/2021] [Accepted: 11/07/2021] [Indexed: 11/03/2022]
Abstract
PURPOSE Tissue magnetic susceptibility sign can potentially be detected on susceptibility weighted imaging (SWI) phase (SW-P). This study aims to investigate its performance for depicting brain susceptibility structures. METHODS A simulation was performed to depict magnetic susceptibility structures of various geometries on SW-P and quantitative susceptibility mapping (QSM). Brain MRI was performed on 25 subjects using SWI on a 3 T MRI system. QSM was generated from the same data. SW-P and QSM were analyzed according to radiological assessment for depicting globus pallidus nuclei, optic radiation white matter tracts, and lateral ventricular choroid plexus calcifications. In 11 of these subjects, CT was available and correlated with SW-P and QSM to assess their performance in quantifying calcifications in the choroid plexus. RESULTS In simulation, the appearance of a sphere on SW-P ranged from centric nodule to mixed positive and negative values as the diameter increased. Large cylinders also appeared as mixed positive and negative values. In comparison, QSM correctly depicted the susceptibility distribution of all magnetic structures. On human brain images, SW-P depicted the globus pallidus and optic radiation with mixed positive and negative values, consistent with simulation, and small choroid plexus calcifications as either mixed positive and negative values or as centric nodules; QSM depicted all structures as solid structures with the expected signs. For measuring calcification in the choroid plexus, QSM vs CT linear regression had a higher coefficient of determination compared to SW-P vs CT and SW-P vs QSM. CONCLUSION Appearance of susceptibility sources on SW-P changes with object size. This problem can be overcome using QSM.
Collapse
Affiliation(s)
- Hong Xie
- Department of Radiology, The First College of Clinical Medical Science, Three Gorges University, Yichang, Hubei Province, China
| | - Hangwei Zhuang
- Department of Biomedical Engineering, Cornell University, Ithaca, NY, USA
| | - Yihao Guo
- Department of Biomedical Engineering, Southern Medical University, Guangzhou, Guangdong Province, China
| | - Ria D Sharma
- Department of Biomedical Engineering, Cornell University, Ithaca, NY, USA
| | - Qihao Zhang
- Department of Radiology, Weill Medical College of Cornell University, New York, NY, USA
| | - Jiahao Li
- Department of Radiology, Weill Medical College of Cornell University, New York, NY, USA
| | - Shimin Lu
- Center for Biomedical Imaging Research, Department of Biomedical Engineering, School of Medicine, Tsinghua University, Beijing, China
| | - Liang Xu
- Department of Radiology, The First College of Clinical Medical Science, Three Gorges University, Yichang, Hubei Province, China
| | | | - Tetsuya Yoneda
- Department of Medical Imaging Sciences, Kumamoto University, Kumamoto, Japan
| | - Pascal Spincemaille
- Department of Radiology, Weill Medical College of Cornell University, New York, NY, USA
| | - Honglei Zhang
- Department of Radiology, Weill Medical College of Cornell University, New York, NY, USA; Department of Radiology, Memorial Sloan Kettering Cancer Center, New York, NY, USA
| | - Hua Guo
- Center for Biomedical Imaging Research, Department of Biomedical Engineering, School of Medicine, Tsinghua University, Beijing, China
| | - Martin R Prince
- Department of Radiology, Weill Medical College of Cornell University, New York, NY, USA
| | - Chengxin Yu
- Department of Radiology, The First College of Clinical Medical Science, Three Gorges University, Yichang, Hubei Province, China
| | - Yi Wang
- Department of Biomedical Engineering, Cornell University, Ithaca, NY, USA; Department of Radiology, Weill Medical College of Cornell University, New York, NY, USA.
| |
Collapse
|
34
|
Quantitative susceptibility mapping reveals brain iron deficiency in children with attention-deficit/hyperactivity disorder: a whole-brain analysis. Eur Radiol 2022; 32:3726-3733. [DOI: 10.1007/s00330-021-08516-2] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/28/2021] [Revised: 11/18/2021] [Accepted: 12/10/2021] [Indexed: 11/04/2022]
|
35
|
Dimov AV, Nguyen TD, Spincemaille P, Sweeney EM, Zinger N, Kovanlikaya I, Kopell BH, Gauthier SA, Wang Y. Global cerebrospinal fluid as a zero-reference regularization for brain quantitative susceptibility mapping. J Neuroimaging 2022; 32:141-147. [PMID: 34480496 PMCID: PMC8752493 DOI: 10.1111/jon.12923] [Citation(s) in RCA: 9] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/18/2020] [Revised: 07/11/2021] [Accepted: 08/09/2021] [Indexed: 01/03/2023] Open
Abstract
BACKGROUND AND PURPOSE The objective ofthis study was to demonstrate a global cerebrospinal fluid (CSF) method for a consistent and automated zero referencing of brain quantitative susceptibility mapping (QSM). METHODS Whole brain CSF mask was automatically segmented by thresholding the gradient echo transverse relaxation ( R2∗) map, and regularization was employed to enforce uniform susceptibility distribution within the CSF volume in the field-to-susceptibility inversion. This global CSF regularization method was compared with a prior ventricular CSF regularization. Both reconstruction methods were compared in a repeatability study of 12 healthy subjects using t-test on susceptibility measurements, and in patient studies of 17 multiple sclerosis (MS) and 10 Parkinson's disease (PD) patients using Wilcoxon rank-sum test on radiological scores. RESULTS In scan-rescan experiments, global CSF regularization provided more consistent CSF volume as well as higher repeatability of QSM measurements than ventricular CSF regularization with a smaller bias: -2.7 parts per billion (ppb) versus -0.13 ppb (t-test p<0.05) and a narrower 95% limits of agreement: [-7.25, 6.99] ppb versus [-16.60, 11.19 ppb] (f-test p<0.05). In PD and MS patients, global CSF regularization reduced smoothly varying shadow artifacts and significantly improved the QSM quality score (p<0.001). CONCLUSIONS The proposed whole brain CSF method for QSM zero referencing improves repeatability and image quality of brain QSM compared to the ventricular CSF method.
