Mild traumatic brain injury and diffuse axonal injury in swine

Browne, Kevin D.; Chen, Xiao-Han; Meaney, David F.; Smith, Douglas H.

doi:10.1089/neu.2011.1913

Cited by 248Traumatic Brain Injury ResearchTraumatic Brain Injury and Neurovascular DisturbancesAutomotive and Human Injury Biomechanics

Mild traumatic brain injury and diffuse axonal injury in swine

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Browne, Kevin D., Chen, Xiao-Han, Meaney, David F., Smith, Douglas H.·2011·Journal of Neurotrauma

DOI 10.1089/neu.2011.1913PMC PMC3172883

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Abstract

Until recently, mild traumatic brain injury (mTBI) or "concussion" was generally ignored as a major health issue. However, emerging evidence suggests that this injury is by no means mild, considering it induces persisting neurocognitive dysfunction in many individuals. Although little is known about the pathophysiological aspects of mTBI, there is growing opinion that diffuse axonal injury (DAI) may play a key role. To explore this possibility, we adapted a model of head rotational acceleration in swine to produce mTBI by scaling the mechanical loading conditions based on available biomechanical data on concussion thresholds in humans. Using these input parameters, head rotational acceleration was induced in either the axial plane (transverse to the brainstem; n=3), causing a 10- to 35-min loss of consciousness, or coronal plane (circumferential to the brainstem; n=2), which did not produce a sustained loss of consciousness. Seven days following injury, immunohistochemical analyses of the brains revealed that both planes of head rotation induced extensive axonal pathology throughout the white matter, characterized as swollen axonal bulbs or varicosities that were immunoreactive for accumulating neurofilament protein. However, the distribution of the axonal pathology was different between planes of head rotation. In particular, more swollen axonal profiles were observed in the brainstems of animals injured in the axial plane, suggesting an anatomic substrate for prolonged loss of consciousness in mTBI. Overall, these data support DAI as an important pathological feature of mTBI, and demonstrate that surprisingly overt axonal pathology may be present, even in cases without a sustained loss of consciousness.

