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It's a thin line: development and validation of Dixon MRI-based semi-quantitative assessment of stress-related bone marrow edema in the wrists of young gymnasts and non-gymnasts

Kox, L S; Kraan, R B J; Mazzoli, V; Mens, M A; Kerkhoffs, G M J J; Nederveen, A J; Maas, M
PURPOSE/OBJECTIVE:To assess reliability and clinical utility of evaluating stress-related metaphyseal water distribution using a semi-quantitative Dixon MRI-based method for early diagnosis of physeal stress injuries in adolescent gymnasts. METHODS:Twenty-four gymnasts with clinically suspected overuse injury of the distal radial physis, 18 asymptomatic gymnasts, and 24 non-gymnast controls aged 12 ± 1.5 years prospectively underwent hand radiographs and 3T MRI of the wrist including coronal T1-weighted and T2-weighted Dixon sequences. Two raters measured metaphyseal water signal fraction in 13 radial and ulnar regions of interest (ROI). Inter- and intrarater reliability, interslice (between 3 middle radial slices), and inter-ROI (between 3 ROIs on same level) reliability were assessed using intraclass correlation coefficients (ICC). Water signal fractions and their within-person ratios in distal versus most proximal ROIs were compared between groups using one-way analysis of variance. RESULTS:Inter- and intrarater ICCs were 0.79-0.99 and 0.94-1.0 for T1-weighted, and 0.88-1.0 and 0.88-1.0 for T2-weighted Dixon. Interslice and inter-ROI ICCs were 0.55-0.94 and 0.95-0.97 for T1-weighted, and 0.70-0.96 and 0.96-0.97 for T2-weighted Dixon. Metaphyseal water signal fraction in symptomatic gymnasts was higher in six distal ROIs compared with asymptomatic gymnasts and in nine ROIs compared with non-gymnasts (p < 0.05). Metaphyseal water score (ratio of distal versus most proximal ROIs) was 1.61 in symptomatic gymnasts and 1.35 in asymptomatic gymnasts on T2-weighted Dixon (p < 0.05). CONCLUSION/CONCLUSIONS:Semi-quantitative Dixon MRI-based water signal fraction assessment has good to excellent reproducibility and shows increased metaphyseal water scores in symptomatic gymnasts compared with asymptomatic gymnastic peers. KEY POINTS/CONCLUSIONS:• The proposed Dixon MRI-based semi-quantitative method for assessment of metaphyseal bone marrow water content is reliable, with off-the-shelf availability and short scan times. • The metaphyseal water score allows comparisons between gymnasts using a within-person reference area for unaffected metaphyseal bone. • As metaphyseal water score was increased in symptomatic gymnasts compared with asymptomatic gymnasts, this semi-quantitative method can potentially be used as an indicator of bone marrow edema in the early diagnosis of gymnastic physeal stress injury.
PMCID:7033069
PMID: 31776745
ISSN: 1432-1084
CID: 5579122

Crossing muscle fibers of the human tongue resolved in vivo using constrained spherical deconvolution

