Localizing Clinical Patterns of Blast Traumatic Brain Injury Through Computational Modeling and Simulation
Abstract
Blast traumatic brain injury is ubiquitous in modern military conflict with significant morbidity and mortality. Yet the mechanism by which blast overpressure waves cause specific intracranial injury in humans remains unclear. Reviewing of both the clinical experience of neurointensivists and neurosurgeons who treated service members exposed to blast have revealed a pattern of injury to cerebral blood vessels, manifested as subarachnoid hemorrhage, pseudoaneurysm, and early diffuse cerebral edema. Additionally, a seminal neuropathologic case series of victims of blast traumatic brain injury (TBI) showed unique astroglial scarring patterns at the following tissue interfaces: subpial glial plate, perivascular, periventricular, and cerebral gray-white interface. The uniting feature of both the clinical and neuropathologic findings in blast TBI is the co-location of injury to material interfaces, be it solid-fluid or solid-solid interface. This motivates the hypothesis that blast TBI is an injury at the intracranial mechanical interfaces. In order to investigate the intracranial interface dynamics, we performed a novel set of computational simulations using a model human head simplified but containing models of gyri, sulci, cerebrospinal fluid (CSF), ventricles, and vasculature with high spatial resolution of the mechanical interfaces. Simulations were performed within a hybrid Eulerian—Lagrangian simulation suite (CTH coupled via Zapotec to Sierramore »
- Authors:
-
- Sandia National Lab. (SNL-NM), Albuquerque, NM (United States)
- Brooke Army Medical Center, Fort Sam Houston, TX (United States)
- Michigan State Univ., East Lansing, MI (United States)
- Brooke Army Medical Center, Fort Sam Houston, TX (United States) ; Michigan State Univ., East Lansing, MI (United States)
- Publication Date:
- Research Org.:
- Sandia National Lab. (SNL-NM), Albuquerque, NM (United States)
- Sponsoring Org.:
- USDOE National Nuclear Security Administration (NNSA)
- OSTI Identifier:
- 1784960
- Report Number(s):
- SAND-2021-5014J
Journal ID: ISSN 1664-2295; 695740
- Grant/Contract Number:
- AC04-94AL85000
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Frontiers in Neurology
- Additional Journal Information:
- Journal Volume: 12; Journal ID: ISSN 1664-2295
- Publisher:
- Frontiers Media S.A.
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Miller, Scott T., Cooper, Candice Frances, Elsbernd, Paul, Kerwin, Joseph, Mejia-Alvarez, Ricardo, and Willis, Adam M. Localizing Clinical Patterns of Blast Traumatic Brain Injury Through Computational Modeling and Simulation. United States: N. p., 2021.
Web. doi:10.3389/fneur.2021.547655.
Miller, Scott T., Cooper, Candice Frances, Elsbernd, Paul, Kerwin, Joseph, Mejia-Alvarez, Ricardo, & Willis, Adam M. Localizing Clinical Patterns of Blast Traumatic Brain Injury Through Computational Modeling and Simulation. United States. https://doi.org/10.3389/fneur.2021.547655
Miller, Scott T., Cooper, Candice Frances, Elsbernd, Paul, Kerwin, Joseph, Mejia-Alvarez, Ricardo, and Willis, Adam M. Thu .
"Localizing Clinical Patterns of Blast Traumatic Brain Injury Through Computational Modeling and Simulation". United States. https://doi.org/10.3389/fneur.2021.547655. https://www.osti.gov/servlets/purl/1784960.
