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Concussion is commonly characterized by a cascade of neurometabolic changes following injury. Magnetic Resonance Spectroscopy (MRS) can be used to quantify neurometabolites non-invasively. Longitudinal changes in neurometabolites have rarely been studied in pediatric concussion, and fewer studies consider symptoms. This study examines longitudinal changes of neurometabolites in pediatric concussion and associations between neurometabolites and symptom burden. Participants who presented with concussion or orthopedic injury (OI, comparison group) were recruited. The first timepoint for MRS data collection was at a mean of 12 days post-injury (n = 545). Participants were then randomized to 3 (n = 243) or 6 (n = 215) months for MRS follow-up. Parents completed symptom questionnaires to quantify somatic and cognitive symptoms at multiple timepoints following injury. There were no significant changes in neurometabolites over time in the concussion group and neurometabolite trajectories did not differ between asymptomatic concussion, symptomatic concussion, and OI groups. Cross-sectionally, Choline was significantly lower in those with persistent somatic symptoms compared to OI controls at 3 months post-injury. Lower Choline was also significantly associated with higher somatic symptoms. Although overall neurometabolites do not change over time, choline differences that appear at 3 months and is related to somatic symptoms.
Injuries and illnesses can alter the normal bilateral symmetry of the brain, and determining the extent of this disruption may be useful in characterizing the pathology. One way of quantifying brain symmetry is in terms of bilateral correlation of diffusion tensor metrics between homologous white matter tracts. With this approach, we hypothesized that the brains of patients with a concussion are more asymmetrical than those of healthy individuals without a history of a concussion. We scanned the brains of 35 normal individuals and 15 emergency department patients with a recent concussion. Fractional anisotropy (FA), mean diffusivity (MD), axial diffusivity (AD), and radial diffusivity (RD) were determined for regions of interest (ROI) defined by a standard white-matter atlas that included 21 bilateral ROIs. For each ROI pair, bilateral correlation coefficients were calculated and compared between the two subject groups. A symmetry index, defined as the ratio between the difference and the sum of bilateral measures, was also calculated for each ROI pair and compared between the groups. We found that in normal subjects, the extent of symmetry varied among regions and individuals, and at least subtle forms of structural lateralization were common across regions. In patients, higher asymmetry was found overall as well as in the corticospinal tract specifically. Results indicate that a concussion can manifest in brain asymmetry that deviates from a normal state. The clinical utility of characterizing post-concussion pathology as abnormal brain asymmetry merits further exploration.
Studies using blood-oxygenation-level-dependent functional magnetic resonance imaging (BOLD fMRI) have characterized how the resting brain is affected by concussion. The literature to date, however, has largely focused on measuring changes in the spatial organization of functional brain networks. In the present study, changes in the temporal dynamics of BOLD signals are examined throughout concussion recovery using scaling (or fractal) analysis. Imaging data were collected for 228 university-level athletes, 61 with concussion and 167 athletic controls. Concussed athletes were scanned at the acute phase of injury (1-7 days postinjury), the subacute phase (8-14 days postinjury), medical clearance to return to sport (RTS), 1 month post-RTS and 1 year post-RTS. The wavelet leader multifractal approach was used to assess scaling ( c1 ) and multifractal ( c2 ) behavior. Significant longitudinal changes were identified for c1 , which was lowest at acute injury, became significantly elevated at RTS, and returned near control levels by 1 year post-RTS. No longitudinal changes were identified for c2 . Secondary analyses showed that clinical measures of acute symptom severity and time to RTP were related to longitudinal changes in c1 . Athletes with both higher symptoms and prolonged recovery had elevated c1 values at RTS, while athletes with higher symptoms but rapid recovery had reduced c1 at acute injury. This study provides the first evidence for long-term recovery of BOLD scale-free brain dynamics after a concussion.
