Cited by 236Traumatic Brain Injury and Neurovascular DisturbancesTraumatic Brain Injury ResearchAutomotive and Human Injury Biomechanics

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Pathobiology of traumatically induced axonal injury in animals and man

Povlishock, John T·1993·Annals of Emergency Medicine

DOI 10.1016/s0196-0644(05)82738-6

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Abstract

Study objectives Although diffuse axonal injury is recognized as a consistent feature of traumatic brain injury, there is confusion regarding its pathogenesis. To provide insight into its pathogenesis, animal models of traumatic brain injury complemented by post mortem human analyses were used. Design In animals, anterograde tracers together with antibodies targeting the neurofilament subunits were used in light and electron microscopic analyses of axonal injury. In humans, antibodies to the neurofilament subunits also were used to follow diffuse axonal injury. Animals were followed from minutes to months after injury, whereas humans were studied from six hours to 59 days after injury. Measurements and main results In neither animals nor humans did traumatic brain injury cause direct axonal tearing. Instead, the traumatic brain injury triggered focal intra-axonal change in the 68-kd neurofilament subunit, which became disordered in its alignment and resulted in impaired axoplasmic transport. This caused axonal swelling and disconnection. The sequence of axonal change was similar in animals and man; however, its temporal progression was slower in humans. Conclusion Traumatically induced axonal damage is triggered first by focal intra-axonal change involving the neurofilament subunits. This neurofilament change is due to either direct mechanical failure of the axonal cytoskeleton or the initiation of a biochemical event that causes neurofilament disassembly. In general, the tem…