Collapse
Affiliation(s)
- Alexey V. Dimov
- Department of Radiology, Weill Cornell Medicine, New York, USA
| | - Thanh D. Nguyen
- Department of Radiology, Weill Cornell Medicine, New York, USA
| | | | | | - Nicole Zinger
- Department of Neurology, Weill Cornell Medicine, New York, USA
| | | | - Brian H. Kopell
- Nash Family Center for Advanced Circuit Therapeutics, Icahn School of Medicine at Mount Sinai, New York, USA
| | | | - Yi Wang
- Department of Radiology, Weill Cornell Medicine, New York, USA
| |
Collapse
|
36
|
Li KR, Avecillas-Chasin J, Nguyen TD, Gillen KM, Dimov A, Chang E, Skudin C, Kopell BH, Wang Y, Shtilbans A. Quantitative evaluation of brain iron accumulation in different stages of Parkinson's disease. J Neuroimaging 2021; 32:363-371. [PMID: 34904328 DOI: 10.1111/jon.12957] [Citation(s) in RCA: 18] [Impact Index Per Article: 4.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/26/2021] [Revised: 11/23/2021] [Accepted: 11/23/2021] [Indexed: 01/02/2023] Open
Abstract
BACKGROUND AND PURPOSE Excessive brain iron deposition is involved in Parkinson's disease (PD) pathogenesis. However, the correlation of iron accumulation in various brain nuclei is not well-established in different stages of the disease. This cross-sectional study aims to evaluate quantitative susceptibility mapping (QSM) as an imaging technique to measure brain iron accumulation in PD patients in different stages compared to healthy controls. METHODS Ninety-six PD patients grouped by their Hoehn and Yahr (H&Y) stages and 31 healthy controls were included in this analysis. The magnetic susceptibility values of the substantia nigra (SN), red nucleus (RN), caudate, putamen, and globus pallidus were obtained and compared. RESULTS Iron level was increased in the SN of PD patients in all stages versus controls (p < .001), with no significant difference within stages. Iron in the RN was significantly increased in stage II versus controls (p = .013) and combined stages III and IV versus controls (p < .001). The iron levels in caudate, putamen, and globus pallidus were not different between any groups. CONCLUSIONS Our data suggest iron accumulation occurs early in the disease course and only in the SN and RN of these patients. This is a large cross-sectional study of brain iron deposition in PD patients according to H&Y staging. Prospective studies are warranted to further validate QSM as a method to follow brain iron, which could serve as a disease biomarker and a therapeutic target.
Collapse
Affiliation(s)
- Kailyn R Li
- Department of Radiology, Weill Cornell Medicine, NewYork-Presbyterian Hospital, New York, New York, USA.,MD Program, Weill Cornell Medicine, New York, New York, USA
| | | | - Thanh D Nguyen
- Department of Radiology, Weill Cornell Medicine, NewYork-Presbyterian Hospital, New York, New York, USA
| | - Kelly M Gillen
- Department of Radiology, Weill Cornell Medicine, NewYork-Presbyterian Hospital, New York, New York, USA
| | - Alexey Dimov
- Department of Radiology, Weill Cornell Medicine, NewYork-Presbyterian Hospital, New York, New York, USA
| | - Eileen Chang
- Department of Radiology, Weill Cornell Medicine, NewYork-Presbyterian Hospital, New York, New York, USA
| | - Carly Skudin
- Department of Radiology, Weill Cornell Medicine, NewYork-Presbyterian Hospital, New York, New York, USA
| | - Brian H Kopell
- Department of Neurosurgery, Mount Sinai Hospital, New York, New York, USA
| | - Yi Wang
- Department of Radiology, Weill Cornell Medicine, NewYork-Presbyterian Hospital, New York, New York, USA
| | - Alexander Shtilbans
- Department of Neurology, Weill Cornell Medicine, NewYork-Presbyterian Hospital, New York, New York, USA.,Department of Neurology, Hospital for Special Surgery, New York, New York, USA
| |
Collapse
|
37
|
Weingärtner S, Desmond KL, Obuchowski NA, Baessler B, Zhang Y, Biondetti E, Ma D, Golay X, Boss MA, Gunter JL, Keenan KE, Hernando D. Development, validation, qualification, and dissemination of quantitative MR methods: Overview and recommendations by the ISMRM quantitative MR study group. Magn Reson Med 2021; 87:1184-1206. [PMID: 34825741 DOI: 10.1002/mrm.29084] [Citation(s) in RCA: 25] [Impact Index Per Article: 6.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/15/2021] [Revised: 10/20/2021] [Accepted: 10/27/2021] [Indexed: 12/26/2022]
Abstract
On behalf of the International Society for Magnetic Resonance in Medicine (ISMRM) Quantitative MR Study Group, this article provides an overview of considerations for the development, validation, qualification, and dissemination of quantitative MR (qMR) methods. This process is framed in terms of two central technical performance properties, i.e., bias and precision. Although qMR is confounded by undesired effects, methods with low bias and high precision can be iteratively developed and validated. For illustration, two distinct qMR methods are discussed throughout the manuscript: quantification of liver proton-density fat fraction, and cardiac T1 . These examples demonstrate the expansion of qMR methods from research centers toward widespread clinical dissemination. The overall goal of this article is to provide trainees, researchers, and clinicians with essential guidelines for the development and validation of qMR methods, as well as an understanding of necessary steps and potential pitfalls for the dissemination of quantitative MR in research and in the clinic.