@article{osti_1784960,
title = {Localizing Clinical Patterns of Blast Traumatic Brain Injury Through Computational Modeling and Simulation},
author = {Miller, Scott T. and Cooper, Candice Frances and Elsbernd, Paul and Kerwin, Joseph and Mejia-Alvarez, Ricardo and Willis, Adam M.},
abstractNote = {Blast traumatic brain injury is ubiquitous in modern military conflict with significant morbidity and mortality. Yet the mechanism by which blast overpressure waves cause specific intracranial injury in humans remains unclear. Reviewing of both the clinical experience of neurointensivists and neurosurgeons who treated service members exposed to blast have revealed a pattern of injury to cerebral blood vessels, manifested as subarachnoid hemorrhage, pseudoaneurysm, and early diffuse cerebral edema. Additionally, a seminal neuropathologic case series of victims of blast traumatic brain injury (TBI) showed unique astroglial scarring patterns at the following tissue interfaces: subpial glial plate, perivascular, periventricular, and cerebral gray-white interface. The uniting feature of both the clinical and neuropathologic findings in blast TBI is the co-location of injury to material interfaces, be it solid-fluid or solid-solid interface. This motivates the hypothesis that blast TBI is an injury at the intracranial mechanical interfaces. In order to investigate the intracranial interface dynamics, we performed a novel set of computational simulations using a model human head simplified but containing models of gyri, sulci, cerebrospinal fluid (CSF), ventricles, and vasculature with high spatial resolution of the mechanical interfaces. Simulations were performed within a hybrid Eulerian—Lagrangian simulation suite (CTH coupled via Zapotec to Sierra Mechanics). Because of the large computational meshes, simulations required high performance computing resources. Twenty simulations were performed across multiple exposure scenarios—overpressures of 150, 250, and 500 kPa with 1 ms overpressure durations—for multiple blast exposures (front blast, side blast, and wall blast) across large variations in material model parameters (brain shear properties, skull elastic moduli). All simulations predict fluid cavitation within CSF (where intracerebral vasculature reside) with cavitation occurring deep and diffusely into cerebral sulci. These cavitation events are adjacent to high interface strain rates at the subpial glial plate. Larger overpressure simulations (250 and 500kPa) demonstrated intraventricular cavitation—also associated with adjacent high periventricular strain rates. Additionally, models of embedded intraparenchymal vascular structures—with diameters as small as 0.6 mm—predicted intravascular cavitation with adjacent high perivascular strain rates. The co-location of local maxima of strain rates near several of the regions that appear to be preferentially damaged in blast TBI (vascular structures, subpial glial plate, perivascular regions, and periventricular regions) suggest that intracranial interface dynamics may be important in understanding how blast overpressures leads to intracranial injury.},
doi = {10.3389/fneur.2021.547655},
journal = {Frontiers in Neurology},
number = ,
volume = 12,
place = {United States},
year = {Thu May 20 00:00:00 EDT 2021},
month = {Thu May 20 00:00:00 EDT 2021}
}
Works referenced in this record:
CTH: A Software Family for Multi-Dimensional Shock Physics Analysis
book, January 1995
- Hertel, E. S.; Bell, R. L.; Elrick, M. G.
- Shock Waves @ Marseille I
Measurements of mechanical anisotropy in brain tissue and implications for transversely isotropic material models of white matter
journal, July 2013
- Feng, Yuan; Okamoto, Ruth J.; Namani, Ravi
- Journal of the Mechanical Behavior of Biomedical Materials, Vol. 23
Vascular and Inflammatory Factors in the Pathophysiology of Blast-Induced Brain Injury
journal, March 2015
- Elder, Gregory A.; Gama Sosa, Miguel A.; De Gasperi, Rita
- Frontiers in Neurology, Vol. 6
Effects on Neurons and Hippocampal Slices by Single and Multiple Primary Blast Pressure Waves From Detonating Spherical Cyclotrimethylenetrinitramine (RDX) Explosive Charges
journal, March 2018
- Piehler, Thuvan; Zander, Nicole; Banton, Rohan
- Military Medicine, Vol. 183, Issue suppl_1
Mechanics of blast loading on the head models in the study of traumatic brain injury using experimental and computational approaches
journal, July 2012
- Ganpule, S.; Alai, A.; Plougonven, E.
- Biomechanics and Modeling in Mechanobiology, Vol. 12, Issue 3
When Physics Meets Biology: Low and High-Velocity Penetration, Blunt Impact, and Blast Injuries to the Brain
journal, May 2015
- Young, Leanne; Rule, Gregory T.; Bocchieri, Robert T.
- Frontiers in Neurology, Vol. 6
The evolution of the treatment of traumatic cerebrovascular injury during wartime: A review
journal, May 2010
- Bell, Randy S.; Ecker, Robert D.; Severson, Meryl A.
- Neurosurgical Focus, Vol. 28, Issue 5
Traumatic Brain Injury Hospitalizations of U.S. Army Soldiers Deployed to Afghanistan and Iraq
journal, January 2010
- Wojcik, Barbara E.; Stein, Catherine R.; Bagg, Karen
- American Journal of Preventive Medicine, Vol. 38, Issue 1
Comparison of Toxicity Associated With Early Morning Versus Late Afternoon Radiotherapy in Patients With Head-and-Neck Cancer: A Prospective Randomized Trial of the National Cancer Institute of Canada Clinical Trials Group (HN3)
journal, January 2009
- Bjarnason, Georg A.; MacKenzie, Robert G.; Nabid, Abdenour
- International Journal of Radiation Oncology*Biology*Physics, Vol. 73, Issue 1
Investigation of Cavitation as a Possible Damage Mechanism in Blast-Induced Traumatic Brain Injury
journal, July 2012
- Goeller, Jacques; Wardlaw, Andrew; Treichler, Derrick
- Journal of Neurotrauma, Vol. 29, Issue 10
Experimental Investigation of Cavitation as a Possible Damage Mechanism in Blast-Induced Traumatic Brain Injury in Post-Mortem Human Subject Heads
journal, April 2017
- Salzar, Robert S.; Treichler, Derrick; Wardlaw, Andrew
- Journal of Neurotrauma, Vol. 34, Issue 8
Simulation of Blast-Induced Early-Time Intracranial Wave Physics leading to Traumatic Brain Injury
journal, April 2009
- Taylor, Paul A.; Ford, Corey C.