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Neuronal somatic plasmalemmal permeability and dendritic beading caused by head rotational traumatic brain injury in pigs–An exploratory study
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“Various imaging and post-mortem studies have demonstrated axonal injury in areas of changing tissue density, including this gray to white matter interface in human TBI (Peerless and Rewcastle, 1967; Grady et al., 1993; Povlishock, 1993; Stojanovski et al., 2019).”
Background
Immediate and Medium-term Changes in Cortical and Hippocampal Inhibitory Neuronal Populations after Diffuse TBI
Carron, S. F., Yan, E. B., Allitt, B. J., & Rajan, R. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.07.020 · Cited by 13
Acute-Phase Neurofilament Light and Glial Fibrillary Acidic Proteins in Cerebrospinal Fluid Predict Long-Term Outcome After Severe Traumatic Brain Injury
Andersson, E., Öst, M., Dalla, K., Zetterberg, H., Blennow, K., & Nellgård, B. (2024) · Neurocritical Care · doi:10.1007/s12028-024-01998-0 · Cited by 11
“When neurons are exposed to trauma, intracellular damage leads to axonal swelling and disconnection and the NfL passes into the CSF [5].”
Preliminary Study on Diffuse Axonal Injury by Fourier Transform Infrared Spectroscopy Histopathology Imaging
Yang, T.-T., He, G., Zhang, X., Chang, L., Zhang, H.-D., Ripple, M., Fowler, D., & Li, L. (2014) · Journal of Forensic Sciences · doi:10.1111/1556-4029.12290 · Cited by 11
“metabolic disruption from damage to the internal cytoskeleton proteins and a loss of membrane integrity (4,14,15).”
Background
Lack of Axonal Sprouting of Spared Propriospinal Fibers Caudal to Spinal Contusion Injury Is Attributed to Chronic Axonopathy
Steencken, A. C., Siebert, J., & Stelzner, D. (2009) · Journal of Neurotrauma · doi:10.1089/neu.2009.0934 · Cited by 11
Coma
Young, G. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.04471.x · Cited by 10
Characterisation of Ionic and Lipid Gradients within Corpus Callosum White Matter after Diffuse Traumatic Brain Injury in the Rat.
Hartnell, D., Gillespie-Jones, K. L., Ciornei, C., Hollings, A. L., Thomas, A., Harrild, E., Reinhardt, J., Paterson, D., Alwis, D., Rajan, R., et al. (2019) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.9b00257 · Cited by 9
Diffuse Axonal Injury
Su, E. R., & Bell, M. J. (2015) · Frontiers in neuroscience · doi:10.1201/b18959-4 · Cited by 40
Physical Injury to the Nervous System
Leestma, J. E., & Thibault, K. L. (2014) · CRC Press eBooks · doi:10.1201/b16882-13 · Cited by 4
Characterization of neurite dystrophy after trauma by high speed structured illumination microscopy and lattice light sheet microscopy
Phillips, J. K., Sherman, S. A., Cotton, K. Y., Heddleston, J. M., Taylor, A. B., & Finan, J. D. (2018) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2018.12.005 · Cited by 11
Dynamic correlation of diffusion tensor imaging and neurological function scores in beagles with spinal cord injury
Li, J., Liu, C., Yang, D.-G., Meng, Q.-R., Li, D.-P., Yang, M., Sun, W., Zhang, W., Cai, C., Du, L., et al. (2018) · Neural Regeneration Research · doi:10.4103/1673-5374.232485 · Cited by 9
“As MD changes from lower than normal (acute) to above normal (subacute), a process known as “pseudo-normalization” occurs, demonstrating that the evolution of MD is complicated (Salmond et al., 2006; Rutgers et al., 2008).”
Background
The neurocognitive basis of compromised autonomy after traumatic brain injury: Clinical and ethical considerations
Lux, W. (2007) · Neurotherapeutics · doi:10.1016/j.nurt.2007.04.002 · Cited by 8
Posttraumatic headache: a neurobehavioral disorder.
Saper, J. (2000) · Archives of Neurology · doi:10.1001/archneur.57.12.1776 · Cited by 8
Serum Levels of Neurofilament-H are Elevated in Patients Suffering From Severe Burns
Gatson, J. W., Liu, M.-M., Rivera-Chávez, F. A., Minei, J., & Wolf, S. (2015) · Journal of Burn Care & Research · doi:10.1097/bcr.0000000000000176 · Cited by 7
Big Data, Artificial Intelligence, and Machine Learning in Neurotrauma
Agoston, D. V. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-809556-0.00004-6 · Cited by 7
Longterm Increased S100B Enhances Hippocampal Progenitor Cell Proliferation in a Transgenic Mouse Model
Rodrigues, L., Wartchow, K., Buchfelder, M., Souza, D., Gonçalves, C., & Kleindienst, A. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23179600 · Cited by 6
Neuropsychologists diagnose traumatic brain injury
Wade, J. B., DeMatteo, D. S., & Hart, R. P. (2004) · Brain Injury · doi:10.1080/02699050310001646198 · Cited by 3
Does white matter and vascular injury from repetitive head impacts lead to a novel pattern on T2 FLAIR MRI? A hypothesis proposal and call for research
Miner, A. E., Groh, J. R., Farris, C. W., Hattiangadi, S., Cui, A., Brickman, A. M., Alshikho, M. J., Rabinovici, G. D., Rosen, H. J., Cobigo, Y., et al. (2025) · Alzheimer s & Dementia · doi:10.1002/alz.70085 · Cited by 5
Post-Traumatic Interpeduncular Cistern Hemorrhage as a Marker for Brainstem Lesions
Beretta, L., Anzalone, N., Dell'Acqua, A., Calvi, M., & Gemma, M. (2010) · Journal of Neurotrauma · doi:10.1089/neu.2009.1054 · Cited by 5
“Experimental (Gennarelli et al., 1982; Povlishock, 1993), clinical (Kampf et al., 1998), neuropathological and neuroradiological (Gentry et al., 1988a; Godersky et al., 1990; Parizel et al., 1998; Povlishock, 1992, 1995) evidence suggests that as the intensity of the forces causing DAI increase,…”
Posttraumatic headache--a myth?
Warner, J. (2000) · Archives of Neurology · doi:10.1001/archneur.57.12.1778 · Cited by 5
IgG immunohistochemistry for the assessment of brain injuries in forensic autopsies.
Nogami, M., Takatsu, A., Endo, N., & Ishiyama, I. (1999) · Legal Medicine · doi:10.1016/s1344-6223(99)80016-9 · Cited by 5
Detection of diffuse axonal injury in forensic pathology
Hostiuc, S., Pirici, D., Negoi, I., Ion, D. A., & Ceauşu, M. (2014) · Romanian Journal of Legal Medicine · doi:10.4323/rjlm.2014.145 · Cited by 6
“More recently however, this hypothesis was disputed by various authors who proved that axonal disconnection is a slow progressive process [22-25], primary axotomy being a relatively rare event [26].”
Result
Diminished white matter integrity four decades after traumatic brain injury in Vietnam War veterans
Cummins, T., Xia, Y., Elias, A., Lamb, F., Pannek, K., Doré, V., Bourgeat, P., Salvado, O., Fripp, J., Hopwood, M., et al. (2021) · GLOBAL PSYCHIATRY ARCHIVES · doi:10.52095/gp.2021.8112 · Cited by 4
“Damage occurs due to the straining and shearing of axons, as the head undergoes accelerationdeceleration forces as well as the harming effects of excitatory neurotransmitters released following neural insult (Povlishock, 1993; Santhakumar et al., 2001).”
BackgroundResultInfluential
Mild traumatic brain injury
Alexander, M. P. (1996) · Neurology · doi:10.1212/wnl.46.5.1489 · Cited by 4
Cerebral Blood Flow in Acute Brain Injury
Andrews, P., Souter, M., & Mascia, L. (1997) · doi:10.1007/978-3-662-13450-4_61 · Cited by 4
Neuroimaging and Traumatic Brain Injury
Bigler, E. (1996) · doi:10.1007/978-1-4899-1769-0_10 · Cited by 4
Selected Issues in Forensic Neuropsychology
Goodyear, B., & Umetsu, D. (2002) · Springer eBooks · doi:10.1007/0-306-47923-0_12 · Cited by 3
“This typically takes the form of diffuse axonal injury (DAI), which is hypothesized to result from compression or stretching of axons (Povlishock, 1993), particularly in long white matter tracts or around white and gray matter junctions.”
Background
The Central Fluid Percussion Brain Injury in a Gyrencephalic Pig Brain: Scalable Diffuse Injury and Tissue Viability for Glial Cell Immunolabeling following Long-Term Refrigerated Storage
Pavlichenko, M., & Lafrenaye, A. D. (2023) · Biomedicines · doi:10.3390/biomedicines11061682 · Cited by 2
Bioscience Frontiers in Neuromedical Interventions Following Brain Injury
Ashley, M. J., Weintraub, A. H., & Ripley, D. L. (2010) · CRC Press eBooks · doi:10.1201/9781439849828-c12
Microstructural Alterations of Gray and White Matter in Active Young Boxers with Sports-Related Concussions
Huang, W., Yan, J., Zheng, Y., Wang, J., Hu, W., & Zhang, J. (2024) · Journal of Neurotrauma · doi:10.1089/neu.2024.0015 · Cited by 2
“7 Furthermore, the potential for injury or “ bruising ” in the GM areas of the brain after mild traumatic brain injury (mTBI) is another important factor worth consideration.”
Microglial process convergence onto injured axonal swellings, a human postmortem brain tissue study
Logan-Wesley, A. L., Gorse, K., & Lafrenaye, A. D. (2024) · Scientific Reports · doi:10.1038/s41598-024-71312-7 · Cited by 1
“Microtubules are also impacted by calcium influx following TBI and ultimately lead to a reactive axonal swelling as anterogradely transported proteins and organelles pool at the end of the proximal axon 38–40 .”
A spatially specified systems pharmacology therapy for axonal recovery after injury
Siddiq, M. M., Johnson, N. P., Zorina, Y., Yadaw, A. S., Toro, C. A., Hansen, J., Rabinovich, V., Gregorich, S. M., Xiong, Y., Tolentino, R. E., et al. (2023) · Frontiers in Pharmacology · doi:10.3389/fphar.2023.1225759 · Cited by 3
“Axonal damage is first induced by neurofilament (microtubule) disassembly, and inflammation can lead to apoptosis and inhibit regeneration (Povlishock, 1993; McDonald and Sadowsky, 2002; Sengottuvel et al., 2011).”
Background
Brain Perfusion Imaging (SPECT-Tc-99m HM-PAO) in Diagnosis of Diffuse Axonal Injury
Marks, W., Brockhuis, B., Lass, P., Wieczorek, D., Zapaśnik, A., Lasek, J., & Witkowski, Z. (2006) · doi:10.1097/00013414-200606000-00008 · Cited by 1
“These forces destroy structures in the long axis of the brain, mainly axons and small vessels.(2,4) Lesions are found at the gray-white matter border, rostral brain stem, and corpus callosum.”
Background
Les traumatismes cranio-cérébraux mineurs
Hungerbuhler, J. (2004) · Douleur et Analgésie · doi:10.1007/bf03016188 · Cited by 1