Collapse
Affiliation(s)
- Sebastian Weingärtner
- Department of Imaging Physics, Delft University of Technology, Delft, The Netherlands
| | - Kimberly L Desmond
- Brain Health Imaging Centre, Centre for Addiction and Mental Health, Toronto, Ontario, Canada.,Department of Psychiatry, University of Toronto, Toronto, Ontario, Canada
| | - Nancy A Obuchowski
- Department of Quantitative Health Sciences, Cleveland Clinic, Cleveland, Ohio, USA
| | - Bettina Baessler
- Institute of Diagnostic and Interventional Radiology, University Hospital Zurich, Zurich, Switzerland
| | - Yuxin Zhang
- Department of Medical Physics, University of Wisconsin-Madison, Madison, Wisconsin, USA.,Department of Radiology, University of Wisconsin-Madison, Madison, Wisconsin, USA
| | - Emma Biondetti
- Department of Neuroscience, Imaging and Clinical Sciences, D'Annunzio University of Chieti and Pescara, Chieti, Italy
| | - Dan Ma
- Department of Biomedical Engineering, Case Western Reserve University, Cleveland, Ohio, USA
| | - Xavier Golay
- Brain Repair & Rehabilitation, Institute of Neurology, University College London, United Kingdom.,Gold Standard Phantoms Limited, Rochester, United Kingdom
| | - Michael A Boss
- Center for Research and Innovation, American College of Radiology, Philadelphia, Pennsylvania, USA
| | | | - Kathryn E Keenan
- National Institute of Standards and Technology, Boulder, Colorado, USA
| | - Diego Hernando
- Department of Medical Physics, University of Wisconsin-Madison, Madison, Wisconsin, USA.,Department of Radiology, University of Wisconsin-Madison, Madison, Wisconsin, USA
| | | |
Collapse
|
38
|
Bossoni L, Hegeman-Kleinn I, van Duinen SG, Bulk M, Vroegindeweij LHP, Langendonk JG, Hirschler L, Webb A, van der Weerd L. Off-resonance saturation as an MRI method to quantify mineral- iron in the post-mortem brain. Magn Reson Med 2021; 87:1276-1288. [PMID: 34655092 PMCID: PMC9293166 DOI: 10.1002/mrm.29041] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/23/2021] [Revised: 09/17/2021] [Accepted: 09/20/2021] [Indexed: 12/24/2022]
Abstract
Purpose To employ an off‐resonance saturation method to measure the mineral‐iron pool in the postmortem brain, which is an endogenous contrast agent that can give information on cellular iron status. Methods An off‐resonance saturation acquisition protocol was implemented on a 7 Tesla preclinical scanner, and the contrast maps were fitted to an established analytical model. The method was validated by correlation and Bland‐Altman analysis on a ferritin‐containing phantom. Mineral‐iron maps were obtained from postmortem tissue of patients with neurological diseases characterized by brain iron accumulation, that is, Alzheimer disease, Huntington disease, and aceruloplasminemia, and validated with histology. Transverse relaxation rate and magnetic susceptibility values were used for comparison. Results In postmortem tissue, the mineral‐iron contrast colocalizes with histological iron staining in all the cases. Iron concentrations obtained via the off‐resonance saturation method are in agreement with literature. Conclusions Off‐resonance saturation is an effective way to detect iron in gray matter structures and partially mitigate for the presence of myelin. If a reference region with little iron is available in the tissue, the method can produce quantitative iron maps. This method is applicable in the study of diseases characterized by brain iron accumulation and can complement existing iron‐sensitive parametric methods.
Collapse
Affiliation(s)
- Lucia Bossoni
- C. J. Gorter Center for High field MRI, Department of Radiology, Leiden University Medical Center, Leiden, The Netherlands
| | | | - Sjoerd G van Duinen
- Department of Pathology, Leiden University Medical Center, Leiden, The Netherlands
| | - Marjolein Bulk
- C. J. Gorter Center for High field MRI, Department of Radiology, Leiden University Medical Center, Leiden, The Netherlands.,Department of Neurology, Alzheimer Center, Erasmus University Medical Center, Rotterdam, The Netherlands
| | - Lena H P Vroegindeweij
- Department of Internal Medicine, Center for Lysosomal and Metabolic Diseases, Porphyria Center Rotterdam, Erasmus University Medical Center, Rotterdam, The Netherlands
| | - Janneke G Langendonk
- Department of Internal Medicine, Center for Lysosomal and Metabolic Diseases, Porphyria Center Rotterdam, Erasmus University Medical Center, Rotterdam, The Netherlands
| | - Lydiane Hirschler
- C. J. Gorter Center for High field MRI, Department of Radiology, Leiden University Medical Center, Leiden, The Netherlands
| | - Andrew Webb
- C. J. Gorter Center for High field MRI, Department of Radiology, Leiden University Medical Center, Leiden, The Netherlands
| | - Louise van der Weerd
- C. J. Gorter Center for High field MRI, Department of Radiology, Leiden University Medical Center, Leiden, The Netherlands.,Department of Human Genetics, Leiden University Medical Center, Leiden, The Netherlands
| |
Collapse
|
39
|
Lorio S, Sedlacik J, So PW, Parkes HG, Gunny R, Löbel U, Li YF, Ogunbiyi O, Mistry T, Dixon E, Adler S, Cross JH, Baldeweg T, Jacques TS, Shmueli K, Carmichael DW. Quantitative MRI susceptibility mapping reveals cortical signatures of changes in iron, calcium and zinc in malformations of cortical development in children with drug-resistant epilepsy. Neuroimage 2021; 238:118102. [PMID: 34058334 PMCID: PMC8350142 DOI: 10.1016/j.neuroimage.2021.118102] [Citation(s) in RCA: 8] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/15/2020] [Revised: 04/14/2021] [Accepted: 04/19/2021] [Indexed: 12/21/2022] Open
Abstract
OBJECTIVE Malformations of cortical development (MCD), including focal cortical dysplasia (FCD), are the most common cause of drug-resistant focal epilepsy in children. Histopathological lesion characterisation demonstrates abnormal cell types and lamination, alterations in myelin (typically co-localised with iron), and sometimes calcification. Quantitative susceptibility mapping (QSM) is an emerging MRI technique that measures tissue magnetic susceptibility (χ) reflecting it's mineral composition. We used QSM to investigate abnormal tissue composition in a group of children with focal epilepsy with comparison to effective transverse relaxation rate (R2*) and Synchrotron radiation X-ray fluorescence (SRXRF) elemental maps. Our primary hypothesis was that reductions in χ would be found in FCD lesions, resulting from alterations in their iron and calcium content. We also evaluated deep grey matter nuclei for changes in χ with age. METHODS QSM and R2* maps were calculated for 40 paediatric patients with suspected MCD (18 histologically confirmed) and 17 age-matched controls. Patients' sub-groups were defined based on concordant electro-clinical or histopathology data. Quantitative investigation of QSM and R2* was performed within lesions, using a surface-based approach with comparison to homologous regions, and within deep brain regions using a voxel-based approach with regional values modelled with age and epilepsy as covariates. Synchrotron radiation X-ray fluorescence (SRXRF) was performed on brain tissue resected from 4 patients to map changes in iron, calcium and zinc and relate them to MRI parameters. RESULTS Compared to fluid-attenuated inversion recovery (FLAIR) or T1-weighted imaging, QSM improved lesion conspicuity in 5% of patients. In patients with well-localised lesions, quantitative profiling demonstrated decreased χ, but not R2*, across cortical depth with respect to the homologous regions. Contra-lateral homologous regions additionally exhibited increased χ at 2-3 mm cortical depth that was absent in lesions. The iron decrease measured by the SRXRF in FCDIIb lesions was in agreement with myelin reduction observed by Luxol Fast Blue histochemical staining. SRXRF analysis in two FCDIIb tissue samples showed increased zinc and calcium in one patient, and decreased iron in the brain region exhibiting low χ and high R2* in both patients. QSM revealed expected age-related changes in the striatum nuclei, substantia nigra, sub-thalamic and red nucleus. CONCLUSION QSM non-invasively revealed cortical/sub-cortical tissue alterations in MCD lesions and in particular that χ changes in FCDIIb lesions were consistent with reduced iron, co-localised with low myelin and increased calcium and zinc content. These findings suggest that measurements of cortical χ could be used to characterise tissue properties non-invasively in epilepsy lesions.