The midbrain is biomechanically susceptible to force loading from repetitive subconcussive head impacts (RSHI), is a site of tauopathy in chronic traumatic encephalopathy (CTE), and regulates functions (e.g., eye movements) often disrupted in concussion. In a prospective longitudinal design, we demonstrate there are reductions in midbrain white matter integrity due to a single season of collegiate football, and that the amount of reduction in midbrain white matter integrity is related to the amount of rotational acceleration to which players' brains are exposed. We then replicate the observation of reduced midbrain white matter integrity in a retrospective cohort of individuals with frank concussion, and further show that variance in white matter integrity is correlated with levels of serum-based tau, a marker of blood-brain barrier disruption. These findings mean that noninvasive structural MRI of the midbrain is a succinct index of both clinically silent white matter injury as well as frank concussion.
Mild traumatic brain injury (mTBI) presents a substantial burden to patients, families, and health care systems. Whereas, recovery can be expected in the majority of patients, a subset continues to report persisting somatic, cognitive, emotional, and/or behavioral problems, generally referred to as post-concussion syndrome (PCS). However, this term has been the subject of debate since the mechanisms underlying post-concussion symptoms and the role of pre- and post-injury-related factors are still poorly understood. We review current evidence and controversies concerning the use of the terms post-concussion symptoms vs. syndrome, its diagnosis, etiology, prevalence, assessment, and treatment in both adults and children. Prevalence rates of post-concussion symptoms vary between 11 and 82%, depending on diagnostic criteria, population and timing of assessment. Post-concussion symptoms are dependent on complex interactions between somatic, psychological, and social factors. Progress in understanding has been hampered by inconsistent classification and variable assessment procedures. There are substantial limitations in research to date, resulting in gaps in our understanding, leading to uncertainty regarding epidemiology, etiology, prognosis, and treatment. Future directions including the identification of potential mechanisms, new imaging techniques, comprehensive, multidisciplinary assessment and treatment options are discussed. Treatment of post-concussion symptoms is highly variable, and primarily directed at symptom relief, rather than at modifying the underlying pathology. Longitudinal studies applying standardized assessment strategies, diagnoses, and evidence-based interventions are required in adult and pediatric mTBI populations to optimize recovery and reduce the substantial socio-economic burden of post-concussion symptoms.
Concussion is a major health concern, associated with short-term deficits in physical function, emotion and cognition, along with negative long-term health outcomes. However, we remain in the early stages of characterizing MRI markers of concussion, particularly during the first week post-injury when symptoms are most severe. In this study, 52 varsity athletes were scanned using Magnetic Resonance Imaging (MRI), including 26 athletes with acute concussion (scanned 1-7 days post-injury) and 26 matched control athletes. A comprehensive set of functional and structural MRI measures were analyzed, including cerebral blood flow (CBF) and global functional connectivity (Gconn) of grey matter, along with fractional anisotropy (FA) and mean diffusivity (MD) of white matter. An analysis comparing acutely concussed athletes and controls showed limited evidence for reliable mean effects of acute concussion, with only MD showing spatially extensive differences between groups. We subsequently demonstrated that the number of days post-injury explained a significant proportion of inter-subject variability in MRI markers of acutely concussed athletes. Athletes scanned at early acute injury (1-3 days) had elevated CBF and Gconn and reduced FA, but those scanned at late acute injury (5-7 days) had the opposite response. In contrast, MD showed a more complex, spatially-dependent relationship with days post-injury. These novel findings highlight the variability of MRI markers during the acute phase of concussion and the critical importance of considering the acute injury time interval, which has significant implications for studies relating acute MRI data to concussion outcomes.
Developing an accurate and reliable injury predictor is central to the biomechanical studies of traumatic brain injury. State-of-the-art efforts continue to rely on empirical, scalar metrics based on kinematics or model-estimated tissue responses explicitly pre-defined in a specific brain region of interest. They could suffer from loss of information. A single training dataset has also been used to evaluate performance but without cross-validation. In this study, we developed a deep learning approach for concussion classification using implicit features of the entire voxel-wise white matter fiber strains. Using reconstructed American National Football League (NFL) injury cases, leave-one-out cross-validation was employed to objectively compare injury prediction performances against two baseline machine learning classifiers (support vector machine (SVM) and random forest (RF)) and four scalar metrics via univariate logistic regression (Brain Injury Criterion (BrIC), cumulative strain damage measure of the whole brain (CSDM-WB) and the corpus callosum (CSDM-CC), and peak fiber strain in the CC). Feature-based machine learning classifiers including deep learning, SVM, and RF consistently outperformed all scalar injury metrics across all performance categories (e.g., leave-one-out accuracy of 0.828-0.862 vs. 0.690-0.776, and .632+ error of 0.148-0.176 vs. 0.207-0.292). Further, deep learning achieved the best cross-validation accuracy, sensitivity, AUC, and .632+ error. These findings demonstrate the superior performances of deep learning in concussion prediction and suggest its promise for future applications in biomechanical investigations of traumatic brain injury.