Authors: Povlishock, J. T.
Affiliations: Virginia Commonwealth University (US)
Corresponding author: Povlishock, John T
Venue: Annals of Emergency Medicine
Publisher: Elsevier BV
Published: 1993-06
Volume: 22
Issue: 6
Pages: 980-986
ISSN: 0196-0644 (ISSN-L)
DOI: 10.1016/s0196-0644(05)82738-6
OpenAlex: W1986550170
Cited by: 236
References: 0
Citations by year: 2026: 1 · 2025: 2 · 2024: 4 · 2023: 5 · 2022: 5 · 2019: 5 · 2018: 10 · 2017: 9 · 2016: 6 · 2015: 15 · 2014: 7 · 2013: 4 · 2012: 15
FWCI: 7.52
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Annals of Emergency Medicine (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Clinical Neurology › Traumatic Brain Injury and Neurovascular Disturbances
Health Sciences › Medicine › Clinical Neurology › Traumatic Brain Injury Research
Physical Sciences › Engineering › Biomedical Engineering › Automotive and Human Injury Biomechanics
Keywords: traumatic brain injury, diffuse axonal injury, neurofilament subunits, axonal transport, axonal swellings, axonal cytoskeleton
MeSH terms: Animals, Axons, Brain Injuries, Humans

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Pathobiology of traumatically induced axonal injury in animals and man

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