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Concussion is thought to be a type of DAI because axons may be injured due to stretching.
“As a neuropathological definition, concussion is thought to be a type of DAI because axons may be injured due to stretching (104, 105).”
From Pituitary Dysfunction After Traumatic Brain Injury: A Clinical and Pathophysiological Approach (2015) · cites this paper as [104]
The Discussion describes DAI as an important pathological feature of mild TBI or concussion and says axonal deformation may mechanically damage axons. It does not define concussion itself as a type of DAI; the Discussion cautions that the scope of the DAI designation in mild TBI remains uncertain. (LLM, conf=0.84)
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Large animal models of traumatic brain injury
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Animal models of traumatic brain injury
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The potential for animal models to provide insight into mild traumatic brain injury: Translational challenges and strategies
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A porcine model of traumatic brain injury via head rotational acceleration
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“Recently, we have used these simplified scaling relationships to transfer the rotational accelerations associated with concussion in humans, described in recent studies to be 5600–8000 rad/s [128 – 132], to equivalent rotational motions in the smaller young adult swine brain [114].”
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Sports-Related Concussions in Youth
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A Longitudinal Diffusion Tensor Imaging Study Assessing White Matter Fiber Tracts after Sports-Related Concussion
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Towards clinical management of traumatic brain injury: a review of models and mechanisms from a biomechanical perspective
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Large animal models of stroke and traumatic brain injury as translational tools
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Effect of Docosahexaenoic Acid on a Biomarker of Head Trauma in American Football
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Pre-Clinical Traumatic Brain Injury Common Data Elements: Toward a Common Language Across Laboratories
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Microglia processes associate with diffusely injured axons following mild traumatic brain injury in the micro pig
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Evidence That the Blood Biomarker SNTF Predicts Brain Imaging Changes and Persistent Cognitive Dysfunction in Mild TBI Patients
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The Dynamics of Concussion: Mapping Pathophysiology, Persistence, and Recovery With Causal-Loop Diagramming
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Sex Differences in Anthropometrics and Heading Kinematics Among Division I Soccer Athletes
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Validation of a Helmet-Based System to Measure Head Impact Biomechanics in Ice Hockey
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Reactive gliosis in traumatic brain injury: a comprehensive review
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Default Mode Network in Concussed Individuals in Response to the YMCA Physical Stress Test
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Lateral impacts correlate with falx cerebri displacement and corpus callosum trauma in sports-related concussions
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Human Traumatic Brain Injury Results in Oligodendrocyte Death and Increases the Number of Oligodendrocyte Progenitor Cells
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Traumatic axonal injury (TAI): definitions, pathophysiology and imaging—a narrative review
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Clinical Relevance of Behavior Testing in Animal Models of Traumatic Brain Injury
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The closed-head impact model of engineered rotational acceleration (CHIMERA) as an application for traumatic brain injury pre-clinical research: A status report.
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Measurement of Hybrid III Head Impact Kinematics Using an Accelerometer and Gyroscope System in Ice Hockey Helmets
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Microglia dynamics in adolescent traumatic brain injury
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Longitudinal changes in the DTI measures, anti-GFAP expression and levels of serum inflammatory cytokines following mild traumatic brain injury
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MR Imaging Applications in Mild Traumatic Brain Injury: An Imaging Update
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Mild Traumatic Brain Injury in Translation
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The Immune System's Role in the Consequences of Mild Traumatic Brain Injury (Concussion)
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Concussion Induces Hippocampal Circuitry Disruption in Swine
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Young pigs exhibit differential exploratory behavior during novelty preference tasks in response to age, sex, and delay
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Reaffirmed Limitations of Meta-Analytic Methods in the Study of Mild Traumatic Brain Injury: A Response to Rohling et al.
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A Review of Impact Testing Methods for Headgear in Sports: Considerations for Improved Prevention of Head Injury Through Research and Standards
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On automated model discovery and a universal material subroutine for hyperelastic materials
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Loss of Consciousness Is Related to White Matter Injury in Mild Traumatic Brain Injury
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Large animal models of traumatic brain injury
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Sport and Nonsport Etiologies of Mild Traumatic Brain Injury: Similarities and Differences
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Roadmap for Advancing Pre-Clinical Science in Traumatic Brain Injury
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Impact of traumatic brain injury on sleep structure, electrocorticographic activity and transcriptome in mice
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Investigation of Cross-Species Scaling Methods for Traumatic Brain Injury Using Finite Element Analysis
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A prospective microstructure imaging study in mixed-martial artists using geometric measures and diffusion tensor imaging: methods and findings
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Brain structure alterations and cognitive impairment following repetitive mild head impact: An in vivo MRI and behavioral study in rat
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Neurological Assessment and Its Relationship to CSF Biomarkers in Amateur Boxers
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Brainstem Evoked Potential Indices of Subcortical Auditory Processing After Mild Traumatic Brain Injury
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Imaging in Pediatric Concussion: A Systematic Review
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White Matter Abnormalities and Cognitive Deficit After Mild Traumatic Brain Injury: Comparing DTI, DKI, and NODDI
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Diffusion Tensor Imaging (DTI) Correlates of Self-Reported Sleep Quality and Depression Following Mild Traumatic Brain Injury
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Diffuse Axonal Injury
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Concussion leads to widespread axonal sodium channel loss and disruption of the node of Ranvier
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Rapid and Reversible Development of Axonal Varicosities: A New Form of Neural Plasticity
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A Systematic Review of Structural and Functional Imaging Correlates of Headache or Pain after Mild Traumatic Brain Injury
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A Porcine Model of Peripheral Nerve Injury Enabling Ultra-Long Regenerative Distances: Surgical Approach, Recovery Kinetics, and Clinical Relevance
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Vascular injury is associated with repetitive head impacts and tau pathology in chronic traumatic encephalopathy
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Dynamic Changes in Neural Circuit Topology Following Mild Mechanical Injury In Vitro
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Primary Blast Exposure Increases Hippocampal Vulnerability to Subsequent Exposure: Reducing Long-Term Potentiation
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Novel strain analysis informs about injury susceptibility of the corpus callosum to repeated impacts
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Blue-Light Therapy following Mild Traumatic Brain Injury: Effects on White Matter Water Diffusion in the Brain
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Review of the UBC Porcine Model of Traumatic Spinal Cord Injury
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Challenges and Demand for Modeling Disorders of Consciousness following Traumatic Brain Injury
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Mechanisms of Local Stress Amplification in Axons near the Gray-White Matter Interface
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Understanding microglial responses in large animal models of traumatic brain injury: an underutilized resource for preclinical and translational research
Grovola, M. R., von Reyn, C. R., Loane, D. J., & Cullen, D. K. (2023) · Journal of Neuroinflammation · doi:10.1186/s12974-023-02730-z · Cited by 32 · see citing works