Collapse
Affiliation(s)
- Sara Lorio
- Developmental Neurosciences, Great Ormond Street Institute of Child Health, University College London, London, UK; Wellcome EPSRC Centre for Medical Engineering, School of Biomedical Engineering and Imaging Sciences, King's College London, St Thomas' Hospital, London SE1 7EH, UK
| | - Jan Sedlacik
- Biomedical Engineering Department, School of Biomedical Engineering & Imaging Sciences, King's College London, London, UK; Center for the Developing Brain, School of Biomedical Engineering and Imaging Sciences, King's College London, London, UK
| | - Po-Wah So
- Department of Neuroimaging, Maurice Wohl Clinical Neuroscience Institute, Institute of Psychiatry, Psychology and Neuroscience, King's College London, UK
| | - Harold G Parkes
- Department of Neuroimaging, Maurice Wohl Clinical Neuroscience Institute, Institute of Psychiatry, Psychology and Neuroscience, King's College London, UK
| | - Roxana Gunny
- Department of Radiology, Great Ormond Street Hospital for Children NHS Foundation Trust, London, UK
| | - Ulrike Löbel
- Department of Radiology, Great Ormond Street Hospital for Children NHS Foundation Trust, London, UK
| | - Yao-Feng Li
- Developmental Biology and Cancer Programme, UCL Great Ormond Street Institute of Child Health, University College London and Department of Histopathology, Great Ormond Street Hospital for Children NHS Foundation Trust, London, UK; Pathology Department, Tri-Service General Hospital and National Defence Medical Centre, Taipei, Taiwan, ROC
| | - Olumide Ogunbiyi
- Developmental Biology and Cancer Programme, UCL Great Ormond Street Institute of Child Health, University College London and Department of Histopathology, Great Ormond Street Hospital for Children NHS Foundation Trust, London, UK
| | - Talisa Mistry
- Developmental Biology and Cancer Programme, UCL Great Ormond Street Institute of Child Health, University College London and Department of Histopathology, Great Ormond Street Hospital for Children NHS Foundation Trust, London, UK
| | - Emma Dixon
- MRI Group, Department of Medical Physics and Biomedical Engineering, University College London, London, UK
| | - Sophie Adler
- Developmental Neurosciences, Great Ormond Street Institute of Child Health, University College London, London, UK
| | - J Helen Cross
- Developmental Neurosciences, Great Ormond Street Institute of Child Health, University College London, London, UK
| | - Torsten Baldeweg
- Developmental Neurosciences, Great Ormond Street Institute of Child Health, University College London, London, UK
| | - Thomas S Jacques
- Developmental Biology and Cancer Programme, UCL Great Ormond Street Institute of Child Health, University College London and Department of Histopathology, Great Ormond Street Hospital for Children NHS Foundation Trust, London, UK
| | - Karin Shmueli
- MRI Group, Department of Medical Physics and Biomedical Engineering, University College London, London, UK
| | - David W Carmichael
- Developmental Neurosciences, Great Ormond Street Institute of Child Health, University College London, London, UK; Wellcome EPSRC Centre for Medical Engineering, School of Biomedical Engineering and Imaging Sciences, King's College London, St Thomas' Hospital, London SE1 7EH, UK.
| |
Collapse
|
40
|
Boehm C, Sollmann N, Meineke J, Ruschke S, Dieckmeyer M, Weiss K, Zimmer C, Makowski MR, Baum T, Karampinos DC. Preconditioned water-fat total field inversion: Application to spine quantitative susceptibility mapping. Magn Reson Med 2021; 87:417-430. [PMID: 34255370 DOI: 10.1002/mrm.28903] [Citation(s) in RCA: 9] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/19/2021] [Revised: 05/14/2021] [Accepted: 06/07/2021] [Indexed: 02/05/2023]
Abstract
PURPOSE To (a) develop a preconditioned water-fat total field inversion (wfTFI) algorithm that directly estimates the susceptibility map from complex multi-echo gradient echo data for water-fat regions and to (b) evaluate the performance of the proposed wfTFI quantitative susceptibility mapping (QSM) method in comparison with a local field inversion (LFI) method and a linear total field inversion (TFI) method in the spine. METHODS Numerical simulations and in vivo spine multi-echo gradient echo measurements were performed to compare wfTFI to an algorithm based on disjoint background field removal (BFR) and LFI and to a formerly proposed TFI algorithm. The data from 1 healthy volunteer and 10 patients with metastatic bone disease were included in the analysis. Clinical routine computed tomography (CT) images were used as a reference standard to distinguish osteoblastic from osteolytic changes. The ability of the QSM methods to distinguish osteoblastic from osteolytic changes was evaluated. RESULTS The proposed wfTFI method was able to decrease the normalized root mean square error compared to the LFI and TFI methods in the simulation. The in vivo wfTFI susceptibility maps showed reduced BFR artifacts, noise amplification, and streaking artifacts compared to the LFI and TFI maps. wfTFI provided a significantly higher diagnostic confidence in differentiating osteolytic and osteoblastic lesions in the spine compared to the LFI method (p = .012). CONCLUSION The proposed wfTFI method can minimize BFR artifacts, noise amplification, and streaking artifacts in water-fat regions and can thus better differentiate between osteoblastic and osteolytic changes in patients with metastatic disease compared to LFI and the original TFI method.