Voskuilen, Luuk; Mazzoli, Valentina; Oudeman, Jos; Balm, Alfons J M; van der Heijden, Ferdinand; Froeling, Martijn; de Win, Maartje M L; Strijkers, Gustav J; Smeele, Ludi E; Nederveen, Aart J
BACKGROUND:Surgical resection of tongue cancer may impair swallowing and speech. Knowledge of tongue muscle architecture affected by the resection could aid in patient counseling. Diffusion tensor imaging (DTI) enables reconstructions of muscle architecture in vivo. Reconstructing crossing fibers in the tongue requires a higher-order diffusion model. PURPOSE:To develop a clinically feasible diffusion imaging protocol, which facilitates both DTI and constrained spherical deconvolution (CSD) reconstructions of tongue muscle architecture in vivo. STUDY TYPE:Cross-sectional study. SUBJECTS/SPECIMEN:One ex vivo bovine tongue resected en bloc from mandible to hyoid bone. Ten healthy volunteers (mean age 25.5 years; range 21-34 years; four female). FIELD STRENGTH/SEQUENCE:-field inhomogeneity correction. The scan of the healthy volunteers was divided into four parts, in between which the volunteers were allowed to swallow, resulting in a total acquisition time of 10 minutes. ASSESSMENT:The ability of resolving crossing muscle fibers using CSD was determined on the bovine tongue specimen. A reproducible response function was estimated and the optimal peak threshold was determined for the in vivo tongue. The quality of tractography of the in vivo tongue was graded by three experts. STATISTICAL TESTS:The within-subject coefficient of variance was calculated for the response function. The qualitative results of the grading of DTI and CSD tractography were analyzed using a multilevel proportional odds model. RESULTS:Fiber orientation distributions in the bovine tongue specimen showed that CSD was able to resolve crossing muscle fibers. The response function could be determined reproducibly in vivo. CSD tractography displayed significantly improved tractography compared with DTI tractography (P = 0.015). DATA CONCLUSION:The 10-minute diffusion imaging protocol facilitates CSD fiber tracking with improved reconstructions of crossing tongue muscle fibers compared with DTI. LEVEL OF EVIDENCE:2 Technical Efficacy: Stage 1 J. Magn. Reson. Imaging 2019;50:96-105.
PMCID:6617996
PMID: 30648339
ISSN: 1522-2586
CID: 5579072

A noninvasive MRI based approach to estimate the mechanical properties of human knee ligaments

Naghibi, Hamid; Mazzoli, Valentina; Gijsbertse, Kaj; Hannink, Gerjon; Sprengers, Andre; Janssen, Dennis; Van den Boogaard, Ton; Verdonschot, Nico
Characterization of the main tibiofemoral ligaments is an essential step in developing patient-specific computational models of the knee joint for personalized surgery pre-planning. Tensile tests are commonly performed in-vitro to characterize the mechanical stiffness and rupture force of the knee ligaments which makes the technique unsuitable for in-vivo application. The time required for the limited noninvasive approaches for properties estimation based on knee laxity remained the main obstacle in clinical implementation. Magnetic resonance imaging (MRI) technique can be a platform to noninvasively assess the knee ligaments. In this study the aim was to explore the potential role of quantitative MRI and dimensional properties, in characterizing the mechanical properties of the main tibiofemoral ligaments. After MR scanning of six cadaveric legs, all 24 main tibiofemoral bone-ligaments-bone specimens were tested in vitro. During the tensile test cross sectional area of the specimens was captured using ultrasound and force-displacement curve was extracted. Digital image correlation technique was implemented to check the strain behavior of the specimen and rupture region and to assure the fixation of ligament bony block during the test. The volume of the specimen was measured using manual segmentation data, and quantitative MR parameters as T2
PMID: 30769233
ISSN: 1878-0180
CID: 5579082

Accelerated 4D phase contrast MRI in skeletal muscle contraction

Mazzoli, Valentina; Gottwald, Lukas M; Peper, Eva S; Froeling, Martijn; Coolen, Bram F; Verdonschot, Nico; Sprengers, Andre M; van Ooij, Pim; Strijkers, Gustav J; Nederveen, Aart J
PURPOSE:3D time-resolved (4D) phase contrast MRI can be used to study muscle contraction. However, 3D coverage with sufficient spatiotemporal resolution can only be achieved by interleaved acquisitions during many repetitions of the motion task, resulting in long scan times. The aim of this study was to develop a compressed sensing accelerated 4D phase contrast MRI technique for quantification of velocities and strain rate of the muscles in the lower leg during active plantarflexion/dorsiflexion. METHODS:Nine healthy volunteers were scanned during active dorsiflexion/plantarflexion task. For each volunteer, we acquired a reference scan, as well as 4 different accelerated scans (k-space undersampling factors: 3.14X, 4.09X, 4.89X, and 6.41X) obtained using Cartesian Poisson disk undersampling schemes. The data was reconstructed using a compressed sensing pipeline. For each scan, velocity and strain rate values were quantified in the gastrocnemius lateralis, gastrocnemius medialis, tibialis anterior, and soleus. RESULTS:) was consistently 0 for all the acquisitions. No significant differences were observed for the strain rate eigenvalues as a function of acceleration factor. CONCLUSIONS:Data undersampling combined with compressed sensing reconstruction allowed obtainment of time-resolved phase contrast acquisitions with 3D coverage and quantitative information comparable to the reference scan. The 3D sensitivity of the method can help in understanding the connection between muscle architecture and muscle function in future studies.
PMID: 29508449
ISSN: 1522-2594
CID: 5579052