Microglia processes associate with diffusely injured axons following mild traumatic brain injury in the micro pig
Lafrenaye, A. D., Todani, M., Walker, S. A., & Povlishock, J. T. (2015) · Journal of Neuroinflammation · doi:10.1186/s12974-015-0405-6 · Cited by 98 · see citing works
Diffusion Tensor Imaging of the Evolving Response to Mild Traumatic Brain Injury in Rats
Hoogenboom, W. S., Rubin, T. G., Ye, K. Q., Cui, M., Branch, K. C., Liu, J., Branch, C. A., & Lipton, M. L. (2019) · Journal of Experimental Neuroscience · doi:10.1177/1179069519858627 · Cited by 32 · see citing works
Axonal pathology in traumatic brain injury
Johnson, V. E., Stewart, W., & Smith, D. H. (2013) · Experimental Neurology · doi:10.1016/j.expneurol.2012.01.013 · Cited by 1,273 · see citing works
Self-citation
Diverse changes in microglia morphology and axonal pathology during the course of 1 year after mild traumatic brain injury in pigs
Grovola, M. R., Paleologos, N., Brown, D. P., Tran, N., Wofford, K. L., Harris, J. P., Browne, K. D., Shewokis, P. A., Wolf, J. A., Cullen, D. K., et al. (2021) · Brain Pathology · doi:10.1111/bpa.12953 · Cited by 24 · see citing works
Self-citation
Induction of Diffuse Axonal Brain Injury in Rats Based on Rotational Acceleration
Frank, D., Melamed, I., Gruenbaum, B. F., Grinshpun, J., Kuts, R., Shvartsur, R., Azab, A. N., Assadi, M. H., Vinokur, M., & Boyko, M. (2020) · Journal of Visualized Experiments · doi:10.3791/61198 · Cited by 10 · see citing works

Authors: Browne, K. D., Chen, X.-H., Meaney, D. F., & Smith, D. H.
Affiliations: University of Pennsylvania (US)
Center for Brain Injury and Repair, Department of Neurosurgery, University of Pennsylvania, Philadelphia, Pennsylvania.
Corresponding author: Smith, Douglas H.
ORCID: Browne, Kevin D.
Meaney, David F.
Smith, Douglas H.
Venue: Journal of Neurotrauma
Publisher: SAGE Publications
Published: 2011-09
Volume: 28
Issue: 9
Pages: 1747-1755
ISSN: 0897-7151 (ISSN-L)
1557-9042
DOI: 10.1089/neu.2011.1913
PMC: PMC3172883
OpenAlex: W2064707507
Cited by: 248
References: 59
Citations by year: 2026: 6 · 2025: 10 · 2024: 11 · 2023: 20 · 2022: 16 · 2021: 17 · 2020: 19 · 2019: 21 · 2018: 24 · 2017: 20 · 2016: 24 · 2015: 18 · 2014: 14 · 2013: 12 · 2012: 12
FWCI: 9.84
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.liebertpub.com/nv/resources-tools/text-and-data-mining-policy/121/ (tdm)
Locations: Journal of Neurotrauma (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (NS08803, NS‐056202)
National Institute of Neurological Disorders and Stroke (NS-038104, R01NS038104, NS-08803, P01NS056202, NS 056202)
Topics: Health Sciences › Medicine › Epidemiology › Traumatic Brain Injury Research
Health Sciences › Medicine › Neurology › Traumatic Brain Injury and Neurovascular Disturbances
Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Automotive and Human Injury Biomechanics
Keywords: mild traumatic brain injury, concussion, diffuse axonal injury, porcine model, axonal pathology, neurofilaments, white matter, brainstem, loss of consciousness, neurocognitive impairment
MeSH terms: Acceleration, Animals, Brain, Brain Concussion, Rotation, Swine, Unconsciousness, Diffuse Axonal Injury

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Mild traumatic brain injury and diffuse axonal injury in swine

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