Collapse
Affiliation(s)
- Christof Boehm
- Department of Diagnostic and Interventional Radiology, School of Medicine, Klinikum rechts der Isar, Technical University of Munich, Munich, Germany
| | - Nico Sollmann
- Department of Diagnostic and Interventional Neuroradiology, School of Medicine, Klinikum rechts der Isar, Technical University of Munich, Munich, Germany.,TUM-Neuroimaging Center, Klinikum rechts der Isar, Technical University of Munich, Munich, Germany.,Department of Diagnostic and Interventional Radiology, University Hospital Ulm, Ulm, Germany
| | | | - Stefan Ruschke
- Department of Diagnostic and Interventional Radiology, School of Medicine, Klinikum rechts der Isar, Technical University of Munich, Munich, Germany
| | - Michael Dieckmeyer
- Department of Diagnostic and Interventional Neuroradiology, School of Medicine, Klinikum rechts der Isar, Technical University of Munich, Munich, Germany
| | | | - Claus Zimmer
- Department of Diagnostic and Interventional Neuroradiology, School of Medicine, Klinikum rechts der Isar, Technical University of Munich, Munich, Germany.,TUM-Neuroimaging Center, Klinikum rechts der Isar, Technical University of Munich, Munich, Germany
| | - Marcus R Makowski
- Department of Diagnostic and Interventional Radiology, School of Medicine, Klinikum rechts der Isar, Technical University of Munich, Munich, Germany
| | - Thomas Baum
- Department of Diagnostic and Interventional Neuroradiology, School of Medicine, Klinikum rechts der Isar, Technical University of Munich, Munich, Germany
| | - Dimitrios C Karampinos
- Department of Diagnostic and Interventional Radiology, School of Medicine, Klinikum rechts der Isar, Technical University of Munich, Munich, Germany
| |
Collapse
|
41
|
Xu M, Guo Y, Cheng J, Xue K, Yang M, Song X, Feng Y, Cheng J. Brain iron assessment in patients with First-episode schizophrenia using quantitative susceptibility mapping. NEUROIMAGE-CLINICAL 2021; 31:102736. [PMID: 34186296 PMCID: PMC8254125 DOI: 10.1016/j.nicl.2021.102736] [Citation(s) in RCA: 26] [Impact Index Per Article: 6.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Received: 02/20/2021] [Revised: 04/30/2021] [Accepted: 06/17/2021] [Indexed: 11/28/2022]
Abstract
Patients with first-episode schizophrenia had significantly decreased QSM values in the bilateral substantia nigra, left red nucleus and left thalamus. Patients with first-episode schizophrenia had significantly increased regional volumes in the bilateral putamen and bilateral substantia nigra. QSM provides superior sensitivity over R2* mapping in the evaluation of schizophrenia-related iron alterations. QSM values in regions that showed intergroup differences did not exhibited significant correlations with PANSS scores. Purpose Decreased serum ferritin level was recently found in schizophrenia. Whether the brain iron concentration in schizophrenia exists abnormality is of research significance. Quantitative susceptibility mapping (QSM) was used in this study to assess brain iron changes in the grey matter nuclei of patients with first-episode schizophrenia. Methods The local ethics committee approved the study, and all subjects gave written informed consent. Thirty patients with first-episode schizophrenia and 30 age and gender-matched healthy controls were included in this study. QSM and effective transverse relaxation rate (R2*) maps were reconstructed from a three-dimensional multi-echo gradient-echo sequence. The inter-group differences of regional QSM values, R2* values and volumes were calculated in the grey matter nuclei, including bilateral caudate nucleus, putamen, globus pallidus, substantia nigra, red nucleus, and thalamus. The diagnostic performance of QSM and R2* was evaluated using receiver operating characteristic curve. The correlations between regional iron variations and clinical PANSS (Positive and Negative Syndrome Scale) scores were assessed using partial correlation analysis. Results Compared to healthy controls, patients with first-episode schizophrenia had significantly decreased QSM values (less paramagnetic) in the bilateral substantia nigra, left red nucleus and left thalamus (p < 0.05, FDR correction). QSM proved more sensitive than R2* regarding inter-group differences. The highest diagnostic performance for first-episode schizophrenia was observed in QSM value of the left substantia nigra (area under the curve, AUC = 0.718, p = 0.004). Regional volumes of bilateral putamen and bilateral substantia nigra were increased (p < 0.05, FDR correction) in first-episode schizophrenia. However, both QSM and R2* values did not show significant correlations with PANSS scores (p > 0.05). Conclusion This study reveals decreased iron concentration in grey matter nuclei of patients with first-episode schizophrenia. QSM provides superior sensitivity over R2* in the evaluation of schizophrenia-related brain iron changes. It demonstrated that QSM may be a potential biomarker for further understanding the pathophysiological mechanism of first-episode schizophrenia.
Collapse
Affiliation(s)
- Man Xu
- Department of MRI, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China
| | - Yihao Guo
- MR Collaboration, Siemens Healthcare Ltd, Guangzhou, China
| | - Junying Cheng
- Department of MRI, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China
| | - Kangkang Xue
- Department of MRI, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China
| | - Meng Yang
- Department of MRI, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China
| | - Xueqin Song
- Department of Psychiatry, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China
| | - Yanqiu Feng
- School of Biomedical Engineering, Southern Medical University, Guangzhou, China; Guangdong Provincial Key Laboratory of Medical Image Processing, Key Laboratory of Mental Health of the Ministry of Education & Guangdong-Hong Kong-Macao Greater Bay Area Center for Brain Science and Brain-Inspired Intelligence, Southern Medical University, Guangzhou, China.
| | - Jingliang Cheng
- Department of MRI, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China.
| |
Collapse
|
42
|
Gozt A, Hellewell S, Ward PGD, Bynevelt M, Fitzgerald M. Emerging Applications for Quantitative Susceptibility Mapping in the Detection of Traumatic Brain Injury Pathology. Neuroscience 2021; 467:218-236. [PMID: 34087394 DOI: 10.1016/j.neuroscience.2021.05.030] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/17/2021] [Revised: 05/24/2021] [Accepted: 05/25/2021] [Indexed: 12/16/2022]
Abstract
Traumatic brain injury (TBI) is a common but heterogeneous injury underpinned by numerous complex and interrelated pathophysiological mechanisms. An essential trace element, iron is abundant within the brain and involved in many fundamental neurobiological processes, including oxygen transportation, oxidative phosphorylation, myelin production and maintenance, as well as neurotransmitter synthesis and metabolism. Excessive levels of iron are neurotoxic and thus iron homeostasis is tightly regulated in the brain, however, many details about the mechanisms by which this is achieved are yet to be elucidated. A key mediator of oxidative stress, mitochondrial dysfunction and neuroinflammatory response, iron dysregulation is an important contributor to secondary injury in TBI. Advances in neuroimaging that leverage magnetic susceptibility properties have enabled increasingly comprehensive investigations into the distribution and behaviour of iron in the brain amongst healthy individuals as well as disease states such as TBI. Quantitative Susceptibility Mapping (QSM) is an advanced neuroimaging technique that promises quantitative estimation of local magnetic susceptibility at the voxel level. In this review, we provide an overview of brain iron and its homeostasis, describe recent advances enabling applications of QSM within the context of TBI and summarise the current state of the literature. Although limited, the emergent research suggests that QSM is a promising neuroimaging technique that can be used to investigate a host of pathophysiological changes that are associated with TBI.