An advanced magnetic resonance imaging perspective on the etiology of deep tissue injury

Nelissen, Jules L; Traa, Willeke A; de Boer, Hans H; de Graaf, Larry; Mazzoli, Valentina; Savci-Heijink, C Dilara; Nicolay, Klaas; Froeling, Martijn; Bader, Dan L; Nederveen, Aart J; Oomens, Cees W J; Strijkers, Gustav J
Early diagnosis of deep tissue injury remains problematic due to the complicated and multifactorial nature of damage induction and the many processes involved in damage development and recovery. In this paper, we present a comprehensive assessment of deep tissue injury development and remodeling in a rat model by multiparametric magnetic resonance imaging (MRI) and histopathology. The tibialis anterior muscle of rats was subjected to mechanical deformation for 2 h. Multiparametric in vivo MRI, consisting of T2, T2*, mean diffusivity (MD), and angiography measurements, was applied before, during, and directly after indentation as well as at several time points during a 14-day follow-up. MRI readouts were linked to histological analyses of the damaged tissue. The results showed dynamic change in various MRI parameters, reflecting the histopathological status of the tissue during damage induction and repair. Increased T2 corresponded with edema, muscle cell damage, and inflammation. T2* was related to tissue perfusion, hemorrhage, and inflammation. MD increase and decrease was reported on the tissue's microstructural integrity and reflected muscle degeneration and edema as well as fibrosis. Angiography provided information on blockage of blood flow during deformation. Our results indicate that the effects of a single damage-causing event of only 2 h of deformation were present up to 14 days. The initial tissue response to deformation, as observed by MRI, starts at the edge of the indentation. The quantitative MRI readouts provided distinct and complementary information on the extent, temporal evolution, and microstructural basis of deep tissue injury-related muscle damage. NEW & NOTEWORTHY We have applied a multiparametric MRI approach linked to histopathology to characterize damage development and remodeling in a rat model of deep tissue injury. Our approach provided several relevant insights in deep tissue injury. Response to damage, as observed by MRI, started at some distance from the deformation. Damage after a single indentation period persisted up to 14 days. The MRI parameters provided distinct and complementary information on the microstructural basis of the damage.
PMID: 29494291
ISSN: 1522-1601
CID: 5579042

Accelerated 4D self-gated MRI of tibiofemoral kinematics

Mazzoli, Valentina; Schoormans, Jasper; Froeling, Martijn; Sprengers, Andre M; Coolen, Bram F; Verdonschot, Nico; Strijkers, Gustav J; Nederveen, Aart J
Anatomical (static) magnetic resonance imaging (MRI) is the most useful imaging technique for the evaluation and assessment of internal derangement of the knee, but does not provide dynamic information and does not allow the study of the interaction of the different tissues during motion. As knee pain is often only experienced during dynamic tasks, the ability to obtain four-dimensional (4D) images of the knee during motion could improve the diagnosis and provide a deeper understanding of the knee joint. In this work, we present a novel approach for dynamic, high-resolution, 4D imaging of the freely moving knee without the need for external triggering. The dominant knee of five healthy volunteers was scanned during a flexion/extension task. To evaluate the effects of non-uniform motion and poor coordination skills on the quality of the reconstructed images, we performed a comparison between fully free movement and movement instructed by a visual cue. The trigger signal for self-gating was extracted using principal component analysis (PCA), and the images were reconstructed using a parallel imaging and compressed sensing reconstruction pipeline. The reconstructed 4D movies were scored for image quality and used to derive bone kinematics through image registration. Using our method, we were able to obtain 4D high-resolution movies of the knee without the need for external triggering hardware. The movies obtained with and without instruction did not differ significantly in terms of image scoring and quantitative values for tibiofemoral kinematics. Our method showed to be robust for the extraction of the self-gating signal even for uninstructed motion. This can make the technique suitable for patients who, as a result of pain, may find it difficult to comply exactly with instructions. Furthermore, bone kinematics can be derived from accelerated MRI without the need for additional hardware for triggering.
PMID: 28873255
ISSN: 1099-1492
CID: 5579022