- Journal of Biomechanical Engineering, Vol. 131, Issue 6
Development of a Finite Element Model for Blast Brain Injury and the Effects of CSF Cavitation
journal, February 2012
- Panzer, Matthew B.; Myers, Barry S.; Capehart, Bruce P.
- Annals of Biomedical Engineering, Vol. 40, Issue 7
Investigation of blast-induced traumatic brain injury
journal, March 2014
- Taylor, Paul A.; Ludwigsen, John S.; Ford, Corey C.
- Brain Injury, Vol. 28, Issue 7
Concussion, microvascular injury, and early tauopathy in young athletes after impact head injury and an impact concussion mouse model
journal, January 2018
- Tagge, Chad A.; Fisher, Andrew M.; Minaeva, Olga V.
- Brain, Vol. 141, Issue 2
Skull Flexure from Blast Waves: A Mechanism for Brain Injury with Implications for Helmet Design
journal, September 2009
- Moss, William C.; King, Michael J.; Blackman, Eric G.
- Physical Review Letters, Vol. 103, Issue 10
A Biomechanical Analysis of the Causes of Traumatic Brain Injury in Infants and Children
journal, January 2004
- Goldsmith, Werner; Plunkett, John
- American Journal of Forensic Medicine & Pathology, Vol. 25, Issue 2
Induction of oxidative and nitrosative damage leads to cerebrovascular inflammation in an animal model of mild traumatic brain injury induced by primary blast
journal, July 2013
- Abdul-Muneer, P. M.; Schuetz, Heather; Wang, Fang
- Free Radical Biology and Medicine, Vol. 60
An animal-to-human scaling law for blast-induced traumatic brain injury risk assessment
journal, September 2014
- Jean, A.; Nyein, M. K.; Zheng, J. Q.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 43
Materials Characterization of Cranial Simulants for Blast-Induced Traumatic Brain Injury
journal, January 2020
- Wermer, Anna; Kerwin, Joseph; Welsh, Kelsea
- Military Medicine, Vol. 185, Issue Supplement_1
Response to Comment on "Chronic Traumatic Encephalopathy in Blast-Exposed Military Veterans and a Blast Neurotrauma Mouse Model"
journal, October 2012
- Goldstein, L. E.; McKee, A. C.
- Science Translational Medicine, Vol. 4, Issue 157
Time-dependent changes of protein biomarker levels in the cerebrospinal fluid after blast traumatic brain injury: Proteomics and 2DE
journal, December 2012
- Ahmed, Farid; Gyorgy, Andrea; Kamnaksh, Alaa
- ELECTROPHORESIS, Vol. 33, Issue 24
Characterisation of interface astroglial scarring in the human brain after blast exposure: a post-mortem case series
journal, August 2016
- Shively, Sharon Baughman; Horkayne-Szakaly, Iren; Jones, Robert V.
- The Lancet Neurology, Vol. 15, Issue 9
Localized Tissue Surrogate Deformation due to Controlled Single Bubble Cavitation
journal, April 2015
- Hong, Y.; Sarntinoranont, M.; Subhash, G.
- Experimental Mechanics, Vol. 56, Issue 1
Strain rate-dependent induction of reactive astrogliosis and cell death in three-dimensional neuronal–astrocytic co-cultures
journal, July 2007
- Cullen, D. Kacy; Simon, Crystal M.; LaPlaca, Michelle C.