Collapse
Affiliation(s)
- Aleksandra Gozt
- Curtin University, Faculty of Health Sciences, Curtin Health Innovation Research Institute, Bentley, WA Australia; Perron Institute for Neurological and Translational Science, Nedlands, WA Australia
| | - Sarah Hellewell
- Curtin University, Faculty of Health Sciences, Curtin Health Innovation Research Institute, Bentley, WA Australia
| | - Phillip G D Ward
- Australian Research Council Centre of Excellence for Integrative Brain Function, VIC Australia; Turner Institute for Brain and Mental Health, Monash University, VIC Australia
| | - Michael Bynevelt
- Neurological Intervention and Imaging Service of Western Australia, Sir Charles Gairdner Hospital, Nedlands, WA Australia
| | - Melinda Fitzgerald
- Curtin University, Faculty of Health Sciences, Curtin Health Innovation Research Institute, Bentley, WA Australia; Perron Institute for Neurological and Translational Science, Nedlands, WA Australia.
| |
Collapse
|
43
|
Wen Y, Spincemaille P, Nguyen T, Cho J, Kovanlikaya I, Anderson J, Wu G, Yang B, Fung M, Li K, Kelley D, Benhamo N, Wang Y. Multiecho complex total field inversion method (mcTFI) for improved signal modeling in quantitative susceptibility mapping. Magn Reson Med 2021; 86:2165-2178. [PMID: 34028868 DOI: 10.1002/mrm.28814] [Citation(s) in RCA: 14] [Impact Index Per Article: 3.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/20/2020] [Revised: 02/20/2021] [Accepted: 03/28/2021] [Indexed: 12/11/2022]
Abstract
PURPOSE Typical quantitative susceptibility mapping (QSM) reconstruction steps consist of first estimating the magnetization field from the gradient-echo images, and then reconstructing the susceptibility map from the estimated field. The errors from the field-estimation steps may propagate into the final QSM map, and the noise in the estimated field map may no longer be zero-mean Gaussian noise, thus, causing streaking artifacts in the resulting QSM. A multiecho complex total field inversion (mcTFI) method was developed to compute the susceptibility map directly from the multiecho gradient echo images using an improved signal model that retains the Gaussian noise property in the complex domain. It showed improvements in QSM reconstruction over the conventional field-to-source inversion. METHODS The proposed mcTFI method was compared with the nonlinear total field inversion (nTFI) method in a numerical brain with hemorrhage and calcification, the numerical brains provided by the QSM Challenge 2.0, 18 brains with intracerebral hemorrhage scanned at 3T, and 6 healthy brains scanned at 7T. RESULTS Compared with nTFI, the proposed mcTFI showed more accurate QSM reconstruction around the lesions in the numerical simulations. The mcTFI reconstructed QSM also showed the best image quality with the least artifacts in the brains with intracerebral hemorrhage scanned at 3T and healthy brains scanned at 7T. CONCLUSION The proposed multiecho complex total field inversion improved QSM reconstruction over traditional field-to-source inversion through better signal modeling.
Collapse
Affiliation(s)
- Yan Wen
- Meinig School of Biomedical Engineering, Cornell University, Ithaca, New York, USA.,Department of Radiology, Weill Cornell Medicine, New York, New York, USA
| | | | - Thanh Nguyen
- Department of Radiology, Weill Cornell Medicine, New York, New York, USA
| | - Junghun Cho
- Meinig School of Biomedical Engineering, Cornell University, Ithaca, New York, USA.,Department of Radiology, Weill Cornell Medicine, New York, New York, USA
| | - Ilhami Kovanlikaya
- Department of Radiology, Weill Cornell Medicine, New York, New York, USA
| | | | - Gaohong Wu
- General Electrical Healthcare, Waukesha, Wisconsin, USA
| | - Baolian Yang
- General Electrical Healthcare, Waukesha, Wisconsin, USA
| | - Maggie Fung
- General Electrical Healthcare, Waukesha, Wisconsin, USA
| | - Ke Li
- General Electrical Healthcare, Waukesha, Wisconsin, USA
| | | | | | - Yi Wang
- Meinig School of Biomedical Engineering, Cornell University, Ithaca, New York, USA.,Department of Radiology, Weill Cornell Medicine, New York, New York, USA
| |
Collapse
|
44
|
Lindemeyer J, Worthoff WA, Shymanskaya A, Shah NJ. Iterative Restoration of the Fringe Phase (REFRASE) for QSM. Front Neurosci 2021; 15:537666. [PMID: 34054401 PMCID: PMC8155380 DOI: 10.3389/fnins.2021.537666] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/24/2020] [Accepted: 04/01/2021] [Indexed: 12/03/2022] Open
Abstract
In quantitative susceptibility mapping (QSM), reconstructed results can be critically biased by misinterpreted or missing phase data near the edges of the brain support originating from the non-local relationship between field and susceptibility. These data either have to be excluded or corrected before further processing can take place. To address this, our iterative restoration of the fringe phase (REFRASE) approach simultaneously enhances the accuracy of multi-echo phase data QSM maps and the extent of the area available for evaluation. Data loss caused by strong local phase gradients near the surface of the brain support is recovered within the original phase data using harmonic and dipole-based fields extrapolated from a robust support region toward an extended brain mask. Over several iterations, phase data are rectified prior to the application of further QSM processing steps. The concept is successfully validated on numerical phantoms and brain scans from a cohort of volunteers. The increased extent of the mask and improved numerical stability within the segmented globus pallidus confirm the efficacy of the presented method in comparison to traditional evaluation.