Brain injury/concussion is a growing epidemic throughout the world. Although evidence supports association between traumatic brain injury (TBI) and disturbance in brain glucose metabolism, the underlying molecular mechanisms are not well established. Previously, we reported the release of cellular prion protein (PrPc) from the brain to circulation following TBI. The PrPc level was also found to be decreased in insulin-resistant rat brains. In the present study, we investigated the molecular link between PrPc and brain insulin resistance in a single and repeated mild TBI-induced mouse model. Mild TBI was induced in mice by dropping a weight (~95 g at 1 m high) on the right side of the head. The procedure was performed once and thrice (once daily) for single (SI) and repeated induction (RI), respectively. Micro PET/CT imaging revealed that RI mice showed significant reduction in cortical, hippocampal and cerebellum glucose uptake compared to SI and control. Mice that received RI also showed significant motor and cognitive deficits. In co-immunoprecipitation, the interaction between PrPc, flotillin and Cbl-associated protein (CAP) observed in the control mice brains was disrupted by RI. Lipid raft isolation showed decreased levels of PrPc, flotillin and CAP in the RI mice brains. Based on observation, it is clear that PrPc has an interaction with CAP and the dislodgment of PrPc from cell membranes may lead to brain insulin resistance in a mild TBI mouse model. The present study generated a new insight into the pathogenesis of brain injury, which may result in the development of novel therapy.
Mild traumatic brain injury/concussion (mTBI) accounts for 70-90% of all reported TBI cases and causes long-lasting neurological consequences in 10-40% of patients. Recent clinical studies revealed increased blood-brain barrier (BBB) permeability in mTBI patients, which correlated with secondary damage after mTBI. However, the cascade of cellular events initiated by exposure to blood-borne factors resulting in sustained damage is not fully understood. We previously reported that astrocytes respond atypically to mTBI, rapidly losing many proteins essential to their homeostatic function, while classic scar formation does not occur. Here, we tested the hypothesis that mTBI-induced BBB damage causes atypical astrocytes through exposure to blood-borne factors. Using an mTBI mouse model, two-photon imaging, an endothelial cell-specific genetic ablation approach, and serum-free primary astrocyte cultures, we demonstrated that areas with atypical astrocytes coincide with BBB damage and that exposure of astrocytes to plasma proteins is sufficient to initiate loss of astrocyte homeostatic proteins. Although mTBI resulted in frequent impairment of both physical and metabolic BBB properties and leakage of small-sized blood-borne factors, deposition of the coagulation factor fibrinogen or vessel rupture were rare. Surprisingly, even months after mTBI, BBB repair did not occur in areas with atypical astrocytes. Together, these findings implicate that even relatively small BBB disturbances are sustained long term, and render nearby astrocytes dysfunctional, likely at the cost of neuronal health and function.
Pediatric mild traumatic brain injury (TBI) and concussion are a public health challenge with up to 30% of patients experiencing prolonged recovery. Pediatric patients presenting to concussion clinics often have ongoing impairments and may be at increased risk for persistent symptoms. Understanding this population is critical for improved prognostic estimates and optimal treatment.