Water and fat separation in real-time MRI of joint movement with phase-sensitive bSSFP

Mazzoli, Valentina; Nederveen, Aart J; Oudeman, Jos; Sprengers, Andre; Nicolay, Klaas; Strijkers, Gustav J; Verdonschot, Nico
PURPOSE:To introduce a method for obtaining fat-suppressed images in real-time MRI of moving joints at 3 Tesla (T) using a bSSFP sequence with phase detection to enhance visualization of soft tissue structures during motion. METHODS:The wrist and knee of nine volunteers were imaged with a real-time bSSFP sequence while performing dynamic tasks. For appropriate choice of sequence timing parameters, water and fat pixels showed an out-of-phase behavior, which was exploited to reconstruct water and fat images. Additionally, a 2-point Dixon sequence was used for dynamic imaging of the joints, and resulting water and fat images were compared with our proposed method. RESULTS:The joints could be visualized with good water-fat separation and signal-to-noise ratio (SNR), while maintaining a relatively high temporal resolution (5 fps in knee imaging and 10 fps in wrist imaging). The proposed method produced images of moving joints with higher SNR and higher image quality when compared with the Dixon method. CONCLUSIONS:Water-fat separation is feasible in real-time MRI of moving knee and wrist at 3 T. PS-bSSFP offers movies with higher SNR and higher diagnostic quality when compared with Dixon scans. Magn Reson Med 78:58-68, 2017. © 2016 International Society for Magnetic Resonance in Medicine.
PMID: 27417271
ISSN: 1522-2594
CID: 5578992

Assessment of passive muscle elongation using Diffusion Tensor MRI: Correlation between fiber length and diffusion coefficients

Mazzoli, Valentina; Oudeman, Jos; Nicolay, Klaas; Maas, Mario; Verdonschot, Nico; Sprengers, Andre M; Nederveen, Aart J; Froeling, Martijn; Strijkers, Gustav J
In this study we investigated the changes in fiber length and diffusion parameters as a consequence of passive lengthening and stretching of the calf muscles. We hypothesized that changes in radial diffusivity (RD) are caused by changes in the muscle fiber cross sectional area (CSA) as a consequence of lengthening and shortening of the muscle. Diffusion Tensor MRI (DT-MRI) measurements were made twice in five healthy volunteers, with the foot in three different positions (30° plantarflexion, neutral position and 15° dorsiflexion). The muscles of the calf were manually segmented on co-registered high resolution anatomical scans, and maps of RD and axial diffusivity (AD) were reconstructed from the DT-MRI data. Fiber tractography was performed and mean fiber length was calculated for each muscle group. Significant negative correlations were found between the changes in RD and changes in fiber length in the dorsiflexed and plantarflexed positions, compared with the neutral foot position. Changes in AD did not correlate with changes in fiber length. Assuming a simple cylindrical model with constant volume for the muscle fiber, the changes in the muscle fiber CSA were calculated from the changes in fiber length. In line with our hypothesis, we observed a significant positive correlation of the CSA with the measured changes in RD. In conclusion, we showed that changes in diffusion coefficients induced by passive muscle stretching and lengthening can be explained by changes in muscle CSA, advancing the physiological interpretation of parameters derived from skeletal muscle DT-MRI.
PMID: 27862471
ISSN: 1099-1492
CID: 5579002