Collapse
Affiliation(s)
- Johannes Lindemeyer
- Institute of Neuroscience and Medicine-4, Forschungszentrum Jülich, Jülich, Germany
| | - Wieland A Worthoff
- Institute of Neuroscience and Medicine-4, Forschungszentrum Jülich, Jülich, Germany
| | | | - N Jon Shah
- Institute of Neuroscience and Medicine-4, Forschungszentrum Jülich, Jülich, Germany.,Institute of Neuroscience and Medicine-11, Forschungszentrum Jülich, Jülich, Germany.,JARA-BRAIN-Translational Medicine, Aachen, Germany.,Department of Neurology, Rheinisch-Westfälische Technische Hochschule (RWTH) Aachen University, Aachen, Germany
| |
Collapse
|
45
|
Xu J, Xiao C, Song W, Cui X, Pan M, Wang Q, Feng Y, Xu Y. Elevated Heme Oxygenase-1 Correlates With Increased Brain Iron Deposition Measured by Quantitative Susceptibility Mapping and Decreased Hemoglobin in Patients With Parkinson's Disease. Front Aging Neurosci 2021; 13:656626. [PMID: 33815094 PMCID: PMC8012799 DOI: 10.3389/fnagi.2021.656626] [Citation(s) in RCA: 23] [Impact Index Per Article: 5.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/21/2021] [Accepted: 02/26/2021] [Indexed: 11/18/2022] Open
Abstract
Background: Brain iron deposition, low hemoglobin (HGB), and increased heme oxygenase-1 (HO-1) have been implicated in Parkinson’s disease (PD). However, the association among them in PD is poorly studied. Objective: To explore the association of the level of HO-1 with brain iron deposition and low level of HGB in PD. Methods: A total of 32 patients with PD and 26 controls were recruited for this study. C57BL/6 male mice were used in generating 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-induced chronic PD model. The Levels of serum HO-1 and HGB of human subjects and mice were assayed by ELISA, blood routine test, respectively. Quantitative susceptibility mapping (QSM) was used to quantitatively analyze brain iron deposition in human subjects and mice. HO-1 inhibitor (Sn-protoporphyrin, SnPP) was used to suppress the function and expression of HO-1 in PD mice. Correlations between the concentration of serum HO-1 and iron deposition of the region of interests (ROIs), levels of HGB, between the three factors mentioned above, and scores of clinical scales were explored in PD patients. Results: This study revealed significant elevation of the serum HO-1 concentration, iron deposition within bilateral substantial nigra (SN), red nucleus (RN), and putamen (PUT) and decrease of HGB level in PD patients. There was a significantly positive correlation between the serum HO-1 concentration and iron deposition within SN, an inverse correlation between the serum HO-1 concentration and HGB level in PD patients. A significant increase in HO-1 expression of serum and iron deposition in SN was also observed in the PD mouse model, and the SnPP could significantly reduce iron deposition in the SN. Conclusions: The high level of HO-1 may be the common mechanism of iron deposition and low HGB in PD. Therefore, the findings presented in this study indicate that HO-1 correlates with brain iron deposition and anemia in PD.
Collapse
Affiliation(s)
- Jinghui Xu
- Department of Neurology, Nanfang Hospital, Southern Medical University, Guangzhou, China.,Department of Rehabilitation Medicine, The Third Affiliated Hospital, Sun Yat-sen University, Guangzhou, China
| | - Chi Xiao
- Department of Neurology, Nanfang Hospital, Southern Medical University, Guangzhou, China
| | - Weizheng Song
- Department of Neurosurgery, the Eighth People's Hospital of Chengdu, Chengdu, China
| | - Xiangqin Cui
- Department of Neurology, Nanfang Hospital, Southern Medical University, Guangzhou, China
| | - Mengqiu Pan
- Department of Neurology, Guangdong 999 Brain Hospital, Guangzhou, China
| | - Qun Wang
- Department of Neurology, Nanfang Hospital, Southern Medical University, Guangzhou, China
| | - Yanqiu Feng
- Guangdong Provincial Key Laboratory of Medical Image Processing, Southern Medical University, Guangzhou, China
| | - Yunqi Xu
- Department of Neurology, Nanfang Hospital, Southern Medical University, Guangzhou, China
| |
Collapse
|
46
|
Dimov AV, Christoforidis GA, Saadat N, Liu MM, Jeong YI, Roth S, Niekrasz M, Carroll TJ. QSM in canine model of acute cerebral ischemia: A pilot study. Magn Reson Med 2021; 85:1602-1610. [PMID: 33034078 DOI: 10.1002/mrm.28498] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/25/2020] [Revised: 06/28/2020] [Accepted: 08/05/2020] [Indexed: 11/07/2022]
Abstract
PURPOSE In the present study, we investigated the potential of QSM to assess the physiological state of cortical tissue in the middle cerebral artery occlusion canine model of a cerebral ischemia. METHODS Experiments were performed in 8 anesthetized canines. Gradient echo, perfusion, and DWI data of brains at normal and ischemic states were acquired. In the postprocessed susceptibility and quantitative cerebral blood flow maps, changes in values within the middle cerebral artery-fed cortical territories were quantified both on the ischemic and normal contralateral hemisphere side. RESULTS QSM values in critically ischemic tissue were significantly different from contralateral values-namely, susceptibility increase was observed in the cases in which cerebral perfusion was maintained above the threshold of neuronal death. Furthermore, the data indicates presence of a significant correlation between the changes in susceptibility values, cerebral perfusion, and the infarct volume and pial collateral scores. Additionally, our data suggests that difference in cortical susceptibility is prospectively indicative of the infarct growth rate. CONCLUSION In an experimental permanent middle cerebral artery occlusion model, QSM was shown to correlate with the functional parameters characterizing viability of ischemic tissue, thus warranting further research on its ability to provide complementary information during acute stroke MRI examinations in humans.
Collapse
Affiliation(s)
- Alexey V Dimov
- Department of Radiology, University of Chicago, Chicago, Illinois, USA
| | | | - Niloufar Saadat
- Department of Radiology, University of Chicago, Chicago, Illinois, USA
| | - Mira M Liu
- Department of Radiology, University of Chicago, Chicago, Illinois, USA
| | - Yong I Jeong
- Department of Radiology, University of Chicago, Chicago, Illinois, USA
| | - Steven Roth
- Department of Anesthesiology, University of Illinois, College of Medicine, Chicago, Illinois, USA
| | - Marek Niekrasz
- Department of Surgery, University of Chicago, Chicago, Illinois, USA
| | - Timothy J Carroll
- Department of Radiology, University of Chicago, Chicago, Illinois, USA
| |
Collapse
|
47
|
|
48
|
Chary K, Nissi MJ, Nykänen O, Manninen E, Rey RI, Shmueli K, Sierra A, Gröhn O. Quantitative susceptibility mapping of the rat brain after traumatic brain injury. NMR IN BIOMEDICINE 2021; 34:e4438. [PMID: 33219598 DOI: 10.1002/nbm.4438] [Citation(s) in RCA: 15] [Impact Index Per Article: 3.8] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 06/22/2019] [Revised: 10/13/2020] [Accepted: 10/14/2020] [Indexed: 06/11/2023]
Abstract
The primary lesion arising from the initial insult after traumatic brain injury (TBI) triggers a cascade of secondary tissue damage, which may also progress to connected brain areas in the chronic phase. The aim of this study was, therefore, to investigate variations in the susceptibility distribution related to these secondary tissue changes in a rat model after severe lateral fluid percussion injury. We compared quantitative susceptibility mapping (QSM) and R2 * measurements with histological analyses in white and grey matter areas outside the primary lesion but connected to the lesion site. We demonstrate that susceptibility variations in white and grey matter areas could be attributed to reduction in myelin, accumulation of iron and calcium, and gliosis. QSM showed quantitative changes attributed to secondary damage in areas located rostral to the lesion site that appeared normal in R2 * maps. However, combination of QSM and R2 * was informative in disentangling the underlying tissue changes such as iron accumulation, demyelination, or calcifications. Therefore, combining QSM with R2 * measurement can provide a more detailed assessment of tissue changes and may pave the way for improved diagnosis of TBI, and several other complex neurodegenerative diseases.
