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A Porcine Model of Traumatic Brain Injury via Head Rotational Acceleration
Open accessAbstract
Unique from other brain disorders, traumatic brain injury (TBI) generally results from a discrete biomechanical event that induces rapid head movement. The large size and high organization of the human brain makes it particularly vulnerable to traumatic injury from rotational accelerations that can cause dynamic deformation of the brain tissue. Therefore, replicating the injury biomechanics of human TBI in animal models presents a substantial challenge, particularly with regard to addressing brain size and injury parameters. Here we present the historical development and use of a porcine model of head rotational acceleration. By scaling up the rotational forces to account for difference in brain mass between swine and humans, this model has been shown to produce the same tissue deformations and identical neuropathologies found in human TBI. The parameters of scaled rapid angular accelerations applied for the model reproduce inertial forces generated when the human head suddenly accelerates or decelerates in falls, collisions, or blunt impacts. The model uses custom-built linkage assemblies and a powerful linear actuator designed to produce purely impulsive non-impact head rotation in different angular planes at controlled rotational acceleration levels. Through a range of head rotational kinematics, this model can produce functional and neuropathological changes across the spectrum from concussion to severe TBI. Notably, however, the model is very difficult to employ, requiring a highly skilled team for medical management, biomechanics, neurological recovery, and specialized outcome measures including neuromonitoring, neurophysiology, neuroimaging, and neuropathology. Nonetheless, while challenging, this clinically relevant model has proven valuable for identifying mechanisms of acute and progressive neuropathologies as well as for the evaluation of noninvasive diagnostic techniques and potential neuroprotective treatments following TBI.
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“Indeed, the complex neuroanatomy and neurophysiology of the human brain, such as cortical folding, substantial white matter, and specific pathophysiology compared to the rodent brain, may facilitate distinct post-injury neuropathology (137).”
From The Inflammatory Continuum of Traumatic Brain Injury and Alzheimer’s Disease (2018) · cites this paper as [137]
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“To further establish links between macro- and micro-biomechanical features as well as to advance scaling to human injuries, the HYGE device has been used to subject physical models of the skull brain structures to identical loading conditions used to produce specific brain injuries in animals [63, 65, 66, 104, 126].”
Self-citationCullen, D., Vernekar, V. N., & LaPlaca, M. (2011) · Journal of Neurotrauma · doi:10.1089/neu.2011.1841 · Cited by 112 · cited 1×
“Moreover, in closed-head diffuse brain injury, the dominant mode of brain tissue deformation is shear strain, owing to the shear modulus being at least several orders of magnitude lower than the bulk modulus of brain tissue [56, 70, 80, 81].”
Self-citationCerebral Concussion in the Monkey: An Experimental Model
Ommaya, A., Hirsch, A., Flamm, E., & Mahone, R. H. (1966) · Science · doi:10.1126/science.153.3732.211 · Cited by 112 · cited 1×
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Repeated Traumatic Brain Injury Affects Composite Cognitive Function in Piglets
Friess, S. H., Ichord, R., Ralston, J., Ryall, K. A., Helfaer, M. A., Smith, C., & Margulies, S. S. (2009) · Journal of Neurotrauma · doi:10.1089/neu.2008.0845 · Cited by 111 · cited 1×
“Ongoing studies are expanding the use of this model to include novel measurements as well as to translate outcomes utilized in pediatric swine, including behavioral assessment [100, 109, 146], neurophysiological changes [134, 146, 147], and multi-model neuromonitoring [101 – 103, 137].”
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“In this fashion, this model produces pure impulsive non-impact head rotation in different planes at controlled rotational acceleration levels [64, 79, 98, 126] (Fig.”
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Evolution of neurofilament subtype accumulation in axons following diffuse brain injury in the pig.
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“While the lack of positive findings in clinical studies may reflect the complexity and heterogeneity of human TBI and challenges in clinical trial design [28], it may also serve as a cautionary tale of the inability of rodent models to replicate the pathophysiology and neurodegenerative sequelae of clinical TBI [49].”
Self-citationIn vivo imaging of rapid deformation and strain in an animal model of traumatic brain injury.
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A clinical comparison of penetrating and blunt traumatic brain injuries
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Self-citationNeuronal Response to High Rate Shear Deformation Depends on Heterogeneity of the Local Strain Field
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“Ongoing studies are expanding the use of this model to include novel measurements as well as to translate outcomes utilized in pediatric swine, including behavioral assessment [100, 109, 146], neurophysiological changes [134, 146, 147], and multi-model neuromonitoring [101 – 103, 137].”
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“It is a significant challenge to achieve sufficient head rotational acceleration in small rodents to mimic the tissue-level forces without inducing compression effects or rupture of the vasculature, although some have proposed models for this purpose [83, 84].”