Soccer is the most popular sport in the world and, since it is a contact sport, players are at risk for head injury, including concussion. Here, we proposed to investigate the association of heading and concussion with macroscopic brain structure among adult amateur soccer players. For this study, 375 amateur soccer players (median age 23 years) completed HeadCount-12m to estimate heading over the 12 months prior to MRI and lifetime concussion. T1-weighted 3D magnetization prepared rapid acquisition gradient echo (MP-RAGE) MRI was performed at 3 Tesla. Parcellation was performed using Freesurfer to extract regional gray and white matter volumes as well as regional cortical thickness and total intracranial volume. Regional cortical brain volumes were normalized by total intracranial volume. We categorized heading into quartiles and concussion as 0, 1 or 2 or more. Generalized linear regressions were used to test the association of heading or concussion with each brain morphometry metric, including age and sex, as covariates. Neither heading nor concussion were associated with reduced brain volume or cortical thickness. We observed that greater heading was associated with greater gray matter volume in the left inferior parietal area, which may reflect effects related to training.
Mild traumatic brain injury (mTBI) represents a significant burden for individuals, economies, and healthcare systems worldwide. Recovery protocols focus on medication and physiotherapy-based interventions. Animal studies have shown that antioxidants, branched-chain amino acids and omega-3 fatty acids may improve neurophysiological outcomes after TBI. However, there appears to be a paucity of nutritional interventions in humans with chronic (≥1 month) symptomology post-mTBI. This systematic literature review aimed to consolidate evidence for nutrition and dietary-related interventions in humans with chronic mTBI. The review was registered with the International Prospective Register of Systematic Reviews (PROSPERO; CRD42021277780) and conducted following the Preferred Reporting for Systematic Reviews and Meta-Analyses (PRISMA) guidelines. Three reviewers searched five databases (PubMed/MEDLINE, Web of Science, SPORTDiscus, CINAHL Complete and Cochrane), which yielded 6164 studies. Nine studies met the inclusion criteria. The main finding was the lack of interventions conducted to date, and a quality assessment of the included studies was found to be fair to good. Due to heterogeneity, a meta-analysis was not feasible. The six nutrition areas identified (omega-3 fatty acids, melatonin, Enzogenol®, MLC901, ketogenic diet and phytocannabinoids) were safe and well-tolerated. It was found that these nutritional interventions may improve cognitive failures, sleep disturbances, anxiety, physical disability, systolic blood pressure volume and sport concussion assessment tool scores following mTBI. Potential areas of improvement identified for future studies included blinding, reporting compliance, and controlling for confounders. In conclusion, further research of higher quality is needed to investigate the role of nutrition in recovery from mTBI to reduce the burden of chronic outcomes following mTBI.
Magnetic resonance imaging (MRI) diffusion studies have shown chronic microstructural tissue abnormalities in athletes with history of concussion, but with inconsistent findings. Concussions with post-traumatic amnesia (PTA) and/or loss of consciousness (LOC) have been connected to greater physiological injury. The novel mean apparent propagator (MAP) MRI is expected to be more sensitive to such tissue injury than the conventional diffusion tensor imaging. This study examined effects of prior concussion severity on microstructure with MAP-MRI. Collegiate-aged athletes (N = 111, 38 females; ≥6 months since most recent concussion, if present) completed semistructured interviews to determine the presence of prior concussion and associated injury characteristics, including PTA and LOC. MAP-MRI metrics (mean non-Gaussian diffusion [NG Mean], return-to-origin probability [RTOP], and mean square displacement [MSD]) were calculated from multi-shell diffusion data, then evaluated for associations with concussion severity through group comparisons in a primary model (athletes with/without prior concussion) and two secondary models (athletes with/without prior concussion with PTA and/or LOC, and athletes with/without prior concussion with LOC only). Bayesian multilevel modeling estimated models in regions of interest (ROI) in white matter and subcortical gray matter, separately. In gray matter, the primary model showed decreased NG Mean and RTOP in the bilateral pallidum and decreased NG Mean in the left putamen with prior concussion. In white matter, lower NG Mean with prior concussion was present in all ROI across all models and was further decreased with LOC. However, only prior concussion with LOC was associated with decreased RTOP and increased MSD across ROI. Exploratory analyses conducted separately in male and female athletes indicate associations in the primary model may differ by sex. Results suggest microstructural measures in gray matter are associated with a general history of concussion, while a severity-dependent association of prior concussion may exist in white matter.