Collapse
Affiliation(s)
- Karthik Chary
- A. I. Virtanen Institute for Molecular Sciences, University of Eastern Finland, Kuopio, Finland
| | - Mikko J Nissi
- Department of Applied Physics, University of Eastern Finland, Kuopio, Finland
- Research Unit of Medical Imaging, Physics and Technology, University of Oulu, Oulu, Finland
| | - Olli Nykänen
- Department of Applied Physics, University of Eastern Finland, Kuopio, Finland
| | - Eppu Manninen
- A. I. Virtanen Institute for Molecular Sciences, University of Eastern Finland, Kuopio, Finland
| | - Ramón I Rey
- Clinical Neurosciences Research Laboratory, Department of Neurology, Health Research Institute of Santiago de Compostela, University of Santiago de Compostela, Santiago de Compostela, Spain
| | - Karin Shmueli
- Department of Medical Physics and Biomedical Engineering, University College London, London, UK
| | - Alejandra Sierra
- A. I. Virtanen Institute for Molecular Sciences, University of Eastern Finland, Kuopio, Finland
| | - Olli Gröhn
- A. I. Virtanen Institute for Molecular Sciences, University of Eastern Finland, Kuopio, Finland
| |
Collapse
|
49
|
Karsa A, Punwani S, Shmueli K. An optimized and highly repeatable MRI acquisition and processing pipeline for quantitative susceptibility mapping in the head-and-neck region. Magn Reson Med 2020; 84:3206-3222. [PMID: 32621302 DOI: 10.1002/mrm.28377] [Citation(s) in RCA: 23] [Impact Index Per Article: 4.6] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/19/2019] [Revised: 05/06/2020] [Accepted: 05/23/2020] [Indexed: 02/11/2024]
Abstract
PURPOSE Quantitative Susceptibility Mapping (QSM) is an emerging technique sensitive to disease-related changes including oxygenation. It is extensively used in brain studies and has increasing clinical applications outside the brain. Here we present the first MRI acquisition protocol and QSM pipeline optimized for the head-and-neck region together with a repeatability analysis performed in healthy volunteers. METHODS We investigated both the intrasession and the intersession repeatability of the optimized method in 10 subjects. We also implemented two, Tikhonov-regularisation-based susceptibility calculation techniques that were found to have higher contrast-to-noise than existing methods in the head-and-neck region. Repeatability was evaluated by calculating the distributions of susceptibility differences between repeated scans and the corresponding minimum detectable effect sizes (MDEs). RESULTS Deep brain regions had higher QSM repeatability than neck regions. As expected, intrasession repeatability was generally better than intersession repeatability. Susceptibility maps calculated using projection onto dipole fields for background field removal were more repeatable than using the Laplacian boundary value method in the head-and-neck region. Small (short-axis diameter <5 mm) lymph nodes had the lowest repeatability (MDE = 0.27 ppm) as imperfect segmentation included some of the surrounding paramagnetic fatty fascia, highlighting the importance of accurate region delineation. MDEs in the larger lymph nodes (0.16 ppm), submandibular glands (0.10 ppm), and especially the parotid glands (0.06 ppm) were much lower, comparable to those of the brain regions. CONCLUSIONS The high repeatability of the acquisition and pipeline optimized for QSM will facilitate clinical studies in the head-and-neck region.
Collapse
Affiliation(s)
- Anita Karsa
- Department of Medical Physics and Biomedical Engineering, University College London, London, United Kingdom
- Centre for Medical Imaging, University College London, London, United Kingdom
| | - Shonit Punwani
- Centre for Medical Imaging, University College London, London, United Kingdom
| | - Karin Shmueli
- Department of Medical Physics and Biomedical Engineering, University College London, London, United Kingdom
- Centre for Medical Imaging, University College London, London, United Kingdom
| |
Collapse
|
50
|
Boehm C, Diefenbach MN, Makowski MR, Karampinos DC. Improved body quantitative susceptibility mapping by using a variable-layer single-min-cut graph-cut for field-mapping. Magn Reson Med 2020; 85:1697-1712. [PMID: 33151604 DOI: 10.1002/mrm.28515] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/17/2020] [Revised: 08/20/2020] [Accepted: 08/21/2020] [Indexed: 12/18/2022]
Abstract
PURPOSE To develop a robust algorithm for field-mapping in the presence of water-fat components, large B 0 field inhomogeneities and MR signal voids and to apply the developed method in body applications of quantitative susceptibility mapping (QSM). METHODS A framework solving the cost-function of the water-fat separation problem in a single-min-cut graph-cut based on the variable-layer graph construction concept was developed. The developed framework was applied to a numerical phantom enclosing an MR signal void, an air bubble experimental phantom, 14 large field of view (FOV) head/neck region in vivo scans and to 6 lumbar spine in vivo scans. Field-mapping and subsequent QSM results using the proposed algorithm were compared to results using an iterative graph-cut algorithm and a formerly proposed single-min-cut graph-cut. RESULTS The proposed method was shown to yield accurate field-map and susceptibility values in all simulation and in vivo datasets when compared to reference values (simulation) or literature values (in vivo). The proposed method showed improved field-map and susceptibility results compared to iterative graph-cut field-mapping especially in regions with low SNR, strong field-map variations and high R 2 ∗ values. CONCLUSIONS A single-min-cut graph-cut field-mapping method with a variable-layer construction was developed for field-mapping in body water-fat regions, improving quantitative susceptibility mapping particularly in areas close to MR signal voids.
Collapse
Affiliation(s)
- Christof Boehm
- Department of Diagnostic and Interventional Radiology, Technical University of Munich, Munich, Germany
| | - Maximilian N Diefenbach
- Department of Diagnostic and Interventional Radiology, Technical University of Munich, Munich, Germany.,Division of Infectious Diseases and Tropical Medicine, University Hospital, LMU Munich, Munich, Germany
| | - Marcus R Makowski
- Department of Diagnostic and Interventional Radiology, Technical University of Munich, Munich, Germany
| | - Dimitrios C Karampinos
- Department of Diagnostic and Interventional Radiology, Technical University of Munich, Munich, Germany
| |
Collapse
|