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Physiological and Pathological Responses to Head Rotations in Toddler Piglets
Ibrahim, N. G., Ralston, J., Smith, C. M., & Margulies, S. (2010) · Journal of Neurotrauma · doi:10.1089/neu.2009.1212 · Cited by 53
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Self-citationIn situ deformations in the immature brain during rapid rotations.
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“To further establish links between macro- and micro-biomechanical features as well as to advance scaling to human injuries, the HYGE device has been used to subject physical models of the skull brain structures to identical loading conditions used to produce specific brain injuries in animals [63, 65, 66, 104, 126].”
Self-citationFriess, S., Naim, M. Y., Kilbaugh, T., Ralston, J., & Margulies, S. S. (2012) · Laboratory Animals. Journal of the Laboratory Animal Science Association · doi:10.1258/la.2011.011084 · Cited by 25
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Meng, X., Browne, K., Huang, S.-M., Cullen, D. K., Tofighi, M., & Rosen, A. (2012) · doi:10.1049/el.2012.0281 · Cited by 15
Self-citationCarotid Artery Blood Flow Decreases after Rapid Head Rotation in Piglets
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Cited by
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Mechanical disruption of the blood–brain barrier following experimental concussion
Johnson, V. E., Weber, M. T., Xiao, R., Cullen, D. K., Meaney, D. F., Stewart, W. B., Jr., & Smith, D. H. (2018) · Acta Neuropathologica · doi:10.1007/s00401-018-1824-0 · Cited by 163
“The parameters are based on Holbourn’s Scaling Equation [63], where the interaction of brain mass with the level of head rotational acceleration is taken into account [19, 39].”
MethodSelf-citationLarge animal models of traumatic brain injury
Vink, R. (2017) · Journal of Neuroscience Research · doi:10.1002/jnr.24079 · Cited by 150
“With these technical adjustments, the pig inertial acceleration model has been able to produce graded neuropathological and functional changes that are correlated to the severity of injury (Cullen et al., 2016).”
MethodThe Inflammatory Continuum of Traumatic Brain Injury and Alzheimer’s Disease
Kokiko-Cochran, O. N., & Godbout, J. P. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00672 · Cited by 128
“Indeed, the complex neuroanatomy and neurophysiology of the human brain, such as cortical folding, substantial white matter, and specific pathophysiology compared to the rodent brain, may facilitate distinct post-injury neuropathology (137).”
BackgroundLarge animal models of stroke and traumatic brain injury as translational tools
Sorby‐Adams, A., Vink, R., & Turner, R. J. (2018) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00163.2017 · Cited by 108
Mechanosensation in traumatic brain injury
Keating, C. E., & Cullen, D. K. (2020) · Neurobiology of Disease · doi:10.1016/j.nbd.2020.105210 · Cited by 109
“These characteristics allow for pathology to develop in patterns and extents seen in humans (Cullen et al., 2016; McKee et al., 2009; Meaney et al., 1995).”
BackgroundSelf-citation
Metadata
- Authors
- Cullen, D. K., Harris, J. P., Browne, K. D., Wolf, J. A., Duda, J. E., Meaney, D. F., Margulies, S. S., & Smith, D. H.
- Affiliations
- Philadelphia VA Medical Center (US)
- University of Pennsylvania (US)
- Corresponding author
- Cullen, D. Kacy
- ORCID
- Venue
- Methods in Molecular Biology
- Publisher
- Springer New York
- Published
- 2016
- Volume
- 1462
- Pages
- 289-324
- ISSN
- 1064-3745 (ISSN-L)
- 1940-6029
- PMC
- PMC5553045
- OpenAlex
- W2514627507
- Cited by
- 142
- References
- 166
- Citations by year
- 2026: 17 · 2025: 15 · 2024: 15 · 2023: 18 · 2022: 18 · 2021: 11 · 2020: 13 · 2019: 16 · 2018: 11 · 2017: 8
- FWCI
- 72.55
- Type
- book chapter
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Methods in molecular biology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- U.S. Department of Veterans Affairs (IK2 RX001479, I01-RX001097)
- National Institute of Neurological Disorders and Stroke (R01NS038104, R01NS092398, R01NS088176, R01NS050598, R01NS101108, T32NS043126)
- National Institute of Biomedical Imaging and Bioengineering (R01EB021293)
- Topics
- Physical Sciences › Engineering › Biomedical Engineering › Automotive and Human Injury Biomechanics
- Health Sciences › Medicine › Clinical Neurology › Traumatic Brain Injury and Neurovascular Disturbances
- Health Sciences › Medicine › Clinical Neurology › Traumatic Brain Injury Research
- Keywords
- traumatic brain injury, porcine model, angular acceleration, head rotation, brain deformation, injury biomechanics, concussion, linear actuator, neuropathology
- MeSH terms
- Acceleration, Brain Injuries, Traumatic, Animals, Biomechanical Phenomena, Biopsy, Disease Models, Animal, Humans, Immunohistochemistry, Rotation, Swine, Neuroimaging
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