A novel diffusion-tensor MRI approach for skeletal muscle fascicle length measurements

Oudeman, Jos; Mazzoli, Valentina; Marra, Marco A; Nicolay, Klaas; Maas, Mario; Verdonschot, Nico; Sprengers, Andre M; Nederveen, Aart J; Strijkers, Gustav J; Froeling, Martijn
Musculoskeletal (dys-)function relies for a large part on muscle architecture which can be obtained using Diffusion-Tensor MRI (DT-MRI) and fiber tractography. However, reconstructed tracts often continue along the tendon or aponeurosis when using conventional methods, thus overestimating fascicle lengths. In this study, we propose a new method for semiautomatic segmentation of tendinous tissue using tract density (TD). We investigated the feasibility and repeatability of this method to quantify the mean fascicle length per muscle. Additionally, we examined whether the method facilitates measuring changes in fascicle length of lower leg muscles with different foot positions. Five healthy subjects underwent two DT-MRI scans of the right lower leg, with the foot in 15° dorsiflexion, neutral, and 30° plantarflexion positions. Repeatability of fascicle length measurements was assessed using Bland-Altman analysis. Changes in fascicle lengths between the foot positions were tested using a repeated multivariate analysis of variance (MANOVA). Bland-Altman analysis showed good agreement between repeated measurements. The coefficients of variation in neutral position were 8.3, 16.7, 11.2, and 10.4% for soleus (SOL), fibularis longus (FL), extensor digitorum longus (EDL), and tibialis anterior (TA), respectively. The plantarflexors (SOL and FL) showed significant increase in fascicle length from plantarflexion to dorsiflexion, whereas the dorsiflexors (EDL and TA) exhibited a significant decrease. The use of a tract density for semiautomatic segmentation of tendinous structures provides more accurate estimates of the mean fascicle length than traditional fiber tractography methods. The method shows moderate to good repeatability and allows for quantification of changes in fascicle lengths due to passive stretch.
PMCID:5210383
PMID: 28003562
ISSN: 2051-817x
CID: 5579012

Diffusion-prepared neurography of the brachial plexus with a large field-of-view at 3T

Oudeman, Jos; Coolen, Bram F; Mazzoli, Valentina; Maas, Mario; Verhamme, Camiel; Brink, Wyger M; Webb, Andrew G; Strijkers, Gustav J; Nederveen, Aart J
PURPOSE/OBJECTIVE:To study diffusion-prepared neurography optimized for a large field-of-view (FOV) to include the neck and both shoulders. In a large FOV poor homogeneity of the magnetic field (B0 ) often leads to poor image quality and possibly to poor diagnostic accuracy. The aim was therefore to find an optimal (combination of) shimming method(s) for diffusion-prepared neurography in a large FOV. MATERIALS AND METHODS/METHODS:A 3D diffusion-prepared sequence with a large FOV was tested with and without the use of a susceptibility-matched pillow combined with image-based (IB) or standard shimming in six healthy volunteers on a 3T system. B0 , B1 , signal to noise ratio (SNR), and contrast to noise ratio (CNR) were compared between all protocols. Additionally, nerve visibility, fat suppression, artifacts, and overall image quality were ordinally (5-point scale) assessed by two readers. Furthermore, correlations between B0 and B1 (offset and variation) and SNR, CNR, and image quality were explored. RESULTS:The use of the susceptibility-matched pillow led to a 43% reduction of B0 variation over the brachial plexus compared to the situation without a pillow (P < 0.05). The combination of the pillow with IB-shimming and the optimized diffusion-prepared sequence resulted in good nerve visibility, good fat suppression, no artifacts that would hinder clinical diagnosis, and a good overall quality (median scores ≥4). Reducing B0 variation was associated with SNR, CNR, and the above-mentioned scored features (P < 0.05). CONCLUSION/CONCLUSIONS:The use of a susceptibility-matched pillow in combination with IB-shimming enables robust and high-quality neurography of the complete brachial plexus.
PMID: 26251015
ISSN: 1522-2586
CID: 5578982