Concussion or mild traumatic brain injury is the most common form of traumatic brain injury with potentially long-term consequences. Current objective diagnosis and treatment options are limited to clinical assessment, cognitive rest, and symptom management, which raises the real danger of concussed patients being released back into activities where subsequent and cumulative injuries may cause disproportionate damages. This study conducted a cross-sectional multi-modal examination investigation of the temporal changes in behavioural and brain changes in a mouse model of concussion using magnetic resonance imaging. Sham and concussed mice were assessed at day 2, day 7, and day 14 post-sham or injury procedures following a single concussion event for motor deficits, psychological symptoms with open field assessment, T2-weighted structural imaging, diffusion tensor imaging (DTI), neurite orientation density dispersion imaging (NODDI), stimulus-evoked and resting-state functional magnetic resonance imaging (fMRI). Overall, a mismatch in the temporal onsets and durations of the behavioural symptoms and structural/functional changes in the brain was seen. Deficits in behaviour persisted until day 7 post-concussion but recovered at day 14 post-concussion. DTI and NODDI changes were most extensive at day 7 and persisted in some regions at day 14 post-concussion. A persistent increase in connectivity was seen at day 2 and day 14 on rsfMRI. Stimulus-invoked fMRI detected increased cortical activation at day 7 and 14 post-concussion. Our results demonstrate the capabilities of advanced MRI in detecting the effects of a single concussive impact in the brain, and highlight a mismatch in the onset and temporal evolution of behaviour, structure, and function after a concussion. These results have significant translational impact in developing methods for the detection of human concussion and the time course of brain recovery.
The American Congress of Rehabilitation Medicine (ACRM) in 2010 called for more head injury research on gender disparities to bridge the gender gap for the short-and long-term effects of TBI, including sexual and reproductive outcomes. In this paper, we review the state of the literature before and after the ACRM announcement, and evaluate how research teams have considered females and mildly injured TBI(mTBI)/concussion groups in post-TBI-related changes in sexual functioning.
When properly implemented and processed, anatomic T 1-weighted magnetic resonance imaging (MRI) can be ideal for the noninvasive quantification of white matter (WM) and gray matter (GM) in the living human brain. Although MRI is more suitable for distinguishing GM from WM than computed tomography (CT), the growing clinical use of the latter technique has renewed interest in head CT segmentation. Such interest is particularly strong in settings where MRI is unavailable, logistically unfeasible or prohibitively expensive. Nevertheless, whereas MRI segmentation is a sophisticated and technically-mature research field, the task of automatically classifying soft brain tissues from CT remains largely unexplored. Furthermore, brain segmentation methods for MRI hold considerable potential for adaptation and application to CT image processing. Here we demonstrate this by combining probabilistic, atlas-based classification with topologically-constrained tissue boundary refinement to delineate WM, GM and cerebrospinal fluid (CSF) from head CT images. The feasibility and utility of this approach are revealed by comparison of MRI-only vs. CT-only segmentations in geriatric concussion victims with both MRI and CT scans. Comparison of the two segmentations yields mean Sørensen-Dice coefficients of 85.5 ± 4.6% (WM), 86.7 ± 5.6% (GM) and 91.3 ± 2.8% (CSF), as well as average Hausdorff distances of 3.76 ± 1.85 mm (WM), 3.43 ± 1.53 mm (GM) and 2.46 ± 1.27 mm (CSF). Bootstrapping results suggest that the segmentation approach is sensitive enough to yield WM, GM and CSF volume estimates within ~5%, ~4%, and ~3% of their MRI-based estimates, respectively. To our knowledge, this is the first 3D segmentation approach for CT to undergo rigorous within-subject comparison with high-resolution MRI. Results suggest that (1) standard-quality CT allows WM/GM/CSF segmentation with reasonable accuracy, and that (2) the task of soft brain tissue classification from CT merits further attention from neuroimaging researchers.
Concussions are one of the most common causes for emergency room use in the United States (US) among youth and adolescents; however, prevalence data on concussion in this population are inconsistent. A growing body of literature has explored associations of a range of variables with pediatric concussion, but they have not been explored simultaneously in a well-powered sample in the US. The present study aimed to present lifetime concussion prevalence, evaluate demographic, psychological, and cognitive correlates of concussion, and assess for differences across these variables based on age of first concussion in a large sample of US children.
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