- Brain Research, Vol. 1158
The Complexity of Biomechanics Causing Primary Blast-Induced Traumatic Brain Injury: A Review of Potential Mechanisms
journal, October 2015
- Courtney, Amy; Courtney, Michael
- Frontiers in Neurology, Vol. 6
Cavitation nucleation in gelatin: Experiment and mechanism
journal, February 2018
- Kang, Wonmo; Adnan, Ashfaq; O'Shaughnessy, Thomas
- Acta Biomaterialia, Vol. 67
Blast-related traumatic brain injury
journal, September 2013
- Rosenfeld, Jeffrey V.; McFarlane, Alexander C.; Bragge, Peter
- The Lancet Neurology, Vol. 12, Issue 9
Investigation of the elastic modulus, tensile and flexural strength of five skull simulant materials for impact testing of a forensic skin/skull/brain model
journal, April 2017
- Falland-Cheung, Lisa; Waddell, J. Neil; Chun Li, Kai
- Journal of the Mechanical Behavior of Biomedical Materials, Vol. 68
In vitro studies of primary explosive blast loading on neurons: Explosive Blast Loading on Neurons
journal, April 2015
- Zander, Nicole E.; Piehler, Thuvan; Boggs, Mary E.
- Journal of Neuroscience Research, Vol. 93, Issue 9
Death on the battlefield (2001–2011): Implications for the future of combat casualty care
journal, January 2012
- Eastridge, Brian J.; Mabry, Robert L.; Seguin, Peter
- Journal of Trauma and Acute Care Surgery, Vol. 73
Characteristics of an Explosive Blast-Induced Brain Injury in an Experimental Model
journal, November 2011
- de Lanerolle, Nihal C.; Bandak, Faris; Kang, Dewey
- Journal of Neuropathology & Experimental Neurology, Vol. 70, Issue 11
Blast-induced phenotypic switching in cerebral vasospasm
journal, July 2011
- Alford, P. W.; Dabiri, B. E.; Goss, J. A.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 31
Skull Flexure as a Contributing Factor in the Mechanism of Injury in the Rat when Exposed to a Shock Wave
journal, July 2011
- Bolander, Richard; Mathie, Blake; Bir, Cynthia
- Annals of Biomedical Engineering, Vol. 39, Issue 10
Wartime Traumatic Aneurysms
journal, January 2010
- Bell, Randy S.; Vo, Alexander H.; Roberts, Ryan
- Neurosurgery, Vol. 66, Issue 1
Primary Blast Brain Injury Mechanisms: Current Knowledge, Limitations, and Future Directions
journal, January 2018
- Fievisohn, Elizabeth; Bailey, Zachary; Guettler, Allison
- Journal of Biomechanical Engineering, Vol. 140, Issue 2
A New Theory on the Dynamics of Brain Concussion and Brain Injury
journal, September 1958
- Gross, Arthur G.
- Journal of Neurosurgery, Vol. 15, Issue 5
Blast-induced traumatic brain injury: the experience from a level I trauma center in southern Thailand
journal, December 2018
- Tunthanathip, Thara; Khocharoen, Kanutpon; Phuenpathom, Nakornchai
- Neurosurgical Focus, Vol. 45, Issue 6
Wartime Traumatic Cerebral Vasospasm
journal, December 2006
- Armonda, Rocco A.; Bell, Randy S.; Vo, Alexander H.
- Neurosurgery, Vol. 59, Issue 6
Blast Exposure in Rats with Body Shielding Is Characterized Primarily by Diffuse Axonal Injury
journal, June 2011
- Garman, Robert H.; Jenkins, Larry W.; Switzer, Robert C.
- Journal of Neurotrauma, Vol. 28, Issue 6
Influence of high deformation rate, brain region, transverse compression, and specimen size on rat brain shear stress morphology and magnitude
journal, April 2017
- Haslach, Henry W.; Gipple, Jenna M.; Leahy, Lauren N.
- Journal of the Mechanical Behavior of Biomedical Materials, Vol. 68
Primary Blast Exposure Increases Hippocampal Vulnerability to Subsequent Exposure: Reducing Long-Term Potentiation
journal, October 2016
- Effgen, Gwen B.; Ong, Tiffany; Nammalwar, Shruthi
- Journal of Neurotrauma, Vol. 33, Issue 20
Explosive Blast Neurotrauma
journal, June 2009
- Ling, Geoffrey; Bandak, Faris; Armonda, Rocco
- Journal of Neurotrauma, Vol. 26, Issue 6
Neuronal Response to High Rate Shear Deformation Depends on Heterogeneity of the Local Strain Field
journal, September 2006
- Cullen, D. Kacy; LaPlaca, Michelle C.
- Journal of Neurotrauma, Vol. 23, Issue 9
Biomechanical Assessment of Brain Dynamic Responses Due to Blast Pressure Waves
journal, October 2009
- Chafi, M. S.; Karami, G.; Ziejewski, M.
- Annals of Biomedical Engineering, Vol. 38, Issue 2